, Volume 453, Issue 1, pp 107–120

Feeding, egg production, and egg hatching success of the copepods Acartia tonsa and Temora longicornis on diets of the toxic diatom Pseudo-nitzschia multiseries and the non-toxic diatom Pseudo-nitzschia pungens

  • Jean A. Lincoln
  • Jefferson T. Turner
  • Stephen S. Bates
  • Claude Léger
  • David A. Gauthier


In 1987, there was an episode of shellfish poisoning in Canada with human fatalities caused by the diatom Pseudo-nitzschia multiseries, which produced the toxin domoic acid. In order to examine whether domoic acid in this diatom serves as a grazing deterrent for copepods, we compared feeding rates, egg production rates, egg hatching success and mortality of the calanoid copepods Acartia tonsa and Temora longicornis feeding on unialgal diets of the toxic diatom P. multiseries and the similarly-sized non-toxic diatom Pseudo-nitzschia pungens. Copepods were collected in summers of 1994, 1995 and 1996 from Shediac Bay, New Brunswick, Canada, near Prince Edward Island, the site of the 1987 episode of domoic acid shellfish poisoning. Rates of ingestion of the toxic versus the non-toxic diatom by A. tonsa and T. longicornis were similar, with only one significantly different pair of values obtained in 1994, for which A. tonsa had a higher mean rate of ingestion of the toxic than the non-toxic diatom. Thus, domoic acid did not appear to retard grazing. Analyses of copepods with high performance liquid chromatography (HPLC) revealed that copepods accumulated domoic acid when feeding on P. multiseries. Egg production rates of copepods when feeding on P. multiseries and P. pungens were very low, ranging from 0 to 2.79 eggs female−1 d−1. There did not appear to be differential egg production or egg hatching success on diets of the toxic and non-toxic diatoms. Mortality of females on the toxic diet was low, ranging from 0 to 20%, with a mean of 13%, and there was no apparent difference between mortality of copepods feeding on toxic versus non-toxic diatoms. Egg hatching success on both diets, although based on few eggs, ranged between 22% and 76%, with a mean percentage hatching of 45%. Diets of the non-toxic diatom plus natural seawater assemblages supplemented with dissolved domoic acid, revealed similar rates and percentages when compared to previous experiments. In summary, none of the variables measured indicated adverse effects on copepods feeding on the toxic compared to the non-toxic diatom.

copepod feeding domoic acid Pseudo-nitzschia multiseries 


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  1. Anderson, D. M., 1989. Toxic algal blooms and red tides: a global perspective. In Okaichi, T., D. M. Anderson & T. Nemoto (eds), Red Tides. Biology, Environmental Science and Toxicology. Elsevier, New York, Amsterdam, London: 11–16.Google Scholar
  2. Anderson, D. M. & A. W. White, 1992. Marine biotoxins at the top of the food chain. Oceanus 35: 55–61.Google Scholar
  3. Ban, S., C. Burns, J. Castel, Y. Chaudron, E. Christou, R. Escribano, S. Umani, S. Gasparini, F. Ruiz, M. Hoffmeyer, A. Ianora, H. Kang, M. Laabir, A. Lacoste, A. Miralto, X. Ning, S. Poulet, V. Rodriguez, J. Runge, J. Shi, M. Starr, S. Uye & Y. Wang, 1997. The paradox of diatom-copepod interactions. Mar. Ecol. Prog. Ser. 157: 287–293.Google Scholar
