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Open Access Research article

Gall volatiles defend aphids against a browsing mammal

Michael Rostás12*, Daniel Maag24, Makihiko Ikegami1 and Moshe Inbar3

Author Affiliations

1 Bio-Protection Research Centre, Lincoln University, PO Box 85084, Lincoln 7647, New Zealand

2 Department of Botany II, University of Würzburg, Würzburg 97082, Germany

3 Department of Evolutionary & Environmental Biology, University of Haifa, Haifa 31905, Israel

4 Laboratory of Fundamental and Applied Research in Chemical Ecology, Institute of Biology, University of Neuchâtel, 2009, Neuchâtel, Switzerland

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BMC Evolutionary Biology 2013, 13:193  doi:10.1186/1471-2148-13-193

Published: 11 September 2013

Abstract

Background

Plants have evolved an astonishing array of survival strategies. To defend against insects, for example, damaged plants emit volatile organic compounds that attract the herbivore’s natural enemies. So far, plant volatile responses have been studied extensively in conjunction with leaf chewing and sap sucking insects, yet little is known about the relationship between plant volatiles and gall-inducers, the most sophisticated herbivores. Here we describe a new role for volatiles as gall-insects were found to benefit from this plant defence.

Results

Chemical analyses of galls triggered by the gregarious aphid Slavum wertheimae on wild pistachio trees showed that these structures contained and emitted considerably higher quantities of plant terpenes than neighbouring leaves and fruits. Behavioural assays using goats as a generalist herbivore confirmed that the accumulated terpenes acted as olfactory signals and feeding deterrents, thus enabling the gall-inducers to escape from inadvertent predation by mammals.

Conclusions

Increased emission of plant volatiles in response to insect activity is commonly looked upon as a “cry for help” by the plant to attract the insect’s natural enemies. In contrast, we show that such volatiles can serve as a first line of insect defences that extends the ‘extended phenotype’ represented by galls, beyond physical boundaries. Our data support the Enemy hypothesis insofar that high levels of gall secondary metabolites confer protection against natural enemies.

Keywords:
Capra hircus; Enemy hypothesis; Extended phenotype; Herbivory; Intraguild predation; Plant defence; Tannins; Terpenes; Volatile organic compounds