The role of environmental factors in the long-term evolution of the marine biological pump

Abstract

The biological pump—the transfer of atmospheric carbon dioxide to the ocean interior and marine sediments as organic carbon—plays a critical role in regulating the long-term carbon cycle, atmospheric composition and climate. Despite its centrality in the Earth system, the response of the biological pump to biotic innovation and climatic fluctuations through most stages of Earth’s history has been largely conjectural. Here we use a mechanistic model of the biological carbon pump to revisit the factors controlling the transfer efficiency of carbon from surface waters to the ocean interior and marine sediments. We demonstrate that a shift from bacterioplankton-dominated to more eukaryote-rich ecosystems is unlikely to have considerably impacted the efficiency of Earth’s biological pump. In contrast, the evolution of large zooplankton capable of vertical movement in the water column would have enhanced carbon transfer into the ocean interior. However, the impact of zooplankton on the biological carbon pump is still relatively minor when compared with environmental drivers. In particular, increased ocean temperatures and greater atmospheric oxygen abundance lead to notable decreases in global organic carbon transfer efficiency. Taken together, our results call into question causative links between algal diversification and planetary oxygenation and suggest that climate perturbations in Earth’s history have played an important and underappreciated role in driving both carbon sequestration in the ocean interior and Earth surface oxygenation.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Schematic of the mechanistic model of the ocean biological carbon pump discussed in the text.
Fig. 2: The impact of first-order changes to plankton ecology on the ocean biological carbon pump.
Fig. 3: The impact of ocean temperature and atmospheric oxygen abundance on the ocean biological carbon pump.
Fig. 4: The strength of the biological carbon pump through geologic time.

Data availability

We have chosen not to deposit the data at this time but declare that data supporting the findings of this study are available within this article and its Supplementary Information, and all additional data are available from the corresponding author on request.

Code availability

All additional computer codes are available from the corresponding author on request.

References

  1. 1.

    Gwizd, S. J. Paleoceanography of the Eastern Equatorial Pacific: Insights from a new Carnegie Platform Stratigraphic Record. MS thesis, Univ. California, Santa Barbara (2015).

  2. 2.

    Boyd, P. W. & Trull, T. W. Understanding the export of biogenic particles in oceanic waters: is there consensus? Prog. Oceanogr. 72, 276–312 (2007).

    Google Scholar 

  3. 3.

    Volk, T. & Hoffert, M. I. in The Carbon Cycle and Atmospheric CO2: Natural Variations Archean to Present Vol. 32 (eds Sundquist, E. T. & Broecker, W. S.) 99–110 (American Geophysical Union, 1985).

  4. 4.

    Ducklow, H. W., Steinberg, D. K. & Buesseler, K. O. Upper ocean carbon export and the biological pump. Oceanography 14, 50–58 (2001).

    Google Scholar 

  5. 5.

    Fowler, S. W. & Knauer, G. A. Role of large particles in the transport of elements and organic compounds through the oceanic water column. Prog. Oceanogr. 16, 147–194 (1986).

    Google Scholar 

  6. 6.

    Alldredge, A. L. & Silver, M. W. Characteristics, dynamics and significance of marine snow. Prog. Oceanogr. https://doi.org/10.1016/0079-6611(88)90053-5 (1988).

  7. 7.

    Lyons, T. W., Reinhard, C. T. & Planavsky, N. J. The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506, 307–315 (2014).

    Google Scholar 

  8. 8.

    Lenton, T. M., Boyle, R. A., Poulton, S. W., Shields-Zhou, G. A. & Butterfield, N. J. Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era. Nat. Geosci. 7, 257–265 (2014).

    Google Scholar 

  9. 9.

    Butterfield, N. J. Plankton ecology and the Proterozoic–Phanerozoic transition. Paleobiology 23, 247–262 (1997).

    Google Scholar 

  10. 10.

    Knoll, A. H. & Nowak, M. A. The timetable of evolution. Sci. Adv. 3, e1603076 (2017).

    Google Scholar 

  11. 11.

    Butterfield, N. J. Oxygen, animals and oceanic ventilation: an alternative view. Geobiology 7, 1–7 (2009).

    Google Scholar 

  12. 12.