  4. Bates, S. S., C. J. Bird, A. S.W. De Freitas, R. Foxall, M.W. Gilgan, L. A. Hanic, G. E. Johnson, A.W. McCulloch, P. Odense, R. Pocklington, M. A. Quilliam, P. G. Sim, J. C. Smith, D. V. Subba Rao, E. C. D. Todd, J. A Walter & J. L. C. Wright, 1989. Pennate diatom Nitzschia pungens as the primary source of domoic acid, a toxin in shellfish from eastern Prince Edward Island, Canada. Can. J. Fish. aquat. Sci. 46: 1203–1215.Google Scholar
  5. Bates, S. S., A. S. W. De Freitas, J. E. Milley, R. Pocklington, M.A. Quilliam, J. C. Smith & J. Worms, 1991. Controls on domoic acid production by the diatom Nitzschia pungens f. multiseries in culture: nutrients and irradiance. Can. J. Fish. aquat. Sci. 48: 1136–1144.Google Scholar
  6. Bates, S. S., C. Léger, B. A. Keafer & D. M. Anderson, 1993a. Discrimination between domoic-acid-producing and nontoxic forms of the diatom Pseudonitzschia pungens using immunofluorescence. Mar. Ecol. Prog. Ser. 100: 185–195.Google Scholar
  7. Bates, S. S., J. Worms & J. C. Smith, 1993b. Effects of ammonium and nitrate on domoic acid production by Nitzschia pungens in batch culture. Can. J. Fish. aquat. Sci. 50: 1248–1254.Google Scholar
  8. Bates, S. S., D. J. Douglas, G. J. Doucette & C. Léger, 1995. Enhancement of domoic acid production by reintroducing bacteria to axenic cultures of the diatom Pseudo-nitzschia multiseries. Nat. Toxins 3: 428–435.Google Scholar
  9. Bates, S. S., C. Léger & K.M. Smith, 1996. Domoic acid production by the diatom Pseudo-nitzschia multiseries as a function of division rate in silicate-limited chemostat culture. In Yasumoto, T., Y. Oshima & Y. Fukuyo (eds), Harmful and Toxic Algal Blooms. Intergov. Oceanogr. Comm. UNESCO, Paris: 163–166.Google Scholar
  10. Buskey, E. J. & D. A. Stockwell, 1993. Effects of a persistent 'brown tide' on zooplankton populations in the Laguna Madre of south Texas. In Smayda, T. J. & Y. Shimizu, (eds), Toxic Phytoplankton Blooms in the Sea. Elsevier, Amsterdam: 659–666.Google Scholar
  11. Citarella, G., 1982. Le zooplancton de la baie de Shédiac (Nouveau-Brunswick). J. Plankton Res. 4: 791–812.Google Scholar
  12. Dale, B. & C. M. Yentsch, 1978. Red tide and paralytic shellfish poisoning. Oceanus 21: 41–49.Google Scholar
  13. Debonnel, G., L. Beauchesne & C. De Montigny, 1989. Domoic acid the alleged 'mussel toxin', might produce its neurotoxic effect through kainate receptor activation: an electrophysiological study in the rat dorsal hippocampus. Can. J. Physiol. Pharmacol. 67: 29–33.Google Scholar
  14. Dutz, J., 1998. Repression of fecundity in the neritic copepod Acartia clausi exposed to the toxic dinoflagellate Alexandrium lusitanicum: relationship between feeding and egg production. Mar. Ecol. Prog. Ser. 175: 97–107.Google Scholar
  15. Edgar, R. K. & K. Laird, 1993. Computer simulation of error rates of Poisson-based interval estimates of phytoplankton abundance. Hydrobiologia 264: 65–77.Google Scholar
  16. Edler, L., 1978. Recommendations on methods for marine biological studies in the Baltic Sea: phytoplankton and chlorophyll. Baltic Marine Biologists No. 5: 38 pp.Google Scholar
  17. Fritz, L., M. Quilliam, J. L. C. Wright, A. M. Beale & T. M. Work, 1992. An outbreak of domoic acid poisoning attributed to the pennate diatom Pseudo-nitzschia australis. J. Phycol. 28: 439–442.Google Scholar
  18. Frost, B. W., 1972. Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol. Oceanogr. 17: 805–815.Google Scholar
  19. Gaudy, F., 1974. Feeding four species of pelagic copepods under experimental conditions. Mar. Biol. 25: 125–141.Google Scholar
