Abstract
The planktonic copepod Calanus finmarchicus is a dominant member of the zooplankton community in the lower St. Lawrence Estuary in eastern Canada. Blooms of the toxic marine dinoflagellate Alexandrium excavatum which produces high cellular levels of paralytic shellfish poisoning (PSP) toxins, occur during the period of high C. finmarchicus production in summer in this region. To study the feeding behaviour of C. finmarchicus in the presence of Alexandrium spp., experiments were conducted in which female adult copepods collected from the St. Lawrence Estuary between May and September 1991 were exposed under controlled conditions to two toxic isolates of A. excavatum (Pr18b and Pr11f) from the estuary and to a non-toxic control (PLY 173) of a closely related species, A. tamarense isolated from the Tamar Estuary, Plymouth, U.K. Clearance rates on non-toxic A. tamarense cells averaged 5.5 ml ind-1 h-1 but were nearzero with either toxic isolate. When presented with a mixture of A. excavatum and the non-toxic diatom Thalassiosira weissflogii in varying proportions, C. finmarchicus fed upon the diatom but avoided the toxic dinoflagellate. Although feeding rates on A. excavatum were very low, toxin analysis by high-performance liquid chromatography with fluorescence detection (HPLC-FD) revealed that the PSP toxins were accumulated in copepods exposed to toxigenic dinoflagellates.
The toxin composition in copepods was similar to that of the toxic dinoflagellate, but not necessarily identical, particularly after short-term (2-h) exposure, when relatively elevated levels of N-sulfocarbamoyl toxins were detected. The evidence suggests that C. finmarchicus ingests toxic dinoflagellate cells, either mistakenly or during exploratory bouts of feeding, and accumulates PSP toxins in its gut system and perhaps in other tissues.
Similar content being viewed by others
References
Anderson DM (1989) Toxic algal blooms and red tides: a global perspective. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides: biology, environmental science and toxicology. Elsevier, New York, pp 11–16
Anderson DM, Kulis DM, Sullivan JJ, Hall S, Lee C (1990) Dynamics and physiology of saxitoxin production by the dinoflagellates Alexandrium spp. Mar Biol 104:511–524
Boyer GL, Sullivan JJ, Andersen RJ, Harrison PJ, Cembella AD (1986) Use of high performance liquid chromatography to investigate the production of paralytic shellfish toxins by Protogonyaulax spp. in culture. Mar Biol 93:361–369
Boyer GL, Sullivan JJ, Andersen RJ, Harrison PJ, Taylor FJR (1985) The assimilation of PSP toxins by the copepod Tigriopus californicus from dietary Protogonyaulax catenella. In: Anderson DM, White AW, Baden DG (eds) Toxic dinoflagellates. Elsevier, New York, pp 407–412
Cembella AD, Shumway SE, Lewis NI (1993) Anatomical distribution and spatio-temporal variation in paralytic shellfish toxin composition in two bivalve species from the Gulf of Maine. J Shellfish Res 12:389–403
Cembella A, Sullivan JJ, Boyer GL, Taylor FJR, Andersen RJ (1987) Variation in shellfish toxin composition within the Protogonyaulax tamarensis/catenella species complex. Biochem Systematics Ecol 15:171–186
Cembella AD, Therriault J-C (1989) Population dynamics and toxin composition of Protogonyaulax tamarensis from the St. Lawrence estuary. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides: biology, environmental science and toxicology. Elsevier, New York, pp 81–84
Cembella AD, Therriault J-C, Béland P (1988) Toxicity of cultured isolates and natural populations of Protogonyaulax tamarensis from the St. Lawrence estuary. J Shellfish Res 7:611–621
de LaFontaine Y, Demers S, Runge J (1991) Pelagic food web interactions and productivity in the Gulf of St. Lawrence: a perspective. In: Therriault J-C (ed) The Gulf of St. Lawrence: small ocean or big estuary? Can Spec Publ Fish aquat Sciences 113, pp 99–123
Esaias WE, Curl HC, Jr (1972) Effect of dinoflagellate bioluminescence on copepod ingestion rates. Limnol Oceanogr 17:901–906
Fortier L, Levasseur ME, Drolet R, Therriault J-C (1992) Export production and the distribution of fish larvae and their prey in a coastal jet frontal region. Mar Ecol Prog Ser 85:203–218
Frost BW (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
Geraci JR, Anderson DM, Timperi RJ, St Aubin DJ, Early GA, Prescott JH, Mayo CA (1989) Humpback whales (Megaptera novaeangliae) fatally poisoned by dinoflagellate toxin. Can J Fish aquat Sciences 46:1895–1998
Gill CW, Harris RP (1987) Behavioural responses of the copepods Calanus helgolandicus and Temora longicornis to dinoflagellate diets. J mar biol Ass UK 67:785–801
Gosselin S, Fortier L, Gagne JA (1989) Vulnerability of marine fish larvae to the toxic dinoflagellate Protogonyaulax tamarensis. Mar Ecol Prog Ser 57:1–10
Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 29–60
Hayashi T, Shimizu Y, White AW (1982) Toxin profile of herbivorous zooplankton during a Gonyaulax bloom in the Bay of Fundy. Bull Jap Soc scient Fish 48:1673
Huntley M (1988) Feeding biology of Calanus: a new perspective. Hydrobiologia 167/168:83–99
Huntley M, Sykes P, Rohan S, Marin V (1986) Chemically-mediated rejection of dinoflagellate prey by the copepods Calanus pacificus and Paracalanus parvus: mechanism, occurrence and significance. Mar Ecol Prog Ser 28:105–120
Huppertz B, Levasseur M (1993) Monitorage du phytoplancton toxique dans l'estuaire et le golfe du Saint-Laurent en 1990. Rapp tech Can Sci hal aquat No 1922, pp 1–51
Ives DJ (1985) The relationship between Gonyaulax tamarensis cell toxin levels and copepod ingestion rates. In: Anderson DM, White AW, Baden DG (eds) Toxic dinoflagellates. Elsevier, New York, pp 413–418
Ives DJ (1987) Possible mechanisms underlying copepod grazing responses to levels of toxicity in red tide dinoflagellates. J exp mar Biol Ecol 112:131–145
McClatchie S (1988) Functional response of the euphausid Thysanoessa raschii grazing on small diatoms and toxic dinoflagellates. J mar Res 46:631–646
Plourde S, Runge J (1993) Reproduction of the planktonic copepod Calanus finmar chicus in the Lower St. Lawrence Estuary: relation to the cycle of phytoplankton production and evidence for a Calanus pump. Mar Ecol Prog Ser 102:217–227
Poulet SA, Ianora A, Miralto A, Meijer L (1994) Do diatoms arrest embryonic development in copepods? Mar Ecol Prog Ser 111:79–86
Robineau B, Fortier L, Gagné JA, Cembella A (1991a) Comparison of the response of five larval fish species to the toxic dinoflagellate Alexandrium excavatum (Braarud) Balech. J exp mar Biol Ecol 152:225–242
Robineau B, Gagné J, Fortier L, Cembella A (1991b) Potential impact of a toxic dinoflagellate (Alexandrium excavatum) bloom on the survival of fish and crustacean larvae. Mar Biol 108:293–301
Runge JA (1988) Should we expect a relationship between primary production and fisheries? The role of copepod dynamics as a filter of trophic variability. Hydrobiologia 167/168:61–71
Runge JA, Simard Y (1990) Zooplankton of the St. Lawrence Estuary: the imprint of physical processes on its composition and dynamics, Chap 13. In: El-Sabh MI, Silverberg N (eds) Oceanography of a large-scale estuarine system: the St. Lawrence. Springer-Verlag, New York, pp 296–320
Runge JA (1992) Transfer of phycotoxins in the pelagic food web (Report of Working Group #4) In: Therriault J-C, levasseur M (eds) Proceedings of the third Canadian workshop on harmful marine algae. Can tech Rep Fish aquat Sci 1893:73–80
Sullivan JJ, Wekell MM (1986) The application of high performance liquid chromatography in a paralytic shellfish poisoning program. In: Kramer DE, Liston J (eds) Seafood quality determination. Elsevier, New York, pp 357–371
Sykes PF, Huntley ME (1987) Acute physiological reactions of Calanus pacificus to selected dinoflagellates; direct observations. Mar Biol 94:19–24
Therriault J-C, Painchaud J, Levasseur M (1985) Factors controlling the occurrence of Protogonyaulax tamarensis and shellfish toxicity in the St. Lawrence Estuary: fresh-water runoff and the stability of the water column. In: Anderson DM, White AW, Baden DG (eds) Toxic dinoflagellates. Elsevier, New York, pp 141–146
Uye S, Takamatsu K (1990) Feeding interactions between planktonic copepods and red-tide flagellates from Japanese coastal waters. Mar Ecol Prog Ser 59:97–107
Watras CJ, Garcon VC, Olson RJ, Chisholm SW, Anderson DM (1985) The effect of zooplankton grazing on estuarine blooms of the toxic dinoflagellate Gonyaulax tamarensis. J Plankton Res 7:891–908
White AW (1980) Recurrence of fish kills of Atlantic herring (Clupea harengus harengus) caused by dinoflagellate toxins transferred through herbivorous zooplankton. Can J Fish aquat Sciences 37:2262–2265
White AW (1981) Marine zooplankton can accumulate and retain dinoflagellate toxins and cause fish kills. Limnol Oceanogr 26:103–109
White AW (1982) The scope of impact of toxic dinoflagellate blooms on finfish of Canada. Can tech Rep Fish aquat Sci 1063:1–5
White HH (1979) Effects of dinoflagellate bioluminescence on the ingestion rates of herbivorous zooplankton. J exp mar Biol Ecol 36:217–224
Author information
Authors and Affiliations
Additional information
Communicated by R. J. Thompson, Saint John's
Rights and permissions
About this article
Cite this article
Turriff, N., Runge, J.A. & Cembella, A.D. Toxin accumulation and feeding behaviour of the planktonic copepod Calanus finmarchicus exposed to the red-tide dinoflagellate Alexandrium excavatum . Marine Biology 123, 55–64 (1995). https://doi.org/10.1007/BF00350323
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00350323