Endohelminth Fauna of Teleost Fishes from Coasts of Şile Region of the Black Sea.

A total of 508 fish specimens belonging to 19 species collected in the coast of Şile region of the Black sea were examined to detect the presence of endohelminths. Of this, 357 (70.27%) were found to be infected with parasites. 15 distinct helminths species were recovered including four species of nematodes, seven digenean species, one species of cestodes and three species of acanthocephalans. It was also determined that the species of nematode Hysterothylacium aduncum was the most common parasite and the most diverse endohelminth fauna was found in Gobius niger and Solea vulgaris, with five species. Furthermore, it should be noted that Capillaria gracilis is reported for the first time from the Turkish coasts. The infection rates, hosts, and parasites are listed in this paper.

Introduction

Fish are aquaculture resources with a significant economic value, and present essential nutrients amongst the foods of animal origin (Öztürk, 2005). Fish constantly live amongst parasites in the waters of their natural environment (Taşçi & Topçu, 1990). These parasites not only reduce the nutritional value of the fish, but also hamper their growth, reproduction, and feeding capabilities (Özan & Kır, 2005). While the majority of the parasites involved with fish present no danger to humans, it is also known that the ones harmful for humans tend to have more than one development stage (Adams ). Aquatic environments are continuously exposed to different types of waste materials, and such pollution is known to cause an increase in the prevalence of diseases and anomalies encountered in fish populations (Turgut & Özgül, 2009). Since the pollution in these environments is most often of chemical nature, the fish and other animals that act as hosts for the parasites are weakened and lose immune resistance, which in turn causes gaps in the ecological nutritional chain (Oğuz, 1996). The fact that researches focused on fish diseases has gained increased attention and importance in recent years also makes it necessary to gain more insight into the parasitic fauna of fish (Demirtaş, 2011).

This study was, therefore, performed to determine the endohelminth fauna of the fish caught from the coastal areas of the Şile region of the Black Sea.

Materials and Methods

The Study Area

This study was performed between February 2010 and December 2013 in the Şile district of İstanbul province. Şile (Fig.1) is located towards the northwest of the country, along the northeast edges of the Marmara Region, facing the Black Sea coasts of the Kocaeli Peninsula. The Black Sea is a semi-closed inland sea with an average depth of 1300 m and a total surface area of 420.000 km2. The Black Sea is also the world’s largest anoxic sea, with an oxygenated upper layer of approximately 100 – 150 meter depth, while the lower layers are anoxic and contains hydrogen sulfide (Güngör & Çağatay, 2010).

Fig. 1

Map of Şile province in which the study was performed.

Fish Material and Sample collection

The fishers of the coasts of Şile usually hunt shoreline fish. A total of 508 fish distributed over 19 species was obtained from these fishers between February 2010 and December 2013. Fish were collected either alive or as fresh dead and transported to the land inside canisters filled with seawater. The dissections of the fish were performed in the port of Şile, and one specimen from each species was reserved to perform species identification. Fish species were identified using the guidelines established by Slastenenko (1955), Geldiay (1969), and Can & Bilecenoğlu (2005). Mid-caudal lengths of the fish were measured and recorded, and the interior organs of the fish were removed by inserting a thin-point scissor into the anus and cutting towards the anterior of the fish body. To make it easier to identify any parasitic presence, the specimens were placed into a petri dish containing physiological saline. The parasites were first searched macroscopically within the body cavity and in interior organs, and any visible parasites were collected into watch-glass using pasteur pipettes to be preserved in physiological saline.

The digestive tracts of the fish were cut from the stomach to the intestines. The contents of the intestines were investigated, and the intestinal epithelium was scraped to search for the presence of any parasites. Livers were cut into small pieces, which were then grounded for microscopic evaluation. Air and gall bladders of the fish were punctured and searched for any parasites. The samples were evaluated under a binocular stereomicroscope, and any nematodes detected were collected into plastic tubes containing 70 % alcohol. The number and location of the parasites within the body were recorded along with the date, the fish species, and the parasite type and count in a sticker used as a label for the tubes, which were then stored until the slides were prepared. Other parasites, meanwhile, were placed between slide glasses and fixed using the A.F.A (Acetic acid + formaldehyde + alcohol) solution, then kept in jars containing 70 % alcohol until their permanent slides were prepared.

