in

Frugivore-fruit size relationships between palms and mammals reveal past and future defaunation impacts

  • 1.

    Fleming, T. H. & Kress, W. J. The Ornaments of Life: Coevolution and Conservation in the Tropics (Univ. Chicago Press, 2013).

    Google Scholar 

  • 2.

    Comita, L. S. et al. Testing predictions of the Janzen-Connell hypothesis: a meta-analysis of experimental evidence for distance- and density-dependent seed and seedling survival. J. Ecol. 102, 845–856 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  • 3.

    Howe, H. F. & Smallwood, J. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13, 201–228 (1982).

    Article  Google Scholar 

  • 4.

    Jordano, P. in Seeds: The Ecology of Regeneration in Plant Communities 2nd edn (ed. Fenner, M.) 125–165 (CABI, 2000).

  • 5.

    Janzen, D. H. & Martin, P. S. Neotropical anachronisms: the fruits the gomphotheres ate. Science 215, 19–27 (1982).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 6.

    Guimarães, P. R., Galetti, M. & Jordano, P. Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. PLoS ONE 3, e1745 (2008).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 7.

    Galetti, M. et al. Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340, 1086–1090 (2013).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 8.

    Bender, I. M. A. et al. Morphological trait matching shapes plant-frugivore networks across the Andes. Ecography 41, 1910–1919 (2018).

    Article  Google Scholar 

  • 9.

    Faurby, S. & Svenning, J. C. Historic and prehistoric human-driven extinctions have reshaped global mammal diversity patterns. Divers. Distrib. 21, 1155–1166 (2015).

    Article  Google Scholar 

  • 10.

    Smith, F. A., Smith, R. E. E., Lyons, S. K. & Payne, J. L. Body size downgrading of mammals over the late Quaternary. Science 360, 310–313 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 11.

    Dirzo, R. et al. Defaunation in the Anthropocene. Science 345, 401–406 (2014).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 12.

    Martin, P. & Klein, R. Quaternary Extinctions: A Prehistoric Revolution. (Univ. Arizona Press, 1984).

    Google Scholar 

  • 13.

    Campos-Arceiz, A. & Blake, S. Megagardeners of the forest—the role of elephants in seed dispersal. Acta Oecol. 37, 542–553 (2011).

    ADS  Article  Google Scholar 

  • 14.

    Ripple, W. J. et al. Collapse of the world’s largest herbivores. Sci. Adv. 1, e1400103 (2015).

    ADS  PubMed  PubMed Central  Article  Google Scholar 

  • 15.

    Carbone, C., Cowlishaw, G., Isaac, N. & Rowcliffe, J. M. How far do animals go? Determinants of day range in mammals. Am. Nat. 165, 290–297 (2005).

    PubMed  Article  PubMed Central  Google Scholar 

  • 16.

    Pires, M. M., Guimaraes, P. R., Galetti, M. & Jordano, P. Pleistocene megafaunal extinctions and the functional loss of long-distance seed-dispersal services. Ecography 41, 153–163 (2018).

    Article  Google Scholar 

  • 17.

    Galetti, M. et al. Ecological and evolutionary legacy of megafauna extinctions. Biol. Rev. 93, 845–862 (2017).

    PubMed  Article  PubMed Central  Google Scholar 

  • 18.

    Jansen, P. A. et al. Thieving rodents as substitute dispersers of megafaunal seeds. Proc. Natl Acad. Sci. USA 109, 12610–12615 (2012).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 19.

    Onstein, R. E. et al. To adapt or go extinct? The fate of megafaunal palm fruits under past global change. Proc. R. Soc. B 285, 20180882 (2018).

    PubMed  Article  PubMed Central  Google Scholar 

  • 20.

    Young, H. S., McCauley, D. J., Galetti, M. & Dirzo, R. Patterns, causes, and consequences of Anthropocene defaunation. Annu. Rev. Ecol. Evolut. Syst. 47, 333–358 (2016).

    Article  Google Scholar 

  • 21.

    Galetti, M. & Dirzo, R. Ecological and evolutionary consequences of living in a defaunated world. Biol. Conserv. 163, 1–6 (2013).

    Article  Google Scholar 

  • 22.

    Emer, C., Galetti, M., Pizo, M. A., Jordano, P. & Verdú, M. Defaunation precipitates the extinction of evolutionarily distinct interactions in the Anthropocene. Sci. Adv. 5, eaav6699 (2019).

