in

Phytoplankton community structuring and succession in a competition-neutral resource landscape

  • 1.

    MacArthur, R. H., Wilson, E. O. The theory of island biogeography. in Monographs in Population Biology (Princeton University Press, Princeton, NJ, 1967)

  • 2.

    Hubbell, S. P. The unified neutral theory of biodiversity and biogeography. in Monographs in Population Biology, Vol. 32 (Princeton University Press, Princeton, NJ, 2001).

  • 3.

    Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Google Scholar 

  • 4.

    Ryther, J. Photosynthesis and fish production in the sea. Science 166, 72–76 (1969).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 5.

    Cushing, D. A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified. J. Plankton Res. 11, 1–13 (1989).

    Article 

    Google Scholar 

  • 6.

    Barber, R. T. & Hiscock, M. R. A rising tide lifts all phytoplankton: growth response of other phytoplankton taxa in diatom‐dominated blooms. Glob. Biogeoch. Cycl. 20, GB4S03 (2006).

    Google Scholar 

  • 7.

    Siegel, D. A. et al. Global assessment of ocean carbon export by combining satellite observations and food-web models. Global Biogeochem. Cycl. 28, 181–196 (2014).

    CAS 
    Article 

    Google Scholar 

  • 8.

    Buesseler, K. O., Boyd, P. W., Black, E. E. & Siegel, D. A. Metrics that matter for assessing the ocean biological carbon pump. Proc. Natl Acad. Sci. USA 117, 9679–9687 (2020).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 9.

    Irwin, A. J., Finkel, Z. V., Schofield, O. M. & Falkowski, P. G. Scaling-up from nutrient physiology to the size-structure of phytoplankton communities. J. Plankt. Res. 28, 459–471 (2006).

    Article 

    Google Scholar 

  • 10.

    Litchman, E., Klausmeier, C. A. & Yoshiyama, K. Contrasting size evolution in marine and freshwater diatoms. Proc. Natl Acad. Sci. USA 106, 2665–2670 (2009).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 11.

    Tozzi, S., Schofield, O. & Falkowski, P. Historical climate change and ocean turbulence as selective agents for two key phytoplankton functional groups. Mar. Ecol. Prog. Ser. 274, 123–132 (2004).

    Article 

    Google Scholar 

  • 12.

    Follows, M. J., Dutkiewicz, S., Grant, S. & Chisholm, S. W. Emergent biogeography of microbial communities in a model ocean. Science 315, 1843–1846 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 13.

    Gregg, W. W., Casey, N. W. & Rousseaux, C. S. Global surface ocean carbon estimates in a model forced by MERRA NASA Technical Report Series on Global Modeling and Data Assimilation. NASA TM-2013-104606, Vol. 31, 39 (2013).

  • 14.

    Hulburt, E. M. Competition for nutrients by marine phytoplankton in oceanic, coastal, and estuarine regions. Ecology 51, 475–484 (1970).

    Article 

    Google Scholar 

  • 15.

    Siegel, D. A. Resource competition in a discrete environment: why are plankton distributions paradoxical? Limnol. Oceanogr. 43, 1133–1146 (1998).

    Article 

    Google Scholar 

  • 16.

    Cyr, H., Peters, R. H. & Downing, J. A. Population density and community size structure: comparison of aquatic and terrestrial systems. Oikos 80, 139–149 (1997).

    Article 

    Google Scholar 

  • 17.

    White, E. P., Ernest, S. M., Kerkhoff, A. J. & Enquist, B. J. Relationships between body size and abundance in ecology. Trends Ecol. Evol. 22, 323–330 (2007).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 18.

    McCauley, D. J. et al. On the prevalence and dynamics of inverted trophic pyramids and otherwise top-heavy communities. Ecol. Lett. 21, 439–454 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 19.

    West, G. B., Brown, J. H. & Enquist, B. J. A general model for the origin of allometric scaling laws in biology. Science 276, 122–126 (1997).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 20.

    West, G. B., Brown, J. H. & Enquist, B. J. The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284, 1677–1679 (1999).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 21.

    Sheldon, R. W., Prakash, A. & Sutcliffe, W. Jr The size distribution of particles in the Ocean 1. Limnol. Oceanogr. 17, 327–340 (1972).

    Article 

    Google Scholar 

  • 22.

