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Ecol Res (2015) 30: 527–535 DOI 10.1007/s11284-015-1250-x

O R I GI N A L A R T IC L E

Luca Luiselli • Fabio Petrozzi • Konrad Mebert Marco A. L. Zuffi • Giovanni Amori

Resource partitioning and dwarfism patterns between sympatric snakes in a micro-insular Mediterranean environment

Received: 1 December 2014 / Accepted: 18 February 2015 / Published online: 27 February 2015  The Ecological Society of Japan 2015

Abstract Islands provide an evolutionary window, where a simplified natural network combined with unusual environmental conditions promote selective processes that trigger rapid changes in biological constituents of a species. The Mediterranean island of Montecristo, Italy, provides such a situation with a reduced fauna and flora compared to the mainland. We measured body size (SVL) and recorded diet of the two snake species occurring on the island, the Asp Viper (Vipera aspis) and the Western Whip Snake (Hierophis viridiflavus), and compared these data with populations of conspecifics from the mainland. Compared to mainland populations, the three principal results are: (1) no obvious niche shift along the food or habitat axes between the two snake species; (2) significant body size shift (insular dwarfism) of the whip snake by 30 %, and ca. 10 % in the viper; and (3) arboreal ambushing in the viper to add an alternative diet (birds) compared to mainland populations

Electronic supplementary material The online version of this article (doi:10.1007/s11284-015-1250-x) contains supplementary material, which is available to authorized users. L. Luiselli (&) Æ F. Petrozzi Niger Delta Ecology and Biodiversity Conservation Unit, Department of Applied and Environmental Biology, Rivers State University of Science and Technology, PMB 5080, Nkpolu, Port Harcourt, Rivers State, Nigeria E-mail: [email protected] L. Luiselli Æ F. Petrozzi Environmental Studies Centre Demetra, via Olona 7, 00198 Rome, Italy K. Mebert Section of Conservation Biology, Department of Environmental Sciences, University of Basel, St. Johanns-Vorstadt 10, 4056 Basel, Switzerland M. A. L. Zuffi Museo di Storia natural dell’Universita` di Pisa, Calci, Pisa, Italy G. Amori CNR Institute of Ecosystem studies, Viale dell’Universita` 32, 00181 Rome, Italy

(more mice) to compensate for the lack of suitable micro-mammals on Montecristo Island. Keywords Snakes Æ Insular syndrome Æ Mediterranean Æ Ecological relationships

Introduction Islands represent a privileged scenario to observe and explore ecological and evolutionary mechanisms. In particular, small islands and islets are especially prone to show unusual adaptations in indigenous species, including dramatic morphological changes and even unexpected behavioral adaptations (e.g., Lomolino 1985). Insular dwarfism is such a phenomenon, which results from the reduction in body size of ‘‘normally’’ larger animals (mean sized mainland individuals) over a number of generations (Sondaar 1977; Prothero and Sereno 1982; Case 1978). This process has occurred many times throughout evolutionary history, with examples ranging from dinosaurs to mammals, such as elephants and their relatives (Herridge 2010). Examples are also known in modern reptiles. For instance, Python reticulatus, one of the largest snake species of the world reaching up to 7 m in length (Barone 2004), are known to grow only up to around 2 m in length on the Flores Sea islands of Selayar, Kayuadi and Tanahjampea (Python reticulatus kayuadi; see also Auliya 2006). Another well known trait for some terrestrial snakes, in particular vipers, is that they may become semi-arboreal on islands with depressed food resource availability and complement their diet with birds (Nilson et al. 1999; Martins et al. 2002; Shine and Xi Lin 2002; Meik et al. 2010). Several explanations have been proposed for the mechanism that produces such dwarfism, mostly in mammals (Raia and Meiri 2006; Van Den Bergh et al. 2008). A relevant mechanism involves a selective process, whereby food availability on the island is decreased compared to mainland populations, and thus, indi-

