The dual impact of Ostreopsis cf. ovata on Mytilus galloprovincialis and Paracentrotus lividus: Toxin accumulation and pathological aspects
Published:
Jan 14, 2021
Keywords:
Ostreopsis Mytilus galloprovincialis Paracentrotus lividus Mussels sea urchins toxicity.
Abstract
Blooms of the toxic dinoflagellates Ostreopsis have become common along rocky shores of the Mediterranean Sea. In addition to health problems for beach-goers, Ostreopsis toxins may accumulate in benthic marine animals used for human consumption, which however at times have shown signals of stress and even mortality. In order to elucidate the actual relationships between Ostreopsis and benthic invertebrates, we exposed mussels Mytilus galloprovincialis and sea urchins Paracentrotus lividus from the Gulf of Naples to cultures and natural material of O. cf. ovata and assessed feeding and adverse effects on the animals, along with their acquired toxicity. Mussels exposed to O. cf. ovata for 24 hours filtered the microalgae at different rates, depending on both mussel size and microalgal density, and became weakly toxic in some cases. Under longer exposure most animals died and all survivors were toxic. Detoxification of a naturally toxic mussel populations from an area affected by O. cf. ovata blooms took more than two weeks. Sea urchins fed with the red alga Asparagopsis taxiformis epiphytised by O. cf. ovata did not show damages and became mildly toxic in some cases. However, the direct exposure of sea urchins to O. cf. ovata cultures caused the partial or total loss of the spines in a density-dependent way, with the death of the animals at the highest microalgal concentrations. Milder effects were registered with sonicated cultures or toxin extracts. Our results indicate that the balance between toxicity and animal health in these invertebrates depends on the mode and intensity of exposure to the toxic microalga, while the response varies between the two species but also within the same species. This scenario matches the variety of responses of benthic populations recorded in the natural environment in areas affected by O. cf. ovata blooms.
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SARDO, A., ROSSI, R., SOPRANO, V., CIMINIELLO, P., FATTORUSSO, E., CIRINO, P., & ZINGONE, A. (2021). The dual impact of Ostreopsis cf. ovata on Mytilus galloprovincialis and Paracentrotus lividus: Toxin accumulation and pathological aspects. Mediterranean Marine Science, 22(1), 59–72. https://doi.org/10.12681/mms.24160
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- Vol. 22 No. 1 (2021)
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- Research Article
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References
Abdennadher, M., Zouari, A.B., Sahnoun, W.F., Alverca, E., Penna, A. et al., 2017. Ostreopsis cf. ovata in the Gulf of Gabès (south-eastern Mediterranean Sea): morphological, molecular and ecological characterization. Harmful Algae, 63, 56-67.
Accoroni, S., Totti, C., 2016. The toxic benthic dinoflagellates of the genus Ostreopsis in temperate areas: a review. Advances in Oceanography and Limnology, 7 (1), 1-15.
Aligizaki. K., Katikou, P., Nikolaidis, G., Panou, A., 2008. First episode of shellfish contamination by palytoxin-like compounds from Ostreopsis species (Aegean Sea, Greece). Toxicon, 51 (3), 418-427.
Amzil, Z., Sibat, M., Chomerat, N., Grossel, H., Marco-Miralles, F. et al., 2012. Ovatoxin-a and palytoxin accumulation in seafood in relation to Ostreopsis cf. ovata blooms on the French Mediterranean coast. Marine Drugs, 10 (2), 477-496.
Andersen, R.A., Kawaky, M., 2005. Chapter 6: Traditional Microalgae Isolation Techniques. p. 83-100. In: Algal Culturing Techniques. Andersen, R.A. (Eds). Elsevier Academic Press, Hong Kong.
Argyle, P.A., Harwood, D.T., Rhodes, L.L., Champeau, O., Tremblay, L.A., 2016. Toxicity assessment of New Zealand and Pacific dinoflagellates Ostreopsis and Gambierdiscus (Dinophyceae) extracts using bioassays. New Zealand Journal of Marine and Freshwater Research, 50 (3), 444-456.
ARPAC, 2008. Il monitoraggio dell’Ostreopsis ovata lungo il litorale della Campania (giugno-agosto 2007), http://www. arpacampania.it/ pubblicazioni.asp.
