A multicomponent model of phytoplankton size structure

Size-fractionated filtration (SFF) is a direct method for estimating pigment concentration in various size classes. It is also common practice to infer the size structure of phytoplankton communities from diagnostic pigments estimated by high-performance liquid chromatography (HPLC). In this paper, the three-component model of Brewin et al. (2010) was fitted to coincident data from HPLC and from SFF collected along Atlantic Meridional Transect cruises. The model accounted for the variability in each data set, but the fitted model parameters differed for the two data sets. Both HPLC and SFF data supported the conceptual framework of the three-component model, which assumes that the chlorophyll concentration in small cells increases to an asymptotic maximum, beyond which further increase in chlorophyll is achieved by the addition of larger celled phytoplankton. The three-component model was extended to a multicomponent model of size structure using observed relationships between model parameters and assuming that the asymptotic concentration that can be reached by cells increased linearly with increase in the upper bound on the cell size. The multicomponent model was verified using independent SFF data for a variety of size fractions and found to perform well (0.628 ≤ r ≤ 0.989) lending support for the underlying assumptions. An advantage of the multicomponent model over the three-component model is that, for the same number of parameters, it can be applied to any size range in a continuous fashion. The multicomponent model provides a useful tool for studying the distribution of phytoplankton size structure at large scales.

[1]  Nicholas H Mann,et al.  Phages of the marine cyanobacterial picophytoplankton. , 2003, FEMS microbiology reviews.

[2]  T. Platt,et al.  Patterns of biomass-size spectra from oligotrophic waters of the Northwest Atlantic [review article] , 2003 .

[3]  Annick Bricaud,et al.  Retrievals of a size parameter for phytoplankton and spectral light absorption by colored detrital matter from water‐leaving radiances at SeaWiFS channels in a continental shelf region off Brazil , 2006 .

[4]  Patrick M. Holligan,et al.  Phytoplankton pigments and functional types in the Atlantic Ocean: A decadal assessment, 1995–2005 , 2009 .

[5]  S. Sathyendranath,et al.  The influence of the Indian Ocean Dipole on interannual variations in phytoplankton size structure as revealed by Earth Observation , 2012 .

[6]  Marcel Babin,et al.  Toward a taxon‐specific parameterization of bio‐optical models of primary production: A case study in the North Atlantic , 2005 .

[7]  G. Tilstone,et al.  Latitudinal variation of the balance between plankton photosynthesis and respiration in the eastern Atlantic Ocean , 2001 .

[8]  Stéphane Blain,et al.  An ecosystem model of the global ocean including Fe, Si, P colimitations , 2003 .

[9]  M. Clokie,et al.  Cyanophage infection and photoinhibition in marine cyanobacteria. , 2004, Research in microbiology.

[10]  Sheng Zhang,et al.  Dynamics and size structure of phytoplankton in the coastal waters of Singapore , 2000 .

[11]  N. Welschmeyer Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments , 1994 .

[12]  Charles S. Yentsch,et al.  A bridge between ocean optics and microbial ecology , 1989 .

[13]  J. Cullen,et al.  A semi-analytical model of the influence of phytoplankton community structure on the relationship between light attenuation and ocean color , 1999 .

[14]  S. Sathyendranath,et al.  A three-component model of phytoplankton size class for the Atlantic Ocean , 2010 .

[15]  William K. W. Li,et al.  Coherent assembly of phytoplankton communities in diverse temperate ocean ecosystems , 2006, Proceedings of the Royal Society B: Biological Sciences.

[16]  Trevor Platt,et al.  A three component classification of phytoplankton absorption spectra: Application to ocean-color data , 2011 .

[17]  Janet W. Campbell,et al.  The lognormal distribution as a model for bio‐optical variability in the sea , 1995 .

[18]  H. Bouman,et al.  Bio-optical properties of the subtropical North Atlantic. I. Vertical variability , 2000 .

[19]  Robert J. W. Brewin,et al.  Comparison of two methods to derive the size-structure of natural populations of phytoplankton , 2014 .

[20]  R. W. Sheldon,et al.  The Size Distribution of Particles in the OCEAN1 , 1972 .

[21]  B. Peterson,et al.  Particulate organic matter flux and planktonic new production in the deep ocean , 1979, Nature.

[22]  Patrick Raimbault,et al.  Size fraction of phytoplankton in the Ligurian Sea and the Algerian Basin (Mediterranean Sea): size distribution versus total concentration , 1988 .

[23]  P. Holligan,et al.  Surface phytoplankton pigment distributions in the Atlantic Ocean: an assessment of basin scale variability between 50°N and 50°S , 2000 .

[24]  B. Efron Bootstrap Methods: Another Look at the Jackknife , 1979 .

[25]  Jim Aiken,et al.  An absorption model to determine phytoplankton size classes from satellite ocean colour , 2008 .

