Primary Production, an Index of Climate Change in the Ocean: Satellite-Based Estimates over Two Decades

Primary production by marine phytoplankton is one of the largest fluxes of carbon on our planet. In the past few decades, considerable progress has been made in estimating global primary production at high spatial and temporal scales by combining in situ measurements of primary production with remote-sensing observations of phytoplankton biomass. One of the major challenges in this approach lies in the assignment of the appropriate model parameters that define the photosynthetic response of phytoplankton to the light field. In the present study, a global database of in situ measurements of photosynthesis versus irradiance (P-I) parameters and a 20-year record of climate quality satellite observations were used to assess global primary production and its variability with seasons and locations as well as between years. In addition, the sensitivity of the computed primary production to potential changes in the photosynthetic response of phytoplankton cells under changing environmental conditions was investigated. Global annual primary production varied from 38.8 to 42.1 Gt C yr−1 over the period of 1998–2018. Inter-annual changes in global primary production did not follow a linear trend, and regional differences in the magnitude and direction of change in primary production were observed. Trends in primary production followed directly from changes in chlorophyll-a and were related to changes in the physico-chemical conditions of the water column due to inter-annual and multidecadal climate oscillations. Moreover, the sensitivity analysis in which P-I parameters were adjusted by ±1 standard deviation showed the importance of accurately assigning photosynthetic parameters in global and regional calculations of primary production. The assimilation number of the P-I curve showed strong relationships with environmental variables such as temperature and had a practically one-to-one relationship with the magnitude of change in primary production. In the future, such empirical relationships could potentially be used for a more dynamic assignment of photosynthetic rates in the estimation of global primary production. Relationships between the initial slope of the P-I curve and environmental variables were more elusive.

[1]  M. Grant,et al.  Assessing the fitness-for-purpose of satellite multi-mission ocean color climate data records: A protocol applied to OC-CCI chlorophyll-a data , 2017, Remote sensing of environment.

[2]  M. F. Macedo,et al.  Annual variation of environmental variables, phytoplankton species composition and photosynthetic parameters in a coastal lagoon , 2001 .

[3]  Andrea Pisano,et al.  The Copernicus Marine Environment Monitoring Service Ocean State Report , 2016 .

[4]  F. Mélin Potentiel de la télédétection pour l'analyse des propriétés optiques du système océan-atmosphère et application à l'estimation de la photosynthèse phytoplanctonique , 2003 .

[5]  R. Bidigare,et al.  Photosynthetic physiology and physicochemical forcing in the Arabian Sea, 1995 , 2002 .

[6]  S. Lohrenz,et al.  Photophysiological and light absorption properties of phytoplankton communities in the river‐dominated margin of the northern Gulf of Mexico , 2017, Journal of geophysical research. Oceans.

[7]  T. Platt,et al.  Impact of El Niño Variability on Oceanic Phytoplankton , 2017, Front. Mar. Sci..

[8]  W. Richard,et al.  TEMPERATURE AND PHYTOPLANKTON GROWTH IN THE SEA , 1972 .

[9]  Craig M. Lee,et al.  A multi-method autonomous assessment of primary productivity and export efficiency in the springtime North Atlantic. , 2018, Biogeosciences.

[10]  Michele Scardi,et al.  Assessing the Uncertainties of Model Estimates of Primary Productivity in the Tropical Pacific Ocean Revised , 2008 .

[11]  David M. Karl,et al.  Seasonal and interannual variability in primary production and particle flux at Station ALOHA , 1996 .

[12]  T. Platt,et al.  Remote sensing of water-column primary production , 2013 .

[13]  T. Platt,et al.  Primary Production Distribution , 2001 .

[14]  Robert J. W. Brewin,et al.  Influence of light in the mixed-layer on the parameters of a three-component model of phytoplankton size class , 2015 .

[15]  T. Platt,et al.  Day‐to‐day variations in the spring‐summer photosynthetic parameters of coastal marine phytoplankton , 1983 .

