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Trophic Niche Overlap in Two Syntopic Colubrid Snakes (Hierophis Viridiflavus and Zamenis Longissimus) with Contrasted Lifestyle

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Trophic Niche Overlap in Two Syntopic Colubrid Snakes (Hierophis Viridiflavus and Zamenis Longissimus) with Contrasted Lifestyle Amphibia-Reptilia 33 (2012): 37-44 Trophic niche overlap in two syntopic colubrid snakes (Hierophis viridiflavus and Zamenis longissimus) with contrasted lifestyles Hervé Lelièvre1,2,∗, Pierre Legagneux3, Gabriel Blouin-Demers4, Xavier Bonnet1, Olivier Lourdais1 Abstract. In many organisms, including snakes, trophic niche partitioning is an important mechanism promoting species coexistence. In ectotherms, feeding strategies are also influenced by lifestyle and thermoregulatory requirements: active foragers tend to maintain high body temperatures, expend more energy, and thus necessitate higher energy income. We studied diet composition and trophic niche overlap in two south European snakes (Hierophis viridiflavus and Zamenis longissimus) in the northern part of their range. The two species exhibit contrasted thermal adaptations, one being highly mobile and thermophilic (H. viridiflavus) and the other being elusive with low thermal needs (Z. longissimus). We analyzed feeding rate (proportion of snakes with indication of a recent meal) and examined more than 300 food items (fecal pellets and stomach contents) in 147 Z. longissimus and 167 H. viridiflavus. There was noticeable overlap in diet (overlap of Z. longissimus on H. viridiflavus = 0.62; overlap of H. viridiflavus on Z. longissimus = 0.80), but the similarity analyses showed some divergence in diet composition. Dietary spectrum was wider in H. viridiflavus, which fed on various mammals, birds, reptiles, and arthropods whereas Z. longissimus was more specialized on mammals and birds. The more generalist nature of H. viridiflavus was consistent with its higher energy requirements. In contrast to our expectation, feeding rate was apparently higher in Z. longissimus than in H. viridiflavus, but this could be an artifact of a longer transit time in Z. longissimus, given its lower mean body temperature. These results allow a better understanding of the ability to coexist in snakes belonging to temperate climate colubrid communities. Keywords: dietary habits, energetics, Hierophis viridiflavus, snake, trophic niche, Zamenis longissimus. Introduction specialized species that feed on a single prey type (e.g. Luiselli, 2003) to generalist species Among predators, snakes represent a homoge- that opportunistically feed on prey in relation to neous group as they almost all forage on live their availability (e.g. Rodriguez-Robles, 2002; animals and generally feed on very large prey Brischoux, Bonnet and Shine, 2008; Halstead, relative to their own size (Cundall and Greene, Mushinsky and McCoy, 2008). Within snake 2000; Vincent et al., 2006; but see Shine et al., communities, dietary niche partitioning may 2004). Most are gape-limited predators ingest- be a mechanism limiting potential competition ing their prey whole (Mushinsky, 1987; Cun- (Toft, 1985; Luiselli, 2006a). dall and Greene, 2000; Greene, 2001). Nev- Differences in dietary resource use between ertheless, snakes exhibit marked variation in syntopic snake species are often associated with their degree of dietary specialization (Tanaka divergence in multiple phenotypic traits such and Ota, 2002; Luiselli, 2006a): from highly as lifestyle, morphology, behaviour, and phys- iology (Mori and Vincent, 2008). It is note- 1 - Centre d’Études Biologiques de Chizé, CNRS, 79360 worthy that differing food habits are not nec- Villiers en Bois, France essarily driven by interspecific competition. 2 - Université de Poitiers, 40 avenue du Recteur Pineau, 86022 Poitiers, France Dietary differences can also reflect contrasted 3 - Département de biologie, Université Laval, Québec, eco-physiological strategies that drive energy G1V 0A6 Canada requirements (Secor and Nagy, 1994). In a 4 - Département de biologie, Université d’Ottawa, Ottawa, Ontario, K1N 6N5 Canada recent review, Luiselli (2006a) showed that ∗Corresponding author; e-mail: the degree of food partitioning in sympatric [email protected] snakes varied among geographic areas, and © Koninklijke Brill NV, Leiden, 2012. DOI:10.1163/156853811X620022 38 H. Lelièvre et al. that this variation could be explained partly overlap to evaluate the possibility of interspe- by the level of trophic competition. Luiselli cific competition along this niche axis. (2006a) proposed to distinguish “cold Europe” from “Mediterranean Europe” snake communi- ties, because these communities differ in the Materials and methods number of sympatric species potentially com- Hierophis viridiflavus and Zamenis longissimus are south peting for food. The rationale for such dis- European oviparous colubrids. H. viridiflavus is a typi- tinction was that sympatric