On the intriguing occurrence of Rhinoclemmys punctularia (Daudin, 1801) in coastal plains of eastern Rio de Janeiro, Brazil

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1 Herpetology Notes, volume 7: (2014) (published online on 12 November 2014) On the intriguing occurrence of Rhinoclemmys punctularia (Daudin, 1801) in coastal plains of eastern Rio de Janeiro, Brazil Salvatore Siciliano 1, *, Jailson F. de Moura 1, Davi C. Tavares 1,2, Carlos Eduardo Silva de Amorim 1 and Carlos Alexandre R. Matias 3,4 The geographical distribution of many Brazilian freshwater turtles is poorly known, with few references regarding this subject (Pritchard and Trebbau, 1984; Iverson, 1992; Vanzolini, 1994). However, considerable effort has been made to update such data in recent years (e.g.bour and Zaher, 2005; Loebmann et al., 2006; Loebmann, 2008; Molina et al., 2009; Costa et al., 2010). The coastal region of Brazil is one of the country s most disturbed and exploited areas as a result of over 500 years of intense human settlement that followed Brazil s discovery by Portuguese sailors (Rocha et al., 2005). Consequently, the remaining vegetated coastal strips are undergoing extensive human impact, with increasing degradation of coastal sand plains, sand dunes, lakes, swamps and beach habitats ( restingas ) along the Brazilian coast (Araújo and Lacerda, 1987; Araújo, 1991; 2000; Rocha and Bergallo, 1997). Under such historical pressure, restingas may offer a number of suitable habitats for the aquatic turtles, which are 1 Escola Nacional de Saúde Pública/FIOCRUZ & Grupo de Estudos de Mamíferos Marinhos da Região dos Lagos (GEMM-Lagos), Rua Leopoldo Bulhões, º. andar, sala 611. Manguinhos, Rio de Janeiro, RJ Brazil 2 Universidade Estadual do Norte Fluminense UENF, Programa de Pós-graduação em Ecologia e Recursos Naturais/CBB LCA. Av. Alberto Lamego, Parque Califórnia, Campos dos Goytacazes, RJ Brazil 3 Universidade Federal Rural do Rio de Janeiro UFRRJ, Departamento de Epidemiologia e Saúde Pública DESP, Instituto de Veterinária IV. BR-465, Km 7, Seropédica, RJ Brazil 4 Programa de Pós-graduação em Saúde Pública e Meio Ambiente, Escola Nacional de Saúde Pública/FIOCRUZ. Rua Leopoldo Bulhões, º. andar. Manguinhos, Rio de Janeiro, RJ Brazil * Corresponding author gemmlagos@gmail.com found in coastal lakes and swamps. This paper reports two specimens of Aperema (Rhinoclemmys punctularia) recently found as the result of a large effort to survey beaches and associated habitats of the eastern Rio de Janeiro state coastline. These ecosystems are currently under tremendous pressure from fire, urbanization and general eradication, and for this reason our turtle records are noteworthy and underscore the importance of such environments. The Grupo de Estudos de Mamíferos Marinhos da Região dos Lagos (GEMM-Lagos, the Lagos Region Study Group on Marine Mammals/ENSP/FIOCRUZ) regularly patrols beaches in search of strandings along ca. 250 km of the eastern Rio de Janeiro State coast between latitudes S and 23 S, approximately. Since 1999, GEMM-Lagos maintains a regional reporting network and database of sea turtles, seabirds and marine mammal strandings, which includes information on both live-stranded and dead, beach-cast specimens. In addition, reports of diverse stranded non-marine animals are also made on a regular basis, which usually comprises rodents and marsupials, egrets and passerines, as well as terrestrial, aquatic and semiaquatic turtles. Considering the paucity of information of the reptile fauna of the eastern coast of Rio de Janeiro, especially for aquatic and terrestrial turtles, and the need for the conservation of their habitats, we provide noteworthy records of two non-marine turtles recently found by GEMM-Lagos. One specimen of R. punctularia was observed alive at Parque Natural Municipal dos Pássaros, Rio das Ostras municipality (RO), in December 2008 (Figure 1, record #1). The provenience of this turtle is unknown but the facility receives only wild reptiles, birds and mammals donated by the general public as well as specimens found by City Hall personnel inside RO boundaries.