[16]  R. Bidigare,et al.  Phytoplankton photosynthesis parameters along 140°W in the equatorial Pacific , 1995 .

[17]  Trevor Platt,et al.  Regionally and seasonally differentiated primary production in the North Atlantic , 1995 .

[18]  H. Bouman,et al.  Reconciling models of primary production and photoacclimation [Invited]. , 2020, Applied optics.

[19]  Lizhen Lin,et al.  Photosynthetic parameters in the northern South China Sea in relation to phytoplankton community structure , 2015 .

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

[21]  H. Bouman,et al.  Carbon-to-chlorophyll ratio and growth rate of phytoplankton in the sea , 2009 .

[22]  T. Platt,et al.  Ocean primary production and available light: further algorithms for remote sensing , 1988 .

[23]  R. C. Groman,et al.  The Biological and Chemical Oceanography Data Management Office , 2011 .

[24]  H. Melling,et al.  Observations in the Ocean , 2012 .

[25]  Trevor Platt,et al.  Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton , 1980 .

[26]  T Platt,et al.  Effect of the particle-size distribution on the backscattering ratio in seawater. , 1994, Applied optics.

[27]  M. Vernet,et al.  Primary production throughout austral fall, during a time of decreasing daylength in the western Antarctic Peninsula , 2012 .

[28]  K. Safi,et al.  Size‐fractionated phytoplankton biomass and photosynthesis in Manukau Harbour, New Zealand , 1996 .

[29]  T. Platt,et al.  Nutrient control of phytoplankton photosynthesis in the Western North Atlantic , 1992, Nature.

[30]  T. Platt,et al.  Remote sensing of phytoplankton pigments: A comparison of empirical and theoretical approaches , 2001 .

[31]  D. Nychka,et al.  Consistency of modelled and observed temperature trends in the tropical troposphere , 2008 .

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

[33]  Marcel Babin,et al.  Relationship between photosynthetic parameters and different proxies of phytoplankton biomass in the subtropical ocean , 2007 .

[34]  T. Piatt,et al.  Ocean primary production calculated by spectral and broad-band models , 1992 .

[35]  Trevor Platt,et al.  Estimators of primary production for interpretation of remotely sensed data on ocean color , 1993 .

[36]  J. Forbes,et al.  Determination of photosynthetic capacity in coastal marine phytoplankton: effects of assay irradiance and variability of photosynthetic parameters , 1986 .

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

[38]  R. G. Budd,et al.  Phytoplankton photosynthesis and growth in contrasting regions of Manukau Harbour, New Zealand , 1993 .

[39]  T. Platt,et al.  Primary production by phytoplankton : analytic solutions for daily rates per unit area of water surface , 1990, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[40]  M. Estrada,et al.  Effect of solar UVR on the production of particulate and dissolved organic carbon from phytoplankton assemblages in the Indian Ocean , 2015 .

[41]  T. Platt,et al.  Computation of aquatic primary production: extended formalism to include effect of angular and spectral distribution of light , 1989 .

[42]  S. Menden‐Deuer Structure-dependent phytoplankton photosynthesis and production rates: implications for the formation, maintenance, and decline of plankton patches , 2012 .

[43]  A. D. Barton,et al.  Seasonal to interannual predictability of oceanic net primary production inferred from satellite observations , 2019 .

[44]  G. Daneri,et al.  Primary production and phytoplanktonic biomass in shallow marine environments of central Chile: Effect of coastal geomorphology , 2007 .

[45]  André Morel,et al.  Light scattering and chlorophyll concentration in case 1 waters: A reexamination , 1998 .

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

[47]  Atul K. Jain,et al.  Global Carbon Budget 2018 , 2014, Earth System Science Data.

[48]  I. Yashayaev,et al.  Spring phytoplankton communities of the Labrador Sea (2005–2014): pigment signatures, photophysiology and elemental ratios , 2016 .

[49]  Watson W. Gregg,et al.  Global ocean primary production trends in the modern ocean color satellite record (1998–2015) , 2019, Environmental Research Letters.