Balcioğlu, E.B., Aksu, A., Balkis, N., Öztürk, B., 2017. Origin and distribution of Polycyclic Aromatic Hydrocarbons (PAHs) in Mediterranean mussels (Mytilus galloprovincialis Lamarck, 1819) of the Turkish Straits system. Polycyclic Aromatic Compounds, 40 (1), 50-60.
Blanco, J., Fernandez, M.L., Miguez, A., Moroño, A., 1999. Okadaic acid depuration in the mussel Mytilus galloprovincialis: one- and two-compartment models and the effect of environmental conditions. Marine Ecology Progress Series, 176, 153-163.
Blanco, J., 2019. Accumulation of Dinophysis toxins in bivalve molluscs. Toxins, 10 (11), 453.
Boudouresque, C., Verlaque, M., 2013. Paracentrotus lividus. p. 297-327. In: Developments in Aquaculture and Fisheries Science. Sea Urchins: Biology and Ecology. Lawrence J.M. (Ed). Elsevier, Amsterdam.
Bricelj, V.M., Lee, J.H., Cembella, A.D., Anderson, D.M., 1990. Uptake kinetics of paralytic shellfish toxins from the dinoflagellate Alexandrium fundyense in the mussel Mytilus edulis. Marine Ecology Progress Series, 63, 177-188.
Bricelj, V.M, Shumway, S.E., 1998. Paralytic shellfish toxins in bivalve molluscs: occurrence, transfer kinetics, and biotransformation. Reviews in Fisheries Science, 6(4), 315-383.
Briggs, L., Rhodes, L., Munday, R., Towers, N., 1998. Detection of palytoxin using a haemolysis neutralisation assay. In: Proceedings of the 10th New Zealand Marine Biotoxin Science Workshop, New Zealand Marine Biotoxin Management Board, Wellington.
Brissard, C., Herrenknecht, C., Séchet, V., Hervé, F., Pisapia, F. et al., 2014. Complex toxin profile of French Mediterranean Ostreopsis cf. ovata strains, seafood accumulation and ovatoxins prepurification. Marine Drugs, 12, 2851-2876.
Carella, F., Sardo, A., Mangoni, O., Di Cioccio, D., Urciuolo, G. et al., 2015. Quantitative histopathology of the Mediterranean mussel (Mytilus galloprovincialis L.) exposed to the harmful dinoflagellate Ostreopsis cf. ovata. Journal of Invertebrate Pathology, 127, 130-140.
Castellano, I., Migliaccio, O., Ferraro, G., Maffioli, E., Marasco, D. et al., 2018. Biotic and environmental stress induces nitration and changes in structure and function of the sea urchin major yolk protein toposome. Scientific Reports, 8:4610.
Chebib, H., Cembella, A.D., Anderson, P., 1993. Differential paralytic shellfish toxin accumulation and detoxification kinetics in transplanted populations of Mytilus edulis exposed to natural blooms of Alexandrium excavatum. pp. 383-388. In: Toxic phytoplankton blooms in the sea. Smayda T.J, Shimizu Y. (Eds). Elsevier, Amsterdam.
Ciminiello, P., Dell’Aversano, C., Dello Iacovo, E., Fattorusso, E., Forino, M. et al., 2010. Complex palytoxin-like profile of Ostreopsis ovata. Identification of four new ovatoxins by high-resolution liquid chromatography/mass spectrometry. Rapid Communications in Mass Spectrometry, 24, 2735- 2744.
Ciminiello, P., Dell’Aversano, C., Dello Iacovo, E., Fattorusso, E., Forino, M. et al., 2011. Palytoxin in seafood by liquid chromatography tandem mass spectrometry: investigation of extraction efficiency and matrix effect, Analytical and Bioanalytical Chemistry, 401(3), 1043-1050.
Ciminiello, P., Dell’Aversano, C., Fattorusso, E., Forino, M., Magno, G.S. et al., 2006. The Genoa 2005 outbreak. Determination of putative palytoxin in Mediterranean Ostreopsis ovata by a new liquid chromatography tandem mass spectrometry method. Analytical Chemistry, 78 (17), 6153- 6159.
David, H., Moita, M.T., Laza-Martinez, A., Silva, A.D., Mateus, M. et al., 2012. First bloom of Ostreopsis cf. ovata in the continental Portuguese coast. Harmful Algae News, 45, 12-13.
