Toxigenic Pfiesteria species-Updates on biology, ecology, toxins, and impacts

Harmful Algae

Volumn 14, Issue , 2012, Pages 196-230

  Burkholder, JoAnn M ^a   Marshall, Harold G ^b  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b OLD DOMINION UNIVERSITY   (United States)

Author keywords

Axenic; Estuaries Fish kills; Nutrients; Nutrition; Phagotrophy; Toxins

Indexed keywords

ALGAE; BREVOORTIA TYRANNUS; DINOPHYCEAE; MAMMALIA; PFIESTERIA; PFIESTERIA PISCICIDA; PFIESTERIA SHUMWAYAE;

EID: 84856095251     PISSN: 15689883     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.hal.2011.10.022     Document Type: Article

References (286)

1. Abraham A., Plakas S.M., Wang Z., Jester E., El Said K.R., Granade H., Henry M., Blum P., Pierce R., Dickey R.W. Characterization of polar brevetoxin derivatives isolated from Karenia brevis cultures and natural blooms. Toxicon 2006, 48:104-115.
2. Adolf J.E., Bachvaroff T., Place A.R. Can cryptophyte abundance trigger toxic Karlodinium veneficum blooms in eutrophic estuaries?. Harmful Algae 2008, 8:119-128.
3. Adolf J.E., Krupatkina D., Bachvaroff T., Place A.R. Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae 2007, 6:400-412.
4. Ajuzie C.C. Toxic Prorocentrum lima induces abnormal behaviour in juvenile sea bass. J. Appl. Phycol. 2008, 20:19-27.
5. Alavi M.R. Predator/prey interaction between Pfiesteria piscicida and Rhodomonas mediated by a marine alpha proteobacterium. Microb. Ecol. 2004, 47:48-58.
6. Anderson J.T., Hood R.R., Zhang X. Quantification of Pfiesteria piscicida growth and encystment parameters using a numerical model. Mar. Ecol. Prog. Ser. 2003, 246:105-113.
7. Bacvaroff T.R., Adolf J.E., Squier A.H., Harvey H.R., Place A.R. Characterization and quantification of karlotoxins by liquid chromatography - mass spectrometry. Harmful Algae 2008, 7:473-484.
8. Bachvaroff T.R., Adolf J.E., Place A.R. Strain variation in Karlodinium veneficum (Dinophyceae): toxin profiles, pigments, and growth characteristics. J. Phycol. 2009, 45:137-153.
9. Backer L.C., Niskar A.S., Rubin C., Blindauer K., Christianson D., Naeher L., Rogers H.S. Environmental public health surveillance: possible estuary-associated syndrome. Environ. Health Perspect. 2001, 109:797-801.
10. Baek S.H., You K., Katano T., Shin K. Effects of temperature, salinity, and prey organisms on the growth of three Pfiesteria-like heterotrophic dinoflagellates. Plankton Benthos Res. 2010, 5:31-38.
11. Baker J.A., Ferguson M.S. Growth of platyfish (Platypoecilus maculatus) free from bacteria and other microorganisms. Proc. Soc. Exp. Biol. Med. 1942, 51:116-119.
12. Bates H.A., Kostricken R., Rapoport H. The occurrence of saxitoxin and other toxins in various dinoflagellates. Toxicon 1978, 16:595-601.
13. Bates S.S., Douglas D.J., Doucette G.J., Léger C. Enhancement of domoic acid production by reintroducing bacteria to axenic cultures of the diatom Pseudo-nitzschia multiseries. Nat. Toxins 1995, 3:428-435.
14. Bentley R., Bennett J.W. Construction polyketides: from collie to combinatorial biosynthesis. Annu. Rev. Microbiol. 1999, 53:411-446.
15. Bergmann F., Parnas I., Reich K. Observations on the mechanism of action and on the quantitative assay of ichthyotoxin from Prymnesium parvum Carter. Toxicol. Appl. Pharmacol. 1963, 5:637-649.
16. Berry J.P., Reece K.S., Rein K.S., Baden D.G., Haas L.W., Ribeiro W.L., Shields J.D., Snyder R.V., Vogelbein W.K., Gawley R.E. Are Pfiesteria species toxicogenic? Evidence against production of ichthyotoxins by Pfiesteria shumwayae. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:10970-10975.
17. Blackwell, A.H., 2004. Reviews of journal manuscripts: nasty, petty, arrogant. The Chronicle of Higher Education 46, B10, June 2.
18. Blazer V.S., Lilley J.H., Schill W.B., Kiryu Y., Densmore C.L., Panyawachira V., Chinabut S. Aphanomyces invadans in Atlantic menhaden along the east coast of the United States. J. Aquat. Anim. Health 2002, 14:1-10.
19. Blazer V.S., Vogelbein W.K., Densmore C.L., May E.B., Lilley J.H., Zwerner D.E. Aphanomyces as a cause of ulcerative skin lesions of menhaden from Chesapeake Bay tributaries. J. Aquat. An. Health 1999, 11:340-349.
20. Boczar B.A., Beitler M.K., Liston J., Sullivan J.J., Cattolico R.A. Paralytic shellfish toxins in Protogonyaulax tamarensis and Protogonyaulax catenella in axenic culture. Plant Physiol. 1988, 88:1285-1290.
21. Boenigk J., Arndt H. Comparative studies on the feeding behavior of two heterotrophic nanoflagellates: the filter feeding choanoflagellate Monosiga ovata and the raptorial feeding kinetoplastid Rhynchomonas nasuta. Aquat. Microb. Ecol. 2000, 22:243-249.
22. Boesch D. Presentation to the Society of Environmental Journalists 2002, Society of Environmental Journalists, Baltimore, MD, October.
23. Bomber J.W., Tindall D.R., Miller D.M. Genetic variability in toxin potencies among seventeen clones of Gambierdiscus toxicus (Dinophyceae). J. Phycol. 1989, 25:617-625.
24. Botes L., Smit A.J., Cook P.A. The potential threat of algal blooms to the abalone (Haliotis midae) mariculture industry situated around the South African coast. Harmful Algae 2003, 2:247-259.
25. Bourdelais A., Tomas C., Naar J., Kubanek J., Baden D. New fish-killing alga in coastal Delaware produces neurotoxins. Environ. Health Perspect. 2002, 110:465-470.
26. Bowers H.A., Tengs T., Glasgow H.B., Burkholder J.M., Rublee P.A., Oldach D.W. Development of real-time PCR assays for rapid detection of Pfiesteria piscicida and related dinoflagellates. Appl. Environ. Microbiol. 2000, 66:4641-4648.
27. Bowers H.A., Trice T.M., Magnien R.E., Goshorn D.M., Michael B., Schaefer E.F., Rublee P.A., Oldach D.W. Detection of Pfiesteria spp. by PCR in surface sediments collected from Chesapeake Bay tributaries (Maryland). Harmful Algae 2006, 5:342-351.
28. Boyer G.L. The occurrence of cyanobacterial toxins in New York lakes: lessons from the MERHAB-Lower Great Lakes program. Lake Reservoir Manage. 2007, 23:153-160.
29. Brown E.M. On Oodinium ocellatum Brown, a parasitic dinoflagellate causing epidemic disease in marine fish. Proc. Zool. Soc. Lond. 1934, 3:583-607.
30. Burkholder J., Eggleston D., Glasgow H., Brownie C., Reed R., Melia G., Kinder C., Janowitz G., Corbett R., Posey M., Alphin T., Toms D., Deamer N., Springer J. Comparative impacts of two major hurricane seasons on the Neuse River and western Pamlico Sound. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:9291-9296.
31. Burkholder J.M., Glasgow H.B. Pfiesteria piscicida and other Pfiesteria-like dinoflagellates: Behavior, impacts, and environmental controls. Limnol. Oceanogr. 1997, 42:1052-1075.
32. Burkholder J.M., Glasgow H.B. Science ethics and its role in early suppression of the Pfiesteria issue. Hum. Organ. 1999, 58:443-455.
33. Burkholder J.M., Glasgow H.B. The life cycle and toxicity of Pfiesteria piscicida, revisited. J. Phycol. 2002, 38:1261-1267.
34. Burkholder J.M., Glasgow H.B., Deamer-Melia N.J. Overview and present status of the toxic Pfiesteria complex. Phycologia 2001, 40:186-214.
35. Burkholder J.M., Glasgow H.B., Deamer-Melia N., Springer J., Parrow M.W., Zhang C., Cancellieri P.J. Species of the toxic Pfiesteria complex, and the importance of functional type in data interpretation. Environ. Health Perspect. 2001, 109:715-730.
36. Burkholder J.M., Marshall H.G., Glasgow H.B., Seaborn D.W., Deamer-Melia N.J. The standardized fish bioassay procedure for detecting and culturing actively toxic Pfiesteria, used by two reference laboratories for Atlantic and Gulf Coast states. Environ. Health Perspect. 2001, 109:745-756.
