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Marine Biology

, Volume 151, Issue 4, pp 1205–1214 | Cite as

Effects of the toxic dinoflagellate Gymnodinium catenatum on uptake and fate of paralytic shellfish poisons in the Pacific giant lions-paw scallop Nodipecten subnodosus

  • Norma A. Estrada
  • Nestor Lagos
  • Carlos García
  • Alfonso N. Maeda-Martínez
  • Felipe Ascencio
Research Article

Abstract

Juvenile Pacific giant lions-paw scallops Nodipecten subnodosus were fed the toxic dinoflagellate Gymnodinium catenatum, a producer of paralytic shellfish poison (PSP), supplied with Isochrysis galbana (a nontoxic microalgae). Short-term (<24 h) experiments were performed to determine clearance and ingestion rates of G. catenatum. Kinetics of PSP was examined in longer-term experiments (>2 days). At high food concentrations, juvenile scallops showed production of pseudofeces, partial shell valve closure, and reduction in feeding. According to HPLC analysis, the only toxins present in the dinoflagellate G. catenatum and in the scallops were the gonyautoxins (GTXs), except in the labial palps and digestive gland, where trace amounts of saxitoxin (STX) were present in scallops. These tissues could play an important role in toxin biotransformation. The ranking of toxin concentration in tissues was: digestive gland > labial palps > intestine > gills > mantle > adductor muscle, where the total contribution of viscera was more than 80% of the total toxin body burden. Juvenile scallops exhibited no apparent detrimental physiological responses during the long-term feeding experiment. The dinoflagellate may contribute nutrients to the scallop, in addition to the microalgae I. galbana. The dinoflagellate may enhance cell uptake and byssus production. Once PSP accumulated during the first 12 days, it was slowly eliminated. The limited capacity for accumulating toxins in the adductor muscle favors domestic marketing of scallops.

Keywords

Bivalve Dinoflagellate Digestive Gland Paralytic Shellfish Poison Saxitoxin 
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.

Notes

Acknowledgments

We thank personnel at the Laboratorio de Bioquímica de Membrana of the Universidad de Chile for analyzing toxins and M. de Jesus Romero for assistance with laboratory work at CIBNOR. Financial support was provided by Centro de Investigaciones Biológicas del Noroeste (CIBNOR grant AC 3.1) and Consejo Nacional de Ciencia y Tecnología of Mexico (CONACYT fellowship 172583) to N.A.E.