    Jonasz, M. & Fournier, G. Light Scattering by Particles in Water: Theoretical and Experimental Foundations. (Elsevier, 2011).

  • 23.

    Huete-Ortega, M., Cermeno, P., Calvo-Díaz, A. & Maranon, E. Isometric size-scaling of metabolic rate and the size abundance distribution of phytoplankton. Proc. Royal Soc. B 279, 1815–1823 (2012).

    Article 

    Google Scholar 

  • 24.

    Marañón, E. Cell size as a key determinant of phytoplankton metabolism and community structure. Annu. Rev. Mar. Sci. 7, 241–264 (2015).

    Article 

    Google Scholar 

  • 25.

    Riley, G. A., Stommel, H. M., Bumpus, D. F. Quantitative ecology of the plankton of the western North Atlantic. Bulletin of the Bingham Oceanographic Collection 12 (Yale Univ., New Haven, CT, 1949)

  • 26.

    Evans, G. T. & Parslow, J. S. A model of annual plankton cycles. Biol. Oceanogr. 3, 327–347 (1985).

    Google Scholar 

  • 27.

    Margalef, R. Perspectives in Ecological Theory. 111 pp (Univ. Chicago Press, Chicago, Ill, 1968).

  • 28.

    Behrenfeld, M. J. & Boss, E. S. Resurrecting the ecological underpinnings of ocean plankton blooms. Ann. Rev. Mar. Sci. 6, 167–194 (2014).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 29.

    Behrenfeld, M. J. & Boss, E. S. Student’s tutorial on bloom hypotheses in the context of phytoplankton annual cycles. Glob. Change Biol. 24, 55–77 (2018).

    Article 

    Google Scholar 

  • 30.

    Strom, S. L. & Buskey, E. J. Feeding, growth, and behavior of the thecate heterotrophic dinoflagellate Oblea rotunda. Limnol. Oceanogr. 38, 965–977 (1993).

    Article 

    Google Scholar 

  • 31.

    Strom, S. L., Macri, E. L. & Olson, M. B. Microzooplankton grazing in the coastal Gulf of Alaska: Variations in top-down control of phytoplankton. Limnol. Oceanogr. 52, 1480–1494 (2007).

    Article 

    Google Scholar 

  • 32.

    Wirtz, K. W. Who is eating whom? Morphology and feeding type determine the size relation between planktonic predators and their ideal prey. Mar. Ecol. Progr. Ser. 445, 1–12 (2012).

    Article 

    Google Scholar 

  • 33.

    Kiørboe, T. How zooplankton feed: mechanisms, traits and trade-offs. Biol. Rev. 86, 311–339 (2011).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 34.

    Hansen, B., Bjornsen, P. K. & Hansen, P. J. The size ratio between planktonic predators and their prey. Limnol. Oceanogr. 39, 395–403 (1994).

    Article 

    Google Scholar 

  • 35.

    Sommer, U. & Sommer, F. Cladocerans versus copepods: the cause of contrasting top–down controls on freshwater and marine phytoplankton. Oecologia 147, 183–194 (2006).

    PubMed 
    Article 

    Google Scholar 

  • 36.

    Hébert, M.-P., Beisner, B. E. & Maranger, R. Linking zooplankton communities to ecosystem functioning: Toward an effect-trait framework. J. Plankton Res. 39, 3–12 (2017).

    Article 
    CAS 

    Google Scholar 

  • 37.

    Fuchs, H. L. & Franks, P. J. Plankton community properties determined by nutrients and size-selective feeding. Mar. Ecol. Progr. Ser. 413, 1–15 (2010).

    Article 

    Google Scholar 

  • 38.

    Sutherland, K. R., Madin, L. P. & Stocker, R. Filtration of submicrometer particles by pelagic tunicates. Proc. Natl Acad. Sci. USA 107, 15129–15134 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 39.

    Dadon-Pilosof, A., Lombard, F., Genin, A., Sutherland, K. R. & Yahel, G. Prey taxonomy rather than size determines salp diets. Limnol. Oceanogr. 64, 1996–2010 (2019).

    Article 

    Google Scholar 

  • 40.

    Antoine, D., Andre, J. M. & Morel, A. Oceanic primary production 2. Estimation at global scale from satellite (coastal zone color scanner) chlorophyll. Global Biogeochem. Cycl. 10, 57–69 (1996).

