Herpetology Notes, volume 8: 661-667 (2015) (published online on 21 December 2015)

Anuran richness (Amphibia: Anura) in remnant forest fragments of Araucaria Forest and Atlantic Rainforest in Paraná, Brazil

Peterson T. Leivas1,3,*, Amanda S. Beltramin1, Reginaldo A. Machado2 and Maurício O. Moura3

Abstract. Our goal was to assess the species composition, reproductive modes and conservation status of the anurans of Araucaria Forest and Atlantic Rain Forest in the Campina Grande do Sul (CGS) and Bocaiúva do Sul (BS), in the state of Paraná, Brazil. The list of species was assembled based on field and museum records. We recorded 35 species that showed 11 different reproductive modes. Thirty five species occurred in CGS and 20 in BS, one species is classified as “data deficient” under the IUCN criteria while just two species hold this classification within the state. richness in these areas correspond to 24% of the known species diversity known for Paraná. Species richness and community composition correspond to the regional phytophysiognomy and local environmental heterogeneity.

Keywords: Anuran fauna, inventory, Atlantic Forest, Campina Grande do Sul, Bocaiúva do Sul.

Introduction From the Brazilian biomes, the Atlantic Forest Domain is considered to be the most diverse, with nearly 529 The Neotropical region holds the largest anuran anuran species, of which 60% are endemic (Haddad diversity of the world, and host eight biodiversity et al., 2013). Nevertheless, the anuran fauna of the hotspots. Within this region, Brazil is the country that Atlantic Forest is heavily threatened by anthropogenic possesses the greatest number of anuran 988 species factors, such as destruction (e.g.: real estate (Segalla et al., 2014). Approximately 40% of these occupation, expansion of agriculture and livestock) and species were described in the last 26 years (Pyron and degradation of native biota (e.g.: introduction of exotic Wiens, 2011). The increase in the described number of species) (Silvano and Segalla, 2005) and the synergism species, although associated to a variety of factors, is between these factors can potentially further aggravated mainly due to local species inventory and the situation, leading to alteration in the abundance and studies that catalogue diversity. These studies are species richness. This can affect the general structure of essential especially in countries that are greatly diverse communities, causing a cascade effect of biodiversity and have sizable environmental conflicts. loss (Stuart et al., 2004; Silvano and Segalla, 2005). Knowledge on the anuran fauna of the state of Paraná is restricted to a few portions of the state, and there are several gaps, especially on the occurrence and species 1 Universidade Federal do Paraná (UFPR). Programa de Pós- distribution. The available information is primarily Graduação em Ecologia e Conservação. Caixa postal 19020. related to the description of new species (e.g.: Garey et CEP 81531-980. Curitiba, PR, Brasil. al., 2012), new species occurrences for the state (e.g.: 2 Universidade Federal do Acre (UFAC). Laboratório de Conte et al., 2010), population studies of native (e.g.: Herpetologia, Centro Multidisciplinar, Campus Floresta. Hiert, Hoper and Moura, 2012) and exotic (e.g.: Leivas, CEP 69980-000. Cruzeiro do Sul, AC, Brasil. Moura and Fávaro, 2012) species and description of 3 Universidade Federal do Paraná (UFPR). Departamento de Zoologia. Caixa postal 19020. CEP 81531-980. Curitiba, PR, specie richness or checklist of species occurring in Brasil. particular areas (e.g.: Machado et al., 1999; Conte and * Corresponding author e-mail: [email protected] Rossa-feres, 2007). 662 Peterson T. Leivas et al.

Figure 1. Map showing the study areas of Araucaria Forest (triangles) and Atlantic Rain Forest (circle) phytogeographic domains, in the counties of Campina Grande do Sul (dark gray) and Bocaiúva do Sul (light gray), Paraná, Brazil.

