Departamento De Zoología Epizoítos Y Parásitos
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DEPARTAMENTO DE ZOOLOGÍA EPIZOÍTOS Y PARÁSITOS DE LA TORTUGA BOBA (CARETTA CARETTA) EN EL MEDITERRÁNEO OCCIDENTAL FRANCISCO JAVIER BADILLO AMADOR UNIVERSITAT DE VALENCIA Servei de Publicacions 2007 Aquesta Tesi Doctoral va ser presentada a Valencia el dia 12 de Març de 2007 davant un tribunal format per: - D. Vicente Roca Velasco - D. Enrique García Raso - D. Enrique Macpherson - D. Francisco Esteban Montero Royo - Dª. Mercedes Fernández Martínez Va ser dirigida per: D. Francisco Javier Aznar Avendaño D. Juan Antonio Raga Esteve ©Copyright: Servei de Publicacions Francisco Javier Badillo Amador Depòsit legal: I.S.B.N.:978-84-370-6828-2 Edita: Universitat de València Servei de Publicacions C/ Artes Gráficas, 13 bajo 46010 València Spain Telèfon: 963864115 DEPARTAMENT DE ZOOLOGIA EPIZOÍTOS Y PARÁSITOS DE LA TORTUGA BOBA (CARETTA CARETTA) EN EL MEDITERRÁNEO OCCIDENTAL TESIS DOCTORAL Por Francisco Javier Badillo Amador Directores Francisco Javier Aznar Avendaño Juan Antonio Raga Esteve Valencia, Enero 2007 1 FRANCISCO JAVIER AZNAR AVENDAÑO, Investigador del programa “Ramón y Cajal” en el Departamento de Zoología de la Facultad de Ciencias Biológicas de la Universitat de València, y JUAN ANTONIO RAGA ESTEVE, Profesor Titular del Departamento de Zoología de la Facultad de Ciencias Biológicas de la Universitat de València CERTIFICAN: que Francisco Javier Badillo Amador ha realizado bajo nuestra dirección y con el mayor aprovechamiento el trabajo de investigación recogido en esta memoria, y que lleva por título: “Epizoítos y parásitos de la tortuga boba (Caretta caretta) en el Mediterráneo occidental”, para optar al grado de Doctor en Ciencias Biológicas. Y para que así conste, en cumplimiento de la legislación vigente, expedimos el presente certificado en Burjassot a 15 de enero de 2007. Francisco Javier Aznar Avendaño Juan Antonio Raga Esteve 2 A Raquel 3 La vida es aquello que te va sucediendo mientras estás empeñado en hacer otros planes John Lennon 4 Summary This study focussed on the epibiontes and endoparasitic fauna in the Loggerhead turtle (Caretta carretta) in the Western Mediterranean. Concerning the epizoites, 39 taxons belonging to the following phyla: Cnidaria, Annelida, Crustacea, Mollusca and Ectoprocta, were found. Only a few of them are truly specific to marine turtles, such as the balanomorph cirripeds from the Chelonibiidae and Platylepadiidae families, the harpacticoid copedod Balaenophilus sp., the hirudinean Ozobranchus margoi and the amphipod Podocerus chelonophilus. A second group of species such as the tanaidacean Hexapleomera robusta, the isopods Caprella andreae and Hyale grimaldi, and the decapod Planes minutus, are strongly associated with the marine turtles, although they have also been found in other habitats. The last group, and the greater in number, was formed by non-specific species that can colonize other inert or live substrates. These species are frequently found in the epibiont community of marine turtles. This group includes the cirripeds Lepas spp, Conchoderma virgatum, and Balanus sp; bivalve molluscs, amphipods, sedentary polychaetes, one hidrozoan and bryozoans. Some of these findings are of special interest since these species have never been found in the Mediterranean: the balanid barnacle Stephanolepas muricata, a specialist in marine turtles and the copepod Balaenophilus sp. Some species were recorded for the first time as epizoites of C. caretta, such as the mollusc Bittium sp., the isopod Idotea sp., and the amphipod Jassa sp. Furthermore, the lepadid barnacle Lepas anserifera and the bivalves Hiatella arctica and Musculus sp. were recorded for the first time as epizoites from the Mediterranean. The external wash of the loggerhead turtles studied showed a high prevalence of harpacticoid copepods of the Balaenophilidae family. A comparative morphometric study between the samples and Balaenophilus umigamecolus revealed differences indicative for a new species of the genus Balaenophilus. Since a definitive assignation has not been carried out to date and awaiting the results from studies being continued, such samples were referred as Balaenophilus sp. At the same time an updated description of B. umigamecolus, first described in Japan, was carried out. The use of SEM techniques allowed for the detection of new, previously miss- described features, as well as for the correction of others already described. Due to the controversy in the current literature referred to the feeding habits of Balaenophilus spp., a study was carried out in order to find out what type of association exist with their hosts. Thus, B. unisetus that lives in few species of Mysticetes was studied, as well as the species found in C. caretta in the Western