1932

Abstract

Phytoplankton size structure controls the trophic organization of planktonic communities and their ability to export biogenic materials toward the ocean's interior. Our understanding of the mechanisms that drive the variability in phytoplankton size structure has been shaped by the assumption that the pace of metabolism decreases allometrically with increasing cell size. However, recent field and laboratory evidence indicates that biomass-specific production and growth rates are similar in both small and large cells but peak at intermediate cell sizes. The maximum nutrient uptake rate scales isometrically with cell volume and superisometrically with the minimum nutrient quota. The unimodal size scaling of phytoplankton growth arises from ataxonomic, size-dependent trade-off processes related to nutrient requirement, acquisition, and use. The superior ability of intermediate-size cells to exploit high nutrient concentrations explains their biomass dominance during blooms. Biogeographic patterns in phytoplankton size structure and growth rate are independent of temperature and driven mainly by changes in resource supply.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-marine-010814-015955
2015-01-03
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/marine/7/1/annurev-marine-010814-015955.html?itemId=/content/journals/10.1146/annurev-marine-010814-015955&mimeType=html&fmt=ahah

Literature Cited

  1. Aksnes DL, Egge JK. 1991. A theoretical model for nutrient uptake in phytoplankton. Mar. Ecol. Prog. Ser. 70:65–72 [Google Scholar]
  2. Arbones B, Castro CG, Alonso-Pérez F, Figueiras FG. 2008. Phytoplankton size structure and water column metabolic balance in a coastal upwelling system: the Ría de Vigo, NW Iberia. Aquat. Microb. Ecol. 50:169–79 [Google Scholar]
  3. Armstrong RA. 1994. Grazing limitation and nutrient limitation in marine ecosystems: steady state of an ecosystem model with multiple food chains. Limnol. Oceanogr. 39:597–608 [Google Scholar]
  4. Atkinson D, Ciotti BJ, Montagnes DSJ. 2003. Protists decrease in size linearly with temperature: ca. 2.5% °C−1. Proc. R. Soc. B 270:2605–11 [Google Scholar]
  5. Azam F, Fenchel T, Field J, Gray J, Meyer-Reil L, Thingstad F. 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10:257–63 [Google Scholar]
  6. Banavar JR, Maritan A, Rinaldo A. 1999. Size and form in efficient transportation networks. Nature 399:130–32 [Google Scholar]
  7. Banse K. 1982. Cell volumes, maximal growth rates of unicellular algae and ciliates, and the role of ciliates in the marine pelagial. Limnol. Oceanogr. 27:1059–71 [Google Scholar]
  8. Barton AD, Pershing AJ, Litchman E, Record NR, Edwards KF. et al. 2013. The biogeography of marine plankton traits. Ecol. Lett. 16:522–34 [Google Scholar]
  9. Bec B, Collos Y, Vaquer A, Mouillot D, Souchu P. 2008. Growth rate peaks at intermediate cell size in marine photosynthetic picoeukaryotes. Limnol. Oceanogr. 53:863–67 [Google Scholar]
  10. Behrenfeld MJ, Boss ES. 2014. Resurrecting the ecological underpinnings of ocean plankton blooms. Annu. Rev. Mar. Sci. 6:167–94 [Google Scholar]
  11. Beman JM, Arrigo KR, Matson PA. 2005. Agricultural runoff fuels large phytoplankton blooms in vulnerable areas of the ocean. Nature 434:211–14 [Google Scholar]
  12. Blasco D, Packard TT, Garfield PC. 1982. Size dependence of growth rate, respiratory electron transport system activity, and chemical composition in marine diatoms in the laboratory. J. Phycol. 18:58–63 [Google Scholar]
