Marine Biology

, Volume 151, Issue 5, pp 2003–2012 | Cite as

Transfer of brevetoxins to a tellinid bivalve by suspension- and deposit-feeding and its implications for clay mitigation of Karenia brevis blooms

  • Anne-Gaëlle HauboisEmail author
  • V. Monica Bricelj
  • Jerôme Naar
Research Article


Blooms of the brevetoxin-producing Karenia brevis in the Gulf of Mexico cause massive fish kills, food poisoning and adverse respiratory effects in humans. Sedimentation of toxic cells following inert clay application could reduce toxin incorporation by commercially important suspension-feeding bivalves and thus prevent direct public health impacts, but could potentially lead to brevetoxin (PbTx) accumulation by benthic deposit-feeders. The goal of this study was therefore to compare suspension- and deposit-feeding as pathways for brevetoxins. We investigated: (1) the effect of toxic K. brevis on both feeding modes using a facultative deposit-suspension feeding tellinid bivalve, the clam Macoma balthica, as a model species and (2) the relative effectiveness of brevetoxin transfer via suspension- and deposit-feeding over 24-h exposure. Sedimentation of K. brevis was achieved by treatment with 0.25 g phosphatic clay l−1 and brevetoxin concentrations were measured by ELISA. Karenia brevis reduced both suspension- and deposit-feeding activity. This study demonstrates that brevetoxins can be rapidly accumulated by a surface deposit-feeding bivalve from sedimented K. brevis cells and that comparable toxin levels can be attained by both suspension- and deposit-feeding modes [1.2–1.6 μg PbTx (g tissue wet weight)−1]. Deposit-feeding clams generally do not pose a direct threat to humans but may provide a pathway for brevetoxin food web transfer.


Dinoflagellate Macoma Balthica Toxic Dinoflagellate Clam Tissue Inhalant Siphon 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Funding for this work was provided by NOAA ECOHAB via a grant awarded to D. Anderson at WHOI, USA. We thank D. Anderson and M. Sengco (WHOI) for providing clay and the K. brevis Wilson strain, R. Pierce (Mote Marine Lab, FL, USA) for his helpful advice, and the research team from the shellfish lab at IMB/NRC for assistance in clam sampling.


