Ali Serhan TARKAN, Fitnat Güler EKMEKÇİ, Lorenzo VILIZZI

Parasites of the common carp Cyprinus carpio L., 1758 (Teleostei: Cyprinidae) from water bodies of Turkey: updated checklist and review for the 1964 2014 period

A synopsis is provided of the parasites of common carp Cyprinus carpio L. from water bodies of Turkey based on literaturedata from 1964 to 2014. In total, 45 studies were included in the review and these provided data from 41 water bodies, comprising 12man-made reservoirs, 21 natural lakes, and 8 water courses. Forty-one different taxa (including molluscan Glochidium sp.) in totalwere recorded. Of these taxa, 2 had not been previously reviewed for Turkey, and 4 were excluded from the list because of dubiousidentification. The Turkish parasite fauna of common carp living under natural conditions was dominated by ciliates (Ciliophora)among the protozoans and by flatworms (Platyhelminthes) among the metazoans, and this was both in terms of occurrence on fish andacross water bodies. The absence of 7 taxa from both the European and North American checklists can be explained by the locationof Turkey at the frontier between Asia and Europe. Additionally, the parasite fauna of the common carp in Turkey was consistentlydifferent from that of the far eastern species specimens. Lack of differences among water bodies in both taxon richness and compositionindicates overall homogeneity, likely a result of the species relatively long-term establishment across the region. It is suggested thatmanagement options could benefit from this level of homogeneity.

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Aksoy S, Saglam N, Dorucu M (2006) External parasites of three cyprinid fish species from Lake Hazar in Turkey. Indian Vet J 83: 100101.
Alaş A, Öktener A, Solak K (2010). A study on the morphology of Argulus f oliaceus Lin., 1758 (Crustacea; Branchiura) procured from Çavuşcu Lake (Central Anatolia-Turkey) with scanning electron microscopy. Turk J Biol 34: 147151.
Anderson MJ (2001a). Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58: 626639.
Anderson MJ (2001b). A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 3246.
Anderson MJ, Gorley RN, Clarke KR (2008). PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. Plymouth, UK: PRIMER-E Ltd.
Arslan N, Öktener A (2012). A general review of parasitic Annelida (Hirudinea) recorded from different habitats and hosts in Turkey. Turk J Zool 36: 141145.
Aslan B (2009). Ağrı ili Murat Nehri ile Erzurum ili Aras Nehrinden yakalanan bazı balıkların endohelmintlerinin araştırılması. MSc, Atatürk University, Erzurum, Turkey (in Turkish).
Aydoğdu A, Altunel FN (2002). Doğancı Baraj Gölünden (Bursa) yakalanan bazı balıklarda kaydedilen helminthler. Türk Parazitol Derg 26: 8792 (in Turkish).
Aydogdu A, Kostadinova A, Fernandez M (2003). Variations in the distribution of parasites in the common carp, Cyprinus carpio, from Lake Iznik, Turkey: population dynamics related to season and host size. Helminthologia 40: 3340.
Aydogdu A, Öztürk MO, Oguz MC, Altunel F (2001). Investigations on metazoon parasites of common carp (Cyprinus carpio L. 1758) in Dalyan Lagoon, Karacabey, Turkey. Acta Vet-Beograd 51: 351358.
Aydoğdu A, Yıldırımhan HS, Altunel FN (1997). İznik Gölünde yaşayan balıkları (Cyprinus carpio L.) üzerinde yaşayan bazı metazoon parazitler üzerine araştırmalar. Türk Parazitol Derg 21: 442445 (in Turkish).
Balon EK (1995). The common carp, Cyprinus carpio: its wild origin, domestication in aquaculture, and selection as colour nishikigoi. Guelph Ichthyol Rev 3: 155.
Balon EK (2006). The oldest domesticated fishes, and the consequences of an epigenetic dichotomy in fish culture. Aqua J Ichth Aquat Biol 11: 4786.
Barata S, Dörücü M (2014). Karakaya Baraj Gölü Kömürhan bölgesinden yakalanan bazı balıklarda endohelmintlerin araştırılması. Fırat Üniv Fen ve Müh Bil Derg 26: 5968 (in Turkish).
Baru V, Peňáz M, Kohlmann K (2002). Cyprinidae 2. Part III: Carassius to Cyprinus. Gasterosteidae. In: Bănărescu PM, Paepke HJ, editors. The Freshwater Fishes of Europe. Vol. 5/III. Wiebelsheim, Germany: Aula-Verlag, pp. 85179.
