Dusky grouper massive die-off in a Mediterranean marine reserve


DIEGO K. KERSTING
https://orcid.org/0000-0002-2049-7849
CELIA GARCÍA-QUINTANILLA
NAGORE QUINTANO
https://orcid.org/0000-0002-0158-0268
ITZIAR ESTENSORO
https://orcid.org/0000-0002-6218-2191
MARÍA DEL MAR ORTEGA-VILLAIZAN
https://orcid.org/0000-0003-2065-0601
Resumen

The dusky grouper Epinephelus marginatus (Lowe, 1834) is a key predator in shallow Mediterranean rocky habitats. Due to fishing pressure and slow population dynamics, dusky grouper populations are declining across their distribution range. Here we document a massive die-off of E. marginatus in the Columbretes Islands Marine Reserve (NW Mediterranean Sea) during the summer and early autumn of 2023. The mortality event was triggered by a Betanodavirus infection. Genetic characterization of isolates from the affected fish confirmed that they belong to the RGNNV genotype. Our findings indicate that such disease outbreaks can be particularly severe in areas with dense dusky grouper populations, potentially undermining the historical conservation effectiveness of marine protected areas. Although our results do not determine whether the infection originated from wild or farmed fish, it is essential to implement monitoring and early detection systems for Betanodavirus infections in both wild and farmed fish to prevent cross-infections.

