The perils of an unreliable partner: Ant-barrel cactus mutualisms in the face of invasion

Background/Question/Methods Invasive species alter the dynamics of mutualisms when quantitative or qualitative differences exist between native participants and invaders. Invasive ants are of interest in this respect because they often become more abundant and exhibit higher levels of aggression compared to the native ants they replace. In food-for-protection mutualisms between ants and plants with extra-floral nectaries (EFNs), invasive ants might therefore provide superior defense against herbivores. Enhanced protective services, however, do not always translate into net benefits for plants; invasive ants, for example, may harass pollinators or provide intermittent protection. In coastal southern California the invasive Argentine ant (Linepithema humile) visits EFNs on the coast barrel cactus (Ferocactus viridescens), a locally distributed and threatened species. In areas not invaded by Argentine ants, more than 20 species of native ants visit EFNs produced by F. viridescens. Following invasion by L. humile, however, this diverse native ant assemblage collapses to one where Argentine ants become numerically dominant and most native ants disappear. We combined observational and experimental approaches to quantify how the Argentine ant affects key attributes of this ant-cactus mutualism. Results/Conclusions Field data broadly support the existence of a mutualism between ants and F. viridescens. Ants discouraged a common herbivore (Narnia wilsoni (Hemiptera: Coreidae)) from feeding on cacti, and this form of herbivory reduced mass per individual seed and seed mass per plant. Evidence that ants benefit from EFNs primarily comes from their ubiquitous presence on cacti. Compared to Crematogaster californica, the most common native ant in the system, L. humile exhibited lower per capita effectiveness at deterring herbivores but may often compensate by recruiting large numbers of workers to cacti. Compared to plants where L. humile intermittently tended, for example, regularly tended cacti had fewer herbivores and increased mass per seed, seed mass per fruit, and seed mass per plant. Despite the putative benefits of Argentine ant visitation, we found that many cacti in invaded areas received intermittent seasonal protection, whereas cacti in uninvaded areas received consistent protection from a diversity of native ant species throughout the growing season. A significant and positive linear relationship exists between the mass per seed of individual cacti and the number of ant species present on plants throughout the season. Native ant diversity may thus act as insurance in the maintenance of this mutualism.