Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Effects of short-term exposure to paralytic shellfish toxins on clearance rates and toxin uptake in five species of New Zealand bivalve

Andrea M. Contreras A B E , Islay D. Marsden C and Murray H. G. Munro D
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, University of Canterbury, Christchurch, New Zealand.

B Present address: IFREMER, Laboratoire Phycotoxines, Nantes, France.

C School of Biological Sciences, University of Canterbury, Christchurch, New Zealand.

D Department of Chemistry, University of Canterbury, Christchurch, New Zealand.

E Corresponding author. Email: andrea.contrerasg@gmail.com

Marine and Freshwater Research 63(2) 166-174 https://doi.org/10.1071/MF11173
Submitted: 3 August 2011  Accepted: 10 October 2011   Published: 28 November 2011

Abstract

Algal blooms produced by toxic dinoflagellates have increased worldwide, resulting in economic losses to aquaculture and fisheries. Bivalve species differ in their ability to feed on toxin-producing dinoflagellates and this could result in differences in toxin accumulation among species. In New Zealand, the effects of paralytic shellfish poisoning (PSP) toxins on the physiology of bivalve molluscs are relatively unknown. We hypothesised that the feeding responses of five New Zealand bivalve species exposed to PSP-toxic dinoflagellates would be species-specific, affecting their accumulation of toxins. Each species was exposed to toxic and non-toxic species of Alexandrium spp. and clearance rate used as an index of sensitivity to PSP toxins. Clearance rates for the mussel Perna canaliculus and the clam Dosinia anus were unaffected by the presence of toxic dinoflagellates, whereas the rate in the scallop Pecten novaezelandiae decreased significantly. There were variable results for the clam Paphies donacina and the oyster Ostrea chilensis. Species-specific biotransformation of PSP-toxins had taken place in the bivalve tissues. We conclude that the rate of accumulation of PSP toxins in the tissues of the bivalve species was influenced by their feeding behaviour and the different chemical processes that had taken place in their tissues.

Additional keywords: biotransformation, decarbamoylation, Dosinia anus, epimerisation, Ostrea chilensis, Paphies donacina, Pecten novaezelandiae, Perna canaliculus.


References

Basti, L., Nagai, K., Shimasaki, Y., Oshima, Y., Honjo, T., and Segawa, S. (2009). Effects of the toxic dinoflagellate Heterocapsa circularisquama on the valve movement behaviour of the Manila clam Ruditapes philippinarum. Aquaculture 291, 41–47.
Effects of the toxic dinoflagellate Heterocapsa circularisquama on the valve movement behaviour of the Manila clam Ruditapes philippinarum.Crossref | GoogleScholarGoogle Scholar |

Bricelj, V., and Shumway, S. (1998). Paralytic shellfish toxins in bivalve molluscs: occurrence, transfer kinetics, and biotransformation. Reviews in Fisheries Science 6, 315–383.
Paralytic shellfish toxins in bivalve molluscs: occurrence, transfer kinetics, and biotransformation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtVCjt7s%3D&md5=d4b599f63e536c2bd855c92db3df68b7CAS |

Bricelj, V., Lee, J., Cembella, A., and Anderson, D. (1990). Uptake kinetics of paralytic shellfish toxins from the dinoflagellate Alexandrium fundyense in the mussel Mytilus edulis. Marine Ecology Progress Series 63, 177–188.
Uptake kinetics of paralytic shellfish toxins from the dinoflagellate Alexandrium fundyense in the mussel Mytilus edulis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmtVKnsb8%3D&md5=3611387c753538c1ad5194a56992148dCAS |

Bricelj, V., Lee, J., and Cembella, A. (1991). Influence of dinoflagellate cell toxicity on uptake and loss of paralytic shellfish toxins in the northern quahog, Mercenaria mercenaria. Marine Ecology Progress Series 74, 33–46.
Influence of dinoflagellate cell toxicity on uptake and loss of paralytic shellfish toxins in the northern quahog, Mercenaria mercenaria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmt1yksbs%3D&md5=2c55a812a557268bed1b23cb2fe77c70CAS |

Bricelj, V., Cembella, A., Laby, D., Shumway, S., and Cucci, T. (1996). Comparative physiological and behavioral responses to PSP toxins in two bivalve molluscs, the softshell clam, Mya arenaria, and surfclam, Spisula solidissima. In ‘Harmful and Toxic Algal Blooms’. (Eds T. Yasumoto, Y. Oshima and Y. Fukuyo.) pp. 405–408. (UNESCO: Paris.)

