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Dilution of specialist pathogens drives productivity benefits from diversity in plant mixtures

Author

Listed:
  • Guangzhou Wang

    (National Academy of Agriculture Green Development, China Agricultural University
    University of Kansas)

  • Haley M. Burrill

    (University of Kansas
    University of Kansas
    University of Oregon)

  • Laura Y. Podzikowski

    (University of Kansas
    University of Kansas)

  • Maarten B. Eppinga

    (University of Zurich)

  • Fusuo Zhang

    (National Academy of Agriculture Green Development, China Agricultural University)

  • Junling Zhang

    (National Academy of Agriculture Green Development, China Agricultural University)

  • Peggy A. Schultz

    (University of Kansas
    University of Kansas)

  • James D. Bever

    (University of Kansas
    University of Kansas)

Abstract

Productivity benefits from diversity can arise when compatible pathogen hosts are buffered by unrelated neighbors, diluting pathogen impacts. However, the generality of pathogen dilution has been controversial and rarely tested within biodiversity manipulations. Here, we test whether soil pathogen dilution generates diversity- productivity relationships using a field biodiversity-manipulation experiment, greenhouse assays, and feedback modeling. We find that the accumulation of specialist pathogens in monocultures decreases host plant yields and that pathogen dilution predicts plant productivity gains derived from diversity. Pathogen specialization predicts the strength of the negative feedback between plant species in greenhouse assays. These feedbacks significantly predict the overyielding measured in the field the following year. This relationship strengthens when accounting for the expected dilution of pathogens in mixtures. Using a feedback model, we corroborate that pathogen dilution drives overyielding. Combined empirical and theoretical evidence indicate that specialist pathogen dilution generates overyielding and suggests that the risk of losing productivity benefits from diversity may be highest where environmental change decouples plant-microbe interactions.

Suggested Citation

  • Guangzhou Wang & Haley M. Burrill & Laura Y. Podzikowski & Maarten B. Eppinga & Fusuo Zhang & Junling Zhang & Peggy A. Schultz & James D. Bever, 2023. "Dilution of specialist pathogens drives productivity benefits from diversity in plant mixtures," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-44253-4
    DOI: 10.1038/s41467-023-44253-4
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    1. Ylva Lekberg & Carlos A. Arnillas & Elizabeth T. Borer & Lorinda S. Bullington & Noah Fierer & Peter G. Kennedy & Jonathan W. Leff & Angela D. Luis & Eric W. Seabloom & Jeremiah A. Henning, 2021. "Nitrogen and phosphorus fertilization consistently favor pathogenic over mutualistic fungi in grassland soils," Nature Communications, Nature, vol. 12(1), pages 1-8, December.
    2. Markus Lange & Nico Eisenhauer & Carlos A. Sierra & Holger Bessler & Christoph Engels & Robert I. Griffiths & Perla G. Mellado-Vázquez & Ashish A. Malik & Jacques Roy & Stefan Scheu & Sibylle Steinbei, 2015. "Plant diversity increases soil microbial activity and soil carbon storage," Nature Communications, Nature, vol. 6(1), pages 1-8, November.
    3. Forest Isbell & Vincent Calcagno & Andy Hector & John Connolly & W. Stanley Harpole & Peter B. Reich & Michael Scherer-Lorenzen & Bernhard Schmid & David Tilman & Jasper van Ruijven & Alexandra Weigel, 2011. "High plant diversity is needed to maintain ecosystem services," Nature, Nature, vol. 477(7363), pages 199-202, September.
    4. Ingrid M. Parker & Megan Saunders & Megan Bontrager & Andrew P. Weitz & Rebecca Hendricks & Roger Magarey & Karl Suiter & Gregory S. Gilbert, 2015. "Phylogenetic structure and host abundance drive disease pressure in communities," Nature, Nature, vol. 520(7548), pages 542-544, April.
    5. Manuel Delgado-Baquerizo & Carlos A. Guerra & Concha Cano-Díaz & Eleonora Egidi & Jun-Tao Wang & Nico Eisenhauer & Brajesh K. Singh & Fernando T. Maestre, 2020. "The proportion of soil-borne pathogens increases with warming at the global scale," Nature Climate Change, Nature, vol. 10(6), pages 550-554, June.
    6. Michel Loreau & Andy Hector, 2001. "Partitioning selection and complementarity in biodiversity experiments," Nature, Nature, vol. 412(6842), pages 72-76, July.
    7. Calcagno, Vincent & de Mazancourt, Claire, 2010. "glmulti: An R Package for Easy Automated Model Selection with (Generalized) Linear Models," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 34(i12).
    8. Felicia Keesing & Lisa K. Belden & Peter Daszak & Andrew Dobson & C. Drew Harvell & Robert D. Holt & Peter Hudson & Anna Jolles & Kate E. Jones & Charles E. Mitchell & Samuel S. Myers & Tiffany Bogich, 2010. "Impacts of biodiversity on the emergence and transmission of infectious diseases," Nature, Nature, vol. 468(7324), pages 647-652, December.
    9. Scott A. Mangan & Stefan A. Schnitzer & Edward A. Herre & Keenan M. L. Mack & Mariana C. Valencia & Evelyn I. Sanchez & James D. Bever, 2010. "Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest," Nature, Nature, vol. 466(7307), pages 752-755, August.
    10. Michel Loreau & Andy Hector, 2001. "Erratum: Partitioning selection and complementarity in biodiversity experiments," Nature, Nature, vol. 413(6855), pages 548-548, October.
    Full references (including those not matched with items on IDEAS)

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