Oceanography The Official Magazine of
The Oceanography Society
Volume 30 Issue 01

View Issue TOC
Volume 30, No. 1
Pages 45 - 57


Harmful Algal Blooms in Fjords, Coastal Embayments, and Stratified Systems: Recent Progress and Future Research

By Elisa Berdalet , Marina Montresor, Beatriz Reguera, Suzanne Roy, Hidekatsu Yamazaki, Allan Cembella, and Robin Raine 
Jump to
Article Abstract Citation References Copyright & Usage
Article Abstract

Harmful algal blooms (HABs) are natural phenomena that result from the interplay of biological, chemical, physical, and sedimentary processes occurring at different temporal and spatial scales. This paper provides an integrated description of HAB dynamics occurring at the mesoscale (10–100 km, sensu Haury et al., 1978) in confined and semi-confined coastal environments and under stratified water column conditions in a diversity of habitats where HAB events occur. It also focuses on relevant aspects occurring at fine-scale and even smaller cellular scales that are critical to species interactions with their environments. Examples include the key role of life-history stages in the recurrence of HABs in certain embayments; the physical-biological interactions driving the formation, maintenance, and decline of thin layers of plankton, including harmful microalgae; the fascinating, but poorly understood, domain of small-scale chemical interactions between HAB species and components of the food web; the potential link between human activities and climate change; and the trends in HAB occurrence. Development of new observing and sampling technologies and of new modeling approaches has resulted in greater understanding of these phenomena. Two Core Research Projects initiated under the GEOHAB Implementation Strategy, “HABs in Fjords and Coastal Embayments” and “HABs in Stratified Systems,” are discussed and priorities for future research toward improving the management and mitigation of HAB impacts are outlined.


Berdalet, E., M. Montresor, B. Reguera, S. Roy, H. Yamazaki, A. Cembella, and R. Raine. 2017. Harmful algal blooms in fjords, coastal embayments, and stratified systems: Recent progress and future research. Oceanography 30(1):46–57, https://doi.org/10.5670/oceanog.2017.109.


Alldredge, A.L., T.J. Cowles, S. MacIntyre, J.E.B. Rines, P.L. Donaghay, C.F. Greenlaw, D.V. Holliday, M.M. Dekshenieks, J.M. Sullivan, and J.R.V. Zaneveld. 2002. Occurrence and mechanisms of formation of a dramatic thin layer of marine snow in a shallow Pacific fjord. Marine Ecology Progress Series 233:1–12, https://doi.org/​10.3354/meps233001.

Alves de Souza, C., D. Pecqueur, E. Le Floc’h, S. Mas, C. Roques, B. Mostajir, F. Vidussi, L. Velo-Suárez, M. Sourisseau, E. Fouilland, and L. Guillou. 2015. Significance of plankton community structure and nutrient availability for the control of dinoflagellate blooms by parasites: A modeling approach. PLoS ONE 10(6):e0127623, https://doi.org/10.1371/journal.pone.0127623.

Anderson, D.M., B.A. Keafer, J.L. Kleindinst, D.J. McGillicuddy Jr., J.L. Martin, K. Norton, C.H. Pilskaln, J.L. Smith, C.R. Sherwood, B. Butman. 2014. 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 Research Part II 103:6–26, https://doi.org/10.1016/j.dsr2.2013.10.002.

Artigas, M.L., C. Llebot, O.N. Ross, N.Z. Neszi, V. Rodellas, J. Garcia-Orellana, P. Masqué, J. Piera, M. Estrada, and E. Berdalet. 2014. Understanding the spatio-temporal variability of phytoplankton biomass distribution in a microtidal estuary. Deep Sea Research Part II 101:180–192, https://doi.org/10.1016/j.dsr2.2014.01.006.

Azanza, R.V. 2013. Harmful Algal Blooms in tropical embayments affected by monsoons. Pp. 20–23 in 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. S. Roy, V. Pospelova, M. Montresor, and A.D. Cembella, eds, IOC and SCOR, Paris, France, and Newark, Delaware, USA.

Azanza, R.V., M.L. Brosnahan, D.M. Anderson, I. Hense, M. Montresor. In press. The role of life cycle characteristics on harmful algal bloom dynamics. In Global Ecology and Oceanography of Harmful Algal Blooms (GEOHAB). P.M. Glibert, E. Berdalet, M. Burfot, G. Pitcher, and M. Zhou, Ecological Studies Series, Springer.