Although all biomes in Paraná suffer anthropogenic in the counties of Campina Grande do Sul (CGS) and pressure, the Atlantic Rainforest (“Floresta Ombrófila Bocaiúva do Sul (BS), Paraná, Brazil (Maack, 2012). Densa” - FOD) and the Araucaria Forest (“Floresta de The region lies in the first plateau of Paraná, about Araucária or Floresta Ombrófila Mista” - FA) have 920m of altitude, and has a Subtropical Temperate been drastically reduced and only less than 8% of the climate classified as Cfa according to Köppen-Geiger original vegetation remains (Morellato and Haddad, (Maack, 2012). The surveyed areas are a mosaic of 2000). Information on the anuran fauna is currently forest fragments surrounded by anthropogenically limited to a few sites on the east slope of the Serra do modified areas (e.g.: agriculture, livestock and recreation Mar Mountains. activities). Given the importance of FA and FOD for biodiversity In CGS we sampled two areas, one within the FA maintenance of Brazilian anuran fauna, and due to the domain (-25.283333 S, -49.033333 W, datum= WGS lack of information in several regions of the Paraná state, 84) and another within the FOD domain (-24.983333 S, we here provide the species composition, description - 48.616667 W, datum = WGS 84). In BS we sampled of the reproductive modes, and suggest a conservation an area of the FA (-25.24000 S, -49.034167 W, datum status for the species occurring in FOD and FA in = WGS 84) (Figure 1). Campina Grande do Sul and Bocaiúva do Sul, Paraná, In CGS, in the FA area, we sampled in: (a) a marsh Brazil. with interior shrubby vegetation and marginal woody vegetation, (b) a set of four permanent ponds with Materials and Methods marginal shrubby and woody vegetation, (c) a stream of sandy bed in the interior of a forest fragment. In the Study site FOD area (CGS), we sampled: (a) two permanent ponds Fieldwork was conducted in Araucaria Forest (FA) and in the interior of the forest, (b) a marsh with interior Atlantic Rain Forest (FOD) phytogeographic domains shrubby vegetation and marginal woody vegetation, Anuran richness in forest fragments of Araucaria Forest and Atlantic Rainforest 663

Figure 2. Anuran species recorded in Campina Grande do Sul and Bocaiúva do Sul, Paraná, in Araucaria Forest and Atlantic Rain Forest. A = Ischnocnema henselii; B = Rhinella icterica; C = Proceratophrys boiei; D = Aplastodiscus perviridis; E = Dendropsophus elegans; F = D. minutus; G = Hypsiboas albopunctatus; H = H. bischoffi; I = Scinax aromothyella; J = Leptodactylus latrans; K = L. notoaktites; L = Lithobates catesbeianus. Photos: Peterson Trevisan Leivas.

(c) a stream with a rocky bed in the interior of a forest during four months, (12 days of sampling in each area) fragment. In BS we sampled the following sites: (a) a set with two people as sampling effort, at twilight or during of five permanent ponds with shrubby vegetation and the night (6:00 pm to 11:00 pm). marginal woody vegetation, (b) a stream with a rocky We consulted the available inventory of reproductive bed in the interior of the forest fragment with marginal sites and we used visual and auditory opportunistic shrubby vegetation. search to investigate the areas (Crump and Scott Jr., 1994; Scott Jr. and Woodward, 1994). Initially, we explored Data collection the reproductive sites for 10 minutes, so that we could We elaborated the species list for each county identify the local species through their vocalizations. identifying the forest formation in which the species Later, we actively searched for amphibian species in were registered, based on field sampling and museum those sites, using transects. During the samplings, we records. We conducted field sampling in three different captured, photographed and released the individuals. seasons. We sampled the areas in CGS between July The advertisement call of one male per species was 2001 and July 2002 (FA), and October 2012 to January recorded to confirm identification. We gathered data 2013 (FOD). We sampled the area in BS from December of species from museum records of the herpetological 2009 to November 2010. collection of Museu de História Natural Capão da We sampled the areas of FA in CGS and BS monthly Imbuia, Curitiba, Paraná. We used records made up to (two days per month). This totals 24 days of sampling in June 2012 (Appendix 1) and we adopted the taxonomy each area, with two people as sampling effort, at twilight proposed by Frost (2014). or during the night (6:00 pm to 11:00 pm). We sampled the areas of FOD in CGS for three days per month, 664 Peterson T. Leivas et al.

Table 1. List of anuran species recorded in Campina Grande do Sul and Bocaiúva do Sul in the vegetation domain of Atlantic Rain Forest and Araucaria Forest with information on their reproductive modes, regional, national and international threat status. FOD = Atlantic Rain Forest; FA = Araucaria Forest; STATUS = Global (IUCN), national (NA) and state (ES) threat status. LC = least concern; (DD) = data deficient. Reproductive mode classification follows Haddad and Prado (2005), Abrunhosa, Wogel and Pombal (2006), Haddad, Toledo and Prado (2008), Kopp, Signorelli and Bastos (2010) and Silva et al. (2012).

