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No state change in pelagic fish production and biodiversity during the Eocene–Oligocene transition

Nature Geoscience volume 13, pages 238–242 (2020)Cite this article

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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.

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Fig. 1: A 34 Ma reconstruction palaeomap showing the sites included in this study.
Fig. 2: IARs from sites included in this study, arranged approximately from northernmost to southernmost latitude, show no significant trends across the E/O (light-blue horizontal line).
Fig. 3: Range charts from DSDP Site 596 (top) and ODP Site 689 (bottom) showing the occurrences of each of the 66 tooth morphotypes described in this study, ordered on the x axis by first occurrence within each site.

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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/.

Change history

References

  1. Liu, Z. et al. Global cooling during the Eocene-Oligocene climate transition. Science 323, 1187–1190 (2009).

    Article  Google Scholar 

  2. 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).

    Article  Google Scholar 

  3. 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).

    Article  Google Scholar 

  4. 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).

    Article  Google Scholar 

  5. Fischer, A. G. & Arthur, M. A. Secular variations in the pelagic realm. Soc. Econ. PA 25, 19–50 (1977).

    Google Scholar 

  6. 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).

    Article  Google Scholar 

  7. Berger, W. H. Cenozoic cooling, Antarctic nutrient pump, and the evolution of whales. Deep-Sea Res. Pt II 54, 2399–2421 (2007).

    Article  Google Scholar 

  8. 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).

    Article  Google Scholar 

  9. 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).

    Article  Google Scholar 

  10. 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).

    Article  Google Scholar 

  11. 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).

    Article  Google Scholar 

  12. 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).

    Article  Google Scholar 

  13. 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).

    Article  Google Scholar 

  14. 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).

    Google Scholar 

  15. 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).

    Article  Google Scholar 

  16. 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).

    Article  Google Scholar 

  17. 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).

    Article  Google Scholar 

  18. 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).

  19. 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).

  20. 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).

    Article  Google Scholar 

  21. 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).

    Article  Google Scholar 

  22. 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).

    Google Scholar 

  23. 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).

    Article  Google Scholar 

  24. 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).

    Article  Google Scholar 

  25. Houben, A. J. et al. Reorganization of Southern Ocean plankton ecosystem at the onset of Antarctic glaciation. Science 340, 341–344 (2013).

    Article  Google Scholar 

  26. 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).

    Article  Google Scholar 

  27. 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).

    Article  Google Scholar 

  28. 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).

    Article  Google Scholar 

  29. 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).

    Article  Google Scholar 

  30. 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).

    Article  Google Scholar 

  31. 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).

    Article  Google Scholar 

  32. 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).

    Article  Google Scholar 

  33. 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).

    Article  Google Scholar 

  34. 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).

    Article  Google Scholar 

  35. 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).

    Google Scholar 

  36. 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).

    Article  Google Scholar 

  37. Fordyce, R. E. & Marx, F. G. Gigantism precedes filter feeding in baleen whale evolution. Curr. Biol. 28, 1670–1676 (2018).

    Article  Google Scholar 

  38. Fordyce, R. E. & Jones, C. in Penguin Biology (eds Davis, L. S. & Darby, J. T.) 419–446 (Academic Press, 1990).

  39. Rogers, A. D. Evolution and biodiversity of Antarctic organisms: a molecular perspective. Phil. Trans. R. Soc. Lond. 362, 2191–2214 (2007).

    Article  Google Scholar 

  40. 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).

    Google Scholar 

  41. Near, T. J. et al. Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proc. Natl Acad. Sci. 109, 3434–3439 (2012).

    Article  Google Scholar 

  42. Polovina, J. J., Howell, E. A. & Abecassis, M. Ocean’s least productive waters are expanding. Geophys. Res. Lett. 35, L03618 (2008).

    Article  Google Scholar 

  43. 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).

    Article  Google Scholar 

  44. 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).

    Google Scholar 

  45. Hsu, K. J. et al. Site 522. Initial Rep. Deep Sea 73, 187–270 (1984).

    Google Scholar 

  46. Dadey, K. A., Janecek, T. & Klaus, A. Dry-bulk density: its use and determination. Proc. Ocean Drill. Prog. Sci. Results 126, 551–554 (1992).

    Google Scholar 

  47. 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).

    Google Scholar 

  48. Norris, R. D. et al. Site U1406. Proc. Integr. Ocean Drill. Program 342, https://doi.org/10.2204/iodp.proc.342.107.2014 (2014).

  49. Tauxe, L., Tucker, P., Petersen, N. P. & Labrecque, J. L. The magnetostratigraphy of Leg 73 sediments. Palaeogeogr. Palaeoclimatol. Palaeoecol. 42, 65–90 (1983).

    Article  Google Scholar 

  50. Gradstein, F. M., Ogg, J. G. & Schmitz, M. The Geologic Time Scale 2012 (Elsevier, 2012).

  51. 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).

    Article  Google Scholar 

  52. Iverson, R. L. Control of marine fish production. Limnol. Oceanogr. 35, 1593–1604 (1990).

    Article  Google Scholar 

  53. Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.4-4 (2017); https://CRAN.R-project.org/package=vegan

  54. 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).

    Article  Google Scholar 

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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.

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Authors and Affiliations

  1. Harvard Society of Fellows, Harvard University, Cambridge, MA, USA

    Elizabeth C. Sibert

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

    Elizabeth C. Sibert & Ella T. Frigyik

  3. Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, USA

    Elizabeth C. Sibert, Michelle E. Zill & Richard D. Norris

  4. Department of Earth and Planetary Sciences, University of California Riverside, Riverside, CA, USA

    Michelle E. Zill

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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.

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Correspondence to Elizabeth C. Sibert.

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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.

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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

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