  13. Bopp L, Aumont O, Cadule P, Alvain S, Gehlen M. 2005. Response of diatoms distribution to global warming and potential implications: a global model study. Geophys. Res. Lett. 32:L19606 [Google Scholar]
  14. Boyd PW, Trull TW. 2007. Understanding the export of biogenic particles in oceanic waters: Is there consensus?. Prog. Oceanogr. 72:276–312 [Google Scholar]
  15. Boyd PW, Watson AJ, Law CS, Abraham ER, Trull T. et al. 2000. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 407:695–702 [Google Scholar]
  16. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB. 2004. Toward a metabolic theory of ecology. Ecology 85:1771–89 [Google Scholar]
  17. Calbet A. 2001. Mesozooplancton grazing effect on primary production: a global comparative analysis in marine ecosystems. Limnol. Oceanogr. 46:1824–30 [Google Scholar]
  18. Calbet A. 2008. The trophic roles of microzooplankton in marine systems. ICES J. Mar. Sci. 65:325–31 [Google Scholar]
  19. Calbet A, Landry MR. 2004. Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr. 49:51–57 [Google Scholar]
  20. Cavender-Bares KK, Karl DM, Chisholm SW. 2001. Nutrient gradients in the western North Atlantic Ocean: relationship to microbial community structure and comparison to patterns in the Pacific Ocean. Deep-Sea Res. I 48:2373–95 [Google Scholar]
  21. Cermeño P, Figueiras FG. 2008. Species richness and cell-size distribution: size structure of phytoplankton communities. Mar. Ecol. Prog. Ser. 357:79–85 [Google Scholar]
  22. Cermeño P, Lee J-B, Wyman K, Schofield OM, Falkowski PG. 2011. Competitive dynamics in two species of marine phytoplankton under non-equilibrium conditions. Mar. Ecol. Prog. Ser. 429:19–28 [Google Scholar]
  23. Cermeño P, Marañón E, Harbour DS, Figueiras FG, Crespo BG. et al. 2008. Resource levels, allometric scaling of population abundance, and marine phytoplankton diversity. Limnol. Oceanogr. 53:312–18 [Google Scholar]
  24. Cermeño P, Marañón E, Harris RP, Harbour DS. 2006a. Invariant scaling of phytoplankton abundance and cell size in contrasting marine environments. Ecol. Lett. 9:1210–15 [Google Scholar]
  25. Cermeño P, Marañón E, Pérez V, Serret P, Fernández E, Castro CG. 2006b. Phytoplankton size structure and primary production in a highly dynamic coastal ecosystem (Ría de Vigo, NW-Spain): seasonal and short-time scale variability. Estuar. Coast. Shelf Sci. 67:251–66 [Google Scholar]
  26. Cermeño P, Marañón E, Rodríguez J, Fernández E. 2005a. Large-sized phytoplankton sustain higher carbon-specific photosynthesis than smaller cells in a coastal eutrophic ecosystem. Mar. Ecol. Prog. Ser. 297:51–60 [Google Scholar]
  27. Cermeño P, Marañón E, Rodríguez J, Fernández E. 2005b. Size dependence of coastal phytoplankton photosynthesis under vertical mixing conditions. J. Plankton Res. 27:473–83 [Google Scholar]
  28. Chang FH, Marquis EC, Chang CW, Gong GC, Hsieh CH. 2013. Scaling of growth rate and mortality with size and its consequence on size spectra of natural microphytoplankton assemblages in the East China Sea. Biogeosciences 10:5267–80 [Google Scholar]
  29. Chen BZ, Liu HB. 2011. Relationships between phytoplankton growth and cell size in surface oceans: interactive effects of temperature, nutrients, and grazing. Limnol. Oceanogr. 55:965–72 [Google Scholar]
