The presence of the Red-eared slider, Trachemys scripta elegans ...

5
Trachemys scripta elegans (Wied, 1838) is a freshwater turtle that occurs in the Mississippi Valley, USA (Ernst & Lovich, 2009). Due to the vivid colored shell of hatchlings, the species was introduced in the animal pet trade in the 1950s and rapidly became the most commonly sold turtle all over the world (Franke & Telecky, 2001; Ernst & Lovich, 2009). Statistics are impressive with about 52 million specimens exported from USA during the 1989-1997 years and more than 23 million during the 1998-2002 years (Franke & Telecky, 2001; Schlaepfer, Hoover and Dodd Jr., 2005). It is a medium sized species; adult males and females can attain, respectively, 20 and 28 cm of carapace length (Ernst & Lovich, 2009). This is one of the reasons that sooner or later almost all turtle “owners” release their animals somewhere from city parks to natural environments (Ferronato et al., 2009; F. B. Molina personal observation). Invasive species are a matter of concern because they can impact native species through competitive exclusion, niche displacement, hybridization, introgression, predation and even extinction (Mooney & Cleland, 2001). Trachemys s. elegans is a generalist species with broad ecological niche (Ernst & Lovich, 2009) that has been introduced in many countries in Europe (Cadi & Joly, 2004; Pupins, 2007), Africa (Baard & Villiers, 2000), Asia (Haramura, Yamane and Mori, 2008; Xu et al., 2012), Oceania (Burgin, 2006; Feldman, 2007), North America (Townsend et al., 2002; Thomson, Spinks and Shaffer, 2010), Central America (Powell, 2005), and South America (Iriarte, Lobos and Jaksic, 2005; Alcalde et al., 2012). It can compete with local species (Cadi & Joly, 2004; Polo-Cavia, López and Martín, 2008, 2011) and can transmit bacteria (Hidalgo-Vila et al., 2008) and worms (Verneau et al., 2011) to them. It is included among top 100 world’s worst invasive alien species (Lowe et al., 2000). In Brazil, the commercialization of T. s. elegans is forbidden since 1998 (Magalhães & São-Pedro, 2012). Nevertheless, the species was already detected as an invasive organism in many municipalities of the states of São Paulo (Molina, 2006; Barbo, 2008; Ferronato et al., 2009; Cristino, 2013), Rio de Janeiro (Salles & Silva-Soares, 2010), Espírito Santo (Silva-Soares et al., 2011), Minas Gerais (H. C. Costa, personal communication), Paraná (Instituto Horus, 2005), Santa Catarina (Tortato, Bressan and Kunz, 2014), Rio Grande do Sul (Quintela, Loebmann and Gianuca, 2006; Bujes, 2011), Mato Grosso do Sul (Instituto Horus, 2005), Goiás (Instituto Horus, 2005), Distrito Federal (Horta, 2004; Vieira & Costa, 2006), Tocantins (Instituto Horus, 2005) and Amazonas (Instituto Horus, 2005). Almost nothing is known about its population status in Brazilian ecosystems. In the morning of July 08 2013, one of us (RAM) observed a melanistic male T. s. elegans in a pond watered by a creek that runs from Paraibuna reservoir, in a private property close to the 53 rd km of Tamoios highway, in the municipality of Paraibuna, state of São Paulo, Brazil (−23.511619°; −45.547192°; figure 1). Herpetology Notes, volume 7: 437-441 (2014) (published online on 5 July 2014) The presence of the Red-eared slider, Trachemys scripta elegans (Wied, 1838) (Testudines, Emydidae), an invasive species, in the Paraibuna river basin, Southeastern Brazil Renato Augusto Martins 1 , André Moreira Assalim 1 and Flavio de Barros Molina 2,3, * 1 Instituto Biovida para Conservação da Biodiversidade. Rua Gentil Moreira, 147, Centro, CEP 16370-000, Promissão, SP, Brasil 2 Museu de Zoologia da Universidade de São Paulo. Av. Nazaré 481, Ipiranga, CEP 04263-000, São Paulo, SP, Brasil 3 Universidade de Santo Amaro, Campus I, Rua Prof. Enéas de Siqueira Neto 340, Jardim das Imbuias, CEP 04829-300, São Paulo, SP, Brasil * Corresponding author e-mail: [email protected]

Transcript of The presence of the Red-eared slider, Trachemys scripta elegans ...

Page 1: The presence of the Red-eared slider, Trachemys scripta elegans ...

