Article | Published:

Change in dominance determines herbivore effects on plant biodiversity

Nature Ecology & Evolution (2018) | Download Citation

Abstract

Herbivores alter plant biodiversity (species richness) in many of the world’s ecosystems, but the magnitude and the direction of herbivore effects on biodiversity vary widely within and among ecosystems. One current theory predicts that herbivores enhance plant biodiversity at high productivity but have the opposite effect at low productivity. Yet, empirical support for the importance of site productivity as a mediator of these herbivore impacts is equivocal. Here, we synthesize data from 252 large-herbivore exclusion studies, spanning a 20-fold range in site productivity, to test an alternative hypothesis—that herbivore-induced changes in the competitive environment determine the response of plant biodiversity to herbivory irrespective of productivity. Under this hypothesis, when herbivores reduce the abundance (biomass, cover) of dominant species (for example, because the dominant plant is palatable), additional resources become available to support new species, thereby increasing biodiversity. By contrast, if herbivores promote high dominance by increasing the abundance of herbivory-resistant, unpalatable species, then resource availability for other species decreases reducing biodiversity. We show that herbivore-induced change in dominance, independent of site productivity or precipitation (a proxy for productivity), is the best predictor of herbivore effects on biodiversity in grassland and savannah sites. Given that most herbaceous ecosystems are dominated by one or a few species, altering the competitive environment via herbivores or by other means may be an effective strategy for conserving biodiversity in grasslands and savannahs globally.

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Data availability

While not all raw species abundances are publicly available because of lack of permission from data owners (contact individual data set owners listed in Supplementary Table 1), all data generated and analysed during the current study (site-level richness response to herbivory, site-level Berger–Parker and Simpson’s dominance response to herbivory, site ANPP, and site MAP) are provided in Supplementary Table 2.

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Acknowledgements

Funding for this synthesis was provided for by USDA AFRI Foundational Conference Grant (award no. 2018-67013-27400). We would like to thank the National Evolutionary Synthesis Center (Grasslands Working Group), the School of Global Environmental Sustainability at Colorado State University and the National Center for Ecological Analysis and Synthesis for hosting working meetings that led to these analyses. We also thank M. Ritchie, D. Augustine and R. Pringle for helpful comments on an earlier version of the manuscript. Any use of trade, firm or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. Individual sites acknowledge funding support: Kenya Long-term Exclosure Experiment—NFS DEB 12-56004; Jornada—NSF DEB-0618210; Konza Prairie and Kruger National Park—NSF DEB 0841917; Kruger National Park—NSF DEB 1712786.

Author information

Author notes

    • Ayana Angassa

    Present address: Department of Animal Science and Production, Botswana University of Agriculture and Natural Resources, Gaborone, Botswana

    • Dan G. Milchunas

    Present address: PO Box 943, LaPorte, CO, USA

Affiliations

  1. Department of Biology, University of North Carolina at Greensboro, Greensboro, NC, USA

    • Sally E. Koerner
  2. Department of Biology and Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO, USA

    • Melinda D. Smith
    • , Alan K. Knapp
    •  & Nathan P. Lemoine
  3. Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA, USA

    • Deron E. Burkepile
  4. Jornada LTER Program & Plant and Environmental Sciences Department, New Mexico State University, Las Cruces, NM, USA

    • Niall P. Hanan
  5. Department of Earth and Planetary Sciences, Johns Hopkins University, Baltimore, MD, USA

    • Meghan L. Avolio
  6. Department of Biology, University of New Mexico, Albuquerque, NM, USA

    • Scott L. Collins
    •  & Lauren E. Baur
  7. Department of Viticulture and Enology, University of California, Davis, Davis, CA, USA

    • Elisabeth J. Forrestel
  8. Department of Marine and Environmental Sciences, Northeastern University, Boston, MA, USA

    • Stephanie Eby
  9. South African Environmental Observation Network, Ndlovu Node, Scientific Services, Kruger National Park, Phalaborwa, South Africa

    • Dave I. Thompson
  10. School of Geography, Archaeology, and Environmental Studies, University of the Witwatersrand, Johannesburg, South Africa

    • Dave I. Thompson
  11. Tecnológico Nacional de México/I.T. Roque, Celaya, Mexico

    • Gerardo A. Aguado-Santacruz
  12. Jornada Basin LTER Program, New Mexico State University, Las Cruces, NM, USA

