Oecologia Australis 20(2): 247-258, 2016 10.4257/oeco.2016.2002.08
ANURAN FAUNA OF THE HIGH-ELEVATION AREAS OF THE PARQUE NACIONAL DA SERRA DOS ÓRGÃOS (PARNASO), SOUTHEASTERN BRAZIL
Manuella Folly 1,*, Andressa de M. Bezerra 1, Joice Ruggeri 1, Fábio Hepp 2, Ana M. P. Telles de Carvalho-e-Silva 3, Marcia dos R. Gomes 1 & Sergio P. de Carvalho-e-Silva 1
1Universidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Zoologia, Laboratório de Anfíbios e Répteis, Ilha do Fundão, Rio de Janeiro, RJ, Brazil. CEP 21941-590. 2Universidade Federal do Rio de Janeiro, Departamento de Vertebrados, Setor de Herpetologia, Museu Nacional, Rio de Janeiro, RJ, Brazil. CEP 20940-040. 3Universidade Federal do Estado do Rio de Janeiro, Instituto de Biociências, Departamento de Zoologia, Laboratório de Biossistemática de Anfíbios, Urca, Rio de Janeiro, RJ, Brazil. CEP 22290-240. E-mails: [email protected]; [email protected]; [email protected]; [email protected]; [email protected]; [email protected]; [email protected].
ABSTRACT There is a lack of knowledge regarding the diversity of anurans in high-elevation areas of the Brazilian Atlantic Forest. In order to improve the knowledge about the diversity of this group in this kind of environment, we pres- ent a list of anuran amphibians recorded in high-elevation areas (above 1,200 m) of the Parque Nacional da Serra dos Órgãos (PARNASO), in southeastern Brazil. The list was compiled based on primary data (from fieldwork) and on secondary data (from surveys of institutional collections). Twenty-eight species belonging to seven families were recorded: Brachycephalidae (6 species), Bufonidae (3 spp.), Cycloramphidae (4 spp.), Hemiphractidae (5 spp.), Hylidae (8 spp.), Hylodidae (1 sp.), and Odontophrynidae (1 sp.). According to the IUCN Red List, eight of those species are classified as “Data Deficient” and two species have not been assessed yeti.e ( ., Dendrophryniscus organensis and Fritziana sp. nov.). Ten species are classified as “Least Concern” but with populations in decline, although six of them (Bokermannohyla carvalhoi, B. circumdata, Ischnocnema parva, Proceratophrys appendiculata, Scinax albicans and Zachaenus parvulus) were frequently found during fieldwork at PARNASO and seem to be locally abundant. The other eight species classified as “Least Concern” have stable populations. We add three species to the list of anurans endemic to the high-elevation areas of Serra dos Órgãos (Cycloramphus organensis, D. organensis, and Fritziana sp. nov.), raising to 14 the number of endemic taxa in the area. Keywords: Anura; Atlantic Forest; altitude; survey.
