at Parque Estadual da Serra do Tabuleiro
Transcrição
at Parque Estadual da Serra do Tabuleiro
Herpetology Notes, volume 7: 11-15 (2014) (published online on 25 January 2014) Reproduction of two exotic species of Trachemys Agassiz, 1857 (Testudines, Emydidae) at Parque Estadual da Serra do Tabuleiro, state of Santa Catarina, southern Brazil Marcos Adriano Tortato1, Raíssa Fries Bressan1,2* and Tobias Saraiva Kunz1,2 The genus Trachemys Agassiz, 1857 includes 15 species and is distributed from the mid-western United States to southern South America (Seidel, 2002). Trachemys scripta elegans (Wied, 1838) is native to the west of the United States and occurs from the state of Virginia until the north of Florida (Fritz and Havaš, 2007, van Djik et al., 2011). During the last decades, hatchlings and juveniles of this species have been extensively commercialized all over the world as pets, therefore, established populations are known in several countries (e.g. Ficetola, Monti and Padoa-Schioppa, 2002; Cadi et al., 2004; Bunnel, 2005; Shiau et al., 2006; Perry et al., 2007; Pupins, 2007; Soorae, Quarqaz and Gardner, 2008; O’Keeffe, 2009; Kitowski and Pachol, 2009; Izquierdo et al., 2010), including Brazil (Vieira and Costa, 2006; Ferronato et al., 2009; Bujes, 2011; Silva-Soares et al., 2011), where importation and commercialization were forbidden in 1991 by the federal environmental agency (IBAMA) (Souza et al., 2007). Trachemys dorbigni (Duméril and Bibron, 1835) is the southernmost species of the genus. It is present in practically all Uruguayan territory (Cabrera, 1998; Achaval and Olmos, 2007), in northeastern Argentina – from the provinces of Misiones and Corrientes to the La Plata River (Waller and Chebez, 1987; Cabrera, 1998; Alcalde et al., 2012) and in southern Brazil, in the central-south portion of the state of Rio Grande do Caipora Cooperativa, Avenida Desembargador Vitor Lima, 260, Sala 513 CEP 88040-400, Carvoeira, Florianópolis – SC, Brasil. 2 Programa de Pós-Graduação em Biologia Animal, Laboratório de Herpetologia, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Brasil. Av. Bento Gonçalves, 9500, sala 109, Agronomia, Porto Alegre-RS, Brasil, CEP 91509-900. *Corresponding author: [email protected] 1 Sul reaching, by the coastal plain, the northeast region of this state, close to the border with the state of Santa Catarina (Lema and Ferreira, 1990; Lema, 1994; Santos et al., 2005; Bujes, 2010; Alcalde et al., 2012). Recently, Trachemys dorbigni was recorded in two conservation units in southeast and south Brazil. An adult female was found at the Parque Estadual Morro do Diabo, southwest of the state of São Paulo, in the Paraná River Basin (Zaher et al., 2009; Santos et al., 2009). This record was attributed to introduction or recent distribution expansion of the species (Santos et al., 2009). In the west of the state of Santa Catarina, the species was recorded at the Parque Estadual das Araucárias, (Hartmann and Giassom, 2008). Since the species’ occurrence in the southern Brazilian plateau is very unlikely this specimen may also represents a case of introduction. Hatchlings and juveniles of T. dorbigni are also commercialized as pets in many Brazilian states (Molina and Gomes, 1998a; Bujes and Verrastro, 2008). Even though it is probably a native species of the southern coastal plain of the state of Santa Catarina (Bujes, 2010), T. dorbigni, as well as T. s. elegans, was officially considered an invasive alien species by this state’s environmental agency (CONSEMA, 2010), because of its presence in regions outside its natural range, specifically in the ombrophilous dense forest of the eastern region of the state. The Parque Estadual da Serra do Tabuleiro (PEST) is located in the mid-east