Reproductive Modes, Habitat Use, and Richness of Anurans from Chapada Dos Veadeiros, Central Brazil
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NORTH-WESTERN JOURNAL OF ZOOLOGY 10 (2): 365-373 ©NwjZ, Oradea, Romania, 2014 Article No.: 141505 http://biozoojournals.ro/nwjz/index.html Reproductive modes, habitat use, and richness of anurans from Chapada dos Veadeiros, central Brazil Guilherme Ramalho Chagas Cataldi SANTORO1,* and Reuber Albuquerque BRANDÃO2 1. Programa de Pós-graduação em Zoologia, Instituto de Biologia, Universidade de Brasília – DF. Campus Universitário Darcy Ribeiro, CEP 70910-900, Brasília, DF, Brazil. 2. Universidade de Brasília, Laboratório de Fauna e Unidades de Conservação, Departamento de Engenharia Florestal, Caixa Postal 04357. CEP 70919-970. Brasília, DF, Brazil. *Corresponding author, G.R.C.C. Santoro, E-mail: [email protected] Received: 06. February 2014 / Accepted: 14. March 2014 / Available online: 16. October 2014 / Printed: December 2014 Abstract. Anurans have the largest number of reproductive modes among vertebrates, and are especially diverse in New World Tropical Forests. However, species inhabiting open and drier biomes present reproductive modes adapted for breeding in these environments. Despite recent studies, the diversity of reproductive modes, species richness, and distribution of anurans in the Cerrado is still poorly known. The Chapada dos Veadeiros, in Central Brazil, harbors high species richness and endemism. This region is located in the central portion of the Cerrado and presents various physiognomies, especially those associated with high altitude plateaus (above 900 m a.s.l.). Herein, we evaluated the diversity of reproductive modes, habitat use, and conservation status of anurans from the Chapada dos Veadeiros. We found 54 species from eight families, which presented 14 reproductive modes, including a new mode for the Cerrado. Anuran richness in the Chapada dos Veadeiros is the highest in the Cerrado, highlighting its importance for the biome biodiversity. Among the species, 66% are Cerrado endemics, occurring mainly in open areas. Moreover, five species are known only from the region, and six have not been described yet. Most species occur in typical Cerrado formations, are terrestrial, and breed in lentic environments. Leptodactylids had the highest diversity of reproductive modes, followed by Hylids. In general, species showed adaptations for breeding in dry environments, being foam nests the most characteristic breeding strategy. Anuran conservation in the Cerrado depends on the maintenance of environmental heterogeneity of open areas. Key words: Cerrado, breeding, reproductive biology, amphibian richness, phytophysiognomies. Introduction Provete et al. 2011, Conte et al. 2013). The constraints generated by the specific re- Anurans have the greatest reproductive diversity quirements related to the reproductive modes of all tetrapods (Duellman & Trueb 1986), with 39 causes high habitat specificity in anurans (Ber- different reproductive modes (Haddad & Prado toluci & Rodrigues 2002). Therefore, regions with 2005). The classification of these categories of re- high structural complexity (Oda et al. 2009) and productive strategies is based on oviposition site, environmental heterogeneity (Diniz-Filho et al. egg characteristics, and type of parental care 2005) tend to present higher amphibian richness. (Salthe & Duellman 1973, Toledo et al. 2012). Dif- Previous studies suggested that anurans tend to ferent populations of the same species may exhibit segregate their reproductive periods temporally distinct reproductive modes due to competition or and spatially, so they can coexist and diminish the changes in oviposition site availability (Touchon & effects of competition (Oda et al. 2009, Kopp et al. Warkentin 2007, Toledo et al. 2012). 2010, Brandão et al. 2013). Nevertheless, historical The New World wet forests have the highest factors may also influence breeding activities and diversity of reproductive modes for anurans site preferences (Kopp & Eterovick 2006). (Wells 2007). The Brazilian Atlantic forest, for ex- The anuranfauna of open formations devel- ample, harbors 27 out of 39 known modes oped a series of evolutionary adaptations, primar- (Haddad & Prado 2005). Several studies con- ily related to breeding in dry environments with a ducted in open and seasonal biomes showed a well-defined seasonality (Duellman & Trueb smaller diversity of reproductive modes compared 1986). The majority of their reproductive strategies to forested biomes, and most species limit its re- involve adaptations for desiccation and sun expo- productive activity to the rainy season and use sure (Haddad & Prado 2005). Amphibians in sea- mainly lentic water bodies for egg laying (Haddad sonal biomes usually have a short reproductive & Prado 