The Chicxulub bolide impact 66 million years ago drove the near-instantaneous collapse of ocean ecosystems. The devastating loss of diversity at the base of ocean food webs probably triggered cascading extinctions across all trophic levels1,2,3 and caused severe disruption of the biogeochemical functions of the ocean, and especially disrupted the cycling of carbon between the surface and deep sea4,5. The absence of sufficiently detailed biotic data that span the post-extinction interval has limited our understanding of how ecosystem resilience and biochemical function was restored; estimates6,7,8 of ecosystem ‘recovery’ vary from less than 100 years to 10 million years. Here, using a 13-million-year-long nannoplankton time series, we show that post-extinction communities exhibited 1.8 million years of exceptional volatility before a more stable equilibrium-state community emerged that displayed hallmarks of resilience. The transition to this new equilibrium-state community with a broader spectrum of cell sizes coincides with indicators of carbon-cycle restoration and a fully functioning biological pump9. These findings suggest a fundamental link between ecosystem recovery and biogeochemical cycling over timescales that are longer than those suggested by proxies of export production7,8, but far shorter than the return of taxonomic richness6. The fact that species richness remained low as both community stability and biological pump efficiency re-emerged suggests that ecological functions rather than the number of species are more important to community resilience and biochemical functions.
This is a preview of subscription content
Subscription info for Chinese customers
We have a dedicated website for our Chinese customers. Please go to naturechina.com to subscribe to this journal.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Schulte, P. et al. The Chicxulub asteroid impact and mass extinction at the Cretaceous–Paleogene boundary. Science 327, 1214–1218 (2010).
Coxall, H. K., D’Hondt, S. & Zachos, J. C. Pelagic evolution and environmental recovery after the Cretaceous–Paleogene mass extinction. Geology 34, 297–300 (2006).
Bown, P. R., Lees, J. A. & Young, J. R. in Coccolithophores: from Molecular Processes to Global Impact (eds Thierstein, H. R. & Young, J. R.) 481–508 (Springer, 2004).
D’Hondt, S. Consequences of the Cretaceous/Paleogene mass extinction for marine ecosystems. Annu. Rev. Ecol. Evol. Syst. 36, 295–317 (2005).
Henehan, M. J., Hull, P. M., Penman, D. E., Rae, J. W. B. & Schmidt, D. N. Biogeochemical significance of pelagic ecosystem function: an end-Cretaceous case study. Phil. Trans. R. Soc. B 371, 20150510 (2016).
Kirchner, J. W. & Weil, A. Delayed biological recovery from extinctions throughout the fossil record. Nature 404, 177–180 (2000).
Sepúlveda, J., Wendler, J. E., Summons, R. E. & Hinrichs, K.-U. Rapid resurgence of marine productivity after the Cretaceous–Paleogene mass extinction. Science 326, 129–132 (2009).
Alegret, L., Thomas, E. & Lohmann, K. C. End-Cretaceous marine mass extinction not caused by productivity collapse. Proc. Natl Acad. Sci. USA 109, 728–732 (2012).
Birch, H. S., Coxall, H. K., Pearson, P. N., Kroon, D. & Schmidt, D. N. Partial collapse of the marine carbon pump after the Cretaceous–Paleogene boundary. Geology 44, 287–290 (2016).
Bown, P. Selective calcareous nannoplankton survivorship at the Cretaceous–Tertiary boundary. Geology 33, 653–656 (2005).
Gallala, N., Zaghbib-Turki, D., Arenillas, I., Arz, J. A. & Molina, E. Catastrophic mass extinction and assemblage evolution in planktic foraminifera across the Cretaceous/Paleogene (K/Pg) boundary at Bidart (SW France). Mar. Micropaleontol. 72, 196–209 (2009).
Hull, P. Life in the aftermath of mass extinctions. Curr. Biol. 25, R941–R952 (2015).
Barnosky, A. D. et al. Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems. Science 355, eaah4787 (2017).
Hodgson, D., McDonald, J. L. & Hosken, D. J. What do you mean, ‘resilient’? Trends Ecol. Evol. 30, 503–506 (2015).