37. Burkholder J.M., Glibert P.M. Intraspecific variability: an important consideration in forming generalizations about toxigenic algal species. Afr. J. Mar. Sci. 2006, 28:177-180.
38. Burkholder J.M., Glibert P.M., Skelton H. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 2008, 8:77-93.
39. Burkholder J.M., Gordon A.S., Moeller P.D., Law J.M., Coyne K.J., Lewitus A.J., Ramsdell J.S., Marshall H.G., Deamer N.J., Cary S.C., Kempton J.W., Morton S.L., Rublee P.A. Demonstration of toxicity to fish and to mammalian cells by Pfiesteria species: comparison of assay methods and multiple strains. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:3471-3476.
40. Burkholder J.M., Mallin M.A., Glasgow H.B. Fish kills, bottom-water hypoxia, and the toxic Pfiesteria complex in the Neuse River and Estuary. Mar. Ecol. Prog. Ser. 1999, 179:301-310.
41. Calbet A., Bertos M., Fuentes-Grühewald C., Alacid E., Figueroa R., Renom B., Garcés E. Intraspecific variability in Karlodinium veneficum: growth rates, mixotrophy, and lipid composition. Harmful Algae 2011, 10:654-667.
42. Cancellieri P.J., Burkholder J.M., Deamer-Melia N.J., Glasgow H.B. Chemosensory attraction of zoospores of the estuarine dinoflagellates, Pfiesteria piscicida and P. shumwayae, to finfish mucus and excreta. J. Exp. Mar. Biol. Ecol. 2001, 264:29-45.
43. Caron D.A. Enrichment, isolation, and culture of free-living heterotrophic flagellates. Handbook of Methods in Aquatic Microbial Ecology 1993, 77-89. CRC Press, Boca Raton, FL. P.F. Kemp, B.F. Sherr, E.B. Sherr, J.J. Cole (Eds.).
44. Centers for Disease Control and Prevention (CDC) Notice to readers: possible estuary associated syndrome. Morb. Mortal. Wkly. Rep. 1999, 48:381-382.
45. Centers for Disease Control and Prevention (CDC) Surveillance for possible estuary-associated syndrome - six states, 1998-1999. Morb. Mortal. Wkly. Rep. 2000, 49:372-374.
46. Chang F.H., Anderson D.M., Kulis D.M., Till D.G. Toxin production of Alexandrium minutum (Dinophyceae) from the Bay of Plenty, New Zealand. Toxicon 1997, 35:393-409.
47. Chinain M., Laurent N., Pauillac S., Legrand A.M. Effects of an artificial medium and axenic culturing on toxicity of cultured Gambierdiscus toxicus. Proceedings of the International Symposium on Ciguatera and Marine Natural Products 1994, 91-98. Asian Pacific Research Foundation, Honolulu. Y. Hokama, P.J. Scheuer, T. Yasumoto (Eds.).
48. Chinain M., Darius H.T., Ung A., Cruchet P., Wang Z., Ponton D., Laurent D., Pauillac S. Growth and toxin production in the ciguatera-causing dinoflagellate Gambierdiscus polynesiensis (Dinophyceae) in culture. Toxicon 2009, 10.1016/j.toxicon.2009.06.013.
49. Chubin D.E., Hackett E.J. Peerless Science: Peer Review and U.S. Science Policy 1990, State University of New York (SUNY) Press, NY.
50. Coyne K.J., Hare C.E., Popels L.C., Hutchins D.A., Cary S.C. Distribution of Pfiesteria piscicida cyst populations in sediments of the Delaware Inland Bays, USA. Harmful Algae 2006, 5:363-373.
51. Coyne K.J., Hutchins D.A., Hare C.E., Cary S.C. Assessing temporal and spatial variability in Pfiesteria piscicida distributions using molecular probing techniques. Aquat. Microb. Ecol. 2001, 24:275-285.
52. Cusack C.K., Bates S.S., Quilliam M.A., Patching J.W., Raine R. Confirmation of domoic acid production by Pseudo-nitzschia australis (Bacillariophyceae) isolated from Irish waters. J. Phycol. 2002, 38:1106-1112.
53. Dafni Z., Shilo M. The cytotoxic principle of the phytoflagellate Prymnesium parvum. J. Cell Biol. 1966, 28:461-471.
54. Dafni Z. The cytotoxin of Prymnesium parvum. J. Protozool. 1964, 11(Suppl.):461-471. (Article 128).
55. Deeds J.R., Terlizzi D.E., Adolf J.E., Stoecker D.K., Place A.R. Toxic activity from cultures of Karlodinium micrum (= Gyrodinium galatheanum) (Dinophyceae) - a dinoflagellate associated with fish mortalities in an estuarine aquaculture facility. Harmful Algae 2004, 1:169-189.
56. Douglas D.J., Bates S.S. Production of domoic acid, a neurotoxic amino acid, by an axenic culture of the marine diatom Nitzschia pungens f. multiseries Hasle. Can. J. Fish. Aquat. Sci. 1992, 49:85-90.
57. Dowhan W. Molecular basis for membrane phospholipid diversity: why are there so many lipids?. Annu. Rev. Biochem. 1997, 66:199-232.
58. Drebes G., Schnepf E. Paulsenella Chatton (Dinophyta), ectoparasites of marine diatoms: development and taxonomy. Helgoland. Meeresunt. 1988, 42:563-581.
59. Drgon T., Saito K., Gillevet P.M., Sikaroodi M., Whitaker B., Krupatkina D.N., Argemi F., Vasta G.R. Characterization of ichthyocidal activity of Pfiesteria piscicida: dependence on the dinospore cell density. Appl. Environ. Microbiol. 2005, 71:519-529.
60. Droop M.R. Water-soluble factors in the nutrition of Oxyrrhis marina. J. Mar. Biol. Assoc. U.K. 1959, 38:605-620.
61. Droop M.R. Nutritional investigation of phagotrophic protozoa under axenic conditions. Helegol. Wiss. Meersunters. 1970, 20:272-277.
62. Duncan P.M., Parris B., Schultz S., Jones J., Gordon A., Dyer B., Marshall H. Behavioral effects and drug vulnerability in rats exposed to Pfiesteria toxin. Neurotoxicol. Teratol. 2005, 27:701-710.
63. Egerton T.A., Marshall H.G. Feeding preferences and grazing rates of Pfiesteria piscicida and a cryptoperidiniopsoid preying on fish blood cells and algal prey. Harmful Algae 2006, 5:419-426.
64. Elbrächter M., Meyer B. Plate pattern variability and plate overlap in a clonal culture of the freshwater dinoflagellate, Peridinium umbonatum Stein species complex (Dinophyta). Neues Jahrbuch für Palaentologie Abhandlungen 2001, 219:221-227.
65. Eriksen N.T., Hayes K.C., Lewitus A.J. Growth responses of the mixotrophic dinoflagellates, Cryptoperidiniopsis sp. and Pfiesteria piscicida, to light under prey-saturated conditions. Harmful Algae 2002, 1:191-203.
66. Errera R.M., Campbell L. Osmotic stress triggers toxin production by the dinoflagellate Karenia brevis. Proc. Natl. Acad. Sci. U.S.A. 2011, 10.1073/pnas.1104247108.
67. Fairey E.R., Edmunds J.S., Deamer-Melia N.J., Glasgow H.B., Johnson F.M., Moeller P.R., Burkholder J.M., Ramsdell J.S. Reporter gene assay for fish killing activity produced by Pfiesteria piscicida. Environ. Health Perspect. 1999, 107:711-714.
68. Fairey E.R., Edmunds J.S.G., Ramsdell J.S. A cell based assay for brevetoxins, saxitoxins and ciguatoxins using a stably expressed c-fos-luciferase reported gene. Anal. Biochem. 1997, 25:129-132.
69. Feinstein T.N., Traslavina R., Sun M.-Y., Lin S. Effects of light on photosynthesis, grazing, and population dynamics of the heterotrophic dinoflagellate Pfiesteria piscicida (Dinophyceae). J. Phycol. 2002, 38:659-669.
70. Felsenstein J. Inferring Phylogenies 2004, Sinauer Associates, Inc., Sunderland, MA, 664 p.
71. Fensin E.E. Occurrence and ecology of the dinoflagellate Karlodinium micrum in estuaries of North Carolina, USA. Harmful Algae 2002 2004, 62-64. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, St. Petersburg, FL. K.A. Steidinger, J.H. Landsberg, C.R. Tomas, G.A. Vargo (Eds.).
72. Fensome R.A., Taylor F.J.R., Norris G., Sarjeant W.A.S., Wharton D.I., Williams G.L. A Classification of Living and Fossil Dinoflagellates. Micropaleontology 1993, Sheridan Press, Hanover, PA, 351 p. (Special Publication Number 7).
