Notas / Notes

 

New records of the Chinese turtles Mauremys reevesii (Gray, 1831) and Mauremys sinensis (Gray, 1834) (Testudines, Geoemydidae) in southern Spain

Juan Pablo González de la Vega1, Juan García-de-Lomas2, 3* & José Luis Rodríguez-Andrés3

1 C/ Cruz, 8, 3a A, 21006, Huelva, España

Email: latasti@hotmail.com — ORCID iD: https://orcid.org/0000-0003-2930-7033

2, 3 Agencia de Medio Ambiente y Agua de Andalucía, 41092, Sevilla, España

2 Grupo I+D Estructura y Dinámica de Ecosistemas Acuáticos, Universidad de Cádiz, España

Email: juan.garciadelomas@uca.es — ORCID iD: https://orcid.org/0000-0002-1818-1941

3 Email: josel.rodriguez.andres@juntadeandalucia.es — ORCID iD: https://orcid.org/0000-0001-9923-7961


* Correspondig autor: juan.garciadelomas@uca.es

 

ABSTRACT

The trade of freshwater turtles as pets and their eventual release or escape has led to new naturalized alien species that eventually form invasive populations in aquatic ecosystems. The import of alien Mauremys spp. species implies a new threat to the conservation of aquatic ecosystems, due to their ability to hybridise with the native species Mauremys leprosa. In this work, 16 new records of naturalised specimens of the Asian turtles Mauremys reevesii and Mauremys sinensis in Andalusia (southern Spain) are documented. Most of them (13) were found in artificial aquatic environments associated with urban areas, although the rest were found in protected natural areas sharing the habitat with natural populations of M. leprosa. These new records recreate the pattern of sale-release-naturalization-invasion that has already occurred with other alien turtle species. The number of alien Mauremys specimens imported into Spain (more than 100,000 since 2006) suggests that the current number of naturalised specimens could be much higher than reported in publications.

Keywords: pet trade; turtles; naturalisation; invasion; hybridisation.

 

RESUMEN

Nuevas citas de los galápagos chinos Mauremys reevesii (Gray, 1831) y Mauremys sinensis (Gray, 1834) (Testudines, Geoemydidae) en España

El comercio de quelonios acuáticos como animales de compañía y su eventual liberación o escape ha conllevado la detección de especies exóticas naturalizadas o formando poblaciones invasoras en ecosistemas acuáticos. La importación de Mauremys spp. exóticos implica una nueva amenaza para la conservación de los ecosistemas acuáticos, debido a su capacidad de hibridarse con la especie nativa Mauremys leprosa. En este trabajo se documentan 16 nuevos registros de ejemplares asilvestrados de los galápagos asiáticos Mauremys reevesii y Mauremys sinensis en Andalucía (sur de España). La mayor parte de ellos (13) corresponden a ambientes acuáticos artificiales asociados a áreas urbanas y el resto se encontraron en espacios naturales protegidos con poblaciones naturales de M. leprosa. Estas nuevas citas ponen de manifiesto que los nuevos taxones comercializados reproducen el patrón de venta-abandono-naturalización-invasión ya acaecido con otras especies exóticas de galápagos. El número de ejemplares de Mauremys exóticos importados en España (más de 100.000 desde 2006) sugiere que el número real de ejemplares asilvestrados podría ser bastante mayor al documentado en los trabajos publicados.

Palabras clave: comercio de mascotas; tortugas; naturalización; invasión; hibridación.

 

Recibido/Received: 15/01/2021; Aceptado/Accepted: 05/04/2021; Publicado en línea/Published online: 15/07/2021

Citation / Cómo citar este artículo: González de la Vega, J. P., García-de-Lomas, J. & Rodríguez-Andrés, J. L. 2021. New records of the Chinese turtles Mauremys reevesii (Gray, 1831) and Mauremys sinensis (Gray, 1834) (Testudines, Geoemydidae) in southern Spain. Graellsia, 77(2): e142. https://doi.org/10.3989/graellsia.2021.v77.306

Copyright: © 2021 SAM & CSIC. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0) License.


