Advertisement

The Role of Life Cycle Characteristics in Harmful Algal Bloom Dynamics

  • Rhodora V. Azanza
  • Michael L. Brosnahan
  • Donald M. Anderson
  • Inga Hense
  • Marina Montresor
Chapter
Part of the Ecological Studies book series (ECOLSTUD, volume 232)

Abstract

Life cycle-based adaptations are integral to the ecology of most organisms. For the toxic microalgal species Pyrodinium bahamense, Alexandrium fundyense, Pseudo-nitzschia spp., and Nodularia spumigena, the properties and behaviours of their life cycle stages enable them to thrive in diverse marine environments. Planktonic blooms of these species are associated with a range of negative impacts including fisheries closures and animal die-offs. As a result, their bloom dynamics have been studied extensively, illustrating the ways that each organism’s life cycle is adaptive to recurring biotic and abiotic stressors. Both P. bahamense and A. fundyense form thick-walled resting cysts that play a major role in the dynamics of episodic blooms and can lie dormant for extended intervals in bottom sediments. These cysts function effectively in both tropical and temperate habitats. Nodularia spumigena uses a related but different strategy by producing akinetes that help in its recurrence. Pseudo-nitzschia species do not form resting or benthic stages, but undergo sexuality to counteract the progressive decrease in cell size due to cell division with a rigid siliceous frustule. These life cycles are clearly adaptable to a broad range of environments as shown by their widespread distribution and abundance. Continued investigation of these life cycles, especially stage-specific interactions with biotic and abiotic conditions, is likely to provide further insights into algal species ecology broadly, including responses to global climate change, ocean acidification, and coastal nutrient enrichment.

Notes

Acknowledgments

The authors acknowledge the support of (1) the Department of Science and Technology (DOST), Philippines, for R.V. Azanza; (2) the National Science Foundation (OCE-0430724, OCE-0911031, and OCE-1314642) and National Institutes of Health (NIEHS-1P50-ES021923-01) through the Woods Hole Center for Oceans and Human Health, MIT Sea Grant (NA14OAR4170077), and Woods Hole Sea Grant (NA14OAR4170074, R/P-84) for M. Brosnahan and D. Anderson; (3) the national flagship programme RIcerca ITaliana per il MARE (RITMARE) for M. Montresor; and (4) the Cluster of Excellence “CliSAP” (EXC177), University of Hamburg, funded by the German Science Foundation (DFG) for I. Hense. Thanks go to J.C. Dungca-Santos for manuscript typing and Seija Hällfors (Syke) for providing the picture of N. spumigena.

References

  1. Amato A, Orsini L, D’Alelio D et al (2005) Life cycle, size reduction patterns, and ultrastructure of the pennate planktonic diatom Pseudo-nitzschia delicatissima (Bacillariophyceae). J Phycol 41:542–556CrossRefGoogle Scholar
  2. Amin SA, Hmelo LR, van Tol HM et al (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98–101PubMedCrossRefGoogle Scholar
  3. Amorim A, Dale B (1998) Distribution of cysts from toxic or potentially toxic dinoflagellates along the Portuguese coast. In: Reguera B, Blanco J, Fernandez M et al (eds) Harmful algae. Proceedings of the 8th International Conference on harmful algae, Vigo, Spain, 25–29 June 1997. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Paris, pp 64–65Google Scholar
  4. Anderson CR, Siegel DA, Kudela RM et al (2009) Empirical models of toxigenic Pseudo-nitzschia blooms: potential use as a remote detection tool in the Santa Barbara Channel. Harmful Algae 8:478–492CrossRefGoogle Scholar
  5. Anderson DM (1989) Toxic algal blooms and red tides: a global perspective. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides: biology, environmental science, and toxicology. Elsevier Science Publishing Co. Inc., New York, pp 11–16Google Scholar
