First Reproduction Report of Trachemys Scripta in Portugal Ria Formosa Natural Park, Algarve

Home , Emys, European pond turtle, Pseudemys, Trachemys

Limnetica, 37 (1): 61-67(2018). DOI: 10.23818/limn.37.06 © Asociación Ibérica de Limnología, Madrid. Spain.ISSN: 0213-8409

First reproduction report of Trachemys scripta in Portugal Ria Formosa Natural Park, Algarve

Bruno Herlander Martins1,*, Fábia Azevedo2 and José Teixeira1,3

1 CIBIO - UP / InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto. Campus Agrário de Vairão, 4485-661 Vairão, Portugal. 2 RIAS - ALDEIA, Centro de Recuperação e Investigação de Animais Selvagens. Parque Natural da Ria Formosa, 8700 Quelfes-Olhão, Portugal. 3 CIIMAR - Interdisciplinary Centre of Marine and Environmental Research. Rua dos Bragas, 289, 4050-123 Porto, Portugal.

* Corresponding author: [email protected]

Received: 04/02/15 Accepted: 10/08/17

ABSTRACT First reproduction report of Trachemys scripta in Portugal - Ria Formosa Natural Park, Algarve We report the widespread occurrence of Trachemys scripta at Ria Formosa Natural Park, in sympatric conditions with native populations of Emys orbicularis and Mauremys leprosa, and the first confirmed case of successful reproduction in Portugal. The continuous naturalization reports of this invasive species, whose distribution has expanded worldwide in the last decades, confirm the need to implement urgent management measures for nature conservation, especially given the vulnerability of Emys orbicularis populations. Key words: invasive species, Portugal, reproduction, Trachemys scripta

RESUMO Primeiro relatório da reprodução de Trachemys scripta em Portugal – Parque Natural da Ria Formosa, Algarve Neste trabalho apresenta-se evidências sobre a ocorrência generalizada de Trachemys scripta no Parque Natural da Ria Formosa, em condições simpátricas com populações nativas de Emys orbicularis e Mauremys leprosa, e o primeiro caso confirmado de reprodução com sucesso em Portugal. A contínua naturalização com sucesso desta espécie invasora, cuja sua distribuição tem vindo a aumentar por todo o mundo nas últimas décadas, confirma a necessidade de implementação de medidas de gestão urgentes para a conservação da natureza, especialmente dada a vulnerabilidade das populações de Emys orbicularis. Palavras chave: espécies invasoras, Portugal, reprodução, Trachemys scripta 62 Martins et al.

INTRODUCTION of its range (IUCN, 2014), and is therefore Lourenço (19.6 hectares), Quinta do Lago (1.5 signs were higher. This dog was trained during protected by European legislation (Cox & hectares), Dunas Douradas (1 hectares) and the LIFE Trachemys project, with the help of a The introduction of exotic species, and subse- Temple, 2009) and subject of numerous conser- Garrão (0.82 hectares), located along a 5 km specialized dog trainer, to detect eggs, juveniles quent competitive interactions between these vation projects (e.g. Cadi & Miquet, 2004; costal stretch in the Loulé council. The trapping or adult Trachemys specimens. species and the native fauna, are identified as Lacomba & Sancho, 2004; Ducotterd et al., 2008; techniques used were nine floating traps checked All captured individuals were measured, important drivers for global loss of biodiversity Schweitzer et al., 2008; Fritz & Chiari, 2013; once a week, fourteen hoop traps checked every weighed and numbered with a four numerical (Primack, 1997; Mooney et al., 2005; Hulme et Teixeira et al., 2013). In Portugal there are rising two days and hand nets whenever it was appropri- code, unique to each individual, which was placed al., 2009; Butchart et al., 2010). The slider turtle, concerns about this species, since E. orbicularis ate. All traps were distributed according to the on the marginal plates of the carapace through Trachemys scripta, native to the eastern and is considered Endangered (Cabral et al., 2005) size and shape of the water bodies, in order to notches realized with a small saw. The carapace central United States of America, is considered and coexists with the native Mediterranean pond evenly cover their entire area, giving six floating length and carapace width were measured using a one of the world´s worst invasive alien species turtle Mauremys leprosa, which may increase traps and six hoop traps at São Lourenço, two caliper (precision: 0.1 mm) and the weight was (Lowe et al., 2000). The main cause of introduc- their spatial segregation (Segurado & Figueiredo, floating traps and three hoop traps at Quinta do recorded with a precision scale (precision: 0.1 g). tion into the wild stems from their massive trade 2007). So the early detection of