A comparison of the physiological responses, behaviour and biotransformation of paralytic shellfish poisoning toxins in a surf-clam (Paphies donacina) and the green-lipped mussel (Perna canaliculus)
Islay D. Marsden A D , Andrea M. Contreras A , Lincoln MacKenzie B and Murray H.G. Munro C
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand.
B Cawthron Institute, Private Bag 2, Nelson, New Zealand.
C Department of Chemistry, University of Canterbury, Private Bag 4800, Christchurch, New Zealand.
D Corresponding author. Email islay.marsden@canterbury.ac.nz
Marine and Freshwater Research 67(8) 1163-1174 https://doi.org/10.1071/MF14374
Submitted: 21 November 2014 Accepted: 30 March 2015 Published: 27 August 2015
Abstract
The accumulation of paralytic shellfish toxins (PSTs) in bivalves is species specific. We compared the physiological responses and the toxin profiles in tissues of the burrowing surf clam, Paphies donacina, and the green-lipped mussel, Perna canaliculus, exposed to the toxic dinoflagellate Alexandrium tamarense. Bivalves were supplied with the toxic algae for 10 days, then allowed a detoxification period of 8 days. Clearance rates of mussels and clams were similar when fed either with toxic A. tamarense or non-toxic A. margalefi. Byssus production in the mussel was inhibited and exhalent siphon activity in clams was erratic following exposure to A. tamarense. There were considerable differences in the toxic profile between the dinoflagellate A. tamarense, and tissues of the mussel and the surf clam, indicating that bioconversion of the PSTs had taken place. Toxin profiles of the tissues were both species and tissue specific. Following an 8-day detoxification period, total PSTs in mussels had fallen to safe concentrations below 50 µg per 100 g, whereas concentrations in clams remained high, with an average value greater than 600 µg STX di-HCL equivalents per 100 g. The results confirmed that mussels and clams are important monitoring organisms for toxic algal blooms and can be used to minimise the health risk of PSTs to humans.
Additional keywords: Alexandrium tamarense, bivalve behaviour and physiology, PST.
References
Abouabdellah, R., Taleb, H., Bennouna, A., Erler, K., Abdeghani, C., and Moukrim, A. (2008). Paralytic shellfish poisoning toxin profile of mussels Perna perna from southern Atlantic coasts of Morocco. Toxicon 51, 780–786.| Paralytic shellfish poisoning toxin profile of mussels Perna perna from southern Atlantic coasts of Morocco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlSju7w%3D&md5=438b3e6f14e982ed5201531cb5361f96CAS | 18237757PubMed |
Beitler, M., and Liston, J. (1990). Uptake and tissue distribution of PSP toxins in butter clams. In ‘Toxic Marine Phytoplankton’. (Eds E. Granéli, B. Sundström, L. Edler and D. Anderson.) pp. 257–262. (Elsevier: New York.)
Bricelj, V., and Shumway, S. (1998). Paralytic shellfish toxins in bivalve molluscs: occurence, transfer kinetics, and biotransformation. Reviews in Fisheries Science 6, 315–383.
| Paralytic shellfish toxins in bivalve molluscs: occurence, transfer kinetics, and biotransformation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtVCjt7s%3D&md5=e21f4dd79f28a11fcdc7a8f18d11a3edCAS |
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=d087f97ef6c1c8c2603d252efcf36d52CAS |
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=c5f2d80d84d61c8bbc48d4a0515aced8CAS |
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. (IOC of UNESCO: Paris.)
Bricelj, V. M., Ford, S. E., Lambert, C., Barbou, A., and Paillard, C. (2011). Effects of toxic Alexandrium tamarense on behaviour, hemocyte responses and development of brown ring disease in Manila clams. Marine Ecology Progress Series 430, 35–48.
| Effects of toxic Alexandrium tamarense on behaviour, hemocyte responses and development of brown ring disease in Manila clams.Crossref | GoogleScholarGoogle Scholar |
Campbell, A., McLeod, C., Pointon, A., Hudson, D., and Nicholls, C. (2013). Review of the 2012 paralytic shellfish toxin event in Tasmania associated with the dinoflagellate alga Alexandrium tamarense. A SafeFish Review, FRDC Project 2012/060, Adelaide, June 2013. Available at http://www.frdc.com.au/research/Documents/Final_reports/2012-060-DLD.pdf [Verified 13 June 2015].