  6. Anderson DM (1997) Bloom dynamics of toxic Alexandrium species in the northeastern US. Limnol Oceanogr 42:1009–1022CrossRefGoogle Scholar
  7. Anderson DM, Alpermann TJ, Cembella AD, Collos Y, Masseret E, Montresor M (2012) The globally distributed genus Alexandrium: Multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14:10–35PubMedPubMedCentralCrossRefGoogle Scholar
  8. Anderson DM, Chisholm SW, Watras CJ (1983) The importance of life cycle events in the population dynamics of Gonyaulax tamarensis. Mar Biol 76:179–190CrossRefGoogle Scholar
  9. Anderson DM, Keafer BA (1987) An endogenous annual clock in the toxic marine dinoflagellate Gonyaulax tamarensis. Nature 325:616–617PubMedCrossRefGoogle Scholar
  10. Anderson DM, Keafer BA, Kleindinst JL et al (2014a) Alexandrium fundyense cysts in the Gulf of Maine: long-term time series of abundance and distribution, and linkages to past and future blooms. Deep Sea Res Part II 103:6–26CrossRefGoogle Scholar
  11. Anderson DM, Kulis DM, Binder BJ (1984) Sexuality and cyst formation in the dinoflagellate Gonyaulax tamarensis: cyst yield in batch cultures. J Phycol 20:418–425CrossRefGoogle Scholar
  12. Anderson DM, McGillicuddy DJ Jr, DeGrasse SL et al (eds) (2014b) Harmful algae in the Gulf of Maine: oceanography, population dynamics, and toxin transfer in the food web. Deep Sea Res Part II 103:1–376Google Scholar
  13. Anderson DM, Morel FMM (1979) The seeding of two red tide blooms by the germination of benthic Gonyaulax tamarensis hypnocysts. Estuar Coast Mar Sci 8:279–293CrossRefGoogle Scholar
  14. Anderson DM, Stonzenbach KD (1985) Selective retention of two dinoflagellates in a well-mixed estuarine embayment: The importance of diel vertical migration and surface avoidance. Mar Ecol Prog Ser 25:39–50CrossRefGoogle Scholar
  15. Anderson DM, Taylor CD, Armbrust EV (1987) The effects of darkness and anaerobiosis on dinoflagellate cyst germination. Limnol Oceanogr 32:340–351CrossRefGoogle Scholar
  16. Anderson DM, Townsend DW, McGillicuddy DJ et al (eds) (2005) The ecology and oceanography of toxic Alexandrium fundyense blooms in the Gulf of Maine. Deep Sea Res II 52:2365–2876Google Scholar
  17. Anderson DM, Wall D (1978) Potential of benthic cysts of Gonyaulax tamarensis and G. excavata in initiating toxic dinoflagellate blooms. J Phycol 14:224–234CrossRefGoogle Scholar
  18. Anglès S, Garcés E, Hattenrath-Lehmann TK et al (2012) In situ life-cycle stages of Alexandrium fundyense during bloom development in Northport Harbor (New York, USA). Harmful Algae 16:20–26CrossRefGoogle Scholar
  19. Azanza RV (1997) Contributions to the understanding of the bloom dynamics of Pyrodinium bahamense var. compressum: a toxic red tide causative organism. Sci Diliman 9:1–6Google Scholar
  20. Azanza RV (2013) Harmful algal blooms in tropical embayments affected by monsoons. In: Roy S, Pospelova V, Montresor M et al (eds) GEOHAB 2013. Global ecology and oceanography of harmful algal blooms, GEOHAB core research project: HABs in fjords and coastal embayments. Second open science meeting. progress in interpreting life history and growth dynamics of harmful algal blooms in fjords and coastal environments. IOC and SCOR, Paris, France and Newark, DE, USA, pp 20–23Google Scholar
  21. Azanza RV, Siringan FP, San Diego-McGlone ML et al (2004) Horizontal dinoflagellate cyst distribution, sediment characteristics and benthic flux in Manila Bay, Philippines. Phycol Res 52:376–386Google Scholar
  22. Azanza RV, Taylor FJRM (2001) Are Pyrodinium blooms in the Southeast Asian region recurring and spreading? A view at the end of the millennium. Ambio 30:356–364PubMedCrossRefGoogle Scholar
  23. Balech E (1985) A rediscription of Pyrodinium bahamense Plate (Dinoflagellata). Rev Paleobot Palynol 45:17–34CrossRefGoogle Scholar
