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Home , Chironius, Chironius carinatus, Chironius exoletus, Chironius flavolineatus, Chironius multiventris, Chironius scurrulus

Herpetology Notes, volume 13: 1-5 (2020) (published online on 08 January 2020)

Review of prey items recorded for of the (, ), including the first record of Osteocephalus as prey

Igor Joventino Roberto1,2* and Aline Ramos Souza1

The Neotropical sipo snakes of the genus Chironius 1971; Rodriguez and Duellman, 1994; Jungfer, 2010). include 22 of diurnal, actively foraging snakes The other similar species of Osteocephalus that occurs (Dixon et al., 1993; Kok, 2010; Fernandes and Hamdan, in the same area, O. oophagus, have shorter hind limbs 2014; Hamdan and Fernandes, 2015). They are mostly (tibia length 19.5–31.2 mm; foot length: 13.8–22.5 mm), batrachophagous but will also prey upon , , and the frontoparietals flanges are not visible (Jungfer and rodents (Cunha and Nascimento, 1978; Dixon and and Schiesari, 1995). Soini, 1986; Duellman, 2005). We collected information is a diurnal that forages regarding Chironius spp. prey items from the literature in terrestrial and arboreal environments (Martins and to assess the level of dietary specialization within the Oliveira, 1999; Dixon et al., 1993). It occurs in both genus. Here, we summarize this information and report primary and secondary forests (Dixon et al., 1993). The the first record of Osteocephalus as prey for these scarce information on diet in this species comes mainly snakes. from the eastern Pará state and , and anurans are On 3 January 2018 we found a recently road-killed reported as the most common prey item (Trachycephalus, female Chironius multiventris (Snout-vent length 128.5 , , Scinax cf. x-signatus and cm, tail length 78.0 cm) at the Vila de Balbina in the “Hyla”), followed by lizards (Tropidurus, Anolis and municipality of Presidente Figueiredo, Amazonas State Polychrus) (Cunha and Nascimento, 1978; Cunha and (01°56’ 24.96”S, 59°27’22.93”W). The specimen was Nascimento, 1982; Dixon and Soini, 1986; Dixon et al., deposited in the Zoological Collection Prof. Paulo 1993; Rodrigues et al., 2015). Since C. multiventris is Bührnheim, Universidade Federal do Amazonas, a diurnal snake species, and O. taurinus has nocturnal Manaus, (CZPB-RP 1017). While examining the habits, the event may have occurred when O. gut contents, we found a prey item that has not been taurinus was resting in an arboreal refuge during the reported in the diet of this snake species. day. The specimen found in the stomach of C. multiventris A literature search performed using Google Scholar, was identified as Osteocephalus taurinus by the presence Scielo, Herpetological Review and books covering the of green bones, lateral edges of the frontoparietals elevated diet and natural history of Chironius spp. produced and forming distinct ridges (visible frontoparietals information for 18 species of Chironius (Table 1). flanges), dorsal surfaces of tibia and foot with brown No information on diet was found for C. brazili, C. transversal bands, and tibia length (38.93 mm) and foot challenger, C. diamantina or C. maculoventris. The length (26.55 mm) (Trueb, 1970; Trueb and Duellman, majority of prey items reported from species of Chironius are anurans representing 72 species from 12 families, with a predominance of hylids and leptodactylids. Chironius flavopictus, C. laevicollis, C. leucometapus, C. laurenti, C. septentrionalis, C. vicenti, and C. spixii have only had anurans reported as dietary components. 1 Programa de Pós-Graduação em Zoologia, Universidade Two species of Bolitoglossa salamanders are recorded, Federal do Amazonas, Manaus, Amazonas 69077–000, but only in C. fuscus and C. grandisquamus Brazil. . Lizards 2 Florida Museum of Natural History, University of Florida, are the second most diverse prey item, with 12 species Gainesville, Florida 32611, USA. from six families having been recorded in the diets of * Corresponding author. E-mail: [email protected] seven species of Chironius. Followed by birds, that 2 Igor Joventino Roberto & Aline Ramos Souza

Table 1. List of prey items recorded for Chironius spp in literature and in this study; (X = prey items identified taxonomically in literature only until Class level).

