1 Herpetology Notes, volume 7: (2014) (published online on 16 April 2014) Anurans from the municipality of Ilha Grande, Parnaíba River Delta, Piauí, northeastern Brazil Etielle Barroso de Andrade 1,2*, José Roberto S. Almeida Leite 2,3 and Gilda Vasconcellos de Andrade 4 Abstract. The municipality of Ilha Grande is located on the largest island of the Parnaíba River Delta, in northern Piauí State, Brazil, and has a high biodiversity due to influences of the Cerrado and Caatinga biomes and the Coastal Marine Zone. Despite the high complexity of the habitats, divided into environments such as beaches, sand dunes and coastal tablelands, the amphibian fauna of the majority of the islands is still unknown. Given the lack of substantiated knowledge about amphibians from the northern state region, this study presents a list of anuran of the Ilha Grande municipality. Twenty-one species were identified belonging to five families, representing about 35% of the species of Piauí. This study adds seven new species to the list known to the municipality and presents the first record of Leptodactylus natalensis in the state. Keywords. Amphibians, Ilha Grande de Santa Isabel, survey, frogs. Introduction The amphibian fauna of the northern region of Piauí State remained unknown for about 30 years due to the lack of studies on characterizing the species in the region, which led to a false idea of a low representation of this group in the state. During this period, the only records of amphibians in Piauí were restricted to a preliminary list with 10 species provided by Caramaschi and Jim (1983a; b) in the municipality of Picos, central region of the state, which included the description of two new species (Elachistocleis piauiense and Dendropsophus soaresi). Only after 2007, several studies were conducted in the coastal region of the state in order to list the amphibian fauna and provide information on the occurrence of new species (Silva et al., 2007; Leite Junior et al., 2008; Loebmann and Mai, 2008; Loebmann et al. 2010; Macedo et al., 2011). Despite being a short coastline of just 66 km, the very north of Piauí has a high biodiversity mainly due to the 1 Programa de Pós-Graduação em Biodiversidade e Biotecnologia, BIONORTE, Universidade Federal do Maranhão, UFMA, , São Luís, MA, Brasil. 2 Núcleo de Pesquisa em Biodiversidade e Biotecnologia, BIOTEC, Campus de Parnaíba, Universidade Federal do Piauí, UFPI, , Parnaíba PI, Brasil. 3 Universidade Federal do Piauí, UFPI, Campus de Parnaíba, , Parnaíba PI, Brasil. 4 Universidade Federal do Maranhão, UFMA, , São Luís, MA, Brasil. *Corresponding author. influences of the Caatinga and Cerrado biomes and the Coastal Marine Zone (CEPRO, 1996) and this area is fully included in the Environmental Protection Area of the Parnaíba Delta (Área de Proteção Ambiental Delta do Parnaíba) (IBAMA, 1998). The Parnaíba River Delta is configured as a dynamic geomorphological area, consisting of about 80 islands (2750 km²) formed from the Parnaíba River and its effluents, and is considered the only open sea delta in the Americas (IBAMA, 1998; MMA/SDS, 2002). Ilha Grande municipality located in the coastal region of Piauí has a wide range of environments (beaches, sand dunes and coastal tablelands) (CEPRO, 1996), for some of which the herpetofauna is not well known. Thus, this study aims to increase the knowledge of the amphibian fauna of northern Piauí, providing an anuran checklist for species found in different environments in the Ilha Grande municipality including new records for this municipality. Materials and Methods The study was conducted in the municipality of Ilha Grande ( S; W), located in the largest island of Parnaíba River Delta (Figure 1). The island is separated from the mainland by the Igaraçu River, one of the principal effluents of Parnaíba River. The climate is characterized by temperatures ranging from 25 to 30 C and average annual rainfall exceeding 1,200 mm, concentrated mainly from January to May (IBAMA, 1998). The island s soil is mainly formed
