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Home , Ceratophrys, Pico da Neblina

Herpetology Notes, volume 14: 435-438 (2021) (published online on 26 February 2021)

New records of the Horned toad (Rhinella ceratophrys): filling distribution gaps in lowland forests in the Brazilian Amazon

Afonso José Cruz Gonçalves Pereira1,2,*, Vinícius Tadeu de Carvalho3,4, Alexandre Pinheiro de Almeida2,4, Rommel R. Rojas4, Marcelo Gordo2, Luciana Frazão5, Robson W. Avila6, and Marcelo Menin2

The harbours the highest diversity of night times (Rodríguez and Duellman, 1994; Fenolio et anuran in the world (Duellman, 1999; Vacher al., 2012; Rojas-Runjaic et al., 2017). et al., 2020), but the geographic distribution boundaries Currently, its known geographic distribution of several species remains uncertain, mainly due to the encompasses northeast Peru, east Ecuador, southeast absence and difficulties of inventories in remote areas. and south and north Thus, this lack of information hinders the elaboration of (Rojas-Runjaic et al., 2017; Frost, 2020). In Brazil, good conservation plans (Verdade et al., 2012). Rojas-Runjaic et al. (2017) reported the occurrence The toad genus Rhinella Fitzinger, of R. ceratophrys between 400 – 1,800 m a.s.l., in the 1826 is one of the most diverse in Bufonidae Gray, Amazon uplands, specifically at the Pico da Neblina 1825, comprising 92 species (Frost, 2020). A distinctive National Park, municipality of São Gabriel da Cachoeira, species in this genus is Rhinella ceratophrys (Boulenger, northern Amazonas State. Apart from these records, no 1882), easily distinguishable from all other species of bufonids in South America by the presence of ‘horns’, i.e., dermal triangular flaps over the eyelids (Fenolio et al., 2012). This species inhabits primary forests, and occurs in both lowland and upland Amazonian forests (Fenolio et al., 2012; Rojas-Runjaic et al., 2017). Individuals of R. ceratophrys live on the ground amidst leaf litter in humid forests, being apparently restricted to non-flooded forest, and also active in both day and

1 Secretaria de Estado de Educação e Qualidade de Ensino do Amazonas, Escola Estadual Frei André da Costa, 69550-903, Tefé, Amazonas, Brazil. 2 Universidade Federal do Amazonas, Instituto de Ciências Biológicas, Av. General Rodrigo Otávio Jordão Ramos, 6200, 69080-900, Manaus, Amazonas, Brazil. 3 Universidade Regional do Cariri, Rua Cel. Antônio Luiz, 1161, 63105-000, Crato, Ceará, Brazil. 4 Laboratório de Evolução e Genética , Departamento de Genética, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Av. Rodrigo Octávio Jordão Ramos, 6200, Mini–Campus, Coroado I, 69080-900, Manaus, Amazonas, Brazil. 5 BIONORTE, Av. Carvalho Leal, 177, Prédio Anexo 4° andar, 69065-001, Manaus, AM, Brazil. 6 Núcleo Regional de Ofiologia, Departamento de Biologia, Centro de Ciências, Universidade Federal do Ceará, 60440- Figure 1. Adult female (CTGA-N 2187) (A) and juvenile 900, Fortaleza, Ceará, Brazil. (CTGA-N 1864) (B) of Rhinella ceratophrys, both recorded * Corresponding author. E-mail: [email protected] in the left bank of the Japurá River, Amazonas State, Brazil. © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. Photos by Vinicius T. de Carvalho. 436 Afonso José Cruz Gonçalves Pereira et al. additional information has been published and therefore 81.7 mm; CTGA-N 1858, adult male, SVL = 46.1 mm; many aspects of its geographical distribution remain CTGA-N 1864, juvenile; CTGA-N 2345, adult female, unknown. SVL = 66.6 mm), both in the Universidade Federal do Herein we registered six individuals of Rhinella Amazonas, municipality of Manaus, Amazonas State, ceratophrys in opposite banks of the Japurá River Brazil. (1.7186° S, 69.1283° W, 97 m a.s.l, left bank; 1.8461° The identification of Rhinella ceratophrys (Fig. 1) was S, 69.0295° W, 103 m a.s.l., right bank), municipality based on diagnosis provided by Fenolio et al. (2012), of Japurá, Amazonas State, Brazil. All individuals were which included, in addition to the triangular dermal found in the leaf-litter, in a non-flooded forest (“terra- flaps projecting over the eyelids, dermal flap projections firme”), during field campaigns between 22 August and at the corners of the mouth, distinct canthus rostralis, 20 September 2014. Two individuals were found near a loreal region concave, and larger size of adults when stream, but calls were not heard. compared to Rhaebo nasicus (Werner, 1903), a species All individuals were collected, fixed and deposited in with which Rhinella ceratophrys has historically been the Herpetological Collection of the National Institute confused. We updated the species distribution map for Amazonian Research (INPA-H 38226, juvenile, using datasets from the literature (Fig. 2) and records snout-vent length [SVL] = 19.01 mm), in the Zoological of R. ceratophrys available in the Global Biodiversity Collection Prof. Paulo Bührnheim - Amphibia section of Information Facility platform (GBIF: http://www.gbif. the Federal University of Amazonas (CZPB-AA 1422, org). Some coordinates from the literature were inferred juvenile, SVL = 21.34 mm), and in the Animal Genetics using geoprocessing software QGIS v. 3.10.1 (QGIS Tissue Collection (CTGA-N 2187, adult female, SVL = Development Team, 2020).

