A decade of research on pfiesteria spp. and their toxins: Unresolved questions and an alternative hypothesis

Seafood and Freshwater Toxins: Pharmacology, Physiology, and Detection, Second Edition

Volumn , Issue , 2008, Pages 717-751

  Place, A R ^a   Saito, K ^a   Deeds, J R ^b   Robledo, J A F ^a   Vasta, G R ^a  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85009436486     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (175)

1. Harvell, C.D. et al., Emerging marine diseases—climate links and anthropogenic factors, Science 285, 1505, 1999.
2. Grattan, L.M. et al., Learning and memory difficulties after environmental exposure to waterways containing toxin-producing Pfiesteria or Pfiesteria-like dinoflagellates, Lancet 352, 532, 1998.
3. Bever, C.T., Jr. et al., Neurologic symptoms following Pfiesteria exposure: case report and literature review, MdMed. J. 47, 120, 1998.
4. Burkholder, J.M. et al., New ‘phantom’ dinoflagellate is the causative agent of major estuarine fish kills, Nature 358, 407, 1992.
5. Burkholder, J.M. and Glasgow, H.B., Interactions of a toxic estuarine dinoflagellate with microbial predators and prey, Archiv. Protistenk. 145, 177, 1995.
6. Steidinger, K.A. et al., Pfiesteria piscicida gen. et spp. nov. (Pfiesteriaceae fam. nov.), a new toxic dinoflagellate with a complex life cycle and behavior, J. Phycol. 32, 157, 1996.
7. Lewitus, A.J. et al., Discovery of the “phantom” dinoflagellate in Chesapeake Bay, Estuaries 18, 373, 1995.
8. Deeds, J.R. et al., Treatment options for the control of an ichthyotoxic dinoflagellate in an estuarine aquaculture facility: a case study, Proceedings of the Second International Conference on Harmful Algae Management and Mitigation, 177, 2002.
9. Daugbjerg, N. et al., Phylogeny of some of the major genera of dinoflagellates based on ultra-structure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates, Phycologia 39, 302, 2000.
10. Kane, A.S. et al., Fish lesions in the Chesapeake Bay: Pfiesteria-like dinoflagellates and other etiologies, Md Med. J. 47, 106, 1998.
11. Matuszak, D.L. et al., Toxic-Pfiesteria—surveillance for human disease in Maryland, Md Med. J. 47, 144, 1998.
12. Levin, E.D. et al., Pfiesteria toxin and learning performance, Neurotoxicol. Teratol. 21, 215, 1999.
13. Levin, E.D. et al., Rapid neurobehavioral analysis of Pfiesteria piscicida effects in juvenile and adult rats, Neurotoxicol. Teratol. 22, 533, 2000.
14. Haselow, D.T. et al., Gastrointestinal and respiratory tract symptoms following brief environmental exposure to aerosols during apfiesteria-related fish kill, J. Toxicol. Environ. Health A 63, 553, 2001.
15. Burkholder, J.M. et al., Fish kills linked to a toxic ambush-predator dinoflagellate: distribution and environmental conditions., Mar. Ecol. Prog. Ser. 124, 43, 1995.
16. Glasgow, H.B., Jr. et al., Insidious effects of a toxic estuarine dinoflagellate on fish survival and human health, J. Toxicol. Environ. Health. 46, 501, 1995.
17. Burkholder, J.M. and Glasgow, H.B., Pfiesteria piscicida and other Pfiesteria-like dinoflagellates: behavior, impacts, and environmental controls, Limnol. Oceanogr. 42, 1052, 1997.
18. Berry, J.P. et al., Are Pfiesteria species toxicogenic? Evidence against production of ichthyotoxins by Pfiesteria shumwayae, Proc. Natl. Acad. Sci. USA 99, 10970, 2002.
19. Litaker, R.W. et al., Life cycle of the heterotrophic dinoflagellate Pfiesteria piscicida (Dinophyceae). J. Phycol. 38, 442, 2002.
20. Vogelbein, W.K. et al., Pfiesteria shumwayae kills fish by micropredation not exotoxin secretion, Nature 418, 967, 2002.
21. Peglar, M.T. et al., Identification of amoebae implicated in the life cycle of Pfiesteria and Pfiesteria-like dinoflagellates, J. Eukaryot. Microbiol. 51, 542, 2004.
