Skip to main content

Advertisement

SpringerLink
Log in

Can Organisms Regulate Global Biogeochemical Cycles?

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Global biogeochemical cycles are being profoundly affected by human activities; therefore, it is critical to understand the role played by organisms in their regulation. Autotrophic organisms can regulate nutrient abundance at local scales through resource consumption, but most resources are inaccessible to them at global scales, either because of physical barriers or because of the presence of non-assimilable chemical forms of nutrients. Here we present a generic model of resource access limitation and apply it to the oceanic cycles of iron, phosphorus, and silicon to examine whether phytoplankton can regulate the concentrations of these key nutrients. Our model predicts that autotrophs cannot at the same time strongly impact accessible nutrients and exert perfect regulation on inaccessible nutrients. We show that the ability of organisms to regulate inaccessible nutrient pools strongly depends on passive physical and chemical flows, and on the fraction of the system that is accessible to organisms. Components of global climate change such as increasing water column stratification might result in a further decrease of the biotic regulation of inaccessible nutrients in freshwater and marine systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • Adjou M, Tréguer P, Dumousseaud C, Corvaisier R, Brzezinski MA, Nelson DM. 2011. Particulate silica and Si recycling in the surface waters of the Eastern Equatorial Pacific. Deep Sea Res II 58:449–61.

    Article  CAS  Google Scholar 

  • Arrigo KR. 2005. Marine microorganisms and global nutrient cycles. Nature 437:349–55.

    Article  CAS  PubMed  Google Scholar 

  • Baker AR, Croot PL. 2010. Atmospheric and marine controls on aerosol iron solubility in seawater. Mar Chem 120:4–13.

    Article  CAS  Google Scholar 

  • Benitez-Nelson CR. 2000. The biogeochemical cycling of phosphorus in marine systems. Earth Sci Rev 51:109–35.

    Article  CAS  Google Scholar 

  • Bouwman AF, Beusen AHW, Billen G. 2009. Human alteration of the global nitrogen and phosphorus soil balances for the period 1970–2050. Glob Biogeochem Cycles 23:GB0A04.

    Article  Google Scholar 

  • Boyd PW, Ellwood MJ. 2010. The biogeochemical cycle of iron in the ocean. Nat Geosci 3:675–82.

    Article  CAS  Google Scholar 

  • Boyd PW, Mackie DS, Hunter KA. 2010. Aerosol iron deposition to the surface ocean—modes of iron supply and biological responses. Mar Chem 120:128–43.

    Article  CAS  Google Scholar 

  • Brandes JA, Devol AH, Deutsch C. 2007. New developments in the marine nitrogen cycle. Chem Rev 107:577–89.

    Article  CAS  PubMed  Google Scholar 

  • Canfield DE. 2014. Oxygen: a four billion years history. Princeton: Princeton University Press.

    Google Scholar 

  • Carpenter SR. 2005. Eutrophication of aquatic ecosystems: bistability and soil phosphorus. Proc Natl Acad Sci USA 102:10002–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Denman KL, Brasseur G, Chidthaisong A, Ciais P, Cox PM, Dickinson RE, Hauglustaine D, Heinze C, Holland E, Jacob D, Lohmann U, Ramachandran S, da Silva Dias PL, Wofsy SC, Zhang X. 2007. Couplings between changes in the climate system and biogeochemistry. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, Eds. Climate change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Diaz RJ, Rosenberg R. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321:926–9.

    Article  CAS  PubMed  Google Scholar 

  • Doney SC. 2010. The growing human footprint on coastal and open-ocean biogeochemistry. Science 328:1512–16.

    Article  CAS  PubMed  Google Scholar 

  • Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–42.

    Article  PubMed  Google Scholar 

  • Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Högberg P, Linder S, Mackenzie FT, Iii BM, Pedersen T, Rosenthal Y, Seitzinger S, Smetacek V, Steffen W. 2000. The global carbon cycle: a test of our knowledge of Earth as a system. Science 290:291–6.

    Article  CAS  PubMed  Google Scholar 

  • Franz J, Krahmann G, Lavik G, Grasse P, Dittmar T, Riebesell U. 2012. Dynamics and stoichiometry of nutrients and phytoplankton in waters influenced by the oxygen minimum zone in the eastern tropical Pacific. Deep Sea Res I 62:20–31.

    Article  CAS  Google Scholar 

  • Free A, Barton NH. 2007. Do evolution and ecology need the Gaia hypothesis? Trends Ecol Evol 22:611–19.

    Article  PubMed  Google Scholar 

  • Fung IY, Meyn SK, Tegen I, Doney SC, John JG, Bishop JKB. 2000. Iron supply and demand in the upper ocean. Glob Biogeochem Cycles 14:281–95.