    ADS  PubMed  PubMed Central  Article  Google Scholar 

  • 23.

    Gardner, C. J., Bicknell, J. E., Baldwin-Cantello, W., Struebig, M. J. & Davies, Z. G. Quantifying the impacts of defaunation on natural forest regeneration in a global meta-analysis. Nat. Commun. 10, 4590 (2019).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 24.

    Dransfield, J. et al. Genera Palmarum — The Evolution and Classification of Palms (Royal Botanic Gardens, 2008).

    Google Scholar 

  • 25.

    Couvreur, T. L. P. & Baker, W. J. Tropical rain forest evolution: palms as a model group. BMC Biol. 11, 48 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  • 26.

    Terborgh, J. W. in Conservation Biology: the Science of Scarcity and Diversity (ed. Soulé, M. E.) 330–344 (Sinauer Associates, 1986).

  • 27.

    Zona, S. & Henderson, A. A review of animal-mediated seed dispersal of palms. Selbyana 11, 6–21 (1989).

    Google Scholar 

  • 28.

    Muñoz, G., Trøjelsgaard, K. & Kissling, W. D. A synthesis of animal-mediated seed dispersal of palms reveals distinct biogeographical differences in species interactions. J. Biogeogr. 46, 466–484 (2019).

    Article  Google Scholar 

  • 29.

    Kissling, W. D. et al. PalmTraits 1.0: a species-level functional trait database for palms worldwide. Sci. Data 6, 178 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  • 30.

    Govaerts, R. & Dransfield, J. World Checklist of Palms (Royal Botanic Gardens, 2005).

    Google Scholar 

  • 31.

    Brummitt, R. K., Pando, F., Hollis, S. & Brummitt, N. A. World Geographical Scheme for Recording Plant Distributions (TDWG, 2001).

  • 32.

    Cade, B. S. Model averaging and muddled multimodel inferences. Ecology 96, 2370–2382 (2015).

    PubMed  Article  PubMed Central  Google Scholar 

  • 33.

    Wheelwright, N. T. Fruit size, gape width, and the diets of fruit-eating birds. Ecology 66, 808–818 (1985).

    Article  Google Scholar 

  • 34.

    Lord, J. M. Frugivore gape size and the evolution of fruit size and shape in southern hemisphere floras. Austral Ecol. 29, 430–436 (2004).

    Article  Google Scholar 

  • 35.

    Levey, D. J. Seed size and fruit-handling techniques of avian frugivores. Am. Nat. 129, 471–485 (1987).

    Article  Google Scholar 

  • 36.

    Corlett, R. T. How to be a frugivore (in a changing world). Acta Oecol. 37, 674–681 (2011).

    ADS  Article  Google Scholar 

  • 37.

    Göldel, B., Kissling, W. D. & Svenning, J. C. Geographical variation and environmental correlates of functional trait distributions in palms (Arecaceae) across the New World. Bot. J. Linn. Soc. 179, 602–617 (2015).

    Article  Google Scholar 

  • 38.

    Kissling, W. D. et al. Cenozoic imprints on the phylogenetic structure of palm species assemblages worldwide. Proc. Natl Acad. Sci. USA 109, 7379–7384 (2012).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 39.

    Barnosky, A. D., Koch, P. L., Feranec, R. S., Wing, S. L. & Shabel, A. B. Assessing the causes of late Pleistocene extinctions on the continents. Science 306, 70–75 (2004).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 40.

    Sandom, C., Faurby, S., Sandel, B. & Svenning, J. C. Global late Quaternary megafauna extinctions linked to humans, not climate change. Proc. R. Soc. B 281, 20133254 (2014).

    PubMed  Article  PubMed Central  Google Scholar 

  • 41.

    Doughty, C. E. et al. Megafauna extinction, tree species range reduction, and carbon storage in Amazonian forests. Ecography 39, 194–203 (2015).

    Article  Google Scholar 

  • 42.

    Galetti, M., Donatti, C. I., Pires, A. S., Guimarães Jr, P. R. & Jordano, P. Seed survival and dispersal of an endemic Atlantic forest palm: the combined effects of defaunation and forest fragmentation. Bot. J. Linn. Soc. 151, 141–149 (2006).