Species Birds Mammals References Muller, 1969; Sazima and Haddad, Boana faber, Bokermannohyla hylax, Scinax 1992; Martins et al., 1993; Dixon et al., sp, Leptodactylus latrans, Leptodactylus gr. Hemidactylus 1993; Marques and Sazima, 2004; Chironius bicarinatus X latrans, , Ischnocnema sp, mabouia Oliveira, 2008; Hartmann et al., 2009a, Ischnocnema guenteri, Thoropa miliaris. Hartmann et al., 2009b; Almeida et al., 2018; Vrcibradic and Eisfeld, 2016. Mole and Urich, 1891; Mole and Boana boans, Itapotihyla langsdorffii, Pseudis Cnemidophorus Urich, 1894; Wehekind, 1955; Dixon et X Rodentia paradoxa. lemniscatus al., 1993; Silva et al., 2010; Bovo and Sueiro, 2012; Rodrigues et al., 2015. Bolitoglossa altamazonica, Dendropsophus Dixon and Soini, 1977; Duellman, bifurcus, Dendropsophus marmoratus, Boana 1978; Cunha and Nascimento, 1982; albopunctata, Boana geographica, Boana Hemidactylus Sazima and Haddad, 1992; Dixon et lanciformis, Boana punctata, Ecnomiohyla mabouia, al., 1993; Castanho, 1996; Marques miliaria, Itapotihyla langsdorffii, Thecadactylus and Sazima, 2004; Rodrigues, 2005; Phyllomedusa distincta, Phyllomedusa rapicauda, Anolis França et al., 2008; Hartmann et al., tomopterna, Scinax garbei, Scinax ruber, sp, Urostrophus 2009b; Bernarde and Abe, 2010; Trachycephalus mesophaeus, Leptodactylus vautieri. Rodrigues et al., 2015; Santos-Costa et latrans, Pristimantis sp, Thoropa taophora, al., 2015; Marques et al., 2016; Hudson Lithobates palmipes, Tadpole (not identified). et al., 2019. Boana albopunctata, Boana bischofii, Boana Dixon et al., 1993; Pombal Jr, 2007; raniceps, Bokermannohyla alvarengai, Scinax França et al., 2008; Pinto et al., 2008; Hemidactylus cf. fuscovarius, Scinax cf. x-signatus, Scinax Rodrigues et al., 2015; Marques et al., mabouia gr. ruber, Leptodactylus fuscus, Physalaemus 2016; Passos et al., 2017; Aximoff et cf. cuvieri, Thoropa miliaris, Thoropa sp. al., 2017. Phyllomedusa sp, Smilisca phaeota, Chironius flavopictus Leptodactylus pentadactylus, Leptodactylus Dixon et al., 1993. poecilochilus, Pristimantis sp. Boana faber, Bokermannohyla circumdata, Dixon et al., 1993; Marques, 1998; Bokermannohyla hylax, Itapotihyla Drymophila Chironius foveatus Rocha et al., 1999; Hartmann et al., langsdorffii, , Proceratophrys squamata 2009b; Rodrigues and Noronha, 2014. appendiculata. Bolitoglossa sp, Allobates sp, Phyllobates sp, Dendropsophus sp, Boana multifasciata, Beebe, 1946; Dixon and Soini, 1977; Ololygon argyreornata, Scinax sp, Kentropyx sp, Ayarzaguena, 1987; Dixon et al., 1993; Trachycephalus typhonius, Leptodactylus Anolis sp, Martins and Oliveira, 1999; Marques fuscus, Leptodactylus petersii, Leptodactylus Chironius fuscus X Rodentia Gonatodes and Sazima, 2004; Hartmann et al., mystaceus, Leptodactylus cf. wagneri, humeralis, 2009b; Palmuti et al., 2009; Physalaemus cf. ephippifer, Haddadus Gonatodes sp. Nascimento et al., 2013; Muscat et al., binotatus, Pristimantis sp, Ischnocnema sp, 2017; Silva-Ferreira et al., 2017. Thoropa miliaris, Thoropa taophora, Adelophryne gutturosa. Bolitoglossa sp, Leptodactylus savagei, Myrmeciza Dixon et al., 1993; McCranie, 2011; Chironius grandisquamis Pristimantis sp, Strabomantis bufoniformis. exsul Visco and Sherry, 2015. Dixon et al., 1993; Hartmann et al., Chironius laevicollis Leptodactylus latrans. 2009. Chironius laurenti Anurans Marques et al., 2005.

