Rising water temperatures, reproduction and recruitment of an invasive oyster, Crassostrea gigas, on the French Atlantic coast

Abstract

The recent appearance and invasion of feral oysters (Crassostrea gigas) along the northern European Atlantic coast, underscores the necessity to investigate the relationship between environmental variables, reproductive physiology, larval development and recruitment. We studied these relationships at both high (HT) and intermediate (IT) – turbidity sites, through historical data on water temperatures, multi-parameter environmental probes, histological analyses, and field collections of planktonic larvae and settled post-larvae in 2005 and 2006. A progressive warming trend was observed, especially since 1995, when oyster proliferation first became severe. Threshold temperatures for oocyte growth, larval development and settlement were achieved in both 2005 and 2006. The HT site showed greater numbers of larvae and post-larvae than the IT site for both years, with the highest numbers of post-larvae observed at both sites during the warmer summer of 2006. These results suggest that increased temperatures in northern European waters allow successful reproduction, larval development, and recruitment of C. gigas. High turbidity conditions further enhance this success.

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.