Vibrio hepatarius septicemia with subacute enteritis in common guitarfish, Rhinobatos rhinobatos

Year 2023, Volume: 8 Issue: 2, 211 - 217, 30.06.2023

Kemal Bağcı , Neslihan Köstebekci , Merve Taşgın , Ebrucan Bulut , Kübra Balcı , Ece Yurddas , Nihed Ajmi , Burak Ozdemir , Fatih Hira Aytekin , Özkan Yavaş , Muhammed Duman

https://doi.org/10.35229/jaes.1281938

Abstract

Common guitarfish (Rhinobatos rhinobatos) are an endangered species and are placed on the red list of “Critically Endangered, CR” by the International Union for Conservation of Nature. Guitarfish are kept in captivity and are protected in public aquaria globally, but there is limited information about the diseases for this species. In this research, mortalities (14%) observed in common guitarfish in a public aquarium are reported. Severe hemorrhagic lesions on the ventral body side and reduced feed intake were observed in the affected animals. Two guitarfish were referred for necropsy, microbiological and histopathological examination. Macroscopic findings included severe ecchymotic hemorrhages in the ventral body, bloating of the gastrointestinal tract due to invasive mass, and hyperemia of the colon vessels and obstruction of the colon lumen. Histopathological examination revealed degenerations and necrosis in the liver, desquamation of intestinal villi, severe mononuclear cell infiltration and fibrosis in distal intestine, severe bacterial aggregates in different organs, pancreatitis, vasculitis, and filamentous bacteria-like structures. Vibrio hepatarius was isolated and identified with multilocus sequence analysis (MLSA); multilocus sequence typing (MLST) revealed that the agent belonged to a novel sequence type, 247. After the first description of V. hepatarius in wild healthy adults of Whiteleg shrimp (Litopenaeus vannamei) from Ecuador, this is the first report of deaths due to V. hepatarius observed in common guitarfish kept in captivity in a public aquarium.

Keywords

Vibrio hepatarius, common guitarfish, ornamental fish, aquarium fish diseases

Supporting Institution

TUBİTAK

Project Number

1919B012004874

Thanks

The study was supported from TUBITAK 2209-A project with project number: 1919B012004874. We are grateful to Assoc. Prof. Dr. Taci Cangul for scientific contributions.

Gitar balıklarında (Rhinobatos rhinobatos) Vibrio hepatarius kaynaklı subakut enteritik septisemi

Abstract

Gitar balığı (Rhinobatos rhinobatos) nesli tükenmekte olan bir balık türdür ve Uluslararası Doğayı Koruma Birliği tarafından "Kritik Tehlike Altında, CR" kırmızı listesine alınmıştır. Gitar balığı çoğunlukla akvaryumlarda tutulur ve küresel olarak halka açık akvaryumlarda korunmaya çalışır, ancak bu türün hastalıkları hakkında sınırlı bilgi bulunmaktadır. Bu araştırmada halka açık bir akvaryumda gitar balıklarında görülen mortalitelere neden olan enfeksiyon (%14) araştırılmıştır. Etkilenen hayvanlarda vücudun ventral tarafında önemli hemorajik lezyonlar ve yem alımında azalma gözlenmiştir. İki gitar balığı otopsi, mikrobiyolojik ve histopatolojik inceleme için laboratuvara soğuk zincir altında gönderilmiştir. Makroskobik bulgular ventral bölgede ekimotik kanamalar, invaziv kitle nedeniyle gastrointestinal sistemde şişkinlik ve kolon damarlarında hiperemi ve kolon lümeninde tıkanıklık tespit edilmiştir. Histopatolojik incelemede karaciğerde dejenerasyon ve nekroz, barsak villuslarında deskuamasyon, barsak distalinde şiddetli mononükleer hücre infiltrasyonu ve fibrozis, farklı organlarda ciddi bakteriyel kümelenmeler, pankreatit, vaskülit ve filamentli bakteri benzeri yapılar belirlenmiştir. Vibrio hepatarius etken izolasyonu yapılmış ve multilocus sekans analizi (MLSA) ile karakterize edilmiştir. Multilocus sekans tiplemesi (MLST), etkenin yeni bir sekans tipi olan ST 247'ye ait olduğunu ortaya koymuştur. Ekvador'dan Whiteleg karidesinin (Litopenaeus vannamei) doğal sağlıklı yetişkinlerinde V. hepatarius'un ilk tanımından sonra, bu etkene bağlı ölümler gitar balıklarında ilk defa rapor edilmektedir.

