Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-06-08T22:28:06.291Z Has data issue: false hasContentIssue false
  • English
  • Français

Variation of parasite and fungi infection between farmed and wild mussels (Mytilus galloprovincialis Lamarck, 1819) from the Adriatic Sea

Published online by Cambridge University Press:  28 August 2018

Ines Kovačić ,
Emina Pustijanac ,
Andreja Ramšak ,
Dora Šebešćen  and
Sanja Lipić
Ines Kovačić*
Affiliation:
Faculty of Educational Sciences, Juraj Dobrila University of Pula, Zagrebačka 30, HR – 52100 Pula,Croatia Department of Natural and Health Sciences, Juraj Dobrila University of Pula, Zagrebačka 30, HR – 52100 Pula, Croatia
Emina Pustijanac
Affiliation:
Faculty of Educational Sciences, Juraj Dobrila University of Pula, Zagrebačka 30, HR – 52100 Pula,Croatia
Andreja Ramšak
Affiliation:
National Institute of Biology, Marine Biology Station Piran, Fornače 41, SLO – 6330 Piran, Slovenia
Dora Šebešćen
Affiliation:
Faculty of Educational Sciences, Juraj Dobrila University of Pula, Zagrebačka 30, HR – 52100 Pula,Croatia
Sanja Lipić
Affiliation:
Faculty of Educational Sciences, Juraj Dobrila University of Pula, Zagrebačka 30, HR – 52100 Pula,Croatia
*
Correspondence should be addressed to: Ines Kovačić, Faculty of Educational Sciences, Juraj Dobrila University of Pula, Zagrebačka 30, HR – 52100 Pula, Croatia email: ikovacic@unipu.hr
Get access Rights & Permissions [Opens in a new window]

Abstract

Investigation of parasites and diseases affecting molluscs of ecological and economic interest is critical for the management of native stocks and aquaculture. In recent years, much attention has been devoted to investigating the World Organisation for Animal Health listed infectious diseases, so that communities can be prepared to attend public health emergencies and avoid severe income losses. In this context, the health status of Mytilus galloprovincialis Lamarck, 1819 was analysed in two aquaculture sites (Strunjan Bay and Piran Bay, Slovenia), and in four natural mussel beds (Adriatic Croatia International Marinas Pula and Rovinj and St Catherine, Croatia; Marina Koper, Slovenia) along the coast of the northern Adriatic Sea. The mussels were sampled in February and April 2014, and processed for histological examination of several endosymbionts and pathogens that frequently occur in mytilid mussels. Endosymbionts and pathogens were not detected in farmed mussels. Prokaryotic inclusion bodies, the protozoan Nematopsis, Ancistrocoma-like ciliates, haplosporidian-like plasmodia, turbellarian Urastoma cyprinae, and basophilic inclusion bodies were observed in digestive gland cryosections of wild mussels from the coastal region of the northern Adriatic. Fungal spores of Psilocybe sp., Ulocladium sp. and Alternaria sp. were detected between the digestive tubules based on their morphology. Diagnostic PCR did not reveal infection with Marteilia refringens during the studied period, neither in wild nor farmed mussels. We confirmed the site effects on prevalence of infected mussels. Thus, we can conclude that wild areas are more exposed to endobionts and parasites than aquaculture sites.