Becer ZA, Kara D (1998). Kovada Gölünden yakalanan sazan (Cyprinus carpio L. 1758) balıklarının populasyon yapısı ve parazitleri üzerine bir araştırma. Türk Parazitol Derg 22: 199 203 (in Turkish).
Bråten T (1966). Host specificity in Schistocephalus solidus. Parasitology 4: 657664.
Buhurcu Hİ, Öztürk MO (2007). Akşehir Gölündeki Cyprinus carpio Linnaeus, 1758 ve Alburnus nasreddini Battalgil, 1944nin endoparazit faunası üzerine bir araştırma. Fırat Üniv Fen ve Müh Bil Derg 19: 109113 (in Turkish).
Burgu A, Oğuz T, Körting W, Güralp N (1988). İç Anadolunun bazı yörelerinde tatlısu balıklarının parazitleri. Etlik Vet Mikrob Derg 6: 143166 (in Turkish).
Cengizler İ, Aytac N, Sahan (Azizoğlu) A, Ozak AA, Genç E (2001). Ectoendo parasite investigation on mirror carp (Cyprinus carpio L., 1758) captured from the River Seyhan, Turkey. E.Ü. Su Ürün Derg 18: 8790.
Cengizler İ, Sarıhan E, Çevik C (1991). Almus (Tokat) Baraj Gölünde yaşayan cyprinidlerde ligulosis araştırması. In: Ege Üniv Su Ürünleri Fakültesi, Eğitimin 10. Yılında Su Ürünleri Sempozyumu. İzmir, Turkey: Ege University, pp. 371375 (in Turkish).
Çetinkaya O (2010). Distribution, ecology and use of common carp (Cyprinus carpio) in Turkey. In: 1st International Symposium of Fisheries and Fishing Tourism, Zbornik Radova Proceedings. Boračko Lake, Bosnia and Herzegovina; 2324 June 2010.
Boračko Lake, Bosnia and Herzegovina: Center for Fisheries Neretva Konjic, pp. 173188.
Ceylan Y (2002). Çapalı gölü (Dinar-Afyon) balıklarının parazitolojik yönden incelenmesi. MSc, Süleyman Demirel University, Isparta, Turkey (in Turkish).
Chien SM (1974). Dactylogyrids from North American cyprinids of the genus Nocomis. The Bellicus group. J Parasitol 60: 585594.
Chistiakov DA, Voronova NV (2009). Genetic evolution and diversity of common carp Cyprinus carpio L. Cent Eur J Biol 4: 304312.
Chubb JC (1977). Seasonal occurrence of helminths in freshwater fishes. Part 1. Monogenea. In: Dawes B, editor. Advances in Parasitology. Vol. 15. London, UK: Academic Press, pp. 133 200.
Çolak HS (2013). Metazoan parasites of fish species from Lake Sığırcı (Edirne, Turkey). Turk J Vet Anim Sci 37: 200205.
Copp GH, Bianco PG, Bogutskaya NG, Erős T, Falka I, Ferreira MT, Fox MG, Freyhof J, Gozlan RE, Grabowska J et al. (2005). To be, or not to be, a non-native freshwater fish? J Appl Ichthyol 21: 242262.
Demirtaş M, Şenel Ü (2012). Terkos Gölündeki sazan (Cyprinus carpio L. 1758)da gölüren ektoparazitlerin mevsimsel dağılımları. Erciyes Üniv Fen Bilim Enst Derg 15: 5258 (in Turkish).
Dörücü M, İspir Ü (2005). Keban Baraj Gölünden avlanabilen balık türlerinde iç paraziter hastalıkların incelenmesi. Fırat Üniv Fen ve Mühendislik Bilim Derg 17: 400404 (in Turkish).
Dove ADM, Fletcher AS (2000). The distribution of the introduced tapeworm Bothriocephalus acheilognathi in Australian freshwater fishes. J Helminthol 74: 121128.
Erkul BS (1997). Ankara yöresindeki tatlısu balıklarında görülen helmint enfeksiyoları. PhD, Ankara University, Ankara, Turkey (in Turkish).
Geldiay R, Balık S (1974). Türkiye tatlı su balıklarında rastlanan başlıca iç ve dış parazitler. Ege Üniversitesi Fen Fakültesi Monografiler Serisi No. 14. İzmir, Turkey: Ege University (in Turkish).
Hoffmann GL (1999). Parasites of North American Freshwater Fishes. 2nd ed. New York, NY, USA: Cornell University Press.
