Recent extinctions disturb path to equilibrium diversity in Caribbean bats


Islands are ideal systems to model temporal changes in biodiversity and reveal the influence of humans on natural communities. Although theory predicts biodiversity on islands tends towards an equilibrium value, the recent extinction of large proportions of island biotas complicates testing this model. The well-preserved subfossil record of Caribbean bats—involving multiple insular radiations—provides a rare opportunity to model diversity dynamics in an insular community. Here, we reconstruct the diversity trajectory in noctilionoid bats of the Greater Antilles by applying a dynamic model of colonization, extinction and speciation to phylogenetic and palaeontological data including all known extinct and extant species. We show species richness asymptotes to an equilibrium value, a demonstration of natural equilibrium dynamics across an entire community. However, recent extinctions—many caused by humans—have wiped out nearly a third of island lineages, dragging diversity away from equilibrium. Using a metric to measure island biodiversity loss, we estimate it will take at least eight million years to regain pre-human diversity levels. Our integrative approach reveals how anthropogenic extinctions can drastically alter the natural trajectory of biological communities, resulting in evolutionary disequilibrium.

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Figure 1: Quaternary diversity of noctilionoid bats in the GA.
Figure 2: Bootstrap precision estimates of the parameters of the DI model.
Figure 3: Expected future noctilionoid bat endemic diversity in the GA for the high human impact scenario.


  1. 1

    Harmon, L. J. & Harrison, S. Species diversity is dynamic and unbounded at local and continental scales. Am. Nat. 185, 584–593 (2015).

  2. 2

    Manceau, M., Lambert, A. & Morlon, H. Phylogenies support out-of-equilibrium models of biodiversity. Ecol. Lett. 18, 347–356 (2015).

  3. 3

    Phillimore, A. B. & Price, T. D. Density-dependent cladogenesis in birds. PLoS Biol. 6, e71 (2008).

  4. 4

    Rabosky, D. L. & Glor, R. E. Equilibrium speciation dynamics in a model adaptive radiation of island lizards. Proc. Natl Acad. Sci. USA 107, 22178–22183 (2010).

  5. 5

    MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 1967).

  6. 6

    Morgan, G. S. & Woods, C. A. Extinction and the zoogeography of West Indian land mammals. Biol. J. Linn. Soc. 28, 167–203 (1986).

  7. 7

    Weigelt, P., Steinbauer, M. J., Cabral, J. S. & Kreft, H. Late Quaternary climate change shapes island biodiversity. Nature 532, 99–102 (2016).

  8. 8

    Soto-Centeno, J. A. & Steadman, D. W. Fossils reject climate change as the cause of extinction of Caribbean bats. Sci. Rep. 5, 7971 (2015).

  9. 9

    Blackburn, T. M., Cassey, P., Duncan, R. P., Evans, K. L. & Gaston, K. J. Avian extinction and mammalian introductions on oceanic islands. Science 305, 1955–1958 (2004).

  10. 10

    Steadman, D. W. et al. Vertebrate community on an ice-age Caribbean island. Proc. Natl Acad. Sci. USA 112, 201516490 (2015).

  11. 11

    Brace, S., Turvey, S. T., Weksler, M., Hoogland, M. L. P. & Barnes, I. Unexpected evolutionary diversity in a recently extinct Caribbean mammal radiation. Proc. R. Soc. B 282, 20142371–20142371 (2015).

  12. 12

    MacPhee, R. D. E. in American Megafaunal Extinctions at the End of the Pleistocene. (ed. Haynes, G. ) 169–193 (Springer, 2009).

  13. 13

    Dávalos, L. M. & Russell, A. L. Deglaciation explains bat extinction in the Caribbean. Ecol. Evol. 2, 3045–3051 (2012).

  14. 14

    Dávalos, L. M. & Turvey, S. T. in Bones, Clones, and Biomes: the History and Geography of Recent Neotropical Mammals (eds Patterson, B. & Costa, L. ) 157–202 (Univ. Chicago Press, 2012).

  15. 15

    Rojas, D., Warsi, O. M. & Dávalos, L. M. Bats (Chiroptera: Noctilionoidea) challenge recent origin of neotropical diversity. Syst. Biol. 65, 432–448 (2016).

  16. 16

    Fleming, T. H. & Racey, P. A. Island Bats: Evolution, Ecology, and Conservation. (Univ. Chicago Press, 2010).

  17. 17

    Cardillo, M., Gittleman, J. L. & Purvis, A. Global patterns in the phylogenetic structure of island mammal assemblages. Proc. R. Soc. B 275, 1549–1556 (2008).

  18. 18

    Iturralde-Vinent, M. A. & MacPhee, R. D. E. Paleogeography of the Caribbean region: implications for Cenozoic biogeography. Bull. Am. Mus. Nat. Hist. 238, 1–95 (1999).

  19. 19

    Ricklefs, R. E. & Bermingham, E. Nonequilibrium diversity dynamics of the Lesser Antillean avifauna. Science 294, 1522–1524 (2001).

  20. 20

    Valente, L. M., Phillimore, A. B. & Etienne, R. S. Equilibrium and non-equilibrium dynamics simultaneously operate in the Galápagos Islands. Ecol. Lett. 18, 844–852 (2015).

