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Home , Alsodidae, Aplastodiscus perviridis, Crossodactylus schmidti, Dendropsophus anceps, Dendropsophus sanborni, Elachistocleis bicolor

Herpetology Notes, volume 11: 543-551 (2018) (published online on 25 July 2018)

Anurans of anthropogenic areas and remnants of Semideciduous in western State of Paraná,

Peterson Trevisan Leivas1,*, Pedro de Oliveira Calixto1, Cristiane Hiert2 and Michel Varajão Garey3

Abstract. Here we present the first species list of anurans from western parts of the State of Paraná, Brazil, including many areas that had never been sampled before, as a contribution to the knowledge of the distribution of . The regional species list was compiled based on new field records, museum collections and literature records in the counties of Cascavel, Céu Azul, Foz do Iguaçu, Matelância, Santa Tereza do Oeste, Santa Terezinha do Itaipu and São Miguel do Iguaçu. A total of 36 species were recorded in our study. Twenty-two species were recorded exclusively in the field, two only in museum collections and one species is only recorded in the literature. and are the most well represented families out of the 10 recorded from museum and literature records with 20 and six species, respectively. Two species were globally classified as Near Threatened ( schmidti and bigibbosa) and one species was regionally classified as Critically Endagered (Vitreona uranoscopa). Lithobates catesbeianus an exotic invasive species was recorded in four counties. Most of the recorded species occurred only in open area. The species richness observed in each county was lower than those found in other areas of semideciduous forest in the State of Paraná.

Key words: Amphibia, anura, inventory, Atlantic Forest

Introduction of the Atlantic Forest is one of the richest in the world, with 88% of the species being endemic to this biome Surveys of anuran communities provide basic (Haddad et al., 2013). Moreover, the Atlantic Forest information relevant for the and distribution is a biome that suffers mostly from loss and of species, and play a fundamental role in the fragmentation, remaining only about 11-16% of its development of species conservation and management original coverage, which is now highly fragmented in plans (Silvano and Segalla, 2005; Toledo, 2009). These the landscape (Ribeiro et al., 2009). The deforestation surveys are especially important in regions with high problem is even more evident in some specific forest biodiversity and endemism, and those that present some types, such as the semideciduous forest (SEF), target level of threat to their remnants, such as the Atlantic of the most drastic vegetation reduction due to rapid Forest biome (Eterovick et al., 2005). The anurofauna expansion of agricultural areas. It is estimated that only about 7% of the original area remains (Ribeiro et al., 2009). Most of Paraná’s territory is covered by SEF, which houses a lower richness of anurans species than the 1 Programa de Pós-Graduação em Zoologia, Universidade Federal do Paraná - UFPR, Caixa Postal 19031, CEP 81531- dense ombrophilous , and higher than the mixed 980, Curitiba, Paraná, Brasil. ombrophilous forest (e.g., Araucária Forest) (Rossa- 2 Universidade Estadual do Centro-Oeste - UNICENTRO, Feres et al., 2017). In comparison with ombrophilous Caixa Postal 3010, CEP 85040-080, Guarapuava, Paraná, forests, SEF presents lower altitudinal and latitudinal Brasil. gradients, and lower degree of environmental 3 Laboratório de Ecologia de Metacomunidades, Instituto heterogeneity, especially of humid , which Latino-Americano de Ciências da Vida e da Natureza, possibly explains the reduced number of species that Universidade Federal da Integração Latino-Americana - UNILA, Av. Tarquínio Joslin dos Santos, 1000, CEP 85870- occur in this type of forest (Haddad and Prado, 2005; 901, Foz do Iguaçu, Paraná, Brasil. Brassaloti et al., 2010; Rossa-Feres et al., 2017). * Corresponding author. E-mail: [email protected] Specifically in the State of Paraná, anuran inventories 544 Peterson Trevisan Leivas et al.

do Iguaçu, Matelândia, Santa Tereza do Oeste, Santa Terezinha do Itaipu, and São Miguel do Iguaçu in southern Brazil. With this work we hope to reduce the Wallacean shortfall (e.g., geographic distribution data) about (Hortal et al., 2015).

