1932

Abstract

The biodiversity of the plankton has been interpreted largely through the monocle of competition. The spatial distancing of phytoplankton in nature is so large that cell boundary layers rarely overlap, undermining opportunities for resource-based competitive exclusion. Neutral theory accounts for biodiversity patterns based purely on random birth, death, immigration, and speciation events and has commonly served as a null hypothesis in terrestrial ecology but has received comparatively little attention in aquatic ecology. This review summarizes basic elements of neutral theory and explores its stand-alone utility for understanding phytoplankton diversity. A theoretical framework is described entailing a very nonneutral trophic exclusion principle melded with the concept of ecologically defined neutral niches. This perspective permits all phytoplankton size classes to coexist at any limiting resource level, predicts greater diversity than anticipated from readily identifiable environmental niches but less diversity than expected from pure neutral theory, and functions effectively in populations of distantly spaced individuals.

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2024-01-17
2024-04-13
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Literature Cited

  1. Adler PB, HilleRisLambers J, Levine JM. 2007. A niche for neutrality. Ecol. Lett 10:95104
    [Google Scholar]
  2. Aksnes DL, Egge JK. 1991. A theoretical model for nutrient uptake in phytoplankton. Mar. Ecol. Prog. Ser 70:6572
    [Google Scholar]
  3. Alonso D, Etienne RS, McKane AJ. 2006. The merits of neutral theory. Trends Ecol. Evol. 21:45157
    [Google Scholar]
  4. Armstrong RA. 2003. A hybrid spectral representation of phytoplankton growth and zooplankton response: the “control rod” model of plankton interaction. Deep-Sea Res. II 50:2895916
    [Google Scholar]
  5. Barberán A, Casamayor EO, Fierer N. 2014. The microbial contribution to macroecology. Front. Microbiol. 5:203
    [Google Scholar]
  6. Barton AD, Dutkiewicz S, Flierl G, Bragg J, Follows MJ. 2010. Patterns of diversity in marine phytoplankton. Science 327:150911
    [Google Scholar]
  7. Beckmann A, Schaum CE, Hense I. 2019. Phytoplankton adaptation in ecosystem models.. J. Theor. Biol. 468:6071
    [Google Scholar]
  8. Behrenfeld MJ, Bisson KM, Boss E, Gaube P, Karp-Boss L. 2022. Phytoplankton community structuring in the absence of resource-based competitive exclusion. PLOS ONE 17:e0274183
    [Google Scholar]
  9. Behrenfeld MJ, Boss ES, Halsey KH. 2021a. Phytoplankton community structuring and succession in a competition-neutral resource landscape. ISME Commun 1:12
    [Google Scholar]
  10. Behrenfeld MJ, Halsey KH, Boss E, Karp-Boss L, Milligan AJ, Peers G. 2021b. Thoughts on the evolution and ecological niche of diatoms. Ecol. Monogr. 91:e01457
    [Google Scholar]
  11. Behrenfeld MJ, O'Malley R, Boss E, Karp-Boss L, Mundt C 2021c. Phytoplankton biodiversity and the inverted paradox. ISME Commun 1:52
    [Google Scholar]
  12. Bell G. 2001. Neutral macroecology. Science 293:241318
    [Google Scholar]
  13. Brauer VS, Stomp M, Bouvier T, Fouilland E, Leboulanger C et al. 2015. Competition and facilitation between the marine nitrogen-fixing cyanobacterium Cyanothece and its associated bacterial community. Front. Microbiol 5:795
    [Google Scholar]
  14. Button DK. 1991. Biochemical basis for whole-cell uptake kinetics: specific affinity, oligotrophic capacity, and the meaning of the Michaelis constant. Appl. Environ. Microbiol. 57:203338
    [Google Scholar]
  15. Button DK. 1998. Nutrient uptake by microorganisms according to kinetic parameters from theory as related to cytoarchitecture. Microbiol. Mol. Biol. Rev. 62:63645
    [Google Scholar]
  16. Button DK, Robertson BR. 2001. Determination of DNA content of aquatic bacteria by flow cytometry. Appl. Environ. Microbiol. 67:163645
    [Google Scholar]
  17. Caswell H. 1976. Community structure: a neutral model analysis. Ecol. Monogr. 46:32754
    [Google Scholar]
