Effects of environmental factors on the daily growth rate of Pecten maximus juveniles in the Bay of Brest (France)

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Abstract

The study of the effects of environmental factors on the daily growth of Pecten maximus juveniles (one- and two-year olds) in the Bay of Brest was prompted by the decline of the scallop fishery in the Bay. Scallops over 30 mm in shell length were collected monthly from October 1994 to November 1995. Daily shell growth rings were counted using image analysis. Multiple stepwise regression analyses were performed to identify environmental parameters significantly affecting mean daily shell growth rates of one- and two-year-old juveniles in 1994 and 1995. Normal growth of Pecten shells is mainly regulated by bottom-water temperature, salinity and, to a lesser extent, river flow, rather than food. In 1995, three major toxic blooms of Gymnodinium cf. nagasakiense were recorded, leading to major reductions in shell growth rates. The effect of the toxic blooms on the natural Pecten populations was all the more important as no wild scallop spat settled on artificial collectors during the 1995 summer toxic events, and no pre-recruits originating from the 1995 spawnings were sampled on the bottom, despite good-quality spawnings. Two growth retardations were observed for one-year-old juveniles during the summer of 1995: the first one appears to be related to the sedimentation of a Rhizosolenia delicatulaChaetoceros sociale bloom. It is suggested that the large aggregates of these diatoms led to clogging of the scallop gills. The second growth decrease was explained by the first bloom of G. cf. nagasakiense. The second and third dinoflagellate blooms were not associated with daily growth rate decreases in one-year-old scallops. The toxic effect of the dinoflagellate blooms was greater for two-year-old than for one-year-old juveniles; higher filtration rates and/or a differently oriented metabolism, compared with younger individuals, would explain these variations.

Introduction

In the Bay of Brest, the annual production of scallops, Pecten maximus (L.), dropped from 1500–2600 tons in the 1950s to 100–300 tons from 1963 onwards. The 114 tons landed in 1993–1994 accounted for ca. 17% of scallop stocks; the 1994 recruitment did not compensate for mortalities occurring between October 1993 and October 1994. Annual fluctuations in recruitment and survival of scallop juveniles are therefore critical for the management of exploited stocks. This study focuses on the environmental factors affecting the daily growth rate of one- and two-year-old scallops in the Bay. The Pecten population experienced a benthic pre-recruitment in 1994 that was greater than that observed in previous years. The exceptionally high numbers of post-larvae settled in Japanese collectors in 1994 (>300 post-larvae per collector; Chauvaud et al., 1996), in combination with several successful spawnings (Paulet et al., 1995) provided the first indications of good reproduction. By the end of 1994, 4.73 million pre-recruits were estimated to have been added to the local scallop population. This number is three times higher than that observed the year before (Fifas, pers. comm.). These age 0 individuals, at the beginning of the 1994–1995 winter, had a mean shell height of 33 mm, which is an exceptional size for the Bay of Brest (a height of 25 mm is usually observed). This larger size was not maintained during the second year of growth, however. The 1994 class had a mean shell size of 62 mm in October 1995, which is similar to the mean observed over the last ten years (65 mm; Paulet, unpublished). In addition, a clearly visible extra ring, indicating a growth rate decrease, was observed in all age groups of the scallop population; the extra ring would indicate the occurrence of a period of stress during the summer of 1995. This disruption in the growth of natural juvenile and adult scallop populations occurred at the same time as the summer mass mortalities of post-larvae in the hatchery located in the southern basin of the Bay (Tinduff, Plougastel). Simultaneously with these events was the occurrence of an exceptionally lengthy and severe toxic bloom of Gymnodinium cf. nagasakiense (dinoflagellate) within the Bay (Arzul et al., 1995). In particular, mass mortalities of post-larvae within the rearing tanks were found to be associated with high Gymnodinium counts in the water (Muzellec, pers. comm.).

