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Toxicity and histopathological effects of toxic dinoflagellate, Alexandrium catenella exudates on larvae of blue mussel, Mytilus galloprovincialis, and Pacific oyster, Crassostrea gigas
Corresponding Author(s) : Supono Supono
Jurnal Ilmiah Perikanan dan Kelautan, Vol. 12 No. 2 (2020): JURNAL ILMIAH PERIKANAN DAN KELAUTAN
Abstract
Highlight
- Toxicity and pathological effects of A. catenella were investigated on shellfish larvae
- Unfiltered exudates of A. catenella caused significant mortality of blue mussel larvae
- Application of 0.22 mm filtration on A. fundyense exudates potentially decrease the toxicity effects
- Pathological effects of A. catenella occurred as early as 3 h after exposure
- The prevalence and intensity of necrosis increased with exposure duration to A. catenella exudates
Abstract
Blooms of the toxic dinoflagellate Alexandrium catenella have affected shellfish industries globally due to their capacity to produce paralytic shellfish toxins(PST). This study aimed to investigate the toxicity effect of exudate A. catenella on larvae of blue mussel Mytilus galloprovincialis and Pacific oyster Crassostrea gigas and filtration methods to reduce the toxic effect. Blue mussel and Pacific oyster larvae were assessed their survival and histopathological changes after exposure to extracellular exudates of A. catenella ranging from 100 to 1,000 cells ml-1 . The results showed that exposure to exudate A. catenella caused significantly higher larval mortality (39 to 52%) than exposure to an equivalent biovolume of the nontoxic species, Tisochrysis lutea (33%) or unfed controls (17%). Filter-sterilization (0.22 µm) of exudates and activated carbon filtration decreased the mortality of Pacific oyster larvae to a level similar to controls (unfed), with the exception of the highest concentrations (600 and 1,000 cells ml-1 ) and mortality of bluemussel larvae mortality by 32% respectively. Blue mussel larvae exposed to exudate A. catenella showed pathological changes mainly in the stomach (digestive gland and style sac) as early as three hours after onset of exposure. The findings of this study suggest that early detection of blooms in the vicinity of mussel and Pacific oyster hatcheries and taking steps to mitigate their effects, is important to reduce the effects of A. catenella blooms on shellfish larval rearing.
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- Abi-Khalil, C., Lopez-Joven, C., Abadie, E., Savar, V., Amzil, Z., Laabir, M., & Rolland, J. L. (2016). Exposure to the paralytic shellfish toxin producer Alexandrium catenella increases the susceptibility of the oyster Crassostrea gigas to pathogenic vib- rios. Toxins, 8(1):24. https://doi.org/10.3390/tox- ins8010024
- Anderson, D. M., Alpermann, T. J., Cembella, A. D., Collos, Y., Masseret, E., & Montresor, M. (2012). The globally distributed Alexandrium: multifacet- ed roles in marine ecosystems and impacts on human health. Harmful Algae, 14:10-35. https://doi. org/10.1016/j.hal.2011.10.012
- Anderson, D. M., Hoagland, P., Kaoru, Y., & White, A. W. (2000). Estimated annual economic impacts from harmful algal blooms (HABs) in the United States. Technical Report. National Oceanic and Atmospheric Administration Norman OK Nation- al Severe Storms Lab :97 p.
- Anderson, D. M., Reguera, B., Pitcher, G. C., & Enevoldsen, H. O. (2010). The IOC international harmful algal bloom program: history and science impacts. Oceanography, 23(4):72-85.
- Basti, L., Endo, M., Segawa, S., Shumway, S. E., Tanaka, Y., & Nagai, S. (2016). Prevalence and intensity of pathologies induced by the toxic dinoflagellate, Heterocapsa circularisquama, in the Mediterranean mussel, Mytilus galloprovincialis. Aquatic Toxicology, 163:37-50. https://doi.org/10.1016/j. aquatox.2015.03.012
- Bolch, C. J. S., Harwood, T., Untari, L., Murray, S., Hallegraeff, G., & Turnbull, A. (2014, November). Al- exandrium tamarense Group I as the cause of PST on the east coast of Tasmania, Australia. 14th International Conference on Harmful Algae, Wellington New Zealand.