    Article  Google Scholar 

  • 43.

    Beaune, D., Fruth, B., Bollache, L., Hohmann, G. & Bretagnolle, F. Doom of the elephant-dependent trees in a Congo tropical forest. For. Ecol. Manag. 295, 109–117 (2013).

    Article  Google Scholar 

  • 44.

    Wotton, D. M. & Kelly, D. Frugivore loss limits recruitment of large-seeded trees. Proc. R. Soc. B 278, 3345–3354 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  • 45.

    Harrison, R. D. et al. Consequences of defaunation for a tropical tree community. Ecol. Lett. 16, 687–694 (2013).

    PubMed  Article  PubMed Central  Google Scholar 

  • 46.

    Pérez-Méndez, N., Jordano, P., García, C. & Valido, A. The signatures of Anthropocene defaunation: cascading effects of the seed dispersal collapse. Sci. Rep. 6, 24820 (2016).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 47.

    Nevo, O. et al. Frugivores and the evolution of fruit colour. Biol. Lett. 14, 20180377 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 48.

    Nevo, O., Razafimandimby, D., Jeffrey, J. A. J., Schulz, S. & Ayasse, M. Fruit scent as an evolved signal to primate seed dispersal. Sci. Adv. 4, eaat4871 (2018).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 49.

    Bueno, R. S. et al. Functional redundancy and complementarities of seed dispersal by the last neotropical megafrugivores. PLoS ONE 8, e56252 (2013).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 50.

    Sekar, N., Lee, C.-L. & Sukumar, R. Functional nonredundancy of elephants in a disturbed tropical forest. Conserv. Biol. 31, 1152–1162 (2017).

    PubMed  Article  PubMed Central  Google Scholar 

  • 51.

    Campos-Arceiz, A., Traeholt, C., Jaffar, R., Santamaria, L. & Corlett, R. T. Asian tapirs are no elephants when it comes to seed dispersal. Biotropica 44, 220–227 (2012).

    Article  Google Scholar 

  • 52.

    Corlett, R. T. The impact of hunting on the mammalian fauna of tropical asian forests. Biotropica 39, 292–303 (2007).

    Article  Google Scholar 

  • 53.

    Vidal, M. M., Pires, M. M. & Guimarães Jr, P. R. Large vertebrates as the missing components of seed-dispersal networks. Biol. Conserv. 163, 42–48 (2013).

    Article  Google Scholar 

  • 54.

    Heinen, J. H., van Loon, E. E., Hansen, D. M. & Kissling, W. D. Extinction-driven changes in frugivore communities on oceanic islands. Ecography 41, 1245–1255 (2017).

    Article  Google Scholar 

  • 55.

    Valido, A. & Olesen, J. M. Frugivory and seed dispersal by lizards: a global review. Front. Ecol. Evolut. 7, 49 (2019).

    Article  Google Scholar 

  • 56.

    Florens, F. B. V. et al. Disproportionately large ecological role of a recently mass-culled flying fox in native forests of an oceanic island. J. Nat. Conserv. 40, 85–93 (2017).

    Article  Google Scholar 

  • 57.

    Vizentin-Bugoni, J. et al. Structure, spatial dynamics, and stability of novel seed dispersal mutualistic networks in Hawai‘i. Science 364, 78–82 (2019).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 58.

    Muñoz-Gallego, R., Fedriani, J. M. & Traveset, A. Non-native mammals are the main seed dispersers of the ancient mediterranean palm Chamaerops humilis L. in the balearic islands: rescuers of a lost seed dispersal service? Front. Ecol. Evolut. 7, 161 (2019).

    Article  Google Scholar 

  • 59.

    Pires, M. M. Rewilding ecological communities and rewiring ecological networks. Perspect. Ecol. Conserv. 15, 257–265 (2017).

    Google Scholar 

  • 60.

    Schleuning, M. et al. Ecological networks are more sensitive to plant than to animal extinction under climate change. Nat. Commun. 7, 13965 (2016).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 61.

    Maisels, F. et al. Devastating decline of forest elephants in central Africa. PLoS ONE 8, e59469 (2013).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 62.

    Valiente-Banuet, A. et al. Beyond species loss: the extinction of ecological interactions in a changing world. Funct. Ecol. 29, 299–307 (2014).

    Article  Google Scholar 

  • 63.