 

CONTENTS

ABSTRACT

RESUMEN

Acknowledgements

References

The pet trade is one of the main introduction pathways of invasive alien species. Exotic freshwater turtles are a worldwide paradigm of invasion from imported pets that are later abandoned into aquatic ecosystems by their owners or escape confinement (Lockwood et al., 2019). In Spain, alien turtles outcompete the native endangered terrapins: the European pond turtle, Emys orbicularis (Linnaeus, 1758), and the Spanish terrapin, Mauremys leprosa (Schweigger, 1812) (Polo-Cavia et al., 2010a, 2010b, 2011). The trade of red-eared slider Trachemys scripta subsp. elegans (Wied, 1838) was banned in Europe in 1997 following salmonellosis outbreaks in children and biodiversity concerns (Woodward et al., 1997). However, other freshwater turtle species such as Chrysemys picta (Schneider, 1783), Graptemys spp., Macrochelys temminckii Troost, 1835, alien Mauremys spp., Pelomedusa subrufa (Bonnaterre, 1789), Pelusios spp., or even a subspecies of the banned taxon (Trachemys scripta subsp. scripta (Thunberg, 1792)) have been imported into Spain (Cites Trade Database, 2020) although they may also be reservoirs of pathogens and invade aquatic ecosystems (e.g., Martínez-Silvestre et al., 2015; Sancho et al., 2015; Back et al., 2016). In 2013, the Spanish legislation (Royal Decree 613/2013) banned the trade of Trachemys scripta (Thunberg in Schoepff, 1792), Chrysemys picta and Pseudemys peninsularis Carr, 1938. Three years later, the list of invasive alien species of Union concern also banned Trachemys scripta according to the Commission implementing regulation 2016/1141. Despite these regulation advances, many unbanned pond turtle species have been imported in the last two decades, including some dangerous species such as the snapping turtle Chelydra serpentina (Linnaeus, 1758) (Cites Trade Database, 2020). To date, up to 21 freshwater alien chelonian taxa have been reported in Spanish natural, seminatural or artificial wetlands: Apalone ferox (Schneider, 1783), Chrysemys picta, Chelydra serpentina, Graptemys ouachitensis (Cagle, 1953), Graptemys pseudogeographica (Gray, 1831), Macrochelys temminckii, Mauremys mutica (Cantor, 1842), Mauremys reevesii (Gray, 1831), Mauremys sinensis (Gray, 1834), Pseudemys concinna (Le Conte, 1830), Pseudemys nelsoni Carr, 1938, Pseudemys rubriventris (Le Conte, 1830), Pelodiscus sinensis (Wiegmann, 1835), Pelomedusa subrufa, Trachemys decussata (Gray, 1831), Trachemys emolli (Legler, 1990), Trachemys ornata (Gray, 1831), Trachemys scripta subsp. elegans, Trachemys scripta subsp. scripta, Trachemys scripta elegans x Trachemys scripta scripta, and Trachemys scripta subsp. troostii (Holbrook, 1836) (Mateo et al., 2011; Balmori, 2014 and references therein; Campos-Such et al., 2015; Cruz et al., 2015; Martínez-Silvestre et al., 2015; Poch et al., 2020).

The case of alien taxa of the genus Mauremys is of particular concern due to their ability to hybridise with the native species Mauremys leprosa (Nickl, 2015; Sancho et al., 2020). Between 2006 and 2019, 55,825 live individuals of Reeves‘ pond turtle Mauremys reevesii and 45,320 live individuals of the Chinese stripe-necked turtle Mauremys sinensis have been imported into Spain, mainly from China, Hong Kong, Taiwan and Japan (Cites Trade Database, 2020). Although these species have been imported more recently and in much smaller quantities than Trachemys scripta elegans (up to 900,068 individuals until the year 2000; Cites Trade Database, 2020), their eventual release into the natural environment represents a conservation concern, particularly for the native Mauremys leprosa. Until now, the presence of naturalised specimens of M. sinensis was documented in the regions of Valencia and Catalonia (Campos-Such et al., 2015; Martínez-Silvestre et al., 2015, 2019), whereas M. reevesii was cited in Galicia (Ayres, 2016) and Catalonia (Poch et al., 2020).

Considering that early detection is an essential tool for efficient management, new citations of Mauremys reevesii and Mauremys sinensis from southern Spain were compiled from different sources (mainly naturalists, amateurs or nature managers) between 2009 and 2020. All records were georeferenced, using the UTM projection and the ETRS1989 reference system, in extended zone 30, in accordance with European standards. Only those citations that could be validated through photographs or captured specimens were included. In total, 15 new validated records were collected: seven records corresponded to M. reevesii and eight records to M. sinensis (Table 1; Fig. 1). All M. reevesii records showed the characteristic yellowish striping and blotching extending down the neck from the snout, whereas M. sinensis showed the characteristic parallel, narrow yellow stripes on their heads, necks and parts of their legs (Fig. 1).