Trachemys scripta elegans (Wied, 1838) is a freshwater turtle that occurs in the Mississippi Valley, USA (Ernst & Lovich, 2009). Due to the vivid colored shell of hatchlings, the species was introduced in the animal pet trade in the 1950s and rapidly became the most commonly sold turtle all over the world (Franke & Telecky, 2001; Ernst & Lovich, 2009). Statistics are impressive with about 52 million specimens exported from USA during the 1989-1997 years and more than 23 million during the 1998-2002 years (Franke & Telecky, 2001; Schlaepfer, Hoover and Dodd Jr., 2005).

It is a medium sized species; adult males and females can attain, respectively, 20 and 28 cm of carapace length (Ernst & Lovich, 2009). This is one of the reasons that sooner or later almost all turtle “owners” release their animals somewhere from city parks to natural environments (Ferronato et al., 2009; F. B. Molina personal observation). Invasive species are a matter of concern because they can impact native species through competitive exclusion, niche displacement, hybridization, introgression, predation and even extinction (Mooney & Cleland, 2001). Trachemys s. elegans is a generalist species with broad ecological niche (Ernst & Lovich, 2009) that has been introduced

in many countries in Europe (Cadi & Joly, 2004; Pupins, 2007), Africa (Baard & Villiers, 2000), Asia (Haramura, Yamane and Mori, 2008; Xu et al., 2012), Oceania (Burgin, 2006; Feldman, 2007), North America (Townsend et al., 2002; Thomson, Spinks and Shaffer, 2010), Central America (Powell, 2005), and South America (Iriarte, Lobos and Jaksic, 2005; Alcalde et al., 2012). It can compete with local species (Cadi & Joly, 2004; Polo-Cavia, López and Martín, 2008, 2011) and can transmit bacteria (Hidalgo-Vila et al., 2008) and worms (Verneau et al., 2011) to them. It is included among top 100 world’s worst invasive alien species (Lowe et al., 2000).

In Brazil, the commercialization of T. s. elegans is forbidden since 1998 (Magalhães & São-Pedro, 2012). Nevertheless, the species was already detected as an invasive organism in many municipalities of the states of São Paulo (Molina, 2006; Barbo, 2008; Ferronato et al., 2009; Cristino, 2013), Rio de Janeiro (Salles & Silva-Soares, 2010), Espírito Santo (Silva-Soares et al., 2011), Minas Gerais (H. C. Costa, personal communication), Paraná (Instituto Horus, 2005), Santa Catarina (Tortato, Bressan and Kunz, 2014), Rio Grande do Sul (Quintela, Loebmann and Gianuca, 2006; Bujes, 2011), Mato Grosso do Sul (Instituto Horus, 2005), Goiás (Instituto Horus, 2005), Distrito Federal (Horta, 2004; Vieira & Costa, 2006), Tocantins (Instituto Horus, 2005) and Amazonas (Instituto Horus, 2005). Almost nothing is known about its population status in Brazilian ecosystems.

In the morning of July 08 2013, one of us (RAM) observed a melanistic male T. s. elegans in a pond watered by a creek that runs from Paraibuna reservoir, in a private property close to the 53rd km of Tamoios highway, in the municipality of Paraibuna, state of São Paulo, Brazil (−23.511619°; −45.547192°; figure 1).

Herpetology Notes, volume 7: 437-441 (2014) (published online on 5 July 2014)

The presence of the Red-eared slider, Trachemys scripta elegans (Wied, 1838) (Testudines, Emydidae), an invasive species,

in the Paraibuna river basin, Southeastern Brazil

Renato Augusto Martins1, André Moreira Assalim1 and Flavio de Barros Molina2,3,*

1 Instituto Biovida para Conservação da Biodiversidade. Rua Gentil Moreira, 147, Centro, CEP 16370-000, Promissão, SP, Brasil

2 Museu de Zoologia da Universidade de São Paulo. Av. Nazaré 481, Ipiranga, CEP 04263-000, São Paulo, SP, Brasil

3 Universidade de Santo Amaro, Campus I, Rua Prof. Enéas de Siqueira Neto 340, Jardim das Imbuias, CEP 04829-300, São Paulo, SP, Brasil

* Corresponding author e-mail: [email protected]

Page 2: The presence of the Red-eared slider, Trachemys scripta elegans ...

During the rainy season, from November to February, the creek overflows and connects with the pond forming a possible water course for turtle dispersal (figure 2). Paraibuna reservoir has a maximum surface area of 224 km², a maximum depth of 98m, and is formed by the waters of Paraibuna and Paraitinga rivers (Dias et al., 2005). It is part of the Paraiba do Sul river basin that runs toward the Atlantic Ocean and is situated between the cities of São Paulo and Rio de Janeiro, the most populated areas in Brazil. Although Paraiba do Sul river valley is highly impacted by anthropogenic activities, presenting margins dominated by grasses, Paraibuna and Paraitinga rivers, that drain Bocaina Plateau, are better preserved with margins covered mainly by shrubs and trees (Pinto et al., 2009).