Varol, O. in Nannofossils and their Applications. British Micropaleontological Society Series (eds Crux, J. A. & van Heck, S. E.) 267–310 (Ellis Horwood, 1989).
Pospichal, J. J. in The Cretaceous–Tertiary Event and Other Catastrophes in Earth History. Geological Society of America Special Paper 307 (eds Ryder, G. et al.) 335–360 (Geological Society of America, 1996).
Vellekoop, J. et al. Rapid short-term cooling following the Chicxulub impact at the Cretaceous–Paleogene boundary. Proc. Natl Acad. Sci. USA 111, 7537–7541 (2014).
MacLeod, K. G., Quinton, P. C., Sepúlveda, J. & Negra, M. H. Postimpact earliest Paleogene warming shown by fish debris oxygen isotopes (El Kef, Tunisia). Science 360, 1467–1469 (2018).
Sprain, C. J. et al. The eruptive tempo of Deccan volcanism in relation to the Cretaceous–Paleogene boundary. Science 363, 866–870 (2019).
Zachos, J. C., McCarren, H., Murphy, B., Röhl, U. & Westerhold, T. Tempo and scale of late Paleocene and early Eocene carbon isotope cycles: implications for the origin of hyperthermals. Earth Planet. Sci. Lett. 299, 242–249 (2010).
Gibbs, S. J. et al. Scaled biotic disruption during early Eocene global warming events. Biogeosciences 9, 4679–4688 (2012).
Esmeray-Senlet, S. et al. Evidence for reduced export productivity following the Cretaceous/Paleogene mass extinction. Paleoceanography 30, 718–738 (2015).
Alegret, L. & Thomas, E. Deep-sea environments across the Cretaceous/Paleogene boundary in the eastern South Atlantic Ocean (ODP leg 208, Walvis Ridge). Mar. Micropaleontol. 64, 1–17 (2007).
Buesseler, K. O. & Boyd, P. W. Shedding light on processes that control particle export and flux attenuation in the twilight zone of the open ocean. Limnol. Oceanogr. 54, 1210–1232 (2009).
Fischer, G. & Karakaş, G. Sinking rates and ballast composition of particles in the Atlantic Ocean: implications for the organic carbon fluxes to the deep ocean. Biogeosciences 6, 85–102 (2009).
Hansen, B. et al. The size ratio between planktonic predators and their prey. Limnol. Oceanogr. 39, 395–403 (1994).
Gerstel, J., Thunell, R. & Ehrlich, R. Danian faunal succession: Planktonic foraminiferal response to a changing marine environment. Geology 15, 665–668 (1987).
Fuqua, L. M., Bralower, T. J., Arthur, M. A. & Patzkowsky, M. E. Evolution of calcareous nannoplankton and the recovery of marine food webs after the Cretaceous–Paleocene mass extinction. Palaios 23, 185–194 (2008).
Barnosky, A. D. et al. Has the Earth’s sixth mass extinction already arrived? Nature 471, 51–57 (2011).
Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).
Reich, P. B. et al. Impacts of biodiversity loss escalate through time as redundancy fades. Science 336, 589–592 (2012).
Westerhold, T., Röhl, U., Donner, B. & Zachos, J. C. Global extent of early Eocene hyperthermal events: a new Pacific benthic foraminiferal isotope record from Shatsky Rise (ODP Site 1209). Paleoceanogr. Paleoclimatol. 33, 626–642 (2018).
Westerhold, T. & Röhl, U. Data report: revised composite depth records for Shatsky Rise Sites 1209, 1210, and 1211. In Proc. Ocean Drilling Program, Scientific Results 198 (eds. Bralower, T. J. et al.) 1–26 (2006).
Dinarès-Turell, J., Westerhold, T., Pujalte, V., Röhl, U. & Kroon, D. Astronomical calibration of the Danian stage (Early Paleocene) revisited: settling chronologies of sedimentary records across the Atlantic and Pacific Oceans. Earth Planet. Sci. Lett. 405, 119–131 (2014).