INTRODUCTION southeastern Brazil (Eterovick et al. 2005). Only a small portion of what currently remains of the The Brazilian anuran fauna is currently Atlantic Forest is known to occur within legally represented by 1,026 species, corresponding to protected areas (Laurance 2009, Lemes et al 2014). 16% of the global anuran diversity (Segalla et The Atlantic Forest biome encompasses the al. 2014, Frost 2016). The Brazilian Atlantic vegetation that occurs along the Brazilian coast Forest (sensu Ab’Saber 1977) has been labeled as (extending some distance inland), from the state of one of the 34 biodiversity hotspots in the world Rio Grande do Norte to the state of Rio Grande do (Mittermeier et al. 2011), harboring about 430 Sul (Delabie et al. 2000). The vegetation mainly species of anurans, of which 80% are endemic consists of dense ombrophilous forest, mixed to that biome (Cruz & Feio 2007, Lemes et al. ombrophilous forest and seasonal forests, including 2014). Nevertheless, due to anthropogenic action, associated ecosystems, such as mangroves and salt the Atlantic Forest is nowadays composed by only marshes (Veloso 1992, Joly et al. 1999). It also 12% of its original area (Ribeiro et al. 2009, SOS encompasses areas of high-elevation, including Mata Atlântica 2014), and most of the remnant the montane grasslands called campos de altitude patches are found in the mountains of the Serra (Safford 1999).Campos de altitude are composed do Mar and Serra da Mantiqueira ranges in by open vegetation habitats present above 1,900 248 Anuran from High-elevation Area PARNASO m of altitude in the Serra do Mar and Serra da Hamer & McDonnel 2008, Laurance 2008). In the Mantiqueira ranges that are relatively poorly Atlantic Forest, some amphibian populations that studied (Safford 1999). There are few studies so were once abundant have decreased dramatically, far conducted in this ecosystem, focusing mainly mainly in the regions of Serra do Mar and Serra da on plants (Safford 1999), birds (Mallet-Rodrigues Mantiqueira (Heyer et al. 1988, Weygoldt 1989). et al. 2010, Vasconcelos & Rodrigues 2010) and Experimental studies, monitoring and mammals (Geise et al. 2004). inventories are useful in reporting amphibian Currently, there are a few studies comprising declines (Biek et al. 2002). It is also important to the amphibian composition in areas above 1200 m conduct studies that provide support for amphibian a.s.l. in the Atlantic Forest. Most studies about the conservation, especially in areas without previous anuran fauna from highlands consist of descriptions knowledge of the local anuran fauna (Rocha et al. of new species (e.g., Pombal et al. 1998, Alves et 2003, Diniz-Filho et al. 2004). Therefore, here al. 2006, Weber et al. 2011). Nevertheless, Cruz & we present a list of anuran species recorded in Feio (2007) reviewed the diversity and endemism high-elevation areas (above 1,200 m a.s.l.) within of anuran species from “mountain areas” of Serra the PARNASO, in the Serra dos Órgãos mountain do Mar and Serra da Mantiqueira, and Siqueira range. et al. (2011) surveyed the anuran species present in two high-altitude sites in the Serra dos Órgãos MATERIAL AND METHODS region, inserted in the Serra do Mar of state of Rio de Janeiro. Study area The Parque Nacional da Serra dos Órgãos (PARNASO) is inserted in the Atlantic Forest The Serra do Mar mountain range complex biome and contains some of the highest peaks of is located at the Atlantic Forests morphoclimatic the Serra dos Órgãos mountain range, such as Pedra domain (Ab’Saber 1977) of the coast of the do Açu (2,245 m a.s.l.) and Pedra do Sino (2,275 states of Santa Catarina, Paraná, São Paulo and m a.s.l.; ICMBIO 2008). Relatively little is known Rio de Janeiro (Cruz & Feio 2007). The Parque about the ecology, biogeography, or developmental Nacional da Serra dos Órgãos (PARNASO) history of these “sky island” formations (Safford is a national park located in the mountains of 1999). PARNASO has a high diversity of habitats, the Serra dos Órgãos range in the central part which in turn promotes a high diversity of animal of the Serra do Mar complex, in the state of species (ICMBIO 2008). It harbors a great part Rio de Janeiro. This conservation area (The of the overall diversity and endemic species of headquarter of Teresópolis is at 22°24’ and 22°32’ the Atlantic Forest, including around 100 species S; 42°69’ and 43°06’ W) encompasses part of the of anuran amphibians (ICMBIO 2008). It also municipalities of Teresópolis, Petrópolis, Magé and represents the type locality for at least 20 species Guapimirim, totaling an area of 20,024 ha of dense of anurans, of which seven are endemic of this ombrophilous forest and highland forest. High- mountainous massif (Carvalho-e-Silva et al. in elevation areas (above 1,200 m a.s.l.) are present prep.). The Serra dos Órgãos was identified by the only in Teresópolis and Petrópolis (ICMBIO 2008; ministry of the environment as an area of extreme Figure 1), representing around 60% of the park’s biological importance (Cronemberg & Viveiros area (Cronemberg & Viveiros de Castro 2007). de Castro 2007). The PARNASO thus protects an PARNASO has an average annual temperature of important part of the Atlantic Forest’s biodiversity. 19°C, and rainfall varies between 1,500 mm and Worldwide amphibian declines have 3,000 mm per year (ICMBIO 2008). been reported and several factors are suggested Fieldwork was conducted in high-elevation to be responsible for it, such as habitat loss and areas along the Pedra do Sino trail, municipality fragmentation; contamination of water and soil of Teresópolis. The altitudinal range chosen for by chemical pollutants; climate change; and sampling in the present work (1,200 – 2,250 m introductions of exotic species (Blaustein et al. a.s.l.) was based on the altitudinal range of the 1994, Alford & Richards 1999, Lips et al. 2005, Pedra do Sino trail, which starts at 1,200 m a.s.l.
