Mertensiella The Dice snake, Natrix tessellata

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Mertensiella The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species

Editor

Konrad Mebert on behalf of the Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V.

Number 18 Rheinbach, 20 September 2011 I

Supplier: DGHT, Postfach 1421, 53351 Rheinbach, Germany, [email protected] ISSN 0934-6643 ISBN 978-3-9812565-4-3 © 2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde (DGHT) e. V., Rheinbach Production: Andreas Mendt, DGHT-office Print: Druck Center Meckenheim GmbH & Co. KG, D-53340 Meckenheim Homepage: www.dght.de

Photo front cover: A heavily gravid dice snake at its uppermost location at 800 m a.s.l. in the Leventina Valley, Ticino, Switzerland. Photo: Konrad Mebert Photos back cover: Left below – a dice snake (Natrix tessellata) that swallowed a common frog (Rana temporaria) with only its hands still sticking out, Maggia Valley, Ticino, Switzerland. Photo: Konrad Mebert Right above – a dice snake captured a minnow in Lake Cornino, northeastern Italy. Photo: Wolfgang Pölzer Right below – a dice snake passing dripping water, Sava River, Slovenia. Photo: Miha Krofel

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Contents Guicking, Daniela & Ulrich Joger: Molecular Phylogeography of the Dice Snake................................................ 1 Mebert, Konrad: Geographic Variation of Morphological Characters in the Dice Snake (Natrix tessellata).....................................................................................................................................................................11 Brecko, Jonathan, Bart Vervust, Anthony Herrel & Raoul Van Damme: Head Morphology and Diet in the Dice Snake (Natrix tessellata).................................................................................................................. 20 Lenz, Sigrid & Almuth Schmidt: Ergebnisse eines bundesweiten Projektes zur Förderung der Würfelnatter-Populationen und ihrer Lebensräume.......................................................................................................30 Neumann, Christian & Konrad Mebert: Migration Behavior of Endangered Dice Snakes (Natrix tessellata) at the River Nahe, Germany.................................................................................................................39 Trobisch, Dietmar & Andrea Gläßer-Trobisch: The Rearing of Dice Snakes: Part of a Concept for the Sustainable Conservation of Endangered, Isolated Dice Snake Populations in Western Germany.............................................................................................................................................................. 49 Obst, Fritz Jürgen & Peter Strasser: Das sächsische Vorkommen der Würfelnatter im Elbtal bei Meißen................................................................................................................................................................................58 Mebert, Konrad: Introduced and Indigenous Populations of the Dice Snake (Natrix tessellata) in the Central Alps – Microgeographic Variation and Effect of Inbreeding............................................................... 71 Mazza, Gaëtan, Jean-Claude Monney & Sylvain Ursenbacher: Structural Habitat Partitioning of Natrix tessellata and Natrix maura at Lake Geneva, Switzerland.................................................... 80 Metzger, César, Philippe Christe & Sylvain Ursenbacher: Diet Variability of Two Convergent Natricine Colubrids in an Invasive-Native Interaction............................................................................ 86 Mebert, Konrad: Sexual Dimorphism in the Dice Snake (Natrix tessellata) from the Central Alps.................. 94 Conelli, Alberto, E., Marco Nembrini & Konrad Mebert: Different Habitat Use of Dice Snakes (Natrix tessellata) among Three Populations in Canton Ticino, Switzerland – a Radiotelemetry Study....................................................................................................................................................100 Mebert, Konrad, Alberto E. Conelli, Marco Nembrini & Benedikt R. Schmidt: Monitoring and Assessment of the Distribution of the Dice Snake in Ticino, Southern Switzerland.......................................117 Scali, Stefano: Ecological Comparison of the Dice Snake (Natrix tessellata) and the Viperine Snake (Natrix maura) in Northern Italy............................................................................................................................131 Mebert, Konrad & Wolfgang Pölzer: Fatal Hunting Accidents: Killing of Dice Snakes (Natrix tessellata) by Bullheads (Cottus gobio)............................................................................................................... 145 Capula, Massimo, Ernesto Filippi, Lorenzo Rugiero & Luca Luiselli: Dietary, Thermal and Reproductive Ecology of Natrix tessellata in Central Italy: A Synthesis................................................................... 147 Mebert, Konrad, Benny Trapp, Andrea Dall’Asta, Petr Velenský & Wolfgang Böhme: Hybrids between Natrix tessellata and N. natrix/maura.............................................................................................154 Velenský, Mikuláš, Petr Velenský & Konrad Mebert: Ecology and Ethology of Dice Snakes (Natrix tessellata) in the City District Troja, Prague..................................................................................................... 157 Vlček, Petr, Vít Zavadil, Daniel Jablonski & Konrad Mebert: Dice Snake (Natrix tessellata) in the Baltic Sea Drainage Basin (Karvinsko District in Silesia, Czech Republic).................................................. 177 III

Kammel, Werner & Konrad Mebert: Effects of Rehabilitation of the Polluted River System Mur in Styria in Austria and Construction of Hydroelectric Power Plants on Fish Fauna and Distribution of the Dice Snake........................................................................................................................................... 188 Smole-Wiener, Anna Karina: Verbreitung, Habitatnutzung und Gefährdung der Würfelnatter (Natrix tessellata) in Kärnten, Österreich........................................................................................................................ 197 Žagar, Anamarija, Miha Krofel, Marijan Govedič & Konrad Mebert: Distribution and Habitat Use of Dice Snakes (Natrix tessellata) in Slovenia.......................................................................................... 207 Jelić, Dušan & Suvad Lelo: Distribution and Status Quo of Natrix tessellata in Croatia, and Bosnia and Herzegovina...................................................................................................................................................... 217 Janev Hutinec, Biljana & Konrad Mebert: Ecological Partitioning between Dice Snakes (Natrix tessellata) and Grass Snakes (Natrix natrix) in Southern Croatia................................................................225 Mebert, Konrad, Trapp, Benny, Guido Kreiner, Herbert Billing, Jeroen Speybroeck & Maya Henggeler: Nocturnal Activity of Natrix tessellata, a Neglected Aspect of its Behavioral Repetoire................234 Carlsson, Martin, Simon Kärvemo, Marian Tudor, Michal Sloboda, Andrei D. Mihalca, Ioan Ghira, Lucia Bel & David Modrý: Monitoring a Large Population of Dice Snakes at Lake Sinoe in Dobrogea, Romania.............................................................................................................................................. 237 Kärvemo, Simon, Martin Carlsson, Marian Tudor, Michal Sloboda, Andrei D. Mihalca, Ioan Ghira, Lucia Bel & David Modrý: Gender Differences in Seasonal Movement of Dice Snakes in Histria, Southeastern Romania........................................................................................................................245 Mihalca, Anrei Daniel: Parasitism in the Dice Snake (Natrix tessellata) – a Literature Review..................... 255 Strugariu, Alexandru, Iulian Gherghel, Ioan Ghira, Severus D. Covaciu-Marcov & Konrad Mebert: Distribution, Habitat Preferences and Conservation of the Dice Snake (Natrix tessellata) in Romania............................................................................................................................................272 Naumov, Borislav, Nikolay Tzankov, Georgi Popgeorgiev, Andrei Stojanov & Yurii Kornilev: The Dice Snake (Natrix tessellata) in Bulgaria: Distribution and Morphology.......................................................288 Sterijovski, Bogoljub, Rastko Ajtić, Ljiljana Tomović, Sonja Djordjević, Marko Djurakić, Ana Golubović, Jelka Crnobrnja-Isailović, Jean-Marie Ballouard, Fifi Groumpf & Xavier Bonnet: Natrix tessellata on Golem Grad, FYR of Macedonia: A Natural Fortress Shelters a Prosperous Snake Population.............................................................................................................................................298 Ioannidis, Yannis & Konrad Mebert: Habitat Preferences of Natrix tessellata at Strofylia, Northwestern Peloponnese, and Comparison to Syntopic N. natrix....................................................................... 302 Kotenko, Tatiana I., Shaitan, S.V., Starkov, V.G. & O. I. Zinenko: The Northern Range Limit of the Dice Snake (Natrix tessellata) in Ukraine and the Don River Basin in Russia...............................................311 Bakiev, Andrey, Alexander Kirillov & Konrad Mebert: Diet and Parasitic Helminths of Dice Snakes from the Volga Basin, Russia................................................................................................................................ 325 Litvinov, Nikolay, Andrey Bakiev & Konrad Mebert: Thermobiology and Microclimate of the Dice Snake at its Northern Range Limit in Russia.........................................................................................................330 Ratnikov, Viatcheslav Yu. & Konrad Mebert: Fossil Remains of Natrix tesselllata from the Late Cenozoic Deposits of the East European Plain............................................................................................................... 337 Tuniyev, Boris, Sako Tuniyev, Tom Kirschey & Konrad Mebert: Notes on the Dice Snake (Natrix tessellata) from the Caucasian Isthmus............................................................................................................................343

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Frotzler, Norbert, Nino Davitashvili, Konrad Mebert: Distribution of the Dice Snake (Natrix tessellata) in Georgia (Transcaucasia) and Comparative Notes on the Genus Natrix.............................. 357 Göçmen, Bayram, Kerim Çiçek, Mehmet Z. Yildiz, Mehmet K. Atatür, Yunus E. Dinçaslan & Konrad Mebert: A Preliminary Study on the Feeding Biology of the Dice Snake (Natrix tessellata) in Turkey................................................................................................................................................365 Dínçaslan, Yunus E., Hüseyín Arikan, Ísmaíl Hakki Uğurtaş & Konrad Mebert: Morphology and Blood Proteins of Dice Snakes from Western Turkey............................................................................................370 Göçmen, Bayram & Konrad Mebert: The Rediscovery of Natrix tessellata on Cyprus....................................... 383 Shehab, Adwan H., Aroub Al Masri & Zuhair S. Amr: The Dice Snake (Natrix tessellata) in Syria: Distribution, Trade and Conservation.............................................................................................................................388 Amr, Zuhair S., Konrad Mebert, Nashat Hamidan, Mohammad Abu Baker & Ahmad Disi: Ecology and Conservation of the Dice Snake (Natrix tessellata) in Jordan.............................................................. 393 Baha El Din, Sherif: Distribution and Recent Range Extension of Natrix tessellata in Egypt...........................401 Ahmadzadeh, Faraham, Konrad Mebert, Saeedeh Ataei, Elham Rezazadeh, Leili Allah Goli & Wolfgang Böhme: Ecological and Biological Comparison of Three Populations of Dice Snakes (Natrix tessellata) from the Southern Caspian Sea Coast, Iran...................................................................................403 Rajabizadeh, Mehdi, Soheila Javanmardi, Nasrullah Rastegar-Pouyani, Rasoul Karamiani, Masoud Yusefi, Hasan Salehi, Ulrich Joger, Konrad Mebert, Hamidreza Esmaeili, Hossein Parsa, haji Gholi Kami & Eskandar Rastegar-Pouyani: Geographic Variation, Distribution, and Habitat of Natrix tessellata in Iran...................................................................................................414 Liu, Yang, Konrad Mebert & Lei Shi: Notes on Distribution and Morphology of the Dice Snake (Natrix tessellata) in China................................................................................................................................................ 430

Photo Notes Mebert, Konrad & Thomas Ott: Mating Aggregations in Natrix tessellata...........................................................437 Trapp, Benny & Konrad Mebert: Upward Position of Eyes and Nostrils of the Dice Snake for Breaking the Water Surface?.............................................................................................................................................. 440 Mebert, Konrad & Maya Henggeler: Unique Albino of Dice Snakes (Natrix tessellata)?.................................441 Cafuta, Vesna: First Report of Melanistic Dice Snakes (Natrix tessellata) in Slovenia....................................... 442 Mebert, Konrad & Benny Trapp: Luring a Dice Snake by Wave Action in the Water – a Predatory Response to a Moving Aquatic Prey?.......................................................................................................445 Velikov, Ilian: Dice Snake Feeds on Spiny Invasive Fish............................................................................................ 447 Mebert, Konrad: Unsuitable Food for Dice Snakes (Natrix tessellata)!.................................................................. 448 Jelić, Dušan: Record of Natrix tessellata as a Prey of Hierophis gemonensis.......................................................... 450 Jelić, Dušan: The Gull Larus cachinnans (Pallas, 1811) as Natural Predator of Natrix tessellata (Laurenti, 1768).................................................................................................................................................................. 451 Mebert, Konrad: Terrestrial Dice Snakes: How far from Water a Semiaquatic Snakes Ventures Out?.............453

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Film Egerer, Eric & Konrad Mebert: Dice Snake, the Shy Water Beauty.....................................................456 and DVD

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Preface

about the dice snake, N. tessellata. For two years, I resisted these requests, as I feared an excessive amount of private work and insufficient voluntary authors to contribute articles. Indeed, I was aware of only little contemporary research on Natrix tessellata at that time. Yet, I knew, from my personal research with this species, I had folders and drawers full with data that awaited its publication for more than a decade. After renewed requests by the DGHT, I conceded some interest. But as mentioned above, my fear about the comprehensiveness and work load such a project requires was justified. It maybe comes at no surprise that during the four years of producing this volume at least 16 children were born to authors in this Mertensiella. Darwin wishes them all a happy welcome.

Had I known, what it takes to produce and edit such a voluminous compendium about a single reptile species, I would probably never put myself on this strenuous path. With more than 3000 hours of my personal time, and not counting those of other participants, the task was monumental. The result speaks for itself with a total of 57 articles and one DVD, involving more than 122 co-/authors, with contributions from more than 22 countries, while touching 14 additional countries in summary articles. To elucidate the production of such a cross-border endeavour and for reasons of my personal laborious involvement into compiling this book, I opted to incorporate also personal accounts into the evolution of this Mertensiella volume 18, besides the usual aspects of history, content, and format. The Beginning From 2005 on I was asked several times by a representative of the German Herpetological Society DGHT (Deutsche Gesellschaft für Herpetologie und Terrarienkunde) whether I would head the production and edit a Mertensiella volume (a book series with each volume loosely treating a particular herpetological topic)

It was not until late 2007, that I seriously considered this editorial task. Weeks before the annual DGHT meeting in October in Hallein, Austria, I briefly did a search to see, whether there are sufficient potential contributions for such a volume, setting the goal to incorporate at least 20 articles. To my surprise, this goal was quickly achieved up to the meeting and I subsequently agreed to proceed with this project. To my second surprise, the number of contributions has tripled half a year later, accumulating to more than 100 co-authors on the mailing list. Since the amount of potential contributions exceeded my initial expectations by far, I asked to partition the articles into two volumes for a speedier release of a first volume. Even though, that idea did not materialize, and hence, required the increased amount of time for the release of the now single volume, the waiting for this Mertensiella about the dice snake was hopefully worth the patience. It is not a full monography, as some important aspects such as experimental behavioral studies or inner anatomy are missing [for interesting articles about morphological aspects see the histological investigation about the venom apparatus in the dice snake (Gygax 1968, 1971) and the skin sensory organs by Walztöhny & Ziswiler (1979)]. However, this volume represents the status quo of knowledge about this versatile, semi-aquatic snake species. It was in the early 1990s, when I first worked with the dice snake, researching morphological aspects for my Master thesis at the University of Zürich, Switzerland (Mebert 1993, and related articles on pages 11, 71, and 94. A couple of years later, M. Gruschwitz, S. Lenz, V. Lanka and me produced a large contribution (> 60 pages, Gruschwitz et al. 1999) about the dice snake in the Handbuch series by W. Böhme. In this monographic review, it was my personal goal to incorporate all available literature about the dice snake, even translating it VII

from different languages. Although I did not get access to all pertinent references, in particular missing various articles from the period and geography referring to the former Soviet Union, the text was and remained up to this Mertensiella the most comprehensive about N. tessellata. Already during the 90s, I wondered, why a snake species with such an extensive Palaearctic distribution and locally high abundance didn’t receive more attention. Indeed, the dice snake is one of the few snake species that naturally occurs on three continents, including Europe, Asia, and Africa. In latter case, it ranges at least for a few hundred kilometers into Egypt (Baha El Din p. 401), but possibly being in the process of expanding farther south along the Nile River towards Sudan. The others snake species sharing the three-continent distribution are N. natrix, Malpolon (insignitus) monspessulanus, Macroprotodon cucullatus, and Eryx jaculus. The reasons for the lack of attention to N. tessellata in most of the last century probably relates to its missing in countries of Western and Middle Europe with a long tradition of natural science, in particular France, Great Britain, the Benelux countries, and Scandinavia, where instead the grass snake, N. natrix, and the adder, Vipera berus, are/were common species and easy to study. The distribution of the dice snake in Austria, Germany and Switzerland, other countries with a long history of natural science, is relatively reduced with only peripheral or a few small, isolated populations, whereas in Italy, yet another country with a great herpetological emphasis, the ecological research on dice snake occurred only in the last decade of the 20th Century with studies concentrated around L. Luiselli (see p. 147 for a review by Capula et al.). But I presume that this lack is not going to persist. Then, with the fall of the Iron Curtain, Eastern and Western European countries increasingly promote exchange and homogenization of intercultural and scientific affairs, a trend affecting also like-minded herpetologists. As a consequence, I expect a higher rate of studies and publications about the dice snake in the future to come. Already the large scale research by international teams at Histria, Romania (Carlsson et al. p. 237, Kärvemo et al. p. 245), and Golem Grad, FYR Macedonia (Sterijovski et al. p. 298), are signs of this “spring” in international research collaborations.

diaeval towns and lowland riparian lands in Germany, Austria, and Czech Republic, south to steep mountain river valleys in the Swiss and Italian Alps, to the ancient Colosseum in Rome and the Acropolis in Athens, the pyramids of Giza in Egypt, the ancient cities and ruins of Ephesos, Petra, Palmyra, and Persepolis in Turkey, Jordan, Syria, and Iran, respectively, to the rivers in the steppes of Russia, Ukraine, and Kazakhstan, to the Basra Swamps in Iraq, to coastal areas of the Mediterranean, Black, and Caspian seas, to valleys and plateaus in mountains of the Caucasus, the Hindu Kush and Pamir in Afghanistan, and it expanded as far east in Asia as to experience oriental influences in north-western China, even inhabiting the fringes around the Tarim desert. A second goal was to edit and format the articles to become “easy” to read, so they could be understood globally by most interested in biology and reptiles. Hence, English became the preferred text language due to its international access and ease to understand. Consequently, I helped in the compilation of English written articles, where this became suitable. Only three articles were left in the German language, a concession to the predominantly German membership of the DGHT that supported this project. Editorial and Review Process, Co-authorships

Goals

Besides writing in English, which is a foreign language for most authors in this volume, there were several problems that arose from an international and “intercultural” project of this scope. For example, many valuable references are written in languages “foreign” to the respective authors, including German, containing many relevant publications (historic and recent) about the dice snake. Furthermore, many “older” articles are difficult to access in remote libraries or are chapters in a book, that is expensive or not on the market anymore. To reduce that problem, I acquired the permission from the “Aula Verlag” (publishing house) to disseminate the monographic chapter about N. tessellata from the “Handbuch der Reptilien und Amphibien Europas” (Gruschwitz et al. 1999). Even though the Handbuchtext is in German, free translation programs are available online, and so the text could serve as a relevant tool to compare the information in each contribution with already existing ones.

The principal goal for this Mertensiella about N. tessellata evolved from originally containing a collection of articles about the dice snake with a focus on middle Europe to finally representing the status quo of knowledge of this species across its huge range. In accordance with its large distribution, there is probably no other snake species that lives in the neighborhood of so many diverse landscapes and influential historic societies at the same time. For example, it occurs in the sight of me-

Possibly due to great heterogeneity of subject-related knowledge, insufficient time for a volume without impact factor, and variable English skills among authors and reviewers, the review process itself quickly became unsatisfactory. Nontheless, my desire was to homogenize the texts into “legible” English and to have incorporated up-to-date literature related to the dice snake and various topics in the volume. These aspiring goals resulted in my frequent involvment as a principal re-

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viewer, as I could benefit from a particularly large collection and readings on related literature accumulated over two decades in this field, and from decent English skills (after having spent 9 years in the USA) and analytical writing. Even though, there were some discussions about the required quality, scope, and comprehensiveness of the articles, in which not all authors agreed to my challenging propositions, I finally had to stand behind this volume. Hence, I asked everyone to invest their time to get the best out of their contributions, in terms of content, English, structure, quality of illustrations, and sound interpretation of their results. I regarded it as very important, that texts are sound and generally understandable, that the messages in images and graphs are evident. One should be able to follow the information without having to consult technical books, dictionaries, or detailed maps. Consequently, a number of authors preferred that I get involved directly as a co-author to incorporate pertinent information from my own data on more than 1000 specimens of this species and from my studies on related American Natricines (Mebert 2010), to complement missing geographic data, rework graphs, utilize my literature collection, and finally to reword and structure many parts in the texts. Ultimately, the comprehensive effort and work devoted to the co-authored articles, in addition to the countless hours put into the other articles, has required an extraordinary use of private time over four years, but ultimately has added in harmonizing at least partially among the extremely heterogeneous forms of the originally submitted articles. As a result, I hope the information put together in this Mertensiella is satisfactory to a large potential readership. As this volume should represent the status quo of knowledge on N. tessellata, we rather worked hard to include as many articles as possible than just to reject them. Hence, based on an early list of putative contributions, only three submissions were reviewed/rejected and never made it into a revised version, including articles from Albania, Russia, and Moldova. Three other articles went through the first review process, but were finally withdrawn by the authors for various reasons, including articles from Romania, Israel, and Armenia. Another 15–20 potential articles were initially suggested, but ultimately were never submitted in a written form, including suggested titles from Slovakia, Lebanon, Greece, Iran, Kazakhstan, Hungary, Romania, Serbia, Montenegro, Austria, and the Czech Republic. All these putative articles may still be published sometime in the future in other books or journals. Besides the initial three, more global articles, the content is structured in a geographic mode, as the sequence of the principal articles roughly follows in a north-to-south direction, beginnig with articles in the West (central Europe) and ending in the East (China). The prinicpal articles are followed by the short Photo Notes and a brief introductory text to the DVD.

Format We formatted most of the articles to be independent from other articles in this volume, so they could be distributed electronically as PDFs, respectively as “standalone” papers. Consequently, cross referencing to other articles in this Mertensiella was not indicated as “this volume” in the literature list, but was noted as in a regular journal by using author names and year in the text, and the full citation format in the literature list. For similar reasons, we left some general, repetitive information among the articles. I decided also to focus on content and sound explanation of issues in the articles, and be relatively tolerant on inconsistencies in grammar and formats within and among articles. For example, it would take an excessive and inappropriate amount of time to research and harmonize all the language-related different naming of persons and locations, as well as corresponding rules that originate from such a multitude of cultures as can be found in this Mertensiella. With “Photo Notes” a new style of articles was incorporated. These short articles use photographs concerning various aspects of N. tessellata followed by a brief text (kind of an extended legend). Such a document contains one picture or a set of pictures, rendering information and observations that do not normally find entry into a standard article, but are considered worthy to be published. With this volume of the Mertensiella series, a change of its physical size from a smaller format to a DIN A4 format was selected for a number of reasons. First, the Mertensiella series is a supplement to the “Salamandra”, the herpetological science-journal of the DGHT published in English with an international focus. This and the “Elaphe”, the society’s internal and German-written journal, are published in DIN A4 format. Hence, the new Mertensiella format is in line with the other principal publications of the DGHT. Second, the A4 format allows for more flexibility and larger figures. And third, it reduces the thickness (page number) of an already large volume. Content Several contributions reflect rudimentary studies in terms of methods, temporal duration and number of individual snakes included. Some studies have been executed as “short” projects, ill-financed and without direct academic support. Some projects were financed by local authorities. They may lack long-term data or do not represent a multi-year investigation, as is often desired for a comprehensive understanding on a species- or population-level. Consequently, there are fewer conclusions that can be drawn. However, the overall data gathered still merit their publication, as the sum of smaller studies may still lead to a larger understanding. The articles IX

may also serve as a platform or stepping stone for subsequent studies. The contents in this Mertensiella are very variable. A few contributions deal with the genetic and morphological variation across large areas of its vast distribution, e.g. phylogeography by Guicking & Joger (p. 1), or geographic variation and sexual dimorphism of external morphological characters by Mebert (p. 11, p. 94). That significant morphological geographic variation exists across even relatively short distances of 40 to 100 km and can help to identify the origin of introduced dice snakes was exemplified by Mebert (p. 71). Furthermore, he elaborates the high frequency of scale abnormalities in introduced dice snakes, and relates deformed ventral scales to fused vertebrae. This and the occurrence of exceptionally short (in body segments) dice snakes is viewed in the context of inbreeding in introduced populations, as the few specimens that started the population constituted a severe bottleneck. Brecko et al. (p. 20) found significantly narrower and more streamlined heads in dice snakes from populations that consumed fish than in dice snakes those with frogs in their stomachs, suggesting a phenotypically plastic response to the local abundance of prey types. Some basic articles provide first or updated national accounts on the geographic distribution, conservation status, and observations on habitat and other ecological aspects of N. tessellata, e.g. for Croatia (Jelić & Lelo p. 217), Romania (Strugariu et al. p. 272), Egypt (Baha el Din p. 401), Jordan (Amr et al. p. 393), and with the inclusion of some morphological data also for Bulgaria (Naumov et al. p. 288), Iran (Rajabizadeh et al. p. 414), and China (Liu et al. p. 430). Other articles deal with similar topics on a more regional level, e.g. Dínçaslan et al. (p. 370), for western Turkey, who included also information on geographic variation of blood serum proteins, Ahmadzadeh et al. (p. 403) for the south-eastern coast of the Caspian Sea in Iran, including also data on reproduction and population characteristics, and Smole–Wiener (p. 197), and Kammel & Mebert (p. 188), for Carinthia and Styria in southern Austria, respectively. Latter contribution also reports on the recolonization by the dice snake after a larger river rehabilitation program and looks at the effects of hydroelectric power plants. Tuniyev et al. (p. 343) present new and old distribution data, and accounts on color pattern, sympatric herpetofauna, activity and conservation of dice snakes along the Caucasus isthmus, except for most of Georgia, which is covered by Frotzler et al. (p. 357). Latter updated the geographic distribution of the dice snake in Georgia and compared its habitat with the sympatric grass snake. Some authors report or include information on recently detected, new peripheral populations and surprising rediscoveries of dice snakes, such as the 500 km range extension across the Tarim desert in China (Liu et al. p. 430), first populations of the Baltic Sea Drainage Basin (Vlček et al. p. 177), redisX

coveries on the island of Cyprus (Göçmen & Mebert p. 383), and within the capital of Romania, Bucharest (Strugariu et al. p. 272). In Germany, Lenz & Schmidt (p. 30) summarized the results of an extensive, nationwide project to support the few remaining populations of dice snakes with various practical measures of habitat improvement. One of the measures included the rearing and subsequent release of dice snakes to support the population of the Lahn River with juveniles about which Trobisch & Gläßer-Trobisch report (p. 49). The most northern population in Germany is the focus of a historical account and assessment of its problematic conservation status (Obst & Strasser p. 58). A summary about the fossil data of N. tessellata from the East European Plain is given by Ratnikov & Mebert (p. 337). The oldest fossil records of N. tessellata originate from the Middle Pliocene and suggest a continuous presence since that period, but its range limits varied with frequent climatic and topographic fluctuations. Covering part of that same region, Kotenko et al. (p. 311) investigated the current northern range limit of N. tessellata and a few environmental correlates in more details for Ukraine and the Don River Basin in Russia. Farther east in the Samara region, Russia, Litvinov et al. (p. 330) investigated the most northern population confirmed for N. tessellata, situated along the Volga River. They also measured various body and ambient temperatures and experimentally tested the temperature optimum for dice snakes. Similarly, Scali (p. 131) compared temperature and other ecological variables between N. tessellata and its congeneric competitor, the viperine snake N. maura, at one of their few sites of natural sympatry in northern Italy. Differences were found in microhabitat selection and temporal activity, as the dice snake was observed in comparatively deeper streams, being more piscivorous, and less nocturnal. These two species were also compared at a site in Switzerland, where N. maura occurs autochthonous and N. tessellata was introduced many decades ago. Compared with the viperine snake, N. tessellata occupied shore zones that were relatively more open and inhabited more often steep slopes. Metzger et al. (p. 86) found a large overlap in the trophic niche between both species at the same site, regarding seasonal preferences and prey types. In this case, the introduction of the larger N. tessellata and the subsequent trophic competition probably is the principal cause for the decline in the native N. maura population over the last two decades. Information on other interspecific differences with the grass snake N. natrix regarding feeding/foraging, as well as aquatic and terrestrial habitat use, are presented through studies in Croatia (Janev Hutinec & Mebert p. 225), Greece (Ioannidis & Mebert p. 302), and marginally also for Georgia (Frotzler et al. p. 357), Italy (Capula et al. p. 147), and Iran (Ahmadzadeh et al. p. 403). The Greek study also looks at the pattern of hiber-

nation, terrestrial activity and the high road mortality of more than 1000 N. tessellata annually on a 2 km shore road of the study site. Line transect methods were applied to compare utilized with non-utilized habitats by dice snakes in Slovenia (Zagar et al. p. 207), whereas Mebert et al. (p. 117) calculated detection probability and site occupancy to assess the conservation status of dice snakes in Ticino, representing the principal autochthonous distribution in Switzerland. Both studies show that dice snakes can find appropriate habitat to maintain healthy populations in even intensively cultivated and anthropogenic modified landscapes, as long as a narrow belt of suitable structure along water bodies and sufficient prey persists. Most snake species are usually rather secretive and difficult to sample in sound numbers for population level studies. Therefore, the unusually high density in some populations of the dice snake renders this species as an extremely valuable representative of snakes to be utilized for scientific purposes of this species and to foster greater understanding for the biology of snakes in general. In this context, long term studies in central Italy (Capula et al. p. 147), and more recently, large scale studies initiated in coastal Romania (Carlsson et al. p. 237, Kärvemo et al. p. 245) and on an island in Prespa Lake, FYR of Macedonia (Sterijovski et al. p. 298), have been (or will be) compiling a multitude of relevant data on the natural history of N. tessellata. Studied aspects included dietary habits, thermal ecology, reproduction, various behavioral aspects, parasite load, and hormones. A comprehensive literature review on parasitism in dice snakes is presented by Mihalca (p. 255), whereas Bakiev et al. (p. 325) researched parasites and diet in individuals from the Volga River Basin, Russia. Unusual is the find of a juvenile adder (Vipera berus) in the stomach of a juvenile dice snake. Similarly unusual is the consumption of a larger green lizard and a mouse found in a diet analysis of Turkish dice snakes (Göçmen et al. p. 365). Three small radiotelemetric studies give us a greater insight into the activity pattern of individual N. tessellata. For example, Neumann & Mebert (p. 39) report on a short study in Germany, where three gravid females were radiotracked almost daily over two months. They found little movements of the snakes only up to 15 m away from the water line and up to 100 m along the shore during the summer. Interestingly to note that these semi-aquatic snakes descended only every 4–5 days from their terrestrial shelter on the river bank to forage in the water, but else remained on land to rest and thermoregulate. Conelli et al. (p. 100) revealed seasonal movements (different summer and winter habitats) at one site in southern Switzerland, whereas the dice snakes at two other sites in the region remained relatively sedentary, i.e. were active and hibernated in the same area. A radiotelemetric study in Prague, Czech

Republic, found individual movement differences within one population, as some snakes migrated from the shore habitat inland to the hibernaculum for the winter, whereas other individuals hibernated directly in the river bank, the actual summer foraging habitat (Velenský et al. p. 157). They collected also many other fascinating information, such as data on ecdysis and oviposition, duration of hibernation, and rapid colonization and population growth at that particular site after a complete shore reconstruction. Short contributions deal with the rare occurrence of interspecific hybrids in the genus Natrix (Mebert et al. p. 154), anecdotal accounts of nocturnal behavior in dice snakes (Mebert et al. p. 234), and fatal hunting accidents of dice snakes (Mebert & Pölzer p. 145). Even shorter are the Photo Notes, which illustratively present information on feeding of introduced spiny fish, and more unusual stomach contents such as small rocks (Velikov p. 447, Mebert p. 448, respectively), the first records on melanistic dice snakes from Slovenia and the only known albino in this species (Cafuta p. 442, Mebert p. 441, respectively), predation by a snake and a gull (Jelić p. 450, p. 451, respectively), large mating aggregations (Mebert & Ott p. 437), distance records from the water (Mebert p. 453), brief accounts on a successful method to manually attract dice snakes by elicitating waves in the water (Mebert & Trapp p. 445), and an impressive image of a dice snake in the water, with its upward position of eyes and nostrils just above the water surface, which likely enables the dice snake to remain partially submerged in the water as a visual protection against predators (Trapp & Mebert p. 440). Not only in Photo Notes, but overall in this Mertensiella, we used plenty of pictures and graphs, as figures often convey the messages more efficiently than lengthy descriptions. Finally, the volume is complemented with a DVD by Egerer & Mebert, showing various sequences of the dice snake in its natural environment with footages about foraging, courting, and other activities in Austria and Greece. Parallel Activities and Future Perspective In the process of producing this Mertensiella about the dice snake, opportunities were taken in 2009 to promote international research for this species in a workshop at the SEH- (Societas Europea Herpetologica) Meeting in Kuşadasi, Turkey, and at a field herpetological conference in Bad Kreuznach, Germany, focusing on N. tessellata with a more middle European perspective. Latter was also the result of the dice snake having been selected and promoted as the “reptile of the year – 2009” by the DGHT (Lenz et al. 2009). What will the future bring in regards to research with N. tessellata. The large scale studies in Macedonia (Sterijovski et al. p. 298) and Romania (Carlsson et XI

al. p. 237, Kärvemo et al. p. 245) likely will continue. Possibly, new population level studies will join, as locations in Montenegro, Bulgaria, Greece, and at many sites along the Caspian Sea are particularly suited due to high densities of dice snakes. A finer phylogeography for populations in the Balkans could shed light on the ancient Greek clade compared to more recent BalkanEuropean clade north of Greece (Guicking & Joger p. 1). A radiotelemetric study is currently investigating the interspecific situation between N. tessellata and N. maura at Lake Geneva, Switzerland (S. Ursenbacher, pers. comm.). Peripheral populations will attract more attention in the future, in particular the distribution in Poland, the expansion in Egypt towards Sudan, the mountains in southern Romania, the limital distribution from Persepolis to the Persian Gulf in Iran, and also in Pakistan and China. Further studies that I am personally involved or interested are: (a) a potential study about the effects of environmental contaminants and parasites on dice snakes from the Caspian Sea coast of Azerbaijan; (b) a re-assessment of the population status of dice snakes at Lake Alpnach, central Switzerland, after the population has experienced a severe breakdown in the mid-1990s; (c) investigating the origin of the introduced dice snakes in Lake Zürich by genetic means; (d) assessment of the conservation needs and supporting measures for the northernmost German population at Meissen; (e) relationship and origin of the Baltic Basin populations; (f) populations ecology of dice snakes on Aegean islands; (g) marine habits in populations from the Mediterranean to the Caspian Sea; (h) colonization of islands by means of msats; (i) and various publishing project on already existing data. Finally, I would like to thank the DGHT for supporting this comprehensive project, in particular Andreas Mendt for his layout work, Jörn Köhler for his variable advice and help as a chief editor, and DGHT-vice president Axel Kwet, for his patience and endurance listening to my worries, lamenting, and his subsequent assistance. I would like to express my sincere gratitude to all authors for their contributions and to get through the multi-layered revision process with me. It was often not easy, but I am certain, that one way or another, we all have benefitted from this project. At the end, we can be proud of the product in our hands. Many thanks to Goran Dusej (adviser of my diploma work with N. tessellata), Michael Gruschwitz, Sigrid Lenz, Iliana and Alice Mebert and Maya Henggeler, all who somewhere crossed my path that finally led to this Mertensiella. Merenschwand, September 2011 Konrad Mebert

XII

References Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Gygax, P. (1968): Die Entwicklung der Giftdrüse bei Natrix tessellata. – Rev. Suisse Zool. 75: 549–557. Gygax, P. (1971): Entwicklung, Bau und Funktion der Giftdrüse (Duvernoy‘s gland) von Natrix tessellata. – Acta trop. 28: 226–274. Lenz, S., Mebert, K. & J. Hill (2008): Die Würfelnatter: Reptil des Jahres 2009. – In: Die Würfelnatter, Reptil des Jahres, Aktionsbroschüre. – DGHT, Rheinbach, Deutschland. Mebert, K. (1993): Untersuchungen zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Mebert, K. (2010): Massive Hybridization and Species Concepts, Insights from Watersnakes. – VDM Verlag, Saarbrücken, Germany. Walztöhny, D. & V. Ziswiler (1979): Vergleichend - morphologische Untersuchungen an den Hautsinnesorganen der Blindschleiche Anguis fragilis (Anguidae) und der Würfelnatter, Natrix tessellata (Colubridae). – Rev. Suisse Zool. 86 (3): 705–712.

MERTENSIELLA 18

1-10

20 September 2011

ISBN 978-3-9812565-4-3

Molecular Phylogeography of the Dice Snake Daniela Guicking & Ulrich Joger Abstract. Molecular phylogenetic and phylogeographic studies based on mitochondrial cytochrome b sequences and nuclear ISSR-PCR genomic fingerprinting were performed to elucidate the evolutionary history and intraspecific variation of Natrix tessellata. The results of our studies revealed a well-resolved phylogeny and identified nine mitochondrial DNA haplotype clades, associated with animals from Iran, southern Greece, Jordan/Egypt, Turkey, Caucasus, Kazakhstan, Uzbekistan, Crete, and Europe except for southern Greece, respectively. Molecular data suggest that N. tessellata originated in southwest Asia during the Miocene and underwent a basal radiation around the Miocene-Pliocene boundary with further differentiation of the Middle Asian and European lineages during the Pleistocene. Nuclear data suggest admixture of mitochondrial clades in northern Turkey and the northeastern Aral Sea region. Low geographic differentiation among specimens of the main European lineage points to a severe population bottleneck during the late Pleistocene. Key words. Serpentes, Natrix tessellata, phylogeography, molecular genetics

Introduction To shed light on the evolution and intraspecific variation of the dice snake (Natrix tessellata, Laurenti 1768), we performed a series of molecular phylogenetic and phylogeographic studies (Guicking et al. 2002, Guicking 2004, Guicking et al. 2004, Guicking et al. 2006, Guicking et al. 2009). The use of molecular markers has proven particularly useful in taxa that show only weak and mainly clinal geographic variation of phenotypic traits, as is probably the case in N. tessellata (Laňka 1978, Mebert 1993, Gruschwitz et al. 1999). Molecular markers have the great advantage that they can be easily applied to any living organism and offer a nearly unlimited pool of variability. Variation in molecular markers that are selectively neutral or close to neutral provides tools for dating divergence times, and thus allows to estimate a temporal framework for the evolutionary history of a species, even if it is not or only scarcely represented in the fossil record (Cruzan & Templeton 2000). In phylogeny, molecular tools are applied to reveal the relationships between taxa. In phylogeography, geographical patterns of genetic structure are described and used to infer the history and processes underlying that structure (Avise et al. 1987, Avise 2000, Knowles & Maddison 2002). Today, a variety of molecular markers are available for studying geographic association and evolution. Due to its high mutation rate, strictly maternal inheritance and ease of handling, mitochondrial DNA (mtDNA) has been, and still is, the preferred marker system for phylogeographic studies in animals (Bermingham & Moritz 1998, Avise 2000). Whenever possible, additional information is gathered from the nuclear genome. Due to the different mode of inheritance (the mitochondrial genome is maternally inherited, the nuclear genome biparentally) a comparative analysis of data from the two genomes allows infer-

ence of distribution and gene flow patterns that cannot be obtained from a single data set alone. In the present study, we review the most important results from a number of molecular phylogenetic and phylogeographic studies on N. tessellata, paying particular attention to the temporal-spatial origin of the species, its intraspecific diversity, and geographic distribution of variation. Material and Methods As a source of DNA, blood or tissue samples were collected from living animals, road kills and museum specimens. In addition, we used shed skin when available. In total, samples from 305 specimens were included (see Appendix). DNA was isolated following standard protocols (Sambrook & Russell 2001). Sequences of the mitochondrial cytochrome b gene and three subunits of the NADH-Dehydrogenase were obtained and analysed by phylogenetic methods based on maximum parsimony, maximum likelihood and Bayesian inference (for more details see Guicking et al. 2006, 2009). The robustness of individual branches was assessed by nonparametric bootstrapping (Felsenstein 1985). Genomic ISSR-PCR (inter simple sequence repeats polymerase chain reaction) fingerprints were generated to compare nuclear data against mitochondrial data. ISSR-PCR involves primers during DNA amplification that are designed from di-, tri- or tetranucleotide repeat motifs and thus are complementary to microsatellites (simple sequence repeats). Because of the abundance of microsatellites in the genome, a single oligonucleotide will usually prime several fragments of different lengths in each PCR. Gelelectrophoretic separation of PCR products thus generates characteristic multi-locus fingerprint patterns of the template DNA. Fragment patterns are interpreted as

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

1

Daniela Guicking & Ulrich Joger

dominant markers and are transferred into a 0/1 matrix coding for absence/presence of individual fragments in each sample. Data were analysed using the software programs MEGA 3.0 (Kumar et al. 2004), PAUP 4.0b10 (Swofford 2002), MrBAYES 3.0b4 (Huelsenbeck & Ronquist 2001), Arlequin 3.11 (Excoffier et al. 2005), and Structure 2.2 (Pritchard et al. 2000, Falush et al. 2003, Falush et al. 2007). A “molecular clock” approach was used to estimate the most important divergence times. Different methods based on fossil or paleogeographic data were applied to calibrate the clock. A detailed description of this procedure is provided and discussed in Guicking et al. (2006). From these calculations we estimated the evolutionary rate of the cytochrome b gene in Natrix tessellata at about 1.35% sequence divergence per one million years. Because evolutionary rates may vary strongly even within individual genes of a single species (reviewed in Avise et al. 1992), all time estimates presented in this study must be treated with caution and should not be over-interpreted. To elucidate the evolutionary history of Natrix tessellata in central Europe, more detailed phylogeographic analyses were performed on the corresponding cytochrome b sequences. Phylogenetic relationships among mtDNA were reconstructed by a statistical parsimony network approach as implemented in the program TCS 1.21 (Clement et al. 2000). To test for past demographic change, a mismatch distribution (Rogers & Harpending 1992) was constructed and compared to the expected distribution under a population increase model (“sudden expansion model”) (Slatkin & Hudson 1991, Rogers & Harpending 1992, Rogers 1995), using the program Arlequin 3.11 (Excoffier et al. 2005). The comparison of the sum of square deviation (SSD) between the observed and estimated mismatch distribution was used as a test statistic for the estimated stepwise expansion models (Schneider & Excoffier 1999). Following the method of Rogers (1995) and Schneider & Excoffier (1999), the observed value of the age ex-

pansion parameter (τ) was used to estimate the time of the expansion. This was done based on the relationship τ = 2ut (where u is the sum of per-nucleotide mutation rates in the region of DNA under study and t is the expansion time in generations; Rogers 1995). According to Gruschwitz et al. (1999), a minimum generation time of three years was assumed for these estimations (this is equivalent to the year of first parturition). More detailed information on the procedures of PCR based amplification, sequencing of target regions, ISSRPCR and subsequent data analysis are given in the corresponding original publications (Guicking et al. 2006, Guicking et al. 2009). Results and Discussion Evolution within the Genus Natrix To elucidate the evolution and relationships among the three extant members of the genus Natrix, we performed a phylogenetic study including 44 samples (6 from N. maura, 23 from N. natrix and 15 from N. tessellata) covering the entire distribution ranges of the species (Guicking et al. 2006). Both strands of four mitochondrial genes (cytochrome b, NADH dehydrogenase subunit 1, 2, ND 4 with a total of 3806 nucleotides) were sequenced and phylogenetically analysed. As tree topologies from the four genes did not differ significantly, as verified by a partition homogeneity test, final topologies were obtained from the combined dataset of all four genes. Our data provide good evidence that Natrix maura represents the most basal species of the genus and is sister species to N. natrix and N. tessellata (Fig. 1). Furthermore, phylogeographic analysis of the data identified N. natrix as the only species with a European origin, whereas N. maura and N. tessellata probably originated in northern Africa and southwestern Asia, respectively. The three Natrix species therefore might be interpreted as representatives of three main zoogeographic regions

Fig. 1. Genus phylogeny (left) and hypothesized origin (right) of the three extant Natrix species during the Middle Miocene (approximate distribution of land masses 20 million years ago after Rögl & Steininger 1984).

2

A Range-Wide Molecular Phylogeography of Natrix tessellata

that have contributed to the evolution of European biota (Steininger et al. 1985). Divergence times between all three species pairs were estimated to date back to the late-early or early-middle Miocene (about 15-20 mya). Based on these data, we hypothesized that the evolution of the three extant Natrix species may be correlated with major paleogeological events (Guicking et al. 2006). The genus Natrix most likely originated in southern Asia (see also Hecht 1930). Differentiation of N. maura from the other species may be explained by vicariant evolution on the African and Eurasian continents (Fig. 1). During the lateearly Miocene around 18 to 20 mya the Arabian and Turkish plates collided for the first time and allowed the exchange of terrestrial fauna between Eurasia and Africa (Rögl & Steininger 1984, Steininger et al. 1985). At this time, the ancestors of N. maura might have invaded Africa. Subsequent isolation of the African lineage, possibly as a result of the reopening of the seaway between the Mediterranean and the Indo-Pacific during the middle Miocene (Rögl & Steininger 1984), led to independent evolution of the two populations, giving rise to N. maura in Africa and to N. natrix and N. tes-

Fig. 2. Bayesian phylogram of nine major lineages in Natrix tessellata based on 116 cytochrome b haplotypes. Numbers above branches are Bayesian clade support values (first number) and maximum parsimony bootstrap values (second number).

sellata in Eurasia. Subsequent differentiation of N. natrix and N. tessellata may be explained by fragmentation of the ancestral Eurasian population north and south of the Paratethys seaway that extended from central Europe to Middle Asia throughout most of the Miocene (Rögl & Steininger 1984). According to our hypothesis, the northern populations expanded into Europe and gave rise to the extant N. natrix, while the southern populations remained in southern Asia and eventually evolved into N. tessellata (Fig. 1). Providing our temporal-spatial estimates and interpretations are roughly correct, we may conclude that N. tessellata most likely originated in southwest Asia, where it separated from its sister species N. natrix during the Middle Miocene. Evidence of Strong Intraspecific Differentiation Intraspecific variation in Natrix tessellata was studied based on mitochondrial haplotypes from 305 samples of N. tessellata, covering most of the species’ distribution range (Guicking et al. 2009). Haplotypes were defined on the basis of complete cytochrome b gene sequences (1117 nucleotides). To investigate possible admixture among mtDNA lineages, 163 samples were further analysed by genomic ISSR-PCR finger­printing, including all major cytochrome b clades except for one (clade ‘Jordan’). Mitochondrial data revealed nine major assemblages, that were labelled ‘Iran’ (I), ‘Greece’ (G), ‘Jordan’ (J), ‘Turkey’ (T), ‘Kazakhstan’ (K), ‘Uzbekistan’ (U), ‘Caucasus’ (A), ‘Crete’ (C), and ‘Europe’ (E), referring to the main distribution ranges (Figs. 2, 3). All lineages were well supported by Bayesian clade support and maximum parsimony bootstrap values. In all trees, lineage ‘Iran’ was placed as the most basal group, suggesting the geographic origin of the species in Iran or nearby (see above). Strong evidence of sister relationships was found for lineages ‘Crete’ and ‘Europe’ as well as ‘Caucasus’ and ‘Uzbekistan’. The latter two formed the sister group to ‘Kazakhstan’ and these three together the sister group to ‘Turkey’. Nuclear ISSR-PCR data supported lineages ‘Iran’, ‘Greece’, ‘Crete’, and ‘Europe’ as independent evolutionary clades. No clear differentiation was found between lineages ’Kazakhstan’ and ’Uzbekistan’ on the one hand and ’Turkey’ and ’Caucasus’ on the other hand. Furthermore, analysis of ISSR-PCR data revealed a few specimens that originated from contact zones of two different mitochondrial lineages and comprised alleles from both lineages, suggesting events of recent intergradation. Such snakes of mixed mitochondrial clades were found in the Syr-Darja delta northeast of the Aral Sea (involving lineages ‘Kazakhstan’ and ‘Uzbekistan’), in the Caucasus region (involving lineages ‘Turkey’ and ‘Caucasus’), and in northwest Turkey (involving lineages ‘Europe’, ‘Turkey’ and ‘Greece’) (Fig. 3, Appendix). Assuming an evolutionary rate of 1.35% sequence divergence per one million years for the cytochrome

3

Daniela Guicking & Ulrich Joger

Fig. 3. Geographic distribution of Natrix tessellata phylogeographic lineages (color codes as in Fig. 2). The grey area represents the approximate distribution range of N. tessellata according to Bannikov et al. (1977) and Gruschwitz et al. (1999). Twocolored symbols represent animals with admixed origin from two mitochondrial clades, as revealed by nuclear ISSR-PCR data (see text).

b gene (Guicking et al. 2006), inter-lineage distances of up to more than 8% suggest that intraspecific divergence in N. tessellata probably started about 6-5 million years ago at the Miocene-Pliocene boundary (Table 1). Climate cooling and fluctuating environmental conditions at the end of the Miocene (Crowley & North 1991) might have caused a series of extinction and fragmentation events that promoted vicariant evolution of fragmented populations. Furthermore, the desiccation of the Mediterranean about 6 million years ago, known as the Messinian salinity crisis (Hsü et al. 1977, Krijgsman et al. 1999), might have facilitated range expansions into the Mediterranean region. An estimated divergence time of 5.5 million years between lineage ‘Greece’ and the other lineages suggests that the ancestral Asian population might have expanded westward around the Miocene-Pliocene boundary. Reflooding of the Mediterranean at the end of the Messinian about 5 million years

4

ago might have isolated the population in southern Greece. Also, the mountains leading north to south in mainland Greece might have promoted differentiation of the ‘Greece’ lineage. Sister relationships and relatively small among-lineage distances between clades ‘Turkey’, ‘Caucasus’, ‘Kazakhstan’, and ‘Uzbekistan’ suggest at least one colonization event from southwest Asia to the east during the late Pliocene and early Pleistocene. Further subdivision of the eastern lineage might have been facilitated by another expansion from central Asia west to the Caucasus region. The variable paleogeological history of the Middle Asian river systems during the Pliocene, e.g., the repeatedly changing direction of the Paleo-Oxus (present-day Amu-Darja) flowing either into the Caspian Sea or the Aral Sea depression (reviewed in Létolle & Mainguet 1996), might have facilitated and promoted expansions and fragmentations in the region.

27

4

24

22

18

27

4

176

Jordan (J)

Turkey (T)

Kazakhstan (K)

Uzbekistan (U)

Caucasus (A)

Crete (C)

Europa (E)

Sample size 3

Greece (G)

Lineage Iran (I)

I .0054 .0777 .0752-.0797 .0752 .0734-.0770 .0719 .0680-.0788 .0766 .0734-.0788 .0788 .0761-.0815 .0772 .0743-.0806 .0814 .0806-.0824 .0797 .0771-.0824 .0783 .0752-.0824 .0755 .0707-.0833 .0774 .0725-.0824 .0770 .0725-.0797 .0809 .0779-.0842 .0787 .0770-.0824 .0761 .0717-.0833

.0206

G 5.6-5.9

.0740 .0707-.0779 .0743 .0725-.0761 .0745 .0716-.0770 .0757 .0725-.0788 .0727 .0716-.0735 .0699 .0671-.0725

.0027

5.6-6.1

J 5.4-5.7

.0409 .0331-.0466 .0393 .0358-.0457 .0406 .0367-.0466 .0614 .0555-.0681 .0643 .0591-.0707

.0323

5.2-5.8

5.2-6.2

T 5.0-5-8

.0266 .0233-.0313 .0241 .0197-.0286 .0678 .0654-.0708 .0683 .0636-.0726

.0107

2.5-3.5

5.4-5.6

5.4-6.1

K 5.4-5.8

.0190 .0170-.0215 .0697 .0680-.0708 .0686 .0645-.0725

.0072

1.7-2.3

2.7-3.4

5.3-5.7

5.4-5.9

U 5.6-6.0

.0683 .0662-.0699 .0677 .0636-.0708

.0081

1.3-1.6

1.5-2.1

2.7-3.5

5.4-5.8

5.8-6.2

A 5.5-6.0

1.7-2.2 .0090

.0264 .0233-.0296

4.7-5.2

4.8-5.4

4.7-5.4

4.4-5.2

5.0-5.4

5.3-6.2

E 5.6-6.1

.0009

4.9-5.2

5.0-5.2

4.8-5.2

4.1-5.0

5.3-5.4

5.7-6.1

C 5.7-6.1

Tab. 1. Average genetic distances based on mitochondrial cytochrome b sequences and divergence times between nine major phylogenetic clades of Natrix tessellata. Below diagonal: uncorrected p-distances, average and minimum to maximum values, above diagonal: estimated minimum to maximum divergence times between lineages when assuming a constant rate of 1.35% sequence divergence per one million years. Values in the diagonal indicate maximum within-clades cytochrome b p-distances.

A Range-Wide Molecular Phylogeography of Natrix tessellata

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Genetic distances between lineages ‘Crete’ and ‘Europe’ were about 2.6%, suggesting that these two lineages separated in the late Pliocene or early Pleistocene. The population on Crete, therefore, most likely is autochthonous. Because there is good evidence from paleogeological and biogeographical data that the island of Crete did not have contact to the mainland since the end of the Messinian (Beerli et al. 1996), colonization to or from Crete probably occurred by transmarine dispersal. This seems not unlikely because Natrix tessellata inhabits variably saline environment along the coasts from the Adriatic to the Caspian Seas (Lapini et al. 1999, Gruschwitz et al. 1999). Because of the persistence of the Greek lineage on the Peloponnese and in southern Greece, we may hypothesize that colonization to (or from) Crete might have taken place from the Turkish mainland (assuming a probable occurrence of lineage ‘Europe’ on the western coast of Turkey in the past). A stepping stone model could be assumed for dispersal between the Turkish mainland and Crete including the islands Karpathos and Rhodos, of which at least Rhodos is currently inhabited by N. tessellata (Gruschwitz et al. 1999). A more comprehensive sampling and analysis of animals from Anatolia and Rhodos could help clarify the historical processes that explain the relationship between European and Cretan N. tessellatas. Such a study is projected by P. Kyriazi from the Natural History Museum of Crete and colleagues. Pleistocene Glacial Refugia and Postglacial Expansion Routes The phylogeography of European fauna and flora has been greatly influenced by Pleistocene climatic oscillations (Hewitt 1996, Taberlet et al. 1998, Jansson & Dynesius 2002). From the early Pliocene onwards, climatic conditions experienced frequent oscillations that finally led to the series of major glaciations that characterized the Pleistocene (Webb & Bartlein 1992, Hewitt 2000). During major glaciations, polar ice sheets spread considerably across northern temperate areas, reducing temperatures and compressing marine and vegetation zones southward (Hewitt 2001). In Europe, the glacial ice covered Scandinavia and the northern parts of Germany and Poland as well as the mountain ranges of the Alps and the Pyrenees. Permafrost extended south to the Alps (Hewitt 1996). Less dramatic vegetation changes apparently occurred in Middle Asia (Tarasov et al. 2000). The sparse data available from that region suggest steppe as the prevailing vegetation type around the last glacial maximum and thus provide no evidence that biomes differed strongly from today. As a consequence of climatic cooling, many species went extinct in the northern parts of their distribution ranges, and some dispersed to new locations or survived in climatically favored southern refugia. The most important glacial refugia in Europe were located in the south of the continent, i.e., Iberia, Italy, the Bal-

6

kans, or further to the east, near the Caspian Sea and in the Caucasus Mountains (reviewed in Hewitt 1996, Taberlet 1998, Hewitt 2000). The main refugia were isolated from each other due to the Mediterranean Sea in the south and the east-west oriented mountain ranges of the Alps and the Pyrenees in the north. Thus, genetic differentiation between populations restricted to different refugia was enhanced (Taberlet et al. 1998). In warmer periods, species expanded from glacial refugia and recolonized formerly unsuitable habitats further north (Hewitt 1996, Hewitt 2000). Postglacial northward range expansions can be assumed for lineages ‘Caucasus’ and ‘Europe’, because the present-day distribution of these two lineages clearly extend into areas that were uninhabitable during glacial periods. Sampling of Natrix tessellata from the Caucasus and adjacent regions was too scarce to allow deeper phylogeographic analyses. However, we may presume that glacial refugia of the ‘Caucasus’ lineage were located along the coasts of the Caspian and Black Seas, where the climate was tempered by the influence of the large water bodies (Tarasov et al. 2000). From these refugia, post-glacial colonization most likely followed the river systems of Wolga, Ural, Don, and along the northern coasts of the Black and Caspian Seas. To consider effects of Pleistocene glaciations on central European Natrix tessellata, cytochrome b data obtained from lineage ‘Europe’ were further analyzed phylogeographically. Overlaying information of sample localities on a statistical parsimony network according to six drainage systems (defined as Aegean Sea drainages, Danube catchment area, isolated central European populations in Germany and the Czech Republic, Adriatic Sea drainages of the Balkans peninsula, Italy east of the Apennines, and Italy west of the Apennines) revealed some geographic association (Fig. 4). Approximately half of the network comprised haplotypes found in Italy and along the Adriatic coast of the Balkans peninsula, and the other half comprised haplotypes found in the Balkans and in central Europe. Short connecting branches of one or two mutational steps between both halves of the network indicated only weak phylogenetic divergence between the groups. The observed closer association of populations between both sides of the Adriatic coast, the Balkans and the Italian ones, than in comparison to other Balkan populations farther east, indicates a barrier function of the Dinaric mountains and comparatively strong gene flow across the Adriatic Sea. The latter is probably a result of lower sea levels during glacial periods (Fairbanks 1989) that led to desiccation of the northern Adriatic Sea, and hence, facilitated faunal exchange (see also Lenk et al. 1999). Haplotypes from Slovenian N. tessellata were found in both halves of the network (haplotypes marked with an asterisk in Fig. 4), suggesting that in Slovenia, N. tessellata originating from both, the Italian and the Balkan peninsula, came into contact, consistent with observations of a “Slovenian gap” in other organisms (Hewitt 1999).

A Range-Wide Molecular Phylogeography of Natrix tessellata

Fig. 4. Above: Statistical parsimony network of all cytochrome b haplotypes belonging to lineage ‘Europe’. Each line represents one mutational change, and black dots represent missing intermediate haplotypes. Six geographic regions were defined as shown in the map (middle) and overlaid on the network to illustrate geographic association of haplotypes. Haplotypes found in Slovenian Natrix tessellata are indicated by an asterisk. Below: Frequency distribution of pairwise number of mutational differences (mismatch distribution) between individuals of European N. tessellata. Diamonds represent the observed data, the bold curve is the “sudden expansion model” fitted to the data, and thin lines delineate the 2.5 and 97.5 percentile values of 1000 simulated samples.

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There is no doubt that Natrix tessellata went extinct in central Europe during glacial periods and survived only in climatically favored southern refugia. However, it is not yet known where glacial refugia were located and at what time the population was at its minimum. The mismatch distribution fitted well the predicted distribution under a model of sudden expansion (SSD  =  0.0025, P(SSDobs)  =  0.193; Raggedness index = 0.0182, P(Ragobs) = 0.463; Fig. 4), providing good evidence that the present European N. tessellata populations originate from a small founder population. Assuming a divergence rate of approximately 1.35% per million years for the cytochrome b gene, the 95% confidence interval estimates for τ (2.76–5.28) suggested that the founder population expanded between 91,000 and 175,000 years ago or earlier if a generation time of more than three years is taken as a basis. Although these time estimates should be treated with extreme caution, we may use the information to postulate the following scenario for the late Pleistocene population dynamics of European N. tessellata: During the penultimate glaciation (prior 131 ka BP), which was one of the most severe glaciations of the Pleistocene (Crowley & North 1991), the European lineage of N. tessellata most likely survived only in one or a few southern refugia that were presumably located on the Turkish peninsula, where warmer climates persisted (see also Hewitt 1999). The assumption of a main refugium in Turkey seems particularly convincing in the case of the European N. tessellata, as the climatically most favored refugia in the Balkans in southern Greece (see Tzedakis 1993) were occupied by the ancient ‘Greece’ lineage and consequently not available for the ‘Europe’ lineage. During the last interglacial (131–114 ka BP), the refugial population of the European lineage rapidly expanded into middle Europe and Italy, bypassing the Greek lineage, which was separated by water and mountains. During the last glaciation (114–12 ka BP), the European N. tessellata experienced less dramatic extinction than during earlier glaciations and could possibly survive in distinct refugia in the Balkans (north of the Greek refugium) and in Italy. Closely related haplotypes in central Europe and the Balkans suggest that re-colonization of central Europe during the current interglacial originated from populations on the Balkans and most likely followed the river system of the Danube (see also Guicking et al. 2004). This is also indicated by Holocene fossil records from the upper Danube valley in Germany (Markert 1976). Presentday isolated populations in Germany and the Czech Republic are best interpreted as remnants of a more widespread Middle European distribution range during climatic optima of the Holocene (the Atlanticum, 8 to 5 ka BP, and the Subboreal, 5 to 2.5 ka BP). Provided this scenario is correct, the weak population structure presently observed on the European mainland (Fig. 4) may be interpreted as the beginning divergence of populations that survived the last one or few glaciations in distinct refugia on the Italian and Balkan peninsulas.

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Acknowledgments Numerous people have contributed sample material or helped in one way or the other to make sample material available for us. We are extremely grateful to all of them: T. Amann, A. G. Bakiev, B. Blosat, Y. Chikin, J. Crnobrnja Isailovic, G. Dücker, T. Dujsebaeva, H.-P. Eckstein, H. Enting, W. Fiedler, B. Gautschi, N. Godetsch, M. Gruschwitz, A. Herzberg, A. Hille, S. Kalyabina-Hauf, A. Kapla, L. Krecsag, P. Lenk, S. Lenz, D. Malakhov, G. Mantziou, W. Mayer, P. Mikulicek, D. Modry, G. Nilson, N. Orlov, E. Rastegar, N. Rastegar-Pouyani, E. Razetti, A. Schmidt, K. Smole-Wiener, A. Sproll, S. Tome, O. Türkozan, S. Ursenbacher, U. Utiger, A. Westerström, M. Vogrin, and M. A. L. Zuffi. We would further like to thank Robin Lawson for his contribution to the phylogeny of the genus and many helpful advices, as well as Konrad Mebert for his helpful reviews of our text. Eskandar Rastegar kindly sequenced some Iranian samples. All molecular analyses were performed in the institute of Michael Wink, University of Heidelberg. Financial support for our studies was provided by the Deutsche Forschungs­gemeinschaft (Jo 134-7, Jo 134-9, Wi 719-18) and INTAS (436 RUS 113/665/0-1). References Avise, J.C. (2000): Phylogeography – The History and Formation of Species. – Harvard University Press, Cambridge, USA. Avise, J.C., Arnold, J., Ball, R.M., Bermingham, E., Lamb, T., Neigel, J.E., Reeb, C.A. & N.C. Saunders (1987): Intraspecific phylogeography: The mitochondrial DNA bridge between population genetics and systematics. – Annual Review of Ecology and Systematics 18: 489–522. Avise, J.C., Bowen, B.W., Lamb, T., Meylan, A.B. & E. Bermingham (1992): Mitochondrial DNA evolution at a turtle’s pace: Evidence for low genetic variability and reduced microevolutionary rate in the Testudines. – Molecular Biology and Evolution 9: 457–473. Bannikov, A.G., Darevskij, I.S., Iscenko, V.G., Rustamov, A.K. & N.N. Scerbak (1977): Identification of the Amphibians and Reptiles of the SSSR. – Prosvescenije, Moscow, Russia (in Russian). Beerli, P., Hotz, H. & T. Uzzell (1996): Geologically dated sea barriers calibrate a protein clock for Aegean water frogs. – Evolution 50: 1676–1687. Bermingham, E. & C. Moritz (1998): Comparative phylogeography: concepts and applications. – Molecular Ecology 7: 367–369. Clement, M., Posada, D., & K.A. Crandall (2000): TCS: A computer program to estimate gene genealogies. – Molecular Ecology 9: 1657–1659. Crowley, T.J. & G.R. North (1991): Paleoclimatology. – Oxford University Press, New York. Cruzan, M.B. & A.R. Templeton (2000): Paleoecology and coalescence: Phylogeographic analysis of hypotheses from the fossil record. – Trends in Ecology and Evolution 15: 491–496. Excoffier, L., Laval, G. & S. Schneider (2005): Arlequin ver. 3.11: An integrated software package for population genetics data analysis. – Evolutionary Bioinformatics Online 1: 47–50. Fairbanks, R.G. (1989): A 17,000-year glacio-eustatic sea level record: Influence of melting rates on the Younger Dryas event and deep-ocean circulation. – Nature 342: 637–642.

A Range-Wide Molecular Phylogeography of Natrix tessellata Falush, D., Stephens, M. & J.K. Pritchard (2003): Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. – Genetics 164: 1567– 1587. Falush, D., Stephens, M. & J.K. Pritchard (2007): Inference of population structure using multilocus genotype data: Dominant markers and null alleles. – Molecular Ecology Notes 7: 574–578. Felsenstein, J. (1985): Confidence limits on phylogenies: An approach using the bootstrap. – Evolution 39: 783–791. Gruschwitz, M., Lenz, S., Mebert, K. & V. Lanka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Guicking, D. (2004): Molecular phylogeography and evolution of western Palearctic water snakes (genus Natrix, Reptilia). – Ph.D. dissertation, University of Heidelberg, Germany. Guicking, D., Joger, U. & M. Wink (2002): Molecular phylogeography of the viperine snake (Natrix maura) and the dice snake (Natrix tessellata): First results. – Biota 3: 49–59. Guicking, D., Herzberg, A. & M. Wink (2004): Population genetics of the dice snake (Natrix tessellata) in Germany: Implications for conservation. – Salamandra 40: 217–234. Guicking, D., Lawson, R., Joger, U. & M. Wink (2006): Evolution and phylogeny of the genus Natrix (Serpentes: Colubridae). – Biological Journal of the Linnean Society 87: 127–143. Guicking, D., Joger, U. & M. Wink (2009): Cryptic diversity in a Eurasian water snake (Natrix tessellata): Evidence from mitochondrial sequence data and nuclear ISSR-PCR fingerprinting. – Organisms, Diversity and Evolution 9(3): 201–214. Hecht, G. (1930): Systematik, Ausbreitungsgeschichte und Ökologie der europäischen Arten der Gattung Tropidonotus (Kuhl) Boie H. – Mitteilungen aus dem Zoologischen Museum Berlin 16: 244–393. Hewitt, G.M. (1996): Some genetic consequences of ice ages, and their role in divergence and speciation. – Biological Journal of the Linnean Society 58: 247–276. Hewitt, G.M. (1999): Post-glacial re-colonization of European biota. – Biological Journal of the Linnean Society 68: 87–112. Hewitt, G.M. (2000): The genetic legacy of the Quarternary ice ages. – Nature 405: 907–913. Hewitt, G.M. (2001): Speciation, hybrid zones and phylogeography – or seeing genes in space and time. – Molecular Ecology 10: 537–549. Hsü, K.J., Montadert, L., Bernoulli, D., Cita, M.B., Erickson, A., Garrison, R.E., Kidd, R.B., Mèlierés, F., Müller C. & R. Wright (1977): History of the Mediterranean salinity crisis. – Nature 267: 399–403. Huelsenbeck, J.P. & F. Ronquist (2001): MrBayes: Bayesian inference of phylogenetic trees. – Bioinformatics Applications Note 17: 754–755. Jansson, R. & M. Dynesius (2002): The fate of clades in a world of recurrent climatic change: Milankovich oscillations and evolution. – Annual Review of Ecology and Systematics 33: 741–777. Knowles, L.L. & W.P. Maddison (2002): Statistical phylogeography. – Molecular Ecology 11: 2623–2635. Krijgsman, W., Hilgen, F.J., Raffi, I., Sierro, F.J. & D.S. Wilson (1999): Chronology, causes and progression of the Messinian salinity crisis. – Nature 400: 652–655. Kumar, S., Tamura, K. & M. Nei (2004): MEGA3: Integrated Software for Molecular Evolutionary Analysis and Sequence Alignment. – Briefings in Bioinformatics 5: 150–163.

Lanka, V. (1978): Variabilität und Biologie der Würfelnatter (Natrix tessellata). – Acta Universitatis Carolinae, Biologica 1975– 1976: 167–207. Lapini, L., Dall’Asta, A., Bressi, N., Dolce, S. & P. Pellarini (1999): Atlante Corologico degli Anfibi e dei Rettili del FriuliVenezia Giulia. – Ed. Museo Friulano di Storia naturale 43, Udine, Italy. Lenk, P., Fritz, U., Joger, U. & M. Wink (1999): Mitochondrial phylogeography of the European pond turtle, Emys orbicularis (Linnaeus, 1758). – Molecular Ecology 8: 1911–1922. Létolle, R. & M. Mainguet (1996): Der Aralsee: Eine ökologische Katastrophe. – Springer-Verlag, Berlin, Germany. Markert, D. (1976): Erstmalige Verwendung quartärer Reptilreste bei palökologischen Rekonstruktionsversuchen am Beispiel des oberen Donauraumes um die Wende des Pleistozän/Holozän. – Ph.D. dissertation, Eberhard-Karls-Universität, Tübingen, Germany. Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti) 1768 in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Pritchard, J.K., Stephens, M. & P. Donnelly (2000): Inference of population structure using multilocus genotype data. – Genetics 155: 945–959. Rögl, F. & F.F. Steininger, (1984): Neogene Paratethys, Mediterranean and Indo-Pacific seaways. In: Brenchley, P. (Ed.): Fossils and Climate. – John Wiley & Sons, Chichester, UK: 171–200. Rogers, A.R. (1995): Genetic evidence for a Pleistocene population explosion. – Evolution 49: 608–615. Rogers, A.R. & H. Harpending (1992): Population growth makes waves in the distribution of pairwise genetic distances. – Molecular Biology and Evolution 9: 552–559. Sambrook, J. & D.W. Russell (2001): Molecular Cloning. A Laboratory Manual, 3rd Ed. – Cold Spring Harbor Laboratory Press, New York, USA. Schneider, S. & L. Excoffier (1999): Estimation of past demographic parameters from the distribution of pairwise differences when mutation rates vary among sites: Application to human mitochondrial DNA. – Genetics 152: 1079–1089. Slatkin, M. & R.R.Hudson (1991): Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. – Genetics 129: 555–562. Steininger, F.F., Rabeder, G. & F. Rögl (1985): Land mammal distribution in the Mediterranean Neogene: A consequence of geokinematic and climatic events. – In: Stanley, D.J. & F.-C. Wezel (Eds.): Geological Evolution of the Mediterranean Basin. – Springer Publisher, New York: 559–571. Swofford, D.L. (2002): PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10. – Sinauer Associates, Sunderland, USA. Taberlet, P., Fumagalli, L., Wust-Saucy A.-G. & J.-F. Cosson (1998): Comparative phylogeography and postglacial colonization routes in Europe. – Molecular Ecology 7: 453–464. Tarasov, P.E., Volkova, V.S., Webb, T., Guiot, J., Andreev, A.A., Bezusko, L.G., Bezusko, T.V., Bykova, G.V., Dorofeyuk, N.I., Kvavadze, E.V., Osipova, I.M., Panova, N.K. & D.V. Sevastyanov (2000): Last glacial maximum biomes reconstructed from pollen and plant macrofossil data from northern Eurasia. – Journal of Biogeography 27: 609–620. Tzedakis, P.C. (1993): Long-term tree populations in northwest Greece through multiple Quaternary climatic cycles. – Nature 364: 437–440.

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Daniela Guicking & Ulrich Joger Webb, T.I. & P.J. Bartlein (1992): Global changes during the last 3 million years: Climatic controls and biotic responses. – Annual Review of Ecology and Systematics 23: 141–173.

Appendix Locality data of Natrix tessellata samples (sample numbers are given in parenthesis). Asterisks indicate localities that comprised individuals with ISSR-PCR alleles from two mitochondrial lineages. Sample coordinates are given in Guicking et al. (2009). Lineage Iran: Lar Valley (1), Kermanshah Prov. (2) Lineage Greece: Peloponnese, Gialova (1), Peloponnese, Kalogria (8), Golf of Arta (12), Etoloakarnania (1), Ioánnina (5) Lineage Jordan: Jordan: River Zarqa (3); Egypt (1) Lineage Turkey: Iran: Lar Valley (1); Azerbaidshan: Zangelan Region (1); Armenia (2); Turkey: Birecik (1), Malatya (1), Kemah (1), Ararat (2), Sarkale (6), Sinop (1), Catalzeytin (1), Eskiçaga (1), Lake Yeniçaga (5) Lineage Kazakhstan: Kazakhstan: Almaty Region (6), River Ili (2), Karatau mountains (2), Lake Kamyslebas (2), Raim (3)*; Uzbekistan: near Gazalkent (6); Tashkent: River Syr-Darja (1) Lineage Uzbekistan: Uzbekistan: near Urganc (2), Kungrad (4), Amu-Darja Delta (5), Djanpyk (1), Lake Ashikol (1), Aral Sea (2); Kazakhstan: Baskara (1), Lake Tschebas (1), Syr-Darja Delta (1)

Lineage Caucasus: Iran: near Mashhad (2), Guilan Prov. (1), Lemir (4); Georgia: Agara (1), near Tbilisi (3), Rustavi (7)*; Chechnia: Chechen-Ingush (1); Russia: Astrakhan Region (3), Samara Region (1); Ukraine: Nikolaev Region (1); Kazakhstan: Kaulschur River (2), River Turgai (1) Lineage Crete: Greece: Crete, Áyios Nicólaos (3), Crete, Finika (1) Lineage Europe: Turkey: Sile (1)*, Sapanca (2)*; Greece: Seres (2), Northeast (1), Kastoria (1); Montenegro: Lake Skadar (3), Spuz (1); Bosnia and Herzegovina: Lake Jezero (3); Serbia: Veliki Rzav (2), Crna Kamenica (1), Luznicka dolina (1), Tresnja (1), Kostolac (1); Croatia: Zadar (1); Bulgaria: no locality (2), near Sozopol (1); Romania: Danube Delta (8), Banat (1), Cluj (1); Hungary: Lake Balaton (3); Slovakia: near Bratislava (5); Austria: Carinthia, Lake Wörther (5), Carinthia, River Drau (12); Czech Republic: River Eger (16), River Berounka (6); Germany: River Lahn (11), River Mosel (10), River Nahe (7); Slovenia: near Zalec (1), near Celje (2), River Drava (4), Lepena (1), River Sava (11), Ljubljana (1), River Soca (1), Polovnik (3), Istria (2), Mirna Pec (3), River Dragonija (1), Portoroz (1); Italy: Grado (5), Tezze (1), Lake Garda (5), Castelleone (1), near Ottono (1), near Varzi (2), Vigevano (1), Somma Lombardo (1), Lari (1), Lazio (4), Lago di Lesina (4), near Taranto (3), near Baragiano (1); Switzerland: Lake Lugano (5)

Authors Daniela Guicking, Universität Kassel, Systematik und Morphologie der Pflanzen, Heinrich-Plett-Str. 40, 34132 Kassel, Germany, e-mail: [email protected]; Ulrich Joger, Staatliches Naturhistorisches Museum, Pockelsstr. 10, 38106 Braunschweig, Germany.

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MERTENSIELLA 18

11-19

20 September 2011

ISBN 978-3-9812565-4-3

Geographic Variation of Morphological Characters in the Dice Snake (Natrix tessellata) * Konrad Mebert Abstract. Pholidotic characters and a few body proportions have been investigated in dice snakes (Natrix tessellata) from the western limit south of the Alps to those from northeastern Turkey. All scale characters vary clinally, mostly with increasing values in representatives from west (Italy) to east (Turkey). With the donation of a large private data collection by the late E. Kramer, the geographic variation of ventral scale counts could be studied across the entire range of N. tessellata. The ventrals not only increase from west to east, but also from south (Egypt to Iraq) to north (northwest of the Caspian Sea), and from lowlands to mountains in southern areas. The possibility of climaparallel variation in scale characters is briefly discussed. Body proportions show no large-scale geographic correlation, but rather appear to depend on environmental characteristics pertinent to a particular population. Key Words. Natrix tessellata, morphology, geographic variation, cline, driving forces

Introduction The geographic variation of exterior features within the huge range of the dice snake (Natrix tessellata, Laurenti 1768) has not been well studied to date. Approximately 100 years ago, Dürigen (1897) and Schreiber (1912) have investigated the variation of scale characters and color morphs in N. tessellata, and included also earlier works by other authors. In 1930, Hecht tried to evaluate the morphological variation in dice snakes, but ultimately, the samples of these researchers were not representative for a species with such an extensive range. Mostly, related works of the dice snake concerned morphological variation on a national level, e.g. Romania (Fuhn & Vancea 1961), Ukrainian Carpathians (Shcherbak & Shcherban 1980), Czech and Slovakian republics (Kminiak & Kaluz 1983, RehÁk 1992), Western Germany (Lenz & Gruschwitz 1993), Austria (Zimmermann & Fachbach 1996), Israel (Werner & Shapira 2011), China (Liu et al. 2011), Turkey (Dincaslan et al. 2011), Iran (Rajabizadeh et al. 2011), and Bulgaria (Naumov et al. 2011). Some studies give summarized mean values for snakes originating from widely distributed localities. For example, Baran (1976) applied such mean values for dice snake samples covering the huge area from the Dalmatian Coast, to Israel and Iran, whereas Bannikov et al. (1977) showed similar results averaged over all the former Soviet States. But information about geographic variation is lost in these summary results. A closer look at geographic variation across borders without loosing the perspective for regional character expression was achieved by Laňka (1978). He noted differences in the number of ocular scales and to a smaller extent also concerning the number of labial

shields between animals of the North (Czech Republic) and the South (Romanian-Bulgarian Black Sea Shore). Southern dice snakes tend to have a higher number of scales/shields. Unfortunately, sexual dimorphic scale-characters in dice snakes, in particular the number of ventrals and subcaudals, and to some degree even the number of postoculars or the arrangement of some labials (Mebert 1993), should be analyzed separated by sex in order not to confound regional expression of characters. Therefore, an earlier work by the author attempted to diminish this lack of precision and method by analyzing a number of morphological characters on a regional basis, but over a larger geographic area and separated by sex (Mebert 1993, 1996, Gruschwitz et al. 1999). However, these studies focused on a comparison of autochthonous and allochthonous populations of dice snakes from the central Alps (Mebert 2011a), including an analysis of sexualdimorphism (Mebert 2011b), and only a few data were presented about the wider geographic variation of morphological characters. Finally, Kramer et al. (1982) published one paragraph with nine lines on data about the whole-range geographic variation of 9 morphological characters based on 850 preserved specimens. Their preliminary results divided the dice snake into a Mediterranean and an East European-Asian group. This study was not further elaborated, but the raw data was donated to the author (see below). Even though, this report will remain preliminary as well, since more data already received are not included and await new and different statistical analyses, the presentation of data on a finer geographic scale on some selected and easy quantifiable characters of morphology is feasible, reflecting the scope of variation in this truly

*) This article is in honor of the late Eugen Kramer, who submitted his meticulously acquired data on more than 600 preserved dice snakes and never had the chance to see its inclusion in studies such as this one. ©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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palearctic species. Due to its meristic characteristic and the large variation embedded, the analysis is focused on ventral scale values, which are exemplary in demonstrating the variation across a large geographic area. Material and Methods The database consists of three principal sets: Set 1 relates to personal field sampling (n = 170), Set 2 to museum specimens (n = 204), and Set 3 to the private data collection of E. Kramer (n = 600). Set 1: Field sampling was conducted between 1990 and 1991 at two lakes, Lake Lugano in southern Switzerland (n: females = 44, males = 44) and Lake Garda in northern Italy (n: females = 44, males = 44). Only adult snakes were sampled (total length ≥ 40 cm, ≈ SVL of 32 cm) to reduce the influence of allometric growth and different size/age classes. Furthermore, only animals, which still possess the entire tail (tail tip visible), were used. The snakes have been measured and marked in the laboratory and released afterwards at their site of capture. Set 2: This group consisted of 197 dice snakes (88 females and 109 males) from the Natural History Museum of Geneva (MHNG) and another 37 preserved specimens from various collections. Latter included a few single, private specimens, as well as 14 females and 3 males from Western China measured by N. Helfenberger at the Chengdu Institute of Biology (see Liu et al. 2011), and 4 females and 3 males from Egypt stored at the Alexander König Museum, Bonn, Germany. Set 3: The original data collection by E. Kramer consisted of a few morphological characters, e.g. the number of ventrals/subcaudals, ocular scales, dorsal rows at the 100th ventral scale, dorsal blotches, and sublabials. The counts of ventrals and subcaudals were included in my study, as they are highly quantifiable, show sufficient geographic variations and are compatible with my data recording. Kramer’s original data volume contained 850 specimens, of which 600 specimens (281 females and 319 males) were applied for a whole-range analysis. Data on the remaining 250 specimens were redundant with my previously acquired data, as they related to Swiss specimens, which I have sufficiently covered in data Set 1, and others relate to preserved specimens from the MHNG from data Set 2. Finally, Kramer’s data helped greatly to expand the scope to study the variability of the dice snake across a large geographic area. An additional large data set of n = 289 dice snakes previously applied for a microgeographic analysis, comparing allochthonous with autochthonous populations from the central Alps (Mebert 2011a), was not included, as it was irrelevant in the perspective of this widegeography analysis. For data sets 1 and 2, a total of 36 out of 53 characters (weight, pholidosis, lengths, color and pattern) were initially analyzed. The selected characters include ventrals, subcaudals, dorsal and caudal scale-row reductions, various labial and ocular scales,

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contact between eye and supralabials, total length, and relative tail length. These morphological data were acquired from specimens mainly originating in an area from middle Europe to Turkey, but with the additional specimens from Egypt and China mentioned above. The definitions of characters, method of measuring, and application of statistical procedures for absolute and relative data is explained in Mebert (1993, 2011a), but is briefly indicated in the text, where it was deemed helpful to prevent misunderstanding. Specimens from geographically associated regions were grouped together especially for snakes originating from the same or closely connected drainage areas, in sensu river systems. If two close water systems are separated by a topographic barrier, than the samples of those areas were lumped only when they did not show major differences in the selected characters. The same method was applied to a selected group relating to a very large area, as for example in the Italian group, in which specimens from the far distant regions between Southern and Northern Italy do not show significant differences. Finally, published data were included from regions where the author has no or insufficient material, and where the results for each sex were separately shown. Results and Discussion Ventrals (data sets 1–3) General articles reviewing scale characteristics of a snake species often present the extreme values of scalation counts to reveal their maximum range within the species or at least on a regional basis (see Gruschwitz et al. 1999). For comparative reasons, this is briefly reviewed in the following accounts. Dice snakes with the highest mean values of ventrals originate from the region north of the Black Sea between the Crimea Peninsula and the Volga delta (Caspian Sea, see below). The highest individual number of ventrals are also from dice snakes in this region (ventrals = 193), based on a female and two males. Farther east towards China, southeast towards Iran and from the Northern Turkey south to Egypt and the Persian Gulf, the number of ventrals decreases; a female from Egypt with 152 ventrals and two males with 159 ventrals, one from Egypt and one from Israel, were the lowest values found. In literature, the lowest ventral number is 148 (Schreiber 1912) and may belong to a dice snake from the Levant or Egypt as well. Alternatively, Schreiber’s particular low ventral minimum probably originates from the morphological similar viperine snake (Natrix maura), that generally exhibits lower ventral numbers (Schätti 1982), and was often confused with N. tessellata in the past. In his text, Schreiber (1912) mentions explicit the dice snake from France, where actually only the viperine snake occurs. The highest ventral count of 198 is listed in Hecht (1930), which is the maximum value normally referred to in publications. This record probably belongs to a specimen from the region north

Geographic Variation in Morphology of Natrix tessellata

of the Black Sea, where the highest values are found, but no locality is explicit mentioned for this specimen in Hecht’s publication. Furthermore, before Dow­ling (1951) suggested the widely accepted ventral-counting method, the anterior preventrals scales were included in counting ventrals,, thus resulting in a slightly higher number of individual ventrals. Within N. tessellata, this concerns mostly 1 to 2 preventrals in an individual, but up to 6 were also found. The descriptive data show that ventrals in N. tessellata vary clinally over distance. Four geographic models have been selected to illustrate the clines of mean values, roughly in an east-west direction (Figs. 1–4). With a few exceptions, most regional values (means) selected for a

Fig. 3. Northern cline of the number of ventral scales (means) in Natrix tessellata; n adjacent to the mean value. Lit (= value from Literature without n). Regions are: CzSl (Czech and Slovak republics, data by RehÁk 1992), UkCa (Ukrainian Carpathians, data by Shcherbak & Shcherban 1980), Roma (Romania, data by Fuhn & Vancea 1961), TuBS (Turkish Black Sea Coast), NoBS (North of Black Sea), EaCS (East of Caspian Sea), Kaza (Kazakhstan), NElb (North of Elburs Mts.), TkIr (Turkmenistan-Iran border area), TkUz (Turkmenistan-Uzbekistan area), AfTz (Afghanistan-Tadzikistan), Kirg (Kyrgyzistan), NWCh (North-Western China), KiCh (Kizil, China).

Fig. 1. An eastern Circum-Mediterranean cline of the number of ventral scales (means) in Natrix tessellata; n adjacent to the mean value. Regions are: PoPl (Po Plain, northern Italy and adjacent southern Switzerland), WeBa (Western Balkan), Gree: (Greece), TuBS (Turkish Black Sea Coast), TuWc (Turkish Western Coast), TuSC (Turkish South Coast), Isra (from north to south in Israel, data by Werner & Shapira 2011), Egyp (from Nile delta to El Faiyum, Egypt).

Fig. 2. Central-Southern cline of the number of ventral scales (means) in Natrix tessellata; n adjacent to the mean value. Regions are: LSWT (Lakes Region of South-West Turkey), TuSy (Turkish-Syrian border area), NoIr: (Northern Iraq), CeIr (Central Iraq), SoIr (Southern Iraq).

Fig. 4. Clinal variation in the number of subcaudal scales (means) in Natrix tessellata; n adjacent to the mean value; Lit (= value from Literature without n). Regions are: PoPl (Po Plain, northern Italy and adjacent southern Switzerland), WeBa (Western Balkan), Gree: (Greece), TuBS (Turkish Black Sea Coast), NeTu: Northeastern Turkey (Region between the town Kars and Lake Van), LSWT (Lakes Region of South-West Turkey), Isra (from north to south in Israel, data by Werner & Shapira 2011), Egyp (from Nile delta to El Faiyum, Egypt).

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cline are based on a minimum sample of n = 5 per sex in order to remove the variation caused by sexualdimorphism of ventrals (Mebert 2011b). Yet, the clines vary parallel in both sexes. The graphs certainly simplify the overall geographic variation, in particular in mountainous areas such as southern and eastern Turkey, where the geographic variation probably is increased due to temporary isolation. But the clines provide an overview of the variation in a species with a huge distribution. The clines orientate themselves along putative natural expansion routes including river systems, coastal areas and mountains. A first, eastern Circum-Mediterranean cline is depicted in Figure 1. Ventral values increase in eastern direction, beginning at the western edge of its distribution, the Po Plain (southern Switzerland and northern Italy) following along the eastern Adriatic coast, across Greece to reach the highest values in this cline along the Turkish Black Sea coast. From there, ventral values decrease in populations around the Turkish Mediterranean coast, and continue to decline along the Levantine coast to reach the lowest mean of ventrals for this species in Egypt. A second cline (Fig. 2) begins with relatively high values of ventrals in the Lakes Region of southwestern Turkey. This cline of ventral values decreases into the lowlands of southeastern Turkey/northern Syria. From there and from adjacent northern Iraq, ventral values in dice snakes continue to decrease in southern direction along Euphrates River as far as southern Iraq. A third cline (not shown) represents the central area of distribution and begins with high ventral values in northeastern Turkey. From there, the ventrals counts are slightly decreasing, but maintaining high values, following a route along the Zagros Mountains into central Iran (incl. Tehran). The cline ends with slightly lower ventral values in Fars, in southern Central Iran. A fourth, the Northern cline, is supported by various literature data in its western part. It begins with relatively small values in the Czech Republic (Fig. 3), continues with steadily increasing values southeast along the Carpathians into Romania, and farther east to finally reach the highest ventral values for N. tessellata in an area between the Black Sea and the northern half of the Caspian Sea. Here, the dice snakes exhibit on average 18 ventrals more than conspecifics in Western Europe. The cline decreases again along the low-lying areas east of the Caspian Sea to reach its regional low along the southern coast of the Caspian Sea. From there, ventral values increase again into the various mountainous areas towards the East as far as into China and Afghanistan. Subcaudals As for ventrals, there appears to be a clinal increase in the number of subcaudals from west (Italy) to east as far as Turkey. The highest values in males are reached in western Balkan and in females in Greece (Fig. 4).

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The probably isolated population at Lake Iliki, central Greece, is excluded in this analysis, because it shows various unusual characters (Mebert 1993). Turkish dice snakes exhibit low numbers of subcaudals similar to specimens from Western Europe. Animals from the Near East also show on average low numbers of subcaudals. Three males from the area between Western Syria and Egypt possess the lowest absolute values of 59 subcaudals and a female from Bralos, south of Lamia in central Greece, shows the minimum with 47 subcaudals, equal to those reported by other authors (see refs. in Mebert 1993). The highest number of 87 subcaudals were reported by Bannikov et al. (1971). Overall, the subcaudal variations are more subtle and less prominent over geographic distances than the clines in the ventral counts. As in ventrals, there are high values in N. tessellata from the area between the Black Sea and the northern half of the Caspian Sea, but similar high values can be found in different areas in Europe and Asia. Color Polymorphism A dice snake, varying from olive to beige, grey, and brown, with 4–5 rows of dorsal blotches is the common form and occurs anywhere in its large distribution. Large and small spotted dice snakes may occur in the same populations (see Tuniyev et al. 2011). But in the Levant and Egypt, small spots and a prominent blackish nuchal angle is the common morph (Baha el Din 2011, Werner & Shapira 2011). Other variations, such as melanistic and spotless (concolor) morphs can be locally absent to be very abundant, but occur over most of its huge range, including recently discovered ones, such as two concolor dice snakes from Prague, Czech Republic (Fig. 5), and Lake Garda, Italy (Mebert 1993, and Figs. 6a–e), or the melanistic dice snakes in Slovenia, Cafuta (2011).

Fig. 5. Patternless (concolor) Natrix tessellata from Prague. A hatchling and an adult with dorsal and ventral view. Photos: Petr & Mikulas Velenský

Geographic Variation in Morphology of Natrix tessellata

Melanism in dice snakes occurs in temperate wet to mediterranean dry areas, on mainland or islands (Mebert 2011c). They occur with a constant frequency of 10%–17% at Lake Lugano in southern Switzerland (Mebert 1993, Fig. 7), only to be completely unknown in nearby Lake Como 10 km farther east without any physical barrier between the two lakes. There is no visible pattern, where melanistic or concolor dice snakes occur, except that their frequency appears to be higher towards the center of its distribution, mainly between the southern Balkan and the Caspian Sea. But they are also known from areas north of the Black Sea, east into Kazakhstan, Kyrgyzstan, Uzbekistan, and south into Iran, Iraq and Syria (Mebert 2011c, and E. Kramer, unpubl. data). A rare morph, in which the blotches are partially striped or at least appear to be stretched longitudinally, has been found occasionally at the Caspian Sea (Tuniyev et al. 2011), Syria (e.g. Ataibe east of Damascus), and at Persepolis, northeast of Shiraz, southern Iran (Mertens 1969 and E. Kramer, unpubl. data). This

Fig. 6. Large variation of dorsal and ventral pattern in Natrix tessellata from Lake Garda in Italy, including concolors, weakly spotted to prominently spotted specimens; a–d (dorsal views), e (ventral view). Photos: Konrad Mebert.

Fig. 7. A male and female (insert left) of melanistic Natrix tessellata from Lake Lugano, Switzerland. Photos: Herbert Billing & Konrad Mebert.

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Fig. 8. Tendency to striping and longitudinally stretched dorsal blotches in Natrix tessellata from Lake Iliki, Greece. Preserved females from the Natural History Museum of Geneva. Photos: Konrad Mebert.

form occurs also with a constant frequency at Lake Iliki, in central Greece (Mertens 1969) (Fig. 8). Additional Morphological Characters (data sets 1 and 2) A number of additional scale characters have been investigated in N. tessellata from an area between Western Europe to Eastern Turkey. Similar to the number of ventral counts, these characters show a clinal variation with increasing values for both sexes from west to east. For example, the ventral position (relative to the ith number of ventral scales, see Mebert 2011a) of the bilateral reduction from 19 to 17 dorsal scale-rows is shifted more posterior, i.e. closer to the vent, in specimens from farther east, with the highest values were recorded

Fig. 9. Clinal variation of the subcaudal scale position (means) of the scale-rows reductions to 8 caudal rows (= R8Cau) in Natrix tessellata; reR8Cau (%): relative position [(R8Cau/subcaudals)*100]; n adjacent to the mean value; regions are: PoPl (Po Plain, northern Italy and adjacent southern Switzerland), WeBa (Western Balkan), Gree (Greece), NeTu: Northeastern Turkey (Region between the town Kars and Lake Van).

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in dice snakes from Greece (see Mebert 2011b). In comparison to snakes from Italy, the position of the reductions in Greek females is shifted by an average of 10.4%, and in males by 9.0%, towards the vent. Hence, these reductions occur approximately 17 to 20 ventrals farther posterior in Greek animals. An additional reduction to 15 dorsal scale-rows on the trunk is very rare in dice snakes east of Italy (3 out of 158 snakes), whereas up to 30% of western snakes reduce down to 15 scalerows. The situation is comparable for corresponding scalerow reductions on the tail, but in this trait, snakes from north eastern Turkey exhibit the highest values. The reduction to 8 dorsal scale-rows is shown as an example in Figure 9. Similar to scale-row reductions on the trunk, the increase in the caudal reductions in north eastern Turkish dice snakes amounts from 5% to 10%. Labial and ocular scales tend to increase also from west to east. For example 27.5% of the female and 7.6% of the male dice snakes from areas east of Italy evolved more than 10 sublabials, including three females with 12 sublabials and one male with unilaterally 13 sublabials. In comparison, no snake from natural populations in Western Europe showed more than 10 sublabials. Regarding postocular scales, 90.5% of the dice snakes in the eastern group show 4 or more postoculars, whereby the increase to higher values in eastern populations begins at Greece. In more western dice snakes, only about 40% showed 4 or more postoculars. The situation is similar but less prominent in the number of preoculars. Finally, in approximately 90% of the eastern dice snakes the eye is in contact with only the fourth supralabial scale. The comparable value for snakes from western populations is substantially decreased and varies from 13% to 55%, as the eye in western dice snakes is commonly in touch with the fourth and fifth supralabials. The longest dice snake was measured by Calinescu (1931) and originates from a specimen from Romania with a total length of 130 cm, including 22 cm for the tail. However, the total length is dependent on the population, respectively locality, and not on the latitude itself, i.e. dice snakes from warmer, southern areas are not automatically larger, as was often written in semi-popular publications (see refs. in Mebert 1993). Even between genetically closely related to identical populations, specimens achieve often different average total lengths, probably due to variable ecological causes, including microclimate, food, pollution, and predation, and consequently individual survival and growth. For example, based on large samples and equal methods (Mebert 1993, 2011a), adult dice snakes of allochthonous populations in Switzerland at the lakes Geneva, Alpnach, and Brienz, achieved on average greater lengths and weights than their parental population in climatically warmer Ticino, southern Switzerland, or similarly from another autochthonous population at Lake Garda, Italy, with the smallest specimens in this comparison (Mebert 2011b). Tails of dice snakes from western Balkan and Greece are

Geographic Variation in Morphology of Natrix tessellata

Even small samples like the ones from Verzasca Valley, Lake Iliki, and central Turkey are correctly grouped. This means that the remarkable geographic variation of the dice snake enables the correct allocation of a specimen with unknown geographic origin by using a multitude of morphological characters as in this study. For example, the number of ventrals and subcaudals in Israeli dice snakes resemble more those of western European specimens than the physically closer northern Turkish dice snakes. However, the Israeli snakes are correctly grouped with the Near East-Turkey sample, because of the inclusion of additional characters like scalerow reductions. Mechanisms of Geographic Variation of Pholidosis

Fig. 10. Cluster phenogram showing the phenetic relationships in Natrix tessellata among different regions of Europe to the Near East (eastern Mediterranean). The analysis was processed with relative values of body proportions, positions of scale row reductions, and numbers of ventral/subcaudal/ cephalic scales (Mebert 1993, 2011a). The regions are in alphabetical order: CeIt (central Italiy), CeTu (central Turkey), Gree (Greek mainland, without specimens from Lake Iliki), LaAl (Lake Alpnach, alpine Switzerland), LaBr (Lake Brienz, alpine Switzerland), LaGa (Lake Garda, northern Italy), LaGe (Lake Geneva, western Switzerland), LaIl (Lake Iliki, central Greece), LaLu (Lake Lugano, southern Switzerland), MaVa (Maggia Valley, southern Switzerland), NeEa (Near East), NeTu (North eastern Turkey), Turi (Turin, north western Italy), VeVa (Verzasca Valley, southern Switzerland), WeBa (Western Balkan, especially Dalmatian coastal region).

on average from 1% to 4% longer (relative to SVL) than in other conspecifics from western Europe to northeastern Turkey. To investigate whether the intraspecific morphological variation is suitable to indicate physical proximity and potentially phylogenetic relatedness, a cluster analysis based on 27 normally distributed characters (various body proportions, positions of scale-rows reductions, and numbers of ventral/subcaudal scales) was processed by the method of WPGMA (Weighted Average Linkage), using standardization and correlation of mean values and standard deviation (sexes separated). Figure 10 shows phenetic similarity among male dice snakes. A similar phenetic diagram for females is displayed in Mebert (2011a). The cluster analysis groups dice snakes that are from contiguous areas, and thus confirms that phenetic similarity represents relatedness.

The geographic variation of pholidotic characters in Natrix tessellata is large, but its clinal pattern precludes any partitioning into regional groups, or even distinct systematic taxa. I anticipate that a future study may show that the geographic variation of morphological characters in the dice snake is consistent with the genetic structure (nine major clades in N. tessellata based on cytochrome b sequences) and phylogeographic history already investigated (e.g. Guicking et al. 2009, Guicking & Joger 2011). It may also require a geographically more fine-scaled analysis, in particular along the contact zones of putative genetic or morphological groups. The clines imply some history of relatedness and regional temporary isolation, as their ranges expand and retract due to environmental changes. Another issue relates to the potential ecological causes of the observed clinal variation of pholidotic characters, e.g. climatic factors. It has been shown that scale numbers decrease towards cooler and moister environments in Californian snakes species Klauber (1941), as well as in a thermal experiment with Thamnophis species Fox et al. (1961). However, in the related North American natricines Nerodia sipedon and N. fasciata, the number of ventral scales and dorsal scale-row reductions increases in populations from cooler, more northerly or mountainous (only N. sipedon) regions (Mebert 2010). This suggests that a cooler climate promoted the evolution of a greater body volume via higher scale numbers, and thus body segments, to increase clutch mass (higher number or greater size of embryos) and food intake to compensate for a shorter activity season. Such a scenario may fit the most prominent clinal increase of ventral scale counts in dice snakes from the lowlands of the North Arabian Peninsula (Iraq, Syria) northward to the area with the highest ventral counts between the Black and the Caspian seas. Furthermore, there is a tendency in southern areas for increasing scale numbers from populations in the lowlands towards those in the mountains, e.g. in Turkey and the mountains between Iraq and Iran. These meristic variations are probably correlated with environmental factors, given the large seasonal climatic differences in those areas.

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A similar climaparallel variation was detected in the lizard genus Liolaemus from Chile, whereby scale numbers increase with a correlated decrease of scales size towards the moister and cooler south (Hellmich 1951). However, the reduced scale counts in northern and cooler areas of Europe compared to values in the warmer Mediterranean area contradicts the simplicity of the hypothesis and indicate that other selective forces may also play a role in shaping the variation of pholidotic characters. Even though, if the scale number-climate correlation is valid in some regions, other regions possibly experience a different composition of selective forces with a distinct outcome. More complicate is the search for direct causative factors for the climaparallel variation of scale characters, and is beyond the scope of this report. Just briefly a few accounts in this regard to indicate the complexity of this issue. Soulé (1966) and Soulé & Kerfoot (1972) found within American Agamid lizards that small scales absorb heat better and reduce water loss, thus small scales have an advantage in cool and dry regions. Otherwise Thorpe & Baez (1987, 1993) registered that within the lizards Gallotia galloti from the Canarian Island Teneriffa and G. stehlini from Gran Canaria specimens originating from cooler and higher sites have larger scales. They assumed that scale size might depend on daily and annual temperature extremes and not on the average temperature. Finally, Horton (1972), in a study of Australian scincid lizards of the genus Egernia, found that not the scales themselves but the skin between them is relevant for the water economy. His data do no show a logical relation between scale size and regional temperature differences. Horton (1972) deduced the variation of scale pattern to a pleiotropic effect, involved in physiological adaptations to temperature and humidity. That means the scale pattern would not adapt to ecological conditions itself. Nevertheless, Schmidtler (1986) demonstrated a geographic variation parallel to climatic parameters of seven pholidosis-characters in Turkish green lizards of the genus Lacerta. In general, related forms have higher scale numbers in warmer, moister regions. I compared his data from Turkish populations with dice snake populations from the same areas (Mebert 1993). The dice snakes exhibited an opposite trend to the lizards. Schmidtler’s conclusions should be interpreted in the view that only one of his seven chosen characters has a relation with body surface, which might play a thermoregulatory role in climate adaptations. I do not doubt that climatic factors have their influence on scale characters within reptiles, but the conflicting results and interpretations previously presented suggest that many more factors have to be considered to solve this problem. Ultimately, the numbers of ventrals and subcaudals of dice snakes from the hot regions of Egypt, Near East and southern Iraq are similar to the ones in Italian and Switzerland, but the climate is not.

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Acknowlegements My sincere thanks go to G. Dusej, V. Ziswiler, N. Helfenberger, B. Schätti, C. Mauerhofer, H. Billing, and M. Henggeler, who all helped variously at some stage to accomplish this and related studies. References Baha el Din, S. (2011): Distribution and recent range extension of Natrix tessellata in Egypt. – Mertensiella 18: 401–402. Bannikov, A. G., Darevskii, I.S. & A.K. Rustamov (1971): Amphibians and Reptiles of the SSSR. - Publ. Mysl, Moscow (in Russian). Bannikov, A.G., Darevskii, I.S., Iszczenko, W.G., Rustamov, A.K. & N.N. Shcherbak (1977): Opredelitelj zemnowodrychi presmykajuscichsja fauny SSSR. (Identification of Amphibians and Reptiles of the SSSR). – Proswesenije, Moscow (in Russian). Baran, I (1976): Türkiye yilanlarinin taksonomik revizyonu ve cogafi dagilislari. – TBTAK Yayinlari No 309, T.B.A.G. Seri No 9, Ankara. Cafuta, V (2011): First report of melanistic dice snakes (Natrix tessellata) in Slovenia. – Mertensiella 18: 442. Calinescu, R. (1931): Contributiuni sistematice si zoogeografice la studiul amphibiilor si retilelor din Rominia. – Mem. Sect. Stint. Acad. rom. Bucuresti 7: 119–291. Dincaslan, Y.E., Arikan, H., Ugurtas, H.I. & K. Mebert (2011): Morphology and blood proteins of dice snakes from western Turkey. – Mertensiella 18: 370–382. Dowling, H.G. (1951): A proposed standard system of counting ventrals in snakes. – British Journal of Herpetology 1: 97–99. Fuhn, I.E. & S. Vancea (1961): Fauna Republici Romine. - Fauna Romine 14(2) Bucuresti. Fox, W., Gordon, D. & M.H. Fox (1961): Morphological effects of low temperatures during the embryonic development of the garter snake, Thamnophis elegans. – Zoologica 42(5): 57–71. Dürigen, B. (1897): Deutschlands Amphibien und Reptilien. – Magdeburg, Germany. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Guicking, D. & U. Joger (2011): A range-wide molecular phylogeography of Natrix tessellata. – Mertensiella 18: 1–10 Guicking, D., Joger, U. & M. Wink (2009): Cryptic diversity in a Eurasian water snake (Natrix tessellata, Serpentes: Colubridae): Evidence from mitochondrial sequence data and nuclear ISSR-PCR fingerprinting. – Organisms, Diversity & Evolution 9: 201–214. Hecht, G. (1930): Systematik, Ausbreitungsgeschichte und Őkologie der europäischen Arten der Gattung Tropidonotus (Kuhl) Boie H. − Mitteilungen aus dem Zoologischen Museum in Berlin 16: 244–393. Hellmich, W.C. (1951): On ecotypic and autotypic characters, a contribution to the knowledge of the evolution of the genus Liolaemus (Iguanidae). – Evolution 5(4): 359–369. Horton, D.R. (1972): Lizard scale and adaptation. – Syst. Zool. 21(4): 441–443.

Geographic Variation in Morphology of Natrix tessellata Kminiak, M. & S. Kaluz (1983): Evaluation of sexual dimorphism in snakes (Ophidia, Squamata) based on external morphological characters. – Folia Zoologica 32(2): 259–270. Kramer, E., Linder, A. & B. Mermillod (1982): Systematische Fragen zur europäischen Schlangenfauna. - Vertebrata Hungarica, TOM. XXI: 195-201. Laňka, V. (1978): Variabilität und Biologie der Würfelnatter (Natrix tessellata). – Acta Universitatis Carolinae, Biologica 1975– 1976: 167–207. Lenz, S. & M. Gruschwitz (1993): Zur Merkmalsdifferenzierung und -variation der Würfelnatter, Natrix tessellata (Laurenti 1768) in Deutschland. – Mertensiella 3: 269–300. Liu, Y., Mebert, K. & L. Shi (2011): Notes on distribution and morphology of the dice snake (Natrix tessellata) in China. – Mertensiella 18: 430–436. Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zurich, Switzerland. Mebert, K. (1996): Comparaison morphologique entre des populations introduites et indigènes de Natrix tessellata de l’Arc Alpin. – Bull. Soc. Herp. Fr. 80: 15–25. Mebert, K. (2010): Massive Hybridization and Species Concepts, Insights from Watersnakes. – VDM Verlag, Saarbrücken, Germany. Mebert, K. (2011a): Introduced and indigenous populations of the dice snake (Natrix tessellata) in the Central Alps – Microgeographic variation and effect of inbreeding. – Mertensiella 18: 71–79. Mebert, K. (2011b): Sexual dimorphism in the dice snake (Natrix tessellata). . – Mertensiella 18: 94–99. Mebert, K. (Ed.) (2011c): The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species. – Mertensiella 18, DGHT, Rheinbach, Germany. Mertens, R. (1969): Zur Synonymie und Variabilität der Würferlnatter (Natrix tessellata). – Senckenbergiana Biologica 50(3/4): 125–131. Naumov, B., Tzankov, N., Popgeorgiev, G., Stojanov, A. & Y. Kornilev (2011): The dice snake (Natrix tessellata) in Bulgaria: distribution and morphology. – Mertensiella 18: 288–297.

Rajabizadeh, M., Javanmardi, S., Rastegar-Pouyani, N., Karamiani, R., Yusefi, M., Salehi, H., Joger, U., Mebert, K., Esmaeili, H., Parsa, H., Gholi Kami, H. & E. RastegarPouyani. (2011): Geographic variation, distribution and habitat of Natrix tessellata in Iran. – Mertensiella 18: 414–429. RehÁk, I. (1992): Distribution, ecology and variability of snakes in Czecho-Slovakia. – Korsós, Z. & I. Kiss (Eds): Proc. Sixth Ord. Gen. Meet. – S.E.H., Budapest 1991: 383–388. Shcherbak, N.N. & M.I. Shcherban (1980): Amphibians and Reptiles of the Ukrainian Carpathians. – Naukova Dumka, Kiev (in Russian). Schätti, B. (1982): Bemerkungen zur Ökologie, Verbreitung und intraspezifische Variation der Vipernatter, Natrix maura (L. 1758). – Revue Suisse de Zoologie 89(2): 521–542 Schmidtler, J.F. (1986): Orientalische Smaragdeidechsen: 3. Klimaparallele Pholidosisvariation. – Salamandra 22(4): 242–258. Schreiber, E. (1912): Herpetologia Europaea (2. Auflage). – Fischer, Jena, Germany. Soulé, M. (1966): Trends in the insular radiation of a lizard. – Amer. Natur. 100(910): 47–64. Soulé & M. & W.C. Kerfoot (1972): On the climatic determination of scale size in a lizard. – Syst. Zool. 21(1): 97–105. Thorpe, R.S. & M. Baez (1987): Geographic variation within an island: univariate and multivariate contouring of scalation, size, and shape of the lizard Gallotia galloti. – Evolution 41(2): 256–268. Thorpe, R.S. & M. Baez (1993): Geographic Variation in scalation of the lizard Gallotia stehlini within the island of Gran Canaria. – Biological Journal of the Linnean Society 48(1): 75–87. Tuniyev, B., Tuniyev, S., Kirschey, T. & K. Mebert (2011): Notes on the dice snake, Natrix tessellata, from the Caucasian Isthmus. – Mertensiella 18: 343–356. Werner, Y.L. & T. Shapira (2011): A brief review of Morphological variation in Natrix tessellata in Israel: between sides, among individuals, between sexes, and among regions. – Turkish Journal of Zoology 35(4): 451–466. Zimmermann P. & G. Fachbach (1996): Verbreitung und Biologie der Würfelnatter, Natrix tessellata tessellata (Laurenti, 1768), in der Steiermark (Österreich). – Herpetozoa 8(3/4): 99–124.

Author Konrad Mebert, Siebeneichenstrasse 31, 5634, Merenschwand, Switzerland, e-mail: [email protected].

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MERTENSIELLA 18

20-29

20 September 2011

ISBN 978-3-9812565-4-3

Head Morphology and Diet in the Dice Snake (Natrix tessellata) Jonathan Brecko, Bart Vervust, Anthony Herrel & Raoul Van Damme Abstract. In aquatic natricine snakes, piscivorous species tend to have narrow streamlined heads, while species that prey on frogs have broader heads. This pattern is thought to reflect the antagonistic design requirements of fast underwater striking on the one hand and the consumption of bulky prey on the other. Here we test whether a similar correlation between head shape and diet exists at the intraspecfic level, by quantifying head shape and diet in the frontal striking aquatic natricine snake Natrix tessellata. Our results show that museum specimens with fish in their stomachs had significantly narrower and more streamlined heads than individuals with frogs in their stomachs. Given that diet is strongly determined by local abundance of potential prey, these results suggest strong population-level divergence in head size and shape in this species. Future studies need to establish whether the observed differences in head shape have a genetic basis, or result from phenotypic plasticity. Key words. Natrix tessellata, feeding, fish, frogs, prey capture, trade-off.

Introduction Aquatic natricine snakes have recently become a model system for studies of evolutionary convergence (Vincent et al. 2006a, 2009, Herrel et al. 2008). Previous studies have demonstrated convergent evolution of narrow streamlined heads in species of piscivorous natricines that use a frontal strike to capture prey (Alfaro 2002, Hibbits & Fitzgerald 2005, Herrel et al. 2008). As the hyoid bone is strongly reduced in snakes as a result of the specialization of the tongue for chemoreception (McDowell 1972, Schwenk 1994), snakes cannot use suction feeding to capture prey underwater. Consequently, it is predicted that frontally striking aquatic snakes should have streamlined heads to minimize drag and bow-waves induced by the forward movement of the predator (Vogel 1981, Young 1991, Herrel et al. 2008). Conversely, species specializing on bulky prey such as frogs and toads are often characterized by broad and wide heads (Forsman & Lindell 1993, Vincent et al. 2006b, Vincent & Mori 2008). As snakes cannot reduce their prey (but see Jayne et al. 2002), the maximum size of the prey eaten is a direct function of the size of the head of the snake (Pough & Groves 1983, Rodriguez-Robles et al. 1999, Cundall & Greene 2000, Vincent et al. 2006b) thus putting strong selective pressures on the evolution of wide heads. A trade-off between the ability of snakes to capture prey underwater using a forward strike mode and their ability to eat large, bulky prey is thus predicted (Herrel et al. 2008). While there is ample evidence for a relationship between prey type (fish versus frogs) and head shape across aquatic snake species, it is unclear whether a similar connection exists within a species (Snell et al. 1988, Losos & Irschick 1994, Herrel et al. 2001). Indeed, although an essential component of micro-evolutionary theory, empirical evidence for functional tradeoffs at the intraspecific level is scarce on the whole (Van

Damme et al. 2002). Here, we quantify head shape and diet in the aquatic dice snake, Natrix tessellata. The dice snake seems an appropriate study species because it is a piscivore (Luiselli & Rugiero 1991, Filippi et al. 1996, Gruschwitz et al. 1999, Luiselli et al. 2007, Ghira et al. 2009, Göçmen et al. 2011) that uses frontal strikes to capture prey underwater (Bilcke et al. 2006). And it has a well adapted visual system allowing it to better focus while submerged than in its congener N. natrix (Schaeffel & Mathis 1991). Moreover it is also known to eat frogs and other amphibians across parts of its range, although it is still unclear whether this happens frequently (Gruschwitz et al. 1999, Brecko & Herrel pers. obs.). Our personal observations on Greek Islands, e.g. Serifos, show that they probably consume almost exclusively amphibians due to annually drying up of streams and puddles, rendering the aquatic habitat not suitable for fish. We predict that individuals, whose diet predominantly consists of fish, will have narrower and more streamlined heads than individuals from populations including frogs in their diet. Materials and Methods Study Animals We measured snakes of the species Natrix tessellata contained in the following museums: Musée Nationale d’Histoire Naturelle in Paris, France; Forschungsmuseum Alexander Koenig in Bonn, Germany; Natural History Museum in London, UK; California Academy of Sciences in San Francisco, USA; The Field Museum in Chicago, USA; and the Senckenberg Institute in Frankfurt, Germany (see Appendix I). This resulted in a database with a total of 576 snakes. Specimen catalog numbers and locality data are listed in Appendix I. The animals measured were both juveniles and adults of both sex, however the specimens with a prey in their stomach

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Jonathan Brecko, Bart Vervust, Anthony Herrel & Raoul Van Damme

(and used for this paper) were all adults. We determined the sex of a subset of the animals by dissection of the cloacal region. Morphometrics We measured the snout-vent length (SVL) and tail length of all specimens using a measuring tape and a piece of string. Additionally, we measured the following characteristics of the head displayed in Figure 1: (1) head length, as the distance from the back of the skull (posterior edge of the parietal bone as determined by palpation) to the tip of the snout; (2) head width, measured at the widest part of the posterior cephalic region; (3) lower jaw length, as the distance between the posterior end of the compound bone and the tip of the dentary bone; (4) the distance from the corner of the mouth to the tip of the dentary bone; (5) head height, measured at the highest point of the head; (6) and quadrate length, defined as the length from the quadrate-lower jaw joint to the anterior dorsal most aspect of the quadrate at the quadrate-supratemporal joint. All these characteristics were measured using digital calipers (Mitutoyo; 0.01 mm). We also took digital pictures of the head in dorsal, ventral, lateral and frontal views on all specimens. A background grid was included for scaling purposes. The pictures were used to measure the surface area of the head in dorsal, ventral, lateral and frontal view with

the aid of the surface measurement tool in TpsDig 2.10 (Suny at Stony Brook). The lateral surface area was calculated by summing left and right side measurements and dividing by two, unless one of the sides showed any kind of unnatural deformation, in which case the measurement was based on one side only. On the pictures we also measured the inter-ocular and inter-nostril lengths, as the distance between the eyes and the distance between the nostrils (no. 7 and 8 on Figure 1, respectively). Diet We evaluated the presence of prey in the stomach by palpation. If prey were detected, a small incision through the abdominal scales and muscles was made to expose the stomach at the level of the prey. The stomach was opened and prey items were removed and stored in a 70% aqueous ethanol solution. After removing the prey from the stomach, pictures were taken of all prey for subsequent identification. Statistics We used SPSS (version 13.0, SPSS Inc., Chicago, IL, USA) for statistical analyses. All morphometric variables were Log10 transformed before analyses to ensure normality by eliminating the effect of allometric growth. To reduce the dimensionality, e.g. remove the effect of different size classes in the dataset, and to explore shape variation within species, unstandardized residuals of the regression of the cranial traits on SVL were used as input for a principal component analysis with varimax rotation. Factors with eigenvalues greater than 1 were extracted and used as input for subsequent analyses of variance testing for differences in head shape between snakes that had eaten frogs versus fish. Finally, Spearman rank correlations were used to test for associations between head shape and the number of prey retrieved from the stomach of each snake. We used discriminant analysis to predict the sex of the animals that were not dissected for sex determination. However we failed to obtain a large enough subset of animals with known/ predicted sex and with prey in their stomach. This made it impossible to statistically look for differences in head morphology between the sexes with ingested prey. Results

Fig. 1. Dorsal and lateral view of the head of a Natrix tessellata specimen, illustrating the morphometric variables determined on each specimen (see also text): (1) head length, (2) head width, (3) lower jaw length, (4) distance from corner of mouth to tip of dentary bone, (5) head height, (6) quadrate length, (7) inter-ocular length, (8) inter-nostril length.

Fifty-two out of the total 576 snakes examined had detectable prey in their stomachs. Of the individuals with prey in their stomachs, 19 had eaten frogs and 33 had eaten fish. The number of prey items per stomach varied between 1 and 9. Most of these specimens (n = 34) had one prey item in their stomach, 12 snakes contained remains of 2 or 3 prey items, and the others had swallowed 5, 6, 7, 8 and even 9 prey items. In the latter cas-

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Head Morphology and Diet in Natrix tessellata

es, prey typically consisted of small fish, tadpoles, and froglets, but occasionally also included small adult frogs and newts. None of the specimens examined contained both, amphibious and fish prey. Table 1 reports head and body characteristics of snake specimens that had eaten fish and amphibians, respectively. A principal component analysis on the regressed craniometric data produced two new composite axes that jointly explained approximately 75% of the total variation in the data set. Whereas the first axis was highly and positively correlated with the relative length of the head, the second axis was highly and positively correlated with the relative frontal surface area and the relative distance between the eyes and nostrils (Tab. 2). A plot of the individuals in multivariate space composed of the first two factors shows clear separation of individuals that had fish or frogs in their stomachs (Fig. 2). Head shape differed only between fish-eating and frog-eating individuals on the second axis (Univariate F-tests: Axis 1: F1,50 = 2.53, P = 0.12; Axis 2: F1, 50 = 6.85, P = 0.012); individuals that had fish in their stomachs re-

Tab. 2: Results of a factor analysis performed on the head morphometric data. Loadings greater than 0.8 are in bold. % variation explained eigenvalue residual head length (mm) residual head width residual head height residual lower jaw length residual jaw outlever residual quadrate length residual dorsal surface area residual frontal surface area residual lateral surface area residual ventral surface area residual interocular distance (mm) residual internasal distance (mm)

factor 1 44.49 7.64 0.80 0.70 0.72 0.87 0.85 0.84 0.69 0.39 0.43 0.51 0.25 0.12

factor 2 30.54 1.36 0.38 0.36 0.32 0.29 0.23 0.05 0.54 0.83 0.49 0.57 0.87 0.87

Tab. 1. Descriptive data representing head measurements in snakes with either fish or frogs in their stomach. Both absolute and relative (residuals of the regression of head lengths on SVL) dimensions are indicated. Descriptive Statistics Head length (mm) Head width (mm) Head height (mm) Lower jaw length (mm) Mouth-tip (mm) Quadratum (mm) Dorsal surface (mm²) Frontal surface (mm²) Lateral surface (mm²) Ventral surface (mm²) Distance nostrils (mm) Distance eyes (mm) SVL (cm) Tail length (cm)

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Prey Fish Frog Fish Frog Fish Frog Fish Frog Fish Frog Fish Frog Fish Frog Fish Frog Fish Frog Fish Frog Fish Frog Fish Frog Fish Frog Fish Frog

Mean 14,11 15,54 9,58 12,27 7,13 8,95 19,28 21,67 11,05 12,34 5,66 6,70 159,64 240,13 82,86 135,70 106,58 143,63 139,37 209,83 4,43 5,34 6,46 8,04 39,06 45,16 10,41 10,69

Absolute

SE 0,72 1,15 0,61 1,08 0,46 0,94 1,16 1,71 0,69 1,00 0,45 0,77 19,70 42,87 10,94 23,91 13,37 25,89 19,23 39,71 0,31 0,47 0,41 0,66 3,08 3,74 0,90 1,15

Mean -0,006 -0,014 -0,017 0,023 -0,008 0,012 0,002 -0,004 -0,004 -0,014 -0,006 -0,024 -0,025 0,011 -0,041 0,020 -0,027 -0,036 -0,060 -0,031 -0,022 -0,002 -0,030 0,007

Relative

SE 0,007 0,010 0,010 0,013 0,009 0,017 0,008 0,011 0,010 0,014 0,014 0,016 0,015 0,028 0,019 0,034 0,015 0,028 0,020 0,028 0,010 0,019 0,009 0,016

Jonathan Brecko, Bart Vervust, Anthony Herrel & Raoul Van Damme

Fig. 2. Graph illustrating the results of a factor analysis performed on the size-corrected craniometric data. Note that individuals with fish in their stomachs (closed circles) exhibit relatively narrower snouts than individuals with frogs in their stomachs (open circles).

vealed narrower snouts (smaller distance between the eyes and nostrils) and a reduced frontal surface area (Figs. 2, 3). Scores on the first principal component axis correlated with the number of prey found in the stomach (Spearman r = -0.413; P = 0.001). Thus snakes that had more prey in their stomachs had relatively shorter heads. We do not have enough data to statistically test for differences in head morphology between populations of which the diet is known. But we placed the data for the head morphology (PCA axis 2, Fig. 4) against the population information together with the known diet of individuals for that region. The two out of five populations with on average the widest head shape and four

Fig. 4. Graph illustrating the results of the second axis of the factor analysis performed on the craniometric data against the locality data. Illustrated are the top five populations with the on average largest frontal head shape and the on average smallest frontal head shape. The triangles with the top upward are populations that have fed on frogs. The downward positioned triangles are populations that have fed on fish. The circles represent populations without a known diet. There is a trend that populations with on average a larger frontal head shape feed on frogs, whereas the populations with the smallest frontal head shape feed on fish.

out of five populations with the most narrow head shape appear to be feeding on frog and fish respectively. The other populations had no individuals with any stomach contents, so their diet remains unclear. Discussion

Fig. 3. Plot illustrating the difference in head shape between snakes that had fish and frogs in their stomachs. Snakes feeding on fish have significantly narrower snouts than snakes feeding on frogs. Illustrated are means ± standard errors.

