Influence of seasonality on the presence of okadaic acid associated with Dinophysis species: A four-year study in Sardinia (Italy)
https://doi.org/10.4081/ijfs.2021.8947
Submitted: 5 March 2020
Accepted: 24 June 2020
Published: 25 March 2021
Accepted: 24 June 2020
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
In Sardinia (Italy), bivalve molluscs production plays an important role in the trade balance. Diarrhoetic shellfish poisoning (DSP), an intoxication caused by the ingestion of bivalve molluscs that have accumulated high levels of Okadaic acid (OA), may represent a serious risk for the public health and a remarkable economic loss for the producers. Aim of this work was to improve knowledge about the repeatability of OA accumulation phenomena in various seasons trying to understand whether or not there was a trend. Also, the interaction between toxic algae and OA accumulation was examined. In this study, data of lipophilic toxins, water temperature and abundance of DSP-producing microalgal species were collected in a four-year period (2015–2018) in coastal production areas of Sardinia. Several episodes of OA positive values (>160 eq μgAO/Kg pe, Reg 853/04) were recorded during the study period in different production areas of Sardinia and in different seasons. A seasonal repeatability of OA accumulation in molluscs was observed in some production areas; moreover, different temporal gaps between the presence of toxic algae and OA accumulation were reported. Toxicity was observed almost exclusively in Mytilus galloprovincialis Lamark (99%), being this matrix the most abundant species bred in Sardinia.
Anderson DM, Gilbert PM, Burkholder JM, 2002. Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:562-84.
Allen JJ, Anderson D, Burford M., Dyhrman S, Flynn K, Gilbert PM, Graneli E, Heil C, Sellner K, Smayda T, Zhou M, 2006. Global Ecology and Oceanography of Harmful Algal Blooms, Harmful Algal Blooms in Eutrophic Systems. GEHOAB Report 410C and SCOR. GEOHAB, Paris/Baltimore, MD. USA, pp 1-74.
Alves-de-Souza C, Varela D, Contreras C, de La Iglesia P, Fernández P, Hipp B, Lagos N, 2014. Seasonal variability of Dinophysis spp. and Protoceratium reticulatum associated to lipophilic shellfish toxins in a strongly stratified Chilean fjord. Deep-Sea Res Pt II 101:152-62.
Anderson DM, Alpemann TJ., Cembella AD, Collos Y, Masseret E, Montreson M, 2012. The globally distributed genus Alexandrium: multificated roles in marine ecosystems and impacts on human health. Harmful Algae 14:10-35.
Aune T, Espenes A, Aasen JAB, Quilliam MA, Hess P, Larsen S, 2012. Study of possible combined toxic effects of azaspiracid-1 and okadaic acid in mice via the oral route. Toxicon 60:895-906.
Bauder AG, Cembella AD, Quilliam MA, 1996. Dynamics of diarrheic shellfish toxins from the dinoflagellate, Prorocentrum Lima, in the bay scallop, Argopecten irraddians. In: Yasumoto T , Oshima Y, Fukuyo Y, eds. Harmful and Toxic Phytoplankton Blooms IOC/UNESCO, Paris, pp 433-81.
Basti L, Uchida H, Matsushima R, Watanabe N, Suzuki T, Yamatogi T, Nagai S, 2015. Influence of temperature on growth and production of pectenotoxin-2 by a monoclonal culture of Dinophysis caudata. Mar Drugs 13:7124-73.
Bazzoni AM, Mudadu AG, Lorenzoni G, Soro B, Bardino N, Arras I, Sanna G, Vodret B, Bazzardi R, Marongiu, Virgilio S, 2018. Detection of Dinophysis species and associated okadaic acid in farmed shellfish: a two-year study from the western Mediterranean area. J Vet Res 62:137-44.
Boni L, Milandri A, Poletti R, Pompei M, 1993. DSP cases along the coastal of Emila Romagna (Northwestern Adriatic sea). In: Smayda TJ, ed. Toxic Phytoplancton Blooms in the Sea. Elsevier, Amsterdam, pp 475-81.
Chavez FP, Messiè M, Pennington JT, 2011. Marine primary production in relation to climate variability and change. Annu Rev Mar Sci 3:222-60.
Edwards M., Johns DG, Leterme SC, Svendsen E, Richardson AJ, 2006. Regional climate change and harmful algal blooms in the northeast Atlantic. Limnol Oceanogr 51:820-29.
