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.

The Pliocene marine megafauna extinction and its impact on functional diversity

Abstract

The end of the Pliocene marked the beginning of a period of great climatic variability and sea-level oscillations. Here, based on a new analysis of the fossil record, we identify a previously unrecognized extinction event among marine megafauna (mammals, seabirds, turtles and sharks) during this time, with extinction rates three times higher than in the rest of the Cenozoic, and with 36% of Pliocene genera failing to survive into the Pleistocene. To gauge the potential consequences of this event for ecosystem functioning, we evaluate its impacts on functional diversity, focusing on the 86% of the megafauna genera that are associated with coastal habitats. Seven (14%) coastal functional entities (unique trait combinations) disappeared, along with 17% of functional richness (volume of the functional space). The origination of new genera during the Pleistocene created new functional entities and contributed to a functional shift of 21%, but minimally compensated for the functional space lost. Reconstructions show that from the late Pliocene onwards, the global area of the neritic zone significantly diminished and exhibited amplified fluctuations. We hypothesize that the abrupt loss of productive coastal habitats, potentially acting alongside oceanographic alterations, was a key extinction driver. The importance of area loss is supported by model analyses showing that animals with high energy requirements (homeotherms) were more susceptible to extinction. The extinction event we uncover here demonstrates that marine megafauna were more vulnerable to global environmental changes in the recent geological past than previously thought.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Elevated extinction rates of marine megafauna in the late Pliocene.
Figure 2: Changes in coastal marine megafauna functional diversity from the Pliocene (pre-extinction) to the Pleistocene (post-extinction).
Figure 3: Reduction of neritic areas as a putative extinction driver.
Figure 4: Thermoregulation explains the susceptibility of genera to the Pliocene megafauna extinction.

References

  1. 1.

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

    Article  PubMed  Google Scholar 

  2. 2.

    McCauley, D. J. et al. Marine defaunation: animal loss in the global ocean. Science 347, 1255641 (2015).

    Article  PubMed  Google Scholar 

  3. 3.

    Harnik, P. G. et al. Extinctions in ancient and modern seas. Trends Ecol. Evol. 27, 608–617 (2012).

    Article  PubMed  Google Scholar 

  4. 4.

    Miller, K. G. et al. The phanerozoic record of global sea-level change. Science 310, 1293–1298 (2005).

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    De Boer, B., van de Wal, R. S. W., Bintanja, R., Lourens, L. J. & Tuenter, E. Cenozoic global ice-volume and temperature simulations with 1-D ice-sheet models forced by benthic delta O-18 records. Ann. Glaciol. 51, 23–33 (2010).

    Article  Google Scholar 

  6. 6.

    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).

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Lisiecki, L. E. & Raymo, M. E. Plio–Pleistocene climate evolution: trends and transitions in glacial cycle dynamics. Quat. Sci. Rev 26, 56–69 (2007).

    Article  Google Scholar 

  8. 8.

    Van Woesik, R. et al. Hosts of the plio-pleistocene past reflect modern-day coral vulnerability. Proc. R. Soc. Lond. B Biol. Sci. 279, 2448–2456 (2012).

    Article  Google Scholar 

  9. 9.

    Valentine, J. W. & Jablonski, D. Biotic effects of sea-level change: the pleistocene test. J. Geophys. Res. Solid Earth 96, 6873–6878 (1991).

    Article  Google Scholar 

  10. 10.

    Lewison, R. L., Crowder, L. B., Read, A. J. & Freeman, S. A. Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol. Evol. 19, 598–604 (2004).

    Article  Google Scholar 

  11. 11.

    McClain, C. R. et al. Sizing ocean giants: patterns of intraspecific size variation in marine megafauna. PeerJ 3, e715 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Marx, F. G. & Uhen, M. D. Climate, critters, and cetaceans: Cenozoic drivers of the evolution of modern whales. Science 327, 993–996 (2010).

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Pyenson, N. D. & Sponberg, S. N. Reconstructing body size in extinct crown Cetacea (Neoceti) using allometry, phylogenetic methods and tests from the fossil record. J. Mamm. Evol. 18, 269–288 (2011).

    Article  Google Scholar 

  14. 14.

    Uhen, M. D. & Pyenson, N. D. Diversity estimates, biases, and historiographic effects: resolving cetacean diversity in the tertiary. Palaeontol. Electronica 10, 1–22 (2007).

