A soil‐nesting invasive ant disrupts carbon dynamics in saplings of a foundational ant–plant

Abstract

Abstract Nearly every terrestrial ecosystem hosts invasive ant species, and many of those ant species construct underground nests near roots and/or tend phloem‐feeding hemipterans on plants. We have a limited understanding of how these invasive ant behaviours change photosynthesis, carbohydrate availability and growth of woody plants. We measured photosynthesis, water relations, carbohydrate concentrations and growth for screenhouse‐reared Acacia drepanolobium saplings on which we had manipulated invasive Pheidole megacephala ants and native Ceroplastes sp. hemipterans to determine whether and how soil nesting and hemipteran tending by ants affect plant carbon dynamics. In a field study, we also compared leaf counts of vertebrate herbivore‐excluded and ‐exposed saplings in invaded and non‐invaded savannas to examine how ant invasion and vertebrate herbivory are associated with differences in sapling photosynthetic crown size. Though hemipteran infestations are often linked to declines in plant performance, our screenhouse experiment did not find an association between hemipteran presence and differences in plant physiology. However, we did find that soil nesting by P. megacephala around screenhouse plants was associated with >58% lower whole‐crown photosynthesis, >31% lower pre‐dawn leaf water potential, >29% lower sucrose concentrations in woody tissues and >29% smaller leaf areas. In the field, sapling crowns were 29% smaller in invaded savannas than in non‐invaded savannas, mimicking screenhouse results. Synthesis. We demonstrate that soil nesting near roots, a common behaviour by Pheidole megacephala and other invasive ants, can directly reduce carbon fixation and storage of Acacia drepanolobium saplings. This mechanism is distinct from the disruption of a native ant mutualism by P. megacephala, which causes similar large declines in carbon fixation for mature A. drepanolobium trees. Acacia drepanolobium already has extremely low natural rates of recruitment from the sapling to mature stage, and we infer that these negative effects of invasion on saplings potentially curtail recruitment and reduce population growth in invaded areas. Our results suggest that direct interactions between invasive ants and plant roots in other ecosystems may strongly influence plant carbon fixation and storage.