  30. Chisholm SW. 1992. Phytoplankton size. Primary Productivity and Biogeochemical Cycles in the Sea PG Falkowski 213–37 New York: Plenum [Google Scholar]
  31. Clarke A, Meredith MP, Wallace MI, Brandon MA, Thomas DN. 2008. Seasonal and interannual variability in temperature, chlorophyll and macronutrients in northern Marguerite Bay, Antarctica. Deep-Sea Res. II 55:1988–2006 [Google Scholar]
  32. Cullen J, Yang X, MacIntyre HL. 1992. Nutrient limitation and marine photosynthesis. Primary Productivity and Biogeochemical Cycles in the Sea PG Falkowski 69–88 New York: Plenum [Google Scholar]
  33. Daufresne M, Lengfellner K, Sommer U. 2009. Global warming benefits the small in aquatic ecosystems. Proc. Natl. Acad. Sci. USA 106:12788–93 [Google Scholar]
  34. Davidson EA, Janssens IA. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–73 [Google Scholar]
  35. Davidson EA, Janssens IA, Luo Y. 2006. On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Glob. Change Biol. 12:154–64 [Google Scholar]
  36. DeLong JP, Okie JG, Moses ME, Sibly RM, Brown JH. 2010. Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life. Proc. Natl. Acad. Sci. USA 107:12941–45 [Google Scholar]
  37. Doney SC. 2006. Plankton in a warmer world. Nature 444:695–96 [Google Scholar]
  38. Droop MR. 1973. Some thoughts on nutrient limitation in algae. J. Phycol. 9:264–72 [Google Scholar]
  39. Edwards KF, Thomas MK, Klausmeier CA, Litchman E. 2012. Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton. Limnol. Oceanogr. 57:554–66 [Google Scholar]
  40. Enquist BJ, Brown JH, West GB. 1998. Allometric scaling of plant energetics and population density. Nature 395:163–65 [Google Scholar]
  41. Eppley RW. 1972. Temperature and phytoplankton growth in the sea. Fish. Bull. 70:1063–85 [Google Scholar]
  42. Falkowski PG, Barber R, Smetacek V. 1998. Biogeochemical controls and feedbacks on ocean primary production. Science 281:200–6 [Google Scholar]
  43. Falkowski PG, Oliver MJ. 2007. Mix and match: how climate selects phytoplankton. Nat. Rev. Microbiol. 5:813–19 [Google Scholar]
  44. Fenchel T. 1974. Intrinsic rate of natural increase: the relationship with body size. Oecologia 14:317–26 [Google Scholar]
  45. Finkel ZV. 2001. Light absorption and size scaling of light-limited metabolism in marine diatoms. Limnol. Oceanogr. 46:86–94 [Google Scholar]
  46. Finkel ZV, Beardall J, Flynn KJ, Quigg A, Rees TAV, Raven JA. 2010. Phytoplankton in a changing world: cell size and elemental stoichiometry. J. Plankton Res. 32:119–37 [Google Scholar]
  47. Finkel ZV, Irwin AJ, Schofield O. 2004. Resource limitation alters the 3/4 size scaling of metabolic rates in phytoplankton. Mar. Ecol. Prog. Ser. 273:269–79 [Google Scholar]
  48. Follows MJ, Dutkiewicz S. 2011. Modeling diverse communities of marine microbes. Annu. Rev. Mar. Sci. 3:427–51 [Google Scholar]
  49. Forster J, Hirst AG, Atkinson D. 2012. Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proc. Natl. Acad. Sci. USA 109:19310–14 [Google Scholar]
  50. Geider RJ. 1987. Light and temperature dependence of the carbon to chlorophyll a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytoplankton. New Phytol. 106:1–34 [Google Scholar]
  51. Geider RJ, Platt T, Raven JA. 1986. Size dependence of growth and photosynthesis in diatoms: a synthesis. Mar. Ecol. Prog. Ser. 30:93–104 [Google Scholar]
  52. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL. 2001. Effects of size and temperature on metabolic rate. Science 293:2248–51 [Google Scholar]
