Hidden trade-off in a food-for-protection mutualism: Higher fungal infection and lower survival of nectar-producing galls when ants don’t tend

Background/Question/Methods

Mutualisms are reciprocal beneficial outcomes from species interactions. Mutualisms can undergo breakdown (i.e., one or both partners exit the relationship) due to variable circumstances, and breakdown consequences vary with partner dependency. In obligate mutualisms, breakdown is usually lethal, whereas the consequences are less clear in facultative mutualisms. The mealy oak gall wasp (Disholcaspis cinerosa) engages in a facultative food-for-protection mutualism in which the production of nectar reward by the gall wasp attracts arboreal ants that in turn deter parasitoids. When galls fail to recruit ants, they become vulnerable to not just parasitoids but also to sooty mold growth due to excess nectar on the gall’s surface. In urban environments where ant recruitment is less reliable, we have observed a novel polymorphism in which some galls do not produce nectar. As the accumulation of nectar can lead to potentially detrimental fungal infection, we hypothesize that the halt of reward production is a response of facultative mutualists to mutualism breakdown. To test this, we used a field-based factorial ant-exclusion experiment to monitor the survival of 1,000 galls. In doing so, we assess the survival associated trade-offs that are incurred across multiple interacting trophic levels as we artificially manipulate a mutualism-breakdown

Results/Conclusions

In a test of mutualism-breakdown of a facultative mutualism between a nectar-producing gall wasp and tending ant communities, we confirmed that when tending ants were excluded there was a significant increase in parasitoid attack. We also demonstrate that nectar production is positively correlated with sooty mold growth and that when ants are excluded from nectar-producing galls sooty mold infection increases. Furthermore, we found that sooty mold growth on untended nectar-producing galls posed an even greater threat to gall wasp survival than parasitism did to untended non-nectar producing galls. Interestingly, we also found that for untended galls, parasitoid attack was highest when nectar was present. Taken together, these findings suggest that nectar is an attractant not just for mutualistic ants, but also for both mold and parasitoids. When ants do not tend, gall wasp nectar production becomes a risky venture as it significantly increases the threat of fungal infection and parasitism. Therefore, the safest strategy for galls that occupy habitats where ants are an unreliable partner is to suspend nectar production altogether. For this reason, we suggest that stopping reward production is a viable response to facultative mutualism breakdown.