Skip to main content Accessibility help

Large-scale dinoflagellate bloom species Prorocentrum donghaiense and Karenia mikimotoi reduce the survival and reproduction of copepod Calanus sinicus

  • Jia-Ning Lin (a1) (a2), Jing-Jing Song (a1) (a2) (a3), Tian Yan (a1), Qing-Chun Zhang (a1) and Ming-Jiang Zhou (a1)...


Large-scale blooms of dinoflagellates, such as Prorocentrum donghaiense and Karenia mikimotoi, have occurred frequently in the East China Sea (ECS) in recent decades. However, little is known about their effects on the entire life history of copepods. Under laboratory conditions, we investigated the effects of these two common dinoflagellates on the survival of Calanus sinicus individuals at different stages and on reproduction of this copepod. Compared with the control treatment (Skeletonema costatum), the presence of P. donghaiense and K. mikimotoi decreased the survival rates of adults and nauplii during the 16 days of the experiment. Survival of nauplii decreased to 49% and 48%, respectively, relative to the nearly 80% survival of adults. Among the six stages of nauplii, individuals at NII and NIII were more susceptible to P. donghaiense and K. mikimotoi. Lower egg production rates were also observed when copepods were exposed to P. donghaiense and K. mikimotoi, and hatching success decreased only with exposure to P. donghaiense. These results suggest that blooms of the two common dinoflagellates may have detrimental effects on the survival of nauplii and the reproduction of C. sinicus, which may pose a major threat to the recruitment of C. sinicus.


Corresponding author

Correspondence should be addressed to: T. Yan, Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China email:


