and Grass Snakes

MERTENSIELLA 18

225-233

20 September 2011

ISBN 978-3-9812565-4-3

Ecological Partitioning between Dice Snakes (Natrix tessellata) and Grass Snakes (Natrix natrix) in Southern Croatia Biljana Janev Hutinec & Konrad Mebert Abstract. Dense populations of the dice snake (Natrix tessellata) and grass snake (Natrix natrix) occur syntopically at the Baćina lakes in southern Croatia. Aspects of putative interspecific competition regarding feeding habits, habitat use and activity have been studied. During two years of investigation, we found that differences in feeding habits were the most important factors preventing putative competition between these two species. The dice snake fed exclusively on eight species of fish, whereas the diet of the grass snake consisted mainly of amphibians, but occasionally included also fish with six different species recorded. Differences concerning fish types and habitat use have also been observed. Dice snakes consumed more benthic fish and preferred slow running (lotic) aquatic systems compared to grass snakes that inhabited more often quiet (lentic) systems, such as ponds. Although both species prefer substratum with an abundance of plants, significantly more dice snakes were associated with stony substratum. The two species differed also in their positions in the water column. Dice snakes were frequently found foraging on the benthic ground and in the middle of the water body, whereas grass snakes were almost always observed on the surface. Key words. Ecology, competition, food partitioning, dice snake, Natrix tessellata, grass snake, N. natrix, benthic foraging, stony structure

Introduction Closely related species are often ecologically similar and may experience a strong competitive relationship when living in syntopy (Sale 1974, Connel 1983, Schoener 1983, Werner & Gilliam 1984). Such competition might be a major biotic factor influencing structure of animal communities that can lead to morphological and behavioral differences between two similar or closely related species in coexistence. Such an “in situ” morphological difference is termed character displacement (Brown & Wilson 1956), which refers to the increased difference between the two species where their ranges overlap in order to promote reproductive isolation. On the other hand, if relevant separation has not been achieved between two closely related, reproductive compatible species, they face increased hybridization, as were found in related Natricine snakes from North America (Mebert 2010). Corresponding studies of niches are mainly concentrated on competitive relationships and measures of niche breadths/overlaps to investigate the resource partitioning of food, time of activity and terrain among species sharing the same habitat (Mushinsky & Hebrard 1977, Gregory 1978, Pianka & Huey 1978, Reinert 1984a, Capula & Luiselli 1994). Although the concept of the ecological niche is difficult to explain by numbers, it helps us when we want to understand the structure of an animal community. There are numerous ways of measuring niche breadth such as the Levin’s index (Levins 1968), Shannon-Wiener’s index (Colwel & Futuyma 1971), Smith’s index (Smith 1982) and others. The niche overlap, related to interspecific and intraspecific competition, can be measured using MacArthur-Levin’s index (1967), Pianka’s measure (Pianka 1973) or the percentage of overlap (Renkonen 1938).

Investigations of ecological niche relationships between sympatric snake species usually follow a protocol made for lizards (Pianka 1973) involving three major niche categories – food, place and time of activity. Species may differ in the use of those categories, which in turn decreases competition and allows their coexistence. An overview of resource partitioning in herpetological community was elaborated by Toft (1985). In general it is considered that differences in habitat use, by selecting distinct microhabitats, are the most common cause of ecological separation of sympatric animal species and thus, enabling their coexistence (Schoener 1974). However, Toft (1985) noted a different strategy for snake communities, where prey is often the most important resource partitioned. Numerous studies have been dealing with this topic in snakes, whether they concern interspecific differences in habitat selection (e.g. Shine 1977, Reinert 1984a, Luiselli & Rugiero 1990) or intraspecific differences based on sex and age categories (e.g. Mushinsky et al. 1980, Reinert 1984b, Rugiero et al. 1994, Luiselli et al. 1994, Lind & Welsh 1994). For example, interspecific differences in foraging strategies, habitat use and the time of activity are often the results of distinct prey availabilities. Different time of foraging reduces the chance of direct encounter with a similar-minded species and therefore increases the possibility of finding prey not used by the putative competitor. Schoener (1974) stated that the majority of animals showing differences in the use of time are predators. However, such foraging differences have rarely been found in snakes (Toft 1985), even though, some studies such as by Mushinsky & Hebrard (1977) showed that different time of activities appeared to be the main reason to avoid competition in four syntopic watersnakes species. In snakes, niche dif-