The specimen showed intense ontogenetic melanism (Lovich, McCoy and Garstka, 1990) and had elongated front claws. It was measured with a caliper (210 mm of

Renato Augusto Martins et al.438

Figure 1. Map showing the location (red dot) of the pond where a male of Trachemys scripta elegans was seen in the municipality of Paraibuna, state of São Paulo, southeastern Brazil.

Figure 2. Pond where one adult male of Trachemys scripta elegans was observed in the municipality of Paraibuna, state of São Paulo, southeastern Brazil. The yellow arrow shows the pond and the red arrow shows one arm of Paraibuna reservoir. The white line refers to the water course between the reservoir and the pond (satellite image downloaded with Google Earth, captured on January 6, 2014).

Page 3: The presence of the Red-eared slider, Trachemys scripta elegans ...

The presence of the invasive Trachemys scripta elegans in Southeastern Brazil 439

carapace length, 160 mm of carapace width, and 170 mm of plastron length), weighed with a dynamometer (910 g), photographed (figure 3) and released.

To check the possible existence of a turtle population in the area, the four local residents (a 65 and a 40 year old men, a 35 year old woman, and an 11 year old girl) were interviewed. According to them, adult and young red-eared slider turtles (ca. 5 to 20 cm of carapace length) are commonly seen in local ponds and creeks watered by the reservoir. We can be sure that they correctly identified the species because native fauna is composed only of side-necked turtle species. The eldest resident interviewed dated their presence to twenty years ago. According to him, the animals are seen mainly during December and January, a period that correspond to the end of spring and beginning of summer in south hemisphere. At São Paulo Zoo, located about 110 km to the west, T. s. elegans was seen successfully nesting in outside exhibits from September to February (F. B. Molina, personal observation).

The possible presence of a Trachemys scrita elegans population in the Paraibuna reservoir could represent a threat to local species, such as Phrynops geoffroanus (Schweigger, 1812) and Hydromedusa tectifera Cope,

1869. As aquatic macroinvertebrates and fishes are important items in their diet (Souza & Abe, 2000; Bonino et al., 2009; Ernst & Lovich, 2009; Alcalde, Derocco and Rosset, 2010; Deconte, 2012), the occurrence of feeding niche displacement and even competitive exclusion cannot be ruled out.

It is also important to consider that this place is situated not far from upper Paraiba do Sul river (ca. 20km south), where the endangered chelid turtle Mesoclemmys hogei (Mertens, 1967) is found in the middle and lower course (Drummond & Molina, 2008), and from the Parque Estadual da Serra do Mar (ca. 10 km north), the largest continuous extension of Atlantic Rain Forest (a hotspot) preserved in Brazil (Instituto Florestal, 2008), and an important habitat of Hydromedusa maximiliani (Mikan, 1820) and H. tectifera (Marques & Sazima, 2004; Famelli et al., 2011).

There is therefore an urgent need for conservation measures. We agree with the suggestions made by Ferronato et al. (2009), especially the need to develop research on the impact of Trachemys scripta elegans on Neotropical freshwater turtles and to establish a control program designed to remove alien turtle specimens from natural environments.

Figure 3. Melanistic adult male of Trachemys scripta elegans observed in a pond in the municipality of Paraibuna, state of São Paulo, southeastern Brazil (photo by Renato A. Martins).

Page 4: The presence of the Red-eared slider, Trachemys scripta elegans ...

Acknowledgements. We would like to thank the companies Ecologic – Centro de Avaliações e Perícias Ambientais and DERSA – Desenvolvimento Rodoviário S.A., for supporting the work and contributing financially. We also thank Bruno de Oliveira Ferronato and three anonymous reviewers for commenting the manuscript.

References

Alcalde, L., Derocco, N.N., Rosset, S.D. (2010): Feeding in syntopy: Diet of Hydromedusa tectifera and Phrynops hilarii (Chelidae). Chelonian Conservation and Biology 9: 33-44.

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: 128-133.

Baard, E.H.W., De Villiers, A.L. (2000): State of biodiversity: Western Cape Province, South Africa Amphibians and Reptiles. In: Western Cape State of Biodiversity 2000, p. 1-31. Stellenbosch, Western Cape Conservation Board.

