Skip to main content
Log in

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

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abbott BC, Ballantine D (1957) The toxin from Gymnodinium veneficum Ballantine. J Mar Biol Ass UK 36:169–189

    Google Scholar 

  • 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 28:415–419

    Google Scholar 

  • Adolf JE, Krupatkina D, Bachvaroff T, Place AR (2007) Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae 6:400–412

    Article  CAS  Google Scholar 

  • 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)

  • Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726

    Google Scholar 

  • 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 429–532

    Google Scholar 

  • Ballantine D (1956) Two new marine species of Gymnodinium isolated from the Plymouth area. J Mar Biol Ass UK 35:467–474

    Article  Google Scholar 

  • Ballantine D, Morton JE (1956) Filtering, feeding, and digestion in the lamellibranch Lasaea rubra. J Mar Biol Ass UK 35:241–274

    Google Scholar 

  • 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

  • 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)

  • Berenberg C, Patterson GW (1981) The relationship between dietary phytosterols and the sterols of wild and cultivated oysters. Lipids 16:276–278

    Article  CAS  Google Scholar 

  • Braarud T (1959) A red water organism from Walvis Bay (Gymnodinium galatheanum n. sp.). In: Sparck R (ed) Galathea report, Copenhagen, pp 137–138

  • 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 331:147–159

    Article  Google Scholar 

  • Brownlee EF, Sellner SG, Sellner KG (2005) Prorocentrum minimum blooms: potential impacts on dissolved oxygen and Chesapeake Bay oyster settlement and growth. Harmful Algae 4:593–602

    Article  CAS  Google Scholar 

  • 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)

  • 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 1–18

    Google Scholar 

  • Dam HG, Colin SP (2005) Prorocentrum minimum (clone Exuv) is nutritionally insufficient, but not toxic to the copepod Acartia tonsa. Harmful Algae 4:575–584

    Article  CAS  Google Scholar 

  • 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 28:421–425

    Google Scholar 

  • Deeds JR, Reimschuessel R, Place AR (2006) Histopathological effects in fish exposed to the toxins from Karlodinium micrum. J Aquat Anim Health 18:136–148

    Article  Google Scholar 

  • 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 177–181

  • 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 1:169–189

    Article  CAS  Google Scholar 

  • 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 145–147

  • 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 58:223–230

    Article  PubMed  Google Scholar 

  • 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 2:283–299

    Article  CAS  Google Scholar 

  • 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 62–64

  • 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 28:277–281

    Google Scholar 

  • 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)

  • 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 21:1977–1991

    Article  Google Scholar 

  • 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 42:1096–1112

    Article  Google Scholar 

  • Gladu PK, Patterson GW, Wikfors GH, Chitwood DJ, Lusby WR (1990) The occurrence of brassicasterol and epibrassicasterol in the Chromophycota. Comp Biochem Physiol 97B:491–494

    CAS  Google Scholar 

  • 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 48–53

  • 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 24:875–883

    Article  CAS  Google Scholar 

  • 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 18:198–209

    Google Scholar 

  • 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):1–7

    Google Scholar 

  • Gordon AS, Dyer B (2005) Relative contribution of exotoxin and micropredation to icthyotoxicity of two strains of Pfiesteria shumwayae (Dinophyceae). Harmful Algae 4:423–431

    Article  CAS  Google Scholar 

  • 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 361–363

  • Grzebyk D, Denardou A, Berland B, Pouchus YF (1997) Evidence of a new toxin in the red-tide dinoflagellate Prorocentrum minimum. J Plankton Res 19:1111–1124

    Article  CAS  Google Scholar 

  • Hallegraeff GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32:79–99

    Google Scholar 

  • 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 4:449–470

    Article  CAS  Google Scholar 

  • Jeong HJ, Song JY, Lee CH, Kim ST (2004) Feeding by larvae of the mussel Mytilus galloprovincialis on red-tide dinoflagellates. J Shellfish Res 23:185–195

    Google Scholar 

  • 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 1:233–241

    Article  CAS  Google Scholar 

  • 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 67:589–604

    Article  Google Scholar 

  • Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10:113–390

    Article  Google Scholar 

  • 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 48:75–84

    Article  PubMed  CAS  Google Scholar 

  • Li A, Stoecker DK, Coats DW (2000a) Mixotrophy in Gyrodinium galatheanum (Dinophyceae): grazing responses to light intensity and inorganic nutrients. J Phycol 36:33–45

    Article  CAS  Google Scholar 

  • Li A, Stoecker DK, Coats DW (2000b) Spatial and temporal aspects of Gyrodinium galatheanum in Chesapeake Bay: distribution and mixotrophy. J Plankton Res 22:2105–2124

    Article  Google Scholar 

  • 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 12:411–415

    Google Scholar 

  • 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 707–722

    Google Scholar 

  • Nielsen MV, Strømgren T (1991) Shell growth-response of mussels (Mytilus edulis) exposed to toxic microalgae. Mar Biol 108:263–267

    Article  Google Scholar 

  • 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 5:736–748

    Article  Google Scholar 

  • Shumway SE (1990) A review of the effects of algal blooms on shellfish and aquaculture. J World Aquacul Soc 21:65–104

    Article  Google Scholar 

  • 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 467–514

    Google Scholar 

  • 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 13:322–331

    Article  Google Scholar 

  • 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 4:525–531

    Article  Google Scholar 

  • 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 335–370

    Google Scholar 

  • 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 70:59–65

    CAS  Google Scholar 

  • 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 218:63–76

    Article  Google Scholar 

  • Wikfors GH (2005) A review and new analysis of trophic interactions between Prorocentrum minimum and clams, scallops, and oysters. Harmful Algae 4:585–592

    Article  Google Scholar 

  • 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 188:313–328

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Diane K. Stoecker.

Additional information

Communicated by B.S. Stewart.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stoecker, D.K., Adolf, J.E., Place, A.R. et al. Effects of the dinoflagellates Karlodinium veneficum and Prorocentrum minimum on early life history stages of the eastern oyster (Crassostrea virginica). Mar Biol 154, 81–90 (2008). https://doi.org/10.1007/s00227-007-0901-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-007-0901-z

Keywords

Navigation