Body Size and Ectoparasitic Infestations in the Mediterranean Pond Turtle Mauremys leprosa (Testudines, Geoemydidae) in Majen Belahriti Pond (North-Eastern Algeria)
Abstract
Morphological parameters were measured on a population of the Mediterranean pond turtle Mauremys leprosa (Schweigger, 1812) in Majen Belahriti pond in the region of Guelma (North-east of Algeria). Females exhibited a longer carapace length (CL) at 177 ± 23.85 mm, surpassing that of males (151.45 ± 31.12 mm), and they also displayed a higher body weight (BW) at 756.52 ± 243.91 g, which was notably greater than that of males (453.09 ± 224.42 g). Placobdella nabeulensis Ben Ahmed, Gajda, Utevsky, Kwist & Świątek, 2023 (Hirudinida, Glossiphoniidae) was identified as the only ectoparasite affecting M. leprosa, with an average body length and width of 11 ± 5.83 mm and 5.1 ± 2.89 mm respectively. The intensity, represented by the average number of leeches per turtle, was calculated to be 2.21 ± 1.31 for this specific population and a prevalence rate of 21.17 %. The tail region showed the highest parasite load, indicating its increased susceptibility compared to other body parts.
References
Agha, M., Ennen, J. R., Nowakowski, A. J., Lovich, J. E., Sweat, S. C. & Todd, B. D. 2018. Macroecological patterns of sexual size dimorphism in turtles of the world. Journal of Evolutionary Biology, 31, 336-345.
Araújo, P., Segurado, P. & Raimundo, N. 1997. Bases para a conservação das tartarugas de água doce, Mauremys leprosa e Emys orbicularis. Estudos de Biologia e Conservação da Natureza, 24. Instituto da Conservação da Natureza. Lisboa, 1-72.
Araújo, P. & Segurado, P., 2008. Mauremys leprosa. In: Loureiro, A., N. Ferrand de Almeida, M. A. Carretero, Paulo, O. S., eds. Atlas dos Anfíbios e Répteis de Portugal. Instituto da Conservaçao da Natureza e da Biodiversidade. Lisboa, 131-132.
Amo, L., López, P. & Martín, J. 2004. Prevalence and intensity of haemogregarinid blood parasites in a population of the Iberian rock lizard Lacerta monticola. Parasitological Research, 94, 290-293.
Bashirichelkasari, N. & Yadollahvandmiandoab, R. 2017. Placobdella costata an Ectoparasite for Mauremys caspica in North of Iran. Journal of Aquaculture Research & Development, 8, 9-10.
Bakhouche, B., Tiar, G., Djemadi, I., Draidi, K. & Daniel, E., 2019. Phenology and population structure of the Mediterranean stripe-necked terrapin Mauremys leprosa (Schweigger, 1812) in the Reghaïa Lake (Northern Algeria). Basic and Applied Herpetology, 33, 43-51.
Ben Ahmed, R., Rohdhane, Y. & Tekaya, S. 2015. Check list and Distribution of Marine and freshwater leeches (Annelida, Clitellata, Hirudinea) in Tunisia with identification key. Ecologica Montenegrina, 2(1), 3-19.
Berry, J. F. & Shine, R. 1980. Sexual size dimorphism and sexual selection in turtles (Order Testudines). Oecologia, 44, 185-191.
Bertolero, A. & Busack, S. D. 2017. Mauremys leprosa (Schoepff in Schweigger 1812) -Mediterranean pond turtle, Spanish terrapin. Mediterranean stripe-necked terrapin. Chelonian Research Monogphy, 5, 1-19.
Bielecki, A., Cichocka, J. M., Jabłoński, A., Jeleń, I., Ropelewska, E., Biedunkiewicz, A., Terlecki, J., Nowakowski, J. J., Pakulnicka, J. & Szlachciak, J. 2012. Coexistence of Placobdella costata (Fr. Müller, 1846) (Hirudinida: Glossiphoniidae) and mud turtle Emys orbicularis. Biologia, 67 (4), 731-738.
https://doi.org/10.2478/s11756-012-0069-y
Castanet, J. 1988. Les méthodes d'estimation de l'âge chez les chéloniens. Mesogée, 48, 21-28.