2005, Prado et al. 2005, Kopp et al. 2010, period and utilize accumulated water or some mi- 366 G.R.C.C. Santoro & R.A. Brandão Figure 1. The Chapada dos Veadeiros National Park (black line). White circles represent surveyed localities. crohabitats that retain humidity for egg deposi- conservation priority for Cerrado amphibians due tion, such as burrows, rock crevices, tree holes, to its high richness and endemicity (Diniz-Filho et and fallen logs; Duellman & Trueb 1986, Eterovick al. 2005). Its climatic stability during the late Pleis- & Fernandes 2001, Wells 2007, Kopp et al. 2010). tocene provided a refuge for Cerrado fauna, ex- Thus, even terrestrial breeders depend on water plaining its high richness (Werneck et al. 2012). A for eggs development (Gomez-Mestre et al. 2012). portion of this region (about 65,000 ha) is pro- The Cerrado is the most diverse savanna in tected by the Chapada dos Veadeiros National the world (Klink & Machado 2005), showing a Park and other small private reserves, but most of strongly seasonal climate, with a wet and warm the region lacks effective conservation policies, de- (October to April) and a dry and cold seasons spite its biological relevance. (May to September). Its original area comprised Herein, we provide data on habitat use, re- 23% of the Brazilian territory and is characterized production modes, and conservation status of the by a complex landscape with great horizontal het- anuranfauna from the Chapada dos Veadeiros Na- erogeneity in the distribution of open, savanic, tional Park and surrounding areas. and forested habitats (Ribeiro & Walter 1998). As a consequence, species distribution differs among those areas (Colli et al. 2002). About 52% of the 213 Materials and Methods anurans recorded for the Cerrado are endemic (Valdujo et al. 2012). Despite the recognized anu- Study area Fieldwork was conducted in the Chapada dos Veadeiros, ran richness in the central and northern portions Northern Goiás, central Brazil (between the latitudes 13° of the Cerrado, most of the surveys were focused and 15° S; and longitudes 47° to 49° W; Felfili 2007). The on the southern region of the Cerrado or near ur- Chapada dos Veadeiros National Park comprises four ban areas (Colli et al. 2002). Some studies showed municipalities: Alto Paraíso de Goiás, Cavalcante, Colinas that the diversity of Cerrado amphibians is greater do Sul, and Teresina de Goiás (Fig. 1). This region is char- in open habitats (Brandão & Araújo 2001, Valdujo acterized by highlands (up to 1670m a.s.l.), covered et al. 2011, 2012). Although some species use for- mainly by fields and open Cerrado physiognomies (Fig. 2). The soil is shallow and seasonally wet. The climate is ested habitats, the majority is adapted to open tropical highland (Köppen’s Cwa), with monthly mean habitats (Brandão & Araujo 2001), which are ex- temperatures ranging from 21°C to 22°C and 1,550 mm of tremely threatened (Silva & Bates 2002). mean annual rainfall (Ramalho et al. 2013). Forested habi- The region of the Chapada dos Veadeiros is a tats correspond to less than 5% of landscape (Felfili 2007). Diversity and reproduction of Cerrado anurans 367 Figure 2. Examples of physiognomies in the Chapada dos Veadeiros. A – Grassland (Campo limpo), B – Bush grassland (Campo sujo), C – Wet grassland (Campo alagável), D - Cerrado sensu strictu, E – Valley with gallery Forest, F – Riparian forest. Deep valleys are present in the surrounding and have We classified species by their habitats, reproduction more dense forests (Fig. 2). Grasslands are less repre- habitats, typical perch, distribution, and reproductive sented at low altitudes. The region has complex and het- modes (Table 1). The reproductive mode classification erogeneous vegetation, including open grasslands (campo (Haddad & Prado 2005) was based on natural history ob- limpo), bush grasslands (campo sujo), gallery forests, wet servations and collection information. grasslands (veredas) with Buritis (Mauritia flexuosa) palms, wet grasslands (campos alagáveis), and highland grass- lands (campos de altitude; Fig. 2). Results During the last 20 years, several researchers from the We recorded 54 anuran species from eight families Universidade de Brasília, including us, surveyed anurans and 19 genera. The most diverse family is Hylidae, in the Chapada dos Veadeiros National Park and its sur- roundings (Fig. 1). We used these records, along with an- followed by Leptodactylidae (Table 1). More than urans deposited in the Herpetological Collection of the half (66%) of the species are Cerrado endemics Universidade de Brasília (CHUNB) to establish the list of and five of them are known to occur only in the species occurring in the region. We also included de- study area (Adenomera juikitam, Hypsiboas ericae – scribed species from recent publications associated to the Fig. 3A;