Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics

Abstract

The process of nutrient transfer through an ecosystem is an important determinant of production, food-chain length, and species diversity. The general view is that the rate and efficiency of nutrient transfer up the food chain is constrained by herbivore-specific capacity to secure N-rich compounds for survival and production. Using feeding trials with artificial food, we show, however, that physiological stress-response of grasshopper herbivores to spider predation risk alters the nature of the nutrient constraint. Grasshoppers facing predation risk had higher metabolic rates than control grasshoppers. Elevated metabolism accordingly increased requirements for dietary digestible carbohydrate-C to fuel-heightened energy demands. Moreover, digestible carbohydrate-C comprises a small fraction of total plant tissue-C content, so nutrient transfer between plants and herbivores accordingly becomes more constrained by digestible plant C than by total plant C:N. This shift in herbivore diet to meet the altered nutrient requirement increased herbivore body C:N content, the C:N content of the plant community from which grasshoppers select their diet, and grasshopper fecal C:N content. Chronic predation risk thus alters the quality of animal and plant tissue that eventually enters the detrital pool to become decomposed. Our results demonstrate that herbivore physiology causes C:N requirements and nutrient intake to become flexible, thereby providing a mechanism to explain context dependence in the nature of trophic control over nutrient transfer in ecosystems.

Fig. 1.

Grasshopper nutrient intake and excretion during feeding trials with artificial diets. The experiment was conducted to discern the dietary response of grasshoppers to predation risk. (A) Grasshoppers were presented diets with either 7% protein and 28% digestible carbohydrate or 28% protein and 7% digestible carbohydrate. The solid lines represent intake rails (the balance of nutrients contained in diets) that define the boundaries of the nutritional space for all potential nutrient intake (55). The dashed line represents the nutrient intake target revealed by grasshoppers feeding on the two different diets. In the absence of predation risk, grasshoppers preferred a diet with 1:1 ratio of protein and carbohydrate intake rather than a diet matching their body elemental ratio. Grasshoppers facing risk consumed slightly higher amounts of dietary N than control grasshoppers, and consumed much greater dietary C. (B) Grasshoppers in the feeding trials excreted similar levels of C, reflecting higher respiration of C in risk conditions than in control conditions. Consequently, excess N intake in risk conditions is released in the feces. This result leads to differences in fecal C:N content between risk and control conditions. Values are mean ± SE.

Fig. 2.

Pathways through which C:N change impacts the ecosystem. Changes in herbivore physiological demand for C and N in response to predation risk can lead to shifts in C:N content of organic material along four pathways that eventually lead to the organic-matter pool to be decomposed. (A) C:N composition of herbivore body tissue. (B) C:N composition of herbivore feces. (C) Changes in C:N content of the herb community as a result of mediation of Solidago-competitive dominance by herbivory in the face of predation risk. Solid red arrows indicate direct trophic interactions; dashed red arrows indicate a nontrophic fear effect. Arrow thickness indicates food preference under risk conditions. Green arrows indicate the source and fate of tissue C and N in the ecosystem. Values are mean ± SE. *, significant difference (P < 0.05).