Indirect Effects of an Introduced Ungulate on Pollination and Plant Reproduction

Herbivores can affect plants not only directly through browsing and trampling, but also indirectly through other species. For example, herbivores could affect the interaction between plants and their pollinators. Because plant population density may affect plant–pollinator interactions and plant reproductive success, we hypothesized that herbivores could affect pollination and plant reproduction indirectly by modifying plant population density. Unlike previous hypotheses, which concerned individual-level effects on vegetative and reproductive traits, our hypothesis focuses on population-level effects and involves a feedback mechanism. To test this hypothesis, we conducted field studies in the temperate forest of the southern Andes, where introduced ungulates are a major source of anthropogenic alteration. For 10 animal-pollinated understory plants, we compared population density, pollinator visitation, pollen deposition in stigmas, and reproduction in four pairs of grazed and ungrazed sites. We found evidence of indirect effects of ungulates on pollination and reproduction only for the herb Alstroemeria aurea (Alstroemeriaceae). The general lack of evidence for indirect effects on most of the species may result from resistance to cattle browsing and trampling, or low statistical power. For A. aurea, we present additional evidence from trampling and hand-pollination experiments, plus path analyses of the effect of density on pollination and reproduction showing that: (1) cattle decrease the absolute and relative population density of this species through trampling; (2) density, particularly relative density, affects pollen deposition on stigmas; and (3) conspecific pollen deposition affects reproduction. Thus, our results indicate that, by directly reducing the population density of A. aurea, cattle are indirectly affecting its reproduction.