Humans have artificially enhanced the productivity of terrestrial and aquatic ecosystems on a global scale by increasing nutrient loading. While the consequences of eutrophication are well-known, most studies tend to examine short-term responses relative to the time scales of heritable adaptive change. Thus, the potential role of adaptation by organisms in stabilizing the response of ecological systems to such perturbations is largely unknown. We tested the hypothesis that adaptation by a generalist consumer (Daphnia pulicaria) to toxic prey (cyanobacteria) mediates the response of lake ecosystems to nutrient enrichment. Using a manipulative field experiment in limnocorrals, we examined the interactive effects of nutrient enrichment and consumer genotype (sensitive vs. tolerant to toxic prey) on algal abundance and species composition. We then tested theoretical predictions of how the magnitude of consumer effects should vary with productivity by conducting simultaneous mesocosm experiments across 11 ponds that spanned a large gradient in total phosphorus. One set of simultaneous mesocosm experiments (6 ponds) was conducted in the spring with highly edible prey, and the second set (5 ponds) in the fall when grazing-resistant and toxic prey (i.e., cyanobacteria) were common. We manipulated consumer genotype (control, sensitive, and tolerant D. pulicaria) in replicate mesocosms within each pond for both sets of experiments.
Sensitive and tolerant D. pulicaria genotypes had comparable effects on algal biomass under ambient (unfertilized) conditions. In contrast, tolerant genotypes resulted in a greater than 80% reduction in algal biomass versus no effect of sensitive genotypes under fertilized conditions, relative to the no Daphnia control. The interactive effects of fertilization and Daphnia genotype on algal biomass were mediated by the positive response of the invasive and toxic cyanobacterium Cylindrospermopsis raciborskii and an associated cyanotoxin (saxitoxin) to nutrient enrichment. In the cross-pond, gradient experiment, the relative effect of D. pulicaria on algal biomass generally increased with productivity. However, these effects were contingent on prey traits and consumer genotype. Tolerant D. pulicaria strongly suppressed toxic cyanobacteria in nutrient-rich ponds, but sensitive D. pulicaria did not. Our results demonstrate that organismal adaptation is critical for understanding and predicting ecosystem-level consequences of anthropogenic environmental perturbations.