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Morphological and molecular identification of Gyrodactylus bubyri Osmanov, 1965 (Monogenea: Gyrodactylidae) from Caucasian dwarf goby, Knipowitschia caucasica (Berg) (Actinopterygii: Gobionellidae) from a Black Sea lagoon

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Abstract

Gyrodactylus bubyri Osmanov, 1965, a monogenean parasite of Caucasian dwarf goby Knipowitschia caucasica (Berg) described from Aral Sea and subsequently reported from the same host from Strymon River, Greece, is recorded from Atanasovsko Lake, Bulgarian Black Sea coast (the first record of G. bubyri from the Black Sea basin). The species is redescribed by light and scanning electron microscopy as well as the ITS rDNA sequence is obtained. As comparative materials, specimens of G. bubyri from K. caucasica (Strymon River), G. charon Vanhove and Huyse in Vanhove et al., 2014 from Knipowitschia milleri (Acheron Delta, Greece) and G. micropsi Gläser, 1974 from Potamoschistus microps from North Sea (Belgium) are studied. Comparative morphology and molecular data demonstrate that G. micropsi is a junior synonym of G. bubyri (new synonymy). The validity of G. charon is questioned, pending examination of additional materials in order to prove it as a distinct species or as a junior synonym of G. bubyri.

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References

  • Ahnelt H, Bianco PG (1990) Orsinigobius milleri n. sp., a new species of freshwater goby from W-Greece (Pisces: Gobiidae). Annalen des Naturhistorischen Museums in Wien. Serie B für Botanik und Zoologie 91:1–6

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Berg LS (1916) Fishes of fresh waters of the Russian Empire. In Russian, Department of Agriculture, Moscow

  • Bianco PG, Bullock AM, Miller PM, Roubal FR (1987) A unique teleost dermal organ in a new European genus of fishes (Teleostei: Gobioidei). J Fish Biol 31:797–803

  • Dmitrieva E, Dimitrov G (2002) Variability in the taxonomic characters of Black Sea gyrodactylids (Monogenea). Syst Parasitol 51:199–206

    Article  CAS  PubMed  Google Scholar 

  • Dmitrieva EV, Skidan N (2005) Gyrodactylus leopardinus sp. n. (Monogenea)—a parasite of Pomatoschistus marmoratus (Gobiidae) from the Sea of Azov. Vestnik Zoologii 39(3):17–22

    Google Scholar 

  • Duncker G (1928) Teleostei Physoclisti. 9. Gobiiformes. In: Die Tierwelt der Nord- und Ostsee. Unspecified Publisher, Berlin

  • Ergens RR (1985) Order Gyrodactylea, Family Gyrodactylidae. In: Gussev AV (ed) Key to Parasites of Freshwater Fishes of the Fauna of USSR. Volume 2, Part 1. Parasitic metazoans. In Russian, Nauka, Leningrad

    Google Scholar 

  • Gaevskaya AV (2012) Parasites and diseases of fishes in the Black Sea and the Sea of Azov. I. Marine, brackish and diadromous fishes. In Russian, EKOSI-Gidrofizika, Sevastopol

    Google Scholar 

  • Gaevskaya AV, Gussev AV, Deliamure SL, Donez ZS, Iskova NI, Kornyushin VV, Kovaleva AA, Smogorzhevskaya LA, Solonchenko AI, Shtetin GA, Shulman SS, Margaritov NM, Markevich AP, Mordvinova TN, Naydenova NN, Nikolaeva VM, Paruchin AM, Pogorelzeva TP (1975) Handbook of Parasites of Vertebrate Animals in Black Sea and the Sea of Azov. In Russian, Naukova Dumka, Kiev

    Google Scholar 

  • Geets A, Appleby C, Ollevier F (1999) Host-dependent and seasonal variation in opisthaptoral hard parts of Gyrodactylus cf. arcuatus from three Pomatoschistus spp. and G. arcuatus from Gasterosteus aculeatus: a multivariate approach. Parasitology 119:27–40

    Article  PubMed  Google Scholar 

  • Gheorghiev JM (1966) Composition d’espece et caracteristique des Gobiides (Pisces) en Bulgaria. Proceedings of the Research Institute of Fisheries and Oceanography. Varna 7:159–228, In Bulgarian

    Google Scholar 

  • Gill T (1863) Descriptions of the gobioid genera of the western coast of temperate North America. Proc Acad Natl Sci Phila 15:262–267