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

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Biljana Janev Hutinec & Konrad Mebert

ferences in sympatric snakes have been found for both, in the use of habitat (Brown & Parker 1982) and the utilization of prey (Reynolds & Scott 1982). Although dice snakes (Natrix tessellata, Laurenti 1768) and grass snakes (Natrix natrix, Linnaeus 1758) are widely distributed species and occur often in sympatry, their interspecific relationship is poorly investigated. In recent studies in Croatia, herpetologists usually investigated the distribution and taxonomy of reptiles, while data on biology and ecology were scarce (Radovanović 1941, 1951, 1964, Mršić 1978, 1987, Tvrtković 1984, De Luca 1988, Tvrtković & Kletečki 1993, Kletečki 1995, Schmidtler 1999, Jelic& Lelo 2011). There are just a few data regarding interspecific competition between the dice and grass snakes in the recent past, primarily from Italy (Luiselli & Rugiero 1991, Filippi et al. 1996) and from Greece (Ioannidis & Mebert 2011). A few investigations about the interspecific relationship between N. tessellata and N. maura have also been compilated recently (e.g. Mazza et al. 2011, Metzger et al. 2011, Scali 2011) The grass and dice snakes have different foraging strategies. The grass snake is an active forager, usually hunting prey that are sit-and-wait predators, such as frogs (Hailey & Davies 1986a). On the contrary, the dice snake is described as a sit-and-wait predator (Radovanović 1951, Gruschwitz et al. 1999) preferring active foraging prey such as fish swimming in the water column (Luiselli et al. 2007). Despite of these general accounts, dice snakes, like the grass snake, have locally been observed as active foragers, searching fish in holes and crevices (e.g. Gruschwitz et al. 1999, Mebert 2001, 2007, Kwet & Mebert 2009). The diet of the snake subfamily Natricinae is relatively well known, especially of the North American species (Godley 1980, Halloy & Burghardt 1990, Miller & Mushinsky 1990, Manjarrez & Garcia 1991, Seigel 1992, Mebert 2010), whereas European species are less well investigated (Madsen 1983, Hailey & Davies 1986b, Luiselli & Rugiero 1991, Luiselli et al. 2007). The diet of dice snakes in Europe predominantly consists of fish (Bressi 1995, Filippi et al. 1996, Gru schwitz et al. 1999, Luiselli et al. 2007). Dice snakes from central Italy consumed mostly cyprinid fish and to a smaller proportion amphibians (2 of 18 stomachs with food), a green frog and tadpoles of the common toad Bufo bufo (Luiselli & Rugiero 1991). The prey types of the dice snake found by Bressi (1995) are the following fish species: Gambusia holbrooki, Gobius sp. and Atherina boyeri. Filippi et al. (1996) recorded also fish as the most important prey, in particular from the Cyprinidae family, Leuciscus cephalus, Scardinius erythrophtalmus, and the Gobiidae family, Cobitis taenia. These and additional studies on the diet by this group involving dice snakes (Luiselli et al. 2007) came to similar conclusions and are summarized by Capula et al. (2011). There are just a few related data reported from Croatia (Radovanović 1951), which also state that the diet composition of dice snakes consist mainly of fishes. In

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addition, Radovanović (1951) recorded adult frogs, tadpoles, water shrews and other small animals as part of the diet, and reported both hunting strategies, ambush and actively searching prey. Larger fish or those that were difficult to handle, were carried on land and swallowed after the prey became weak due to oxygen shortage. In contrast to the former species, the diet of the grass snake mainly consists of amphibians and it exhibits a wider niche breadth than the dice snake by including fish, reptiles, small mammals and birds (see reviews in Kabisch 1999 and Gruschwitz et al. 1999). Filippi et al. (1996) described that in 17% of males and in 9% of females the stomachs contained fishes, while the remainder were amphibians. Luiselli & Rugiero (1991) found that the proportion of amphibians in the grass snake diet was 92.67%. Hailey & Davies (1986a) recorded the green frog (Pelophylax ridibundus) as the only prey of the grass snake, while Sternfeld & Steiner (1952) concluded that the principal prey of the grass snake in middle Europe is the brown frog (Rana temporaria), whereas the common toad (Bufo bufo), and the edible frog (Pelophylax kl. esculentus) are occasionally consumed. He also mentioned that juvenile grass snakes ate newts and their larvae. Finally, Madsen (1983) recorded mainly the common toad as a prey for Swedish N. natrix with only a few fishes and brown frogs (R. temporaria and R. arvalis) added. Materials and Methods Investigations were carried out at the Baćina lakes in Dalmatia, southern Croatia (Fig. 1). The lakes are situated two kilometres northwest from Ploče and consist of six submerged sinkholes of which five are connected to one another and one is separated (43° 4’37.03”N, 17°25’23.66”E). The total area of the lakes is 138 hectares and the maximum recorded depth is 31 meters. The lakes are a specific karstic phenomenon. The largest part of this karstic area is made of Cretaceous lime-