France J, Mozetič P, 2006. Ecological characterization of toxic phytoplankton species (Dinophysis spp., Dinophyceae) in Slovenian mariculture areas (Gulf of Trieste, Adriatic Sea) and the implications for monitoring. Mar Pollut Bull 52:1504-16.
Fu FX, Tatters AO, Hutchins DA, 2012. Global change and the future of harmful algal blooms in the ocean. Mar Ecol Progr Ser 470:207-233.
Hallengraeff GM, 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99.
Hallengraeff GM, 2003. Harmful Algal Blooms: a Global Overview, Manual on Harmful Marine Microalgae. UNESCO Publishing, Paris: 25-50.
Hegaret H, Shumway SE, Wilkfors GH, Pate S, Burkholder JM, 2008. Potential transfer of harmful algae through relocation of bivalve molluscs. Mar Ecol Progr Ser 361:169-81.
Heisler J, Gilbert PM., Burkholder JM, Anderson DM, Cochlan W, Dennison WC, Dortch Q, Gobler CJ, Heil CA, Humphries E, Lewitus A, Magnien R, Marshall HG, Sellner K, Stockwell DA, Suddleson M, 2008. Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8:3-13.
Lee JS, Igarashi T, Fraga S, Dahl E, Howgaard P, Yasumoto T, 1989. Determination of diarrhetic shellfish toxins in various dinoflagellate species. J. Appl Phycol 1:147-52.
Moore SK, Trainer VL, Mantua NJ, Parker MS, Laws EA, Backer LC, Fleming LE, 2008. Impact of climate variability and future climate change on harmful algal blooms and human health. Environ Health. doi:10.1186/1476-069X-7-S2-S4
Naustvoll LJ, Gustad E, Dahl E, 2013. Monitoring of Dinophysis species and diarrhetic shellfish toxins in Flødevigen Bay, Norway: inter-annual variability over a 25-year time series. Food Addit Contam 29:1605-15.
Nincevic-Gladan Z, Skejic S, Buzancic M, Marovic I, Arapov J, Ujevic I, Bojanic N, Grbec B, Kuspilic G, Vidjak O, 2008. Seasonal variability in Dinophysis spp. abundances and diarrhetic shellfish poisoning outbreaks along the eastern Adriatic coast. Bot Mar 51:449-63.
Padedda BM, Pulina S, Magni P, Sechi N, Lugliè A, 2012. Phytoplankton dynamics in relation to environmental changes in a phytoplankton-dominated Mediterranean lagoon (Cabras Lagoon, Italy). AIOL J 3:147-69.
Pitcher GC, Calder D, 2000. Harmful algal blooms of the southern Benguela Current: a review and appraisal of monitoring from 1989 to 1997. S Afr J Mar Sci 22:257-71.
Philips EJ, Badylak S, Christman M, Wolny J, Brame J, Garland J, Hall L, Hart J, Landsberg J. Lasi M, Lockwood J, Paperno R, Scheidt D, Staples A, Steindinger K, 2011. Scales of temporal and spatial variability in the distribution of harmful algae species in Indian River Lagoon, Florida, USA. Harmful Algae 10:277-90.
Pizzarro G, Paz B, Gonzales-Gil S, Franco JM, Roguera B, 2009. Seasonal variability of lipophilic toxins during a Dinophysis acuta bloom in Wester Iberia. Differences between picked cells and plankton concentrates. Harmful Algae 8:926-37.
Roguera B, Velo-Suarez R, Park M, 2012. Harmful Dinophysis species: a review. Harmful Algae 14:87-106.
Roguera R, Riobo P, Rodriguez F, Diaz PA, Pizzarro G, Paz B, Franco JM, Blanco J, 2014. Dinophysis toxins: causative organisms, distribution and fate in shellfish. Mar Drugs 12:394-461.
Tibirica C, Fernandes LF, Mafra Junior LL, 2015. Seasonal and spatial patterns of toxigenic species of Dinophysis and Pseudonitschia in a subtropical Brazilian estuary. Braz J Oceanograr. https://doi.org/10.1590/S1679-87592015071906301
Utermohl H, 1958. Zur vervollkommung der quantitativen phytoplankton-methodik. Verh Int Verein Theor Angew Limnol 9: 1–39.
Wells ML., Trainer VL, Smayda TJ, Karlson BSO, Trick CG, Kuelda RM, Ishikawa A, Berbard S, Wulff A, Anderson AM, Cochlan WP, 2015. Harmful algal blooms and climate change: learning from the past and present to forecast the future. Harmful Algae 49:68-83.