Oecol. Aust., 20(2): 247-258, 2016 Folly et al. 249
Figure 1. Locality where the majority of the fieldwork was conducted (white star; Pedra do Sino trail, Teresópolis, state of Rio de Janeiro, Brazil). and ends near the mountain’s peak at 2,250 m a.s.l. in mist. Shrubs and small trees between 5 m and (Cronemberg & Viveiros de Castro 2007). 10 m in height dominate the vegetation. Trees The area presents altitudinal variation of typically have crooked trunks covered by moss the vegetation and soil characteristics. Therefore, and epiphytes. we used the altitudinal classification found in • Campos de altitude (Figure 2B) – above 1,900 Mallet-Rodrigues et al. (2010), and present a quick m a.s.l.: dominated by shrubby and herbaceous description based on the management planning for vegetation that grows among rocky outcrops. PARNASO (ICMBIO 2008): There is low input of organic matter and the vegetation is more xeric-adapted. The soil is • Montane Forest (“Floresta Montana”) – from shallow and solar radiation is intense. In areas 500 m to 1,500 m a.s.l.: formation with extensive with steep slopes and greater exposure to vegetation stratification. Its structure varies wind and rain, the rock is bare with almost no according to the specific conditions of each area. vegetation coverage. Large trees reaching up to 40 m high dominate the tree layer and there are deep soils of composite Sampling crystalline rocks. • High Montane Forest (“Floresta Pluvial Alto- From 2009 to 2013, we conducted six Montana”; Figure 2A) – from 1,500 m to 1,900 m surveys in the area (one or two per year) during a.s.l.: it is a typical humid forest, often enveloped both the rainy and dry seasons, totaling 15
Figure 2. Sampling sites: (A) High Montane Forest; (B) Campos de altitude; (C) Pitfall trap system set in campos de altitude.