region of Santa Catarina (Fig. 1). With 84.130 ha, it is the largest terrestrial conservation unit in the state, and includes several vegetation physiognomies of the Atlantic Forest Biome, such as ombrophilous dense forest, cloud forest, mixed ombrophilous forest (Araucaria forest), altitudinal fields, restingas and mangroves (Ishy et al., 2009). The coastal plain located at the eastern portion of the PEST, known as Restinga da Baixada do Maciambu (RBM), is adjacent to the Atlantic Ocean (27o50’ S; 48o50’ W), and 12 Marcos Adriano Tortato et al. Figure 1. Map showing the location (black star) of the Restinga da Baixada do Maciambu and the Visitors Centre of the Parque Estadual da Serra do Tabuleiro, State of Santa Catarina (SC), Brazil. RS = state of Rio Grande do Sul; PR = state of Paraná. presents mainly grassland formations with shrubs and scattered trees found in the driest areas over the sand ridges. Extensive humid areas are found between sand ridges, formed by perennial lakes connecting to marshes during the rainy season. Cyperaceae and Tifaceae are dominant families (Klein, 1981). Four turtle species are known to exist in the RBM: the chelid turtles Phrynops hilarii (Duméril and Bibron, 1835) (Tortato, 2007) and Hydromedusa tectifera Cope, 1869 (M. Tortato, pers. obs.) and the exotic emydids T. s. elegans (Wied, 1838) (Tortato, 2007; this study), and T. dorbigni (this study), as well as some specimens of the introduced tortoise, Chelonoidis carbonaria (Spix, 1824) (M. Tortato, pers. obs.). At least P. hilarii is known to nest in this area (Tortato, 2007). In September and October 2006, three T. dorbigni females were recorded nesting in the RBM (fig. 2A). Two records occurred on September 17th, between 9 and 11 a.m.; the first nest was 12 cm deep and contained nine eggs; the second nest, located 30 cm away from the first, was 16 cm deep and contained 10 eggs. Both were above the maximum water level, 1.5 m away from a dry water channel and approximately 140 m away from a perennial pond. On October 18th, around 1 p.m., the third nesting female was found on a sand ridge covered by low vegetation (grasslands). This female laid five eggs in a 15 cm deep nest. It was cloudy and rainy in both days when T. dorbigni nesting was recorded. Females of this species may lay at least two clutches per year as was verified by Vanzolini (1997) and corroborated by Molina and Gomes (1998b) and Bager, Freitas and Krause (2007). Clutch size recorded at the Taim Ecological Station, Rio Grande do Sul state, varied from six to 19 eggs (Bager, Freitas and Krause, 2007), while Fagundes, Bager and Cechin (2010) recorded a clutch size varying from four to 15 eggs. On October 20th a tegu lizard (Tupinambis merianae) was observed digging and preying on eggs from the second nest. Lizards of the genus Tupinambis are well known predators of vertebrates’ eggs, including turtles (e.g. Krause, Gomes and Leyser, 1982; Gonçalves, Cechin and Bager, 2007; Tortato, 2007; Salera-Jr., Malvasio and Portelinha, 2009; Schneider, Ferrara and Vogt, 2009; Fagundes, Bager and Cechin, 2010; Schneider et al., 2011). Reproduction of two exotic species of Trachemys Agassiz, 1857 The nesting activity of T. dorbigni observed in the PEST occurred at the beginning of the species egglaying season, known to extend from September to February (Krause, Gomes and Leyser, 1982; Bager, Freitas and Krause, 2007; Gonçalves, Cechin and Bager, 2007; Fagundes, Bager and Cechin, 2010). The occurrence of nesting during rainy days may be a way to prevent desiccation of eggs or the elevation of females’ body temperature (Moll and Legler, 1971). On September 1st 2006, three Trachemys hatchlings were observed; one was being predated by a burrowing owl (Athene