Metazoan Parasite Faunas of Three Gobiid Species (Actinopterygii: Gobiidae) Inhabiting the Lower Kizilirmak Delta in Samsun: A Comparative Study/Samsun'da Asagi Kizilirmak Deltasinda Yasayan Uc Kaya Baliginin (Actinopterygii: Gobiidae) Karsilastirmali Metazoan Parazit Faunasi.
The family Gobiidae is one of the largest taxons of fish and vertebrate animals. It comprises >2000 species with >200 genera. They are abundant worldwide in every kind of environment, including tropical to temperate marine, estuarine, and freshwater (1). A total of 5 out of 27 species of this family, which inhabited the Black Sea (2), Neogobius, Proterorhinus, and Pomatoschistus are the most common genera of the family. Neogobius fluviatilis and Proterorhinus marmoratus are native species in the Ponto --Caspian basin. Their native habitats include the coastal zones of the Black Sea, Caspian Sea, Azov Sea, and Marmara Sea (3-5). Pomatoschistus marmoratus is a species of the Mediterranean Basin and is widespread in the Eastern Atlantic, Mediterranean, Black Sea, Azov Sea, and Suez Canal (3, 6). The gobiid fishes play important roles in the ecosystem. Regarding food chains, the gobies are secondary consumers and are themselves prey for larger fish, sea birds, and seals. Their availability for predators implies that they are important transmitters of parasites, which complete their life cycle in several hosts (7). Gobiids may be definitive, intermediate, or paratenic hosts of parasites such as digene-ans, cestodes, and nematodes. Owing to their ecological tolerance, small sizes, habitation, and diversity, gobiids are appropriate fishes to study the course of colonization by parasites (8).
Several studies are available about the helminths of lagoons and estuaries in the northwestern Black Sea (9-21). Although there is considerable information available on the parasite fauna of gobiids mainly from the northern coasts of the Black Sea, only few studies have reported on those of the gobiids that reside close to Turkish coasts (22-24). In Turkey, there is so far only one published study on the metazoan parasite fauna of Neogobius melanostomus, which is not a gobiid species investigated in the present study (23). Moreover, no published study has reported on the metazoan parasites of N. fluviatilis, Pr. marmoratus, and Po. marmoratus from the southern coast of the Black Sea so far. Thus, more studies are required to determine the metazoan parasite fauna of various gobiid species.
The aim of the present study was to investigate and compare the metazoan parasite faunas that occur on N. fluviatilis, Pr. marmoratus, and Po. marmoratus from the Lower Kizilirmak Delta located on the southern coastal zones of the Black Sea. The results are comparable with those of a few previous studies, which investigated in different coastal zones from the Black Sea. The results of the present study present new data about parasite--host relationship.
The three gobiid species were fished from the Lower Kizilirmak Delta, which is located on the border of Samsun city (41[grados]38'38.84" N and 36[grados]04'09.89" E) and lies at the sea level. The specimens of these fishes were caught using fishing nets and electroshock device. Sampling was conducted over a 1-year period. A total of 221 specimens of the three gobiid species, N. fluviatilis (160), Pr. marmoratus (45), and Po. marmoratus(16), were investigated for the presence of helminths. The fishes were measured and weighed, and their external and internal organs were carefully examined.
Parasitological Indices and Statistical Analysis
The prevalence, mean intensity, and abundance for metazoan parasites from monkey goby N. fluviatilis, tubenose goby Pr. marmoratus, and marbled goby Po. Marmoratus were determined according to Bush et al. (25). The standard error for mean intensity is provided. The Czekanowski--Sorensen Index (ICS, %) was used to compare the helminth faunas (26). The significance of the host--parasite relationship was determined according to the abundance values. The scales used for species were >2 for core species, 0.6-2 for secondary species, 0.2-0.6 for satellite species, and 0.2 for rare species (27). The tendency to participate in the infra-community was evaluated in terms of the infracommunity index with >0.30 as the highest value. The mean infracommunity was characterized as the mean number of parasite species per host individual (28). The species evenness was calculated according to the formula provided by Zander et al. (7). The evenness values > 0.6 represented a greater part of the homogeneity with >0.7 being a high homogeneity. All statistical tests were carried out using GraphPad Instat 3.0 for Windows 2000 (Software, San Diego, CA, USA) software (p<0.05: statistically significant).