T. scripta occur- Lago, one floating trap and three hoop traps at All the invasive species individuals were identi- as pets over the last decades, from turtle farms in rence and the confirmation of its reproduction in Dunas Douradas and two hoop traps at Garrão. fied following Ernst & Lovich, 2009 and LIFE the USA to foreign markets (Telecky, 2001). Until new locations are key factors to the efficient The floating traps were placed in deeper areas Trachemys, 2012 and delivered on Official recently, they were legally sold in Europe as development and implementation of adequate where there were a greater number of individuals Reception Centers. Here, whenever evidence of hatchlings (3-4 cm carapace length), and their conservation measures and will contribute to in thermoregulation or in areas with few supports eggs development were detected by inguinal owners are rarely prepared to maintain them in raise the public awareness about this problematic for thermoregulation. The hoop traps were placed palpation, females were radiographed. All E. captivity when they start to grow (reaching up to situation. on the border of the water bodies in areas where orbicularis and M. leprosa individuals were 30 cm carapace length). This common situation In Portugal, at Ria Formosa Natural Park the activity of individuals was higher and the trap immediately released at the capture site, after leads to frequent releases of these animals in the (PNRF) where M. leprosa and E. orbicularis could be conveniently hide. Adding to that, in being given the individual code. wild, resulting in the introduction and establish- populations coexist, T. scripta are sympatric. This order to evaluate the occurrence and abundance ment of many T. scripta populations into different area is populated with high densities of M. leprosa of T. scripta individuals throughout the PNRF RESULTS natural freshwater ecosystems. and contains one of the most important Portuguese area, visual surveys were performed every month, Currently this turtle has been reported as populations of E. orbicularis (Cabral et al., 2005), during the three years, around the main water During the study period, we captured in the four introduced into the wild outside its natural range therefore, it has been implemented a conservation bodies and streams along the Natural Park. wetlands where the trapping techniques were throughout all continents: Europe (Luiselli et al., project in the region in this regard (LIFE Trache- Lastly, in July of 2013, an intensive search with a implemented a total of 259 individuals of differ- 1997; Miranda & Leunda, 2010), Africa (New- mys - LIFE09 NAT/ES/000529). Here we report detection dog was conducted to detect nests ent freshwater turtle invasive species, with 99 berry, 1984), Asia (Chen & Lue, 1998), Oceania the widespread occurrence at PNRF and the first around the São Lourenço wetland, where nesting individuals being captured during the first year, (Burgin, 2006) and America (Thomson et al., confirmed case of successful reproduction of T. 2010). Once introduced, the main requirement for scripta in the wild, in Portugal. its invasion is the occurrence of successful reproduction. Therefore, firm evidence about its repro- MATERIALS AND METHODS duction is a key step towards understanding and managing its possible impacts on the invaded The Ria Formosa Natural Park (PNRF), located in ecosystem (Herbold & Moyle, 1986). Neverthe- the Algarve Region (South Portugal), is a protect- less, during the last decade T. scripta has been ed area including a 60 km stretch of the Algarve confirmed to reproduce in several European coastline and occupies an area of about 18 400 countries, namely in different Mediterranean hectares. Especially important because of its countries such as Italy (Ficetola et al., 2003), biological richness, it has the status of a Natural France (Cadi et al., 2004) and Spain (Pérez-Santi- Park and is classified by the Ramsar Convention gosa et al., 2008). as a wetland of international interest. In Europe, T. scripta has been reported to From 2011 to 2013, between March and compete with native turtle species for basking November, when the freshwater turtles activity is places and food (Cadi & Joly, 2003; 2004; higher (Lebboroni & Chelazzi, 1991; Cadi & Pérez-Santigosa et al., 2011). This situation is Joly, 2000), a set of permanent trapping particularly alarming for the European pond turtle techniques were implemented along four Emys orbicularis, which is considered as near wetlands of special interest for the presence of E. threatened and in sharp decline in several regions orbicularis and M. leprosa populations: São