22. Marshall, H.G. et al., Comparative culture and toxicity studies between the toxic dinoflagellate Pfiesteria piscicida and a morphologically similar cryptoperidiniopsoid dinoflagellate, J. Exp. Mar. Biol. Ecol. 255, 51, 2000.
23. Burkholder, J.M. et al., Species of the toxic Pfiesteria complex, and the importance of functional type in data interpretation, Environ. Health Perspect. 109 (Suppl 5), 667, 2001.
24. Burkholder, J.M. et al., Overview and present status of the toxic Pfiesteria complex (Dinophyceae), Phycologia 40, 186, 2001.
25. Moeller, P.D.R. et al., Metal complexes and free radical toxins produced by Pfiesteria piscicida, Environ. Sci. Technol. 2007.
26. Morris, J.G., Jr. et al., Occupational exposure to Pfiesteria species in estuarine waters is not a risk factor for illness, Environ. Health Perspect. 114, 1038, 2006.
27. Grattan, L.M., Current status and future directions for the investigation and management of the human health effects of exposure to Pfiesteria piscicida or Pfiesteria-like dinoflagellates, Md Med. J. 47, 148, 1998.
28. Shoemaker, R.C. and Hudnell, H.K., Possible estuary-associated syndrome: symptoms, vision, and treatment, Environ. Health Perspect. 109, 539, 2001.
29. Wyatt, T. and Jenkinson, I.R., Notes on Alexandrium population dynamics, J. Plankton Res. 19, 551, 1997.
30. Garces, E. et al., A recurrent and localized dinoflagellate bloom in a Mediterranean beach, J. Plankton Res. 21, 2373, 1999.
31. Godhe, A. et al., Polymerase chain reaction in detection of Gymnodinium mikimotoi and Alexandrium minutum in field samples from southwest India, Mar. Biotechnol. (NY) 3, 152, 2001.
32. Vogelbein, W.K. et al., Skin ulcers in estuarine fishes: a comparative pathological evaluation of wild and laboratory-exposed fish, Environ. Health Perspect. 109 (Suppl 5), 687, 2001.
33. Dodge, J.D., Some uses for scanning electron microscopy in dinoflagellate taxonomy, Br. Phycol. J. 12, 118, 1977.
34. Dodge, J.D. et al., Fine structure of the red-bloom dinoflagellate Glenodinium sanguineum, from Lake Tovel (N. Italy), Arch. Hydrobiol. 78, 125, 1987.
35. Gardiner, W.E. and Dawes, C.J., Ultrastructural observation on the small unarmoured dinoflagellate Cyrodinium estuariale Hulburt, J. Phycol. 1983.
36. Taylor, F.J.R., Scanning electron microscopy of thecae of the dinoflagellate genus Ornithocercus, J. Phycol. 7, 249, 1971.
37. Taylor, F.J.R. and Fukuyo, Y. Morphological features of the motile cell of Pyrodinium bahamense, in WorldFish Center conference proceedings, Hallegraeff, G.M. and Maclean, J.L. WorldFish Center, Bandar Seri Begawan (Brunei Darussalam), May 23-30, 1989.
38. Steidinger, K. et al., Classification and identification of Pfiesteria and Pfiesteria-like species, Environ. Health Perspect. 109 (Suppl 5), 661, 2001.
39. Porter, C.H. and Collins, F.H., Species-diagnostic differences in a ribosomal DNA internal transcribed spacer from the sibling species Anopheles freeborni and Anopheles hermsi (Diptera: Culicidae), Am. J. Trop. Med. Heg. 45, 271, 1991.
40. Field, K.G. et al., 18S rRNA sequences of Leishmania enriettii promastigote and amastigote, Int. J. Parasitol. 21, 483, 1991.
41. Cai, J. et al., PCR cloning and nucleotide sequence determination of the 18S rRNA genes and internal transcribed spacer 1 of the protozoan parasites Cryptosporidium parvum and Cryptosporidium muris, Biochim. Biophys. Acta 1131, 317, 1992.
42. Liu, Y. et al., Sequence and variability of the 5.8S and 26S rRNA genes of Pneumocystis carinii, Nucleic Acids Res. 20, 3763, 1992.
43. Olsen, G.J. and Woese, C.R., Ribosomal RNA: a key to phylogeny, FASEB J. 7, 113, 1993.
44. Campbell, B.C. et al., Evolutionary origin of whiteflies (Hemiptera: Sternorrhyncha: Aleyrodidae) inferred from 18S rDNA sequences, Insect. Mol. Biol. 3, 73, 1994.
