Herpetology Notes, volume 14: 945-947 (2021) (published online on 29 June 2021)

“Lady and the Tramp”: aff. braestrupi (: ) as prey of two Erythrolamprus miliaris (Serpentes: Dipsadidae)

Letícia Leitão-Martins*,¹, Lucas Rosado Mendonça², Carlos Henrique De-Oliveira-Nogueira³, Hender Lélis Rezende Maciel¹, and Leonardo Serafim da Silveira¹

Gymnophiona () is the least known Amphibia Brazil (Gans, 1964; Dixon, 1983). Presenting diurnal order, which can be related with the predominant and nocturnal habits, it is a generalist species associated fossoriality of most species (Nussbaum and Wilkinson, with humid environments (Marques et al., 2001). Its 1989; Gower and Wilkinson 2005). Typhlonectidae diet covers a wide variety of and fishes, (Taylor, 1968) includes the semi-aquatic and aquatic although lizards, and even a mammal have caecilians of South America from five known genera already been registered as prey for this species (Araujo, (Wilkinson and Nussbaum, 2006; Wilkinson et al., 2011; 1985; Marques and Souza, 1993; Palmuti et al., 2009; Maciel, 2016): (Nussbaum & Wilkinson, Vrcibradic et al., 2012; Batista et al., 2019). A recent 1995), Chthonerpeton (Peters, 1880), overview by van den Burg (2020) shows that 77% of (Taylor, 1968), Potamotyphlus (Taylor, 1968) and its diet is based primarily on amphibians, but a single (Peters, 1880). The genus Chthonerpeton record for Gymnophiona was found. currently includes eight species, seven of which are As individuals of the same species generally acquire present in Brazil (Napoli et al., 2015). Only one species similar resources to survive and reproduce, intraspecific of the genus, Chthonerpeton braestrupi (Taylor, 1968), competition may alter their reproductive success is registered for the state of Rio de Janeiro (Dorigo et (Rinkevick and Loya, 1985; Begon et al., 2007). al., 2018), although the of the Chthonerpeton Although intraspecific interactions can occur indirectly, from this region is still in review and might soon result intraspecific competition usually occurs directly in a new species (Maciel, 2016). between individuals that defend territories (Begon et al., Erythrolamprus miliaris (Linnaeus, 1758) is a dipsadid 2007). Predation of Chthonerpeton viviparum Parker & widely distributed throughout South America, Wettstein, 1929 by E. miliaris has already been reported occurring in Argentina, Bolivia, Brazil, Colombia, in the literature (Albolea, 1998; Chicarino et al., 1998; Ecuador, French Guiana, Guyana, Peru, Suriname, and Marques and Sazima, 2004). However, here we include Venezuela (Wallach et al., 2014; Nogueira et al., 2020). a novel prey species to the list (van den Burg, 2020) It is considered as a common species in southeastern and report the first intraspecific competition event of two individuals of E. miliaris for one individual of Chthonerpeton aff. braestrupi. On 20 December 2019, we found two Erythrolamprus ¹ Núcleo de Estudos e Pesquisas em Animais Selvagens, miliaris simultaneously preying on a single Laboratório de Morfologia e Patologia , Universidade while performing fieldwork in a Restinga area, in the Estadual do Norte Fluminense, Av. Alberto Lamego, 2000, Reserva Particular do Patrimônio Natural (RPPN) 28013-602 Campos dos Goytacazes, Rio de Janeiro, Brazil. Caruara, in the municipality of São João da Barra, Rio 2 Departamento de Biologia, Programa de Pós-graduação em de Janeiro State, Brazil. The snakes were located in a Zoologia, Av. Gen. Rodrigo Otávio Jordão Ramos 6200, 69080-900 Manaus, Amazonas, Brazil. puddle on a dirt road at the edge of a flooded area, while ³ Instituto de Biociências, Universidade Federal de Mato disputing and trying to swallow the prey from opposite Grosso do Sul, Cidade Universitária, 79002-970 Campo ends (Fig. 1). The dispute generated lacerations in Grande, Mato Grosso do Sul, Brazil. the caecilian which exposed eggs in its final third of * Corresponding author. E-mail: [email protected] the body, allowing to determine the individual as a © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. female. We observed the event for five minutes, until 946 Letícia Leitão-Martins et al.