Yasumoto T, Oshima Y, Yamaguchi M, 1978. Occurence of a new type of shellfish poisoning in the Tohoku district. Bull Jpn Soc Sci Fish 44:1249-55.
Yasumoto T, Sugawara W, Fukuyo Y, Oguri H, Higarashi T, Fujita N, 1980. Identification of Dinophysis fortii as the causative organism of diarrhetic shellfish poisoning in the Tohoku district. Bull Jpn Soc Sci Fish 46:1405-11.
Allen JJ, Anderson D, Burford M., Dyhrman S, Flynn K, Gilbert PM, Graneli E, Heil C, Sellner K, Smayda T, Zhou M, 2006. Global Ecology and Oceanography of Harmful Algal Blooms, Harmful Algal Blooms in Eutrophic Systems. GEHOAB Report 410C and SCOR. GEOHAB, Paris/Baltimore, MD. USA, pp 1-74.
Alves-de-Souza C, Varela D, Contreras C, de La Iglesia P, Fernández P, Hipp B, Lagos N, 2014. Seasonal variability of Dinophysis spp. and Protoceratium reticulatum associated to lipophilic shellfish toxins in a strongly stratified Chilean fjord. Deep-Sea Res Pt II 101:152-62.
Anderson DM, Alpemann TJ., Cembella AD, Collos Y, Masseret E, Montreson M, 2012. The globally distributed genus Alexandrium: multificated roles in marine ecosystems and impacts on human health. Harmful Algae 14:10-35.
Aune T, Espenes A, Aasen JAB, Quilliam MA, Hess P, Larsen S, 2012. Study of possible combined toxic effects of azaspiracid-1 and okadaic acid in mice via the oral route. Toxicon 60:895-906.
Bauder AG, Cembella AD, Quilliam MA, 1996. Dynamics of diarrheic shellfish toxins from the dinoflagellate, Prorocentrum Lima, in the bay scallop, Argopecten irraddians. In: Yasumoto T , Oshima Y, Fukuyo Y, eds. Harmful and Toxic Phytoplankton Blooms IOC/UNESCO, Paris, pp 433-81.
Basti L, Uchida H, Matsushima R, Watanabe N, Suzuki T, Yamatogi T, Nagai S, 2015. Influence of temperature on growth and production of pectenotoxin-2 by a monoclonal culture of Dinophysis caudata. Mar Drugs 13:7124-73.
Bazzoni AM, Mudadu AG, Lorenzoni G, Soro B, Bardino N, Arras I, Sanna G, Vodret B, Bazzardi R, Marongiu, Virgilio S, 2018. Detection of Dinophysis species and associated okadaic acid in farmed shellfish: a two-year study from the western Mediterranean area. J Vet Res 62:137-44.
Boni L, Milandri A, Poletti R, Pompei M, 1993. DSP cases along the coastal of Emila Romagna (Northwestern Adriatic sea). In: Smayda TJ, ed. Toxic Phytoplancton Blooms in the Sea. Elsevier, Amsterdam, pp 475-81.
Chavez FP, Messiè M, Pennington JT, 2011. Marine primary production in relation to climate variability and change. Annu Rev Mar Sci 3:222-60.
Edwards M., Johns DG, Leterme SC, Svendsen E, Richardson AJ, 2006. Regional climate change and harmful algal blooms in the northeast Atlantic. Limnol Oceanogr 51:820-29.
France J, Mozetič P, 2006. Ecological characterization of toxic phytoplankton species (Dinophysis spp., Dinophyceae) in Slovenian mariculture areas (Gulf of Trieste, Adriatic Sea) and the implications for monitoring. Mar Pollut Bull 52:1504-16.
Fu FX, Tatters AO, Hutchins DA, 2012. Global change and the future of harmful algal blooms in the ocean. Mar Ecol Progr Ser 470:207-233.
Hallengraeff GM, 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99.
Hallengraeff GM, 2003. Harmful Algal Blooms: a Global Overview, Manual on Harmful Marine Microalgae. UNESCO Publishing, Paris: 25-50.
Hegaret H, Shumway SE, Wilkfors GH, Pate S, Burkholder JM, 2008. Potential transfer of harmful algae through relocation of bivalve molluscs. Mar Ecol Progr Ser 361:169-81.
Heisler J, Gilbert PM., Burkholder JM, Anderson DM, Cochlan W, Dennison WC, Dortch Q, Gobler CJ, Heil CA, Humphries E, Lewitus A, Magnien R, Marshall HG, Sellner K, Stockwell DA, Suddleson M, 2008. Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8:3-13.
