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A chronicle of a killer alga in the west: ecology, assessment, and management of Prymnesium parvum blooms

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An Erratum to this article was published on 10 September 2015

Abstract

Since the mid-1980s, fish-killing blooms of Prymnesium parvum spread throughout the USA. In the south central USA, P. parvum blooms have commonly spanned hundreds of kilometers. There is much evidence that physiological stress brought on by inorganic nutrient limitation enhances toxicity. Other factors influence toxin production as well, such as stress experienced at low salinity and temperature. A better understanding of toxin production by P. parvum remains elusive and the identities and functions of chemicals produced are unclear. This limits our understanding of factors that facilitated the spread of P. parvum blooms. In the south central USA, not only is there evidence that the spread of blooms was controlled, in part, by migration limitation. But there are also observations that suggest changed environmental conditions, primarily salinity, facilitated the spread of blooms. Other factors that might have played a role include altered hydrology and nutrient loading. Changes in water hardness, herbicide use, system pH, and the presence of toxin-resistant and/or P. parvum-inhibiting plankton may also have played a role. Management of P. parvum in natural systems has yet to be attempted, but may be guided by successes achieved in small impoundments and mesocosm experiments that employed various chemical and hydraulic control approaches.

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References

  • Almeida-Paz, F. A., P. J. Gates, S. Fowler, A. Gallimore, B. Harvey, N. P. Lopes, J. Stark, C. B. W. Staunton, J. Klinowski & J. B. Spencer, 2003. Sodium monensin dehydrate. Acta Crystallography 59: 1050–1052.

    Google Scholar 

  • Ankley, G. T., R. S. Bennett, R. J. Erickson, D. J. Hoff, M. W. Hornugn, R. D. Johnson, D. R. Mount, J. W. Nichols, C. L. Russom, P. K. Schmieder, J. A. Serrano, J. E. Tietge & D. L. Villeneuve, 2010. Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environmental Toxicology and Chemistry 29: 730–741.

    Article  CAS  PubMed  Google Scholar 

  • Baas-Becking, L. G. M., 1943. Geobiologie of Inleiding Tot de Milieukunde. Van Stockkum & Zoon, The Hague.

    Google Scholar 

  • Baker, J. W., J. P. Grover, B. W. Brooks, F. Ureña-Boeck, D. L. Roelke, R. M. Errera & R. Kiesling, 2007. Growth and toxicity of Prymnesium parvum (Haptophyta) as a function of salinity, light and temperature. Journal of Phycology 43: 219–227.

    Article  Google Scholar 

  • Baker, J. W., J. P. Grover, R. Ramachandrannair, C. Black, T. W. Valenti Jr, B. W. Brooks & D. L. Roelke, 2009. Growth at the edge of the niche: an experimental study of the harmful alga Prymnesium parvum. Limnology and Oceanography 54: 1679–1687.

    Article  CAS  Google Scholar 

  • Barkoh, A., D. G. Smith & J. W. Schlechte, 2003. An effective minimum concentration of un-ionized ammonia nitrogen for controlling Prymnesium parvum. North American Journal of Aquaculture 65: 220–225.

    Article  Google Scholar 

  • Barkoh, A. & L. T. Fries (eds), 2005. Management of Prymnesium parvum at Texas State Fish Hatcheries. Management Data Series 236. Texas Parks and Wildlife Department, Austin.

    Google Scholar 

  • Barkoh, A., D. G. Smith & G. M. Southard, 2010. Prymnesium parvum control treatments for fish hatcheries. Journal of the American Water Resources Association 46: 161–169.

    Article  CAS  Google Scholar 

  • Barone, R., G. Castelli & L. Naselli-Flores, 2010. Red sky at night cyanobacteria delight: the role of climate in structuring phytoplankton assemblage in a shallow, Mediterranean lake (Biviere di Gela, southeastern Sicily). Hydrobiologia 639: 43–53.

    Article  CAS  Google Scholar 

  • Barreiro, A., C. Guisande, I. Maneiro, T. P. Lien, C. Legrand, T. Tamminen, S. Lehtinen, P. Uronen & E. Granéli, 2005. Relative importance of the different negative effects of the toxic haptophyte Prymnesium parvum on Rhodomonas salina and Brachionus plicatilis. Aquatic Microbial Ecology 38: 259–267.

    Article  Google Scholar 

  • Beijerinck, M. W., 1913. De infusies en de ontdekking der backteriën. In Jaarboek van de KoninklijkeAkademie van Wetenschappen. Muller, Amsterdam.

  • Bertin, M. J., P. V. Zimba, K. R. Beauchesne, K. M. Huncik & P. D. Moeller, 2012a. The contribution of fatty acid amides to Prymnesium parvum Carter toxicity. Harmful Algae 20: 117–125.

    Article  CAS  Google Scholar 

  • Bertin, M. J., P. V. Zimba, K. R. Beauchesne, K. M. Huncik & P. D. Moeller, 2012b. Identification of toxic fatty acid amides isolated from the harmful alga Prymnesium parvum Carter. Harmful Algae 20: 111–116.

    Article  CAS  Google Scholar 

  • Bertin, M. J., D. C. Voronca, R. W. Chapman & P. D. Moeller, 2014. The effect of pH on the toxicity of fatty acids and fatty acid amides to rainbow trout gill cells. Aquatic Toxicology 146: 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Beszteri, S., I. Yang, N. Jaeckisch, U. Tillmann, S. Frickenhaus, G. Glöckner, A. Cembella & U. John, 2012. Transcriptomic response of the toxic prymnesiophyte Prymnesium parvum (N. Carter) to phosphorus and nitrogen starvation. Harmful Algae 18: 1–15.

    Article  CAS  Google Scholar 

  • Blossom, H. E., N. G. Andersen, S. A. Rasmussen & P. J. Hansen, 2014a. Stability of the intra- and extracellular toxins of Prymnesium parvum using a microalgal bioassay. Harmful Algae 32: 11–21.

