The dinoflagellate Alexandrium minutum affects development of the oyster Crassostrea gigas, through parental or direct exposure

Abstract

Harmful algal blooms are a threat to aquatic organisms and coastal ecosystems. Among harmful species, the widespread distributed genus Alexandrium is of global importance. This genus is wellknown for the synthesis of paralytic shellfish toxins which are toxic for humans through the consumption of contaminated shellfish. While the effects of Alexandrium species upon the physiology of bivalves are now well documented, consequences on reproduction remain poorly studied. In France, Alexandrium minutum blooms have been recurrent for the last decades, generally appearing during the reproduction season of most bivalves including the oyster Crassostrea gigas. These blooms could not only affect gametogenesis but also spawning, larval development or juvenile recruitment. This study assesses the effect of toxic A. minutum blooms on C. gigas reproduction. Adult oysters were experimentally exposed to A. minutum, at environmentally realistic concentrations (10 2 to 10 3 cells mL −1) for two months during their gametogenesis and a control group, not exposed to A. minutum was fed with a non-toxic dinoflagellate. To determine both consequences to next generation and direct effects of A. minutum exposure on larvae, the embryo-larval development of subsequent offspring was conducted with and without A. minutum exposure at 10 2 cells mL −1. Effects at each stage of the reproduction were investigated on ecophysiological parameters, cellular responses, and offspring development. Broodstock exposed to A. minutum produced spermatozoa with decreased motility and larvae of smaller size which showed higher mortalities during settlement. Embryo-larval exposure to A. minutum significantly reduced growth and settlement of larvae compared to non-exposed offspring. This detrimental consequence on larval growth was stronger in larvae derived from control parents compared to offspring from exposed parents. This study provides evidence that A. minutum blooms, whether they occur during gametogenesis, spawning or larval development, can either affect gamete quality and/or larval development of C. gigas, thus potentially impacting oyster recruitment. 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.

Effects of marine harmful algal blooms on bivalve cellular immunity and infectious diseases: A review

“…Effects of HABs upon bivalve reproduction and on physiology through parental exposure were reported recently (e.g. Basti et al, 2013;Castrec et al, 2019Castrec et al, , 2020Rolton et al, 2015), and could ultimately alter bivalve population fitness in the case of repeated blooms. Adaptations of bivalve populations to recurrent toxic blooms, reflected by differential physiological responses between populations (Navarro et al, 2014), can lead to the emergence of resistant genotypes (Bricelj et al, 2010(Bricelj et al, , 2005.…”

“…Lassudrie et al, 2014;Medhioub et al, 2012; see review of Landsberg, 2002). BEC have allelopathic, lytic, and oxidative activity reported upon microalgae, protists, or bivalve gametes (Arzul et al, 1999;Castrec et al, 2019;Flores et al, 2012;Le Goïc et al, 2014Lelong et al, 2011;Long et al, 2018b;Tillmann and John, 2002). Toxins (intraand extracellular) as well as BEC produced by HABs can be harmful to bivalves (e.g.…”

“…extracellular compounds toward different cells, such as microalgae, protists, or bivalve gametes (Arzul et al, 1999;Castrec et al, 2019;Flores et al, 2012;Le Goïc et al, 2014Lelong et al, 2011;Long et al, 2018b;Tillmann and John, 2002). Although PST can be released extracellularly (Lefebvre et al, 2008;Persson et al, 2012), many studies reported the bioactivity of extracellular compounds produced by non-PST Alexandrium strains, demonstrating that these effects are independent from PSTs (Bianchi et al, 2019;Borcier et al, 2017;Castrec et al, 2019Castrec et al, , 2020Ford et al, 2008;Long et al, 2018b;Tillmann et al, 2007;Tillmann and John, 2002). Only a few studies focused on the characterization of these compounds, and their precise nature remains unknown (Flores et al, 2012;Ma et al, 2011Ma et al, , 2009).…”

The toxic dinoflagellate Alexandrium minutum impairs the performance of oyster embryos and larvae

“…The embryo development up to D-larvae involves only endogenous exchanges (Bayne, 2017b), and D-larvae are unable to ingest Alexandrium cells due to their relatively large size (23-29 μm) (Raby et al, 1997;Helm et al, 2004); -Exp2 = umbonate larvae exposure: from 13 days post-fertilization (dpf) (larvae shell height 163.7 ± 1.3 µm) to 15 dpf. These umbonate planktotrophic larvae (Rico-Villa et al, 2006) are not able to feed on A. minutum cells at a mean shell length of 150 ± 22 µm (Castrec et al, 2019); -Exp3 = eyed larvae exposure: from 20 dpf (larvae shell height 295.2 ± 2.3 µm, percentage of eyed larvae 40.9 ± 3.9) to 21 dpf. These eyed competent larvae are also planktotrophic larvae with high phytoplankton consumption (Rico-Villa et al, 2006), and are able to feed on Alexandrium cells (Castrec et al, 2019).…”

“…Direct exposure of early life stages to PST-producing Alexandrium strains decreased larval activity, survival, growth, and settlement of several bivalve species, including C. gigas, Pinctada fucata martensii, Chlamys farreri, and Argopecten irradians (Matsuyama et al, 2001;Yan et al, 2001Yan et al, , 2003Mu and Li, 2013;Basti et al, 2015). Moreover, adult oysters C. gigas exposed to A. minutum produced spermatozoa with decreased motility and larvae of smaller size which exhibited higher mortalities during settlement, demonstrating that larval development could also be affected via exposure of parents to harmful algae (Haberkorn et al, 2010;Castrec et al, 2019).…”