Material and Methods Study area.—We sampled an area of the geological formation at Serra Geral in the Paraná basin, which holds the third plateau in western Paraná. According to the Köppen-Geiger classification, the climate of the area is Cfa, which means subtropical humid mesothermal with hot summers, infrequent frosts and trend of Figure 1. Map of the study area showing the counties sampled concentration of rainfalls during the summer months (light gray), State of Paraná in dark gray. Numbers indicate the county name as following: Cascavel (1), Céu Azul (2), Foz do with no defined rainy season (Maack, 2012). Iguaçu (3), Matelândia (4), Santa Tereza do Oeste (5), Santa The region is inserted in the Atlantic Forest biome, Terezinha do Itaipu (6) and São Miguel do Iguaçu (7). The covered by SEF, mainly at an intermediate stage of abreviations of countries as following: (AR); Brazil forest succession (Ribeiro et al., 2009). In the limit (BR); (BO); (PY); and Uruguay (UY). between western and central Paraná there are portions of forest, forming a region of ecotone between these two floristic formations. The regional landscape is a mosaic of forest fragments, including the greatest in SEF are even scarcer; only the counties of Londrina, forest remnant of SEF (e.g., Iguaçu National Park), Ortigueira, Telêmaco Borba and Três Barras do Paraná including cultivation, livestock, and urban areas. have anuran species lists (Bernarde and Anjos, 1999; Machado et al., 1999; Bernarde and Machado, 2000; Data collection.—The regional species list was Machado and Bernarde, 2002; Nazaretti and Conte, compiled based on field records, data from specimens 2015; Santos and Conte, 2016). deposited in museums and literature records for seven Recognising the gap in knowledge regarding the anuran counties in western Paraná, southern Brazil, named: community across much of Paraná, we aimed to describe Cascavel, Céu Azul, Foz do Iguaçu, Matelândia, Santa the composition of anuran species in anthropogenic Tereza do Oeste, Santa Terezinha do Itaipu and São areas and remnants of SEF in parts of western Paraná, Miguel do Iguaçu (Figure 1, Table 1). For the field data, specifically in the counties of Cascavel, Céu Azul, Foz we sampled forest remnants and open areas (farmlands 1