Limnetica, 37(1): 61-67 (2018)

contained 15 T. s. elegans eggs that we removed constant recruitment from the surroundings. The et al., 1997), Italy (Ficetola et al., 2003) and to prevent their future hatchling. For all the other results of the surveys performed throughout the France (Cadi et al., 2004), the confirmed repro- 10 females, the X-rays revealed 17 eggs on aver- three years on the study area, support the idea of a duction of T. scripta at Ria Formosa Natural Park age (minimum 15/maximum 21). wider distribution of the population that can in Portugal reinforces the possibility of perma- The surveys performed throughout all the provide the conditions for a successful naturaliza- nent establishment of this species within all the Natural Park area confirmed the permanent tion. Adding to that, the high number of captured Mediterranean region. This data enhances the presence of T. scripta populations scattered all hatchlings, still with the presence of umbilical urgent need to strengthen the European legisla- over the Natural Park during the three years and scar and absence of growing rings, suggest the tion, banning the trade of all T. scripta subspecies, all the estimates of observed individuals indicated existence of successful reproduction, since they trade control and population management by the constant occurrence of hundreds of individu- all are smaller than the mean for T. scripta hatch- promoting an European Invasion Alert Network als (adults and juveniles) each year. lings described by Janzen et al. (2000). Further- and early eradication campaigns from natural The detection dog was used for testing 4 sites, more, hundreds of individuals of both gender and wetlands. identified as more suitable for nesting near the different ages captured and observed throughout border of São Lourenço wetland, in a total of the PNRF, as well as the several adult egg-bearing ACKNOWLEDGMENTS approximately 2 hectares, with 2 visits of 1 females encountered near nesting sites, support hour/per site. One nest of T. s. elegans was detect- the idea that they were able to adapt to the natural This research was supported by the LIFE Trache- ed, at the same area where most of the newly conditions and to establish successfully. This mys project (LIFE09 NAT/ES/000529). We thank hatched nests and a female nesting during the situation increases the direct competition with DogAlgarve, especially the dog trainer Américo spring were already encountered. The nest native turtles, adding a new disturbance factor Lopes and everyone who helped in the fieldwork, contained 14 eggs with newly hatched T. s. and increasingly restricting the places where they especially Thijs Valkenburg, Tiago Ventura, Mauro elegans and some still hatching, that we also occur naturally and the invasion process has not Hilário, Jael Palhas and António Cotão. removed immediately. occurred yet. Lastly, the use of a detection dog for reproduction evidence, even it has not been used REFERENCES 81 during the second year and 79 during the third DISCUSSION extensively, showed certain success, giving the year (Fig. 1). At the same time, we captured a location of one nest that provided evidence of BURGIN, S. 2006. Confirmation of an estab- total of 341 different individuals of E. orbicularis Our study showed that T. scripta occurs in high reproduction of T. scripta and confirmed the lished population of exotic turtles in urban and 2286 of M. leprosa, with 156 E. orbicularis densities in the study area and confirmed for the promising application of this technique, initially Sydney. Australian Journal of Zoology, 33, and 1487 M. leprosa being captured in the first first time the reproduction of this species in developed in Australia by the Queensland Depart- 379-384. DOI: 10.7882/AZ.2006.011 year, 141 E. orbicularis and 531 M. leprosa in the Portugal. The high number of captured and ment of Natural Resources (O’Keeffe, 2005). BUTCHART, S. H. M., M. WALPOLE, B. second year and 44 E. orbicularis and 268 M. removed individuals from natural conditions, These results are alarming and represent a COLLEN, A. VAN STRIEN, J. P. W. leprosa in the third year (Fig. 1). From all the repeatedly over the three years of study, reveals viable invasive population, co-occurring with SCHARLEMANN, R. E. A. ALMOND, J. E. captured invasive species individuals, 253 where an established population and the occurrence of important native populations of E. orbicularis. M. BAILLIE, B. BOMHARD, C. BROWN, J. from different sub-species of T. scripta, especial- Without an intensive control and population man- BRUNO, K. E. CARPENTER, G. M. CARR, ly T. s. elegans (n=236), but also T. s. scripta agement, this situation can lead to a massive and J. CHANSON, A. M. CHENERY, J. CSIRKE, (n=8), T. s. troosti (n=1) and hybrids between T. s. widespread naturalization of this species, with N. C. DAVIDSON, F. DENENER, M. elegans and T. s. scripta (n=8) (Fig. 2). The irreversible negative impacts on native fauna and FOSTER, A. GALLI, J. N. GALLOWAY, P. remaining individuals were Pseudemys concinna on the ecosystem functioning, similarly to what GENOVESI, R. D. GREGORY, M. HOCK- (n=3), Pseudemys nelsoni (n=2) and Graptemys has been observed in other areas throughout INGS, V. KAPOS, J. F. LAMARQUE, F. pseudogeographica (n=1) (Fig. 2). Overall, from Europe (Cadi et al., 2004; Pérez-Santigosa et al., LEVERINGTON, J. LOH, M. A. MCGEOCH, the captured sample, most individuals were 2008). L. MCRAE, A. MINASYAN, M. H. MOR- breeding adults, especially females, together with Although T. scripta is very common and CILLO, T. E. E. OLDFIELD, D. PAULY, S. a high number of juveniles and some hatchlings popular as a pet, its invasive status and impact on QUADER, C. REVENGA, J. R. SAUER, B. (Table 1). All hatchlings had the umbilical scar on local ecosystems and native species are still SKOLNIK, D. SPEAR, D. STAN- the middle of their plastron and none had growing unknown for the general public. The evidence of WELL-SMITH, S. N. STUART, A. SYMES, rings on the carapace. Among all the adult successful reproduction and establishment by this M. TIERNEY, T. D. TYRRELL, J. C. VIÉ & females captured, 11 T. s. elegans were egg-bear- species in the study area might be a first sign to R. WATSON. 2010. Global Biodiversity: ing females, identified by palpation, including help rising public awareness for this problem. Indicators of Recent Declines. Science, 328: one that was already covering the nest, near the Together with the successful reproduction 1164-1168. DOI: 10.1126/science.1187512 border of São Lourenço wetland. The nest reports of T. scripta in Spain (Martinez-Silvestre CABRAL, M. J., J. ALMEIDA, P. R. ALMEI-