Bricelj, V., Ford, S., Lambert, C., Barbou, A., and Paillard, C. (2011). Effects of toxic Alexandrium tamarense on behavior, hemocyte responses and development of brown ring disease in Manila clams. Marine Ecology Progress Series 430, 35–48.
Effects of toxic Alexandrium tamarense on behavior, hemocyte responses and development of brown ring disease in Manila clams.Crossref | GoogleScholarGoogle Scholar |

Cembella, A., Shumway, S., and Lewis, N. (1993). Anatomical distribution and spatio-temporal variation in paralytic shellfish toxin composition in two bivalve species from the Gulf of Maine. Journal of Shellfish Research 12, 389–403.

Cembella, A., Shumway, S., and Larocque, R. (1994). Sequestering and putative biotransformation of paralytic shellfish toxins by the sea scallop Placopecten magellanicus: seasonal and spatial scales in natural populations. Journal of Experimental Marine Biology and Ecology 180, 1–22.
Sequestering and putative biotransformation of paralytic shellfish toxins by the sea scallop Placopecten magellanicus: seasonal and spatial scales in natural populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmsFWksbg%3D&md5=e6c6aa02942126b0cfaf1f9a9400618eCAS |

Coughlan, J. (1969). The estimation of filtering rate from the clearance of suspensions. Marine Biology 2, 356–358.
The estimation of filtering rate from the clearance of suspensions.Crossref | GoogleScholarGoogle Scholar |

Estrada, N., Lagos, N., Garcia, C., Maeda-Martinez, A., and Ascencio, F. (2007). Effects of the toxic dinoflagellate Gymnodinium catenatum on uptake and fate of paralytic shellfish poisons in the Pacific giant lions-paw scallop Nodipecten subnodosus. Marine Biology 151, 1205–1214.
Effects of the toxic dinoflagellate Gymnodinium catenatum on uptake and fate of paralytic shellfish poisons in the Pacific giant lions-paw scallop Nodipecten subnodosus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXks1ahtLk%3D&md5=a184f47cffa95edc07dbe48b95ec27e4CAS |

Fast, M., Cembella, A., and Ross, N. (2006). In vitro transformation of paralytic shellfish toxins in the clams Mya arenaria and Protothaca staminea. Harmful Algae 5, 79–90.
In vitro transformation of paralytic shellfish toxins in the clams Mya arenaria and Protothaca staminea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWlu7g%3D&md5=75b9085df7a6fa0b0d176f714895577aCAS |

Guillard, R. (1975). Culture of phytoplankton for feeding marine invertebrates. In ‘Culture of Marine Invertebrate Animals’. (Eds W. Smith and M. Chanley.) pp. 29–60. (Plenum Press: New York.)

Haberkorn, H., Tran, D., Massabuau, J. C., Ciret, P., Savar, V., and Soudant, P. (2011). Relationship between valve activity, microalgae concentration in the water and toxin accumulation in the digestive gland of the Pacific oyster Crassostrea gigas exposed to Alexandrium minutum. Marine Pollution Bulletin 62, 1191–1197.
Relationship between valve activity, microalgae concentration in the water and toxin accumulation in the digestive gland of the Pacific oyster Crassostrea gigas exposed to Alexandrium minutum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVCntr0%3D&md5=90aa7f53f629bfae29ed9467c8d81853CAS |

Hallegraeff, G. (1993). A review of harmful algae blooms and their apparent global increase. Phycologia 32, 79–99.
A review of harmful algae blooms and their apparent global increase.Crossref | GoogleScholarGoogle Scholar |