[50]  David A. Siegel,et al.  Carbon‐based primary productivity modeling with vertically resolved photoacclimation , 2008 .

[51]  J. Nishioka,et al.  Phytoplankton community responses to iron and CO2 enrichment in different biogeochemical regions of the Southern Ocean , 2017, Polar Biology.

[52]  Lawrence W. Harding,et al.  Phytoplankton production in two east coast estuaries: Photosynthesis-light functions and patterns of carbon assimilation in Chesapeake and Delaware Bays , 1986 .

[53]  H. Bouman,et al.  Operational estimation of primary production at large geographical scales , 2008 .

[54]  K. Arrigo,et al.  Continued increases in Arctic Ocean primary production , 2015 .

[55]  B. Cole,et al.  Significance of biomass and light availability to phytoplankton productivity in San Francisco Bay , 1984 .

[56]  C. Gallegos Phytoplankton photosynthesis, productivity, and species composition in a eutrophic estuary: comparison of bloom and non-bloom assemblages , 1992 .

[57]  T. Fisher,et al.  Photosynthesis patterns in Chesapeake Bay phytoplankton: short- and long-term responses of P-l curve parameters to light , 1985 .

[58]  R. Goericke,et al.  Primary production in the subarctic Pacific Ocean: Project SUPER , 1993 .

[59]  S. Strom,et al.  Light limitation of summer primary production in the coastal Gulf of Alaska: physiological and environmental causes , 2010 .

[60]  K. Richardson,et al.  Constraining the Distribution of Photosynthetic Parameters in the Global Ocean , 2016, Front. Mar. Sci..

[61]  Trevor Platt,et al.  The spectral irradiance field at the surface and in the interior of the ocean: A model for applications in oceanography and remote sensing , 1988 .

[62]  Trevor Platt,et al.  Remote sensing of assimilation number for marine phytoplankton , 2014 .

[63]  Trevor Platt,et al.  Remote sensing of oceanic primary production: computations using a spectral model , 1989 .

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

[65]  S. Strom,et al.  Spring phytoplankton in the eastern coastal Gulf of Alaska: Photosynthesis and production during high and low bloom years , 2016 .

[66]  Trevor Platt,et al.  Mathematical formulation of the relationship between photosynthesis and light for phytoplankton , 1976 .

[67]  R. Goericke,et al.  Phytoplankton growth and herbivory in the subarctic Pacific: A chemotaxonomic analysis , 1991 .

[68]  A. Jassby,et al.  THE RELATIONSHIP BETWEEN PHOTOSYNTHESIS AND LIGHT FOR NATURAL ASSEMBLAGES OF COASTAL MARINE PHYTOPLANKTON 1 , 1976 .

[69]  M. J. Hameedi Changes in specific photosynthetic rate of oceanic phytoplankton from the northeast Pacific Ocean , 1977, Helgoländer wissenschaftliche Meeresuntersuchungen.

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

[71]  P. Pepin,et al.  Photosynthesis–irradiance parameters of marine phytoplankton: synthesis of a global data set , 2017 .

[72]  M. Gall,et al.  Photosynthetic parameters in water masses in the vicinity of the Chatham rise, south pacific ocean, during late summer , 1997 .

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

[74]  T. Platt,et al.  Spatial Structure of Pelagic Ecosystem Processes in the Global Ocean , 1999, Ecosystems.

[75]  D. Antoine,et al.  Oceanic primary production: 2. Estimation at global scale from satellite (Coastal Zone Color Scanner) chlorophyll , 1996 .

[76]  L. Oziel,et al.  The evolution of light and vertical mixing across a phytoplankton ice-edge bloom , 2019, Elementa: Science of the Anthropocene.

[77]  Mati Kahru,et al.  Phytoplankton absorption, photosynthetic parameters, and primary production off Baja California: summer and autumn 1998 , 2004 .

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

[79]  T. Platt,et al.  An estimate of global primary production in the ocean from satellite radiometer data , 1995 .