Fig. 1: Study area – Baćina lakes.

Ecological Partitioning of Dice and Grass Snakes in Croatia

Tab. 1. Snake samples from Baćina lakes in 1997 and 1998.

1997 (n = 257) 1998 (n = 159)

Grass snake n = 185 juv adult total 98 26 124 juv adult total 55 6 61

juv 33 juv 44

Dice snake n = 231 adult total 100 133 adult total 54 98

stone and dolomite beds. These lakes contain fully freshwater despite the proximity of the Adriatc Sea. According to the data from an ecological study (Mrakovčić et al. 1995) an increased salinity of 1–9 promille was recorded in some sections of the lakes. The area experiences a Mediterranean climate with dry and hot summers and mild winters (Filipčić 1989). The lakes belong to the Mediterranean evergreen vegetation zone dominated by Quercus ilex. The shallow areas exhibit a vegetation mix of marshes and wet habitats with Phragmites australis as the characteristic species. Some floating plant species are: Nymphaea alba, Nuphar luteum, whereas the shore area is overgrown by Scirpus lacustris and Carex elata. Twenty-four fish species were recorded (Mrakovčić et al. 1995). The field work was carried out between May and October in 1997 and 1998 with 37 field days altogether. During the first year 257 individual snakes have been caught with an additional 44 recaptures (a total of 301 captures). From the 172 captures in the second year, 159 have been different specimens (Tab. 1). According to size, snakes were divided into two categories – adult and juvenile snakes. Hence, categories are not defined on actual physiological and reproductive status of specimens. Snout-vent length (SVL) of 35 cm was considered the upper limit for juvenile dice snakes, whereas 40 cm SVL was applied to the slightly larger grass snakes. Although snakes were measured and sexed, this categorization was not considered in the statistical analysis for this paper. The study area was searched along the coast and in the water. A boat was used for water searching. Snakes were caught by hand and palpated to obtain ingested food. All snakes were released on the same place where they were caught. Contents of the stomach were fixed in 70% alcohol for further laboratory analysis. The stomach content of snakes, whose prey was already taken before, as well as weak specimens, gravid females, or females that recently laid eggs, were not palpated. But these individuals were included in the statistical analysis not related to diet. Prey was determined up to species level, or only to the genus, family or class, if it was too damaged by digestion. Prey was classified according to size/ontogenetic stages (tadpoles, froglets or adult frogs). Due to morphological and ecological similarity, the gobiid fish species Pomatoschistus canestini and Knipowitschia sp. were lumped in the statistical analysis.