Keywords

endobiontsfungiparasitesmusselMarteilia refringensMytilus galloprovincialisAdriatic Sea
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Special Issue 8: Special Section: European Marine Biology Symposium Papers 2018 , December 2018 , pp. 1871 - 1879
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aarab, N., Pampanin, D.M., Nævdal, A., Øysæd, K.B., Gastaldi, L. and Bechmann, R.K. (2008) Histopathology alterations and histochemistry measurements in mussel, Mytilus edulis collected offshore from an aluminium smelter industry (Norway). Marine Pollution Bulletin 57, 569–574.Google Scholar
Adlard, R.D., Chollet, B., Institut français de recherche pour l'exploitation de la mer, European Commission Directorate-General for Health and Consumer Protection and International Office of Epizootics (2003) Histology and anatomo-pathology of molluscs: a guide for diagnosticians. La Tremblade: Ifremer.Google Scholar
Aranguren, R. and Figueras, A. (2016) Moving from histopathology to molecular tools in the diagnosis of molluscs diseases of concern under EU legislation. Frontiers in Physiology 7, 538.Google Scholar
ARSO 2014 Common database on monitoring of water quality data. Ljubljana: Environmental Agency of the Republic of Slovenia.Google Scholar
Biango-Daniels, M.N. and Hodge, K.T. (2018) Sea salts as a potential source of food spoilage fungi. Food Microbiology, 69, 89–95.Google Scholar
Bignell, J.P., Dodge, M.J., Feist, S.W., Lyons, B., Martin, P.D., Taylor, N.G.H., Stone, D., Travalent, L. and Stentiford, G.D. (2008) Mussel histopathology: effects of season, disease and species. Aquatic Biology 2, 1–15.Google Scholar
Bignell, J.P., Stentiford, G.D., Taylor, N.G.H. and Lyons, B.P. (2011) Histopathology of mussels (Mytilus sp.) from the Tamar estuary, UK. Marine Environmental Research 72, 25–32.Google Scholar
Bihari, N., Mičić, M., Fafanđel, M., Hamer, B., Jakšić, Ž. and Batel, R. (2004) Seawater quality of Adriatic coast, Croatia, based on toxicity, genotoxicity and DNA integrity assay. Acta Adriatica 45, 75–81.Google Scholar
Boehs, G., Villalba, A., Ceuta, L.O. and Luz, J.R. (2010) Parasites of three commercially exploited bivalve mollusc species of the estuarine region of the Cachoeira river (Ilheus, Bahia, Brazil). Journal of Invertebrate Pathology 103, 43–47.Google Scholar
Borzykh, O.G. and Zvereva, L.V. (2015) Mycobiota of the bivalve mollusk Anadara broughtoni (Schrenck, 1867) from various parts of Peter the Great Bay, Sea of Japan. Russian Journal of Marine Biology 41, 321–323.Google Scholar
Bower, S.M., McGladdery, S.E. and Price, I.M. (1994) Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annual Review of Fish Diseases 4(Supplement C), 1–199.Google Scholar
Bratoš, A., Glamuzina, B. and Benović, A. (2004) Hrvatsko školjkarstvo – prednosti i ograničenja (Croatian shellfisheries aquaculture - advantages and disadvantages). Naše More 51, 59–62.Google Scholar
Bricelj, M. and Rejec Brancelj, I. (2009) Integrated coastal zone management: case study on the Slovenian Mediterranean=Celovito upravljanje obalnega obmocja. Varstvo narave 22, 47–62.Google Scholar
Burgos-Aceves, M.A. and Faggio, C. (2017) An approach to the study of the immunity functions of bivalve haemocytes: physiology and molecular aspects. Fish and Shellfish Immunology 67, 513–517.Google Scholar
Burgos-Aceves, M.A., Cohen, A., Smith, Y. and Faggio, C. (2018) A potential microRNA regulation of immune-related genes in invertebrate haemocytes. Science of the Total Environment 621, 302–307.Google Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. and Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Cable, J., Barber, I., Boag, B., Ellison, A.R., Morgan, E.R., Murray, K., Pascoe, E.L., Sait, S.M., Wilson, A.J. and Booth, M. (2017) Global change, parasite transmission and disease control: lessons from ecology. Philosophical Transactions Royal Society B 372, 20160088.Google Scholar