Chironius leucometapus Leptodactylidae. Dixon et al., 1993.

Proctoporus or Chironius monticola , Leptodactylidae. Euspondylus, Dixon et al., 1993. Anolis sp Anolis Osteocephalus taurinus, Trachycephalus sp, fuscoauratus, Dixon and Soini, 1977; Cunha and Chironius multiventris Leptodactylus spp, Scinax x-signatus, Polychrus Nascimento, 1982; Dixon et al., 1993; Pristimantis spp. marmoratus, Rodrigues et al., 2015; This study. Tropidurus hispidus Boana albopunctata, Boana cf. lundii, Scinax Schupp, 1913; Amaral, 1918, Amaral, nasicus, Scinax fuscovarius, Scinax ruber, 1933; Gliesch, 1925; Dixon et al., Chironius quadricarinatus Scinax sp, Leptodactylidae, Physalaemus cf. X X 1993; França et al., 2008; Pinto et al., fuscomaculatus, Physalaemus cf. cuvieri, 2008. Physalaemus cuvieri. Boana lanciformis, Boana xerophylla, Boana Dixon and Soini, 1977; Duellman, sp, Phyllomedusa camba, Scinax gr.ruber, 1978; Cunha and Nascimento, 1993; Leptodactylus knudseni, Leptodactylus Dixon et al., 1993; Martins and pentadactylus, Leptodactylus mystaceus, Oliveira, 1999; Bernarde and Abe, Leptodactylus cf. wagneri. 2010; Silva et al., 2010. Chironius septentrionalis Hylidae, Leptodactylidae. X Dixon et al., 1993.

Boana xerophylla, Leptodactylus gr. latrans, Chironius spixii Dixon et al., 1993. Pristimantis sp, Elachistocleis pearsei. Pristimantis shrevei, Pristimantis sp, Henderson et al., 1988; Henderson and Chironius vincenti Eleutherodactylus johnstonei, Powell, 2009. Eleutherodactylus spp.

Review of prey items recorded for snakes of the genus Chironius 3 were recorded in the diet of six species of Chironius. References

