Cite this paper:
YANG Xiaoqian, WEN Xin, ZHOU Chengxu, ZHU Xiaojuan, MENG Ran, LUO Qijun, YAN Xiaojun. Comparative study of brine shrimp bioassay-based toxic activities of three harmful microalgal species that frequently blooming in aquaculture ponds[J]. HaiyangYuHuZhao, 2018, 36(5): 1697-1706

Comparative study of brine shrimp bioassay-based toxic activities of three harmful microalgal species that frequently blooming in aquaculture ponds

YANG Xiaoqian1, WEN Xin1,4, ZHOU Chengxu1,2, ZHU Xiaojuan1, MENG Ran3, LUO Qijun1,2, YAN Xiaojun1,2,3
1 School of Marine Science, Ningbo University, Ningbo 315211, China;
2 Key Laboratory of Marine Biotechnology of Zhejiang Province, Ningbo University, Ningbo 315211, China;
3 Li Dak Sum Yip Yio Chin Kenneth Li Marine Biopharmaceutical Research Center, Ningbo University, Ningbo 315211, China;
4 Senior High School of Yudu, Ganzhou 343200, China
Typical harmful micro-algal species constantly occurred in high density in marine aquaculture ponds in Xiangshan and Sanmen Bay, Zhejiang Province. Fates of the microalgal cells influenced by activity of the cultured animals largely determined the effects of the harmful microalgae. However, it is difficult to detect the in situ process. In this paper, toxic activities of three harmful microalga, namely Prymnesium parvum, Pleurochrysis elongata, Karlodinium veneficum, which were isolated from the local ponds, were comparatively studied based on brine shrimp toxic bioassays. Different lethal activities of live cells, cell debris, cellular extracts, and cell free mediums prepared by different process were analyzed. The results showed that, (1) all of the three microalgal species had density and time dependent lethal effects on Artermia nauplii, while P. parvum was the most toxic one and had acute lethal effects in 5 h. No such acute lethal effects were observed in P. elongata or K. veneficum; (2) live cells, cell debris and cellular extracts of P. parvum had the same lethal pattern. Prymnesins, toxin from P. parvum, is probably not exotoxic active; For P. elongata, toxic activity mainly came from live cells and cell debris; For K. veneficum, toxic activity was relatively lower compared with the other two species. However, Karlotoxin, toxin from K. veneficum, is exotoxic active. Physical disturbance triggered K. veneficum cells actively releasing toxins, which made it an active predator.
Key words:    Prymnesium parvum|Pleurochrysis elongata|Karlodinium veneficum|Artemia nauplii|toxic activity   
Received: 2017-05-10   Revised:
PDF (2004 KB) Free
Print this page
Add to favorites
Email this article to others
Articles by YANG Xiaoqian
Articles by WEN Xin
Articles by ZHOU Chengxu
Articles by ZHU Xiaojuan
Articles by MENG Ran
Articles by LUO Qijun
Articles by YAN Xiaojun
Adolf J E, Krupatkina D, Bachvaroff T, Place A R. 2007.Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae, 6(3):400-412.
Bachvaroff T R, Adolf J E, Place A R. 2009. Strain variation in Karlodinium veneficum (Dinophyceae):toxin profiles, pigments, and growth characteristics. Journal of Phycology, 45(1):137-153.
Baker J W, Grover J P, Brooks B W, Ureña-Boeck F, Roelke D L, Errera R, Kiesling R L. 2007. Growth and toxicity of Prymnesium parvum (Haptophyta) as a function of salinity, light, and temperature. Journal of Phycology, 43(2):219-227.
Brooks B W, James S V, Valenti T W Jr, Urena-Boeck F, Serrano C, Berninger J P, Schwierzke L, Mydlarz L D, Grover J P, Roelk D L. 2010. Comparative toxicity of Prymnesium parvum in inland waters. JAWRA Journal of the American Water Resources Association, 46(1):45-62.
Calbet A, Bertos M, Fuentes-Grünewald C, Alacid E, Figueroa R, Renom B, Garcés E. 2011. Intraspecific variability in Karlodinium veneficum:growth rates, mixotrophy, and lipid composition. Harmful Algae, 10(6):654-667.
Deeds J R, Place A R. 2006. Sterol specific membrane interactions with the toxins from Karlodinium micrum(Dinophyceae)-a strategy for self-protection. African Journal of Marine Science, 28(2):421-425.
Deeds J R, Terlizzi D E, Adolf J E, Stoecker D K, Place A R. 2002. Toxic activity from cultures of Karlodinium micrum(=Gyrodinium galatheanum) (Dinophyceae)-a dinoflagellate associated with fish mortalities in an estuarine aquaculture facility. Harmful Algae, 1(2):169-189.
Edvardsen B, Imai I. 2006. The ecology of harmful flagellates within Prymnesiophyceae and Raphidophyceae. In:Granéli E, Turner J T eds. Ecology of Harmful Algae.Springer-Verlag, New York, p.67-79.