The permanent slides of the nematodes were prepared by placing them between the glass and cover slides and covering them with glycerine-gelatine. For the other parasite groups, the permanent mounts were prepared as suggested by Baylis (1922), Wardle (1932), Pantin (1960), Cable (1976), Bylund , and Pritchard & Kruse (1982). Parasite species were identified through the guidelines of Dawes (1947), Yorke & Maplestone (1962), Schell (1970), Fagerholm (1982), Khalil , Gibson , Jones , Yamaguthi (1955a), Yamaguthi (1955b), Yamaguthi (1955c). The prevalence, mean intensity, and mean abundance values for all parasite species were calculated as suggested by Bush .

Ethical Approval and/or Informed Consent

For this study formal consent is not required.

Results

As the endohelminths of a total of 508 fish belonging to 19 different species were inspected as part of the study, 15 different helminth species were encountered. 357 out of the 508 fish inspected (70.27 %) were found to be infected with parasites, and a total of 3813 parasites were detected amongst all the fish. 313 of the fish (61.6 %) were found to be infected with nematodes, 75 (14.76 %) were infected with Digeneans, 35 (6.88 %) were infected with Cestoda and 18 (3.54 %) were infected with Acanthocephala group of parasites. A total of 3288 Nematodes, 398 Digeneans, 81 Cestodes, and 46 Acanthocephalans were determined throughout the specimens (Table 1).

Table 1

Data for the identified parasites for each fish species.

	Parasite Type	Host	EFC	IFC	PCH	P %	MI	MA
CESTODA	Progrillotia dasyatidis	Chelidonichthys lucerna	2	2	4	100	2	2
		Gaidropsarus mediterraneus	19	11	28	58	2.6	1.47
		Gobius niger	32	11	29	34.4	2.6	0.9
		Mullus surmuletus	54	9	18	17	2	0.33
		Scorpaena porcus	46	2	2	4.3	1	0.04
DIGENEA	Helicometra fasciata	Caspialosa pontica	32	7	12	22	1.7	0.4
		Gobius niger	32	3	7	9.4	2.3	0.2
		Platichthys flesus	1	1	41	100	41	41
		Scorpaena porcus	46	27	150	59	5.56	3.26
		Solea vulgaris	8	2	13	25	6.5	1.63
	Helicometra insolata	Solea vulgaris	8	1	10	12.5	10	1.25
		Symphodus tinca	1	1	4	100	4	4
	Anisocladium fallax	Uranoscopus scaber	44	6	33	14	5.5	0.8
	Anisocladium gracile	Uranoscopus scaber	44	16	42	36	2.6	1
	Anisocoelium capitellatum	Uranoscopus scaber	44	18	73	41	4.1	1.7
	Prodistomum polonii	Trachurus mediterraneus	68	6	12	9	0.18	0.18
	Monascus filiformis	Mullus surmuletus	54	1	1	2	1	0.019
NEMATODA	Hysterothylacium aduncum	Caspialosa pontica	32	23	180	72	8	5.4
		Chelidonichthys lucerna	2	2	8	100	4	4
		Engraulis encrasicolus	33	17	115	52	7	4
		Gaidropsarus mediterraneus	19	10	103	53	10.3	5.4
		Gobius niger	32	25	268	78.1	11	8.4
		Merlangius merlangus euxinus	107	79	922	74	12	9
		Mullus surmuletus	54	13	23	24	1.8	0.43
		Sarda sarda	6	3	27	50	9	4.5
		Sciaena umbra	2	1	3	50	3	1.5
		Scorpaena porcus	46	19	115	41.3	6.05	2.5
		Solea vulgaris	8	2	57	25	28.5	7.1
		Spicara smaris	32	25	369	78.1	14.8	11.5
		Symphodus tinca	1	1	2	100	2	2
		Trachinus draco	11	10	30	91	3	2.3
		Trachurus mediterraneus	68	49	631	72.1	13	9.3
		Uranoscopus scaber	44	28	369	64	13.2	8.4
	Philometra sp.	Trachinus draco	11	1	8	9.1	8	0.73
		Trachurus mediterraneus	68	1	4	1.5	4	0.06
	Cucullanellus minutus	Solea vulgaris	8	2	10	25	29	7.1
		Symphodus tinca	1	1	13	100	13	13
	Capillaria gracilis	Gobius niger	32	2	13	6.3	7	0.4
		Mullus surmuletus	54	1	18	1.9	18	0.33
ACANTHOCEPHALA	Acanthocephaloides irregularis	Gaidropsarus mediterraneus	19	1	5	5.3	5	0.26
		Gobius niger	32	3	9	9.4	3	0.28
		Scorpaena porcus	46	9	23	20	2.56	0.5
	Neoechinorhynchus agilis	Liza aurata	9	4	6	44	1.5	0.6
	Solearhynchus kostylewi	Solea vulgaris	8	1	3	12.5	3	0.38

