Marine Biology

, Volume 154, Issue 1, pp 81–90 | Cite as

Effects of the dinoflagellates Karlodinium veneficum and Prorocentrum minimum on early life history stages of the eastern oyster (Crassostrea virginica)

  • Diane K. Stoecker
  • Jason E. Adolf
  • Allen R. Place
  • Patricia M. Glibert
  • Donald W. Meritt
Research Article


The bloom-forming dinoflagellates Prorocentrum minimum and Karlodinium veneficum can have detrimental effects on some marine life, including shellfish, but little is known about their effects on early life history stages of bivalves. In the Chesapeake Bay region, blooms of these dinoflagellates overlap with the spawning season of the eastern oyster, Crassostrea virginica. In laboratory experiments, we compared the effects of P. minimum and K. veneficum on the survival and development of embryos and larvae of the eastern oyster. At 104 cells ml−1, P. minimum did not have a negative effect on embryos and larvae in 2-day exposures. The yield of D-hinge larvae was equal to or greater than in control treatments. At 2 × 104 cells ml−1 (approximately equal biomass to the P. minimum treatment) K. veneficum caused significant mortality to oyster embryos within 1 day and almost no embryos developed into D-hinge larvae. This effect was not alleviated by the provision of an alternate food source (Isochrysis sp.). Significant mortality was observed when larvae were exposed to K. veneficum at concentrations of 104 cells ml−1 (approximately 5 ng ml−1 of karlotoxin). The K. veneficum cultures used in these experiments were relatively low in toxin content, more toxic strains could be expected to cause mortality at lower cell concentrations. Survival and maturation of embryos and larvae may be reduced when spawns of the eastern oyster coincide with high bloom densities of K. veneficum.


Dinoflagellate Isochrysis Eastern Oyster Toxin Content Early Life History Stage 
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.



We thank K. de la Cerda for her participation in the project, which was supported by a Chesapeake Teacher Research Fellowship, A. Padeletti for assistance in the oyster hatchery, J. Alexander for assistance with algal cultures, and G. H. Wikfors for advice and encouragement. Research conducted in summer 2006 was supported by the NOAA Chesapeake Bay Fisheries Research Program—Non-native Oyster Initiative to UMCES (grant #NA05NMF4571234). Toxin analyses were supported by grants from NOAA Coastal Oceans Program (grant #NA04NOS4780276), Centers for Disease Control and Prevention (Grant #U50/CCU 323376) and the Maryland Department of Health and Mental Hygiene to University of Marine Biotechnology Institute. This is contribution number 4117 from the University of Maryland Center for Environmental Science, contribution number 07-176 from the Center of Marine Biotechnology, and number 219 from the ECOHAB program.