[80]  P. Holligan,et al.  Photosynthetic parameters of phytoplankton from 50°N to 50°S in the Atlantic Ocean , 1999 .

[81]  Trevor Platt,et al.  Spectral effects in bio-optical control on the ocean system , 2007 .

[82]  T. Platt,et al.  Recovery of photosynthesis parameters from in situ profiles of phytoplankton production , 2016 .

[83]  Karen Evans,et al.  Effects of climate variability on the distribution and fishing conditions of yellowfin tuna (Thunnus albacares) in the western Indian Ocean , 2013, Climatic Change.

[84]  Richard W. Gould,et al.  An Ocean-Colour Time Series for Use in Climate Studies: The Experience of the Ocean-Colour Climate Change Initiative (OC-CCI) , 2019, Sensors.

[85]  T. Platt,et al.  Absorption and photosynthetic action spectra for natural phytoplankton populations: Implications for production in the open ocean1 , 1985 .

[86]  Michele Scardi,et al.  A comparison of global estimates of marine primary production from ocean color , 2006 .

[87]  C. Gallegos,et al.  An incubation procedure for estimating carbon-to-chlorophyll ratios and growth-irradiance relationships of estuarine phytoplankton , 1996 .

[88]  F. Chai,et al.  Primary productivity and its regulation in the equatorial Pacific during and following the 1991–1992 El Niño , 1996 .

[89]  Y. Huot,et al.  Photosynthetic parameters in the Beaufort Sea in relation to the phytoplankton community structure , 2013 .

[90]  Stewart J. Cohen,et al.  Climate Change 2014: Impacts,Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change , 2014 .

[91]  H. Kao,et al.  Contrasting Eastern-Pacific and Central-Pacific Types of ENSO , 2009 .

[92]  H. Bouman,et al.  Size Class Dependent Relationships between Temperature and Phytoplankton Photosynthesis-Irradiance Parameters in the Atlantic Ocean , 2018, Front. Mar. Sci..

[93]  P. Boyd,et al.  Predicting rates of primary production in the vicinity of the Subtropical Convergence east of New Zealand , 1999 .

[94]  H. Bouman,et al.  Dependence of light-saturated photosynthesis on temperature and community structure , 2005 .

[95]  W. Thomas ON NITROGEN DEFICIENCY IN TROPICAL PACIFIC OCEANIC PHYTOPLANKTON: PHOTOSYNTHETIC PARAMETERS IN POOR AND RICH WATER1 , 1970 .

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

[97]  S. Sathyendranath,et al.  Model of phytoplankton absorption based on three size classes. , 2011, Applied optics.

[98]  T. Platt,et al.  Biological production models as elements of coupled, atmosphere-ocean models for climate research , 1991 .

[99]  Dariusz Stramski,et al.  Phytoplankton class‐specific primary production in the world's oceans: Seasonal and interannual variability from satellite observations , 2010 .

[100]  T. Platt,et al.  Oceanic Primary Production: Estimation by Remote Sensing at Local and Regional Scales , 1988, Science.

[101]  Gavin H. Tilstone,et al.  Accuracy Assessment of Primary Production Models with and without Photoinhibition Using Ocean-Colour Climate Change Initiative Data in the North East Atlantic Ocean , 2018, Remote. Sens..

[102]  James C. McWilliams,et al.  North Pacific Gyre Oscillation links ocean climate and ecosystem change , 2008 .

[103]  M. Gibbs,et al.  Seasonal changes in factors controlling phytoplankton growth in Beatrix Bay, New Zealand , 1997 .

[104]  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 .

[105]  N. Garcia,et al.  Environmental factors influencing the seasonal dynamics of spring algal blooms in and beneath sea ice in western Baffin Bay , 2019, Elementa: Science of the Anthropocene.

[106]  Marcel Babin,et al.  Relating phytoplankton photophysiological properties to community structure on large scales , 2008 .

[107]  Corinne Le Quéré,et al.  Combined constraints on global ocean primary production using observations and models , 2013 .