INTRODUCTION of its range (IUCN, 2014), and is therefore Lourenço (19.6 hectares), Quinta do Lago (1.5 signs were higher. This dog was trained during protected by European legislation (Cox & hectares), Dunas Douradas (1 hectares) and the LIFE Trachemys project, with the help of a The introduction of exotic species, and subse- Temple, 2009) and subject of numerous conser- Garrão (0.82 hectares), located along a 5 km specialized dog trainer, to detect eggs, juveniles quent competitive interactions between these vation projects (e.g. Cadi & Miquet, 2004; costal stretch in the Loulé council. The trapping or adult Trachemys specimens. species and the native fauna, are identified as Lacomba & Sancho, 2004; Ducotterd et al., 2008; techniques used were nine floating traps checked All captured individuals were measured, important drivers for global loss of biodiversity Schweitzer et al., 2008; Fritz & Chiari, 2013; once a week, fourteen hoop traps checked every weighed and numbered with a four numerical (Primack, 1997; Mooney et al., 2005; Hulme et Teixeira et al., 2013). In Portugal there are rising two days and hand nets whenever it was appropri- code, unique to each individual, which was placed al., 2009; Butchart et al., 2010). The slider turtle, concerns about this species, since E. orbicularis ate. All traps were distributed according to the on the marginal plates of the carapace through Trachemys scripta, native to the eastern and is considered Endangered (Cabral et al., 2005) size and shape of the water bodies, in order to notches realized with a small saw. The carapace central United States of America, is considered and coexists with the native Mediterranean pond evenly cover their entire area, giving six floating length and carapace width were measured using a one of the world´s worst invasive alien species turtle Mauremys leprosa, which may increase traps and six hoop traps at São Lourenço, two caliper (precision: 0.1 mm) and the weight was (Lowe et al., 2000). The main cause of introduc- their spatial segregation (Segurado & Figueiredo, floating traps and three hoop traps at Quinta do recorded with a precision scale (precision: 0.1 g). tion into the wild stems from their massive trade 2007). So the early detection of T. scripta occur- Lago, one floating trap and three hoop traps at All the invasive species individuals were identi- as pets over the last decades, from turtle farms in rence and the confirmation of its reproduction in Dunas Douradas and two hoop traps at Garrão. fied following Ernst & Lovich, 2009 and LIFE the USA to foreign markets (Telecky, 2001). Until new locations are key factors to the efficient The floating traps were placed in deeper areas Trachemys, 2012 and delivered on Official recently, they were legally sold in Europe as development and implementation of adequate where there were a greater number of individuals Reception Centers. Here, whenever evidence of hatchlings (3-4 cm carapace length), and their conservation measures and will contribute to in thermoregulation or in areas with few supports eggs development were detected by inguinal owners are rarely prepared to maintain them in raise the public awareness about this problematic for thermoregulation. The hoop traps were placed palpation, females were radiographed. All E. captivity when they start to grow (reaching up to situation. on the border of the water bodies in areas where orbicularis and M. leprosa individuals were 30 cm carapace length). This common situation In Portugal, at Ria Formosa Natural Park the activity of individuals was higher and the trap immediately released at the capture site, after leads to frequent releases of these animals in the (PNRF) where M. leprosa and E. orbicularis could be conveniently hide. Adding to that, in being given the individual code. wild, resulting in the introduction and establish- populations coexist, T. scripta are sympatric. This order to evaluate the occurrence and abundance ment of many T. scripta populations into different area is populated with high densities of M. leprosa of T. scripta individuals throughout the PNRF RESULTS natural freshwater ecosystems. and contains one of the most important Portuguese area, visual surveys were performed every month, Currently this turtle has been reported as populations of E. orbicularis (Cabral et al., 2005), during the three years, around the main water During the study period, we captured in the four introduced into the wild outside its natural range therefore, it has been implemented a conservation bodies and streams along the Natural Park. wetlands where the trapping techniques were throughout all continents: Europe (Luiselli et al., project in the region in this regard (LIFE Trache- Lastly, in July of 2013, an intensive search with a implemented a total of 259 individuals of differ- 1997; Miranda & Leunda, 2010), Africa (New- mys - LIFE09 NAT/ES/000529). Here we report detection dog was conducted to detect nests ent freshwater turtle invasive species, with 99 berry, 1984), Asia (Chen & Lue, 1998), Oceania the widespread occurrence at PNRF and the first around the São Lourenço wetland, where nesting individuals being captured during the first year, (Burgin, 2006) and America (Thomson et al., confirmed case of successful reproduction of T. 2010). Once introduced, the main requirement for scripta in the wild, in Portugal. its invasion is the occurrence of successful reproduction. Therefore, firm evidence about its repro- MATERIALS AND METHODS duction is a key step towards understanding and managing its possible impacts on the invaded The Ria Formosa Natural Park (PNRF), located in ecosystem (Herbold & Moyle, 1986). Neverthe- the Algarve Region (South Portugal), is a protect- less, during the last decade T. scripta has been ed area including a 60 km stretch of the Algarve confirmed to reproduce in several European coastline and occupies an area of about 18 400 countries, namely in different Mediterranean hectares. Especially important because of its countries such as Italy (Ficetola et al., 2003), biological richness, it has the status of a Natural France (Cadi et al., 2004) and Spain (Pérez-Santi- Park and is classified by the Ramsar Convention gosa et al., 2008). as a wetland of international interest. In Europe, T. scripta has been reported to From 2011 to 2013, between March and compete with native turtle species for basking November, when the freshwater turtles activity is places and food (Cadi & Joly, 2003; 2004; higher (Lebboroni & Chelazzi, 1991; Cadi & Pérez-Santigosa et al., 2011). This situation is Joly, 2000), a set of permanent trapping particularly alarming for the European pond turtle techniques were implemented along four Emys orbicularis, which is considered as near wetlands of special interest for the presence of E. Figure 1. Total of distinct captured individuals per year from the different populations of invasive and native freshwater turtle species. threatened and in sharp decline in several regions orbicularis and M. leprosa populations: São Total de indivíduos distintos capturados por ano das diferentes populações de espécies invasoras e nativas de tartarugas-de-água-doce.

