sign in sign up
<<
Home , Bahia, Philodryas nattereri

Herpetology Notes, volume 14: 843-846 (2021) (published online on 31 May 2021)

The short life of a juvenile neotropical : a record of cannibalism in nattereri (Steindachner, 1870)

Alcéster Diego Coelho-Lima1,2,*, Dâmela Teixeira Cardoso2,3, and Daniel Cunha Passos1,4

Cannibalism, the consumption of conspecific known aspects of its natural history. Its generalist diet individuals, is a behaviour widely recorded among (Sales et al., 2020) includes primarily vertebrates, (e.g., Fox, 1975; Polis, 1981), with records mainly (Vitt, 1980), but also anurans (Guedes in several groups, including invertebrates (Polis and et al., 2018), (Mesquita et al., 2010), Farley, 1979; Baur, 1990), ray-finned fishes (Forney, (Mesquita et al., 2011), and (Coelho-Lima 1976; Boldt et al., 2012), mammals (Bygott, 1972; et al., 2019). Nevertheless, up to now there was no Dorward, 2015), and (Bernarde and Abe, record of cannibalism for this . In this report, 2010; Barros et al., 2011). Among snakes, cannibalism we describe the first case of P. nattereri preying a reports were historically considered opportunistic conspecific individual. events (e.g., Braz et al., 2006), commonly associated On 17 January 2018 at approximately 13:00 h, during with dietary generalists (Polis and Myers, 1985). fieldwork at Moita dos Porcos, Caetité Municipality, However, it has also been suggested that cannibalism Bahia State, northeastern (14.1581°S, in snakes has a high energy advantage for the cannibal 42.5172°W, elevation 1022 m), we collected a female (Cundall and Greene, 2000; Lourdais et al., 2005), a P. nattereri (snout–vent length, SVL = 831 mm; tail fact that can explain the relatively high frequency of length, TL = 328 mm, Fig. 1) in a high-elevation these behaviours in several families (e.g., Boidae – habitat dominated by grasses, with few Barros et al., 2011; – Wiseman et al., 2019; trees and shrubs scattered, locally named campo sujo Dipsadidae – Morais et al., 2020; Elapidae – Maritz et (Munhoz and Felfili, 2006). After being placed in a al., 2019; Viperidae – Freiria et al., 2006). transport container, the snake regurgitated a juvenile The mid-sized dipsadid snake Philodryas nattereri conspecific (SVL = 315 mm, TL = 135 mm, Fig. 1). (Steindachner, 1870) is a species widely distributed The prey was still alive after regurgitation, had multiple in open areas of (Guedes et al., 2014). bite marks along its trunk and tail, and presented with It is diurnal, terricolous, shows sexual dimorphism peeling of dorsal scales consistent with the action of with females being larger than males (Passos et al., the predator’s palatal teeth (Fig. 2). Both specimens 2014), and its trophic ecology is one of the best- were properly euthanized with 5% lidocaine, fixed in 10% formalin, preserved in 70% ethanol, and deposited in the Coleção Herpetológica do Semiárido (CHSA) at the Universidade Federal Rural do Semi-Árido 1 Laboratório de Ecologia e Comportamento , under accession numbers CHSA R 763 (predator) and Universidade Federal Rural do Semi-Árido, Mossoró, Rio CHSA R 764 (prey). The taxonomic determination of Grande do Norte 59625-900, Brazil. both specimens as P. nattereri was made by checking 2 Laboratório de Ecologia do Semiárido, Departamento de chromatic (typical brown colour pattern) and meristic Ciências Humanas, Universidade do Estado da Bahia, (21–21–17 dorsal scale rows) diagnostic characters Caetité, Bahia 46400-000, Brazil. (Vanzolini et al., 1980). 3 Laboratório de Estudo Animal, Departamento de Ciências Humanas, Universidade do Estado da Bahia, Caetité, Bahia Cannibalism has been previously recorded for other 46400-000, Brazil. dipsadid snakes, including Erythrolamprus miliaris 4 Departamento de Biociências, Centro de Ciências Biológicas (Braz et al., 2006), Lygophis dilepis (Escalona, 2012), e da Saúde, Universidade Federal Rural do Semi-Árido, Oxyrhopus clathratus (Maia and Travaglia-Cardoso, Mossoró, 59625-900, Brazil. 2017), Thamnodynastes phoenix (Morais et al., 2020), * Corresponding author. E-mail: [email protected] and even in Pseudablabes patagoniensis (previously © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. Philodryas patagoniensis; Pontes et al., 2002; Hartmann 844 Alcéster Diego Coelho-Lima et al.

