Herpetology Notes, volume 13: 361-363 (2020) (published online on 03 May 2020)

Report of new predator-prey interactions of Erythrolamprus miliaris (Linnaeus, 1758)

Matthijs P. van den Burg1,* and Ingrid R. Miguel2

Neotropical form one of the most biodiverse preferences (e.g. Michaud and Dixon, 1989; Sazima groups of herpetofauna, making up an important part and Haddad, 1992; Martins et al. 1993; Rocha and of their ecosystems (Guedes et al., 2018). Information Vrcibradic, 1998; Mattos et al., 2016; Batista et al., about their dietary niche and trophic level provides 2019). Overall, these reports indicate that prey mainly important knowledge to our understanding of these concern of and fish, with more rare complex systems. Such data can be collected through reports of reptilian and mammalian prey items. Despite field observations (e.g. Zobel et al., 2018; Sellmeijer this high diversity of reported prey species, its wide and van den Burg, 2020), stomach, faeces or intestine geographical occurrence and time-demanding effort contents (Marques et al., 2006; Bellini et al., 2015; to collect observational data suggest many unreported Unger et al., 2020), and also through the assessment of prey species remain to be identified. camera trap footage (Akcali et al., 2019). Direct field Here, we report two observations of E. miliaris observations of predator-prey as well as other intra- feeding behaviour involving unreported prey species and interspecies interactions are important to help to made during night field surveys for improve our knowledge about species niches, as well as anceps (Lutz, 1929) behaviour at Rebio União, in the their conservation. state of Rio de Janeiro, Brazil (GPS: -22.42723°N, - Erythrolamprus miliaris (Linnaeus, 1758) is a 42.03722°W). These observations were recorded in common South American dipsadid with a large a natural pond with aquatic plant vegetation mostly geographical distribution (Dixon 1983, 1989; Nogueira consisting of Juncus sp. and Typha domingensis. On 27 et al., 2019a,b). Locally it occurs in water-rich October 2019, at 20:48 h, we observed an E. miliaris near bodies of running or standing water (both fresh strike, capture, and consume an adult Dendropsophus and brackish-saline water), and it is active both during elegans (Wied-Neuwied, 1824) (Fig. 1A). The individual the day and night (Sazima and Haddad, 1992; Marques of D. elegans was sitting on a stem of Juncus sp. at and Souza, 1993). E. miliaris is regarded as a diet about 4 cm above the water surface, as the was generalist that consumes live prey without constriction nearby foraging while actively tongue-flickering. Upon or envenomation (but see Sazima and Strüssmann recognition of the prey, the snake lashed towards it and [1990] and Gomes et al. [2017] for necrophagy reports). struck it on the lateral side of the head. Subsequently, Numerous studies have contributed with observational the snake adjusted the prey so to swallow it head-first. evidence to the current knowledge of its broad diet This whole event took about 2.5 min. The other event took place on 28 October 2019, at 22:01 h, as we observed another E. miliaris capture and prey on an adult Dendropsophus anceps (Fig. 1B). Precisely, while observing the D. anceps individual at about 45 cm above the water surface, we noticed a 1 Department of Biogeography and Global Change, Museo nearby failed predation attempt by an E. miliaris on a Nacional de Ciencias Naturales, Consejo Superior de D. elegans that was positioned 55 cm above the water Investigaciones Científicas, C/ José Gutiérrez Abascal 2, surface on a Juncus sp. stem. The snake paused for 28006 Madrid, Spain. about 20 s, and then started tongue flickering again, 2 Universidade Federal do Rio de Janeiro, Museu Nacional, Departamento de Vertebrados, Setor de Herpetologia, Quinta continuing foraging by turning around towards the D. da Boa Vista, 20940-040, Rio de Janeiro, RJ, Brazil. anceps. After a short movement, the snake noticed the * Corresponding author. E-mail: [email protected] D. anceps and lashed towards it, striking it on the lateral 362 Matthijs P. van den Burg & Ingrid R. Miguel

Figure 1. Two events of Erythrolamprus miliaris predation on (A) Dendropsophus elegans, and (B) on D. anceps, both at Rebio União, Rio de Janeiro state, Brazil.