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Chelonian la captura y manejo de galápagos. Informe Conservation and Biology, 3: 87-90. LIFE Trachemys nº8. Conselleria d´Infraes- COX, N. A. & H. J. TEMPLE. 2009. European tructures, Territori i Medi Ambient, 39pp. Red List of Reptiles. Luxembourg: Office for LOWE, S., M. BROWNE, S. BOUDJELAS & Official Publications of the European Com- M. DE POORTER. 2000. 100 of the World’s munities. Worst Invasive Alien Species: A selection DUCOTTERD, J. M., D. MOSIMANN & A. from the Global Invasive Species Database. CADI. 2008. European pond turtle (Emys The Invasive Species Specialist Group (ISSG) orbicularis) conservation program in Switzer- of the World Conservation Union (IUCN). land. Revista Española de Herpetología, 22: LUISELLI, L., M. CAPULA, D. CAPZZI, E. 115-119. PHILIPPI, V. TRUJILLO JESUS & C. ANI- INTRODUCTION of its range (IUCN, 2014), and is therefore Lourenço (19.6 hectares), Quinta do Lago (1.5 signs were higher. This dog was trained during protected by European legislation (Cox & hectares), Dunas Douradas (1 hectares) and the LIFE Trachemys project, with the help of a The introduction of exotic species, and subse- Temple, 2009) and subject of numerous conser- Garrão (0.82 hectares), located along a 5 km specialized dog trainer, to detect eggs, juveniles quent competitive interactions between these vation projects (e.g. Cadi & Miquet, 2004; costal stretch in the Loulé council. The trapping or adult Trachemys specimens. species and the native fauna, are identified as Lacomba & Sancho, 2004; Ducotterd et al., 2008; techniques used were nine floating traps checked All captured individuals were measured, important drivers for global loss of biodiversity Schweitzer et al., 2008; Fritz & Chiari, 2013; once a week, fourteen hoop traps checked every weighed and numbered with a four numerical (Primack, 1997; Mooney et al., 2005; Hulme et Teixeira et al., 2013). In Portugal there are rising two days and hand nets whenever it was appropri- code, unique to each individual, which was placed al., 2009; Butchart et al., 2010). The slider turtle, concerns about this species, since E. orbicularis ate. All traps were distributed according to the on the marginal plates of the carapace through Trachemys scripta, native to the eastern and is considered Endangered (Cabral et al., 2005) size and shape of the water bodies, in order to notches realized with a small saw. The carapace central United States of America, is considered and coexists with the native Mediterranean pond evenly cover their entire area, giving six floating length and carapace width were measured using a one of the world´s worst invasive alien species turtle Mauremys leprosa, which may increase traps and six hoop traps at São Lourenço, two caliper (precision: 0.1 mm) and the weight was (Lowe et al., 2000). The main cause of introduc- their spatial segregation (Segurado & Figueiredo, floating traps and three hoop traps at Quinta do recorded with a precision scale (precision: 0.1 g). tion into the wild stems from their massive trade 2007). So the early detection of T. scripta occur- Lago, one floating trap and three hoop traps at All the invasive species individuals were identi- as pets over the last decades, from turtle farms in rence and the confirmation of its reproduction in Dunas Douradas and two hoop traps at Garrão. fied following Ernst & Lovich, 2009 and LIFE the USA to foreign markets (Telecky, 2001). Until new locations are key factors to the efficient The floating traps were placed in deeper areas Trachemys, 2012 and delivered on Official recently, they were legally sold in Europe as development and implementation of adequate where there were a greater number of individuals Reception Centers. Here, whenever evidence of hatchlings (3-4 cm carapace length), and their conservation measures and will contribute to in thermoregulation or in areas with few supports eggs development were detected by inguinal owners are rarely prepared to maintain them in raise the public awareness about this problematic for thermoregulation. The hoop traps were placed palpation, females were radiographed. All E. captivity when they start to grow (reaching up to situation. on the border of the water bodies in areas where orbicularis and M. leprosa individuals were 30 cm carapace length). This common situation In Portugal, at Ria Formosa Natural Park the activity of individuals was higher and the trap immediately released at the capture site, after leads to frequent releases of these animals in the (PNRF) where M. leprosa and E. orbicularis could be conveniently hide. Adding to that, in being given the individual code. wild, resulting in the introduction and establish- populations coexist, T. scripta are sympatric. This order to evaluate the occurrence and abundance ment of many T. scripta populations into different area is populated with high densities of M. leprosa of T. scripta individuals throughout the PNRF RESULTS natural freshwater ecosystems. and contains one of the most important Portuguese area, visual surveys were performed every month, Currently this turtle has been reported as populations of E. orbicularis (Cabral et al., 2005), during the three years, around the main water During the study period, we captured in the four introduced into the wild outside its natural range therefore, it has been implemented a conservation bodies and streams along the Natural Park. wetlands where the trapping techniques were throughout all continents: Europe (Luiselli et al., project in the region in this regard (LIFE Trache- Lastly, in July of 2013, an intensive search with a implemented a total of 259 individuals of differ- 1997; Miranda & Leunda, 2010), Africa (New- mys - LIFE09 NAT/ES/000529). Here we report detection dog was conducted to detect nests ent freshwater turtle invasive species, with 99 berry, 1984), Asia (Chen & Lue, 1998), Oceania the widespread occurrence at PNRF and the first around the São Lourenço wetland, where nesting individuals being captured during the first year, (Burgin, 2006) and America (Thomson et al., confirmed case of successful reproduction of T. 2010). Once introduced, the main requirement for scripta in the wild, in Portugal. its invasion is the occurrence of successful reproduction. Therefore, firm evidence about its repro- MATERIALS AND METHODS duction is a key step towards understanding and managing its possible impacts on the invaded The Ria Formosa Natural Park (PNRF), located in ecosystem (Herbold & Moyle, 1986). Neverthe- the Algarve Region (South Portugal), is a protect- less, during the last decade T. scripta has been ed area including a 60 km stretch of the Algarve confirmed to reproduce in several European coastline and occupies an area of about 18 400 countries, namely in different Mediterranean hectares. Especially important because of its countries such as Italy (Ficetola et al., 2003), biological richness, it has the status of a Natural France (Cadi et al., 2004) and Spain (Pérez-Santi- Park and is classified by the Ramsar Convention gosa et al., 2008). as a wetland of international interest. In Europe, T. scripta has been reported to From 2011 to 2013, between March and compete with native turtle species for basking November, when the freshwater turtles activity is places and food (Cadi & Joly, 2003; 2004; higher (Lebboroni & Chelazzi, 1991; Cadi & Pérez-Santigosa et al., 2011). This situation is Joly, 2000), a set of permanent trapping particularly alarming for the European pond turtle techniques were implemented along four Emys orbicularis, which is considered as near wetlands of special interest for the presence of E. threatened and in sharp decline in several regions orbicularis and M. leprosa populations: São