    • John P. Anderson
  13. Department of Biology, Wake Forest University, Winston-Salem, NC, USA

    • T. Michael Anderson
  14. School of Animal and Range Sciences, Hawassa University, Hawassa, Ethiopia

    • Ayana Angassa
  15. Centre for Ecological Sciences, Indian Institute of Science, Bangalore, India

    • Sumanta Bagchi
  16. Department of Aquatic Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands

    • Elisabeth S. Bakker
  17. Alice Springs, Northern Territory, Australia

    • Gary Bastin
  18. Department of Wildland Resources and Ecology Center, Utah State University, Logan, UT, USA

    • Karen H. Beard
    • , Andrew Kulmatiski
    • , Kyle C. Nehring
    •  & Kari E. Veblen
  19. U.S. Geological Survey, Northern Rocky Mountain Science Center, Bozeman, MT, USA

    • Erik A. Beever
  20. Department of Ecology, Montana State University, Bozeman, MT, USA

    • Erik A. Beever
  21. Department of Biology, University of Central Florida, Orlando, FL, USA

    • Patrick J. Bohlen
  22. Archbold Biological Station, MacArthur Agro-ecology Research Center, Venus, FL, USA

    • Elizabeth H. Boughton
  23. UCSB Kenneth S. Norris Rancho Marino Reserve, Cambria, CA, USA

    • Don Canestro
  24. INTA Cuenca del Salado, Grupo de Producción Vegetal, Rauch, Buenos Aires, Argentina

    • Ariela Cesa
  25. IFEVA-CONICET, Facultad de Agronomía, Universidad de Buenos Aires, Buenos Aires, Argentina

    • Enrique Chaneton
  26. State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Yangling, China

    • Jimin Cheng
    •  & Liang Guo
  27. Environmental Studies, University of California, Santa Barbara, CA, USA

    • Carla M. D’Antonio
  28. Université Grenoble Alpes, Irstea, UR LESSEM, Saint-Martin-d’Hères, France

    • Claire Deleglise
    •  & Gregory Loucougaray
  29. Institut Polytechnique Rural/Institut de Formation et de Recherche Appliquee, Katibougou, Mali

    • Fadiala Dembélé
  30. Ecosystem Mangement Science, Science Division, NSW Office of Environment and Heritage, Merimbula, New South Wales, Australia

    • Josh Dorrough
  31. Centre for Ecosystem Studies, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, Australia

    • David J. Eldridge
  32. Brackenridge Field Laboratory, University of Texas, Austin, TX, USA

    • Barbara Fernandez-Going
  33. Island Ecology and Biogeography Group, Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias, Universidad de La Laguna, La Laguna, Canary Islands, Spain

    • Silvia Fernández-Lugo
  34. Department of Natural Resource Sciences, Thompson Rivers University, Kamloops, British Columbia, Canada

    • Lauchlan H. Fraser
  35. Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada

    • Bill Freedman
    •  & Gonzalo García-Salgado
  36. Department of Zoology and Physiology, University of Wyoming, Laramie, WY, USA

    • Jacob R. Goheen
  37. New Zealand Forest Surveys, Napier, New Zealand

    • Sean Husheer
  38. Université des Sciences, des Techniques et des Technologies (USTTB), Bamako, Mali

    • Moussa Karembé
  39. School of Biological Sciences, University of Nebraska, Lincoln, NE, USA

    • Johannes M. H. Knops
  40. School of Natural Resource Management, Nelson Mandela University, George, South Africa

    • Tineke Kraaij
  41. Department of Biological and Environmental Sciences, University of Jyväskylä, Jyväskylä, Finland

    • Minna-Maarit Kytöviita
  42. Facultad de Agronomía, Universidad de la República, Montevideo, Uruguay

    • Felipe Lezama
  43. CERZOS-CONICET and Departamento de Biología, Bioquímica y Farmacia, UNS, Bahía Blanca, Argentina

    • Alejandro Loydi
  44. Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, CO, USA

    • Dan G. Milchunas
  45. South African Environmental Observation Network: Arid Lands Node, Prince Albert, South Africa

    • Suzanne J. Milton
  46. Department of Ecology, Environment and Evolution, La Trobe University, Bundoora, Victoria, Australia

    • John W. Morgan
  47. Arthur Rylah Institute, Department of Environment, Land, Water and Planning, Heidelberg, Victoria, Australia

