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Herpetology Notes, volume 10: 547-560 (2017) (published online on 16 October 2017)

Anurans from the mountain chain Serra do Mar: a critical area for conservation in the Atlantic ,

Felipe Siqueira Campos1, 2,* and Ricardo Lourenço-de-Moraes3

Abstract. We present an anuran inventory of the mountain region of the Serra do Mar, Brazil, located in the biome. We conducted a fieldwork comprising the major and best well-preserved Atlantic Forest remnants from Brazil, using acoustic and visual nocturnal/diurnal assessments. In total, we recorded 99 anuran , of which about 70% are endemic to the Atlantic Forest and represent around 20% of all amphibian species described for this biome. The high levels of endemism, the distribution patters and the conservation status of the anuran species turn the mountains of the Serra do Mar into a key conservation region for within the Atlantic Forest hotspot.

Keywords. Amphibia, Atlantic Forest, species inventory, species distribution, conservation.

Introduction recognized amphibian species and several more species that still need to be described (Silva and Casteleti, 2003; The Atlantic Forest biome represents one of the Haddad et al., 2013). five most important hotspots on Earth The Serra do Mar is a mountain chain that extends (Mittermeier et al., 2011). Originally, it covered around for more than 1,000 km (Almeida and Carneiro, 1998), 1,500,000 km2 of which only about 12% (194,524 km2) stretching from the south of the Espírito Santo state remains in Brazil, Paraguay and Argentina (Ribeiro to the North of the state (Rizzini, et al., 2009), corresponding to about 100,000 km2 of 1979; Olson et al., 2001). This is an area of extreme Brazilian forest remnants (Tabarelli et al., 2005). This biological importance that covers 8% of the Atlantic biome faces high rate of loss (Teixeira et al., Forest biome and accounts more than 13% of the 2009), which is one of the main causes of amphibian remaining forest (Ribeiro et al., 2009). The Brazilian extinctions (Stuart et al., 2004; Becker et al., 2007; Ministry of the Environment has rated this region with Ferreira et al., 2016). Despite this, Atlantic Forest is the highest priority towards conservation within the still considered the leader biome in amphibian diversity Atlantic Forest hotspot (MMA, 2000). According to in Brazil (Haddad et al., 2013), accounting for more the biogeographical sub-regions proposed by Silva and than 50% of all amphibian species (Haddad et al., Casteleti (2003), Serra do Mar covers the best well- 2013). Their geographical characteristics with wide preserved remnants, which holds 36.5% of its original altitudinal range have favoured high species richness vegetation (Ribeiro et al., 2009). This region has been and high levels of endemism, including more than 500 highly fragmented, with 79% of the remaining smaller than 0.5 km2. However, part of the biome still covers wide forest remnants, with fragments larger than 1,000 km2 along the coastal mountains of 1 Departament de Biologia Evolutiva, Ecologia i Ciències state, larger than 500 km2 in the Paraná state, and larger Ambientals, Facultat de Biologia, Universitat de Barcelona, than 300 km2 in the state (Ribeiro et al., ES-08028, Barcelona, Spain. 2009). On the altitudinal gradient, Serra do Mar also 2 CAPES Foundation, Ministry of Education of Brazil, 70040- has continuous forests ranging from the sea level up to 020, Brasília, DF, Brazil. 2,300 m (Almeida and Carneiro, 1998). 3 Departamento de Ecologia, Laboratório de Herpetologia e Comportamento , Universidade Federal de Goiás, A key factor accounting for amphibian species richness 74001-970, Goiânia, GO, Brazil. in the Atlantic Forest is the large number of * Corresponding author e-mail: [email protected] and microhabitats (Haddad, 1998), which favours the 548 Felipe Siqueira Campos & Ricardo Lourenço-de-Moraes