    Article  CAS  Google Scholar 

  • Blossom, H. E., S. A. Rasmussen, N. G. Andersen, T. O. Larsen, K. F. Nielsen & P. J. Hansen, 2014b. Prymnesium parvum revisited: relationship between allelopathy, ichthyotoxicity, and chemical profiles in 5 strains. Aquatic Toxicology. doi:10.1016/j.aquatox.2014.10.006.

    PubMed  Google Scholar 

  • Brooks, B. W., S. V. James, T. W. Valenti Jr, F. Urena-Boeck, C. Serrano, J. P. Berninger, L. Schwierzke, L. D. Mydlarz, J. P. Grover & D. L. Roelke, 2010. Comparative toxicity of Prymnesium parvum in inland waters. Journal of American Water Resources Association 46: 45–62.

    Article  CAS  Google Scholar 

  • Brooks, B. W., J. P. Grover & D. L. Roelke, 2011. Prymnesium parvum, an emerging threat to inland waters. Environmental Toxicology and Chemistry 30: 1955–1964.

    Article  CAS  PubMed  Google Scholar 

  • Brussaard, C. P. D., B. Kuipers & M. J. W. Veldhuis, 2005. A mesocosm study of Phaeocystis globosa population dynamics I. Regulatory role of viruses in bloom control. Harmful Algae 4: 859–874.

    Article  Google Scholar 

  • Burkholder, J. M., 1998. Implications of harmful microalgae and heterotrophic dinoflagellates in management of sustainable marine fisheries. Ecological Applications 8: 37–62.

    Article  Google Scholar 

  • Cichewicz, R. H. & K. D. Hambright, 2010. A revised amino group pK a for prymnesins does not provide decisive evidence for a pH-dependent mechanism of Prymnesium parvum’s toxicity. Toxicon 55: 1035–1037.

    Article  CAS  PubMed  Google Scholar 

  • Croft, M. T., A. D. Lawrence, E. Raux-Deery, M. J. Warren & A. G. Smith, 2005. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438: 90–93.

    Article  CAS  PubMed  Google Scholar 

  • Croft, M. T., M. J. Warren & A. G. Smith, 2006. Algae need their vitamins. Eukaryotic Cell 5: 1175–1183.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dafni, Z., S. Ulitzur & M. Shilo, 1972. Influence of light and phosphate on toxin production and growth of Prymnesium parvum. Journal of General Microbiology 70: 199–207.

    Article  CAS  Google Scholar 

  • Daniel, T. C., A. N. Sharpley & J. L. Lemunyon, 1998. Agricultural phosphorus and eutrophication: a symposium overview. Jouranl of Environmental Quality 27: 251–257.

    Article  CAS  Google Scholar 

  • Davis, S. L., D. L. Roelke, B. W. Brooks, V. M. Lundgren, F. Withrow & W. C. Scott, 2015. Rotifer-Prymnesium parvum interactions: the role of lake bloom history. Aquatic Microbial Ecology. Accepted.

  • Dawson, D., M. M. VanLandeghem, W. H. Asquith & R. Patiño. Long-term trends in reservoir water quality and quantity in two major river basins of the southern Great Plains, USA. Lake and Reservoir Management. In Review.

  • deNoyelles, F., W. D. Kettle & D. E. Sinn, 1982. The responses of plankton communities in experimental ponds to atrazine, the most heavily used pesticide in the United States. Ecology 63: 1285–1293.

    Article  CAS  Google Scholar 

  • Doucette, G. J., E. R. McGovern & J. A. Babinchak, 1999. Algicidal bacteria active against Gymnodiniumbreve (Dinophyceae). I. Bacterial isolation and characterization of killing activity. Journal of Phycology 35: 1447–1454.

    Article  Google Scholar 

  • Droop, M. R., 1973. Some thoughts on nutrient limitation in algae. Journal of Phycology 9: 264–272.

    CAS  Google Scholar 

  • Droop, M. R., 1983. 25 years of algal growth kinetics: a personal review. Botanica Marina 26: 99–112.

    Article  Google Scholar 

  • Dugdale, R. C., 1967. Nutrient limitation in the sea: dynamics, identification, and significance. Limnology and Oceanography 12: 685–695.

    Article  Google Scholar 

  • Edvardsen, B. & E. Paasche, 1998. Bloom dynamics and physiology of Prymnesium and Chrysochromulina. In Anderson, D. M., A. D. Cembella & G. M. Hallegraff (eds), The Physiological Ecology of Harmful Algal Blooms. Springer, Heidelberg: 193–208.

    Google Scholar 

  • Errera, R. M., D. L. Roelke, R. Kiesling, B. W. Brooks, J. P. Grover, L. Schwierzke, F. Ureña-Boeck, J. W. Baker & J. L. Pinckney, 2008. The effect of imbalanced nutrients and immigration on Prymnesium parvum community dominance and toxicity: results from in-lake microcosm experiments, Texas, USA. Aquatic Microbial Ecology 52: 33–44.

    Article  Google Scholar 

  • Fistarol, G. O., C. Legrand & E. Granéli, 2003. Allelopathic effect of Prymnesium parvum on a natural plankton community. Marine Ecology Progress Series 255: 115–125.

    Article  Google Scholar 

  • Fistarol, G. O., C. Legrand & E. Granéli, 2005. Allelopathic effect on a nutrient-limited phytoplankton species. Aquatic Microbial Ecology 41: 153–161.

    Article  Google Scholar 

  • Fu, X. F., A. O. Tatters & D. A. Hutchins, 2012. Global change and the future of harmful algal blooms in the ocean. Marine Ecology Progress Series 470: 207–233.

    Article  CAS  Google Scholar 

  • Gavis, J., 1976. Munk and Riley revisited: nutrient diffusion transport and rates of phytoplankton growth. Journal of Marine Research 34: 161–179.

    Google Scholar 

  • Genitsaris, S., K. A. Kormas & M. Moustaka-Gouni, 2009. Microscopic eukaryotes living in a dying lake (Lake Koronia, Greece). FEMS Microbiology Ecology 69: 75–83.

    Article  CAS  PubMed  Google Scholar 

  • Granéli, E., 2006. Kill your enemies and eat them with the help of your toxins: an algal strategy. African Journal of Marine Science 28: 331–336.