In total, the following 13 metazoan parasite species were found: 2 monogenea (Gyrodactylus proterorhini and Gyrodactylus sp.) 6 digenean metacercariae (Tylodelphys clavata, Diplostomum spathaceum, Apatemon gracilis, Posthodiplostomum sp., Ascocotyle sp., and Echinostoma sp.), 1 cestoda (Bothriocephalus acheilognathi), 3 nematodes (Spiroxys contortus, Eustrongylides excisus, and Contraceacum rudolphii), and 1 arthropoda Ergasilus (sieboldi). The monkey goby has the richest parasite fauna with 11 parasite species. Although the monkey goby was infected with 11 parasite species has the richest parasite fauna, the marbled goby was infected with only 4 parasite species. The highest prevalence and abundance values (77.8% and 49.02) were found in tubenose goby infected with 9 parasite species (Table 1).
The monogenean Gyrodactylus proterorhini and the digenean metacercariae Tylodelphys clavata and Echinostoma sp. were determined in three gobiid fishes. Contraceacum rudolphii occurred only in tubenose goby; Spiroxys contortus and Eustrongylides excisus were found only in monkey goby, and Gyrodactylus sp. occurred only in marbled goby (Table 1). Four species, G. proterorhini, Apatemon gracilis, Posthodiplostomum sp., and Echinostoma sp., played core roles in the metazoan parasite faunas of gobies from the Lower Kizilirmak Delta. G. proterorhini, A. gracilis, and Posthodiplostomum sp. were essential in the tubenose goby parasite fauna and Echinostoma sp. in the monkey and tubenose goby parasite faunas. Moreover, Echinostoma sp. was core in all cases except in marbled goby (Table 1).
The species composition of metazoan faunas of the three gobiid species differed, and the parasite species richness was variable among the gobiid fishes. The metazoan parasite fauna of the marbled goby, which is of Mediterranean origin, differed markedly from those of the monkey and tubenose gobies (Table 1). The homogeneity of the parasite component faunas was low in monkey and tubenose gobies, but it was high in marbled goby (Table 2). The mean infracommunity index (ICI) of the monkey goby was higher than that of the marbled goby. The ICI of the tubenose goby differed from that of the monkey and marbled gobies (Table 2). A high Czekanowski--Sorensen index, indicating a close similarity, was observed in the metazoan parasite fauna of the monkey and tubenose gobies (/cs=80.0%) (Table 3).
Data on parasites of various gobiid fishes found in the Black Sea coast are previously reported (12-17, 20, 21, 29-31). These studies include the parasites of the three gobiid species (N. fluviatilis, Pr. marmoratus, and Po. marmoratus) and 34 metazoan parasite species (Table 4). We found 13 parasite species; 6 species were reported on in a previous study, but 7 species, including Gyrodactylus sp., Bothriocephalus acheilognathi, Echinostoma sp., Posthodiplostomum sp., Ascocotyle sp., S. contortus, and Ergasilus sieboldi, were mentioned from the three examined gobiids for the first time in the Black Sea (Table 4). Parasites such as the trematodes Pygidiopsis genata (metacercaria), Cryptocotyle concavum met., Cryptocotyle lingua met., and Timoniella imbutiforme met., nematode Dichelyne minutus, and acanthocephalan Acanthocephaloides propinquus were previously observed in the three gobiids in various sites of the northwestern Black Sea and Crimean coasts. Overall, these parasite species are typical for the resident gobiids in the Black Sea, but we did not find them during our study. C. concavum, C. lingua, P. genata, T. imbutiforme, D. minutus, and A. propinquus are brackish water and marine parasite species. Moreover, the first intermediate hosts of these parasites are also absent in fresh waters (7, 14). The absence of parasites mentioned in the present study could be explained by low salinity in our study area (approximately 1%).