Our results show that individuals that consumed fish had more streamlined heads than individuals with frogs in their stomachs (see Fig. 5). These data thus confirm prior suggestions that striking at prey frontally under water may impose a constraint on the evolution of head shape in these snakes. Although we predicted that individuals who consumed frogs would have a larger relative head width as principal determining factor, our results show that inter-ocular length and projected frontal surface play a more important role. The larger projected frontal surface of the head may increase drag during striking and swimming of the frog eating specimens. It would therefore be interesting to compare the underwater striking performance and gape distance of dice snakes selecting between the two types of prey, as well as their habitat use and behavior. If these intraspecific differences in morphology mirror those found among Natricine species, we predict that specimens with relatively large frontal surfaces will be found in drier habi-

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Head Morphology and Diet in Natrix tessellata

Fig. 5. Illustration of the two extreme head morphologies observed in Natrix tessellata utilizing different prey. Specimen A with only fish in its stomach differs significantly in head shape from specimen B which had eaten only frogs.

tats and engage less in swimming than their streamlined conspecifics. Further investigations using geometric morphometric techniques based on pictures taken from live animals may be especially insightful in determining differences in shape. Overall, projected frontal surface may be constrained in aquatic snakes for energetic reasons as narrow heads may improve a snake’s hydrodynamic profile and minimize drag while swimming under water (see Hibbits & Fitzgerald 2005). If so, this may explain why aquatic snakes are generally characterized by an extreme elongation of the quadrate as this would provide them with a performance advantage for eating large prey (Vincent et al. 2009) and at the same time would allow them to maintain a streamlined head shape. However, measurements of the energetic cost of locomotion in snakes with different head shapes are needed to explicitly test this hypothesis. Despite the fact that our data for Natrix tessellata suggest a constraint on head shape in snakes that use frontal strikes to capture prey underwater, it is known that other species characterized by much wider heads do also prey on fish (e.g. Natrix maura: Pleguezuelos & Moreno 1989, Santos & Llorente 1998, Schätti 1999, Santos et al. 2000, Agkistrodon piscivorous: Vincent et al. 2004a, b, 2005). Previous works on aquatic prey capture in snakes have suggested an important role of behavioral strategies that may mitigate the constraints imposed by striking at prey in a dense medium like water (Drummond 1983, Hailey & Davies 1986, Alfaro 2002, Bilcke et al. 2006). Alternatively, snakes with wide heads may just suffer from a highly reduced strike performance (Vincent et al. 2005, Bilcke et al. 2007) and only prey on small fish when present in high densities (Hailey & Davies 1986) as observed in drying water bodies during the summer (Savitzky 1992, Schätti 1999). Our dietary dataset was not large enough to take into account differences between the sexes and look statistically at population differences in diet and head shape. However there appeared to be no difference between

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the number of females and males with frog or fish in their stomach as they preyed upon fish and frogs in equal numbers, but the overall number was too small to statistically determine differences between the sexes. Other work on a larger morphological dataset of Natrix tessellata did not show any differences between the sexes (Brecko et al., submitted). However, significant intersexual differences in prey composition, with the females taking more anurans than males have been found at three sites in central Italy (Luiselli et al. 2007, Capula et al. 2011). Preliminary results on population differences show a trend of populations with a large mean frontal surface and distance between the eyes and nostrils feeding on frogs, whereas those with a small overall frontal surface tend to feed on fish (Fig. 5). This conclusion is supported by further observations. For example, Esterbauer (1985, 1994) observed that frogs are commonly, but not exclusively, consumed by N. tessellata in southwestern Syria, in the same general area of large-headed population at Lake Tiberiade (Fig. 5). The slender head morphology suggesting a fish diet in specimens from Lake Garda in Figure 5 is supported by Mebert (1993, 1996), who captured nearly 100 N. tessellata from this lake for a morphological study and retrieved serveral dozens of fish, but not a single amphibian from the snake stomachs. On the other hand, we did not find populations in which individuals have a mixed diet, although this occurs to a low proportion also in predominantly fish-eating populations (e.g. Luiselli et al. 2007, and refs. in Mebert 2011). The question remains if the individuals or populations which have an average overall frontal surface will prey upon both frogs and fish in equal numbers. It would therefore be interesting to look at the habitat and behavior of the ‘large headed’ N. tessellata’s. It can be predicted that, as the main preferred prey of N. tessellata is fish (Gruschwitz et al. 1999, Schätti 1999), the habitat of large headed frog eating N. tessellata’s is completely different from the normal situation. Perhaps the environment is drier, with streams and puddles only periodically maintaining water, resulting that

Jonathan Brecko, Bart Vervust, Anthony Herrel & Raoul Van Damme

fish do not exist in the habitat, or frogs are simply more numerous (e.g. Esterbauer 1985, 1994). Interpopulational differences in head morphology have been documented in many snakes (e.g. Forsman 1991, Aubret et al. 2004). Also in Natrix tessellata Mebert (1993, 1996) found significant microgeographic variations in the posterior head length (distance between eye and mouth corner) and width of frontal shield between populations of approximately 30 km distance in mountainous terrain. However, no diet analysis has accompanied that study. Future studies testing whether the observed differences in head shape observed between individuals and/or populations have a genetic basis or are the result of phenotypic plasticity are warranted as plasticity has been suggested as an important mechanism driving the initial divergence of populations in the face of changing ecological conditions in squamates (Losos 2000, Aubret et al. 2004). Acknowledgements We would like to thank the curators of the museums that allowed us to visit the collections and for their assistance during our stay at the different museums. We are especially grateful to the Field Museum of Natural History and the Californian Academy of Sciences who made a visit possible by means of a grant of the Scholarship Committee (FM) and a Charles Stearns Memorial Grant in Aid in Herpetology (CAS). JB is funded by a Ph.D. grant of the Instituut voor de Aanmoediging van Innovatie door Wetenschap en Technologie in Vlaanderen (Institute for the Promotion of Innovation by Science and Technology in Flanders). References Alfaro, M.E. (2002): Forward attack modes of aquatic feeding garter snakes. – Functional Ecology 16: 204–215. Aubret, F., Shine, R. & X. Bonnet (2004): Adaptive developmental plasticity in snakes. – Nature 31: 261–262. Bilcke, J., Herrel, A. & P. Aerts (2007): Effect of prey- and predator size on the capture success of an aquatic snake. – Belgian Journal of Zoology 137: 191–195. Bilcke, J., Herrel, A. & R. Van Damme (2006): Correlated evolution of aquatic prey capture strategies in European and American Natricine snakes. – Biological Journal of the Linnean Society 88: 73–83. Capula, M., Filippi, E., Rugiero, L. & L. Luiselli (2011): Dietary, thermal and reproductive ecology of Natrix tessellata in central Italy: A Synthesis. – Mertensiella 18: 147–153. Cundall, D. & H.W. Greene (2000): Feeding in snakes. – In: SCHWENK, K. (Ed.): Feeding: Form, Function and Evolution in Tetrapod Vertebrates. – Academic Press, London: 293–333. Drummond, H. (1983): Aquatic foraging in garter snakes: a comparison of specialists and generalists. – Behaviour 86: 1–30. Esterbauer, H. (1985): Zur Herpetofauna Südwestsyriens. – Herpetofauna 7: 23–34.

Esterbauer, H. (1994): Lebensweise und Verhalten der Würfelnatter im Masil al Fawwar (Syrien). – DATZ 47: 308–311 Filippi, E., Capula, M., Luiselli, L. & U. Agrimi (1996): The prey spectrum of Natrix natrix (Linnaeus, 1758) and Natrix tessellata (Laurenti, 1768) in sympatric populations (Squamata: Serpentes: Colubridae). – Herpetozoa 8: 155–164. Forsman, A. (1991): Adaptive variation in head size in Vipera berus L. populations. – Biological Journal of the Linnean Society 43: 281–296. Forsman, A. & L.E. Lindell (1993): The advantage of a big head: swallowing performance in adders, Vipera berus. – Functional Ecology 7: 183–189. Ghira, I., Butănescu, D. & B. Marosi (2009): Feeding behavior of the dice snake (Natrix tessellata). – Herpetologica Romanica 3: 1–7. Göçmen, B., Çiçek, K., Yildiz, M.Z., Atatür, M.K., Dinçaslan Y.E. & K. Mebert (2011): A preliminary study on the feeding biology of the dice snake, Natrix tessellata, in Turkey. – Mertensiella 18: 365–369. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581–644. Hailey, A. & P.M.C. Davies (1986): Diet and foraging behavior of Natrix maura. – Herpetological Journal 1: 53–61. Herrel, A., Meyers, J.J. & B. Vanhooydonck (2001): Correlations between habitat use and body shape in a phrynosomatid lizard (Urosaurus ornatus): a population-level analysis. – Biological Journal of the Linnean Society 74: 305–314. Herrel, A., Vincent, S.E., Alfaro, M.E., Van Wassenbergh, S., Vanhooydonck, B. & D.J. Irschick (2008): Morphological convergence as a consequence of extreme functional demands: examples from the feeding system of natricine snakes. – Journal of Evolutionary Biology 21: 1438–1448. Hibbits , T.J. & L.A. Fitzgerald (2005): Morphological and ecological convergence in two natricine snakes. – Biological Journal of the Linnean Society 85: 363–371. Jayne, B., Voris, H.K. & P.K.L. Ng (2002): Herpetology: Snake circumvents constraints on prey size. – Nature 418: 143–143. Losos, J.B. (2000): Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. – Evolution 54: 301–305. Losos, J.B. & D.J. Irschick (1994): Adaptation and constraint in the evolution of specialization of Bahamian Anolis lizards. – Evolution 48: 1786–1798. Luiselli, L., Capizzi, D., Filippi, E., Anibaldi, C., Rugiero, L. & M. Capula (2007): Comparative diets of three populations of an aquatic snake (Natrix tessellata, Colubridae) from Mediterranean streams with different hydric regimes. – Copeia 2007: 426–435. Luiselli, L. & L. Rugiero (1991): Food niche partitioning by water snakes (genus Natrix) at a freshwater environment in Central Italy. – Journal of Freshwater Ecology 6: 439–444. McDowell, S.B. (1972): The evolution of the tongue of snakes and its bearing on snake origins. – In: Dobzhansky, T., Hecht, M.K. & W.C. Steere (Eds.): Evolutionary Biology, Vol. 6. Appleton-Century-Crofts, New York: 191–273

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Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Mebert, K. (1996): Comparaison morphologique entre des populations introduites et indigenes de Natrix tessellata de I’Arc Alpin. – Bull. Soc. Herp. Fr. 80: 15–25. Mebert, K. (Ed.) (2011): The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species. – Mertensiella 18, DGHT, Rheinbach, Germany. Pleguezuelos, J.M. & M. Moreno (1989): Alimentacion primaveral de Natrix maura (Linneaus, 1758) (Ophidia, Colubridae) en el S.E. de la Peninsula Iberica. – Revista Espanola De Herpetologia 3: 221–236. Pough, F.H. & J.D. Groves (1983): Specializations of the body form and food habits of snakes. – American Zoologist 23: 443–454. Rodriguez-Robles, J.A., Bell, C.J. & H.W. Greene (1999): Gape size and evolution of diet in snakes: feeding ecology of erycine boas. – Journal of Zoology 248: 49–58. Santos, X. & G.A. Llorente (1998): Sexual and size-related differences in the diet of the snake Natrix maura from the Ebro Delta, Spain. – Herpetological Journal 8: 161–165. Santos, X., Gonzalez-Solis, J. & G.A. Llorente (2000): Variation in the diet of the viperine snake Natrix maura in relation to prey availability. – Ecography 23: 185–192. Savitzky, B.A.C. (1992): Laboratory studies on piscivory in an opportunistic predator, the cottonmouth, Agkistrodon piscivorus. - In: Campbell, J.A. & E.D. Brodie, Jr. (Eds.): Biology of the Pitvipers. – The University of Texas at Arlington Press, USA: 347–368. Schätti, B. (1999): Natrix maura (Linnaeus 1758) - Vipernatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 483–503. Schaeffel, F. & U. Mathis (1991): Underwater vision in semi-aquatic European snakes. – Naturwissenschaften 78: 373–375. Schwenk, K. (1994): Why do snakes have forked tongues? – Science 263: 1573–1577.

Snell, H.L., Jennings, R.D., Snell, H.M. & S. Harcourt (1988): Intrapopulation variation in predator-avoidance performance of Galápagos lava lizards: the interaction of sexual and natural selection. – Evolutionary Ecology 2: 353–369. Van Damme, R., Vanhooydonck, B., Aerts, P. & F. De Vree (2002): Evolution of lizard locomotion: context and constraint. – In: Bels, V., Gasc, J.P. & A. Casinos (Eds.): Vertebrate Biomechanics and Evolution. – BIOS Scientific Publishers, Oxford: 267–282. Vincent, S.E. & A. Mori (2008): Determinants of feeding performance in free-ranging pit-vipers (Viperidae: Ovophis okinavensis): key roles for head size and body temperature. – Biological Journal of the Linnean Society 93: 53–62. Vincent, S.E., Brandley, M.C, Herrel, A. & M.E. Alfaro (2009): Convergence in trophic morphology and feeding performance among piscivorous natricine snakes. – Journal of Evolutionary Biology 22: 1203–1211. Vincent, S.E., Dang, P.D., Herrel, A. & N.J. Kley (2006a): Morphological integration and adaptation in the snake feeding system: a comparative phylogenetic study. – Journal of Evolutionary Biology 19(5): 1545–1554. Vincent, S.E., Herrel, A. & D.J. Irschick (2004a): Sexual dimorphism in head shape and diet in the cottonmouth snake (Agkistrodon piscivorus). – Journal of Zoology 264: 53–59. Vincent, S.E., Herrel, A. & D.J. Irschick (2004b): Ontogeny of intersexual head shape and prey selection in the pitviper Agkistrodon piscivorus. – Biological Journal of the Linnean Society, 81: 151–159. Vincent, S.E., Herrel, A. & D.J. Irschick (2005): Aquatic versus terrestrial strike performance and kinematics in the pitviper, Agkistrodon piscivorus. – Journal of Experimental Zoology 303: 476–488. Vincent, S.E., Moon, B.R., Shine, R. & A. Herrel (2006b): Functional meaning of “prey size” in water snakes (Nerodia fasciata, Colubridae). – Oecologia 147: 204–211. Young, B.A. (1991): The influences of the aquatic medium on the prey capture system of snakes. – Journal of Natural History 25: 519–531. Vogel, S. (1981): Life in Moving Fluids. – Willard Grant Press, Boston, USA.

Authors Jonathan Brecko, Bart Vervust, Konrad Mebert, Raoul Van Damme, Dept. Biology, University of Antwerp, Universiteitsplein 1, B-2610 Antwerp, Belgium, e-mail: [email protected]; Anthony Herrel, UMR 7179 C.N.R.S/M.N.H.N., Département d’Ecologie et de Gestion de la Biodiversité, 57 rue Cuvier, Case postale 55, 75231, Paris Cedex 5, France.

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Appendix I MNHN Paris Catalog No. **25*44 **25*51-3 **25*54 (A-Q) **35*350-2 **8501 *84*155 1925.47 1925.49-50 1926.32-6 1935.347 1935.349 1961.381 1963.1008 1990.4602 1991.1622-4 1991.1626 1991.1646-7 1991-1658 3177 (A-B) 5639 5645 6181 6185 (A-B) 641-2 6469-70

  Yamouné, Syria Ataïbe, Syria Ataïbe, Syria Hama, Syria Batoum, Russia Serpilor, Ukraine Ataïbe, Syria Ataïbe, Syria Smyrne, Turkey Iraq Hama, Syria Bologna, Italy Peloponnese, Greece Bologna, Italy Lake Tiberiade, Syria Lake Tiberiade, Syria Ataïbe, Syria Lake Gotscha, Armenia Dalmatia, Croatia Caspian Sea Caspian Sea Lake Gotscha, Armenia Lake Gotscha, Armenia Serpilor, Ukraine Lake Tiberiade, Syria

ZFMK Bonn Catalog No. 7570-9 7585-89 7590-623 7625-37 9921-4 9928-35 13930 15685-6 19186

  Po Delta, Italy Beysehir, Turkey Antalya, Turkey Antalya, Turkey Sweti Thoma, Bulgaria Sweti Thoma, Bulgaria Bireçik, Turkey Shiraz, Iran Pescasseroli, Italy

ZFMK Bonn Catalog No. 21012-7 23287-9 23295-9 24681-3 25712-3 27537 31611-13 31750-1 34668 38508 41225 41550 41986-8 42803-4 44057 46977 49130-2 49134-7 49139-41 51888 53037-8 54789 56869 62501-2 64942-4 71561 71563-5 71682-3 76326-8 82106 82108 82114-5 83031-4 84048-50 84053 MKHTG

  Lake Homs, Syria Bad Kreuznach, Germany Peloponnese, Greece Trient, Italy Lake Homs, Syria Nahr-el-Kabir, Syria Shiraz, Iran Bad Kreuznach, Germany LHbN, Germany Bireçik, Turkey S-Tirol, Italy RPL, Germany Lake Prespa, Greece North Syria North Syria Sile, Turkey LHbN, Germany LHbN, Germany LHbN, Germany Sivas, Turkey Terracina, Italy Castiglione del Lago, Italy Hatay, Turkey Peloponnese, Greece Djebel Druz, Syria Mazanderan, Iran Mazanderan, Iran Peloponnese, Greece Peloponnese, Greece Peloponnese, Greece Peloponnese, Greece Peloponnese, Greece Peloponnese, Greece Peloponnese, Greece Messenien, Greece Turkey

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Head Morphology and Diet in Natrix tessellata

NHM London Catalog No. 1908.8.7.20-1 1909.4.20.37-45 1915.12.28.35-37 1919.12.19.4-5 1919.7.18.3-5 1937.7.2.22-33 1955.1.11.25-9 1957.1.13.11-4 1969.2602-8 1970.1433-4 1980.1963-5 60.3.19.1285 60.3.19.1288-9 60.3.19.1330 79.8.15.32 90.5.17.8 95.12.28.16

  Caspian Sea Ataïbe, Syria Smyrna, Turkey Basra, Iraq Basra, Iraq Lake Huleh, Israël Tripoli, Libia Armioun, Libanon Bijar, Kurdistan Bosnia-Herzegovina Boracko Jezero, FJR Iraq Iraq Jeruzalem, Israël Caspian Sea Iraq Smyrna, Turkey

The Field Museum Catalog No. 19502 19513 19517 19522 19525-7 19529-30 19532-5 19537-44 19546-50 19552-66 19569 19572-3 19581 19594 19598 19622 20856 20893

  Iraq Iraq Iraq Iraq Iraq Iraq Iraq Iraq Iraq Iraq Iraq Iraq Palestine Mozul, Iraq Mozul, Iraq Iraq Iraq Persia

28

The Field Museum Catalog No. 20896-907 20909-11 20914-5 20917-8 20920-1 20925 20930-1 20935 20937-8 20941-2 20944-7 20949 20952-5 20957 20964-7 21908 22720-2 22809 25324 25326 26352-4 26359-60 26372-73 26373 26377 26380 26382 26387 26389 48508 72116 74413-5 74611 75285 75287-8 79163-70 130811-6 134379

  Persia Persia Persia Persia Persia Persia Persia Persia Persia Persia Persia Persia Persia Persia Persia Palestine Iraq S-Tirol, Austria Syria Syria Iraq Persia Iraq Iraq Iraq Iraq Iraq Iraq Iraq Palestine Gharbîya, Egypt Israël Lebanon Gharbîya, Egypt Damietta, Egypt Izmir, Turkey Iran Romania

Jonathan Brecko, Bart Vervust, Anthony Herrel & Raoul Van Damme

The Field Museum Catalog No. 141607 141618 141653 141655 141657 141660 141662-3 141668-9 141671 161112 161180 161204 171217-8 171220-26 171228-9 171232 171234-6 171238-9 171241 171243 171245 171247-8 200215-25 234281-2

Mazanderan, Iran Iran Iran Iran Khorassan, Iran Fars, Iran Fars, Iran Fars, Iran Fars, Iran Afghanistan Afghanistan Afghanistan Iran Iran Kurdistan Iran Iran Iran Iran Iran Iran Iran Kant Co, Kirgisia Former USSR

CAS San Francisco Catalog No. 17086 55190 87424 105192-202 105607 105755-6 105795-6 105825 111687-92 115972 119972

  Styria, Austria Austria Tantura, Israël Antalya, Turkey Hopa, Turkey Igdir, Turkey Dogubayazit, Turkey Pülümür, Turkey Ardesen, Turkey Pagman, Afghanistan Ardi, Turkey

CAS San Francisco Catalog No. 147589 157112-3 167859-60 167863-77 168038-45 170295 CAS 180050 CAS 182698-700 CAS 182854 CAS 182971-74 CAS 183087-94 CAS 183095-102 CAS 183103-112 CAS 183113-117 CAS 183118-122 CAS 185158 CAS 185292-316 CAS 192900-1 CAS 197118-21 CAS 197139 CAS 210871-2 CAS 215245 CAS 217585-99 CAS 217742 CAS 218068 CAS 218242-4 CAS 219929

Asraq, Jordania Alkut, Iraq Konqi River, China Konqi River, China Konqi River, China Gorna Brezica, Bulgaria Ashgabad, Turkmenistan Tersko-Kumskaya, Russia Kumtorkala, Dagestan Chambaylyk, Russia Stansstad, Swiss Brienzersee, Swiss Genfersee, Swiss Albogassio, Swiss Lake Garda, Italy Ashgabad, Turkmenistan Astrakhan, Russia Tersko-Kumskaya, Russia Korla, China Yining, China Kresna-Hancheto, Bulgaria Primorsko, Bulgaria Gelinkaya, Turkey Kortukeli, Turkey Haran, Turkey Kilis, Turkey Ropotamo river, Bulgaria

NHMS Frankfurt Catalog No. 52771

  Serpilor, Ukraine

29

MERTENSIELLA 18

30-38

20 September 2011

ISBN 978-3-9812565-4-3

Ergebnisse eines bundesweiten Projektes zur Förderung der Würfelnatter-Populationen und ihrer Lebensräume Sigrid Lenz & Almuth Schmidt Zusammenfassung. Im Rahmen eines Erprobungs- und Entwicklungsvorhabens wurden in den Jahren 1997 bis 2001 verschiedenste Massnahmen zur Förderung der deutschen Populationen und Lebensräume der Würfelnatter (Natrix tessellata) an den Flüssen Mosel, Lahn und Elbe getestet. An der Elbe wurde, nach Prüfung und ggf. Verbesserung der vorhandenen Habitatfaktoren, ein Wiederansiedlungsversuch am ehemals besiedelten Standort gestartet. Mittels Wasserbau- und Pflegemassnahmen wurden die Lebensräume an Lahn und Mosel entwickelt und vergrössert. Um ein Verbundsystem an der Lahn zu etablieren wurden zwei Gründerpopulationen initiiert. Zur Vermeidung des Strassentodes wurden Leiteinrichtungen erprobt. Summary. In a testing and development project carried out from 1997 to 2001, different measures were conducted on the rivers Mosel, Lahn and Elbe to protect and support the populations and habitats of the dice snake (Natrix tessellata). On the river Elbe, a once occupied habitat was examined and after improving its formerly suboptimal factors, captive bred hatchlings were reintroduced. On the river Lahn, open gravel areas were recreated and two new founder-populations were started. By reconstruction of the watercourse and reconfiguration of the landscape, the available habitat was considerably extended on the banks of the river Mosel. To avoid road-kills different guidance and deflection systems were tested. Key words: Natrix tessellata, habitat improvement, reintroduction, follow-up control

Einleitung

Projektgebiete und Zielsetzung

In den wärmebegünstigten Flusstälern von RheinlandPfalz bestehen einzelne Reliktpopulationen der Würfelnatter (Natrix tessellata), die nördlich des mitteleuropäischen Verbreitungsareals isoliert sind (vgl. Abb. 1). Nachdem die Art entlang des Rheins spätestens zu Beginn des 19. Jahrhunderts ausgestorben ist (vgl. Gruschwitz 1985), sind die Vorkommen an seinen Nebenflüssen Lahn, Mosel und Nahe verinselt (vgl. Abb.  2). Die Bestände und geeigneten Habitate sind in den letzten Jahrzehnten deutlich zurückgegangen (vgl. Gruschwitz et al. 1999) und nach wie vor stark gefährdet. Die Würfelnatter gilt daher in Deutschland als „vom Aussterben bedroht“ (Bitz & Simon 1996, Kühnel et al. 2009). Bis in die 1950er Jahre bestand zudem eine isolierte Population an der Elbe bei Meißen (Zimmermann 1910), die aufgrund zunehmender Gewässerverschmutzung, damit einhergehender Fischsterben und des ufernahen Strassenbaus ausstarb (Obst 1976, 1990). Im Jahr 1997 wurde vor dem Hintergrund der starken Gefährdung von Flussauenbiotopen und ihrer Leitart Würfelnatter ein vierjähriges Erprobungs- und Entwicklungsvorhaben (E+E-Projekt) modellhaft für bedrohte Reptilienarten an Bundeswasserstrassen gestartet. Der Schwerpunkt lag dabei auf der Entwicklung und Erprobung praktischer Schutzmassnahmen für die Würfelnatterpopulationen an Mosel, Lahn und Elbe, ihre charakteristische Begleitfauna und ihre Lebensräume (Lenz et al. 2006).

Die Zielsetzung basierte auf den aktuellen und auch historischen Voraussetzungen der Standorte. Mosel: Natrix tessellata war bis zum Beginn des 19. Jahrhunderts an der Unter- und Mittelmosel weit verbreitet (Noll 1888, Le Roi & Reichensperger 1913, Hecht 1929). Durch verschiedenartige gravierende Eingriffe (u.a. Bau uferparalleler Strassen, Trockenlegung von

Abb. 1. Verbreitung der Würfelnatter, die deutschen Populationen sind markiert (Rheinland-Pfalz – roter Pfeil, Meißen – schwarzer Pfeil), aus Lenz et al. (2008). Distribution of the dice snake, the German populations are marked (Rhineland-Palatinate – red arrow, Meißen – black arrow) from Lenz et al. (2008).

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Sigrid Lenz & Almuth Schmidt

Abb. 3: Ehemaliges Campingplatz-Gelände an der Mosel vor der Umgestaltung, Zustand 1993. Former camping site at the river Mosel prior its restructuring, state 1993. Foto: S. Lenz

kehr auf einer angrenzenden Bundesstrasse zu schützen (vgl. Abb. 3). Abb. 2. Verbreitung der Würfelnatter in Rheinland-Pfalz (verändert nach Gruschwitz 1985) Distribution of the dice snake in Rhineland-Palatinate (modified after Gruschwitz 1985).

Lahn: Auch an diesem Fluss bestand historisch ein flächiges Vorkommen am Unter- und Mittellauf (u.a.

Bunenfeldern) in die Uferstrukturen und besonders den Ausbau zur Bundeswasserstrasse in den 60er Jahren wurde das Vorkommen der Würfelnatter auf eine kleine Reliktpopulation am Unterlauf reduziert (Gruschwitz 1978, 1985, vgl. Abb. 2). Ziel war es hier, den Lebensraum der Art durch die naturnahe Umgestaltung einer angrenzenden, vormals als Campingplatz genutzten Fläche, zu erweitern und gleichzeitig gegen den Ver-

Abb. 4. Planskizze zur Gestaltung der Erweiterungsfläche an der Mosel (Karte H. Burger). Plan for habitat extension on the river Mosel (plan: H. Bur­ ger).

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Nationwide Support for the Dice Snake in Germany

Abb. 5. (oben) Anlage einer grossflächigen Bucht an der Mosel; (unten) Teilbereiche der ehemaligen Uferbefestigung bleiben als Vorschüttung erhalten. (above) Establishment of a large indentation in the banks of the river Mosel, (below) parts of the former embarkments are retained. Foto: S. Lenz

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Abb. 6: An der Lahn wurde ein Schwimmbagger eingesetzt um die Uferstrukturen zu verbessern. On the river Lahn a swimming dredge was used to improve the structures oft he river bank. Foto: A. Herzberg

Abb. 7. Leit- und Abweissystem zur Minimierung des Strassentodes von Würfelnattern. Guidance and deflection system to prevent road kills of dice snake. Foto: S. Lenz

Kirschbaum 1858, Noll 1869, Hecht 1929, Mertens 1947), von dem aktuell nur die am weitesten flussaufwärts gelegene Population im Unterwasser eines Wehres übrig geblieben ist (u.a. Lenz & Gruschwitz 1993). Da der Neubau dieses Wehres und damit die Beeinträchtigung oder auch der Verlust des einzigen Lebensraums bevorstand, sollte ein System von Trittsteinen entlang des Flusslaufes entstehen, begleitet von Wiederansiedlungsversuchen an zwei Standorten (vgl. auch Herzberg & Schmidt 2001).

Pflegemassnahmen

Elbe: Bei Meißen waren Vorkommen der Würfelnatter bis in die 1950er Jahre bekannt (Obst 1976), die dann wahrscheinlich durch den Bau ufernaher Strassen, Uferbegradigung, zunehmende Gewässerverschmutzung u.ä. erloschen. Auch hier handelte es sich um eine isolierte Reliktpopulation (vgl. Abb. 1); weiter südlich bestehen Vorkommen entlang der Elbe in der Tschechischen Republik (vgl. Gruschwitz et al. 1999). Seit der deutschen Wiedervereinigung 1989 wurden verstärkt Bemühungen zur Verbesserung der Wasserqualität und der Gewässerstrukturen an der Elbe unternommen, so dass zu Projektbeginn am ehemals besiedelten Standort bei Meißen wieder gute Lebensbedingungen für die Würfelnatter entstanden waren. Nach eingehender Prüfung und ggf. Optimierung der Habitatfaktoren wie Nahrungsressourcen, Winterquartiere, Gefährdungen usw. sollte hier ein Wiederansiedlungsversuch mit Tieren gleicher biogeographischer Herkunft erfolgen. Massnahmen Entsprechend der Zielsetzung wurde für jeden Standort ein spezielles Massnahmenpaket erarbeitet, konzipiert und umgesetzt. Zusammenfassend stellten sich die Massnahmen wie folgt dar:

An allen Standorten wurden gezielt Uferabschnitte in exponierter Lage freigestellt. Diese Pflegemassnahmen dienten an allen Standorten der Optimierung der bereits (abschnittweise) besiedelten Habitate oder auch der Schaffung neu zu erschliessender „Trittstein-Lebensräume“, die die Ausbreitung der Bestände entlang des Flusslaufs fördern sollten. Ziel war es dabei immer die Beschattung ufernaher Freiflächen und Flachwasserzonen sowie von Winterquartieren zu minimieren. Zusätzlich wurden potenzielle Eiablagesubstrate in Form von Schnittguthaufen eingebracht, aber auch Pferdemist mit hohem Strohanteil – ein Material, das an einigen Standorten seit Jahren zur Eiablage der Würfelnatter genutzt wird (Lenz & Gruschwitz 1992). Umgestaltung der Uferlinie Mit Hilfe wasserbaulicher Massnahmen wie dem Ausheben strömungsberuhigter Buchten, z.T. auch mit vorgelagerten Wellenbrechern, der Abflachung der Ufer an der Wasserlinie, der Schaffung dauerhafter Sonnenund Versteckplätze usw. wurden Lebensräume erweitert oder auch gänzlich neu gestaltet. An der Mosel wurde nach vorausgehender wasserbaulicher Planung und Genehmigung das rechte Ufer auf einer Länge von 270 m vollständig neu profiliert, um in dieser Kiesaue den vorhandenen Lebensraum einer im Bestand rückläufigen Würfelnatterpopulation zu erweitern und zu optimieren (Lenz & Schmidt 2002, vgl. Abb. 4 u. 5). An der Lahn wurden mittels eines Schwimmbaggers kleinräumig Buchten und Flachufer angelegt, um in Kombination mit den Pflegemassnahmen Trittsteinhabitate zu schaffen (vgl. Abb. 6)

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Nationwide Support for the Dice Snake in Germany

blech mit einer Höhe von 40 cm, die oben rechtwinklig abgekantet wurden (vgl. Abb. 7). An beiden Standorten wurden jeweils mindestens 500 m installiert, wobei das System sich an unterschiedlichste Geländebedingungen anpassen musste, d.h. entlang von Mauern, durch kleine Bäche, in der Böschung und auch im Grünland. Wiederansiedlungsversuche

Abb. 8. Freilandvitrine zur Information über Biologie und Schutz der Würfelnatter. Outdoor show case offering information on biology and protection of the dice snake. Foto: S. Lenz

Leit- und Abweissysteme entlang von Strassen An Elbe und Mosel werden die Standorte von Verkehrswegen durchschnitten, so dass die Gefahr des „Strassentodes“ für die Würfelnattern hoch war. Um die Individuenverluste zu minimieren wurden Leit- und Abweissysteme entwickelt und installiert. Zur Anwendung kamen speziell konzipierte Systeme aus verzinktem Stahl-

Die Wiederansiedlung von Würfelnattern wurde in drei Gebieten erprobt, ausgehend von unterschiedlichen Voraussetzungen und mit verschiedenen Strategien. An der Elbe wurden Schlangen aus tschechischen Beständen in Menschenobhut unter naturnahen Bedingungen nachgezüchtet und jeweils nach der ersten Überwinterung bei Meißen freigesetzt (1999 und 2000 je 75 Tiere). Die nächstgelegenen tschechischen Populationen an der Elbe liegen in einer Entfernung von ca. 50 km zum ehemals besiedelten Aussetzungsstandort. An der Lahn kamen zwei Strategien zum Einsatz: Ein Standort (ca. 12 km flussab der Ursprungspopulation) wurde mit nachgezüchteten Jungtieren besiedelt. Es wurden 66 Juvenes nach der 1. Überwinterung freigesetzt, deren Elterntiere vom gleichen Flusslauf stammen. An einem zweiten Standort wurden sukzessive in der ca. 15 km flussauf gelegenen Ursprungspopulation abgefangene Jungtiere, verteilt über eine ganze Aktivitätsperiode, freigelassen (insgesamt 53 Exemplare).

Abb. 9. Ein Freilandterrarium bot die Möglichkeit Würfelnattern zu beobachten und zu fotografieren ohne den Lebensraum zu betreten. Outdoor terrarium, which allowed to observe and to photograph dice snakes without entering the habitat. Foto: S. Lenz

34

Sigrid Lenz & Almuth Schmidt

Abb. 10. Titelbild der Kinderbroschüre „Würfel“. Cover of the children brochure “Würfel” (Eng. = “Dice”)

Abb. 11. Felsige, steinige Uferabschnitte am Wiederansiedlungsstandort in Meißen, Elbe. Rocky structures along the river bank at the reintroduction site in Meißen, Elbe. Foto: S. Lenz

Begleituntersuchungen, Monitoring An alle Aussetzungen schloss sich ein intensives, zweijähriges Monitoring an. Zudem wurden alle Massnahmen von der Planungsphase bis zur Ausführung begleitet und im Anschluss deren Effektivität bewertet. Dazu

Abb. 12. Beispiel für Pflegemassnahmen: Reich strukturiertes Unterwasser eines Wehres an der Lahn: (oben) vor, (Mitte) unmittelbar nach, und (unten) 8 Jahre nach der Durchführung von Entbuschungsmassnahmen. Example for management measures: Structurally rich spillway area of a weir at the river Lahn: (above) before, (middle) shortly after, and (below) 8 years after scrub removal. Fotos: A. Schmidt, A. Herzberg, S. Lenz

wurden neben den Beständen der Würfelnatter auch aussagekräftige Gruppen der Begleitfauna (wie Fische, Reptilien, Amphibien, Vögel, Heuschrecken, Libellen, Laufkäfer und aquatische Mollusken) und die Flora der Uferlebensräume engmaschig untersucht.

35

Nationwide Support for the Dice Snake in Germany

Besucher- und Freizeitlenkung, Öffentlichkeitsarbeit Der gesamte Projektzeitraum war von einer intensiven und vielgestaltigen Öffentlichkeitsarbeit begleitet. Neben einer kontinuierlichen Internet-Präsentation (www. wuerfelnatter.de, mittlerweile nicht mehr aktuell) wurden Poster und Broschüren erarbeitet. Hauptzielgruppe dabei waren die lokalen Bevölkerung und die Freizeitnutzer an und auf den Gewässern. Vor Ort wurde durch Vortragsveranstaltungen, gezielte Pressearbeit und standortspezifische Faltblätter und Schilder informiert. Für die Lahn wurde zusätzlich ein Merkblatt für Kanuten herausgegeben. An der Elbe entstanden eine Freilandvitrine mit Informationen zur Würfelnatter (vgl. Abb. 8), ihrem Lebensraum und dem Stand des Projektes sowie ein Freilandterrarium, das die Beobachtungen von Würfelnattern ermöglichte (vgl. Abb. 9). Hier wurden auch gezielt umweltdidaktische Aspekte mit einbezogen: es entstand ein reich bebildertes Heft für Grundschulkinder (vgl. Abb. 10), ausserdem übernahmen Schüler einer nahegelegenen Schule die Betreuung des Freilandterrariums. Ergebnisse und Diskussion Durch die gezielten Pflegemassnahmen wurden Verbesserungen in der Struktur von Natrix tessellata-Lebensräumen erreicht. Es entstanden flächenhaft besonnte Areale von hoher Attraktivität für die xerothermophil adaptierte Würfelnatter und ihre Begleitzoozönose. Freigestellte Flächen im Ufer- und Böschungsbereich wurden innerhalb einer Vegetationsperiode von entsprechend adaptierten Heuschrecken und Laufkäfern besiedelt und tragen damit zu einer Steigerung der Artenvielfalt bei. Der aquatische Lebensraum wird durch den Einschlag einzelstehender Ufergehölze deutlich aufgewertet, da sich bereits im Folgejahr kleine Buchten und z.T. Kolke bilden, die als Fischlaichzonen genutzt wurden. Auch die Würfelnatter reagiert innerhalb kurzer Zeit positiv auf derartige neue Lebensraumstrukturen, wie durch häufige Sichtbeobachtungen in den optimierten Bereichen zu belegen ist. Die Haltbarkeit und damit die Langzeit-Wirksamkeit sind sehr von der Struktur der Lebensräume abhängig. Am Standort Elbe ist das Ufer von Mauern und Felsstrukturen geprägt (vgl. Abb. 11), weshalb die Freistellung auf dem kargen Boden auch jetzt, nach mittlerweile 10 Jahren, zumindest in Teilbereichen noch erkennbar und wirksam ist. An der Lahn erwies sich die nachhaltige Pflege als deutlich problematischer: Die Lahn ist durch ein System von Stauhaltungen in ihrer Fliessgeschwindigkeit und -dynamik stark eingeschränkt, was zu einer Eutrophierung der Auenbereiche und damit zu einem expansiven Wachstum besonders von Hochstauden und Neophyten führt, die nur mit jährlichen Pflegeeinsätzen zu kontrollieren sind. Über mehrere Jahre erfolgreich war die initiale Entbuschung nur im Unterwasserbereiche von Wehren, da dort durch massiven

36

Holzeinschlag die Strömungsverhältnisse günstig beeinflusst werden konnten (vgl. Abb. 12). Dauerhafte und grossflächigere Habitatverbesserungen wurden durch wasserbauliche Massnahmen vor allem am Standort Mosel erzielt. Bereits im ersten Jahr nach der Fertigstellung wanderten Würfelnattern in den renaturierten Uferabschnitt ein. Langfristige Effekte, etwa im Sinne einer Steigerung des Würfelnatterbestandes oder einer Akzeptanz durch die Begleitzoozönose konnten im Projektrahmen nicht erfasst werden, da die Wasserbaumassnahme genehmigungs-, akzeptanz- und witterungsbedingt erst gegen Ende des Projektzeitraumes umgesetzt werden konnte. Aktuell, d.h. 10 Jahre nach Abschluss des Projektes haben alle angelegten Habitatstrukturen Bestand, eine der Buchten ist jedoch in Teilen verlandet. Der Abschnitt wird in Gänze von Würfelnattern genutzt, der nach Fang-WiederfangMethoden geschätzte Bestand hat sich, ausgehend von ca. 100 – 120 Tieren zu Projektbeginn, mehr als verdreifacht, das besiedelte Areal hat sich deutlich vergrössert (Lenz 2009). Die entwickelten und an Elbe und Mosel installierten Reptilienleitsysteme erfüllen im Wesentlichen ihren Zweck. Es war möglich, sie an alle gegebenen Geländeprofile anzupassen und dauerhaft abzudichten. Aufgrund unterschiedlicher behördlicher Auflagen (besonders entlang einer Bundesstrasse) muss die Konstruktionsweise zwangsläufig standortspezifisch angepasst werden. Anders als bei Amphibienanlagen liegt die Haupteinsatzzeit in der Vegetationsperiode, weshalb die Bleche kontinuierlich von überrankender Vegetation freigehalten werden müssen. Im Frühjahr werden die Anlagen zudem auf Schäden durch Unterspülung, Nagergänge u.ä. kontrolliert. Der Aufwand für Pflege und Wartung ist also hoch, aber unverzichtbar, da nur so die Systeme effektiv arbeiten. An der Elbe wurden durch fast tägliche Kontrollen, besonders während der Rückwanderung im Frühjahr, insgesamt 12 überfahrene Würfelnattern in 3 Jahren (2000–2002) gefunden – bei einem nach Fang-Wiederfang-Methoden geschätzten Bestand von mehr als 100 Tieren also ca. 10%. An der Mosel ging die Zahl der Strassenopfer von bis zu 10 Tieren pro Jahr vor dem Bau des Leitsystems auf ca. 2 pro Jahr zurück. An beiden Standorten zeigten sich zwei Nebeneffekte der Leitsysteme: (1) Die Bleche bieten Wanderlinien für die Reptilien. Adulte Tiere legen daher oft grössere Strecken (> 500 m) parallel zur Strasse zurück und können in Einzelfällen den Schutz der Systeme verlassen, in dem sie die endständig im 90°-Winkel montierte Abweisbleche umwandern. Es ist daher zu empfehlen, die Anlagen möglichst grossflächig zu installieren, um die Gefahr des Strassentodes weitestgehend zu minimieren. (2) Die Metallkonstruktionen in sonnenexponierter Lage heizen sich deutlich stärker auf als die Umgebung. Daher entsteht auf den flussseits gelegenen, durch kontinuierliche Pflege geschaffenen Freiflächen eine hohe

Sigrid Lenz & Almuth Schmidt

Stauwärme. Hier liegen bevorzugte Sonnenplätze verschiedener Reptilienarten. Aufgrund dieser Besonderheit besteht während der ganzen Aktivitätsperiode ein hoher Kontroll- und Abdichtungsbedarf, nicht nur zu den eigentlichen Wanderzeiten vor und nach der Überwinterung. Ein weiterer Aspekt des Projektes lag auf den Wiederansiedlungsversuchen an Lahn und Elbe. Die ersten Ergebnisse stellen sich wie folgt dar: An der Elbe zeigten die Wiederbeobachtungsraten in den ersten beiden Jahren nach der Aussetzung einen positiven Trend. Zum Abschluss des Projektes im Jahr 2001 konnte mittels einer Fang-Wiederfang-Untersuchung eine Populationsstärke von ca. 100 Tieren, d.h. 2/3 der Aussetzungszahl, ermittelt werden. Zudem gelang im gleichen Jahr der Nachweis einer eigenständigen Reproduktion am Aussetzungsstandort. Nach diesen ersten positiven Ergebnissen führte die Jahrhundertflut der Elbe im August 2002 jedoch zu erheblichen Bestandseinbussen (Gruschwitz & Lenz 2002). Der betreffende Uferabschnitt war für mehrere Wochen bis zu 6 m hoch überflutet, weshalb einige Tiere verdriftet wurden, andere in die nahegelegenen höheren Weinbergslagen auswichen. Stichprobenartige Untersuchun-

Abb. 13. Zerstörung eines wichtigen Überwinterungslebensraums der Würfelnatter an der Lahn durch vollständiges Verfugen während des Winterhalbjahrs. Destruction of an important hibernation habitat on the river Lahn by complete sealing during winter. Foto: S. Lenz

gen aus den Jahren 2003 und 2005, die im Auftrag der sächsischen Naturschutzverwaltung durchgeführt wurden, zeigten eine geringe Beobachtungsdichte. Sie belegen jedoch das Vorhandensein verschiedener Alterstufen und eine jährliche erfolgreiche Reproduktion (Lenz 2006). Ein Jungtiernachweis gelang 2007 (Tscherper, Fotobeleg), und auch in den Folgejahren wurden bei sporadischen Kontrollen immer mehrere Einzeltiere nachgewiesen. Inzwischen bezeugen weitere Funde von mehreren Schlüpflingen im Herbst 2010, dass diese Population weiterhin reproduziert (Obst & Strasser 2011). An der Lahn müssen die beiden Standorte und Wiederansiedlungsstrategien differenziert betrachtet werden. Im ersten Gebiet wurden im Frühsommer 66 Nachzuchttiere freigesetzt. Bereits im Jahr der Aussetzung war die Wiederbeobachtungsrate niedrig, im Folgejahr wurde nur noch ein Tier gesehen. Seitdem gelang bei sporadischen Kontrollen kein Nachweis mehr. Mehrere Gründe kommen für das vermutliche Scheitern dieses Wiederansiedlungsversuches in Frage: (1) Der Sommer nach der Aussetzung war von mehreren jahreszeitlich untypischen Hochwasserereignissen bestimmt, die zu einer Überflutung des gesamten Gebietes führten. (2) Zudem waren in diesem durch zahlreiche Geschiebeinseln geprägten Flussabschnitt die vorausgehenden Freistellungsmassnahmen nur sehr kurzzeitig wirksam; bereits am Ende des ersten Sommers waren kaum noch Freiflächen erhalten. (3) Beide Aspekte erschwerten zudem die Begehung des Geländes und letztlich das Monitoring deutlich. In einem zweiten Gebiet wurden sukzessive über eine ganze Aktivitätsperiode einjährige Wildfänge ausgesetzt. In den beiden ersten Jahren nach der Wiederansiedlung liessen Nachweishäufigkeit und Verteilung der Beobachtungen auf eine erfolgreiche Nutzung des neuen Lebensraums schliessen. Mittlerweile hat sich eine seit mehreren Jahren eigenständig reproduzierende Population hier eingestellt (Lenz 2007), Fang-Wiederfang-Untersuchungen wurden bislang nicht durchgeführt, jedoch werden jährlich Jungtiere, Subadulti sowie adulte Schlangen beider Geschlechter beobachtet. Die vor Start des Projektes einzige am Flusslauf Lahn bestehende Population diente als Quelle für die beiden Wiederansiedlungsversuche. Daher wurde sie vor und nach der Entnahme von trächtigen Weibchen bzw. Jungtieren einer Bestandserfassung unterzogen. Wie diese Fang-Wiederfang-Untersuchungen im Vergleich zeigen, wurde der Bestand nicht nachhaltig beeinträchtigt und lag bei Projektende gleichbleibend bei ca. 200 Individuen. Nach Abschluss des Projektes kam es an dieser Ursprungspopulation zu einem deutlichen Bestandseinbruch, verursacht durch massive Eingriffe in die Winterquartiere (vgl. Abb. 13). Im März wurden an einer vormals unverfugten Bruchsteinmauer alle Ritzen und Spalten verfüllt. Es ist anzunehmen, dass daraufhin zahlreiche dort überwinternde Würfelnattern ihre Rückzugsräume nicht mehr verlassen konnten. Dank

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Nationwide Support for the Dice Snake in Germany

der erstaunlichen Regenerationsfähigkeit von Würfelnatter-Populationen wurde auch dieser Einbruch mittlerweile kompensiert und die ursprüngliche Bestandsgrösse wieder erreicht (Lenz 2007). Danksagung Unser Dank für die finanzielle Unterstützung des E+E- Projektes gilt dem Bundesamt für Naturschutz, den Bundesländern Sachsen und Rheinland-Pfalz sowie der DGHT. Anschlussuntersuchungen waren dank der Unterstützung der sächsischen Naturschutzverwaltung und des Landesamtes für Umwelt, Wasserwirtschaft und Gewerbeaufsicht RheinlandPfalz möglich, welches seit 2006 auch ein Monitoring der Populationen übernommen hat. Ein besonderer Dank gilt Andrea Herzberg für die engagierte Mitarbeit während des Projektes. Literatur Bitz, A. & L. Simon (1996): Die neue „Rote Liste der bestandsgefährdeten Lurche und Kriechtiere in Rheinland-Pfalz“. – In: Bitz, A., Fischer, K., Simon, L., Thiele, R. & M. Veith (Eds.): Die Amphibien und Reptilien in Rheinland-Pfalz, Bd. 2. – Landau, GNOR: 615–618. Gruschwitz, M. (1978): Untersuchungen zu Vorkommen und Lebensweise der Würfelnatter (Natrix t. tessellata) im Bereich der Flüsse Mosel und Lahn (Rheinland-Pfalz). – Salamandra 14(2): 80–89. Gruschwitz, M. (1985): Status und Schutzproblematik der Würfelnatter (Natrix tessellata Laurenti 1768) in der Bundesrepublik Deutschland. – Natur und Landschaft 60: 353–356. Gruschwitz, M., Lenz, S., Mebert, K. & V. Lanka (1999): Natrix tessellata (Laurenti 1768) – Würfelnatter. – In: W. Böhme (Hrsg.): Handbuch der Amphibien und Reptilien Europas. Band 3/IIA: Schlangen II. – AULA-Verlag, Wiesbaden: 581– 644. Gruschwitz, M. & S. Lenz (2002): Würfelnatter übersteht Jahrhundertflut an der Elbe. – Elaphe 10(4): 40–44. Hecht, G. (1929): Zur Kenntnis der Nordgrenzen der mitteleuropäischen Reptilien. – Mitt. aus d. Zool. Museum Berlin 14: 501–597. Herzberg, A. & A. Schmidt (2001): Bericht zum Stand des Entwicklungs- und Erprobungsvorhabens „Würfelnatter“ der DGHT – 2. Teil: Erprobungsstandort Lahn. – Elaphe 9(3): 73–80. Kirschbaum, L.K.(1862/63): Die Reptilien und Fische des Herzogthums Nassau.– Jahrbücher d. Vereins für Naturk. im Herzogthum Nassau, Heft 17+18: 86–89. Kühnel, K.-D., Geiger, A., Laufer, H., Podloucky, R. & M. Schlüpmann (1998): Rote Liste und Gesamtartenliste der Lurche (Amphibia) und Kriechtiere (Reptilia) Deutschlands (Stand: Dezember 2008) − In: Haupt, H., Ludwig,

G., Gruttke, H., Binot-Hafke, M., Otto, C. & A. Pauly (Eds.) (2009): Rote Liste gefährdeter Tiere, Pflanzen und Pilze Deutschlands, Band I: Wirbeltiere. Bundesamt für Naturschutz: Naturschutz und biologische Vielfalt, Bonn 70(1). Lenz, S. (2006): Zur aktuellen Situation der Würfelnatter an der Elbe. – Elaphe 14(1): 12–14. Lenz, S. (2007): Schlussbericht 2007 über Untersuchungen zur Bestands- und Gefährdungssituation der Würfelnatter (Natrix t. tessellata) an Nahe und Lahn. – unveröffentlichter Projektbericht i.A. des Landesamtes für Umwelt, Wasserwirtschaft und Gewerbeaufsicht, Mainz. Lenz, S. (2009): Schlussbericht 2009 über Untersuchungen zur Bestands- und Gefährdungssituation der Würfelnatter (Natrix t. tessellata) an der Mosel. – unveröffentlichter Projektbericht i.A. des Landesamtes für Umwelt, Wasserwirtschaft und Gewerbeaufsicht, Mainz. Lenz, S. & M. Gruschwitz (1992): Artenschutzprojekt Würfelnatter (Natrix tessellata): – Flora und Fauna in Rheinland Pfalz. – Beiheft 6: 55–60. Lenz, S. & M. Gruschwitz (1993): Zur Populationsökologie der Würfelnatter, Natrix t. tessellata (Laurenti 1768) in Deutschland (Reptilia: Serpentes: Colubridae). – Mertensiella 3: 253–268. Lenz, S., Gruschwitz, M., Schmidt, A. & A. Herzberg (2006): Entwicklung und Vernetzung von Lebensräumen sowie Populationen bundesweit bedrohter Reptilien an Bundeswasserstrassen am Beispiel der Würfelnatter (Natrix tessellata) an den Flüssen Mosel, Lahn und Elbe. – Natur und Landschaft 3: 152–157 Lenz, S., Mebert, K. & J. Hill (2008): Die Würfelnatter: Reptil des Jahres 2009. – In: Die Würfelnatter, Reptil des Jahres, Aktionsbroschüre. – DGHT, Rheinbach, Deutschland. Lenz, S. & A. Schmidt (2002): Bericht zum Stand des Entwicklungs- und Erprobungsvorhabens „Würfelnatter“ der DGHT – 2. Teil: Erprobungsstandort Mosel. – Elaphe 10(1): 53–59. Le Roi, O. & A. Reichensperger (1913): Die Tierwelt der Eifel in ihrer Beziehung zu Vergangenheit und Gegenwart. – Eifelfestschrift zur 25-jährigen Jubelfeier des Eifelvereins, Bonn: 186–212. Mertens, R. (1947): Die Kriechtiere und Lurche des RheinMain-Gebietes. – Frankfurt (W. Kramer). Noll, F.C. (1869): Die Würfelnatter (Tropidonotus tessellatus) eine deutsche Schlange. – Zool. Garten 10: 299–304. Noll, F.C. (1888): Die Würfelnatter an der Mosel. – Zool. Garten 29: 242–243. Obst, F.J. (1976): Die Würfelnatter bei Meißen – ein erloschenes Vorkommen (Reptilia, Ophidia, Colubridae). – Zool. Abh. Staat. Mus. Tierk. Dresden 34: 47–52. Obst, F.J. (1990): „Die Würfelnatter bei Meißen - ein erloschenes Vorkommen“- nur ein bedauerlicher Fakt oder eine Herausforderung. – Feldherpetologie, Erfurt 1989: 16–22. Obst, F.J. & P. Strasser (2011): Das Sächsische Vorkommen der Würfelnatter im Elbtal bei Meissen. – Mertensiella 18: 58–70. Zimmermann, R. (1910): Über das Vorkommen der Würfelnatter im Königreich Sachsen. – Wochenschr. F. Aquar Terrarienkde., Beilage Lacerta 2: 8.

Autoren Sigrid Lenz, Am Wallgraben 8, 56751 Polch, Germany, e-mail: [email protected]; Almuth Schmidt, Zinzendorfer Straße 9, 56564 Neuwied, Germany.

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MERTENSIELLA 18

39-48

20 September 2011

ISBN 978-3-9812565-4-3

Migration Behavior of Endangered Dice Snakes (Natrix tessellata) at the River Nahe, Germany Christian Neumann & Konrad Mebert Abstract. The valley of the river Nahe is known to sustain the largest population of dice snakes in Germany. The population is further dispersed into half a dozen subpopulations along the approximately 15 km long Nahe River. A frequented road splits most of the habitat, leading to numerous traffic casualties of snakes every year. Because of its isolation to other populations of dice snakes and its relatively large population size, an active protection of the Nahe population can be considered to be fundamental for the conservation of this nationally endangered species. In 2007, a radiotelemetry study was carried out at one of the subpopulations to analyze the migration behavior of the dice snakes to provide ecological data for future conservation strategies. Five adult female dice snakes were tagged with subcutaneous implanted transmitters to construct movement profiles. The calculated homerange varied depending on the analysis method from 0.22 ha (95% Kernel) to 0.27 ha (MCP). The tagged snakes were mainly active at air temperatures between 20–26 °C and partially cloudy sky. Activity in the water or near the shore was detected every 4–5 days, mostly between 15–18 pm. The daily movement of the tagged snakes was in 80% less than 30 m. Key words. Activity, Germany, homerange, Kernel density estimation, MCP, mobility, Natrix tessellata, radiotelemetry Zusammenfassung. Die Kernlebensraum der grössten deutschen Würfelnatterpopulation am Fluss Nahe, Rheinland-Pfalz, Deutschland, wird fast entlang des gesamten Flusslaufs von einer teils stark frequentierten Strasse zerschnitten. Hier werden jedes Jahr Dutzende Würfelnattern überfahren. Dies ist eine ernstzunehmende Gefahr für die isolierte Population, die sich entlang des ca. 15 km langen Flussabschnitts auf etwa ein halbes Dutzend Subpopulationen verteilt. Im Jahr 2007 wurde an einem dieser Subpopulationen eine radiotelemetrische Studie durchgeführt, um durch genauere Bewegungskenntnisse effektivere Schutzmassnahmen durchführen zu können. Hierfür wurden fünf adulte Würfelnatterweibchen mit subcutan implantierten Sendern versehen und deren Bewegungsprofile erstellt. Der ermittelte Aktionsraum beträgt je nach Auswertungsmethode zwischen ca. 0.22 ha (95% Kernel) und 0.27 ha (MCP). Die Hauptaktivität der Senderschlangen war bei 20–26 °C Lufttemperatur und wechselhafter Bewölkung. Aktivität im Wasser oder in Ufernähe war etwa alle 4–5 Tage zu verzeichnen, in über 50% der Fälle dann zwischen 15 und 18 Uhr nachmittags. Die täglich zurückgelegte Strecke der Senderschlangen war in 80% der Fälle unter 30 m. Stichworte. Aktivität, Deutschland, Natrix tessellata, Homerange, Kernel-Dichteverteilung, MCP, Mobilität, Radiotelemetrie

Introduction The Nahe Valley is home of the largest population of dice snakes in Germany (Fig. 1). The valley is not only a suitable habitat for dice snakes and other reptiles, but is also a popular destination for local recreation because of its picturesque landscape and almost mediterranean subclimate. A district road runs parallel to the river, thus dissecting the habitat of the dice snake population. Especially in spring and summer, this road is strongly frequented by several hundred cyclists every day. In the nineties, the population at the Nahe River was estimated at 250–350 individuals (Lenz & Herzberg 1996), but a more recent assessment along the entire 15– 20 km long section of the river estimates approximately 800–1400 individuals (Lenz 2007), which are distributed across about half a dozen subpopulations (Lenz 2007). Numerous dice snakes are killed every year by road traffic, mostly during the spring and autumn mi-

grations (Niehuis 1996). At one of those migration spots, an increased mortality rate of dice snake has been reported by locals since 2001, despite the installation of a protective guiding fence along the road. Subsequently in 2002 and 2006, this site was the focus of a capture-recapture study and a monitoring of the migratory routes of juvenile dice snakes (Lenz 2007). But these methods provided only limited results, because large parts of this site, especially the shoreline and its preferred basking spots, were difficult to impossible to access. To complement the missing information on this site, a radiotele­ metry study was initiated in 2007, incorporated into a MS thesis of the senior author. The results should provide further data to allow for more effective conservation strategies at this accident hotspot. Main objectives were the identification of the migratory routes, the oviposition sites, diurnal shelter and the hibernaculas. The results of the radiotelemetry study are the focus of this paper.

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Christian Neumann & Konrad Mebert

Fig. 1. Dice snake Natrix tessellata from the river Nahe. Photo: Benny Trapp.

Research Area The research area is located in the German Federal Land “Rheinland-Pfalz” (Eng. = Rhineland-Palatinate) and is part of the natural landscape unit “Nordpfälzer Berg­ land” (Eng. = Northern Palatinate hill-country). The Nahe River meanders through this hilly country and flows into the river Rhine at the town Bingen. The name

of the river Nahe is celtic origin and means „wild river“. The investigated area is about 120 m a.s.l. The Nahe is relatively shallow and produces temporarily a strongly fluctuating water flow (level at Boos: 3 m3/s to 694 m3/s), rendering it unnavigable (Lenz & Herzberg 1996). Thus only a few hydro-engineering measures were carried out in the Nahe Valley, enabling the river to remain relatively natural. It contains extensive gravelbanks and the zones of shallow water yield a rich fish fauna (Fig. 2). Especially the run-offs of the weirs offer a perfect habitat for dice snakes (Lenz & Herzberg 1996, Niehuis 1996). The valley of the river Nahe is predominated by a xerothermic climate with continental characteristics: high temperatures, sparse rainfall and long vegetation periods (Uhlig 1954). The mean annual temperature in Bad Kreuznach, the largest town in the district, is 9.5 °C (1961–1990; Deutscher Wetterdienst), which is 4 °C higher than in the adjacent low mountain ranges of the Hunsrück. The average temperatures in July range 18–19 °C (Niehuis 1996). The vegetation period is six weeks longer than in the nearby Hunsrück. It starts on the 30 April and ends on the 10 October (Blaufuss & Reichert 1992). In Bad Kreuznach the total annual precipitation is 517 mm/m2, which is one third less than the German average of approximately 800 mm/m2 (1961–1990; Deutscher Wetterdienst). In the vegetation growth

Fig. 2. Habitat of Natrix tessellata at the river Nahe: Photo: Benny Trapp.

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Migration of Dice Snakes at River Nahe, Germany

period from May–July the rainfall in this area accumulates only 160–180 mm (Niehuis 1996). Therefore, the Nahe Valley is one of the warmest and driest regions in whole Germany. Today, the Nahe Valley is shaped by viniculture with many steep and rocky slopes used for cultivating vine grapes or left temporary as fallow land, yielding arid grassland and dry slope. An abundance of crevices and dry stone walls provide an ideal habitat for many reptiles, yielding large populations of grass snakes (Natrix natrix), smooth snakes (Coronella austriaca), western green lizards (Lacerta bilineata) and European wall lizards (Podarcis muralis) (Lenz & Herzberg 1996). The Nahe Valley is also home of the largest dice snake population (N. tessellata) in Germany. Three parts of the valley with a total area of approximately 300 ha have been declared as nature protection areas (NSG) and are also part of the European ecological network Natura 2000. The district road K58 runs parallel to the shore along most of the river course and is also part of the “NaheRadwanderweg” (Nahe bike tour road), which is highly frequented by cyclists from spring to autumn. Every year dozens of dice snakes are killed along this route, especially during the spring and autumn migrations, but also while basking on the asphalt road (Niehuis 1996). The road’s dissection of the snake habitat is the most serious threat for this isolated population at the Nahe River. The nearest population of dice snakes at the rivers Mosel and Lahn are more than 60 km air distance away and thus, an exchange of individuals is not possible (Niehuis 1996). Another relevant threat for the local population at the Nahe River is the disturbance through recreation activities. Despite of a ban by the local public authority, certain tributaries of the river are strongly frequented by canoeists and people with rubber boats in the summer months (Niehuis 1996). In summary, the river Nahe can be characterized as an ideal habitat for dice snakes due to a close-to-nature river course, containing numerous gravel banks and areas of shallow water for fishing, and a xerothermic microclimate along slopes, vineyards, and dry stone walls, providing many suitable hiding places and sites for oviposition and incubation. The survey took place on one of the population hotspots, an approximately 800 m long section along the river Nahe. The center of this area extends over approximately 400 m along the district road. This is the section where the highest number of dice snakes is killed each year. For reasons of protection, I abstain from a more detailed description as well as supplemental map material.

Fig. 3. Transmitters from different views; the button cell (battery) is visible in the bottom view.

width of 12 mm and a height of 10 mm (see Fig. 3). The weight was 4.5 g with a pulse rate of 40 per minute and a pulse length of 15 ms. The transmitters were designed for a minimum runtime of four months according to Bio­ track. A maximum range of 150 m was determined via two blind tests on a plain without obstacles. Measuring inaccuracy at a distance of 75 m was approximately 5 m, at a distance of mare than 120 m up to 10 m. The receiver „TRX-16S“ from Wildlifematerials International Inc, USA (http://www.wildlifematerials.com) in combination with a Yagi-antenna was used to detect the transmitter signals. One main focus of this study was the identification of the local oviposition sites, so only adult females were considered for the implantation of transmitters, which were implanted subcutaneously (Figs. 4 and 5). Isofluran was used for the anaesthetization. After the surgery, the dice snakes were kept in quarantine for 4–5 days before being released at the site of their capture. The implantations of the transmitters were carried out by the veterinarian J. Wiechert (Mainz, Germany).

Materials and Methods General methods followed recommendations by Amrhein (2006). Transmitters (Biotrack Ltd., UK: http:// www.biotrack.co.uk) were spheres with a length and

Fig. 4. Subcutaneous implanting of the transmitter.

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Christian Neumann & Konrad Mebert

gon-method (MCP) (Mohr 1947) and the Kernel-density-estimation (Haller 1996, Worton 1989). For the construction of the Multi-Convex-Polygon the software „Convex_Hulls v.1.23“ (Jenness 2007) was applied. The more significant Fixed-Kernel-density-estimation was carried out with Hawth’s Analysis Tools for ArcGIS (Beyer 2004). This study was authorized by the public authority “Struktur- und Genehmigungsdirektion Nord – Rheinland Pfalz”, file number: 425-104.133.0701. Results and Discussion Behavior Results

Fig. 5. A dice snake directly after surgery, still numb from the anaesthetization; the red arrow shows the location of the subcutaneous transmitter.

To record the movement pattern of tagged dice snakes, I applied crossing-bearing and homing-in methods. Most of the research area consists of steep slopes with gradients of 60–70% and was difficult or impossible to access. Consequently, the tagged snakes had to be located usually indirectly by crossing-bearing. The first radiotelemetric localizations were made about one hour after releasing the tagged snakes into their natural habitat. The acquisition of telemetric data started on 15 May 2007 and ended on 13 July 2007. The recordings were usually conducted for six days in a row, followed by a pause of 1–2 days. Daily localizations begun around 9:30 am and ended duirng the sunset between 20 and 21 pm. The tagged dice snakes were located once per hour and crossing-bearing data measured within 1–3 minutes. Along with each localization the air temperature and the cloudiness were recorded. Data collected from the release site until the last registered movement were used to calculate the home range, which was analysed with the Multi-Convex-Poly­

Five mature female dice snakes were tagged with transmitters, whereof only three individuals provided sufficient data over an extended duration for further analysis (Tab. 1). The first localizations of any snake yielded no data, because the signals of the transmitters were missing for 2–4 days following the release of the snake. The snakes presumably continued to remain hidden deep in a crevice, where transmitter signals were absorbed by the rock, in order to completely heal their wounds after surgery. The calculated home range varies depending on the analysis method from 0.23 ha (95%-Kernel-density estimation) to 0.27 ha (Multi-Convex-Polygon-method). These calculated home ranges cover only the summer habitat without spring- and autumn migrations. The re-

Tab. 2: Calculated Home range of adult female dice snakes; Multi-Convex-Polygon (MCP) and Fixed Kernel estimation.  

MCP

Snake No. 1 Snake No. 2 Snake No. 3 Average

3549 m2 1746 m2 2798 m2 2698 m2

95% Kernel 2389 m2 1830 m2 2669 m2 2296 m2

90% Kernel 1405 m2 1259 m2 1530 m2 1398 m2

50% Kernel 281 m2 321 m2 278 m2 293 m2

Tab. 1: Basic data on dice snakes tagged with transmitters; „No. of days recording/location points” is the time span between date of release and date of last reported activity. Tagged snake Date of capture Date of release Sex Total-length [cm] Weight [g] Reproductive status at capture Later recapture/sighting Duration of telemetric recording No. of days recording No. of location points Weight ratio transmitter/body (%)

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No. 1 10 May 2007 15 May 2007 ♀ 93 302 None No 15 May – 13 July 40 257 1.49

No. 2 10 May 2007 15 May 2007 ♀ 94 256 None No 15 May – 13 July 15 88 1.76

No. 3 30 May 2007 5 June 2007 ♀ 96 306 Gravid Recapture 5 June – 21 June 13 97 1.47

Migration of Dice Snakes at River Nahe, Germany

sults also indicate that females dice snakes were rather loyal to their site (Tab. 2; 50% Kernel). Their home ranges stretched maximally 100 m parallel to the shoreline and up to 15 m deep on land. In central and southern Switzerland (Bendel 1997, Conelli & Nembrini 2007, Conelli et al. 2011) and in Prague, Czech Republic (Velenský et al. 2011), researchers observed similar to more distant movements of dice snakes in the summer, usually along a stretch parallel to the shoreline of 100–500 m, and max. up to ~ 1000 m. But their spring and autumn data show increased distances migrated to and from the hibernation sites. The radiotelemetered data revealed that female dice snakes stayed mostly on land during the day. The hiding places of the snakes were in the crevices of a steep slope with a south western exposition, approximately 5 m above mean water level. The maximum distance to the shoreline was less than 10 m. The entrance of the crevices and its proximity was often used as a spot to thermoregulate. In the case of an imminent threat such as an approaching person, the snakes were able to retreat quickly to their hiding place within approximately 3 seconds. Even though there was sufficient areas with

trees and srcub, radio tracked dice snakes on land were always located in semi-open to fully open, rocky segments of the shore environment. The principal terrestrial habitat that was used for thermoregulation and as nocturnal shelter consisted of a road-supporting wall made of large block stones (Fig. 6). Registered movements were normally short migrations from their shelter to other basking spots with better expositions or less vegetation, usually not farther away than 5–15 m. All tagged dice snakes were located in their terrestrial habitat within 15 m from the shoreline. The average daily covered distance was less than 30 m in about 80% of all localizations. The longest registered daily movement by a dice snake was 250–260 m, from which ~200 m were covered in water. Every 4–5 days, the female dice snakes descended from their basking spots or shelter high up on the sloped wall, passed a semi-open area, containing a tree, a few bushes, and plenty of herbaceous plants (Fig. 7) to finally enter the water for 1–2 hours of fishing. The successful snakes landed with the fish at the semi-open area to swallow it and returned right after consummation to their shelter to digest (Fig. 6). Foraging activity

Fig. 6. Radio tracked dice snakes were predominantly located in this open, road-supporting wall made of large block stones that were used for thermoregulation and nocturnal sheltering.

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Christian Neumann & Konrad Mebert

Fig. 7. This semi-open area was passed by the dice snakes to enter the water, and used again to consume a fish that they brought on land. Shortly after complete ingestion, they returned to their basking site to digest the prey (see Fig. 6).

(entering the water) was rarely before 12 am (less than 10%), but was recorded mostly in the afternoon between 15–18 pm (~55.9%) (Fig. 8). These results resemble the observations by Lenz & Gruschwitz (1993) from another German population of dice snakes, where 10% of active individuals were observed up to 12 am and ~80% between 13 and 17 pm. Observation on Czech dice snakes point towards a similar behavior (Lanka 1978). On days with registered movement in the river, the daily distance of radiotelemetred snakes covered was usually between 50–100 m. The active outdoor residence times were short, as most snakes remained in the water or in close proximity during one or two hourly localisations (Fig. 8). Average residence time was ~90 minutes; longest residence time was ~150 minutes. This contrasts the statement that dice snakes in a proximate population at the river Lahn spend most of the afternoon in the water (Lenz & Gruschwitz 1993). However, those data were not acquired through independent radiotelemetry nor constant observation of individuals, hence, terrestrial stay in the afternoon may have been missed when the snakes remained invisibly hidden on land.

44

The rare and short residence times in the river are also contrary to the information of Mertens (1947) and Blab & Vogel (1996) who noted that dice snakes stay for several hours in the water. But the short stay in the water in this study might relate to a behavior strategy of gravid females in which they prevent cooling their body to promote embryogenesis. In this context, they may search for a terrestrial site with better conditions for thermoregulation and ultimately oviposit away from the water or simply stay on land to thermoregulate and accelerate embryogenesis (Dusej 2007, Mebert 2011). Observed time spans of up to two weeks in which the gravid snakes did not visit the river suggest such a particular behavior. The different distances moved by each of three snakes are shown in Figure 9. Snake No. 1 provided the largest amount of data (40 days, 257 location points, cf. Tab. 1). Snake No. 2 seemed to be the most active one with frequent short movements. However snake No. 3, which remained most of the time in hiding, covered the longest single daily distance of about 250 m. But on the day of the long distance movement, the Nahe River expe-

Migration of Dice Snakes at River Nahe, Germany

Fig. 9. Daily movement of tagged snakes; n = number of recorded days (cf. Tab. 2); less than 10 m movement is categorized as „no activity“, because of possible measuring inaccuracy. Fig. 8. Daytime activity of tagged snakes in water or on land at a distance of approx. 5 m from the shoreline; n = number of hourly localizations in water or near shore; d = number of days with localizations in the river or on land near the shore; x = n/d

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Christian Neumann & Konrad Mebert

rienced a high tide from heavy rainfall of the previous days. Hence, this distance may be a result of a drift and a remigration (Lenz & Gruschwitz 1993). This study has further confirmed the observations made by Trutnau (1981) and Lenz & Gruschwitz (1993) concerning the relation of air temperature and main activity. The activity peak of snakes No. 1 and No. 2 could be registered at a temperature range of 20–25 °C and partially cloudy sky, which is in accordance to the hitherto assumed range of preferred air temperatures between 20–26 °C, and 19–26 °C respectively. Problems with Radiotelemetry Originally, it was intended to collect data from the mating season in May (for the identification of the mating places) until the start of hibernation in September/October (for the identification of the hibernation sites). Therefore, transmitters were chosen with a minimum operating time of 4 months. Due to the planed operating time, relatively large transmitters were selected, which may be able to have biased the snake’s behavior. Yet, the weight ratio transmitter/body was substantially below the recommended (Kenward 2001) maximum of 5% (cf. Tab. 1). Another issue that might had an effect on the snake’s behavior concerns a possible postsurgery trauma. The transmitters greatly stretched the skin around the implantation area (Fig. 5), which may have caused the snake to behave unnaturally for a couple of days by remain hidden for a longer period after its release than usual. Movements of snake No. 1 have been recorded nearly up to the end of this study. Apparently, this snake had the least problems with the implanted transmitter. Snake No. 2 appeared to produce problems with the transmitter, because signals indicated a termination of its movements three weeks after its release. The transmitter sig-

Fig. 10. Tagged snake with an open, dry wound. The transmitter is visible (red arrow). Apparently the snake had some shedding problems because of the surgery seam.

46

nal was located directly under the asphalt of the district road at a site which is used by the dice snakes as a resting place. The signal accuracy was determined to half a meter using homing-in-method. Either dice snake No. 2 was able to successfully stripe off the transmitter or it died in its resting place. No verification was possible due to the inaccessible location under the asphalt. After the last registered movement of this snake, an additional 166 localisations were taken over a time span of about 3 weeks until the end of the radiotelemetric survey. Snake No. 3, which was recaptured during the survey, had shedding problems along the suture of the implantation area and the transmitter was visible through an open wound in the skin (Fig. 10). The snake excoriated its skin, presumably to get rid off the implanted transmitter. Fortunately the wound was dry and not inflamed. After the recapture, snake No.3 was brought back to the veterinary clinic and the transmitter was removed. The snake was then kept for ten days in a terrarium for recovery, and subsequently released into its natural habitat (Fig. 11). While recovering in the veterinary clinic snake No. 3 laid 16 eggs in the night from 2 to 3 July. The eggs were incubated at 27 °C and hatched after 37–41 days and a last egg was laid after 47 days. One ovoposition site was later found in autumn by digging suspected substrates. The site contained 70 open eggs in a compost pile in about 20 cm depth. The pile was located ~50 m away from the shoreline and about 1.5–2 m above the waterline. On noon of 13 July an exhausted, emaciated adult female dice snake was found only 3–4 m away from the compost pile. This observation suggests that this individual has just laid eggs on this day or the night before and that the clutch is indeed from at least one dice snake. The time span for oviposition is nearly the same as Velenský et al. (2011) observed in a Czech population of dice snake (5–15 July).

Fig. 11. The same snake approx. two weeks after removal of the transmitter on its release day. For disinfection and a better healing, Dentisept®-salve was applied on the wound.

Migration of Dice Snakes at River Nahe, Germany

The radiotelemetric survey ended abruptly on the 13 July, a defective contact in the receiver disabled the continuing of data collection. It was not feasible to acquire a substitute receiver within 2 weeks. At this time, snake No. 4 had been tagged only for 11 days with 47 localisations and snake No. 5 for less than a week, therefore the collected data were insufficient to be included into the analysis (less than the recommended 30 localisations by Kenward, 2001). Without a receiver it was impossible to track the tagged snakes in the following weeks, a period in which the visible activity (or outdoor presence) of adult dice snakes decreases drastically about 90% at this site. Such a decrease of dice snake activity in the summer has been observed by several authors (Hecht 1928/1929, Lanka 1978, Lenz & Gruschwitz 1993, Mebert 2001, 2007) and is presumed to relate to an aestivation (summer rest) period. Conclusions It was clear at the start of this project that only some of the goals could be accomplished due to the tight schedule allowed for a M.S. study (usually only three months are permitted by the university for data acquisition until finished draft). So it came to no surprise that not all goals of this survey could be achieved. For example, the identification of the migratory routes of dice snakes failed, because of the insufficient movement data of the tagged snakes and the short duration of the radiotelemetric survey in the spring/summer (May–July), which was outside the migration period. Such migrations routes of dice snakes in early spring and autumn have been detected in radio-tracked dice snakes from Ticino, southern Switzerland (Conelli & Nembrini 2007, Conelli et al. 2011) and in Prague, Czech Republic (Velenský et al. 2011). The relatively late start at 9:30 am for the daily radiotelemetric localizations was presumably the reason for the failed identification of the oviposition sites. Lenz & Gruschwitz (1993) suggested that the egg laying takes place at night or in the early morning, which was confirmed by the overnight oviposition of snake No. 3. Luckily, information about oviposition sites was acquired after finding such a site in autumn by digging suspected substrates. Due to the breakdown of the receiver, it was not possible to locate the hibernation sites in late autumn. Despite of the scarce data, this study provided some interesting information about the behavior of local dice snakes, such as the reduction of movements in gravid females. Because of the presumably greater mobility of male than female dice snakes (see refs. in Conelli & Nembrini 2007), tagging of male dice snakes may be more appropriate for future identification of migratory routes, but the issues with their lower weight, and thus the requirement of smaller transmitters, should be resolved first. According to A. Conelli (pers. comm.), the telemetry method should be improved in order to

i) reduce the size of transmitters while enhancing their life span, ii) simplify the implantation procedure, thus minimizing the impact on the animals’ physiology and health, and iii) reduce the effort by operators in the field (e.g. apply automatic GPS localization and data analysis). Finally, collecting data over more than one year may produce more reliable information than a short survey over only a couple of months. Acknowledgments I wish to thank the following persons and institutions: Sigrid Lenz (Polch, Germany) for the introduction to the world of dice snakes and her general assistance for this project, Jutta Wiechert (Mainz, Germany) for implanting the transmitters and keeping the snakes in quarantine, my brother Sebastian Neumann (University Mainz, Germany) for his general assistance and proofreading, Torsten Kaster (Mainz, Germany) for his general tips in snake handling and the practical use of radiotelemetry as well as his assistance for the fieldwork, , Benny Trapp (Germany) for his great photographs, Department 4 of the public authority “LUWG” (Mainz, Germany) for the general support and the public authority “Struktur- und Genehmigungsdirektion Nord – Rheinland Pfalz” (Koblenz, Germany) for granting me the authorization for this project. References Amrhein, V. (2006): Radiotelemetrie. – In: Naguib, M. (Ed.): Methoden der Verhaltensbiologie. –Springer Verlag, Germany: 194–197. Bendel, P.(1997): Zur Physiologie, Morphometrie und Populationsökologie der Würfelnatter Natrix tessellata am Alpnachersee. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Beyer, H.L. (2004): Hawth’s Analysis Tools for ArcGIS. – Available at: http://www.spatialecology.com/htools. Blab, J. & H. Vogel (1996): Amphibien und Reptilien Erkennen und Schützen: Alle Mitteleuröpäischen Arten. Biologie, Bestand, Schutzmassnahmen. – BLV-Verlagsgesellschaft, München, Germany. Blaufuss, A. & H. Reichert (1992): Die Fauna des Nahegebietes und Rheinhessens. – Pollicia Nr.26, Bad Dürkheim (Eigenverlag). Conelli, A. E. & M. Nembrini (2007): Studio radiotelemetrico dell’habitat della Biscia tassellata, Natrix tessellata (Laurenti, 1768). – Bollettino della Società Ticinese di Scienze Naturali 95: 45–54. Conelli, A. E., Nembrini, M. & K. Mebert (2011): Different habitat use of dice snakes, Natrix tessellata, among three populations in Ticino Canton, Switzerland – A radiotelemetry study Mertensiella 18: 100–116. Deutscher Wetterdienst (1996): Gerhard Müller-Westermeier: Klimadaten von Deutschland: Zeitraum 1961­–1990. – Offenbach, Germany. – Available at: http://www.dwd.de. Dusej, G. (2007): Die Würfelnatter: Lebensweise und Schutzmöglichkeiten. – karch, Neuchatel, Switzerland. Jenness, J. (2007): Convex Hulls. – Available at: http://www.jennessent.com/arcview/convex_hulls.htm . Jenness Enterprises, Flagstaff, USA.

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Christian Neumann & Konrad Mebert Haller, R. (1996): Homerange- und Habitatanalysen. Entwicklung von Methoden zur Nutzung von Geographischen Informationssystemen in der Wildforschung. – M.S. thesis, Geo­ graphisches Institut Zürich, Switzerland. Hecht, G. (1928/1929): Zur Kenntnis der Nordgrenzen der Mitteleuropäischen Reptilien. –Mitteilungen des Zoologischen Museum Berlin 14(3/4): 502–597. Kenward, R. (2001): A Manual for Wildlife Radio Tagging. – Aca­demic Press London. Laňka, V. (1978): Variabilität und Biologie der Würfelnatter (Natrix tessellata). – Acta Universitatis Carolinae, Biologica 1975– 1976: 167–207 Lenz, S. (2006): Kurzbericht über Leistungen zur Pflege und Ent­wicklung der Würfelnatter-Lebensräume sowie zu Ergebnisse der Würfelnatter-Beobachtungen 2006. – Struktur- und Genehmigungsdirektion Nord, Koblenz, Germany. Lenz, S. (2007): Schlussbericht der Untersuchungen zur Bestands- und Gefährdungssituation der Würfelnatter (Natrix t. tessellata) an der Nahe. – Landesamt für Umweltschutz und Gewerbeaufsicht, Oppenheim, Germany. Lenz, S. & M. Gruschwitz (1993): Zur Autökologie der Würfelnatter, Natrix tessellata (Laurenti 1768) in Deutschland. – Mertensiella 3: 235–252. Lenz, S. & A. Herzberg (1996): Pflege- und Entwicklungsplan für das Nahetal von der Glanmündung bis Bad Kreuznach. – Landesamt für Umweltschutz und Gewerbeaufsicht, Oppenheim, Germany.

Mebert, K. (2001): Die Würfelnatterpopulation am Alpnachersee – In: NAGON (Ed.): Amphibien und Reptilien in Unterwalden. – NAGON, Grafenort, Switzerland 2: 158–163. Mebert, K. (2007): Die Würfelnatter am Brienzersee. – In: Jahrbuch 2007, Uferschutzverband Thuner- und Brienzersee. – UTB Selbstverlag, Thun, Switzerland: 169–180. Mebert, K. (Ed.) (2011): The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species. – Mertensiella 18, DGHT, Rheinbach, Germany. Mertens, R. (1947): Die Lurche und Kriechtiere des RheinMain-Gebietes. – Verlag Dr. Waldemar Kramer, Frankfurt/ Main, Germany. Mohr, C.O. (1947): Tables of equivalent populations of North American small mammals. – American Midland Naturalist 37: 223–249. Niehuis, M. (1996): Würfelnatter – Natrix tessellata (Laurenti, 1768). – In: Bitz, A., Fischer, K., Simon, L., Thiele, R. & M. Veith (Eds.): Die Amphibien und Reptilien in RheinlandPfalz. – GNOR-Eigenverlag, Landau, Germany 2: 429–450. Trutnau, L. (1981): Schlangen im Terrarium, Bd. 1: Ungiftige Schlangen. – Ulmer-Verlag, Germany. Uhlig, H. (1954): Landkreis Kreuznach. – Die Landkreise in Rheinland-Pfalz, Bd. 1 – Speyer, Germany. Velenský, M., Velenský, P. & K. Mebert (2011): Ecology and ethology of dice snakes, Natrix tessellata, in the city district Troja, Prague. – Mertensiella 18: 157–176. Worton, B.J. (1989): Kernel Methods for estimating the utilization distribution in home-range studies. – Ecology 70(1): 164– 168.

Authors Christian Neumann, Hegelstrasse 20, 55122 Mainz, Germany, e-mail: [email protected]; Konrad Mebert, Siebeneichenstrassse 31, 5634 Merenschwand, Switzerland.

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MERTENSIELLA 18

49-57

20 September 2011

ISBN 978-3-9812565-4-3

The Rearing of Dice Snakes: Part of a Concept for the Sustainable Conservation of Endangered and Isolated Populations in Western Germany Dietmar Trobisch & Andrea Gläßer-Trobisch Abstract. As part of a large project on the conservation of three remnant populations of dice snakes in western Germany, we managed the rearing of dice snakes with the aim of their reintroduction. A detailed service contract was issued between the German Herpetological Society (DGHT) as contractee and the authors as contractors. Eight gravid dice snakes were caught in June 1999 in the nature reserve “Schleuse (= lock) Hollerich” along the River Lahn and subsequently housed in terraria. After oviposition by each female, the snakes were returned and released at their place of origin. A total of 97 eggs were laid, of which 77 hatchlings emerged. They were reared for their first year in captivity and their growth was documented regularly. Some snakes showed symptoms of disease and a small number died. In June 2000, 66 young dice snakes were released into the nature reserve “Nieverner Wehr (= weir)”, a stepping stone habitat on the River Lahn, that was newly designed in connection with the aforementioned test and development project. Key words. Squamata, Natrix tessellata, western Germany, Rhineland-Palatinate, River Moselle, River Lahn, reintroduction, stepping stone habitat, rearing. Zusammenfassung. In Deutschland ist die Würfelnatter Natrix tessellata vom Aussterben bedroht und besteht aus nur noch drei autochthonen, kleinen, isolierten Populationen im Westen des Landes an den Rhein-Nebenflüssen Mosel, Lahn und Nahe im Bundesland Rheinland-Pfalz. Eine vierte Population im Osten des Landes an der Elbe im Bundesland Sachsen war in der Mitte des 20. Jahrhunderts ausgestorben und wurde im Rahmen des im Folgenden beschriebenen Projektes wiederangesiedelt (Schmidt & Lenz 2001). Von 1997 bis 2001 fand unter der Trägerschaft der Deutschen Gesellschaft für Herpetologie und Terrarienkunde (DGHT) ein Erprobungs- und Entwicklungsvorhaben statt unter dem Titel „Entwicklung und Vernetzung von Lebensräumen sowie Populationen bundesweit bedrohter Reptilien an Bundeswasserstraßen am Beispiel der Würfelnatter an den Flüssen Mosel, Lahn und Elbe“. Das Vorhaben wurde vom Bundesamt für Naturschutz mit Mitteln des Bundesumweltministeriums und von den Ländern Rheinland-Pfalz und Sachsen gefördert (Herzberg et al. 1997). Als Bestandteil dieses sogenannten „Würfelnatterprojekts“ wurde unter anderem die Aufzucht von Würfelnattern in Menschenobhut mit dem Ziel der Wiederansiedlung durchgeführt. In einem Werkvertrag zwischen der DGHT (Auftraggeber) und den Autoren (Auftragnehmer) waren deren Aufgaben genau vorgeschrieben. Es wird im Zusammenhang mit der Haltung und Pflege der Tiere auch über den erforderlichen Zeitaufwand und die Finanzierung des Projektes berichtet. Acht trächtige Weibchen wurden im Juni 1999 im Naturschutzgebiet „Schleuse Hollerich“ an der Lahn gefangen und in Terrarien untergebracht. Nachdem alle je ein Gelege abgesetzt hatten, wurden sie wieder zu ihrem Fundort zurückgebracht. Aus insgesamt 97 Eiern schlüpften 77 Jungtiere, die ein Jahr lang in Zimmerterrarien aufgezogen wurden. Ihr Wachstum wurde regelmäßig dokumentiert. Bei einigen Schlangen traten Krankheitssymptome auf, an denen manche auch verstarben. Im Juni 2000 wurden 66 Würfelnattern im Naturschutzgebiet „Nieverner Wehr“, einem im Zusammenhang mit dem anfangs erwähnten Erprobungs- und Entwicklungsvorhaben neu gestalteten Trittsteinhabitat an der Lahn, ausgesetzt. Schlagwörter. Natrix tessellata, Westdeutschland, Rheinland-Pfalz, Mosel, Lahn, Erprobungs- und Entwicklungsvorhaben, Wiederansiedlung, Trittsteinhabitat, Aufzucht.

Introduction In Germany, dice snakes are threatened by extinction with only three autochthonous, but small and isolated populations remaining in the western Federal State of Rhineland-Palatinate along the Rhine tributaries Moselle, Lahn and Nahe (Gruschwitz & Günther 1996, Gruschwitz et al. 1999, Niehuis 1996). To increase the chance for the long-term survival of these populations, the so-called “Dice Snake Project” was set up by the German Federal Ministry for the Environment, Nature Conservation and Nuclear Safety (BMU) within

the framework of “Testing and Development Projects in Nature Conservation and Landscape Management”. The project was titled “Development and Cross-linkage of Habitats and Populations of Nationally Threatened Reptiles alongside German Federal Waterways, Using the Example of Dice Snakes on the Rivers Moselle, Lahn and Elbe”. A fourth German population existed on the River Elbe in the eastern Federal State of Saxony. It became extinct in the middle of the 20th century, but an attempt to restart a new population with dice snakes from the nearby Czech Republic was part of the aforementioned project (Schmidt & Lenz 2001). The Ger-

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Tab. 1. List of expenses in DM (Deutsche Mark, the German currency before the introduction of the Euro; 1 DM is equivalent to approximately 0,51 Euro). five aqua-terraria (custom made) lease for the shared use of a trout farm for foodfish lease deposit for a second rearing project for 2000 renovation costs for a quarantine room (to house wild-caught females) heating, light, and equipment for the quarantine room and terraria containers and substrate (vermiculite) for incubation food-fish (approx. 30,000 units) mileage allowance (for 4228 km) total Fig. 1. Hatchling.

600 200 50 325 50 6 2199 11,077

Tab. 2. Temporal expenditures in hours.

man Herpetological Society (Deutsche Gesellschaft für Herpetologie und Terrarienkunde, hereafter DGHT) was the head of this project, which was sponsored by the Federal Agency for Nature Conservation, the Federal States of Rhineland-Palatinate and Saxony as well as the RWE Energie AG, an energy producing firm. The latter is using regional water courses as resources and is additionally involved in the protection of the remnant populations of dice snakes. The purpose of this rearing project (see Fig. 1 for a hatchling) was to support the dice snake populations particularly in the nature reserve Dieblich along the River Moselle. Material and Methods Framework In May 1999 a service contract was closed between the DGHT and the authors, in which the framework was laid down. The principal aims involved the rearing of dice snakes, including hibernation and husbandry until their release the subsequent year. On behalf of the DGHT, Sigrid Lenz and Andrea Herzberg were appointed to supervise this project, as both conducted their contemporary field research on the corresponding dice snake populations. The Appendix shows a detailed description of our tasks which was part of the contract. Point one of this description refers to a publication of the Journal of the Cologne Zoo (Gruschwitz et al. 1992), describing the husbandry set up for Natrix tessellata. These guidelines were the binding rules to follow for this project and included the continuous maintenance of the hatchlings and the omission of a forced hibernation to reduce mortality rate with the purpose to release subsequently as many juveniles as possible into their natural habitat.

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furnishing of a quarantine room for the wildcaught females maintenance work for the aqua-terraria of maternal snakes (60 days × 0.5 h) assemblage of the tables and furnishing of the aqua-terraria for the juveniles construction of the fish basins daily checks and feeding of food-fish (approx. 300 days × 0.5 h/day) car mileage (4,228 km) daily care expenditure on dice snakes (feeding and cleaning) (approx. 300 days × 1.5 h/day) weight- and length-measurements (10 × 2 h) total

16 30 8 8 150 42   450 20 724

Financial and Temporal Expenditures The contractually agreed fee for our husbandry work was 12,104.35 DM (Deutsche Mark, the German currency before the introduction of the Euro 1999 (book money), respectively 2002 (cash money), amounting to approximately 6190 Euro (1 DM is equivalent to 0,51129 Euro). The fee was paid in three installments. Our costs (in DM) are listed in Table 1 and the hours invested in the different tasks are listed in Table 2. Provision of Food-Fish The guideline, to rear the young dice snakes solely on live fish, was a logistical challenge. A larger quantity of cold water fish of a suitable size was only available in spring and autumn, when the fish ponds were harvested. For us it proved to be very difficult to feed regu-

Rearing of Dice Snakes

Tab. 3. Length and weight of gravid dice snakes. animal no. 1 2 3 4 5 6 7 8

length [cm] 89,5 81,5 93,5 89,0 82,0 86,0 70,8 82,0

weight [g] 206 147 229 212 161 211 107 135

larly more than 70 small water snakes with a sufficient amount of live fish and this task seemed to be unfeasible during frost periods in the winter. Fortunately, we found a cooperative trout farmer, using a former public swimming pool. Water from a well was constantly flowing through the pool basin, keeping the temperature ≥ 6 °C, even during frost periods. We rented these facilities to keep sufficient live fish for the dice snakes to survive the winter months (Figs. 2 and 3). Fig. 2. Housing of food-fish in the pool basin.

Rearing Report Origin of the Gravid Dice Snakes A group of herpetologists and interested individuals made a first attempt to sample gravid dice snakes from the nature reserve in Dieblich on the River Moselle on 13 June 1999 (Fig. 4). Unfortunately, only juvenile snakes were discovered. Consequently, the group decided to take snakes from a nature reserve about 45 km away from Dieblich named “Schleuse Hollerich” near Nassau on the River Lahn, from where five gravid females were collected on the following day. Another three gravid dice snakes were obtained from the same location on 30 June 1999 (Tab. 3). Fig. 3. Housing of food-fish in separate containers.

Accommodation of Gravid Females

Fig. 4. Group of herpetologists and interested individuals, searching for gravid dice snakes in the nature reserve in Dieblich on the River Moselle, Germany.

To disturb the gravid females as little as possible, they were housed in a separate non-heated room in the basement and daily checks were limited to the bare necessities, such as controlling the behaviour, providing with fresh water, offering food and removing eggs. Six snakes were visibly in the moulting phase. In our long-term experience, the moulting phase of highly gravid female dice snakes indicates a proximate oviposition. This indication helped to assess the reproduction advance, as eggs were clearly palpable only in three snakes (individual snake no. 1, 3, and 6), even though all eight individuals contained fertilized eggs (Tab. 4). We examined the faeces of all dice snakes microscopically for parasites through native preparation (fresh, unfixed and mostly undyed preparation of blood, excreta, secretory prod-

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Tab. 4. Reproduction data of female dice snakes. shedding oviposition clutch size (in- weight of female date date fertile eggs) after oviposition 1 20.06. 01.07. 19(1) 132 2 19.06. 01.07. 7(5) ­-3 20.06. 04.07. 15(0) 120 4 19.06. 04.07. 14(2) 117 5 03.07. 04.07. 12(0) 96 6 27.06. 08.07. 11(0) 134 7 08.07. 11.07. 8(0) 70 8 12.07. 18.07. 11(0*) 89 *The fertility of the eggs of this clutch could not be judged exactly. animal no.

ucts, tissue and contents of organs for microscopical evidence of living pathogenic organisms). Nearly all samples contained microorganisms (flagellates) and eggs of worms (strongylides). After consulting some veterinarians of the “AG Amphibien- und Reptilienkrankheiten” (Working Group for Amphibian and Reptile Diseases) of the DGHT, we dispensed with carrying out antiparasite treatments before oviposition based on their recommendations. The eight animals were housed in five aqua-terraria with the measurements 100 cm x 60 cm x 50 cm (L × W × H). One third of the floor space was partitioned off by a 10 cm high glass wall and subsequently

weight of the clutch 111,7 --­ 101,7 94,6 67,4 69,6 46,3 88,6

hatching date 03.-04.08. 05.08. 06.-07.08. 06.-07.08. 08.-09.08. 10.-12.08. 14.-15.08. 20.-21.08.

duration of number of incubation hatchlings 33-34 13 35 2 33-34 14 33-34 12 35-36 12 33-35 10 34-35 8 33-34 6

filled with water. Since peat has proved to be an attractive oviposition substrate for snakes, it was used as floor cover for the dry sections of the terraria. These sections were furnished with flat pieces of cork bark and slates for shelter as well as branches for climbing. As heat source, we used a 50 Watt heating cable and a 40 Watt incandescent reflector lamp. For additional lighting, strip lights were fixed above the terraria. The temperatures in the individual basins ranged between 22 °C and 35 °C (underneath the lamp) during the day, whereas all heating and lighting was switched off for ten hours during the night. Trout fry of about 10 cm length was offered as food, but none of the gravid females accepted any before oviposition. Oviposition and Return of the Mothers All females shed their skin before oviposition and laid a viable clutch of eggs in the moist peat, both under the slate plates and under the cork bark (Tab. 4). The freshly laid eggs were discovered mostly early in the morning, but in two cases the process was not finished until midday. One or two days after oviposition, the dice snakes began to feed on the trout fry. After a suitable recovery

Fig. 5. Incubator with boxes containing clutches of dice snakes.

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Fig. 6. Clutch of dice snake no. 1, beginning of hatching.

Rearing of Dice Snakes

phase and treatment with 50 mg/kg body weight Panacur® p.o. against nematodes the animals were returned to their place of origin. In our opinion the deworming was necessary, because the parasitic pressure empirically increases in husbandry conditions (Ippen et al. 1985, Mutschmann 2008). Incubation and Hatching The eggs were bedded into moistened vermiculite (one part vermiculite to two parts water). For each clutch of eggs a separate plastic container was used. The incubation temperature in the industrial heating cabinet was constant between 28 and 29 °C (Fig. 5). During the incubation period of 33 to 35 days, photographic documentation of the eggs was carried out every ten days (Fig. 6). The young snakes were weighed and measured immediately after hatching. The weight was between 2.76 g and 5.11 g with an average weight of 4.11 g. The total lengths ranged between 20.2 cm and 26.4 cm, and the average length was 23.4 cm.

Fig. 7. Aqua-terraria to house the hatchlings of dice snakes.

Husbandry and Development of the Young Snakes For the rearing, the young snakes were transferred from the quarantine room to the terraria room. Until registration of the individual data of biometrics, pholidosis and body colour (see Lenz & Gruschwitz 1993b), the young snakes were kept in plastic terraria, separated by clutch origin. The interior consisted of a waterbowl, large enough to function as a bathing basin, and cork bark as shelter. Until the first shedding, which took place six to twelve days after hatching, the small snakes were kept on slightly damp paper towel. Later on we used beechwood chips as substrate. As the room temperature in the terraria room was always between 24 °C and 26 °C during the day, additional heating of the rearing enclosures was not required. First food consumption took place within fourteen days after their first shed. As food-fish we used topmouth gudgeon (Pseudorasbora parva), sunbleak (Leucaspius delineatus) and common carp (Cyprinus carpio) of suitable sizes, later supplemented with goldfish (Carassius auratus), guppies (Poecilia reticulate) and trout fry (Oncorhynchus mykiss). To stimulate the feeding behaviour and for a better control of ingestion, live fish was offered in Petri dishes every one or two days. After the individual registration was completed, we distributed the young snakes according to their body mass amongst the five aqua-terraria which had been previously used for housing the wild-caught females. Prior to this, these terraria were thoroughly disinfected and subsequently filled with beechwood chips as substrate and furnished with flat pieces of cork bark and climbing branches. As heat source we used a 40 Watt incandescent reflector lamp, which was on for twelve hours a day. These terraria were placed in another room (Fig. 7) with

Fig. 8. Juvenile dice snakes sitting on branches.

a daytime temperature of approximately 22  °C, which allowed us to dispense the heating cable we had previously used in the basement. The young snakes preferred to stay under or on the cork bark pieces near the lamp and particularly on the climbing branches (Fig. 8), but fled into the water at the slightest disturbance. Since the dice snake is a diurnal snake in Central Europe (Lenz & Gruschwitz 1993a, Gruschwitz et al. 1999), which frequently basks, we presumed that UV irradiation every one to two days was adequate (light source: Osram Vitalux 300 Watt). The actual radiation time was extended gradually from an initial five to thirty minutes. The daily feeding was later extended to intervals of two to three days. Even in the aqua-terraria we initially used Petri dishes for feeding. But as soon as the snakes began to feed regularly from the Petri dishes, we offered foodfish in the water area of the terraria. The young snakes used a sit-and-wait strategy to forage, while positioned at the edge of the water area or on overhanging branches, and successfully dashed forward to capture their prey. This behaviour was a little bit different from that described in Gruschwitz & Günther (1996), according to whom dice snakes are said to ambush their prey only under water. Smaller fish were devoured directly in the water, larger ones mostly on land or on the branches. Every feeding had to be strictly monitored, because

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ously weighed and measured once a month (Figs. 9 and 10). During the period from early January to mid-June 2000, the adolescent snakes shed their skin about every 34 days. Problems During the Rearing Period

Fig. 9. Increase of weight of hatched dice snakes.

Fig. 10. Increase of length of hatched dice snakes.

of the danger that dice snakes accidentally devour each other because of their voraciousness and food envy, despite of abundant food supply. Most of the accidents happen, when two snakes grab and start to devour the same fish. After the two snake heads meet in the process of ingestion and both being unable or unwilling to release the fish, one of the two snakes continues with the swallowing movement, and hence, devours also the other snake, which is still attached to the fish. Many other attacks happen, when snakes, after getting in contact with fish, take on their smell and therefore are mistaken for prey by the other snakes. Yet some snakes even attack their conspecifics just as they are sensing prey. To monitor their growth, the young snakes were continu-

Already within the first weeks, we noticed, that three of the young dice snakes didn’t gain as much weight as the others. They were separated and subsequently force-fed. A first force-feeding was sufficient for two of them that started feeding by themselves thereafter. The third specimen exhibited skin nodules (Fig. 11), wasted away and died a few weeks later. Two other young snakes died without any evident symptoms of disease during the first weeks. Meanwhile subcutaneous nodes were apparent at four more snakes, one of which died shortly thereafter. A veterinary examination of the two deceased snakes with nodules resulted in the diagnosis of “Pocken” (colloquial for a vesicle disease, not variola). The three surviving animals and three more, which meanwhile displayed the same symptoms, had the nodules surgically removed. Subsequently they were treated with Baytril®. Unfortunately, even several consecutive operations, including aftercare with antibiotics, proved to be unsuccessful. One of the already mentioned animals and one further infected specimen were studied histologically post mortem in the Institute of Veterinary Pathology of the Justus Liebig University, Gießen. Their pathological report revealed the diagnosis of high-grade gout (Urikopathie) and stated that a congenital renal insufficiency could not be excluded. A bacteriological examination of these two snakes and samples of foodfish were conducted as well as an examination of the latter for pollutants (antibiotics and pesticides), but without conclusive results. Blood tests of sick as well as of outwardly healthy snakes revealed increased uric acid levels. Two of the surviving sick snakes showed severe weakness, head trembling and slight coordination problems. A virological examination of one of these animals came up negative, but the diagnosis of gout was confirmed histologically. In total, four of the outwardly sick snakes survived and were handed over to the project management. Release of the Snakes

Fig. 11. Juvenile dice snake with skin nodules.

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The upper nature conservation authority of northern Rhineland-Palatinate in the City of Coblence, called “Struktur- und Genehmigungsdirektion Nord”, ruled that the mixing of dice snakes from the River Moselle with offspring from the River Lahn wasn’t justified in order to maintain genetic integrity of the isolated populations. Such presumptions were confirmed later by unexpected large genetic differences between the populations of Moselle and Lahn (Guicking et al. 2004). Subsequently, it was decided to use the young snakes

Rearing of Dice Snakes

Fig. 12. Release of the young dice snakes into the nature reserve “Nieverner Wehr” at the River Lahn, Germany.

from our project for colonizing a stepping stone habitat on the River Lahn (Herzberg & Schmidt 2001). At the same time, the dice snake population on the River Moselle should be supported by measures to improve its habitat (Lenz & Schmidt 2002). On 15 June 2000, 66 nearly one-year old dice snakes from the current project were released into the nature reserve “Nieverner Wehr” on the River Lahn (Fig. 11, Herzberg & Schmidt 2001). This event was filmed by a television team of the “Südwestfunk” and later featured in the TV-program “Treffpunkt im Grünen”. Discussion The husbandry project with dice snakes has rendered us a couple of valuable information. For example, now we refrain from using beechwood chips as floor substrate for terraria. Although they are considered to be relatively sterile, they become mouldy at the slightest contact with moisture. Moreover, small wood chips easily adhere to food and, when ingested by the snakes, could lead to obstruction, serious internal injuries or even to death. We were able to prevent this during our project, because we supervised the feeding and immediately removed any particles sticking to the food-fish. Keeping snakes in groups may pose problems during the feeding process. To prevent the risk of mutual swallowing, the animals should be separated for feeding, which causes stress. In our experience, many snakes, in particular mammal feeding species, which are fed in intervals of one week or more, can be easily separated. Fish-eating snakes, which have to be fed in shorter intervals of two or three days, would have to be disturbed more frequently. But each husbandry situation requires an individual assessment of their modus. Moreover, it is difficult to organize the separation of a large number of snakes to feed with live fish. In our opinion, warm hibernation was not the best precondition for reintroduction of dice snakes into the wild. Kirmse (1994) explicitly emphasizes the impor-

tance of cold hibernation for our native reptiles. Concerning a conservation project for the green lizards (Lacerta v. viridis) in Brandenburg, Germany, he describes the danger for animals being released into the outdoors after spending the winter in warm terraria. When released outdoors in the early summer, the lizards vanished to hibernation, stimulated by the cool nights still occurring during this period. Not until August, the lizards surfaced again and became active. When temperatures decreased during autumn, they did not burrow deep enough for hibernation. They were freezing or starving to death. Likewise, the green lizards and European pond terrapins (Emys orbicularis) maintained in the conservation station Rhinluch/Brandenburg in indoor terraria, will categorically be released into nature only in spring after a cold hibernation period (N. Schneeweiss pers. comm.). During our long-term husbandry of various species of snakes, we never experienced a case of gout. We think, it is quite unusual for young snakes, whose mothers were wild-caught, to fall ill of gout, in some cases even before their first intake of food (see “Problems during the rearing period”). According to Gruschwitz (pers. comm.), these symptoms are already known in dice snakes from the nature reserve “Schleuse Hollerich” on the River Lahn. It might be supposed, that these are temporary or local effects related to environmental stress (Gautschi et al. 2002), or in the worst case, are already the signs of an inbreeding depression (Gucking et al. 2004). Acknowledgements For valuable advice, endeavours and voluntary help, we are especially grateful to the following members of the AG Reptile Diseases of the DGHT: Silvia Blahak, Staatliches Veterinäruntersuchungsamt Detmold, Udo Hetzel, Institute of Veterinary Pathology of the Justus Liebig University Gießen, Susanne Fleck, Hanau, Gunther Köhler, Senckenberg Research Institute and Natural History Museum, Frankfurt/ Main, Hans-Dieter Lehmann, Hirschberg, Frank Mittenzwei, Biebergemünd, Frank Mutschmann, Berlin, Walter Sachsse, Institute of Genetics of the Johannes Gutenberg University Mainz, Jutta Wiechert, Mainz and Peernel Zwart, EK Bunnik, Netherlands. Further we would like to thank Angelika and Siegfried Troidl, Fürth, for editing our pictures, Sabine Eilberg, Wallmerod, and Rudi Heins, Bilkheim, for assisting in the translation and particularly Konrad Mebert, Merenschwand, Switzerland, for his constructive reviews of our manuscript. References Gautschi, B., Joshi, J., Widmer, A. & J.C. Koella (2002): Increased frequency of scale anomalies and loss of genetic variation in serially bottlenecked populations of the dice snake, Natrix tessellata. – Conservation Genetics 3: 235-245 Gruschwitz, M. & R. Günther (1996): Würfelnatter – Natrix tessellata. – In: Günther, R. (Ed.): Die Amphibien und Reptilien Deutschlands. – Gustav Fischer Verlag, Jena, Germany: 684–699.

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Dietmar Trobisch & Andrea Gläßer-Trobisch Gruschwitz, M., Lenz, S., Jes, H. & G. Nogge (1992): Die Nachzucht der Würfelnatter (Natrix tessellata Laurenti, 1768) im Aquarium des Kölner Zoos – Ein Beitrag zum Artenschutz. – Zeitschrift des Kölner Zoo 35(3): 117–125. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1786) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Guicking, D., Herzberg, A. & M. Wink (2004): Population genetics of the dice snake (Natrix tessellata) in Germany: implications for conservation. – Salamandra 40(3/4): 217–234. Herzberg, A., Lenz, S. & H.-J. Schäfer (Ed. DGHT)(1997): Flussauen und Würfelnatter – Entwicklung neuer Lebensräume an Bundeswasserstraßen. – DGHT, Rheinbach, Germany. Herzberg, A. & A.D. Schmidt (2001): Bericht zum Stand des Erprobungs- und Entwicklungsvorhabens „Würfelnatter“ der DGHT – 2. Teil: Erprobungsstandort Lahn. – Elaphe 9(4): 73– 80. Ippen, R., Schröder, H.-D. & K. Elze (1985): Handbuch der Zootierkrankheiten. Vol. 1 – Reptilien. – Akademie-Verlag, Berlin, Germany. Kirmse, W. (1994): Zur aktuellen Situation der brandenburgischen Smaragdeidechse (Lacerta v. viridis). – Die Eidechse 5(11): 2–4.

Lenz, S. & M. Gruschwitz (1993a): Zur Autökologie der Würfelnatter, Natrix t. tessellata (Laurenti, 1768) in Deutschland. – Mertensiella 3: 235–252. Lenz, S. & M. Gruschwitz (1993b): Zur Merkmalsdifferenzierung und -variation der Würfelnatter, Natrix t. tessellata (Laurenti, 1768) in Deutschland. – Mertensiella 3: 269–300. Lenz, S. & A.D. Schmidt (2002): Bericht zum Stand des Erprobungs- und Entwicklungsvorhabens „Würfelnatter“ der DGHT – 3. Teil: Erprobungsstandort Mosel. – Elaphe 10(1): 53–59. Mutschmann, F. (2008): Erkrankungen bei Schlangen. – Edition Chimaira, Frankfurt am Main, Germany. Niehuis, M. (1996): Würfelnatter – Natrix tessellata (Laurenti, 1768). – In: Bitz, A., Fischer, K., Simon, L., Thiele, R. & M. Veith (Eds.): Die Amphibien und Reptilien in RheinlandPfalz, Vol. 2 – GNOR-Eigenverlag, Landau, Germany: 429– 450. Schmidt, A.D. & S. Lenz (2001): Bericht zum Stand des Erprobungs- und Entwicklungsvorhabens „Würfelnatter“ der DGHT – 1. Teil: Erprobungsstandort Elbe. – Elaphe 9(3): 60– 66.

Authors Dietmar Trobisch, Andrea Gläßer-Trobisch, Hauptstraße 7, 56414 Bilkheim, Germany, e-mail: [email protected]

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Appendix Part of the service contract that describes the husbandry guidelines of protected dice snakes for the purpose of reintroduction (in German).

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20 September 2011

ISBN 978-3-9812565-4-3

Das sächsische Vorkommen der Würfelnatter im Elbtal bei Meißen Fritz Jürgen Obst & Peter Strasser Zusammenfassung. Die Entdeckung des isolierten Vorkommens der Würfelnatter bei Meißen durch F.A. Thiel im Jahre 1883 und der Übernahme dieser faunistischen Neuigkeit in die zoologische Literatur werden beschrieben. Ebenso wird die spezielle geographische und klimatische Situation des Würfelnatter-Habitats bei Meißen dargestellt und der Zusammenhang dieses Isolats mit den Vorkommen der Art im Flusssystem der Elbe und an deren Nebenflüssen Eger (Ohře), Moldau bzw. Berounka in der tschechischen Republik erörtert. Anschliessend wird das Schicksal der Meißner Population durch ständige anthropogene Beeinträchtigungen bis hin zu weitgehender Habitatszerstörung durch Strassenbaumassnahmen und zum Erlöschen der Population um 1936/38 beschrieben. In den Jahren 1999/2000 erfolgt im Rahmen eines deutschlandweiten Projekts zugunsten der Würfelnatter ein Wiederansiedlungsversuch an der Elbe bei Meißen. Insgesamt 152 Individuen, die zum kleineren Teil Wildfänge, zum grösseren Teil Gefangenschaftsnachzuchten von Würfelnattern von der Eger (Ohře) und der Berounka in der Tschechischen Republik waren, wurden in Meißen ausgesetzt. Die wieder angesiedelte Population erlitt durch starken Strassenverkehr, durch Habitatsverkleinerung und durch das Extrem-Hochwasser der Elbe von 2002 starke Verluste. Gegenwärtig befindet sie sich mit der geschätzten Maximalgrösse von 25 Exemplaren im existentiellen Grenzbereich. Auf Grund der anhaltenden negativen Einflüsse kann keine zuverlässige Prognose für eine positive Zukunft gegeben werden. Schlagwörter. Natrix tessellata, Meißen, Geschichte, Status der Populationen Summary. The discovery of an isolated population of the dice snake near Meißen by F.A. Thiel in 1883 and the entering of this faunistic novelty into the zoological literature are described. The particular geographical and climatic situation of the dice snake habitat at Meißen is portrayed and the connection of this isolate with the occurrence of the species in the river system of the Elbe and its tributaries Eger (Ohře), Vltava and Berounka, respectively, in the Czech Republic is discussed. This is followed by a description of the fate of the Meißen population that was marked by continuous anthropogenic impairment up to the near-complete destruction of its habitat through the construction of roads and ended with the extinction of the population around 1936/38. In 1999/2000, a reintroduction project that covered the whole of Germany saw the attempt of re-establishing the dice snake along the River Elbe at Meißen. A total of 152 individuals were released in Meißen, consisting for a smaller part of wild-caught and for a larger portion of captive-bred specimens of dice snakes from the rivers Eger (Ohře) and Berounka in the Czech Republic. The reintroduced population subsequently suffered severe losses through high traffic volumes on the roads, shrinking habitats, and the extreme floods of the Elbe in 2002. Estimated at presently comprising a mere 25 specimens at maximum, it is at its existential limits. As negative influences continue to be exerted, no reliable prognosis for a more positive future can be suggested. Key words. Natrix tessellata, Meißen, history, population status.

Die Entdeckung des Vorkommens In deutschen Faunenwerken tauchte ab der Jahrhundertwende 1900 zum rheinischen Vorkommen der Würfelnatter nun auch ein Hinweis auf die Art in Sachsen an der Elbe bei Meißen auf. Urheber der „publizistischen Welle“, auf der die sächsischen Würfelnattern bis in unsere Tage durch die faunistische Literatur Deutschlands schwammen, war Fickel (1893) mit seiner Arbeit „Die Literatur über die Tierwelt des Königreichs Sachsen“. Wenige Jahre später nahm Geisenheyner (1898) die Gelegenheit wahr, die von Fickel mitgeteilte Existenz einer Würfelnatter-Population bei Meißen im „Zoologischen Garten“, einer weit verbreiteten und renommierten deutschen zoologischen Zeitschrift, der breiten Öffentlichkeit bekannt zu machen. Die Würfelnatter bei Meißen an der Elbe ist der nordwestlichst iso-

lierte Fundpunkt dieser Art mit einer deutlichen Distanz von ca. 83 km zu den nächstgelegenen, böhmischen Populationen (Tschechien) am Oberlauf der Elbe und ihrer Zuflüsse Eger und Moldau und der noch grösseren Disjunktion (400 km) zu den rheinländischen Würfelnatter-Isolaten im Westen Deutschlands. Damit war die Voraussetzung gegeben, dass die Meißener Würfelnattern aufgrund ihrer zoogeografischen und faunistischen Bedeutung immer wieder in Faunenwerken unterschiedlichster Art erwähnt wurden. Allerdings blieb es bei kurzen, z.T. repetitiven Hinweisen, während ein kontinuierliches Berichten über das Schicksal dieser Population unterlassen wurde. Der eigentliche Entdecker der Würfelnatter bei Meißen war ein Modelleur der Königlichen Porzellanmanufaktur Meißen, Ferdinand August Thiel (1839– 1920). Die erste Veröffentlichung seiner Würfelnatter-

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Fritz Jürgen Obst & Peter Strasser

Abb. 1. Die erste Veröffentlichung eines Würfelnatter-Fundes in einer Beilage zum „Meißner Tageblatt“: (oben) Frontseite der Beilage, (unten) Ausschnitt mit Absatz über den Würfelnatter-Fund. Fotos: Peter Strasser. Fig. 1. The first publication of a find of the dice snake in a supplement to the newspaper, “Meißner Tageblatt”: (above) Front page of the supplement, (below) snippet containing the note on the find of the dice snake. Photographs: Peter Strasser.

Abb. 2. Das einzige erhaltene Präparat der Würfelnatter von Meißen aus dem Senckenberg-Museum, Frankfurt/Main: (oben) Präparatglas mit der Nummer aus der Privatsammlung von Oskar Boettger, (Mitte) dorsale Ansicht des Präparats, (unten) ventrale Ansicht. Fotos: Frank Höhler, Staatl. Museum f. Tierkunde, Dresden. Fig. 2. The only preserved specimen of a dice snake from Meißen still in existence, in the Senckenberg Museum collection, Frankfurt/Main: (above) Storage glass with the number from the private collection of Oskar Boettger, (middle) dorsal view of the specimen, (below) ventral view. Photographs: Frank Höhler, Staatl. Museum f. Tierkunde, Dresden.

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Geschichte der Würfelnatter bei Meißen, Deutschland

Abb. 3. Die Elbe bei Meißen. Schiffszieher („Bomätscher“) an der Engstelle „Knorre-Felsen“, dem Würfelnatter-Habitat im ursprünglichen Zustand. Radierung von C.G. Ehrlich, 1770. Foto: Peter Strasser. Fig. 3. The River Elbe at Meißen. Tow-roper at the river narrow “Knorre Rock” with the dice snake habitat in its original condition. Etching by C.G. Ehrlich, 1770. Photograph: Peter Strasser.

Abb. 4. (Beschreibung siehe nächste Seite) Fig. 4. (Description see next page)

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Abb. 6. Blick auf den Meißner Winterhafen für kleinere Nutz- und Sportschiffe, der durch eine Dammaufschüttung abgegrenzt ist, Juni 2010. Foto: Konrad Mebert. Fig. 6. View of the Meißen winter Harbour for smaller commercial and leisure vessels with its artificial dyke in June of 2010. Photograph: Konrad Mebert.

Abb. 5. Der Fürstengraben, ein reichlich wasserführender Bach, der den östlichen Beginn des Würfelnatter–Habitats markiert. Foto: Konrad Mebert. Fig. 5. The “Fürstengraben”, a substantial stream, marks the eastern limits of the dice snake habitat. Photograph: Konrad Mebert. Abb. 4 (linke Seite): Überblick über das Würfelnatter-Habitat in Meißen: (oben) Links im Bild das alte Gasthaus „Zur Knorre“, rechts der Strassendurchbruch, dann der Rest des abgetragenen Knorre-Felsens mit der Benno-Kanzel auf seiner Spitze, dann der Uferbereich vor den Weinbergs-Terrassen des Katzensprungs, Einmündung des Meißner Winterhafens in Höhe des Dampfers, mit einer rot-weissen Stange markiert; rechts im Bild die gebogene Mole des Meißner Winterhafens; (unten) Habitat-Abschnitt am Winterhafen. Gut erkennbar am Fusse des Strassen-Geländers das helle Metall-Abweissystem, welches das Schlangenhabitat zum Fluss bzw. zum Hafenbecken begrenzt, während das xerotherme Hinterland des „Katzensprung“-Weinbergs dadurch für die Schlangen abgeriegelt ist. Fotos: Peter Strasser. Fig. 4 (left page): Overview of the dice snake habitat in Meißen: (oben) the old tavern “Zur Knorre“ on the left, the road cut on the right, followed by the remainder of the removed Knorre Rock with the Benno Pulpit on its peak, then the embankment area in front of the vineyard terraces of the “Katzensprung”, and the outlet of the Meißen “Winter Harbour” marked with a red and white pole at the level of the steamer; the curved pier of the Meißen “Winter Harbour” on the right of the picture; (unten) portion of the habitat at the winter harbour. The lightcoloured metal deflector system, which delimits the snake habitat from the river and the harbour basin, respectively, and effectively prevents the snakes from entering the xerothermic hinterland of the Katzensprung vineyard, is well visible at the bottom of the road railing. Photographs: Peter Strasser.

Abb. 7. Die 400 m lange Dammaufschüttung begünstigt einen grossen Ruhigwasserbereich, der einen optimalen Laichplatz für prädestinierte Fischarten der Elbe darstellt und den Würfelnattern aller Altersklassen als Jagdgrund dienen dürfte. Foto: Konrad Mebert. Fig. 7. The 400 m artificial dyke facilitates a large area of calm water that makes for an optimal spawning site for selected fish species of the River Elbe and likely forms a rich hunting territory for dice snakes of all age classes. Photograph: Konrad Mebert.

Funde erfolgte am 4. Oktober 1892 in einer Beilage zum „Meißner Tageblatt“ (Anonymus 1892a, Abb. 1a, b). Einen Tag später übernahm der überregionale „Dresdner Anzeiger“ (Anonymus 1892b) diese Meldung. Dieser Bericht diente Fickel (1893) für seine bibliografische Übersicht zur sächsischen Fauna. Schliesslich übernahm Geisenheyner (1898) diese Information, die er allerdings durch briefliche Nachfragen beim Informanten Thiel mit interessanten Details versehen konnte. So

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Abb. 8. Überblick des Würfelnatter-Habitat in Meißen zur Zeiten der Beobachtungen von Arthur Klengel, 1927. Urheber Verlag Brück und Sohn Meißen. Reproduktion: Peter Strasser. Fig. 8. Overview of the dice snake habitat in Meißen at the time of the observations by Arthur Klengel, 1927. Adopted from the publishing house, Urheber Verlag Brück und Sohn Meißen. Reproduction: Peter Strasser.

gibt Geisenheyner an, dass Thiel seine ersten Würfelnatter-Funde bereits neun Jahre vor der Publikation, also im Oktober 1883 gemacht hatte. 1892 übergab Thiel der „Naturwissenschaftlichen Gesellschaft ISIS zu Meißen“ zwei in Alkohol konservierte Beleg-Exemplare seiner Meißner Würfelnattern, die anschliessend zu Geisenheyner nach Bad Kreuznach geschickt wurden und über Geisenheyner schliesslich zu Oskar Boettger (1844–1910) nach Frankfurt/Main gelangten.

Abb. 9. Würfelnatter-Habitat mit der Schotterbank vor dem Knorre-Felsen im 2008. Das limitierende Abweis-System ist vor der Strasse gut sichtbar. Foto: Peter Strasser. Fig. 9. Dice snake habitat with the gravel shore in front of the Knorre Rock in 2008. The limiting deflector system can be seen in front of the road. Photograph: Peter Strasser.

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Boettger war damals eine renommierte Autorität in der kleinen herpetologischen Szene Deutschlands. Boettger übergab diese Belegexemplare, die er zunächst seiner privaten Sammlung einverleibt hatte, im Jahre

Abb. 10. Kernzone des Würfelnatter-Habitats 2008 mit Weinbergterrasse. Links ist die Befestigungsmauer unterhalb der Uferstrasse zu sehen. Das graue Band entlang der Strasse zeigt das Abweis-System mit Metallplanken. Foto: Peter Strasser. Fig. 10. Core zone of the dice snake habitat with a vineyard terrace in 2008. On the left is the retaining wall below the embankment road visible. The grey band along the road marks the deflector system of metal strips. Photograph: Peter Strasser.

Fritz Jürgen Obst & Peter Strasser

Abb. 11. Die Steinbefestigung des Uferhabitats war teilweise mit Beton versiegelt, ist aber wie hier über große Flächen lückig gefügt, Juni 2010. Foto: Konrad Mebert. Fig. 11. The rocky solidification of the embankment habitat was partly sealed with concrete, but large patches, such as shown here, are full of gaps, June of 2010. Photograph: Konrad Mebert.