  18. Chave J. 2004. Neutral theory and community ecology. Ecol. Lett. 7:24153
    [Google Scholar]
  19. Chen J, Liu H, Bai Y, Qi J, Qi W et al. 2022. Mixing regime shapes the community assembly process, microbial interaction and proliferation of cyanobacterial species Planktothrix in a stratified lake. J. Environ. Sci. 115:10313
    [Google Scholar]
  20. Chesson P. 1994. Multispecies competition in variable environments. Theor. Popul. Biol. 45:22776
    [Google Scholar]
  21. Chesson P. 2000. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31:34366
    [Google Scholar]
  22. Chust G, Irigoien X, Chave J, Harris RP. 2013. Latitudinal phytoplankton distribution and the neutral theory of biodiversity. Glob. Ecol. Biogeogr. 22:53143
    [Google Scholar]
  23. Dadon-Pilosof A, Lombard F, Genin A, Sutherland KR, Yahel G. 2019. Prey taxonomy rather than size determines salp diets. Limnol. Oceanogr. 64:19962010
    [Google Scholar]
  24. Darwin C. 1859. On the Origin of Species by Means of Natural Selection London: Murray
  25. Fisher RA. 1922. On the dominance ratio. Proc. R. Soc. Edinb. 42:32141
    [Google Scholar]
  26. Fisher RA. 1930. The Genetical Theory of Natural Selection Oxford, UK: Clarendon
  27. Flynn KJ, Skibinski DO. 2020. Exploring evolution of maximum growth rates in plankton. J. Plankt. Res. 42:497513
    [Google Scholar]
  28. Flynn KJ, Skibinski DO, Lindemann C. 2018. Effects of growth rate, cell size, motion, and elemental stoichiometry on nutrient transport kinetics. PLOS Comput. Biol. 14:e1006118
    [Google Scholar]
  29. Follett CL, Dutkiewicz S, Ribalet F, Zakem E, Caron D et al. 2022. Trophic interactions with heterotrophic bacteria limit the range of Prochlorococcus.. PNAS 119:e2110993118
    [Google Scholar]
  30. Follows MJ, Dutkiewicz S. 2011. Modeling diverse communities of marine microbes. Annu. Rev. Mar. Sci. 3:42751
    [Google Scholar]
  31. Fox JW, Nelson WA, McCauley E. 2010. Coexistence mechanisms and the paradox of the plankton: quantifying selection from noisy data. Ecology 91:177486
    [Google Scholar]
  32. Fuchs HL, Franks PJ. 2010. Plankton community properties determined by nutrients and size-selective feeding. Mar. Ecol. Prog. Ser. 413:115
    [Google Scholar]
  33. Gause GF. 1934. Experimental analysis of Vito Volterra's mathematical theory of the struggle for existence. Science 79:1617
    [Google Scholar]
  34. Giovannoni SJ, Britschgi TB, Moyer CL, Field KG. 1990. Genetic diversity in Sargasso Sea bacterioplankton. Nature 345:6063
    [Google Scholar]
  35. Giovannoni SJ, Thrash JC, Temperton B. 2014. Implications of streamlining theory for microbial ecology. ISME J. 8:155365
    [Google Scholar]
  36. Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL et al. 2005. Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:124245
    [Google Scholar]
  37. Goericke R. 2011. The structure of marine phytoplankton communities—patterns, rules, and mechanisms. Calif. Coop. Ocean. Fish. Investig. Rep. 52:18297
    [Google Scholar]
  38. Gregory TR. 2001. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol. Rev. 76:65101
    [Google Scholar]
  39. Hansen B, Bjornsen PK, Hansen PJ. 1994. The size ratio between planktonic predators and their prey. Limnol. Oceanogr. 39:395403
    [Google Scholar]
  40. Hardin G. 1960. The competitive exclusion principle: An idea that took a century to be born has implications in ecology, economics, and genetics. Science 131:129297
    [Google Scholar]
  41. Hébert M-P, Beisner BE, Maranger R. 2017. Linking zooplankton communities to ecosystem functioning: toward an effect-trait framework. J. Plankt. Res. 39:312
    [Google Scholar]
  42. Hellweger FL, van Sebille E, Fredrick ND. 2014. Biogeographic patterns in ocean microbes emerge in a neutral agent-based model. Science 345:134649
    [Google Scholar]
  43. Herrick J. 2011. The genome pace-maker hypothesis: a DNA based synthesis of genome size, DNA replication/repair and evolution. DNA Microarrays, Synthesis and Synthetic DNA MJ Campbell 175223. New York: Nova Sci.