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Astruch, P., Boudouresque, C.F., Rouanet, É., Diréach, L.L., Bonhomme, P. et al., 2018. A quantitative and functional assessment of fish assemblages of the Port-Cros Archipelago (Port-Cros National Park, north-western Mediterranean Sea). Scientific Reports of the Port-Cros National Park, 32, 17-82.
Bandín, I., Souto, S., 2020. Betanodavirus and VER disease: A 30-year research review. Pathogens, 9 (2), 106.
Berzak, R., Scheinin, A., Davidovich, N., Regev, Y., Diga, R. et al., 2019. Prevalence of nervous necrosis virus (NNV) and Streptococcus species in wild marine fish and crustaceans from the Levantine Basin, Mediterranean Sea. Diseases of Aquatic Organisms, 133 (1), 7-17.
Boukedjouta, R., Pretto, T., Abbadi, M., Biasini, L., Toffan, A. et al., 2020. Viral encephalopathy and retinopathy is endemic in wild groupers (genus Epinephelus spp.) of the Algerian coast. Journal of Fish Diseases, 43 (7), 801-812.
Bovo, G., Gustinelli, A., Quaglio, F., Gobbo, F., Panzarin, V. et al., 2011. Viral encephalopathy and retinopathy outbreak in freshwater fish farmed in Italy. Diseases of Aquatic Organisms, 96 (1), 45-54.
Breuil, G., Bonami, J. R., Pepin, J. F., Pichot, Y., 1991. Viral infection (picorna-like virus) associated with mass mortalities in hatchery-reared sea-bass (Dicentrarchus labrax) larvae and juveniles. Aquaculture, 97 (2), 109-116.
Chérif, N., Thiéry, R., Castric, J., Biacchesi, S., Brémont, M. et al., 2009. Viral encephalopathy and retinopathy of Dicentrarchus labrax and Sparus aurata farmed in Tunisia. Veterinary Research Communications, 33 (4), 345-353.
Ciulli, S., Galletti, E., Grodzki, M., Alessi, A., Battilani, M. et al., 2007. Isolation and genetic characterization of Betanodavirus from wild marine fish from the Adriatic sea. Veterinary Research Communications, 31, 221-224.
Coll, J., Linde, M., García-Rubies, A., Riera, F., Grau, A.M., 2004. Spear fishing in the Balearic Islands (west central Mediterranean): Species affected and catch evolution during the period 1975-2001. Fisheries Research, 70 (1), 97-111.
Condini, M.V., García-Charton, J.A., García, A.M., 2018. A review of the biology, ecology, behavior and conservation status of the dusky grouper, Epinephelus marginatus (Lowe 1834). Reviews in Fish Biology and Fisheries, 28 (2), 301-330.
Costa, Z.J., Thompson, K.D., 2016. Understanding the interaction between Betanodavirus and its host for the development of prophylactic measures for viral encephalopathy and retinopathy. Fish & Shellfish Immunology, 53, 35-49.
Doan, Q.K., Vandeputte, M., Chatain, B., Morin, T., Allal, F., 2017. Viral encephalopathy and retinopathy in aquaculture: a review. Journal of Fish Diseases, 40 (5), 717-742.
Estes, J.A., Terborgh, J., Brashares, J.S., Power, M.E., Berger, J. et al., 2011. Trophic downgrading of planet earth. Science, 333 (6040), 301-306.
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, 13-24.
García-Rubies, A., Hereu, B., Zabala, M., 2013. Long-Term Recovery Patterns and Limited Spillover of Large Predatory Fish in a Mediterranean MPA. PLoS One, 8 (9), e73922.
Grane-Feliu, X., Bennett, S., Hereu, B., Aspillaga, E., Santana- Garcon, J., 2019. Comparison of diver operated stereo- video and visual census to assess targeted fish species in Mediterranean marine protected areas. Journal of Experimental Marine Biology and Ecology, 520, 151205.
Guidetti, P., Baiata, P., Ballesteros, E., Franco, A.D., Hereu, B. et al., 2014. Large-Scale Assessment of Mediterranean Marine Protected Areas Effects on Fish Assemblages. PLoS One, 9 (4), e91841.
Hackradt, C.W., García-Charton, J.A., Harmelin-Vivien, M., Pérez-Ruzafa, Á., Le Diréach, L. et al., 2014. Response of Rocky Reef Top Predators (Serranidae: Epinephelinae) in and Around Marine Protected Areas in the Western Mediterranean Sea. PLoS One, 9 (6), e98206.
Haddad-Boubaker, S., Boughdir, W., Sghaier, S., Souissi, J.B., Megdich, A. et al., 2014. Outbreak of Viral Nervous Necrosis in Endangered Fish species Epinephelus costae and E. marginatus in Northern Tunisian Coasts. Fish Pathology, 49 (2), 53-56.
Kara, H.M., Chaoui, L., Derbal, F., Zaidi, R., de Boisséson, C. et al., 2014. Betanodavirus‐associated mortalities of adult wild groupers E pinephelus marginatus (Lowe) and Epinephelus costae (Steindachner) in Algeria. Journal of Fish Diseases, 37 (3), 273-278.
Kersting, D.K., Bensoussan, N., Linares, C., 2013. Long- Term Responses of the Endemic Reef-Builder Cladocora caespitosa to Mediterranean Warming. PLoS One, 8 (8), e70820.
Lampert, Y., Berzak, R., Davidovich, N., Diamant, A., Stern, N. et al., 2020. Indigenous versus Lessepsian Hosts: Nervous Necrosis Virus (NNV) in Eastern Mediterranean Sea Fish. Viruses, 12 (4), 430.
Lloret, J., Riera, V., 2008. Evolution of a Mediterranean Coastal Zone: Human Impacts on the Marine Environment of Cape Creus. Environmental Management, 42 (6), 977-988.
Lloret, J., Zaragoza, N., Caballero, D., Font, T., Casadevall, M. et al., 2008. Spearfishing pressure on fish communities in rocky coastal habitats in a Mediterranean marine protected area. Fisheries Research, 94 (1), 84-91.
Louisy, P., 2022. Guide d’identification des poissons marins: Europe et Méditerranée. Ulmer, Paris, 512 pp.
Marino, G., Azzurro, E., 2001. Nodavirus in dusky grouper Epinephelus marginatus, (Lowe 1834) of the Natural Marine Reserve of Ustica, South Thyrrenian sea. Biologia Marina Mediterranea, 8, 837-841.
Munday, B.L., Kwang, J., Moody, N., 2002. Betanodavirus infections of teleost fish: A review. Journal of Fish Diseases, 25 (3), 127-142.
Munday, B.L., Langdon, J.S., Hyatt, A., Humphrey, J.D., 1992. Mass mortality associated with a viral-induced vacuolating encephalopathy and retinopathy of larval and juvenile barramundi, Lates calcarifer Bloch. Aquaculture, 103 (3), 197-211.
Myers, R.A., Baum, J.K., Shepherd, T.D., Powers, S.P., Peterson, C.H., 2007. Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science, 315(5820), 1846-1850.
OIE - World Organisation for Animal Health, 2016. Manual of diagnostic tests for aquatic animals. OIE, Paris, 589pp.
OIE - World Organisation for Animal Health, 2019. Manual of diagnostic tests for aquatic animals. OIE, Paris, 550pp.
Panzarin, V., Fusaro, A., Monne, I., Cappellozza, E., Patarnello, P. et al., 2012. Molecular epidemiology and evolutionary dynamics of betanodavirus in southern Europe. Infection, Genetics and Evolution, 12 (1), 63-70.
Pollard, D.A., Afonso, P., Bertoncini, A.A., Fennessy, S., Francour, P. et al., 2018. Epinephelus marginatus. The IUCN Red List of Threatened Species 2018: E.T7859A100467602. https://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS. T7859A100467602.en. Accessed 21 May 2024.
R Core Team, 2024. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org
Reñones, O., Polunin, N.V.C., Goni, R., 2002. Size related dietary shifts of Epinephelus marginatus in a western Mediterranean littoral ecosystem: An isotope and stomach content analysis. Journal of Fish Biology, 61 (1), 122-137.
Reñones, O., Piñeiro, C., Mas, X., Goñi, R., 2007. Age and growth of the dusky grouper Epinephelus marginatus (Lowe 1834) in an exploited population of the western Mediterranean Sea. Journal of Fish Biology, 71 (2), 346-362.
Sano, M., Nakai, T., Fijan, N., 2011. Viral diseases and agents of warmwater fish. p 166-244. In: Fish Diseases and Disorders. Volume 3: Viral, Bacterial and Fungal Infections.
Woo, P.T.K., Bruno, D.W. (Eds). CABI, London. Tamura, K., Stecher, G., Kumar, S., 2021. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38 (7), 3022-3027.
Ucko, M., Colorni, A., Diamant, A., 2004. Nodavirus infections in Israeli mariculture. Journal of Fish Diseases, 27 (8), 459-469.
Valencia, J., Grau, A., Pretto, T., Pons, J., Jurado-Rivera, J. et al., 2019. Viral encephalopathy and retinopathy (VER) disease in Epinephelus marginatus from the Balearic Islands marine protected areas. Diseases of Aquatic Organisms, 135 (1), 49-58.
Valls, A., Gascuel, D., Guénette, S., Francour, P., 2012. Modeling trophic interactions to assess the effects of a marine protected area: Case study in the NW Mediterranean Sea. Marine Ecology Progress Series, 456, 201-214.
Vendramin, N., Patarnello, P., Toffan, A., Panzarin, V., Cappellozza, E. et al., 2013. Viral Encephalopathy and Retinopathy in groupers (Epinephelus spp.) in southern Italy: A threat for wild endangered species? BMC Veterinary Research, 9 (1), 20.
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