 Table 1. Sampled areas in counties of western State of Paraná, Brazil, detailing geographic coordinates (Céu Azul, Foz do Iguaçu 1 Table 1. Sampled areas in counties of western State of Paraná, Brazil, detailing geographic and Santa 2Tereza coordinates do Oeste (Céu are Azul,the central Foz do coordinatesIguaçu and Santa of county), Tereza dotype Oeste of arearea, the type central of coordinatessampled environments of county), and number of sampled areas3 (NSE).type of Oarea, = open type area;of sampled F = forest; environments Df = dam and in number forest; ofDo sampled = dam inareas open (NSE). area; O Swf = open = area; F in = forest; Swo = swamp in open area;4 Pfforest; = Df in = forest;dam in Poforest; = pond Do = in dam open in openarea; area; St = Swfstream = swamp in forest. in forest; Swo = swamp in open area; Pf 5 = pond in forest; Po = pond in open area; St = stream in forest. 6 County Geographic coordinates Area Environment NSE Cascavel -25.02 S/-53.55 W F Df, Swf, St, F 7 Céu Azul -25.15 S/-53.84 W F, O Swo, St, Pf, F 9 Foz do Iguaçu -25.51 S/-54.58 W F, O Swf, Swo, Pf, Po, St 16 Matelândia -25.20 S/-54.02 W F, O Df, Do, Swo, St 9 Santa Tereza do Oeste -25.05 S/-53.61 W F, O Sw, St, Pf, Po 8 Santa Terezinha de Itaipú -25.39 S/-54.34 W F, O Do, Swo, F, St 11 São Miguel do Iguaçu -25.37 S/-54.31 W F Df, Swf, St 8 7 Anurans of anthropogenic areas and remnants of Semideciduous Forest in Brazil 545 and urban areas) in these counties. We selected the Literature and museum data were also compiled. sampling sites based on the structural features of water The bibliographic data includes published articles and bodies in order to sample the largest possible variety the list of species collected in the management plan of environments (Table 1). Two people (PTL, CH and of Iguacu National Park. The search for articles was MVG) performed the sampling in all counties, both done on Google Scholar using the keywords “county during the day (9:00 – 17:00) and twilight and night name” AND “Amphibia”. For the compilation of (17:30 - 22:30h). museum data, herpetological collections were searched In Céu Azul, Foz do Iguaçu and Santa Tereza do through the online database speciesLink, and records Oeste only aquatic breeding sites were sampled (13 from the folowing collections were included: Museu lotic and 20 lentic water bodies), applying a visual and de Ciências e Tecnologia of Pontifícia Universidade acoustic active search (Crump and Scott, 1994) and Católica do Rio Grande do Sul (MCP-PUCRS), Centro sampling tadpoles using a hand dipnet (mesh 3mm2). de Coleções Taxonômicas of Universidade Federal Sampling was carried out between September 2014 de Minas Gerais (UFMG-ICB), Coleção “Célio F. B. and March 2018, which is the breeding season for the Haddad” of Universidade Estadual Paulista campus great majority of species in western Paraná. Each water Rio Claro (CFBH), Coleção de Anfíbios adultos of body was sampled three times during this period. The Universidade Estadual Paulista campus São José do first sampling was carried out between September and Rio Preto (DZSJRP) and Coleção de Anfíbios of Museu October, the second between November and December de Zoologia of Universidade Estadual de Campinas and the third between January and March. Each (ZUEC). In addition, the authors personally visited breeding sites were sampled during one hour applying the collection of Museu de História Natural Capão da both sampling methods, totalling an effort of three hours Imbuia (MHNCI). per breeding site. Species nomenclature was updated following Frost In Cascavel, Matelândia, Santa Terezinha de Itaipú and (2017). Anuran threat status was determined according São Miguel do Iguaçu anurans were sampled applying to international, national and regional criteria. Population visual and acoustic active search methods (Crump and trends and international threat status for each species Scott, 1994) using four predetermined transects that were based on data available on the IUCN “Red List crossed aquatic breeding sites (Crump and Scott, 1994). of Threatened Species version 2017.3” (IUCN, 2017). Transects with breeding sites were sampled during two The national database follows Ordinance nº 444 of 17 hours during the day and two hours during the night, December 2014 (Brasil, 2014) and regionally follows totalling an effort of four hours/day. In these counties Livro Vermelho da Fauna Ameaçada no Estado do we collected data in August (winter) and November Paraná (Mikich and Bérnils, 2004). (spring) 2010 and in February (summer), and May (autumn) 2011. Each area was sampled for two days in Results each season, totalising eight days of sampling per area. A total of 36 species were recorded in western Paraná, Morphological diagnoses and analysis of the southern Brazil (Table 2). Twenty-two species were advertisement calls were performed to confirm the recorded exclusively in the field, two only in museum taxonomic identity of the species recorded (e.g. collections and one species was recorded only in the according Haga et al. 2014). literature (Table 2). Only the MHNCI presented records Vocalizations were recorded with an external directional of anurans from the study region, and all specimens microphone (Yoga HT 81), coupled to an H2n digital collected are from Foz do Iguaçu (Appendix 1). In audio recorder positioned at a maximum distance of 1 field, 33 anuran species representing ten families were m to the calling males. Calls were analysed using Raven recorded (Table 2). Hylidae was the richest family with 1.2 software (16 bits of resolution, 44 kHz of frequency 20 species (55.5%), followed by Leptodactylidae with sampling, FFT and frame length of 256 samples). All six species (16.7%), Bufonidae and specimens collected were anesthetized and killed, fixed with two species (5.6% each one), and six families in 10% formalin and stored in 70% ethanol (adults) (, Centrolenidae, , , or 10% formalin (tadpoles). All adult specimens Phyllomedusidae, and Ranidae) with only one and tadpoles are housed in Coleção de Anfíbios at species (each one represents 2.8%). The ranid species Universidade Federal da Integração Latino-Americana Lithobates catesbeianus is an exotic and invasive (CA-UNILA) (Appendix 1). species. Regarding the environmental occurrence, 17 546 Peterson Trevisan Leivas et al.

Table 2. Anuran species recorded in the seven counties of western State of Paraná, southern Brazil: Cascavel (CS), Céu Azul (CA), Foz do Iguaçu (FI), Matelândia (MA), Santa Tereza do Oeste (SO), Santa Terezinha do Itaipu (SI), and São Miguel do Iguaçu (SM). Source of the species record in each county: field survey (1), museum collections (2), and literature (3). Population status accordingTable to 2.the Anuran IUCN species (2017): recorded Stb in (stable), the seven countiesUnk (Unknown), of western State Dec of Paraná, (Decreasing) southern Brazil: and IncCascavel (Increasing). (CS), Céu Azul Environmental (CA), Foz do Iguaçu occurrence (FI), Matelândia (Env):(MA), SantaF (forest), Tereza doO Oeste(open (SO), area), Santa and Terezinha B (both). do Itaipu (SI), and São Miguel do Iguaçu (SM). Source of the species record in each county: field survey (1), museum collections (2), and literature (3). Population status according to the IUCN (2017): Stb (stable), Unk (Unknown), Dec (Decreasing) and Inc (Increasing). Environmental occurrence (Env): F (forest), O (open area), and B (both).