De Donno, A., Grassi, T., Bagordo, F., Idolo, A., Serio, F. et al., 2012. detection of viruses in coastal seawater using Mytilus galloprovincialis as an accumulation matrix. Food and Environmental Virology, 4, 81-88.
Durando, P., Ansaldi, F., Oreste, P., Moscatelli, P., Marensi, L. et al., 2007. Collaborative group for the Ligurian syndromic algal surveillance. Eurosurveillance, 12, E070607.
Faimali, M., Giussani, V., Piazza, V., Garaventa, F., Corrà, C., et al., 2012. Toxic effects of harmful benthic dinoflagellate Ostreopsis ovata on invertebrate and vertebrate marine organisms. Marine Environmental Research, 76, 97-107.
Ferreira, C.E.L., 2006. Sea urchins killed by toxic algae. Journal of Marine Biological Association Global Marine Environment, 3, 22–23.
Fukuyo, Y., 1981. Taxonomical study on benthic dinoflagellates collected in coral reefs. Bulletin of the Japanese Society of Scientific Fisheries, 47, 967-978.
Gallitelli, M., Ungaro, N., Addante, L.M., Procacci, V., Gentiloni Silver, N., et al., 2005. Respiratory illness as a reaction to tropical algal blooms occurring in a temperate climate. Journal of American Medical Association, 239 (21), 2599- 2600.
García-Altares, M., Tartaglione, L., Dell’Aversano, C., Carnicer, O., De La Iglesia, P et al., 2015. The novel ovatoxin-g and isobaric palytoxin (so far referred to as putative palytoxin) from Ostreopsis cf. ovata (NW Mediterranean Sea): structural insights by LC-high resolution MSn. Analytical and Bioanalytical Chemistry, 407, 1191-1204.
Gazeau, F., Alliouane, S., Bock, C., Bramanti, L., Correa, M.L. et al., 2014. Impact of ocean acidification and warming on the Mediterranean mussel (Mytilus galloprovincialis). Frontiers in Marine Science, 1, 62.
Giussani, V., Costa, E., Pecorino, D., Berdalet, E., De Giampaulis, G. et al., 2016. Effects of the harmful dinoflagellate Ostreopsis cf. ovata on different life cycle stages of the common moon jellyfish Aurelia sp. Harmful Algae, 57, 49-58.
Gladan, N.Ž., Arapov, J., Casabianca, S., Penna, A., Honsell, G. et al., 2019. Massive occurrence of the harmful benthic dinoflagellate Ostreopsis cf. ovata in the eastern Adriatic Sea. Toxins, 11, 300.
Gleibs S., Mebs, D., 1999. Distribution and sequestration of palytoxin in coral reef animals. Toxicon, 37 (11), 1521-1527.
Gorbi, S., Avio, G.C., Benedetti, M., Totti, C., Accoroni, S. et al., 2013. Effects of harmful dinoflagellate Ostreopsis cf. ovata exposure on immunological, histological and oxidative responses of mussels Mytilus galloprovincialis. Fish & Shellfish Immunology, 35 (3), 941-950.
Gorbi, S., Bocchetti, R., Binelli, A., Bacchiocchi, S., Orletti, R. et al., 2012. Biological effects of palytoxin-like compounds from Ostreopsis cf. ovata: a multibiomarkers approach with mussels Mytilus galloprovincialis. Chemosphere, 89 (5), 623-632.
Guéguen, M., Lassus, P., Laabir, M., Bardouil, M., Baron, R. et al., 2008. Gut passage times in two bivalve molluscs fed toxic microalgae: Alexandrium minutum, A. catenella and Pseudo-nitzschia calliantha. Aquatic Living Resources, 21, 21-29.
Guendouzi, Y., Soualili, D.L., Fowler, S.W., Boulahdid, M., 2020. Environmental and human health risk assessment of trace metals in the mussel ecosystem from the Southwestern Mediterranean. Marine Pollution Bullettin, 151, 110820.
Guerrini, F., Pezzolesi, L., Feller, A., Riccardi, M., Ciminiello, P. et al., 2010. Comparative growth and toxin profile of cultured Ostreopsis ovata from the Tyrrhenian and Adriatic Seas. Toxicon, 55 (2-3), 211-220.