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viduals with reduced energy requirements are favoured over a few generations, additionally promoted by the absence of predators. In Australian tiger snakes (Notechis spp.), insular dwarfism occurs on islands where prey animals are smaller than those normally taken by mainland snakes (Keogh et al. 2005). Small snakes may be better adapted to take small prey, since prey size preference in snakes is generally proportional to body size (e.g., Luiselli et al. 2012). Variation in body size also affects both, reproductive characteristics and thermoregulation physiology (e.g. (Pough 1980). Smaller size usually leads to shorter gestation periods and generation times, and thus reduces energy expenses and needs for reproduction, rendering another advantage of dwarfism for population experiencing suboptimal insular conditions (Van Den Bergh et al. 2008). Regarding thermoregulation, a smaller-sized body takes up or absorbs heat quicker than a large body (Pough 1980). But overall, the main factor driving insular dwarfism among carnivores is thought to relate to size and availability of prey resources (Raia and Meiri 2006). Once the size range of insular prey has been reduced, it is predicted that strong natural selection would lead to a genetic assimilation for optimizing snake body size. The Mediterranean islands are good areas to investigate ecological phenomena linked to insular syndromes, because of their well-known history and because several noteworthy islands populations have been identified so far (e.g., Amori and Masseti 1996). Among the Mediterranean islands, the Montecristo Island in the Tyrrhenian Sea is particularly noteworthy, because, despite its small surface, it houses two snake species that are also widespread on the Italian peninsula, the Asp Viper (Vipera aspis) and the Western Whip Snake (Hierophis viridiflavus) (Vanni and Zuffi 2011; Zuffi et al. 2011), which can become potential competitors when resource availability is depressed (Luiselli 2006). Our primary aims in this paper are to investigate patterns of body size shifts and ecological niche partitioning in the two above-mentioned snake species, with particular reference to the trophic and spatial niche axes. The reptilian survey is complemented by a survey of lizard-habitat transect data. More specifically for the snakes, we ask the following key questions: (1) Are the Montecristo populations of snakes similar in body size to their mainland conspecifics, or do they show any type of island syndrome (gigantism or dwarfism)? (2) Do snakes exhibit unusual hunting strategies in the island? (3) Do the two snake species partition trophic and/or habitat niche axes on Montecristo Island?

Materials and methods Study area Montecristo Island, 10.39 km2 area, is an island of the Tuscan Archipelago, located in the Tyrrhenian Sea (4220¢N 1019¢E/4233¢N 1031¢E; central Italy). The island is basically a massive rock (highest elevation: Monte della Fortezza, 645 m), with several rock ledges rising steeply from the sea. Scattered patches of soil accumulated between exposed rocks, in rock fissures, and dried stream beds allow the growth of scrub and tree, although the historic small oak forest has been severely degraded by the introduced goats (Amori and Masseti 1996). The island of Montecristo, like all the islands of the archipelago, has a mild climate, with a constant sea breeze, ambient temperatures often >30 C, and very little rainfall (average annual values much lower than 500 mm. The climate is characterized by mild and moderately rainy winters and summers that are hot and dry, but sometimes very muggy. Protocol Field sampling on Montecristo Island was conducted during several periods within the last 15 years. One author (MALZ) visited the island between April and July, 1999, 2000, 2001, 2003–2008; the other authors conducted island tours in May, July and August 2014. Daily field research lasted between approximately 0700 and 1800 h. MALZ conducted field surveys, through random transects including all different types of habitats across the entire island, whereas the 2014 survey focused in the western part of the island, where snakes were most conspicuous near the only stream bed containing at least remnants of water throughout the year. Transects with similar areas were equally distributed along each category of habitat. We carefully examined bushes and rock-cavities where the snakes used to spend long periods of the day. Indeed, a number of individuals was encountered and caught whilst we were moving through completely shaded terrain. For each reptile sightings/captures obtained during 2014, habitat type was categorized as: (1) patches of ferns; (2) low Mediterranean vegetation (dominated by Erica arborea) along rocky gullies; (3) pine forest (Pinus pinaster); (4) or exposed granite masons without vegetation, and the presence as well as basic morphological and ecological data of the target species was recorded. Quantitative VES (Visual Encounter Surveys; Vignoli et al. 2009) devoted to assess the relative abundance of most reptile species (2 snakes and 1 lizard) on the island were conducted during visits in May, July and August in 2014 by the other au-