Table 1.— New records of Mauremys reevesii and Mauremys sinensis in Andalucía (southern Spain). All records corresponded to adult specimens. Coordinates are indicated in UTM projection, datum ETRS1989, zone 30, according to European standards.

Tabla 1.— Nuevas citas de Mauremys reevesii y Mauremys sinensis en Andalucía (sur de España). Todos los registros correspondieron a ejemplares adultos. Las coordenadas se indican en la proyección UTM, datum ETRS1989, zona 30, conforme a los estándares europeos.

Species Date UTM X UTM Y Altitude (m) Locality, Province Habitat type Source (observer)
Mauremys reevesii 08/06/2020 290484 4008421 2 Arroyo Negro Natural Microreserve, La Línea de la Concepción, Cádiz Natural Cerpa-González, R.M.
Mauremys reevesii 11/03/2020 368539 4064327 45 Botanic Garden, University of Málaga Artificial Fernández-Meléndez, E.
Mauremys reevesii 05/05/2018 363185 4050784 20 ‘La Paloma’ garden, Benalmádena, Málaga Artificial González-de-la-Vega, J.P.
Mauremys reevesii 12/11/2019 373292 4064806 13 Garden beside the Cathedral, Málaga Artificial González-de-la-Vega, J.P.
Mauremys reevesii 30/09/2019 443450 4105640 779 ‘Parque de la Estación’, Otura, Granada Artificial Marín-Escribano, J.M.
Mauremys reevesii 18/08/2017 445899 4113838 660 ‘Parque Federico García Lorca’, Granada Artificial Fernández-Cardenete, J.R.
Mauremys reevesii 07/05/2017 363672 4052553 96 Garden at ‘Altos del Olivar’ urbanisation, Torremolinos, Málaga Artificial González-de-la-Vega, J.P.
Mauremys sinensis 20/06/2019 234901 4145340 5 ‘Parque del Alamillo’, Sevilla Artificial Verdejo-Díaz, P.A.
Mauremys sinensis 01/10/2020 141119 4126066 6 ‘Laguna del Portil’ Natural Reserve, Punta Umbría, Huelva Natural Rodríguez-Andrés, J.L.
Mauremys sinensis 30/10/2020 445899 4113838 660 ‘Parque Federico García Lorca’, Granada Artificial Luna-Fernández, A.
Mauremys sinensis 05/06/2019 151751 4124665 15 Botanic Garden ‘José Celestino Mutis’, Palos de la Frontera, Huelva Artificial Bonaño-Quiñones, L.
Mauremys sinensis 22/02/2009 141180 4125741 5 Open land beside ‘Laguna del Portil’ Natural Reserve, Punta Umbría, Huelva Natural González-de-la-Vega, J.P.
Mauremys sinensis 19/06/2016 363185 4050784 20 ‘La Paloma’ garden, Benalmádena, Málaga Artificial González-de-la-Vega, J.P.
Mauremys sinensis 11/06/2019 237678 4144578 8 ‘Miraflores’ garden, Sevilla Artificial Verdejo-Díaz, P.A.
Mauremys sinensis 05/10/2017 308951 4074854 602 Garden in Arriate, Málaga Artificial Melgar-Gómez, R.

Fig. 1.— Specimens of Mauremys reevesii observed in Málaga (left) and Mauremys sinensis found in Laguna del Portil Natural Reserve, Huelva (right). Photos by Juan Pablo González de la Vega©.

Fig. 1.— Ejemplares de Mauremys reevesii observados en Málaga (izquierda) y Mauremys sinensis encontrado en la Reserva Natural Laguna del Portil, Huelva (derecha). Fotos de Juan Pablo González de la Vega©.

 

In sum, the new records included five of the eight provinces of Andalusia. Most of them (12/15) were found in artificial lakes, while the rest were found in protected areas (the ‘Arroyo Negro’ and ‘Laguna del Portil’ natural reserves), sharing the habitat with natural populations of M. leprosa. All locations were adjacent to urban centres, which may favour the reception of abandoned pets. Both species constitute new records to Andalusia.

