Elsevier

Aquaculture

Volume 298, Issues 3–4, 7 January 2010, Pages 338-345
Aquaculture

Behavioral responses of Crassostrea gigas exposed to the harmful algae Alexandrium minutum

https://doi.org/10.1016/j.aquaculture.2009.10.030Get rights and content

Abstract

We describe the valve-activity behavior of oysters, Crassostrea gigas, exposed experimentally to the harmful alga Alexandrium minutum (≈ 3500 cell ml 1) for 7-day periods under laboratory conditions. Our aim was to assess behavioral responses of oyster species during a mimicked bloom exposure. We determined different characteristic parameters of valve activity, such as daily valve opening duration, daily number of micro-closures, and valve-opening amplitude using a High Frequency–Non Invasive valvometer. In comparison with oysters exposed to non-toxic algae, T-Isochrysis or Heterocapsa triquetra, the valve activity of C. gigas is measurably different when exposed to toxic algae A. minutum. Surprisingly, daily valve-opening duration increased, as well as micro-closure activity, while valve-opening amplitude decreased. The response to A. minutum is fast, within 1 h after algae exposure. Following A. minutum exposure, recovery to control patterns was observed within 4–5 days. The behavioral alterations upon exposure to A. minutum can be thus used as a complementary physiological variable to other well-established physiological and biochemical measurements.

Introduction

Toxic algae blooms are a major problem in the world, in terms of aquatic ecosystem risks, human health, and economy (Bricelj and Shumway, 1998). Specifically, toxin accumulation in marine bivalves is a common phenomenon during algal blooming events that can lead to a closure of shellfish harvest for human consumption (Cembella and Todd, 1993).

Previous studies showed that filter-feeding bivalves exhibit different behavioral responses when exposed to a toxic algal bloom (Bricelj and Shumway, 1998). Responses may be related to the relative toxicity of compounds produced by the algae (Bricelj et al., 1996), toxins accumulated in the tissues of bivalves (Bricelj et al., 1991), and the history of harmful algal bloom exposure in any given ecosystem (Shumway and Cucci, 1987). Toxic algae of the genus Alexandrium are an important source of marine toxins in contaminated bivalves (Balech, 1990). Alexandrium minutum is found in coastal and estuarine waters. It is established in the coastal waters of Europe (Northeast Atlantic, North Sea, Baltic, Sea, Mediterranean and Black Sea), Southeast Asian Waters (South China Sea) and in parts of Southern Australia and New Zealand (Chang et al., 1995, Hallegraeff, 1993). This species also has been reported in North America (Page et al., 2001). The species A. minutum can reach up to 1.8 · 108 cells/L in natural marine European coastal waters (Belin and Raffin, 1998). Oysters, such as C. gigas, are known to reduce filtration rate when exposed to toxic dinoflagellate algae Alexandrium sp. (Bardouil et al., 1993, Lassus et al., 1999). Interestingly, C. gigas has been classified as having average sensitivity, in terms of response to paralytic shellfish poisoning toxins (PSP toxins) produced by toxic dinoflagellates. Indeed, oysters accumulate less PSP toxins than the mussel Mytilus edulis, described as a non-sensitive species (Bricelj and Shumway, 1998) that does not modify its nutrition activity. Oysters, such as C. gigas or C. virginica accumulate more toxin than the clam Mya arenaria, a highly sensitive species, which shows modified burrowing activity and reduces or even stops filtration activity under similar exposure. The scallop Argopecten maximus appears to be very sensitive to PSP toxins as well, increasing valve-clapping frequency and closing the shell under similar exposure conditions (Bricelj and Shumway, 1998).

In the present study, we describe the valve activity of Pacific oysters C. gigas during a 7-day exposure period to an ecologically relevant concentration of A. minutum. Valve activity was measured with a laboratory-made valvometer (Chambon et al., 2007, Tran et al., 2003; http://www.domino.u-bordeaux.fr/molluscan_eye). The original feature of this valvometer is that it uses lightweight electrodes with high sensitivity and with minimal experimental constraints. We report here different measures of valve-activity response, such as changes in daily valve-opening duration, number of micro-closures, or partial closures, and valve-opening amplitude. Our aim was to characterize, under simplified but well-controlled laboratory conditions, a putative behavioral alteration which might sign the impact of A. minutum on the oyster. The response to this toxic alga was compared to behavior of oysters in the presence of the non-toxic algae Isochrysis galbana clone Tahitian (T-Iso) or Heterocapsa triquetra.

