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Anuran Amphibians of a Protected Area in the Northern Atlantic Forest with Comments on Topotypic and Endangered Populations

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Anuran Amphibians of a Protected Area in the Northern Atlantic Forest with Comments on Topotypic and Endangered Populations Herpetology Notes, volume 13: 61-74 (2020) (published online on 03 February 2020) Anuran amphibians of a protected area in the northern Atlantic Forest with comments on topotypic and endangered populations Marcos Jorge Matias Dubeux1,2,*, Ubiratan Gonçalves1,2,3, Filipe Augusto Cavalcanti do Nascimento1,2, and Tamí Mott1,2 Abstract. Over 600 species of amphibians occur in the Atlantic Forest, 80% of which are endemic. Among the eight recognized biogeographic regions of the Atlantic Forest, the Pernambuco Biogeographic Sub-Region, north of the São Francisco River, has been the most deforested and least studied. Here we provide a list of anuran amphibians from the Environmental Protection Area of Catolé and Fernão Velho, state of Alagoas, Brazil, located in the northern Atlantic Forest. We provide habitat utilization data for all recorded species and discuss the conservation status of topotypic and endangered populations. Forty species of 20 genera and nine families of anurans were registered. Hylidae was the richest family with 19 species followed by Leptodactylidae with nine, Bufonidae with four, Microhylidae and Phyllomedusidae with two each, and Aromobatidae, Craugastoridae, Hemiphractidae and Odontophrynidae with one each. Three anuran species were originally described from this conservation unit (Chiasmocleis alagoana, Phyllodytes edelmoi and Ololygon skuki), four are threatened (Allobates olfersioides, Chiasmocleis alagoana, Hylomantis granulosa and Ololygon skuki) and two are Data Deficient for conservation assessment (Gastrotheca fissipes and Pithecopus nordestinus). This anuran species list should prove useful to decision makers when planning conservation strategies. Keywords. Amphibia, Conservation Unit, Inventory, Hotspot, Ololygon skuki. Resumo. Mais de 600 espécies de anfíbios ocorrem na Mata Atlântica, sendo 80% delas endêmicas. Dentre as oito regiões biogeográficas reconhecidas para essa área, a Sub-região Biogeográfica Pernambuco, ao norte do rio São Francisco, tem sido a mais desmatada e a menos estudada. Apresentamos aqui uma lista de anfíbios anuros da Área de Proteção Ambiental de Catolé e Fernão Velho, no estado de Alagoas, Brasil, localizado na região norte da Mata Atlântica. Fornecemos dados de utilização de habitat para todas as espécies registradas e discutimos o status de conservação das populações topotípicas e ameaçadas. Quarenta espécies de 20 gêneros e nove famílias de anuros foram registradas. Hylidae foi a família mais rica com 19 espécies seguida por Leptodactylidae com nove, Bufonidae com quatro, Microhylidae e Phyllomedusidae com duas cada, e Aromobatidae, Craugastoridae, Hemiphractidae e Odontophrynidae com uma espécie cada. Três espécies de anuros foram originalmente descritas a partir desta unidade de conservação (Chiasmocleis alagoana, Phyllodytes edelmoi e Ololygon skuki), quatro estão ameaçadas (Allobates olfersioides, Chiasmocleis alagoana, Hylomantis granulosa e Ololygon skuki) e duas apresentam dados deficientes para serem avaliadas quanto ao seu status de conservação (Gastrotheca fissipes e Pithecopus nordestinus). A presente lista de espécies de anuros poderá ser útil para tomadas de decisão no planejamento de estratégias de conservação. Palavras-chave. Amphibia, Unidade de Conservação, Inventário, Hotspot, Ololygon skuki. Introduction The Neotropical region has the greatest diversity 1 Universidade Federal de Alagoas, Instituto de Ciências of amphibians in the world, with more than 1,700 Biológicas e da Saúde, Campus A.C. Simão, CEP 57072-900 catalogued species (Vences and Kohler, 2008), Maceió, Alagoas, Brazil. 2 accounting for approximately 20% of the total global Universidade Federal de Alagoas, Museu de História Natural, CEP 57010-020 Maceió, Alagoas, Brazil. diversity known for this group (Frost, 2019). This 3 MANEFAU Consultoria e Serviços Ambientais LTDA – EPP, diversity is not evenly distributed, with the Atlantic CEP 57057-260 Maceió, Alagoas, Brazil. Forest ecoregion, a global hotspot of biological * Corresponding author. E-mail: diversity, having the highest diversity, endemicity and [email protected] 62 Marcos Jorge Matias Dubeux et al. number of threatened amphibian species (sensu Myers just a few isolated fragments (<100 km2) surrounded by et al., 2000; Silvano and Segalla, 2005; Verdade et al., areas of monoculture and pasture (Ribeiro et al., 2009). 