Campina Grande do Sul Bocaiúva do Sul STATUS PHOTO Reproductive FAMILY / SPECIES Field Museum Field Museum modes IUCN NA ES FA FOD BRACHYCEPHALIDAE Ischnocnema henselii (Peters, 1870) X X X 23 LC 2A BUFONIDAE Rhinella abei (Baldissera-Jr, Caramaschi and Haddad, 2004) X X X X 1 or 2 LC R. icterica (Spix, 1824) X X X X 1 LC 2B HYLIDAE Aplastodiscus albosignatus (A.Lutz and B. Lutz, 1938) X X X X 5 LC A. perviridis (A. Lutz in B. Lutz, 1950) X X X 5 LC 2D Bokermannohyla circumdata (Cope, 1871) X X 4 LC B. hylax (Heyer, 1985) X 4 LC Dendropsophus elegans (Wied-Neuwied, 1824) X 24 LC 2E D. minutus (Peters, 1872) X X X X 1 LC 2F D. werneri (Cochran, 1952) X 1 LC D. microps (Peters, 1872) X X 1 LC Hypsiboas albopunctatus (Spix, 1824) X X 1 LC 2G H. bischoffi (Boulenger, 1887) X X X X 1 LC 2H H. faber (Wied-Neuwied, 1821) X X X 4 LC H. prasinus (Burmeister, 1856) X X X X 1 or 2 LC H. semiguttatus (A. Lutz, 1925) X X 2 LC distincta A. Lutz in B. Lutz, 1950 X X X X 24 LC Scinax aromothyella Faivovich, 2005 X 1 DD 2I S. fuscovarius (A. Lutz, 1925) X X X 1 LC S. perereca Pombal, Haddad and Kasahara, 1995 X X 1 LC S. rizibilis (Bokermann, 1964) X X 11 LC Sphaenorhynchus caramaschii Toledo, Garcia, Lingnau and X X X X 1 or 2 LC Haddad, 2007 HYLODIDAE Crossodactylus caramaschii Bastos and Pombal, 1995 X 3 LC LEPTODACTYLIDAE Leptodactylus gr. marmoratus X X X 32 LC Leptodactylus latrans (Steffen, 1815) X X X 11 LC 2J L. notoaktites (Heyer, 1978) X X 30 LC 2K Physalaemus cuvieri (Fitzinger, 1826) X X 11 LC P. gracilis (Boulenger, 1883) X 11 LC P. lateristriga (Steindachner, 1864) X X X X 11 --- P. maculiventris (Lutz, 1925) X X 11 or 28 LC DD MICROHYLIDAE Chiasmocleis leucosticta (Boulenger, 1888) X 10 LC DD Elachistocleis bicolor (Guérin-Méneville, 1838) X 1 LC ODONTOPHRYNIDAE Proceratophrys boiei (Wied-Neuwied, 1825) X X X 1 LC 2C Odontophrynus americanus (Duméril and Bibron, 1841) X 1 LC RANIDAE Lithobates catesbeianus (Shaw, 1802) X X X 1 LC 2L TOTAL 26 24 17 20 0 

Data analysis methodology were not exactly the same and in order to compare the observed richness and the estimated Studies on species inventory in different communities richness for each area, we used the non-parametrical might produce different results, even if the methodology estimator Chao II (Chao and Shen, 2004). We calculated and sampling effort used were similar (Hortal, Borges the estimates from 1000 randomizations in the software and Gaspar, 2006). Since our sampling effort and EstimateS version 8.2.0. Anuran richness in forest fragments of Araucaria Forest and Atlantic Rainforest 665