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thors. In total and considering the effort made by various researchers, as they moved independently of each other through the field site, a total effort of research equal to 340 man-hours was performed during the 2014 season. Each captured specimen was sexed (according sexual dimorphism of the tail root region—males keep their precloacal body thickness across approximately the first 10 subcaudals, but tail thickness tapers of in females subcaudal by subcaudal), measured snout-vent-length (SVL), tail length, body mass, and for the vipers, photographed them for subsequent re-identifications based on their dorsal and cephalic pattern. Otherwise, they were individually marked by ventral scale clipping. The diet of the two species of snakes was studied by dissection of museum vouchers (MSNT, Museum Natural History, University of Pisa; MZUF, Museum Natural History University of Florence), by stereo-microscopic analysis of feces (Saviozzi and Zuffi 1997) of personally sampled animals, and occasionally by direct observation of animals during in situ feeding behavior (Luiselli and Agrimi 1991; Luiselli and Rugiero 1991; Luiselli and Angelici 1996). The same specimen was never subjected to more than a single method of diet data collection, thus assuring that all the reported prey items were independent. Feces of captured snakes were obtained by gentle massage of the abdominal region. Cloacal swabs were preserved in 90 % alcohol for further analysis in the laboratory. After the examination of stomach contents, snakes were released at the same sites where they had been previously captured (Capula and Luiselli 1990). Furthermore in 2014, the relative abundance of lizards was evaluated by VES method separately (independently) from the snake’s VES, using standardized transects, laid across the main habitats available on the island. Each lizard transect lasted 10 min and corresponded to about 80 m linear paths. A total of 47 independent transects were carried out. The number of transects laid in the various habitat types was grossly proportional to the relative habitat types availability at the island. The observed reptiles were not captured in order to minimize disturbance. In order to avoid pseudo-replication of the observed samples, the various surveys for relative abundance of lizards were never been made along the same paths. In order to compare body length (SVL) of Montecristo vipers and whip snakes with mainland conspecifics, we also recorded SVL of museum vouchers and free-living specimens captured along the coast of Tuscany, central Italy (Tables S1, S2). Statistical analyses Correlations between two variables were performed using Pearson’s correlation coefficient after testing the normality of the data distribution using the Kolmogorov–Smirnov test. The averages are always given in the text followed by ±1 standard deviation. Compar-

isons between frequencies were performed using v2 test. Niche breadth for habitat and food were measured by the following formula: , n X Diet breadth ðBÞ ¼ 1 pi2 i¼1

where pi is the frequency of consumption of a certain resource by a given target species. The formula assumes that the values tend to increase with increasing generalism of the target species. The niche overlap between species (Ojk) in the diet and in the space were calculated using the symmetric formula of Pianka (1986): n P

pij  pik Ojk ¼ sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi n n P P pij2 pik 2 i¼1

i¼1

i¼1

In this formula, pij represents the frequency of consumption of a certain resource by the species j and pik that concerning the species k. The values vary from 0 (no overlap) to 1 (total overlap), for which, for example, an overlap value of 0.75 indicates an overlap of 75 % in resource use. The null hypothesis of an even sex-ratio was tested by v2 test; mean differences in body length (SVL) between sexes were tested by Student t test, and the heterogeneity of the slopes relative to the tail length versus the body length of males versus females by a one-way Analysis of Covariance (ANCOVA). Differences in SVL between Montecristo versus mainland snakes of either species were assessed by Student t-test. Parametric tests were applied after having verified normality of data distribution with Kolmogorov–Smirnov test. In order to determine the potential upper size limit of both males and females in the two study species, we bootstrapped the observed sample for a total of 9999 times, following the procedure in PAST software. Interspecific differences in the frequency of utilization of the various prey types were also analyzed by v2 test. In order to analyze the relationships between snake and lizard abundances, we calculated the estimated population density of lizards and whip snakes by the program DISTANCE 5.0 (Buckland et al. 2001). In this program, a detection function (g(x)) described the probability of detecting an object (a lizard or a snake in our study case) given that it is at distance x from the line transect under survey. Assuming that lizards and whip snakes had a homogenous distribution along transects, we analyzed collected data using the uniform model (‘strictly monotonically non–increasing’/‘estimate variance empirically’) as detection function. This detection function has been considered an ‘omnibus’ function for cases such as ours (Buckland et al. 1993). Statistical analyzes were performed using the software PAST, and by ECOSIM PROFESSIONAL. The

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alpha level of 5 % was assigned, and the tests were always carried out two-tailed. Means are presented ±1 standard deviation.