of the body. Similarly, to the previous predation event, Batista, S.F, Facure, K.G., Marques, O.A.V. (2019): First record of the snake adjusted its prey so to consume it head-first, mammal consumption by Erythrolamprus miliaris. How wide is which took 6 min to complete. In both cases, prey items the diet of this water snake? Herpetology Notes 12: 713–715. Bellini, G.P., Giraudo, A.R., Arzamendia, V., Etchepare, E.G. held on to the nearby vegetation during the event (Fig. (2015): Temperate snake community in South America: is 1). diet determined by phylogeny or ecology? PLoS ONE 10: This report further strengthens the importance of e0123237. prey within the diet of E. miliaris, adding two Brasileiro, C.A., Sawaya, R.J., Kiefer, M.C., Martins, M. (2005): species of Dendropsophus, with only Dendropsophus Amphibians of an open Cerrado fragment in southeastern Brazil. minutus reported before our observations (Sazima and Biota Neotropica 5: 93–109. Haddad, 1992). Given the high Brazilian amphibian Campos, F.S, Brito, D., Solé, M. (2014): Diversity patterns, research trends and mismatches of the investigative efforts to diversity (Brasileiro et al., 2005; Jenkins et al., 2013, amphibian conservation in Brazil. Anais da Academia Brasileira 2015; Campos et al., 2014), the current number of de Ciências 86: 1873–1886. reported amphibian prey species for E. miliaris is likely Dixon, J.R. (1983): Taxonomic status of the South American a vast underestimation of the true amphibian diversity snakes miliaris, L. amazonicus, L. chrysostomus, L. predated by this generalist feeder. mossoroensis and L. purpurans (: Serpentes). Copeia 3: 791–802. Acknowledgements. We thank Manoela Woitovicz Cardoso and Dixon, J.R. (1989): A key and checklist to the Liophis with Laryssa Santos for helping during fieldwork, which was performed country lists and maps. Smithsonian Herpetological Information under permit # 68467-3, granted by Reserva Biológica União 79: 1–43. and Instituto Chico Mendes de Conservação da Biodiversidade Gomes, D.F., Gonzalez, R.C., Silva-Soares, T. (2017): (ICMBio). We thank Coordenação de Aperfeiçoamento de pessoal Erythrolamprus miliaris (Linnaeus, 1758) (Serpentes: de Nível Superior (CAPES) and Fundação de Amparo a Pesquisa Dipsadidae): report on an unusual event of necrophagy. do Estado do Rio de Janeiro (FAPERJ) for financial support. Herpetology Notes 10: 417–419. Guedes, T. B., Sawaya, R. J., Zizka, A., Laffan, S., Faurby, S., References Pyron, R. A. et al. (2018): Patterns, biases and prospects in the distribution and diversity of Neotropical snakes. Globale Akcali, C.K., Pérez-Mendoza, H.A., Salazar-Valenzuela, D., Ecology and Biogeography 27: 14–21. Kikuchi, D.W., Guayasamin, J.M., Pfenning, D.W. (2019): Jenkins, C.N., Pimm, S.L., Joppa, L.N. (2013): Global patterns of Evaluating the utility of camera traps in field studies of terrestrial vertebrate diversity and conservation. Proceedings of predation. PeerJ 7: e6487. the National Academy of Sciences 110: 2602–2610. Report of new predator-prey interactions of Erythrolamprus miliaris 363

Jenkins, C.N., Alves, M.A.S., Uezu, A., Vale, M.M. (2015): Rocha, C.F.D., Vrcibradic, D. (1998): as predators of Patterns of vertebrate diversity and protection in Brazil. PLoS vertebrates and as preys in a resting of southeastern ONE 10: e0145064. Brazil. Ciência e Cultura 50: 364–368. Marques, O.A.V., Sawaya, R.J., Stender-Oliverra, F., Franca, F.G.R. Sazima, I., Haddad, C.F.B. (1992): Répteis da Serra do Japi: notas (2006): Ecology of the colubrid snake Pseudablabes agassizii sobre história natural. In: História Natural da Serra do Japi. in south-eastern South America. Herpetological Journal 16: Ecologia e Preservação de uma area florestal no sudeste do 37–45. Brasil, pp. 212–231. Morellato, L.P.C., Ed., Campinas, BRA, Marques, O.A.V., Souza, V.C. (1993): Nota sobre atividade Editora da Unicamp/FAPESP. alimentar de Liophis miliaris no ambiente marinho (Serpentes, Sazima, I., Strüssmann, C. (1990): Necrofagia em serpents Colubridae). Revista Brasileira de Biologia 53: 645–648. brasileiras: exemplos e Previsões. Revista Brasileira de Biologia Martins, M., Sazima, I., Silvia, G.E. (1993): Predators of the nest 50: 463–468. building gladiator , Hyla faber, in southeastern Brazil. Sellmeijer, B., van den Burg, M.P. (2020): Tadpole predation in the Amphibia-Reptilia 14: 307–309. chemically defended Oophaga pumilio (Anura: Dendrobatidae) Mattos, R.O., Lauvers, W.D., Mônico, A.T. (2016): Erythrolamprus by Oxybelis aeneus (: Colubridae). Herpetology Notes miliaris (Cobra D’água; Military Ground Snake). Diet. 13: 301–303. Herpetological Review 47: 682. Unger, S.D., Bodinof-Jachowski, C., Diaz, L., Williams, L. (2020): Michaud, E.J., Dixon, J.R. (1989): Prey items of 20 species of Adult female Eastern hellbender Cryptobranchus alleganiensis the neotropical colubrid snake genus Liophis. Herpetological (Cryptobranchidae) conspecific cannibalism confirmed via Review 20: 39–41. DNA barcoding. Herpetology Notes 13: 169–170. Nogueira, C.C., Argôlo, A.J.S., Arzamendia, V., Azevedo, J.A., Zobel, M., van Wagensveld, T.P., Madden, H., van den Burg, M.P. Barbo, F.E., Bérnils, B.E. et al. (2019a): Atlas of Brazilian (2018): Orange-bellied racer (Alsophis rufiventris); diet and snakes: verified point-locality maps to mitigate the Wallacean arboreality. The Herpetological Bulletin 144: 26–28. shortfall in megadiverse snake fauna. South American Journal of Herpetology 14: 1–274. Nogueira, C., Cisneros-Heredia, D.F., Gonzales, L., Schargel, W., Rivas, G. (2019b): Erythrolamprus miliaris. The IUCN Red List of Threatened Species 2019: e.T44581708A44581717. Downloaded on 30 October 2019.

Accepted by Rodrigo Gonzalez