Herpetology Notes, volume 12: 1169-1171 (2019) (published online on 11 November 2019)

First case of opportunistic cannibalism in brasiliensis (Steindachner, 1864) (Anura: )

Walter F. Periard Jr.¹,* and Matheus S. França¹

Anurans play an important role in trophic interactions of Auricchio & Salomão (2002), and dissected via a as predators and prey (Duellman and Trueb, 1986; ventral incision to access the stomach and investigate Siqueira et al., 2006; Wells, 2007; de Oliveira et al., its contents (Figure 2a), from which we removed a 2018), including regularly reported incidences of smaller, partially digested C. brasiliensis, confirming cannibalism (e.g. Pombal, 2007; Toledo et al., 2007; that the larger of the two had indeed consumed Measey et al., 2015; Carmo and Woitovicz-Cardoso, the smaller (Figure 2b). The larger had snout- 2018). The genus Cycloramphus Tschudi, 1838 (Amphibia, Anura) comprises 28 species endemic to the southeastern Brazilian rainforest. Cycloramphus brasiliensis (Steindachner, 1864) (Figure 1) occurs at elevations of 150–1200 m and is found only in the Atlantic Rainforest of Serra dos Órgãos and Serra da Mantiqueira, in the state of Rio de Janeiro (Carvalho- e-Silva et al. 2004; Maia-Carneiro et al., 2012a; Rocha et al., 2015; Frost, 2018). Its diet is known to comprise insects including ants, cockroaches, and beetles, as well as other arthropods such as arachnids and gastropods (Maia-Carneiro et al., 2012b). During fieldwork on 22nd September 2017 in Reserva Ecológica de Guapiaçu, Rio de Janeiro, we collected two anurans identified as C. brasiliensis, as per the description of Heyer (1983). One animal was noticeably larger than the other, and both were placed in the same collection bag. Upon inspection approximately three hours after collection, only the larger of the two frogs remained, and this animal presented an enlarged stomach not apparent at the time of collection. The bag had remained closed, it was thus considered unlikely that the smaller individual had escaped. The remaining specimen was euthanized according to the protocol

Figure 2. Stomach and stomach contents of Cycloramphus ¹ Departamento de Vertebrados, Setor de Herpetologia, Museu brasiliensis (MNRJ 91886) showing the ventral incision and Nacional, Quinta da Boa Vista, São Cristóvão, Rio de distended stomach (A), and the smaller, partially digested Janeiro, RJ – CEP: 20940-040. C. brasiliensis cannibalized by MNRJ 91886 in the same * Corresponding author. E-mail: [email protected] collection bag, and recovered from its stomach contents (B). 1170 Walter F. Periard Jr. & Matheus S. França

Figure 1. Cycloramphis brasiliensis in life. Specimen MNRJ 92506 (not this study) in dorsolateral (A) and ventral (B) view. Images courtesy of Setor de Herpetologia, Museu Nacional, UFRJ (MNFoto 92506_07 and 92506_13: Pedro Pinna).