terrestrial snakes cal racer according to its morphological (slender body, long tail, large eyes), behavioural (fast, diurnal, terres- in southern Europe, where potential competi- trial), and ecological (high levels of activity and exposure) tion is high, feed upon the most abundant prey characteristics (Naulleau, 1984; Luiselli, 2006b). Z. longis- species and minimize trophic competition by se- simus shows strong morphological and behavioural simi- larities (constricting abilities, semi-arboreal, highly secre- lecting prey of different sizes, rather than prey tive) to ratsnakes (Naulleau, 1984; Burbrink and Lawson, from different species. Other studies, however, 2007). These two species differ in their range of preferred body temperature (Tset): H. viridiflavus is thermophilic (Tset revealed marked divergences in dietary pref- ◦ 27.5-31 C) whereas Z. longissimus prefers cooler temper- ◦ erence among Mediterranean snakes (Rugiero, ature (Tset 21.5-25.5 C; Lelièvre et al., 2010a). We con- ducted our study at the Centre d’Études Biologiques de Capizzi and Luiselli, 2002; Capizzi et al., 2008). ◦ ◦ The lack of a clear pattern in the degree of di- Chizé in Western France (46 07 N; 00 25 O). The study site is a 2600-ha biological reserve managed by the Office etary overlap within snake communities may National des Forêts, dominated by deciduous trees (Fagus, be caused by interpopulation variation in envi- Quercus, Carpinus, Acer), regeneration areas characterized ronmental factors such as habitat structure or by scrubby species (Rubus, Clematis), and grasslands. Cli- matic conditions are temperate oceanic with annual precipi- prey availability (e.g. Rodriguez-Robles, 2002; tation between 800 and 1000 mm, annual mean temperature ◦ Tanaka and Ota, 2002). of 12 C, and annual sunlight of 2000 h. We studied dietary composition of two syn- Snakes were captured during the activity season (April to October) between 1984 and 2009 under concrete boards topic south European snakes (European whip- (120 × 80 cm) disposed throughout the study site (Bonnet snake Hierophis viridiflavus and Aesculapian and Naulleau, 1996; Bonnet, Naulleau and Shine, 1999). Zamenis longissimus Concrete boards are located in edge habitats and are used by snake ) in the northern part snakes for thermoregulation. Each snake captured was mea- of their ranges. These two species are appropri- sured for snout-vent length (SVL, to the nearest ±0.5 cm) ate models to examine the link between lifestyle and body mass (BM, to the nearest ±1 g), and individually marked by ventral scale clipping. Individuals were divided and dietary habits because they are of similar in 3 age classes: neonates (SVL < 40 cm and BM < 15 g), size, but illustrate two distinct ecological orien- juveniles (40 < SVL < 80 cm and 15 < BM < 100 g), tations in snakes (“racer” versus “ratsnake”; see and adults (SVL > 80 cm and BM > 100 g). Each snake was ventrally palpated to detect the presence of prey in the materials and methods for details on terminol- digestive tract. Prey in the stomach and/or abundant faeces ogy). H. viridiflavus is a very active snake that with undigested remains (scales, feathers, etc.) indicate a selects higher body temperatures and exhibits recent meal (<1 week; Bonnet et al., 2011), therefore the proportion of snakes with a prey in the stomach was used higher energetic requirements than the elusive as an index of feeding rate. Food items were collected if Z. longissimus (Lelièvre et al., 2010a, 2011). voluntary regurgitation or defecation occurred in the cap- We expected that the difference in energy re- ture bag. Almost 50% of prey items were identified to the lowest taxon possible and the remaining 50% were only quirements should translate into dietary differ- classified at the prey category level (mammal, bird, reptile, ences. Specifically, we expected that H. virid- or arthropod). We identified prey from faecal pellets using iflavus should be an opportunistic forager ex- tooth shape or hair for mammals (Debrot et al., 1982; Erome and Aulagnier, 1982), using feather for birds, scales for rep- hibiting a wider spectrum of prey, and a higher tiles, and exoskeleton for arthropods. Because only regur- feeding rate, compared to Z. longissimus.Be- gitation allows counting the number of prey items from the cause both species largely dominate the snake same species (in faeces only the number of different prey types could be assessed), we could not estimate the num- community at our study site (jointly represent- ber of prey items accurately. Thus, we used the frequency ing over 80% of captures), we assessed diet of occurrence of each prey type in our analyses. Diet and lifestyle in two snake species 39 To assess the similarity in diet composition between to H. viridiflavus. Over the study period, for groups (species, sex, and age class), we used the ANOSIM both species, the proportion of snakes captured procedure. ANOSIM is a non-parametric
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