45. Joffe, B.I. et al., Ordered arrangement and rearrangement of chromosomes during spermatogenesis in two species of planarians (Plathelminthes), Chromosoma 107, 173, 1998.
46. Mugridge, N.B. et al., Phylogenetic relationships of the genus Frenkelia: a review of its history and new knowledge gained from comparison of large subunit ribosomal ribonucleic acid gene sequences, Int. J. Parasitol. 29, 957, 1999.
47. On, S.L.W., Taxonomy of Campylobacter, Arcobacter, Helicobacter and related bacteria: current status, future prospects and immediate concerns, J. Appl. Microbiol. 90, 1S, 2001.
48. Glasgow, H.B. et al., A second species of ichthyotoxic Pfiesteria (Dinamoebales, Dinophyceae). Phycologia 40, 234, 2001.
49. Zardoya, R. et al., Revised dinoflagellate phylogeny inferred from molecular analysis of large-subunit ribosomal RNA gene sequences, J. Mol. Biol. 41, 637, 1995.
50. Litaker, R.W. et al., The Reclassification of Pfiesteria shumwayae (Dinophyceae): Pseudopfiesteria, gen. nov., J. Phycol. 41, 643, 2005.
51. Litaker, R.W. et al., The phylogenetic relationship of Pfiesteria piscicida, cryptoperidiniopsoid spp., Amyloodinium ocellatum and a pfiesteria-like dinoflagellate to other dinoflagellates and apicomplex-ans, J. Phycol. 35, 1379, 1999.
52. Oldach, D.W. et al., Heteroduplex mobility assay-guided sequence discovery: elucidation of the small subunit (18S) rDNA sequences of Pfiesteria piscicida and related dinoflagellates from complex algal culture and environmental sample DNA pools, Proc. Natl. Acad. Sci. USA 97, 4303, 2000.
53. Jakobsen, K.S. et al., Discovery of the toxic dinoflagellate Pfiesteria in northern European waters, Proc. Biol. Sci. 269, 211, 2002.
54. Jeong, H.J. et al., Stoeckeria algicida n. gen., n. spp. (Dinophyceae) from the coastal waters off Southern Korea: morphology and small subunit ribosomal DNA gene sequence, J. Eukaryot. Microbiol. 52, 382, 2005.
55. Rublee, P.A. et al., Detection of the Dinozoans Pfiesteria piscicida and P shumwayae: a review of detection methods and geographic distribution, J. Eukaryot. Microbiol. 52, 83, 2005.
56. Zhang, H. et al., Phylogeny of dinoflagellates based on mitochondrial cytochrome b and nuclear small subunit rDNA sequence comparisons, J. Phycol. 41, 411, 2005.
57. Seaborn, D.W. et al., A group of dinoflagellates similar to Pfiesteria as defined by morphology and genetic analysis, Harmful Algae 5, 2006.
58. Marshall, H.G. et al., Taxonomy of Pfiesteria (Dinophyceae), Harmful Algae 5, 481, 2006.
59. Parrow, M.W. and Burkholder, J.M., The sexual life cycles of Pfiesteria piscicida and cryptoperidin-iopsoids (Dinophyceae), J. Phycol. 40, 664, 2004.
60. Chorus, I. and Bartram, J., Toxic Cyanobacteria in Water—A Guide to Their Public Health Consequences, Monitoring and Management, E & EN Spon for the World Health Organization, New York, 1999.
61. Edvardsen, B. and Paasche, E., Bloom dynamics and physiology of Prymnesium and Chrysochromulina, in Physiological Ecology of Harmful Algae, Anderson, D.M. et al. Springer-Verlag, Berlin, 1998, p. 193.
62. Anderson, D.M., Toxic variability in Alexandrium, in The Fourth International Conference on Toxic Marine Phytoplankton, Granéli, E. et al. Elsevier, New York, 1991, p. 41.
63. Burkholder, J.M. and Glasgow, H.B., The life cycle and toxicity of Pfiesteria piscicida revisited, J. Phycol. 38, 1261, 2002.
64. Gordon, A.S. et al., Characterization of Pfiesteria ichthyocidal activity, Appl. Environ. Microbiol. 71, 6463; author reply 6464, 2005.
65. Glibert, P.M. et al., Direct uptake of nitrogen by Pfiesteria piscicida and Pfiesteria shumwayae, and nitrogen nutritional preferences, Harmful Algae 5, 380, 2006.
