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Cyclic evolution of phytoplankton forced by changes in tropical seasonality

Nature volume 601, pages 79–84 (2022)Cite this article

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Abstract

Although the role of Earth’s orbital variations in driving global climate cycles has long been recognized, their effect on evolution is hitherto unknown. The fossil remains of coccolithophores, a key calcifying phytoplankton group, enable a detailed assessment of the effect of cyclic orbital-scale climate changes on evolution because of their abundance in marine sediments and the preservation of their morphological adaptation to the changing environment1,2. Evolutionary genetic analyses have linked broad changes in Pleistocene fossil coccolith morphology to species radiation events3. Here, using high-resolution coccolith data, we show that during the last 2.8 million years the morphological evolution of coccolithophores was forced by Earth’s orbital eccentricity with rhythms of around 100,000 years and 405,000 years—a distinct spectral signature to that of coeval global climate cycles4. Simulations with an Earth System Model5 coupled with an ocean biogeochemical model6 show a strong eccentricity modulation of the seasonal cycle, which we suggest directly affects the diversity of ecological niches that occur over the annual cycle in the tropical ocean. Reduced seasonality in surface ocean conditions favours species with mid-size coccoliths, increasing coccolith carbonate export and burial; whereas enhanced seasonality favours a larger range of coccolith sizes and reduced carbonate export. We posit that eccentricity pacing of phytoplankton evolution contributed to the strong 405,000-year cyclicity that is seen in global carbon cycle records.

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Fig. 1: Noelaerhabdaceae coccolith morphology and accumulation, eccentricity, and climate over the last 2.8 million years.
Fig. 2: MDI concept.
Fig. 3: Modelled NPP seasonal contrast under different eccentricity configurations and MDI.

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Data availability

All coccolith morphological data, as well as all model outputs described in the paper (including NPP and main oceanic and atmospheric variables) are archived at the SEANOE open access data repository: https://doi.org/10.17882/84031. LMDZ, XIOS, NEMO and ORCHIDEE are released under the terms of the CeCILL license. OASIS-MCT is released under the terms of the Lesser GNU General Public License (LGPL). IPSL-CM5A2 source code is publicly available through svn, with the following commands line : svn co http://forge.ipsl.jussieu.fr/igcmg/svn/modipsl/branches/publications/IPSLCM5A2.1_11192019 modipsl ; cd modipsl/util ; ./model IPSLCM5A2.1. The mod.def file provides information regarding the different revisions used, namely: NEMOGCM branch nemo_v3_6_STABLE revision 6665; XIOS2 branchs/xios-2.5 revision 1763; IOIPSL/src svn tags/v2_2_2; LMDZ5 branches/IPSLCM5A2.1 rev 3591; branches/publications/ORCHIDEE_IPSLCM5A2.1.r5307 rev 6336; and OASIS3-MCT 2.0_branch (rev 4775 IPSL server). The login/password combination requested at first use to download the ORCHIDEE component is anonymous/anonymous. We recommend that you refer to the project website: http://forge.ipsl.jussieu.fr/igcmg_doc/wiki/Doc/Config/IPSLCM5A2 for a proper installation and compilation of the environment.

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Acknowledgements

This paper is a contribution of the Climate research group at CEREGE. This research uses samples provided by the IODP. We thank the scientists, technical staff and crews of IODP expeditions 353 and 363 and IMAGES expeditions 3 and 13; A. Fruy and S. Sergi for sample preparation assistance; and the CEA–CCRT for providing access to the HPC resources of TGCC under the allocation 2019-A0070102212 made by GENCI. We acknowledge French ANR projects CALHIS (L.B.), iMonsoon (C.T.B.) and AMOR (Y.D.), and INSU project CALVE (C.T.B.) and FRB project COCCACE (L.B.) , which provided funding for this work. IODP France provided post-cruise funding to L.B. and C.T.B.

Author information

Author notes

  1. Nicolas Barbarin

    Present address: TOTAL S.A., Pau, France

  2. Samantha Bova

    Present address: Department of Geological Sciences, San Diego State University, San Diego, CA, USA

  3. Pauline Cornuault

    Present address: MARUM, Universität Bremen, Bremen, Germany

  4. Emmeline Gray

    Present address: The Open University, Milton Keynes, UK

Authors and Affiliations

  1. Aix-Marseille University, CNRS, IRD, INRAE, CEREGE, Aix-en-Provence, France

    Luc Beaufort, Clara T. Bolton, Anta-Clarisse Sarr, Baptiste Suchéras-Marx, Yannick Donnadieu, Nicolas Barbarin, Pauline Cornuault, Yves Gally, Emmeline Gray, Jean-Charles Mazur & Martin Tetard

  2. Department of Marine and Coastal Sciences, and Earth and Planetary Sciences, Rutgers, State University of New Jersey, New Brunswick, NJ, USA

    Yair Rosenthal & Samantha Bova

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Contributions

L.B. designed the study. L.B., Y.G., N.B. and M.T. developed automated artificial intelligence methods. L.B., C.T.B., J.-C.M., P.C., E.G. and S.B. prepared samples and/or generated data. A.-C.S. designed and ran the model simulations, in collaboration with Y.D. L.B. and C.T.B. analysed the morphometric data. L.B., C.T.B., A.-C.S., B.S.-M., Y.D. and Y.R. discussed interpretations. L.B., C.T.B. and A.-C.S. wrote the manuscript with contributions from B.S.-M., Y.D. and Y.R.