Section snippets

Oyster characteristics and general conditions

The study was carried out in Brest (Brittany, France), in October–November 2007 (experiment 1) and December–January 2008 (experiment 2) with pacific oysters, Crassostrea gigas (Thunberg). Oysters were obtained from a shellfish farm in Kerner Island (Morbihan, France). Two homogenous groups of diploid oysters (n = 16/experiment) were chosen a priori according to the shell length (75 ± 8 mm shell length; 34.5 ± 7.6 g total fresh weight, shell plus flesh). During experiment 1, oysters were distributed

A. minutum exposure

During the exposure to A. minutum, the flow renewal of alga supply in the experimental tank of both experiments was 14 ml min 1 from the supply tank at constant concentration of A. minutum, which was in average 4981 ± 253 cell ml 1 (experiment 1 — 8 days, 2 samples in supply tank) and 4545 ± 323 cell ml 1 (experiment 2–7 days, 2 samples in supply tank), i.e. equivalent to 6.7 ng ml 1 STX eq (experiment 1) and 5.9 ng ml 1 STX eq (experiment 2). In the experimental tank, the concentration of A. minutum

Discussion

The objective of this work was to test under laboratory conditions how an exposure to the dinoflagellate A. minutum in a bloom simulation could induce a change in valve activity behavior in Pacific oysters, C. gigas. Valve activity recording and behavioral parameters to test water quality have been available for years. The pioneering developments date back to the turn of the 20th century (Hopkins, 1931, Marceau, 1909, Nelson, 1921). This is not the place for an extensive review, but among the

Acknowledgements

The authors would like to thank Gilles Durrieu and Mohamedou Sow for their help and discussions about the HFNI valvometer and Christine Schwimmer for the correction of English language. Thank you to Gary Wikfors for stimulating and constructive remarks. All experiments presented in this paper complied with the law in effect in France, where they were performed.

References (54)

  • E. Bagoien et al.

    Effects of two paralytic shellfish toxin producing dinofagellates on the pelagic harpacticoid copepod Euterpina acutifrons

    Mar. Biol.

    (1996)
  • E. Balech

    Four new dinoflagellates

    Helgol. Meeresunters.

    (1990)
  • M. Bardouil et al.

    Experimental study of the effect of a toxic microalgal diet on feeding of the oyster Crassostrea gigas Thunberg

    J. Shellfish Res.

    (1993)
  • C. Belin et al.
  • J. Borcherding

    Ten years of practical experience with the Dreissena-Monitor, a biological early warning system for continuous water quality monitoring

    Hydrobiologia

    (2006)
  • J.-F. Bouget et al.

    Dispositif de surveillance biologique de la qualité d'eau d'un site conchylicole estuarien utilisant un biocapteurs valvaire muni d'huîtres et de moules

    Tech. Sci. Méthodes

    (1997)
  • V.M. Bricelj et al.

    Paralytic shellfish toxins in bivalve mollusks: occurrence, transfer kinetics, and biotransformation

    Rev. Fish. Sci.

    (1998)
  • V.M. Bricelj et al.

    Uptake kinetics of paralytic shellfish toxins from the dinoflagellate Alexandrium fundyense in the mussel Mytilus edulis

    Mar. Ecol. Prog. Ser.

    (1990)
  • V.M. Bricelj et al.

    Influence of dinoflagellate cell toxicity on uptake and loss of paralytic shellfish toxins in the northern quahog, Mercenaria mercenaria

    Mar. Ecol. Prog. Ser.

    (1991)
  • V.M. Bricelj et al.

    Comparative physiological and behavioral responses to PSP toxins in two bivalve mollusks, the softshell clam, Mya arenaria and surfclam, Spisula solidissima

  • V.M. Bricelj et al.

    Sodium channel mutation leading to saxitoxin resistance in clams increases risk of PSP

    Nature

    (2005)
  • C. Chambon et al.

    Influence of the parasite worm Polydora sp. on the behavior of the oyster Crassostrea gigas: a study of the respiratory impact and associated oxidative stress

    Mar. Biol.

    (2007)
  • F.H. Chang et al.

    The first toxic shellfish outbreaks and the associated phytoplankton blooms in early 1993 in New Zealand

  • F.G. Doherty et al.

    Valve closure response of the Asiatic clam Corbicula fluminea exposed to cadmium and zinc

    Hydrobiologia

    (1987)
  • J.L. Dupuy et al.

    Gonyaulax washingtonensis, its relationship to Mytilus californianus and Crassostrea gigas as a source of PSP toxin in Sequim bay, Washington

    Proc. Natl. Shellfish. Ass.

    (1967)
  • S.E. Ford et al.

    Deleterious effects of a non PST bioactive compound(s) from Alexandrium tamarense on bivalve hemocytes

    Mar. Biol.

    (2008)
  • D.M. Frank et al.

    A fiber optic sensor for high resolution measurement and continuous monitoring of valve gape in bivalve molluscs

    J. Shellfish Res.

    (2007)
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