Skip to main content
SpringerLink
Log in

Low abundance of the dinoflagellates,Pfiesteria piscicida, P. shumwayae, andCryptoperidiniopsis spp., in South Carolina tidal creeks and open estuaries

  • Published:
Estuaries Aims and scope Submit manuscript

Abstract

The toxicPfiesteria complex are a group of dinoflagellates that have received considerable attention in recent years as causative factors in fish kill or lesion events in North Carolina estuaries and in the Pocomoke River of Chesapeake Bay. In response to the potentialPfiesteria threat, the South Carolina Task Group on Harmful Algae was formed in late 1997 and implemented programs to monitor harmful algal blooms and respond to fish kills or lesion events with particular emphasis on the Bushy Park (Cooper River, Charleston) region, a site of annually recurrent menhaden lesion events.Pfiesteria piscicida, Pfiesteria shumwayae, andCryptoperidiniopsis spp. were documented in South Carolina estuaries. Routine monitoring and fish kill or lesion event sampling consistently indicated low abundances compared to estimates from similar programs in North Carolina and Maryland that sampled areas with a history ofPfiesteria toxic activity. The finding thatPfiesteria-like organism (PLO) abundances were always low in samples collected during menhaden lesion events in Bushy Park suggested other causes for lesion progression, althoughPfiesteria spp. could not be ruled out as a factor in lesion initiation. Based on the previously demonstrated positive relationship between PLO abundance, chlorophylla, and inorganic nutrient concentrations (in laboratory experiments and North Carolina field observations), we hypothesized that the relatively low abundance ofPfiesteria spp. and other PLO (e.g.,Cryptoperidiniopsis) in South Carolina estuaries is related to the relatively low supply of phytoplankton prey, as supported by interstate comparisons in chlorophylla concentrations. Nitrate concentrations were generally much lower in South Carolina estuaries. Estuarine eutrophication may be an important consideration in explaining interstate differences in susceptibility toPfiesteria-related toxic events.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature Cited

  • Adachi, M., Y. Sako, andY. Ishida. 1996. Identification of the toxic dinoflagellatesAlexandrium catenella andA. tamarense (Dinophyceae) using DNA probes and whole-cell hybridization.Journal of Phycology 32:1049–1052.

    Article  Google Scholar 

  • Ahrenholz, D. W., J. F. Guthrie, and R. M. Clayton. 1987. Observations of ulcerative mycosis infections on Atlantic menhaden (Brevoortia tyramnus). National Oceanic and Atmospheric Administration Technical Memorandum NMFS-SEFC-196, Beaufort, North Carolina.

  • Anderson, D. M. 1989. Toxic algal blooms and red tides: A global perspective, p. 11–16.In T. Okaichi, D. M. Anderson, and T. Nemoto (eds.), Red Tides: Biology, Environmental Science and Toxicology. Elsevier Science, New York.

    Google Scholar 

  • Backer, L. C., A. S. Niskar, C. Rubin, K. Blindauer, D. Christianson, L. Naeher, andH. S. Rogers. 2001. Environmental public health surveillance: Possible estuary-associated syndrome.Environmental Health Perspectives 109:797–801.

    Article  Google Scholar 

  • Berdalet, E. andM. Estrada. 1993. Effects of turbulence on several dinoflagellate species, p. 737–740.In T. J. Smayda and Y. Shimizu (eds.), Toxic Phytoplankton Blooms in the Sea. Elsevier Science, New York.

    Google Scholar 

  • Bricker, S. B., C. G. Clement, D. E. Pirhalla, S. P. Orlando, andD. R. G. Farrow. 1999. National estuarine eutrophication assessment: Effects of nutrient enrichment in the nation’s estuaries. National Oceanic and Atmospheric Administration, National Ocean Service, Silver Spring, Maryland.

    Google Scholar 

  • Burkholder, J. M. andH. B. Glasgow, Jr. 1997. Interactions of a toxic estuarine dinoflagellate with microbial predators and prey.Archives für Protistenkunde 145:177–188.