2 220 Etielle Barroso de Andrade Figure 1. Schematic map of the sampled areas in the municipality of Ilha Grande. The capital letters represent the sampling areas: area A (inter-dune), B (woody vegetation) and C (restinga vegetation). The dotted line represents the political division between the towns of Ilha Grande and Parnaíba. by sand dunes, which enables the formation of several temporary ponds. There are four main vegetation types: 1) mangrove, a terrestrial ecosystem on a silty substrate (limoso), influenced by the presence of an estuary; 2) carnaubal, a region located in the southeastern part of the island subject to frequent accumulations of water during the rainy season, forming extensive wetlands and with dominant presence of Carnauba wax palm (Copernicia prunifera); 3) fruticeto restinga, characterized by the presence of shrub vegetation on sand dunes, and 4) herbaceous fields which extend across the front portion of the island to the edge of the beach (SEPLAN, 2008). Sampling was carried out in three different areas selected to represent the several environments on the island used by amphibians for breeding. Area A (inter-dune), located further south of the municipality, if compared to the other two sites, is predominantly composed of shrub vegetation and suffers a strong anthropogenic influence; area B, located in the central-west of the municipality, has denser vegetation with a predominance of woody vegetation; and Area C located at the north end of the municipality, is characterized by an open area with restinga vegetation with the presence of herbaceous or pioneer species (Figure 2). Samples were performed monthly (September 2008 to August 2009) in each area using the visual encounter survey and auditory survey methods (Crump and Scott, 1994; Zimmerman, 1994). The temporary ponds were observed only once in each night, being slowly explored for about one hour. Observations started at dusk, around 18:00 h, and finished at about 0:00 h or according to the decrease in the activity of frog vocalizing. Voucher specimens were collected (collecting permit / ICMBio) and housed in the Coleção Zoológica Delta do Parnaíba (CZDP) (Zoological Collections of the Panaíba River Delta), Campus de Parnaíba, Universidade Federal do Piauí. Results and Discussion We recorded 21 species belonging to 11 genera and five families: Leptodactylidae (10), Hylidae (7), Bufonidae (2), Odontophrynidae (1) and Microhylidae (1) (Table 1; Figure 3). Leptodactylidae is the most frequent family when considering the species belonging to the Leiuperidae family as a subfamily of Leptodactylidae, following Pyron and Wiens (2011). Regarding the amphibian richness of northern Piauí, Silva et al. (2007) also performed a study on
3 Anurans from the municipality of Ilha Grande, Parnaíba River Delta, Piauí, Brazil 221 Figure 2. Sampled habitats in the municipality of Ilha Grande, Piauí. A-B corresponds to A area (inter-dune) in the schematic map; C-D corresponds to B area (woody vegetation); E-F corresponds to C area (restinga vegetation). See schematic map above. anurans in the dunes of the Ilha Grande municipality, and recorded the presence of 14 species in the region: Rhinella granulosa, R. jimi, Dendropsophus nanus, Hypsiboas raniceps, Scinax x-signatus, Phyllomedusa nordestina, Physalaemus albifrons, Pleurodema diplolister, Pseudopaludicola mystacalis, Leptodactylus fuscus, L. macrosternum, L. pustulatus, L. vastus and Elachistocleis ovalis. Leite Júnior et al. (2008) increased the geographic distribution of Scinax fuscomarginatus for the north coast of northeastern region, recording the species including in the Ilha Grande municipality. The present study therefore adds
