Ant handling changes myrmecochore seed coat microbiomes and alters diversity of seed-borne plant pathogenic fungi

Chloe L. Lash, Melissa A. Cregger, Anne M. Kinkopf, Nicole Buerger, Dawn M. Klingeman, Charles Kwit

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

The putative benefits to seeds in myrmecochory (ant-mediated seed dispersal) are often cast in a reward context. However, microbes have been mostly overlooked as seed mortality agents in myrmecochory, as have potential treatments provided by ant-handling. We investigated the effects of ant handling on the diversity of seed coat fungal communities of three myrmecochorous plant species. Ant-handling altered measures of both alpha and beta diversity of fungal communities. Ant-handled seeds harboured different overall fungal communities and plant pathogen communities than non-ant-handled seeds. The myrmecochore pathogenic fungal community showed high dissimilarity (high pairwise community turnover) between ant-handled and control seeds, while beta diversity measures for ant-handled seeds and seeds with manually removed elaiosomes were less dissimilar. Ant handling may offer an additional benefit to myrmecochorous seeds via the reduction in the seed coat pathogenic community, which may be driven by elaiosome removal or as a by-product of ant cleaning behaviours and chemical secretions. Read the free Plain Language Summary for this article on the Journal blog.

Original languageEnglish
Pages (from-to)861-874
Number of pages14
JournalFunctional Ecology
Volume38
Issue number4
DOIs
StatePublished - Apr 2024

Funding

Ant and seed collections were done with permits through The Nature Conservancy and the Virginia Department of Conservation and Recreation's Natural Heritage Program. Thanks to Ryan Klopf for assistance with field site access and Steve and Carol Croy for allowing us to collect fruits from their property. Samantha Kisare, Samantha Sturiale, Kane Lawhorn, Bruce Martin, Henry Davie, Austin Davis, and Jamie Albert assisted with collections. Thanks to Kimberly Gwinn, James Fordyce, and Kimberly Sheldon for suggestions on earlier versions of this manuscript. Thanks to James Fordyce and Samuel Borstein for assistance with statistical analysis and Stephanie Kivlin for assistance with preliminary trials. Chloe Lash was supported by The Lewis and Clark Fund for Exploration and Field Research from the American Philosophical Society, and the Horton H Hobbs and Johns Creek Endowment Funds through Mountain Lake Biological Station. Anne Kinkopf and Nicole Buerger were supported through the University of Tennessee Institute of Agriculture's Explore BiGG Data REEU (Research and Extension Experiential Learning for Undergraduates, funded by the United States Department of Agriculture) under the direction of Dr. Kimberly Gwinn. Dawn Klingeman and Melissa Cregger were supported in this collaboration by the Genomic Science Program, United States Department of Energy, Office of Science, Biological and Environmental Research, as part of the Plant Microbe Interfaces Scientific Focus Area at ORNL (Oak Ridge National Laboratory is managed by UT\u2010Battelle, LLC, for the United States Department of Energy under contract DEAC05\u201000OR22725.) under the direction of Dr. Kimberly Gwinn. Ant and seed collections were done with permits through The Nature Conservancy and the Virginia Department of Conservation and Recreation's Natural Heritage Program. Thanks to Ryan Klopf for assistance with field site access and Steve and Carol Croy for allowing us to collect fruits from their property. Samantha Kisare, Samantha Sturiale, Kane Lawhorn, Bruce Martin, Henry Davie, Austin Davis, and Jamie Albert assisted with collections. Thanks to Kimberly Gwinn, James Fordyce, and Kimberly Sheldon for suggestions on earlier versions of this manuscript. Thanks to James Fordyce and Samuel Borstein for assistance with statistical analysis and Stephanie Kivlin for assistance with preliminary trials. Chloe Lash was supported by The Lewis and Clark Fund for Exploration and Field Research from the American Philosophical Society, and the Horton H Hobbs and Johns Creek Endowment Funds through Mountain Lake Biological Station. Anne Kinkopf and Nicole Buerger were supported through the University of Tennessee Institute of Agriculture's Explore BiGG Data REEU (Research and Extension Experiential Learning for Undergraduates, funded by the United States Department of Agriculture) under the direction of Dr. Kimberly Gwinn. Dawn Klingeman and Melissa Cregger were supported in this collaboration by the Genomic Science Program, United States Department of Energy, Office of Science, Biological and Environmental Research, as part of the Plant Microbe Interfaces Scientific Focus Area at ORNL (Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the United States Department of Energy under contract DEAC05-00OR22725.) under the direction of Dr. Kimberly Gwinn.

FundersFunder number
Horton H Hobbs and Johns Creek Endowment Funds
Biological and Environmental Research
U.S. Department of Energy
Virginia Department of Conservation and Recreation's Natural Heritage Program
Office of Science
Institute of Agriculture, University of Tennessee
U.S. Department of Agriculture
American Philosophical Society
Oak Ridge National LaboratoryDEAC05‐00OR22725

    Keywords

    • ant–plant–fungal interaction
    • microbiome
    • myrmecochory
    • plant pathogens
    • seed dispersal

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