The blue mussel Mytilus edulis is vulnerable to the toxic dinoflagellate Karlodinium armiger—Adult filtration is inhibited and several life stages killed

Binzer, Sofie Bjørnholt; Lundgreen, Regitze B. C.; Berge, Terje; Hansen, Per Juel; Vismann, Bent

doi:10.1371/journal.pone.0199306

Cited by 11 publications

(4 citation statements)

References 56 publications

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“…Algae effects were also investigated. Lethal effects of toxic dinoflagellate algae were reported in M. galloprovincialis with Ostreopsis cf ovata (Carella et al, 2015) and in M. edulis with Karlodinium armiger (Binzer et al, 2018). On sheltered rocky shores, the presence of epibiotic algae on the shell was reported to increase the mortality risk in both mussel species (O'Connor, 2010).…”

Section: Resultsmentioning

confidence: 99%

Mortality of marine mussels Mytilus edulis and M. galloprovincialis: systematic literature review of risk factors and recommendations for future research

Lupo

Bougeard²,

Bihan

et al. 2020

Reviews in Aquaculture

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The aim of this study was to summarise the literature reporting the risk factors for mortality in the mussel species Mytilus edulis and Mytilus galloprovincialis in order to identify potential science-based solutions to prevent or mitigate mussel mortality outbreaks. We followed the PRISMA methodology: Preferred Reporting Items for Systematic Reviews and Meta-Analyses. The studied corpus of 91 publications (114 studies) was highly heterogeneous with respect to the methodological approaches used to define or estimate mussel mortality and the related putative risk factors. Results showed that the mortality risk of both mussel species M. edulis and M. galloprovincialis varied across the seasons, increased with an elevated seawater temperature above a thermal threshold of 20 and 24°C, respectively, decreased by protecting mussels from predation, and was associated with the presence of pathogens in M. edulis. For M. galloprovincialis, using mussel spat from the same area where the farming is carried out and farming them together with another mussel species appears to reduce the mortality risk. However, for M. edulis, this could be achieved by using pure crosses and in particular mussel spat having a selected genotype. For wild bed conservation, sand accumulation and anthropogenic sedimentation should be minimised. Our analysis showed that current approaches to this research topic are limited and are unlikely to yield actionable evidence to identify mussel mortality prevention or mitigation strategies. Therefore, recommendations are offered to increase the ability of future eco-epidemiological research to identify multiple exposures associated with mussel mortality, underpinned by standardised efforts and cooperative initiatives.

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Section: Resultsmentioning

confidence: 99%

Mortality of marine mussels Mytilus edulis and M. galloprovincialis: systematic literature review of risk factors and recommendations for future research

Lupo

Bougeard²,

Bihan

et al. 2020

Reviews in Aquaculture

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“…The majority of studies on bivalves and DST and PTX are focused on depuration processes [6,17,[19][20][21][22][23][24] or physiological effects [25,26]. The physiological effects on bivalves of other harmful algal toxins have received far more attention [27][28][29][30][31][32][33][34][35][36]. Reduced clearance rates have been observed in M. edulis exposed for one hour to the toxic dinoflagellate Karenia mikimotoi (= Gyrodinium aureolum, > 600 cells ml -1 ) [27].…”

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confidence: 99%

“…Reduced clearance rates have been observed in M. edulis exposed for one hour to the toxic dinoflagellate Karenia mikimotoi (= Gyrodinium aureolum, > 600 cells ml -1 ) [27]. Presence of the karmitoxin producing dinoflagellate Karlodinium armiger has been shown to cause immediately cessation of clearance in M. edulis and to kill eggs, embryos and adult individuals of M. edulis [36]. The effects of the PST producing dinoflagellate, Alexandrium catenella (= Protogonyaulax tamarensis) on seven different bivalve species have been shown to be species dependent [28].…”

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confidence: 99%

Effects of the DSP-toxic dinoflagellate Dinophysis acuta on clearance and respiration rate of the blue mussel, Mytilus edulis