    Article  Google Scholar 

  • Granéli, E. & N. Johansson, 2003a. Effects of the toxic haptophyte Prymnesium parvum on the survival and feeding of a ciliate: the influence of different nutrient conditions. Marine Ecology Progress Series 254: 49–56.

    Article  Google Scholar 

  • Granéli, E. & N. Johansson, 2003b. Increase in the production of allelopathic substances by Prymnesium parvum cells grown under N- or P-deficient conditions. Harmful Algae 2: 135–145.

    Article  CAS  Google Scholar 

  • Granéli, E. & P. J. Hansen, 2006. Allelopathy in harmful algae: a mechanism to compete for resources? In Granéli, E. & J. T. Turner (eds), Ecology of Harmful Algae, Ecological Studies, Vol. 189. Springer, Berlin: 189–201.

    Chapter  Google Scholar 

  • Granéli, E. & P. S. Salomon, 2010. Factors influencing allelopathy and toxicity in Prymnesium parvum. Journal of the American Water Resources Association 46: 108–120.

    Article  CAS  Google Scholar 

  • Granéli, E., B. Edvardsen, D. L. Roelke & J. A. Hagström, 2012. The ecophysiology and bloom dynamics of Prymnesium spp. Harmful Algae 14: 260–270.

    Article  Google Scholar 

  • Green, J. C., D. J. Hibberd & R. N. Pienaar, 1982. The taxonomy of Prymnesium (Prymnesiophyceae) including a description of a new cosmopolitan species, P. patellifera sp. nov., and further observations on P. parvum N. Carter. Journal of the British Phycological Society 17: 363–382.

    Article  Google Scholar 

  • Ground, T. A. & A. W. Groeger, 1994. Chemical classification and trophic characteristics of Texas reservoirs. Lake and Reservoir Management 10: 189–201.

    Article  Google Scholar 

  • Grover, J. P., 1989. Phosphorus-dependent growth kinetics of 11 species of freshwater algae. Limnology and Oceanography 34: 341–348.

    Article  CAS  Google Scholar 

  • Grover, J. P. & F.-B. Wang, 2013. Dynamics of a model of microbial competition with internal nutrient storage in a flowing habitat. Applied Mathematics and Computation 225: 747–764.

    Article  Google Scholar 

  • Grover, J. P. & F.-B. Wang, 2014. Competition and allelopathy with resource storage: two resources. Journal of Theoretical Biology 351: 9–24.

    Article  PubMed  Google Scholar 

  • Grover, J. P., R. W. Sterner & J. L. Robinson, 1999. Algal growth in warm temperate reservoirs: nutrient-dependent kinetics of individual taxa and seasonal patterns of dominance. Archiv für Hydrobiologie 145: 1–23.

    CAS  Google Scholar 

  • Grover, J. P., H. S. B. Hsu & F. B. Wang, 2009. Competition and coexistence in flowing habitats with a hydraulic storage zone. Mathematical Biosciences 222: 42–52.

    Article  PubMed  Google Scholar 

  • Grover, J. P., J. W. Baker, D. L. Roelke & B. W. Brooks, 2010. Mathematical models of population dynamics of Prymnesium parvum in inland waters. Journal of American Water Resources Association 46: 92–107.

    Article  Google Scholar 

  • Grover, J. P., K. W. Crane, J. W. Baker, B. W. Brooks & D. L. Roelke, 2011. Spatial variation of harmful algae and their toxins in flowing-water habitats: a theoretical exploration. Journal of Plankton Research 33: 211–228.

    Article  CAS  Google Scholar 

  • Grover, J. P., D. L. Roelke & B. W. Brooks, 2012. Modeling of plankton community dynamics characterized by algal toxicity and allelopathy: a focus on historical Prymnesium parvum blooms in a Texas reservoir. Ecological Modelling 227: 147–161.

    Article  CAS  Google Scholar 

  • Grover, J. P., D. L. Roelke, B. W. Brooks, G. M. Gable, M. T. Neisch, N. J. Hayden, T. W. Valenti Jr, K. N. Prosser, G. D. Umphres & N. C. Hewitt, 2013. Ammonium treatments to suppress toxic blooms of Prymnesium parvum in a subtropical lake of semi-arid climate: results from in situ mesocosm experiments. Water Research 47: 4274–4285.

    Article  CAS  PubMed  Google Scholar 

  • Guo, W., 1983. The reason for the fish death at aquacultural experimental station at Ningxia and the distribution of Prymnesium parvum in Ningxia. Jouranl of the Dalian Fisheries College 1: 43–48. (in Chinese).

    Google Scholar 

  • Guo, M., P. J. Harrison & F. J. R. Taylor, 1996. Fish kills related to Prymnesium parvum N. Carter (Haptophyta) in the People’s Republic of China. Jouranl of Applied Phycology 8: 111–117.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hambright, K. D., R. M. Zamor, J. D. Easton, K. L. Glenn, E. J. Remmel & A. C. Easton, 2010. Temporal and spatial variability of an invasive toxigenic protist in a North American subtropical reservoir. Harmful Algae 9: 568–577.

    Article  Google Scholar 

  • Hambright, K. D., 2012. Golden algae and the health of Oklahoma Lakes. Lakeline Fall issue: 33–38.

  • Hambright, K. D., J. D. Easton, R. M. Zamor, J. Beyer, A. C. Easton & B. Allison, 2014. Regulation of growth and toxicity of a mixotrophic microbe: implications for understanding range expansion in Prymnesium parvum. Freshwater Science 33: 745–754.

    Article  Google Scholar 

  • Hambright, K. D., J. E. Beyer, J. D. Easton, R. M. Zamor, A. C. Easton & T. C. Hallidayschult, 2015. The niche of an invasive marine microbe in a subtropical freshwater impoundment. ISME Journal 9: 256–264.

    Article  PubMed  Google Scholar 

  • Hansen, B., P. K. Bjornsen & P. J. Hansen, 1994. The size ratio between planktonic predators and their prey. Limnology and Oceanography 39: 395–403.

