Herpetology Notes, volume 12: 705-708 (2019) (published online on 03 July 2019)

New records of interspecific amplexus in Neotropical anurans

Fernanda Cristina Ferreira Lirio1, Thiago Gechel Kloss2, Thiago Silva-Soares3,4, João Felipe Riva Tonini4,5, Alexander Tamanini Mônico1,3, and Rodrigo Barbosa Ferreira1,*

Successful intraspecific communication in anurans is specific (interspecific) amplexus and ultimately dependent on species-specific aspects of morphology, decrease mating success (Marco and Lizana, 2002; chemical signals, vocalization and sexual dimorphism Wells, 2007), because interspecific amplexus causes (Bowcock et al., 2008). Furthermore, some anurans use loss of energy and may result in unviable hybridization specialized behaviour to signal unwanted amplexus, (Haddad, 1994). Reports of interspecific amplexus have such as release calls and body vibrations or inflations been documented in various Neotropical species (Bowcock et al., 2008; Mollov et al., 2010; Izzo et al., especially for the and Bufonidae families 2012). These communication cues might not always be (Hettyey and Pearman, 2003; Wells, 2007). Herein, we effective, leading some anuran males to attempt to mate report four cases of interspecific amplexus, aiming to with females or males of other species, and even with increase the natural history knowledge of these events inanimate objects (e.g., Mollov et al., 2010; Moldowan in anurans of the Atlantic Forest. et al., 2013). The urge of explosive breeders (i.e., Our observation on interspecific amplexus date from limited days of reproductive season) to find mates is 2010 to 2017, all from the municipality of Santa Teresa often quoted as resulting in more frequent interspecific (19.9333ºS, 40.6008ºW), Espírito Santo state, Brazil. amplexus (Theis and Caldart, 2015; Gül et al., 2018; The matings in interspecific amplexus were visually Guerra, et al., 2018). monitored during 15 minutes and photographed. The In Neotropical frog assemblages, many species overlap individuals were captured for identification, but were in breeding season resulting in large aggregation of not collected. The sex of the individuals were not males at breeding (Ferreira et al., 2012). Such determined. Taxonomic classification followed Frost scenarios may increase the chance of non-species- (2017). We observed four interspecific amplexus events involving seven species of anurans: Ololygon argyreornata (Miranda-Ribeiro, 1926), Ololygon kautskyi Carvalho-e-Silva and Peixoto, 1991, Boana 1 Programa de Pós-Graduação em Ecologia de Ecossistemas, semilineata (Spix, 1824), langsdorffii Universidade Vila Velha, Avenida Comissão José Dantas de (Duméril and Bibron, 1841), Trachycephalus Melo 21, Boa Vista II, Vila Velha, Espírito Santo, 29102-920, mesophaeus (Hensel, 1867) (Hylidae), Brazil. binotatus (Spix, 1824) () and 2 Departamento de Ciências Biológicas, Universidade do Estado crombiei Heyer and Wolf, 1989 de Minas Gerais, Avenida Olegário Maciel 1427, Industrial, (). All recorded interspecific pairs Ubá, Minas Gerais, 36502-000, Brazil. 3 Programa de Capacitação Institucional, Instituto Nacional included Hylidae species (71% species). The species da Mata Atlântica, Avenida José Ruschi 04, Santa Teresa, displayed axillary amplexus, with an individual Espírito Santo, 29650-000, Brazil. positioned on the back of the other individual and 4 Departamento de Biologia, Universidade Federal do Espírito grasping it under the armpits. No oviposition was Santo, Av. Fernando Ferrari 514, Goiabeiras, Vitória, Espírito observed during these amplexus. Santo, 29075-910, Brazil. On 3 July 2010 at around 20:00h, we observed 5 Department of Organismic and Evolutionary Biology, Museum Harvard University of Comparative Zoology 26 Oxford St, an Ololygon kautskyi and a Boana semilineata in Cambridge, MA 02138, USA. amplexus on marginal vegetation of a pond near an * Corresponding author. E-mail: [email protected] urban fragment (������������������������������������ 706 Fernanda Cristina Ferreira Lirio et al.

Figure 1. Interspecific amplexus: (A) Ololygon kautskyi and Boana semilineata, (B) Itapotihyla lansgdorffii and Trachycephalus mesophaeus, (C) Ololygon kautskyi and , (D) and Ololygon argyreornata recorded in the municipality of Santa Teresa, Espírito Santo, Brazil. Photo by: A) Fernanda C. F. Lirio, B) Thiago G. Kloss, C) Thiago Silva- Soares, and D) Rodrigo B. Ferreira.