Barbo, F.E. (2008): Os répteis no município de São Paulo: aspectos históricos, diversidade e conservação. In: Além do Concreto: Contribuições para a Proteção da Biodiversidade Paulistana, p. 234-267. Malagoli, L.R., Bajestero, F.B., Whately, M., Eds., São Paulo, Editora Instituto Socioambiental.

Bonino, M.F., Lescano, J.N., Haro, J.G., Leynaud, G.C. (2009): Diet of Hydromedusa tectifera (Testudines-Chelidae) in a mountain stream of Córdoba province, Argentina. Amphibia-Reptilia 30: 545-554.

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): 14-18.

Burgin, S. (2006): Confirmation of an established population of exotic turtles in urban Sydney. Australian Zoologist 33(3): 379-384.

Cadi, A., Joly, P. (2004): Impact of the introduction of the red-eared slider (Trachemys scripta elegans) on survival rates of the European pond turtle (Emys orbicularis). Biodiversity and Conservation 13: 2511-2518.

Cristino, L.G. (2013): Fôlego de tartaruga. Unesp Ciência (42): 36-41.

Deconte, M.R. (2012): Impacto antrópico na dieta do cágado-de-barbicha, Phrynops geoffroanus (Testudines, Chelidae) no rio Uberabinha, Uberlândia, Minas Gerais. Unpublished MSc thesis, Universidade Federal de Uberlândia, Uberlândia, 49 pp.

Dias, N.W., Batista, G.T., Targa, M.S., Catelani, C.S. (2005): Análise da carga de sedimentos da represa de Paraibuna com base em dados multiespectrais. In: XVI Simpósio Brasileiro de Recursos Hídricos, p. 1-17. João Pessoa, ABRH.

Drummond, G.M., Molina, F.B. (2008): Phrynops hogei Mertens, 1967. In: Livro Vermelho da Fauna Brasileira Ameaçada de Extinção, V.2, p. 355-357. Machado, A.B.M., Drummond, G.M., Paglia, A.P., Eds., Brasília, DF, Ministério do Meio Ambiente/Belo Horizonte, Fundação Biodiversitas.

Ernst, C.H., Lovich, J.E. (2009): Turtles of the United States and Canada. Baltimore, Johns Hopkins University Press.

Famelli, S., Bertoluci, J., Molina, F.B., Matarazzo-Neuberger, W.M. (2011): Structure of a population of Hydromedusa maximiliani (Testudines, Chelidae) from Parque Estadual da Serra do Mar, an Atlantic rainforest preserve in Southeastern Brazil. Chelonian Conservation and Biology 10(1): 132-137.

Feldman, M.L. (2007): The Red-eared slider turtle (Trachemys scripta elegans) in New Zealand. Turtle and Tortoise Newsletter (10): 15-18.

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.

Franke, J., Telecky, T.M. (2001): Reptiles as Pets: An Examination of the Trade in Live Reptiles in the United States. Washington, The Humane Society of the United States.

Haramura, T., Yamane, M., Mori, A. (2008): Preliminary survey on the turtle community in a lotic environment of the Kizu River. Current Herpetology 27(2): 101-108.

Hidalgo-Vila, J., Díaz-Paniagua, C., Pérez-Santigosa, N., de Frutos-Escobar, C., Herreo-Herrero, A. (2008): Salmonella in free-living exotic and native turtles and in pet exotic turtles from SW Spain. Research in Veterinary Science 85: 449-452.

Horta, G.F. (2004): Levantamento de espécies de quelônios semi-aquáticos no Parque Olhos D’Água. Unpublished BSc thesis, Centro Universitário de Brasília, Brasília, 29 pp.

Instituto Florestal (2008): Plano de Manejo do Parque Estadual da Serra do Mar. Secretaria do Estado do Meio Ambiente, São Paulo, SP.

Instituto Horus de Desenvolvimento e Conservação Ambiental. (2005): Trachemys scripta. Available at: http://www.institutohorus.org.br/index.php?modulo=inf_ficha_trachemys_scripta. Last accessed on 2 September 2013.

Iriarte, J.A., Lobos, G.A., Jaksic, F.M. (2005): Invasive vertebrate species in Chile and their control and monitoring by governmental agencies. Revista Chilena de Historia Natural 78: 143-154.

Lovich, J.E., McCoy, C.J., Garstka, W.R. (1990): The development and significance of melanism in the slider turtle. In: Life history and ecology of the slider turtle, p. 233-254. Gibbons, J.W., Ed., Washington, D.C., Smithsonian Institution Press.

Lowe, S., Browne, M., Boudjelas, S., De Poorter, M. (2000): 100 of the world’s worst invasive alien species – a selection from the global invasive species database. The Invasive Species Specialist Group (ISSG) of the Species Survival Commission (SSC). World Conservation Union (IUCN). Available at http://www.issg.org/database/species/reference_files/100English.pdf. Last accessed on 29 August 2013.

Magalhães, A.L.B., São-Pedro, V.A. (2012): Illegal trade on non-native amphibians and reptiles in southeast Brazil: The status of e-commerce. Phyllomedusa 11(2) 155-160.

Marques, O.A.V., Sazima, I. (2004): História natural dos répteis da Estação Ecológica Juréia-Itatins. In: Estação Ecológica Juréia-Itatins: Ambiente físico, flora e fauna, p. 257-277. Marques, O. A. V., Duleba, W., Eds., Ribeirão Preto, Holos Editora.

Molina, F.B. (2006): Ambientes urbanos e a fauna de répteis no Estado de São Paulo: entre desconhecidos, desaparecidos e indesejáveis. In: Parques urbanos e meio ambiente: desafios

Renato Augusto Martins et al.440

Page 5: The presence of the Red-eared slider, Trachemys scripta elegans ...

de uso, p. 203-222. Glezer, R., Mantovani, M.S.M., Orgs., São Paulo, Parque Cientec/USP.

Mooney, H.A., Cleland, E.E. (2001): The evolutionary impact of invasive species. Proceedings of the National Academy of Science of the United States of America 98(10): 5446-5451.

Quintela, F.M., Loebmann, D., Gianuca, N.M. (2006): Répteis continentais do município de Rio Grande, Rio Grande do Sul, Brasil. Biociências 14(2): 180-188.

Pinto, B.C.T., Araújo, F.G., Rodrigues, V.D., Hughes, R.M. (2009): Local and ecoregion effects on fish assemblage structure in tributaries of the Rio Paraíba do Sul, Brazil. Freshwater Biology 54: 2600-2615.

Polo-Cavia, N., López, P., Martín, J. (2008): Interspecific differences in responses to predation risk may confer competitive advantages to invasive freshwater turtle species. Ethology 114: 115-123.

Polo-Cavia, N., López, P., Martín, J. (2011): Aggressive interactions during feeding between native and invasive freshwater turtles. Biological Invasions 13: 1387-1396.

Powell, M.A. (2005): Mayan reptiles. Iguana 12(2): 112-122.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: 37-46.

Salles, R.O.L., Silva-Soares, T. (2010): Répteis do município de Duque de Caxias, Baixada Fluminense, Rio de Janeiro, Sudeste do Brasil. Revista Biotemas 23(2): 135-144.

Schlaepfer, M.A., Hoover, C., Dodd Jr., C.K. (2005): Challenges in evaluating the impact of the trade in amphibians and reptiles on wild populations. BioScience 55(3): 256-264.

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. Check List 7(3): 290-298.

Souza, F.L., Abe, A.S. (2000): Feeding ecology, density and biomass of the freshwater turtle, Phrynops geoffroanus, inhabiting a polluted urban river in south-eastern Brazil. Journal of Zoology 252: 437-446.

Thomson, R.C., Spinks, P.Q., Shaffer, H.B. (2010): Distribution and abundance of invasive Red-eared sliders (Trachemys scripta elegans) in California’s Sacramento River Basin and possible impacts on native western pond turtles. Chelonian Conservation and Biology 9(2): 297-302.

Tortato, M.A., Bressan, R.F., Kunz, T.S. (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. Herpetology Notes 7: 11-15.

Townsend, J.H., Krysko, K.L., Reppas, A.T., Sheehy III, C.M. (2002): Noteworthy records for introduced reptiles and amphibians from Florida, USA. Herpetological Review 33(1): 75.

Verneau, O., Palacios, C., Platt, T., Alday, M., Billard, E., Allienne, J.F., Basso, C., Du Preez, L.H. (2011): Invasive species threat: Parasite phylogenetics reveals patterns and processes of host-switching between non-native and native captive freshwater turtles. Parasitology 138: 1778-1792.

Vieira, C.S., Costa, E.M.M. (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.

Xu, H., Qiang, S., Genovesi, P., Ding, H., Wu, J., Meng, L., Han, Z., Miao, J., Hu, B., Guo, J., Sun, H., Huang, C., Lei, J., Le, Z., Zhang, X., He, S., Wu, Y., Zheng, Z., Chen, L., Jarošík, V., Pyšek, P. (2012): An inventory of invasive alien species in China. NeoBiota 15: 1-26.

Accepted by Diogo Provete; associate editor: Spartak Litvinchuk

The presence of the invasive Trachemys scripta elegans in Southeastern Brazil 441