Hide All
Arendt, K., Jónasdóttir, S., Hansen, P.J. and Gärtner, S. (2005) Effects of dietary fatty acids on the reproductive success of the calanoid copepod Temora longicornis. Marine Biology 146, 513530.
Berggreen, U., Hansen, B. and Kiørboe, T. (1988) Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production. Marine Biology 99, 341352.
Calliari, D. and Tiselius, P. (2005) Feeding and reproduction in a small calanoid copepod: Acartia clausi can compensate quality with quantity. Marine Ecology Progress Series 298, 241250.
Carotenuto, Y., Ianora, A., Buttino, I., Romano, G. and Miralto, A. (2002) Is postembryonic development in the copepod Temora stylifera negatively affected by diatom diets? Journal of Experimental Marine Biology and Ecology 276, 4966.
Chen, Q. (1964) Study on the reproduction, sex ratio and body size of Calanus sinicus. Oceanology Limnology Sinica 6, 272287. [in Chinese]
Chen, T.Y., Tian, Y., Wang, L.P., Bin, Z. and Zhou, M.J. (2007a) The effect of the causative algae of large-scale HAB in the East China Sea on egg hatching of Argopecten irradians, and population growth of Brachionus plicatilis and Moina mongolica. Acta Oceanologica Sinica 26, 112122.
Chen, Y., Tian, Y. and Zhou, M.J. (2007b) Effects of Prorocentrum donghaiense and Alexandrium catenella on the material transfer in a simulated marine food chain. Acta Oceanologica Sinica 27, 39643972. [in Chinese]
Chen, Y., Yan, T., Yu, R. and Zhou, M. (2011) Toxic effects of Karenia mikimotoi extracts on mammalian cells. Chinese Journal of Oceanology and Limnology 29, 860868.
Colin, S.P. and Dam, H.G. (2002) Testing for toxic effects of prey on zooplankton using sole versus mixed diets. Limnology and Oceanography 47, 14301437.
Colin, S.P. and Dam, H.G. (2003) Effects of the toxic dinoflagellate Alexandrium fundyense on the copepod Acartia hudsonica: a test of the mechanisms that reduce ingestion rates. Marine Ecology Progress Series 248, 5565.
Da Costa, R.M., Franco, J., Cacho, E. and Fernández, F. (2005) Toxin content and toxic effects of the dinoflagellate Gyrodinium corsicum (Paulmier) on the ingestion and survival rates of the copepods Acartia grani and Euterpina acutifrons. Journal of Experimental Marine Biology and Ecology 322, 177183.
Dam, H.G. and Colin, S.P. (2005) Prorocentrum minimum (clone Exuv) is nutritionally insufficient, but not toxic to the copepod Acartia tonsa. Harmful Algae 4, 575584.
Frangópulos, M., Guisande, C., Maneiro, I., Riveiro, I. and Franco, J.M. (2000) Short-term and long-term effects of the toxic dinoflagellate Alexandrium minutum on the copepod Acartia clausi. Marine Ecology Progress Series 203, 161169.
Galvão, I.B. (2004) Effect of the food quality (taxonomy and biochemical composition of the microalgae) on the reproduction and survival of the copepod Acartia Tonsa, from the Kiel Bight. PhD thesis. Christian-Albrechts-Universität, Kiel, Germany.
Glibert, P.M., Burkholder, J.M. and Kana, T.M. (2012) Recent insights about relationships between nutrient availability, forms, and stoichiometry, and the distribution, ecophysiology, and food web effects of pelagic and benthic Prorocentrum species. Harmful Algae 14, 231259.
Guo, B., Zhang, B. and Jin, X. (2010) Diet composition and ontogenetic variation in feeding habits of juvenile small yellow croaker Pseudosciaena polyactis Bleeker in the Yellow Sea. Journal of Fishery Sciences of China 17, 289297. [in Chinese]
Harris, R., Irigoien, X., Head, R., Rey, C., Hygum, B., Hansen, B.W., Niehoff, B., Meyer-Harms, B. and Carlotti, F. (2000) Feeding, growth, and reproduction in the genus Calanus. ICES Journal of Marine Science 57, 17081726.
Huo, Y.Z., Wang, S.W., Sun, S., Li, C.L. and Liu, M.T. (2008) Feeding and egg production of the planktonic copepod Calanus sinicus in spring and autumn in the Yellow Sea, China. Journal of Plankton Research 30, 723734.
Ianora, A., Miralto, A., Poulet, S.A., Carotenuto, Y., Buttino, I., Romano, G., Casotti, R., Pohnert, G., Wichard, T. and Colucci-D'Amato, L. (2004a) Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429, 403407.
Ianora, A., Turner, J.T., Esposito, F., Carotenuto, Y., d'Ippolito, G., Romano, G., Fontana, A., Guisande, C. and Miralto, A. (2004b) Copepod egg production and hatching success is reduced by maternal diets of a non-neurotoxic strain of the dinoflagellate Alexandrium tamarense. Marine Ecology Progress Series 280, 199210.
Irigoien, X., Harris, R., Head, R. and Harbour, D. (2000) The influence of diatom abundance on the egg production rate of Calanus helgolandicus in the English Channel. Limnology and Oceanography 45, 14331439.
Ismar, S.M., Hansen, T. and Sommer, U. (2008) Effect of food concentration and type of diet on Acartia survival and naupliar development. Marine Biology 154, 335343.
Jenkinson, I.R. and Arzul, G. (2002) Mitigation by cysteine compounds of rheotoxicity, cytotoxicity and fish mortality caused by the dinoflagellates, Gymnodinium mikimotoi and G. cf. maguelonnense. In Hallegraeff, G., Blackburn, S., Bolch, C. and Lewis, R. (eds) Harmful algal blooms 2000. Paris: IOC of UNESCO, pp. 461464.
