Resurrecting the ecological underpinnings of ocean plankton blooms.

Nutrient and light conditions control phytoplankton division rates in the surface ocean and, it is commonly believed, dictate when and where high concentrations, or blooms, of plankton occur. Yet after a century of investigation, rates of phytoplankton biomass accumulation show no correlation with cell division rates. Consequently, factors controlling plankton blooms remain highly controversial. In this review, we endorse the view that blooms are not governed by abiotic factors controlling cell division, but rather reflect subtle ecosystem imbalances instigated by climate forcings or food-web shifts. The annual global procession of ocean plankton blooms thus represents a report on the recent history of predator-prey interactions modulated by physical processes that, almost coincidentally, also control surface nutrient inputs.

[1]  T. Braarud,et al.  A Quantitative Study of the Phytoplankton in the Bay of Fundy and the Gulf of Maine (including Observations on Hydrography, Chemistry and Turbidity) , 1935 .

[2]  H. Sverdrup,et al.  On Conditions for the Vernal Blooming of Phytoplankton , 1953 .

[3]  O. Østvedt Zooplankton investigations from weather ship M in the Norwegian Sea, 1948-49 , 1955 .

[4]  E. Nielsen The Balance between Phytoplankton and Zooplankton in the Sea , 1958 .

[5]  D. H. Cushing,et al.  The seasonal variation in oceanic production as a problem in population dynamics , 1959 .

[6]  J. Ryther Photosynthesis and fish production in the sea. , 1969, Science.

[7]  T. Berman,et al.  Quantitative and Qualitative Changes in the Phytoplankton of Lake Kinneret, Israel, 1972-1975 , 1977 .

[8]  A. Longhurst,et al.  Materials for plankton modelling: Vertical distribution of Atlantic zooplankton in summer , 1979 .

[9]  M. Landry Switching between herbivory and carnivory by the planktonic marine copepod Calanus pacificus , 1981 .

[10]  J. M. Colebrook,et al.  Continuous plankton records: seasonal variations in the distribution and abundance of plankton in the North Atlantic Ocean and the North Sea , 1982 .

[11]  R. Wetzel,et al.  Effects of Differential Growth and Mortality in the Seasonal Succession of Phytoplankton Populations in Lawrence Lake, Michigan , 1982 .

[12]  K. Banse Cell volumes, maximal growth rates of unicellular algae and ciliates, and the role of ciliates in the marine pelagial1,2 , 1982 .

[13]  M. Tilzer Estimation of phytoplankton loss rates from daily photosynthetic rates and observed blomass changes in Lake Constance , 1984 .

[14]  D. M. Nelson,et al.  Phytoplankton Bloom Produced by a Receding Ice Edge in the Ross Sea: Spatial Coherence with the Density Field , 1985, Science.

[15]  E. Haugen,et al.  The distribution and abundance of phototrophic ultraplankton in the North Atlantic1,2 , 1985 .

[16]  J. Raven,et al.  GROWTH, PHOTOSYNTHESIS AND MAINTENANCE METABOLIC COST IN THE DIATOM PHAEODACTYLUM TRICORNUTUM AT VERY LOW LIGHT LEVELS 1 , 1986 .

[17]  Sallie W. Chisholm,et al.  Food selection by copepods: discrimination on the basis of food quality , 1988 .

[18]  T. Parsons,et al.  Comparative oceanic ecology of the plankton communities of the subarctic Atlantic and Pacific oceans , 1988 .

[19]  S. Fitzwater,et al.  Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic , 1988, Nature.

[20]  G. Evans A framework for discussing seasonal succession and coexistence of phytoplankton species , 1988 .

[21]  J. Grover INFLUENCE OF CELL SHAPE AND SIZE ON ALGAL COMPETITIVE ABILITY 1 , 1989 .

[22]  W. Broenkow,et al.  Vertex: phytoplankton/iron studies in the Gulf of Alaska , 1989 .

[23]  Curtis A. Suttle,et al.  Infection of phytoplankton by viruses and reduction of primary productivity , 1990, Nature.

[24]  P. Tiselius,et al.  Foraging behaviour of six calanoid copepods: observations and hydrodynamic analysis , 1990 .

[25]  P. Falkowski,et al.  Role of eddy pumping in enhancing primary production in the ocean , 1991, Nature.

[26]  T. Platt,et al.  Critical depth and marine primary production , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  N. Welschmeyer,et al.  Pigment-specific rates of phytoplankton growth and microzooplankton grazing in the open subarctic Pacific Ocean , 1991 .