2 668 Salvatore Siciliano et al. Figure 1. Location records of specimens of Aperema (Rhinoclemmys punctularia) found in the coastal plains of eastern Rio de Janeiro state, Brazil. Photographs were taken at Parque dos Pássaros facilities (Figure 2). The turtle was released in a RO coastal lagoon within a few days of its arrival at Parque Natural Municipal dos Pássaros. Following this first report, on 7 December 2011, a second R. punctularia specimen was found by locals on the beach of Orla 500, Cabo Frio, in the early morning (Figure 2, record #2). It was believed to be a sea turtle and several attempts were made by locals to release the turtle into the sea. As they did not succeed, the GEMM-Lagos personnel were called for assistance. On site, we noticed that it was a semiaquatic turtle specimen rather than a sea turtle and took measurements and photographs for our records (Figure 3). The specimen was released in a small lake in the vicinity of the original capture site. It has been regularly re-sighted in the area since then. By January 2014 it weighed 990 grams, with carapace measurements 197 mm long, 140 mm wide, and 70 mm high. Rhinoclemmys punctularia (Daudin, 1801), popularly known in Northern Brazil as Aperema, is the only member of the Geoemydidae in Brazil. The Aperema inhabits rivers and lakes, has small orange spots on the dorsal surface of the head and is distributed throughout South America (Gans, 1980; Ernst and Barbour, 1989). It is common in coastal regions as far east as Belém, Pará State, with few reports in Central Amazonia, between the states of Maranhão and Pará, and a doubtful record exists from eastern Rio Grande do Norte (Pritchard and Trebbau, 1984; Ávila-Pires et al., 2010; Dornas et al., 2011). Although this may be considered a highly unexpected occurrence, the R. punctularia Cabo Frio specimen could be living in the nearby Praia Rasa Reserve, a protected area under jurisdiction of the Brazilian Navy. This particular site possesses swamps, marshes and coastal lakes in near-pristine condition, which can provide shelter to medium sized mammals and reptiles, such as capybaras and caimans (SS, personal observation). In fact, range extensions for R. punctularia were recently reported for Tocantins and Maranhão, central-north Brazil, well inside the Cerrado biome (Dornas et al., 2011; Silva et al., 2011; Pereira et al., 2013). These records are clear evidence of the general lack of information on the geographical distribution of Brazilian terrestrial and freshwater turtles, particularly

3 On the intriguing occurrence of Rhinoclemmys punctularia in Brazil 669 Figure 2. Dorsal view (A), plastron view (B) and details of the carapace (C) and head (D) of the Aperema (Rhinoclemmys punctularia) specimen found in Rio das Ostras, eastern Rio de Janeiro state, Brazil in December R. punctularia, (Pritchard and Trebbau, 1984; Iverson, 1992; Vanzolini, 1994). Not surprisingly, as a possible result of increased search effort, there are now available numerous articles covering the range extensions of some terrestrial and aquatic turtles in Brazil (e.g. Molina et al., 2009; Sousa and Novelli, 2009; Costa et al., 2010; Silveira and Valinhas, 2010). Indeed, the description of a new species of side-necked turtle (genus Mesoclemmys) within the Cerrado-Caatinga biomes in Northeastern Brazil (Bour and Zaher, 2005) is equally remarkable. We must consider the possibility of the present R. punctularia specimens as being of captive origin that escaped or unintentionally introduced in the area. If a captive origin is to be considered, they probably came from an unknown breeding facility. Authorized breeders are listed in: criadouros/conservacionistas.pdf, and no breeders are found in the Cabo Frio Rio das Ostras surroundings. In addition, Aperema turtles have not been a component of the common wildlife trade in south-southeastern Brazil. In contrast, Trachemys dorbigni and Trachemys scripta elegans are traditionally kept as pets elsewhere in south-southeastern Brazil. Additionally, Chelonoidis carbonaria and C. denticulata are commonly kept as pets in most parts of Brazil. In fact, specimens of Trachemys scripta elegans and C. denticulata are frequently found in the houses of the various surrounding municipalities including Cabo Frio, Armação dos Búzios, Casimiro de Abreu, São Pedro D Aldeia, Iguaba Grande, Araruama and Rio das Ostras. Strays of such species are often reported to our group. We can also speculate that specimens of R. punctularia were brought as pets from the Amazon region and released after they increased in size. However, the possibility of a relictual population of Rhinoclemmys occurring in a small area in eastern Rio de Janeiro state cannot be disregarded. The restingas of eastern Rio de Janeiro are important areas of reptilian endemism (Rocha et al., 2005). This particular stretch of coastal vegetation is home to endemic species of lizards (Liolaemus lutzae and Cnemidophorus littoralis) in addition to a recently described Colubridae (Tantilla

