First Report of Ligula intestinalis (Cestoda: Pseudophyllidea) in Barbus ercisianus (Cypriniformes: Cyprinidae) from the Nemrut Crater Lake, Turkey

Abstract

Van Basin has a rich geographical structure in terms of water resources and endemic fish species. In this study, Ligula intestinalis parasite, which is the host of Barbus ercisianus living in Nemrut Crater Lake, was recorded for the first time. The parasite was described molecularly as well as morphologically. In this context, a primer set was designed for molecular identification for the 28S rRNA gene region of L. intestinalis. Real-Time PCR results with the designed primers gave positive results in all parasite samples. The results were confirmed by a single peak (87) in the HRM analysis.

Keywords

• Cestodes
• Fish diseases
• Fish parasites
• Real-Time PCR

Nemrut Krater (Turkey) Gölü’nde Yaşayan Barbus ercisianus (Cypriniformes: Cyprinidae) Balık Türünde Ligula intestinalis (Cestoda: Pseudophyllidea)‘in İlk Bildirimi

Öz

Van Gölü Havzası su kaynakları ve endemik balık türleri açısından zengin bir coğrafi yapıya sahiptir. Bu çalışmada Nemrut Krater Gölü‘nde yaşayan Barbus ercisianus‘ta konakçı olan Ligula intestinalis parazitinin ilk kez kaydı verilmiştir. Parazit, morfolojik tanımlamanın yanı sıra moleküler olarak da tanımlanmıştır. Bu bağlamda, moleküler tanımlama için, L. intestinalis‘in 28S rRNA gen bölgesini hedef alan bir primer seti tasarlanmıştır. Tasarlanan primerler ile gerçekleştirilen Real-Time PCR sonuçları tüm parazit örneklerinde pozitif sonuç vermiştir. Elde edilen sonuçlar, HRM analizinde tek bir pik (87) ile doğrulanmıştır.

Anahtar Kelimeler

• Sestodlar
• Balık hastalıkları
• Balık parazitleri
• Real-Time PCR

References

1. Adızel, O., Yıldız, M. Z., Ünal, M., Azizoğlu, E., Öztürk, F., & Akman, B. (2017). Biodiversity of Van Reed, Eastern Turkey. Commagene Journal of Biology, 1, 16-26.
2. Başaran, A. & Kelle, A. (1976). Devegeçidi Baraj Gölü’nde yaşayan bazı balık türlerinde Ligula intestinalis, plerocercoidlerinin yayılma oranı ve etkileri. Biyoloji Dergisi, 26, 45-56.
3. Bouzid, W., Lek, S., Mace, M., Ben Hassine, O., Etienne, R., Legal, L., & Loot G. (2008a). Genetic diversity of Ligula intestinalis (cestoda: Diphyllobothriidea) based on analysis of inter‐simple sequence repeat markers. Journal of Zoological Systematics and Evolutionary Research, 46, 289-296.
4. Bouzid, W., Stefka, J., Hypsa, V., Lek, S., Scholz, T., Legal, L., Hassine, O. K. B. & Loot, G. (2008b). Geography and host specificity: Two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (cestoda: Diphyllobothriidae). International Journal for Parasitology, 38, 1465-1479.
5. Cantoray, R. & Özcan, A. (1975). Ligulose in freshwater fish in Elazig. Fırat Üniversiresi Veteriner Fakültesi Dergisi, 2, 298-301.
6. Chapman, A., Vallejo, V., Mossie, K. G., Ortiz, D., Agabian, N. & Flisser, A. (1995). Isolation and characterization of species-specific DNA probes from Taenia solium and Taenia saginata and their use in an egg detection assay. Journal of Clinical Microbiology, 33, 1283-1288.
7. Demirkuş, N., Koyuncu, M. & Gül, M. (2018). Endemic plants of Lake Van Basin. Anatolian Journal of Botany, 2, 70-83.
8. Demirtaş, M. & Altındağ, A. (2011). The seasonal infection distribution of Ligula intestinalis Plerocercoid L., 1758 on some fishes (Cyprinidae) living in Terkos Lake. Van Veterinary Journal, 22, 147-151.