Illoul, H., Hernandez, F. R., Vila, M., Adjas, N., Younes, A. A. et al., 2012. The genus Ostreopsis along the Algerian coastal waters (SW Mediterranean Sea) associated with a human respiratory intoxication episode. Cryptogamie Algologie, 33, 209-216.
Jauffrais, T., Marcaillou, C., Herrenknecht, C., Truquet, C., Séchet, V. et al., 2012. Azaspiracid accumulation, detoxification and biotransformation in blue mussels (Mytilus edulis) experimentally fed Azadinium spinosum. Toxicon, 60 (4), 582-595.
Keller, M.D., Selvin, R.C., Claus, W., Guillard, R.R.L., 1987. Media for the culture of oceanic ultraphytoplankton. Journal of Phycology, 23, 633-638.
Kwong, R.W.M., Wang, W.X, Lamb, P.K.S., Yu, P.K.N., 2006. The uptake, distribution and elimination of paralytic shellfish toxins in mussels and fish exposed to toxic dinoflagellates. Aquatic Toxicology, 80, 82-91.
Lamon, S., Consolati, S.G., Fois, F., Cambula, M.G., Pes, M. et al., 2019. Occurrence, seasonal distribution, and molecular characterization of Vibrio vulnificus, Vibrio cholerae, and Vibrio parahaemolyticus in shellfish (Mytilus galloprovincialis and Ruditapes decussatus) collected in Sardinia (Italy). Journal of Food Protection, 82 (11), 1851-1856.
Landsberg, J.H., 2002. The Effects of Harmful Algal Blooms on Aquatic Organisms. Reviews in Fisheries Science, 10 (2), 113-390.
Louzao, M.C., Espiña, B., Cagide, E., Ares, I.R., Alfonso, A. et al., 2010. Cytotoxic effect of palytoxin on mussel. Toxicon, 56 (5), 842-847.
Mafra Jr., L.L., Ribas, T., Pereira Alves, T., Proença, L.A.O., Schramm, M.A. et al., 2015. Differential okadaic acid accumulation and detoxification by oysters and mussels during natural and simulated Dinophysis blooms. Fisheries Science, 81,749-762.
Malagoli, D., Casarini, L., Ottaviani, E., 2008. Effects of the marine toxins okadaic acid and palytoxin on mussel phagocytosis. Fish & Shellfish Immunology, 24 (2), 180-186.
Mangialajo, L., Ganzin, N., Accoroni, S., Asnaghi, V., Blanfuné, A. et al., 2011. Trends in Ostreopsis proliferation along the Northern Mediterranean coasts. Toxicon, 57, 408- 420.
Migliaccio, O., Castellano, I., Di Cioccio, D., Tedeschi, G., Negri, A. et al., 2016. Subtle reproductive impairment through nitric oxide-mediated mechanisms in sea urchins from an area affected by harmful algal blooms. Scientific Reports, 6, 26086.
Moestrup, Ø., Akselmann-Cardella, R., Churro, C., Fraga, S., Hoppenrath, M. et al. (Eds) (2009 onwards). IOC-UNESCO Taxonomic Reference List of Harmful Micro Algae. Accessed at http:// www.marinespecies.org/hab on 2020- 03-16.
Nascimento, S.M., Monteiro, P.O., Alencar, A.G., Meneguelli, A.C., 2010. Epi-benthic dinoflagellates from the Rio de Janeiro coastline, Brazil. In: GEOHAB Open Science Meeting: HABs in Benthic Systems, Honolulu, Hawaii, USA, 21- 23 June, 2010, 13-14.
Nascimento, S.M., Monteiro, P.O., Ferreira, C.E.L., González- Rodriguez, E., 2008. Ostreopsis ovata blooms on Rio de Janeiro coast. Harmful Algal News, 37, 1-4.
Neves, R.A., Contins, M., Nascimento, S.M., 2018. Effects of the toxic benthic dinoflagellate Ostreopsis cf. ovata on fertilization and early development of the sea urchin Lytechinus variegatus. Marine Environmental Research, 135, 11-17.
Pagano, G., Thomas, P., Guida, M., Palumbo, A., Romano, G. et al., 2017. Sea urchin bioassays in toxicity testing: I. Inorganics, organics, complex mixtures and natural products. Expert Opinion on Environmental Biology, 6,1.