To calculate the niche breadth, a standardised Shannon-Wiener index was applied (Colwell & Futuyma 1971), and for niche overlap Pianka´s modification of MacArthur – Levin´s index was used (Pianka 1973). Percentage was used to express proportion of snakes that had prey, proportion of prey species/types, proportion of microhabitats used by snake species and type of activity. Prey was separated into following categories: Anurans (tadpoles, froglets, adults); fish (benthic species, surface swimmer). In benthic fishes following species were classified: Blennius fluviatilis, Knipowitschia sp., Pomatoschistus canestrini, whereas surface swimmers were Alburnus albidus, Atherina boyeri, Gambusia affinis, Leuciscus sp. and Rutilus basak. There were eight transects placed along the shore that differ in size from 70–350 m (a total of 1500 m long) and by microhabitat. The microhabitats were defined as: (1) slowly running water, (2) ponds, (3) canals, (4) shallow lake, and (5) area of common reed. The type of capture site was recorded and first distinguished between (1) land or (2) water (incl. water depth and distance from land), and secondly among substrate types (stony or vegetated incl. density of vegetation). Water depths were categorized as (1) shallow water (0–10 cm), (2) medium deep water (10–50 cm) and (3) deep water (more than 50 cm). Vegetation density was assessed and divided subjectively into five different categories which were assigned the numbers 1 to 5, whereby 1 had the least density and 5 the highest. Depending on the position in water column, it was distinguished between: (1) surface (snake was on the water surface), (2) water bodies (snake was in the middle of the water column), and (3) ground (snake was recorded on the ground of the lakes). Following types of activity were recorded and defined: (1) hunting while either swimming or laying quietly in the water or foraging submerged (includes position of the snake and depth of the water), (2) non-hunting moving in water (water depth at the snakes’ first observed position), (3) moving on land (includes distance from water and direction), (4) feeding, (5) thermoregulation (basking on land, including distance from water, or on a floating object in the water), (6) resting (positioned beneath some object – type of object was recorded, e.g. stone, board etc.). Results Three main niche dimensions, habitat, diet, and time were considered and evaluated. Summary statistic results of the overlap between the two species in these dimensions are given in Tables 2 and 3. The differences of the niche breadth and overlap between dice snakes and grass snakes are generally small, but largest in prey species, followed by substrate (niche breadth, Tab. 2) or microhabitat (niche overlap, Tab. 3).

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Tab. 2. Values of niche breadth in dice snake (Natrix tessellata) and grass snake (Natrix natrix) from Baćina lakes. J’ = Standardized Shannon-Wiener measure of niche breadth, T = Natrix tessellata, N = Natrix natrix.

J’

T N

Hour 0.952 0.881

Season 0.874 0.909

Microhabitat 0.870 0.842

Water depth 0.959 0.918

Substrate 0.727 0.640

Prey species 0.792 0.864

Tab. 3. Values of food-, time- and space niche overlap between dice snake (Natrix tessellata) and grass snake (Natrix natrix) from Baćina lakes. Ojk =Pianka’s modification of the niche overlap index.

Ojk

Fishes / amphibians 0.471

Ojk

Microhabitat 0.302

Food niche Prey species 0.260

Fish types 0.718

Water depth 0.990

Position in water 0.671

Hour 0.899

Time niche Season 0.852

Space niche

The stomach contents were collected from 71 dice snakes and 22 grass snakes. Differences between those two species in prey consumption was statistically significant (c2 = 6.875, df = 1, P < 0.0087). Because some specimens were not palpated in order to obtain their food content, due to their reproductive status or weak condition, the actual number of snakes having prey in their stomach was higher than investigated, 100 individuals in dice snakes (40.5 %) and 44 in grass snakes (20.1 %) contained food. A total of 95 prey items were identified from the 71 dice snakes, and 26 prey items were retrieved from the 22 grass snakes. Diet of dice snakes was composed exclusively of fishes, whereas in grass snakes fishes were represented with 40.8%, and the remainder being amphibians with 59.2% (Fig. 2), which is also reflected in a larger niche breadth of prey species (Tab. 2). Consequently, Pianka’s measure of diet overlap Ojk regarding prey

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Water/land position 0.942

taxa (amphibians vs. fishes) was at an intermediate level of 0.471. Relating to the prey species, having in mind that tadpoles and recently metamorphosed froglets of Pelophylax ridibundus were separately considered, and fish species Pomatoschistus canestrini and Knipowitschia sp. were treated together, there was little overlap between the two aquatic snakes with Ojk only at 0.260. A total of eight fish species in dice snakes and six fish species in grass snakes were determined (Tab. 4). Depending on pertinent ecological characteristics (swimming depth) of fish prey, the interspecific difference of the Natrix species was obvious. The amount of benthic fish consumed by dice snakes is with 64.1% three times higher than the comparative diet in grass snakes (18.18%). The majority of fish prey species in grass snakes were surface swimmers (Fig. 3). Tab. 4. Quantitative and qualitative composition of diet in dice snakes and grass snakes from Baćina lakes obtained by palpating. Prey species

Fig. 2. Diet composition of dice snakes (Natrix tessellata) and grass snakes (Natrix natrix) from Baćina lakes. White bar = amphibians, black bars = fish.

