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Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals

Authors

  • Roxina Soler,

  • Jeffrey A. Harvey,

  • Andre F. D. Kamp,

  • Louise E. M. Vet,

  • Wim H. Van der Putten,

  • Nicole M. Van Dam,

  • Josef F. Stuefer,

  • Rieta Gols,

  • Cornelis A. Hordijk,

  • T. Martijn Bezemer


R. Soler (r.soler@nioo.knaw.nl), J. A. Harvey, A. F. D. Kamp, L. E. M. Vet, W. H. Van der Putten, N. M. Van Dam, and T. M. Bezemer, Dept of Multitrophic Interactions, Netherlands Institute of Ecology (NIOO-KNAW), P.O. Box 40, NL-6666 ZG Heteren, the Netherlands. – LEMV, TMB and R. Gols, Laboratory of Entomology, Wageningen Univ. and Research Centre, P.O. Box 8031, NL-6700 EH Wageningen, the Netherlands. – WHVP and TMB, Laboratory of Nematology, Wageningen Univ. and Research Centre, P.O. Box 8123, NL-6700 ES Wageningen, the Netherlands. – J. F. Stuefer, Dept of Experimental Plant Ecology, Radboud Univ. Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, the Netherlands. – C. A. Hordijk, Dept of Microbial Wetland Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Rijksstraatweg 6, NL-3631 AC Nieuwersluis, the Netherlands.

Abstract

It is widely reported that plants emit volatile compounds when they are attacked by herbivorous insects, which may be used by parasitoids and predators to locate their host or prey. The study of herbivore-induced plant volatiles and their role in mediating interactions between plants, herbivores and their natural enemies have been primarily based on aboveground systems, generally ignoring the potential interactions between above and belowground infochemical- and food webs. This study examines whether herbivory by Delia radicum feeding on roots of Brassica nigra (black mustard) affects the behaviour of Cotesia glomerata, a parasitoid of the leaf herbivore Pieris brassicae, mediated by changes in plant volatiles. In a semi-field experiment with root-damaged and root-undamaged plants C. glomerata prefers to oviposit in hosts feeding on root-undamaged plants. In addition, in a flight-cage experiment the parasitoid also prefers to search for hosts on plants without root herbivores. Plants exposed to root herbivory were shown to emit a volatile blend characterized by high levels of specific sulphur volatile compounds, which are reported to be highly toxic for insects, combined with low levels of several compounds, i.e. beta-farnesene, reported to act as attractants for herbivorous and carnivorous insects. Our results provide evidence that the foraging behaviour of a parasitoid of an aboveground herbivore can be influenced by belowground herbivores through changes in the plant volatile blend. Such indirect interactions may have profound consequences for the evolution of host selection behaviour in parasitoids, and may play an important role in the structuring and functioning of communities.

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