Results Abundance, sex-ratio and habitat use For estimating relative abundance, sex-ratio and habitat use, we analyzed only data collected in 2014. In total, excluding recaptures of both species, 94 specimens of whip snakes (59 males and 35 females; sex-ratio skewed towards males: v2 = 6.13, df = 1, P < 0.05) and 29 specimens of vipers were examined (14 males and 15 females; even sex-ratio: v2 = 0.14, df = 1, P = 0.854). These numbers reflect the abundance ratio of the two snake species, as the viper was clearly less abundant than the whip snake. The capture sites of the snake individuals (year 2014) are shown in Fig. 1. The two species were grossly similar in terms of insular distribution and habitat use (Ojk = 0.710; Fig. 2). Nonetheless, with very few exceptions, the vipers appeared to be limited to the small, mainly shaded streams and pools that are accompanied by dense fern stands. In contrast, the whip snake frequents all types of habitats all over the island (Fig. 2).

Diets

Fig. 1 Map of Montecristo island, showing the localities of capture of Vipera aspis and Hierophis viridiflavus. Filled squares Hierophis viridiflavus. Filled dots syntopy between the two species. Note that there is no single locality where Vipera aspis occurs alone

Data on the diet of the two species of snakes are presented in Table 1. Overall, the taxonomic composition of the diet of both predators appear to be similar (Ojk = 0.824), with a considerable greater trophic niche breadth in the whip snake than in the viper (B = 3.883 vs 2.685). Both, the whip snake and the viper fed mainly on lizards and passerines, with no statistical difference in the taxonomic composition of the diet between the two species (v2 = 5.28, P = 0.615). The vipers have also showed some previously undescribed behavioral adaptations for this island population, and for Asp Viper in general. Some vipers [20.7 % of the sample (recaptures excluded)] were observed climbing into shrubs or low tree branches, where they settled into an ambushing position on twigs and branches, and often acted agitated and ready to strike when approached. While ambushing, the viper kept neck and head suspended in the air and in a lurking position, while the tail anchored the entire body to the branch (Fig. 3). Podarcis sicula density at the 47 transect spots, modeled by DISTANCE, averaged 10.44 ± 12.99 individuals x ha1, and the whip snake density at the same transect spots was 0.96 ± 2.27 individuals x ha1. There was a significantly positive relationship between the modeled density of whip snakes and that of lizards across line transects (Pearson’s r = 0.89, r2 = 0.79, P < 0.001; Fig. 4). No such analysis was performed with V. aspis, because too few viper individuals were observed during the quantitative standardized transects.

Fig. 2 Habitat niche partitioning (expressed as percent of snakes found in each habitat type) between sympatric snakes at Montecristo island. Sample size: n = 29 for Vipera aspis and n = 94 for Hierophis viridiflavus

531 Table 1 Synoptic table of the diet of the two species of snakes at Montecristo island VA Rattus rattus (rat) Passeriformes (birds) Montacilla cinerea Phylloscopus collybita Phoenicurus ochruros Muscicapa striata Hippolais polyglotta Squamata (reptiles) Podarcis sicula (lizard) Hierophis viridiflavus juv (snake) Anura (frogs) Discoglossus sardus Orthoptera (insects) Locusta migratoria other Insect remains Total (prey items)

1 6 (no ID)

HV 0 5 1 1 1 1 1

5 0

10 1

1

7

0 0 13

1 1 25

Counted are the number of individual snakes containing certain prey, Hierophis viridiflavus (HV, N = 25), Vipera aspis (VA, N = 13)

Fig. 4 Relationship between DISTANCE-modeled densities (individuals x ha1) of whip snakes and lizards across 47 line transects, in the Montecristo island. For statistical details, see the text

Bootstrap analyses with 9999 resamplings showed that the potential upper size limit for vipers on the Montecristo Island can be slightly greater than that observed in this study (485 mm in males and 460 mm in females). Adult Montecristo whip snakes (SVL: x = 711.4 ± 65.5 mm, median = 711 mm) had a significantly lower SVL (t = 7.67, P < 0.0001) than mainland conspecifics (x = 905.2 ± 203.9 mm, median = 955 mm, n = 55). Vipers were also significantly shorter in Montecristo (SVL: x = 453.9 ± 28.6 mm, median = 460 mm) than in the mainland (x = 538.7 ± 65.5 mm, median = 542.5 mm, n = 44) (t = 6.56, P < 0.0001). Fig. 3 A male Vipera aspis, ambushing for birds, on Montecristo Island

