Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Seasonal dynamics of Alexandrium tamarense and occurrence of paralytic shellfish poisoning toxins in bivalves in Nanji Islands, East China Sea

Tao Jiang A D , Yixiao Xu B D , Yang Li C , Tianjiu Jiang A E , Feng Wu A and Fan Zhang A
+ Author Affiliations
- Author Affiliations

A Research Center of Harmful Algae and Marine Biology, Jinan University, Guangzhou 510632, China.

B School of Geographical and Oceanographic Sciences, Nanjing University, Nanjing 210093, China.

C College of Life Science, South China Normal University, Guangzhou 510630, China.

D These two authors participated equally.

E Corresponding author. Email: tjiangtj@jnu.edu.cn

Marine and Freshwater Research 65(4) 350-358 https://doi.org/10.1071/MF13001
Submitted: 3 January 2013  Accepted: 20 August 2013   Published: 28 October 2013

Abstract

A monitoring program for seasonal dynamics of A. tamarense and paralytic shellfish poisoning toxins (PSTs) in bivalves was carried out from April 2006 to March 2007 in Nanji Islands, East China Sea. Low abundances of A. tamarense (fewer than 4.0 × 102 cells L–1) were first observed on 15 April 2006. During middle May, blooms of A. tamarense were documented, with the mean density of 3.8 × 103 cells L–1 and 0.75 × 103 cells L–1, corresponding to surface and bottom water columns, respectively. Environmental conditions of temperature range 18–20°C and salinity range 29.5–31 coincided with a high abundance of A. tamarense in the region, and the bloom collapse was likely to be a response to P limitation. Toxin concentrations in cultured Patinopecten yessoensis, Mytilus galloprovincialis and wild Mytilus coruscus during A. tamarense blooms ranged from 68.9 to 96.3 μg STXeq per 100 g flesh. Toxin profiles were similar among bivalve shellfish samples, dominated by C1 and C2 in 51.4–64.6 mol% of toxins, with an average of 60.6 mol%, followed by GTX5, GTX1–GTX4, dcGTX2 and dcGTX3. However, from January to March 2007, lower toxin concentrations, 18.9–40.8 μg STXeq per 100 g were found only in the wild Oyster sp., comprising GTX4, GTX5 and GTX1.

Additional keywords: HABs, marine biotoxins.


References

Anderson, D. M. (1997). Bloom dynamics of toxic Alexandrium species in the northeastern US. Limnology and Oceanography 42, 1009–1022.
Bloom dynamics of toxic Alexandrium species in the northeastern US.Crossref | GoogleScholarGoogle Scholar |

Anderson, D. M., Kulis, D. M., Qi, Y. Z., Zheng, L., Lu, S. H., and Lin, Y. T. (1996). Paralytic shellfish poisoning in southern China. Toxicon 34, 579–590.
Paralytic shellfish poisoning in southern China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xjs1Cru78%3D&md5=840509981caa52f5707d923cda3fb9d1CAS | 8783452PubMed |

AOAC (Association of Official Analytical Chemists) (2000). AOAC official method 959.08, paralytic shellfish poison, biological method. In ‘Official Methods of Analysis of AOAC International’. 17th edn. (Ed. W. Horwitz.) pp. 59–61. (AOAC International: Gaithersburg, MD.)

Bravo, I., Franco, J. M., and Reyero, M. I. (1998). PSP toxin composition of three life cycle stages of Gymnodinium catenatum. In ‘Harmful Algae’. (Eds B. Reguera, J. Blanco, M. L. Fernandez and T. Wyatt.) pp. 356–358. (Xunta de Galicia and IOC of UNESCO and Grafisant: Santiago de Compostela, Spain.)

Bricelj, V. M., and Shumway, S. E. (1998). Paralytic shellfish toxins in bivalve molluscs: occurrence, transfer kinetics, and biotransformation. 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=7524bbfa90a81df1099c15b6c107bd1fCAS |

Bricelj, V. M., Lee, J. H., Cembella, A. D., and Anderson, D. M. (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=5f0ddb288398ca1d3c86f443bc63c50aCAS |

Etheridge, S. M. (2010). Paralytic shellfish poisoning: seafood safety and human health perspectives. Toxicon 56, 108–122.
Paralytic shellfish poisoning: seafood safety and human health perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXms1CjsLw%3D&md5=0d8b02396c5f45bf3b3e861a40d6fe3dCAS | 20035780PubMed |

FAO (2004). ‘Marine Biotoxins.’ (Food and Agriculture Organization of the United Nations: Rome.)