73. Fleming J.J., Du Bois J. A synthesis of (+)-saxitoxin. J. Am. Chem. Soc. 2006, 128:3926-3927.
74. Freitag M., Beszteri S., Vogel H., John U. Effects of physiological shock treatments on toxicity and polyketide synthase gene expression in Prymnesium parvum (Prymnesiophyceae). Eur. J. Phycol. 2011, 46:193-201.
75. Gabrielsen T.M., Minge M.A., Espelund M., Tooming-Klunderud A., Patil V., Nederbragt A.J., Otis C., Turmel M., Shalchian-Tabriz K., Lemieux C., Jakobsen K.S. Genome evolution of a tertiary dinoflagellate plastid. PLoS ONE 2011, 6(4):e19132. 10.1371/journal.pone.0019132.
76. Garrison D.L., Conrad S.M., Eilers P.P., Waldron E.M. Confirmation of domoic acid production by Pseudonitzschia australis (Bacillariophyceae) cultures. J. Phycol. 1992, 28:604-607.
77. Gifford D.J., Caron D.A. Sampling, preservation, enumeration and biomass of protozooplankton. ICES Zooplankton Methodology Manual 2000, 193-221. Academic Press, London. R.P. Harris, H.-R. Skjoldal, J. Lenz, P.J. Wiebe, M.E. Huntley (Eds.).
78. Giner J.-L., Zhao H., Tomas H.C. Sterols and fatty acids of three harmful algae previously assigned as Chattonella. Phytochemistry 2008, 59:2167-2171.
79. Glasgow H.B., Burkholder J.M., Mallin M.A., Deamer-Melia N.J., Reed R.E. Field ecology of toxic Pfiesteria complex species, and a conservative analysis of their role in estuarine fish kills. Environ. Health Perspect. 2001, 109:715-730.
80. Glasgow H.B., Burkholder J.M., Morton S.L., Springer J. A second species of ichthyotoxic Pfiesteria (Dinamoebales, Dinophyceae). Phycologia 2001, 40:234-245.
81. Glasgow H.B., Burkholder J.M., Schmechel D.E., Tester P.A., Rublee P.A. Insidious effects of a toxic estuarine dinoflagellate on fish survival and human health. J. Toxicol. Environ. Health 1995, 46:501-522.
82. Glibert P.M., Burkholder J.M., Parrow M.W., Lewitus A.J., Gustafson D.E. Direct uptake of nitrogen by Pfiesteria piscicida and Pfiesteria shumwayae, and nitrogen nutritional preferences. Harmful Algae 2006, 5:380-394.
83. Gordon A.S., Dyer B. Relative contribution of exotoxin and micropredation to ichthyotoxicity of two strains of Pfiesteria shumwayae (Dinophyceae). Harmful Algae 2005, 4:423-431.
84. Gordon A.S., Dyer B.J., Seaborn D., Marshall H.G. Comparative toxicity of Pfiesteria spp., prolonging toxicity of P. piscicida in culture and evaluation of toxin(s) stability. Harmful Algae 2002, 1:85-94.
85. Gordon A.S., Marshall H.G., Shumway H.G., Coyne S.E., Lewitus K.J., Lewitus A.J., Mallin M.A., Rublee P.A. Characterization of Pfiesteria ichthyocidal activity. Appl. Environ. Microbiol. 2005, 71:6463-6464.
86. Granéli, E., Edvardsen, B., Roelke, D.L., Hagström, J.A. The ecophysiology and bloom dynamics of Prymnesium spp. Harmful Algae, this issue, doi:10.1016/j.hal.2011.10.024.
87. Grattan L.M., Oldach D., Perl T.M., Lowitt M.H., Matuszak D.L., Dickson C., Parrott C., Shoemaker R.C., Wasserman M., Hebel J.R., Charache P., Morris J.G. Problems in learning and memory occur in persons with environmental exposure to waterways containing toxin-producing Pfiesteria or Pfiesteria-like dinoflagellates. Lancet 1998, 352:532-539.
88. Griffith, D., Shecter, A., Borre, K, Kelley, V., 1998. Occupational risks of crabbing: a report with special emphasis on the public health threat of Pfiesteria piscicida. An exploratory study of possible human health effects of deteriorating water quality among North Carolina crabbers, research on toxic algae: Pfiesteria-like organisms. North Carolina Sea Grant Publication No. UNC-56-98-02. North Carolina State University, Raleigh, NC.
89. Guillard R.R.L. Culture of phytoplankton for feeding marine invertebrates. Culture of Marine Invertebrate Animals 1975, 29-60. Plenum Press, New York. W.L. Smith, M.H. Chanley (Eds.).
90. Guillard R.R.L. Culture methods. Manual on Harmful Marine Microalgae. IOC Manual and Guides No. 33 1995, 45-62. UNESCO, Paris. G.M. Hallegraeff, D.M. Anderson, A.D. Cembella (Eds.).
91. Guillard R.R.L., Keller M.D. Culturing dinoflagellates. Dinoflagellates 1984, 391-442. Academic Press, London. D.L. Spector (Ed.).
92. Guisande C.M., Frangópulos M., Maneiro I., Vergara A.R., Riveiro I. Ecological advantages of toxin production by the dinoflagellate Alexandrium minutum under phosphorus limitation. J. Microbiol. Methods 2007, 69:425-430.
93. Guynup, S., 2002. When a Tiny Microbe Became a Cash Cow. Blue Ridge Press, Monday, August 12. Available at: http://sharonguynup.com/Sharon_Website/Articles_1_1_files/BRP%2520Pfiesteria.pdf.
94. Hansen P.J. Phagotrophic mechanisms and prey selection in mixotrophic phytoflagellates. Physiological Ecology of Harmful Algal Blooms 1998, 525-537. Springer-Verlag, Berlin. D.M. Anderson, A.D. Cembella, G.M. Hallegraeff (Eds.).
95. Hansen P.J., Calado A.J. Phagotrophic mechanisms and prey selection in free-living dinoflagellates. J. Eukaryot. Microbiol. 1999, 46:382-389.
96. Haque S.M., Onoue Y. Variation in toxin compositions of two harmful raphidophytes. Chattonella antiqua and Chattonella marina, at different salinities. Environ. Toxicol. 2002, 17:113-118.
97. Henrikson J.C., Gharfeh M.S., Easton A.C., Easton J.D., Glenn K.L., Shadfan M., Mooberry S.L., Hambright K.D., Cichewicz R.H. 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 2010, 55:1396-1404.
98. Hillebrand H., Dürselen C.-D., Kirschtel D., Pollingher U., Zohary T. Biovolume calculation for pelagic and benthic microalgae. J. Phycol. 1999, 35:403-424.
99. Hiroishi S., Okada H., Imai I., Yoshida T. High toxicity of the novel bloom-forming species Chattonella ovata (Raphidophyceae) to cultured fish. Harmful Algae 2005, 4:783-787.
100. Hold G.L., Smith E.A., Birkbeck T.H., Gallacher S. Comparison of paralytic shellfish toxin (PST) production by the dinoflagellates Alexandrium lusitanicum NEPCC 253 and Alexandrium tamarense NEPCC 407 in the presence and absence of bacteria. FEMS Microbiol. Ecol. 2001, 36:223-234.
101. Hoshaw R.W., Rosowski J.R. Methods for microscopic algae. Handbook of Phycological Methods 1973, 53-68. Cambridge University Press, London. J.R. Stein (Ed.).
102. Hudnell H.K. Chronic biotoxin-associated illness: multiple-system symptoms, a vision deficit, and effective treatment. Neurotoxicol. Teratol. 2005, 27:733-743.
103. Humphries E.M. Pfiesteria piscicida and Pfiesteria shumwayae - Associations With Environmental Parameters 2002, Delaware Department of Natural Resources and Environmental Control, Dover.
104. Igarashi T., Aritake S., Yasumoto T. Biological activities of prymnesin-2 isolated from a red tide alga Prymnesium parvum. Nat. Toxins 1998, 6:35-41.
105. Igarashi T., Satake M., Yasumoto T. Structures and partial stereochemical assignments for prymnesin-1 and prymnesin-2: potent hemolytic and ichthyotoxic glycosides isolated from the red tide alga Prymnesium parvum. J. Am. Chem. Soc. 1999, 121:8499-8511.
106. Inoue, A., 1978. Axenic culture, p. 2. In: Yasumoto, T. (Ed.), Studies on the Toxigenic Dinoflagellate Found as the Likely Cause of Ciguatera. Report to the South Pacific Commission, 4 p. Available at: http://www.spc.int/DigitalLibrary/Doc/FAME/Reports/Yasumoto_78_ToxigenicCiguatera.pdf.
107. International Panel on Climate Change (IPCC), 2007. Climate change 2007 - the synthesis report. Fourth Assessment Report (AR4) of the United Nations Intergovernmental Panel on Climate Change. IPCC. Available at: http://www.ipcc.ch/ipccreports/ar4-syr.htm.