    Bartley, J. K. & Kah, L. C. Marine carbon reservoir, Corg–Ccarb coupling, and the evolution of the Proterozoic carbon cycle. Geology 32, 129–132 (2004).

    Google Scholar 

  13. 13.

    Zhang, S. et al. Sufficient oxygen for animal respiration 1,400 million years ago. Proc. Natl Acad. Sci. USA 113, 1731–1736 (2016).

    Google Scholar 

  14. 14.

    Isson, T. T. et al. Tracking the rise of eukaryotes to ecological dominance with zinc isotopes. Geobiology 16, 341–352 (2018).

    Google Scholar 

  15. 15.

    Love, G. D. et al. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature https://doi.org/10.1038/nature07673 (2009).

  16. 16.

    Knoll, A. H. & Sperling, E. A. Oxygen and animals in Earth history. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.1401745111 (2014).

  17. 17.

    Planavsky, N. J. et al. No evidence for high atmospheric oxygen levels 1,400 million years ago. Proc. Natl Acad. Sci. 113, E2550–E2551 (2016).

    Google Scholar 

  18. 18.

    Vannier, J. & Chen, J. Y. The early Cambrian colonization of pelagic niches exemplified by Isoxys (Arthropoda). Lethaia 33, 295–311 (2000).

    Google Scholar 

  19. 19.

    Knoll, A. H., Javaux, E. J., Hewitt, D. & Cohen, P. Eukaryotic organisms in Proterozoic oceans. Philos. Trans R. Soc. Lond. B 361, 1023–1038 (2006).

    Google Scholar 

  20. 20.

    Falkowski, P. G. in Encyclopedia of Biodiversity 2nd edn, 552–564 (Elsevier, 2013).

  21. 21.

    Logan, B. E. & Wilkinson, D. B. Fractal geometry of marine snow and other biological aggregates. Limnol. Oceanogr. 35, 130–136 (1990).

    Google Scholar 

  22. 22.

    Berry, W. B. N., Wilde, P. & Quinby-Hunt, M. S. Paleozoic (Cambrian through Devonian) anoxitropic biotopes. Palaeogeogr. Palaeoclimatol. Palaeoecol. 74, 3–13 (1989).

    Google Scholar 

  23. 23.

    Butterfield, N. J. Oxygen, animals and aquatic bioturbation: an updated account. Geobiology 16, 3–16 (2018).

    Google Scholar 

  24. 24.

    Polyakova, Y. I. Late Cenozoic evolution of northern Eurasian marginal seas based on the diatom record. Polarforschung 69, 211–220 (1999).

    Google Scholar 

  25. 25.

    Harwood, D. M., Nikolaev, V. A. & Winter, D. M. Cretaceous records of diatom evolution, radiation, and expansion. Paleontol. Soc. Pap. 13, 33–59 (2007).

    Google Scholar 

  26. 26.

    Lenton, T. M. & Daines, S. J. The effects of marine eukaryote evolution on phosphorus, carbon and oxygen cycling across the Proterozoic–Phanerozoic transition. Emerg. Top. Life Sci. https://doi.org/10.1042/ETLS20170156 (2018).

  27. 27.

    Tziperman, E., Halevy, I., Johnston, D. T., Knoll, A. H. & Schrag, D. P. Biologically induced initiation of Neoproterozoic snowball-Earth events. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.1016361108 (2011).

  28. 28.

    Jokulsdottir, T. & Archer, D. A stochastic, Lagrangian model of sinking biogenic aggregates in the ocean (SLAMS 1.0): model formulation, validation and sensitivity. Geosci. Model Dev. 9, 1455–1476 (2016).

    Google Scholar 

  29. 29.

    Dzierzbicka-Głowacka, L. Encounter rates in zooplankton. Pol. J. Environ. Stud. 15, 243–257 (2006).

    Google Scholar 

  30. 30.

    Archibald, K. M., Siegel, D. A. & Doney, S. C. Modeling the impact of zooplankton diel vertical migration on the carbon export flux of the biological pump. Global Biogeochem. Cycles 33, 181–199 (2019).

    Google Scholar 

  31. 31.

    Middelburg, J. J. A simple rate model for organic matter decomposition in marine sediments. Geochim. Cosmochim. Acta 53, 1577–1581 (1989).