Westerhold, T. et al. Astronomical calibration of the Paleocene time. Palaeogeogr. Palaeoclimatol. Palaeoecol. 257, 377–403 (2008).
Bown, P. R. & Young, J. R. in Calcareous Nannofossil Biostratigraphy (ed. Bown, P. R.) 16–28 (Chapman & Hall, 1998).
Perch-Nielsen, K. in Plankton Stratigraphy (eds. Bolli, H. M. et al.) 427–555 (Cambridge Univ. Press, 1985).
Bown, P. R. Paleocene calcareous nannofossils from Tanzania (TDP sites 19, 27 and 38). J. Nannoplankton Res. 36, 1–32 (2016).
Young, J. R., Bown, P. R. & Lees, J. A. Nannotax 3. http://www.mikrotax.org/Nannotax3/; accessed 2015–2019.
Bown, P. R. et al. A Paleogene calcareous microfossil Konservat-Lagerstätte from the Kilwa Group of coastal Tanzania. Geol. Soc. Am. Bull. 120, 3–12 (2008).
Paillard, D., Labeyrie, L. & Yiou, P. Macintosh program performs time-series analysis. Eos 77, 379 (1996).
Cleland, E. E. Biodiversity and ecosystem stability. Nature Education Knowledge 3, 14 (2011).
Gradstein, F. M., Ogg, J. G., Schmitz, M. D. & Ogg, G. M. The Geologic Time Scale 2012 1st edn (Elsevier, 2012).
Mai, H., Perch-Nielsen, K., Willems, H. & Romein, A. J. T. Fossil coccospheres from the K/T boundary section from Geulhemmerberg, The Netherlands. Micropaleontology 43, 281–302 (1997).
Mai, H., Hildebrand-Habel, T., Perch-Nielsen, K. V. S. & Willems, H. Paleocene coccospheres from DSDP leg 39, Site 356, Sao Paulo Plateau, S Atlantic Ocean. J. Nannoplankton Res. 20, 21–29 (1998).
Gibbs, S. J., Sheward, R. M., Bown, P. R., Poulton, A. J. & Alvarez, S. A. Warm plankton soup and red herrings: calcareous nannoplankton cellular communities and the Palaeocene–Eocene thermal maximum. Phil. Trans. R. Soc. A 376, 20170075 (2018).
Schmidt, A. et al. Selective environmental stress from sulphur emitted by continental flood basalt eruptions. Nat. Geosci. 9, 77–82 (2016).
Westerhold, T., Röhl, U., Donner, B., McCarren, H. K. & Zachos, J. C. A complete high-resolution Paleocene benthic stable isotope record for the central Pacific (ODP Site 1209). Paleoceanography 25, PA2216 (2011).
Littler, K., Röhl, U., Westerhold, T. & Zachos, J. C. A high-resolution benthic stable-isotope record for the South Atlantic: implications for orbital-scale changes in Late Paleocene–Early Eocene climate and carbon cycling. Earth Planet. Sci. Lett. 401, 18–30 (2014).
Coccioni, R. et al. The Dan-C2 hyperthermal event at Gubbio (Italy): global implications, environmental effects, and cause(s). Earth Planet. Sci. Lett. 297, 298–305 (2010).
Shipboard Scientific Party. Site 1209. In Proc. Ocean Drilling Program, Initial Reports 198 (eds. Bralower, T. J. et al.) 1–102 (2002).
Westerhold, T., Röhl, U., Frederichs, T., Bohaty, S. M. & Zachos, J. C. Astronomical calibration of the geological timescale: closing the middle Eocene gap. Clim. Past 11, 1181–1195 (2015).
Stap, L. et al. High-resolution deep-sea carbon and oxygen isotope records of Eocene thermal maximum 2 and H2. Geology 38, 607–610 (2010).
Zeebe, R. E., Westerhold, T., Littler, K. & Zachos, J. C. Orbital forcing of the Paleocene and Eocene carbon cycle. Paleoceanography 32, 440–465 (2017).
Birch, H., Coxall, H. K. & Pearson, P. N. Evolutionary ecology of Early Paleocene planktonic foraminifera: size, depth habitat and symbiosis. Paleobiology 38, 374–390 (2012).