cunicularia) and the other two were in a pond 13 about 50 m away from the T. dorbigni nesting site. Of these, one was collected (maximum carapace length 39 mm; fig. 2B-C), identified as T. s. elegans, and deposited in the Collection of Reptiles of the Departamento de Ecologia e Zoologia of the Universidade Federal de Santa Catarina, Santa Catarina, Brazil (CHUFSC 866). Considering that they were found in late winter, it is possible that these hatchlings had overwintered in the nest (see Bager, Fagundes and Piedras, 2007). The collected individual already presented a completely unfolded shell and a partially closed umbilical scar. Figure 2. Trachemys spp. recorded in the PEST. 2A) Female T. dorbigni photographed after nesting (nest 02); 2B) Dorsal view of the T. s. elegans hatchling (CHUFSC 866); 2C) Ventral view of the same hatchling. 14 The establishment of reproductive populations of T. scripta in the European Union is related to warmer climates and higher precipitation (Ficetola, Thuiller and Padoa-Schioppa, 2009) and its establishment risk was evaluated as moderate (Kopecky, Kalous and Patoka, 2013). There is no data about the establishment of reproductive T. scripta populations in Brazil, and the same is true for T. dorbigni populations out of its natural range. Field observations indicate that T. dorbigni is more abundant than T. scripta in the PEST. If these were reproductive populations, as our data suggest, T. dorbigni could be favored by the resemblance and geographic proximity to its natural range of distribution. Acknowledgements. The authors would like to thank the Fundação do Meio Ambiente of the state of Santa Catarina (FATMA), the staff of the Visitors Centre of the Parque Estadual da Serra do Tabuleiro, Alex Bager and Silvia Ziller for their help and information provided. We would like to specially thank Flavio de Barros Molina for the valuable contributions and for reviewing the manuscript. References Achaval, F., Olmos, A. (2007): Anfibios y reptiles del Uruguay, 3rd Edition. Montevideo, Zonalibro. 160p. Alcalde, L., Derocco, N.N., Rosset, S.D., Williams, J.D. (2012): Southernmost localities of Trachemys dorbigni and first record of Trachemys scripta elegans for Argentina (Cryptodira: Emydidae). Chelonian Conservation and Biology 11(1): 128133. Bager, A., Fagundes, C.K., Piedras, S.R.N. (2007): Trachemys dorbignyi (Brazilian Slider). Hatchling overwintering. Herpetological Review 38(3): 335-336. Bager, A., Freitas, T.R.O., Krause L. (2007): Nesting Ecology of a Population of Trachemys dorbignyi (Emydidae) in Southern Brazil. Herpetologica 63(1): 56-65. Bujes, C.S. (2010): Os Testudines continentais do Rio Grande do Sul, Brasil: taxonomia, história natural e conservação. Iheringia Série Zoologia 100(4): 413-424. Bujes, C.S. (2011): Chelonia Project - Study Group for Freshwater Turtle Conservation and Biology in Southern Brazil: Introduction of Trachemys scripta elegans in the Jacuí Delta. Turtle and Tortoise Newsletter 15: 14–17. Bujes, C.S., Verrastro, L. (2008): Quelônios do delta do Rio Jacuí, RS, Brasil: uso de hábitats e conservação. Natureza e Conservação 6(2): 47–60. Bunnel, C.G. (2005): Field survey of red-eared sliders (Trachemys scripta elegans) in the Lower Fraser River Valley, British Columbia, in 2005. Wildlife Afield 2(2): 51-57. Cabrera, M.R. (1998): Las tortugas continentales de Sudamérica Austral, 1st Edition. Córdoba, BR Copias. 