    Article  Google Scholar 

  • Harris, C. A., A. P. Scott, A. C. Johnson, G. H. Panter, D. Sheahan, M. Roberts & J. P. Sumpter, 2014. Principles of sound ecotoxicology. Environmental Science and Technology 46: 3100–3111.

    Article  CAS  Google Scholar 

  • Hayden, N. J., D. L. Roelke, B. W. Brooks, J. P. Grover, M. T. Neisch, T. W. Valenti Jr, K. N. Prosser, G. M. Gable, G. D. Umphres & N. C. Hewitt, 2012. Beyond hydraulic flushing: deep water mixing takes the harm out of a haptophyte bloom. Harmful Algae 20: 42–57.

    Article  Google Scholar 

  • Henrikson, J. C., M. S. Gharfeh, A. C. Easton, J. D. Easton, K. L. Glenn, M. Shadfan, S. L. Mooberry, K. D. Hambright & R. H. Cichewicz, 2010. Reassessing the ichthyotoxin profile of cultured Prymnesium parvum (golden algae) and comparing it to samples collected from recent freshwater bloom and fish kill events in North America. Toxicon 55: 1396–1404.

    Article  CAS  PubMed  Google Scholar 

  • Hughes-Martiny, J. B., B. J. M. Bohannan, J. H. Brown, R. K. Colwell, J. A. Fuhrman, J. L. Green, M. C. Horner-Devine, M. Kane, J. A. Krumins, C. R. Kuske, P. J. Morin, S. Naeem, L. Øvreås, A. L. Reysenbach, V. H. Smith & J. T. Staley, 2006. Microbial biogeography: putting microorganisms on the map. Nature 4: 102–112.

    Google Scholar 

  • Igarashi, T., M. Satake & T. Yasumoto, 1996. Prymnesin-2: a potent ichthyotoxic and hemolytic glycoside isolated from the red alga Prymnesium parvum. Journal of the American Chemical Society 118: 479–480.

    Article  CAS  Google Scholar 

  • Igarashi, T., M. Satake & T. Yasumoto, 1999. Structures and partial stereochemical assignments for prymnesin-1 and prymnesin-2: potent ichthyotoxic and hemolytic glycosides isolated from the red alga Prymnesium parvum. Journal of the American Chemical Society 121: 8499–8511.

    Article  CAS  Google Scholar 

  • Israel, N. M. D., M. N. VanLandeghem, S. D. Denny, J. Ingle & R. Patiño, 2014. Golden alga presence and abundance are inversely related to salinity in a high-salinity river ecosystem, Pecos River, USA. Harmful Algae 39: 81–91.

    Article  CAS  Google Scholar 

  • James, T. & A. De La Cruz, 1989. Prymnesium parvum Carter (Chrysophyceae) as a suspect of mass mortalities of fish and shellfish communities in western Texas. Texas Journal of Science 41: 429–430.

    Google Scholar 

  • James, S. V., T. W. Valenti, K. N. Prosser, J. P. Grover, D. L. Roelke & B. W. Brooks, 2011a. Sunlight amelioration of Prymnesium parvum acute toxicity to fish. Journal of Plankton Research 33: 265–272.

    Article  Google Scholar 

  • James, S. V., T. W. Valenti, D. L. Roelke, J. P. Grover & B. W. Brooks, 2011b. Probabilistic ecological assessment of microcystin-LR: a case study of allelopathy to Prymnesium parvum. Journal of Plankton Research 33: 319–332.

    Article  CAS  Google Scholar 

  • Johansson, N. & E. Granéli, 1999. Influence of different nutrient conditions on cell density, chemical composition and toxicity of Prymnesium parvum (Haptophyta) in semi-continuous cultures. Journal of Experimental and Marine Biology and Ecology 239: 243–258.

    Article  CAS  Google Scholar 

  • Johnsen, T. M., W. Eikrem, C. D. Olseng, K. E. Tollefsen & V. Bjerknes, 2010. Prymnesium parvum: the Norwegian experience. Journal of the American Water Resources Association 46: 6–13.

    Article  Google Scholar 

  • Jones, A. C., T. S. V. Liao, F. Z. Najar, B. A. Roe, K. D. Hambright & D. A. Caron, 2013. Seasonality and disturbance: annual pattern and response of the bacterial and microbial eukaryotic assemblages in a freshwater ecosystem. Environmental Microbiology 15: 2557–2572.

    Article  PubMed  Google Scholar 

  • Jonsson, P. R., H. Pacvia & G. Toth, 2009. Formation of harmful algal blooms cannot be explained by allelopathic interactions. Proceedings of the National Academy of Sciences 106: 11177–11182.

    Article  CAS  Google Scholar 

  • Kawachi, M., I. Inouye, O. Maeda & M. Chihara, 1991. The haptonema as a food-capturing device – observations on Chrysochromulinahirta (Prymnesiophyceae). Phycologia 30: 563–573.

    Article  Google Scholar 

  • Karp-Boss, L., E. Boss & P. A. Jumars, 1996. Nutrient fluxes to planktonic osmotrophs in the presence of fluid motion. Oceanography and Marine Biology: An Annual Review 34: 71–107.

    Google Scholar 

  • Katsiapi, M., P. Polykarpou, E. Michaloudi, K. A. Kormas, H. Karayanni & M. Moustaka-Gouni, 2014. Prymnesium parvum: invading the Mediterranean inland waters. Hydrobiologia In Review (this issue).

  • Kiely, T., D. Donaldson & A. Grube, 2004. Pesticides Industry Sales and Usage 2000 and 2001 Market Estimates. U.S. Environmental Protection Agency Technical Report: 48 pp.

  • Kimmel, B. L. & A. W. Groeger, 1984. Factors controlling primary production in lakes and reservoirs: a perspective. Lake and Reservoir Management 1: 277–281.

