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Environmental Factors Contributing to the Development and Demise of a Toxic Dinoflagellate (Karlodinium veneficum) Bloom in a Shallow, Eutrophic, Lagoonal Estuary

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Abstract

A dense bloom of the ichthyotoxic dinoflagellate Karlodinium veneficum was discovered in the Neuse River Estuary, North Carolina, on 19 October 2006 and was associated with four subsequent fish kills. Microscopic, photopigment, DNA, and toxicological techniques confirmed bloom identity and toxicity. High-resolution spatio-temporal data from ship-board and fixed automated sampling stations provided a unique opportunity to investigate the environmental conditions that initiated, maintained, and terminated the K. veneficum bloom. Bloom initiation and growth were favored by high nutrient availability and reduced dispersal during the period of declining riverine discharge after Tropical Storm Ernesto. K. veneficum out-competed other co-occurring dinoflagellates, perhaps because of the production of karlotoxins that are known to act as grazing deterrents and to facilitate mixotrophic feeding. Once the bloom was established, small-scale hydrodynamic processes, coupled with vertical migration, concentrated cells along a frontal convergence to high densities (>200,000 cells per milliliter). By 26 October 2006, wind mixing and possible nutrient stress disrupted the bloom. Release of cell-bound toxins during the bloom collapse likely accounted for the associated fish kill events where fish were reported as exhibiting typical symptoms of karlotoxin poisoning. The dynamics of this bloom underscore the tight control of harmful algal blooms by meteorological forcing, hydrology, and sediment nutrient input in this shallow lagoonal estuary.

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Acknowledgment

Thanks to the dedicated technicians of the Paerl, Litaker (Mark W. Vandersea), and Place laboratories for their analytical contributions. Thanks to A. Joyner for help in generating the site map. R. Waggett, B. Peierls, and W. G. Sunda provided constructive critiques of the manuscript. This work was supported by the North Carolina Department of Environment and Natural Resources (ModMon Program), the North Carolina Sea Grant Program, the US EPA-STAR-EaGLe Program, and the National Science Foundation, Ecosystems, Environmental Geochemistry and Biology (EGB) and Ecology of Infectious Diseases (EID) Programs. Toxin analyses were supported by grants from NOAA Coastal Oceans Program (grant no. NA04NOS4780276), Centers for Disease Control and Prevention (grant no. U50/CCU 323376) and the Maryland Department of Health and Mental Hygiene to University of Marine Biotechnology Institute. This is contribution number 220 from the NOAA ECOHAB program and contribution number 07-172 from the University of Maryland Biotechnology Institute, Center of Marine Biotechnology.

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Authors and Affiliations

  1. Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, NC, 28557, USA

    Nathan S. Hall & Hans W. Paerl

  2. National Oceanographic and Atmospheric Administration/National Ocean Service, Beaufort Laboratory, Beaufort, NC, 28516, USA

    R. Wayne Litaker

  3. Environmental Sciences Section, North Carolina Division of Water Quality, Raleigh, NC, 27699-1621, USA

    Elizabeth Fensin

  4. Center of Marine Biotechnology, University of Maryland Biotechnology Institute, Baltimore, MD, 21202, USA

    Jason E. Adolf, Holly A. Bowers & Allen R. Place

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  1. Nathan S. Hall
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  2. R. Wayne Litaker
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  3. Elizabeth Fensin
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  4. Jason E. Adolf
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Correspondence to Nathan S. Hall.

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Hall, N.S., Litaker, R.W., Fensin, E. et al. Environmental Factors Contributing to the Development and Demise of a Toxic Dinoflagellate (Karlodinium veneficum) Bloom in a Shallow, Eutrophic, Lagoonal Estuary. Estuaries and Coasts: J CERF 31, 402–418 (2008). https://doi.org/10.1007/s12237-008-9035-x

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