    CAS 
    Article 

    Google Scholar 

  • 41.

    Brewin, R. J. W. et al. A three-component model of phytoplankton size class for the Atlantic Ocean. Ecol. Model. 221, 1472–1483 (2010).

    CAS 
    Article 

    Google Scholar 

  • 42.

    Marañón, E., Cermeño, P., Latasa, M. & Tadonléké, R. D. Temperature, resources, and phytoplankton size structure in the ocean. Limnol. Oceanogr. 5, 1266–1278 (2012).

    Article 

    Google Scholar 

  • 43.

    Kerr, S. R., Dickie, L. M. The Biomass Spectrum: a Predator-prey Theory of Aquatic Production (Columbia University Press, 2001).

  • 44.

    Behrenfeld, M. J., et al. Annual boom-bust cycles of polar phytoplankton biomass revealed by space-based lidar. Nat. Geosci. 2017; https://doi.org/10.1038/NGEO2861.

  • 45.

    Kiorboe, T. Turbulence, phytoplankton cell size, and the structure of pelagic food-webs. Adv. Mar. Biol. 29, 1–72 (1993).

    Article 

    Google Scholar 

  • 46.

    DeLong, J. P. & Vasseur, D. A. Size-density scaling in protists and the links between consumer–resource interaction parameters. J. Animal Ecol. 81, 1193–1201 (2012).

    Article 

    Google Scholar 

  • 47.

    Smetacek, V. Diatoms and the ocean carbon cycle. Protist 150, 25–32 (1999).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 48.

    Smetacek, V., Assmy, P. & Henjes, J. The role of grazing in structuring Southern Ocean pelagic ecosystems and biogeochemical cycles. Antarct. Sci. 16, 541–558 (2004).

    Article 

    Google Scholar 

  • 49.

    Behrenfeld, M. J., Halsey, K. H., Boss, E., Karp-Boss, L., Milligan, A. J. & Peers, G. Thoughts on the evolution and ecological niche of diatoms. Ecol. Monogr. 2021; in press.

  • 50.

    Glibert, P. M. Margalef revisited: a new phytoplankton mandala incorporating twelve dimensions, including nutritional physiology. Harmful Algae 55, 25–30 (2016).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 51.

    Margalef, R. Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanolog. Acta 1, 493–509 (1978).

    Google Scholar 

  • 52.

    Cullen, J. J. & MacIntyre, J. G. Behavior, physiology and the niche of depth-regulating phytoplankton. Nato ASI Ser. G Ecol. Sci. 41, 559–580 (1998).

  • 53.

    Kemp, A. E. & Villareal, T. A. The case of the diatoms and the muddled mandalas: Time to recognize diatom adaptations to stratified waters. Prog. Oceanogr. 167, 138–149 (2018).

    Article 

    Google Scholar 

  • 54.

    Kudela, R. M. Does horizontal mixing explain phytoplankton dynamics? Proc. Natl Acad. Sci. USA 107, 18235–18236 (2010).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 55.

    Wyatt, T. Margalef’s mandala and phytoplankton bloom strategies. Deep Sea Res. II 101, 32–49 (2014).

    Article 

    Google Scholar 

  • 56.

    Waite, A., Fisher, A., Thompson, P. A. & Harrison, P. J. Sinking rate versus cell volume relationships illuminate sinking rate control mechanisms in marine diatoms. Mar. Ecol. Prog. Ser. 157, 97–108 (1997).

    Article 

    Google Scholar 

  • 57.

    Moore, J. K. & Villareal, T. A. Size-ascent rate relationships in positively buoyant marine diatoms. Limnol. Oceanogr. 41, 1514–1520 (1996).

    Article 

    Google Scholar 

  • 58.

    Bienfang, P. & Szyper, J. Effects of temperature and salinity on sinking rates of the centric diatom Ditylum brightwellii. Biol. Oceanogr. 1, 211–223 (1982).

    Google Scholar 

  • 59.

    Bienfang, P., Szyper, J. & Laws, E. Sinking rate and pigment responses to light-limitation of a marine diatom – implications to dynamics of chlorophyll maximum layers. Oceanolog. Acta 6, 55–62 (1983).

    CAS 

    Google Scholar 

  • 60.