  1. Abbott BC, Ballantine D (1957) The toxin from Gymnodinium veneficum Ballantine. J Mar Biol Ass UK 36:169–189Google Scholar
  2. Adolf JE, Bachvaroff TR, Krupatkina DN, Nonogaki H, Brown PJP, Lewitus AJ, Harvey HR, Place AR (2006) Species specificity and potential roles of Karlodinium micrum toxin. Afr J Mar Sci 28:415–419Google Scholar
  3. Adolf JE, Krupatkina D, Bachvaroff T, Place AR (2007) Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae 6:400–412CrossRefGoogle Scholar
  4. Alexander JA, Stoecker DK, Meritt DW, Alexander ST, Padeletti A, Johns D, Van Heukelem L, Glibert PM (2007) Differential feces and pseudofeces production by the oyster Crassostrea ariakensis when exposed to diets containing harmful dinoflagellate and raphidophyte species. J Shellfish Res (in press)Google Scholar
  5. Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726Google Scholar
  6. Andersen RA, Berges JA, Harrison PJ, Watanabe MM (2005) Appendix A: recipes for freshwater and seawater media. In: Andersen RA (ed) Algal culturing techniques. Elsevier Inc., Academic Press, Amsterdam, pp 429–532Google Scholar
  7. Ballantine D (1956) Two new marine species of Gymnodinium isolated from the Plymouth area. J Mar Biol Ass UK 35:467–474CrossRefGoogle Scholar
  8. Ballantine D, Morton JE (1956) Filtering, feeding, and digestion in the lamellibranch Lasaea rubra. J Mar Biol Ass UK 35:241–274Google Scholar
  9. Bachvaroff TR, Adolf JE, Squier A, Harvey HR, Place AR (2007) Characterization and quantification of karlotoxins by liquid chromatography-mass spectrometry. Harmful Algae, doi: 10.1016/j.hal.2007.10.003
  10. Bachvaroff TR, Adolf JE, Place AR (2008) Phylogeography of Atlantic Coast Karlodinium veneficum Strains: a genetic correlate of toxin type. In: Proceedings of the XII International Harmful Algae Meeting, pp xxx (in press)Google Scholar
  11. Berenberg C, Patterson GW (1981) The relationship between dietary phytosterols and the sterols of wild and cultivated oysters. Lipids 16:276–278CrossRefGoogle Scholar
  12. Braarud T (1959) A red water organism from Walvis Bay (Gymnodinium galatheanum n. sp.). In: Sparck R (ed) Galathea report, Copenhagen, pp 137–138Google Scholar
  13. Bricelj VM, MacQuarrie SP (2007) The effects of brown tide (Aureococcus anophagefferens) on hard clam Mercenaria mercenaria larvae and implications for benthic recruitment. Mar Ecol Prog Ser 331:147–159CrossRefGoogle Scholar
  14. Brownlee EF, Sellner SG, Sellner KG (2005) Prorocentrum minimum blooms: potential impacts on dissolved oxygen and Chesapeake Bay oyster settlement and growth. Harmful Algae 4:593–602CrossRefGoogle Scholar
  15. Brownlee EF, Sellner SG, Sellner KG, Nonogaki H, Adolf JE, Bachvaroff TR, Place AR (2007) Crassostrea ariakensis and C. virginica responses to ichthyotoxic Karlodinium veneficum. J Shellfish Res (in press)Google Scholar
  16. Carriker MR, Gaffney PM (1996) A catalogue of selected species of living oysters (Ostreacea) of the world. In: Kennedy VS, Newell RIE, Eble AF (eds) The Eastern Oyster Crassostrea virginica. Maryland Sea Grant College, College Park, pp 1–18Google Scholar
  17. Dam HG, Colin SP (2005) Prorocentrum minimum (clone Exuv) is nutritionally insufficient, but not toxic to the copepod Acartia tonsa. Harmful Algae 4:575–584CrossRefGoogle Scholar
  18. Deeds JR, Place AR (2006) Sterol-specific membrane interactions with the toxins from Karlodinium micrum (Dinophyceae)—a strategy for self-protection? Afr J Mar Sci 28:421–425Google Scholar
  19. Deeds JR, Reimschuessel R, Place AR (2006) Histopathological effects in fish exposed to the toxins from Karlodinium micrum. J Aquat Anim Health 18:136–148CrossRefGoogle Scholar
  20. Deeds JR, Mazzarcaccaro AA, Terlizzi DE, Place AR (2002a) Treatment options for the control of an icthyotoxic dinoflagellate in an estuarine aquaculture facility: a case study. In: Hall S, Etheridge S, Anderson D, Kleindinst J, Zhu M, Zou Y (eds) Harmful algae management and mitigation Asia–Pacific economic cooperatio (Singapore): APEC Publication #204-MR-04.2, pp 177–181Google Scholar
  21. Deeds JR, Terlizzi DE, Adolf JE, Stoecker DK, Place AR (2002b) Toxic activity from cultures of Gyrodinium galatheanum (Dinophyceae)-a dinoflagellate associated with fish mortalities in an estuarine aquaculture facility. Harmful Algae 1:169–189CrossRefGoogle Scholar