64 Martins et al.

contained 15 T. s. elegans eggs that we removed constant recruitment from the surroundings. The et al., 1997), Italy (Ficetola et al., 2003) and to prevent their future hatchling. For all the other results of the surveys performed throughout the France (Cadi et al., 2004), the confirmed repro- 10 females, the X-rays revealed 17 eggs on aver- three years on the study area, support the idea of a duction of T. scripta at Ria Formosa Natural Park age (minimum 15/maximum 21). wider distribution of the population that can in Portugal reinforces the possibility of perma- The surveys performed throughout all the provide the conditions for a successful naturaliza- nent establishment of this species within all the Natural Park area confirmed the permanent tion. Adding to that, the high number of captured Mediterranean region. This data enhances the presence of T. scripta populations scattered all hatchlings, still with the presence of umbilical urgent need to strengthen the European legisla- over the Natural Park during the three years and scar and absence of growing rings, suggest the tion, banning the trade of all T. scripta subspecies, all the estimates of observed individuals indicated existence of successful reproduction, since they trade control and population management by the constant occurrence of hundreds of individu- all are smaller than the mean for T. scripta hatch- promoting an European Invasion Alert Network als (adults and juveniles) each year. lings described by Janzen et al. (2000). Further- and early eradication campaigns from natural The detection dog was used for testing 4 sites, more, hundreds of individuals of both gender and wetlands. identified as more suitable for nesting near the different ages captured and observed throughout border of São Lourenço wetland, in a total of the PNRF, as well as the several adult egg-bearing ACKNOWLEDGMENTS approximately 2 hectares, with 2 visits of 1 females encountered near nesting sites, support hour/per site. One nest of T. s. elegans was detect- the idea that they were able to adapt to the natural This research was supported by the LIFE Trache- ed, at the same area where most of the newly conditions and to establish successfully. This mys project (LIFE09 NAT/ES/000529). We thank hatched nests and a female nesting during the situation increases the direct competition with DogAlgarve, especially the dog trainer Américo spring were already encountered. The nest native turtles, adding a new disturbance factor Lopes and everyone who helped in the fieldwork, Figure 2. Total of captured individuals per year from the various invasive freshwater turtle species. Total de indivíduos contained 14 eggs with newly hatched T. s. and increasingly restricting the places where they especially Thijs Valkenburg, Tiago Ventura, Mauro capturados por ano das várias espécies invasoras de tartaru- elegans and some still hatching, that we also occur naturally and the invasion process has not Hilário, Jael Palhas and António Cotão. gas-de-água-doce. removed immediately. occurred yet. Lastly, the use of a detection dog for reproduction evidence, even it has not been used REFERENCES 81 during the second year and 79 during the third DISCUSSION extensively, showed certain success, giving the year (Fig. 1). At the same time, we captured a location of one nest that provided evidence of BURGIN, S. 2006. Confirmation of an estab- total of 341 different individuals of E. orbicularis Our study showed that T. scripta occurs in high reproduction of T. scripta and confirmed the lished population of exotic turtles in urban and 2286 of M. leprosa, with 156 E. orbicularis densities in the study area and confirmed for the promising application of this technique, initially Sydney. Australian Journal of Zoology, 33, and 1487 M. leprosa being captured in the first first time the reproduction of this species in developed in Australia by the Queensland Depart- 379-384. DOI: 10.7882/AZ.2006.011 year, 141 E. orbicularis and 531 M. leprosa in the Portugal. The high number of captured and ment of Natural Resources (O’Keeffe, 2005). BUTCHART, S. H. M., M. WALPOLE, B. second year and 44 E. orbicularis and 268 M. removed individuals from natural conditions, These results are alarming and represent a COLLEN, A. VAN STRIEN, J. P. W. leprosa in the third year (Fig. 1). From all the repeatedly over the three years of study, reveals viable invasive population, co-occurring with SCHARLEMANN, R. E. A. ALMOND, J. E. captured invasive species individuals, 253 where an established population and the occurrence of important native populations of E. orbicularis. M. BAILLIE, B. BOMHARD, C. BROWN, J. from different sub-species of T. scripta, especial- Without an intensive control and population man- BRUNO, K. E. CARPENTER, G. M. CARR, ly T. s. elegans (n=236), but also T. s. scripta Table 1. Characterization of the population sample of freshwa- agement, this situation can lead to a massive and J. CHANSON, A. M. CHENERY, J. CSIRKE, (n=8), T. s. troosti (n=1) and hybrids between T. s. ter turtle invasive species captured. Acl – Average carapace widespread naturalization of this species, with N. C. DAVIDSON, F. DENENER, M. elegans and T. s. scripta (n=8) (Fig. 2). The length; Acw – Average carapace width; Aw - Average weight. irreversible negative impacts on native fauna and Caracterização da amostra da população de espécies de FOSTER, A. GALLI, J. N. GALLOWAY, P. remaining individuals were Pseudemys concinna tartarugas-de-água-doce invasoras capturada. Acl – Compri- on the ecosystem functioning, similarly to what GENOVESI, R. D. GREGORY, M. HOCK- (n=3), Pseudemys nelsoni (n=2) and Graptemys mento médio da carapaça; Acw – Largura média da carapaça; has been observed in other areas throughout INGS, V. KAPOS, J. F. LAMARQUE, F. pseudogeographica (n=1) (Fig. 2). Overall, from Aw – Peso médio. Europe (Cadi et al., 2004; Pérez-Santigosa et al., LEVERINGTON, J. LOH, M. A. MCGEOCH, the captured sample, most individuals were 2008). Captured individuals from invasive freshwater turtle species L. MCRAE, A. MINASYAN, M. H. MOR- breeding adults, especially females, together with (N = 259) Although T. scripta is very common and CILLO, T. E. E. OLDFIELD, D. PAULY, S. a high number of juveniles and some hatchlings Adults (n = 145) popular as a pet, its invasive status and impact on QUADER, C. REVENGA, J. R. SAUER, B. Females (n = 124) Acl (21.2cm); Acw (16.1cm); Aw (1455.5g) (Table 1). All hatchlings had the umbilical scar on Males (n = 21) Acl (16.7cm); Acw (13.0cm); Aw (628.8g) local ecosystems and native species are still SKOLNIK, D. SPEAR, D. STAN- the middle of their plastron and none had growing unknown for the general public. The evidence of WELL-SMITH, S. N. STUART, A. SYMES, rings on the carapace. Among all the adult Juveniles (n = 93) successful reproduction and establishment by this Females (n = 50) Acl (10.3cm); Acw (8.7cm); Aw (198.4g) M. TIERNEY, T. D. TYRRELL, J. C. VIÉ & females captured, 11 T. s. elegans were egg-bear- Males (n = 36) Acl (12.7cm); Acw (10.2cm); Aw (299.1g) species in the study area might be a first sign to R. WATSON. 2010. Global Biodiversity: ing females, identified by palpation, including Undetermined (n = 7) Acl (8.5cm); Acw (7.2cm); Aw (90.0g) help rising public awareness for this problem. Indicators of Recent Declines. Science, 328: one that was already covering the nest, near the Hatchlings (n = 21) Together with the successful reproduction 1164-1168. DOI: 10.1126/science.1187512 border of São Lourenço wetland. The nest Undetermined (n = 21) Acl (3.2cm); Acw (3.1cm); Aw (7.4g) reports of T. scripta in Spain (Martinez-Silvestre CABRAL, M. J., J. ALMEIDA, P. R. ALMEI-

Limnetica, 37(1): 61-67 (2018)

