Ant-aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences

Abstract

The honeydew composition and production of four aphid species feeding on Tanacetum vulgare, and mutualistic relationships with the ant Lasius niger were studied. In honeydew of Metopeurum fuscoviride and Brachycaudus cardui, xylose, glucose, fructose, sucrose, maltose, melezitose, and raffinose were detected. The proportion of trisaccharides (melezitose, raffinose) ranged between 20% and 35%. No trisaccharides were found in honeydew of Aphis fabae, and honeydew of Macrosiphoniella tanacetaria consisted of only xylose, glucose and sucrose. M. fuscoviride produced by far the largest amounts of honeydew per time unit (880 μg/aphid per hour), followed by B. cardui (223 μg/aphid per hour), A. fabae (133 μg/aphid per hour) and M. tanacetaria (46 μg/aphid per hour). The qualitative and quantitative honeydew production of the aphid species corresponded well with the observed attendance by L. niger. L. niger workers preferred trisaccharides over disaccharides and monosaccharides when these sugars were offered in choice tests. The results are consistent with the ants' preference for M. fuscoviride, which produced the largest amount of honeydew including a considerable proportion of the trisaccharides melezitose and raffinose. The preference of L. niger for B. cardui over A. fabae, both producing similar amounts of honeydew, may be explained by the presence of trisaccharides and the higher total sugar concentration in B. cardui honeydew. M. tanacetaria, which produced only low quantities of honeydew with no trisaccharides was not attended at all by L. niger.

Evolution of microbial markets

“…In some primate species, mating opportunities are exchanged for grooming services (13,14). Aphids exchange honeydew, a nutritious resource, for ant-protection services (15,16). Although biological markets typically involve the exchange of different commodities, primate-grooming markets are an example in which the same commodity is provided by both partners (17,18).…”

“…Individuals discriminate, choosing a partner based on differences in the price or quality of the commodity offered (24). Ants choose aphids producing the highest quality of honeydew and remunerate them with high-quality protection services (15,25). Similarly, in primate-mating markets, males that offer more grooming are rewarded with more mating opportunities (13,26).…”

Regulation of ants' foraging to resource productivity

“…We followed the experimental procedure developed by Mailleux et al (2000) to test the behaviour of L. niger foragers when faced with six droplets of sucrose solution. The concentration of the tested sucrose solution was 0.6 M, within the density limits found in honeydew droplets actually emitted by aphids tended by L. niger (Vö lkl et al 1999). We chose to deliver a 0.3 µl droplet at each food source, a volume that compelled most foragers to search for additional sources in order to reach their desired volume.…”

Costs and constraints in aphid‐ant mutualism

“…This observation led to the hypothesis that aphids have evolved to synthesize melezitose from glucose and sucrose in the phloem sap to attract ants. Vo¨lkl et al (1999) simultaneously reared four aphid species (also described in ''Mediation of host plants on aphid-ant interactions'' in relation to the study by Stadler et al 2002) on the host plant tansy T. vulgare, and compared the composition of carbohydrates in the honeydew of the four species. Melezitose was detected in the honeydew of the two higher ranking of ant-attended species (Me.…”