  22. Deeds JR, Kibler SR, Tester PA, Place AR (2004) Geographic strain variation in toxin production in Karlodinium micrum (Dinophyceae) from Southeastern estuaries of the United States. In: Steidinger KA, Landsberg JH, Tomas CR, Vargo GA (eds) Harmful Algae 2002. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, St Petersburg, pp 145–147Google Scholar
  23. Estes RM, Friedman CS, Elston RA, Herwig RP (2004) Pathogenicity testing of shellfish hatchery bacterial isolates on Pacific oyster Crassostrea gigas larvae. Dis Aquat Org 58:223–230PubMedCrossRefGoogle Scholar
  24. Fan C, Glibert PM, Burkholder JM (2003) Characterization of the affinity for nitrogen, uptake kinetics, and environmental relationships for Prorocentrum minimum in natural blooms and laboratory cultures. Harmful Algae 2:283–299CrossRefGoogle Scholar
  25. Fensin EE (2004) Occurrence and ecology of the dinoflagellate Karlodinium micrum in estuaries of North Carolina, USA. In: Steidinger KA, Landsberg JH, Tomas CR, Vargo GA (eds) Harmful Algae 2002. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, St Petersburg, pp 62–64Google Scholar
  26. Fensin EE (2006) Impact of tropical storms and drought on the dinoflagellates Karlodinium micrum and Prorocentrum minimum in estuarine rivers of North Carolina, USA. Afr J Mar Sci 28:277–281Google Scholar
  27. Galimany E, Place AR, Ramón M, Jutson M, Pipe RK (2007) The effects of feeding Karlodinium veneficum (PLY#103; Gymnodinium veneficum Ballantine) to the blue mussel Mytilus edulis. Harmful Algae XXX (available online 2 June 2007)Google Scholar
  28. Garcés E, Delgado M, Masó M, Camp J (1999) In situ growth rate and distribution of the ichthyotoxic dinoflagellate Gyrodinium corsicum Paulmier in an estuarine embayment (Alfacs Bay, NW Mediterranean Sea). J Plankton Res 21:1977–1991CrossRefGoogle Scholar
  29. Garcés E, Fernandez M, Penna A, Van Lenning K, Gutierrez A, Camp J, Zapata M (2006) Characterization of NW Mediterranean Karlodinium spp. (Dinophyceae) strains using morphological, molecular, chemical, and physiological methodologies. J Phycol 42:1096–1112CrossRefGoogle Scholar
  30. Gladu PK, Patterson GW, Wikfors GH, Chitwood DJ, Lusby WR (1990) The occurrence of brassicasterol and epibrassicasterol in the Chromophycota. Comp Biochem Physiol 97B:491–494Google Scholar
  31. Glibert PM, Magnien RE (2004) Harmful algal blooms in the Chesapeake Bay, USA: common species, relationships to nutrient loading, management approaches, successes and challenges. In: Hall S, Etheridge S, Anderson D, Kleindinst J, Zhu M, Zou Y (eds) Harmful algae management and mitigation Asia–Pacific economic cooperatio (Singapore):APEC Publication #204-MR-04.2, pp 48–53Google Scholar
  32. Glibert PM, Magnien RE, Lomas MW, Alexander J, Fan C, Haramoto E, Trice TM, Kana TM (2001) Harmful algal blooms in the Chesapeake and Coastal Bays of Maryland, USA: comparisons of 1997, 1998, and 1999 events. Estuaries 24:875–883CrossRefGoogle Scholar
  33. Glibert PM, Seitzinger S, Heil CA, Burkholder JM, Parrow MW, Codispoti LA, Kelly V (2005) The role of eutrophication in the global proliferation of harmful algal blooms. Oceanography 18:198–209Google Scholar
  34. Glibert PM, Alexander J, Meritt DW, North EW, Stoecker DK (2007) Harmful algae pose additional challenges for oyster restoration: impacts of the harmful algae Karlodinium veneficum and Prorocentrum minimum on early life history stages of the oysters Crassosrtea virginica and Crassostrea ariakensis. J Shellfish Res 26(4):1–7Google Scholar
  35. Gordon AS, Dyer B (2005) Relative contribution of exotoxin and micropredation to icthyotoxicity of two strains of Pfiesteria shumwayae (Dinophyceae). Harmful Algae 4:423–431CrossRefGoogle Scholar
  36. Goshorn D, Deeds J, Tango P, Poukish C, Place A, McGinty M, Butler W, Luckett C, Magnien R (2004) Occurrence of Karlodinium mirum and its association with fish kills in Maryland estuaries. In: Steidinger KA, Landsberg JH, Tomas CR, Vargo GA (eds) Harmful Algae 2002. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, pp 361–363Google Scholar
  37. Grzebyk D, Denardou A, Berland B, Pouchus YF (1997) Evidence of a new toxin in the red-tide dinoflagellate Prorocentrum minimum. J Plankton Res 19:1111–1124CrossRefGoogle Scholar
  38. Hallegraeff GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32:79–99Google Scholar
  39. Heil CA, Glibert PM, Fan CL (2005) Prorocentrum minimum (Pavillard) Schiller—a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4:449–470CrossRefGoogle Scholar
  40. Jeong HJ, Song JY, Lee CH, Kim ST (2004) Feeding by larvae of the mussel Mytilus galloprovincialis on red-tide dinoflagellates. J Shellfish Res 23:185–195Google Scholar