- Borcier, E., Morvezen, R., Boudry, P., Miner, P., Charrier, G., Laroche, J., & Hegaret, H. (2017). Effects of bioactive extracellular compounds and paralytic shellfish toxins produced by Alexandrium minutum on growth and behaviour of juvenile great scallops Pecten maximus. Aquatic Toxicology, 184, 142-154. https://doi.org/10.1016/j.aquatox.2017.01.009 Bricelj, V. M.,
- Bricelj, V. M., Lee, J. H., & Cembella, A. D. (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.
- Bricelj, V. M., Ford, S. E., Lambert, C., Barbou, A., & Paillard, C. (2011). Effects of toxic Alexandrium tamarense on behavior, hemocyte response and de- velopment of brown ring disease in Manila clams. Marine Ecology Progress Series, 430:35-48. https://doi.org/10.3354/meps09111
- Brown, C., & Tettelbach, L. P. (1988). Characterization of nonmotile Vibrio sp. pathogenic to larvae of Mercenaria mercenaria and Crassostrea virginica. Aquaculture, 74(3):195-204.
- Castrec, J., Hégaret, H., Huber, M., Le Grand, J., Huvet, A., Tallec, K., Boulais, M., Soudant, P., & Fabioux, C. (2020). The toxic dinoflagellate Alexandrium minutum impairs the performance of oyster embryos and larvae. Harmful Algae, 92: 101744. https:// doi.org/10.1016/0044-8486(88)90363-8
- Cembella, A., & John, U. (2006). Molecular physiology of toxin production and growth regulation in harmful algae. In: Granéli, E, Turner, J T (Eds.) Ecology of harmful algae (pp. 215-227). Springer.
- Contreras, A. M., Marsden, I. D., & Munro, M. H. (2012). 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(2):166-174. https:// doi.org/10.1071/MF11173
- Detree C., Núñez-Acuña, G., Roberts, S., & Gallardo-Escárate, C. (2016). Uncovering the Complex Transcriptome Response of Mytilus chilensis against Saxitoxin: Implications of Harmful Algal Blooms on Mussel Populations. PLoS One, 11(10): e0165231. https://doi.org/10.1371/journal. pone.0165231
- Feist, S., & Bucke, D. (1983). A double-embedding technique for processing larval oysters for light microscopy. Bulletin of the European Association of Fish Pathologists, 1-2.
- Galimany, E., Sunila, I., Hégaret, H., Ramon, M., & Wikfors, G. H. (2008). Experimental exposure of the blue mussel (Mytilus edulis, L.) to the toxic dinoflagellate Alexandrium catenella: Histopathology, immune responses, and recovery. Harmful Algae, 7(5):702-711. https://doi.org/10.1016/j. hal.2008.02.006
- Haberkorn, H., Lambert, C., Le Goí¯c, N. P., Moal, J., Sequet, M., Gueguen, M., Sunila, I., & Soudant, P. (2010). Effects of Alexandrium minutum exposure on nutrition related process and reproductive output in oyster Crassostrea gigas. Harmful Algae, 9(5):427-439. https://doi.org/10.1016/j.
- Hallegraeff, G. M. (2014). Harmful algae and their toxins: progress, paradoxes and paradigm shifts. In: G. P. Rossini (Ed.). Toxins and biologically active compounds from microalgae (pp. 4-20). CRC Press.
- Hallegraeff, G. M., Bolch, C. J. S., Condie, S., Dorantes-Aranda, J. J., Murray, S., Quinlan, R., Ruvindy, R., Turnbull, A., Ugalde, S., & Wilson, K. (2017). Unprecedented Alexandrium blooms in a previously low biotoxin risk area of Tasmania, Australia. In: Proceedings of the 17th International Conference on Harmful Algal Blooms. International Society for the Study of Harmful Algae and Intergovernmental Oceanographic Comission of UNESCO 2017.
