Indirect interactions in terrestrial plant communities: emerging patterns and research gaps

Indirect interactions occur when the effect of one species on another is mediated by a third species. These interactions occur in most multi-species assemblages and are diverse in their mechanistic pathways. The interest in indirect interactions has increased exponentially over the past three decades, in recognition of their importance in determining plant community dynamics and promoting species coexistence. Here, we review the literature on indirect interactions among plants published since 1990, using a novel synthetic framework that accounts for and classifies intervening species and mechanisms within trophic networks. The objectives of this review are: (1) to identify the geographical regions and ecosystem types where indirect interactions have been examined; (2) to summarize the information on the number of trophic levels examined in studies of indirect interactions; (3) to test whether the frequency of indirect interactions varies across environmental gradients; and (4) to identify the experimental approaches most commonly used in studies of indirect interactions. Studies examining indirect interactions in plants have been conducted primarily in the Northern Hemisphere, with a focus on grasslands and forests. The majority of studies (67%) examined two trophic levels. Indirect facilitation and apparent competition are the interactions that have been most frequently examined, with the latter being reported more frequently in relatively productive environments. Other indirect interactions reported include associational resistance, exploitative competition or facilitation, shared defenses, and trophic cascades. Generally, field experiments tested indirect interactions based on single target species. While the majority of studies on indirect interactions dealt with basic ecology issues, several studies have dealt with such interactions in the context of biological invasions (18%) and rangeland management (12%). This review allowed us identifying a number of research needs, including the study of non-feeding interactions and that for more realistic complex designs, explicitly testing indirect interactions across different trophic levels, in geographical regions that have been under-examined to date, and in stressful ecosystems.