DOI: 10.2478/s11686-014-0232-4 © W. Stefański Institute of Parasitology, PAS Acta Parasitologica, 2014, 59(2), 259–262; ISSN 1230-2821 Presence of the leech Placobdella costata in the south of the Iberian Peninsula David Romero, Jesús Duarte*, Lucía Narváez-Ledesma, Miguel Ángel Farfán and Raimundo Real Grupo de Investigación Biogeografía, Diversidad y Conservación. Departamento de Biología Animal, Facultad de Ciencias, Universidad de Málaga, 29071 Málaga, Spain Abstract Placobdella costata is a leech specific to freshwater turtle Emys orbicularis. Both genera are native to North America and have co-evolved and undergone dispersion through the Palearctic. The leech is present throughout the Mediterranean area, always associated with E. orbicularis. Their only known presence in the Iberian Peninsula is in the north and center of the peninsula. Here we present the first description of the leech in southern Spain (Andalusia) in association with a small fragmented population of fresh-water turtles in which E. orbicularis and Mauremys leprosa coexist. Unusually, the leech was found attached to the carapace of a male M. leprosa. Keywords Hirudinida, ectoparasite, freshwater turtles, southern of Spain Introduction Most leeches are bloodsucking ectoparasites, most species being parasitic on vertebrates (Sawyer 1986). However, some species have become specialized on very specific hosts. Whereas most leeches of the genus Placobdella (Hirudinida: Glossiphoniidae) have mainly been recorded on fish, amphibians, crocodiles and turtles, Placobdella costata primarily feeds on the blood of freshwater turtles (Sket and Trontelj 2008, Bielecki et al. 2012). It may facultatively feed on the blood of birds and mammals (Sapkarev 1964). Thus, P. costata is the only Palearctic leech that feeds on reptilian blood and mainly on Emys orbicularis. According to Siddall et al. (2005) the genus Placobdella is a North American clade and the only exception is P. costata that is also found in Europe. Similarly, the genus Emys is of American origin and probably underwent dispersal to the Paleartic region during the Tertiary (Siddall et al. 2005). Fossil records and genetic data suggest that P. costata could have arrived in Europe attached to Emys in the early Miocene (Fritz 1998; Lenk et al. 1999). Currently, P. costata is a widely distributed leech in the European Mediterranean area. It occurs from the Iberian Peninsula to the Balkan Peninsula and the Black Sea coast (Bielecki et al. 2012). It is also ranges from Morocco to Iran and the northern Caucasus (Saglam 2001). In the Iberian Peninsula there are only two records of P. costata, both of them describes this species on the European pond turtle E. orbicularis (Ayres and Alvarez 2008). These authors found that, in central and northern Spain, this leech was always attached to the plastron of juvenile E. orbicularis. Although the presence of Placobdella spp. in southern Spain (Andalusia) has been recently reported, the exact details of their location and host are not yet known (Domínguez 2012). Therefore, the presence of this leech in the south of the Iberian Peninsula is likely but not well documented. P. costata reproduces in summer (Sawyer 1986) although its life cycle has not been studied completely. The species displays parental care, another characteristic feature of specialists (Bielecki et al. 2012). Individuals take care of embryos or young outside the hosts. Leeches are most commonly found on turtles inhabiting lakes and ponds. They prefer places in the shallowest parts of the littoral zone, with dense vegetation (Sapkarev 1964) where they probably wait for potential hosts. Whereas other species of Placobdella leeches have been observed feeding from the blood sinuses of the plastron and carapace bones of turtles (Siddall and Gaffney 2004), P. costata are usually attached to the neck and groin regions, where the skin is thin and unarmoured, or to the middle part of the plastron (Ayres and Alvarez 2008; *Corresponding author: [email protected] Unauthenticated Download Date | 6/17/17 10:05 PM 260 Bielecki et al. 2012). There is no description in the literature of the P. costata leech feeding from the carapace of E. orbicularis, where it is probably more difficult to locate blood sinuses. On the other hand, P. costata has only been reported as feeding on a freshwater turtle species other than E. orbicularis in Asia, where it is parasitic on Mauremys caspica (Bielecki et al. 2012). In this communication, we present the first description of a Placobdella leech attached to and feeding on the carapace of Mediterranean pond turtle Mauremys leprosa. As far as we know, this is also the first time a Placobdella leech has been found on a Mediterranean pond turtle in the Iberian Peninsula as a result of a systematic sampling (but see Domínguez 2012). Materials and Methods Between May 2011 and June 2013, we have been capturing and marking freshwater turtles in the Grazalema (UTM 30STF97) and Los Alcornocales (UTM 30STF85) Natural Parks (Fig. 1) using crab creels. Samplings were carried out in four different seasonal ponds of no more than 0.5 hectares, one river course and one small marsh, all of them located in David Romero et al. the province of Málaga (Andalucía, south of Spain) where E. orbicularis is very scarse. All the area is surrounded by cork oaks Quercus suber and gall oaks Quercus faginea forest. The ponds have a maximum depth of 50 cm, but the creels were installed in a shallower part (20 cm). The ponds also have a dense but narrow border of grasses and reeds. E. orbicularis