Effects of the estuarine dinoflagellate Pfiesteria shumwayae (Dinophyceae) on survival and grazing activity of several shellfish species

Shumway, Sandra E.; Burkholder, JoAnn M.; Springer, Jeffrey

doi:10.1016/j.hal.2006.04.013

Cited by 47 publications

(38 citation statements)

References 66 publications

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“…Springer et al (2002) demonstrated the passage of intact cysts of toxic Pfiesteria piscicida Steidinger et Burkholder though the digestive tract of oysters and their ability to recover from the feces within 24 h of gut passage, yielding viable flagellated cells. Toxic strains of the closely related species Pfiesteria shumwayae Glasgow et Burkholder showed the same, although more limited, capability in oysters, scallops, mussels and clams (Shumway et al 2006). Thus, based upon previous studies (Bardouil et al 1993, Bricelj et al 1993, Laabir & Gentien 1999, Bauder & Cembella 2000, Li et al 2001, Springer et al 2002 and our preliminary observations, it appears likely that transplanted bivalve molluscs could introduce HABs into new areas; however, the relative risk associated with different bivalve and HAB species remains poorly understood.…”

Section: Introductionmentioning

confidence: 78%

Potential transport of harmful algae via relocation of bivalve molluscs

Hégaret¹,

Shumway²,

Wikfors³

et al. 2008

Mar. Ecol. Prog. Ser.

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Aquaculture and restoration activities with bivalve molluscs often involve moving individuals from one body of water to another. Our study tests the hypothesis that harmful algae ingested by source populations of shellfish can be introduced into new environments by means of these shellfish relocations. Cultures of several harmful algal strains, including Prorocentrum minimum, Alexandrium fundyense, Heterosigma akashiwo, Aureococcus anophagefferens, Karenia mikimotoi and Alexandrium monilatum, were fed to various species of bivalve molluscs, Crassostrea virginica, Argopecten irradians irradians, Mercenaria mercenaria, Mytilus edulis, Mya arenaria, Venerupis philippinarum and Perna viridis, to assess the ability of the algal cells to pass intact though the digestive tracts of the shellfish and subsequently multiply in number. Ten individuals of each shellfish species were exposed for 2 d to a simulated harmful algal bloom at a natural bloom concentration. The shellfish were removed after exposure, and maintained for 2 further days in ultra-filtered seawater. Biodeposits (feces) were collected after 24 and 48 additional hours, and observed under light microscopy for the presence or absence of intact, potentially viable algal cells or temporary cysts. Subsamples of biodeposits were transferred into both algal culture medium and filtered seawater and monitored for algal growth. Intact cells of most harmful algal species tested were seen in biodeposits. Generally, harmful algae from the biodeposits collected in the first 24 h after transfer re-established growing populations, but algae could less often be recovered from the biodeposits collected after 48 h. These data provide evidence that transplanted bivalve molluscs may be vectors for the transport of harmful algae and that a short holding period in water without algae may mitigate this risk. Further, preliminary results indicate that emersion may also serve to mitigate the risk of transport.

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Section: Introductionmentioning

confidence: 78%

Potential transport of harmful algae via relocation of bivalve molluscs

Hégaret¹,

Shumway²,

Wikfors³

et al. 2008

Mar. Ecol. Prog. Ser.

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“…Contrastingly, in vivo exposure of C. virginica and C. gigas to A. fundyense and A. minutum, respectively, did not induce immunosuppression nor toxicity (Hégaret et al 2007b;Haberkorn et al 2010b). Temporary cysts of A. fundyense and A. minutum have been observed in the stomach, digestive gland and biodeposits of bivalves (Shumway et al 2006;Galimany et al 2008b;Hégaret et al 2008b;Haberkorn et al 2010b), indicating that the algal cells may transform into cysts as they pass through the digestive system. The release of toxic substances might then be reduced, causing less effect on bivalve tissues and haemocytes during in vivo exposures compared with in vitro experiments.…”

