Aphid-ant mutualism: How do aphids focus ant foraging?

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 identify the chemical factors that attract ants and that maintain their mutualistic relationships with aphids. The perception and behavioral impact of Aphis fabae alarm pheromone, namely (E)-β-farnesene, on Lasius niger were firstly investigated using electroantennography and a four-arm olfactometer. Aphis fabae honeydew sugar composition was subsequently analyzed while the foraging and recruiting behaviour of L. niger scouts towards each of the identified sugars was studied. Clear electrical depolarisations were observed from L. niger scout antennae to stimulations of A. fabae alarm pheromone. Scouts were significantly attracted toward (E)-β-farnesene in the four-arm olfactometer, suggesting for the first time that the latter compound is a key chemical in the establishment of the mutualism. Aphis fabae honeydew consisted of 9 identified mono-, di- and tri-saccharides and 8 hydrocarbons that could not be identified. The main identified sugars were sucrose, fructose, glucose and melezitose. L. niger scouts showed the following drinking preferences for the tested sugars: melezitose = sucrose = raffinose > glucose = fructose > maltose = trehalose = melibiose = xylose, with a recruitment launched toward the first three sugars. Therefore, ant scouts may use aphid semiochemicals to locate at distance an aphid colony and subsequently estimate honeydew quality by tasting it before recruiting conspecifics and establishing a mutualistic relationship.