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Krill body size drives particulate organic carbon export in West Antarctica

Abstract

The export of carbon from the ocean surface and storage in the ocean interior is important in the modulation of global climate1,2,3,4. The West Antarctic Peninsula experiences some of the largest summer particulate organic carbon (POC) export rates, and one of the fastest warming rates, in the world5,6. To understand how warming may alter carbon storage, it is necessary to first determine the patterns and ecological drivers of POC export7,8. Here we show that Antarctic krill (Euphausia superba) body size and life-history cycle, as opposed to their overall biomass or regional environmental factors, exert the dominant control on the POC flux. We measured POC fluxes over 21 years, the longest record in the Southern Ocean, and found a significant 5-year periodicity in the annual POC flux, which oscillated in synchrony with krill body size, peaking when the krill population was composed predominately of large individuals. Krill body size alters the POC flux through the production and export of size-varying faecal pellets9, which dominate the total flux. Decreases in winter sea ice10, an essential habitat for krill, are causing shifts in the krill population11, which may alter these export patterns of faecal pellets, leading to changes in ocean carbon storage.

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Fig. 1: WAP POC flux time series from 1992 to 2013.
Fig. 2: Annual POC flux oscillates on a five-year periodicity.
Fig. 3: Summer Antarctic krill body size drives annual POC flux.

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Data availability

The data analysed in this study can be found at: https://doi.org/10.6073/pasta/cb0ee837fd2615ae133dcfdc0b806571, https://doi.org/10.6073/pasta/d0b492b09b678d55db046e27ebe9d1c1, https://doi.org/10.6073/pasta/2afc968fad7d40c989de532f52e6720b, https://doi.org/10.6073/pasta/03e6d72a78bc2512ef5bb327e686f8fa, https://doi.org/10.6073/pasta/60b41cfa5eaa7298f84b9ac291037403, https://doi.org/10.5281/zenodo.7723853 and https://doi.org/10.6073/pasta/585ba08c3ab00f7d36f3756bb8e7f79b. Bathymetry data can be found at https://doi.org/10.7289/V5C8276M.

References

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

  2. Sarmiento, J. L., Hughes, T. M., Stouffer, R. J. & Manabe, S. Simulated response of the ocean carbon cycle to anthropogenic climate warming. Nature 393, 245–249 (1998).

    Article  CAS  ADS  Google Scholar 

  3. Marinov, I. et al. Impact of oceanic circulation on biological carbon storage in the ocean and atmospheric pCO2. Glob. Biogeochem. Cycles 22, GB3007 (2008).

    Article  ADS  Google Scholar 

  4. Studer, A. S. et al. Increased nutrient supply to the Southern Ocean during the Holocene and its implications for the pre-industrial atmospheric CO2 rise. Nat. Geosci. 11, 756–760 (2008).

    Article  ADS  Google Scholar 

  5. Honjo, S. in Polar Oceanography (ed Smith, W. O. Jr) 322–353 (Academic, 1990).

  6. Meredith, M. P., Stefels, J. & van Leeuwe, M. Marine studies at the western Antarctic Peninsula: priorities, progress and prognosis. Deep Sea Res. Part II 139, 1–8 (2017).

    Article  Google Scholar 

  7. Bopp, L. et al. Potential impact of climate change on marine export production. Glob. Biogeochem. Cycles 15, 81–99 (2001).

    Article  CAS  ADS  Google Scholar 

  8. Passow, U. & Carlson, C. A. The biological pump in a high CO2 world. Mar. Ecol. Prog. Ser. 470, 249–271 (2012).

    Article  CAS  ADS  Google Scholar 

  9. Cadée, G. C., González, H. & Schnack-Schiel, S. B. Krill diet affects faecal string settling. Polar Biol. 12, 75–80 (1992).

    Article  Google Scholar 

  10. Stammerjohn, S. & Maksym, T. in Sea Ice 3rd edn (ed. Thomas, D. N.) Ch. 10 (John Wiley & Sons, 2017).

  11. Atkinson, A. et al. Krill (Euphausia superba) distribution contracts southward during rapid regional warming. Nat. Clim. Change 9, 142–147 (2019).

    Article  ADS  Google Scholar 

  12. Knox, F. & McElroy, M. B. Changes in atmospheric CO2: influence of the marine biota at high latitude. J. Geophys. Res. Atmos. 89, 4629–4637 (1984).

    Article  CAS  ADS  Google Scholar 

  13. Siegel, D. A., DeVries, T., Cetinić, I. & Bisson, K. M. Quantifying the ocean’s biological pump and its carbon cycle impacts on global scales. Annu. Rev. Mar. Sci. 15, 329–356 (2022).