Figure 2. Map of the geographic distribution of Rhinella ceratophrys in northern South America. Different countries are represented by acronyms: BRA: Brazil; PER: Peru; ECU: Ecuador; COL: Colombia; VEN: Venezuela. Red stars indicate the new records reported in this study. White triangles indicate previous records in Brazil (Rojas-Runjaic et al., 2017). Yellow dots indicate other literature records (Rivero, 1961; Cochran and Goin, 1970; Coloma, 1991; La Marca, 1992; Ruiz-Carranza et al., 1996; Vélez-Rodrigues, 1999; Lynch, 2005; Cisneros-Heredia, 2006; Catenazzi and Bustamante, 2007; Yánez-Muñoz and Chimbo, 2007; Yánez-Muñoz and Venegas, 2008; Fenolio et al., 2012; Márquez et al., 2017; Rojas-Runjaic et al., 2017; Suárez-Mayorga and Lynch, 2017; Ortiz et al., 2018; Acosta-Galvis, 2019; Barrio-Amorós et al., 2019; Medina-Rangel et al., 2019; Osorno-Muñoz et al., 2019; Ramírez-Jaramillo, 2019; Señaris and Rojas-Rujaic, 2019). New records of the Horned toad (Rhinella ceratophrys) in the Brazilian Amazon 437

We provide the second record of Rhinella ceratophrys annotated species list, distribution, and conservation. in Brazil, and the first record of this species for lowland & Conservation 13: 1–198. forests in the Brazilian Amazon (below 400 m a.s.l.). Boulenger, G.A. (1882): Catalogue of the Batrachia Salientia s. Ecaudata in the Collection of the British Museum. London, Our new locality records partially fill a gap between Taylor and Francis. previously documented localities in southeastern Catenazzi, A., Bustamante, M. (2007): and . Colombia (ca. 70 km west) and those in northern Brazil In: Perú: Nanay, Mazán, Arabela, p. 130–134. Vriesendorp, (ca. 445 km northeast) (Fig. 2). Although this species C., Álvarez, J.A., Barbagelata, N., Alverson, W.S., Moskovits, was known from the lowlands of the north-western D.K., Eds., Chicago, Rapid Biological Inventories Report 18, The Field Museum. Amazon in Colombia and Peru, near the border with Cisneros-Heredia, D.F. (2006): La Herpetofauna de la Estación Brazil, and expected in the Brazilian Amazon lowlands de Biodiversidad Tiputini, Ecuador. Unpublished PhD thesis, (Fenolio et al., 2012; Rojas-Runjaic et al., 2017), no Universidad San Francisco de Quito, Quito, Ecuador. records had been provided for the latter. Cochran, D.M., Goin, C.J. (1970): of Colombia. Bulletin of Given that Rhinella ceratophrys may represent a the United States National Museum 288: 1–655. complex of morphologically cryptic species (Fenolio Coloma, L.A. (1991): Anfibios del Ecuador: lista de especies, ubicación altitudinal y referencias bibliográficas. Ecociencia 2: et al., 2012), new studies on its systematics including 1–46. molecular data will be essential to assess genetic Duellman, W.E. (1999): Distribution patterns of amphibians in divergences among populations throughout its range South America. In: Patterns of Distribution of Amphibians, A (Rojas-Runjaic et al., 2017). Particular emphasis is Global Perspective, p. 255–328. Duellman, W.E., Ed., Maryland required in the characterisation of its advertisement and Baltimore, Johns Hopkins University Press. Fenolio, D.B., Mendelson III, J.R., Lamar, W.W. (2012): New call and tadpole morphology, since they are relevant diagnosis and description of variation among adult Rhinella for the of R. ceratophrys but still unknown ceratophrys (Boulenger) (Amphibia: Bufonidae), with notes (Rodríguez and Duellman,1994; Fenolio et al., 2012). on ecology and distribution. South American Journal of Moreover, little is known about the ecology of this Herpetology 7: 9–15. species. Therefore, we encourage studies on the Fitzinger, L.J.F.L. (1826): Neue Classification der Reptilien nach distribution and ecology of this toad to better assess its ihren Natürlichen Verwandtschaften nebst einer Verwandtschafts- Tafel und einem Verzeichnisse der Reptilien-Sammlung des K. conservation status. K. Zoologisch Museum’s zu Wien. 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Accepted by Renato Nali