[26]  H. Claustre,et al.  Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans , 2009, Proceedings of the National Academy of Sciences.

[27]  S. Maritorena,et al.  Phytoplankton pigment and absorption characteristics along meridional transects in the Atlantic Ocean , 2002 .

[28]  Toru Hirawake,et al.  Remote sensing of size structure of phytoplankton communities using optical properties of the Chukchi and Bering Sea shelf region , 2011 .

[29]  Dariusz Stramski,et al.  Spectral dependency of optical backscattering by marine particles from satellite remote sensing of the global ocean , 2006 .

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

[31]  P. Boyd,et al.  Does planktonic community structure determine downward particulate organic carbon flux in different oceanic provinces , 1999 .

[32]  Trevor Platt,et al.  Remote sensing of phytoplankton functional types , 2008 .

[33]  Y. Yamanaka,et al.  A comparison between phytoplankton community structures derived from a global 3D ecosystem model and satellite observation , 2013 .

[34]  I. McLAREN Effects of Temperature on Growth of Zooplankton, and the Adaptive Value of Vertical Migration , 1963 .

[35]  I. N. McCave Vertical flux of particles in the ocean , 1975 .

[36]  R. Bidigare,et al.  Accessory pigments versus chlorophyll a concentrations within the euphotic zone: A ubiquitous relationship , 2000 .

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

[38]  Jerry Blackford,et al.  Ecosystem dynamics at six contrasting sites: a generic modelling study , 2004 .

[39]  John J. Cullen,et al.  Effects of nitrate on the diurnal vertical migration, carbon to nitrogen ratio, and the photosynthetic capacity of the dinoflagellate Gymnodinium splendens , 1981 .

[40]  R. Peters The Ecological Implications of Body Size , 1983 .

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

[42]  Carlos M. Duarte,et al.  Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production , 2000 .

[43]  James Harle,et al.  Potential consequences of climate change for primary production and fish production in large marine ecosystems , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  David A. Siegel,et al.  Retrieval of the particle size distribution from satellite ocean color observations , 2009 .

[45]  J. Raven,et al.  Temperature and algal growth , 1988 .

[46]  J. Blanchard,et al.  Ecosystem size structure response to 21st century climate projection: large fish abundance decreases in the central North Pacific and increases in the California Current , 2013, Global change biology.

[47]  S. Doney,et al.  Response of ocean phytoplankton community structure to climate change over the 21st century: partitioning the effects of nutrients, temperature and light , 2010 .

[48]  R. ParsonsT,et al.  Jellyfish Population Explosions: Revisiting a Hypothesis of Possible Causes , 2002 .

[49]  B. Franz,et al.  Examining the consistency of products derived from various ocean color sensors in open ocean (Case 1) waters in the perspective of a multi-sensor approach , 2007 .

[50]  John J. Cullen,et al.  Assessment of the relationships between dominant cell size in natural phytoplankton communities and the spectral shape of the absorption coefficient , 2002 .

[51]  John A. Raven,et al.  The twelfth Tansley Lecture. Small is beautiful: the picophytoplankton , 1998 .

[52]  J. Ras,et al.  Validation of MERIS reflectance and chlorophyll during the BENCAL cruise October 2002: preliminary validation of new demonstration products for phytoplankton functional types and photosynthetic parameters , 2007 .

[53]  J. Aiken,et al.  Pigment adaptations in surface phytoplankton along the eastern boundary of the Atlantic Ocean , 2004 .

[54]  T. Platt,et al.  Modelling the time-evolution of phytoplankton size spectra from satellite remote sensing , 2011 .

[55]  P. Holligan,et al.  Patterns of phytoplankton size structure and productivity in contrasting open-ocean environments , 2001 .

[56]  Robert J. W. Brewin,et al.  Deriving phytoplankton size classes from satellite data: Validation along a trophic gradient in the eastern Atlantic Ocean , 2013 .

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

[58]  W. Sunda,et al.  Interrelated influence of iron, light and cell size on marine phytoplankton growth , 1997, Nature.

[59]  Yasuhiro Yamanaka,et al.  NEMURO—a lower trophic level model for the North Pacific marine ecosystem , 2007 .

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

[61]  K. Denman,et al.  Organisation in the pelagic ecosystem , 1977, Helgoländer wissenschaftliche Meeresuntersuchungen.

[62]  Annick Bricaud,et al.  Estimation of new primary production in the Benguela upwelling area, using ENVISAT satellite data and a model dependent on the phytoplankton community size structure , 2008 .

[63]  A. Bricaud,et al.  Theoretical results concerning light absorption in a discrete medium, and application to specific absorption of phytoplankton , 1981 .

[64]  S. Chisholm,et al.  Marine Viruses Exploit Their Host's Two-Component Regulatory System in Response to Resource Limitation , 2012, Current Biology.