1900 geschenkweise an seine Dienststelle, das Senckenberg-Museum Frankfurt a. M. Eines der beiden Präparate ist heute noch unter der Nummer SMF 17456 im Senckenberg-Museum erhalten und stellt den einzigen verfügbaren historischen Beleg für das Vorkommen bei Meißen dar (Abb. 2a, b, c). Thiel konnte in den Jahren 1894 und 1896 weitere Würfelnattern an seinem Meißner Fundpunkt sammeln, darunter auch ein trächtiges Weibchen als Beleg für die Reproduktion dieser Population, wie Geisenheyner ebenfalls mitteilt. Das Habitat der Meißner Würfelnattern Das historische Habitat ist ein rechts der Elbe unterhalb Meißens gelegener Uferabschnitt von 600–700 m Länge. Hier lenkt ein inselartiges Felsmassiv, der Bocksberg (169 m M.ü.M), den von Südost nach Nordwest verlaufenden Elbstrom stark westlich ab, so dass das Prallufer des Stroms nahezu parallel zur südexponierten Hanglage des Bocksberges verläuft. Die Hanglagen des

Bocksberges werden seit Jahrhunderten als terrassierte Steilhang-Reblagen genutzt. Im Bereich des Würfelnatter-Vorkommens heisst die Reblage „Katzensprung“ und gilt als eine der besten Lagen im Meißner Weinbau-Gebiet, vermutlich als Folge eines besseren Mikroklimas (generell höhere Temperaturen), begünstigt durch die Exposition des Hanges. Sowohl die Neigung wie auch die zum Sonnenverlauf angenähert parallel gegebene Hanglage fördern eine höhere Absorption und längere Aufnahme der Sonnenstrahlung. Westlich läuft der Bocksberg in den elbufernahen Knorre-Felsen aus (Abb. 3, 4a). Der Bocksberg selbst ist Teil des Meißner Syenodiorit-Granit-Massivs, das elbaufwärts und elbabwärts von Meißen durch markante Berge mit Felsabhängen, die vorwiegend durch jahrhundertelangen Steinbruchbetrieb entstanden sind, die Weitung des Dresdner Elbtalkessels abschliesst und die Elbe über mehrere Kilometer wieder in ein gewundenes Tal zwängt. Diese Berge sind an ihren südlichen Abhängen deutlich klimatisch begünstigt und in der lokalen Floristik und Faunistik

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Abb. 12. Überfahrene subadulte Würfelnatter am 18 Juni 2010 vor der Brücke über den Fürstengraben. Foto: Peter Strasser Fig. 12. Road-killed subadult dice snake found near the bridge across the Fürstengraben on 18 June 2010. Photograph: Peter Strasser

als Habitate submediterraner und anderer thermophiler Arten bekannt. Das betrifft in zoologischer Hinsicht am Bocksberg insbesondere wirbellose Tiere, wie z. B. die Schnirkelschnecke Cepaea vindobonensis oder die Ameisen-Arten Leptothorax affinis und Camponotus caryae fallayi, die Weissfleckige Zartschrecke (Leptophyes albovittata) und verschiedene wärmeliebende Bockkäfer-Arten, unter denen besonders der Purpurbock (Purpuricenus kaehleri) zu nennen wäre (Klausnitzer 1982). Der Bocksberg läuft im Bereich des WürfelnatterHabitats westlich in den Knorre-Felsen aus, der vor der Stromregulierung im 19. Jahrhundert sogar bis in den Flusslauf der Elbe als Schifffahrts-Hindernis hineinragte (Abb. 4a). Bis zum teilweisen Abbruch des KnorreFelsens zwischen 1936 und 1938, der für den Bau der Fahrstrasse parallel zum Flusslauf durchgeführt wurde, verlief dort zwischen dem Uferbereich der Elbe und den Weinbergsterrassen des „Katzensprungs“ lediglich ein schmaler Treidlerweg (ein Weg für die Schiffszieher entlang des Flussufers, Abb. 3). Die Krönung des Knorre-Felsens, die massig-felsige sogenannte „Benno-Kanzel“, blieb aber glücklicherweise erhalten, ebenso die reichen Kuhschellen-Bestände (Pulsatilla pratense) auf dem Felsen. Am östlichen Beginn des Würfelnatter–Habitats mündet ein reichlich wasserführender Bach, der sogenannte „Fürstengraben“, in die Elbe (Abb. 5). In seinem Oberlauf führt dieser Zufluss den Namen „Niederauer Dorfgraben“. Der Mündungsbereich dieses Baches wurde durch den anprallenden Elbstrom zu einem sich gut erwärmenden Laichgewässer für Elbfische angestaut. Das war für die Ernährung der Würfelnatter-Population eine gute Voraussetzung. Diese Situation verbesserte

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sich noch, als 1875 der Mündungsbereich des Fürstengrabens durch eine 400 m lange Dammaufschüttung gegen den Strom zum Meißner Winterhafen für kleinere Nutz- und Sportschiffe ausgebaut wurde und damit ein grosser Ruhigwasserbereich als optimaler Laichplatz für dafür prädestinierte Fischarten der Elbe entstand (Abb. 4b, 6, 7). Zum Zeitpunkt der Entdeckung der Meißner Würfelnatter-Population war deren Habitat durch eine störungsfreie Verbindung des Ufer-Lebensraumes und Wasser-Jagdreviers der Schlangen am Elbufer selbst und im Mündungsbereich des Fürstengrabens mit dem Landhabitat in den xerothermen Legestein-Terrassen des dahinterliegenden Weinbaugebietes charakterisiert, die den Schlangen als Wärme- und Eiablage-Plätze und als hochwassersicheres Überwinterungsgebiet dienten. Der südexponierte Knorre-Felsen des Bocksberges war damals wie heute der wichtigste Faktor für die Gewährleistung des xerothermen Kleinklimas in wesentlichen Teilen des Würfelnatter-Habitates. Die herpetologische Begleitfauna der Würfelnatter in ihrem Meißner Habitat bestand damals wie heute zunächst aus den Amphibien Erdkröte (Bufo bufo), die im gesamten Bereich anzutreffen ist, und einer Seefrosch-Population (Pelophylax ridibundus), die im warmen Wasser des Winterhafens lebt. Die Reptilien haben in der allgegenwärtigen Zauneidechse (Lacerta agilis), die individuenreich in den Weinbergsterrassen, genauso aber auch auf der grasbewachsenen Hafenmole des Winterhafens lebt, ihren auffälligsten Vertreter. Während des Jahrhundert-Hochwassers im August 2002 flüchteten die Zauneidechsen von der Hafenmole zum Teil auf Treibgut im Elbstrom (Prokoph 2003). Die Blindschleiche (Anguis fragilis) ist in den etwas bodenfeuchteren Teilen des Würfelnatter-Habitats zu finden. Auch die Glatt- oder Schlingnatter (Coronella austriaca) tritt regelmässig am Hang des Bocksbergs und in den Weinbergsterrassen auf. Als weitere Schlange kommt im Bereich des Winterhafens und des Fürstengrabens die Ringelnatter (Natrix natrix) vor. In den letzten Jahren sind im Meißner Winterhafen einige Exemplare nordamerikanischer Schmuckschildkröten (Trachemys scripta ssp.) als allochthone Reptilien aufgetreten. Eine Reproduktion dieser Schildkröten konnte bislang nicht beobachtet werden. Zur politischen Zuordnung des Würfelnatter-Habitats wäre noch anzumerken, dass der Bocksberg Flurbereich der damals selbständigen Gemeinde Proschwitz war. Sie grenzt an die Siedlung Niederfähre, eine kleine Elbfischer- und -schiffer-Gemeinde, die bereits 1890 in die grosse rechtselbige Gemeinde Cölln, die vis-avis zum linkselbigen Meißen gelegen war, eingemeindet wurde. Cölln vereinigte sich 1901 mit Meißen, das seitdem zu beiden Seiten des Elbstroms gelegen ist. Erst 1994 wurde Proschwitz nach Meißen eingemeindet, so dass erst seitdem das Würfelnatter-Habitat auch Stadtflur von Meißen ist.

Fritz Jürgen Obst & Peter Strasser

Das Schicksal der Meißner Würfelnatter-Population nach 1900 bis zum Erlöschen Der nächste Lokal-Faunist, der sich mit den Würfelnattern von Meißen befasste, war 1910 und noch einmal 1922, Rudolf Zimmermann (1887–1943). Er berichtete damals, dass es ihm allerdings nicht gelungen sei, selbst Würfelnattern zu beobachten. Offenbar war zu diesem Zeitpunkt die Schlangenpopulation schon so klein, dass Zimmermann die Bestätigung des Vorkommens misslang. Es ist zu vermuten, dass die infolge der aufblühenden Industrie im rechtselbigen Meißen und die unkontrollierten Abflüsse von Industrie-Abwässern als GiftSchübe immer wieder zu Fisch-Sterben führten, die der Würfelnatter-Population als Endglied einer Nahrungskette schwer zugesetzt haben. Sie müssen als wichtiger Faktor gelten, der zum starken Rückgang der Population führte. In den Folgejahren war es der Meißner LokalFaunist und Heimatforscher Arthur Klengel (1881– 1954), der 1919 und 1932 über seine Beobachtungen der Würfelnattern berichtet. Ihm verdanken wir insbesondere die wiederholten Beobachtungen, dass sich die Schlangen nach ihrer Fischjagd in die Legesteinmauern der Weinbergsterrassen zurückgezogen haben (Abb. 8). Leider fehlen uns Dokumentationen, die die Auswirkungen der massiven Veränderungen des Habitats durch die bereits erwähnten Durchbruchsarbeiten am Knorrefelsen für den Strassenbau 1936–1938 belegen. Die neue Strasse wurde durch eine mehrere Meter hohe abgeschrägte Steinbefestigung gegen den Strom geschützt, so dass auch das Uferhabitat massiv verändert wurde (Abb. 9, 10). Die Steinbefestigung war teilweise mit Beton versiegelt, über grosse Flächen hingegen lückig gefügt, so dass gute Rückzugsplätze für die Schlangen zugängig blieben (Abb. 11). Es ist sehr wahrscheinlich, dass aber vor allem die entstandene Unterbrechung zwischen dem Fluss- und Landhabitat die Würfelnatter-Population zum Erlöschen gebracht hat. Die xerothermen Hänge des Katzensprungs haben für die Optimierung des Wärmehaushaltes der Schlangen nach den Jagdgängen in der meist suboptimal kühlen Elbe eine herausragende Bedeutung. Dabei wurde die asphaltierte Fahrstrasse in doppelter Sicht zum Verhängnis: einerseits lud die aufgewärmte Asphaltdecke die Schlangen bereits zum Verweilen und Aufwärmen ein und minderte ihr Bestreben, schnell in die schützenden Legestein-Mauern zu gelangen, andererseits wurden die Schlangen leicht zum Opfer des Autoverkehrs, ganz gleich, ob sie die Strasse nur überqueren oder ob sie diese gar als Aufwärme-Platz nutzen wollten und liegenblieben (Abb. 12). Ausserdem haben die Felssprengungen und der Transport des beträchtlichen Abraums sowie dessen partielle Verbauung zu einer Hochufer-Strasse entlang des Katzensprungs sicherlich einer beträchtlichen Individuen-Anzahl der kleinen Würfelnatter-Population damals unmittelbar das Leben gekostet. Die limitierte Grösse des Habitats

sowie die Gefahr für eine Inzucht bei einer solch kleinen Population waren weitere Faktoren, die den Niedergang dieser Population beeinflusst haben könnten. Nach dem Zweiten Weltkrieg besuchte der aus Radebeul bei Dresden stammende Zoologe Ehrhard Frommhold (1925–1980) in den 1950er Jahren wiederholt das Würfelnatter-Habitat, ohne dass ihm ein Wiedernachweis der Schlangen gelang (pers. Mitt. an Obst). Da Frommhold einerseits die Hoffnung, doch noch einmal die Würfelnatter wiederfinden zu können, noch nicht endgültig begraben wollte, und ihm andererseits klar war, wie schwer die Beweisführung für die Postulierung des Erlöschens zu erbringen sei, verzichtete er auf eine Publikation seiner Befunde. Zum anderen verhinderte die Verlegung seines Wohnsitzes nach Cottbus und später nach Halberstadt weitere Recherchen vor Ort. Erst 1969 gelangte durch Eberhardt Pietzsch, einem Dresdner Amateur-Biologen, eine neue Meldung zur Meißner Würfelnatter in der Zeitschrift „Deutscher Angelsport“ in Umlauf. Pietzsch behauptete, die Würfelnatter im linkselbig gelegenen Saubach-Tal, einem kleinen, kühlen Elbezufluss, wiederentdeckt zu haben. Sein ausführliches Manuskript zu diesem „neuen Fundpunkt“ gelangte 1970 über die Berliner Zoologen Prof. Dr. Heinrich Dathe (1910–1991) vom Berliner Tierpark und Prof. Dr. Günther Peters (1932), dem damaligen Herpetologen des Berliner Museums für Naturkunde, zum Zwecke eventueller Publikation an das Staatl. Museum für Tierkunde nach Dresden. Dort nahm der ältere Mitautor vorliegenden Beitrages (Obst) die Überprüfung des Sachverhaltes vor und führte in den Jahren 1970–74 zahlreiche Exkursionen an den „neuen Fundpunkt“ sowie an die klassische Lokalität an der Knorre/ Katzensprung bei Meißen durch. Die negativen Ergebnisse und die Schlussfolgerung, dass die WürfelnatterPopulation von Meißen definitiv erloschen sei, wurden von Obst 1976 publiziert. Er schloss sich in dieser Arbeit auch der bereits von Geisenheyner (1898) und Mertens (1947) geäusserten Ansicht an, dass das ehemalige Meißner Würfelnatter-Vorkommen eine Reliktvorkommen aus einem inter-, bzw. postglazialen Ausbreitungs-Optimum der Art sein müsse und keinesfalls eine Neubesiedelung aus historischer Zeit darstelle. Diese Einschätzung korrespondiert auch mit der Bewertung mitteleuropäischer Vorkommen der Aeskulapnatter (Zamenis longissimus) als Relikte solcher Warmzeiten (Mlynarski 1961a, b), wie sie im Atlantikum, also vor ca. 6000 bis 10’000 Jahren BP, herrschten (Wikipedia 2010). Eine trittsteinartige Vernetzung des Meißner Vorkommens der Würfelnatter mit den in 100 km bzw. 150 km stromaufwärts Meißens gelegenen Fundpunkten der Art in der Tschechischen Republik hat sich in neuerer Zeit niemals nachweisen lassen. Ein ursprünglicher Zusammenhang dieser reliktären Populations-Kette ist hingegen sehr wahrscheinlich.

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Die Wiederansiedlung der Würfelnatter bei Meißen 1999/2000 Den gedanklichen Ursprung für das Wiederansiedlungs-Projekt der Würfelnatter von 1999/2000 lieferte bereits Obst (1989), der aufgrund der Untersuchungen Laňkas (1978) zur Situation der Würfelnatter in der damaligen Tschechoslowakei und von Gruschwitz (1978) zur Situation der Würfelnatter in den rheinlandpfälzischen Populationen an der Mosel und der Lahn zum Schluss kam, dass die Kriterien für ein funktionsfähiges Würfelnatter-Habitat nach Gruschwitz (1978) wieder erfüllt werden bzw. mit leistbarem Aufwand erfüllbar sind. Folglich müsste ein WiederansiedlungsVersuch auf der Basis von Ursprungs- bzw. Nachzuchttieren aus tschechischen Populationen (vom Fluss-System der Elbe) vertretbar sein. Die Begründung der „Rekonstruktion eines Naturdenkmals“ gegenüber berechtigten zoologischen Einwänden (z. B. fehlendes Habitat, Einführung fremder Tiere), wurde von Obst (1989) bewusst in den Kontext zur Diskussion über die Sinnhaftigkeit der Rekonstruktion verlorener historischer oder künstlerischer Denkmale gesetzt, die letztlich alle nur aus dem subjektiven philosophischen Standpunkt der Erhaltung naturnaher Zustände oder deren Wiederherstellung, aus dem festen Willen der Ausführenden und wegen deren herpetologischen Interessen begründbar sind. In der Endphase der DDR mit ihren gravierenden wirtschaftlichen Schwierigkeiten war allerdings an die Realisierung der Wiederansiedlung einer Schlangenart nicht mehr zu denken. Die unmittelbar nach dieser letzten Publikation zur Meißner Würfelnatter folgende politische Wende 1989 und der Beitritt der DDR zur Bundesrepublik Deutschland im Jahre 1990 brachten es mit sich, dass Michael Gruschwitz, Autor der zitierten Studie über die

Abb. 13. Würfelnatter am Abweis-System vor dem Wege an der Knorre, 2002. Foto: Peter Strasser. Fig. 13. Dice snake at the deflector system in front of the path at the Knorre, 2002. Photograph: Peter Strasser.

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westdeutschen Würfelnatter-Populationen, im neu gebildeten „Sächsischen Staatsministerium für Umwelt und Landwirtschaft“ des wiedergegründeten Freistaates Sachsen eingestellt wurde. 1997 wurde dann ein „Erprobungs- und Entwicklungsvorhaben zur Entwicklung und Vernetzung von bundesweit bedrohten Reptilien an Bundeswasserstrassen am Beispiel der Würfelnatter an den Flüssen Mosel, Lahn und Elbe“ in Zusammenarbeit zwischen dem Bundesamt für Naturschutz mit den entsprechenden Fachministerien der Bundesländer Rheinland-Pfalz und Sachsen ins Leben gerufen. In diesem Zusammenhang brachte Gruschwitz, der damals auch für den Fachbereich Feldherpetologie und Naturschutz im Vorstand der DGHT (Deutsche Gesellschaft für Herpetologie und Terrarienkunde) zuständig war, ein Wiederansiedlungsprojekt auf der Basis der bereits genannten Erörterungen zur Realisierung. Gruschwitz vollzog zusammen mit Sigrid Lenz und anderen Mitarbeitern aus den westdeutschen Projekten über die Würfelnatter,die Planung und Durchführung dieses Wiederansiedlungs–Projektes, allerdings unter Ausschluss ortsansässiger sächsischer Feldherpetologen, die sich teilweise in der DGHT, aber auch in „neuen“, ehemals westdeutschen Naturschutz-Organisationen wie NABU (Naturschutzbund Deutschland e. V.) und BUND (Bund für Umwelt und Naturschutz Deutschland e.V.) nach Auflösung der entsprechenden Organisationen der DDR, vor allem des „Kulturbundes der DDR“, neu organisiert hatten. Nach Ansicht der Autoren ist dieser Schritt bedauernswert, da dadurch einem solchen Vorhaben das lokale Wissen und die lokale Förderung und Personenunterstützung fehlt, die es nach Projektsterminierung für ein weiteres Gedeihen der Population dringend braucht. 1997 und 1998 erfolgten im Rahmen dieses Projekts, das von der RWE-Energie-AG finanziell massgeblich

Abb. 14. Würfelnatter im Brombeer-Gestrüpp an der steinbefestigten Elb-Böschung an der Knorre, 2008. Foto: Peter Strasser. Fig. 14. Dice snake in a blackberry thicket on the rock-reinforced embankment slope of the Elbe at the Knorre, 2008. Photograph: Peter Strasser.

Fritz Jürgen Obst & Peter Strasser

unterstützt wurde, unter Leitung von Gruschwitz und Lenz Voruntersuchungen zu Flora, Fauna und den Habitat-Strukturen an der Knorre bzw. dem Katzensprung bei Meißen, die erwartungsgemäss positiv ausfielen. Als praktische Massnahmen folgten vor allem am Elbufer Steinschüttungen zur Verbesserung der Uferstruktur und die Errichtung von Bruthilfen in Gestalt von Totholz-Haufen zur Eiablage-Animation. Die seit 1939/1940 bestehende Fahrstrasse und der nach 1990 neu entstandene Elbradweg, die das Uferhabitat von der Hanglage der Weinbergsterrassen trennen, wurden durch ein Abweis-System mittels Metallplanken gegen das Überklettern durch die Schlangen gesichert und damit das zukünftige Würfelnatter-Habitat auf den Elbufer-Bereich reduziert, d. h. gegenüber dem historischen Habitat de facto halbiert (Abb. 9, 10). Am 4 Juni 1999 erfolgte im Beisein des damaligen sächsischen Umweltministers, Dr. Rolf Jähnichen und von Mitarbeitern des tschechischen Umweltministeriums, geleitet von Dr. Petr Roth, die erste Freisetzung von 76 tschechischen Würfelnattern an der Knorre: 35 juvenile Nachzucht-Schlangen, Elterntiere von der Berounka (Nebenfluss der Moldau); 32 juvenile Nachzucht-Schlangen, Elterntiere von der Eger (Ohře); 9 Wildfänge adulter Schlangen, ebenfalls von der Eger (Ohře). Am 29 Mai 2000 erfolgte, ebenfalls wieder im Beisein des sächsischen Umweltministers, nunmehr des Amtsnachfolgers Steffen Flath und tschechischer Gäste, die zweite Freisetzung von tschechischen Würfelnattern an der Knorre mit 76 juvenilen Nachzucht-Schlangen von der Eger (Ohře). Damit waren innerhalb von zwei Jahren 152 Würfelnatter ins historische Habitat an der Knorre ausgesetzt worden. Diese Massnahme war hauptsächlich der Hilfsbereitschaft und dem Interesse der tschechischen Kollegen Petr Roth, Vit Zavadil, Vaclav Laňka und Roman Rožinek, neben Laňka ein erfolgreicher Züchter der tschechischen Würfelnattern, zu verdanken. Das Schicksal der freigesetzten Schlangen wurde von zwei Seiten parallel beobachtet. Lenz wurde zunächst seitens des sächsischen Staatsministeriums für Umwelt und Landwirtschaft, vertreten durch Gruschwitz, mit der Verfolgung der Entwicklung beauftragt. Andererseits hatten sich herpetologisch erfahrene Meißner und Dresdner Naturfreunde zusammengefunden, die regelmässig das Würfelnatterhabitat beobachteten. Diese Gruppe formierte sich 2003 zu einem gemeinnützigen Verein, „Freunde der Meißner Würfelnatter e.V.“ unter Vorsitz des pensionierten Meißner Kreistierarztes Klaus-Dieter Legde. Während Lenz sporadische Kontroll- und Arbeitsgänge in Meißen durchführte, konnten Vertreter der „Meißner Würfelnatter-Freunde“ eine konstante Erfolgskontrolle aufrecht erhalten. So konnten sie im Zeitraum vom 28 Juni 1999, also kurz nach der ersten Aussetzung beginnend, bis zum 15 Juni 2010 insgesamt 53 Totfunde von überfahrenen Würfelnattern bergen, eine Zahl, die wir bei der sehr kleinen Populationsgrösse als hoch erachten. Wenn man be-

rücksichtigt, dass die von den Vereinsmitgliedern geborgenen Totfunde auf Fahrstrasse und Radweg gewissermassen „in Konkurrenz“ zu den verpassten Strassenopfern stehen, die von örtlichen Aasfressern wie Kolkrabe und andere Rabenvögel, Möwen und Turmfalken, im Falle von toten Jungschlangen aber bereits von Singvögeln wie Drosselartigen vertilgt wurden, darf man mit hoher Wahrscheinlichkeit eine wesentlich höhere Zahl von Strassentoten veranschlagen. Völlig unkontrollierbar und deshalb in keine Zahlen fassbar sind hingegen die Verluste von lebenden Würfelnattern durch Prädatoren. Vereinzelt beobachtet wurden Fischreiher, die eine Schlange erbeutet hatten. Für Juvenile ebenfalls gefährlich wurden die im Habitat lebenden zahlreichen Stockenten und Möwen sowie die bereits erwähnten diversen Raben- und grösseren Singvögel. Ebenso unkontrollierbar sind die Verdriftungsverluste durch den am Habitat schnellfliessenden Elbstrom. Insbesondere habitat-erkundende Schlangen unmittelbar nach den Freisetzungen und frisch geschlüpfte Jungtiere werden mit hoher Wahrscheinlichkeit verdriftet. Während der regelmässig auftretenden „normalen“ Hochwässer ist die Verdriftung auch eingewöhnter Individuen sicherlich ein ernstzunehmender Gefährdungsfaktor für die Würfelnatter-Population. Im Abschlussbericht des Erprobungs- und Entwicklungsvorhabens schätzte Lenz et al. (2001) die Populationsgrösse auf ca. 100 Tiere (Lenz & Schmidt 2011). Diese Populationsgrösse konnten aus o. g. Gründen von den Beobachtern aus den Reihen der „Freunde der Meißner Würfelnatter e.V.“ nicht nachvollzogen werden. Zudem wurden bei der Berechnung der Populationsgrösse in Lenz et al. (2001) eine Division beim Lincoln-Index vergessen und eine (mathematisch) unerlaubte Berechnung bei der Jolly-Seber-Methode angewandt (Strasser 2003 unpubl.). Beide Schätzungen ergaben eine (zu hohe!) Populationsgrösse von etwa 100 Tieren. Die von Lenz et al. (2001) ebenfalls angewandte Schnabel-Methode und das von uns nachgerechnete Resultat für den Lincoln-Index ergaben eine „realistischere“ Populationsgrösse von ca. 50 Tieren Ende Oktober 2001. Allerdings dürfte eine Populationsschätzung nur ein Jahr nach der zweiten Aussetzung als noch wenig aufschlussreich über den Erfolg der Wiederansiedlung gelten. In der weiteren Entwicklung ereignete sich mit dem „Jahrhundert-Hochwasser“ vom August 2002 ein gravierendes Ereignis: Das gesamte, durch die Abweiser an Radweg und Strasse limitierte Würfelnatter-Habitat wurde tagelang von reichlich 2 m Wasser überflutet. Mit dem Anstieg des Elbpegels war damit das gesamte „Hinterland“ des Habitats für die Schlangen zugänglich. Beim Rückgang des Hochwassers waren die grösstenteils unbeschadet gebliebenen Metallplanken des Abweis-Systems ein Hindernis, das die Rückkehr in den zugewiesenen Habitatbereich stark behinderte (Abb. 13). Begünstigend für die erhöhte Verdriftungs-Gefahr, die infolge der schnellfliessenden gewaltigen Wassermassen ohnehin bestand, wirkten die als Hochwasser-

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Geschichte der Würfelnatter bei Meißen, Deutschland

Treibgut mitgeführten Sträucher, Bäume und Äste, die im Habitat während des Hochwassers zeitweilig festhingen und eine Schein-Zuflucht für die Schlangen bildeten, jedoch im Verlauf des Geschehens – nun eventuell mit den Schlangen – weitergetrieben wurden. Ein vergleichbares Extrem-Hochwasser war vor 2002 letztmalig 1845, also gut 150 Jahre früher, im weitgehend noch ursprünglichen Elbstrom-Verlauf zu beobachten gewesen. Gruschwitz veranlasste weitere Monitorings der Würfelnatter-Population durch Lenz (2003, unpubl. und 2005, unpubl.) ohne Beteiligung der Mitglieder des Vereins „Freunde Meißner Würfelnatter e.V.“ Die Quantität der Sichtmeldungen konnten von den vereinsinternen Beobachtern nicht bestätigt werden. Der Widerspruch zwischen diesen Ergebnissen (Lenz 2006) und den Beobachtungen des Vereins (Strasser & Obst 2006), sowie dem Ausbleiben jeglicher, mehrfach zugesicherter finanzieller Unterstützung der Vereinsaktivitäten durch das Sächsischen Staatsministerium für Umwelt und Landwirtschaft, führte zur Auflösung des Vereins bereits im Jahre 2005 (Legde 2005). Die Arbeit zur Beobachtung und Unterstützung der wiederangesiedelten Würfelnattern wurde daraufhin von den ehemaligen Vereinsmitgliedern unabhängig weitergeführt. Um für den vorliegenden Bericht aktuelle Aussagen über den Zustand der wiederangesiedelten Population treffen zu können, führten ehemalige Vereinsmitglieder der „Freunde der Meißner Würfelnatter“ unter der Leitung der Autoren vom 14 April 2008 bis zum 13 Oktober 2008 ein erneutes Monitoring durch. Insgesamt wuden 130 Kontrollgänge an 93 Beobachtungstagen durchgeführt. Alle Kontrollgänge fanden nur in Wettersituationen statt, die für die Schlangen günstig und für Sichtungen erfolgversprechend waren. Um die zu erwartende geringe Zahl von Schlangen nicht zu beunruhigen, wurde bewusst auf Fang- und Wiederfang-Methoden verzichtet und ausschliesslich nur die Sichtung als Nachweis verwendet. Es wurden 17 Sichtungen gemacht, von denen 12 mit Fotos belegt werden konnten (Abb. 14). Ausserdem konnten eine Exuvie sowie acht Totfunde geborgen werden. Die ausnahmslos strassentoten Schlangen waren drei Adulti und fünf Juvenile kurz nach ihrem Schlupf. Die vergleichende Auswertung der Lebend-Beobachtungen bzw. deren fotografischer Dokumentation ergab, dass sie wahrscheinlich auf acht Individuen basieren. Dabei konnte nur ein sicheres Männchen diagnostiziert werden, alle anderen Exemplare waren höchstwahrscheinlich Weibchen, was ein Geschlechterverhältnis von 1:7 ergab. Nur eines der beobachteten Tiere war halbwüchsig (1–2-jährig), alle anderen eindeutig Adulti. Zwar konnte erfreulicherweise auch 2008 die Reproduktion der Population nachgewiesen werden, doch wurden neben lediglich einem lebenden Schlüpfling, der auf der Strasse im Jahre 2008 gefunden und über das Abweissystem ins zugewiesene Habitat verbracht wurde, nur die o. g. fünf strassentoten Schlüpflinge geborgen. Der Fund eines 1-jährigen Tieres am 9 Juni 2010

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zeugt auch vom Reproduktionserfolg im Jahre 2009, und 1 Schlüpfling am 23 September sowie 4 Schlüpflinge am 4 und 5 Oktober zeugen von kontinuierlicher, wenn auch dürftiger Reproduktion im 2010. Ob und wie viele weitere Juvenile überlebt haben und die kleine Population verstärken, bleibt abzuwarten. Eine neue Eiablage-Hilfe, die dank der Unterstützung durch die Untere Naturschutzbehörde des Kreises Meißen im Zentrum des Habitats deponiert werden konnte, wurde von den Würfelnattern nicht genutzt. Die Funde der Juvenes erfolgten überwiegend am Ostende des Habitats, wo der Fürstengraben einmündet. Das ist zugleich ca. 250 m von der neuen Eiablage-Hilfe entfernt. Wie ist die Zukunft der Meißner WürfelnatterPopulation einzuschätzen? Betrachtet man alle Beobachtungsergebnisse, die seit 1999 gesammelt wurden, drängt sich der Eindruck auf, dass man mit dem Wiederansiedlungsprojekt völlig unbeabsichtigt jene Faktoren ermittelt hat, die 1936–38 zum Erlöschen der nativen Population geführt haben. (1) In einem kleinen Habitat mit einer kleinen Schlangen-Population ist die Auflösung des Komplexes ökologischer Faktoren, deren positives Zusammenwirken die Existenz der Tiere am Nordwest-Rand ihres Art-Areals ermöglicht, in seinen Auswirkungen äusserst kritisch. (2) Wie wir heute einschätzen, wäre nur durch die brückenartige Aufbockung der beiden habitatzerschneidenden Verkehrswege auf 700 m Länge eine Methode zu finden, die das u. E. nach unerlässliche Zusammenwirken zwischen dem in Bezug auf die Temperatur meist suboptimalen Wasserhabitat und dem durch die Steilhänge des Bocksberges respektive Knorre-Felsens und der Weinbergsterrassen des Katzensprungs natürlich begrenzten xerothermen Landhabitats gewährleistet (Abb. 10). Ob die für diese Strassenbau-Massnahme erforderlichen erheblichen Mittel beschaffbar sind, scheint uns jedoch sehr fraglich. (3) Eine Unterführung von Strasse und Radweg durch eine Anzahl von „Amphibien-Tunneln“ halten wir für keinen wirksamen Ersatz, da die kühlen, abgedunkelten Tunnel keinen Wander-Anreiz für die thermophilen Schlangen bieten, die Wärmeplätze aufsuchen wollen. (4) Die derzeitig von uns geschätzte Populationsgrösse von ein bis maximal zwei Dutzend Individuen hat aber wahrscheinlich doch die Chance einer Populationszunahme, wie erfolgreiche, aber illegale Freisetzungs-Experimente an verschiedenen Lokalitäten in der Schweiz mit ähnlich kleinen Individuen-Zahlen hoffen lassen (Bendel 1997, Mebert 1993, 1996, 2001, 2007, Lenz et al. 2008, Kwet & Mebert 2009). Anscheinend ist Natrix tessellata keine Spezies, die unter derartigen individuenarmen Ausgangs-Populationen schnell einer genetischen Limitierung erliegt. Eine genetische Verarmung konnte aber in isolierten, ausgesetzten Populationen in der Schweiz beobachtet werden (Gautschi et al. 2002), sowie morophologische Abnormitäten, die

vermutlich auf Inzucht zurückzuführen sind (Mebert 2011). Bei einer anderen Schlangenart, der Kreuzotter Vipera berus, verhalfen wissenschaftlich begleitete Aussetzungen zu einer Erholung einer isolierten Population, die unter 40 adulte Tiere gesunken war (Madsen et al. 1996, 1999, 2004) (5) Eine Aufstockung der Population durch erneute Freisetzungen weiterer Exemplare könnte natürlich ihrem baldigen Erlöschen entgegenwirken. Es ist aber anzunehmen, dass die Mehrzahl erneut freigesetzter Individuen denselben Faktoren zum Opfer fallen wird wie die grosse Anzahl ihrer Vorgänger von 1999/2000. (6) Unbeschadet der kritischen Situation, die wir hier darstellen, erscheint uns die Ausweisung des Würfelnatter-Habitats als Flächennaturdenkmal hinreichend begründet. Wir schlagen die entsprechende Unterschutzstellung vor. (7) Zusammenfassend sind wir der Meinung, dass nur die unter Punkt 2. benannte Massnahme einen dauerhaften Erfolg des Wiederansiedlungsprojektes der Würfelnatter in Meißen gewährleisten könnte. Ohne die generelle Wiederherstellung ihres ursprünglichen Gesamt-Habitats bleibt die kleine Population wahrscheinlich mehr oder weniger lange im existenziellen Grenzbereich. In dieser Situation kann sie jederzeit durch natürliche oder artifizielle Ereignisse gravierender Natur wieder zum Erlöschen gebracht werden. Danksagung Für ihre Mitarbeit am Monitoring 2008 in Meißen danken wir Frau Armgard Manitz und Herrn Klaus-Dieter Legde, beide Meißen, sowie den Herren Hans-Joachim Geissler und Sebastian Gebauer, Coswig. Für administrative Unterstützung durch Genehmigungen des Monitorings danken wir der Unteren Naturschutzbehörde des Kreises Meißen. Dieselbe Behörde unterstützte uns zudem durch dringende Pflegemassnahmen im Habitat und durch Einbringen neuer Eiablage-Hilfen, wofür wir besonders Herrn Henning Klein dankbar sind. Für Unterstützung beim Erstellen des Manuskripts und der Recherche zu historischen Hintergrundinformationen danken wir Frau Susann Rautenberg, Dresden, verbindlich. Herrn Konrad Mebert, Schweiz, gilt unser ausdrücklicher Dank für die kritische Durchsicht und zahlreichen Vorschlägen zur Verbesserung des Manuskripts. Literatur Anonymus (1892a): Die Würfelnatter (Tropidonotes tessellatus) wiederholt am Katzensprung bei Meißen gefangen. – Meißner Tageblatt Nr. 231: 5 (vom 04. Oktober 1892). Anonymus (1892b): Die Würfelnatter (Tropidonotes tessellatus) wiederholt am Katzensprung bei Meißen gefangen. – Dresdner Anzeiger Nr. 279: 4 (vom 05. Oktober 1892). Bendel, P.(1997): Zur Physiologie, Morphometrie und Populationsökologie der Würfelnatter Natrix tessellata am Alpnachersee. – Diplomarbeit, Zoologisches Museum der Univ. Zürich, Schweiz. Fickel, J. (1893): Die Literatur über die Tierwelt des Königreiches Sachsen. – Programm des Wettiner-Gymnasiums Dresden.

Gautschi, B., Widmer, A., Joshi, J. & J.C. Koella (2002): Increased frequency of scale anomalies and loss of genetic variation in serially bottlenecked populations of the dice snake, Natrix tessellata. – Conservation Genetics 3: 235–245 Geisenheyner, L. (1898): Zum Kapitel „Hausratte und Würfelnatter“. – Zool. Garten 39: 1-4. Gruschwitz, M. (1978): Untersuchungen zu Vorkommen und Lebensweise der Würfelnatter (Natrix t. tessellata) im Bereich der Flüsse Mosel und Lahn (Rheinland-Pfalz). – Salamandra 14(2): 80–89. Klausnitzer, B. (1982): Insekten, Mollusken. – In: Zühlke, D. (Hrsg.): Elbtal und Elbhügelland bei Meißen. – Werte unserer Heimat, Bd. 32, Berlin. Klengel, A. (1919): Die Würfelnatter am Katzensprung. – In: Die Meißner Heimat. – Monatsbeilage zur Tageszeitung „Meißner Neueste Nachrichten“. Klengel, A. (1932): Meißner Heimat, Coswig: 36 und 92–94. Kwet, A. & K. Mebert (2009): Die Würfelnatter (Natrix tessellata): Das Reptil des Jahres 2009. – Reptilia 80: 40–50. Laňka, V. (1978): Variabilität und Biologie der Würfelnatter (Natrix tessellata). – Acta Univ. Carol. Biol. Praha 1975–76: 167–207. Legde, K.-D. (2005): Protokoll der Mitgliederversammlung (Jahreshauptversammlung) des Fördervereins „Freunde der Meißner Würfelnatter e.V.“ vom 2. März 2005. – unveröff. vereinsinterne Schrift. Ledge, K.-D. & P. Strasser (2003): Gründung, Zielstellung und Aktivitäten des Fördervereins „Freunde der Meißner Würfelnatter e.V.“ – Elaphe, Rheinbach 11(4): 50–53. Lenz, S., Herzberg, A. & A. Schmidt (2001): Abschlussbericht zum Erprobungs- und Entwicklungsvorhaben: Entwicklung und Vernetzung von Lebensräumen sowie Populationen bundesweit bedrohter Reptilien am Beispiel der Würfelnatter (Natrix tessellata) an den Flüssen Mosel, Lahn und Elbe, unveröffentl. Projektbericht, DGHT, Rheinbach. Lenz, S. (2003): Untersuchungen der Bestandssituation der Würfelnatter (Natrix tessellata) an der Elbe bei Meißen – unveröffentl. Untersuchungsbericht im Auftrag des Staatl. Umweltfachamtes Radebeul. Lenz, S. (2005): Bestandsuntersuchung der wiederangesiedelten, reproduzierenden Population der Würfelnatter zur Bewertung der Populationsentwicklung und der aktuellen Bestandssituation an der Elbe bei Meißen. – unveröffentl. Untersuchungsbericht im Auftrag des Regierungspräsidiums Dresden. Lenz, S. (2006): Zur aktuellen Situation der Würfelnatter an der Elbe. – Elaphe, Rheinbach 14(1): 12–14. Lenz, S. & A. Schmidt (2011): Ergebnisse eines deutschweiten Projektes zur Förderung der Würfelnatter-Populationen und ihrer Lebensräume. – Mertensiella 18: xxx–yyy. Lenz, S., Mebert, K. & J. Hill (2008): Die Würfelnatter: Reptil des Jahres 2009. – In: Die Würfelnatter, Reptil des Jahres, Aktionsbroschüre. – DGHT, Rheinbach, Deutschland. Madsen, T., Shine, R., Olsson, M. & H. Wittzell (1999): Restoration of an inbred adder population. – Nature 402: 34–35. Madsen, T., Stille, B. & R. Shine (1996): Inbreeding depression in an isolated population of adders (Vipera berus). – Biological Conservation 75: 113–118. Madsen, T., Ujvari, B. & M. Olsson (2004): Novel genes continue to enhance population growth in adders (Vipera berus). – Biological Conservation 120: 145–147. Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti) 1768 in der Schweiz und im südlichen Alpenraum. – Diplomarbeit, Zoologisches Museum der Univ. Zürich, Schweiz.

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Mebert, K. (1996): Comparaison morphologique entre des populations introduites et indigènes de Natrix tessellata de l’Arc Alpin. − Bull. Soc. Herp. Fr. 80: 15–25. Mebert, K. (2001): Die Würfelnatterpopulation am Lopper. – In: NAGON (Ed.): Amphibien und Reptilien in Unterwalden. – NAGON, Grafenort, Schweiz 2: 158–163. Mebert, K. (2007): Die Würfelnatter am Brienzersee. – In: Jahrbuch 2007, Uferschutzverband Thuner- und Brienzersee – UTB Selbstverlag, Thun, Schweiz: 169–180. Mebert, K (2011): Introduced and Indigenous Populations of the Dice Snake (Natrix tessellata) in the Central Alps – Microgeographic Variation and Effect of Inbreeding. – Mertensiella 18: 71–79. Mertens, R. (1947): Die Lurche und Kriechtiere des RheinMain-Gebietes. – Senckenberg-Buch 16, Frankfurt/M. Mlynarski, M. (1961a): Serpents pliocènes et pleistocènes de la Pologne avec la revue critique des Colubridés fossiles. – Folia Quarternaria, Krakow 4: 1–45. Mlynarski, M. (1961b): Faune quarterneire de serpents (Colubridae) de Giebultów pres Cracovie, Pologne. – Folia Quarternaria, Krakow 6: 1–9. Obst, F.J. (1976): Die Würfelnatter bei Meißen – ein erloschenes Vorkommen (Reptilia, Ophidia, Colubridae). – Zool. Abh. Mus. Tierk. Dresden 34(4): 47–55. Obst, F.J. (1989): „Die Würfelnatter bei Meißen – ein erloschenes Vorkommen“ – nur ein bedauerlicher Fakt oder eine Herausforderung? – Feldherpetol., Erfurt: 16–22.

Pietzsch, E. (1969): Angeln, Beobachten, Auswerten. – Deutscher Angelsport 21(7): 150, 155. Prokoph, U. (2003): Feldherpetologische Beobachtungen am Rande der Flutkatastrophe an der Elbe bei Meißen im August 2002. – Die Eidechse, Rheinbach 14(2): 61–63. Strasser, P. (2003): Über einige Aspekte der Wiederansiedlung der Würfelnatter (Natrix tessellata) an der Elbe bei Meißen 1999 bis 2003. – Verein „Freunde der Meißner Würfelnatter“ e. V., – unveröffentl. vereinsinterner Bericht. Strasser, P. & F.J. Obst (2006): Zur aktuellen Situation der Würfelnatter an der Elbe – Anmerkungen zum Bericht durch Mitglieder des ehemaligen Vereins „Freunde der Meißner Würfelnatter e.V.“. – Elaphe, Rheinbach 14(2): 13–15. Strasser, P. (2009): Die Würfelnatter – Reptil des Jahres 2009. – Mitteilungen für sächsische Feldherpetologen und Ichthyofaunisten, NABU, Landesverband Sachsen e.V., Leipzig: 7–9. Zimmermann, R. (1910): Über das Vorkommen der Würfelnatter im Königreich Sachsen. – Wochenschr. f. Aquar.- u. Terrar. kunde, Beilage Lacerta 7: 8. Zimmermann, R. (1922): Ein Beitrag zur Lurch- und Kriechtierfauna des ehemaligen Königreichs Sachsen. – Arch. f. Naturgesch. Berlin 88: 245-267. Wikipedia (2010): Atlantikum. – Available at: http://de.wikipedia. org/w/index.php?oldid=71584232

Autoren Fritz Jürgen Obst, Dr. Rudolf-Friedrichs-Str. 27, 01445 Radebeul, Deutschland; Peter Strasser, Niederfährer Str. 55, 01662 Meißen, Deutschland.

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MERTENSIELLA 18

71-79

20 September 2011

ISBN 978-3-9812565-4-3

Introduced and Indigenous Populations of the Dice Snake (Natrix tessellata) in the Central Alps – Microgeographic Variation and Effect of Inbreeding Konrad Mebert Abstract Scale characteristics and body proportions of dice snakes (Natrix tessellata) in the central Alps were compared with life samples among three populations introduced into Swiss lakes north of the Alps (lakes Alpnach, Brienz, and Geneva) and two indigenous populations from southern Switzerland and northern Italy (lakes Lugano and Garda). Additional preserved specimens from the Maggia Valley, southern Switzerland), were subsequently included in a reanalysis to directly compare morphological characteristics of introduced populations with their parental populations. Indeed, introduced dice snakes from the lakes Alpnach and Brienz are phenetically closest to the population from the Maggia Valley. Dice snakes from the introduced population of Lake Geneva show intermediate characters expression between specimens from the Maggia Valley and the Lakes of Lugano and Garda, confirming their putative mixed origin. An increased degree of abnormal morphological traits in the introduced populations suggests an inbreeding effect. Key words: Natrix tessellata, microgeographic variation, allochthonous, autochthnous, inbreeding

Introduction The dice snake (Natrix tessellata) is not a “typical” element of the alpine fauna in Switzerland, but it occupies rivers and lakes up to an altitude of approximately 800 m a.s.l. along the southern versant of the Alps (Kramer & Stemmler 1992). Its natural distribution in Switzerland mainly is restricted to the water courses in Canton Ticino (= Italian Switzerland), that drain into Italy’s Po River system (Hofer et al. 2001). However, there are four populations in Switzerland north of Alps that derive from dice snakes that were introduced approximately 15 (the latest) to 85 (the oldest) years ago (Mebert 1993, 2001, 2007, Gruschwitz et al. 1999, Meyer et al. 2009). The dice snakes at the introduced (allochthonous) sites have developed into relatively large populations and persist along some shore sections of the lakes Alpnach, Brienz, Geneva, and Zurich (Fig. 1). However, this morphological analysis concerns only the first three introduced sites (besides the indigenous ones), since the population at a site in Lake Zurich was established years after the completion of this study. The information regarding the origin of the introduced animals at lakes Alpnach, Brienz, and Geneva, was very vague and inconclusive throughout this study in the early 1990s (Mebert 1993). Yet, persistent oral reports indicated that the respective dice snakes were sampled by different people or groups of people from within the Canton Ticino, southern Switzerland. One aspect of this study was to investigate the microgeograhpic variation to find a phenetic correlation, and thus an indication of potential relateness, among introduced populations on one hand, and with parental dice

snakes from their putative region of origin (Canton Ticino) on the other hand. Dice snakes from Lake Lugano (= Lake Ceresio) were selected to represent Canton Ticino, as that lake-population was relatively easy to access, in the past as today (Mebert et al. 2011). It was expected that if microgeographic variation is substantial within Natrix tessellata, phenetic similarity would indicate a pattern of decent, i.e. morphological resemblance between two populations indicates a true relationship. However, there is a risk that morphological adaptations would produce similar phenotypes among also non-related populations that experience similar environmental conditions, such as parallel evolution. But this was less expected, because the time span since the introduction up to the sampling in the early 1990s was relatively short (30–65 years) for such morphological convergence to take place. To put morphological variations among introduced and potential source populations into perspective with a non-related, yet natural population, dice snakes from Lake Garda in Italy were included in the analysis. Hence, dice snakes from Lake Garda served not only as a mean to elucidate some microgeographic variation between natural populations of “Central Alp dice snakes”, but also as a reference population to the potential morphological differences between indigenous (from Ticino) and introduced dice snakes. Lake Garda is within the same climatic region as Lake Lugano, but is located 130 km southeast from it (Fig. 1). It would require > 360 km travel distance along water courses to connect the two lakes. All five lake-populations from within the Central Alps were studied with an extensive set of morphological characteres, including body proportions and pho-

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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lidotic characters. Subsequent to the completion of the principal study, persons responsible for some introductions could be interviewed, which helped to track in more detail the history of introductions. They confirmed that the general region of origin for the introduced populations was the Canton Ticino (Mebert 1993). For example in the case of Lake Alpnach, the origin of the parental populations of dice snakes was more precisely allocated to the Maggia Valley, Canton Ticino. Between 15–25 dice snakes were translocated and introduced into Lake Alpnach. Maggia Valley is 30 km airdistance from Lake Lugano and even 45 km along water courses, which would be the more likely route for any potential gene flow due to the semiaquatic nature of this species. But both distances are too far to account for a direct relationship between the dice snakes from Maggia Valley and Lake Lugano. Consequently, an additional sample of preserved dice snakes from the Maggia Valley was measured (Mebert 1996). An extraordinary note: The capture and release of animals into a new site is illegal and may cause a severe damage to the local indigenous fauna. Such issues are currently investigated with the dice snakes at Lake Geneva (e.g. Lenz et al. 2008, Metzger et al. 2009, 2011, Mazza et al. 2011).

Materials and Methods At least 40 adult dice snakes (total length > 40 cm, ≈ SVL of 31–33 cm) of each sex (total n = 433) were sampled at each of three introduced population north of the Swiss Alps, the lakes Alpnach, Brienz, and Geneva, and at two lakes with indigenous populations south of the Alps, the lakes Lugano (Canton Ticino, southern Switzerland) and Garda (Italy) (Fig. 1). The snakes were transported to the laboratory for measurements and subsequently returned and released at their site of capture. More than 50 morphological characters were recorded, including pholidotic characters (arrangement, abnormality, and numbers of scales), color pattern, and body proportions, such as several lengths at the head, as well as trunk and tail proportions. The definitions of characters and methods of measuring are explained in Mebert (1993), but are briefly indicated in the text, where it was deemd helpful to prevent misunderstanding. An additional 26 preserved specimens (Muséum d’Histoire Naturelle de Genève) from the Maggia Valley (Mebert 1993) were included in a subsequent analyis. The normal distribution of the characters was tested according Shapiro-Wilk with the UNIVARIATE procedure (SAS® Procedure Guide, 1990). An ANOVA was processed with SAS to reveal characters exhibiting sig-

Fig. 1. Location of introduced and indigenous populations of Natrix tessellata in this study. Introduced populations are LaAl (Lake Alpnach), LaBr (Lake Brienz), LaGe (Lake Geneva), and LaZu (Lake Zurich, not studied); indigenous populations are LaLu (Lake Lugano), LaGa (Lake Garda), and MaVa (Maggia Valley).

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Variation and Inbreeding in N. tessellata from the Central Alps

nificant differences among populations. Characters with a normal distribution were tested with GLM, and nonnormal characters like the non-parametric cephalic scale characters with the procedure NPAR1WAY, applying a 2-sample Wilcoxon test (SAS/STAT®User’s Guide vol. 2, 1989). To investigate the significance levels for differences among the populations, normally distributed characters were analyzed as ratios (e.g. head width/ head length, tail length/SVL) to reduce the confounding influence of animals from different size classes. In addtion, these transformed characters were processed by a WPGMA (Weighted Average Linkage) method within the software ‘Ntwahl’ by G. Bächli (Zoological Museum of the University of Zurich, Switzerland) for a cluster analysis to investigate the phenetic relationship among populations.

Tab. 1. Frequency of abnormal ventral and subcaudal scales in Natrix tessellata from introduced and indigenous populations of the Central Alps: (A) semi-ventrals, (B) split ventrals, (C) fused subcaudals; LaAl (Lake Alpnach), LaBr (Lake Brienz), LaGe (Lake Geneva), LaLu (Lake Lugano), and LaGa (Lake Garda) A LaAl Females 37% Males 52%

LaBr 54% 45%

LaGe 14% 25%

LaLu 16% 14%

LaGa 10% 22%

Results Microgeographic Variation Only the statistically most significant or striking differences among the three introduced (Alpnach, Brienz, Geneva) and the two indigenous (Lugano, Garda) populations are shown here. Additional results and elaboration can be found in Mebert (1993, 1996), and in two additional reports relating to global variation and sexual dimorphism in Mebert (2011a, b). The relevant morphological distinctions among the populations are: (1) the number of abnormal ventral and subcaudal scales; (2) the position of the scale row reduction on the tail; (3) the number of labial scales; (4) the number of ocular scales; (5) the contact of the supralabial scales with the eye; (6) the posterior head length, i.e. the distance between the posterior end of the eye and the posterior end of the supralabials; (7) the width of the frontal shield; (8) total length. The mean and range of the number of ventral and subcaudal scales are similar among the five populations. But the dice snakes from the lakes Alpnach and Brienz show a high incidence of abnormalities, including many specimens with semi-ventrals (= only half-sided developed ventral scales, Tab. 1A) and split ventrals (= divided ventral scales, showing a suture in the middle, Tab. 1B, also Velenský et al. 2011). A single individual could exhibit up to 18 abnormal ventral scales. In total, 37% of the males from Lake Alpnach and 54% of the males from Lake Brienz, as well as 52% of the females of Lake Alpnach and 45% of the females of Lake Brienz exhibit semi-ventrals (Tab. 1A). In comparison, the frequency of abnormal pholidosis in dice snakes from Lake Geneva is reduced and approaches values found in the natural populations south of the Alps. The situation concerning the split ventrals is similar (Tab. 1B): the dice snakes from the lakes Alpnach and Brienz exhibit a higher frequency of abnormal expression (29–45%) than snakes from natural populations with the exception of the males from Lake Lugano, which show a similar frequency of split ventrals (32%).

B Females Males

LaAl 37% 45%

LaBr 29% 29%

LaGe 11% 17%

LaLu 14% 32%

LaGa 2% 10%

C Females Males

LaAl 39% 36%

LaBr 17% 35%

LaGe 32% 40%

LaLu 11% 30%

LaGa 12% 7%

Dice snakes from the three introduced populations generally show a high frequency of laterally fused subcaudals (17–40%, Tab. 1C). However, this frequency is comparable to the fused subcaudals found in 30% of

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autochtonous males from Lake Lugano. Usually, dice snakes from natural populations show a decreased frequency of fused subcaudal scales (2–12%). The tendency of developing a higher degree of abnormalities in the introduced populations of the lakes Alpnach and Brienz is reinforced by the discovery of five males that exhibit an unusually large reduction of the number of ventral scales from 15% to 20% (Fig. 2). Males from the central Alpine region (n > 200) have on average 170 ventral scales (with the minimum found at 161, Mebert 1993). But the five dwarf males exhibit ventral scales counts from 130 to 140. X-rays not only confirm that the vertebrae are equally reduced, but that the positions of semi-ventrals correlate with fused vertebrae (Fig. 3). Fig. 4. Pattern of dorsal scale row reduction. The reduction occurs bilaterally, whereby two longitudinal scale rows (light red) are reduced to one row (dark red). The position of the reduction is related to the ith number of ventral scale. In this example, begin with the first scale of the reduced row (dark red), count in a zig-zag way to the venter by following the yellow scales up to the ventral scale Nr. 104, which represents the ith number of ventral scale for this reduction.

Fig. 2. Effect of inbreeding? A dwarf male Natrix tessellata from the introduced population of Lake Brienz with only 139 ventrals and many abnormal scales (white lines).

Fig. 3. X-ray of the same specimen as in Fig. 2. The white lines point to fused vertebrae, corresponding with abnormal ventral scales.

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In most mid-sized snakes, the number of longitudinal dorsal scale rows is being reduced bilaterally towards the vent and tail (Fig. 4). In dice snakes, such scale row reductions occur near the mid-body and again near the vent (cloaca). Multiple reductions of scale rows over even shorter body segments occur on the tail, enabling its drastic tapering. The average ventral positions of such “bilateral scale row reductions” are valuable meristic characters and quantitative traits. On the tails of dice snakes, well identifiable reductions occur from 8 scale rows down to 6 and again down to 4 scale rows. These reductions occur in introduced snakes significantly closer to the vent than in indigenous dice snakes (Fig. 5). Another significant difference relates to head proportions. The posterior head length of dice snakes from the lakes Alpnach and Brienz, and to a lesser degree those from Lake Geneva, are larger than in snakes from the natural populations of the lakes Lugano and Garda (Fig. 6). Despite these differences between introduced and natural populations, a cluster analysis based on 27 normally distributed characters (body proportions, positions of scale row reductions, and numbers of ventral/ subcaudal scales) show that the dice snakes from the introduced populations phenetically resemble more their geographically nearest dice snakes from the lakes Lugano and Garda, than the individuals from the Balkan or those as far as the Near East (for females see Fig. 7). A similar phenetic diagram for males is displayed in Mebert (2011a). The analysis shows also that female dice snakes from all three introduced populations are phenetically closest to eachother, which also applies to the introduced males of the lakes Alpnach and Brienz,

Variation and Inbreeding in N. tessellata from the Central Alps

Fig. 5. Relative positions (% of subcaudal scales beginning at vent) of scale row reductions on the tail in Natrix tessellata from the Central Alps. The lower, middle and upper horizontal borders of a box represent the quartiles of 25%, 50%, and 75% of the data (medians), respectively. Displayed are the average reduction positions from 6 down to 4 scale rows in males (left), and from 8 down to 6 rows in females (right). Blue shows the three populations from the same genetic stock, the Maggia Valley, whereas reddish represents other populations with different origins (see text): introduced populations LaAl (Lake Alpnach), LaBr (Lake Brienz), and LaGe (Lake Geneva); indigenous poplations LaLu (Lake Lugano), LaGa (Lake Garda), and MaVa (Maggia Valley).

whereas the males from Lake Geneva group closer with males from the lakes Lugano and Garda (Mebert 2011a). Origin of Introduced Snakes and Reanalysis Subsequent interviews with responsible persons have revealed that the population at Lake Alpnach originates from 15–25 dice snakes sampled in the Maggia Valley in 1944 and 1945. The snakes were then transported over the Gotthard Pass (> 2000 m a.s.l.), which is the direct route and pass leading northward through the adjacent alpine ridges, thus posing the natural barrier for any current northward expansion of this species. The dice snakes were subsequently released at the shore of Lake Alpnach, near Stansstad. These Maggia-individuals constitute the initial stock of an increasing population at that lake, which provides suitable conditions along its southerly exposed rocky shores (Fig. 8). Around 1960, approximately 60 specimens were removed from this growing population and introduced at Lake Brienz in another alpine valley (Fig. 1). To adequately incorporate the new information, 26 preserved dice snakes from the parental population of the Maggia Valley were morphologically investigated. The results showed indeed the close phenetic affinity between the dice snakes from the lakes Alpnach and Brienz with those from Maggia Valley, in particular the larger posterior head length (Fig. 6) and the positions of scale row reductions on the tail (Fig. 5). The similar and extraordinary variation of these characters not only

Fig. 6. Posterior head length (relative) of Natrix tessellata from introduced and indigenous populations in the Central Alps (see text for definition of posterior head length): labels and colors as in Figure 5m; (a) M = males, (b) F = females.

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Fig. 7. Phenetic relationships in Natrix tessellata among different regions of Europe to the Near East (eastern Mediterranean). The analysis was processed with relative values of body proportions, positions of scale row reductions, and numbers of ventral/ subcaudal/cephalic scales (Mebert 1993). The regions are in alphabetical order: CeIt (central Italiy), CeTu (central Turkey), Gree (Greek mainland, without specimens from Lake Iliki), LaAl (Lake Alpnach), LaBr (Lake Brienz), LaGa (Lake Garda), LaGe (Lake Geneva), LaIl (Lake Iliki, Greece), LaLu (Lake Lugano), MaVa (Maggia Valley), NeEa (Near East), NeTu (Northeastern Turkey), Turi (Turin, northwest Italy), VeVa (Verzasca Valley, Ticino, southern Switzerland), WeBa (Western Balkan, especially Dalmatian coastal region).

support the verbal report about the origin of the dice snakes from the lakes Alpnach and Brienz, but their distinct expression demonstrates also the impressive degree of microgeographic variation over a short distance, namely those between dice snakes from Maggia Valley and those from Lake Lugano, approximately 40 km farther south (see Mebert 1993 for more examples). A first report of a dice snake at Lake Geneva dates back to 1925 (Morton 1926), who found a specimen at St. Saphorin, the core of its actual range along this

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lake today. First verbal accounts indicated that the dice snakes at this locality also originate from the Maggia Valley. But, dice snakes from Lake Geneva often show a character expression intermediate between individuals from Maggia Valley (and its sister population at the lakes Alpnach and Brienz) and those from Lake Lugano, in particular the number of abnormal scales (Tab. 1), the position of scale row reductions on the tail (Fig. 5), and the posterior head length (Fig. 6). But subsequent investigations revealed, that several introductions followed

Variation and Inbreeding in N. tessellata from the Central Alps

Fig. 8. The rocky shore of Lake Alpnach, site of the second oldest introduction of N. tessellata.

into the Lake Geneva between the 1950s and 1960s with dice snakes not only from Maggia Valley, but also from the area around Lake Lugano (see Mebert 1996, Metzger 2011) Discussion The phenetic similarity among some populations corroborate the verbal accounts that the origin of the introduced dice snakes predominantly lies in the Maggia Valley, but other sites in Ticino are involved for the population at Lake Geneva. This strongly suggests that the larger posterior head length and the “closer-to-vent dorsal scale row reductions on the tail” found in dice snakes from the introduced populations have a genetic basis, since these characters are similarly expressed in their parental population from the Maggia Valley and discriminate against other natural populations in Ticino and Italy. Other characters that significantly distinguish the introduced populations from the indigenous ones likely have been evolved after the introduction event. Among these characters are the higher frequency of ventral

and subcaudal scale abnormalities in introduced populations, but also the lower number of labial scales, the higher number of ocular scales, a higher frequency of a contact of the eye with only the fourth supralabial scale, a narrower frontal scale, and a larger total length (see Mebert 1993). The modifications of these caracters might be the consequence of random changes in allele frequencies, resulting from the fact that the founder population was very small. Or they may be the result of environmental factors, such as a lower temperature during embryonic development at the release site compared to the site of the parental population south of the Alps. A character change due to contamination of the lakes Alpnach and Brienz is unlikely, as they are considered as relatively clean. But the climate at these lakes are generally cooler than at sites south of the Alps. The influence of cool temperatures during embryonic development has been demonstrated by the works of Fox et al. (1961) and Osgood (1978), and more recently by Löwenborg et al. (2010). They showed that the temperature in related natricines influences the frequency of scale abnormalities and the number of ventral scales developed. Fox et al. (1961) found up to five ventral less (3% in average) in progeny of Thamnophis elegans terrestris

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maintained at 18 to 30 °C during gestation. But even though the climate is cooler in the introduced populations north of the Alps, the lakes of Brienz and Alpnach experience still a comparativley similar climate as other “normal” dice snake populations in the Czech Republic (e.g. Laňka 1978, Velenský et al. 2011), which have not developed such a frequency of abnormal scales. Moreover, in view of the limited distribution of the Alpnach and Brienz populations, each covering about 2 to 3 km lakeshore, and the high density of snakes (Bendel 1997, Borgula 2001), one would expect a much higher incidence of such abnormalities if they were the consequence of climate or pollution, because such factors would affect all individuals at this small site. The increase in the number of abnormal scales seems more likely due to inbreeding, arising from the limited number of snakes originally introduced. Moreover, the unusual reduction of 15% to 20% of ventral scales and associated vertebrae, concerning 5 of 80 males from the lakes Alpnach and Brienz, is not known from any other population. This reduction is also much larger than the 3% found by Fox et al. (1961). Another parallel may be drawn to neighboring Germany, where the isolation of their population was viewed as a potential cause for the high rate of abnormal scales, in particular of cephalic scales (Lenz & Gruschwitz 1993). A total of 82.6% of indivdiuals exhibit at least one “abnormal” scale. However, their definition of abnormal phenotypic expression is much broader than in the current study, thus, increasing the number of “abnormal” individuals. For example, the frequency of split ventral scales in the isolated populations at the river Lahn in Germany (< 10% of individuals affected) is less than in the dice snakes from Lake Lugano (14%–32%). But the frequency of abnormally developed cephalic scales in German dice snakes from the Lahn River is striking (Lenz & Gruschwitz 1993). The related effect of inbreeding on scale expression in snakes was also shown by Schwaner (1990). He showed that in the Australian elapid of the Notechis scutatus-ater complex, populations from small islands had a higher frequency of abnormalities paired with a higher rate of homozygosities, thus indicating inbreeding, than populations from the larger islands. The potential for a correlation between inbreeding and increased abnormal scale expression is also real for the introduced dice snake populations. In a follow up work to this study, Gautschi et al. (2002) investigated the genetic diversity in dice snakes from the lakes Alpnach and Brienz with that of indigenous individuals from the lakes Lugano and Garda. They found a severe reduction in the allelic diversity of microsatellites and a loss of observed heterozygosity in the introduced populations. The reduction of genetic diversity was stronger in the serially bottlenecked population of Lake Brienz than in the population that was bottlenecked only once (Lake Alpnach). They also found a significant relationship between the occurrence of scale abnormalities and individual heterozygosity. Even though the range

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of variation of morphological characters is similar between introduced and indigenous populations of the lakes Lugano and Garda, as well as the parental population (Maggia Valley), the introductions had an obvious effect on the genetic diversity and the frequency of abnormal scale. It is not certain, what these morphological and genetic deviations will mean for the future of the introduced populations of dice snakes. But the current situation may provide valuable information for future conservation strategies that target the relocation of individuals to generate new populations. Acknowledgements I would like to thank Vinzenz Ziswiler and Goran Dušej, both formerly from the Zoological Museum of the University of Zurich, Switzerland, for their personal investment into this study. Maya Henggeler was tremendously helpful in generating the graphs. References Bendel, P. (1997): Zur Physiologie, Morphometrie und Populationsökologie der Würfelnatter Natrix tessellata am Alpnachersee. – M.S. thesis, Zoological Museum, University of Zurich, Switzerland. Borgula, A. (2001): Die Würfelnatter während und nach dem Bau des Seeuferwegs am Lopper. – Naturforschende Gesellschaft Ob- und Nidwalden (NAGON), Grafenort, Switzerland: 186–193. Fox, W., Gordon, D. & M.H. Fox (1961): Morphological effects of low temperatures during the embryonic development of the garter snake, Thamnophis elegans. – Zoologica 42(5): 57–71. Gautschi, B., Widmer, A., Joshi, J. & J.-C. Koella (2002): Increased frequency of scale anomalies and loss of genetic variation in serially bottlenecked populations of the dice snake, Natrix tessellata. – Conservation Genetics 3: 235–245. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA Verlag, Wiesbaden, Germany: 581– 644. Kramer, E. & O. Stemmler (1992): Nos Reptiles. – Publication du Musée d’Histoire Naturelle, Bâle. 21. Laňka, V. (1978): Variabilität und Biologie der Würfelnatter (Natrix tessellata). – Acta Universitatis Carolinae, Biologica 1975– 76: 167–207 Lenz, S. & M. Gruschwitz (1993): Zur Merkmalsdifferenzierung und -variation der Würfelnatter, Natrix tessellata (Laurenti 1768) in Deutschland. – Mertensiella 3: 269–300. Lenz, S., Mebert, K. & J. Hill (2008): Die Würfelnatter: Reptil des Jahres 2009. – In: Die Würfelnatter, Reptil des Jahres, Aktionsbroschüre. – DGHT, Rheinbach, Deutschland. Löwenborg, K., Shine, R. & M. Hagman (2010): Fitness disadvantages to disrupted embryogenesis impose selection against suboptimal nest-site choice by female grass snakes, Natrix natrix (Colubridae). – Journal of Evolutionary Biology: 177–183. Mazza, G., Monney, J.-C. & S. Ursenbacher (2011): Structural habitat partitioning of Natrix tessellata and Natrix maura at Lake Geneva, Switzerland. – Mertensiella 18: 80–85.

Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zurich, Switzerland. Mebert, K. (1996): Comparaison morphologique entre des populations introduites et indigènes de Natrix tessellata de l’Arc Alpin. – Bull. Soc. Herp. Fr. 80: 15–25 Mebert, K. (2001): Die Würfelnatterpopulation am Alpnachersee – In: Nagon (Ed.): Amphibien und Reptilien in Unterwalden. – Nagon, Grafenort, Switzerland 2: 158–163. Mebert, K. (2007). The dice snake at Lake Brienz. – In: Annual Volume 2007, Shore-Conservation of the lakes Brienz and Thun. – UTB Publishing, Thun: 169–180 (in German). Mebert, K. (2011a): Geographic variation of morphological characters in the dice snake Natrix tessellata (Laurenti 1768). – Mertensiella 18: 11–19. Mebert, K. (2011b): Sexual dimorphism in the dice snake (Natrix tessellata) from the Central Alps. – Mertensiella 18: 94–99. Mebert, K., Conelli, A.E., Nembrini, M. & B.R. Schmidt (2011): Monitoring and assessment of the distribution of the dice snake in Ticino, southern Switzerland. – Mertensiella 18: 117–130. Metzger, C., Christe, P. & S. Ursenbacher (2011): Diet variability of two convergent natricine colubrids in an invasivenative interaction. – Mertensiella 18: 86–93.

Metzger, C., Ursenbacher, S. & P. Christe (2009): Testing the competitive exclusion principle using various niche parameters in a native (Natrix maura) and an introduced (N. tessellata) colubrid. – Amphibia-Reptilia 30: 523–531. Meyer, A., Zumbach, S., Schmidt. B. & J.-C. Monney (2009): Auf Schlangenspuren und Krötenpfaden – Amphibien und Reptilien der Schweiz. – Haupt Verlag, Bern, Switzerland. Morton, W. (1926): Une nouvelle couleuvre pour la faune vaudoise. – Bulletin de la Société Vaudoise des Sciences Naturelles 56: 181–183. Osgood, D.W. (1978): Effects of temperature on the development of meristic characters in Natrix fasciata. – Copeia 1978(1): 33– 47. ® SAS Institute Inc., SAS/STAT User’s Guide, Version 6, Fourth Edition, Volume 2, Cary, NC: SAS Institute Inc., 1989. ® SAS Institute Inc., SAS Procedures Guide, Version 6, Third Edition, Volume 2, Cary, NC: SAS Institute Inc., 1989. Schwaner, T.D. (1990): Geographic variation in scale and skeletal anomalies of tiger snakes (Elapidae: Notechis scutatus-ater complex) in southern Australia. – Copeia 1990(4): 1168–1173. Velenský, M., Velenský, P. & K. Mebert (2011): Ecology and ethology of dice snakes, Natrix tessellata, in the city district Troja, Prague. – Mertensiella 18: 157–176.

Author Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland, e-mail: [email protected].

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Structural Habitat Partitioning of Natrix tessellata and Natrix maura at Lake Geneva, Switzerland Gaëtan Mazza, Jean-Claude Monney & Sylvain Ursenbacher Abstract. In Switzerland all eight snake species are threatened and have been added to the Swiss Red List with different levels of concern. The most threatened is the viperine snake, Natrix maura, a semi-aquatic snake, which is considered as “Critically Endangered” (CR) in Switzerland. Only one population is presently living on the shores of Lake Geneva, mainly located between St-Saphorin and Treytorrens (Canton Vaud). But the population size estimation trends show a drastic reduction of this species. Alteration of the lake shore structure and the introduction of the ecologically very similar dice snake, Natrix tessellata, since the 1920s could be the causes of the observed decline of the viperine snake in the last 15 years. A higher fecundity and a larger body size render the alien species probably more competitive and possibly have a key role on the population decrease of the native species. In order to test the hypothesis of competition between both species, their habitats between St-Saphorin and Treytorrens were described in detail in order to detect differential interspecific use. In total 23 environmental variables were measured at the study area and data were subsequently analysed using tests of proportion. Results indicate that the dice snake prefers slopes with limited vegetation height (0.5–1 m), but inhabits also slopes with light vegetation cover and relatively narrow littoral zones. In contrast, the habitat use of the viperine snake relates to littoral zones with less steep slopes, but abundant vegetation. In addition, wide littoral zones seem to be preferred by the native species, such as the region near Treytorrens where the viperine snake was observed to be most numerous. Results obtained in this study were used to suggest particular shore management action, in particular to promote the native species. Key words. Habitat partitioning, introduction, interspecific competition, Natrix tessellata, Natrix maura, Lake Geneva

Introduction All snake species in Switzerland are present on the Swiss Red List for threatened species and the threat for most species is increasing (Monney & Meyer 2005). The main reason for this regression is the destruction and the fragmentation of their environment (Hofer et al. 2001). Indeed snakes require various environments in order to complete their life cycle, including a hunting area, open segments for thermoregulation, covered sites for daily shelters, oviposition and hibernacula sites, etc… Increasing urbanisation and draining of wetlands have drastically changed natural habitats and impacts on the species have sometimes become irreversible. Thus conservation plans for these species must be focused mainly on renaturalisation of the landscape as well as to preserve and manage the remnant habitats optimal for reptiles. The viperine snake, Natrix maura (Linnaeus 1758) is a highly threatened semi-aquatic snake, considered as critically endangered (CR) on the last Red List of the Swiss Threatened Reptiles (Monney & Meyer 2005). Hofer et al. (2001) suggested that pollution, human disturbance and landscape modifications are the major reasons for the decline of this species. But locally, other threats may negatively impact population size of viperine snakes. Indeed, the dice snake (Natrix tessellata Laurenti 1768), which was voluntarily introduced on the

shores of Lake Geneva near Le Lavaux between Vevey and Lausanne since the 1920s (Morton 1925), with specimens mostly from the lower Ticino, southern Switzerland (Mebert 1993, 1996), has a very similar ecological niche and possibly poses a competitive threat on N. maura. Since its first introduction and subsequent ones in the 1950s and 1960s (J. Garzoni and S. Monbaron pers. comm.), the population size of this alien species appears to have increased dramatically to become the dominant semi-aquatic snake species at the Le Lavaux region. Koller & Ursenbacher (1996) estimated the adult female population size of the viperine snake at 300 individuals compared to 500 adult females of local dice snakes. Later, a study summarizing observations from 1996 to 2006, clearly showed a major reduction of the viperine snake population and a simultaneous increase of the dice snake numbers (Ursenbacher et al. 2006). Recent studies deal with the dietary aspect of this local native-invasive system (Metzger et al. 2009, Metzger et al. 2011). In order to preserve this remnant population of N. maura, additional knowledge about the role of the potential interspecific competition with the dice snake is needed. This study was consequently focused on the habitat occupancy by the two species. The aim was to analyse the habitat at Le Lavaux where the two snakes coexist between St-Saphorin and Epesses, in order to find potential differences in the utilization of the hab-

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itats and consequently propose a management plan to improve the state of the native species. Material and Method The study consisted of three phases. First, the different habitats in the study area (Le Lavaux, Lake Geneva, Switzerland), which stretches along 4 km shoreline between St-Saphorin and Treytorrens, were defined. Second, the different habitats were described in details, and third, the frequency of each species in the different habitats was estimated. For each phase a specific protocol was conducted. The study area was split into three geographic sections (variable 3, Tab. 1): St-Saphorin, Rivaz and Treytorrens. The habitat evaluation was carried out only between the lake and the parallel running railway (a section between 1 and 10 m width), where most of the individuals have been observed. Primary Habitat Variables (Linear Segmentation) Two criteria were evaluated to define the primary nature of available habitat along the shoreline. First, the habitats were categorized as “slope” or “wall” (variable 1, Tab. 1). The former category represents a shore segment con-

sisting of a more or less gentle slope between the lake and the railway (Fig. 1). The latter category was made of a vertical concrete wall that raises from the lake (Fig. 2), and whose horizontal top, interspersed with some vegetation, was frequently used by basking snakes, sometimes limiting drastically the snakes’ access to the lake. The second main criteria related to the vegetation cover. Both “wall” and “slope” habitats were categorized depending on the principal vegetation structure and the dominant stratum (variable 2: secondary structure). This first protocol allowed determining the main groups of habitat along the lake’s shore. Secondary Habitat Variables An additional protocol was applied with a secondary set of variables that describes the various habitats in more details. The following characteristics were noted: general data (variables 3–7, 13–15: coordinates, surface, degree of the slope, orientation, access to the lake, granulometry of stones/blocks, i.e. measurement of their size distribution, proportions of concrete embankment and sections without vegetation), characteristics of the feet of the lakeside embankment (first ca. 0.5–1.0 m from the waterline; variable 8–12: mineral composition, presence/ absence of vegetation, type of vegetation), surface char-

Table 1: List of variables used to describe the different habitats where Natrix maura and N. tessellata coexist. Variables 1) Main structure 2) Secondary structure (principal vegetation cover) 3) Site 4) Length of habitat (parallel shoreline) 5) Width of habitat 6) Angle of slope (degrees) 7) Orientation 8) Lakeside embankment 9) Vegetation of the lakeshore 10) Ivy plants on the lakeshore 11) Bushes on the lakeshore 12) Trees on the lakeshore 13) non-obstructed access to the lake 14) Diameter of shore stones (centimetres) 15) Percentage of concrete surfaces (percent) 16) Surfaces without vegetation (percent) 17) Presence of mowing waste 18) Presence of humus 19) Length of the littoral zone (meters) 20) Vegetation height (centimetres) 21) Humidity, sensu Landolt (1977) 22) Luminosity, sensu Landolt (1977) 23) Temperature, sensu Landolt (1977) 1

Categories Slope or wall 1 9 types of slopes / 6 types of walls St-Saphorin / Rivaz / Treytorrens Meters Meters 60° SW / S / SE Stone blocks / beach / other Yes / No Yes / No Yes / No Yes / No Yes / No 100 No / 75 No / 75 Yes / No Yes / No / Other 10 300 1/2/3/4/5 1/2/3/4/5 1/2/3/4/5

as described in Material and Method

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acteristics of the slope or wall (variables 16–18: mean, percentage of surfaces without vegetation, presence/absence of mowing waste and humus), the aquatic habitat (variable 19: width of the first meters of the littoral zone, the area between the average waterline on the shore and the outer line where the prodominant rocks/stones still break trough the water surface), determination of the dominant plant species (not listed) its height (variable 20), and climatic factors (variables 21–23: humidity, temperature and amount of sunshine based on the vegetation and Landolt evaluation [cf. Landolt 1977]). The total of 23 variables and the selected categories are listed in Table 1 and examples of a slope and a wall habitat are depicted in Figures 1 and 2. Natrix Observation Protocol The number of observed individuals of both species was noted for all different habitats. The entire site (4 km) was searched 17 times between 16 July and 11 August 2007. The observations where conducted without catching the snakes. Although both species have different probability to be observed (variable “catchability”; N. tessellata have a higher catchability, SU unpubl. obs.), the variability in the percentages of N. maura observed is proportional to the variation of the percentage of occurrence of N.

Fig. 1: Study area considered as “Slope” (see Tab. 1)

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maura. Consequently, if the percentage of N. maura in one habitat is twice that in another habitat, the real proportion in the former segment is also twice as large. Additional information such as weather conditions and localisation (GPS coordinates) were also noted. Statistical Analyses We tested if a significant higher or lower proportion of viperine snakes were observed for some of the 23 retained variables using a test of proportion (also known as binomial distribution test). Statistical analyses were conducted with the program Minilab®, which produces exact P-values without particular conditions (ChavazCirilli pers. comm.). However the statistical tests were conducted only when the total number of Natrix specimens was ≥ 15 individuals per habitat type. Results We determined 86 different habitats (all have at least one different value of the 23 variables) in the study area, which was estimated at about 14,000 m2. One fourth was considered as “wall”, the rest being categorized as “slope”. We observed 387 Natrix specimens (307 N. tes-

Gaëtan Mazza, Jean-Claude Monney & Sylvain Ursenbacher

cies or latter species competitively displaces the native species. Compared with Treytorrens and Rivaz, St. Saphorin is more exposed to the south (82%) and contains a higher proportion of concrete surface (14%, compared to only 4% in Treytorrens). The shore at St. Saphorin yields also a narrower littoral zone, as 45% of its littoral zone is less than 5 m wide. Its vegetation is also short and mainly (76%) ranges between 0.5 and 1.0 m. In Treytorrens 138 dice snakes (74.6%) and 47 viperine snakes (25.4%) were observed. Even though the alien species is still more frequent, the proportion of the native species is considerably higher than in St. Saphorin. Here, 33% of the littoral surface is oriented to the southwest, and 30% consists of a “wall” with a vegetation strip on top. The vegetation at Treytorrens is slightly more humid compared to St-Saphorin. Discussion Distinct Results in the Different Geographic Sections

Fig. 2: Study area considered as “Wall” (see Tab. 1)

sellata = 79%, and 80 N. maura = 21%). To simplify, we subsequently used a proportion of 80% of dice snakes and 20% of viperine snakes for subsequent analyses from this region. Statistical Analyses Dice snakes were significantly more frequent in the StSaphorin area (binomial test, P = 0.001), as well as where the slope is more orientated to the south (P = 0.036) or the proportion of concrete is larger on the banks (≥75% of concrete; P = 0.007). In addition, the proportion of dice snake is also significantly higher when the bank is steeper (P = 0.047) or with a short vegetation height of 0.5–1.0 m (P = 0.032). On the other hand, the observed frequency of viperine snake is significantly higher at Rivaz (P = 0.05) or where most of the habitat structure consists of vertical “walls” with a grassy strip on the top (P = 0.044). A marginally significant higher proportion of N. maura was also observed at Treytorrens (P = 0.065), as well as where the slope is orientated to southwest (P = 0.052), or where there was a higher mean humidity (P = 0.051). The habitat characteristics at St. Saphorin, where only three viperine snakes of a total 80 Natrix specimens were observed, either seem to be more suited to the alien spe-

The study revealed important differences on interspecific use and possibly preferences of the available habitats between the two Natrix species. Indeed the environment at St-Saphorin is statistically more favourable to the dice snake, whereas those at Rivaz and Treytorrens seem to be slightly more preferred by the native viperine snake. In 2007, a removal program of the alien dice snake was initiated by two of the authors (SU and JCM) that focused on Rivaz area. More than 100 dice snakes had already been removed during this study. This program consequently could have biased the results for the Rivaz region presented herein, and hence, the discussion will be focused on the two other areas, St-Saphorin and Treytorrens. The results indicate that St-Saphorin is less favourable to the viperine snake as this section is more orientated to the south, the littoral zone is often very short and the vegetation is relatively high. On the opposite, the Treytorrens section seems more preferred by the native species due to a more southwestern orientation of the coast with more “wall” habitats characterized by a strip above of short vegetation. These different habitat parameters between St. Saphorin and Treytorrens could be associated to distinct habitat requirements by the two species and might explain the different proportions of each species observed. However, no such studies have been performed here or elsewhere that would confirm such interspecific differences. Only Scali et al. (2001) and Scali (2011) demonstrated the use of different microhabitats between both species, as well as different feeding behaviour. However, our location is clearly different, because the only available food is fish and the habitat size and variation is very limited. Consequently, both species are not able to select or evade to substantially different ecological niches in this particular location.

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Biological Aspects One important factor differentiating the two species’ habitat is the orientation of the shores. It seems that the dice snake prefers southern orientation. We suggest that this species is comparatively more thermophilic and, hence, occupies habitat segments with a more direct solar radiation. Our observation is in contradiction to the conclusions of Hofer et al. (2001), who suggested that the dice snake prefers a south-western exposition. This conclusion was however based on the analyses of all locations of the dice snake in Switzerland, with most observations conducted in the Ticino region, southern Switzerland, where the species is native and more widespread. An explanation about this discrepancy could be the warmer climatic conditions in Ticino (compared to the shores of the Lake Geneva), where the dice snake is not required to seek the warmest locations. On the opposite, this species needs to find the warmest locations on the shore of Lake Geneva and consequently prefers southern exposition. This hypothesis could also explain why this species can be found in locations without any vegetation, thus experiencing warmer temperatures. On the opposite the viperine snake seems to be more related to habitats exposed to the south-west, which are more frequent in the Treytorrens and Rivaz sections. The solar radiation in these locations is perhaps limited and thus present less extreme conditions, that are perhaps more favourable to the native species. However, the viperine snake, which approaches its northern limit in Switzerland, obviously inhabits also these more thermophilic habitat, if the alien species would not be present, thus indicating a possible effect of competitive exclusion or displacement. A narrow littoral zone seems to be favoured by the dice snake. Indeed 42 N. tessellata were observed in such habitat compared to only four N. maura. The larger body size of the introduced species enables them to consume larger prey than the native species. Thus the viperine snakes can find smaller prey species in a shallower littoral zone. The dice snake on the opposite can feed on larger prey that occurs in relatively deeper water in the lake (≥ 5m), confirming comparative observations by Scali (2011). Another scenario suggests that the competition between the two species implies that the dice snake is the physically stronger competitor and occupies the more favourable places such as slopes, displacing the weaker native competitor to the less suitable habitat of vertical walls, where it indeed was more common. The habitats with the slope allow an easy access to the lake, which is relevant as the only feeding ground. By being competitively excluded, the native species may have to regroup in the “wall” habitats. In Rivaz and Treytorrens “wall” habitats represent 30% of the area compared to 13% St-Saphorin. However, no such competitive scramble behaviour has been observed between the two species, in particular dice snakes physically forcing viperine snake out of the suitable habitat along the slopes. Mech-

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anisms, by which such a direct competition should happen, are not known in snakes. But our additional observations may suggest that the viperine snake appears to be more agile than the dice snake, especially when the individuals contain any prey in their stomach. Therefore, N. maura is perhaps more adapted to climb walls and reach basking locations that are not easily accessible. Humidity is another factor that likely influences the selection of habitats. During the 17 sampling days, a high concentration of snakes (58 dice snakes and 21 viperine snakes) were found in Treytorrens along a gentle slope of 15 m that yielded a large portion of the blackberry Rubus fruticosus between two shrubby areas. Although, this location structurally resembled other habitats, the mean humidity estimated by the Landolt coefficients was the highest observed in this study. This parameter can be an explanation of the high density observed there, but other factors may also have an impact, such as the several composts in gardens of a nearby village that offer suitable places for oviposition in June and July. Observations of matings in those gardens and regular findings of newborns by the villagers corroborate this presumption. In addition, we also observed juveniles during this study near this village (five out of the six observed newborns). Management Suggestions Our results suggest that the main management proposals could be the creation of new nesting sites in the study area. Such sites should be mounds (min 1 m high) constituted of rests of mowing and cut branches, as have been used elsewhere (Gruschwitz et al. 1999). Incorporating additional holes and crevices in the concrete zones would increase the amount of vegetation in those places that are currently dominated by the alien dice snake. Indeed, a higher density of vegetation would favour the native viperine snake. Finally the eradication measures of the alien species should be extended, because at St-Saphorin (where no removal program is conducted) the alien species strongly dominates. Acknowledgements This work was conducted by GM as a Bachelor Thesis at the University of Applied Sciences – Western Switzerland (HESSO) of Lullier. We thank Claude Fischer for general help, Nicole Chavaz-Cirilli and Benedikt Schmidt for the help in statistical analyses and Patrice Prunier for botanical identifications, and Konrad Mebert for suggestions on the text. This work was conducted with the authorization and the support of «La Conservation de la Faune du Canton de Vaud» and the karch (Centre for the coordination of the protection of amphibians and reptiles of Switzerland).

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References Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Hofer, U., Monney, J.-C. & G. Dusej (2001): Les Reptiles de Suisse – Répartition, Habitats, Protection. – Birkhäuser Verlag, Basel, Switzerland. Koller, N. & S. Ursenbacher (1996): Etude et estimation de l’effectif de couleuvres vipérines (Natrix maura) et de couleuvres tessellées (Natrix tessellata) dans le Lavaux. – Travail de certificat. Lausanne, Université de Lausanne, Switzerland. Landolt, E. (1977): Ökologische Zeigerwerte zur Schweizer Flora. – Stiftung Rübel, Switzerland. Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Mebert, K. (1996): Comparaison morphologique entre des populations introduites et indigenes de Natrix tessellata de I’Arc Alpin. – Bull. Soc. Herp. Fr. 80: 15–25. Metzger, C., Ursenbacher, S. & P. Christe (2009): Testing the competitive exclusion principle using various niche parameters in a native (Natrix maura) and an introduced (N. tessellata) colubrid. – Amphibia-Reptilia 30: 523–531.

Metzger, C., Christe, P. & S. Ursenbacher (2011): Diet variability of two convergent natricine colubrids in an invasivenative interaction. – Mertensiella 18: 86–93. Monney, J.-C. & A. Meyer (2005): Liste Rouge des Reptiles Menacés en Suisse. Edit. Office Fédéral de l’Environnement, des Forêts et du Paysage, Berne, et Centre de coordination pour la protection des amphibiens et des reptiles de Suisse (karch), Berne. – Série OFEFP: L’environnement pratique. Morton, W. (1925): Une nouvelle couleuvre pour la faune vaudoise. – Bulletin de la Société vaudoise des Sciences naturelles 56: 181–183. Scali, S. (2010): Ecological comparison of the dice snake (Natrix tessellata) and the viperine snake (Natrix maura) in northern Italy. – Mertensiella 18: 131–144. Scali, S., Dimitolo, G. & S. Montonati (2001): Attivita notturna comparata di Natrix maura e Natrix tessellata. – Pianura Scienze e storia dell’ambiente padano 13: 287–290 Ursenbacher, S., Monney, J.-C. & U. Hofer (2006): Diminution des couleuvres vipérines (Natrix maura) observées dans le Lavaux et implication des couleuvres tessellées (Natrix tessellata) dans cette diminution. – Résumé du 13ème colloque herpétologique du KARCH. Berne, Switzerland.

Authors Gaëtan Mazza, Rue d’Or 12, CH-1700 Fribourg, Suisse, e-mail: [email protected]; Jean-Claude Monney, karch, Centre de Coordination pour la Protection des Amphibiens et des Reptiles de Suisse, Passage Maximilien-de-Meuron 6, 2000 Neuchâtel, Switzerland; Sylvain Ursenbacher, Department of Environmental Sciences, Section of Conservation Biology, University of Basel, St. Johanns-Vorstadt 10, 4056 Basel, Switzerland, e-mail: [email protected].

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Diet Variability of Two Convergent Natricine Colubrids in an Invasive-Native Interaction César Metzger, Philippe Christe & Sylvain Ursenbacher Abstract. In cases of introductions where the exogenous species is morphologically and ecologically very convergent with one, or more, of the native species, the potential for resource (trophic, territory, sun, shelter, etc.) competition is high. In this regard we investigated in 2007 and 2008 the potential role of trophic resource competition in the invasive-native species system Natrix maura-N. tessellata on the shores of Lake Geneva in Switzerland, of which this paper is the follow-up. We confirmed, among other results, a strong similarity in the diet of both species and were able to calculate a large overlap of their trophic niches (Metzger et al. 2009). In addition to that work we report herein patterns of within-year variation of the diets of both snakes, and report on the observation of individual foraging behavior observed in an artificial environment. Key words. Alien species, colubrids, diet, foraging behavior, Natricinae, seasonal variation

Introduction Introduced species may play a key role in the ecosystem in which they have established themselves, even more so when they show patterns of invasiveness. After a period during which the newly introduced species is almost undetectable in the environment, called the lagging period, its population may grow sometimes dramatically (Elton 1958, Williamson 1996). It is often then that the invasion is detected and characterized as such. Those invasive species may become very problematic when cohabiting with ecologically similar species. Direct (e.g. predation, territorial exclusion) or indirect (e.g. food, hibernaculas) competition may arise and start reshaping the local species populations (Wilcove et al. 1998, Byers 2000). Natrix maura and N. tessellata are very similar species even though they have a mostly allopatric distribution (Guicking et al. 2008). Both species cooccur naturally only in a few locations in northern Italy (Scali 2011). Although not adelphotaxons (sister species), both species are ecologically and morphologically very convergent probably due to adaptation to similar ecological niches (Gruschwitz et al. 1999, Schätti 1999), using the environment in seemingly similar fashion (Metzger et al. 2009, Mazza et al. 2011), and having a similar diet in allopatric regions (Bilcke et al. 2006 for a review, Santos et al. 2006, Luiselli et al. 2007) as well as in our region of sympatry in southwestern Switzerland (Metzger et al. 2009). Clear genetic segregation between both species has been shown by phylogeographic studies (Guicking et al. 2006, Guicking et al. 2008) and although some rare events of hybridization in captivity have been reported, none in the wild have ever been found (Kabisch 1999, Schätti 1999). The dice snake was introduced into several lakes north of the Alps in Switzerland, where it is extralimital

of its natural distribution area (Mebert 1993, Lenz et al. 2008). An initial introduction (first mention 1925: Morton 1926) followed by subsequent introductions in the 1950s and 1960s (Garzoni & Monbaron pers. comm.) on the northern shore of Lake Geneva led to a large population of hundreds of individuals. After 10 years of monitoring of this invasive-native species system (1999 to present, Koller & Ursenbacher 1999, Monney 2004, Ursenbacher & Monney 2007, Ursenbacher & Monney 2008, Mazza et al. 2011, Ursenbacher et al. submitted) the decline of the native colubrid population was estimated at -4.4% per year (Ursenbacher et al. submitted), indicating potential effect of the introduced species on the native one. In order to evaluate if a competition for food occurs and to better understand the feeding behavior of both species coexisting in the the same region of Lake Geneva (also called Lake Leman) in southwestern Switzerland, we studied in situ the invasive-native species system N. maura-N. tessellata along the shores of the lake, as well as in vitro in an aquarium setting for basic behavioral observations at the University of Lausanne. In this paper we report on our use of a comparative diet analysis to evaluate trophic regime variation from stomach contents of wild caught snakes and direct observation of feeding behaviors in aquaria to understand the ecological types of prey species found in the snakes’ diets. The present report is an accompanying document to Metzger et al. (2009). Material and Methods Study Area The area of introduction of Natrix tessellata is situated on the northern shore of Lake Geneva, in the region called the Lavaux (about 70 km east-north-east from Geneva, Switzerland). The species occurs in a nar-

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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row strip of riparian slope of about 3.5 km in length and 3 to 10 meters in width, which was used as a transect for sampling the snakes. This zone is appropriate for ecological and conservation studies, since it is narrow and severely hinders natural dispersion of the species due to its natural (deep and broad lake) and artificial barriers (abutting and uphill to the north of the habitat are: railroad tracks, a 5 to 10 m high concrete wall, a road; and on the eastern and western parts the area is flanked by urbanized regions such as towns or villages). These barriers also hinder the access for potential land-dwelling predators and humans resulting in a rather calm and safe area for snakes. It also limits the possible adaptation to other ecological niches. With its good geographical orientation (southerly exposed) this rather xeric slope terrain (between about 12° and 40° slope) receives optimal solar radiation and temperature conditions during most of the active field season. In addition the easy access to a large reservoir of trophic resources in the lake permits abundant feeding. As a result of all these beneficial conditions, this region has one of Switzerland’s highest density of reptiles (Koller & Ursenbacher 1999, Metzger et al. 2009). Unlike other regions inhabited by these snake species (Bilcke et al. 2006, Santos et al. 2006, Luiselli et al. 2007), this area is entirely devoid of amphibians, thus leaving only fish as available trophic resource (Monney 2004). The area also has heterogeneous vegetation, with patches of naked stones, pioneer vegetation interspersed between larger sections of highly vegetated terrain (Metzger et al. 2009, Mazza et al. 2011).

Artificial Environment Observations Twenty snakes, ten of each species, were kept in heterospecific pairs for 2 to 5 days in aqua-terraria with simulated lake bottom conditions (rocky bottom, with some larger rocks scattered around) and fed after 24 hours of acclimation with either one open-water free-swimming fish (either a roach, Rutilus rutilus, or a perch, Perca fluviatilis) or a small shoal of roach. The behavior and hunting strategies of the snakes in presence or absence of the prey were assessed by visual observation from the side or the top of the tank. To reduce the risk of distractions or disturbances by external, artificial incentives (e.g. humans passing by the tank), all sides of the aqua-terraria were blocked by card-board, leaving only a thin longitudinal opening to observe the inside of the tank. The top of the aqua-terraria was not blocked but nothing else than lights and the roof was visible over the aqua-terraria. The terrarium part of the installation consisted of a wooden box with an opening on its bottom to let the snakes access the aquarium part, again reducing visual distractions for the snakes (Fig. 1).

Data Sampling Fieldwork consisted of manually capturing snakes of both species along the transect during the activity season in 2007 (July and August) and in 2008 (May through September). Sampling lasted between 5 and 7 hours, starting when the first solar radiations reached the ground in the area, which coincides with the earliest possible sightings of snakes (Metzger pers. obs.). Upon capture snakes were measured (snout vent length; to the nearest mm), weighted (to the nearest 0.1 g), their sex was determined by examining the sexual dimorphic shape of tail root (Mebert 1993; juveniles were not sexed due to the potential risk of incorrect sex determination: Filippi 1995), their exact geographical location and time and date of capture were recorded. Regurgitation reflex was induced by gentle ventral palpation. Regurgitated prey items were measured (length and width, sensu Delling 2003, see also Metzger et al. 2009 for a more detailed explanation), and determined in the field when possible, or otherwise preserved in 70% EtOH for further careful examination.

Fig. 1. In vitro observational set-up. Top-part shows the “dry area” or terrarium, lower part the “wet area” or aquaria. Passage from one to the other area was allowed by a large tree branch lying on an inclined slate, represented in the figure only by an inclined plane.

Statistical Procedure We used a fairly new procedure to estimate the similarity of the seasonal variations in diet of both snake species. This procedure, called PerMANOVA, is a nonparametric method for multivariate analysis of variance based on a multivariate analogue to Fisher’s F-Ratio and using subsequent permutations to calculate the P-value (Anderson 2001). It was analyzed using the software R (version 2.4.1, R Development Core Team 2006) with

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the Vegan Package and its ‘adonis’ function (Oksanen et al. 2007). Results We captured and measured 77 Natrix maura (58 females, 13 males and 6 juveniles) and 213 N. tessellata (158 females, 33 males and 22 juveniles). Only 22% of females and 15% of males regurgitated identifiable prey items, and thus were included in the analysis. Juvenile regurgitations (three of each natricine species) were not included in the analysis for obvious statistical reasons and sex determination problems. The prey species examination using both, external (color, shape) and internal characters (counting of fin rays), resulted in the identification of six distinct Actinopterygii species of which five were found in both predators’ stomach contents and only one species (Lota lota, the burbot) was found twice in N. tessellata solely. The three most frequent prey species in both snakes’ diets, occurring in the same order of predominance in both snake species, were: Cottus gobio (the European bullhead, 43.5% in N. maura and 61.4% in N. tessellata), Perca fluviatilis (the European perch, 26.1% in N. maura and 14.1% in N. tessellata), Rutilus rutilus (the common roach, 17.4% in N.maura and 10.5% in N. tessellata). Other, less frequent prey types in the diets of both snakes were the common bleak (Alburnus alburnus) with 4.3% in N. maura and 7.0% in N. tessellata

and the gudgeon (Gobio gobio) with a higher prevalence of 8.7% in N. maura as that in N. tessellata of only 3.5%. The burbot was found twice in N. tessellata, which represented 3.5% of its diet. No significant diet difference between the two snake species was found as detailed in Metzger et al. (2009). Seasonal Variation in Diet Composition Plotting the regurgitated prey against date of regurgitation showed a distinct pattern in prey capture per month. In Figures 2a and 2b, seasonal diet of the two natricines show a similar pattern of prey types captured per month. The frequency of C. gobio, the most frequently preyed fish, was higher in the early season and decreased until the mid-season. Snakes started to regurgitate P. fluviatilis in July and did so until the end of the season. R. rutilus was regurgitated throughout most of the season, with the exception of May where none of this species was recovered. A. alburnus was only occasionally regurgitated during the months of June and July. The data with L. lota is to be taken with caution since only two specimens were regurgitated in July and both by N. tessellata. Due to similarity between the diet patterns observed in both species (PerMANOVA, F = 0.161, P = 0.96) we pooled the datasets to obtain an overall view of the captured species per month throughout both years of fieldwork (Figs. 2c, d). With up to 46.15% of the to-

Fig. 2. Percentage of regurgitated prey species by month in (a) Natrix maura; (b) Natrix tessellata; and (c) both snake species pooled. (d) Number of regurgitated prey species by month, both snake species pooled.

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tal amount of regurgitations, June was the month with the highest number of recovered prey items, followed by July with 26.92% of the regurgitations, August with 11.54%, and May with 10.26%, respectively. September, the last month of the active season showed also the least amount of recovered prey items with only 5.13%. Diet Variation with Regard to Geographical Location Plotting the prey species regurgitated against the position along the transect, where the predator was captured, showed some structuring along the shore (Fig. 3). Especially C. gobio and P. fluviatilis had an uneven distribution along the shore with the latter predominantly found between kilometers 10.2 and 11.4 and the former between kilometers 11.4 and 11.7 and again between 12.1 and 13.1. Although the boundaries were not clear and with some overlap, regions with a predominance of one of the two species of prey were observed. The other prey species were not regurgitated in large enough proportions to show regional partitioning tendencies along the transect. Foraging Behaviors The observation of 10 different snakes of each species in artificial conditions allowed us to identify five distinct hunting strategies to hunt three principal behavioral types of prey (Figs. 4, 5). Both species of snakes showed all five hunting strategies. Depending on the type of prey available in the tank the snakes would exhibit different hunting strategies. When the prey were bottom-dwelling fishes, or when there were no prey available to hunt, snakes would either actively search the gravel and rocks

Fig. 4. Categories of fish behavior.

with their head, using their bodies and tails in a slow swimming motion and move forward (Strategy N°1) or hold themselves to a rock with their tail to avoid floating up to the surface, their body in a distinct ready-to-strike S-shape and sit and wait at the bottom of the tank (Strategy N°2). This behavior, which we named the “lurking behavior”, was also exhibited when the prey were pelagic fishes, solitary or in shoals. In addition to the lurking behavior, pelagic fishes were also hunted actively with snakes swimming through fish shoals (Strategy N°3), although this method did not appear to be very effective. Provided a branch or any other support was stretched over the water surface, snakes would spend time on this support looking at the surface of the water or even stretching their body to maintain the head just under the surface of the water and observing the movements in water (Strategy N°4). This passive strategy was rather an observation behavior than a hunting behavior per se, since no fish were ever captured directly from this position. But if a fish was spotted, the snake would immediately slide into the water and swim after the fish, another marginally effective hunting behavior (Strategy N°5).

Fig. 3. Distribution of regurgitated prey species along the transect.

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Fig. 5. Categories of snake hunting strategies and behaviors.

Prey Handling In Metzger et al. (2009) we showed that 97.5% (n = 80) of collected prey were regurgitated tail first, which means that snakes ate their prey headfirst in almost every case. In our aqua-terraria observations snakes would catch fish by biting them at any random position on the fish body. The fish were in most cases dragged out of the water and then the snake would progressively move its upper and lower jaws alternately to position the prey headfirst in its mouth. Sometimes, when snakes did not manage to get out of the water quickly, the prey repositioning motion would be executed in the water. Discussion In a previous study we showed that the diet composition of the two natricine colubrids studied was significantly similar, with a strong overlap (between 75 and 95 %) of the trophic niches (Metzger et al. 2009). We show here that the composition of the diets of both snakes is not constant throughout the season but is subject to important variations. Both species showed similar patterns of variation in diet composition, indicating that this variation is not predator specific but rather due to some environmental or third party factors directly or indirectly acting on the availability of prey or even on the prey

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populations in the lake. The early season as well as the late season (months of May and September) did not yield many regurgitated prey, as during these months not many snakes were captured due to the variably bad weather and colder temperatures. In addition, variance in the sensitivity of snakes to seasonal climatic changes can account for snakes becoming active at different time points in late April, in May, and even in early June, depending on the temperature and humidity. Variation in the hibernaculas’ permeability to external temperature and humidity variations might also influence the emergence of each snake. A similar reasoning can be applied to the end of the season, when snakes progressively return to their hibernaculas. The main season (end of May to end of August) had a good abundance of regurgitated prey. Variation in prey species abundance in the regurgitations during the main season may be accounted for by seasonal migrations of fish species. Fish have been shown to demonstrate patterns of diel migration as well as migration throughout the season in response to various incentives such as temperature changes at various depths in the water column, migration and abundance of plankton and search for spawning places among others (Lucas & Baras 2000, 2001). Although some of the species captured by N. maura and N. tessellata have more sedentary behaviors, such as the bullhead (C. gobio: Morris 1954, Knaepkens et al. 2005, Smyly 1957), others are clearly

César Metzger, Philippe Christe & Sylvain Ursenbacher

open-water free-swimming migratory fishes (perch, P. fluviatilis: Allen 1934, Wang & Eckmann 1994, Eckmann & Imbrock 1996, roach, R. rutilus: Vøllestad & L’Abée-Lund 1987, L’Abée-Lund & Vøllestad 1987, Horppila et al. 1996, Järvalt et al. 2005). The major variation can also be explained by the birth and growth of cyprinids and perch during the season, reaching sizes big enough for the snakes to predate in July and August. At that time, big shoals of late juveniles (subadults) search for food along the shore and can consequently be eaten by the two Natrix species. In addition to seasonal variation, a certain portion of the variation could be explained by capture success, some prey species being far easier to capture. The bullhead is a rather sedentary fish, sheltering under rocks during the day and being more active at night (Tomlinson & Perrow 2003). It would make a perfect prey for the colubrids that are active during the day, searching the bottom of the lake for fish hidden between rocks. We were able to confirm this behavioral tendency by observing 10 snakes kept in tanks in the laboratory with no specific treatment other than a recreated facsimile of the natural environment and feeding them every 4–5 days with live fish. Observational Study In order to better understand the foraging behavior of N. maura and N. tessellata and better interpret the results obtained from the diet analysis, we set up 20 snakes, 10 from each species, in aqua-terraria and observed their foraging and feeding behaviors. Although we tried to control for potential biases, such as disturbances to snakes and their prey by visual cues of movements outside the aqua-terraria, artificial environment behavioral studies will always remain somewhat biased due to the very simple fact that they are done in artificial environments. Nonetheless in our case, the observation of the foraging and feeding behavior of the snakes in such conditions may still bring some realistic elements of response and contribute to our general understanding of their natural behavior. Predators which are not very specialized on one type of prey need to be able to exhibit various hunting strategies in order to cope with the various behaviors exhibited by their prey. From the regurgitation data, we were able to identify species of prey that belong to very different behavioral types of fish including pelagic and benthic fish but also diurnal and nocturnal ones. N. maura and N. tessellata, being ectothermic and thus mostly diurnal organisms in the temperate climate of continental Europe, hunt predominantly during the day. Hunting requires the expenditure of large amounts of energy, even more when hunting in a large body of water such as Lake Geneva where constant swimming in variable water currents is required. Indeed swimming requires a lot of energy and the water is colder than the air during the summer, which decreases the body temperature

of the organism, lowering at the same time the available energy for motor activity. Catching nocturnal prey is possible for diurnal predators by actively searching between and under rocks for the day shelters of those prey. C. gobio is known to take shelter under rocks during the day and thus is an easy prey, which might contribute to their high prevalence in the snakes’ diets. All other prey items regurgitated are diurnal pelagic fishes, mostly swimming in shoals. To catch these prey snakes developed mainly two strategies, the passive “sit-andwait strategy”, or lurking behavior (also termed ambush behavior), and the active “swimming through the shoal strategy”. While the first strategy appeared to be more efficient by catching prey with a precise and fast strike, the low amount of prey swimming by close enough to be caught by such strikes lowered this strategy’s comparative success. On the one hand swimming through a shoal is less efficient at catching the prey but there are a lot more prey available close by which in turn increases the success rate. The optimization of success rate probably explains why both strategies are being exhibited and neither one was selected against. Due to obvious morphological constraints fish cannot be ingested in every way. They can either be eaten headfirst or tail first. But our observations confirmed the data from our previous study (Metzger et al. 2009), which showed prey being almost always eaten headfirst. We argue here that this behavior has evolved for two reasons. Fish have scales and fins that are strong solid structures, sometimes very sharp and long, but invariably growing outwards of the body in an aboral (away from the mouth) orientation. Thus eating a prey tail first might be hindered by the fins and scales protruding, and could eventually lead to the wounding of the predator. Secondly when the predator is hunting in the water, especially in larger bodies of water such as lakes, it might have to swallow its prey while still in the water. If the snake manages to place the prey headfirst in its mouth, the chances that the prey will escape by swimming are decreased since fish are highly efficient at swimming forward but only marginally so backwards. In addition to this, many fish species, when caught by a predator show sudden tail thrashes to liberate themselves from the predator. These thrashes were also observed in fishes caught headfirst by the snakes, but the ensuing result was that the fish pushes itself quicker into the mouth of the snake. This could be a case of counter adaptive fleeing behavior of fish, selected for by other predators’ different hunting strategies (such as larger fish, or diving piscivorous birds that might not care about the orientation of the prey caught). Implications for the Invasive-Native Species System The herein shown similar pattern of seasonal variation in diet of both snake species, and taking into account the large diet overlap index calculated in Metzger et al. (2009), corroborating the aforementioned conclu-

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sion, implies a seasonal variation in the composition of the fish community in this region. Potential effects of this variation on the invasive-native species system in question are unclear. We hypothesize that the early season, and the accessibility to prey during this period of higher energetic requirements (cool weather, reduced sunlight, mating activities, reproduction and preparation of the females for gestation are factors which happen early during the year in both species in this region, J.-C. Monney pers. comm.), may impact the reproductive success of the females and thus ultimately the overall fitness of the species. In the past 11 years of monitoring both species in this region, a clear tendency for earlier emergence from hibernation in N. tessellata than in N. maura was observed (pers. obs., and J.-C. Monney pers. comm.), which could give the former species a head start on feeding, especially considering that in the early season the availability of prey appeared to be reduced. We suggest that this longer feeding period of N. tessellata from emergence to oviposition can account for their tendency to produce more eggs (Ursenbacher et al. submitted) and it might even influence the quality of the eggs produced (more reserves in the eggs, leading to stronger juveniles at hatching) resulting in an increased fitness. Together with our observations and conclusions, the yearly N. maura population decline calculated by Ursenbacher et al. (submitted) indicates an indirect detrimental effect of the introduced N. tessellata on the native N. maura. Further investigations are needed, and are underway, to understand the exact nature of the (probably) indirect interaction leading to the slow replacement of the local species by its congeneric competitor. Acknowledgments G. Mazza, G. Cisarovsky, C. Longchamp, and J.-C. Monney were very helpful during sampling in the field. J.-C. Monney, G.-D. Guex and Konrad Mebert helped with useful insights and teachings. M. Hall gave us some of his time for statistical advice. Our research was supported by the KARCH and the Conservation de la Faune du Canton de Vaud (C.M. and S.U.). The handling and study of live snakes was allowed by the Conservation de la Faune du Canton de Vaud (Autorisation spéciale N°974) and the Service de la Consommation et des Affaires Vétérinaires du Canton de Vaud. References Allen, K.R. (1934): The food and migration of the perch (Perca fluviatilis) in Windermere. – Journal of Animal Ecology 4(2): 264–273. Anderson, M.J. (2001): A new method for non-parametric multivariate analysis of variance. – Austral Ecology 26(1): 32–46. Byers, J.E. (2000): Competition between two estuarine snails: implications for invasions of exotic species. – Ecology 81(5): 1225–1239.

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Bilcke, J., Herrel, A. & R. Van Damme (2006): Correlated evolution of aquatic prey-capture strategies in European and American natricine snakes. – Biological Journal of the Linnean Society 88: 73–83. Delling, B. (2003): Species Diversity and Phylogeny of Salmo with Emphasis on Southern Trouts (Teleostei, Salmonidae). – Stockholm University, Stockholm, Sweden. Eckmann, R. & F. Imbrock (1996): Distribution and diel vertical migration of Eurasian perch (Perca fluviatilis L.) during winter. –Annales Zoologici Fennici 33: 679–686. Elton, C. (1958): The Ecology of Invasions by Animals and Plants. – London, UK, Methuen. Filippi, E. (1995): Aspetti dell’Ecologia di due Communità di Colubridi e Viperidi (Reptilia, Serpentes) di un’Area dell’Italia Centrale (Monti della Tolfa, Lazio). – unpubl. M.S. thesis, Università “La Sapienza”, Rome, Italy. Guicking, D., Griffiths, R.A., Moore, R.D., Joger, U. & M. Wink (2006): Introduced alien or persecuted native? Resolving the origin of the viperine snake (Natrix maura) on Mallorca. – Biodiversity and Conservation 15: 3045–3054. Guicking, D., Joger, U. & M. Wink (2008): Molecular phylogeography of the viperine snake Natrix maura (Serpentes: Colubridae): evidence for strong intraspecific differentiation. – Organisms Diversity and Evolution 8: 130–145. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Horppila, J., Malinen, T. & H. Peltonen (1996): Density and habitat shifts of a roach (Rutilus rutilus) stock assessed within one season by cohort analysis, depletion methods and echosounding. – Fisheries Research 28(2): 151–161. Järvalt, A., Krause, T. & A. Palm (2005): Diel migration and spatial distribution of fish in a small stratified lake. – Hydrobiologia 547: 197–203. Kabisch, K. (1999): Natrix natrix (Linnaeus, 1758) – Ringelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 513–580 Knaepkens, G., Baekelandt, K. & M. Eens (2005): Assessment of the movement behaviour of the bullhead (Cottus gobio), an endangered European freshwater fish. – Animal Biology 55: 219–226. Koller, N., & S. Ursenbacher (1999): Estimation de l’effectif de couleuvres vipérines (Natrix maura) et de couleuvres tessellées (N. tessellata) dans le Lavaux. – In: Bertola C., Goumand, C. & J.-F. Rubin (Eds.): Actes du Colloque Pluridisciplinaire “Découvrir le Léman, 100 ans après FrançoisAlphonse Forel”. – Musée du Léman, Slatkine, Nyon-Genève, Switzerland: 313–322. L’Abée-Lund, J.H. & L.A. Vøllestad (1987): Feeding migration of roach, Rutilus rutilus (L.), in Lake Arungen, Norway. – Journal of Fish Biology 30(3): 349–355. Lenz, S., Mebert, K., & J. Hill (2008): Die Würfelnatter (Natrix tessellata). – In: DGHT (Ed.): Die Würfelnatter – Reptil des Jahres 2009. – DGHT, Rheinbach, Germany: 6–32. Lucas, M.C. & E. Baras (2000): Methods for studying spatial behaviour of freshwater fishes in the natural environment. – Fish and Fisheries 1(4): 283–316 Lucas, M.C. & E. Baras (2001): Migration of Freshwater Fishes. – Wiley-Blackwell, West-Sussex, UK.

César Metzger, Philippe Christe & Sylvain Ursenbacher Luiselli, L., Capizzi, D., Filippi, E., Anibaldi, C., Rugiero, L. & M. Capula (2007): Comparative diets of three populations of an aquatic snake (Natrix tessellata, Colubridae) from Mediterranean streams with different hydric regimes. – Copeia 2007: 426–435. Mazza, G., Monney, J.-C. & S. Ursenbacher (2011): Structural habitat partitioning of Natrix tessellata and Natrix maura at Lake Geneva, Switzerland. – Mertensiella 18: 80–85. Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti 1768) in der Schweiz und im südlichen Alpenraum. – unpubl. M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Metzger, C., Ursenbacher, S. & P. Christe (2009): Testing the competitive exclusion principle using various niche parameters in a native (Natrix maura) and an introduced (N. tessellata) colubrid. – Amphibia-Reptilia 30: 523–531. Monney, J.-C. (2004): Monitoring de Populations de Peptiles dans le Canton de VD, 1999–2003. – Rapport interne non publié 22, Koordinationsstelle für Amphibien- und Reptilienschutz in der Schweiz, Neuchâtel, Switzerland. Morris, D. (1954): The reproductive behaviour of the river bullhead (Cottus gobio L), with special reference to the fanning activity. – Behaviour 7(1): 1–32. Morton, W. (1926): Une nouvelle couleuvre pour la faune vaudoise. – Bulletin de la Société Vaudoise des Sciences Naturelles 56: 181–183. Oksanen, J., Kindt, R. Legendre, P. & B. O’Hara (2007): vegan: Community Ecology Package version 1.8-5. http://cran.rproject.org/ Santos, X., Vilardebo, E., Casals, F., Llorente, G.A., Vinyoles, D. & A. De Sostoa (2006): Wide food availability favours intraspecific trophic segregation in predators: the case of a water snake in a Mediterranean river. – Animal Biology 56: 299–309. Scali, S. (2011): Ecological comparison of the dice snake (Natrix tessellata) and the viperine snake (Natrix maura) in northern Italy. – Mertensiella 18: 131–144.

Schätti, B. (1999): Natrix maura (Linnaeus, 1758) – Vipernatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 483–503. Smyly, W.J.P. (1957): The life history of the bullhead or miller’s thumb (Cottus gobio L.). – Proceedings of the Zoological Society of London 128: 431–453. Tomlinson, M.L. & M.R. Perrow (2003): Ecology of the Bullhead. Conserving Natura 2000 Rivers Ecology Series 4. – English Nature, Peterborough, England. Ursenbacher, S. & J.-C. Monney (2007): Conservation de la couleuvre vipérine (Natrix maura) sur les rives lémaniques: éradication de la couleuvre tessellée (Natrix tessellata). – Rapport préliminaire interne non publié, Koordinationsstelle für Amphibien- und Reptilienschutz in der Schweiz, Neuchâtel, Switzerland. Ursenbacher, S. & J.-C. Monney (2008): Conservation de la couleuvre vipérine (Natrix maura) sur les rives lémaniques: éradication de la couleuvre tessellée (Natrix tessellata). – Rapport intermédiaire non publié, Koordinationsstelle für Amphibien- und Reptilienschutz in der Schweiz, Neuchâtel, Switzerland. Ursenbacher, S., Monney, J.-C. & U. Hofer (submitted): Capture-recapture study of the alien species, Natrix tessellata, and the native species, N. maura, in Switzerland: Will the native species survive? Vøllestad, L.A. & J.H.L’Abée-Lund (1987): Reproductive biology of stream-spawning roach, Rutilus rutilus. – Environmental Biology of Fishes 18(3): 219–227. Wang, N. & R. Eckmann (1994): Distribution of perch (Perca fluviatilis L.) during their first year of life in Lake Constance. – Hydrobiologia 277: 135–143. Wilcove, D.S., Rothstein, D., Dubow, J., Phillips, A. & E. Losos (1998): Quantifying threats to imperiled species in the United States. – BioScience 48(8): 607–615. Williamson, M. (1996): Biological Invasions. – London, Chapman & Hall.

Authors César Metzger1, Philippe Christe, Department of Ecology and Evolution, University of Lausanne, Biophore, 1015 Lausanne, Switzerland, e-mail: [email protected]; Sylvain Ursenbacher, Department of Environmental Sciences, Section of Conservation Biology, University of Basel, StJohanns-Vorstadt 10, 4056 Basel, Switzerland. 1 Present Address: Zoological Institute, University of Basel, Vesalgasse 1, 4051 Basel, Switzerland.

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Sexual Dimorphism in the Dice Snake (Natrix tessellata) from the Central Alps Konrad Mebert Abstract. In the process of a morphological study, scale characteristics and body proportions of dice snakes (Natrix tessellata) from the central Alps in Switzerland and northern Italy were investigated. Compared to males, female dice snakes exhibit lower ventral and subcaudal counts, a more posterior reduction of dorsal scale-rows on the trunk, but a less posterior one on the tail, a greater relative tail length, body width and posterior head length, but a narrower head. The sexual dimorphic characters are partitioned into three groups, relating to embryogenesis, copulating behavior, and foraging, that possibly promoted their evolution. Key words. Dice snake, morphology, gender differences, driving forces, embryogenesis, copulating behavior, foraging

Introduction The dice snake (Natrix tessellata), as most related natricine snakes, is a sexually highly dimorphic snake species (Mebert 1993, 1996, 2010). Based on a study about the microgeographic variation of dice snakes in the Central Alps, comparing introduced and indigenous populations, individuals were also investigated for sex dependent character expression. Sexualdimorphism results from gender based differences in various aspects of natural history and annual activities. The males of N. tessellata like in most temperate snakes, court and mate after emergence from hibernation. But except for some feeding and shedding, they often behave more secretive than females throughout the remainder of their seasonal activity, possibly to avoid predation. In contrast, females require an increased food input after a successful mating to provide sufficient energy to develop embryos. Their behavior is accordingly adapted to optimize embryogenesis, including foraging, thermoregulation, and searching a site for oviposition. These gender associated differences in behavior and tasks has promoted the evolution of sexualdimorphic characters. This study reports on the variation and extent of sexualdimorphic characters of pholidosis and body proportions in N. tessellata from the Central Alps.

(Mebert 1993, 2011a). Almost 200 preserved dice snakes from the Natural History Museum of Geneva were additionally measured to investigate the consistency of sexualdimorphic expression over a wider geographic area, including a study on geographic variation per se (Mebert 2011b). Gender of each snake was determined by assessing the sexualdimorphic thickness of the tail base. In females, the tail base visually tapers within the first 10 subcaudal scales. In males, the circumference remains equal for approx. the first 10 subcaudal scales. In cases of doubts, a sonde was inserted to investigate the extent of the genital-pockets, which are < 10 subcaudals in females and > 10 subcaudals in males. More than 50 morphological characters were recorded, including pholidotic, color pattern, and body proportions, such as several cephalic lengths, as well as trunk and tail proportions. The definitions of characters and methods of measuring is explained in detail in Mebert (1993), but is briefly indicated in the text, where it was deemed helpful to prevent misunderstanding. An ANOVA was processed with SAS procedures to reveal characters exhibiting significant differences between the sexes (see Mebert 1993 and 2011a for more statistical details regarding tests of normal and non-normal characters, and ratios applied to prevent bias by different size classes).

Material and Methods

Results and Discussion

A total of 433 dice snakes were sampled in 1990 and 1991 from five populations, three from north of the Swiss Alps, the lakes Alpnach, Brienz, and Geneva, and two from south of the Alps, the lakes Lugano (Canton Ticino, southern Switzerland) and Garda (Italy). At each lake, the sample consisted of at least 40 adult (total length > 40 cm) males and 40 adult females. The snakes were transferred to the laboratory, measured and subsequently returned and released at their sampling site

Significant differences exist between the sexes. Consult Mebert (1993 and 2011a) for a more detailed listing of the geographic values of sexual dimorphic variation, as only the most prominent differences are briefly presented here. An often used character to show sexual dimorphism in snakes is the number of ventral scales (Mebert 1993). Females from the Central Alps exhibit on average 5 ventral scales less than males, a difference that is consist-

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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ent throughout mid-latitudes of Eastern Europe (e.g. Fuhn & Vancea 1961, Shcherbak & Shcherban 1980, Kminiak & Kaluz 1983) and as far as Northeast Turkey (Tab. 1). For all other characters, the morphological analysis permits to partition the results into three distinct groups, based on putative driving forces that promoted the formation of sexual dimorphic characters within the dice snake. Some sexual dimorphic values listed below are larger in females (>), others in males ( males females > males females > males

Group 2 number of subcaudals males > females subcaudal position of the dorsal scale-rows reduction males > females on the tail males > females relative tail length Group 3 posterior head length head width

males < females males > females

Group 1 summarizes characters, which provide the females more body volume compared to males, probably to optimize their reproductive output, such as a high number or large size of eggs. A larger body volume could be achieved by increasing the number of ventral segments, since each vertebra is linked to a ventral scale (Kramer 1961). This is the case for the related North

Fig. 1. Sexual dimorphism of ventrals and subcaudals in Natrix tessellata. Only dice snakes from northern Italy and Switzerland are included. 0 Females, ● Males.

Tab. 1. Geographic variation and sexualdimorphic expression of the number of ventral scales (means) in Natrix tessellata. PoPl: Po Plain, northern Italy and adjacent southern Switzerland, WeBa: Western Balkan, Gree: Greece, TuBS: Turkish Black Sea coast, NeTu: Northeastern Turkey (Region between the town Kars and Lake Van).

PoPl WeBa Gree TuBS NeTu

Mean number of ventral scales Females n Males n 165.6 123 170.2 105 165.8 10 172.0 32 170.4 31 173.9 38 171.2 6 175.7 4 174.0 22 178.4 28

American natricines of the genus Nerodia (e.g. Mebert 2010). Interestingly, female dice snakes have not evolved higher ventral counts, but instead show significantly fewer ventrals than males (Tab. 1, Fig. 1). A closer look at the comprehensive morphological studies by Thorpe (1973, 1979) about the grass snake (Natrix natrix), and by Schätti (1999) about the viperine snake (N. maura), shows that the males of these congeners similarly evolved larger ventral counts than females (see below). Hence, I presume that some phylogenetic constraints among the Natrix species prevented the evolution of a larger number of ventrals and trunk segments in females. But the average difference of 1 ventral scale between the sexes of N. maura is clearly smaller than in the dice and the grass snakes, whose females’ produce on average 4–5 ventrals less than males. However, females reach substantially larger total and trunk (SVL) lengths (Fig. 2) and a wider body (and weight consequently, Mebert 1993), which might serve as a compensation for the lower number of ventrals. The amount of longer body growth varies among the population of the Central Alps from 9 cm at Lake Alpnach to 25 cm at Lake Geneva (n = at least 40 adult snakes for each sex and population, Fig. 2), possibly due to different ecological conditions. Females also reduce their dorsal scale-rows on the trunk from bilaterally 19 to 17 rows (Fig. 3), and additionally down to 15 rows farther caudal (posterior), i.e. nearer to the vent (Figs. 3 and 4). With the resulting increase of scales in the posterior section of the trunk, females gain additional body volume and perhaps a more elastic body surface to develop and store embryos. In a wider geographic context, the sexually dimorph scale-rows reductions remain, but the difference increases to approximately 4% in relation to an average ventral count. Table 2 shows the ventral position of scale-rows reduction in absolute and relative values for the average bilateral reduction from 19 scale-rows down to 17, which is exemplary for the other reductions down to 19, and 15, dorsal scale-rows, respectively. Group 2 refers to sexually dimorphic characters rendering the males more volume at the tail base, en-

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Fig. 2. Gender and population differences in total body length based on ≤ 40 adult dice snake with complete tails per sex and per population: LaAl (Lake Alpnach), LaBr (Lake Brienz), LaGe (Lake Geneva), LaLu (Lake Lugano), LaGa (Lake Garda).

Fig. 3. Pattern of a dorsal scale-row reduction. The reduction occurs bilaterally, whereby two longitudinal scale rows are reduced to one row (see scales with horizontal black dots). The position of the reduction is related to the ith number of ventral scale. The ventral position is derived by following in a zig-zag way (see black dots) from the first scale of the reduced row down to the ventral scale Nr. 104, which represents the ith number of ventral scale for this reduction.

abling the storage of their hemipenes. On average, male dice snake exhibit 10 more subcaudals, which approximates the length of the hemipenes stored in the tail base (Fig. 1). Table 3 shows a similar gender difference across a much wider geographic range as far as Northeast Turkey. In concert with the sex character, the males evolved a 4–5% longer tail (Fig. 5), and reduce scale-rows on the tail more posterior, unlike the more posterior reduction on the trunk in females (Fig. 4). The geographic variation of caudal scale-rows reductions is accompanied by a constant gender differences in its relative position (Tab. 4). The table shows the mean subcaudal position of the bilateral reductions from 8 to 6 scale-rows, exemplary for the various other scale-rows reductions on the tail. Alternatively to the space gaining hypothesis, the longer tail in males might enhance the copulatory effectiveness, whilst the tails of males can be better wrapped around females during copulation (Semlitsch & Gibbons 1982). Group 3 consists of two head lengths. The relative posterior head length (= distance between the eye and

Tab. 2. Geographic variation and gender difference of the ventral scale position (means) of the reduction from 19 to 17 dorsal scale-rows. reR17Do (%): relative position [(R17Do/ventrals)*100], R17Do: absolute value of the reduction position to an ith ventral scale; PoPl: Po Plain, northern Italy and adjacent southern Switzerland, WeBa: Western Balkan, Gree: Greece, NeTu: Northeastern Turkey (Region between the town Kars and Lake Van). See Mebert (2011a) for a more detailed description of reduction pattern.

