Cell Size as a Key Determinant of Phytoplankton Metabolism and Community Structure
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.
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TOWARD A METABOLIC THEORY OF ECOLOGY
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., & West, G. B. (2004) · Ecology · doi:10.1890/03-9000 · Cited by 7,779 · see citing works
Temperature sensitivity of soil carbon decomposition and feedbacks to climate change
Davidson, E. A., & Janssens, I. A. (2006) · Nature · doi:10.1038/nature04514 · Cited by 6,919 · see citing works
The Ecological Role of Water-Column Microbes in the Sea
Azam, F., Fenchel, T., Field, J., Gray, J. S., Meyer-Reil, L., & Thingstad, T. F. (1983) · Marine Ecology Progress Series · doi:10.3354/meps010257 · Cited by 5,398 · see citing works
A General Model for the Origin of Allometric Scaling Laws in Biology
West, G. B., Brown, J. H., & Enquist, B. J. (1997) · Science · doi:10.1126/science.276.5309.122 · Cited by 5,016 · see citing works
Effects of Size and Temperature on Metabolic Rate
Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M., & Charnov, E. L. (2001) · Science · doi:10.1126/science.1061967 · Cited by 3,810 · see citing works
Biogeochemical Controls and Feedbacks on Ocean Primary Production
Falkowski, P. G., Barber, R. T., & Smetacek, V. (1998) · Science · doi:10.1126/science.281.5374.200 · Cited by 2,848 · see citing works
Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton
Menden-Deuer, S., & Lessard, E. (2000) · Limnology and Oceanography · doi:10.4319/lo.2000.45.3.0569 · Cited by 2,499 · see citing works
Processes and patterns of oceanic nutrient limitation
Moore, C. M., Mills, M. M., Arrigo, K. R., Berman-Frank, I., Bopp, L., Boyd, P. W., Galbraith, E. D., Geider, R. J., Guieu, C., Jaccard, S. L., et al. (2013) · Nature Geoscience · doi:10.1038/ngeo1765 · Cited by 2,236 · see citing works
Self-citationKleiber, M. (1932) · Hilgardia · doi:10.3733/hilg.v06n11p315 · Cited by 2,222 · see citing works
Global warming benefits the small in aquatic ecosystems
Daufresne, M., Lengfellner, K., & Sommer, U. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902080106 · Cited by 1,726 · see citing works
A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization
Boyd, P. W., Watson, A. J., Law, C. S., Abraham, E. R., Trull, T. W., Murdoch, R. C., Bakker, D. C. E., Bowie, A. R., Buesseler, K. O., Chang, H., et al. (2000) · Nature · doi:10.1038/35037500 · Cited by 1,614 · see citing works
On the variability of respiration in terrestrial ecosystems: moving beyond Q 10
Davidson, E. A., Janssens, I. A., & Luo, Y. (2005) · Global Change Biology · doi:10.1111/j.1365-2486.2005.01065.x · Cited by 1,314 · see citing works
Trait-Based Community Ecology of Phytoplankton
Litchman, E., & Klausmeier, C. A. (2008) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.39.110707.173549 · Cited by 1,286 · see citing works
Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems
Calbet, A., & Landry, M. (2004) · Limnology and Oceanography · doi:10.4319/lo.2004.49.1.0051 · Cited by 1,202 · see citing works
Phytoplankton in a changing world: cell size and elemental stoichiometry
Finkel, Z. V., Beardall, J., Flynn, K. J., Quigg, A. S., Rees, T. A. V., & Raven, J. A. (2009) · Journal of Plankton Research · doi:10.1093/plankt/fbp098 · Cited by 1,159 · see citing works
Allometric scaling of plant energetics and population density
Enquist, B. J., Brown, J. H., & West, G. B. (1998) · Nature · doi:10.1038/25977 · Cited by 933 · see citing works
Litchman, E., Klausmeier, C. A., Schofield, O., & Falkowski, P. G. (2007) · Ecology Letters · doi:10.1111/j.1461-0248.2007.01117.x · Cited by 924 · see citing works
Size and form in efficient transportation networks
Banavar, J. R., Maritan, A., & Rinaldo, A. (1999) · Nature · doi:10.1038/20144 · Cited by 856 · see citing works
