Aphid as a network creator for the plant‐associated arthropod community and its consequence for plant reproductive success

Ecological communities consist of antagonistic and mutualistic interactions that can vary in their strength. Indirect effects act among species within or across trophic levels through multiple pathways in an interaction network. Although there are many studies showing indirect effects in ecological communities, we know little about how indirect effects impact the wider community by linking other direct and indirect interactions. Herbivore‐induced indirect effects are ubiquitous and powerful forces in structuring ecological communities. In a plant‐associated network, aphids have the potential to connect multiple interactions through ant‐ and plant‐mediated indirect effects on co‐occurring and/or temporally separated species. We examined how aphids affect the interaction network on tall goldenrod, Solidago altissima, based on data of arthropod species on it with and without the aphid, Uroleucon nigrotuberculatum, using structural equation modelling (SEM) analysis. The presence of aphids greatly changed the strength of several species interactions throughout the season. In the early season, aphids had negative indirect effects on leafhoppers and moth caterpillars through ants. On the other hand, aphid‐induced leaf regrowth decreased scale insects but increased grasshoppers in the late season, when the aphid was no longer present. Moreover, the aphid‐generated interactions increased seed production of tall goldenrods, due to indirect pathways through the leaf regrowth. The aphid thus played a critical role as a network creator in determining the interaction network by generating ant‐ and plant‐mediated indirect effects. In particular, the aphid‐induced leaf regrowth contributed to interaction diversity (i.e. total number of positive/negative interactions and link density per each species) by connecting arthropod species in the early and late seasons. We disentangled the complexity of direct and indirect pathways generated by the aphid (i.e. keystone herbivore), which largely determines community structure of associated arthropods and plant reproductive success. Our study combining ant‐ and plant‐mediated indirect interactions mediated by the aphid provides a basis of better understanding of the underlying mechanisms of how the impact of the keystone herbivore can spread through plant‐based insect networks via direct and indirect pathways. A lay summary is available for this article.