  • Gläser H-J (1974) Eine neue Artengruppe des Subgenus Gyrodactylus (Paranephrotus) (Monogenea, Gyrodactylidae). Zool Anz 192:271–278

    Google Scholar 

  • Gussev AV (1983) Methods for collecting and processing materials of monogeneans parasitizing fishes. In Russian, Nauka, Leningrad

    Google Scholar 

  • Huyse T, Malmberg G (2004) Molecular and morphological comparisons between Gyrodactylus ostendicus n. sp. (Monogenea: Gyrodactylidae) on Pomatoschistus microps (Krøyer) and G. harengi Malmberg, 1957 on Clupea harengus membras L. Syst Parasitol 58:105–113

    Article  PubMed  Google Scholar 

  • Huyse T, Volckaert FAM (2002) Identification of a host-associated species complex using molecular and morphometric analyses, with the description of Gyrodactylus rugiensoides n. sp. (Gyrodactylidae, Monogenea). Int J Parasitol 32:907–919

    Article  CAS  PubMed  Google Scholar 

  • Huyse T, Audenaert V, Volckaert FAM (2003) Speciation and host–parasite relationships in the parasite genus Gyrodactylus (Monogenea, Platyhelminthes) infecting gobies of the genus Pomatoschistus (Gobiidae, Teleostei). Int J Parasitol 33:1679–1689

    Article  PubMed  Google Scholar 

  • Huyse T, Malmberg G, Volckaert FAM (2004) Four new species of Gyrodactylus von Nordmann, 1832 (Monogenea, Gyrodactylidae) on gobiid fishes: combined DNA and morphological analyses. Syst Parasitol 59:103–120

    Article  PubMed  Google Scholar 

  • Huyse T, Pampoulie C, Audenaert V, Volckaert FAM (2006) First report of Gyrodactylus spp. (Platyhelminthes: Monogenea) in the Western Mediterranean Sea: molecular and morphological descriptions. J Parasitol 92:682–690

    Article  CAS  PubMed  Google Scholar 

  • Iljin BS (1927) Key to gobies (family Gobiidae) from the Sea of Azov and the Black Sea (preliminary report). Trudy Azovo-Chernomorskoy Nauchno-Promyslovoy Ekspeditsii 2:128–143, In Russian

  • Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Kottelat, Cornol, Switzerland, and Freyhof, Berlin, Germany

    Google Scholar 

  • Krasnovyd V, Kvach Y, Drobiniak O (2012) The parasite fauna of the gobiid fish (Actinopterygii, Gobiidae) in the Sukhyi Lyman, Black Sea. Vestnik Zoologii 46(6):e-1–e-8

    Article  Google Scholar 

  • Krøyer HN (1838) Denmarks fiske. Triers Officin, Kjobenhavn

  • Malmberg G (1970) The excretory systems and the marginal hooks as basis for the systematic of Gyrodactylus (Trematoda, Monogenea). Arkiv för Zoologi 2:1–235

    Google Scholar 

  • Matĕjusová I, Gelnar M, McBeath AJA, Collins CM, Cunningham CO (2001) Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). Int J Parasitol 31:738–745

    Article  PubMed  Google Scholar 

  • Mo TA (1991a) Variations of opisthaptoral hard parts of Gyrodactylus salaris Malmberg, 1957 (Monogenea: Gyrodactylidae) on rainbow trout Oncorhynchus mykiss (Walbaum, 1792) in a fish farm, with comments on the spreading of the parasite in south-eastern Norway. Syst Parasitol 20:1–9

  • Mo TA (1991b) Variations of opisthaptoral hard parts of Gyrodactylus salaris Malmberg, 1957 (Monogenea: Gyrodactylidae) on parr of Atlantic Salmon Salmo salar L. in laboratory experiments. Syst Parasitol 20:11–19

  • Mo TA (1993) Seasonal variations of the opisthaptoral hard parts of Gyrodactylus derjavini Mikailov, 1975 (Monogenea: Gyrodactylidae) on brown trout Salmo trutta L. parr and Atlantic salmon S. salar L. parr in the River Sandvikselva, Norway. Syst Parasitol 26:225–231

    Article  Google Scholar 

  • Mo TA, Appleby C (1990) A special technique for studying haptoral sclerites of monogeneans. Syst Parasitol 17:103–108