    Google Scholar 

  • Burkholder, J. M. andH. B. Glasgow, Jr. 1997. The ichthyotoxic dinoflagellate,Pfiesteria piscicida: Behavior, impacts, and environmental controls.Limnology and Oceanography 42:1052–1075.

    Google Scholar 

  • Burkholder, J. M., H. B. Glasgow, Jr., andN. Deamer-Melia. 2001. Overview and present status of the toxicPfiesteria complex (Dinophyceae).Phycologia 40:186–214.

    Google Scholar 

  • Burkholder, J. M., H. B. Glasgow, Jr., andC. W. Hobbs. 1995. Fish kills linked to a toxic ambush-predator dinoflagellate: Distribution and environmental conditions.Marine Ecology Progress Series 124:43–61.

    Article  Google Scholar 

  • Burkholder, J. M., M. A. Mallin, andH. B. Glasgow, Jr. 1999. Fish kills, bottom-water hypoxia, and the toxicPfiesteria complex in the Neuse River and estuary.Marine Ecology Progress Series 179:301–310.

    Article  Google Scholar 

  • Burkholder, J. M., M. A. Mallin, H. B. Glasgow, Jr.,L. M. Larsen, M. R. McIver, G. C. Shank, N. Deamer-Melia, D. S. Briley, J. Springer, B. W. Touchette, andE. K. Hannon. 1997. Impacts to a coastal river and estuary from rupture of a large swine waste holding lagoon.Journal of Environmental Quality 26:1451–1466.

    CAS  Google Scholar 

  • Dame, R., M. Alber, D. Allen, M. Mallin, C. Montague, A. Lewitus, A. Chalmers, R. Gardner, C. Gilman, B. Kjerfve, J. Pinckney, andN. Smith. 2000. Estuaries of the south Atlantic Coast of North America: Their geographical signatures.Estuaries 23:793–819.

    Article  CAS  Google Scholar 

  • Estrada, M. andE. Berdalet. 1998. Effects of turbulence on phytoplankton, p. 601–618.In D. M. Anderson, A. D. Cembella, and G. M. Hallegraeff (eds.), Physiological Ecology of Harmful Algal Blooms. Springer-Verlag, Berlin, Germany.

    Google Scholar 

  • Glasgow, Jr.H. B. andJ. M. Burkholder. 2000 Water quality trends and management implications from a five-year study of a eutrophic estuary.Ecological Applications 10:1024–1046.

    Article  Google Scholar 

  • Glasgow, Jr.H. B., J. M. Burkholder, M. A. Mallin, N. J. Deamer-Melia, andR. E. Reed. 2001a. Field ecology of toxicPfiesteria complex species and a conservative analysis of their role in estuarine fish kills.Environmental Health Perspectives 109:715–730.

    Article  CAS  Google Scholar 

  • Glasgow, Jr.H. B., J. M. Burkholder, S. L. Morton, andJ. Springer. 2001b. A second species of icthyotoxicPfiesteria (Dinamoebales, Dinophyceae).Phycologia 40:234–245.

    Google Scholar 

  • Glasgow, Jr.H. B., J. M. Burkholder, D. Schmechel, P. A. Tester, andP. Rublee. 1995. Insidious effects of a toxic estuarine dinoflagellate on fish survival and human health.Journal of Toxicology and Environmental Health 46:501–522.

    Article  CAS  Google Scholar 

  • Glover, H. E. andI. Morris. 1979. Photosynthetic carboxylating enzymes in marine phytoplankton.Limnology and Oceanography 23:510–519.

    Google Scholar 

  • Grattan, L., D. Oldach, T. Perl, M. Lowitt, D. Matuszak, C. Dickson, C. Parrott, R. Shoemacher, M. Wasserman, J. R. Hebel, P. Charache, andJ. G. Morris, Jr. 1998. Problems in learning and memory occur in persons with environmental exposure to water ways containing toxin-producingPfiesteria orPfiesteria-like dinoflagellates.Lancet 352:532–539.