characterized by monthly mean temperatures of at least 18 °C and high annual rainfall averages (> 2,000 mm; Walsh, 1996). Vegetation types comprise tree mosaics with different shifts in floristic composition as elevation increases and are classified as montane and sub-montane rain forest composed of moist broadleaf trees (Rizzini, 1979; Olson et al., 2001). We sampled each Protected Area for 10 days between January and March 2015 (wet season) from 5 pm to 1 am, totalling 480 hours of sampling effort per person (i.e., two researchers). In all localities, we used acoustic and visual nocturnal/diurnal assessments at different microhabitats along a 2,000 m forest transect in each sampled site (e.g., streams, swamps, bromeliads, bamboos, burrows, rocks, vegetation, and leaf-litter). Figure 1. Map of the sampled sites in the mountain chain Serra do Mar, Brazil, representing their corresponded forest We focused the study in an altitudinal range lower than remnants and altitude at a spatial resolution of 0.1 latitude/ 300 m and higher than 700 m above sea level (asl). We longitude degrees. 1. Parque Ecológico Spitzkopf, SC; 2. identified the species by comparing their morphological Parque Estadual Pico do Marumbi, PR; 3. Estação Ecológica characteristics observed in the field and reviewing de Juréia-Itatins, SP; 4. Parque Estadual da Serra do Mar their original or revalidated descriptions to support the Núcleo , SP; 5. ���������������������������� taxonomic identifications. We followed Frost (2017) for Órgãos, RJ; 6. Reserva Biológica Augusto Ruschi, ES. the amphibian nomenclature.

Results and Discussion In the six Protected Areas surveyed in the mountain number of habitat-specialist species (Lourenço-de- chain Serra do Mar, we found 99 anuran species Moraes et al., 2013). In addition, there is a high degree distributed in 13 families and 31 genera (Table 1, Figs. of isolation among populations, due to the rugged 3–8). About 70% of the sampled species are endemic relief with rivers and mountains that may represent to the Brazilian Atlantic Forest and represents around biogeographic barriers (Haddad, 1998; Marques et al., 20% of all amphibian species described for this biome. 1998). We found the highest species richness in the “Parque Species inventories are crucial for answering central Estadual da Serra do Mar Núcleo Caraguatatuba” questions in biogeography (Lomolino, 2004), ecology (34 species) and the lowest in the “Parque Ecológico (Brown et al., 1996) and evolutionary biology (Holt, Spitzkopf” (23 species). We found approximately 2003). Additionally, species lists are critical to indicate twice the number of species in lowland areas (<300 knowledge gaps, as well as to identify priority areas m asl.) than highland areas (>700 m asl.), of which for conservation (e.g., Toledo and Batista, 2012; 60 species occurred exclusively below 300 m, 22 Verdade et al., 2012; Campos et al., 2014). In this species exclusively above 700 m, and 17 species in context, we carried out fieldwork comprising the major both altitudinal ranges (Table 1). Among the different forest remnants of the mountain chain Serra do Mar, microhabitats searched, we observed 36% of the species supplementing the current amphibian dataset for this in swamps, 18% in streams, 17% in leaf-litter, 15% in region and highlighting the importance of these forests trees, 8% in bromeliads, 3% in rocks, 2% burrows, and for the species conservation status. 1% in bamboos. In this study, we presented the first anuran species Material and Methods list for the Parque Ecológico Spitzkopf, in the Santa We conducted fieldwork at six Protected Areas located Catarina state, and the Parque Estadual da Serra do in the mountain chain Serra do Mar, Brazil (Figs. 1 Mar Núcleo Caraguatatuba, in the São Paulo state. Our and 2). The general climate of this region is tropical results showed four new species distribution records for wet with frequent rain occurring every month (Walsh, the studied region, expanding the knowledge about the 1996). This non-seasonal tropical rain forest climate is occurrence of anurans in the mountain chain Serra do Anurans from the mountain chain Serra do Mar, Brazil 549

Figure 2. Some environments of the sampled sites in the mountain chain Serra do Mar, Brazil. A) Rocky stream in the Parque Ecológico Spitzkopf, SC; B) Mountain chain in the Parque Estadual Pico do Marumbi, PR; C) Forest fragment in the Estação Ecológica de Juréia-Itatins, SP; D) Forest bromeliads in the Parque Estadual da Serra do Mar Núcleo Caraguatatuba, SP; E) Mountain chain in the Parque Nacional da Serra dos Órgãos, RJ; F) Dense ombrophylous forest in the Reserva Biológica Augusto Ruschi, ES.