Berdalet, E., R. Kudela, E. Urban, H. Enevoldsen, N.S. Banas, L. Mackenzie, M. Montresor, M. Burford, C.J. Gobler, B. Karlson, and others. 2017. GlobalHAB: A new program to promote international research, observations, and modeling of harmful algal blooms in aquatic systems. Oceanography 30(1):70–81, https://doi.org/10.5670/oceanog.2017.111.

Berdalet, E., G. Llaveria, and R. Simó. 2011. Modulation of dimethylsulfoniopropionate (DMSP) concentration in an Alexandrium minutum (Dinophyceae) culture by small-scale turbulence: A link to toxin production? Harmful Algae 10:88–95, https://doi.org/10.1016/j.hal.2011.08.003.

Berdalet, E., M.A. McManus, O.N. Ross, H. Burchard, F.P. Chavez, J.S. Jaffe, I.R. Jenkinson, R. Kudela, I. Lips, U. Lips, and others. 2014. Understanding harmful algae in stratified systems: Review of progress and future directions. Deep Sea Research Part II 101:4–20, https://doi.org/10.1016/​j.dsr2.2013.09.042.

Bouwman, L., A. Beusen, P.M. Glibert, C. Overbeek, M. Pawlowski, J. Herrera, S. Mulsow, R. Yu, and M. Zhou. 2013. Mariculture: Significant and expanding cause of coastal nutrient enrichment. Environmental Research Letters 8:044026, https://doi.org/10.1088/1748-9326/8/4/044026.

Bravo, I., and R. Figueroa. 2014. Towards an ecological understanding of dinoflagellate cyst functions. Microorganisms 2:11–32, https://doi.org/10.3390/microorganisms2010011.

Brosnahan, M.L., L. Velo-Suárez, D.K. Ralston, S.E. Fox, T.R. Sehein, A. Shalapyonok, H.M. Sosik, R.J. Olson, and D.M. Anderson. 2015. Rapid growth and concerted sexual transitions by a bloom of the harmful dinoflagellate Alexandrium fundyense (Dinophyceae). Limnology and Oceanography 60:2,059–2,078, https://doi.org/​10.1002/lno.10155.

Campbell, L., R.J. Olson, H.M. Sosik, A. Abraham, D.W. Henrichs, C.J. Hyatt, and E.J. Buskey. 2010. First harmful Dinophysis (Dinophyceae, Dinophysiales) bloom in the U.S. is revealed by automated imaging flow cytometry. Journal of Phycology 46:66–75.

Cembella, A.D., D.A. Ibarra, J. Diogène, and E. Dahl. 2005. Harmful algal blooms and their assessment in fjords and coastal embayments. Oceanography 18(2):158–171, https://doi.org/​10.5670/oceanog.2005.51.

Clement, A., L. Lincoqueo, M. Saldivia, C.G. Brito, F. Muñoz, C. Fernández, F. Pérez, C.P. Maluje, N. Correa, V. Moncada, and G. Contreras. 2016. Exceptional summer conditions and HABs of Pseudochattonella in southern Chile create record impacts on salmon farms. Harmful Algae News 53:1–3.

Collos, Y., C. Jauzein, W. Ratmaya, P. Souchu, E. Abadie, and A. Vaquer. 2014. Comparing diatom and Alexandrium catenella/tamarense blooms in Thau lagoon: Importance of dissolved organic nitrogen in seasonally N-limited systems. Harmful Algae 37:84–91, https://doi.org/10.1016/​j.hal.2014.05.008.

Cosgrove, S., A. Ní Rathaille, and R. Raine. 2014. The influence of bloom intensity on the encystment rate and persistence of Alexandrium minutum in Cork Harbor, Ireland. Harmful Algae 31:114–124, https://doi.org/10.1016/j.hal.2013.10.015.

Crespo, B.G., B.A. Keafer, D.K. Ralston, H. Lind, F. Dawson, and D.M. Anderson. 2011. Dynamics of Alexandrium fundyense blooms and shellfish toxicity in the Nauset Marsh System of Cape Cod (Massachusetts, USA). Harmful Algae 12:26–38, https://doi.org/10.1016/j.hal.2011.08.009.