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.
Chen, C. C., and Chou, H. N. C. (2002). Fate of paralytic shellfish poisoning toxins in purple clam Hiatula rostrata, in outdoor culture and laboratory culture. Marine Pollution Bulletin 44, 733–738.
| Fate of paralytic shellfish poisoning toxins in purple clam Hiatula rostrata, in outdoor culture and laboratory culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtVSlu7w%3D&md5=546347e4656c4b716242cadad85d22e3CAS |
Choi, M., Hsieh, D., Lam, P., and Wang, W. (2003). Field depuration and biotransformation of paralytic shellfish toxins in scallop Chlamys nobilis and green-lipped mussel Perna viridis. Marine Biology 143, 927–934.
| Field depuration and biotransformation of paralytic shellfish toxins in scallop Chlamys nobilis and green-lipped mussel Perna viridis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovVKmsr0%3D&md5=0799a39f1cd21eb6c7d391c197491111CAS |
Contreras, A. M., Marsden, I. D., and Munro, M. H. G. (2012a). Effects of short-term exposure to paralytic shellfish toxins on clearance rates and toxin uptake in five species of New Zealand bivalve. Marine and Freshwater Research 63, 166–174.
| Effects of short-term exposure to paralytic shellfish toxins on clearance rates and toxin uptake in five species of New Zealand bivalve.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhsl2ntrg%3D&md5=692bb40590d224e9ea0c5511216219f9CAS |
Contreras, A. M., Marsden, I. D., and Munro, M. H. G. (2012b). Physiological effects and biotransformation of PSP toxins in the New Zealand scallop, Pecten novaezelandiae. Journal of Shellfish Research 31, 1151–1159.
| Physiological effects and biotransformation of PSP toxins in the New Zealand scallop, Pecten novaezelandiae.Crossref | GoogleScholarGoogle Scholar |
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 |
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=8b5b93a25e013d11e89bf3a536e9584cCAS |
Goldberg, E. D., Koide, M., Hodge, V., Flegal, A. R., and Martin, J. (1983). US mussel watch: 1977–1978 results on trace metals and radionuclides. Estuarine, Coastal and Shelf Science 16, 69–93.
| US mussel watch: 1977–1978 results on trace metals and radionuclides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhs1Kmurk%3D&md5=fea01c4687bb37450f9848bbeabc2a1aCAS |
Guillard, L. (1975). Culture of phytoplankton for feeding marine marine invertebrates. In ‘Culture of Marine Invertebrate Animals’. (Eds W. Smith, M. Chaney.) pp. 29–60. (Plenum Press: New York.)
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 |
Hallegraeff, G. (2010). Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. Journal of Phycology 46, 220–235.
| Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvF2rur0%3D&md5=1327f340161b14abbec9248f356593d1CAS |
Hégaret, H., Wikfors, G. H., and Shumway, S. E. (2007). Diverse feeding responses of five species of bivalve mollusc when exposed to three species of harmful algae. Journal of Shellfish Research 26, 549–559.
| Diverse feeding responses of five species of bivalve mollusc when exposed to three species of harmful algae.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=9bce9996a62aa2a06694718a9f47f12bCAS | 11600155PubMed |
Jaime, E., Gerdts, G., and Luckas, B. (2007). In vitro transformation of PSP toxins by different shellfish tissues. Harmful Algae 6, 308–316.
