title: A mechanism for sequence specificity in plant-mediated interactions between herbivores.
abstract: Herbivore communities are shaped by indirect plant-mediated interactions whose outcomes are strongly dependent on the sequence of herbivore arrival. However, the mechanisms underlying sequence specificity are poorly understood. We examined the mechanisms that govern sequence-specific effects of the interaction between two specialist maize herbivores, the leaf feeder Spodoptera frugiperda and the root feeder Diabrotica virgifera virgifera. In the field, S. frugiperda reduces D. v. virgifera abundance, but only when it arrives on the plant first. In behavioral experiments, D. v. virgifera larvae continued feeding on plants that they had infested before leaf infestation, but refused to initiate feeding on plants that were infested by S. frugiperda before their arrival. Changes in root-emitted volatiles were sufficient to elicit this sequence-specific behavior. Root volatile and headspace mixing experiments showed that early-arriving D. v. virgifera larvae suppressed S. frugiperda-induced volatile repellents, which led to the maintenance of host attractiveness to D. v. virgifera. Our study provides a physiological and behavioral mechanism for sequence specificity in plant-mediated interactions and suggests that physiological canalization of behaviorally active metabolites can drive sequence specificity and result in strongly diverging herbivore distribution patterns.
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, Bern, 3013, Switzerland.
authors.forename: Wei
authors.initials: W
authors.lastname: Huang
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, Bern, 3013, Switzerland.
authors.forename: Christelle A M
authors.initials: CA
authors.lastname: Robert
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, Bern, 3013, Switzerland.|INRA, UMR1349 IGEPP, Le Rheu, F-35653, France.
authors.forename: Maxime R
authors.initials: MR
authors.lastname: Hervé
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, Bern, 3013, Switzerland.
authors.forename: Lingfei
authors.initials: L
authors.lastname: Hu
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, Bern, 3013, Switzerland.
authors.forename: Zoe
authors.initials: Z
authors.lastname: Bont
authors.affiliation: Institute of Plant Sciences, University of Bern, Altenbergrain 21, Bern, 3013, Switzerland.
authors.forename: Matthias
authors.initials: M
authors.lastname: Erb
mesh_terms: D000818:Animals; D001517:Coleoptera / Q000502:physiology*; D005246:Feedback; D060434:Herbivory; D018517:Plant Roots / Q000378:metabolism; D010944:Plants / Q000469:parasitology*; D018411:Spodoptera / Q000502:physiology*; D055549:Volatile Organic Compounds / Q000032:analysis
chemical_list: D055549:Volatile Organic Compounds
keywords: 
  Diabrotica virgifera virgifera
  ; 
  Spodoptera frugiperda
  ; 
  Zea mays
  ; aboveground−belowground interactions; induced resistance; physiological canalization; plant-herbivore interactions; volatile organic compounds