Nutrient limitation controls the strength of behavioral trophic cascades in high elevation streams

Indirect effects of predators on primary producers vary over space and time. Key components of the environmental context underlying that variability include the bottom-up supply of resources and the defense, mobility and foraging efficiency of primary consumers. We manipulated key resources that limit primary producers and tested the effects of system enrichment on the strength of top-down interactions between top predators (Salvelinus fontinalis), different types of grazing invertebrates and algae in high elevation streams of Colorado, USA. We added nitrogen and phosphorus to flow-through microcosms powered by stream water and tested the direct effects of chemical cues from brook trout on the behavior of sedentary, predator-resistant (caddisflies) and mobile, predator-vulnerable grazers (mayflies), and the indirect cascading effects of predators on: (1) the biomass of algae mediated by grazer behavior and (2) the impact of grazers on algal biomass accrual. Recognizing the value of whole-ecosystem experiments, we also tested the effects of supplementing nutrients to two headwater fishless streams on the impact of grazers on algae and the performance (growth rates) of four predominant grazer species compared to two adjacent reference streams with ambient (limited) nutrients. In both experiments, algal biomass increased with added nutrients where consumption by grazers was swamped by increased algal accrual due to enrichment. Results of the microcosm experiment were consistent with a context-dependent behavioral trophic cascade whereby predator cues increased the biomass of algae only in treatments with enriched nutrients and mobile, predator-vulnerable grazers (Baetis mayflies). Baetis showed risk-sensitive behavioral responses to fish cues, which resulted in cascading effects on algae only under enrichment. In contrast, behavior of sedentary, predator-resistant caddisflies (Allomyia) was unaffected by predator cues and a cascade was never observed. The whole ecosystem experiment revealed no aggregative responses by grazers but instead, strong developmental responses of all grazer species to nutrient enrichment. Growth rates of grazers increased with mobility, with the highest rates occurring for mobile, predator-vulnerable Baetis mayflies in enriched streams. Our results emphasize the importance of experimentally testing the context-dependency of trophic cascades, and are consistent with the hypothesis that nutrient limitation may reduce the strength of trophic cascades.