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Alexandrium Fundyense and A. Catenella) Have Minimal Apparent Evects on Oyster Hemocytes

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Alexandrium Fundyense and A. Catenella) Have Minimal Apparent Evects on Oyster Hemocytes Mar Biol (2007) 152:441–447 DOI 10.1007/s00227-007-0703-3 RESEARCH ARTICLE Toxic dinoXagellates (Alexandrium fundyense and A. catenella) have minimal apparent eVects on oyster hemocytes Hélène Hégaret · Gary H. Wikfors · Philippe Soudant · Christophe Lambert · Sandra E. Shumway · Jean Baptiste Bérard · Patrick Lassus Received: 1 August 2005 / Accepted: 9 April 2007 / Published online: 8 May 2007 © Springer-Verlag 2007 Abstract The possible eVect of Alexandrium spp. con- in C. virginica and measured toxin accumulation in C. taining paralytic shellWsh poisoning (PSP) toxins on the gigas. The only signiWcant correlation found was between hemocytes of oysters was tested experimentally. In one toxin accumulation at one temperature and higher numbers trial, eastern oysters, Crassostrea virginica Gmelin, were of circulating live and dead hemocytes in C. gigas. The PSP exposed to bloom concentrations of the sympatric dinoXa- toxins are known to interfere speciWcally with sodium- gellate, Alexandrium fundyense Balech, alone and in a channel function; therefore, the Wnding that the toxins had mixture with a non-toxic diatom, Thalassiosira weissXogii no eVect on measured hemocyte functions suggests that (Grun) Fryxell et Hasle. Subsequently, another experiment sodium-channel physiology is not important in these hemo- exposed PaciWc oysters, Crassostrea gigas Thunberg, to a cyte functions. Finally, because oysters were exposed to the mixed suspension of the sympatric, toxic species Alexand- living algae, not puriWed toxins, there was no evidence of rium catenella (Whedon et Kofoid) Balech, with T. bioactive compounds other than PSP toxins aVecting hemo- weissXogii. Measurements of numbers of oyster hemocytes, cytes in the two species of Alexandrium studied. percentages of diVerent cell types, and functions (phagocy- tosis, reactive oxygen species (ROS) production, and mor- tality) were made using Xow-cytometry. During and after Introduction exposure, almost no signiWcant eVects of Alexandrium spp. upon hemocyte numbers, morphology, or functions were Paralytic shellWsh poisoning (PSP) toxins are produced by a detected, despite observations of adductor-muscle paralysis number of dinoXagellates including Alexandrium spp. (formerly included in the genus Protogonyaulax or Gonyaulax), Gymnodinium catenatum, and Pyrodinium bahamense. Suspension feeders, such as bivalve molluscs, Communicated by J.P. Grassle. are the principal vectors transferring these phytotoxins to H. Hégaret · S. E. Shumway humans and other consumers of shellWsh, as bivalves accu- Marine Science Department, mulate toxins from the toxic algae they consume (Bricelj University of Connecticut, 1080 Shennecossett Road, and Shumway 1998). Capacity to accumulate PSP toxin Groton, CT 06340, USA diVers among bivalve species (Shumway et al. 1988; Gainey G. H. Wikfors (&) and Shumway 1988a; Bricelj and Shumway 1998; Bricelj NOAA Fisheries, Northeast Fisheries Science Center, et al. 2005). For example, when exposed simultaneously to 212 Rogers Avenue, Milford, CT 06460, USA a toxic algal bloom, oysters accumulated lower levels of e-mail: [email protected] toxins than did mussels (Lassus et al. 1999). P. Soudant · C. Lambert Despite apparent tolerance of accumulated PSP and LEMAR UMR 6539, IUEM-UBO, other toxins in their soft tissues, some bivalves may have Place Nicolas Copernic, Plouzané, France reduced survival and growth (Shumway 1990). Other stud- V J. B. Bérard · P. Lassus ies provide evidence of sub-lethal e ects, such as reduced IFREMER, BP 21105, Nantes, 44311, France clearance rates in juvenile bay scallops (Argopecten irradians 123 442 Mar Biol (2007) 152:441–447 irradians), northern quahogs (Mercenaria mercenaria), diVerences in experimental design and protocols for hemo- soft-shell clams (Mya arenaria), blue mussels (Mytilus edu- cyte-parameter analyses. lis), and Xat oysters (Ostrea edulis) in the presence of toxic Alexandrium spp. cells (Lesser and Shumway 1993). Simi- larly, Lassus et al. (1996) reported reduced clearance rates Materials and methods in PaciWc oysters (Crassostrea gigas) exposed to A. tama- rense and Shumway and Cucci (1987) demonstrated its Two experiments were conducted in which oysters were eVects on shell-valve closure and mucus production in sev- exposed to cultures of toxin-producing strains of dinoXa- eral bivalve species. Changes in heart rate of bivalves have gellates, Alexandrium spp. and then analyzed for hemocyte also been observed in the presence of A. tamarense (Gainey parameter changes: one was conducted in May 2004 at the and Shumway 1988b). Li et al. (2002) showed a decline in Milford Laboratory (Connecticut, USA), and