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.

Late Cenozoic cooling restructured global marine plankton communities

Nature volume 614, pages 713–718 (2023)Cite this article

Subjects

Abstract

The geographic ranges of marine organisms, including planktonic foraminifera1, diatoms, dinoflagellates2, copepods3 and fish4, are shifting polewards owing to anthropogenic climate change5. However, the extent to which species will move and whether these poleward range shifts represent precursor signals that lead to extinction is unclear6. Understanding the development of marine biodiversity patterns over geological time and the factors that influence them are key to contextualizing these current trends. The fossil record of the macroperforate planktonic foraminifera provides a rich and phylogenetically resolved dataset that provides unique opportunities for understanding marine biogeography dynamics and how species distributions have responded to ancient climate changes. Here we apply a bipartite network approach to quantify group diversity, latitudinal specialization and latitudinal equitability for planktonic foraminifera over the past eight million years using Triton, a recently developed high-resolution global dataset of planktonic foraminiferal occurrences7. The results depict a global, clade-wide shift towards the Equator in ecological and morphological community equitability over the past eight million years in response to temperature changes during the late Cenozoic bipolar ice sheet formation. Collectively, the Triton data indicate the presence of a latitudinal equitability gradient among planktonic foraminiferal functional groups which is coupled to the latitudinal biodiversity gradient only through the geologically recent past (the past two million years). Before this time, latitudinal equitability gradients indicate that higher latitudes promoted community equitability across ecological and morphological groups. Observed range shifts among marine planktonic microorganisms1,2,8 in the recent and geological past suggest substantial poleward expansion of marine communities even under the most conservative future global warming scenarios.

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

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Fig. 1: Planktonic foraminiferal ecogroups.
Fig. 2: Late Cenozoic climate, specialization indices, and richness.
Fig. 3: Changes in low-ESI zones over the past 8 Myr.

Data availability

All data were sourced from the Triton dataset7 (https://doi.org/10.1038/s41597-021-00942-7).

Code availability

The code used to perform all analyses is available at https://github.com/anshuman21111/foram-networks.

References

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

    Article  ADS  CAS  PubMed  Google Scholar 

  2. Barton, A. D., Irwin, A. J., Finkel, Z. V. & Stock, C. A. Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities. Proc. Natl Acad. Sci. USA 113, 2964–2969 (2016).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  3. Beaugrand, G., Reid, P. C., Ibanez, F., Lindley, J. A. & Edwards, M. Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296, 1692–1694 (2002).

    Article  ADS  CAS  PubMed  Google Scholar 

  4. Cheung, W. W., Watson, R. & Pauly, D. Signature of ocean warming in global fisheries catch. Nature 497, 365–368 (2013).

    Article  ADS  CAS  PubMed  Google Scholar 

  5. Herbert-Read, J. E. et al. A global horizon scan of issues impacting marine and coastal biodiversity conservation. Nat. Ecol. Evol. 6, 1262–1270 (2022).

    Article  PubMed  Google Scholar 

  6. Yasuhara, M. & Deutsch, C. A. Paleobiology provides glimpses of future ocean. Science 375, 25–26 (2022).

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Fenton, I. S. et al. Triton, a new species-level database of Cenozoic planktonic foraminiferal occurrences. Sci. Data 8, 160 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Strack, A., Jonkers, L., Rillo, M. C., Hillebrand, H. & Kucera, M. Plankton response to global warming is characterized by non-uniform shifts in assemblage composition since the last ice age. Nat. Ecol. Evol. 6, 1871–1880 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Barnosky, A. D. et al. Has the Earth’s sixth mass extinction already arrived? Nature 471, 51–57 (2011).

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Mokany, K. & Ferrier, S. Predicting impacts of climate change on biodiversity: a role for semi‐mechanistic community‐level modelling. Divers. Distrib. 17, 374–380 (2011).

