Progress in understanding harmful algal blooms: Paradigm shifts and new technologies for research, monitoring, and management

Annual Review of Marine Science

Volumn 4, Issue , 2012, Pages 143-176

  Anderson, Donald M ^a   Cembella, Allan D ^b   Hallegraeff, Gustaaf M ^c  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^c UNIVERSITY OF TASMANIA   (Australia)

Author keywords

climate change; ecogenomics; fish kills; red tide; shellfish toxicity

Indexed keywords

ALLELOCHEMICALS; COASTAL RESOURCES; DIVERSE FIELDS; ECOGENOMICS; ENVIRONMENTAL STRESSORS; FISH KILLS; GENETIC BASIS; HARMFUL ALGAL BLOOMS; HUMAN HEALTH; PARADIGM SHIFTS; PHYTOPLANKTON SPECIES; PUBLIC HEALTH; RED TIDE; STRAIN VARIATION;

ALGAE CONTROL; EUTROPHICATION; PLANTS (BOTANY); RESEARCH; RESEARCH AND DEVELOPMENT MANAGEMENT;

CLIMATE CHANGE;

ALLELOCHEMICAL; BACTERIUM; CLIMATE CHANGE; COASTAL ZONE MANAGEMENT; CONSERVATION MANAGEMENT; ECOLOGICAL IMPACT; ENVIRONMENTAL STRESS; EUTROPHICATION; GENOMICS; GRAZING; MANAGEMENT PRACTICE; MONITORING SYSTEM; PARADIGM SHIFT; PARALYTIC SHELLFISH POISONING; PHYTOPLANKTON; PUBLIC HEALTH; RED TIDE; REGULATORY APPROACH; RESEARCH WORK; TECHNOLOGICAL DEVELOPMENT; TOXIN; ZOOPLANKTON;

ALGAL BLOOM; ANIMAL; CLIMATE CHANGE; ENVIRONMENTAL MONITORING; HUMAN; METHODOLOGY; RESEARCH; REVIEW; SEA;

ANIMALS; CLIMATE CHANGE; ENVIRONMENTAL MONITORING; HARMFUL ALGAL BLOOM; HUMANS; OCEANS AND SEAS; RESEARCH;

EID: 83655192963     PISSN: 19411405     EISSN: 19410611     Source Type: Journal    
DOI: 10.1146/annurev-marine-120308-081121     Document Type: Review

References (151)