EFC: Evaluated Fish Count, IFC: Infected Fish Count, PCH: Parasite Count in Host, P: Prevalence, MI: Mean Intensity, MA: Mean Abundance

The only Cestoda encountered as part of the study was the Progrillotia dasyatidis, which belongs to the Progrillotiidae family. The species identified for the Digenean group are as follows: Helicometra fasciata and Helicometra insolata species belonging to the Opecoelidae family, Anisocladium fallax, Anisocladium gracile, and Anisocoelium capitellatum belonging to the Acanthostomidae family, Prodistomum polonii of the Lepocreadiidae family, and Monascus filiformis of the Fellodistomidae family. As for nematodes, the species identified consisted of Hysterothylacium aduncum of the Anisakidae family, Philometra sp. of the Philometridae family, Cucullanellus minutus of the Cucullanidae family, and Capillaria gracilis of the Capillaridae family. Finally, the species identified for the Acanhocephala consisted of Acanthocephaloides irregularis of the Arhythmacanthidae family, Neoechinorhynchus agilis of the Neoechinorhynchidae family, and Solearhynchus kostylewi of the Echinorhynchidae family (Table 1). Amongst these, Capillaria gracilis was identified for the first time in Turkey as part of the present study (Fig. 2).

Fig. 2

Capillaria gracilis.A: eggs, B: Anterior, C: Posterior (♀)

Considering the relationship with the inspected fish species and corresponding parasite species, the highest number of species of parasites was found in Gobius niger and Solea vulgaris fish species, each of which were infected with 5 different types of parasites. Scorpaena porcus, Mullus surmuletus, and Uranoscopus scaber were infected with four different species of parasites, Gaidropsarus mediterraneus, Symphodus tinca, and Trachurus mediterraneus were infected with three different species of parasites, Caspialosa pontica, Chelidonichthys lucerna, and Trachinus draco were infected with two different species of parasites, and Engraulis encrasicolus, Liza aurata, Merlangius merlangus euxinus, Platichthys flesus, Sarda sarda, Sciaena umbra, and Spicara smaris were found to be infected with only one type of parasite. The highest prevalence for the parasite species encountered as part of this study was that of H. aduncum with 84.5 %. H. aduncum was also the parasite species that infected the highest number of different species of fish (16 species). P. dasyatidis and H. fasciata share the second most prevalent distribution with 26.3 %. A. fallax, A. gracile, A. capitellatum, M. filiformis, P. polonii, N. agilis and S. kostylewi each share 5.3 % prevalence and they were each encountered only in a single species of fish.

Discussion

Until 2005, a total of 114 parasitic helminths (87 Platyhelminthes, 16 Nemathelminthes, 9 Acanthocephala, 2 Annelida) were reported in the first checklist that could be considered a report for the marine fish of Turkey, recorded as observed from 65 marine fish (Öktener, 2005). Various other researchers (Oğuz, 1996; Keser, 2002; Tuncel, 2003; Oguz & Bray, 2006; Oğuz & Kvach, 2006; Keser ; Oguz & Bray, 2008; Akmirza, 2012; Tepe & Oguz, 2013; Tepe ) have also performed different studies for the parasite fauna of the marine fish of Turkey.

For the Cestoda, the Progrillotia dasyatidis species of the Progrillotiidae family was first determined for the seas surrounding Turkey in a Gobius niger (Oguz & Bray, 2008), and was later reported to be present in Gobius niger, Uranoscopus scaber, Gaidropsarus mediterraneus, Ophidion rochei and Mullus barbatus (Tepe ). In the present study, the only species encountered for the Progrillotiidae family was Progrillotia dasyatidis, which was identified in Gobius niger, Mullus surmuletus, Gaidropsarus mediterraneus, Chelidonichthys lucerne, and Scorpaena porcus fish species.