Lee JS, Igarashi T, Fraga S, Dahl E, Howgaard P, Yasumoto T, 1989. Determination of diarrhetic shellfish toxins in various dinoflagellate species. J. Appl Phycol 1:147-52.
Moore SK, Trainer VL, Mantua NJ, Parker MS, Laws EA, Backer LC, Fleming LE, 2008. Impact of climate variability and future climate change on harmful algal blooms and human health. Environ Health. doi:10.1186/1476-069X-7-S2-S4
Naustvoll LJ, Gustad E, Dahl E, 2013. Monitoring of Dinophysis species and diarrhetic shellfish toxins in Flødevigen Bay, Norway: inter-annual variability over a 25-year time series. Food Addit Contam 29:1605-15.
Nincevic-Gladan Z, Skejic S, Buzancic M, Marovic I, Arapov J, Ujevic I, Bojanic N, Grbec B, Kuspilic G, Vidjak O, 2008. Seasonal variability in Dinophysis spp. abundances and diarrhetic shellfish poisoning outbreaks along the eastern Adriatic coast. Bot Mar 51:449-63.
Padedda BM, Pulina S, Magni P, Sechi N, Lugliè A, 2012. Phytoplankton dynamics in relation to environmental changes in a phytoplankton-dominated Mediterranean lagoon (Cabras Lagoon, Italy). AIOL J 3:147-69.
Pitcher GC, Calder D, 2000. Harmful algal blooms of the southern Benguela Current: a review and appraisal of monitoring from 1989 to 1997. S Afr J Mar Sci 22:257-71.
Philips EJ, Badylak S, Christman M, Wolny J, Brame J, Garland J, Hall L, Hart J, Landsberg J. Lasi M, Lockwood J, Paperno R, Scheidt D, Staples A, Steindinger K, 2011. Scales of temporal and spatial variability in the distribution of harmful algae species in Indian River Lagoon, Florida, USA. Harmful Algae 10:277-90.
Pizzarro G, Paz B, Gonzales-Gil S, Franco JM, Roguera B, 2009. Seasonal variability of lipophilic toxins during a Dinophysis acuta bloom in Wester Iberia. Differences between picked cells and plankton concentrates. Harmful Algae 8:926-37.
Roguera B, Velo-Suarez R, Park M, 2012. Harmful Dinophysis species: a review. Harmful Algae 14:87-106.
Roguera R, Riobo P, Rodriguez F, Diaz PA, Pizzarro G, Paz B, Franco JM, Blanco J, 2014. Dinophysis toxins: causative organisms, distribution and fate in shellfish. Mar Drugs 12:394-461.
Tibirica C, Fernandes LF, Mafra Junior LL, 2015. Seasonal and spatial patterns of toxigenic species of Dinophysis and Pseudonitschia in a subtropical Brazilian estuary. Braz J Oceanograr. https://doi.org/10.1590/S1679-87592015071906301
Utermohl H, 1958. Zur vervollkommung der quantitativen phytoplankton-methodik. Verh Int Verein Theor Angew Limnol 9: 1–39.
Wells ML., Trainer VL, Smayda TJ, Karlson BSO, Trick CG, Kuelda RM, Ishikawa A, Berbard S, Wulff A, Anderson AM, Cochlan WP, 2015. Harmful algal blooms and climate change: learning from the past and present to forecast the future. Harmful Algae 49:68-83.
Yasumoto T, Oshima Y, Yamaguchi M, 1978. Occurence of a new type of shellfish poisoning in the Tohoku district. Bull Jpn Soc Sci Fish 44:1249-55.
Yasumoto T, Sugawara W, Fukuyo Y, Oguri H, Higarashi T, Fujita N, 1980. Identification of Dinophysis fortii as the causative organism of diarrhetic shellfish poisoning in the Tohoku district. Bull Jpn Soc Sci Fish 46:1405-11.
1.
Mudadu AG, Bazzoni AM, Bazzardi R, Lorenzoni G, Soro B, Bardino N, Arras I, Sanna G, Vodret B, Virgilio S. Influence of seasonality on the presence of okadaic acid associated with <em>Dinophysis</em> species: A four-year study in Sardinia (Italy). Ital J Food Safety [Internet]. 2021 Mar. 25 [cited 2024 Apr. 20];10(1). Available from: https://www.pagepressjournals.org/ijfs/article/view/8947
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