Mar. We reported the first state records for (IUCN, 2017). We found only one species classified as erythromera in the Espírito Santo state, henseli Vulnerable (VU), three as Near Threatened (NT), and and Adenomera nana in the Paraná state, and four as Data Deficient (DD). In this context, several pipilans in the São Paulo state. studies have highlighted that the lack of information Table 1 shows the conservation status of the recorded regarding amphibian species occurrence needs to species according to the IUCN red list categories be straightaway addressed by scientific researchers, 550 Felipe Siqueira Campos & Ricardo Lourenço-de-Moraes

Figure 3. Some amphibian species sampled in the mountain chain Serra do Mar, Brazil. A) Adenomera bokermanni; B) Aplastodiscus albosignatus; C) Aplastodiscus arildae; D) Aplastodiscus ehrhardti; E) caramaschii; F) Bokermannohyla circumdata; G) Bokermannohyla hylax; H) Brachycephalus ephippium. Anurans from the mountain chain Serra do Mar, Brazil 551

Figure 4. Some amphibian species sampled in the mountain chain Serra do Mar, Brazil. A) Cycloramphus acangatan; B) Cycloramphus brasiliensis; C) branneri; D) Dendropsophus microps; E) Euparkerella cochranae; F) Gastrotheca albolineata; G) Haddadus binotatus; H) Crossodactylus gaudichaudii. 552 Felipe Siqueira Campos & Ricardo Lourenço-de-Moraes

Figure 5. Some amphibian species sampled in the mountain chain Serra do Mar, Brazil. A) Hylodes heyeri; B) Hylodes pipilans; C) Boana albomarginata; D) Boana bischoffi; E) Boana crepitans; F) Boana semilineata; G) Boana faber; H) Ischnocnema erythromera. Anurans from the mountain chain Serra do Mar, Brazil 553

Figure 6. Some amphibian species sampled in the mountain chain Serra do Mar, Brazil. A) Ischnocnema guentheri; B) Ischnocnema parva; C) Leptodactylus notoaktites; D) goeldii; E) Myersiella microps; F) nanus; G) Proceratophrys boiei (gray pattern); H) Proceratophrys boiei (orange pattern). 554 Felipe Siqueira Campos & Ricardo Lourenço-de-Moraes

Figure 7. Some amphibian species sampled in the mountain chain Serra do Mar, Brazil. A) Proceratophrys appendiculata; B) Macrogenioglottus alipioi; C) ; D) ; E) ; F) Ololygon albicans; G) Ololygon argyreornata; H) Ololygon catharinae. Anurans from the mountain chain Serra do Mar, Brazil 555

Figure 8. Some amphibian species sampled in the mountain chain Serra do Mar, Brazil. A) Ololygon flavoguttata; B) Ololygon littoralis C) Ololygon v-signatus D) granulatus; E) Scinax hayii; F) miliaris; G) uranoscopa; H) Zachaenus parvulus. 556 Felipe Siqueira Campos & Ricardo Lourenço-de-Moraes

Table 1. Anuran species registered in the six Protected Areas surveyed in the mountain chain Serra do Mar, Brazil, according to their Red List categories (IUCN, 2017) and altitudinal ranges recorded. 1. Parque Ecológico Spitzkopf, SC; 2. Parque Estadual Pico do Marumbi, PR; 3. Estação Ecológica de Juréia-Itatins, SP; 4. Parque Estadual da Serra do Mar Núcleo Caraguatatuba, SP; 5.��������������������������������������� � ; 6. Reserva Biológica Augusto Ruschi, ES.

Sampled sites Altitude Species Red list Category 1 2 3 4 5 6 <300m >700m Family Brachycephalus ephippium (Spix, 1824) LC X Ischnocnema erythromera (Heyer, 1984) DD X Ischnocnema aff guentheri (Steindachner, 1864) LC X X Ischnocnema henselii (Peters, 1872) LC X Ischnocnema oea (Heyer, 1984) NT X Ischnocnema parva (Girard, 1853) LC X Family Bufonidae Dendrophryniscus brevipollicatus Jiménez de la Espada, 1870 LC X Dendrophryniscus leucomystax Izecksohn, 1968 LC X Rhinella abei (Baldissera-Jr, Caramaschi & Haddad, 2004) LC X X (Wied-Neuwied, 1821) X (Spix, 1824) LC X X Rhinella henseli (Lutz, 1934) LC X Rhinella hoogmoedi Caramaschi & Pombal, 2006 LC X (Spix, 1824) LC X Rhinella ornata (Spix, 1824) LC X X Rhinella schneideri (Werner, 1894) LC X Family Centrolenidae Vitreorana eurygnatha (Lutz, 1925) LC X Vitreorana uranoscopa (Müller, 1924) LC X Family Craugastoridae Euparkerella cochranae Izecksohn, 1988 LC X Haddadus binotatus (Spix, 1824) LC X X Family 2 Cycloramphus acangatan Verdade & Rodrigues, 2003 VU X Cycloramphus boraceiensis Heyer, 1983 LC X Cycloramphus brasiliensis (Steindachner, 1864) NT X Thoropa miliaris (Spix, 1824) LC X X Zachaenus parvulus (Girard, 1853) LC X Family Eleutherodactylidae Adelophryne glandulata Lourenço-de-Moraes, Ferreira, NE X Fouquet & Bastos 2014 Family Hemiphractidae Fritziana fissilis (Miranda Ribeiro, 1920) LC X Fritziana ohausi (Wandolleck, 1907) LC X Gastrotheca albolineata (Lutz & Lutz, 1939) LC X Family Aplastodiscus albofrenatus (Lutz, 1924) LC X X Aplastodiscus albosignatus (Lutz & Lutz, 1938) LC X X Aplastodiscus arildae (Cruz & Peixoto, 1987) LC X Aplastodiscus ehrhardti (Müller, 1924) LC X Aplastodiscus leucopygius (Cruz & Peixoto, 1985) LC X Aplastodiscus perviridis Lutz, 1950 LC X Aplastodiscus weygoldti (Cruz & Peixoto, 1987) NT X Boana albomarginata (Spix, 1824) LC X Boana albopunctata (Spix, 1824) LC X Boana bischoffi (Boulenger, 1887) LC X Boana caingua (Carrizo, 1991) LC X Boana crepitans (Wied-Neuwied, 1824) LC X X