Davidson, K., R.J. Gowen, P. Tett, E. Bresnan, P.J. Harrison, A. McKinney, S. Milligan, D.K. Mills, J. Silke, and A.M. Crooks. 2012. Harmful algal blooms: How strong is the evidence that nutrient ratios and forms influence their occurrence? Estuarine Coastal and Shelf Science 115:399–413, https://doi.org/10.1016/j.ecss.2012.09.019.

Dekshenieks, M.M., P.L. Donaghay, J.M. Sullivan, J.E.B. Rines, T.R. Osborn, and M.S. Twardowski. 2001. Temporal and spatial occurrence of thin phytoplankton layers in relation to physical processes. Marine Ecology Progress Series 223:61–71, https://doi.org/10.3354/meps223061

Díaz, P.A., C. Molinet, M. Seguel, M. Díaz, G. Labra, and R.I. Figueroa. 2014a. Coupling planktonic and benthic shifts during a bloom of Alexandrium catenella in Southern Chile: Implications for bloom dynamics and recurrence. Harmful Algae 40:9–22, https://doi.org/10.1016/j.hal.2014.10.001.

Díaz, P.A., M. Ruiz-Villarreal, L. Velo-Suárez, I. Ramilo, P. Gentien, M. Lunven, L. Fernand, R. Raine, and B. Reguera. 2014b. Tidal and wind-event variability and the distribution of two groups of Pseudo-nitzschia species in an upwelling-influenced ría. Deep Sea Research Part II 101:163–179, https://doi.org/10.1016/j.dsr2.2013.09.043.

Durham, W.M., J.O. Kessler, and R. Stocker. 2009. Disruption of vertical motility by shear triggers formation of thin phytoplankton layers. Science 323:1,067–1,070, https://doi.org/10.1126/science.1167334.

Elferink, S., S. Neuhaus, S. Wohlrab, K. Toebe, D. Voß, M. Gottsching, N. Lundholm, B. Krock, B.P. Koch, O. Zielinski, and others. 2016. Molecular diversity patterns among various phytoplankton size-​fractions in West Greenland in late summer. Deep Sea Research Part I 121:54–69, https://doi.org/​10.1016/​j.dsr.2016.11.002.

Escalera, L., Y. Pazos, M.D. Doval, and B. Reguera. 2012. A comparison of integrated and discrete depth sampling for monitoring toxic species of Dinophysis. Marine Pollution Bulletin 64:106–113, https://doi.org/10.1016/j.marpolbul.2011.10.015.

Estrada, M., J. Solé, S. Anglès, and E. Garcés. 2010. The role of resting cysts in Alexandrium minutum population dynamics. Deep Sea Research Part II 57:308–321, https://doi.org/10.1016/​j.dsr2.2009.09.007.

Farrell, H., P. Gentien, L. Fernand, M. Lunven, B. Reguera, S. González-Gil, and R. Raine. 2012. Scales characterising a high density thin layer of Dinophysis acuta Ehrenberg and its transport within a coastal jet. Harmful Algae 15:36–46, https://doi.org/10.1016/j.hal.2011.11.003.

Fernández-Tejedor, M., L.M. Elandaloussi, E. Mallat, E. Cañete, A. Caillaud, P. Riobó, B. Paz, J. Franco, D. Ibarra, A.D. Cembella, and others. 2008. The Ebro Delta coastal embayments, a GEOHAB pilot site for the study of HAB population dynamics. Pp. 114–116 in Proceedings of the 12th International Conference on Harmful Algae. Ø. Moestrup, chief ed., ISSHA and IOC-UNESCO, Copenhagen, Denmark.

Fistarol, G.O., C. Legrand, K. Rengefors, and E. Graneli. 2004. Temporary cyst formation in phytoplankton: A response to allelopathic competitors? Environmental Microbiology 6:791–798, https://doi.org/10.1111/j.1462-2920.2004.00609.x.

Foloni-Neto, H., R. Lueck, Y. Mabuchi, H. Nakamura, M. Arima, and H. Yamazaki. 2014. A new quasi-​horizontal glider to measure biophysical microstructure. Journal of Atmospheric and Oceanic Technology, 31:2,278–2,293, https://doi.org/10.1175/JTECH-D-13-00240.1.

Gentien, P., P. Donaghay, H. Yamazaki, R. Raine, B. Reguera, and T. Osborn. 2005. Harmful algal blooms in stratified environments. Oceanography 18(2):172–183, https://doi.org/​10.5670/oceanog.2005.52.