Oecol. Aust., 20(2): 247-258, 2016 250 Anuran from High-elevation Area PARNASO sampling days. We used three complementary RESULTS methods for sampling adult anurans: active search, acoustic search, and pitfall traps (see Calleffo We report twenty-eight anuran species 2002); and one method for sampling tadpoles: from high-elevation areas of PARNASO, active search. belonging to seven families (Table 1 and Figure We performed the active and acoustic 3): Brachycephalidae (6 species), Bufonidae (3 searches randomly along the Pedra do Sino trail. spp.), Cycloramphidae (4 spp.), Hemiphractidae In addition, four Y and I-shaped pitfall traps (5 spp.), Hylidae (8 spp.), Hylodidae (1 sp.), and (consisting of 60 L buckets five meters far apart, Odontophrynidae (1 sp.). Fourteen of these species with drift fences) were set in campos de altitude were sampled during the field expeditions (2009- at Pedra do Sino: the first three were located in 2013). different sites close to the “Pedra da Baleia” Dendrophryniscus cf. brevipollicatus (22°27’37.0”S / 43°01’40.0”W; 2,131 m a.s.l) with (ZUFRJ: 11275 – 11276) and Ischnocnema cf. five, seven, and eight buckets, respectively; the last nasuta (ZUFRJ: 9661) could not be identified one, with four buckets, was located in the “Vale das at the specific level due to the morphological Orquídeas” (22°27’26.5”S / 43°01’10.4” W; 1,975 differences observed in the recorded specimens m a.s.l) (Figure 2C). The pitfall traps remained compared to the known and described species of open during the survey period (between two and each genus, even though the former is very similar four days) and were checked daily. For the capture to D. brevipollicatus and the latter is very similar of tadpoles in the streams and in the bromeliads we to I. nasuta. used hand sieves and an entomological aspirator, Ischnocnema aff.guentheri is supposed to be respectively. a new species according to Gehara et al. (2013); Adults and tadpoles were collected and these authors restrict the name Ischnocnema photographed. Adults were anesthetized and killed guentheri to only one population in the municipality with lidocaine injection (with insulin syringe of Rio de Janeiro, Brazil. Therefore, any other needles) and tadpoles were immersed in a solution population previously associated with this species of lidocaine as specified in the Brazilian laws name, as the others populations in the state of (Diretriz Brasileira para o Cuidado e a Utilização Rio de Janeiro and the states of Santa Catarina, de Animais para Fins Científicos e Didáticos Paraná, São Paulo, Minas Gerais are actually four – Concea). Specimens were deposited at the undescribed species. Amphibian Collection of the Departamento de Zoologia, Universidade Federal do Rio de Janeiro DISCUSSION (ZUFRJ) according to authorization (18155) provided by ICMBIO The highest species richness was observed We obtained additional data from the at 1,200–1,500 m with 26 species, of which 13 zoological collections of the Universidade Federal were exclusive to that altitudinal range (Table 1). do Estado do Rio de Janeiro (Coleção de Anfíbios Between 1,501–1,900 m we observed 14 species, da Universidade Federal do Estado do Rio de of which none were exclusive to that range. Above Janeiro – UNIRIO), Universidade Federal Rural 1,900 m we observed seven species of which only do Rio de Janeiro (Coleção Eugenio Izecksohn – one was exclusive to that elevation (Figure 4). EI), and Universidade Federal do Rio de Janeiro Species richness decreased with elevation above (ZUFRJ), which encompass more than 20 years 1,500 m a.s.l. This pattern, known as a “diversity of fieldwork in the area. We only included in our bulge” has been described by Grytnes & Vetaas inventory specimens from PARNASO that have (2002). The species richness found was inversely been sampled within the altitudinal range used in proportional to the altitudinal increase. This result the present work (1,200 – 2,250 m a.s.l.). The list may be due to the type of vegetation found at of examined specimens is given in Appendix 1. the lower altitudes (montane forest), as the taller Taxonomic nomenclature used throughout the text and more closed tree canopy in those sites would follows Frost (2016). not only provide shelter to different species of