  14. Long, M. C. et al. Strong Southern Ocean carbon uptake evident in airborne observations. Science 374, 1275–1280 (2021).

    Article  CAS  PubMed  ADS  Google Scholar 

  15. Arteaga, L., Haëntjens, N., Boss, E., Johnson, K. S. & Sarmiento, J. L. Assessment of export efficiency equations in the Southern Ocean applied to satellite‐based net primary production. J. Geophys. Res. Oceans 123, 2945–2964 (2018).

    Article  ADS  Google Scholar 

  16. Nöthig, E. M. & von Bodungen, B. Occurrence and vertical flux of faecal pellets of probably protozoan origin in the southeastern Weddell Sea (Antarctica). Mar. Ecol. Prog. Ser. 56, 281–289 (1989).

  17. Palanques, A., Isla, E., Puig, P., Sanchez-Cabeza, J. A. & Masqué, P. Annual evolution of downward particle fluxes in the Western Bransfield Strait (Antarctica) during the FRUELA project. Deep Sea Res. Part II 49, 903–920 (2002).

    Article  CAS  ADS  Google Scholar 

  18. Manno, C. et al. Continuous moulting by Antarctic krill drives major pulses of carbon export in the north Scotia Sea, Southern Ocean. Nat. Commun. 11, 6051 (2020).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  19. Karl, D. M. & Lukas, R. The Hawaii Ocean Time-series (HOT) program: background, rationale and field implementation. Deep Sea Res. Part II 43, 129–156 (1996).

    Article  CAS  ADS  Google Scholar 

  20. Conte, M. H., Ralph, N. & Ross, E. H. Seasonal and interannual variability in deep ocean particle fluxes at the Oceanic Flux Program (OFP)/Bermuda Atlantic Time Series (BATS) site in the western Sargasso Sea near Bermuda. Deep Sea Res. Part II 48, 1471–1505 (2001).

    Article  ADS  Google Scholar 

  21. Wynn-Edwards, C. A. et al. Particle fluxes at the Australian Southern Ocean Time Series (SOTS) achieve organic carbon sequestration at rates close to the global median, are dominated by biogenic carbonates, and show no temporal trends over 20-years. Front. Earth Sci. 8, 329 (2020).

    Article  ADS  Google Scholar 

  22. Schofield, O. et al. Decadal variability in coastal phytoplankton community composition in a changing West Antarctic Peninsula. Deep Sea Res. Part I 124, 42–54 (2017).

    Article  CAS  Google Scholar 

  23. Vaughan, D. G. et al. Recent rapid regional climate warming on the Antarctic Peninsula. Climatic Change 60, 243–274 (2003).

    Article  Google Scholar 

  24. Stammerjohn, S. E. & Scambos, T. A. Warming reaches the South Pole. Nat. Clim. Chang. 10, 710–711 (2020).

    Article  ADS  Google Scholar 

  25. Atkinson, A., Siegel, V., Pakhomov, E. A., Jessopp, M. J. & Loeb, V. A re-appraisal of the total biomass and annual production of Antarctic krill. Deep Sea Res. Part I 56, 727–740 (2009).

    Article  Google Scholar 

  26. Loeb, V. et al. Effects of sea-ice extent and krill or salp dominance on the Antarctic food web. Nature 387, 897–900 (1997).

    Article  CAS  ADS  Google Scholar 

  27. Cavan, E. L. et al. The importance of Antarctic krill in biogeochemical cycles. Nat. Commun. 10, 4742 (2019).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

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

    Article  ADS  Google Scholar 

  29. Atkinson, A., Schmidt, K., Fielding, S., Kawaguchi, S. & Geissler, P. A. Variable food absorption by Antarctic krill: relationships between diet, egestion rate and the composition and sinking rates of their fecal pellets. Deep Sea Res. Part II 59, 147–158 (2012).

    Article  ADS  Google Scholar 

  30. Gleiber, M. R., Steinberg, D. K. & Ducklow, H. W. Time series of vertical flux of zooplankton fecal pellets on the continental shelf of the western Antarctic Peninsula. Mar. Ecol. Prog Ser. 471, 23–36 (2012).

    Article  ADS  Google Scholar 

  31. Lampitt, R. S. & Antia, A. N. Particle flux in deep seas: regional characteristics and temporal variability. Deep Sea Res. Part I 44, 1377–1403 (1997).

    Article  CAS  Google Scholar 

  32. Décima, M. et al. Salp blooms drive strong increases in passive carbon export in the Southern Ocean. Nat. Commun. 14, 425 (2023).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  33. Pauli, N. C. et al. Krill and salp faecal pellets contribute equally to the carbon flux at the Antarctic Peninsula. Nat. Commun. 12, 7168 (2021).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  34. 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. Part II 138, 116–125 (2017).