108. Jakobsen H.H., Hansen P.J. Prey size selection, grazing and growth response of the small heterotrophic dinoflagellate Gymnodinium sp. and the ciliate Balanion comatum - a comparative study. Mar. Ecol. Prog. Ser. 1997, 158:75-86.
109. Jakobsen K.S., Tengs T., Vatne A., Bowers H.A., Oldach D.W., Burkholder J.M., Glasgow H.B., Rublee P.A., Klaveness D. Discovery of the toxic dinoflagellate, Pfiesteria, from northern European waters. Proc. R. Soc. Lond. (B) 2002, 269:211-214.
110. Jariv J. The toxin of Prymnesium parvum. Bull. Res. Council Israel 1955, 5A:96.
111. Jeong H.J., Ha J.H., Park J.H., Kim J.H., Kang N.S., Kim S., Kim J.S., Yoo Y.D., Yih W.H. Distribution of the heterotrophic dinoflagellate Pfiesteria piscicida in Korean waters and its feeding on mixotrophic dinoflagellates, raphidophytes, and fish blood cells. Aquat. Microbial. Ecol. 2006, 44:263-275.
112. Jeong H.J., Kim J.S., Song J.Y., Kim J.H., Kim T.H., Kim S.K., Kang N.S. Feeding by heterotrophic protists and copepods on the heterotrophic dinoflagellates Pfiesteria piscicida. Stoeckeria algicida, and Luciella masanensis. Mar. Ecol. Prog. Ser. 2007, 349:199-211.
113. Jeong H.J., Seong J., Park J.Y., Kim J.H., Kim S., Lee I., Lee S.H., Ha J.H., Yih W.H. Stoeckeria algicida n. gen., sn. sp. (Dinophyceae) from the coastal waters off southern Korea: morphology and small subunit ribosomal DNA gene sequence. J. Eukaryot. Microbiol. 2005, 52:382-390.
114. Jeong H.J., Yoo Y.D., Kim J.S., Seong K.A., Kang N.S., Kim T.H. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 2010, 45:65-91.
115. Johansson N., Granéli E. Influence of different nutrient conditions on cell density, chemical composition and toxicity of Prymnesium parvum (Haptophyta) in semi-continuous cultures. J. Exp. Mar. Biol. Ecol. 1999, 239:243-258.
116. John E.H., Flynn K.J. Growth dynamics and toxicity of Alexandrium fundyense (Dinophyceae): the effect of changing N:P supply ratios on internal toxin and nutrient levels. Eur. J. Phycol. 2000, 35:11-23.
117. John U., Beszteria B., Derell E., Van de Peer Y., Read B., Moreau H., Cembella A. Novel insights into evolution of protistan polyketide synthases through phylogenomic analysis. Protist 2008, 159:21-30.
118. Kamykowski D.M., Reed R.E., Kirkpatrick G.J. Comparison of sinking velocity, swimming, rotation and path characteristics among six marine dinoflagellate species. Mar. Biol. 1992, 113:319-328.
119. Keppler C.J., Hoguet J., Smith K., Ringwood A.H., Lewitus A.J. Sublethal effects of the toxic alga Heterosigma akashiwo on the southeastern oyster (Crassostrea virginica). Harmful Algae 2004, 4:275-285.
120. Khan S., Arakawa O., Onoue Y. A toxicological study of the marine phytoflagellate Chattonella antiqua (Raphidophyceae). Phycologia 1996, 35:239-244.
121. Kim D., Nakamura A., Okamoto T., Komatsu N., Oda T., Iida T., Ishimatsu A., Muramatsu T. Mechanism of superoxide anion generation in the toxic red tide phytoplankton Chattonella marina: possible involvement of NAD(P)H oxidase. Biochim. Biophys. Acta 2000, 1524:220-227.
122. Kotaki Y., Koike K., Sato S., Ogata T., Fukuyo Y., Kodama M. Confirmation of domoic acid production of Pseudo-nitzschia multiseries isolated from Ofunato Bay, Japan. Toxicon 1999, 37:677-682.
123. Kozakai H., Oshima Y., Yasumoto T. Isolation and structural elucidation of hemolysin from the phytoflagellate Prymnesium parvum. Agric. Biol. Chem. 1982, 46:233-236.
124. Kozelka P.B., Bruland K.W. Chemical speciation of dissolved Cu, Zn, Cd, Pb in Narragansett Bay, Rhode Island. Mar. Chem. 1998, 60:267-282.
125. Krantz G., Burkholder J.M., Glasgow H.B. Response of oysters to a culture of toxin-producing " phantom" dinoflagellates. Proceedings of the Annual Meeting of the National Shellfish Association 1994, 24.
126. Lannan C.N., Winton J.R., Fryer J.L. Fish cell lines: establishment and characterization of nine cell lines from salmonids. In Vitro 1984, 20:671-676.
127. Larsen A., Eikrem W., Paasche E. Growth and toxicity in Prymnesium patelliferum (Prymnesiophyceae) isolated from Norwegian waters. Can. J. Bot. 1993, 71:1357-1362.
128. Leatherland J.F., Ballantyne J.S., Van Der Kraak G. Diagnostic assessment of non-infectious disorders of captive and wild fish populations and the use of fish as sentinel organisms for environmental studies. Fish Diseases and Disorders, vol. 2. Non-infectious Disorders 1998, 335-366. CABI Publishing, Wallingford, UK. J.F. Leatherland, P.T.K. Woo (Eds.).
129. Lenz J. Introduction. Zooplankton Methodology Manual 2000, 1-32. International Council for Exploration of the Sea, Academic Press, San Diego, CA. R.P. Harris, P.H. Wiebe, J. Lenz, H.R. Skjoldal, M. Huntley (Eds.).
130. Lessard E.J., Swift E. Species-specific grazing rates of heterotrophic dinoflagellates in oceanic waters, measured with a dual-label radioisotope technique. Mar. Biol. 1985, 87:289-296.
131. Levin E.D. A rat model of the cognitive impairment from Pfiesteria piscicida exposure. Environ. Health. Perspect. 2001, 109:757-763.
132. Levin E.D., Blackwelder W.P., Glasgow H.B., Burkholder J.M., Moeller P.D.R., Ramsdell J.S. Learning impairment caused by Pfiesteria toxin infusion into the hippocampus of rats. Neurotox. Teratol. 2003, 25:419-426.
133. Levin E.D., Rezvani A.H., Christopher N.C., Glasgow H.B., Deamer-Melia N.J., Burkholder J.M., Moser V.C., Jensen K. Rapid neurobehavioral analysis of Pfiesteria piscicida effects in juvenile and adult rats. Neurotoxicol. Teratol. 2000, 22:533-540.
134. Levin E.D., Schmechel D.E., Burkholder J.M., Deamer-Melia N.J., Moser V.C., Harry G.J. Persisting learning deficits in rats after exposure to Pfiesteria piscicida. Environ. Health Perspect. 1997, 105:1320-1325.
135. Levin E.D., Simon B.B., Schmechel D.E., Glasgow H.B., Deamer-Melia N.J., Burkholder J.M., Moser V.C., Jensen K., Harry G.J. Pfiesteria toxin and learning performance. Neurotoxicol. Teratol. 1999, 21:215-221.
136. Levine J.F., Hawkins J.H., Dykstra M.J., Noga E.J., Moye D.W., Cone R.S. Epidemiology of ulcerative mycosis in Atlantic menhaden in the Tar-Pamlico river estuary, North Carolina. J. Aquat. An. Health 1990, 2:162-171.
137. Levy M.G., Litaker R.W., Goldstein R.J., Dykstra M.J., Vandersea M.W., Noga E.J. Piscinoodinium, a fish-ectoparasitic dinoflagellate, is a member of the class Dinophyceae, subclass Gymnodiniphycidae: convergent evolution with Amyloodinium. J. Parasitol. 2007, 93:1006-1015.
138. Lewitus A.J., Burkholder J.M., Glasgow H.B., Glibert P.M., Willis B.M., Hayes K.C., Burke M.K. Mixotrophy and nutrient uptake by Pfiesteria piscicida (Dinophyceae). J. Phycol. 1999, 35:1430-1437.
139. Lewitus A.J., Glasgow H.B., Burkholder J.M. Kleptoplastidy in the toxic dinoflagellate, Pfiesteria piscicida (Dinophyceae). J. Phycol. 1999, 35:303-312.
140. Lewitus A.J., Wetz M.S., Willis B.M., Burkholder J.M., Glasgow H.B. Grazing activity of Pfiesteria piscicida (Dinophyceae) and susceptibility to ciliate predation vary with toxicity status. Harmful Algae 2006, 5:427-434.
141. Li A.S., Stoecker D.K., Adolf J.E. Feeding, pigmentation, photosynthesis and growth of the mixotrophic dinoflagellate Gyrodinium galatheanum. Aquat. Microb. Ecol. 1999, 19:163-176.