  41. Kempton JW, Lewitus AJ, Deeds JR, Law JM, Wilde SB, Place AR (2002) Toxicity of Karlodinium micrum (Dinophyceae) associated with a fish kill in a South Carolina brackish retention pond. Harmful Algae 1:233–241CrossRefGoogle Scholar
  42. Kroger K, Gardner JPA, Rowden AA, Wear RG (2006) Long-term effects of a toxic algal bloom on subtidal soft-sediment macroinvertebrate communities in Wellington Harbour, New Zealand. Estuar Coastal Shelf Sci 67:589–604CrossRefGoogle Scholar
  43. Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10:113–390CrossRefGoogle Scholar
  44. Leverone JR, Blake NJ, Pierce RH, Shumway SE (2006) Effects of the dinoflagellate Karenia brevis on larval development in three species of bivalve mollusc from Florida. Toxicon 48:75–84PubMedCrossRefGoogle Scholar
  45. Li A, Stoecker DK, Coats DW (2000a) Mixotrophy in Gyrodinium galatheanum (Dinophyceae): grazing responses to light intensity and inorganic nutrients. J Phycol 36:33–45CrossRefGoogle Scholar
  46. Li A, Stoecker DK, Coats DW (2000b) Spatial and temporal aspects of Gyrodinium galatheanum in Chesapeake Bay: distribution and mixotrophy. J Plankton Res 22:2105–2124CrossRefGoogle Scholar
  47. Luckenbach MW, Sellner KG, Shumway SE, Greene K (1993) Effects of 2 bloom-forming dinoflagellates, Prorocentrum minimum and Gyrodinium uncatenum, on the growth and survival of the eastern oyster, Crassostrea virginica (Gmelin 1791). J Shellfish Res 12:411–415Google Scholar
  48. MacKenzie CLJ (1996) Chapter 21. Management of natural populations. In: Kennedy VS, Newell RIE, Eble AF (eds) The eastern oyster Crassostrea virginica. Maryland Sea Grant College, College Park, pp 707–722Google Scholar
  49. Nielsen MV, Strømgren T (1991) Shell growth-response of mussels (Mytilus edulis) exposed to toxic microalgae. Mar Biol 108:263–267CrossRefGoogle Scholar
  50. Padilla DK, Doall MH, Gobler CJ, Hatson A, O’Boyle K (2006) Brown tide alga, Aureococcus anophagefferens, can affect growth but not survivorship of Mercenaria mercenaria larvae. Harmful Algae 5:736–748CrossRefGoogle Scholar
  51. Shumway SE (1990) A review of the effects of algal blooms on shellfish and aquaculture. J World Aquacul Soc 21:65–104CrossRefGoogle Scholar
  52. Shumway SE (1996) Chapter 13. Natural environmental factors. In: Kennedy VS, Newell RIE, Eble AF (eds) The eastern oyster Crassostrea virginica. Maryland Sea Grant College, College Park, pp 467–514Google Scholar
  53. Summerson HC, Peterson CH (1990) Recruitment failure of the bay scallop, Argopecten irradians concentricus, during the 1st red tide, Ptychodiscus brevis, outbreak recorded in North-Carolina. Estuaries 13:322–331CrossRefGoogle Scholar
  54. Tango PJ, Magnien R, Butler W, Luckett C, Luckenbach M, Lacouture R, Poukish C (2005) Impacts and potential effects due to Prorocentrum minimum blooms in Chesapeake Bay. Harmful Algae 4:525–531CrossRefGoogle Scholar
  55. Thompson RJ, Newell RIE, Kennedy VS, Mann R (1996) Chapter 9. Reproductive processes and early development. In: Kennedy VS, Newell RIE, Eble AF (eds) The eastern oyster Crassostrea virginica. Maryland Sea Grant College, College Park, pp 335–370Google Scholar
  56. Vaque D, Felipe J, Sala MM, Calbet A, Estrada M, Alcaraz M (2006) Effects of the toxic dinoflagellate Karlodinium sp. (cultured at different N/P ratios) on micro and mesozooplankton. Sci Mar 70:59–65Google Scholar
  57. Wear RG, Gardner JPA (2001) Biological effects of the toxic algal bloom of February and March 1998 on the benthos of Wellington Harbour, New Zealand. Mar Ecol Progr Ser 218:63–76CrossRefGoogle Scholar
  58. Wikfors GH (2005) A review and new analysis of trophic interactions between Prorocentrum minimum and clams, scallops, and oysters. Harmful Algae 4:585–592CrossRefGoogle Scholar
  59. Wikfors GH, Smolowitz RM (1995) Experimental and histological studies of 4 life-history stages of the Eastern oyster, Crassostrea virginica, exposed to a cultured strain of the dinoflagellate Prorocentrum minimum. Biol Bull 188:313–328CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Diane K. Stoecker
    • 1
  • Jason E. Adolf
    • 2
  • Allen R. Place
    • 2
  • Patricia M. Glibert
    • 1
  • Donald W. Meritt
    • 1
  1. 1.Horn Point LaboratoryUniversity of Maryland Center for Environmental ScienceCambridgeUSA
  2. 2.Center of Marine BiotechnologyUniversity of Maryland Biotechnology InstituteBaltimoreUSA

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