Boana faber (Wied-Neuwied, 1821) LC X X Boana prasina (Burmeister, 1856) LC X Boana raniceps (Cope, 1862) LC X 2

Cycloramphus boraceiensis Heyer, 1983 LC X Cycloramphus brasiliensis (Steindachner, 1864) NT X Thoropa miliaris (Spix, 1824) LC X X Zachaenus parvulus (Girard, 1853) LC X Family Eleutherodactylidae Adelophryne glandulata Lourenço-de-Moraes, Ferreira, NE X Fouquet & Bastos 2014 Family Hemiphractidae Fritziana fissilis (Miranda Ribeiro, 1920) LC X Fritziana ohausi (Wandolleck, 1907) LC X Gastrotheca albolineata (Lutz & Lutz, 1939) LC X Family Hylidae Aplastodiscus albofrenatus (Lutz, 1924) LC X X Aplastodiscus albosignatus (Lutz & Lutz, 1938) LC X X Aplastodiscus arildae (Cruz & Peixoto, 1987) LC X Aplastodiscus ehrhardti (Müller, 1924) LC X Aplastodiscus leucopygius (Cruz & Peixoto, 1985) LC X Aplastodiscus perviridis Lutz, 1950 LC X Aplastodiscus weygoldti (Cruz & Peixoto, 1987) NT X Anurans from the mountain chain Serra do Mar, Brazil Boana albomarginata (Spix, 1824) LC X 557 Boana albopunctata (Spix, 1824) LC X Table 1. Continued.Boana bischoffi (Boulenger, 1887) LC X Boana caingua (Carrizo, 1991) LC X Boana crepitans (Wied-Neuwied, 1824) Sampled sites LC XAltitude X Species Red list Category 1 2 3 4 5 6 <300m >700m BoanaFamily faber Brachycephalidae (Wied-Neuwied, 1821) LC X X BoanaBrachycephalus prasina (Burmeister, ephippium (Spix, 1856) 1824) LC X X 3 BoanaIschnocnema raniceps erythromera (Cope, 1862) (Heyer, 1984) DD LC X X BoanaIschnocnema semilineata aff guentheri (Spix, 1824) (Steindachner, 1864) LC X X IschnocnemaBokermannohyla henselii caramaschii (Peters, 1872)(Napoli, 2005) LC X X IschnocnemaBokermannohyla oea circumdata(Heyer, 1984) (Cope, 1871) NTLC X X IschnocnemaBokermannohyla parva hylax (Girard, (Heyer, 1853) 1985) LC X X DendropsophusFamily Bufonidae bipunctatus (Spix, 1824) LC X DendropsophusDendrophryniscus branneri brevipollicatus (Cochran, Jiménez 1948) de la Espada, 1870 LC X DendropsophusDendrophryniscus decipiens leucomystax (Lutz, Izecksohn, 1925) 1968 LC X DendropsophusRhinella abei (Baldissera-Jr, elegans (Wied-Neuwied, Caramaschi &1824) Haddad, 2004) LC X X DendropsophusRhinella crucifer giesleri (Wied-Neuwied, (Mertens, 1950)1821) LC X DendropsophusRhinella granulosa microps (Spix, (Peter, 1824) 1872) LC X X DendropsophusRhinella henseli minutus(Lutz, 1934) (Peters, 1872) LC X DendropsophusRhinella hoogmoedi nanus Caramaschi (Boulenger, & 1889)Pombal, 2006 LC X DendropsophusRhinella icterica werneri (Spix, 1824) (Cochran, 1952) LC X DendropsophusRhinella ornata (Spix,sanborni 1824) (Schmidt, 1944) LC X X RhinellaItapotihyla schneideri langsdorffii (Werner, (Duméril 1894) & Bibron, 1841) LC X OlolygonFamily Centrolenidae albicans (Bokermann, 1967) LC X OlolygonVitreorana arduous eurygnatha Peixoto, (Lutz, 2002 1925) DD LC X X OlolygonVitreorana argyreornata uranoscopa (Miranda-Ribeiro,(Müller, 1924) 1926) LC X OlolygonFamily Craugastoridae brieni (Fouquete & Pyburn, 1972) LC X OlolygonEuparkerella catharinae cochranae (Boulenger, Izecksohn, 1888 1988) LC X X OlolygonHaddadus flavoguttata binotatus (Spix, (Lutz 1824) & Lutz, 1939) LC X X OlolygonFamily Cycloramphidae littoralis (Pombal & Gordo, 1991) LC X OlolygonCycloramphus perpusilla acangatan (Lutz Verdade& Lutz, 1939)& Rodrigues, 2003 VU LC X Ololygon v-signatus (Lutz, 1968) LC X Scinax fuscovarius (Lutz, 1925) LC X Scinax granulatus (Peters, 1871) LC X Scinax hayii (Barbour, 1909) LC X 4 Trachycephalus mesophaeus (Hensel, 1867) LC X Family Crossodactylus caramaschii Bastos & Pombal, 1995 LC X Crossodactylus gaudichaudii Duméril and Bibron, 1841 LC X Hylodes asper (Müller, 1924) LC X X Hylodes cardosoi (Lingnau, Canedo & Pombal, 2008) LC X Hylodes heyeri Haddad, Pombal & Bastos, 1996 DD X Hylodes meridionalis (Mertens, 1927) LC X Hylodes pipilans Canedo & Pombal, 2007 DD X X (Baumann, 1912) LC X Family Adenomera bokermanni (Heyer, 1973) LC X Adenomera marmorata (Steindachner, 1867) LC X Adenomera nana Müller, 1922 LC X Leptodactylus fuscus (Schneider, 1799) LC X Leptodactylus labyrinthicus (Spix, 1824) LC X Leptodactylus latrans (Steffen, 1815) LC X Leptodactylus mystacinus (Burmeister, 1861) LC X Leptodactylus notoaktites Heyer, 1978 LC X X Leptodactylus podicipinus (Cope, 1862) LC X Physalaemus cuvieri Fitzinger, 1826 LC X Physalaemus nanus (Boulenger, 1888) LC X Physalaemus signifer (Girard, 1853) LC X