Discussion Morphometrics SVL of whip snakes averaged 720.0 ± 67.2 mm (n = 67) in males and 685.8 ± 55.6 mm (n = 42) in females, with males being significantly larger than females (t = 2.74, P < 0.01). The largest individual was a male of 873 mm, whereas the largest female was 790 mm long. Males and females did not differ significantly in terms of the slopes of tail length versus SVL (one-way ANCOVA: F1,71 = 1.982, P = 0.164; Fig. 5), but males exhibited a relatively longer tail. Bootstrap analyses (with 9999 resamplings) revealed that the potential upper size limit for male whip snakes at Montecristo is 746 mm (SVL), and that of females is 700 mm. With regard to vipers, the two sexes reached nearly identical body size (SVL—males x = 458.8 ± 35.2 mm, n = 14; females x = 449.3 ± 20.9 mm, n = 15; t = 0.886, P = 0.383). The two sexes also did not differ in terms of their relationships of tail length relative to body length (one-way ANCOVA: F1,26 = 1.707, P = 0.203).

In summary, the three principal results are: (1) no ‘‘new’’ shift in resource partitioning along the food or habitat axes between the two snake species; but significant adaptations of both snake species to the micro-insular conditions provided on Montecristo Island by (2) the dwarfism of the whip snake, and (3) the adaptation of the viper to an alternative diet compared to mainland populations (i.e. birds instead of rodents, Luiselli and Agrimi 1991; Saviozzi and Zuffi 1997). Following, we discuss all three aspects with a wider scope on snake biology. Do the two snake species partition the trophic and/or habitat niche axes? The high overlap along both dimensions in our data suggest that the two snake species do not partition the niche, neither the trophic nor the habitat niche axes, in a

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Fig. 5 Relationships between body and tail lengths in the studied sample of Hierophis viridiflavus. Black dots males; gray dots females. For the statistical details, see the text

way that is different from mainland populations (Luiselli 2006). Instead, the interspecific differences that we observed, especially along the various habitat types, seem to depend essentially on species-specific requirements, with one species (whip snake) appearing considerably more generalist than the other. Concerning the ecological distribution of snakes across the island habitats, our study revealed that the relative abundance of whip snakes across habitats followed the relative abundance of lizards. This finding is in agreement with our dietary data showing that this snake species feeds essentially on lizards and birds in this Mediterranean island, as micro-mammals, a relevant food component for mainland whip snakes, is missing on the island (e.g. Tolfa populations in northern Latium; see Rugiero and Luiselli 1995; Capizzi and Luiselli 1996). Are the Montecristo populations of snakes similar in body size to their mainland conspecifics, or do they show any type of island syndrome? The theoretical largest size for Montecristo island whip snakes was calculated as less than 800 mm SVL by our bootstraps, whereas the average body size that these snakes reach on peninsular Italy ranges between 1000 and 1100 mm SVL (different sites), which is more than 30 % larger (Fornasiero et al. 2007; Vanni and Zuffi 2011; Luiselli et al. unpublished data). However, the Montecristo population of whip snakes still maintains a sexual size dimorphism, in which the male exhibits the larger gender, as in mainland conspecifics (Vanni and Zuffi 2011). The process of insular dwarfing can occur over rather short periods by evolutionary standards (Evans 2012). And it might be not surprising, that among the numerous cases of island dwarfing in vertebrate species (e.g., Burness et al. 2001; Raia and Meiri 2006; Evans 2012), there are also several species of