  1. Anderson DM (1997) Turning back the harmful red tide. Nature 388:513–515CrossRefGoogle Scholar
  2. Archambault MC, Bricelj VM, Grant J, Anderson DM (2004) Effects of suspended and sedimented clays on juvenile hard clams, Mercenaria mercenaria, within the context of harmful algal bloom mitigation. Mar Biol 144:553–565CrossRefGoogle Scholar
  3. Baden DG, Mende TJ, Szmant AM, Trainer VL, Edwards RA, Roszell LE (1988) Brevetoxin binding: molecular pharmacology versus immunoassay. Toxicon 26:97–103CrossRefGoogle Scholar
  4. Bardouil M, Bohec M, Bougrier S, Lassus P, Truquet P (1996) Feeding responses of Crassostrea gigas (Thunberg) to inclusion of different proportions of toxic dinoflagellates in their diet. Oceanol Acta 19:177–182Google Scholar
  5. Bayne BL, Iglesias JIP, Hawkins AJS, Navarro E, Heral M, Deslous-Paoli JM (1993) Feeding behavior of the mussel Mytilus edulis. Mar Ecol Prog Ser 55:47–54CrossRefGoogle Scholar
  6. Bricelj VM, Lee JH, Cembella AD (1991) Influence of dinoflagellate cell toxicity on uptake and loss of paralytic shellfish toxins in the northern quahog Mercenaria mercenaria. Mar Ecol Prog Ser 74:33–46CrossRefGoogle Scholar
  7. Bricelj MV, Cembella AD, Laby D, Shumway SE, Cucci TL (1996) Comparative physiological and behavioral responses to PSP toxins in two bivalve mollusks, the soft clam, Mya arenaria, and surfclam, Spisula solidissima. In: Yasomoto Y, Oshima Y, Fukuyo Y (eds) Harmful and toxic algal blooms. IOC-UNESCO, Paris, pp 405–408Google Scholar
  8. Camp DK, Lyons WG, Perkins TH (1998) Checklist of selected shallow-water marine invertebrates of Florida. Florida Marine Research Institute Technical Report, 239 pGoogle Scholar
  9. Colin SP, Dam HG (2003) Effects of the toxic dinoflagellate Alexandrium fundyense on the copepod Acartia hudsonica: a test of the mechanisms that reduce ingestion rates. Mar Ecol Prog Ser 248:55–65CrossRefGoogle Scholar
  10. Dickey RW, Plakas SM, Jester ELE, Elsiad KR, Johannessen JN, Flewelling LJ, Scott P, Hammond DG, VanDolah FM, Leighfield TA, Bottein Y, Ramsdell JS, Busman M, Moeller PD, Pierce RH, Henry MS, Poli MA, Walker CS, Kurtz J, Naar J, Baden DG, Musser SM, Truman P, Quilliam MA, Stirling D, Hawryluk TP, Wekell MM, Hungerford JM, Yoshimoto K (2004) Multi-laboratory study of five methods for the determination of brevetoxins in shellfish tissue extracts. In: Steidinger K (ed) Harmful algae 2002, pp 300–303Google Scholar
  11. Fletcher GC, Hay BE, Scott MF (1998) Detoxifying Pacific oysters (Crassostrea gigas) of the neurotoxic shellfish poison (NSP) produced by Gymnodinium breve. J Shell Res 17:1637–1641Google Scholar
  12. Flewelling LJ, Naar JP, Abbott JP, Baden DG, Barros NB, Bossart GD, Bottein MYD, Hammond DG, Haubold EM, Heil CA, Henry MS, Jacocks HM, Leighfield TA, Pierce RH, Pitchford TD, Rommel SA, Scott PS, Steidinger KA, Truby EW, Van Dolah FM, Landsberg JH (2005) Red tides and marine mammal mortalities. Nature 435:755–756CrossRefGoogle Scholar
  13. Greene RM, Walker CC, Murrell MC, Kurtz JC, Stanley RS, Genthner FG (2000) High brevetoxin concentrations in Gymnodinium breve blooms along the northwest Florida coast during 1999. J Phycol 36:25–26CrossRefGoogle Scholar
  14. Guillard RRL, Hargrave BT (1993) Stichochyisis immobilis is a diatom, not a chrysophyte. Phycologia 32:234–236CrossRefGoogle Scholar
  15. Hua Y, Lu W, Henry MS, Pierce RH, Cole RB (1996) On-line liquid chromatography-electrospray ionization mass spectrometry for determination of the brevetoxin profile in natural “red tide” algae blooms. J Chromato A 750:115–125CrossRefGoogle Scholar
  16. Hughes RN (1969) A study of feeding in Scrobicularia plana. J Mar Biol Assoc UK 49:805–823CrossRefGoogle Scholar
  17. Hummel H (1985) Food intake and growth in Macoma balthica (Mollusca) in the laboratory. Neth J Sea Res 19:77–83CrossRefGoogle Scholar