    Article  CAS  Google Scholar 

  • Gruber N. 2011. Warming up, turning sour, losing breath: ocean biogeochemistry under global change. Philos Trans R Soc A 369:1980–96.

    Article  CAS  Google Scholar 

  • Gruber N, Galloway JN. 2008. An Earth-system perspective of the global nitrogen cycle. Nature 451:293–6.

    Article  CAS  PubMed  Google Scholar 

  • Huston MA, DeAngelis DL. 1994. Competition and coexistence: the effects of resource transport and supply rates. Am Nat 144:954–77.

    Article  Google Scholar 

  • Jickells TD, An ZS, Andersen KK, Baker AR, Bergametti G, Brooks N, Cao JJ, Boyd PW, Duce RA, Hunter KA, Kawahata H, Kubilay N, laRoche J, Liss PS, Mahowald N, Prospero JM, Ridgwell AJ, Tegen I, Torres R. 2005. Global iron connections between desert dust, ocean biogeochemistry, and climate. Science 308:67–71.

    Article  CAS  PubMed  Google Scholar 

  • Karl DM. 2002. Nutrient dynamics in the deep blue sea. Trends Microbiol 10:410–18.

    Article  CAS  PubMed  Google Scholar 

  • Karl DM, Tien G, Dore J, Winn CD. 1993. Total dissolved nitrogen and phosphorus concentrations at US-JGOFS station ALOHA: redfield reconciliation. Mar Chem 41:203–8.

    Article  CAS  Google Scholar 

  • Klausmeier CA, Litchman E, Daufresne T, Levin SA. 2004. Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429:171–4.

    Article  CAS  PubMed  Google Scholar 

  • Krishnamurthy A, Moore JK, Mahowald N, Luo C, Zender CS. 2010. Impacts of atmospheric nutrient inputs on marine biogeochemistry. J Geophys Res Biogeosci 115:G01006.

    Article  Google Scholar 

  • Kylafis G, Loreau M. 2008. Ecological and evolutionary consequences of niche construction for its agent. Ecol Lett 11:1072–81.

    Article  PubMed  Google Scholar 

  • Kylafis G, Loreau M. 2011. Niche construction in the light of niche theory. Ecol Lett 14:82–90.

    Article  PubMed  Google Scholar 

  • Laruelle GG, Roubeix V, Sferratore A, Brodherr B, Ciuffa D, Conley DJ, Dürr HH, Garnier J, Lancelot C, Le Thi Phuong Q, Meunier J-D, Meybeck M, Michalopoulos P, Moriceau B, Ní Longphuirt S, Loucaides S, Papush L, Presti M, Ragueneau O, Regnier P, Saccone L, Slomp CP, Spiteri C, Van Cappellen P. 2009. Anthropogenic perturbations of the silicon cycle at the global scale: Key role of the land-ocean transition. Glob Biogeochem Cycles 23:GB4031.

    Article  Google Scholar 

  • Lenton TM. 1998. Gaia and natural selection. Nature 394:439–47.

    Article  CAS  PubMed  Google Scholar 

  • Lenton TM. 2001. The role of land plants, phosphorus weathering and fire in the rise and regulation of atmospheric oxygen. Glob Change Biol 7:613–29.

    Article  Google Scholar 

  • Lenton TM, Watson AJ. 2000a. Redfield revisited: 1. Regulation of nitrate, phosphate, and oxygen in the ocean. Glob Biogeochem Cycles 14:225–48.

    Article  CAS  Google Scholar 

  • Lenton TM, Watson AJ. 2000b. Redfield revisited: 2. What regulates the oxygen content of the atmosphere? Glob Biogeochem Cycles 14:249–68.

    Article  CAS  Google Scholar 

  • Lenton T, Watson A. 2011. Revolutions that made the Earth. Oxford, UK: Oxford University Press.

    Book  Google Scholar 

  • Loh AN, Bauer JE. 2000. Distribution, partitioning and fluxes of dissolved and particulate organic C, N and P in the eastern North Pacific and Southern Oceans. Deep Sea Res I 47:2287–316.

    Article  CAS  Google Scholar 

  • Loreau M. 1996. Coexistence of multiple food chains in a heterogeneous environment: interactions among community structure, ecosystem functioning, and nutrient dynamics. Math Biosci 134:153–88.

    Article  CAS  PubMed  Google Scholar 

  • Loreau M. 2010. From populations to ecosystems: theoretical foundations for a new ecological synthesis. Princeton: Princeton University Press.

    Book  Google Scholar 

  • Lovelock JE, Margulis L. 1974. Atmospheric homeostasis by and for the biosphere: the Gaia hypothesis. Tellus 26:2–10.