Growth physiology and fate of diatoms in the ocean: a review
Sarthou, G., Timmermans, K. R., Blain, S., et al. (2004) · Journal of Sea Research · doi:10.1016/j.seares.2004.01.007 · Cited by 839 · see citing works
Encyclopedia of ocean sciences
(2002) · Choice Reviews Online · doi:10.5860/choice.39-3717 · Cited by 838 · see citing works
SOME THOUGHTS ON NUTRIENT LIMITATION IN ALGAE1
Droop, M. R. (1973) · Journal of Phycology · doi:10.1111/j.1529-8817.1973.tb04092.x · Cited by 813 · see citing works
The suspension and sinking of phytoplankton in the sea
Smayda, T. J. (1970) · Oceanography and Marine Biology/Oceanography and marine biology - an annual review · Cited by 802 · see citing works
Turbulence, Phytoplankton Cell Size, and the Structure of Pelagic Food Webs
Kiørboe, T. (1993) · Advances in marine biology · doi:10.1016/s0065-2881(08)60129-7 · Cited by 731 · see citing works
The predominance of quarter‐power scaling in biology
Savage, V. M., Gillooly, J. F., Woodruff, W. H., West, G. B., Allen, A. P., Enquist, B. J., & Brown, J. H. (2004) · Functional Ecology · doi:10.1111/j.0269-8463.2004.00856.x · Cited by 713 · see citing works
Geider, R. J. (1987) · New Phytologist · doi:10.1111/j.1469-8137.1987.tb04788.x · Cited by 696 · see citing works
Verity, P. G., Robertson, C. Y., Tronzo, C. R., Andrews, M. G., Nelson, J. R., & Sieracki, M. E. (1992) · Limnology and Oceanography · doi:10.4319/lo.1992.37.7.1434 · Cited by 655 · see citing works
The twelfth Tansley Lecture. Small is beautiful: the picophytoplankton
Raven, J. A. (1998) · Functional Ecology · doi:10.1046/j.1365-2435.1998.00233.x · Cited by 641 · see citing works
Projected 21st century decrease in marine productivity: a multi-model analysis
Steinacher, M., Joos, F., Frölicher, T. L., Bopp, L., Cadule, P., Cocco, V., Doney, S. C., Gehlen, M., Lindsay, K., Moore, J. K., et al. (2010) · Biogeosciences · doi:10.5194/bg-7-979-2010 · Cited by 635 · see citing works
Increasing importance of small phytoplankton in a warmer ocean
Morán, X. A. G., López‐Urrutia, Á., Calvo‐Díaz, A., & Li, W. K. W. (2009) · Global Change Biology · doi:10.1111/j.1365-2486.2009.01960.x · Cited by 610 · see citing works
Intrinsic rate of natural increase: The relationship with body size
Fenchel, T. (1974) · Oecologia · doi:10.1007/bf00384576 · Cited by 610 · see citing works
Diatoms and the Ocean Carbon Cycle
Smetacek, V. S. (1999) · Protist · doi:10.1016/s1434-4610(99)70006-4 · Cited by 608 · see citing works
Scaling the metabolic balance of the oceans
López‐Urrutia, Á., Martin, E. S., Harris, R., & Irigoien, X. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601137103 · Cited by 591 · see citing works
Agricultural runoff fuels large phytoplankton blooms in vulnerable areas of the ocean
Michael Beman, J., Arrigo, K. R., & Matson, P. A. (2005) · Nature · doi:10.1038/nature03370 · Cited by 581 · see citing works
Warming and Resource Availability Shift Food Web Structure and Metabolism
O’Connor, M. I., Piehler, M. F., Leech, D. M., Antón, A., & Bruno, J. F. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000178 · Cited by 560 · see citing works
Warming-induced reductions in body size are greater in aquatic than terrestrial species
Forster, J., Hirst, A. G., & Atkinson, D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210460109 · Cited by 557 · see citing works
Chisholm, S. W. (1992) · Springer eBooks · doi:10.1007/978-1-4899-0762-2_12 · Cited by 553 · see citing works
Resurrecting the Ecological Underpinnings of Ocean Plankton Blooms
Behrenfeld, M. J., & Boss, E. (2013) · Annual Review of Marine Science · doi:10.1146/annurev-marine-052913-021325 · Cited by 505 · see citing works
Doney, S. C. (2006) · Nature · doi:10.1038/444695a · Cited by 481 · see citing works
Understanding the export of biogenic particles in oceanic waters: Is there consensus?