  18. Ishida H, Nozawa A, Nukaya H, Rhodes L, McNabb P, Holland PT, Tsuji K (2004) Confirmation of brevetoxin metabolism in cockle, Austrovenus stutchburyi, and greenshell mussels, Perna canaliculus, associated with New Zealand neurotoxic shellfish poisoning, by controlled exposure to Karenia brevis. Toxicon 43:701–712CrossRefGoogle Scholar
  19. Kirkpatrick B, Flemming LE, Squicciarini D, Backer LC, Clark R, Abraham W, Benson J, Cheng YS, Johnson D, Pierce R, Zaias J, Bossart GD, Baden DG (2004) Literature review of Florida red tide: implications for human health effects. Harmful Algae 3:99–115CrossRefGoogle Scholar
  20. Lassus P, Bardouil M, Beliaeff B, Masselin P, Naviner M, Truquet P (1999) Effect of a continuous supply of the toxic dinoflagellate Alexandrium minutum on the feeding behavior of the Pacific oyster (Crassostrea gigas). J Shellfish Res 18:211–216Google Scholar
  21. Lesser MP, Shumway SE (1993) Effects of toxic dinoflagellates on clearance rates and survival in juveniles bivalve mollusks. J Shellfish Res 12:377–381Google Scholar
  22. Leverone JR, Shumway SE, Blake NJ (2007) Comparative effects of the toxic dinoflagellate Karenia brevis on clearance rates in juveniles of four bivalve molluscs from Florida, USA. Toxicon (in press)Google Scholar
  23. Levinton JS (1991) Variable feeding behavior in three species of Macoma (Bivalvia: Tellinacea) as a response to water flow and sediment transport. Mar Biol 110:375–383CrossRefGoogle Scholar
  24. Lewis MA, Dantin DD, Walker CC, Kurtz JC, Greene RM (2003) Toxicity of clay flocculation of the toxic dinoflagellate, Karenia brevis, to estuarine invertebrates and fish. Harmful Algae 2:235–246CrossRefGoogle Scholar
  25. Li SC, Wang WX, Hsieh DPH (2001) Feeding and absorption of the toxic dinoflagellate Alexandrium tamarense by two marine bivalves from the South China Sea. Mar Biol 139:617–624CrossRefGoogle Scholar
  26. Mackenzie L, Rhodes L, Till D, Chang FK, Kaspar H, Haywood A, Kapa J, Walker B (1995) A Gymnodinium sp. Bloom and contamination of shellfish with lipid soluble toxins in New Zealand, Jan–April 1993. In: Lassus P et al (eds) Harmful marine algal blooms. Intercept Ltd, France, pp 795–800Google Scholar
  27. Magana HA, Contreras C, Villareal TA (2003) A historical assessment of Karenia brevis in the western Gulf of Mexico. Harmful Algae 2:163–171CrossRefGoogle Scholar
  28. Matsuyama Y, Uchida T, Honjo T (1999) Effect of harmful dinoflagellates, Gymnodinium mikimotoi and Heterocapsa circularisquama, red-tide on filtering rate of bivalves mollusks. Fish Sci 65:248–253CrossRefGoogle Scholar
  29. Morohashi A, Satake M, Naoki H, Kaspar HF, Oshima Y, Yasumato T (1999) Brevetoxin B4 isolated from greenshell mussels Perna canaliculus, the major toxin involved in neurotoxic shellfish poisoning in New Zealand. Nat Toxins 7:45–48CrossRefGoogle Scholar
  30. Na G, Choi W, Chun Y (1996) A study on red tide control with loess suspension. J Aquac 9:239–245Google Scholar
  31. Naar J. Bourdelais A, Tomas C, Kubanek J, Whitney PL, Flewelling L, Steidinger K, Lancaster J, Baden DG (2002) A competitive ELISA to detect brevetoxins from Karenia brevis (formely Gymnodinium breve) in seawater, shellfish, and mammalian body fluid. Environ Health Perspect 110:179–185CrossRefGoogle Scholar
  32. Naar J, Flewelling L, Lenzi A, Landsberg J, Jacocks H, Musser S, Bourdelais A, Steidinger K, Baden D (2003) Experimental bioaccumulation of ichthyotoxic brevetoxins in healthy fish. Poster at the Second Symposium on Harmful Marine Algae in the US, Woods Hole, Massachusetts***Google Scholar