    Google Scholar 

  32. 32.

    Katsev, S. & Crowe, S. A. Organic carbon burial efficiencies in sediments: the power law of mineralization revisited. Geology 43, 607–610 (2015).

    Google Scholar 

  33. 33.

    Quinlan, A. V. The thermal sensitivity of Michaelis–Menten kinetics as a function of substrate concentration. J. Franklin Inst. 310, 325–342 (1980).

    Google Scholar 

  34. 34.

    Quinlan, A. V. The thermal sensitivity of generic Michaelis–Menten processes without catalyst denaturation or inhibition. J. Therm. Biol. 6, 103–114 (1981).

    Google Scholar 

  35. 35.

    Segschneider, J. & Bendtsen, J. Temperature-dependent remineralization in a warming ocean increases surface pCO2 through changes in marine ecosystem composition. Global Biogeochem. Cycles 27, 1214–1225 (2013).

    Google Scholar 

  36. 36.

    John, E. H., Wilson, J. D., Pearson, P. N. & Ridgwell, A. Temperature-dependent remineralization and carbon cycling in the warm Eocene oceans. Palaeogeogr. Palaeoclimatol. Palaeoecol. 413, 158–166 (2014).

    Google Scholar 

  37. 37.

    Iversen, M. H., Ploug, H. & Wegener, A. Ballast minerals and the sinking carbon flux in the ocean: carbon-specific respiration rates and sinking velocity of marine snow aggregates. Biogeosciences 7, 2613–2624 (2010).

    Google Scholar 

  38. 38.

    Klaas, C. & Archer, D. E. Association of sinking organic matter with various types of mineral ballast in the deep sea: implications for the rain ratio. Global Biogeochem. Cycles 16, 1116 (2002).

    Google Scholar 

  39. 39.

    Bianchi, D., Stock, C., Galbraith, E. D. & Sarmiento, J. L. Diel vertical migration: ecological controls and impacts on the biological pump in a one-dimensional ocean model. Global Biogeochem. Cycles 27, 478–491 (2013).

    Google Scholar 

  40. 40.

    Kunze, E. Biologically generated mixing in the ocean. Annu. Rev. Mar. Sci. 11, 215–226 (2019).

    Google Scholar 

  41. 41.

    Katija, K. Biogenic inputs to ocean mixing. J. Exp. Biol. 215, 1040–1049 (2012).

    Google Scholar 

  42. 42.

    Kunze, E. Fluid mixing by swimming organisms in the low-Reynolds-number limit. J. Mar. Res. 69, 591–601 (2011).

    Google Scholar 

  43. 43.

    Arnosti, C., Jørgensen, B. B., Sagemann, J. & Thamdrup, B. Temperature dependence of microbial degradation of organic matter in marine sediments: polysaccharide hydrolysis, oxygen consumption, and sulfate reduction. Mar. Ecol. Prog. Ser. 165, 59–70 (1998).

    Google Scholar 

  44. 44.

    Marsay, C. M. et al. Attenuation of sinking particulate organic carbon flux through the mesopelagic ocean. Proc. Natl Acad. Sci. USA 112, 1089–1094 (2015).

    Google Scholar 

  45. 45.

    Laakso, T. A. & Schrag, D. P. A small marine biosphere in the Proterozoic. Geobiology 17, 161–171 (2019).

    Google Scholar 

  46. 46.

    Dore, J. E., Lukas, R., Sadler, D. W., Church, M. J. & Karl, D. M. Physical and biogeochemical modulation of ocean acidification in the central North Pacific. Proc. Natl Acad. Sci. USA 106, 12235–12240 (2009).

    Google Scholar 

  47. 47.

    McDonnell, A. M. P. & Buesseler, K. O. Variability in the average sinking velocity of marine particles. Limnol. Oceanogr. 55, 2085–2096 (2010).

    Google Scholar 

  48. 48.

    Alonso-Gonz lez, I. J. et al. Role of slowly settling particles in the ocean carbon cycle. Geophys. Res. Lett. 37, L13608 (2010).

    Google Scholar 

  49. 49.

