Defence variation within a guild of aphid-tending ants explains aphid population growth

Abstract

Mutualism studies often focus on the service provided by single species, while variation in benefits provided by multiple partners is less understood. Ant-aphid food-for-protection mutualisms are suitable to study the implications of intra-guild service variation because they often involve several ant species with varying levels of aggressiveness. We studied an aphid species and its associated ant guild to address whether intra-guild defence variation against aphid natural enemies explains aphid performance on plants (thistles). We surveyed plants with natural abundances of aphids associated with different ant species and estimated aphid population growth. We conducted confrontation experiments between ant species and aphid natural enemies (ladybugs and hoverfly larvae). In plants patrolled by the most aggressive ant species, we determined the ant's probability of expelling aphid natural enemies and tested whether ant exclusion affects the abundance of aphids and their natural enemies. The ant Dorymyrmex tener was the most abundant and frequent species on plants and the most aggressive against aphid natural enemies. Aphid populations grew faster on plants patrolled by D. tener compared to plants patrolled by Camponotus distinguendus or D. richteri. Field experiments confirmed that D. tener effectively expels aphid natural enemies from plants. When D. tener was excluded, the density of aphids decreased, while the abundance of aphid natural enemies increased. The disruption of aphid predation by aggressive and numerically dominant ant species is a determinant of aphid population dynamics. This study illustrates the importance of considering intra-guild service variation to better understand multi-partner mutualisms.