4 222 Etielle Barroso de Andrade Table 1. List of anuran collected in the municipality of Ilha Grande with the local distribution of species among the sampled habitats and their occurrences in the different morphoclimatic domains. Sampled habitats: ID - Inter-Dunes; RV - Restinga Vegetation; WV - Woody Vegetation. Biomes: AM - Amazon Rain Forest; CA - Caatinga; CE - Cerrado; AF - Atlantic Rain Forest; W wide distribution in open and forested areas. DD - Deficient data. Bufonidae Taxon Habitat Biome Rhinella jimi (Stevaux, 2002) ID, WV CE, CA, AF Rhinella mirandaribeiroi (Gallardo, 1965) ID AM, CE Hylidae Dendropsophus gr. microcephalus (Cope, 1886) ID, WV, RV AM, CE, CA Dendropsophus nanus (Boulenger, 1889) ID, WV, RV W Hypsiboas raniceps (Cope, 1862) ID, WV, RV W Scinax fuscomarginatus (A. Lutz, 1925) ID W Scinax gr. ruber (Laurenti, 1768) ID, WV AM, CE, CA Scinax x-signatus (Spix, 1824) ID, WV, RV W Phyllomedusa nordestina Caramaschi, 2006 ID, WV, RV CE, CA Leptodactylidae Adenomera gr. marmorata (Laurenti, 1768) WV CE, AF Leptodactylus fuscus (Schneider, 1799) ID, WV, RV W Leptodactylus macrosternum (Miranda-Ribeiro, 1926) ID, WV, RV CE, CA Leptodactylus natalensis (Lutz, 1930) WV CA, AF Leptodactylus pustulatus (Peters, 1870) ID, WV, RV CE Leptodactylus vastus (Lutz, 1930) ID, WV CE, CA Physalaemus albifrons (Spix, 1824) ID, WV, RV CE, CA Physalaemus cuvieri (Fitzinger, 1826) ID W Pseudopaludicola aff. mystacalis (Cope, 1887) ID, WV, RV W Pleurodema diplolister (Peters, 1870) ID, WV CE, CA Microhylidae Elachistocleis piauiensis (Caramaschi & Jim, 1983) ID, RV CE, CA Odontophrynidae Proceratophrys caramaschii (Cruz, Nunes & Juncá, 2012) ID DD seven new species to this list (Rhinella mirandaribeiroi, Adenomera gr. marmorata, Leptodactylus natalensis, Dendropsophus gr. microcephalus, Scinax gr. ruber, Physalaemus cuvieri and Proceratophrys caramaschii). Only E. ovalis, recorded by the previous authors, was not reported here, however, it is believed that the previous identification possibly refers to E. piauienses (Loebmann and Mai, 2008). The number of species found in this study was identical to the study by Loebmann and Mai (2008) in which 21 species were found during a survey in seven localities along the coast of Piauí (except in the municipality of Ilha Grande). Four of these were not recorded here (Dendropsophus minutus, Scinax nebulosus, Trachycephalus typhonius and Leptodactylus troglodytes). On the other hand, four taxa were not found by the previous authors (S. fuscomarginatus, L. natalensis, L. pustulatus and Adenomera gr. marmorata). This indicates that least 26 species are likely to occur in Ilha Grande. Furthermore, in 2011 the occurrence of Hypsiboas crepitans was recorded in the municipality of Parnaíba (Macedo et al., 2011), 15 km from the current collection areas, suggesting the inclusion of this species in the records of Ilha Grande. The number of species recorded in this study was also similar to that of two other municipalities in the coastal zone of the Ceará State, Caucaia and Pacajús, both with 20 species (Borges-Nojosa et al., 2010) and higher than reports by Andrade et al. (2012) in the Araioses municipality in the coastal region of Maranhão State (nine spp.). This study presented a higher number of species compared to other Caatinga areas of the
5 Anurans from the municipality of Ilha Grande, Parnaíba River Delta, Piauí, Brazil 223 Figure 3. Anurans recorded in the municipality of Ilha Grande, northeastern Brazil, Piauí, from September 2008 to August Family Hylidae: A Scinax x-signatus; B Scinax gr. ruber; C Scinax fuscomarginatus; D Dendropsophus nanus; E Dendropsophus gr. microcephalus; F Hypsiboas raniceps; G Phyllomedusa nordestina. Family Leptodactylidae: H Leptdactylus macrosternum; I Adenomera gr. marmorata; J Leptdactylus pustulatus; K Leptodactylus vastus; L Leptodactylus fuscus; M Leptodactylus natalensis; N Physalaemus cuvieri; O Physalaemus albifrons; P Pseudopaludicola aff. mystacalis; Q Pleurodema diplolister. Family Bufonidae: R Rhinella jimi; S Rhinella mirandaribeiroi. Family Microhylidae: Elachistocleis piauiensis. Family Odontophrynidae: U - Proceratophrys caramaschii.