vent length of 57.7 mm, and although we omitted to specimens were collected under permit number 13088-9 from perform an internal inspection for sexual characteristics, Instituto Chico Mendes de Conservação da Biodiversidade. this specimen was assumed to be female given the size- based dimorphism reported for other Cycloramphus References taxa (Brasileiro et al., 2007; Weber et al., 2011). The Auricchio, P., Salomão, M.G. (2002): Tecnicas de preparação e specimen and its stomach contents were fixed in 10% coleta de vertebrados para fins cientificos e didáticos. Instituto formalin, stored in 70% alcohol, and deposited in the Pau Brasil de Historia Natural. Herpetological Collection of the Departamento de Brasileiro, C.A., Haddad, C.F.B., Sawaya, R.J., Sazima, I. (2007): A new and threatened island-dwelling species of Cycloramphus Vertebrados, Museu Nacional, Universidade Federal do (Anura: Cycloramphidae) from southeastern Brazil. Rio de Janeiro (MNRJ 91886). Herpetologica 63: 501–510. Although we consider the enforced proximity of the Carmo, L.F.F., Woitovicz-Cardoso, M. (2018): Spoiling friendship: two frogs in our study to be an atypical (i.e. unnatural) First report on predation of anuran by Aparasphenodon brunoi situation, to our knowledge this is the first report of (i) Miranda-Ribeiro, 1920 (Anura: Hylidae). Herpetology Notes vertebrate prey consumption and (ii) cannibalism in 11: 375–377. the diet of C. brasiliensis. The only previous dietary Carvalho-e-Silva, S.P., Heyer, R. (2004): Cycloramphus brasiliensis. The IUCN Red List of Threatened Species 2004: e. study of C. brasiliensis indicated an arthropod prey- T56361A11467337. http://dx.doi.org/10.2305/IUCN.UK.2004. base but had limited sampling (n = 11) (Maia-Carneiro RLTS.T56361A11467337.en. Accessed on 17 September 2018. et al., 2012b). However, cannibalism has been reported Duellman, W.E., Trueb, L. (1986): Biology of . in this genus (adult predation on post-metamorphic C. Baltimore, Johns Hopkins University Press. boraceiensis Heyer 1983) (Kakazu, 2009), indicating Frost, D.R. (2018): Species of the World: an Online that further dietary investigations of cycloramphid frogs Reference. Version 6.0. Available at http://research.amnh.org/ are necessary in order to fully understand the range of herpetology/amphibia/index.html. Accessed on 11th September 2018. prey items, and proclivity toward cannibalism in this Heyer, W. (1983): Variation and systematics of frogs of the genus family. Cycloramphus (Amphibia, ). Arquivos de Zoologia São Paulo 30: 235–339. Acknowledgments. We thank our external reviewer William Kakazu, S. (2009): Dieta de Cycloramphus boraceiensis (Anura; Vaz as well as Renan M. de Oliveira for suggestions and critical Cycloramphidae) em riachos da Mata Atlântica, litoral norte review of a previous version of this manuscript. We thank José do Estado de São Paulo, sudeste do Brasil. Tese de BSc não Pombal for allowing access to laboratory resources at Museu publicada, Universidade Estadual Paulista “Júlio de Mesquita Nacional, Universidade Federal do Rio de Janeiro, and the support Filho” Instituto de Biociências – Rio Claro. of collection managers Pedro Pinna and Manoela Woitovicz. We Maia-Carneiro, T., Dorigo, T.A., Almeida-Gomes, M., Van are grateful to Nicholas J. Locke from Reserva Ecológica de Sluys, M. & Rocha, C.F.D. (2012a): New altitudinal records Guapiaçu for making the facility available during our fieldwork, of the endemic species Cycloramphus brasiliensis (Anura, and D. Geber for the opportunity to carry out fieldwork. The Cycloramphidae) from the Atlantic Rainforest in the state of Rio First case of opportunistic cannibalism in Cycloramphus brasiliensis 1171

de Janeiro, southeastern Brazil. Brazilian Journal of Biology 72: 225–226. Maia-Carneiro, T., Dorigo, T.A., Almeida-Gomes, M., Van Sluys, M., & Rocha, C.F.D. (2012b): Feeding habits, microhabitat use, and daily activity of Cycloramphus brasiliensis (Anura: Cycloramphidae) from the Atlantic Rainforest, Brazil. Zoologia (Curitiba) 29: 277–279. Measey, G.J., Vimercati, G., De Villiers, F.A., Mokhatla, M.M., Davies, S.J., Edwards, S., Altwegg, R. (2015): eat frog: exploring variables influencing anurophagy. PeerJ 3: e1204. de Oliveira, R. M., Schilling, A. C., Solé, M. (2018): Trophic ecology of two Pithecopus species (Anura: Phyllomedusidae) living in syntopy in southern Bahia, Brazil. Studies on Neotropical Fauna and Environment 54: 10–21. Pombal Jr, J.P. (2007): Notas sobre predação em uma taxocenose de anfíbios anuros no sudeste do Brasil. Revista Brasileira de Zoologia 24: 841–843. Rocha, C.F.D., Siqueira, C.C., Ariani, C.V., Vrcibradic, D., Guedes, D.M., Kiefer, M.C., Almeida-Gomes, M., Goyannes-Araújo, P., Borges-Júnior, V.N.T., Van Sluys, M. (2015): Differential success in sampling of Atlantic Forest amphibians among different periods of the day. Brazilian Journal of Biology 75: 261–267. Siqueira, C.C., Van Sluys, M., Ariani, C.V. & Rocha C.F.D. (2006): Feeding ecology of miliaris (Anura, Cycloramphidae) in four areas of Atlantic Rain Forest, southeastern Brazil. Journal of Herpetology 40: 520–525. Toledo, L.F., Ribeiro, R.S., Haddad, C.F.B. (2007): Anurans as prey: an exploratory analysis and size relationships between predators and their prey. Journal of Zoology 271: 170–177. Weber, L.N., Verdade, V.K., Salles, R.D.L., Fouquet, A., De Carvalho-e-Silva, S.P. (2011): A new species of Cycloramphus Tschudi (Anura: Cycloramphidae) from the Parque Nacional da Serra dos Órgãos, southeastern Brazil. Zootaxa 2737: 19–33. Wells, K.D. (2007): The Ecology and Behavior of Amphibians. Chicago, The University of Chicago Press.

Accepted by Jim Labisko