Refining the Occurrence of Viral Encephalopathy and Retinopathy, Photobacteriosis, and Vibriosis in Connection with Seawater Physicochemical Parameters: A Five-Year Case Study


Published: Feb 5, 2024
Keywords:
physicochemical parameters of water fish diseases Dicentrarchus labrax
EFTHIMIOS SPINOS
GEORGE KATSELIS
MICHAIL AGGELOS VALSAMIDIS
MARI DANIELLA WHITE
VASILEIOS BAKOPOULOS
Abstract

The marine environment and its physicochemical parameters play a pivotal role in the context of fish farming. Fundamental physicochemical factors of water, including temperature (T°C), salinity (S psu), dissolved oxygen (D.O. mg/l), and pH, exert a profound influence on the physiology of farmed aquatic animals and the composition of microbial communities. This study aimed to establish correlations between documented disease occurrences in sea bass intensive rearing and the prevailing physicochemical parameters of water. The objective was to analyse the significance of these parameters in disease outbreaks and develop a predictive model for the outbreak risk of key diseases. To this end, real-time physicochemical data were collected daily over five years (2011-2015) from two fish farms (A and B) located in the Gulf of Argostoli, island of Cephalonia, Western Greece. The focus was on incidences of Viral Encephalopathy and Retinopathy (VER), Photobacteriosis caused by Photobacterium damselae subsp. piscicida (PHDP) and Vibriosis caused by Vibrio anguillarum serotype O1 (VAO1). Statistically significant correlations were found between increasing water temperature and salinity and the occurrence of VER, PHDP, and VAO1 diseases. The reduction of dissolved oxygen, when combined with other parameters, synergistically triggered the manifestation of these three diseases. The study’s findings were discussed within the context of their potential to predict disease outbreaks based on fluctuations in the physicochemical parameters of water and anticipated climate change scenarios.

Article Details
  • Section
  • Research Article
Downloads
Download data is not yet available.
References
Abou Anni, I.S., Bianchini, A., Barcarolli, I.F., 2016. Salinity influence on growth, osmoregulation and energy turnover in juvenile pompano Trachinotus marginatus (Cuvier 1832). Aquaculture, 455, pp. 63-72.
Alaliyat, S., Yndestad, H., Davidsen, P.I., 2019. An agent-based approach for predicting patterns of pathogen transmission between aquaculture sites in the Norwegian fjords. Aquaculture, 505, 98-111.
Alicia, E., Toranzo, B., Magariños, Romalde, J.L., 2005. A review of the main bacterial fish diseases in mariculture systems. Aquaculture, 246 (1-4), 37-61.
Austin, B., Austin, D.A., 2016. Bacterial Fish Pathogens: Disease of Farmed and Wild Fish, (6th ed.) Springer International Publishing., V.,
Adams, A., Richards, R.H., 1995. Some biochemical properties and antibiotic sensitivities of Pasteurella piscicida isolated in Greece and comparison with strains from Japan, France and Italy. Journal of Fish Diseases, 18 (1), 1-7.
Bakopoulos, V., Nikolaou, I., Kalovyrna, N., Amirali, E., Kokkoris, G. et al., 2015. Prevention of fish photobacteriosis. Comparison of the efficacy of intraperitoneally administered commercial and experimental vaccines. Mediterranean Marine Science, 16 (2), 385-392.
Bakopoulos, V., Palaiologos, A., Poulos, K., Malatestas, K., Dimitrakopoulou, E. et al., 2018. Efficacy testing of anti-VNN vaccine formulations against the RGNNV b-nodavirus genotype in European sea bass (Dicentrarchus labrax). 3rd International Congress on Applied Ichthyology & Aquatic Environment, HydroMedit 2018, Volos, Greece, 8-11 November 2018.
Bellos, G., Angellidis, P., Miliou, H., 2015. Effect of Temperature and Seasonality Principal Epizootiological Risk Factor on Vibriosis and Photobacteriosis Outbreaks for European Sea Bass in Greece (1998-2013). Journal of Aquaculture Research & Development, 6 (5), 1-6.
Beman, J.M., Chow, C.E., King, A.L., Feng, Y., Fuhrman, J.A. et al., 2011. Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proceedings of the National Academy of Sciences, 108 (1), 208-213.
Boeuf, G., Payan, P., 2001. How should salinity influence fish growth. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 130 (4) 411-423.
Choi, K., Cope, W. G., Harms, C. A., Law, J. M., 2013. Rapid decreases in salinity. but not increases, lead to immune dysregulation in Nile tilapia Oreochromis niloticus (L.). Journal of Fish Diseases, 36 (4), 389-399.