6 224 Etielle Barroso de Andrade Figure 3 (continued) Northeast: Cratéus - Ceará (18 spp.) (Borges-Nojosa and Cascon, 2005); Betânia - Pernambuco (19 spp.) (Borges-Nojosa and Santos, 2005), Boa Vista (nine spp.) and São João do Cariri (16 spp.) in Paraíba (Vieira et al., 2007). This suggests a comparatively high species richness in Ilha Grande in relation to other, similar sites in the region. The amphibian fauna of Piauí is currently composed of about 60 species (Macedo et al., 2011; Roberto et al., 2013; Dal Vechio et al., 2013; present study). Thus, with the new records from this study, Ilha Grande ranks as the fourth most specie-rich municipality in Piauí, corresponding to about 35% of the anuran fauna recorded in the state, after Ribeiro Gonçalves (n = 32, 53%), Caxingó (n = 26, 43%) and Brejo do Piauí (n = 22, 36%) (Robert et al., 2013). According to Robert et al. (2013), although Piauí State not has endemic species, the location between the Cerrado and Caatinga favors the species occurrence of both biomes. These authors performed a compilation of data in the literature and supplemented with additional faunal inventories in three municipalities, providing information about the occurrence of most species found in the state. The species presented in this study further reinforce the influence of Cerrado and Caatinga biomes in the species composition of coastal region of Piauí. It is also possible that the amphibian species diversity of Piauí State as a whole is underestimated, due to the large areas that have not been sampled and due the presence of species with complex cryptic taxonomic status. Species of the genus Pseudopaludicola illustrate this complexity well, their small body size and cryptic
7 Anurans from the municipality of Ilha Grande, Parnaíba River Delta, Piauí, Brazil 225 color making them difficult to diagnose (Carvalho, 2012; Dal Vechio et al. 2013). This difficulty is quite visible in Piauí State, where three distinct species possibly occur: Pseudopaludicola parnaíba, recently described from the midwestern region of the state (Roberto et al., 2013), and two others identified by different authors as Pseudopaludicola aff. mystacalis (Silva et al., 2007; Dal Vechio et al., 2013; present study) and Pseudopaludicola gr. falcipes (Caramaschi and Jim, 1983a; 1983b; Loebmann and Mai, 2008), which are widely distributed in the state. The distributions of the last two are inclusive of the coastal region of the state (Loebmann and Mai, 2008; present study). Similarly to the genus Psudopaludicola, the species of the groups Adenomera marmorata, Scinax ruber and Dendropsophus microcephalus also present taxonomic uncertainties (Angulo et al., 2003; Dal Vechio et al., 2013; Medeiros et al., 2013). Due to the difficulty of identifying individuals from populations of Scinax fuscovarius, S. x-signatus registered in the domains Cerrado and Caatinga, Dal Vechio et al. (2013) has taken a conservative position and refer to these species only as Scinax gr. ruber 1 and 2. However, there is quite a marked similarity between individuals treated as S. x-signatus and a consensus on their identification by several authors (Silva et al., 2007; Loebmann and Mai, 2008; Roberto et al., 2013; present study). There is still a need to taxonomically define the populations of the S. fuscovarius and the S. ruber group. Furthermore, it was not possible to reach a precise diagnosis for Adenomera gr. marmorata and Dendropsophus gr. microcephalus, so both are treated generically here. I therefore urge the need for a revision of these groups in the state and I highlight the possibility of at least four new species in the region of the Parnaíba River Delta (Pseudopaludicola sp., Adenomera sp., Scinax sp. and Dendropsophus sp.). Except S. fuscomarginatus and R. mirandaribeiroi, the remaining species were found vocalizing in the sampled areas. Most species showed an extended period of vocalization throughout the year, with an average variation of six months of activity, mainly