    [Google Scholar]
  44. Holt RD. 1977. Predation, apparent competition, and the structure of prey communities. Theor. Pop. Biol. 12:197229
    [Google Scholar]
  45. Huang W, de Araujo Campos PR, de Oliveira VM, Ferreira FF. 2016. A resource-based game theoretical approach for the paradox of the plankton. PeerJ 4:e2329
    [Google Scholar]
  46. Hubbell SP. 1979. Tree dispersion, abundance and diversity in a tropical dry forest. Science 203:1299309
    [Google Scholar]
  47. Hubbell SP. 1997. A unified theory of biogeography and relative species abundance and its application to tropical rain forests and coral reefs. Coral Reefs 16:S921
    [Google Scholar]
  48. Hubbell SP. 2001. The Unified Neutral Theory of Biodiversity and Biogeography Princeton, NJ: Princeton Univ. Press
  49. Hubbell SP. 2005. Neutral theory in community ecology and the hypothesis of functional equivalence. Funct. Ecol. 19:16672
    [Google Scholar]
  50. Huisman J, Johansson AM, Folmer EO, Weissing FJ. 2001. Towards a solution of the plankton paradox: the importance of physiology and life history. Ecol. Lett. 4:40811
    [Google Scholar]
  51. Huisman J, Weissing FJ. 1999. Biodiversity of plankton by species oscillations and chaos. Nature 402:40710
    [Google Scholar]
  52. Huisman J, Weissing FJ. 2000. Reply: coexistence and resource competition. Nature 407:694
    [Google Scholar]
  53. Hutchinson GE. 1941. Ecological aspects of succession in natural populations. Am. Nat. 75:40618
    [Google Scholar]
  54. Hutchinson GE. 1961. The paradox of the plankton. Am. Nat. 95:13745
    [Google Scholar]
  55. Jessup CM, Forde SE. 2008. Ecology and evolution in microbial systems: the generation and maintenance of diversity in phage-host interactions. Res. J. Microbiol. 159:38289
    [Google Scholar]
  56. Karp-Boss L, Boss E, Jumars PA. 1996. Nutrient fluxes to planktonic osmotrophs in the presence of fluid motion. Oceanogr. Mar. Biol. 34:71108
    [Google Scholar]
  57. Kerr SR. 1974. Theory of size distribution in ecological communities. J. Fish. Res. 31:185962
    [Google Scholar]
  58. Kiefer DA, Berwald J. 1992. A random encounter model for the microbial planktonic community. Limnol. Oceanogr. 37:45767
    [Google Scholar]
  59. Kimura M. 1968. Evolutionary rate at the molecular level. Nature 217:62426
    [Google Scholar]
  60. Kiørboe T. 2011. How zooplankton feed: mechanisms, traits and trade-offs. Biol. Rev. 86:31139
    [Google Scholar]
  61. Knowles B, Bonachela JA, Behrenfeld MJ, Bondoc KG, Cael BB et al. 2020. Temperate infection in a virus-host system previously known for virulent dynamics. Nat. Commun 11:4626
    [Google Scholar]
  62. Leigh EG Jr. 2007. Neutral theory: a historical perspective. Evol. Biol. 20:207591
    [Google Scholar]
  63. Leimar O. 2002. Evolutionary change and Darwinian demons. Selection 2:6572
    [Google Scholar]
  64. Lynch MD, Neufeld JD. 2015. Ecology and exploration of the rare biosphere. Nat. Rev. Microbiol. 13:21729
    [Google Scholar]
  65. MacArthur RH, Wilson EO. 1963. An equilibrium theory of insular zoogeography. Evolution 17:37387
    [Google Scholar]
  66. MacArthur RH, Wilson EO. 1967. The Theory of Island Biogeography Princeton, NJ: Princeton Univ. Press
  67. Mas A, Jamshidi S, Lagadeuc Y, Eveillard D, Vandenkoornhuyse P. 2016. Beyond the black queen hypothesis. ISME J 10:208591
    [Google Scholar]
  68. Masuda Y, Yamanaka Y, Hirata T, Nakano H. 2017. Competition and community assemblage dynamics within a phytoplankton functional group: simulation using an eddy-resolving model to disentangle deterministic and random effects. Ecol. Model. 343:114
    [Google Scholar]
  69. Masuda Y, Yamanaka Y, Hirata T, Nakano H, Kohyama TS. 2020. Inhibition of competitive exclusion due to phytoplankton dispersion: a contribution for solving Hutchinson's paradox. Ecol. Model. 430:109089
    [Google Scholar]
  70. McKane AJ, Alonso D, Solé RV. 2004. Analytic solution of Hubbell's model of local community dynamics. Theor. Popul. Biol. 65:6773
    [Google Scholar]