Monechi, S., Reale, V., Bernaola, G. & Balestra, B. The Danian/Selandian boundary at Site 1262 (South Atlantic) and in the Tethyan region: biomagnetostratigraphy, evolutionary trends in fasciculiths and environmental effects of the latest Danian event. Mar. Micropaleontol. 98, 28–40 (2013).
Aubry, M.-P., Bord, D. & Rodriguez, O. New taxa of the order Discoasterales Hay 1977. Micropaleontology 57, 269–288 (2011).
Monechi, S., Reale, V., Bernaola, G. & Balestra, B. Taxonomic review of early Paleocene fasciculiths. Micropaleontology 58, 351–365 (2012).
Agnini, C. et al. High-resolution nannofossil biochronology of middle Paleocene to early Eocene at ODP Site 1262: implications for calcareous nannoplankton evolution. Mar. Micropaleontol. 64, 215–248 (2007).
Cramer, B. S., Wright, J. D., Kent, D. V. & Aubry, M.-P. Orbital climate forcing of δ13C excursions in the late Paleocene–early Eocene (chrons C24n–C25n). Paleoceanography 18, 1097 (2003).
Nicolo, M. J., Dickens, G. R., Hollis, C. J. & Zachos, J. C. Multiple early Eocene hyperthermals: their sedimentary expression on the New Zealand continental margin and in the deep sea. Geology 35, 699–702 (2007).
Lourens, L. J. et al. Astronomical pacing of late Palaeocene to early Eocene global warming events. Nature 435, 1083–1087 (2005).
Zachos, J. C. et al. A transient rise in tropical sea surface temperature during the Paleocene–Eocene thermal maximum. Science 302, 1551–1554 (2003).
Zachos, J. C. et al. Rapid acidification of the ocean during the Paleocene-Eocene thermal maximum. Science 308, 1611–1615 (2005).
Bernaola, G. et al. Evidence of an abrupt environmental disruption during the mid-Paleocene biotic event (Zumaia section, western Pyrenees). Bull. Geol. Soc. Am. 119, 785–795 (2007).
Quillévéré, F., Aubry, M.-P., Norris, R. D. & Berggren, W. A. Paleocene oceanography of the eastern subtropical Indian Ocean: an integrated magnetobiostratigraphic and stable isotope study of ODP hole 761B (Wombat Plateau). Palaeogeogr. Palaeoclimatol. Palaeoecol. 184, 371–405 (2002).
Arenillas, I., Molina, E., Ortiz, S. & Schmitz, B. Foraminiferal and δ13C isotopic event-stratigraphy across the Danian–Selandian transition at Zumaya (northern Spain): chronostratigraphic implications. Terra Nova 20, 38–44 (2008).
Bornemann, A. et al. Latest Danian carbon isotope anomaly and associated environmental change in the southern Tethys (Nile Basin, Egypt). J. Geol. Soc. Lond. 166, 1135–1142 (2009).
Jehle, S., Bornemann, A., Deprez, A. & Speijer, R. Planktic foraminiferal response to the latest Danian event in the Pacific Ocean (ODP Site 1210). Geophysical Research Abstracts 17, EGU2015–9115 (2015).
Schmitz, B. et al. High-resolution iridium, δ13C, δ18O, foraminifera and nannofossil profiles across the latest Paleocene benthic extinction event at Zumaya, Spain. Palaeogeogr. Palaeoclimatol. Palaeoecol. 133, 49–68 (1997).
Schmitz, B., Molina, E. & von Salis, K. The Zumaya section in Spain: a possible global stratotype section for the Selandian and Thanetian stages. Newsl. Stratigr. 36, 35–42 (1998).
Kroon, D. & Zachos, J. C. & Leg 208 Scientific Party. Leg 208 synthesis: Cenozoic climate cycles and excursions. In Proc. Ocean Drilling Program, Scientific Results 208 (eds. Kroon, D. et al.) 1–55 (2007).