66. Guillard, R.R.L., Culture of phytoplankton for feeding marine invertebrates, in Culture of Marine Invertebrate Animals, Smith, W.L. and Chanley, M.H. Plenum Press, New York, 1975, p. 26.
67. Feinstein, T.N. et al., Effects of light on photosynthesis, grazing, and population dynamics of the heterotrophic dinoflagellate Pfiesteira piscicida (Dionphyceae), J. Phycol. 38, 659, 2002.
68. Saito, K. et al., Effect of biotic and abiotic factors on in vitro proliferation, encystment, and excystment of Pfiesteria piscicida, Appl. Environ. Microbiol. 73, 6410, 2007.
69. Lewitus, A.J. et al., Kleptoplastidy in the toxic dinoflagellate Pfiesteira piscicida (Dinophyceae), J. Phycol. 35, 305, 1999.
70. Balzer, I. and Hardeland, R., Effects of indoleamines and short photoperiods on the encystment of Gonyaulax polyedra, Chronobiol. Int. 9, 260, 1992.
71. Anderson, J.T. et al., Formation of two types of cysts by a mixotrophic dinoflagellate, Pfiesteria piscicida, Mar. Ecol. Prog. Ser. 246, 95, 2003.
72. Coyne, K.J. and Craig Cary, S., Molecular approaches to the investigation of viable dinoflagellate cysts in natural sediments from estuarine environments, J. Eukaryot. Microbiol. 52, 90, 2005.
73. Burkholder, J.M. et al., Demonstration of toxicity to fish and to mammalian cells by Pfiesteria species: comparison of assay methods and strains, Proc. Natl. Acad. Sci. USA 102, 3471, 2005.
74. Cancellieri, PJ. et al., Chemosensory attraction of zoospores of the estuarine dinoflagellates, Pfiesteria piscicida and P shumwayae, to finfish mucus and excreta, J. Exp. Mar. Biol. Ecol. 264, 29, 2001.
75. Deeds, J.R. and Place, A.R., Sterol specific membrane interactions with the toxins from Karlodinium micrum (Dinophyceae) - A strategy for self-protection, Afr. J. Mar. Sci. 28, 421, 2006.
76. Parrow, M.W. et al., Contaminant-free cultivation of Pfiesteria shumwayae (Dinophyceae) on a fish cell line, Aquat. Microb. Ecol. 39, 97, 2005.
77. Parrow, M.W. et al., The taxonomy and growth of a Crypthecodinium species (Dinophyceae) isolated from a brackish-water fish aquarium, Afr. J. Mar. Sci. Harmful Algae 28, 185, 2006.
78. Meyer, E.P. and Barclay, L.A., Feild manual for the investigation offish kills, US Department of the Interior Fish and Wildlife Service, Fish and Wildlife Service Resource Publication, Washington, DC, 1990, p. 220.
79. Burkholder, J.M., The lurking perils of Pfiesteria, Sci. Am. 281, 42, 1999.
80. Magnien, R.E. et al., Associations between Pfiesteria, fish health and environmental conditions in Maryland. Final Report: Tidewater Ecosystem Assessment, Department of Natural Resources, Maryland, 2000, p. 37.
81. Glasgow, H.B. et al., Field ecology of toxic Pfiesteria complex species and a conservative analysis of their role in estuarine fish kills, Environ. Health Perspect. 109 (Suppl 5), 715, 2001.
82. Kane, A.S. et al., Etiologies, observations and reporting of estuarine finfish lesions, Mar. Environ. Res. 50, 473, 2000.
83. Law, M., Differential diagnosis of ulcerative lesions in fish, Environ. Health Perspect. 109 (Suppl 5), 681, 2001.
84. Fairey, E.R. et al., Reporter gene assay for fish-killing activity produced by Pfiesteria piscicida, Environ. Health. Perspect. 107, 711, 1999.
85. Moeller, P.D. et al., Current progress in isolation and characterization of toxins isolated from Pfiesteria piscicida, Environ. Health Perspect. 109 (Suppl 5), 739, 2001.
86. Levin, E.D. et al., Learning impairment caused by a toxin produced by Pfiesteria piscicida infused into the hippocampus of rats, Neurotoxicol. Teratol. 25, 419, 2003.
