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Rapid recovery of Patagonian plant–insect associations after the end-Cretaceous extinction

Nature Ecology & Evolution volume 1, Article number: 0012 (2017) Cite this article

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Abstract

The Southern Hemisphere may have provided biodiversity refugia after the Cretaceous/Palaeogene (K/Pg) mass extinction. However, few extinction and recovery studies have been conducted in the terrestrial realm using well-dated macrofossil sites that span the latest Cretaceous (late Maastrichtian) and early Palaeocene (Danian) outside western interior North America (WINA). Here, we analyse insect-feeding damage on 3,646 fossil leaves from the latest Maastrichtian and three time slices of the Danian in Chubut, Patagonia, Argentina (palaeolatitude approximately 50° S). We test the southern refugial hypothesis and the broader hypothesis that the extinction and recovery of insect herbivores, a central component of terrestrial food webs, differed substantially from WINA at locations far south of the Chicxulub impact structure in Mexico. We find greater insect-damage diversity in Patagonia than in WINA during both the Maastrichtian and Danian, indicating a previously unknown insect richness. As in WINA, the total diversity of Patagonian insect damage decreased from the Cretaceous to the Palaeocene, but recovery to pre-extinction levels occurred within approximately 4 Myr compared with approximately 9 Myr in WINA. As for WINA, there is no convincing evidence for survival of any of the diverse Cretaceous leaf miners in Patagonia, indicating a severe K/Pg extinction of host-specialized insects and no refugium. However, a striking difference from WINA is that diverse, novel leaf mines are present at all Danian sites, demonstrating a considerably more rapid recovery of specialized herbivores and terrestrial food webs. Our results support the emerging idea of large-scale geographic heterogeneity in extinction and recovery from the end-Cretaceous catastrophe.

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Figure 1: Insect damage on latest Cretaceous and early Palaeocene leaves from Chubut, Argentina.
Figure 2: Insect-feeding damage richness for late Cretaceous and Palaeocene floras from Patagonia and WINA.
Figure 3: Occurrences of 69 insect damage types through four time slices spanning the latest Cretaceous to early Palaeocene in Patagonia, Argentina.

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References

  1. McLoughlin, S., Carpenter, R. J., Jordan, G. J. & Hill, R. S. Seed ferns survived the end-Cretaceous mass extinction in Tasmania. Am. J. Bot. 95, 465–471 (2008).

    Article  PubMed  Google Scholar 

  2. Jiang, S., Braklower, T. J., Patzkowsky, M. E., Kump, L. R. & Schueth, J. D. Geographic controls on nannoplankton extinction across the Cretaceous/Palaeogene boundary. Nat. Geosci. 3, 280–285 (2010).

    Article  CAS  Google Scholar 

  3. Barreda, V. D. et al. Cretaceous/Paleogene floral turnover in Patagonia: drop in diversity, low extinction, and a Classopollis spike. PLoS ONE 7, e52455 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Wilf, P., Cúneo, N. R., Escapa, I. H., Pol, D. & Woodburne, M. O. Splendid and seldom isolated: the paleobiogeography of Patagonia. Annu. Rev. Earth Planet. Sci. 41, 561–603 (2013).

    Article  CAS  Google Scholar 

  5. McLoughlin, S., Carpenter, R. J. & Pott, C. Ptilophyllum muelleri (Ettingsh.) comb. nov. from the Oligocene of Australia: last of the Bennettitales? Int. J. Plant Sci. 172, 574–585 (2011).

    Article  Google Scholar 

  6. Vajda, V., Raine, J. I. & Hollis, C. J. Indication of global deforestation at the Cretaceous-Tertiary boundary by New Zealand fern spike. Science 294, 1700–1702 (2001).

    Article  CAS  PubMed  Google Scholar 

  7. Vajda, V. & McLoughlin, S. Fungal proliferation at the Cretaceous-Tertiary boundary. Science 303, 1489 (2004).

    Article  CAS  PubMed  Google Scholar 

  8. Iglesias, A. et al. A Paleocene lowland macroflora from Patagonia reveals significantly greater richness than North American analogs. Geology 35, 947–950 (2007).

