Does primary productivity modulate the indirect effects of large herbivores? A global meta-analysis

Indirect effects of large mammalian herbivores (LMH), while much less studied than those of apex predators, are increasingly recognized to exert powerful influences on communities and ecosystems. The strength of these effects is spatiotemporally variable, and several sets of authors have suggested that they are governed in part by primary productivity. However, prior theoretical and field studies have generated conflicting results and predictions, underscoring the need for a synthetic global analysis. We conducted a meta-analysis of the direction and magnitude of large mammalian herbivore-initiated indirect interactions using 67 published studies comprising 456 individual responses. We georeferenced 41 of these studies (comprising 253 responses from 33 locations on five continents) to a satellite-derived map of primary productivity. Because predator assemblages might also influence the impact of large herbivores, we conducted a similar analysis using a global map of large carnivore species richness. In general, LMH reduced the abundance of other consumer species and also tended to reduce consumer richness, although the latter effect was only marginally significant. There was a pronounced reduction in the strength of negative (i.e. suppressive, due e.g., to competition) indirect effects of LMH on consumer abundance in more productive ecosystems. In contrast, positive (facilitative) indirect effects were not significantly correlated with productivity, likely because these comprised a more heterogeneous array of mechanisms. We found no effect of carnivore species richness on herbivore-initiated indirect effect strength. Our findings help to resolve the fundamental problem of ecological contingency as it pertains to the strength of an understudied class of multitrophic interactions. Moreover, these results will aid in predicting the indirect effects of anthropogenic wildlife declines and irruptions, and how these effects might be mediated by climatically driven shifts in resource availability. To the extent that intact ungulate guilds help to suppress populations of small animals that act as agricultural pests and disease reservoirs, the negative impacts of large mammal declines on human well-being may be relatively stronger in low-productivity areas.