Hoffmann RC (1995). Environmental change and the culture of common carp in medieval Europe. Guelph Ichthyol Rev 3: 5785.
Innal D, Erkakan F (2006). Effects of exotic and translocated fish species in the inland waters of Turkey. Rev Fish Biol Fish 16: 3950.
İnnal D, Keskin N, Erkakan F (2007). Distribution of Ligula intestinalis (L.) in Turkey. Turk J Fish Aquat Sci 7: 1922.
Jeney Z, Jeney G (1995). Recent achievements in studies on diseases of common carp (Cyprinus carpio L.). Aquaculture 129: 397 420.
Karakişi H, Demir S (2012). Metazoan parasites of the common carp (Cyprinus carpio L., 1758) from Tahtalı Dam Lake (İzmir). Türk Parazitol Derg 36: 174177.
Kartal K, Öztürk MO (2009). Akşehir Gölü (Konya)ndeki bazı balıkların (Cyprinus carpio Linnaeus, 1758; Cobitis simplicispinna Hanko, 1924) ektoparazit faunası üzerinde araştırmalar. Türk Parazitol Derg 33: 101106 (in Turkish).
Kayis S, Ozcelep T, Capkin E, Altinok I (2009). Protozoan and metazoan parasites of cultured fish in Turkey and their applied treatments. Bamidgeh 61: 93102.
Kennedy CR (1993). Introductions, spread and colonization of new localities by fish helminth and crustacean parasites in the British Isles: a perspective and appraisal. J Fish Biol 43: 287 301.
Kılınçaslan MO (2009). Yamula Baraj Gölü(Kayseri)nde yaşayan bazı ekonomik balık türlerinde parazitolojik incelemeler. MSc, Çukurova University, Adana, Turkey (in Turkish).
Kır İ, Ayvaz Y, Barlas M, Tekin Özan S (2004). Karacaören I Baraj Gölünde yaşayan sazan (Cyprinus carpio L., 1758)lardaki parazitlerin mevsimsel dağılımları ve etkileri. Türk Parazitol Derg 28: 4549 (in Turkish).
Kır İ, Samancı İ, Erdoğan M (2013). The relationship between growth and parasites in carp (Cyprinus carpio L., 1758) inhabiting Karacaören II Dam Lake. Pakistan J Zool 45: 14511453.
Kır İ, Tekin Özan S (2007). Helminth infections in common carp, Cyprinus carpio L., 1758 (Cyprinidae) from Kovada Lake (Turkey). Türk Parazitol Derg 31: 232236.
Kirpitchnikov VS (1999). Genetics and Breeding of Common Carp. Paris, France: INRA.
Kosswig C (1955). Zoogeography of the Near East. Syst Biol 4: 4973.
Kutlu HL, Öztürk MO (2006). Karamık Gölü (Afyonkarahisar)deki Cyprinus carpio Linnaeus, 1758 (sazan)nun metazoon parazitleri üzerinde anatomik, morfolojik ve ekolojik bir araştırma. Ege Üniv Su Ürün Derg 23: 389393 (in Turkish).
Lom J (1981). Fish invading dinoflagellates: a synopsis of existing and newly proposed genera. Folia Parasitol 28: 311.
Memiş D, Kohlmann K (2006). Genetic characterization of wild common carp (Cyprinus carpio L.) from Turkey. Aquaculture 258: 257262.
Molnár K (2009). Data on the parasite fauna of the European common carp Cyprinus carpio carpio and Asian common carp Cyprinus carpio haematopterus support an Asian ancestry of the species. AACL Bioflux 2: 391400.
Oğuz MC (1991). Bursa yöresindeki bazı tatlı sulardan (Kodacere- Ekinli-Uluabat) yakalan sazan balığı (Cyprinus carpio L. 1758) ekto parazitleri üzerine bir araştırma. Türk Parazitol Derg 15: 103110 (in Turkish).
Oğuz MC, Öztürk MO, Altunel FN, Ay YD (1996). Uluabat (Apolyont) Gölünde yakalanan sazan balıkları (Cyprinus carpio L. 1758) üzerine parazitolojik bir araştırma. Türk Parazitol Derg 20: 97103 (in Turkish).
Öktener A (2003). A checklist of metazoan parasites recorded in freshwater fish from Turkey. Zootaxa 394: 128.
Öktener A (2014). Revision of parasitic helminths reported in freshwater fish from Turkey with new records. Transylv Rev Syst Ecol Res 16: 156.
Öktener A, Torcu Koç H, Erdoğan Z (2009). Fish/parasites interrelationships in Turkey: a review. Ittiopatologia 6: 121 139.
