Abstract
The Eocene/Oligocene (E/O) boundary (~33.9 million years ago) has been described as a state change in the Earth system marked by the permanent glaciation of Antarctica and a proposed increase in oceanic productivity. Here we quantified the response of fish production and biodiversity to this event using microfossil fish teeth (ichthyoliths) in seven deep-sea sediment cores from around the world. Ichthyolith accumulation rate (a proxy for fish biomass production) shows no synchronous trends across the E/O. Ichthyolith accumulation in the Southern Ocean and Pacific gyre sites is an order of magnitude lower than that in the equatorial and Atlantic sites, demonstrating that the Southern Ocean was not a highly productive ecosystem for fish before or after the E/O. Further, tooth morphotype diversity and assemblage composition remained stable across the interval, indicating little change in the biodiversity or ecological role of open-ocean fish. While the E/O boundary was a major global climate-change event, its impact on pelagic fish was relatively muted. Our results support recent findings of whale and krill diversification suggesting that the pelagic ecosystem restructuring commonly attributed to the E/O transition probably occurred much later, in the late Oligocene or Miocene.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Enhanced fish production during a period of extreme global warmth
Nature Communications Open Access 06 November 2020
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 per month
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Rent or buy this article
Get just this article for as long as you need it
$39.95
Prices may be subject to local taxes which are calculated during checkout



Data availability
The ichthyolith accumulation data generated in this study, along with all age model and accumulation rate calculations, are available in Supplementary Tables 1–20, and on the Pangaea Database at https://doi.org/10.1594/PANGAEA.910379. We have also included an appendix with photographs of all tooth morphotypes identified in this study, and high-resolution digital images of each microfossil are available via Dryad at https://doi.org/10.5061/dryad.nk98sf7q5.
Code availability
All code used in this study is available at https://github.com/esibert/EO_Fish/.
References
Liu, Z. et al. Global cooling during the Eocene-Oligocene climate transition. Science 323, 1187–1190 (2009).
Diester-Haass, L. & Zahn, R. Paleoproductivity increase at the Eocene-Oligocene climatic transition; ODP/DSDP sites 763 and 592. Palaeogeogr. Palaeoclimatol. Palaeoecol. 172, 153–170 (2001).
Wade, B. S. et al. Multiproxy record of abrupt sea-surface cooling across the Eocene-Oligocene transition in the Gulf of Mexico. Geology 40, 159–162 (2012).
Zachos, J., Pagani, M., Sloan, L., Thomas, E. & Billups, K. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693 (2001).
Fischer, A. G. & Arthur, M. A. Secular variations in the pelagic realm. Soc. Econ. PA 25, 19–50 (1977).
Robert, C. & Kennett, J. P. Antarctic continental weathering changes during Eocene-Oligocene cryosphere expansion: clay mineral and oxygen isotope evidence. Geology 25, 587–590 (1997).
Berger, W. H. Cenozoic cooling, Antarctic nutrient pump, and the evolution of whales. Deep-Sea Res. Pt II 54, 2399–2421 (2007).
Coxall, H. K. & Wilson, P. A. Early Oligocene glaciation and productivity in the eastern equatorial Pacific: insights into global carbon cycling. Paleoceanography 26, PA2221 (2011).
Egan, K. E., Rickaby, R. E. M., Hendry, K. R. & Halliday, A. N. Opening the gateways for diatoms primes Earth for Antarctic glaciation. Earth Planet Sci. Lett. 375, 34–43 (2013).
Moloney, C. L. & Field, J. G. The size-based dynamics of plankton food webs. I. A simulation model of carbon and nitrogen flows. J. Plankton Res. 13, 1003–1038 (1991).
Moloney, C. L., Field, J. G. & Lucas, M. I. The size-based dynamics of plankton food webs. II. Simulations of three contrasting southern Benguela food webs. J. Plankton Res. 13, 1039–1092 (1991).
Pyenson, N. D. & Vermeij, G. J. The rise of ocean giants: maximum body size in Cenozoic marine mammals as an indicator for productivity in the Pacific and Atlantic oceans. Biol. Lett. 12, 20160186 (2016).
Pyenson, N. D., Kelley, N. P. & Parham, J. F. Marine tetrapod macroevolution: physical and biological drivers on 250 Ma of invasions and evolution in ocean ecosystems. Palaeogeogr. Palaeoclimatol. Palaeoecol. 400, 1–8 (2014).