1. Adolf JE, Place AR, Stoecker DK, Harding LV. 2007. Modulation of polyunsaturated fatty acids in mixotrophic Karlodinium veneficum (Dinophyceae) and its prey, Storeatula major (Cryptophyceae). J. Phycol. 43:1259-70
2. Alpermann TJ, Beszteri B, John U, Tillmann U, Cembella AD. 2009. Implications of life-history transitions on the population genetic structure of the toxigenic marine dinoflagellate Alexandrium tamarense. Mol. Ecol. 18:2122-33
3. Alpermann TJ, Tillmann U, Beszteri B, Cembella AD, John U. 2010. Phenotypic variation and genotypic diversity in a planktonic population of the toxigenic marine dinoflagellate Alexandrium tamarense (Dinophyceae). J. Phycol. 46:18-32
4. Andersen RA, ed. 2005. Algal Culturing Techniques. New York: Elsevier. 596 pp.
5. Anderson DM. 1989. Toxic algal blooms and red tides: A global perspective. In Red Tides: Biology, Environmental Science and Toxicology, ed. T Okaichi, DM Anderson, T Nemoto, pp. 11-16. New York: Elsevier
6. Anderson DM. 1998. Physiology and bloom dynamics of toxic Alexandrium species, with emphasis on life cycle transitions. In The Physiological Ecology of Harmful Algal Blooms, ed. DM Anderson, AD Cembella, GM Hallegraeff, pp. 29-48. Heidelberg, Germany: Springer-Verlag
7. Anderson DM. 2008. Harmful algal blooms and ocean observing systems: Needs, present status and future potential. In Fisheries for Global Welfare and Environment, ed. K Tsukamoto, T Kawamura, T Takeuchi, TD Beard Jr, MJ Kaiser, pp. 317-34. Tokyo: Terrapub
8. Anderson DM, Andersen P, Bricelj VM, Cullen JJ, Rensel JE. 2001. Monitoring and management strategies for harmful algal blooms in coastal waters. APEC 201-MR-01.1, Asia Pac. Econ. Program Singap. and Intergov. Oceanogr. Comm. Tech. Ser. 59, Paris
9. Anderson DM, Burkholder JM, Cochlan WP, Glibert PM, Gobler CJ, et al. 2008. Harmful algal blooms and eutrophication: Examining linkages from selected coastal regions of the United States. Harmful Algae 8:39-53
10. Anderson DM, Cembella AD, Hallegraeff GM, eds. 1998. The Physiological Ecology of Harmful Algal Blooms. Heidelberg, Germany: Springer-Verlag. 600 pp.
11. Anderson DM,Glibert PM, Burkholder JM. 2002. Harmful algal blooms and eutrophication: Nutrient sources, composition, and consequences. Estuaries 25:704-26
12. Anderson DM, Kulis DM, Doucette GJ, Gallager JC, Balech E. 1994. Biogeography of toxic dinoflagellates in the genus Alexandrium from the northeast United States and Canada as determined by morphology, bioluminescence, toxin composition, and mating compatibility. Mar. Biol. 120:467-78
13. Anderson DM, Kulis DM, Keafer BA, Gribble KE, Marin R, Scholin CA. 2005a. Identification and enumeration of Alexandrium spp. from the Gulf of Maine using molecular probes. Deep-Sea Res. Part II 52:2467-90
14. Anderson DM, Stock CA, Keafer BA, Bronzino Nelson A, Thompson B, et al. 2005b. Alexandrium fundyense cyst dynamics in the Gulf of Maine. Deep-Sea Res. Part II 52:2522-42
15. Anderson DM, Townsend DW, McGillicuddy DJ, Turner JT, eds. 2005c. The ecology and oceanography of toxic Alexandrium fundyense blooms in the Gulf of Maine. Deep-Sea Res. Part II 52(19-21). 512 pp. Armbrust EV. 2009. The life of diatoms in the world's oceans. Nature 459:185-92
16. Bates SS, Bird CJ, de Freitas ASW, Foxall R, Gilgan M, et al. 1989. Pennate diaton Nitzschia pungens as the primary source of domoic acid, a toxin in shellfish from eastern Prince Edward Island, Canada. Can. J. Fish. Aquat. Sci. 46:1203-15
17. Bates SS, Douglas DJ, Doucette GJ, Léger C. 1995. Effects of reintroducing bacteria on domoic acid production by axenic cultures of the diatom Pseudonitzschia pungens f. multiseries. In HarmfulMarine Algal Blooms, ed. P Lassus, G Arzul, E Erard, P Gentien, C Marcaillou-Le Baut, pp. 401-6. Paris: Lavoisier Sci.
18. Beardall J, Raven JA. 2004. The potential effects of global climate change onmicroalgal photosynthesis, growth and ecology. Phycologia 43:26-41
19. Berdalet E. 1992. Effects of turbulence on the marine dinoflagellate Gymnodinium nelsoni. J. Phycol. 28:267-72
20. Berg GM, Glibert PM, Lomas MW, Burford MA. 1997. Organic nitrogen uptake and growth by the chrysophyte Aureococcus anophagefferens during a brown tide event. Mar. Biol. 129:377-87