Boyd, P. W., & Trull, T. W. (2006) · Progress In Oceanography · doi:10.1016/j.pocean.2006.10.007 · Cited by 473 · see citing works
Response of diatoms distribution to global warming and potential implications: A global model study
Bopp, L., Aumont, O., Cadule, P., Alvain, S., & Gehlen, M. (2005) · Geophysical Research Letters · doi:10.1029/2005gl023653 · Cited by 455 · see citing works
Mix and match: how climate selects phytoplankton
Falkowski, P. G., & Oliver, M. J. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1751 · Cited by 443 · see citing works
DeLong, J. P., Okie, J. G., Moses, M. E., Sibly, R. M., & Brown, J. H. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1007783107 · Cited by 442 · see citing works
Phytoplankton blooms: a ‘loophole’ in microzooplankton grazing impact?
Irigoien, X., Flynn, K. J., & Harris, R. (2005) · Journal of Plankton Research · doi:10.1093/plankt/fbi011 · Cited by 437 · see citing works
Edwards, K. F., Thomas, M. K., Klausmeier, C. A., & Litchman, E. (2012) · Limnology and Oceanography · doi:10.4319/lo.2012.57.2.0554 · Cited by 414 · see citing works
Protists decrease in size linearly with temperature:ca. 2.5% °C−1
Atkinson, D., Ciotti, B. J., & Montagnes, D. J. S. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2003.2538 · Cited by 375 · see citing works
The biogeography of marine plankton traits
Barton, A. D., Pershing, A. J., Litchman, E., Record, N. R., Edwards, K. F., Finkel, Z. V., Kiørboe, T., & Ward, B. A. (2013) · Ecology Letters · doi:10.1111/ele.12063 · Cited by 375 · see citing works
Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems
Yvon‐Durocher, G., Montoya, J. M., Trimmer, M., & Woodward, G. (2010) · Global Change Biology · doi:10.1111/j.1365-2486.2010.02321.x · Cited by 374 · see citing works
Banse, K. (1982) · Limnology and Oceanography · doi:10.4319/lo.1982.27.6.1059 · Cited by 365 · see citing works
A size‐structured food‐web model for the global ocean
Ward, B. A., Dutkiewicz, S., Jahn, O., & Follows, M. J. (2012) · Limnology and Oceanography · doi:10.4319/lo.2012.57.6.1877 · Cited by 361 · see citing works
Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake and use
Emilio Marañón, C., Cermeño, P., López‐Sandoval, D. C., Rodríguez‐Ramos, T., Sobrino, C., Huete‐Ortega, M., Blanco, J. M., & Rodríguez, J. (2012) · Ecology Letters · doi:10.1111/ele.12052 · Cited by 360 · see citing works
Montagnes, D. J. S., & Franklin, M. (2001) · Limnology and Oceanography · doi:10.4319/lo.2001.46.8.2008 · Cited by 340 · see citing works
Guidi, L., Stemmann, L., Jackson, G. A., et al. (2009) · Limnology and Oceanography · doi:10.4319/lo.2009.54.6.1951 · Cited by 339 · see citing works
Curvature in metabolic scaling
Kolokotrones, T., Savage, V. M., Deeds, E. J., & Fontana, W. (2010) · Nature · doi:10.1038/nature08920 · Cited by 337 · see citing works
Calbet, A. (2001) · Limnology and Oceanography · doi:10.4319/lo.2001.46.7.1824 · Cited by 336 · see citing works
The trophic roles of microzooplankton in marine systems
Calbet, A. (2008) · ICES Journal of Marine Science · doi:10.1093/icesjms/fsn013 · Cited by 328 · see citing works
A theoretical model for nutrient uptake in phytoplankton
Aksnes, D. L., & Egge, J. (1991) · Marine Ecology Progress Series · doi:10.3354/meps070065 · Cited by 321 · see citing works
Climate change and the timing, magnitude, and composition of the phytoplankton spring bloom
