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Plant susceptibility to a shared herbivore is reduced by belowground competition with neighbors

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Abstract

Spatial variation in plant community composition is an important driver of variation in susceptibility to herbivores. In close proximity, certain neighbors can attract or repel herbivores to a focal plant (“associational effects”). Neighboring plants may also compete for resources, modifying their phenotype in ways that affect susceptibility to herbivores. To test whether and how competition contributes to associational effects, we manipulated the sharing of belowground resources among plant neighbors (spotted Joe Pye weed and common boneset) that serve as alternate hosts for an herbivorous beetle. In the field, the beetle Ophraella notata laid more eggs and inflicted more damage on plants of both species that were released from belowground competition with neighbors. Competition also weakened the effects of neighbor identity during field trials, reducing associational susceptibility. When beetles were forced to choose between the two host species in cage trials, competition again reduced beetle use of Joe Pye weed as a secondary host. To test the role of plant traits related to herbivore defense and nutrition, we quantified leaf protein, specific leaf area, and trichomes, and conducted behavioral assays on leaf disks. Beetles did not distinguish between Joe Pye weed treatments at the leaf disk level, and competition did not impact specific leaf area and protein. Trichome density was higher in both species in the preferred treatment. Overall, our results suggest that belowground interactions between plants may mediate the strength of associational effects, as secondary hosts become more attractive when released from competition with primary host plants.

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Data availability

Study data are available from the corresponding author on reasonable request.

Code availability

Code used in analysis is available from the corresponding author on reasonable request.

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Acknowledgements

The authors would like to thank Tyler Coverdale for helpful feedback on the experimental design, Amy Hastings for assistance with leaf trait analysis methods, and undergraduate researcher Lei Lei Wu for her help with experimental setup and data collection.

Funding

Experiments were funded by the Cornell Andrew W. Mellon Student Research Grant and the Paul P. Feeny Graduate Student Research Fund.

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  1. Katherine D. Holmes

    Present address: Binghamton University, Binghamton, USA

Authors and Affiliations

  1. Cornell University, Ithaca, USA

    Katherine D. Holmes, Erika L. Mudrak & Alison G. Power

  2. University of Massachusetts Amherst, Amherst, USA

    Zoe L. Getman-Pickering

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Contributions

KH formulated the research question and developed the experimental design with EM. Experiments were performed by KH, with leaf tissue analyses contributed by ZG-P. Data analysis was performed by KH under the guidance of EM and AGP. KH and AGP wrote the manuscript, with feedback from EM and ZG-P.

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Correspondence to Katherine D. Holmes.

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Additional information

Communicated by Merijn Kant.

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Supplementary file1 (DOCX 767 KB)

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Holmes, K.D., Getman-Pickering, Z.L., Mudrak, E.L. et al. Plant susceptibility to a shared herbivore is reduced by belowground competition with neighbors. Oecologia 203, 113–124 (2023). https://doi.org/10.1007/s00442-023-05454-2

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