    Article  Google Scholar 

  • Koid, A. E., Z. Liu, R. Terrado, A. C. Jones, D. A. Caron & K. B. Heidelberg, 2014. Comparative transcriptome analysis of four prymnesiophyte algae. PLoS One 9: e97801.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Koski, M., M. Rosenberg, M. Viitasalo, S. Tanskanen & U. Sjolund, 1999. Is Prymnesium patelliferum toxic for copepods? Grazing, egg production, and egestion of the calanoid copepod Eurytemoraaffinis in mixtures of “good” and “bad” food. ICES Journal of Marine Science 56: 131–139.

    Article  Google Scholar 

  • Kurten, G. L., A. Barkoh, L. T. Fries & D. C. Begley, 2007. Combined nitrogen and phosphorus fertilization for controlling the toxigenic alga Prymnesium parvum. North American Journal of Aquaculture 69: 214–222.

    Article  Google Scholar 

  • Kurten, G. L., A. Barkoh, D. C. Begley & L. T. Fries, 2010. Refining nitrogen and phosphorus fertilization strategies for controlling the toxigenic alga Prymnesium parvum. Journal of the American Water Resources Association 46: 170–186.

    Article  CAS  Google Scholar 

  • Kurten, G. L., A. Barkoh, D. C. Begley & L. T. Fries, 2011. Nutrient manipulation to control the toxic alga Prymnesium parvum: verification of treatments and resolution of the issue of elevated pH. North American Journal of Aquaculture 73: 141–152.

    Article  Google Scholar 

  • La Claire II, J. W., 2006. Analysis of expressed sequence tags from the harmful alga, Prymnesuim parvum (Prymesiophyceae, Haptophyta). Marine Biotechnology 8: 534–546.

    Article  CAS  Google Scholar 

  • Lakshminarayana, J. S. S., H. J. O’Neill, S. D. Jonnavithula, D. A. Leger & P. H. Milburn, 1992. Impact of atrazine-bearing agricultural tile drainage discharge on planktonic drift of a natural stream. Environmental Pollution 76: 201–210.

    Article  CAS  PubMed  Google Scholar 

  • Landsberg, J. H., 2002. The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science 10: 113–390.

    Article  Google Scholar 

  • Larsen, A., 1999. Prymnesium parvum and P. patelliferum (Haptophyta) – one species. Phycologia 38: 541–543.

    Article  Google Scholar 

  • Larsen, A. & S. Bryant, 1998. Growth rate and toxicity of Prymnesium parvum and Prymnesium patelliferum (Haptophyta) in response to changes in salinity, light and temperature. Sarsia 83: 409–418.

    Google Scholar 

  • Legrand, C., N. Johansson, G. Johnsen, K. Y. Borsheim & E. Granéli, 2001. Phagotrophy and toxicity variation in the mixotrophic Prymnesium patelliferum (Haptophyceae). Limnology and Oceanography 46: 1208–1214.

    Article  Google Scholar 

  • Legrand, C., K. Rengefors, G. O. Fistarol & E. Granéli, 2003. Allelopathy in phytoplankton – biochemical, ecological and evolutionary aspects. Phycologia 42: 406–419.

    Article  Google Scholar 

  • Leibold, M. A., M. Holyoak, N. Mouquet, P. Amarasekare, J. M. Chase, M. F. Hoopes, R. D. Holt, J. B. Shurin, R. Law, D. Tilman, M. Loreau & A. Gonzalez, 2004. The metacommunity concept: a framework for multi-scale community ecology. Ecology Letters 7: 601–613.

    Article  Google Scholar 

  • Lewis, W. M. J., 1986. Evolutionary interpretations of allelochemical interactions in phytoplankton algae. American Naturalist 127: 184–194.

    Article  Google Scholar 

  • Lundgren, V. M., D. L. Roelke, J. P. Grover, B. W. Brooks, K. N. Prosser, W. C. Scott, C. A. Laws & G. D. Umphres, 2013. Interplay between ambient surface water mixing and manipulated hydraulic flushing: implications for harmful algal bloom mitigation. Ecological Engineering 60: 289–298.

    Article  Google Scholar 

  • Lundgren, V. M., D. L. Roelke, B. W. Brooks, E. Granéli, S. L. Davis, T. Baty & W. C. Scott, 2015. Prymnesium parvum invasion success into coastal bays of the Gulf of Mexico: Galveston Bay case study. Harmful Algae 43: 31–45.

    Article  Google Scholar 

  • Lutz-Carrillo, D. J., G. M. Southard & L. T. Fries, 2010. Global genetic relationships among isolates of golden alga (Prymnesium parvum). Journal of the American Water Resources Association 46: 24–32.

    Article  Google Scholar 

  • Manning, S. R. & J. W. La Claire II, 2013. Isolation of polyketides from Prymnesium parvum (Haptophyta) and their detection by liquid chromatography/mass spectrometry metabolic fingerprint analysis. Analytical Biochemistry 442: 189–195.

    Article  CAS  PubMed  Google Scholar 

  • Mariussen, E., G. N. Nelson & F. Fonnum, 2005. A toxic extract of the marine phytoflagellate Prymnesium parvum induces calcium-dependent release of glutamate from rate brain synaptasomes. Journal of Toxicology and Environmental Health Part A 68: 67–79.

    Article  CAS  PubMed  Google Scholar 

  • McKnight, D. M., S. W. Chisholm & D. R. F. Harleman, 1983. CuSO4 treatment of nuisance algal blooms in drinking water reservoirs. Environmental Management 7: 311–320.

    Article  CAS  Google Scholar 

  • Michaloudi, E., M. Moustaka-Gouni, S. Gkelis & K. Pantelidakis, 2009. Plankton community structure during an ecosystem disruptive algal bloom of Prymnesium parvum. Journal of Plankton Research 31: 301–309.

    Article  CAS  Google Scholar 

  • Michaloudi, E., M. Moustaka-Gouni, K. Pantelidakis, M. Katsiapi & S. Genitsaris, 2012. Plankton succession in the temporary Lake Koronia after intermittent dry-out. Journal of Plankton Research 31: 301–309.