108p. Cadi, A., Delmas, V., Preevot-Julliard, A.C., Joly, P., Pieaud, C., Girondot, M. (2004): Successful reproduction of the introduced slider turtle (Trachemy scripta elegans) in the South of France. Marcos Adriano Tortato et al. Aquatic Conservation: Marine and Freshwater Ecosystems 14(3): 237-246. CONSEMA (2010). Conselho Estadual de Meio Ambiente. Resolução CONSEMA Nº 11, de 17 de dezembro de 2010. Fagundes, C.K., Bager, A., Cechin, S.T.Z. (2010): Trachemys dorbigni in an anthropic environment in southern Brazil: II) Reproductive ecology. Herpetological Journal 20(3): 195-199. Ferronato, B.O., Marques, T.S., Guardia, I., Longo, A.L.B., Piña, C.I., Bertoluci, J., Verdade, L.M. (2009): The turtle Trachemys scripta elegans (Testudines, Emydidae) as an invasive species in a polluted stream of southeastern Brazil. Herpetological Bulletin 109: 29-34. Ficetola, G.F., Monti, A., Padoa-Schioppa, E. (2002): First record of reproduction of Trachemys scripta in the Po Delta. Annali del Museo Civico di Storia Naturale di Ferrara 5: 125-128. Ficetola, G.F., Thuiller, W., Padoa-Schioppa, E. (2009): From introduction to the establishment of alien species: bioclimatic differences between presence and reproduction localities in the slider turtle. Diversity and Distributions 15(1): 108–116. Fritz, U., Havas, P. (2007): Checklist of Chelonians of the World. Vertebrate Zoology 57(2): 149-368. Gonçalves, F.A., Cechin, S.T.Z., Bager, A. (2007): Predação de ninhos de Trachemys dorbigni (Duméril & Bibron) (Testudines, Emydidae) no extremo sul do Brasil. Revista Brasileira de Zoologia 24(4): 1063-1070. Hartmann, P.A., Giassom, L.O.M. (2008): Répteis. In: A fauna das áreas de influência da Usina Hidrelétrica de Quebra-Queixo, p.111-130. Cherem, J.J., Kammers, M., Eds, Erechim, Habilis. 192p. Ishiy, S.T., Nunes, A., Souza, A. de, Marterer, B.T.P., Brasil, D.M., Mussatto, E. (2009): Parque Estadual da Serra do Tabuleiro: retratos da flora e da fauna, 1st Edition. Florianópolis, criAG. 80p. Izquierdo, G.A., Del Cueto, F.F., Rodríguez-Pereira, A., Avia, M.L. (2010): Distribution records of non-native terrapins in Castilla and León region (Central Spain). Aquatic Invasions Records 5(3): 303-308. Kitowski, I., Pachol, D. (2009). Monitoring the trade turnover of red-eared terrapins (Trachemys scripta elegans) in pet shops of the Lublin Region, East Poland. North-Western Journal of Zoology 5(1): 34–39. Klein, M.R. (1981). Fisionomia, importância e recursos da vegetação do Parque Estadual da Serra do Tabuleiro. Sellowia 33: 5-54. Kopecký, O., Kalous, L., Patoka, J. (2013). Establishment risk from pet-trade freshwater turtles in the European Union. Knowledge and Management of Aquatic Ecosystems, (410). Krause, L., Gomes, N., Leyser, K.L. (1982): Observações sobre a nidificação e desenvolvimento de Chrysemys dorbigni (Duméril & Bibron, 1835) (Testudines, Emydinae) na Estação Ecológica do Taim, Rio Grande do Sul. Revista Brasileira de Zoologia 1(1): 79-90. Lema, T. (1994): Lista comentada dos répteis ocorrentes no Rio Grande do Sul, Brasil. Comunicações do Museu de Ciências e Tecnologia da PUCRS - Serie Zoologia 7: 41-150. Lema, T., Ferreira, M.T.S. (1990): Contribuição ao conhecimento dos Testudines do Rio Grande do Sul (Brasil) – Lista sistemática 15 Reproduction of two exotic species of Trachemys Agassiz, 1857 comentada (Reptilia). Acta Biologica Leopoldensia 12(1): 125164. Molina, F.B., Gomes, N. (1998a): Breeding and nesting behaviour of d’Orbigny’s slider turtle at São Paulo Zoo. International Zoo Yearbook 36: 162-170. Molina, F.B., Gomes, N. (1998b): Incubação artificial dos ovos e processo de eclosão em Trachemys dorbignyi (Duméril & Bibron) (Reptilla, Testudines, Emydidae). Revista Brasileira de Zoologia 15(1): 135-143. Moll, E.O., Legler, J.M. (1971): The life history of a Neotropical slider turtle, Pseudemys scripta (Schoepff), in Panamá. Bulletin of the Los Angeles County Museum of Natural History - Science 11: 1-102. O’Keeffe, S. (2009). The Practicalities of Eradicating Red-eared Slider Turtles (Trachemys scripta elegans). Alien: The Invasive Species