Campo, B. & Ruiz, E. 2019. Anfibios y reptiles de Aragón. Atlas de distribución. Guía gráfica. Consejo de Protección de la Naturaleza de Aragón, 127-130.
Campos-Such, D., Miñarro, M. & Valls, L. 2016. Localización de un ejemplar asilvestrado de Mauremys sinensis en la Comunidad Valenciana. Boletín de la Asociación Herpetológica Española, 27(1): 97-99
Custodio, E., Manzano, M. & Montes, C. 2009. Las aguas subterráneas en Doñana: Aspectos ecológicos y sociales. Agencia Andaluza del Agua, Consejería de Medio Ambiente. Sevilla, 1-240.
Da Silva, E. 2002. Mauremys leprosa. In: Pleguezuelos J. M., Márquez, R. & Lizana, M. Eds. Atlas y Libro Rojo de los Anfibios y Reptiles de España. Dirección General de Conservación de la Naturaleza. Asociación Herpetológica Española, Madrid, 143-146.
Diaz-Paniagua, C., Keller, C. & Andreu, A.C. 2001. Long-term demographic fluctuations of the spur-thighed tortoise Testudo graecain in SW. Spain. Ecography, 24, 707-721.
Díaz-Paniagua, C., Andreu, A. C. & Keller, C. 2015. Galápago leproso, Mauremys leprosa. In: Salvador, A. & Marco, A., eds. Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid.
Domènech, F., Marquina, R., Soler, L., Valls, L., Aznar, F. J., Fernández, M., Navarro, P. & Lluch, J. 2016. Helminth fauna of the invasive American red-eared slider Trachemys scripta in eastern Spain: potential implications for the conservation of native terrapins. Journal of Natural History, 50 (7-8), 467-481.
Domínguez, J. & Villarán, A. 2017. Presencia de hirudíneos sobre Mauremys leprosa. Boletín de la Asociación Herpetológica Española, 28 (1), 17-22.
Farzali, S. & Saglam, N. 2020. The status of the leech fauna (Annelida, Hirudinea) at the Eastern region of Azerbaijan. Journal of Wildlife and Biodiversity, 4 (4), 40-52.
Fediras, S., Rouag, R., Ziane, N., Olivier, A., Béchet, A. & Benyacoub, S. 2017. Prevalence of Placobdella costata (Fr. Müller, 1846) (Hirudinida: Glossiphoniidae) on the European pond turtle Emys orbicularis in North-east Algeria. Herpetological Notes, 10, 3-8.
Fraysse, N. P. 2002. Contribution à l'étude de l'Emyde lepreuse Mauremys leprosa (Schweigger, 1812). PhD thesis, Paul-Sabatier de Toulouse University.
Freedberg, S., Greives, T. J., Ewert, M. A., Demas, G. E. & Nelson, C. E. 2008. Incubation environment affects immune system development in a turtle with environmental sex determination. Journal of Herpetology, 42, 536-541.
Gálvez, Á. & Albero, L. 2017. Nuevas citas de herpetofauna en la Plana de Requena-Utiel (Comunidad Valenciana). Boletín de la Asociación Herpetológica Española, 28 (2), 26-31.
Guerdoud, O. & Benyahia, M. 2021. Structure et démographie d'une population d'Emyde lépreuse (Mauremys leprosa) dans le Lac Noir. Master thesis. Badji Mokhtar University. Annaba.
Gibbons, J. W. 1990. Sex ratios and their significance among turtle populations. In: Life History and Ecology of the Slider Turtle. Smithsonian Institution Press. Washington, D.C.
Iglesias, R., García-Estévez, J. M., Ayres, C., Acuña, A. & Cordero-Rivera, A. 2015. First reported outbreak of severe spirorchiidiasis in Emys orbicularis, probably resulting from a parasite spillover event. Diseases of aquatic organisms, 113 (1), 75-80.
Keller, C. 1997. Ecología de poblaciones de Mauremys leprosa y Emys orbicularis en El Parque Nacional de Doñana. Ph.D. Thesis, Sevilla University.