Keywords

Vibrio hepatarius, gitar balığı, akvaryum balığı, akvaryum balığı hastalıkları

Project Number

1919B012004874

References

• Del-Pozo, J., Crumlish, M., Turnbull, J. F., & Ferguson, H. W. (2010). Histopathology and ultrastructure of segmented filamentous bacteriaassociated rainbow trout gastroenteritis. Veterinary Pathology, 47(2), 220–230. DOI: 10.1177/0300985809359381
• Dulvy, N. K., Fowler, S. L., Musick, J. A., Cavanagh, R. D., Kyne, P. M., Harrison, L. R., Carlson, J. K., Davidson, L. N. K., Fordham, S. V., Francis, M. P., Pollock, C. M., Simpfendorfer, C. A., Burgess, G. H., Carpenter, K. E., Compagno, L. J. V., Ebert, D. A., Gibson, C., Heupel, M. R., Livingstone, S. R., … White, W. T. (2014). Extinction risk and conservation of the world’s sharks and rays. ELife, 2014(3). DOI: 10.7554/eLife.00590.001
• Emam, A.M., Hashem, M., Gadallah, A.O. & Haridy, M. (2019). An outbreak of Vibrio alginolyticus infection in aquarium-maintained dark-spotted (Himantura uarnak) and Tahitian (H. fai) stingrays. The Egyptian Journal of Aquatic Research; Elsevier. DOI: 10.1016/J.EJAR.2019.05.003
• FAO. (2020). The State of World Fisheries and Aquaculture 2020. https://www.fao.org/state-offisheries-aquaculture Felsenstein, J. (1985). Confidence Limits on Phylogenies: An Approach Using the Bootstrap. Evolution, 39(4), 783. DOI: 10.2307/2408678
• Fioravanti, M.L. & Florio, D. (2017). Common Diseases in Marine Ornamental Fishes. In R. Calado, I. Olivotto, M. P. Oliver, & J. G. Holt (Eds.), Marine Ornamental Species Aquaculture (pp. 347-380). John Wiley & Sons, Ltd. DOI: 10.1002/9781119169147.CH19
• Garner, M. M. (n.d.). Special Focus: Diseases of Aquatic Animals A Retrospective Study of Disease in Elasmobranchs. DOI: 10.1177/0300985813482147
• Geng, Y., Liu, D., Han, S., Zhou, Y., Wang, K.Y., Huang, X.L., Chen, D.F., Peng, X. & Lai, W.M. (2014). Outbreaks of vibriosis associated with Vibrio mimicus in freshwater catfish in China. Aquaculture, 433, 82-84. DOI: 10.1016/J.AQUACULTURE.2014.05.053
• Hurst, C.J. (2016). The Rasputin Effect: When Commensals and Symbionts Become Parasitic. In C. J. Hurst (Ed.), Advances in Environmental Microbiology (Vol. 3). Springer International Publishing. DOI: 10.1007/978-3-319-28170-4.
• Ina-Salwany, M.Y., Al-saari, N., Mohamad, A., Mursidi, F.A., Mohd-Aris, A., Amal, M.N.A., Kasai, H., Mino, S., Sawabe, T. & Zamri-Saad, M. (2019). Vibriosis in Fish: A Review on Disease Development and Prevention. Journal of Aquatic Animal Health, 31(1), 3-22. DOI: 10.1002/AAH.10045
• Jabado, R., Pacoureau, N., Diop, M., Dia, M., Ba, A., Williams, A., Dossa, J., Badji, L., Seidu, I., Chartrain, E., Leurs, G., Tamo, A., Porriños, G., VanderWright, W., Derrick, D., Doherty, P., Soares, A., De Bruyne, G. & Metcalfe, K. (2021). Common Guitarfish. The IUCN Red List of Threatened Species 2021. https://doi.org/https://dx.doi.org/10.2305/IUCN. UK.2021-1.RLTS.T63131A124461877.en