  21. 21

    Stoetzel, E., Royer, A., Cochard, D. & Lenoble, A. Late Quaternary changes in bat palaeobiodiversity and palaeobiogeography under climatic and anthropogenic pressure: new insights from Marie-Galante, Lesser Antilles. Quat. Sci. Rev. 143, 150–174 (2016).

  22. 22

    Giovas, C. M. & Fitzpatrick, S. M. Prehistoric migration in the Caribbean: past perspectives, new models and the ideal free distribution of West Indian colonization. World Archaeol. 46, 569–589 (2014).

  23. 23

    Graham, A. Geohistory models and cenozoic paleoenvironments of the Caribbean region. Syst. Bot. 28, 378–386 (2003).

  24. 24

    Whittaker, R. J., Triantis, K. A. & Ladle, R. J. A general dynamic theory of oceanic island biogeography. J. Biogeogr. 35, 977–994 (2008).

  25. 25

    Gillespie, R. & Roderick, G. Evolution: geology and climate drive diversification. Nature 509, 297–298 (2014).

  26. 26

    Borregaard, M. K. et al. Oceanic island biogeography through the lens of the general dynamic model: assessment and prospect. Biol. Rev. (2016).

  27. 27

    Marshall, C. R. & Quental, T. B. The uncertain role of diversity dependence in species diversification and the need to incorporate time-varying carrying capacities. Phil. Trans. R. Soc. B. 371, 20150217 (2016).

  28. 28

    Warren, B. et al. Islands as model systems in ecology and evolution: progress and prospects fifty years after MacArthur-Wilson. Ecol. Lett. 18, 200–217 (2015).

  29. 29

    Quental, T. B. & Marshall, C. R. Diversity dynamics: molecular phylogenies need the fossil record. Trends Ecol. Evol. 25, 434–441 (2010).

  30. 30

    Helmus, M. R., Mahler, D. L. & Losos, J. B. Island biogeography of the Anthropocene. Nature 513, 543–546 (2014).

  31. 31

    Herrera, J. P. & Dávalos, L. M. Phylogeny and divergence times of lemurs inferred with recent and ancient fossils in the tree. Syst. Biol. 65, 772–791 (2016).

  32. 32

    Schipper, J. et al. The status of the world’s land and marine mammals: diversity, threat, and knowledge. Science 322, 225–30 (2008).

  33. 33

    Fleming, T. H., Murray, K. L. & Carstens, B. C. in Evolution, Ecology, and Conservation of Island Bats (eds Fleming, T. H. & Racey, P. A. ) 116–150 (Univ. Chicago Press, 2010).

  34. 34

    Dávalos, L. M. in Island Bats: Ecology, Evolution, and Conservation. (eds Fleming, T. H. & Racey, P. A. ) 96–115 (Univ. Chicago Press, 2010).

  35. 35

    Hoffmann, F. G. & Baker, R. J. Systematics of bats of the genus Glossophaga (Chiroptera: Phyllostomidae) and phylogeography in G. soricina based on the Cytochrome-b gene. J. Mamm. 82, 1092–1101 (2001).

  36. 36

    Silva-Taboada, G. Fossil Chiroptera from cave deposits in central Cuba, with description of two new species (Genera Pteronotus and Mormoops) and the first West Indian record of Mormoops megalophylla . Acta Zool. Crac. 19, 33–73 (1974).

  37. 37

    Koopman, K. & Williams, E. Fossil Chiroptera collected by H.E. Anthony in Jamaica. Am. Mus. Novit. 1519, 1–29 (1951).

  38. 38

    Choate, J. R. & Birney, E. C. Sub-recent Insectivora and Chiroptera from Puerto Rico, with the description of a new bat of the genus Stenoderma . J. Mamm. 49, 400–412 (1968).

  39. 39

    Etienne, R., Pigot, A. & Phillimore, A. How reliably can we infer diversity-dependent diversification from phylogenies? Methods Ecol. Evol. 7, 1092–1099 (2016).

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We thank A. Phillimore for discussions regarding DAISIE. We thank M. Lim, A. Phillimore, D. Rojas and L. Yohe for comments on the manuscript. Illustrations were produced by A. Tejedor. L.V. was funded by the Alexander von Humboldt Foundation, the Brandenburg Ministry of Science, Research and Culture and the German Research Foundation (DFG Grant VA 1102/1-1). L.M.D. was supported by the National Science Foundation (DEB-1442142). R.S.E. was supported by the Netherlands Organisation for Scientific Research (NWO) through a VICI grant.

Author information

L.M.D. and L.V. designed the study and wrote the manuscript. L.V. performed the analyses. R.S.E. provided theoretical input and developed analytic tools. All authors read and commented on the manuscript.

Correspondence to Liliana M. Dávalos.

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Supplementary information

Supplementary Information

Supplementary Figures 1–8, Supplementary Tables 1–4, Supplementary References (PDF 879 kb)

Supplementary Data 1

Consensus datasets for the three extinction scenarios used in the DAISIE analyses. (XLSX 41 kb)

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Valente, L., Etienne, R. & Dávalos, L. Recent extinctions disturb path to equilibrium diversity in Caribbean bats. Nat Ecol Evol 1, 0026 (2017).

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