Conides, A., Kougioufas, P., Glykokokalos, S., Asimakopoulou, G., Konstantinopoulou, A. et al., (2006). Investigation of eutrophic conditions of the Argostoli Bay of Kefallinia in relation to the fish farming activities. Expert opinion a. 148118 / 1-2-2006 HCMR. p. 5. 8-26. 28. 34. 40. 44-45.
Dalla, V.L., Zanella, L., Patarnello, P., Paolucci, L., Belvedere, P., et al., 2000. Development of a sensitive diagnostic assay for fish nervous necrosis virus based on RT-PCR plus nested PCR. Journal of Fish Diseases, 23 (5) 321-327.
Doblin, M.A., Van Sebille, E., 2016. Drift in ocean currents impacts intergenerational microbial exposure to temperature. Proceedings of the National Academy of Sciences, 113 (20), 5700-5705.
Eissa, A.E., Abou-Okada, M., Alkurdi, A.R.M., El Zlitne, R.A., Prince, A., et al., 2021. Catastrophic mass mortalities caused by Photobacterium damselae affecting farmed marine fish from Deeba Triangle, Egypt. Aquaculture Research, 52 (9), 4455-4466.
Ellis, A.E., 1989. Vibriosis of Salmonids in Scotland. Department of Agriculture and Fisheries for Scotland. Aquaculture Information Series Number 7.
Essam, H.M., Abdellrazeq, G.S., Tayel, S.I., Torky, H.A., Fadel, A.H., 2016. Pathogenesis of Photobacterium damselae subspecies infections in sea bass and sea bream. Microbial Pathogenesis, 99, 41-50.
Frans, I., Michiels, C.W., Bossier, P., Willems, K.A., Lievens, B. et al., 2011. Vibrio anguillarum as a fish pathogen: virulence factors, diagnosis and prevention. Journal of Fish Diseases, 34 (9), 643-661.
Frerichs, G.N., Tweedie, A., Starkey, W.G., Richards, R.H., 2000. Temperature, pH and electrolyte sensitivity, and heat, UV and disinfectant inactivation of sea bass (Dicentrarchus labrax) neuropathy nodavirus. Aquaculture, 185 (1-2), 13-24.
Fytianos, K., 1996. The pollution of the Seas, 2nd Edition. pp 71-74. 84. Grisez, L., Ollevier, F., 1995. Comparative Serology of the Marine Fish Pathogen Vibrio anguillarum. Applied and Environmental Microbiology, 61 (12), 4367-4373.
Hadj-Kacem, Ν., Aldrin, J.F., Romestand, Β., 1986. Influence immediate du brossage des bacs sur certains parameters anguins du loup d’ elevage Dicentrarchus labrax L.: effet du stress. Aquaculture, 59 (1) 53-59.
Hata, N., Okinaka, Y., Sakamoto, T., Iwamoto, T., Nakai, T., 2007. Upper temperature limits for the multiplication of betanodaviruses. Fish Pathology, 42 (4), 225-228.
Heenatigala, P.P.M., Fernando, M.U.L., 2016. Occurrence of bacteria species responsible for vibriosis in shrimp pond culture systems in Sri Lanka and assessment of the suitable control measures. Sri Lanka Journal Aquatic Science, 21 (1), 1-17.
Hickey, M.E., Lee, J.L., 2018, A comprehensive review of Vibrio (Listonella) anguillarum: ecology, pathology and prevention. Reviews in Aquaculture, 10 (3), 585-610.
Huang, Z., Ma, A., Wang, X., et al., 2015. Interaction of temperature and salinity on the expression of immunity factors in different tissues of juvenile turbot Scophthalmus maximus based on response surface methodology. Chinese Journal of Oceanology and Limnology, 33, 28–36.
Kanno, T., Nakai, T., Muroga, K., 2011. Mode of transmission of vibriosis among AyuPlecoglossus altivelis. Journal of Aquatic Animal Health, 1 (1), 2-6.
Korun, J., Timur, G., 2005. The first pasteurellosis case in cultured sea bass (Dicentrarchus labrax L.) at low marine water temperatures in Turkey. Israeli Journal of Aquaculture - Bamidgeh, 57, 197-206.
Krkošek, M., 2017. Population biology of infectious diseases shared by wild and farmed fish. Canadian Journal of Fisheries and Aquatic Sciences, 74 (4), 620-628.