    Tucker, M. A. et al. Moving in the Anthropocene: global reductions in terrestrial mammalian movements. Science 359, 466–469 (2018).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 64.

    Sales, L. P., Ribeiro, B. R., Pires, M. M., Chapman, C. A. & Loyola, R. Recalculating route: dispersal constraints will drive the redistribution of Amazon primates in the Anthropocene. Ecography 42, 1789–1801 (2019).

    Article  Google Scholar 

  • 65.

    Humphreys, A. M., Govaerts, R., Ficinski, S. Z., Lughadha, E. N. & Vorontsova, M. S. Global dataset shows geography and life form predict modern plant extinction and rediscovery. Nat. Ecol. Evolut. 3, 1043–1047 (2019).

    Article  Google Scholar 

  • 66.

    Cronk, Q. Plant extinctions take time. Science 353, 446–447 (2016).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 67.

    Svenning, J. C. et al. Science for a wilder Anthropocene: synthesis and future directions for trophic rewilding research. Proc. Natl Acad. Sci. USA 113, 898–906 (2016).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 68.

    Galetti, M., Pires, A. S., Brancalion, P. H. & Fernandez, F. A. Reversing defaunation by trophic rewilding in empty forests. Biotropica 49, 5–8 (2017).

    Article  Google Scholar 

  • 69.

    Fricke, E. C., Tewksbury, J. J. & Rogers, H. S. Defaunation leads to interaction deficits, not interaction compensation, in an island seed dispersal network. Glob. Change Biol. 24, e190–e200 (2017).

    Article  Google Scholar 

  • 70.

    Meyer, C., Weigelt, P. & Kreft, H. Multidimensional biases, gaps and uncertainties in global plant occurrence information. Ecol. Lett. 19, 992–1006 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  • 71.

    Kissling, W. D. et al. Quaternary and pre-Quaternary historical legacies in the global distribution of a major tropical plant lineage. Glob. Ecol. Biogeogr. 21, 909–921 (2012).

    Article  Google Scholar 

  • 72.

    Cheke, A. S. & Dahl, J. F. The Status of bats on western Indian Ocean islands, with special reference to Pteropus. Mammalia 45, 205–238 (1981).

    Article  Google Scholar 

  • 73.

    Prescott, G. W., Williams, D. R., Balmford, A., Green, R. E. & Manica, A. Quantitative global analysis of the role of climate and people in explaining late Quaternary megafaunal extinctions. Proc. Natl Acad. Sci. USA 109, 4527–4531 (2012).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 74.

    Martin, P. S. in Quaternary Extinctions: A Prehistoric Revolution (eds Martin, P. S. & Klein, R. G.) 354–403 (Univ. Arizona Press, 1984).

  • 75.

    Miller, G. H. et al. Ecosystem collapse in Pleistocene Australia and a human role in megafaunal extinction. Science 309, 287–290 (2005).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 76.

    Faurby, S. et al. PHYLACINE 1.2: the phylogenetic atlas of mammal macroecology. Ecology 99, 2626 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 77.

    Kissling, W. D. et al. Establishing macroecological trait datasets: digitalization, extrapolation, and validation of diet preferences in terrestrial mammals worldwide. Ecol. Evolut. 4, 2913–2930 (2014).

    Article  Google Scholar 

  • 78.

    International Union for Conservation of Nature and Natural Resources. The IUCN Red List of threatened species. Version 2018-2. IUCN http://www.iucnredlist.org (2018).

  • 79.

    Tiffney, B. H. Vertebrate dispersal of seed plants through time. Annu. Rev. Ecol. Evolut. Syst. 35, 1–29 (2004).

    Article  Google Scholar 

  • 80.

    Franãğa, L. D. M. et al. Review of feeding ecology data of Late Pleistocene mammalian herbivores from South America and discussions on niche differentiation. Earth Sci. Rev. 140, 158–165 (2015).

    ADS  Article  CAS  Google Scholar 

  • 81.

    MacFadden, B. J. & Shockey, B. J. Ancient feeding ecology and niche differentiation of Pleistocene mammalian herbivores from Tarija, Bolivia: morphological and isotopic evidence. Paleobiology 23, 77–100 (1997).

    Article  Google Scholar 

  • 82.