snakes (e.g., boids: Boback 2006; elapids: Aubret et al. 2004a; Keogh et al. 2005). These authors found that body size shifts have evolved very rapidly among various island populations due to similar and strong selective pressures on the different islands, and that components of genetics and adaptive plasticity are involved (Aubret et al. 2004b). However, in colubrids, such as the whip snake, species tend to be prone to island ‘gigantism’ instead of ‘dwarfism’ (Boback 2003 for a review), thus indicating that the whip snake case described here is rather unusual (but see Zuffi 2007). Previous investigations on whip snakes from the Island of Corsica and its satellite island Giraglia provide further evidence for insular dwarfism in this species (Delaugerre and Cheylan 1992; Delaugerre 2013), as the specimens on these islands reach similar body sizes as the whip snakes on Montecristo Island. Boback (2003) summarized, that the type of principal diet that features snakes in micro-island environments is the main cause to determine body size and differences with mainland conspecific populations (Zuffi et al. 2010), regardless of any genetic differences that may come along. For instance, in the Japanese Izu islands, the Colubrid Elaphe quadrivirgata attains a gigantic size (over 2000 mm in length, versus an average length of about 800 mm on the other islands). This large size probably is a result of foraging on abundant eggs of sea birds and chicks (Hasegawa and Moriguchi 1989), with similar results found in related colubrids (e.g., Kohno and Ota 1991; Mori 1994), but also in elapids (Shine 1987; Schwaner and Sarre 1988; Aubret et al. 2004a). Insular dwarfism is achieved much quicker than gigantism, which evolves more gradual. For example in mammals, latter authors found that insular body size decrease is found to be over 30 times greater than the maximum rate of body mass increase for a tenfold change. They suggest that the evolution of larger size likely is interrupted by a series of physical constraints (novel adaptations to reproduction, food, thermoregulation, etc.) that must be overcome. In contrast, body size decrease is accompanied by rapid maturity, high birth rates, and short lifespans, which are natural history traits that facilitate rapid adaptations (selection) to a novel and extreme environment (Evans 2012). Body size shift might not be that large in reptiles compared to mammals, but the over 30 % decrease of body size in whip snakes from Montecristo Island still is remarkable. A parallel trend to the dwarfism in whip snakes was also found in the asp viper from Montecristo Island, but at a much lower magnitude. Indeed, Montecristo vipers, here adult females (SVL mean at 450 mm; n = 15), were between 10 and 20 % shorter than females of mainland Italian Vipera aspis (see data from Tuscan mainland reported in this paper, but also data from other sources: SVL mean at 510 mm, n = 19; 540 mm, n = 8; 560 mm, n = 58; data from Luiselli and Zuffi 2002; Gentilli et al. 2004; Luiselli et al. unpublished data), where many large specimens exceed 650 mm in

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body length. Even the vipers of Sicily (subspecies hugyi) from where the Montecristo vipers likely originate (Barbanera et al. 2009; Masseti and Zuffi 2011) are larger (SVL mean 540 mm, n = 8, data from Luiselli and Zuffi 2002). Comparative results (small body size, non-mammal diet) are known from several other snake species (Case 1978; Schwaner and Sarre 1988; Shine 1987; Madsen and Shine 1993; Marques et al. 2002; Keogh et al. 2005; Meik et al. 2010; Aubret 2012). As reviewed in Case (1978) and Aubret (2012), predominant explanations for dwarfism and gigantism include the effects of ecological release (from predation, parasitism, and interspecific competition) and resource limitation on islands (intraspecific competition). Shifts in island body size may also arise through a complex mosaic of mechanisms that occur on different but overlapping timescales, such as genetic drift, phenotypic plasticity, and sexual selection, as well as many abiotic factors, such as island size, isolation time, latitude, and distance to the mainland (Aubret 2012). But data from reptiles show, that there is a strong correlation between snake size and available prey size and correlated type (Shine 1987; Schwaner and Sarre 1988; Keogh et al. 2005; Aubret 2012). Madsen and Shine (1993) showed with a common garden experiment that the dwarfism displayed in an island population of European grass snake (Natrix natrix) can be achieved by phenotypic plasticity alone (as response to prey size in general), or by a combination of (1) increased adaptive plasticity, to respond to extreme selection pressure to increase head (jaw) and body size particularly in the gape-limited neonate snakes, and (2) directional selection for larger snakes (neonates to adults), probably within a few generations in the early stages of colonizations or relevant ecological changes (Tanaka 2011; Aubret 2014). An example with rapid adaptive changes in morphology (head morphology, bite strength, and digestive tract structure) and social structure over ca. 36 years has been well documented in an experimental lizard study on an island (Herrel et al. 2008). The rapid morphological change and the effect of presumably phenotypic plasticity appears to fit the scenario for both snake species on Montecristo Island as well. We suggest, that the lack of micro-mammals (particularly mice and shrews) has selected for smaller size in both snake species, albeit with variably strong effects. Available data are limited though, but the current diet of whip snakes in Montecristo appears similarly generalist as the diet of mainland conspecifics, which however also include micro-mammals in the diet and rely less often on amphibians (e.g., Rugiero and Luiselli 1995; Capizzi and Luiselli 1996). A few arthropod remains were found in whip snake guts. These items were certainly ingested purposely by snakes, as they were found intact in their stomachs. Although song birds are also frequent prey items, their accessibility (difficult to catch) and availability (abundant only during short migration periods) reduce their relative value compared to micro-mammals. Feeding on birds can lead to gigan-