| In vitro transformation of PSP toxins by different shellfish tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlWns74%3D&md5=bdbaeafe7eaeee20b36f3b08c301592eCAS |
Jester, R., Rhodes, L., and Beuzenberg, V. (2009). Uptake of paralytic shellfish poisoning and spirolide toxins by paddle crabs (Ovalipes catharus) via a bivalve vector. Harmful Algae 8, 369–376.
| Uptake of paralytic shellfish poisoning and spirolide toxins by paddle crabs (Ovalipes catharus) via a bivalve vector.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivFymt7s%3D&md5=a31af6a881dd4e08e34b3f04cfb256e4CAS |
John, U., Litaker, R. W., Montresor, M., Murray, S., Brosnahan, M. L., and Anderson, D. M. (2014). Formal revision of the Alexandrium species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular based classification. Protist 165, 779–804.
| Formal revision of the Alexandrium species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular based classification.Crossref | GoogleScholarGoogle Scholar | 25460230PubMed |
Kimbrough, K. L., Johnson, W. E., Lauenstein, G. G., Christensen, J. D., and Apeti, D. A. (2008). Mussel Watch Program. An assessment of two decades of contaminant monitoring in the nation’s coastal zone. NOAA National Status & Trends, NOAA Technical Memorandum NOS NCCOS 74, Silver Spring, MD. Available at http://ccma.nos.noaa.gov/publications/MWTwoDecades.pdf [Verified 20 August 2015].
Kwong, R. W., Lam, P., and Yu, P. (2006). The uptake, distribution and elimination of paralytic shellfish toxins in mussels and fish exposed to toxic dinoflagellates. Aquatic Toxicology 80, 82–91.
| The uptake, distribution and elimination of paralytic shellfish toxins in mussels and fish exposed to toxic dinoflagellates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvV2ms78%3D&md5=9d1a672fbfa098dea8bde79c2923f3cbCAS | 16959334PubMed |
Landsberg, J. H. (2002). The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science 10, 113–390.
| The effects of harmful algal blooms on aquatic organisms.Crossref | GoogleScholarGoogle Scholar |
Lesser, M., and Shumway, S. E. (1993). Effects of toxic dinoflagellates on clearance rates and survival in juvenile bivalve molluscs. Journal of Shellfish Research 12, 377–381.
Li, S., Wang, W., and Hsieh, D. (2002). Effects of toxic dinoflagellate Alexandrium tamarense on the energy budgets and growth of two marine bivalves. Marine Environmental Research 53, 145–160.
| Effects of toxic dinoflagellate Alexandrium tamarense on the energy budgets and growth of two marine bivalves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovVert70%3D&md5=2d885370d18f7508aa5bf6908012caf0CAS | 11829010PubMed |
Lilly, E. L., Halanych, K. M., and Anderson, D. M. (2007). Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae). Journal of Phycology 43, 1329–1338.
| Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltlSru7o%3D&md5=898ea74b372cfc4f6b934b17b93e71a1CAS |
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=e95cedfe2a072237089bb4633ae234d1CAS | 17805834PubMed |
MacDonald, B., Bacona, G., and Ward, J. (1998). Physiological responses of infaunal (Mya arenaria) and epifaunal (Placopecten magellanicus) bivalves to variations in the concentration and quality of suspended particles II. Absorption efficiency and scope for growth. Journal of Experimental Marine Biology and Ecology 219, 127–141.
| Physiological responses of infaunal (Mya arenaria) and epifaunal (Placopecten magellanicus) bivalves to variations in the concentration and quality of suspended particles II. Absorption efficiency and scope for growth.Crossref | GoogleScholarGoogle Scholar |
MacKenzie, A. L. (2014). The risk to New Zealand shellfish aquaculture from paralytic shellfish poisoning (PSP) toxins. New Zealand Journal of Marine and Freshwater Research 48, 430–465.
| The risk to New Zealand shellfish aquaculture from paralytic shellfish poisoning (PSP) toxins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFaktbzO&md5=683192043d7c916f879f195ee53b5926CAS |
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, A.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=984b1969b8e21b9894df8246c1239c7eCAS |
MacKenzie, A. L., Knight, B., and Harwood, T. (2014). New Zealand paralytic shellfish poisoning update: 2014. Cawthron Report 2526 prepared for the Ministry for Primary Industries, Food Safety. Cawthron Institute, Nelson, New Zealand.