21. Blauw AN, Los FJ, Huisman J, Peperzak L. 2010. Nuisance foam events and Phaeocystis globosa blooms in Dutch coastal waters analyzed with fuzzy logic. J. Mar. Syst. 83:115-26
22. Bodeanu N, Ruta G. 1998. Development of the planktonic algae in the Romanian Black Sea sector in 1981- 1996. Harmful Algae: Proc. 8th Int. Conf.Harmful Algae, ed.BReguera, J Blanco,MLFernandez,TWyatt, pp. 188-91. Paris: Xunta de Galicia and Intergov. Oceanogr. Comm. UNESCO
23. Bolch CJS, de Salas MF. 2007. A review of the molecular evidence for ballast water introduction of the toxic dinoflagellates Gymnodinium catenatum and the Alexandrium "tamarensis complex" to Australasia. Harmful Algae 6:465-85
24. Bowers HA, Tomas C, Tengs T, Kempton JW, Lewitus AJ, Oldach DW. 2006. Raphidophyceae [Chadefaud ex Silva] systematics and rapid identification: Sequence analyses and real-time PCR assays. J. Phycol. 2:1333-48
25. Casteleyn G, Chepurnov VA, Leliaert F, Mann DG, Bates SS, et al. 2008. Pseudo-nitzschia pungens (Bacillariophyceae): A cosmopolitan diatom species? Harmful Algae 7:241-57
26. Cembella AD. 2003. Chemical ecology of eukaryotic microalgae in marine ecosystems. Phycologia 42:420-47
27. Cembella AD, Bauder AG, Lewis NI, Quilliam MA. 2001. Association of the gonyaulacoid dinoflagellate Alexandrium ostenfeldii with spirolide toxins in size-fractionated plankton. J. Plankton Res. 23:1413-19
28. Cembella AD, Sullivan JJ, BoyerGL, Taylor FJR, Anderson RJ. 1987. Variation in paralytic shellfish toxin composition within the Protogonyaulax tamarensis/catenella species complex: Red tide dinoflagellates. Biochem. Syst. Ecol. 15:171-86
29. Chan LL, Hodgkiss IJ, Lam PKS, Wan JMF, Chou H-N, et al. 2005. Use of 2-DE to differentiate morphospecies of Alexandrium minutum, a PSP toxin-producing agent of harmful algal blooms. Proteomics 5:1580-93
30. Chan LL, Sit WH, Lam PKS, Hsieh DPH, Hodgkiss IJ, et al. 2006. Identification and characterization of a 'biomarker of toxicity' from the proteome of the paralytic shellfish toxin-producing dinoflagellate, Alexandrium tamarense. Proteomics 6:654-66
31. Charleson RJ, Lovelock JE, Andreae MO, Warren SG. 1987. Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326:655-61
32. 2 in a green alga. Nature 431:566-69
33. Coyne KJ, Handy SM, Demir E, Whereat EB, Hutchins DA, et al. 2005. Improved quantitative real-time PCR assays for enumeration of harmful algal species in field samples using an exogenous DNA reference standard. Limnol. Oceanogr. Methods 3:381-91
34. Dale B. 2001. The sedimentary record of dinoflagellate cysts: Looking back into the future of phytoplankton blooms. Sci. Mar. 65:257-72
35. DaugbjergN,HansenG,Larsen J,MoestrupØ. 2000. Phylogeny of some of themajor genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmored dinoflagellates. Phycologia 39:302-17
36. De Salas MF, Laza-Martínez A, Hallegraeff GM. 2008. Five new species of Karlodinium and one new Takayama (Kareniaceae, Dinophyceae) from open Southern Ocean waters. J. Phycol. 44:241-57
37. Dorantes-Aranda JJ, Waite TD, Godrant A, Rose AL, Tovar CD, et al. 2011. Novel application of a fish gill cell line assay to assess ichthyotoxicity of harmful marine microalgae. Harmful Algae 10:366-73
38. 2, temperature and irradiance on themarine coccolithophore Emiliania huxleyi (Prymnesiophyceae). Eur. J. Phycol. 43:87-98
39. Franks PJS. 1997. Coupled physical-biological models for the study of harmful algal blooms. Ocean Res. 19:153-60
40. Franks PJS, Anderson DM. 1992. Alongshore transport of a toxic phytoplankton bloom in a buoyancy current: Alexandrium tamarensis in the Gulf of Maine. Mar. Biol. 112:153-64
41. Fux E, Smith JL, Tong M, Guzmán L, Anderson DM. 2011. Toxin profiles of five geographical isolates of Dinophysis spp. from North and South America. Toxicon 57:275-87
42. Garcés E, Montresor M, Lewis J, Rengefors K, Anderson DM, Barth H, eds. 2010. Phytoplankton life cycles and their impacts on the ecology of harmful algal blooms. Deep-Sea Res. Part II 57(3-4). 164 pp.
43. Gentien P, Lunven M, Lazure P, Youenou A, Crassous MP. 2007. Motility and autotoxicity in Karenia mikimotoi (Dinophyceae). Philos. Trans. R. Soc. B 362:1937-46