  20. Gill, C. W. & R. P. Harris, 1987. Behavioural responses of the copepods Calanus helgolandicus and Temora longicornis to dinoflagellate diets. J. mar. biol. Ass. U.K. 67: 785–801.Google Scholar
  21. Gossett, W. S., 1907. On the error of counting with a haemocytometer. Biometrika 5: 351–360.Google Scholar
  22. Guillard, R. R. L., 1973. Division rates. In Stein, J. R. (ed.), Handbook of Phycological Methods. Cambridge University Press: 289–311.Google Scholar
  23. Hallegraeff, G. M., 1993, A review of harmful algal blooms and their apparent global increase. Phycologia 32: 79–99.Google Scholar
  24. Hitchcock, G. L., 1982. A comparative study of the size-dependent organic composition of marine diatoms and dinoflagellates. J. Plankton Res. 4: 363–377.Google Scholar
  25. Huntley, M. E., P. Ciminiello & M. D. G. Lopez, 1987. Importance of food quality in determining development and survival of Calanus pacificus (Copepoda: Calanoida). Mar. Biol. 95: 103–113.Google Scholar
  26. Huntley, M. E., P. Sykes, S. Rohan & V. Marin, 1986. Chemicallymediated rejection of dinoflagellate prey by the copepods Calanus pacificus and Paracalanus parvus: mechanism, occurrence and significance. Mar. Ecol. Prog. Ser. 28: 105–120.Google Scholar
  27. Ianora, A., 1998. Copepod life history traits in subtemperate regions. J. mar. Syst. 15: 337–349.Google Scholar
  28. Ianora, A., S. A. Poulet & A. Miralto, 1995. A comparative study of the inhibitory effect of diatoms on the reproductive biology of the copepod Temora stylifera. Mar. Biol. 121: 533–539.Google Scholar
  29. Ives, J. D., 1985. The relationship between Gonyaulax tamarensis cell toxin levels and copepod ingestion rates. In Anderson, D. M., A.W. White & D. G. Baden (eds), Toxic Dinoflagellates. Elsevier, Amsterdam: 413–418.Google Scholar
  30. Kiø rboe, T., 1989. Phytoplankton growth rate and nitrogen content: implications for feeding and fecundity in a herbivorous copepod. Mar. Ecol. Prog. Ser. 55: 229–234.Google Scholar
  31. Kleppel, G. S., 1993. On the diets of calanoid copepods. Mar. Ecol. Prog. Ser. 99: 183–195.Google Scholar
  32. Lincoln, J. A., 1998. Feeding, egg production and egg hatching success of the copepods Acartia tonsa and Temora longicornis on diets of the toxic diatom Pseudo-nitzschia multiseries and the non-toxic diatom Pseudo-nitzschia pungens. Master of Science thesis, University of Massachusetts Dartmouth: 108 pp.Google Scholar
  33. Maeda, M., T. Kodama, T. Tanaka, Y. Ohfune, K. Nomoto, K. Nishimura & T. Fujita, 1984. Insecticidal and neuromuscular activities of domoic acid and its related compounds. J. Pesticide Sci. 9: 27–32.Google Scholar
  34. McAlice, B. J., 1981. On the post-glacial history of Acartia tonsa (Copepoda: Calanoida) in the Gulf of Maine and the Gulf of St. Lawrence. Mar. Biol. 64: 267–272.Google Scholar
  35. Parrish, K. K. & D. F. Wilson, 1978. Fecundity studies on Acartia tonsa (Copepoda: Calanoida) in standardized culture. Mar. Biol. 46: 65–81.Google Scholar
  36. Perl, T.M., L. Bedard, T. Kosatsky, J. C. Hockin, E. C. D. Todd & R. S. Remis, 1990. An outbreak of toxic encephalopathy caused by eating mussels contaminated with domoic acid. N. Eng. J. Med. 322: 1775–1780.Google Scholar
  37. Pocklington, R., J. E. Milley, S. S. Bates, C. J. Bird, A. S. W. De Freitas & M. A. Quilliam, 1989. Trace determination of domoic acid in seawater and phytoplankton by high-preformance liquid chromatography of the fluorenylmethoxycarbonyl (FMOC) derivative. Intern. J. Envir. Anal. Chem. 38: 351–368.Google Scholar