Oecol. Aust., 20(2): 247-258, 2016 Folly et al. 251 M CA MF MF MF Continue... HMF, CA HMF, MF, HMF MF, MF, HMF MF, HMF MF, HMF MF, Vegetation MF, HMF, CA HMF, MF, MF, HMF, CA HMF, MF, MF, HMF, CA HMF, MF, . 2011, Frost 2016). . 2011, The altitudinal ranges of Weber et al Weber Pitfall Visual Visual, Visual, method Sampling Acoustic, Pitfall Visual, Acoustic Visual, Visual, Acoustic Visual, Visual, Acoustic, Visual, floor Shrubs Leaf-litter Leaf-litter Leaf-litter Leaf-litter Leaf-litter Leaf-litter Preferred vegetation Campos de Bromeliads Bromeliads Forest floor Forest floor Herbaceous altitude microhabitats X X X X X >1,900 (PARNASO), their status of conservation according to the International (PARNASO), Órgãos X X X X X X X X 1900 1501– X X X X X X X X X X X 1500 1200– Altitudinal range (m a.s.l.) . (2010) and (ICMBIO 2008): Montane Forest (MF), High (HMF) campos de altitude Status LC – St LC – St LC –Dc LC – Dc LC – Dc DD – Dc in IUCN DD – Un DD – Un DD – Un et al (Miranda- (Spix, 1824) * (Noble, 1924) Taxa (Lutz, 1974) (Cochran, 1948)* (Spix, 1824)* Bufonidae cf . brevipollicatus Dendrophryniscus Carvalho-e-Silva, organensis Dendrophryniscus Mongin, Izecksohn & Carvalho-e-Silva, 2010 Rhinella icterica Cycloramphidae Cycloramphus eleutherodactylus Ribeiro, 1920) Weber, Verdade, Verdade, Weber, Cycloramphus organensis Salles, Fouquet, & Carvalho-e-Silva, 2011 Cycloramphus stejnegeri Ischnocnema cf. nasuta Ischnocnema parva (Girard, 1853) * Zachaenus parvulus (Girard, 1853)* Ischnocnema aff. guentheri Ischnocnema gualteri Ischnocnema holti Brachycephalidae Brachycephalus ephippium (CA). IUCN status categories are: Least Concern (LC); Data Deficient (DD); Stable population (St); Declining population (Dc); Unknown status (Un); * Data collected in collected (Dc); Unknown status (Un); * Data population (St); Declining population (DD); Stable Deficient Data (LC); Concern Least are: (CA). IUCN status categories the fieldwork. Table 1. List of anurans from high-elevation areas the Parque Nacional da Serra dos Table Vegetation was classified according to Mallet-Rodrigues Vegetation Union for Conservation of Nature and Natural Resources (IUCN), altitudinal ranges (meters above sea level – m a.s.l.) within the study area. each species are categorized according to our records from fieldwork, zoological collections and literature data (Duellman & Gray 1983,
Oecol. Aust., 20(2): 247-258, 2016 252 Anuran from High-elevation Area PARNASO MF MF MF MF MF MF MF MF MF MF, HMF MF, MF, HMF MF, MF, HMF MF, Vegetation MF, HMF, CA HMF, MF, MF, HMF, CA HMF, MF, Visual Visual Visual method Sampling Visual, Acoustic Visual, Visual, Acoustic Visual, Acoustic Visual, Visual, Acoustic Visual, Visual, Acoustic Visual, Visual, Acoustic Visual, stream stream stream stream stream stream stream Shrubs streams Streams Bamboo Leaf-litter Preferred Rocks near Bromeliads Bromeliads microhabitats Vegetation near Vegetation Vegetation near Vegetation Vegetation near Vegetation near Vegetation Vegetation near Vegetation near Vegetation near Vegetation X X >1,900 X X X X X 1900 1501– X X X X X X X X X X X X X X 1500 1200– Altitudinal range (m a.s.l.) Status LC – St LC – St LC – St LC – Dc LC – Dc LC – Dc LC – Dc LC – Dc LC – Dc DD – Dc DD – Dc in IUCN DD – Un DD – Un (Günther, 1873)* (Günther, (Peixoto, 1981)* (Lutz, 1973) Taxa (Cruz & Peixoto, 1987)* Miranda-Ribeiro, 1920* (Lutz, 1924) (Bokermann, 1967) Hylodidae Hylodes charadranaetes Heyer & Cocroft, 1986 Odontophrynidae appendiculata Proceratophrys Phasmahyla guttata Scinax obtriangulatus Scinax albicans Hylidae Aplastodiscus arildae Aplastodiscus flumineus (Cruz & Peixoto, 1985)* Aplastodiscus musicus (Lutz, 1949) Bokermannohyla carvalhoi (Cope, 1871)* Bokermannohyla circumdata Gastrotheca ernestoi Gastrotheca (Wandolleck, 1907)* Fritziana ohausi (Wandolleck, Fritziana sp. nov.* Hemiphractidae Fritziana fissilis (Miranda-Ribeiro, 1920)* ...Continued
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Figure 3. Anuran specimens from high-elevation areas of PARNASO, RJ, Brazil; A) Ischnocnema holti; B) Brachycephalus ephippium; C) Zachaenus parvulus; D) Proceratophrys appendiculata; E) Cycloramphus eleutherodactylus; F) C. organensis; G) Dendrophryniscus organensis; H) Fritziana sp. nov.; I-J) Gastrotheca ernestoi; K) Aplastodiscus musicus; L) A. flumineus; M) A. arildae; N) Bokermannohyla circumdata; O) B. carvalhoi. Photos A and H by Felipe Quintarelli Machado; Photo C by Daniel de Góes; Photo G by Cyro de Luna-Dias; All other photos by Sergio Potsch de Carvalho-e-Silva.
