Print PageIndirect effects may occur when one species alters the effect that another species has on a third. Exotic ungulates may indirectly affect plant communities by altering nutrient cycles, disturbance regimens and/or disrupting mutualistic interactions. In the temperate forest of Patagonia exotic ungulates were introduced as livestock and game. The northern portion of this forest harbors a unique keystone interaction comprised a hummingbird (Sephanoides sephaniodes), a mistletoe (Tristerix corymbosus), and the marsupial (Dromiciops gliroides); more than 20% of the woody flora species rely on the interactions of these species. Aristotelia chilensis is the main host of the mistletoe in this forest. Thus, if exotic ungulates reduce the number of A. chilensis, this could drastically reduce the number of mistletoes and potentially disrupt a key seed dispersal mutualism. Here, we examined the effect of exotic ungulates on A. chilensis and their indirect effects on the mistletoe-marsupial interaction at eight invaded sites and eight sites where exotic ungulates were not present (intact sites). We assessed the abundance of these species and evaluated a series of habitat variables at each site. Additionally, we experimentally excluded vertebrate herbivores to assess their direct effects on an A. chilensis.
Results/Conclusions
The abundance of A. chilensis was 7x greater in intact than in invaded sites. However, there was no difference in the number of A. chilensis seedlings between intact and invaded sites. The exclosure experiment showed that in just a month deer consumed 99% of the A. chilensis leaves outside the exclosure. In addition, by browsing on A. chilensis, exotic ungulates indirectly affected the population persistence of the keystone mistletoe: the density of mistletoes was 33x greater in intact than in invaded sites. Moreover, browsing by introduced ungulates altered the composition of the understory plant community, thus likely indirectly influencing the marsupial. At all of the invaded sites, we failed to detect the presence of marsupials. However, marsupials are present at each of the intact sites. Local extinctions of this marsupial have been associated with complete disruption of mistletoe seed dispersal. Not surprisingly, there were no mistletoe seeds or seedlings at invaded sites. Our results show that exotic ungulates, by browsing on A. chilensis, indirectly affected the keystone interactions between the mistletoe and the marsupial, and their disruption may have cascading effects through the rest of the ecosystem, threatening a much larger set of interactions.