  33. Naar J, Weidner A, Kubanek J, Flewelling L, Bourdelais A, Jacocks H, Steidinger KA, Pierce R, and Baden DG (2004) Bioaccumulation, biodepuration, and biotransformation of brevetoxins by shellfish: an issue for shellfish monitoring. In: Steidinger, K (ed) Harmful algae 2002, pp 488–490Google Scholar
  34. O’Shea TJ, Rathbun GB, Bonde RK, Buergelt CD, Odell DK (1991) An epizootic of Florida manatees associated with a dinoflagellate bloom. Mar Mamm Sci 7:165–179CrossRefGoogle Scholar
  35. Pierce RH (1986) Red tide (Ptychodiscus brevis) toxin aerosols: a review. Toxicon 24:955–965CrossRefGoogle Scholar
  36. Pierce RH, Henry MS, Blum PC, Lyons JI, Cheng YS, Yazzie D, Zhou Y (2003) Brevetoxin concentrations in marine aerosol: human exposure levels during a Karenia brevis harmful algal bloom. Bull Environ Contam Toxicol 70:161–165CrossRefGoogle Scholar
  37. Pierce RH, Henry MS, Higham CJ, Blum PC, Sengco MR, Anderson DM (2004) Removal of harmful algal cells (Karenia brevis) and toxins from seawater culture by clay flocculation. Harmful Algae 3:141–148CrossRefGoogle Scholar
  38. Plakas SM, El Said KR, Jester ELE, Granade HR, Musser SM, Dickey RW (2002) Confirmation of brevetoxin metabolism in the eastern oyster (Crassostrea virginica) by controlled exposures to pure toxins and to Karenia brevis cultures. Toxicon 40:721–729CrossRefGoogle Scholar
  39. Plakas SM, Wang Z, ElSaid KR, Jester ELE, Granade HR, Flewelling LJ, Scott P, Dickey RW (2004) Brevetoxin metabolism and elimination in the Eastern oyster (Crassostrea virginica) after controlled exposures to Karenia brevis. Toxicon 44:677–685CrossRefGoogle Scholar
  40. Poli MA, Musser SM, Dickey RW, Eilers PP, Hall S (2000) Neurotoxic shellfish poisoning and brevetoxin metabolites: a case study from Florida. Toxicon 38:981–993CrossRefGoogle Scholar
  41. Rossi F, Herman PMJ, Middelburg JJ (2004) Interspecific and intraspecific variation in δ13C and δ15N in deposit- and suspension-feeding bivalves (Macoma balthica and Cerastoderma edule): evidence of ontogenic changes in feeding mode of Macoma balthica. Limnol Oceanogr 49:408–414CrossRefGoogle Scholar
  42. Roszell LE, Schulman LS, Baden DG (1990) Toxin profiles are dependent on growth stages in cultured Ptychodiscus brevis. In: Graneli E et al (eds) Toxic marine phytoplankton. Elsevier, Amsterdam, pp 403–406Google Scholar
  43. Sengco MR, Li A, Tugend K, Kulis D, Anderson DM (2001) Removal of red- and brown-tide cells using clay flocculation. 1. Laboratory culture experiments with Gymnodinium breve and Aureococcus anophagefferens. Mar Ecol Prog Ser 210:41–53CrossRefGoogle Scholar
  44. Shumway SE, Cucci TL, Newell RC, Yentsch CM (1985) Particle selection, ingestion, and absorption in filter-feeding bivalves. J Exp Mar Biol Ecol 91:77–92CrossRefGoogle Scholar
  45. Taghon GL (1981) Beyond selection: optimal ingestion rate as a function of food value. Am Nat 118:202–214CrossRefGoogle Scholar
  46. Tester PA, Steidinger KA (1997) Gymnodinium breve red tide blooms: initiation, transport, and consequences of surface circulation. Limnol Oceanogr 42:1039–1051CrossRefGoogle Scholar
  47. Tester PA, Turner JT, Shea D (2000) Vectorial transport of toxins from dinoflagellate Gymnodinium breve through copepods to fish. J Plankton Res 22:47–61CrossRefGoogle Scholar
  48. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge, p 504Google Scholar
  49. Ward JE, Shumway SE (2004) Separating the grain from the chaff: particle selection in suspension- and deposit-feeding bivalves. J Exp Mar Biol Ecol 300:83–130CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Anne-Gaëlle Haubois
    • 1
    Email author
  • V. Monica Bricelj
    • 1
  • Jerôme Naar
    • 2
  1. 1.Institute for Marine BiosciencesNational Research Council of CanadaHalifaxCanada
  2. 2.Center for Marine ScienceUniversity of North Carolina at WilmingtonWilmingtonUSA

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