142. Li-Chan E.C.Y., Powrie W.D., Nakai S. The chemistry of eggs and egg products. Egg Science and Technology 1995, 105-175. Haworth Press, Binghamton, New York, NY. W.J. Stadelman, O.J. Cotterill (Eds.).
143. Lin S., Mulholland M.R., Zhang H., Feinstein T.N., Jochem F.J., Carpenter E.J. Intense grazing and prey-dependent growth of Pfiesteria piscicida (Dinophyceae). J. Phycol. 2004, 40:1062-1073.
144. Lin S., Zhang H., Dubois A. Low abundance distribution of Pfiesteria piscicida in Pacific and western Atlantic as detected by mtDNA-18S rDNA real-time polymerase chain reaction. J. Plankt. Res. 2006, 28:667-681.
145. Lin S., Zhang H., Hou Y., Zhuang Y., Miranda L. High-level diversity of dinoflagellates in the natural environment, revealed by assessment of mitochondrial cox1 and cob genes for dinoflagellate DNA barcoding. Appl. Environ. Microbiol. 2009, 75:1279-1290.
146. Litaker R.W., Steidinger K.A., Mason P.L., Landsberg J.H., Shields J.D., Reece K.S., Haas L.W., Vogelbein W.K., Vandersea M.W., Kibler S.R., Tester P.A. The reclassification of Pfiesteria shumwayae (Dinophyceae): Pseudopfiesteria, gen. nov. J. Phycol. 2005, 41:643-651.
147. Litaker R.W., Tester P.A., Colorni A., Levy M.G., Noga E.J. The phylogenetic relationship of Pfiesteria piscicida, cryptoperidiniopsoid sp., Amyloodinium ocellatum and a pfiesteria-like dinoflagellate to other dinoflagellates and apicomplexans. J. Phycol. 1999, 35:1379-1389.
148. Litaker R.W., Vandersea M.W., Kibler S.R., Madden V.J., Noga E.J., Tester P.A. Life cycle of the heterotrophic dinoflagellate Pfiesteria piscicida (Dinophyceae). J. Phycol. 2002, 38:442-463.
149. Litaker R.W., Vandersea M.W., Kibler S.R., Reece K.S., Stokes N.A., Steidinger K.A., Millie D.F., Bendis B., Pigg R., Tester P.A. Variability among dinoflagellate ITS region sequences: identification of Pfiesteria piscicida (Dinophyceae) and Pfiesteria-like organisms using ITS-specific PCR assays. J. Phycol. 2003, 39:754-761.
150. Lom J., Lawler A.R. An ultrastructural study on the mode of attachment in dinoflagellates invading gills of Cyprinodontidae. Protistologica 1973, 9:293-309.
151. Lovko V.J., Vogelbein W.K., Shields J.D., Haas L.W., Reece K.S. A new larval fish bioassay for testing the pathogenicity of Pfiesteria spp. (Dinophyceae). J. Phycol. 2003, 39:600-609.
152. Lowitt M., Kauffman L. Pfiesteria and the skin. Maryland Med. J. 1998, 47:124-126.
153. Magnien, R.E., Goshorn, D., Michael, B., Tango, P., Karrh, R., 2000. Associations between Pfiesteria, fish health and environmental conditions in Maryland. Final Report. Tidewater Ecosystem Assessment, Maryland Department of Natural Resources, Annapolis, 37 p.
154. Maldonado M.T., Hughes M.P., Rue E.L., Wells M.L. The effect of Fe and Cu on growth and domoic acid production by Pseudo-nitzschia multiseries and Pseudo-nitzschia australis. Limnol. Oceanogr. 2002, 47:515-526.
155. Mallin M.A., Burkholder J.M., Larsen L.M., Glasgow H.B. Response of two zooplankton grazers to an ichthyotoxic estuarine dinoflagellate. J. Plankt. Res. 1995, 17:351-363.
156. Manning S.R., La Claire J.W. Prymnesins: toxic metabolites of the golden alga, Prymnesium parvum Carter (Haptophyta). Mar. Drugs 2010, 8:678-704.
157. Marahiel M.A., Stachelhaus T., Mootz H.D. Modular peptide synthetases involved in non-ribosomal peptide synthesis. Chem. Rev. 1997, 97:2651-2674.
158. Marshall H.G., Gordon A., Seaborn D., Dyer B., Dunstan W., Seaborn A. Comparative culture and toxicity studies between toxic dinoflagellate Pfiesteria piscicida and a morphologically similar cryptoperidiniopsoid dinoflagellate. J. Exp. Mar. Biol. Ecol. 2000, 255:51-74.
159. Marshall H.G., Hargraves P.E., Elbrächter M., Burkholder J.M., Parrow M.W., Allen E.H., Knowlton V.M., Rublee P.A., Hynes W.L., Egerton T.A., Remington D.L., Wyatt K.B., Coyne K.J., Lewitus A.J., Henrich V.C. Taxonomy of Pfiesteria (Dinophyceae). Harmful Algae 2006, 5:481-496.
160. Marshall J.A., de Salas M., Oda T., Hallegraeff G.M. Superoxide production by marine algae. 1. Survey of 37 species from 6 classes. Mar. Biol. 2005, 147:533-540.
161. Marshall J.A., Nichols P., Hamilton B., Lewis R., Hallegraeff G.M. Synergistic role of reactive oxygen species and free fatty acids. Harmful Algae 2003, 2:273-281.
162. Mason P.L., Litaker R.W., Jeong H.J., Ha J.H., Reece K.S., Stokes N.A., Park J.Y., Steidinger K.A., Vandersea M.W., Kibler S., Tester P.A., Vogelbein W.K. Description of a new genus of pfiesteria-like dinoflagellate. Luciella gen. nov. (Dinophyceae), including two new species: Luciella masanensis sp. nov. and Luciella atlantis sp. nov. J. Phycol. 2007, 43:799-810.
163. Mason P.L., Vogelbein W.K., Haas L.W., Shields J.D. An improved stripping technique for lightly armored dinoflagellates. J. Phycol. 2003, 39:253-258.
164. Matsuoka K. Cyst and thecate forms of Pyrophacus steinii (Schiller) Wall et Dale, 1971. Trans. Proc. Palaeontol. Soc. Jpn. NS 1985, 140:240-262.
165. McCulloch P., Odense P., Pocklington R., Quilliam M.A., Sim P.G., Smith J.C., Rao D.V.S., Todd E.C.D., Walter J.A., Wright J.L.C. Pennate diatom Nitzschia pungens as the primary source of domoic acid, a toxin in shellfish from eastern Prince Edward Island, Canada. Can. J. Fish. Aquat. Sci. 1989, 46:1203-1215.
166. McGinn, M.P., 1971. Axenic cultivation of Noctiluca scintillans. Ph.D. dissertation. Fordham University, New York, NY, 150 p.
167. Menden-Deuer S., Lessard E.J. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 2000, 45:569-579.
168. Menden-Deuer S., Lessard E.J., Satterberg J. Effect of preservation on dinoflagellate and diatom cell volume and consequences for carbon biomass predictions. Mar. Ecol. Prog. Ser. 2001, 222:41-50.
169. Mill T., Hendry D.G., Richardson H. Free-radical oxidants in natural waters. Science 1980, 207:886-887.
170. Moeller P.D.R., Beauchesne K.R., Huncik K.M., Davis W.C., Christopher S.J., Riggs-Gelasco P., Gelasco A. Metal complexes and free radical toxins produced by Pfiesteria piscicida. Environ. Sci. Technol. 2007, 41:1166-1172.
171. Moeller P.D.R., Morton S.L., Mitchell B.A., Sivertsen S.K., Fairey E.R., Mikulski T.M., Glasgow H.B., Deamer-Melia N.J., Burkholder J.M., Ramsdell J.S. Current progress in isolation and characterization of toxins isolated from Pfiesteria piscicida. Environ. Health Perspect. 2001, 109:739-743.
172. Moestrup Ø. Economic aspects: 'Blooms', nuisance species, and toxins. The Haptophyte Algae 1994, 265-285. Oxford University Press, New York. J.C. Green, B.S.C. Leadbeater (Eds.).
173. Montresor M., Marino D. New observation on the life cycle of Pyrophacus horologium Stein (Dinophyceae). Bol. Soc. Adriatica Sci. 1994, 75:261-268.
174. Moore M.V. Density-dependent predation of early instar Chaoborus feeding on multispecies prey assemblages. Limnol. Oceanogr. 1988, 33:256-268.
175. Morgan G. Silencing Scientists and Scholars in Other Fields: Power, Paradigm Controls, Peer Review, and Scholarly Communication 1998, Ablex Publishing Corporation, Greenwich, CT.
176. Morrill L.C., Loeblich A.R. A survey of body scales in dinoflagellates and a revision of Cachonina and Heterocapsa (Pyrrhophyta). J. Plankt. Res. 1981, 3:53-65.
