Herpetology Notes, volume 10: (2017) (published online on 19 April 2017)

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1 Herpetology Notes, volume 10: (2017) (published online on 19 April 2017) Predation on Rhinella mirandaribeiroi (Gallardo, 1965) (Anura; Bufonidae) by a Neotropical snake, including a list with predation events for species of the genus Rhinella Seixas Rezende Oliveira 1, *, Marluci Baldo Fachi 2, Diego Afonso Silva 3 and Alessandro R. Morais 4 Amphibians are important components in many food chains (Wells, 2007) as prey for diverse taxonomic groups, such as invertebrates, fishes, other amphibians, reptiles, birds, and mammals (Toledo, 2005; Toledo et al., 2007). However, many amphibian species have chemical defense against their predators (Wells, 2007); this includes the toads belonging to the genus Rhinella, which possess highly toxic skin secretions (Ford and Cannatella, 1993). These secretions can be lethal when a given predator ingests species of the genus Rhinella (Barbosa et al., 2009). But some species seem to be immune to toxicity of these secretions, because they can ingest toads without major problems (Toledo et al., 2007). Currently, Rhinella is composed by 91 species, which are naturally found in part of North America and throughout Central and South Americas (Frost, 2016). Only Rhinella marina (Linnaeus, 1758) is considered as invasive, because it was introduced in the Antilles, Hawaii, Fiji, Philippines, Taiwan, New Guinea, 1 Programa de Pós-Graduação em Biodiversidade e Conservação, Instituto Federal Goiano, Campus Rio Verde, , Cx Postal 66, Rio Verde, GO, Brazil. 2 Programa de Pós-Graduação em Ecologia e Conservação, Universidade do Estado de Mato Grosso Campus Nova Xavantina, , Cx Postal 08 Nova Xavantina, MT, Brazil. 3 Programa de Pós-Graduação em Ecologia e Conservação, Universidade do Estado de Mato Grosso Campus Nova Xavantina, , Cx Postal 08 Nova Xavantina, MT, Brazil. 4 Instituto Federal Goiano, Campus Rio Verde, , Cx Postal 66, Rio Verde, GO, Brazil. * Corresponding author seixasbiologia@gmail.com Australia and other Pacific islands (Frost, 2016). Rhinella mirandaribeiroi (Gallardo, 1965) is a mediumsized species included in the R. granulosa group (Narvaes and Rodrigues, 2009), and it is commonly distributed in Cerrado areas from Central Brazil and in enclaves of Cerrado in the Brazilian Amazon, as the Noel Kampf National Park in Bolivia (Narvaes and Rodrigues, 2009). Herein, we reported a case of predation on R. mirandaribeiroi by a Neotropical snake and, additionally, we provided a list reporting predation events for other 17 species of the genus Rhinella. On 14 September 2011 at around 20:20h, we observed an adult Helicops angulatus (Linnaeus, 1758) consuming an adult R. mirandaribeiroi (Figure 1). The event took place in a pond ( S; W; Datum = WGS84; c. 667 m a.s.l.) located ~30 km from Aparecida do Rio Doce county, Goiás state, Brazil. Three R. mirandaribeiroi individuals were vocalizing in the water when we observed the snake approaching the toads. The register of this predation lasted around two minutes, where we observed the snake capturing, subduing, and ingesting one of the toads. After the predation, the snake remained in the pond for a few minutes, but it was not collected by us. In the present study, we describe for the first time the predation of R. mirandaribeiroi by H. angulatus. Helicops angulatus is widely distributed in Brazil (Roberto et al. 2009) and among their food items are other bufonids, such as: Rhinella margaritifera (Guimarães et al. 2010) and R. marina (Kaefer and Montanarin, 2011). In addition to the new case of predation described above, we searched the literature for studies that reported other predation events on species from the genus Rhinella. In this sense, our main strategy was to access the papers published in the following journals: Herpetological Review, Herpetology Notes and Herpetological

2 152 Seixas Rezende Oliveira et al. Figure 1. Individual of Helicops angulatus capturing, subduing, and ingesting an adult of Rhinella mirandaribeiroi, Aparecida do Rio Doce, Goiás, Brazil. Bulletin. Additionally, we used Google to find papers published until December 2016, using the combination of the following keywords: predation, Rhinella, Bufo, and Chaunus. Overall, we found 77 studies that reported predation events on 17 anuran species of the genus Rhinella (table 1). Fifty-three species have been recorded so far as predators of Rhinella spp., being 41 reptiles, 12 mammals, 8 amphibians, 5 birds, 3 fishes, 3 spiders, 2 crustaceans, 2 insects and one an annelid (table 1). The snakes Erythrolamprus poecilogyrus poecilogyrus, Helicops angulatus, and Lygophis anomalus have been reported as predators for three different toad species (Table 1). Until the present study, R. mirandaribeiroi was not reported as prey for other species; however R. granulosa, a closely related species to R. mirandaribeiroi, has been recorded as prey for more than 15 vertebrate species (table 1). Narvaes and Rodrigues (2009) conducted an extensive review of the Rhinella granulosa group, therefore 9 (53%) out of 17 predation events reported for R. granulosa could be assigned to other species of this group, since they were published before this review. Finally, we found information available only for 18 (19%) out of 91 species of the genus Rhinella, therefore a knowledge gap is still evident. In this sense, our results contribute to the knowledge on natural history aspects for the species of this genus and could be useful to guide future experimental and observational studies. Acknowledgments. ARM and SRO acknowledge FAPEG (Fundação de Amparo à Pesquisa do Estado de Goiás) and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for fellowships. Financial support was provided by FAPEG (n : and ).