[28]  K. Banse Grazing, Temporal Changes of Phytoplankton Concentrations, and the Microbial Loop in the Open Sea , 1992 .

[29]  H. Ducklow,et al.  Introduction to the JGOFS North Atlantic bloom experiment , 1993 .

[30]  J. R. Nelson,et al.  Grazing, growth and mortality of microzooplankton during the 1989 North Atlantic spring bloom at 47°N, 18°W , 1993 .

[31]  C. Garside,et al.  The “f-ratio” on 20°W during the North Atlantic Bloom Experiment , 1993 .

[32]  H. Ducklow,et al.  Plankton succession and carbon cycling at 47°N 20°W during the JGOFS North Atlantic Bloom Experiment , 1993 .

[33]  V. Smetácek,et al.  Organism life cycles, predation, and the structure of marine pelagic ecosystems , 1996 .

[34]  Raphael Kudela,et al.  A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean , 1996, Nature.

[35]  M. Viitasalo,et al.  Prey switching behaviour in the planktonic copepod Acartia tonsa , 1996 .

[36]  F. Chai,et al.  Iron and grazing constraints on primary production in the central equatorial Pacific: An EqPac synthesis , 1997 .

[37]  K. Johnson,et al.  The behaviour of iron and other trace elements during the IronEx-I and PlumEx experiments in the Equatorial Pacific , 1998 .

[38]  A. Longhurst Ecological Geography of the Sea , 1998 .

[39]  T. D. Dickey,et al.  Influence of mesoscale eddies on new production in the Sargasso Sea , 1998, Nature.

[40]  Franz J. Weissing,et al.  Critical depth and critical turbulence: Two different mechanisms for the development of phytoplankton blooms , 1999 .

[41]  Elizabeth L. Mann,et al.  Differential response of equatorial Pacific phytoplankton to iron fertilization , 1999 .

[42]  D. Vaulot,et al.  Prochlorococcus growth rates in the central equatorial Pacific: an application of the fmax approach , 1999 .

[43]  Cole,et al.  Trophic cascades revealed in diverse ecosystems. , 1999, Trends in ecology & evolution.

[44]  M. Radenac,et al.  Picophytoplankton dynamics in the equatorial Pacific: Growth and grazing rates from cytometric counts , 1999 .

[45]  M. Cabrini,et al.  The insidious effect of diatoms on copepod reproduction , 1999, Nature.

[46]  Trine Dale,et al.  Seasonal development of phytoplankton at a high latitude oceanic site , 1999 .

[47]  A. Calbet,et al.  Mesozooplankton influences on the microbial food web: Direct and indirect trophic interactions in the oligotrophic open ocean , 1999 .

[48]  R. Bidigare,et al.  Biological response to iron fertilization in the eastern equatorial Pacific (IronEx II). III. Dynamics of phytoplankton growth and microzooplankton grazing , 2000 .

[49]  Andrew J. Watson,et al.  A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization , 2000, Nature.

[50]  S. Strom,et al.  Phytoplankton blooms are strongly impacted by microzooplankton grazing in coastal North Pacific waters , 2001 .

[51]  S. Doney,et al.  An intermediate complexity marine ecosystem model for the global domain , 2001 .

[52]  V. Smetácek,et al.  Status, trends and the future of the marine pelagic ecosystem , 2002, Environmental Conservation.

[53]  D. A. Siegel,et al.  The North Atlantic Spring Phytoplankton Bloom and Sverdrup's Critical Depth Hypothesis , 2002, Science.

[54]  J. Huisman,et al.  How Do Sinking Phytoplankton Species Manage to Persist? , 2002, The American Naturalist.

[55]  J. Nishioka,et al.  A Mesoscale Iron Enrichment in the Western Subarctic Pacific Induces a Large Centric Diatom Bloom , 2003, Science.

[56]  Jan O. Backhaus,et al.  Convection and primary production in winter , 2003 .

[57]  Xiaoping Zhou,et al.  Marine ecology: Spring algal bloom and larval fish survival , 2003, Nature.

[58]  K. Broad,et al.  Environmental ‘loopholes’ and fish population dynamics: comparative pattern recognition with focus on El Niño effects in the Pacific , 2003 .

[59]  T. Kiørboe Population regulation and role of mesozooplankton in shaping marine pelagic food webs , 2004, Hydrobiologia.

[60]  B. Quéguiner,et al.  Availability of iron and major nutrients for phytoplankton in the northeast Atlantic Ocean , 2004 .

