Ophiophagy in Hierophis viridiflavus (Lacépède, 1789) (Serpentes, Colubridae): More than occasional?

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1 Scripta Herpetologica. Studies on Amphibians and Reptiles in honour of Benedetto Lanza: pp , 2014 Ophiophagy in Hierophis viridiflavus (Lacépède, 1789) (Serpentes, Colubridae): More than occasional? Massimo Capula 1 *, Mauro Grano 2, Cristina Cattaneo 3, Francesca Contini 4 1 Museo Civico di Zoologia - Via U. Aldrovandi 18, Roma, Italy 2 Via Valcenischia 24, Roma, Italy 3 Via Eleonora d Arborea 12, Roma, Italy 4 Associazione Culturale Onlus Oletepsiuchè, c/o Museo Civico di Zoologia Via Aldrovandi 18, Roma, Italy * Corresponding author: massimo.capula@comune.roma.it Abstract. In the present paper two cases of ophiophagy (viperophagy and cannibalism) by Hierophis viridiflavus are reported. In H. viridiflavus ophiophagy probably occurs in response to low level of usual prey availability (lizards and rodents) and high abundance of snakes. This indicates that H. viridiflavus has a prey spectrum much wider than that currently known and exhibits local variation in diet composition according to prey availability, thus suggesting that ophiophagy would be not an occasional feeding habit in the species. Keywords. Hierophis viridiflavus, ophiophagy, cannibalism, Italy. Ophiophagy is a feeding behavior relatively common among snakes (see e.g. Polis and Myers, 1985; Mushinsky, 1987). With the exception of those species completely adapted to eat other snakes, such as e.g. Ophiophagus hanna (Cantor, 1836), Clelia clelia (Daudin, 1803) or Lampropeltis spp., ophiophagy is considered as an aberrant behaviour released by an inappropriate stimulus (Fox, 1975). In snakes this phenomenon is known to occur either in the field or under captive conditions. For instance, ophiophagy occurs after long periods of fasting, when a snake is stimulated by a prey situated within its striking range, regardless of whether or not the prey is another snake or a conspecific (cannibalism) (Bruno and Maugeri, 1990). Ophiophagy was also observed in boids when two specimens share a terrarium and select the same prey (Gasc, 1994). In Europe, there are no truly ophiophagic snakes, but some colubrid species such as Coronella austriaca Laurenti, 1768, Dolichophis jugularis (Linnaeus, 1758), Hierophis viridiflavus (Lacépède, 1789), Malpolon monspessulanus (Hermann, 1804), and Zamenis situla (Linnaeus, 1758) are known to prey occasionally on other snakes, including vipers - e.g. Montivipera xanthina (Gray, 1849) in the case of Dolichophis jugularis - and conspecific (Vanni and Lanza, 1977; Gasc, 1994; Göçmen et al., 2008; Cattaneo, 2011a,b; Vanni and Zuffi, 2010). Ophiophagy and 49