    Article  Google Scholar 

  11. Pörtner, H.-O. et al. eds IPCC: Climate Change 2022: Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge Univ. Press, 2022).

  12. Pontarp, M. et al. The latitudinal diversity gradient: novel understanding through mechanistic eco-evolutionary models. Trends Ecol. Evol. 34, 211–223 (2019).

    Article  PubMed  Google Scholar 

  13. Schumm, M. et al. Common latitudinal gradients in functional richness and functional evenness across marine and terrestrial systems. Proc. R. Soc. B 286, 20190745 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Rutherford, S., D’Hondt, S. & Prell, W. Environmental controls on the geographic distribution of zooplankton diversity. Nature 400, 749–753 (1999).

    Article  ADS  CAS  Google Scholar 

  15. Worm, B., Lotze, H. K. & Myers, R. A. Predator diversity hotspots in the blue ocean. Proc. Natl Acad. Sci. USA 100, 9884–9888 (2003).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  16. Tittensor, D. P. et al. Global patterns and predictors of marine biodiversity across taxa. Nature 466, 1098–1101 (2010).

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Fenton, I. S., Pearson, P. N., Dunkley Jones, T. & Purvis, A. Environmental predictors of diversity in recent planktonic foraminifera as recorded in marine sediments. PLoS ONE 11, e0165522 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Chaudhary, C., Saeedi, H. & Costello, M. J. Bimodality of latitudinal gradients in marine species richness. Trends Ecol. Evol. 31, 670–676 (2016).

    Article  PubMed  Google Scholar 

  19. Chaudhary, C., Richardson, A. J., Schoeman, D. S. & Costello, M. J. Global warming is causing a more pronounced dip in marine species richness around the equator. Proc. Natl Acad. Sci. USA 118, e2015094118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Rillo, M. C., Miller, C. G., Kučera, M. & Ezard, T. H. G. Intraspecific size variation in planktonic foraminifera cannot be consistently predicted by the environment. Ecol. Evol. 10, 11579–11590 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Yasuhara, M. et al. Past and future decline of tropical pelagic biodiversity. Proc. Natl Acad. Sci. USA 117, 12891–12896 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  22. Thomas, E. Descent into the icehouse. Geology 36, 191–192 (2008).

    Article  ADS  Google Scholar 

  23. Fenton, I. S. et al. The impact of Cenozoic cooling on assemblage diversity in planktonic foraminifera. Phil. Trans. R. Soc. B 371, 20150224 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Crame, J. A. Early Cenozoic evolution of the latitudinal diversity gradient. Earth Sci. Rev. 202, 103090 (2020).

    Article  Google Scholar 

  25. Yasuhara, M. et al. Time machine biology. Oceanography 33, 16–28 (2020).

    Article  Google Scholar 

  26. Alegret, L., Arreguín-Rodríguez, G. J., Trasviña-Moreno, C. A. & Thomas, E. Turnover and stability in the deep sea: benthic foraminifera as tracers of Paleogene global change. Global Planet. Change 196, 103372 (2021).

    Article  Google Scholar 

  27. Gaskell, D. E. et al. The latitudinal temperature gradient and its climate dependence as inferred from foraminiferal δ18O over the past 95 million years. Proc. Natl Acad. Sci. USA 119, e2111332119 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Mannion, P. D., Upchurch, P., Benson, R. B. & Goswami, A. The latitudinal biodiversity gradient through deep time. Trends Ecol. Evol. 29, 42–50 (2014).

    Article  PubMed  Google Scholar 

  29. Raja, N. B. & Kiessling, W. Out of the extratropics: the evolution of the latitudinal diversity gradient of Cenozoic marine plankton. Proc. R. Soc. B 288, 20210545 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Herbert, T. D. et al. Late Miocene global cooling and the rise of modern ecosystems. Nat. Geosci. 9, 843–847 (2016).

    Article  ADS  CAS  Google Scholar 

  31. Steinthorsdottir, M. et al. The Miocene: the future of the past. Paleoceanogr. Paleoclimatology 36, e2020PA004037 (2021).