Fauchot, J., Levasseur, M., Roy, S., Gagnon, R., and Weise, A. M. (2005). Environmental factors controlling Alexandrium tamarense (Dinophyceae) growth rate during a red tide event in the St Lawrence Estuary (Canada). Journal of Phycology 41, 263–272.
Environmental factors controlling Alexandrium tamarense (Dinophyceae) growth rate during a red tide event in the St Lawrence Estuary (Canada).Crossref | GoogleScholarGoogle Scholar |

Fu, X. C., Zhao, R. S., Nie, X. Z., Ni, H. S., Zhu, L. F., and Jiang, Y. F. (1982). Food poisoning caused by snail – Nassirius sp. Chinese Journal of Preventive Medicine 16, 140–143.
| 1:STN:280:DyaL3s%2Fis1Kmug%3D%3D&md5=e925af62a150fdbabcfe07915c4e2a39CAS | 7128320PubMed |

Guéguen, M., Bardouil, M., Baron, R., Lassus, P., Truquet, P., Massardier, J., and Amzil, Z. (2008). Detoxification of pacific oyster Crassostrea gigas fed on diets of Skeletonema costatum with and without silt, following PSP contamination by Alexandrium minutum. Aquatic Living Resources 21, 13–20.
Detoxification of pacific oyster Crassostrea gigas fed on diets of Skeletonema costatum with and without silt, following PSP contamination by Alexandrium minutum.Crossref | GoogleScholarGoogle Scholar |

Ichimi, K., Yamasaki, M., Okumura, Y., and Suzuki, T. (2001). The growth and cyst formation of a toxic dinoflagellate, Alexandrium tamarense, at low water temperatures in northeastern Japan. Journal of Experimental Marine Biology and Ecology 261, 17–29.
The growth and cyst formation of a toxic dinoflagellate, Alexandrium tamarense, at low water temperatures in northeastern Japan.Crossref | GoogleScholarGoogle Scholar | 11438103PubMed |

Justić, D., Rabalais, N. N., Turner, R. E., and Dortch, Q. (1995). Changes in nutrient structure of river-dominated coastal waters – Stoichiometric nutrient balance and its consequences. Estuarine, Coastal and Shelf Science 40, 339–356.
Changes in nutrient structure of river-dominated coastal waters – Stoichiometric nutrient balance and its consequences.Crossref | GoogleScholarGoogle Scholar |

Kwong, R. W. M., Wang, W. X., Lam, P. K. S., and Yu, P. K. N. (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=79b00214fda2b7ebfc084bf32a551d43CAS |

Lassus, P., Baron, R., Garen, P., Truquet, P., Masselin, P., Bardouil, M., Leguay, D., and Amzil, Z. (2004). Paralytic shellfish poison outbreaks in the Penze estuary: environmental factors affecting toxin uptake in the oyster, Crassostrea gigas. Aquatic Living Resources 17, 207–214.
Paralytic shellfish poison outbreaks in the Penze estuary: environmental factors affecting toxin uptake in the oyster, Crassostrea gigas.Crossref | GoogleScholarGoogle Scholar |

Li, Y., Lu, S. H., Jiang, T. J., Xiao, Y. P., and You, S. P. (2011). Environmental factors and seasonal dynamics of Prorocentrum populations in Nanji Islands National Nature Reserve, East China Sea. Harmful Algae 10, 426–432.
Environmental factors and seasonal dynamics of Prorocentrum populations in Nanji Islands National Nature Reserve, East China Sea.Crossref | GoogleScholarGoogle Scholar |

Nishihama, Y. (1982). Seasonal abundance of Protogonyaulax sp. causing paralytic shellfish poisoning in Funka Bay, Hokkaido, Japan, 1978–1980. In ‘Proceeding of The North Pacific Aquaculture Symposium’. Report 82-2. (Ed. B. R. Melteff and R. A. Nevé.) pp. 319–327. (University of Alaska Sea Grant College Program, Fairbanks, Alaska: AK.)