According to previous studies, five of the listed species, G. proterorhini, A. gracilis, T. clavata, Diplostomum spathaceum, and E. excisus, have been reported in the monkey goby from different localities of the Black Sea (14, 16, 21, 31, present study) (Table 4). Similarly, G. proterorhini and C. rudolphii have been previously reported in the tubenose goby (20, 21). G. proterorhini is a specific species for gobiids inhabiting the Black and Azov Seas and their estuaries (32). Additionally, it is reported in various rivers belonging to the Black Sea drainage within the natural living area of the Ponto--Caspian gobiids (20, 29, 33). To date, Zosterisessor ophiocephalus, Gobius cobitis, Gobius niger, N. melanostomus, N. fluviatilis, Neogobiusplatyrostris, Mesogobius batrachocephalus, and Neogobius kessleri have been reported as host of G. proterorhini (19, 23, 34-40). To the best of our knowledge, the occurrence of G. proterorhini in Po. marmoratus is reported for the first time in this study. A new host has been added to the host list of G. proterorhini. Until today, three Gyrodactylus species that are known to parasitize Po. Marmoratus include G. branchialis and G. ostendicus that are reported from the western Mediterranean Sea (41) and G. leopardinus that is reported from the Azov Sea (30, 42).
To date, 47 metazoan parasite species have been mentioned in the Black Sea basin according to data from different authors (Table 4). We found 13 parasite species; 7 of these had already been mentioned in published studies, but 6 species, Ascocotyle sp., Posthodiplostomum sp., Echinostoma sp., B. acheilognathi, S. contortus, and E. sieboldi, were mentioned from three gobiid fishes for the first time. Particularly, tendency to join the infra-community of Echinostoma sp., which is a limnetic parasite species, differs from other parasites in the present study (Table 2). The species composition of the metazoan fauna of gobiid fishes from the Lower Kizilirmak Delta located on the southern coastal zones of the Black Sea differed from those reported from various sites of the northern coastal zone of the Black Sea. The results of the present study indicated that the euryhaline and limnetic species are prevalent in this basin, but the marine and brackish water species are prevalent in its northern part. The gobiid parasite fauna does not show homogeneity in the Black Sea (34). It consists of Ponto--Caspian, Mediterranean, Boreal--Atlantic, and limnetic parasite species that are attributed to the different ranges of euryhalinity of the hosts. Thus, the species composition of the gobiid metazoan fauna in the present study is formed according to the ecology of the host species.
The present study comprises current data regarding the metazoan parasite fauna of gobiids in the Lower Kizilirmak Delta from the Black Sea. The data presented in this paper contribute to the list of parasite species that inhabit this basin. In general, the metazoan parasite communities of the three gobiid fishes from the Lower Kizilirmak Delta comprised limnetic species and differed from the other regions of the Black Sea.
Ethics Committee Approval: Ethics committee approval was received for this study from the Animal Experiments Local Ethics Committee of Sinop University (Date: 01.03.2010).
Peer-review: Externally peer-reviewed.
Author contributions: Concept--T.O., A.G.; Design--T.O., A.G.; Supervision--T.O., A.G.; Resource--T.O., A.G.; Materials--T.O., A.G.; Data Collection and/or Processing--A.G., T.O.; Analysis and /or Interpretation--T.O., A.G.; Literature Search--A.G. T.O.; Writing--T.O.; Critical Reviews--T.O., A.G.
Acknowledgements: The authors would like to thank Prof. Dr. Ahmet OZER who shared their valuable opinions during the study.
Conflict of Interest: No conflict of interest was declared by the authors.
Financial Disclosure: This study was financially supported by the Scientific and Technological Research Council of Turkey (TUBITAK; project number 1,100,424). The authors are grateful for their valuable support.