Gentien, P., M. Lunven, P. Lazure, A. Youenou, and M.P. Crassous. 2007. Motility and autotoxicity in Karenia mikimotoi (Dinophyceae). Philosophical Transactions of the Royal Society B 362:1,937–1,946, https://doi.org/​10.1098/rstb.2007.2079.

GEOHAB. 2008. Global Ecology and Oceanography of Harmful Algal Blooms, GEOHAB Core Research Project: HABs in Stratified Systems. SCOR and IOC, Paris, France, and Newark, Delaware, USA, 59 pp. 

GEOHAB. 2010. Global Ecology and Oceanography of Harmful Algal Blooms, GEOHAB Core Research Project: HABs in Fjords and Coastal Embayments. A. Cembella, L. Guzmán, S. Roy, J. Diogène, eds, IOC and SCOR, Paris, France, and Newark, Delaware, 57 pp. 

GEOHAB. 2011. GEOHAB Modelling: A Workshop Report. D.J. McGillicuddy Jr., P.M. Glibert, E. Berdalet, C. Edwards, P. Franks, and O. Ross, eds, IOC and SCOR, Paris and Newark, Delaware, 85 pp. 

GEOHAB. 2013. 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. S. Roy, V. Pospelova, M. Montresor, and A. Cembella, eds, IOC and SCOR, Paris, France, and Newark, Delaware, USA, 52 pp.

Glibert, P.M., and M.A. Burford. 2017. Globally changing nutrient loads and harmful algal blooms: Recent advances, new paradigms, and continuing challenges. Oceanography 30(1):58–69, https://doi.org/10.5670/oceanog.2017.110.

Gobler, C.J., and W.G. Sunda. 2012. Ecosystem disruptive algal blooms of the brown tide species, Aureococcus anophagefferens and Aureoumbra lagunensis. Harmful Algae 14:36-45, https://doi.org/​10.1016/j.hal.2011.10.013.

Hallegraeff, G.M. 2010. Ocean climate change, phytoplankton community responses, and harmful algal blooms: A formidable predictive challenge. Journal of Phycology 46:220–235, https://doi.org/10.1111/j.1529-8817.2010.00815.x.

Haury, L.R., J.A. McGowan, and P.H. Wiebe. 1978. Patterns and processes in the time-space scales of plankton distribution. Pp. 277–327 in Spatial Pattern in Plankton Communities. J.H. Steele, ed., Plenum, Springer Science, New York.

Hernández, C., P.A. Díaz, C. Molinet, and M. Seguel. 2016. Exceptional climate anomalies and northwards expansion of paralytic shellfish poisoning outbreaks in southern Chile. Harmful Algae News 54:1–2.

Ianora, A., M.G. Bentley, G.S. Caldwell, R. Cassotti, A.D. Cembella, J. Engström-Öst, C. Halsband, E. Sonneschein, C. Legrand, C.A. Llewellyn, and others. 2011. The relevance of marine chemical ecology to plankton and ecosystem function: An emerging field. Marine Drugs 9:1,625–1,648, https://doi.org/10.3390/md9091625.

IMO (International Maritime Organization). 2017. International Convention for the Control and Management of Ships’ Ballast Water and Sediments (BMW). http://www.imo.org/en/About/Conventions/ListOfConventions/Pages/International-Convention-for-the-Control-and-Management-of-Ships’-Ballast-Water-and-Sediments-(BWM).aspx.

Jenkinson, I.R., E. Berdalet, W.-C. Chin, S. Herminghaus, S. Leterme, J.G. Mitchell, M. Orchard, R. Qiu, L. Seuront, P. Wang, and others. 2015. Micro- and nano-fluidics around HAB cells. Pp. 171–174 in Marine and Fresh-Water Harmful Algae: Proceedings of the 16th International Conference on Harmful Algae, Wellington, New Zealand 27th-31st October 2014. L. MacKenzie, ed, Cawthron Institute, Nelson, New Zealand, and International Society for the Study of Harmful Algae (ISSHA).

Jenkinson, I.R., and J. Sun. 2010. Rheological properties of natural waters with regard to plankton thin layers: A short review. Journal of Marine Systems 83:287–297, https://doi.org/10.1016/​j.jmarsys.2010.04.004.

Jessup, D.A., M.A. Miller, J.P. Ryan, H.M. Nevins, H.A. Kerkering, A. Mekebri, D.B. Crane, T.A. Johnson, and R.M. Kudela. 2009. Mass stranding of marine birds caused by a surfactant-​producing red tide. PLoS ONE 4:e4550, https://doi.org/10.1371/journal.pone.0004550.

