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

Published online by Cambridge University Press:  11 May 2015

Jia-Ning Lin ,
Jing-Jing Song ,
Tian Yan ,
Qing-Chun Zhang  and
Ming-Jiang Zhou
Jia-Ning Lin
Affiliation:
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China University of Chinese Academy of Sciences, Beijing 100049, China
Jing-Jing Song
Affiliation:
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China University of Chinese Academy of Sciences, Beijing 100049, China Marine Nekton Research Centre, Marine Biology Institute of Shandong Province, Qingdao, China
Tian Yan*
Affiliation:
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
Qing-Chun Zhang
Affiliation:
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
Ming-Jiang Zhou
Affiliation:
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
*
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: [email protected]
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Abstract

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.

Keywords

Prorocentrum donghaienseKarenia mikimotoiCalanus sinicussurvivalreproduction
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 6 , September 2015 , pp. 1071 - 1079
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

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, 513–530.CrossRefGoogle Scholar
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, 341–352.CrossRefGoogle Scholar
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, 241–250.CrossRefGoogle Scholar
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, 49–66.CrossRefGoogle Scholar
Chen, Q. (1964) Study on the reproduction, sex ratio and body size of Calanus sinicus. Oceanology Limnology Sinica 6, 272–287. [in Chinese]Google Scholar
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, 112–122.Google Scholar
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, 3964–3972. [in Chinese]Google Scholar
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, 860–868.CrossRefGoogle Scholar
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, 1430–1437.CrossRefGoogle Scholar
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, 55–65.CrossRefGoogle Scholar
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, 177–183.CrossRefGoogle Scholar
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, 575–584.CrossRefGoogle Scholar
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, 161–169.CrossRefGoogle Scholar
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.Google Scholar
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, 231–259.CrossRefGoogle Scholar
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, 289–297. [in Chinese]Google Scholar
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, 1708–1726.CrossRefGoogle Scholar
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, 723–734.CrossRefGoogle Scholar
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, 403–407.CrossRefGoogle ScholarPubMed
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, 199–210.CrossRefGoogle Scholar
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, 1433–1439.CrossRefGoogle Scholar
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, 335–343.CrossRefGoogle Scholar
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. 461–464.Google Scholar
Jónasdóttir, S. (1994) Effects of food quality on the reproductive success of Acartia tonsa and Acartia hudsonica: laboratory observations. Marine Biology 121, 67–81.CrossRefGoogle Scholar
Jónasdóttir, S. and Kiørboe, T. (1996) Copepod recruitment and food composition: do diatoms affect hatching success? Marine Biology 125, 743–750.CrossRefGoogle Scholar
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, 139–150.CrossRefGoogle Scholar
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, 2719–2722.CrossRefGoogle ScholarPubMed
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, 328–339.CrossRefGoogle Scholar
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, 55–63. [in Chinese]Google Scholar
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]Google Scholar
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, 95–102.CrossRefGoogle Scholar
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, 302–310.CrossRefGoogle ScholarPubMed
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, 2263–2271. [in Chinese]Google Scholar
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, 493–505.CrossRefGoogle Scholar
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, 145–168.CrossRefGoogle Scholar
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, 1–9. [in Chinese]Google Scholar
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, 39–56.CrossRefGoogle Scholar
Omori, M. and Ikeda, T. (1984) Methods in marine zooplankton ecology. New York, NY: John Wiley & Sons.Google Scholar
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, 283–293.CrossRefGoogle Scholar
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, 45–63.CrossRefGoogle Scholar
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, 187–199.CrossRefGoogle Scholar
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, 151–176.CrossRefGoogle Scholar
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, 156–170.CrossRefGoogle Scholar
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, 5829–5832.CrossRefGoogle Scholar
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, 3537–3540.CrossRefGoogle Scholar
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, 550–556.CrossRefGoogle Scholar
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.Google Scholar
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, 855–865.CrossRefGoogle Scholar
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]Google Scholar
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, 693–704.CrossRefGoogle Scholar
State Ocean Administration. (2012) Bulletin of Marine Environmental Quality of China. www.soa.goc.cn.Google Scholar
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, 187–199.CrossRefGoogle Scholar
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, 63–73.CrossRefGoogle Scholar
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, 15–30.CrossRefGoogle Scholar
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]Google ScholarPubMed
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, 371–382.CrossRefGoogle Scholar
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]Google Scholar
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, 133–139. [in Chinese]Google Scholar
Xie, Z.H. (2009) Effect of Prorocentrum donghaiense on feeding and digestive enzyme activity of Calanus Sinicus. Oceanologia et Limnologia Sinica 40, 494–499. [in Chinese]Google Scholar
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, 1081–1085. [in Chinese]Google ScholarPubMed
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. 436–440.Google Scholar
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, 723–731.CrossRefGoogle Scholar
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, 9–18.CrossRefGoogle ScholarPubMed
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 133–149.Google Scholar
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, 1483–1489.CrossRefGoogle Scholar
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]Google ScholarPubMed
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, 140–150.CrossRefGoogle Scholar
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, 367–373.CrossRefGoogle Scholar