A new threat to Sardina pilchardus in the northwestern Mediterranean: Genetic validation of the presence of lethal parasites in pelagic eggs and ovaries
Published:
Apr 9, 2024
Keywords:
Sardina pilchardus Ichthyodinium chabelardi protistan parasite vertical transmission Catalan coast
Abstract
Over the past few decades, the fishing industry and species conservationists have grown increasingly concerned about the decrease in catches and poor health of European sardines (Sardina pilchardus), particularly in the northwestern Mediterranean region. The species is threatened by a number of factors, including parasite illnesses, rising seawater temperatures, and overfishing. Increasing seawater temperatures due to climate change might lead to the proliferation of protistan parasites, such as Ichthyodinium chabelardi. This parasite has been documented in the literature to cause 100% larval mortality in sardines, which may have detrimental effects on fish populations and the fishing industry. We confirmed the existence of I. chabelardi in pelagic eggs and the ovaries of European sardines from the Catalan coast (northwestern Mediterranean) by means of stereomicroscopic analysis and a genetic methodology for parasite identification. The incidence of this infection was 22.5% in ovarian tissue and 11.5% in eggs. In this study, we present new data on the vertical transmission of I. chabelardi from one generation to another in sardines captured in the Mediterranean region. Interpreting outbreaks of I. chabelardi, especially in sardine populations, requires further research into the transmission of infection and improving our understanding of protozoan parasites.
Article Details
- How to Cite
-
FRIGOLA-TEPE, X., PÉREZ-BIELSA, N., CABALLERO-HUERTAS, M., OLLÉ-VILANOVA, J., MUÑOZ, M., & VIÑAS, J. (2024). A new threat to Sardina pilchardus in the northwestern Mediterranean: Genetic validation of the presence of lethal parasites in pelagic eggs and ovaries. Mediterranean Marine Science, 25(1), 151–159. https://doi.org/10.12681/mms.35580
- Section
- Research Article
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
Downloads
Download data is not yet available.
References
Albo-Puigserver, M., Sánchez, S., Coll, M., Bernal, M., Sáez- Liante, R. et al., 2020. Year-round energy dynamics of sardine and anchovy in the north-western Mediterranean Sea. Marine Environmental Research, 159, 105021.
Albo-Puigserver, M., Pennino, M.G., Bellido, J.M., Colmenero, A.I., Giráldez, A. et al., 2021. Changes in life history traits of small pelagic fish in the western Mediterranean Sea. Frontiers in Marine Science, 8, 570354.
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.
Bernal, M., Stratoudakis, Y., Wood, S., Ibaibarriaga, L., Uriarte, A. et al., 2011. A revision of daily egg production estimation methods, with application to Atlanto-Iberian sardine. 1. Daily spawning synchronicity and estimates of egg mortality. ICES Journal of Marine Science, 68 (3), 519-527.
Brosset, P., Lloret, J., Muñoz, M., Fauvel, C., Van Beveren, E. et al., 2016. Body reserves mediate trade-offs between life-history traits: new insights from small pelagic fish reproduction. Royal Society Open Science, 3 (10), 160202.
Brown, L.L., Cox, W.T., Levine, R.P., 1997. Evidence that the causal agent of bacterial cold-water disease Flavobacterium psychrophilum is transmitted within salmonid eggs. Diseases of Aquatic Organisms, 29 (3), 213-218.
Caballero‐Huertas, M., Soto, M., Ribas, L., 2021. Reviewing Pseudoloma neurophilia infections in the popular zebrafish model. Reviews in Aquaculture, 13 (4), 1816-1827.
Caballero-Huertas, M., 2023. Variability in the health status and reproductive traits of European sardine stocks in the Mediterranean. Implications for fishery management. Ph.D. Thesis. Universitat de Girona, Spain, 293 pp.
Caballero-Huertas, M., Palomba, M., Frigola-Tepe, X., Muñoz, M., Mattiucci, S. et al., 2023. Ascaridoid parasites in European sardine throughout the annual cycle: Variability in parasitic load according to host stock features. International Journal for Parasitology: Parasites and Wildlife, 20, 1-11.
Carriço, D., Henriques, E., Meneses, I., Costa, J.L., Veríssimo, A. et al., 2022. Mortality of Sardine and Horse Mackerel Eggs by Parasitism, Impact on the Survival of Early Life Stages. Biology and Life Sciences Forum, 13, 46.
Chaves‐Pozo, E., Montero, J., Cuesta, A., Tafalla, C., 2010. Viral hemorrhagic septicemia and infectious pancreatic necrosis viruses replicate differently in rainbow trout gonad and induce different chemokine transcription profiles. Developmental and Comparative Immunology, 34 (6), 648-658.