[65]  Annick Bricaud,et al.  Spatial‐temporal variations in phytoplankton size and colored detrital matter absorption at global and regional scales, as derived from twelve years of SeaWiFS data (1998–2009) , 2012 .

[66]  G. Dall’Olmo,et al.  Particle backscattering as a function of chlorophyll and phytoplankton size structure in the open-ocean. , 2012, Optics express.

[67]  X. Irigoien,et al.  Latitudinal variation in plankton size spectra in the Atlantic Ocean , 2006 .

[68]  G. Bratbak,et al.  Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms , 1993 .

[69]  Annick Bricaud,et al.  Natural variability of phytoplanktonic absorption in oceanic waters: Influence of the size structure of algal populations , 2004 .

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

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

[72]  R. Eppley,et al.  Growth Rates of Marine Phytoplankton: Correlation with Light Absorption by Cell Chlorophyll a , 1966 .

[73]  J. Raven,et al.  Size dependence of growth and photosynthesis in diatoms: a synthesis , 1986 .

[74]  T. Platt,et al.  Discrimination of diatoms from other phytoplankton using ocean-colour data , 2004 .

[75]  Ian G. Droppo,et al.  Filtration in Particle Size Analysis , 2006 .

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

[77]  L. Legendre,et al.  From Individual Plankton Cells To Pelagic Marine Ecosystems And To Global Biogeochemical Cycles , 1991 .

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

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

[80]  Walker O. Smith,et al.  Temperature effects on export production in the open ocean , 2000 .

[81]  K. Denman,et al.  The structure of pelagic marine ecosystems. , 1978 .

[82]  Trevor Platt,et al.  A two‐component model of phytoplankton absorption in the open ocean: Theory and applications , 2006 .

[83]  L. Prieur,et al.  An optical classification of coastal and oceanic waters based on the specific spectral absorption curves of phytoplankton pigments, dissolved organic matter, and other particulate materials1 , 1981 .

[84]  Stephanie Dutkiewicz,et al.  A size‐structured food‐web model for the global ocean , 2012 .

[85]  J. G. Field,et al.  The size-based dynamics of plankton food webs. I. A simulation model of carbon and nitrogen flows , 1991 .

[86]  H. Claustre,et al.  Vertical distribution of phytoplankton communities in open ocean: An assessment based on surface chlorophyll , 2006 .

[87]  P. Croot,et al.  Picophytoplankton - a comparative study of their biochemical composition and photosynthetic properties , 2005 .

[88]  T. Thingstad,et al.  Control of phytoplankton growth in nutrient recycling ecosystems. Theory and terminology , 1990 .

[89]  Julia Uitz,et al.  A phytoplankton class-specific primary production model applied to the Kerguelen Islands region (Southern Ocean) , 2009 .

[90]  T. Probyn Nitrogen uptake by size-fractionated phytoplankton populations in the southern Benguela upwelling system , 1985 .

[91]  Hervé Claustre,et al.  Phytoplankton pigment distribution in relation to upper thermocline circulation in the eastern Mediterranean Sea during winter , 2001 .

[92]  Ralf Goericke,et al.  Top‐down control of phytoplankton biomass and community structure in the monsoonal Arabian Sea , 2002 .

[93]  Masahiko Fujii,et al.  The Value of Adding Optics to Ecosystem Models: A Case Study , 2007 .

[94]  R. Riegman,et al.  Size-differential control of phytoplankton and the structure of plankton communities , 1993 .

[95]  C. Mouw,et al.  Optical determination of phytoplankton size composition from global SeaWiFS imagery , 2010 .

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

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

[98]  S. Gibb,et al.  Improved resolution of mono- and divinyl chlorophylls a and b and zeaxanthin and lutein in phytoplankton extracts using reverse phase C-8 HPLC , 1997 .

[99]  Y. Yamanaka,et al.  Synoptic relationships between surface Chlorophyll- a and diagnostic pigments specific to phytoplankton functional types , 2011 .

[100]  D. Schlesinger,et al.  Specific Growth Rates of Freshwater Algae in Relation to Cell Size and Light Intensity , 1981 .

[101]  M. Silver,et al.  Primary production, sinking fluxes and the microbial food web , 1988 .

[102]  J. Aiken,et al.  Functional links between bioenergetics and bio-optical traits of phytoplankton taxonomic groups: an overarching hypothesis with applications for ocean colour remote sensing , 2007 .

[103]  Dag L. Aksnes,et al.  A theoretical model for nutrient uptake in phytoplankton , 1991 .

[104]  G. Kulk,et al.  Distinct differences in photoacclimation potential between prokaryotic and eukaryotic oceanic phytoplankton , 2011 .

[105]  E. Marañón,et al.  Temperature, resources, and phytoplankton size structure in the ocean , 2012 .