Oshima, Y. (1995a). Chemical and enzymatic transformation of paralytic shellfish toxins in marine organisms. In ‘Harmful Marine Algal Bloom’. (Eds P. Lassus, G. Arzul, P. Erard, C. Gentien and C. Marcaillou.) pp. 475–480. (Lavoisier: Paris.)

Oshima, Y. (1995b). Post-column derivatization HPLC methods for paralytic shellfish poisons. In ‘Manual on Harmful Marine Microalgae’. (Eds G. M. Hallegraeff, D. M. Anderson and A.D. Cembella.) pp. 81–94. (UNESCO: Paris.)

Oshima, Y., Bolch, C. J., and Hallegraeff, G. M. (1992). Toxin composition of resting cysts of Alexandrium tamarense (Dinophyceae). Toxicon 30, 1539–1544.
Toxin composition of resting cysts of Alexandrium tamarense (Dinophyceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXjsVajsA%3D%3D&md5=eca52c6b83f9482f8020e1a909670c85CAS | 1488762PubMed |

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=499a24a71ba2a0c883f8573737c42d72CAS | 16168451PubMed |

Sekiguchi, K., Ogata, T., Kaga, S., Yoshida, M., Fukuyo, Y., and Kodama, M. (2001). Accumulation of paralytic shellfish toxins in the scallop Patinopecten yessoensis caused by the dinoflagellate Alexandrium catenella in Otsuchi Bay, Iwate Prefecture, northern Pacific coast of Japan. Fisheries Science 67, 1157–1162.
Accumulation of paralytic shellfish toxins in the scallop Patinopecten yessoensis caused by the dinoflagellate Alexandrium catenella in Otsuchi Bay, Iwate Prefecture, northern Pacific coast of Japan.Crossref | GoogleScholarGoogle Scholar |

Shimada, H., Sawada, M., Kuribayashi, T., Nakata, A., Miyazono, A., and Asami, H. (2010). Spatial distribution of the toxic dinoflagellate Alexandrium tamarense in summer in the Okhotsk Sea off Hokkaido, Japan. Plankton and Benthos Research 5, 1–10.
Spatial distribution of the toxic dinoflagellate Alexandrium tamarense in summer in the Okhotsk Sea off Hokkaido, Japan.Crossref | GoogleScholarGoogle Scholar |

Sommer, H., and Meyer, K. F. (1937). Paralytic shellfish poisoning. Archives of Pathology 24, 560–598.
| 1:CAS:528:DyaA1cXhvVGjsg%3D%3D&md5=110183d923a0e86462649b76c5fcf121CAS |

Song, X. K., Ma, J. X., Liu, Y. H., Liu, L. J., Ma, Y. Q., Ren, L. H., and Tang, X. C. (2009). Evolution and formation causes of Alexandrium tamarense red tide in the sea area of the Nanhuangcheng Island. Transactions of Oceanology and Limnology 4, 93–98.

Sorokin, Y. I., Sorokin, P. Y., and Ravagnan, G. (1996). On an extremely dense bloom of the dinoflagellate Alexandrium tamarense in lagoons of the Po river delta: impact on the environment. Journal of Sea Research 35, 251–255.
On an extremely dense bloom of the dinoflagellate Alexandrium tamarense in lagoons of the Po river delta: impact on the environment.Crossref | GoogleScholarGoogle Scholar |

Sullivan, J. J., Simon, M. G., and Iwaoka, W. T. (1983). Comparison of HPLC and mouse bioassay methods for determining PSP toxins in shellfish. Journal of Food Science 48, 1312–1314.
Comparison of HPLC and mouse bioassay methods for determining PSP toxins in shellfish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXltVSns7Y%3D&md5=2f416a830019b725479c7a548ff43a7cCAS |