Cury, P., Bakun, A., Crawford, R.J., Jarre, A., Quinones, R.A. et al., 2000. Small pelagics in upwelling systems: patterns of interaction and structural changes in “wasp-waist” ecosystems. ICES Journal of Marine Science, 57 (3), 603-618.
Cutarelli, A., Amoroso, M.G., De Roma, A., Girardi, S., Galiero, G. et al., 2014. Italian market fish species identification and commercial frauds revealing by DNA sequencing. Food Control, 37 (1), 46-50.
FAO, 2022. The State of World Fisheries and Aquaculture 2022. Towards Blue Transformation. https://doi.org/10.4060/ cc0461en (Accessed 22 March 2024).
Fensome, R.A., Gocht, H., Stover, L.E., Williams, G.L., 1993. The Eisenack Catalog of Fossil Dinoflagellates Vol. 2. p. 829-1461. P.E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, Germany.
Fernández-Corredor, E., Albo-Puigserver, M., Pennino, M.G., Bellido, J.M., Coll, M., 2021. Influence of environmental factors on different life stages of European anchovy (Engraulis encrasicolus) and European sardine (Sardina pilchardus) from the Mediterranean Sea: A literature review. Regional Studies in Marine Science, 41, 101606.
Frigola-Tepe, X., Caballero-Huertas, M., Viñas, J., Muñoz, M., 2022. Influence of thermal regimes on the relationship between parasitic load and body condition in European sardine along the Catalan coast. Fishes, 7 (6), 358.
Ganias, K., Somarakis, S., Machias, A., Theodorou, A., 2004. Pattern of oocyte development and batch fecundity in the Mediterranean sardine. Fisheries Research, 67 (1), 13-23.
Ganias, K., 2009. Linking sardine spawning dynamics to environmental variability. Estuarine, Coastal and Shelf Science, 84 (3), 402-408.
Garrido, S., Silva, A., Pastor, J., Dominguez, R., Silva, A. V. et al., 2015. Trophic ecology of pelagic fish species off the Iberian coast: diet overlap, cannibalism and intraguild predation. Marine Ecology Progress Series, 539, 271-285.
Gestal, C., Novoa, B., Posada, D., Figueras, A., Azevedo, C., 2006. Perkinsoide chabelardi n. gen., a protozoan parasite with an intermediate evolutionary position: possible cause of the decrease of sardine fisheries? Environmental Microbiology, 8 (6), 1105-1114.
Gleason, F.H., Nagarkar, M., Chambouvet, A., Guillou, L., 2019. A review of the characteristics of the dinoflagellate parasite Ichthyodinium chabelardi and its potential effect on fin fish populations. Marine and Freshwater Research, 70 (9), 1307-1316.
Hollande, A., Cachon, J., 1952. Un parasite des oeufs de sardine: l’Ichthyodinium chabelardi, nov. gen., nov. sp. Comptes Rendus de l’Academie des Sciences, 235, 976-977.
Hollande, A. Cachon, J., 1953. Morphologie et évolution d’un Péridinien parasite des oeufs de sardine (Ichthyodinium chabelardi). Station Aquatique Pêches Ceutaglione, 4, 321-331.
Ishimaru, K., Iida, N., Okada, T., Miyashita, S., 2012. Ichthyodinium infection in the embryos and yolk sac larvae of Pacific bluefin tuna Thunnus orientalis. Fish Pathology, 47 (4), 143-146.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M. et al., 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647-1649.
Keskin, E., Atar, H.H., 2012. Genetic structuring of European anchovy (Engraulis encrasicolus) populations through mitochondrial DNA sequences. Mitochondrial DNA, 23 (2), 62-69.
Keskin, E., Atar, H.H., 2013. DNA barcoding commercially important fish species of Turkey. Molecular Ecology Resources, 13 (5), 788-797.
Kocan, R.M., Hershberger, P.K., Elder, N.E., 2001. Survival of the North American strain of viral hemorrhagic septicemia virus (VHSV) in filtered seawater and seawater containing ovarian fluid, crude oil and serum‐enriched culture medium. Diseases of Aquatic Organisms, 44 (1), 75-78.
Marinaro, J.Y., 1971. Contribution à l’étude des oefus et larves pelàgiques de poissons Mediterraneans. V. Oeus pelàgiques de la Baie d’Alger. Pelagos, 3, 1-118.
Meneses, I., Vendrell, C., Stratoudakis, Y., 2003. Mackerel (Scomber scombrus) eggs parasitized by Ichthyodinium chabelardi in the north-east Atlantic: an overlooked source of mortality. Journal of Plankton Research, 25 (9), 1177-1181.
Míguez, B., Combarro, M.P., 2003. Bacteria associated with sardine (Sardina pilchardus) eggs in a natural environment (Ría de Vigo, Galicia, northwestern Spain). FEMS Microbiology Ecology, 44 (3), 329-334.