44. Gentien P, Lunven M, Lehaitre M, Duvent JL. 1995. In situ depth profiling of particle sizes. Deep-Sea Res. Part I 42:1297-312
45. Glibert PM, Mayorga E, Seitzinger S. 2008. Prorocentrum minimum tracks anthropogenic nitrogen and phosphorus inputs on a global basis: Application of spatially explicit nutrient export models. Harmful Algae 8:33-38
46. Glob. Ecol. Oceanogr. Harmful Algal Blooms. 2006. Global ecology and oceanography of harmful algal blooms: HABs in eutrophic systems. GEOHAB Rep. 4, ed. P Glibert, Intergov. Oceanogr. Comm. UNESCO and Sci. Comm. Ocean. Res., Paris and Baltimore
47. Gobler CJ, Berry DL, Dyhrman ST,Wilhelm SW, Salamov A, et al. 2011. Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proc. Natl. Acad. Sci. USA 108:4352-57
48. Goffredi SK, Jones W, Scholin C, Marin R, Hallam S, Vrjenhoek RC. 2006. Molecular detection of marine larvae. Mar. Biotechnol. 8:149-60
49. Gordon BR, LeggatW. 2010. Symbiodinium: Invertebrate symbioses and the role of metabolomics. Mar. Drugs 8:2546-68
50. Granéli E,Turner J, eds. 2006. Ecology of Harmful Algae. Ecol. Stud. Ser. 189. Heidelberg,Germany: Springer- Verlag. 413 pp.
51. Gribble KE, Keafer BA, Quilliam MA, Cembella AD, Kulis DM, et al. 2005. Distribution and toxicity of Alexandrium ostenfeldii (Dinophyceae) in the Gulf of Maine, USA. Deep-Sea Res. Part II 52:2745-63
52. Hackett JD, ScheetzTE, Yoon HS, SoaresMB, BonaldoMF, et al. 2005. Insights into a dinoflagellate genome through expressed sequence tag analysis. BMC Genomics 6:80
53. Hackett JD, Wisecaver JH, Brosnahan ML, Kulis DM, Anderson DM, et al. 2011. Independent evolution of saxitoxin synthesis in cyanobacteria and dinoflagellates. Mol. Biol. Evol. In press
54. Hallegraeff GM. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99
55. Hallegraeff GM. 2010. Ocean climate change, phytoplankton community responses, and harmful algal blooms: A formidable predictive challenge. J. Phycol. 46:220-35
56. Hallegraeff GM, Anderson DM, Cembella AD, eds. 2003. Manual on Harmful Marine Microalgae. UNESCO Monogr. Oceanogr. Methodol. 11. Paris: UNESCO. 792 pp.
57. Haywood AJ, Scholin CA, Marin R III, Petrik K, Pigg R, et al. 2009. Detection of Karenia brevis in Florida coastal waters using sandwich hybridization assays in two formats. Proc. 6th Int. Conf. Molluscan Shellfish Saf., pp. 95-100. R. Soc. N.Z. Misc. Ser. 71. Wellington, New Zealand: R. Soc. N.Z.
58. He R, McGillicuddy DJ, Keafer BA, AndersonDM. 2008. Historic 2005 toxic bloom of Alexandrium fundyense in the western Gulf of Maine: 2: Coupled biophysical numerical modeling. J. Geophys. Res. Oceans 113:C07040
59. Hiller S, Krock B, Cembella A, Luckas B. 2007. Rapid detection of cyanobacterial toxins in precursor ion mode by liquid chromatography tandem mass spectrometry. J. Mass Spectrom. 42:1238-50
60. Holligan PM. 1979. Dinoflagellate blooms associated with tidal fronts around the British Isles. Toxic Dinoflag. Blooms: Proc. 2nd Int. Conf. Toxic Dinoflag. Blooms, ed. DL Taylor, HH Seliger, pp. 249-56. New York: Elsevier/North Holland
61. Huntley M, Sykes P, Rohan S, Marin V. 1986. Chemically-mediated rejection of dinoflagellate prey by the copepods Calanus pacificus and Paracalanus parvus: Mechanism, occurrence and significance. Mar. Ecol. Prog. Ser. 28:105-20
62. 2 world. Science 320:336-40
63. Intergov. Panel Clim. Change. 2008. Climate Change 2007: Impacts, Adaptation and Vulnerability: Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge Univ. Press
64. Ishida Y, Yoshinaga I, Kim M-C, Uchida A. 1997. Possibility of bacterial control of harmful algal blooms. Prog. Microb. Ecol.: Proc. 7th Int. Symp. Microb. Ecol., Santos, Sao Paulo, Brazil 1995, ed. MT Martins, MIZ Sato, JM Tiedje, LCN Hagler, J Dobereiner, PS Sanchez, pp. 495-500. Brazil: SBM/ICOME
65. Jaeckisch N, Singh R, Curtis B, Cembella A, John U. 2008. Genomic characterization of the spirolideproducing dinoflagellate Alexandrium ostenfeldii with special emphasis on PKS genes. Harmful Algae: Proc. 12th Int. Conf. Harmful Algae, ed. O Moestrup, G Doucette, H Enevoldsen, A Godhe, G. Hallegraeff, et al., pp. 65-67. Copenhagen: Int. Soc. Stud. Harmful Algae and Intergov.Oceanogr.Comm.UNESCO