Kiørboe, T. 2010. How zooplankton feed: Mechanisms, traits and trade-offs. Biological Review 86:311–339, https://doi.org/​10.1111/j.1469-185X.2010.00148.x.

Kremp, A. 2013. Diversity of dinoflagellate life cycles: Facets and implications of complex strategies. Pp. 197–205 in Biological and Geological Perspectives of Dinoflagellates. J.M. Lewis, F. Marret and L. Bradley, eds, The Micropalaeontological Society, Special Publications, Geological Society, London. 

Lasker, R. 1978. Fishing for anchovies off California. Marine Pollution Bulletin 9:320–321, https://doi.org/​10.1016/0025-326X(78)90240-0.

Le Gac, M., G. Metegnier, N. Chomerat, P. Malestroit, J. Quere, O. Bouchez, R. Siano, C. Destombe, L. Guillou, and A. Chapelle. 2016. Evolutionary processes and cellular functions underlying divergence in Alexandrium minutum. Molecular Ecology 25:5,129–5,143, https://doi.org/10.1111/mec.13815.

Llebot, C., J. Solé, M. Delgado, M. Fernández-Tejedor, J. Camp, and M. Estrada. 2011. Hydrographical forcing and phytoplankton variability in two semi-enclosed estuarine bays. Journal of Marine Systems 86:69–86, https://doi.org/10.1016/​j.jmarsys.2011.01.004.

Lundholm, N., M. Ellegaard, and A. Clarke. 2010. A 100-year record of changing Pseudo-nitzschia species in Denmark related to nitrogen loading and temperature. Harmful Algae 9:449–457, https://doi.org/10.1016/j.hal.2010.03.001.

Lunven, M., J.F. Guillaud, A. Youenou, M.P. Crassous, R. Berric, E. Le Gall, R. Kerouel, C. Labry, and A. Aminot. 2005. Nutrient and phytoplankton distribution in the Loire River plume (Bay of Biscay, France) resolved by a new Fine Scale Sampler. Estuarine, Coastal and Shelf Science 65:94–108, https://doi.org/10.1016/j.ecss.2005.06.001.

Masunaga, E., and H. Yamazaki. 2014. A new tow-yo instrument to observe high-resolution coastal phenomena. Journal of Marine Systems 129:425–436. https://doi.org/10.1016/j.jmarsys.2013.09.005.

McGillicuddy, D.J. Jr., D.W. Townsend, R. He, B.A. Keafer, J.L. Kleindinst, Y. Li, J.P. Manning, D.G. Mountain, M.A. Thomas, and D.M. Anderson. 2011. Suppression of the 2010 Alexandrium fundyense bloom by changes in physical, biological, and chemical properties of the Gulf of Maine. Limnology and Oceanography 56:2,411–2,426, https://doi.org/10.4319/lo.2011.56.6.2411.

McManus, M.A., A.L. Alldredge, A. Barnard, E. Boss, J. Case, T.J. Cowles, P.L. Donaghay, L. Eisner, D.J. Gifford, C.F. Greenlaw, and others. 2003. Changes in characteristics, distribution and persistence of thin layers over a 48-hour period. Marine Ecology Progress Series 261:1–19.

Montresor, M., C. Di Prisco, D. Sarno, F. Margiotta, and A. Zingone. 2013. Diversity and germination patterns of diatom resting stages at a coastal Mediterranean site. Marine Ecology Progress Series 484:79–95, https://doi.org/10.3354/meps10236.

Montresor, M., L. Vitale, D. D’Alelio, and M.I. Ferrante. 2016. Sex in marine planktonic diatoms: Insights and challenges. Progress in Phycological Research 3:61–75, https://doi.org/10.1127/pip/​2016/0045.

Ní Rathaille, A., and R. Raine. 2011. Seasonality in the excystment of Alexandrium minutum and Alexandrium tamarense in Irish coastal waters. Harmful Algae 10:629–635, https://doi.org/10.1016/​j.hal.2011.04.015.

Onda, D.F.L., A.O. Lluisma, and R.V. Azanza. 2014. Development, morphological characteristics and viability of temporary cysts of Pyrodinium bahamense var. compressum (Dinophyceae) in vitro. European Journal of Phycology 49:265–275, https://doi.org/10.1080/09670262.2014.915062.