  24. Bohm A (1931) Peridineen aus dem Persischen Golf und dem Golf von Oman. Arch Protistenk 74:188–197Google Scholar
  25. Bornet E, Flahault C (1888) Revision des Nostacacees heterocystees continues dans les principaux herbiers de France (quatrieme et dernier fragment). Ann Sci Nat Bot 7:177–262Google Scholar
  26. Bravo I, Fraga S, Figueroa RI et al (2010) The intricacies of dinoflagellate pellicle cysts: the example of Alexandrium minutum cysts from a bloom-recurrent area (Bay of Baiona, NW Spain). Deep Sea Res II 57:166–174CrossRefGoogle Scholar
  27. Brosnahan ML, Farzan S, Keafer BA et al (2014) Complexities of bloom dynamics in the toxic dinoflagellate Alexandrium fundyense revealed through DNA measurements by imaging flow cytometry coupled with species-specific rRNA probes. Deep Sea Res II 103:185–198CrossRefGoogle Scholar
  28. Brosnahan ML, Velo-Suárez L, Ralston DK et al (2015) Rapid growth and concerted sexual transitions by a bloom of the harmful dinoflagellate Alexandrium fundyense (Dinophyceae). Limnol Oceanogr 60:2059–2078PubMedPubMedCentralCrossRefGoogle Scholar
  29. Burford MA, Hamilton DP, Wood SA (2018) Emerging HAB research issues in freshwater environments. In: Glibert PM, Berdalet E, Burford M et al (eds) Global ecology and oceanography of harmful algal blooms. Springer, Cham, pp 381–402CrossRefGoogle Scholar
  30. Cayetano AC, Yñiguez AT, Villanoy CL et al (2013) Improving the validity and robustness of a harmful algal bloom model through genetic algorithm-based optimization. J Environ Sci Manage Special Issue 1:21–28Google Scholar
  31. Chepurnov VA, Mann DG, Sabbe K et al (2005) Sexual reproduction, mating system chloroplast dynamics and abrupt cell size reduction in Pseudo-nitzschia pungens from the North Sea (Bacillariophyta). Eur J Phycol 40:379–395CrossRefGoogle Scholar
  32. Choi CJ, Brosnahan ML, Sehein TR, Anderson DM, Erdner DL (2017) Insights into the loss factors of phytoplankton blooms: The role of cell mortality in the decline of two inshore Alexandrium blooms. Limnol Oceanogr 62:1742–1753CrossRefGoogle Scholar
  33. Corrales RA, Crisostomo R (1996) Variation of Pyrodinium cyst density in Manila Bay, Philippines. In: Yasumoto T, Oshima Y, Fukuyo Y (eds) Harmful and toxic algal blooms. IOC of UNESCO, Paris, pp 181–184Google Scholar
  34. Corrales RA, Reyes M, Martin M (1995) Notes on the encystment and excystment of Pyrodinium bahamense var. compressum in vitro. In: Lassus P, Arzul G, Erard-Le Denn E et al (eds) Harmful marine algal blooms. Lavoisier Science Publ., Paris, pp 573–578Google Scholar
  35. Cox PA, Banack SA, Murch SJ et al (2005) Diverse taxa of cyanobacteria produce β-N-methylamino-L-alanine, a neurotoxic amino acid. Proc Natl Acad Sci USA 102:5074–5078PubMedPubMedCentralCrossRefGoogle Scholar
  36. Crespo BG, Keafer BA, Ralston DK, Lind H, Dawson F, Anderson DM (2011) Dynamics of Alexandrium fundyense blooms and shellfish toxicity in the Nauset Marsh System of Cape Cod (Massachusetts, USA). Harmful Algae 12:26–38PubMedPubMedCentralCrossRefGoogle Scholar
  37. Czerny J, Barcelos e Ramos J, Riebesell U (2009) Influence of elevated CO2 concentrations on cell division and nitrogen fixation rates in the bloom-forming cyanobacterium Nodularia spumigena. Biogeosciences 6:1865–1875CrossRefGoogle Scholar
  38. D’Alelio D, Amato A, Luedeking A et al (2009) Sexual and vegetative phases in the planktonic diatom Pseudo-nitzschia multistriata. Harmful Algae 8:225–232CrossRefGoogle Scholar
  39. D’Alelio D, Ribera d’Alcalà M, Dubroca L et al (2010) The time for sex: a biennial life cycle in a marine planktonic diatom. Limnol Oceanogr 55:106–114CrossRefGoogle Scholar
  40. Doucette GJ, Cembella AD, Boyer GL (1989) Cyst formation in the red tide dinoflagellate Alexandrium tamarense (Dinophyceae): effects of iron stress. J Phycol 25:721–731CrossRefGoogle Scholar