    Article  CAS  Google Scholar 

  • Guillard, R. R. L. 1975. Culture of phytoplankton for feeding marine invertebrates, p. 29–60.In W. L. Smith and M. H. Chaney (eds.), Culture of Marine Invertebrate Animals. Plenum Press, New York.

    Google Scholar 

  • Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase.Phycologia 32:79–99.

    Google Scholar 

  • Hawes, C. 1988. Subcellular localization of macromolecules by microscopy, p. 103–130.In C. H. Shaw (ed.), Plant Molecular Biology. Kluwer Academic Publishers, New York.

    Google Scholar 

  • Kempton, J. W. 1999. PCR and FISH assays for the detection ofPfiesteria piscicida. M.S. Thesis, University of North Carolina at Greensboro, Greensboro, North Carolina.

    Google Scholar 

  • Law, M. 2001. Differential diagnosis of ulcerative lesions in fish.Environmental Health Perspectives 109:681–686.

    Article  Google Scholar 

  • Lewittus, A. J., J. M. Burkholder, H. B. Glasgow, Jr.,P. M. Glibert, B. M. Willis, K. C. Hayes, andM. K. Burke. 1999a. Mixotrophy and nutrient uptake byPfiesteria piscicida (Dinophyceae).Journal of Phycology 35:1430–1437.

    Article  Google Scholar 

  • Lewitus, A. J., H. B. Glasgow, andJ. M. Burkholder. 1999b. Kleptoplastidy in the toxic dinoflagellate,Pfiesteria piscicida (Dinophyceae).Journal of Phycology 35:303–312.

    Article  Google Scholar 

  • Lewitus, A. J., K. C. Hayes, S. G. Gransden, H. B. Glasgow, Jr.,J. M. Burkholder, P. M. Glibert, andS. L. Morton. 2002. Ecological characterization of a widespread red tide in South Carolina estuaries: A newly observed phenomenon, p. 129–132.In G. M. Hallegraeff, S. Blackburn, C. Bolch, and R. Lewis (eds.), Proceedings of the Ninth International Conference on Harmful Algal Blooms. Intergovernmental Oceanographic Commission, United Nations Educational, Scientific, and Cultural Organization, Paris, France.

    Google Scholar 

  • Lewitus, A. J. and A. F. Holland. In press. Initial results from a multi-institutional collaboration to monitor harmful algal blooms in South Carolina.Environmental Monitoring and Assessment.

  • Lewitus, A. J., E. T. Koepfler, andJ. T. Morris. 1998. Seasonal variation in the regulation of phytoplankton by nitrogen and grazing in a salt marsh estuary.Limnology and Oceanography 43:636–646.

    CAS  Google Scholar 

  • Lin, S. andE. J. Carpenter. 1996. An empirical protocol for whole-cell immunofluorescence of marine phytoplankton.Journal of Phycology 32:1083–1094.

    Article  Google Scholar 

  • Lund, J. W. G., C. Kipling, andE. D. LeCren. 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimates by counting.Hydrobiologia 11:143–170.

    Article  Google Scholar 

  • Margalef, R. 1978. Life-forms of phytoplankton as survival alternatives in an unstable environment.Oceanologica Acta 1:493–509.

    Google Scholar 

  • Marshall, H. G., A. S. Gordon, D. W. Seaborn, B. Dyer, W. M. Dunstan, andM. Seaborn. 2000. Comparative culture and toxicity studies betwen the toxic dinoflagellatePfiesteria piscicida and a morphologically similar cryptoperidiniopsoid dinoflagellate.Journal of Experimental Marine Biology and Ecology 255:51–74.

    Article  CAS  Google Scholar 

  • Morris, Jr.,J. G. 1999.Pfiesteria, “the cell from hell,” and other toxic algal nightmares.Clinical Infectious Diseases 28:1191–1198.