- Hégaret, H., Wikfors, G. H., & 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(2):549-559. https://doi. org/10.2983/0730-8000 (2007) 26 [549:D- FROFS]2.0.CO;2
- Hoagland, P., Anderson, D. M., Kaoru, Y., & White, A. W. (2002). The economic effects of harmful algal blooms in the United States: estimates, as- sessment issues and information needs. Estuaries, 25(4):819-837.
- Jacobson, P. J., Farris, J. L., Neves, R., & Cherry, D. S. (1993). Use of neutral red to assess survival of juvenile freshwater mussels (Bivalvia: Unionidae) in bioassays. Transactions of American Microscopical Society, 78-80. https://doi. org/10.2307/3226786
- John, U., Litaker, R. W., Montresor, M., Murray, S., Brosnahan, M. L., & Anderson, D. M. (2014). For- mal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist, 165(6):779-804. https://doi.org/10.1016/j.protis.2014.10.001
- Kwan, T. N., & Bolch, C. J. (2015). Genetic diversity of culturable Vibrio in an Australian blue mussel Mytilus galloprovincialis hatchery. Disease of Aquatic Organisms, 116(1):37-46. https://doi. org/10.3354/dao02905
- Kwan, T. N, Bolch, C., & Bowman, J. (2017). Necrotic disease in bivalve larval cultures. Microbiology Australia 38, 131-133.
- Kwong, R. W., Wang, W. X., Lam, P. K., & Yu, P. K. (2006). The uptake, distribution and elimination of paralytic shellfish toxins in mussels and fish exposed to toxic dinoflagellates. Aquatic Toxicology, 80(1):82-91. https://doi.org/10.1016/j.aquatox.2006.07.016
- Lee, J. H., Cembella, A., & Anderson, D. M. (1990). Uptake kinetics of paralytic shellfish toxins from the dinoflagellate Alexandrium catenella in the mussel Mytilus edulis. Marine Ecology Progress Series, 63:177-188.
- Mardones, J., Dorantes-Aranda, J. J., Nichols, P. D., & Hallegraeff, G. M. (2015). Fish gill damage by the dinoflagellate Alexandrium catenella from Chilean fjords: Synergistic action of ROS and PUFA. Harmful Algae, 49:40-49. https://doi.org/10.1016/j.
- Marsden, I. D., & Shumway, S. E. (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. https://doi.org/10.1080/00288330.1992. 9516530
- Matsuyama, Y. (2001). Effects of harmful algae on the early planktonic larvae of the oyster, Crassostrea gigas, Harmful Algal Blooms 2000. IOC-UNES- CO, pp. 411-414.
- Mu, C., & Li, Q. (2013). Effects of the dinoflagellate, Alexandrium catenella on the early development of the Pacific oyster Crassostrea gigas. Journal of Shellfish Research, 32(3):689-694. https://doi. org/10.2983/035.032.0310
- Munir, S., Burhan, Z. N., Nias, T., Morton, S. L., & Siddiqui, P. J. A. (2015). Morphometric forms, biovolume and cellular carbon content of dinoflagellates from polluted waters on the Karachi coast, Pakistan. Indian Journal of Geo-Marine Science, 44(1):19- 25. http://hdl.handle.net/123456789/34614
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- Pate, S. E. (2007). Impacts of the toxic dinoflagellate Alexadrium monilatum on three ecologically important shellfish species. Master Thesis. Raleigh: North Carolina State University.