• Jolley, K.A., Bray, J.E. & Maiden, M.C.J. (2018). Openaccess bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications [version 1; referees: 2 approved]. Wellcome Open Research, 3. DOI: 10.12688/wellcomeopenres.14826.1.
• Kang, G., Choi, K.M., Joo, M.S., Woo, W.S. & Park, C.I. (2022). A case report of secondary infection by Vibrio splendidus associated with gas bubble disease in syngnathid fishes (Syngnathus schlegeli and Hippocampus haema). Fisheries and Aquatic Sciences, 25(1), 40-48. DOI: 10.47853/FAS.2022.E5.
• Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution, 35(6), 1547. DOI: 10.1093/MOLBEV/MSY096.
• Li, G., Zhao, D., Huang, L., Sun, J., Gao, D., Wang, H., Tan, Y. & Liang, L. (2006). Identification and phylogenetic analysis of Vibrio vulnificus isolated from diseased Trachinotus ovatus in cage mariculture. Aquaculture, 261(1), 17-25. DOI: 10.1016/j.aquaculture.2006.07.013.
• Lieke, T., Meinelt, T., Hoseinifar, S.H., Pan, B., Straus, D. L. & Steinberg, C.E.W. (2020). Sustainable aquaculture requires environmental-friendly treatment strategies for fish diseases. In Reviews in Aquaculture (Vol. 12, Issue 2, pp. 943–965). John Wiley & Sons, Ltd. DOI: 10.1111/raq.12365.
• Marudhupandi, T., Kumar, T.T.A., Prakash, S., Balamurugan, J. & Dhayanithi, N.B. (2017). Vibrio parahaemolyticus a causative bacterium for tail rot disease in ornamental fish, Amphiprion sebae. Aquaculture Reports, 8, 39-44. DOI: 10.1016/J.AQREP.2017.09.004.
• McCarthy, D.H. (1976). Vibrio disease in eels. Journal of Fish Biology, 8(4), 317-320. DOI: 10.1111/J.1095-8649.1976.TB03955.X.
• Nei, M. & Kumar, S. (2000). Molecular Evolution and Phylogenetics. Oxford University Press. OIE. (2015). Aquatic Animal Health Surveillance . In Aquatic Animal Health Code (pp. 1-28). https://www.oie.int/fileadmin/Home/eng/Health_ standards/aahc/2010/chapitre_aqua_ani_surveilla nce.pdf.
• Pramila, S. & Lipton, A.P. (2018). Occurrence of Vibrio mediterranei Pujalte and Garay, 1986 in aquarium reared marine ornamental fish. Journal of the Marine Biological Association of India, 60(2), 118-122. DOI: 10.6024/jmbai.2018.60.2.1928-18.
• Rahman, M.S., Martino, M.E., Cardazzo, B., Facco, P., Bordin, P., Mioni, R., Novelli, E. & Fasolato, L. (2014). Vibrio trends in the ecology of the venice lagoon. Applied and Environmental Microbiology, 80(8), 2372-2380. DOI: 10.1128/AEM.04133-13.
• Ransangan, J. & Mustafa, S. (2009). Identification of Vibrio harveyi isolated from diseased Asian seabass Lates calcarifer by use of 16S ribosomal DNA sequencing. Journal of Aquatic Animal Health, 21(3), 150-155. DOI: 10.1577/H09-002.1.
• Sampaio, A., Silva, V., Poeta, P. & Aonofriesei, F. (2022). Vibrio spp.: Life Strategies, Ecology, and Risks in a Changing Environment. Diversity, 14(2), 97. DOI: 10.3390/d14020097.