Lacaplain, B. & Noel, F. 2019. Les sangsues d'eau douce du Nord-ouest de la France (Annelida-Hirudinida) - Normandie, Bretagne, Pays de la Loire- Recherche, récolte et identification. GRETIA, UMS PatriNat AFB-CNRS-MNHN, 92 p.
Laghzaoui, E. M., Abbad, A. & El Mouden, E. L. 2020. Host-parasite association of Placobdella costata (Glossiphoniidae: Hirudinea) and Mauremys leprosa (Geoemydidae: Testudinoidea) in aquatic ecosystems of Morocco. Parasitological Research, 119, 3459-3467.
https://doi.org/10.1007/s00436-020-06809-x
Martínez-Silvestre, A., Flecha, C. & Soler, J. 2011. Observaciones de interacciones entre Trachemys scripta elegans y Mauremys leprosa en el pantano del Foix (Barcelona). Boletín de la Asociación Herpetológica Española, 23(1): 106-109
Mateo, J. A., Pleguezuelos, J. M., Fahd, S., Géniez, P. & Martínez-Medina, F. J. 2003. Los anfibios, los reptiles y el estrecho de Gibraltar. Un ensayo sobre la herpetofauna de Ceuta y su entorno. Instituto de Estudio Ceutíes. Ceuta.
Meyer, L., Du Preez, L., Bonneau, E., Héritier, L., Quintana, M. F., Valdeón, A., Sadaoui, A., Nadia Kechemir-Issad, N., Palacios, C. & Verneau, O. 2015. Parasite host-switching from the invasive American red-eared slider, Trachemys scripta elegans, to the native Mediterranean pond turtle, Mauremys leprosa, in natural environments. Aquatic Invasions, 10 (1), 79-91.
https://doi.org/10.3391/ai.2015.10.1.08
Muñoz, A. & Nicolau, B. 2006. Sexual dimorphism and allometry in the stripe-necked terrapin, Mauremys leprosa, in Spain. Chelonian Conservation and Biology, 5, 87-92.
Olivier, A. 2002. Ecologie, traits d'histoire de vie et conservation d'une population de Cistude d'Europe Emys orbicularis en Camargue. Laboratoire de Biogéographie et Ecologie des Vertébrés. Ph.D. Thesis, Ecole Pratique des Hautes Etudes.
Palacios, C., Urrutia, C., Knapp, N., Quintana, M. F., Bertolero, A., Simon, G., Du Preez, L. & Verneau, O. 2015. Demographic structure and genetic diversity of Mauremys leprosa in its Northern range reveal new populations and a mixed origin. Salamandra, 51, 221-230.
Polo-Cavia, N., López, P. & Martín, J. 2010. Competitive interactions during basking between native and invasive freshwater turtle species. Biological Invasions, 12: 2141-2152. 2011. Aggressive interactions during feeding between native and invasive freshwater turtles. Biological Invasions, 13, 1387-1396.
Pérez-Santigosa, N., Florencio, M., Hidalgo-Vila, J. & Díaz-Paniagua, C. 2011. Does the exotic invader turtle, Trachemys scripta elegans, compete for food with coexisting native turtles? Amphibia-Reptilia, 32, 167-175.
Romero, D., Duarte, J., Narváez-Ledesma L., Farfán, M. & Real, R. 2014. Presence of the leech Placobdella costata in the South of the Iberian Peninsula. Acta Parasitologica, 59(2), 259-262.
Servan, J., Zaborski, P., Dorizzi, M. & Pieau, C. 1989. Détermination du sexe ratio adulte de la tortue Emys orbicularis dans des populations provenant de 7 étangs de Brenne (Indre, France). Canadian Journal of Zoology, 67, 1279-1284.
Vamberger, M. & Trontelj, P. 2007. Placobdella costata (Fr.Müller, 1846) (Hirudinea: Glossiphoniidae), a leech species new for Slovenia. Natura Sloveniae, 9 (1), 35-40.
Yadollah, R. & Kami, H. G. 2014. Habitat changes and its impacts on the Caspianpond turtle Mauremys caspica population in the Golestan and Mazandaran provinces of Iran. Journal of Aquaculture Research and Development, 5, 1-4.