    Morosi, E. & Ubilla, M. Dietary and palaeoenvironmental inferences in Neolicaphrium recens Frenguelli, 1921 (Litopterna, Proterotheriidae) using carbon and oxygen stable isotopes (Late Pleistocene; Uruguay). Hist. Biol. 31, 196–202 (2017).

    Article  Google Scholar 

  • 83.

    MacFadden, B. J. Diet and habitat of toxodont megaherbivores (Mammalia, Notoungulata) from the late Quaternary of South and Central America. Quat. Res. 64, 113–124 (2005).

    Article  Google Scholar 

  • 84.

    Domingo, L., Prado, J. L. & Alberdi, M. T. The effect of paleoecology and paleobiogeography on stable isotopes of Quaternary mammals from South America. Quat. Sci. Rev. 55, 103–113 (2012).

    ADS  Article  Google Scholar 

  • 85.

    DeSantis, L. R. G., Field, J. H., Wroe, S. & Dodson, J. R. Dietary responses of Sahul (Pleistocene Australia-New Guinea) megafauna to climate and environmental change. Paleobiology 43, 181–195 (2017).

    Article  Google Scholar 

  • 86.

    Karger, D. N. et al. Data descriptor: climatologies at high resolution for the earth’s land surface areas. Sci. Data 4, 170122 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  • 87.

    Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).

    Article  Google Scholar 

  • 88.

    Braconnot, P. et al. Evaluation of climate models using palaeoclimatic data. Nat. Clim. Change 2, 417–424 (2012).

    ADS  Article  Google Scholar 

  • 89.

    Kissling, W. D. & Carl, G. Spatial autocorrelation and the selection of simultaneous autoregressive models. Glob. Ecol. Biogeogr. 17, 59–71 (2008).

    Article  Google Scholar 

  • 90.

    Bivand, R. et al. spatialreg: spatial regression analysis. GitHub https://r-spatial.github.io/spatialreg/ (2019).

  • 91.

    Burnham, K. P. & Anderson, D. R. Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach 2nd edn (Springer, 2002).

  • 92.

    Grueber, C. E., Nakagawa, S., Laws, R. J. & Jamieson, I. G. Multimodel inference in ecology and evolution: challenges and solutions. J. Evolut. Biol. 24, 699–711 (2011).

    CAS  Article  Google Scholar 

  • 93.

    Harrison, X. A. et al. A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ 6, e4794 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 94.

    Bartoń, K. MuMIn: multi-model inference. CRAN https://cran.r-project.org/package=MuMIn (2019).

  • 95.

    Galipaud, M., Gillingham, M. A. F. & Dechaume-Moncharmont, F.-X. A farewell to the sum of Akaike weights: The benefits of alternative metrics for variable importance estimations in model selection. Methods Ecol. Evolut. 8, 1668–1678 (2017).

    Article  Google Scholar 

  • 96.

    Zuber, V. & Strimmer, K. High-dimensional regression and variable selection using CAR scores. Stat. Appl. Genet. Mol. Biol. 10, 34 (2011).

    MathSciNet  MATH  Article  Google Scholar 

  • 97.

    Grömping, U. Relative importance for linear regression in R: the package relaimpo. J. Stat. Softw. 17, 1–27 (2006).

    Article  Google Scholar 

  • 98.

    Mooers, A. Ø., Faith, D. P. & Maddison, W. P. Converting endangered species categories to probabilities of extinction for phylogenetic conservation prioritization. PLoS ONE 3, e3700 (2008).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 99.

    Davis, M., Faurby, S. & Svenning, J. C. Mammal diversity will take millions of years to recover from the current biodiversity crisis. Proc. Natl Acad. Sci. USA 115, 11262–11267 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 100.

    International Union for Conservation of Nature and Natural Resources. IUCN Red List categories and criteria: version 3.1, 2nd edn (IUCN, 2012).

  • 101.

    Hoffmann, M. et al. The impact of conservation on the status of the world’s vertebrates. Science 330, 1503–1509 (2010).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 102.

    Di Marco, M. et al. A retrospective evaluation of the global decline of carnivores and ungulates. Conserv. Biol. 28, 1109–1118 (2014).

    PubMed  Article  PubMed Central  Google Scholar 


  • Source: Ecology - nature.com

    Publisher Correction: Science diplomacy for plant health

    Validating the physics behind the new MIT-designed fusion experiment