References

  1. Anderson DM, Kulis DM, Sullivan JJ, Hall S, Lee C (1990) Dynamics and physiology of saxitoxin production by the dinoflagellates Alexandrium spp. Mar Biol 104:511–524CrossRefGoogle Scholar
  2. Andrinolo D, Santinelli N, Otaño S, Sastre V, Lagos N (1999) Paralytic shellfish toxins in mussels and Alexandrium tamarense at Valdes Peninsula, Chubut, Patagonia Argentina: Kinetic of natural depuration. J Shellfish Res 18:203–209Google Scholar
  3. Balech E (1964) El plancton de Mar de Plata durante el periodo 1961–1962. Bol Inst Biología Marina U. Nat., Buenos Aires, Mar de Plata 4:1–42Google Scholar
  4. Bardouil M, Bohec M, Cormerais M, Bougrier S, Lassus P (1993) Experimental study of the effects of a toxic microalgal diet on feeding of the oyster Crassostrea gigas Thunberg. J Shellfish Res 12:417–422Google Scholar
  5. Bauder AG, Cembella AD, Bricelj VM, Quilliam MA (2001) Uptake and fate of diarrhetic shellfish poisoning toxins from the dinoflagellate Prorocentrum lima in the bay scallop Argopecten irradians. Mar Ecol Prog Ser 3:39–52CrossRefGoogle Scholar
  6. Berntsson KM, Jonsson PR, Wanberg SA, Carlsson AS (1997) Effects of broodstock diets on fatty acid composition, survival and growth rates in larvae of the European flat oyster, Ostrea edulis. Aquaculture 154:139–153CrossRefGoogle Scholar
  7. Blackburn SI, Hallegraeff GM, Bolch CJS (1989) Vegetative reproduction and sexual life cycle of the toxic dinoflagellate Gymnodinium catenatum from Tasmania, Australia. J Phycol 25:577–590CrossRefGoogle Scholar
  8. Blanco-Pérez J, Morono A, Franco J, Reyero MI (1997) PSP detoxification kinetics in the mussel Mytilus galloprovincialis. One and two compartment models and the effect of some environmental variables. Mar Ecol Prog Ser 158:165–175CrossRefGoogle Scholar
  9. Bricelj MV, Lee JH, Cembella AD, Anderson DM (1990) Uptake kinetics of paralytic shellfish toxins from the dinoflagellate Alexandrium fundyense in the mussel Mytilus edulis. Mar Ecol Prog Ser 63:177–188CrossRefGoogle Scholar
  10. 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
  11. Bricelj VM, Cembella A (1995) Fate of gonyautoxins in surfclams, Spisula solidissima, grazing upon toxigenic Alexandrium. In: Lassus P, Arzul G, Erard E, Gentien P, Marcaillou C (eds) Proceedings of the 6th international conference on toxic marine phytoplankton, Nantes, France, Lavoisier, Paris, pp 413–418Google Scholar
  12. Bricelj VM, Laby D, Cembella AD (1996a) Differential sensitivity and PSP toxin accumulation in two clam species, Spisula solidissima and Mya arenaria. J Shellfish Res 15:502Google Scholar
  13. Bricelj VM, Cembella AD, Lavy D, Shumway SE, Cucci TL (1996b) Comparative phisiological and behavioral responses to PSP toxins in two bivalve molluscs, the softshell clam, Mya arenaria, and surfclam, Spisula solidissima. In: Yasumoto T, Oshima Y, Fukuyo Y (eds) Harmful and toxic algal blooms. UNESCO, París, pp 405–408Google Scholar
  14. Bricelj VM, Shumway SE (1998) Paralytic shellfish toxins in bivalve molluscs: occurrence, transfer kinetics, and biotransformation. Rev Fish Sci 6:315–383CrossRefGoogle Scholar
  15. Cembella AD, Lewis NI, Shumway SE (1993) An interespecific comparison of paralytic shellfish poisons in marine bivalves: anatomical and spatio-temporal variation in toxin composition. J Shellfish Res 12:389–403Google Scholar
  16. Cembella AD, Shumway SE, Larocque R (1994) Sequestering and putative biotransformation of paralytic shellfish toxins by the sea scallop Placopecten magellanicus: Seasonal and spatial scales in natural populations. J Exp Mar Biol Ecol 180:1–22CrossRefGoogle Scholar
  17. Coughland J (1969) The estimation of filtering rate from the clearance of suspension. Mar Biol 2:356–358CrossRefGoogle Scholar
  18. Díaz MA, Martínez G (1992) Efecto de diferentes dietas sobre el balance energético en juveniles de Argopecten purpuratus L. Rev Biol Mar Valparaiso 27:163–173Google Scholar
  19. Dupuy JL, Sparks AK (1967) Gonyaulax washingtonensis, its relationship to Mytilus californianus and Crassostrea gigas as a source of paralytic shellfish toxin in Sequim Bay, Washington. Proc Natl Shellfisheries Assoc 58:2Google Scholar