Caceres-Martinez, J., Vasquez-Yeomans, R. and Sluys, R. (1998) The turbellarian Urastoma cyprinae from edible mussels Mytilus galloprovincialis and Mytilus californianus in Baja California, NW Mexico. Journal of Invertebrate Pathology 72, 214–219.Google Scholar
Capillo, G., Silvestro, S., Sanfilippo, M., Fiorino, E., Giangrosso, G., Ferrantelli, V., Vazzana, I. and Faggio, C. (2018) Assessment of electrolytes and metals profile of the Faro Lake (Capo Peloro Lagoon, Sicily, Italy) and its impact on Mytilus galloprovincialis. Chemistry and Biodiversity 15, 1800044. doi 10.1002/cbdv.201800044.Google Scholar
Carnegie, R.B., Arzul, I. and Bushek, D. (2016) Managing marine mollusc diseases in the context of regional and international commerce: policy issues and emerging concerns. Philosophical Transactions of the Royal Society B: Biological Sciences 371, 20150215.Google Scholar
Ceuta, L.O. and Boehs, G. (2012) Parasites of the mangrove mussel Mytella guyanensis (Bivalvia: Mytilidae) in Camamu Bay, Bahia, Brazil. Brazilian Journal of Biology 72, 421–427.Google Scholar
Cova, A.W., Serafim Júnior, M., Boehs, G. and Souza, J.M.d. (2015) Parasites in the mangrove oyster Crassostrea rhizophorae cultivated in the estuary of the Graciosa River in Taperoá, Bahia. Revista Brasileira de Parasitologia Veterinária 24, 21–27.Google Scholar
Ein-Gil, N., Ilan, M., Carmeli, S., Smith, G.W., Pawlik, J.R. and Yarden, O. (2009) Presence of Aspergillus sydowii, a pathogen of gorgonian sea fans in the marine sponge Spongia obscura. ISME Journal 3, 752–755.Google Scholar
Faggio, C., Pagano, M., Alampi, R., Vazzana, I. and Felice, M.R. (2016) Cytotoxicity, haemolymphatic parameters, and oxidative stress following exposure to sub-lethal concentrations of Quaternium-15 in Mytilus galloprovincialis. Aquatic Toxicology 180, 258–265.Google Scholar
Faggio, C., Tsarpali, V. and Dailianis, S. (2018) Mussel digestive gland as a model for assessing xenobiotics: an overview. Science of the Total Environment 636, 220–229.Google Scholar
FAO (2015) National aquaculture sector overview. Rome: FAO.Google Scholar
Center for Marine Research (2014) Coastal Cities Pollution project 2. Final report. Center for Marine Research.Google Scholar
Francisco, C.J., Hermida, M.A. and Santos, M.J. (2010) Parasites and symbionts from Mytilus galloprovincialis (Lamark, 1819) (Bivalves: Mytilidae) of the Aveiro estuary Portugal. Journal of Parasitology 96, 200–205.Google Scholar
Gombač, M. (2010) Protozoan infestation dynamics and occurrence of neoplasias in digestive gland of Mediterranean mussels (Mytilus galloprovincialis) in Slovene Sea in correlation with sea temperature, salinity and oxygenation. PhD thesis. Ljubljana University, Ljubljana, Slovenia.Google Scholar
Gombač, M., Kušar, D., Ocepek, M., Pogačnik, M., Arzul, I., Couraleau, Y. and Jenčič, V. (2014) Marteiliosis in mussels: a rare disease? Journal of Fish Diseases 37, 805–814.Google Scholar
Gulka, G. and Chang, P.W. (1985) Pathogenicity and infectivity of a rickettsia-like organism in the sea scallop, Placopecten magellanicus. Journal of Fish Diseases 8, 309–318.Google Scholar
Hamer, B., Korlević, M., Durmiši, E., Nerlović, V. and Bierne, N. (2012) Nuclear marker Me 15-16 analyses of Mytilus galloprovincialis populations along the eastern Adriatic coast. Cahiers de Biologie Marine 53, 35.Google Scholar
Kanduč, T., Šlejkovec, Z., Falnoga, I., Mori, N., Budič, B., Kovačić, I., Pavičić-Hamer, D. and Hamer, B. (2018) Environmental status of the NE Adriatic Sea, Istria, Croatia: Insights from mussel Mytilus galloprovincialis condition indices, stable isotopes and metal(loid)s. Marine Pollution Bulletin 126, 525–534.Google Scholar
Khan, R.A. (1991) Influence of pollution on parasites of aquatic animals. Annales de Parasitologie Humaine et Comparee 66(Suppl 1), 49–51.Google Scholar
