Digenean species diversity in teleost fish from a nature reserve off Corsica, France (Western Mediterranean), and a comparison with other Mediterranean regions

Data on the digenean parasites of 2238 teleosts from the Scandola Nature Reserve off Corsica are presented. These represent the largest general survey of digenean parasites attempted in the Mediterranean region and is the result of major collections and systematic reports published over the past 20 years. The number of different digenean species recorded from 63 fish species was 102. Full parasite-host and host-parasite lists are presented, with information on the geographical distribution of the parasites, their site within the host and the prevalence, adundance and intensity of the infections. The digenean fauna of teleosts off Corsica is compared with that in other regions of the Mediterranean and the Black Sea. A more detailed analysis of the diversity of these parasites in sparid fishes indicates that the digenean diversity off Corsica is far greater than that in other parts of the Mediterranean.


Introduction
The present study is an attempt at a qualitative and quantitative approach to the study of the digenean fauna of marine teleosts from the Western Mediterranean. The study area is the Scandola Nature Reserve, located on the most western part of the coast of northern Corsica,France (42u239N,8u339E). This nature reserve extends all along a steeply sloped, rocky, high-energy shore, widely exposed to the open sea, and is almost devoid of calm or euryhaline waters. This study is the result of a long research period, which began in 1986. During this period, numerous data have been published concerning the identification of the digeneans collected in teleosts from the Scandola Reserve (Bartoli 1987; Bartoli and Bray 1987, 1990Bartoli et al. 1988Bartoli et al. , 1989aBartoli et al. , 1989bBartoli et al. , 1989cBartoli et al. , 1989dBartoli et al. , 1993Bartoli et al. , 1994Bartoli et al. , 2000aBartoli et al. , 2000bBartoli et al. , 2003aBartoli et al. , 2003b; Bartoli and Gibson 1989, 1991, 1998Gibson and Bray 1989;Holmes and Bartoli 1993;Bray and Bartoli 1996;Le Pommelet et al. 1997;Jousson and Bartoli 1999Sasal et al. 1999;. Table I. Digenean species collected from teleost fishes off Scandola Nature Reserve in family order and their distribution (recent references with useful descriptions or illustrations are provided).
For each host species and for each of their digenean species, various parasitological indices and information on the site of the parasites are presented in Table II. This table shows that some digeneans were very prevalent and abundant, while others were very rare. With regard to the sites used by the parasites, all available niches were used by digeneans in Gaidropsarus mediterraneus, Mullus surmuletus, Scorpaena porcus and Serranus scriba. For all other hosts, some sites were never used, these usually being the stomach and gall-bladder. Nevertheless, the stomach only was occupied in Gobius cobitis, G. cruentatus, Salaria pavo and Spicara maena.
Some digenean species were very restricted in their distribution and were limited, for example, to: (1) the stomach for Arnola microcirrus, Hemiurus luehei, Lecithochirium fusiforme, L. grandiporum, L. rufoviride and L. musculus (nevertheless, single individuals of L. musculus were found in the pyloric caeca of Serranus scriba, the middle intestine of Mullus surmuletus and in the posterior intestine of Symphodus tinca-according to Gibson and Bray (1986), L. musculus can occur in a range of teleosts which feed on gobies that harbour gravid worms in their body cavity; these accidental hosts may have these worms, at least temporarily, in the intestine); (2) the pyloric caeca for Bucephalus marinus, Monorchis monorchis, Podocotyle
In Table III, we present a parasite-host list. Of the 102 digenean species found in the teleosts from Scandola, 55 were oioxenic (53.9%), 13 stenoxenic (12.7%) and 34 (33.3%) euryxenic (terminology of Euzet and Combes 1980). Of the 34 euryxenic species, nine were restricted to sparids (five digenean species found in two hosts, three in three hosts, one in six hosts), 17 were parasites of two to five unrelated fish host species, six of six to 10 unrelated hosts and two of .11 unrelated hosts. These latter two cases refer to Lecithochirium musculus and forms of Helicometra (which will probably prove to be a species complex).
With the exception of the nine euryxenic species found in sparids, all of the other 25 euryxenic species are found in unrelated fish families. Among these 25 euryxenic digeneans: 14 parasitize fish hosts belonging to two different families, six parasitize fish hosts belonging to three different families, two parasitize fish hosts belonging to four    different families, one parasitizes fish hosts belonging to five different families, one parasitizes fish hosts belonging to nine different families and one parasitizes fish hosts belonging to 12 different families. Nevertheless, two digenean species are found in the family pair Congridae-Lophiidae, two others are in the pair Triglidae-Lophiidae and two others in the Labridae-Sparidae-Blenniidae. For these euryxenic species, the relationships between the parasites and their hosts probably have an ecological basis (e.g. foodwebs).
In Table IV, we compare the data collected from each teleost species studied in the Scandola Nature Reserve with those reported from the same teleost species in other areas of the Mediterranean and the Black Seas. Such a comparison is not easy because: (1) the sample size varies; and (2) the digenean species reported are sometimes different. In this study, the validity and synonymy of the different digenean species reported by the various authors are not discussed.
In a specific geographical area, the ratio of the total number of the digenean species found in all fish species studied (N) to the number of fish species examined (N9), which corresponds to the mean number of digenean species per host species, i.e. M5N/N9, is a reflection of digenean species diversity. Table IV shows that the highest ratio (3.8) is observed off the Scandola Nature Reserve. By contrast, the lowest ratio is reported for the Adriatic (1.9; 2.0; 0.6: the last value could be wrong due to the nature of the data provided by Radujkovic and Raibaut 1989), while an intermediate situation is observed for the Eastern Mediterranean (2.6; 2.9; 2.1).

Digean species diversity in teleosts
the north-western coast of Italy (Table IV). These two places are not widely distant and the striking contrast appears not to be related to sampling effort, since the sample numbers are similar in these two areas (2238 fish for Scandola 2110 for the north-western coast of Italy).
As an example, eight digenean species were found in 69 specimens of three Trachurus spp. from Scandola (i.e. 27 T. mediterraneus+17 T. picturatus+25 T. trachurus569; often these three species are reported as 'T. trachurus'), but only two from 66 along the western coast of Italy. For a particular host fish, the number of digenean species recovered tends to increase in step with the sample size. Nevertheless, we have found seven digenean species in three Conger conger from off Scandola, while only one has been reported in 106 C. conger from western Italy. Similarly, seven digenean species were found in 13 Dentex dentex from off Scandola, while only two were reported from 111 of these fishes from the western Italian coast. Table VI shows a comparison of the digenean fauna for the same 21 teleost species (i.e. restricted to those hosts recorded by the Italians) studied both off Scandola and the northwestern coast of Italy (see list in Table IV). The ratio value (N/N9) for off the Scandola Nature Reserve (4.8) is much higher than that for the north-western coast of Italy (2.0), even though the sampling numbers in the first area (742) are significantly lower than that of the second (2110).
The very high digenean species diversity observed off the Scandola Nature Reserve is probably related to the high general level of biodiversity reported in the region (Miniconi et al. 1990;Verlaque 1990;Merella 1991;Verlaque et al.1999). This high level of biodiversity is related to the stability of the equilibrium of the ecosystem in this wellpreserved area (protected for 25 years), which is devoid of major pollutants and opens Table V. Digenean species diversity in the well-studied sparid fishes (data from table IV).