another was the clearance rate of the clam Ruditapes philippinarum done in June 2004 at the IFREMER facility in Nantes exposed to highly toxic A. tamarense, and decreases in (France). Eastern oysters, C. virginica Gmelin, were stud- absorption eYciency of both clams (R. philippinarum) and ied in Milford, and PaciWc oysters, C. gigas Thunberg, were mussels (Perna viridis) coincident with toxin accumulation. studied in Nantes. Depending upon the bivalve species, morphological eVects of accumulated paralytic phycotoxins from A. tamarense Experimental oysters are seen in diVerent organs, especially in the digestive gland and the kidney, and less commonly in other organs, Eastern oysters, C. virginica, obtained from the F.M. such as the adductor muscle and the gonad (Lassus et al. Flower Hatchery (Oyster Bay, New York, USA), were used 1999; Bougrier et al. 2001; Choi et al. 2003). These diverse in the Milford experiment. Before being transferred to eVects of PSP-containing dinoXagellates on bivalve mol- experimental basins, oysters (ca. 30 mm shell height) were luscs suggest that other aspects of physiological processes conditioned in running, unWltered seawater (17°C) in the may also be aVected. Milford Laboratory. These oysters were not gametogenic. Invertebrates, including bivalves, have no acquired Triploid PaciWc oysters, C. gigas, used for the two immunity and are therefore, limited to an innate immune experiments in Nantes were obtained from a producer in Le response to pathogens, parasites, and physical injury (Jane- Croisic, France. These oysters were produced by the hatch- way 1994), which is mediated by chemical agents and spe- ery Vendée Naissain, and were grown in basins. The exper- cialized cells called hemocytes circulating throughout the imental oysters (9.1 § 1.6 g wet weight, ca. 60 mm shell body. Hemocytes recognize and attempt to eliminate non- height) were acclimated in basins containing running sea- self particles within an open vascular system and tissues, water for 6 days at the experimental temperature of but they do not “remember” a prior experience with a harm- 16 § 0.5°C and were transferred into experimental units ful agent and more eVectively protect an individual in sub- after being cleaned. Triploid oysters were chosen because, sequent exposures. Recent studies in the laboratory and in compared to diploids, they are thought to have faster the Weld (Hégaret et al. 2005a, b) of eVects of the harmful growth and better survival for aquaculture production (Nell dinoXagellate Prorocentrum minimum on bivalves were the 2002). Moreover, triploids do not produce gametes, which, Wrst to show eVects on hemocytes. These eVects included if present at the time of the experiment, could interfere with changes in morphological and functional parameters, such hemocyte analyses by contaminating hemolymph samples. as: concentrations and proportions of the diVerent hemo- cyte types, production of reactive oxygen species, phagocy- Algal cultures tosis or the percentage of dead hemocytes in eastern oysters (C. virginica) and northern bay scallops (A. irradians). The For the experiment in Milford, strains of A. fundyense bioactive compound or compounds in P. minimum respon- Balech (BF 2) and non-toxic T. weissXogii (Grun.) Fryxell sible for these eVects have not been identiWed. In the pres- et Hasle (TW) were obtained from the Milford Laboratory ent study, we evaluated hemocyte characteristics and microalgal culture collection. This strain of A. fundyense functions in: (1) C. virginica exposed to A. fundyense, two causes mortality in bay scallops after 24 h exposure to sta- species that co-occur on the east coast of north America, tionary-phase cells (Hégaret and Wikfors 2005a). Both BF and (2) C. gigas exposed to A. catenella, species that co- 2 and TW contain bacterial contaminants, but cultures were occur in western Europe. Experimental exposures used cul- managed aseptically to preclude contamination with additional tured algae and included additional variables, such as algal microbes. Strain TW was cultured in the “E + Si Medium” cell density, combination with non-toxic algae, and temper- seawater enrichment of Ukeles (1973) at a salinity of 15; ature. The two experiments were done independently and, BF 2 was cultured in E medium at 30. Carboy cultures, in part, for diVerent purposes. Thus, there were some grown under continuous illumination (300 Em¡2 s¡1) in a 123 Mar Biol (2007) 152:441–447 443 temperature controlled (18°C) room, were managed semi- T. weissXogii were monitored with a Coulter Multisizer and continuously, with half the volume harvested and replaced a microscope (using an Utermohl counting chamber) every aseptically every 7 days. morning during two experiments conducted at 12 or 18°C For the experiment in Nantes, strains of A. catenella with oysters pre-conditioned for 5 days to each tempera-
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