Edvardsen B, Paasche E. 1998. Bloom dynamics and physiology of Prymnesium and Chrysochromulina. In:Anderson D M, Cembella A D, Hallegraeff G M eds.Physiological Ecology of Harmful Algal Blooms.Springer-Verlag, Heidelberg. p.193-208.
Faimali M, Giussani V, Piazza V, Garaventa F, Corrà C, Asnaghi V, Privitera D, Gallus L, Cattaneo-Vietti R, Mangialajo L, Chiantore M. 2012. Toxic effects of harmful benthic dinoflagellate Ostreopsis ovata on invertebrate and vertebrate marine organisms. Marine Environmental Research, 76:97-107.
Fresnel J, Probert I, Billard C. 2001. Pyrmnesium faveolatum sp. nov. (Prymnesiopyceae), a new toxicspecies from the Mediterranean Sea. Vie et Milieu, 51(1):89-97.
Granéli E, Edvardsen B, Roelkec D L, Hagström J A. 2012.The ecophysiology and bloom dynamics of Prymnesium spp. Harmful Algae, 14:260-270.
Granéli E, Johansson N. 2003. Effects of the toxic haptophyte Prymnesium parvum on the survival and feeding of a ciliate:the influence of different nutrient conditions.Marine Ecology Progress Series, 254:49-56.
Granéli E, Salomon P S. 2010. Factors influencing allelopathy and toxicity in Prymnesium parvum. JAWRA Journal of the American Water Resources Association, 46(1):108-120.
Hameed S, Sultana V, Ara J, Ehteshamul-Haque S, Athar M. 2009. Toxicity of Fusarium solani strains on brine shrimp(Artemia salina). Zoological Research, 30(4):468-472.
Henrikson J C, Gharfeh M S, Easton A C, Easton J D, Glenn K L, Shadfan M, Mooberry S L, Hambright K D, Cichewicz R H. 2010. Reassessing the ichthyotoxin profile of cultured Prymnesium parvum (golden algae) and comparing it to samples collected from recent freshwater bloom and fish kill events in North America. Toxicon, 55(7):1 396-1 404.
Hewlett P S, Plackett R L. 1979. An Introduction to the Interpretation of Quantal Responses in Biology. University Park Press, Baltimore. p.11-19.
Hickman C P. 1967. Biology of the Invertebrates. CV Mosby Company, St. Louis.
Houdan A, Bonnard A, Fresnel J, Fouchard S, Billard C, Probert I. 2004. Toxicity of coastal coccolithophores(Prymnesiophyceae, Haptophyta). Journal of Plankton Research, 26(8):875-883.
Igarashi T, Aritake S, Yasumoto T. 1998. Biological activities of prymnesin-2 isolated from a red tide alga Prymnesium parvum. Natural Toxins, 6(1):35-41.
James S V, Valenti T W Jr, Prosser K N, Grover J P, Roelke D L, Brooks B W. 2011. Sunlight amelioration of Prymnesium parvum acute toxicity to fish. Journal of Plankton Research, 33(2):265-272.
Jiang Y, Zhou C X, Luo Q J, Ma B. 2009. Lethal effects of different Pleurochrysis carterae cells on brine shrimp.Asian Journal of Ecotoxicology, 4(4):561-568. (in Chinese)
Kempton J W, Lewitus A J, Deeds J R, Law J M, Place A R. 2002. Toxicity of Karlodinium micrum (Dinophyceae) associated with a fish kill in a South Carolina brackish retention pond. Harmful Algae, 1(2):233-241.
Kiene R P, Linn L J, Bruton J A. 2000. New and important roles for DMSP in marine microbial communities. Journal of Sea Research, 43(3-4):209-224.
Larsen A, Bryant S, Båmstedt U. 1998. Growth rate and toxicity of Prymnesium parvum and Prymnesium patelliferum (Haptophyta) in response to changes in salinity, light, and temperature. Sarsia, 83(5):409-418.
Manning S R, La Claire J W Ⅱ. 2010. Prymnesins:toxic metabolites of the golden alga, Prymnesium parvum Carter (Haptophyta). Marine Drugs, 8(3):678-704.
Martínez-Porchas M, Martínez-Córdova L R, Porchas-Cornejo M A, López-Elías J A. 2010. Shrimp polyculture:a potentially profitable, sustainable, but uncommon aquacultural practice. Reviews in Aquaculture, 2(2):73-85.
Martinez-Porchas M, Martinez-Cordova L R. 2012. World aquaculture:environmental impacts and troubleshooting alternatives. The Scientific World Journal, 2012:Article ID 389623.
Michael A S, Thompson C G, Abramovitz M. 1956. Artemia salina as a test organism for bioassay. Science, 123(3194):464.
Not F, Siano R, Kooistra W H C F, Simon N, Vaulot D, Probert I. 2012. Diversity and ecology of eukaryotic marine phytoplankton. Advances in Botanical Research, 64:1-53.