    Article  Google Scholar 

  32. Brown, R. M., Chalk, T. B., Crocker, A. J., Wilson, P. A. & Foster, G. L. Late Miocene cooling coupled to carbon dioxide with Pleistocene-like climate sensitivity. Nat. Geosci. 15, 664–670 (2022).

    Article  ADS  CAS  Google Scholar 

  33. Guillermic, M., Misra, S., Eagle, R. & Tripati, A. Atmospheric CO2 estimates for the Miocene to Pleistocene based on foraminiferal δ11B at Ocean Drilling Program Sites 806 and 807 in the Western Equatorial Pacific. Clim. Past 18, 183–207 (2022).

    Article  Google Scholar 

  34. Jablonski, D., Roy, K. & Valentine, J. W. Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient. Science 314, 102–106 (2006).

    Article  ADS  CAS  PubMed  Google Scholar 

  35. Yasuhara, M., Hunt, G., Dowsett, H. J., Robinson, M. M. & Stoll, D. K. Latitudinal species diversity gradient of marine zooplankton for the last three million years. Ecol. Lett. 15, 1174–1179 (2012).

    Article  PubMed  Google Scholar 

  36. Ezard, T. H. G., Aze, T., Pearson, P. N. & Purvis, A. Interplay between changing climate and species' ecology drives macroevolutionary dynamics. Science 332, 349–351 (2011).

    Article  ADS  CAS  PubMed  Google Scholar 

  37. Peters, S. E., Kelly, D. C. & Fraass, A. J. Oceanographic controls on the diversity and extinction of planktonic foraminifera. Nature 493, 398–401 (2013).

    Article  ADS  CAS  PubMed  Google Scholar 

  38. Woodhouse, A. et al. Adaptive ecological niche migration does not negate extinction susceptibility. Sci. Rep. 11, 15411 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  39. Yasuhara, M., Tittensor, D. P., Hillebrand, H. & Worm, B. Combining marine macroecology and palaeoecology in understanding biodiversity: microfossils as a model. Biol. Rev. 92, 199–215 (2017).

    Article  PubMed  Google Scholar 

  40. Bindoff, N. L. in IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (eds Pörtner, H.-O. et al.) (IPCC, Cambridge Univ. Press, 2019).

  41. Aze, T. et al. A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data. Biol. Rev. 86, 900–927 (2011).

    Article  PubMed  Google Scholar 

  42. Delmas, E. et al. Analysing ecological networks of species interactions. Biol. Rev. 94, 16–36 (2019).

    Article  PubMed  Google Scholar 

  43. Rojas, A., Calatayud, J., Kowalewski, M., Neuman, M. & Rosvall, M. A multiscale view of the Phanerozoic fossil record reveals the three major biotic transitions. Commun. Biol. 4, 309 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Swain, A., Devereux, M. & Fagan, W. F. Deciphering trophic interactions in a mid-Cambrian assemblage. iScience 24, 102271 (2021).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  45. Shaw, J. O. et al. Disentangling ecological and taphonomic signals in ancient food webs. Paleobiology 47, 385–401 (2021).

    Article  Google Scholar 

  46. Swain, A., Maccracken, S., Fagan, W. & Labandeira, C. Understanding the ecology of host plant–insect herbivore interactions in the fossil record through bipartite networks. Paleobiology 48, 239–260 (2022).

    Article  Google Scholar 

  47. Poisot, T., Canard, E., Mouquet, N. & Hochberg, M. E. A comparative study of ecological specialization estimators. Methods Ecol. Evol. 3, 537–544 (2012).

    Article  Google Scholar 

  48. Westerhold, T. et al. An astronomically dated record of Earth’s climate and its predictability over the last 66 million years. Science 369, 1383–1387 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  49. Boscolo-Galazzo, F. and Crichton, K.A. et al. Temperature controls carbon cycling and biological evolution in the ocean twilight zone. Science 371, 1148–1152 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  50. Boscolo-Galazzo, F. et al. Late Neogene evolution of modern deep-dwelling plankton. Biogeosciences 19, 743–762 (2022).