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- Shumway, S. E., & Cucci, T. L. (1987). The effects of the toxic dinoflagellate Protogonyaulax tamarensis on the feeding and behaviour of bivalve molluscs. Aquatic Toxicology, 10(1):9-27. https://doi. org/10.1016/0166-445X(87)90024-5
- Sutton, D. C., & Garrick, R. (1993). Bacterial disease of cultured giant clam Tridacna gigas larvae. Disease of Aquatic Organisms, 16(1):47-53. Doi: 10.3354/ dao016047
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- Tillman, U., & Hansen, P. J. (2009). Allelopathic effects of Alexandrium tamarense on other algae: evidence from mixed growth experiments. Aquatic Microbial Ecology, 57(1):101-112. https://doi. org/10.3354/ame01329
- Tillman, U., John, U., & Cembella, A. (2007). On the allelochemical potency of the marine dinoflagellate Alexandrium onstenfeldii against heterotrophic and autotrophic protists. Journal of Plankton Research, 29(6):527-543. https://doi.org/10.1093/plankt/ fbm034
- Tillmann, U., & John, U. (2002). Toxic effects of Alexandrium spp. on heterotrophic dinoflagellates: an allelochemical defence mechanism independent of PSP-toxin content. Marine Ecology Progress Series, 230:47-58. https://doi.org/10.3354/ meps230047
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References
Abi-Khalil, C., Lopez-Joven, C., Abadie, E., Savar, V., Amzil, Z., Laabir, M., & Rolland, J. L. (2016). Exposure to the paralytic shellfish toxin producer Alexandrium catenella increases the susceptibility of the oyster Crassostrea gigas to pathogenic vib- rios. Toxins, 8(1):24. https://doi.org/10.3390/tox- ins8010024
Anderson, D. M., Alpermann, T. J., Cembella, A. D., Collos, Y., Masseret, E., & Montresor, M. (2012). The globally distributed Alexandrium: multifacet- ed roles in marine ecosystems and impacts on human health. Harmful Algae, 14:10-35. https://doi. org/10.1016/j.hal.2011.10.012
Anderson, D. M., Hoagland, P., Kaoru, Y., & White, A. W. (2000). Estimated annual economic impacts from harmful algal blooms (HABs) in the United States. Technical Report. National Oceanic and Atmospheric Administration Norman OK Nation- al Severe Storms Lab :97 p.
Anderson, D. M., Reguera, B., Pitcher, G. C., & Enevoldsen, H. O. (2010). The IOC international harmful algal bloom program: history and science impacts. Oceanography, 23(4):72-85.
Basti, L., Endo, M., Segawa, S., Shumway, S. E., Tanaka, Y., & Nagai, S. (2016). Prevalence and intensity of pathologies induced by the toxic dinoflagellate, Heterocapsa circularisquama, in the Mediterranean mussel, Mytilus galloprovincialis. Aquatic Toxicology, 163:37-50. https://doi.org/10.1016/j. aquatox.2015.03.012
Bolch, C. J. S., Harwood, T., Untari, L., Murray, S., Hallegraeff, G., & Turnbull, A. (2014, November). Al- exandrium tamarense Group I as the cause of PST on the east coast of Tasmania, Australia. 14th International Conference on Harmful Algae, Wellington New Zealand.
Borcier, E., Morvezen, R., Boudry, P., Miner, P., Charrier, G., Laroche, J., & Hegaret, H. (2017). Effects of bioactive extracellular compounds and paralytic shellfish toxins produced by Alexandrium minutum on growth and behaviour of juvenile great scallops Pecten maximus. Aquatic Toxicology, 184, 142-154. https://doi.org/10.1016/j.aquatox.2017.01.009 Bricelj, V. M.,
Bricelj, V. M., Lee, J. H., & Cembella, A. D. (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.
Bricelj, V. M., Ford, S. E., Lambert, C., Barbou, A., & Paillard, C. (2011). Effects of toxic Alexandrium tamarense on behavior, hemocyte response and de- velopment of brown ring disease in Manila clams. Marine Ecology Progress Series, 430:35-48. https://doi.org/10.3354/meps09111
Brown, C., & Tettelbach, L. P. (1988). Characterization of nonmotile Vibrio sp. pathogenic to larvae of Mercenaria mercenaria and Crassostrea virginica. Aquaculture, 74(3):195-204.