177. Morris J.G., Grattan L.M., Wilson L.A., Meyer W.A., McCarter R., Bowers H.A., Hebel J.R., Matuszak D.L., Oldach D.W. Occupational exposure to Pfiesteria species in estuarine waters is not a risk factor for illness. Environ. Health Perspect. 2006, 14:1038-1043.
178. Morris P.O. Acute Symptoms Reported by Persons Exposed to Fish Kills Associated with Pfiesteria piscicida 1996, Occupational and Environmental Epidemiology Section, Division of Epidemiology, North Carolina State Department of the Environment, Health, and Natural Resources, Raleigh.
179. Murata M., Yasumoto T. The structure, elucidation, and biological activities of high molecular weight algal toxins: maxitotoxin, prymnesins, and zooxanthellatoxins. Nat. Prod. Rep. 2000, 17:293-314.
180. Nakamura A., Okamoto T., Komatsu N., Ooka S., Oda T., Ishimatsu A., Muramatsu T. Fish mucus stimulates the generation of superoxide anion by Chattonella marina and Heterosigma akashiwo. Fish. Sci. 1999, 64:866-869.
181. National Research Council (NRC) Drinking Water and Health, vol. 9 1977, Safe Drinking Water Committee, NRC. National Academy Press, Washington, DC.
182. Nigrelli R.F. The morphology, cytology and life-history of Oodinium ocellatum Brown, a dinoflagellate parasite on marine fishes. Zoologica 1936, 21:129-164.
183. Noga E.J. Propagation in cell culture of the dinoflagellate Amyloodinium, an ectoparasite of marine fishes. Science 1987, 236:1302-1304.
184. Noga E.J. Fungal diseases in marine and estuarine fishes. Pathobiology of Marine and Estuarine Organisms 1993, 85-100. CRC Press, Boca Raton. J.A. Couch, J.W. Fournie (Eds.).
185. Noga E.J. Skin ulcers in fish: Pfiesteria and other etiologies. Toxicol. Pathol. 2000, 28:807-823.
186. Noga E.J. Fish Disease - Diagnosis and Treatment 2000, Iowa State University Press, Ames.
187. Noga E.J., Khoo L., Stevens J.B., Fan Z., Burkholder J.M. Novel toxic dinoflagellate causes epidemic disease in estuarine fish. Mar. Pollut. Bull. 1996, 32:219-224.
188. Nygaard K., Tobisen A. Bacterivory in algae: a survival strategy during nutrient limitation. Limnol. Oceanogr. 1993, 38:273-279.
189. Oestmann D.J., Lewis D.H. Improved cell culture propagation of Amyloodinium ocellatum. Dis. Aquat. Org. 1996, 24:173-178.
190. Oldach D.W., Delwiche C., Jakobsen K.S., Tengs T., Brown E.G., Kempton J.W., Schaefer E.F., Bowers H., Glasgow H.B., Burkholder J.M., Steidinger K.A., Rublee P.A. Heteroduplex mobility assay guided sequence discovery: elucidation of the small subunit (18S) rDNA sequence of Pfiesteria piscicida and related dinoflagellates from complex algal culture and environmental sample DNA pools. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:4303-4308.
191. Park T.-G., Bell E.M., Pearce I., Rublee P.A., Bolch C.J.S., Hallegraeff G.M. Detection of a novel ecotype of Pfiesteria piscicida (Dinophyceae) in an Antarctic saline lake by real-time PCR. Polar Biol. 2007, 30:843-848. 10.1007/s00300-006-0244-0.
192. Parnas I., Reich K., Bergmann F. Photoinactivation of cultures of Prymnesium parvum Carter. Appl. Microbiol. 1962, 10:237-239.
193. Parrow M.W., Burkholder J.M. Flow cytometric determination of zoospore DNA content and population DNA distribution in cultured Pfiesteria spp. (Pyrrhophyta). J. Exp. Mar. Biol. Ecol. 2002, 267:35-51.
194. Parrow M.W., Burkholder J.M. Erratum to " Flow cytometric determination of zoospore DNA content and population DNA distribution in cultured Pfiesteria spp. (Pyrrhophyta)" [Journal of Experimental Marine Biology and Ecology 267 (2002) 35-51" J. Exp. Mar. Biol. Ecol. 2002, 268:1. (First sentence: " The Publisher regrets that, although the authors were guaranteed that their paper would be published in 2001, the publisher failed to do so and the paper was published in January 2002" ).
195. Parrow M.W., Burkholder J.M. Reproduction and sexuality in Pfiesteria shumwayae (Dinophyceae). J. Phycol. 2003, 39:697-711.
196. Parrow M.W., Burkholder J.M. The sexual life cycles of Pfiesteria piscicida and cryptoperidiniopsoids (Dinophyceae). J. Phycol. 2004, 40:664-673.
197. Parrow M.W., Burkholder J.M., Deamer N.J., Ramsdell J.S. Contaminant-free cultivation of Pfiesteria shumwayae (Dinophyceae) on a fish cell line. Aquat. Microb. Ecol. 2005, 39:97-105.
198. Parrow M.W., Burkholder J.M., Deamer N.J., Zhang C. Vegetative and sexual reproduction in Pfiesteria spp. (Dinophyceae) cultured with algal prey, and inferences for their classification. Harmful Algae 2002, 1:5-33.
199. Parrow M.W., Glasgow H.B., Burkholder J.M., Zhang C. Comparative response to algal prey by Pfiesteria piscicida, Pfiesteria shumwayae sp. nov., and a co-occurring 'lookalike' species. Harmful Algal Blooms 2000 2001, 101-104. IOC of UNESCO, Paris. G.M. Hallegraeff, S.I. Blackburn, C.J. Bolch, R.J. Lewis (Eds.).
200. Pastorok R.A. Prey vulnerability and size selection by Chaoborus larvae. Ecology 1981, 62:1311-1324.
201. Patterson D.J. The diversity of eukaryotes. Am. Nat. 1999, 154:S96-S124.
202. Peglar M.T., Nerad T.A., Anderson O.R., Gillevet P.M. Identification of amoebae implicated in the life cycle of Pfiesteria and Pfiesteria-like dinoflagellates. J. Eukaryot. Microbiol. 2004, 51:42-552.
203. Perez R., Liu L., Lopez J., An T., Rein K.S. Diverse bacterial PKS sequences derived from okadaic acid-producing dinoflagellates. Mar. Drugs 2008, 6:164-179.
204. Pfiesteria Glossary of Pfiesteria-related terms 2001, U.S. Environmental Protection Agency, Baltimore, MD, 9 pp.
205. Place A.R., Saito K., Deeds J.R., Robledo J.A.F., Vasta G.R. A decade of research on Pfiesteria spp. and their toxins: unresolved questions and an alternative hypothesis. Seafood and Freshwater Toxins 2008, 717-751. CRC Press, New York. L.M. Botana (Ed.).
206. Plumley F.G. Marine algal toxins: biochemistry, genetics, and molecular biology. Limnol. Oceanogr. 1997, 42:252-264.
207. Point D., Bareille G., Pinaly H., Belin C., Donard O.F.X. Multielemental speciation of trace elements in estuarine waters with automated on-site UV photolysis and resin chelation coupled to inductively coupled plasma mass spectrometry. Talanta 2007, 72:1207-1216.
208. Porter K.G. Phagotrophic phytoflagellates in microbial food webs. Hydrobiologia 1988, 159:89-97.
209. Prince E.K., Lettieri L., McCurdy K.J., Kubanek J. Fitness consequences for copepods feeding on a red tide dinoflagellate: deciphering the effects of nutritional value, toxicity, and feeding behavior. Oecologia 2006, 147:479-488.
210. Quesenberry M., Saito K., Krupatkina D.N., Robledo J.A.F., Drgon T., Pecher W.T., O'Leary N., Alavi M., Miller T., Schneider R., Belas R., Deeds J., Place A., Zohar Y., Vasta G.R. Bioassay for ichthyocidal activity of Pfiesteria piscicida: characterization of a culture flask assay format. J. Appl. Phycol. 2002, 14:241-245.
211. Ray S.M., Wilson W.B. Effects of unialgal and bacteria-free cultures of Gymnodinium breve on fish. Fishery Bulletin 123. Fish. Bull. U.S. Fish Wildl. Serv. 1957, 57:469.
212. Reich K., Parnas I. Effect of illumination on ichthyotoxin in an axenic culture of Prymnesium parvum Carter. J. Protozool. 1962, 9:38-40.
213. Reich K., Rotberg M. Some factors influencing the formation of toxin poisonous to fish in bacteria free cultures of Prymnesium. Bull. Res. Counc. Israel 1958, 7B:199-202.
