Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Climate change has altered zooplankton-fuelled carbon export in the North Atlantic

Nature Ecology & Evolution volume 3, pages 416–423 (2019)Cite this article

Subjects

Abstract

Marine plankton have been conspicuously affected by recent climate change, responding with profound spatial relocations and shifts in the timing of their seasonal occurrence. These changes directly affect the global carbon cycle by altering the transport of organic material from the surface ocean to depth, with consequences that remain poorly understood. We investigated how distributional and abundance changes of copepods, the dominant group of zooplankton, have affected biogenic carbon cycling. We used trait-based, mechanistic models to estimate the magnitude of carbon transported downward through sinking faecal pellets, daily vertical migration and seasonal hibernation at depth. From such estimates for over 200,000 community observations in the northern North Atlantic we found carbon flux increased along the northwestern boundary of the study area and decreased in the open northern North Atlantic during the past 55 years. These changes in export were primarily associated with changes in copepod biomass, driven by shifting distributions of abundant, large-bodied species. Our findings highlight how recent climate change has affected downward carbon transport by altering copepod community structure and demonstrate how carbon fluxes through plankton communities can be mechanistically implemented in next-generation biogeochemical models with size-structured representations of zooplankton communities.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Code availability

All analyses were conducted in the R environment32. Maps were created with the software Generic Mapping Tools43. Code generated for analyses and mapping is available from the corresponding author upon reasonable request.

Data availability

Data generated to support the findings of this study are available within the paper and its supplementary information files.

References

  1. Sigman, D. M. & Boyle, E. A. Glacial/interglacial variations in atmospheric carbon dioxide. Nature 407, 859–869 (2000).

    Article  CAS  Google Scholar 

  2. Sanders, R. et al. The biological carbon pump in the North Atlantic. Prog. Oceanogr. 129, 200–218 (2014).

    Article  Google Scholar 

  3. Steinberg, D. K. & Landry, M. R. Zooplankton and the ocean carbon cycle. Ann. Rev. Mar. Sci. 9, 413–444 (2017).

    Article  Google Scholar 

  4. Stamieszkin, K. et al. Size as the master trait in modeled copepod fecal pellet carbon flux. Limnol. Oceanogr. 60, 2090–2107 (2015).

    Article  CAS  Google Scholar 

  5. Turner, J. T. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog. Oceanogr. 130, 205–248 (2015).

    Article  Google Scholar 

  6. Hays, G. C. Zooplankton avoidance activity. Nature 376, 650 (1994).

    Article  Google Scholar 

  7. Hansen, A. N. & Visser, A. W. Carbon export by vertically migrating zooplankton: an optimal behavior model. Limnol. Oceanogr. 61, 701–710 (2016).

    Article  CAS  Google Scholar 

  8. Steinberg, D. K. et al. Zooplankton vertical migration and the active transport of dissolved organic and inorganic carbon in the Sargasso Sea. Deep Sea Res. Part I Oceanogr. Res. Pap. 47, 137–158 (2000).

    Article  CAS  Google Scholar 

  9. Al-Mutairi, H. & Landry, M. R. Active export of carbon and nitrogen at Station ALOHA by diel migrant zooplankton. Deep Sea Res. Part II Top. Stud. Oceanogr. 48, 2083–2103 (2001).

    Article  CAS  Google Scholar 

  10. Ohman, M. D. & Romagnan, J.-B. Nonlinear effects of body size and optical attenuation on Diel Vertical Migration by zooplankton. Limnol. Oceanogr. 61, 765–770 (2016).

    Article  Google Scholar 

  11. Dahms, H. U. Dormancy in the Copepoda—an overview. Hydrobiologia 306, 199–211 (1995).

    Article  Google Scholar 

  12. Brun, P., Payne, M. R. & Kiørboe, T. A trait database for marine copepods. Earth Syst. Sci. Data 9, 99–113 (2017).

    Article  Google Scholar 

  13. Jónasdóttir, S. H., Visser, A. W., Richardson, K. & Heath, M. R. Seasonal copepod lipid pump promotes carbon sequestration in the deep North Atlantic. Proc. Natl Acad. Sci. U. SA 112, 12122–12126 (2015).