Based on the list of occurring species, we indicated the modes (Table 1): mode 1 was exhibited by16 species, threat status of the species, according to international, mode 11 by six species, mode 2 by four species, and national, and regional criteria (Table 1). Data were mode 4 by three species. Modes 5 and 24 were exhibited retrived from: the IUCN “Red List of Threatened by two species. Modes 3, 10, 23, 28, 30 and 32 were Species version 2013.2” (IUCN, 2013); the national red exhibited by only one species. Four species exhibited list “Livro Vermelho Da Fauna Brasileira Ameaçada de more than one reproductive mode. Extinção” (Machado, Drummond and Paglia, 2008); the According to the IUCN list, from the recorded species, regional red list “Livro Vermelho da Fauna Ameaçada 33 species are classified as “LC” (least concern), one no Estado do Paraná” (Mikich and Bérnils, 2004). species (S. aromothyella) is classified as “DD” (data We also indicated the reproductive modes for each deficient) and one species (P. lateristriga) is not yet recorded species according to the records from Haddad assessed. No species fit any national threat category. and Prado (2005), Abrunhosa, Wogel and Pombal Physalaemus maculiventris and C. leucosticta are (2006), Haddad, Toledo and Prado (2008), Kopp, classified as “DD” in Paraná (Table 1). Signorelli and Bastos (2010) and Silva et al. (2012). Discussion Results Our results showed that at least 35 species occurs in We registered a total of 35 species: 20 species were our surveyed areas. The computed estimated richness is recorded in BS and 35 in CGS (Table 1). From all the close to the observed values at both sites and the Chao2 species registered in CGS, 32 species were identified in curves are asymptotic suggesting our sampling protocol the field, 17 in museum (48 specimens) and 15 both in (field and museum) worked properly to determine field and museum. All species of BS were recorded only species richness. However, as the estimators are lower in the field (Table 1). In CGS we estimated a species bound (Chao, 1984) it should be viewed as a minimum richness of 26 (26 - 26.85 species) and 25 species (24 richness. Despite of this, this number of species is similar - 31.12 species) for the FA and FOD area, respectively. to previous published inventories in areas of Araucaria In BS, we estimated a species richness of 20 (20 - 20.62 forest (Conte and Machado, 2005; Conte and Rossa- species). Feres, 2007; Cunha, Oliveira and Hartmann, 2010). On The species recorded are distributed in eight families: the contrary, this number is well below published values Brachycephalidae (one species), Bufonidae (two for Atlantic rain forest sites (Feio and Caramaschi, 2002; species), Hylidae (19 species), Hylodidae (one species), Armstrong and Conte, 2010). Leptodactylidae (seven species), Microhylidae (two At both sites we sampled as many microhabitats species), Odontophrynidae (two species) and Ranidae as possible and discover that in general FA and FOD (one species) (Table 1 and Figure 2). The most are extremely similar to each other, roughly 60% representative families were the Hylidae holding 54.28% of similarity (Table 1). At a regional scale, there is a of the recorded species, followed by Leptodactylidae tendency of anuran species to occur according to the (20% of the recorded species). The families Bufonidae, vegetation type (Conte and Rossa-Feres, 2006; Von Microhylidae and Odontophrynidae held 5.71% of May et al., 2010). Some Araucaria forest and Atlantic representatives each, and