66. James KJ, Moroney C, Roden C, Satake M, Yasumoto T, et al. 2003. Ubiquitous 'benign' alga emerges as the cause of shellfish contamination responsible for the human toxic syndrome, azaspiracid poisoning. Toxicon 41:145-51
67. Jenkinson I, Arzul G. 1998. Effect of the flagellates Gymnodinium mikimotoi, Heterosigma akashiwo and Pavlova lutheri on flow through fish gills. Harmful Algae: Proc. 8th Int. Conf. Harmful Algae, ed. B Reguera, J Blanco ML Fernandez, T Wyatt, pp. 425-28. Paris: Xunta de Galicia and Intergov. Oceanogr. Comm. UNESCO
68. Jeong HJ, Kim JS, Kim JH, Kim ST, Seong KA. 2005a. Feeding and grazing impact of the newly described heterotrophic dinoflagellate Stoeckeria algicida on the harmful alga Heterosigma akashiwo. Mar. Ecol. Prog. Ser. 295:69-78
69. Jeong HJ, Yoo YD, Park JY, Song JY, Kim ST, et al. 2005b. Feeding by phototrophic red-tide dinoflagellates: Five species newly revealed and six species previously known to be mixotrophic. Aquat. Microb. Ecol. 40:133-50
70. John U, Beszteri B, Derelle E, van de Peer Y, Read B, et al. 2008. Novel insights into evolution of protistan polyketide synthases through phylogenomic analysis. Protist 159:21-30
71. John U, Beszteri S, Gloeckner G, Singh R, Medlin LK, Cembella AD. 2010. Genomic characterization of the ichthyotoxic prymnesiophyte Chrysochromulina polylepis, and the expression of polyketide synthase genes in synchronised cultures. Eur. J. Phycol. 45:215-29
72. Jones KL, Mikulski CM, Barnhorst A, Doucette GJ. 2010. Comparative analysis of bacterioplankton assemblages from Karenia brevis bloom and nonbloom water on the west Florida shelf (Gulf of Mexico, USA) using 16S rRNA gene clone libraries. FEMS Microbiol. Ecol. 73:468-85
73. Kamykowski D. 1974. Possible interactions between phytoplankton and semidiurnal internal tides. J. Mar. Res. 32:67-89
74. Kellmann R, Mihali TK, Jeon YJ, Pickford R, Pomati F, Neilan BA. 2008. Biosynthetic intermediate analysis and functional homology reveal a saxitoxin gene cluster in cyanobacteria. Appl. Environ. Microbiol. 74:4044-53
75. Kirkpatrick GJ, Millie DF,MolineMA, Schofield O. 2000. Optical discrimination of a phytoplankton species in natural mixed populations. Limnol. Oceanogr. 45:467-71
76. Kirkpatrick GJ, Orrico C, MolineMA, Oliver M, Schofield OM. 2003. Continuous hyperspectral absorption measurements of colored dissolved organic material in aquatic systems. Appl. Opt. 42:6564-68
77. Kodama M, Doucette GJ, Green DH. 2006. Relationships between bacteria and harmful algae. See Granéli & Turner 2006, pp. 243-55
78. Kooistra WHCF, Sarno D, Balzano S, Gu H, Andersen RA, Zingone A. 2008. Global diversity and biogeography of Skeletonema species (Bacillariophyta). Protist 159:177-93
79. Krock B, Seguel CG, Valderrama K, Tillmann U. 2009. Pectenotoxins and yessotoxin from Arica Bay, North Chile as determined by tandem mass spectrometry. Toxicon 54:364-67
80. La Claire JW. 2006. Analysis of expressed sequence tags from the harmful alga, Prymnesium parvum (Prymnesiophyceae, Haptophyta). Mar. Biotechnol. 8:534-46
81. Langer G, Nehrke G, Probert I, Ly J, Ziveri P. 2009. Strain-specific responses of Emiliania huxleyi to changing seawater carbonic chemistry. Biogeosci. Discuss. 6:4361-83
82. Lefebvre KA, Bargu S, Kieckhefer T, Silver MW. 2002. From sanddabs to blue whales: The pervasiveness of domoic acid. Toxicon 40:971-77
83. LegrandC, Rengefors K, Fistarol GO, Granéli E. 2003. Allelopathy in phytoplankton: Biochemical, ecological and evolutionary aspects. Phycologia 42:406-19
84. Li Y, He R, McGillicuddy DJ Jr, Anderson DM, Keafer BA. 2009. Investigation of the 2006 Alexandrium fundyense bloom in the Gulf of Maine: In situ observations and numerical modeling. Cont. Shelf Res. 29:2069-82
85. Lidie KL, Ryan JC, Barbier M, Van Dolah FM. 2005. Gene expression in the Florida red tide dinoflagellate Karenia brevis: Analysis of an expressed sequence tag (EST) library and development of aDNAmicroarray. Mar. Biotechnol. 7:1-14
86. Lilly EL, HalaynchKM, Anderson DM. 2007. Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae). J. Phycol. 43:1329-38