Etik Komite Onayi: Bu calisma icin etik komite onayi Sinop Universitesi, Hayvan Deneyleri Yerel Etik Kurulu'ndan (01.03.2010) alinmistir.
Hakem Degerlendirmesi: Dis bagimsiz.
Yazar Katkilari: Fikir--T.O., A.G.; Tasarim--T.O., A.G.; Denetleme--T.O., A.G.; Veri Toplanmasi ve/veya Islemesi--A.G., T.O.; Analiz ve/veya Yorum--T.O., A.G.; Literatur Taramasi--A.G., T.O., Yaziyi Yazan--T.O.; Elestirel Inceleme--T.O., A.G.
Tesekkur: Yazarlar, calismanin yurutulmesinde degerli goruslerini bizlerle paylasan Prof. Dr. Ahmet OZER'e tesekkur ederler.
Cikar Catismasi: Yazarlar cikar catismasi bildirmemislerdir.
Finansal Destek: Bu calisma, Turkiye Bilimsel ve Teknolojik Arastirma Kurumu (TUBITAK, proje numarasi 1104244) tarafindan maddi olarak desteklenmistir.
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Arzu Guven [iD], Turkay Ozturk [iD]
Department of Fish Diseases, Sinop University Faculty of Fisheries and Aquatic Sciences, Sinop, Turkiye
Cite this article as: Guven A, Ozturk T. Metazoan Parasite Faunas of Three Gobiid Species (Actinopterygii: Gobiidae) Inhabiting the Lower Kizilirmak Delta in Samsun: A Comparative Study. Turkiye Parazitol Derg 2018; 42:33-8.
Address for Correspondence / Yazisma Adresi: Turkay Ozturk E.mail: email@example.com
Received: 30.10.2017 Accepted: 11.12.2017
Gelis Tarihi: 30.10.2017 Kabul Tarihi: 11.12.2017
Table 1. Component community of parasites of three gobiid fishes from the Lower Kizilirmak Delta (bold data for homogeneity) Neogobius fluviatilis (n=160) Host species P MI[+ or -]SE A Gyrodactylus proterorhini 9.4 2.7[+ or -]0.6 0.25 Gyrodactylus sp. - - - Ascocotyle sp. met. 4.4 1.3[+ o -]0.2 0.06 Echinostoma sp. met. 60.0 16.7[+ or -]2.1 10.03 Tylodelphys clavata met. 15.0 3.5[+ or -]1.8 1.19 Diplostomum 18.8 6.6[+ or -]1.4 1.24 spathaceum met. Apatemon gracilis met. 3.8 5.0[+ or -]2.1 1 Posthodiplostomum sp. 6.3 5.7[+ or -]2.3 0.36 met. Bothriocephalus 5.0 1.4[+ or -]0.3 0.07 acheilognathi pl. Spiroxys contortus L3 2.5 1.4[+ or -]0.4 0.04 Eustrongylides excisus L3 2.5 1.6[+ or -]0.6 0.05 Contraceacum rudolphii L3 - - - Ergasilus sieboldi 8.8 1.3[+ or -]1.2 0.31 Total 75 18.4[+ or -]2.1 (ab) 13.78 Proterorhinus marmoratus (n=45) Host species P MI[+ or -]SE A Gyrodactylus proterorhini 28.9 15.2[+ or -]3.9 4.40 Gyrodactylus sp. - - - Ascocotyle sp. met. - - - Echinostoma sp. met. 37.8 15.4[+ or -]5.3 5.82 Tylodelphys clavata met. 28.9 4.8[+ or -]1.4 1.38 Diplostomum 13.3 2.0[+ or -]0.6 0.27 spathaceum met. Apatemon gracilis met. 46.7 63.9[+ or -]16.2 29.84 Posthodiplostomum sp. 17.8 38.9[+ or -]12.6 6.91 met. Bothriocephalus 17.8 1.3[+ or -]0.2 0.22 acheilognathi pl. Spiroxys contortus L3 - - - Eustrongylides excisus L3 - - - Contraceacum rudolphii L3 8.9 1.8[+ or -]0.5 0.16 Ergasilus sieboldi 2.2 1.0[+ or -]0.00 0.02 Total 77.8 63.0[+ or -]15.4 (b) 49.02 Pomatoschistus marmoratus (n=16) Host species P MI[+ or -]SE A Gyrodactylus proterorhini 12.5 2.5[+ or -]05 0.31 Gyrodactylus sp. 6.25 26.0[+ or -]0.0 