Quillévéré, F., Norris, R. D., Kroon, D. & Wilson, P. A. Transient ocean warming and shifts in carbon reservoirs during the early Danian. Earth Planet. Sci. Lett. 265, 600–615 (2008).
van Heck, S. E. & Prins, B. A refined nannoplankton zonation for the Danian of the central North Sea. Abh. Geol. Bundesanstalt 39, 285–303 (1987).
Sáez, A. G. et al. in Coccolithophores – from Molecular Processes to Global Impact (eds Thierstein, H. R. & Young, J. R.) 251–270 (Springer 2004).
Young, J. R., Geisen, M. & Probert, I. A review of selected aspects of coccolithophore biology with implications for palaeobiodiversity estimation. Micropaleontology 51, 267–288 (2005).
Young, J. R., Liu, H., Probert, I., Aris-Brosou, H. & de Vargas, C. Morphospecies versus phylospecies concepts for evaluating phytoplankton diversity: the case of the coccolithophores. Cryptogam. Algol. 35, 353–377 (2014).
This research used samples provided by the International Ocean Discovery Program. We thank the Royal Society for funding S.J.G. through a URF. R.M.S. was funded jointly through a Vice Chancellor’s studentship from the University of Southampton and a Natural Environment Research Council (NERC) studentship (award reference 1272561) and H.K. was supported in part by a UCL Dean’s prize. We thank the European Union for post-doctoral research funding for S.A.A. (grant ERC-2013-CoG-617303). A.R. was supported in part by an award from the Heising-Simons Foundation as well as by grant ERC-2013-CoG-617303. We thank T. Ezard for contributions to the interpretation of the datasets and P. Wilson for his independent editing of the manuscript.
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Peer review information Nature thanks Appy Sluijs and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Extended data figures and tables
Extended Data Fig. 1 Location of ODP Site 1209 (black star) with respect to model-simulated late Cretaceous major ocean current and circulation patterns.
a, Barotropic stream function (Sv) simulated in a late Cretaceous configuration of the cGENIE Earth system model47. b, Surface ocean current field (black arrows) for the same circulation state as a overlaid on annual average sea surface temperature (SST) (colours). Scale for current vectors on the right, along with a truncated temperature scale to highlight the distribution of comparable temperature regimes. Red arrows illustrate inferred flow paths relevant to the position of ODP Site 1209 (marked by a star).
a–d, Left, δ13C bulk and stable isotopes as in Fig. 1a. Dark green, benthic32; light green, bulk. Downcore plots of ΣCV (a), Bray–Curtis dissimilarity (b), Simpson’s index (d; grey dashed lines; black line indicates the 150-kyr moving average) and the variance (in 150-kyr windows) in the Simpson’s index (c). Vertical grey lines in a and b show the level of background inferred from rank order plots of these data. All four metrics (ΣCV, Bray–Curtis dissimilarity, Simpson’s index and variance in the Simpson’s index) show a distinction of volatility between early Danian regime 1 (n = 137 data points) and regime 2 (the rest of the record, n = 861 data points). For example, the Wilcoxon rank-sum (W) value for the Simpson’s record was W = 46,646; P < 0.001 on first differences with 95% confidence limits of −0.013, −0.006. A W value of zero would support a null hypothesis. The test was two-sided. The Simpson’s index shows a diversity minimum in the earliest Danian and then a rapid increase and steady long-term trend towards more diverse, more even communities, but with high variability in the early Danian. This fluctuation in the Simpson’s index, as recorded by the variance of the record (c) shows similar patterns to Bray–Curtis dissimilarity and ΣCV with high variance in the early Danian before dropping down. The variance in the Simpson’s index also shows high background fluctuations and a sustained increase in amplitude of fluctuations around the isotope shift in the Palaeocene Carbon Isotope Maximum, reflecting oligotroph diversification, which the Simpson’s index shows strongly due to its higher sensitivity to rare taxa. In effect, metric sensitivity to the richness in taxa and rare taxa increased from a to c (from abundance variance to diversity variance). Note, the Simpson’s index can only be calculated on full assemblage data and therefore the record extends only from 66 to 55.5 Myr ago.
Extended Data Fig. 3 Relative abundance of key nannoplankton groups and abundance of reworked specimens per 100 nannofossils.