    Article  CAS  Google Scholar 

  • Mitchell, J. G., L. Seuront, M. J. Doubell, D. Losic, N. H. Voelcker, J. Seymour & R. Lal, 2013. The role of diatom nanostructures in biasing diffusion to improve uptake in a patchy nutrient environment. PLoS One 8: e59548.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moestrup, O., 1994. Economic aspects: blooms, nuisance species, and toxins. In Green, J. C. & B. S. C. Leadbeater (eds), The Haptophyte Algae. Systematics Association Special, Vol. 51. Clarendon Press, Oxford: 265–285.

    Google Scholar 

  • Moeller, P. D., K. R. Beauchesne, K. M. Huncik, W. C. Davis, S. J. Christopher, P. Riggs-Gelasco & A. K. Gelasco, 2007. Metal complexes and free radical toxins produced by Pfiesteria piscicida. Environmental Science and Technology 41: 1166–1172.

    Article  CAS  PubMed  Google Scholar 

  • Monod, J., 1950. La technique de la culture continue: Theorie et applications. Annales d”Institut Pasteur, Lille 79: 390–410.

    CAS  Google Scholar 

  • Neisch, M. T., D. L. Roelke, B. W. Brooks, J. P. Grover & M. P. Masser, 2012. Stimulating effect of Anabaena sp. exudate on Prymnesium parvum. Journal of Phycology 48: 1045–1049.

    Article  Google Scholar 

  • Nejstgaard, J. C. & P. T. Solberg, 1996. Repression of copepod feeding and fecundity by the toxic haptophyte Prymnesium patelliferum. Sarsia 81: 339–344.

    Google Scholar 

  • Nelson, J. & M. Byrd, 2011. Occurrence of Prymnesium parvum (Golden Alga) in Texas intertidal waters 2008 and 2009. Management Data Series No. 264. Texas Parks and Wildlife Department: 26 pp.

  • Oikonomou, A., M. Katsiapi, H. Karayanni, M. Moustaka-Gouni & K. A. Kormas, 2012. Plankton microorganisms coinciding with two consecutive mass fish kills in a newly reconstructed lake. The Scientific World Journal. doi:10.1100/2012/504135.

    PubMed Central  PubMed  Google Scholar 

  • Padilla, G. M., 1970. Growth and toxigenesis of the chrysomonad Prymnesium parvum as a function of salinity. Journal of Protozoology 17: 456–462.

    Article  CAS  Google Scholar 

  • Palenik, B. & F. M. M. Morel, 1991. Comparison of cell-surface L-amino acid oxidases from several marine phytoplankton. Marine Ecology-Progress Series 59: 195–201.

    Article  Google Scholar 

  • Patiño, R., D. Dawson & M. M. VanLandeghem, 2014. Retrospective analysis of associations between water quality and toxic blooms of golden alga (Prymnesium parvum) in Texas reservoirs: Implications for understanding dispersal mechanisms and impacts of climate change. Harmful Algae 33: 1–11.

    Article  Google Scholar 

  • Pflugmacher, S., 2002. Possible allelopathic effects of cyanotoxins, with reference to microcystin-LR, in aquatic ecosystems. Environmental Toxicology 17: 407–413.

    Article  CAS  PubMed  Google Scholar 

  • Pienaar, R. N., 1980. Observations on the structure and composition of the cyst of Prymnesium (Prymnesiophyceae). Electron Microscopy Society of Southern Africa – Proceedings 10: 73–74.

    Google Scholar 

  • Prosser, K. N., T. W. Valenti Jr, N. J. Hayden, M. T. Neisch, N. Hewitt, G. D. Umphres, G. M. Gable, J. P. Grover, D. L. Roelke & B. W. Brooks, 2012. Low pH preempts bloom development of a toxic haptophyte. Harmful Algae 20: 156–164.

    Article  CAS  Google Scholar 

  • Remmel, E. J., N. Kohmescher, J. H. Larson & K. D. Hambright, 2011. An experimental analysis of harmful algae–zooplankton interactions and the ultimate defense. Limnology and Oceanography 56: 461–470.

    Article  Google Scholar 

  • Remmel, E. J. & K. D. Hambright, 2012. Toxin assisted micropredation: experimental evidence shows that contact micropredation rather than exotoxicity is the role of Prymnesium toxins. Ecology Letters 15: 126–132.

    Article  PubMed  Google Scholar 

  • Rhodes, K. & C. Hubbs, 1992. Recovery of the Pecos River from a red tide fish kill. Southwestern Naturalist 37: 178–187.

    Article  Google Scholar 

  • Roelke, D. L., R. Errera, R. Kiesling, B. W. Brooks, J. P. Grover, L. Schwierzke, F. Ureña-Boeck, J. Baker & J. L. Pinckney, 2007. Effects of nutrient enrichment on Prymnesium parvum population dynamics and toxicity: results from field experiments, Lake Possum Kingdom, USA. Aquatic Microbial Ecology 46: 125–140.

    Article  Google Scholar 

  • Roelke, D. L., G. M. Gable, T. W. Valenti, J. P. Grover, B. W. Brooks & J. L. Pinckney, 2010a. Hydraulic flushing as a Prymnesium parvum bloom-terminating mechanism in a subtropical lake. Harmful Algae 9: 323–332.

    Article  Google Scholar 

  • Roelke, D. L., L. Schwierzke, B. W. Brooks, J. P. Grover, R. M. Errera, T. W. Valenti Jr & J. L. Pinckney, 2010b. Factors influencing Prymnesium parvum population dynamics during bloom formation: results from in-lake mesocosm experiments. Journal of the American Water Resources Association 46: 76–91.

    Article  CAS  Google Scholar 

  • Roelke, D. L., J. P. Grover, B. W. Brooks, J. Glass, D. Buzan, G. M. Southard, L. Fries, G. M. Gable, L. Schwierzke-Wade, M. Byrd & J. Nelson, 2011. A decade of fish-killing Prymnesium parvum blooms in Texas: roles of inflow and salinity. Journal of Plankton Research 33: 243–254.

    Article  Google Scholar 

  • Roelke, D. L., B. W. Brooks, J. P. Grover, G. M. Gable, L. Schwierzke-Wade & N. C. Hewitt, 2012. Anticipated human population and climate change effects on algal blooms of a toxic haptophyte in the south-central USA. Canadian Journal of Fisheries and Aquatic Sciences 69: 1389–1404.