Mori, K., Yamamoto, K., Teruya, K., Shiozawa, S., Yoseda, K. et al., 2007. Endoparasitic dinoflagellate of the genus Ichthyodinium infectin fertilized eggs and hatched larvae observed in the seed production of leopard coral grouper Plectropomus leopardus. Fish Pathology, 42, 49-57.
Pedersen, B.H., 1993. Embryos and yolk-sac larvae of turbot Scophthalmus maximus are infested with an endoparasite from the gastrula stage onwards. Diseases of Aquatic Organisms, 17, 57-57.
Pedersen, B.H., Buchmann, K., Køie, M., 1993. Baltic larval cod Gadus morhua are infested with a protistan endoparasite in the yolk sac. Diseases of Aquatic Organisms, 16 (1), 29-33.
Pedersen, B. H., Køie, M., 1994. A protistan endoparasite in embryos and yolk-sac larvae of cod Gadus morhua and turbot Scophthalmus maximus. Diseases of Aquatic Organisms, 19, 39-46.
Pennino, M.G., Bachiller, E., Lloret-Lloret, E., Albo-Puigserver, M., Esteban, A. et al., 2020. Ingestion of microplastics and occurrence of parasite association in Mediterranean anchovy and sardine. Marine Pollution Bulletin, 158, 111399.
Ramírez, F., Coll, M., Navarro, J., Bustamante, J., Green, A.J., 2018. Spatial congruence between multiple stressors in the Mediterranean Sea may reduce its resilience to climate impacts. Scientific reports, 8 (1), 1-8.
Ramírez, F., Pennino, M.G., Albo-Puigserver, M., Steenbeek, J. Bellido, J.M. et al., 2021. SOS small pelagics: A safe operating space for small pelagic fish in the western Mediterranean Sea. Science of the Total Environment, 756, 144002.
Rensel, J.E., Whyte, J.N.C., 2003. Finfish mariculture and harmful algal blooms. Manual on Harmful Marine Microalgae. Monographs on Oceanic Methodology, 11, 693-722.
Rodriguez, J.M., Alemany, F., Garcia, A., 2017. A guide to the eggs and larvae of 100 common Western Mediterranean Sea bony fish species. Food and Agriculture Organization of the United Nations, 256 pp.
Ruppert, K.M., Kline, R.J., Rahman, M.S., 2019. Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: A systematic review in methods, monitoring, and applications of global eDNA. Global Ecology and Conservation, 17, e00547.
Sanders, J.L., Watral, V., Clarkson, K., Kent, M.L., 2013. Verification of intraovum transmission of a microsporidium of vertebrates: Pseudoloma neurophilia infecting the zebrafish, Danio rerio. PLoS One, 8, e76064.
Skovgaard, A., Meneses, I., Angélico, M.M., 2009. Identifying the lethal fish egg parasite Ichthyodinium chabelardi as a member of Marine Alveolate Group I. Environmental Microbiology, 11 (8), 2030-2041.
Skovgaard, A., Meyer, S., Overton, J. L., Støttrup, J., Buchmann, K., 2010. Ribosomal RNA gene sequences confirm that protistan endoparasite of larval cod Gadus morhua is Ichthyodinium sp. Diseases of aquatic organisms, 88 (2), 161-167.
Sørensen, S.R., Tomkiewicz, J., Skovgaard, A., 2014. Ichthyodinium identified in the eggs of European eel (Anguilla anguilla) spawned in captivity. Aquaculture, 426, 197-203.
Stratoudakis, Y., Barbosa, A., Meneses, I., 2000. Infection of sardine eggs by the protistan endoparasite Ichthyodinium chabelardi off Portugal. Journal of Fish Biology, 57 (2), 476-482.
Timi, J.T., Poulin, R. 2020. Why ignoring parasites in fish ecology is a mistake. International Journal for Parasitology, 50 (10-11), 755-761.
Van Beveren, E., Bonhommeau, S., Fromentin, J.M., Bigot, J.L., Bourdeix, J.-H. et al., 2014. Rapid changes in growth, condition, size and age of small pelagic fish in the Mediterranean. Marine biology, 161 (8), 1809-1822.
Yamkasem, J., Tattiyapong, P., Kamlangdee, A., Surachetpong, W., 2019. Evidence of potential vertical transmission of tilapia lake virus. Journal of Fish Diseases, 42 (9), 1293-1300.
Yuasa, K., Kamaishi, T., Mori, K.I., Hutapea, J.H., Permana, G.N. et al., 2007. Infection by a protozoan endoparasite of the genus Ichthyodinium in embryos and yolk-sac larvae of yellowfin tuna Thunnus albacares. Fish Pathology, 42 (1), 59-66.