• Sonia, G. & Lipton, A. (2012). Antibiotic susceptibility of Vibrio species isolated from the captive–reared tropical marine ornamental blue damsel fish, Pomacentrus caeruleus (Quoy and Gaimard,. Ijms, 41(August), 348-354. http://nopr.niscair.res.in/handle/123456789/1455 2
• Sumithra, T.G., Reshma, K.J., Anusree, V.N., Sayooj, P., Sharma, S.R.K., Suja, G., Amala, P.V., Joseph, S. & Sanil, N.K. (2019). Pathological investigations of Vibrio vulnificus infection in Genetically Improved Farmed Tilapia (Oreochromis niloticus L.) cultured at a floating cage farm of India. Aquaculture, 511, 734217. https://doi.org/10.1016/J.AQUACULTURE.2019 .734217.
• Suzer, B., Yalgın, F., Saticioglu, I.B., Taskin, M., Yavas, O. & Duman, D. (2022). Macroscopic examination of cownose rays (Rhinoptera bonasus). J. Anatolian Env. and Anim. Sciences, 7(4), 444-450. DOI: 10.35229/jaes.1177624.
• Taskin, M., Ajmi, N., Bagci, K., Yurddas, E., Suzer, B., Altun, S. & Duman, M. (2022). The common guitarfish Rhinobatos rhinobatos: A descriptive anatomical study and proposed dissection techniques. Journal of Veterinary Medicine Series C: Anatomia Histologia Embryologia. DOI: 10.1111/AHE.12860.
• Thompson, F.L., Thompson, C.C., Hoste, B., Vandemeulebroecke, K., Gullian, M. & Swings, J. (2003). Vibrio fortis sp. nov. and Vibrio hepatarius sp. nov., isolated from aquatic animals and the marine environment. International Journal of Systematic and Evolutionary Microbiology, 53(5), 1495–1501. DOI: 10.1099/ijs.0.02658-0.
• Tomasoni, M., Esposito, G., Mugetti, D., Pastorino, P., Stoppani, N., Menconi, V., Gagliardi, F., Corrias, I., Pira, A., Acutis, P.L., Dondo, A., Prearo, M. & Colussi, S. (2022). The Isolation of Vibrio crassostreae and V. cyclitrophicus in Lesser-Spotted Dogfish (Scyliorhinus canicula) Juveniles Reared in a Public Aquarium. Journal of Marine Science and Engineering, 10(1), 114. DOI: 10.3390/jmse10010114.
• Turgay, E., Yardımcı, R.E. & Karataş, S. (2018). First case report of Vibrio harveyi infection in salema (Sarpa salpa) in a public aquarium. Süleyman Demirel Üniversitesi Eğirdir Su Ürünleri Fakültesi Dergisi, 14(3), 166-172.
• Won, K.M., Kim, K.H. & Park, S.Il. (2009). Vibrio harveyi associated with deep skin ulcer in river puffer, Takifugu obscures, exhibited in a public aquarium. Aquaculture Research, 40(8), 963– 967. DOI: 10.1111/J.1365-2109.2008.02151.X.
• Yeoh, H.I., Izzatty, R., Furusawa, G., Amirul, A.A.A., Shu-Chien, A.C. & Sung, Y.Y. (2021). The Vibrio-predatory filamentous bacteria effectively removed acute hepatopancreatic necrosis disease (AHPND) causative Vibrio parahaemolyticus in vitro. Aquaculture Reports, 21(October), 100910. DOI: 10.1016/j.aqrep.2021.100910.
• Zhang, X.H., He, X. & Austin, B. (2020). Vibrio harveyi: a serious pathogen of fish and invertebrates in mariculture. Marine Life Science and Technology, 2(3), 231-245. DOI: 10.1007/S42995-020-00037- Z/TABLES/3