Castrec, J., Hégaret, H., Huber, M., Le Grand, J., Huvet, A., Tallec, K., Boulais, M., Soudant, P., & Fabioux, C. (2020). The toxic dinoflagellate Alexandrium minutum impairs the performance of oyster embryos and larvae. Harmful Algae, 92: 101744. https:// doi.org/10.1016/0044-8486(88)90363-8
Cembella, A., & John, U. (2006). Molecular physiology of toxin production and growth regulation in harmful algae. In: Granéli, E, Turner, J T (Eds.) Ecology of harmful algae (pp. 215-227). Springer.
Contreras, A. M., Marsden, I. D., & Munro, M. H. (2012). 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(2):166-174. https:// doi.org/10.1071/MF11173
Detree C., Núñez-Acuña, G., Roberts, S., & Gallardo-Escárate, C. (2016). Uncovering the Complex Transcriptome Response of Mytilus chilensis against Saxitoxin: Implications of Harmful Algal Blooms on Mussel Populations. PLoS One, 11(10): e0165231. https://doi.org/10.1371/journal. pone.0165231
Feist, S., & Bucke, D. (1983). A double-embedding technique for processing larval oysters for light microscopy. Bulletin of the European Association of Fish Pathologists, 1-2.
Galimany, E., Sunila, I., Hégaret, H., Ramon, M., & Wikfors, G. H. (2008). Experimental exposure of the blue mussel (Mytilus edulis, L.) to the toxic dinoflagellate Alexandrium catenella: Histopathology, immune responses, and recovery. Harmful Algae, 7(5):702-711. https://doi.org/10.1016/j. hal.2008.02.006
Haberkorn, H., Lambert, C., Le Goí¯c, N. P., Moal, J., Sequet, M., Gueguen, M., Sunila, I., & Soudant, P. (2010). Effects of Alexandrium minutum exposure on nutrition related process and reproductive output in oyster Crassostrea gigas. Harmful Algae, 9(5):427-439. https://doi.org/10.1016/j.
Hallegraeff, G. M. (2014). Harmful algae and their toxins: progress, paradoxes and paradigm shifts. In: G. P. Rossini (Ed.). Toxins and biologically active compounds from microalgae (pp. 4-20). CRC Press.
Hallegraeff, G. M., Bolch, C. J. S., Condie, S., Dorantes-Aranda, J. J., Murray, S., Quinlan, R., Ruvindy, R., Turnbull, A., Ugalde, S., & Wilson, K. (2017). Unprecedented Alexandrium blooms in a previously low biotoxin risk area of Tasmania, Australia. In: Proceedings of the 17th International Conference on Harmful Algal Blooms. International Society for the Study of Harmful Algae and Intergovernmental Oceanographic Comission of UNESCO 2017.
Hégaret, H., Wikfors, G. H., & 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(2):549-559. https://doi. org/10.2983/0730-8000 (2007) 26 [549:D- FROFS]2.0.CO;2
Hoagland, P., Anderson, D. M., Kaoru, Y., & White, A. W. (2002). The economic effects of harmful algal blooms in the United States: estimates, as- sessment issues and information needs. Estuaries, 25(4):819-837.
Jacobson, P. J., Farris, J. L., Neves, R., & Cherry, D. S. (1993). Use of neutral red to assess survival of juvenile freshwater mussels (Bivalvia: Unionidae) in bioassays. Transactions of American Microscopical Society, 78-80. https://doi. org/10.2307/3226786
John, U., Litaker, R. W., Montresor, M., Murray, S., Brosnahan, M. L., & Anderson, D. M. (2014). For- mal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist, 165(6):779-804. https://doi.org/10.1016/j.protis.2014.10.001
Kwan, T. N., & Bolch, C. J. (2015). Genetic diversity of culturable Vibrio in an Australian blue mussel Mytilus galloprovincialis hatchery. Disease of Aquatic Organisms, 116(1):37-46. https://doi. org/10.3354/dao02905
Kwan, T. N, Bolch, C., & Bowman, J. (2017). Necrotic disease in bivalve larval cultures. Microbiology Australia 38, 131-133.