PoPl WeBa Gree NeTu

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Females 55.1 62.8 65.5 62.2

Mean ventral position of dorsal scale-rows reduction from 19 to 17 rows reR17Do (%) R17Do (absolute) n Males n Females ales 121 52.4 104 91.3 89.1 7 58.4 22 105.0 100.7 19 61.4 26 110.7 106.1 13 58.2 14 107.7 105.9

Konrad Mebert

Tab. 3. Geographic variation and gender difference of the number of subcaudal scales (means); PoPl: Po Plain, northern Italy and adjacent southern Switzerland, WeBa: Western Balkan, Gree: Greece, TuBS: Turkish Black Sea coast, NeTu: Northeastern Turkey (Region between the town Kars and Lake Van).

PoPl WeBa Gree TuBS NeTu

Females 61.8 63.7 67.2 59.5 60.9

Mean number of subcaudals n Males 97 71.7 9 74.4 27 72.4 4 70.0 21 70.0

n 89 27 37 4 25

the terminal end of the last supralabial scale / total head length) is significantly longer in females than in males, who, on the other hand, exhibit a comparatively wider head (Fig. 6).

The distinctive head dimensions between the sexes of the dice snake might indicate different food niches concerning the prey size (Shine 1986). For example, the longer head reflects also a longer jaw, which allows females to generally feed on larger fish prey and to use the increased energy for reproduction. The broader head in males may indicate their proportionally higher consumption rate of bulky frogs, which show their seasonal peak in early spring, when the water is still relatively cool for fishing activities. Wider heads have been correlated with frog-feeding in dice snakes (Brecko et al. 2011), albeit their analysis focused on a wide geographic scale and neither investigated intrapopulational nor intergender variation in detail. The sexual dimorphism in the dice snake shown above is paralleled by similarly directed sex differences in the two other congeners, the grass snake (N. natrix) and viperine snake (N. maura). For example in the grass snake, in addition to the males’ higher ventral counts, the numbers of subcaudals, positions of caudal scale-

Fig. 4. Gender differences in the positions of dorsal and caudal scale-rows reductions. The relative ventral/subcaudal positions (% to the number of ventrals and subcaudals) of the reductions down to 19, 17 and 15 dorsal scale-rows, as well as down to 8, 6 and 4 caudal scale-rows, is shown. The inferior, the middle and the superior horizontal barrier of the boxes represent the values after 25, 50 and 75% of the data set (medians). Only dice snakes from Northern Italy or Switzerland are included.

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Tab. 4: Geographic variation of the subcaudal scale position (means) of the reductions from 8 to 6 caudal scale-rows. R6Cau: absolute mean values of the reduction position to a subcaudal scale; reR6Cau (%): relative position [(R6Cau/subcaudals)*100]; PoPl: Po Plain, northern Italy and adjacent southern Switzerland, WeBa: Western Balkan, Gree: Greece, NeTu: Northeastern Turkey (Region between the town Kars and Lake Van).

PoPl WeBa Gree NeTu

Females 14.2 16.0 18.1 18.7

R6Cau (absolute) n Males 121 23.1 6 26.0 18 24.1 13 27.1

n 104 22 27 14

Females 22.6 23.8 27.9 30.2

reR6Cau (%) n Males 97 32.0 4 35.3 16 34.7 9 38.2

n 89 13 24 13

rows reductions, relative tail length, body width and head length are similarly different between the sexes as in the dice snake (Thorpe 1973, 1979, Mebert 1993). Also in the viperine snakes, the number of ventrals and subcaudals, total body length and relative tail length are similarly sexually dimorph (Schätti 1982). Although no investigation on ecological causes for sexual dimorphism in the dice or any other Natrix species has been conducted, conclusions can be drawn from related studies (see also comprehensive survey and review by Shine 1989). For example, Shine (1978) postulated two reasons, why within most snake species the females reach a larger body length than males: (1) Natural selection favors large body mass in females, because fecundity is directly proportional with the body size, and (2) smaller bodies in males are selectively favored in order to be more mobile and thus being able to find more females during the mating season. Similarly, Fitch (1981) mentioned that in those reptiles having experienced a selection towards large clutches and relatively large newborns, a correlated selection for large

females took place, reflected by the evolution of a corresponding sexual dimorphism. Semlitsch & Gibbons (1982) showed a similar sexual dimorphism relative to body and tail lengths in two semi-aquatic Nerodia water snake species. They attributed this to natural selection, in which larger females are favored for reproductive reasons and a corresponding selective pressure is lacking in males. Further studies on several semi- to fully aquatic snake species (Shine 1986) and similar trends in many other snakes (Shine 1991) support these conclusions. Differences associated with climate may intertwine with the selective pressures leading to sexual dimorphism, and may produce additional interspecific differences in the number of ventrals and scale-rows reductions, as were found in Nerodia sipedon and Nerodia fasciata (Mebert 2010). Fitch (1981) demonstrated that squamate reptiles of moderate climates produce larger females, and associated this with their temporally limited reproduction phase in comparison to tropical species. Hence, temperate reptiles experience a higher selective pressure to enlarge the body mass in order to

Fig. 5. Sexual dimorphism of trunk and tail length. Only dice snakes coming from Northern Italy or Switzerland are included. 0 Females, ● Males.

Fig. 6. Sexual dimorphism in head length (posterior) and head width. Only dice snakes from northern Italy and Switzerland are included. 0 Females, ● Males.

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develop as many offspring as possible in a very short season. A study comparing semi-aquatic Nerodia sipedon and Nerodia fasciata of temperate/subtropical and moutainous/lowland populations corroborates the climatic correlation of such variations (Mebert 2010). He found a corresponding increase in ventral number and posterior scale-rows reduction in representatives from cooler areas. Fitch (1981) stated that the generally larger females of the natricine Thamnophis sirtalis also feed on larger prey. This enables females to benefit on a wider food spectrum compared to males and sub-adults, which in turn reduces the intraspecific competition. Such a sexdependent food niche was also found in Nerodia rhombifera and Nerodia cyclopion, whereby the larger females also feed on larger prey than males do (Mushinsky et al. 1982). Similar selection pressure may have produced females of the aquatic file snake (Acrochordus arafurae) to evolve a significantly heavier body in relation to body length compared to males (Shine 1986). Shine observed that the sexes of this Australian water snake use separate habitat niches during the rainy season and that females feed on larger fish than males with the same body length (Shine 1991). In summary, the study shows that there is a multitude of sexually dimorphic characters in Natrix tessellata as is known from other natricines. The sexual dimorphism likely reflects various gender-based differences in behavior and associated tasks in their annual activity cycles.

References Brecko, J., Vervust, B., Herrel, A. & R. Van Damme (2011): Head morphology and diet in the dice snake (Natrix tessellata). – Mertensiella 18: 20–29. Fitch, H.S. (1981): Sexual size differences in reptiles. – University of Kansas Museum of Natural History Miscellaneous Publications 70: 1–72. Fuhn, I.E. & S. Vancea (1961): Fauna Republici Romine. - Fauna Romine 14(2) Bucurest. Kminiak, M. & S. Kaluz (1983): Evaluation of sexual dimorphism in snakes (Ophidia, Squamata) based on external morphological characters. – Folia Zoologica 32(2): 259–270. Kramer, E. (1961): Variation, Sexualdimorphismus, Wachstum und Taxonomie von Vipera ursinii (Bonaparte, 1835) und Vi-

peria kaznakovi (Nikol’skij, 1909). – Revue Suisse de Zoologie 68(41): 627–725. Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Mebert, K. (1996): Comparaison morphologique entre des populations introduites et indigenes de Natrix tessellata de I’Arc Alpin. – Bull. Soc. Herp. France 80: 15–25. Mebert, K. (2010): Massive Hybridization and Species Concepts, Insights from Watersnakes. – VDM Verlag, Saarbrücken, Germany. Mebert, K. (2011a): Introduced and indigenous populations of the dice snake (Natrix tessellata) in the Central Alps – Microgeographic variation and effect of inbreeding. – Mertensiella 18: 71–79. Mebert, K. (2011b): Geographic variation of morphological characters in the dice snake Natrix tessellata (Laurenti 1768). – Mertensiella 18: 11–19. Mushinsky, H.R., Hebrard, J.J. & D.S. Vodopich (1982): Ontogeny of water snake foraging ecology. – Ecology 63(6): 1624– 1629. Shcherbak, N.N. & M.I. Shcherban (1980): Amphibians and Reptiles of the Ukrainian Carpathians. – Naukova Dumka, Kiev (in Russian). Schätti, B. (1982): Bemerkungen zur Ökologie, Verbreitung und intraspezifische Variation der Vipernatter, Natrix maura (Linné 1758). – Revue Suisse de Zoologie 89(2): 521–542. Semlitsch, R.D. & J.W. Gibbons (1982): Body size dimorphism and sexual selection in two species of water snakes. – Copeia 4: 974–976. Shine, R. (1978): Sexual size dimorphism and male combat in snakes. – Oecologia 33: 269–277. Shine (1986): Sexual differences in morphology and niche utilization in an aquatic snake, Acrochordus arafurae. – Oecologia 69: 260–267. Shine (1989): Ecological causes for the evolution of sexual dimorphism: A review of the evidence. – The Quarterly Review of Biology 64(4): 419–461. Shine (1991): Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. – The American Naturalist 138(1): 103–122. Thorpe, R.S. (1973): Intraspecific Variation of the Ringed Snake Natrix natrix (L.). – Ph.D. dissertation, C.N.A.A. Thorpe, R.S. (1979): Multivariate analysis of the population systematics of the ringed snake, Natrix natrix (L). – Proceedings of the Royal Society of Edingburgh 78B: 1–62.

Author Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland, e-mail: [email protected].

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ISBN 978-3-9812565-4-3

Different Habitat Use of Dice Snakes, Natrix tessellata, among Three Populations in Canton Ticino, Switzerland – a Radiotelemetry Study Alberto E. Conelli, Marco Nembrini & Konrad Mebert Abstract. Nine adult female dice snakes, Natrix tessellata, from three different sites were tracked during an entire season using radiotelemetry. The study sites represent the variation of habitats occupied by dice snakes in the canton Ticino (southern Switzerland); a relatively intact and protected river delta (Bolle di Magadino), a semi-natural stream (Arbedo) and a lake ecosystem with strong human influence (Riva San Vitale). The radio-tracked dice snakes were found only in the immediate surroundings of the open water surface with 97% of the locations occurring at less than 20 m distance from the water. The most frequent structures selected by the monitored animals for sheltering, thermoregulation and oviposition were artificial rocky embankments (rip-raps) and other similar retaining works (i.e. stone walls) covered with light vegetation and well exposed to the sun. The snakes avoided forest habitat with dense monotonous vegetation or artificial stream reaches with concrete banks and a low ecomorphological value (lack of microstructure). The rather long monitoring period at the Bolle di Magadino site allowed us to identify relevant seasonal changes in their habitat use. During the fall, the snakes moved from the summer habitat towards the hibernation sites at the edge of the flood plain. In spring, they used the same migration route to return to their summer habitat. Key words. Natrix tessellata, Bolle di Magadino, Arbedo, Riva San Vitale, natural and anthropogenic habitat, seasonal migration

Introduction The dice snake (Colubridae: Natrix tessellata, Laurenti 1768) is a semiaquatic species that inhabits most watercourses that are rich in fish and provide shores with a variable, mostly rocky structure. Its natural distribution in Switzerland is limited to areas south of the alpine mountain range, predominantly in Canton (= province) Ticino and in the two southern valleys, Misox and Poschiavo, in the Canton Grison. Introduced populations north of the Alps have persisted at the lakes of Geneva, Brienz, Alpnach, and Zürich (Mebert 1993, Hofer et al. 2001, Mebert et al. 2011). Natrix tessellata is considered as one of the most threatened reptiles in Switzerland (Hofer et al. 2001) It is classified in category EN (endangered) according to criteria of the IUCN for the Red List of threatened reptiles in Switzerland (Monney & Meyer 2005). Its habitats are in progressive decline due to disadvantageous alterations of watercourses, such as obstructions, cemented and sealed walls along shores, dredgings, reclamations of land near the watercourse, corrections of the river bed, and modifications of the water regimen (Hofer et al. 2001, Fossati & Maddalena 2003). The permanent Committee of the European Council, in charge of the implementation of the Berne Convention, has formally demanded the protection of the dice snake populations in the canton Ticino, in particular those of the Sopraceneri (northern Ticino), based on the recommendation n° 26 of 1991. The strategy of the Canton Ticino for the study and conservation of its amphibians and reptiles has targeted the protection of the dice

Fig. 1. Three study sites with distinct ecosystems for Natrix tessellata in Canton Ticino, southern Switzerland.

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Fig. 2. Mixture of lentic and lotic systems: Nature Reserve Bolle di Magadino, a protected alluvial area: (above) Aerial view of the delta region, (middle) in the middle of the image a dyke made of block stones – the summer habitat for many dice snakes, (below) and quiet backwaters, typcial for this alluvial zone.

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Radiotracked Dice Snakes in Switzerland

Tab. 1. Basic data of radio-tracked female dice snakes N. tessellata for each site in Canton Ticino, Switzerland. †: early termination of radio-tracking due to death or other reasons (see text).

ID B1 B2 B3 B4 A1 A2 A3 R1 R2 Total Mean

Site

Bolle di Magadino Bolle di Magadino Bolle di Magadino Bolle di Magadino Arbedo Arbedo Arbedo Riva S.Vitale Riva S.Vitale -

Weight at capture [g]

Date of release [all 2004]

First localization [all 2004]

Last localization [all 2005]

22 Aug

240

05 Sep

09 Sep

23 Aug †

226

20

500

26 Aug

151

05 Sep

09 Sep

17 Sep

359

44

940

20 Aug

170

05 Sep

09 Sep

13 May †

246

19

570

23 Aug

160

05 Sep

09 Sep

25 Sep

381

47

1110

16 Aug 24 Aug 01 Sep

360 194 157

05 Sep 05 Sep 05 Sep

17 Sep 17 Sep 17 Sep

13 Mar † 20 Sep 07 Sep

177 368 371

17 32 47

240 270 830

19 Aug

157

05 Sep

14 Sep

09 Apr †

207

16

100

19 Aug

153

05 Sep

09 Sep

21 Apr †

224

17

40

-

199

-

-

-

381 283

259 29

511

Fig. 3. Lotic system: Traversagna stream at Arbedo, a seminatural torrential stream typically used by N. tessellata in Ticino: (above) Aerial view, (below) upstream view.

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n of Monitoring radio Duration localiza[days] tions

Date of capture [all 2004]

Shore habitat [m]

snake as one of its priorities, encouraging the scientific research of this species (Fossati & Maddalena 2003). The objective of this study is to improve our knowledge of the ecology of N. tessellata by means of radiotelemetry, and finally to develop and refine the modes of conservation for the populations in Ticino (Conelli & Nembrini 2007). The collected data constitute a base for the elaboration of recommendations for the management of biotopes and water courses, and has supported

Alberto E. Conelli, Marco Nembrini & Konrad Mebert

Fig. 5. Radio-transmitter of 5.25 g.

Fig. 6. Implantation of radio-transmitters under anesthesia performed by Bernd Schildger, veterinarian of “Tierpark Dählhölzli”, Bern.

Fig. 7. Radiotelemetric localization in the field by the first author.

the preparation of a cantonal action plan (Conelli & Nembrini 2009) for the conservation of the populations of N. tessellata in Canton Ticino. Material and Methods Study Sites Fig. 4. Lentic system: Southeastern area of Lake Lugano/ Ceresio, a lake with strong anthropogenic influence; yellow arrow pointing to the area frequented by radio-tracked dice snakes: (above) Aerial view with the town Riva San Vitale at the southern end, (middle) view towards the southeastern end of the lake, (below) shore road with a house and trees below the road, which is used by local N. tessellata.

The study was conducted in three ecosystems considered representative habitats of this species in Canton Ticino (Fig. 1): (1) lentic/lotic system: Nature Reserve of the Bolle di Magadino, a protected alluvial delta with a dyke made of block stones and quiet backwaters (Fig. 2); (2) lotic system: Traversagna at Arbedo, a semi-natural torrential stream (Fig. 3); (3) lentic system: Riva San Vi-

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Radiotracked Dice Snakes in Switzerland

Fig. 8. Radio localizations of dice snakes in Ticino, southern Switzerland. Localization for each individual snake per site is represented by a different color: (above) Bolle di Magadino, (middle) Traversagna stream, (below) Lake Lugano near Riva San Vitale.

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Fig. 9. Predominant use of little to heavily compromised, anthropogenic structures (ecomorphology categories II-green and III-yellow) by N. tessellata along the Traversagna stream, Ticino, southern Switzerland.

Fig. 11. Anthropogenic structures preferably used by dice snakes along the shore road in Riva San Vitale, southern Switzerland.

Fig. 10. Anthropogenic structures preferably used by dice snakes along the Traversagna stream: (above) in 2001 constructed rip-rap, (below) old stone wall.

Fig. 12. Anthropogenic structures such as this dam called “Diga della Pepa” made of block stones preferably used by dice snakes in the Bolle di Magadino.

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Radiotracked Dice Snakes in Switzerland

Fig. 13. Sealed north-faced wall along the Traversagna stream that was never utilized by the radio-tracked dice snakes.

tale, Lake Lugano/Ceresio, a lake with strong anthropogenic influence (Fig. 4). Animals Nine female N. tessellata with body masses ≥ 150 g were caught within these three study sites during the month of August 2004 with the permission of the public authority,: four individuals from the Bolle di Magadino, three from Arbedo, and two individuals from Riva San Vitale (Tab. 1). Surgical implantation and field methods principally followed known techniques (e.g. Parker & Brown 1972, Reinert & Cundall 1982, Reinert & Kodrich 1982, Reinert 1992, Aebischer et al.1993). After sterilization with ethylene oxide, the radio-transmitter of 5.25 g weight (model SB-2T, Holohil Systems Ltd. Carp, Ontario, Fig. 5), corresponding to 2.1–4.7% (avg. 3.1%) of the snake’s mass, were surgically inserted under anesthesia posterior the peritoneal cavity (performed by Bernd Schildger, veterinarian Tierpark Dählhölzli, Bern, Fig. 6). This technique was preferred over the use of external transmitters (Ciofi & Chelazzi 1991) due to the long duration of the study and the terrestrial activity of these snakes, rendering an internal transmitter less obstructive for movements in its habitat and frequent contact with the substrate (Weatherhead & Anderka 1984, Újvari & Korsos 2000, Dusej 2003, Wisler 2006). The life of the battery enabled radiotelemetric localizations of the dice snakes for the duration of one year. Fig. 14 (right). Radio-tracked dice snakes selected hibernation sites (yellow arrows) within anthropogenic structures in the immediate vicinity of water: from top down (first) within a road supporting wall in the Bolle di Magadino, (second) inbetween block stones at the Traversagna stream (third) in a wall under a waste container place at the Traversagna stream (fourth) in the road supporting wall and within the concrete roof of a lakeshore house near Riva San Vitale.

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Fig. 15. Body (snakes) and ambient (outside the hibernacula) temperatures during hibernation in N. tessellata of Ticino, Switzerland.

After surgery the snakes were monitored in a terrarium for approximately 48 hours and then released at the exact location of their capture. The entire operation was

subject to an authorization procedure of the Federal Decree for the Protection of Animals (OPAn).

Fig. 16. Summer (yellow circle) and winter (white oval) habitats for N. tessellata in the Bolle di Magadino, Ticino, southern Switzerland. Red oval denotes a post-hibernation residence for dice snakes (see Fig. 17) that was used for several weeks until their migration (blue oval) to the summer habitat.

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Radiotracked Dice Snakes in Switzerland

Tab. 2. Comparative use of anthropogenic and natural sites of radio-tracked dice snakes in Ticino, southern Switzerland. Number of localizations (%) Structures

Magadino

Arbedo

Riva S. Vitale

Anthropogenic habitats Rip-rap (bank made of block stones) Road support made of block stones Stone retaining wall Garden Building

89 49 28 12 -

(68%) (38%) (22%) (9%)

58 52 6 -

(60%) (54%)

Natural habitats Reed grass Reed ecotone / wet meadow Wet meadow Natural shore with structural elements (shrubs, blocks, lumber)

41 22 17 1

(32%) (17%) (13%) (1%)

38 -

(40%)

2 -

1

(1%)

38

(40%)

Total

130

(100%)

96

(100%)

Data Acquisition Weekly radiotelemetric localizations were conducted during daylight hours (09:00–18:00), using two portable receivers (TR-4, Ltd Telonics., USA) fitted with handheld antennas for long and short-haul (14K-RA and RA1A, Ltd. Telonics., USA, Fig. 7). No nocturnal activity (19:00–01:30) as in Scali et al. (2001) was studied. The method of “homing in” was applied to locate the snakes (White & Garrot 1990), and, if feasible, followed by a visual confirmation, while avoiding disturbance as much as possible. Following parameters were recorded at each location: (1) the date and time, (2) weather data (temperature at 1 m above the ground, wind estimated with the Beaufort Scale, cloud cover), (3) GPS coordinates, (4) body temperature by remote sensing, (5) habitat structure in the immediate vicinity, (6) behavior of

(6%)

31 11 10 10

(94%)

Total 178 101 28 29 10 10

(69%) (39%) (11%) (11%) (4%) (4%)

(6%)

81 22 17 1

(31%) (8%) (7%) ( 0.05). The backward elimination method excluded from the analysis all third-order effects (i.e. interactions among the three variables included in the analysis), but it selected four significant second-order effects (i.e. interactions between pairs of variables), listed in Table 4. Two of them included species as a key variable, one linked to the habitat, the other to the daytime, highlighting the differ-

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Stefano Scali

Tab. 2. Results of GLM for the comparison between species of ambient and body temperatures, controlled for capture year and month. Significant values are in bold. Factor Species * Year

Species * Month

Year * Month

Species

Year

Month

Dependent Variable Tb Ta Ts Tw Tb Ta Ts Tw Tb Ta Ts Tw Tb Ta Ts Tw Tb Ta Ts Tw Tb Ta Ts Tw

df

F

P

2 2 2 2 2 2 2 2 7 7 7 7 1 1 1 1 3 3 3 3 6 6 6 6

0.280 0.238 5.173 0.336 0.981 1.036 0.603 0.096 1.963 3.675 0.297 3.789 0.302 0.038 4.168 0.496 9.955 9.389 4.918 7.422 10.205 9.138 2.812 10.353

0.757 0.789 0.008 0.716 0.380 0.361 0.550 0.909 0.074 0.002 0.953 0.002 0.584 0.845 0.045 0.484 0.000 0.000 0.004 0.000 0.000 0.000 0.017 0.000

ences in habitat use and in daily activity between Natrix maura and N. tessellata. On the contrary, habitat use was not influenced by season but depended on daytime for both species. The differences in daily activity were particularly significant and showed a peak in the afternoon for N. tessellata, whereas N. maura seemed to be more active during the night and in the morning (Fig. 7). This result was confirmed by frequencies of individuals captured by month, underlining that nocturnal activity of both species occurred only in the warmest months (Fig. 7). The result was not influenced by the sampling year, because no difference was observed in number of individuals for habitat for both species (N. maura: c² = 11.798, df = 8, p > 0.05; N. tessellata: c² = 9.710, df = 6, p > 0.05). Both species were often found on the shores and in the deep water, but some habitats were used in different ways by the two snake taxa. In particular, N. maura was often captured under stones in the water or in the pools on the gravel shore, whereas N. tessellata used more frequently land sites than N. maura (Fig. 8). Only a few observational data about feeding habits were collected in this study. At Site B, both Natrix species preyed on two fish species, Leuciscus souffia and

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Tab. 3. Frequencies of individuals of Natrix maura and N. tessellata in relation to season, daily activity and microhabitat at site B (Val Trebbia); habitat codes for capture sites: land (on land); stone (in shallow water under stones); shore (swimming in shallow water 30 cm). Season Daytime

Habitat

Spring Summer Morning Afternoon Night Land Stone Shore Pool Water (lotic)

N. maura 22 36 17 16 25 4 9 29 7 9

N. tessellata 23 26 12 24 13 10 2 27 0 10

Thymallus thymallus. However, N. maura had a wider prey spectrum by feeding also on Padogobius martensii and larvae of two amphibian species, Triturus carnifex and Bufo bufo. Some N. tessellata were observed eating small prey in the water immediately after the capture, whereas larger fish were brought on the shores before ingesting them. The low number of prey collected does not allow statistical analyses of data. Discussion Natrix maura and N. tessellata showed many ecological similarities, by sharing the same general habitats including streams and rivers with gravel shores and plenty of fish that both species consume. The similar ecological preferences have usually no effect on populations of either species, since their natural distribution is parapatric with the exception of limited area in northern Italy. There, the coexistence of the two similar Natrix species potentially leads to a strong competition for habitat and/or food (Metzger et al. 2009). It can be assumed that some mechanisms of resource partitioning existed or have evolved in this case of syntopy in northern Italy. Preliminary ecological data do show such ecological partitioning, which is discussed below. The two snakes exhibited similar thermal ecologies, in fact some differences were recorded only for substratum temperatures, but they were due to different ambient temperatures among sampling years. N. maura and N. tessellata preferred the same body temperatures even among different sites and they maintained similar temperature values throughout the year, since no difference was detected among activity months among all sites. Water temperature played a major role in determining body temperature of both snake taxa in this study, being strongly correlated with it for individuals captured in water. The correlation between body and wa-

Ecological comparison of Natrix tessellata and N. maura

Tab. 4. Results of loglinear analysis for comparison of habitat use, daily and seasonal activity between Natrix maura and N. tessellata at Site B (Val Trebbia). Variables Daytime*Habitat Species*Habitat Species*Daytime Season*Daytime

df 8 4 2 2

L² Chi-square change 17.687 19.299 8.329 25.870

ter temperatures was also demonstrated for N. maura by authors who studied thermoregulatory behavior of this species (Hailey & Davies 1987, Patterson & Davies 1982, Jaén-Peña & Pérez-Mellado 1989). On the contrary, the two species showed a different thermal behavior in relation to other ambient temperatures: N. maura’s body temperature is also correlated to air temperature, whereas N. tessellata seemed to depend more on substratum temperature. Litvinov et al. (2011) found also a dependence of body temperatures on environmental temperatures of dice snakes from Russia, including air and substratum temperatures. However, these authors processed no correlational analysis.

P 0.0001

4.32

0.0377

0.51

0.4762

August, when gender differences were equal for all years of sufficiently collected data (Fig. 2 and Tab. 3). Later in October (intervals 12 and 13) the frequency of males dropped to a stable ratio of 0.4 (Fig. 2), i.e., significantly more females were visible towards the end of the active season (Tab. 3). Discussion Seasonal variation in movement patterns is common in many species of snakes (e.g. Madsen 1984, Gregory et al. 1987, Shine et al. 2001a, Brito 2003). This study provides comprehensive data of seasonal differences of the activity pattern in a population of Natrix tessellata from Histria. This population shows a bimodal spring/autumn peak of activity, with the majority of snakes being observed in spring when all snakes exit hibernation and most matings occur, as well as in autumn with their return to the hibernation sites. The low frequency of captures of both sexes during the summers may not only be an effect of the absence of snakes in the immediate proximity to the hibernation site, but possibly also due to low activity and even subterranean aestivation (see e.g. Brown & Weatherhead (2000). There are established activity differences between males and females in the literature. For N. tessellata and many other species of snakes in the temperate zone, males are often observed to exit hibernation prior to females (Seigel & Ford 1987), and remain near the hibernation site in order to reproduce with females as they emerge (Phelps 1978, Garstka et al. 1982). As in some other natricine taxa , e.g. Thamnophis sirtalis (Aleksiuk & Gregory 1974) and N. maura (Santos & Llorente 2001), the maturation of the spermatozoa and follicles in N. tessellata occur in the late summer or fall, prior to entering the hibernation, i.e., postnuptial spermat-

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ogenesis and vitellogenesis increases (Seigel & Ford 1987, Bendel 2001). In some other species of temperate snakes, e.g. Vipera berus (Viitanen 1967, Nilson 1980), males emerge in advance of females to bask and complete spermatogenesis prior to the mating season. At our study site matings were observed just after emergence from hibernation (e.g. 30 March 2006) and we suggest that here too, male N. tessellata generally emerge earlier from hibernation than females to maximize their reproductive success by increasing their chances to encounter reproductive females, which is consistent with our observations of a male predominance among captures in early spring (at least 72% during interval 1, Figs. 2 and 4.). The same pattern has previously been recorded for other temperate natricine species, such as N. natrix (Madsen 1984), and Shine et al. (2001b) observed 75% of Canadian T. sirtalis being males during early spring. A higher frequency of males than females after emergence from hibernation has been observed in N. tessellata elsewhere (Gruschwitz et al. 1999, Mebert 2001, 2007) with the exception of a population in Germany (Lenz & Gruschwitz 1993a). Females of N. tessellata differ in reproductive traits in comparison to males, in that females have a later reproductive age (Zimmermann & Fachbach 1996) and a large proportion might not mate every year (Luiselli & Zimmermann 1997). Consequently, females may opt to leave the hibernation site directly after emergence, if non-reproductive, or shortly after mating if reproductive (e.g. Shine et al. 2001a). We suggest that the rapid spring movements of females away from the hibernation site occur as a result of: (1) avoidance of courting males due to increased energy costs and interference with feeding and basking (Aldridge et al. 2005 and references therein), (2) the high predation risk where many snakes are aggregated (Gregory et al. 1987), and (3) movements in order to initiate foraging in the nearby lake. If so, males should be more likely to be encountered around the hibernation area than females, where they remain active and exposed. Indeed, almost half (2023 individuals) of all snakes in this study were caught during April (intervals 1 and 2), of which 66 % (1330) were males. Later in the mating season, from May until June, the proportion of males decreases (intervals 3–6). This is probably caused by male movements to summer foraging habitats in adjacent lakes, whereas gravid females remain in the vicinity of the ruins to thermoregulate and forage in the nearby lake during their vitellogenesis peak (Figs. 2, 4, 5). According to our data, end of June to early July is the period of ovipositing in this population. This is also the time when the males are least visible, with a consistent proportion of 0.2 for all study years (Fig. 2). Thermoregulatory activities and search for suitable ovipositing sites might increase the visibility of females and, hence, their detectability (Madsen 1987). In addition, large numbers of males may be absent, because they have moved to foraging habitats or simply remain

P       < 0.0001   0.0051   < 0.0001 X2       20.077   7.839   16.355 N     145 232 33 60 147 225

Onset of hibernation 12-13

N 4 22 31 45 20 42 9  25

X2   12.462   2.579   7.086   7.529

P   0.0004   0.1083   0.0052   0.0060

Autumn mating interval 10-11 N X2 P             143     121 1.833 0.1757 2*     3*     38 50 1.636 0.2008 General foraging interval 7-9

Vitellogenesis peak interval 4-6 N X2 P 9     68 45.208 < 0.0001 90     158 18.645 < 0.0001 15     15 0.000 1.000 3 11 4.571 0.0325   M F M F M F M F   2005   2006   2007   2008  

N 309 236 824 414 152 148 207 73

Spring mating interval 1-3 X2 P 9.78 0.0018     135.78 < 0.0001     0.053 0.8174     64.129 < 0.0001        

Tab. 3. Differences in numbers of males and females distributed across five annual activity phases and tested statistically. Bold P-values show significant gender differences in each year.

Gender-based Movement Differences in Dice Snakes

underground to aestivate, protected from surface predators, while conserving energy. As Brown & Weatherhead (2000) hypothesized in their study about the related Northern water snakes (Nerodia sipedon), males may pursue a survival strategy following spring mating and remain secretive during the later part of the season. However, additional studies on the natricine snakes T. sirtalis and N. sipedon show differences in habitat use between males and gravid females (Gregory 1974, Roth & Green 2006). Males and non-gravid females of N. sipedon inhabit areas closer to the foraging ground than do gravid females (Pattishall & Cundall 2009). The high densities of females of N. tessellata occurring near the hibernation area in Histria also during summer may not be generalized to other populations. For example, in an alluvial plain in Ticino, Switzerland, female N. tessellata move away from hibernation sites to a summer habitat, where they likely also oviposit, whereas other females from a nearby river habitat do stay along the river (Conelli et al. 2011). Differences in female movements in different populations are suggested to occur due to resource variations between habitats. The abundance of suitable ovipositing sites in Histria, i.e., several thousand meters of stone walls and piles of rock, may attract gravid females to stay in the vicinity instead of trying to find alternative places for ovipositing. Egg clutches are frequently encountered inside the stone walls during the archaeological excavations and occasionally during our herpetological field work (S. Kärvemo. pers obs.). Additional places for incubation of eggs could be in soil, sawdust, under roots, leaves, composts or other fermenting vegetation (Gruschwitz et al. 1999). This applies at least partially also to Histria, where ovipositing also in sandy soil has been observed one kilometre away from the ruins (M. Sloboda pers. obs.). After ovulation (July, Bendel 2001), all snakes in the population can be expected to simply forage for food or possibly aestivate, and thus, females may also leave the vicinity of the ruins post ovipositing. This might be the reason for the very low capture rate of snakes (n = 18 in 2006, Fig. 3) in interval 8, still skewed towards females. The total number of snakes caught did not increase until interval 10 (late August). At this time, encounters of males among the ruins started to become more frequent (M. Carlsson pers. obs.), and the proportion of males caught rose to a near equal sex ratio. We suggest that the generally increased number of snakes and the higher proportion of males is a sign of autumn mating activity (Seigel & Ford 1987), resulting in the intensified presence among the ruins. Autumn matings have been documented for a number of natricine species (e.g. Schwartz et al. 1989, Greene et al. 1999, Santos & Llorente 2001), including N. tessellata (see refs. in Gruschwitz et al. 1999). One autumn mating was observed in Histria, 20 September 2006 (I. Ghira, pers. obs.). Possibly, increased activity around the ruins is due to some individual snakes entering “hibernation” already in late summer, as has been observed

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Simon Kärvemo, Martin Carlsson, Marian Tudor, Michal Sloboda, Andrei D. Mihalca, Ioan Ghira, Lucia Bel & David Modrý

Fig. 3. Total number of Natrix tessellata caught during each interval and year. Missing bars indicate intervals without fieldwork. The periods on the x-axis are explained in Tab.1.

Fig. 4. The daily percentage of males (dots) and the total number of snakes caught (bars) during the periods of emergence from hibernation and mating, late March to late April in 2006 (the year of the most extensive field work).

elsewhere (Prestt 1971, Velenský et al. 2011). A presumed proximal cue for the initiation of autumn activity is suggested by Gibbons & Semlitsch (2001); “…movement to winter denning areas presumably occurs during the late summer or autumn in response to photoperiod regardless of environmental temperatures…” The sex ratio for all data combined is close to a 1:1 ratio (53% males and 47% females). The slightly higher

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proportion of males might result from the majority of snakes being captured in spring, when more males are encountered. We presume that the proportion of males would increase further if the field work had started earlier in the spring (see below). Gruschwitz (1986) determined a sex ratio of 71% females and 29% males in a German population of N. tessellata. This highly unbalanced sex ratio is difficult to explain, although differ-

Gender-based Movement Differences in Dice Snakes

Fig. 5. A dice snake in July 2006 with a syrman goby (Neogobidus syrman) form the lake Sinoe, Histria. Photo: Simon Kärvemo

ences in observed sex-ratios of snakes vary considerably between years (Parker & Plummer 1987). A later study of the same N. tessellata population showed a more balanced sex ratio (Lenz & Gruschwitz 1993b), supporting the conclusions of Parker & Plummer (1987). Variations in captures of males and females between different investigations are not surprising, given that sex ratios in snakes can differ depending on the season or in what habitat the collections are performed (Parker & Plummer 1987). However, we cannot exclude that the observed total sex ratio for all years combined in the Histria population (53% males to 47 % females) indeed corresponds to a factual skew in the sex-ratio. Nevertheless, until more information is available, we consider the observed annual fluctuations of the sex-ratio and the slight skew overall to be artefacts from fluctuating fieldwork success (Carlsson et al. 2011). The consistently larger proportion of females captured (0.6 females to 0.4 males, Fig. 2) in late September and early October for all years deserves some attention. During this period snakes are almost exclusively encountered in the immediate surroundings of the actual hibernation dens. As all snakes must hibernate, it is reasonable to assume a balanced sex ratio. The consist-

ent between-years difference in the sex ratio of captured snakes towards the end of the season may be a result of unequal capture probability at the hibernation site. It can be argued that females are more likely to be captured than males during this time of year. Females are generally larger in size and arguably easier to spot and catch for a field worker. If so, the proportion of males might have been underestimated to some extent throughout the study. This rationale, however, is in contrast to findings in a North American natricine species. It has been shown that females of the Northern watersnake, Nerodia sipedon, have a greater flight propensity (flight initiation distance) than males and juveniles when approached by a human (Cooper et al. 2008). This might suggests that adult males are easier to catch than females. Naturally, the results from the Northern water snake do not necessarily apply to Natrix tessellata, as it is a different species with a potentially different behavioural repertoire. But if sex does affect flight propensity, we should expect a reversed gender specific capture ratio to that observed here. The overall skew in observed sex ratio for all years combined, does allow for the possibility of males being easier to catch than females, especially given that big snakes are predominantly females. In contrast, the

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Simon Kärvemo, Martin Carlsson, Marian Tudor, Michal Sloboda, Andrei D. Mihalca, Ioan Ghira, Lucia Bel & David Modrý

consistently reversed and much more pronounced skew during autumn appears not as artefactual, but in need of some biological explanation. Several explanations for finding a larger proportion of females in autumn have been proposed: (1) females have finished their oviposition and are more active when not gravid (Gregory et al. 1987). (2) Females may initiate hibernation one or two weeks before males (Lenz & Gruschwitz 1993b). Consequently females could have a larger probability to get caught earlier in the autumn compared to males. This implies that a large proportion of late males may have been missed in our study. Finally, (3) females may linger at the hibernation site, and exploit opportunities to bask, as thermoregulation may be more important for the females’ next reproductive investment than the males’ spermatogenesis (Bona-Gallo & Licht 1983). In a study about the reproductive cycles in female N. tessellata, Bendel (2001) suggested that their annual reproductive investment continues in August with the follicular maturation. With any of the three explanations listed above being true, one arguably would expect to encounter more females than males in late autumn, especially in sunny weather. Because, field work was terminated before the end of October, we can not fully assess the second explanation, whether more males than females enter hibernation later in October or early November. However, field work was conducted until about two weeks after the last foraging snakes were observed and we consider it unlikely that we would have missed enough males to account for the skewed sex ratio in late autumn. Time constraints have precluded fieldwork until the very end of snake activity. Yet, data and observations from subsequent years suggest that although the sex ratio tends to become equalised in late October, less snakes are also encountered in late October –early November compared to early-mid October (M. Carlsson unpublished, M. Tudor pers. obs.). We believe our data fits a combination of explanations 1 and 3 above. Females may remain active longer and exploit basking opportunities to a higher extent than do males. Further, given lower metabolic requirements than females, males may be entering hibernation over a longer period, at a low but steady rate, starting already in August. This hypothesis rests on the premise that females experience a greater need than males to maximize their food intake in order to recover from the energy drain of pregnancy, prepare for reproduction the following year or simply to maximize growth. Thus, we expect that at the time when foraging activity in the water had ceased and hibernation could no longer be postponed, more females than males should be expected to enter into hibernation. In conclusion, our results show that Natrix tessellata has two seasonal peaks of activity around the hibernation area, one in spring and one in autumn. In addition, our study suggests that there is a gender difference in activity and movements of N. tessellata. In early spring, males leave the hibernation prior to females to maximize the mating success. They remain near the hibernation site for several weeks before moving to foraging

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habitats. The females, however, leave the area after mating, but remain in the vicinity for oviposition and thermoregulation. During summer foraging, males may disperse farther than pregnant females or aestivate, given their lower energy requirements. Towards the end of summer an increase of males encountered may be due to autumn mating activity and/or a male-biased early retreat into hibernation, leaving females to be the more frequently encountered gender in September and October. Acknowledgements Carl Trygger’s Foundation, the Swedish Institute, Helge Ax:son Johnson’s Foundation and the Foundation for Zoological Research have provided financial support for this project. We thank Konrad Mebert and an anonymous reviewer for valuable comments and suggestions, significantly improving the quality of this paper. Permission for conducting the field investigation has been given by the Danube Delta Biosphere Reserve Administration. Alexandru Suceveanu, director of the Archaeological Institute in Bucharest, and especially Constantin Chera, director of the Museum of National History and Archaeology in Constanţa, have given us permission to work inside the museum area and provided invaluable assistance. We would like to thank Vlad Haisiuc, Tudor Ghira, Adrian Gliga, Attila Keleman, Vlad Vancia, Paul Székely, Diana Butănescu, Béla Marosi, Paul Nemes and Vide Ohlin for field assistance. The project was formerly in collaboration with the Romanian Herpetological Society and is now a collaboration between Ovidius University of Constanţa and Uppsala University, Sweden. References Aldridge, R.D., Bufalino A.P. & A. Reeves (2005): Pheromone communication in the watersnake, Nerodia sipedon: A mechanistic difference between semi-aquatic and terrestrial species. – American Midland Naturalist 154: 140-150. Aleksiuk, M. & P. Gregory (1974): Regulation of seasonal mating behavior in Thamnophis sirtalis parietalis. – Copeia: 681– 689. Bendel, P.(2001: Zur Physiologie der Würfelnatter Natrix tessellata Laurenti 1786 am Alpnachersee. – In: NAGON (Ed.): Amphibien und Reptilien in Unterwalden. – NAGON, Grafenort, Switzerland 2: 162-175. Best, P.B. & D.M. Schell (1996): Stable isotopes in southern right whale (Eubalaena australis): Baleen as indicators of seasonal movements, feeding and growth. – Marine Biology 124: 483– 494. Bishop, A.L., Kirkland, P.D., McKenzie, H.J., Spohr, L.J., Barchia, I.M. & M.J. Muller (1995): Distribution and seasonal movements of Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae) at the southern limits of its distribution in New South Wales and their correlation with arboviruses affecting livestock. – Journal of Australian Entomology 34: 289–298.

Gender-based Movement Differences in Dice Snakes Boisvert, J.H., Huffman, R.W. & K.P. Reese (2005): Home range and seasonal movements of Columbian sharp-tailed grouse associated with conservation reserve program and mine reclamation. – Western North American Naturalist 64: 36–44. Bona-Gallo, A. & Licht. P (1983): Effects of temperature on sexual receptivity and ovarian recrudescence in the garter snake, Thamnophis sirtalis parietalis. – Herpetologica. 39(2): 173-182. Bonnet, X., Naulleau, G. & R. Shine (1999): The danger of leaving home: Dispersal and mortality in snakes. – Biological Conservation 89: 39–50. Brito, J.C. (2003): Seasonal variation in movements, home range, and habitat use by male Vipera latastei in northern Portugal. – Journal of Herpetology 37(1): 155–160. Brown, G.P. & P.J. Weatherhead (2000): Thermal ecology and sexual dimorphism in Northern water snake, Nerodia sipedon. – Ecological Monographs 70(2): 311-330. Capula, M., Filippi, E., Rugiero, L. & L. Luiselli (2011): Dietary, thermal and reproductive Ecology of Natrix tessellata in Central Italy: a synthesis. – Mertensiella 18: 147–153. Carlsson, M., Kärvemo, S., Tudor, M., Sloboda, M., Mihalca, A.D., Ghira, I., Bel, L. & D. Modrý (2011): Monitoring a large population of dice snakes at Lake Sinoe in Dobrogea, Romania. – Mertensiella 18: 237–244. Conelli, A.E. & M. Nembrini (2007): Studio radiotelemetrico dell’habitat della Biscia tassellata, Natrix tessellata (Laurenti, 1768). – Bollettino della Società Ticinese di Scienze Naturali 95: 45-54. Conelli, A.E., Nembrini, M. & K. Mebert (2011): Different habitat use of dice snakes, Natrix tessellata, among three populations in Ticino Canton, Switzerland. – A radiotelemetry study Mertensiella 18: 100–116. Cooper, W.E., Attum, O. & B. Kingsbury (2008): Escape behaviors and flight initiation distance in the common water snake Nerodia sipedon. – Journal of Herpetology 42: 493-500. Dubey, S., Brown, G. P., Madsen, T. & R. Shine (2008): Malebiased dispersal in a tropical Australian snake (Stegonotus cucullatus, Colubridae). – Molecular Ecology 17(15): 3506-3514. Durner, G. M. & J. E. Gates (1993): Spatial ecology of black rat snakes on Remington farms, Maryland. – Journal of Wildlife Management. 57(4): 812–826. Garstka, W. R., Camazine, B. & D. Crews. (1982): Interactions of behaviour and physiology during the annual reproductive cycle of the red-sided garter snake (Thamnophis sirtalis parietalis). – Herpetologica 38(1): 104-123. Gerald, G.W., Bailey, M.A. & J.N. Holmes (2006): Movements and activity range sizes of Northern Pinesnakes (Pituophis melanoleucus melanoleucus) in Middle Tennessee. – Journal of Herpetology 40(4): 503–510. Gibbons, J. & R. Semlitsch (1987, reprinted in 2002): Activity patterns. – In: Seigel, R., Collins, J. & S. Novak (Eds.): Snakes: Ecology and Evolutionary Biology. – The Blackburn Press, New Jersey, USA: 397–421. Greene, B.D., Dixon, J.R., Whiting, M.J. & J.M. Mueller (1999): Reproductive Ecology of the Concho Water Snake, Nerodia harteri paucimaculata. – Copeia 3: 701–709 Gregory, P. (1974): Patterns of spring emergence of the red-sided garter snake (Thamnophis sirtalis parietalis) in the Interlake region of Manitoba. – Canadian Journal of Zoology 52: 1063–1069. Gregory, P., Macartney, J. & K. Larsen (1987, reprinted in 2002): Spatial patterns and movements. – In: Seigel, R., Collins, J. & S. Novak (Eds.): Snakes: Ecology and Evolutionary Biology. – The Blackburn Press, New Jersey: 366–395.

Gruschwitz, M. (1986): Notes on the Ecology of the dice snake, Natrix tessellata Laur. in West Germany. – In: Roček, Z. (Ed.): Studies of Herpetology. –. Charles University Press, Prague, Czech Rep.: 499–502. Gruschwitz, M., Lenz, S., Mebert, K. & V. Lanka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Amphibien und Reptilien Europas Band 3/II Schlangen (Serpentes) II:. – AULA-Verlag, Wiesbaden, Germany: 581–644. Keogh, J.S., Webb, J.K. & R. Shine (2007): Spatial genetic analysis and long-term mark-recapture data demonstrate male-biased dispersal in a snake. – Biology Letters 3: 33–35. Lenz, S. & M. Gruschwitz (1993a): Zur Autökologie der Würfelnatter, Natrix t. tessellata (Laurenti 1768) in Deutschland (Reptilia: Serpentes: Colubridae). – Mertensiella 3: 235–252. Lenz, S. & M. Gruschwitz (1993b): Zur Populationsökologie der Würfelnatter, Natrix t. tessellata (Laurenti 1768) in Deutschland (Reptilia: Serpentes: Colubridae). – Mertensiella 3: 253–268. Lucas, M.C. & E. Batley (1996): Seasonal movements and behaviour of adult barbel Barbus barbus, a riverine cyprinid fish: Implications for management. – Journal of Applied Ecology 33: 1345–1358. Luiselli, L. & P. Zimmermann (1997). Thermal ecology and reproductive cyclicity of the snake Natrix tessellata in southeastern Austria and central Italy: A comparative study. – Amphibia-Repilia 18: 383–396. Luiselli, L., Capizzi, D., Filippi, E., Anibaldi., C, Rugiero, L. & M. Capula (2007): Comparative diets of three populations of an aquatic snake (Natrix tessellata, Colubridae) from Mediterranean streams with different hydric regimes. – Copeia 2: 426–435. Madsen, T. (1984): Movements, home range size and habitat use of radio-tracked grass snakes (Natrix natrix) in Southern Sweden. – Copeia 3: 707–713. Madsen, T. (1987): Cost of reproduction and female life-history tactics in a population of grass snakes, Natrix natrix, in southern Sweden. – Oikos 49: 129–132. Mebert, K. (2001): Die Würfelnatterpopulation am Lopper. – In: NAGON (Ed.): Amphibien und Reptilien in Unterwalden. – NAGON, Grafenort, Switzerland 2: 158-163. Mebert, K. (2007): Die Würfelnatter am Brienzersee. – In: Jahrbuch 2007, Uferschutzverband Thuner- und Brienzersee – UTB Selbstverlag, Thun, Switzerland: 169-180. Mebert, K. (Ed.) (2011): The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species . – Mertensiella 18, DGHT, Rheinbach, Germany. Necas, P., Modrý, D. & V. Zavadil (1997): Czech Recent and Fossil Amphibians and Reptiles. – Edition Chimara, Frankfurt am Main, Germany. Neumann, C. & K. Mebert (2011): Migration behavior of endangered dice snakes (Natrix tessellata) at the River Nahe, Germany. – Mertensiella 18: 39–48. Nilson, G. (1980): Male reproductive cycle of the European adder, Vipera berus, and its relation to annual activity periods. – Copeia: 729–737. Parker, W. & V. Plummer (1987, reprinted in 2002): Population ecology. – In: Seigel, R., Collins, J. & S. Novak (Eds.): Snakes: Ecology and Evolutionary Biology. – The Blackburn Press, New Jersey, USA: 253–301. Pattishall, A. & D. Cundall (2009): Habitat use by synurbic watersnakes (Nerodia sipedon). – Herpetologica 65(2): 183– 198.

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Simon Kärvemo, Martin Carlsson, Marian Tudor, Michal Sloboda, Andrei D. Mihalca, Ioan Ghira, Lucia Bel & David Modrý Pearson, D., Shine, R. & A. Williams (2005): Spatial ecology of a threatened python (Morelia spilota imbricata) and the effects of anthropogenic habitat change. – Austral Ecology 30: 261–274. Phelps, T.W. (1978): Seasonal movement of the snakes Coronella austriaca, Vipera berus and Natrix natrix in southern England. – British Journal of Herpetology 5: 775–761. Pilliod, D.S., Peterson, C.R. & P.I. Ritson (2002): Seasonal migration of Columbia spotted frogs (Rana lutiventris) among complementary resources in a high mountain basin. – Canadian Journal of Zoology 80: 1849–1862. Pluto, T.G. & E.D. Bellis (1988): Seasonal and annual movements of riverine map turtles, Graptemys geographica. – Journal of Herpetology 22(2): 152–158. Prestt, I. (1971): An ecological study of the viper Vipera berus, in southern Britain. – Journal of Zoology 164: 373–418. Roth, T.C., Greene, B.D. & C.M. Taylor (2006): Movement patterns and home range use of the northern watersnake (Nerodia sipedon). – Copeia 3: 544–551. Santos, X. & G. Llorente (2001): Seasonal variation in reproductive traits of the oviparous watersnake, Natrix maura, in the Ebro Delta of northeastern Spain. – Journal of Herpetology 35: 653–660. Schwartz, J.M., McCracken, G.F. & B.M. Burghardt (1989): Multiple paternity in wild populations of the garter snake, Thamnophis sirtalis. – Behavioral Ecology and Sociobiology 25: 269–273. Seigel, R. & N. Ford, (1987, reprinted in 2002): Reproductive ecology. – In: Seigel, R., Collins, J. & S. Novak (Eds.): Snakes: Ecology and Evolutionary Biology. – The Blackburn Press, New Jersey, USA: 211–252.

Shine, R., Elphick, M.J., Harlow, P.S., Moore, I.T., LeMaster, M. P. & R.T. Mason (2001a): Movements, mating, and dispersal of red-sided gartersnakes (Thamnophis sirtalis parietalis) from a communal den in Manitoba. – Copeia 1: 82–91. Shine, R., LeMaster, M.P., Moore, I.T., Olsson, M.M. & R.T. Mason (2001b): Bumpus in the snake den: Effects of sex, size, and body condition on mortality of red-sided garter snake. – Evolution 55(3): 598–604. Street, D. (1979): The Reptiles of Northern and Central Europe. – B.T. Batsford Ltd, London. Sun, L., Shine, R., Debi, Z. & T. Zhengren, (2001): Biotic and abiotic influences on activity patterns of insular pit-vipers (Gloydius shedaoensis, Viperidae) from north-eastern China. – Biological Conservation 97: 387–398. Tierson, W.C., Mattfeld, G.F., Sage, R.W., Jr. & D.F. Behrend (1985): Seasonal movements and home ranges of white-tailed deer in the Adirondacks. – Journal of Wildlife Management 49: 760–769. Velenský, M., Velenský, P. & K. Mebert (2011): Ecology and ethology of an urban population: dice snakes, Natrix tessellata, of Prague, Czech Republic. – Mertensiella 18: 157–176. Viitanen, P. (1967): Hibernation and seasonal movements of the viper, Vipera berus berus (L.), in Southern Finland. – Societas Zoologica Botanica Fennica Vanamo 4: 472–576. Weatherhead, P.J. & K.A. Prior (1992): Preliminary observations of habitat use and movements of the eastern massasauga rattlesnake (Sistrurus c. catenatus). – Journal of Herpetology 26(4): 447–452. Zimmermann, P. & G. Fachbach (1996): Verbreitung und Biologie der Würfelnatter, Natrix tessellata tessellata (Laurenti, 1768), in der Steiermark (Österreich). – Herpetozoa 8: 99–124.

Authors Simon Kärvemo, Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden; Martin Carlsson*, Evolutionary Biology Centre, Uppsala University, Sweden; Marian Tudor, Natural Science Faculty, Ovidius University of Constanta, Romania; Andrei D. Mihalca, Lucia Bel, Faculty of Veterinary Medicine, Cluj-Napoca, Romania; Michal Sloboda, David Modrý Faculty of Veterinary Medicine, Brno, Czech Republic; David Modrý , Institute of Parasitology of CAS, České Budějovice, Czech Republic; Ioan Ghira, Faculty of Biology, Cluj-Napoca, Romania. *Corresponding author and current address: Population and Conservation Biology, Department of Ecology and Evolution, Uppsala University, Norbyv, 18D, 75236 Uppsala, Sweden, e-mail: [email protected].

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MERTENSIELLA 18

255-271

20 September 2011

ISBN 978-3-9812565-4-3

Parasitism in the Dice Snake (Natrix tessellata) – a Literature Review Andrei Daniel Mihalca Abstract. A review of studies on the parasitic fauna of dice snakes is presented. The highest number of parasitological works originates from former soviet authors. The systematic diversity of parasites is high and includes Protozoa (4 genera), Trematoda (19 genera), Cestoda (3 genera), Acanthocephala (2 genera), Nematoda (22 genera) and Arthropoda (1 genus). General life-cycles and contamination routes, as well as the pathogenic effect of parasites on dice snakes, are discussed. Keywords. Squamata, Natrix tessellata, parasites, helminth, protozoa, trematoda, cestoda, nematoda, arthropoda

Introduction Since its description by Laurenti in 1768, several authors published results regarding parasitic fauna of dice snakes from various locations throughout its distribution range. By far, the highest amount of parasitological works on Natrix tessellata relates to former soviet authors dealing with helminth fauna. Except original articles and communications, several reviews on parasitic helminths of reptiles from the former USSR were published, usually as part of a general review on reptile parasite fauna. For example, Sharpilo (1964) reviewed the larval nematodes parasitic in reptiles from Ukraine and followed with an extensive review on parasitic helminths of reptiles from the USSR (Sharpilo 1976). Two bibliographical lists were published by Markov et al. (1969) for ecology and parasitology (i.e. parasitic protozoa, helminths and arthropods) of Squamata and by Markov et al. (1972) for helminthology (trematodes, cestodes, nematodes and acanthocephalans) of Squamata. More recent reviews on the helminths of reptiles from the Volga basin were published by Evlanov et al. (1996, 2001, 2002) and Kirillov (2002, 2006) with Bakiev (2004) summarizing the previous data on parasites of snakes from the middle Volga region. Reviews on protozoa of reptiles were made by Ovezmukhammedov (1987, 1991). However, all of these reviews are available only in Russian and are focused on specific regions of the former USSR. One review work published in English, including data on dice snakes is the extensive checklist of nematodes parasitic in amphibians and reptiles by Baker (1987). The current review presents a systematic account of all parasitic species recorded in N. tessellata across its entire geographical range. Original papers, communications, case reports and reviews are all considered and cited. Specific data on epidemiology, life cycles and pathology will be mentioned where available. Comments on possible misidentification are also provided.

Diversity, Ecology and Biology of Parasites in Natrix tessellata Ecology of a host greatly influences its parasitic fauna. As in many other semiaquatic snakes, the diversity of parasitic species in dice snakes is relatively high. Most of the parasitological publications on N. tessellata are host reports from certain geographical areas, with the majority of them including data on parasite location in the host and epidemiological results (prevalence, intensity range, mean intensity). All these data are summarized in Tables 1–6. The general overview of literature suggests that the majority of the examined snakes are infected by helminth parasites (prevalence of parasitism was 100% in many of the studies), whereas protozoans and arthropods have rarely been reported. One reason for the low number of protozoans reported in dice snakes is because usually parasitological exams skipped the techniques for unicellular parasites and focused on helminth fauna instead. Even though, some studies included microscopic examinations, their results were negative for protozoan parasites (Markov & Bogdanov 1965, Markov et al. 1969). Except mites, arthropod parasites were rarely reported, mainly because of the partly aquatic life style of dice snakes. Like in the case of protozoans, few studies included ectoparasitological data, and if they did, most reported negative results (Markov & Bogdanov 1960, 1964, Markov et al. 1969). Among helminths, adult and larval trematodes are the most prevalent parasites in N. tessellata (Biserkov 1989, Kirin 1994, Kirillov et al. 2001, Kirillov 2002, 2006). In a study about the Volga Delta, Ivanov (1952, 1954) found that 100% of the dissected N. tessellata were infected with trematodes, 20% with nematodes and 5% with each, cestodes and acanthocephalans. Regarding the number of species, nematodes constituted the most diverse group in dice snakes. Overall, 22 genera of nematodes, 19 of trematodes, 4 of protozoans, 3 of cestodes, 2 of acanthocephalans and one genus of Arthropoda have been found in N. tessellata. However, in some

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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populations, trematodes yielded the most diverse group of helminth parasites in N. tessellata (Dubinina 1950, Dubinin 1952, 1953, Ivanov 1952, 1954, Sharpilo 1959a, 1959b, Markov et al. 1962, 1969, Bakiev & Kirillov 2000, Kirillov & Kirillova 2007). Helminth infection in N. tessellata usually occurs following ingestion of prey infected with larval stages. Dice snakes prey normally on fish, but variably also on amphibians (Filippi et al. 1996, Gruschwitz et al. 1999, Luiselli et al. 2007). Both prey groups may host such internal parasites. For example, Dubinin (1949) showed experimentally that larvae of the acanthocephalan fish parasite Corynosoma strumosum infected dice snakes. Mihalca et al. (in prep,) applied molecular methods to prove that natural infection of snakes with larvae of Eustrongylides excisus occurred after consumption of infected fish. Dice snakes can be hosts to parasites which are homoxenous (i.e. those parasites which require a single host for completing their life cycle) or heteroxenous (i.e. requiring at least two hosts to complete their life cycle; the host in which the adult parasites live are called definitive hosts; the hosts where immature stages of the parasites develop are the intermediate hosts). For many of the heteroxenous helminths listed as being parasitic in N. tessellata, snakes are definitive hosts. For those helminths which were found as larval forms (noted with * in Tabs. 1–6), snakes are intermediate hosts (obligatory or facultative). If a dice snake is able to transmit these larval forms to the next host, which naturally preys on snakes, remains a question until further studies. However, Sudarikov et al. (1991) succeeded in experimentally infecting young cats using infective larval stages (called metacercariae) of trematodes of the genus Neodiplostomum collected from dice snakes. In another experimental trial, Ryzhenko (1968) infected definitive hosts using larval stages (plerocercoids) of Spirometra erinaceieuropaei collected from N. tessellata. In some cases, parasites found in the stomach of dice snakes are just mechanically transmitted and are not able to infect the snake. In these cases, they are just parasites of the prey and qualify as pseudoparasites for snakes. For example nematode larvae parasitic in fish are frequently found alive in the stomach of dice snakes, and usually pass digestive tract of the snake without infecting it (Mihalca pers. obs.). Such parasitic forms listed in the Tables 1–6 are correspondingly commented in footnotes. Protozoa At least four genera of protozoans are mentioned as parasitic in N. tessellata (Tab. 1). One of the most intriguing findings is Haemogregarina sp. in the erythrocytes of dice snakes by Vakker (1970), as these hemoprotozoans are exclusively found in chelonians. As suggested by Telford (2009), these hemoprotozoans probably belong to the genus Hepatozoon. The sarco-

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mastigophorans (a phylum including the so called “flagellated protozoans”) are common findings in the intestine of snakes. For instance, genera Proteromonas and Chilomastix were found in the digestive tracts of many snake, lizard and chelonian species (Barnard & Upton 1994). An uncommon localization in the blood was cited in dice snakes by Vakker (1970) for Proteromonas. As this genus is specifically an intestinal parasite, it is most likely a misidentification or a fecal contamination of blood smears. However, sarcomastigophorans were reported in blood of dice snakes by Markov et al. (1964), but with no specific identification. Generally, blood of snakes can be parasitized by at least two genera of flagellated protozoa: Leishmania and Trypanosoma (Telford 2009). As Leishmania does not have mobile stages in the blood of vertebrates, I presume that the blood forms found by Vakker (1970) and by Markov et al. (1964) were members of the genus Trypanosoma. Hemoparasites morphologically identified as Pirhemocyton (Vakker 1970) where later shown to be of viral origin (Telford 2009). Intestinal flagellates described as Trichomonas by Işfan (1965) might belong to another genus of the order Trichomonadida, as generic identification based on direct light microscopy is currently considered uncertain. Moreover, genus Trichomonas is parasitic only in warm-blooded animals. Hence, I suggest, that the forms identified by Işfan (1965) might be any of the other genera of Trichomonadida that have been found in snakes such as Hypotrichomonas, Monocercomonas or Tetratrichomonas (Barnard & Upton 1994). Trematoda So far, 19 genera of trematodes (flukes), all from the subclass Digenea, have been reported in N. tessellata (Tab. 2). Except one genus (Diplodiscus), all the trematodes for which dice snakes are definitive hosts belong to the superfamily Plagiorchioidea, indicating a close coevolution: Allopharynx, Plagiorchis (Plagiorchiidae), Encyclometra (Encyclometridae), Leptophalus, Macrodera (Fig. 1), Paralepoderma (Leptophalidae), Opisthioglyphe, Telorchis (Telorchiidae), Cephalogonimus (Cephalogonimidae), Patagium (Auridistomidae) and Astiotrema (incertae saedis). The life cycle of Paralepoderma cloacicola was described in dice snakes by Dabrowolskij (1969). Yildirimhan et al. (2007), citing Căpuşe (1971), wrongly included the trematode Telorchis assula on the checklist of parasites in N. tessellata, as Căpuşe found it only in Natrix natrix. The genus Diplodiscus (superfamily Paramphistomiformes) was reported only once, in Bulgaria (Kirin 1994). Its life-cylce is not known. For all the other genera listed in Table 2, dice snakes are intermediate hosts. Even if not always mentioned by authors, according to the generally known and accepted life-cycle patterns of trematodes, all larval stages found in different organs of snakes are metacercariae or

Review of Parasitism in Natrix tessellata

Tab. 1. Protozoa reported in Natrix tessellata Species

Location in host Geographic data

Flagellata sp. Flagellata sp.

blood -

Proteromonas lacertae intestine blood1 Chilomastix wenyoni intestine erythrocytes Haemogregarina sp.2 Pirhemocyton sp.3 blood intestine Trichomonas sp.4

Prevalence (%)

Astrakhanskaya, Russia 16.7 Bulgaria Astrakhanskaya, Russia Kazakhstan Kazakhstan Kazakhstan Kazakhstan Romania

16.7 5.4 1.1 1.1 2.6

Intensity range Reference (mean intensity) Markov et al. 1964 Tomova & Golemansky 2001 Markov et al. 1964 Vakker 1970 Vakker 1970 Vakker 1970 Vakker 1970 Işfan 1965

Probably misidentification Probably an undescribed species of Hepatozoon 3 Currently Pirhemocyton like inclusions are considered iridoviruses (Telford 2009) 4 Probably some other genus from the order Trichomonadida 1 2

mesocercariae. The five genera of trematodes reported as larval stages in dice snakes belong to the superfamily Diplostomoidea: Alaria, Codonocephalus, Neodiplostomum, Pharingostomum (Diplostomidae), and Strigea (Strigeidae). Amphibians are second intermediate hosts for these genera (Niewiadomska 2002), so dice snakes could acquire the infection after preying on anurans. Sudarikov (1960, 1962) concluded that dice snakes are competent intermediate hosts for Strigea strigis, S. sphaerula, Neodiplostomum spathoides and Alaria alata; moreover, he later succeeded (Sudarikov 1991) in experimentally infecting young cats using metacercariae of Neodiplostomum collected from dice snakes. Azygia (Azygiidae) found by Moravec (1963) in the stomach of one dice snake is a case of pseudoparasitism, as this genus is a typical parasite of fish. The finding of adult specimens of the genus Cryptocotyle (Heterophyi-

Fig. 1. Adult Macrodera longicollis in a lung of Natrix tessellata.

dae) parasitic in the intestine of dice snakes by Sharpilo (1976) is arguable. Members of family Heterophyidae infect their definitive hosts (birds and mammals) through an amphibian or a fish stage, usually a metacercariae (Pearson 2008), so I consider the finding of Sharpilo as a pseudoparasite. Cestoda As in the case of trematodes, cestodes (tapeworms) are encountered in dice snakes either as adult stages or as various larval forms. The only cestode species for which dice snakes serve as definitive host is Ophiotaenia europaea (Proteocephalidae) (Rego 1994). Biserkov & Genov (1988) experimentally showed that copepods serve as intermediate hosts for O. europaea. Later, during an experimental trial, Biserkov & Kostadinova (1997) using copepods infected with procercoids (first larval stages) of O. europaea only partly succeeded to infect dice snakes. They found only encysted larval forms (plerocercoids) in the infected snakes and were not able to obtain fully developed adult tapeworms. They stated that its life cycle probably includes three different and subsequent hosts, so snakes are susceptible to infection only if they ingest the second intermediate vertebrate host. When captured, as a defense mechanism, dice snakes spread an obnoxious smelling secretion from the cloaca. Infective body segments (gravid proglotids) of O. europaea are often eliminated (Fig. 2) during this defensive behavior (Mihalca 2007). Two other cestode species were reported as larval stages in dice snakes. Spirometra erinaceieuropaei (Diphyllobothriidae), a parasite of carnivorous mammals, is frequently encountered as larval stage (plerocercoids) in all tetrapod vertebrates, including snakes (Fig. 3) and other reptiles (Bray et al. 1994). Snakes get the parasite after ingesting infected fish. Several life-cycle trials using larval forms of S. erinaceieuropaei collected

257

258

Macrodera longicollis

Leptophalus nigrovenosus

Cryptocotyle concavum*1 Diplodiscus subclavatus Encyclometra caudata Encyclometra colubrimurorum

Cephalogonimus retusus Codonocephalus urnigerus*

lung lung lung lung lung lung lung lung lung lung lung

fat, muscles, mouth, liver, kidneys pericardium, blood vessels, serosa of body cavity, fat tail hypodermic tissue, fat body cavity, fat tissue, internal organs heart, esophagus, mouth, urinary organs stomach intestine intestine intestine internal organs muscles, subcutaneous, internal organs intestine cloaca stomach stomach esophagus, stomach, intestine stomach stomach esophagus, stomach, intestine digestive tube digestive stomach stomach mouth mouth, pharynx, esophagus

Alaria alata*

Azygia lucii1 Allopharynx amudariensis Astiotrema monticelli

Location in host

Species

100 10 25 11.1 10 5 10 10 5.31 5 100 22.2 10 50 3.5 3 45.4 2.65 -

Ukraine Armenia Astrakhanskaya, Russia Astrakhanskaya, Russia Volgogradskaya, Russia Czech Republic Turkmenistan Ukraine Astrakhanskaya, Russia Bulgaria Astrakhanskaya, Russia Volga Delta, Russia Ukraine Bulgaria Astrakhanskaya, Russia Astrakhanskaya, Russia Volga Delta, Russia Ukraine Ukraine Astrakhanskaya, Russia Azerbaijan Bulgaria Bulgaria Volga Delta, Russia Bulgaria Azerbaijan; Belarus; Georgia; Russia; Ukraine Volga Delta, Russia Volga Delta, Russia Dnieper River, Ukraine Astrakhanskaya, Russia Volgogradskaya, Russia Kazakhstan Turkmenistan Bulgaria Samarskaya, Russia Volga Delta, Russia Romania 50 11.1 40 12.5 81.1 8 5.6 30 45

75

Prevalence (%)

Volga Delta, Russia Volga Delta, Russia

Geographic data

1-2 5 (5) (9) 3 (3) 1-4 2 (2) 1-5 1-2 (1.3)

(4) 7-11 (9) 1 (1) 57 (57) (3.5) 7 (7) 1-2 1 (1) 3–80 (34.4) (12) (43.3) 1-2 1 (1) 1-6 1-2 -

Intensity range (mean intensity) 15-500 (224.2)

Tab. 2. Trematodes reported in Natrix tessellata

Sharpilo 1959b Darevskiy 1961 Markov et al. 1962 Sudarikov 1962 Markov et al. 1969 Moravec 1963 Velikanov & Sharpilo 2002 Sharpilo 1959b Markov et al. 1962 Kirin 1996a, Kirin 1996b Markov et al. 1962 Ivanov & Semyenova 2000 Sharpilo 1976 Kirin, 1994 Markov et al. 1962 Dubinina 1950 Dubinina 1953 Sharpilo 1959a Sharpilo 1959b Markov et al. 1962 Sharpilo 1976 Kirin, 1994 Biserkov 1996 Ivanov & Semyenova 2000 Kirin, 1994 Sharpilo 1976, Evlanov et al. 1996, Bakiev & Kirillov 2007 Ivanov 1952 Dubinina 1953 Sharpilo 1959a Markov et al. 1962 Markov et al. 1969 Vakker 1970 Velikanov 1982 Biserkov 1996 Bakiev & Kirillov 2000 Ivanov & Semyenova 2000 Mihalca et al. 2007b

Dubinin 1952 Dubinina 1950

Reference

Andrei Daniel Mihalca

Strigea sphaerula*

Plagiorchis elegans

Patagium lazarewi Pharingostomum cordatum*

Opisthioglyphe ranae Paralepoderma cloacicola

muscles, internal organs lung, heart, other internal organs all internal organs, mesentery, fat, muscles, serosa of body cavity fat, body cavity, serosa of internal organs

Neodiplostomum attenuatum* Neodiplostomum spathoides*

mesentery muscles, internal organs intestine cloaca cloaca cloaca digestive intestine, cloaca, urinary bladder cloaca cloaca intestine, cloaca intestine intestine fat, body cavity, serosa of internal organs fat, mesentery, serosa of internal organs intestine intestine stomach intestine intestine serosa of internal organs, body cavity, mesentery, fat, muscles internal organs, fat mesentery, fat, serosa of internal organs muscles, internal organs

Location in host

Species 20 100 5 25 20 40 16.7 33.3 20 25 7.08 8 10 0.88 100 20 25 3.3 22.2 10 83.3 15 37.5 27.8 70

Astrakhanskaya, Russia; Kulaly Island, Kazakhstan Astrakhanskaya, Russia Volgogradskaya, Russia Turkmenistan Volga Delta, Russia Volga Delta, Russia Volga Delta, Russia Volga Delta, Russia Ukraine Ukraine Europe Volgogradskaya, Russia Bulgaria Bulgaria Volga Delta, Russia Bulgaria Volga Delta, Russia Volga Delta, Russia Astrakhanskaya, Russia Astrakhanskaya, Russia Volgogradskaya, Russia Kazakhstan Samarskaya, Russia Europe Germany Volga Delta, Russia Volga Delta, Russia Samarskaya, Russia Volga Delta, Russia Astrakhanskaya, Russia Astrakhanskaya, Russia Volgogradskaya, Russia Samarskaya, Russia Volga Delta, Russia

Prevalence (%)

Volga Delta, Russia Volga Delta, Russia Volga Delta, Russia Volga Delta, Russia

Geographic data

(2.3) 25-78 (46.3) 1-40 1-202

4-17 (10.5) 1-160 (80.5) 1-9 2-5 5-15 (10) 2-3 (2.5) 1-3 15-60 1-6 1 200-500 (14.7) 2-7 (4.5) 1-66 4 (4) 100-120

1 (1)

Intensity range (mean intensity) 2-87 (44.5) 53-500

Markov et al. 1962 Sudarikov 1962 Markov et al. 1969 Bakiev & Kirillov 2000 Ivanov & Semyenova, 2000

Sudarikov 1962 Markov et al. 1969 Velikanov 1982 Ivanov & Semyenova 2000 Ivanov & Semyenova 2000 Dubinina 1950 Dubinina 1953 Sharpilo 1959a Sharpilo, 1959b Dabrowolskij 1969 Markov et al. 1969 Kirin, 1994 Biserkov 1996 Ivanov & Semyenova 2000 Kirin, 1994 Dubinina 1950 Dubinina, 1953 Markov et al. 1962 Sudarikov 1962 Markov et al. 1969 Vakker 1970 Bakiev & Kirillov 2000 Linstow 1878, Boulenger 1913 Brauer 1911 Ivanov 1952 Ivanov & Semyenova 2000 Kirillov 2000 Dubinina 1953

Markov et al. 1962

Ivanov & Semyenova 2000 Dubinin 1952 Dubinina 1950 Dubinina 1953A

Reference

Review of Parasitism in Natrix tessellata

Tab. 2. Trematodes reported in Natrix tessellata (continued)

259

260

* Larval stages 1 Probably pseudoparasites (see text for details)

Telorchis stossichii

intestine intestine

body cavity, lung, liver, kidneys, other organs body cavity, mesentery, intestinal wall, internal organs lung, fat, muscles, internal organs subcutaneous, fat, mesentery, serosa of internal organs muscles, internal organs intestine intestine intestine intestine intestine intestine intestine intestine intestine intestine intestine intestine intestine intestine

Strigea strigis*

Telorchis assula

Location in host

Species

100 50 35 50 2.2 16.7 40 100 50 45 13.1 37.5 59.8 27.43 43 66.7 70 -

Volga Delta, Russia Volga Delta, Russia Ukraine Astrakhanskaya, Russia Astrakhanskaya, Russia Volgogradskaya, Russia Kazakhstan Turkmenistan Samarskaya, Russia Volga Delta, Russia Volga Delta, Russia Volga Delta, Russia Ukraine Astrakhanskaya, Russia Romania Volgogradskaya, Russia Kazakhstan Daghestan, Russia Turkmenistan Bulgaria Bulgaria Samarskaya, Russia Volga Delta, Russia Azerbaijan; Georgia; Kalmykia, Russia; Kirgizia Turkey Bulgarua 71 3.54

-

Prevalence (%)

Volga Delta, Russia

Geographic data

1-21 (7.3) 1-2

3-15 1-32 2-28 (12.5) 1-40 (36.1) 6-15 (9.3) 1-3 2-76 2-55 1-18 -

10-150 (68) 9-27 (19.5)

(250)

Intensity range (mean intensity) -

Tab. 2. Trematodes reported in Natrix tessellata (continued)

Yildirimhan et al. 2007 Kirin 1994

Vakker 1970 Velikanov 1982 Bakiev & Kirillov 2000, Kirillov 2000 Ivanov & Semyenova 2000 Ivanov 1952 Dubinina 1953 Sharpilo 1959b Markov et al. 1962 Işfan 1965 Markov et al. 1969 Vakker 1970 Markov et al. 1972 Velikanov 1982 Kirin, 1994 Biserkov 1996 Bakiev & Kirillov 2000, Kirillov 2000 Ivanov & Semyenova 2000 Bakiev & Kirillov 2007

Sharpilo 1959a Markov et al. 1962 Sudarikov 1962 Markov et al. 1969

Dubinina 1950 Dubinina 1953

Dubinin 1952

Reference

Andrei Daniel Mihalca

Review of Parasitism in Natrix tessellata

Fig. 2. Ophiotaenia europaea gravid proglotid emerging from a cloaca of Natrix tessellata.

a vertebrate. However, in many cases an additional host (usually a lower vertebrate) intermediates the transmission from the arthropod to the vertebrate. Even if reptiles were often reported as definitive hosts for adult acanthocephalans, dice snake are host only for the larval forms, therefore being intermediate hosts (Tab. 4). Two species belonging to two genera were reported in N. tessellata. For the genus Corynosoma the first intermediate hosts are marine amphipods, while definitive hosts are seals. Fish are facultative intermediate hosts (Kennedy 2006) and are responsible for transmitting the larval parasites to dice snakes. Genus Sphaerirostris is parasitic in birds and intermediate hosts are insects. Many reptile species have been found infected with larval stages of this parasite (Hromoda et al. 2000). As dice snakes do not feed on insects, accidental infection might occur after ingestion of frogs. Nematoda

Fig. 3. Plerocercoid of Spirometra erinaceieuropaei in Natrix natrix.

from dice snakes were performed. Ryzhenko (1968) experimentally infected dogs, cats and foxes using plerocercoids from N. tessellata. Development of this parasite in the body of dice snakes from procercoids to plerocercoids takes place in the muscles and subcutaneous tissue (Dubinina 1951). Plerocercoids of S. erinaceieuropaei collected from dice snakes have also been used in morphological studies by Gofman-Kadoshnikov et al. (1968). The second cestode genus recorded as larvae from dice snakes is Mesocestoides (Mesocestoididae). The first larval stage is not known. In snakes, the second larval forms (called tetrathyridium) are present. Adult parasites are hosted by carnivorous mammals and rarely by birds (Rausch 1994). Acanthocephala Also known as thorny-headed worms, the acanthocephalans have a complex heteroxenous life-cycle, typically involving two hosts. The intermediate host is always an arthropod while the definitive host is always

The most diverse group of helminths parasitic in dice snakes are nematodes. At least 22 genera of nematodes have been reported in dice snakes, 12 as adults and 10 as larvae (Tab. 5). Life cycle of nematodes is complex, as is their development and transmission. From the 12 genera of nematodes for which dice snakes are hosts to adults, six have homoxenous (direct) development (Rhabdias, Strongyloides, Oxysomatium, Aplectana, Oswaldocruzia and Kalicephalus), so contamination of snakes occurs from the environment, either orally, or transcutaneously. The remaining six genera (Amplicaecum, Angusticacecum, Hexametra, Abbreviata, Dracunculus and Camallanus) have heteroxenous life-cycle and infection of snakes follows ingestion of an intermediate or paratenic (accidental, transport) fish or amphibian hosts. Order Rhabditida is present as adults in dice snakes with two genera. In the genus Strongyloides contamination of snakes is via transcutaneous penetration of larvae from the environment (Anderson 2000). In the genus Rhabdias (Fig. 4), contamination of snakes is oral, although in amphibian hosts, transcutaneous infection has been repeatedly reported. The possibility of contamination of snakes through a transport paratenic hosts has been suggested but not proved yet (Anderson 2000). From the order Ascaridida five genera were reported as adults in dice snakes (Oxysomatium, Aplectana, Amplicaecum, Angusticacecum and Hexametra). Life cycles of the genera Oxysomatium and Aplectana have not been studied so far in reptiles. However, in members of the same family parasitic in other vertebrates, the life cycle was shown to be homoxenous. In some species of the genus Aplectana parasitic in frogs, infection of host occurred by oral contamination (Anderson 2000), so this possibility should also be considered for snakes. In the genus Amplicaecum only one species has been studied with regards to its life-cycle. Anderson (2000) sug-

261

262

* Larval stages

Spirometra erinaceieuropaei*

subcutaneous serosa of lungs -

26.7 81.6 11.1 -

75 88 75 11.1 55

Georgia, Azerbaijan Romania Turkey Volga Delta, Russia Volga Delta, Russia Volga Delta, Russia Angren, Uzbekistan Astrakhanskaya, Russia; Kulaly Island, Kazakhstan Tashkentskaya, Uzbekistan Astrakhanskaya, Russia Volga Delta, Russia Daghestan, Russia Azerbaijan; Tajikistan

intestine intestine intestine subcutaneous, muscles, body cavity subcutaneous, muscles, body cavity subcutaneous, muscles, body cavity body cavity subcutaneous, body cavity

intestine intestine intestine intestine intestine intestine intestine intestine

Volga Delta, Russia Volga Delta, Russia Ukraine 22.2 Ukraine 33.3 Astrakhanskaya, Russia; Kulaly 55 Island, Kazakhstan Czech Republic 83.3 Germany USSR Volgogradskaya, Russia 50 Turkmenistan Daghestan, Russia Bulgaria 48 Samarskaya, Russia 77.8

subcutaneous, muscles, body cavity intestine intestine intestine intestine

Prevalence (%)

Mesocestoides sp.* Ophiotaenia europaea

Geographic data

Location in host

Species

Tab. 3. Cestoda reported in Natrix tessellata

4-18 (8.7) 2 (2) -

1-9 (3.5) 3-36 (14.28) 1-17 (23.2)

1-12 3-12 (8) 2-8 1-36

Intensity range (mean intensity) 200 (57)

Abdushukurova et al. 1966 Gofman-Kadoshnikov et al. 1968 Ryzhenko 1969 Markov et al. 1972 Bakiev & Kirillov 2007

Moravec 1963 Odening 1963 Frese 1965 Markov et al. 1969 Velikanov 1982 Markov et al. 1972 Biserkov 1996 Bakiev & Kirillov 2000, Kirillov 2000 Bakiev & Kirillov 2007 Mihalca et al. 2007b Yildirimhan et al. 2007 Dubinin 1952 Dubinina 1951 Dubinina 1953 Markov & Bogdanov 1960 Markov et al. 1962

Dubinina 1950 Dubinina 1953 Sharpilo 1959a Sharpilo 1959b Markov et al. 1962

Reference

Andrei Daniel Mihalca

Review of Parasitism in Natrix tessellata

Tab. 4. Acanthocephala reported in Natrix tessellata Species

Location in host Geographic data

Prevalence

Corynosoma strumosum*

pericardium body cavity body cavity body cavity mesentery mesentery

22.2 20 5 11.1

Sphaerirostris teres*

Volga Delta, Russia1 Ukraine Ukraine Turkmenistan Astrakhanskaya, Russia Chu-Iliyskoye, Kazakhstan

* Larval stages 1 Experimental infection

Intensity range (mean intensity) 2-5 (3.5) 1 (1) 10-14

Reference Dubinin 1952 Sharpilo 1959a Sharpilo 1959b Velikanov 1982 Markov et al. 1962 Markov & Bogdanov 1965

gested that the intermediate hosts for the other species might be amphibians. Bogdanov (1954) showed that larvae of this nematode penetrate into the gastric wall of dice snakes during hibernation. However, the presence of the genus Angusticacecum in snakes is questionable and I presume that it is a misidentification, as only one species, A. holopterum, is known as a parasite of turtles (Baker 1987). The genus Hexametra includes heteroxenous species parasitic in snakes and lizards. All life-cycle studies suggest that the development of larvae takes place in the internal organs of small mammals (Anderson 2000). But how dice snakes, as non-mammal eating snakes, get infected remains unclear. Dice snakes are definitive hosts for two genera of the order Strongylida (Oswaldocruzia and Kalicephalus). Both are homoxenous and contamination occurs orally with infective third stage larvae directly from the environment (Anderson 2000). However, in some species of Oswaldocruzia transcutaneous penetration of larvae has been described (Anderson 2000). Three genera belonging to the order Spirurida have been reported in dice snakes as definitive hosts: Abbreviata, Dracunculus and Camallanus, all three with heteroxenous life-cycle. Members of the genus Abbreviata

use insects as intermediate hosts, but it is unclear how they succeed in infecting snakes. Nevertheless, for some species, anuran paratenic hosts have been recorded (Anderson 2000). Camallanus found in dice snakes are likely pseudoparasites, as both species of the genus are typically fish parasites (Anderson 2000). Genus Dracunculus uses as first intermediate host a copepod. Ingestion of copepods by snakes is usually via a fish or an amphibian paratenic host (Anderson 2000). Larval nematodes from ten genera (Anisakis, Agamospirura, Ascarops, Contracaecum, Eustrongylides, Physocephalus, Porrocaecum, Spirocerca, Spiroxys and Streptocara) were found in N. tessellata. As dice snakes are intermediate hosts, they are all heteroxenous nematodes. The majority of larval nematodes genera found in dice snakes belong to the order Spirurida (Agamospirura, Ascarops, Physocephalus, Spirocerca, Spiroxys and Streptocara). Adults of the genera Ascarops, Physocephalus and Spirocerca are parasites of mammals (definitive hosts) and insects (intermediate hosts). Larval stages have been also described in many other vertebrates which serve as paratenic hosts (Anderson 2000). Snakes are almost certainly infected after ingesting anuran para-

Fig. 4. Adult Rhabdias fuscovenosa in a lung of Natrix tessellata.

Fig. 5. SEM of the anterior end of a fourth stage larvae of Eustrongylides excisus collected from a dice snake.

263

264

stomach -

stomach and intestine wall digestive tube wall stomach, intestine wall, liver, body cavity intestine wall esophagus, stomach, intestine wall stomach stomach wall stomach, intestine stomach wall intestine body cavity intestine intestine stomach, intestine wall, liver, subcutaneous intestine intestine intestine intestine

intestinal wall body cavity, mesentery, subcutaneous, tongue, vagina, pericardium subcutaneous, body cavity, pericardium -

Abbreviata sp. Abbreviata abbreviata

Agamospirura biruchi1* Agamospirura longioesophaga* Agamospirura magna* Agamospirura minuta* Agamospirura natricis* Amplicaecum schikhobalovi

Contracaecum sp.*

Dracunculus oesophagea

Camallanus truncatus3

Camallanus lacustris3

Aplectana ivanitzkyi Aplectana brumpti Ascarops strongylina*

Angusticaecum holopterum2 Anisakis sp.*

Location in host

Species

Tab. 5. Nematoda reported in Natrix tessellata

50 20 -

Astrakhanskaya, Russia Turkmenistan

72.2 9.1 11.7

75 57 38.9 80 6.5 2.2 11.1 -

22.2 -

Prevalence (%)

Ukraine Turkmenistan Volga Delta, Russia

Czech Republic Ukraine Bulgaria Samarskaya, Russia

Ukraine Ukraine Azerbaijan; Ukraine Ukraine Volga Delta, Russia Uzbekistan Uzbekistan Chu-Iliyskoye, Kazakhstan Tashkentskaya, Uzbekistan Kazakhstan Kazakhstan Azerbaijan Turkmenistan Daghestan, Russia Ukraine Ukraine

Daghestan, Russia Europe

Geographic data

(5.5) -

-

1-8 3 (3) 1-2

1-5 (5.9) 4-7 1-23 (6.5) 2 (2) -

Intensity range (mean intensity) 1-13 (7) -

Markov et al. 1962 Velikanov 1982

Moravec 1963 Sharpilo 1976 Kirin 2002 Kirillov & Evlanov 1999, Bakiev & Kirillov 2000, Kirillov 2000 Sharpilo 1964 Velikanov 1982 Ivanov 1954

Markov et al. 1972 Boulenger 1913, Fuhn & Vancea 1961 Sharpilo 1976 Sharpilo 1964 Sharpilo 1964; 1976 Sharpilo 1964 Dubinina 1953 Bogdanov 1954, Sharpilo 1976 Markov & Bogdanov 1960 Markov & Bogdanov 1965 Abdushukurova et al. 1966 Vakker 1970 Vakker 1970 Sharpilo 1976 Velikanov 1982 Markov et al. 1972 Sharpilo 1976 Sharpilo 1964

Reference

Andrei Daniel Mihalca

Porrocaecum sp.* Rhabdias fuscovenosus

Oswaldocruzia filiformis Oxysomatium brevicaudatum Physocephalus sexalatus*

Kalicephalus viperae Oswaldocruzia goezei

lung lung lung

lung lung lung lung lung lung lung Azerbaijan Romania Turkey

Volga Delta, Russia Volga Delta, Russia Ukraine Astrakhanskaya, Russia Atyrauskaya, Kazakhstan Czech Republic Volgogradskaya, Russia Kazakhstan Daghestan, Russia Turkmenistan Bulgaria Samarskaya, Russia

lung lung lung lung

35 42

100 37.5 54.3 54 66.7

100 15 22.2 65

30 12.5 2.2 -

46 5 -

Turkey Astrakhanskaya, Russia former USSR Azerbaijan Astrakhanskaya, Russia Volgogradskaya, Russia former USSR Europe Kazakhstan Turkmenistan Turkmenistan Europe

8.3 17 9.1 85 85.2

Prevalence (%)

Volga Delta, Russia Volga Delta, Russia Bulgaria Ukraine Bulgaria Romania Romania Romania

intestine intestine intestine, stomach intestine intestine stomach, intestine wall, liver lung

body cavity body cavity mesentery mesentery subcutaneous, body cavity subcutaneous, muscles, serosa of esophagus, stomach, intestine and liver, lung muscles intestine intestine

Eustrongylides excisus*

Geographic data

6-21 (12.4) 1-125 (20.54)

4-85 6-20 (14.6) 1-300 8-90

20-48 45-100 (63)

(5.7) 2 (2) -

1-6 (2.5) 1 (1) -

Intensity range (mean intensity) 1 1-10 2 (2) 3-22 1-22

Moravec 1963 Markov et al. 1969 Vakker 1970 Markov et al. 1972 Velikanov 1982 Biserkov 1995 Bakiev & Kirillov 2000, Kirillov 2000 Bakiev & Kirillov 2007 Mihalca et al. 2007b Yildirimhan et al. 2007

Yildirimhan et al. 2007 Markov et al. 1962 Sharpilo 1976, Sprent 1978, Baker 1987 Sharpilo 1976 Markov et al. 1962 Markov et al. 1969 Sharpilo 1976, Baker 1987 Baker 1987 Vakker 1970 Velikanov 1982 Velikanov 1982 Rudolphi 1819, Linstow 1878; Boulenger 1913, Fuhn & Vancea 1961, Baker 1987 Dubinina 1953 Ivanov 1954 Sharpilo 1959a Markov et al. 1962

Dubinin 1952 Dubinina 1953 Biserkov 1995 Sharpilo 1964 Kirin 2002 Mihalca et al. 2007a Mihalca et al. 2007b Mihalca 2007

Reference

Tab. 5. Nematoda reported in Natrix tessellata (continued)

Hexametra quadricornis

Location in host

Species

Review of Parasitism in Natrix tessellata

265

266

Abdushukurova et al. 1966 Markov et al. 1969 Velikanov 1982 Biserkov 1995 Sharpilo 1974, Sharpilo 1976 Velikanov 1982 Sharpilo 1976 Strongyloides mirzai

* Larval stages 1 Validity of the genus is questionable, as only larval stages are known 2 Probably misidentification 3 Probably pseudoparasites (see text for details)

Streptocara crassicauda*

Spiroxys contortus*

2 (2) 6 (6) 3 (3) 2.2 12.5 3 Tashkentskaya, Uzbekistan Volgogradskaya, Russia Turkmenistan Bulgaria Ukraine Turkmenistan Azerbaijan

Markov & Bogdanov 1965 Vakker 1970 Sharpilo 1976 Chu-Iliyskoye, Kazakhstan Kazakhstan Russia

serosa of intestine and internal organs stomach, intestine wall stomach, intestine wall, body cavity, muscles, lungs, liver, subcutaneous liver subcutaneous, serosa of internal organs intestine stomach, intestine wall, body cavity intestine Spirocerca lupi*

Prevalence (%) Intensity range (mean intensity) 11.1 4-12 6.5 Geographic data Location in host Species

Tab. 5. Nematoda reported in Natrix tessellata (continued)

Reference

Andrei Daniel Mihalca

tenic hosts. Nematodes of the genus Spiroxys are parasitic in chelonians. Intermediate hosts are copepods but also many paratenic hosts have been reported, including invertebrates, fish, amphibians and other reptiles (Anderson 2000). As in the case of other nematodes, in the absence of experimental trials, we can only assume that snakes are infected after preying on infected fish or anurans. Genus Streptocara includes cosmopolitan parasites of waterfowl. Amphipod crustaceans are intermediate hosts and fish are paratenic hosts (Anderson 2000). Snakes acquire the parasite by ingesting infected paratenic fish hosts. Genus Agamospirura is known only by larval stages. Adults were never found, so its validity is questionable (Chubb 1980). Three genera of larval nematodes from the order Ascaridida have been described from snakes (Anisakis, Contracaecum and Porrocaecum). Definitive hosts for Anisakis are marine mammals (pinnipeds and cetaceans) but larval forms have been found parasitic in different tissues of many metazoans, both invertebrates and vertebrates. Most common intermediate hosts are marine invertebrates, but a great variety of fish species serve as intermediate or paratenic hosts (Anderson 2000). Dice snakes acquire the parasites after feeding on infected fish. Larvae of Contracaecum have been found encysted in the stomach wall of dice snakes from Ukraine (Sharpilo 1964). Adults of these nematodes are parasitic in the stomach of piscivorous birds and mammals (Anderson 2000). Snakes are accidental hosts and are infected from various species of fish. Adults of Porrocaecum are parasites of birds. Earthworms are first intermediate hosts (Anderson 2000), so snake contamination is likely to be associated with paratenic anurans. Very common findings in piscivorous snakes are larvae of Eustrongylides (Dioctophymatidae) (Mihalca 2006). Adults are parasitic in piscivorous birds and snakes are infected by eating fish (Sloboda et al. 2010). They proved that natural infection of snakes with larval Eustrongylides excisus occurred after consumption of infected Gobiidae fish. Larvae from snakes (Fig. 5) were identified as fourth stage larvae of this parasitic nematode (Mihalca et al. 2006). Arthropoda Despite of many parasitological studies in dice snakes, arthropods are rarely reported (Tab. 6). The only ectoparasitic arthropoda found on dice snakes was Ophionyssus natricis (Fig. 6), a generalist mite associated with various snake species. Pathogenic Effect of Parasites on Dice Snakes Few studies are available on the effect of parasites on N. tessellata. Moreover, all these data refer to free-ranging dice snakes, while results from captive snakes are ab-

Review of Parasitism in Natrix tessellata

Tab. 6. Arthropoda reported in Natrix tessellata Species Ophionyssus natricis

Location Geographic data in host

Prevalence (%)

skin skin skin skin skin

20 100 1.1 -

Astrakhanskaya, Russia Tashkentskaya, Uzbekistan Kazakhstan Germany Russia

Intensity range (mean intensity) 25-160 -

Reference Markov et al. 1964 Abdushukurova et al. 1966 Vakker 1970 Lanka 1975 Bakiev 2007

sent. Nevertheless, this snake species is not a common terrarium species. In 1961, Darevskiy, during a zoological field investigation in a mountain steppe zone in Armenia, noticed that most dice snakes had their dorsal area of tail abnormally thickened and sometimes abruptly shortened, ending with a fresh scar. Enlarged hypodermic cellular tissue as well as fat and muscle tissues of tails were filled with a large number of larval trematodes of the genus Alaria. During the dissection of some snakes the same

larval forms were found encysted in fat deposits of the snakes. Engelmann (1970) showed that heavy infection with Ophiotaenia europaea in dice snakes can be fatal for the host. The effect of infection with larval Eustrongylides excisus on N. tessellata was extensively studied in the Histria ruins, Romania (Mihalca 2007, Mihalca et al. 2007a). The most evident sign of infection was the presence of subcutaneous nodules visible in the dorsal area (Fig. 7), mainly in the middle third of the body. Size of

Fig. 6. The parasitic mite Ophionyssus natricis.

Fig. 8. Muscular rupture caused by fourth stage larva of Eustrongylides excisus in Natrix tessellata.

Fig. 7. Massive infection of Natrix tessellata with fourth stage larvae of Eustrongylides excisus. Note the presence of subcutaneous nodules.

Fig. 9. Pulmonar rupture caused by fourth stage larva of Eustrongylides excisus in Natrix tessellata.

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nodules was variable, with a maximum diameter of 9 mm. Each of these nodules contained dead or living parasites. Large nodules often contained 2 or 3 coiled larvae. A severe clinical sign noticed in individual dice snakes was paralysis of variable degree (Carlsson pers. obs.). Of the 24 paralyzed snakes, 62.5 % had visible larval nodules under the skin (Mihalca 2007). In some paralyzed snakes, the prolapsed hemipenis showed noticeable erosions and necrosis of the mucosa. Gross lesions associated with larval eustrongylidosis consisted of muscular (Fig. 8) and pulmonary (Fig. 9) ruptures, haematomas and granulomas in different tissues (Mihalca 2007). Histological sections revealed nematode larvae surrounded by a capsule, forming a parasitic granuloma with 3 layers: macrophage layer, lymphocyte layer, and fibrous capsule (Mihalca et al. 2007a). Verminous pneumonia in N. tessellata was reported by Zwart & Jansen (1969). They treated the snakes with intraperitoneal injections of Ripercol (tetramisole), applying a dosage of 10 mg/kg, and antibiotic therapy (oxytetracycline) orally once a day for two weeks. Aknowledgements The author is indebted to K. Mebert for all valuable advices during the preparation of this manuscript. Tremendous work has been done by A. Bakiev and A. Kirillov in providing me English translations of all Russian literature on the subject. Thanks also to P. Nikolov for providing Bulgarian reprints. Valuable advices during my early career were and are still kindly provided by D. Modrý and V. Cozma. Thanks also to the team of Histria field work during 2005–2007 (I. Ghira, M. Carlsson, M. Sloboda, S. Karvemo, L. Bel and B. Ferşedi). References Abdushukurova, R.U., Markov, G.S. & O.P. Bogdanov (1966): K parasitofaune vodyanogo uzha (On the parasite fauna of dice snakes). – Posvonochnyie zhivotnyie Sredney Asii, Tashkent: 215–220 (in Russian). Anderson, R.C. (2000): Nematode parasites of vertebrates: their development and transmission. – Second Edition, CAB International. Baker, M.R. (1987): Synopsis of the nematoda parasitic in amphibians and reptiles. – Memorial University of Newfoundland, Occasional Papers in Biology no. 11. Bakiev, A.G. (2004): Parasity i hizshiki (Parasites and predators). – Zmeyi Volzhsko-Kamskogo kraya, Proceedings of the Samara Scientific Centre of RAS, Samara: 96–108 (in Russian). Bakiev, A.G. (2007): Osnovnyie itogi isucheniya parasitov zmey Volzhskogo basseyna. Soobszhenie 2. Parasitiformnyie kleszhi (Basic results of parasite study in snakes from Volga River Basin. Report 2 Parasitimorphous ticks). – Proceedings of the Mordovia University, Biological Sciences 4: 69–72 (in Russian). Bakiev, A.G. & A.A. Kirillov (2000): Pitanie i helminthofauna sovmestno obitayuzhih v Srednem Povolzhye zmey Natrix natrix i N. tessellata (Colubridae) (Diet and helminthofauna of

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Natrix natrix and N. tessellata (Colubridae) co-inhabiting the middle Volga Region). – Proceedings of the Samara Scientific Centre of RAS 22(4): 330–333 (in Russian). Bakiev, A.G. & A.A. Kirillov (2007): Osnovnyie itogi isucheniya parasitov zmey Volzhskogo basseyna. Soobszhenie 1. Prosteyzhie i helminti (Basic results of parasite studies in snakes from Volga River Basin. Report 1. Protozoa and helminths) – Proceedings of the Mordovia University, Biological Sciences 4: 60–69 (in Russian). Barnard, S.M. & S.J. Upton (1994): A veterinary guide to the parasites of reptiles. – Volume 1. Protozoa – Krieger Publishing Company, Malabar, Florida. Biserkov, V. (1989): Helminti na vlechugite ot razred Squamata v Bylgarija – faunistichni, morfologichni i biologichni izsledvanija (Helminths of the Reptiles from the Order Squamata in Bulgaria – Fauna, Morphology and Biology) – Ph.D. dissertation, Sofia (in Bulgarian). Biserkov, V. (1996): New records of Nematodes and Acanthocephalans from snakes in Bulgaria. – Comptes rendus de l’Academie Bulgare des Sciences 49(1): 76–78. Biserkov, V. & T. Genov (1988): (On the life cycle of Ophiotaenia europaea Odening, 1963 (Cestoda: Ophiotaeniidae)). – Khelmintologia 25: 7–14 (in Bulgarian). Biserkov, V. & A. Kostadinova (1997): Development of the plerocercoid I of Ophiotanenia europaea in reptiles – International Journal for Parasitology 27(12): 1513–1516. Bogdanov, O.P. (1954): О zarazhenii vodyanogo uzha Ophidascaris natricis Jamaguti, 1935. (About an invasion into dice snakes by Ophidascaris natricis Jamaguti, 1935) – Proceedings of the Institute of Zoology and Parasitology, Tashkent, Parasitological Collection 3: 81–83 (in Russian). Boulenger, G.A. (1913): The snakes of Europe. – Methusen & Co. Ltd, London. Brauer, A. (1911): Acanthocephalen. Register der Acanthocephalen und parasitischen Plattwürmer, geordnet nach ihren Wirten, Heft 16 – In: Lühe, M. (Ed.): Süsswasserfauna Deutschlands. Eine Exkursionsfauna. – Verlag Von Gustav Fischer, Jena. Bray, R.A., Jones, A. & K.I. Andersen (1994): Order Pseudophyllidea. – In: Khalil, L.F., Jones A. & R.A. Bray (Eds.): Keys to the Cestode Parasites of Vertebrates. – CAB International. Căpuşe, I. (1971): Contributions a l’etude des trematodes parasites chez les reptiles du Roumanie – Travaux du Museum d’histoire Naturelle “Grigore Antipa” 11: 33–40. Chubb, J.C. (1980): Seasonal occurrence of helminths in freshwater fishes. Part III. Larval cestoda and nematoda – Advances in Parasitology 18: 2–175. Dabrowolskij, A.A. (1969): (The life cycle of Paralepoderma cloacicola Lühe, 1909) – Vest. Leningr. Gos. Univ., Ser. Biol. 9(2): 28–38 (in Russian). Darevskiy, I.S. (1961): Interesnyiy sluchay zarazheniya vodyanogo uzha lichinkami trematod (An interesting case of invasion in dice snake by larval trematodes) – Proceedings of the Academy of Sciences of Armenian SSR. – Biological Sciences 14(1): 99–101 (in Russian). Dubinin, V.B. (1949): Eksperimentalnyie issledovaniya nad ciklami rasvitiya nekotoryih parasiticheskih chervey delti Volgi (Experimental studies of life cycles of some parasitic worms in the Volga River Delta) – Parasitological Collection of the Zoological Institute of the Academy of Sciences of USSR 11: 126–160 (in Russian). Dubinin, V.B. (1952): Fauna lichinok parasiticheskih chervey posvonochnih zhivotnih delti reki Volgi (Fauna of parasitic

Review of Parasitism in Natrix tessellata larvae of vertebrates from the Volga River Delta) – Parasitological Collection of the Zoological Institute of the Academy of Sciences of USSR 14: 213–265 (in Russian). Dubinina, M.N. (1950): Ekologicheskoye issledovaniye parasitofauni ozernoy lyagushki (Rana ridibunda Pall.) delti Volgi (Ecological study of the parasite fauna of the frog (Rana ridibunda) Pall. from the Volga Delta) – Parasitological Collection of the Zoological Institute of the Academy of Sciences of USSR 12: 300–351 (in Russian). Dubinina, М.N. (1951): O biologii i rasprostranenii Diphyllobothrium erinacei-europaei (Rud., 1819) Iwata, 1933 (About the biology and spreading of Diphyllobothrium erinacei-europaei (Rud., 1819) Iwata, 1933) – Zool. Zh. 30(5): 421–429 (in Russian). Dubinina, М.N. (1953): Dinamika parasitofauni uzhey primorskoy chasti delti Volgi (Dynamics of the parasite fauna of dice snakes in the seaside part of the Volga Delta). – Proceedings of the Zoological Institute of the Academy of Sciences of the USSR 13: 171–190 (in Russian). Engelmann, W.E. (1970): Bandwürmer als Parasiten bei Schlangen (Tapeworms as parasites of snakes). – Aquarium und Terrarium 17: 280 (in German). Evlanov, I.A., Kirillov, A.A., Bakiev, A.G. & A.L. Malenev (1996): Katalog parasiticheskih chervey presmyikayuzshihsya basseyna Volgi (Catalogue of parasitic worms of reptiles from the Volga Basin) – Actual problems of herpetology and toxicology. – Scientific Proceedings Collection 2: 67–72 (in Russian). Evlanov, I.A., Kirillov, A.A., Chihlyaev, I.V., Guzova, N.Y. & L.V. Zhilchova (2001): Parasiti posvonochnih zhivotnih Samarskoy oblasti. Chast 1. Systematicheskiy catalog (Parasites of Vertebrates of the Samarskaya Region. Part 1. Systematic Catalogue) – Institute of Ecology of Volga River Basin of RAS Publishing House, Togliatti: 1–75 (in Russian). Evlanov, I.A., Kirillov, A.A., Chihlyaev, I.V., Guzova, N.Y. & L.V. Zhilchova (2002): Parasiti posvonochnih zhivotnih Samarskoy oblasti. Chast 2: Raspredelenie parasitov po vidam hosyaev (Parasites of vertebrates of Samarskaya Region. Part 2. Distribution of Parasites among Hosts). – Institute of Ecology of Volga River Basin of RAS Publishing House, Togliatti: 1–20 (in Russian). Filippi, E., Capula, M., Luiselli, L. & U. Agrimi (1996): The prey spectrum of Natrix natrix (Linnaeus, 1758) and Natrix tessellata (Laurenti, 1768) in sympatric populations (Squamata: Serpentes: Colubridae). – Herpetozoa 8(3-4): 155–164. Frese, V.I. (1965): Proteocephalyati – lentochnie helminti rib, amphibiy i reptiliy. Osnovy cestodologii. Vol. 5 (Proteocephalata – Helminths of Fish, Amphibians and Reptiles. Cestodes, vol. 5) – Nauka, Moscow (in Russian). Fuhn, I.E. & Ş. Vancea (1961): Fauna Republicii Populare Române. Volumul XIV. Fascicula 2. Reptilia (Fauna of the People’s Republic of Romania. Volume XIV. Tome 2. Reptilia). – Publishing House of the Academy of the People’s Republic of Romania, Bucharest (in Romanian). Gofman-Kadoshnikov, P.B., Chizhova, T.P. & A.S. Artamoshin (1968): (Anatomo-histological structure and biology of plerocercoids of Diphyllobothrium erinacei (Rud. 1819) Iwata 1933). – Proceedings of the Astrakhan Preserve 11: 97–113 (in Russian). Hromada, M., Dudiòák, V. & R. Yosef (2000): An inside-out perspective of the true shrikes. A review of the helminthofauna. – The Ring 22(1): 185–204. Işfan, T. (1965): Contribuţii la studiul paraziţilor intestinali la Natrix tesselatus (Contributions to the study of the helminths of Natrix tesselatus). – Studii şi cercetări biologice, Seria zoologie 17(5): 415–423 (in Romanian).

Ivanov, A.S. (1952): Parasiticheskie chervil reptiliy delti Volgi (Sosalszhiki) (Parasitic worms of reptiles of the Volga Delta (Flat worms)). – Proceedings of the Astrakhan Pedagogical Institute 10: 325–330 (in Russian). Ivanov, A.S. (1954): Parasiticheskie chervil reptiliy delti Volgi (Kruglie chervi) (Parasitic worms of reptiles of the Volga Delta (Round worms)). – Proceedings of the Astrakhan Pedagogical Institute 11: 458–465 (in Russian). Ivanov, V.М. & N.N. Semyenova (2000): Vidovoy sostav I ekologicheskie osobennosti trematod reptiliy delti Volgi (The species composition and ecological characteristics of trematodes from reptiles in the Volga delta). – Parazitologiia 34(3): 228– 233 (in Russian). Kennedy, C.R. (2006): Ecology of the Acanthocephala. – Cambridge University Press. Kirillov, A.A. (2000) Fauna helmintov reptiliy Samarskoy oblasti (Helminth fauna of reptiles from Samarskaya Region). – Proceedings of the Samara Scientific Centre of RAS 2(4): 324–329 (in Russian). Kirillov, A.A. (2002): Helminti prersmikayuszhihsya Srednego Povolzhya (fauna, ekologiya, bioindikaciya) (Helminths of reptiles of Middle Volga Region (fauna, ecology, bioindication)). – Dissertation abstract for a Ph.D. in biology, Moscow: 1–19 (in Russian). Kirillov, A.A. (2006): Ekologo-faunisticheskiy analis helmintov ophidiofauni Srednego Povolzhya (Ecological and faunistic analysis of helminths of snake fauna from Middle Volga Region). – Actual problems of Herpetology and Toxicology, Scientific Proceedings Collections 9: 74–81 (in Russian). Kirillov, A.A., Chihlyaev, I.V. & I.A. Evlanov (2001): Issledovaniya helmintov amphibiy i reptiliy v Samarskoy oblasti (Study of helminths parasitic in amphibians and reptiles Samarskaya Region). – Samarskiy side in Russian history, Papers of the Scientific Conference in Samara: 278–281 (in Russian). Kirillov, A.A. & I.A. Evlanov (1999): Harakteristika helmintofauni obiknovennogo i vodyanogo uzhey Samarskoy Luki (Characteristics of helminth fauna of grass and dice snakes from the Samarskaya Luka Peninsula). – Samarskaya Luka on the Threshold of the 3rd Millenium, Togliatti: 204–205 (in Russian). Kirillov, A.A. & N.Y. Kirillova (2007): Parasitirovanie u reptiliy Samarskoy oblasti helmintov, svoystvennim drugim zhivotnim (Helminths specific for other animals as parasites of reptiles). –Actual problems of herpetology and toxicology, Scientific Proceedings Collection 10: 70–72 (in Russian). Kirin, D. (1994) (Contribution to the trematode fauna of the water snake Natrix tessellata (Laur., 1768) (Reptilia, Colubridae) in Bulgaria). – Scientific Works of the University of Plovdiv “Paisii Hilendarski”, Biology 30(6): 35–39 (in Bulgarian). Kirin, D. (1996a): (Helminths (class Trematoda, class Monogenea) on reptiles (Reptilia) from different habitats of South Bulgaria). – Scientific Works of the University of Plovdiv “Paisii Hilendarski”, Biology, 32(6): 5–11 (in Bulgarian). Kirin, D. (1996b.) (Platyhelminth Parasites from Reptiles in South Bulgaria – Morphology, Fauna, Ecology and Distribution)). – Ph.D. dissertation, University of Plovdiv (in Bulgarian). Kirin, D. (2002): New records of the helminth fauna of grass gnake, Natrix natrix L., 1758 and dice snake, Natrix tessellata Laurenti, 1768 (Colubridae: Reptilia) in South Bulgaria. – Acta Zoologica Bulgarica 54(1): 49–53. Lanka, V. (1978): Variabilität und Biologie der Würfelnatter (Natrix tessellata). – Acta Universitatis Carolinae, Biologica 1975– 1976: 167–207.

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Andrei Daniel Mihalca Linstow, O. von (1978): Compendium der Helminthologie. – Hahsche Buchhandlung, Hannover. Luiselli, L., Capizzi, D., Filippi, E., Anibaldi, C., Rugiero, L. & M. Capula (2007): Comparative diets of three populations of an aquatic snakes (Natrix tessellata, Colubridae) from Mediterranean streams with different hydric regimes. – Copeia 2007: 426–435. Markov, G.S. & O.P. Bogdanov (1960): Helminti i kleszhi - parasiti zmey Sredney Asii (Helminths and ticks – parasites of snakes in Middle Asia). – Uzbekhistan Biological Zh. 2: 35–41 (in Russian). Markov, G.S. & O.P. Bogdanov (1965): Noviye danniye po parasitologii zmey Sredney Asii i Kasahstana (New data on parasitology of snakes in Middle Asia and Kazakhstan). – Herpetology, Tashkent: 79–90 (in Russian). Markov, G.S., Honyakina, Z.P. & I.N. Grigoryeva (1972): Materiali po helmintofaune yaszherizh i zmey Dagestana (Papers on helminthology of lizards and snakes in Dagestan). – Studies on zoology and parasitology in Dagestan, Mahachkala: 29–61 (in Russian). Markov, G.S., Ivanov, V.P., Kryuchkov, B.P., Lukyanova, Z.F., Nikulin, V.P. & V.F. Chernobay (1964): Prosteyshie i kleszhi – parasiti presmikayuszhihsya Pricaspiya (Protozoa and ticks – parasites of reptiles of Caspian Sea County). – Scientific Articles of the Volgograd State Pedagogical Institute 16: 90–98 (in Russian). Markov, G.S., Ivanov, V.P., Nikulin, V.P. & V.F. Chernobay (1962): Helminthofauna presmikayuszhihsya delti Volgi i pricaspiyskih stepey (Helminthofauna of reptiles in the Volga Delta and steppes of the Caspian Sea County) – Proceedings of the Astrakhan Preserve 6: 145–172 (in Russian). Markov, G.S., Kosareva, N.A. & B.S. Kubantsev (1969): Materiali po ekologii i parasitologii yaszherizh i zmey v Volgogradskoy oblasti (Papers on ecology and parasitology of lizards and snakes in the Volgograd Region). – Parasitic Animals, Volgograd: 198–220 (in Russian). Mihalca, A.D. (2006): Eustrongylides infection in reptiles. A review of literature with new host and geographical records. – Lucrări ştiinţifice medicină veterinară, Timişioara 39: 37–40. Mihalca, A.D. (2007): Fauna parazitară la ţestoasa de apă europeană (Emys orbicularis), şopârla de câmp (Lacerta agilis) şi şarpele de casă (Natrix natrix) din fauna spontană a României (Parasitic Fauna of Free-ranging European Pond Turtle (Emys orbicularis), Sand Lizard (Lacerta agilis) and Grass Snake (Natrix natrix) in Romania). – Ph.D. dissertation, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca, Romania (in Romanian). Mihalca, A.D., Fictum, P., Škorič, M., Sloboda, M., Kärvemo, S., Ghira, I., Carlsson, M. & D. Modrý (2007a): Severe granulomatous lesions in several organs from Eustrongylides larvae in a free-ranging dice snake, Natrix tessellata. – Veterinary Pathology 44: 103–105. Mihalca, A.D., Gherman, C., Ghira, I. & V. Cozma (2007b): Helminth parasites of reptiles (Reptilia) in Romania – Parasitology Research 101(2): 491–492. Mihalca, A.D., Sloboda, M., Ghira, I., Modrý, D., Gherman, C. & V. Cozma (2006): Aspecte electronomicroscopice ale larvelor de stadiul 4 de Eustrongylides sp. parazite la şerpi de apă (Natrix tessellata) (SEM aspects of forth stage larvae of Eustrongylides sp. from dice snakes (Natrix tessellata)). – Revista Scientia Parasitologica 7(1–2): 109–111 (in Romanian). Moravec, F. (1963): (The recognition of the helminth fauna of our reptiles). – Publications de la Faculte des Sciences de l’Universite J.E.Purkyne, Brno 8(446): 353–396 (in Czech).

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Niewiadomska, K. (2002): Superfamily Diplostomoidea Poirier, 1886. – In: Gibson, D.I., Jones, A. & R.A. Bray (Eds.): Keys to Trematoda, vol. 1. – CAB International. Odening, K. (1963): Zum systematischen Status und zur Verbreitung der in Europäischen Schlangen schmarotzenden Proteocephalidae (Cestoidea: Proteocephala) nebst Bemerkungen zur Gattungszugehörigkeit einer madegassischen Proteocehalidaeart aus Schlangen. – Zeitschrift fur Parasitenkunde 23: 226–234. Ovezmukhammedov, A. (1987): Protistofauna reptiliy (Protozoa Fauna of Reptiles). – Ilyim Ashhabad (in Russian). Ovezmukhammedov, A. (1991): Leyshmanii reptiliy (Leishmanias of Reptiles). – Ilyim Ashhabad (in Russian). Pearson, J. (2008): Family Heterophyidae. – In: Bray, R.A., Gibson, D.I. & A. Jones (Eds.): Keys to Trematoda, vol. 3. – CAB International. Rausch, R.L. (1994): Family Mesocestoididae. – In: Khalil, L.F., Jones, A. & R.A. Bray (Eds.): Keys to the Cestode Parasites of Vertebrates. – CAB International. Rego, A.A. (1994): Order Proteocephalidea. – In: Khalil, L.F., Jones, A. & R.A. Bray (Eds.): Keys to the Cestode Parasites of Vertebrates. – CAB International. Rudolphi, C.A. (1819): Entozoorum Synopsis. – Berolini Subtibus Augusti Rücker. Ryzhenko, G.F. (1968): K voprosu o definitivnyih chosyaevah Spirometra erinacei-europaei (On questions about definitive hosts of Spirometra erinacei-europaei). – Bulletin of the AllUnion Helmintology Institute of K.I. Skryabin 2: 89–91 (in Russian). Ryzhenko, G.F. (1969): Biologiya i morphologiya Spirometra erinacei-europaei (Rudolphi, 1819) – vosbuditelya spirometrosa i sparganumosa zhivotnih i cheloveka (Biology and morphology of Spirometra erinacei-europaei (Rudolphi, 1819) – pathogenesis of spirometrosis and sparganosis of animals and man) – Ph.D. dissertation abstract, Moscow: 1–24 (in Russian). Sharpilo, V.P. (1959a): K posnaniyu helmintofauni nekotorih reptiliy USSR (Study of helminth fauna of some reptiles in Ukrainian SSR) – Proceeding of the Helminthological Laboratory of the Academy of Sciences of the USSR 9: 370–376 (in Russian). Sharpilo, V.P. (1959b): K posnaniyu helmintofauni uzhey USSR (Study of helminth fauna of grass and diced snakes in Ukrainian SSR). – Questions of Ecology: Papers of the Third Ecological Conference, Vol. 3, Univers. Publish., Kiev: 232–239 (in Russian). Sharpilo, V.P. (1964): Lichinochniye formi nematod – parasiti reptiliy funi Ukrainskoy SSR (Larval forms of nematodes parasitic in reptiles of Ukrainian SSR fauna) – Problems of Parasitology. – Proceeding of the Ukrainian Scientific Parasitological Society 3: 112–124 (in Russian). Sharpilo, V.P. (1976): Parasiticheskie chervil presmikayuszhihsya fauni SSSR (Parasitic Worms of Reptiles of the USSR fauna). – Naukova Dumka Publish., Kiev (in Russian). Sloboda, M., Mihalca, A.D., Falka, I., Petrželková, K.J., Carlsson, M., Ghira, I. & D. Modrý (2010): Are gobiid fish more susceptible to predation if parasitized by Eustrongylides excisus? An answer from robbed snakes. – Ecology Research 25: 469–473. Sprent, J.F.A. (1978): Ascaridoid nematodes of amphibians and reptiles: Polydelphis, Travassosascaris n.g. and Hexametra. – Journal of Helminthology 52: 355–384. Sudarikov, V.E. (1960): K biologii trematod Strigea strigis (Schrank, 1788) i S. sphaerula (Rud., 1803) (On the biology of trematodes Strigea strigis (Schrank, 1788) and S. sphaerula

Review of Parasitism in Natrix tessellata (Rud., 1803)). – Proceeding of the Helminthological Laboratory of the Academy of Sciences of the USSR 10: 217–226 (in Russian). Sudarikov, V.E. (1962): Fauna mesocercariev i metacercariev trematod otryada Strigeidida (La Rue, 1926) amphibiy i reptiliy delti Volgi (Mesocercaria and metacercaria fauna of the order Strigeidida (La Rue, 1926) of amphibians and reptiles in the Volga Delta). – Proceedings of the Astrakhan Preserve 6: 181–196 (in Russian). Sudarikov, V.E., Lomakin, V.V. & N.N. Semyenova (1991): Trematoda Pharyngostomum cordatum (Alariidae, Hall et Wigdor, 1918) i yeye zhisnenniy cicl v usloviyah delti Volgi (Trematoda Pharyngostomum cordatum (Alariidae, Hall et Wigdor, 1918) and its life cycle in conditions of theVolga Delta). – Helminths of animals, Nauka Publish., Moscow: 142–147 (in Russian). Telford, S.R. Jr. (2009). Hemoparasites of the Reptilia: Color Atlas and Text. – CRC Press, Taylor & Francis Group, Boca Raton, Florida. Tomova, C. & V. Golemansky (2001): Protozoan parasites of amphibians (Amphibia:Anura) and reptiles (Reptilia:Squamata) from Bulgaria. – Acta Zoologica Bulgarica 53(1): 41–46.

Vakker, V.G. (1970): Parasitofauna reptiliy yuga Kasahstana i ih rol v circulacii nekotorih helmintov cheloveka i zhivotnih (Parasite fauna of reptiles of South Kazakhstan and its role in circulation of some helminths of man and animals. – Autosynopsis of Ph.D. dissertation in biology, Alma-Ata (in Russian). Velikanov, V.P. (1982): (Helminth fauna of the snake Natrix tessellata in the Turkmen SSR). – Izvestiya Akademii Nauk Turkmenskoi SSR Seriva Bioiogicheskikh Nauk 1: 46–50 (in Russian). Velikanov, V.P. & V.P. Sharpilo (2002): (On the rare and locally distributed palaerctic species of the reptile parasitic worms: Allopharynx amudariensis (Trematoda, Plagiorchiidae)). – Vestnik Zoologii 36: 65–68 (in Russian). Yildirimhan, H.S., Bursey, C.R. & S.R. Goldberg (2007): Helminth parasites of the grass snake, Natrix natrix, and the dice snake, Natrix tessellata (Serpentes: Colubridae) from Turkey. – Comparative Parasitology 74(2): 343–354. Zwart, P. & J. Jr. Jansen (1969): Treatment of lungworm in snakes with tetramisole. – Veterinary Record 84(14): 374.

Author Andrei Daniel Mihalca, Faculty of Veterinary Medicine, Cluj-Napoca, Calea Mănăştur 3-5, Cluj-Napoca, 400372 Romania, e-mail: [email protected].

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ISBN 978-3-9812565-4-3

Distribution, Habitat Preferences and Conservation of the Dice Snake (Natrix tessellata) in Romania Alexandru Strugariu, Iulian Gherghel, Ioan Ghira, Severus D. Covaciu-Marcov & Konrad Mebert Abstract. In Romania, the dice snake (Natrix tessellata) has been, until recently omitted from any specific studies and its national distribution and ecology is only known from accounts in numerous dispersed papers which discuss the general distribution of the herpetofauna in several regions. Here we aim to present an updated review of the historical and current distribution, habitat preferences, and the current conservation status of the dice snake in Romania. The species is widespread in western Romania, in the interior and to the west of the Carpathian Basin (Transylvania) where it inhabits large rivers, fish farms and thermal aquatic habitats. In southwestern Romania, the species is common along the main rivers (Danube, Cerna, Jiu). In southern Romania it has been recorded in several habitats (mostly in natural ponds located in deciduous forests and in a few habitats along the Danube). In eastern Romania (Moldavia), the species has been recorded from five localities in the past century. Despite numerous recent surveys, only three populations were recently confirmed to have survived. In the southeastern part of the country (Dobrudja), it is also a common species in brackish lakes, lagoons, and fish farms. Based on the total number of localities in which the species has been recorded and the number of recently confirmed localities, we propose a status of vulnerable (VU) for Natrix tesellata in Romania. Key words. Squamata, Natrix tessellata, altitudinal distribution, anthropogenic factors, extinct population, thermal habitats, vulnerable species

Introduction The dice snake, Natrix tessellata (Laurenti 1768) is one of the most widespread palearctic reptile species, inhabiting parts of central, southern and south-eastern Europe, the Near East and east into Afghanistan and China (Gasc et al. 1997, Gruschwitz et al 1999). The dice snake is one of three semi-aquatic snake species of the genus Natrix. It is morphologically and ecologically more similar to the viperine snake, Natrix maura, but phylogenetically closer to the grass snake, Natrix natrix (Guicking et al. 2006, Joger et al. 2007). While at many localities N. tessellata is sympatric with N. natrix, it occurs in sympatry with N. maura only in a restricted region in northern Italy (Scali 2011), and replaces it in much of central and in Eastern Europe (Joger et al. 2007). The restricted zones of overlap approach those of ecologically similar European vipers (e.g. Vipera aspis and V. ammodytes) and colubrine snakes (e.g. Hierophis gemonensis and H. viridiflavus) (e.g. Gasc et al. 1997). Natrix tessellata is more associated to an aquatic habitat than N. natrix (e.g. Ioannidis & Mebert 2011, Janev Hutinec & Mebert 2011). In Romania, it is usually found in aquatic bodies or in the immediate vicinity of these, and very rarely at great distances from these habitats (Fuhn & Vancea 1961). The species feeds mostly on fish but also, to a lesser degree, on adult frogs, tadpoles and newts (Fuhn & Vancea 1961, Filippi et al. 1996, Luiselli 2006). Despite its wide range, most European dice snake populations present a low genetic diversity due to recent colonization from populations farther south (Jo-

ger et al. 2007, Guicking et al. 2009, Guicking & Joger 2011). As low genetic diversity can lead to a decrease of its adaptive potential or increase of inbreeding (e.g. Frankham 2005), characteristics that together with numerous anthropogenic factors could require a conservation status of a higher vulnerability for many if not the majority of European dice snake populations. The first step in assessing the conservation status of species and realizing a proper management plan for its protection is to acquire a detailed knowledge of the species’ distribution and preferred habitats (e.g. Ghira et al. 2002, Sas et al. 2008a). In Romania, prior 2000, this was very difficult to be performed due to the fact that little effort has been put into the study of its herpetofauna. Until today, the most complete overview of the distribution of Romanian reptiles remains the monograph published by Fuhn & Vancea (1961). Since its publication, no proper attempts to update the distribution of reptile species in Romania have been made. However, since 2000, numerous field surveys have been performed in most regions of Romania, that significantly contributed to the knowledge of the distribution of the reptilian species, bringing numerous new records for almost all reptiles known to occur in the country, including N. tessellata (e.g. Covaciu-Marcov et al. 2005a, b, 2006a, c, 2007a, b, 2008a, b, 2009, Ghira et al. 2002, Ghiurcă et al. 2005, 2006, Strugariu et al. 2006a, b, 2007, 2008a, b, c, Strugariu & Gherghel 2008, Gherghel et al. 2008). Little was known of Romanian reptiles until recently, being limited to anecdotal observations presented in faunistical studies, including for the dice snake.