Bulletin 28: 19-25. Perry, G., Owen, J.L., Petrovic, C., Lazell, J., Egelhoff J. (2007): The red-eared slider, Trachemys scripta elegans, in the British Virgin Islands. Applied Herpetology 4(1): 88-89. Pupins, M. (2007): First report on recording of the invasive species Trachemys scripta elegans, a potential competitor of Emys orbicularis in Latvia. Acta Universitatis Latviensis (723): 3746. Salera Jr., G., Malvasio, A., Portelinha, T.C.G. (2009): Avaliação da predação de Podocnemis expansa e Podocnemis unifilis (Testudines, Podocnemididae) no rio Javaés, Tocantins. Acta Amazonica 39(1): 207-214. Santos, T.G. dos, Kopp, K.A., Spies, M.R., Trevisan, R., Cechin, S. T.Z. (2005): Répteis do campus da Universidade Federal de Santa Maria, RS, Brasil. Biota Neotropica 5(1): 171-178. Santos, T.G. dos, Vasconcelos, T. da S., Molina, F. de B., Zaher H. (2009): First record of Trachemys dorbigni (Duméril & Bibron, 1835) (Testudines, Emydidae) in a remnant of Mesophytic Semideciduous Forest of São Paulo State, southeastern Brazil. Herpetological Bulletin 108: 27-30. Schneider, L., Ferrara, C.R., Vogt, R.C. (2009): Phrynops geoffroanus (Geoffroy’s side necked turtle). Nest predation. Herpetological Review 40(4): 436. Schneider, L., Ferrara, C.R., Vogt, R.C., Guilhon A.V. (2011): Nesting ecology and nest predation of Phrynops geoffroanus (Testudines, Chelidae) in the Guaporé River of the Brazilian and Bolivian Amazon. Chelonian Conservation and Biology 10(2): 206-212. Seidel, M.E. (2002): Taxonomic observations on extant species and subspecies of slider turtles, genus Trachemys. Journal of Herpetology 36(2): 285-292. Shiau, T.W., Hou, P.C., Wu, S.H., Tu, M.C. (2006): A survey on alien pet reptiles in Taiwan. Taiwania 51(2): 71-80. Silva-Soares, T., Ferreira, R.B., Salles, R.O.L., Rocha, C.F.D. (2011): Continental, insular and coastal marine reptiles from the municipality of Vitória, state of Espírito Santo, southeastern Brazil. Checklist 7(3): 290-298. Soorae, P.S., Quarqaz, M.A., Gardner, A.S. (2008): An overview and checklist of the native and alien herpetofauna of the United Arab Emirates. Herpetological Conservation and Biology 5(3): 529-536. Souza, V.L., Santos, T.M. dos, Peña, A.P., Luz, V.L.F., Reis, I.J. dos. (2007): Caracterização dos répteis descartados por mantenedores particulares e entregues ao Centro de Conservação e Manejo de Répteis e Anfíbios – RAN. Revista de Biologia Neotropical 4(2): 149-160. Tortato, M.A. (2007): Contribuição ao conhecimento de Phrynops hilarii (Duméril & Bibron, 1835) (Testudines, Chelidae) em área de restinga no estado de Santa Catarina, Sul do Brasil. Biotemas 20(1): 119-122. Van Dijk, P.P., Iverson, J.B., Shaffer, H.B., Bour, R., Rhodin, A.G.J. (2011): Turtles of the World, 2011 Update: Annotated Checklist of Taxonomy, Synonymy, Distribution, and Conservation Status. Chelonian Research Monographs (5): 165–242. Vanzolini, P.E. (1997): A note on the reproduction of Trachemys dorbigni (Testudines, Emydidae). Revista Brasileira de Biologia 57(2): 165-175. Vieira, C.S.; Costa, E.M.M. da. (2006). Análise da estrutura populacional de Trachemys scripta elegans (Chelonia) no Parque Ecológico Olhos D’Água - Brasília-DF. Universitas: Ciências da Saúde 4(1-2): 1-8. Waller, T., Chebez, J.C. (1987): Notas sobre las tortugas de la Provincia de Misiones, Argentina e inclusion de Phrynops williamsi Rhodin y Mittermeier, 1983 (Testudines, Chelidae) en la herpetofauna argentina. Historia Natural 7(5): 53-59. Zaher, H., Barbo, F.E., Martínez, P.S., Nogueira, C., Rodrigues, M.T., Sawaya, R.J. (2011): Répteis do Estado de São Paulo: conhecimento atual e perspectivas. Biota Neotropica 11(1a): http://www.biotaneotropica.org.br/v11n1a/en/abstract?inventor y+bn0051101a2011. Accepted by Mirco Solé