Relative abundance of coccoliths from all groups included in the ΣCV metric are shown, coloured according to clade (as in Fig. 1b) and ordered by stratigraphic appearance. Cretaceous survivor taxa were counted as individual species but have been grouped together here, comprising mostly Zeugrhabdotus with lower abundances of Cyclagelosphaera, Markalius and Neocrepidolithus.
Stratigraphic distribution of important species grouped as incoming (brown), survivor (green) or disappearing (blue) taxa. A subset of Cretaceous taxa is shown, with the latest Maastrichtian diversity for families shown alongside the number of survivors. Gradualistic evolutionary transitions indicated by close spacing and arrows indicate genus-level transitions. The nannoplankton data are primarily from our work but are largely consistent with published sources10,15,16,37,74. Diversity and cell-volume records are also shown in Fig. 3. Cp., Cruciplacolithus; Dan-C2, L C29n, hyperthermals; LDE, Late Danian Event; Neobisc., Neobiscutum; NP = nannofossil biozone; Prae., Praeprinsius.
Extended Data Fig. 5 Effects of window duration and depth or age sampling on ΣCV and Bray–Curtis dissimilarity.
a–c, Influence of different window duration (75–1,000 kyr) (a) and sampling in either the depth or age domain (c) on ΣCV, and effect of window duration on Bray–Curtis dissimilarity (b). c, Side-by-side results of ΣCV calculated using evenly spaced samples in either the depth domain or the age domain using a depth window duration of 60 cm, which is broadly equivalent to the 150-kyr time window. When ΣCV is plotted in the depth domain the main patterns are retained, indicating that no significant artefacts arise from the applied age model. The boundaries between the Myr sections, at which the taxa included in the ΣCV change (black dots), are marked on a. There are no obvious artefacts across the Myr windows with changes in the most abundant taxa.
a–c, Models range from a standard genus-level stratophenetic tree (a) through two successively conservative scenarios (b, c) grouping closely related taxa—that is, recently diverged taxa based on morphological and stratigraphic range data. Nannoplankton taxonomy is primarily based on the morphology and crystallographic ultrastructure of exoskeletal coccoliths but the addition of genetic data for modern taxa confirmed that this approach is robust75,76,77. Evolutionary models are stratophenetic, because we have high-quality stratigraphic information but lack the range of meaningful homologous morphological characters to allow a cladistic analysis. a, Genus-level phylogeny based on an extensive species-level stratophenetic tree. b, c, Different ancestry options used to test for artefacts and sensitivity in variance/dissimilarity that may result from equal weighting of closely related versus more-distantly related taxa. b, Ancestry model option 1 is highly conservative and merges major sub-family groups (shown by shaded boxes) around five nodes shown by black circles. c, Ancestry model option 2 merges the most-closely related genera (shaded boxes) around eight nodes.
a, b, Analyses of the influences of two additional models of shared ancestry (Extended Data Fig. 6a) on the ΣCV (a) and Bray–Curtis dissimilarity (b) datasets. In red, the original analysis in which each genus is weighted equally. In grey, analysis of the conservative ancestry model that merges genera into major sub-family groups (ancestry model option 1; Extended Data Fig. 6b). In black, analysis of the moderately conservative ancestry model (option 2; Extended Data Fig. 6c), which merges the most-closely related genera. The Bray–Curtis dissimilarity analysis shows very little sensitivity to variation in the taxonomic hierarchies. The ΣCV displays some sensitivity, particularly at the Late Danian Event (around 62 Myr ago); however, the main patterns are retained between the original and option 2. Some variance is lost in the less-realistic analysis of option 1, in which grouping of key genera that are found in the same families dampens the variance, in particular, in the early Danian. However, the values of early Danian variance still remain anomalously high compared to the rest of the record.
About this article
Cite this article
Alvarez, S.A., Gibbs, S.J., Bown, P.R. et al. Diversity decoupled from ecosystem function and resilience during mass extinction recovery. Nature 574, 242–245 (2019). https://doi.org/10.1038/s41586-019-1590-8