Ichimi, K., Suzuki, T., and Yamasaki, M. (2001). Non-selective retention of PSP toxins by the mussel Mytilus galloprovincialis fed with the toxic dinoflagellate Alexandrium tamarense. Toxicon 39, 1917–1921.
Non-selective retention of PSP toxins by the mussel Mytilus galloprovincialis fed with the toxic dinoflagellate Alexandrium tamarense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntlKhtb0%3D&md5=f8bc5b59583a8458fb92824224846dfbCAS |

Jaime, E., Gunnar, G., and Bernd, L. (2007). In vitro transformation of PSP toxins by different shellfish tissue. Harmful Algae 6, 308–316.
In vitro transformation of PSP toxins by different shellfish tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlWns74%3D&md5=26a2dff8f65ade7ce7d98b3fbd6119caCAS |

Jørgensen, C. (1976). Growth efficiencies and factors controlling size in some mytilid bivalves, especially. Mytilus edulis L.: a review and interpretation. Ophelia 15, 175–192.

Kvitek, R., and Beitler, M. (1991). Relative insensitivity of butter clam neurons to saxitoxin: a pre-adaption for sequestering paralytic shellfish poisoning toxins as a chemical defense. Marine Ecology Progress Series 69, 47–54.
Relative insensitivity of butter clam neurons to saxitoxin: a pre-adaption for sequestering paralytic shellfish poisoning toxins as a chemical defense.Crossref | GoogleScholarGoogle Scholar |

Lassus, P., Fremy, J., Ledoux, M., Bardouil, M., and Bohec, M. (1989). Patterns of experimental contamination by Protogonyaulax tamarensis in some French commercial shellfish. Toxicon 27, 1313–1321.
Patterns of experimental contamination by Protogonyaulax tamarensis in some French commercial shellfish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXptlGkug%3D%3D&md5=d4ea66cd7687a38eace5666334d3305cCAS |

Lassus, P., Wildish, D., Bardouil, M., Martin, J., Bohec, M., and Bougrier, S. (1996). Echophysiological study of toxic Alexandrium spp. effects on the oyster Crassostrea gigas. In ‘Harmful and Toxic Algal Blooms’. (Eds T. Yasumoto, Y. Oshima and Y. Fukuyo.) pp. 409–412. (UNESCO: Paris.)

Lassus, P., Amzil, Z., Baron, R., Séchet, V., Barillé, L., Abadie, E., Bardouil, M., Sibat, M., Truquet, P., Bereard, J., and Guéguen, M. (2007). Modelling the accumulation of PSP toxins in Thau Lagoon oysters (Crassostrea gigas) from trials using mixed cultures of Alexandrium catenella and Thalassiosira weissflogii. Aquatic Living Resources 20, 59–67.
Modelling the accumulation of PSP toxins in Thau Lagoon oysters (Crassostrea gigas) from trials using mixed cultures of Alexandrium catenella and Thalassiosira weissflogii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1Krsb8%3D&md5=9366c226052b9baa530d5ec90863cea5CAS |

Lee, J. (1993). The kinetics of PSP toxin transfer from the toxic dinoflagellate, Alexandrium spp. to two bivalve mollusc species, Mytilus edulis and Mercenaria mercenaria. M.Sci. Thesis, University of New York, New York.

Loeblich, A. R., and Smith, V. E. (1968). Chloroplast pigments of the marine dinoflagellate Gyrodinium resplendens. Lipids 3, 5–13.
Chloroplast pigments of the marine dinoflagellate Gyrodinium resplendens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXkslensA%3D%3D&md5=2d6b6d8eba6b9015e2256a4017186d45CAS |

Luckenbach, M., Sellner, K. G., Shumway, S. E., and Greene, K. (1993). Effects of two bloom-forming dinoflagellates, Prorocentrum minimum and Gyrodinium uncatenum, on the growth and survival of the eastern oyster, Crassostrea virginica (Gmelin 1791). Journal of Shellfish Research 12, 411–415.

MacKenzie, L., White, D., and Adamson, J. (1996). Temporal variation and tissue localization of paralytic shellfish toxins in the New Zealand tuatua (surfclam), Paphies subtriangulata. Journal of Shellfish Research 15, 735–740.