    Article  CAS  Google Scholar 

  • Martin-Jézéquel V, Hildebrand M, Brzezinski MA. 2000. Silicon metabolism in diatoms: implications for growth. J Phycol 36:821–40.

    Article  Google Scholar 

  • Moore JK, Doney SC, Glover DM, Fung IY. 2001. Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep Sea Res II 49:463–507.

    Article  Google Scholar 

  • Redfield AC. 1934. On the proportions of organic derivations in sea water and their relation to the composition of plankton. In: Daniel RJ, Ed. James Johnstone memorial volume. Liverpool: University Press of Liverpool. p 177–92.

    Google Scholar 

  • Redfield AC. 1958. The biological control of chemical factors in the environment. Am Sci 46:205–21.

    CAS  Google Scholar 

  • Rees AP. 2012. Pressures on the marine environment and the changing climate of ocean biogeochemistry. Philos Trans R Soc A 370:5613–35.

    Article  CAS  Google Scholar 

  • Riebesell U, Körtzinger A, Oschlies A. 2009. Sensitivities of marine carbon fluxes to ocean change. Proc Natl Acad Sci USA 106:20602–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sañudo-Wilhelmy SA, Kustka AB, Gobler CJ, Hutchins DA, Yang M, Lwiza K, Burns J, Capone DG, Raven JA, Carpenter EJ. 2001. Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411:66–9.

    Article  PubMed  Google Scholar 

  • Sarthou G, Timmermans KR, Blain S, Tréguer P. 2005. Growth physiology and fate of diatoms in the ocean: a review. J Sea Res 53:25–42.

    Article  CAS  Google Scholar 

  • Schlesinger WH. 1997. Biogeochemistry: an analysis of global change. San Diego, CA: Academic Press.

    Google Scholar 

  • Seitzinger S, Harrison JA, Böhlke JK, Bouwman AF, Lowrance R, Peterson B, Tobias C, Drecht GV. 2006. Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16:2064–90.

    Article  CAS  PubMed  Google Scholar 

  • Smith VH, Schindler DW. 2009. Eutrophication science: where do we go from here? Trends Ecol Evol 24:201–7.

    Article  PubMed  Google Scholar 

  • Smith VH, Tilman GD, Nekola JC. 1999. Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 100:179–96.

    Article  CAS  PubMed  Google Scholar 

  • Stramma L, Johnson GC, Sprintall J, Mohrholz V. 2008. Expanding oxygen-minimum zones in the tropical oceans. Science 320:655–8.

    Article  CAS  PubMed  Google Scholar 

  • Tréguer PJ, De La Rocha CL. 2013. The world ocean silica cycle. Annu Rev Mar Sci 5:477–501.

    Article  Google Scholar 

  • Tyrrell T. 1999. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400:525–31.

    Article  CAS  Google Scholar 

  • Tyrrell T. 2013. On Gaia: a critical investigation of the relationship between life and Earth. Princeton: Princeton University Press.

    Book  Google Scholar 

  • Vitousek PM, Field CB. 1999. Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46:179–202.

    CAS  Google Scholar 

  • Vitousek PM, Naylor R, Crews T, David MB, Drinkwater LE, Holland E, Johnes PJ, Katzenberger J, Martinelli LA, Matson PA, Nziguheba G, Ojima D, Palm CA, Robertson GP, Sanchez PA, Townsend AR, Zhang FS. 2009. Nutrient imbalances in agricultural development. Science 324:1519–20.

    Article  CAS  PubMed  Google Scholar 

  • Weber T, Deutsch C. 2012. Oceanic nitrogen reservoir regulated by plankton diversity and ocean circulation. Nature 489:419–22.

    Article  CAS  PubMed  Google Scholar 

  • Yool A, Tyrrell T. 2003. Role of diatoms in regulating the ocean’s silicon cycle. Glob Biogeochem Cycles 17:1103.

    Article  Google Scholar 

Download references

Acknowledgments

We thank Claire de Mazancourt for valuable comments on the manuscript. This work was supported by the TULIP Laboratory of Excellence (ANR-10-LABX-41).

Author information

Authors and Affiliations

  1. Centre for Biodiversity Theory and Modelling, Station d’Ecologie Expérimentale du CNRS, 09200, Moulis, France

    Anne-Sophie Auguères & Michel Loreau

Authors
  1. Anne-Sophie Auguères
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michel Loreau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anne-Sophie Auguères.

Additional information

Author contributions

ML conceived the idea, ASA and ML built and analyzed the model, ASA wrote the first draft of the manuscript, and both authors contributed substantially to revisions.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 62 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Auguères, AS., Loreau, M. Can Organisms Regulate Global Biogeochemical Cycles?. Ecosystems 18, 813–825 (2015). https://doi.org/10.1007/s10021-015-9864-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-015-9864-y

Keywords

Search

Navigation