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Intraspecific Variation in Plant Defense Alters Effects of Root Herbivores on Leaf Chemistry and Aboveground Herbivore Damage

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Abstract

Root herbivores can indirectly affect aboveground herbivores by altering the food quality of the plant. However, it is largely unknown whether plant genotypes differ in their response to root herbivores, leading to variable defensive phenotypes. In this study, we investigated whether root-feeding insect larvae (Agriotes sp. larvae, wireworms) induce different responses in Plantago lanceolata plants from lines selected for low and high levels of iridoid glycosides (IG). In the absence of wireworms, plants of the “high-IG line” contained approximately twofold higher levels of total IG and threefold higher levels of catalpol (one of the IG) in leaves than plants from the “low-IG line,” whereas both lines had similar levels of IG in roots. In response to wireworms, roots of plants from both lines showed increased concentrations of catalpol. Leaves of “low-IG line” plants increased catalpol concentrations in response to wireworms, whereas catalpol concentrations of leaves of “high-IG line” plants decreased. In contrast, glucose concentrations in roots of “low-IG” plants decreased, while they increased in “high-IG” plants after feeding by wireworms. The leaf volatile profile differed between the lines, but was not affected by root herbivores. In the field, leaf damage by herbivores was higher in wireworm-induced compared to noninduced “low-IG” plants and lower in wireworm-induced compared to noninduced “high-IG” plants, despite induction of catalpol in leaves of the “low-IG” plants and reduction in “high-IG” plants. This pattern might arise if damage is caused mainly by specialist herbivores for which catalpol may act as feeding stimulant rather than as deterrent. The present study documents for the first time that intraspecific variation in plant defense affects the outcome of plant-mediated interactions between root and shoot herbivores.

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Acknowledgments

We thank Wiecher Smant for analyzing plant N and C concentrations, Sander Van Beersum for determining the arbuscular mycorrhizal fungi colonization of the roots, and Kees Hordijk for the gas chromatography–mass spectrometry measurements. The study was financed by the EU-funded Marie-Curie training network BIORHIZ (“Biotic Interactions in the Rhizosphere as Structuring Forces for Plant Communities,” MRTN-CT-2003-505090). Publication 4324 Netherlands Institute of Ecology (NIOO-KNAW).

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Authors and Affiliations

  1. Netherlands Institute of Ecology (NIOO-KNAW), Centre for Terrestrial Ecology, P.O. Box 40, 6666 ZG, Heteren, The Netherlands

    Susanne Wurst, Nicole M. Van Dam, Arjen Biere & Wim H. Van der Putten

  2. Ökologie der Pflanzen, Freie Universität Berlin, Altensteinstr. 6, 14195, Berlin, Germany

    Susanne Wurst

  3. Departamento de Ecoloxía e Bioloxía Animal, Universidade de Vigo, E-36310, Vigo, Spain

    Fernando Monroy

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  1. Susanne Wurst
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  2. Nicole M. Van Dam
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  3. Fernando Monroy
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  4. Arjen Biere
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  5. Wim H. Van der Putten
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Correspondence to Susanne Wurst.

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Wurst, S., Van Dam, N.M., Monroy, F. et al. Intraspecific Variation in Plant Defense Alters Effects of Root Herbivores on Leaf Chemistry and Aboveground Herbivore Damage. J Chem Ecol 34, 1360–1367 (2008). https://doi.org/10.1007/s10886-008-9537-9

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