Ophiophagy in Coronella Austriaca:� �� �� �� Hierophis Viridiflavus and First Direct Observations of Predation on Vipera Aspis

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Herpetology Notes, volume 13: 1107-1110 (2020) (published online on 28 December 2020)

Ophiophagy in Coronella austriaca:� �� �� �� Hierophis viridiflavus and first direct observations of predation on Vipera aspis

Matteo Riccardo Di Nicola1,*, Lilli Zecchin2, Maurizio D’Amico3, and Francesco Paolo Faraone4

The smooth snake Coronella austriaca Laurenti, 1768 preyed on only by adults (Brown et al., 2013; Reading is a medium/small-sized colubrid snake (total length and Jofré, 2013). usually up to 70 cm, rarely up to 80 cm [Geniez, 2018]) Coronella austriaca can directly swallow smaller prey with a Euro-Siberian (with Caucasian and Anatolian alive, while killing larger prey by constriction (Bruno extensions) chorotype (Sindaco et al., 2013). It is and Maugeri, 1990; Speybroeck et al., 2016; Geniez, distributed across most of Europe (except for Ireland, 2018). Northern England and Central-Northern Scandinavia) Ophiophagy represents only a small part of the C. and eastwards reaching western Kazakhstan, the austriaca diet (Rugiero et al., 1995; Luiselli et al., 1996; Caucasus, northern Anatolia and northern Iran. The Drobenkov, 2000; Reading and Jofré, 2013; Drobenkov, species is polytypic and two subspecies are currently 2014), but it has been directly observed or detected recognised: C. a. austriaca Laurenti, 1768 and C. a. by stomach and faecal contents on several occasions acutirostris Malkmus, 1995 (Sindaco et al., 2013; (including various episodes of cannibalism). The main Speybroeck et al., 2016; Di Nicola et al., 2019). ophiophagy records available in the literature for the The trophic spectrum is a widely studied aspect in smooth snake are summarised in Table 1. C. austriaca. Lacertids are usually its main prey, but In this work we report, according to our knowledge, rodents and shrews are also an important component the first case of predation on a young western whip of their diet; slow-worms, young snakes, saurian eggs snake, Hierophis viridiflavus (Lacépède, 1789) by an and, less frequently, even amphibians, bird nestlings adult smooth snake. and eggs and invertebrates are eaten (Goddard, 1984; The observation occurred on 11 May 2020, in the Galán, 1988; Rugiero et al., 1995; Luiselli et al., 1996; municipality of Camposampiero (Po Valley, Padova, Amat, 1998; Arnold and Ovenden, 2002; Kreiner, 2007; Italy) on the edge of a cultivated field (coordinates: Moreira et al., 2011; Brown et al., 2013; Reading and 45.559028°N, 11.956389°E; elevation: 21 m a.s.l.). The Jofré, 2013; Drobenkov, 2014; Jofré and Reading, observation began with the smooth snake constricting 2020). the western whip snake, holding its head in its mouth A body size-related variation in diet is known for C. (Fig. 1A); the situation lasted more than 45 minutes, after austriaca, with larger species preyed on by larger snakes which the actual swallowing started (Fig. 1B). In order (Luiselli et al., 1996; Reading and Jofré, 2013). Lizards not to disturb the delicate phase of the swallowing, the are preyed upon by both young and adult snakes while author moved away from the snakes; half an hour later small mammals, slow-worms and snakes tend to be the swallowing was still in progress and after another hour there was no trace of the snakes, not even after surveying the surroundings. The swallowing started when the western whip snake was likely dead. The absence of its corpse, as well as that of the predator itself, 1 Via Bobbio, 20144 Milano, Italy. is a possible indication of the success of predation, since 2 ViaStraelle S. Pietro, 35012 Camposampiero, Padova, Italy. death can occur in cases of feeding on legless reptiles 3 ASL 1 Abruzzo U.O.C. Castel di Sangro, Serv. Vet. Sanità Animale. (Kolanek et al., 2020). 4 Viale Regione Siciliana S.E., 90129 Palermo, Italy. The snakes were not captured, so it was not possible to * �� carry out measurements and morphometric evaluations 1108 Matteo Riccardo Di Nicola et al.