214. Rhodes L.L., Adamson J.E., Rublee P.A., Schaefer E.F. Geographic distribution of Pfiesteria spp. (Pfiesteriaceae) in Tasman Bay and Centerbury, New Zealand. N.Z. J. Mar. Freshwat. Res. 2006, 40:211-220.
215. Rhodes L.L., Burkholder J.M., Glasgow H.B., Rublee P.A., Allen C., Adamson J.E. Pfiesteria shumwayae (Pfiesteriaceae) in New Zealand. N.Z. J. Mar. Freshwat. Res. 2002, 36:621-630.
216. Roman M., Reaugh M., Zhang X. Ingestion of the dinoflagellate, Pfiesteria piscicida, by the calanoid copepod, Acartia tonsa. Harmful Algae 2006, 5:435-441.
217. Roth P.B., Mikulski C.M., Doucette G.J. Influence of microbial interactions on the susceptibility of Karenia spp. to algicidal bacteria. Aquat. Microb. Ecol. 2008, 50:251-259.
218. Rublee P.A., Allen C., Schaefer E., Rhodes L., Adamson J., Lapworth C., Burkholder J., Glasgow H.B. Global distribution of toxic Pfiesteria complex species detected by PCR assay. Harmful Algae 2002 2004, 320-322. Fl. Fish and Wildlife Cons. Commun. FL Inst. Oceanogr., Inter-governmental Oceanographic Commission of UNESCO, St. Petersburg, FL. K.A. Steidinger, J.H. Landsberg, C.R. Tomas, G.A. Vargo (Eds.).
219. Rublee P.A., Kempton J., Schaefer E., Allen C., Harris J., Oldach D.W., Bowers H., Tengs T., Burkholder J., Glasgow H.B. Use of molecular probes to assess geographic distribution of Pfiesteria species. Environ. Health Perspect. 2001, 109:765-767.
220. Rublee P.A., Kempton J., Schaefer E., Burkholder J., Glasgow H.B., Oldach D. PCR and FISH detection extends the range of Pfiesteria piscicida in estuarine waters. V. J. Sci. 1999, 50:325-336.
221. Rublee P.A., Nuzzi R., Waters R., Burkholder J.M. Pfiesteria piscicida and Pfiesteria shumwayae in coastal waters of Long Island, New York, U.S.A. Harmful Algae 2006, 5:374-379.
222. Rublee P.A., Remington D., Schaefer E., Marshall M.M. Detection of the dinozoans Pfiesteria piscicida and P. shumwayae: a review of detection methods and geographic distribution. J. Eukaryot. Microbiol. 2005, 52:83-89.
223. Saito K., Drgon T., Krupatkina D.N., Drgonova J., Terlizzi D.E., Mercer N., Vasta G.R. Effect of biotic and abiotic factors on in vitro proliferation, encystment, and excystment of Pfiesteria piscicida. Appl. Environ. Microbiol. 2007, 73:6410-6420.
224. Samet J., Bignami G.S., Feldman R., Hawkins W., Neff J., Smayda T. Pfiesteria: Review of the science and identification of research gaps. Report for the National Center for Environmental Health, Centers for Disease Control and Prevention. Environ. Health Perspect. 2001, 109:639-659.
225. Santschi P.H., Lenhart J.J., Honeyman B.D. Heterogeneous processes affecting trace contaminant distribution in estuaries: the role of natural organic matter. Mar. Chem. 1997, 58:99-125.
226. Sanvik S.L.H., Bilski P., Pakulski J.D., Chignell C.F., Coffin R.B. Photogeneration of singlet oxygen and free radicals in dissolved organic matter isolated from the Mississippi and Atchafalaya River plumes. Mar. Chem. 2000, 69:139-152.
227. Sasaki M., Takeda N., Fuwa H., Watanabe R., Satake M., Oshima Y. Synthesis of the JK/LM-ring model of prymnesins, potent hemolytic and ichthyotoxic polycyclic ethers isolated from the red tide alga Prymnesium parvum: confirmation of the relative configuration of the K/L-ring juncture. Tetrahedron Lett. 2006, 47:5687-5691.
228. Schmechel D.E., Koltai D. Potential human health effects associated with laboratory exposure to Pfiesteria piscicida. Environ. Health Perspect. 2001, 109:775-780.
229. Schnepf E., Deichgräber G. " Myzocytosis," a kind of endocytosis with implications to compartmentalization in endosymbiosis: observations in Paulsenella (Dinophyta). Naturwissenschaften 1984, 71:218-219.
230. Schnepf E., Elbrächter M. Nutritional strategies in dinoflagellates - a review with emphasis on cell biological aspects. Eur. J. Protistol. 1992, 28:3-24.
231. Seaborn D.W., Tengs T., Cerbin S., Kokocinski M., Marshall H.G. A group of dinoflagellates similar to Pfiesteria as defined by morphology and genetic analysis. Harmful Algae 2006, 5:1-8.
232. Seong K.A., Jeong H.J., Kim S., Kim G.H., Kang J.H. Bacterivory by co-occurring red-tide algae, heterotrophic nanoflagellates, and ciliates. Mar. Ecol. Prog. Ser. 2006, 322:85-97.
233. Sheng J., Malkiel E., Katz J., Adolf J., Belas R., Place A.R. Digital holographic microscopy reveals prey-induced changes in swimming behavior of predatory dinoflagellates. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:17512-17517.
234. Shilo M. Formation and mode of action of algal toxins. Bacteriol. Rev. 1967, 31:180-193.
235. Shilo M. The toxic principles of Prymnesium parvum. The Water Environment: Algal Toxins and Health 1981, 37-47. Plenum Press, New York. W.W. Carmichael (Ed.).
236. Shilo M., Aschner M. Factors governing the toxicity of cultures containing phytoflagellate Prymnesium parvum Carter. J. Gen. Microbiol. 1953, 8:333-343.
237. Shimizu Y. Microalgal metabolites. Curr. Opin. Microbiol. 2003, 6:236-243.
238. Shumway S.E., Burkholder J.M., Springer J. Effects of the estuarine dinoflagellate Pfiesteria shumwayae (Dinophyceae) on survival and grazing activity of several shellfish species. Harmful Algae 2006, 5:442-458.
239. Simonsen S., Moestrup Ø. Toxicity tests in eight species of Chrysochromulina (Haptophyta). Can. J. Bot. 1997, 75:129-136.
240. Prymnesium parvum Workshop Report for 2003 2003, Texas Parks and Wildlife Department, Austin. L. Singhurst, D. Sager (Eds.).
241. Skelton H.M., Burkholder J.M., Parrow M.W. Axenic cultivation of the heterotrophic dinoflagellate Pfiesteria shumwayae and observations of feeding behavior. J. Phycol. 2008, 44:1614-1624.
242. Skelton H.M., Burkholder J.M., Parrow M.W. Axenic cultivation of the heterotrophic dinoflagellate Pfiesteria shumwayae in a semi-defined medium. J. Eukaryot. Microbiol. 2009, 56:73-82.
243. Skovogaard A., Hansen P.J. Food uptake in the harmful alga Prymnesium parvum mediated by excreted toxins. Limnol. Oceanogr. 2003, 48:1161-1166.
244. Skulberg O.M., Aune T., Underdahl B. The phytoflagellate Prymnesium parvum: account of toxicological knowledge. Vatten 1993, 49:155-160.
245. Small H.J., Shields J.D., Haas L.W., Vogelbein W.K., Moss J., Reece K.S. Genetic variation among strains of Pseudopfiesteria shumwayae and Pfiesteria piscicida (Dinophyceae). J. Phycol. 2009, 45:1315-1322.
246. Smayda T.J. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr. 1997, 42:1137-1153.
247. Smith C.G., Music S.I. Pfiesteria in North Carolina: the medical inquiry continues. N.C. Med. J. 1998, 59:216-220.
248. Smith S.A., Noga E.J., Bullis R.A. Mortality in Tilapia aurea due to a toxic dinoflagellate bloom. Proceedings of the Third International Colloquium of Pathology in Marine Aquaculture 1988, 167-168.
249. Spero H.J., Morée M.D. Phagotrophic feeding and its importance to the life cycle of the holozoic dinoflagellate, Gymnodinium fungiforme. J. Phycol. 1981, 17:43-51.
250. Spiegelstein M.Y., Paster Z., Assort B.C. Purification and biological activity of Gymnodinium breve toxins. Toxicon 1973, 11:85-93.
251. Spitze K. Functional response of an ambush predator: Chaoborus americanus predation on Daphnia pulexi. Ecology 1985, 66:938-949.
252. Springer, J.J., 2000. Interactions between two commercially important species of bivalve molluscs and the toxic estuarine dinoflagellate, Pfiesteria piscicida. M.S. thesis. Department of Marine, Earth and Atmospheric Sciences, North Carolina State University, Raleigh.
253. Springer J., Shumway S.E., Burkholder J.M., Glasgow H.B. Interactions between the toxic estuarine dinoflagellate. Pfiesteria piscicida and two species of bivalve molluscs. Mar. Ecol. Prog. Ser. 2002, 245:1-10.