  41. Eichner M, Rost B, Kranz SA (2014) Diversity of ocean acidification effects on marine N2 fixers. J Exp Mar Biol Ecol 457:199–207CrossRefGoogle Scholar
  42. Fauchot J, Saucier FJ, Levasseur M et al (2008) Wind-driven river plume dynamics and toxic Alexandrium tamarense blooms in the St. Lawrence estuary (Canada): a modeling study. Harmful Algae 7:214–227CrossRefGoogle Scholar
  43. Fehling J, Davidson K, Bolch C et al (2006) Seasonality of Pseudo-nitzschia spp. (Bacillariophyceae) in western Scottish waters. Mar Ecol Prog Ser 323:91–105CrossRefGoogle Scholar
  44. Feifel KM, Fletcher SJ, Watson LR et al (2015) Alexandrium and Scrippsiella cyst viability and cytoplasmic fullness in a 60-cm sediment core from Sequim Bay, WA. Harmful Algae 47:56–65CrossRefGoogle Scholar
  45. Franks PSJ, Anderson DM (1992) Alongshore transport of a toxic phytoplankton bloom in a buoyancy current: Alexandrium tamarense in the Gulf of Maine. Mar Biol 112:153–164CrossRefGoogle Scholar
  46. Fryxell GA, Garza SA, Roelke DL (1991) Auxospore formation in an Antarctic clone of Nitzschia subcurvata Hasle. Diatom Res 6:235–245CrossRefGoogle Scholar
  47. Furio EF, Azanza RV, Fukuyo Y et al (2012) Review of geographical distribution of dinoflagellate cysts in Southeast Asian coasts. Coastal Mar Sci 35:20–33Google Scholar
  48. Galat DL, Verdin JP, Sims LL (1990) Large-scale patterns of Nodularia spumigena blooms in Pyramid Lake, Nevada, determined from Landsat imagery: 1972-1986. Hydrobiologia 197:147–164CrossRefGoogle Scholar
  49. GEOHAB (2001) Global ecology and oceanography of harmful algal blooms, science plan. Glibert P, Pitcher G (eds) SCOR and IOC, Baltimore and Paris, 86 ppGoogle Scholar
  50. Giddings SN, MacCready P, Hickey BM et al (2014) Hindcasts of potential harmful algal bloom transport pathways on the Pacific Northwest coast. J Geophys Res Oceans 119:2439–2461CrossRefGoogle Scholar
  51. Glibert PM, Pitcher GC, Bernard S et al (2018) Advancements and continuing challenges of emerging technologies and tools for detecting harmful algal blooms, their antecedent conditions and toxins, and applications in predictive models. In: Glibert PM, Berdalet E, Burford M et al (eds) Global ecology and oceanography of harmful algal blooms. Springer, Cham, pp 339–357CrossRefGoogle Scholar
  52. Hallegraeff GM (1998) Transport of toxic dinoflagellates via ships ballast water: bioeconomic risk assessment and efficacy of possible ballast water management strategies. Mar Ecol Prog Ser 168:297–309CrossRefGoogle Scholar
  53. Hallegraeff GM (2010) Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J Phycol 46:220–235CrossRefGoogle Scholar
  54. Hallegraeff GM, Bolch CJ (1991) Transport of toxic dinoflagellate cysts via ships’ ballast water. Mar Poll Bull 22:27–30CrossRefGoogle Scholar
  55. He R, McGillicuddy DJ Jr, Keafer BA et al (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).  https://doi.org/10.1029/2007JC004601
  56. Hense I (2007) Regulative feedback mechanisms in cyanobacteria-driven systems: a model study. Mar Ecol Prog Ser 339:41–47CrossRefGoogle Scholar
  57. Hense I, Beckmann A (2006) Towards a model of cyanobacteria life cycle – effects of growing and resting stages on bloom formation of N2-fixing species. Ecol Model 195:205–218CrossRefGoogle Scholar
  58. Hense I, Beckmann A (2015) A theoretical investigation of the diatom cell size reduction-restitution cycle. Ecol Model 317:66–82CrossRefGoogle Scholar
  59. Hense I, Burchard H (2010) Modelling cyanobacteria in shallow coastal seas. Ecol Model 221:238–244CrossRefGoogle Scholar
  60. Hense I, Meier HM, Sonntag S (2013) Projected climate change impact on Baltic Sea cyanobacteria: climate change impact on cyanobacteria. Clim Change 119:391–406CrossRefGoogle Scholar
