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Herpetofauna of Protected Areas in the Caatinga VI: the Ubajara National Park, Ceará, Brazil

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Herpetofauna of Protected Areas in the Caatinga VI: the Ubajara National Park, Ceará, Brazil Herpetology Notes, volume 12: 727-742 (2019) (published online on 09 July 2019) Herpetofauna of protected areas in the Caatinga VI: the Ubajara National Park, Ceará, Brazil Déborah P. de Castro1,2,3,*, Sarah Mângia4,5, Felipe de M. Magalhães4, David L. Röhr6, Felipe Camurugi4, Ricardo R. da Silveira-Filho4,7, Margarida M. X. da Silva1,3, John A. Andrade-Oliveira1, Tiago A. de Sousa1, Frederico G. Rodrigues França8, D. James Harris9, Adrian A. Garda4,6, and Diva M. Borges-Nojosa1,3,9 Abstract. We present a list of amphibians and reptiles collected in Ubajara National Park, Ceará, Brazil, from April 2014–May 2015. The local herpetofauna was sampled using active searches and pitfall traps, divided into four altitudinal bands along the park. We recorded a total of 71 species, including 25 frogs, one caecilian, one amphisbaenian, two turtles, 19 lizards, and 23 snakes. The species accumulation curve reached an asymptote for amphibians, but reptiles remain underestimated. Our work is the result of a standardized study on the herpetofauna of protected areas in northeastern Brazil. The results presented here contribute to the knowledge on the richness of protected areas in the Caatinga and can serve as a basis for future studies of populations, ecology, distribution, and environmental impact on herpetofaunal assemblages. Keywords. Amphibians, Brejos de Altitude, Caatinga, Inventory, Northeastern Brazil, Reptiles Introduction Ab’Saber, 1998). However, these current environmental conditions were not permanent in the past, since the The Caatinga domain was initially considered Caatinga passed through wetter climates associated a homogeneous landscape poor in biodiversity with humid vegetation during the Pleistocene (Auler et (Vanzolini, 1963). It is characterized by deciduous al., 2004). Around 210,000 years ago, regular cycles of xerophytic and thorny vegetation such as cactus, shrubs, moister climate allowed the replacement of part of the and small trees, and by a severe water deficit caused semi-arid vegetation of the Caatinga by forests, while by intense and unpredictable dry seasons (Cole, 1960; 1 Núcleo Regional de Ofiologia, Universidade Federal do Ceará, 6 Departamento de Botânica e Zoologia, Centro de Biociências, Campus do Pici, Bloco 905, Fortaleza, Ceará 60455-760, Universidade Federal do Rio Grande do Norte, Campus Brazil. Universitário, Lagoa Nova, Natal, Rio Grande do Norte 2 Current address: Faculdade de Educação de Itapipoca, 59072-970, Brazil. Universidade Estadual do Ceará, Av. Monsenhor Tabosa, 7 Current address: LECOT – Laboratório de Ecologia de Itapipoca, Ceará, 62500-000, Brazil. Transições, Departamento de Ciências Biológicas, 3 Programa de Pós-Graduação em Ecologia e Recursos Naturais, Universidade do Estado do Mato Grosso, 78690-000, Nova Universidade Federal do Ceará- UFC, Departamento de Xavantina, Mato Grosso, Brazil. Biologia, Campus do Pici, Fortaleza, Ceará 60440-900, 8 Centro de Ciências Aplicadas e Educação, Universidade Brazil. Federal da Paraíba, Campus IV – Litoral Norte, Rua da 4 Programa de Pós-Graduação em Ciências Biológicas, Mangueira, Rio Tinto, Paraíba 58297-000, Brazil Universidade Federal da Paraíba–UFPB, Centro de Ciências 9 Centro de Investigação da Biodiversidade e Recursos Exatas e da Natureza, Cidade Universitária, João Pessoa, Genéticos, Universidade do Porto, Campus Agrário de Vairão, Paraíba 58000-000, Brazil. Rua Padre Armando Quintas, Vairão, Vila do Conde, 4485- 5 Current address: Mapinguari – Laboratório de sistemática, 661, Portugal. biogeografia e história natural de anfíbios e répteis, * Corresponding author. E-mail: [email protected] Universidade Federal do Mato Grosso do Sul, Instituto de Biociências, 79070-900, Campo Grande, Mato Grosso do Sul, Brazil. 728 Déborah P. de Castro et al. expansions of the Caatinga occurred during colder and strict protection areas. In Ceará State, of the nine drier climates (Wang et al., 2004). Currently, rainforest protected areas, only the Ubajara National Park, located enclaves (called Brejos de Altitude in northeastern in Ibiapaba Plateau, has a more rigorous level of Brazil) occur in isolated areas surrounded by semi-arid protection (ICMBIO, 2014). Caatinga vegetation (Ab’Sáber, 1977). Such remnants The Ibiapaba Plateau region has been the subject of persist on the slopes and top of higher-altitude areas some studies on reptile and amphibian assemblages in such as the Baturité, Borborema, Ibiapaba, and Araripe recent years (Loebmann and Haddad, 2010; Botero et plateaus in northeastern Brazil. al., 2014). In the herpetofaunal list from the Ibiapaba Due to the milder climatic conditions, these relictual