MacKenzie, L., de Salas, M., Adamson, J., and Beuzenberg, V. (2004). The dinoflagellate genus Alexandrium (Halim) in New Zealand coastal waters: comparative morphology, toxicity and molecular genetics. Harmful Algae 3, 71–92.
The dinoflagellate genus Alexandrium (Halim) in New Zealand coastal waters: comparative morphology, toxicity and molecular genetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhslGmsbc%3D&md5=7ed4b2c418f20db1667adfc85e7baf38CAS |

Marsden, I., and Shumway, S. (1992). Effects of the toxic dinoflagellate Alexandrium tamarense on the greenshell mussel Perna canaliculus. New Zealand Journal of Marine and Freshwater Research 26, 371–378.
Effects of the toxic dinoflagellate Alexandrium tamarense on the greenshell mussel Perna canaliculus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXit1Oqs78%3D&md5=e7e0d371541f0cc57c643b1f8cd0e257CAS |

Nagai, K., Honjo, T., Go, J., Yamashita, H., and Oh, S. J. (2006). Detecting the shellfish killer Heterocapsa circularisquama (Dinophyceae) by measuring bivalve valve activity with a Hall element sensor. Aquaculture 255, 395–401.
Detecting the shellfish killer Heterocapsa circularisquama (Dinophyceae) by measuring bivalve valve activity with a Hall element sensor.Crossref | GoogleScholarGoogle Scholar |

Navarro, J., and Contreras, A. (2010). An integrative response by Mytilus chilensis to the toxic dinofagellate Alexandrium catenella. Marine Biology 157, 1967–1974.
An integrative response by Mytilus chilensis to the toxic dinofagellate Alexandrium catenella.Crossref | GoogleScholarGoogle Scholar |

Navarro, J., Aguila, B., Machmar, F., Chaparro, O., and Contreras, A. (2011). Dynamic of intoxication and detoxification in juveniles of Mytilus chilensis (Bivalvia: Mytilidae) exposed to paralytic shellfish toxins. Aquatic Living Resources 24, 93–98.
Dynamic of intoxication and detoxification in juveniles of Mytilus chilensis (Bivalvia: Mytilidae) exposed to paralytic shellfish toxins.Crossref | GoogleScholarGoogle Scholar |

Newell, R. I. E. (1979). ‘Biology of Intertidal Animals.’ (Marine Ecological Surveys Ltd: Faversham, UK.)

Oshima, Y. (1995). Chemical and enzymatic transformation of paralytic shellfish toxins in marine organisms. In ‘Harmful Marine Algal Blooms: Proceedings of the Sixth International Conference on Toxic Marine Phytoplankton’. (Ed. P. Lassus.) pp. 475–480. (Lavoisier: Nantes, France.)

Oshima, Y., Sugino, K., Itakura, H., Hirota, M., and Yasumoto, T. (1990). Comparative studies on paralytic shellfish toxin profile of dinoflagellates and bivalves. In ‘Toxic Marine Phytoplankton’. (Eds E. Granéli, B. Sundström, L. Edler and D. Anderson.) pp. 391–396. (Elsevier: New York.)

Rodríguez Rodríguez, G., Villasante, S., and García Negro, M. (2011). Are red tides affecting economically the commercialization of the Galician (NW Spain) mussel farming? Marine Policy 35, 252–257.
Are red tides affecting economically the commercialization of the Galician (NW Spain) mussel farming?Crossref | GoogleScholarGoogle Scholar |

Rourke, W. A., Murphy, C. J., Pitcher, G., Van De Riet, J. M., Burns, B. G., Thomas, K. M., and Quilliam, M. A. (2008). Rapid postcolumn methodology for determination of paralytic shellfish toxins in shellfish tissue. Journal of AOAC International 91, 589–597.
| 1:CAS:528:DC%2BD1cXntlWqtLo%3D&md5=82c904561948a8ae126f1e9fbad1795dCAS |