  61. Holtermann KE, Bates SS, Trainer VL et al (2010) Mass sexual reproduction in the toxigenic diatoms Pseudo-nitzschia australis and P. pungens (Bacillariophyceae) on the Washington coast. J Phycol 46:41–52CrossRefGoogle Scholar
  62. Huber AL (1984) Nodularia (Cyanobacteriaceae) akinetes in the sediments of the peel-harvey estuary, Western Australia: potential inoculum source for Nodularia blooms. Appl Environ Microbiol 47(2):234–238PubMedPubMedCentralGoogle Scholar
  63. Ishikawa A, Hattori M, Imai I (2007) Development of the “plankton emergence trap/chamber (PET Chamber)”, a new sampling device to collect in situ germinating cells from cysts of microalgae in surface sediments of coastal waters. Harmful Algae 6:301–307CrossRefGoogle Scholar
  64. John U, Litaker RW, Montresor M et al (2014) Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist 165(6):779–804PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kahru M, Elmgren R (2014) Multidecadal time series of satellite-detected accumulations of cyanobacteria in the Baltic Sea. Biogeosciences 11:3619–3633CrossRefGoogle Scholar
  66. Karlson AML, Nascimento FJA, Suikkanen S et al (2012) Benthic fauna affects recruitment from sediments of the harmful cyanobacterium Nodularia spumigena. Harmful Algae 20:126–131CrossRefGoogle Scholar
  67. Kooistra WHCF, Gersonde R, Medlin LK et al (2007) The origin and evolution of the diatoms: their adaptation to a planktonic existence. In: Falkowski PG, Knoll AH (eds) Evolution of primary producers in the sea. Elsevier Academic Press, Burlington, pp 207–250CrossRefGoogle Scholar
  68. Kruger T, Monch B, Oppenhauser S et al (2010) LC-MS/MS determination of the isomeric neurotoxins BMAA (β-N-methylamino-L-alanine) and DAB (2, 4-diaminobutyric acid) in cyanobacteria and seeds of Cycas revoluta and Lathyrus latifolius. Toxicon 55(2):547–557PubMedCrossRefGoogle Scholar
  69. Lane JQ, Raimondi PT, Kudela RM (2009) Development of a logistic regression model for the prediction of toxigenic Pseudo-nitzschia blooms in Monterey Bay, California. Mar Ecol Prog Ser 383:37–51CrossRefGoogle Scholar
  70. Lefebvre KA, Robertson A (2010) Domoic acid and human exposure risks: a review. Toxicon 56:218–230PubMedCrossRefGoogle Scholar
  71. Lefebvre KA, Bargu S, Kieckhefer T, Silver MW (2002) From sanddabs to blue whales: the pervasiveness of domoic acid. Toxicon 40:971–977PubMedCrossRefGoogle Scholar
  72. Lehtimaki J, Moisander P, Sivonen K et al (1997) Growth, nitrogen fixation, and nodularin production by two Baltic Sea cyanobacteria. Appl Environ Microbiol 63:1647–1656PubMedPubMedCentralGoogle Scholar
  73. Lelong A, Hégaret H, Soudant P et al (2012) Pseudo-nitzschia (Bacillariophyceae) species domoic acid and amnesic shellfish poisoning: revisiting previous paradigms. Phycologia 51:168–216CrossRefGoogle Scholar
  74. Li Y, He R, McGillicuddy DJ Jr et al (2009) Investigation of the 2006 Alexandrium fundyense bloom in the Gulf of Maine: In-situ observations and numerical modeling. Cont Shelf Res 29:2069–2082PubMedPubMedCentralCrossRefGoogle Scholar
  75. Lilly EL, Halanych KM, Anderson DM (2007) Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae). J Phycol 43:1329–1338CrossRefGoogle Scholar
  76. Lim HC, Teng ST, Leaw CP et al (2013) Three novel species in the Pseudo-nitzschia pseudodelicatissima complex: P. batesiana sp. nov., P. lundholmiae sp. nov., and P. fukuyoi sp. nov. (Bacillariophyceae) from the Strait of Malacca, Malaysia. J Phycol 49:902–916PubMedPubMedCentralGoogle Scholar
  77. Lundholm N, Clarke A, Ellegaard M (2010) A 100-year record of changing Pseudo-nitzschia species in a sill-fjord in Denmark related to nitrogen loading and temperature. Harmful Algae 9:449–457CrossRefGoogle Scholar
  78. Margulis L, Sagan D (1985) Origins of sex. Yale University Press, New HavenGoogle Scholar
  79. Matrai P, Thompson B, Keller M (2005) Circannual excystment of resting cysts of Alexandrium spp. from eastern Gulf of Maine populations. Deep Sea Res II 52:2560–2568CrossRefGoogle Scholar
