Global change drives modern plankton communities away from the pre-industrial state


The ocean—the Earth’s largest ecosystem—is increasingly affected by anthropogenic climate change1,2. Large and globally consistent shifts have been detected in species phenology, range extension and community composition in marine ecosystems3,4,5. However, despite evidence for ongoing change, it remains unknown whether marine ecosystems have entered an Anthropocene6 state beyond the natural decadal to centennial variability. This is because most observational time series lack a long-term baseline, and the few time series that extend back into the pre-industrial era have limited spatial coverage7,8. Here we use the unique potential of the sedimentary record of planktonic foraminifera—ubiquitous marine zooplankton—to provide a global pre-industrial baseline for the composition of modern species communities. We use a global compilation of 3,774 seafloor-derived planktonic foraminifera communities of pre-industrial age9 and compare these with communities from sediment-trap time series that have sampled plankton flux since ad 1978 (33 sites, 87 observation years). We find that the Anthropocene assemblages differ from their pre-industrial counterparts in proportion to the historical change in temperature. We observe community changes towards warmer or cooler compositions that are consistent with historical changes in temperature in 85% of the cases. These observations not only confirm the existing evidence for changes in marine zooplankton communities in historical times, but also demonstrate that Anthropocene communities of a globally distributed zooplankton group systematically differ from their unperturbed pre-industrial state.

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Fig. 1: Concept of the comparison between Anthropocene and pre-industrial communities.
Fig. 2: Changes in planktonic foraminifera communities in response to Anthropocene sea-surface temperature change.
Fig. 3: Global planktonic foraminifera communities change consistently with historical temperature trends.
Fig. 4: Robustness of the sign of change in planktonic foraminifera community composition.

Data availability

The ForCenS core top planktonic foraminifera dataset is available at Pangaea ( and the HadISST data are available from the UK Met Office ( NOAA ERSST v.5 data were provided by the NOAA/OAR/ESRL PSD ( Taxonomically harmonized shell flux data are available at

Code availability

Code is available at


  1. 1.

    IPCC. Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013).

  2. 2.

    Abram, N. J. et al. Early onset of industrial-era warming across the oceans and continents. Nature 536, 411–418 (2016).

  3. 3.

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

  4. 4.

    Beaugrand, G., McQuatters-Gollop, A., Edwards, M. & Goberville, E. Long-term responses of North Atlantic calcifying plankton to climate change. Nat. Clim. Change 3, 263–267 (2013).

  5. 5.

    Hoegh-Guldberg, O. & Bruno, J. F. The impact of climate change on the world’s marine ecosystems. Science 328, 1523–1528 (2010).

  6. 6.

    Waters, C. N. et al. The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science 351, aad2622 (2016).

  7. 7.

    Field, D. B., Baumgartner, T. R., Charles, C. D., Ferreira-Bartrina, V. & Ohman, M. D. Planktonic foraminifera of the California Current reflect 20th-century warming. Science 311, 63–66 (2006).

  8. 8.

    Spielhagen, R. F. et al. Enhanced modern heat transfer to the Arctic by warm Atlantic Water. Science 331, 450–453 (2011).

  9. 9.

    Siccha, M. & Kucera, M. ForCenS, a curated database of planktonic foraminifera census counts in marine surface sediment samples. Sci. Data 4, 170109 (2017).

  10. 10.

    Rosenzweig, C. et al. Attributing physical and biological impacts to anthropogenic climate change. Nature 453, 353–357 (2008).

  11. 11.

    Hillebrand, H. et al. Biodiversity change is uncoupled from species richness trends: consequences for conservation and monitoring. J. Appl. Ecol. 55, 169–184 (2018).

  12. 12.

    Gonzalez, A. et al. Estimating local biodiversity change: a critique of papers claiming no net loss of local diversity. Ecology 97, 1949–1960 (2016).

  13. 13.

    Morey, A. E., Mix, A. C. & Pisias, N. G. Planktonic foraminiferal assemblages preserved in surface sediments correspond to multiple environment variables. Quat. Sci. Rev. 24, 925–950 (2005).

  14. 14.

    Bé, A. W. H. & Tolderlund, D. S. in The Micropaleontology of Oceans (eds Funnell, B. M. & Riedel, W. R.) Ch. 6, 105–149 (Cambridge Univ. Press, 1971).]

  15. 15.

    Morard, R. et al. Surface ocean metabarcoding confirms limited diversity in planktonic foraminifera but reveals unknown hyper-abundant lineages. Sci. Rep. 8, 2539 (2018).

  16. 16.

    Rebotim, A. et al. Factors controlling the depth habitat of planktonic foraminifera in the subtropical eastern North Atlantic. Biogeosciences 14, 827–859 (2017).

  17. 17.

    CLIMAP Project Members. Seasonal Reconstruction of the Earth’s surface at the Last Glacial Maximum. Map and Chart Series MC-36 (ed. McIntyre, A.) (Geological Society of America, 1981).

  18. 18.

    Kucera, M. et al. Reconstruction of sea-surface temperatures from assemblages of planktonic foraminifera: multi-technique approach based on geographically constrained calibration data sets and its application to glacial Atlantic and Pacific Oceans. Quat. Sci. Rev. 24, 951–998 (2005).

  19. 19.

    Ruddiman, W. F., Tolderlund, D. S. & Bé, A. W. H. Foraminiferal evidence of a modern warming of the North Atlantic Ocean. Deep Sea Res. 17, 141–155 (1970).

  20. 20.

    Berger, W. H. Planktonic Foraminifera: selective solution and paleoclimatic interpretation. Deep Sea Res. 15, 31–43 (1968).

  21. 21.

    Berger, W. H. Planktonic Foraminifera: selective solution and the lysocline. Mar. Geol. 8, 111–138 (1970).

  22. 22.

    Archer, D. E. An atlas of the distribution of calcium carbonate in sediments of the deep sea. Glob. Biogeochem. Cycles 10, 159–174 (1996).

  23. 23.

    von Gyldenfeldt, A.-B., Carstens, J. & Meincke, J. Estimation of the catchment area of a sediment trap by means of current meters and foraminiferal tests. Deep Sea Res. 47, 1701–1717 (2000).

  24. 24.

    van Sebille, E. et al. Ocean currents generate large footprints in marine palaeoclimate proxies. Nat. Commun. 6, 6521 (2015).

  25. 25.

    Enquist, B. J. et al. in Advances in Ecological Research Vol. 52 (eds Pawar, S. et al.) 249–318 (Academic, 2015).

  26. 26.

    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).

  27. 27.

    Jonkers, L. & Kučera, M. Global analysis of seasonality in the shell flux of extant planktonic Foraminifera. Biogeosciences 12, 2207–2226 (2015).

  28. 28.

    Prell, W. The Stability of Low-Latitude Sea-Surface Temperatures, an Evaluation of the CLIMAP Reconstruction with Emphasis on the Positive SST Anomalies. Report No. TR025 (US Department of Energy, 1985).

  29. 29.

    Darling, K. F. & Wade, C. M. The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes. Mar. Micropaleontol. 67, 216–238 (2008).

  30. 30.

    R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2016).

  31. 31.

    Juggins, S. rioja: Analysis of Quaternary Science Data. R package version 0.9-15.1 (2017).

  32. 32.

    Wickham, H. Reshaping data with the reshape package. J. Stat. Softw. 21, 1–20 (2007).

  33. 33.

    Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).

  34. 34.

    Hijmans, R. J., Williams, E. & Vennes, C. geosphere: Spherical Trigonometry. R package version 1.5-7 (2017).

  35. 35.

    Wickham, H. & Bryan, J. readxl: Read Excel Files. R package version 1.1.0 (2018).

  36. 36.

    Harrell, F. E. Jr. Hmisc: Harrell Miscellaneous. R package version 4.1-1 (2018).

  37. 37.

    Hijmans, R. J. et al. raster: Geographic Data Analysis and Modeling. R package version 2.6-7. (2017).

  38. 38.

    Pebesma, E. J. & Bivand, R. S. Classes and methods for spatial data in R. R News 5, 9–13 (2005).

  39. 39.

    Bivand, R. S., Pebesma, E. & Gómez-Rubio, V. Applied Spatial Data Analysis with R (Springer, 2008).

  40. 40.

    Bivand, R. et al. rgdal: Bindings for the 'Geospatial' Data Abstraction Library. R package version 1.3-1 (2018).

  41. 41.

    Berger, W. H. & Heath, G. R. Vertical mixing in pelagic sediments. J. Mar. Res. 26, 134–143 (1968).

  42. 42.

    Burwicz, E. B., Rüpke, L. H. & Wallmann, K. Estimation of the global amount of submarine gas hydrates formed via microbial methane formation based on numerical reaction-transport modeling and a novel parameterization of Holocene sedimentation. Geochim. Cosmochim. Acta 75, 4562–4576 (2011).

  43. 43.

    Boudreau, B. P. Mean mixed depth of sediments: the wherefore and the why. Limnol. Oceanogr. 43, 524–526 (1998).

  44. 44.

    Al-Sabouni, N., Kucera, M. & Schmidt, D. N. Vertical niche separation control of diversity and size disparity in planktonic foraminifera. Mar. Micropaleontol. 63, 75–90 (2007).

  45. 45.

    Huang, B. et al. NOAA Extended Reconstructed Sea Surface Temperature (ERSST). Version 5 (NOAA National Centers for Environmental Information, 2017).

  46. 46.

    Huang, B. et al. Further exploring and quantifying uncertainties for extended reconstructed sea surface temperature (ERSST) version 4 (v4). J. Clim. 29, 3119–3142 (2016).

  47. 47.

    Asahi, H. & Takahashi, K. A 9-year time-series of planktonic foraminifer fluxes and environmental change in the Bering Sea and the central subarctic Pacific Ocean, 1990–1999. Prog. Oceanogr. 72, 343–363 (2007).

  48. 48.

    Deuser, W. G. & Ross, E. H. Seasonally abundant planktonic foraminifera of the Sargasso Sea; succession, deep-water fluxes, isotopic compositions, and paleoceanographic implications. J. Foraminiferal Res. 19, 268–293 (1989).

  49. 49.

    Deuser, W. G., Ross, E. H., Hemleben, C. & Spindler, M. Seasonal changes in species composition, numbers, mass, size, and isotopic composition of planktonic foraminifera settling into the deep Sargasso Sea. Palaeogeogr. Palaeoclimatol. Palaeoecol. 33, 103–127 (1981).

  50. 50.

    Northcote, L. C. & Neil, H. L. Seasonal variations in foraminiferal flux in the Southern Ocean, Campbell Plateau, New Zealand. Mar. Micropaleontol. 56, 122–137 (2005).

  51. 51.

    Guptha, M. V. S., Curry, W. B., Ittekkot, V. & Muralinath, A. S. Seasonal variation in the flux of planktic Foraminifera; sediment trap results from the Bay of Bengal, northern Indian Ocean. J. Foraminiferal Res. 27, 5–19 (1997).

  52. 52.

    Žarić, S., Donner, B., Fischer, G., Mulitza, S. & Wefer, G. Sensitivity of planktic foraminifera to sea surface temperature and export production as derived from sediment trap data. Mar. Micropaleontol. 55, 75–105 (2005).

  53. 53.

    Reuter, R. T., Jonkers, L. & Kucera, M. Planktonic foraminifera shell flux data from sediment trap CB-3. PANGAEA (2016).

  54. 54.

    Ortiz, J. D. & Mix, A. C. The spatial distribution and seasonal succession of planktonic foraminifera in the California Current off Oregon, September 1987 – September 1988. Geol. Soc. Lond. Spec. Publ. 64, 197–213 (1992).

  55. 55.

    Jensen, S. Planktische Foraminiferen im Europaischen Nordmeer: Verbreitung und Vertikalfluss sowie ihre Entwicklung wahrend der letzten 15000 Jahre. PhD thesis, Univ. Kiel (1998).

  56. 56.

    Poore, R. Z., Tedesco, K. A. & Spear, J. W. Seasonal flux and assemblage composition of planktic foraminifers from a sediment-trap study in the northern Gulf of Mexico. J. Coast. Res. 63, 6–19 (2013).

  57. 57.

    Reynolds, C. E., Richey, J. N. & Poore, R. Z. Seasonal Flux and Assemblage Composition of Planktic Foraminifera from the Northern Gulf of Mexico, 2008–2012. US Geological Survey Open-File Report 2013–1243 (USGS, 2013).

  58. 58.

    Jonkers, L., Reynolds, C. E., Richey, J. & Hall, I. R. Lunar periodicity in the shell flux of planktonic foraminifera in the Gulf of Mexico. Biogeosciences 12, 3061–3070 (2015).

  59. 59.

    Wolfteich, C. M. Sattelite-Derived Sea Surface Temperature, Mesoscale Variability, And Foraminiferal Production in the North Atlantic. MSc thesis, MIT and WHOI (1994).

  60. 60.

    Jonkers, L., Brummer, G.-J. A., Peeters, F. J. C., van Aken, H. M. & De Jong, M. F. Seasonal stratification, shell flux, and oxygen isotope dynamics of left-coiling N. pachyderma and T. quinqueloba in the western subpolar North Atlantic. Paleoceanography 25, PA2204 (2010).

  61. 61.

    Jonkers, L., van Heuven, S., Zahn, R. & Peeters, F. J. C. Seasonal patterns of shell flux, δ18O and δ13C of small and large N. pachyderma (s) and G. bulloides in the subpolar North Atlantic. Paleoceanography 28, 164–174 (2013).

  62. 62.

    Reuter, R. T., Jonkers, L., Brummer, G. J. & Kucera, M. Planktonic foraminifera shell flux data from sediment trap IRM-1. PANGAEA (2018).

  63. 63.

    Mohtadi, M. et al. Low-latitude control on seasonal and interannual changes in planktonic foraminiferal flux and shell geochemistry off south Java: A sediment trap study. Paleoceanography 24, PA1201 (2009).

  64. 64.

    Rigual-Hernández, A. S., Sierro, F. J., Bárcena, M. A., Flores, J. A. & Heussner, S. Seasonal and interannual changes of planktic foraminiferal fluxes in the Gulf of Lions (NW Mediterranean) and their implications for paleoceanographic studies: two 12-year sediment trap records. Deep Sea Res. 66, 26–40 (2012).

  65. 65.

    Donner, B. & Wefer, G. Flux and stable isotope composition of Neogloboquadrina pachyderma and other planktonic foraminifers in the Southern Ocean (Atlantic sector). Deep Sea Res. 41, 1733–1743 (1994).

  66. 66.

    Storz, D., Schulz, H., Waniek, J. J., Schulz-Bull, D. E. & Kučera, M. Seasonal and interannual variability of the planktic foraminiferal flux in the vicinity of the Azores Current. Deep Sea Res. 56, 107–124 (2009).

  67. 67.

    Kuroyanagi, A., Kawahata, H., Nishi, H. & Honda, M. C. Seasonal changes in planktonic foraminifera in the northwestern North Pacific Ocean: sediment trap experiments from subarctic and subtropical gyres. Deep Sea Res. 49, 5627–5645 (2002).

  68. 68.

    Sagawa, T., Kuroyanagi, A., Irino, T., Kuwae, M. & Kawahata, H. Seasonal variations in planktonic foraminiferal flux and oxygen isotopic composition in the western North Pacific: implications for paleoceanographic reconstruction. Mar. Micropaleontol. 100, 11–20 (2013).

  69. 69.

    Alderman, S. E. Planktonic Foraminifera in the Sea of Okhotsk: Population and Stable Isotopic Analysis from a Sediment Trap. MSc thesis, MIT and WHOI (1996).

  70. 70.

    Sautter, L. R. & Thunell, R. C. Seasonal succession of planktonic foraminifera; results from a four-year time-series sediment trap experiment in the Northeast Pacific. J. Foraminiferal Res. 19, 253–267 (1989).

  71. 71.

    King, A. L. & Howard, W. R. Planktonic foraminiferal flux seasonality in Subantarctic sediment traps: a test for paleoclimate reconstructions. Paleoceanography 18, 1019 (2003).

  72. 72.

    Curry, W. B., Ostermann, D. R., Guptha, M. V. S. & Ittekkot, V. Foraminiferal production and monsoonal upwelling in the Arabian Sea: evidence from sediment traps. Geol. Soc. Lond. Spec. Publ. 64, 93–106 (1992).

  73. 73.

    Mohiuddin, M. M., Nishimura, A., Tanaka, Y. & Shimamoto, A. Regional and interannual productivity of biogenic components and planktonic foraminiferal fluxes in the northwestern Pacific Basin. Mar. Micropaleontol. 45, 57–82 (2002).

  74. 74.

    Mohiuddin, M. M., Nishimura, A. & Tanaka, Y. Seasonal succession, vertical distribution, and dissolution of planktonic foraminifera along the Subarctic Front: implications for paleoceanographic reconstruction in the northwestern Pacific. Mar. Micropaleontol. 55, 129–156 (2005).

  75. 75.

    Xiang, R. et al. Seasonal flux variability of planktonic foraminifera during 2009–2011 in a sediment trap from Xisha Trough, South China Sea. Aquat. Ecosyst. Health Manage. 18, 403–413 (2015).

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We thank R. Reuter for help with foraminifera analysis and acknowledge funding by the Volkswagen Stiftung for the MarBAS (Marine Biodiversität—Analyse über zeitliche und räumliche Skalen) project as well as by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) through Germany’s Excellence Strategy (EXC-2077, grant no 390741603). M.K. was funded through DFG-Research Center/Cluster of Excellence ‘The Ocean in the Earth System’.

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Nature thanks Andrew J. Fraass, Anthony Richardson and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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L.J. and M.K. designed research. L.J. compiled and analysed the data. All authors discussed the results and contributed to the writing of the manuscript.

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Correspondence to Lukas Jonkers.

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Extended data figures and tables

Extended Data Fig. 1 Pre-industrial age of the sedimentary samples.

Mean age in years of core top sediment estimate using the depth solution of a previous study41 (contours). The grey box denotes the likely average ages of the core top sediments based on our best estimate of sediment accumulation rate (in cm per 1,000 years (kyr)) and bioturbation depth. Irrespective of the sampling date (mostly pre-1980), the average sedimentary species composition predates the Anthropocene.

Extended Data Fig. 2 Linear regression between dissimilarity and latitudinal distance in the sedimentary species assemblages.

The relationship (shown in red) is used to estimate the latitudinal displacement based on the dissimilarity between the modern and pre-industrial species composition. Example for time series S47 from the south of New Zealand (Extended Data Table 1).

Extended Data Fig. 3 Insensitivity of planktonic foraminifera assemblage change to size fraction.

The direction of change for planktonic foraminifera species communities (warming or cooling) was inferred from sediment-trap time series for which the samples were larger than 125 μm and larger than 150 μm. Colours and symbols are as in Fig. 3b. W and C indicate warming and cooling, respectively, with the first letter indicating the historical change and the second the change as indicated by the species composition. Both small and large shell sizes are dominated by a change in the species community that is consistent with the direction of historical change in temperatures. The observed pattern is thus insensitive to the inclusion of sediment-trap time series that used a slightly smaller size fraction than the sediment samples.

Extended Data Fig. 4 Assessing uncertainty in the historical change in temperatures by comparing the HadISST and ERSST temperature products.

a, Comparison of the relationships between the historical change in temperature and the difference between the modern and sedimentary species composition (based on linear regression weighted to the duration of the time series; see also Fig. 2a). The relationship has a similar slope for both sea-surface temperature products, even though the relationship based on ERSST data has a larger uncertainty. Shaded error envelopes show 95% confidence intervals of the regression. b, Histograms of consistency and direction of changes in the species communities (Fig. 3a). The pattern of change is broadly similar for both products, which indicates that although the observations are to some degree sensitive to the uncertainty in the historical change in temperatures, they are largely consistent between the two datasets.

Extended Data Table 1 Sediment-trap time series used to determine modern species compositions

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Jonkers, L., Hillebrand, H. & Kucera, M. Global change drives modern plankton communities away from the pre-industrial state. Nature 570, 372–375 (2019).

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