Shumway, S., and Cucci, T. (1987). The effects of the toxic dinoflagellate Protogonyaulax tamarensis on the feeding and behaviour of bivalve molluscs. Aquatic Toxicology (Amsterdam, Netherlands) 10, 9–27.
The effects of the toxic dinoflagellate Protogonyaulax tamarensis on the feeding and behaviour of bivalve molluscs.Crossref | GoogleScholarGoogle Scholar |

Shumway, S., Cucci, T., Newell, R., and Yentsch, C. (1985). Particle selection, ingestion and absorption in filter feeding bivalves. Journal of Experimental Marine Biology and Ecology 91, 77–92.
Particle selection, ingestion and absorption in filter feeding bivalves.Crossref | GoogleScholarGoogle Scholar |

Shumway, S., Sherman-Caswell, S., and Hurst, J. (1988). Paralytic shellfish poisoning in Maine: monitoring a monster. Journal of Shellfish Research 7, 643–652.

Shumway, S., Barter, J., and Sherman-Caswell, S. (1990). Auditing the impact of toxic algal blooms in oysters. Environmental Auditor 2, 41–56.

Shumway, S., Sherman, S., Cembella, A., and Selvin, R. (1994). Accumulation of paralytic shellfish toxins by surfclams, Spisula solidissima (Dillwyn, 1987) in the Gulf of Maine: seasonal changes, distribution between tissues, and notes on feeding habits. Natural Toxins 2, 236–251.
Accumulation of paralytic shellfish toxins by surfclams, Spisula solidissima (Dillwyn, 1987) in the Gulf of Maine: seasonal changes, distribution between tissues, and notes on feeding habits.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M%2FktVOhtQ%3D%3D&md5=f40b6826dc68f639218ca84362bdcea8CAS |

Silvert, W., Bricelj, V., and Cembella, A. (1998). Dynamic modelling of PSP toxicity in the surfclam (Spisula solidissima): multicompartmental kinetics and biotransformation. In ‘Harmful Algae’. (Eds B. Reguera, J. Blanco, M. Fernández and T. Wyatt.) pp. 437–440. (Xunta de Galicia and UNESCO: Vigo, Spain.)

Snedecor, G. W., and Cochran, W. G. (1989). ‘Statistical Methods.’ 8th edn. (Blackwell: Ames, IA.)

Sullivan, J., Iwaoka, W., and Liston, J. (1983). Enzymatic transformation of PSP toxins in the littleneck clam (Protothaca staminea). Biochemical and Biophysical Research Communications 114, 465–472.
Enzymatic transformation of PSP toxins in the littleneck clam (Protothaca staminea).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXltF2lsro%3D&md5=200758928fd7981dcdd7bb8a01e97d78CAS |

Tran, D., Haberkorn, H., Soudant, P., Ciret, P., and Massabuau, J. C. (2010). Behavioral responses of Crassostrea gigas exposed to the harmful algae Alexandrium minutum. Aquaculture 298, 338–345.
Behavioral responses of Crassostrea gigas exposed to the harmful algae Alexandrium minutum.Crossref | GoogleScholarGoogle Scholar |

Twarog, B., Hidaka, T., and Yamaguchi, H. (1972). Resistance to tetrodotoxin and saxitoxin in nerves of bivalve molluscs. Toxicon 10, 273–278.
Resistance to tetrodotoxin and saxitoxin in nerves of bivalve molluscs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XksVCju7s%3D&md5=e3da7db9237c09dd37997608400c8a53CAS |

Widdows, J. (1978). Combined effects of body size, food concentration and season on the physiology of Mytilus edulis. Journal of the Marine Biological Association of the United Kingdom 58, 109–124.
Combined effects of body size, food concentration and season on the physiology of Mytilus edulis.Crossref | GoogleScholarGoogle Scholar |

Winter, J. E. (1978). A review of the knowledge of suspension-feeding in lamellibranchiate bivalves, with especial reference to artificial aquaculture systems. Aquaculture 13, 1–33.
A review of the knowledge of suspension-feeding in lamellibranchiate bivalves, with especial reference to artificial aquaculture systems.Crossref | GoogleScholarGoogle Scholar |