    Villareal, T. A., Pilskaln, C. H., Montoya, J. P. & Dennett, M. Upward nitrate transport by phytoplankton in oceanic waters: balancing nutrient budgets in oligotrophic seas. PeerJ 2, e302 (2014).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 61.

    Irigoien, X., Flynn, K. J. & Harris, R. P. Phytoplankton blooms: a “loophole” in micozooplankton grazing impact? J. Plankton Res. 27, 313–321 (2005).

    Article 

    Google Scholar 

  • 62.

    Bolaños, L. M., et al. Small phytoplankton dominate western North Atlantic biomass. ISME J: 1–12, https://doi.org/10.1038/s41396-020-0636-0 (2020).

  • 63.

    Guillard, R., Kilham, P. The ecology of marine planktonic diatoms. in The Biology of Diatoms, Vol. 13, 372–469 (Blackwell Oxford, 1977).

  • 64.

    Malviya, S. et al. Insights into global diatom distribution and diversity in the world’s ocean. Proc. Natl Acad. Sci. USA 113, E1516–E1525 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 65.

    Barton, A. D., Finkel, Z. V., Ward, B. A., Johns, D. G. & Follows, M. J. On the roles of cell size and trophic strategy in North Atlantic diatom and dinoflagellate communities. Limnol. Oceanogr. 58, 254–266 (2013).

    Article 

    Google Scholar 

  • 66.

    Edwards, K. F. Mixotrophy in nanoflagellates across environmental gradients in the ocean. Proc. Natl Acad. Sci. USA 116, 6211–6220 (2019).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 67.

    Boyd, P. W. Environmental factors controlling phytoplankton processes in the Southern Ocean. J. Phycol. 38, 844–861 (2002).

    Article 

    Google Scholar 

  • 68.

    Fauchereau, N., Tagliabue, A., Bopp, L. & Monteiro, P. M. The response of phytoplankton biomass to transient mixing events in the Southern Ocean. Geophys. Res. Lett. 38, L17601 (2011).

    Article 

    Google Scholar 

  • 69.

    Wolfe, G. V., Steinke, M. & Kirst, G. O. Grazing-activated chemical defence in a unicellular marine alga. Nature 387, 894–897 (1997).

    CAS 
    Article 

    Google Scholar 

  • 70.

    Colin, S. P. & Dam, H. G. Effects of the toxic dinoflagellate Alexandrium fundyense on the copepod Acartia hudsonica: a test of the mechanisms that reduce ingestion rates. Mar. Ecol. Prog. Ser. 248, 55–65 (2003).

    Article 

    Google Scholar 

  • 71.

    Van Donk, E., Ianora, A. & Vos, M. Induced defences in marine and freshwater phytoplankton: a review. Hydrobiol. 668, 3–19 (2011).

    Article 
    CAS 

    Google Scholar 

  • 72.

    Pohnert, G., Steinke, M. & Tollrian, R. Chemical cues, defense metabolites and the shaping of pelagic interspecific interactions. Trends Ecol. Evol. 22, 198–204 (2007).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 73.

    DeMott, W. R. & Moxter, F. Foraging cyanobacteria by copepods: responses to chemical defense and resource abundance. Ecology 72, 1820–1834 (1991).

    Article 

    Google Scholar 

  • 74.

    Ger, K. A., Naus-Wiezer, S., De Meester, L. & Lürling, M. Zooplankton grazing selectivity regulates herbivory and dominance of toxic phytoplankton over multiple prey generations. Limnol. Oceanogr. 64, 1214–1227 (2019).

    Article 

    Google Scholar 

  • 75.

    Smayda, T. J. & Reynolds, C. S. Community assembly in marine phytoplankton: application of recent models to harmful dinoflagellate blooms. J. Plankt. Res. 23, 447–461 (2001).

    Article 

    Google Scholar 

  • 76.

    Acevedo-Trejos, E., Brandt, G., Bruggeman, J. & Merico, A. Mechanisms shaping size structure and functional diversity of phytoplankton communities in the ocean. Sci. Rep 5, 8918 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 77.

    Cuesta, J. A., Delius, G. W. & Law, R. Sheldon spectrum and the plankton paradox: two sides of the same coin—a trait-based plankton size-spectrum model. J. Math. Biol. 76, 67–96 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 78.

    Hutchinson, G. E. Ecological aspects of succession in natural populations. Amer. Nat. 75, 406–418 (1941).