  38. Scholin, C. A., F. Gulland, G. J. Doucette, S. Benson, M. Busman, F. P. Chavez, J. Cordaro, R. DeLong, A. De Vogelaere, J. Harvey, M. Haulena, K. Lefebvre, T. Lipscomb, S. Loscutoff, L. J. Lowenstine, R. Marin III, P. E. Miller, W. A. McLellan, P. D. R. Moeller, C. L. Powell, T. Rowles, P. Silvagni, M. Silver, T. Spraker, V. Trainer & F. M. Van Dolah, 2000. Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature 403: 80–84.Google Scholar
  39. Scott, T., 1905. On some Entomostraca from the Gulf of St. Lawrence. Trans. nat. Hist. Soc. Glasgow 7: 46–52.Google Scholar
  40. Shumway, S. E., 1990. A review of the effects of algal blooms on shellfish and aquaculture. J.World Aquaculture Soc. 21: 65–105.Google Scholar
  41. Smayda, T. J., 1989. Primary production and the global epidemic of phytoplankton blooms in the sea: a linkage? In Cosper, E. M., V. M. Bricelji & E. J. Carpenter (eds), Novel Phytoplankton Bloom. Causes and Impacts of Recurrent Brown Tides and Other Unusual Blooms. Springer-Verlag: 449–483.Google Scholar
  42. Smith, J. C., R. Cormier, J. Worms, C. J. Bird, M. A. Quillam, R. Pocklington, R. Angus & L. Hanic, 1990. Toxic blooms of the domoic acid containing diatom Nitzschia pungens in the Cardigan River, Prince Edward Island, in 1988. In Granéli, E., B. Sundström, L. Edler & D. M. Anderson (eds) Toxic Marine Phytoplankton. Elsevier, Amsterdam: 227–232.Google Scholar
  43. Sokal, R. R. & F. J. Rohlf, 1995. Biometry. 3rd edn. W.H. Freeman, San Francisco: 887 pp.Google Scholar
  44. Steidinger, K. A., 1983. A re-evaluation of toxic dinoflagellate biology and ecology. Prog. phycol. Res. 2: 147–188.Google Scholar
  45. Stottrup, J. G. & J. Jensen, 1990. Influence of algal diet on feeding and egg-production of the calanoid copepod Acartia tonsa Dana. J. exp. mar. Biol. Ecol. 141: 87–106.Google Scholar
  46. Sykes, P. F. & M. E. Huntley, 1987. Acute physiological reactions of Calanus pacificus to selected dinoflagellates: direct observations. Mar. Biol. 94: 19–24.Google Scholar
  47. Teegarden, G. J. & A. D. Cembella, 1996. Grazing of toxic dinoflagellates, Alexandrium spp., by adult copepods of coastal Maine: implications for the fate of paralytic shellfish toxins in marine food webs. J. exp. mar. Biol. Ecol. 196: 145–176.Google Scholar
  48. Tester, P. A. & J. T. Turner, 1990. How long does it take copepods to make eggs? J. exp. mar. Biol. Ecol. 141: 169–182.Google Scholar
  49. Todd, E. C. D., 1993. Domoic acid and amnesic shellfish poisoning - A review. J. Food Protect. 56: 69–83.Google Scholar
  50. Turner, J. T. & D. M. Anderson, 1983. Zooplankton grazing during dinoflagellate blooms in a Cape Cod embayment, with observations of predation upon tinitinnids by copepods. Pubbl. Sta. Zool. Napoli: Mar. Ecol. 4: 359–374.Google Scholar
  51. Turner, J. T. & P. A. Tester, 1989. Zooplankton feeding ecology: grazing during an expatriate red tide. In Cosper, E. M., V. M. Bricelj & E. J. Carpenter (eds), Novel Phytoplankton Blooms: Causes and Impacts of Recurrent Brown Tides and Other Unusual Blooms, Coastal and Estuarine Studies 35. Springer-Verlag, Berlin: 359–374.Google Scholar
  52. Turner, J. T. & P. A. Tester, 1997. Toxic marine phytoplankton, zooplankton grazers and pelagic food webs. Limnol. Oceangr. 42: 1203–1214.Google Scholar