Kwong, R. W., Wang, W. X., Lam, P. K., & Yu, P. K. (2006). The uptake, distribution and elimination of paralytic shellfish toxins in mussels and fish exposed to toxic dinoflagellates. Aquatic Toxicology, 80(1):82-91. https://doi.org/10.1016/j.aquatox.2006.07.016
Lee, J. H., Cembella, A., & Anderson, D. M. (1990). Uptake kinetics of paralytic shellfish toxins from the dinoflagellate Alexandrium catenella in the mussel Mytilus edulis. Marine Ecology Progress Series, 63:177-188.
Mardones, J., Dorantes-Aranda, J. J., Nichols, P. D., & Hallegraeff, G. M. (2015). Fish gill damage by the dinoflagellate Alexandrium catenella from Chilean fjords: Synergistic action of ROS and PUFA. Harmful Algae, 49:40-49. https://doi.org/10.1016/j.
Marsden, I. D., & Shumway, S. E. (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. https://doi.org/10.1080/00288330.1992. 9516530
Matsuyama, Y. (2001). Effects of harmful algae on the early planktonic larvae of the oyster, Crassostrea gigas, Harmful Algal Blooms 2000. IOC-UNES- CO, pp. 411-414.
Mu, C., & Li, Q. (2013). Effects of the dinoflagellate, Alexandrium catenella on the early development of the Pacific oyster Crassostrea gigas. Journal of Shellfish Research, 32(3):689-694. https://doi. org/10.2983/035.032.0310
Munir, S., Burhan, Z. N., Nias, T., Morton, S. L., & Siddiqui, P. J. A. (2015). Morphometric forms, biovolume and cellular carbon content of dinoflagellates from polluted waters on the Karachi coast, Pakistan. Indian Journal of Geo-Marine Science, 44(1):19- 25. http://hdl.handle.net/123456789/34614
Núñez-Vázquez, E. J., Gárate-Lizarraga, I., BandSchmidt, C. J., Tapia, A. C., Cortes, D. J., Sandovai, F. E., Tapia, A. H., & Guzman, J. J. (2011). Impact of harmful algal blooms on wild and cultured animals in the Gulf of California. Journal of Environmental Biology, 32(4):413-423.
Olenina, I., Hajdu, S., Edler, L., Andersson, A., Wasmund, N., Busch, S., Göbel, J., Gromisz, S., Huseby, S., Huttunen, M., Jaanus, A., Kokkonen, P., Ledaine, I., & Niemkiewicz, E. (2006). Biovolumes and size-classes of phytoplankton in the Baltic Sea. Baltic Sea Environment Proceeding (106): 144p.
Pate, S. E. (2007). Impacts of the toxic dinoflagellate Alexadrium monilatum on three ecologically important shellfish species. Master Thesis. Raleigh: North Carolina State University.
Samson, J. C., Shumway, S. E., & Weis, J. S. (2008). Effects of the toxic dinoflagellate, Alexandrium catenella on three species of larval fish: a food-chain approach. Journal of Fish Biology, 72(1):168-188.
Shumway, S. E., & Cucci, T. L. (1987). The effects of the toxic dinoflagellate Protogonyaulax tamarensis on the feeding and behaviour of bivalve molluscs. Aquatic Toxicology, 10(1):9-27. https://doi. org/10.1016/0166-445X(87)90024-5
Sutton, D. C., & Garrick, R. (1993). Bacterial disease of cultured giant clam Tridacna gigas larvae. Disease of Aquatic Organisms, 16(1):47-53. Doi: 10.3354/ dao016047
Thompson, P.A., Montagnes, D. J., & Shaw, B. A. (1994). The influence of three algal filtrates on the grazing rate of larval oysters (Crassostrea gigas), determined by fluorescent microscopheres. Aquaculture, 119:237-247. https://doi.org/10.1016/0044-8486 (94)90178-3
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