Brachycephalidae, Hylodidae rainforest sites are near each other, particularly on the and Ranidae were each represented by 2.85% of the east of the state of Paraná, therefore high similarity species. between these two biomes was expected (Conte and As for the occurrence of species within the forest Rossa-Feres, 2006; Gardner et al., 2007; Blair and formations, 10 species (Odontophrynus americanus, Doan, 2009). Hypsiboas albopunctatus, H. semiguttatus, Scinax Although, there was more specialized reproductive aromothyella, S. perereca, S. rizibilis, Physalaemus modes (such as modes 4, 11, 23, 24 and 32), most of the cuvieri, P. gracilis, Elachistocleis bicolor and Lithobates species we sampled display the reproductive mode 1 or catesbeianus) were registered only in FA and seven 11, and both modes are linked to reproductive patterns species (Bokermannohyla circumdata, Dendropsophus in permanent ponds (Haddad and Prado, 2005). Mode elegans, D. werneri, D. microps, Crossodactylus 1 is the most primitive and generalized reproductive caramaschii, P. maculiventris and Chiasmocleis mode of anura (Gomez-Mestre, Pyron and Wiens, leucosticta) only in FOD. 2012). As both of our sampling sites have permanent The recorded species displayed at least 11 reproductive ponds, the dominance of these modes likely mirror the 666 Peterson T. Leivas et al. availability of reproductive sites as well as contributes Bland, L.M., Collen, B., Orme, C.D.L., Bielby, J. (2012): Data to the observed similarity between FA and FOD. uncertainty and the selectivity of extinction risk in freshwater Most of the recorded species have stable populations, invertebrates. Diversity and Distribuition 18: 1211-1220. Cassini, C.S., Cruz, C.A.G., Caramaschi, U. (2010): Taxonomic based on the IUCN classification criteria (IUCN, 2013). review of Physalaemus olfersii (Lichtenstein & Martens, 1856) Currently, only one detected species is classified as with revalidation of Physalaemus lateristriga (Steindachner, data deficient, DD (S. aromothyella) and only one 1864) and description of two new related species (Anura: species (P. lateristriga) is not assessed yet. For both Leiuperidae). Zootaxa 2491: 1-33. these species we encourage the need to gather more Chao, A. (1984): Non-parametric estimation of the number of information (Bland et al., 2012, Morais et al., 2013). classes in a population. Scandinavian Journal of Statistics 11: Using only the approximation of the known geographic 265-270. Chao, A., Shen, T.J. (2004): Nonparametric Prediction in range size of each species (Kolenc et al., 2007; Cassini, Species Sampling. Journal of Agricultural, Biological, and Cruz and Caramaschi, 2010; Pereyra et al., 2012; Environmental Statistics 9(3): 253-269. Batista and Bastos, 2014) both species should probably Conte, C.E., Machado, R.A. (2005): Riqueza de espécies e be categorized as Least Concern (more than 20.000 distribuição espacial e temporal em comunidade de anuros km2, IUCN, 2013, Morais et al., 2013). However, it is (Amphibia: Anura) em uma localidade de Tijucas do Sul, important to note that population studies of Paraná, Brasil. Revista Brasileira de Zoologia 22: 940-948. Conte, C.E., Nomura, F., Machado, R.A., Kwet, A., Lingnau, employing accurate census techniques are still scarce in R., Rossa-Feres, D.C. (2010): Novos registros na distribuição Brazil (Vasconcelos and Colli, 2009; Hiert, Hoper and geográfica de anuros na Floresta com Araucária e considerações Moura, 2012) therefore a more accurate analyses should sobre suas vocalizações. Biota Neotropica 10: 201-224. be