87. Kaiser, J., Microbiology. The science of Pfiesteria: elusive, subtle, and toxic, Science 298, 346, 2002.
88. Kaiser, J., Microbiology. The Pfiesteria conundrum: more study, less certainty, Science 303, 25, 2004.
89. Levin, E.D., A rat model of the cognitive impairment from Pfiesteria piscicida exposure, Environ. Health Perspect. 109 (Suppl 5), 757, 2001.
90. Schmechel, D.E. and Koltai, D.C., Potential human health effects associated with laboratory exposures to Pfiesteria piscicida, Environ. Health Perspect. 109 (Suppl 5), 775, 2001.
91. El-Nabawi, A. et al., The N-methyl-D-aspartate neurotransmitter receptor is a mammalian brain target for the dinoflagellate Pfiesteria piscicida toxin, Toxicol. Appl. Pharmacol. 169, 84, 2000.
92. Moe, C.L. et al., Cohort studies of health effects among people exposed to estuarine waters: North Carolina, Virginia, and Maryland, Environ. Health Perspect. 109 (Suppl 5), 781, 2001.
93. Swinker, M. et al., Estuary-associated syndrome in North Carolina: an occupational prevalence study, Environ. Health Perspect. 109, 21, 2001.
94. Guillard, R.R.L. and Brand, L.E., Toxic Dinoflagellates, in The 3rd International Conference on Toxic Dinoflagellates, Anderson, D.M. et al. Elsevier, St. Andrews, New Brunswick, Canada, 1985, p. 538.
95. Monger, B.C. et al., Feeding selection of heterotrophic marine nanoflagellates based on the surface hydrophobicity of their picoplankton prey, Limnol. Oceanogr. 44, 1917, 1999.
96. Alavi, M. et al., Bacterial community associated with Pfiesteria-like dinoflagellate cultures, Environ. Microbiol. 3, 380, 2001.
97. Alavi, M.R., Predator/prey interaction between Pfiesteria piscicida and Rhodomonas mediated by a marine alpha proteobacterium, Microb. Ecol. 47, 48, 2004.
98. Burkholder, J.M. et al., 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. 109 (Suppl 5), 745, 2001.
99. Miller, T.R. and Belas, R., Dimethylsulfoniopropionate metabolism by Pfiesteria-associated Roseobacter spp., Appl. Environ. Microbiol. 70, 3383, 2004.
100. Guillard, R.R.L., The center for culture of marine phytoplankton: history, structure, function and future, J. Protozool. 35, 255, 1988.
101. Ford, M.J. and Mitton, J.B., Population structure of the pink barnacle, Tetraclita squamosa rubescens, along the California coast, Mol. Mar. Biol. Biothechnol. 2, 147, 1993.
102. Camper, J.D. et al., Mitochondrial DNA variation among red snapper (Lutjanus campechanus) from the Gulf of Mexico, Mol. Mar. Biol. Biotechnol. 2, 154, 1993.
103. Geller, J.B. et al., Interspecific and intrapopulation variation in mitochondrial ribosomal DNA sequences of Mytilus spp. (Bivalvia: Mollusca), Mol. Mar. Biol. Biotechnol. 2, 44, 1993.
104. Bucklin, A. and Kann, L., Mitochondrial DNA variation of copepods: markers of species identity and population differentiation in Calanus, Biol. Bull. Mar. Biol. Lab. Woods Hole 181, 357, 1991.
105. Scholin, C.A. et al., Two distinct small subunit ribosomal RNA genes in the North American toxic dinoflagellate Alexandriumfundyense (Dinophyceae), J. Phycol. 29, 209, 1993.
106. Sako, Y. et al., Specific monoclonal antibodies and DNA probes for the identification of the toxic dinoflagellate genus Alexandrium, in 6th International Conference on Toxic Marine Phytoplankton, Oct 1993, Lassus, P. et al Lavoisier Publishing, Nantes, France, 1995, p. 77.
107. Scholin, C. et al., Detection of HAB species using lectin, antibody and DNA probes, in Manual on Harmful Marine Microalgae, 2nd ed., Hallegraeff, G.M. et al. UNESCO Monographs on Oceanographic Methodology, Paris, France, 2003, p. 131.
108. Anderson, D.M. et al., Identification and enumeration of Alexandrium spp. from the Gulf of Maine using molecular probes, Deep Sea Res. 52, 2467, 2005.
109. Rollo, F. et al., Molecular typing of the red-tide dinoflagellate Gonyaulaxpolyedra in phytoplankton suspensions, Aquat. Microb. Ecol. 9, 55, 1995.