    Article  ADS  Google Scholar 

  51. Keller, G. in The Miocene Ocean: Paleoceanography and Biogeography Vol. 163, 177–196 (Geological Society of America, 1985).

  52. Holbourn, A. E. et al. Late Miocene climate cooling and intensification of southeast Asian winter monsoon. Nat. Commun. 9, 1584 (2018).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  53. Willeit, M., Ganopolski, A., Calov, R., Robinson, A. & Maslin, M. The role of CO2 decline for the onset of Northern Hemisphere glaciation. Quat. Sci. Rev. 119, 22–34 (2015).

    Article  ADS  Google Scholar 

  54. Hayashi, T. et al. Latest Pliocene Northern Hemisphere glaciation amplified by intensified Atlantic meridional overturning circulation. Commun. Earth Environ. 1, 25–10 (2020).

    Article  ADS  Google Scholar 

  55. Lam, A. R., Crundwell, M. P., Leckie, R. M., Albanese, J. & Uzel, J. P. Diachroneity rules the mid-latitudes: a test case using late Neogene planktic foraminifera across the Western Pacific. Geosciences 12, 190 (2022).

    Article  ADS  Google Scholar 

  56. Lowery, C. M., Bown, P. R., Fraass, A. J. & Hull, P. M. Ecological response of plankton to environmental change: thresholds for extinction. Annu. Rev. Earth Planet. Sci. 48, 403–429 (2020).

    Article  ADS  CAS  Google Scholar 

  57. Rillo, M. C. et al. On the mismatch in the strength of competition among fossil and modern species of planktonic Foraminifera. Global Ecol. Biogeogr. 28, 1866–1878 (2019).

    Article  Google Scholar 

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

    Article  ADS  Google Scholar 

  59. Monllor-Hurtado, A., Pennino, M. G. & Sanchez-Lizaso, J. L. Shift in tuna catches due to ocean warming. PLoS ONE 12, e0178196 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Brook, B. W., Sodhi, N. S. & Bradshaw, C. J. Synergies among extinction drivers under global change. Trends Ecol. Evol. 23, 453–460 (2008).

    Article  PubMed  Google Scholar 

  61. Mora, C. et al. Biotic and human vulnerability to projected changes in ocean biogeochemistry over the 21st century. PLoS Biol. 11, e1001682 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Renaudie, J., Lazarus, D.B. & Diver, P. NSB (Neptune Sandbox Berlin): an expanded and improved database of marine planktonic microfossil data and deep-sea stratigraphy. Palaeontol. Electron. 23, p.a11 (2020).

    Google Scholar 

  63. Pearson, P. N. in Atlas of Oligocene Planktonic Foraminifera (eds Wade, B. S. et al) 415–428 (Cushman Foundation of Foraminiferal Research, 2018).

  64. Liow, L. H., Skaug, H. J., Ergon, T. & Schweder, T. Global occurrence trajectories of microfossils: environmental volatility and the rise and fall of individual species. Paleobiology 36, 224–252 (2010).

    Article  Google Scholar 

  65. Lazarus, D., Weinkauf, M. & Diver, P. Pacman profiling: a simple procedure to identify stratigraphic outliers in high-density deep-sea microfossil data. Paleobiology 38, 144–161 (2012).

    Article  Google Scholar 

  66. Woodhouse, A. et al. Paleoecology and evolutionary response of planktonic foraminifera to the Plio-Pleistocene intensification of Northern Hemisphere glaciations. Preprint at EGUsphere https://doi.org/10.5194/egusphere-2022-844 (2022).

  67. Woodhouse, A. et al. Paleoecology and evolutionary response of planktonic foraminifera to the mid-Pliocene Warm Period and Plio-Pleistocene bipolar ice sheet expansion. Biogeosciences 20, 121–139 (2023).

    Article  ADS  Google Scholar 

  68. Dormann, C. F., Fründ, J., Blüthgen, N. & Gruber, B. Indices, graphs and null models: analyzing bipartite ecological networks. Op. Ecol. J. 2, 7–24 (2009).

    Article  Google Scholar 

  69. Swain, A. et al. Sampling bias and the robustness of ecological metrics for plant-damage-type association networks. Ecology https://doi.org/10.1002/ecy.3922 (2022).

  70. Julliard, R., Clavel, J., Devictor, V., Jiguet, F. & Couvet, D. Spatial segregation of specialists and generalists in bird communities. Ecol. Lett. 9, 1237–1244 (2006).

    Article  PubMed  Google Scholar 

  71. Vaughan, I. P. et al. econullnetr: an R package using null models to analyse the structure of ecological networks and identify resource selection. Methods Ecol. Evol. 9, 728–733 (2018).

    Article  MathSciNet  Google Scholar 

Download references

Acknowledgements

A.W. and C.M.L. were supported by the University of Texas Institute for Geophysics, A.S. and W.F.F. were supported by the University of Maryland (UMD) and A.J.F. receives funding from NSERC through DGECR-2022-00141 and RGPIN-2022-03305. A.S. additionally acknowledges training and technical support from the COMBINE programme at UMD, the James S. McDonnell Foundation (JSMF), and the Society of Fellows at Harvard University. The authors thank the University of Leeds; the creators of the Triton dataset (to which A.W. also contributed): I. Fenton, T. Aze, D. Lazarus, J. Renaudie, A. Dunhill, J. Young and E. Saupe; the International Ocean Discovery Program, and all predecessor scientific ocean drilling programmes and staff;  and P. Pearson, B. Huber, J. Partin, S. D’Hondt and M. Leckie for scientific discussion of the manuscript.

Author information

Author notes

  1. These authors contributed equally: Adam Woodhouse, Anshuman Swain

Authors and Affiliations

  1. University of Texas Institute for Geophysics, University of Texas at Austin, Austin, TX, USA

    Adam Woodhouse & Christopher M. Lowery

  2. Department of Biology, University of Maryland, College Park, MD, USA

    Anshuman Swain & William F. Fagan

  3. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA

    Anshuman Swain

  4. Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA

    Anshuman Swain

  5. Department of Paleobiology, National Museum of Natural History, Washington, DC, USA

    Anshuman Swain

  6. School of Earth and Ocean Sciences, University of Victoria, Victoria, British Columbia, Canada

    Andrew J. Fraass

  7. Invertebrate Paleontology, The Academy of Natural Sciences of Drexel University, Philadelphia, PA, USA

    Andrew J. Fraass

  8. School of Earth Science, University of Bristol, Bristol, UK

    Andrew J. Fraass

Authors
  1. Adam Woodhouse
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anshuman Swain
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. William F. Fagan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrew J. Fraass
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christopher M. Lowery
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.W. and A.S. formulated the study, generated the data and performed the analyses. All authors contributed to the interpretation of data. A.W. and A.S. conceived and plotted the figures. A.S. wrote the code to perform analyses. All authors contributed to the writing and editing of the manuscript.

Corresponding author

Correspondence to Adam Woodhouse.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature thanks Moriaki Yasuhara and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer review reports are available.

Additional information

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

Extended data figures and tables

Extended Data Table 1 Major network metrics used in this study
Full size table

Supplementary information

Supplementary Information

This file contains supplementary information and figures relating to the manuscript.

Reporting Summary

Peer Review File

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Woodhouse, A., Swain, A., Fagan, W.F. et al. Late Cenozoic cooling restructured global marine plankton communities. Nature 614, 713–718 (2023). https://doi.org/10.1038/s41586-023-05694-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-023-05694-5

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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