performed by IUCN specialists. Conte, C.E., Rossa-Feres, D.C. (2006): Diversidade e ocorrência While providing anuran inventory data from two sites temporal da anurofauna (Amphibia: Anura) em São José dos in southern Brazil we increased the know distribution Pinhais, Paraná, Brasil. Revista Brasileira de Zoologia 23: 162- records of anura for FA and FOD. Also, we here report 175. Conte, C.E., Rossa-Feres, D.C. (2007): Riqueza e distribuição the record of L. catesbeianus (an invasive species), that espaço-temporal de anuros em um remanescente de Floresta de can potentially have a negative impact on native species Araucária no sudeste do Paraná. Revista Brasileira de Zoologia (Leivas, Leivas and Moura, 2012). 24: 1025-1037. Crump, M.L., Scott Jr., N.J. (1994): Visual encounter surveys. Acknowledgements. This research was partially supported In: Measuring and Monitoring Biological Diversity - Standard by grants from the Conselho de Desenvolvimento Cientifico e Methods for Amphibians, p. 84-92. Heyer, W.R., Donnelly, Tecnólogico – CNPq (process 475461/2007 and 312357/2006) to M.A., McDiarmid, R.W., Hayek, L.A.C., Foster, M.S., Eds., Mauricio O. Moura. Amanda Beltramin and Peterson T. Leivas Washington, Smithsonian. received, respectively, a masters and doctoral stipend from the Cunha, A.K., Oliveira, I.S., Hartmann, M.T. (2010): Anurofauna Coordenação de Aperfeiçoamento de Pessoal de Nivel Superior da Colônia Castelhanos, na área de proteção ambiental de - CAPES. We thank the manager of the herpetological collection Guaratuba, Serra do Mar paranaense, Brasil. Biotemas 23(2): from Museu de História Natural Capão da Imbuia, Julio Leite 123-134. for allowing our access to the collection, Angie de Souza who Feio, R.N., Caramaschi, U. (2002): Contribuição ao conhecimento assisted to assess the species records from the museum and Bruno da herpetofauna do nordeste do estado de Minas Gerais, Brasil. Kazuo Nakagawa for assistance during field work. Phyllomedusa 1(2): 105-111. Frost, D.R. (2014): Amphibian Species of the World: an Online References Reference, version 6.0, American Museum of Natural History, New York, USA. Available at: http://research.amnh.org/ Abrunhosa, P.A., Wogel, H., Pombal Jr., P.J. (2006): Anuran herpetology/amphibia/index.html. Last accessed on 7 September temporal occupancy in a temporary pond from the Atlantic rain 2014. forest, southeastern Brazil. Herpetological Journal 16(2): 115- Gardner, T.A., Fitzherbert, E.B., Drewes, R.C., Howell, K.M., 122. Caro, T. (2007): Spatial and Temporal Patterns of Abundance Armstrong, C.G., Conte, C.E. (2010): Taxocenose de anuros and Diversity of an East African Leaf Litter Amphibian Fauna. (Amphibia: Anura) em uma área de Floresta Ombrófila Densa Biotropica 39: 105-113. no sul do Brasil. Biota Neotropica 10: 39-46. Garey, M.V., Lima, A.M.X., Hartmann, M.T., Haddad, C.F.B. Batista, V.G., Bastos, R.P. (2014): Anurans from a Cerrado-Atlantic (2012): A new species of miniaturized toadlet, genus Forest ecotone in Campos Gerais region, southern Brazil. Check Brachycephalus (Anura: Brachycephalidae), from southern List 10(3): 574-582. Brazil. Herpetologica 68:266-271. Blair, C., Doan, T.M. (2009): Patterns of Community Structure Gomez-Mestre, I., Pyron, R.A., Wiens, J.J. (2012): Phylogenetic and Microhabitat Usage in Peruvian Pristimantis (Anura: analyses reveal unexpected patterns in the evolution of Strabomantidae). Copeia 2: 303-312. reproductive modes in . Evolution 66: 3687-3700. Anuran richness in forest fragments of Araucaria Forest and Atlantic Rainforest 667