    Google Scholar 

  15. 15.

    Boessenecker, R. W. Pleistocene survival of an archaic dwarf baleen whale (Mysticeti: Cetotheriidae). Naturwissenschaften 100, 365–71 (2013).

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Ando, T. & Fordyce, R. E. Evolutionary drivers for flightless, wing-propelled divers in the Northern and Southern hemispheres. Palaeogeogr. Palaeoclimatol. Palaeoecol. 400, 50–61 (2014).

    Article  Google Scholar 

  17. 17.

    Olson, S. L. An early pliocene marine avifauna from Duinefontein Cape Province South Africa. Ann. S. Afr. Mus. 95, 147–164 (1985).

    Google Scholar 

  18. 18.

    Sorbi, S., Domning, D. P., Vaiani, S. C. & Bianucci, G. Metaxytherium subapenninum (Bruno, 1839) (Mammalia, Dugongidae), the latest sirenian of the mediterranean basin. J. Vert. Paleontol. 32, 686–707 (2012).

    Article  Google Scholar 

  19. 19.

    Velez-Juarbe, J., Domning, D. P. & Pyenson, N. D. Iterative evolution of sympatric seacow (Dugongidae, Sirenia) assemblages during the past similar to 26 million years. PloS ONE 7, e31294 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Domning, D. P. Sirenians, seagrasses, and Cenozoic ecological change in the Caribbean. Palaeogeogr. Palaeoclimatol. Palaeoecol. 166, 27–50 (2001).

    Article  Google Scholar 

  21. 21.

    Pimiento, C. & Balk, M. A. Body-size trends of the extinct giant shark Carcharocles megalodon: a deep-time perspective on marine apex predators. Paleobiology 41, 479–490 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Pimiento, C. & Clements, C. F. When did Carcharocles megalodon become extinct? A new analysis of the fossil record. PloS ONE 9, e111086 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Dodd, C. K. & Morgan, G. S. Fossil sea-turtles from the early Pliocene Bone Valley Formation, Central Florida. J. Herpetol. 26, 1–8 (1992).

    Article  Google Scholar 

  24. 24.

    Leonard-Pingel, J. S., Jackson, J. B. C. & O’Dea, A. Changes in bivalve functional and assemblage ecology in response to environmental change in the Caribbean Neogene. Paleobiology 38, 509–524 (2012).

    Article  Google Scholar 

  25. 25.

    Estes, J. A. et al. Trophic downgrading of planet Earth. Science 333, 301–306 (2011).

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Doughty, C. E. et al. Global nutrient transport in a world of giants. Proc. Natl Acad. Sci. USA 113, 868–873 (2016).

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Malhi, Y. et al. Megafauna and ecosystem function from the Pleistocene to the Anthropocene. Proc. Natl Acad. Sci. USA 113, 838–846 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Boessenecker, R. W. A new marine vertebrate assemblage from the Late Neogene Purisima Formation in Central California, part II: pinnipeds and cetaceans. Geodiversitas 35, 815–940 (2012).

    Article  Google Scholar 

  29. 29.

    Villeger, S., Novack-Gottshall, P. M. & Mouillot, D. The multidimensionality of the niche reveals functional diversity changes in benthic marine biotas across geological time. Ecol. Lett. 14, 561–568 (2011).

    Article  PubMed  Google Scholar 

  30. 30.

    Raup, D. M. & Sepkoski, J. J. Jr Mass extinctions in the marine fossil record. Science 215, 1501–1503 (1982).

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Bambach, R. K., Bush, A. M. & Erwin, D. H. Autecology and the filling of ecospace: key metazoan radiations. Palaeontology 50, 1–22 (2007).

    Article  Google Scholar 

  32. 32.

    Mouillot, D., Graham, N. A. J., Villeger, S., Mason, N. W. H. & Bellwood, D. R. A functional approach reveals community responses to disturbances. Trends Ecol. Evol. 28, 167–177 (2013).

    Article  PubMed  Google Scholar 

  33. 33.

    Aberhan, M. & Kiessling, W. Persistent ecological shifts in marine molluscan assemblages across the end-Cretaceous mass extinction. Proc. Natl Acad. Sci. USA 112, 7207–7212 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Foster, W. J. & Twitchett, R. J. Functional diversity of marine ecosystems after the Late Permian mass extinction event. Nat. Geosci. 7, 233–238 (2014).