Figure 1. Predation attempt of two Erythrolamprus miliaris individuals (arrows) on a single Chthonerpeton aff. braestrupi in the RPPN Fazenda Caruara, São João da Barra, Rio de Janeiro State, Brazil. Photo by Carlos Henrique de Oliveira Nogueira. the moment when one of the snakes halted its predation al., 1998; Marques and Sazima 2004), our record is not attempt. Both snakes were collected, with the caecilian surprising. However, we highlight the dispute between still in the mouth of one of the snakes, which eventually two individuals of the same species and of different sexes was released in the collection bag. All individuals were over a poorly studied species. Intraspecific competition deposited in the herpetological collection of the Núcleo events might be difficult to observe in fieldwork, de Estudos e Pesquisas em Animais Selvagens (NEPAS) but it has been registered for some snakes (Himes of the Universidade Estadual do Norte Fluminense 2003; Flores et al., 2010; Escalona, 2012), and might Darcy Ribeiro (UENF) under the vouchers: HNF 850: indicate a shortage of resources in the region (Begon E. miliaris, male, snout-vent length (SVL) = 59.8 cm; et al., 2007). Such competition can drive ecological HNF 851: E. miliaris, female, SVL = 66.3 cm; HNF variations, forcing them to seek new resources, acquire 849: C. aff. braestrupi, female, SVL = 32.4 cm. After greater sexual dimorphism, or even provoke speciation sexing both snakes, we found that it was the male that (Bolnick 2004; Svanback and Bolnick, 2006). first released the caecilian. The caecilian was identified This record expands our knowledge on natural history by the Gymnophiona specialist Adriano Maciel based and trophic relationships of Erythtrolamprus miliaris on the number of primary annuli and the position of the and Chthonerpeton aff. braestrupi; on the other hand, tentacles. it highlights the scarcity of basic ecological data for Predation records of Chthonerpeton aff. braestrupi neotropical caecilians. are rare. The species is preyed upon by the coral snake Acknowledgement. We thank the project “Herpetofauna do Micrurus corallinus (Merrem, 1820) (Gonzales et al., Norte Fluminense” (ICMBio/SISBIO capture permit # 72011-1) 2018). Since Erythrolamprus miliaris has a generalist for allowing the fieldwork. We are grateful to Adriano Maciel for diet and is known to prey Chthonerpeton viviparum helping us with the identification of the caecilian and suggestions Parker & Wettstein, 1929, (Albolea, 1998; Chicarino et for the improvement of the manuscript. We would like to thank Chthonerpeton aff. braestrupi as prey of two Erythrolamprus miliaris 947 the managers of RPPN Fazenda Caruara for their authorisation Marques, O.A.V., Eterovic, A., Sazima, I. (2001): Serpentes and support for conducting research in the area. da Mata Atlântica: guia ilustrado para a Serra do Mar. Holos Editora. References Marques, O.A.V., Sazima, I. (2004): História natural dos répteis da estação ecológica Juréia-Itatins. In: Marques, O.A.V. Duleba, W. Albolea, A.B.P. (1998): Padrões de atividade em serpentes (Eds), Estação ecológica Juréia-Itatins. Ambiente Físico, Flora e não peçonhentas de interesse medico: Helicops modestus Fauna. Holos Editora. (Colubridae: Xenodontinae) e Liophis miliaris (Colubridae: Marques, O.A.V., Souza, V.C. (1993): Nota sobre a atividade Xenodontinae) e sua relação com a epidemologia. Unpublished alimentar de Liophis miliaris no ambiente marinho. Revista MSc thesis, Universidade de Guarulhos, Guarulhos, Brazil. Brasileira de Biologia 53: 645–648. Araújo, A.F.B. (1985): Partilha de recursos em uma guilda Napoli, M.F., Soeiro, M., Trevisan, C.C., Silva, R.M.L. (2015): de lagartos de restinga (Sauria). Unpublished MSc thesis, New record of Chthonerpeton noctinectes da Silva, Britto- Department of Zoology, UNICAMP, Campinas, Brazil. Pereira and Caramaschi, 2003 (Gymnophiona, Typhlonectidae) Batista, S.F., Facure, K.G., Marques, O.A.V. (2019): First record of from the Monte Cristo Island, Todos-os-Santos Bay, Bahia State, mammal consumption by Erythrolamprus