Haddad, C.F.B., Prado, C.P.A. (2005): Reproductive modes in of extant frogs, salamanders, and caecilians. Molecular frogs and their unexpected diversity in the Atlantic Forest of Phylogenetics and Evolution 61: 543-583. Brazil. Bioscience 55: 207-217. Scott Jr., N., Woodward, B.D. (1994): Surveys at breeding sites. Haddad, C.F.B., Toledo, L.F., Prado, C.P.A. (2008): Anfíbios da In: Measuring and Monitoring Biological Diversity - Standard Mata Atlântica: guia dos anfíbios anuros da Mata Atlântica. São Methods for Amphibians, p. 118-125. Heyer, W.R., Donnelly, Paulo, Neotropica. M.A., McDiarmid, R.W., Hayek, L.A.C., Foster, M.S., Eds., Haddad, C.F.B., Toledo, L.F., Prado, C.P.A., Loebmann, D., Washington, Smithsonian. Gasparini, J.L., Sazima, I. (2013): Guia dos Anfíbios da Mata Segalla, M.V., Caramaschi, U., Cruz, C.A.G., Grant, T., Haddad, Atlântica: Diversidade e Biologia. São Paulo, Anolis Books C.F.B., Langnone, J., Garcia, P.C.A. (2014): Brazilian Editora. Amphibians: List of Species. Herpetologia Brasileira 3(2): 37- Hiert, C., Hoper, J.J., Moura, M.O. (2012): Constant breeding and 48. low survival rates in the subtropical Striped in southern Silva, F.R., Almeida-Neto, M., Prado, V.H.M., Haddad, C.F.B., Brazil. Journal of Zoology 288: 151-158. Rossa-Feres, D.C. (2012): Humidity levels drive reproductive Hortal, J., Borges, P.A.V., Gaspar, C. (2006): Evaluating the modesand phylogenetic diversity of amphibians in the Brazilian performance of species richness estimators: sensitivity to sample Atlantic Forest. Journal of Biogeography 39: 1720-1732. grain size. Journal of Ecology 75: 274-287. Silvano, D.L., Segalla, M.V. (2005): Conservação de anfíbios no IUCN - International Union For Conservation For Nature (2013): Brasil. Megadiversidade 1: 79-86. The IUCN red list of threatened species, version 2013.2. Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, Available at: http://www.iucnredlist.org. Last accessed on 7 A.S.L., Friscman, D.L., Waller, R.W. (2004): Status and trends September 2014. of amphibians declines and extinctions worldwide. Sicence 306: Kolenc, F., Borteiro, C., Tedros, M., Prigioni, C. (2007): The 1783-1786. tadpole of Scinax aromothyella (Anura: Hylidae) from Uruguay. Vasconcelos, M.M., Colli, G.R. (2009): Factors affecting the Studies on Neotropical Fauna and Environment 42: 175-180. population dynamics of two toads (Anura: Bufonidae) in a Kopp, K., Signorelli, L., Bastos, R.P. (2010): Distribuição temporal seasonal Neotropical savanna. Copeia 2009(2): 266-276. e diversidade de modos reprodutivos de anfíbios anuros no Von May, .R., Jacobs, J.M., Santa-Cruz, R., Valdivia, J., Huamán, Parque Nacional das Emas e entorno, Estado de Goiás, Brasil. J.M., Donnelly, M.A. (2010): Amphibian community structure Iheringia 100(3):192-200. as a function of forest type in Amazonian Peru. Journal of Leivas, P.T., Leivas, F.W., Moura, M.O. (2012): Diet and trophic Tropical Ecology 26: 509-519. niche of Lithobates catesbeianus (Amphibia: Anura). Zoologia 29(5): 405-412. Leivas, P.T., Moura, M.O., Fávaro, L.F. (2012): The reproductive biology of the invasive Lithobates catesbeianus (Amphibia: Anura). Journal of Herpetology 46: 153-161. Maack, R. (2012): Geografia física do estado Paraná, 4nd Edition. Curitiba, UEPG. Machado, R.A., Bernarde, P.S., Morato, S.A.A., Anjos, L. (1999): Análise comparada da riqueza de anuros entre duas áreas com diferentes estados de conservação no município de Londrina, Paraná, Brasil (Amphibia, Anura). Revista Brasileira de Zoologia 16(4): 997-1004. Appendix 1. List of catalogued specimens from the Machado, A.M.B., Drummond, G.M., Paglia, A.P. (2008): Livro counties of Campina Grande do Sul hosted in the vermelho da fauna brasileira ameaçada de extinção. Brasília, MMA. herpetological collection of Museu de História Natural Mikich, S.B., Bérnils, R. (2004): Livro vermelho da fauna ameaçada Capão da Imbuia, Curitiba (MHNCI), Paraná, Brazil, no Estado do Paraná. Curitiba, Governo do Paraná. analyzed for this study. Morais, A.R., Siqueira, M.N., Lemes, P., Maciel, N.M., Marco Jr., MHNCI N°: 866, 2142, 2144, 2145, 2146, 2147, 4311, P.M., Brito, D. (2013): Unraveling the conservation status of 4312, 4367, 4368, 4369, 4370, 4371, 4372, 4373, 4374, Data Deficient species. Biological conservation 166: 98-102. 4375, 4376, 4377, 4378, 4379, 4380, 4381, 4382, 4383, Morellato, L.P.C., Haddad, C.F.B. (2000): Introduction: The 4384, 4385, 4386, 4387, 4601, 4602, 4603, 4604, 4605, brazilian atlantic forest. Biotropica 32: 786-792. Pereyra, M.O., Borteiro, C., Baldo, D., Kolenc, F., Conte, C.E. 4606, 4607, 4608, 4609, 4610, 4611, 4612, 4613, 4614, (2012): Advertisement call of the closely related species Scinax 4615, 4616, 4617, 4618, 4619, 4620, 4621, 4622, 4623, aromothyella Faivovich 2005 and S. berthae (Barrio 1962), 4624, 6576, 6577, 6578, 6579, 6580, 6581, 6582, 6583. with comments on the complex calls in the S. catharinae group. Herpetological Journal 22: 133-137. Pyron, R.A., Wiens, J.J. (2011): A large-scale phylogeny of Accepted by Angelica Crottini Amphibia including over 2800 species, and revised classification