    CAS  Article  Google Scholar 

  35. 35.

    Dineen, A. A., Fraiser, M. L. & Sheehan, P. M. Quantifying functional diversity in pre- and post-extinction paleocommunities: a test of ecological restructuring after the end-Permian mass extinction. Earth Sci. Rev. 136, 339–349 (2014).

    Article  Google Scholar 

  36. 36.

    Duffy, J. E., Lefcheck, J. S., Stuart-Smith, R. D., Navarrete, S. A. & Edgar, G. J. Biodiversity enhances reef fish biomass and resistance to climate change. Proc. Natl Acad. Sci. USA 113, 6230–6235 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Dick, D. G. & Maxwell, E. E. The evolution and extinction of the ichthyosaurs from the perspective of quantitative ecospace modelling. Biol. Lett. 11, 20150339 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Lawton, J. H. What do species do in ecosystems. Oikos 71, 367–374 (1994).

    Article  Google Scholar 

  39. 39.

    Altieri, A. H. et al. Tropical dead zones and mass mortalities on coral reefs. Proc. Natl Acad. Sci. USA 114, 3660–3665 (2017).

    Google Scholar 

  40. 40.

    Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Wernberg, T. et al. Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169–172 (2016).

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Silvestro, D., Schnitzler, J., Liow, L. H., Antonelli, A. & Salamin, N. Bayesian estimation of speciation and extinction from incomplete fossil occurrence data. Syst. Biol. 63, 349–367 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Villafaña, J. A. & Rivadeneira, M. M. Rise and fall in diversity of Neogene marine vertebrates on the temperate Pacific coast of South America. Paleobiology 40, 659–674 (2014).

    Article  Google Scholar 

  44. 44.

    Finnegan, S. et al. Paleontological baselines for evaluating extinction risk in the modern oceans. Science 348, 567–570 (2015).

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Mouillot, D. et al. Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs. Proc. Natl Acad. Sci. USA 111, 13757–13762 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Coux, C., Rader, R., Bartomeus, I. & M., T. J. Linking species functional roles to their network roles. Ecol. Lett. 19, 762–770 (2016).

    Article  PubMed  Google Scholar 

  47. 47.

    Lefcheck, J. S. & Duffy, J. E. Multitrophic functional diversity predicts ecosystem functioning in experimental assemblages of estuarine consumers. Ecology 96, 2973–2983 (2015).

    Article  PubMed  Google Scholar 

  48. 48.

    Dehling, D. M., Jordano, P., Schaefer, H. M., Boehning-Gaese, K. & Schleuning, M. Morphology predicts species’ functional roles and their degree of specialization in plant–frugivore interactions. Proc. R. Soc. Lond. B Biol. Sci. 283, 20152444 (2016).

    Article  Google Scholar 

  49. 49.

    Cadotte, M. W., Carscadden, K. & Mirotchnick, N. Beyond species: functional diversity and the maintenance of ecological processes and services. J. Appl. Ecol. 48, 1079–1087 (2011).

    Article  Google Scholar 

  50. 50.

    Kozlowski, J. & Gawelczyk, A. T. Why are species’ body size distributions usually skewed to the right? Funct. Ecol. 16, 419–432 (2002).

    Article  Google Scholar 

  51. 51.

    Duffy, J. E. Biodiversity loss, trophic skew and ecosystem functioning. Ecol. Lett. 6, 680–687 (2003).

    Article  Google Scholar 

  52. 52.

    Duffy, J. E. Biodiversity and ecosystem function: the consumer connection. Oikos 99, 201–219 (2002).

    Article  Google Scholar 

  53. 53.

    Holland, S. M. Sea level change and the area of shallow-marine habitat: implications for marine biodiversity. Paleobiology 38, 205–217 (2012).

    Article  Google Scholar 

  54. 54.

    Jackson, J. B. C., Jung, P., Coates, A. G. & Collins, L. S. Diversity and extinction of tropical American mollusks and emergence of the isthmus of Panama. Science 260, 1624–1626 (1993).

    CAS  Article  PubMed  Google Scholar 

  55. 55.