Substrate 0.878

Dice snake Grass snake n of prey items n of prey items Alburnus albidus 7 2 Atherina boyeri 11 2 Blennius fluviatilis 17 0 Gambusia affinis 11 3 Knipowitschia sp. 23 2 Leuciscus cephalus albus 1 1 Leuciscus sp. 1 0 Pomatoschistus canestrini 19 0 Rutilus basak 2 1 Pelophylax ridibundus – 0 6 larvae Pelophylax ridibundus – 0 9 froglets Undetermined fishes 3 0 Total 95 26


Fig. 3. Selection of prey type in dice snakes (Natrix tessellata) and grass snakes (Natrix natrix) according to preferred swimming depth of fish species. Black = benthic, white = water column.

Fig. 5. Position of snakes in the water column. Legend defines proportion of snakes found on the water surface, within the water column (intermediate), and on the lake bottom.

There were significant differences in using microhabitats between dice snakes and grass snakes, resulting in a very low niche overlap Ojk for those two species of 0.302. Shallow lake, area of common reed and canals were chosen similarly frequent. An obvious difference was in their frequency of using ponds (dice snakes 4.8%, grass snakes 32.6%), and running water (dice snake 23.1%, grass snake 4.34%) (Fig. 4). A significant difference was also found for substrate use. Although both species mainly used substrate with dense vegetation (53.3% of dice snakes and 81.5% of grass snakes), dice snakes were found more frequently on stony substrate (31.4%) than grass snakes (4.35%). The majority of dice snakes were caught in water (71.6 %), whereas in grass snakes the proportion of animals caught in water (53.3%) and land was similar (46.7%). Dice snakes appeared to forage most often on the lake ground and were similarly frequently detected in the water column and the surface (Fig. 5). In contrast, nearly all grass snakes (93.6%) were observed on the water surface, and those detected on the lake ground or in the middle of the water body were so in shallow water

(depth < 50 cm). Yet, the overlap between these two species is with Ojk = 0.671 still relatively high. For dice snakes a visually greater activity was recorded in the first part of the year from May–July, whereas for grass snakes activity was greater in the second part of the year from July–October (Fig. 6). Dice snakes extended their activity over a longer daily period than syntopic grass snakes. Difference in types of activity between dice snakes and grass snakes is shown in Fig. 7.

Fig. 4. Microhabitat usage in dice snakes and grass snakes at Baćina lakes.

Fig. 7. Proportional distribution of activity types summarized over two seasons in dice snakes (Natrix tessellata) and grass snakes (Natrix natrix) from Baćina lakes.

Fig. 6. Annual activity of dice snakes and grass snakes from Baćina lakes: number/days – number of snakes caught per field day.

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Discussion The syntopic populations of dice and grass snakes at Baćina lakes in southern Croatia appear to reduce their interspecific competition mainly by a distinct diet – especially in the prey types (fishes or amphibians) and associated with this, a different microhabitat use of prey, lotic vs. lentic aquatic system. Known differences in their trophic niche and a low dietary interspecific competition could be confirmed in this study (Luiselli & Rugiero 1991, Filippi et al. 1996, Gruschwitz et al. 1999, Kabisch 1999). The dice snakes are specialized in feeding on fishes (100%), whereas the diet of grass snakes predominately consists of amphibians (59.2%), keeping in mind that this niche overlap is low with Ojk = 0.471. As in this study, Luiselli & Rugiero (1991) have identified a broader niche breadth in grass snakes compared to dice snakes, while the overlap of the taxonomic composition of prey species was Ojk = 0.535. Similarly, Filippi et al. (1996) also recorded a dietary specialisation on fish in dice snakes (97%), whereas in sympatric grass snakes only 17% of males and 9% of females consumed fish. In a further comparison, Luiselli & Rugiero (1991) emphasized that the grass snakes preyed on terrestrial as well as aquatic species, whereas the dice snakes fed exclusively upon aquatic ones. An important result of this study is the observation, that these two semi-aquatic snake species likely avoid competition by foraging for different fish prey. Dice snakes prefer benthic fish, whereas grass snakes hunt fish on the water surface. Considering this difference in prey selection, as well as the related vertical position occupied by the snakes in the water column, the dice snakes appear to be adapted to exploit deeper water and the grass snake more the water surface. In Italy, Luiselli et al. (2007) and Capula et al. (2011) found dice snakes preying only on 10 of 15 fish species present in their study areas. Difference in feeding frequency varies between these two species and reflects the greater adaptation of the dice snake to the aquatic environment. The proportion of dice snakes with prey was twice as high (40.5%) than that of grass snakes (20.1%). Similarly in Italy, where Filippi et al. (1996) showed that more dice snakes contained prey compared to syntopic grass snakes (57.5% and 42.1%, respectively). Additional data from the same region yielded a similar proportion (53.8%) of dice snakes containing prey (Luiselli et al. 2007). The proportion of grass snakes containing prey was similar in other studies and varied between 15–25% (Madsen 1983, Hailey & Davies 1986a, Janev 1995). Proportions of snakes containing food is similar for other species within the subfamily of Natricinae (Seigel 1992), which might indicate that Baćina lakes provide dice snakes a particular suitable foraging ground or that this species generally represents a well-adapted piscivorous reptilian taxon. Certainly its huge distribution in rivers and lakes from Germany to Egypt and east to China hint to the successful evolution of this aquatic species, similar to the equally successful grass snake, albeit both are exhibiting a different set of ecological preferences.