Jónasdóttir, S. (1994) Effects of food quality on the reproductive success of Acartia tonsa and Acartia hudsonica: laboratory observations. Marine Biology 121, 6781.
Jónasdóttir, S. and Kiørboe, T. (1996) Copepod recruitment and food composition: do diatoms affect hatching success? Marine Biology 125, 743750.
Jónasdóttir, S.H., Visser, A.W. and Jespersen, C. (2009) Assessing the role of food quality in the production and hatching of Temora longicornis eggs. Marine Ecology Progress Series 382, 139150.
Kim, D., Sato, Y., Oda, T., Muramatsy, T., Maysuyama, Y. and Honjo, T. (2000) Specific toxic effect of dinoflagellate Heterocapsa circularisquama on the rotifer Brachionus plicatilis. Bioscience, Biotechnology, and Biochemistry 64, 27192722.
Kleppel, G., Burkart, C.A. and Tomas, C. (1998) Egg production of the copepod Acartia tonsa in Florida Bay during summer. 1. The roles of food environment and diet. Estuaries 21, 328339.
Li, C., Wang, R. and Sun, S. (2003) Horizontal distribution and feeding activities of Calanus sinicus in the anchovy spawning ground in the southern Yellow Sea. Journal of Fisheries of China 27, 5563. [in Chinese]
Li, J., Sun, S., Li, C., Pu, X. and Zhang, Z. (2006) The effects of different diets on the survival and development of copepod nauplii. Marine Sciences 30, 13. [in Chinese]
Li, J., Sun, S., Li, C., Zhang, Z. and Pu, X.M. (2008) Effects of different diets on the reproduction and naupliar development of the copepod Acartia bifilosa. Journal of Experimental Marine Biology and Ecology 355, 95102.
Lin, J.N., Yan, T., Zhang, Q.C., Wang, Y.F., Liu, Q. and Zhou, M.J. (2014) In situ detrimental impacts of Prorocentrum donghaiense blooms on zooplankton in the East China Sea. Marine Pollution Bulletin 88, 302310.
Liu, S. and Xu, Z. (2011) Comparison of zooplankton lists between Coilia mystus food contents and collections from the Yangtze River Estuary & Hangzhou Bay. Acta Ecologicia Sinica 31, 22632271. [in Chinese]
Lu, D., Goebel, J., Qi, Y., Zou, J., Han, X., Gao, Y. and Li, Y. (2005) Morphological and genetic study of Prorocentrum donghaiense Lu from the East China Sea, and comparison with some related Prorocentrum species. Harmful Algae 4, 493505.
Lu, D., Qi, Y., Gu, H., Dai, X., Wang, H., Gao, Y., Shen, P., Zhang, Q., Yu, R. and Lu, S. (2014) Causative species of harmful algal blooms in Chinese coastal waters. Algological Studies 145, 145168.
Meng, T. (2002) Studies on the feeding of anchovy (Engraulis japonicus) at different life stages on zooplankton in the Middle and Southern Waters of the Yellow Sea. Marine Fisheries Research 24, 19. [in Chinese]
Murray, M.M. and Marcus, N.H. (2002) Survival and diapause egg production of the copepod Centropages hamatus raised on dinoflagellate diets. Journal of Experimental Marine Biology and Ecology 270, 3956.
Omori, M. and Ikeda, T. (1984) Methods in marine zooplankton ecology. New York, NY: John Wiley & Sons.
Peterson, W.T. and Painting, S.J. (1990) Developmental rates of the copepods Calanus australis and Calanoides carinatus in the laboratory, with discussion of methods used for calculation of development time. Journal of Plankton Research 12, 283293.
Pond, D., Harris, R., Head, R. and Harbour, D. (1996) Environmental and nutritional factors determining seasonal viability of Calanus helgolandicus in coastal waters off Plymouth, UK. Marine Ecology Progress Series 143, 4563.
Poulet, S., Escribano, R., Hidalgo, P., Cueff, A., Wichard, T., Aguilera, V., Vargas, C. and Pohnert, G. (2007) Collapse of Calanus chilensis reproduction in a marine environment with high diatom concentration. Journal of Experimental Marine Biology and Ecology 352, 187199.
Sarno, D., Kooistra, W.H.C.F., Medlin, L.K., Percopo, I. and Zingone, A. (2005) Diversity in the genus Skelletonema (Bacillariophyceae): II. An assessment of the taxonomy of S. costatum-like species with the description of four new species. Journal of Phycology 41, 151176.
Sarno, D., Kooistra, W.H.C., Balzano, S., Hargraves, P.E. and Zingone, A. (2007) Diversity in the genus Skelletonema (Bacillariophyceae): III. Phylogenetic position and morphological variability of Skelletonema costatum and Skelletonema grevillei, with the description of Skelletonema ardens sp. nov. Journal of Phycology 43, 156170.
Satake, M., Shoji, M., Oshima, Y., Naoki, H., Fujita, T. and Yasumoto, T. (2002) Gymnocin-A, a cytotoxic polyether from the notorious red tide dinoflagellate, Gymnodinium mikimotoi. Tetrahedron Letters 43, 58295832.
Satake, M., Tanaka, Y., Ishikura, Y., Oshima, Y., Naoki, H. and Yasumoto, T. (2005) Gymnocin-B with the largest contiguous polyether rings from the red tide dinoflagellate, Karenia (formerly Gymnodinium) mikimotoi. Tetrahedron Letters 46, 35373540.
Sellem, F., Pesando, D., Bodennec, G., El Abed, A. and Girard, J.P. (2000) Toxic effects of Gymnodinium cf. mikimotoi unsaturated fatty acids to gametes and embryos of the sea urchin Paracentrotus lividus. Water Research 34, 550556.