Sommer, U. J., & Lengfellner, K. (2008) · Global Change Biology · doi:10.1111/j.1365-2486.2008.01571.x · Cited by 313 · see citing works
Modeling Diverse Communities of Marine Microbes
Follows, M. J., & Dutkiewicz, S. (2011) · Annual Review of Marine Science · doi:10.1146/annurev-marine-120709-142848 · Cited by 307 · see citing works
Patterns of phytoplankton size structure and productivity in contrasting open-ocean environments
Marañón, E., Holligan, P. M., Barciela, R. M., et al. (2001) · Marine Ecology Progress Series · doi:10.3354/meps216043 · Cited by 302 · see citing works
Self-citationTransport limitation of nutrient uptake in phytoplankton1
Pasciak, W. J., & Gavis, J. (1974) · Limnology and Oceanography · doi:10.4319/lo.1974.19.6.0881 · Cited by 291 · see citing works
Schmoker, C., Hernández‐León, S., & Calbet, A. (2013) · Journal of Plankton Research · doi:10.1093/plankt/fbt023 · Cited by 285 · see citing works
Whale-Fall Ecosystems: Recent Insights into Ecology, Paleoecology, and Evolution
Smith, C. R., Glover, A. G., Treude, T., Higgs, N. D., & Amon, D. J. (2014) · Annual Review of Marine Science · doi:10.1146/annurev-marine-010213-135144 · Cited by 275 · see citing works
Picoplanktonic community structure on an Atlantic transect from 50°N to 50°S
Zubkov, M. V., Sleigh, M. A., Tarran, G. A., Burkill, P. H., & Leakey, R. J. G. (1998) · Deep Sea Research Part I Oceanographic Research Papers · doi:10.1016/s0967-0637(98)00015-6 · Cited by 272 · see citing works
Microbial food webs and the export of biogenic carbon in oceans
Legendre, L., & Fèvre, J. L. (1995) · Aquatic Microbial Ecology · doi:10.3354/ame009069 · Cited by 272 · see citing works
Light absorption and size scaling of light‐limited metabolism in marine diatoms
Finkel, Z. V. (2001) · Limnology and Oceanography · doi:10.4319/lo.2001.46.1.0086 · Cited by 269 · see citing works
Kruskopf, M., & Flynn, K. J. (2005) · New Phytologist · doi:10.1111/j.1469-8137.2005.01601.x · Cited by 265 · see citing works
A Mechanistic Approach to Plankton Ecology
Kiørboe, T. (2018) · Princeton University Press eBooks · doi:10.2307/j.ctv39x7mp · Cited by 259 · see citing works
Food-web mediated export of biogenic carbon in oceans:hydrodynamic control
Legendre, L., & Rassoulzadegan, F. (1996) · Marine Ecology Progress Series · doi:10.3354/meps145179 · Cited by 258 · see citing works
Cavender‐Bares, K. K., Karl, D. M., & Chisholm, S. W. (2001) · Deep Sea Research Part I Oceanographic Research Papers · doi:10.1016/s0967-0637(01)00027-9 · Cited by 246 · see citing works
Temperature, resources, and phytoplankton size structure in the ocean
Marañón, E., Cermeño, P., Latasa, M., et al. (2012) · Limnology and Oceanography · doi:10.4319/lo.2012.57.5.1266 · Cited by 242 · see citing works
Self-citationMesoscale vertical motion and the size structure of phytoplankton in the ocean
Rodríguez, J., Tintoré, J., Allen, J. T., et al. (2001) · Nature · doi:10.1038/35066560 · Cited by 233 · see citing works
Clarke, A., Meredith, M. P., Wallace, M. I., et al. (2008) · Deep Sea Research Part II Topical Studies in Oceanography · doi:10.1016/j.dsr2.2008.04.035 · Cited by 226 · see citing works
Basin-scale variability of phytoplankton biomass, production and growth in the Atlantic Ocean
Marañón, E., Holligan, P. M., Varela, M., et al. (2000) · Deep Sea Research Part I Oceanographic Research Papers · doi:10.1016/s0967-0637(99)00087-4 · Cited by 221 · see citing works