tism, but this involves less mobile birds, such as large immobile chicks and nesting birds that are not consumed in our island (Shine 1987; Schwaner and Sarre 1988; Keogh et al. 2005). A comparable example to the dwarf whip snakes on Montecristo are dwarf tiger snakes on Roxby Island, Australia, where the only prey items available are three small species of lizard with a maximum weight of approximately 10 g (Schwaner 1985). Much less is known about the dwarf tiger snakes from the highly isolated Flinders Ranges, mainland southern Australia, but anecdotal evidence suggests that they feed only on seasonally available tadpoles (Keogh et al. 2005). In contrast, islands with ‘‘larger’’ endotherms, such as large mice, shrews, and bird chicks permitted the evolution of large sized tiger snakes (Schwaner 1985; Schwaner and Sarre 1988). Alternatively, the small whip snakes on Montecristo Island may compensate the lack of large, easy accessible endotherms (micro-mammals, young birds or eggs) by consuming increased numbers of smaller prey (lizards, passerine birds). However, as King (2002) stated, handling of small prey, including catching and manipulating, becomes more difficult in large snakes with large mouths (King 2002). Furthermore, the foraging costs increases as lizards are relatively fast and difficult to catch. Large whip snake would encounter many physical barriers, when chasing lizards through the densely covered terrain (stems, twigs, leaves) on Montecristo Island. Already Mushinsky et al. (1982) and Miller and Mushinsky (1990) demonstrated in other species that large snakes prefer larger prey items and King (2002) showed that large snakes simply drop small prey items from their diet. Body size shift in the Montecristo vipers might have evolved by similar mechanism as in whip snakes. A small sample of adult vipers sampled between 1982 and 1985, a time when micro-mammals in the form of young rats were available, showed a mean SVL of ca. 570 mm (n = 6), 20 % larger than our adult vipers sampled in 2014, 2 years after the completion of a rat eradication program, with a mean SVL of ca. 450 mm (n = 15). Although the sample size is rather small for the period, when young rats were still available, the reduced body size measured in the 2014 samples, at least, indicate a similar parallel direction of body size decrease in Montecristo vipers as in whip snakes. Are there any type of behavioral modifications in the island versus mainland populations of the studied species? It is noteworthy that, a diet based essentially on birds, and the concomitant behavioral specializations for foraging on birds on elevated perches that we observed in Montecristo vipers are almost unheard in conspecific populations from the mainland, whose diet consisted predominantly of terrestrial mammals and lizards (Capula and Luiselli 1990; Luiselli and Agrimi 1991; Saviozzi and Zuffi 1997; Rugiero et al. 2012). Nonetheless,

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the same (partial) adaptation to prey upon birds, with very similar behavioral postures as those described herein, have been observed in China’s insular populations of Shedao Island pitvipers (Gloydius shedaoensis) that feed only on migratory birds (Shine and Xi Lin 2002), as well as in endemic insular Milos vipers (Macrovipera (lebetina) schweizeri) in Greece (Nilson et al. 1999; Mallow et al. 2003) and the Golden lancehead viper (Bothrops insularis) of the coast of Brazil (Martins et al. 2002). Acknowledgments We thank for their help, support, and information Leonardo Pettinari, Enrico Lupetti, Luciana Andriolo, Giorgio Marsiaj, Alessio Orsini, Maurizio Mannini, Gianpiero Sammuri, and Davide Zenobi. Two anonymous referees considerably improved the submitted draft. Ministero Politiche Agricole e Forestaly kindly gave permission of access to the Montecristo island, and snakes were captured under authorization of the Ministry of Environment and the Parco nazionale dell’Arcipelago Toscano. The Parco nazionale dell’Arcipelago Toscano funded the present research project (CIG Z9A0C38542).

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