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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In Romania, the dice snake is considered to be a relatively widespread and common species in most regions of the country (Fuhn & Vancea 1961, Fuhn 1969, Iftime 2005a). The “Romanian Red Data Book of Vertebrates” classifies the species as near threatened (Iftime 2005a). This status was probably given as a consequence of the relatively wide range of the species in Romania, and because of this, the data are rather few compared to the potentially suitable habitat. Since no or few data on population sizes or other biological aspects were available, aside from a long term study currently conducted in Histria near the Black Sea coast (e.g. Carlsson et al. 2011, Kärvemo et al. 2011), Iftime did not take into account that a significant part of the total records are very old and not confirmed by recent surveys. The aim of the present study is to review all available data on the distribution and habitat preferences of the dice snake in Romania, and discuss its current conservation status in the country. Material and Methods The present review contains data from the literature, unpublished observations of the authors and other herpetologists. Based on these data, we compiled an updated list of localities in Romania from where N. tessellata has been recorded. Only records referring to precise localities or unambiguous precise geographic areas were considered for this study. For example, records referring to entire rivers, river basins, and mountain ranges were not included. The range of the dice snake in Romania was divided, according to the natural geographic areas and col-

lecting gaps into five regions (Fig. 1): Transylvania (the western slopes of the eastern Carpathians, the northern slopes of the southern Carpathians, the northern group of the western Carpathians, the Transylvanian Plateau, the western Hills and western Plains), southwestern Romania (mostly the southern group of the western Carpathians and the western slopes of the southern Carpathians), Romanian Moldavia (from the eastern slopes of the eastern Carpathians to the Prut River), southern Romania (from the southern slopes of the southern Carpathians to the Danube river) and Dobrudja (southeastern Romania). Descriptive statistics of the altitudinal distribution were also calculated for these groups. Since the altitudinal data presented a non-normal distribution, we used non-parametric tests (Kruskal-Wallis ANOVA and Mann-Whitney U test) for the statistical comparison. Statistica 6.0 for Windows and XLStat Pro software were used for all statistical procedures. Taking into consideration the rapid landscape alterations which have taken place in Romania since 1989 (i.e. fall of the communism), we divided the available records of the dice snake into ‘very old’ records (made between the years 1800–1949) ‘old’ records (made between the years 1950–1999) and ‘recent’ records (after the year 2000). Regional conservation issues are discussed in the light of the previous papers and the personal observations of the authors. All results concerning habitat preferences of the dice snake are based on observations of the authors, unless stated otherwise. The maps, as well as the geographical information, were processed with GIS software (ArcGIS 9.3), using vector files (which represented localities, rivers and lakes) and raster files (Digital Elevation Model) as layers. From these, we extracted altitudes for each locality

Fig. 1. The historical-geographical regions of Romania where the Natrix tessellata was recorded: (1) Transylvania, (2) southwestern Romania, (3) southern Romania, (4) Dobrudja, (5) Romanian Moldavia.

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Fig. 2. Distribution of the dice snake (Natrix tessellata) in Romania. The black square in a red circle denotes the documented extinct population from Tarcău (Neamţ County) in Romanian Moldavia.

where Natrix tessellata was recorded in Romania. The projection used in processing the data was Stereo 70, DP 1970. The results of the locality based distribution were graphically presented in 10 × 10 km UTM maps on a national level. Results Locality Records Natrix tessellata was recorded in all major historical-geographical regions of Romania (n = 284): Transylvania, southwestern Romania, southern Romania, Romanian Moldavia and Romanian Dobrudja (Fig. 2, Appendix). The vast majority of records are new, in each region. The records are far from being equally distributed among the regions, the vast majority originating from Transylvania, followed by Dobrudja, southwestern Romania, southern Romania and Moldavia (Fig. 3). Throughout the range of the dice snake in Romania, recent locality records (those made for the first time or reconfirmed after the year 2000) contributed in all regions more than 70% of the records, except for Romanian Moldavia with 60% (Fig. 4). However, the relatively large portion of ‘old’, not recently confirmed, records from Romanian Moldavia is based on a low sample size of five localities (Fig. 4). Numerous localities were identified, particularly in Transylvania, which need further studies in order to confirm the presence/absence of the

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dice snake. The extinction of one population of N. tessellata in Romania has been adequately documented: Tarcău, Neamţ County, Romanian Moldavia (see Appendix, Fig. 2 and Discussion). Altitudinal Distribution The mean overall altitude of N. tessellata records in Romania is 246.97 m (SD = 166.52; Min. = -0.99 m; Max. = 885.17 m; n = 285). Figure 5 presents descriptive statistics of the altitudinal distribution of N. tessellata for

Fig. 3. National proportion of Natrix tessellata records for the five geographical regions in Romania.

Alexandru Strugariu, Iulian Gherghel, Ioan Ghira, Severus D. Covaciu-Marcov & Konrad Mebert

Fig. 4. Ratio of ‘very old’ (1800–1949), ‘old’ (1950–1999), and ‘recent’ (post 2000), records of Natrix tessellata in the five geographical regions of Romania. Sample size is given in brackets (N).

each region in Romania. The altitudinal range of the records varies significantly among the five regions (Kruskal-Wallis ANOVA; p < 0.0001). There are no significant differences between the occupied altitudes of southwestern Romania and Romanian Moldavia or between Transylvania and Romanian Moldavia (Mann-Whitney U, p > 0.05 for both groups). However, significant differences were detected for all other two-region comparisons (p < 0.05). Habitat Preferences In Transylvania, the dice snake is most abundant along the main courses of the larger rivers (e.g. the Mureş, Olt, Someş and Criş rivers; Fig. 6E), the adjacent swamps and

Fig. 5. Descriptive statistics of the altitudinal distribution of Natrix tessellata in Romania. Sample size is the same as in Fig. 4.

other still water bodies, whereas they are uncommon in smaller rivers or streams (Fig. 6C). It is very common around the thermal springs of Băile “First Mai” near Oradea, northwestern Transylvania (Fig. 6H). There are anecdotal accounts, that dice snakes have rapidly colonized man-made fish ponds in this region. In southwestern Romania, N. tessellata is most abundant in the rapid flowing mountain river, Cerna where they inhabit rocky riparian sections (Fig 6B). At Băile Herculane, numerous dice snakes, especially young specimens (< 50 cm), were observed by AS in the sulfurous thermal springs and pools which are adjacent to the Cerna River. Similar habitats are inhabited along the Danube and Jiu rivers and some of their tributaries, rivulets and streams (Fig 6I). In southern Romania, the species is found in natural, medium sized ponds and lakes with dense shore vegetation (Fig 6J), which are generally located in or near deciduous forests. The species is also present along the Danube River, and in Bucharest along the dyked Dâmboviţa River (Fig 6G). In Romanian Moldavia, the dice snake has been observed at the Brateş Lake, the extreme southeast of the region. This large reservoir lake was created before the 1990s, modifying the course of the Prut River. It has no obvious aquatic vegetation cover. But reeds, among which dice snakes can forage for fish, are present at various places along the shore. The edge of the lake is dyked and the western shore is bordered by a large slope, providing potential shelter for resting, hibernation, oviposition, and rapidly warming rocky surface for thermoregulatory activities (Fig 6A, 7). In the western part of Romanian Moldavia, the dice snake was only recorded at four localities. According to Băcescu & Matei (1958), the (now) extinct population from Tarcău (Neamţ County) inhabited an artificial fish pond and nested in sawdust piles, both of them having been destroyed. Two other recently recorded localities are situated near

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A

D

B

E

C

F

Fig. 6. Various habitats of Natrix tessellata in Romania: (A) Brateş Lake, Galaţi County, Romanian Moldavia; photo by A. Strugariu, (B) Cerna River, Caraş-Severin County, southwestern Romania; photo by A. Strugariu, (C) natural lake with dense surrounding vegetation, Cluj County, Transylvania; photo by I. Ghira, (D) natural lake in a limestone canyon, surrounded by thermophilious deciduous forests; dice snakes have been observed emerging from hibernation and basking in the rocky slopes above the lake, Constanţa County, Dobrudja; photo by A. Strugariu, (E) Mureş river, Mureş County, Transylvania; photo by I. Ghira, (F) the mouth of the Danube River into the Black Sea at Sfântu Gheorghe in the Danube Delta, Tulcea County, Dobrudja; photo by A. Strugariu, (G) urban and dycked sector of the Dâmboviţa River in Bucharest, southern Romania; photo by T. Sahlean, (H) natural thermal pond from Băile ”First Mai”, near Oradea, Bihor County, Transylvania; photo by H.V. Bogdan, (I) Danube River near Orşova , Mehedinţi County, southwestern Romania; photo by I. Sas, (J) natural pond with a rich surrounding vegetation, situated within a large deciduous forest at Comana, Giurgiu County, southern Romania. Photo: I. Gherghel.

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G

I

H

J

Fig. 6. (continued)

the Siret River without precise data on their habitats (Ghiurcă et al. 2006). In Romanian Dobrudja, N. tessellata is quite rare in the Danube Delta, but common along the Danube River itself. It is very common and abundant in the brakish waters of the Razelm-Sinoe Lagoon system (Carlsson et al. 2011), and in most freshwater and brakish lakes and swamps located along the Black Sea coast. These are sometimes dyked and lack any vegetation. In southern Dobrudja, the species inhabits natural lakes situated in small limestone canyons (Fig 6C). The south facing slopes of the limestone canyons are usually used as basking, nesting and hibernation sites. Occasionally, dice snakes have been observed in marine habitats and on the sandy beaches of the Black Sea (pers. obs. AS). Discussion Distribution and Habitat Preferences The range map in Figure 2 appearently displays an uneven distribution of Natrix tessellata in Romania. However, there are several factors that may influence our current knowledge of the distribution of dice snakes in this country. For example, the herpetofauna of Transylvania

has been more intensively studied than other regions in Romania, resulting in regionwide records (Ghira et al. 2002). However, according to these authors some of its locality data originated from sources of uncertain reliability, such as personal communications from local people who identified reptile species on the basis of photographs, or from old museum specimens that may include erroneous labels. In a comparative case, recent publications about the distribution of ‘brown frogs’ (Rana dalmatina and R. arvalis) in Transylvania or Romania by Demeter & Hartel (2007) and Sas et al. (2008a,b) mention several erroneous records provided by Ghira et al. (2002). Therefore, we urge to reconfirm such uncertain records exhibited in Ghira et al. (2002, see Appendix). Despite the possibility that some locality records from Transylvania are erroneous, the large number of historical and recent publications (e.g. Bielz 1888, Mehely 1918, Fejervary-Langh 1943, Fuhn & Vancea 1961, Covaciu-Marcov et al. 2000, 2003b, c, d, 2005a, b, 2007a, b,) show that N. tessellata is evenly distributed across Transylvania, likely reflecting the largest number of dice snake populations in Romania. Dobrudja is another area which has been of great interest to Romanian and foreign herpetologists due to its relatively rich reptile fauna, which includes several

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southern species (e.g. Covaciu-Marcov et al. 2006a). The dice snake is a constant presence along the natural course of the Danube River, towards its delta and in lakes along the Black Sea coast (Fig. 2). However, a surprising aspect is its absence or rareness in much of the Danube Delta. This area has been constantly surveyed by herpetologists, but the dice snake has been observed only at a few sites (e.g. Fuhn & Vancea 1961, Fuhn 1971, Kotenko et al. 1993, Török 2004). To our knowledge, no hypotheses have been proposed to explain the absence or very low abundance of the dice snake in what normally appears to be a relatively good habitat. However, as stated by newer studies and reviews compiled in Mebert (2011), N. tessellata prefers open areas with rocky shores interspersed with some vegetation. It is less common in alluvial plains with shading plant cover as in the Danube Delta (Fig 6F). That habitat appears to suit more the grass snake (N. natrix), which is very common and highly abundant throughout the Danube Delta (Strugariu et al. in prep.). In southwestern Romania, the first records of the dice snake originate from the 19th Century (Frivaldsky 1823, Mehely 1918). Here, only a few herpetofaunistc surveys have been conducted until after the year 2000, and the regional distribution of the species was previously greatly underestimated. Recently, detailed surveys revealed the presence of N. tessellata in numerous new localities and reported the species to be relatively abundant in some habitats (Iftime 2005b, Covaciu-Marcov et al. 2005a, b, 2009, Sahlean et al. 2008). Yet, since these studies often concentrated on small areas, much of southwestern Romania remains uncharted and it is probable that the dice snake is present in several additional localities. Southern Romania and Romanian Moldavia are the regions in which the dice snake appears to be least frequent. In southern Romania, the absence of locality records for the dice snake could have been attributed to the lack of surveys. However, in recent years, several authors have undertaken herpetofaunistic surveys of that region (e.g. Török 2001, Lazăr et al. 2005, Ţibu & Strugariu 2007) with only few localities yielding dice snakes during three surveys (Iftime 2005c, Iftime & Iftime 2007, 2008). Yet, records of dice snakes along most rivers at the border between southern Romania and Bulgaria (Naumov et al. 2011) indicate, that this species has been overlooked and exhibits a wider distribution in southern Romania. The population from the capital Bucharest was only recently rediscoverd after it was considered extinct by Iftime (2001). There, dice snakes are still present in urban environment within a sector of the Dâmboviţa River (T. Sahlean, pers. comm. 2009). Yet, we presume that numerous areas of southern Romania, that contain potential habitats for dice snakes, await the discovery of dice snakes, in particular if search methods focus on this species. A similar situation dislcoses in Romanian Moldavia. Historically, it was the least studied region concerning the herpetofauna and the dice snake was only re-

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corded from two localities during the mid 20th Century (Băcescu & Matei 1958, Fuhn & Vancea 1961, Ionescu et al. 1968). After 2000, numerous herpetofaunistic studies have been conducted here, succeeding in several new records of reptile species (Covaciu-Marcov et al. 2003a, 2006a, c, 2008b, Ghiurcă et al. 2005, 2006, Strugariu et al. 2006a, b, 2007, 2008b, c, Strugariu & Gherghel 2008, Gherghel et al. 2007, 2008). However, only three new localities were obtained for N. tessellata (Ghiurcă et al. 2006, Strugariu & Gherghel 2008). The latest discovered population from Brateş Lake in Galaţi County has probably been colonized from the nearby Danube River (Strugariu & Gherghel 2008). A previously known populations from Tarcău (Neamţ County) has become extinct (Gherghel et al. 2008), whereas the other historical record from Poiana Sărata, Bacău County by Fuhn & Vancea (1961), has not been confirmed yet despite a rapid survey of the area in 2008 (A. Strugariu, unpubl. data). Several areas of Romanian Moldavia, especially in the southwest (Vrancea County), the many water courses and lakes along the border with Moldavia, and the extreme northeast (eastern Botoşani County) appear to contain several habitats suitable for N. tessellata. But these areas have not yet been properly studied. Our recent data show the altitudinal distribution of the dice snake in Romania up to 900 m a.s.l., close to previous altitudinal records of up to 1000 m a.s.l (Fuhn & Vancea 1961). Similar upper altitudinal limits for the dice snake have been observed in southern areas of other central and eastern European countries, e.g. up to ~900 m a.s.l. in Austria, Switzerland and Croatia (Zimmermann & Fachbach 1996, Gruschwitz et al. 1999, Lenz et al. 2008, Jelic & Suvad 2011), an erratic single record from 1800 m a.s.l. in northern Italy (Scali & Gentilli 2006), but with more finds in the same Italian region as well as in Bulgaria for localities between 1100 m and 1475 m (Bruno & Maugeri 1990, Naumov et al.

Fig. 7. A death feigning, uniformly colored young dice snake from the recently discovered population at Brateş Lake in Romanian Moldavia. Photo: A. Strugariu.

Alexandru Strugariu, Iulian Gherghel, Ioan Ghira, Severus D. Covaciu-Marcov & Konrad Mebert

2011, R. Bennati pers. comm.). But the species is known to populate altitudes above 2000 m in the southern areas of the former Soviet Union (see Gruschwitz et al 1999 and references therein), Turkey and Iran (Bruno & Maugeri 1990, Rajabizadeh et al. 2011). In Romania, N. tessellata reaches the highest elevations in Transylvania (Fig. 4), where suitable habitats are available at relatively high altitudes, influenced by a milde climate from the west. Farther east in Romanian Moldavia, suitable habitats with well oxygenated mountain streams and rivers rich in various fish species apparently are present at higher altitudes, but this region is characterized by a much cooler, continental climate with Baltic influences from the north (e.g. Tufescu et al. 1995). Hence, higher elevations in this region, such as the eastern slopes of the Carpathians, are populated mostly by reptile species associated with a cooler climate (e.g. Vipera berus and Zootoca vivipara: see in Strugariu et al. 2006a, b, 2007, 2008 b, Gherghel et al. 2008, Covaciu-Marcov et al. 2008b). In southwestern Romania, suitable habitats for the dice snake are very rare at higher altitudes, whereas the Dobrudja Region in the east of Romania does not get higher than 467 m a.s.l. The accounts above explain the statistical significant variations found in altitudinal distribution. Lastly, it remains unclear why the dice snake was not recorded at higher elevations in southern Romania. More detailed surveys in the area are needed in order to evaluate the distribution and frequency of the dice snake in these regions. The habitats preferred by N. tessellata in Romania are generally similar to those described from other regions of the species’ range. It occurs in various types of running water (rivers and streams), similar to the many lotic systems inhabited in central and southern Europe (see Gruschwitz et al 1999 and refs. therein). Medium sized to very large natural or man made lakes, ponds and fishfarms are also commonly inhabited by the species in Romania, as reported from other areas in its range, e.g. in Switzerland, Italy, Hungary, Croatia, Greece (Gruschwitz et al. 1999, Herczeg et al. 2005, Mebert 2001, Mebert 2007, Ioannidis & Mebert 2011, Janev Hutinec & Mebert 2011, Mebert et al. 2011). One of the largest dice snake populations is found in the brackish waters of the Razelm-Sinoe Lagoon system, adjacent to the Danube Delta. The species also uitilizes the Black Sea (thriving along its rocky shores) and is sometimes found in brackish water lakes adjacent to the coast. In the northwestern part of Transylvania (Băile “First Mai”, located near Oradea, Bihor County) and in, at least, one locality in southwestern Romania (Băile Herculane, Caraş-Severin County), the dice snake frequently inhabits natural thermal springs with elevated temperatures from 25–30°C in the Băile “First Mai” – CovaciuMarcov et al. 2006b). In Băile ”First Mai” it populates thermal ponds, whereas in the latter it inhabits thermal springs which flow into the Cerna River. However, the springs are usually too small to provide a permanent habitat for the dice snake. The usage of thermal water by the dice snake was previously recorded only from Hun-

gary (see Gruschwitz et al 1999). The thermal ponds from Băile “First Mai” have recently received increased attention due to the particular biology of the amphibians (especially Pelophylax ridibundus) inhabiting them (Covaciu-Marcov et al. 2006b). Several life history traits (e.g. larva size, reproductive cycle) of these amphibians are significantly influenced by the thermal quality of the habitats, most impressively, the absence of hibernation (Covaciu-Marcov et al. 2006b). However, no such data have been collected regarding the influence of these thermal water systems on the biology of the dice snake, nor any other coexisting semi-aquatic reptile species (e.g. Natrix natrix or Emys orbicularis). Conservation Even if the distribution of the dice snake in Romania is fairly well known today, almost no data with regards to the species’ biology, including population sizes, microhabitat selection, seasonal activity and movements are known from this country. Therefore, establishing proper management plans or a pertinent conservation status based on national data is difficult and needs to rely on informationn from other regions (see articles in Mebert 2011). Several factors which threaten dice snake populations have been sporadically mentioned in the Romanian literature. One of the major factors is the culturally induced direct persecution of the species. For example, Fuhn (1969) quotes a paragraph from a Romanian fishing magazine in which the author describes how he killed three dice snakes which were eating Barbus sp. and states that the dice snake represents a major threat to the native Romanian fish populations. This view was shared by Băcescu & Matei (1958) who mentioned that the dice snake is a major threat to the fishes in fish farms, and gave instructions, how to obliterate the N. tessellata populations without killing the ‘harmles’ (= because not consuming fish) grass snakes (N. natrix). By the time that Ionescu et al. (1968) had conducted their survey of the area where Băcescu & Matei (1958) cited a very large dice snake population, only very few specimens could be detected. At present, the population is extinct, probably as a result of direct persecution (Gherghel et al. 2008). Thus, due to its feeding habits, the dice snake seems to be more vulnerable for direct persecution than its congeneric grass snake. The species is sympatric with Vipera ammodytes in many areas between southwestern Romania and Dobrudja. In areas where the presence of the viper is known by the locals or tourists, the dice snake is frequently killed as a result of confusion between the two species. Numerous snakes killed by humans have been observed throughout the species’ range during our field surveys (A. Strugariu, I. Gherghel, I. Ghira, S.D. Covaciu-Marcov, unpubl.). Road mortality is a common anthropogenic factor which negatively affects the herpetofauna in numerous regions of Europe (e.g. Brito & Alvares 2004, Stru-

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gariu et al. 2008a, Sahlean et al. 2008,). Roads occur frequently in habitats colonized by dice snakes. Several surveys reported road mortality as a major threat to the populations in Romania (e.g. Iftime 2001, Covaciu-Marcov et al. 2009). However, no quantitative study has ever been conducted on the influence of road mortality on Romanian reptile populations. But first assessments have been published from a locality with high road mortality in Greece (Ioannidis & Mebert 2011). Another important factor, which for example threatens the dice snake population at the Razelm-Sinoe Lagoon system, was only recently identified as the increasing number of snakes infected by the Eustrongylides excisus nematode (Mihalca et al. 2007, Carlsson et al. 2011). Studies revealed that aproximatly 50% of all adult dice snakes from that area were infected with this nematode and that numerous specimens were dying as a result of this. Several authors have tried to establish the conservation status of the Romanian herpetofauna. For example, Cogălniceanu & Venczel (1993) and Iftime (2001) considered N. tessellata to be a vulnerable (VU) species at a national level, whereas a few years later, Iftime (2005a) changed that status in the Red Data Book of Vertebrates from Romania to be near threatened (NT). The dice snake is a strictly protected species in Romania since 1993 (Law 13/1993 – following adherence to the Bern Convention) and has recently been classified as a species of community interest which requires strict protection (Romanian Government Order 57 / 2007). Given the relatively large number of old, unconfirmed localities from where the species was reported, the fact that the recent literature describes only few populations with a high abundance of dice snakes, and the numerous factors that threaten the snake (especially the direct persecution), we classify the species as vulnerable (VU) on a national level. However, this status should only be considered preliminary, since further studies are required to establish its proper conservation status, inlcuding geographic inventories, particularly to bridge the gap in southern Romania, and preferably detailed studies on the population biology of N. tessellata. Acknowledgements We are grateful to T. Sahlean (Bucharest, Romania) for sharing his unpublished observations with us, and to H. V. Bogdan for sharing a photograph of the thermal pond habitats. I. Sas (Oradea, Romania) and L. Krecsak (Budapest, Hungary) are greatly acknowledged for their comments on a previous version of the manuscript. Dr. D. Cogălniceanu (Constanţa, Romania), Dr. A. Iftime (Bucharest, Romania) and Z. Török (Tulcea, Romania) are acknowledged for providing a part of the cited literature.

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References Băcescu, M. (1934): Contributions á la faune des reptiles de Dobrogea. – Ann. Scient. Univ. Jassy 19(1–4): 317–330. Băcescu, M. & D. Matei (1958): Şarpele de apă (Natrix tessellata L.) în bazinul superior al Bistriteţi. – Natura 10(5): 137–139 (in Romanian). Bielz, E.A. (1888): Die Fauna der Wirbeltiere Siebenbürgens nach ihrem jetzigem Bestande. – Verh. Mitt. Siebenb. Ver. Hermannstadts 38: 15–120. Brito, J.C. & F.J. Alvares (2004): Patterns of road mortality in Vipera latastei and Vipera seoanei from northern Portugal. – Amphibia-Reptilia 25: 459–465. Bruno, S. & S. Maugeri (1990): Serpenti d’Italia e d’Europa. – Mondadori, Milano. Călinescu, R. (1931): Contribuţiuni sistematice şi zoogeografice la studiul amfibiilor şi reptilelor din România. – Mem. Secţ. Ştiinţ. Acad. Romîne, Bucureşti 7: 119–291 (in Romanian). Carlsson, M., Kärvemo, S., Tudor, M., Sloboda, M., Mihalca, A.D., Ghira, I., Bel, L. & D. Modrý (2011): Monitoring a large population of dice snakes at Lake Sinoe in Dobrogea, Romania. – Mertensiella 18: 237–244. Cogălniceanu, D. & M., Venczel (1993): Consideraţii privind ocrotirea şi conservarea populaţiilor de amfibieni şi reptile. – Ocrotirea naturii şi a mediului înconjurător 37(2): 109–114 (in Romanian). Covaciu-Marcov, S.D., Ghira I. & M. Venczel (2000): Contribuţii la studiul herpetofaunei din zona Oradea. – Nymphaea, Folia Naturae Bihariae XXVIII: 143–158 (in Romanian). Covaciu-Marcov, S.D., Sas, I., Cicort-Lucaciu, A. & E.H. Kovacs (2003a): Notes upon the herpetofauna of the northern area of the Botoşani County (Romania). – Studii şi Cercetări, Biologie, Universitatea din Bacău 8: 201–205. Covaciu-Marcov, S.D., Sas, I., Cupşa, D., Meleg, G. & B. Bud (2003b): Studii herpetologice în regiunea Munţilor Pădurea Craiului şi Plopişului (Jud. Bihor, România). – Analele Universităţii din Oradea, Fascicula Biologie Tom X: 81–95 (in Romanian). Covaciu-Marcov, S.D., Telcean, I., Cupşa, D., Sas, I. & A. Cicort (2003c): Contribuţii la cunoaşterea herpetofaunei regiunii bazinului hidrografic mediu şi inferior al Crişului Negru (Jud. Bihor, România). – Muzeul Olteniei Craiova. Oltenia. Studii şi Comunicări. Ştiinţele Naturii XIX: 189–194 (in Romanian). Covaciu-Marcov, S.D., Telcean, I., Georgeta, S., Sas, I. & A. Cicort (2003d): Contibuţii la cunoaşterea herpetofaunei regiunii Beiuş, Jud. Bihor, România. – Nymphaea, Folia Naturae Bihariae XXX: 127–141 (in Romanian). Covaciu-Marcov, S.D., Cicort-Lucaciu, A.Ş., Sas, I., Bredet, A. & H. Bogdan (2005a): The herpetofauna from the basin of Mureş river in Arad County, Romania. – Environment & Progress, Cluj-Napoca 4: 147–152. Covaciu-Marcov, S.D., Sas, I., Cicort-Lucaciu, A., Peter, I. & H. Bogdan (2005b): Notes upon the herpetofauna of the south-west area of the county of Caraş-Severin, Romania. – Revue Roumaine de Biologie, Biol. Anim. 50(1-2): 47–56. Covaciu-Marcov, S.D., Ghira, I., Cicort-Lucaciu, A.Ş., Sas, I., Strugariu, A. & H. Bogdan (2006a): Contribution to the knowledge regarding the geographical distribution of the herpetofauna of Dobrudja, Romania. – North-Western Journal of Zoology 2(2): 88–125. Covaciu-Marcov, S.D., Sas, I. & A.Ş. Cicort-Lucaciu (2006b): Amfibienii apelor termale din vestul României. – Editura Uni-

Alexandru Strugariu, Iulian Gherghel, Ioan Ghira, Severus D. Covaciu-Marcov & Konrad Mebert versităţii din Oradea, Romania (in Romanian with English summary). Covaciu-Marcov, S.D., Sas, I., Cicort-Lucaciu, A.Ş., Bogdan, H. & M. Groza (2006c): Contributions to the knowledge regarding the composition and geographical distribution of the herpetofauna from Moldavia between the Siret and Prut rivers. – Muzeul Olteniei Craiova, Oltenia, Studii şi Comunicări Ştiinţele Naturii 22: 131–136. Covaciu-Marcov, S.D., Cicort-Lucaciu, A.Ş., Ile, R.D., Pascondea, A. & R. Vatamaniuc (2007a): Contributions to the study of the geographical distribution of the herpetofauna in the North-East area of Arad County in Romania. – Herpetologica Romanica 1: 62–69. Covaciu-Marcov, S.D., Cicort-Lucaciu, A.Ş., Lazăr, V., Szeibel, N. & L. Balaj (2007b): The herpetofauna of the lower hydrographical basin of Crişul Alb, the District of Arad (Romania). – Muzeul Olteniei Craiova, Oltenia, Studii şi Comunicări, Ştiinţele Naturii Tom XXIII: 143–148. Covaciu-Marcov, S.D., Cicort-Lucaciu, A.Ş., Bogdan, H.V., Ferenţi, S. & A. Filimon (2008a): New contributions to the study of the geographic distribution of the herpetofauna of the south-west Dobrudja, Romania. – Analele Universităţii din Craiova, Seria Biologie, Horticultură, Tehnologia Prelucrării Produselor Agricole, Ingineria Mediului XIII: 5358. Covaciu-Marcov, S.D., Cicort-Lucaciu, A.Ş., Sas, I., Strugariu, A., Cacuci, P. & I. Gherghel (2008b): Contributions to the knowledge regarding the composition and geographical distribution of the herpetofauna from Northern Moldavia (Sucaeva and Botoşani Counties, Romania). – North-Western Journal of Zoology 4(1): 25–47. Covaciu-Marcov, S.D., Cicort-Lucaciu, A.Ş., Gaceu, O., Sas, I., Fer i, S. & H.V. Bogdan (2009): The herpetofauna of the south-western part of Mehedinţi County, Romania. – NorthWestern Journal of Zoology 5(1): 142–164. Cruce, M. (1971): Contribuţii la studiul faunei herpetologice din Oltenia. – Analele Universităţii din Craiova III, Ştudii agricole, biologice 3: 389–393 (in Romanian). Demeter, L. & T. Hartel (2007): On the absence of Rana dalmatina from the Ciuc basin, Romania. – North-Western Journal of Zoology 3(1): 9–23. Fejervary-Langh, A. M. (1943): Beiträge und Berichtigungen zum Reptilien–Teil des ungarischen Faunenkataloges. – Fragm. Faun. Hungar. 6(3): 81–98. Filippi, E., Capula, M., Luiselli, L. & U. Agrimi (1996): The prey spectrum of Natrix natrix (Linnaeus, 1758) and Natrix tessellata (Laurenti, 1768) in sympatric populations. – Herpetozoa 8(3/4): 155–164. Frankham, R. (2005): Genetics and extinction. – Biological Conservation 126: 131–140. Frivaldsky, E. (1823): Monographia Serpentum Hungariae. – Pestini, Typis Nobilis Joannis Thomae Trattner de Petróza vii. Fuhn, I.E. (1969): Broaşte, şerpi, şopârle. – Colecţia Natura şi Omul. Editura Ştiinţifică, Bucureşti (in Romanian). Fuhn, I.E. & Ş. Vancea (1961): Fauna Republicii Populare Române XIV (2) – Reptilia. – Editura Academiei R.P.R., Bucureşti (in Romanian). Gasc, J.P., Cabela, A., Crnobrnja-Isailovic, J., Dolmen, D., Grossenbacher, K., Haffner, P., Lescure, J., Martens, H., Martínez-Rica, J.P., Maurin, H., Oliveira, M.E., Sofianidou, T.S., Veith, M. & A. Zuiderwijk (Eds.) (1997): Atlas of Amphibians and Reptiles in Europe. – Collection Patrimoines Naturels 29. – Societas Europaea Herpetologica, Muséum National d’Histoire Naturelle & Service du Petrimone Naturel, Paris, France.

Gherghel, I., Strugariu, A., Ghiurcă, D., Roşu, S. & M.V. Huţuleac-Volosciuc (2007): The composition and distribution of the herpetofauna from the Valea Neagră River basin (Neamţ County, Romania). – Herpetologica Romania 1: 70–76. Gherghel, I., Strugariu, A., Ghiurcă, D. & A.Ş. Cicort-Lucaciu (2008): The herpetofauna from the Bistriţa River basin (Romania): Geographical distribution. – North-Western Journal of Zoology 4(1): 71–103. Ghira, I., M., Venczel, S.D., Covaciu-Marcov, G., Mara, P., Ghile, T., Hartel, Z., Török, L., Farkas, T., Racz, Z., Farcas & T., Brad (2002): Mapping of Transylvanian Herpetofauna. - Nymphaea, Folia naturae Bihariae 29: 145–203. Ghiurcă, D., Roşu, S. & I. Gherghel (2005): Preliminary data concerning the herpetofauna in Neamţ County (Romania). – Analele Universităţii din Oradea, Fascicula Biologie 12: 53–62. Ghiurcă, D., Rang, C. & S. Roşu (2006): Preliminary data concerning the herpetofauna in Bacău county. – Bacău, Studii şi Cercetări, Biologie 10: 91–98. Gruschwitz, M., Lenz, S., Mebert, K. & V. Lanka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581–644. Guicking, D. & U. Joger (2011): A range-wide molecular phylogeography of Natrix tessellata. – Mertensiella 18: 1–10. Guicking, D., Joger, U. & M. Wink (2009): Cryptic diversity in a Eurasian water snake (Natrix tessellata): Evidence from mitochondrial sequence data and nuclear ISSR-PCR fingerprinting. – Organisms, Diversity and Evolution 9(3): 201–214. Guicking, D., Lawson, R., Joger, U. & M. Wink (2006): Evolution and phylogeny of the genus Natrix (Serpentes: Colubridae). – Biological Journal of the Linnean Society 87: 127–143. Herczeg, G., Szabo, K. & Z. Korsos (2005): Asymmetry and population characteristics in dice snakes (Natrix tessellata): an interpopulation comparison. – Amphibia-Reptilia 26: 422– 426. Iftime, A. (2001): Lista roşie comentată a amfibienilor şi reptilelor din România. – Ocrotirea Naturii şi Mediului Înconjurător, 44/45: 39–49 (in Romanian). Iftime, A. (2005a): Natrix tessellata (Laurenti, 1768). – In: Botnariuc, N. & V. Tatole (Eds.): Cartea Roşie a Vertebratelor din România. – Editura Academiei Române, Bucharest, Romania (in Romanian). Iftime, A. (2005b): New observations on the herpetofauna from Domogled-Valea Cernei National Park and Porţile de Fier Natural Park (Romania). – Travaux du Museum National d’Histoire Naturelle “Grigore Antipa” (Bucharest) XLVIII: 327–337. Iftime, A. (2005c): Herpetological observations in the Danube Floodplain sector in the Giurgiu County (Romania). – Travaux du Museum National d’Histoire Naturelle “Grigore Antipa” (Bucharest) XLVIII: 339–348. Iftime, A. & O. Iftime (2007): Some records of the herpetofauna of the Danube Floodplain in the Balta Ialomiţei area (Romania). – Travaux du Museum National d’Histoire Naturelle “Grigore Antipa” (Bucharest) L: 273–281. Iftime, A. & O. Iftime (2008): Observations on the herpetofauna of the Giurgiu County (Romania). – Travaux du Museum National d’Histoire Naturelle “Grigore Antipa” (Bucharest) LI: 209–218. Ioannidis, Y. & K. Mebert (2011): Habitat preferences of Natrix tessellata at Strofylia, northwestern Peloponnese, and comparison to syntopic N. natrix. – Mertensiella 18: 302–310.

281

The Dice Snake (Natrix tessellata) in Romania Ionescu, V., Miron, I., Munteanu, D. & V. Simionescu (1968): Vertebratele din bazinul montan al Bistriţei. – Lucrările staţiunii de cercetări biologice, geologice şi geografice Stejarul, Pângaraţi: 356–437 (in Romanian). Janev Hutinec, B. & K. Mebert (2011). Ecological partitioning among dice snakes (Natrix tessellata) and grass snakes (Natrix natrix) in southern Croatia. – Mertensiella 18: 225–233. Jelić, D. & L. Suvad (2011): Distribution and status quo of Natrix tessellata in Croatia, Bosnia and Herzegovina. – Mertensiella 18: xxx–yyy. Joger, U., Fritz, U., Guicking, D., Kalyabina-Hauf, S., Nagy, Z.T. & M. Wink (2007): Phylogeography of western Palearctic reptiles – Spatial and temporal speciation patterns. – Zoologischer Anzeiger 242: 293–313. Kärvemo, S., Carlsson, M., Tudor, M., Sloboda, M., Mihalca, A., Ghira, I., Bel, L. & D. Modrý (2011): Gender differences in seasonal movements in a Romanian dice snake population. – Mertensiella 18: 245–254. Kiritzescu, C. (1901): Enumeraţia reptilelor şi batracienilor din România. – Publ. Soc. Nat. Romania 1 (in Romanian). Kotenko, T., Oţel, V. & A. Fedorchenko (1993): Herpetological investigations in the Danube Delta Biosphere Reserve in 1992. – Analele Ştiinţifice ale Institutului Delta Dunării 2: 99–107. Lazăr, V., Covaciu-Marcov, S.D., Sas, I., Pusta, C. & E.H. Kovacs (2005): The herpetofauna in the district of Dolj (Romania). – Analele Ştiinţifice ale Universităţii “Al. I. Cuza” Iaşi, s. Biologie animală Tom LI: 151–158. Lenz, S., Mebert, K., & J. Hill (2008): Die Würfelnatter (Natrix tessellata). – In: DGHT (Ed.): Die Würfelnatter – Reptil des Jahres 2009. – DGHT, Rheinbach, Germany: 6–32. Luiselli, L. (2006): Broad geographic, taxonomic and ecological patterns of interpopulation variation in the diatary habits of snakes. – Web Ecology 6: 2–16. Mebert, K. (2001): Die Würfelnatter am Lopper. – In: Amphibien und Reptilien in Unterwalden. – NAGON, Vol. II: 158–163. Mebert, K. (2007): Die Würfelnatter am Brienzersee. – In: Jahrbuch 2007, Uferschutzverband Thuner- und Brienzersee. – UTB Selbstverlag, Thun, Switzerland: 169–180. Mebert, K. (Ed.) (2011): The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species. – Mertensiella 18, DGHT, Rheinbach, Germany Mebert, K., Conelli, A.E., Nembrini, M. & B.R. Schmidt (2011): Monitoring and assessment of the distribution of the dice snake in Ticino, southern Switzerland. – Mertensiella 18: 117–130. Mehely, L. (1918): Reptilia et Amphibia, in Fauna Regni Hungaricae 1: 1–12. Mertens, R. (1957): Tierleben im Donau-Delta, 1. Lurche und Kriechtiere. – Natur und Volk 87(5): 160–169. Mihalca, A.D., Fictum, P., Skoric, M., Sloboda, M., Kärvemo, S., Ghira, I., Carlsson, M. & D. Modry (2007): Severe granulomatous lesions in several organs from Eustrongylides larvae in a free-ranging dice snake, Natrix tessellata. – Veterinary Pathology 44: 103–105. Naumov, B., Tzankov, N., Popgeorgiev, G., Stojanov, A. & Y. Kornilev (2011): The dice snake (Natrix tessellata) in Bulgaria: distribution and morphology. – Mertensiella 18: 288–297. Petrescu, M., Dinu, C., Radu, A. & V. Cuzic (2003): The monitoring of the fluvial lakes from south-western Dobrogea. – Studii şi Cercetări, Biologie, Universitatea din Bacău 8: 193– 197.

282

Sahlean, C.T., Strugariu, A., Zamfirescu, Ş., Pavel, A., Puşcaşu, C.M. & I. Gherghel (2008): A herpetological hotspot in peril: Anthropogenic impact upon the amphibian and reptile populations from the Băile Herculane tourist resort, Romania. – Herpetologica Romanica. 2: 37–46. Sas, I., Covaciu-Marcov, S.D., Demeter, L., Cicort-Lucaciu, A.Ş. & A. Strugariu (2008a): Distribution and status of the moor frog (Rana arvalis) in Romania. – In: Glandt, D. & R. Jehle (Eds.): Der Moorfrosch/The Moor Frog. – Laurenti Verlag, Bielefed, Germany: 337–354. Sas, I., Covaciu-Marcov, S.D. & E.H. Kovacs (2008b): Is the conservation of the moor frog problematic in Romania? – Herpetologica Romanica 2: 57–60. Scali, S. & A. Gentilli (2006): Natrix tessellata, Dice snake. – In: Sindaco, R., Doria, G., Razzeti, E. & F. Bernini (Eds.): Atlas of Italian Amphibians and Reptiles. – Edizioni Polistampa, Societas Herpetologica Italica, Firenze. Strugariu, A. & I. Gherghel (2008): A preliminary report on the composition and distribution of the herpetofauna in the Lower Prut River Basin (Romania). – North-Western Journal of Zoology 4(1): 49–69. Strugariu, A., Sahlean, T.C., Voloşciuc-Huţuleac, M.V. & C.M. Puşcaşu (2006a): Preliminary data regarding the distribution of reptilian fauna in Suceava County (Romania). – North-Western Journal of Zoology 2(1): 39–43. Strugariu, A., Sahlean, T.C., Voloşciuc-Huţuleac, M.V., Sas, I., Puşcaşu, C.M. & I. Gherghel (2006b): Contributions to the study of the herpetofauna from the Suceava River Basin (Suceava County, Romania). – Studii şi Comunicări, Complexul Muzeal de Ştiinţele Naturii “Ion Borcea” Bacău 21: 437–446. Strugariu, A., Gherghel, I., Puşcaşu, C.M. & T.C. Sahlean (2007): The current status of the herpetofauna and the important herpetofaunal areas from Suceava County (Romania). – Analele Ştiinţifice ale Universităţii “Al. I. Cuza” Iaşi, s. Biologie animală. Tom LIII: 167–174. Strugariu, A., Gherghel, I., Zamfirescu, Ş.R. & T.C. Sahlean (2008a): Spatial distribution of the herpetofauna from the upper and middle Moldova river basin (Romania). – Travaux du Museum National d’Histoire Naturelle “Grigore Antipa” (Bucharest) LI: 231–241. Strugariu, A., Sos, T., Gherghel, I., Ghira, I., Sahlean, T.C., Puşcaşu, C.M. & M.V. Huţuleac-Volosciuc (2008c): Distribution and current status of the herpetofauna from the northern Măcin Mountains area (Tulcea County, Romania). – Analele Ştiinţifice ale Universităţii “Al. I. Cuza” Iaşi, s. Biologie animală. Tom LIV: 191–206. Strugariu, A., Zamfirescu, Ş.R., Nicoară, A., Gherghel, I., Sas, I., Puşcaşu, C.M. & T. Bugeac (2008c): Preliminary data regarding the distribution and status of the herpetofauna in Iaşi County (Romania). – North-Western Journal of Zoology 4(1): 1–23. Ţibu, P. & A. Strugariu (2007): A new record for the blotched snake Elaphe sauromates in Romania. – North-Western Journal of Zoology 3(1): 62–65. Török, Zs. (1995): Actual state of the North-Dobrogean Herpetofauna. – E.M.E. Muz. Fuz. (Cluj-Napoca) 5: 110–117. Török, Zs. (2001): Herpetological inevstigations in the Lower Danube area (Calafat-Călăraşi sector). – Studii şi Cercetări, Biologie, Universitatea din Bacău 6: 115–119. Török, Zs. (2004): Herpetological investigations in the Danube Delta Biosphere Reserve (Romania) in 2003. – Analele Ştiinţifice ale Institutului Delta Dunării 10: 81–83.

Alexandru Strugariu, Iulian Gherghel, Ioan Ghira, Severus D. Covaciu-Marcov & Konrad Mebert Rajabizadeh, M., Javanmardi, S., Rastegar-Pouyani, N., Karamiani, R., Yusefi, M., Salehi, H., Joger, U., Mebert, K., Esmaeili, H., Parsa, H., Gholi Kami, H. & E. RastegarPouyani. (2011): Geographic variation, distribution and habitat of Natrix tessellata in Iran. – Mertensiella 18: 414–429.

Tufescu, V., Giurcăneanu, C. & I. Mierlă (1995): Geografia României. – Ed. Didactică şi Pedagogică, Bucharest (in Romanian). Zimmermann, P. & G. Fachbach (1996): Verbreitung und Biologie der Würfelnatter, Natrix tessellata tessellata (Laurenti, 1768), in der Steiermark (Österreich). – Herpetozoa 8(3/4): 99–124.

Appendix List of Romanian localities with N. tessellata. The information for each record is listed into following, sequential categories: locality, county, UTM code, elevation (a.s.l.), GPS coordinates, source in parenthesis including number for literature references at the end of the Appendix, and special remarks. Personal observations were included only if there were no more recent published records (R.C. = Requires confirmation): Counties: CS = Caraş-Severin, GJ = Gorj, MH = Mehedinţi, AB = Alba, AR = Arad, BH = Bihor, BN = Bistriţa Năsăud, BV = Braşov, CJ = Cluj, CV = Covasna, HD = Hunedoara, HR = Harghita, MM = Maramureş, MS = Mureş, SB = Sibiu, SJ = Sălaj, SM = Satu Mare, TM = Timiş, BC = Bacău, GL = Galaţi, NT = Neamţ, CT = Constanţa, TL = Tulcea, CL = Călăraşi, GR = Giurgiu, B = Bucharest (capital city of Romania, not included in a county). SOUTHWESTERN ROMANIA Susca, CS, EQ45, 77 m, 44° 47’ 2.9674” N 21° 31’ 58.3512” E, (1); Baile Herculane, CS, FQ17, 156 m, 44° 52’ 52.4562” N 22° 24’ 52.1976” E, (2, 3, 4, 5), Decreasing population; Bazias, CS, EQ36, 277 m, 44° 48’ 48.3586” N 21° 23’ 56.5061” E, (6, 3, 1, 4); Belobresca, CS, EQ45, 80 m, 44° 47’ 10.6023” N 21° 30’ 43.7974” E, (1); Berzasca, CS, EQ74, 76 m, 44° 38’ 51.1347” N 21° 57’ 28.1134” E, (1); Cornea, CS, FQ08, 350 m, 45° 02’ 29.7483” N 22° 19’ 30.7411” E, (1); Coronini, CS, EQ54, 96 m, 44° 40’ 46.7550” N 21° 40’ 55.4705” E, (1); Divici, CS, EQ35, 74 m, 44° 46’ 56.6947” N 21° 28’ 53.0614” E, (1); Crusovita, CS, EQ64, 167 m, 44° 40’ 56.2888” N 21° 48’ 45.5596” E, (1); Cozla, CS, EQ74, 68 m, 44° 37’ 43.4209” N 22° 00’ 20.2488” E, (1); Liborajdea, CS, EQ64, 229 m, 44° 40’ 33.2797” N 21° 46’ 55.6974” E, (1); Mehadia, CS, FQ07, 164 m, 44° 54’ 17.3029” N 22° 21’ 58.2002” E, (7, 3), R.C.; Liubcova, CS, EQ74, 74 m, 44° 39’ 16.1988” N 21° 53’ 33.7510” E, (1); Macesti, CS, EQ45, 84 m, 44° 45’ 20.0023” N21° 36’ 31.0672” E, (1); Moldova Veche, CS, EQ45, 71 m, 44° 43’ 18.4944” N21° 37’ 10.6472” E, (1); Radimna, CS, EQ46, 85 m, 44° 47’ 40.1687” N 21° 33’ 43.4324” E, (1); Pojejena, CS, EQ45, 72 m, 44° 46’ 22.8779” N 21° 34’ 12.1495” E, (1); Sichevita, CS, EQ64, 104 m, 44° 41’ 47.8207” N 21° 50’ 41.5799” E, (1); Targu Jiu, GJ, FQ78, 208 m, 45° 02’ 17.5016” N 23° 16’ 37.8244” E, (8, 3), R.C.; Svinita, MH, EQ82, 75 m, 44° 30’ 4.9124” N 22° 05’ 32.9835” E, (I. Ghira, pers. obs. 1995), R.C.; Baia de Arama, MH, FQ48, 280 m, 44° 59’ 57.2462” N 22° 48’ 27.9872” E, (9), R.C.; Dubova, MH, FQ04, 63 m, 44° 37’ 10.3086” N 22° 16’ 3.8795” E, (10); Eşelniţa, MH, FQ04, 62 m, 44° 41’ 1.8812” N 22° 22’ 10.4565” E, (4, 10); Ilovita, MH, FQ15, 108 m, 44° 45’ 24.1025” N 22° 28’ 32.6326” E, (10), R.C.; Orsova, MH, FQ15, 62 m, 44° 42’ 10.9616” N 22° 24’ 40.9493” E, (11, S.D. Covaciu-Marcov, pers. obs. 2009); Schitu Topolnitei, MH, FQ25, 528 m, 44° 46’ 18.3531” N 22° 35’ 12.0536” E, (10); Plavisevita, MH, EQ93, 64 m, 44° 34’ 21.3530” N 22° 14’ 1.8035” E, (6, 11, 4); Vârciorova, CS, EQ35, 368 m, 45° 19’ 37.7379” N 22° 21’ 3.4502” E, (4); Bahna, MH, EQ15, 130 m, 44° 46’ 30.7271” N 22° 30’ 0.7114” E, (4, 10); Gura Văii, CS, EQ35, 60 m, 44° 40’ 5.3065” N 22° 33’ 36.2271” E, (12, 4) TRANSYLVANIA Abrud, AB, FS52, 604 m, 46° 16’ 22.0231” N 23° 04’ 9.6635” E, (13), R.C.; Brazesti, AB, FS74, 471 m, 46° 23’ 55.2187” N 23° 19’ 1.2837” E, (13), R.C.; Ganesti, AB, FS63, 576 m, 46° 23’ 20.3704” N 23° 07’ 47.1343” E, (13), R.C.; Galda de sus, AB, FS92, 350 m, 46° 13’ 28.7137” N 23° 33’ 47.1389” E, (13), R.C.; Gura Rosiei, AB, FS53, 583 m, 46° 18’ 27.0375” N 23° 03’ 12.2286” E, (13), R.C.; Lunca Larga, AB, FS85, 621 m, 46° 31’ 29.9517” N 23° 25’ 37.8465” E, (13), R.C.; Lunca, AB, FS84, 415 m, 46° 26’ 22.1059” N 23° 27’ 36.5822” E, (13), R.C.; Lunca Larga, AB, FS63, 558 m, 46° 22’ 43.1305” N 23° 07’ 48.0586” E, (13), R.C.; Lupsa, AB, FS63, 516 m, 46° 22’ 8.7798” N 23° 12’ 22.4892” E, (13), R.C.; Ocolis, AB,

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FS85, 428 m, 46° 28’ 43.1311” N 23° 28’ 0.9518” E, (13), R.C.; Posaga de Jos, AB, FS84, 437 m, 46° 25’ 53.2115” N 23° 26’ 23.3786” E, (13), R.C.; Poiana Galdei, AB, FS92, 394 m, 46° 14’ 31.4027” N 23° 31’ 54.6436” E, (13), R.C.; Runc, AB, FS85, 493 m, 46° 30’ 4.5719” N 23° 27’ 12.6964” E, (13), R.C.; Sartas, AB, FS74, 500 m, 46° 23’ 30.7588” N 23° 17’ 49.5088” E, (13), R.C.; Salciua de Sus, AB, FS84, 451 m, 46° 23’ 36.1590” N 23° 24’ 5.0648” E, (13), R.C.; Vidolm, AB, FS95, 427 m, 46° 28’ 50.0990” N 23° 30’ 56.9437” E, (13), R.C.; Aciuta, AR, FS12, 216 m, 46° 17’ 13.4869” N 22° 27’ 11.2066” E, (14); Arad, AR, ES21, 109 m, 46° 10’ 17.0639” N 21° 20’ 2.1157” E, (6, 3), R.C.; Soimos, AR, ES50, 128 m, 46° 06’ 24.4113” N 21° 43’ 7.9916” E, (1); Beliu, AR, ES74, 123 m, 46° 29’ 33.0246” N 21° 59’ 12.3892” E, (13), R.C.; Berindia, AR, ES83, 156 m, 46° 19’ 15.6313” N 22° 09’ 37.7699” E, (14); Bocsig, AR, ES74, 126 m, 46° 25’ 17.5061” N 21° 56’ 28.3439” E, (13), R.C.; Brazii, AR, FS02, 193 m, 46° 14’ 29.3429” N 22° 20’ 9.4231” E, (14); Barzava, AR, ES70, 142 m, 46° 06’ 40.6047” N 21° 58’ 35.9680” E, (15); Buceava-soimus, AR, FS01, 294 m, 46° 12’ 10.9547” N 22° 20’ 31.2212” E, (14); Chisineu-Cris, AR, ES35, 94 m, 46° 31’ 20.9979” N 21° 31’ 0.8661” E, (13), R.C.; Chisindia, AR, ES82, 178 m, 46° 17’ 30.2461” N 22° 05’ 53.0279” E, (14); Cladova, AR, ES50, 147 m, 46° 08’ 8.5465” N 21° 39’ 21.5357” E, (13), R.C.; Conop, AR, ES60, 146 m, 46° 06’ 11.9515” N 21° 53’ 0.6068” E, (15); Dieci, AR, ES93, 175 m, 46° 19’ 3.3244” N 22° 14’ 57.5611” E, (13), R.C.; Cuias, AR, FR09, 187 m, 46° 00’ 11.0027” N 22° 17’ 42.1352” E, (15); Gura Vaii, AR, FS02, 175 m, 46° 17’ 38.2327” N 22° 23’ 54.5742” E, (14); Gurahont, AR, FS02, 181 m, 46° 16’ 11.9238” N 22° 20’ 30.2182” E, (14); Halalis, AR, ER99, 171 m, 46° 00’ 40.1765” N 22° 12’ 18.7335” E, (15); Iacobini, AR, FS02, 206 m, 46° 13’ 51.7195” N 22° 20’ 31.7174” E, (14); Lalasint, AR, ES70, 141 m, 46° 04’ 20.3702” N 22° 00’ 33.1303” E, (15); Lipova, AR, ES50, 129 m, 46° 05’ 22.9443” N 21° 41’ 39.1851” E, (15); Minisu de Sus, AR, ES72, 212 m, 46° 17’ 1.5470” N 22° 00’ 48.9078” E, (16); Madrigesti, AR, FS01, 259 m, 46° 12’ 10.8735” N 22° 18’ 11.0236” E, (14); Milova, AR, ES60, 145 m, 46° 06’ 20.2607” N 21° 48’ 7.5915” E, (15); Monorostia, AR, ES70, 148 m, 46° 06’ 13.1433” N 22° 00’ 45.9205” E, (15); Nadab, AR, ES34, 94 m, 46° 28’ 55.9967” N 21° 30’ 44.4203” E, (13), R.C.; Olari, AR, ES43, 102 m, 46° 23’ 11.7970” N 21° 32’ 45.4940” E, (13), R.C.; Nadas, AR, ES71, 188 m, 46° 13’ 26.5438” N 21° 56’ 49.2443” E, (16); Paiuseni, AR, ES82, 256 m, 46° 14’ 58.4845” N 22° 05’ 45.0319” E, (14); Plescuta, AR, FS02, 196 m, 46° 18’ 17.7284” N 22° 25’ 38.4547” E, (14); Pecica, AR, ES01, 99 m, 46° 10’ 10.7229” N 21° 04’ 13.8141” E, (13), R.C.; Radna, AR, ES50, 126 m, 46° 05’ 35.1287” N 21° 41’ 5.6703” E, (15); Sebis, AR, ES83, 138 m, 46° 22’ 23.5548” N 22° 07’ 53.3915” E, (14); Secas, AR, FS02, 242 m, 46° 13’ 45.0606” N 22° 18’ 17.2183” E, (14); Savarsin, AR, ER99, 171 m, 46° 01’ 1.1593” N 22° 14’ 9.5049” E, (15); Taut, AR, ES72, 138 m, 46° 17’ 39.9751” N 21° 54’ 48.3096” E, (13), R.C.; Vasoaia, AR, ES82, 457 m, 46° 15’ 19.8137” N 22° 03’ 48.8490” E, (14); Varadia de Mures, AR, ER89, 149m, 46° 00’ 42.3773” N 22° 09’ 36.0409” E, (15); Suncuius, BH, FT10, 297 m, 46° 56’ 48.3744” N 22° 32’ 10.9222” E, (17); Soimi, BH, ES87, 162 m, 46° 41’ 8.1164” N 22° 07’ 26.6496” E, (17); Sustiu, BH, FS15, 280 m, 46° 29’ 52.7797” N 22° 27’ 36.0573” E, (17); Beius, BH, FS06, 188 m, 46° 40’ 5.6298” N 22° 21’ 7.5962” E, (18); Balnaca, BH, FS19, 396 m, 46° 56’ 30.9508” N 22° 34’ 23.5973” E, (18); Bratca, BH, FS29, 326 m, 46° 55’ 35.9333” N 22° 36’ 18.7237” E, (18); Borz, BH, ES96, 157 m, 46° 40’ 28.1553” N 22° 11’ 18.6900” E, (17); Briheni, BH, FS05, 328 m, 46° 29’ 56.3712” N 22° 23’ 55.7915” E, (17); Bulz, BH, FS29, 558 m, 46° 54’ 40.9441” N 22° 40’ 24.1039” E, (18); Budureasa, BH, FS17, 354 m, 46° 40’ 43.0797” N 22° 29’ 44.4358” E, (17); Carpinet, BH, FS14, 316 m, 46° 27’ 18.1602” N 22° 29’ 40.8377” E, (17); Dumbravita de Codru, BH, ES86, 344 m, 46° 39’ 30.0953” N 22° 10’ 12.8729” E, (17); Finis, BH, FS06, 191 m, 46° 38’ 57.2529” N 22° 18’ 57.3842” E, (13), R.C.; Grosi, BH, FT11, 247 m, 47° 02’ 43.2784” N 22° 28’ 48.7193” E, (18); Lazuri, BH, FS08, 244 m, 46° 47’ 42.9190” N 22° 24’ 46.3169” E, (17); Oradea, BH, ET71, 126 m, 47° 03’ 23.0870” N 21° 55’ 52.0712” E, (6, 3, 19); Rontau, BH, ET70, 157 m, 47° 00’ 17.7027” N 21° 59’ 32.8948” E, (13, 19); Rosia, BH, FS08, 238 m, 46° 48’ 1.2403” N 22° 23’ 45.8876” E, (17); Santandrei, BH, ET61, 112 m, 47° 04’ 0.3953” N 21° 51’ 19.6406” E, (19, 13); Telechiu, BH, ET91, 190 m, 47° 03’ 8.6459” N 22° 16’ 25.5764” E, (18); Sanmartin, BH, ET70, 151 m, 47° 00’ 25.3736” N 21° 58’ 26.3074” E, (19, 13); Sannicolau de Beius, BH, ES87, 142 m, 46° 41’ 40.4233” N 22° 06’ 54.4709” E, (20); Tinaud, BH, FT01, 235 m, 47° 03’ 8.1839” N 22° 26’ 6.0530” E, (18); Tetchea, BH, FT01, 212 m, 47° 02’ 45.4667” N 22° 19’ 38.5912” E, (18); Uileacu de Beius, BH, ES97, 158 m, 46° 41’ 5.2256” N 22° 13’ 22.5164” E, (20); Urvind, BH, ET91, 193 m, 47° 04’ 1.5931” N 22° 17’ 2.0545” E, (18); Vadu Crisului, BH, FT10, 275 m, 46° 59’ 6.6024” N 22° 30’ 56.0535” E, (18); Urvis de Beius, BH, ES87, 193 m, 46° 41’ 26.1713” N 22° 09’ 29.9018” E, (17); Vascau, BH, FS14, 291 m, 46° 28’ 29.2453” N 22° 28’ 32.5476” E, (17); Sieu-Sfantu, BN, KN92, 274 m, 47° 09’ 4.1207” N 24° 17’ 54.1937” E, (13), R.C.; Bozies, BN, KN81, 409 m, 47° 02’ 4.8677” N 24° 10’ 38.7552” E, (13), R.C.; Brateni, BN, LM09, 354 m, 46° 54’ 54.4197” N 24° 23’ 44.7589” E, (13), R.C.; Chiochis, BN, KN80, 339 m, 46° 58’ 53.7301” N 24° 10’ 41.7443” E, (13), R.C.; Cociu, BN, KN83, 261 m, 47° 12’ 1.6029” N 24° 13’ 14.9815” E, (13), R.C.; Ghinda, BN, LN12, 441 m, 47° 08’ 10.1442” N 24° 34’ 27.8207” E, (13), R.C.; Ilva Mica, BN, LN24, 414 m, 47° 18’ 28.3434” N 24° 39’ 41.2244” E, (13), R.C.; Josenii Bargaului, BN, LN23, 464 m, 47° 12’ 37.8903” N 24° 40’ 41.9053” E, (13), R.C.; Manic, BN, KN80, 355 m, 46° 57’ 46.7940” N 24° 12’ 13.4953” E, (13), R.C.; Matei, BN, KN90, 337 m, 46° 58’ 43.7433” N 24° 15’ 52.6283” E, (13), R.C.; Micestii de Campie, BN, KM99, 352 m, 46° 51’ 37.9568” N 24° 18’ 37.2969” E, (13), R.C.; Petris, BN, LN11, 411 m, 47° 06’ 10.4106” N 24° 37’ 21.3984” E, (13), R.C.; Ragla, BN, LN11, 458 m, 47° 04’ 13.7513” N 24° 37’ 14.6747” E, (13), R.C.; Telciu, BN, LN05, 388 m, 47° 25’ 49.4149” N 24° 23’ 49.4486” E, (13), R.C.; Saniacob, BN, KN91, 399m, 47° 03’ 37.2258” N 24° 17’ 1.6995” E, (13), R.C.; Strugureni, BN, KN80, 332 m, 46° 58’ 50.8955” N 24° 12’ 24.5516” E, (13), R.C.; Tonciu, BN, LN00, 325 m, 46° 59’ 58.4583” N 24° 22’ 43.0334” E, (13), R.C.; Brasov, BV, LL95, 582 m, 45° 39’ 6.9047” N 25° 35’ 22.4623” E, (21, 3), R.C.; Alunis, CJ, GT01, 325 m, 47° 02’ 25.0370” N 23° 44’ 54.8925” E, (13), R.C.; Bont, CJ, GT20, 322 m, 46° 59’ 14.7741” N 23° 55’ 42.9734” E, (13), R.C.; Buru, CJ, FS95, 370, 46° 30’ 27.3686” N 23°

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Alexandru Strugariu, Iulian Gherghel, Ioan Ghira, Severus D. Covaciu-Marcov & Konrad Mebert

36’ 9.3733” E, (13), R.C.; Caseiu, CJ, GT13, 236 m, 47° 11’ 48.5326” N 23° 51’ 21.9720” E, (13), R.C.; Caprioara, CJ, FT91, 406 m, 47° 06’ 11.0169” N 23° 31’ 48.7036” E, (13), R.C.; Chinteni, CJ, FS99, 474 m, 46° 51’ 42.1610” N 23° 32’ 28.4578” E, (13), R.C.; Cluj-Napoca, CJ, FS98, 347 m, 46° 46’ 17.6062” N 23° 35’ 30.2692” E, (2, 3), R.C.; Cornesti, CJ, GT01, 340 m, 47° 02’ 10.9730” N 23° 40’ 44.3260” E, (13), R.C.; Dabaca, CJ, GT00, 314 m, 46° 58’ 16.0030” N 23° 40’ 34.3809” E, (13), R.C.; Filea de Jos, CJ, FS96, 548 m, 46° 37’ 10.9152” N 23° 30’ 22.9353” E, (13), R.C.; Gherla, CJ, GT21, 254 m, 47° 01’ 42.6095” N 23° 54’ 38.9353” E, (6, 3), R.C.; Gadalin, CJ, GS19, 307 m, 46° 50’ 24.6612” N 23° 50’ 57.1486” E, (13), R.C.; Geaca, CJ, KM79, 312 m, 46° 51’ 21.8649” N 24° 05’ 37.5645” E, (13), R.C.; Mihai Viteazu, CJ, GS15, 328 m, 46° 32’ 30.9199” N 23° 45’ 10.9173” E, (13), R.C.; Luna, CJ, GS25, 296 m, 46° 30’ 16.2239” N 23° 55’ 16.9186” E, (13), R.C.; Luncani, CJ, GS25, 282 m, 46° 28’ 20.9846” N 23° 57’ 9.2217” E, (13), R.C.; Ploscos, CJ, GS16, 352 m, 46° 38’ 36.6375” N 23° 50’ 29.3203” E, (13), R.C.; Rugasesti, CJ, GT13, 265 m, 47° 13’ 54.8536” N 23° 52’ 23.5737” E, (13), R.C.; Sacalaia, CJ, GT20, 310 m, 46° 57’ 54.8115” N 23° 55’ 13.4395” E, (13), R.C.; Suatu, CJ, GS28, 342 m, 46° 46’ 18.8497” N 23° 58’ 12.0379” E, (13), R.C.; Stejeris, CJ, GS14, 343 m, 46° 27’ 56.2112” N 23° 44’ 15.7125” E, (13), R.C.; Samboieni, CJ, KN71, 536 m, 47° 02’ 2.0961” N 24° 02’ 52.4334” E, (13), R.C.; Sanmartin, CJ, KN71, 367 m, 47° 00’ 50.0211” N 24° 04’ 11.9324” E, (13), R.C.; Sucutard, CJ, KM79, 292 m, 46° 53’ 48.8063” N 24° 04’ 13.3801” E, (13), R.C.; Tureni, CJ, GS06, 516 m, 46° 37’ 10.2549” N 23° 42’ 9.8812” E, (13), R.C.; Taga, CJ, KN70, 291 m, 46° 56’ 33.6735” N 24° 02’ 55.5835” E, (13), R.C.; Baraolt, CV, LM90, 479 m, 46° 04’ 33.8652” N 25° 35’ 59.2664” E, (13), R.C.; Batanii Mari, CV, LM90, 512 m, 46° 05’ 19.6049” N 25° 41’ 52.1847” E, (13), R.C.; Belin-Vale, CV, LL98, 542 m, 45° 55’ 55.9639” N 25° 36’ 24.9076” E, (13), R.C.; Chilieni, CV, ML07, 522 m, 45° 50’ 16.4659” N 25° 48’ 11.3671” E, (13), R.C.; Chichis, CV, ML06, 505 m, 45° 46’ 37.6606” N 25° 48’ 32.6477” E, (13), R.C.; Miclosoara, CV, LL99, 485 m, 46° 00’ 29.7086” N 25° 34’ 55.3422” E, (13), R.C.; Moacsa, CV, ML28, 541 m, 45° 52’ 10.5135” N 25° 58’ 10.6274” E, (13), R.C.; Ozun, CV, ML17, 513 m, 45° 47’ 57.9637” N 25° 50’ 54.8942” E, (13), R.C.; Padureni, CV, ML18, 558 m, 45° 53’ 10.3125” N 25° 55’ 53.9246” E, (13), R.C.; Turia, CV, ML29, 608 m, 46° 02’ 12.3339” N 26° 03’ 11.2275” E, (3), R.C.; Zalan, CV, ML09, 631 m, 45° 57’ 33.2617” N 25° 49’ 9.5297” E, (13), R.C.; Bejan-Tarnavita, HD, FR48, 234 m, 45° 56’ 16.1176” N 22° 49’ 38.2398” E, (13), R.C.; Bretea Muresana, HD, FR38, 179 m, 45° 56’ 17.4924” N 22° 42’ 44.0036” E, (13), R.C.; Bretea Romana, HD, FR55, 261 m, 45° 39’ 40.2779” N 23° 00’ 58.4455” E, (13), R.C.; Branisca, HD, FR38, 182 m, 45° 55’ 9.7167” N 22° 46’ 27.8842” E, (13), R.C.; Deva, HD, FR48, 190 m, 45° 52’ 55.6920” N 22° 54’ 19.3752” E, (6, 3), R.C.; Gradistea de Munte, HD, FR75, 527 m, 45° 37’ 59.8581” N 23° 13’ 1.0706” E, (13), R.C.; Pui, HD, FR64, 413, 45° 31’ 0.4805” N 23° 05’ 43.9514” E, (3), R.C.; Simeria, HD, FR57, 201 m, 45° 51’ 1.6002” N 23° 00’ 40.0437” E, (13), R.C.; Santuhalm, HD, FR58, 191 m, 45° 51’ 28.8906” N 22° 57’ 18.2264” E, (13), R.C.; Tarnava de Cris, HD, FS21, 232 m, 46° 11’ 25.9899” N 22° 37’ 15.4552” E, (13), R.C.; Zam, HD, FR19, 181 m, 46° 00’ 24.9649” N 22° 26’ 49.5311” E, (13), R.C.; Ditrau, HR, LM88, 752 m, 46° 48’ 28.4356” N 25° 30’ 19.3474” E, (13), R.C.; Izvoru Muresului, HR, MM06, 885 m, 46° 37’ 24.7772” N 25° 42’ 50.8694” E, (13), R.C.; Sancraieni, HR, MM12, 657 m, 46° 18’ 23.8626” N 25° 50’ 46.3005” E, (13), R.C.; Baia Mare, MM, FT98, 229 m, 47° 39’ 37.2297” N 23° 35’ 2.0699” E, (13), R.C.; Firiza, MM, FT99, 400 m, 47° 45’ 26.3107” N 23° 36’ 31.3223” E, (I. Ghira, pers. obs. 1995), R.C.; Lapus, MM, KN76, 385 m, 47° 29’ 43.1433” N 24° 00’ 38.9991” E, (13), R.C.; Saulia, MS, KM86, 348 m, 46° 38’ 18.9815” N 24° 12’ 57.9330” E, (13), R.C.; Branco venesti, MS, LM29, 415 m, 46° 51’ 24.4827” N 24° 44’ 53.8616” E, (13), R.C.; Cipau, MS, KM94, 281 m, 46° 26’ 57.6690” N 24° 16’ 44.5502” E, (13), R.C.; Gheorghe Doja, MS, LM04, 302 m, 46° 27’ 48.4409” N 24° 30’ 31.4877” E, (13), R.C.; Iclanzel, MS, KM95, 300, 46° 31’ 35.6090” N 24° 16’ 37.8064” E, (13), R.C.; Iernut, MS, KM84, 282 m, 46° 27’ 6.7054” N 24° 14’ 13.7689” E, (13), R.C.; Ludus, MS, KM75, 275 m, 46° 29’ 6.5778” N 24° 05’ 48.3916” E, (13), R.C.; Mogoaia, MS, KM87, 346 m, 46° 40’ 15.9005” N 24° 13’ 57.7655” E, (13), R.C.; Sarmasu, MS, KM88, 343 m, 46° 45’ 0.0667” N 24° 10’ 6.3278” E, (13), R.C.; Sabed, MS, LM07, 379 m, 46° 39’ 54.0978” N 24° 27’ 1.2546” E, (13), R.C.; Sighisoara, MS, LM32, 349 m, 46° 13’ 18.3588” N 24° 47’ 48.8013” E, (13), R.C.; Sanpaul, MS, KM94, 283^m, 27’ 22.1753” N 24° 21’ 3.6998” E, (13), R.C.; Taureni, MS, KM76, 299 m, 46° 34’ 47.9290” N 24° 04’ 46.0736” E, (13), R.C.; Zau de Campie, MS, KM86, 304 m, 46° 36’ 52.8379” N 24° 07’ 44.6396” E, (13), R.C.; Viilor, MS, LM32, 362 m, 46° 14’ 46.2960” N 24° 49’ 1.2401” E, (13), R.C.; Avrig, SB, KL96, 384 m, 45° 43’ 37.8830” N 24° 22’ 39.7680” E, (13), R.C.; Boita, SB, KL85, 373 m, 45° 38’ 0.8180” N 24° 15’ 38.0805” E, (13), R.C.; Laslea, SB, LM11, 343 m, 46° 12’ 24.2673” N 24° 39’ 28.3824” E, (13), R.C.; Lotrioara, SB, KL85, 470 m, 45° 34’ 26.5975” N 24° 13’ 59.8482” E, (13), R.C.; Porumbacu de Jos, SB, LL07, 395 m, 45° 45’ 32.1801” N 24° 27’ 19.0745” E, (13), R.C.; Sibiu, SB, KL77, 433 m, 45° 47’ 39.9922” N 24° 08’ 57.4472” E, (3), R.C.; Turnu Rosu, SB, KL85, 396 m, 45° 38’ 22.2076” N 24° 18’ 0.5926” E, (3), R.C.; Buciumi, SJ, FT51, 340 m, 47° 02’ 40.9717” N 23° 02’ 43.5824” E, (13), R.C.; Ciumarna, SJ, FT62, 293 m, 07’ 26.8828” N 23° 07’ 52.3897” E, (13), R.C.; Jibou, SJ, FT73, 191 m, 47° 15’ 36.5404” N 23° 15’ 27.1548” E, (13), R.C.; Huseni, SJ, FT32, 273 m, 47° 11’ 3.7274” N 22° 48’ 15.2242” E, (13), R.C.; Lupoaia, SJ, FT72, 219 m, 47° 11’ 28.3040” N 23° 15’ 12.2679” E, (13), R.C.; Napradea, SJ, FT74, 195 m, 47° 21’ 49.7535” N 23° 19’ 20.5771” E, (13), R.C.; Paduris, SJ, FT81, 394 m, 47° 05’ 50.7445” N 23° 24’ 41.2000” E, (13), R.C.; Recea Mica, SJ, FT42, 311 m, 47° 11’ 21.5145” N 22° 57’ 52.7725” E, (13), R.C.; Pria, SJ, FT41, 389 m, 47° 02’ 52.2709” N 22° 53’ 20.1704” E, (13), R.C.; Salatig, SJ, FT64, 203 m, 47° 21’ 51.8313” N 23° 08’ 22.9193” E, (13), R.C.; Somes-Odorhei, SJ, FT74, 183 m, 47° 19’ 17.2498” N 23° 15’ 51.0886” E, (13), R.C.; Sanpetru Almasului, SJ, FT71, 256 m, 47° 04’ 57.5889” N 23° 20’ 15.8968” E, (13), R.C.; Tranis, SJ, FT74, 184 m, 47° 19’ 56.8446” N 23° 18’ 18.5486” E, (13), R.C.; Zalau, SJ, FT52, 265 m, 47° 10’ 46.1028” N 23° 03’ 26.6042” E, (13), R.C.; Ady Endre, SM, FT27, 121 m, 47° 34’ 53.4030” N 22° 36’ 58.1652” E, (13), R.C.; Berveni, SM, FT19, 117 m, 47° 45’ 21.4556” N 22° 28’ 23.7972” E, (13), R.C.; Bocicau, SM, FU62,

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139 m, 48° 05’ 41.3404” N 23° 09’ 10.7438” E, (13), R.C.; Calinesti-Oas, SM, FU70, 234 m, 47° 54’ 55.4739” N 23° 17’ 31.6530” E, (13), R.C.; Certeze, SM, FU80, 263 m, 47° 54’ 10.6938” N 23° 28’ 10.2730” E, (13), R.C.; Cauas, SM, FT16, 116 m, 47° 34’ 10.7212” N 22° 32’ 41.0830” E, (13), R.C.; Dacia, SM, FT28, 115 m, 47° 43’ 59.3478” N 22° 39’ 23.6626” E, (13), R.C.; Domanesti, SM, FT18, 114 m, 47° 42’ 48.9564” N 22° 35’ 24.8006” E, (13), R.C.; Ghenci, SM, FT17, 119 m, 47° 37’ 52.8433” N 22° 31’ 43.3843” E, (13), R.C.; Luna, SM, FU80, 263 m, 47° 51’ 3.9033” N 23° 25’ 31.7989” E, (13), R.C.; Lucaceni, SM, FT18, 113 m, 47° 44’ 34.9715” N 22° 28’ 19.9073” E, (13), R.C.; Orasu Nou, SM, FU70, 154 m, 47° 50’ 1.8025” N 23° 17’ 36.9655” E, (13), R.C.; Tur, SM, FU70, 180 m, 47° 52’ 58.6262” N 23° 23’ 7.9477” E, (13), R.C.; Tiream, SM, FT17, 121 m, 47° 36’ 49.1561” N 22° 28’ 11.7340” E, (13), R.C.; Urziceni, SM, FT08, 119 m, 47° 44’ 0.8360” N 22° 24’ 25.3510” E, (13), R.C.; Lugoj, TM, ER75, 123 m, 45° 41’ 9.1242” N 21° 54’ 8.6117” E, (6, 3), R.C.; Nadrag, TM, ER95, 284 m, 45° 38’ 51.9196” N 22° 11’ 34.7015” E, (6, 3), R.C.; Timisoara, TM, ER16, 95 m, 45° 45’ 31.4902” N 21° 13’ 47.6902” E, (6, 3), R.C. ROMANIAN MOLDAVIA Lilieci, BC, MM96, 174 m, 46° 37’ 41.0836” N 26° 52’ 21.7688” E, (22); Poiana Sarata, BC, MM51, 441 m, 46° 08’ 36.7303” N 26° 27’ 21.5481” E, (3), R.C.; Racaciuni, BC, NM03, 129 m, 46° 19’ 42.3739” N 27° 00’ 49.3748” E, (22); Galati, GL, NL83, 24 m, 45° 26’ 13.1697” N 28° 03’ 23.7194” E, (23); Tarcau, NT, MM39, 394 m, 46° 53’ 17.8471” N 26° 07’ 58.6509” E, (24, 25), Extinct acc. Gherghel et al. (2008) DOBRUDJA Albesti, CT, PJ15, 29 m, 43° 48’ 10.3950” N 28° 25’ 43.9732” E, (3, A. Strugariu, pers. obs. 2004); Cernavoda, CT, NK81, 15 m, 44° 20’ 32.8141” N 28° 02’ 1.1294” E, (12, 3), R.C.; Bugeac, CT, NJ38, 9 m, 44° 05’ 44.5828” N 27° 26’ 13.3623” E, (3), R.C.; Cochirleni, CT, NK70, 30 m, 44° 16’ 32.3184” N 28° 00’ 7.3410” E, (26); Constanta, CT, PJ39, 48 m, 44° 10’ 35.3686” N 28° 37’ 58.6360” E, (27); Dunareni, CT, NJ69, 62 m, 44° 12’ 9.2624” N 27° 47’ 35.7574” E, (28); Floriile, CT, NJ68, 86 m, 44° 08’ 38.3284” N 27° 50’ 7.4574” E, (26); Istria, CT, PK33, 22 m, 44° 34’ 26.3497” N 28° 42’ 54.6380” E, (29, 30); Mamaia-Sat, CT, PK20, 9 m, 44° 17’ 17.9669” N 28° 36’ 53.4436” E, (27); Mamaia, CT, PJ29, 4 m, 44° 14’ 7.4413” N 28° 37’ 39.0594” E, (31, 27); Mangalia, CT, PJ25, 15 m, 43° 48’ 54.3454” N 28° 34’ 46.9819” E, (32, 3, 27); Navodari, CT, PK20, 6 m, 44° 19’ 26.0082” N 28° 36’ 36.5824” E, (T. Sahlean, observed in 1988, pers. comm. 2009), R.C.; Oltina, CT, NJ59, 31 m, 44° 09’ 48.3199” N 27° 40’ 13.8621” E, (3), R.C; Vadu, CT, PK32, 14 m, 44° 27’ 2.7735” N 28° 44’ 11.3527” E, (27); Vlahii, CT, NJ69, 26 m, 44° 12’ 10.9804” N 27° 52’ 4.8257” E, (26); Atmagea, TL, PK18, 210 m, 44° 57’ 54.5912” N 28° 26’ 5.1184” E, (12, 3), R.C.; Babadag, TL, PK37, 24 m, 44° 53’ 37.5630” N 28° 43’ 22.5568” E, (32, 3, 27); Caraorman, TL, PK89, -1 m, 45° 04’ 31.3116” N 29° 23’ 42.9066” E, (I. Ghira, pers. obs. 1995), R.C.; Enisala, TL, PK47, 14 m, 44° 52’ 54.0499” N 28° 49’ 12.3769” E, (3, 27); Isaccea, TL, PL11, 20 m, 45° 16’ 22.3487” N 28° 27’ 38.3557” E, (27); Jurilovca, TL, PK45, 15 m, 44° 45’ 23.7364” N 28° 52’ 39.5323” E, (27); Mahmudia, TL, PK69, 25 m, 45° 05’ 10.2103” N 29° 05’ 8.1864” E, (12, I. Ghira, pers. obs. 1995), R.C.; Nufaru, TL, PL50, 27 m, 45° 08’ 50.2871” N 28° 55’ 16.4589” E, (27); Murighiol, TL, PK78, 6 m, 45° 02’ 14.6090” N 29° 10’ 3.4558” E, (A. Strugariu, pers. obs. 2007); Parches, TL, PL20, 32 m, 45° 12’ 52.5426” N 28° 35’ 35.5726” E, (27); Rachelu, TL, PL01, 35 m, 45° 17’ 14.7226” N 28° 19’ 13.9939” E, (27); Revarsarea, TL, PL01, 27 m, 45° 16’ 37.8545” N 28° 23’ 29.8932” E, (27); Sarichioi, TL, PK47, 23 m, 44° 56’ 39.3732” N 28° 51’ 6.2573” E, (27); Smardan, TL, NL71, 5 m, 45° 17’ 8.1793” N 28° 00’ 22.6367” E, (27, 33); Sfantu Gheorghe, TL, QK07, 1 m, 44° 53’ 47.0707” N 29° 35’ 47.1116” E, (29, A. Strugariu, pers. obs. 2007); Somova, TL, PL30, 17 m, 45° 11’ 25.3380” N 28° 39’ 52.5450” E, (27); Tulcea, TL, PL40, 17 m, 45° 10’ 39.1972” N 28° 48’ 7.2662” E, (12, 30, 27); Zebil, TL, PK37, 8 m, 44° 56’ 39.7905” N 28° 46’ 7.5583” E, (27); Popina, TL, PK58, 26 m, 44° 58’ 6.8591” N 28° 58’ 33.5435” E, (29), R.C.; Gura Portitei, TL, PK54, 0 m, 44° 40’ 38.1433” N 28° 59’ 18.4770” E, (29), R.C. SOUTHERN ROMANIA Calarasi, CL, NJ29, 22 m, 44° 11’ 31.7833” N 27° 20’ 20.7232” E, (34); Dorobantu, CL, MJ99, 19 m, 44° 13’ 16.4843” N 26° 57’ 1.7744” E, (I. Ghira, pers. obs. 1995), R.C.; Clejani, GR, LK90, 83 m, 44° 19’ 3.0812” N 25° 42’ 7.8698” E, (35); Calugareni, GR, MJ19, 50 m, 44° 10’ 21.0704” N 25° 59’ 53.2711” E, (35); Comana, GR, MJ39, 49 m,44° 10’ 18.0252” N 26° 08’ 52.1172” E, (35); Bucuresti, B, MK22, 88 m, 44° 26’ 12.1750” N 26° 06’ 8.8910” E, (3, 36), rediscovered (T. Sahlean, pers. comm. 2009) Appendix reference list Covaciu-Marcov et al. 2005a (1), Mehely 1918 (2), Fuhn & Vancea 1961 (3), Iftime 2005b (4), Sahlean et al. 2008 (5), Fejervary-Langh 1943 (6), Frivaldski 1823 (7), Calinescu 1931 (8), Cruce 1971 (9), Covaciu-Marcov et al. 2009 (10), Fuhn 1970 (11), Kiritzescu 1901 (12),Ghira et al. 2002 (13), Covaciu-Marcov et al. 2007a (14), Covaciu-Marcov et al. 2005b (15), Covaciu-Marcov et al. 2007b (16), Covaciu-Marcov et al. 2003a (17), Co-

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vaciu-Marcov et al. 2003b (18), Covaciu-Marcov et al. 2000 (19), Covaciu-Marcov et al. 2003c (20), Bielz 1888 (21), Ghiurca et al. 2006 (22), Strugariu & Gherghel 2008 (23), Băcescu & Matei 1958 (24), Ionescu et al. 1968 (25), Covaciu-Marcov et al. 2008a (26), Covaciu-Marcov et al. 2006a (27), Peterscu et al. 2003 (28), Török 1995, 2004 (29, 30), Mertens 1957 (31), Băcescu 1934 (32), Strugariu et al. 2008c (33), Iftime & Iftime 2007, 2008 (34, 35), Iftime 2001 (36)

Authors Alexandru Strugariu, Iulian Gherghel, Faculty of Biology, “Alexandru Ioan Cuza” University, Carol I. Blvd. Nr. 20 A, 700 556, Iaşi, Romania, e-mail address: [email protected]; Ioan Ghira, Faculty of Biology-Geology, “Babeş-Bolyai” University, Kogălniceanu Str., 400 084, Cluj-Napoca, Romania; Severus D. Covaciu-Marcov, Faculty of Sciences, University of Oradea, Universităţii Str. No. 1, 410 087 Oradea, Romania; Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland

287

MERTENSIELLA 18

288-297

20 September 2011

ISBN 978-3-9812565-4-3

The Dice Snake (Natrix tessellata) in Bulgaria: Distribution and Morphology Borislav Naumov, Nikolay Tzankov, Georgi Popgeorgiev, Andrei Stojanov & Yurii Kornilev Abstract. This is the first comprehensive study on the dice snake (Natrix tessellata) in Bulgaria. To assess its current distribution, we combined published data (n = 191) and unpublished observations (n = 188) collected between 1985 and 2008 and mapped 379 localities on a 10 × 10 km UTM grid. The species has wide distribution in Bulgaria, found in 22% of 10 × 10 km UTM squares. It inhabits areas below 1000 m a.s.l., with two records of 1100 m and 1420 m a.s.l. Analysis of 13 pholidosis traits of 22 males and 44 females revealed a low and typical level of sexual dimorphism with significant differences in the number of ventrals and subcaudals. We suggest that N. tessellata recently extended its range in Bulgaria along the Black Sea coast and major rivers. Key words. Natrix tessellata, dice snake, distribution, Bulgaria, pholidosis, sexual dimorphism, UTM

Introduction The first account for Natrix tessellata in Bulgaria was provided by Werner (1898), who reported of finding the species in the city of Varna. In the beginning of the 20th century Vasil Kovachev published several articles and one monograph on the Bulgarian herpetofauna (e.g. Kovatscheff 1903, Kowatscheff 1905, Kovachev 1912), in which numerous localities for N. tessellata were listed. The first mapping and summary on the distribution of the species in Bulgaria was made by Buresch & Zonkow (1934). Afterwards numerous publications provided single localities for N. tessellata along with data on other reptile and amphibian species (e.g. Müller 1939, Beschkov 1961, Petrov et al. 2001). Naumov & Stanchev (2010) made the first attempt at mapping the species using a UTM grid. In Bulgaria the morphology and ecology of dice snakes have received little attention. Only Beshkov (1978) published data on the biology and ecology of N. tessellata from the Maleshevska Mountain (SW Bulgaria), and Kabisch (1966) published short notes on the feeding of this species. The shortcomings of data about the dice snake in Bulgaria sets our incentive to analyze all available information on the distribution and pholidosis of N. tessellata in this country. Materials and Methods To map the distribution of Natrix tessellata in Bulgaria, we used data from our personal field observations between 1985 and 2008, unpublished data provided by colleagues, as well as all available literature. The distribution data were transferred on a 10 × 10 km UTM grid. Unlike our personal observations, the precise altitude of most published localities is unknown. Therefore,

when possible, we assigned locations to altitude bands of 500 m. Furthermore, we analyzed 13 pholidosis traits of 66 dice snakes (22 males and 44 females): number of ventrals (V; after Dowling 1951), subcaudals (Scd), dorsal scale rows at neck level (D1: one head-length posterior of the jaw, whereas head-length is measured from the tip of the snout to the posterior end of the jaw), at midbody (D2: mid-point between head and cloaca), and the anal region (D3: one head-length anterior to the cloaca), supralabials (Slab: right + left), sublabials (Sublab: right + left), preoculars (Preoc: right + left), postoculars (Postoc: right + left), first temporals (T1: right + left; first row behind the postoculars), second temporals (T2: right + left; second row), preventrals (Prv: gular scales anterior to the ventrals that are broader than longer), and anal scute (An: divided / undivided). The difference between sexes was analyzed using ANOVA (Statistica v7.0; StatSoft 2004). The preserved specimens are in the scientific collections of the National Museum of Natural History in Sofia (n = 62) and the Regional Natural History Museum in Plovdiv (n = 4). The specimens were collected from numerous localities throughout Bulgaria. Results and Discussion A set of 191 specific localities (occurring in 133 UTM squares) of Natrix tessellata in Bulgaria are reported in 61 publications, listed in Appendix 1 and the reference section. In Appendix 2 we provide previously unpublished data on 188 localities (165 UTM squares), collected between 1985 and 2009. All together, these localities fall within 271 UTM squares based on a 10 × 10 km grid, which represents roughly 22% of all squares within Bulgaria (Fig. 1). The distribution of the localities suggests that the species is wide-ranging across Bulgaria.

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Borislav Naumov, Nikolay Tzankov, Georgi Popgeorgiev, Andrei Stojanov & Yurii Kornilev

Fig. 1. Distribution of Natrix tessellata in Bulgaria by UTM grid.

We hypothesize that temperatures are a major limiting factor for species survival and distribution in Bulgaria. For example, the highest number of localities is found along the relatively warm Black Sea coast and the valleys of Maritsa and Struma rivers (Fig. 2). We have studied these regions extensively (see Figs. 3a, b and 4) and suggest that they provide an optimal habitat for foraging and thermoregulation for dice snakes (e.g. Kabisch 1966, Nöllert et al. 1986, Thieme 1986). During multiple visits between 1990 and 2009 to the Black Sea coast and the nearby lakes, we often observed high densities of dice snakes, reaching sometimes hundreds of individuals (including juveniles) per 100 m transect, e.g. in the Yaylata place (northeast of Varna), the Protected Area “Poda” near Burgas, and Zmiiskiya ostrov (Snake Island, southeast of Burgas). In contrast, our observations suggest that the density of N. tessellata in the upper portions of the rivers in the interior of the country is several times lower than in the lowlands. For example, in a small open stream in the western Stara Planina Mountain, visited regularly for eight years during an intensive study on the yellow-bellied toad (Bombina variegata; Beshkov & Jameson 1980), only two dice snakes were observed (V. Beshkov, pers. comm.). We presume that these were not individuals from a potential reproductive population nearby, but rather were caught while

carrying out short-term movement between more suitable habitats or were simply exploring new habitats. However, only a study focusing more closely on the dice snake in that area would possibly provide more conclusive results. Interestingly, no records of N. tessellata are known from the regions of Dobrudzha and Ludogorie (square NJ, Figs. 1 and 2). The lack of data for Dobrudzha and Ludogorie is likely due to insufficient search efforts, as suitable water bodies are available in the form of numerous micro-reservoirs well suited for dice snakes. However, a possible limiting factor for the species distribution in that area is the lack of rivers to serve as possible dispersal corridors to these water bodies. We were able to assign 374 locations from our personal data and the available literature into altitude belts. Of those, 320 localities fall into the belt of 0–500 m a.s.l., 52 are in the belt of 500–1000 m a.s.l., and only two originate from altitudes higher than 1000 m a.s.l. In northern Bulgaria (north of the Stara Planina ridge) we have observed N. tessellata only on three occasions at altitudes above 500 m a.s.l. (600 m at Vasilyovo, 510 m at Cherni Osam, and 630 m at Etropole). Without providing specific localities, Yankov (2001) mentioned that the dice snake is rarely observed in the rivers of the “Central Balkan” National Park (Middle Stara Planina) up to about

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Fig. 2. Map of Bulgaria with major landmarks.

700 m a.s.l. It is not clear, however, whether that reference includes the rivers on the northern slope of the ridge, i.e. those flowing into northern Bulgaria. Hence, we tentatively agree that 700 m is the maximum known altitude for dice snakes in northern Bulgaria. In contrast, there are substantially more records of dice snakes

above 500 m a.s.l. from southern Bulgaria (south of the ridge of Stara Planina). We attribute this to the much larger area above 500 m a.s.l. in southern than northern Bulgaria and the greater herpetological search effort in southern Bulgaria. There are only two records of dice snakes observed above 1000 m a.s.l. (1100 m a.s.l., above

Fig. 3. Black Sea coast near Shabla (UTM: PJ), 15 July 2010; (a) beach area, (b) backwater. Photos: Borislav Naumov.

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Borislav Naumov, Nikolay Tzankov, Georgi Popgeorgiev, Andrei Stojanov & Yurii Kornilev

Fig. 4. Struma River in Kresna Gorge (UTM: FM), 3 September 2008. Photo: Borislav Naumov.

Vlahi village, Pirin Mountain, Beschkov 1961; 1420 m a.s.l., near Kirilova polyana, Rila Mountain, Tzankov et al., in press). Cited maximum altitudes from two neighboring countries are as follows: 1000 m a.s.l. for Romania (Fuhn & Vançea 1961), and 2200 m a.s.l. for the mountains at Zagori in continental Greece (Bruno & Maugeri 1990), albeit latter likely indicates rather a single, erratic record, possibly from a specimen migrating to or from a hibernation site higher up the slope from small alpine lakes at 1770, 1950 m a.s.l., as there are no suitable habitats at elevation < 2000 m a.s.l. on these mountains. But even taking into account a lower vertical distribution in Greece, e.g. between 1500 to 2000 m a.s.l., it would render support to our hypothesis that the vertical distribution of dice snakes in the Balkans is negatively correlated with latitude. We believe that higher localities in Bulgaria do not provide suitable climatic conditions for the survival of dice snakes. In Bulgaria, mountains typically have small fast-flowing rivers that contain cold water and predominantly shady banks preventing suitable areas for thermoregulation and embryogenesis. Therefore, the lack of any records of dice snakes likely reflects real absence.

The observed level of morphological variation is relatively low but typical for that species (see examples in Gruschwitz et al. 1999). Both sexes differ significantly in their mean number of ventrals (V) and subcaudals (Scd; Table 1). In males, the V (ANOVA: F = 58.86; P < 0.001) vary from 165 to 179 with a mean of 173 ± 3.55, whereas females exhibit smaller numbers of V, which vary from 161 to 174 with a mean of 167 ± 3.06. The Scd (ANOVA: F = 101.26; P < 0.001) vary in males from 67 to 74 with a mean of 71 ± 2.20, and in females from 53 to 71 with a mean of 62 ± 3.66. This sexual dimorphism is typical for Natrix tessellata and concurs with analyses across its range in Europe and the Middle East (Mebert 1993, Gruschwitz et al. 1999). The difference in preoculars (Preoc) is also statistically significant, but the results from the Levene and Brown–Forsythe’s tests for the homogeneity of variances suggest this trait should not be used to separate between sexes. No other traits show significant differences. Morphological similarity to western and central European N. tessellata (Mebert 1993, Gruschwitz et al. 1999), molecular, and subfossil data support the notion that this species expanded rapidly northward after the

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Table 1. Variations (ANOVA) of pholidosis between male and female Natrix tessellata. St.d. is ±1 standard deviation. See text for explanation of pholidosis characters.

V Scd D1 D2 D3 Slab Sublab Preoc Postoc T1 T2 Prv An

Mean 173.32 71.00 19.36 19.09 17.00 16.14 19.86 5.09 7.68 2.00 4.23 4.18 2.00

Males (n = 22) Min Max 165 179 67 74 19 21 19 21 17 17 15 18 18 21 4 6 6 10 2 2 3 6 3 5 2 2

St.d. 3.55 2.20 0.73 0.43 – 0.56 0.64 0.92 0.95 – 0.75 0.79 –

end of the last glaciation (Würm) along the Danube basin and the Black Sea coast. The dice snakes must have colonized the currently isolated populations in Germany and the Czech Republic between the beginning of the Holocene up until their climatic optima (the Atlanticum, 8 to 5 ka BP, and the Subboreal, 5 to 2.5 ka BP). Holocene fossil records of dice snakes from the upper Danube valley in Germany (Markert 1976) corroborate the rapid postglacial dispersal of this species. This concurs also with the low differentiation in mtDNA between central and eastern European dice snakes (Guicking et al. 2006, Guicking et al. 2009, Guicking & Joger 2011). Guicking & Joger (2011) suggested that Turkey and the Black Sea region (including Bulgaria) served as a refugium for dice snakes during the last Würm glaciation, a region where the climate was ameliorated by the influence of the water body (Tarasov et al. 2000).

Mean 167.14 62.46 19.18 19.07 17.00 16.00 19.91 5.61 7.80 2.00 4.07 4.00 2.00

Females (n = 44) Min Max 161 174 53 71 19 21 19 21 17 17 14 17 18 21 4 7 6 9 2 2 3 5 2 6 2 2

St.d. 3.06 3.66 0.54 0.33 – 0.43 0.64 0.75 0.82 – 0.33 0.81 –

p 20 meters

Natrix tessellata % (n = 192) 37.0 41.1 18.8 3.1

Natrix natrix % (n = 238) 27.3 36.6 23.1 13.0

Presence of fish No No No Yes No No Yes Yes Yes

Presence of anuran Scarce Abundant Abundant Scarce Abundant Temporary No Abundant Temporary

Salinity level Freshwater Freshwater Freshwater Brackish-Saltwater Freshwater Freshwater-brackish Saltwater Freshwater Brackish

frogs, probably are underrepresented in the samples due to the difficulty to recognize them from a moving car. The full list is presented in Table 3. Nearly 44% (n = 103) of all road casualties were N. tessellata. A 2.1 km segment of the road that passes between the Prokopos Lagoon and Mavra Vouna Hill was responsible for a disproportionably large percentage of road casualties, the majority of wich were N. tessellata (Fig. 4). From 3 to 7 systematic road surveys were conducted monthly from January 2003 until December 2004 to estimate the mortality rate on this road section. The results were pooled as daily mortality rates for N. tessellata per month and are pre-

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Habitat Differences in Dice and Grass Snakes on the Peloponnese

Tab. 3: Taxa and numbers of individuals of reptiles and amphibians found dead on the network of paved and unpaved roads in the Strofylia area between January 2003 and June 2004. Those numbers do not include road casualties from the 2.1 km road segment north of Prokopos Lagoon where more systematic road surveys were conducted. Observations by B. Trapp (pers. comm.) add following species as casualties from that road, but not listed in the table: Ablepharus kitaibeli, Lissotriton graecus, and Bufo bufo. Amphibians Bufo (sensu lato) viridis Hyla arborea Pelobates syriacus Pelophylax or Rana sp. Reptiles Turtles and tortoises Emys orbicularis Mauremys rivulata Testudo hermanni Testudo marginata Lizards Pseudopus apodus Anguis cephallonicus Podarcis taurica Lacerta trilineata Snakes Hierophis gemonensis Platyceps najadum Elaphe quatuorlineata Zamenis situla Zamenis longissimus Malpolon insignitus Natrix natrix Natrix tessellata Vipera ammodytes Total

19 7 9 8

2 6 3 1 3 1 9 7 9 5 5 4 1 10 18 103 6 236

sented in Figure 5. The mean daily mortality rate from all counts was 3.25 individuals/day. There was a peak in spring (March to May) after which the numbers were relatively stable through the summer and most of the autumn. Road mortality sharply declined in winter. The additional road surveys in 2005–2006 showed no significant difference of mean daily mortality rate for the relevant months compared to the counts in 2003 and 2004 (x2 = 0.470, 0.25 < Pp < 0.50). A comparison of dead and alive individuals on the road during the survey days shows a strong relationship of 0.933 (F = 15.84, P < 0.0001). This means that road activity greatly increases the risk of being killed (coefficient of determination = 0.870). Active individuals were observed from February until November. Only one N. tessellata was found moving on land in January at a temperature of 14 °C (shadow) and water temperature of 10.5 °C. The beginning of the active season was around the mid-February. The highest frequency of snakes was

306

Fig. 4. Road casualities of Natrix tessellata and N. natrix. Photo: Benny Trapp.

Fig. 5. Mean daily mortality rate per month of Natrix tessellata on a 2.1 km road segment north of Prokopos Lagoon, Strofylia, Greece. Data collected during surveys in 2003 and 2004.

recorded from March until May with a decrease in summer and a second much lower peak in September and October, which involved mainly younger individuals of less than 45 cm including a few newborns under 25 cm (Fig. 6). Activity ceased after the first 10 days of November and by then, most of the snakes had retreated to their hibernacula where they remained for almost three months. From February until the mid of June most individuals were observed during the midday (43%) and morning (32%). This changed drastically in the summer and up to October, when most individuals were recorded in the evening and at night (59%). During two days (18 April 2003 and 29 October 2004), the search for active snakes was intensified by repeating road surveys every 2 hours for a 24 h period. The activity pattern that was observed in those two days was more or less similar with the previous results (Fig. 7). During the 24 h-survey in April there was a constant presence of snakes during the day with a sharp decline after dark, whereas in October the snakes were present in the morning hours

Yannis Ioannidis & Konrad Mebert

Discussion

Fig. 6. Daily mean number of active Natrix tessellata per month (bars) along a 2.1 km road segment north of Prokopos Lagoon, Strofylia, Greece, plotted against minimum and maximum water levels (triangles) and mean air temperatures (circles). Grey part of the bar represents adults and white part individuals under 45 cm total length. Data collected during surveys in 2003 and 2004.

Fig. 7. Number of active Natrix tessellata during road counts on 18 April 2003 (triangles) and 29 October 2004 (squares) along a 2.1 km road segment north of Prokopos Lagoon, Strofylia, Greece. The horizontal axis is time in GMT+2.

with a decline at noon and a significant increase around dusk and at the early night hours. The salinity of the Prokopos lagoon varies significantly during the year. In 2004 an environmental station 20 meters from the northern coast, where the road surveys were conducted and a connection to the sea exists, measured the salinity of the water. It ranged from 0.7 to 28 ppm (= psu) with the exception of the period from July to September, when the salinity increased to values between 32 to 43 ppm. A second station in the southern part of the lagoon where the majority of freshwater is collected, recorded similar fluctuations but the maximum salinity was with 29 ppm much lower. N. tessellata were active in the northern part of the lagoon even when the salinity reached saltwater levels.

The degree of habitat overlap between the two species is low in Strofylia, even though both species can be found in a similar variety of aquatic habitats and do not exclude each other (weak correlation of a negative Spearman’s coeffcient), but they inhabit the variety of aquatic habitats to different proportions. For example, Natrix tessellata prefers the larger water bodies that support large fish populations and avoids areas with temporary water, such as streams, ponds, and wet meadows. It seems to cope well with increased levels of salinity and the densest populations have been observed in a lagoon that yields brackish to saltwater during most of the year (Fig. 8). In contrast, N. natrix is distributed more evenly across the various water types. It appears to frequent similarly often temporary and permanent water bodies and prefers smaller open water bodies with abundance of shore- and floating-vegetation that have the largest breeding concentrations of frogs and toads such as ponds, wet meadows, marsh and shallow lake. A similar low overlap in the use of water habitats between N. tessellata and N. natrix has also been reported from southern Croatia (Janev Hutinec & Mebert 2011). The low interspecific overlap was attributed to their different availability and preference of prey, as N. tessellata was feeding exclusively on fish and N. natrix mostly on amphibians. In sympatric populations from Central Italy, N. tessellata is feeding exclusively on fully aquatic prey consisting of fish and tadpoles, whereas the more terrestrial N. natrix feeds to approximately 90% on amphibians, including migrating toads (Luiselli & Rugiero 1991, Filippi et al. 1996). An increased underwater vision ability of N. tessellata compared to N. natrix has been technically investigated and confirmed by Schaeffel & Mathis (1991). The availability of preferable prey items in correlation with distinct behavior was not studied in the Strofylia area, but could also explain the differences in habitat preferences (see Tab. 1 for availability and abundance of prey types in different habitats). For example, the absence of N. tessellata from the surveyed stream is not understandable at the first glance, as this species has been observed in many rivers and streams throughout Greece (Trapp 2007, Valakos et al. 2008). However, stream-lake segregation has also been observed in the region of Prespa Lake, northern Greece, where N. tessellata is considered more common in or near the lakes and N. natrix is found in drainage ditches and streams (Ioannidis & Bousbouras 1997). But elsewhere, N. tessellata also inhabits streams (see refs. in Gruschwitz et al. 1999) or simply occupies all available open aquatic habitats, lentic and lotic systems (Mebert et al. 2011a). For example, N. tessellata thrives in three Mediterranean streams of central Italy with permanent or temporary water, where it feeds up to 90% on fish (Luiselli et al. 2007). At our study site in Strofylia, the observed absence of fish and the scarcity of frogs in the studied stream probably render that aquatic habitat un-

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Habitat Differences in Dice and Grass Snakes on the Peloponnese

Fig. 8. A Natrix tessellata hunting in Prokopos Lagoon, a large brackish water body with a high abundance of fish. Photo: Benny Trapp.

suitable for N. tessellata and supports only a low number of N. natrix. Although both species have been observed mainly near or in the water, N. tessellata seems to exhibit a more aquatic behavior than N. natrix as was often reported from other areas (e.g. Filippi et al. 1996, Gruschwitz et al. 1999). More than a third of N. tessellata (37%) were observed in the water. Other studies have reported much higher frequencies of observations in the water (e.g. Lenz & Gruschwitz 1993, Janev Hutinec & Mebert 2011), but this could be related to the sampling methods, as in both refered studies sampling was concentrated directly along the coast or in the water. In this study, the sampling time was spent proportionately to the size of each habitat and the water area represented a relatively small portion ( 30 °C) and a cool water bath. The body temperature decrease was 2.2 °C/min and the increase followed by 0.3–0.4 °C/min untill a preferred body temperature of about 28 °C was reached. Key words. Natrix tessellata, body temperatures, environmental impact, heating and cooling rate, Samara province.

Introduction In Russia, the dice snake, Natrix tessellata, reaches the 54° Northern Latitude along the Volga River as far north as Samara oblast (province) , where they have been documented as early as 1636 (Olearius 1906). Putative findings of dice snakes at localities farther north in Ulyanovsk province (Osipova 1993) and the Republic of Tatarstan (Popov 1949) could not be confirmed after many years of personal field prospecting in these regions. There are a few literature data from far Eastern Europe and central Asia on the thermobiology of dice snakes. For example, Bogdanov (1962) reports that in the Murgab Valley, Turkmenia, dice snakes emerge in spring at air temperatures ≥ 15.5 °C and surface temperature ≥ 16.0 °C. Shcherbak (1966) points out, that in the Crimea, Ukraine, dice snakes were observed on 15 April during cloudy weather at an air temperature of 10.0 °C. He measured a minimum cloacal temperature of 12 °C, and a maximum temperature of 31 °C, with the highest frequency of snakes found at air temperatures from 18.0–26.0 °C. For the Ukrainian Carpathians, Shcherbak & Shcherban (1980) observed dice snakes on sunny days on 24 April at an air temperature of 19 °C, and on 1 July at 32 °C with a soil temperature of 36 °C, whereas the cloacal temperatures of the snakes ranged from 29.0–32.3 °C. Chikin (1981) points out that dice snakes from a mountainous part of the Augren flood-plain in Uzbekistan emerged from hibernation on 8 April at an air temperature of 18.5 °C, soil temperature in the sun of 19.5 °C and in the shadow of 15.5 °C, respectively. Emergence in the last ten days of April started when ambient temperature was equal to the temperature inside a hibernation shelter (16.8–17.3 °C). Most dice snakes were visibly active on the surface in late May at 11.30 am at air

temperatures from 25.8–27.2 °C and relative humidity of 55–70%, probably due to mating activities. Beginning in June, these Uzbek dice snakes exhibited two activity peaks daily (morning and afternoon) due to a mid-day decrease in surface presence when air temperature rose above 28.0 °C. Snakes reached cloacal temperature from 13.0–13.5 °C to 26.5–27.4 °C after 20–25 minutes of basking and maintained it on this level by thermotactic behavior. In Western Europe, Luiselli & Zimmermann (1997) studied some aspects of thermal ecology and reproductive cyclicity in two populations of the dice snake, one in central Italy and one in southern Austria. The climate was significant colder at the Austrian site. But snakes of both populations were similar in various traits, including average body temperature, higher body temperature of gravid than non-gravid individuals, significantly higher substratum temperatures selected by gravid than by non-gravid individuals, trends of relationships between body, air and substratum temperatures, average length of reproductive females, and average preparturition mass of reproductive females. However, Austrian snakes were found in water significantly less often than their Italian conspecifics (19.23% and 77.27% of snakes were found in water respectively), and exhibited a lower frequency of reproduction (biannual rather than annual) than Italian ones. Another Italian study by Scali (2011) found similar results in regards to dice snakes, except that body temperatures were lower probably due to a substantial portion of nocturnal captures in cooler water in his data set. Despite all these information from previous studies, the data are mostly snippets and not standardized. No comparative data are available from the northern range limit of the dice snake, where a restraint climate with cool temperatures exerts relevant restrictions on the

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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survival of regional populations. We thus try to provide more detailed information of the thermobiology and microclimatic characteristics of habitats occupied by dice snake from its northern range limit. Material, Methods and Terminology Snakes were sampled at the Samara Bend, National Park “Samarskaya Luka”, Volzhskiy district, Samara province, Russia, from late April to early May in 2001–2008 (see Figs. 1a, b for habitats in this region). For each individual, various temperature data in the field were measured before the snakes were brought into a laboratory to record temperatures in an experimental set up. Additional observations were made in July 2008. The sex of 107 from a total of 123 snakes was determined by examining sexualdimorphic tailroot thickness or in the case of doubt by applying a rectal sonde. A thermistor sensor connected to a digital micromultimeter was used to measure surface air temperature 3–5

Fig. 1. Habitat of N. tessellata near its northern limit along the Volga River: (a) Snake Creek from up on the hill, Samara Bend, National Park “Samarskaya Luka”, Volzhskiy district, Samara province, Russia, (b) shore area inhabited by N. tessellata at Perevoloki, approximately 30 km west of the Snake Creek, Syzranskiy district, Samara province, Russia. Photos: (a) Irinia Gerasimova, (b) Nastja Poklonzewa

cm above the ground and the temperature of the substrate where the snake was collected. The sensor is calibrated using electric thermometer “Checktemp” (“Hanna instruments”, Portugal) with a digital display and a resolution of 0.1 °C. The same sensor was used to record body temperatures (internal and external). External body temperature of dice snakes was measured by holding the temperature-sensitive element of the thermistor on the skin for several seconds. Temperatures were taken at six points: midbody dorsal, midbody ventral, top of the head (parietal), throat, dorsal and ventral side of the tail. In the field we measured the snake’s internal body temperature in the esophagus and in the cloaca, but during laboratory experiments we measured the internal body temperature in the stomach and in the cloaca of the snake. Even though, cloaca temperature does not reflect actual internal body temperature, we measured it to acquire a comparative value to the multitude of studies on snake thermobiology that applied cloaca temperature to approach internal body temperature. Esophagus and stomach temperatures are practically always higher than cloaca temperature. A temperature registrator – iBDL “logger-tablet” (“Dallas Semiconductor”, USA) was introduced into the snake’s stomach to acquire internal body temperatures. Long-term temperature and humidity from the habitat was measured with iBDL-HS data-loggers, and instant relative humidity was taken with a portable device “Hydrocheck” (“Hygrocheck”, USA). Specific capacity of the heat absorption and emission by a substratum was measured by a portable heat-flux density register IPP2 (“Eksis”, Russia). Strength and capacity (watts/m2) of light flux and ultraviolet radiation reaching the spot, where a dice snake was captured, was measured with a combined device “TKA-PKM” (“TKA”, Russia). We estimated the influence of ambient temperature on internal body temperature with the help of the Plokhinskiy method (Lakin 1990). Ambient temperature is a combination of substrate surface temperature where the snake was located and a surface air temperature from the same spot. To investigate a snake’s optimal temperature, the one it deliberately prefers, we exposed individuals experimentally to slowly rising temperatures. We consider individual body temperature at the snake’s desired optimum, when the rising internal body temperature reaches an ambient temperature, above which it begins to actively thermoregulate by seeking a cooler place. This optimal temperature is calculated, not measured, by the two temperature curves (internal body and ambient) on the diagram, representing the experimentally rising temperartures. The intersection of the two curves corresponds to the optimal internal body temperature. Results and Discussion Field Data Dice snakes in the Samara Bend emerge from hibernation between late April and early May and subsequently

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Temperatures and Dice Snake at its Northern Border in Russia

begin with mating. The hibernacula and place of mass maiting are located along sections of southerly exposed rocky banks of the Volga River. All snakes sampled and obeserved in this region were melanistic (Fig. 2). The dynamic of surface air temperatures and relative humidity was recorded in a habitat near the Snake Creek over approximately 36 hours between the evening of 30 April and morning 2 May, 2008 (Fig. 3). On 1 May, the surface air temperature rose from 4.6 °C at 7:20 h up to 25.2 °C at 16:30 h. The relative air humidity varied from 20.5% at 16:50 h on 1 May to 82.5% at 5:30 h on 2 May. All microclimatic results and body temperatures of dice snakes from the Samara Bend are presented in Table 1. Statistically significant differences between males and females and their place of capture (during thermoregulation) were revealed for the following traits: specific capacity for heat emission of substratum (t = 8.14, Р
0.05). In summary, females prefer more illuminated (= open) places that receive intense ultraviolet radiation and light flux, consequently, their thermoregulatory spots yielded a higher heat emission. However, their body temperature is only slightly higher than that of males, which may be due to the mixture of gravid with non-gravid females in our sample. Luiselli & Zimmermann (1997) found that gravid female dice snakes in Italy and Austria exhibited higher body (cloacal) temperatures than non-gravid females due to selecting spots for thermoregulation with higher air and substrate temperatures. We suggest that non-gravid females resemble males in thermoregulatory needs and activities, as both groups would not be urged to achieve higher body temperatures to develop embryos like gravid females do. But the abbreviated sampling period in this study up into early May likely had the larger impact in generating our small sexual difference in body temperatures. Our sampling scheme covered the mating period though, but unlike in Luiselli & Zimmermann (1997), it missed the relevant period of embryogenesis, and hence, the most relevant period of thermoregulatory active gravid females, i.e. when they are expected to seek higher temperatures. Males exhibited a higher temperature on the surface of their tails, ventrally and dorsally. Probably, this sexual difference is related to the smaller sizes of males, producing also a larger surface/volume ratio at the tail, and hence, a more rapidly heatable body segment.

Fig. 3. Spring surface air temperature and humidity in a habitat near Snake Creek in the Samara Bend, Russia (evening 30 April – 2 May 2008).

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Tab. 1. Microclimatic results and various body temperatures in dice snakes from the Samara Bend, Russia: Sexes combi. (= Sexes combined), M = mean, m = standard error. Sexes combi. (n = 123)

Field variable Surface air temperature (°С) Substrate temperature (°С) Specific capacity of incident heat (W/m2) Specific capacity for heat emission of substrate (W/m2) Illumination (intensity of light receiving, in klx) Specific capacity for light flux (W/m2) Specific capacity of ultraviolet radiation (W/m2) Relative humidity (%) Internal body temperature (°С) esophagus Cloacal temperature (°С) Mid-dorsal temperature (°С) Ventral temperature (°С) Parietal temperature (°С) Throat temperature (°С) Tail temperature, dorsal (°С) Tail temperature, ventral (°С)

23.8 ± 0.41 14.0–38.6 25.4 ± 0.56 13.2–40.7 206.6 ± 60.4 188.9–280.0 78.3 ± 22.7 35.0–170.0 82.7 ± 7.66 55.1–122.7 328.2 ± 30.4 218.8–487.2 4.8 ± 0.74 0.6–9.8 51.3 ± 4.91 27.0–68.0 26.4 ± 0.31 14.8–33.2 24.3 ± 0.33 14.6–32.3 23.4 ± 0.28 14.8–33.0 23.4 ± 0.26 15.1–32.2 23.1 ± 0.29 16.0–30.8 23.5 ± 0.28 16.2–31.4 24.0 ± 0.36 19.5–29.6 24.1 ± 0.38 18.2–29.6

The intensity strength index shows the influence of air and substrate surface temperatures on body temperature of dice snakes (Tab. 2). Ambient temperature significantly influences body temperatures of all snakes analysed (P < 0.01), thus corroborating results by Luiselli & Zimmermann (1997) and Scali (2011). When substrate and air temperatures increase, the internal body temperature of a thermoregulating dice snake also increases correspondingly. At our study site, the associ-

Males (n = 60) M ± m / min–max 24.4 ± 0.61 14.0-38.6 25.7 ± 0.71 16.1-40.7 204.6 ± 2.30 191.9–280.0 73.0 ± 20.70 35.0–170.0 78.9 ± 8.30 55.1–102.2 313.4 ± 11.48 218.8–471.4 4.1 ± 0.53 0.6–5.0 47.3 ± 3.91 27.0–68.0 25.9 ± 0.44 14.8–33.2 24.2 ± 0.48 14.6–32.2 22.9 ± 0.44 14.8–33.0 23.1 ± 0.40 15.1–32.2 22.9 ± 0.38 16.0–30.0 23.2 ± 0.37 16.2–30.0 24.5 ± 0.37 21.7–29.6 24.7 ± 0.36 22.0–29.6

Females (n = 47) 23.5 ± 0.66 15.7-38.6 26.4 ± 0.96 15.8-40.7 207.3 ± 2.23 188.9–240.6 82.8 ± 16.80 38.6–165.0 101.0 ± 7.00 94.0–122.7 342.5 ± 13.70 233.9–487.2 5.2 ± 0.63 2.9–9.8 52.7 ± 4.17 36.0–66.0 26.5 ± 0.50 17.9–31.5 24.3 ± 0.56 15.4–32.3 23.8 ± 0.42 18.0–29.8 23.7 ± 0.41 18.5–30.0 23.2 ± 0.42 16.0–30.8 23.6 ± 0.41 16.9–31.4 22.8 ± 0.64 19.5–26.5 22.5 ± 0.76 18.2–26.7

ated basking behavior usually took place in the morning after snakes left their shelter. The internal body temperature was raised up to an optimum level, at which point the snakes switched to other activities, such as mating and foraging (termed r thermoregulation). Alternatively, at reaching a desired temperature level, thermoregulating snakes exhibited a behavior to maintain that temperature to promote relevant physiological processes (e.g. embryogenesis, digestion, ecdysis) and avoid dan-

Tab. 2. Strength index values of ambient temperature impact on body temperature of dice snakes. Ambient temperature Air temperature (%) Substrate temperature (%)

Sexes combined (n = 123) 59.38 65.01

Males (n = 60) 55.68 64.32

Females (n = 47) 59.88 67.03

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Temperatures and Dice Snake at its Northern Border in Russia

gerous overheating, a strategy termed “K thermoregulation” according to Hailey & Davies (1987). We found, that if the ambient temperature continues rising for a only few degrees (< 3 °C) beyond an optimum level, the snake’s body temperature increased with an appreciable backlog slower and remained below the ambient

temperature. If ambient temperatures continued rising, a snake retreated to a shelter with lower temperatures than on the surfcace. Finally, the point, where the curves of internal body temperature and ambient temperature intersect, is viewed as the absolute temperature optimum fot the snake. At this point, the substratum temperature is equal to the preferred ambient temperature. In dice snakes, the point of an absolute temperature optimum was measured and identified for both sexes combined at 28.0 °C (Fig. 4a). This temperature confirms similar results about preferred body temperatures in dice snakes from other areas in Europe, e.g. Luiselli & Zimmermann (1997) and Velenský et al. (2011). There is a sexual difference, as the male’s absolute optimum temperature was determined at 27.0 °C (Fig. 4b), whereas the female’s preferred temperatures two degrees higher at 29.0 °C (Fig. 4c). This result corroborates the 0.6 °C higher body temperatures found in females than in males (t = 2.02; P < 0.05), and reflects the observation by Luiselli & Zimmermann (1997) for dice snakes and by Brown & Weatherhead (2000) for a related North American natricine, as in both species females prefered places with relatively higher temperature. Experimental Data Dice snakes exhibit a natural behavior of fleeing into the water, when a large potential predator such as a human approaches. But unlike in the summer, the water temperature in the spring is relatively cold at around 15 °C. Under such circumstances, the snakes do not stay long in the water and return to the shore after a few minutes to reach temperatures more suitable for their physiological needs. We have performed controlled experiments to elucidate the dynamics of internal body temperature of dice snakes when they are immersed in cold water in natural basins. Prior to the experimental immersion of a large female dice snake (SVL 870 mm, tail length 170 mm), she was confined for half an hour on a sunny warm substrate with a high temperature range between 40.0–54.4 °C. The body temperature of the snake was recorded by the register-tablet iBDL placed in the stom-

Fig. 4. Relationship of substrate temperature / body temperature of Natrix tessellata: a) sexes combined, b) a male, c) a female. X-axis: Classes of substrate temperatures; whereby a class represents a mean of several measurements of substrate temperature. The mean of simultaneously measured body temperatures of snakes is also shown for each class. Classes contain different numbers of temperature measurement. The range of class intervals was defined by using BrooksKarruzers formula. i=

x max − x min , i – range of class intervals; xmax, xmin = max. 5 ⋅ lg n

and min. of substrate temperatures; n = number of substrate temperature measurements

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Fig. 5. Dynamics of internal body (stomach) temperature in a dice snakes immersed into cold water. Arrows indicate moments of imnmersion into and removal from water.

ach. During this heating period the snake’s body temperature reached its maximum at 35.6 °C. The temperature of the cooling bath ranged from 14.8–16.0 °C, Subsequent to the immersion of the snake, its body cooled rapidly. Within nine minutes the body temperature dropped to 19.7 °C by an average of 2.2 deg/min until it stabilized at the level of the water temperature. After removing the snake from the water, its body temperature slowly began to rise at an average of 0.3 deg/min, until it leveled at 27.9 °C. The speed of temperature rise was nearly seven times less than its decrease. An even faster cooling rate of 4.0 deg/min was obtained by immersing a male dice snake (Fig. 5). Presumably its smaller size (SVL 570 mm, tail length 150 mm) was responsible for the rapid cooling In summer, the water temperature at the Samara Bend ranges from 22.5–26.4 °C (mean 23.9 ± 0.57 °C), and the body temperature of dice snakes removed from the water produced similar values from 20.7–28.3 °С (mean 23.6 ± 1.08 °С), i.e. it approximately corresponded to the water temperature, similar to results found for dice snakes in Luiselli & Zimmermann (1997), Scali (2011), and Velenský et al. (2011) Under such temperature conditions, dice snakes can stay for a long period in the water and still maintain a fair amount of relevant physiological processes.