9. Elp, M., Atıcı, A. A., Şen, F. & Duyar, H. A. (2016). Distribution of Fish Species in the Van Lake Basin. Yuzuncu Yil University Journal of Agricultural Science, 26, 563-568.
10. Flisser, A., Reid, A., Garcia-Zepeda, E. & Mcmanus, D. (1988). Specific detection of Taenia saginata eggs by DNA hybridisation. Lancet, 17, 1429-1430.
11. Geldiay, R. & Balık, S. (2009). Türkiye tatlısu balıkları. İzmir: Ege Üniversitesi Basımevi.
12. Gonzalez, L. M., Montero, E., Morakote, N., Puente, S., De Tuesta, J. L. D., Serra, T., López-Velez, R., Mcmanus, D. P., Harrison, L. J. & Parkhouse, R. M. E. (2004). Differential diagnosis of Taenia saginata and Taenia saginata asiatica taeniasis through PCR. Diagnos Microbiol Infec Disease, 49, 183-188.
13. Gonzalez, L. M., Montero, E., Puente, S., López-Velez, R., Hernández, M., Sciutto, E., Harrison, L. J., Parkhouse, R. M. E. & Gárate, T. (2002). PCR tools for the differential diagnosis of Taenia saginata and Taenia solium taeniasis/cysticercosis from different geographical locations. Diagnostic Microbiology and Infectious Disease, 42, 243-249.
14. Hajirostamloo, M. (2009). A report on occurrence and parasite-host of Ligula intestinalis in Sattarkhan Lake (East Azerbaijan-Iranian). International Scholarly and Scientific Research & Innovation, 3, 458-461.
15. Harrison, L., Delgado, J. & Parkhouse, R. (1990). Differential diagnosis of Taenia saginata and Taenia solium with DNA probes. Parasitology, 100, 459-461.
16. İnnal, D., Keskin, N. & Erk’akan, F. (2007). Distribution of Ligula intestinalis in Turkey. Turkish Journal of Fisheries and Aquatic Sciences, 7, 19-22.
17. Karaman, M. (1971). Revision der barben europas, vorderasiatischen arten des genus capoeta (varicorhinus, partim). Ham Zool Mus Ins, 66, 17-54.
18. Kayis, S., Ozcelep, T., Capkin, E. & Altinok, I. (2009). Protozoan and metazoan parasites of cultured fish in Turkey and their applied treatments. Israeli Journal of Aquaculture – Bamigdeh, 61(1-4):93-102.
19. Kennedy, C. & Burrough, R. (1981). The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilis rutilis. Journal of Fish Biology, 19, 105-126.
20. Koyun, M., Ulupınar, M. & Gül, A. (2015). Seasonal distribution of metazoan parasites on kura barbell (Barbus lacerta) in Eastern Anatolia, Turkey. Pakistan Journal of Zoology, 47, 1253-1261.
21. Kuluöztürk, M. F. & Doğru, M. (2015). Natural radioactivity levels on surface water of Nemrut Crater Lake (Bitlis, Turkey). Acta Physica Polonica A, 128, 397-399.
22. Kurttaş, T. & Tezcan, L. (2018). Water resources potential of Nemrut Caldera Lakes. Süleyman Demirel University Journal of Natural and Applied Sciences, 22, 823-831.
23. Mehraban, H. R., Sayyadzadeh, G., Malekzehi, H. & Ahmadi, A. (2015). First report of infection with the tapeworm Ligula intestinalis (Linnaeus, 1758) plerocercoids in persian bleak, Alburnus hohenackeri kessler, 1870 in Southeastern Iranian. Iranian J Ichthyol. Iranian Journal of Ichthyology, 1, 12-16.
24. Olson, P., Littlewood, D., Griffiths, D., Kennedy, C. & Arme, C. (2002). Evidence for the co-existence of separate strains or species of Ligula in lough neagh, Northern Ireland. Journal of Helminthology, 76, 171-174.
25. Önalan, S. (2016). Determination of phenotypic, serotypic and genotypic differences between Garvieae isolates obtained from rainbow trout farms in Van, Bitlis, Mus and Hakkari provinces. In: PhD Thesis. Van Yuzuncu Yıl University, Institute of Science, Van, Turkey.
26. Pinchi, V., Focardi, M., Martinelli, D., Norelli, G., Carboni, I., Gozzini, A., Romolini, C., Torricelli, F. & Ricci, U. (2013). DNA extraction method from teeth using qiacube. Forensic Science International: Genetics Supplement Series,4, 276-277.
27. Rishi, A. & Mcmanus, D. (1988). Molecular cloning of Taenia solium genomic DNA and characterization of taeniid cestodes by DNA analysis. Parasitology, 97, 161-176.
28. Saç, G., Serezli, E. E. & Okgerman, H. (2015). The occurrence of Ligula intestinalis in its fish host Rutilus rutilus and the effects of parasite on the fish growth (Büyükçekmece Reservoir, Turkey). Journal of Aquaculture Engineering and Fisheries Research, 2, 142-150.
29. Sakai, M. (1999). Current research status of fish immunostimulants. Aquaculture, 172, 63-92.
30. Şekercioğlu, Ç. H., Anderson, S., Akçay, Eç, Bilgin, Rç, Can, O. E., Semiz, G., Tavşanoğlu Ç., Yokeş, M. B., Soyumert, A., İpekdal, K., Sağlam, I. K., Yücel, M. & Dalfes, H. N. (2011). Turkeys globally important biodiversity in crisis. Biological Conservation, 144, 2752-2769.
31. Şen, F., Atıcı, A. A. & Elp, M. (2018). Endemic Fish Species of Van Lake Basin. Yuzuncu Yil University Journal of Agricultural Science, 28, 63-70.
32. Stefka, J., Gilleard, J., Grillo, V. & Hypsa, V. (2007). Isolation and characterization of microsatellite loci in the tapeworm Ligula intestinalis (cestoda: Pseudophyllidea). Molecular Ecology Notes, 7, 794-796.
33. Toyran, K., Adızel, Ö. & Azizoğlu, E. (2018). Road kills of mammal species in the Van Lake Basin (Turkey). Biological Diversity and Conservation, 11, 40-44.
34. Uzbilek, M. K. & Yıldız, H. Y. (2002). A report on spontaneous diseases in the culture of grass carp (Ctenopharyngodon idella Val. 1844), Turkey. Turkish Journal of Veterinary and Animal Sciences, 26, 407-410.
35. Wyatt, R. & Kennedy, C. (1989). Host‐constrained epidemiology of the fish tapeworm Ligula intestinalis. Journal of Fish Biology, 35, 215-227.