    Article  CAS  Google Scholar 

  35. Siegel, V., Reiss, C. S., Dietrich, K. S., Haraldsson, M. & Rohardt, G. Distribution and abundance of Antarctic krill (Euphausia superba) along the Antarctic Peninsula. Deep Sea Res. Part I 77, 63–74 (2013).

    Article  Google Scholar 

  36. Reiss, C. S. in Biology and Ecology of Antarctic Krill Advances in Polar Ecology (ed. Siegel, V.) 101–144 (Springer, 2016).

  37. Siegel, V. Age and growth of Antarctic Euphausiacea (Crustacea) under natural conditions. Mar. Biol. 96, 483–495 (1987).

    Article  Google Scholar 

  38. Fraser, W. R. & Hofmann, E. E. A predator’s perspective on causal links between climate change, physical forcing and ecosystem response. Mar. Ecol. Prog Ser. 265, 1–15 (2003).

    Article  ADS  Google Scholar 

  39. Saba, G. K. et al. Winter and spring controls on the summer food web of the coastal West Antarctic Peninsula. Nat. Commun. 5, 4318 (2014).

    Article  CAS  PubMed  ADS  Google Scholar 

  40. Steinberg, D. K. et al. Long-term (1993–2013) changes in macrozooplankton off the Western Antarctic Peninsula. Deep Sea Res. Part I 101, 54–70 (2015).

    Article  Google Scholar 

  41. Meyer, B. et al. The winter pack-ice zone provides a sheltered but food-poor habitat for larval Antarctic krill. Nat. Ecol. Evol. 1, 1853–1861 (2017).

    Article  PubMed  Google Scholar 

  42. Siegel, V. in Antarctic Ocean and Resources Variability (ed. Sahrhage, D.) 219–230 (Springer, 1988).

  43. Nicol, S. Krill, currents, and sea ice: Euphausia superba and its changing environment. Bioscience. 56, 111–120 (2006).

    Article  Google Scholar 

  44. Kawaguchi, S. in Biology and Ecology of Antarctic Krill (ed. Siegel, V.) 225–246 (Springer, 2016).

  45. Tarling, G. A. & Fielding, S. in Biology and Ecology of Antarctic Krill (ed. Siegel, V.) 279–319 (Springer, 2016).

  46. Belcher, A. et al. Krill faecal pellets drive hidden pulses of particulate organic carbon in the marginal ice zone. Nat. Commun. 10, 889 (2019).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  47. Belcher, A. et al. The potential role of Antarctic krill faecal pellets in efficient carbon export at the marginal ice zone of the South Orkney Islands in spring. Polar Biol. 40, 2001–2013 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Fielding, S. et al. Interannual variability in Antarctic krill (Euphausia superba) density at South Georgia, Southern Ocean: 1997–2013. ICES J. Mar. Sci. 71, 2578–2588 (2014).

    Article  MathSciNet  Google Scholar 

  49. Conroy, J. A., Reiss, C. S., Gleiber, M. R. & Steinberg, D. K. Linking Antarctic krill larval supply and recruitment along the Antarctic Peninsula. Integr. Comp. Biol. 60, 1386–1400 (2020).

    Article  PubMed  Google Scholar 

  50. Cavan, E. L. & Boyd, P. W. Effect of anthropogenic warming on microbial respiration and particulate organic carbon export rates in the sub-Antarctic Southern Ocean. Aquat. Microb. Ecol. 82, 111–127 (2018).

    Article  Google Scholar 

  51. Fuller, W. A. Introduction to Statistical Time Series 698 (Wiley, 1996).

  52. Waters, K. J. & Smith, R. C. Palmer LTER: a sampling grid for the Palmer LTER program. Antarctic J. US 27, 236–239 (1992).

    Google Scholar 

  53. Ducklow, H. W. et al. Particle export from the upper ocean over the continental shelf of the west Antarctic Peninsula: a long-term record, 1992–2007. Deep Sea Res. Part II 55, 2118–2131 (2008).

    Article  ADS  Google Scholar 

  54. Knap, A., Michaels, A. F., Close, A., Ducklow, H. W. & Dickson, A. Protocols for the Joint Global Ocean Flux Study (JGOFS) Core Measurements (UNESCO, 1994).

  55. Karl, D. M., Dore, J. E., Hebel, D. V. & Winn, C. in Marine Particles: Analysis and Characterization (eds Hurd, D. C. & Spencer, D. W.) 71–77 (American Geophysical Union, 1991).

  56. Kim, H. & Ducklow, H. W. A decadal (2002–2014) analysis for dynamics of heterotrophic bacteria in an Antarctic coastal ecosystem: variability and physical and biogeochemical forcings. Front. Mar. Sci. 3, 214 (2016).