    Article  Google Scholar 

  • Roelke, D. L., H.-P. Li, N. J. Hayden, C. J. Miller, S. E. Davis, A. Quigg & Y. Buyukates, 2013. Co-occurring and opposing freshwater inflow effects on phytoplankton biomass, productivity and community composition of Galveston Bay, USA. Marine Ecology Progress Series 477: 61–76.

    Article  Google Scholar 

  • Rosetta, C. H. & G. B. McManus, 2003. Feeding by ciliates on two harmful algal bloom species, Prymnesium parvum and Prorocentrum minimum. Harmful Algae 2: 109–126.

    Article  Google Scholar 

  • Sager, A. Barkoh, D. L. Buzan, L. Fries, J. Glass, G. Kurten, J. Ralph, L. Singhurst, G. Southard & L. Riley, 2008. Toxic Prymnesium parvum: a potential threat to U.S. Reservoirs. In Allen, M. S., S. Sammons & M. J. Maccina (eds), Balancing Fisheries Management and Water Uses for Impounded River Systems. American Fisheries Society, Bethesda, MD: 261–273.

    Google Scholar 

  • Schwierzke, L., D. L. Roelke, B. W. Brooks, J. P. Grover, T. W. Valenti Jr, M. Lahousse, C. J. Miller & J. L. Pinckney, 2010. Prymnesium parvum population dynamics during bloom development: a role assessment of grazers and virus. Journal of American Water Resources Association 46: 63–75.

    Article  CAS  Google Scholar 

  • Schwierzke-Wade, L., D. L. Roelke, B. W. Brooks, J. P. Grover & T. W. ValentiJr, 2011. Prymnesium parvum bloom termination: role of hydraulic dilution. Journal of Plankton Research 33: 309–318.

    Article  Google Scholar 

  • Shilo, M., 1967. Formation and mode of action of algal toxins. Bacteriological Reviews 31: 180–193.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Shilo, M. & M. Aschner, 1953. Factors governing the toxicity of cultures containing the phytoflagellate Prymnesium parvum Carter. Journal of General Microbiology 8: 333–343.

    Article  CAS  PubMed  Google Scholar 

  • Skingel, T. R., S. E. Spencer, C. Q. Le 1, C. A. Serrano, L. D. Mydlarz, B. J. Scarbrough, K. A. Schug, B. W. Brooks & J. P. Grover, 2010. Hemolytic toxicity and nutritional status of Prymnesium parvum during population growth. Aquatic Microbial Ecology 61: 141–148.

    Article  Google Scholar 

  • Skovgaard, A. & P. J. Hansen, 2003. Food uptake in the harmful alga Prymnesium parvum mediated by excreted toxins. Limnology and Oceanography 48: 1161–1166.

    Article  CAS  Google Scholar 

  • Smayda, T. J., 1990. Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic. In Granéli, E. (ed.), Toxic Marine Phytoplankton. Elsevier, New York: 29–40.

    Google Scholar 

  • Sopanen, S., M. Koski, P. Kuuppo, P. Uronen, C. Legrand & T. Tamminen, 2006. Toxic haptophyte Prymnesium parvum affects grazing, survival, egestion and egg production of the calanoid copepods Eurytemora affinis and Acartia bifilosa. Marine Ecology Progress Series 327: 223–232.

    Article  CAS  Google Scholar 

  • Southard, G. M., L. T. Fries & A. Barkoh, 2010. Prymnesium parvum: the Texas experience. Journal of the American Water Resources Association 46: 14–23.

    Article  Google Scholar 

  • Sterner, R. W., 1989. The role of grazers in phytoplankton succession. In Sommer, U. (ed.), Plankton Ecology. Springer, Berlin: 107–170.

    Chapter  Google Scholar 

  • Talarski, A. E., 2014. Genetic basis for ichthyotoxicity and osmoregulation in the euryhaline haptophyte, Prymnesium parvum N. Carter. Ph.D. Dissertation, University of Texas at Austin: 141 pp.

  • Texas Water Development Board (TWDB), 2012. Water for Texas 2012 State Water Plan: 314 pp. http://www.twdb.texas.gov/waterplanning/swp/2012/index.asp.

  • Texas Parks & Wildlife Department (TPWD), 2003. Prymnesium parvum, Workshop Report, Austin, TX. http://www.tpwd.state.tx.us/landwater/water/environconcerns/hab/.

  • Tillmann, U., 2003. Kill and eat your predator: a winning strategy of the planktonic flagellate Prymnesium parvum. Aquatic Microbial Ecology 32: 73–84.

    Article  Google Scholar 

  • Ulitzur, S. & M. Shilo, 1964. A sensitive assay system for determination of the ichthyotoxicity of Prymnesium parvum. Journal of General Microbiology 36: 161–169.

    Article  CAS  PubMed  Google Scholar 

  • Ulitzur, S. & M. Shilo, 1966. Mode of action of Prymnesium parvumi chthyotoxin. Journal of Protozoology 13: 332–336.

    Article  CAS  Google Scholar 

  • Umphres IV, G. D., D. L. Roelke & M. D. Netherland, 2012. A chemical approach for the mitigation of Prymnesium parvum blooms. Toxicon 60: 1235–1244.

    Article  CAS  PubMed  Google Scholar 

  • Umphres IV, G. D., D. L. Roelke & M. D. Netherland, 2013. The potential algaecide flumioxazin has little effect on growth, survival and feed conversion of the bluegill sunfish Lepomis macrochirus. Aquaculture 380–383: 80–83.

    Article  CAS  Google Scholar 

  • Uronen, P., S. Lehtinen, C. Legrand, P. Kuuppo & T. Tamminen, 2005. Haemolytic activity and allelopathy of the haptophyte Prymnesium parvum in nutrient-limited and balanced growth conditions. Marine Ecology Progress Series 299: 137–148.