2 Capula et al. cannibalism were also reported, in the field and in captive conditions, for the small Mediterranean viper Vipera latastei Boscá, 1878 (Freiria et al., 2006). In the present paper two additional cases of viperophagy and cannibalism by the Western whip snake, Hierophis viridiflavus, are reported. Hierophis viridiflavus is a colubrid snake inhabiting southwestern Europe. This snake is an euryphagous and aggressive species characterized by broad ecological tolerance (Vanni and Zuffi, 2010). Its feeding behavior is opportunistic, as indicated by the consumption of different preys in different habitats and/or geographic areas: e.g. in mainland Italy this species is known to feed mainly upon lizards, rodents and small birds (Capizzi et al., 1995; Rugiero and Luiselli, 1995; Capizzi and Luiselli, 1996; Capula et al., 1997; Rugiero et al., 2002; Capizzi et al., 2008), but on Montecristo Island (Tuscan Archipelago, Tyrrhenian Sea) it was frequently recorded foraging on the Tyrrhenian painted frog (Discoglossus sardus Tschudi, 1837; Zuffi, 2001), and on Ustica Island (ca. 80 km N off W Sicily, Tyrrhenian Sea) it can also feed on green toads (Bufo siculus Stöck, Sicilia, Belfiore, Buckley, Lo Brutto, Lo Valvo, Arculeo, 2008) (Filippi et al., 2003). In addition, some cases of predation on vipers and colubrid snakes were also reported (Erber, 1864; Froesch-Franzon, 1977; Vanni and Zuffi, 2010). In particular, the available literature data refer to the predation of: (1) an adult Vipera aspis (Linnaeus, 1758) (snout-vent length, SVL: 62 cm) by a male H. viridiflavus (SVL: 126 cm) in France (Besançon; Duron and Acolat, 1956); (2) an adult Vipera aspis (SVL: 75 cm) by an adult H. viridiflavus (SVL: 137 cm) in central Italy (the two individuals were observed, but not collected, at the locality «Le Foci» ( N E) near the Poggibonsi village, Province of Siena, Tuscany); (3) an adult female Vipera aspis (SVL: 56 cm) by a large adult male H. viridiflavus (SVL: 137 cm) in central Italy (Montecerboli, N E, Pomarance village, Province of Pisa, Tuscany; see Fig. 1); the two individuals were preserved in alcohol and are stored in the herpetological collections of the Museo di Storia Naturale dell Università di Firenze, Sezione di Zoologia La Specola, collection number: MZUF 19875)(Vanni and Lanza, 1977; Filippi, 1994); (4) a juvenile Zamenis longissimus (Laurenti, 1768) from the locality Macchia della Manziana ( N E), near the Manziana village (Province of Rome, Latium, central Italy), which was regurgitated by an adult individual H. viridiflavus after abdominal palpation in the field (see Capizzi et al., 2008). Finally, it must be noted that in H. viridiflavus two cases of cannibalism are also known: Schmidlin et al. (1996) recorded a case of oophagy, and Naulleau (1987) reported a case of an adult male (SVL: 130 cm) which regurgitated a smaller conspecific (SVL: 60 cm) in the Réserve Nationale de Chizé (SW France) on 14 August With regard to the two cases of ophiophagy presented here, in the first case it was possible to record an adult individual H. viridiflavus preying upon an adult individual Vipera aspis in a natural habitat (edges of an oak forest). Predation was observed during field work on 20 July 2003, at 11:00 hr a.m., at the locality Corchia (630 m a.s.l.; N E), near Berceto village (Province of Parma, Emilia-Romagna, northern Italy). It was also possible to take some pictures of 50

3 Ophiophagy in Hierophis viridiflavus Figure 1. Female Vipera aspis almost completely swallowed by a male Hierophis viridiflavus (Montecerboli, near the Pomarance village, Province of Pisa, Tuscany; Museo Zoologico La Specola, Florence, central Italy; collection number: MZUF 19875). Figure 2. Adult individual Hierophis viridiflavus preying upon an adult individual Vipera aspis in a natural habitat (edges of an oak forest) at the locality Corchia, near the Berceto village (Province of Parma, Emilia-Romagna, northern Italy). this unusual case of predation (see Fig. 2), which was observed lasting for about 4 minutes in situ. During this lapse of time H. viridiflavus was observed biting hardly an adult Vipera aspis behind the head and trying to swallow it. Apparently due to our disturbance, H. viridiflavus regurgitated the viper and both fled. In the sec- 51

4 Capula et al. Figure 3. Cannibalistic behavior in Hierophis viridiflavus: adult female having almost completely swallowed another adult but somewhat smaller conspecific of unknown sex (Villa Borghese, Rome, Latium, central Italy; Museo Civico di Zoologia of Rome, collection number: MCZRVR/02006). ond case it was possible to document the occurrence of cannibalism by analyzing a H. viridiflavus sample preserved in alcohol and stored in the herpetological collections of the Museo Civico di Zoologia of Rome (Italy) (collection number: MCZ- RVR/02006). This sample was collected at the locality Villa Borghese ( N E, Rome, Latium, central Italy) on 25 September 1955 and is represented by an adult female Hierophis viridiflavus (SVL: 107,5 cm; individual with broken tail) which was collected in the field while she was swallowing almost completely another adult but somewhat smaller conspecific of unknown sex. The tail of the preyed individual protrudes from the mouth of the female for 26,6 cm (Fig. 3). Our data, together with those reported in the literature, give further evidence for the predation of snakes by adult individuals H. viridiflavus and support the hypothesis that the species is probably immune to viper venom (Schreiber, 1912; Vanni and Lanza, 1977). The concentration of observations of ophiophagy by H. viridiflavus (seven cases accurately documented to date) may be related to the cumulative probability by the observers to encounter this euryoecic species, which is the most common and widespread snake in Italy (Vanni and Zuffi, 2010). In view of the scarcity of records of ophiophagy in European colubrid snakes, the evidence of at least four cases of viperophagy (with Vipera aspis as a prey species), one case of predation upon Zamenis longissimus, and three cases of cannibalism always involving H. viridiflavus is intriguing. Although our study was not designed to investigate the proximate and ultimate causes of H. viridiflavus dietary shifts, the most parsimonious assumption is that in all the above mentioned cases ophiophagy could have occurred in response to low level of usual prey availability (lizards and rodents) and high abundance of snakes. It is in fact well known that snakes inhabiting areas with low availability lev- 52