Figure 1. Adult female (above) and juvenile (below) Philodryas nattereri from Caetité, Bahia, Brazil. The juvenile (CHSA R 764) was preyed upon by the adult (CHSA R 763). and Marques, 2005; Melo-Sampaio et al. 2020). Cardoso, 2017). Although cannibalism in snakes Although ophiophagous behaviour had already been sometimes occurs between adult individuals (e.g., documented in P. nattereri (Oxybelis aeneus – Mesquita Capella et al., 2011), mothers are well known to and Borges-Nojosa, 2009; Leptodeira annulata – ingest their non-viable eggs or neonates (Mitchell Guedes, 2017; Oxyrhopus trigeminus – Coelho-Lima and Groves, 1993), and maternal cannibalism may be et al., 2019; Lygophis dilepis – Sales et al., 2020), the a beneficial strategy to obtain energy after the period present record is the first case of cannibalism reported of high reproductive demand (Lourdais et al., 2005; for this species. Mociño-Deloya et al., 2009). In cannibalism, predatory individuals are generally The event reported herein included a female P. larger than their prey (Polis, 1981) and in nature, nattereri much larger than the minimum reproductive cannibalism is an important source of mortality for size reported for the species (Mesquita et al., 2011) several species, which may have density-dependent and a small juvenile (Passos et al., 2014). Likely effects in cases of low resource availability or in explanations include that a larger individual simply contexts of high intraspecific competition (Siqueira fed on a smaller conspecific (following the general and Rocha, 2008; Maritz et al., 2019). On the other trend noted by Polis, 1981), or that this event hand, a lot of cannibalism happens in captivity, either constitutes maternal cannibalism (see Lourdais et al., between neonates or between parents and their young, 2005; Mociño-Deloya et al., 2009). However, since the possibly influenced by the environmental stress to relatedness of the involved individuals is unknown, it which captive snakes are subjected (Cardoso-Junior is not possible to determine the actual scenario. et al., 1990; Braz et al., 2006; Maia and Travaglia- Until quite recently, ophiophagy in P. nattereri had Cannibalism in Philodryas nattereri 845 been considered occasional (Mesquita and Borges- References

Nojosa, 2009; Guedes, 2017) but the most recent Barros, M.M., Draque, J.F., Micucci, P.A., Waller, T. (2011): records (Coelho-Lima et al., 2019; Sales et al., Natural history notes. Eunectes notaeus (Yellow Anaconda). 2020) suggest that ophiophagy is more common in Diet / cannibalism. Herpetological Review 42(2): 290–291. P. nattereri than thought, as has been suggested for Baur, B. (1990): Possible benefits of egg cannibalism in the other snakes (Maritz et al., 2019). Our finding expands land snail Arianta arbustorum (L.). Functional Ecology 4(5): the knowledge on the trophic ecology in Philodryas, 679–684. Bernarde, P.S., Abe, A.S. (2010): Hábitos alimentares de serpentes and we hope that this record contributes to push em Espigão do Oeste, Rondônia, Brasil. Biota Neotropica forward the understanding on behavioural ecology of 10(1): 167–173. neotropical snakes. Boldt, J.L., Buckley, T.W., Rooper, C.N., Aydin, K. (2012): Factors influencing cannibalism and abundance of walleye Acknowledgments. We thank Rhamon Malheiro, Bruna Moura pollock (Theragra chalcogramma) on the Eastern Bering Sea and Vitória Santos for their help during our fieldwork, Guilherme Shelf, 1982–2006. Fishery Bulletin 110: 293–306. Souza, resident of Moita dos Porcos locality, for the receptivity Braz, H.B.P., Lopes, P.H., Rocha, M.M.T., Furtado, M.F.D. and logistical support during field activities, Lander Alves for (2006): Liophis miliaris (Common Water Snake). Cannibalism. assistance with the phytosociological description of the area, Herpetological Bulletin 97: 36–37. Paulo Machado for his critical review of a previous version of Bygott, J.D. (1972): Cannibalism among wild chimpanzees. this manuscript, and Daniela Pareja Mejía and the anonymous Nature 238: 410–411. reviewer for the valuable suggestions in our text. We also thank Capella, J., Mateo, J.A., Mayol, J., Pleguezuelos, J.M. (2011): Instituto Chico Mendes de Conservação da Biodiversidade for Canibalismo en Macroprotodon mauritanicus en la isla de authorizing the zoological material collection license (license Mallorca. Boletín de la Asociación Herpetológica Española number 9292-1). ADCL thanks FAPERN and CAPES (Finance 22: 44–46. Code – 001) for providing a graduate (masters) scholarship. Cardoso-Junior, R.P., Lula, L.A.B.M., Iwasaki, M., Oliveira, S.M. (1990): Análise radiológica na ofiofagia de filhote de serpente alternatus (Viperidade, Crotalinae). Memórias do