    Article  Google Scholar 

  • Noga, E. J. 1993. Fungal diseases in marine and estuarine fishes, p. 85–100.In J. A. Couch and J. W. Fournie (eds.). Pathobiology of Marine and Estuarine Organisms. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Noga, E. J. andM. J. Dykstra. 1986. Oomycete fungi associated with ulcerative mycosis in Atlantic menhaden.Journal of Fish Diseases 9:47–53.

    Article  Google Scholar 

  • Noga, E. J., L. Khoo, J. B. Stevens, Z. Fan, andJ. M. Burkholder. 1996. Novel toxic dinoflagellate causes epidemic disease in estuarine fish.Marine Pollution Bulletin 32:219–224.

    Article  CAS  Google Scholar 

  • North Carolina Department of Environment, Health and Natural Resources. 1996. Classifications and Water Quality Standards Applicable to Surface Waters of North Carolina. North Carolina Administrative Code Sections 15A NCAC2B.0100 and 15A NCAC2B.0200. North Carolina Environmental Management Commission, Raleigh, North Carolina.

    Google Scholar 

  • Oldach, D. W., C. F. Delwiche, K. S. Jakobsen, T. Tengs, E. G. Brown, J. W. Kempton, E. F. Schaefer, H. Bowers, H. B. Glasgow, Jr.,J. M. Burkholder, K. A. Steidinger, andP. A. Rublee. 2000. Heteroduplex mobility assay guided sequence discovery: Elucidation of the small subunit (18S) rDNA sequence ofPfiesteria piscicida from complex algal culture and environmental sample DNA pools.Proceedings of the National Academy of Sciences 97:4304–4308.

    Article  Google Scholar 

  • Paerl, H. W. 1997. Coastal eutrophication and harmful algal blooms: Importance of atmospheric deposition and ground-water as “new” nitrogen and other nutrient sources.Limnology and Oceanography 42:1152–1165.

    Article  Google Scholar 

  • Parrow, M. W., H. B. Glasgow, Jr.,J. M. Burkholder, andC. Zhang. 2002. Comparative response to algal prey byPfiesteria piscicida, Pfiesteria shumwayae sp. nov., and a co-occurring ‘lookalike’ species.In G. M. Hallegraeff, S. Blackburn, C. Bolch, and R. Lewis (eds.), Proceedings of the Ninth International Conference on Harmful Algal Blooms. Intergovernmental Oceanographic Commission, United Nations Educational, Scientific and Cultural Organization, Paris, France.

    Google Scholar 

  • Pollingher, U. andE. Zemel. 1981. In situ and experimental evidence of the influence of turbulence on cell division processes ofPeridinium cinctum formawestii (Lemm.) Lefèvre.British Phycological Journal 16:281–287.

    Article  Google Scholar 

  • Rublee, P. A., J. Kempton, E. Schaefer, C. Allen, J. Harris, D. W. Oldach, H. Bowers, T. Tengs, J. M. Burkholder, andH. B. Glasgow, Jr. 2001. Use of molecular probes to assess geographic distribution ofPfiesteria species.Environmental Health Perspectives 109:765–767.

    Article  CAS  Google Scholar 

  • Rublee, P. A., J. Kempton, E. Schaefer, J. M. Burkholder, H. B. Glasgow, Jr., andD. Oldach. 1999. PCR and FISH detection extends the range ofPfiesteria piscicida in estuarine waters.Virginia Journal of Science 50:325–336.

    Google Scholar 

  • Samet, J., G. S. Bignami, R. Feldman, W. Hawkins, J. Neff, andT. Smayda. 2001.Pfiesteria: Review of the science and identification of research gaps. Report for the National Center for Environmental Health, Centers for Disease Control and Prevention.Environmental Health Perspectives 109:639–659.

    Article  CAS  Google Scholar 

  • Schaefer, E. F. 1997. A DNA assay to detect the toxic dinoflaprobe.Pfiesteria piscicida, and the application of a PCR based probe, M.S. Thesis, University of North Carolina at Greensboro, Greensboro, North Carolina.

    Google Scholar 

  • Schmechel, D. E. andD. C. Koltai. 2001. Potential human health effects associated with laboratory exposures toPfiesteria piscicida.Environmental Health Perspectives 109:775–779.