Persson, A., B.C. Smith, G.H. Wikfors, and J.H. Alix. 2013. Differences in swimming patterns between life cycle stages of the toxic dinoflagellates Alexandrium fundyense. Harmful Algae 21–22:36–43, https://doi.org/10.1016/​j.hal.2012.11.005.

Pitcher, G.C., A.B. Jiménez, R.M. Kudela, and B. Reguera. 2017. Harmful algal blooms in eastern boundary upwelling systems: A GEOHAB Core Research Project. Oceanography 30(1):22–35, https://doi.org/10.5670/oceanog.2017.107.

Pizarro, G., B. Paz, S. González-Gil, J.M. Franco, and B. Reguera. 2009. Seasonal variability of lipophilic toxins during a Dinophysis acuta bloom in western Iberia: Differences between picked cells and plankton concentrates. Harmful Algae 8:926–937, https://doi.org/10.1016/j.hal.2009.05.004.

Raine, R. 2014. A review of the biophysical interactions relevant to the promotion of HABs in stratified systems: The case study of Ireland. Deep Sea Research Part II 101:21–31, https://doi.org/10.1016/​j.dsr2.2013.06.021.

Raine, R., G. McDermott, J. Silke, K. Lyons, G. Nolan, and C. Cusack. 2010. A simple short range model for the prediction of harmful algal events in the bays of southwestern Ireland. Journal of Marine Systems 83:150–157, https://doi.org/10.1016/​j.jmarsys.2010.05.001.

Ralston, D.K., B.A. Keafer, M.L. Brosnahan, and D.M. Anderson. 2014. Temperature dependence of an estuarine harmful algal bloom: Resolving interannual variability in bloom dynamics using a degree-day approach. Limnology and Oceanography 59:1,112–1,126, https://doi.org/​10.4319/lo.2014.59.4.1112.

Rengefors, K., A. Kremp, T.B.H. Reusch, and A.M. Wood. 2017. Genetic diversity and evolution in eukaryotic phytoplankton: Revelations from population genetic studies. Journal of Plankton Research, https://doi.org/10.1093/plankt/fbw098.

Reguera, B., L. Velo-Suárez, R. Raine, and M.G. Park. 2012. Harmful Dinophysis species: A review. Harmful Algae 14:87–106, https://doi.org/10.1016/​j.hal.2011.10.016.

Richlen, M.L., D.L. Erdner, L.A.R. McCauley, K. Libera, and D.M. Anderson. 2012. Extensive genetic diversity and rapid population differentiation during blooms of Alexandrium fundyense (Dinophyceae) in an isolated salt pond on Cape Cod, MA, USA. Ecology and Evolution 2:2,583–2,594, https://doi.org/10.1002/ece3.373.

Rines, J.E.B., P.L. Donaghay, M.M. Dekshenieks, J.M. Sullivan, and M.S. Twardowski. 2002. Thin layers and camouflage: Hidden Pseudo-nitzschia spp. (Bacillariophyceae) populations in a fjord in the San Juan Islands, Washington, USA. Marine Ecology Progress Series 225:123–137.

Rodellas, V., J. García-Orellana, G. Tezzi, E. Berdalet, and P. Masqué. 2017. Using the radium quartet to distinguish groundwater discharge: Fresh groundwater vs. seawater recirculation through sediments. Geochimica Cosmochimica Acta 196:58–73, https://doi.org/10.1016/j.gca.2016.09.016.

Roy, S., M. Parenteau, O. Casas-Monroy, and A. Rochon. 2012. Coastal ship traffic: A significant introduction vector for potentially harmful dinoflagellates in eastern Canada. Canadian Journal of Fisheries and Aquatic Sciences 69:627–644, https://doi.org/10.1139/f2012-008.

Ryan, J.P., M.A. McManus, J.D. Paduan, and F.P. Chavez. 2008. Phytoplankton thin layers caused by shear in frontal zones of a coastal upwelling system. Marine Ecology Progress Series 354:21–34, https://doi.org/10.3354/meps07222.

Ryan, J.P., M.A. McManus, and J.M. Sullivan. 2010. Interacting physical, chemical and biological forcing of phytoplankton thin-layer variability in Monterey Bay, California. Continental Shelf Research 30:7–16, https://doi.org/10.1016/​j.csr.2009.10.017.