Öktener A, Trilles JP, Leonardos I (2007). Five ectoparasites from Turkish fish. Türk Parazitol Derg 31: 154157.
Önsoy B, Filiz H, Tarkan AS, Bilge G, Tarkan AN (2011). Occurrence of non-native fishes in a small man-made lake (Lake Ula, Muğla): past, present, future perspectives. Turk J Fish Aquat Sci 11: 209215.
Özbek M, Öztürk MO (2010). Kunduzlar Baraj Gölü (Kırka, Eskişehir)nde yaşayan bazı balıkların Ligula intestinalis plerocercoid L., 1758 enfeksiyonu üzerine araştırmalar. Türk Parazitol Derg 34: 112117 (in Turkish).
Özer A (2002). Co-existence of Dactylogy rus anchoratus Dujardin, 1845 and D. extensus Mueller & Van Cleave, 1932 (Monogenea), parasites of common carp (Cyprinus carpio). Helmintologia 39: 4550.
Özer A, Erdem O (1999). Ectoparasitic protozoa fauna of the common carp (Cyprinus carpio L., 1758) caught in the Sinop region of Turkey. J Nat Hist 32: 441454.
Özer A, Erdem O (1999). The relationship between occurrence of ectoparasites, temperature and culture conditions: a comparison of farmed and wild common carp (Cyprinus carpio L., 1758) in the Sinop region of northern Turkey. J Nat Hist 33: 483491.
Öztürk MO (2005). Eber Gölü (Afyon)ndeki sazan (Cyprinus carpio L.)ların metazoon parazitleri üzerine bir araştırma. Türk Parazitol Derg 29: 204210 (in Turkish).
Öztürk MO (2010). Manyas Gölü (Bandırma)ndeki Cyprinus carpio L.nun Gy rodactylus (Monogenoidea, Platyhelminthes) enfeksiyonu üzerine bir araştırma. Afyon Kocatepe Üniv Fen Bilim Derg 2: 105113 (in Turkish).
Öztürk MO (2011a). Emre Baraj Gölü (Afyonkarahisar)deki üç cyprinid balık türünün helmint faunası üzerine bir araştırma. Afyon Kocatepe Üniv Fen Bilim Derg 11: 2329 (in Turkish).
Öztürk MO (2011b). Kunduzlar Baraj Gölü (Kırka, Eskişehir)ndeki balıkların sestod faunası üzerine incelemeler. Afyon Kocatepe Üniv Fen Bilim Derg 11: 5156 (in Turkish).
Öztürk MO (2011c). Manyas Gölü (Balıkesir)nde yaşayan bazı balıkların Paradiplozoon homoion (Monogenea, Diplozoidae) enfeksiyonu üzerine araştırmalar. Fırat Üniv Fen Fen Bilim Derg 23: 5761 (in Turkish).
Öztürk MO (2012). Emre Baraj Gölü (Afyonkarahisar)ndeki üç cyprinid balık türünün Argulus f oliaceus enfeksiyonu üzerine araştırma. İstanbul Üniv Vet Fak Derg 38: 183190 (in Turkish).
Öztürk MO, Altunel FN (2006). A study of the metazoan parasite fauna of Cyprinus carpio L. (common carp) linked to seasonal changes and host ages in Lake Manyas, Turkey. Bull Eur Assoc Fish Pathol 26: 252259.
Öztürk MO, Bulut S (2006). Selevir Baraj Gölü (Afyonkarahisar)ndeki Cyprinus carpio L. (sazan)nun metazoon parazit faunası üzerine bir araştırma. Fırat Üniv Fen ve Mühendislik Bilim Derg 18: 143149 (in Turkish).
Öztürk T, Özer A (2014). Monogenean fish parasites, their host preferences and seasonal distributions in the Lower Kızılırmak Delta (Turkey). Turk J Fish Aquat Sci 14: 367378.
Panek FM (1987). Biology and ecology of carp. In: Cooper EL, editor. Carp in North America. Bethesda, MD, USA: American Fisheries Society, pp. 115.
Paperna I (1964). The metazoan parasite fauna of Israel inland water fishes. Bamidgeh 16: 366.
Pişkin Ç, Utuk AE (2008). Şanlıurfa balıklıgöl sazanlarında Dactylogy rus sp. ve Trichodina sp. olgusu. Etlik Vet Mikrobiyol Derg 19: 912 (in Turkish).
