Abstract
Plants link interactions between aboveground and belowground organisms. Herbivore-induced changes in plant chemistry are hypothesized to impact entire food webs by changing the strength of trophic cascades. Yet, few studies have explored how belowground herbivores affect the behaviors of generalist predators, nor how such changes may act through diverse changes to the plant metabolome. Using a factorial experiment, we tested whether herbivory by root-knot nematodes (Meloidogyne incognita) affected the aboveground interaction among milkweed plants (Asclepias fascicularis or Asclepias speciosa), oleander aphids (Aphis nerii), and aphid-tending ants (Linepithema humile). We quantified the behaviors of aphid-tending ants, and we measured the effects of herbivore treatments on aphid densities and on phytochemistry. Unexpectedly, ants tended aphids primarily on the leaves of uninfected plants, whereas ants tended aphids primarily at the base of the stem of nematode-infected plants. In nematode-infected plants, aphids excreted more sugar per capita in their ant-attracting honeydew. Additionally, although plant chemistry was species-specific, nematode infection generally decreased the richness of plant secondary metabolites while acting as a protein sink in the roots. Path analysis indicated that the ants’ behavioral change was driven in part by indirect effects of nematodes acting through changes in plant chemistry. We conclude that belowground herbivores can affect the behaviors of aboveground generalist ant predators by multiple paths, including changes in phytochemistry, which may affect the attractiveness of aphid honeydew rewards.
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All data and corresponding R code will be archived in Dryad https://doi.org/10.5061/dryad.wm37pvmkv
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Acknowledgements
We are deeply indebted to Michael Reichelt (MPICE, Jena, Germany) for helping us to think broadly about milkweed chemistry. We also thank Sybille Lorenz (MPICE, Jena, Germany) for analyzing our samples by UHPLC-ESI-HRMS, and we thank the members of the Pringle Lab, the Plant-Insect Group (“PIG”) at UNR, and three anonymous reviewers for their constructive comments on the manuscript. EGP was funded by an Alexander von Humboldt Fellowship, and both authors were funded by the University of Nevada, Reno.
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FMM and EGP conceived and designed the experiments. FMM performed the experiments. FMM and EGP analyzed and interpreted the data and wrote the manuscript.
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Communicated by Colin Mark Orians.
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Mundim, F.M., Pringle, E.G. Phytochemistry-mediated disruption of ant–aphid interactions by root-feeding nematodes. Oecologia 194, 441–454 (2020). https://doi.org/10.1007/s00442-020-04777-8
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DOI: https://doi.org/10.1007/s00442-020-04777-8