87. Lilly EL, Kulis DM, Gentien P, Anderson DM. 2002. Paralytic shellfish poisoning toxins in France linked to a human-introduced strain of Alexandrium catenella from the western Pacific: Evidence from DNA and toxin analysis. J. Plankton Res. 24:443-52
88. Litaker RW, Vandersea MW, Faust MA, Kibler SR, Chinain M, et al. 2009. Taxonomy of Gambierdiscus including four new species, Gambierdiscus caribaeus, Gambierdiscus carolinianus, Gambierdiscus carpenteri and Gambierdiscus ruetzleri (Gonyaulacales, Dinophyceae). Phycologia 48:344-90
89. Longhurst A, Sathyendranath S, Platt T, Caverhill C. 1995. An estimate of global primary production in the ocean from satellite radiometer data. J. Plankton Res. 17:1245-71
90. Ma H, Krock B, Tillmann U, Cembella A. 2010. Towards characterization of lytic compound(s) produced by Alexandrium tamarense. Harmful Algae 2008: Proc. 13th Int. Conf. Harmful Algae, ed. K Ho, M Zhou, Y Qi, pp. 142-46. Hong Kong: Int. Soc. Stud. Harmful Algae and Intergov. Oceanogr. Comm. UNESCO
91. Marshall JA, Nichols PD, Hamilton B, Lewis RJ, Hallegraeff GM. 2003. Ichthyotoxicity of Chattonella marina (Raphidophyceae) to damselfish (Acanthochromis polycanthus): The synergistic role of reactive oxygen species and free fatty acids. Harmful Algae 2:273-81
92. Masseret E,Grzebyk D, Nagai S,Genovesi B, Lasserre B, et al. 2009. Unexpected genetic diversity among and within populations of the toxic dinoflagellate Alexandrium catenella as revealed by nuclear microsatellite markers. Appl. Environ. Microbiol. 75:2037-45
93. McGillicuddy DJ Jr. 2010. Models of harmful algal blooms: Conceptual, empirical, and numerical approaches. J. Mar. Syst. 83:105-7
94. McGillicuddy DJ Jr, Anderson DM, Lynch DR, Townsend DW. 2005. Mechanisms regulating large-scale seasonal fluctuations in Alexandrium fundyense populations in the Gulf of Maine: Results from a physicalbiological model. Deep-Sea Res. Part II 52:2698-14
95. McGillicuddy DJ Jr, Townsend DW, He R, Keafer BA, Kleindinst JL, et al. 2011. Suppression of the 2010 Alexandrium fundyense bloom by changes in physical, biological, and chemical properties of the Gulf of Maine. Limnol. Oceanogr. In press
96. Monroe EA, Van Dolah FM. 2008. The toxic dinoflagellate Karenia brevis encodes novel type I-like polyketide synthases containing discrete catalytic domains. Protist 159:471-82
97. Montagna PA, Stockwell D, Street G. 1993. Effect of the Texas brown tide on Mulinia lateralis populations and feeding. J. Shellfish Res. 12:142
98. Mooney BD,Dorantes-Aranda JJ, Place AR,Hallegraeff GM. 2011. Ichthyotoxicity of gymnodinioid dinoflagellates (Kareniaceae): Activity of PUFA and superoxide against sheepshead minnow larvae and rainbow trout gill cells. Mar. Ecol. Prog. Ser. 426:213-24
99. Nagai S, Nishitani G, Sakamoto S, Sugaya T, Lee CK, et al. 2009. Genetic structuring and transfer of marine dinoflagellate Cochlodinium polykrikoides in Japanese and Korean coastal waters revealed bymicrosatellites. Mol. Evol. 18:2337-52
100. Nézan E, Chomérat N. 2011. Vulcanodinium rugosum gen. et sp. nov. (Dinophyceae), un nouveau dinoflagellé marin de la c ôte méditerranéenne française. Cryptogamie Algologie 32:3-18
101. Nielsen LT, Jakobsen HH, Hansen PJ. 2010. High resilience of two coastal plankton communities to twentyfirst century seawater acidification: Evidence from microcosm studies. Mar. Biol. Res. 6:542-55
102. Nosenko T, Lidie KL, Van Dolah FM, Lindquist E, Cheng J-F, et al. 2006. Chimeric plastid proteome in the Florida "Red Tide" dinoflagellate Karenia brevis. Mol. Biol. Evol. 23:2026-38
103. Oda T, Ishimatsu A, Shimada S, Takeshita S, Muramatsu T. 1992. Oxygen-radical-mediated toxic effects of the red tide flagellate Chattonella marina on Vibrio alginolyticus. Mar. Biol. 112:505-9
104. Okaichi T. 1997. Red tides in the Seto Inland Sea. In Sustainable Development in the Seto Inland Sea, Japan: From the Viewpoint of Fisheries, ed. T Okaichi, Y Yanagi, pp. 251-304. Tokyo: Terrapub ORION Exec. Steer. Comm. 2005. Ocean Observatories Initiative Science Plan. Washington, DC: ORION. 102 pp.
105. Park MG, Kim S, Kang YG, Yih W. 2006. First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquat. Microb. Ecol. 45:101-6
