Rising water temperatures, reproduction and recruitment of an invasive oyster, Crassostrea gigas, on the French Atlantic coast
Introduction
Suspension-feeding bivalves are coastal ecosystem engineers that regulate matter and energy fluxes by coupling pelagic and benthic processes (see Dame and Olenin (2005) for reviews). In the 20th century, over-exploitation, pollution, and disease led to a worldwide decline in native oyster populations, accompanied by economic losses and ecological changes (Newell, 1988, Quayle, 1988, Ruesink et al., 2005). The Pacific cupped oyster, Crassostrea gigas, was voluntarily introduced in several new coastal areas around the world for aquaculture purposes, because of its rapid growth rate, high tolerance to environmental variations and low susceptibility to oyster diseases (Coleman, 1986, Smith et al., 1986, Grizel and Héral, 1991).
Although successful introductions of C. gigas occurred particularly in northern temperate countries of Europe and North America, water temperatures precluded substantial larval recruitment in the northernmost regions (Le Borgne et al., 1973, Gruet et al., 1976, Goulletquer, 1995, Drinkwaard, 1999). France is a particularly interesting case, since the occurrence of massive and regular feral C. gigas recruitments in the southern Atlantic regions, but not in the northern ones, suggested that the limit for the successful larval development was situated south of Bourgneuf Bay (Goulletquer and Héral, 1991, Robert and Gérard, 1999). However, in the past decade, feral oysters have proliferated on northern European Atlantic coasts, unrelated to new introductions, and C. gigas is now considered to be an invasive organism from Spain to the North Sea (Reise et al., 1999, Wehrmann et al., 2000, Cognie et al., 2006, Brandt et al., 2008). This phenomenon is particularly visible in northern French turbid bays, where the feral C. gigas build long-lasting reefs and colonize racks on which are attached farmed C. gigas bags (Martin et al., 2004, Martin et al., 2005). In these areas, trophic competition with feral oysters has been suggested to explain the decline in farmed oyster growth performance in the last 10 years (Cognie et al., 2006). Although reproduction performances of farmed adult oysters are being elucidated (Dutertre et al., in press), field studies on natural recruitment are also necessary to understand the recent feral oyster invasion (Underwood and Fairweather, 1989, Grosberg and Levitan, 1992, Smaal et al., 2005).
Optimal larval development of C. gigas requires a water temperature higher than 22 °C during at least two weeks (Arakawa, 1990, Shatkin et al., 1997, Rico-Villa et al., 2008) and oyster larvae are affected by food quality and quantity (Baldwin and Newell, 1995, Powell et al., 2002, Rico-Villa et al., 2008). As larval survival is the determining element for the settlement of feral oyster populations (Gosling, 2003), environmental influences on larval development need to be clarified by field studies, especially in turbid coastal waters which are characterized by seasonal and short-term variations of the environmental conditions (Mann, 1982).
In an attempt to determine the causes of the recent invasion of feral oysters, in northern cold temperate ecosystems, the present study analyzed the larval development and post-larval recruitment of C. gigas at the southern and northern geographic extremes of Bourgneuf Bay in relation to real-time monitored environmental factors.
Section snippets
Adult oyster sampling and tissue fixation
Feral and farmed oysters were collected at two oyster-farming sites in Bourgneuf Bay, between February 2005 and July 2006 (Fig. 1, Haure and Baud, 1995). The northern site, La Coupelasse (47°1′34.7″N, 2°1′55.9″W), is a high-turbidity mudflat compared to the southern sandy-muddy bottom site, Gresseloup (46°57′2.6″N, 2°7′53.4″W).
At the beginning of the study, in February 2005, adult farmed oysters (shell length = 69.2 ± 4.9SD mm, originating from 18-month hatchery-born spats), were installed, at both
Seston quantity and quality
Over the sampling period, SPM, POM and chl-a concentrations were always higher at the HT site compared to the IT site (Fig. 2A–C – two-way ANOVA, p < 0.01). The monthly mean POM:SPM ratio, used to estimate potential food dilution, was lower at the HT site in 2005 and 2006 (Fig. 3A, t-test, p < 0.01). On the other hand, the monthly mean chl-a:POM ratio, used to estimate food quality, was higher at the HT site in 2005 (Fig. 3B, t-test, p < 0.01), while no significant difference between sites was
Water temperature and recent oyster invasion
At approximately 28 000 tons, the feral oyster stock in Bourgneuf Bay equals 70% of the annual farmed oyster production (Cognie et al., 2004, Martin et al., 2004, Martin et al., 2005). Water temperature variations, since the introduction of C. gigas for aquaculture, clearly show that the onset of the feral oyster invasion coincided with a marked water warming (Fig. 4). Indeed, between 1970 and 1995, when annual mean water temperature was usually lower than the median temperature (13.4 °C),
Conclusion
The historical data presented here clearly show that C. gigas proliferation in the Bourgneuf Bay ecosystem corresponds to warmer water temperatures, particularly since 1995. A similar evolution in water temperatures has been recorded at more northerly sites (Wadden Sea), also corresponding to increasing C. gigas recruitment (Diederich et al., 2005). The underlying processes of reproduction and development are acutely sensitive to such warming through the threshold temperatures of oocyte growth
Acknowledgements
We thank David Lecossois for the installation of the animals used in this study in oyster bags at his farm, and Odile Aumaille for technical assistance in histological analyses. Research funding was provided by the Syndicat Mixte pour le Développement de l’Aquaculture et de la Pêche (SMIDAP) de la Région des Pays de la Loire, and M. Dutertre was supported by a PhD scholarship from the Ministère Français de la Recherche et de l’Enseignement Supérieur.
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2020, Continental Shelf ResearchCitation Excerpt :2005; Dunstan and Bax, 2007; Butler et al., 2012; Berestyck et al., 2009; Excoffier et al.,. 2009; Sexton et al., 2009; Woodin et al., 2013). In comparison, documentation of range shift dynamics, beyond the observation of a shift in distributional pattern, is limited (Gilman, 2006; Hellmann et al., 2008; Castaños et al., 2009; Troost, 2010; Woodin et al., 2013) with the dynamic spread of introduced species offering a disproportionate number of case histories in the marine realm (Sagarin et al., 1999; Troost, 2010; Dutertre et al., 2010; Wethey et al.,. 2016) and with little documentation of range shifts for continental shelf species. On the continental shelf off the northeast coast of the U.S., two provincial boundaries are in play which delineate respectively the Virginian province historically delineated by Cape Hatteras and Cape Cod (Hale, 2010), inhabited by cold temperate species, and the intrusion of the Acadian Province (Hale, 2010), inhabited by boreal species, into the Mid-Atlantic by the cold pool (Lentz, 2017).