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Conifer Monoterpene Chemistry during an Outbreak Enhances Consumption and Immune Response of an Eruptive Folivore

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Abstract

Changes in the chemical composition of plant defense compounds during herbivory can impact herbivore resource allocation patterns and thereby herbivore survival, growth, and immune response against endoparasitoid infection. Few studies have investigated folivore responses to changes in plant chemistry that occur under outbreak conditions in mature conifer systems. Using data from an earlier observational field study, we carried out laboratory bioassays to test how variation in monoterpenes in piñon pine trees (Pinus edulis, Pinaceae) during an outbreak affects growth, consumption, and immune response of a specialist herbivore, the Southwestern tiger moth (Lophocampa ingens, Arctiidae). Larvae were fed on artificial diets containing four monoterpenes at concentrations that mimicked those observed in undamaged and herbivore-damaged trees in situ during an outbreak. Damaged trees contained 30% lower total monoterpene concentrations, likely reflecting volatile losses as observed in a previous field study Trowbridge et al. (Ecology 95:1591–1603, Trowbridge et al. 2014). Herbivores reared on diets mimicking terpene concentrations in the needles of damaged trees exhibited an approximately 60% increase in consumption relative to larvae reared on diets characteristic of trees without herbivore damage. Higher consumption was accompanied by a 40% increase in immune response with no change in growth rate. These observations suggest preferential resource allocation towards immunity and/or a strong genetic component that determines growth under these conditions. These outcomes, which favor the herbivore, point to: (i) a potential positive feedback mechanism that may increase L. ingens’s chance of escaping parasitism during the early phases of an outbreak; and (ii) the important role of monoterpenes in mediating conifer-folivore interactions specifically for P. edulis, which has suffered large-scale drought-induced mortality events exacerbated by the presence of insects.

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Acknowledgements

Funding was provided by a University of Colorado Graduate School Beverly Sears Grant awarded to A. Trowbridge and NSF grant #0500560 to R. Monson and D. Bowers. We thank Caitlin Kelly for guidance with preparing artificial diets, Patricia Kazimier and Melissa Bernatis for their assistance with insect rearing, Jonathan Kleinman for his assistance with bead dissections and photographs, and Ken Keefover-Ring for GC-MS support. The manuscript was greatly improved by the comments of Paul Stoy, Carolina Quintero, Susan Whitehead, and Yan Linhart.

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA

    Amy M. Trowbridge, M. Deane Bowers & Russell K. Monson

  2. Department of Land Resources and Environmental Sciences, Montana State University, 334 Leon Johnson Hall, Bozeman, MT, 59717, USA

    Amy M. Trowbridge

  3. School of Natural Resources and the Environment and Laboratory of Tree Ring Research, University of Arizona, Tucson, AZ, 85721, USA

    Russell K. Monson

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  1. Amy M. Trowbridge
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  2. M. Deane Bowers
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Correspondence to Amy M. Trowbridge.

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Trowbridge, A.M., Bowers, M.D. & Monson, R.K. Conifer Monoterpene Chemistry during an Outbreak Enhances Consumption and Immune Response of an Eruptive Folivore. J Chem Ecol 42, 1281–1292 (2016). https://doi.org/10.1007/s10886-016-0797-5

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