Self-citationLandry, M., Constantinou, J., Latasa, M., et al. (2000) · Marine Ecology Progress Series · doi:10.3354/meps201057 · Cited by 220 · see citing works
The allometry of algal growth rates
Tang, E. P. Y. (1995) · Journal of Plankton Research · doi:10.1093/plankt/17.6.1325 · Cited by 216 · see citing works
Armstrong, R. A. (1994) · Limnology and Oceanography · doi:10.4319/lo.1994.39.3.0597 · Cited by 208 · see citing works
A Mechanistic Approach to Plankton Ecology
Kiørboe, T. (2009) · Princeton University Press eBooks · doi:10.1515/9780691190310 · Cited by 208 · see citing works
Size dependence of growth and photosynthesis in diatoms: a synthesis
Geider, R., Piatt, T., & Raven, J. (1986) · Marine Ecology Progress Series · doi:10.3354/meps030093 · Cited by 204 · see citing works
Strom, S., Macri, E., & Olson, M. B. (2007) · Limnology and Oceanography · doi:10.4319/lo.2007.52.4.1480 · Cited by 195 · see citing works
Karentz, D., & Smayda, T. J. (1984) · Marine Ecology Progress Series · doi:10.3354/meps018277 · Cited by 188 · see citing works
Resource limitation alters the 3/4 size scaling of metabolic rates in phytoplankton
Finkel, Z. V., Irwin, A. J., & Schofield, O. (2004) · Marine Ecology Progress Series · doi:10.3354/meps273269 · Cited by 188 · see citing works
SIZE‐DEPENDENT PHOSPHORUS UPTAKE KINETICS AND CELL QUOTA IN PHYTOPLANKTON1
SMITH, R. E. H., & Kalff, J. (1982) · Journal of Phycology · doi:10.1111/j.1529-8817.1982.tb03184.x · Cited by 173 · see citing works
Marañón, E., Behrenfeld, M., González, N., et al. (2003) · Marine Ecology Progress Series · doi:10.3354/meps257001 · Cited by 172 · see citing works
Self-citationThingstad, T. F., Øvreås, L., Egge, J. K., Løvdal, T., & Heldal, M. (2005) · Ecology Letters · doi:10.1111/j.1461-0248.2005.00768.x · Cited by 170 · see citing works
Ward, B. A., Dutkiewicz, S., & Follows, M. J. (2013) · Journal of Plankton Research · doi:10.1093/plankt/fbt097 · Cited by 167 · see citing works
Determination of nutrient uptake kinetic parameters: a comparison of methods
Harrison, P., Parslow, J., & Conway, H. (1989) · Marine Ecology Progress Series · doi:10.3354/meps052301 · Cited by 167 · see citing works
Stæhr, P. A. U., & Sand‐Jensen, K. (2005) · Freshwater Biology · doi:10.1111/j.1365-2427.2005.01490.x · Cited by 164 · see citing works
Nutrient Limitation of Marine Photosynthesis
Cullen, J. J., Yang, X., & MacIntyre, H. L. (1992) · Springer eBooks · doi:10.1007/978-1-4899-0762-2_5 · Cited by 162 · see citing works
Cermeño, P., Marañón, E., Pérez, V., et al. (2006) · Estuarine Coastal and Shelf Science · doi:10.1016/j.ecss.2005.11.027 · Cited by 159 · see citing works
Self-citationCapacity of herbivorous protists to control initiation and development of mass phytoplankton blooms
Sherr, E. B., & Sherr, B. (2009) · Aquatic Microbial Ecology · doi:10.3354/ame01358 · Cited by 148 · see citing works
Raven, J. A. (1987) · New Phytologist · doi:10.1111/j.1469-8137.1987.tb00149.x · Cited by 145 · see citing works
Effect of phytoplankton cell size on transient-state nitrate and ammonium uptake kinetics
Stolte, W., & Riegman, R. (1995) · Microbiology · doi:10.1099/13500872-141-5-1221 · Cited by 144 · see citing works
Chen, B., & Liu, H. (2010) · Limnology and Oceanography · doi:10.4319/lo.2010.55.3.0965 · Cited by 137 · see citing works
