IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-44253-4.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44253-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-44253-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. Michel Loreau & Andy Hector, 2001. "Partitioning selection and complementarity in biodiversity experiments," Nature, Nature, vol. 412(6842), pages 72-76, July.
    3. 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).
    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. 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.
    6. 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.
    7. 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.
    8. 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.
    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)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Luiz A. Domeignoz-Horta & Seraina L. Cappelli & Rashmi Shrestha & Stephanie Gerin & Annalea K. Lohila & Jussi Heinonsalo & Daniel B. Nelson & Ansgar Kahmen & Pengpeng Duan & David Sebag & Eric Verrecc, 2024. "Plant diversity drives positive microbial associations in the rhizosphere enhancing carbon use efficiency in agricultural soils," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Cameron Wagg & Christiane Roscher & Alexandra Weigelt & Anja Vogel & Anne Ebeling & Enrica Luca & Anna Roeder & Clemens Kleinspehn & Vicky M. Temperton & Sebastian T. Meyer & Michael Scherer-Lorenzen , 2022. "Biodiversity–stability relationships strengthen over time in a long-term grassland experiment," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Chun-Wei Chang & Takeshi Miki & Hao Ye & Sami Souissi & Rita Adrian & Orlane Anneville & Helen Agasild & Syuhei Ban & Yaron Be’eri-Shlevin & Yin-Ru Chiang & Heidrun Feuchtmayr & Gideon Gal & Satoshi I, 2022. "Causal networks of phytoplankton diversity and biomass are modulated by environmental context," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Liting Zheng & Kathryn E. Barry & Nathaly R. Guerrero-Ramírez & Dylan Craven & Peter B. Reich & Kris Verheyen & Michael Scherer-Lorenzen & Nico Eisenhauer & Nadia Barsoum & Jürgen Bauhus & Helge Bruel, 2024. "Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Maria Pergola & Enrica De Falco & Michele Cerrato, 2024. "Grassland Ecosystem Services: Their Economic Evaluation through a Systematic Review," Land, MDPI, vol. 13(8), pages 1-21, July.
    6. Sarah R. Weiskopf & Forest Isbell & Maria Isabel Arce-Plata & Moreno Di Marco & Mike Harfoot & Justin Johnson & Susannah B. Lerman & Brian W. Miller & Toni Lyn Morelli & Akira S. Mori & Ensheng Weng &, 2024. "Biodiversity loss reduces global terrestrial carbon storage," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    7. Garba, Ismail I. & Bell, Lindsay W. & Chauhan, Bhagirath S. & Williams, Alwyn, 2024. "Optimizing ecosystem function multifunctionality with cover crops for improved agronomic and environmental outcomes in dryland cropping systems," Agricultural Systems, Elsevier, vol. 214(C).
    8. Gabriela Woźniak & Monika Malicka & Jacek Kasztowski & Łukasz Radosz & Joanna Czarnecka & Jaco Vangronsveld & Dariusz Prostański, 2022. "How Important Are the Relations between Vegetation Diversity and Bacterial Functional Diversity for the Functioning of Novel Ecosystems?," Sustainability, MDPI, vol. 15(1), pages 1-16, December.
    9. Yuxin Liu & Chenjing Fan & Dongdong Xue, 2024. "A Review of the Effects of Urban and Green Space Forms on the Carbon Budget Using a Landscape Sustainability Framework," Sustainability, MDPI, vol. 16(5), pages 1-29, February.
    10. Jonathan S. Lefcheck & Graham J. Edgar & Rick D. Stuart-Smith & Amanda E. Bates & Conor Waldock & Simon J. Brandl & Stuart Kininmonth & Scott D. Ling & J. Emmett Duffy & Douglas B. Rasher & Aneil F. A, 2021. "Species richness and identity both determine the biomass of global reef fish communities," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    11. D. G. Kapayou & E. M. Herrighty & C. Gish Hill & V. Cano Camacho & A. Nair & D. M. Winham & M. D. McDaniel, 2023. "Reuniting the Three Sisters: collaborative science with Native growers to improve soil and community health," Agriculture and Human Values, Springer;The Agriculture, Food, & Human Values Society (AFHVS), vol. 40(1), pages 65-82, March.
    12. Chuangang Gong & Dazhi Ni & Yuna Liu & Yalei Li & Qingmei Huang & Yu Tian & Hao Zhang, 2024. "Herbaceous Vegetation in Slope Stabilization: A Comparative Review of Mechanisms, Advantages, and Practical Applications," Sustainability, MDPI, vol. 16(17), pages 1-18, September.
    13. Barbara Emmenegger & Julien Massoni & Christine M. Pestalozzi & Miriam Bortfeld-Miller & Benjamin A. Maier & Julia A. Vorholt, 2023. "Identifying microbiota community patterns important for plant protection using synthetic communities and machine learning," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    14. György Barabás & Christine Parent & Andrew Kraemer & Frederik Perre & Frederik Laender, 2022. "The evolution of trait variance creates a tension between species diversity and functional diversity," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    15. Ulrich, Werner & Gotelli, Nicholas J. & Strona, Giovanni & Godsoe, William, 2024. "Reconsidering the Price equation: Benchmarking the analytical power of additive partitioning in ecology," Ecological Modelling, Elsevier, vol. 491(C).
    16. Douglas Toledo & Cristiane Akemi Umetsu & Antonio Fernando Monteiro Camargo & Idemauro Antonio Rodrigues Lara, 2022. "Flexible models for non-equidispersed count data: comparative performance of parametric models to deal with underdispersion," AStA Advances in Statistical Analysis, Springer;German Statistical Society, vol. 106(3), pages 473-497, September.
    17. Sergei Schaub & Nadja El Benni, 2024. "How do price (risk) changes influence farmers’ preferences to reduce fertilizer application?," Agricultural Economics, International Association of Agricultural Economists, vol. 55(2), pages 365-383, March.
    18. Gaowen Yang & Masahiro Ryo & Julien Roy & Daniel R. Lammel & Max-Bernhard Ballhausen & Xin Jing & Xuefeng Zhu & Matthias C. Rillig, 2022. "Multiple anthropogenic pressures eliminate the effects of soil microbial diversity on ecosystem functions in experimental microcosms," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    19. Huang, Wei & Manevska-Tasevska, Gordana & Hansson, Helena, 2024. "Does ecologization matter for technical efficiency in crop production? A case of Swedish agriculture," Land Use Policy, Elsevier, vol. 138(C).
    20. Voinson, Marina & Smadi, Charline & Billiard, Sylvain, 2022. "How does the host community structure affect the epidemiological dynamics of emerging infectious diseases?," Ecological Modelling, Elsevier, vol. 472(C).

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-44253-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.