The results suggest that the introduction of Mauremys reevesii and M. sinensis is not an anecdotal fact, but rather reproduces the ‘sale-release-naturalisation-invasion’ process that has already occurred with other exotic freshwater turtles marketed as pets and other regions (Sancho & Lacomba, 2016; Poch et al., 2020). There are several limitations for a new record to be reported: (i) the taxon must ‘cross’ a person’s view or be captured, and detectability decreases at low population size (Metha et al., 2007). In fact, the M. sinensis specimen found at ‘Laguna del Portil’ Natural Reserve was captured after six days of an alien turtle control campaign that used six baited fyke nets per day (lake surface = 12 ha). (ii) The taxon must be differentiated from a native taxon and be correctly identified. For this purpose, a high-quality picture or a captured specimen is needed, as well as certain expertise. (iii) The new record must be published. As a consequence, the current abundance of alien Mauremys spp. in the field may be much higher than documented in publications (García-de-Lomas et al., 2016; Vall-llosera & Cassey, 2017). Therefore, further surveillance of aquatic ecosystems is recommended to detect the presence of alien Mauremys species early and to implement rapid response actions.

Moreover, the increasing records of alien Mauremys spp. in Spain provides further evidence that all the turtle taxa marketed as pets are prone to be released and become a conservation threat. This fact suggests that banning particular species in the form of ‘blacklists’, far from solving the problem, may favour the trade of unbanned species (García-de-Lomas & Vilà, 2015). Thus, banning the movement and sale of all freshwater alien turtles apart from specifically permitted non-invasive, non-harmful species (in the form of a ‘white’ list) could help reverse the current trend of naturalisation and invasion.


AcknowledgementsTop

The authors thank L. Bonaño-Quiñones, R.M. Cerpa-González, J.R. Fernández-Cardenete, E. Fernández-Meléndez, A. Luna-Fernández, J.M., Marín-Escribano, R. Melgar Gómez and P.A. Verdejo-Díaz for sharing their turtle observations that allowed their identification.