The Importance of Respiration Losses in Controlling the Size Distribution of Marine Phytoplankton
Laws, E. A. (1975) · Ecology · doi:10.2307/1934972 · Cited by 133 · see citing works
Scaling of phytoplankton photosynthesis and cell size in the ocean
Maraóón, E., Cermeóo, P., Rodríguez, J., Zubkov, M. V., & Harris, R. (2007) · Limnology and Oceanography · doi:10.4319/lo.2007.52.5.2190 · Cited by 129 · see citing works
Self-citationPhytoplankton Cell Size Reduction in Response to Warming Mediated by Nutrient Limitation
Peter, K. H., & Sommer, U. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071528 · Cited by 125 · see citing works
Cermeño, P., Marañón, E., Rodríguez, J., et al. (2005) · Marine Ecology Progress Series · doi:10.3354/meps297051 · Cited by 118 · see citing works
Self-citationResource Supply Overrides Temperature as a Controlling Factor of Marine Phytoplankton Growth
Emilio Marañón, C., Cermeño, P., Huete‐Ortega, M., López‐Sandoval, D. C., Mouriño‐Carballido, B., & Rodríguez‐Ramos, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099312 · Cited by 114 · see citing works
Villareal, T. A., Woods, S., Moore, J. K., & Culver-Rymsza, K. (1996) · Journal of Plankton Research · doi:10.1093/plankt/18.7.1103 · Cited by 109 · see citing works
Pigment specific growth and grazing rates of phytoplankton in the central equatorial Pacific
Latasa, M., Landry, M. R., Schlüter, L., et al. (1997) · Limnology and Oceanography · doi:10.4319/lo.1997.42.2.0289 · Cited by 107 · see citing works
Isometric size-scaling of metabolic rate and the size abundance distribution of phytoplankton
Huete‐Ortega, M., Cermeño, P., Calvo‐Díaz, A., & Emilio Marañón, C. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2011.2257 · Cited by 105 · see citing works
Evaluation of In Situ Phytoplankton Growth Rates: A Synthesis of Data from Varied Approaches
Laws, E. A. (2013) · Annual Review of Marine Science · doi:10.1146/annurev-marine-121211-172258 · Cited by 103 · see citing works
Reul, A., Rodrı́guez, V., Jiménez‐Gómez, F., Blanco, J. M., Bautista, B., Sarhan, T., Guerrero, F., Ruiz, J., & García‐Lafuente, J. (2005) · Continental Shelf Research · doi:10.1016/j.csr.2004.09.016 · Cited by 102 · see citing works
Rodríguez, J., Blanco, J. M., Jiménez‐Gómez, F., et al. (1998) · Deep Sea Research Part I Oceanographic Research Papers · doi:10.1016/s0967-0637(98)00030-2 · Cited by 93 · see citing works
Maximal growth rates of Antarctic phytoplankton: Only weak dependence on cell size
Sommer, U. J. (1989) · Limnology and Oceanography · doi:10.4319/lo.1989.34.6.1109 · Cited by 93 · see citing works
Phytoplankton growth rates in the Atlantic subtropical gyres
Emilio Marañón, C. (2005) · Limnology and Oceanography · doi:10.4319/lo.2005.50.1.0299 · Cited by 92 · see citing works
Blasco, D., Packard, T. T., & Garfield, P. C. (1982) · Journal of Phycology · doi:10.1111/j.1529-8817.1982.tb03156.x · Cited by 91 · see citing works
Size-structured planktonic ecosystems: constraints, controls and assembly instructions
Poulin, F., & Franks, P. J. S. (2010) · Journal of Plankton Research · doi:10.1093/plankt/fbp145 · Cited by 89 · see citing works
López-Sandoval, D. C., Rodríguez-Ramos, T., Cermeño, P., Sobrino, C., & Marañón, E. (2014) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2014.04.013 · Cited by 88 · see citing works
Self-citationWhy are there no picoplanktonic O2 evolvers with volumes less than 10−19 m3?