from January to July. Five species showed an explosive reproduction pattern, lasting from one (L. natalensis, P. cuvieri and P. diplolister) to two months (P. caramaschii and E. piauiensis), restricted to the months of February and March. Physalaemus cuvieri showed an atypical vocalization pattern in the region since several authors reported an extended reproductive period of five months (Zina et al., 2007; Santos et al., 2008; Oda et al., 2009), while P. diplolister vocalized at the beginning of the period with the highest rainfall, supporting the studies of Cardoso and Arzabe (1993) and Vieira et al. (2007). Due to lack of information on reproductive biology of P. camaschii, E. piauiensis and L. natalensis it was not possible to make a comparison with patterns of behavior for these species. Although most species found in the region can be considered typical for open formations of South America and of wide geographical distribution, both in open areas as well as in forested areas (Frost, 2013), knowledge of amphibian species in the Parnaíba River Delta is of great importance since it provides subsidies to propose priority areas for conservation based on the distribution patterns of species. Besides contributing information about the anuran fauna of northern Piauí, this study also records the first occurrence of L. natalensis in the state. Acknowledgements. We thank Ednaldo Nascimento da Rocha, Geilson Faustino da Rocha and Rafael Guimarães Macedo for help during fieldwork. Pedro Militão and Maria das Graças for their hospitality during the research, and Pedro da Costa Silva, who besides sharing his deep knowledge of the Delta region, was the key piece during our field trips. Gabriela Elisabeth Carvalho for the revision of English. To IBAMA for granting a collecting authorization (Licence nº /2009) and to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior CAPES for the scholarship granted to the Programa de Pós Graduação em Biodiversidade e Conservação and to CNPq for funding through the Universal Project /2007-1/ Edital MCT/CNPq 15/2007. References Andrade, E.B., Leite-Júnior, J.M.A., Silva-Leite, R.R., Vieira, D.L., Santos, R.C., Silva, V.G., Barbosa, E.A., Souza, V.V., Leite, J.R.S.A. (2012): Anuran diversity on the Ilha do Caju, Parnaíba Delta River, Maranhão State, Northeastern Brazil. Revista Biociências, Taubaté 18(1): Angulo, A., Cocroft, R.B., Reichle, S. (2003): Species identity in the genus Adenomera (Anura: Leptodactylidae) in southeastern Peru. Herpetologica 59(4): Borges-Nojosa, D.M., Cascon, P. (2005): Herpetofauna da Área Reserva da Serra das Almas, Ceará. In: Análise das Variações da Biodiversidade do Bioma Caatinga, p Araújo, F.S., Rodal, M.J.N., Barbosa, M.R.V., Eds., Brasília, Ministério do Meio Ambiente. Borges-Nojosa, D.M., Prado, F.M.V., Borges-Leite, M.J., Gurgel- Filho, N.M., Bacalini, P. (2010): Avaliação do Impacto do Manejo Florestal Sustentável na Herpetofauna de Duas Áreas de Caatinga nos Municípios de Caucaia e Pacajus no Estado do Ceará. In: Uso Sustentável e Conservação dos Recursos Florestais da Caatinga, p Gariglio, M.A., Sampaio, E.V.S.B., Cestaro, L.A., Kageyama, P.Y., Eds., Brasília, Serviço Florestal Brasileiro: MMA.
8 226 Borges-Nojosa, D.M., Santos, E.M. (2005): Herpetofauna da Área de Betânia e Floresta, Pernambuco. In: Análise das Variações da Biodiversidade do Bioma Caatinga, p Araújo, F.S., Rodal, M.J.N., Barbosa, M.R.V., Eds., Brasília, Ministério do Meio Ambiente. Caramaschi, U., Jim, J. (1983a): A new microhylid frog, genus Elachistocleis (Amphibia, Anura). Herpetologica 39(4): Caramaschi, U., Jim, J. (1983b): Uma nova espécie de Hyla do grupo marmorata do Nordeste Brasileiro (Amphibia, Anura, Hylidae). Revista Brasileira de Biologia 43(2): Cardoso, A.J., Arzabe, C. (1993): Corte e desenvolvimento larvário de Pleurodema diplolistris (Anura: Leptodactylidae). Revista Brasileira de Biologia 53(4): Carvalho, T.R. (2012): A new species of Pseudopaludicola Miranda-Ribeiro (Leiuperinae: Leptodactylidae: Anura) from the Cerrado of southeastern Brazil with a distinctive advertisement call pattern. Zootaxa 3328: CEPRO (1996): Macrozoneamento Costeiro do Estado do Piauí: Relatório ambiental e sócio-econômico. Teresina. Crump, M.L., Scott Jr, N.J. (1994): Visual encounter surveys. In: Measuring and Monitoring Biological Diversity Standard Methods for Amphibians, p Heyer, W.R., Donnelly, M.A.R., McDiarmid, W., Hayek, L.A.C., Foster, M.S. Eds., Smithsonian Institution Press, Washington. Dal Vechio, F.D., Recorder, R., Rodrigues, M.T., Zaer, H. (2013): The herperofauna of the Estação Ecológica Uruçuí-Uma, state of Piauí, Brazil. Papeis Avulsos de Zoologia 53(16): Frost, D.R. (2013): Amphibian Species of the World: an online reference. Version amphibia/index.html. New York: American Museum of Natural History. IBAMA (1998): Proteção e controle de ecossistemas costeiros: manguezais da Baía de Babitonga/Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis. Coleção meio ambiente. Série estudos pesca, 25. Brasília. 145p. Leite, Jr. J.M.A., Sampaio, J.M.S., Silva-Leite, R.R., Toledo, L.F., Loebmann, D., Leite, J.R.S.A. (2008): Amphibia, Anura, Hylidae, Scinax fuscomarginatus: Distribution extension. Check List 4: Loebmann, D., Mai, A.C.G. (2008): Amphibia, Anura, Coastal Zone, state of Piauí, Northeastern Brazil. Check List 4: Loebmann, D., Orrico, V.G.D., Cassini, C., Giasson, L.O.M. (2010): Anfíbios. In: Guia Ilustrado: Biodiversidade do Litoral do Piauí, p MAI, A.C.G., Loebmann, D. Eds., Sorocaba: Gráfica e Editora Paratodos. Macedo, R.G., Andrade, E.B., Leite, J.R.S.A. (2011): New record and distribution extension of Hypsiboas crapitans (Weid- Neuwied, 1824) (Anura, Hylidae) to the northern part of the state of Piauí, Brasil. Revista CEPSUL Biodiversidade e Conservação Marinha 2(1): Medeiros, L.R., Lourenço, L.B., Rossa-Feres, D.C., Lima, A.P., Andrade, G.V., Giaretta, A.A., Egito, G.T.B.T., Recco-Pimentel, S.M. (2013): Comparative cytogenetic analysis of some species of the Dendropsophus microcephalus group (Anura, Hylidae) in the light of phylogenetic. BMC Genetics 14(59): Etielle Barroso de Andrade MMA/SDS (2002): Zoneamento Ecológico-Econômico do Baixo Rio Parnaíba: Subsídios técnicos, Relatório Final. Brasília. Oda, F.H., Bastos, R.P., Lima, M.A.C.S. (2009): Taxocenose de anfíbios anuros no Cerrado do Alto Tocantins, Niquelândia, Estado de Goiás: diversidade, distribuição local e sazonalidade. Biota Neotropica 9(4): Pyron, R.A., Wiens, J.J. (2011): A large-scale phylogeny of amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution 61: Roberto, I.J., Ribeiro, S.C., Loebmann, D. (2013): Amphibians of the state of Piauí, Northeastern Brazil: a preliminary assessment. Biota Neotropica 13(1): Santos, T.G., Kopp, K., Spies, M.R., Trevisan, R., Cechin, S.Z. (2008): Distribuição temporal e espacial de anuros em área de Pampa, Santa Maria, RS. Iheringia, Série Zoológica 98(2): SEPLAN - Secretaria de Planejamento do Estado do Piauí (2008): Plano Diretor Participativo de Ilha Grande-PI. Relatório final, Diagnósticoe Prognóstico. Ilha Grande, v.1. Silva, G.R., Santos, C.L., Alves, M.R., Sousa, S.D.V., Annunziata, B.B. (2007): Anfíbios das Dunas Litorâneas do Extremo Norte do Estado do Piauí, Brasil. Sitientibus, Série Ciências Biológicas 7: Vieira, W.L.S., Arzabe, C., Santana, G.G. (2007): Composição e distribuição espaço-temporal de anuros no Cariri paraibano, Nordeste do Brasil. Oecologia Brasiliensis 11(3): Zimmerman, B.L. (1994): Audio strip transects. Pp In: Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Heyer, W.R., Donnelly, M.A., McDiarmid, R.W., Hayek, L.C., Foster, M. S. (Eds.). Smithsonian Institution Press, Washington D.C., U.S.A. Zina, J., Ennser, J., Pinheiro, S.C.P., Haddad, C.F.B., Toledo, L.F. (2007): Taxocenose de anuros de uma mata semidecídua do interior do Estado de São Paulo e comparações com outras taxocenoses do Estado, Brasil. Biota Neotropica 7(2): Accepted by Philip de Pous; Managing Editor: Christoph Liedtke