  80. McGillicuddy DJ Jr, Anderson DM, Lynch DR et al (2005) Mechanisms regulating large-scale seasonal fluctuations in Alexandrium fundyense populations in the Gulf of Maine: Results from a physical-biological model. Deep Sea Res Part II 52:2698–2714CrossRefGoogle Scholar
  81. McGillicuddy DJ Jr, Townsend DW, He R 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 56:2411–2426PubMedPubMedCentralCrossRefGoogle Scholar
  82. McGillicuddy DJ Jr, Townsend DW, Keafer BA et al (2014) Georges Bank: a leaky incubator of Alexandrium fundyense blooms. Deep Sea Res Part II 103:163–173CrossRefGoogle Scholar
  83. McQuoid MR (2005) Influence of salinity on seasonal germination of resting stages and composition of microplankton on the Swedish west coast. Mar Ecol Prog Ser 289:151–163CrossRefGoogle Scholar
  84. Mertens KN, Wolny J, Carbonell-Moore C et al (2015) Taxonomic re-examination of the toxic armored dinoflagellate Pyrodinium bahamense Plate 1906: can morphology or LSU sequencing separate P. bahamense var. compressum from var. bahamense? Harmful Algae 41:1–24CrossRefGoogle Scholar
  85. Moeys S, Frenkel J, Lembke C et al (2016) A sex-inducing pheromone triggers cell cycle arrest and mate attraction in the diatom Seminavis robusta. Sci Rep 6:19252PubMedPubMedCentralCrossRefGoogle Scholar
  86. Montresor M, Di Prisco C, Sarno D et al (2013) Diversity and germination patterns of diatom resting stages at a coastal Mediterranean site. Mar Ecol Prog Ser 484:79–95CrossRefGoogle Scholar
  87. Montresor M, Vitale L, D’Alelio D et al (2016) Sex in marine planktonic diatoms: insights and challenges. Perspect Phycol.  https://doi.org/10.1127/pip/2016/0045
  88. Morquecho L, Alonso-Rodriguez R, Martinez-Tecuapacho GA (2014) Cyst morphology, germination characteristics, and potential toxicity of Pyrodinium bahamense in the Gulf of California. Bot Mar 57:303–314CrossRefGoogle Scholar
  89. O’Neil JM, Davis TW, Burford MA et al (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334CrossRefGoogle Scholar
  90. Olenin S, Gollasch S, Jonusas S et al (2000) En-route investigations of plankton in ballast water on a ship’s voyage from the Baltic Sea to the open Atlantic coast of Europe. Int Rev Hydrobiol 85:577–596CrossRefGoogle Scholar
  91. Onda DFL, Lluisma AO, Azanza RV (2014) Development, morphological characteristics and viability of temporary cysts of Pyrodinium bahamense var. compressum (Dinophyceae) in vitro. Eur J Phycol 49(3):265–275CrossRefGoogle Scholar
  92. Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1:27–37PubMedCrossRefGoogle Scholar
  93. Paerl HW, Hall NS, Calandrino ES (2011) Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci Total Environ 409:1739–1745PubMedCrossRefGoogle Scholar
  94. Pfiester LA, Anderson DM (1987) Dinoflagellate life cycles and their environmental control. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell Scientific Publications, Ltd., Oxford, pp 611–648Google Scholar
  95. Pilskaln CH, Hayashi K, Keafer BA et al (2014) Benthic nepheloid layers in the Gulf of Maine and Alexandrium cyst inventories. Deep Sea Res II 103:55–65CrossRefGoogle Scholar
  96. Pitcher GC, Figueiras FG, Kudela RM et al (2018) Key questions and recent research advances on harmful algal blooms in eastern boundary upwelling systems. In: Glibert PM, Berdalet E, Burford M et al (eds) Global ecology and oceanography of harmful algal blooms. Springer, Cham, pp 205–227CrossRefGoogle Scholar
  97. Plate L (1906) Pyrodinium bahamense n.g, n.sp. die. Leucht-Peridinee des “Feuersees” von Nassau, Bahamas. Arch Protistenkd 7:411–429Google Scholar
  98. Quijano-Scheggia S, Garcés E, Andree K et al (2009) Homothallic auxosporulation in Pseudo-nitzschia brasiliana (Bacillariophyta). J Phycol 45:100–107PubMedCrossRefGoogle Scholar