Lages, M.A., Balado, M., Lemos, M.L., 2019. The Expression of Virulence Factors in Vibrio anguillarum Is Dually Regulated by Iron Levels and Temperature. Frontiers in Microbiology, 10,2335.
Larsen, J.L., 1984. Vibrio anguillarum: influence of temperature, PH, NaCl concentration and incubation time on growth. Journal of Applied Bacteriology, 57 (2),237-246.
Lattos, A., Giantsis, A.I., Tsavea, E., Kolygas, M., Athanassopoulou, F. et al., 2022. Virulence Genes and In Vitro Antibiotic Profile of Photobacterium damselae Strains, Isolated from Fish Reared in Greek Aquaculture Facilities. International Journal Animals, 12 (22), 3133.
Le Breton, A., Grisez, L., Sweetman, J., Olievier, F., 1997. Viral nervous necrosis (VNN) associated with mass mortalities in cage-reared seabass Dicentrarchus labrax (L.). Journal of fish diseases, 20 (2),145-151.
Lopez-Jimena, B., Cherif, N., Garcia-Rosado, E., Infante, C., Cano, I. et al., 2010. A combined RT-PCR and dot-blot hybridization method reveals the coexistence of SJNNV and RGNNV betanodavirus genotypes in wild meagre (Argyrosomus regius). Journal of Applied Microbiology, 109 (4), 1361-1369.
López-Olmeda, J.F., Oliveira, C., Kalamarz, H., Kulczykowska, E., Delgado, M.J., et al., 2009. Effects of water salinity on melatonin levels in plasma and peripheral tissues and on melatonin binding sites in European sea bass (Dicentrarchus labrax). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 152 (4), 486-490.
Lucas, S.J., Southgate, C.P., Tucker, S.C., 2019. Aquaculture: Farming Aquatic Animals and Plants. Third Edition. Edited and Published by John Wiley & Sons Ltd, 2019, p. 204.
Magarinos, B., Romalde, J.L., Bandín, I., Fouz, B., Toranzo, A.E., 1992. Phenotypic. antigenic and molecular characterization of Pasteurella piscicida strains isolated from fish. Applied and Environmental Microbiology, 58, (10), 3316-3322.
Maia, S., Marques, S.C., Dupont, S., Neves, M., Pinto, H.J. et al., 2022. Effects of ocean acidification and warming on the development and biochemical responses of juvenile shrimp Palaemon elegans (Rathke, 1837). Marine Environmental Research, 176, 105580.
Makridis, P., Mente, E., Grundvig, H., Gausen, M., Koutsikopoulos, C. et al., 2018. Monitoring of oxygen fluctuations in seabass cages (Dicentrarchus labrax L.) in a commercial fish farm in Greece. Aquaculture Research, 49 (2), 684-691.
Matanza, X.M., Osorio, C.R., 2018. Transcriptome changes in response to temperature in the fish pathogen Photobacterium damselae subsp. damselae: Clues to understand the emergence of disease outbreaks at increased seawater temperatures.
PLoS One, 13 (12), e0210118. Ndong, D.Y.Y., Lin, Y.H., Vaseeharan, B., Chen, J.C., 2007. The immune response of tilapia Oreochromis mossambicus and its susceptibility to Streptococcus iniae under stress in low and high temperatures. Fish & Shellfish Immunology 226, 686-694.
NLWRA, 2002. National Land and Water Resources Audit. Ögüt, H., 2001. Modeling of Fish Disease Dynamics: A New Approach to an Old Problem. Turkish Journal of Fisheries and Aquatic Sciences, 1 (2), 67-74.
Ortuno, J., Esteban, M.A., Meseguer, J. 2001. Effects of shortterm crowding stress on the gilthead sea bream Sparus aurata L. innate immune response. Fish & Shellfish Immunology, 11 (2) 187-197.
Person-Le Ruyet, J., Mahé, K., Le Bayon, N., Le Delliou, H., 2004. Effects of temperature on growth and metabolism in a Mediterranean population of European sea bass Dicentrarchus labrax. Aquaculture, 237 (1-4), 269-280.
Pham, T.H., Cheng, T.C., Wang, P.C., Chen, S.C., 2021. Protective efficacy of four heat-shock proteins as recombinant vaccines against photobacteriosis in Asian seabass (Lates calcarifer). Fish & Shellfish Immunology, 111, 179-188.
Popovic, T., Rakovac, N., Rakovac, C., Perovic, R., Perovic, S.I., 2007. Commercial phenotypic tests (API 20E) in diagnosis of fish bacteria: a review. Veterinární medicína, 52 (2), 49-53.