    • Claire Moxham
  48. Conservation Ecology Group, University of Groningen, Groningen, The Netherlands

    • Han Olff
  49. Department of Biology, University of Florida, Gainesville, FL, USA

    • Todd M. Palmer
  50. Department of Life Sciences, University of Alcalá, Alcalá de Henares, Spain

    • Salvador Rebollo
  51. The Nature Conservancy, Lander, WY, USA

    • Corinna Riginos
  52. Research Unit Community Ecology, Swiss Federal Institute for Forest, Snow and Landscape Research, Birmensdorf, Switzerland

    • Anita C. Risch
    • , Martin Schütz
    •  & Martijn L. Vandegehuchte
  53. Department of Conservation Biology, Estación Biológica de Doñana CSIC, Sevilla, Spain

    • Marta Rueda
  54. School of Biology, University of Leeds, Leeds, UK

    • Mahesh Sankaran
  55. National Centre for Biological Sciences, Tata Institute of Fundamental Research, GKVK Campus, Bangalore, India

    • Mahesh Sankaran
    •  & Yadugiri V. Tiruvaimozhi
  56. Graduate School of Environment and Information Sciences, Yokohama National University, Yokohama, Japan

    • Takehiro Sasaki
  57. U.S. Geological Survey, Fort Collins Science Center and Colorado State University, Fort Collins, CO, USA

    • Kathryn A. Schoenecker
  58. School of Applied and Biomedical Science, Federation University, Ballarat, Victoria, Australia

    • Nick L. Schultz
  59. Department of Biology, Technische Universität Darmstadt, Darmstadt, Germany

    • Angelika Schwabe
    •  & Christian Storm
  60. Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa

    • Frances Siebert
  61. Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands

    • Christian Smit
  62. University of Wisconsin Green Bay, Natural and Applied Sciences, Green Bay, WI, USA

    • Karen A. Stahlheber
  63. USDA-ARS, Fort Keogh Livestock and Range Research Laboratory, Miles City, MT, USA

    • Dustin J. Strong
    •  & Lance T. Vermeire
  64. College of Animal Science and Technology, Northwest A&F University, Yangling, China

    • Jishuai Su
  65. Earth Research Institute, University of California, Santa Barbara, CA, USA

    • Claudia Tyler
  66. Office of Environment and Heritage, Buronga, New South Wales, Australia

    • James Val
  67. Terrestrial Ecology Unit, Department of Biology, Ghent University, Ghent, Belgium

    • Martijn L. Vandegehuchte
  68. Department of Biological Sciences, Kent State University, Kent, OH, USA

    • David Ward
  69. Lhasa National Ecological Research Station, Key Laboratory of Ecosystem Network Observation and Modelling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, China

    • Jianshuang Wu
  70. Department of Plant Sciences, University of California, Davis, Davis, CA, USA

    • Truman P. Young
  71. Mpala Research Centre, Nanyuki, Kenya

    • Truman P. Young
  72. National Hulunber Grassland Ecosystem Observation and Research Station/Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, China

    • Qiang Yu
  73. Department of Botany, University of Wyoming, Laramie, WY, USA

    • Tamara Jane Zelikova

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Contributions

S.E.K. managed the project including conceptualizing the questions, collecting and analysing the data, developing the figures and writing the manuscript. M.D.S. conceptualized the questions and wrote the manuscript. D.E.B. conceptualized the questions, collected the data and wrote the manuscript. N.P.H. performed simulations and wrote the manuscript. M.L.A. and N.P.L. executed the path analyses and developed the figures. S.L.C. and A.K.K. wrote the manuscript. S.E., E.J.F. and D.I.T. contributed to data collection and management. S.E.K., M.D.S., D.E.B., N.P.H., M.L.A., S.L.C., A.K.K., N.P.L., E.J.F., S.E. and D.I.T. attended multiple working groups to complete this manuscript while all other co-authors contributed data to the synthesis; all authors (both members of the working group and not) edited the manuscript. See the author contribution table (Supplementary Table 11) for a complete list of contributions.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Sally E. Koerner.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–4 and Supplementary Tables 1–10

  2. Reporting Summary

  3. Supplementary Table 11

    Detailed list of author contributions

About this article

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DOI

https://doi.org/10.1038/s41559-018-0696-y