110. Banks, M.A. et al., Discrimination between closely related Pacific oyster species (Crassostrea) via mitochondrial DNA sequences coding for large subunit rRNA, Mol. Mar. Biol. Biotechnol. 2, 129, 1993.
111. Zietkiewicz, E. et al., Genome fingerprinting by simple sequence repeat (SSR)-anchored polymerase chain reaction amplification, Genomics 20, 176, 1994.
112. Williams, J.G. et al., Genetic analysis using random amplified polymorphic DNA markers, Meth. Enzymol. 218, 704, 1993.
113. Olivier, M. et al., Random amplified polymorphic DNA (RAPD) sequences as markers for canine genetic studies, J. Hered. 90, 78, 1999.
114. Rublee, P.A. et al., PCR and FISH detection extends the range of Pfiesteria piscicida in estuarine waters, Va. J. Sci. 50, 325, 1999.
115. Saito, K. et al., Characterization of the rRNA locus of Pfiesteria piscicida and development of standard and quantitative PCR-based detection assays targeted to the nontranscribed spacer, Appl. Environ. Microbiol. 68, 5394, 2002.
116. Bowers, H.A. et al., Development of real-time PCR assays for rapid detection of Pfiesteria piscicida and related dinoflagellates, Appl. Environ. Microbiol. 66, 4641, 2000.
117. Litaker, R.W. et al., Identification of Pfiesteria piscicida (Dinophyceae) and Pifesteria-like organisms using internal transcribed spacer-specific PCR assays, J. Phycol. 39, 754, 2003.
118. Zhang, H. and Lin, S., Detection and quantification of Pfiesteria piscicida by using the mitochondrial cytochrome b gene, Appl. Environ. Microbiol. 68, 989, 2002.
119. Coyne, K.J. et al., Assessing temporal and spatial variability in Pfiesteria piscicida distributions using molecular techniques, Aquat. Microb. Ecol. 24, 275, 2001.
120. Robledo, J.A. et al., Nucleotide sequence variability in the nontranscribed spacer of the rRNA locus in the oyster parasite Perkinsus marinus, J. Parasitol. 85, 650, 1999.
121. Rublee, P.A. et al., Use of molecular probes to assess geographic distribution of Pfiesteria species, Environ. Health Perspect. 109 (Suppl 5), 765, 2001.
122. Lewitus, A.J. and Holland, A.F., Initial results from a multi-institutional collaboration to monitor harmful algal blooms in South Carolina, Environ. Monit. Assess. 81, 361, 2003.
123. Rublee, P.A. et al., Pfiesteria piscicida and Pfiesteria shumwayae in coastal waters of Long Island, New York, USA, Harmful Algae 5, 374, 2006.
124. Rhodes, L.L. et al., Pfiesteria shumwayae (Pfiesteriaceae) in New Zealand, N. Z. J. Freshwater Mar. Sci. 36, 621, 2002.
125. Anderson, D.M. and Wall, D., Potential importance of benthic cysts of Gonyaulax tamarensis and G. excavata in initiating toxic dinoflagellate blooms, J. Phycol. 14, 224, 1978.
126. Anderson, D.M. and Morel, F.M.M., Seeding of 2 red tide blooms by the germination of benthic Gonyaulax tamarensis hypnocysts, Estuar. Coast. Mar. Sci. 8, 279, 1979.
127. Heaney, S.I. et al., The role of the cyst stage in the seasonal growth of the dinoflagellate Ceratium hirundinella within a small productive lake, Br. Phycol. J. 18, 47, 1983.
128. Kim, Y.O. et al., Role of cyst germination in the bloom initiation of Alexandrium tamarense (Dinophyceae) in Masan Bay, Korea, Aquat. Microb. Ecol. 29, 279, 2002.
129. Steidinger, K.A., Implications of dinoflagellate life-cycles on initiation of Gymnodinium breve red tides, Environ. Lett. 9, 129, 1975.
130. Litaker, W. et al., Electrochemical detection of DNA or RNA from harmful algal bloom species, in Harmful Algal Blooms 2000., Hallagraeff, G.M. et al. Intergovernmental Oceanographic Commission of Unesco, Paris, France, 2000, p. 242.
131. Euteneuer, U. and Schliwa, M., Persistent, directional motility of cells and cytoplasmic fragments in the absence of microtubules, Nature 310, 58, 1984.