Unidentified rodents were recorded only for Chironius Almeida, L.S., Almeida, L.H., Pedrozo, M., Moroti, M.T. (2018): carinatus and C. fuscus. Prey items recorded from Chironius bicarinatus: diet. Herpetological Review 49(4): 750. Chironius flavolineatus in the states of Minas Gerais, São Amaral, A. (1918): Contribuição a biologia dos ophidios brasileiros Paulo and Goiás (Pinto et al., 2008; Passos et al., 2017; I-II. Nota prévia; Coleção trabalhos do Instituto Butantan 2: 1. Aximoff et al., 2017) need further investigation given Amaral, A. (1933): Mecanismo e gênero de alimentação de the recent description of Chironius brazili (Hamdan serpentes do Brasil. Boletim de Biologia de São Paulo 1: 2–�4. and Fernandes, 2015), which is extremely similar to C. Aximoff, I., Cintra, H., Pontes, J. (2017): Chironius flavolineatus (Boettger’s Sipo). Diet and habitat use. Herpetological Review flavolineatus in external morphology and coloration and 48(1):� 205� 06. which can occur in sympatry with C. flavolineatus in Ayarzaguena, J. (1987): Primer reporte para de those states (Hamdan and Fernandes, 2015). Adelophryne gutturosa (Leptodactylidae), datos sobre su Most species of Chironius are not strictly biología. Memorias Sociedad de Ciencias Naturales La Salle bathracophagous. However, the high proportion and 45(123): 159–160. diversity of anuran prey reported in their diet along Beebe, W. (1946): Field Notes on the snakes of Kartabo, British with the fact that many of these anuran species have Guiana and Caripito, Venezuela. ��������� 31: 11��2. toxic skin secretions (e.g., Phyllobates, Osteocephalus, Bernarde, P.S., Abe, A.S. (2010): Food habits of snakes from Espigão do Oeste, Rondônia, Brazil. Biota Neotropica 10: Trachycephalus and Itapotihyla; Toledo and Jared, 167� � 73. 1995; Daly, 1995; Costa et al., 2005), suggest a high Bovo, R.P., Sueiro, L.R. (2012): Records of predation on Itapotihyla level of diet specialization may exist among several langsdorffii (Anura: Hylidae) by Chironius bicarinatus species within the genus. It is likely that more species (Serpentes: Colubridae) with notes on foraging substrate. of squamates and mammals are consumed by Chironius Notes 5:� 291� 92. spp. than have been reported given the large number of Castanho, L.M. (1996): Phyllomedusa distincta (Leaf-). species with sympatric distributions. However, the low Predation. Herpetological Review 27(3): 141. Costa, T.O.G., Morales, R.A.V., Brito, J.P., Gordo, M., Pinto, number of natural history studies in these snakes makes A.C., Bloch Jr, C. (2005): Occurrence of bufotenin in the it difficult to accurately ascertain the true extent of prey Osteocephalus genus (Anura: Hylidae). Toxicon 46:���� 371� . diversity within the genus. The prey items in many Cunha, O.R., Nascimento, F.P. (1978): Ofídios da Amazônia X - As dietary records were identified only to higher taxonomic cobras da região leste do Pará. Publicações Avulsas do Museu levels, such as “lizards” or “rodents”, or they used Paraense Emilio Goeldi 31: 1�218. generalized taxonomic names such as “Hyla” (Dixon Cunha, O.R., Nascimento, F.P. (1982): Ofídios da Amazônia XV and Soini, 1977; Cunha and Nascimento, 1978; Dixon - As espécies de Chironius da Amazônia oriental (Pará, Amapá et al., 1993). Other dietary records do not identify the e Maranhão). (Ophidia: Colubridae). Memórias do Instituto Butantan 46: 139�172. species of Chironius, such as the record of a Chironius Cunha, O.R., Nascimento, F.P. (1993): Ofídios da Amazônia. As sp. consuming an Iguana iguana (Rivas et al., 1998). cobras da região leste do Para. Boletim do Museu Paraense Duellman (2005) hypothesized that Chironius spp. can Emilio Goeldi, Série. Zoologia 9: 1–191. shift their dietary preferences based on the availability Daly, J.W. (1995): The chemistry of poisons in skin. of food items, which may involve feeding more on Proceedings of the National Academy of Sciences of the United anurans during the rainy season and then switching to States of America 92: 9–13. lizards during the dry season. However, this hypothesis Dixon, J.R., Soini, P. (1977): The reptiles of the upper Amazon currently remains untested. More natural history data basin, Iquitos region, Peru. II. Crocodilians, turtles, and snakes. Milwaukee Public Museum. Contributions in Biology and are needed to assess the full diversity of prey items Geology 12: 1–71. consumed by snakes in the genus Chironius and to Dixon, J.R., Soini, P. (1986): The Reptiles of the Upper Amazon test whether diet preferences relate to seasonality and Basin, lquitos Region, Peru., Milwaukee, USA, Milwaukee changes in food availability. Public Museum. Dixon, J.R., Wiest, J.A., Cei, J.M. (1993): Revision of the tropical Acknowledgments. This study was financed in part by the snake Chironius Fitzinger (Serpentes, Colubridae). Monogafie Coordenação de Aperfeiçoamento de Pessoal de Nível Superior— Museo Regionale di Scienze Naturali XIII: 1–279. Brasil (CAPES)—Finance code 001 doctoral fellowship to Igor Duellman, W.E. (1978): The biology of an equatorial herpetofauna Joventino Roberto (88882.156872/2016-01). Adrian Barnett and in Amazonian Equador. Miscellaneous Publications. Museum of Coleman M. Sheehy III reviewed earlier drafts of this manuscript Natural History of the University of Kansas 65: 1–352. and assisted with the English. We thank Javier C. Suaréz and Duellman, W.E. (2005): Cusco Amazónico: The lives of amphibians Sasha J. Tetzlaff for their suggestions and comments on the and reptiles in an Amazonian rainforest. New York, USA, manuscript. Comstock Publishing Associates. 4 Igor Joventino Roberto & Aline Ramos Souza

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Accepted by Javier Cortés Suárez