1.63 Ascocotyle sp. met. - - - Echinostoma sp. met. 25 1.3[+ or -]0.3 0.31 Tylodelphys clavata met. 18.8 1.0[+ or -]0.0 0.19 Diplostomum - - - spathaceum met. Apatemon gracilis met. - - - Posthodiplostomum sp. - - - met. Bothriocephalus - - - acheilognathi pl. Spiroxys contortus L3 - - - Eustrongylides excisus L3 - - - Contraceacum rudolphii L3 - - - Ergasilus sieboldi - - - Total 43.8 6.0[+ or -]4.0 (a) 2.63 n: number of examined fish; P: prevalence (%); MI: mean intensity; SE: standard error; A: abundance; met.: metacercaria; pl.: plerocercoid; L3: L3 stage Table 2. Infracommunity index Neogobius Proterorhinus Pomatoschistus fluviatilis marmoratus marmoratus Gyrodactylus 0.07 0.14 0.30 proterorhini Gyrodactylus sp. 0.09 Ascocotyle sp. met. 0.03 Echinostoma sp. 0.44 0.24 0.40 met. Tylodelphys clavata 0.11 0.14 0.30 met. Diplostomum 0.14 0.07 spathaceum met. Apatemon gracilis 0.03 0.23 met. Posthodiplosto-mum 0.05 0.09 sp. met. Bothriocephalus 0.04 0.09 acheilognathi pl. Spiroxys contortus 0.02 L3 Eustrongylides 0.02 excisus L3 Contraceacum 0.04 rudolphii L3 Ergasilus sieboldi 0.06 0.01 Mean infracommunity 1.82 2.02 1.43 Species richness 11 9 4 Shannon Index 1.06 1.30 0.99 Species evenness 0.44 0.56 0.72 (ICI>0.30). met.: metacercaria; pl.: plerocercoid, L3: L3 stage; ICI: infracommunity index Table 3. Czekanowski-S0rensen Index (%) in helminth fauna of various gobiid species in the study area Nf Pr Po Neogobius fluviatilis (Nf) 100.0 - - Proterorhinus marmoratus (Pr) 80.0 100 - Pomatoschistus marmoratus (Po) 40.0 46.0 100 Table 4. List of the metazoan parasites reported from three gobiid fishes in different geographical localities in the Black Sea region Neogobius fluviatilis Gyrodactylus proterorhini , Present study Gyrodactylus leopardinus Gyrodactylus sp. Ascocotyle sp. met. Present study Echinostoma sp. met. Present study Tylodelphys clavata met.  Present study, Diplostomum spathaceum ,  Present study Apatemon gracilis met.  Present study Posthodiplostomum sp. met. Present study Cryptocotyle concavum met. , , , , , ,  Cryptocotyle lingua met. , , , , , Pygidiopsis genata met. , , , ,  Acanthostomum imbutiformis , , , , Stephanostomum bicoranatum Monascus filiformis  Pronopyrmna ventricosa  Pronopyrmna petrowi  Magnibursatus skrjabini Asymphylodora imitans  Asymphylodora pontica  Aphalloides coelomicola Galactosomum lacteum  Paratimonia gobii Nicolla skrjabini ,  Holostephaluscobitis met.  Ichthyocotylurus variegatus  Rhipidocotyle companula met.  Maritrema subdolum met.  Proteocephalus gobiorum , ,  Proteocephalus torulosus  Ligula pavlovskii , ,  Bothriocephalus gregarius Bothriocephalus acheilognathi pl. Present study Agamonema sp. L3  Contraceacum rudolphii L3  Contraceacum microcephalum Eustrongylides excisus L3 , , , Present study Dichelyne minutus , , , ,  Cucullanus heterochrous  Streptocara crassicauda  Raphidascaris acus , ,  Pseudocapillaria tomentosa  Spiroxys contortus Present study Acanthocephaloides propinquus , , ,  Telosentis exiguus , ,  Ergasilus sieboldi Present study Thersitina gasterostei  Proterorhinus marmoratus Gyrodactylus proterorhini , , , Present study Gyrodactylus leopardinus Gyrodactylus sp. Ascocotyle sp. met. Echinostoma sp. met. Present study Tylodelphys clavata met. Present study Diplostomum spathaceum Present study Apatemon gracilis met. Present study Posthodiplostomum sp. met. Present study Cryptocotyle concavum met. , , , , ,  Cryptocotyle lingua met. , , ,  Pygidiopsis genata met. ,  Acanthostomum imbutiformis ,  Stephanostomum bicoranatum  Monascus filiformis  Pronopyrmna ventricosa  Pronopyrmna petrowi  Magnibursatus skrjabini ,  Asymphylodora imitans Asymphylodora pontica Aphalloides coelomicola Galactosomum lacteum Paratimonia gobii Nicolla skrjabini Holostephaluscobitis met. Ichthyocotylurus variegatus Rhipidocotyle companula met. Maritrema subdolum met. Proteocephalus gobiorum  Proteocephalus torulosus Ligula pavlovskii Bothriocephalus gregarius Bothriocephalus acheilognathi pl. Present study Agamonema sp. L3 Contraceacum rudolphii L3 , Present study Contraceacum microcephalum Eustrongylides excisus L3 Present study Dichelyne minutus , , , ,  Cucullanus heterochrous Streptocara crassicauda  Raphidascaris acus Pseudocapillaria tomentosa Spiroxys contortus Acanthocephaloides propinquus , , ,  Telosentis exiguus  Ergasilus sieboldi Thersitina gasterostei Pomatoschistus marmoratus Gyrodactylus proterorhini Present study Gyrodactylus leopardinus  Gyrodactylus sp. Present study Ascocotyle sp. met. Echinostoma sp. met. Present study Tylodelphys clavata met. Present study Diplostomum spathaceum Apatemon gracilis met. Posthodiplostomum sp. met. Cryptocotyle concavum met. , , , ,  Cryptocotyle lingua met. , , ,  Pygidiopsis genata met. ,  Acanthostomum imbutiformis , , ,  Stephanostomum bicoranatum Monascus filiformis Pronopyrmna ventricosa  Pronopyrmna petrowi Magnibursatus skrjabini Asymphylodora imitans Asymphylodora pontica , , ,  Aphalloides coelomicola , , ,  Galactosomum lacteum Paratimonia gobii , , ,  Nicolla skrjabini Holostephaluscobitis met. Ichthyocotylurus variegatus Rhipidocotyle companula met. Maritrema subdolum met. Proteocephalus gobiorum Proteocephalus torulosus Ligula pavlovskii Bothriocephalus gregarius ,  Bothriocephalus acheilognathi pl. Agamonema sp. L3 Contraceacum rudolphii L3 Contraceacum microcephalum  Eustrongylides excisus L3 Present study Dichelyne minutus , , ,  Cucullanus heterochrous Streptocara crassicauda Raphidascaris acus Pseudocapillaria tomentosa Spiroxys contortus Acanthocephaloides propinquus ,  Telosentis exiguus  Ergasilus sieboldi Thersitina gasterostei met.: metacercaria; pl.: plerocercoid; L3: L3 stage
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|Title Annotation:||Original Investigation / Ozgun Arastirma|
|Author:||Guven, Arzu; Ozturk, Turkay|
|Publication:||Turkish Journal of Parasitology|
|Date:||Mar 1, 2018|
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