Helicometra fasciata is known to have a high host infection spread and was reported first for Turkey in the Sea of Marmara Gaidropsarus mediterraneus, Gobius cobitis, Scorpena scrofa, Symphodus tinca, Trachurus trachurus, and Zosterisessor ophiocephalus fish species caught from the shores of Mudanya (Oğuz, 1995; Oguz & Bray, 2006). It was also reported for Pagellus erythrinus, Scorpaena porcus, Conger conger, and Trigla lucerna species caught in the Aegean Sea (Akmirza, 2000, 2001), Conger conger fish of the Gökçeada shores (Akmirza, 2012), and in the intestines of Scorpaena porcus fish species caught from the Eastern Black Sea shores (Tepe & Oguz, 2013; Tepe ). In the present study, Helicometra fasciata were encountered in Caspialosa pontica, Gobius niger, Platichthys flesus, Scorpaena porcus, and Solea vulgaris fish. The highest infection rate for this species was determined for Platichthys flesus (100 %). Another species of the Helicometra genus, Helicometra insolata, is of Atlantic origin, and this species was previously encountered in Turkey in the Marmara Sea along the shorelines of Mudanya, in Symphodus tinca (Oğuz, 1995). In the present study, this species was determined in Symphodus tinca and Solea vulgaris, and the mean intensity was found to be highest in Solea vulgaris with a value of 10.

Anisocladium fallax is the endoparasite of the Uranoscopus scaber fish, and was previously reported to be present in the Mudanya shores of the Sea of Marmara (Oğuz, 1995; Oguz & Bray, 2006), in the Gökçeada Island shores of the Aegean Sea (Akmirza, 2013), and the Eastern Black Sea shores (Tepe, 2011; Tepe ). In the present study, a total of 44 Uranoscopus scaber fish were inspected, and 6 of them were found to be infected with Anisocladium fallax. The infection rate was 14 %, and the mean intensity was determined as 5.5.

In Turkey, Anisocladium gracile was before determined in the intestines of Uranoscopus scaber (Tepe, 2011; Tepe ). The parasite was also reportedly present in the digestive tract of the same host in the Western Mediterranean Sea (Bartoli & Gibson, 2000; Bartoli ). The prevalence of this parasite in the Uranoscopus scaber caught in the Marseille shores of the Western Mediterranean Sea was reported as 72.7 %, and as 100 % in fish from the Corsican shores. The mean intensity for Marseilles and Corsica fish were reported as 15.5 and 11, respectively (Bartoli & Gibson, 2000). In the present study, the prevalence of the parasite in Uranoscopus scaber was determined as 36 %, while the mean intensity was found to be 2,6.

Anisocoelium capitellatum is a parasite that infects the gall bladder of Uranoscopus scaber and was detected in Turkey the first time in the Marmara Sea, around the shores of Mudanya by Oğuz (1995). Tepe (2011) and Tepe have also reported the parasite to be present around the shores of the Eastern Black Sea. In the present study which focused on the shorelines of Şile, 18 out of the 44 Uranoscopus scabers inspected were found to contain the parasite (41 %), and the mean intensity was determined as 4.1.

Prodistomum polonii which was previously only encountered in the intestines of Trachurus mediterraneus’, was reportedly present in the Trachurus trachurus of the Dardanelle Strait of Turkey by Keser . In the present study, this species was found to have a prevalence of 9 %, and mean intensity and abundance of 0.18.

Another Digenean species, Monascus filiformis, has previously been reported in Turkey in the shores of Mudanya, infecting the Symphodus tinca fish (Oguz & Bray, 2006). This species of parasites was also reported for the Trachurus trachurus of the Sea of Marmara (Keser ). In the present study, Monascus filiformis was encountered only in a single fish (2 % prevalence) of Mullus surmuletus.

Hysterothylacium aduncum was first encountered in Turkey in Trachurus mediterraneus and Engraulis encrasicholus and Sprattus sprattus (Öktener, 2005). Doğanay (1994) and Ismen & Bingel (1999) have reported the parasite in Merlangius merlangus of the Turkish coasts of the Black Sea. Furthermore, some of the anchovies obtained from the fish market of Eskişehir was reported to be infected with Contracaecum sp. (Yetim, 1985). The parasite was also encountered in Merluccius merluccius, Gobius niger, and Trachurus trachurus caught in the Sea of Marmara (Oğuz, 1995; Keser ), in Scomber japonicas of the Aegean Sea (Akmirza, 1997), in the Trachurus trachurus obtained from Erzurum fish market (Özkan ), and later in Pagellus erythrinus and Lophius piscatorius caught nearby the Gökçeada Island (Akmirza, 2013). In this study, H. aduncum was determined to be present with a very high prevalence (84.5 %), and was found to have infected Caspialosa pontica, Chelidonichthys lucerna, Engraulis encrasicolus, Gaidropsarus mediterraneus, Gobius niger, Merlangius merlangus euxinus, Mullus surmuletus, Sarda sarda, Sciaena umbra, Scorpaena porcus, Solea vulgaris, Spicara smaris, Symphodus tinca, Trachinus draco, Trachurus mediterraneus, and Uranoscopus scaber. The mean intensity of the parasite was the highest in Solea vulgaris with 28.5, and the mean abundance was the highest in Spicara smaris 11.5.