    Article  Google Scholar 

  9. Clyde, W. C. et al. New age constraints for the Salamanca Formation and lower Río Chico Group in the western San Jorge Basin, Patagonia, Argentina: implications for Cretaceous-Paleogene extinction recovery and land mammal age correlations. Geol. Soc. Am. Bull. 126, 289–306 (2014).

    Article  CAS  Google Scholar 

  10. Comer, E. E. et al. Sedimentary facies and depositional environments of diverse early Paleocene floras, north-central San Jose Basin, Patagonia, Argentina. Palaios 30, 553–573 (2015).

    Article  Google Scholar 

  11. Case, J. A. & Woodburne, M. O. South American marsupials: a successful crossing of the Cretaceous-Tertiary boundary. Palaios 1, 413–416 (1986).

    Article  Google Scholar 

  12. Apesteguía, S., Gómez, R. O. & Rougier, G. W. The youngest South American rhynchocephalian, a survivor of the K/Pg extinction. Proc. R. Soc. B. 281, 20140811 (2014).

    Article  PubMed  Google Scholar 

  13. Witts, J. D. et al. Macrofossil evidence for a rapid and severe Cretaceous–Paleogene mass extinction in Antarctica. Nat. Commun. 7, 11738 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kennedy, E. M. Late Cretaceous and Paleocene terrestrial climates of New Zealand: leaf fossil evidence from South Island assemblages. N. Z. J. Geol. Geophys. 46, 295–306 (2003).

    Article  Google Scholar 

  15. Pole, M. & Vajda, V. A new terrestrial Cretaceous-Paleogene site in New Zealand—turnover in macroflora confirmed by palynology. Cretac. Res. 30, 917–938 (2009).

    Article  Google Scholar 

  16. Steinthorsdottir, M., Vajda, V. & Pole, M. Global trends of pCO2 across the Cretaceous–Paleogene boundary supported by the first Southern Hemisphere stomatal proxy-based pCO2 reconstruction. Palaeogeogr. Palaeoclimatol. Palaeoecol. http://dx.doi.org/10.1016/j.palaeo.2016.04.033 (2016).

  17. Wilf, P., Labandeira, C. C., Johnson, K. R. & Ellis, B. Decoupled plant and insect diversity after the end-Cretaceous extinction. Science 313, 1112–1115 (2006).

    Article  CAS  PubMed  Google Scholar 

  18. Labandeira, C. C., Johnson, K. R. & Wilf, P. Impact of the terminal Cretaceous event on plant-insect associations. Proc. Natl Acad. Sci. USA 99, 2061–2066 (2002).

    Article  CAS  PubMed  Google Scholar 

  19. Currano, E. D. et al. Sharply increased insect herbivory during the Paleocene-Eocene Thermal Maximum. Proc. Natl Acad. Sci. USA 105, 1960–1964 (2008).

    Article  CAS  PubMed  Google Scholar 

  20. Donovan, M. P., Wilf, P., Labandeira, C. C., Johnson, K. R. & Peppe, D. J. Novel insect leaf-mining after the end-Cretaceous extinction and the demise of Cretaceous leaf miners, Great Plains, USA. PLoS ONE 9, e103542 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Carvalho, M. R. et al. Insect leaf-chewing damage tracks herbivore richness in modern and ancient forests. PLoS ONE 9, e94950 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Wing, S. L. et al. Late Paleocene fossils from the Cerrejón Formation, Colombia, are the earliest record of Neotropical rainforest. Proc. Natl Acad. Sci. USA 106, 18627–18632 (2009).

    Article  CAS  PubMed  Google Scholar 

  23. Wappler, T., Currano, E. D., Wilf, P., Rust, J. & Labandeira, C. C. No post-Cretaceous ecosystem depression in European forests? Rich insect-feeding damage on diverse middle Palaeocene plants, Menat, France. Proc. R. Soc. B 276, 4271–4277 (2009).

    Article  PubMed  Google Scholar 

  24. Wappler, T. & Denk, T. Herbivory in early Tertiary Arctic forests. Palaeogeogr. Palaeoclimatol. Palaeoecol. 310, 283–295 (2011).