    Article 

    Google Scholar 

  • 79.

    Tilman, D. Resource competition between plankton algae: an experimental and theoretical approach. Ecology 58, 338–348 (1977).

    CAS 
    Article 

    Google Scholar 

  • 80.

    Tilman, D., Mattson, M. & Langer, S. Competition and nutrient kinetics along a temperature gradient: An experimental test of a mechanistic approach to niche theory 1. Limnol. Oceanogr. 26, 1020–1033 (1981).

    Article 

    Google Scholar 

  • 81.

    Sommer, U. Nutrient competition between phytoplankton species in multispecies chemostat experiments. Archiv hydrobiol. 96, 399–416 (1983).

    Google Scholar 

  • 82.

    Sommer, U. Comparison between steady state and non-steady state competition: experiments with natural phytoplankton. Limnol. Oceanogr. 30, 335–346 (1985).

    CAS 
    Article 

    Google Scholar 

  • 83.

    Tilman, D. Resource Competition and Community Structure (Princeton University Press, 1982).

  • 84.

    Sommer, U. The role of competition for resources in phytoplankton succession. in Plankton Ecology. Berlin, Heidelberg: Springer. 1989, pp. 57-106.

  • 85.

    Burd, A. B. & Jackson, G. A. Particle aggregation. Annu. Rev. Mar. Sci. 1, 65–90 (2009).

    Article 

    Google Scholar 

  • 86.

    Kahl, L. A., Vardi, A. & Schofield, O. Effects of phytoplankton physiology on export flux. Mar. Ecol. Prog. Ser. 354, 3–19 (2008).

    CAS 
    Article 

    Google Scholar 

  • 87.

    Guidi, L. et al. Effects of phytoplankton community on production, size and export of large aggregates: a world-ocean analysis. Limnol. Oceanogr. 54, 1951–1963 (2009).

    Article 

    Google Scholar 

  • 88.

    Kiørboe, T., Lundsgaard, C., Olesen, M. & Hansen, J. L. S. Aggregation and sedimentation processes during a spring phytoplankton bloom: a field experiment to test coagulation theory. J. Mar. Res. 52, 297–323 (1994).

    Article 

    Google Scholar 

  • 89.

    Prairie, J. C., Montgomery, Q. W., Proctor, K. W. & Ghiorso, K. S. Effects of phytoplankton growth phase on settling properties of marine aggregates. J. Mar. Sci. Engineer. 7, 265 (2019).

    Article 

    Google Scholar 

  • 90.

    Lima-Mendez, G. et al. Determinants of community structure in the global plankton interactome. Science 348, 6237 (2015).

    Article 
    CAS 

    Google Scholar 

  • 91.

    Sañudo-Wilhelmy, S. A., Gómez-Consarnau, L., Suffridge, C. & Webb, E. A. The role of B vitamins in marine biogeochemistry. Ann. Rev. Mar. Sci. 6, 339–367 (2014).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 92.

    Helliwell, K. E. The roles of B vitamins in phytoplankton nutrition: new perspectives and prospects. New Phytol. 216, 62–68 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 93.

    Chisholm, S. W. et al. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334, 340–343 (1988).

    Article 

    Google Scholar 

  • 94.

    Caputo, A., Nylander, J. A. & Foster, R. A. The genetic diversity and evolution of diatom-diazotroph associations highlights traits favoring symbiont integration. FEMS Microbiol. Lett. 366, fny297 (2019).

    CAS 
    PubMed Central 
    Article 

    Google Scholar 

  • 95.

    Decelle, J. et al. An original mode of symbiosis in open ocean plankton. Proc. Natl Acad. Sci. USA 109, 18000–18005 (2012).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 96.

    Decelle, J. et al. Algal remodeling in a ubiquitous planktonic photosymbiosis. Curr. Biol. 29, 968–978 (2019).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 97.

    Behrenfeld, M. J. et al. The North Atlantic aerosol and marine ecosystem study (NAAMES): science motive and mission overview. Front. Mar. Sci. 6, 122 (2019).

    Article 

    Google Scholar 

  • 98.

    Menden-Deuer, S. & Lessard, E. J. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45, 569–579 (2000).

    CAS 
    Article 

    Google Scholar 


  • Source: Ecology - nature.com

    Negative emissions, positive economy

    Individual US diets show wide variation in water scarcity footprints