ReferencesTop

Ayres, C., 2016. Mauremys reevesi (Gray, 1831), familia Geoemydidae, en liberdade no Noroeste de España: o primeiro de moitos en Europa? Braña, 14: 58-59. Available from https://sghn.org/wp-content/uploads/2018/06/AYRES-FERNANDEZ_Mauremys-reevesi_Gray1831_familia_Geoemydae_liberdade_Noroeste_Espanha_BRANHA_2016.pdf. [accessed 22 Dec. 2020]
Back, D-S., Shin, G.-W., Wendt, M. & Heo, G.-J. 2016. Prevalence of Salmonella spp. in pet turtles and their environment. Laboratory Animal Research, 32(3): 166-170. https://doi.org/10.5625/lar.2016.32.3.166
Balmori, A. 2014. Utilidad de la legislación sobre especies invasoras para la conservación de las especies de galápagos ibéricos. Boletín de la Asociación Herpetólogica Española, 25: 68-74.
Campos-Such, D., Miñarro, M. & Valls, L. 2015. Localización de un ejemplar asilvestrado de Mauremys sinensis en la Comunidad Valenciana. Boletín de la Asociación Herpetológica Española, 27(1): 97-99.
CITES Trade Database 2020. Available from https://trade.cites.org/es/cites_trade/. [accessed 22 Dec. 2020].
Cruz, D., Delgado, P., López, V. & Montero, J. 2015. Presencia de Apalone ferox en el Parque Natural de las Lagunas de Ruidera (Ciudad Real). Boletín de la Asociación Herpetológica Española, 26(1): 89 -91.
García-de-Lomas, J., Dana, E.D., Chaves, J., Ramírez, J.M. & Lineros, A. 2016. Entre pitones y panteras: encuentros con animales exóticos peligrosos en Andalucía. El Corzo, 4: 62-71. Available from http://sociedadgaditanahistorianatural.com/wp-content/uploads/2016/02/09_ElCorzo4_2016_encuentros_especies_peligrosas.pdf. [accessed 20 Dec. 2020].
García-de-Lomas, J. & Vilà M. 2015. Lists of harmful alien organisms: Are the national regulations adapted to the global world? Biological Invasions, 17: 3081-3091. https://doi.org/10.1007/s10530-015-0939-7
Lockwood, J.L., Welbourne, D.J., Romagosa, C.M., Cassey, P., Mandrak, N.E., Strecker, A., Leung, B., Stringham, O.C., Udell, B., Episcopio-Sturgeon, D.J., Tlusty, M.F., Sinclair, J., Springborn, M.R., Pienaar, E.F., Rhyne, A.L. & Keller, R. 2019. When pets become pests: the role of the exotic pet trade in producing invasive vertebrate animals. Frontiers in Ecology and the Environment, 17(6): 323-330. https://doi.org/10.1002/fee.2059
Martínez-Silvestre, A., Guinea, D., Ferrer, D. & Pantchev, N. 2015. Parasitic enteritis associated with the camallanid nematode Serpinema microcephalus in wild invasive turtles (Trachemys, Pseudemys, Graptemys and Ocadia) in Spain. Journal of Herpetological Medicine and Surgery, 25: 48-52. https://doi.org/10.5818/1529-9651-25.1.48
Martínez-Silvestre, A., Soler, J. & Cano, J.M. 2019. Adaptación y reproducción de Mauremys sinensis a las condiciones naturales del nordeste de la península ibérica. Boletín de la Asociación Herpetológica Española, 30: 75-78.
Mateo, J.A., Ayres, C. & López-Jurado, L. F. 2011. Los anfibios y reptiles naturalizados en España: Historia y evolución de una problemática reciente. Boletín de la Asociación Herpetológica Española, 22: 2-42.
Metha, S.V., Haight, R.G., Homans, F.R., Polasky, S. & Venette, R.C. 2007. Optimal detection and control strategies for invasive species management. Ecological Economics, 61: 237-245. https://doi.org/10.1016/j.ecolecon.2006.10.024
Nickl, S. 2015. Kann denn liebe sünde sein? Eine randnotiz zu hybriden aus Mauremys leprosa und Mauremys reevesii. Marginata, 44: 60-64.
Poch, S., Sunyer, P., Pascual, G., Boix, D., Campos, M., Cruset, E. et al.. 2020. Alien chelonians in north-eastern Spain: new distributional data. The Herpetological Bulletin, 151: 1-5. https://doi.org/10.33256/hb151.15
Polo-Cavia, N., Gonzalo, A., López, P. & Martín, J. 2010a. Predator recognition of native but not invasive turtle predators by naïve anuran tadpoles. Animal Behaviour, 80(3): 461-466. https://doi.org/10.1016/j.anbehav.2010.06.004
Polo-Cavia, N., López, P. & Martín, J. 2010b. Competitive interactions during basking between native and invasive freshwater turtle species. Biological Invasions, 12(7): 2141-2152. https://doi.org/10.1007/s10530-009-9615-0
Polo-Cavia, N., López, P. & Martín, J. 2011. Aggressive interactions during feeding between native and invasive freshwater turtles. Biological Invasions, 13(6): 1387-1396. https://doi.org/10.1007/s10530-010-9897-2
Sancho, V. & Lacomba, J.I. 2016. Expansion of Trachemys scripta in the Valencian Community (Eastern Spain). In: Proceedings of the International Symposium on Freshwater Turtles Conservation. Águas e Parque Biologico de Gaia. Vila Nova de Gaia: 41-49.
Sancho, V., Lacomba, J.I., Bataller, J.V. & Pradillo, A. 2015. Manual para el Control y Erradicación de Galápagos Invasores Conselleria d’Agricultura, Medi Ambient, Canvi Climàtic i Desenvolupament Rural. Generalitat Valenciana, Valencia. Colección Manuales Técnicos de Biodiversidad, 6. Available from https://agroambient.gva.es/documents/91061501/161549814/Manual+para+el+Control+y+Erradicaci%C3%B3n+de+gal%C3%A1pagos+invasores/af90059e-5137-42f1-aabb-6a26dd699d17 [accessed 23 Jan. 2021].
Sancho, V., Lacomba, I., Bataller, J.V., Veríssimo, J. & Velo-Antón, G. 2020. First report of hybridization between Mauremys leprosa and Mauremys sinensis highlights the risk of exotic Mauremys spp. pet trade. Basic and Applied Herpetology, 34: 75-81. https://ojs.herpetologica.org/index.php/bah/article/view/186/102. [accessed 24 Jan 2021].
Vall-llosera, M. & Cassey, P. 2017. Leaky doors: private captivity as a prominent source of bird introductions in Australia. PLoS ONE, 12: e0172851. https://doi.org/10.1371/journal.pone.0172851
Woodward, D.L., Khakhria, R. & Johnson, W.M. 1997. Human salmonellosis associated with exotic pets. Journal of Clinical Microbiology, 35: 2786-2790. https://doi.org/10.1128/jcm.35.11.2786-2790.1997