558 Felipe Siqueira Campos & Ricardo Lourenço-de-Moraes

Table 1. Continued.

Sampled sites Altitude Species Red list Category 5 1 2 3 4 5 6 <300m >700m Family BrachycephalidaeMicrohylidae BrachycephalusMyersiella microps ephippium (Duméril (Spix, & Bibron, 1824) 1841) LC X IschnocnemaFamily erythromera (Heyer, 1984) DD X IschnocnemaMacrogenioglottus aff guentheri alipioi Carvalho,(Steindachner, 1946 1864) LC X X IschnocnemaProceratophrys henselii appendiculata (Peters, 1872) (Günther, 1873) LC X X IschnocnemaProceratophrys oea boiei (Heyer, (Wied-Neuwied, 1984) 1825) NTLC X X IschnocnemaFamily Phyllomedusidae parva (Girard, 1853) LC X FamilyPhyllomedusa Bufonidae burmeisteri Boulenger, 1882 LC X DendrophryniscusPhyllomedusa distincta brevipollicatus Lutz, 1950 Jiménez de la Espada, 1870 LC X DendrophryniscusPhyllomedusa rohdei leucomystax Mertens, 1926 Izecksohn, 1968 LC X RhinellaTotal abei (Baldissera-Jr, Caramaschi & Haddad, 2004) 23 31 29 34 25 29 LC - 78 X 40 X 1 Rhinella crucifer (Wied-Neuwied, 1821) X Rhinella granulosa (Spix, 1824) LC X X 2 Rhinella henseli (Lutz, 1934) LC X Rhinella hoogmoedi Caramaschi & Pombal, 2006 LC X 3 environmentalRhinella icterica managers (Spix, 1824) and policy-makers (e.g., temperatures in the future LC (Lourenço-de-Moraes, X 2016). Haddad,4 Rhinella 2008; ornataTrindade-Filho (Spix, 1824) et al., 2012, Morais et Therefore, we recommend LC that the Xdesign Xof amphibian al., 2013).Rhinella schneideri (Werner, 1894) conservation plans in LC this region X must attempt to 5 The currentFamily forest Centrolenidae remnants from the Serra do Mar are incorporate ecological connectivity assessments in the Vitreorana eurygnatha (Lutz, 1925) LC X considered as key conservation sites within the Brazilian remaining fragments of both lowlands and highlands Vitreorana uranoscopa (Müller, 1924) LC X Atlantic ForestFamily Craugastoridaehotspot, which reveal a high congruence areas. This may represent an alternative mechanism of ecologicalEuparkerella and cochranae evolutionary Izecksohn, patterns 1988 of amphibian to mitigate potential impacts LC related to X the Atlantic biodiversityHaddadus (Campos binotatus (Spix, et al.,1824) 2017). Our findings Forest amphibians. In LCthis context, X future X researches highlightedFamily valuable Cycloramphidae occurrence data regarding the should address ways to improve or implement these anuran speciesCycloramphus in one acangatan of the mostVerdade species-rich & Rodrigues, 2003 regions on conservation practices. VUIn line with X our findings, some Earth. According to Vasconcelos et al. (2014), the Serra other studies in the Atlantic Forest have also warned do Mar between São Paulo and states about the need to invest in amphibian conservation near comprise a high richness of small-ranged species and is high altitude areas (Carnaval et al., 2009; Lemes and classified as a distinct biogeographic domain for anurans. Loyola, 2013; Dias et al., 2014; Loyola et al., 2014), Rödder et al. (2007) also highlighted the portion of Serra which retain high humidity provided by well-preserved do Mar from the Espírito Santo state with extraordinary forest cover. Although the strength of this study heavily amphibian species richness. Antecedent biogeoclimatic relies on good studies on amphibian conservation in the factors as the refuges of the late Pleistocene may have Serra do Mar, our results highlight the importance of an important role in this current species richness pattern maintaining forest remnants in an attempt to provide a (Carnaval et al., 2009). However, processes determining straightforward representation of the amphibian species anuran occurrence in specific environments, such as that occur in this region. highland areas remain poorly known, where information on the diversity of amphibians remains fragmented Acknowledgements. We thank Rodrigo B. Ferreira and Gabriela (Garey et al., 2014; Garey and Provete, 2016). Due to Bittencourt-Silva for the useful comments on the manuscript, and the difficulty of access, the highland areas of Serra do Leire Rincón for the English review. We thank the COTEC/SP, Mar have historically suffered little interference from IAP/PR and Chico Mendes Institute for the logistical support anthropogenic activities compared to lowland areas and sampling permits (ICMBio 30344, 44755). We are grateful (Garey and Provete, 2016), which hampered the human to the “Museu de Biologia Prof. Mello Leitão” and the “Parque occupation and helped to preserve the amphibian species Ecológico Spitzkopf” for the fieldwork support. We also thank Rafael Rosa for help during the fieldwork in the “Parque Estadual that occur in these regions. da Serra do Mar Núcleo Caraguatatuba”, as well as Paulo R. Melo- The establishment of conservation efforts along Sampaio and Leandro O. Drummond in the “Parque Nacional the current forest remnants in the Serra do Mar can da Serra dos Órgãos”. This study was supported by CAPES ensure the amphibian species persistence in the Foundation (99999.001180/2013-04) and CNPq (140710/2013-2, mountainous regions, which probably will keep lower 152303/2016-2). Anurans from the mountain chain Serra do Mar, Brazil 559