132. Lee, J. et al., Principles of locomotion for simple-shaped cells, Nature 362, 167, 1993.
133. Burkholder, J.M. and Glasgow, H.B., Jr., Trophic controls on stage transformations of a toxic ambush-predator dinoflagellate, J. Eukaryot. Microbiol. 44, 200, 1997.
134. Grattan, L.M. et al., Neurobehavioral complaints of symptomatic persons exposed to Pfiesteria piscicida or morphologically related organisms, Md Med. J. 47, 127, 1998.
135. Samet, J. et al., 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. 109 (Suppl 5), 639, 2001.
136. Drgon, T. et al., Characterization of ichthyocidal activity of Pfiesteria piscicida: dependence on the dinospore cell density, Appl. Environ. Microbiol. 71, 519, 2005.
137. Quesenberry, M.S. et al., Bioassay for ichthyocidal activity of Pfiesteria piscicida: characterization of a culture flask assay format, J. Appl. Phycol. 14, 241, 2002.
138. Springer, J.J. et al., Interactions between the toxic estuarine dinoflagellate Pfiesteria piscicida and two species of bivalve molluscs, Mar. Ecol. Prog. Ser. 245, 1, 2002.
139. Deeds, J.R. et al., Hemolytic and ichthyotoxic activity from cultures of Karlodinium micrum (Dinophyceae) associated with fish mortalities in an estuarine aquaculture facility, Harmful Algae 1, 169, 2002.
140. Kempton, J.W. et al., Toxicity of Karlodinium micrum (Dinophyceae) associated with a fish kill in a South Carolina brackish retention pond. Harmful Algae 1, 233, 2002.
141. Tashjian, A.H.J., Clonal strains of hormone-producing pituitary cells, Methods Enzymol. 58, 527, 1979.
142. Xi, D. et al., Maitotoxin activates type L-voltage dependent calcium channels and induces a calcium-dependent membrane depolarization in GH4C1 pituitary cells, J. Biol. Chem. 267, 25025, 1992.
143. Xi, D. et al., Maitotoxin induces calcium entry by nimodipine sensitive and insensitive pathways in GH4C1 pituitary cells, Biochem. Pharmacol. 166, 49, 1996.
144. Mosmann, T., Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays, J. Immunol. Meth. 65, 55, 1983.
145. Fairey, E.R. and Ramsdell, J.S., Reporter gene assays for algal-derived toxins, Nat. Toxins 7, 415, 1999.
146. Kimm-Brinson, K.L. et al., Identification of a P2X7 receptor in GH(4)C(1) rat pituitary cells: a potential target for a bioactive substance produced by Pfiesteria piscicida, Environ. Health Perspect. 109, 457, 2001.
147. Peng, Y.G. et al., Neuroexcitatory and neurotoxic actions of the amnesic shellfish poison, domoic acid, Neuroreport 5, 981, 1994.
148. Peng, Y.G. et al., Neuroexcitatory actions of ciguatoxin on brain regions associated with thermoregulation, Neuroreport 6, 305, 1995.
149. Peng, Y.G. and Ramsdell, J.S., Brain fos is a sensitive biomarker for the lowest observed neuroexcitatory effects of domoic acid, Fundam. Appl. Toxicol. 31, 162, 1996.
150. Robertson, L.M. et al., Regulation of c-fos expression in transgenic mice requires multiple interdependent transcription control elements, Neuron 14, 241, 1995.
151. McClellan-Green, P.D. et al., Consumer health risks due to incidental exposure of fish to Pfiesteria piscicida, in Research on Toxic Algae: Pfiesteria-like Organisms, Sea Grant North Carolina, Raleigh, North Carolina, USA, 1998.
152. Kaiser, J., Pfiesteria debate. Is sugary toxin the smoking gun? Science 298, 945, 2002.
153. Lin, S. et al., Low abundance distribution of Pfiesteria piscicida in pacific and western atlantic as detected by mtDNA-18S rDNA real-time polymerase chain reaction, J. Plankton Res. 28, 667, 2006.
154. Goshorn, D. et al., Occurrence of Karlodinium micrum and its association with fish kills in Maryland estuaries, in Harmful algae, 2002, Steidinger, K. et al., St. Petersburg, FL, 2004, p. 361.
155. Fensin, E.E., Occurrence and ecology of the dinoflagellate Karlodinium micrum in estuaries of North Carloina, USA. In Harmful Algae, 2002 Proceedings. Steidinger, K.A. et al. St. Petersberg, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, 62, 2004.