Oecol. Aust., 20(2): 247-258, 2016 254 Anuran from High-elevation Area PARNASO treefrogs but also keep the leaf-litter layer humid assemblages in PARNASO and PETP may be due to and deep along the forest floor, where the anuran them being located within the same mountain range fauna is abundant (Rocha et al. 2004). On the other and connected by a continuous habitat corridor and hand, the difficulty in accessing higher elevation having similar environmental influences. Despite sites, such as campos de altitude, and the limited the similarities found in the high-elevation areas of knowledge about the fauna found in this ecosystem both sites, several species are apparently exclusive may have influenced the sample size, showing the to one of the two localities: PETP (21 species) and necessity of continuing to do fieldwork in these PARNASO (14 species). high-elevation areas. Siqueira et al. (2011) removed two species Seven endemic species were previously [Gastrotheca albolineata (Lutz & Lutz 1939) and reported for the altitudinal region in the Serra dos Hylodes charadranaetes] from the previous list of Órgãos Mountains (Cruz & Feio 2007, Weber et amphibians endemic to the high-elevation areas al. 2011) and were also recorded for the high- of the Serra dos Órgãos compiled by Cruz & Feio elevation areas at the present study: Aplastodiscus (2007), and added two species (Holoaden pholeter flumineus, A. musicus, Bokermannohyla carvalhoi, Pombal, Siqueira, Dorigo, Vrcibradic & Rocha, Cycloramphus organensis, C. stejnegeri, Hylodes 2008 and Brachycephalus garbeanus Miranda- charadranaetes and Ischnocnema gualteri. We Ribeiro 1920), maintaining the list with currently also recorded 14 species that have been reported 11 species. We add three more species to the list: for high-elevation areas within the Parque Cycloramphus organensis, Dendrophryniscus Estadual dos Três Picos (PEPT) (Siqueira et al. organensis, and Fritziana sp. nov., raising to 2011): Aplastodiscus arildae, Bokermannohyla 14 the number of amphibian species considered carvalhoi, B. circumdata, Dendrophryniscus cf. endemic of high-elevation areas in the Serra dos brevipollicatus, Fritziana fissilis, Gastrotheca Órgãos region. ernestoi, Hylodes charadranaetes, Ischnocnema Lemes et al. (2014) predict a decline of aff. guentheri, I. holti, I. parva, Rhinella icterica, anuran species richness within protected areas Scinax albicans, S. obtriangulatus and Zachaenus in the Atlantic Forest under the change climate parvulus. The similarity of the anuran fauna conditions by the year 2050. Additionally, the
Figure 4. Species richness observed at three different ranges: 1,200–1,500 m; 1,501–1,900 m and above 1,500 m a.s.l. On left the number of species, on right the number of endemic species for each range. Note species richness decreasing proportionally to elevation.
