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 stressresponse 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.ecological stoichiometry | metabolism | nutrient balance | physiological stress | predator-prey interaction

Interactive effects of predation risk and conspecific density on the nutrient stoichiometry of prey

“…Organisms under predation risk can alter their resource use and metabolic demand (Guariento and Esteves 2013; Sheriff and Thaler 2014), and consequently, their nutritional budget, body nutrient composition, and excretion rates and ratios (Hawlena and Schmitz 2010a,b; Dalton and Flecker 2014). The nutrient demand of an organism is affected by the intensity of its physiological processes, which, among other factors, might depend on its level of stress (Steiner and Van Buskirk 2009; Hawlena and Schmitz 2010b).…”

“…On the other hand, if such a metabolic increase is maintained over the long term (i.e., days), the prey is forced to relocate energy from growth or storage to meet the metabolic energy demand. This mechanism may inhibit prey biomass production and nutrient excretion, and, in extreme cases, promote the breakdown of body proteins into glucose (i.e., gluconeogenesis) (Hawlena and Schmitz 2010a,b). Adjustments in the foraging behavior of prey related to resource choice can prevent the deleterious effects of the increase in energy demand induced by predation risk (Hawlena and Schmitz 2010a,b).…”

“…This mechanism may inhibit prey biomass production and nutrient excretion, and, in extreme cases, promote the breakdown of body proteins into glucose (i.e., gluconeogenesis) (Hawlena and Schmitz 2010a,b). Adjustments in the foraging behavior of prey related to resource choice can prevent the deleterious effects of the increase in energy demand induced by predation risk (Hawlena and Schmitz 2010a,b). Therefore, alterations in the nutrient excretion of prey in response to predation risk might affect rapid nutrient cycling and mineralization through organism ingestion and posterior excretion, while alterations in the resource choices of prey might affect slow nutrient cycling and organic matter left to the detritivore chain (Vanni 2002).…”

“…2012). For example, Melanoplus femurrubrum grasshoppers facing spider predation risk have a greater demand for carbon (C) than control grasshoppers do, leading to changes in the grasshoppers’ diet, with consequences that affect nutrient recycling (Hawlena and Schmitz 2010a). Not many studies have investigated whether and how predation risk might directly and indirectly modify prey body and excretion nutrient stoichiometry, respectively (Dalton and Flecker 2014).…”

“…Not many studies have investigated whether and how predation risk might directly and indirectly modify prey body and excretion nutrient stoichiometry, respectively (Dalton and Flecker 2014). The general stress paradigm (GSP) (Hawlena and Schmitz 2010a) asserts that predation risk ultimately increases the organism's energetic demand, shifting the fate of C from secondary production to maintenance and resulting in the release of excess nutrients associated with structural tissues, mostly nitrogen (N) and phosphorus (P). The rationale behind this hypothesis derives from the notion of organism threshold elementary ratio (TER) (Frost et al.…”