(Figure 1A). Both species have prolonged breeding species belong to different families. Ololygon kautskyi (Hartmann et al., 2010; Ferreira et al., 2012). Both breeds in the dry season at small streams in the forest species have been reported using marginal vegetation and has larval development (Carvalho-e-Silva and of ponds for intraspecific reproduction (Ferreira et al., Peixoto, 1991). Haddadus binotatus breeds in the rainy 2012; Haddad et al., 2013); however, previous reported season and has direct development, laying eggs on the interspecific amplexus events involved only a female of leaf litter (Costa and Carvalho-e-Silva, 2010). Boana semilineata being amplected by a male Boana On 30 October 2015 at around 20:00h, we observed a albomarginata (Spix, 1824)(Prado and Pombal, 2005). Physalaemus crombiei and an Ololygon argyreornata in On 12 October 2013 at around 21:00h, we observed amplexus in a marsh at the Augusto Ruschi Biological an Itapotihyla langsdorffii and a Trachycephalus Reserve (19.9069°S, 40.5534°W). These species also mesophaeus in amplexus on vegetation near a belong to different families. Both species use temporary floodplain (19.9729°S, 40.5286°W) at the Santa Lúcia pools for breeding (Carvalho-e-Silva and Carvalho Biological Station (Figure 1B). This amplexus occurred e Silva, 1998; Prado and Pombal, 2005) (Figure 1D). during a period of explosive reproduction of the two Ololygon argyreornata is an explosive breeder whereas species. This reproductive strategy has been reported P. crombiei is a prolonged breeder (Pupin et al., 2010; for both species (Wells, 1977; Prado et al., 2003). These Wells, 1977). species usually use the same for reproduction, In an anuran assemblage, different species may use being observed in permanent and temporary ponds the same resources for reproduction (e.g., breeding (Borges-Martins et al., 2007; Narvaes et al., 2009). sites and season). Most species in our observations On 06 October 2017 at around 22:00h, we observed share the same reproductive habitat in the rainy season. an Ololygon kautskyi and a Haddadus binotatus in Thus, species in these assemblages are more likely amplexus in a marsh at São Lourenço Municipal to be involved in interspecific amplexus. Contrarily, Reserve (19.9257°S, 40.6177°W; Figure 1C). These Ololygon kautskyi and Haddadus binotatus pair, usually New records of interspecific amplexus in Neotropical anurans 707 reproduce in different seasons and habitats (Dias et Gül, S., Özdemir, N., Dursun, C. (2018): First record of interspecific al., 2012). It is likely H. binotatus was foraging near amplexus behaviour between Bufotes variabilis (Pallas, 1769) humid habitat (i.e., stream) and was amplected by and Pelophylax ridibundus (Pallas, 1771) with Bufo bufo O. kautskyi on its way toward the breeding habitat. (Linnaeus, 1758) (Anura: Bufonidae) from Turkey. ������������ Notes 11: 153–155. Although we have not observed oviposition, several Haddad, C.F.B., Cardoso, A.J., Castanho, L.M. (1990): Hibridação studies on anurans have shown successful oviposition natural entre Bufo ictericus e Bufo crucifer (Amphibia, Anura). of interspecific pairs (Haddad et al., 1990; Sullivan and Revista Brasileira de Biologia 50: 739–744. Lamb, 1988; Haddad et al., 1994). We suggest future Haddad, C.F.B., Pombal-Júnior, J.P., Batistic, R.F. (1994): Natural studies to capture and maintain interspecific pairs in a hybridization between diploid and tetraploid species of leaf laboratory setting to investigate possible oviposition , genus Phyllomedusa (Amphibia). ���������������������� and viability of offspring. 28: 425–430. Haddad, C.F.B.; Toledo, L.F.; Prado, C.P.A.; Loebmann, D.; Gasparini, J.L.; Sazima, I. (2013): Guia de anfíbios da Acknowledgments. We thank the Bromeligenous Project Mata Atlântica: diversidade de biologia. �������������� for the fieldwork logistical support. ���� ������������������� Anolisbooks. Coordenação de Aperfeiçoamento de Pessoal de Nível Superior Hettyey, A., Pearman, P.B. (2003): Social environment and - Brasil (CAPES; - FCLF: 001-1774502; RBF: 0823-2015), reproductive interference affect reproductive success in the frog Conselho Nacional de Desenvolvimento Científico e Tecnológico Rana latastei. Behavioral Ecology 14: 294–300. 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Accepted by Christoph Liedtke