[61]  Michael R. Landry,et al.  Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems , 2004 .

[62]  M. Edwards,et al.  Impact of climate change on marine pelagic phenology and trophic mismatch , 2004, Nature.

[63]  K. Banse Steemann Nielsen and the zooplankton , 2002, Hydrobiologia.

[64]  William Miller,et al.  The decline and fate of an iron-induced subarctic phytoplankton bloom , 2004, Nature.

[65]  James H. Brown,et al.  Linking the global carbon cycle to individual metabolism , 2005 .

[66]  Ulf Riebesell,et al.  Synthesis of iron fertilization experiments: From the iron age in the age of enlightenment , 2005 .

[67]  John Marra,et al.  Primary productivity in the Arabian Sea: A synthesis of JGOFS data , 2005 .

[68]  Xabier Irigoien,et al.  Phytoplankton blooms: a ‘loophole’ in microzooplankton grazing impact? , 2005 .

[69]  David A. Siegel,et al.  Carbon‐based ocean productivity and phytoplankton physiology from space , 2005 .

[70]  S. Batten,et al.  Effects on zooplankton of a warmer ocean: Recent evidence from the Northeast Pacific , 2007 .

[71]  C. S. Wong,et al.  Climatological mean and decadal change in surface ocean pCO2, and net seaair CO2 flux over the global oceans , 2009 .

[72]  R. Olson,et al.  A submersible imaging‐in‐flow instrument to analyze nano‐and microplankton: Imaging FlowCytobot , 2007 .

[73]  D. Caron,et al.  Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold waters , 2007 .

[74]  E. Boyle,et al.  Mesoscale Iron Enrichment Experiments 1993-2005: Synthesis and Future Directions , 2007, Science.

[75]  M. Fujii,et al.  Influences of initial plankton biomass and mixed layer depths on the outcome of iron-fertilization experiments , 2007 .

[76]  Sallie W. Chisholm,et al.  Emergent Biogeography of Microbial Communities in a Model Ocean , 2007, Science.

[77]  Joanna J. Waniek,et al.  Phytoplankton growth conditions during autumn and winter in the Irminger Sea, North Atlantic , 2007 .

[78]  Nicholas R. Bates,et al.  Eddy/Wind Interactions Stimulate Extraordinary Mid-Ocean Plankton Blooms , 2007, Science.

[79]  K. Arrigo,et al.  Primary production in the Southern Ocean, 1997–2006 , 2008 .

[80]  S. Blain,et al.  Distribution of dissolved iron during the natural iron-fertilization experiment KEOPS (Kerguelen Plateau, Southern Ocean) , 2008 .

[81]  Tommy D. Dickey,et al.  The transient oasis: Nutrient-phytoplankton dynamics and particle export in Hawaiian lee cyclones , 2008 .

[82]  U. Sommer,et al.  Climate change and the timing, magnitude, and composition of the phytoplankton spring bloom , 2008 .

[83]  Stephen C. Riser,et al.  Observations of pigment and particle distributions in the western North Atlantic from an autonomous float and ocean color satellite , 2008 .

[84]  Á. López-Urrutia The metabolic theory of ecology and algal bloom formation , 2008 .

[85]  M. Behrenfeld,et al.  Evolved physiological responses of phytoplankton to their integrated growth environment , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[86]  J. Karstensen,et al.  The seasonal pCO2 cycle at 49°N/16.5°W in the northeastern Atlantic Ocean and what it tells us about biological productivity , 2008 .

[87]  E. Mauceli,et al.  Viral Glycosphingolipids Induce Lytic Infection and Cell Death in Marine Phytoplankton , 2009 .

[88]  J. Sarmiento,et al.  Decadal variability in North Atlantic phytoplankton blooms , 2009 .

[89]  E. Achterberg,et al.  Iron limitation of the postbloom phytoplankton communities in the Iceland Basin , 2009 .

[90]  C. McClain A decade of satellite ocean color observations. , 2009, Annual review of marine science.

[91]  T. Platt,et al.  Basin-Scale Coherence in Phenology of Shrimps and Phytoplankton in the North Atlantic Ocean , 2009, Science.

[92]  A. Vehmaa,et al.  Development of phytoplankton in Lake Pääjärvi (Finland) during under-ice convective mixing period , 2009, Aquatic Ecology.

[93]  Taro Takahashi,et al.  Skill metrics for confronting global upper ocean ecosystem-biogeochemistry models against field and remote sensing data , 2009 .

