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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.

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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.

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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.

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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.

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Correspondence to Catalina Pimiento.

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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

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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

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