    Budd, A. F., Johnson, K. G. & Stemann, T. A. in Evolution and Environment in Tropical America (eds Jackson, B. C., Budd, A. F. & Coates, A. G.) 168–204 (Univ. Chicago Press, 1996).

  56. 56.

    Allmon, W. D., Emslie, S. D., Jones, D. S. & Morgan, G. S. Late Neogene oceanographic change along Florida’s west coast: evidence and mechanisms. J. Geol. 104, 143–162 (1996).

    Article  Google Scholar 

  57. 57.

    Klaus, J. S. et al. Rise and fall of Pliocene free-living corals in the Caribbean. Geology 39, 375–378 (2011).

    Article  Google Scholar 

  58. 58.

    Todd, J. A. et al. The ecology of extinction: molluscan feeding and faunal turnover in the Caribbean Neogene. Proc. R. Soc. Lond. B Biol. Sci. 269, 571–577 (2002).

    CAS  Article  Google Scholar 

  59. 59.

    O’Dea, A. et al. Environmental change preceded Caribbean extinction by 2 million years. Proc. Natl Acad. Sci. USA 104, 5501–5506 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Smith, J. T. & Jackson, J. B. C. Ecology of extreme faunal turnover of tropical American scallops. Paleobiology 35, 77–93 (2009).

    Article  Google Scholar 

  61. 61.

    Valenzuela-Toro, A. M., Gutstein, C. S., Varas-Malca, R. M., Suarez, M. E. & Pyenson, N. D. Pinniped turnover in the South Pacific Ocean: new evidence from the Plio−Pleistocene of the Atacama Desert, Chile. J. Vert. Paleontol. 33, 216–223 (2013).

    Article  Google Scholar 

  62. 62.

    Metcalf, J. L. et al. Synergistic roles of climate warming and human occupation in Patagonian megafaunal extinctions during the last deglaciation. Sci. Adv. 2, e1501682 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Pimiento, C. et al. Geographical distribution patterns of Carcharocles megalodon over time reveal clues about extinction mechanisms. J. Biogeogr. 43, 1645–1655 (2016).

    Article  Google Scholar 

  64. 64.

    McNab, B. K. Resources and energetics determined dinosaur maximal size. Proc. Natl Acad. Sci. USA 106, 12184–12188 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Grady, J. M., Enquist, B. J., Dettweiler-Robinson, E., Wright, N. A. & Smith, F. A. Evidence for mesothermy in dinosaurs. Science 344, 1268–1272 (2014).

    CAS  Article  PubMed  Google Scholar 

  66. 66.

    Payne, J. L., Bush, A. M., Heim, N. A., Knope, M. L. & McCauley, D. J. Ecological selectivity of the emerging mass extinction in the oceans. Science 14, aaf2416 (2016).

    Google Scholar 

  67. 67.

    Boyles, J. G., Seebacher, F., Smit, B. & McKechnie, A. E. Adaptive thermoregulation in endotherms may alter responses to climate change. Integr. Comp. Biol. 51, 676–690 (2011).

    Article  PubMed  Google Scholar 

  68. 68.

    McNab, B. K. Energetics, body size, and the limits to endothermy. J. Zool. 199, 1–29 (1983).

    Article  Google Scholar 

  69. 69.

    Wright, D. H. Species-energy theory: an extension of species-area theory. Oikos 1, 496–506 (1983).

    Article  Google Scholar 

  70. 70.

    Pyenson, N. D. & Lindberg, D. R. What happened to grey whales during the Pleistocene? The ecological impact of sea level change on benthic feeding areas in the North Pacific Ocean. PloS ONE 6, e21295 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Davidson, A. D. et al. Drivers and hotspots of extinction risk in marine mammals. Proc. Natl Acad. Sci. USA 109, 3395–3400 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Wilmers, C. C., Estes, J. A., Edwards, M., Laidre, K. L. & Konar, B. Do trophic cascades affect the storage and flux of atmospheric carbon? An analysis of sea otters and kelp forests. Front Ecol. Environ. 10, 409–415 (2012).

    Article  Google Scholar 

  73. 73.

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

  74. 74.

    Silvestro, D., Salamin, N. & Schnitzler, J. PyRate: a new program to estimate speciation and extinction rates from incomplete fossil data. Methods Ecol. Evol. 5, 1126–1131 (2014).

    Article  Google Scholar 

  75. 75.

