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Digenean Parasites of Labrid Fishes (Labridae: Symphodus) from Turkish Coasts of the Black Sea: New Records

©Copyright 2021 The Author(s) Available online at https://dergipark.org.tr/ase ABSTRACT In the present study digenean parasite faunas of four labrid fishes, Symphodus tinca, S. rossali, S. cinereus and S. ocellatus were investigated and compared. A total of 52 fish specimens were caught on the Black Sea coast near Sinop, Turkey, over two years. Eight digenean species were found in the four labrid fishes. These are Helicometra fasciata, Gaevskajatrema perezi, Proctoeces maculatus, Phyllodistomum crenilabri, Galactosomum lacteum, Condylocotyla pilodora, Metadena pauli and Opecoelidae gen. sp. Each digenean species on their respective hosts were counted, their prevalence, mean intensity and abundance values were determined. While the maximum parasite diversity was found in S. tinca, S. ocellatus was infected with the fewest parasites. Total parasite abundance was significantly high in S. roissali, which was infected with four species. A close resemblance was observed in the digenean parasite faunas of S. tinca and S. roissali. The core, secondary, satellite, and rare species in the digenean parasite community of each host were determined. This study contains the first data on the digenean parasites of labrid fish on Turkish Black Sea coast. Phyllodistomum crenilabri and Metadena pauli are new parasite records in Turkish fish parasite fauna, while Condylocotyla pilodora is a new parasite record for the labrid fishes.


INTRODUCTION
The family Labridae is one of the large taxons of fish, comprising approximately 580 species in 82 genera and they are widely dispersed in tropical and temperate marine waters around the world (Hanel, Westneat, & Sturmbauer, 2002). A total of 20 species of this family have been recorded from the Turkish Sea to date (Bilecenoğlu, Kaya, Cihangir, & Çiçek, 2014). A total of 5 out of 8 species of this family, which inhabit the Black Sea, are the species of the Symphodus genus. The native habitats of the genus Symphodus are the coastal zones of the East Atlantic Ocean, the Mediterranean and the Black Sea. They are found to a depth of 1-50 m near rocks and eel-grass beds. Labrid fish are not target species commercially. However, labrid fish are often caught by fishermen that focus on fishing for other species (Choat & Bellwood, 1998;Nelson, 2006). Digenean parasites provide important information about the aquatic ecosystem since they have complex life cycles, during which several groups of marine animals are used as intermediate hosts. There are a lot of published data on digenean parasites of labrid fishes from the Mediterranean and Black Sea (Sey, 1970;Nikolaeva & Solonchenko, 1970;Parukhin, Naidenova, & Nikolaeva, 1971;Gaevskaya & Solonchenko, 1989;Campos, Carbonell, & Pellicer, 1990;Campos & Carbonell, 1994;Sasal, Niquil, & Bartoli, 1999;Korniychuk, 2001;Bartoli, Gibson, & Bray, 2005;Gargouri, Elbohli, & Maamouri, 2010;Radujkovic & Sundic, 2014;Munoz & Diaz, 2015).
The aim of this research study is to investigate digenean parasites of four labrid fishes collected from the Sinop coast of the Black Sea. This study is the first survey on digenean parasites of the labrid fishes on the Turkish Black Sea coast.

MATERIALS AND METHODS
The present study was carried out between May 2015 and April 2017. The fish specimens were sampled with gill nets by fishermen from the Sinop coast of the Black Sea (42°01′ 55′ N, 35°16′ 36′ E). The caught fish were transported to the parasitology laboratory of the Faculty of Fisheries and Aquatic Sciences at Sinop University. A total of 52 specimens of the four labrid species, Symphodus tinca (27), S. cinereus (16), S. roissali (7) and S. ocellatus (2) were investigated for the digenean parasites. The fish were examined within 24 h of capture. At necropsy, the fishes were measured and weighed. Skin, fins, gills, eyes, brain, liver, stomach, intestine, kidney, urinary and gall bladder were examined under the dissecting microscope. The number of parasites was counted individually and the site of infection was recorded. Parasite specimens were studied in both alive and permanent preparations. For identification, the parasites were fixed in Bouin's fluid between slide and coverglass without pressure, stained with acetic carmine and mounted in Canada balsam. Permanent preparations were examined using a light microscope (Olympus microscope BX53) at magnification X10 and X100. The prevalence (P, %), mean intensity (MI), and abundance (A) values of each digenean parasites were calculated following the definitions of Bush, Lafferty, Lotz, & Shostak, (1997). The standard deviation (SD) of the mean intensity was calculated. The Kruskal-Wallis test (Nonparametric ANOVA) was performed to compare the mean intensity values of digenean parasites in each fish host. The analyses were carried out using the computer programmes GraphPad Instat 3.0. P-values less than 0.05 were considered to be significant. The significance of the digenean parasite fauna was determined by using an abundance (A) index according to the scale presented in Zander, Reimer, Barz, Dietel, & Strohbach, (2000), as follows; A>2: core species, A=0.6-2: secondary species, A=0.2-0.6: satellite species, A<0.2: rare species. The Czekanowski-Sørensen Index (ICS, %) was used to compare the digenean faunas of four Symphodus spp. (Sørensen, 1948).