Figure 1. A-B: Predation on a young western whip snake (Hierophis viridiflavus) by an adult smooth snake (Coronella austriaca) (Photo credits: Lilli Zecchin). C-D: Predation on a young asp viper (Vipera aspis) by an adult smooth snake (Coronella austriaca) (Photo credits: Maurizio D’Amico). E-F: Predation on a subadult asp viper (Vipera aspis) by an adult smooth snake (Coronella austriaca) (Photo credits: Maurizio D’Amico).

to trace age and sex of the two individuals. However, as is compatible with that of a male (Zuffi, pers. comm.). for the western whip snake, the dorsal pattern and the As for the smooth snake, the general size and the type general size were indicative of its young age (Vanni and and size of prey suggest that it was an adult. Zuffi, 2011); the number of subcaudal scales visible in We also report two observations of C. austriaca one of the photographs (about 104 pairs) does not allow predation on asp viper, Vipera aspis (Linnaeus, 1789). sexing, because the value falls within a range possible According to our knowledge, evidence of predation on for both sexes (male: 97-124 pairs; female: 95-117 pairs V. aspis by C. austriaca exists only for a single case [Schätti and Vanni, 1986]), but the appearance of the tail discovered through the analysis of stomach contents Ophiophagy in Coronella austriaca 1109

Table Table1. Main 1. ophiophagy Main ophiophagy records for records the Smooth for the snake Smooth (Coronella snake austriaca (Coronella). N. austriaca = Number). of N. preyed = Number items. of preyed items.

Prey Type of observation Country Reference N Species Age 1 Coronella austriaca juvenile Ingesta Spain Galan, 1988 2 Coronella austriaca - Ingesta/Fecal remains Italy Luiselli et al., 1996 1 Coronella austriaca juvenile Ingesta Spain Amat, 1998 5 Coronella austriaca - Ingesta Belarus Drobenkov, 2014 2 Coronella austriaca juvenile Direct observation* Turkey Uysal et al., 2019 1 Coronella austriaca juvenile Fecal remains England Jofré and Reading, 2020 1 Coronella austriaca adult Direct observation** England Jofré and Reading, 2020 1 Hierophis viridiflavus juvenile Direct observation Italy This study 1 Natrix helvetica - Fecal remains England Reading and Jofré, 2013 1 Natrix natrix juvenile Direct observation Romania Strugariu et al., 2014 1 Vipera aspis juvenile Ingesta Italy Rugiero et al., 1995 1 Vipera aspis juvenile Direct observation Italy This study 1 Vipera aspis subadult Direct observation Italy This study 1 Vipera berus - Ingesta/Fecal remains Italy Luiselli et al., 1996 1 Vipera berus juvenile Direct observation The Netherlands Groen, 2018 1 Vipera seoanei juvenile Direct observation Spain Pardavila et al., 2012 * Two cases observed in captivity: maternal predation on an offspring and between two young individuals of similar size. ** Attempt of predation on an adult female by an adult male.

(Rugiero et al., 1995), making these the first cases The data reported here increase knowledge on the of direct observations of the event involving these prey spectrum of the smooth snake and confirm that species. ophiophagy appears as a more common behaviour in The first observation occurred on 2 May 2012, in the this species than previously thought. municipality of Castel di Sangro (L’Aquila, Italy) on the edge of an uncultivated field, in a semi-anthropised area Acknowledgements. We are grateful to Mattia Menchetti for a (coordinates: 41.769111°N, 14.127056°E; elevation: pre-review of the manuscript; Thomas Zabbia, Marco A. L. Zuffi, 817 m a.s.l.). An adult smooth snake of about 50 cm Giacomo Bruni and Giampaolo Montinaro for their advice. (total length) captured a young asp viper (probably born References the previous summer). The observation started when C. austriaca had already started to swallow the viper (Fig. Amat, F. (1998): Datos sobre la biología y ecología de la culebra 1C). The estimated time for the complete ingestion, lisa europea Coronella austriaca en el Pirineo Oriental. Boletín which was successful (Fig. 1D), was less than half an de la Asociación Herpetológica Española 9: 22–27. Arnold, N., Ovenden, D. (2002): Reptiles and Amphibians of hour. Britain and Europe (Collins Field Guide). �� England, The second observation occurred on 14 May 2020, United Kingdom, Collins. again in the municipality of Castel di Sangro (L’Aquila, Brown, D.S., Ebenezer, K.L., Symondson, W.O.C. (2013): Italy) in a bushy meadow pasture (coordinates: Molecular analysis of the diets of snakes: Changes in prey 41.797611°N, 14.085722°E; elevation: 1092 m a.s.l.). exploitation during development of the rare smooth snake In this case, an adult smooth snake of over 60 cm preyed Coronella austriaca. Molecular Ecology 23: 3734–3743. on a subadult asp viper of over 30 cm (total length). The Bruno, S., Maugeri, S. (1990): Serpenti d’Italia e d’Europa. Milan, Italy, Editoriale Giorgio Mondadori. observation started when the C. austriaca was still only Di Nicola, M.R., Cavigioli, L., Luiselli, L., Andreone, F. (2019): constricting the viper (Fig. 1E). The constriction lasted Anfibi & Rettili d’Italia. Latina, Italy, Edizioni Belvedere. over an hour while the swallowing (Fig. 1F) lasted Drobenkov, S.M. (2000): Ecology of Smooth Snake (Coronella approximately two hours. austriaca Laur.) in Belarus. �� 7: 135–138. 1110 Matteo Riccardo Di Nicola et al.