    Silvestro, D., Cascales-Miñana, B., Bacon, C. D. & Antonelli, A. Revisiting the origin and diversification of vascular plants through a comprehensive Bayesian analysis of the fossil record. New Phytol. 207, 425–436 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Hoeting, J. A., Madigan, D., Raftery, A. E. & Volinsky, C. T. Bayesian model averaging: a tutorial. Stat. Sci. 14, 382–417 (1999).

    Article  Google Scholar 

  77. 77.

    Gibbard, P. L., Head, M. J. & Walker, M. J. Formal ratification of the Quaternary system/period and the Pleistocene series/epoch with a base at 2.58 Ma. J. Quat. Sci 25, 96–102 (2010).

    Article  Google Scholar 

  78. 78.

    Laliberté, E. & Shipley, B. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-11 (2011).

  79. 79.

    Maire, E., Grenouillet, G., Brosse, S. & Villeger, S. How many dimensions are needed to accurately assess functional diversity? A pragmatic approach for assessing the quality of functional spaces. Glob. Ecol. Biogeogr. 24, 728–740 (2015).

    Article  Google Scholar 

  80. 80.

    Kowalewski, M. I. & Novack-Gottshall, P. H. in Quantitative Methods in Paleobiology (eds Alroy, J. & Hunt, G.) 19–54 (The Paleontological Society, 2010).

  81. 81.

    Foote, M. Origination and extinction components of taxonomic diversity: general problems. Paleobiology 26, 74–102 (2000).

    Article  Google Scholar 

  82. 82.

    Amante, C. & Eakins, B. W. 2009 ETOPO1 1 Arc-Minute Global Relief Model: Procedures, Data Sources and Analysis (NOAA Technical Memorandum NESDIS NGDC-24, National Geophysical Data Center, accessed June 2017).

  83. 83.

    Hijmans, R. J. et al. Package ‘raster’. R package version 2.5-8 (2015).

  84. 84.

    Bates, D. & Martin, M. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article  Google Scholar 

  85. 85.

    Walsh, C., Mac Nally, R. & Walsh, M. C. The hier. part package. R package version 1.4-0 (2003).

Download references

Acknowledgements

We thank M. Sánchez-Villagra for his support during the development of this research, S. Villegér, A. Antonelli, F. Leprieur, J. Lefcheck and L. Gamfeldt for their valuable suggestions, C. Ricotta and K. Boersma for their assistance with the use of R functions, B. Mcnab and M. Balk for their insights on thermoregulation, and J. Velez-Juarbe for his support assigning traits to marine mammals. We are grateful for the constructive comments provided by P. Novack-Gottshall, which significantly improved this work. PyRate analyses were run at the high-performance computing centre Vital-IT of the Swiss Institute of Bioinformatics (Lausanne, Switzerland). C.P. was supported by a Forschungskredit postdoctoral fellowship from the University of Zurich (FK-15-105), J.N.G. was supported by a European Union Marie Curie Career Integration Grant (FP7 MC CIG 61893), D.S. was funded by the Swedish Research Council (2015-04748) and S.V. was first supported by the Universidad de Alcalá postdoctoral programme, and then by the Alexander von Humboldt Foundation and the Federal Ministry for Education and Research (Germany). This is the Paleobiology Database publication number 284.

Author information

Affiliations

Authors

Contributions

C.P., J.N.G. and C.J. designed the research, C.P., J.N.G. and M.D.U. performed the research, C.P., J.N.G., C.F.C., D.S., S.V. and M.D.U. analysed the data, C.P. and J.N.G. wrote the paper, and C.F.C., S.V., D.S., M.D.U. and C.J. improved the final manuscript.

Corresponding author

Correspondence to Catalina Pimiento.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

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

Electronic supplementary material

Supplementary Information

Supplementary Methods, 9 Supplementary Tables, 12 Supplementary Figures

Supplementary Dataset 1

Species included in the analysis with details on class, maximum body size, guild, vertical position, habitat, metabolic control and status

Supplementary Dataset 2

References supporting marine megafaunal occurrences

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pimiento, C., Griffin, J.N., Clements, C.F. et al. The Pliocene marine megafauna extinction and its impact on functional diversity. Nat Ecol Evol 1, 1100–1106 (2017). https://doi.org/10.1038/s41559-017-0223-6

Download citation

Further reading

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