106. Penna A, Magnani M. 1999. Identification of Alexandrium (Dinophyceae) species using PCR and rDNAtargeted probes. J. Phycol. 35:615-21
107. Prince EK,Myers TL, Kubanek J. 2008. Effects of harmful algal blooms on competitors: Allelopathic mechanisms of the red tide dinoflagellate Karenia brevis. Limnol. Oceanogr. 53:531-41
108. Pollinger U, Zemel E. 1981. In situ and experimental evidence of the influence of turbulence on cell division processes of Peridinium cinctum forma westii (Lemm.) Lefévre. Br. J. Phycol. 16:281-87
109. Quilliam MA. 2003. The role of chromatography in the hunt for red tide toxins. J. Chromatogr. A 100:527-48
110. Raine R, McDermott G, Silke J, Lyons K, Nolan G, Cusack C. 2010. A simple short range model for the prediction of harmful algal events in the bays of southwestern Ireland. J. Mar. Syst. 83:150-57
111. Rensel JE. 1993. Severe blood hypoxia of Atlantic salmon (Salmo salar) exposed to themarine diatom Chaetoceros concavicornis. In Toxic Phytoplankton Blooms in the Sea, ed. TJ Smayda, Y Shimizu, pp. 625-30. Amsterdam: Elsevier
112. Rhodes L, Scholin CA, Tyrrell JV, Adamson J, Todd K. 2001. The integration of DNA probes into New Zealand's routine phytoplankton monitoring programs. In Harmful Algal Blooms 2000: Proc. 9th Int. Conf. Harmful Algal Blooms, ed.GMHallegraeff, SI Blackburn, CJ Bolch, RJ Lewis, pp. 429-32. Paris: Intergov. Oceanogr. Comm. UNESCO
113. Rhodes L, Smith KF, Munday R, Selwood A, McNabb P, et al. 2010. Toxic dinoflagellates (Dinophyceae) from Rarotonga, Cook Islands. Toxicon 56:751-58
114. Richardson TL, Pinckney JL. 2004. Monitoring of the toxic dinoflagellate Karenia brevis using gyroxanthinbased detection methods. J. Appl. Phycol. 16:315-28
115. 2. Nature 407:364-67
116. Roman J, McCarthy JJ. 2010. The whale pump: Marine mammals enhance primary productivity in a coastal basin. PLoS One 5:e13255
117. Rost B, Zondervan I, Wolf-GladrowD. 2008. Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: Current knowledge, contradictions and research directions. Mar. Ecol. Prog. Ser. 373:227-37
118. Ruiz Sebastián C, Etheridge SM, Cook PA, O'Ryan C, Pitcher GC. 2005. Phylogenetic analysis of toxic Alexandrium (Dinophyceae) isolates from South Africa: Implications for the global phylogeography of the Alexandrium tamarense species complex. Phycologia 44:49-60
119. Salomon PS, Imai I. 2006. Pathogens of harmful microalgae. See Granéli & Turner 2006, pp. 271-82
120. Scholin CA, Anderson DM. 1994. Identification of species and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae): I: RFLP analysis of SSU rRNA genes. J. Phycol. 30:744-54
121. Scholin CA, Buck KR, Britschgi T, Cangelosi G, Chavez FP. 1996. Identification of Pseudo-nitzschia australis (Bacillariophyceae) using rRNA-targeted probes in whole cell and sandwich hybridization formats. Phycologia 35:190-97
122. Scholin CA, Doucette G, Jensen S, Roman B, Pargett D, et al. 2009. Remote detection of marine microbes, small invertebrates, harmful algae and biotoxins using the Environmental Sample Processor (ESP). Oceanography 22:158-67
123. Scholin CA,Hallegraeff GM, AndersonDM. 1995. Molecular evolution of the Alexandrium tamarense 'species complex' (Dinophyceae): Dispersal in theNorth American andWest Pacific regions. Phycologia 34:472-85
124. Skovgaard A, Hansen PJ. 2003. Food uptake in the harmful alga Prymnesium parvum mediated by excreted toxins. Limnol. Oceanogr. 48:1161-66
125. Smayda TJ. 1989. Primary production and the global epidemic of phytoplankton blooms in the sea: A linkage? In Novel Phytoplankton Blooms: Causes and Impacts of Recurrent Brown Tide and Other Unusual Blooms, ed. EM Cosper, EJ Carpenter, M. Bricelj, pp. 213-28. New York: Springer-Verlag
126. Smayda TJ. 1997. Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr. 42:1137-53
127. Smetacek V. 2001. A watery arms race. Nature 411:745
128. Smil V. 2001. Enriching the Earth: Fritz Haber, Carl Bosch, and the Transformation of World Food. Cambridge, MA: MIT Press
129. Steidinger KA, Wolny JL, Haywood AJ. 2008. Identification of Kareniaceae (Dinophyceae) in the Gulf of Mexico. Nova Hedwig. 133:269-84