Drobenkov, S.M. (2014): Distribution, ecological traits and Reading, C., Jofré, G. (2013): Diet composition changes correlated conservation of the smooth snake (Coronella austriaca) in with body size in the Smooth snake, Coronella austriaca, Belarus. Acta Biologica Universitatis Daugavpiliensis 14: 21– inhabiting lowland heath in southern England. Amphibia- 27. Reptilia 34: 463–470. Geniez, P. (2018): Snakes of Europe, North Africa and the Middle Rugiero, L., Capula, M., Filippi, E., Luiselli, L. (1995): Food habits East. A photographic guide. Princeton, New Jersey, USA, of Mediterranean populations of the Smooth snake (Coronella Princeton University Press. austriaca). Herpetological Journal 5: 316–318. Galán, P. (1988): Segregación ecológica en una comunidad de Schätti, B., Vanni, S. (1986): Intraspecific variation in Coluber ofidios. Doñana: Acta Vertebrata 15: 59–78. viridiflavus Lacépède, 1789, and validity of its subspecies Goddard, P. (1984): Morphology, growth, food habits and population (Reptilia, Serpentes, Colubridae). Revue Suisse de Zoologie 93: characteristics of the Smooth snake Coronella austriaca in 219–232. southern Britain. Journal of Zoology 204: 241–257. Sindaco, R., Venchi, A., Grieco, C. (2013): The Reptiles of the Groen, J. (2018): It’s a snake-eat-snake world: Predation on an Western Palearctic. 2. Annotated checklist and distributional adder (Vipera berus) by a smooth snake (Coronella austriaca) atlas of the snakes of Europe, North Africa, Middle East and in a nature reserve in the north of the Netherlands. Herpetology Central Asia, with an Update to Volume 1. Latina, Italy, Edizioni Notes 11: 729–731. Belvedere. Jofré, G.M., Reading, C.J. (2020): Cannibalism in smooth snakes, Speybroeck, J., Beukema, W., Bok, B., Van Der Voort, J. (2016): Coronella austriaca. Herpetological Journal 30: 168–172. Field Guide to the Amphibians & Reptiles of Britain and Europe. Kolanek, A., Pastrykiewicz, M., Borawski, W., Bury, S. (2020): London, England, United Kingdom, Bloomsbury Publishing Coronella austriaca (smooth snake) - mortality after prey Plc. ingestion. The Herpetological Bulletin 152: 32–33. Strugariu, A., Hutelac-Volosciuc, M.V., Dincă, P.C., Zamfirescu, Kreiner, G. (2007): The Snakes of Europe. Frankfurt, Germany, S.R., Sahlean, T.C. (2014): Smooth snake (Coronella austriaca) Edition Chimaira. predation on a live grass snake (Natrix natrix) in eastern Luiselli, L., Capula, M., Shine, R. (1996): Reproductive output, Romania. Herpetologica Romanica 8: 29–32. costs of reproduction, and ecology of the smooth snake, Uysal, I., Gül, C., Tosunoğlu, M. (2019): Breeding and Cannibalism Coronella austriaca, in the eastern Italian Alps. Oecologia 106: Behaviours of Captive Coronella austriaca (Colubridae) in a 100–110. Terrarium. Journal of the Institute of Science and Technology Moreira, P.L., Diamantino, J.L., Conde, J.C., Martins, F.A.F. 9: 1926–1930. (2011): Smooth snakes at an Iberian mountain isolate and Vanni, S., Zuffi, M.A.L. (2011): Hierophis viridiflavus.�� the relationship with compting southern smooth snakes. �� d’Italia, vol. XLV, Reptilia, p. 509-516. Corti, C., Capula, M., Herpetological Journal 21: 161–168. Luiselli, L., Sindaco, R., Razzetti, E., Eds, Bologna, Italy, Pardavila, X., Lamosa, A., Martínez-Freira, F. (2012): Primera cita Calderini. de depredación de Coronella austriaca sobre Vipera seoanei. Boletín de la Asociación Herpetológica Española 23: 60–61.

Accepted by Christoph Liedtke