    Article  Google Scholar 

  57. Martinson, D. G. & Iannuzzi, R. A. in Antarctic Sea Ice: Physical Processes, Interactions and Variability Vol. 74 (ed. Jeffries, M. O.) 243–271 (American Geophysical Union, 1998).

  58. Siegel, V. & Loeb, V. Length and age at maturity of Antarctic krill. Antarctic. Science 6, 479–482 (1994).

    Google Scholar 

  59. Reid, K. & Brierley, A. S. The use of predator-derived krill length–frequency distributions to calculate krill target strength. CCAMLR Sci. 8, 155–163 (2001).

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Acknowledgements

This research was supported by NSF grants OPP 9011927, 9632763, 0217282 2026045, 0823101, and 1440435 for the Palmer Long-Term Ecological Research (PAL-LTER) project. R.T. thanks the NSF Graduate Research Fellowship Program, and the Department of Earth and Environmental Sciences at Columbia University for support. W.R.F. acknowledges support from the Detroit Zoological Society and NSF Office of Polar Programs (ANT-1745018). We are grateful to the officers and crews of the MV Polar Duke and ARSV Laurence M. Gould, and the science and logistics support on the PAL-LTER research cruises. This work would not be possible without the PAL-LTER field teams who aided in data collection. We thank D. Karl (University of Hawaii), who started the sediment-trap time series in 1992; T. Houlihan (1992–1997) and C. Carrillo (1998–2002) who supervised University of Hawaii sediment-trap deployments; and N. Shelton (2014–2019) for management efforts, deployment and recovery of Lamont-Doherty Earth Observatory sediment traps. U. Magaard (1992–2002) and H. Quinby (2003–2006) supervised sample analyses at University of Hawaii and VIMS, respectively. We thank J. Cope, M. Gleiber and J. Conroy (Virginia Institute of Marine Science) who compiled and supplied krill data for this analysis; R. Ross and L. Quetin for PAL-LTER krill collection and data before 2009; and PAL-LTER colleagues for discussions.

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R.T.: conceptualization, acquisition of data, formal analysis, visualization, writing—original draft. H.W.D.: conceptualization, acquisition of data, writing—review and editing, funding acquisition. D.K.S.: acquisition of data, writing—review and editing. W.R.F.: acquisition of data, writing—review and editing. R.T., H.W.D., D.K.S. and W.R.F. approved the submitted version for publication.

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Correspondence to Rebecca Trinh.

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Extended data figures and tables

Extended Data Fig 1 Bathymetric map of the Antarctic Peninsula.

Location of PAL–LTER sampling stations (black circles) within grid lines labeled –100-600, Palmer Station on Anvers Island (yellow triangle), and long-term sediment trap (red diamond), Marguerite Bay, and Charcot Island are shown. White dashed lines separate geographical coast, shelf, and slope regions of the West Antarctic Peninsula.

Extended Data Fig. 2 Annual POC flux is not a function of peak POC flux duration.

The regression is non-significant (R2 = 0.026, p = 0.54).

Extended Data Fig. 3 Annual POC flux does not correlate with total krill abundance.

a) Annual POC flux (blue circles) and total krill abundance anomaly (black diamonds) time series from 1993–2012. b) Annual POC flux as a function of total krill abundance anomaly (R= –0.15, p = 0.13).

Extended Data Fig. 4 Annual POC flux is not driven by adult krill abundance.

a) Annual POC flux (blue circles) and adult krill abundance anomaly (black diamonds) time series from 1993–2012. b) Annual POC flux as a function of adult krill abundance anomaly (R2 = 0.063, p = 0.35).

Extended Data Fig. 5 Annual POC flux oscillates in sync with adult krill body size obtained through net tows and penguin diets.

Annual POC flux (blue circles), annual mean adult krill body size from net tows (black diamonds), and annual mean adult krill body size from Adélie penguin diets (red squares) time-series from 1993–2012.

Extended Data Fig. 6 Penguin derived krill body size and annual POC flux.

Annual POC flux as a function of annual mean adult krill body size from Adélie penguin diet time-series (R2 = 0.36, p = 0.01).

Extended Data Fig. 7 Krill body size is negatively correlated with krill abundance.

a) Annual mean krill body size (from net tows) as a function of annual krill abundance (R2 = −0.50, p < 0.001). b) Annual mean total krill body size from Adélie penguin diets as a function of annual total krill abundance anomaly (R2 = –0.43, p = 0.001).

Extended Data Table 1 Influence of ecological parameters on POC flux

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Trinh, R., Ducklow, H.W., Steinberg, D.K. et al. Krill body size drives particulate organic carbon export in West Antarctica. Nature 618, 526–530 (2023). https://doi.org/10.1038/s41586-023-06041-4

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