Herpetology Notes, volume 10: 665-667 (2017) (published online on 23 November 2017)

Predation on the brilliant-thighed poison frog Allobates femoralis (Aromobatidae) by the Amazonian water snake Helicops angulatus (Dipsadidae)

Carlos Eduardo Costa-Campos1,*, Pedro Hugo Esteves Silva2, Luã Euriqui Santos Guerra1 and Jackson Cleiton Sousa1

Allobates femoralis (Boulenger, 1884) is a small Trinidad, Ecuador, French Guiana and northern and pan-Amazonian aromobatid frog widely distributed northeastern regions of Brazil (Roberto et al., 2009). It throughout the Amazon and Guianas in Colombia, usually feeds upon fish, frogs (Bufonidae, Hylidae and Ecuador, Peru, Bolivia, Brazil, French Guiana, Suriname Leptodactylidae, including eggs and tadpoles), aquatic and Guyana (Amézquita et al., 2009; Frost, 2017). lizards and earthworms (Martins and Oliveira, 1998; The species was considered a Batesian and Müllerian Silva Jr. et al., 2003; Guimarães et al., 2010; Kaefer and mimic of aposematic species of the dendrobatid frogs Montanarin, 2011; Rocha and López-Baucells, 2013; genera Ameerega and Adelphobates (Darst et al., 2006; Strüssmann et al., 2013; Teixeira et al., 2017). Amézquita et al., 2017). Here, we report a H. angulatus specimen containing Reproductive individuals of A. femoralis can have an adult A. femoralis in its gut. We captured the snake relatively large home ranges, occupying a variety at Cancão Municipal Natural Park, in the municipality of microhabitats for feeding and mating (Ringler et of Serra do Navio, State of Amapá, Brazil (0.90275°N; al., 2009; Ringler et al., 2012). Territorial males emit 52.00497°W; Datum = WGS84), an area that covers advertisement calls from elevated structures above the 370.26 hectares of Amazon forest. forest floor and defend nesting sites, while females Our register occurred on 22 April 2017, at 20:15 usually move through the habitat for choosing partners h, when a female H. angulatus (SVL = 519 mm; tail (Ringler et al., 2012). Males attend terrestrial eggs length = 198 mm; body mass = 115 g; Fig. 1) was deposited in a leaf nest until tadpoles emerge and are found in a shallow natural pool on a trail along an transported to a water body usually on the back of upland forest. The snake was euthanized with an the male (Lima et al., 2006). In all these reproductive intramuscular injection in the cervical region with 2 mL phases, males and females are exposed to predators. of the anaesthetic thiopental to check for endoparasite Adults are diurnal, and males vocalize in the afternoon, presence. The posterior dissection revealed a partially peaking between 15:00–16:00 h (Kaefer et al., 2012). digested adult of A. femoralis (SVL = 29.7 mm) in the Helicops angulatus (Linnaeus, 1758) is a semi- snake’s stomach. Judging by the body direction of the aquatic and primarily nocturnal dipsadid snake that frog, it was swallowed by the head. The ventral pattern inhabits ponds, streams and rivers of Venezuela, was still recognizable, which permitted the species Guiana, Suriname, Colombia, Brazil, Bolivia, Peru, identification (Fig.1). Frog and snake were initially preserved in 10% formalin and then stored in 70% ethanol and housed in the Herpetological collection of Laboratório de Herpetologia from Universidade Federal do Amapá, under the care of Carlos Eduardo Costa 1 Universidade Federal do Amapá, Departamento de Ciências Campos (CECCAMPOS 01247, 01248). Biológicas e da Saúde, Laboratório de Herpetologia. Macapá, In spite of being currently considered as part of a AP, Brazil, CEP: 68.903-419. Müllerian mimicry system (Amézquita et al., 2017), 2 Universidade Federal do Amapá, Departamento de Ciências Biológicas e da Saúde, Laboratório de Zoologia. Macapá, AP, very few records exist about what organisms actually Brazil, CEP: 68.903-419. prey on A. femoralis (see Ringler et al., 2010). Predation * Corresponding author e-mail: [email protected] risk is reduced in Müllerian mimics because their 666 Carlos Eduardo Costa-Campos et al.

Figure 1. Stomach contents of a Helicops angulatus with a partly digested Allobates femoralis at municipality of Serra do Navio, Amapá, Brazil. A. Allobates femoralis in the stomach contents. B. Partly digested A. femoralis and dorsal view of the H. angulatus. C. Partly digested A. femoralis and ventral view of the H. angulatus.

aposematic colouration resembles the conspicuous In sum, our observation adds evidence on the foraging colouration of unpalatable or toxic prey (Amézquita et behaviour in terrestrial habitats by this semi-aquatic al., 2017). In the study area, A. femoralis is the most snake and represents the first record of A. femoralis as abundant anuran species, being recorded calling in the prey to H. angulatus. forest floor during the day and co-occurring with a toxic species, A. pulchripecta (Costa-Campos et al., 2016). Acknowledgments. We thank Lucas Forti for the suggestions Previous research on the diet of H. angulatus reported on an earlier version of this manuscript. We also thank Instituto aquatic and terrestrial vertebrates as fish, anurans Chico Mendes de Conservação da Biodiversidade (ICMBio), (bufonids, hylids and leptodactylids) and lizards (teiids) Christoph Jaster (Parque Nacional Montanhas do Tumucumaque) as prey items (Martins and Oliveira, 1998; Albuquerque for the permits and the support in fieldwork. et al., 2013; Oliveira et al., 2017; Teixeira et al., 2017). Although this species is considered nocturnal, diurnally References active species that were present in the diet, such as A. Albuquerque, R.L., Laranjeiras, D.O., Protázio, A.S., Santana, D.J., femoralis, could indicate some diurnal foraging or Rodrigues, R., Mesquita, D.O., França, F.G.R. (2013): Helicops that such prey were captured while inactive at night angulatus (watersnake). Diet. Herpetological Review 44 (3): (Rodrigues et al., 2015; Teixeira et al., 2017). 522–523. Predation on Allobates femoralis by Helicops angulatus 667