References Bogdanov, O.P. (1962): Reptiles of Turkmenia. – The Turkmen Academy of Science, Ashkhabad, Turkmenistan (in Russian). Brown, G.P. & P.J. Weatherhead (2000). Thermal ecology and sexual size dimorphism in northern water snakes, Nerodia sipedon. – Ecological Monographs 70: 311-330. Chikin, Y.A. (1981): Dice snake activity in a mountainous part of the Augren River. – In: Darevskij, I.S., Ananjeva, N.B., Barkagan, I.S., Borkin, L.Y., Sokolova, T.M. & N.N. Ščerbak (Eds.): Problems of Herpetology, Proceeding of the III Herpetological Conference. – Abstracts, Nauka, Leningrad 5: 151 (in Russian). Hailey, A. & P.M.C. Davies (1987): Activity and thermoregulation of the snake Natrix maura. 1. r and K thermoregulation. – Journal of Zoology of London 213: 71–80. Lakin, G.F. (1990): Biometry. – Visshaya shcola, Moscow (in Russian). Luiselli, L. & P. Zimmermann (1997): Thermal ecology and reproductive cyclicity of the snake Natrix tessellata in southeastern Austria and central Italy: A comparative study – Amphibia-Reptilia 18: 383–396. Olearius, A. (1906): Description of Travel to Moscovia and via Moscovia to Persia and back. –Publ. A.S. Suvorin, Saint-Petersburg, Russia (in Russian). Osipova, V.B. (1993): Amphibians and reptiles. – In: Vertebrates of Ulyanovsk Province. – Simbirskaya Kniga, Ulyanovsk: 50– 63 (in Russian). Popov, V.A. (1949): Reptiles. – In: Fauna of Tataria (Vertebrates). – Kazan: 141–149 (in Russian). Scali, S. (2011): Ecological comparison of the dice snake (Natrix tessellata) and the viperine snake (Natrix maura) in northern Italy. – Mertensiella 18: 131–144. Shcherbak, N.N. (1966): Amphibians and Reptiles of the Crimea. – Naukova dumka, Kiev (in Russian).

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Shcherbak, N.N. & M.I. Shcherban (1980): Amphibians and Reptiles of the Ukrainian Carpathians. – Naukova Dumka, Kiev (in Russian).

Velenský, M., Velenský, P. & K. Mebert (2011): Ecology and ethology of dice snakes, Natrix tessellata, in the city district Troja, Prague. – Mertensiella 18: 157–176.

Authors Nikolay Litvinov, Perm State Pedagogic University, Sibirskaya str. 24, Perm, 614990, Russia, e-mail: [email protected]; Andrey Bakiev, Institute of Ecology of the Volga River Basin of Russian Academy of Sciences, Komzina str. 10, Togliatti, 445003, Russia; Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland, e-mail: [email protected].

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MERTENSIELLA 18

337-342

20 September 2011

ISBN 978-3-9812565-4-3

Fossil Remains of Natrix tessellata from the Late Cenozoic Deposits of the East European Plain Viatcheslav Yu. Ratnikov & Konrad Mebert Abstract. At present, only 10 localities with fossil remains of Natrix tessellata of Pliocene-Holocene age are known from the East European plain. They are exclusively represented by trunk vertebrae. Due the application of a single diagnostic character, the CL/NAW ratio (centrum length/width of interzygapophyseal constriction), the majority of East European Natrix fossils were determined as Natrix cf. natrix, and a smaller number as Natrix cf. tessellata. The oldest fossil records of N. natrix and N. tessellata originate from the Middle Pliocene. The data conclude that N. tessellata inhabited the East European plains continuously since the Late Pliocene until present, but that its range varied due to the frequent climatic and topographic changes. Key words. Natrix tessellata, fossils, stratigraphic distribution, East European Plain, history.

Introduction Fossil finds of the dice snake, Natrix tessellata, or its immediate predecessor are not numerous. Holman (1998) and Szyndlar (1991) identified 14 Pliocene and Pleistocene localities in Central and Western Europe, which are in Hungary (Uppermost Pliocene MN 17: Villány-3, Nagyharsány-hegy, Villány-6; Lower Pleistocene: Beremend-4), Poland (Lower Pleistocene: Żabia Cave), Czech Republic (Lower Pleistocene: Stránzá Skála Hill), Romania (Lower Pleistocene: Betfia; Middle Pleistocene: Braşov), Greece (Middle Pleistocene: Tourkobounia; Upper Pleistocene: Gerani 1), Germany (Upper Pleistocene: Holocene: Euerwanger Bühl, Malerfels, Spitzbubenhöhle), and Croatia (Upper Pleistocene: Šandalja). Older Natrix fossils from the Late Miocene (MN 13) of Polgárdi, Hungary, were allocated to N. tessellata (Szunyoghy 1932). However, Venczel (1994) reinvestigated the same remains and concluded that they represent an intermediate morphology between N. longivertebrata and N. natrix. They are determined now as Natrix cf. N. longivertebrata and the presence of N. tessellata and N. natrix at this locality has been concluded as erroneous. Results and Discussion Natrix Taxa and Diagnosis of Fossils The delicate morphological elements of fossil remains of snakes are frequently destroyed and leave little physical evidence to work with. Since all fossil remains are represented by trunk vertebrae, we have only the presence and shape of the hypapophysis to allocate the bones to the correct subfamily within the Colubridae (see Figs. 1 and  2). Such hypapophyses are widespread within the snake families, and, for example, are also present in the Viperidae and Elapidae. The distinct vertebral structures of these groups and their diagnostic features have been

described elsewhere (Hallock et al. 1990, Holman et al. 1990, Holman 1991, 1998, Szyndlar 1984, 1991, Ivanov 1996). The vertebrae of the subfamily Natricinae differ from those of the Viperidae in having a sigmoid hypapophysis, posteriorly vaulted neural arches, shorter parapophyseal processes and much longer centra. Furthermore, they differ from those of the Elapidae in having lightly built vertebrae, exhibiting much longer centra and strong subcentral ridges. Sensu Szyndlar (1984), trunk vertebrae of Natrix tessellata differ from those of N. natrix by having pointed distal hypapophyses and parapophyseal processes, whereas these structures in the latter species are characterized by obtuse tips (Fig. 3). But Holman (1998) found some variation of these characters in N. natrix. Comparative material investigated by the senior author confirms these variations (see Figs. 1 and 2), and renders these characters less useful. Unfortunately, the fragile elements distinguishing Natrix species are rarely available as fossil remains, requiring an alternative method to diagnose and allocate bony structures to closely related snake taxa. Such a method was introduced by Auffenberg (1963), who applied complementary distinctive features based on measurements and numerical indexes. Especially the ratio CL/NAW (centrum length/width of interzygapophyseal constriction) yielded a valuable tool (Fig. 4). The ratio ranges in N. tessellata between 1.08 and 1.44, but exhibits significant higher values in N. natrix, 1.45–2.07 (Szyndlar 1984, and personal data). The majority of the East European fossil remains, classified as Natrix cf. tessellata, were determined by the CL/ NAW ratio. There are two other Natrix species, with which fossil remains of N. tessellata could be easily confused, N. maura (Holman 1998) and N. megalocephala (Orlov & Tunijev 1987, 1992). However, the current range of the former species lies far to the west from the East European plain. For this reason, we regard N. maura as an unlikely candidate for the fossils studied, though theo-

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Fig. 3. Morphological differences between trunk vertebrae of Natrix natrix (left) and N. tessellata (right) (after Szyndlar 1984). Fig. 1. Trunk vertebra of Natrix natrix: A – dorsal view, B – ventral view, C – lateral view.

Fig. 4. Principal measurements of snake vertebrae applied (after Auffenberg 1963): CL – centrum length, NAW – width of interzygapophyseal constriction.

Fig. 2. Trunk vertebra of Natrix tessellata: A – dorsal view, B – ventral view, C – lateral view.

retically, any vertebrae could belong to N. maura, especially those from older sediments. Fossil remains of the second taxon, N. megalocephala, a species closely related to or being conspecific with N. natrix, were not available for this study. Moreover, this species is not unanimously regarded as valid (e.g. Velenský 1997, Orlov & Tunijev 1999, Guicking et al. 2006). Fossil Remains of Natrix tessellata Within the East European plain, there are currently 10 localities known that revealed fossil remains of Natrix tessellata from the Pliocene through the Holocene (Fig. 5, Ratnikov 2002a, b 2003). Table 1 shows the numbers

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of fossils found at each locality in the East European plain. A prevoius record of N. tessellata from Zmeevka-2 (Ratnikov 1989, 2002a) has subsequently been determined as incorrect. Stratigraphic positions of localities are shown in Table 2. The oldest fossil records of N. tessellata in Eastern Europe are from the Pliocene sediments of Kotlovina (Ukraine). Unfortunately, the fauna sample at this site is mixed from three horizons, consisting of very little Lower Pliocene (MN 15b: approx. 4.0–3.5 million BP), about 70% from the Middle Pliocene (MN16: 3.5–2.6 million BP), and about 30% from the Upper Pliocene (MN17: 2.6–1.8 million BP) (A.S. Tesakov pers. comm.). The most likely age of N. tessellata vertebrae is Middle Pliocene due to the large proportion of this horizon. Thus, if this hypothesis is correct, the oldest fossil of N. tessellata dates back to the Middle Pliocene. Vertebrae of N. natrix are found at the same locality, which roughly coincides with its oldest fossil remains from Central Europe from the Beremend-1 locality in Hungary (Szyndlar 1991).

Fossil Dice Snakes of the East European Plain

Begin of Divison (Mya BP)

Horizons, Su- Localities perhorizons

Level

Division Superdivision Section

Table 2. Stratigraphic distribution of localities of Natrix tessellata fossils. The begin of the period of stratigraphic boundaries is given on the base of Stratigraphic Code (2006).

Drozdy Lopatino Srednyaya Akhtuba

Holocene 0.01 Upper (Late)

Valdai

Fig. 5. Locations of fossil finds of Natrix tessellata. Broken line indicates the northern limits of its current range.

Locality Gradizhsk Drozdy Kotlovina Lopatino Morozovka Morozovka-1 = Cherevichnoye Ozyornoe-2 Srednyaya Akhtuba Chernyi Yar Volnaya Vershina-3

N 1 1 5 1 1 1 2 25 7 1

Middle Lower (Early)

0.8

Lichvinian Oksky Muchkupian Don Iliinsky Pokrovian

Volnaya Vershina-3 Gradizhsk

Morozovka-1 = Cherevichnoye

Lower (Early)

1.8

Ozyornoye - 2

Petropavlovsk

Upper (Late)

Neopleistocene Eopleistocene

Table 1. List of localities and respective number of specimens studied (n).

Morozovka

Srednerussky Chernyi Yar

MN 17 Pliocene

Various hypotheses of the current distribution of Natrix species have been proposed. Recently Guicking et al. (2006) suggested that the three extant species (N. maura, N. natrix and N. tessellata) had already appeared in the Miocene. They concluded that N. maura is basal and diverged from their ancestor first between 18–27 mya, whereas N. natrix and N. tessellata are sister species that evolved million of years later, between 13–22 mya. Their results are based on a molecular clock constructed from two data sets. The first one relates to amino acid distances of diverging snake groups, whereas the second one applied the nucleotide sequences divergence of four protein-coding mitochondrial genes. The molecular clock was then calibrated with two geological events, the Messinian salinity crisis and the first collision of the African and Arabian plates with the Eurasia (Guicking et al. 2006).

Mikulin

MN 16 5.3

Kotlovina

MN 15

However, there are no reliable fossil remains from the Miocene to corroborate this evolutionary scenario. In contrast, the fossil data of recent Natrix taxa are much younger. The earliest N. maura (reported as N. cf. maura) are not older than the lower Pliocene and originate from France (MN 15: Bailon 1991) and Spain (MN

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16: Blain 2005). In this context, it is certainly interesting to notice, that there are up to 14 million years difference between the proposed origin of the N. tessellata lineage approximately 16–17 mya (Guicking et al. 2006, Guicking & Joger 2011) and its oldest fossil data from the Middle Pliocene, approximately 3 mya (see above). Taking into account that intraspecific radiation in N. tessellata was suggested to have begun 5–6 mya at the Miocene-Pliocene boundary (Guicking & Joger 2009, 2011), it would leave that species with approximately 10 million years of stasis, a long period without any additional divergence nor evolutionary change. On the other hand, it reveals the limits of molecular clock applications and N. tessellata might be much younger than suggested by Guicking et al. (2006). The Pleistocene history of fauna is closely connected to large climatic fluctuations (cold glacial and warm interglacial periods) associated with the expansion and retraction of continental ice sheets, which in turn substantially affected the geographic composition of flora and fauna (see refs. in Blondel & Vigne 1993, Mebert 2010). Thus, geographic conditions during the Pleistocene constantly varied, and so did the distribution of species inhabiting temperate zones. However, natural zones and their inhabitants did not simply shift southward following the movements of ice sheets. Findings of so-called mixed faunas in the temperate zones in Pleistocene sites of Eastern Europe and America, including “northern” and “southern” species that are ecologically incompatible today, (e.g. Agadzhanyan 1972, Holman 1976, 1980, 1986, Blondel & Vigne 1993, Markova 1994, Rekovets 1995, Mebert 2010) suggest other, more complex version of events. During continental glaciations there was a displacement of the tundra zone southwards and steppe zone northwards, as forest areas shrank and developed into a mosaic pattern (Baryshnikov & Markova 2002, Markova 2000, 2004a, b, Markova et al. 2002a, b, 2003, 2006, Rekovets & Nadachowski 2007). Large forests became ever less, being gradually reduced to small wooded fragements in river valleys. As a result, an extensive periglacial ‘hyperzone’ was formed, consisting of mixed landscapes with periglacial tundra-steppes, periglacial tundra-forest-steppes, and periglacial forest-steppes. There are no such analog landscapes today. The ranges of many animals moved in concert with the geographic changes of vegetation zones: tundra species penetrated far to the south, cold-resistant steppe species spread to the north, and forest species remained in the residual woodlands. Thus, refugia for forest species existed within the limits of periglacial hyperzone, inhabited mainly by steppe and tundra species. In accordance with the mixed vegetation zones, the on-site composition of mammal fossils from glacial periods shows a mixture of tundra and steppe species, occasionally added with forest forms (e.g. Agadzhanyan 1972, Markova 1994, Rekovets 1995). This is in contrast with East European species of amphibians and reptiles, where no typical tundra forms exist, and no com-

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parable mixed herpetofaunas have been observed. Only the degree of herpetofaunistic diversity distinguishes different climatic periods. The herpetofaunas from glacials usually are depauperate, whereas those from interglacials show an increased diversity including thermophilic southern forms. In the particular case of N. tessellata we suggest that its range extended rather than was reduced during the early phase of glacials, as a consequence of the replacement of wooded areas by steppes (Ratnikov 2009). The associated decrease of shading vegetation during the early glacial promoted the expansion of N. tessellata north into the newly opened aquatic areas, facilitating solar radiation to reach the ground and substanatially warming its preferred microhabitat, rocky shores, a habitat niche with which it is still associated today (Gruschwitz et al. 1999). East-European Plio-Pleistocene findings of N. tessellata are distributed across seven stratigraphic horizons (Tab. 2). They stem from warm interglacials, except the one from Chernyi Yar, which was formed during a glacial period, when the front of glaciers were at distances not less than 700 km (Shik et al. 2006). The general climate during the formation of the Chernyi Yar site was very dry but warm. Its surrounding landscape was an open steppe or semidesert with disjunct meadows, whereas forest existed only in river valleys. The diversity of herpetofauna at this site was with approximately 15 species very high (Ratnikov 2001, 2002a). But the fossil findings of a Lemmus sp., a small mammal, at the same site, representing the most southern site of a lemming on the Russian plain (Kirillova & Svitoch 1994), indicates the contemporaneous existence of tundra elements, and thus, the mixed nature of the Chernyu Yar fauna. Three additional localities were formed during the Holocene. Overall, it appears likely that N. tessellata occupied the East European plain constantly since the Late Pliocene, but its range changed continuously according to environmental fluctuations. Figure 5 shows the sites Kotlovina (Middle Pliocene), Morozovka-1 = Cherevichnoye (Eopleistocene), Ozyornoe-2 (Lichvin horizon of the Middle Neopleistocene) and Chernyi Yar (Middle Russia superhorizon of Middle Neopleistocene) which lie within the limits of the present range of N. tessellata . However, the fossils from the sites Gradizhsk (Iliinka horizon of the Lower Neopleistocene), Volnaya Vershina-3 (Muchkap horizon of the Lower Neopleistocene) and Morozovka (Mikulino horizon of Upper Neopleistocene) show significant deviations from the present range of N. tessellata. Moreover, two of the three Holocene localities of N. tessellata, Lopatino (Pre-Boreal Interstadial approximately 11.6–10.7 thousands BP) and Drozdy (Boreal stage, approx. 10.7–9.3 thousands BP), are located far north of the current range limit of this species. They explicitly confirm that the range of N. tessellata changed significantly in connection with variations of environmental conditions, even during the relatively short interglacial, the Holocene, that we experience today (Markova et

Fossil Dice Snakes of the East European Plain

al. 2003, Monin 1980, Monin & Shishkov 1979, Stuiver et al. 1998). The extralimital fossil records and the existence of several isolated populations of N. tessellata north of its present range between Germany and Russia (e.g. Gruschwitz et al. 1999, Kotenko et al. 2011, Litvinov et al. 2011) are farther facts, that corroborate the existence of a larger range of N. tessellata in earlier periods of the Holocene. This range extension probably coincides with the climatic optimum of the Atlanticum (= HTM, Holocene Thermal Maximum), a period with slightly higher temperatures approximately 5700 to 9300 BP (see Atlantikum, Wikipedia 2011). Acknowledgments The authors thank J.C. Rage, France, and Z. Szyndlar, Poland, for helpful comments and C. Gleed-Owen, UK, for the initial correction of the English version. The study was supported by grant from the Russian Foundation for Basic Research (No. 07-04-00694) References Agadzhanyan, A.K. (1972): Lemming faunas from Middle and Late Pleistocene. – Bull. Komissii po izutcheniyu chetvertichnogo perioda 39: 67–81 (in Russian). Auffenberg, W. (1963): The fossil snakes of Florida. – Tulane studies in zoology 10(3): 131–216. Baryshnikov, G.F. & A.K. Markova (2002): Chapter 7. Fauna (Theriocomplexes of Late Pleistocene). – In: Dynamica landshaftnykh componentov i vnutrennikhl morskikh basseinov Severnoi Eurasii za posledniye 130,000. – Let. GEOS, Moscow, Russia: 123–138. Bailon, S. (1991): Amphibiens et Reptiles du Pliocène et du Quaternaire de France et d’Espagne: mise en place et évolution des faunes. – M.S. thèse, Université Paris 7, France. Blain, H.A. (2005): Contribution de la paléoherpétofaune (Amphibia & Squamata) à la connaissance de l’évolution du climat et du paysage du Pliocène supérieur au Pleistocène moyen d’Espagne. – M.S. thèse, Mus. Hist. Nat. Paris, Inst. Paléont. Humaine, France. Blondel, J. & J-D. Vigne (1993): Space, time, and man as determinants of diversity of birds and mammals in the Mediterranean region. – In: Ricklefs, R.E. & D. Schluter (Eds.): Species Diversity in Ecological Communities: Historical and Geographical Perspectives. – University of Chicago Press, USA: 135–146. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Guicking, D. & U. Joger (2009): Cryptic diversity in a Eurasian water snake (Natrix tessellata, Serpentes: Colubridae): Evidence from mitochondrial sequence data and nuclear ISSR-PCR fingerprinting. – Organisms, Diversity & Evolution 9: 201–214. Guicking, D. & U. Joger (2011): A range-wide molecular phylogeography of Natrix tessellata. – Mertensiella 18: 1–10.

Guicking, D., Lawson, R., Joger, U. & M. Wink (2006): Evolution and phylogeny of the genus Natrix (Serpentes: Colubridae). – Biological Journal of the Linnean Society 87(1): 127– 143. Hallock, L.A., Holman, J.A. & M.R. Warren (1990): Herpetofauna of the Ipswichian Interglacial Bed (Late Pleistocene) of the Itteringham Gravel Pit, Norfolk, England. – Journal of Herpetology 24(1): 33–39. Holman, J.A. (1976): Paleoclimatic implications of “ecologically incompatible” herpetological species (late Pleistocene: southeastern United States). – Herpetologica 32: 290–295. Holman, J.A. (1980): Paleoclimatic implications of Pleistocene herpetofaunas of eastern and central North America. – Transactions of the Nebraska Academy of Sciences 8: 131–140. Holman, J.A. (1986): The known herpetofauna of the late Quaternary of Virginia poses a dilemma. – In: McDonald, J.N. & S.O. Byrd (Eds.): The Quaternary of Virginia: A Symposium Volume. – Publication of the Virginia Division of Mineral Resources 75: 36–42. Holman, J.A. (1991): Fossil history of the grass snake (Natrix natrix) with emphasis on the British fossil record. – British Herpetological Society Bulletin 36: 8–13. Holman, J.A. (1998): Pleistocene Amphibians and Reptiles in Britain and Europe. – Oxford University Press, New York. Holman, J.A., Stuart, A.J. & J.D. Clayden (1990): A middle pleistocene herpetofauna from Cudmore Grove, Essex, England, and its paleogeographic and paleoclimatic implications. – Journal of Vertebrate Paleontology 10(1): 86–94. Ivanov, M. (1996): Old biharian reptiles from the Mala Dohoda Quarry (Moravian karst). – Scripta Fac. Nat. Univ. Masaryk. Brun. 24 (1994), (Geology.): 9–26. Kirillova, I.V. & A.A. Svitoch (1994): New findings of Middle Pleistocene small mammals in the Chernyi Yar section (Lower Povolzhye) and there stratigraphic value. – Doklady akademii nauk 334(6): 731–734 (in Russian). Kotenko, T. I., Shaitan, S.V., Starkov, V.G. & O.I. Zinenko (2011): The northern range limit of the dice snake (Natrix tessellata) in Ukraine and the Don River basin in Russia. – Mertensiella 18: xxx–yyy. Litvinov, N., Bakiev, A. & K. Mebert (2011): Microclimatic conditions of habitats and thermobiology of the dice snake along the northern limit in Russia. – Mertensiella 18: 330–336. Markova, A.K. (1994): Pleistocene landscapes of the Russian Plain by fauna of small mammals. – Bull. Moskovskogo obshestva ispytatelei prirody, Otdel Geol. 69(1): 64–68. Markova, A.K. (2000): The Mikulino (= Eemian) mammal faunas of the Russian Plain and Crimea. – Geologie en Mijnbouw/Netherlands Journal of Geosciences 79(2/3): 293–301. Markova, A.K. (2004a): 3.7. Pleistocene faunas of mammal of East Europe. – In: Structura, Dinamica i Evolutsia Prirodnykh Geosistem, Vol. 1. – Publishing House of the Moscow State University, Moscow: 583–598 (in Russian). Markova, A.K. (2004b): Reconstruction of paleolandscapes of Lichvin interglacial on materials of fauna of fine mammal of East Europe. – Izvestiya AS (Geographical Series) 2: 39–51 (in Russian). Markova, A.K., van Kolfschoten, T., Simakova, A.N., Puzachenko, A.Yu. & E.A.Belonovskaya (2006): European ecosystems during the period of the late glacial Bölling-Allerod Warming (10.9–12.4 ka) indicated by palynological and theriological data. – Izvestiya AS (Geographical Series) 1: 15– 25 (in Russian).

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Viatcheslav Yu. Ratnikov & Konrad Mebert Markova, A.K., Simakova, A.N., Puzachenko, A.Yu. & L.M. Kitaev (2002a): Environments of the Russian plain during the Middle Valdai Briansk Interstade (33,000–24,000 yr BP) indicated by fossil mammals and plants. – Quaternary Research 57: 391–400. Markova, A.K., Simakova, A.N. & A.Yu. Puzachenko (2002b): Ecosystems of Eastern Europe in the late glacial maximum of the Valdai Glaciation (24–18 ka B.P.) based on floristic and theriological data. – Doklady Earth Sciences 387(8): 925–928. Markova, A.K., Simakova, A.N. & A.Yu. Puzachenko (2003): Ecosystems of Eastern Europe in the Holocene Atlantic Optimum based on floristic and theriologic data. – Doklady Earth Sciences 391(4): 545–549. Mebert, K. (2010): Massive Hybridization and Species Concepts, Insights from Watersnakes. – VDM Verlag, Saarbrücken, Germany. Monin, A.S. (1980): Popular History of the Earth. – Nauka, Moscow (in Russian). Monin, A.S. & Yu.A. Shishkov (1979): History of a Climate. – Hydrometeoizdat, Leningrad, Russia (in Russian). Orlov, N.L. & B.S. Tunijev (1987): Nowyj wid uza Natrix megalocephala sp. nov. s Kawkaza (Ophidia: Colubridae). – Tr. Zool. Inst. AN USSR 158: 116–130 Orlov, N.L. & B.S. Tunijev (1992): A new species of grass snake, Natrix megalocephala, from the Caucasus (Ophidia: Colubridae). – Asiatic Herpetol. Res. 4: 42–54. Orlov, N.L. & B.S. Tunijev (1999): Natrix megalocephala (Laurenti, 1786) – Grosskopf-Ringelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 505–512. Ratnikov, V.Yu. (1989): The Upper Quaternary herpetofaunas of the Belgorod region. – Paleontol. Zhurn. 22(3): 124–127. Ratnikov V. Yu. (2001): Herpetofauna from Cherny Yar Sands of the Cherny Yar-Nizhnee Zaimishche Section, Lower Povolzhye (Volga Region). – Paleontological Journal 35(6): 72–77. Ratnikov, V.Yu. (2002a): Late Cenozoic amphibians and reptiles of the East-European plain. – Trudy Nauchno-Issledovatelskogo Instituta Geologii Voronezhskogo Universiteta, Voronezh, 10 (in Russian). Ratnikov, V.Yu. (2002b): New findings of amphibians and reptiles in the base muchkapian localities of Upper Don Basin. – Vestnik Voronezhscogo Universiteta. Geologia 1: 73–79 (in Russian).

Ratnikov, V.Yu. (2003): Eopleistocene herpetofauna of Morozovka-1 locality. – Vestnik Voronezhscogo universiteta, Geologia 2: 78–82 (in Russian). Ratnikov, V.Yu. (2009): Fossil remains of modern amphibian and reptile species as the material for studing the history of their distribution. – Trudy Nauchno-Issledovatelskogo Instituta Geologii Voronezhskogo Universiteta, Voronezh, 59 (in Russian) Rekovets, L.I. (1995): Periglacial micromammal faunas from the Late Pleistocene of Ukraine. – Acta zool. cracov. 38(1):129–138. Rekovets, L.I. & A. Nadachowski (2007): The evolution of Biocoenoses of the Periglacial Zone in Late Pleistocene Eastern Europe. – Vestnik zoologii 41(3): 197–206. Shik, S.M., Zarrina, E.P., & V.V. Pisareva (2006): Neopleistocene stratigraphy and paleogeography of the Center and Southern European Russia. – In: Palinologicheskiye, Klimatostratigraphicheskiye i Geoecologicheskiye Rekonstruktsii [Reconstruction from Palinology, Climatostratigraphy and Geoecology]. – Nauka, Sankt-Peterburg: 85–121 (in Russian). Stratigraphic Code of Russia (2006): Third Edition. – Zhamoida, A.I. (Ed.). – Spb.: VSEGEI Press (in Russian). Stuiver, M., Reimer, P.J., Bard, E., Beck, J.W., Burr, G.S., Hughen, K.A., Kromer, B., McCormac, G., van der Plicht, J. & M. Spurk (1998): INTCAL98 radiocarbon age calibration, 24,000-0 cal D.P. – Radiocarbon: 1041–1084. Szunyoghy, J. von (1932): Beiträge zur vergleichenden Formenlehre des Colubridenschädels, nebst einer kraniologischen Synopsis der fossilen Schlangen ungarns mit nomenklatorischen, systematischen und phyletischen Bemerkungen. – Acta Zool. 13: 1–56. Szyndlar, Z. (1984): Fossil snakes from Poland. – Acta zool. cracov. 28(1): 1–156. Szyndlar, Z. (1991): A review of Neogene and Quaternary snakes of Central and Eastern Europe. Part II: Natricinae, Elapidae, Viperidae. – Estudios geol. 47: 237–266. Venczel, M. (1994): Late Miocene snakes from Polgárdi (Hungary). – Acta zool. cracov. 37(1): 1–29. Velenský, P. (1997): Natrix megalocephala Orlov et Tunijev, 1987: A new species of the European reptiles fauna? – Gazella 24: 177– 186. Wikipedia (2011): Atlantikum. – Available at: http://de.wikipedia. org/wiki/Atlantikium

Authors Viatscheslav Yu. Ratnikov, Voronezh State University, University sq. 1, Voronezh, 394006, Russia, e-mail: vratnik@yandex. ru; Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland.

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20 September 2011

ISBN 978-3-9812565-4-3

Notes on the Dice Snake (Natrix tessellata) from the Caucasian Isthmus Boris Tuniyev, Sako Tuniyev, Tom Kirschey & Konrad Mebert Abstract. A summary of general aspects of dice snakes from the Caucasian Isthmus, including areas west to the Sea of Azov and east to the Caspian Sea, is presented. The aspects include notes on color pattern, distribution, habitat and sympatric herpetofauna. We conclude this report with relevant accounts on the daily activity and conservation of dices snakes in the Caucasus biogeographic region. Key words. Natrix tessellata, distribution, morphology, biology, nocturnal activity, conservation, habitat, Caucasus, Caspian Sea

Introduction The Caucasian biogeographic region includes the mountain ranges of the Greater Caucasus, Lesser Caucasus and Talysh (as the northern part of Alborz [or Elburs] mountain range), as well as the Colchic and Caspian lowlands between these mountain ranges. The Greater Caucasus is an 1100 km long mountain range spanning from the northeastern coast of the Black Sea eastward to the Caspian Sea with an average altitude of 601 m a.s.l. and with the top of Mt. Elbrus, Russia, at 5642 m a.s.l., the highest peak in Europe (Fig. 1). Traditionally, herpetologists studying the reptilian fauna of the Caucasus focused mainly on rock lizards and vipers (e.g. Lantz & Cyren 1947, Lukina 1963, Darevsky 1967, Bischoff 1988, Orlov & Tuniyev 1990, Nilson et al. 1995, Ryabinin et al. 1996, MacCulloch et al. 2000, Tuniyev

Fig. 1. The Greater and Lesser Caucasus. Copyright and map adapted from WWF Caucaus PO.

& Ostrovskikh 2001, Tuniyev & Tuniyev 2008, Tuniyev et al. 2009). The dice snake, Natrix tessellata, even though one of the most widespread snake species along the Caucasian Isthmus, has received little attention and most published information about this species relates to distribution and general aspects of its biology (e.g. Chernov 1939, Muskhelishvili 1970, Bannikov et al. 1977, Alekperov 1978, Ananjeva et al. 2004). In this report, we present our personal observations and previously unpublished accounts of N. tessellata from the Caucasus. We briefly review relevant references, but are not trying to provide all available information from the literature. A more detailed account concerning N. tessellata in Georgia is found in Frotzler et al. (2011). Morphological Variation Color pattern of dice snakes and its polymorphism in general is described exhaustively in Bannikov et al. (1977) and Gruschwitz et al. (1999). As all over its vast range, the most frequent dorsal color pattern of dice snakes from the Caucasus is characterized by black blotches on a lighter ground, varying from brown, olive to grey (Figs. 2–4). Numerous synonyms demonstrating the morphological variation of dice snakes refer to specimens from the Caucasus and Transcaspian region. The early description of Enhydris caspia by Oken (1816) with olive-green dorsal and yellow ventral coloration is geographically close, but may be just outside the Caucasus, as its origin was described as “from the river Rhymnus into the Caspian Sea”. Rhymnus fluvius was labeled by Philippus Ferrarius (1738) in his Novum Lexicon Geographicum to denote the Ural River just north of the Caucasus. But at least eight synonyms describing Caucasian and West-Caspian representatives of Natrix tessellata were published in the 19th century: Coluber reticulatus Ménétriès 1832, Coluber muravievii, Coluber griseus Dwigubsky 1832, Coluber elaphoides Brandt 1838, Tropidonotus tessellatus var. sparsus Dürigen 1897

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Fig. 2. Light brown Natrix tessellata with round blotches, Absheron National Park, Azerbaijan. Photo: T. Kirschey

Fig. 3. A grey juvenile Natrix tessellata from Mzymta River, Sochi, Russia. Photo: B. & S. Tuniyev

and Tropidonotus tessellatus var. hagenbecki, lineaticollis, nigerrima Werner 1897. Coluber elaphoides was described by Brandt (1838) as a large unicolored species from the western coast of the Caspian Sea to northern Persia. According to our (TK) observations, the “elaphoides” (or unicolored)-morphs are rather common, especially along the Caspian Sea coast (up to 19 %, n = 143) They show the same dorsal color range as the blochted N. tessellata (Fig. 5). However, the supralabials and sublabials of these morphs are often lighter. Unicolored N. tessellata are known over most of its range, for example from northern Italy (Mebert 1993), Czech Republic (Mebert 2011), to southern Macedonia (Kwet & Mebert 2010), the western Black Sea Coast (http://en.balcanica.info), western Turkey (Dincaslan et al. 2011) and east to the Caspian Sea (Gruschwitz et al. 1999), but their occurrence is local with a variable frequency. In his comprehensive work about the herpetofauna of Germany, Dürigen (1897) described another variety from the Caucasus by comparing preserved specimens from the Zoological Museum Berlin. This “brown-speckled” variety (termed sparus) is characterized by five dorsal rows of blotches with distinct brownish keels on each scale, and similar brownish pattern on supralabials and temporal scales. Dürigen mentioned, that only a few Caucasian representatives belong to this variety. But our (TK) observations from the Absheron Peninsula and some Caspian Sea islands in Azerbaijan show that locally up to 10% of dice snakes exhibit these characters (n = 143). Similar brown to even reddish keeled specimens are known from throughout its wide range (Gruschwitz et al. 1999). Another synonym, Tropidonotus tessellatus var. nigerrima Werner 1897, links to the high incidence of melanism in Transcaspian dice snakes. Concordantly, we observed quite often melanistic individuals within the Caucasus region, especially along the coast of the Sea of Azov (approximately 10%) and at higher elevation in Armenia, e.g. at Lake Sevan, where about 50% of the population is mela-

Fig. 4. Blotch size variation in Natrix tessellata: (above) large blotched dice snake; (below) small blotched specimen, both Absheron National Park, Azerbaijan. Photo: T. Kirschey Fig. 5. The „elaphoides“ (= unicolored) morph of Natrix tessellata, Absheron National Park, Azerbaijan. Photo: T. Kirschey

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Fig. 6. Melanistic Natrix tessellata with fully black eyes caught after landing on a shell and sand beach, Absheron National Park, Azerbaijan. Photo: T. Kirschey

nistic and sites above 2500 m a.s.l. On Absheron Peninsula and in Lenkoran lowland at the Caspian Sea coast approximately 15% of specimens were melanistic (Fig. 6). Similar to other color morphs, such melanism in N. tessellata is known from many regions (see summaries in Mertens 1957, Muggiasca & Gandolla 1976, Gruschwitz et al. 1999). It occurs in low frequencies in some areas, where a single melanistic specimen was occasionally found (e.g. Cafuta 2011) or as a significant proportion in separate populations, such as at 10–17% in Lake Lugano, Switzerland (Schweizer 1962, Kramer & Stemmler 1986, Mebert 2007, Lenz et al. 2008) or 20% on the Mediterranean island Korfu (Wütschert 1984). Overall, the color pattern of N. tessellata from the Caucasus includes the known variations for this species (Gruschwitz el al. 1999), but a particular high diversity can be locally concentrated and include many morphs instead of just 2–3 as in many other areas (Mertens 1969, this study). However, newly hatched and juvenile N. tessellata from the Black Sea coast along the Caucasus often display well expressed light cervical patches, resembling the lunar spot of the closely related N. natrix. This patch is framed above by a black angle that extends caudad over a few scales, which is unlike the vertical (ventrad) orientation of the black angle in N. natrix ssp. (but see for an exception in Baha el Din 2011). A strong contrasting black angle is known from many juveniles throughout the range of N. tessellata (see refs. in Gruschwitz et al. 1999, Mebert 2007, Lenz et al. 2008). But such a light cervical patch occurs as a significant proportion (> 5%) only locally, as for example in parts of Israel (Grillitsch & Werner 2009). A rare morph (Mertens 1969, Mebert 2011), in which the blotches are partially striped or at least appear to be stretched longitudinally, also occurs along the Caspian Sea (Fig. 7). A case of dicephalism in a dice snake is reported from Azerbaijan by a single picture within a coffee table book from the Soviet Union period (Budagov 1980). The pic-

Fig. 7. Natrix tessellata with a tendency to striped blotches, Babur North Island, Azerbaijan. Photo: T. Kirschey

Fig. 8. Two-headed Natrix tessellata, Azerbaijan. Photo: Yu. Shamilov

ture shows a proarchodichotomous specimen with two heads and long necks, and a single body and tail (Fig. 8). It was photographed by Yu. Shamilov but no information about date and locality of the picture are given. The specimen also never entered the scientific collection of the Zoological Institute of the National Academy of Sciences in Baku. Distribution in the Caucasus Natrix tessellata ranges across all of the Caucasian Isthmus, except for higher elevations in the vast mountains. The Caucasus Isthmus is divided into a Greater Caucasus (including a western, central, and eastern part) in the north and a Lesser Caucasus in the south (Fig. 1). Within the Greater Caucasus the dice snake is missing in the middle-mountain belt (600–1800 m) and in the highmountain landscapes (>1800 m) of Western and Central Caucasus. For example, it reaches elevations up to 600 m a.s.l. on the Western Caucasus, near the Russian settlements of Krasnaya Polyana and Kalinovoe Ozero (Fig. 9). Only in the Eastern Caucasus does N. tessel-

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Fig. 9. Localities mentioned in the text and/or where Natrix tessellata has been observed by the authors: (1) Gulf of Azov Sea (Krasnodar Territory, Russian Federation); (2) Taman Peninsula (Krasnodar Territory, Russian Federation); (3) Bugasskaya Spit (Krasnodar Territory, Russian Federation); (4) Lake Abrau (Krasnodar Territory, Russian Federation); (5) River Pshenakha (Krasnodar Territory, Russian Federation); (6) River Shakhe (Krasnodar Territory, Russian Federation); (7) Sochi (Krasnodar Territory, Russian Federation); (8) Gorge Akhzu (River Mzymta) (Krasnodar Territory, Russian Federation), and Krasnaya Polyana and Kalinovoe Ozero just west and north of the indicated dot; (9) River Laba (Krasnodar Territory, Russian Federation); (10) Pitsunda-Myusserskiy Reserve (Abkhazia Republic); (11) Kolkhidsky Reserve (Georgia); (12) River Charnali (Georgia); (13) Itum-Kale Hollow (Chechen Republic, Russian Federation); (14) Botlikh Hollow (Daghestan Republic, Russian Federation); (15) Daghestan Reserve (Daghestan Republic, Russian Federation); (16) Tabasaran District of Daghestan (Daghestan Republic, Russian Federation); (17) River Rubas (Dagestan Republic, Russian Federation); (18) River Samur (Daghestan Republic, Russian Federation); (19) Gobustan Reserve (Azerbaijan); (20) Kyzyl-Agach Reserve (Azerbaijan); (21) Lake Sevan (Armenia); (22) River Vedi (Gorovan Sands of Khosrov Reserve, Armenia); (23) Ekhegnadzor gorge of Arpa river (Armenia); (24) Zangezur ridge (Armenia); (25) River Akera (Azerbaijan); (26) River Arax (Armenia); (27) Altiagač (Altyaghach) National Park (Azerbaijan); (28) Absheron National Park (Azerbaijan); (29) Jinikh (= Dzhinikh) Daghestan Republic, Russian Federation; (30) Kurush (= Qurush) Daghestan Republic, Russian Federation; (31) Daevaechi Liman (Azerbaijan); (32) Rivers Mazymchay and Katekhchay in Zaqatala Reserve (Azerbaijan); (33) River Türyanchay and upper Yukhan-Shirvan-Channel in Agdash Region (Azerbaijan); (34) Elat [Aelaet] coastline and offshore islands (Azerbaijan); (35) Shirvan National Park (Azerbaijan); (36) Lake Ag-Göl in Ag-Göl National Park and Bash Mil-Qarabagh Collector Channell (Azerbaijan); (37) Shahagach-Qamishovka coastline in Astara Region (Azerbaijan); (38) Züngülash in Hirkan National Park at the border with Iran (Azerbaijan); (39) Armash fish hatchery, (Armenia) by R. Nessing (in litt.).

lata range into the middle-mountain belts, for example in the Itum-Kale valley along the Chanty-Argun River, Chechnya, and in neighboring Daghestan near the village Botlikh along the Andiyskoye Koysu River and in the valley of the Samur River at the border to Azerbaijan (Fig. 9). According (Khonjakina 1969) N. tessellata reaches in southern Daghestan also the high-mountain landscape near the villages Jinikh (= Dzhinikh up to 1906 m) and Kurush (= Qurush up to 2243 m) and even surpasses 2500 m in some areas. In the lowland of Daghestan and some islands of Caspian Sea, it occurs down to –25 m below sea level. In the Lesser Caucasus, N. tessellata is known up to 2000 m a.s.l. at Lake Sevan in Armenia (Fig. 10). The distribution of N. tessellata in the mountains of the Western Caucasus correlates with Neogobius rhodi346

oni – its basic fish prey in the Caucasus. Such a preference of Neogobius sp. by this snake was previously noted by Krasawtzev (1934). In the Yew-box tree grove of the Caucasian Reserve, we watched a young dice snake (total length = 240 mm), feeding on a Neogobius rhodioni with a total length of 68 mm (Fig. 11). A dice snake (total length = 746 mm) caught in the Apsta River (Abkhazia) vomited a trout (Salmo fario, total length = 270 mm). On Mount Maliy Akhun near Sochi, we observed a juvenile N. tessellata hunting for larvae of Rana macrocnemis. N. tessellata occurs also on the shores of the Sea of Azov, Black Sea and Caspian Sea (Fig. 12). Due to its ability to inhabit brackish to strongly salty water (Gru­ schwitz et al. 1999, Ahmadzadeh et al. 2011), it occupies areas inaccessible for other Caucasian represen-

Natrix tessellata in the Caucasus

Fig. 10. Lake Sevan at 1.900 m a.s.l., Armenia. Photo: B. & S. Tuniyev

Fig. 13. Taman Peninsula, Russia. Photo: B. & S. Tuniyev

Fig. 11. Gobiid fish are the principal prey of N. tessellata along the Caucasus isthmus: (A) A juvenile dice snake swallowing a Neogobius rhodioni at the Black Sea coast, Photo: B. & S. Tuniyev; (B) a dice snake vomited three adult monkey gobies N. fluviatilis and (C) a single specimen is swallowing one at Absheron National Park, Azerbaijan. Photos: T. Kirschey

Fig. 14. Oil drilling platform inhabited by Natrix tessellata. Photo: T. Kirschey

Fig. 12. Sandy shore habitat of Natrix tessellata at the Sea of Azov, Russia. Photo B. & S. Tuniyev

tatives of the genus Natrix. The coastal habitats apparently provide ideal conditions for N. tessellata, as for decades, we have observed high densities of this species along the coast of the Caspian Sea of Daghestan to Azerbaijan, and also in the surroundings of the Taman Peninsula at the Black Sea (Figs. 9, 13) and the Sea of Azov. The density of the coastal populations were 20– 30 specimens per 100 m at the Caspian Sea, up to 10 specimens per 100 m at the Sea of Azov and the Taman coast, but only single specimens were observed along the Black Sea coast of the Caucasus. The dice snake is able to swim considerable distances off shore to forage for fish in the sea. Near Sochi it was caught in the Black Sea at distance 200 m from the shore and vomited a stargazer (Uranoscopus scaber), a bottom-dwelling fish. Laňka (1978) observed an adult dice snake approximately 3 km distant from the Bulgarian coast in the Black Sea. In Azerbaijan, dice snakes were found sitting on historical oil drilling platforms in the Caspian Sea up to a maximum of 4 km distance to the next platform or island, and up to 8–9 km away from the mainland coast (Fig. 14). Khonjakina (1969) lists additional saltwater

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fish species consumed by the dice snake from the Caspian Sea in Daghestan (Scardinius erythrophthalmus, Tinca tinca, Blicca bjoerkna, Barbus sp., Gambusia holbrooki, Perca fluviatilis, Neogobius sp., Gasterosteus aculeatus, Clupeonella sp., Rutilus caspicus, Rutilus rutilus), whereas Gruschwitz et al. (1999) briefly review the fish prey and corresponding references from the Black Sea. Our observations from the Sea of Azov, Russia, to the Absheron National Park in Azerbaijan show the preference of gobiid fishes during their spawning season from April to June, including Neogobius syrman, N. fluviatilis (Fig. 11), N. bathybius, N. kessleri, Chasar bathybius, Mesogobius nonultimus. One of the authors (TK) has used regurgitating dice snakes, sampled along the coast, to detect some of the gobiid fishes listed in the IUCN Red List during their spawning period. Habitat and Sympatric Herpetofauna in the Caucasus Natrix tessellata inhabits river valleys and canyons covered by forest vegetation (Figs. 15, 16), including subtropical polydominant colchic forest with dense undergrowth (Fig. 17), as well as the slow-moving lowland rivers of alluvial plains (Fig. 18) and any open stretches of river banks, seas and alpine lakes with some microstructure along their banks and shores (e.g. Lake Sevan, Armenia, Fig. 10) deprived of arboreal and shrub vegetation (Fig. 19). The habitat of N. tessellata is closely related to water, because it principally feeds on fish. But activities of daily shelter, mating, gestation, oviposition, and hibernation are normally also accomplished in close proximity to water bodies (Gruschwitz et al. 1999, Conelli & Nembrini 2007, Conelli et al. 2011, Neumann & Mebert 2011, Velenský et al. 2011). However in Transcaucasia (the geographical region south of the Greater Caucasus mountains, primarily encompassing Armenia, Azerbaijan, and Georgia, but reaching as far west as Sochi, Russia, the hibernation sites are frequently located at distances of more than 2 km from their

Fig. 16. Gorge Akhzu, River Mzymta, Russia. Photo: B. & S. Tuniyev

Fig. 17. Box forest at Mzymta River, Sochi, Russia. Photo: B. & S. Tuniyev

Fig. 15. River Shakhe, Russia. Photo: B. & S. Tuniyev

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summer habitat along the water courses. Thus, hibernation areas such as along the Zangezur ridge in the Megrinskiy district, Armenia, are selected on steep rocky slopes and usually are exposed toward the east or south (Figs. 9, 20). In the Tabasaran district of Daghestan, we observed N. tessellata along the Rubas River at the foothills of the

Natrix tessellata in the Caucasus

Fig. 18. Delta of Kuban River, Russia. Photo: B. & S. Tuniyev

northern slopes of the principal Caucasian Chain (Figs. 9, 21). There they inhabit elevations between 100 to 250 m a.s.l. in the poplar (Populus alba) riparian forest, in wetland vegetation along Rubas River with Phragmites australior and Typha angustifolia as the dominant grass species and Bolboschoenus maritimus as the subdominant species. Here, N. tessellata is sympatric with its close relative N. natrix, as well as with other herpetofaunistic elements such as Emys orbicularis, Mauremys caspica, and Pelophylax ridibundus. In the semiarid Itum-Kale valley, Chechnya (Fig. 9), N. tessellata is common in the riparian Hippophae

Fig. 20. Hibernation site on the rocky slope of the Zangezur Ridge, Armenia. Photo: B. & S. Tuniyev

Fig. 19. River Vedi, Gorovan Sands, Armenia. Photo: B. & S. Tuniyev

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Fig. 21. Low flowing River Rubas near Syrtych settlement, Daghestan, Russia. Photo: B. & S. Tuniyev

rhamnoides forest along the Chanty-Argun River. Undergrowth bushes consist of Berberis vulgaris and Rosa canina. Here, N. tessellata occurs together with Hyla arborea, Bufo viridis and Pelophylax ridibundus. At the Caspian Sea shore the dice snake is one of the most common reptile species. It inhabits numerous very small islands in high densities (Kirschey et al. 2009, Schmidt & Uppenbrink 2009), e.g. Cape Absheron

Fig. 23. Habitat of Natrix tessellata along the Caspian Sea, a flooded field of a former watermelon culture in the northern part of Absheron National Park, Azerbaijan. Habitat features include reeds, salt lagoons, beaches and the sea. Photo: T. Kirschey

(= Suiti Island, see Langhammer 2009) in Absheron National Park or Bula (= Khaerae Zirae) belonging to the Elat Archipelago. Some of them are remarkable far from the shore, like Gil (2.5 km), Boyuk Tava (6.0 km), Chigill (9.0 km) and Kichik Tava (10.5 km). These islands consist mainly of shell limestone and are covered

Fig. 22. Gil Island (N 39°56’56, E 49°29’00): Habitat of Natrix tessellata with large mud volcanoes (see insert), Azerbaijan. Historic offshore platforms for the oil industry are visible in the background. Photo: T. Kirschey

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Fig. 24. Island Boyuk Tava (N 40°24’05, E 50°24’16), approximately 6 km offshore the cape of Absheron Peninsula, Azerbaijan, inhabited by Natrix tessellata. Photo: T. Kirschey

Fig. 25. Island Babur North (N 39°59’52, E 49°25’54), approximately 2.2 km offshore the coastline close to the town of Elat (Alat), Azerbaijan, is inhabited by high numbers of N. tessellata and a breeding colony of the yellow-legged gull (Larus cachinnans). Photo: T. Kirschey

by shell sand with a sparse vegetation of Sysimbrium irio, Spergularia salina, Malva parviflora and Phragmites australis (see Fig. 22, and for a detailed vegetation cross sections and a list of islands inhabited by N. tessellata in Schmidt & Uppenbrink 2009). Remarkably rocky structures are lacking on most of these islands, but a few have mud volcanoes (insert in Fig. 22) and little-covered ridges of sands and pebbles with crevices which provide potential shelter. The dice snake is the only reptile species on the smaller islands, whereas some of the larger islands are inhabited by sympatric reptiles, such as Eremias velox, Cyrtopodion caspius and Ablepharus pannonicus. A detailed description of the habitats in the Absheron National Park is given by Langhammer (2009). Figures 23–25 depict coastal areas associated with N. tessellata along the Caspian Sea of Azerbaijan, mainland and islands.

Fig. 26. Semi-arid habitat of Natrix tessellata in the Gobustan Reserve, Azerbaijan. At least when filled with water, dice snakes can be found in the ravines and wadis in a rocky area surrounded by gengiz steppe with wormwood Artemisia fragrans. Photo: Mehdi Aliev, Institute of Zoology, Azerbaijan National Academy of Sciences.

Fig. 27. Karst lakes at 400 m a.s.l. south of the Altiagač National Park (Altyaghach NP), Azerbaijan, where Natrix tessellata and N. natrix occur syntopic. Photo: T. Kirschey

In the Gobustan (= Qobustan) State Reserve of Azerbaijan, N. tessellata was found on the Chaynizya Mountain (= Kagniza-Dag) by one of the authors (BT) where it inhabits a vast marine terrace with steep hills and a dense network of ravines (Figs. 9, 26). The habitat is a gengiz desert with the thistle Salsola gemmascens nodulosa and wormwood Artemisia fragrans prevailing. Dice snakes have been observed in the temporarily filled water courses up to mid-May, depending on the rainfall. It is not clear, however, whether they aestivate through the dry summer and wait for the autumn rainfall, or retreat to the Caspian Sea nearby. The sympatric reptilian species are Eremias velox, Ophisops elegans, Testudo graeca, Telescopus fallax, Typhlops vermicularis, Eirenis collaris, Platyceps najadum, Hierophis schmidti, Hemorrhois ravergieri, and Macrovipera lebetina. In the same

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Fig. 28. This Wadi in the Altiagač-Khizi foothills, Azerbaijan, is inhabited by Natrix tessellata. It came to scientific interest some years ago, since the northernmost population of Euphrate poplar (Populus euphraticus) was discovered there. Photo: T. Kirschey

reserve N. tessellata occupies a rather narrow stretch of a sandy desert along ephemeral creeks flanked by thorny patches of semi shrubs (Caragana sp., Salsola ericoides) interspersed with Tamarix meyeri trees. Here, sympatric herpetofaunistic species are Ophisops elegans, Hemorrhois ravergieri, and Macrovipera lebetina. In Altiagač region in Khizi district of Azerbaijan, N. tessellata is found in the valleys of Chigilchay and Gozluchay Rivers in Juniper heathlands with Juniperus excelsa and karst eutrophic lakes (Fig. 27) and the wadis with Tamarix ramossisima and Populus euphratica (Fig. 28). In the Lachin district of Azerbaijan N. tessellata inhabits a canyon of the Akera River (Fig. 9), which provides a variably rocky habitat along its steep banks (up to 30°) at elevations between 600–800 m a.s.l. in open Juniper forests [Juniperetum fruticosum] with Juniperus foetidissima, J. excelsa polycarpos and a shrub vegetation in the second layer. Coexisting herpetofaunistic species are Lacerta media, Darevskia raddei, Laudakia caucasia, Typhlops vermicularis, Eirenis modestus, E. collaris, Platyceps najadum, Marcovipera lebetina, and Bufo viridis.

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In neighboring Armenia we observed N. tessellata in a canyon of the Arpa River between Yeghegnadzor and Areni (Fig. 9). The snakes inhabited the riparian gallery forests at elevations between 800–1000 m a.s.l. with the following dominant trees: Salix australior, Ulmus carpinifolia, and concomitant Morus alba, Elaeagnus caspius and Tamarix meyeri. Numerous herpetological species are sympatric with the dice snake: Bufo vridis, Hyla savignyi, Pelophylax ridibundus, Pseudopus apodus, Ophisops elegans, Lacerta media, Hemorrhois ravergieri, Hierophis schmidti, and Macrovipera lebetina. The dice snake also occupies the frigana vegetation on the right-bank slopes of the canyon, which consists of a south-easterly exposed 40° steep slope with a prevailing vegetation of Rhamnus pallasii and subdominant Ephedra major procera. Sympatric herpetological species are Typhlops vermicularis, Hierophis schmidti, Hemorrhois ravergieri, Eirenis punctatolineatus, E. collaris, Trachylepis septemtaeniata transcaucasica, and Bufo viridis. In the Megri district of southern Armenia N. tessellata occurs at high elevations of 1800 m a.s.l. near the spring of the Megri River (Fig. 9). The vegetation con-

Natrix tessellata in the Caucasus

Fig. 29. A collage of nocturnal Natrix tessellata landing on the beach between 10 pm and midnight fed with fish at Absheron National Park, Azerbaijan. Photos: K. Mebert

Fig. 30. A dice snake pinched her lower jaw in a shell, presumably representing a hunting accident. Photo: T. Kirschey.

sists of a light oak formation [Quercetum friganosum] dominated by Quercus macranthera with a small density of 0.1–0.3 (i.e. 10–30%) and occasionally up to 1.0. Sympatric reptiles are Darevskia raddei, Lacerta media, L. strigata, Ablepharus bivittatus, Montivipera raddei, Laudakia caucasia, Platyceps najadum, and Hierophis schmidti. Behavioral Aspects of Dice Snakes in the Caucasus The majority of publications report that Natrix tessellata is characterized by diurnal activity (see refs. in Gru­ schwitz et al. 1999). Some publications presumed that this species aestivates in crevices and holes during hot and dry summer periods (e. g. Hecht 1930, Lenz & Gruschwitz 1993, Mebert 2007). However, nocturnal activity, as we have already reported from these snakes (Tunijev 2001), is a potentially overlooked behavior alternative to diurnal behavior during the hot summer

Fig. 31. Defensive coiling and striking of a Natrix tessellata from Tsav River, Armenia. This behavior resembles the defensive posture of the highly venomous and syntopic Macrovipera lebetina. Photo: B. & S. Tuniyev

Fig. 32. Deep gorges inhabited by Natrix tessellata in the Mazymchay River, Zakatala Reserve, Azerbaijan. Photo: T. Kirschey

season. Nocturnal activity is common in American natricine snakes and it usually depends on temperature, season and latitude (Gibbons & Dorcas 2004, Mebert 2010). Such a behavior was also reported in the closely related viperine snake (N. maura), with a greater proportion of individuals observed by night during July and August (Hailey & Davies 1987, Jaén-Peña & Peréz-Mellado 1989, Scali 2011). In N. tessellata, it has recently been observed in different locations of its range (in Italy, Scali et al. 2001, Scali 2011; in Greece, Mebert et al. 2011; in Hungary, Kreiner 2007). We conclude that nocturnal activity in N. tessellata is rather widespread, as we have observed them to be active at night up to 12 pm in different districts of the Western Caucasus and along the coast of the Caspian Sea (e.g. Abrau Lake, Laba River, see Fig. 9). On 2 July 2011, authors TK and KM observed numerous dice snakes landing with full stomachs between dusk and midnight

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along the Absheron Peninsula at the Bay of Baku, Azerbaijan (Fig. 29). In one such case, a dice snake landed with a shell having clamped into the lower jaw (Fig. 30). We presume that this was an accidental by-catch while trying to snap at or dig out a ground fish on the shell loaded benthos of the shallow Caspian Sea. A dice snake from the Tsav River in southern Armenia was found to exhibit a defense behavior similar to that of the syntopic Levant viper (Macrovipera lebetina). It included coiling, putting its front body into an S-shape, hissing, and most important a forward striking with the head, while keeping the mouth closed (Fig. 31). Single components of this defense behavior are known from dice snakes throughout its range (Gruschwitz et al. 1999, Mebert 2007, Lenz et al. 2008). However, a viper-like defense behavior imitation with the inclusion of a forward striking is rather rare, but has been observed by one author (KM) in a dice snake from Lake Garda, Italy, and was filmed by him in a related grass snake (Natrix natrix) from Slavonski Brod (Croatia) and one from Maggia Valley (Switzerland) (K. Mebert unpubl.), while a strike with a bite has been reported only twice (see refs. in Gruschwitz et al. 1999). We presume that many elements of behavior, including those for defense, exist in variable compositions in a population. Depending on the environmental needs and advantages, selection will locally favor one or the other behavioral set, but can rapidly (within generations) lead to an adaption for new sets of environmental conditions, affecting also the predator response. Conservation Status in the Caucasus Our observations conclude that the populations of Natrix tessellata in the Caucasus are relatively stable and locally form large concentrations. Snakes have been strongly exploited in the past, when up to 60 thousand skins of N. tessellata were collected in the 1940s along the Caspian Sea coast (Markov 1934). Along the Black Sea coast of the Caucasus, a decline in the numbers of these snakes has been noted, possibly associated with the dramatic transformations of river valleys and foothills and due to a highly intensive resort development along the entire Russian Black Sea coast. For some coastal localities in Georgia the situation and problems are quite similar (Tarkhnishvili et al. 2002). For central Azerbaijan the rapid urbanization and industrialization, especially highway construction and pollution by the petrol industry, is a threat to dice snake habitats. This species is protected on the territories of several preserves and national parks of the Caucasus, such as in the Caucasian State Biosphere Reserve, Sochi National Park, Rostov Reserve, Daghestan Reserve (Russia), Pitsunda-Myusserskiy Reserve (region of Abkhazia), Kolkhidskiy Reserve, Kintrish reserve (Georgia), Kyzyl-Agač Reserve, Zaqatala Reserve (Fig. 32), Türyanchay Reserve, Gobustan Reserve, Altiagač National Park, Absheron National Park, Ag-Göl National Park, Shirvan National Park, Hirkan National Park (Azer-

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baijan), National Park of Sevan, and Reserves of Khosrov and Shikakhoh (Armenia). References Ahmadzadeh, F., Mebert, K., Ataei, S., Rezazadeh, E., Allah Goli, L. & W. Böhme (2011): Ecological and biological comparison of three populations of the dice snake, Natrix tessellata, from the southern Caspian Sea Coast, Iran. – Mertensiella 18: 403–413. Alekperov, A.M. (1978): Zemnovodnyje I presmykajuscijesja Azerbaidzhana. – Izd. “Elm”, Baku. Ananjeva, N.B., Orlov, N.L., Khalikov, R.G., Darevsky, I.S., Rjabov, S.A. & A.V. Barabanov (2004): Atlas presmykajuscihsja Severnoy Evrasii. – ZIN RAN. Baha el Din, S. (2011): Distribution and recent range extension of Natrix tessellata in Egypt. – Mertensiella 18: 401–402. Bannikov, A.G., Darevsky, I.S., Ischenko, V.G., Rustamov, A.K. & N.N. Scherbak (1977): Opredelitel zemnovodnyh i presmykajuscijhsja fauny SSS. – Izd. “Prosveschenye”, Moscow. Bischoff, W. (1988): Zur Verbreitung und Systematik der Zauneidechse, Lacerta agilis Linnaeus, 1758. – Mertensiella 1: 11–30. Budagov, V.A. (1980): The Nature of Azerbaijan. – Izd. Ishyg, Baku. Cafuta, V (2011): First report of melanistic dice snakes (Natrix tessellata) in Slovenia. – Mertensiella 18: 442–444. Chernov, S.A. (1939): Herpetologicheskaja fauna Armjanskoy SSR i Nakhichevanskoy ASSR. – Zool. Sb. Arm. Fil. AN SSSR. Bd. 1: 79–194. Conelli, A.E. & M. Nembrini (2007): Studio radiotelemetrico dell’habitat della Biscia tassellata, Natrix tessellata (Laurenti 1768) in tre popolazioni del Cantone Ticino (Svizzera). – Bollettino della Società Ticinese di Scienze Naturali 95: 45–54. Conelli, A.E., Nembrini, M. & K. Mebert (2011): Different habitat use of dice snakes (Natrix tessellata) among three populations in Ticino Canton, Switzerland. – A radiotelemetry study Mertensiella 18: 100–116. Darevsky, I.S. (1967): Skalnye yascheritcy Kavkaza. – Izd. “Nauka”, Leningrad. Dincaslan, Y.E., Arikan, H., Ugurtas, H.I. & K. Mebert (2011): Morphology and blood proteins of dice snakes from western Turkey. – Mertensiella 18: 370–382. Dürigen, B. (1897): Die Amphibien und Reptilien Deutschlands. - Creutzsche Verlagshandlung, Magdeburg. Frotzler, N., Davitashvili, N. & K. Mebert (2011): Distribution of the dice snake (Natrix tessellata) in Georgia (Transcaucasia) and comparative notes on the genus Natrix. – Mertensiella 18: 357–364. Grillitsch, H. & Y.L. Werner (2009): The southern limit of Natrix natrix in the Levant: A detective story. – Herpetozoa 22: 65–74. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas. Band 3/IIA: Schlangen II. – AULA-Verlag, Wiesbaden: 581–644. Hailey, A. & P.M.C. Davies (1987): Activity and thermoregulation of the snake Natrix maura. 1. r and K thermoregulation. – Journal of Zoology 213: 71–80. Hecht, G. (1930): Systematik, Ausbreitungsgeschichte und Ökologie der europäischen Arten der Gattung Tropidonotus (Kuhl) H. Boie. – Mit­t. Zool. Mus. Berlin 16: 244–393.

Natrix tessellata in the Caucasus Jaén-Peña, M.J. & V. Pérez-Mellado (1989): Temperatures corporales y ritmos de actividad en una población de Natrix maura (L.) del Sistema Central. – Doñana, Acta Vertebrata, 16(2): 203–217. Khonjakina, Z.P. (1969): Materialy po rasprostraneniju i biologii vodjanogo uzha v Dagestane. – Spornik nauchnykh soobscheniy kaf. zool. DGU Сб. – Makhachkala: 82–84. Kirschey, T., Schmidt, S. & T. Iskanderov (2009): Distribution of reptiles on small islands in the Caspian Sea within the territory of Azerbaijan. – 15th European Congress of Herpetology, Kuşadasi, Turkey: 196. Kramer, E. & O. Stemmler (1988): Schematische Verbreitungs­ karten der Schweizer Reptilien. – Revue Suisse de Zoologie 93(3): 779–802. Krasawtzev, B.A. (1934): O pitanii nekotorykh zmej v Dagestane. – Izv. 1 i 2 Severo-Kavkazskogo Ped. Instituta. Bd. 2/P. Ordzhonikidze: 221–222. Kreiner, G. (2007): Schlangen Europas. – Edition Chimaira, Frankfurt am Main, Germany. Kwet, A. & K. Mebert (2010): The Dice Snake – Natrix tessellata. – Reptilia (GB) 72: 39–43. Laňka, V. (1978): Variabilitat und Biologie der Würfelnatter (Natrix tessellata). – Acta Universitatis Carolinae Biologica 1975– 1976: 106–207. Lantz, L. & C. Cyrén (1947): Les lezards sylvicoles de la Caucasie. – Bull. Soc. Zool. France, T. 72: 169–191. Langhammer, M. (2009): Ecology of coastal plant communities at Absheron National Park, Azerbaijan. – M.S. thesis, University of Greifswald. Available at: www.succow-stiftung.de/ tl_files/pdfs_downloads/Diplomarbeiten/2009_Maria_Langhammer_Diplomarbeit.pdf. Lenz, S. & M. Gruschwitz (1993): Zur Autökologie der Würfelnatter, Natrix t. tessellata (Laurenti 1768), in Deutschland. – Mertensiella 3: 235–252. Lenz, S., Mebert, K. & J. Hill (2008): Die Würfelnatter: Reptil des Jahres 2009. –Aktionsbroschüre. – DGHT, Rheinbach, Germany. Lukina, G.P. (1963): Taxonomichesky status i biologia skalnykh jascheric Lacerta saxicola Eversmann iz severo-zapadnogo predela rasprostranenija na Kavkaze. – Doklady Academii Nauk AzSSR No 6: 53–61. MacCulloch, R.D., Fu, J., Darevsky, I.S. & R.W. Murphy (2000): Genetic evidence for species status of some Caucasian rock lizards in the Darevskia saxicola group. – Amphibia-Reptilia 21(2): 169–176. Markov, E.L. (1934): Okhotnichje khozjastvo Zakavkazja. – Izd. ZakGIZ, Tiflis, Georgia. Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Mebert, K. (2007). The dice snake at Lake Brienz. – In: Annual Volume 2007, Shore-Conservation of the lakes Brienz and Thun. – UTB Publishing, Thun: 169–180 (in German). Mebert, K. (2010): Massive Hybridization and Species Concepts, Insights from Watersnakes. – VDM Verlag, Saarbrücken, Germany. Mebert, K. (2011): Geographic variation of morphological characters in the dice snake Natrix tessellata (Laurenti 1768). – Mertensiella 18: 11–19. Mebert, K., Trapp, B., Kreiner, G., Billing, H., Speybroeck, J. & M. Henggeler (2011): Nocturnal activity in Natrix tessel-

lata: a neglected aspect of its behavioral repetoire. – Mertensiella 18: 234–236. Mertens, R. (1957): Die Würfelnatter (Natrix tessellata) der Schlangeninsel. – Senck. Biol. 38: 271–275. Mertens, R. (1969): Zur Synonymie und Variabilität der Würfelnatter (Natrix tessellata). – Senckenbergiana Biologica 50(3/4): 125–131. Muggiasca, F. & E. Gandolla (1976): I rettili del Ticino. – Canobbio-Lugano, Switzerland. Muskhelishvili, T. (1970): Presmykajuscijesja vostochnoj Gruzii. – Izd. “Mezniereba”, Tbilisi. Neumann, C. & K. Mebert (2011): Migration behavior of endangered dice snakes (Natrix tessellata) at the River Nahe, Germany. – Mertensiella 18: 39–48. Nilson, G., Tuniyev, B.S., Orlov, N.L., Höggren, M. & C. Andrén (1995): Systematics of the vipers of the Caucasus: polymorphism or sibling species? – Asiatic Herpet. Research 6: 1–26. Oken, L. (1816): Lehrbuch der Naturgeschichte III. 3. Theil. Zoologie. 2. Abtheilung Fleischthiere. – August Schmid & Comp., Jena: 232–233. Orlov, N. & B.S. Tuniyev (1990): Three Species in the Vipera kaznakovi Complex (Eurosibirian Group) in the Caucasus: their present distribution, possible genesis, and phylogeny. – Asiatic Herpet. Research 3: 1–36. Ryabinin, D.M., Grechko, V.V., Darevsky, I.S., Ryskov, A.P. & S.K. Semenova (1996): Comparative study of DNA repetitive sequences by means of restriction endonucleases among populations and subspecies of some lacertid lizard species. – Russian Journal of Herpetology 3(2): 178–185. Scali, S. (2011): Ecological comparison of the dice snake (Natrix tessellata) and the viperine snake (Natrix maura) in northern Italy. – Mertensiella 18: 131–144. Scali, S., Dimitolo, G. & S. Montonati (2001): Attività notturna comparata di Natrix maura e Natrix tessellata. – Pianura 13: 287–290. Schmidt, S. & M. Uppenbrink (Eds.) (2009): Potential analysis for further nature conservation in Azerbaijan – A spatial and political investment strategy. – Geozon Science Media, Greifswald. Available at: www.succow-stiftung.de/tl_files/pdfs_ downloads/Buecher und Broschueren/mava_web.pdf. Schweizer, H. (1962): Beitrag zur Kenntnis der schwarzen Würfelnatter am Luganer See. – Aquar. Terrar. Zeitschrift 15: 47–50. Tarkhnishvili, D., Kandaurov, A. & A. Bukhnikashvili (2002): Declines of amphibians and reptiles in Georgia during the 20th century: virtual vs. actual problems. – Zeitschrift für Feldherpetologie 9(1): 89–107. Tuniyev, B.S. (2001): Nochnaja aktivnost reptiliy Zapadnogo Kavkaza. Mater. – Nauch.-prakt. Konf. Majkop: 229–230. Tuniyev, B.S., Orlov, N.L., Ananjeva, N.B. & A.L. Agasyan (2009): Zmei Kavkaza: taxonomicheskoye raznoobrazie, rasprostranenie, okhrana. – Izd. KMK, St.-Petesburg - Moscow. Tuniyev, B.S. & S.V. Ostrovskikh (2001): Two new species of vipers of the “kaznakovi” complex (Ophidia: Viperinae) from the Western Caucasus. - Russian Journal of Herpetology 8(2): 117–126. Tuniyev S.B. & B.S. Tuniyev (2008): Intraspecific variation of the sand lizard (Lacerta agilis) from the Western Caucasus and description of a new subspecies Lacerta agilis mzymtensis ssp. nov. (Reptilia: Sauria). – Russian Journal of Herpetology 15(1): 55–66.

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Velenský, M., Velenský, P. & K.Mebert (2011): Ecology and ethology of dice snakes (Natrix tessellata) in the city district Troja, Prague. – Mertensiella 18: 157–176.

Werner, F. (1897): Über einige noch unbeschriebene Reptilien und Batrachier. – Zoologischer Anzeiger 20: 261–267. Wütschert, R. (1984): Neues über die Reptilienfauna der Insel Korfu. – Salamandra 20 (4): 221–228.

Authors Boris S. Tuniyev, Sako Tuniyev, Sochi National Park, Sochi, Russia, e-mail: [email protected]; Tom Kirschey, Fürstenberger Str. 6, 16775 Menz, Germany, e-mail: [email protected]; Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland, e-mail: [email protected].

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20 September 2011

ISBN 978-3-9812565-4-3

Distribution of the Dice Snake (Natrix tessellata) in Georgia (Transcaucasia) and Comparative Notes on the Genus Natrix Norbert Frotzler, Nino Davitashvili & Konrad Mebert Abstract. Natrix tessellata is relatively common and widely distributed in Georgia. It inhabits most aquatic habitats available in the country. The vertical distribution spans from 0–600 m in the west and 900 m in the east, with few observations up to 1100 m a.s.l, but a negative correlation between precipitation and occurrence at higher altitudes has been documented. Compared to the grass snake (Natrix natrix), the dice snake has a lower abundance in climatically wet areas, whereas N. tessellata occurs more frequently in semi-arid regions. Key words. Distribution, habitat, Natrix tessellata, Caucasus, Republic of Georgia Zusammenfassung. In Georgien ist Natrix tessellata häufig und weit verbreitet. Sie besiedelt hier die meisten aquatischen Habitatstypen des Landes. Die vertikale Verbreitung liegt zwischen 0 und 600 m im Westen und 900 m im Osten, mit wenigen Beobachtungen bis zu 1100 m über Meer. Eine negative Korrelation zwischen Niederschlag und Vorkommen in grösserer Höhe wurde dokumentiert. Im Vergleich zur Ringelnatter (Natrix natrix), besiedelt die Würfelnatter die humiden Landesteile in geringerer Häufigkeit, während sich dieses Verhältnis in semi-ariden Gebieten kehrt. Schlagwörter. Verbreitung, Habitate, Natrix tessellata, Kaukasus, Georgien

Introduction Dice snakes rank second among Georgian snake-species in distribution area and abundance, just behind the almost ubiquitous grass snake (pers. obs.). Despite this abundance, previous authors working on the Georgian herpetofauna have not paid much attention to this species. Unfortunately, lack of detailed information about sites of occurrence and insufficient map resolution has prevented a clear identification of localities in many Soviet-era publications. At present, only two publications provide some reliable information about the distribution of the species within Georgia (Nikolski 1913, Muskhelishvili 1970). The present article is based on recent field observations and aims at presenting an updated account on the distribution of the dice snake and a critical review of data from the literature. The new distribution data well fill the gaps in the report by Tuniyev et al. (2011) on the distribution of the dice snake along the Caucasian Isthmus. Material and Methods Numerous herpetological observations were made during botanical studies from 1997 to 2008 and during an excursion by a team of the ÖGH, Österreichische Gesellschaft für Herpetologie = Austrian Society of Herpetology (Frotzler et al. 2008). The information was not specifically gathered for an investigation on Natrix tessellata, but localities, where snakes have been observed, were recorded during the botanical field work and herpetological field trips; no particular counting of individuals per site was conducted. To complete the account

on the Georgian distribution of N. tessellata, data from Nikolski (1913) and Muskhelishvili (1970) were incoporated, whereas David Tarkhnishvili and Tom Kirschey provided information based on their personal unpublished observations. Geographically unclear descriptions of localities have been disregarded. Data from the literature have been marked with asterisks in the text and distinct symbols on the map (Fig. 1). Results and Discussion Dice snakes are quite common in most areas of Georgia. They have mainly been recorded at elevations between 0 m at the Black Sea to ca. 600 m a.s.l. in the humid western parts, but reaching up to 900 m on drier plateaus of the east. Only few records of sites at elevations > 1000 m a.s.l. from the central and eastern parts of the Lesser Caucasus have been documented and these are situated in regions where precipitation levels are low (up to approximately 600 mm mean annual precipitation). For example, a single observation at Khertvisi (1126 m) on the upper reaches of the Mtkvari (Kura) during an excursion in 2007 confirms their presence at much higher elevations in at least the central part of the Lesser Caucasus. Although Nikolski (1913) stated that Natrix tessellata does not occur in the alpine zone of Georgian mountain ranges, Muskhelishvili (1970) supposed the species to be present here too. Records from the higher, mountainous regions of the Greater Caucasus are still lacking and evidence of occurrences in this part of Georgia is confined to riverbeds and foothills along the southern margins of the mountain chains.

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Fig. 1. Map of Georgia, showing the sites where N. tessellata is known to occur. Shaded areas: regions >1500 m a.s.l., triangles: data from literature and from unpubl. observations of D. Tarkhnishvili and T. Kirschey, circles: personal observations of the authors. Numbers 2–12 refer to figures. Abb. 1. Karte von Georgien mit den bekannten Fundorten von N. tessellata. Graue Flächen: Gebiete >1500 m Seehöhe, Dreiecke: Angaben aus der Literatur und nicht publizierte Beobachtungen von D. Tarkhnishvili und T. Kirschey, Kreise: Eigene Beobachtungen der Autoren. Nummern 2–12 beziehen sich auf die Abbildungen.

However, Nikolski (1913) mentioned an occurrence at Tsalka “close to Tbilisi”. Tsalka lies at 1400 m in the eastern part of the Lesser Caucasus, ca. 60 km west of Tbilisi, but this record needs to be confirmed since at that time it was common to label locations by referring to the nearest town. Hence, the account may refer to locations somewhere downstream along the Khrami or Algeti rivers on the road from Tbilisi to Tsalka, where the occurrence of dice snakes was confirmed later. Nevertheless, an occurrence at Tsalka cannot be ruled out at the moment. In Georgia, N. tessellata inhabits several different types of water bodies, such as ponds, lakes, marshes, brooks, rivers and channels, with either still or slow to fast running water. It is found in almost every type of landscape (lowland swamp forests and marshes at the Black Sea coast, where annual precipitation exceeds 2000 mm, to steppes and semi-deserts in the east, Figs. 1–12). The only exceptions are high mountain regions and dense montane forests in areas with particulary wet climates, probably due to the dice snake’s preference for open, sun-exposed habitats (Mebert 2011). The highest concentration of localities lies within the dry basins of central and eastern Georgia with numerous records from the catchments of all the main river systems. The species has also populated the majority of persistent lentic (non- or slow-moving) water bodies, such as ponds and lakes in that area. N. tessellata appears to have benefited from some aspects of agriculture, as it was often observed in plantations of water reserves and artificial channels used either for drainage or irrigation.

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In eastern Georgia, we sometimes found the dice snake in substantially higher numbers than the grass snake, especially on the banks of water bodies with more or less bare ground or open vegetation. Occasionally, N. tessellata even occurs in ditches along temporary brooks in gorges and ravines of savannas, steppes and semi-deserts of the Shiraki region in the southeast, where grass snakes were never observed. An analogous situation has been reported from the Iberian Peninsula, where N. maura is more frequent than the sympatric N. natrix astreptophora in drier regions (Braña 1998). In semi-deserts of the Shiraki-region in southeastern Georgia, the dice snake appears to depend exclusively on tadpoles and juveniles of the marsh frog, Pelophylax ridibundus, for food. Generally, in riparian forests of central and eastern Georgia, the two species were observed to be roughly equally distributed, but frequencies varied considerably between sites. In contrast, in the humid west, grass snakes were observed in much higher numbers than N. tessellata; often up to ratios of a couple of dozens grass snakes to one dice snake. Here, the dice snake can be found in various coastal habiats, including brackish and even marine environments along the Black Sea. It inhabits the Kolkheti lowlands, reaching the forelands and foothills of the Greater Caucasus along the Rioni River and its tributaries. Although some observations were made in swamp forests such as in the Kolkheti Nature Reserve at the Pichora River, close to Poti, a preference for more open habitats seems to be apparent. Frequent fieldwork in Adjara´s forests (southwestern Georgia), well known

Distribution of Natrix tessellata in Georgia

Fig. 2. Swamp at the southern edge of Paleostomi Lake at the Black Sea coast near Poti. In western Georgia, dice snakes are widely distributed along the coast and the Kolkheti lowlands. They occur in high densities mainly in more open habitats. Abb. 2. Sumpf am südlichen Ufer des Paleostomi-Sees an der Schwarzmeerküste bei Poti. In Westgeorgien ist die Würfelnatter im Küstenbereich und in der Kolchis-Ebene weit verbreitet. Grössere Populationen sind vor Allem in offeneren Bereichen anzutreffen.

Fig. 3a. Habitat of the dice snake at the mouth of the Chorokhi River: a pond next to the river; (insert) a dice snake from there. Photos: T. Bader & C. Riegler Abb. 3a. Würfelnatternbiotop im mündungsnahen Bereich des Tschorochi Flusses: ein Weiher nahe dem Fluss; (eingefügt) eine Würfelnatter daraus.

Fig. 3b. Charnali Valley, Adjara. At low elevations, N. tessellata occurs along small rivers in the hilly terrain in the coastal region. Photo: T. Bader & C. Riegler Abb. 3b. Tscharnali-Tal, Adscharien. In niedrigen Lagen des Hügellandes der Küstenregion kommt N. tessellata an kleineren Flüssen vor.

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Fig. 4. Khertvisi (1126 m a.s.l.) in the Lesser Caucasus, where the Paravani River (left) meets the upper Mtkvari (right), is the highest altitude, where we observed a N. tessellata (insert). Photo: T. Bader & C. Riegler Abb. 4. Chertwisi (1126 m Seehöhe) im Kleinen Kaukasus, wo der Parawani-Fluss (links) auf den Oberlauf der Kura trifft (rechts), ist das höchstgelegene Vorkommen, wo wir eine N. tessellata (eingefügt) beobachten konnten.

Fig. 5. Kus Tba (Turtle Lake), Tbilisi. N. tessellata occurs in almost all suitable habitats around the capital. Photo: T. Bader & C. Riegler Abb. 5. Kus Tba (Schildkrötensee), Tiflis. N. tessellata kommt in beinahe allen geeigneten Habitaten um die Hauptstadt vor.

for their richness in endemics, did not yield any dice snakes apart from the coastal region, where the species is quite common in swampy areas of the lowlands (e.g. Denk et. al. 2001). At low elevations, it also occurs along

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Fig. 6. Artificial channel for irrigation near Gardabani, southeast of Tbilisi. Dice snakes profit from plantations of artificial lakes, ponds, water reservoirs and channels. Abb. 6. Künstlicher Bewässerungskanal bei Gardabani, südöstl. Tiflis. Würfelnattern profitieren von künstlich angelegten Seen, Teichen, Wasserspeichern und Kanälen.

small rivers of the densely forested, hilly terrain along the coast up to 200 m a.s.l. In the Chorokhi Valley, the species occurs in drier conditions upstream in the Turk-

Distribution of Natrix tessellata in Georgia

Fig. 7. Djandaris Tba, a typical steppe lake in the Gardabani region southeast of Tbilisi at the border to Azerbaijan. Compared with N. natrix, dice snakes are more prone to open banks of water bodies. Abb. 7. Dschandaris Tba, ein typischer Steppensee in der Gardabani-Region südöstl. Tiflis an der Grenze zu Aserbeidschan. Im Vergleich mit N. natrix werden von der Würfelnatter offene Uferbereiche eher vorgezogen.

Fig. 9. Tchatchuna Reserve south of the Iori River (background), southeastern Georgia at the border to Azerbaijan. Here N. tessellata was found in small ditches along temporary brooks. Abb. 9. Tschatschuna Reservat südlich des Iori-Flusses (Hintergrund), Südostgeorgien an der Grenze zu Aserbeidschan. Hier fanden wir N. tessellata an Wasserlöchern entlang temporärer Gerinne.

Fig. 8. Iori Reserve, narrow stripe of Gallery forest and shrubs at the Iori River, southeastern Georgia. In drier regions of eastern Georgia, N. tessellata is more frequent than N. natrix. Abb. 8. Iori Reservat, schmaler Streifen uferbegleitender Gehölze am Iori-Fluss, Südostgeorgien. In trockeneren Gebieten Ostgeorgiens ist N. tessellata häufiger als N. natrix.

Fig. 10. Chiauri, floodplain forest at the Alazani River, Kakheti, eastern Georgia. In riparian forests of central and eastern Georgia, both Natrix species appear to be roughly equally distributed. Abb. 10. Tschiauri, Auwald am Alasani-Fluss, Kacheti, Ostgeorgien. In den Auwäldern Zentral- und Ostgeorgiens kommen beide Natrix-Arten in annähernd gleicher Dichte vor.

ish part of the valley. Therefore, we presume that it occupies more or less continuously the entire river valley and the lower courses of its tributaries, but probably in variable frequencies. In contrast, N. tessellata seems to have been replaced by the grass snake in montane forests in Adjara´s hinterland, where the latter occurs in very high numbers. This is an area with extraordinary high precipitation (up to > 4000 mm), that is more or less equally distributed over the year. Such ecological characteristics are more suitable to N. natrix (see reports in Mebert 2011). Furthermore, competition for tadpoles and other relevant resources by the large number of grass snakes, in particular the juveniles, may be additional factors leading to the absence of N. tessellata

in this area. The much broader diet of N. natrix, which benefits from the almost year round supply of amphibians, such as Pelophylax ridibundus, Rana macrocnemis and Bufo verrucosissimus is in marked contrast to the mainly piscivorous N. tessellata, although locally dice snakes feed on anurans. We found that eggs and hatchlings of grass snakes in Adjara´s humid forests seem to be of particularly large size, similar to reports for individuals from Sochi, also eastern Black Sea, by Velenský (1997). Interestingly, most (but not all) specimens of the grass snakes, that were found within rich and dense forests, were melanistic, with particular large heads, sometimes even in

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Fig. 11. Aragvi Valley at Ananuri (900 m a.s.l.), Greater Caucasus. N. tessellata is quite common on gravel beds along rivers of lower parts of the Greater Caucasus Abb. 11. Aragwi-Tal bei Ananuri (900 m Seehöhe), Grosser Kaukasus. An den Schotterbänken der Flüsse der tiefer gelegenen Teile des Grossen Kaukasus ist N. tessellata recht häufig anzutreffen.

Fig. 12. Upper Iori Valley, foothills of the Greater Caucasus. Here, the occurrence of dice snakes is mentioned in the literature. Abb. 12. Tal des oberen Iori, Vorgebirge des Grossen Kaukasus. In der Literatur werden Vorkommen der Würfelnatter hier erwähnt.

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Fig. 13. Young male specimen of N. natrix from the mountains east of Kirnati, Adjara, with a prominent broad head. Adults of this morph are apparently always black. Abb. 13. Junges Männchen einer N. natrix aus den Bergen östl. Kirnati, Adscharien mit auffallend breitem Kopf. Adulte Exemplare dieser Form sind anscheinend immer schwarz gefärbt.

Distribution of Natrix tessellata in Georgia

Fig. 14. Dice snake, N. tessellata, with typical coloration and pattern from Georgia: (large) from the mouth of the Chorokhi River; (small insert) from Ananuri, 900 m a.s.l., Aragvi Valley, Greater Caucasus. Photos: N. Frotzler & C. Riegler Abb. 14. Würfelnattern, N. tessellata, mit typischer Färbung und Zeichnung aus Georgien: (grosse Abb) vom Mündungsbereich des Tschorochi; (kleine Abb.) aus Ananuri (900 m Seehöhe, Aragwi-Tal, Grosser Kaukasus).

relatively small males (Fig. 13). Such forms have been proposed as a new species, the bighead grass snake Natrix megalocephala, by Orlov & Tunijev (1987). However, subsequent accounts including few data on genetics, morphology and ecology of those individuals do not conclude that N. megalocephala represents a distinct species (Hille 1997, Velenský 1997, Orlov & Tuniyev 1999, Jandzik 2005). Rather, they suggest the existence of a distinct morph of the grass snake which is endemic to ancient coastal regions of Pleistocene refuges, when the Caucasus was a peninsula. This morph may represent an ecotype or an incipient species, whose further independent evolution may have been interrupted by introgression from the regional common form, N. natrix scutata. Most Georgian specimens display the pattern and coloration typical of N. tessellata with a dorsal color of olive, to brown or grey (Fig. 14, Gruschwitz et al. 1999). Melanistic individuals were reported from Kutaisi and Ajameti at the eastern edge of the Kolkheti lowlands and from Kobuleti at the Black Sea coast. Acknowledgements We are grateful to David Tarkhnishvili, who helped with the search for literature and with data from per-

sonal observations. Tom Kirschey provided additional data from personal observations. Thomas Bader and Christoph Riegler contributed with photos of habitats and snakes (Figs. 3, 4, 5, 6, 12, and in 13, 14). Thanks to Hugh Rice who improved the initial version of the English text. References Braña, F. (1998): Natrix natrix (Linnaeus, 1758). – In: Salvador, A. (Ed.): Fauna Ibérica vol. 10, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas (csic), Madrid: 454–466. Denk, T., Frotzler, N. & N. Davitashvili (2001): Vegetational patterns and distribution of relict taxa in humid temperate forests and wetlands of Georgia (Transcaucasia). – Biological Journal of the Linnean Society 72: 287–332. Frotzler, N., Bader, T. & C. Riegler (2008): Herpetologische Exkursion nach Georgien – 3.–20. Mai 2007. Availabe at: http://www.herpetofauna.at/berichte/georgien2007/Georgien_Teil1.php Gruschwitz, M., Lenz, S., Mebert, K. & V. Lanka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Hille, A. (1997): Biochemical variation between populations of the western and eastern grass snake (Natrix Natrix) from

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Norbert Frotzler, Nino Davitashvili & Konrad Mebert the transition zone in Nordrhein-Westfalen, Germany. – In: Böhme, W., Bischoff, W. & T. Ziegler (Eds.): Herpetologia Bonnensis: 177–184. Jandzik, D. (2005): Record of a black-coloured Natrix in northeastern Turkey, with comments on the validity of the bigheaded grass snake, Natrix megalocephala Orlov & Tuniyev, 1987. – Zoology in the Middle East 34: 27–34. Mebert, K. (Ed.) (2011): The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species. – Mertensiella 18, DGHT, Rheinbach, Germany. Muskhelishvili, T.A. (1970): Natrix tessellata. – In: Muskhelishvili, T.A. (Ed.), Пресмыкающиеся Восточной Грузии (Reptiles of Eastern Georgia). – Mecniereba, Tbilisi: 135–142. Nikolski, A.M. (1913): Tropidonotus tessellatus Laur. – In: Nikolski, A.M. (Ed.): Herpetologia Caucasica. – The Caucasus Museum, Tbilisi: 130–143 (in Russian). Orlov, N.L. & B.S. Tuniyev (1987): Новый вид ужа Natrix megalocephala sp. nov. с Кавказа (Ophidia: Colubridae) (A new species of water snakes Natrix megalocephala sp. nov. from the Caucasus / Ophidia: Colubridae). – Proceedings of the Zool. Inst. Academy of Sciences USSR 158: 116–130. Orlov, N.L. & B.S. Tuniyev (1999): Natrix megalocephala (Orlov & Tuniyev, 1987) – Grosskopf-Ringelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 505–612. Tuniyev, B., Tuniyev, S., Kirschey, T. & K. Mebert (2011): Notes on the dice snake, Natrix tessellata, from the Caucasian Isthmus. – Mertensiella 18: 343–356. Velenský, P. (1997): Natrix megalocephala, Orlov et Tuniyev, 1987: A new species of the European reptiles fauna? – Gazella, Prague 24: 177–186.

Appendix List of locality records of Natrix tessellata in Georgia, sorted by physiographic regions (in bold); data from literature with asterisks. Abkhazeti: Gagra*, Bichvinta (Tarkhnishvili, pers. obs. mid-1970s), Gudauta*, Tsebelda*. Guria, Rioni estuary: Poti, Paleostomi Lake (Fig. 2), Pichora River (Kolkheti Nature Reserve). Imereti, upper Rioni River: Kutaisi, Ajameti. Adjara: Kobuleti, Kintrishistskali (Kirschey, pers. obs. 2006), Mouth or Chorokhi River (Fig. 3a), Charnali Valley (Fig. 3b), Batumi, Lower Chorokhi Valley, Lower Adjaristskali Valley (Kirschey, pers. obs. 2006). Meskhet-Javakheti, upper Mtkvari River: Khertvisi (Fig. 4), Akhaltsikhe*, Chobiskhevi near Borjomi. Kartli, Mtkvari River and tributaries: Surami*, Gori, Uplistsikhe, Liakhvi River*, Tana River*, Kaspi*, Lekhura River*, Chala*, Samtavisi*, Natakhtari*, Mtskheta, Saguramo*. Kartli, Tbilisi and surroundigs: Kus Tba (Fig. 5), Lisis Tba, Vereskheoba, Didube* (probably extinct), Tbilisis Sghva*. Gardabani, lower Mtkvari River: Rustavi, Iaghluja*, Gardabani (Fig. 6), Djandaris Tba (Fig. 7), Garedji*. Kvemo Kartli, Algeti River: Marneuli. Khrami River: “Tsalka“* (Eastern Smaller Caucasus), Bolnisi. Shiraki, Iori River: Ucharma*, Sartichala, Sagaredjo, Didi Shiraki, Iori Reserve (Fig. 8), Tchatchuna Reserve (Fig. 9), Pantishara*, Eldari, Kasristskali*. Kakheti, Alazani River and tributaries: Telavi, Chiauri (Fig. 10), Lower Alazani River. Foreland of the Greater Caucasus: Lechkumi* (Tskhenistskali River), Tkibuli*, Ananuri (Aragvi Valley, Fig. 11), Basaletis Tba near Dusheti* (Aragvi Valley), Orkhevi* (Upper Iori River, Fig. 12), Lagodekhi.

Authors Norbert Frotzler, Institute of Palaeontology, University of Vienna, Geozentrum, Althanstrasse 14, 1090 Vienna, Austria, e-mail: [email protected]; Nino Davitashvili, Environmental Manager, USAID Economic Prosperity Initiative (EPI), 6, Samgebro St, Tbilisi 0105, Georgia; Konrad Mebert, Siebeneichenstrasse 31, 5634, Merenschwand, Switzerland

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MERTENSIELLA 18

365-369

20 September 2011

ISBN 978-3-9812565-4-3

A Preliminary Study on the Feeding Biology of the Dice Snake, Natrix tessellata, in Turkey Bayram Göçmen, Kerim Çiçek, Mehmet Z. Yildiz, Mehmet K. Atatür, Yunus E. Dinçaslan & Konrad Mebert Abstract. Food composition of the Dice snake, Natrix tessellata, was studied in the Anatolian part of Turkey. A total of 76 prey items were recorded from 51 museum specimens and compared between sexes and age groups. The diet of N. tessellata consists almost entirely of fishes (72.4%). The remaining stomach contents were insects (7.9%), gastropods (2.6%), amphibians (14.5%), reptiles (1.3%), and mammals (1.3%). Our results confirm that Turkish N. tessellata forage predominantly in water. Food composition did not differ significantly between sexes and age groups, but the largerst prey items were consumed by relatively large females. Key words. Squamata, Serpentes, Natrix tessellata, food composition, Turkey Zusammenfassung. Eine Nahrungsanalyse von Würfelnattern, Natrix tessellata, aus dem anatolischen Teil der Turkei wurde vorgenommen. Ein Total von 76 Beutetieren wurde in 51 Museumsexemplaren gefunden und zwischen den Geschlechtern und Altersgruppen verglichen. Die Nahrung der N. tessellata bestand fast gänzlich aus Fischen (72.4%). Die übrigen Magenbefunde waren Insekten (7.9%), Schnecken (2.6%), Amphibien (14.5%), Reptilien (1.3%), und Säuger (1.3%). Unsere Resultate bestätigen, dass N. tessellata hauptsächlich im Wasser auf Nahrungssuche geht. Es gab keine deutliche geschlechtsspezifische oder altersbedingte Unterschiede in der Nahrungswahl, außer dass die größten Beutetiere von relativen großen Weibchen konsumiert wurden.

Introduction

Materials and Methods

Snakes can be expected to exhibit unusual feeding habits compared to other ectothermic vertebrates because of their elongated morphology and ecological characteristics, e.g. being obligate carnivores, swallowing their prey whole, and preferring a solitary life style. Analyses of global feeding preferences in snakes are ideally suited to illustrate the unusual nature of feeding behavior of these fascinating animals (Luiselli 2006). The majority of snake species inhabiting the Mediterranean region have a large geographical distribution (e.g. Bruno & Maugeri 1990, Schultz 1996) and are ecologically little specialized (e.g. Pleguezuelos & Moreno 1990, Luiselli & Agrimi 1991, Capula & Lui­ selli 2002, Pleguezuelos & Fahd 2004, Filippi et al. 2005, Luiselli et al. 2005, Santos et al. 2005). The dice snake, Natrix tessellata, is a medium sized semi-aquatic snake with a maximum length of around 130 cm (Gru­ schwitz et al. 1999). While there are several studies on the feeding habits of N. tessellata (e.g. Laňka 1978, Luiselli & Rugiero 1991, Lenz & Gruschwitz 1993, Filippi et al. 1996, Zimmermann & Fachbach 1996, Luiselli et al. 2007), there are no detailed studies describing diets or feeding behavior in Turkish populations. The aim of the present work is to determine the types and diversity of prey consumed by dice snakes, Natrix tessellata, of Anatolia, to contribute to the general knowledge of the ecology of Turkish populations of this species.

We examined the stomach contents of 51 preserved specimens of Natrix tessellata (15 males, 20 females, 16 juveniles) from the herpetological museum at the Zoology Department, Ege University (ZDEU), collected from different parts of Anatolia, Turkey (see Appendix). We investigated stomach contents by making a midventral incision to open the stomach. We did not dissect type specimens or specimens in poor condition. For each specimen with prey in its stomach, we recorded its locality, snout-vent length (SVL), and total length (TL) in millimeters. The prey items were determined to the lowest possible taxonomic level. Snakes were grouped according to their sex and size (juvenile: < 280 mm SVL; adult: > 280 mm SVL). Adult size was based on a male with straw colored testes and the mentioned minimal length, presumably representing maturity (dissection by second author). Such small size of mature males is also reflected in the successfull reproduction event involving a one-year old N. tessellata under captive conditions (Trobisch-Gläßer & Trobisch 2001). The proportion of specific prey taxa in the diet of N. tessellata (n%) and the frequency of snakes containing a specific prey taxa (f%) was calculated. Some stomach contents included pebbles and soil particles. However, we assume that this material was ingested accidentally during feeding, and, hence, we did not consider it as a part of the diet. To estimate the similarity in the diet between adults, juveniles and the sexes, Pianka’s overlap index (Pianka 1973) was applied. This index varies between 0 (no similarity) and 1 (large similarity). Food-niche breadth was

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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calculated using Shannon’s index (Shannon 1948). Undetermined prey items were not considered in our calculation of food-niche breadth and similarity. All niche calculations were done using the “EcoSim 700” program (Gotelli & Entsminger 2009) and all statistical analyses were performed using SPSS 10.0 with the alpha level set at 5%. Results Sexes differed in SVL (Student’s t-test, t1, 49 = 3.130, P = 0.003) and TL (t1, 49 = 3.018, P = 0.004) with females being slightly larger than males (Tab. 1). A total of 76 prey items were retrieved and determined from the stomachs. All snakes contained prey. The number of prey items in a stomach varied between 1 and 5 (mean: 1.0 ± 0.92). More than one prey item was found in 16 specimens (31.37%), the other 35 specimens (68.62%) contained a single prey item. A comparison among males, females and juveniles showed no statistical difference in consuming distinct prey taxa (One-Way ANOVA, F2, 48 = 2.595, P = 0.085). Members of four vertebrate groups (Actinopterygii, Amphibia, Reptilia, and Mammalia) and two invertebrate groups (Gastropoda, Insecta) were found in the stomach contents (Tab. 2). Fish constituted the primary prey group consumed (n% = 72.4%). Among the prey groups, the most diverse one was Insecta (7.9%) with four families identified: Carabidae (1.3%), Scarabaeidae (2.6%), Dytisciade (1.3%), and Formicidae (2.6%). Gastropods (2.6 %) were detected only in males, while both sexes contained insects. Interestingly, only Dytiscus marginalis is an aquatic species. Largest prey ingested were the fish Esox lucius (approx. TL 230 mm), the lizard Lacerta trilineata (approx. TL 200 mm) and a mouse Dryomys nitedula (approx. TL 320 mm), which all were found in large females N. tessellata (TL= 88.70; 85.80; 91.50 mm respectively). Only 14.4% of the food content consisted of terrestrial prey items (members of Carabidae, Scarabaeidae, Formicidae, Bufonidae, Lacertidae, Gliridae), whereas the remaining 85.6% were aquatic prey. The large majority of the food contents (89.5%) consisted of vertebrates. As suggested by Pianka’s niche overlap index, the two sexes shared a large similarity in their diet (Tab. 3). Food niche breadth (Shannon’s index) was 0.872, 0.838 and 0.798 in males, females and juveniles, respectively.

Discussion Based on our data, Natrix tessellata appears to be predominantly piscivorous in Anatolia, which concurs with most observations from other regions (see refs. in Gru­ schwitz et al. 1999), but also from Turkey (Franzen et al. 2008). However, the proportion of fish items in the diet of N. tessellata can vary greatly. For example, in populations from Central Italy, it ranged from 59.25% (Luiselli & Rugiero 1991), 60-66% (Bagnoli 1985), to approximately 97% (Filippi et al. 1996, Luiselli et al. 2007) and to 98% in southern Austria (Zimmermann & Fachbach 1996). Besides fish, the second largest proportion on prey items in N. tessellata consists of amphibians, mostly anurans and often their tadpoles, which are consumed by juvenile snakes (Luiselli et al. 2007). The proportion of amphibian diet in N. tessellata varies geographically to approximately complement the missing fish diet (see review in Gruschwitz et al. 1999). For example, Darevskij & Terentev (1967) pointed out that in Russian populations 58% of the prey consisted of fishes, the remainder being amphibians. In some Asian population, N. tessellata consumes more amphibians than fish, with some sites lacking fish whereas others contain an abundance of fish (see Esterbauer 1985, 1994 for southwestern Syria; Selkownikov cit. in Nikolskij 1916 for Azerbaijan; and Hecht 1930 for mountain streams of western Asia). The proportion of amphibian diet is much smaller in populations of N. tessellata from Western Europe. Although, the complementing proportion in the diet of central Italian N. tessellata consisted mostly of amphibians, it constitutes a small portion. For example, Filippi et al. (1996) found that less than 3% of prey items consisted of the anurans Rana italica and Bufo bufo. Also in Italy, Luiselli et al. (2007) found between 1.1-4.7% of anuran prey. Interestingly, such geographic variation appears to have an influence on the head morphology of N. tessellata (Brecko et al. 2011). Our dietary results of N. tessellata across a broad area in Anatolia indicate a medium level of fish consumption with 72.4% fish prey. The overall high freqeuncy of aquatic prey in the diet of Anatolian N. tessellata confirms that this species in our study area principally forages in water, hunting for fish that it ingests under-water or on land. According to Schaeffel & Mathis (1991), underwater vision is well developed in N. tessellata and superior in comparison to its congener N. natrix, which is specialized on anuran

Table 1. Morphometric data (mean, standard deviation, min.–max.) for Anatolian Natrix tessellata in mm; snout–vent length (SVL) and total length (TL).

Males (n = 15) Females (n = 20) Juveniles (n = 16)

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SVL 478.6 (12.61) 310.0 – 860.0 564.3 (14.07) 288.0 – 850.0 221.0 (3.20) 160.0 – 280.0

TL 599.7 (10.75) 390.0 – 812,0 701.0 (17.30) 370.0 – 1060.0 280.0 (3.65) 220.0– 350.0

Feeding Biology of the Dice Snake in Turkey

Table 2. Food composition of Anatolian Natrix tessellata (n = 51; 15 males, 20 females, 16 juv.). n (%): absolute number of a particular prey taxa; (proportion of that particular prey taxon compared to all prey taxa found); f (%): absolute number of snakes containing a particular prey taxa (proportion of snakes containing a particular prey taxon).

Prey taxa Gastropoda, Pulmonata Lymnaeidae, Lymnaea sp. Planorbidae, Planorbis sp. Insecta Coleoptera Carabidae, Carabus sp. Scarabaeidae Dytiscidae, Dytiscus marginalis Hymenoptera, Formicidae Actinopterygii Cypriniformes Cyprinidae, Cyprinus carpio Cyprinidae, Carassius carassius Cyprinidae, Alburnus sp. Cyprinidae, Leuciscus cephalus Esociformes Esocidae, Esox lucius Amphibia Anura, Ranidae, Pelophylax bedriaga Anura, Bufonidae, Pseudepidalea variabilis juv. Urodela, Salamandridae, Lissotriton vulgaris Reptilia, Lacertidae, Lacerta trilineata Mammalia, Gliridae, Dryomys nitedula

Number of Prey Items (n%) M F J 2 (8.3) 1 (4.2) 1 (4.2) 2 (8.3) 2 (7.7) 2 (7.1) 2 (7.7) 1 (3.8) 2 (9.1) 1 (3.8) 2 (8.3) 17 (70.8) 19 (73.1) 19 (67.9) 12 (50.0) 9 (34.6) 12 (42.9) 1 (4.2) 1 (3.6) 1 (4.2) 3 (11.5) 3 (10.7) 2 (8.3) 3 (11.5) 2 (7.1) 1 (3.6) 1 (3.8) 1 (3.8) 3 (12.5) 1 (3.8) 7 (25.0) 3 (12.5) 1 (3.8) 2 (7.1) 4 (14.3) 1 (3.6) 1 (3.8) 1 (3.8)

diet. An increase in visual acuity underwater thus allows specialization towards fish prey in N. tessellata. Compared with other reptiles, N. tessellata is relatively more specialized with respect to feeding habits (Toft 1985). Although 14.4% of the food content of N. tessellata consisted of terrestrial prey and included insects, reptiles and mammals, they represent animal species that also inhabit the shore zone of water bodies. We suggest that N. tessellata consumed such prey during their foraging activity along the shoreline or while moving into or out of the water. Although uncommon, such terrestrial prey has been variably reported by several authors (see review in Gruschwitz et al. 1999). But it cannot be excluded that terrestrial prey migth be consumed passively, either that they were in the stomach of the actual fish or frog prey of N. tessellata, or were picked up while floating accidentially on the water suface, as it is imaginable for insects. Here again, depending on the geographic location, such terrestrial and semi-aquatic prey items show different frequencies in the stomach content of N. tessellata. This shows that feeding of the species is not fixed to fish and does exhibit some plasticity for the selection of prey, possibly depending on their availability. The larger size of female N. tessellata has been previously reported from many areas throughout its distribu-

Total n %

Total f %

2 (2.6) 1 (1.3) 1 (1.3) 6 (7.9) 2(2.6) 1 (1.3) 2 (2.6) 1 (1.3) 2 (2.6) 55 (72.4) 38 (43.4) 2 (2.6) 7 (9.2) 7 (9.2) 1 (1.3) 1 (1.3) 1 (1.3) 11 (14.5) 6 (7.9) 4 (5.3) 1 (1.3) 1 (1.3) 1 (1.3)

2 (3.9) 1 (2.0) 1 (2.0) 4 (7.8) 2(3.9) 1 (2.0) 1 (2.0) 1 (2.0) 1 (2.0) 41 (80.4) 21 (41.2) 2 (3.9) 7 (13.7) 5 (9.8) 1 (2.0) 1 (2.0) 1 (2.0) 6 (11.8) 4 (7.8) 1 (2.0) 1 (2.0) 1 (2.0) 1 (2.0)

tion (see review in Gruschwitz et al. 1999, Zimmermann & Fachbach 1996, Luiselli et al. 2007). Sexual dimorphism in body size has been related primarily to fecundity selection, which favors an increase in maternal abdominal volume (Shine 1993). This might be achieved by larger body sizes only, as in Palearctic taxa of Natricinae including N. tessellata (Mebert 1993, Gru­ schwitz et al. 1999), or an increase in body size and the number of ventral scales as in the genus Nerodia, American Natricinae related to N. tessellata (Mebert 2010). It is a common trait in aquatic and semi-aquatic snakes that females have also a larger head than males by equal SVL (Shine 1986) but in particular also for Natricinae (Gregory 2004) such as N. tessellata (Mebert 1993). The cephalic sexual-dimorphism may work in concert with a general larger body size of females to promote a different prey spectrum and ecological niche for each gender, in particular to gain extra energy to allocate to the growth of embryos (Shine 1991, 1993 or to restore energy after oviposition (Luiselli & Rugiero 2005). Luiselli et al. (2007) suggested that since females are larger, they also have a wider food spectrum, as their larger jaws allow ingesting larger prey. Their conclusion was supported by sexual dietary differences they found in Italian N. tessellata with an increased data set (Luiselli 2007), after the same group of authors did not de-

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Table 3. Values of Pianka’s overlap index on food composition (prey taxa) between sexes.

Males Females Juveniles

Males 0.986 0.975

Females 0.986 0.954

Juveniles 0.975 0.954 -

tect such differences previously with a smaller sample from the same study site (see Filippi et al. 1996). Although, our results for populations from Anatolia indicate a strong similarity in prey taxa between males and females (Tab. 3), they corroborate the Italian findings. The females also showed a tendency to consume larger prey than males, in particular as the three largest food contents (a fish, a lizard, and a mouse) were all found in stomachs of female snakes. With this in mind and the relatively small sample size (n = 51) in our study compared to the Italian study (n = 2255), we can not decline the possibility of sex-dependent prey differences, in size or type. Several authors have previously reported differences in feeding habits between adult and juvenile snakes, with adults typically displaying a broader food spectrum, e.g. for natricine snakes in Afronatrix anoscopus (Luiselli et al. 2003), or Natrix natrix (Luiselli & Rugiero 1991). In contrast, juveniles of Natrix maura (Santos & Llorente 1998) and Nerodia rhombifer (Plummer & Goy 1984, Gibbons & Dorcas 2004) showed a broader food spectrum. While our results are statistically not significant, they resemble more the results from the Italian studies led by L. Luiselli (see above) in that the food niche breadths of adults (Shannon’s index: males = 0.872, females = 0.838) are slightly broader than that of juveniles (0.798). However, Table 3 shows that the food type composition was largely similar among the snake groups. But we can not preclude that this is an articfact of the relatively small sample size in our study (n with prey = 51) N. tessellata inhabits wetlands that are widespread throughout Turkey (Baran & Atatür 1998, Budak & Göçmen 2008). For example, Demirsoy (1997) reported that N. tessellata is quite abundant in Turkey and suggested that the main factors endangering their survival are habitat degradation and destruction, the drying out of wetlands, pollution, and spreading urbanization. Although consequences of the increasingly prominent effects of global warming for the habitat of N. tessellata are not clear, we suggest the need of establishing sustainable policies in agricultural countries like Turkey as precautionary measurement. Because N. tessellata depends strongly on water, it will face threats by the destruction of wetlands. It is currently not listed in any category of the IUCN Red List of 2008 in Turkey and its status remains unclear. We therefore regard that providing an appropriate conservation status for N. tessellata in Turkey would be an important measure to ensure its future survival. 368

References Bagnoli, C. (1985): Anfibi e Rettili della Provincia di Roma. – Provincia di Roma, Ass. Sanita e Ambiente, WWF Lazio, Italy. Baran, I. & M.K. Atatür (1998): Turkish Herpetofauna (Amphibians & Reptiles). – Ministry of Environment, Ankara, Turkey. Brecko, J., Vervust, B., Herrel, A. & R. van Damme (2011): The relationships between head morphology and diet in the dice snake (Natrix tessellata). – Mertensiella 18: 20–29. Bruno, S. & S. Maugeri (1990): Serpenti d’ Italia e d’ Europa. – Editoriale Giorgio Mondadori, Milano, Italy. Budak, A. & B. Göçmen (2008): Herpetoloji. –Fen Fakültesi Kitaplar Serisi, 194, Ege Üniversitesi Basımevi, Bornova, İzmir, E. Ü. Capula, M. & L. Luiselli (2002): Feeding strategies of Elaphe longissima from contrasting Mediterranean habitats in central Italy. – Ital. J. Zool. 69: 153–156. Darevskij, I.S. & P.V. Terentev (1967): Estimation of energy flow through amphibian and reptile populations. – Proceedings of Working Meeting Jablonna 1966, Institute of Ecology, Polish Academy of Sciences: 181–197 (in Russian). Demirsoy, A. (1997): Türkiye Sürüngenleri. – Monografi, Meteksan Yayınları, Meteksan Baskı Tesisleri, Ankara, Turkey. Esterbauer, H. (1985): Zur Herpetofauna Südwestsyriens. – Herpetofauna 7: 23–34. Esterbauer, H. (1994): Lebensweise und Verhalten der Würfelnatter im Masil al Fawwar (Syrien). – DATZ 47: 308–311. Filippi, E., Capula, M., Luiselli, L. & U. Agrimi (1996): The prey spectrum of Natrix natrix (Linnaeus, 1758) and Natrix tessellata (Laurenti, 1768) in sympatric populations. – Herpetozoa 8: 155–164. Filippi, E., Rugiero, L., Capula, M., Capizzi, D. & L. Luiselli (2005): Comparative food habits and body size of five populations of Elaphe quatuorlineata: The effects of habitat variation, and the consequences of intersexual body size dimorphism on diet divergence. – Copeia 2005: 517–525. Franzen, M., Bussmann, M., Kordges, T. & B. Thiesmeier (2008): Die Amphibien und Reptilien der Südwest-Türkei. – Lauernti Verlag, Bielefeld, Germany. Gibbons, J.W. & M.E. Dorcas (2004): North American Watersnakes. – University of Oklahoma Press, Norman, Oklahoma, USA. Gotelli, N.J. & G.L. Entsminger (2009): EcoSim: Null Model Software for Ecology. – Version 7. Acquired Intelligence Inc. & Kesey-Bear. Jericho, VT 05465. Available at http://garyentsminger.com/ecosim.htm. Gregory, P.T. (2004): Sexual dimorphism and allometric size variation in a population of grass snakes (Natrix natrix) in southern England. – Journal of Herpetology 38: 231–240. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Hecht, G. (1930): Systematik, Ausbreitungsgeschichte und Ökologie der Europäischen Arten der Gattung Tropidonotus (Kuhl) H. Boie. – Mit­t. Zool. Mus. Berlin, 16: 244–393. Laňka, V. (1978): Variabilität und Biologie der Würfelnatter (Natrix tessellata). – Acta Universitatis Carolinae, Biologica 1975– 1976: 167–207. Lenz, S. & M. Gruschwitz (1993): Zur Autökologie der Würfelnatter, Natrix t. tessellata (Laurenti, 1768) (Reptilia: Serpentes: Colubridae) in Deutschland. – Mertensiella 3: 235–252.

Feeding Biology of the Dice Snake in Turkey Luiselli L., Capizzi D., Filippi E., Anibaldi C., Rugiero L. & M. Capula (2007): Comperative diets of three populations of an aquatic snake (Natrix tessellata, Colubridae) from different Mediterranean streams with different hydric regimes. – Copeia 2007(2): 426–435. Luiselli, L & L. Rugiero (1991): Food niche partitioning by water snakes (genus Natrix) at a freshwater environment in central Italy. – Journal of Freshwater Ecology. 6(4): 439–444. Luiselli, L & L. Rugiero (2005): Individual reproductive success and clutch size of a population of the semi-aquatic snake Natrix tessellata from central Italy: Are smaller males and larger females advantaged? – Revue d’Ecologie (Terre et Vie) 60: 77–81. Luiselli, L. (2006): Broad geographic, taxonomic and ecological patterns of interpopulation variation in the dietary habits of snakes. – Web Ecology 6:2–16. Luiselli, L. & U. Agrimi (1991): Composition and variation of the diet of Vipera aspis francisciredi in relation to age and reproductive stage. – Amphibia-Reptilia 12: 137–144. Luiselli, L., Filippi, E. & M. Capula (2005): Geographic variation in diet composition of the grass snake (Natrix natrix) along the mainland and an island of Italy: The effects of habitat type and interference with potential competitors. – Herpetological Journal 15: 221–230. Luiselli, L., Akani, G.C., Angelici, F.M., Politano, E., Ude, L. & S.M. Wariboko (2003): Diet of the semi-aquatic snake, Afronatrix anoscopus (Colubridae) in southern Nigeria. – African Journal of Herpetology 52: 123–126. Mebert, K. (1993): Untersuchungen zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Lauernti, 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Mebert, K. (2010): Massive Hybridization and Species Concepts, Insights from Watersnakes. – VDM Verlag, Germany. Nikolskij, A.M. (1916): Fauna of Russia and adjacent countries, Vol. II, Ophidia. – Israel Program for Scientific Translations, Jerusalem 1964. Pianka, E.R. (1973): The structure of lizard communities. – Ann. Rev. Ecol. Syst. 4: 53–74. Pleguezuelos, J.M. & S. Fahd (2004): Body size, diet, and reproductive ecology of Coluber hippocrepis in the Rif (Northern Morocco). – Amphibia-Reptilia 25: 287–301. Pleguezuelos, J.M. & M. Moreno (1990): Alimentación de Coluber hippocrepis en el SE de la peninsula Iberica. – AmphibiaReptilia 11: 325–337. Plummer, M.V. & J.M. Goy (1984): Ontogenetic dietary shift of water snakes (Nerodia rhombifera) in a fish hatchery. – Copeia 1984: 550–552. Santos, X. & G.A. Llorente (1998): Sexual and size-related differences in the diet of the snake Natrix maura from the Ebro Delta, Spain. – Herpetological Journal 8: 161–165. Santos, X., Llorente, G.A., Feriche, M., Pleguezuelos, J.M., Casals, F. & A. de Sostoa (2005): Food availability induces geographic variation in reproductive timing of an aquatic oviparous snake (Natrix maura). – Amphibia-Reptilia 26: 183–191.

Shine, R. 1986. Sexual differences in morphology and niche utilization in an aquatic snake, Acrochordus arafurae. – Oecologia 69: 260–267. Shine, R. (1991): Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. – American Naturalist 138: 103–122. Shine, R. (1993): Sexual dimorphism in snakes. – In: Seigel. R.A. & J.T. Collins (Eds.): Snakes: Ecology and Behaviour. – McGraw-Hill, New York, USA: 49–86. Schaeffel, F. & U. Mathis (1991): Underwater vision in semiaquatic European snakes. – Naturwissenschaften 78: 373–375. Schultz, K.D. (1996): A Monograph of the Colubrid Snakes of the Genus Elaphe Fitzinger. – Koeltz Scientific Books, Wurselen, Germany. Shannon, C.E. (1948): A mathematical theory of communication. – B ­ ell System Technical Journal 27: 379–423. Toft, C.A. (1985): Resource partitioning in amphibians and reptiles. – Copeia 1985: 1–20. Trobisch-glässer & Trobisch (2001): Ein Mauerblümchen in der Terraristik: Die Würfelnatter Natrix tessellata (Laurenti, 1768). – Elaphe 9(4): 17–24. Zimmermann P. & G. Fachbach (1996): Verbreitung und Biologie der Würfelnatter, Natrix tessellata tessellata (Laurenti, 1768), in der Steiermark (Österreich). – Herpetozoa 8(3/4): 99–124.

Appendix Specimens examined ZDEU. 20/1957, 1 female, 1 juvenile, Lake Nazik (Van); ZDEU. 78/1964, 1 juvenile, Burdur; ZDEU. 103/1965, 1 male, Kargıca Village, Silifke (Mersin); ZDEU. 98/1965, 1 male, Kadirli (Adana); ZDEU. 59/1967, 1 juvenile, Kozan (Adana); ZDEU. 129/1968, 1 juvenile, Karamürsel Airport (Kocaeli); ZDEU. 65/1968, 6 males, 3 females, 8 juv, Lake Apolyont (Bursa); ZDEU. 162/1969, 1 juvenile, Viranşehir (Şanlıurfa); ZDEU. 191/1969, 1 juvenile, Bitlis; ZDEU. 223/1969, 1 male, Çiftekayalar Village, Pınarbaşı (İzmir); ZDEU. 25/1971, 1 juvenile, Kemalpaşa creek (İzmir); ZDEU. 136/1996, 1 male, Aydınlı Village, Ereğli (Konya); ZDEU. 141/1996, 1 female, Yeniyıldız Village, Ulukışla (Niğde); ZDEU. 19/2003, 1 male, 1 female, Lake Eber (Afyonkarahisar); ZDEU. 21/2003, 2 females, Lake Karamık (Afyonkarahisar); ZDEU. 27/2003, 2 females, Lake Karamık (Afyonkarahisar); ZDEU. 23/2003, 2 females, 1 juvenile, Lake Akşehir (Afyonkarahisar); ZDEU. 27/2003, 2 females, Lake Akşehir (Afyonkarahisar); ZDEU. 24/2004, 1 male, Lake Karamık (Afyonkarahisar); ZDEU. 264/2005, 3 females, 2 females, Lake Beyşehir (Konya); ZDEU. 00/2008, 1 male, 1 female, Lake Sarıkum (Sinop).

Authors Bayram Göçmen, Kerim Çiçek, Mehmet Kutsay Atatür, Ege University, Faculty of Science, Biology Department, Bornova, Izmir, Turkey, e-mail: [email protected]; Mehmet Zülfü Yildiz, Harran University, Faculty of Arts and Sciences, Biology Department, Osmanbey Campus, Sanliurfa, Turkey; Yunus Emre Dinçaslan, Environmental Protection Agency for Special Areas, 35680 Eskifoça/İzmir, Turkey; Konrad Mebert, Siebeneichenstrassse 31, 5634 Merenschwand, Switzerland.

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ISBN 978-3-9812565-4-3

Morphology and Blood Proteins of Dice Snakes from Western Turkey* Yunus Emre Dinçaslan, Hüseyin Arikan, İsmail Hakki Uğurtaş & Konrad Mebert Abstract. Dice snakes Natrix tessellata from the Lakes Region in southwestern Turkey (Beyşehir, Akşehir-Eber, Karamuk lakes) and from Uluabat Lake, Marmara Region in northwestern Turkey were compared by means of morphology (pholidosis, body measurement ratio, color pattern) and blood-serum proteins that were analyzed by polyacrylamide gel electrophoresis and densitometry methods. Pholidosis (number of preocular and supralabial scales) and color-pattern, as well as electrophoretic figures of blood serum proteins, showed significant differences between the dice snakes from Beyşehir Lake compared to those of other lakes in the region, as well as those from Uluabat Lake. Some thoughts on those differences and its relevance to taxonomic questions are presented. Key words. Ophidia, colubridae, morphology, polyacrylamide gel electrophoresis, south- and northwestern Turkey.

Introduction The dice snake Natrix tessellata (Laurenti, 1768) has a widespread distribution from Germany and Italy in the west to southeast Europe and Egypt in the south, across Russia and Arabian countries to Central Asia such as North Afghanistan (possibly North Pakistan) and West China (Gruschwitz et al. 1999, Sindaco et al. 2000). This species can be found across Turkey up to an altitude of 2500 m in suitable biotopes (Başoğlu & Baran 1980). There are many studies that tried to shed light on the taxonomy and systematic of N. tessellata. Initial taxonomic grouping was based on morphological comparisons, including morphometric characters and ratios, pholidosis and color-pattern (Strauch 1873, Bedriaga 1879, Boettger 1888, Boettger 1890, Schreiber 1912, Venzmer 1919, Werner 1902, Werner 1903, Werner 1919, Hecht 1930, Bodenheimer 1944, Mertens & Wermuth 1960, Fuhn & Vancea 1961, Kramer & Schnurrenberger 1963, Mertens 1969, Baran 1976, Lanka 1978, Lenz & Gruschwitz 1993, Mebert 1993, 1996, and Göçmen & Böhme 2002). Baran (1976) indicated that N. tessellata from Turkey is consistent with the nominate subspecies N. tessellata tessellata. However, only one supposedly morphologically distinct subspecies has been accepted up to the last century (Hecht 1930), with that being questioned as well by Gruschwitz et al. (1999). The first indication of a different Natrix tessellata subspecies living in Turkey originated from Bedriaga’s (1879) assignation of dice snakes caught around Çanakkale, Trabzon, and Valley Fırat as Tropidonotus hydrus (based on Pallas’ 1771 Coluber hydrus with typically 3 preoculars and 4 postoculars), whereby Tropidonotus is the former generic name of Natrix. Although Boettger (1888, 1890), Venzmer (1919) and Werner (1902, 1919) agreed with this idea for Turkish dice

snakes, Dürigen (1897), Schreiber (1912), Hecht (1930), Bodenheimer (1944), and Mebert (2011) reported variably that the arrangements of ocular scales exhibits a more complex geographic variation and that 3 preocular and 4 postouclar scales were also found in samples from other areas of N. tessellata. Therefore, the former authors declared T. hydrus and N. tessellata as synonyms, which was followed by other authors for dice snakes from the same general area (e.g. Mertens 1969, Gruschwitz et al. 1999, Mebert 2011). Other described subspecies of the dice snake from Turkey have been disregarded after additional analyses. For example, Baran (1976) suggested in his review of material collected across Turkey that N. tessellata vosseleri (Werner 1914) from the area between Antalya and Burdur should be accepted as synonymous with the nominate subspecies. Hecht (1930) described N. viperinus from Turkey. But Mertens & Wermuth (1960) declared that the characteristics of N. viperinus actually belonged to N. maura, a closely relates species whose nearest populations are 1000s of km away in northern Italy. Kramer & Schnurrenberger (1963) also shared this idea of those individuals being N. maura, whereas Baran (1976) accepted N. viperinus as a synonym of the nominate species (N. tessellata). Regardless, whether the former ssp. designation originates from, for example, mislabeled and foreign N. maura or whether those Natrix specimens are somewhat aberrant Turkish N. tessellata, there is no clear argument based on morphological data to maintain any other taxonomic unit for Turkey than the nominate form up to this moment. However, genetic investigation indicates that northern and eastern Turkey (southern, central and western areas have not been studied) is inhabited be a different clade of N. tessellata than specimens from the extreme northwestern area of Turkey (Guicking et al. 2009, Guicking & Joger 2011).

* Some data in this manuscript were included in the Ph.D. thesis of Yunus Emre Dinçaslan. ©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Yunus Emre Dinçaslan, Hüseyin Arikan, İsmail Hakki Uğurtaş & Konrad Mebert

Due to the extensive and often clinal variation of morphological characters across the vast range of dice snakes (see Mebert 2011), it may not be sufficient to elaborate the taxonomic and systematic arrangement in this species based on morphological properties alone. In order to fine-scale the morphological variation, test for geographic differences and infer phylogeographic pattern and determine taxonomic affiliations for N. tessellata from western Turkey, dice snakes from populations in the Lakes Region and from the Marmara Region were compared, morphologically and serologically.

