The impact of antipredator behavior on resource biomass and distribution has been widely demonstrated in laboratory settings, yet tests of the magnitude of trait-mediated indirect effects (TMIE) in wild populations are rare. One of the few wild systems where TMIEs have been strongly supported is a model single-predator (puma), single-prey (vicuña) system in San Guillermo National Park, Argentina, where spatial patterns of predation risk increased biomass of vegetation in herbivore exclosures, but only in refuge habitats. However, a recent mange outbreak resulted in a profound collapse of the vicuña population (99% decline), transforming a TMIE to a density-mediated indirect effect (DMIE) on forage plants. Here, we quantify the magnitude of the cascading effects of this shift and test two alternative hypotheses to explain its mechanism: 1) mange makes vicuñas more vulnerable to puma predation (i.e. pumas remain the primary top-down force, but their major impact shifts from being trait- to density-mediated); or 2) mortality in vicuñas is dominated by the direct impact of mange (i.e. mange displaces pumas as the primary top-down force).
Results/Conclusions
We did not observe a shift in puma predation distribution (i.e. more kills in the refuge) or magnitude (i.e. higher kill rates) in concordance with the mange epidemic. Therefore, we did not find evidence that mange changed the relationship between pumas and vicuñas, but rather that mange itself was the driver of the DMIE. We found that increases in greenness (measured by the Normalized Difference Vegetation Index, or NDVI) and forage biomass occurred only in refuge habitats where TMIEs had been documented, indicating a breakdown in the TMIE. Time since mange was a strong predictor of NDVI increase, but only in refuges, and forage biomass increased by over 1000% in refuge habitats (a similar magnitude increase as found in earlier exclosure experiments). The magnitude of the effect indicates that the strength of the mange-induced DMIE on forage was similar to that of the previous predator-induced TMIE. Our results suggest that disease can transform a predator-induced TMIE-dominated system into a disease-induced DMIE-dominated system. We also show how controlled experiments can be used to examine the magnitude of different mechanisms of top-down forcing when confronted with environmental change.