Reproduction of Trachemys scripta in Portugal 65 contained 15 T. s. elegans eggs that we removed constant recruitment from the surroundings. The et al., 1997), Italy (Ficetola et al., 2003) and to prevent their future hatchling. For all the other results of the surveys performed throughout the France (Cadi et al., 2004), the confirmed repro- 10 females, the X-rays revealed 17 eggs on aver- three years on the study area, support the idea of a duction of T. scripta at Ria Formosa Natural Park age (minimum 15/maximum 21). wider distribution of the population that can in Portugal reinforces the possibility of perma- The surveys performed throughout all the provide the conditions for a successful naturaliza- nent establishment of this species within all the Natural Park area confirmed the permanent tion. Adding to that, the high number of captured Mediterranean region. This data enhances the presence of T. scripta populations scattered all hatchlings, still with the presence of umbilical urgent need to strengthen the European legisla- over the Natural Park during the three years and scar and absence of growing rings, suggest the tion, banning the trade of all T. scripta subspecies, all the estimates of observed individuals indicated existence of successful reproduction, since they trade control and population management by the constant occurrence of hundreds of individu- all are smaller than the mean for T. scripta hatch- promoting an European Invasion Alert Network als (adults and juveniles) each year. lings described by Janzen et al. (2000). Further- and early eradication campaigns from natural The detection dog was used for testing 4 sites, more, hundreds of individuals of both gender and wetlands. identified as more suitable for nesting near the different ages captured and observed throughout border of São Lourenço wetland, in a total of the PNRF, as well as the several adult egg-bearing ACKNOWLEDGMENTS approximately 2 hectares, with 2 visits of 1 females encountered near nesting sites, support hour/per site. One nest of T. s. elegans was detect- the idea that they were able to adapt to the natural This research was supported by the LIFE Trache- ed, at the same area where most of the newly conditions and to establish successfully. This mys project (LIFE09 NAT/ES/000529). We thank hatched nests and a female nesting during the situation increases the direct competition with DogAlgarve, especially the dog trainer Américo spring were already encountered. The nest native turtles, adding a new disturbance factor Lopes and everyone who helped in the fieldwork, contained 14 eggs with newly hatched T. s. and increasingly restricting the places where they especially Thijs Valkenburg, Tiago Ventura, Mauro elegans and some still hatching, that we also occur naturally and the invasion process has not Hilário, Jael Palhas and António Cotão. removed immediately. occurred yet. Lastly, the use of a detection dog for reproduction evidence, even it has not been used REFERENCES 81 during the second year and 79 during the third DISCUSSION extensively, showed certain success, giving the year (Fig. 1). At the same time, we captured a location of one nest that provided evidence of BURGIN, S. 2006. Confirmation of an estab- total of 341 different individuals of E. orbicularis Our study showed that T. scripta occurs in high reproduction of T. scripta and confirmed the lished population of exotic turtles in urban and 2286 of M. leprosa, with 156 E. orbicularis densities in the study area and confirmed for the promising application of this technique, initially Sydney. Australian Journal of Zoology, 33, and 1487 M. leprosa being captured in the first first time the reproduction of this species in developed in Australia by the Queensland Depart- 379-384. DOI: 10.7882/AZ.2006.011 year, 141 E. orbicularis and 531 M. leprosa in the Portugal. The high number of captured and ment of Natural Resources (O’Keeffe, 2005). BUTCHART, S. H. M., M. WALPOLE, B. second year and 44 E. orbicularis and 268 M. removed individuals from natural conditions, These results are alarming and represent a COLLEN, A. VAN STRIEN, J. P. W. leprosa in the third year (Fig. 1). From all the repeatedly over the three years of study, reveals viable invasive population, co-occurring with SCHARLEMANN, R. E. A. ALMOND, J. E. captured invasive species individuals, 253 where an established population and the occurrence of important native populations of E. orbicularis. M. BAILLIE, B. BOMHARD, C. BROWN, J. from different sub-species of T. scripta, especial- Without an intensive control and population man- BRUNO, K. E. CARPENTER, G. M. CARR, ly T. s. elegans (n=236), but also T. s. scripta agement, this situation can lead to a massive and J. CHANSON, A. M. CHENERY, J. CSIRKE, (n=8), T. s. troosti (n=1) and hybrids between T. s. widespread naturalization of this species, with N. C. DAVIDSON, F. DENENER, M. elegans and T. s. scripta (n=8) (Fig. 2). The irreversible negative impacts on native fauna and FOSTER, A. GALLI, J. N. GALLOWAY, P. remaining individuals were Pseudemys concinna on the ecosystem functioning, similarly to what GENOVESI, R. D. GREGORY, M. HOCK- (n=3), Pseudemys nelsoni (n=2) and Graptemys has been observed in other areas throughout INGS, V. KAPOS, J. F. LAMARQUE, F. pseudogeographica (n=1) (Fig. 2). Overall, from Europe (Cadi et al., 2004; Pérez-Santigosa et al., LEVERINGTON, J. LOH, M. A. MCGEOCH, the captured sample, most individuals were 2008). L. MCRAE, A. MINASYAN, M. H. MOR- breeding adults, especially females, together with Although T. scripta is very common and CILLO, T. E. E. OLDFIELD, D. PAULY, S. a high number of juveniles and some hatchlings popular as a pet, its invasive status and impact on QUADER, C. REVENGA, J. R. SAUER, B. (Table 1). All hatchlings had the umbilical scar on local ecosystems and native species are still SKOLNIK, D. SPEAR, D. STAN- the middle of their plastron and none had growing unknown for the general public. The evidence of WELL-SMITH, S. N. STUART, A. SYMES, rings on the carapace. Among all the adult successful reproduction and establishment by this M. TIERNEY, T. D. TYRRELL, J. C. VIÉ & females captured, 11 T. s. elegans were egg-bear- species in the study area might be a first sign to R. WATSON. 2010. Global Biodiversity: ing females, identified by palpation, including help rising public awareness for this problem. Indicators of Recent Declines. Science, 328: one that was already covering the nest, near the Together with the successful reproduction 1164-1168. DOI: 10.1126/science.1187512 border of São Lourenço wetland. The nest reports of T. scripta in Spain (Martinez-Silvestre CABRAL, M. J., J. ALMEIDA, P. R. ALMEI-

Limnetica, 37(1): 61-67 (2018)