  20. Franca S, Almeida JF (1989) Paralytic shellfish poisons in bivalve molluscs on the Portuguese coast caused by a bloom of the dinoflagellate Gymnodinium catenatum. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides: biology, environmental science and toxicology. Elsevier, New York, pp 93–96Google Scholar
  21. Fukuyo Y, Kodama M, Ogata T, Ishimaru T, Matsuoka K, Okaichi T, Maala MA, Ordones JA (1993) Occurrence of Gymnodinium catenatum in Manila Bay, The Philippines. In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton in the sea. Elsevier, Amsterdam, pp 875–880Google Scholar
  22. García C, Mardones P, Sfeir A, Lagos N (2004) Simultaneous presence of paralytic and diarrheic shellfish poisoning toxins in Mytilus chilensis samples collected in the Chiloe Island, Austral Chilean Fjords. Biol Res 37:721–731CrossRefGoogle Scholar
  23. Gainey LF, Shumway SE (1988) A compendium of the responses of bivalve mollusks to toxic dinoflagellates. J Shellfish Res 7:623–628Google Scholar
  24. Graham HW (1943) Gymnodinium catenatum, a new dinoflagellate from the Gulf of California. Trans Am Microsc Soc 62:259–261CrossRefGoogle Scholar
  25. Hall S, Strichartz G, Moczydlowski E, Ravindran A, Reichardt PB (1990) The saxitoxins: sources, chemistry and pharmacology. In: Hall S, Strichartz GR (eds) Marine toxins. ACS Symposium Series 418, American Chemical Society, Washington, DC, pp 29–65CrossRefGoogle Scholar
  26. Halstead BW, Schantz EJ (1984) Paralytic Shellfish Poisoning. WHO Offset Publication, World Health Organization, Geneva, Switzerland 79:1–60Google Scholar
  27. Hallegraeff GM, Stanley SO, Bolch CJ, Blackburn CI (1989) Gymnodinium catenatum blooms and shellfish toxicity in Southern Tasmania, Australia. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides: biology, environmental science and toxicology. Elsevier, New York, pp 77–80Google Scholar
  28. Ikeda T, Matsumoto S, Sato S, Ogata T, Kodama M, Fukuyo Y, Takayama H (1989) First report on paralytic shellfish poisoning caused by Gymnodinium catenatum Graham (Dynophyceae) in Japan. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides: biology, environmental science and toxicology. Elsevier, New York, pp 411–414Google Scholar
  29. Keen AM (1972) Sea shells of tropical west America. Stanford University Press, Stanford, pp 1064Google Scholar
  30. Kvitek RG, Beitler MK (1988) A case for sequestering of paralytic shellfish toxins as a chemical defense. J Shellfish Res 7:629–636Google Scholar
  31. La Barbera-Sanchez A, Gamboa-Maruez JF (2001) Distribution of Gymnodinium catenatum Graham and shellfish toxicity on the coast of Sucre state, Venezuela, from1989 to 1998. J Shellfish Res 20:1257–1261Google Scholar
  32. Lagos N (1998) Microalgal blooms: a global issue with negative impact in Chile. Biol Res 31:375–386PubMedGoogle Scholar
  33. Lagos N (2003) Paralytic shellfish poisoning phycotoxins: occurrence in South America. Comments Toxicol 9:175–193CrossRefGoogle Scholar
  34. Landsberg JH (1996) Neoplasia and biotoxins in bivalves: is there a connection? J Shellfish Res 15:203–230Google Scholar
  35. Lassus P, Bardouil M, Ledoux M, Murail I, Bohec M, Truquet P, Fremy JM, Romer V (1992) Paralytic phycotoxin uptake by scallops (Pecten maximus). Aquat Living Resources 5:319–324CrossRefGoogle Scholar
  36. Lehane (2000) Paralytic shellfish poisoning: a review. National Office of Animal and Plant Health, Agriculture. Fisheries and Forestry, Australia, CanberraGoogle Scholar
  37. 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
  38. Lodeiros C, Rengel J, Freites L, Morales F. Himmelman JH (1998) Growth and survival of the tropical scallop Lyropecten (Nodipecten) nodosus, maintained in suspended culture at three depths. Aquaculture 165:41–50CrossRefGoogle Scholar
  39. Lora-Vilchis MC, Doktor MN (2001) Evaluation of seven algal diets for spat of the Pacific scallop Argopecten ventricosus. J World Aquac Soc 32:228–235CrossRefGoogle Scholar
  40. Mansour MP, Volkman JK , Jackson AE, Blackburn SI (1999) The fatty acid and sterol composition of five marine dinoflagellates. J Phycol 35:710–720CrossRefGoogle Scholar