130. Stock CA, McGillicuddy DJ, Solow AR, Anderson DM. 2005. Evaluating hypotheses for the initiation and development of Alexandrium fundyense blooms in the western Gulf of Maine using a coupled physicalbiological model. Deep-Sea Res. Part II 52:2715-44
131. Strong AL, Cullen JJ, Chisholm SW. 2009. Ocean fertilization: Science, policy, and commerce. Oceanography 22:236-60
132. Stucken K, John U, Cembella A, Murillo AA, Soto-Liebe K, et al. 2010. The smallest known genomes of multicellular and toxic cyanobacteria: Comparison,minimal gene sets for linked traits and the evolutionary implications. PLoS One 5:e9235
133. Stumpf RP,TomlinsonMC, Calkins JA, Kirkpatrick B, Fisher K, et al. 2009. Skill assessment for an operational algal bloom forecast system. J. Mar. Syst. 76:151-61
134. Takeuchi T, Kokubo T, Fukuyo Y, Matsuoka K. 1995. Quantitative relationship among vegetative cells, planozygotes, and hypnozygotes of Alexandrium catenella (Dinophyceae) in its blooming season at Tanabe Bay, Central Japan. Proc. 7th Int. Conf. Toxic Phytoplankton, ed.TYasumoto, Y Oshima, Y Fukuyo (Abstr.). Paris: Intergov. Oceanogr. Comm. UNESCO
135. Taylor FJR, Pollingher U. 1987. Ecology of dinoflagellates. In The Biology of Dinoflagellates, ed. FJR Taylor, pp. 398-501. Bot. Monogr. 21. Oxford, UK: Blackwell Sci.
136. Teegarden GJ, Cembella AD. 1996. Grazing of toxic dinoflagellates Alexandrium spp. by adult copepods of coastalMaine: Implications for the fate of paralytic shellfish toxins in marine food webs. J. Exp.Mar. Biol. Ecol. 196:145-76
137. Thomas WH, Gibson CH. 1990. Effects of small-scale turbulence on microalgae. J. Appl. Phycol. 2:71-77
138. Tillmann U. 2003. Interactions between planktonic microalgae and protozoan grazers. J. Phycol. 39(Suppl. S1):56
139. Tillmann U, Alpermann T, John U, Cembella A. 2008. Allelochemical interactions and short-term effects of the dinoflagellate Alexandrium on selected photoautotrophic and heterotrophic protists. Harmful Algae 7:52-64
140. Tong M, Kulis DM, Smith JL, Fux E, Hess P, et al. 2011. The effects of growth stage and light intensity on the toxicity of Dinophysis acuminata in the northeast US. Harmful Algae 10:254-64
141. Turner JT. 2006. Harmful algae interactions with marine planktonic grazers. See Granéli & Turner 2006, pp. 259-70
142. Turner JT, Granéli E. 2006. "Top-down" predation control on marine harmful algae. See Granéli & Turner 2006, pp. 355-66
143. Uribe P, Fuentes D, Valdés J, Shmrayahu A, Zúniga A, et al. 2008. Preparation and analysis of an expressed sequence tag library from the toxic dinoflagellate Alexandrium catenella. Mar. Biotechnol. 10:692-700
144. Velo-Suárez L, Reguera B, Gonzáles-Gil S, Lunven M, Lazure P, et al. 2010. Application of a 3D Lagrangian model to explain the decline of a Dinophysis acuminata bloom in the Bay of Biscay. J. Mar. Syst. 83:242-52
145. Walsh JJ, Kirkpatrick G, eds. 2008. Ecology and oceanography of harmful algal blooms in Florida. Cont. Shelf Res. 28(1). 214 pp.
146. Woo SPS, Liu W, Au DWT, Anderson DM, Wu RSS. 2006. Antioxidant responses and lipid peroxidation in gills and erythrocytes of fish (Rhabdosarga sarba) upon exposure to Chattonella marina and hydrogen peroxide: Implications on the cause of fish kills. J. Exp. Mar. Biol. Ecol. 336:230-41
147. Woods J, Barkmann W. 1993. The plankton multiplier: Positive feedback in the greenhouse. J. Plankton Res. 15:1053-74
148. Work TM, Barr B, Beale AM, Fritz L, Quilliam MA, Wright JLC. 1993. Epidemiology of domoic acid poisoning in brown pelicans (Pelecanus occidentalis) and Brandt's cormorants (Phalacrocorax penicillatus) in California. J. Zoo Wildl. Med. 24:54-62
149. Yang I, John U, Beszteri S, Gloeckner G, Krock B, et al. 2010. Comparative gene expression in toxic versus non-toxic strains of the marine dinoflagellate Alexandrium minutum. BMC Genomics 11:248
150. YoungC,TrumanP,BoucherM,Keyzers RA,Northcote P, JordanTW.2009. The algal metabolite yessotoxin affects heterogeneous nuclear ribonucleoproteins in HepG2 cells. Proteomics 9:2529-42
151. Zhou M-J, Shen Z-L, Yu R-C. 2008. Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River. Cont. Shelf Res. 28:1483-89