  99. Raine R, Berdalet E, Yamazaki H et al (2018) Key questions and recent research advances on harmful algal blooms in stratified systems. In: Glibert PM, Berdalet E, Burford M et al (eds) Global ecology and oceanography of harmful algal blooms. Springer, Cham, pp 165–186CrossRefGoogle Scholar
  100. Ralston DK, Brosnhan ML, Fox SE et al (2015) Temperature and residence time controls on an estuarine harmful algal bloom: modeling hydrodynamics and Alexandrium fundyense in Nauset estuary. Estuar Coasts 38:2240–2258CrossRefGoogle Scholar
  101. Ralston DK, Keafer BA, Brosnahan ML et al (2014) Temperature dependence of an estuarine harmful algal bloom: resolving interannual variability in bloom dynamics using a degree-day approach. Limnol Oceanogr 59:1112–1126PubMedPubMedCentralCrossRefGoogle Scholar
  102. Rathaille AN, Raine R (2011) Seasonality in the excystment of Alexandrium minutum and Alexandrium tamarense in Irish coastal waters. Harmful Algae 10(6):629–635CrossRefGoogle Scholar
  103. Rengefors K, Karlsson I, Hansson L-A (1998) Algal cyst dormancy: a temporal escape from herbivory. Proc R Soc Lond B 265:1353–1358CrossRefGoogle Scholar
  104. Rinehart KL, Harada K, Namikoshi M et al (1988) Nodularin, microcystin, and the configuration of Adda. J Am Chem Soc 110:8557–8558CrossRefGoogle Scholar
  105. Rines JEB, Donaghay PL, Dekshenieks MM et al (2002) Thin layers and camouflage: hidden Pseudo-nitzschia spp. (Bacillariophyceae) populations in a fjord in the San Juan Islands, Washington, USA. Mar Ecol Prog Ser 225:123–137CrossRefGoogle Scholar
  106. Roy S, Montresor M, Cembella A (2018) Key questions and recent research advances on harmful algal blooms in fjords and coastal embayments. In: Glibert PM, Berdalet E, Burford M et al (eds) Global ecology and oceanography of harmful algal blooms. Springer, Cham, pp 187–203CrossRefGoogle Scholar
  107. Ruggiero MV, Sarno D, Barra L et al (2015) Diversity and temporal pattern of Pseudo-nitzschia species (Bacillariophyceae) through the molecular lens. Harmful Algae 42:15–24CrossRefGoogle Scholar
  108. Sarno D, Zingone A, Montresor M (2010) A massive and simultaneous sex event of two Pseudo-nitzschia species. Deep Sea Res Part II 57:248–255CrossRefGoogle Scholar
  109. Scalco E, Amato A, Ferrante M et al (2015) The sexual phase of the diatom Pseudo-nitzschia multistriata: cytological and time-lapse cinematography characterization. Protoplasma:1–11.  https://doi.org/10.1007/s00709-015-0891-5
  110. Scalco E, Stec K, Iudicone D et al (2014) The dynamics of sexual phase in the marine diatom Pseudo-nitzschia multistriata (Bacillariophyceae). J Phycol 50:817–828PubMedCrossRefGoogle Scholar
  111. Sekula-Wood E, Schnetzer A, Benitez-Nelson CR et al (2009) Rapid downward transport of the neurotoxin domoic acid in coastal waters. Nat Geosci 2:272–275CrossRefGoogle Scholar
  112. Siringan FP, Azanza RV, Macalalad NJH et al (2008) Temporal changes in the cyst densities of Pyrodinium bahamense var. compressum and other dinoflagellates in Manila Bay, Philippines. Harmful Algae 7:523–531CrossRefGoogle Scholar
  113. Sison-Mangus MP, Jiang S, Tran KN et al (2013) Host-specific adaptation governs the interaction of the marine diatom, Pseudo-nitzschia and their microbiota. ISME J.  https://doi.org/10.1038/ismej.2013.138
  114. Smayda TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42:1137–1153CrossRefGoogle Scholar
  115. Solow AR, Beet AR, Keafer BA et al (2014) Testing for simple structure in a spatial time series with an application to the distribution of Alexandrium resting cysts in the Gulf of Maine. Mar Ecol Prog Ser 501:291–296CrossRefGoogle Scholar
  116. Steidinger K, Tester LS, Taylor FJR (1980) A redescription of Pyrodinium bahamense var. compressa (Bohm) stat. nov. from Pacific red tides. Phycologia 19:329–337CrossRefGoogle Scholar