Selander, S., J. Kubanek, M. Hamberg, M.X. Andersson, G. Cervin, and H. Pavia. 2015. Predator lipids induce paralytic shellfish toxins in bloom-forming algae. Proceedings of the Natural Academy of Sciences of the United States of America 112(20):6,395–6,400, https://doi.org/​10.1073/pnas.1420154112.

Smith, B.C., and A. Persson. 2005. Synchronization of encystment of Scrippsiella lachrymosa (Dinophyta). Journal of Applied Phycology 17:317–321, https://doi.org/10.1007/s10811-005-4944-6.

Steinbuck, J.V., M.T. Stacey, M.A. McManus, O.M. Cheriton, and J.P. Ryan. 2009. Observations of turbulent mixing in a phytoplankton thin layer: Implications for formation, maintenance, and breakdown. Limnology and Oceanography 544:1,353–1,368, https://doi.org/​10.4319/lo.2009.54.4.1353.

Timmerman, A.H.V., M.A. McManus, O.M. Cheriton, R.K. Cowen, A.T. Greer, R.M. Kudela, K. Ruttenberg, and J. Sevadjian. 2014. Hidden thin layers of toxic diatoms in a coastal bay. Deep Sea Research Part II 101:129–140, https://doi.org/10.1016/​j.dsr2.2013.05.030.

Trainer, V.L., B.M. Hickey, and R. Homer. 2002. Biological and physical dynamics of domoic acid production off the Washington coast. Limnology and Oceanography 47:1,438–1,446, https://doi.org/10.4319/lo.2002.47.5.1438.

Velo-Suárez, L., S. González-Gil, P. Gentien, M. Lunven, C. Bechemin, L. Fernand, R. Raine and B. Reguera. 2008. Thin layers of Pseudo-nitzschia spp. and the fate of Dinophysis acuminata during an upwelling-downwelling cycle in a Galician Ría. Limnology and Oceanography 53:1,816–1,834, https://doi.org/10.4319/lo.2008.53.5.1816.

Wells, M.L., V.L. Trainer, T.J. Smayda, B.S.O. Karlson, C.G. Trick, R.M. Kudela, A. Ishikawa, S. Bernard, A. Wulff, D.M. Anderson, and W.P. Cochlan. 2015. Harmful algal blooms and climate change: Learning from the past and present to forecast the future. Harmful Algae 49:68–93, https://doi.org/10.1016/​j.hal.2015.07.009.

Wyatt, T., and I.R. Jenkinson. 1997. Notes on Alexandrium population dynamics. Journal of Plankton Research 19:551–575, https://doi.org/​10.1093/plankt/19.5.551.

Wohlrab, S., M.H. Iversen, and U. John. 2010. A molecular and co-evolutionary context for grazer induced toxin production in Alexandrium tamarense. PLoS ONE 5(11):e15039, https://doi.org/​10.1371/​journal.pone.0015039

Wohlrab, S., U. Tillmann, A. Cembella, and U. John. 2016. Trait changes induced by species interactions in two phenotypically distinct strains of a marine dinoflagellate. International Society for Microbial Ecology Journal 10:2,658–2,668, https://doi.org/10.1038/ismej.2016.57.

Xie, H., P. Lazure, and P. Gentien. 2007. Small scale retentive structures and Dinophysis. Journal of Marine Systems 64:173–188, https://doi.org/​10.1016/j.jmarsys.2006.03.008.

Yamazaki, H., H. Honma, T. Nagai, M.J. Doubell, K. Amakasu, and M. Kumagai. 2010. Multilayer structure and mixing in the upper water column of Lake Biwa during summer 2008. Limnology 11:63–70, https://doi.org/10.1007/s10201-009-0288-2.

Yamazaki, H., C. Locke, L. Umlauf, H. Burchard, T. Ishimaru, and D. Kamykowski. 2014. A Lagrangian model for phototaxis-induced thin layer formation. Deep Sea Research Part II 101:193–206, https://doi.org/10.1016/j.dsr2.2012.12.010.

Copyright & Usage

This is an open access article made available under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution, and reproduction in any medium or format as long as users cite the materials appropriately, provide a link to the Creative Commons license, and indicate the changes that were made to the original content. Images, animations, videos, or other third-party material used in articles are included in the Creative Commons license unless indicated otherwise in a credit line to the material. If the material is not included in the article’s Creative Commons license, users will need to obtain permission directly from the license holder to reproduce the material.