Kovačić, I. and Pustijanac, E. (2017) Parasites and endobiotic fungi in digestive gland cryosections of the mussel Mytilus galloprovincialis in the Northern Adriatic, Croatia. Oceanological and Hydrobiological Studies 46, 414–420.Google Scholar
Kovačić, I., Pavičić-Hamer, D., Pfannkuchen, M. and Usich, M. (2016) Mytilus galloprovincialis (Lamarck, 1819) as host of Mytilicola orientalis (Mori, 1935) in the northern Adriatic Sea: presence and effect. Aquaculture International 25, 211–221.Google Scholar
Kristan, U., Kanduč, T., Osterc, A., Šlejkovec, Z., Ramšak, A. and Stibilj, V. (2014) Assessment of pollution level using Mytilus galloprovincialis as a bioindicator species: the case of the Gulf of Trieste. Marine Pollution Bulletin 89, 455–463.Google Scholar
Le Roux, F., Lorenzo, G., Peyret, P., Audemard, C., Figueras, A., Vivarès, C., Gouy, M. and Berthe, F. (2001) Molecular evidence for the existence of two species of Marteilia in Europe. Journal of Eukaryotic Microbiology 48, 449–454.Google Scholar
Lynch, S.A., Morgan, E., Carlsson, J., Mackenzie, C., Wooton, E.C., Rowley, A.F., Malham, S. and Culloty, S.C. (2014) The health status of mussels, Mytilus spp., in Ireland and Wales with the molecular identification of a previously undescribed haplosporidian. Journal of Invertebrate Pathology 118, 59–65.Google Scholar
Matozzo, V., Pagano, M., Spinelli, A., Caicci, F. and Faggio, C. (2016) Pinna nobilis: a big bivalve with big haemocytes? Fish and Shellfish Immunology 55, 529–534.Google Scholar
Mladineo, I. (2008) Risk assessment of parasitic/symbiotic organisms of the commercially important mytilid Modiolus barbatus (Linnaeus, 1758). Aquaculture Research 39, 1705–1719.Google Scholar
Mladineo, I., Petrić, M., Hrabar, J., Bočina, I. and Peharda, M. (2012) Reaction of the mussel Mytilus galloprovincialis (Bivalvia) to Eugymnanthea inquilina (Cnidaria) and Urastoma cyprinae (Turbellaria) concurrent infestation. Journal of Invertebrate Pathology 110, 118–125.Google Scholar
Morley, N.J. (2010) Interactive effects of infectious diseases and pollution in aquatic molluscs. Aquatic Toxicology 96, 27–36.Google Scholar
Özer, A. and Güneydağ, S. (2015) Seasonality and host–parasite interrelationship of Mytilus galloprovincialis parasites in Turkish Black Sea coasts. Journal of the Marine Biological Association of the United Kingdom 95, 1591–1599.Google Scholar
Pagano, M., Capillo, G., Sanfilippo, M., Palato, S., Trischitta, F., Manganaro, A. and Faggio, C. (2016) Evaluation of functionality and biological responses of Mytilus galloprovincialis after exposure to Quaternium-15 (Methenamine 3-chloroallylochloride). Molecules 21, E144.Google Scholar
Pagano, M., Porcino, C., Briglia, M., Fiorino, E., Vazzana, M., Silvestro, S. and Faggio, C. (2017) The influence of exposure of cadmium chloride and zinc chloride on haemolymph and digestive gland cells from Mytilus galloprovincialis. International Journal of Environmental Research 11, 207–216.Google Scholar
Pavičić-Hamer, D., Kovačić, I., Koščica, L. and Hamer, B. (2016) Physiological indices of maricultured mussel Mytilus galloprovincialis Lamarck, 1819 in Istria, Croatia: seasonal and transplantation effect. Journal of the World Aquaculture Society 47, 768–778.Google Scholar
Queiroga, F.R., Vianna, R.T., Vieira, C.B., Farias, N.D. and Da Silva, P.M. (2015) Parasites infecting the cultured oyster Crassostrea gasar (Adanson, 1757) in Northeast Brazil. Parasitology 142, 756–766.Google Scholar
Ramšak, A., Ščančar, J. and Horvat, M. (2012) Evaluation of metallothioneins in blue mussels (Mytilus galloprovincialis) as a biomarker of mercury and cadmium exposure in the Slovenian waters (Gulf of Trieste): a long-term field study. Acta Adriatica 53, 71–86.Google Scholar