5 Ophiophagy in Hierophis viridiflavus els of the usual food type may develop unusual feeding habits and foraging modes (see e.g., Pough and Groves, 1983; Schwaner and Sarre, 1988, 1990; Capula et al., 1997, 2008; Luiselli et al., 2001; Pearson et al., 2002; Filippi et al., 2003). Alternatively, the fact that three out of the seven cases of ophiophagy mentioned above for H. viridiflavus are referable to cannibalism, and that in nature cannibalism occurs especially among ophiophagous and opportunistic snakes (e.g. the colubrid genera Clelia, Malpolon, Dolichophis and the elapid genera Bungaurs and Ophiophagus; Saint-Girons, 1994; Göçmen et al., 2008), could indicate that H. viridiflavus has a prey spectrum much wider than that currently known, exhibiting local variation in diet composition according to prey availability, and thus that ophiophagy would be not an occasional feeding habit in this species. Under these circumstances we think that a more detailed knowledge concerning the abundance and diversity of the various prey species in the field throughout the distribution range of the generalist predator H. viridiflavus is needed in order to give firm conclusions on this matter. Acknowledgments. The authors are gratefully indebted to Anna Maria Nistri and Stefano Vanni (Museo di Storia Naturale dell Università di Firenze, Sezione di Zoologia La Specola ) for providing useful information and giving the opportunity to photograph the sample (MZUF 19875) preserved in the herpetological collections of the Museo Zoologico La Specola, Florence. The authors also acknowledge Simonetta Peruzzi for the realization of the photographs of the sample MZUF 19875, and Marco Fux for providing the photographic material concerning predation of Vipera aspis by Hierophis viridiflavus in the field. The manuscript benefited from helpful discussion and criticism by Luca Luiselli and Lorenzo Rugiero. References Bruno, S., Maugeri, S. (1990): Serpenti d Italia e d Europa. Editoriale Giorgio Monda dori, Milano. Capizzi, D., Capula, M., Rugiero, L., Luiselli, L. (2008): Dietary patterns of two sympatric Mediterranean snakes (Hierophis viridiflavus and Zamenis longissimus) along a gradient of habitat alteration. Herpetological Journal 18: Capizzi, D., Luiselli, L. (1996): Feeding relationships and competitive interactions between phylogenetically unrelated predators (owls and snakes). Acta Oecol. 17: Capizzi, D., Luiselli, L., Capula, M., Rugiero, L. (1995): Feeding habits of a Mediterranean community of snakes in relation to prey availability. Rev. Ecol. (Terre et Vie) 50: Capula, M., Filippi, E., Luiselli, L., Trujillo Jesus, V.T. (1997): The ecology of the Western Whip Snake, Coluber viridiflavus (Lacépède, 1789) in Mediterranean central Italy (Squamata: Serpentes: Colubridae). Herpetozoa 10: Capula, M., Luiselli, L., Rugiero, L. (2008): Variazioni della dieta in relazione allo stato di conservazione dei siti in Hierophis viridiflavus e Zamenis longissimus (Reptilia: Colubridae) In: Herpetologia Sardiniae, p Corti, C., Ed., Societas Herpetologica Italica. Edizioni Belvedere, Le scienze, 8, Latina. Cattaneo, A. (2011a): Risultati di ricerche erpetologiche condotte nell entroterra di Marmaris (Turchia sud occidentale). Naturalista Siciliano, S. IV, 25: Cattaneo, A. (2011b): Osservazioni sull erpetofauna dell entroterra di Boudrum (Turchia sud-occidentale). Bollettino Soc. Naturalisti Silvia Zenari 35: Duron, P., Acolat, L. (1957): La Couleuvre verte et jaune (Zamenis viridiflavus Lacépède) peut contribuer à la destruction des Vipères. Ann. Sci. Univ. Besançon, Zool. et Phys. 6: Erber, J. (1864): Die Amphibien der österreichischen Monarchie. Mit Anführung der Beobachtun- 53

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