2012). Among the 1,270 conservation units in the Atlantic The Atlantic Forest originally occupied a broad Forest, only 89 are in the Pernambuco BSR, and cover latitudinal area along the east coast of Brazil (3°– less than 3,624 km2, proportionately the BSR of the 31°S and 35°–60°W, Ribeiro et al., 2009). Due to Atlantic Forest with the lowest protected coverage in deforestation and urban expansion, this ecoregion is the country (CNUC/MMA, 2019). Preliminary studies now represented by only 28% of its original extension report that approximately 80 species of anurans occur in (Rezende et al., 2018). The wide latitudinal range and the Pernambuco BSR (MJMD, unpublished data), six of associated climatic variation (about 29º, including which are listed as endangered (ICMBio, 2018; IUCN, tropical and subtropical regions; Ribeiro et al., 2009); 2019). The diversity and conservation threat of Atlantic the longitudinal range, including a precipitation and Forest are certainly underestimated, and will only be humidity gradient from the coast to the mainland better understood with additional studies (Subirá et al., (Ribeiro et al., 2009; Haddad et al., 2013); and variation 2012). in vegetation composition (Pinto and Brito, 2003) and The purpose of this paper is to provide a list of anurans elevation (0–2,700 meters), have favored speciation known to occur in a protected area in the Pernambuco (Vasconcelos et al., 2014). In fact, more than 40% of BSR of the northern Atlantic Forest. Information on Neotropical amphibians occur in the Atlantic Forest, habitat use and the conservation status of topotypic and 80% of which are endemic (Rossa-Feres et al., 2017). endangered populations are provided. Among the eight recognized biogeographic regions of the Atlantic Forest, the Pernambuco Biogeographic Material and methods Sub-Region (Pernambuco BSR; sensu Ribeiro et al., The study was conducted in the Environmental 2009) north of the São Francisco River has been the Protection Area of Catolé and Fernão Velho (EPACFV), most deforested (only 12% of its original coverage a sustainable use conservation unit located in the state remains) and is considered the least studied (Ribeiro of Alagoas, northeastern Brazil (Fig. 1). The area et al., 2009). The Pernambuco BSR currently contains comprises approximately 37.12 km2 and includes a mosaic of phytophysiognomies including ombrophilous forest, mangrove, and the largest fragment of cerrado (savanna-like vegetation) of the BSR (Assis, 2000; Oliveira et al., 2014) with many streams, reservoirs and part of the Mundaú river course (Fig. 2). The climate is classified as tropical with dry summers; annual temperature and rainfall are 22–26 °C and 1,300–1,600 mm, respectively (Alvares et al., 2013). Data Collection.—Studied material included specimens available at the Coleção Herpetológica do Museu de História Natural da Universidade Federal de Alagoas (MUFAL) that were collected from 1994 to 2018, and specimens collected during two field expeditions to fill gaps in the representation of the specimens. The first field expedition took place from 19 to 23 January 2018, and employed active searches without time limitation. The second expedition took Figure 1. Environmental Protection Area of Catolé and place from 2 to 6 July 2018 in the Cerrado enclave, and Fernão Velho (EPACFV), Alagoas state, Brazil. A = Alagoas state, dark-grey area highlights the municipalities included in employed active searches along with pitfall trapping. the EPACFV; B = Location and limits (in green contour) of the Collected specimens were euthanized in 2% lidocaine EPACFV. Municipalities: 1-Rio Largo, 2-Maceió, 3-Satuba, 4- hydrochloride, fixed in 10% formalin and incorporated Santa Luzia do Norte, and 5-Coqueiro Seco; C = EPACFV into MUFAL (authorization SISBio/ICMBio 32920-1, boundary, hydrography and topography. CEUA nº 36/2015 and nº 50/2018). Anuran amphibians of a protected area in the northern Atlantic Forest 63 Figure 2. Habitats in the Environmental Protection Area of Catolé and Fernão Velho (EPACFV), Alagoas state, Brazil. A-Reservoir of the Carmem plant; B- Catolé reservoir; C- Junco lake; D- Permanent pond; E- Tank bromeliads; and F-Temporary pond. Morphological identification was based on available Vermelho da Fauna Brasileira Ameaçada de Extinção literature describing the species, while taxonomic (ICMBio, 2018). The geographic distribution of each nomenclature followed Frost (2019). The conservation species was obtained from Frost (2019) and Haddad et status of each species follow the International Union al. (2013). Reproductive modes followed Haddad and for the Conservation of Nature and Natural Resources Prado (2005) and trophic guilds of tadpoles followed (IUCN, 2019) and the Brazilian Red List — Livro the data compiled by Dubeux et al. (2019). 64 Marcos Jorge Matias Dubeux et al. Results 2019), and the accumulation of information on these species and their areas of occurrence from 2004 to 2018 A total of 282 adult anuran specimens and 125 tadpoles (Subirá et al., 2012). In addition, the fact that data are were assessed (App. 1). Forty species of 20 genera and deficient for evaluating the conservation
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