    Article  Google Scholar 

  • Naydenova NN (1974) Parasite fauna of fishes of the family Gobiidae from the Black Sea and the Sea of Azov. In Russian, Naukova Dumka, Kiev

    Google Scholar 

  • Nordmann A von (1832) Mikrographische Beiträge zur Naturgeschichte der wirbellosen Thiere. Erstes Heft. Reimer, Berlin

  • Osmanov SO (1965) Contribution to the study of monogenean and digenean flukes of fishes from Uzbekistan. Vestnik Karakalpakskogo Filiala Academii Nauk Uzbekskoy SSR 4(22):21–32, In Russian

  • Osmanov SO (1971) Parasites of fishes in Uzbekistan. In Russian, FAN, Tashkent

    Google Scholar 

  • Risso A (1810) Ichthyologie de Nice, ou Histoire naturelle des poissons du Département des Alpes Maritimes. Schoell, Paris

  • Shinn AP, Hansen H, Olstad K, Bachmann L, Bakke TA (2004) The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. thymalli (Monogenea). Folia Parasitol 51:239–252

    Article  PubMed  Google Scholar 

  • Stoyanov B, Neov B, Pankov P, Radoslavov G, Hristov P, Georgiev BB (2015) Redescription of Aphalloides coelomicola Dollfus, Chabaud & Golvan, 1957 (Digenea, Opisthorchioidea) based on specimens from Knipowitschia caucasica (Berg) (Actinopterygii, Gobionellidae) from a Black Sea lagoon, with comments on the systematic position of the genus. Syst Parasitol 91:1–12

    Article  PubMed  Google Scholar 

  • Thacker CE (2013) Phylogenetic placement of the European sand gobies in Gobionellidae and characterization of gobionellid lineages (Gobiiformes: Gobioidei). Zootaxa 3619:369–382

    Article  PubMed  Google Scholar 

  • Vanhove MPM, Economou AN, Zogaris S, Giakoumi S, Zanella D, Volckaert FAM, Huyse T (2014) The Gyrodactylus (Monogenea, Gyrodactylidae) parasite fauna of freshwater sand gobies (Teleostei, Gobioidei) in their centre of endemism, with description of seven new species. Parasitol Res 113:653–668

    Article  PubMed  Google Scholar 

  • Vassilev M, Apostolou A, Velkov B, Dobrev D, Zarev V (2012) Atlas of the gobies (Gobiidae) in Bulgaria. Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Sofia

    Google Scholar 

  • Zietara MS, Arndt A, Geets A, Hellemans B, Volckaert FAM (2000) The nuclear rDNA region of Gyrodactylus arcuatus and G. branchicus (Monogenea: Gyrodactylidae). Journal of Parasitolgy 86:1368–1373

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to Ministry of Environment and Waters of the Republic of Bulgaria for licenses (NCZP-151/11.05.2012 and NCZP-168/29.04.2013) to carry out studies in Atanasovsko Lake Reserve. The field study was based at Atanasovsko Lake Field Station of the Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences; the assistance of the staff of this station as well as of Dr Gergana P. Vasileva, Konstantin Popov and Dr Pavel Nikolov is acknowledged. We are also grateful to Dr Sven Boström from the Department of Invertebrate Zoology at the Swedish Museum of Natural History (Stockholm, Sweden) for loaning voucher and paratype specimens. Dr Arseny A. Makarikov (Novosibirsk, Russia) kindly helped with a copy of the article by Osmanov (1965). Facilities developed in the frames of the projects WETLANET (FP7 CAPACITIES Grant 229802), CEBDER (National Science Fund, Ministry of Education, Youth and Science of the Republic of Bulgaria, Grant DO 02-15/2009) and Phylogenetic ultrastructure markers for parasitic worms. Funded by National Science Fund, Ministry of Education, Youth and Science of the Republic of Bulgaria (YS DO 02-271/18.12.2008) were used in the course of the present study.

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Correspondence to Boyko B. Georgiev.

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Stoyanov, B., Huyse, T., Pankov, P. et al. Morphological and molecular identification of Gyrodactylus bubyri Osmanov, 1965 (Monogenea: Gyrodactylidae) from Caucasian dwarf goby, Knipowitschia caucasica (Berg) (Actinopterygii: Gobionellidae) from a Black Sea lagoon. Parasitol Res 115, 1617–1625 (2016). https://doi.org/10.1007/s00436-015-4899-8

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