  71. Menden-Deuer S, Rowlett J, Nursultanov M, Collins S, Rynearson T. 2021. Biodiversity of marine microbes is safeguarded by phenotypic heterogeneity in ecological traits. PLOS ONE 16:e0254799
    [Google Scholar]
  72. Moore LR, Goericke R, Chisholm SW. 1995. Comparative physiology of Synechococcus and Prochlorococcus: influence of light and temperature on growth, pigments, fluorescence and absorptive properties. Mar. Ecol. Prog. Ser. 116:25975
    [Google Scholar]
  73. Morris JJ, Lenski RE, Zinser ER. 2012. The black queen hypothesis: evolution of dependencies through adaptive gene loss. mBio 3:e00036-12
    [Google Scholar]
  74. Morris RM, Rappe MS, Connon SA, Vergin KL, Siebold WA et al. 2002. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420:80610
    [Google Scholar]
  75. Oliver MJ, Petrov D, Ackerly D, Falkowski P, Schofield OM. 2007. The mode and tempo of genome size evolution in eukaryotes. Genome Res 17:594601
    [Google Scholar]
  76. Partensky F, Hess WR, Vaulot D. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63:10627
    [Google Scholar]
  77. Pearce MT, Agarwala A, Fisher DS. 2020. Stabilization of extensive fine-scale diversity by ecologically driven spatiotemporal chaos. PNAS 117:1457283
    [Google Scholar]
  78. Picoche C, Barraquand F. 2020. Strong self-regulation and widespread facilitative interactions in phytoplankton communities. J. Ecol. 108:223242
    [Google Scholar]
  79. Pigolotti S, Cencini M. 2013. Species abundances and lifetimes: from neutral to niche-stabilized communities. J. Theor. Biol. 338:18
    [Google Scholar]
  80. Pineda A, Bortolini JC, Rodrigues LC. 2022. Effects of space and environment on phytoplankton distribution in subtropical reservoirs depend on functional features of the species. Aquat. Sci. 84:5
    [Google Scholar]
  81. Purves DW, Pacala SW 2005. Ecological drift in niche-structured communities: neutral pattern does not imply neutral process. Biotic Interactions in the Tropics D Burslem, M Pinard, S Hartley 10738. Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  82. Raven JA. 1994. Why are there no picoplanktonic O2 evolvers with volumes less than 10−19 m3?. J. Plankt. Res. 16:56580
    [Google Scholar]
  83. Record NR, Pershing AJ, Maps F. 2014. The paradox of the “paradox of the plankton. .” ICES J. Mar. Sci. 71:23640
    [Google Scholar]
  84. Reynolds RA, Stramski D. 2021. Variability in oceanic particle size distributions and estimation of size class contributions using a non-parametric approach. J. Geophys. Res. Oceans 126:e2021JC017946
    [Google Scholar]
  85. Rothhaupt KO. 1988. Mechanistic resource competition theory applied to laboratory experiments with zooplankton. Nature 333:66062
    [Google Scholar]
  86. Rothhaupt KO. 1996. Laboratory experiments with a mixotrophic chrysophyte and obligately phagotrophic and phototrophic competitors. Ecology 77:71624
    [Google Scholar]
  87. Roy S, Chattopadhyay J. 2007. Towards a resolution of ‘the paradox of the plankton’: a brief overview of the proposed mechanisms. Ecol. Complex. 4:2633
    [Google Scholar]
  88. Sarker S, Feudel U, Meunier CL, Lemke P, Dutta PS, Wiltshire KH. 2018. To share or not to share? Phytoplankton species coexistence puzzle in a competition model incorporating multiple resource-limitation and synthesizing unit concepts. Ecol. Model. 383:15059
    [Google Scholar]
  89. Schattenhofer M, Fuchs BM, Amann R, Zubkov MV, Tarran GA, Pernthaler J. 2009. Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean. Environ. Microbiol. 11:207893
    [Google Scholar]
  90. Scheffer M, Rinaldi S, Huisman J, Weissing FJ. 2003. Why plankton communities have no equilibrium: solutions to the paradox. Hydrobiologia 491:918
    [Google Scholar]
  91. Shuter BJ, Thomas JE, Taylor WD, Zimmerman AM. 1983. Phenotypic correlates of genomic DNA content in unicellular eukaryotes and other cells. Am. Nat. 122:2644
    [Google Scholar]
  92. Siegel DA. 1998. Resource competition in a discrete environment: Why are plankton distributions paradoxical?. Limnol. Oceanogr. 43:113346