    Dunne, J. P., Sarmiento, J. L. & Gnanadesikan, A. A synthesis of global particle export from the surface ocean and cycling through the ocean interior and on the seafloor. Global Biogeochem. Cycles 21, GB4006 (2007).

    Google Scholar 

  50. 50.

    Canfield, D. E., Rosing, M. T. & Bjerrum, C. Early anaerobic metabolisms. Philos. Trans R. Soc. Lond. B 361, 1819–1834 (2006).

    Google Scholar 

  51. 51.

    Martin, J. H., Knauer, G. A., Karl, D. M. & Broenkow, W. W. VERTEX: carbon cycling in the northeast Pacific. Deep Sea Res. 34, 267–285 (1987).

    Google Scholar 

  52. 52.

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

    Google Scholar 

  53. 53.

    Dam, H. G. & Drapeau, D. T. Coagulation efficiency, organic-matter glues and the dynamics of particles during a phytoplankton bloom in a mesocosm study. Deep Sea Res. 2 42, 111–123 (1995).

    Google Scholar 

  54. 54.

    Passow, U. & Alldredge, A. L. Distribution, size and bacterial colonization of transparent exopolymer particles (TEP) in the ocean. Mar. Ecol. Prog. Ser. 113, 185–198 (1994).

    Google Scholar 

  55. 55.

    Engel, A. The role of transparent exopolymer particles (TEP) in the increase in apparent particle stickiness (α) during the decline of a diatom bloom. J. Plankton Res. 22, 485–497 (2000).

    Google Scholar 

  56. 56.

    Alldredge, A. L. & Gotschalk, C. In situ settling behavior of marine snow. Limnol. Oceanogr. 33, 339–351 (1988).

    Google Scholar 

  57. 57.

    Briggs, N., Dall'Olmo, G. & Claustre, H. Major role of particle fragmentation in regulating biological sequestration of CO2 by the oceans. Science 367, 791–793 (2020).

    Google Scholar 

  58. 58.

    Alldredge, A. L., Granata, T. C., Gotschalk, C. C. & Dickey, T. D. The physical strength of marine snow and its implications for particle disaggregation in the ocean. Limnol. Oceanogr. 35, 1415–1428 (1990).

    Google Scholar 

  59. 59.

    Dilling, L. & Alldredge, A. L. Fragmentation of marine snow by swimming macrozooplankton: a new process impacting carbon cycling in the sea. Deep Sea Res. 1 47, 1227–1245 (2000).

    Google Scholar 

  60. 60.

    Iversen, M. H. et al. Sinkers or floaters? Contribution from salp pellets to the export flux during a large bloom event in the Southern Ocean. Deep Sea Res. 2 138, 116–125 (2017).

    Google Scholar 

  61. 61.

    Cohen, J. H. & Forward R. B. Jr in Oceanography and Marine Biology: An Annual Review Vol. 47 (eds Gibson, R. N. et al.) 77–110 (CRC Press, 2009).

  62. 62.

    Bianchi, D., Galbraith, E. D., Carozza, D. A., Mislan, K. A. S. & Stock, C. A. Intensification of open-ocean oxygen depletion by vertically migrating animals. Nat. Geosci. 6, 545–548 (2013).

    Google Scholar 

  63. 63.

    Bollens, S. M., Rollwagen-Bollens, G., Quenette, J. A. & Bochdansky, A. B. Cascading migrations and implications for vertical fluxes in pelagic ecosystems. J. Plankton Res. 33, 349–355 (2011).

    Google Scholar 

Download references

Acknowledgements

C.T.R. and N.J.P. acknowledge funding from the National Aeronautics and Space Administration Astrobiology Institute and the National Science Foundation.

Author information

Affiliations

Authors

Contributions

All authors designed the research. M.F. developed the model and performed model simulations and sensitivity analyses. All authors interpreted model results and wrote the paper.

Corresponding author

Correspondence to Mojtaba Fakhraee.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Primary Handling Editor: Rebecca Neely.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary text and Figs. 1–13.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fakhraee, M., Planavsky, N.J. & Reinhard, C.T. The role of environmental factors in the long-term evolution of the marine biological pump. Nat. Geosci. 13, 812–816 (2020). https://doi.org/10.1038/s41561-020-00660-6

Download citation

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing