Aphid honeydew provides a nutritionally balanced resource for incipient Argentine ant mutualists

Food-for-protection mutualisms can provide resources that subsidize ecological dominance, although their stability often depends on the nutritional match between the traded food and traits to which it is allocated. A well-studied food-for-protection mutualism is the protection by Argentine ants, Linepithema humile, of hemipteran mutualists in return for honeydew, which is generally assumed to be a nutritionally imbalanced food, high in carbohydrates and low in protein. We tested an alternative hypothesis, that the nutritional value of honeydew depends on the composition of life history traits related to survival (worker maintenance) and colony growth (brood production). Using a factorial design, we manipulated ant colony access to aphids, baseline levels of nutritional deprivation, and, by adding or subtracting queens, the ability to invest in growth. We found that aphid access primarily benefited colonies on high-protein, low-carbohydrate diets, suggesting colony nutritional state influences the value of aphid associations. Unexpectedly, we found that worker survival and brood production were positively correlated across treatments, and both decreased with the ants' percentage of nitrogen mass, a proxy for body protein. Moreover, the workers' percentage of fat mass was generally lower in brood-producing colonies, particularly in high-protein treatments, suggesting strong competition among investments for limited carbohydrates. These results suggest that carbohydrate access generally constrains Argentine ant life history and clarifies the links between the nutritional composition of food rewards and the stability of ecologically important mutualisms.