  53. Turner, J. T., P. A. Tester & P. J. Hansen, 1998a. Interactions between toxic marine phytoplankton and metazoan and protistan grazers. In Anderson, D. M., A. D. Cembella & G. M. Hallegraeff (eds), Physiological Ecology of Harmful Algal Blooms. Springer-Verlag, Berlin: 453–474.Google Scholar
  54. Turner J. T., J. A. Lincoln & A. Cembella, 1998b. Effects of toxic and non-toxic dinoflagellates on copepod grazing, egg production and egg hatching success. In Reguera, B., J. Blanco, M. L. Fernandez & T. Wyatt (eds), Harmful Algae. Proceedings of the VIII International Conference on Harmful Algae, Vigo, Spain. UNESCO, Paris: 379–381.Google Scholar
  55. Turriff, N., J. A. Runge & A. D. Cembella, 1995. Toxin accumulation and feeding behaviour of the planktonic copepod Calanus finmarchicus exposed to the red-tide dinoflagellate Alexandrium excavatum. Mar. Biol. 123: 55–64.Google Scholar
  56. Uye, S., 1986. Impact of copepod grazing on the red-tide flagellate Chattonella antiqua. Mar. Biol. 92: 35–42.Google Scholar
  57. Uye, S. I. & K. Takamatsu, 1990. Feeding interactions between planktonic copepods and red-tide dinoflagellates from Japanese coastal waters. Mar. Ecol. Prog. Ser. 59: 97–107.Google Scholar
  58. Villac, M. C., D. L. Roelke, T. A. Villareal & G. A. Fryxell, 1993. Comparison of two domoic acid-producing diatoms: a review. Hydrobiologia 269/270: 213–224.Google Scholar
  59. White, A.W., 1979. Dinoflagellate toxins in phytoplankton and zooplankton fractions during a bloom of Gonyaulax excavata. In Taylor, D. L. & H. H. Seliger (eds), Toxic Dinoflagellate Blooms. Elsevier, Amsterdam: 381–384.Google Scholar
  60. White, A. W., 1981. Marine zooplankton can accumulate and retain dinoflagellate toxins and cause fish klills. Limnol. Oceanogr. 26: 103–109.Google Scholar
  61. Windust, A., 1992. The responses of bacteria, microalgae and zooplankton to the diatom Nitzschia pungens f. multiseries and its toxic metabolite domoic acid. M.S. thesis, Dalhousie University: 107 pp.Google Scholar
  62. Wood, T. M. & L. Shapiro (eds), 1992. Amnesic Shellfish Poisoning: a Workshop Report. Oregon Institute of Marine Biology, Newport, Oregon: 52 pp.Google Scholar
  63. Work, T. M., A. B. Beale, L. Fritz, M. A. Quilliam, M. Silver, K. Buck & J. L. C. Wright, 1992. Domoic acid intoxication of brown pelicans and cormorants in Santa Cruz, California. In Smayda, T. J. & Y. Shimizu (eds), Toxic Phytoplankton Blooms in the Sea. Elsevier, Amsterdam: 643–649.Google Scholar
  64. Wright, J. L. C., R. K. Boyd, A. S. W. De Freitas, M. Falk, R. A. Foxall, W. D. Jamieson, M. V. Laycock, A.W. McCulloch, A. G. McInnes, P. Odense, V. P. Pathak, M. A. Quilliam, M. A. Ragan, P. G. Sim, P. Thibault, J. A. Walter, M. Gilgan, D. J. A. Richard & D. Dewar, 1989. Identification of domoic acid, neuroexcitatory amino acid, in toxic mussels from eastern Prince Edward Island. Can. J. Chem. 67: 481–490.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Jean A. Lincoln
    • 1
  • Jefferson T. Turner
    • 2
  • Stephen S. Bates
    • 3
  • Claude Léger
    • 3
  • David A. Gauthier
    • 1
  1. 1.Department of Biology and Center for Marine Science and TechnologyUniversity of Massachusetts DartmouthNorth DartmouthU.S.A.
  2. 2.Department of Biology and Center for Marine Science and TechnologyUniversity of Massachusetts DartmouthNorth DartmouthU.S.A.
  3. 3.Fisheries and Oceans CanadaGulf Fisheries CentreMonctonCanada

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