Section: Effect Of Harmful Algal Cells On Bivalve Haemocytes and Theimentioning

confidence: 93%

In vitro interactions between several species of harmful algae and haemocytes of bivalve molluscs

et al. 2011

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Harmful algal blooms (HABs) can have both lethal and sublethal impacts on shellfish. To understand the possible roles of haemocytes in bivalve immune responses to HABs and how the algae are affected by these cells (haemocytes), in vitro tests between cultured harmful algal species and haemocytes of the northern quahog (= hard clam) Mercenaria mercenaria, the soft-shell clam Mya arenaria, the eastern and Pacific oysters Crassostrea virginica and Crassostrea gigas and the Manila clam Ruditapes philippinarum were carried out. Within their respective ranges of distribution, these shellfish species can experience blooms of several HAB species, including Prorocentrum minimum, Heterosigma akashiwo, Alexandrium fundyense, Alexandrium minutum and Karenia spp.; thus, these algal species were chosen for testing. Possible differences in haemocyte variables attributable to harmful algae and also effects of haemolymph and haemocytes on the algae themselves were measured. Using microscopic and flow cytometric observations, changes were measured in haemocytes, including cell morphology, mortality, phagocytosis, adhesion and reactive oxygen species (ROS) production, as well as changes in the physiology and the characteristics of the algal cells, including mortality, size, internal complexity and chlorophyll fluorescence. These experiments suggest different effects of the several species of harmful algae upon bivalve haemocytes. Some harmful algae act as immunostimulants, whereas others are immunosuppressive. P. minimum appears to activate haemocytes, but the other harmful algal species tested seem to cause a suppression of immune functions, generally consisting of decreases in phagocytosis, production of ROS and cell adhesion and besides cause an increase in the percentage of dead haemocytes, which could be attributable to the action of chemical toxins. Microalgal cells exposed to shellfish haemolymph generally showed evidence of algal degradation, e.g. loss of chlorophyll fluorescence and modification of cell shape. Thus, in vitro tests allow a better understanding of the role of the haemocytes and the haemolymph in the defence mechanisms protecting molluscan shellfish from harmful algal cells and could also be further developed to estimate the effects of HABs on bivalve molluscs in vivo.

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“…In general, mixotrophic dinoflagellates differ from most grazers in the marine food web by having a large optimal prey size, often corresponding to their own size (Hansen and Calado, 1999). Tube feeding enables dinoflagellates to feed on very large prey (Berge et al, 2008a) and a few primarily heterotrophic dinoflagellates, generally not forming mono-specific high-density blooms, have been reported to ingest rotifers, nauplius and bivalve larvae, nematodes and even finfish by the use of a feeding tube (Calado and Moestrup, 1997;Vogelbein et al, 2002;Shumway et al, 2006;Jeong et al, 2010). This includes ingestion of fish in the primarily heterotrophic Pfiesteria piscicida, which can retain functional plastids from cryptophyte prey and thereby become mixotrophic (Burkholder and Glasgow 1997;Lewitus et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

Marine microalgae attack and feed on metazoans

et al. 2012

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Free-living microalgae from the dinoflagellate genus Karlodinium are known to form massive blooms in eutrophic coastal waters worldwide and are often associated with fish kills. Natural bloom populations, recently shown to consist of the two mixotrophic and toxic species Karlodinium armiger and Karlodinium veneficum have caused fast paralysis and mortality of finfish and copepods in the laboratory, and have been associated with reduced metazooplankton biomass in-situ. Here we show that a strain of K. armiger (K-0688) immobilises the common marine copepod Acartia tonsa in a densitydependent manner and collectively ingests the grazer to promote its own growth rate. In contrast, four strains of K. veneficum did not attack or affect the motility and survival of the copepods. Copepod immobilisation by the K. armiger strain was fast (within 15 min) and caused by attacks of swarming cells, likely through the transfer and action of a highly potent but uncharacterised neurotoxin. The copepods grazed and reproduced on a diet of K. armiger at densities below 1000 cells ml, but above 3500 cells ml À 1 the mixotrophic dinoflagellates immobilised, fed on and killed the copepods. Switching the trophic role of the microalgae from prey to predator of copepods couples population growth to reduced grazing pressure, promoting the persistence of blooms at high densities. K. armiger also fed on three other metazoan organisms offered, suggesting that active predation by mixotrophic dinoflagellates may be directly involved in causing mortalities at several trophic levels in the marine food web.

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Effects of the estuarine dinoflagellate Pfiesteria shumwayae (Dinophyceae) on survival and grazing activity of several shellfish species

Cited by 47 publications

References 66 publications

Potential transport of harmful algae via relocation of bivalve molluscs

Potential transport of harmful algae via relocation of bivalve molluscs

In vitro interactions between several species of harmful algae and haemocytes of bivalve molluscs

Marine microalgae attack and feed on metazoans

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