Pjesteria piscicida and other Pfesteria-like dinoflagellates’: Behavior, impacts, and environmental controls

Toxic PJesteria-like dinoflagellates have been implicated as causative agent; of major fish kills (affecting IO’10” fish) in estuaries and coastal waters of the mid-Atlantic and southeastern U.S. Transformations among an array of flagellated, amoeboid, and encysted stages in the complex life cycle of the representative species, Pjiesteria piscicida, are controlled by the availability of fresh secretions, blood, or other tissues of fish prey. P. piscicidu also is a voracious predator on other estuarine microorganisms. Pjesteria-like dinoflagellates require an unidentified substance(s) commonly found in fresh fish excreta-secreta to initiate toxin production. P. piscicida is lethal to fish at low cell densities (>250-300 cells ml-l), and at sublethal levels (100-250 cells ml-‘) it has been shown to cause ulcerative fish diseases. P. piscicida also has been linked to serious human health impacts. This dinoflagellate is curythermal and euryhaline, with optima for toxic activity by the most lethal stage (toxic zoospores, TZs) at 226°C and 15 psu, respectively. Thus fdr it has shown no light optimum and :s capable of killing fish at any time during a 24-h cycle. In warmer waters (2 15°C) flagellated stages predominate while fish are dying, whereas amoebae predominate in colder conditions and when fish are dead. Nutritional stimuli influencing P. piscicida arc complex; inorganic phosphate apparently can directly stimulate TZs, whereas inorganic phosphate and nitratc indirectly promote increased production of nontoxic zoospores (NTZs, maintained in the absence of live fish, as potential precursors to lethal TZs) by stimulating their algal prey. Organic phosphate (P,) and nitrogen are taken up by P. piscicz’du osmotrophically, and P,, is stimulatory to both TZs and NTZs. The available data point to a critical need to characterize the chronic and acute impacts of toxic Pfiesteriu-like dinoflagellates on fish and other targeted prey in estuarine and coastal waters that are adversely affected by cultural eutrophication. The diverse heterotrophic dinoflagellates (Pyrrhophyta) include free-living estuarine species that demonstrate pronounced chemosensory “ambush-predator” behavior toward algal, protozoan, or fish prey (Spero and Moree 1981; Spero 1982; Ucko et al. 1989; Burkholder et al. 1995a,b, 1997~; Landsberg et al. 199.5). This behavioral pattern apparently is widespread; thus far, it has been reported from the Mediterranean Sea, the Gulf of Mexico, and the western Atlantic. In each case the feeding activity has been strikingly similar: the dinoflagellates swarm up from benthic dormant cysts when they chemically detect the prey’s presence. They deAcknowledgments Funding support for this research was provided by the National Science Foundation (grant OCE 94-3920) the National Sea Grant Marine Biotechnology Program, the U.S. Marine Air Station at Cherry Point/U.S. Fish & Wildlife Service (special thanks to D. Nelson and G. Hartzog), the U.S. EPA, the Neuse River Foundation, the NC Agricultural Research Foundation (project 93-0042), the NC Agricultural Research Foundation (project 06034; special thanks to J. Wynne), the NC Agricultural Research Service (project 06188), the NCSU College of Agriculture & Life Sciences, and the NCSU Department of Botany (special thanks to E. Davies). We are grateful to B. Adams, D. Briley, N. Deamer-Melia, R. Dove, E. Fensin, E. Hannon, A. Hodge, J. Howard, M. Larsen, K. Lynch, J. Manning, and Maryland DNR staff for feld and laboratory assistance in the surveys and(or) nutrient experiments. A. Lewitus and M. Mallin kindly reviewed the manuscript. We dedicate this work to the late Lois Pfiester, in whose honor Pjiiesteria piscicidu was named. Dr. Ptiester’s kindness, and the brilliance inherent in her earlier descriptions of freshwater dinoflagellates that transform among flagellated, saccate, and amoeboid stages, provided the insights that greatly helped us in approaching the complex biology of efiesteria-like dinoflagellates. vour the prey-described in one case as being ripped apart in a “Feeding frenzy” (Spero and Moree 1981)-and then rapidly re-encysr.. Known dinoflagellate species with this behavior include the toxic representative P$esteria piscicida Steidinger & Burkholder (nomen nudem P. piscimorte, P. piscimortuis; Steidinger et al. 1996a) and at least one other toxic Pjiesteria-like species (Steidinger et al. 1996b; K. Steidinger pers. comm.; J.M.B and H.B.G. unpubl. data confirming toxicity). Not surprisingly, P$esteria spp. were first detected following accidental contamination of established prey cultures (Spero and Moree 1981; Smith et al. unpubl.; Noga et al. 1993; Landsberg et al 1995). Other similar and apparently co-occurring dinoflagellate species, including toxic forms, likely have been overlooked because they are small and closely resemble many common nontoxic estuarine clinoflagellates without diagnostic characters that readily enable identification by light microscopy (Spero and Moree 1981; Burkhold-