    Article  Google Scholar 

  14. Visser, A. W., Grønning, J. & Jónasdóttir, S. H. Calanus hyperboreus and the lipid pump. Limnol. Oceanogr. 62, 1155–1165 (2017).

    Article  CAS  Google Scholar 

  15. Bradford-Grieve, J. M. Potential contribution that the copepod Neocalanus tonsus makes to downward carbon flux in the Southern Ocean. J. Plankton Res. 23, 963–975 (2001).

    Article  Google Scholar 

  16. Richardson, A. J. et al. Using continuous plankton recorder data. Prog. Oceanogr. 68, 27–74 (2006).

    Article  Google Scholar 

  17. Johns, D. G. Raw data for copepods in the North Atlantic (25-73N, 80W-20E) 1960–2014 as recorded by the Continuous Plankton Recorder (2016); https://doi.org/10.7487/2016.250.1.1007

  18. Beaugrand, G., Edwards, M. & Legendre, L. Marine biodiversity, ecosystem functioning, and carbon cycles. Proc. Natl Acad. Sci. USA 107, 10120–10124 (2010).

    Article  CAS  Google Scholar 

  19. Sundby, S., Drinkwater, K. F. & Kjesbu, O. S. The North Atlantic Spring-Bloom System—where the changing climate meets the winter dark. Front. Mat. Sci. 3, 28 (2016).

    Google Scholar 

  20. Martinez, E., Antoine, D., D’Ortenzio, F. & de Boyer Montégut, C. Phytoplankton spring and fall blooms in the North Atlantic in the 1980s and 2000s. J. Geophys. Res. 116, C11029 (2011).

    Article  Google Scholar 

  21. Chivers, W. J., Walne, A. W. & Hays, G. C. Mismatch between marine plankton range movements and the velocity of climate change. Nat. Commun. 8, 14434 (2017).

    Article  CAS  Google Scholar 

  22. Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).

    Article  Google Scholar 

  23. Edwards, M. & Richardson, A. J. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430, 881–884 (2004).

    Article  CAS  Google Scholar 

  24. Greene, C. & Pershing, A. J. The response of Calanus finmarchicus populations to climate variability in the Northwest Atlantic: basin-scale forcing associated with the North Atlantic Oscillation. ICES J. Mar. Sci.1536–1544 (2000).

  25. Chust, G. et al. Are Calanus spp. shifting poleward in the North Atlantic? A habitat modelling approach. ICES J. Mar. Sci. 71, 241–253 (2013).

    Article  Google Scholar 

  26. Cermeño, P. et al. The role of nutricline depth in regulating the ocean. Proc. Natl Acad. Sci. USA 105, 20344–20349 (2008).

    Article  Google Scholar 

  27. Palomares-Garcia, R. J., Gomez-Gutierrez, J. & Robinson, C. J. Winter and summer vertical distribution of epipelagic copepods in the Gulf of California. J. Plankton Res. 35, 1009–1026 (2013).

    Article  CAS  Google Scholar 

  28. Guidi, L. et al. Plankton networks driving carbon export in the oligotrophic ocean. Nature 532, 465–470 (2016).

    Article  CAS  Google Scholar 

  29. Boyd, P. W. Toward quantifying the response of the oceans’ biological pump to climate change. Front. Mar. Sci. 2, 1–15 (2015).

    Google Scholar 

  30. IPCC Climate Change 2014 Impacts, Adaptation, and Vulnerability (eds Field, C. B. et al.) 411–484 (Cambridge Univ. Press, 2014); https://doi.org/10.1017/CBO9781107415379.011.

  31. Kiørboe, T. & Hirst, A. G. Shifts in mass scaling of respiration, feeding, and growth rates across life-form transitions in marine pelagic organisms. Am. Nat. 183, E118–E130 (2014).

    Article  Google Scholar 

  32. R. Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2013); http://www.R-project.org/.

  33. Locarini, R. A. et al. World Ocean Atlas 2013, Volume 1: Temperature (NOAA Atlas NESDIS 73, Silver Spring, MD, USA, 2013).

  34. Rayner, N. A. et al. Global analyses of sea surface temperature, sea ice, and night marine air temperature since the late nineteenth century. J. Geophys. Res. 108, 4407 (2003).

    Article  Google Scholar 

  35. Kostadinov, T. S., Milutinović, S., Marinov, I. & Cabré, A. Carbon-based phytoplankton size classes retrieved via ocean color estimates of the particle size distribution. Ocean Sci. 12, 561–575 (2016).