66 Martins et al.

Limnetica, 37(1): 61-67 (2018) INTRODUCTION of its range (IUCN, 2014), and is therefore Lourenço (19.6 hectares), Quinta do Lago (1.5 signs were higher. This dog was trained during protected by European legislation (Cox & hectares), Dunas Douradas (1 hectares) and the LIFE Trachemys project, with the help of a The introduction of exotic species, and subse- Temple, 2009) and subject of numerous conser- Garrão (0.82 hectares), located along a 5 km specialized dog trainer, to detect eggs, juveniles quent competitive interactions between these vation projects (e.g. Cadi & Miquet, 2004; costal stretch in the Loulé council. The trapping or adult Trachemys specimens. species and the native fauna, are identified as Lacomba & Sancho, 2004; Ducotterd et al., 2008; techniques used were nine floating traps checked All captured individuals were measured, important drivers for global loss of biodiversity Schweitzer et al., 2008; Fritz & Chiari, 2013; once a week, fourteen hoop traps checked every weighed and numbered with a four numerical (Primack, 1997; Mooney et al., 2005; Hulme et Teixeira et al., 2013). In Portugal there are rising two days and hand nets whenever it was appropri- code, unique to each individual, which was placed al., 2009; Butchart et al., 2010). The slider turtle, concerns about this species, since E. orbicularis ate. All traps were distributed according to the on the marginal plates of the carapace through Trachemys scripta, native to the eastern and is considered Endangered (Cabral et al., 2005) size and shape of the water bodies, in order to notches realized with a small saw. The carapace central United States of America, is considered and coexists with the native Mediterranean pond evenly cover their entire area, giving six floating length and carapace width were measured using a one of the world´s worst invasive alien species turtle Mauremys leprosa, which may increase traps and six hoop traps at São Lourenço, two caliper (precision: 0.1 mm) and the weight was (Lowe et al., 2000). The main cause of introduc- their spatial segregation (Segurado & Figueiredo, floating traps and three hoop traps at Quinta do recorded with a precision scale (precision: 0.1 g). tion into the wild stems from their massive trade 2007). So the early detection of T. scripta occur- Lago, one floating trap and three hoop traps at All the invasive species individuals were identi- as pets over the last decades, from turtle farms in rence and the confirmation of its reproduction in Dunas Douradas and two hoop traps at Garrão. fied following Ernst & Lovich, 2009 and LIFE the USA to foreign markets (Telecky, 2001). Until new locations are key factors to the efficient The floating traps were placed in deeper areas Trachemys, 2012 and delivered on Official recently, they were legally sold in Europe as development and implementation of adequate where there were a greater number of individuals Reception Centers. Here, whenever evidence of hatchlings (3-4 cm carapace length), and their conservation measures and will contribute to in thermoregulation or in areas with few supports eggs development were detected by inguinal owners are rarely prepared to maintain them in raise the public awareness about this problematic for thermoregulation. The hoop traps were placed palpation, females were radiographed. All E. captivity when they start to grow (reaching up to situation. on the border of the water bodies in areas where orbicularis and M. leprosa individuals were 30 cm carapace length). This common situation In Portugal, at Ria Formosa Natural Park the activity of individuals was higher and the trap immediately released at the capture site, after leads to frequent releases of these animals in the (PNRF) where M. leprosa and E. orbicularis could be conveniently hide. Adding to that, in being given the individual code. wild, resulting in the introduction and establish- populations coexist, T. scripta are sympatric. This order to evaluate the occurrence and abundance ment of many T. scripta populations into different area is populated with high densities of M. leprosa of T. scripta individuals throughout the PNRF RESULTS natural freshwater ecosystems. and contains one of the most important Portuguese area, visual surveys were performed every month, Currently this turtle has been reported as populations of E. orbicularis (Cabral et al., 2005), during the three years, around the main water During the study period, we captured in the four introduced into the wild outside its natural range therefore, it has been implemented a conservation bodies and streams along the Natural Park. wetlands where the trapping techniques were throughout all continents: Europe (Luiselli et al., project in the region in this regard (LIFE Trache- Lastly, in July of 2013, an intensive search with a implemented a total of 259 individuals of differ- 1997; Miranda & Leunda, 2010), Africa (New- mys - LIFE09 NAT/ES/000529). Here we report detection dog was conducted to detect nests ent freshwater turtle invasive species, with 99 berry, 1984), Asia (Chen & Lue, 1998), Oceania the widespread occurrence at PNRF and the first around the São Lourenço wetland, where nesting individuals being captured during the first year, (Burgin, 2006) and America (Thomson et al., confirmed case of successful reproduction of T. 2010). Once introduced, the main requirement for scripta in the wild, in Portugal. its invasion is the occurrence of successful reproduction. Therefore, firm evidence about its repro- MATERIALS AND METHODS duction is a key step towards understanding and managing its possible impacts on the invaded The Ria Formosa Natural Park (PNRF), located in ecosystem (Herbold & Moyle, 1986). Neverthe- the Algarve Region (South Portugal), is a protect- less, during the last decade T. scripta has been ed area including a 60 km stretch of the Algarve confirmed to reproduce in several European coastline and occupies an area of about 18 400 countries, namely in different Mediterranean hectares. Especially important because of its countries such as Italy (Ficetola et al., 2003), biological richness, it has the status of a Natural France (Cadi et al., 2004) and Spain (Pérez-Santi- Park and is classified by the Ramsar Convention gosa et al., 2008). as a wetland of international interest. In Europe, T. scripta has been reported to From 2011 to 2013, between March and compete with native turtle species for basking November, when the freshwater turtles activity is places and food (Cadi & Joly, 2003; 2004; higher (Lebboroni & Chelazzi, 1991; Cadi & Pérez-Santigosa et al., 2011). This situation is Joly, 2000), a set of permanent trapping particularly alarming for the European pond turtle techniques were implemented along four Emys orbicularis, which is considered as near wetlands of special interest for the presence of E. threatened and in sharp decline in several regions orbicularis and M. leprosa populations: São

Reproduction of Trachemys scripta in Portugal 67

Limnetica, 37(1): 61-67 (2018)