The effect of toxic planktonic algal blooms on benthic populations has been the object of a number of studies (e.g. Tangen, 1977, Boalch, 1979, Marsden and Shumway, 1993). The toxicity of these blooms on bivalves, gastropods and even decapods is due to the production of specific toxins and/or the anoxic conditions generated in the environment or to clogging of the gills (Shumway, 1990). The toxins can be transferred directly from the algae to the organisms or indirectly via trophic transfer using the same routes as those observed for carbon flux. Bioaccumulation has been observed in bivalve filter feeders such as Mytilus edulis (Mortensen, 1985, Carreto et al., 1985), Crassostrea gigas (Ikeda et al., 1989), Patinopecten yessoensis (Oshima, 1995), P. albidans (Ikeda et al., 1989) and Chlamys nipponensis (see Shumway, 1990), as well as in top carnivores including fish (herring and mackerel; Haya et al., 1990), sea birds (Work et al., 1993) and marine mammals (Taylor, 1990). The negative effect of these microalgal toxins on the metabolism and growth of bivalves has clearly been demonstrated in C. virginica (Ukeles and Sweeney, 1969, Marsden and Shumway, 1993, Sellner et al., 1995), Perna canaliculus (Marsden and Shumway, 1992) and M. edulis (see Marsden and Shumway, 1993). In the pectinids P. maximus (Erard-Le Denn et al., 1990) and Argopecten irradians (Bricelj et al., 1987), a decrease in growth rate and reproduction has been observed in the presence of certain toxic blooms. In addition, mass mortalities of Ostrea lurida (Woelke, 1961), M. edulis (O'Sullivan, 1978) and Spisula solidissima (Tiffany and Heyl, 1978) have been observed in the presence of Gymnodinium. These dinoflagellates can also cause mass mortalities of P. maximus in experimental tanks (Shumway, 1990) and are known to cause larval (Minchin, 1984), post-larval and juvenile mortalities (Erard-Le Denn et al., 1990) in the wild.

The aim of this study was to determine significant relationships between the growth and survival anomalies observed for P. maximus in 1995 in the Bay of Brest, and the simultaneous presence of toxic blooms. To this end, the daily growth rates of juveniles and the pre-recruitment characteristics were studied in relation to the pattern of change of the main environmental parameters within the Bay.

Section snippets

Study site

The Bay of Brest (Fig. 1) is a semi-enclosed marine ecosystem of 180 km2 that is connected to shelf waters (Iroise) by a narrow (2 km wide) and deep (40 m) strait. The Bay is a shallow basin with 50% of its surface shallower than 5 m (average depth, 8 m). There are five watersheds responsible for freshwater inputs in the Bay, but those from the two main rivers, the Aulne (1842 km2) and the Elorn (402 km2) make up 80% of the total freshwater inputs. Tidal action induces short-term variability in

Meteorological conditions

Climatic features of the study region lead to important seasonal and inter-annual variations of solar radiation, precipitation and wind (Fig. 2). The maximum irradiances for the two years were 3015 J cm−2 day−1 on 9 June 1994 and 2996 J cm−2 day−1 on 22 June 1995. Minimum values were 63 and 47 J cm−2 day−1 on 12 January 1994 and 8 December 1995, respectively. Total solar radiation was similar in both years (384 kJ for 1994 and 402 kJ for 1995). However, the irradiance remained higher in late

Inter-annual variability of meteorological and hydrobiological factors

The rainfall levels recorded during the winter of 1994–1995 were among the highest recorded this century. The flood-related declines in salinity were also atypical, as salinity reached values of 27 and 33 PSU in surface and bottom waters. However, the return to normal spring salinity levels occurred earlier in 1995 than in 1994 (34 vs. 33.5 PSU on 30 March, respectively). During this period, the irradiance levels and water temperatures (11.5°C on 20/04/95 vs. 10.1°C on 20/04/94) were higher in

Conclusion

The study, in the Bay of Brest, of the effects of environmental factors on the daily growth of P. maximus juveniles points out five major results: (1) Normal shell growth (i.e. with a daily shell growth rate similar to that observed for other European scallop populations) of P. maximus juveniles occurs in the Bay of Brest, in the absence of summer toxic blooms; (2) under normal conditions (without toxic blooms), shell growth is mainly regulated by bottom-water temperature. With the exception of

Acknowledgements

The authors thank the crews of the R.V. Côtes d'Aquitaine, Gwen Drez, Sainte-Anne du Portzic, Palangrin II, Laborieux, Kurun and Astre Béni for valuable assistance during the cruises. The authors are also particularly grateful to A. Le Mercier (image analysis), E. Nézan, Y. Del Amo and H. Breton (phytoplankton composition), and to Y. Craignou, Y. Gladu, F. Jean and R. Marc (scuba diving). The study was part of a four-year EC-funded research program on scallop recruitment, undertaken by IFREMER,

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      Moreover, the observation by Thébault et al. (2022) and the results of this study, showing that Mo/Cashell maxima coincide with a preceding reduction in growth rate of the bivalve (Fig. 4), are consistent with and support both assumptions. On the one hand, blooms of Gymnodinium spp. are known to be toxic and negatively affect growth rates in bivalves (Chauvaud et al., 2001, 1998; Widdows et al., 1979). On the other hand, the sedimentation of aggregates can disturb shell growth caused by oxygen depletion and/or gill clogging (Lorrain et al., 2000).

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