    [Google Scholar]
  93. Sommer U. 1985. Comparison between steady state and nonsteady state competition: experiments with natural phytoplankton. Limnol. Oceanogr. 30:33546
    [Google Scholar]
  94. Sommer U. 1986. Nitrate- and silicate-competition among Antarctic phytoplankton. Mar. Biol. 91:34551
    [Google Scholar]
  95. Sommer U, Sommer F. 2006. Cladocerans versus copepods: the cause of contrasting top-down controls on freshwater and marine phytoplankton. Oecologia 147:18394
    [Google Scholar]
  96. Spatharis S, Mouillot D, Chi TD, Danielidis DB, Tsirtsis G. 2009. A niche-based modeling approach to phytoplankton community assembly rules. Oecologia 159:17180
    [Google Scholar]
  97. Sun J, Steindler L, Thrash JC, Halsey KH, Smith DP et al. 2011. One carbon metabolism in SAR11 pelagic marine bacteria. PLOS ONE 6:e23973
    [Google Scholar]
  98. Sutherland KR, Madin LP, Stocker R. 2010. Filtration of submicrometer particles by pelagic tunicates. PNAS 107:1512934
    [Google Scholar]
  99. Thingstad TF. 2000. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems.. Limnol. Oceanogr. 45:132028
    [Google Scholar]
  100. Thingstad TF, Lignell R. 1997. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13:1927
    [Google Scholar]
  101. Tilman D. 1977. Resource competition between planktonic algae: an experimental and theoretical approach. Ecology 58:33848
    [Google Scholar]
  102. Tilman D. 1980. Resources: a graphical-mechanistic approach to competition and predation. Am. Nat. 116:36293
    [Google Scholar]
  103. Tilman D. 1981. Tests of resource competition theory using four species of Lake Michigan algae. Ecology 62:80215
    [Google Scholar]
  104. Tilman D. 1982. Resource Competition and Community Structure Princeton, NJ: Princeton Univ. Press
  105. Ustick LJ, Larkin AA, Garcia CA, Garcia NS, Brock ML et al. 2021. Metagenomic analysis reveals global-scale patterns of ocean nutrient limitation. Science 372:28791
    [Google Scholar]
  106. Vallade MA, Houchmandzadeh B. 2003. Analytical solution of a neutral model of biodiversity. Phys. Rev. E 68:061902
    [Google Scholar]
  107. Venrick EL. 1990. Phytoplankton in an oligotrophic ocean: species structure and interannual variability. Ecology 71:154763
    [Google Scholar]
  108. Villa Martín P, Buček A, Bourguignon T, Pigolotti S. 2020. Ocean currents promote rare species diversity in protists. Sci. Adv. 6:eaaz9037
    [Google Scholar]
  109. Volkov I, Banavar JR, Hubbell SP, Maritan A. 2003. Neutral theory and relative species abundance in ecology. Nature 424:103537
    [Google Scholar]
  110. Ward BA, Collins S. 2022. Rapid evolution allows coexistence of highly divergent lineages within the same niche. Ecol. Lett. 25:183953
    [Google Scholar]
  111. Ward BA, Dutkiewicz S, Barton AD, Follows MJ. 2011. Biophysical aspects of resource acquisition and competition in algal mixotrophs. Am. Nat. 178:98112
    [Google Scholar]
  112. Weitz JS, Stock CA, Wilhelm SW, Bourouiba L, Coleman ML et al. 2015. A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. ISME J 9:135264
    [Google Scholar]
  113. Wilson JB. 2011. The twelve theories of co-existence in plant communities: the doubtful, the important and the unexplored. J. Veg. Sci. 22:18495
    [Google Scholar]
  114. Wirtz KW. 2012. Who is eating whom? Morphology and feeding type determine the size relation between planktonic predators and their ideal prey. Mar. Ecol. Prog. Ser. 445:112
    [Google Scholar]
  115. Wirtz KW. 2013. Mechanistic origins of variability in phytoplankton dynamics: part I: niche formation revealed by a size-based model. Mar. Biol. 160:231935
    [Google Scholar]
  116. Wright S. 1931. Evolution in Mendelian populations. Genetics 16:97159
    [Google Scholar]
  117. Wright S. 1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proceedings of the Sixth Annual Congress on Genetics, Vol. 135666. Austin, TX: Genet. Soc. Am.
    [Google Scholar]
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