Oecol. Aust., 20(2): 247-258, 2016 Folly et al. 255 ranges of some of these species are predicted to improve the knowledge about this important to shift toward higher elevations, where a large ecosystem. number of endemic Atlantic Forest species already Among the ten species classified as “Least occur. Based on these predictions, Lemes et al. Concern”, six (Bokermanohyla carvalhoi, B. (2014) suggested that new protected areas in higher circumdata, I. parva, P. appendiculata, S. albicans altitudes would be more effective in alleviating and Z. parvulus) are found in relatively high the effect of climate change on this endangered abundance at PARNASO, even though they are fauna. In this predicted scenario, mountainous declining globally (IUCN 2015; Table 1). In regions would become a refuge for amphibians. addition, eight species are classified as “Data The risk of the declining populations and the high Deficient” (IUCN 2015). Despite the continuous levels of endemism observed at high-elevation fieldwork in the area, the species Aplastodiscus areas highlight the importance of preserving these flumineus and A. musicus, both reported in this habitats. study, have not been recorded at PARNASO since Cycloramphus organensis is endemic to 2003 and 1995, respectively. All these facts, in the high-elevation areas (Weber et al. 2011). In addition to the diversity and endemism found in addition, a new species, Fritziana sp. nov., is the high-elevation areas of the park, highlight the being described from the high-elevation areas of importance of PARNASO for the conservation of the park (Folly et al. in prep.) and is so far also the Atlantic Forest anuran fauna. restricted to such habitats. Gastrotheca ernestoi and Ischnocnema holti are also probably restricted ACKNOWLEDGMENTS to high-elevation areas in PARNASO, despite not being endemic to the Serra dos Órgãos region We thank Cecilia Cronemberger de Faria and all employees of Parque Nacional da Serra dos Órgãos who contributed to the field trip logistics (Costa et al. 2008, Izecksohn & Carvalho-e-Silva for collecting of specimens and field data. We thank Dr. Oswaldo Luiz 2008, Siqueira et al. 2011). Peixoto for allowing access to the Coleção Eugenio Izecksohn. We thank Felipe Quintarelli Machado and Daniel de Goes for some of the photos The lack of research on the biology and and Kerry Cobb for reviewing the manuscript. Sergio Potsch de Carvalho- demography of tropical anuran faunas complicates e-Silva thanks CNPq for his research grant. The Instituto Chico Mendes de Conservação da Biodiversidade (ICMBIO) for providing authorization for the design of appropriate strategies for the scientific study, number: 18155. The project received grants from Fundação conservation of amphibians (Silvano & Segalla de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (process 2005). This deficiency is more evident regarding the E-26/112.137/2008). fauna of high-elevation areas where, historically, the rugged and mountainous terrain has hampered REFERENCES access (Kattan & Franco 2004). In addition, the anurans of those regions tend to have their Ab’Saber, A. N. 1977. Os domínios morfoclimáticos na América do reproductive activity limited to a few short periods Sul. Primeira aproximação. Geomorfologia, 52, 1–22. Alford, R. A., & Richards, S. J. 1999. Global amphibian declines: each year due to the severe cold weather, making a problem in applied ecology. Annual Review of Ecology it harder to find and