  41. Mansour MP, Volkman JK, Holdworth DG, Jackson AE, Blackburn SI (1999b) Very long-chain (C28) highly unsaturated fatty acids in marine dinoflagellates. Phytochemistry 50:541–548CrossRefGoogle Scholar
  42. Mansour MP, Volkman JK , Blackburn SI (2003) The effect of growth phase on the lipid class, fatty acid and sterol composition in the marine dinoflagellate, Gymnodinium sp. in batch culture. Phytochemistry 63:145–153CrossRefGoogle Scholar
  43. Matsuyama Y, Uchida T, Honjo T (1999) Effects of harmful dinoflagellates, Gymnodinium mikimotoi and Heterocaspa circularisquama, red-tide on filtering rate of bivalve molluscs. Fish Sci 65:248–253CrossRefGoogle Scholar
  44. Napolitano GE, Ackman RG (1993) Fatty acid dynamics in sea scallops Placopecten magellanicus (Gmelin 1971) from Georges Bank, Nova Scotia. J Shellfish Res 12:267–277Google Scholar
  45. Noguchi T, Daigo K, Hashimoto K (1985) Release of paralytic shellfish poison from the exoesqueleton of a Xhantid crab Zosimus aeneus. In: Anderson DM, White AW, Baden DG (eds) Toxic dinoflagellates. Elsevier, New York, pp 293–298Google Scholar
  46. Oshima Y, Blackburn S, Hallegraeff GM (1993) Comparative study on paralytic shellfish toxin profile of the dinoflagellate Gymnodinium catenatum from three different countries. Mar Biol 116:471–476CrossRefGoogle Scholar
  47. Oshima Y (1995a) Postcolumn derivatization liquid chromatographic method for paralytic shellfish toxins. J AOAC Int 78:528–532Google Scholar
  48. Oshima Y (1995b) Chemical and enzymatic transformation of paralytic shellfish toxins in marine organism. In: Lassus P, Arzul G, Erard-Le-Dunn E, Gentien P, Marquillou-Le-Baut C (eds) Harmful marine algal blooms. technique et documentation. Lavoisier, Paris, pp 475–480Google Scholar
  49. Robinson A (1992) Dietary supplements for the reproductive conditioning of Crassostrea gigas kumamoto (Thunberg). II Efects on glycogen, lipid and fatty acid content of broodstock oysters and eggs. J Shellfish Res 11:433–447Google Scholar
  50. Shumway SE, Cucci TL (1987) The effects of the toxic dinoflagellate Protogonyaulax tamarensis on the feeding and behaviour of bivalve mollusc. Aquat Toxicol 10:9–27CrossRefGoogle Scholar
  51. Shumway SE, Cembella AD (1993) The impact of toxic algae on scallop culture and fisheries. Rev Fish Sci 1:121–150CrossRefGoogle Scholar
  52. Shumway SE, Cucci TL, Lesser MP, Bourne N, Bunting B (1997) Particle clearance and selection in three species of juvenile scallops. Aquac Int 5:89–99CrossRefGoogle Scholar
  53. Sullivan JJ (1988) Methods of analysis for DSP and PSP toxins in shellfish. J Shellfish Res 7:587–595Google Scholar
  54. Trider DJ, Castell JD (1979) Effect of dietary lipids on growth, tissue composition and metabolism of the oyster (Crassostrea virginica). J Nutr 110:1303–1309CrossRefGoogle Scholar
  55. Viquez R, Hargraves PE (1995) Anual cycle of potentially harmful dinoflagellates in the Golfo de Nicoya, Costa Rica. Bull Mar Sci 57:467–475Google Scholar
  56. Wildish DJ, Saulnier AM (1993) Hydrodynamic control of filtration in Placopecten magellanicus. J Exp Mar Biol Ecol 174:65–82CrossRefGoogle Scholar
  57. Yuki K., Yoshimatsu S (1987) Morphology of the athecate dinoflagellate Gymnodinium catenatum in culture. Bull Plankton Soc Jpn 34:109–117Google Scholar
  58. Zou Y, Zhu M, Wu R (2001) Accumulation and depuration of paralytic shellfish poisons (PSP) in Chinese scallop Chlamys farrerei. In: Book of abstracts, 2nd international conference on harmful algae management and mitigation, Qingdao, 12–16 November 2001, pp 122Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Norma A. Estrada
    • 1
  • Nestor Lagos
    • 2
  • Carlos García
    • 2
  • Alfonso N. Maeda-Martínez
    • 1
  • Felipe Ascencio
    • 1
  1. 1.Departamento de Patología MarinaCentro de Investigaciones Biológicas del Noroeste (CIBNOR)La PazMexico
  2. 2.Laboratorio Bioquímica de Membrana, Departamento de Fisiología y Biofísica, Facultad de MedicinaUniversidad de ChileSantiagoChile

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