Fitzgerald Erich, M. G. A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales. Proc. R. Soc. Lond. B 273, 2955–2963 (2006).
Zachos, J. C., Quinn, T. M. & Salamy, K. A. High-resolution (104 years) deep-sea foraminiferal stable isotope records of the Eocene–Oligocene climate transition. Paleoceanography 11, 251–266 (1996).
Zhou, L. & Kyte, F. T. Sedimentation history of the South Pacific pelagic clay province over the last 85 million years inferred from the geochemistry of deep sea drilling project Hole 596. Paleoceanography 7, 441–465 (1992).
Mackensen, A. & Ehrmann, W. U. Middle Eocene through early Oligocene climate history and paleoceanography in the Southern Ocean: stable oxygen and carbon isotopes from ODP sites on Maud Rise and Kerguelen Plateau. Mar. Geol. 108, 1–27 (1992).
Lyle, M. W. et al. Site 1217. Proc. Ocean Drill. Prog. Init. Repts 199, https://doi.org/10.2973/odp.proc.ir.199.110.2002 (2002).
van Peer, T. E. et al. Data report: revised composite depth scale and splice for IODP Site U1406. Proc. Integr. Ocean Drill. Program 342, https://doi.org/10.2204/iodp.proc.342.202.2017 (2017).
Sibert, E. C., Hull, P. M. & Norris, R. D. Resilience of Pacific pelagic fish across the Cretaceous/Palaeogene mass extinction. Nat. Geosci. 7, 667–670 (2014).
Salamy, K. A. & Zachos, J. C. Latest Eocene–early oligocene climate change and Southern Ocean fertility: inferences from sediment accumulation and stable isotope data. Palaeogeogr. Palaeoclimatol. Palaeoecol. 145, 61–77 (1999).
Anderson, L. D. & Delaney, M. L. Middle Eocene to early Oligocene paleoceanography from Agulhas Ridge, Southern Ocean (Ocean Drilling Program Leg 177, Site 1090). Paleoceanography 20, PA1013 (2005).
Erhardt, A. M., Pälike, H. & Paytan, A. High-resolution record of export production in the eastern equatorial Pacific across the Eocene-Oligocene transition and relationships to global climatic records. Paleoceanography 28, 130–142 (2013).
Griffith, E. et al. Export productivity and carbonate accumulation in the Pacific Basin at the transition from a greenhouse to icehouse climate (late Eocene to early Oligocene). Paleoceanography 25, PA3212 (2010).
Houben, A. J. et al. Reorganization of Southern Ocean plankton ecosystem at the onset of Antarctic glaciation. Science 340, 341–344 (2013).
Faul, K. L. & Delaney, M. L. A comparison of early Paleogene export productivity and organic carbon burial flux for Maud Rise, Weddell Sea, and Kerguelen Plateau, South Indian Ocean. Paleoceanography 25, PA3214 (2010).
Sarmiento, J. L., Gruber, N., Brzezinski, M. A. & Dunne, J. P. High-latitude controls of thermocline nutrients and low latitude biological productivity. Nature 427, 56–60 (2004).
Cermeno, P., Falkowski, P. G., Romero, O. E., Schaller, M. F. & Vallina, S. M. Continental erosion and the Cenozoic rise of marine diatoms. Proc. Natl Acad. Sci. USA 112, 4239–4244 (2015).
Villa, G., Fioroni, C., Persico, D., Roberts, A. P. & Florindo, F. Middle Eocene to late Oligocene Antarctic glaciation/deglaciation and Southern Ocean productivity. Paleoceanography 29, 223–237 (2014).
Pepin, P. Effect of temperature and size on development, mortality, and survival rates of the pelagic early life history stages of marine fish. Can. J. Fish. Aquat.Sci. 48, 503–518 (1991).
Barrera-Oro, E. The role of fish in the Antarctic marine food web: differences between inshore and offshore waters in the southern Scotia Arc and West Antarctic Peninsula. Antarct. Sci. 14, 293–309 (2003).
Patarnello, T., Bargelloni, L., Varotto, V. & Battaglia, B. Krill evolution and the Antarctic Ocean currents: evidence of vicariant speciation as inferred by molecular data. Mar. Biol. 126, 603–608 (1996).
