Herbivore-induced volatile emissions are altered by soil legacy effects in cereal cropping systems

Shealyn C. Malone,Megan L. Hofland,Justin B. Runyon,Fabian D. Menalled,Amy M. Trowbridge,David K. Weaver,Tim F. Seipel

doi:10.1007/s11104-020-04674-2

Abstract

Aims (main purpose and research question)Soil properties, including microbial composition and nutrient availability, can influence the emissions of plant volatile organic compounds (VOCs) that serve as host-location cues for insect pests and their natural enemies. Agricultural practices have profound effects on soil properties, but how these influence crop VOCs remains largely unknown. The aim of this study was to investigate the effect of agricultural practices on constitutive and herbivore-induced VOC emissions by a major staple crop through soil legacy effects.MethodsIn a full factorial experiment, we measured VOC emissions by wheat (Triticum aestivum) grown in soil inoculum from wheat-fallow or wheat-cover crop rotations that was subjected to feeding by larval Cephus cinctus.Results (main findings)Under herbivory, plants grown in cover crop inoculum emitted greater total VOCs, including higher concentrations of 2-pentadecanone, an insect repellent, and nonanal, a compound important in the recruitment of natural enemies. Plants grown in fallow inoculum showed no differences in emissions whether under herbivory or not. Soil inoculum did not influence VOC emissions of plants in the absence of larval feeding.ConclusionsThese results suggest that agricultural practices influence crop VOC emissions through soil legacy effects. Additionally, crops grown in wheat-fallow rotations may be less successful recruiting natural enemies of pests through herbivore-induced VOC signaling.AbbreviationsVolatile organic compounds (VOCs); herbivore-induced plant volatiles (HIPV); green leaf volatiles (GLVs); northern Great Plains (NGP); wheat stem sawfly (WSS); gas chromatography-mass spectrometry (GC-MS); non-metric multidimensional scaling (NMDS); generalized linear mixed-effects model (GLMM).

Highlights

Plant volatile organic compounds (VOCs) have multiple ecological roles including attracting pollinators, acting as cues for foraging herbivores, and functioning as direct and indirect defense against herbivores (Dudareva et al 2013; Heil 2014; Heil and Karban 2010; Parachnowitsch and Manson 2015)
Soil inoculum did not influence VOC emissions of plants in the absence of larval feeding. These results suggest that agricultural practices influence crop VOC emissions through soil legacy effects
The overall VOC composition varied in response to the interaction of soil inoculum and larval feeding (PERMANOVA Infestation x Soil: F1, 104 = 2.91, P = 0.034), though it only explained a small amount of variation among treatments (R2 = 0.03)

Summary

Introduction

Plant volatile organic compounds (VOCs) have multiple ecological roles including attracting pollinators, acting as cues for foraging herbivores, and functioning as direct and indirect defense against herbivores (Dudareva et al 2013; Heil 2014; Heil and Karban 2010; Parachnowitsch and Manson 2015). Given their central role in mediating plant-insect interactions, it is no surprise that many forms of pest management employ plant VOCs to influence the behavior of pests and their natural enemies (Pickett and Khan 2016; Shrivastava et al 2010). Exciting evidence suggests that pest management utilizing plant volatiles can be applied to existing farming practices through the concept of plant-soil feedbacks (Kaplan et al 2018; Mutyambai et al 2019)

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