County IUCN Env FAMILY/Taxon CS CA FI MA SO SI SM ALSODIDAE (Duméril and Bibron, 1841) 3 Stb F BUFONIDAE Rhinella ornata (Spix, 1824) 1 2,3 Unk F R. schneideri (Werner, 1894) 1 1,2 1 1 1 1 Inc B CENTROLENIDAE Vitreorana uranoscopa (Müller, 1924) 1 Dec F HYLIDAE Aplastodiscus perviridis Lutz, 1950 1 1 2,3 Stb F Boana albopunctata (Spix, 1824) 1 1 1 1 1 1 1 Stb B B. bischoffi (Boulenger, 1887) 1 1 1 1 Stb O B. caingua (Carrizo, 1991) 1 2,3 1 Stb O B. faber (Wied-Neuwied, 1821) 1 1 1 1 Stb B B. prasina (Burmeister, 1856) 1 1 1 1 Stb O B. punctata (Schneider, 1799) 1 Stb O B. raniceps (Cope, 1862) 1 1 1 1 Stb O B. semiguttata (A. Lutz, 1925) 3 Stb O minutus (Peters, 1872) 1 1 1 1 1 1 1 Stb B D. nanus (Boulenger, 1889) 1 1 1,2,3 1 1 1 1 Stb O D. sanborni (Schmidt, 1944) 1 1 Stb O Itapotihyla langsdorffii (Duméril and Bibron, 1841) 1 Dec F Lysapsus limellum Cope, 1862 1 Stb B Ololygon berthae (Barrio, 1962) 2,3 Stb B fuscovarius (Lutz, 1925) 1 1 1,2,3 1 1 1 1 Stb B S. granulatus (Peters, 1871) 1 Stb O S. perereca Pombal, Haddad, and Kasahara, 1995 1 1 1 Unk B S. squalirostris (Lutz, 1925) 1 1 Stb O Trachycephalus dibernadoi Kwet and Soulé 2008 1 Stb F HYLODIDAE Crossodactylus schmidti Gallardo, 1961 1 1 Dec F LEPTODACTYLIDAE fuscus (Schneider, 1799) 1 1 1 1 1 1 Stb O L. latrans (Steffen, 1815) 1 3 1 1 1 Stb B L. mystacinus (Burmeister, 1861) 2,3 1 1 Stb O L. podicipinus (Cope, 1862) 2 1 Stb O aff. gracilis (Boulenger, 1883) 1 Stb O Physalaemus cuvieri Fitzinger, 1826 1 1,2,3 1 1 1 Stb O MICROHYLIDAE bicolor (Guérin-Méneville, 1838) 1 1 1 Stb O ODONTOPHRYNIDAE Proceratophrys avelinoi Mercadal de Barrio and Barrio, 1993 1 Unk F P. bigibbosa (Peters, 1872) 1,2 Dec F PHYLLOMEDUSIDAE Phyllomedusa tetraploidea Pombal and Haddad, 1992 1 Stb B RANIDAE Lithobates catesbeianus (Shaw, 1802) 1 1 1 1 Inc O Total species richness = 36 19 10 22 18 8 11 20 Anurans of anthropogenic areas and remnants of Semideciduous Forest in Brazil 547

Figure 2. Some of the anuran species recorded for western Paraná, Brazil. (a) Rhinella schneideri, (b) Aplastodiscus perviridis, (c) Boana caingua, (d) B. faber, (e) B. prasina, (f) B. punctata, (g) B. raniceps, (h) Dendropsophus sanborni, (i) Phyllomedusa tetraploidea, (j) Scinax granulatus, (l) S. squalirostris, (k) Leptodactylus fuscus, (m) L. podicipinus, (n) Physalaemus cuvieri, (o) P. aff. gracilis, and (p) Proceratophrys avelinoi. 548 Peterson Trevisan Leivas et al.