Plateau Complex, Loebmann and Haddad (2010) moist forests have a high human population density included fieldwork in the National Park of Ubajara, and support high levels of agricultural production but they did not discriminate which species were found (Andrade and Lins, 1964), which has reduced native within the Park as opposed to elsewhere. Botero et al. vegetation to small patches at different successional (2014) included only amphibians of Ubajara National stages, inserted in areas of anthropic use (Sales et al., Park and neighbouring regions. In this study we provide 1998; Araújo et al., 2007). The loss and fragmentation a complete species list of both amphibians and reptiles of habitats can affect the fauna, which remains isolated for the Ubajara National Park. in small vegetation fragments where population sizes are significantly reduced (Borges-Nojosa, 2007). Material and Methods In this sense, strict protection areas are an essential Study site.—Our study was conducted in the Ubajara environmental management tool, to safeguard regions National Park (-3.840250°S, -40.894889°W). The park that are characterized both for their scenic beauty and comprises 6,288 ha and is located in the northwestern the diversity of animal and plant species (Bastos, 2011). portion of Ceará State on the Ibiapaba Plateau, and its Nevertheless, only a small part of the humid mountains perimeter crosses three municipalities, Ubajara, Tianguá, of northeastern Brazil is adequately protected within and Frecheirinha (ICMBIO, 2014; Fig. 1). Because of Figure 1. Location of Ubajara National Park, Ceará State, Brazil (green triangle). Map by Mesquita, A. F. Herpetofauna of protected areas in the Caatinga VI, Ceará, Brazil 729 the proximity to the coast, rainfall is high and reaches cm high (Corn, 1994; Cechin and Martins, 2000). We 1400 mm annually, and average temperature ranges used buckets of different sizes to determine whether from 22–26ºC. The region presents two distinct seasons, a difference in animal capture by species size or with most rainfall concentrated in the first six months composition occurred. Stations were positioned 200 m of the year (Bezerra et al., 1997; FUNCEME, 2014). from each other, and pitfall traps were inspected daily. The vegetation is heterogeneous across the park. Humid We also conducted active searches with four observers, forests are found at higher elevations and replaced at 4 h per day. Four observers actively searched for lower elevations by semi-deciduous tropical rainforest specimens by day (09:00–11:00 h or 15:00–17:00 h) and in sloping areas, and by an arboreal Caatinga (Thorny at night (19:00–21:00 h), in different vegetation types, Deciduous Forest) in the lower areas (Figueiredo, 1997; preferentially at potential amphibian breeding sites. Souza, 1997). Pitfall traps remained open during all study days, and we performed 1344 hours of active searches. Voucher Data collection.—Our fieldwork lasted 84 days and specimens were euthanised with intravenous lidocaine, was divided into four periods within 2014 and 2015, fixed in 10% formalin, and preserved in 70% ethanol. including 03–17 April (15 days), 08 May–07 June 2014 The number of specimens collected was under the (30 days), 02–21 December 2014 (19 days), and 14 permits of the responsible agencies (DPC SISBIO April–02 May 2015 (20 days). We installed two lines of # 39073-4). Voucher material was deposited in the pitfalls traps, a total of 40, in four different elevational Coleção de Herpetologia da Universidade Federal do bands along the park (200, 400, 600, and 800 m; Fig. Ceará (CHUFC) and in the Coleção Herpetológica da 2). Each pitfall array was composed of two 30l and Universidade Federal da Paraíba (CHUFPB-UFPB). two 60l buried buckets, arranged in a Y-formation with Taxonomy follows Segalla et al. (2019) for amphibians buckets interconnected by 5 m long plastic fences, 50 and Costa and Bérnils (2018) for reptiles. Figure 2. Habitat at four different elevational sampling points in Ubajara National Park, Ceará State, Brazil. Elevations are 200 m (A), 400 m (B), 600 m (C), and 800 m (D). Photographs by Castro, D.P. 730 Déborah P. de Castro et al. To evaluate sampling efficiency, we constructed and Haddad (2010) listed this species for the Ibiapaba species accumulation curves separately for amphibians, Plateau, the authors did not specify whether the species lizards, and the entire group of reptiles, considering was recorded inside the Ubajara National Park. individual species abundance (Gotelli and Colwell, The number of amphibian species found in our study 2001). The samples were arranged in random order by represents 45.6% of the 57 amphibians registered by the Mao Tao method since this eliminates the effects of Roberto and Loebmann (2016) for Ceará State. The sampling sequence in the species accumulation curve. number of species found is a subsample of
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