Corresponding authors

Correspondence to Luc Beaufort or Clara T. Bolton.

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Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature thanks Claudia Agnini, Ying Guan, Rosalind Rickaby, Andy Ridgwell and Thomas Westerhold for their contribution to the peer review of this work. Peer reviewer reports are available.

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 Fig. 1 Size and MDI records for each core.

Top panels a to i: Size frequency plots for each individual core used to create the composite record shown in Fig. 1a. Bottom panels a to i: Individual MDI records for each core (black lines and points) plotted with the stacked MDI record (red line). Pearson correlation coefficients between individual sites and the stack vary between 0.71 and 0.93 (P values are all <0.00001).

Extended Data Fig. 2 Time-series analyses of individual records.

a, b, Blackman Tukey cross-spectral analysis between eccentricity and stacked coccolith length (a) and eccentricity and stacked MDI (b). Top: coherency; Bottom: phase (radian). c–k, MTM and evolutive spectral analyses (see Methods) of detrended individual MDI series resampled at 2-kyr intervals (shown on left of each evolutive analysis). Primary orbital periods are shown by red lines.

Extended Data Fig. 3 Decomposition of the Noelaerhabdaceae mass accumulation rate (NoMAR) record into its mass and flux components.

a, Stacked NoMAR record, binned into 2-ky intervals (orange shading) and smoothed with a 30-kyr moving window (orange line), b, Noelaerhabdaceae coccolith flux (blue) and average Noelaerhabdaceae coccolith mass (red). Here, stacked mass and flux records are smoothed with a 30-kyr moving window as in a. c, NoMAR (orange) and MDI (purple) records, smoothed with a 30-kyr moving window. Grey shaded areas represent four described acmes of mid-size Noelaerhabdaceae species19,20,21,82,83.

Extended Data Fig. 4 Ocean–atmosphere model outputs under different orbital configurations.

Top: Yearly maximum contrast in NPP (gC m−2 day−1) for a: EminPmin, b: EmaxPmin and c: EmaxPmax. Low eccentricity values minimize the amplitude of precession variability, thus we only show results for minimum precession value at minimum eccentricity (EminPmin) but the reader can consider those results to be similar for the EminPmax simulation. d and e represent the anomaly of yearly maximum contrast in NPP. At EmaxPmax, the eastern equatorial Indian Ocean exhibits moderate seasonality (a) due to inhibition of the summer productivity induced by lower nutrient concentrations in this area (Extended Data Fig. 6a). In this case, high productivity areas during boreal summer are shifted to south-west of India. Bottom: Late summer (JASO) low-level winds for f: EminPmin, g: EmaxPmin, h: EmaxPmax simulations. i and j represent the anomaly in late summer low-level winds. At EmaxPmax the north-equatorial westerlies (c, e) are confined to south of 10° N owing to the extension above India of the low-pressure area.

Extended Data Fig. 5 Solar radiation and sea-level pressure in model simulations.

Seasonal latitudinal variations of solar radiation at the top of the atmosphere derived from the model (W.m−2); a: EminPmin, b: EmaxPmin, c: EmaxPmax. See Extended Data Table 3 for details of orbital configurations of each simulation. Late summer (JASO) low-level winds for d: EminPmin, e: EmaxPmin, f: EmaxPmax simulations and anomaly in late summer low-level winds, g: EmaxPmin minus EminPmin, h: EmaxPmax minus EminPmax.

Extended Data Fig. 6 Nutrients, temperature and upwelling in model simulations.

a, NO3 concentrations in the surface layer (0-100m). b, Upwelling velocity (averaged between 40 and 80m), c: Sea Surface Temperature (SST). All variables are averaged over JASO. Left: Emin, Middle: EmaxPmin minus EminPmin, Right: EmaxPmax minus EminPmax.

Extended Data Fig. 7 Explanation of non-linearities in coccolithophore evolution.

a, Low-pass filter design for the delay between first appearance datum (FAD) and the beginning of the acme (BA) for E. huxleyi (blue line, lag of two eccentricity cycles) and another possible scenario for another species (red line, lag of one eccentricity cycle). The stepped green line represents E. huxleyi’s existence (0 = absence, 1 = presence). The blue and red curves in all panels are the output series of the 2 low-pass filters described in the Methods. The black curve in a represents coeval eccentricity values. b, c, Bode plots of the 1-cycle lag filter (red) and the 2-cycle lag filter (blue) for magnitude (b) and phase (c) (see Methods). Earth’s primary orbital periods are indicated by shading.

Extended Data Table 1 Characteristics of the nine marine records used in this study
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Extended Data Table 2 Relative calcium carbonate mass contribution per calcareous nannofossil taxon or group for each sediment core
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Extended Data Table 3 Summary of orbital parameters23 used for each simulation and mean yearly contrast of radiation at equator (Wm−2) derived from IPSL-CM5A2
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Beaufort, L., Bolton, C.T., Sarr, AC. et al. Cyclic evolution of phytoplankton forced by changes in tropical seasonality. Nature 601, 79–84 (2022). https://doi.org/10.1038/s41586-021-04195-7

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