MacQuarrie, S. P., and Bricelj, V. M. (2008). Behavioural and physiological responses to PSP toxins in Mya arenaria populations in relation to previous exposure to red tides. Marine Ecology Progress Series 366, 59–74.
| Behavioural and physiological responses to PSP toxins in Mya arenaria populations in relation to previous exposure to red tides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Klur%2FJ&md5=7f8bf1b1f2c0f431e53c2713ad576d22CAS |
Marsden, I. D. (1999). Habitat related adaptations in feeding and respiration of a burrowing surf clam Paphies donacina from an exposed sand beach in New Zealand. Hydrobiologia 405, 179–188.
| Habitat related adaptations in feeding and respiration of a burrowing surf clam Paphies donacina from an exposed sand beach in New Zealand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtVWgtLo%3D&md5=9f23bf6ad1b3259d14ea02b86ebc373cCAS |
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=156db8a5d6d63c12eee3001daa19b951CAS |
May, S. P., Burkholder, J. M., Shumway, S. E., Hégerat, H., and Wikfors, G. H. (2010). Effects of the toxic dinoflagellate Alexandrium monilatum on survival, grazing and behavioural response of three ecologically important bivalve molluscs. Harmful Algae 9, 281–293.
| Effects of the toxic dinoflagellate Alexandrium monilatum on survival, grazing and behavioural response of three ecologically important bivalve molluscs.Crossref | GoogleScholarGoogle Scholar |
Moroño, A., Franco, J., Miranda, M., Reyero, M. I., and Blanco, J. (2001). The effect of mussel size, temperature, seston volume, food quality and volume-specific toxin concentration on the uptake rate of PSP toxins by mussels (Mytilus galloprovincialis) Lmk. Journal of Experimental Marine Biology and Ecology 257, 117–132.
| The effect of mussel size, temperature, seston volume, food quality and volume-specific toxin concentration on the uptake rate of PSP toxins by mussels (Mytilus galloprovincialis) Lmk.Crossref | GoogleScholarGoogle Scholar | 11165303PubMed |
Navarro, J. M., and Contreras, A. M. (2010). An integrative response by Mytilus chilensis to the toxic dinoflagellate Alexandrium catenella. Marine Biology 157, 1967–1974.
| An integrative response by Mytilus chilensis to the toxic dinoflagellate Alexandrium catenella.Crossref | GoogleScholarGoogle Scholar |
Navarro, J., Contreras, A., and Chaparro, O. (2008). Short-term feeding response of the mussel Mytilus chilensis exposed to diets containing the toxic dinoflagellate Alexandrium catenella. Revista Chilena de Historia Natural 81, 41–49.
| Short-term feeding response of the mussel Mytilus chilensis exposed to diets containing the toxic dinoflagellate 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 |
Oikawa, H., Matsuyama, Y., Satomi, M., and Yano, Y. (2008). Accumulation and paralytic shellfish poisoning toxin by the swimming crab Charybdid japonica, in Kure Bay, Hiroshima Prefecture. Fisheries Science 74, 1180–1186.
| Accumulation and paralytic shellfish poisoning toxin by the swimming crab Charybdid japonica, in Kure Bay, Hiroshima Prefecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12itbjI&md5=e75bd79db4adb389e08d11c10b449743CAS |
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’, 18–22 October 1993, Nantes, France. (Ed P. Lassus.) pp. 475–480. (Lavoisier: Paris.)
Oshima, Y., Sugino, K., Itakura, H., Hirota, M., and Yasumoto, T. (1990). Comparative studies on paralytic shellfish toxin profile of dinoflagellates and bivalves. In ‘Toxin Marine Phytoplankton’. (Eds E. Granéli, B. Sundström, L. Edler and D. Anderson.) pp. 391–396. (Elsevier: New York.)