  53. Guidi L, Stemmann L, Jackson GA, Ibanez F, Claustre H. et al. 2009. Effects of phytoplankton community on production, size and export of large aggregates: a world-ocean analysis. Limnol. Oceanogr. 54:1951–63 [Google Scholar]
  54. Gutiérrez-Rodríguez A, Latasa M, Agustí S, Duarte CM. 2011. Distribution and contribution of major phytoplankton groups to carbon cycling across contrasting conditions of the subtropical northeast Atlantic Ocean. Deep-Sea Res. I 58:1115–29 [Google Scholar]
  55. Harrison PJ, Parslow JS, Conway HL. 1989. Determination of nutrient uptake kinetic parameters: a comparison of methods. Mar. Ecol. Prog. Ser. 52:301–12 [Google Scholar]
  56. Huete-Ortega M, Cermeño P, Calvo-Díaz A, Marañón E. 2012. Isometric size-scaling of metabolic rate and the size abundance distribution of phytoplankton. Proc. R. Soc. B 279:1824–30 [Google Scholar]
  57. Huete-Ortega M, Marañón E, Varela M, Bode A. 2010. General patterns in the size scaling of phytoplankton abundance in coastal waters during a 10-year time series. J. Plankton Res. 32:1–14 [Google Scholar]
  58. Irigoien X, Flynn KJ, Harris RP. 2005. Phytoplankton blooms: a “loophole” in microzooplankton grazing impact?. J. Plankton Res. 27:313–21 [Google Scholar]
  59. Karentz D, Smayda TJ. 1984. Temperature and seasonal occurrence patterns of 30 dominant phytoplankton species in Narragansett Bay over a 22-year period (1959–1980). Mar. Ecol. Prog. Ser. 18:277–93 [Google Scholar]
  60. Kiørboe T. 1993. Turbulence, phytoplankton cell-size, and the structure of pelagic food webs. Adv. Mar. Biol. 29:1–72 [Google Scholar]
  61. Kiørboe T. 2008. A Mechanistic Approach to Plankton Ecology Princeton, NJ: Princeton Univ. Press
  62. Kleiber M. 1932. Body size and metabolism. Hilgardia 6:315–53 [Google Scholar]
  63. Kolokotrones T, Savage V, Deeds EJ, Fontana W. 2010. Curvature in metabolic scaling. Nature 464:753–56 [Google Scholar]
  64. Kruskopf M, Flynn KJ. 2005. Chlorophyll content and fluorescence responses cannot be used to gauge reliably phytoplankton biomass, nutrient status or growth rate. New Phytol. 169:525–36 [Google Scholar]
  65. Landry MR, Constantinou J, Latasa M, Brown SL, Bidigare RR, Ondrusek ME. 2000. Biological response to iron fertilization in the eastern equatorial Pacific (IronEx II). III. Dynamics of phytoplankton growth and microzooplankton grazing. Mar. Ecol. Prog. Ser. 201:57–72 [Google Scholar]
  66. Latasa M, Landry MR, Schlüter L, Bidigare RR. 1997. Pigment-specific growth and grazing rates of phytoplankton in the central equatorial Pacific. Limnol. Oceanogr. 42:289–98 [Google Scholar]
  67. Latasa M, Morán XAG, Scharek R, Estrada M. 2005. Estimating the carbon flux through main phytoplankton groups in the northwestern Mediterranean. Limnol. Oceanogr. 50:1447–58 [Google Scholar]
  68. Laws EA. 1975. The importance of respiration losses in controlling the size distribution of marine phytoplankton. Ecology 56:419–26 [Google Scholar]
  69. Laws EA. 2013. Evaluation of in situ phytoplankton growth rates: a synthesis of data from varied approaches. Annu. Rev. Mar. Sci. 5:247–68 [Google Scholar]
  70. Legendre L, Le Fèvre J. 1995. Microbial food webs and the export of biogenic carbon in oceans. Aquat. Microb. Ecol. 9:69–77 [Google Scholar]
  71. Legendre L, Rassoulzadegan F. 1996. Food-web mediated export of biogenic carbon in oceans: hydrodynamic control. Mar. Ecol. Prog. Ser. 145:179–93 [Google Scholar]
