Patterns and ecological implications of historical marine phytoplankton change

There is growing evidence that average global phytoplankton concentrations have been changing over the past century, yet published trajectories of change are highly divergent. Here, we review and analyze 115 published phytoplankton trend estimates originating from a wide variety of sampling instruments to explore the underlying patterns and ecological implica- tions of phytoplankton change over the period of oceanographic measurement (1889 to 2010). We found that published estimates of phytoplankton change were much less variable when estimated over longer time series and consistent spatial scales and from the same sampling instruments. Average phytoplankton concentrations tended to increase over time in near-shore waters and over more recent time periods and declined in the open oceans and over longer time periods. Most published evidence suggests changes in temperature and nutrient supply rates as leading causes of these phytoplankton trends. In near-shore waters, altered coastal runoff and increased nutrient flux from land may primarily explain widespread increases in phytoplankton there. Conversely, in the open oceans, increasing surface temperatures are strengthening water column stratification, reducing nutrient flux from deeper waters and negatively influencing phytoplankton. Phytoplank- ton change is further affected by biological processes, such as changes in grazing regimes and nutrient cycling, but these effects are less well studied at large scales. The possible ecosystem consequences of observed phytoplankton changes include altered species composition and abun- dance across multiple trophic levels, effects on fisheries yield, and changing patterns of export production. We conclude that there is evidence for substantial changes in phytoplankton concen- tration over the past century, but the magnitude of these changes remains uncertain at a global scale; standardized long-term measurements of phytoplankton abundance over time can substan- tially reduce this uncertainty.

[1]  A. Sournia,et al.  The comparative estimation of phytoplanktonic, microphytobenthic and macrophytobenthic primary production in the oceans , 1990 .

[2]  Hans Joachim Schellnhuber,et al.  Declining ocean chlorophyll under unabated anthropogenic CO2 emissions , 2011 .

[3]  R. Bidigare,et al.  Is there a decline in marine phytoplankton? , 2011, Nature.

[4]  Jae S. Choi,et al.  Trophic Cascades in a Formerly Cod-Dominated Ecosystem , 2005, Science.

[5]  David S. Fox,et al.  Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northeast Pacific , 2004, Nature.

[6]  R. Betts,et al.  Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model , 2000, Nature.

[7]  F. Azam,et al.  Microbes, Molecules, and Marine Ecosystems , 2004, Science.

[8]  D. Montagnes,et al.  Protists decrease in size linearly with temperature: ca. 2.5% °C−1 , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[9]  K. Wirtz Mechanistic origins of variability in phytoplankton dynamics: Part I: niche formation revealed by a size-based model , 2013 .

[10]  N. Bond,et al.  Climate projections for selected large marine ecosystems , 2010 .

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

[12]  Noel A Cressie,et al.  Statistics for Spatial Data. , 1992 .

[13]  Martin Edwards,et al.  From plankton to top predators: bottom-up control of a marine food web across four trophic levels. , 2006, The Journal of animal ecology.

[14]  R. Bidigare,et al.  Long-term changes in plankton community structure and productivity in the North Pacific Subtropical Gyre: The domain shift hypothesis , 2001 .

[15]  Paul G. Falkowski,et al.  The role of nutricline depth in regulating the ocean carbon cycle , 2008, Proceedings of the National Academy of Sciences.

[16]  E. Barbier,et al.  Response to Comments on "Impacts of Biodiversity Loss on Ocean Ecosystem Services" , 2007, Science.

[17]  P. Reich,et al.  Impacts of Biodiversity Loss Escalate Through Time as Redundancy Fades , 2012, Science.

[18]  Stanford B. Hooker,et al.  An overview of the SeaWiFS project and strategies for producing a climate research quality global ocean bio-optical time series , 2004 .

[19]  F. Mélin,et al.  Bottom-up control regulates fisheries production at the scale of eco-regions in European seas , 2007 .

[20]  Paul G. Falkowski,et al.  The Evolution of Modern Eukaryotic Phytoplankton , 2004, Science.

[21]  H. Claustre,et al.  Does chlorophyll a provide the best index of phytoplankton biomass for primary productivity studies , 2007 .