Quale, D. B. (1969). Paralytic shellfish poisoning in British Columbia. Bulletin, Fisheries Research Board Canada 168, 1–68.
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=2f3a02086e3a6352a80688ceabd9c575CAS | 18567305PubMed |
Sagou, R., Amanhir, R., Taleb, H., Vale, P., Blaghen, M., and Loutfi, M. (2005). Comparative study on differential accumulation of PSP toxins between cockle (Acanthocardia tuberculatum) and sweet clam (Callista chione). Toxicon 46, 612–618.
| Comparative study on differential accumulation of PSP toxins between cockle (Acanthocardia tuberculatum) and sweet clam (Callista chione).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFSitrzL&md5=608b6599de0f70f6875f476d5d1a3013CAS | 16168451PubMed |
Scholin, C. A., Hallegraeff, G. M., and Anderson, D. M. (1995). Molecular evolution of the Alexandrium tamarense ‘species complex’ (Dinophyceae): dispersal in the North American and West Pacific regions. Phycologia 34, 472–485.
| Molecular evolution of the Alexandrium tamarense ‘species complex’ (Dinophyceae): dispersal in the North American and West Pacific regions.Crossref | GoogleScholarGoogle Scholar |
Shumway, S. E. (1990). A review of the effects of algal blooms on shellfish and aquaculture. Journal of the World Aquaculture Society 21, 65–104.
| A review of the effects of algal blooms on shellfish and aquaculture.Crossref | GoogleScholarGoogle Scholar |
Shumway, S. E. (2011). ‘Shellfish Aquaculture and the Environment.’ (Wiley: Hoboken, NJ, USA.)
Shumway, S., and Cucci, T. (1987). The effects of the toxic dinoflagellate Protogonyaulax tamarensis on the feeding and behaviour of bivalve molluscs. Aquatic Toxicology 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=62170aa1d6b666080cf173f59158203eCAS | 7952949PubMed |
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. Fernandez and T. Wyatt.) pp. 437–440. (Xunta de Galicia: Galicia, Spain; and IOC of UNESCO: Paris.)
Snedecor, G. W., and Cochran, W. G. (1989). ‘Statistical Methods’, 8th edn. (Iowa State University Press: Ames, IA, USA.)
Solórzano, L. (1969). Determination of ammonia in natural waters by the phenolhypochlorite method. Limnology and Oceanography 14, 799–801.
| Determination of ammonia in natural waters by the phenolhypochlorite method.Crossref | GoogleScholarGoogle Scholar |
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=c3bf55009c8157607cfc97522faa0931CAS | 6882435PubMed |
Thorin, S., Bourdages, H., and Vincent, B. (1998). Study of siphon activity in Mya arenaria (L.) in the intertidal zone by means of an underwater video camera. Journal of Experimental Marine Biology and Ecology 224, 205–224.
| Study of siphon activity in Mya arenaria (L.) in the intertidal zone by means of an underwater video camera.Crossref | GoogleScholarGoogle Scholar |
Tran, D., Haberkorn, H., Soudant, P., Ciret, P., and Mssabuau, J.-C. (2010). Behavioural responses of Crassostrea gigas exposed to the harmful algae Alexandrium minutum. Aquaculture 298, 338–345.
| Behavioural 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=97b32e926cdb3522ed6338ded1c5d6efCAS | 5072092PubMed |
Wang, Z.-H., Nie, X.-P., Jiang, S.-J., Zhao, J.-G., Cao, Y., Zhang, Y.-J., and Wang, D.-Z. (2011). Source and profile of paralytic shellfish poisoning toxins in shellfish in Daya Bay, South China Sea. Marine Environmental Research 72, 53–59.
| Source and profile of paralytic shellfish poisoning toxins in shellfish in Daya Bay, South China Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXps1ylu7o%3D&md5=32589109af9aa4acf27a043e912475c8CAS | 21658755PubMed |