  72. Litchman E, Klausmeier CA. 2008. Trait-based community ecology of phytoplankton. Annu. Rev. Ecol. Evol. Syst. 39:615–39 [Google Scholar]
  73. Litchman E, Klausmeier CA, Schofield OM, Falkowski PG. 2007. The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol. Lett. 10:1170–81 [Google Scholar]
  74. López-Sandoval DC, Rodríguez-Ramos T, Cermeño P, Marañón E. 2013. Organic carbon exudation in marine phytoplankton: dependence on cell size and taxon. Mar. Ecol. Prog. Ser. 477:53–60 [Google Scholar]
  75. López-Sandoval DC, Rodríguez-Ramos T, Cermeño P, Sobrino C, Marañón E. 2014. Photosynthesis and respiration in marine phytoplankton: Relationship with cell size, taxonomic affiliation, and growth phase. J. Exp. Mar. Biol. Ecol. 457:151–159 [Google Scholar]
  76. López-Urrutia A, San Martín E, Harris RP, Irigoien X. 2006. Scaling the metabolic balance of the oceans. Proc. Natl. Acad. Sci. USA 103:8739–44 [Google Scholar]
  77. Marañón E. 2005. Phytoplankton growth rates in the Atlantic subtropical gyres. Limnol. Oceanogr. 50:299–310 [Google Scholar]
  78. Marañón E. 2008a. Inter-specific scaling of phytoplankton production and cell size in the field. J. Plankton Res. 30:157–63 [Google Scholar]
  79. Marañón E. 2008b. . Phytoplankton size structure. Encyclopedia of Ocean Sciences JH Steele, KK Turekian, SA Thorpe 445–52 Oxford, UK: Academic, 2nd ed.. [Google Scholar]
  80. Marañón E, Behrenfeld MJ, Gonzalez N, Mouriño B, Zubkov MV. 2003. High variability of primary production in oligotrophic waters of the Atlantic Ocean: uncoupling from phytoplankton biomass and size structure. Mar. Ecol. Prog. Ser. 257:1–11 [Google Scholar]
  81. Marañón E, Cermeño P, Huete-Ortega M, López-Sandoval DC, Mouriño-Carballido B, Rodríguez-Ramos T. 2014. Resource supply overrides temperature as a controlling factor of marine phytoplankton growth. PLoS ONE 9:e99312 [Google Scholar]
  82. Marañón E, Cermeño P, Latasa M, Tadonléké R. 2012. Temperature, resources, and phytoplankton size structure in the ocean. Limnol. Oceanogr. 57:1266–68 [Google Scholar]
  83. Marañón E, Cermeño P, López-Sandoval DC, Rodríguez-Ramos T, Sobrino C. et al. 2013. Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake and use. Ecol. Lett. 16:371–79 [Google Scholar]
  84. Marañón E, Cermeño P, Rodríguez J, Zubkov MV, Harris RP. 2007. Scaling of phytoplankton photosynthesis and cell size in the ocean. Limnol. Oceanogr. 52:2190–98 [Google Scholar]
  85. Marañón E, Holligan PM, Barciela R, Gonzalez N, Mouriño B. et al. 2001. Patterns of phytoplankton size structure and productivity in contrasting open-ocean environments. Mar. Ecol. Prog. Ser. 216:43–56 [Google Scholar]
  86. Marañón E, Holligan PM, Varela M, Mouriño B, Bale AJ. 2000. Basin-scale variability of phytoplankton biomass, production and growth in the Atlantic Ocean. Deep-Sea Res. I 47:825–57 [Google Scholar]
  87. Margalef R. 1978. Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanol. Acta 1:493–509 [Google Scholar]
  88. Menden-Deuer S, Lessard EJ. 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45:569–79 [Google Scholar]
  89. Montagnes DJS, Franklin DJ. 2001. Effect of temperature on diatom volume, growth rate, and carbon and nitrogen content: reconsidering some paradigms. Limnol. Oceanogr. 46:2008–18 [Google Scholar]
  90. Moore CM, Mills MM, Arrigo KR, Berman-Frank I, Bopp L. et al. 2013. Processes and patterns of ocean nutrient limitation. Nat. Geosci. 6:701–10 [Google Scholar]