[94]  Andrew J. Watson,et al.  Climatological Mean and Decadal Change in Surface Ocean Pco(2), and Net Sea-Air Co2 Flux Over the Global Oceans (Vol 56, Pg 554, 2009) , 2009 .

[95]  Thomas R. Anderson,et al.  Influence of grazing formulations on the emergent properties of a complex ecosystem model in a global ocean general circulation model , 2010 .

[96]  G. Gorsky,et al.  The Underwater Vision Profiler 5: An advanced instrument for high spatial resolution studies of particle size spectra and zooplankton , 2010 .

[97]  M. Behrenfeld,et al.  Abandoning Sverdrup's Critical Depth Hypothesis on phytoplankton blooms. , 2010, Ecology.

[98]  Michael J. Behrenfeld,et al.  In situ evaluation of the initiation of the North Atlantic phytoplankton bloom , 2010 .

[99]  Emmanuel Chassot,et al.  Global marine primary production constrains fisheries catches. , 2010, Ecology letters.

[100]  L. A. Coogan,et al.  Volcanic ash fuels anomalous plankton bloom in subarctic northeast Pacific , 2010 .

[101]  S. Chiswell,et al.  Annual cycles and spring blooms in phytoplankton: don't abandon Sverdrup completely , 2011 .

[102]  Richard Sanders,et al.  Export and mesopelagic particle flux during a North Atlantic spring diatom bloom , 2011 .

[103]  A. Vardi,et al.  A chemical arms race at sea mediates algal host-virus interactions. , 2011, Current opinion in microbiology.

[104]  Autonomous data describe North Atlantic spring bloom , 2011 .

[105]  Craig M. Lee,et al.  High-resolution observations of aggregate flux during a sub-polar North Atlantic spring bloom , 2011 .

[106]  Raffaele Ferrari,et al.  Shutdown of turbulent convection as a new criterion for the onset of spring phytoplankton blooms , 2011 .

[107]  Montégut,et al.  Phytoplankton spring and fall blooms in the North Atlantic in the 1980s and 2000s , 2011 .

[108]  Andreas Oschlies,et al.  Can we predict the direction of marine primary production change under global warming? , 2011 .

[109]  J. R. Taylor,et al.  Ocean fronts trigger high latitude phytoplankton blooms , 2011 .

[110]  M. Kahru,et al.  Are phytoplankton blooms occurring earlier in the Arctic? , 2011 .

[111]  R. Bidigare,et al.  Spatially-resolved taxon-specific phytoplankton production and grazing dynamics in relation to iron distributions in the Equatorial Pacific between 110 and 140°W , 2011 .

[112]  S. Giovannoni,et al.  Seasonality in Ocean Microbial Communities , 2012, Science.

[113]  C. McClain,et al.  The role of phytoplankton dynamics in the seasonal and interannual variability of carbon in the subpolar North Atlantic – a modeling study , 2012 .

[114]  Rick A. Reynolds,et al.  Massive Phytoplankton Blooms Under Arctic Sea Ice , 2012, Science.

[115]  Monika Winder,et al.  Phytoplankton response to a changing climate , 2012, Hydrobiologia.

[116]  Jan Kaiser,et al.  Estimates of net community production and export using high-resolution, Lagrangian measurements of O2, NO3−, and POC through the evolution of a spring diatom bloom in the North Atlantic , 2012 .

[117]  M. Pahlow,et al.  Top-down control of marine phytoplankton diversity in a global ecosystem model , 2012 .

[118]  Craig M. Lee,et al.  Eddy-Driven Stratification Initiates North Atlantic Spring Phytoplankton Blooms , 2012, Science.

[119]  S. Henson,et al.  The impact of global warming on seasonality of ocean primary production , 2013 .

[120]  A. D. Barton,et al.  Control of plankton seasonal succession by adaptive grazing , 2013 .

[121]  T. Moore,et al.  Monsoons, Islands, and Eddies: Their Effects on Phytoplankton in the Indian Ocean , 2013 .

[122]  David A. Siegel,et al.  Annual cycles of ecological disturbance and recovery underlying the subarctic Atlantic spring plankton bloom , 2013 .

[123]  K. Banse Reflections about chance in my career, and on the top-down regulated world. , 2013, Annual review of marine science.

[124]  E. Boss,et al.  Regional to global assessments of phytoplankton dynamics from the SeaWiFS mission , 2013 .

[125]  John S. Parslow,et al.  A model of annual plankton cycles , 2013 .