Nunes B S, Carvalho F D, Guilhermino L M, Van Stappen G. 2006. Use of the genus Artemia in ecotoxicity testing.Environmental Pollution, 144(2):453-462.
Nunes B, Carvalho F, Guilhermin L. 2005. Acute toxicity of widely used pharmaceuticals in aquatic species:Gambusia holbrooki, Artemia parthenogenetica and Tetraselmis chuii. Ecotoxicology and Environmental Safety, 61(3):413-419.
Payne T H, Kuwahara S S. 1972. Sterols of the brine shrimp, Artemia salina, from Mono Kake, California. Experientia, 28(9):1 022-1 023.
Place A R, Bowers H A, Bachvaroff T R, Adolf J E, Deeds J R, Sheng J. 2012. Karlodinium veneficum-The little dinoflagellate with a big bite. Harmful Algae, 14:179-195.
Place A R, Harvey H R, Bai X, Coats D W. 2006. Sneaking under the toxin surveillance radar:parasitism and sterol content. African Journal of Marine Science, 28(2):347-353.
Reifel K M, McCoy M P, Tiffany M A, Rocke T E, Trees C C, Barlow S B, Faulkner D J, Hurlbert S H. 2001. Pleurochrysis pseudoroscoffensis (Prymnesiophyceae) blooms on the surface of the Salton Sea, California.Hydrobiologia, 466(1-3):177-185.
Remmel E J, Hambright K D. 2012. Toxin-assisted micropredation:experimental evidence shows that contact micropredation rather than exotoxicity is the role of Prymnesium toxins. Ecology Letters, 15(2):126-132.
Roelke D L, Grover J P, Brooks B W, Glass J, Buzan D, Southard G M, Fries L, Gable G M, Schwierzke-Wade L, Byrd M, Nelson J. 2011. A decade of fish-killing Prymnesium parvum blooms in Texas:roles of inflow and salinity. Journal of Plankton Research, 33(2):243-253.
Sasaki M, Shida T, Tachibana K. 2001. Synthesis and stereochemical confirmation of the HI/JK ring system of prymnesins, potent hemolytic and ichthyotoxic glycoside toxins isolated from the red tide alga. Tetrahedron Letters, 42(33):5 725-5 728.
Schug K A, Skingel T S, Spencer S E, Serrano C A, Le C Q, Schug C A, Valenti T W Jr, Brooks B W, Mydlarz L D, Grover J P. 2010. Hemolysis, fish mortality, and LC-ESIMS of cultured crude and fractionated golden alga(Prymnesium parvum). JAWRA Journal of the American Water Resources Association, 46(1):33-44.
Sheng J, Malkiel E, Katz J, Adolf J E, Place A R. 2010. A dinoflagellate exploits toxins to immobilize prey prior to ingestion. Proceedings of the National Academy of Sciences of the United States of America, 107(5):2 082-2 087.
Simonsen S, Moestrup Ø. 1997. Toxicity tests in eight species of Chrysochromulina (Haptophyta). Canadian Journal of Botany, 75(1):129-136.
Stanley S M, Ries J B, Hardie L A. 2005. Seawater chemistry, coccolithophore population growth, and the origin of Cretaceous chalk. Geology, 33(7):593-596.
Valenti T W Jr, James S V, Lahousse M J, Schug K A, Roelke D L, Grover J P, Brooks B W. 2010. A mechanistic explanation for pH-dependent ambient aquatic toxicity of Prymnesium parvum Carter. Toxicon, 55(5):990-998.
Van Wagoner R M, Deeds J R, Tatters A O, Place A R, Tomas C R, Wright J L C. 2010. Structure and relative potency of several karlotoxins from Karlodinium veneficum. Journal of Natural Products, 73(8):1 360-1 365.
Vanhaecke P, Persoone G, Claus C, Sorgeloos P. 1981. Proposal for a short-term toxicity test with Artemia nauplii.Ecotoxicology and Environmental Safety, 5(3):382-387.
Waggett R J, Tester P A, Place A R. 2008. Anti-grazing properties of the toxic dinoflagellate Karlodinium veneficum during predator-prey interactions with the copepod Acartia tonsa. Marine Ecology Progress Series, 366:31-42.
Xu J L, Zhou H B, Yan X J, Zhou C X, Zhu P, Ma B. 2012.Effect of unialgal diets on the composition of fatty acids and sterols in juvenile ark shell Tegillarca granosa Linnaeus. Journal of Agricultural and Food Chemistry, 60(15):3 973-3 980.
Zhou C X, Fernández N, Chen H M, You Y R, Yan X J. 2011.Toxicological studies of Karlodinium micrum(Dinophyceae) isolated from East China Sea. Toxicon, 57(1):9-18.
Zhou C X, Place A R, Yan X J, Xu J L, Luo Q J, William E, Jiang Y. 2015. Interactions between Karlodinium veneficum and Prorocentrum donghaiense from the East China Sea. Harmful Algae, 49:50-57.