Wang, J. H., and Wu, J. Y. (2009). Occurrence and potential risks of harmful algal blooms in the East China Sea. The Science of the Total Environment 407, 4012–4021.
Occurrence and potential risks of harmful algal blooms in the East China Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXls1Orsrw%3D&md5=6696fd58ed2b0f1c3d73d82b2770a0b4CAS |

Wang, Z. H., Qi, Y. Z., Lu, S. H., Wang, Y., and Matsuoka, K. (2004). Seasonal distribution of dinoflagellate resting cysts in surface sediments from Changjiang River Estuary. Phycological Research 52, 387–395.
Seasonal distribution of dinoflagellate resting cysts in surface sediments from Changjiang River Estuary.Crossref | GoogleScholarGoogle Scholar |

Wang, D. Z., Zhang, S. G., Gu, H. F., Chan, L. L., and Hong, H. S. (2006). Paralytic shellfish toxin profiles, and toxin variability of the genus Alexandrium (Dinophyceae) isolated from the southeast China Sea. Toxicon 48, 138–151.
Paralytic shellfish toxin profiles, and toxin variability of the genus Alexandrium (Dinophyceae) isolated from the southeast China Sea.Crossref | GoogleScholarGoogle Scholar | 16859722PubMed |

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=65ed99158b28c27ab4df6b0b8f890f40CAS | 21658755PubMed |

Yamamoto, T., and Tarutani, K. (1997). Effects of temperature, salinity and irradiance on the growth of toxic dinoflagellate Alexandrium tamarense isolated from Hiroshima bay, Japan. Japanese Journal of Phycology 45, 95–101.

Yamamoto, T., and Tarutani, K. (1999). Growth and phosphate uptake kinetics of the toxic dinoflagellate Alexandrium tamarense from Hiroshima Bay in the Seto Inland Sea, Japan. Phycological Research 47, 27–32.
Growth and phosphate uptake kinetics of the toxic dinoflagellate Alexandrium tamarense from Hiroshima Bay in the Seto Inland Sea, Japan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitlaqsb4%3D&md5=73ebfc63f05bfb1a3cdbe9c1c76ef6c8CAS |

Yamamoto, T., Yoshizu, Y., and Tarutani, K. (1995). Effects of temperature, salinity and irradiance on the growth of toxic dinoflagellate Alexandrium tamarense isolated from Mikawa bay, Japan. Japanese Journal of Phycology 43, 91–98.
| 1:CAS:528:DyaK2MXps12jt7Y%3D&md5=2be4a69267976140372c0365f3922c2eCAS |

Yamamoto, T., Hashimoto, T., Tarutani, K., and Kotani, Y. (2002). Effects of winds, tides and river water runoff on the formation and disappearance of the Alexandrium tamarense bloom in Hiroshima Bay, Japan. Harmful Algae 1, 301–312.
Effects of winds, tides and river water runoff on the formation and disappearance of the Alexandrium tamarense bloom in Hiroshima Bay, Japan.Crossref | GoogleScholarGoogle Scholar |

Yan, T., Zhou, M. J., and Qian, P. Y. (2002). Study on the combined effects of temperature, salinity and irradiance on the growth of dinoflagellate Alexandrium tamarense. Acta Oceanologica Sinica 24, 114–120.
| 1:CAS:528:DC%2BD38Xjt1Cmsbg%3D&md5=a7854eb24e1f14b9b31df7fbc0fbd112CAS |

Zhang, S. L., Liu, Y. L., Chen, L., and Qiu, J. K. (2011). Paralytic shellfish poison in south coastal waters of Zhejiang. Marine Environmental Science 30, 703–706.

Zhou, M. J., Li, J., Luckas, B., Yu, R. C., Yan, T., Hummert, C., and Kastrup, S. (1999). A recent shellfish toxin investigation in China. Marine Pollution Bulletin 39, 331–334.
A recent shellfish toxin investigation in China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntFSisLw%3D&md5=39677fb1160e1894d482734c8a5434a5CAS |

Zhou, M. J., Shen, Z. L., and Yu, R. C. (2008). Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River. Continental Shelf Research 28, 1483–1489.
Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River.Crossref | GoogleScholarGoogle Scholar |