References forced dispersal and uncertainties in spatial conservation planning. PloS One 8: e54323. Almeida, F.F.M., Carneiro, C.D.R. (1998): Origem e evolução da Lomolino, M.V. (2004): Conservation biogeography – Introduction. Serra do Mar. Revista Brasileira de Geociências 28: 135–150. In: Frontiers of biogeography: New directions in the geography Becker, C.G., Fonseca, C.R., Haddad, C.F.B., Batista, R.F., Prado, of nature, p. 293–296. Lomolino, M.V., Heaney, L.R., Eds., P.I. (2007): Habitat split and the global decline of amphibians. Sunderland, USA. Sinauer Associates. Science 318: 1775–1777. Lourenço-de-Moraes, R., Lantyer-Silva, A.S.F., Toledo, L.F., Solé, Brown, J.H., Stevens, G.C., Kaufman, D.M. (1996): The geographic M. (2013): Tadpole, oophagy, advertisement call and geographic range: size, shape, boundaries, and internal structure. Annual distribution of Aparasphenodon arapapa Pimenta, Napoli and Review of Ecology and Systematics 27: 597–623. Haddad 2009 (Anura, Hylidae). ���������������������� 47: Campos, F.S., Brito, D., Sole, M. (2014): Diversity patterns, 575–579. research trends and mismatches of the investigative efforts to Lourenço-de-Moraes, R. (2016): Efeitos da altitude, longitude e amphibian conservation in Brazil. ���������������������������� latitude na composição histórica e ecológica dos anfíbios da de Ciências 86: 1873–1886. Floresta Atlântica brasileira. ����������������������������� Campos, F.S., Lourenço-de-Moraes, R., Llorente, G.A., Solé, M. University of Maringá, Maringá, Brazil. (2017).���������������������������������������������������� � Loyola, R.D., Lemes, P., Brum, F.T., Provete, D.B., Duarte, L.D. evolution. Science Advances 3: e1602929. (2014): Clade-specific consequences of climate change to Carnaval, A.C., Hickerson, M.J., Haddad, C.F.B., Rodrigues, M.T., amphibians in Atlantic Forest protected areas. �cography 37: Moritz, C. (2009): Stability Predicts Genetic Diversity in the 65–72. Brazilian Atlantic Forest Hotspot. Science 323: 785–789. Marques, O.A.V., Abe, A.S., Martins, M. (1998): Estudo Dias, I.R., Medeiros, T.T., Nova, M.F.V., Solé, M. (2014): diagnóstico da diversidade de répteis do Estado de São Paulo. Amphibians of Serra Bonita, southern Bahia: a new hotpoint In: Biodiversidade do Estado de São Paulo, Brasil: síntese do within Brazil’s Atlantic Forest hotspot. ZooKeys 449: 105–130. conhecimento ao final do século XX, p. 27–38. Castro, R.M.C., Ferreira, R.B., Beard, K.H., Crump, M.L. (2016): Breeding Guild Ed., São Paulo, Brazil, Editora Fapesp. Determines Distributions in Response to Edge Effects and Mittermeier, R.A., Turner, W.R., Larsen, F.W., Brooks, T.M., Habitat Conversion in the Brazil’s Atlantic Forest. PloS One 11: Gascon, C. (2011): Global biodiversity conservation: the critical e0156781. role of hotspots. In: Biodiversity hotspots: distribution and Frost, D.R. (2017): Amphibian Species of the World: an Online protection of conservation priority areas, p. 2–22. ������������ Reference. Version 6.0. Avalaible at: http://research.amnh.org/ Habel J.C., Eds., Heidelberg, Germany, Springer. herpetology/amphibia/index.html. Accessed on 15 May 2017. MMA (2000): Avaliação e Ações Prioritárias para a Conservação Garey, M.V., Provete, D.B., Martins, I.A., Haddad, C.F.B., Rossa- da Biodiversidade da Mata Atlântica e Campos Sulinos. Feres, D.C. (2014): Anurans from the Serra da Bocaina National Conservation International do Brasil, Fundação SOS Mata Park and surrounding buffer area, southeastern Brazil. Check Atlântica, Fundação Biodiversitas, Instituto de Pesquisas List 10: 308–316. Ecológicas, Secretaria do Meio Ambiente do Estado de São Garey, M.V., Provete, D.B. (2016): Species composition, Paulo, SEMAD/Instituto Estadual de Florestas-MG. Brasília, conservation status, and sources of threat of anurans in mosaics Brazil, MMA/SBF. of highland of Southern and Southeastern Brazil. Morais, A.R., Siqueira, M.N., Lemes, P., Maciel, N.M., De Marco, Oecologia Australis 20: 94–108. P., Brito, D. (2013): Unraveling the conservation status of Data Haddad, C.F.B. (1998): Biodiversidade dos anfíbios no estado de Deficient species. Biological conservation 166: 98–102. São Paulo. In: Biodiversidade do estado de São Paulo, Brasil: Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., síntese do conhecimento ao final do século XX, p. 15–26. Powell, G.V.N., Underwood, E.C., D’Amico, J.A., Itoua, I., Joly, C.A., Bicudo, C.E.M., Eds., São Paulo, Brazil, Editora Strand, H.E., Morrison, J.C., Loucks, C.J., Allnutt, T.F., Ricketts, FAPESP. T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P., Haddad, C.F.B. (2008): Uma análise da lista brasileira de anfíbios Kassem, K.R. (2001): Terrestrial ecoregions of the world: a new ameaçados de extinção. In: Livro vermelho da fauna brasileira map of life on Earth. ���Science 51: 933–938. ameaçada de extinção, p. 286–325. Machado, A.B.M., Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J., Hirota, Drummond, G.M., Paglia, A.P., Eds., Brasília, Brazil, Ministério M.M. (2009): The Brazilian Atlantic Forest: How much is left, do Meio Ambiente. and how is the remaining forest distributed? ���������������� Haddad, C.F.B., Toledo, L.F., Prado, C.P.A., Loebmann, D., conservation. Biological Conservation 142: 1141–1153. Gasparini, J.L., Sazima, I. (2013): Guia dos anfíbios da Mata Rizzini, C.T. (1979): Tratado de Fitogeografia do Brasil: Aspectos Atlântica – diversidade e biologia. ������������������������� sociológicos e florísticos. São Paulo, Brazil, Editora Hucitec Books. Ltda., Editora da Universidade de São Paulo. Holt, R.D. (2003): On the evolutionary ecology of species’ ranges. Rödder, D., Teixeira, R.L., Ferreira, R.B., Dantas, R.B., Pertel, W., Evolutionary Ecology Research 5: 159–178. Guarneire, G.J. (2007): Anuran hotspots: the municipality of IUCN (2017): The IUCN Red List of Threatened Species. Version Santa Teresa, southeastern Brazil. ���������� 43: 91–110. 2017-1. Available at: http://www.iucnredlist.org. Accessed on Silva, J.M.C., Casteleti, C.H.M. (2003): Status of the biodiversity 12 May 2017. of the Atlantic Forest of Brazil. In: The Atlantic Forest of South Lemes, P., Loyola R.D. (2013): Accommodating species climate- America: biodiversity status, threats, and outlook, p. 43–59. 560 Felipe Siqueira Campos & Ricardo Lourenço-de-Moraes

