Some parasitic copepods of selected Teleost and Chondrichthyan fishes from the Tunisian gulfs

The examination of 415 specimen belonging to twelve species of Teleostean fish and 339 specimen belonging to seven species of Chondrichthyan fish collected from the Tunisian coasts, it enabled us to identify 10 species of parasitic copepods: Lernaeopoda galei, Lernaeocera lusci, Neobrachiella merluccii, Hatschekia mulli, Caligus elongatus, Caligus pageti, Neobrachiella mugilis, Clavellotis fallax, Clavelissa pagri and Clavelissa scombri. The distribution of copepods identified, varies from one host species to another. Merluccius merluccius and Liza saliens present the important number of copepods species. The copepod Hatschekia mulli is the most abundant. The presence of Lernaeopoda galei on Scyliorhinus canicula, Mustelus mustelus and Mustelus punctalatus was reported for the first time in the southern banks of the Mediterranean.


INTRODUCTION
Copepods are common parasites of marine fishes and have been reported from a great range of depths (Boxshall, 1998).This group of ectoparasites exhibits an astounding variety of lifestyles, host associations and morphology, to the extent that their crustacean affinities may be obscured (Huys et al., 2007).More than 2000 species of copepods parasitize marine and freshwater fishes and most are ectoparasitic: they are found all over the external body surface of the host as well as in more sheltered microhabitats that are permanently directly connected to the external environment, including the external nares, the eyes, the oral and branchial cavities, the gills and the cloaca (Rosim et al., 2013).Many copepod parasites negatively affect the appearance and reduced production of species of economically important fish, both from the wild and fish farms, thus making them difficult to market (Aladatohun et al., 2013).It is important to mention that in addition to their impact on host demographics populations, parasites also influence the ecosystem processes that are diverse as competition, migration and speciation of the hosts (Kaouachi et al., 2010).
Copepods parasites have been studied extensively in the world and in Tunisian coast, where they have become pests of Teleost fish species of commercial importance (Kabata, 1958;1984;Faliex and Morand, 1994;Sasal et *Corresponding author.E-mail: feriel.youcef@yahoo.fr. Author(s) agree that this article remains permanently open access under the terms of the Creative Commons Attribution License 4.0 International License  al., 1996).
However, little is known of the diversity of parasitic copepods of Chondrichthyan fishes.The aim of this work is to analyze species of copepods parasitic richness, study copepods specificity and evaluate host epidiomogical characters by calculating infestation parameters.These features will be compared with other studies.

MATERIALS AND METHODS
A total of 415 specimens belonging to twelve species of Teleostean fish and 339 specimens belonging to seven species of Chondrichthyan fish were collected from 4 different Tunisian gulfs: Bizerte, Tunis, Hammamet and Gabès (Figure 1).The host species was identified using the method of Fischer et al. (1987) and Froese and Pauly (2014).Collected copepods were immediately removed from the hosts and preserved in 70% ethanol.Subsequently, specimens were cleared in lactic acid for 2 h prior to examination using stereo and light microscopy.Specimens were dissected on glass-slides and mounted as temporary preparations in lactophenol under a dissecting microscope.Measurements were made using an ocular micrometer.The drawings were made with the aid of a drawing tube.The data, the sampling area, the name and the size of host fish and the position of the parasite were noted.
Parasites species identification was based on morphological features according to Yamaguti (1963), Kabata (1979) and Ho and Kim (2004).The terms prevalence, mean intensity and abundance were used as defined by Margolis et al. (1982) and Bush et al. (1997) (Figure 1).
The hosts, the number of examined fish, the number of the infected fish, the parasitic indices (Prevalence (P), Intensity (I) and Abundance (A)) of each species of copepod were calculated, the specificity and the site of fixation are registered in Table 1.

Parasite spectrum
The examination of the whole fish species enabled us to collect 10 species of parasite copepods of which eight are hosted by Teleost fishes and two others are found in Chondrichthyan fishes (Table 1) (Figures 2 to 11).

Parasitic specificity
The study of parasitic specificity revealed that 3 of the species are O.Oixenous.However, 5 are S. stenoxenous.C. elongatus and L. galei are E. Euryxenous (Table 1).

Epidemiological characteristics of copepods species:
Our results (Table 1) show that, the distribution of  parasitological indices varies from one species to another.The important values of prevalence are observed in M. barbatus (P=29.3%),followed by S. auratus (P=13.33%),Liza saliens (P=10.8%)and M. merluccius (P=10%).However, all other copepods are less frequent and their prevalence is always lower than 10%.Furthermore, the maximum values of intensity is recorded in S. scombrus (I=1.5).M. barbatus shows the highest abundance (A= 0.29) (Figure 12 and Table 1).

Analysis of richness of parasites per family
The analysis of the parasitic richness indicate that the family of Lernaeopodidae present the highest richness (MSR= 6) and the lowest one is recorded on Hatschekiidae (MSR=1) (Figure 14).
Merluccius merluccius and Liza saliens present the highest number of parasitic species (2).In Tunisia, the highest parasitic diversity was mentioned by Benmansour and Ben Hassine (1997)

2010).
However, we found only two species of copepods on Chondrichthyan fish.The study of Essafi (1984) on Chondrichtyan fishes in Tunisian waters allowed in the collection of 22 different species of copepods.Nevertheless, we report for the first time the occurrence of Lernaeopoda galei on Scyliorhinus canicula, Mustelus mustelus and Mustelus punctalatus on the southern banks of the Mediterranean.This can be explained by the scarcity of studies on parasitic copepods of Chondrichthyan fish in this part of the Mediterranean.L. galei parasite in several Chondrichthyan fish species was never harvested on M. punctalatus.This is the first mention of this copepod on this host fish.
The phenomenon of host specificity is the extent to which a parasite is restricted in the range of hosts it utilizes.Levels of host specificity can range through a continuum from high, with the parasite species occurring on only a single host species, to low, with the parasite species occurring on a wide range of phylogenetically unrelated host species (Boxshall, 1998).
The data concerning the dominance of stenoxenous species was different from the results recorded by Raibaut et al. (1998) and Benmansour and Ben Hassine (1997).Those authors showed that the large majority of copepod species are oioxenous.This difference between our results and those of the other authors is probably explained by the small taxonomical and geographical scale of our study.Sasal (1997) proved that studies conducted at different scales may lead to opposite conclusion.

Conclusion
Finally, it is very interesting to note that copepod species      can cause serious fish diseases, even though they present low parasitic indices.According to Company et al. (1999) and Athanassopoulou et al. (2001) parasites that have a low prevalence and abundance and minor pathological effects on their hosts in the wild can easily spreads in populations, confined to rearing systems and causing serious outbreaks of epizootic diseases.Therefore, further investigations are still needed to deepen our knowledge of these ectoparasites of Teleost and Chondrichthyan fish.

Figure 1 .
Figure 1.Location of the study.

Figure 1 :
Figure 1: Location of the study

Table 1 .
Fish species with their epidemiological characteristics, found to be infested by parasitic copepods.