  91. Morán XAG, López-Urrutia Á, Calvo-Díaz A, Li WKW. 2009. Increasing importance of small phytoplankton in a warmer ocean. Glob. Change Biol. 16:1137–44 [Google Scholar]
  92. Niklas KJ. 1994. Size-dependent variations in plant-growth rates and the “3/4-power rules.”. Am. J. Bot. 81:134–44 [Google Scholar]
  93. O'Connor MI, Piehler MF, Leech DM, Anton A, Bruno JF. 2009. Warming and resource availability shift food web structure and metabolism. PLoS Biol. 7:e1000178 [Google Scholar]
  94. Pasciak WJ, Gauis G. 1974. Transport limitation of nutrient uptake in phytoplankton. Limnol. Oceanogr. 19:881–88 [Google Scholar]
  95. Peter KH, Sommer U. 2013. Phytoplankton cell size reduction in response to warming mediated by nutrient limitation. PLoS ONE 8:e71528 [Google Scholar]
  96. Poulin FJ, Franks PJS. 2010. Size-structured planktonic ecosystems: constraints, controls and assembly instructions. J. Plankton Res. 32:1121–30 [Google Scholar]
  97. Raven JA. 1987. The role of vacuoles. New Phytol. 106:357–422 [Google Scholar]
  98. Raven JA. 1994. Why are there no picoplanktonic O2 evolvers with volumes less than 10−19 m3?. J. Plankton Res. 16:565–80 [Google Scholar]
  99. Raven JA. 1998. The twelfth Tansley Lecture. Small is beautiful: the picoplankton. Funct. Ecol. 12:503–13 [Google Scholar]
  100. Reul A, Rodríguez V, Jiménez-Gómez F, Blanco JM, Bautista B. et al. 2005. Variability in the spatio-temporal distribution and size-structure of phytoplankton across an upwelling area in the NW-Alboran Sea (W-Mediterranean). Cont. Shelf Res. 25:589–608 [Google Scholar]
  101. Rodríguez J, Blanco JM, Jiménez-Gómez F, Echevarría F, Gil J. et al. 1998. Patterns in the size structure of the phytoplankton community in the deep fluorescence maximum of the Alboran Sea (southwestern Mediterranean). Deep-Sea Res. I 45:1577–93 [Google Scholar]
  102. Rodríguez J, Tintoré J, Allen JT, Blanco JM, Gomis D. et al. 2001. Mesoscale vertical motion and the size structure of phytoplankton in the ocean. Nature 410:360–63 [Google Scholar]
  103. Sarthou G, Timmermans KR, Blain S, Treguer P. 2005. Growth physiology and fate of diatoms in the ocean: a review. J. Sea Res. 53:25–42 [Google Scholar]
  104. Savage VM, Gillooly JF, Woodruff WH, West GB, Allen AP. et al. 2004. The predominance of quarter-power scaling in biology. Funct. Ecol. 18:257–82 [Google Scholar]
  105. Schmoker C, Hernández-León S, Calbet A. 2013. Microzooplankton grazing in the oceans: impacts, data variability, knowledge gaps and future directions. J. Plankton Res. 35:691–706 [Google Scholar]
  106. Sherr EB, Sherr BF. 2009. Capacity of herbivorous protists to control initiation and development of mass phytoplankton blooms. Aquat. Microb. Ecol. 57:253–62 [Google Scholar]
  107. Smayda TJ. 1970. The suspension and sinking of phytoplankton in the sea. Oceanogr. Mar. Biol. Annu. Rev. 8:353–414 [Google Scholar]
  108. Smetacek V. 1999. Diatoms and the ocean carbon cycle. Protist 150:25–32 [Google Scholar]
  109. Smith REH, Kalff J. 1982. Size-dependent phosphorus uptake kinetics and cell quota in phytoplankton. J. Phycol. 18:275–84 [Google Scholar]
  110. Sommer U. 1989. Maximal growth-rates of Antarctic phytoplankton: only weak dependence on cell size. Limnol. Oceanogr. 34:1109–12 [Google Scholar]
  111. Sommer U, Lengfellner K. 2008. Climate change and the timing, magnitude, and composition of the phytoplankton spring bloom. Glob. Change Biol. 14:1199–208 [Google Scholar]