    Article  Google Scholar 

  25. Scasso, R. A. et al. Integrated bio- and lithofacies analysis of coarse-grained, tide-dominated deltaic environments across the Cretaceous/Paleogene boundary in Patagonia, Argentina. Cretac. Res. 36, 37–57 (2012).

    Article  Google Scholar 

  26. Wilf, P. & Labandeira, C. C. Response of plant-insect associations to Paleocene-Eocene warming. Science 284, 2153–2156 (1999).

    Article  CAS  PubMed  Google Scholar 

  27. Labandeira, C. C., Wilf, P., Johnson, K. R. & Marsh, F. Guide to Insect (and Other) Damage Types on Compressed Plant Fossils Version 3.0. (Smithsonian Institution, 2007); http://paleobiology.si.edu/insects/index.html

    Google Scholar 

  28. Schulte, P. et al. The Chicxulub asteroid impact and mass extinction at the Cretaceous-Paleogene boundary. Science 327, 1214–1218 (2010).

    Article  CAS  PubMed  Google Scholar 

  29. Vajda, V., Ocampo, A., Ferrow, E. & Koch, C. B. Nano particles as the primary cause for long-term sunlight suppression at high southern latitudes following the Chicxulub impact—evidence from ejecta deposits in Belize and Mexico. Gondwana Res. 27, 1079–1088 (2015).

    Article  CAS  Google Scholar 

  30. Aberhan, M. & Kiessling, W. Rebuilding biodiversity of Patagonian marine molluscs after the end-Cretaceous mass extinction. PLoS ONE 9, e102629 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  32. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2013).

Download references

Acknowledgements

The authors thank E. Currano, K. Johnson, P. Puerta, L. Reiner and E. Ruigómez for field and laboratory assistance and T. Bralower, D. Hughes and M. Patzkowsky for discussion. This study was supported by grants to M.P.D. from the Evolving Earth Foundation, the Geological Society of America, Sigma Xi, the Paleontological Society and the P. D. Krynine Memorial Fund of Penn State Department of Geosciences; and to P.W., A.I. and N.R.C. from NSF awards DEB-0919071 and DEB-1556666.

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Authors and Affiliations

  1. Department of Geosciences, Pennsylvania State University, University Park, Pennsylvania, 16802, USA

    Michael P. Donovan & Peter Wilf

  2. Instituto de Investigaciones en Biodiversidad y Medioambiente, CONICET-Universidad Nacional del Comahue, San Carlos de Bariloche, 8400, Argentina

    Ari Iglesias

  3. Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, 20013, DC, USA

    Conrad C. Labandeira

  4. Department of Entomology and Behavior, Ecology, Evolution, and Systematics Program, University of Maryland, College Park, Maryland, 20742, USA

    Conrad C. Labandeira

  5. School of Life Sciences, Capital Normal University, Beijing, 100048, China

    Conrad C. Labandeira

  6. CONICET−Museo Paleontológico Egidio Feruglio, Trelew, 9100, Argentina

    N. Rubén Cúneo

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  1. Michael P. Donovan
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  2. Ari Iglesias
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  3. Peter Wilf
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  4. Conrad C. Labandeira
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  5. N. Rubén Cúneo
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Contributions

M.P.D., A.I., P.W. and C.C.L. designed the research. M.P.D., A.I., P.W. and N.R.C. did the fieldwork. M.P.D., A.I. and C.C.L. collected the DT data. N.R.C. led research on the Lefipán flora. M.P.D. performed the analyses and wrote the manuscript. All authors commented on and substantially contributed to the manuscript.

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Correspondence to Michael P. Donovan.

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The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary Methods, Supplementary Discussion, Supplementary Figures 1–10, Supplementary Tables 1 and 2 and Supplementary References (PDF 1722 kb)

Supplementary Data

Occurrences of insect damage types on Patagonian fossil floras. (XLSX 818 kb)

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Donovan, M., Iglesias, A., Wilf, P. et al. Rapid recovery of Patagonian plant–insect associations after the end-Cretaceous extinction. Nat Ecol Evol 1, 0012 (2017). https://doi.org/10.1038/s41559-016-0012

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