Figure 2. Multiple body injuries of a juvenile Philodryas nattereri (CHSA R 764) after having been swallowed by a larger conspecific in Caetité, Bahia, Brazil. The black arrows indicate some bite scars from the first third of the trunk to the post cloacal region. 846 Alcéster Diego Coelho-Lima et al.

Instituto Butantan 52: 63–68. C.H. (2011): Ecology of Philodryas nattereri in the Brazilian Coelho-Lima, A.D., Filho, J.M.O., Passos, D.C. (2019): Natural semi-arid region. The Herpetological Journal 21(3): 193–198. history notes. Philodryas nattereri (Paraguay Green Racer). Mitchell, J.C., Groves, J.D. (1993): Intraspecific oophagy in Diet. Herpetological Review 50: 601. reptiles. Herpetological Review 24: 126–130. Cundall, D., Greene, H.W. (2000): Feeding in snakes. In: Feeding: Mociño-Deloya, E., Setser, K., Pleguezuelos, J.M., Kardon, A., Form, Function, and Evolution in Tetrapod Vertebrates, p. Lazcano, D. (2009): Cannibalism of nonviable offspring by 293–333. Schwenk, K, Ed., San Diego, California, USA, postparturient Mexican lance-headed rattlesnakes, Crotalus Academic Press. polystictus. Animal Behaviour 77(1): 145–150. Dorward, L.J. (2015): New record of cannibalism in the common Morais, M.D.S.R., Araújo, P.F., , R.M.T., França, F.G.R. hippo, Hippopotamus amphibius (Linnaeus, 1758). African (2020): First record of cannibalism in Thamnodynastes phoenix Journal of Ecology 53(3): 385–387. Franco, Trevine, Montingelli & Zaher, 2017 (Serpentes, Escalona, M. (2012): Cannibalism of Liophis lineatus (Linnaeus) Colubridae). Herpetozoa 33: 17–19. (Serpentes: Colubridae) in natural conditions. Herpetotropicos Munhoz, C.B.R., Felfili, J.M. (2006). Fitossociologia do estrato 7(1–2): 35–37. herbáceo-subarbustivo de uma área de campo sujo no Distrito Forney, J.L. (1976): Year-class formation in the walleye Federal, Brasil. Acta Botanica Brasilica 20(3): 671–685. (Stizostedion vitreum vitreum) population of Oneida Lake, Passos, D.C., Mesquita, P.C.M.D., Rocha, B.A.L., Borges- New York, 1966–73. Journal of the Fisheries Board of Canada Nojosa, D.M. (2014): Dissimilar ab ovo: sexual dimorphism 33(4): 783–792. of Philodryas nattereri Steindachner, 1870 hatchlings and Fox, L.R. (1975): Cannibalism in natural populations. Annual juveniles. Herpetozoa 26(3/40): 178–180. Review of Ecology and Systematics 6(1): 87–106. Polis, G.A., Farley, R.D. (1979): Behavior and ecology of Freiria, F.M., Brito, J.C., Avia, M.L. (2006): Ophiophagy mating in the cannibalistic scorpion, Paruroctonus mesaensis, and cannibalism in Vipera latastei Boscá, 1878 (Reptilia, Stahnke (Scorpionida: Vaejovidae). Journal of Arachnology Viperidae). Herpetological Bulletin 96: 26–28. 