    Article  CAS  Google Scholar 

  • Smayda, T. J. 1990. Novel and nuisance phytoplankton blooms in the sea: Evidence for a global epidemic, p. 29–40.In E. Granéli, B. Sundström, L. Edler, and D. M. Anderson (eds.), Toxic Marine Phytoplankton. Elsevier Science, New York.

    Google Scholar 

  • Smayda, T. J. 1997. Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea.Limnology and Oceanography 42:1137–1153.

    Google Scholar 

  • Steidinger, K., J. Landsberg, R. W. Richardson, E. Truby, B. Blakesley, P. Scott, P. Tester, T. Tengs, P. Mason, S. Morton, D. Seaborn, W. Litaker, K. Reece, D. Oldach, L. Haas, andG. Vasta. 2001. Classification and identification ofPfiesteria andPfiesteria-like species.Environmental Health Perspectives 109:661–665.

    Article  Google Scholar 

  • Stewart, C. N. andL. E. Via. 1993. A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications.BioTechniques 14:748–749.

    CAS  Google Scholar 

  • Tester, P. A. andK. A. Steidinger. 1997.Gymnodinium breve red tide blooms: Initiation, transport, and consequences of surface circulation.Limnology and Oceanography 42:1039–1051.

    Google Scholar 

  • Tester, P. A., R. P. Stumpf, F. M. Vukovich, P. K. Fowler, andJ. T. Turner. 1991. An expatriate red tide bloom: Transport, distribution, and persistence.Limnology and Oceanography 36:1053–1061.

    Article  Google Scholar 

Source of Unpublished Materials

  • Hopkins, S. personal communication. South Carolina Department of Natural Resources, Waddell Mariculture Center, Bluffton, South Carolina.

Download references

Author information

Author notes

  1. Bonnie M. Willis

    Present address: Delaware Department of Natural Resources and Environmental Control, 89 Kings Highway, 19901, Dover, Delaware

Authors and Affiliations

  1. Belle W. Baruch Institute for Marine Biology and Coastal Research, University of South Carolina, 29422-2559, Charleston, South Carolina

    Alan J. Lewitus

  2. South Carolina Department of Natural Resources, Marine Resources Research Institute, 29422-2559, Charleston, South Carolina

    Alan J. Lewitus

  3. South Carolina Department of Health and Environmental Control, and Belle W. Baruch Institute for Marine Biology and Coastal Research, University of South Carolina, 29442, Georgetown, South Carolina

    Kenneth C. Hayes

  4. Belle W. Baruch Institute for Marine Biology and Coastal Research, University of South Carolina, 29442, Georgetown, South Carolina

    Bonnie M. Willis

  5. Center for Applied Aquatic Ecology, North Carolina State University, 27695-7612, Raleigh, North Carolina

    JoAnn M. Burkholder & Howard B. Glasgow

  6. South Carolina Department of Natural Resources, Marine Resources Research Institute, 29422-2559, Charleston, South Carolina

    A. Fred Holland & Philip P. Maier

  7. Biology Department, University of North Carolina at Greensboro, 27402-6174, Greensboro, North Carolina

    Parke A. Rublee

  8. Maryland Department of Natural Resources, 580 Taylor Avenue, D-2, 21401, Annapolis, Maryland

    Robert Magnien

Authors
  1. Alan J. Lewitus
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kenneth C. Hayes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bonnie M. Willis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. JoAnn M. Burkholder
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Howard B. Glasgow
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. Fred Holland
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Philip P. Maier
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Parke A. Rublee
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Robert Magnien
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lewitus, A.J., Hayes, K.C., Willis, B.M. et al. Low abundance of the dinoflagellates,Pfiesteria piscicida, P. shumwayae, andCryptoperidiniopsis spp., in South Carolina tidal creeks and open estuaries. Estuaries 25, 586–597 (2002). https://doi.org/10.1007/BF02804892

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02804892

Keywords

Search

Navigation