Aphid Alarm Pheromone as a Cue for Ants to Locate Aphid Partners

François J Verheggen,Christophe Fischer,Ludovic Sablon,Claire Detrain,Stefan Bartram,Eric Haubruge,Lise Diez,Nicolas Chaline

doi:10.1371/journal.pone.0041841

François J Verheggen, Christophe Fischer + Show 6 more

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https://doi.org/10.1371/journal.pone.0041841

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Abstract

The mutualistic relationships that occur between myrmecophilous aphids and ants are based on the rich food supply that honeydew represents for ants and on the protection they provide against aphid natural enemies. While aphid predators and parasitoids actively forage for oviposition sites by using aphid semiochemicals, scouts of aphid-tending ant species would also benefit from locating honeydew resources by orienting toward aphid pheromone sources. The present study aims to provide additional information on the use of Aphis fabae alarm pheromone, i.e. (E)-β-farnesene (EβF), by ant scouts. The perception and behavioral impact of EβF on Lasius niger were investigated using electroantennography and two bio-assays measuring their attraction and orientation towards aphid semiochemicals. Pronounced electrical depolarizations were observed from L. niger scout antennae to stimulations of A. fabae alarm pheromone, while other sesquiterpenes elicited weak or no responses. L. niger scouts were significantly attracted toward EβF in a four-arm olfactometer, as well as in an two-choice bioassay. These laboratory results suggest for the first time that low amounts of aphid alarm pheromone can be used by L. niger scouts as a cue indicating the presence of aphid colonies and could therefore mediate the aphid-ant partnership in the field.

Highlights

Aphids (Hemiptera, Aphididae) and ants (Hymenoptera, Formicidae) are the protagonists of one of the most studied model of mutualistic relationships in the animal kingdom: the first ones produce a carbohydrate-rich excretion named honeydew, which is collected by some ant species who provide aphids in return with protection and hygiene [1]
As regards ant scouts having chosen the untreated side, we found out a higher, but not statistically significant, percentage (29%) of ‘‘hesitating’’ individuals that first initiated a short movement towards the EbF treated plant before changing side (Fisher’s exact test, P = 0.190)
Our results demonstrate that L. niger have olfactory receptors perceiving A. fabae alarm pheromone, as shown by the positive dose–response relationship in EAG to EbF

Summary

Introduction

Aphids (Hemiptera, Aphididae) and ants (Hymenoptera, Formicidae) are the protagonists of one of the most studied model of mutualistic relationships in the animal kingdom: the first ones produce a carbohydrate-rich excretion named honeydew, which is collected by some ant species who provide aphids in return with protection and hygiene [1]. The communication between both partners was thought to be essentially tactile, as ants palpate aphids’ abdomen using alternatively their two antennae to stimulate the ejection of honeydew droplets. Nothing is known about the possible chemical detection of aphids by ants from a distance, the first encounter between both insect species being usually assumed to occur by chance

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