156. Fensin, E.E., Impact of tropical storms and drought on the dinoflagellates Karlodinium micrum and Prorocentrum minimum in estuarine rivers of North Carolina, USA, Afr. J. Mar. Sci. Harmful Algae 28, 277, 2006.
157. Ballantine, D., Two new marine species of Gymnodinium isolated from the Plymouth area, J. Mar. Biolog. Assoc. U.K. 35, 467, 1956.
158. de Salas, M.F. et al., Takayama (Gymnodiniales, Dinophyceae) gen. nov., a new genus of unarmoured dinoflagellates with sigmoid apical grooves, including the description of two new species, J. Phycol. 39, 1233, 2003.
159. Kite, G.C. and Dodge, J.D., Cell and chloroplast ultrastructure in Gyrodinium aureolum and Gymnodin-ium galatheanum, two marine dinoflagellates containing an unusual carotenoid, Sarsia 73, 131, 1988.
160. Leadbeater, B.S.C. and Dodge, J.D., The fine structure of Woloszynskia micra spp. nov., a new marine dinoflagellate, Br. Phycol. J. 3, 1, 1966.
161. Adolf, J.E. et al., Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium venefi-cum, Harmful Algae 6, 400, 2007.
162. Edvardsen, B. et al., Hemolytic activity in extracts of Chrysochromulinapolylepis grown at different levels of selenite and phosphate, in Toxic Marine Phytoplankton, Graneli, E. et al. Elsevier, New York, 1990, p. 284.
163. Deeds, J.R. et al., Geographic strain variation in toxin production in Karlodinium micrum (Dinophyceae) from Southeastern estuaries of the United States, in Harmful Algae, 2002, Steidinger, K.A. et al. (eds.), Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, St. Petersburg, 2004, p. 145.
164. Bachvaroff, T.R. et al., Liquid chromatographic-mass spectroscopic characterization, detection and quantification of karlotoxins, Harmful Algae (In review), 2007.
165. Deeds, J.R. et al., Histopathological effects in fish exposed to the toxins from Karlodinium micrum, J. Aquat. Anim. Health 18, 136, 2006.
166. Leblond, J.D. and Chapman, PJ., A survey of the sterol composition of the marine dinoflagellates Karenia brevis, Karenia mikimotoi, and Karlodinium micrum: distribution of sterols within other members of the class Dinophyceae, J. Phycol. 38, 670, 2002.
167. Adolf, J.E. et al., Species specificity and potential roles of Karlodinium micrum toxin. African Journal of Marine Science Harmful Algae 2004, Pitcher G.C. et al. 28, 415, 2006.
168. Yariv, J. and Hestrin, S., Toxicity of the extracellular phase of Prymnesium parvum cultures, J. Gen. Microbiol. 24, 165, 1961.
169. Martin, D.F. and Padilla, G.M., Some physiological properties of dinoflagellate toxins, in Physiologically Active Compounds from Marine Organisms, Humm, H.J. and Lane, C.E. (eds.) Marcel Dekker, St. Pertersburg, FL, 1974, p. 151.
170. Echigoya, R. et al., The structures of five new antifungal and hemolytic amphidinol analogs from Amphidinium carterae collected in New Zealand, Harmful Algae 4, 383, 2005.
171. Tillman, D.C. et al., Kill and eat your predator: a winning strategy of the planktonic flagellate Prymnesium parvum, Aquat. Microb. Ecol. 32, 73, 2003.
172. Peng, J. et al., Structure of Karlotoxin-2 from a marine dinoflagellate Karlodinium veneficum, J. Am. Chem. Soc. (in press), 2007.
173. Kubota, T. et al., Cloning of polyketide synthase genes from amphidinolide-producing marine dinoflagellate Amphidinium spp., Biol. Pharm. Bull. 29, 1314, 2006.
174. Thompson, P.A. and Hosja, W., Nutrient limitation of phytoplankton in the upper Swan River estuary, Western Australia, Mar. Freshw. Res. 47, 659, 1996.
175. Horner Rosser, S.M.J., An assessment of nitrogen uptake by diatoms and phytoflagellates in the Swan River estuary, Western Australia using stable isotope enrichment techniques, in 15th International Diatom Symposium, John, J. A.R.G. Gantner, Ruggell, Perth, Australia, 1998, p. 443.