Mediterranean, Balaenophilus sp. The examination of the digestive contents using SEM and immuno-histochemistry techniques, as well as the histopathological study of the injuries associated with Balaenophilus sp., suggested that both species feed on host tissue formed mainly of keratin. The exclusive association of these copepods with whales and marine turtles could be due to their ability to exploit such resource which are relatively scarce in the marine environment. At the same time, and for the first time a quantitative study of some of the limiting factors of the epizoites diversity in C. caretta was carried out. In order to avoid biases caused by the use of stranded specimens, only the presence/absence data of these species was used. Also, it was attempted to quantify the effect that the different sampling methodologies have on the outcome in order to evaluate the impact that these type of biases have on faunistic comparisons between different studies. Based on our results, the potential community of epizoites of any individual of C. caretta in the Western Mediterranean can be formed by a group of specialists (inherent to the community due to historical specialization factors) and a group of non specific species settling on floating substrates (more variable group and dependent on geographical factors). In 5 contrast to studies done in the western Atlantic coast, positive associations were found between the biotic colonization interactions in specialists species and neutral associations in the case of non specialist, in our study area. We did not find exclusive interactions between species. Moreover, we found that the presence of algae of the genus Polysiphonia determines the presence of a group of three frequent specialist species, the malacostraceans Caprella andrene, Hyale grimaldi, and Hexapleomera robusta. Also, the positive relation between the loggerhead turtle size and the number of species of epizoites was statistically confirmed. Finally, the analysis results also suggested a seasonal effect on the species quantity, although this should be confirmed with a larger sample size. Looking at the endoparatites, a total of 10 species of helminths were found, all of them occurring in the digestive tract; 8 digenean trematodes (Enodiotrema megachondrus, Calycodes anthos, Hemiuroidea spp., Pachypsolus irroratus, Rhytidodes gelatinosus, Orchidasma amphiorchis, Plesiochorus cymbiformis, Pleurogonius trinocephalus) and 2 nematodes (Kathalania leptura and Anisakis sp. type I). Apart from Hemiuroidea spp. and Anisakis sp., which are both considered accidental parasites, the rest are marine turtle specialists. The study of the diversity of the gastrointestinal helminth communities of C. caretta showed that these communities formed an isolated system for the exchange of parasites with other marine vertebrates. In the Western Mediterranean the loggerhead turtle should sustain their specialist parasitic fauna since it does not have any exchange with other marine turtles. At the individual level (infracommunity), the loggerhead turtles have very depauperate parasite communities, being formed by species that appear in low prevalence, despite their specialist status. This could be due to the turtle’s ectotermic character, great vagility and wide diet. The comparative analysis of the composition and structure of the helminth communities from two groups of turtles from different origin did not reveal differences, although their diet showed significant differences in at least two groups of preys of great numeric importance, pelagic tunicates and teleosts. It is suggested that this pattern is possibly explained because the digeneans which are specialists on marine turtles use gastropods and/or bivalves as intermediate hosts. Actually some relation (somehow weak) was found between the parasitic fauna and this type of preys. 6 RESUMEN En el presente trabajo se ha realizado un estudio de la fauna de epibiontes y endoparásitos de la tortuga boba (Caretta caretta) en el Mediterráneo occidental. En el apartado de epizoitos, se ha encontrado un total de 39 taxones pertenecientes a los filos Cnidaria, Annelida, Crustacea, Mollusca y Ectoprocta. De ellos, solo un pequeño número son verdaderos especialistas de tortugas marinas, como los cirrípedos balanomorfos de las familias Chelonibiidae y Platylepadiidae, el copépodo Balaenophilus sp, el hirudíneo Ozobranchus margoi y el anfípodo Podocerus chelonophilus. Un segundo grupo de especies presenta un grado de asociación muy alto con las tortugas marinas, aunque también se han hallado en otros hábitats, como el tanaidáceo Hexapleomera robusta, los isópodos Caprella andreae y Hyale grimaldii, y el decápodo Planes minutus. El último grupo, y mas numeroso, se halla compuesto por especies generalistas que pueden colonizar otros sustratos