Figure 2. Continued. Anurans of anthropogenic areas and remnants of Semideciduous Forest in Brazil 549 occur in open areas, nine occur only in forest, and 10 species in western Paraná. Crossodactylus schmidti species occur in both environments (Table 2). occurs in streams inside forests and L. macroglossa According to the IUCN, the majority of species occurs in open and forested areas on rocky soil along found are classified as Least Concern (LC), and only rivers both in mesophytic semideciduous and Araucaria Crossodactylus schmidti and Proceratophrys bigibbosa forests (Conte et al., 2009; Santos et al., 2009; Caldart are classified as Near Threatened (NT). No species from et al., 2010; Haddad et al., 2013). Proceratophrys western Paraná is listed as endangered in the Brazilian bigibbosa occurs in mountainous regions and Araucaria National Red List. In Paraná State Red List, Vitreorana forest plateau, and breeds in small streams (Kwet and uranoscopa is categorized as Data Deficient (DD) and Faivovich, 2001). The major threats to these species are Limnomedusa macroglossa as Critically Endangered deforestation, forest fragmentation and soil and water (CE). Regarding the population status of the species, pollution, and the presence of the exotic Lithobates most species were considered stable (72% of species), catesbeianus (Silvano et al., 2004a; 2004b). Moreover, four species have declining populations (11%), three four species recorded only in the Iguaçu National Park species have unknown population status (8%), two are in population decline: C. schmidti, Itapotihyla species (6%), L. catesbeianus and Rhinella schneideri langsdorffii, P. bigibbosa, and Vitreorana uranoscopa. with increasing population size. Physalaemus aff. Searches for other populations of these species in gracilis has an uncertain taxonomy and therefore is not forest fragments located in western Paraná should be included in the IUCN list (Table 2; IUCN 2017). considered a priority. These findings provide evidence of the effects of fragmentation on these species. In addition, Discussion the acquisition of information about natural history is essential to develop conservation strategies, especially The anurofauna of western Paraná accounts for for data deficient species (e.g., V. uranoscopa) or under 23% of the species of this state (Toledo & some degree of threat (e.g., C. schmidti, P. bigibbosa, Batista, 2012) and 6% of the known species that occur and L. macroglossa) (Mikich and Bérnils, 2004; IUCN, in the Atlantic Forest (Haddad et al., 2013). The species 2017). richness observed in each county was lower than that Western Paraná, excluding Iguaçu National Park, found in other areas of semideciduous forest in Paraná is one of the most deforested and fragmented regions state, such as Telêmaco Borba and Ortigueira counties of the state (Ribeiro et al., 2009) where there are only (27 species; Machado and Bernarde, 2002), Parque small forest fragments and few studies on biodiversity. Estadual Mata dos Godoy in Londrina county (24 This study represents an important contribution to species; Bernarde & Anjos, 1999, Machado et al., 1999), understanding the distribution of biodiversity in and Parque Estadual do Rio Guarany in Três Barras this region. Species lists are essential to reduce the county (23 species; Bernarde and Machado, 2000). It Wallacean shortfall, and this is the starting point for the is quite possible that the sampling effort of the present development of conservation strategies. study was not enough to record all the species from these seven counties located in western Paraná. However, this Acknowledgements. We thank the Instituto Chico Mendes is the first anuran species list of this region, so with the de Conservação da Biodiversidade (ICMBio) for providing increase of sampling effort, especially in the Iguaçu collection permits (SISBIO/40772 and 42012). MVG thanks National Park and other counties of Paraná River bank, the Conselho Nacional de Desenvolvimento Científico e more species should be added to the list. Tecnológico (CNPq, Proc. 422537/2016-0) and UNILA (edital The conservation status of most species is Least PRPPG 109/2017) for financial support. POC thanks Conselho Concern (IUCN, 2017), which is probably related Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a research fellowship (132606/2016-0). PTL thank Fundação to the wide geographic distribution of these species Araucária, Fundação Grupo Boticário de Proteção a Natureza and (e.g., Aplastodiscus perviridis, Dendropsophus nanus, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior Leptodactylus latrans) (Haddad et al., 2013; Frost, (CAPES) for financial support. We thanks Jéssica de L. Jeziorny, 2017), and/or more generalist in relation to habitat use, Fátima R. B. Fernández, Fatima B. Penayo, Tarik A. Kardush, for example, some species are commonly found in urban Lara J. G. de Sousa, Jean P. S. da Silva and Derlis J. V. Ayala for environments, such as Leptodactylus fuscus, Rhinella valuable assistance in the field. schneideri and Scinax fuscovarius (Haddad et al., 2013). Crossodactylus schmidti, Limnomedusa macroglossa and Proceratophrys bigibbosa are the only endangered 550 Peterson Trevisan Leivas et al.

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Accepted by Gabriela Bittencourt-Silva