and M. leprosa coexist in the ponds forming one of the only two populations of E. orbicularis in Málaga province. The sampling effort involved 156 hours-observer and an average of 3 observers per capture day. The creels were installed at dusk and recovered at dawn the next day. Results We captured 92 turtles (10 E. orbicularis and 84 M. leprosa). Only one of the specimens caught had a Placobdella leech attached to its body (Fig. 2). This specimen was an adult Mauremys leprosa that was caught in the smallest seasonal pond, at Grazalema Natural Park. We did not detect any other external parasite in the samples. We tried to extract the leech of the turtle caparace. However, it was firmly affixed and we checked that its proboscis was into the turtle body, inserted in the junction between two caparace shells. Fig. 1. Location of the study area. Los Alcornocales and Sierra de Grazalema natural parks (south of Spain, Andalusia) and capture area in ponds in Los Cucaderos (Sierra de Grazalema, Montejaque, Málaga). The leech was captured at one of the ponds of Los Cucaderos (Sierra de Grazalema natural park) Unauthenticated Download Date | 6/17/17 10:05 PM 261 Leeches in Mediterranean turtles Fig. 2. Male Mauremys leprosa with a Placobdella costata leech attached to its carapace Discussion Two hypotheses have been proposed regarding the coexistence of turtles and leeches: (1) The intensity of the invasion by the leech may be related to their preference for attaching to female turtles with greater length and body weight (Bielecki et al. 2012); this is probably due to the coincidence between the leech reproduction period and female turtles migrating to breeding grounds, thus favouring the leeches dispersing to new water bodies. In our case, despite it being the breeding period, the leech was attached to a large male; and (2) The other hypothesis suggests that bottom-dwelling species are more affected by leeches (Ryan and Lambert 2005). Both E. orbicularis and M. leprosa inhabit muddy bottom areas and although we detected this leech in the pond, it was only attached to M. leprosa. This fact may be explained by the different density of the two species of turtles in the area. Whereas M. leprosa is very abundant (89.4% of captures), E. orbicularis appears to be less abundant (10.6% captures and only 2 recaptures in 3 years). The fact that only one leech was found attached to a turtle out of almost 100 captured turtles and that the parasitic load per turtle is usually high (up to thirteen leeches attached to one female reported by Ayres and Alvarez 2008) suggests that the prevalence of the parasite in the area is low. This fact is consistent with the density and distribution of Emys orbicularis in this southern area. This species presents a very low density metapopulation distribution pattern. Furthermore, this area forms one of the borders of the distribution area of the European pond turtle in the south of Spain. However, taking into account that E. orbicularis is the preferred host of P. costata, the detection of one leech on an M. leprosa specimen suggests that may be more leeches in the area (see Domínguez 2012). Host-parasite population dynamics studies usually assume that transmission rates linearly increase together with host population growth (density-dependent transmission, i.e. social contacts). However, other types of density-independent transmission (sexual contacts) may occur that can have an impact on both the host and parasite populations (Ryder et al. 2007). In this case, small fragmented populations could be more vulnerable to parasites. Both E. orbicularis and M. leprosa are threatened species according IUCN criteria adapted to Spain (Pleguezuelos et al. 2004) and thus the turtle population studied could be considered candidates for conservation. In this regard, the work of Lyles and Dobson (1993) could be of relevance as they suggested that the issue of parasitism should be integrated in survival and recovery plans for threatened species. Finally, we recommended further research on the host-parasite relationship in the case of Emys and Placobdella in the Iberian Peninsula, and the long-term monitoring of Unauthenticated Download Date | 6/17/17 10:05 PM 262 southern populations to determine the real prevalence of the leech in both E. orbicularis and M. leprosa populations. Acknowledgements. D. Romero was supported by a grant from the Ministerio de Educación: AP2007-03633. This study was also supported by project CGL2009-11316 (Ministerio de Ciencia e Innovación, Spain, and FEDER). Captures and marking of freshwater turtles were authorized by Consejería de Medio Ambiente de la Junta de Andalucía References Ayres C., Alvarez A. 2008. On the presence of Placobdella sp. leeches on Emys orbicularis. Acta Biologica Universitatis Daugavpiliensis, 8, 53–55. Bielecki A., Cichocka J.M., Jablonski A., Jelen I., Ropelewska E., Biedunkiewicz A., Terlecki J., Nowakowski J.J., Szlachciak J. 2012. Coexistence of Placobdella costata (Fr. Muller, 1846) (Hirudinida: Glossiphoniidae) and mud turtle Emys orbicularis. Biologia, 67, 1–8. DOI: 10.2478/s11756-012-0069-y. Domínguez J. 2012. Placobdella sp. In: Biodiversidad Virtual/Invertebrados. http://www.biodiversidadvirtual.org/insectarium/Placobdella-sp.-img365014.search.html. Fritz U. 1998. Introduction to zoogeography and subspecific differentiation in Emys orbicularis (Linnaeus, 1758). In: (Eds. U. Fritz, U. Joger, R. Podloucky, J. Servan). Proceeding of the EMYS Symposium Dresden 1996, Germany, 1–27. 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