Silke, J., O'Beirn, F. and Cronin, M. (2005) Karenia mikimotoi: an exceptional dinoflagellate bloom in western Irish waters, summer 2005. Marine environment and health series. Galway: Marine Institute.
Silva, N.J., Tang, K.W. and Lopes, R.M. (2013) Effects of microalgal exudates and intact cells on subtropical marine zooplankton. Journal of Plankton Research 35, 855865.
Song, J.J. (2014) Research of the mechanisms of HABs in the East China Sea affecting material energy utilization of zooplankton and mussel. PhD thesis. Institute of Oceanology, Chinese Academy of Sciences, China. [in Chinese]
Speekmann, C.L., Hyatt, C.J. and Buskey, E.J. (2006) Effects of Karenia brevis diet on RNA: DNA ratios and egg production of Acartia tonsa. Harmful Algae 5, 693704.
State Ocean Administration. (2012) Bulletin of Marine Environmental Quality of China.
Turner, J.T., Ianora, A., Miralto, A., Laabir, M. and Esposito, F. (2001) Decoupling of copepod grazing rates, fecundity and egg-hatching success on mixed and alternating diatom and dinoflagellate diets. Marine Ecology Progress Series 220, 187199.
Turner, J.T., Roncalli, V., Ciminiello, P., Dell'Aversano, C., Fattorusso, E., Tartaglione, L., Carotenuto, Y., Romano, G., Esposito, F. and Miralto, A. (2012) Biogeographic effects of the Gulf of Mexico red tide dinoflagellate Karenia brevis on Mediterranean copepods. Harmful Algae 16, 6373.
Waggett, R.J., Hardison, D.R. and Tester, P.A. (2012) Toxicity and nutritional inadequacy of Karenia brevis: synergistic mechanisms disrupt top-down grazer control. Marine Ecology Progress Series 444, 1530.
Wang, L., Yan, T., Tan, Z. and Zhou, M. (2003) Effects of Alexandrium tamarense and Prorocentrum donghaiense on rotifer Brachionus plicatilis population. Acta Ecologicia Sinica 14, 1151. [in Chinese]
Wang, L., Yan, T., Yu, R. and Zhou, M. (2005) Experimental study on the impact of dinoflagellate Alexandrium species on populations of the rotifer Brachionus plicatilis. Harmful Algae 4, 371382.
Wang, S.W. (2009) Reproduction, population recruitment and life history of Calanus sinicus in the Yellow Sea. PhD thesis. Institute of Oceanology, Chinese Academy of Sciences, China. [in Chinese]
Wang, Z., Yin, Y., Qi, Y., Xie, L.C. and Jiang, T.J. (2001) Histopathological changes in fish gills during Gymnodinium mikimotoi red tide in Guishan Island area, the South China Sea. Acta Oceanologica Sinica 1, 133139. [in Chinese]
Xie, Z.H. (2009) Effect of Prorocentrum donghaiense on feeding and digestive enzyme activity of Calanus Sinicus. Oceanologia et Limnologia Sinica 40, 494499. [in Chinese]
Xu, Z., Hong, B., Zhu, M. and Chen, Y. (2003) Ecological characteristics of zooplankton in frequent HAB areas of the East China Sea in spring. Acta Ecologicia Sinica 14, 10811085. [in Chinese]
Yasumoto, T., Underdal, B., Aune, T., Hormazabal, V., Skulberg, O. and Oshima, Y. (1990) Screening for hemolytic and ichthyotoxic components of Chrysochromulina polylepis and Gyrodinium aureolum from Norwegian coastal waters. In Granell, E. (ed.) Toxic Marine Phytoplankton. Amsterdam: Elsevier, pp. 436440.
Zheng, Y., Dam, H.G. and Avery, D.E. (2011) Differential responses of populations of the copepod Acartia hudsonica to toxic and nutritionally insufficient food algae. Harmful Algae 10, 723731.
Zhou, C.X., Fernandez, N., Chen, H.M., You, Y.R. and Yan, X.J. (2011) Toxicological studies of Karlodinium micrum (Dinophyceae) isolated from East China Sea. Toxicon 57, 918.
Zhou, M. (2010) Environmental settings and harmful algal blooms in the sea area adjacent to the Changjiang River Estuary. Coastal Environmental and Ecosystem Issues of the East China Sea 133149.
Zhou, M., Shen, Z. and Yu, R. (2008) Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River. Continental Shelf Research 28, 14831489.
Zhou, M., Yan, T. and Zhou, J. (2003) Preliminary analysis of the characteristics of red tide areas in Changjiang River estuary and its adjacent sea. Acta Ecologicia Sinica 14, 1031. [in Chinese]
Zingone, A., Percopo, I., Sims, P.A. and Sarno, D. (2005) Diversity in the genus Skeletonema (Bacillariophyceae). I. A reexamination of the type material of S. costatum with the description of S. grevillei sp. nov. Journal of Phycology 41, 140150.
Zou, Y., Yamasaki, Y., Matsuyama, Y., Yamaguchi, K., Honjo, T. and Oda, T. (2010) Possible involvement of hemolytic activity in the contact-dependent lethal effects of the dinoflagellate Karenia mikimotoi on the rotifer Brachionus plicatilis. Harmful Algae 9, 367373.


Related content

Powered by UNSILO

Large-scale dinoflagellate bloom species Prorocentrum donghaiense and Karenia mikimotoi reduce the survival and reproduction of copepod Calanus sinicus

  • Jia-Ning Lin (a1) (a2), Jing-Jing Song (a1) (a2) (a3), Tian Yan (a1), Qing-Chun Zhang (a1) and Ming-Jiang Zhou (a1)...


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.