Material and Methods A total of 93 dice snakes, Natrix tessellata, were collected from the Lakes Region in southwestern Turkey (Fig. 1): lakes of Beyşehir (15 females, 18 males, 3 juveniles), Akşehir-Eber (10 females, 8 males, 11 juveniles), Eğirdir (none found), Karamuk (6 females, 4 males), and from the Uluabat Lake, Marmara Region in northwestern Turkey (7 females, 10 males, 1 juvenile). Each specimen was photographed before they were fixed with 4% formaldehyde in 70% ethanol, and subsequently preserved in 70% ethanol, as described by Başoğlu & Baran (1980). All samples were deposited at ZDEU, the Museum of the Zoological Department, Aegean University (see Appendix). Snakes from the Akşehir and Eber lakes were combined for this analysis, as these lakes are connected over a short distance by the canal of Taşköprü. Following morphological characters were recorded: preoculars, postoculars, temporal scales, sublabials, supralabials, gular scales, dorsal scales, anal plate, supracaudals, ventrals, and various body proportions. Kruskall-Wallis test was applied to investigate differences in non-parametric characters, such as the pholidosis. Mann-Whitney U tests were performed to investigate specific differences among the lakes. To test for differences in body proportions among populations, males and females were lumped for a subsequent ANOVA. Tukey dispersion test method was selected from Multiple Comparisons options of ANOVA. For the serological investigation, blood was taken from the postorbital sinuses following Maclean et al. (1973) and was centrifuged at 600 g for 5 minutes, and subsequently stored at -20 C before further analysis. Electrophoretic separation of the blood-serum proteins was performed according to Özeti & Atatür (1979) and Davis (1964), using a “Canalco Model 1200” apparatus at room temperature. Gels containing separated proteins were stained with 0.5% Amido Black (Naphtol Blue Black 10-B) stain. Excessive stain was removed passively by 7% acetic acid baths. Qualitative evaluations of the gels were made directly from electropherograms. Densitometry curves of the separations were obtained from Gelman ACD-15 39430 densitometry at 500 nm and photographed. Digital calipers with 0.001 mm precision were used for obtaining biometric parameters. All statistical analyses for comparing the pholidosis, body proportions and ratios were processed using SPSS 10.0, Statistica 5.4 and MS Office Excel programs. Analyses were considered to be significant at the 95% confidence level (p < 0.05). Results and Discussion Morphometric and Pholidotic Analysis

Fig. 1. Collected localities of Natrix tessellata. 1. Uluabat Lake, 2. Eber Lake, 3. Akşehir Lake, 4. Karamuk Lake, 5. Eğirdir Lake, 6. Beyşehir Lake.

Mean, standard deviation, and range of pholidosis of the dice snake, Natrix tessellata, from western Turkey are presented in Table 1. Three preocular scales are most common (61.3%), followed by 2 preoculars (35.4%) and

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Morphology and Blood Proteins of Dice Snakes from Western Turkey

Tab. 1. Pholidosis values of dice snakes from lakes Uluabat, Eber, Akşehir, Karamuk, and Beyşehir, western Turkey. Beyşehir Lake Characters Preoculars Postoculars Temporals Sublabials Supralabials Gulars Dorsal scales Anal scale Subcaudals Ventral Beyşehir Lake Characters Preoculars Postoculars Temporals Sublabials Spralabials Gulars Dorsal scales Anal scale Subcaudals Ventrals Akşehir–Eber L. Characters Preoculars Postoculars Temporale Sublabials Supralabials Gulars Dorsal scales Anal scales Subcaudals Ventrals Akşehir–Eber L. Characters Preoculars Postoculars Temporals Sublabials Supralabials Gulars Dorsal scales Anal scales Supracaudals Ventrals

372

Females n Ext. 15 2–3 15 3–4 15 3–3 15 9–10 15 8–9 15 3–6 15 19–19 15 2–2 15 60–72 15 161–182 JUV n Ext. 3 3–3 3 4–4 3 3–3 3 9–9 3 7–8 3 4–4 3 19–19 3 2–2 3 58–67 3 175–179 Females n Ext. 10 1–3 10 3–4 10 3–4 10 9–10 10 7–8 10 3–6 10 19–19 10 2–2 10 53–72 10 168–185 JUV n Ext. 11 2–3 11 3–4 11 3–4 11 9–9 11 7–8 11 4–6 11 19–19 11 2–2 11 60–72 11 171–182

M ± SE 2.87 ± 0.12 3.93 ± 0.12 3.00 ± 0.00 9.67 ± 0.13 8027 ± 0.12 4.00 ± 0.29 19.00 ± 0.00 2.00 ± 0.00 64.73 ± 1.00 174.60 ± 1.76

SD 0.35 0.26 0.00 0.49 0.46 1.13 0.00 0.00 3.88 6.82

M ± SE 3.00 ± 0.00 4.00 ± 0.00 3.00 ± 0.00 9.00 ± 0.00 7.67 ± 0.33 4.00 ± 0.00 19.00 ± 0.00 2.00 ± 0.00 61.67 ± 2.73 176.67 ± 1.20

SD 0.00 0.00 0.00 0.00 0.58 0.00 0.00 0.00 4.73 2.08

M ± SE 2.40 ± 0.27 3.60 ± 0.16 3.50 ± 0.17 9.30 ± 0.15 7.70 ± 0.15 4.80 ± 0.33 19.00 ± 0.00 2.00 ± 0.00 62.00 ± 1.71 174.80 ± 1.76

SD 0.84 0.52 0.53 0.48 0.48 1.03 0.00 0.00 5.40 5.57

M ± SE 2.73 ± 0.14 3.85 ± 0.10 3.09 ± 0.09 9.00 ± 0.00 7.82 ± 0.12 5.45 ± 0.28 19.00 ± 0.00 2.00 ± 0.00 66.55 ± 1.18 176.64 ± 0.96

SD 0.47 0.34 0.30 0.00 0.40 0.93 0.00 0.00 3.91 3.17

Males n Ext. M ± SE 18 2–3 2.89 ± 0.14 18 3–4 3.89 ± 0.14 18 3–4 3.06 ± 0.12 18 9–10 9.67 ± 0.11 18 7–9 8.06 ± 0.15 18 3–6 4.50 ± 0.32 18 19–19 19.00 ± 0.00 18 2–2 2.00 ± 0.00 18 56–72 64.50 ± 1.11 18 167–185 175.78 ± 1.16 JUV + both sexes n Ext. M ± SE 36 2–3 2.89 ± 0.15 36 3–4 3.92 ± 0.14 36 3–4 3.03 ± 0.12 36 9–10 9.61 ± 0.18 36 7–9 8.11 ± 0.19 36 3–6 4.25 ± 0.20 36 19–19 19.00 ± 0.00 36 2–2 2.00 ± 0.00 36 56–72 64.36 ± 0.72 36 161–185 175.36 ± 0.93 Males n Ext. M ± SE 8 1–3 2.63 ± 0.26 8 3–4 3.63 ± 0.18 8 3–4 3.25 ± 0.16 8 9–10 9.13 ± 0.12 8 7–8 7.25 ± 0.16 8 4–6 4.63 ± 0.32 8 19–19 19.00 ± 0.00 8 2–2 2.00 ± 0.00 8 59–74 67.00 ± 1.93 8 168–179 174.88 ± 1.16 JUV + both sexes n Ext. M ± SE 29 1–3 2.59 ± 0.13 29 3–4 3.70 ± 0.08 29 3–4 3.28 ± 0.08 29 9–10 9.14 ± 0.07 29 7–8 7.62 ± 0.09 29 3–6 5.00 ± 0.19 29 19–19 19.00 ± 0.00 29 2–2 2.00 ± 0.00 29 53–74 65.10 ± 0.97 29 168–185 175.52 ± 0.77

SD 0.32 0.32 0.24 0.49 0.64 1,34 0.00 0.00 4.72 4.91 SD 0.32 0.28 0.17 0.49 0.57 1.20 0.00 0.00 4.34 5.57 SD 0.74 0.52 0.46 0.35 0.46 0.92 0.00 0.00 5.45 3.27 SD 0.68 0.46 0.45 0.35 0.49 1.00 0.00 0.00 5.25 4.13

Yunus Emre Dinçaslan, Hüseyin Arikan, İsmail Hakki Uğurtaş & Konrad Mebert

Tab. 1. (continued) Karamuk Lake Characters Preoculars Postoculars Temporals Sublabials Supralabials Gulars Dorsal scales Anal scales Subcaudals Ventrals Karamuk Lake Characters Preoculars Postoculars Temporals Sublabials Supralabials Gulars Dorsal scales Anal scales Subcaudals Ventrals

Females n Ext. 6 2–3 6 3–4 6 3–4 6 9–10 6 7–8 6 4–6 6 19–19 6 2–2 6 56–65 6 166–174 JUV n Ext. – – – – – – – – – – – – – – – – – – – –

Uluabat Lake Characters Preoculars Postoculars Temporals Sublabials Supralabials Gulars Dorsal scales Anal scales Subcaudals Ventrals Uluabat Lake Characters Preoculars Postoculars Temporals Sublabials Supralabials Gulars Dorsal scales Anal scales Subcaudals Ventrals

Females n Ext. 7 2–3 7 3–5 7 3–3 7 9–10 7 8–9 7 3–5 7 19–19 7 2–2 7 64–79 7 170–178 JUV n Ext. 1 3 1 4 1 3 1 10 1 8 1 3 1 19 1 2 1 64 1 174

M ± SE 2.50 ± 0.22 3.67 ± 0.21 3.67 ± 0.21 9.33 ± 0.21 7.33 ± 0.21 5.50 ± 0.34 19.00 ± 0.00 2.00 ± 0.00 58.83 ± 1.66 171.00 ± 1.46

SD 0.55 0.52 0.52 0.52 0.52 0.84 0.00 0.00 4.07 3.58

M ± SE – – – – – – – – – –

SD – – – – – – – – – –

M ± SE 2.57 ± 0.20 3.71 ± 0.29 3.00 ± 0.00 9.43 ± 0.20 8.14 ± 0.14 3.57 ± 0.30 19.00 ± 0.00 2.00 ± 0.00 66.33 ± 0.71 173.29 ± 0.99

SD 0.53 0.76 0.00 0.53 0.38 0.79 0.00 0.00 1.75 2.63

M ± SE 3.00 ± 0.00 4.00 ± 0.00 3.00 ± 0.00 10.00 ± 0.00 8.00 ± 0.00 3.00 ± 0.00 19.00 ± 0.00 2.00 ± 0.00 64.00 ± 0.00 174.00 ± 0.00

SD – – – – – – – – – –

Males n Ext. 4 2–2 4 4–4 4 4–4 4 9–10 4 7–8 4 6–6 4 19–19 4 2–2 4 51–57 4 165–175 JUV + both sexes n Ext. 10 2–3 10 3–4 10 3–4 10 9–10 10 7–8 10 4–6 10 19–19 10 2–2 10 51–65 10 165–175

M ± SE 2.00 ± 0.00 4.00 ± 0.00 4.00 ± 0.00 9.75 ± 0.25 7.25 ± 0.25 6.00 ± 0.00 19.00 ± 0.00 2.00 ± 0.00 53.75 ± 1.60 169.00 ± 2.16

SD 0.00 0.00 0.00 0.50 0.50 0.00 0.00 0.00 3.20 4.32

M ± SE 2.30 ± 0.15 3.80 ± 0.13 3.80 ± 0.13 9.50 ± 0.17 7.30 ± 0.15 5.70 ± 0.21 19.00 ± 0.00 2.00 ± 0.00 56.80 ± 1.40 170.20 ± 1.20

SD 0.48 0.42 0.42 0.53 0.48 0.67 0.00 0.00 4.42 3.79

Males n Ext. M ± SE 10 2–3 2.50 ± 0.17 10 3–4 3.80 ± 0.13 10 3–3 3.00 ± 0.00 10 9–10 9.40 ± 0.16 10 8–9 8.10 ± 0.10 10 3–5 3.80 ± 0.25 10 19–19 19.00 ± 0.00 10 2–2 2.00 ± 0.00 10 64–79 68.20 ± 1.31 10 170–186 175.20 ± 1.55 JUV + both sexes n Ext. M ± SE 18 2–3 2.56 ± 0.12 18 3–5 3.78 ± 0.13 18 3–3 3.00 ± 0.00 18 9–10 9.44 ± 0.12 18 8–9 8.11 ± 0.70 18 3–5 3,67 ± 0.18 18 19–19 19.00 ± 0.00 18 2–2 2.00 ± 0.00 18 64–79 67.29 ± 0.84 18 170–186 174.39 ± 0.95

SD 0.53 0.42 0.00 0.52 0.32 0.79 0.00 0.00 4.13 4.92 SD 0.51 0.55 0.00 0.51 0.32 0.77 0.00 0.00 3.48 4.02

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Morphology and Blood Proteins of Dice Snakes from Western Turkey

Tab. 2. Mann-Whitney-U test evaluation of the number of preocular scales that showed significant differences among populations according to the result of Kruskall-Wallis analysis. U: Mann-Whitney-U value, W: Kruskall-Wallis value, P: significance level.

Populations Beyşehir-Akşehir Beyşehir-Karamuk Beyşehir-Uluabat

U 412.000 74.000 216.000

Preocular scales W P 847.000 0.037 129.000 0.000 387.000 0.000

3 specimens from Akşehir with only 1 preocular (3.2%). Specimens with 4 preoculars, reported by Mebert (1993) from the lakes Brienz and Geneva in Switzerland, were encountered neither in this study nor by Baran (1976) from other parts of Turkey. The mean value of preocular and supralabial scales were found to significantly differ among the populations studied here (p < 0.05). The preoculars of dice snakes from Beyşehir had a slight but significantly higher mean than those of dice snakes from Akşehir, Karamuk, and Uluabat (Tab. 2). This is due to a higher proportion of specimens with 3 preoculars in the Beyşehir population than in the other ones. But the general trend of exhibiting rather 3 than 2 preoculars confirms the general pattern for dice snakes from south of a geographic line between the Hungarian Plains to the Dalmatian Coast of Croatia and east of the Carpathian Mountains (see refs. in Gruschwitz et al. 1999) and was found in other areas in Turkey (Black Seas coast and northeastern Turkey; Mebert 1993, Mebert 2011). But Mebert (1993, 1996) showed, that even in some western European populations of dice snakes, a preponderance of 3 versus 2 precoulars can exist, hence, rendering this character less suitable for large, regional separation of dice snakes. Postocular scales are 5 in 4 specimens (4.3%), 4 in 68 specimens (73.12%) and 3 in 21 specimens, which is in accordance with the general findings summarized in Gruschwitz et al. (1999) and Mebert (1993). Findings of Baran (1976) were in accordance with the findings of Başoğlu & Baran (1980) and Baran & Atatür (1988). Specimens with only 2 postoculars, as mentioned by Lanka (1978), Lenz & Gruschwitz (1993), and Mebert (1993) for many specimens from the Czech Republic, Germany, and Switzerland respectively, were not encountered in this study, but do occur at a low frequency in Turkey (Mebert 1993, 2011). The supralabial scales in all the populations were predominantly 8 in 65 specimens (69.9%), 7 in 22 specimens (23.7%), and 9 in 6 specimens (6.6%) in accordance with current literature. The number of temporal, supralabial, sublabial and gular scales were also consistent with the current literature (Baran 1976, Başoğlu & Baran 1980, Baran & Atatür 1988, Mebert 1993). The mean of supralabials showed significant differences between the Beyşehir-Akşehir and Beyşehir-Karamuk populations (Tab. 3).

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Tab. 3. Mann-Whitney-U test evaluation of the number supralabial scales with significant differences among populations based on a Kruskall-Wallis analysis (see Tab. 2 for column discriptors).

Populations Beyşehir-Akşehir Beyşehir-Karamuk Beyşehir-Uluabat

U 310.000 62.000 320.000

Supralabial scales W P 745.000 0.001 117.000 0.000 491.000 0.924

The number of ventral scales varies geographically little in our study area (Tab. 1), and is generally higher in males (mean = 175.5) than females (mean = 173) across all populations in this study. The data we have found is tentatively in accordance with the literature, albeit the sexualdimorphic difference is rather small within and between populations and even reversed for the specimens from Lake Karamuk. For males, Baran (1976) reported a value of 172.4 ventrals as an average across all Turkey. Mebert (1993) reported a mean of 171.4 (n = 7) and 168.0 (n = 6) ventrals for male and female dice snakes from Akşehir. Even though, the sample size for his Aksehir dice snakes is a little lower than in this study, the difference between the sexes was evident. Concerning the situation across all Turkey, Mebert (1993) showed a high geographic variation of ventral counts in Turkey, with mean values of ~175 for males from the Black Sea coast, 178.4 for males from the Northeast Turkey (region between Kars and Van Lake), 173.1 for the Turkish west coast, and 172.0 for southeastern Turkey (region between Urfa and Adiyaman). Comparatively for female dice snakes, Baran (1976) found an average of 168.8 ventrals, whereas 171.2 ventrals were reported for the Black Sea coast, 174.0 for the Northeast Turkey, 167.1 for the Turkish west coast, and 166.5 for southeastern Turkey (Mebert 1993). A constant and average gender difference of 5 scales for the number of ventrals was found across the entire range of N. tessellata (Mebert 1993, Gruschwitz et al. 1999, Mebert 2011), including Turkey (see above). The decreased sexualdimorphic expression of ventrals in our study may partly due to the small sample size in some of the populations investigated herein, and partly may be based on uncertainties of sex determination. Only further investigations could clarify some of the inconsistencies. Similarly, a lack of sexualdimorphic expression was also found for the subcaudal scales with an average value of 65 (range 51 to 79) in males and 66 in females (range 53 to 79). This is inconsistent with Baran (1976), who found an average difference of approximately 10 scales between the gender, with 70 subcaudals for males and 61 for females. Mebert (1993) showed similar ventral mean values for males from Akşehir, 68 (n = 7) vs. 67 (n = 8) in this study, but females showed substantially lower mean values of 56 (n = 5) in Mebert (1993) vs. 62 (n = 10) in this study (see Tab. 1). Mebert (1993) indicated

Females n Ext. 15 1.8–3.6 15 2.58–5.21 15 3.99–7.51 15 2.82–5.14 15 11.63–24.02 15 5.60–10.91 15 321–830 15 50.1–180.7 15 1.29–1,57 15 0.50–0.72 15 0.42–0.57 15 0.15–0.30

Females n Ext. 10 1.76–3.76 10 2.36–5.92 10 3.34–7.38 10 2.41–4.98 10 10.15–22.15 10 4.95–10.56 10 200.20–710.00 10 50.30–160–80 10 1.34–2.02 10 0.57–0.72 10 0.40–0.56 10 0.20–0.29

Beyşehir Lake Characters RH RW FL FW HL HW BL TL RW/RH FW/FL HW/HL TL/BL

Akşehir-Eber Lakes Chars. RH RW FL FW HL HW BL TL RW/RH FW/FL HW/HL TL/BL

M ± SE 2.74 ± 0.21 4.46 ± 0.30 6.10 ± 0.36 3.82 ± 0.23 17.76 ± 1.00 8.61 ± 0.57 557.47 ± 44.17 126.27 ± 10.03 1.65 ± 0.08 0.63 ± 0.02 0.49–0.02 0.23 ± 0.01

M ± SE 2.88 ± 0.16 4.16 ± 0.23 6.16 ± 2.29 3.84 ± 0.17 18.16 ± 1.00 8.59 ± 0.45 585 ± 41.33 136.44 ± 9.62 1.45 ± 0.02 0.63 ± 0.02 0.48 ± 0.01 0.23 ± 0.01

SD 0.66 0.94 1.14 0.73 3.17 1.80 139.68 31.70 0.26 0.06 0.06 0.03

SD 0.63 0.89 1.12 0.66 3.86 1.75 160.09 37.27 0.09 0.06 0.04 0.04

Males n Ext. 8 1.64–3.75 8 2.68–5.31 8 3.77–7.15 8 2.72–5.06 8 11.25–21.82 8 5.31–10.06 8 280.00–690.00 8 70.95–160.00 8 1.34–1.74 8 0.65–0.72 8 0.35–0.52 8 0.14–0.29

Males n Ext. 18 1.9–3.4 18 3.02–5.27 18 4.32–7.18 18 3.07–5.54 18 15.21–22.50 18 7.08–10.36 18 461–710 18 110.20–170.50 18 1.13–2.26 18 0.55–0.86 18 0.43–0.58 18 0.21–0.29

M ± SE 2.52 ± 0.25 3.89 ± 0.37 5.34 ± 0.42 3.63 ± 0.28 17.15 ± 1.41 7.70 ± 0.73 532.81 ± 58.93 116.97 ± 11.33 1.55 ± 0.05 0.68 ± 0.01 0.45 ± 0.02 0.23 ± 0.02

M ± SE 2.66 ± 1.11 4.02 ± 0.13 6.02 ± 0.15 3.93 ± 0.13 18.21 ± 0.51 8.66 ± 0.22 562.58 ± 16.77 142.59 ± 4.77 1.55 ± 0.07 0.65 ± 0.02 0.48 ± 0.01 0.25 ± 0.01

SD 0.72 1.05 1.20 0.78 3.98 2.06 166.67 32.05 0.13 0.03 0.05 0.04

SD 0.46 0.53 0.65 0.54 2.15 0.95 71.15 18.99 0.30 0.07 0.04 0.03

Both sexes n Ext. 18 1.64–3.76 18 2.36–5.92 18 3.34–7.38 18 2.41–5.06 18 10.15–22.15 18 4.95–10.56 18 200.20–710.00 18 50.30–160.80 18 1.34–2.02 18 0.57–0.72 18 0.35–0.56 18 0.14–0.29

Both sexes n Ext. 33 1.8–3,6 33 2.58–5.27 33 3.99–7.51 33 2.82–5.54 33 11.63–24.02 33 5.60–10.91 33 321–830 33 50.1–180.7 33 1.13–2.26 33 0.50–0. 86 33 0.42–0.58 33 0.15–0.30

M ± SE 2.64 ± 0.16 4.20 ± 0.24 5.76 ± 0.28 3.74 ± 0.17 17.49 ± 0.81 8.21 ± 0.45 546.51 ± 34.90 122.14 ± 7.37 1.60 ± 0.05 0.65 ± 0.01 0.47 ± 0.01 0.23 ± 0.01

M ± SE 2.76 ± 0.09 4.08 ± 0.12 6.08 ± 0.35 3.89 ± 0.10 18.19 ± 0.52 8.63 ± 0.23 572.77 ± 20.62 139.80 ± 4.95 1.50 ± 0.04 0.64 ± 0.01 0.48 ± 0.01 0.25 ± 0.01

SD 0.68 1.00 1.19 0.74 3.45 1.92 148.08 31.27 0.21 0.05 0.06 0.04

SD 0.55 0.71 0.88 0.59 3.00 1.35 118.45 28.44 0.23 0.07 0.04 0.03

Tab. 4. Morphometric data and ratios in both sexes of Natrix tessellata from selected populations in western Turkey. RH: Rostral Height, RW: Rostral Width, FL: Frontal Length, FW: Frontal Width, HL: Head Length from the tip of the rosral scale to the posterior end of the parietal scale, HW: Head Width as the greatest transverse distance between the supraocular scales, BL: Body Length (= SVL), TL: Tail Length, RW/RH: Rostral Ratio, FW/FL: Frontal Ratio, HW/HL: Head Ratio, TL/BL: Tail Ratio) (a. Beyşehir Population, b. Akşehir–Eber Population, c. Karamuk Population, d. Uluabat Population).

Yunus Emre Dinçaslan, Hüseyin Arikan, İsmail Hakki Uğurtaş & Konrad Mebert

375

Females n Ext. 6 2.11–3.06 6 3.21–4.76 6 4.37–6.75 6 3.45–3.96 6 12.84–19.55 6 6.14–10.25 6 370.1–640.1 6 90.50–140.20 6 1.34–1.56 6 0.59–0.83 6 0.48–0.53 6 0.19–0.24

Females n Ext. 7 1.88–2.87 7 2.64–4.59 7 4.34–7.59 7 2.68–4.47 7 12.99–20.83 7 6.38–9.92 7 360–730.50 7 100.70–170.20 7 1.33–1.95 7 0.58–0.83 7 0.46–0.50 7 0.10–0.31

Uluabat L. Characters RH RW FL FW HL HW BL TL RW/RH FW/FL HW/HL TL/BL

Characters RH RW FL FW HL HW BL TL RW/RH FW/FL HW/HL TL/BL

Karamuk L.

376

M ± SE 2.32 ± 0.14 3.47 ± 0.25 5.37 ± 0.43 3.41 ± 0.23 15.84 ± 1.07 7.57 ± 0.49 491.70 ± 50.70 127.51 ± 10.39 1.50 ± 0.08 0.64 ± 0.04 0.48 ± 0.01 0.22 ± 0.04

M ± SE 2.76 ± 0.15 3.96 ± 0.23 5.56 ± 0.31 3.62 ± 0.08 17.99 ± 1.08 9.24 ± 0.67 553.37 ± 40.02 120.50 ± 8.49 1.43 ± 0.03 0.66 ± 0.04 0.51 ± 0.01 0.22 ± 0.01

SD 0.36 0.65 1.15 0.62 2.83 1.29 134.35 27.50 0.22 0.09 0.01 0.10

SD 0.38 0.57 0.76 0.20 2.65 1.65 98.03 20.79 0.08 0.09 0.02 0.02

Ext. 3.10–3.40 4.93–6.06 5.94–7.29 3.55–4.26 16.97–21.23 9.72–11.17 620.5–630.0 120.0–130.0 1.47–1.90 0.58–0.60 0.48–0.66 0.19–0.21

Males n Ext. 10 1.34–3.24 10 2.31–4.43 10 4.18–6.06 10 2.61–3.68 10 12.63–18.37 10 6.12–8.84 10 330.50–560 10 80.70–140.20 10 1.26–2.01 10 0.54–0.73 10 0.47–0.53 10 0.24–0.32

Males n 4 4 4 4 4 4 4 4 4 4 4 4

M ± SE 1.97 ± 0.17 2.95 ± 0.19 4.82 ± 0.17 2.97 ± 0.09 14.13 ± 0.56 7.06 ± 0.30 402.32 ± 20.64 106.33 ± 5.56 1.53 ± 0.07 0.62 ± 0.02 0.50 ± 0.01 0.26 ± 0.01

M ± SE 3.25 ± 0.08 5.72 ± 0.26 6.36 ± 0.31 3.74 ± 0.17 19.70 ± 0.94 10.44 ± 0.41 623.2 ± 2.28 122.63 ± 2.46 1.76 ± 0.10 0.59 ± 0.00 0.54 ± 0.04 0.20 ± 0.00

SD 0.53 0.59 0.54 0.30 1.79 0.93 65.28 17.58 0.23 0.05 0.02 0.02

SD 0.15 0.53 0.63 0.35 1.87 0.82 4.55 4.92 0.21 0.01 0.08 0.01

Both sexes n Ext. 17 1.34–3.24 17 2.31–4.59 17 4.18–7.59 17 2.61–4.47 17 12.63–20.83 17 6.12–9.92 17 330.50–730.50 17 8.70–170.20 17 1.26–2.01 17 0.54–0.83 17 0.46–0.53 17 0.10–0.32

Both sexes n Ext. 10 2.11–3.40 10 3.21–6.06 10 4.37–7.29 10 3.45–4.26 10 12.84–21.23 10 6.14–11.17 10 370.1–640.1 10 90.5 – 140.2 10 1.34–1.90 10 0.58–0.83 10 0.48–0.66 10 0.19–0.24

M ± SE 2.11 ± 0.12 3.16 ± 0.16 5.05 ± 0.21 3.15 ± 0.12 14.83 ± 0.57 7.27 ± 0.26 439.12 ± 25,67 115.85 ± 5.81 1.52 ± 0.05 0.63 ± 0.02 0.49 ± 0.00 0.25 ± 0.02

M ± SE 2.96 ± 0.12 4.66 ± 0.33 5.88 ± 0.25 3.67 ± 0.08 18.68 ± 0.76 9.72 ± 0.46 581.30 ± 5.78 121.35 ± 4.99 1.57 ± 0.07 0.63 ± 0.02 0.52 ± 0.02 0.21 ± 0.01

SD 0.49 0.65 0.86 0.49 2.36 1.09 68.16 23.94 0.22 0.07 0.02 0.07

SD 0.39 1.05 0.79 0.26 2.42 1.45 81.52 15.79 0.22 0.08 0.05 0.02

Morphology and Blood Proteins of Dice Snakes from Western Turkey

Yunus Emre Dinçaslan, Hüseyin Arikan, İsmail Hakki Uğurtaş & Konrad Mebert

the extent of geographic variation in subcaudals for dice snakes from Turkey with following mean values from the Black Sea coast (70 for males and ~59 for females), the Northeast of Turkey (70 for males and ~61 for females), and southeastern Turkey (~73 for males, ~58 for females). Similarly, sexually dimorphic mean differences for subcaudals were found in dice snakes from western Europe (Lenz & Gruschwitz 1993, Mebert 1993, Zimmerman & Fachbach 1996), but also eastern Europe (refs. in Mebert 1993, Gruschwitz et al. 1999). Finally, only further research will show, whether sexualdimorphism of ventral and subcaudal scale counts in N. tessellata from western Turkey exhibits a variation comparable to that in other areas of the country. The significance of sexual dimorphism in pholidotic characters is well documented in natricinae and is ubiquitous (e.g. Mebert 2010). No specimens with 17 dorsally arranged scales at mid body (mid point between snout and vent) were encountered in this study and the number of dorsal scale rows in all specimens was 19 rows. Mebert (1993) investigated the scale row reduction pattern in N. tessellata across a wide area. However, he did not take the snake’s body length (SVL) as a reference, but the number of ventrals instead, counting from the head caudad. Yet, the bilat­­­ rows to 17 rows in eral reduction of scale rows from 19 Swiss and Italian dice snakes still occurred posterior the mid point of the ventral scale number (posterior ~52% -56% of the number of ventrals). That means, converting to the traditional mid point measurement using the entire SVL (with the ~3% head length added), the dorsal scale row reduction from 19 to 17 rows in western European dice snakes would occur posterior 55% to 58% body length, respectively 5% to 8% posterior mid body. Only a few (5%) dice snakes from western Europe exhibited a scale row reduction to 17 scale a long stretch before the mid point of the body, thus, resulting in a traditionally applied mid body scale count of 17 rows (Mebert 1993). Compared to western European dice snakes, the scale row reduction to 17 rows in Greek individuals occurs even ~10% and ~7% farther caudad than in individuals from Northeast Turkey (Mebert 1993), hence, it is not surprising that dice snakes from western Turkey yield 19 rather than 17 scale rows at mid body (this study). Measurement and definitions of body proportions and associated ratio values of investigated populations are presented in Table 4. To identify sexual dimorphism of body proportions, an independent t-test was performed on raw data for each population separately with no differences found between the genders. This too is in contrast to results of explicit sexual dimorphic body proportions found in dice snakes from Switzerland and Italy (for ratios for the tail length, head width and length, and frontal shield, see Mebert 1993, 1996). Sexualdimorphic tail length were also found in Germany (Lenz & Gruschwitz 1993), Austria (Zimmermann & Fachbach 1996), as well as western Balkan and Greece (Mebert 1993). A further investigation on sex alloca-

tion could possibly clarify the inconsistent pattern described here. Across all populations averaged, the head ratios (head width/head length) for dice snakes from western Turkey is 0.50, which is higher than the average of 0.43 for measurements taken from all over Turkey (Baran 1976), resulting in relatively wider head for animals in this study. Comparing maximum lengths of body proportions between the populations, the longest absolute rostral height and width in females were measured in the Akşehir population, the largest frontal length in the Uluabat population, but the largest frontal width, head length, head width, body length and tail length in the Beyşehir population; in males however, the largest rostral height was measured in the Akşehir population, whereas the longest frontal width, frontal length and head width were measured in the Karamuk population, and the longest frontal width, head length, body length and tail length were found in the Beyşehir population. Concerning relative values to compensate for different size classes, the heighest rostral ratio (widest relative rostral width) of 1.34 and tail ratio of 0.15 (relative longest tail) was measured on a specimen from the Akşehir population, the heighest frontal ratio of 0.59 (relative widest frontal shield) was found in the Karamuk population, and the heighest head ratio of 0.42 (relative widest head) in the Beyşehir population. The Tukey dispersion test revealed a significant difference concerning head ratios (HW/HL) (p < 0.05) between populations from Beyşehir and Karamuk. Color-Pattern Analysis Two different color-pattern types were identified among the investigated populations. Color-pattern type frequencies distributed among the populations are shown in Table 5. Unicolored specimens (Type B) were particularly common in the Beyşehir population (n = 21, 58.34%) and in the Uluabat population (n = 8, 44.44%), as such local concentrations of this color form were not found in the samples evaluated by Baran (1976) from different locations of Turkey. However, the occurrence of distinct local frequencies of unicolored and also melanistic dice snakes are known from sites in southern Switzerland to China and, as far is known, do not follow a certain geographic pattern (Mebert 1993). However, a higher frequency of melanistic specimens has been noted locally from various populations (see refs. Tab. 5. Color-pattern types and ratios of Natrix tessellata from the inspected populations in western Turkey. LOCALITIES Beyşehir Lake Akşehir–Eber Lake Karamuk Lake Uluabat Lake

A Type 15 (%41.66) 29 (%100) 10 (%100) 10 (%55.56)

B/C Type 21 (%58.34) 0 0 8 (%44.44)

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a

c

a

c

b

d

b

Fig. 2. Color Pattern of Natrix tessellata from western Turkey: Dorsal and ventral view of spotted Type A with (a) from Karamuk Çay, Afyon, and (b) from, Gölkaşı village, Isparta, at the border with Afyon; (c) dorsal and ventral view of Type B from Beyşehir Lake, Isparta; (d) melanistic specimen from Beyşehir Lake, Type C (see Text for Type description).

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in Gruschwitz et al. 1999, Litvinov et al. 2011, Liu et al. 2011, Tuniyev et al. 2011). It was even used to support the former subspecific status of Natrix tessellata heinrothi (Hecht 1930), but this character was refuted due to similar occurrence of melanistic dice snakes in other populations (e.g. Mertens 1969, Gruschwitz et al. 1999). Type A: These are dice snakes with typically black spots dorsally and laterally over an olive green to gray brown background on the neck and dorsum (Figs. 2a, b). While black spots usually form four rows, some specimens yield also whitish spots to vertical lines between the black spots along frontal and lateral sides of the body. In some individuals black spots on the dorsum begin as four rows, fuse to three rows and split into four rows farther caudad or vice versa. The venter is dirty white or yellowish with black spots on the anterior part of the body, which increasingly expand caudad until they form the principal background color. There may be yellowish-white scattered spots over this background. Type B: This is a unicolored, spotless morph (Fig. 2c). The dorsum is gray to olive green. There may be a black stripe bilaterally over the back of the head, which expandes from the neck and fades caudad but sometimes becomes prominent again posteriorly. The venter is pinkish to white in the front with a black stripe that increasingly widens posteriorly up onto the tail, equivalent to Type A.

Fig. 3. Blood-serum protein electropherograms of representative specimens from two different populations of Natrix tessellata. A: Uluabat, B: Beyşehir. The albumins are the bands on the left end, and the globulins are those adjacent to the left.

Fig. 4. Gel photograph and densitometric tracing curve showing the electrophoretic separation of the blood-serum proteins obtained from a Natrix tessellata of Lake Beyşehir, Turkey. OD: Optical density, S: Start (junction between the stacking and separation of gels).

Type C: These are melanistic dice snakes or abundistic specimens (generally darkening skin, albeit not black) as can be seen in Fig. 2d. Electrophoretic Analysis of Blood-Serum Proteins Sexually mature specimens were used for the electrophoretic analysis of blood-serum proteins. Since there were no qualitative differences between genders, males and females were evaluated together. The electrophoretic figures of blood-serum proteins were similar among Akşehir-Eber, Karamuk and Lake Uluabat populations, and they were subsequently lumped together and compared with dice snakes from the Beyşehir population. Gel photographs directly comparing the electrophoretic separations of blood-serum proteins between a dice snake from Beyşehir Lake and one from the Uluabat population, representing the group with specimens from the Akşehir-Eber, Karamuk and Uluabat lakes, are shown in Figure 3. In addition, a gel photograph of blood-serum proteins with densitometry curves is shown for an individual from the Beyşehir population (Fig. 4) and another one from the Uluabat population (Fig. 5). As seen in Figure 3, dice snakes from the Beyşehir population produced rates of fractions in the albumin region that migrated faster than those from snakes from the Uluabat population (and thus equally

Fig. 5. Gel photograph and densitometric tracing curve showing the electrophoretic separation of the blood-serum proteins obtained from a Natrix tessellata of Lake Uluabat, Turkey OD: Optical density, S: Start (junction between the stacking and separation of gels).

for the remaining populations). Qualitatively, there are 12 fractions in the blood-serum protein samples in the specimen from Beyşehir and Uluabat, 2 in the albumin region and 10 in the globulin region. Small differences are visible between the corresponding fractions in the globulin region (Figs. 4 and 5). Quantitatively, in the Beyşehir specimen the density of the albumin fraction

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is 24.62% and the albumin/globulin (A/G) ratio is 0.327. In the specimen from the Uluabat population, these values are 18.31% and 0.224 respectively. Hence, the albumin fractions and A/G ratio in the Beyşehir population are higher than in the Uluabat population. Many researchers dealing with electrophoretic separations of blood-serum proteins of different amphibian and reptile species declared the taxonomic importance of number, speed and density of protein fractions (Dessauer & Fox 1956, Chen 1967, Ferguson 1980, Arikan et al. 1999). Ferguson (1980) suggested that factors such as genetic variation, age, physiological and environmental conditions affect protein structure. He suggested that among these factors, while some genetic variations may cause qualitative differences, others cause quantitative differences. In this study, electrophoretic analysis of blood-serum proteins showed 1) faster movement of fractions within the albumin region in dice snakes from the Beyşehir population, 2) their higher percentage of albumin fractions, and 3) some small differences at the level of corresponding fractions especially in the globulin region, which serves to differentiate this population from the other studied populations. However, it is not clear to which biological functions these differences are associated, or whether the differences may just show geographic variation by chance without any pertinent biological relevance, but yet be a part of a co-adapted gene complex. Natrix tessellata could not be found at Lake Eğirdir despite various field trips. The reason for this might be the introduction of the pikeperch, Sander (Stizostedion) lucioperca, into the lake, beginning in 1955 and reaching a peak in the 1970s (Campbell 1992, Türkiye Çevre Vakfi 1993, İzci & Kuşat 2006, Kesici & Kesici 2006, Bâlik et al. 2007). After the vaccination of the pikeperch, which was ignorantly introduced into the habitat of N. tessellata, a rapid change occurred in the fauna of Eğirdir Lake (Çetinkaya 2006) which resulted in the extinction of the 8 endemic fish species (Campbell 1992, Küçük & İkiz 2004). The new fish species, known to be an invasive predator, became in a short period the dominant species and caused significant changes in the general fishing regime of the lake (Çetinkaya 2006). This change in the general fauna presumably has affected the feeding habits of N. tessellata, either by direct predation on young dice snakes or by competitively consuming on the prey of dice snakes. However, a newer literature record shows that the dice snakes still survived at Eğirdir Lake and also nearby Kovada Lake (Franzen et al. 2008, M. Franzen pers. comm.). In summary, we found that the Beyşehir population was different from the other inspected populations regarding a few properties of pholidosis (number of preocular and supralabial scales), head ratios, color-pattern and electrophoretic pattern of blood-serum proteins. However, it is surprising that dice snakes from the population of Beyşehir Lake is distinct from regionally close (approx. 70 km) populations of the lakes Akşehir-Eber,

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Karamuk, and possibly Eğirdir, which resemble more the far distant (approx. 270 km) dice snakes from Uluabat Lake. Only future research including a larger and wider sampling scheme, a closer look at the landscape situation including topography and water sheds, and a more detailed morphological and molecular analysis may resolve these questions. References Arikan, H., Atatür, M.K., Çevik, I.E. & Y. Kumlutaş (1999): A serological investigation of Lacerta viridis (Laurenti, 1768) (Sauria: Lacertidae) populations in Turkey. – Turkish Journal of Zoology 23: 227–230. Bâlik, İ., Çubuk, H. & R. Özkök (2007): Spatial distributions of economic fish populations in Lake Eğirdir. – Journal of Fisheries Science.com 1(2): 88–96. Baran, I. (1976): Türkiye Yılanlarının Taksonomik Revizyonu ve Coğrafi Dağılışları. – TBTAK Yayınlar, Turkey. Baran, I & M.K. Atatür (1988): Türkiye Herpetofaunası (Kurbağa ve Sürüngenler). – T.C. Çevre Bakanlığı, Turkey. Başoğlu, M. & I. Baran (1980): Türkiye Sürüngenleri, Kısım II Yılanlar. – Ege Üniversitesi Yayınları. Bedriaga, J. (1879): Verzeichnis der Reptilien und Amphibien Vorder-Asiens. – Bulletin Soc. Nat. Moscow 74(3): 453–568. Bodenheimer, F.S. (1944): Introduction into the knowledge of the Amphibia and Reptilia of Turkey. – Rev. Faculty Science, University of Istanbul Series, Turkey. Boettger, O. (1888): Verzeichnis der von Hrn. E. von Oertzen aus Griechenland und aus Kleinasien mitgebrachten Batrachier und Reptilen. – Sitzungsberichte der Königlich Preussischen Akademie der Wissenschaften zu Berlin 5: 139–186. Boettger, O. (1890): Batrachier und Reptilen aus Kleinasien. – Bericht der Senckenbergischen Naturforschenden Gesellschaft in Frankfurt am Main: 293–295. Campbell, R.N.B. (1992): Food of an introduced population of pike-perch, Stizostedion lucioperca L., in Lake Eğirdir, Turkey. – Aquaculture and Fisheries Management 23: 71–85. Çetinkaya, O. (2006): Türkiye sularına aşılanan veya stoklanan egzotik ve yerli balık türleri, bunların yetiştiricilik, balıkçılık, doğal populasyonlar ve sucul ekosistemler üzerindeki etkileri: Veri tabanı için bir ön çalışma. – I. Balıklandırma Ve Rezervuar Yonetimi Sempozyumu, Antalya, Turkey: 7–9. Chen, P.S. (1967): Separation of serum proteins in different amphibian species by polyacrylamide gel electrophoresis. – Experientia 23: 483–485. Davis, B.J. (1964): Disc electrophoresis-II. Method and application to human serum proteins. – Ann. N. Y. Acad. Sci. 121: 404–427. Dessauer, H.C. & W. Fox (1956): Characteristic electrophoretic patterns of orders of amphibia and reptilia. – Science 124: 225–226. Dürigen, B. (1897): Deutschlands Amphibien und Reptilien. – Madgeburg, Germany. Ferguson, A. (1980): Biochemical Systematics and Evolution. – Blackie and Son, Glasgow and London. Franzen, M., Bussmann, M., Kordges, T. & B. Thiesmeier (1980): Die Amphibien und Reptilien der Südwest-Türkei. – Laurenti Verlag, Bielefeld, Germany. Fuhn, I.E. & S. Vancea (1961): Fauna Republici Romine. – Fauna Romine Bucurest, Romania 14(2).

Yunus Emre Dinçaslan, Hüseyin Arikan, İsmail Hakki Uğurtaş & Konrad Mebert Göçmen, B. & W. Böhme (2002): New evidence of the occurence of the dice snake, Natrix tessellata (Laurenti, 1768) on Cyprus. – Zoology in the Midle East 27: 29–34. Gruschwitz, M., Lenz, S., Mebert, K. & V. Lanka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA Verlag,Wiesbaden, Germany: 581–644. Guicking, D., Joger, U. & M. Wink (2009): Cryptic diversity in a Eurasian water snake (Natrix tessellata): Evidence from mitochondrial sequence data and nuclear ISSR-PCR fingerprinting. – Organisms, Diversity and Evolution 9(3): 201–214. Guicking, D. & U. Joger (2011): A range-wide molecular phylogeography of Natrix tessellata. – Mertensiella 18: 1–10. Hecht, G. (1930): Systematik, Ausbreitungsgeschichte und Ökologie der europaeischen Arten der Gattung Tropidonotus (Kuhl). H. Boie. – Mitt. Zool. Mus. Berlin 16: 244–393. İzci, L.& M. Kuşat (2006): Some population parameters of pikeperch (Sander lucioperca (L., 1758)) in Lake Eğirdir. – SDU, Fen Bilim. Enst. Derg. 10–2: 167–172. Kesici, E. & C. Kesici (2006): The effects of interferences in the natural structure of Lake Egirdir (Isparta) to the ecological disposition of the Lake. EU. – Journal of Fisheres & Aquatic Sciences 23(1/1): 99–103. Kramer, E. & H. Schnurrenberger (1963): Systematik, Verbreitung und Ökologie der Lybischen Schlangen. – Revue Suisse Zool. Genf. 70: 453–568. Küçük, F. & R. İkiz (2004): Antalya Körfezi’ne dökülen akarsuların balık faunası. EU. – Journal of Fisheres & Aquatic Sciences 21(3/4): 287–294. Lanka, V. (1978): Variabilitat und Biologie der Würfelnatter (Natrix tessellata). – Acta Universitatis Carolinae Biologica 1975– 1976: 167–207. Lenz, S. & M. Gruschwitz (1993): Zur Merkmalsdifferenzierung und –variation der Würfelnatter, Natrix tessellata (Laurenti 1768) in Deutschland. – Mertensiella 3: 269–300. Litvinov, N., Bakiev, A. & K. Mebert (2011): Thermobiology and microclimatic of the dice snake at its northern range limit in Russia. – Mertensiella 18: 330–336. Liu, Y., Mebert, K. & L. Shi (2011): Notes on Distribution and Morphology of the dice Snake (Natrix tessellata) in China. – Mertensiella 18: 430–436. Maclean, G.S., Lee, A.K. & K. J. Wilson (1973): A simple method of obtaining blood from lizards. – Copeia 2: 338–339. Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland.

Mebert, K. (1996): Comparaison morphologique entre des populations introduites et indigenes de Natrix tessellata de I’Arc Alpin. – Bull. Soc. Herp. France 80: 15–25. Mebert, K. (2010): Massive Hybridization and Species Concepts, Insights from Watersnakes. – VDM Verlag, Saarbrücken, Germany. Mebert, K. (2011): Geographic variation of morphological characters in the dice snake Natrix tessellata (Laurenti 1768). – Mertensiella 18: 11–19. Mertens, R. (1969): Zur Synonymie und Variabilitat der Würfelnatter (Natrix tessellata). – Senckenbergiana Biologica Band 50(3/4): 125–131. Mertens, R. & H. Wermuth (1960): Die Amphibien und Reptilien Europas (Dritte Liste nach dem Stand vom 1. Januar 1960). – Verlag Waldemar Kramer, Frankfurt am Main, Germany. Özeti, N. & M.K. Atatür (1979): A preliminary survey of the serum-proteins of a population of Mertensiella luschani finikensis Başoğlu & Atatür from Finike in Southwestern Anatolia. – İstanbul Üniversitesi Fen Fakültesi Mecmuası 44(B): 23–29. Pallas, P.S. (1771): Reise durch verschiedene Provinzen des Russischen Reiches I. – Peterburg, Russia. Schreiber, E. (1912): Herpetologia europaea (2. Auflage). – Fischer, Jena, Germany. Sindaco, R., Venchi, A., Carpaneto, G.M. & M. Bologno (2000): The reptiles of Anatolia: a checklist and zoogeographical analysis. – Biogeographia 21: 441–554. Strauch, A. (1873): Die Schlangen des Russischen Reiches. – Memories de’ Academie Imperiale des Sciences de St.-Petersbourg, VII serie, Tome XXI (4). Tuniyev, B., Tuniyev, S., Kirschey, T. & K. Mebert (2011): Notes on the dice snake, Natrix tessellata, from the Caucasian Isthmus. – Mertensiella 18: 343–356. Türkiye Çevre Vakfi (1993): Türkiye’nin Sulak Alanları. – TÇV Yayınları, Önder Matbaa. Venzmer, G. (1919): Zur Schlangenfauna Süd-Kleinasiens, speziell des cilicischen Tauris. – Archiv für Naturgeschichte 83(A)(II): 95–122. Werner, F. (1902): Die Reptilien-und Amphibienfauna von Kleinasien. – SB. Akad. Wiss. Wien, Math.-Naturw. KI. I, III: 1057–1121. Werner, F. (1903): Über Reptilien und Batrachier aus Westasien (Anatolien und Persien). – Zool. Jb. Syst. 19: 329–346. Werner, F. (1919): Reptilien und Amphibien aus dem AmanusGebirge. – Archiv für Naturgeschichte 85(A)(8): 130–141. Zimmermann P. & G. Fachbach (1996): Verbreitung und Biologie der Würfelnatter, Natrix tessellata tessellata (Laurenti, 1768), in der Steiermark (Österreich). – Herpetozoa 8(3/4): 99–124.

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Appendix Specimens (n = 93): The data are given as follows: collections code and number, number and sex (m./f.) of specimens, locality, date of collection and name of collector: ZDEU.65/1968. 1–4 m., 5–6 f., Uluabat Lake, Bursa, 12.05.1968, leg. Z. Eren, ZDEU. 55/1976. 1–2 m., Beyşehir Lake, Konya, 23.04.1976, leg. M. Başoğlu, S. Sezer, ZDEU. 18/1987. 1–1 m., 2–10 juv., Akşehir Lake,Afyon, 07.06.1987, leg. F. Atagün, ZDEU. 48/1988. 1–2 m., 3–3 f., 4–6 juv., Beyşehir Lake, Konya, 06.06.1988, leg. F. Atagün, ZDEU. 19/2003. 1–3 m., 4–7 f., Eber Lake, Afyon, 02.07.2003, leg. Y.E. Dinçaslan, D. Ayaz, ZDEU.

21/2003. 1–2 m., 3–4 f., Karamuk Lake, Çay, Afyon, 30.06.2003, leg. Y. E. Dinçaslan, ZDEU. 23/2003. 1–4 m., 5–10 f., 11–12 juv., Akşehir Lake, Afyon, 03.07.2003, leg. Y. E. Dinçaslan, D. Ayaz, ZDEU. 26/2003. 1–6 m., 7–8 f., Beyşehir Lake, Konya, 04.07.2003, leg. Y. E. Dinçaslan, D. Ayaz, ZDEU. 27/2003. 1–2 f., Karamuk Lake, Afyon, 02.07.2003, leg, Y. E. Dinçaslan, D. Ayaz, ZDEU. 24/2004. 1–2 m., 3–4 f., Karamuk Lake, Afyon, 06.08.2004, leg. Y. E. Dinçaslan, ZDEU. 264/2005. 1–8 m., 9–20 f., Beyşehir Lake, Konya, 19.05.2005, leg. Y. E. Dinçaslan, ZDEU. 265/2005. 1–6 m., 7–11 f., 12–12 juv., Uluabat Lake, Bursa, 09.07.2005, leg. İ. H. Uğurtaş.

Authors Yunus Emre Dinçaslan, Environmental Protection Agency for Special Areas, 35680 Eskifoça/İzmir, Turkey, e-mail: [email protected]; Hüseyin Arikan, Ege University, Science Faculty, Department of Biology, Bornova, İzmir, Turkey; İsmail Hakki Uğurtaş, Uludağ University, Science and Art Faculty, Department of Biology, Nilüfer, Bursa, Turkey; Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland.

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ISBN 978-3-9812565-4-3

The Rediscovery of Natrix tessellata on Cyprus Bayram Göçmen & Konrad Mebert Abstract. We report on the rediscovery of Natrix tessellata on Cyprus. Apart from a single specimen found before 1900 and having the locality labeled as “(Nicosia) Cyprus”, there were only two juveniles collected 1960 in Northern Cyprus and recovered in the herpetological collection of the Zoological Department of the Ege Üniversity, Izmir. These two specimens were labeled with “Gönyeli Lake”, a reservoir lake near Nicosia. The find of a living subadult specimen at this locality in 2007 documents the persisting presence of a relict N. tessellata population in Cyprus. Ventral scale counts of all four preserved specimens are compared with dice snakes from different areas in the eastern Mediterranean. They show intermediate values between those from Egypt in the south and those from north along the southern coast of Turkey. Due to the dice snake’s rarity and continuing habitat changes for agriculture and urbanization on Cyprus, immediate protection measures for this population are urgently needed. Key words. Natrix tessellata, rediscovery, distribution, Cyprus, conservation Zusammenfassung. Wir berichten über die Wiederentdeckung von Natrix tessellata auf Zypern. Außer einem einzigen vor 1900 gefangenen Belegstück mit der bloßen Fundortangabe „(Nikosia) Zypern“ gab es nur zwei Jungtiere, die 1960 in Nordzypern gesammelt worden waren und in der Herpetologischen Sammlung der Ägäischen Üniversität in Izmir aufbewahrt werden. Diese zwei Tiere waren mit der Fundortangabe „Gönyeli Lake“ bei Nikosia etikettiert. Der erneute Fund einer subadulten, lebenden Würfelnatter an dieser Fundstelle belegt das andauernde Vorkommen einer N. tessellata-Reliktpopulation auf Zypern. Bauchschuppen-Werte aller vier Belegstücke wurden mit entsprechenden Werten von Würfelnattern aus dem östlichen Mittelmeerraum verglichen. Die Werte sind intermediär zwischen jenen aus Ägypten im Süden und jenen entlang der Südküste der Türkei im Norden. Wegen ihrer Seltenheit und der andauernden Landschaftveränderungen für Agrikultur und Urbanisation auf Zypern sind unverzügliche Schutzmaßnahmen dieser Population äußerst dringend.

Introduction The first report that this semi-aquatic snake (Natrix tessellata) occurs on Cyprus originates from a visit by J. Sibthorp in 1887. According brief accounts summarized in Baier et al. (2009), Sibthorp applied the Greek name for the dice snake (υεροφιδι) for one of his observations on the island and incorporated this into an unpublished diary. In 1862, Th. Kotschy collected a specimen on Cyprus which F. Steindachner identified as Tropidonotus hydrus Pall (synonym of N. tessellata). This, at least one individual, was the source for the subsequent inclusion of the dice snake into publications (Steindachner 1863, Unger & Kotschy 1865, Boulenger 1888). However, Boulenger (1888) set a question mark on the species list to its occurrence for unknown reasons, but presumably as he has not seen the specimen himself. Ten years later in January of 1899, Cecconi (1899) found two dice snakes near Nicosia. He described those snakes were easily collected underneath larger stones and half buried, as they were probably hibernating and half numb from the seasonal cool temperatures. Probably due to his previous doubts, Boulenger removed the dice snake on a later herpetological checklist for Cyprus (Boulenger 1910), and based on this, N. tessellata was omitted in most subsequent publications by

him and others (see refs. in Baier et al. 2009). Finally, a live specimen was putatively photographed by G.P. Oxtoby (Hengelo/NL) near Larnaca in 1986 (Schätti & Sigg 1989) but latter authors neither published the photo nor did they explicit validate its identification. Osenegg (1989) reported that the photographed specimen was probably mistaken with a young Dolichophis jugularis, and Böhme & Wiedl (1994) suggested also a possible misidentification with N. natrix cypriaca, which occurs nearby. Further attempts to verify the photographed specimen were not successful (Böhme & Wiedl 1994). But additional locality information by Oxtoby (in lit.) was received by Baier et al (2009) and by us recently. Oxtoby described the site as “Dhekelia south road, 400 m from the beach adjacent to a municipal camping. Although, he could not locate the photo anymore, recent communication (January 2011) supported its positive identification by B. Schätti (in litt.). An additional record for the presence of N. tessellata in Cyprus has been revealed by Göçmen & Böhme (2002) based on the old museum material originated from 1960s. Results and Discussion One of the specimens sampled by Cecconi (1899) was for an extended period the only voucher for Cyprus (MCSNT 18024), stored in the Natural History Muse-

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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um of Torino, Italy (Elter 1981 and Fig. 1). It was verified by the late E. Kramer (Schätti & Sigg 1989) and subsequently also examined by the second author (KM). The whereabouts of the second specimen remains unknown. Böhme & Wiedl (1994) shared the opinion that the Torino (Turin) specimen might be introduced to the island by someone. That specimen had 166 ventrals and

Fig. 1. Ventral and dorsal view of the juvenile dice snake from near Nicosia, Northern Cyprus. Stored as MCSNT 18024 in the Natural History Museum of Torino, Italy.

70 subcaudals (Schätti & Sigg 1989, and confirmed by KM). This ventral scale count is intermediate between the mean value of male dice snakes from Egypt (ventrals = 164.8, n = 6) and those from Israel (ventrals = 166.2, n = 42, Werner & Shapira 2011), and is substantially lower than in dice snakes from the nearest mainland, the Turkish southern coastal area between Antalya to Antakya (mean ventrals of males = 177.2, n = 19, Mebert 1993). The low ventral scale values, the rather small dorsal spots, and the prominent black nuchal angle are typical, but not exclusive, for N. tessellata from Egypt to the Levant (E. Kramer in litt, and pers. unpubl. data), supporting the suspicion, that this specimen was introduced from the south. Since naval traffic is common between Cyprus and the nearby mainland in the surrounding mainland, all inhabited by N. tessellata, the possibility of an introduction could not have been dismissed at that moment. In 2002, Göçmen & Böhme (see also Göçmen et al. 2009) published the finding of two preserved N. tessellata in the Zoological Collection of the Aegean University at Bornova-Izmir, Turkey Göçmen & Böhme 2002, Göçmen et al. 2009 (Fig. 2a, b). The two juveniles were sampled in 1960 at Gönyeli Lake, Nicosia, northern Cyprus (Fig. 3). They challenged the view that the Torino voucher specimen from Cyprus could have wrong locality data or was introduced to the island by man. Gönyeli Lake is a site inland, rendering the undeliberate introduction via ships rather unlikely. Finally, on a field excursion to the Gönyeli area in 2007, a first live N. tessellata was sampled at Gönyeli Lake by the senior author (Göçmen et al. 2008). It is a young female (Fig. 4), whose morphological data together with those from the other preserved specimens are listed in Table 1. The four preserved specimens allow

Fig. 2. Juvenile dice snakes sampled in 1960 from Gönyeli Lake, Nicosia, Northern Cyprus. Preserved at the Zoological Department, Ege Üniversity, Izmir, Turkey (ZDEU 114/1960-1 and 2): female (A), male (B).

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Fig. 3. Google image of the Gönyeli Lake, Nicosia, Northern Cyprus, with the new finding indicated in the yellow circle. Tab. 1. Morphological data of four preserved dice snakes. Characters   Head Length(HL) Head width (HW) Snout-vent Length Tail Length (TL) Frontal Length (FL) Rostral Height (RH) Rostral Width (RW) Preoculars (PreO) Postoculars (PostO) Supralabials (SpL) Sublabials (SbL) Temporal (T) Posttemporals (PostT) Ventrals (V) Subcaudals (SubC) Supraoculars (SpO) Frenals (F) Nasal (N) Gulars (G) Anal (A) Dorsals (D)

ZDEU 253/2007-♀ Gönyeli Lakelet, Nicosia/ N. Cyrpus 15.14 9.28 415 112 4.78 1.75 3 3//3 (R//L) 4//4 8//8 9//10 1//1 2//2 168 70 1//1 1//1 1//1 4 1/1 19

ZDEU 114/1960-1 ♂* ZDEU 114/1960-2 ♀* MCSNT 18024 ♂ Gönyeli Lakelet, Nicosia/ Gönyeli Lakelet, Nicosia/ N. Cyrpus N. Cyrpus Nicosia/ N. Cyrpus 11.2 11.1 4.0 3.9 261 238 66.0 56.0 3.5 3.4 1.5 1.4 2.4 2.2 2//2 3//3 2/2 4//4 4//4 4//3 8//8 8//8 8//8 10//10 10//10 10//10 1//1 1//1 1//1 2//2 2//2 175 177 166 72 62 70 1//1 1//1 1//1 1//1 1//1 1//1 1//1 (semidivided) 1//1 1//1 4 4 4 1//1 1//1 1//1 19 19  

*published data in Göçmen & Böhme, 2002-ZME

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Fig. 4. A young female dice snake from Gönyeli Lake, Nicosia, Northern Cyprus, sampled in 2007. Preserved at the Zoological Department, Ege Üniversity, Izmir, Turkey as ZDEU 253/2007.

an update and a brief comparison to other dice snakes in the eastern Mediterranean arc. Although the number of individuals per sex is too small for reasonably calculating the means of ventrals, the substantially higher ventral counts of the Gönyeli specimens compared to the Torino specimen result in a reduced phenetic affinity between Cypriot and Egyptian-Levant dice snakes. The mean ventral count of the three Gönyeli-specimens exhibits a more intermediary state between specimens from the Turkish southern coast and Egypt. Finally, the Cytochrome b sequence of the new specimen shows affinity to individuals from the Turkish coast (Z.T. Nagy, in litt.). Ultimately, only the finding of more Cypriot specimens and particularly the sampling of tissues for a larger genetic analysis will be able to solve the origin of Cypriot dice snakes, whether they are native or introduced, or may represent a combination of both. The life dice snake was discovered in a temporary pool (180 m a.s.l.) within a dry stream bed (Fig. 5) that drains into Gönyeli Lake, less than 1 km north of it. Apparently, the population at that lake has survived the last approximately 50 years since the collection of the two juveniles in 1960. It indicates that the dice snake is able to survive in semi-arid areas, as long there is at

Fig. 5. Site of the life find of a dice snake – a temporary pool in a stream bed north of Gönyeli Lake, Nicosia, Northern Cyprus.

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least temporary water providing some fish or frogs for food. Comparably, Mebert (2011) included various reports on dice snakes from semi-arid areas, from Jordan to Iran and to China. The new find also generates additional hope, that more dice snake populations on Cyprus might be located in the future. Dice snakes possibly survive on low population sizes over extended periods and remain unnoticed for decades. Various recent discoveries of new or reemerging populations of this species in even well explored areas (e.g. northern Czech Republic), and populated cities such as Prague and Bucharest, show that this species was frequently overlooked, that it is a rapid colonizer, or that its population size can increase dramatically once conditions become suitable (see corresponding reports in Mebert 2011). Four separately introduced and initially rapidly growing populations in Switzerland also show exemplary the colonizing potential of this species (cf. Mebert 2011). The apparent rarity of the dice snake on Cyprus and the continuing habitat changes for agriculture and urbanization requires immediate action to protect this population. If conditions for the dice snake on Cyprus are correspondingly improved and managed, it may have a chance to survive and expand from this population to other sites, to finally establish healthy and stable populations on a wider scale on Cyprus. Acknowledgements We are grateful to Nazım Kaşot (Local biologist from Yeşilyurt, Lefke, North Cyprus) for his field assistance and Wolfgang Böhme (Alexander Koenig Museum, Bonn, Germany) for his valuable suggestions and comments on this manuscript. References Baier, F., Sparrow, D.J. & H.J. Wiedl (2009): The Amphibians and Reptiles of Cyprus. – Edition Chimaira, Frankfurt/M. Böhme, W. & H.J. Wiedl (1994): Status and zoogeography of the herpetofauna of Cyprus, with taxonomic and natural history notes on selected species (genera Rena, Coluber, Natrix, Vipera). – Zoology in the Middle East, Heidelberg 10: 31-52.

Boulenger, G.A. (1888): Second list of reptiles and batrachians from Cyprus. – Annals and Magazines of Natural History (6), XII, London: 505–506. Boulenger, G.A. (1910): A list of the reptiles and batrachians of Cyprus. – Bulletin of the Cyprus Natural History Society, Nicosia 1: 1–3. Cecconi, C. (1899): Rettili ed anfibi raccolti nell’isola di Cipro. – Bollettino della Società Romana per. gli Studi Zoologici, Rome 8: 152–155. Elter, O. (1981): La collezione erpetologica del Museuo di Zoologia deIl’Università di Torino. –Torino. Göçmen, B. & W. Böhme (2002) New evidence for the occurrence of the dice snake, Natrix tessellata (Laurenti, 1768) on Cyprus. – Zoology in the Middle East, Heidelberg 27: 29–34. Göçmen, B., Atatür, M.K., Budak, A., Bahar, H., Yildiz, M.Z. & N. Alpagut (2009): Taxonomic notes on the snakes of Northern Cyprus, with observations on their morphologies and ecologies. – Animal Biology 59: 1–30. Göçmen, B., Kaşot, N., Yildiz, M.Z., Sas, I., Akman, B., Yalçinkaya, D. & S. Gücel (2008): Results of the Herpetological Trips to Northern Cyprus. – North-Western Journal of Zoology 4(1): 139–149 Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti) 1768 in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Mebert, K (Ed.) (2011): The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species. – Mertensiella 18, DGHT, Rheinbach, Germany. Osenegg, K. (1989): Die Amphibien und Reptilien der Insel Zypern. – M.S. thesis, University of Bonn, Germany. Schätti, B. & H. Sigg (1989): Die Herpetofauna der Insel Zypern. Teil 2: Schildkröten, Echsen. Schlangen. – Herpetofauna 11(62): 17–26. Steindachner, F. (1863): Verzeichnis der von Dr. Th. Kotschy im Jahre 1862 auf der Insel Cypern gesammelten Schlangen. – Verhandlungen der Zoologischen und Botanischen Gesellschaft, Wien 13: 1123–1124. Unger , F. & T. Kotschy (1865): Die Insel Cypern ihrer physischen und organischen Natur nach mit Rücksicht auf ihre frühere Geschichte. – Vienna, Austria. Werner, Y.L. & T. Shapira (2011): Morphological variation in the dice snake, Natrix tessellata, in Israel: between sides, among individuals, between sexes and among regions. – Turkish Journal of Zoology 35(4): 451-466.

Author Bayram Göçmen, Ege University, Faculty of Science, Biology Department, Zoology Section, Bornova, Izmir / Turkey; e-mail: [email protected]; Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland, e-mail: konradmebert@ yahoo.de.

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The Dice Snake (Natrix tessellata) in Syria: Distribution, Trade and Conservation Adwan H. Shehab, Aroub Al Masri & Zuhair S. Amr Abstract. The dice snake (Natrix tessellata) in Syria occurs primarily in the west, the far north east and along the Euphrates River. Previous and new locality records confirm the known distribution, but also uncover neglected surveys in northern and eastern Syria. A large trade for the national and international pet market is exploiting regional population of dice snakes, in particular in fish hatcheries. A conservation concept of N. tessellata in Syria is not yet realized. Literature review and personal field notes show a commonly known biology of the dice snake in Syria. Key words. Syria, Natrix tessellata, animal market Damascus, threat, new records.

Introduction

Materials and Methods

Throughout the Middle East, Syria is relatively rich in natural freshwater resources as compared with neighboring countries except Turkey. Several permanent rivers and many ponds, lakes and streams cover most of western Syria, providing relevant habitat for the dice snake, Natrix tessellata. However, little has been published about the distribution of N. tessellata in Syria. Few papers addressed the distribution of this snake along with other reptiles in southwestern Syria (Berger-Dell’mour 1986, Sivan & Werner 1992, Esterbauer 1985, 1992). Esterbauer (1994) discussed several aspects of the life history of N. tessellata in southwestern Syria including biology, feeding habits and behaviour. Recently, Amr et al. (2007) addressed the problem of trading in reptiles in Syria, with reference to N. tessellata. In this paper, we discuss the distribution, trade and conservation of N. tessellata in Syria.

Field trips by the authors covering various habitats in Syria were conducted since 1996 to the present. New and published localities for Natrix tessellata were compiled and mapped. Field observations on the biology of N. tessellata were recovered from field note books regarding feeding, other behaviour and ecology. We visited the local animal market in Damascus several times during 2003–2009 and present the observations as well as summary aspects of trade and conservation for N. tessellata in Syria. Results and Discussion Distribution of Natrix tessellata in Syria The dice snake, Natrix tessellata, is distributed throughout the western part of Syria, but it has been observed

Fig. 1 (next page). A: Distribution of N. tessellata in Syria; B: enlarged for SW Syria. New records: (1) Al Salha-Malkieh, (2) Hemo-Al Qamishli, (3) Tabka Malkieh, (5) Ma’adan, (6) Al Tebne, (7) Shat’ha, (8) Ayn Abu Jum’aa, (9) Dier Azour, (10) Mohasan, (11) Al Miadien, (12) Al Ashara, (13) As’ Salihiyyah, (14) Al Boukamal, (15) Tartous Homs Road, (17) Zarzar Lake, (18) Abu Jarash (Damascus), (19) Ghota, (29) Rwehenah Dam, (30) Abdeen, (31) Sadderom, (32) Al-Mozirieb, (33) 10 km E Sweida, (34) Tall Gnaieh, (35) Nabe’ Ira, (36) Saddelaien, (37) Amtan. Previous records: (4) Taftanaz (Lymberakis & Kalionzopoulou 2003), (16) Al Chatib (Martens 1996), (20) Arnah (Esterbauer 1992), (21) Mount Hermon (Sivan & Werner 1992), (22) Hadar (Esterbauer 1992), (23) Masil Al Fawar (Esterbauer 1994), (24) Harfa, SE Halas (Esterbauer 1992), (25) Taranjah (Esterbauer 1992), (26) Khan Uraynibah (Esterbauer 1992), (27) Al Hamidiyah (Esterbauer 1992), (28) Golan (Berger-Dell’mour 1986), (23). Museum records: (5) HUJR 8270–8273, H. Zinner, 1966, Ma’adan, (16) MHNP 1935–346, Homs, (38) ZMUZ 121236, Aleppo, (39) HUJR 8274–8276, coll. H. Zinner 1966, Sabch - 4 km NW of Sabcha, (40) MHNP 1925-47 to 1925-54, Ataibe, near Otaybah and Bahret el Ateibe (= Utaibe, Otaibe, 20 km east of Damascus ), (41) MHNP 1935-349 to 1935–352, Hama, (42) MHNP 1976-364, Palmyra, (43) MHNG 1388.26–1388.29, Fariatian (= Qariatien), (44) MHNP 6469-70, Lake Tiberiade. Abbreviations: HUJR: Herpetological Collection in the Hebrew University of Jerusalem MHNP: Muséum National d’Histoire Naturelle, Paris, France MHNG: Museum Histoire Naturelle de Geneve, Switzerland ZMUZ: Zoological Museum University of Zürich, Switzerland

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only in a few localities in the east (Fig. 1). Most records are from southwestern Syria, where many established populations are known. However, new findings show its extended distribution into eastern Syria along the lower reaches of the tributaries of the Euphrates River as far south as the border with Iraq. This indicates that the Euphrates River is the largest and probably the most relevant aquatic habitat for Natrix tessellata in eastern Syria. Generally, N. tessellata occurs in all accessible aquatic habitats from fish hatcheries, lakes, springs to rivers. N. tessellata appears to be locally very common. It was found in particular high densities along dams and fish ponds. For instance, more than 50 snakes were observed within an hour in Saddelaien near Swieda, and hundreds of snakes were recovered by snake hunters from fish farms around Al-Mozirieb. Particularly interesting is the isolated museum record from Palmira (Palmyra) (Fig. 1), a locality surrounded by deserts. We don’t know, whether dice snakes still exists there, as this record originates from the last century. But at least, it is a witness of a once wider distribution of N. tessellata in Syria, and with that of a different landscape containing more water. The area of Ataibe (Bahr el Aateibe), 20 km east of Damascus, pertain also to an area that has suffered severe to complete water loss, so that we presume the dice snake is extinct there today.

Notes on the Biology of N. tessellata in Syria In southern Syria, the many new fish farms harbor large populations of Natrix tessellata, as they feed on the abundant fish. This area is a small dam fed by tributary wadis and surrounded by relatively thick vegetation. Many N. tessellata are easily spotted there when they come to the surface by only sticking their heads out. In Al-Mozirieb, for instance, hundreds of snakes could be seen in the artificial fish pond, where Tilapia zilli fish is cultivated (Fig. 2). Occasionally, anurans are consumed as well, as a specimen from Sadderom had vomited an adult Pelophylax bedriagae in June 1999. The hibernation period of N. tessellata in southern Syria does not differ much from those reported for Europe, as it lasts from the end of October until the early March (Gruschwitz et al. 1999). Hibernating individuals have been found during January and February 2003 in Saddelaien and Sadderom. They were resting calmly under rocks or old tree branches. . Others have reported on various aspects of N. tessellata in southern Syria. Martens (1996) found the grass snake (N. natrix) coexisting with N. tessellata in the area of Al Chatib with N. tessellata to be more common. Esterbauer (1994) gave a comprehensive account on N. tessellata from southwestern Syria, where he visited

Fig. 2. Fish farm at Al-Mozirieb, yielding a high density of Natrix tessellata.

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Fig. 3. A bag filled with Natrix tessellata collected by snake collectors from the Al-Mozirieb fish farm.

Fig. 4. Hundreds of Natrix tessellata languish in containers for sale in the animal market in Damascus.

some ponds over a period of 8 months, with those at Masil Al Fawar on a daily basis. According to his accounts, N. tessellata was difficult to observe, because it reacted rapidly to human approach by fleeing into the water and hiding or disappearing in the water and under water plants for hours. He also described the combination of feigning death and aposematic behavior of Syrian N. tessellata, including turning its eyes to the mouth corner, opening its mouth, twisting its tail and exposing its contrastingly coloured ventral side. We found the basic dorsal color of N. tessellata to vary from gray, olive, to reddish brown. Very pale yellowish to olive specimens were also observed as well as dark to melanistic specimens. The dark form represents 3% of all our observed specimens (Fig. 3).

area. Each jar contained probably up to 100 snakes (Fig. 4). Other dice snakes at this animal market are collected from Zarzar Lake. In these shops, the unfortunate snakes die within two weeks, presumably due to the stress and/or suffocation inflicted by the crowded conditions and lack of food. Snakes sold to private consumers usually do not survive more than two weeks with their new owners, as some told us that they kept the snakes in fish aquaria without proper feeding and rearing conditions. A great threat stems from the many fish farms that have been established in Syria, There, N. tessellata is persecuted in great numbers. Farmers consider these snakes as a pest that feed on young fish and remove and kill them regularly. In one occasion at a fish farm in AlMozirieb, we observed a bag filled with tens of freshly collected N. tessellata (Fig. 3). In Al Ghab, along the Orontes River, we encountered many killed snakes near fish farms and agricultural areas. The continuance of such illegal trade will very probably affect the status of N. tessellata in Syria, and in the worst case, lead to a drastic decline in local populations. Overcollecting of certain species raises the need to evaluate the level of trade and make sure that it is not causing irreversible declines in wild populations. A proper management plan for a sustainable harvest is desired, as it has been done for another semi-aqautic snake species (Micucci & Waller 2007). In Syria, no records to track the imports and exports of reptiles are available. The lack of information implies that population declines due to overcollecting could be going undetected. Further investigation should focus on the actual number of traded animals in Syria (Amr et al. 2007). The concept of conservation in its broad spectrum is not yet fully realized in Syria, despite the presence of a conservation authority. This is mainly due to lack of experience and knowledge in this multidisciplinary task. Syria has no area-based environmental laws or protected area system dedicated explicitly towards conserving

Trade of N. tessellata in Syria Over the past years, we visited the animal market in downtown Damascus several times. More than 10 shops are specialized in selling live local animals (birds, mammals and reptiles). We have observed that tens of N. tessellata specimens were placed in crowded water containers, including several dead specimens. These snakes are sold for about 2 US$ a piece as “aquarium” animals. They are sent to Turkey and Europe by buses and other land transport as indicated by customs officers on the borders. They are not consumed or used as a subscription for folk medicine or other traditional practices. In 2004, the Royal Society for the Conservation of Nature in Jordan seized a “bag of snakes” which contained over 100 N. tessellata specimens originating from Syria (Amr et al. 2007). These snakes most likely are condemned to die. In February 2009, the senior author visited the animal market in downtown Damascus and observed nine jars filled with snakes (N. tessellata and perhaps a few N. natrix), originating from fish farms in the Al Ghab

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biodiversity. However, the General Commission of Environmental Affairs is currently drafting a nature conservation law, and there is a system of protected forests and rangelands (Amr et al. 2007). Collecting and hunting animals occurs throughout Syria and is said to be increasing. The hunting laws are considered to be strict, but despite the efforts of the authorities, many collect and trade animals illegally. Law enforcement and awareness should be the first priority for the Syrian authorities to regulate this trade. Nonetheless, N. tessellata is still common in Syria. However, reassessment of the local populations is urgently required. Further studies on the populations inhabiting the Euphrates should be conducted in order to check if these populations are also under threat of trade. Acknowledgments We wish to thank Eng. Ibrahim Zaghtiti from the GIS unit (ACSAD) for his help in producing the maps. We also extend our gratitude to Mr. Ahmad Eidek for his help during our visit to the Euphrates and for providing additional records. Our great appreciation goes to Konrad Mebert for his valuable editing of the text and addition of locality records from museum specimens.

References Amr, Z., Shehab A. & M. Abu Baker (2007): Some observations on the herpetofauna of Syria with notes on Trade in reptiles. – Herpetozoa 20: 21–26. Berger-Dell’mour, V.H. (1986): Zur Herpetofauna des Golan. – Annalen des Naturhistorischen Museums in Wien 87B: 59–67. Esterbauer, H. (1985): Zur Herpetofauna Südwestsyriens. – Herpetofauna 7: 23–34. Esterbauer, H. (1992): Die Herpetofauna des östlichen Golanund Hermongebietes. Funde und Bemerkungen zur Systematik und Ökologie. – Zoology in the Middle East 7: 21–54. Esterbauer, H. (1994): Lebensweise und Verhalten der Würfelnatter im Masil al Fawwar (Syrien). – DATZ 47: 308–311 Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Lymberakis, P. & A. Kalionzopoulou (2003): Additions to the herpetofauna of Syria. – Zoology in the Middle East 29: 33–39. Martens, H. (1996): The rediscovery of the grass snake Natrix natrix (L.) in the Levant. – Zoology in the Middle East 12: 59– 64. Micucci, P.A. & T. Waller (2007): The management of yellow anacondas (Eunectes notaeus) in Argentina: From historical misuse to resource appreciation. – Iguana 14(3): 160–171. Sivan, N. & Y.L. Werner (1992): Survey of the reptiles of the Golan Plateau and Mt. Hermon, Israel. – Israel Journal of Zoology 37: 193–211.

Authors Adwan H. Shehab, General Commission for Scientific Agricultural Research (GCSAR), Douma, P. O. Box 113, Damascus, Syria; e-mail: [email protected]; Aroub Al Masri, National Commission for Biotechnology (NCBT), Head of Biodiversity Laboratory, P.O.B. 3839, Damascus, Syria; Zuhair S. Amr, Department of Biology, Jordan University of Science & Technology, Irbid, Jordan.

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Ecology and Conservation of the Dice Snake (Natrix tessellata) in Jordan Zuhair S. Amr, Konrad Mebert, Nashat Hamidan, Mohammad Abu Baker & Ahmad Disi Abstract. The dice snake, Natrix tessellata, in Jordan still occurs in viable populations, particularly in northwestern areas of the country. But numerous populations have become extinct, following habitat degradation due to irrigation and water pollution. Summary notes on morphology and ecology of Jordanian dice snakes is presented, including aspects of habitat and coexisting herpetofauna, mating, diet, defense behavior, predation and parasites. Literature comparisons indicate that the biology of the dice snake in Jordan fits the common profile of this species. Key words. Squamata, Natrix tessellata, Jordan, distribution, threats

Introduction Jordan includes the southern range limit of the dice snake, Natrix tessellata, in the Levant. It is locally a common species, inhabiting most permanent water bodies in Jordan, including the Jordan River wadi system

and adjoining water bodies. In the Eastern Desert, it is confined to the Azraq Oasis. Yet, our knowledge of this snake is restricted to distributional data (Werner 1971, Disi et al. 1988, Amr et al. 1994, El Oran et al. 1994, Disi et al. 1999) and some information on its diet (Amr & Disi 1998) and a few general biological aspects (Disi et al. 2001). Despite of its local abundance, no particular publication about the dice snake in Jordan exists. We fill this void by summarizing our personal data and observations, reflecting a wide spectrum of information on this species in Jordan. Materials and Methods Distributional data for Natrix tessellata are based on previous records cited in the literature and field collections and observations acquired over the past 20 years. Known sites for the dice snake were routinely visited by the senior author, Nashat Hamidan, and Mohammad Abu Baker to observe changes in their habitats. Also, data were obtained from wildlife biologists employed by the Royal Society for Conservation of Nature (RSCN), Jordan. Threats affecting the existing populations are highlighted. The historical distribution of extinct populations is mapped. We compiled also the information on ecological aspects of this species, gathered from literature records and our personal field observations. The data relate to habitat and coexisting herpetofaunistic elements, mating, defense and feeding behavior, diet, predation and parasites. Results and Discussion Morphology and Genetic Relationship of Jordanian Dice Snakes

Fig. 1: Head drawing of Natrix tessellata from King Talal Dam, Jordan (scale bar 1 cm).

Natrix tessellata is a slender snake with the larger sex, females, reaching a maximum total length of 105 cm in Jordan. The general head morphology compares to that

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Fig. 2: Head of Natrix tessellata from Jordan, Zarqa River.

Fig. 3: Close up of Natrix tessellata from Jordan, South Azraq.

Fig. 4: Distribution with localities of Natrix tessellata in Jordan. (1) Yarmouk River, (2) Birkat al Ara’is, (3) Al-Hemma, (4) East Ghor Canal, (5) Jordan River, (6) Jarash, (7) Al-Sukhuna, (8) Zarqa River, (9) Fuhis ponds, (10) South Azraq, (11) North Azraq, (12) Southern end of the Jordan River, (13) Wadi Al Mujib, (14) Wadi bin Hammad, (15) Rakin, (16) Karak, (17) Wadi Musa, (18) Ayl, Petra, (19) Ma’an, (20) Dana.

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of dice snakes from other areas in being narrow with medium-sized eyes (Gruschwitz et al. 1999, Disi et al. 2001). Jordanian specimens exhibit two preoculars (occasionally three), three postoculars (occasionally four), eight upper labials (rarely seven), with the 4th and the 5th labials touching the eye (Figs. 1 and 2). The lower labial row consists of 9–10 scales. There are 19 strongly keeled scales in the middorsal section, 158–189 ventrals and 50–66 paired subcaudals (Disi et al. 2001). The anal scale is divided. The color pattern varies from all shades of gray with various touches of olive. There are four prominent rows of small to large dark brown to black spots on the dorsum (Fig. 3). The two central rows may fuse, forming transverse vertebral bars. The ventral side maybe white, yellow, pink, reddish or black, with medial longitudinal black stripes or blotches, increasing in its cover subcaudad, so that the ventral side of the tail is usually black (Disi et al. 2001). In regards to its intraspecific phylogenetic relationship, Guicking et al. (2006) pointed out that the Jordanian dice snake is closest to those in Egypt (snakes from the intervening region of Israel/Palestine were not

tested). Additionally, as molecular studies revealed unexpected large divergence for currently isolated populations of dice snakes across a relatively small area in Germany (Guicking et al. 2004), we argue for the conservation evaluation of populations in Jordan and adjacent countries. Especially the population from the Azraq Desert Oasis deserves more attention, since it represents an isolated population within the Jordan territory. Distribution in Jordan Jordan represents a part of the southern range limit of Natrix tessellata in the Middle East (Disi et al. 2001). Historically, the dice snake occurred along the Mediterranean freshwater habitats extending from northern Jordan as far south as Petra (Fig. 4). It was recorded from the upper reaches of the Yarmouk River and its wadi systems, as well as from permanent ponds, small streams and springs. The densest populations inhabit the Zarqa River wadi system that extends from the east of Zarqa across Jarash west to the Jordan Valley. This snake is also distributed along the water bodies in the Jordan Valley (streams, springs, irrigation canals, ponds

Table 1: Summary status of Natrix tessellata from known populations in Jordan. “p.o.” designates personal observation. Population site (lit. cit. or p.o.) 1. Yarmouk River, near Al Isha (p.o.) 2. Birkat Al Arayes (p.o.) 3. Al-Hemma (p.o.) 4. East Ghor Canal (Disi et al. 2001) 5. Jordan River, near Shaikh Hussain (p.o.) 6. Jarash (Werner 1971) 7. Al-Sukhuna (p.o.) 8. Zarqa River (Disi et al. 1988, p.o.)

Status of the population Viable Threatened Viable Viable

Presumed cause for extinction or threat to populations No threats are visible Use of water for irrigation No threats are visible No threats are visible

Last visit to the site 2008 2006 2008 2007

Viable

No threats are visible

2008

Extinct Threatened Viable

Alteration of water course Excessive water pumping for agriculture Pollution No threats are visible The pool was dried up completely due to alteration of the main spring for municipal use

2008 2008 2008

9. Fuhis ponds near Amman

Extinct

10. South Azraq (Werner 1971, Nelson 1973)

Viable

No threats are visible

2008

11. North Azraq (Disi et al. 1988)

Extinct

Main spring dried up completely due to extensive water extraction for municipal use

2008

Viable

No threats are visible

2008

Viable

No threats are visible

2008

Viable

No threats are visible

2005

Threatened Threatened Viable Extinct

Use of water for irrigation Use of water for irrigation No threats are visible Alteration of water course

2004 2005 2008 2006

Extinct

Habitat destruction and alteration

2005

Viable

No threats are visible

2005

12. Southern end of the Jordan River, near Karameh (p. o.) 13. Wadi Al Mujib (p.o.) 14. Wadi bin Hammad (El Oran et al. 1994) 15. Rakin (El Oran et al. 1994) 16. Karak (El Oran et al. 1994) 17. Wadi Musa (Amr et al. 1994) 18. Ayl (Amr et al. 1994) 19. Ma’an (Amr et al. 1994, El Oran et al. 1994) 20. Dana (Disi et al. 2001)

2000

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Fig. 5: Al Ghadeer spring, Ma’an, showing the extensive anthropogenic modifications in the habitat with sewage cement canals constructed in the middle of the spring.

etc.) and the Jordan River (Fig. 4). No other localities have been recorded south of Wadi Al Mujib around the Dead Sea basin, despite the presence of some streams draining into the Dead Sea. The dice snake is also missing in the permanent streams of Wadi Araba. The city Ma’an represents the southernmost locality in Jordan, where Al Ghadeer, the only spring in its old town, used to harbor a viable population of dice snakes. The only habitat for dice snakes in eastern Jordan is found isolated in the Azraq Desert Oasis, a unique wetland located in the heart of the semi-arid Jordanian eastern desert system. This oasis consists of pools that are fed by underground springs and occasional floods. It has no connection with any river or stream in the western part of Jordan, but harbors freshwater fish on which the dice snake feed. In summary, based on published records and our personal observations over the past 20 years, the dice snake was recorded from 20 localities in Jordan (Tab. 1). However, it became extinct from five localities, accounting for 25% of the previously known distribution.

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Conservation in Jordan Populations of Natrix tessellata do not appear to be globally threatened (e.g. Gasc et al. 1997, Gruschwitz

Fig. 6: Ayl spring near Petra, where the population of Natrix tessellata disappeared due to extensive changes in its habitat. Note the cement reservoir around the main spring.

Dice Snake in Jordan

Fig. 7: A pond at Birket al Ara’is from the extreme northwestern part of Jordan, where a viable population of Natrix tessellata survived until today.

et al. 1999), even though many populations are locally threatened in a number of western and central European countries (e.g. Lenz et al. 2001, Mikátová et al. 2001, Duda et al. 2007, Dusej 2007, Mebert 2007, Lenz et al. 2008). The key threat is the loss or modification of aquatic habitats in its range. Similar problems impose threats on Jordan populations of the dice snake. Due to continuous water demand for irrigation or municipal usage all over Jordan, many springs were diverted or pumped directly to reservoirs that caused drying up of many water courses in Jordan. Such alteration led to severe decline or even extirpation of many numerous populations of the dice snake. Conservation status of known populations is presented in Table 1. Over the past 25 years, we have witnessed the disappearance of many sites that used to harbor populations of dice snakes. For instance, a viable population that used to inhabit pools and springs in North Azraq disappeared entirely. This snake was very common during our visits between 1975 and 1985. Subsequently, the water was pumped to Amman and Zarqa with all the pools and ponds drying up completely, causing the complete disappearance of this snake as well as the endemic fish Aphanius serhani. Furthermore, we conclude that the dice snake disappeared from the Roman Pools in Ja-

rash in 1985 and from Al Ghadeer spring in 1988, which used to be one of the most southern populations of the dice snake (Fig. 5). In both cases, no dice snake has been observed in the mentioned years after massive anthropogenic modifications altered the habitat of this species to its disadvantage. The dice snake also disappeared from the Ayl ponds in the 1990’s (personal observations, Fig. 6), as well as from the Fuhis pond near Amman in 1985. At another site in northern Jordan near Ibeen, we observed the complete destruction of the aquatic habitat during 1980, killing all water snakes in addition to the rare Syrian spade-foot toad, Pelobates syriacus. The draining of wetlands led also to the total loss of aquatic habitats suitable for dice snakes in some parts of the Azraq Druze pool system. Other potential threats, affecting the current populations of dice snakes in Jordan, include the extensive pollution of several principal water bodies (e.g. Zarqa River) with sewage and other industrial pollutants that may affect fish and amphibians the snakes prey on. Trade of Natrix tessellata is not a common practice in Jordan and it is rarely sold in pet shops, as it is not a popular snake for husbandry due to its nervous behavior and foul odor. It is neither consumed by locals nor prescribed as a source of folk medicine. This is unlike in

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Fig. 8: Pond in the Azraq Nature Reserve with a relict population of Natrix tessellata.

Egypt, where large numbers of this species are collected for the international pet trade (Anon 2005). Similarly in Syria, dice snakes are offered for sale in animal markets and smuggled into Jordan (Amr et al. 2007, Shehab et al. 2011). On the other hand, dice snakes in Jordan are often killed instantly when encountered out of ignorance and general fear of snakes. We found many dead and mutilated snakes along the banks of ponds, irrigation canals and springs in the Jordan Valley, apparently killed by farmers while watering their crops. In Israel, Werner (1988) stated that a significant decrease of dice snake has been noted since it is considered as a pest in fish farms. At present, the dice snake is not included in the IUCN Red Data Book or under any appendix of CITES (Cox et al. 2006). However, it is listed in Appendix II of the Bern Convention. In Jordan, no clear status for dice snakes is envisioned. A legal framework for animal protection in Jordan was initiated in 1973 with the enactment of laws regulating hunting, trading and trapping of wild animals. Despite the presence of a legal framework designated to protect wild animals in Jordan, no article has specifically referred to the protection of reptiles in general and the dice snake in particular. On a more positive note, three populations of N. tessellata receive currently a better protection, as they are located within nature reserve boundaries: 1) Dana Nature Reserve in the highland near Tafila in the southern range of the Mediterranean mountains; 2) Mujib Nature Reserve situated along the eastern side of the Dead Sea, and 3) Azraq Wetland Reserve in the center of the eastern desert of Jordan. All these nature reserves are practicing conservation strategies, whereby all animals, including the dice snake, are fully protected, rendering some relevant conservation means for this species in Jordan. Notes on Ecological Aspects The dice snake is a semi-aquatic snake that requires permanent water bodies for foraging. Despite the current

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aridity of Jordan, the dice snake has colonized, and thus, inhabits most of the water courses along the Jordan and Yarmouk rivers and their tributaries. The dice snake also occurs along small streams and ponds in the Mediterranean mountains, where we observed it taking refuge among the vegetation near water bodies, usually resting under thick bushes of Typha or Phragmites and in muddy areas. Various other reptiles, as well as amphibians and small freshwater fish occur syntopically with the dice snake in this region. For example in Birket al Ara’is (Fig. 7), it coexists with the following aquatic vertebrate fauna: Levant water frog (Pelophylax bedriagae), green toad (Bufo viridis), tree frog (Hyla savignyi), striped-necked terrapin (Mauremys rivulata), and the cyprinid fish (Garra rufa). Also, the Levantine crab, Potamon potamios, is common in its habitat. Other terrestrial reptiles found within the proximity of the pond were the starred agama (Laudakia stellio), the European chameleon (Chamaeleo chamaeleon), the bridled skink (Mabuya vittata) and the Mediterranean spur-thighed tortoise (Testudo graeca) (Rifai & Amr 2004). In the Azraq Nature Reserve, the dice snake inhabits shallow pools that seasonally reach a maximum depth of 40 cm. As a structural element for sheltering, possibly oviposition and foraging, the open pools are bordered by a dense vegetation of Arundo, Phragmites and Typha (Fig. 8). In this habitat, the snake was associated with four species of fish (Cyprinidae: Acanthobrama lissneri; Cyprinodontidae: Aphanius sirhani; and Cichlidae: Tilapia zilli and Oreochromis aureus), and two amphibians (Bufo viridis and Pelophylax bedriagae). Thermoregulation and Mating: We observed thermoregulatory behavior, whereby snakes basked for hours, on several occasions. Snakes selected as substrate either an object just over the water surface (e.g. stones, tree trunk, etc.) or basked on a spot along the shore. For example at the King Talal Dam, we observed the dice snake basking on rocks, mud piles and decayed plant materials. On the 20 May 2003, we observed a mating aggregation near a water course in South Azraq. We estimated more than 50 snakes that were mostly lying on branches of Typha over the water surface. No mating balls were observed, but each male tried to line up along the body of a female and pressed its head on her back. The mating behavior was observed at 8 am and lasted for several hours. This contrasts to a study in the Tolfa Mountains, central Italy, where the dice snake did not show such a pronounced mating peak, but a few courtships by multiple males (2–5 per female) were observed in the water instead (Filippi et al. 1996, Zimmermann & Fachbach 1996, Capula & Luiselli 1997). Generally at the Italian site, mating “balls” were more frequently found in the syntopic grass snake, Natrix natrix. But Schreiber (1912) reported on a large mating aggregation of 150–200 dice snakes, and similarly, large mating balls and aggregation of dice snakes have been observed elsewhere in

Dice Snake in Jordan

its range (Lenz et al. 2008, Mebert & Ott 2011, Sterijovski et al. 2011). Perry & Dmi’el (1988) reported an average of 12–13 eggs per clutch for gravid females captured from a fish farm in Israel, but rangewide up to 37 eggs have been recorded (see Gruschwitz et al. 1999). In Jordan, we found eggs among decaying plants close to the water at the South Azraq site. Prey and Predation: In South Azraq, we found dice snakes feeding on small red belly tilapia, Tilapia zilli, reaching 10 cm in total length. Snakes were also found in fishing nets feeding on small and medium-sized fish. Amr & Disi (1998) examined 18 Natrix tessellata and found only a single snake with food, a green toad (Bufo viridis). We observed also one dice snake that was feeding on a toad in the Fuhis pond (Amman), where no freshwater fish is present. In Syria, Esterbauer (1985, 1994) reported that the dice snake preyed substantially on green frogs, while the flounder, Platichthys flesus, was reported as food in Turkey (Fautz 1986). More diet accounts from Turkey are presented in Göcmen et al. (2011). N. tessellata has many enemies (see review in Gruschwitz et al. 1999). In the Middle East, Ilani & Shalmon (1984) reported a black whip snake, Dolichophis jugularis, consuming a dice snake in Israel. Mienis (1980) and Esterbauer (1994) observed the predation of this snake by the Smyrna Kingfisher, Halcyon smyrnensis, in Palestine and Israel. Feigning death or thanatosis against such predators is common among snakes of the genus Natrix (Livet 1978). It was also observed in dice snakes from Jordan. One specimen in Azraq feigned dead after we tried to pick it up. It then coiled itself with its mouth open and the tongue protruded outside, similar to defense behaviors described in Gruschwitz et al. (1999). In addition, blood was running from its mouth without our physical influence, resembling the situation depicted in Mebert (2007) and Lenz et al. (2008). This behavior is not common, but was also described for Jordan specimens by Disi et al. (2001). Such as well as other defensive behaviors have been observed to vary geographically (Mebert 2007, Tunijev et al. 2011). Parasites: Two digenetic trematodes were recovered from Natrix tessellata in Azraq Shishan and Druze pools by Madi (1976). She recovered also the parasites Macrodera longicollis from the lungs of dice snakes and Telorchis assula (= Cercorchis ercolanii) from its intestine. Comparatively, Macrodera longicollis was also found in N. tessellata and N. natrix from Romania (Mihalca et al. 2007) and in N. natrix from Turkey, Bulgaria and South Moravia (Yildirimhan et al. 2007, Buchvarov et al. 2000, Borkovcová & Kopřiva 2005). Additional parasites from the eastern Mediterranean region were Telorchis assula from Turkey (Yildirimhan et al. 2007). No other studies of parasites have been conducted with dice snakes from other populations of Jordan.

Acknowledgements We greatly appreciate the input and personal data provided by the staff of the Royal Society for the Conservation of Nature (RSCN). Special thanks are extended to Natalia Bolad for the preparation of the map. References Amr, Z.S. & A.M. Disi (1998): Diet of some snakes from Jordan. – Amphibia-Reptilia 19: 436–439. Amr, Z.S., Al-Oran, R. & A.M. Disi (1994): Reptiles of southern Jordan. – The Snake 26: 41–49. Amr, Z., Shehab, A. & M. Abu Baker (2007): Some observations on the herpetofauna of Syria with notes on trade in reptiles. – Herpetozoa 20: 21–26. Anon (2005): Global Reptile Assessment Regional Workshopnon-Mediterranean Reptiles of the Western Palearctic. – Societas Europaea Herpetologica (SEH) 13th Ordinary General Meeting. Bonn, Germany, 27. September – 2. October 2005. Borkovcová, M. & J. Kopřiva (2005): Parasitic helminths of reptiles (Reptilia) in South Moravia (Czech Republic). – Parasitology Research 95: 77–78. Buchvarov, G., Kirin, D. & A. Kostadinova (2000): Platyhelminth parasite assemblage in two species of snakes Natrix natrix and Natrix tessellata (Reptilia, Colubridae) from Bulgaria: Seasonal variation. – Journal of Environmental Protection and Ecology 1: 124–131. Capula, M. & L. Luiselli (1997): A tentative review of sexual behavior and alternative reproductive strategies of the Italian colubrid snakes (Squamata: Serpentes: Colubridae). – Herpetozoa 10: 107–119. Cox, N., Chanson, J. & S. Stuart (2006): The Status and Distribution of Reptiles and Amphibians of the Mediterranaean Basin. – The World Conservation Union (IUCN), Gland, Switzerland and Cambridge, UK. Disi, A.M., Amr, Z.S. & D. Defosse (1988): Contribution to the herpetofauna of Jordan. III. Snakes of Jordan. – The Snake 20: 40–51. Disi, A.M., Modry, D., Bunian, F., Al-Oran, R. & Z. Amr (1999): Amphibians and reptiles of the Badia region of Jordan. – Herpetozoa 12: 135–146. Disi, A.M., Modry, D., Necas, P. & L. Rifai (2001): Amphibians and Reptiles of the Hashemite Kingdom of Jordan: An Atlas and Field Guide. – Edition Chimaira, Frankfurt am Main, Germany. Duda, M., Grillitsch, H., Hill, J. & R. Klepsch (2007): Die Würfelnatter Natrix tessellata (Laurenti, 1768) im Südlichen Wiener Becken und am Alpenostrand (Niederösterreich). – Herpetozoa 20(1/2): 35–56. Dusej, G. (2007): Die Würfelnatter; Lebensweise und Schutzmöglichkeiten. – Koordinationsstelle für Amphibienund Reptilienschutz in der Schweiz – Karch, Neuchâtel, Switzerland. El-Oran, R.M., Al-Melhem, W.N. & Z.S. Amr (1994): Snakes of southern Jordan. – Bollettino di Zoologia 61: 359–367. Esterbauer, H. (1985): Schlangen in Südwestsyrien – Funde und Bemerkungen zur Systematik und Ökologie. – Mitt. Zool. Ges. Braunau 4: 289–296. Esterbauer, H. (1994): Lebensweise ind Verhalten der Würfelnatter im Masil al Fawwar (Syrien). – DATZ 47: 308–311.

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Zuhair S. Amr, Konrad Mebert, Nashat Hamidan, Mohammad Abu Baker & Ahmad Disi Fautz, R. (1986): The flounder, Platichthys flesus, as prey of the dice snake, Natrix tessellata, in Turkey. – Zoology Middle East 1: 118–119. Filippi, E., Capula, M., Luiselli, L. & U. Agriml (1996): The prey spectrum of Natrix natrix (Linnaeus, 1758) and Natrix tessellata (Laurenti, 1768) in sympatric populations. – Herpetozoa 8: 155–164. Gasc, J.P., Cabela, A., Crnobrnja-Isailovic, J., Dolmen, D., Grossenbacher, K., Haffner, P., Lescure, J., Martens, H., Martínez-Rica, J.P., Maurin, H., Oliveira, M.E., Sofianidou, T.S., Veith, M. & A. Zuiderwijk (Eds.) (1997): Atlas of Amphibians and Reptiles in Europe. – Collection Patrimoines Naturels 29 –Societas Europaea Herpetologica, Muséum National d’Histoire Naturelle & Service du Petrimone Naturel, Paris, France. Göçmen, B., Çiçek, K., Yildiz, M.Z., Atatür, M.K., Dinçaslan, Y.E. & K. Mebert (2011): A preliminary study on the feeding biology of the dice snake, Natrix tessellata, in Turkey. – Mertensiella 18: 365–369. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA Verlag,Wiesbaden, Germany: 581– 644. Guicking, D., Herzberg, A. & M. Wink (2004): Population genetics of the dice snake (Natrix tessellata) in Germany: Implications for conservation. – Salamandra 40: 217–234. Guicking, D., Lawson, R., Joger, U. & M.Wink (2006): Evolution and phylogeny of the genus Natrix (Serpentes: Colubridae). – Biological Journal of the Linnean Society 87: 127–143. Ilani, G. & B. Shalmon (1984): Snake eats snake. – Israel Land & Nature 9: 125. Lenz, S., Herzberg, A. & A. Schmidt (2001): Entwicklung und Vernetzung von Lebensräumen sowie Populationen Bundesweit Bedrohter Reptilien an Bundeswasserstrassen am Beispiel der Würfelnatter (Natrix tessellata) an den Flüssen Mosel, Lahn und Elbe. Abschlussbericht zum Erprobungs- und Entwicklungsvorhaben. – DGHT, Rheinbach, Germany. Lenz, S., Mebert, K. & J. Hill (2008): Die Würfelnatter (Natrix tessellata). – In: DGHT (Ed.): Die Würfelnatter – Reptil des Jahres 2009. – DGHT, Rheinbach, Germany: 6–32. Livet, F. (1978): L’ Herpéofaune du Nord-Est de la Montagne Noire. – Doctorat de Spécialité Thesis, Univ. Sciences, Montpellier, France. Madi, M. (1976): Systematic and morphological studies on digenetic trematodes from some aquatic vertebrates of the Azraq area. – M.S. thesis, The Jordan University, Amman, Jordan. Mebert, K. (2007): Die Würfelnatter am Brienzersee. – In: Jahrbuch 2007 Uferschutzverband Thuner- und Brienzersee. – UTB Selbstverlag, Thun, Switzerland: 169–180. Mebert, K. & T. Ott (2011): Mating aggregation in Natrix tessellata. – Mertensiella 18: 437–439.

Mienis, H.K. (1980): A case of predation on Natrix tessellata by the Smyrna kingfisher (Reptilia: Serpentes: Colubridae). – Salamandra 16: 135. Mihalca, A.D., Gherman, C., Ghira, I. & V. Cozma (2007): Helminth parasites of reptiles (Reptilia) in Romania. – Parasitology Research 101: 491–492. Mikátová, B., Zavadil V. & V. Laňka (2001): Dice Snake - Natrix tessellata (Laurenti, 1768). – In: Mikátová, B., Vlašín M. & V. Zavadil (Eds.): Atlas of the Distribution of Rep­tiles in the Czech Republic, – ­AOPK ČR, Brno-Praha, Czech Republic: 140–151 (in Czech and English). Nelson, B. (1973): Azraq: Desert Oasis. – Penguin Books, London. Perry, G. & R. Dmi’el (1988): The reproduction of Natrix tessellata in Israel. – Herpetological Review 19: 56–57. Rifai, L. & Z. Amr (2004): Morphometrics and biology of the striped-necked terrapin, Mauremys rivulata (Valenciennes, 1833), in Jordan (Reptilia: Testudines: Geoemydidae). – Zoologische Abhandlungen (Dresden) 54: 177–197. Schreiber, E. (1912): Herpetologica Europea. – G. Fischer-Verlag, Jena, Germany. Shehab, A.H, Al Masri, A. & Z.S. Amr (2011): The dice snake, Natrix tessellata, in Syria: distribution, trade and conservation. – Mertensiella 18: 388–392. Sterijovski, B, Ajtić, R., Tomović, L., Djordjević, S., Djurakić, M., Golubović, A., Crnobrnja-Isailović, J., Ballouard, J-M., Groumpf, F. & X. Bonnet (2011): Natrix tessellata on Golem Grad, FYR of Macedonia: a natural fortress shelters a prosperous snake population. – Mertensiella 18: 298–301. Tunijev, B., Tunijev, S., Kirschey, T. & K. Mebert (2011): Notes on the dice snake, Natrix tessellata, from the Caucasian Isthmus. – Mertensiella 18: 343–356. Werner, Y.L. (1971): Lizards and snakes from Transjordan, recently acquired by the British Museum (Natural History). – Bulletin of the British Museum (Natural History), Zoology 21: 213–256. Werner, Y.L. (1988): Herpetofaunal survey of Israel (1950–1985), with comments on Sinai and Jordan and on zoogeographical heterogeneity. – In: Yom-Tov, Y. & E. Tchernov (Eds.) – The Zoogeography of Israel. – Dr. W. Junk Publishers, Dordrecht, Netherlands. Yildirimhan, H.S., Bursey, C.R. & S.R. Goldberg (2007): Helminth parasites of the grass snake, Natrix natrix, and the dice snake, Natrix tessellata (Serpentes: Colubridae), from Turkey. – Comparative Parasitology 74: 343–354. Zimmermann, P. & G. Fachbach (1996): Verbreitung und Biologie der Würfelnatter, Natrix tessellata tessellata (Laurenti, 1768), in der Steiermark (Österreich). – Herpetozoa 7: 99–124.

Authors Zuhair, S. Amr, Department of Biology, Jordan University of Science & Technology, Irbid, Jordan, e-mail: [email protected]. jo; Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland; Nashat Hamidan; The Royal Society for the Conservation of Nature, Amman, Jordan; Mohammad Abu Baker, University of Illinois at Chicago, Department Biological Sciences, Chicago, IL 60607, USA; Ahmad Disi, Department of Biology, Jordan University, Amman, Jordan.

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MERTENSIELLA 18

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20 September 2011

ISBN 978-3-9812565-4-3

Distribution and Recent Range Extension of Natrix tessellata in Egypt Sherif Baha El Din Abstract. The distribution of dice snake (Natrix tessellata) in Egypt is briefly summarized based on literature, museum specimens and personal observation. The species is increasingly being used for the local pet trade. But it also has reclaimed new areas in the west of Alexandria, Suez Canal zone, and is extending its area of occurrence southward along the Nile. Key words. Dice snake, Natrix tessellata, range, dispersal, Egypt

The dice snake (Natrix tessellata Laurenti 1768) has become a relatively abundant species in the local pet trade in Egypt. Despite this frequent sampling of wild caught specimens, knowledge of the species’ distribution in the country remains somewhat patchy. Its records in the historical literature have been rather scant. It was first reported by Peters (1863) from the Delta. Anderson (1898) recorded only one example collected at Baltim. Similarly, Flower (1933) and Marx (1968) both reported the species only from a handful sites in the northern Nile Delta (Tab. 1). Based on further specimens and observations made during the past three decades, Werner (1983), Gruschwitz et al. (1999) and Baha El Din (2006) expended the geographic range of the species slightly, stating that it was found throughout the Nile Delta and lower Nile Valley, as far as El Wasta, Fayoum and the Suez Canal zone. Since the construction of the “High Dam” in the late 1960s massive ecological changes took place in the Nile Valley, particularly along the Nile River and its tributaries south of Cairo. The Nile in the pre-dam days was an unpredictable and seasonal water way that became flooded annually, leaving behind its barren sandy banks suit-

able for Nile crocodiles Crocodilus niloticus and Egyptian plovers Pluvialis aegyptius (Aves), both of which are now extinct in the lower portion of the Nile. After the construction of the “High Dam”, the Nile became a steady and slow flowing river. Extensive swamp vegetation gradually took foot along the river banks, which in turn allowed many wetland species, that were confined previously to the delta swamps, to spread southwards along this new ecological corridor, including N. tessellata and Bufo kassasii, as well as reed inhabiting birds such as the purple gallinule Porphiryo porphiryo. In Egypt the species is strongly associated with aquatic habitat, only rarely venturing away from wetlands. It inhabits fresh-water wetlands of all kinds, including rivers, canals, swamps and lake shores. In Egypt it appears to be largely crepuscular or nocturnal, but has also been seen active during the day (pers. obs.). It is particularly common in waterways fringed with dense reeds and other swamp vegetation. The recent abundance of the species in the pet trade is possibly due to better trapping techniques by animal trappers. Snake catchers from the famous animal trading village of Abu Rawash on the outskirts of Cairo ex-

Fig. 1. Natrix tessellata from Giza.

Fig. 2. Lentic habitat of Natrix tessellata near Bilbis, eastern Nile Delta.

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Konrad Mebert

Tab 1. List of known documented records of Natrix tessellata from Egypt. Abbreviations: FMNH = Field Museum of Natural History, Chicago; NMNH = National Museum of Natural History, Washington D.C.; MNHN = Muséum national d’Histoire naturelle, Paris; SMB = Sherif Baha El Din private collection, Cairo; TAU = Tel Aviv University Museum, Tel Aviv; HUJ = The Hebrew University of Jerusalem; UMMZ = University of Michigan Museum of Zoology, Ann Arbor; ZFMK = Zoologisches Forschungsmuseum Alexander Koenig, Bonn. Map reference number 1 2 3 4 5 6 7 8 9 10 11 12

Specimen number or source

Location

District / Governorate

Helwan Gebel Asfar El Hammam 48 km S Port Said Mansoura Ibtu Shirbin - Kafr El Battikh Biyala - El Burg Abu Hammad El Ferdan 7.5 km W Simbellawen Abu Rawash

Cairo Cairo Matruh Port Said Daqahlia Kafr El Sheikh Gharbiya Gharbiya Sharqia Ismailia Daqahlia Giza

13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40

Baha El Din, pers. obs. Baha El Din, pers. obs. Wissam Farag, pers. com. Baha El Din, pers. obs. Flower 1933, Saleh 1997 Stein & Helmy 1994 FMNH-72116, 72117 FMNH-75285, 75286 MNHN-5145 MNHN-5147 NMNH -124722, 124723 UMMZ-181533, Stein & Helmy 1994, ZMFK-50278 FMNH-75287, 75288 UMMZ-181534 HUJ-R 8580,Werner 1983 TAU-10470,Werner 1983 TAU-10526,Werner 1983 Stein & Helmy 1994 Stein & Helmy 1994 Stein & Helmy 1994 Stein & Helmy 1994 Stein & Helmy 1994 Stein & Helmy 1994 Stein & Helmy 1994 Stein & Helmy 1994 Stein & Helmy 1994 Flower 1933 Baha El Din, pers. obs. Baha El Din, pers. obs. Baha El Din, pers. obs. Baha El Din, pers. obs. Baha El Din, pers. obs. SMB-8204 SMB-8215 Baha El Din, pers. obs. Stein & Helmy 1994 Anderson 1898 MNHN-5148 ZMFK-50274/5 ZMFK-50272

Lake Manzala - Gheit El Nasara Kom O Shim 8 km S Ismailia Bitter Lake west side Ismailia Dekrens Gamasa Simbellawen El Mansouria Kafr Hakim Nahya El Ganaien Bahr El Baqar 15 k NW Ismailia - Salhia Rd Shirbin 30 km S Baltim 7.5 km NW Kafr El Sheikh 10 km N Disuq 5 km N Dirut towards Edfina 8 km SW Rosetta Bilbis 5k NE Bilbis Damietta Abu Madi Baltim Ain Ghossein Abgig

Damietta El Faiyum Ismailia Ismailia Ismailia Daqahlia Daqahlia Daqahlia Giza Giza Giza Ismailia Port Said Ismailia Gharbia Kafr El Sheikh Kafr El Sheikh Beheira Beheira Beheira Sharqia Sharqia Damietta Daqahlia Kafr El Sheikh Ismailia El Faiyum Bani Suef

41

ZMFK-50273

plained how they find and catch N. tessellata at night by using strong flashlights under water in fresh water

402

El Wasta: ≈ Abwid desert Masaret Abu Sir

Bani Suef

canals, where the snakes were easily detected and captured.

Sexual Dimorphism in the Dice Snake

Fig. 3. Distribution of Natrix tessellate in Egypt. Numbers correspond to those in the first column in Table 1.

In conclusion, recent evidence shows that the species is certainly widespread in the Nile Delta and is found also in the lower part of the Nile Valley south to at least 29º N, wherever suitable habitats exist. Additional searches are needed to confirm its occurrence further south, but there are no apparent ecological barriers that could prevent it from reaching further south along the Egyptian Nile River, perhaps as far south as Luxor (25°40’N) or Aswan (24°02’N). Its extension into Lake Nasser is uncertain, as the Lake lacks comparable habitats, such as the reed covered shores of the Nile River downstream. But N. tessellata appears ecologically well adapted to aquatic systems in arid areas and colonized fairly rapidly into newly reclaimed areas from the desert in the Suez Canal zone. With an expansion rate of 3 km/year (K. Mebert, pers. comm.), it would reach the Aswan and Lake Nasser in approximately 250 years by itself, and the border with Sudan in another 110 years. More recently it colonized areas west of Alexandria in the vicinity of El Hammam (Wisam Farag, pers. comm.). It is likely that the species will colonize areas recently reclaimed with Nile water in North Sinai.

References Anderson, J. (1898): Zoology of Egypt. I, Reptilia and Batrachia. – B. Quatrich, London. Baha El Din, S.M. (2006): A Guide to the Reptiles and Amphibians of Egypt. – American University in Cairo Press. Flower, S.S. (1933): Notes on the recent reptiles and amphibians of Egypt, with a list of the species recorded from that kingdom. – Proceedings of the Zoological Society of London, 1933: 735–851. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Marx, H. (1968): Checklist of the reptiles and amphibians of Egypt. – Special Publication, United States Navel Medical Research Unit Number 3, Cairo. Saleh, M.A. (1997): Amphibians and Reptiles of Egypt. – Publication of the National Biodiversity Unit, no. 6. Egyptian Environmental Affairs Agency. Stein, K. & Helmy, I. (1994): Some new distribution records for the snakes of Egypt (Squamata: Serpentes). – Bulletin of the Maryland Herpetological Society 3(1): 15–26. Werner, Y.L. (1983): Lizards and snakes from eastern lower Egypt in the Hebrew University of Jerusalem and Tel Aviv University, with range extensions. – Herpetological Review 14: 29–31.

Author Sherif Baha El Din. M, 3 Abdala El Katib St, Dokki, Cairo, Egypt, e-mail: [email protected]

403

MERTENSIELLA 18

403-413

20 September 2011

ISBN 978-3-9812565-4-3

Ecological and Biological Comparison of Three Populations of the Dice Snake (Natrix tessellata) from the Southern Caspian Sea Coast, Iran Faraham Ahmadzadeh, Konrad Mebert, Saeedeh Ataei, Elham Rezazadeh, Leili Allah Gholi & Wolfgang Böhme Abstract. The dice snake (Nartix tessellata) is abundant and widespread in Iran. However, published data are few and concern mostly distributional records and morphological characters. No ecological studies have been published on this species in Iran. During the spring and summer of 2008, a total of 116 N. tessellata were collected. Weight, body length, tail length, total length and lengths of testes and ovaries (to assess vitellogenesis) were measured. Data on some physical characters of the aquatic habitat was obtained at all stations. The mean of characters was compared between stations and each season separated by gender. The sex ratio was not different from 1:1. Juveniles contributed 23% of the population (3:1). Size class distribution was approximative bimodal for both sexes and a pronounced sexual dimorphism was observed. In both sexes weight–length relationship was isometric. Females started to yolk their follicles in May and reach a maximum level in summer. Unlike females, testes activity in males lasted over the entire season. Whereas N. tessellata occurs sympatrically with its congener the grass snake, N. natrix, across most of the southern Caspian Sea coast, the former is more abundant at open sites close to the water and inhabits also saline habitat such as at Gomishan Wetland and Ghaz Harbour. Our measurements showed that N. tessellata specimens from the Gomishan station reached on avearge the largest body proportions. It seems that this station represents a particulary well preserved habitat. Key words. Natrix tessellata, sexual dimorphism, reproduction, Gomishan Wetland, Ghaz Harbour, Sari, Iran.

Introduction Natricinae  is a  subfamily  of Colubridae, containing 28  genera (65–80 species) of snakes  including Natrix (Zaher 1999, Zug et al. 2001). The dice snake, Natrix tessellata (Laurenti 1768), occurs over most of Iran except the arid southeast. Iran lies in the center of its wide distribution, ranging from Germany and Switzerland to the Balkans, the Near East, across Russia, Ukraine, and central Asia into northwestern China (Bannikov et al. 1977, Gruschwitz et al. 1999, Arnold & Ovenden 2002, Göcmen & Böhme 2002, Guicking 2004, Vlček et al. 2010). N. tessellata is mostly sympatric with its congener in Iran, the grass snake N. natrix, but it ranges farther south into Central Iran and Baluchistan (Leviton et al. 1992, Firouz 2000, Latifi 2000, Rastegar– Pouyani et al. 2008, Bagherian & Kami 2009, Guicking et al. 2009). This semi–aquatic snake occupies most aquatic habitats in Iran. It is common along rivers, in ponds, meadows, agricultural wetlands, lakes, and inhabits even seashores. Unlike the grass snake, N. tessellata is strictly associated to the immediate vicinity of aquatic environments and sometimes occurs there in high densities of up to 90 specimens per hectare (Bendel 1997, Gruschwitz et al. 1999, Latifi 2000, Arnold & Ovenden 2002, Shcherbak 2003, Carlsson et al. 2011). N. tessellata feeds on fishes, frogs and tadpoles (Trutnau 1986, Leviton et al. 1992, Filippi et al. 1996, Arnold & Ovenden 2002, Luiselli et al. 2007). Most studies deal-

ing with the biology and ecology of N. tessellata concern European populations (e.g. Mebert 1993, Filippi et al. 1996, refs. in Gruschwitz et al. 1999, Luiselli et al. 2007, Conelli & Nembrini 2007, and refs. in Mebert 2011a). Despite its abundance and widespread distribution in Iran, this species has not been studied in this region. Therefore, our objective was to acquire basic ecological information on N. tessellata in Iran based on the comparison between three coastal populations from the Caspian Sea. This paper attempts to provide some data on the natural history of this species, including its frequency, body size, sexual dimorphism, weight–length relationship, reproduction and habitat use. Material and Methods Study Sites The field study was conducted at three stations along the southeastern Iranian coastline of the Caspian Sea: Gomishan Wetland, Ghaz Harbour and Sari (Fig. 1). The Gomishan Wetland is situated 60 km to the northwest of Gorgan (37º 09’ 07.3” N and 53º 54’ 32” E). It is a large shallow marsh lagoon with a surface area of 20,000 ha, an average depth of 100 cm and a maximum depth of 250 cm. It is inhabited by over 20 species of fish and 100 species of birds, rendering the Gomishan Wetland a high diversity and justifying its strict conservation watch. This wetland is a recreational and educational area and

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Faraham Ahmadzadeh, Konrad Mebert, Saeedeh Ataei, Elham Rezazadeh, Leili Allah Gohli & Wolfgang Böhme

Fig. 1. Northern Iran and the sampling region in the southeastern Caspian Sea.

annually attracts many visitors in all seasons  (Scott 1995, Kiabi et al. 1999). The second station, Ghaz Harbour, is located at the periphery of Gorgan (36º 47’ 41.0” N and 53º 56’ 43.0” E). It is a relevant area for fishing and marine transportation. The third station is located close to Sari, the Capital of Mazandaran Province (36º 32’ 42.9” N and 53º 06’ 41.9” E). The rainy season lasts about seven months with an annual precipitation of more than 1110 mm, enabling a substantial growth season that yields a lush and green landscape. The main habitat at this station consists of large woodlands and fish ponds. Photographic examples of all three stations are depicted in Figure 2. At all three stations, a HACH portable was used to measure following physiochemical characters: temperature (°C), PH, salinity (%) and total dissolved solids TDS (gr/lit). Field Work Field work was focused on spring (April and May) and summer (June and July) months in 2008. Field methods were identical at all study sites. Snakes were searched by walking 1 km transects along both sides of the river banks and/or lakes shores. All specimens were collected by hand in the morning between 8–10 am. Snakes were transferred to the Zoology Laboratory of Environmental Sciences Research Institute, Shahid Beheshti

University, and fixed in 10% formalin. We weighted (W: to the nearest gram) all adult specimens and measured them to the nearest centimeter. Following morphological characters were recorded: SVL (snout–vent length), LCT (length of complete tail from the anal scale to the tip of tail), TL (total length), RTL and LTL (right and left testes lengths) in males, and ROL and LOL (right and left lengths of ovaries) in females to assess their reproductive status. Some of these measurements were used to generate the following ratios to compensate for allometric growth and different size classes in the samples: (LCT/SVL) × 100, (SVL/TL) × 100 and (LCT/TL) × 100. Statistical Analysis Adult female and male snakes were partitioned and separately analyzed from juveniles. Statistical analyses were performed with SPSS ver. 11.5 with significant levels set at 0.05 and 0.01. Means are presented with ± one standard error, and the data set was tested for normality and the assumptions of homogeneity of variances. A transformation was performed for non–normal data sets to better approximate normal distribution or equal variances. The overall sex ratio was assessed using a Chi– square (χ2) test, and sexual size dimorphism (SSD) was analyzed using a t–test. An analysis of variance (ANOVA) followed by Duncan test was performed to detect

405

Biological Aspects of Dice Snakes from the SE Caspian Sea, Iran

Fig. 2. Study sites; Gomishan Wetland A–B; Ghaz Harbour C–D; Sari E–F.

significant differences among the three populations of Natrix tessellata. A scatter plots with regression equations were produced to depict the relationship between some traits (Zar 1999). Results Gomishan Wetland yielded the highest values for temperature (°C), PH, salinity (%) and TDS (gr/lit) followed by Ghaz Harbour and Sari, respectively. Compared to average seawater (3.5%), the water at Gomishan Wetland was 10 x saltier (28%), whereas the water at Sari was brackish (1.3%) (Tab. 1).

406

In spring and summer, a total of 116 Natrix tessellata were sampled with dorsal coloration ranging from grey to olive, and several rows of dorsal spots. The sample was partitioned into 44 females, 45 males, and 27 juvenile from all three stations (Tab.  2). Based on Chi– square tests (χ2) the sex ratio in adults (77% of all specimens) was not different from 1:1 (χ2 = 0.01, df = 1, n = 89, P > 0.05), whereas no such results were obtained from juveniles, comprising 23% of the total sample. The frequency of N. tessellata in SVL-classes for both sexes is shown in Figure 3. Adult specimens ranged in SVL from 35 to 83 cm (x = 56 cm). The graph shows the different size classes in both sexes. In males, the highest frequency of SVL was found in the class of 40–45  cm

Faraham Ahmadzadeh, Konrad Mebert, Saeedeh Ataei, Elham Rezazadeh, Leili Allah Gohli & Wolfgang Böhme

(27%), with more males being relatively abundant in the next larger classes comprising the range of SVL from 50–60 cm. A second large peak of males contained the class of 60–65 cm, represented by 21% of all males. The frequency of females’ SVL varied more across the size classes. A first frequency peak produced the class of 40– 45 cm (11%). The next larger peak consisted of females in the class of 60–65 (18%), followed by another high frequency (16%) of female snakes in the class of 75–80 cm (Fig. 3). There are significant gender differences (P < 0.01) in SVL, TL, LCT/ SVL, SVL/TL, LCT/TL. Only tail length did not show dimorphism based on mean size, when all size classes were lumped, and when absolute sizes were compared (males, R2 = 0.84; females, R2 = 0.61). But regarding absolute values, sexual size dimorphism was quite pronounced with females reaching a larger SVL than males. On the other hand, males showed relatively longer tails than females within a size class (LCT/SVL) (Tab. 3 and Fig. 4). Juveniles (SVL < 30 cm) have not been used in the sexual dimorphism analyses. Total weight ranged from 33 to 389 grams across all specimens. Females were heavier than males. The relation between body weight and total length were plotted separately for males and females (Fig. 5). Both sexes followed almost the same growth curve. The correlation of length–weight relationship was significant (males, R2 = 0.87; females, R2 = 0.79). The smallest “adult” female with enlarged ovary measured 36 cm SVL. Lengths of ovaries (right and left) indicating vitellogenesis were significantly correlated with SVL. This correlation was more pronounced in specimens captured in the summer and the left ovary, than those captured in spring and right ovary (Fig. 6). The smallest male with thickened efferent ducts indicating sexual maturity measured 35 cm SVL. The regression between testes length (right and left) and SVL was statistically significant (Fig. 7). R– square values for summer captures were higher than for spring ones. ANOVA showed significant differences (P < 0.01) among the three stations in absolute measurements of

Fig. 3. Frequency of SVL distribution of adult Natrix tessellata from the southeastern Caspian Sea, Iran.

weight, tail length, SVL, and left testis length in males, but ratios and the length of right testis did not yield any significant differences (Tab. 4). In females, significant differences were obtained in tail length, SVL, and left ovary length, but as in males, there were no considerable differences in ratio values. Duncan tests confirmed these results and rendered that the population of Gomishan Wetland was the most distinct one in the majority of characters. In females these characters included SVL, tail length, and ovary length. No differences were detected between the populations of Ghaz Habour and Sari. Although, there were no statistical differences in weight of females between the populations, specimens from the Gomishan Wetland (240.3190 ± 89.351) were on average heavier than those from Ghaz Harbour (168.3519 ± 109.51) and Sari

Tab. 1. Some physiochemical characters of water, temperature (TEM), PH, salinity (SAL) and total dissolved solids (TDS) measured once in spring at sampling sites in Gomishan Wetland, Ghaz Harbour and Sari. Station Gomishan Wetland Ghaz Harbour Sari

TEM(°C) 21.9 18.19 16.9

PH 8.97 8.4 8.2

Salinity (%) 28.7 2.13 1.3

TDS (gr/lit) 22.2 20.93 20.4

Tab. 2. Number of Natrix tessellata sampled based on station, season and sex/maturity.