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The grass and dice snake differ also in the niche breadth of their hunting strategies. While the grass snake has been observed only actively foraging, the dice snake adds also a sit-and-wait strategy, depending on the situation (Gruschwitz et al. 1999, Mebert 2001, 2007, Luiselli et al. 2007, Kwet & Mebert 2009). Corresponding to the different preference of prey and their habitat, the microhabitat exploited by the two snake species is also markedly different. Amphibians, prey preferred by grass snakes, are more often found in lentic water overgrown by vegetation, such as ponds, whereas the dice snake can easily colonize lotic systems (Gruschwitz et al. 1999). The increased aquatic habits of dice snakes is also reflected in their capture site, as more were caught in water (71.6%) then on land, whereas the number of grass snakes caught in water and on land was almost equal. In a comparative study in Greece, Ioannidis & Mebert (2011) found grass snakes less often in close proximity to water, while sympatric dice snakes were never farther from the water than around 60 meters. Even less aquatic, Eckstein (1993) detected only 12% of grass snakes in water, and the remainder were detected on land. Hailey & Davies (1986a) also noticed more grass snakes on land then in water (67%) and from those active in water 86% were detected on the water surface. However, it can not be assessed how much the detectability in the different studies sites might have affected the number of grass snakes being counted. The research area described in this paper (Baćina lakes) was restricted by the shore line. Because of this, there is a possibility that some sex and age categories chose their habitats, depending on the season, distant from the water. In this context, Filippi et al. (1996) identified that grass snakes were often found far from water where common toads (Bufo bufo) migrate over land after their reproductive period. According to literature data, different use of time to avoid competition is rarely present in snakes from temperate zones (Toft 1985). However, Mushinsky & Hebrard (1977) studied four species of sympatric natricine water snakes in North America and found that time of activity, whether daily or annual, is important in avoiding interspecific competition. The dice snakes at the Baćina lakest are more active in the first part of the year while the grass snakes were more often found in the second part. Besides that dice snakes are more active earlier in the morning and later in the afternoon, the grass snakes were more active during the hottest part of the day. It may require additional investigations to see, whether such interspecific differences might be an artifact of different detectability, e.g. high visibility of dice snakes in an open lake situation vs. little visibility of grass snakes obstructed by their preferred reed habitat, use of those habitat, and daily and seasonal differences in moving patterns. The reason for the extended activity of the dice snakes lies probably in their hunting strategy in correlation with thermoregulation. Hailey & Davies (1986a) described that the grass snake is an active forager and that