Raven, J. A. (1994) · Journal of Plankton Research · doi:10.1093/plankt/16.5.565 · Cited by 85 · see citing works
The allometry of algal respiration
Tang, E. P. Y., & Peters, R. H. (1995) · Journal of Plankton Research · doi:10.1093/plankt/17.2.303 · Cited by 80 · see citing works
Competitive dynamics in two species of marine phytoplankton under non-equilibrium conditions
Cermeño, P., Lee, J. B., Wyman, K., Schofield, O., & Falkowski, P. G. (2011) · Marine Ecology Progress Series · doi:10.3354/meps09088 · Cited by 77 · see citing works
Tadonléké, R. D. (2010) · Limnology and Oceanography · doi:10.4319/lo.2010.55.3.0973 · Cited by 76 · see citing works
Growth rate peaks at intermediate cell size in marine photosynthetic picoeukaryotes
Bec, B., Collos, Y., Vaquer, A., et al. (2008) · Limnology and Oceanography · doi:10.4319/lo.2008.53.2.0863 · Cited by 72 · see citing works
Summer Diatom Blooms in the North Pacific Subtropical Gyre: 2008–2009
Villareal, T. A., Brown, C. G., Brzezinski, M. A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033109 · Cited by 72 · see citing works
Inter-specific scaling of phytoplankton production and cell size in the field
Emilio Marañón, C. (2007) · Journal of Plankton Research · doi:10.1093/plankt/fbm087 · Cited by 67 · see citing works
Size-Dependent Variations in Plant Growth Rates and the "¾ Power Rule"
Niklas, K. J. (1994) · American Journal of Botany · doi:10.1002/j.1537-2197.1994.tb15422.x · Cited by 60 · see citing works
Invariant scaling of phytoplankton abundance and cell size in contrasting marine environments
Cermeño, P., Emilio Marañón, C., Harbour, D., & Harris, R. (2006) · Ecology Letters · doi:10.1111/j.1461-0248.2006.00973.x · Cited by 60 · see citing works
Huete‐Ortega, M., Marañón, E., Varela, M., et al. (2009) · Journal of Plankton Research · doi:10.1093/plankt/fbp104 · Cited by 58 · see citing works
Self-citationMarañón, E. (2009) · Elsevier eBooks · doi:10.1016/b978-012374473-9.00661-5 · Cited by 56 · see citing works
Self-citationEstimating the carbon flux through main phytoplankton groups in the northwestern Mediterranean
Latasa, M., Morán, X. A. G., Scharek, R., et al. (2005) · Limnology and Oceanography · doi:10.4319/lo.2005.50.5.1447 · Cited by 54 · see citing works
Non-uniform scaling in phytoplankton growth rate due to intracellular light and CO2 decline
Wirtz, K. (2011) · Journal of Plankton Research · doi:10.1093/plankt/fbr021 · Cited by 50 · see citing works
Exudation of organic carbon by marine phytoplankton: dependence on taxon and cell size
López‐Sandoval, D. C., Rodríguez‐Ramos, T., Cermeño, P., & Emilio Marañón, C. (2012) · Marine Ecology Progress Series · doi:10.3354/meps10174 · Cited by 47 · see citing works
Species richness and cell-size distribution: size structure of phytoplankton communities
Cermeño, P., & Figueiras, F. G. (2007) · Marine Ecology Progress Series · doi:10.3354/meps07293 · Cited by 41 · see citing works
Arbones, B., Castro, C. G., Alonso‐Pérez, F., et al. (2007) · Aquatic Microbial Ecology · doi:10.3354/ame01160 · Cited by 38 · see citing works
Size dependence of coastal phytoplankton photosynthesis under vertical mixing conditions