Spring Summer

Gomishan Wetland Male Female Juvenile 5 8 5 20 2 0

Male 9 4

Ghaz Harbour Female Juvenile 12 5 8 6

Male 3 4

Sari Female 14 0

Juvenile 8 3

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Tab. 3. Sexual dimorphism of morphological traits of Natrix tessellata from the southeastern Caspian Sea. The last three columns show results from independent two–tailed t–tests for sexual dimorphism (males, n = 45; females, n = 44): SVL (snout–vent length), LCT (length of complete tail from the anal scale to the tip of tail), TL (total length).

Trait SVL LCT TL LCT/TL LCT/SVL SVL/TL

Adult Males Mean ± SD Range 50.8356 ± 08.910 35.30–68.20 14.5067 ± 02.668 10.60–19.60 65.3200 ± 11.423 46.30–86.90 22.2099 ± 01.294 17.73–25.53 28.5693 ± 02.077 21.54–33.55 77.8262 ± 01.220 76.06–82.27

Adult Females Mean ± SD Range 61.9773 ± 12.382 35.90–82.90 15.0886 ± 03.897 03.30–21.08 77.0659 ± 15.634 45.80–103.0 19.4788 ± 02.846 05.75–22.31 24.3274 ± 03.964 06.10–28.72 80.5210 ± 02.846 77.69–94.25

Fig. 4. Relationship between SVL and tail length in males and females of Natrix tessellata from the southeastern Caspian Sea, Iran.

(172.3309 ± 76.289) (Tab. 5). Also in males, there are significant differences in weight, SVL, and tail length, between those from the Gomishan Wetland and the two other stations (P < 0.05). Ratios yielded no differences among the populations. Discussion According to the literature, the color pattern of Natrix tessellata from the southeastern Caspian Sea conforms to the general pattern from other areas of its range (Gruschwitz et al. 1999, Bagherian & Kami 2009). The size class of juveniles selected for specimens with a SVL < 30 cm was based on a male dice snake in this study that exhibited a SVL of 35 cm and showed an enlarged efferent duct and a female with enlarged ovaries at SVL of 36 cm,

408

df 87 87 87 87 87 87

t 4.863 0.824 0.053 5.848 6.343 5.827

P 0.001 0.41 0.001 0.001 0.001 0.001

Fig. 5. Length–weight relationship in males and females of Natrix tessellata from the southeastern Caspian Sea, Iran.

both indicating some sexual maturity. This size at maturity is much smaller than the minimum size limit determined for adult (sexually mature) dice snakes selected in other studies (e.g. Luiselli & Rugiero 2005, Luiselli et al 2007, Carlsson et al. 2011). Their size limit for adult snakes was determined on the smallest males that were found mating (SVL 48–50 cm) and females that developed eggs (SVL 55–58 cm). However, other studies indicated even smaller size of maturity in N. tessellata. For example, Göçmen et al. (2011) found a small male with a SVL of 28 cm showing straw colored testes, indicating maturity. That such a small size for mature males is possible was shown by Trobisch-Glässer & Trobisch (2001), who recorded a one-year old male N. tessellata under captive conditions that successfully copulated, as the mated female subsequently developed and

Faraham Ahmadzadeh, Konrad Mebert, Saeedeh Ataei, Elham Rezazadeh, Leili Allah Gohli & Wolfgang Böhme

Fig. 6. Length of ovaries (right and left) and SVL relationship in Natrix tessellata sampled in spring (April and May) and summer (June and July) along the southeastern Caspian Sea, Iran.

Fig. 7. Length of testes (right and left) and SVL relationship in male Natrix tessellata sampled in spring (April and May) and summer (June and July) along the southeastern Caspian Sea.

layed eggs. Ultimately, it appears that the mimimum size at maturity varies geographically and may even temporally, e.g. fluctuating from year to year depending on temperature and food related individual growths. Beneficial environmental conditions could promote some individuals to grow faster and reproduce successfully at a small size. Such an influence was evaluated in females of the North American natricine Nerodia sipedon, where a change of approx. 4 °C mean air temperature during the growth period would cause a shift of one year in reaching maturity (Brown & Weatherhead 2000). By selecting a juvenile size for individuals of SVL < 30 cm, we are still 5 cm below the size of individuals that showed some morphological indications of sexual maturity in our samples. In the population structure, juveniles contributed approximately one–fourth of the collected snakes. The mature to immature ratio was 3:1 showing significance differences with Mertens’ (1995) results for Natrix natrix (1.1:1). Feaver (1977) and King (1986) calculated this ratio for another watersnake, Nerodia sipedon, respectively, 1.5:1 and 1.3:1. We previously documented 2.5:1 for the related Natrix natrix from the same Iranian stations (Ahmadzadeh et al., submitted). Comparisons within N. tessellata shows that our results of juvenile proportions approach values between 20% and 40% observed in other studies (e.g. Lanka 1978, Lenz & Gruschwitz 1993, Zimmermann & Fachbach 1996). Of course, finding juveniles strongly depends on the season and the microstructure of the habitat, as well as their dispersal. The sex ratio is similar as found in other snake species. Our result showed a normal pattern according Parker & Plummer (1987), indicating a stable population with even numbers in males and females (Pough 2001, Zug 2001, Pleguezuelos & Fahad 2004). N. tessellata from the southeastern Caspian Sea occupy similar habitats as in other regions, by being confined to various aquatic or marshy habitats (Trutnau 1986, Leviton et al. 1992, Filippi et al. 1996, Arnold & Ovenden 2002, Luiselli et al. 2007). The first author found them to predominantly prey on fish, especially Gobiidae, an often preferred prey type (e.g. Gruschwitz et al. 1999), which are abundant in the Gomishan Wetland. In Sari and Ghaz Harbour, it feeds also on cultured fish, similar to accounts in Syria (Shehab et al. 2011). In comparison to the syntopic grass snake Natrix natrix, the home range of a dice snake seems to be relatively small and more closely associated with open water. According to Madsen (1984), grass snakes can occupy a home range of up to 30 ha and an individual snake may cover distances of up to 230 m per day (Nagy & Korsos 1998). Other accounts report even larger home ranges and daily movements of N. natrix (see refs. in Ahmadzadeh, submitted). In comparison, N. tessellata in the current survey were sampled mostly near the lake shores and/or very near the water. This confirms the radiotelemetric results found by Conelli & Nembrini (2007) and Conelli et al. (2011, and refs. therein),

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Tab. 4. Summary of morphological traits in Natrix tessellata (males) from Gomishan Wetland, Ghaz Harbour and Sari stations. The last three columns show results of One–way Variance Analyses (ANOVA) for station comparisons (Gomishan Wetland, n = 25; Ghaz Harbour, n = 13; Sari, n = 7). W (weight), SVL (snout–vent length), LCT (length of complete tail from the anal scale to tip of tail), TL (total length), RTL and LTL (right and left testes lengths).

Trait W (gram) SVL LCT TL LCT/TL LCT/SVL SVL /TL RTL LTL

Gomishan Wetland Mean ± SD 110.6736 ± 37.777 056.5840 ± 07.197 016.1960 ± 02.111 072.7800 ± 09.156 022.2591 ± 00.924 028.6498 ± 01.517 077.7409 ± 00.924 024.2872 ± 07.672 029.4736 ± 07.343

Ghaz Harbour Mean ± SD 060.6938 ± 17.231 043.1308 ± 05.013 012.1923 ± 01.585 055.3231 ± 06.133 022.0743 ± 01.786 028.3882 ± 02.879 077.9257 ± 01.786 018.1677 ± 02.849 014.5062 ± 03.088

Sari Mean ± SD 071.9900 ± 16.015 044.1308 ± 05.013 014.5067 ± 3.6562 057.2429 ± 04.671 022.2099 ± 01.294 028.6185 ± 02.398 077.9459 ± 01.025 017.6914 ± 04.967 015.9886 ± 05.193

df 42 42 42 42 42 42 42 42 42

T 12.87 24.15 22.48 25.42 00.97 00.67 00.13 08.57 00.07

P 0.001 0.001 0.001 0.001 0.90 0.93 0.87 0.07 0.05

Tab. 5. Summary of morphological traits in Natrix tessellata (female) from Gomishan Wetland, Ghaz Harbour and Sari stations. The last three columns show results of One–way Variance Analyses (ANOVA) for station comparisons (Gomishan Wetland, n =10; Ghaz Harbour, n = 20; Sari, n = 14). W (weight), SVL (snout–vent length), LCT (length of complete tail from the anal scale to tip of tail), TL (total length), ROL and LOL (right and left ovarian lengths).

Trait W (gram) SVL LCT TL LCT/TL LCT/SVL SVL /TL ROL LOL

Gomishan Wetland Mean ± SD 240.3190 ± 89.351 072. 1800 ± 07.359 018.5100 ± 02.501 090.6900 ± 09.198 020.4023 ± 01.669 025.6799 ± 02.554 079.5977 ± 01.669 013.2000 ± 04.417 011.9000 ± 07.823

Ghaz Harbour Mean ± SD 168.3519 ± 109.51 058. 6583 ± 15.851 014.4417 ± 04.100 073.1000 ± 19.072 019.9315 ± 02.956 025.0359 ± 04.218 080.068 ± 02.956 006.7500 ± 05.658 004.3333 ± 03.839

indicating that the home range in N. tessellata amounts to an area of approximately 1–2 hectares only. Considering the distribution of length classes according to sex, males had a bimodal and females a trimodal size class distribution (Fig. 3). Although, there were obvious variations in the class distributions of SVL in either sex, they both showed a predominant SVL length class for the ranges of 40–45 and 60–65 cm, respectively. It seems that these variations can be explained by size classes representing cohorts. The class of 40–45 cm likely represents dice snakes in their third year since birth, similar to the size distribution found in Germany (Lenz & Gruschwitz 1993) and Austria (Zimmermann & Fachbach 1996). Specimens in the class of 60–65 cm are more difficult to asign an age, as sexes show different growth trajectories with females probably growing faster than males (Lenz & Gruschwitz 1993). Hence, in this size class we may have males being older than females. Most large females, SVL > 75 cm were more frequently collected in spring than in summer. This may relate to a reproductive motivated seasonal behavior,

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Sari Mean ± SD 172.3309 ± 76.289 059.1500 ± 09.740 013.8864 ± 03.504 073.0364 ± 12.621 018.8120 ± 03.135 023.3263 ± 04.226 081.1875 ± 03.135 009.5455 ± 07.645 006.4545 ± 04.937

df 41 41 41 41 41 41 41 41 41

T 2.33 5.24 6.32 6.07 1.29 1.51 1.29 2.65 5.54

P 0.11 0.00 0.00 0.00 0.28 0.23 0.84 0.83 0.00

as the large females possibly were gravid and moved to sites more distant from the water to thermoregulate and oviposit (Mebert 2011b). Within reptiles, body size is an important life history trait that influences microhabitat type, diet, vulnerability to predators and reproductive success (Blueweiss et al. 1978, Calder 1984). The sexual size dimorphism found in the Iranian Natrix tessellata conforms to similar findings in other populations outside of Iran (e.g. Mebert 1993, Gruschwitz et al. 1999). It is a frequent finding in snakes that females attain larger body size (SVL) than males and conversely males have longer tail and a thicker tail root to store their hemipenis (Shine 2003, Pough 2001, Zug 2001). A longer and more corpulent body in females possibly benefits their storage of embryos (Kaufman & Gibbons 1975). Such sexual dimorphic differences in body proportions are typical in natricine snakes (King 1989, Shine 1993). The lack of significance for the longer tails in males (absolute and not relative size) is based on the lumping of different size classes for that analysis and consequently, the in-

Faraham Ahmadzadeh, Konrad Mebert, Saeedeh Ataei, Elham Rezazadeh, Leili Allah Gohli & Wolfgang Böhme

clusion of large females in our statistical comparison. Else, the sexual dimorphism in relative tail length corresponds well with values for different regions evaluated by Mebert (1993). Using regression equation, we found that the weight of N. tessellata in our study area grows isometrically with the total length in both sexes. These results conform to the broad body size–weight relationship observed in many other snake species (Das 1991, Guyer & Donnelly 1990, Gregory 2004) and is an indicator that this species in doing well in the habitats along the southeastern coast of the Caspian Sea. Most snakes reproduce seasonally with oviposition in the warmest part of the year. Many reproduce by egg–laying, with the number of eggs depending on the body size of the female (Shine 1993, 2003). These general rules account for Natrix tessellata as well. It becomes active by emerging from hibernation from early March into April, and spanning its activity through May until September or November (Latifi 2000, Shcherbak 2003). However, mating was extended and lasted from May to mid of July. In May, after a hibernation period of 7–8 months, females start their vitellogenesis and the subsequent growth of follicles, followed by the size increase of the ovaries (right and left) until they reach their maximum level (as cluster) in summer. This postnuptial pattern follows the reproductive cycle for dice snakes investigated by Bendel (1997, 2001). All collected adult females showed signs of vitellogenesis as they possibly reproduce every year. Unlike the females, it seems male testes activity lasted over the entire season, showing the same pattern of length increase in spring and summer. Hence, the maturation of the spermatozoa in N. tessellata occurs in the late summer or fall, prior to entering hibernation, i.e. the pattern corresponds also to a postnuptial spermatogenesis, as Rutishauser (1996) found for N. tessellata in Switzerland. Our observation showed that in spring males emerge earlier than females, as it was usually reported (see refs. in Gruschwitz et al. 1999). Gomishan Wetland is a natural habitat situated very close to the Caspian Sea with a sparse cover of hydrophilic plants. Ghaz Harbour lies within an agricultural area with many fish farms (Fig. 3). Its environmental features are intermediary to the other two stations. Sari represents a typical Hircanian forestry habitat. The sample sizes of N. tessellata were approximately the same in Gomishan Wetland and Ghaz Harbour, and larger than at Sari station, which might be less suitable due to increased amount of arboreal shading, resulting in cooler temperatures on the ground. On the other hand Gomishan Wetland is also substantially different from the other two stations with a strongly saline environment, almost 10× saltier than seawater. The frequency of N. tessellata in that environment is a clear indication that it can cope well with salt water. At Gomishan Wetland, the largest dice snakes were collected during this study. A richness of fish prey and the open character of the habitat at Gomishan Wetland are certainly favour-

able to promote a large population of N. tessellata. At the other stations, fish farms are probably responsible to support healthy populations of N. tessellata as well. We conclude that N. tessellata thrives at all three stations, and differences in physiochemical water characters among the three stations appear not to be relevant. Finally, the statistically significant morphological differences among N. tessellata over short distances between the three stations in our study correspond to the range of a similar microgeographic variation in N. tessellata from southern Switzerland and northern Italy (Mebert 1993, 1996). These differences posssibly have a local, ecological cause. Acknowledgments This research was supported by Shahid Beheshti University of Tehran (Grant No. 600/3059). Therefore, financial support from the home university is gratefully acknowledged. References Ahmadzadeh, F., Mebert, K., Ataei, S., Hamidi, S., Faghiri, A. & W. Böhme (2011): Some ecological and biological aspects of grass snake, Natrix natrix (Linnaeus, 1758) in the southern coastal area of the Caspian Sea. – (submitted). Arnold, E.N. & D.W. Ovenden (2002): Reptiles and Amphibians of Europe. – Princeton University Press, Princeton. Bagherian, A. & H.G. Kami (2009): Systematic identification of Natrix natrix and Natrix tessellata based on multivariate analysis. – Pajouhesh & Sazandegi 79: 128–134 (in Persian). Bannikov, A.G., Darevsky, I.S., Ishchenko, V.G., Rustamov, A.K. & N.N. Shcherbak (1977): Opredelitel Zemnovodnykh i Presmykayushchikhsya Fauny SSSR (Guide to Amphibians and Reptiles of the USSR Fauna) – Prosveshchenie, Moscow. Bendel, P. (1997): Zur Physiologie, Morphometrie und Populationsökologie der Würfelnatter Natrix tessellata am Alpnachersee. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Bendel, P. (2001): Zur Physiologie der Würfelnatter Natrix tessellata Laurenti 1786 am Alpnachersee. – In: NAGON (Ed.): Amphibien und Reptilien in Unterwalden. – NAGON, Grafenort, Switzerland 2: 162–175. Blueweiss, L., Fox, H., Kudzma, V., Nakashima, D., Peters, R. & S. Sams (1978): Relationships between body size and some life history parameters. – Oecologia 37: 257–272. Brown, G.P. & P.J. Weatherhead (2000): Thermal ecology and sexual size dimorphism in northern water snakes, Nerodia sipedon. – Ecological Monographs 70: 311-330. Calder, W.A. (1984): Size, Function and Life History. – Harvard University Press, Cambridge, MA. . Carlsson, M., Kärvemo, S., Tudor, M., Sloboda, M., Mihalca, A.D., Ghira, I., Bel, L. & D. Modrý (2011): Monitoring a large population of dice snakes at Lake Sinoe in Dobrogea, Romania. – Mertensiella 18: 237–244. Conelli, A.E. & M. Nembrini (2007): Studio radiotelemetrico dell’habitat della Biscia tassellata, Natrix tessellata (Laurenti, 1768) in tre popolazioni del Cantone Ticino (Svizzera). – Bollettino della Società Ticinese di Scienze Naturali 95: 45–54.

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Biological Aspects of Dice Snakes from the SE Caspian Sea, Iran Conelli, A.E., Nembrini, M. & K. Mebert (2011): Different habitat use of dice snakes, Natrix tessellata, among three populations in Ticino Canton, Switzerland. – A radiotelemetry study Mertensiella 18: 100–116. Das, I. (1991): Morphometrics of Eryx conicus (Schneider) at a locality in south India (Squamata: Boidae). – Hamadryad 16(1/2): 21–24. Feaver, P.E. (1977): The demography of a Michigan population of Natrix sipedon with discussions of ophidian growth and reproduction. – Unpubl. dissertation, University of Michigan, Ann Arbor, Michigan. Filippi, E., Capula, M., Luiselli, L. & U. Agrimi (1996): The prey spectrum of the grass snake, Natrix natrix (Linnaeus, 1758), and dice snake, N. tessellata (Laurenti, 1768) in sympatric populations. – Herpetozoa 8(3/4): 155–164. Firouz, E. (2000): A Guide to the Fauna of Iran. – Iran University Press, Tehran, Iran. Göçmen, B., Çiçek, K., Yildiz, M.Z., Atatür, M.K., Dinçaslan, Y.E. & K. Mebert (2011): A preliminary study on the feeding biology of the dice snake, Natrix tessellata, in Turkey. – Mertensiella 18: 365–369. Göçmen, B. & W. Böhme (2002): New evidence for the occurrence of the dice snake, Natrix tessellata (Laurenti, 1968) on Cyprus. – Zoology in the Middle East 27: 29–34. Gregory, P.T. (2004): Sexual dimorphism and allometric size variation in population of grass snakes (Natrix natrix) in southern England. – Journal of Herpetology 38: 231– 240. Gruschwitz, M., Lenz, S., Mebert, K. & V. Lanka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Amphibien und Reptilien Europas Band 3/II Schlangen (Serpentes) II:. – AULA-Verlag, Wiesbaden, Germany. Guicking, D., Herzberg, A. & M. Wink (2004): Population genetics of the dice snake (Natrix tessellata) in Germany: implications for conservation. – Salamandra 40(3/4): 217–234. Guicking, D., Joger, U. & M. Wink (2009): Cryptic diversity in a Eurasian water snake (Natrix tessellata, Serpentes: Colubridae): Evidence from mitochondrial sequence data and nuclear ISSR–PCR fingerprinting. – Organisms Diversity & Evolution 9(3): 201–214. Guyer, C. & M.A. Donnelly (1990): Length-mass relationships among an assemblage of tropical snakes in Costa Rica. – Journal of Tropical Ecology 6: 65–76. Kaufman, G.A. & J.W. Gibbons (1975): Weight–length relationship in thirteen species of snake in the southern United States. – Herpetologica 31: 31–37. Kiabi, H.B., Ghaemi, R.A. & A. Abdoli (1999): Wetland and Riverian Ecosystems of Golestan Province, Department of the Environment, Gorgan, Iran (in Persian). King, R.B. (1986): Population ecology of the Lake Erie water snake, Nerodia sipedon insularum. – Copeia 3: 757–772. King, R.B. (1989): Sexual dimorphism in snake tail length: sexual selection, natural selection, or morphological constraint? – Biological Journal of the Linnean Society 38: 133–154. Lanka, V. (1978): Variabilität und Biologie der Würfelnatter (Natrix tessellata). – Acta Universitatis Carolinae, Biologica 1975– 1976: 167–207. Lenz, S. & M. Gruschwitz (1993): Zur Populationsökologie der Würfelnatter, Natrix t. tessellata (Laurenti 1768) in Deutschland (Reptilia: Serpentes: Colubridae). – Mertensiella 3: 253–268. Latifi, M. (2000): The Snakes of Iran. – Third Edition. – Department of Environment, Tehran, Iran.

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Leviton, A.E., Anderson, S.C., Adler, K. & S.A. Minton (1992): Handbook to Middle East Amphibians and Reptiles. – SSAR, Oxford, Ohio (Contr. to Herpetol. No. 8). Luiselli, L., Capizzi, D., Filippi, E., Anibaldi., C, Rugiero, L. & M. Capula (2007): Comparative diets of three populations of an aquatic snake (Natrix tessellata, Colubridae) from Mediterranean streams with different hydric regimes. – Copeia 2: 426–435. Luiselli, L. & L. Rugiero (2005): Individual reproductive success and clutch size of a population of the semi-aquatic snake Natrix tessellata from central Italy: Are smaller males and larger females advantaged? – Revue d’E´ cologie (Terre Vie) 60: 77–81. Madsen, T. (1984): Movements, home range size and habitat use of radio-tracked grass snakes (Natrix natrix) in Southern Sweden. – Copeia 3: 707–713. Mebert, K. (1993): Untersuchungen zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti, 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Mebert, K. (1996): Comparaison morphologique entre des populations introduites et indigenes de Natrix tessellata de I’Arc Alpin. – Bull. Soc. Herp. France 80: 15–25. Mebert, K. (Ed.) (2011a): The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species. – Mertensiella 18, DGHT, Rheinbach, Germany. Mebert, K. (2011b): Terrestrial dice snakes: how far from water a semiaquatic snake ventures out? – Mertensiella 18: 453–455. Mertens, D. (1995): Population structure and abundance of grass snake, Natrix natrix, in central Germany. – Journal of Herpetology 29(3): 454–456. Nagy, Z.T. & Z. Korsos (1998): Data on movements and thermal biology of grass snake (Natrix natrix) using radiotelemetry. – In: Miaud, C. & R. Guetant (Eds.): Current Studies in Herpetology – Proceedings of the 9th Ordinary General Meeting of the Societas Europaea Herpetologica, (SEH 1998), Le Bourget du Lac., France: 339–343. Parker, W.S. & M.V. Plummer (1987): Population Ecology. – In: Siegel, R.A., Collins, J.T. & S.S. Novak (Eds.): Snakes: Ecology and Evolutionary Biology – Macmillan, New York: 253– 301. Pleguezuelos, J & S. Fahad (2004): Body size, diet and reproductive ecology of Coluber hippocrepis in the Rif (Northern Morocco). – Amphibia–Reptilia 25: 287–302. Pough, F., Andrews, R.M., Cadle, J.E., Crump, M.L., Savitzky, A.H. & K.D. Wells (2001): Herpetology. – Prentice-Hall, New Jersey, USA. Rastegar-Pouyani, N., Kami, H.G., Rajabizadeh, M., Shafiei, S. & S.A. Anderson (2008): Annotated check list of amphibians and reptiles of Iran. – Iranian Journal of Animal Biosystematic (IJAB) 4(1): 43–66. Rutishauser, K. (1996): Zur Physiologie und Populationsöklologie der Würfelnatter Natrix tessellata (Laurenti 1768) am Alpnachersee. – M.S. thesis, University of Zürich, Switzerland. Scott, D.A. (1995): A Directory of Wetlands in the Middle East. – IUCN, the World Conservation Union. Shehab, A.H, Al Masri, A. & Z.S. Amr (2011): The dice snake, Natrix tessellata, in Syria: distribution, trade and conservation. – Mertensiella 18: 388–392. Shine, R. (1993): Sexual dimorphism in snakes. – In: Siegel, R.A. & J.T. Collins (Eds.): Snakes: Ecology and Behavior. – McGraw–Hill, New York: 49–86.

Faraham Ahmadzadeh, Konrad Mebert, Saeedeh Ataei, Elham Rezazadeh, Leili Allah Gohli & Wolfgang Böhme Shine, R. (2003): Reproductive strategies in snakes. – Proc. R. Soc. Lond. B 270: 995–1004. Shcherbak, N.N. (2003): Guide to the Reptiles of the Eastern Palearctic. – Krieger Publishing Company, Florida. Trobisch-Gläßer, A. & D. Trobisch (2001): Ein Mauerblümchen in der Terraristik: Die Würfelnatter Natrix tessellata (Laurenti, 1768). – Elaphe 9(4): 17–24. Trutnau, L. (1986): Non–venomous Snakes. – First English Language Edition, Barron’s Educational Series, Inc., Woodbury, New York. Vlček, P., Najbar, B. & D. Jablonski (2010): First records of the dice snake (Natrix tessellata) from the north-eastern part of the Czech Republic and Poland. – Herpetology Notes 3: 23–26.

Zar, J. H. (1999): Bio Statistical Analysis. – Fourth Edition, Prentice Hall, Upper Saddler River, New Jersey, USA. Zaher, H. (1999): Hemipenial morphology of the South American Xenodontine snakes, with a proposal for a monophyletic Xenodontinae and a reappraisal of colubroid hemipenes. – Bull. Amer. Mus. Nat. Hist. 240: 1–168 Zimmermann, P. & G. Fachbach (1996): Verbreitung und Biologie der Würfelnatter, Natrix tessellata tessellata (Laurenti, 1768) in der Steiermark (Österreich). – Herpetozoa 8(3/4): 99–124. Zug, G.R., Vitt, L.J. & J.P. Caldwell (2001): Herpetology. – Second Edition, Academic Press, San Diego, London.

Authors Faraham Ahmadzadeh*, Department of Biodiversity and Ecosystem Management, Environmental Sciences Research Institute, Shahid Beheshti University G.C., Iran, e–mail: fahmadza@uni–bonn.de; Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland; Saeedeh Ataei, Department of Molecular Genetics, National Institute for Genetic Engineering and Biotechnology, Tehran, Iran; Elham Rezazadeh, Department of Zoology, Faculty of Biological Sciences, Shahid Beheshti University G.C., Iran; Leili Allah Gohli, Department of Environmental Sciences, Faculty of Environment and Energy, Science and Research Campus, Islamic Azad University, Ponak, Tehran, Iran; Wolfgang Böhme, Zoologisches Forschungsmuseum Alexander Koenig (ZFMK), Adenauerallee 160, D–53113 Bonn, Germany. *Current address: Zoologisches Forschungsmuseum Alexander Koenig (ZFMK), Adenauerallee 160, D–53113 Bonn, Germany.

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ISBN 978-3-9812565-4-3

Geographic Variation, Distribution, and Habitat of Natrix tessellata in Iran Mehdi Rajabizadeh, Soheila Javanmardi, Nasrullah Rastegar-Pouyani, Rasoul Karamiani, Masoud Yousefi, Hasan Salehi, Ulrich Joger, Konrad Mebert, Hamidreza Esmaeili, Hossein Parsa, Haji Gholi Kami & Eskandar Rastegar-Pouyani Abstract. The current knowledge of the distribution and habitat of the dice snake, Natrix tessellata, in Iran is based on sampled specimens from 69 localities. In Iran, N. tessellata is widely distributed through humid lowlands to the south of the Caspian Sea, the Alborz and Zagros mountains. Although the species has colonized valleys of large rivers leading through arid plains adjacent to Alborz and Zagros mountains, its occurrence in arid areas of southeastern Iran is currently indicated but still doubtful. In order to study geographic variation of N. tessellata in Iran, a total of 70 specimens, including 41 males and 29 females, were examined. Character variation across latitudes using Spearman test revealed that the ratio of head length to total length in both sexes increases from southern Iran to the north, whereas the number of ventral scales in males decreases significantly (P = 0.01) into the same direction. The results of univariate and multivariate analysis in both sexes separately show that the males from the Fars province (southern Zagros) are significantly different from all other dice snakes in Iran in the ratios of tail length/total length, head length/total length, head length/head width, and number of ventral scales in males, and similarly the females in the ratio of tail length/total length, and the number of subcaudals. We suggest that populations of N. tessellata from the southern Zagros (Fars) are one of the most ancient populations of this species which persisted also during glacial periods. The morphological variations in these populations are the results of long periods of isolation, mixed with influences by environmental factors of the southern Zagros. Key words. Natrix tessellata, habitat, morphological variation, Zagros Mountains, Fars province, Iran. Zusammenfassung. Unsere Kenntnisse über Verbreitung und Habitat der Würfelnatter, Natrix tessellata, in Iran basieren auf Exemplaren von 69 Fundorten. Die Würfelnatter ist im Iran weit verbreitet, vornehmlich in feuchten Tiefländern südlich des Kaspischen Meeres und in den Gebirgsketten des Elbrus und Zagros. Obwohl die Art ihr Areal entlang großer Flüsse in die an Elbrus und Zagros angrenzenden trockenen Steppen besiedelt hatte, ist ihr Vorkommen in Trockengebieten im Südosten des Iran angedeutet, aber fraglich. Um die geographische Variation von N. tessellata im Iran zu analysieren, wurden insgesamt 70 Exemplare von Würfelnattern (41 Männchen und 29 Weibchen) untersucht. Eine Analyse der Merkmalsvariation in Abhängigkeit vom Breitengrad (Spearman-Test) ergab, dass das Verhältnis der Kopflänge zur Gesamtlänge in beiden Geschlechtern vom Südiran zum Nordiran zunimmt und die Zahl der Ventralschuppen bei den Männchen gleichzeitig signifikant (P = 0.01) abnimmt. Die Ergebnisse univariater und multivariater Analysen beider Geschlechter zeigen, dass Männchen der Provinz Fars signifikante Unterschiede zeigen in den Verhältnissen der Kopflänge/Gesamtlänge und der Schwanzlänge/Gesamtlänge, der Kopflänge/ Kopfbreite, der Zahl der Ventralschuppen, während bei den Weibchen entsprechende Unterschiede beim Verhältnis der Schwanzlänge/Gesamtlänge und bei der Zahl der Subcaudalia auftreten. Wir vermuten, dass die Populationen des südlichen Zagrosgebirges (Provinz Fars) zu den ältesten Populationen der Art zählen, welche auch in Eiszeiten nicht ausstarben. Die morphologischen Abweichungen dieser Populationen sind durch lange Isolationszeiten und besondere Umweltfaktoren des südlichen Zagros erklärbar. Schlagwörter. Natrix tessellata, Habitat, morphologische Variation, Zagros Berge, Fars Provinz, Iran

Introduction Natrix tessellata (Laurenti, 1768) is distributed over a wide range, including central and southern Europe (west to Italy and western Germany, excluding Iberia and France), Crete, Cyprus, Anatolia, Syria, Lebanon, Jordan, Israel and northeastern Africa (Egypt, along the Nile) east to Iraq, Iran, Transcaucasia, central Asia, north to Russia up to 54° north latitude, south to northern and eastern Afghanistan and northernmost Pakistan. Finally in the Northeast across Kazakhstan its dis-

tribution ranges into Xinjiang province, northwestern China (Zhao & Adler 1993, Gruschwitz et al. 1999, Szczerbak 2003, Ananjeva et al. 2005, Guicking et al. 2006, Venchi & Sindaco 2006, Mebert 2011a). Only one weakly diverged subspecies, Natrix tessellata heinrothi (Hecht 1930) from the Ukrainian Black Sea island of Ostrov Zmeinyi (Serpilor Island) has been reported yet. Its validity is disputed (Gruschwitz et al. 1999), but new genetic data show more diversity in this taxon across its wide range (Guicking et al. 2006, 2009, Guicking & Joger 2011). Strong genetic differentiation

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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in Iran and other southern populations signals towards the existence of a number of undescribed subspecies. Because of its semi aquatic way of life, the habitat of this species is closely connected to water. In its range close to Iran, the former USSR, it was reported from seashores, riversides and mountains up to 2700 m elevation (Terent’ev & Chernov 1949, Bannikov et al. 1977). Although this species is widely distributed in Iran, little information about geographic variation and habitat of N. tessellata in Iran has been provided until now. Exceptions are the unique books of Latifi (1991, 2000), which provide some information about distribution (based mostly on unprecise locality information) and morphology of this species, and some older literature dealing with the same aspects (Anderson 1963, Leviton et al. 1992, Schmidt 1955). In this work we present the geographic variation of a few commonly applied morphological characters of N. tessellata as well as its distribution and habitat in Iran. Material and Methods Based on extensive field expeditions and examination of collections, a total of 70 Natrix tessellata, including 41 males and 29 females, were collected and examined. The specimens belong to: The Reptiles Collection of the International Center for Science, High Technology and Environmental Sciences Zoological Museum (ICSTZM); Razi University Zoological Museum (RUZM); Zoological Museum of Gorgan University (ZMGU); Collection of Biology department, Shiraz University (CBSU); Eskandar Rastegar-Pouyani personal collection (ERP); Zoological Museum, University of Tehran Collection (ZUTC); Muzeye Mellie Tarikhe Tabiei (MMTT); and the Department of the Environment of Isfahan Province Zoological Collection (DEZC).

Specimens were initially examined for eight metric and 12 meristic characters commonly used in morphological examination of snakes (Thorpe 1975). The measurement of morphometric characters was done using Vernier calipers to the nearest 0.1 mm. Calculating the coefficient of variation (CV) for each character and carrying out a primary Analysis of Variance (ANOVA) revealed that most characters did not contribute to discriminate among potential groups of Iranian N. tessellata. Subsequently, uninformative characters were discarded and the analyses were carried out using four metric and the five most informative meristic characters (Tab. 1). Also six binary and multistate characters were separately analysed. Because patterns of sexual dimorphism in the number of ventral and subcaudal scales had been reported in various populations of N. tessellata (Mebert 1993, Gruschwitz et al. 1999, Mebert 2011b) separate analyses were carried out for males and females. Gender of the specimens was determined through a small incision at the base of tail. To avoid the effect of allometric growth on analyzing morphometric characters, the ratios of metric characters used in the analysis are as follows: TL/ToL x 100, HL/ToL x 100, HL/ HW (see Tab. 1 for definitions). Symmetrical head characters were included as sum of left and right values in the analysis. Since N. tessellata is distributed across a very wide area in Iran, and regarding the limited and scattered number of examined specimens in this study, it was necessary to group the specimens into meaningful OTUs (Operational Taxonomic Unit = geographic group) and check the homogeneity of these OTUs with multivariate statistic parameters before progressing with an analysis of geographic variation (Thorpe. 1984, Wüster et al. 1992). Initially a principal component analysis (PCA) was used to explore the patterns of geographic variation and group the examined specimens into meaning-

Tab. 1. Description of morphological characters examined.

Metric characters

Meristic characters

Binary and multistate characters

SVL (mm) TL (mm) HL (mm) HW (mm) Ven Scd Dor. h Sup (R/L) Inf (R/L) Pre (R/L) Po (R/L) Sub.oc.a (R/L) Sub.oc.p (R/L) T1 (R/L) T2 (R/L) VC

Snout vent length from tip of snout to anterior cloaca Tail length from posterior cloaca to tip of tail Head length from tip of rostrum to end of lower jaw Head width at the widest point, postocular Number of ventrals (Dowling 1951) Number of subcaudal scales on the right side Number of dorsal scales at one head length before cloaca (hind) Number of supralabials Number of infralabials Number of preoculars Number of postoculars Number of anterior suboculars Number of posterior suboculars Number of temporal scales in first row Number of temporal scales in second row Ventral side coloration

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Dice Snake Natrix tessellata in Iran

Fig. 1. Focus of localities of examined specimens of Natrix tessellata in Iran

ful OTUs. Subsequently, to reveal character patterns of different OTUs, descriptive statistical parameters including minimum, maximum, mean and standard error (S.E.) were calculated. Analysis of Variance (ANOVA) was employed to carry out mean comparison of mor-

phological characters between OTUs. Furthermore, seven binary and multistate characters pertaining to head scales numbers and arrangement, and ventral coloration were compared between OTUs using Kruskal-Wallis nonparametric test. Clinal variation between OTUs through latitudes was investigated using Spearman correlation test. All analyses were run by the SPSS (version 15) statistical package. The significance level for all statistical tests was set at P = 0.05. All localities were mapped, including published records, examined museum specimens and 60 localities from personal field tours (Fig. 1); physiography, altitude, vegetation and climate of the localities were documented as well. Latitude of the localities was determined using Google Earth software (2010). Physiography and vegetation of the localities was determined using Land Use Planning Map of Iran (Organization of Forests and Pastures of Iran 1985) and the pertaining climate with the Climate Map of Iran (Khalili 1996). Results Statistical Analysis Construction of Operational Taxonomic Units (OTUs): Principal component analysis (PCA) was run on both sexes separately to investigate patterns of geographic variation and to select informative OTUs for next step

Tab. 2. Factor loadings of the first three principal component (PC) axes on the variables in male specimens. Component Component Matrix(a) Zscore(Tl.Tol.100) Zscore(Hl.Tol.100) Zscore(Hl.Hw) Zscore(Ven) Zscore(Scd) Zscore(Dor. p) Zscore(Sup) Zscore(Inf)

1 .650 .711 .762 -.357 .484 .202 -.160 .150

2 -.467 .437 .273 -.350 -.717 .015 .445 .502

3 .103 .053 -.132 .701 .346 .177 .419 .729

4 -.379 -.086 .285 .251 -.093 .813 -.418 -.044

Tab. 3. Factor loadings of the first three principal component (PC) axes on the variables in female specimens. Component Component Matrix(a) Zscore(Tl.Tol.100) Zscore(Hl.Tol.100) Zscore(Hl.Hw) Zscore(Ven) Zscore(Scd) Zscore(Dor.p) Zscore(Sup) Zscore(Inf)

416

1 .503 -.583 -.341 .641 .810 -.242 .425 .110

2 .320 .673 .713 .257 .149 -.549 .023 .421

3 .719 .164 -.019 -.469 .414 .164 -.527 -.393

4 .132 .136 -.068 -.135 .129 .671 .134 .700

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analysis. Main sampling localities are presented in Figure 1. Results of principal component analyses are shown as scatter plots for both sexes (Tabs. 2, 3, Figs. 2, 3).

Because of relatively limited number of examined specimens, the authors like to put emphasis on obvious differences and leave the more detailed investiga-

Fig. 2. Scatter plot of PCA showing grouped pattern of geographic variation in male Natrix tessellata from Iran

Fig. 3. Scatter plot of PCA showing grouped pattern of geographic variation in female Natrix tessellata from Iran.

417

418

16.85 ± 0.15 15–17

15.85 ± 0.10 15–16

20.36 ± 0.28 19–23

Dor. p

Sup

Inf  

165–179

67.85 ± 1.04 63–74

167–176

173.69 ± 1.09

Ven

20.13 ± 0.30 19–22

16 ± 0.0 16

16.88 ± 0.13 16–17

69.59 ± 0.79 65.91–72

1.87 ± 0.08 1.51–2.19

19.67 ± 0.33 18–20

16 ± 0.0 16

17 ± 0.0 17

63.93 ± 2.21 56–71

169–177

174.67 ± 1.28

1.67 ± 0.07 1.44–1.94

3.56 ± 0.24 3.00–4.57

19.95 ± 0.35 18.58–21.16

6

Fars

19.00 ± 1.0 18–20

16 ± 0.0 16

17 ± 0.0 17

20.24 ± 0.14 20–22

15.94 ± 0.06 15–16

16.82 ± 0.13 15–17

64.44 ± 0.10 55–70

171.71 ± 1.05 165–179

171.00 ± 1.00 170–172 65.00 ± 1.0 64–66

1.86 ± 0.03 1.62–2.12

4.06 ± 0.09 3.50–5.20

20.68 ± 0.29 18.65–22.95

17

N-NE-NW

1.99 ± 0.01 1.98–2.0

4.07 ± 1.18 3.88–4.25

20.02 ± 0.07 19.95–20.09

2

Qom

20.13 ± 0.13 20–21

16 ± 0.0

17 ± 0.0

67 ± 1.61 60–73

167–176

172.50 ± 1.12

1.99 ± 0.07 1.66–2.25

3.94 ± 0.13 3.33–4.61

22.86 ± 0.65 19.23–24.43

8

Males   Kermanshah central Zagros 1

Lar 1

Afus

20.07 ± 0.07 20–21

16 ± 0.0

16.93 ± 0.07 16–17

63.37 ± 0.67 59–67

170–185

175.64 ± 1.08

1.70 ± 0.03 1.52–1.82

3.34 ± 0.10 3.06–4.29

19  

15

17

72

174

1.81

3.71

20  

16

17

65

172

1.29

2.64

19.84 ± 0.26 20.82 20.4 18.56–22.31

14

Fars

tion for future studies. Based on scatter plots of male and female specimens as well as geographic proximity, three OTUs have been selected for N. tessellata in Iran. The first OTU (Northern OTU) contains specimens of Khorasan, Caspian Sea shores and North Western Iran, excluding a single specimen from Lar valley (Fig. 1); the second OTU contains specimens of Kermanshah and central Zagros mountains (OTU of Kermanshah and central Zagros), and the third OTU contains specimens of southern Zagros mountains which all originate from the Fars province (OTU of Fars). Detailed checking of each point in the scatter plot of male specimens shows

Scd

171.63 ± 1.12

1.78 ± 0.09 0.79–2.14

Hl.Hw

3.78 ± 0.08 3.43–3.99

3.95 ± 0.12 2.92–4.55

Hl.Totl.100

21.96 ± 0.39 19.98–23.57

8

21.47 ± 0.25 19.73–22.70

13

N-NE-NW

Tl.Tol.100

N

OTU

Females   Kermanshah central Zagros

Tab. 4. Descriptive statistic (mean, S.E., range) of morphological characters of N. tessellata in Iran partitioned into geographic regions (OTUs). Definition of characters in Table 1.

Dice Snake Natrix tessellata in Iran

that two males were excluded from any OTU, one from Lar valley in central Alborz and one from Afus in high central Zagros. They will be discussed separately. Although males of Kermanshah are more associated to the Northern OTU, the scatter plot of females and their geographic proximity puts them closer to the central Zagros specimens. Hence, all Kermanshah specimens are grouped in the central OTU, combining Kermanshah and central Zagros. With less certainty, the above OTUs can be distinguished in the scatter plot of female specimens too. Two females from Qom should be placed in a separate OTU

Mehdi Rajabizadeh et al.

Fig. 4. Significantly different characters between male-OTUs plus Lar and Afus specimens. OTU-labels from left to right are: N (Northern), K (Kermanshah-central Zagros), F (Fars), L (Lar), A (Afus).

because they are from geographically intermediate sites. Detailed checking of each point in the scatter plot of females revealed that some individuals have been plotted far from other specimens of the same locality which can be explained by individual difference, i.e. as intra population variation, and those individuals are not regarded to represent a separate OTU. Descriptive parameters of each OTU are presented in Table 4. Comparative analysis of means: Detailed checking of significant differences of three OTUs using Analysis of Variance (ANOVA) with LSD post hoc reveals that (a) in males: tail length/total length x 100 (Tl.Tol.100) is significantly different between Kermanshah-central Zagros-OTU and the other two OTUs, head length/total length x 100 (Hl.Tol.100) is significantly different between Fars-OTU and the other OTUs, head length/head width (Hl.Hw) is significantly different among all OTUs and finally the number of ventral scales (Ven) is significantly different between Fars-OTU and Kermanshahcentral Zagros OTU (Tab. 5). (b) In females: tail length/ total length x 100 (Tl.Tol.100) and number of subcaudal scales (Scd) is significantly different between FarsOTU and the other OTUs (Tab. 5). Significantly differ-

ent characters between OTUs are presented schematically in Figures 4 and 5. Nonparametric analysis: Totally six binary and multistate characters examined between different OTUs were analyzed using a Kruskal-Wallis nonparametric test. The results of this analysis are presented in Table 6. Only one character, the arrangement of anterior subocular scales, approached a significant difference between OTUs. Clinal variation through latitudes: To study clinal variation of morphological characters by latitude, all the examined specimens were classified based on nearest latitude into three clusters: near to 36 30’ N latitude, near to 33 30’ N latitude and near to 29 30’ N latitude (Fig. 1). Based on this classification clinal variation of the morphological characters of the specimens were tested using Spearman correlation test. Results of Spearman correlation tests are presented in Table 7. Significant characters are shown schematically in Figures 6 and 7. Grouping our scattered specimens around three latitudes and investigating increase or decrease of quantitative character states through these latitudes have produced clinal variation in four characters. In summary these analy-

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Dice Snake Natrix tessellata in Iran

Tab. 5. Result of Analysis of variance (ANOVA) between North-Northwest-Northeast OTU, Kermanshah-central Zagros OTU and Fars OTU in male and female specimens. For a better resolution, only main OTUs were included and areas with only one or two specimens, e.g. Qom, Lar and Afus, were excluded. ANOVA Female F 8.24

Sig. 0.05

Mean Square 6.09 0.77

Male F 7.88

Sig. 0.05

1.83 0.97

1.88

0.17

8.35 0.51

16.36

0.05

Zscore(Hl.Hw)

0.95 1.04

0.91

0.42

6.63 0.52

12.84

0.05

Zscore(Ven)

1.42 1.01

1.41

0.26

3.52 0.91

3.85

0.03

Zscore(Scd)

3.31 0.86

3.87

0.04

2.19 0.89

2.45

0.10

Zscore(Dor.p)

0.30 1.14

0.26

0.77

0.68 1.07

0.64

0.54

Zscore(Sup)

1.20 1.06

1.13

0.34

0.35 0.55

0.63

0.54

Zscore(Inf)

1.03 0.89

1.16

0.33

0.51 0.91

0.56

0.57

Character Zscore(Tl.Tol.100)

Mean Square 5.27 0.64

Zscore(Hl.Tol.100)

ses revealed that from north (latitude more than 33°) to south the ratios of tail length/total length (TL/Tol x 100) and head length/head width (HL/HW) increase to reach the highest values (i.e. relative longer tails, relative longer heads) in specimens from mid-latitudes, and from there they decrease drastically to the lowest values in specimens from southern latitudes (Fars province). Consistently, the ratio of head length/total length (HL/Tol x 100) decreases from north to south regularly which indicates that specimens from Fars have a shorter tail and a shorter head (with regard to the SVL), while towards the north these measurements increase. The number of ventrals decreases in N. tessellata from Fars towards more northern latitudes. This cline is especially pronounced in males (Fig. 6), but also in females from this study (Fig. 7). Distribution All known localities of Natrix tessellata are shown in Figure 8. The localities originate from field observations by the senior author, localities of examined specimens in collections, reviewing literature, especially Latifi

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(1991, 2000), and personal communications with other herpetologists in Iran. The southernmost known localities of N. tessellata in Iran reach up to northern and central Fars province. Efforts of listed authors for finding any locality of this snake in the south of Fars province or in Bushehr and Bandar Abbas provinces in the vicinity of the Persian Gulf yielded no positive results, hence, its distribution in the southern branches of Zagros Mountains remains unclear. The presence of this species in southeastern Iran is doubtful, even though Latifi (2000) reported N. tessellata from Sistan and Baluchestan provinces without exact localities. On the other hand, the senior author has received unconfirmed reports of the presence of N. tessellata in the Bahr Aseman Mountains in Kerman province which need further confirmation. In summary, the distribution of N. tessellata in Iran is restricted to the Alborz and Azarbaijan Mountains, as well as the northern, central and western parts of the Zagros Mountains and adjacent areas. The species is widely distributed in the plains of northern Alborz that drain into the Caspian Sea. It colonized arid plains in the east of the Caspian Sea and west of the Zagros Mountains but it occurs only along a few freshwater rivers in the central plains of Iran.

Mehdi Rajabizadeh et al.

Fig. 5. Significantly different characters between female-OTUs plus Qom specimens.

Fig. 6. Characters that vary significantly by latitudes in male Natrix tessellata (Spearman Correlation tests).

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Dice Snake Natrix tessellata in Iran

Tab. 6. Comparison of binary and multistate characters, and ventral coloration between three main OTUs. Pre (Preocular scales): bilaterally one Pre (0), bilaterally distinct, one and two Pre, respectively (1), bilaterally two Pre (2), bilaterally distinct, two and three Pre, respectively (3); Po (Postocular scales): bilaterally 2 Po (0), bilaterally distinct, two and three Po, respectively (1), bilaterally three Po (2); Sub.oc.a (Anterior subocular scale): without Sub.oc.a (0), unilaterally one Sub.oc.a (1), bilaterally one scale (2); Sub.oc.p (Posterior subocular scale): without Sub.oc.p (0), unilaterally one Sub.oc.p (1), bilaterally one Sub.oc.p (2), bilaterally distinct, two and one Sub.oc.p, respectively (3), bilaterally two Sub.oc.p (4); T2 (Temporal scales in second row): bilaterally one T2 (0), bilaterally distinct, two and one T2, respectively (1), bilaterally two T2 (2), bilaterally distinct, two and three T2, respectively (3); VC (Venter coloration): typical ventral coloration (0), tendency to unicolor ventral coloration (1).

N-NE-NW Pre Po Sub.oc.a Sub.oc.p T2 VC

0,1,2,3 0,1,2 0,1,2 0,1,2,3,4 1,2,3 0

Male Kermanshahcentral Zagros 2 2 0,1,2 2 2 0

Fars 2 2 0,1,2 0,1,2 1,2 0,1

Asymp. Sig. 0.80 0.13 0.59 0.32 0.15 0.14

N-NENW 0,2 0,2 0,1,2 0,1,2 0,2 0

Female Kermanshahcentral Zagros 2 2 0,2 2 2,3 0

Fars 2 2 0,2 0,1,2 1,2 0,1

Asymp. Sig. 0.58 0.33 0.07 0.19 0.24 0.17

Tab. 7. Spearman correlation tests through latitudes between male and female of Natrix tessellata in Iran. Male

Female

Zscore(Tl.Tol.100)

Correlation Coefficient Sig. (1-tailed)

0.28* 0.04

Correlation Coefficient Sig. (1-tailed)

0.27 0.08

Zscore(Hl.Tol.100)

Correlation Coefficient Sig. (1-tailed)

0.60** 0.00

Correlation Coefficient Sig. (1-tailed)

0.38* 0.02

Zscore(Hl.Hw)

Correlation Coefficient Sig. (1-tailed)

0.42** 0.00

Correlation Coefficient Sig. (1-tailed)

0.28 0.07

Zscore(Ven)

Correlation Coefficient Sig. (1-tailed)

-0.33* 0.02

Correlation Coefficient Sig. (1-tailed)

0.04 0.43

Zscore(Scd)

Correlation Coefficient Sig. (1-tailed)

0.20 0.10

Correlation Coefficient Sig. (1-tailed)

0.10 0.31

Zscore(Dor.p)

Correlation Coefficient Sig. (1-tailed)

-0.09 0.30

Correlation Coefficient Sig. (1-tailed)

-0.05 0.40

Zscore(Sup)

Correlation Coefficient Sig. (1-tailed)

-0.24 0.07

Correlation Coefficient Sig. (1-tailed)

-0.25 0.10

0.06 0.36

Correlation Coefficient Sig. (1-tailed)

0.16 0.20

Zscore(Inf) * **

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Correlation Coefficient Sig. (1-tailed) Correlation is significant at the 0.05 level (1-tailed). Correlation is significant at the 0.01 level (1-tailed).

Mehdi Rajabizadeh et al.

Habitat

Fig. 7. Characters that vary significantly by latitudes in female Natrix tessellata (Spearman Correlation tests).

To assess the habitat of Natrix tessellata in Iran, elevation, vegetation and climate of all the noted localities in Figure 8 were checked carefully and summarized. As a result, the habitat of N. tessellata in Iran can be classified into the following clusters: (1) Lowlands and seashores of Caspian Sea: This area contains plains with elevation between 0–100 m and is restricted between seashore and mountains. The climate is “Wet Caspian” and the original vegetation has mostly been altered into rice plantations. The species is abundant here and due to abundance of surface water and associated prey, it is observed widely in this lowland. (2) High elevated plains and mountainous habitat: This is the predominant habitat of N. tessellata in Iran. It starts at an elevation of 100 m on the northern slopes of the Alborz Mountains. However, in the southern Alborz Mountains, in the Azarbaijan and the Zagros

Fig. 8. All known localities of Natrix tessellata in Iran. Squares represent localities from where specimens have been examined and used in the analysis. Triangles indicate localities reported in museum documents, literatures or reliable personal communications with herpetologists from Iran. Question marks indicate the two localities of N. tessellata in southeastern Iran, mentioned by Latifi (1991, 2000), that require confirmation.

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Dice Snake Natrix tessellata in Iran

mountains, equivalent lowland habitats are replaced by high mountain plains and mountains at about 1000 m elevation, as these mountains are open to the elevated central Iranian plains. In this habitat the species is observed normally near numerous streams and some rivers, artificial dams, pools and springs. Most of the habitats in the Alborz Mountains consist of mountain slopes and valleys with seasonal Mediterranean pasture vegetation fed by spring rains. In the Azarbaijan and Zagros mountains the species also occurs on high elevation plains with low to high density pasture vegetation and mountain slopes with pasture vegetation, which in the Azarbaijan Mountains changes to forests of Juniperus at higher elevations. Farther south, in the Zagros Mountains, the pastures change to Pistacia and Amygdalus vegetation with a Mediterranean climate without spring rain. The maximum elevation records for N. tessellata in this habitat type is from the Lar Valley in the Alborz Mountains, where we found this species inhabiting a lake at the bottom of the valley (2500 m a.s.l., see Fig. 9) and also a mountain brook in a side valley up to 2700 m (Figs. 10, 11). A comparable high locality with N. tessellata at 2500–2700 m a.s.l. is at the bottom of a mountain river valley in the Afus region of the Zagros

Fig. 9. Lar Valley in the Central Alborz Mountains. Photo: M. Ghasemi

Mountains. This locality is a small-artificial reservoir lake with a dam. Dice snakes are abundant in the lake and man made boulders around it. The lake is located at 2544 m a.s.l. and suitable habitat at another pond at 2635 m and mountain brooks higher up to 2700 m. Surrounding mountains rise up to 4000 m and are the type locality of Iranolacerta zagrosica (Rastgar-Pouyani & Nilson 1998) and Iranolacerta brandtii esfahanica (Nilson et al 2003). Both areas are characterized by a cold mountainous climate and by a subalpine steppe with Astragalus sp. as the typical vegetation. Rivers in dry plains: N. tessellata can be found in dry plains along rivers in the eastern area of the Caspian Sea, western Zagros plains and central Iranian plains.. East of the Caspian Sea this species has been recorded from the Atrak River, and in dry plains around Alagol salt lake at elevation of 35 m. In western Zagros N. tessellata occurs along large rivers like Dez and Karun, which originate from the Zagros Mountains, and flow deeply into Khuzestan plains characterized by a hot dry desert climate to finally approach the Persian Gulf. The species has been recorded from western Zagros plains to around Ahvaz city at 15 m a.s.l. In contrast, the species could not extend its distribution into the arid plains of central Iran, which lack large rivers, and has been recorded only from the margins of the central Iranian plains. Along the eastern versant of the Zagros Mountains, the species has been recorded until the end of Zayande rud (river) in the Varzane area, just before the river reaches the Gavkhuni Lagoon where it disappears in the desert. There, N. tessellata has been recorded at an elevation of 1400 m, in an area surrounded by desert and only 1 km from a first sand dune. The river bed is flanked mainly by Tamaryx vegetation. Nearby sand dunes exhibit typical desert halophyte vegetation. South of Alborz, Latifi (1991) recorded a specimen from Varamin, just south of Tehran at the northern margin of the central Iranian plain at an elevation of 900 m. Both these marginal localities of N. tessellata have a semidesert climate. All the rivers which run from Alborz and Zagros mountains into the central Iranian plain become dry or very salty outside the mountain valleys and it seems that these are the limiting factors for a farther expansion of N. tessellata into the dry plains. The species has not been reported from coastal plain of the Persian Gulf in the Khuzestan province yet. Discussion Distribution of Natrix tessellata in Iran

Fig. 10. Locality in the Lar Valley, Central Alborz Mountains, where two N. tessellata were found at 2700 m a.s.l.. Photo: Benny Trapp

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Even after detailed investigations in the course of this review, there is no published report of Natrix tessellata from the plains along the Persian Gulf in southern Iran. Concerning the localities of the species in southeastern Iran, localities in the Kerman province need confirmation, as well as the localities noted by Latifi (2000) in Sistan and Baluchestan provinces, because most of those records originate from snake hunters. Although, Lati-

Mehdi Rajabizadeh et al.

Fig. 11. Natrix tessellata from the Lar Valley, Central Alborz Mountains, feigning death and producing a deterring autoheamorragy. Photo: Benny Trapp

fi (2000) presented some exact localities for snakes of Iran, he usually didn’t trust in the statements of snake hunters. Consequently, most of his published localities are not precise and often the province of the sampled specimens was only reported and more information is not available. Hence, it remains unclear, whether specimens of N. tessellata from Sistan and Baluchestan provinces examined by Latifi originate from those provinces or were transported there for commercial issues. For example in 2008, during a project of the Department of the Environment of Kerman province, the senior author examined a specimen of the related Natrix natrix collected by an amateur herpetologist from a palm garden at Bam City (29 06’ N, 58 21’ E), a city adjacent to the Lut Desert. Until further findings, we presume that this specimen was released there by humans, hence, is not autochthonous. This leaves the localities in the Fars province as the confirmed southern range limit of N. tessellata in Iran, which represent also the southernmost known distribution point of the species in its whole global range. Habitat of Natrix tessellata in Iran Attention to localities of this species in northern Africa (Egypt) reveals that it is restricted to the large water

course (Nile River), immediate tributaries and its delta (Baha el Din 2011). In contrast, the localities in Fars are related to rivers which run through high elevation plains and mountainous areas with natural lakes. The vegetation ranges from pasture to forest and the climate from Mediterranean to montane. For example, the elevation of the Shiraz plain reaches up to 1400 m and Arjan Lake is close to 2000 m a.s.l. An important aspect of Natrix tessellata in Iran is its habitat in the mountains. Although this species uses large rivers to even penetrate into arid plains, its occurrence in high elevated mountain rivers is a natural phenomenon which can lead to local isolation of populations due to climatic fluctuations. In this study the most elevated localities, recorded in Afus region in central Zagros (2700 m) and Lar valley in central Alborz (2700 m) (Fig. 9), yielded specimens that show morphological differences to N. tessellata in lower areas. A specimen with relatively unicolor light venter, an adult female (CBSU C 881) was collected by the senior author and a team from Shiraz University Zoological Department, lead by Dr. H.R. Esmaeili, in Ghale Narenji (29 29’N, 51 44’E), connected to Parishan Lake at about 900 m elevation (Fig. 12). It seems that this phenotype (tendency towards a unicolored venter) has a low frequency in some population of N. tessellata in Fars province. This has not been reported ever from other

425

Dice Snake Natrix tessellata in Iran

Fig. 12. Parishan Lake in Fars province. Photo: Mehdi Rajabizadeh

populations of this snake in Iran, though it is known from populations throughout its range (Mebert 1993, 2011a). Geographic Variation of Natrix tessellata in Iran Although in this article we tried to examine as many specimens of N. tessellata as possible, still the examined material is not sufficient for a complete analysis of geographic variation of this species in Iran. Hence, the conclusions are to be seen as preliminary, yet related to the entire distribution of this species in the country. Geographic variations have been studied with two approaches, describing clinal variations and finding isolated populations. ANOVA shows that male specimens of southern Zagros (Fars) are significantly different in means of four characters from specimens farther north, Alborz and central Zagros. This analysis shows that Fars specimens have a higher number of ventrals (ven) and shorter tail (TL/Tol x 100) than dice snakes from Kermanshah-central Zagros specimens and exhibit a significantly shorter head (HL/HW) and shorter tail relative to the total length (HL/Tol x100) than snakes from both Kermanshah-central Zagros and northern Iran. Fars-females have a significantly lower number of subcaudals and a shorter tail with regard to the total length (Tl/Tol. x 100) than females of other populations in Iran. That the group of N. tessellata in the southern Zagros Mountains (Fars prov.) is distinct from specimens of the rest of Zagros and Alborz moutains receives support from the multivariate analysis of PCA. However, it is known that characters concerning head and body proportions, number of ventral and subcaudal scales vary greatly across regions in N. tessellata (Mebert 1993, Gruschwitz et al. 1999, Brecko et al. 2011, Mebert 2011a) and are even subject to a pronounced microgeographic variation across 100–300 km (Mebert 1996, Mebert 2011c). Underlying mechanisms for the clinal variation of the head length in Iranian N. tessellata are not known.

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Fig. 13. A male Natrix tessellata from Lar valley in the central Alborz Mountains. Photo: Mehdi Rajabizadeh

Geographic variation of head length in N. tessellata has been reported before (Mebert 1993), and was found to be significant for both sexes even across small distances of approximately 30–40 km in southern Switzerland (Mebert 1996). Moreover, Brecko et al. (2011) found differences in head size/shape between frog and fish eating specimens (populations), viewing those diet differences as a potential factor governing geographic variation. Their analysis included many specimens from Iran, but without exact localities. Fish feeding N. tessellata had significantly narrower (relative longer) heads than dice snakes consuming frogs. They stated that it was not clear, whether the observed differences in head shape have a genetic basis or result from phenotypic plasticity. The extensive geographic variation in a number of morphological characters shown in these studies and those found in our study within Iran suggest a more complex pattern, and underlying causative factors. It remains to be seen whether a future analysis with a larger data set can corroborate such geographic variation for N. tessellata in Iran and find corresponding correlations with external factors.

Mehdi Rajabizadeh et al.

Isolated Populations: In the scatter plot of the PCA analysis for the males (Fig. 2), a specimen from Lar valley and one from Afus region take an outlier position with a large Euclidean distance from other populations. At first glance this result indicates the presence of isolated populations, especially in the understanding that these two specimens belong to the two most elevated localities of Natrix tessellata in Iran (up to 2700 m). Detailed morphological examination shows that the Afus specimen is quite unique in dimensions of its head. It has a very short and wide head (low HL/HW of 1.29 in the Afus specimen vs. 1.99 in Kermanshah-central Zagros specimens) and correspondingly low HL/Tol value of 2.94 vs. 3.64. Because these differences are not supported by meristic characters, it is more likely that this is an individual difference which may be caused by innate or external factors, such as a damaged head bone, a disease, or a distortion of the head after preservation. The other distinct N. tessellata is a single male from Lar valley (Fig. 13). This specimen is different from adjacent specimens in the Northern OTU mainly in the number of subcaudals (72 in Lar specimen against a mean of 64.4 in northern specimens) and mean percent of tail length/total length (TL/Tol x 100) (20.82 against 20.68), which indicates that this specimen exhibits a rather low number of subcaudals and correspondingly shorter tail than other male N. tessellata from the Alborz Mountains and Caspian Sea shores. Similar to the specimen from the Afus region, the Lar valley is a highly elevated mountain area in central Alborz with a comparatively cold climate and subalpine vegetation where the unique mountain viper Montivipera latifii has also evolved (its type locality and center of its limited distribution). Although these data come from only one specimen from Lar valley, they indicate that a morphologically distinct population of N. tessellata occurs in Lar valley. However, the difference of approximately 8 subcaudals to the mean of 64.4 subcaudals of the Northern OTU is within the intrapopulational range of normally 10–15 subcaudals (max. range to even 26 subcaudals), as was found in various populations of N. tessellata in western Europe (Mebert 1993). Hence, we believe that for a reliable conclusion on the status and a complete description of the Lar valley population of N. tessellata, further specimens and data are needed. Taxonomic Conclusions: From the taxonomic point of view, the distinguishable clinal variation in morphometric and meristic characters of Natrix tessellata in Iran through latitudes from north to south suggests to debate a potential subspecific differentiation. Detailed examination of the differences between the southern Zagros population (Fars) of N. tessellata and the Alborz and northern Zagros populations shows that this difference is not so clear cut to allow us to treat the Fars population as a separate taxon at this time. But there are significant differences in populations of N. tessellata between Fars province and other populations of the species in the country (see above). A more detailed study, including

a molecular comparison of populations, should be accomplished to clarify whether the Fars population deserves special taxonomic status. Guicking et al (2006, 2009) and Guicking & Joger (2011) in their study about the phylogeny and phylogeography of the genus Natrix and its species included only limited DNA of Iranian specimens, from Kermanshah province and Lar Valley. These were highly different from dice snakes outside Iran but closely related to each other. This study brings further evidence for the distinct status of N. tessellata from Iran. However, we feel not confident to draw any taxonomic conclusions before further molecular studies shed light on the phylogeography of this species in Iran. However, from a global perspective, the Iranian N. tessellata studied by Guicking et al. show such a high genetic distance from all other N. tessellata populations that even the recognition of a separate species of Iranian Dice snakes may be justified. Biogeographic aspect: In order to explain the role of ecological and environmental factors which caused differentiation of the southern Zagros populations of Natrix tessellata from the Alborz and rest of the Zagros populations, we should focus primarily on the biogeographical and geological history of the southern Zagros region. Guicking et al. (2006, 2009) and Guicking & Joger (2011) concluded that N. tessellata evolved in southwest Asia and this evolution may have occurred during at least 5–6 Mya as a result of the varying and fluctuating environmental conditions associated with the deterioration of the climate at the end of the Miocene. Special focus on climate change phenomena in the Iranian plateau shows that during the glaciation period, the south of the Iranian plateau played an important role as a large refugial area for northern reptile species (Rastegar-Pouyani 2005, 2006). Recent studies show that although northern Iran was affected by glacier formation and temperature was significantly reduced during periods of glaciation, such effects of severely cold climate produced a less significant temperature reduction in southern Iran, including southern Zagros (Klinsley 2009, Ahmadi & Feiznia 2006). Therefore, we suggest that numerous taxa of the herpetofauna from northern regions found a refugial area on the Iranian Plateau during periods of glaciation. After the end of each glaciation period, reptile species in the southern refugia moved again to the north and colonized vacant niches. However, our findings of significant morphological differences between northern and southern (Fars) Iranian N. tessellata preclude any conclusion that the glacial refugia of the northern populations were as far south as Fars province. In reference to Guicking et al. (2006, 2009),we suggest that populations of N. tessellata in southern Zagros (Fars) represent one of the oldest populations of this species which did not go extinct during periods of glaciation and its morphological variations present today is the result from a long time of isolation affected by envi-

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ronmental factors of the southern Zagros. In contrast, the morphological similarity among the northern populations is the result of a recent and fast dispersal after the last glaciation. Our preliminary data do not prove that Iranian N. tessellata are a monophyletic group with respect to nonIranian dice snakes. It may turn out that southern Zagros (Fars) populations belong to an even older branch then those Iranian populations which have already been studied with molecular methods. Hence, it is paramount that further phylogenetic studies also include genetic data from populations of N. tessellata from the southern Zagros (Fars province), which may shed a new light on the taxonomy and biogeography of this species. Acknowledgements We are grateful to our friends and colleagues, Azad Teimuri, Ali Gholamhoseini, Mohadeseh Afroosheh, Alireza Motesharei, Hamze Oraei, Meisam Ghasemi, Meisam Mashayekhi, Edris Paya, Benny Trapp, Maya Henggeler, Alexander Westerström and Sulmaz Rafiei. References Ahmadi, H. & S. Feiznia (2006): Quaternary Formations (Theoretical and Applied Principles in Natural Resources). Second Ed. – University of Tehran Press, Tehran. Iran: 256–318. Ananjeva, N.B., Orlov, N.L., Khalikov, R.G. Darevsky, I.S., Ryabov, S.A. & A.V. Barabanov (2004): Colored Atlas of the Reptiles of the North Eurasia (taxonomic diversity, distribution, conservation status). – Zoological Institute of the Russian Academy of Sciences, Saint-Petersburg, Russia (in Russian with English Preface). Anderson, S.C. (1963): Amphibians and Reptiles from Iran. – Proceedings of the California Academy of Science, ser. 4, 31(16): 417–498. Baha el Din, S. (2011): On the distribution and recent range extension of Natrix tessellata in Egypt. – Mertensiella 18: 401– 402. Bannikov, A.G., Darewskij, I.S., Ishenko, V.G. & N.N. Sczerbak (1977): Opredelitelj zemnowodrych i presmykajuscichsja fauny SSSR [Identification of Amphibians and Reptiles of the USSR]. – Moscow: Proswesenije. Brecko, J., Vervust, B., Herrel, A. & R. Van Damme (2011): Head morphology and diet in the dice snake (Natrix tessellata). – Mertensiella 18: 20–29. Dowling, H.G. (1951): A proposed standard system of counting ventrals in snakes. – British Journal of Herpetology 1: 97–99. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) - Würfelnatter. – In: Böhme,W. (Ed.), Handbuch der Reptilien und Amphibien Europas, Band 3/IIA, Schlangen (Serpentes) II. – Aula-Verlag, Wiesbaden: 581–644. Guicking, D. & U. Joger (2011): A range-wide molecular phylogeography of Natrix tessellata. – Mertensiella 18: 1–10. Guicking, D., Lawson, R., Joger, U. & M. Wink (2006): Evolution and phylogeny of the genus Natrix (Serpentes: Colubridae). – Biological Journal of the Linnean Society 87: 127–143.

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Guicking, D., Joger, U. & M. Wink (2009): Cryptic diversity in a Eurasian water snake (Natrix tessellata, Serpentes: Colubridae): Evidence from mitochondrial sequence data and nuclear ISSR-PCR fingerprinting. – Organisms, Diversity & Evolution 9: 201–214. Hecht, G. (1930): Systematik, Ausbreitungsgeschichte und Ökologie der europäischen Arten der Gattung Tropidonotus (Kuhl) H. Boie. – Mitteilungen aus dem Zoologischen Museum in Berlin 16: 244–393. Khalili, A. (1996): Classification of Climates of Iran Using De Martens System. 1:100.000. – Jamab Consulting Company, Iran. Klinsley, D.B. (2009): The deserts of Iran and geomorphological features and its paleoclimatology. Second Ed. – Translated by A. Pashaei – National Geographic Organisation Publication, Tehran, Iran: 299–305. Latifi, M. (1991): The Snakes of Iran. - Contrib. Herpetol. Vol. 7, Soc. for the Study of Amphibian and Reptiles, Athens (Ohio, USA) [Translation]. Latifi, M. (2000): The Snakes of Iran. Third Ed. – Department of the Environment. Tehran. Laurenti, J.N. (1768): Specimen Medium Exhibens Synopsis Reptilium - Vienna, 1–214, pls. i–v. Leviton, A.E., Anderson, S.C., Adler, K. & S.A. Minton (1992): Handbook to Middle East Amphibians and Reptiles. – In: Contrib. Herpetol.,Vol. 8, Soc. for the Study of Amphibians and Reptiles, Athens (Ohio, USA). Mebert, K. (1993): Untersuchungen zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti, 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoological Museum, University of Zürich, Switzerland. Mebert, K. (1996): Comparaison morphologique entre des populations introduites et indigenes de Natrix tessellata de I’Arc Alpin. – Bull. Soc. Herp. France 80: 15–25. Mebert, K. (2011a): Geographic variation of morphological characters in the dice snake Natrix tessellata (Laurenti 1768). – Mertensiella 18: 11–19. Mebert, K. (2011b): Sexual dimorphism in the dice snake (Natrix tessellata). – Mertensiella 18: 94–99. Mebert, K. (2011c): Introduced and indigenous populations of the dice snake (Natrix tessellata) in the Central Alps. – Microgeographic variation and effect of inbreeding. – Mertensiella 18: 71–79. Nilson, G., Rastegar-Pouyani, N., Rastegar-Pouyani, E. & C. Andren (2003): Lacertas of the south and central Zagros Mountains, Iran, with description of two new taxa. – Russian Journal of Herpetology 10: 11–24. Rastegar-Pouyani, N. (2005): A multivariate analysis of geographic variation in the Trapelus agilis complex (Sauria: Agamidae) - Amphibia-Reptilia 26: 159–173. Rastegar-Pouyani, N. (2006): Systematics of the genus Asaccus (Sauria: Gekkonidae) on the Zagros Mountains, Iran. – Proceedings of the 13th General Meeting of the Societas Europaea Herpetologica: 117–121. Rastegar-Pouyani, N. & G. Nilson (1998): A new species of Lacerta (Sauria: Lacertidae) from the Zagros Mountains, Esfahan province, West-Central Iran. Proceedings of the California Academy of Sciences 50: 267–277. Schmidt, K.P. (1955): Amphibians and Reptiles from Iran. – Videnskabelige Meddelesen fra Dansk Naturhistorist Forening 117: 193–207. Szczerbak, N. (2003): Guide to the Reptiles of the Eastern Palearctic. – Krieger Publishing Company, Malabar, USA.

Mehdi Rajabizadeh et al. Terent’ev, P.V. & S.A. Chernov (1949): Key to Amphibian and Reptiles. Third Ed. – Israel Program for Scientific Translation Ltd, Jerusalem. Thorpe, R.S. (1975): Quantitative handling of characters useful in snake systematics with particular reference to intraspecific variation in the ringed snake Natrix natrix (L.) - Biological Journal of the Linnaean Society 7: 27–43. Thorpe, R.S. (1984): Multivariate patterns of geographic variation between the island and mainland populations of the eastern grass snake (Natrix natrix natrix). – Journal of Zoology (London) 204: 551–561.

Venchi, A. & R. Sindaco (2006): Annotated checklist of the reptiles of the Mediterranean countries, with keys to species identification. Part 2 -Snakes (Reptilia, Serpentes). – Annali del Museo Civico di Storia Naturale “G. Doria”, Genova, XCVIII: 259–364. Wüster, W., Otsuka, S., Malhotra, A. & R.S. Thorpe (1992): Population systematics of Russell’s viper: a multivariate study – Biological Journal of the Linnean Society 47: 97–113. Zhao, E. & K. Adler (1993): Herpetology of China. – SSAR, Oxford/Ohio.

Authors Mehdi Rajabizadeh, Department of Biodiversity, Institute of Environmental Science, International Center for Science, High Technology and Environmental Science, Kerman, Iran, e-mail: [email protected]; Soheila Javanmardi, Hamidreza Esmaeili, Department of Biology, College of Sciences, Shiraz University, Shiraz, Iran, Nasrullah Rastegar-Pouyani, Rasoul Karamiani, Department of Biology, Faculty of Science, Razi University, 67149 Kermanshah, Iran; Masoud Yousefi, Eskandar Rastegar-Pouyani, Department of Biology, Tarbiat Moalem University of Sabzevar, PO Box 397 Sabzevar, Iran; Hasan Salehi, Hossein Parsa, School of Biology, College of Science, University of Tehran, Tehran, Iran; Ulrich Joger, State Natural History Museum, Pockelsstr. 10, 38106 Braunschweig, Germany; Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland; Haji Gholi Kami, Department of biology, Faculty of sciences Golestan University, Gorgan, Iran.

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20 September 2011

ISBN 978-3-9812565-4-3

Notes on Distribution and Morphology of the Dice Snake (Natrix tessellata) in China Yang Liu, Konrad Mebert & Lei Shi Abstract. In China the dice snake (Natrix tessellata) is only recorded from the westernmost area, the Xinjiang Uygur Autonomous Region. A brief review on distribution and morphology of the dice snake in China is presented. Scalation was used to quantify its morphological variation in China. The frequency and range of head scale counts (supralabial, infralabial, preocular, postocular, supraocular, temporal), as well as the number of dorsals, ventrals and subcaudals is recorded. Scale variation could be divided into three categories: (1) no variation (dorsal and supraocular), (2) occasional variation (infralabial, preorbital, supralabial, postorbital and temporal), and (3) continuous variation (ventral, subcaudal). The variation of temporal scales is discussed in details. All freshly sampled specimens were deposited in the Museum of Xinjiang Agricultural University. Key words. Natrix tessellata, China, habitat, new distant records, scalation, temporal scales

Introduction The dice snake (Natrix tessellata) has an extensive distribution from central and southern Europe east to the countries of the Middle East and the Nile Delta and across Iran, Russia, Kazakhstan into China (Bannikov et al. 1977, Gruschwitz et al. 1999), from where it is only recorded from the Xinjiang Uygur Autonomous Region (e.g. Shi et al. 2002, Wang et al. 2005). Studies on the dice snake in China have been focused on diet, movement and reproduction (Zhao 1978, Zhao et al. 1998), population ecology (Wang et al. 1987), karyotype analysis (Li et al. 1988) and circulatory system (Zhang et al. 1990). According Wang et al. (1987) and Zhao et al. (1998) the dice snake in China needs at least 4–5 years to reach maturity. Mating season concentrates from early May to early June in China. During the mating season, the dice snake was found to usually occupy in- and outflows of fish ponds, rice fields and other lotic habitats, whereas few have been observed in lentic, relatively still water (Wang et al. 1987). Depending on the habitats and food conditions the diet of dice snakes varied accordingly. In fish ponds, the diet consisted almost exclusively of fish, whereas dice snakes in rice paddies preyed on little toads and tadpoles, but not fish. Again in other habitats insects and rodents were consumed (Wang et al. 1987, Wang et al. 2005). In Wensu County, the dice snake emerged from hibernation in early April. Because of the low temperature, they surfaced only in the afternoon in the first two weeks. They became more active in May to June with activity peaks between 8–10 am and 3–5 pm (Wang et al. 1987). Scalation is a significant character in snake taxonomy (Zhao et al. 1998). Studies on scale variation from a large number of specimens enables a finer taxonomic sorting at inter- and intraspecies levels. Moreover, these data could help to address some phylogenetic and bio-

geographic problems (Chen & Zhao 2007). The purpose of this work is to provide the existing basic information on the morphology, including color pattern, body lengths, and scalation of the dice snakes from Chinese herpetological collections and their geographical distribution. Materials and Method The principal data was obtained from 101 specimens of Natrix tessellata, all deposited in the Museum of Xinjiang Agriculture University. Nine scale counts were recorded: three from the body (trunk) and six from the head (Tab. 1). A few data were received from an earlier acquisition by the second author and N. Helfenberger from the Zoological Museum of the School of Life Science, Sichuan University, Chengdu, Sichuan, China. These data were added after the principal analysis and include 16 dice snakes (2 males, 14 females) from Kizil, near site 17 (Fig. 1) and one male from Kashi City. Ventral scales (VENT) were counted according to Dowling’s (1951) method, and the counting of subcaudals (SUBC), began with the first scale pair posterior to the vent (cloaca) and excluded the terminal tail tip. Cephalic (head) scale counts were made on both sides of the head. We used Microsoft Office Excel 2003 and SPSS 11.5 to analyze the data. Results Distribution In accordance with its aquatic habits (Gruschwitz et al. 1999), the dice snake inhabits freshwater habitats including rivers, ponds, dams, and ditches of oases across all of the Xinjiang Autonomous Region. Consequently, Figure 1 shows a rather discontinuous distribution

©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Fig. 1. Distribution of the dice snake (Natrix tessellata) in China (Solid dots). Red areas indicate a significant microgeographic difference in temporal scale arrangement.

pattern of Natrix tessellata in China. However, it is not clear, to what extent the various oasis-populations are currently isolated from each other. The dice snake is distributed across most districts of the Xinjiang Autonomous Region. For example, Zhao et al. (1998) recorded the dice snake from the following localities (see also Fig. 1): Yining or Ghulja City (1), Nilka County (2), Xinyuan County (3), Gongliu County (4), Tacheng City (5), Toli County (6), Kashi City (7), Hotan County (8), Aksu City (9), Korla City (10) and Urumqi City (11). In addition, we collected it from Wensu County (12), Qitai County (13), Toksun County (14), Qiemo County (15), Huocheng County (16), Baicheng County (17), and Wushi County (18). The distribution altitude of the dice snake in China is from -80 m (Toksun) to 1500 m (Wushi) a.s.l. The dice snake is replaced by the grass snake (Natrix natrix) in the far northern Altai Mountains. But the western Junggar Boundary Mountain in northwest China is a potential area of sympatry for the two natricine snakes. There, we collected the grass snake from Qiege Town, Yumin County (site 19 in Figure 1, N46°13’, E82°50’; 597 m a.s.l.) and the dice snake from nearby Kupu Town, Toli County (site 6, N45°52’, E83°24’; 1287 m). Color Pattern Dorsal surface olive to dark gray, without or with dark spots in an approximative checkerboard pattern; oc-

ciput with a dark transverse stripe forming the letter “V”, whereas dark specimens were less distinct. Figures 2–4 show a small selection of color pattern of Chinese dice snakes. Melanistic specimens can predominate locally, as nine of the 16 investigated specimens from the Zoological Museum of the School of Life Science, Sichuan University, Chengdu, are melanistic (Fig. 4). The greatest SVL (snout-to-vent length) recorded by us was 864 mm (a female specimen from Korla City). Scalation The range of gender-specific ventral and subcaudal scales is given in Table 2. Significant difference exists between males and females in number of subcaudals (T-test: t = 9.985, df = 78, P < 0.0001), whereas males and females do not differ in number of ventral scales (T-test: t = 1.117, df = 98, P = 0.267). The 14 females from Kizil yielded an average ventral count of 175.14 (range 173–179) and subcaudals of 57.46 (range 53–60, n = 13), whereas the three males, including the specimen from Kashi, exhibited a mean of 179.33 ventrals (range 178– 181) and for subcaudals of 68.50 (range 68–69, n = 2, as the third male missed part of its tail). All the snakes had a 19-19-17 dorsal formula (Tab. 3). The frequency of the various states of cephalic scale characters is also shown in Table 3. Overall, the temporal formula of the scales is usually 1+2 (50.5%) but ex-

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Fig. 2. Dice snakes from China; left: A dark specimen collected in Kizil reservoir, Baicheng County, northwestern Tarim Basin; right: A specimen collected in Tatirang Town, Qiemo County, South-eastern Tarim Basin.

Fig. 3. Dice snakes from China; left: Dice snake moving in shallow water, Kekeya Town, suburb of Aksu Region; right: Dice snake leaving the water after comsuming a fish, suburb of Korla City.

pression of other scale arrangements showed large geographic variation. These additional variations of temporal scales could be divided into four categories: 2+2, 1+1+2, 1+3 or 1+2+3 (Fig. 5). There was a significant difference of the ratios of these categories (Chi-square Test: P < 0.01; Tab. 4) between the populations of the Aksu Region (north of the Tarim Basin) and the Yili Region (north of the Eastern Tien Shan Mountains). The dice snakes from Yili exhibited significantly higher frequency (36.21%) of three temporal scales posterior the first single temporal than individuals from the Aksu Region (5.26%).

tial rainfall, whereas the populations are isolated during periods of increased aridity. Natrix tessellata from areas south of the Tarim Basin in Hotan and Qiemo counties (Figs. 1, 6, 7) show that this species occurs substantially farther south in China, approximately 500 km south of the Turpan depression, than previous reports and established distribution maps have indicated (Bruno & Maugeri 1990, Gruschwitz et al. 1999, Lenz et al. 2008). The dice snakes from Qitai County in the southwestern part of the Junggar (or Dzungarian) Basin constitute the currently most eastern occurrence of N. tessellata. It is not known from areas farther into northeastern direction, despite an unsubstantiated indication by Lac (1968) for the Altai Mountains (discussed in Gruschwitz et al. 1999). Already Zhao et al. (1998) and Zhao (2005) have reported on different degrees of scale variation in Chinese snakes, as found in this study with the invariable number of dorsal scale rows to the highly variable arrangement of temporal scales. However, neither in those studies nor in this work are the underlying causes for the distinct degree of variation (no, occasional, and con-

Discussion The dice snake from the Xinjiang Uygur Autonomous Region in China represents the easternmost distribution of this species. However, a few uncertainties remain concerning the connection between the various population-centers located in the oases. We presume that a fluvial corridor exists or has existed in periods of substan-

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Fig. 4. Preserved melanistic dice snakes from Kizil, Xinjiang, China. Specimes from the Zoological Museum of the School of Life Science, Sichuan University, Chengdu, Sichuan, China

stant variation) among the various scale characters in Chinese N. tessellata known. But presumably environmental factors insert distinctively selective forces on the various morphological scale characters. The least that could be said is that the geographic variation in the arrangement of temporal scales possibly reflects vicariant divergence based on the historical separation of the two populations by the high Tien Shan Mountains. But more data is required to evaluate whether these differences are adequate for a subspecific differentiation or not. The ventral scale counts are on average 15 scales higher than in dice snakes form western Europe, and thus, corroborate the proposed clinal increase for this character from west to east, with the highest values (mean VENT males = 182.9, females 188.2) occurring in populations from the northwestern coastal strip of the Caspian Sea (Mebert 1993, Mebert 2011). In comparison, the

Tab. 1. Codes used for scale characters. Variable Number of ventral scales Number of dorsal scales Number of subcaudals Number of preorbitals Number of postorbitals Number of supraoculars Number of supralabials Number of subabials Number of temporals

Code VENT DORS SUBC PREO POST SUPO SUPL SUBL TEMP

subcaudal counts are fluctuating more from west to east. The mean subcaudals of Chinese dice snakes are consistent with values found in dice snakes between the Black and the Caspian Seas (Mebert 1993, Gruschwitz et al. 1999, Mebert 2011). Surprising was the lack of sexual dimorphism in the number of ventrals in the principal data set, since this occurs ubiquitous in natricinae (e.g. Mebert 2010). It is also a common difference between the gender of N. tessellata and differences may even occur across a small area (Mebert 1993, 1996, Gruschwitz et al. 1999). Furthermore, Dincaslan et al. (2011) discuss briefly the possibilty of insufficient sampling and sex determiantion of samples that may lead to an apparent lack of sexual dimorphism. In addition, the lumping of snakes from distinct geographic units due to small sample size could unintentionally erode a locally existing sexual dimorphism. In this context, only the increase of the sample size and a strict geographic comparison would clarify this issue in potential future studies. A post-analysis with additional data from preserved dice snakes from Kizil is consistent with similar sexualdimorphic scale count expression, and thus, does confirm that such gender differences locally exists in China. As allover its wide range, Chinese dice snakes most frequently exhibit 8 supralabials. But the proportion of individuals with more than 8 supralabials (9 or 10 scales) is with ~33% three to six times higher than in populations from Europe (Mebert 1993, Gruschwitz et al. 1999). This pattern is paralleled in sublabials, where the proportion of dice snakes with 11 or more sublabials is particularly high in northeastern Turkey with more

Tab. 2. Variation of ventrals and subcaudals of dice snakes (Natrix tessellata) from China. Variable VENT SUBC

Number of specimens Female Male 64 55

36 25

Female 172-187 55-69

Range

Male 173-186 69-74

Average(mean ± SE) Female Male 180.27 ± 0.39 62.80 ± 0.56

181.12 ± 0.72 71.77 ± 0.57

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Tab. 3. Descriptive statistics on cephalic scale variation in dice snakes (Natrix tessellata) from China; n = 101. Variable SUPL SUBL PREO POST SUPO DORS

Normal pattern (frequency %) 8 (65.31) 10 (73.27) 3 (83.15) 4 (56.42) 1 (100) 19-19-17 (100)

Variations (frequency %) 7 (2.0), 9 (30.69), 10 (2.00) 11 (22.77), 9 (3.96) 2 (14.85), 4 (2.00) 3 (5.94), 5 (35.64), 6 (2.00) none none

1930) was for long the only subspecies accepted, but its validity has been disputed (see refs. in Gruschwitz et al. 1999). Genetically, Guicking et al. (2009) and Guicking & Joger (2011) have succeeded to structure populations of the dice snake, sampled across most of its range, into nine clades based on mitochondrial DNA haplotypes. Due to geographic proximity, Chinese dice snakes (not sampled in the study by D. Guicking) probably would be closest to the Kazakhstan clade. However, that study provided no morphological data to corroborate such a conclusion.

Tab. 4. Comparison of temporal scale variation between two populations of dice snakes (Natrix tessellata) in China. Variation category 2+2

Proportion (n)

Proportion Yili Region Proportion Aksu Region

Significance of difference

5.40% (6)

5.17%

3.51%

P = 0.739

1+1+2

10.89% (11)

1.72%

12.28%

P = 0.008

1+3

13.37% (13)

36.21%

5.26%

P < 0.0001

3.96% (4)

1.72%

6.14%

P = 0.157

1+2+3

Fig. 5. Variation of temporal scales in Chinese dice snakes (Natrix tessellata).

than 20% and thus, resembles the phenotypic frequency in Chinese dice snakes (~27%). Currently, Natrix tessellata has only weakly diverged into geographic units to validate any subspecies determinations based on morphological characters only (Laňka 1978, Mebert 1993). N. t. heinrothi from the Ukrainian Black Sea island of Ostrov Zmeinyi (Hecht

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At the western end of its range, the dice snake in Central and Western Europe is characterized by usually exhibiting 2 preoculars and 3 postoculars (Gruschwitz et al. 1999). The dice snakes east of the Carpathian Mountains and south of the Hungarian plains exhibit predominantly 3 preoculars and 4 postoculars (Laňka 1978) and thus, resemble in this regard dice snakes from central

Yang Liu, Konrad Mebert & Lei Shi

no help either. But to fine-scale the morphological variation, we substantially increased the data set with this study. Future studies should focus on testing for geographic differences to infer phylogeographic pattern, and determine taxonomic affiliations for N. tessellata from China. For that purpose, it is recommended to increase the data acquisition by sampling across many more sites in the Xinjiang Uygur Autonomous Region. Acknowledgments

Fig. 6. Natural habiat inhabited by Natrix tessellata at the bank of Kalakashi River, Hotan (Hetian) County, Xinjiang, China.

Fig. 7. Anthropogenic Habitat inhabited by Natrix tessellata – a wetland in Hotan (Hetian) County.

Asia, associated with the former subspecies N. tessellata hydrus (Pallas 1771). The expression of ocular scales in Chinese dice snakes are well in accordance with the putative N. t. hydrus. However, the expression of pre- and postocular is more variable than the above mentioned references indicate. For example, the frequency of 4 or more postoculars in five populations from Switzerland and northern Italy ranges between 43% and 79% (by a 1:1 sex ratio, n = ~80/population) and can rise in females to 82% (Mebert 1993). In the German population with the highest density of the dice snakes, the frequency of individuals with 4 postoculars is with 58.4% also very high (Lenz & Gruschwitz 1993). Some specimens from the Junggar (or Dzungarian) Basin, site of the most eastern Chinese populations of dice snakes, even have 4 preoculars and 5 postoculars. Due to the extensive variation of scale characters within the dice snake across its wide distribution, it appears not feasible to determine taxanomic groups or relateness based on morphological properties alone. The lack of genetic information from Chinese dice snakes is

This work was supported by the National Natural Science Foundation of China (NSFC30770264, 30360014) and the National Infrastructure of Natural Resources for Science and Technology (2005DKA21403). References Bannikov, A.G., Darevskii, I.S., Iszczenko, W.G., Rustamov, A.K. & N.N. Shcherbak (1977): Opredelitelj zemnowodrychi presmykajuscichsja fauny SSSR. (Identification of Amphibians and Reptiles of the SSSR). – Proswesenije, Moscow (in Russian). Bruno, S. & S. Maugeri (1990): Serpenti d’Italia e d’Europa. – Mondadori, Milano, Italy. Chen, X. & E.M. Zhao (2007): Research on lepidosis variation of Sphenomorphus indicus. – Sichuan Journal of Zoology 26(2): 392–394 (in Chinese). Dincaslan, Y.E., Arikan, H., Ugurtas, H.I. & K. Mebert (2011): Morphology and blood proteins of dice snakes from Western Turkey. – Mertensiella 18: 370–382. Dowling, H.G. (1951): A proposed standard system of counting ventrals in snakes. – British Journal of Herpetology 1: 97–99. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581– 644. Guicking, D. & U. Joger (2011): A range-wide molecular phylogeography of Natrix tessellata. – Mertensiella 18: 1–10. Guicking, D., Joger, U. & M. Wink (2009): Cryptic diversity in a Eurasian water snake (Natrix tessellata): Evidence from mitochondrial sequence data and nuclear ISSR-PCR fingerprinting. – Organisms, Diversity and Evolution 9(3): 201–214. Hecht, G. (1930): Systematik, Ausbreitungsgeschichte und Őkologie der europäischen Arten der Gattung Tropidonotus (Kuhl) Boie H. − Mitteilungen aus dem Zoologischen Museum in Berlin 16: 244–393. Lác, J. (1968): Reptilien des Stromgebietes der Flüsse Hron, Ipec und Slana. II. Teil: Anguidae, Colubridae, Viperidae. – Ochrana Fauny, Bratislava 2(1/2): 15–23. Lenz, S. & M. Gruschwitz (1993): Zur Merkmalsdifferenzierung und -variation der Würfelnatter (Natrix t. tessellata Laurenti 1768) in Deutschland. – Mertensiella 3: 269–300. Lenz, S., Mebert, K. & J. Hill (2008): Die Würfelnatter (Natrix tessellata). – In: DGHT (Ed.): Die Würfelnatter: Reptil des Jahres 2009. – DGHT, Rheinbach, Germany: 6–32. Li, S.Z., Wang, G.Y. & Y.B. Fan (1988): The karyotype analysis of Natrix tessellata. − Journal of August First Agricultural College 11(4): 70–73 (in Chinese).

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The Dice Snake in China Mebert, K. (1993): Untersuchung zur Morphologie und Taxonomie der Würfelnatter Natrix tessellata (Laurenti) 1768 in der Schweiz und im südlichen Alpenraum. – M.S. thesis, University of Zürich, Switzerland. Mebert, K. (1996): Comparaison morphologique entre des populations introduites et indigènes de Natrix tessellata de l’Arc Alpin. − Bull. Soc. Herp. Fr. 80: 15–25. Mebert, K. (2010): Massive Hybridization and Species Concepts, Insights from Watersnakes. – VDM Verlag, Saarbrücken, Germany. Mebert, K. (2011): Geographic variation of morphological characters in the dice snake Natrix tessellata (Laurenti 1768). – Mertensiella 18: 11–19. Nikol’skii, A.M. (1915): Fauna Rossii i sopredelnih stran (Fauna of Russia and adjacent countries). Presmikayushchiesya (Reptilia), Vol. 2. Chelonia and Sauria. − Izd-vo Imp. Akad. Nauk (Imper. Acad. Sci. Press), St. Petersburg (in Russian). Shi, L., Zhou, Y.H. & H. Yuan (2002): Reptile fauna and geographic divisions in Xinjiang Uygur Autonomous Region. – Sichuan Journal of Zoology 21(3): 152–156 (in Chinese).

Wang, G.Y., Fan, Y. & R.X. Zhai (2005): Distribution and ecology of snakes in Xinjiang. – Arid Zone Research 22(2): 181–185 (in Chinese). Wang, G.Y., Qi, W.D., Ma, M., Wang, H. & J.H. Lei (1987): Observations on the population ecology of Natrix tessellata. – Arid Zone Research 4(2): 35–40 (in Chinese). Zhang, T.H., Tian, Y.S. & X.L. Cai (1990): Anatomical studies on the circulatory system in Natrix tessellata. – Journal of August First Agricultural College 13(4): 125–129 (in Chinese). Zhao, E.M. (1978): A preliminary survey of snakes in northern Xinjiang. – Materials for Herpetological Research, Chengdu 4: 7–9 (in Chinese). Zhao, E.M. (2005): Preliminary studies on biology of Enhydris plumbea (Boie, 1827) (Serpentes: Colubridae: Homalopsinae). – Sichuan Journal of Zoology 24(3): 330–332. Zhao, E.M., Huang, M. & Y. Zong et al. (1998): Fauna Sinica, Reptilia, Vol. 3. Squamata, Serpentes. – Science Press, Beijing (in Chinese).

Authors Yang Liu, The College of Animal Science, Xinjiang Agricultural University, Urumqi 830052, China, currently at Chengdu Institute of Biology, Chinese Academy of Science, Chengdu, 610041, China; Konrad Mebert, Siebeneichenstrassse 31, 5634 Merenschwand, Switzerland, e-mail: [email protected]; Lei Shi, The College of Animal Science, Xinjiang Agricultural University, Urumqi 830052, China, e-mail: [email protected].

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PHOTO NOTE Mating Aggregations in Natrix tessellata Already Schreiber (1912) reported on a large mating aggregation of 150–200 dice snakes. Zapf (1969) and Street (1979) mentioned large bundles of dice snakes engaged in mating activities. Such an aggregation is depicted in Lenz et al. (2008) and in Sterijovski et al. (2011). Complementing, we show here a few more examples on large aggregations of dice snakes, mostly reflecting mating balls in spring (Figs. 1–3). The pictures and excerpts depict a mature female surrounded and entwinded by several males. Under suitable conditions, Natrix tessellata is a highly prolific species. Large individual densities likely promote an increased copulation success, as little mate searching is required, and may be a key factor for its colonizing success along linear structures of aquatic systems and locally rapid population growth (see ref. in Mebert 2011).

Fig. 1. Excerpts of photos showing mass aggregations of Natrix tessellata for mating at Lake Alpnach in Switzerland. The collage combines several mating balls photographed on the same day, 8 June 2008. Photos: Thomas Ott

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Fig. 2. Two seasonally early mating balls at Lake Alpnach. (A) 8 May 2010; Photo: Konrad Mebert; (B) 30 April 2006; Photo: Heidi Jost References Lenz, S., Mebert, K. & J. Hill (2008): Die Würfelnatter (Natrix tessellata). – In: DGHT (Ed.): Die Würfelnatter – Reptil des Jahres 2009. – DGHT, Rheinbach, Germany: 6–32. Mebert, K (Ed.) (2011): The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species. – Mertensiella 18, DGHT, Rheinbach, Germany. Schreiber, E. (1912): Herpetologica Europea. – G. Fischer-Verlag, Jena, Germany. Sterijovski, B, Ajtić, R., Tomović, L., Djordjević, S., Djurakić, M., Golubović, A., Crnobrnja-Isailović, J., Ballouard, J-M., Groumpf, F. & X. Bonnet (2011): Natrix tessellata on Golem Grad, FYR of Macedonia: a natural fortress shelters a prosperous snake population. – Mertensiella 18: xxx–yyy. Street, D. (1979): Reptiles of Central and Northern Europe. – London (Bratsford). Zapf, J. (1969): Unsere Nattern. – Carinthia II, Mitt. naturwiss. Ver. Kärnten, Klagenfurt 79: 173–176.

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Authors Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland; Thomas Ott, Titlisstrasse 10, 5022 Rombach, Switzerland.

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PHOTO NOTE Upward Position of Eyes and Nostrils of the Dice Snake to Break the Water Surface? This photograph by the first author (see below) well illustrates the presumed function of the slightly upward position of eyes and nostrils in Natrix tessellata, a characteristic distinction to its relative, the grass snake N. natrix. Eyes and nostrils of the dice snake barely break the upper water layer and pull the water surface next to head a little downwards. It enables the snake to remain submerged and to breathe and inspect activities above the surface, such as those of putative predators, with minimal emergence (see also Egerer & Mebert 2011).

Reference Egerer, E. & K. Mebert (2011). Dice snake, the shy water beauty. – Mertensiella 18: 456 and DVD.

Authors Benny Trapp, Kieler Straße 29a, 42107 Wuppertal, Germany, e-mail: [email protected]; Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland ©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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PHOTO NOTE The Only Known Albino of Dice Snakes (Natrix tessellata)? Does the picture represent the only known albinistic dice snake? We are not sure. But albinos of Natrix tessellata were mentioned to be rare (Muggiasca & Gandolla 1976, Street 1979, Gruschwitz et al. 1999). No concrete reference to any other albinistic dice snake or photograph has been published, except for the pictured specimen inspected by the first author. This albino was first mentioned by Pirotta (1879). It’s a male of 57 cm total length, found on the 9 August 1879 at Tre Miglia, Pavia, northern Italy, deposited in the zoological collection of the Natural History Museum in Pavia.

References Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas. Band 3/IIA: Schlangen II. – AULA-Verlag, Wiesbaden: 581–644. Muggiasca, F. & E. Gandolla (1976): I rettili del Ticino. – Canobbio-Lugano, Switzerland. Pirotta, R. (1879): Di alcuni casi di albinismo nei Rettili. Atti Soc. ital. Sci. nat. 21: 1-4. Street, D. (1979): Reptiles of Central and Northern Europe. – London (Bratsford).

Authors Konrad Mebert, Maya Henggeler, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland, e-mail: konradmebert@gmail. com. ©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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First Report of Melanistic Dice Snakes (Natrix tessellata) in Slovenia There are no published records on melanistic dice snakes from Slovenia. I summarize seven such encounters from the last ten years. Locations of finds are shown in Fig. 1. No photos are available for records that originate from the Sava River; at 200 m a.s.l. near village Sava (23 May 2001 and 30 May 2002, A. Kapla, pers. comm., location 4) and at 183 m a.s.l. near village Breg (26 August 2008, A. Žagar, pers. comm., location 5). Other observed individuals were photographed and are presented in Figs. 2A-B and 3C-E. Additional specimens have been observed at locations 3, 4 and 5, which were normally coloured.

Fig. 1. Locations of melanistic dice snake (Natrix tessellata) in Slovenia

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Fig. 2. Melanistic dice snake from Slovenia. A: On 28 April 2010 in river Poljanska Sora under the dam near village Visoko pri Poljanah (location 1, 375 m a.s.l.). Photo: Karla Rihtaršič, ID determined by Vesna Cafuta B: From 12 May 2008 on the margin of forest near the Sava River by Brežice (location 5, 145 m a.s.l.). Photo: Anamarija Žagar

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Fig. 3: Additional melanistic dice snake, Slovenia. C: Adult from 16 May 2010 by brook Hrastnica in Škofja Loka ca. 200 m away from Poljanska Sora (location 2, 350 m a.s.l.). Photo: Diana Marguč, ID determined by Vesna Cafuta D: From 2 June 2007 basking in grass on the Sora River bank in village Goričane (location 3, 315 m a.s.l.). Photo: Vesna Cafuta E: From 5 August 2011, DOR by brook Blanšcica near Blanča, ca. 950 m away from the Sava River (location 6, 186 m a.s.l.). Photo: Marija Peganc

Acknowledgements The author would like to thank A. Kapla, D. Marguč, K. B. Rihtaršič and A. Žagar for permission to publish their data.

Author Vesna Cafuta, Societas Herpetologica Slovenica, drustvo za preučevanje dvozivk in plazilcev, Večna pot 111, 1000 Ljubljana, Slovenia, e-mail: [email protected].

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PHOTO NOTE Luring a Dice Snake by Wave Action in the Water – a Predatory Response to a Moving Aquatic Prey? During a study about hybridization between two species of North American water snakes, Nerodia sipedon and Nerodia fasciata (Mebert 2008, 2010), the senior author (KM) conducted extensive nocturnal sampling of snakes in knee- to hip-deep water. On numerous occasions, he observed that water snakes often reacted promptly to the frequent small waves on the surface caused by stepping through the water. Subsequent deliberate elicitation of small waves on the water surface by tapping with a stick, the hand or the finger enabled to attract water snakes. In a few cases, this method was used to even lure and catch nocturnal foraging water snakes out of dense reed grass or from within deeper water < 5 meters away, where they were hardly accessible (catchable). The snakes never appeared disturbed or distracted by the strong headlight. The small waves presumably represent a moving frog, an important prey for the investigated water snakes. After a brief discussion about these observations, the second author (BT) tried to reproduce a similar experiment with a dice snake (Natrix tessellata) during a tour to the Peloponnese, Greece. On 13 July 2009, at 23:00 h, BT discovered a foraging dice snake in a 10–15 cm shallow puddle on the edge of a semi-dry river bed near the town of Zacharo (Fig. 1). Similar as with Nerodia, the dice snake did not appear to be disturbed by the strong flashlight and continued its search for prey under water. It was constantly tongueflickering and moved slowly between the stones of the largely barren ground. At a distance of 40–50 cm

Fig. 1. A dice that was lured with moving the index finger just beneath the water surface: below just before luring; above emerging with luring. Photos: Benny Trapp. ©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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from the snake, BT moved his index finger slightly back and forth just below the water surface. Simultaneously, the beam of the flashlight was directed to the snake, while the finger remained in relatively darkness. The snake responded immediately and moved directly towards the moving finger. It stopped at a distance of between 5 and 10 cm before the finger, remained for a few seconds constantly tongue-flickering and left again, but in a completely different direction. This experiment was repeated several times with different directions, twice while the lights were switched off. The dice snake always responded in the same way, whereby it emerged with the head in two of the trials. After eight trials, the snake finally settled on the waters edge and remained inactive (Fig. 2). A hypothetical explanation is that the dice snake responded to the subsurface waves elicited with the moving finger, which likely resembled the waves caused by a moving fish prey. This behavior resembles that of Nerodia water snakes reacting to small waves on the water surface during their nocturnal foraging.

Fig. 2. The dice snake resting on land after the experiment. Photo: Benny Trapp

References Mebert, K. (2008): Good species despite massive hybridization: genetic research on the contact zone between the watersnakes Nerodia sipedon and N. fasciata in the Carolinas, USA. – Molecular Ecology 17: 1918–1929. Mebert, K. (2010): Massive Hybridization and Species Concepts, Insights from Watersnakes. – VDM Verlag, Saarbrücken.

Authors Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland, e-mail: [email protected]; Benny Trapp, Kieler Straße 29a, 42107 Wuppertal, Germany.

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PHOTO NOTE Dice Snake Feeds on Spiny Invasive Fish A dice snake (Natrix tessellata) leaving the water with a freshly caught pumpkinseed (Lepomis gibbosus), dam near the town of Pravetz, western Stara Planina Mts., Bulgaria, early June between 9:00 and 11:00 am. The snake continued to the nearest vegetation cover, struggling with the fish by holding on to its tail. The North American species of sunfish has been introduced to many parts in Europe. At this site, the carnivorous fish is increasingly dominant in the shallow area and appears to have displaced the native fish (perch, carp) into deeper areas of the reservoir lake. Today, the pumpkinseed probably constitutes the main food for the dice snakes. There aren’t any known records of N. tessellata killed after consuming a sunfish. But there is a report from Spain of a viperine snake (N. maura), a close relative, which died after swallowing a pumpkinseed sunfish (Santos & García-Cardenete 2005), likely due to the sharp spikes on the fish’s dorsal fins. It indicates a potential threat of this invasive fish to the native fauna.

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Figs. 1–4. Sequence of a dice snake landing with a pumpkinseed (Lepomis gibbosus), dam near the town of Pravetz, western Stara Planina Mts., Bulgaria. References Santos, X. & L. García-Cardenete (2005): Introducción de peces en ríos de la Cuenca Mediterránea: una amenaza para sus depredadores. – Bol. Asoc. Herpetol. Esp. 16(1/2): 50–51.

Author Ilian Velikov, bl.110, ent. A, ap. 16, Pravetz 2161, Bulgaria, e-mail: [email protected]. ©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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PHOTO NOTE Unsuitable Food for Dice Snakes (Natrix tessellata)! Dice snakes are able to gape their mouth widely as most snakes, when it comes to swallow an oversized prey. A good example is presented in Figure 1, in which a dice snake from the Maggia River, southern Switzerland, consumed a large common frog (Rana temporaria), that possesses a much larger head width than the snake (Fig. 1). Although not completely unsuitable, due to their semi-aquatic habits dice snake rarely consume terrestrial prey, such as reptiles or mammals (see some refs. in Gruschwitz et al. 1999, Mebert 2011). But sometimes they devour unsuitable to even strange food, as these examples from Switzerland demonstrate (Figs. 2 and 3). These food items are unlikely items of their normal diet and it remains a mistery, how these items found their way into the snakes’ stomach. The strange food items in all animals were surgically removed at the Cantonal Animal Clinic of Zürich, and the wounds stitched (Fig. 4). Snakes were released after an additional 1–2 weeks healing period under controlled indoor conditions. How and why these strange “food” items were consumed, can only be speculated. Two ideas are based on the knowledge about the snake species and personal obervations. Snakes are known for their keen olfactory senses, consuming anything that smells like their prey. Indeed, this fact is used to feed piscivorous water snakes with pinkies (young, hairless mice) previously rubbed on fish. Ground fish like the bullhead (Cottus gobio) is such a preferred prey in those lakes, that a dice snake may even risk a fatal accident in its pursuit (Mebert & Pölzer 2011). During scuba diving, I have observed dice snakes actively browsing the lake bottom as deep as 10 m in search of those bullheads which frequently rest between rocks. A bullhead could have left sufficient residues of its body odor on a small rock, that this has become irresistible for the two dice snakes in Figure 2, resulting in their erroneously picking up and swallowing those rocks. Another hypothesis may account for a dice snake from Lake Geneva swallowing the peach pit (peach “stone” in Figures 3 and 4). Personal experience with American and European water snakes corroborate general observations of their reflex-like sudden reaction to moving objects (potential prey), while calm prey sitting nearby is ignored (Mebert 2010, Egerer & Mebert 2011, Tuniyev et al. 2011). Such a behavior may have let a dice snake to snap at the peach pit that was moving with the wave action while floating on the lake surface. References Egerer, E. & K. Mebert (2011): Dice snake, the shy water beauty (Film). – Mertensiella 18, DGHT, Rheinbach, Germany. Gruschwitz , M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA Verlag, Wiesbaden, Germany: 581–644. Mebert, K. (2010): Massive Hybridization and Species Concepts, Insights from Watersnakes. – VDM Verlag, Saarbrücken. Mebert, K. (Ed.) (2011): The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species. – Mertensiella 18, DGHT, Rheinbach, Germany. Mebert, K. & W. Pölzer (2011): Fatal hunting accidents killing dice snakes (Natrix tessellata) and bullheads (Cottus gobio). – Mertensiella 18: 448–449. Tuniyev, B., Tuniyev, S., Kirschey, T. & K. Mebert (2011): Notes on the dice snake (Natrix tessellata) from the Caucasian Isthmus. – Mertensiella 18: 343–356.

Authors Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland, e-mail: [email protected]. ©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Fig. 2. Dice snakes having swallowed a stone, Switzerland: (A) Lake Alpnach, September 1993, (B) Lake Brienz, June 1991. X-Ray: Cantonal Animal Clinic, Zürich

Fig. 1. A dice snake that consumed a common frog (Rana temporaria), Maggia, southern Switzeland, 24 April 2004. Photo: Konrad Mebert

Fig. 4. Before (A) and after (B) the surgical removal of the peach pit from the female dice snake in Figure 3. Photo: Konrad Mebert Fig. 3 (left). A female dice snake consumed a peach pit (stone), Lake Geneva, October 1991. X-Ray: Cantonal Animal Clinic, Zürich

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PHOTO NOTE Record of Natrix tessellata as a prey of Hierophis gemonensis On 13 July 2008, Slavica Sorić (photo author) observed a Balkan whip snake Hierophis gemonensis (Laurenti, 1768) eating a dice snake Natrix tessellata (Laurenti, 1768) on the banks of river Krupa by the “Kudin most” bridge in the vicinity of village Golubić in central coastal Croatia (Fig. 1). It was found among large rocks in low grass on the river bank, about 10 m from the river Krupa (X 5566793, Y 4894008; UTM 10x10 km is WJ69; 65 m a.s.l.). Even tough H. gemonensis feeds on wide variety of animals like lizards, birds, insects and even snakes such as Coronella austriaca and Zamenis longissimus (Henle 1993, Kreiner 2007), N. tessellata in particular was never recorded as food item. But a black whip snake, Dolichophis jugularis, a close relative of the whip snake, was reported to have consumed a dice snake in Israel (Ilani & Shalmon 1984).

References Henle, K. (1993): Coluber gemonensis Laurenti, 1768 – Balkanzornnatter. In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas. – Vol. 3/1. Schlangen I; Aula−Verlag, Wiesbaden, Germany. Ilani, G. & B. Shalmon (1984): Snake eats snake. – Israel Land & Nature 9: 125. Kreiner, G. (2007): Snakes of Europe – All Species from West of the Caucasus Mountains. − Edition Chimaira, Frankfurt am Main, Germany.

Authors Dušan Jelić, State Institute for Nature Protection, Trg Mažuranića 5, 10 000 Zagreb, Croatia, e-mail: [email protected]; Boris Lauš, Croatian Herpetological Society – HYLA, Radučka 15, 10 000 Zagreb, Croatia. ©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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The Gull Larus cachinnans (Pallas, 1811) as Natural Predator of Natrix tessellata (Laurenti, 1768) On 2 April 2010, Z. Pulić observed and filmed the yellow-legged gull Larus cachinnans (Pallas, 1811) eating a live dice snake (Natrix tessellata) (Laurenti, 1768) on the peer of the city of Skradin (Central coastal Croatia) (Fig. 1). Skradin (X 5574598, Y 4852893; UTM 10 × 10 km is WJ75; 3 m a.s.l.) is situated on the banks of Prokljan Lake formed by the Krka River passing through a wide canyon. The water in the lake is brackish but supports many reptilian species better known from freshwater habitats, such as N. tessellata, N. natrix, Emys orbicularis etc. The gull was filmed approaching the snake (approximately 70 cm in length) which was basking on the peer, and catching it by the neck, followed by shaking the prey. The snake appeared unharmed by the shaking and was still alive as it was swallowed. The whole process consuming the snake lasted for approximately two minutes. Local people reported that this feeding behavior by the gulls was frequently observed (Z. pulić, pers. comm.). Yellow-legged gulls are scavengers and predators with a varied diet, consisting of fish, invertebrates (including insects, mollusks and crabs), reptiles, small mammals, bird eggs and chickens (Del Hoyo et al. 1996, Olsen & Larsson 2003, Munilla 1997). Nevertheless, no report exists that this gull species predates on N. tessellata (e.g. Kreiner 2007), but its relative L. ridibundus has been cited as a predator on dice snakes in Gruschwitz et al. (1999).

Fig 1. Still shots of Larus cachinnans at the Krka River estuary while eating a live Natrix tessellata. (film: Z. Pulić) ©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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References Del Hoyo, J., Elliott, A. & J. Sargatal (1996): Handbook of the Birds of the World, Vol 3: Hoatzin to Auks. –Lynx Edicions, Barcelona, Spain. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA Verlag, Wiesbaden, Germany: 581–644. Kreiner, G. (2007): Snakes of Europe – All Species from West of the Caucasus Mountains. − Edition Chimaira, Frankfurt am Main, Germany. Munilla, I. (1997) Henslow’s swimming crab (Polybius henslowii) as an important food for yellow-legged gulls (Larus cachinnans) in NW Spain. – ICES J. Mar. Sci 54: 631–634. Olsen, K.M. & H. Larsson (2004): Gulls of Europe, Asia and North America. – Christopher Helm, London.

Authors Dušan Jelić, State Institute for Nature Protection, Trg Mažuranića 5, 10 000 Zagreb, Croatia, e-mail: [email protected]; Boris Lauš, Croatian Herpetological Society – HYLA, Radučka 15, 10 000 Zagreb, Croatia.

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PHOTO NOTE

Terrestrial Dice Snakes: How far from Water a Semiaquatic Snake Ventures out? Konrad Mebert The dice snake (Natrix tessellata) is known for its close association to water. Monitoring studies mostly located this species within 10 m of the water line (refs. in Gruschwitz et al. 1999). Concerning lager distances, Werner (1938) stated, that N. tessellata leaves the water only for hibernation, oviposition or for utilizing particularly suitable spots for thermoregulation. For example, N. tessellata were discovered at a distance of 80 m to the nearest water body at a locality in southern Austria (Zimmerman & Fachbach 1996). This terrestrial site was linked to an oviposition site. Most reported dice snake findings of 100–500 m distance to water relate to hibernation sites, including a few exceptional large distances of > 1 km (see refs. in Gruschwitz et al. 1999, and in Mebert 2011). However, Esterbauer (1994) found a hatchling in July at 3 km from the nearest water body in southen Syria, indicating that oviposition can also occur rather distant from water. Chernov’s (1954, cit. in Mushelišvili 1970 due Laňka 1978) account of a dice snake at 18 km distance from the Ural River does not clarify whether there were tributaries nearby from where that individual could have originated. Yet, various recent radiotelemetric studies corroborate the close physical association of N. tessellata to water (see reports in Mebert 2011). The figures below show a few additional records for sites relatively distant from water (Figs. 1–3). Furthermore, the records from the Maggia Valley, Switzerland, in Figure 3 indicate, that locally a distinct behavior can evolve, one that is different from other populations in the same general region (e.g. from populations only 10 to 30 km away in the Bolle di Magadino, Conelli et al. 1999). Distances from water might be even larger in some Asian populations, as I.S. Darevsky (in litt.) reported of N. tessellata occupying arid areas in the Ustyurt Plateau, Western Kaszakhstan, where little open water exists and the water snakes supposedly feed on Rhombomys mice. Similar, Dzafaro [or Dzafarof] (1949) mentioned that the dice snakes distant from the Caspian Sea consume also mice, and Jakovlev [or Yakovleva] (1961, 1964) reported dice snakes feeding on young muskrats in a publication about snakes in Kyrgyzstan. Both latter authors were cited in Mushelišvili (1970, due Laňka 1978). Under which ecological conditions such mammal–feeding of an otherwise piscivorous species occurs, e.g. the lack of water bodies, could not be evaluated herein. But it is certainly an interesting topic to research, whether populations of dice snakes once thriving along water bodies in arid areas can switch to mammalian prey after dessication of their foraging habitat. References Conelli, A.E., Nembrini, M. & K. Mebert (2011): Different habitat use of dice snakes, Natrix tessellata, among three populations in Ticino Canton, Switzerland. – A radiotelemetry study – Mertensiella 18: 100–116. Dzafaro, R. D. (1949): Trudy Estesvenno-Istoricheskogo Muzeja im Zardabi, Azerbaijan, Vol. 3 [in Laňka 1978]. Jakovlev, I. D. (1964): Presmykajushchijesja Kirgizii, Frunze [in Laňka 1978]. Esterbauer, H. (1994): Lebensweise und Verhalten der Würfelnatter im Masil al Fawwar (Syrien). – DATZ 47: 308–311. Gruschwitz, M., Lenz, S., Mebert, K. & V. Laňka (1999): Natrix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA-Verlag, Wiesbaden, Germany: 581–644. Laňka, V. (1978): Variabilität und Biologie der Würfelnatter (Natrix tessellata). – Acta Universitatis Carolinae, Biologica 1975–1976: 167–207. Mebert, K. (Ed.) (2011): The Dice Snake, Natrix tessellata: Biology, Distribution and Conservation of a Palaearctic Species. – Mertensiella 18, DGHT, Rheinbach, Germany. Mushelišvili, T.A. (1970): Presmykajuscijesja vostochnoj Gruzii. – Izd. “Mezniereba”, Tbilisi. Werner, F. (1938): Ergebnisse der achten zoologischen Forschungsreise nach Griechenland (Euboea, Tinos, Skiathos, Thasos usw.). – S. ber. Akad. Wiss. Wien, math.-naturw. Kl., (I) 147, 5/10: 151–173. Zimmermann, P. & G. Fachbach (1996): Verbreitung und Biologie der Würfelnatter, Natrix tessellata tessellata (Laurenti, 1768) in der Steiermark (Österreich). – Herpetozoa 8(3/4): 99–124. ©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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Konrad Mebert

Fig. 1. A dice snake approximately 150 m above the Cijevna River, barely visible in the center of the photograph, in Montenegro on 14 May 2004. There is no other water body nearby except a small and steep mountain brook without any fish. Dice snakes presumably need to move up and down the slope to the Cijevna River to feed on fish. In situ Photo: Konrad Mebert

Fig. 3 (next page). Numerous dice snakes have been observed distant from water courses during a monitoring study along the Maggia River, southern Switzerland. These were all gravid females, presumably utilizing spots distant from the river with enhanced thermoregulatory capacities for embryogenesis before and after oviposition: (3A) a gravid dice snake basking on the border of an open field 70 m from the river, Avegno, 6 June 2007; (3B) a gravid dice snake placed half a meter in front

of its basking spot in the herbaceous plants, 60 m from the river bank, Aurigeno, 30 May 2007; (3C) at Cevio–Visletto, gravid dice snakes occupy sites in talus slopes (~ rocky debris) and rip-raps at 130–200 m distance from the river, 24 June 2007. In contrast, males and non-gravid females still occupied sites along the riparian bank. Photos: Konrad Mebert 454

Natrix tessellata Distant from Water

Fig. 2. Left: Dice snakes have been found occupying sites high on the cliffs along the Adriatic coast near Duino, Italy (pers. comm. A. Dell’Asta), and move down to fish in the sea. Right: Accordingly, several dice snakes have been observed at a marine bay between Duino and Villagio Pescatore. Photos: Konrad Mebert

Author Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland, e-mail: [email protected].

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MERTENSIELLA 18

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20 September 2011

ISBN 978-3-9812565-4-3

DVD

Dice Snake (Natrix tessellata) the Elusive Water Beauty The dice snake, Natrix tessellata, is a semi-aquatic snake, exhibiting well adapted behaviors to many types of water bodies. This DVD provides life film sequences of this snake species taken directly from its natural environment at three sites in Europe. This footage complements in a lifelike manner the scientifc articles presented in this Mertensiella volume. First scenes are filmed at the Schwechat River and in the Kamp River Valley near Vienna, Austria. Here, a short clip segment exhibits how close dice snakes can dwell to human society, as the snakes inhabit the supporting wall of the outdoor platform of a restaurant. It is also amazing to see dice snake swimming in rather strong currents and make use of the interstitial topography to move across the stream bottom, possibly to reduce the drag imposed by the current, to be more cryptic against predators and simultaneously ready to snap at any fish prey hiding in the crevices. Before landing, dice snakes often take on a periscope position by “standing” in the water a few meters before the shore with the head barely breaking the surface and the tail anchored around an object on the stream bottom. This way, a snake is able to scan the shore area for any potential danger. The second location shows film sequences from the brackish water lagoon at Kaiafa on the Peloponnese Peninsula, Greece. Dice snakes are shown foraging by a sit-and-wait strategy while hanging from a branch with the head in the water, ambushing mosquitofish passing by. Another scene demonstrates the speed of swallowing a fish, after a dice snake captured a mullet in a more open area of the lagoon. The foraging method is also compared to the sympatric grass snakes (Natrix natrix) which hunts for frogs on the water surface, whereas dice snakes focus on fish below the water surface. In the reed grass of the lagoon good basking places are not common, and dice snakes have to share this resource with the European pond turtle (Emys orbicularis). Dice snakes usually mate on land. But in a sidearm of the lagoon, mating activities could be filmed in the water. The clip shows how males nervously follow receptive females, which by exuding pheromones become irresistible for males. Finally, the reproductive sequence is accomplished with a brief mating act in the water. Astonishing to see in one sequence, that a female, the larger sex, can be quite small (young) to exert an urging “follow-me” response to males. This indicates, that even small females send out attracting pheromones and, hence, possibly are sexually mature before the end of their second year of life. A digitalized sequence from an underwater film made with the super 8 technique in 1982 shows a dice snake foraging on the bottom of Ohrid Lake, FYR Macedonia. Interesting to see, how the snake uses the rocky ground structure to wait motionless before striking for unwary fish, not always successful.

Authors

Eric Egerer, Johannessrtaße 17A, 2371 Hinterbrühl, Austria, e-mail: [email protected]; Konrad Mebert, Sieben­eichenstrasse 31, 5634 Merenschwand, Switzerland. ©  2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

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