Amézquita, A., Lima, A.P., Jehle, R., Castellanos, L., Ramos, O., Ringler, M., Ursprung, E., Hödl W. (2009): Site fidelity and patterns Crawford, A., Gasser, H., Hödl, W. (2009): Calls, colours, shape, of short-and long-term movement in the brilliant-thighed poison and genes: a multi-trait approach to the study of geographic frog Allobates femoralis (Aromobatidae). Behavioral Ecology variation in the Amazonian frog Allobates femoralis. Biological and Sociobiology 63: 1281–1293. Journal of the Linnean Society 98: 826–838. Ringler, M., Ursprung, E., Hödl, W. (2010): Predation on Amézquita, A., Ramos, O., González, M.C., Rodríguez, C., Medina, Allobates femoralis (Boulenger 1884; Anura: Aromobatidae) I., Simões, P.I., Lima, A.P. (2017): Conspicuousness, color by the colubrid snake Xenopholis scalaris (Wucherer 1861). resemblance, and toxicity in geographically diverging mimicry: Herpetology Notes 3: 301–304. The pan-Amazonian frog Allobates femoralis. Evolution 71 (4): Ringler, E., Ringler, M., Jehle, R., Hödl W. (2012): The female 1039–1050. perspective of mating in A. femoralis, a territorial frog with Costa-Campos, C.E., Lima, A.P., Amézquita, A. (2016): The paternal care – a spatial and genetic analysis. PLoS One 7: advertisement call of Ameerega pulchripecta (Silverstone, 1976) e40237. (Anura, Dendrobatidae). Zootaxa 4136 (2): 387–389. Roberto, I.J., Ribeiro, S.C., Delfino, M.M.S., Almeida, W.O. Darst, C.R., Cummings, M.E., Cannatella. D.C. (2006): A (2009): Reptilia, Colubridae, Helicops angulatus: distribution mechanism for diversity in warning signals: conspicuousness extension and rediscovery in the state of Ceará. Check List 5: versus toxicity in poison frogs. Proceedings of the National 118–121. Academy of Sciences USA 103: 5852–5857. Rocha, R., López-Baucells, A. (2013): Predation attempt of Frost, D.R. (2017): Amphibian Species of the World: an Online Hypsiboas boans (Anura: Hylidae) by Helicops angulatus Reference. Version 6.0. Available at: http://research.amnh.org/ (Squamata: Dipsadidae) with notes on defensive behavior. herpetology/amphibia/index.html. Accessed on 15 May 2017. Alytes 30: 1–4. Guimarães, J.A.R., Dias, E.J.R., Oliveira, A.R. (2010): Helicops Rodrigues, G.M., Maschio, G.F., Prudente, A.L.C. (2015): Snake angulatus (Watersnake). Diet and Reproduction. Herpetological assemblages of Marajó Island, Pará state, Brazil. Zoologia 33 Review 41 (1): 93. (1): e20150020. Kaefer, I.L., Montanarin, A. (2011): Helicops angulatus (South Santos, J.C., Cannatella, D.C. (2011): Phenotypic integration American Watersnake). Diet. Herpetological Review 42 (2): emerges from aposematism and scale in poison frogs. 291. Proceedings of the National Academy of Sciences 108: 6175– Kaefer, I.L., Montanarin, A., Costa. R.S., Lima, A.P. (2012): 6180. Temporal Patterns of Reproductive Activity and Site Attachment Silva Jr., N.J., Souza, I.F., Silva, W.V., Ribeiro, R.S.M., Costa, C., of the Brilliant-Thighed Frog Allobates femoralis from Central Valle, N.C., Silva, H.L.R. (2013): Helicops angulatus (Water- Amazonia. Journal of Herpetology 46 (4): 549–554. snake). Diet. Herpetological Review 34: 68. Lima, A.P., Magnusson, W.E., Menin, M., Erdtmann, L.K., Strüssmann, C., Brito, E.S., Marques, O.A.V. (2013): What do Rodrigues, D.J., Keller, C., Hodl, W. (2006): Guia de sapos da water snakes eat? First report of predation by a Neotropical Reserva Adolpho Ducke, Amazônia Central. Manaus, Editora Hydropsini snake on giant earthworms (Glossoscolecidae). Átemma. Salamandra 49 (1) 48–50. Martins, M., Oliveira, E. (1998): Natural history of snakes in Teixeira, C.C., Montag, L.F.A., Santos-Costa, M.C. (2017): Diet forests of the Manaus Region, Central Amazonia, Brazil. Composition and Foraging Habitat Use by Three Species of Herpetological Natural History 6: 78–150.Oliveira, S.R., Fachi, Water Snakes, Helicops Wagler, 1830, (Serpentes: Dipsadidae) M.B., Silva, D.A., Morais, A.R. (2017): Predation on Rhinella in Eastern Brazilian Amazonia. Journal of Herpetology 51 (2): mirandaribeiroi (Gallardo, 1965) (Anura; Bufonidae) by a 215–222. Neotropical snake, including a list with predation events for species of the genus Rhinella. Herpetology Notes 10: 151–155.

Accepted by Igor Kaefer