miliaris. How wide is northeastern Brazil. Herpetology Notes 8: 4–45. the diet of this water snake? Herpetology Notes 12: 713–715. Nogueira, C.C., Argôlo, A.J.S., Arzamendia, V., et al. (2020): Atlas Begon, M., Townsend, C.R., Harper, J.L. (2007): Ecologia – De of brazilian snakes: Verified point-locality maps to mitigate indivíduos a ecossistemas. Fourth edition. Porto Alegre, Rio the Wallacean Shortfall in a megadiverse snake fauna. South Grande do Sul, Brazil. Artmed. American Journal of Herpetology 14: 1–274. Bolnick, D.I. (2004): Can intraspecific competition drive disruptive Nussbaum, R.A., Wilkinson, M. (1989): On the classification and selection? An experimental test in natural populations of phylogeny of caecilians (Amphibia: Gymnophiona), a critical Sticklebacks. Evolution 58: 608–618. review. Herpetological Monographs 3: 1–42. Chicarino, M.S., Endo, W., Marques, O.A.V. (1998): Atividade, Palmuti, C.F.S., Cassimiro, J., Bertoluci, J. (2009): Food habits of ciclo reprodutivo e dieta da cobra-d’água Liophis miliaris, snakes from the RPPN Feliciano Miguel Abdala, and Atlantic na porção sul da Mata Atlântica. In: Congresso Brasileiro de Forest Fragment of southeastern Brazil. Biota Neotropica 9: Zoologia, Recife. Resumos, pp. 271–272. 263–269. Dixon, J.R. (1983): Taxonomic status of the South American Rinkevich, B., Loya, Y. (1985): Intraspecific competition in a snakes Liophis miliaris, L. amazonicus, L. chrysostomus, L. reef coral: Effects on growth and reproduction. Oecologia 66: mossoroensis and L. purpurans (Colubridae: Serpentes). Copeia 100–105. 3: 791–802. Svanback, R. and Bolnick, D.I. (2006): Intraspecific competition Dorigo, T.A., Vrcibradic, D., Rocha, C.F.D. (2018): The amphibians drives increased resource use diversity within a natural of the state of Rio de Janeiro, Brazil: an updated and commented population. Proceeding the Royal Society B. 274: 839–844. list. Papéis Avulsos de Zoologia. 58: 1–12. van den Burg, M.P. (2020): How to source and collate natural Escalona, M. (2012): Cannibalism of Liophis lineatus history information: a case study of reported prey items of (Linnaeus)(Serpentes: Colubridae) in natural conditions. Erythrolamprus miliaris (Linnaeus, 1758). Herpetology Notes Herpetotropicos 7: 35–37 13: 739–746. Flores, E., Jadin, R.C., Orlofske, S.A. (2010): Helicops polylepis Vrcibradic, D., Niemeyer, J., Figueiredo, C.A. (2012): Liophis (Norman’s Keelback). Diet and intraspecific competition. miliaris (Watersnake). Diet. Herpetological Review 43: 147– Herpetological Review 41: 93–94. 148. Gans, C. (1964): A redescription of, and geographic variation in, Wallach, V., Williams, K. L., Boundy, J. (2014): Snakes of the Liophis miliaris Linné, the common water snake of southeastern World. A catalogue of living and extinct species. First Edition. South America. American Museum Novitates 2178: 1–58. Boca Raton, Florida, USA, CRC Press. Gonzales, R.C., Faustino, D., Prado, P., Quinhones, R., Salles, Wilkinson, M., Nussbaum, R.A. (2006): Caecilian phylogeny and R.O.L. (2018): Regurgitating Micrurus corallinus (Serpentes, classification. In: J. M. Exbrayat (ed.), Reproductive Biology Elapidae) reveals another records for the rare caecilian and Phylogeny of Gymnophiona (Caecilians). Enfield, Science Chthonerpeton aff. braestrupi (Gymnophiona, Typhlonectidae). Publisher, Inc., USA. Herpetology Notes 11: 663–665. Wilkinson, M., San Mauro, D., Sherrat, E., Gower, D.J. (2011): Gower, D.J., Wilkinson, M. (2005): Conservation biology of A nine-family classification of caecilians (Amphibia: caecilian amphibians. Conservation Biology 19: 45–55. Gymnophiona). Zootaxa 2874: 41–64. Himes, J.G. (2003): Intra- and interspecific competition among the Water Snakes Nerodia sipedon and Nerodia rhombifer. Journal of Herpetology 37: 126–131. Maciel, A.O. (2016): Sistemática e evolução das cecílias aquáticas (Amphibia: Gymnophiona: Typhlonectidae) com base no estudo de variação morfológica, genética e filogenia molecular. Unpublished PhD thesis, Universidade Federal do Pará, Belém, Accepted by Renato C. Nali Brasil.