In Turkey, Epinephelus gigas, E. aeneus, E. marginatus, E. costae, and Mycteroperca rubra were reported to be infected with Philometra sp. Furthermore, Epinephelus marginatus and Mycteroperca rubra were reported to contain Philometra lateolabracis, while some Pagellus erythrinus were reported to be infected with Philometra filiformis (Öktener, 2005). In the Eastern Black Sea, Uranoscopus scaber and Trachurus mediterraneus were reportedly infected with Philometra globiceps (Tepe, 2011; Tepe & Oguz, 2013). In the present study, the Philometra sp. was found to be present in Trachinus draco and Trachurus mediterraneus, and the infection prevalence of the parasite was found to be the highest in Trachinus draco with 9.1 %

Another nematode species, Cucullanellus minutus, was first reported in Turkey in the Ekinli Lagoon of the Marmara, in Pleuronectes flesus by Oğuz (1989). In our study, Cucullanellus minutus was found to have infected two Solea vulgaris and one Symphodus tinca.

There is some information in the literature that Capillaria sp. was determined in angelfish (Pterophyllum scalare) (Ürkü & Yardimci, 2013). While the Capillaria genus displays a widespread on the fish of Turkey, it is mostly encountered in aquarium and freshwater fish. Doğanay reported it first for the aquarium fish, while it was reported from the freshwater fish for the first time by Türkmen (1990) in Rutilus frisii from the İznik Lake. Later, the Capillaria sp. was identified in the Mullus surmuletus of the Aegean Sea (Akmirza, 2000), while Pseudocapillaria tomentosa was identified within the intestines of Cyprinus carpio of the Manyas (Bird) Lake (Öztürk, 2000). Capillaria sp. was also encountered in the Aphanius danfordii of the Sarıkum Lagoon of the Sinop province (Öztürk & Özer, 2008). In this study, Capillaria gracilis species was encountered in two Mullus surmuletus and a single Gobius niger. Still, it was the most prevalent in Gobius niger with 6.3 %. Since this species was never reported for the marine or inland seas of Turkey, this study is the first to report its presence for theTurkey marine.

Acanthocephaloides irregularis of the Acanthocephala group of parasites was first reported from the Sukhyi Lyman Ukrainian shores and the Bay of Odesa, in Parablennius zvonimiri, Ponticola eurycephalus, Proterorhinus marmoratus and Syngnathus abaster fish (Amin ). The first recording of the parasite group for Turkey was for the Scorpaena porcus of the Black Sea shores with Acanthocephaloides propinquus infection (Tepe, 2011), which was later revised as Acanthocephaloides irregularis (Tepe & Oguz, 2013). Acanthocephaloides irregularis was found to be present in Scorpaena porcus, Gaidropsarus mediterraneus, and Gobius niger fish in this study as well. The highest prevalence of infection was in Scorpaena porcus with 20 %.

Neoechinorhynchus agilis was first encountered in Mugil cephalus (Cleave, 1921). In Turkey, this species was reported to be infecting the Mugil cephalus, Liza aurata, Liza saliens, Liza ramada and Chelon labrosus of the Aegean Sea (Altunel, 1982), in Liza saliens of the Dardanelle Strait (Keser ), and Liza aurata of the Eastern Black Sea (Tepe & Oguz, 2013). In our study, Neoechinorhynchus agilis was only determined in the Liza aurata species of fish with 44 % infection prevalence.

Another Acanthocephala species, Solearhynchus kostylewi, was first reported in Turkey from the Mudanya shores of the Marmara Sea as Acanthocephaloides soleae (Oğuz, 1995), which was later revised as Paracanthocephaloides kostylewi (Oğuz & Kvach, 2006). The same parasite was later identified as Solearhynchus kostylewi (Kvach & Oğuz, 2010). In research performed in the Black Sea, Acanthocephaloides kostylewi was reported as the specific parasite of Solea nasutus (Belofastova, 2004). In our study, Solearhynchus kostylewi was only found to be present in Solea vulgaris with 12.5 % infection prevalence.

Among the reasons for the differences observed in the present study the location where the fish are caught, pollution rate of water, host and intermediate host population, seasonal variations, and methods used can be included.

We hope that this study performed to determine the endohelminth fauna of the fish of the Şile shores of Turkey will present valuable reference opportunities for future studies and will contribute to the insight regarding the diversity of endohelminth of teleost fish of Turkey.