Cermeño, P., Marañón, E., Rodríguez, J., et al. (2005) · Journal of Plankton Research · doi:10.1093/plankt/fbi021 · Cited by 31 · see citing works
Self-citationResource levels, allometric scaling of population abundance, and marine phytoplankton diversity
Cermeño, P., Marañín, E., Harbour, D., Figueiras, F. G., Crespo, B. G., Huete‐Ortega, M., Varela, M., & Harris, R. (2008) · Limnology and Oceanography · doi:10.4319/lo.2008.53.1.0312 · Cited by 30 · see citing works
Self-citationTeixeira, I. G., Figueiras, F. G., Crespo, B. G., et al. (2010) · Estuarine Coastal and Shelf Science · doi:10.1016/j.ecss.2010.10.012 · Cited by 28 · see citing works
Gutiérrez‐Rodríguez, A., Latasa, M., Agustı́, S., & Duarte, C. M. (2011) · Deep Sea Research Part I Oceanographic Research Papers · doi:10.1016/j.dsr.2011.08.003 · Cited by 22 · see citing works
Size-Dependent Variations in Plant Growth Rates and the "¾ Power Rule"
Niklas, K. J. (1994) · American Journal of Botany · doi:10.2307/2445626 · Cited by 21 · see citing works
Chang, F., Marquis, E., Chang, C., et al. (2013) · Biogeosciences · doi:10.5194/bg-10-5267-2013 · Cited by 12 · see citing works
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Nitrogen and phosphorus stress as a tool to induce lipid production in microalgae
Maltsev, Y., Kulikovskiy, M., & Maltseva, S. (2023) · Microbial Cell Factories · doi:10.1186/s12934-023-02244-6 · Cited by 174 · see citing works
“Small species show similar specific volume V (max N) compared to their larger counterparts but have higher nitrogen requirements [96].”
BackgroundAlgal Diversity and Traits Predict Biomass Yield and Grazing Resistance in Wastewater Cultivation
Thomas, P. K., Dunn, G. P., Coats, E. R., Newby, D. T., & Feris, K. P. (2019) · Journal of Applied Phycology · doi:10.1007/s10811-019-01764-2 · Cited by 26 · see citing works
- Authors
- Marañón, E.
- Affiliations
- Departamento de Ecología y Biología Animal, Universidade de Vigo, 36310 Vigo, Spain;
- Venue
- Annual Review of Marine Science
- Publisher
- Annual Reviews
- Published
- 2015-01-03
- Volume
- 7
- Issue
- 1
- Pages
- 241-264
- ISSN
- 1941-0611 (ISSN-L)
- 1941-1405
- OpenAlex
- W2124304330
- Cited by
- 514
- References
- 131
- Citations by year
- 2026: 37 · 2025: 62 · 2024: 60 · 2023: 45 · 2022: 52 · 2021: 50 · 2020: 51 · 2019: 37 · 2018: 49 · 2017: 31 · 2016: 26 · 2015: 14
- FWCI
- 2.09
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annual Review of Marine Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine and coastal ecosystems
- Physical Sciences › Environmental Science › Environmental Chemistry › Aquatic Ecosystems and Phytoplankton Dynamics
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- phytoplankton size structure, cell size, phytoplankton metabolism, allometric scaling, nutrient uptake rate, growth rate, phytoplankton blooms, trophic organization, resource supply, biogeographic patterns
- MeSH terms
- Energy Metabolism, Environmental Monitoring, Eutrophication, Models, Theoretical, Oceans and Seas, Phytoplankton, Seawater, Biomass
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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