  117. Stock CA, McGillicuddy DJ Jr et al (2005) Evaluating hypotheses for the initiation and development of Alexandrium fundyense blooms in the western Gulf of Maine using a coupled physical-biological model. Deep Sea Res Part II 52:2715–2744CrossRefGoogle Scholar
  118. Stoyneva MP (2016) Allochtonous planktonic algae recorded during the last 25 years in Bulgaria and their possible dispersal agents. Hydrobiologia 764:53–64CrossRefGoogle Scholar
  119. Suikkanen S, Kaartokallio H, Halfors S et al (2010) Life cycle strategies of bloom-forming, filamentous cyanobacteria in the Baltic Sea. Deep Sea Res Part II 57(3):199–209CrossRefGoogle Scholar
  120. Sullivan JM, Swift E, Donaghay PL et al (2003) Small-scale turbulence affects the division rate and morphology of two red-tide dinoflagellates. Harmful Algae 2:183–199CrossRefGoogle Scholar
  121. Teng ST, Lim HC, Lim PT et al (2014) Pseudo-nitzschia kodamae sp. nov. (Bacillariophyceae), a toxigenic species from the Strait of Malacca, Malaysia. Harmful Algae 34:17–28CrossRefGoogle Scholar
  122. Timmerman AHV, McManus MA, Cheriton OM et al (2014) Hidden thin layers of toxic diatoms in a coastal bay. Deep Sea Res Part II 101:129–140CrossRefGoogle Scholar
  123. Toth GB, Noren N, Selander E et al (2004) Marine dinoflagellates show induced life-history shifts to escape parasite infection in response to water-borne signals. Proc R Soc B Biol Sci 271:733–738CrossRefGoogle Scholar
  124. Townsend DW, McGillicuddy DJ Jr, Thomaza MA et al (2014) Nutrients and water masses in the Gulf of Maine-Georges Bank region: variability and importance to blooms of the toxic dinoflagellate Alexandrium fundyense. Deep Sea Res Part II 103:238–263CrossRefGoogle Scholar
  125. Trainer VL, Bates SS, Lundholm N et al (2012) Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae 14:271–300CrossRefGoogle Scholar
  126. Vahtera E, Crespo BG, McGillicuddy DJ Jr et al (2014) Alexandrium fundyense cyst viability and germling survival in light vs. dark at a constant low temperature. Deep Sea Res Part II 103:112–119CrossRefGoogle Scholar
  127. Velo-Suárez L, Brosnahan ML, Anderson DM et al (2013) A quantitative assessment of the role of the parasite Amoebophrya in the termination of Alexandrium fundyense blooms within a small coastal embayment. PLoS One 8(12):e81150.  https://doi.org/10.1371/journal.pone.0081150CrossRefPubMedPubMedCentralGoogle Scholar
  128. Villanoy CL, Azanza RV, Altemerano A et al (2006) Attempts to model the bloom of Pyrodinium, a tropical toxic dinoflagellate. Harmful Algae 5:156–183CrossRefGoogle Scholar
  129. Villanoy CL, Corrales RA, Jacinto GS et al (1996) Towards the development of a cyst-based model for Pyrodinium red tides in Manila Bay, Philippines. In: Yasumoto T, Oshima Y, Fukuyo Y (eds) Harmful and toxic algal blooms. IOC-UNESCO, Paris, pp 189–192Google Scholar
  130. Wall D, Dale B (1969) The hystrichospaerid resting spore of the dinoflagellate Pyrodinium bahamense Plate 1906. J Phycol 5:140–149PubMedCrossRefGoogle Scholar
  131. Yñiguez AT, Cayetano A, Villanoy CL et al (2012) Investigating the roles of intrinsic and extrinsic factors in the blooms of Pyrodinium bahamense var. compressum using an individual-based model. Proc Environ Sci 13:1462–1476CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Rhodora V. Azanza
    • 1
  • Michael L. Brosnahan
    • 2
  • Donald M. Anderson
    • 2
  • Inga Hense
    • 3
  • Marina Montresor
    • 4
  1. 1.The Marine Science InstituteUniversity of the PhilippinesQuezon CityPhilippines
  2. 2.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA
  3. 3.Institute for Hydrobiology and Fisheries Science, Center for Earth System Research and SustainabilityUniversity of HamburgHamburgGermany
  4. 4.Integrative Marine Ecology DepartmentStazione Zoologica Anton DohrnNaplesItaly

Personalised recommendations