Rayyan, A., Damianidis, P., Antoniadou, C. and Chintiroglou, C.C. (2006) Protozoan parasites in cultured mussels Mytilus galloprovincialis in the Thermaikos Gulf (north Aegean Sea, Greece). Diseases of Aquatic Organism 70, 251–254.Google Scholar
Roginsky, V. and Lissi, E.A. (2005) Review of methods to determine chain-breaking antioxidant activity in food. Food Chemistry 92, 235–254.Google Scholar
Saffo, M. (1992) Coming to terms with a field: words and concepts in symbiosis. Symbiosis 14, 17–31.Google Scholar
Sallenave-Namont, C., Pouchus, Y.F., Robiou du Pont, T., Lassus, P. and Verbist, J.F. (2000) Toxigenic saprophytic fungi in marine shellfish farming areas. Mycopathologia 149, 21–25.Google Scholar
Santos, A., Hauser-Davis, R.A., Santos, M.J.S. and De Simone, S.G. (2017) Potentially toxic filamentous fungi associated to the economically important Nodipecten nodosus (Linnaeus, 1758) scallop farmed in southeastern Rio de Janeiro, Brazil. Marine Pollution Bulletin 115, 75–79.Google Scholar
Savorelli, F., Manfra, L., Croppo, M., Tornambè, A., Palazzi, D., Canepa, S., Trentini, P.L., Cicero, A.M. and Faggio, C. (2017) Fitness evaluation of Ruditapes philippinarum exposed to Ni. Biological Trace Element Research 177, 384–393.Google Scholar
Sehonova, P., Svobodova, Z., Dolezelova, P., Vosmerova, P. and Faggio, C. (2018) Effects of waterborne antidepressants on non-target animals living in the aquatic environment: a review. Science of the Total Environment 631–632, 789–794.Google Scholar
Svobodová, Z., Richard, L., Jana, M. and Blanka, V. (1993) Water quality and fish health. Rome: Food and Agriculture Organization of the United Nations.Google Scholar
Torre, A., Trischitta, F., Corsaro, C., Mallamace, D. and Faggio, C. (2013a) Digestive cells from Mytilus galloprovincialis show a partial regulatory volume decrease following acute hypotonic stress through mechanisms involving inorganic ions. Cell Biochemistry and Function 31, 489–495.Google Scholar
Torre, A., Trischitta, F. and Faggio, C. (2013b) Effect of CdCl2 on regulatory volume decrease (RVD) in Mytilus galloprovincialis digestive cells. Toxicology in Vitro, 27, 1260–1266.Google Scholar
Tsangaris, C., Moschino, V., Strogyloudi, E., Coatu, V., Ramšak, A., Abu, A., Rana Carvalho, S.F. S., Kosyan, A., Lazarou, Y., Hatzianestis, I., Oros, A. and Tiganus, D. (2016) Biochemical biomarker responses to pollution in selected sentinel organisms across the Eastern Mediterranean and the Black Sea. Environment Science and Pollution Research International 23, 1789–1804.Google Scholar
Tuntiwaranuruk, C., Chalermwat, K., Pongsakchat, V., Meepool, A., Upatham, E.S. and Kruatrachue, M. (2008) Infection of Nematopsis oocysts in different size classes of the farmed mussel Perna viridis in Thailand. Aquaculture 281, 12–16.Google Scholar
Vázquez, N. and Cremonte, F. (2017) Review of parasites and pathologies of the main bivalve species of commercial interest of Argentina and Uruguay, Southwestern Atlantic Coast. Archives of Parasitology 1, 112–123.Google Scholar
Zannella, C., Mosca, F., Mariani, F., Franci, G., Folliero, V., Galdiero, M., Tiscar, P.G. and Galdiero, M. (2017) Microbial diseases of bivalve mollusks: infections, immunology and antimicrobial defense. Marine Drugs 15, 182–218. doi: 10.3390/md15060182.Google Scholar
Zhang, Y., Mu, J., Feng, Y., Kang, Y., Zhang, J., Gu, P.J., Wang, Y., Ma, L.F. and Zhu, Y.H. (2009) Broad-spectrum antimicrobial epiphytic and endophytic fungi from marine organisms: isolation, bioassay and taxonomy. Marine Drugs 7, 97–112.Google Scholar
Zrnčić, S., Le Roux, F., Oraić, D., Sostarić, B. and Berthe, F.C. (2001) First record of Marteilia sp. in mussels Mytilus galloprovincialis in Croatia. Diseases of Aquatic Organism 44, 143–148.Google Scholar
Zvereva, L.V., Zvyagintsev, A.Y. and Ivin, V.V. (2012) Mycological study of ballast waters and sediments of commercial ships in Vladivostok port. Russian Journal of Biological Invasions 3, 188–201.Google Scholar