record individuals during the and Systematics, 30, 133–165. DOI: 10.1146/annurev. cooler season. Moreover, some trapping methods ecolsys.30.1.133 such as pitfall traps, might be less efficient in Alves, A. C. R, Ribeiro, L. F., Haddad, C. F. B., & Reis, S. the campos de altitude as a consequence of the F. 2006. Two new species of Brachycephalus (Anura: rocky soil, which hampers their establishment on Brachycephalidae) from the Atlantic Forest in Paraná State, southern Brazil. Herpetologica, 62(2), 221–233. DOI: the ground. Only thirteen percent (13%) of the 10.1655/05-41.1 species were collected in the pitfall traps during Biek, R., Funk, W. C., Maxell, B.A., & Mills, L.S. 2002. What is field surveys; the other 87% of the species were missing in amphibian decline research: insights from ecological collected during visual and acoustic searches. Thus, sensitivity analysis. Conservation Biology, 16(3), 728–734. high sampling efforts and the usage of more than DOI: 10.1046/j.1523-1739.2002.00433.x one method are necessary for adequate sampling Blaustein, A. R., Wake, D. B., & Sousa, W. P. 1994. Amphibian declines: judging stability, persistence, and the studied area, mainly because of the different susceptibility of populations to local and global extinctions. microhabitats found at those sites. Yet, it is crucial Conservation Biology, 8(1), 60–71. DOI: 10.1046/j.1523- to conduct more studies in high-elevation areas 1739.1994.08010060.x
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Submitted: 29 November 2014 Accepted: 16 April 2016
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APPENDIX 1 4931 – 4933); Hemiphractidae: Fritziana fissilis (ZUFRJ: 9662-9663, 11717 – 11718), Fritziana Material examined. Brachycephalidae: goeldii (ZUFRJ: 8916), Fritziana ohausi (ZUFRJ: Brachycephalus ephippium (ZUFRJ: 11270 12154 – 12155), Fritziana sp. nov. (ZUFRJ: 11680 –11274, 11482-11484; UNIRIO: 2537, 3750), – 11681, 11726, 13978), Gastrotheca ernestoi Ischnocnema parva (ZUFRJ: 11097, 11098, (ZUFRJ: 13974; UNIRIO: 2534); Hylidae: 11281 –11283, 11720, 11721; UNIRIO: 10108, Aplastodiscus arildae (ZUFRJ: 11515; UNIRIO: 3346), Ischnocnema aff. guentheri (ZUFRJ: 4944, 1581, 1590, 1630, 1755), Aplastodiscus 11279, 11280, 13977), Ischnocnema gualteri flumineus (ZUFRJ: 6984 (tadpole); UNIRIO: 1589; (ZUFRJ: 12402), Ischnocnema holti (ZUFRJ9664 EI: 7328), Aplastodiscus musicus (ZUFRJ: 6213, – 9675, 11722-11725, 13975, 13976, 13979, 6345, EI: 7532, 7533; MNRJ: 3213 lectotype, 13992; UNIRIO: 4875), Ischnocnema cf. nasuta 3214 – 3219 paralectotypes), Bokermannohyla (ZUFRJ: 9661); Bufonidae: Dendrophryniscus carvalhoi (ZUFRJ: 10232, 11806, 11809 (tadpole), cf. brevipollicatus (ZUFRJ: 11275 – 11276), 11810; UNIRIO: 1105, 1106, 1136, 1503, 3363), Dendrophryniscus organensis (ZUFRJ: Bokermannohyla circumdata (ZUFRJ: 11265, 9794; UNIRIO: 4946, 2406, 2183) Rhinella 11811), Phasmahyla guttata (ZUFRJ: 6340, 12425; icterica (ZUFRJ: 11805), Cycloramphidae: UNIRIO: 2347), Scinax albicans (ZUFRJ: 11099 Cycloramphus stejnegeri (ZUFRJ: 12113 – – 11102, 12175), Scinax obtriangulatus (ZUFRJ: 12114), Cycloramphus eleutherodactylus (ZUFRJ: 2033), Hylodidae: Hylodes charadranaetes 12403), Cycloramphus organensis (ZUFRJ: (ZUFRJ: 12408 – 12409); Odontophrynidae: 10348 – 10354, 10471 – 10474); Zachaenus Proceratophrys appendiculata (ZUFRJ: 11719, parvulus (ZUFRJ: 14487-14488; UNIRIO: 4925, 12727 11807; UNIRIO: 4471, 4472, 4922).
Oecol. Aust., 20(2): 247-258, 2016