3 Predation on Rhinella mirandaribeiroi by a Neotropical snake 153 Table 1. Species from Rhinella genus and their respective predator species. *Information obtained from supporting information provided by Toledo et a. 2007). ** The predator died after ingesting prey. Prey species Predator species Major group Reference Rhinella abei Xenodon neuwiedii Reptile Maia et al. (2011) Erythrolamprus poecilogyrus poecilogyrus Reptile Toledo et al. (2007)* Rhinella arenarum Oxyptychus striatus Annelid Masetti et al. (2015) Rhinella cf. fernandezae Thamnodynastes hypoconia Reptile Bellini et al. (2013) Rhinella dorbignyi Erythrolamprus poecilogyrus poecilogyrus Reptile Toledo et al. (2007)* Rhinella granulosa Ceratophrys aurita Amphibian Toledo et al. (2007)* Leptodactylus podicipinus Amphibian Toledo et al. (2007)* Rhinella jimi Amphibian Toledo et al. (2007)* / Chaves et al. (2012) Guira guira Bird Mesquita (2009) Theristicus caudatus Bird Toledo et al. (2007)* Megadytes (Bofurcitus) lherminieri Insect Zina et al. (2012) Caiman crocodilus Reptile Toledo et al. (2007)* Erythrolamphus melanotus Reptile Toledo et al. (2007)* Erythrolamprus miliaris merremii Reptile Toledo et al. (2007)* Erythrolamprus poecilogyrus poecilogyrus Reptile Toledo et al. (2007)* / Santos et al. (2010) Leptodeira annulata Reptile Morais and Ávila (2007) / Santos-Silva et al. (2014) Philodryas patagoniensis Reptile Toledo et al. (2007)* Salvator merianae Reptile Almeida et al. (2015) Xenodon merremii Reptile Ribeiro and Freire (2012) Xenodon rabdocephalus Reptile Costa et al. (2015) Phoneutria sp. Spider Silva-Silva et al. (2013) Atelerix pruneri Mammal Toledo et al. (2007)* Chrysocyon brachyurus Mammal Toledo et al. (2007)* Rhinella icterica Procyon cancrivorus Mammal Toledo et al. (2007)* Pseudechis porphyriacus Reptile Toledo et al. (2007)* Thamnodynastes strigatus Reptile Rufatto et al. (2009) Athene cunicularia Bird Protazio et al. (2011) Rhinella jimi Procyon cancrivorus Mammal Santos (2009) Xenodon merremii Reptile Fernandes-Ferreira et al. (2010) Rhinella limensis Philodryas tachymenoides Reptile Barboza et al. (2016) Rhinella major Leptodactylus macrosternum Amphibian Souza et al. (2016) Lycalopex gymnocercus Mammal Schalk and Morales (2012) Rhinella gr. nargaritifera Rhinella marina Amphibian Fróis et al. (2015) Rhinella cf. margaritifera Erythrolamprus typhlus typhlus Reptile Kollarits et al. (2013) Erythrolamprus epinephelus Reptile Toledo et al. (2007)* Rhinella margaritifera Erythrolamprus reginae macrosomus Reptile Toledo et al. (2007)* Helicops angulatus Reptile Guimarães et al. (2010) Tyto alba Bird Calderón-Patrón et al. (2012) Didelphis marsupialis Mammal Toledo et al. (2007)* Galictis vittata Mammal Toledo et al. (2007)* Hemiechinus auritus Mammal Toledo et al. (2007)* Melomys burtoni Mammal Cabrera et al. (2015) Rhinella marina Rattus colletti Mammal Cabrera et al. (2015) Rattus tunneyi Mammal Cabrera et al. (2015) Apalone ferox Reptile Flaherty and Fries (2013) Boiga irregularis Reptile Toledo et al. (2007)* Caiman crocodilus Reptile Batista et al. (2011)