4 670 Salvatore Siciliano et al. Figure 3. Dorsal view (A), plastron view (B), details of the head and carapace (C, D) of the Aperema (Rhinoclemmys punctularia) specimen found on the beach of Orla 500, Cabo Frio, RJ on 7 December sp.) and one amphisbaena (Rocha et al., 2005; Muniz, 2010). Not surprisingly, our specimens were found in an environment with many coastal plain lakes. This agrees with the findings of Wariss et al. (2012) for a coastal area in northeastern Pará state, in which almost 90% of R. punctularia specimens were caught in the coastal plain lakes. The origin of the R. punctularia specimens on the coast of eastern Rio de Janeiro state is of great concern. The nearest confirmed record is from Tocantins, some 1,500 km in linear distance from eastern Rio de Janeiro. Whether they represent an invasive alien species or a naturally occurring population, their occurrence clearly indicates the need of future field surveys to clarify this question. Acknowledgements. Specimens were recovered under permit nr issued by MMA/ICMBio. We are indebted to all the technicians, interns and volunteers of GEMM-Lagos in recent years for their dedicated assistance during field work. CAR Matias and RLQ de Freitas Filho provided the pictures of the reported specimens in the field and lab. References Araújo, D.S.D., Lacerda, L.D. (1987): A natureza da restinga. Ciência Hoje 6: Araújo, D.S.D. (1991): As restingas dizimadas. Ecorio 1: Araújo, D.S.D. (2000): Análise florística e fitogeográfica das restingas do estado do Rio de Janeiro. Unpublished. Universidade Federal do Rio de Janeiro - UFRJ, Rio de Janeiro, 169 pp. Ávila-Pires, T.C.S., Hoogmoed, M.S., Rocha, W.D. (2010): Notes on the vertebrates of northern Pará, Brazil: a forgotten part of the Guianan region, i. Herpetofauna. Boletim do Museu Paraense Emílio Goeldi 5: Bour, R., Zaher, H. (2005): A new species of Mesoclemmys from the open formations of northeastern Brazil (Chelonii, Chelidae). Papéis avulsos de Zoologia 45: Costa, H.C., Molina, F.B., São-Pedro, V.A., Feio, R.N. (2010): Reptilia, Testudines, Kinosternidae, Kinosternon scorpioides scorpioides (Linnaeus, 1766): Distribution extension. Check List 6: Dornas, T., Malvasio, A., Pinheiro, R.T. (2011): Reptilia, Testudines, Geoemydidae, Rhinoclemmys punctularia (Daudin, 1802): New geographical distribution and first record for the state of Tocantins, Brazil. Check List 7: Ernst, C.H., Barbour, R.W. (1989): Turtles of the world, Washington, Smithsonian Institution Press.

5 On the intriguing occurrence of Rhinoclemmys punctularia in Brazil 671 Gans, C. (1980): Répteis do mundo, São Paulo, Universidade de São Paulo. Iverson, J.B. (1992): A revised checklist with distribution maps of the turtles of the world, Richmond, Privately Printed. Loebmann, D., Mai, A.C.G., Garcia, A.M. (2006): Reptilia, Chelidae, Mesoclemmys tuberculata: Geographical distribution extension. Check List 2: Loebmann, D. (2008): Geographic distribution. Mesoclemmys perplexa. Brazil: Ceará. Herpetological Review 39: 236. Molina, F.B., Costa, H.C., São-Pedro, V.A., Feio, R.N. (2009): Reptilia, Testudines, Chelidae, Platemys platycephala platycephala: Distribution extension. Check List 5: Muniz, C. (2010): Nova serpente litorânea. Available at: cienciahoje.uol.com.br/noticias/2010/03/nova-serpentelitoranea Last accessed on 27 Oct Pereira, L.N., Santos, D.L., T.S., V., Oda, F.H. (2013): Filling gaps on the distribution of Rhinoclemmys punctularia (Daudin, 1801) (Testudines: Geoemydidae) in the state of Maranhão, Brazil. Check List 9: Pritchard, P.C.G., Trebbau, P. (1984): The turtles of Venezuela, Ohio, Society for the Study of Amphibians and Reptiles. Rocha, C.F.D., Bergallo, H.G. (1997): Intercommunity variation in the distribution of abundance of dominant lizard species in restinga habitats. Ciência e Cultura 49: Rocha, C.F.D., Van Sluys, M., Bergallo, H.G., Alves, M.a.S. (2005): Endemic and threatened tetrapods in the restingas of the biodiversity corridors of Serra do Mar and of the central da Mata Atlântica in Eastern Brazil. Brazilian Journal of Biology 65: Silva, M.B., Resende, I.M.C., Paranhos, J.D.N., Barreto, L. (2011): Reptilia, Testudines, Geoemydidae, Rhinoclemmys punctularia (Daudin, 1801): Distribution extension. Check List 7: Silveira, A.L., Valinhas, R.V. (2010): Primeiro registro de Mesoclemmys tuberculata (Reptilia, Testudines, Chelidae) em área de Cerrado no estado de Minas Gerais, sudeste do Brasil. Biotemas 23: Sousa, B.M., Novelli, I.A. (2009): Reptilia, Testudines, Chelidae: Hydromedusa tectifera: Distribution extension in Brazil. Check List 5: Wariss, M., Isaac, V.J., Pezzuti, J.C.B. (2012): Habitat use, size structure and sex ratio of the spot-legged turtle, Rhinoclemmys punctularia punctularia (Testudines: Geoemydidae), in Algodoal-Maiandeua island, Pará, Brazil. Revista de Biologia Tropical 60: Vanzolini, P.E. (1994): On the distribution of certain South American turtles (Testudines: Testudinidae & Chelidae). Smithsonian Herpetological Information Service 97: Accepted by Mirco Solé