et al. 2020

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Diarrheic Shellfish Poisoning toxins (DST) are a severe health risk to shellfish consumers and can be a major problem for the shellfish industry. Bivalve molluscs can accumulate DST via ingestion of toxic dinoflagellates like Dinophysis spp., which are the most prominent producers of DST. The effects of DST-containing dinoflagellate Dinophysis acuta on bivalve clearance and respiration rate were investigated in the blue mussel (Mytilus edulis) exposed to different algal densities in a controlled laboratory study. Results showed that M. edulis exposed to D. acuta displayed a reduced clearance rate compared to M. edulis exposed to equivalent bio-volumes of the non-toxic cryptophyte Rhodomonas salina. Furthermore, M. edulis ceased to feed on D. acuta after 1 to 4 h, depending on D. acuta densities. The quickest response was observed at the highest densities of D. acuta. The estimated total amount of DST accumulated in the M. edulis exceeded the regulatory limit for human consumption and furthermore, intoxication of the M. edulis seemed to occur faster at high cell toxicity rather than at high cell density. However, respiration rates were, similar, irrespective of whether M. edulis were fed single diets of R. salina, D. acuta or a mixed diet of both algal species. In conclusion, the DST-containing D. acuta had a severe negative effect on the clearance of M. edulis, which can affect the conditions of the M. edulis negatively. Hence, DST may cause low quality M. edulis, due to reduced feeding when exposed to DST-containing D. acuta. OPEN ACCESSCitation: Nielsen P, Krock B, Hansen PJ, Vismann B (2020) Effects of the DSP-toxic dinoflagellate Dinophysis acuta on clearance and respiration rate of the blue mussel, Mytilus edulis. PLoS ONE 15 (3): e0230176. https://doi.org/10.and project no. 10-078561 (https://ufm.dk/en/researchand-innovation/councils-and-commissions/formercouncils-and-commissions/the-danish-council-forstrategic-research?set_language=en&cl=en) to PN, PJH and BV. The funder had no role in study result in long-time closure of shellfish production areas, which can lead to severe economic consequences for the shellfish industry [2].Known DST-producers include several planktonic dinoflagellate species of the genus Dinophysis and a few epibenthic Prorocentrum species [1,3]. Pelagic Dinophysis spp. have been associated with DSP events in most cases. Okadaic acid (OA) together with its variants dinophysistoxins (DTX) and pectenotoxins (PTX) have all been identified in species of Dinophysis, and to accumulate in filter-feeding bivalves e.g. reviews by [4][5][6]. Mussels accumulate DST and PTX primarily in the digestive gland [7] and a number of studies have shown that DST undergo molecular transformations when ingested by bivalves. OA and DTX are esterified to a range of different fatty acid ester derivatives [6,[8][9][10]. PTX are also esterified but can be further transformed to PTX seco acids and seco acid esters [6,10,11]. The molecular transformation into fatty acid esters and seco acids has been suggested to be...

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“…In particular, contaminants could negatively affect their reproduction as demonstrated in oysters exposed to anthropogenic pollutants (Akcha et al, 2012;Fitzpatrick et al, 2008;Mai et al, 2013;Vignier et al, 2017Vignier et al, , 2015. Experimental studies suggest that harmful algal blooms (HAB), often caused by dinoflagellates, can affect marine bivalve reproduction by altering gamete quality and larval development, growth, and survival (Banno et al, 2018;Basti et al, 2013Basti et al, , 2011Binzer et al, 2018;Bricelj and MacQuarrie, 2007;Castrec et al, 2020Castrec et al, , 2019De Rijcke et al, 2015;Gaillard et al, 2020;Rolton et al, 2018Rolton et al, , 2015Rolton et al, , 2014Tang and Gobler, 2012). In coastal areas, HAB are a recurring phenomenon that can co-occur with the reproduction of free spawning marine organisms (Gaillard et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

The toxic dinoflagellate Alexandrium minutum affects oyster gamete health and fertilization potential

Castrec

Fabioux

Goïc

et al. 2021

Marine Environmental Research

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Dinoflagellates from the globally distributed genus Alexandrium are known to produce both paralytic shellfish toxins (PST) and uncharacterized bioactive extracellular compounds (BEC) with allelopathic, ichthyotoxic, hemolytic and cytotoxic activities. In France, blooms of Alexandrium minutum appear generally during the spawning period of most bivalves. These blooms could therefore alter gametes and/or larval development of bivalves, causing severe issues for ecologically and economically important species, such as the Pacific oyster Crassostrea (=Magallana) gigas. The aim of this work was to test the effects of three strains of A. minutum producing either only PST, only BEC, or both PST and BEC upon oyster gametes, and potential consequences on fertilization success. Oocytes and spermatozoa were exposed in vitro for 2 hours to a range of environmentally realistic A. minutum concentrations (10 to 2.5 × 104 cells mL-1). Following exposure, gamete viability and reactive oxygen species (ROS) production were assessed by flow cytometry, spermatozoa motility and fertilization capacities of both spermatozoa and oocytes were analysed by microscopy. Viability and fertilization capacity of spermatozoa and oocytes were drastically reduced following exposure to 2.5 × 104 cells mL-1 of A. minutum. The BEC-producing strain was the most potent strain decreasing spermatozoa motility, increasing ROS production of oocytes, and decreasing fertilization, from the concentration of 2.5 × 103 cells mL-1. This study highlights the significant cellular toxicity of the BEC produced by A. minutum on oyster gametes. Physical contact between gametes and motile thecate A. minutum cells may also contribute to alter oyster gamete integrity. These results suggest that oyster gametes exposure to A. minutum blooms could affect oyster fertility and reproduction success. Highlights► Oyster spermatozoa and oocytes were exposed in vitro to Alexandrium minutum strains. ► Viability and fertilization capacity of gametes were drastically reduced. ► The toxicity of Alexandrium minutum upon oyster gametes is strain-specific. ► A non-PST-producing strain increased reactive oxygen species production in oocytes. ► This strain also decreased spermatozoa motility and gamete fertilization.Please note that this is an author-produced PDF of an article accepted for publication following peer review. The definitive publisher-authenticated version is available on the publisher Web site.

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The blue mussel Mytilus edulis is vulnerable to the toxic dinoflagellate Karlodinium armiger—Adult filtration is inhibited and several life stages killed

Cited by 11 publications

References 56 publications

Mortality of marine mussels Mytilus edulis and M. galloprovincialis: systematic literature review of risk factors and recommendations for future research

Mortality of marine mussels Mytilus edulis and M. galloprovincialis: systematic literature review of risk factors and recommendations for future research

Effects of the DSP-toxic dinoflagellate Dinophysis acuta on clearance and respiration rate of the blue mussel, Mytilus edulis

The toxic dinoflagellate Alexandrium minutum affects oyster gamete health and fertilization potential

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