Pagliara, P., Caroppo, C., 2012. Toxicity assessment of Amphidinium carterae, Coolia cfr. monotis and Ostreopsis cfr. ovata (Dinophyta) isolated from the northern Ionian Sea (Mediterranean Sea). Toxicon, 60, 1203-1214.
Pearce, I., Marshall, J., Hallegraeff, G.H., 2001. Toxic epiphytic dinoflagellates from East Coast Tasmania. pp. 54-57. In: Harmful Algal Blooms, 2000. Hallegraeff, G., Blackburn, S.I., Bolch, C.J., Lewis, R.J. (Eds). Intergovernmental Oceanographic Commission of UNESCO, Hobart, Tasmania.
Popovic, N.T., Benussi Skukan, A., Džidara, P., Čož -Racovac, R., Strunjak-Perović, I. et al., 2010. Microbiological quality of marketed fresh and frozen seafood caught off the Adriatic coast of Croatia. Veterinarni Medicina, 55, (5), 233-241.
Privitera, D., Giussani, V., Isola, G., Faimali, M., Piazza, V. et al., 2012. Toxic effects of Ostreopsis ovata on larvae and juveniles of Paracentrotus lividus. Harmful Algae, 18, 16-23.
Reis Costa, P., Braga, A.C., Turner, A.D., 2018. Accumulation and elimination dynamics of the hydroxybenzoate saxitoxin analogues in mussels Mytilus galloprovincialis exposed to the toxic marine dinoflagellate Gymnodinium catenatum. Toxins, 10, 428.
Rhodes, L., Adamson, J., Suzuki, T., Briggs, L., Garthwaite, I., 2000. Toxic marine epiphytic dinoflagellates, Ostreopsis siamensis and Coolia monotis (Dinophyceae), in New Zealand. New Zealand Journal of Marine and Freshwater Research, 34, 371-383.
Rhodes, L., Towers, N., Briggs, L., Munday, R., Adamson, J., 2002. Uptake of palytoxin‐like compounds by shellfish fed Ostreopsis siamensis (Dinophyceae). New Zealand Journal of Marine and Freshwater Research, 36, 631-636.
Riobò, P., Paz, B., Franco, J.M., Vázquez, J.A., Murado, M.A. et al., 2008. Mouse bioassay for palytoxin. Specific symptoms and dose-response against dose-death time relationships. Food and Chemical Toxicology, 46, 2639-2647.
Rossi, R., Castellano, V., Scalco, E., Serpe, L., Zingone, A. et al., 2010. New palytoxin-like molecules in Mediterranean Ostreopsis cf. ovata (dinoflagellates) and in Palythoa tuberculosa detected by liquid chromatography-electrospray ionization time-of-flight mass spectrometry. Toxicon, 56, 1381-1387.
Ruocco, N., Bertocci, I., Munari, M., Musco, L., Caramiello, D. et al., 2020. Morphological and molecular responses of the sea urchin Paracentrotus lividus to highly contaminated marine sediments: the case study of Bagnoli-Coroglio brownfield (Mediterranean Sea). Marine Environmental Research, 154, 104865.
Sansoni, G., Borghini, B., Camici, G., Casotti, M., Righini, P. et al., 2003. Fioriture algali di Ostreopsis ovata (Gonyaulacales: Dinophyceae): un problema emergente. Biologia Ambientale, 17 (1), 17-23.
Santos, M., Oliveira, P.B., Moita, M.T., David, H., Caeiro, M.F. et al., 2019. Occurrence of Ostreopsis in two temperate coastal bays (SW Iberia): insights from the plankton. Harmful Algae, 86, 20-36.
Sato, S., Nishimura, T., Uehara, K., Sakanari, H., Tawong, W. et al., 2011. Phylogeography of Ostreopsis along West Pacific Coast, with special reference to a novel clade from Japan. PLoS ONE, 6 (12), e27983.
Scalco, E., Brunet, C., Marino, F., Rossi, R., Soprano, V. et al., 2012. Growth and toxicity responses of Mediterranean Ostreopsis cf. ovata to seasonal irradiance and temperature conditions. Harmful algae, 17, 25-34.