its oxygen consumption is larger, as an adaptation to a more intense activity, than in the closely related semiaquatic viperine snake Natrix maura, wich is an ecological pendant to the dice snake with a very similar niche. The lower oxygen consumption in N. maura is an adjustment to the activity on lower temperatures within a broad thermal niche. On average, body temperature of N. maura is lower than in the grass snake, as they spend increasead amount of time in cool water. Unfortunately, we have no temperature data for the dice snake. But the dice snakes in this study spent a very large amount of time in the water, where they likely experience on average a cooler water (than air) temperatures. Hence, we suggest that as an ecological equivalent of N. maura, the dice snake probably follows a similar model described above. A recent account by Scali (2011) from an area of sympatry between N. maura and N. tessellata showed that the two species prefer similar activity temperatures, but exhibit different patterns of microhabitat use and activity rhythms. The dice snake is more piscivorous and aquatic compared to N. maura and less nocturnal. Another study comparing these two species found great similarities in their trophic niches and experimentally confirmed also the various foraging methods shared by both species (Metzer et al. 2009, Metzer et al. 2011). The smaller and less fecund N. maura, though, appears to emerge from hibernation later than N. tessellata and may miss important feeding opportunities earlier in the season. To get more precise data about interspecific differences in the use of habitat, time, and thermal conditions, radio-telemetric investigations would be suitable. Preliminary studies involving temperature sensitive transmitters are being currently conducted at a site of syntopy between N. maura and N. tessellata, in Switzerland (S. Ursenbacher pers. comm.). At Baćina lakes, all snakes were caught during the day between 6 am and 8 pm, with greater proportion of captures in the middle of day. It is assumed that grass snakes are more active during the day (Mertens 1994) though some authors recorded cases of nocturnal activity (Capula et al. 1994) and several anecdotal observations of nocturnal frog hunting grass snakes from Switzerland and Germany are known to the second author (unpubl. data). Hailey & Davies (1986a) found, that grass snakes under laboratory conditions are primarily diurnal at 15 °C, whereas at 25 °C they become equally active during day and night. Such temperature related shifts of nocturnal to diurnal activities is kown in natricine snakes of temperate zones, described and summarized in Mebert (2010). Nocturnal activity in the dice snake has marginally been known (Scali 2001), but as various recent reports indicate (see refs. in Mebert 2011), this behavior appears to have been largely overlooked. We presume that it occurs more frequent than currently known, at least during warmer periods of the season. Hailey et al. (1982) and Hailey & Davies (1986a) cite reasons for the preferred daily activity of grass

snakes. As eyesight is their most important sense for finding prey, darkness renders the prey less visible to the grass snake. During the night, they also face a bigger risk to encounter some of their nocturnal predators. However, terrestrial amphibians in southern Europe have crepuscular or nocturnal activity which could have caused similar activity pattern in grass snakes, as mentioned above. Furthermore, observations in other natricine species, including Natrix tessellata (Trapp & Mebert 2011) and Nerodia fasciata (Mebert 2010), indicate, that nocturnal snakes rely on tactil senses to detect prey. In addition, as most temperate snake species, grass snakes are more active in spring than in summer (Hailey et al. 1982). As snakes do not have to eat every day, they can reduce their activity and therefore also the risk of being hunted by predators (Madsen 1987). In the sample from Baćina lakes just a small number of juvenile grass snakes were under 25.1 cm of total length, which would correspond to the size category of hatched grass snakes, 13.5 to 22.0 cm (Eckstein 1993, Luiselli et al. 1997). As a result to the small sample size of hatched grass snakes, the category of juvenile snakes included all snakes with a SVL till 40.0 cm. The smallest individuals were caught in June and July. Because of that and the later time of hatching, which for grass snake is in August and September (Eckstein 1993, Luiselli et al. 1997), an apparently increased activity of juveniles grass snakes during the summer is not connected with the hatching but with prey distribution, thermal ecology and the fact that juveniles have to eat more to obtain enough energy for growing (Miller & Mushinsky 1990). In spring, when there are not enough small tadpoles and froglets at the lakes, juvenile snakes may be found on different habitats, which have not been included in this study. In contrast, the increased activity of adult snakes in May and July likely is related to an increased activity demand during that mating period (Madsen 1984, Reading & Davies 1996, Luiselli et al. 1997). Finally, this study revealed that dice snake and grass snake share the same habitat, but do differ in preferences of microhabitat and aquatic prey with their ecological attributes leading to different foraging methods. Comparatively, dice snakes exploit more lotic systems and forage in deeper waters for bottom dwelling fishes, whereas grass snakes inhabit rather lentic systems and are focused more on surface-dwelling prey species including various species of amphibians. Terrestrial habitat of dice snake is associated to a larger degree with stony areas than in grass snakes, which was confirmed by a comparative study in Greece (Ioannidis & Mebert 2011). We hypothesize, that the preference of an open stony area in dice snakes, a habitat promoting quick thermoregulatory activities and possibly prolonged conservation of heat accumulated during the day, might directly compensate their foraging in cooler waters and, thus, their need for higher terrestrial temperatures and/ or prolonged basking behavior than in syntopic grass snakes.

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Authors Biljana Janev Hutinec, Kupreška 6, Zagreb, Croatia, e-mail: [email protected]; Konrad Mebert, Siebeneichenstrassse 31, 5634 Merenschwand, Switzerland, e-mail: [email protected].

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