    Article  Google Scholar 

  • Valenti Jr, T. W., S. V. James, M. Lahousse, K. A. Schug, D. L. Roelke, J. P. Grover & B. W. Brooks, 2010a. A mechanistic explanation for pH-dependent ambient aquatic toxicity of Prymnesium parvum Carter. Toxicon 55: 990–998.

    Article  CAS  PubMed  Google Scholar 

  • Valenti Jr, T. W., S. V. James, M. Lahousse, K. A. Schug, D. L. Roelke, J. P. Grover & B. W. Brooks, 2010b. Influence of pH on amine toxicity and implications for harmful algal bloom ecology. Toxicon 55: 1038–1043.

    Article  CAS  Google Scholar 

  • Van Dolah, F. M., D. L. Roelke & R. Greene, 2001. Health and ecological impacts of harmful algal blooms: risk assessment needs. Human and Ecological Risk Assessment 7: 1329–1345.

    Article  Google Scholar 

  • VanLandeghem, M. M., M. D. Meyer, S. B. Cox, B. Sharma & R. Patiño, 2012. Spatial and temporal patterns of surface water quality and ichthyotoxicity in urban and rural river basins in Texas. Water Research 46: 6638–6651.

    Article  CAS  PubMed  Google Scholar 

  • VanLandeghem, M. M., M. Farooqi, B. Farquhar & R. Patiño, 2013. Impacts of Golden Alga Prymnesium parvum on fish populations in reservoirs of the upper Colorado River and Brazos River basins, Texas. Transactions of the American Fisheries Society 142: 581–595.

    Article  Google Scholar 

  • VanLandeghem, M. M., M. Farooqi, G. M. Southard & R. Patiño, 2014a. Associations between water physicochemistry and Prymnesium parvum presence, abundance, and toxicity in west Texas reservoirs. Journal of the American Water Resources Association. doi:10.1111/jawr.12262.

    Google Scholar 

  • VanLandeghem, M. M., M. Farooqi, G. M. Southard & R. Patiño, 2014b. Spatiotemporal associations of reservoir nutrient characteristics and the invasive Prymnesium parvum in west Texas. Journal of the American Water Resources Association. doi:10.1111/jawr.12261.

    Google Scholar 

  • Vasas, G., M. M-Hamvas, G. Borics, S. Gonda, C. Mathe, K. Jambrik & Z. L. Nagy, 2012. Occurrence of toxic Prymnesium parvum blooms with high protease activity is related to fish mortality in Hungarian ponds. Harmful Algae 17: 102–110.

    Article  Google Scholar 

  • Weissbach, A. & C. Legrand, 2012. Effect of different salinities on growth and intra- and extracellular toxicity of four strains of the haptophyte Prymnesium parvum. Aquatic Microbial Ecology 67: 139–149.

    Article  Google Scholar 

  • Wurbs, R. A., A. S. Karama, I. Saleh & C. K. Ganze, 1993. Natural salt pollution and water supply reliability in the Brazos River basin. Technical Report No. 160, Texas Water Resources Institute: 177 pp.

  • Yariv, J. & S. Hestrin, 1961. Toxicity of the extracellular phase of Prymnesium parvum cultures. Journal of General Microbiology 24: 165–175.

    Article  CAS  PubMed  Google Scholar 

  • Yates, B. S. & W. J. Rogers, 2011. Atrazine selects for ichthyotoxic Prymnesium parvum, a possible explanation for golden algae blooms in lakes of Texas, USA. Ecotoxicology 20: 2003–2010.

    Article  CAS  PubMed  Google Scholar 

  • Zamor, R. M., N. R. Franssen, C. Porter, T. M. Patton & K. D. Hambright, 2014. Rapid recovery of a fish assemblage following an ecosystem disruptive algal bloom. Freshwater Science 33: 390–401.

    Article  Google Scholar 

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Acknowledgments

These sorts of unfunded writing projects actually do require funding, and the co-authors are grateful to their institutes for the indirect support received as part of their position responsibilities. Those institutes are Texas A&M University, Texas Parks and Wildlife Department, Baylor University, University of Texas at Arlington, University of Oklahoma, University of Texas at Austin, National Centers for Coastal Ocean Science, and Texas Cooperative Fish and Wildlife Research Unit (which is jointly supported by U.S. Geological Survey, Texas Tech University, Texas Parks and Wildlife Department, The Wildlife Management Institute, and U.S. Fish and Wildlife Service).

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Authors and Affiliations

  1. Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX, 77843, USA

    Daniel L. Roelke

  2. Inland Fisheries Division, Heart of the Hills Fisheries Science Center, Texas Parks and Wildlife Department, 5103 Junction Highway, Mountain Home, TX, 78058, USA

    Aaron Barkoh

  3. Department of Environmental Science and Center for Reservoir and Aquatic Systems Research, Baylor University, Waco, USA

    Bryan W. Brooks

  4. Department of Biology and Program in Earth and Environmental Science, University of Texas at Arlington, Box 19498, Arlington, USA

    James P. Grover

  5. Program in Ecology and Evolutionary Biology, Department of Biology, University of Oklahoma, Norman, OK, 73019, USA

    K. David Hambright

  6. Department of Molecular Biosciences, University of Texas at Austin, Austin, TX, 78712, USA

    John W. LaClaire II

  7. NOAA Hollings Marine Laboratory, National Centers for Coastal Ocean Science, 331 Fort Johnson Road, Charleston, SC, 29412, USA

    Peter D. R. Moeller

  8. U.S. Geological Survey, Texas Cooperative Fish and Wildlife Research Unit and Departments of Natural Resources Management and Biological Sciences, Texas Tech University, Lubbock, TX, 79409-2120, USA

    Reynaldo Patino

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Correspondence to Daniel L. Roelke.

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Guest editors: Luigi Naselli-Flores & Judit Padisák / Biogeography and Spatial Patterns of Biodiversity of Freshwater Phytoplankton

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Roelke, D.L., Barkoh, A., Brooks, B.W. et al. A chronicle of a killer alga in the west: ecology, assessment, and management of Prymnesium parvum blooms. Hydrobiologia 764, 29–50 (2016). https://doi.org/10.1007/s10750-015-2273-6

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