Shears, N.T., Ross, P.M., 2009. Blooms of benthic dinoflagellates of the genus Ostreopsis; an increasing and ecologically important phenomenon on temperate reefs in New Zealand and worldwide. Harmful Algae, 8 (6), 916-925.
Shears, N.T., Ross, P.M., 2010. Toxic cascades: multiple anthropogenic stressors have complex and unanticipated interactive effects on temperate reefs. Ecology Letters, 13, 1149-1159.
Simonini, R., Orlandi, M., Abbate, M., 2011. Is the toxic dinoflagellate Ostreopsis cf. ovata harmful to Mediterranean benthic invertebrates? Evidences from ecotoxicological tests with the polychaete Dinophilus gyrociliatus. Marine Environmental Research, 72, 230-233.
Sotka, E.E., McCarty, A., Monroe, E.A., Oakman, N., Van Dolah, F.M., 2009. Benthic herbivores are not deterred by brevetoxins produced by the red tide dinoflagellate Karenia brevis. Journal of Chemical Ecology, 35, 851-859.
Svensson, S., 2003. Depuration of okadaic acid (Diarrhetic Shellfish Toxin) in mussels, Mytilus edulis (Linnaeus), feeding on different quantities of nontoxic algae. Aquaculture, 218, (1-4), 277-291.
Tartaglione, L., Mazzeo, A., Dell’Aversano, C., Forino, M., Giussani, V. et al., 2016. Chemical, molecular, and eco-toxicological investigation of Ostreopsis sp. from Cyprus island: structural insights into four new ovatoxins by LCHRMS/ MS. Analytical and Bioanalytical Chemistry, 408 (3), 915-932.
Tibiriçá, C.E.J.A., Leite, I.P., Batista, T.V.V., Fernandes, L.F., Chomérat, N. et al., 2019. Ostreopsis cf. ovata bloom in Currais, Brazil: phylogeny, toxin profile and contamination of mussels and marine plastic litter. Toxins, 11, 446.
Tognetto, L., Bellato, S., Moro, L., Andreoli, C., 1995. Occurrence of Ostreopsis ovata (Dinophyceae) in the Tyrrhenian Sea during summer 1994. Botanica Marina, 38, 291-295.
Totti, C., Accoroni, S., Cerino, F., Cucchiari, E., Romagnoli, T., 2010. Ostreopsis ovata bloom along the Conero Riviera (northern Adriatic Sea): relationship with environmental condition substrata. Harmful Algae, 9, 233-239.
Tubaro, A., Durando, P., Del Favero, G., Ansaldi, F., Icardi, G. et al., 2011. Case definitions for human poisonings postulated to palytoxins exposure. Toxicon, 1, 57 (3), 478-95.
Turki, S., Harzallah, A., Harzallah, A., Sammari, C., 2006. Occurrence of harmful dinoflagellates in two different Tunisian ecosystems: the lake of Bizerte and the Gulf of Gabes. Cahiers De Biologie Marine, 47, 253-259.
Utermöhl, H., 1958. Zur ver vollkommung der quantitativen phytoplankton- methodik. Mitteilung Internationale Vereinigung Fuer Theoretische unde Amgewandte Limnologie, 9, 39.
Yasumoto, T., Oshima, Y., Yamaguchi, M., 1978. Occurrence of a new type of shellfish poisoning in the Tohoku district. Bulletin of the Japanese Society of Scientific Fisheries, 44 (11), 1249-1255.
Zhang, H.,1 Lu, S., Li, Y., Cen, J., Wang, H. et al., 2018. Morphology and molecular phylogeny of Ostreopsis cf. ovata and O. lenticularis (Dinophyceae) from Hainan Island, South China Sea. Phycological Research, 66 (1), 3-14.
Zingone, A., Escalera, L., Aligizaki, K., Fernández-Tejedor, M., Ismael, A. et al., 2021. Toxic marine microalgae and noxious blooms in the Mediterranean Sea: A contribution to the Global HAB Status Report. Harmful Algae, 101843.
Zingone, A., Siano, R., D’Alelio, D., Sarno, D., 2006. Potentially toxic and harmful microalgae from coastal waters of the Campania region (Tyrrhenian Sea, Mediterranean Sea). Harmful Algae, 5, 321-337.