Pörtner, H.O., Peck, M.A., 2010. Climate change effects on fish and fisheries: towards a cause-and-effect understanding. Journal of Fish Biology, 77 (8), 1745-1779.
Sampaio, E., Rosa, R., 2019. Climate change, multiple stressors, and responses of marine biota, p. 264-275 In: Climate Action. Encyclopaedia of the UN Sustainable Development Goals, W. Leal Filho, A. Azul, L. Brandli, P. Özuyar, T. Wall (Eds). Springer, Cham.
Schrøder, M.B., Mikkelsen, H., Børdal, S., Gravningen, K., Lund, V., 2006. Early vaccination and protection of Atlantic cod (Gadus morhua. L. 1758) juveniles against classical vibriosis. Aquaculture, 254, 46–53.
Shetty, M., Maiti, B., Santhosh, K.S., Venugopal, M.N., Karunasagar, I., 2012. Betanodavirus of marine and freshwater fish: distribution. genomic organization. diagnosis and control measures. Indian Journal of Virology, 23, 114-123.
Spinos, E., 2019. Correlation of environmental parameters with the occurrence of diseases in the farmed sea bass Dicentrarchus labrax. L. 1758 and prevention of these diseases. Doctoral Thesis, Department of Marine Sciences, Aegean University. P 127-128 & 132.
Spinos, Ε., Kokkoris, G., Bakopoulos, V., 2017. Prevention of sea bass (Dicentrarchus labrax L. 1758) photobacteriosis and vibriosis. Long term efficacy study of intraperitoneally administered bivalent commercial vaccines. Aquaculture, 471, 172-184.
Spinos, E., Vavasis, Χ., Bakopoulos, V., 2013. First results of correlation of water temperature with clinical signs development of the encephalopathy-retinopathy virus in cultured sea bass in Western Greece. 15th Panhellenic Ichthyologists Conference. Aquatic Ecosystems: uses, effects and management.
Spinos, E., Ramfos, A., Lazaridou, E., Bakopoulos, V., 2012. Ecological study of Argostoli Gulf: Preliminary results of seabed mapping with emphasis on Posidonia oceanica seagrasses. 10th Panhellenic Symposium of Oceanography and Fishery.
Spinos, E., Gerakis, A., Palaiologos, A., Bakopoulos, V., 2018. Effects of temperature and salinity on outbreaks of bacterial diseases of farmed sea bass Dicentrarchus labrax (linnaeus, 1758). 3rd International Congress on Applied Ichthyology & Aquatic Environment, HydroMediT 2018. Volos November 2018, Greece.
Toffan, A., Buratin, A., Toson, M., Fortin, A., Pascoli, F. et al., 2017a. Viral encephalopathy and retinopathy – results from the first interlaboratory proficiency test. Bulletin of the European Association of Fish Pathologists, 37 (2), 70-76.
Toffan, A., Panzarin, V., 2020. Viral Encephalopathy and Retinopathy/ Viral Nervous Necrosis (VER/VNN). In: Zrncic S. (ed.). Diagnostic Manual for the main pathogens in European seabass and Gilthead seabream aquaculture. Zaragoza : CIHEAM, 2020. p. 45-60 (Options Méditerranés: Série B. Etudes et Recherches; n. 75).
Toffan, A., Pascoli, F., Pretto, T., Panzarin V., Abbadi M. et al., 2017b. Viral nervous necrosis in gilthead sea bream (Sparus aurata) caused by reassortant betanodavirus RGNNV/SJNNV: an emerging threat for Mediterranean aquaculture. National Library of Medicine (U.S.A). Scientific Report, 7 (1), 46755.
Varsamos, S., Flik, G., Pepin, J.F., Bonga, S.E.W., Breuil, G., 2006. Husbandry stress during early life stages affects the stress response and health status of juvenile sea bass Dicentrarchus labrax. Fish & Shellfish Immunology, 20 (1), 83-96.
Vryonis, P., 2013. Study of sweet and salt water mixing fields based on seasonal changes in physicochemical parameters. Postgraduate Specialization Diploma. Department of Geology, University of Patras.
Whipple, M.J., Rohovec, J.S., 1994. The effect of heat and low pH on selected viral and bacterial fish pathogens. Aquaculture, 123 (3-4), 179-189. Zar, H.J., 1999. Biostatistical Analysis. Department of Biological Sciences, Nothern Illinois University. p. 270- 271, 286-288.
Most read articles by the same author(s)