Sağlam N (1992). Keban Baraj Gölünden yakalanan balıklarda görülen eksternal parazitlerin incelenmesi. MSc, Fırat University, Elazığ, Turkey (in Turkish).
Scholz T, Brabec J, Králová-Hromadová I, Oros M, Bazsalovicsová E, Ermolenko A, Hanzelová V (2011). Revision of Khawia spp. (Cestoda: Caryophyllidea), parasites of cyprinid fish, including a key to their identification and molecular phylogeny. Folia Parasitol 58: 197223.
Selver MM, Beyazıt A, Tay S, Tokşen E (2013). Sazan baliği (Cyprinus carpio L. 1758) yetiştiriciliği yapilan işletmelerde görülen helmintlerin araştirilmasi. Bornova Vet Bil Derg 35: 18 (in Turkish).
Sönmez ŞN (1996). Mogan Gölü balıklarında parazit faunasının incelenmesi. BSc, Ankara University, Ankara, Turkey (in Turkish).
Soylu E (2009). Monogenean parasites on the gills of some fish species from Lakes Sapanca and Durusu, Turkey. Ege Üniv Su Ürün Derg 26: 247251.
Soylu E, Emre Y (2007). Monogenean and cestode parasites of Pseudophoxinus antalyae, Bogutskaya 1992 and Cyprinus carpio, Linnaeus 1758 from Kepez Antalya, Turkey. Bull Eur Assoc Fish Pathol 27: 2328.
Tarkan AS, Ekmekçi FG, Vilizzi L, Copp GH (2014). Risk screening of non-native freshwater fishes at the frontier between Asia and Europe: first application in Turkey of the Fish Invasiveness Screening Kit (FISK). J Appl Ichthyol 30: 392398.
Tekin-Özan S, Kır İ, Barlas M (2008). Helminth parasites of common carp (Cyprinus carpio L., 1758) in Beyşehir Lake and population dynamics related to month and host size. Turk J Fish Aquat Sci 8: 201205.
Topçu A, Taşçı S (1993). Van Yöresinde bulunan sazan (Cyprinus carpio L. 1758)ların sindirim kanalı helminteri. Yüzüncü Yıl Üniv Vet Fak Derg 4: 121144 (in Turkish).
Turgut E, Develi N, Yeşilayer N, Buhan E (2011). Seasonal occurrence of Ligula intestinalis infection in cyprinids from Almus Dam Lake, Turkey. KSÜ Doğa Bil Derg 14: 911.
Turkish Statistical Institute (2012). Su Ürünleri İstatistikleri/Fishery Statistics 2011. Ankara, Turkey: Turkish Statistical Institute, Printing Division.
Türkmen H, Tüzer E (1992). İznik Gölünnde sazan ve akbalıklararda sindirim kanalı helmint enfeksiyonlarının yaygınlığı. İstanbul Üniv Vet Fak Derg 18: 109119 (in Turkish).
Uzunay E, Soylu E (2006). Sapanca Gölünde yaşayan sazan (Cyprinus carpio Linnaeus, 1758) ve karabalık (Vimba vimba Linnaeus, 1758)ın metazoan parazitleri. Türk Parazitol Derg 30: 141150 (in Turkish).
Vilizzi L (2012). The common carp, Cyprinus carpio, in the Mediterranean region: origin, distribution, economic benefits, impacts and management. Fish Manage Ecol 19: 93110.
Vilizzi L, Tarkan AS, Ekmekçi FG (2013). Stock characteristics and management insights for common carp (Cyprinus carpio) from Anatolia: a review of weightlength relationships and condition factors. Turk J Fish Aquat Sci 13: 759775.
Vilizzi L, Ekmekçi FG, Tarkan AS (2014a). Natural diet of common carp (Cyprinus carpio L., 1758) in Anatolia (Turkey): a review. Med Mar Sci 15: 216218.
Vilizzi L, Ekmekçi FG, Tarkan AS, Jackson ZJ (2015). Growth of common carp Cyprinus carpio in Anatolia (Turkey), and relative to native and invasive areas worldwide. Ecol Freshwat Fish (in press).
Vilizzi L, Tarkan AS, Ekmekçi FG (2014b). Reproductive biology of common carp (Cyprinus carpio L., 1758) in Anatolia (Turkey): a review. Med Mar Sci 15: 218222.
Welcomme RL (1988). International Introductions of Inland Aquatic Species. Fisheries Technical Paper 294. Rome, Italy: FAO.
Yetim M (1985). Eskişehirde tüketilen balıklarda görülen parazitler. MSc, Anadolu University, Eskişehir, Turkey (in Turkish).