7(1): 33–46. Guedes, T.B. (2017): Natural history notes. Philodryas nattereri Polis, G.A., Myers, C.A. (1985): A survey of intraspecific (Paraguay Green Racer). Diet. Herpetological Review 48(3): predation among reptiles and . Journal of 679–680. Herpetology 19: 99–107. Guedes, T.B., Nogueira, C., Marques, O.A.V. (2014): Diversity, Polis, G.A. (1981): The evolution and dynamics of intraspecific natural history, and geographic distribution of snakes in the predation. Annual Review of Ecology and Systematics 12(1): , northeastern Brazil. Zootaxa 3863(1): 1–93. 225–251. Guedes, T.B., Sazima, I., Marques, O.A.V. (2018): Does Pontes, G.M.F., Oliveira, R.B., Di-Bernardo, M.; Borges-Martins, swallowing a toad require any specialisation? Feeding M. (2003): Natural history notes. Philodryas patagoniensis behaviour of the dipsadid snake Philodryas nattereri on the (Papa-pinto). Cannibalism. Herpetological Review 34(2): bufonid toad Rhinella jimi. Herpetology Notes 11: 825–828. 154–154. Hartmann, P.A., Marques, O.A.V. (2005): Diet and habitat use Sales, R.F.D., Sousa, J.D., Lisboa, C.M.C., Marinho, P.H., Freire, of two sympatric species of Philodryas (Colubridae) in South E.M.X., Kokubum, M.N.D.C. (2020): New dietary records Brazil. Amphibia-Reptilia 26: 25–31. and geographic variation in the diet composition of the snake Lourdais, O., Brischoux, F., Shine, R., Bonnet, X. (2005): Philodryas nattereri in Brazil. Cuadernos de Herpetología Adaptive maternal cannibalism in snakes (Epicrates cenchria 34(2): 285–293. maurus, Boidae). Biological Journal of the Linnean Society Siqueira, C.C., Rocha, C.F.D. (2008): Predation by lizards as a 84(4): 767–774. mortality source for juvenile lizards in Brazil. South American Maia, D.C., Travaglia-Cardoso, S.R. (2017): Oxyrhopus Journal of Herpetology 3(1): 82–87. clathratus (Serpentes: Dipsadidae): reproduction and Vanzolini, P.E., Ramos-Costa, A.M.M., Vitt, L.J. (1980): Répteis cannibalism. Oecologia Australis 21(2): 197–200. das . , Brazil, Academia Brasileira de Maritz, B., Alexander, G.J., Maritz, R.A. (2019): The Ciências. underappreciated extent of cannibalism and ophiophagy in Vitt, L.J. (1980): Ecological observations on sympatric African cobras. Ecology 100(2): e02522. Philodryas (Colubridae) in northeastern Brazil. Papéis Avulsos Melo-Sampaio, P.R., Passos, P., Martins, A.R., Moura-Leite, de Zoologia 34(5): 87–98. J.C., Morato, S.A., Venegas, P.J., et al. (2020): A phantom Wiseman, K.D., Greene, H.W., Koo, M.S., Long, D.J. (2019): on the trees: integrative supports a reappraisal of Feeding ecology of a generalist predator, the California rear-fanged snakes classification (Dipsadidae: Philodryadini). kingsnake (Lampropeltis californiae): why rare prey matter. Zoologischer Anzeiger 290: 19–39. Herpetological Conservation and Biology 14(1): 1–30. Mesquita, P.C.M.D., Borges-Nojosa, D.M. (2009): Philodryas nattereri (Paraguay Green Racer): Ophiophagy. Herpetologial Bulletin 108: 36–37. Mesquita, P.C.M.D., Borges-Nojosa, D.M., Monteiro, F.A.R. (2010): Natural history notes. Philodryas nattereri (Paraguay Accepted by Daniela Pareja Mejía Green Racer). Diet. Herpetological Review 41(1): 96. Mesquita, P.C.M.D., Borges-Nojosa, D.M., Passos, D.C., Bezerra,