An ecological cost of plant defence: attractiveness of bitter cucumber plants to natural enemies of herbivores

Anurag A. Agrawal,* Arne Janssen, Jan Bruin, Maarten A. Posthumus and Maurice W. Sabelis Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada. Section Population Biology, University of Amsterdam, Kruislaan 320, 1098 SM Amsterdam, The Netherlands. Laboratory of Organic Chemistry, Wageningen Agricultural University, Dreijenplein 8, 6703 HB Wageningen, The Netherlands. *Correspondence: E-mail: [email protected] Abstract Plants produce defences that act directly on herbivores and indirectly via the attraction of natural enemies of herbivores. We examined the pleiotropic effects of direct chemical defence production on indirect defence employing near-isogenic varieties of cucumber plants (Cucumis sativus) that differ qualitatively in the production of terpenoid cucurbitacins, the most bitter compounds known. In release–recapture experiments conducted in greenhouse common gardens, blind predatory mites were attracted to plants infested by herbivorous mites. Infested sweet plants (lacking cucurbitacins), however, attracted 37% more predatory mites than infested bitter plants (that produce constitutive and inducible cucurbitacins). Analysis of the headspace of plants revealed that production of cucurbitacins was genetically correlated with large increases in the qualitative and quantitative spectrum of volatile compounds produced by plants, including induced production of (E )-b-ocimene (3E )-4,8-dimethyl-1,3,7-nonatriene, (E,E)-a-farnesene, and methyl salicylate, all known to be attractants of predators. Nevertheless, plants that produced cucurbitacins were less attractive to predatory mites than plants that lacked cucurbitacins and predators were also half as fecund on these bitter plants. Thus, we provide novel evidence for an ecological trade-off between direct and indirect plant defence. This cost of defence is mediated by the effects of cucurbitacins on predator fecundity and potentially by the production of volatile compounds that may be repellent to predators.