4 154 Seixas Rezende Oliveira et al. Table 1. Continued. Prey species Predator specie Major grou eference Crocodilus amazonicus Reptile Toledo et al. (2007)* Crocodylus acutus Reptile Beaty and Beaty (2012) Erythrolamprus epinephelus Reptile Toledo et al. (2007)* Rhinella marina Helicops angulatus Reptile Kaefer and Montanarin (2011) Hidroginastes gigas Reptile Costa et al. (2015) Stegonotus cucullatus Reptile Wilson et al. (2014)** Xenodon rabdocephalus Reptile Costa et al. (2015) Rhinella mirandaribeiroi Helicops angulatus Reptile Present study Leptodactylus latrans Amphibian Bovo et al. (2014) Procambarus clarkii Crustacean Banci et al. (2013) Trichodactylus fluviatilis Crustacean Segadilha and Silva-Soares (2015) Rhinella ornata Hoplias cf. malabaricus Fish Toledo et al. (2007)* Salminus brasiliensis Fish Almeida et al. (2009) Lycosa erythrognatha Spider Almeida et al. (2010) Rhinella pombali Lithobates catesbeianus Amphibian Da Silva et al. (2010) Labidus sp. Spider Gomides et al. (2011) Rhiinella gr. proboscídea Erythrolamprus typhlus Reptile Prado et al. (2016) Rhinella proboscidea Philodryas argenteus Reptile Toledo et al. (2007)* Ceratophrys aurita Amphibian Silva-Soares et al. (2016)** Guira guira Bird Briso et al. (2013) Rhinella schneideri Paleosuchus palpebrosus Reptile Toledo et al. (2007)* Salvator merianae Reptile Toledo et al. (2007)* Xenodon merremi Reptile Aroztegui et al. (2008) Rhinella yunga Lethocerus sp. Insect Tortorelli et al. (2016) Rhinella scitula Rhamdia quelen Fish Severo-Neto and Sugai (2014) References Almeida, R.P.S., Lima, J.O., Dias, E.J.R. (2015): Salvator merianae (Tegu). Diet. Herpetological Review 46(3): 436. Almeida, S.C., Agostinho, C.A., Souza, R.M.R. (2009): Rhinella jimi (Cururu Toad) and Leptodactylus vastus (Northeastern Pepper Frog). Predation on bats. Herpetological Review 40(2): Almeida, S.C., Messas, Y.F., Cicchi, P.J.P. (2010): Predation on newly metamorphosed toad Rhinella ornata (Anura: Bufonidae) by the spider, Lycosa erythrognatha (Araneae: Lycosidae). Herpetology Notes 3: Aroztegui A., Álvarez B., Céspedez J. (2008): Waglerophis merremi (False Yarara) Diet. atural History Notes. Herpetological Review 39(4): 475. Banci, K.R.S., Viera, N.F.T., Marinho, P.S., Calixto, P. O., Marques, O.A.V. (2013): Predation of Rhinella ornata (Anura, Bufonidae) by the alien crayfish (Crustacea, Astacidae) Procambarus clarkii (Girard, 1852) in São Paulo, Brazil. Herpetology Notes 6: Barbosa, C.M., Medeiros, M.S., Costa, C.C.M.R., Camplesi, A.C., Sakate, M. (2009): Toad poisoning in three dogs: Case reports. J. Venom Anim Toxin incl Trop Dis 15(4): Barboza, A.C., Pradel, R., Aybar, D., Muñoz, J.M., Venegas, P.J. (2016): Philodryas simonsii (Schmidt s Racer) and Philodryas tachymenoides (Schmidt s Green Racer). Reprodution and Diet. Herpetological Review 47(4): 688. Batista, V.B.G.V., Morato, S.A.A., Paz, A. (2011): Caiman crocodilus (Spectacled Caiman). Prey. Herpetological Review 42(2): 269. Beaty, L., Beaty, S. (2012): Rhinella marina (Cane Toad). Crocodile predation. Herpetological Review 43(3): 471. Bellini, G.P., Arzamendia, V., Giraudo, A.R. (2013): Ecology of Thamnodynastes hypoconia in subtropical temperate South America. Herpetologica 69: Bovo, R.P., Bandeira, L.N., Condez, T.H. (2014): Rhinella ornata (Mexican Spadefoot). Predation by Leptodactylus latrans. Herpetological Review 45(1): 115. Briso, A.L.F., Oda, F.H., Campos, V.A. (2013): Rhinella schneideri (Cururu Toad). Predation. Herpetological Review 44(1): Cabrera, G.E., Crossland, M.R., Pearson, D., Webb, J.K., Shine, R. (2015). Predation on invasive cane toads (Rhinella marina) by native Australian rodents. Journal of Pest Science 88(1): Calderón-Patrón, J.M., Valencia-Herverth, J., Muría-Manzano, R., Andrés-Perez, L. (2012): Rhinella marina (Cane Toad). Predation. Herpetological Review 43(1): 125.

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Herpetological Bulletin 119: Accepted by Mirco Solé