    Article  CAS  Google Scholar 

  36. Schmidtko, S., Johnson, G. C. & Lyman, J. M. MIMOC: a global monthly isopycnal upper-ocean climatology with mixed layers. J. Geophys. Res. Ocean. 118, 1658–1672 (2013).

    Article  Google Scholar 

  37. Amante, C. & Eakins, B. W. ETOPO1 1 Arc-Minute Global Relief Model: Procedures, Data Sources and Analysis NOAA Technical Memorandum NESDIS NGDC-24 (National Geophysical Data Center, 2009); https://doi.org/10.7289/V5C8276M.

  38. Jiang, H. & Kiorboe, T. The fluid dynamics of swimming by jumping in copepods. J. R. Soc. Interface. 8, 1090–1103 (2011).

    Article  Google Scholar 

  39. Rue, H., Martino, S. & Chopin, N. Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. J. R. Stat. Soc. Ser. B (Statistical Methodol. 71, 319–392 (2009).

    Article  Google Scholar 

  40. Blangiardo, M. & Cameletti, M. Spatial and Spatio-temporal Bayesian Models with R-INLA (Wiley, Chichester, UK, 2015).

  41. Gilliam, J. F. & Fraser, D. F. Habitat selection under predation hazard: test of a mModel with foraging minnows. Ecology 68, 1856–1862 (1987).

    Article  Google Scholar 

  42. Kiørboe, T. & Tiselius, P. T. Gut clearance and pigment destruction in a herbivorous copepod, Acartia tonsa, and the determination of in situ grazing rates. J. Plankton Res. 9, 525–534 (1987).

    Article  Google Scholar 

  43. Wessel, P., Smith, W. H. F., Scharroo, R., Luis, J. & Wobbe, F. Generic mapping tools: improved version released. Eos, Trans. Am. Geophys. Union 94, 409–410 (2013).

    Article  Google Scholar 

Download references

Acknowledgements

We acknowledge the Villum foundation for support to the Centre for Ocean Life. Further support was received from the Gordon & Betty Moore Foundation through award no. 5479’ (T.K. and A.V.W.), the NSF GRFP grant no. DGE-1144205 (K.S.) and the European Union 7th Framework Programme (FP7 2007–2013) through grant no. 308299 (NACLIM) (M.R.P.). We thank the scientists at SAHFOS whose efforts over the years helped to establish and maintain the CPR survey and H. van Someren Gréve for the beautiful copepod illustration.

Author information

Authors and Affiliations

  1. Centre for Ocean Life, National Institute of Aquatic Resources, Technical University of Denmark, Kongens Lyngby, Denmark

    Philipp Brun, Andre W. Visser, Mark R. Payne & Thomas Kiørboe

  2. Swiss Federal Research Institute (WSL), Birmensdorf, Switzerland

    Philipp Brun

  3. School of Marine Sciences, University of Maine, Orono, ME, USA

    Karen Stamieszkin

  4. Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA

    Karen Stamieszkin

  5. Sir Alister Hardy Foundation for Ocean Science, Plymouth, UK

    Priscilla Licandro

  6. Plymouth Marine Laboratory, Plymouth, UK

    Priscilla Licandro

  7. Stazione Zoologica Anton Dohrn, Napoli, Italy

    Priscilla Licandro

Authors
  1. Philipp Brun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karen Stamieszkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andre W. Visser
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Priscilla Licandro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mark R. Payne
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Thomas Kiørboe
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

P.B., K.S., A.W.V., M.R.P. and T.K. designed the study. K.S. developed the faecal pellet model. P.L. selected the taxa used and compiled the data. P.B. performed the analysis and prepared the manuscript with contributions and support from the other authors.

Corresponding author

Correspondence to Philipp Brun.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Results, Supplementary Discussion, Supplementary Figs. 1–10, Supplementary Tables 1–3 and Supplementary References

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brun, P., Stamieszkin, K., Visser, A.W. et al. Climate change has altered zooplankton-fuelled carbon export in the North Atlantic. Nat Ecol Evol 3, 416–423 (2019). https://doi.org/10.1038/s41559-018-0780-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-018-0780-3

This article is cited by

Search

Advanced 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