[22]  S. Wood Generalized Additive Models: An Introduction with R , 2006 .

[23]  E. Carmack,et al.  Smallest Algae Thrive As the Arctic Ocean Freshens , 2009, Science.

[24]  Elaine S. Fileman,et al.  Microbial dynamics during the decline of a spring diatom bloom in the Northeast Atlantic , 2007 .

[25]  R. Margalef Life-forms of phytoplankton as survival alternatives in an unstable environment , 1978 .

[26]  F. D’Ortenzio,et al.  Phenological changes of oceanic phytoplankton in the 1980s and 2000s as revealed by remotely sensed ocean‐color observations , 2012 .

[27]  D. Ware,et al.  Bottom-Up Ecosystem Trophic Dynamics Determine Fish Production in the Northeast Pacific , 2005, Science.

[28]  R. Iverson,et al.  Control of marine fish production , 1990 .

[29]  G. Vermeij Shifting sources of productivity in the coastal marine tropics during the Cenozoic era , 2011, Proceedings of the Royal Society B: Biological Sciences.

[30]  Dennis P. Swaney,et al.  Regional nitrogen budgets and riverine N & P fluxes for the drainages to the North Atlantic Ocean: Natural and human influences , 1996 .

[31]  H. Schellnhuber,et al.  Decomposing the effects of ocean warming on chlorophyll a concentrations into physically and biologically driven contributions , 2013 .

[32]  Andreas Oschlies,et al.  Eddy-induced enhancement of primary production in a model of the North Atlantic Ocean , 1998, Nature.

[33]  P. Falkowski,et al.  Phytoplankton productivity in the North Pacific ocean since 1900 and implications for absorption of anthropogenic CO2 , 1992, Nature.

[34]  J. McCarthy,et al.  The Whale Pump: Marine Mammals Enhance Primary Productivity in a Coastal Basin , 2010, PloS one.

[35]  D. Boyce Patterns and drivers of marine phytoplankton change over the past century , 2013 .

[36]  P. Falkowski,et al.  Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean , 1996, Nature.

[37]  F. D’Ortenzio,et al.  Climate-Driven Basin-Scale Decadal Oscillations of Oceanic Phytoplankton , 2009, Science.

[38]  D. Atkinson Temperature and organism size-A biological law for ectotherms? Advances in Ecological Research 25: 1 , 1994 .

[39]  Micheli,et al.  Eutrophication, Fisheries, and Consumer-Resource Dynamics in Marine Pelagic Ecosystems. , 1999, Science.

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

[41]  Francisco P Chavez,et al.  Bottom-up and climatic forcing on the worldwide population of leatherback turtles. , 2008, Ecology.

[42]  Gurvan Madec,et al.  Potential impact of climate change on marine export production , 2001 .

[43]  W. R. Fraser,et al.  Effects of sea-ice extent and krill or salp dominance on the Antarctic food web , 1997, Nature.

[44]  R. Evans,et al.  Bridging ocean color observations of the 1980s and 2000s in search of long-term trends , 2005 .

[45]  Xabier Irigoien,et al.  Large mesopelagic fishes biomass and trophic efficiency in the open ocean , 2014, Nature Communications.

[46]  M. Edwards,et al.  A long‐term chlorophyll dataset reveals regime shift in North Sea phytoplankton biomass unconnected to nutrient levels , 2007 .

[47]  D. Cayan,et al.  Climate and Chlorophyll a: Long-Term Trends in the Central North Pacific Ocean , 1987, Science.

[48]  S. Warren,et al.  Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate , 1987, Nature.

[49]  N. Metzl,et al.  Sensitivity of coccolithophores to carbonate chemistry and ocean acidification , 2011, Nature.

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

[51]  George A. Jackson,et al.  Effects of phytoplankton community on production, size, and export of large aggregates: A world‐ocean analysis , 2009 .

[52]  G. Leduc,et al.  Millennial variability and long‐term changes of the diatom production in the eastern equatorial Pacific during the last glacial cycle , 2011 .

[53]  U. Sommer,et al.  Cladocerans versus copepods: the cause of contrasting top–down controls on freshwater and marine phytoplankton , 2006, Oecologia.

[54]  A. Barnston,et al.  Classification, seasonality and persistence of low-frequency atmospheric circulation patterns , 1987 .

[55]  S. Stammerjohn,et al.  Recent Changes in Phytoplankton Communities Associated with Rapid Regional Climate Change Along the Western Antarctic Peninsula , 2009, Science.

[56]  Mike Rees,et al.  5. Statistics for Spatial Data , 1993 .

[57]  B. Worm,et al.  Integrating global chlorophyll data from 1890 to 2010 , 2012 .

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

[59]  Charles R. McClain,et al.  Subtropical Gyre Variability Observed by Ocean Color Satellites , 2004 .

[60]  B. Worm,et al.  Estimating global chlorophyll changes over the past century , 2014 .

[61]  A. Lopez-Urrutia,et al.  Increasing importance of small phytoplankton in a warmer ocean , 2010 .

[62]  S. Agustí,et al.  Dissolved esterase activity as a tracer of phytoplankton lysis: Evidence of high phytoplankton lysis rates in the northwestern Mediterranean , 1998 .

[63]  A. Ridgwell,et al.  Marine Ecosystem Responses to Cenozoic Global Change , 2013, Science.

[64]  Scott C. Doney,et al.  Projected 21st century decrease in marine productivity: a multi-model analysis , 2009 .

[65]  R. Lasker FIELD CRITERIA FOR SURVIVAL OF ANCHOVY LARVAE: THE RELATION BETWEEN INSHORE CHLOROPHYLL MAXIMUM LAYERS AND SUCCESSFUL FIRST FEEDINGI , 2004 .

[66]  Jarrett E. K. Byrnes,et al.  A global synthesis reveals biodiversity loss as a major driver of ecosystem change , 2012, Nature.

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

[68]  Suranjana Saha,et al.  Empirical Orthogonal Teleconnections , 2000 .

[69]  P. Pepin,et al.  Monitoring changes in phytoplankton abundance and composition in the Northwest Atlantic: a comparison of results obtained by continuous plankton recorder sampling and colour satellite imagery , 2010 .

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

[71]  C. Suttle The significance of viruses to mortality in aquatic microbial communities , 1994, Microbial Ecology.

[72]  C. Suttle Marine viruses — major players in the global ecosystem , 2007, Nature Reviews Microbiology.

[73]  Richard J. Geider,et al.  LIGHT AND TEMPERATURE DEPENDENCE OF THE CARBON TO CHLOROPHYLL a RATIO IN MICROALGAE AND CYANOBACTERIA: IMPLICATIONS FOR PHYSIOLOGY AND GROWTH OF PHYTOPLANKTON , 1987 .

[74]  B. Planque,et al.  Calanus and environment in the eastern North Atlantic. 2. Role of the North Atlantic Oscillation on Calanus finmarchicus and C. helgolandicus , 1996 .

[75]  José A. A. De Oliveira,et al.  Predicting marine phytoplankton community size structure from empirical relationships with remotely sensed variables , 2011 .

[76]  N. Aebischer,et al.  Parallel long-term trends across four marine trophic levels and weather , 1990, Nature.

[77]  Scott C. Doney,et al.  Response of ocean ecosystems to climate warming , 2004 .

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

[79]  S. Nixon,et al.  Chapter 16 – NITROGEN IN ESTUARINE AND COASTAL MARINE ECOSYSTEMS , 1983 .

[80]  J. Hjort,et al.  Fluctuations in the Great Fisheries of Northern Europe: Viewed in the Light of Biological Research , 1914 .

[81]  A. C. Redfield The biological control of chemical factors in the environment. , 1960, Science progress.

[82]  B. Worm,et al.  Effects of sea surface warming on marine plankton. , 2014, Ecology letters.

[83]  B. Worm,et al.  Spatial patterns and predictors of trophic control in marine ecosystems. , 2015, Ecology letters.

[84]  E. Maier‐Reimer,et al.  Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms , 2005, Nature.

[85]  K. Frank,et al.  From mice to elephants: overturning the 'one size fits all' paradigm in marine plankton food chains. , 2015, Ecology letters.

[86]  P. Brimblecombe,et al.  Long-term deposit at Rothamsted, southern England , 1980 .

[87]  J. G. Field,et al.  The Ecological Role of Water-Column Microbes in the Sea* , 1983 .

[88]  B. Hicks,et al.  The atmospheric input of trace species to the world ocean , 1991 .

[89]  K. Frank,et al.  Transient dynamics of an altered large marine ecosystem , 2011, Nature.

[90]  X. Álvarez‐Salgado,et al.  Bottom-up control of common octopus Octopus vulgaris in the Galician upwelling system, northeast Atlantic Ocean , 2008 .

[91]  Marcel R. Wernand,et al.  Trends in Ocean Colour and Chlorophyll Concentration from 1889 to 2000, Worldwide , 2013, PloS one.

[92]  James G. Mitchell,et al.  Iron defecation by sperm whales stimulates carbon export in the Southern Ocean , 2010, Proceedings of the Royal Society B: Biological Sciences.

[93]  B. Worm,et al.  Cascading top-down effects of changing oceanic predator abundances. , 2009, The Journal of animal ecology.

[94]  B. Worm,et al.  Global phytoplankton decline over the past century , 2010, Nature.

[95]  Janet W. Campbell,et al.  The relationship between the standing stock of deep-sea macrobenthos and surface production in the western North Atlantic , 2007 .

[96]  G. Vecchi,et al.  Weakening of tropical Pacific atmospheric circulation due to anthropogenic forcing , 2006, Nature.

[97]  Feldman,et al.  Biological and chemical response of the equatorial pacific ocean to the 1997-98 El Nino , 1999, Science.

[98]  Mark Hebblewhite,et al.  Ecological Consequences of Sea-Ice Decline , 2013, Science.

[99]  J. Dower,et al.  Observations of Biologically Generated Turbulence in a Coastal Inlet , 2006, Science.

[100]  Scott C. Doney,et al.  Factors challenging our ability to detect long-term trends in ocean chlorophyll , 2012 .

[101]  J. Randerson,et al.  Primary production of the biosphere: integrating terrestrial and oceanic components , 1998, Science.

[102]  M. Cardinale,et al.  Multi-level trophic cascades in a heavily exploited open marine ecosystem , 2008, Proceedings of the Royal Society B: Biological Sciences.

[103]  P. Falkowski,et al.  Biogeochemical Controls and Feedbacks on Ocean Primary Production , 1998, Science.

[104]  F. Azam,et al.  The Microbial Loop , 2007 .

[105]  E. Achterberg,et al.  Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability , 2009 .

[106]  K. Wirtz Who is eating whom? Morphology and feeding type determine the size relation between planktonic predators and their ideal prey , 2012 .

[107]  S. Palumbi,et al.  Whales Before Whaling in the North Atlantic , 2003, Science.

[108]  Y. Ishida,et al.  Trophic relations in the subarctic North Pacific ecosystem : possible feeding effect from pink salmon , 1997 .

[109]  A Bakun,et al.  Global Climate Change and Intensification of Coastal Ocean Upwelling , 1990, Science.

[110]  K. Tadokoro,et al.  Interannual–interdecadal variations in zooplankton biomass, chlorophyll concentration and physical environment in the subarctic Pacific and Bering Sea , 1997 .

[111]  Michele Scardi,et al.  Challenges of modeling depth‐integrated marine primary productivity over multiple decades: A case study at BATS and HOT , 2010 .

[112]  P. C. Reid,et al.  Plankton effect on cod recruitment in the North Sea , 2003, Nature.

[113]  Francisco P. Chavez,et al.  From Anchovies to Sardines and Back: Multidecadal Change in the Pacific Ocean , 2003, Science.

[114]  Alberto M. Mestas-Nuñez,et al.  The Atlantic Multidecadal Oscillation and its relation to rainfall and river flows in the continental U.S. , 2001 .

[115]  Alan Y. Chiang,et al.  Generalized Additive Models: An Introduction With R , 2007, Technometrics.

[116]  Watson W. Gregg,et al.  Decadal changes in global ocean chlorophyll , 2002 .

[117]  Melanie Abecassis,et al.  Ocean's least productive waters are expanding , 2008 .

[118]  Relazione delle esperienze fatte a bordo della pontificia pirocorvetta l’Immacolata concezione per determinare la trasparenza del mare; Memoria del P. A. Secchi , 1864 .

[119]  Julian Priddle,et al.  Scales of Interaction Between Antarctic Krill and the Environment , 1988 .

[120]  E. K. Pikitch,et al.  Trophic Downgrading of Planet Earth , 2011, Science.

[121]  U. Sommer,et al.  An indoor mesocosm system to study the effect of climate change on the late winter and spring succession of Baltic Sea phyto- and zooplankton , 2006, Oecologia.

[122]  Antonio J. Busalacchi,et al.  Effects of Penetrative Radiation on the Upper Tropical Ocean Circulation , 2002 .

[123]  H. V. D. Dool,et al.  Sensitivity of Teleconnection Patterns to the Sign of Their Primary Action Center , 2003 .

[124]  C. Mora,et al.  Title Biotic and human vulnerability to projected changes in oceanbiogeochemistry over the 21 st century , 2013 .

[125]  Elizabeth T. Borer,et al.  A cross-ecosystem comparison of the strength of trophic cascades , 2002 .

[126]  Andreas Oschlies,et al.  Future changes in climate, ocean circulation, ecosystems, and biogeochemical cycling simulated for a business‐as‐usual CO2 emission scenario until year 4000 AD , 2008 .

[127]  Scott C. Doney,et al.  Detection of anthropogenic climate change in satellite records of ocean chlorophyll and productivity , 2010 .

[128]  Joaquín Tintoré,et al.  Mesoscale vertical motion and the size structure of phytoplankton in the ocean , 2001, Nature.

[129]  Brian M. Hopkinson,et al.  Effect of Ocean Acidification on Iron Availability to Marine Phytoplankton , 2010, Science.

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

[131]  Simon Jennings,et al.  Global patterns in predator-prey size relationships reveal size dependency of trophic transfer efficiency. , 2010, Ecology.

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

[133]  David A. Siegel,et al.  Climate-driven trends in contemporary ocean productivity , 2006, Nature.

[134]  Jae S. Choi,et al.  Reconciling differences in trophic control in mid-latitude marine ecosystems. , 2006, Ecology letters.

[135]  P. Woodworth,et al.  Declines in phytoplankton cell size in the subtropical oceans estimated from satellite remotely-sensed temperature and chlorophyll, 1998–2007 , 2012 .

[136]  F. Chavez,et al.  Ocean variability in relation to living resources during the 1982–83 El Niño , 1986, Nature.

[137]  V. Smetácek,et al.  Whales sustain fisheries: Blue whales stimulate primary production in the Southern Ocean , 2014 .

[138]  Jian-feng He,et al.  Phytoplankton productivity in newly opened waters of the Western Arctic Ocean , 2012 .

[139]  D. Tilman,et al.  Productivity and sustainability influenced by biodiversity in grassland ecosystems , 1996, Nature.

[140]  John P. Dunne,et al.  Projected expansion of the subtropical biome and contraction of the temperate and equatorial upwelling biomes in the North Pacific under global warming , 2011 .

[141]  A. Schmittner Decline of the marine ecosystem caused by a reduction in the Atlantic overturning circulation , 2005, Nature.

[142]  Jef Huisman,et al.  Global biodiversity patterns of marine phytoplankton and zooplankton , 2004, Nature.

[143]  Richard T. Barber,et al.  On the relationship between stratification and primary productivity in the North Atlantic , 2011 .

[144]  T. Jickells,et al.  Nutrient Biogeochemistry of the Coastal Zone , 1998, Science.

[145]  M. Laamanen,et al.  Long-term changes in summer phytoplankton communities of the open northern Baltic Sea , 2007 .

[146]  P. C. Reid,et al.  Extending the SeaWiFS chlorophyll data set back 50 years in the northeast Atlantic , 2005 .

[147]  S. Jacobs,et al.  Freshening of the Ross Sea During the Late 20th Century , 2002, Science.

[148]  J. Gattuso,et al.  Arctic ocean acidification : pelagic ecosystem and biogeochemical responses during a mesocosm study ” , 2013 .

[149]  Kenneth L. Smith,et al.  Connections between climate, food limitation, and carbon cycling in abyssal sediment communities , 2008, Proceedings of the National Academy of Sciences.

[150]  S. Doney,et al.  Modelling regional responses by marine pelagic ecosystems to global climate change , 2002 .

[151]  M. Piehler,et al.  Warming and Resource Availability Shift Food Web Structure and Metabolism , 2009, PLoS biology.

[152]  P. Burkill,et al.  Cascading Effects of the Loss of Apex Predatory Sharks from a Coastal Ocean , 2007 .

[153]  J. Fasullo,et al.  Warming of the Eurasian Landmass Is Making the Arabian Sea More Productive , 2005, Science.

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

[155]  John R. Post,et al.  Trophic Relationships in Freshwater Pelagic Ecosystems , 1986 .

[156]  L. S. Laurent,et al.  Does the marine biosphere mix the ocean , 2006 .

[157]  M. Piehler,et al.  Correction: Warming and Resource Availability Shift Food Web Structure and Metabolism , 2009, PLoS Biology.

[158]  U. Sommer,et al.  The Baltic Sea spring phytoplankton bloom in a changing climate: an experimental approach , 2012 .

[159]  C. McClain,et al.  Recent trends in global ocean chlorophyll , 2005 .

[160]  R. Rosenberg,et al.  Spreading Dead Zones and Consequences for Marine Ecosystems , 2008, Science.

[161]  Olivier Aumont,et al.  Response of diatoms distribution to global warming and potential implications: A global model study , 2005 .

[162]  U. Sommer,et al.  Copepoda – Cladocera – Tunicata: The role of three major mesozooplankton groups in pelagic food webs , 2002, Ecological Research.

[163]  R. Tibshirani,et al.  Generalized additive models for medical research , 1986, Statistical methods in medical research.

[164]  Francisco P Chavez,et al.  Marine primary production in relation to climate variability and change. , 2011, Annual review of marine science.

[165]  Anthony J. Richardson,et al.  Climate Impact on Plankton Ecosystems in the Northeast Atlantic , 2004, Science.

[166]  James H. Brown,et al.  Toward a metabolic theory of ecology , 2004 .

[167]  Toby Tyrrell,et al.  Phytoplankton Calcification in a High-CO2 World , 2008, Science.

[168]  D. H. Cushing,et al.  Plankton Production and Year-class Strength in Fish Populations: an Update of the Match/Mismatch Hypothesis , 1990 .

[169]  Kerry Emanuel,et al.  How ocean color can steer Pacific tropical cyclones , 2010 .

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

[171]  P. K. Bjørnsen,et al.  The size ratio between planktonic predators and their prey , 1994 .

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

[173]  Elena Litchman,et al.  A Global Pattern of Thermal Adaptation in Marine Phytoplankton , 2012, Science.

[174]  Francesca Malfatti,et al.  Microbial structuring of marine ecosystems , 2007, Nature Reviews Microbiology.

[175]  V. Smetácek Are declining Antarctic krill stocks a result of global warming or decimation of the whales , 2006 .

[176]  Helmut Hillebrand,et al.  Consumer effects decline with prey diversity , 2004 .

[177]  Mark D. Ohman,et al.  Multi‐decadal shoaling of the euphotic zone in the southern sector of the California Current System , 2009 .

[178]  C. Duarte Impacts of Global Warming on Polar Ecosystems , 2008 .

[179]  Paul G. Falkowski,et al.  Cell death in planktonic, photosynthetic microorganisms , 2004, Nature Reviews Microbiology.

[180]  Edward J. Carpenter,et al.  Trichodesmium, a Globally Significant Marine Cyanobacterium , 1997 .

[181]  P. Falkowski,et al.  Photosynthetic rates derived from satellite‐based chlorophyll concentration , 1997 .