254. Steidinger K.A., Burkholder J.M., Glasgow H.B., Hobbs C.W., Truby E., Garrett J., Noga E.J., Smith S.A. Pfiesteria piscicida gen. et sp. nov. (Pfiesteriaceae, fam. nov.), a new toxic dinoflagellate with a complex life cycle and behavior. J. Phycol. 1996, 32:157-164.
255. Steidinger K.A., Landsberg J.H., Matson P.L., Vogelbein W.K., Tester P.A., Litaker R.W. Cryptoperidiniopsis brodyi gen. et sp. nov. (Dinophyceae), a small lightly armored dinoflagellate in the Pfiesteriaceae. J. Phycol. 2006, 42:951-961.
256. Steidinger K.A., Tangen K. Dinoflagellates. Identifying Marine Diatoms and Dinoflagellates 1997, 387-584. Academic Press, Inc., New York. C.R. Tomas (Ed.).
257. Stoecker D.K., Gustafson D.E. Predicting grazing mortality of an estuarine dinoflagellate, Pfiesteria piscicida. Mar. Ecol. Prog. Ser. 2002, 233:33-40.
258. Stoecker D.K., Long A., Suttles S.E., Sanford L.P. Effect of small-scale shear on grazing and growth of the dinoflagellate Pfiesteria piscicida. Harmful Algae 2006, 5:407-418.
259. Stoecker D.K., Stevens K., Gustafson D.E. Grazing on Pfiesteria piscicida by microzooplankton. Aquat. Microb. Ecol. 2000, 22:261-270.
260. Stoecker D.J., Parrow M.W., Burkholder J.M., Glasgow H.B. Grazing by microzooplankton on Pfiesteria piscicida cultures with different histories of toxicity. Aquat. Microb. Ecol. 2002, 28:79-85.
261. Snyder R.V., Guerrero M.A., Sinigalliano C.D., Winshell J., Perez R., Lopez J.V., Rein K.S. Localization of polyketide synthase encoding genes to the toxic dinoflagellate Karenia brevis. Phytochemistry 2005, 66:1767-1780.
262. Su J.Q., Yang X.R., Zheng T.L., Hong H.S. An efficient method to obtain axenic cultures of Alexandrium tamarense - a PSP-producing dinoflagellate. J. Microbiol. Methods 2007, 69:425-430.
263. Sullivan B.E., Andersen R.A. Salinity tolerance of 62 strains of Pfiesteria and Pfiesteria-like heterotrophic flagellates (Dinophyceae). Phycol. Res. 2001, 49:207-214.
264. Swinker M., Koltai D., Wilkins J., Hudnell K., Hall E., Darcey D., Robertson K., Schmechel D., Stopford W., Music S. Estuary associated syndrome in North Carolina: an occupational prevalence study. Environ. Health Perspect. 2001, 109:21-26.
265. Swinker M., Koltai D., Wilkins J., Stopford W. Is there an estuary associated syndrome in North Carolina?. N.C. Med. J. 2001, 62:126-132.
266. Tango P., Magnien R., Goshorn D., Bowers H., Michael B., Karrh R., Oldach D. Associations between fish health and Pfiesteria spp. in Chesapeake Bay and mid-Atlantic estuaries. Harmful Algae 2006, 5:352-362.
267. Tengs T., Bowers H.A., Glasgow H.B., Burkholder J.M., Oldach D.W. Identical ribosomal DNA sequence data from Pfiesteria piscicida (Dinophyceae) isolates with different toxicity phenotypes. Environ. Res. 2003, 93:88-91.
268. Tomas C.R., Bourdelais A., Tomas L.E., Tatters A.O. Growth, nutrient utilization and evidence for toxin production by the new toxic flagellate Chloromorum toxicum. Proceedings of the 3rd Symposium on Harmful Algae in the U.S. Asilomar Conference Grounds near Monterey 2005, 63.
269. Turley C.M. Direct estimates of bacterial numbers in seawater samples without incurring cell loss due to sample storage. Handbook of Methods in Aquatic Microbial Ecology 1993, 143-147. CRC Press, Boca Raton, FL. P.F. Kemp, B.F. Sherr, E.B. Sherr, J.J. Cole (Eds.).
270. Twiner M.J., Chidiac P., Dixon S.J., Trick C.G. Extracellular organic compounds from the ichthyotoxic red tide alga (Heterosigma akashiwo) elevate cytosolic calcium and induce apoptosis in Sf9 cells. Harmful Algae 2005, 4:789-800.
271. Twiner M.J., Dechraoui M.-Y.B., Wang Z., Mikulski C.M., Henry M.S., Pierce R.H., Doucette G.J. Extraction and analysis of lipophilic brevetoxins from the red tide dinoflagellate Karenia brevis. Anal. Biochem. 2007, 369:128-135.
272. Ulitzur S., Shilo M. A sensitive assay system for determination of the ichthyotoxicity of Prymnesium parvum. J. Gen. Microbiol. 1964, 36:161-169.
273. Uribe P., Espejo R.T. Effect of associated bacteria on the growth and toxicity of Alexandrium catenella. Appl. Environ. Microbiol. 2003, 69:659-662.
274. Valenti T.W., James S.V., Lahousse M.J., Schug K.A., Roelke D.L., Grover J.P., Brooks B.W. A mechanistic explanation for pH-dependent ambient aquatic toxicity of Prymnesium parvum Carter. Toxicon 2010, 55:990-998.
275. Vandersea M.W., Litaker R.W., Yonish B., Sosa E., Landsberg J.H., Pullinger C., Moon-Butzin P., Green J., Morris J.A., Kator H., Noga E.J., Tester P.A. Molecular assays for detecting Aphanomyces invadans in ulcerative mycotic fish lesions. Appl. Environ. Microbiol. 2006, 72:1551-1557.
276. Villareal T., Simons J.D., Rublee P.A. Pfiesteria distribution along the Texas (USA) coast. Harmful Algae 2002 2004, 371-373. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography and Intergovernmental Oceanographic Commission of UNESCO, St. Petersburg, FL. K.A. Steidinger, J.L. Landsberg, C.R. Tomas, G.A. Vargo (Eds.).
277. Vogelbein W.K., Shields J.D., Haas L.W., Reece K.S., Zwerner D.E. Skin ulcers in estuarine fishes: a comparative pathological evaluation of wild and laboratory-exposed fish. Environ. Health Perspect. 2001, 109:687-693.
278. Vogelbein W.K., Lovko V.J., Reece K.S. Pfiesteria. Oceans and Human Health - Risks and Remedies from the Seas 2008, 297-325. Academic Press, New York. P.J. Walsh, S.L. Smith, L.E. Fleming, H.M. Solo-Gabriele, W.H. Gerwick (Eds.).
279. Vogelbein W.K., Lovko V.J., Shields J.D., Reece K.S., Mason P.L., Haas L.W., Walker C.C. Pfiesteria shumwayae kills fish by micropredation not exotoxin secretion. Nature 2002, 418:967-970.
280. A Manual on Methods for Measuring Primary Production in Aquatic Environments, International Biological Programs Handbook 12 1974, Blackwell, Oxford, UK. 2nd ed. R.A. Vollenweider (Ed.).
281. Wells M.L., Kozelka P.B., Bruland W. The complexation of dissolved Cu, Zn, Cd and Pb by soluble and colloidal organic matter in Narragansett Bay, RI. Mar. Chem. 1998, 62:203-217.
282. Zafiriou O.C., True M.B., Hayon E. Consequences of OH radical reaction in seawater. Formation and decay of Br22 ion radical. Photochemistry of Environmental Aquatic Systems. American Chemical Society (ACS) Symposium Series 327 1987, ACS Publications, Washington, DC. R.G. Zika, W.J. Cooper (Eds.).
283. Zhang H., Bhattacharya D., Lin S. Phylogeny of dinoflagellates based on mitochondrial cytochrome b and nuclear small subunit rDNA sequence comparisons. J. Phycol. 2005, 41:411-420.
284. Zhang H., Bhattacharya D., Maranda L., Lin S. Mitochondrial cob and cox1 genes and editing of the corresponding mRNAs in Dinophysis acuminata from Narragansett Bay, with special reference to the phylogenetic position of the genus Dinophysis. Appl. Environ. Microbiol. 2008, 74:1546-1554.
285. Zhang H., Lin S. Development of a cob-18S rDNA real-time PCR assay for quantifying Pfiesteria shumwayae in the natural environment. Appl. Environ. Microbiol. 2005, 71:7053-7063.
286. Zhang H., Litaker W., Vandersea M.W., Tester P., Lin S. Geographic distribution of Karlodinium veneficum in the U.S. east coast as detected by ITS-ferredoxin real-time PCR assay. J. Plankt. Res. 2008, 30:905-922.