Historical forest disturbance results in variation in functional resilience of seed dispersal mutualisms

Abstract

Mutualistic interactions provide essential ecosystem functions, such as promoting and maintaining diversity. Understanding if functionally important mutualisms are resilient (able to resist and recover) to anthropogenic disturbance is important to understand the capacity for diversity to recover. Animal-mediated seed dispersal supports plant population growth and community structure, and disturbance of this function can threaten plant diversity and contribute to low resiliency. Ant-mediated seed dispersal mutualisms are particularly sensitive to anthropogenic disturbance, as they rely on one to a few high-quality dispersal partners. In North American eastern deciduous forests (NAEDF), ants in the genus Aphaenogaster are "keystone dispersers" of 30-40% of understory forbs adapted to dispersal by ants (myrmecochores). The majority of present day NAEDF have regenerated from previous disturbance in the form of historical land use change (HLUC), due to clearing for agriculture. Previous studies have revealed that myrmecochore diversity is not resilient to HLUC. Here, we ask if seed dispersal mutualisms are resilient to HLUC and if decreases in mutualistic interactions with partners, Aphaenogaster sp., or increases in antagonistic interactions cause degradation of function. In a large-scale natural experiment (20 sites), we measured seed removal, the abundance of mutualistic partners and other invertebrates interacting with seeds, myrmecochore cover and diversity, along with ant habitat and forest structure. We found lower and more variable seed removal in secondary forests compared to remnant forests. A path analysis of all forests revealed that abundance of mutualists was the primary determinant of variation in seed removal, and that seed damage by antagonists (invasive slugs) negatively affected dispersal and was higher in secondary forests. In a path analysis of remnant forests, the link between mutualist abundance and seed removal was absent, but present in the secondary forest path, suggesting that seed dispersal is more variable and dependent on mutualist abundance in secondary forests and is stable and high in remnant forests. Here we show that functional resilience to HLUC is variable and may impede recovery of understory plant communities. This work provides key insights on the effects of anthropogenic disturbance on mutualistic interactions and how the resilience of critical ecosystem functions impacts diversity resiliency.