  112. Staehr PA, Sand-Jensen K. 2006. Seasonal changes in temperature and nutrient control of photosynthesis, respiration and growth of natural phytoplankton communities. Freshw. Biol. 51:249–62 [Google Scholar]
  113. Steinacher M, Joos F, Frölicher TL, Bopp L, Cadule P. et al. 2010. Projected 21st century decrease in marine productivity: a multi-model analysis. Biogeosciences 7:979–1005 [Google Scholar]
  114. Stolte W, Riegman R. 1995. Effect of phytoplankton cell size on transient-state nitrate and ammonium uptake kinetics. Microbiology 141:1221–29 [Google Scholar]
  115. Strom SL, Macri EL, Olson MB. 2007. Microzooplankton grazing in the coastal Gulf of Alaska: variations in top-down control of phytoplankton. Limnol. Oceanogr. 52:1480–94 [Google Scholar]
  116. Tadonléké R. 2010. Evidence of warming effects on phytoplankton productivity rates and their dependence on eutrophication status. Limnol. Oceanogr. 55:973–82 [Google Scholar]
  117. Tang EPY. 1995. The allometry of algal growth rates. J. Plankton Res. 17:1325–35 [Google Scholar]
  118. Tang EPY, Peters RH. 1995. The allometry of algal respiration. J. Plankton Res. 17:303–15 [Google Scholar]
  119. Teixeira IG, Figueiras FG, Crespo BG, Piedracoba S. 2011. Microzooplankton feeding impact in a coastal upwelling system on the NW Iberian margin: the Ría de Vigo. Estuar. Coast. Shelf Sci. 91:110–20 [Google Scholar]
  120. Thingstad TF, Ovreas L, Egge JK, Lovdal T, Heldal M. 2005. Use of non-limiting substrates to increase size; a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs?. Ecol. Lett. 8:675–82 [Google Scholar]
  121. Verity PG, Robertson CY, Tronzo CR, Melinda AG, Nelson JR, Sieracki ME. 1992. Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic reactions. Limnol. Oceanogr. 37:1434–46 [Google Scholar]
  122. Villareal TA, Brown CG, Brzezinski MA, Krause JW, Wilson C. 2012. Summer diatom blooms in the North Pacific subtropical gyre: 2008–2009. PLoS ONE 7:e33109 [Google Scholar]
  123. Villareal TA, Woods S, Moore JK, Culver-Rymsza K. 1996. Vertical migration of Rhizosolenia mats and their significance to NO3 fluxes in the central North Pacific gyre. J. Plankton Res. 18:1103–21 [Google Scholar]
  124. Ward BA, Dutkiewicz S, Follows MJ. 2014. Modelling spatial and temporal patterns in size-structured marine plankton communities: top-down and bottom-up controls. J. Plankton Res. 36:31–47 [Google Scholar]
  125. Ward BA, Dutkiewicz S, Jahn O, Follows MJ. 2012. A size-structured food-web model for the global ocean. Limnol. Oceanogr. 57:1877–91 [Google Scholar]
  126. West GB, Brown JH, Enquist BJ. 1997. A general model for the origin of allometric scaling laws in biology. Science 276:122–26 [Google Scholar]
  127. Wirtz KW. 2011. Non-uniform scaling in phytoplankton growth rate due to intracellular light and CO2 decline. J. Plankton Res. 33:1325–41 [Google Scholar]
  128. Yvon-Durocher G, Montoya JM, Trimmer M, Woodward G. 2010. Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems. Glob. Change Biol. 17:1681–94 [Google Scholar]
  129. Zubkov MV, Sleigh MA, Tarran GA, Burkill PH, Leakey RJG. 1998. Picoplanktonic community structure on an Atlantic transect from 50°N to 50°S. Deep-Sea Res. I 45:1339–55 [Google Scholar]
/content/journals/10.1146/annurev-marine-010814-015955
Loading
/content/journals/10.1146/annurev-marine-010814-015955
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error