RESULTS AND DISCUSSION
In the present study, a total of eight digenean parasite species including adults of Helicometra fasciata, Gaevskajatrema perezi, Proctoeces maculatus, Phyllodistomum crenilabri and metacercariae of Galactosomum lacteum, Condylocotyle pilodora, Metadena pauli and Opecoelidae gen. sp. were determined in four labrid fish (Table 1 and Figure 1). Table 2 summarises the digenean parasite list with indications of prevalence (%), mean intensity (MI), and abundance (A) values of identified digenean parasites in their respective fish hosts. Our results showed that S. tinca has the richest digenean fauna with 7 digenea species, but S. ocellatus was infected with only 2 digenea species (Table 2). In other words, the most diverse digenean fauna was found in S. tinca; S. ocellatus showed a low diversity with 2 species (Table 2). In this study, the parasite species richness observed in labrid fish may be related to sampling effort. Many more specimens of S. tinca (27 individuals) were examined, compared to S. ocellatus (2 individuals).
The overall mean intensity values of digenea parasite species varied significantly among the four labrid fish (P<0.05). Overall, the highest prevalence and mean intensity values (100% and 73.86) were found in S. roissali, which was infected with 4 digenea species. Galactosomum lacteum occurred only in S. tinca and Condylocotyle pilodora occurred only in S. cinereus ( Table 2).
Metadena pauli was observed as a core species, but G. lacteum and C. pilodora were found as rare species (Table 2). Helicometra fasciata and G. perezi played the role of core in S.tinca and S. roissali. Proctoeces maculatus played the role of core, satellite or  rare parasite depending on the host species. Phyllodistomum crenilabri was core in S. tinca, but secondary in S. ocellatus (Table  2). Moreover, all digenean species found in S. roissali were determined as core species (Table 2).
The digenean species composition and the digenean species richness of the four labrid fishes were found to be different in the present study. A close similarity was observed in the digenea fauna of S. tinca and S. roissali (ICS = 80.0%) ( Table 3). In this study, it was observed that the similarity among the digenean parasite fauna of the Symphodus species was low in general. Moreover, a similarity was not detected in digenea parasite fauna of two of the labrid fish, S. cinereus and S. ocellatus (Table 3).
A high Czekanowski-Sorensen index, indicating a close similarity, was observed in the digenean parasite fauna of the S. tinca and S. roissali (80%). But the digenea fauna of S. cinereus and S. ocellatus were not similar in the present study (Table 3). This may be related to the diet of the labrid hosts. The composition of the parasite fauna depends on many factors. The type of diet is one of them. This may be related with the diet of the labrid hosts. S. cinereus is carnivorous with a slight tendency toward omnivory, mostly consuming polychaetes, foraminiferans and decopod non-crustaceans (Fernandez, Freire, & Gonzalez-Gurriaran, 1995). Whereas S. ocellatus is omnivorous, tending toward herbivory, mostly consume algae, and to a lesser extent bryozoans and hydroids (Kabasakal, 2001).
According to previous studies, it should be considered that the majority of the listed digenea species have been reported from S. tinca (Table 4).
Labridae is one of the most important families of marine fish with its biological diversity and ecological importance, and labrid fishes have distribution worldwide (Nelson, 2006). To date, a total of 134 records of digenean parasites have been enlisted from 127 labrid fish (Munoz & Diaz, 2015). So far, 35 nominal digenean species have been reported in the four labrid fishes in the Mediterranean basin and Black Sea according to data of various authors (Table 4). Four species, H. fasciata, P.maculatus, P. acceptum and G. perezi, are typical digenean parasites of the labrid fishes and have also been reported in both basins (Table 4). Considering the number of digenea species reported in the four labrid fishes, except for the digenea species reported in both basins, it is noteworthy that the species diversity in the Mediterranean basin (19 species) is higher than from the Black Sea (9 species) ( Table 4). The difference in di-   Gaevskaya & Solonchenko (1989), 10. Campos, Carbonell, & Pellicer, (1990), 11. Reversat & Silan (1993), 12. Campos & Carbonell (1994), 13. Bartoli & Bray (1996), 14. Bartoli & Boudouresque (1997), [15]. Korniychuk & Gaevskaya (1999), 6. Sasal, Niquil, & Bartoli, (1999), 17. Bartoli, Morand. Riutort, & Combes, (2000), [18]. Korniychuck (2001), 19. Bartoli, Gibson, & Bray, (2005), 20. Oğuz & Bray (2006) versity of digenean parasites reported from the Mediterranean basin and Black Sea may be related to the number of the intermediate hosts and the variation in physical and chemical parameters of the environment that can influence the host. So far, Condylocotyle pilodora has not been previously recorded in labrid fishes. It is remarkable that this digenean parasite is reported for the first time in labrid fish in the present investigation (Table 4). Thus, the number of digenean parasite species in the four labrid fishes reported in both basins has increased to 36 with the addition of C. pilodora.

CONCLUSIONS
This study revealed the first data on the digenean fauna of four fish species belonging to Sypmhodus genera in Turkish waters, and the data recovered in this paper contribute to the digenean parasites list of labrid fish inhabiting the Black Sea. In addition, these results contain some valuable knowledge, which can be used in future digenean parasite research.

Conflict of interest:
The authors declare that they have no conflicts of interest.
Ethics Committee Approval: All applicable international, national and institutional guidelines for the care and use of animals were followed. The study protocol no. 19 of 13/07/2015 was approved by the Republic of Turkey, Sinop University Experimental Animals Local Ethics committee.