Galindo-Leal, C., Câmara, I.G., Eds., Washington, USA, CABS, Vasconcelos, T.S., Prado, V.H., Silva, F.R., Haddad, C.F.B. (2014): Island Press. Biogeographic distribution patterns and their correlates in the Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, diverse frog fauna of the Atlantic Forest hotspot. PLoS One 9: A.S.L., Fischman, D.L., Waller, R.W. (2004): Status and trends e104130. of amphibian declines and extinctions worldwide. �cience 306: Verdade, V.K., Valdujo, P.H., Carnaval, A.C., Schiesari, L., 1783–1786. Toledo, L.F., Mott, T., Andrade, G.V., Eterovick, P.C., Menin, Tabarelli, M., Pinto, L.P., Silva, J.M.C., Hirota, M., Bede, L. (2005): M., Pimenta, B.V.S., Nogueira, C., Lisboa, C.S., Paula, C.D., Challenges and opportunities for biodiversity conservation in the Silvano, D.L. (2012): A leap further: the Brazilian Amphibian Brazilian Atlantic Forest. Conservation Biology 19: 695–700. Conservation Action Plan. Alytes 29: 27–42. Teixeira, A.M.G., Soares, B.S., Freitas, S.R., Metzger, J.P. (2009): Walsh, R.P.D. (1996): The climate. In: The tropical rain forest: an Modeling landscape dynamics in an Atlantic region: ecological study, p. 159– 205. Richards, P.W., Ed., Cambridge, Implications for conservation. Forest Ecology and Management UK, Cambridge University Press. 257: 1219–1230. Toledo, L.F., Batista, R.F. (2012): Integrative study of Brazilian anurans: geographic distribution, size, environment, , and conservation. Biotropica 44:785–792. Trindade-Filho, J., Carvalho, R.A., Brito, D., Loyola, R.D. (2012): How does the inclusion of Data Deficient species change conservation priorities for amphibians in the Atlantic Forest? Biodiversity and Conservation 21: 2709–2718.

Accepted by Gabriela Bittencourt-Silva