Jarman, S. N., Elliott, N. G., Nicol, S. & McMinn, A. Molecular phylogenetics of circumglobal Euphausia species (Euphausiacea: Crustacea). Can. J. Fish. Aquat.Sci. 57, 51–58 (2000).
D’Amato, M. E., Harkins, G. W., de Oliveira, T., Teske, P. R. & Gibbons, M. J. Molecular dating and biogeography of the neritic krill Nyctiphanes. Mar. Biol. 155, 243–247 (2008).
Sibert, E., Friedman, M., Hull, P., Hunt, G. & Norris, R. Two pulses of morphological diversification in Pacific pelagic fishes following the Cretaceous–Palaeogene mass extinction. Proc. R. Soc. Lond. B 285, 20181194 (2018).
Clementz, M. T., Fordyce, R. E., Peek, S. L. & Fox, D. L. Ancient marine isoscapes and isotopic evidence of bulk-feeding by Oligocene cetaceans. Palaeogeogr. Palaeoclimatol. Palaeoecol. 400, 28–40 (2014).
Fordyce, R. E. & Marx, F. G. Gigantism precedes filter feeding in baleen whale evolution. Curr. Biol. 28, 1670–1676 (2018).
Fordyce, R. E. & Jones, C. in Penguin Biology (eds Davis, L. S. & Darby, J. T.) 419–446 (Academic Press, 1990).
Rogers, A. D. Evolution and biodiversity of Antarctic organisms: a molecular perspective. Phil. Trans. R. Soc. Lond. 362, 2191–2214 (2007).
Baker, A. J., Pereira, S. L., Haddrath, O. P. & Edge, K.-A. Multiple gene evidence for expansion of extant penguins out of Antarctica due to global cooling. Proc. R. Soc. Lond. B 273, 11–17 (2006).
Near, T. J. et al. Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proc. Natl Acad. Sci. 109, 3434–3439 (2012).
Polovina, J. J., Howell, E. A. & Abecassis, M. Ocean’s least productive waters are expanding. Geophys. Res. Lett. 35, L03618 (2008).
Cramer, B. S., Miller, K. G., Barrett, P. J. & Wright, J. D. Late Cretaceous–Neogene trends in deep ocean temperature and continental ice volume: reconciling records of benthic foraminiferal geochemistry (δ18O and Mg/Ca) with sea level history. J. Geophys. Res. Oceans 116, C12023 (2011).
Sibert, E. C., Cramer, K. L., Hastings, P. A. & Norris, R. D. Methods for isolation and quantification of microfossil fish teeth and elasmobranch dermal denticles (ichthyoliths) from marine sediments. Palaeontol. Electron. 20, 1–14 (2017).
Hsu, K. J. et al. Site 522. Initial Rep. Deep Sea 73, 187–270 (1984).
Dadey, K. A., Janecek, T. & Klaus, A. Dry-bulk density: its use and determination. Proc. Ocean Drill. Prog. Sci. Results 126, 551–554 (1992).
Snoeckx, H., Rea, D., Jones, C. & Ingram, B. Eolian and silica deposition in the central North Pacific: results from Sites 885/886. Proc. Ocean Drill. Prog. Sci. Results 145, 219–230 (1995).
Norris, R. D. et al. Site U1406. Proc. Integr. Ocean Drill. Program 342, https://doi.org/10.2204/iodp.proc.342.107.2014 (2014).
Tauxe, L., Tucker, P., Petersen, N. P. & Labrecque, J. L. The magnetostratigraphy of Leg 73 sediments. Palaeogeogr. Palaeoclimatol. Palaeoecol. 42, 65–90 (1983).
Gradstein, F. M., Ogg, J. G. & Schmitz, M. The Geologic Time Scale 2012 (Elsevier, 2012).
Hsiang, A. Y. et al. AutoMorph: Accelerating morphometrics with automated 2D and 3D image processing and shape extraction. Methods Ecol. Evol. 9, 605–612 (2018).
Iverson, R. L. Control of marine fish production. Limnol. Oceanogr. 35, 1593–1604 (1990).
Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.4-4 (2017); https://CRAN.R-project.org/package=vegan
Liow, L. H. & Nichols, J. D. Estimating rates and probabilities of origination and extinction using taxonomic occurrence data: capture–mark–recapture (CMR) approaches. Paleontol. Soc. Papers 16, 81–94 (2010).
Acknowledgements
The authors thank the International Ocean Discovery Program (IODP) for providing samples. This work was supported by the Scripps Institution of Oceanography Graduate Division, the Harvard Society of Fellows, the Digital Imaging Facility at the Museum of Comparative Zoology at Harvard University and a William F. Milton Grant to E. Sibert.
Author information
Authors and Affiliations
Contributions
E.C.S. and R.D.N. conceived the study, which was initiated by M.E.Z. for her MS degree in the lab of R.D.N. M.E.Z. processed the ichthyolith samples for all sites, compiled the productivity datasets and calculated IAR with input from E.C.S. Teeth were imaged by E.C.S., and the individual teeth were classified by E.T.F. with input from E.C.S. E.C.S. and R.D.N. wrote the initial draft of the manuscript, and all authors contributed to the final version of the paper.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Peer review information Primary Handling Editor: James Super.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data
Extended Data Fig. 1 A compilation of palaeoproductivity proxies (barium in brown and silica in blue-green), compared to the ichthyolith accumulation rates produced in this study.
All data were re-converted from the reported raw concentration values of the original studies to mass accumulation rates, based on GTS2012 age models50 and shipboard-reported dry bulk density. Barium and silica data from ODP Site 1217 was reported by the shipboard scientific party and downloaded from the JANUS Database18. Barium and silica data for DSDP Site 596 was reported in Zhou and Kyte (1992)16. Barium and silica Data for ODP Site 689 was reported in Faul and Delaney (2010)26. ODP Site 748 has no reported silica or barium data. Nearby ODP Site 744 silica data was reported by Salamy and Zachos (1999)21. Please see the supplemental data tables for additional details on the reported productivity proxy values.
Extended Data Fig. 2 A comparison of sediment mass accumulation rate (gray) with the raw concentration values for ichthyoliths per gram (black), barium concentration (parts per million) and opal abundance (% silica) for ODP Site 1217.
The Yellow box highlights a two-million year period of elevated sediment MAR that is associated with an increase in the concentration of ichthyoliths and barium but not silica.
Extended Data Fig. 3 Rarefaction curves for DSDP Site 596 and ODP Site 689.
Both sites are underestimating total morphotype diversity, as range-through diversity is not accounted for in this analysis, though it is clear that the two oldest samples (>40 Ma) in ODP Site 689 have lower rarefied diversity than the younger samples, despite having much higher total numbers of ichthyoliths. Further, DSDP Site 596 has overall higher rarefied diversity estimated at each sample size, showing that the South Pacific Gyre had a higher species richness overall than the Antarctic during this study interval. There is no systematic shift in total richness across the E/O at either site.
Extended Data Fig. 4 Capture-mark-recapture analysis output showing constant rates of origination (blue) and extinction (red) throughout the study interval for DSDP Site 596 and ODP Site 689.
Note that at both locations, origination slightly outpaces extinction, revealing an overall trend towards increasing species richness during the Late Eocene and Early Oligocene.
Extended Data Fig. 5 Various diversity metrics from DSDP Site 596 and ODP Site 689 showing little change in sampled tooth morphotype diversity across the E/O.
Note that calculation of rarefied richness allows for a maximum resample size of the smallest sample in the dataset, so the richness estimates for ODP Site 689 are lower than they may otherwise be due to the small sample size. Rarefaction curves for both sites are seen in Extended Data Fig. 3.
Supplementary information
Supplementary Information
Type catalogue for all tooth morphotypes considered in this study.
Supplementary Tables 1–20
All raw data used to construct the figures in the manuscript, including ichthyolith metrics generated in this study, as well as age models updated to GTS 2012, barium accumulation and silica accumulation. Each tab includes one supplementary table.
Rights and permissions
About this article
Cite this article
Sibert, E.C., Zill, M.E., Frigyik, E.T. et al. No state change in pelagic fish production and biodiversity during the Eocene–Oligocene transition. Nat. Geosci. 13, 238–242 (2020). https://doi.org/10.1038/s41561-020-0540-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41561-020-0540-2
This article is cited by
-
Enhanced fish production during a period of extreme global warmth
Nature Communications (2020)