Predation on Rhinella Mirandaribeiroi (Gallardo, 1965) (Anura; Bufonidae)
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Herpetology Notes, volume 10: 151-155 (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 Oliveira1,*, Marluci Baldo Fachi2, Diego Afonso Silva3 and Alessandro R. Morais4 Amphibians are important components in many food Australia and other Pacific islands (Frost, 2016). chains (Wells, 2007) as prey for diverse taxonomic Rhinella mirandaribeiroi (Gallardo, 1965) is a medium- groups, such as invertebrates, fishes, other amphibians, sized species included in the R. granulosa group reptiles, birds, and mammals (Toledo, 2005; Toledo (Narvaes and Rodrigues, 2009), and it is commonly et al., 2007). However, many amphibian species have distributed in Cerrado areas from Central Brazil and chemical defense against their predators (Wells, 2007); in enclaves of Cerrado in the Brazilian Amazon, as this includes the toads belonging to the genus Rhinella, the Noel Kampf National Park in Bolivia (Narvaes which possess highly toxic skin secretions (Ford and and Rodrigues, 2009). Herein, we reported a case of Cannatella, 1993). These secretions can be lethal when predation on R. mirandaribeiroi by a Neotropical snake a given predator ingests species of the genus Rhinella and, additionally, we provided a list reporting predation (Barbosa et al., 2009). But some species seem to be events for other 17 species of the genus Rhinella. immune to toxicity of these secretions, because they On 14 September 2011 at around 20:20h, we can ingest toads without major problems (Toledo et al., observed an adult Helicops angulatus (Linnaeus, 1758) 2007). consuming an adult R. mirandaribeiroi (Figure 1). The Currently, Rhinella is composed by 91 species, which event took place in a pond (18°00’42” S; 51°12’07” W; are naturally found in part of North America and Datum = WGS84; c. 667 m a.s.l.) located ~30 km from throughout Central and South Americas (Frost, 2016). Aparecida do Rio Doce county, Goiás state, Brazil. Only Rhinella marina (Linnaeus, 1758) is considered Three R. mirandaribeiroi individuals were vocalizing as invasive, because it was introduced in the Antilles, in the water when we observed the snake approaching Hawaii, Fiji, Philippines, Taiwan, New Guinea, 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 1 Programa de Pós-Graduação em Biodiversidade e study, we describe for the first time the predation of R. Conservação, Instituto Federal Goiano, Campus Rio Verde, mirandaribeiroi by H. angulatus. Helicops angulatus is 75901-970, Cx Postal 66, Rio Verde, GO, Brazil. widely distributed in Brazil (Roberto et al. 2009) and 2 Programa de Pós-Graduação em Ecologia e Conservação, Universidade do Estado de Mato Grosso Campus Nova among their food items are other bufonids, such as: Xavantina, 78690-000, Cx Postal 08 Nova Xavantina, MT, Rhinella margaritifera (Guimarães et al. 2010) and R. Brazil. marina (Kaefer and Montanarin, 2011). 3 Programa de Pós-Graduação em Ecologia e Conservação, In addition to the new case of predation described above, Universidade do Estado de Mato Grosso Campus Nova we searched the literature for studies that reported other Xavantina, 78690-000, Cx Postal 08 Nova Xavantina, MT, predation events on species from the genus Rhinella. In Brazil. 4 Instituto Federal Goiano, Campus Rio Verde, 75901-970, Cx this sense, our main strategy was to access the papers Postal 66, Rio Verde, GO, Brazil. published in the following journals: Herpetological * Corresponding author e-mail: [email protected] Review, Herpetology Notes and Herpetological 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 (table 1). Narvaes and Rodrigues (2009) conducted published until December 2016, using the combination an extensive review of the Rhinella granulosa group, of the following keywords: “predation”, “Rhinella”, therefore 9 (53%) out of 17 predation events reported “Bufo”, and “Chaunus”. Overall, we found 77 studies for R. granulosa could be assigned to other species of that reported predation events on 17 anuran species this group, since they were published before this review. of the genus Rhinella (table 1). Fifty-three species Finally, we found information available only for 18 have been recorded so far as predators of Rhinella (19%) out of 91 species of the genus Rhinella, therefore spp., being 41 reptiles, 12 mammals, 8 amphibians, 5 a knowledge gap is still evident. In this sense, our results birds, 3 fishes, 3 spiders, 2 crustaceans, 2 insects and contribute to the knowledge on natural history aspects one an annelid (table 1). The snakes Erythrolamprus for the species of this genus and could be useful to guide poecilogyrus poecilogyrus, Helicops angulatus, and future experimental and observational studies. Lygophis anomalus have been reported as predators for three different toad species (Table 1). Acknowledgments. ARM and SRO acknowledge FAPEG Until the present study, R. mirandaribeiroi was not (Fundação de Amparo à Pesquisa do Estado de Goiás) and CAPES reported as prey for other species; however R. granulosa, (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) a closely related species to R. mirandaribeiroi, has been for fellowships. Financial support was provided by FAPEG (n°: recorded as prey for more than 15 vertebrate species 201210267001108 and 201610267001018). 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 aO. 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 Lygophis anomalus Reptile Toledo et al. (2007)* Oxyptychus striatus Annelid Masetti et al. (2015) Rhinella cf. fernandezae Thamnodynastes hypoconia Reptile Bellini et al. (2013) Erythrolamprus poecilogyrus poecilogyrus Reptile Toledo et al. (2007)* Rhinella dorbignyi Lygophis anomalus 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) Lygophis anomalus Reptile Toledo et al. (2007)* 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) Leptodactylus macrosternum Amphibian Souza et al. (2016) Rhinella major 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) 154 Seixas Rezende Oliveira et al. Table 1. Continued. Prey species Predator specieV Major grouS5eference 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