We present a framework to explain how prey stress responses to predation can resolve context dependency in ecosystem properties and functions such as food chain length, secondary production, elemental stoichiometry, and cycling. We first describe the major nonspecific physiological stress mechanisms and their ecologically relevant consequences. We next synthesize the evidence for prey physiological responses to predation risk and demonstrate that they are similar across taxa and fit well within the general stress paradigm. We then illustrate the utility of our idea by applying our understanding of the ecological consequences of stress to explain how herbivore‐prey physiological antipredator responses affect ecosystem dynamics. We hypothesize that stressed herbivores should forage on plant species with higher digestible carbohydrates than should unstressed herbivores to meet heightened energy demands. Increased consumption of carbohydrate‐rich plants should reduce their relative abundance in the community, hence altering the quantity and quality of plant litter entering the detrital pool. We further hypothesize that stress should change the elemental composition and energy content of prey excreta, egesta, and carcasses that enter the detrital pool. Finally, prey stress should lower energy and nutrient conversion efficiency and hence the transfer of materials and energy up the food chain, which should, in turn, weaken the association between ecosystem productivity and food chain length.
Predators are predominantly valued for their ability to control prey, as indicators of high levels of biodiversity and as tourism attractions. This view, however, is incomplete because it does not acknowledge that predators may play a significant role in the delivery of critical life-support services such as ecosystem nutrient cycling. New research is beginning to show that predator effects on nutrient cycling are ubiquitous. These effects emerge from direct nutrient excretion, egestion or translocation within and across ecosystem boundaries after prey consumption, and from indirect effects mediated by predator interactions with prey. Depending on their behavioural ecology, predators can create heterogeneous or homogeneous nutrient distributions across natural landscapes. Because predator species are disproportionately vulnerable to elimination from ecosystems, we stand to lose much more from their disappearance than their simple charismatic attractiveness.
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
Aboveground consumers are believed to affect ecosystem functioning by regulating the quantity and quality of plant litter entering the soil. We uncovered a pathway whereby terrestrial predators regulate ecosystem processes via indirect control over soil community function. Grasshopper herbivores stressed by spider predators have a higher body carbon-to-nitrogen ratio than do grasshoppers raised without spiders. This change in elemental content does not slow grasshopper decomposition but perturbs belowground community function, decelerating the subsequent decomposition of plant litter. This legacy effect of predation on soil community function appears to be regulated by the amount of herbivore protein entering the soil.
1. There is a large and growing interest in non-consumptive effects (NCEs) of predators. Diverse and extensive evidence shows that predation risk directly influences prey traits, such as behaviour, morphology and physiology, which in turn, may cause a reduction in prey fitness components (i.e. growth rate, survival and reproduction). An intuitive expectation is that NCEs that reduce prey fitness will extend to alter population growth rate and therefore population size.2. However, our intensive literature search yielded only 10 studies that examined how predator-induced changes in prey traits translate to changes in prey population size. Further, the scant evidence for risk-induced changes on prey population size have been generated from studies that were performed in very controlled systems (mesocosm and laboratory), which do not have the complexity and feedbacks of natural settings. Thus, although likely that predation risk alone can alter prey population size, there is little direct empirical evidence that demonstrates that it does. There are also clear reasons that risk effects on population size may be much smaller than the responses on phenotype and fitness components that are typically measured, magnifying the need to show, rather than infer, effects on population size.3. Herein we break down the process of how predation risk influences prey population size into a chain of events (predation risk affects prey traits, which affect prey fitness components and population growth rate, which affect prey population size), and highlight the complexity of each transition. We illustrate how the outcomes of these transitions are not straightforward, and how environmental context strongly dictates the direction and magnitude of effects. Indeed, the high variance in prey responses is reflected in the variance of results reported in the few studies that have empirically quantified risk effects on population size. It is therefore a major challenge to predict population effects given the complexity of how environmental context interacts with predation risk and prey responses. 4. We highlight the critical need to appreciate risk effects at each level in the chain of events, and that changes at one level cannot be assumed to translate into changes in the next because of the interplay between risk, prey responses, and the environment. The gaps in knowledge we illuminate underscore the need for more evidence to substantiate the claim that predation risk effects extend to prey | 1303Journal of Animal Ecology SHERIFF Et al. K E Y W O R D Santi-predator response, fear effects, indirect effects, non-lethal effects, phenotypic plasticity, predation risk, predator-prey interactions, trait-mediated effects F I G U R E 1 The chain of events from predation risk to prey population size. Predation risk (level A) acts to alter prey phenotype (level B), which can influence fitness components (growth rate, fecundity and survival; double-headed arrows again represent the feedbacks possible) and population growth rate (level C). These effects...
Trophic cascades-the indirect effects of carnivores on plants mediated by herbivores-are common across ecosystems, but their influence on biogeochemical cycles, particularly the terrestrial carbon cycle, are largely unexplored. Here, using a 13 C pulse-chase experiment, we demonstrate how trophic structure influences ecosystem carbon dynamics in a meadow system. By manipulating the presence of herbivores and predators, we show that even without an initial change in total plant or herbivore biomass, the cascading effects of predators in this system begin to affect carbon cycling through enhanced carbon fixation by plants. Prolonged cascading effects on plant biomass lead to slowing of carbon loss via ecosystem respiration and reallocation of carbon among plant aboveground and belowground tissues. Consequently, up to 1.4-fold more carbon is retained in plant biomass when carnivores are present compared with when they are absent, owing primarily to greater carbon storage in grass and belowground plant biomass driven largely by predator nonconsumptive (fear) effects on herbivores. Our data highlight the influence that the mere presence of predators, as opposed to direct consumption of herbivores, can have on carbon uptake, allocation, and retention in terrestrial ecosystems.experimental ecosystem ecology | animal-mediated carbon cycling | carbon tracer experiment | carbon retention T rophic downgrading-the disproportionate loss of species occupying top trophic levels of ecosystems-is a symptom of global biodiversity decline (1). Cutting short trophic chains in ecosystems causes significant changes in plant community biomass, composition, and diversity (2). These changes come about because loss of carnivores leads to increased impacts of herbivores on plant biomass through changes in herbivore density and foraging strategies (3).It is becoming increasingly recognized that the cascading effects of carnivores may affect ecosystem carbon dynamics as well. By altering the impact of herbivores on plants, carnivores may indirectly regulate the amount and type of plant biomass available for photosynthetic carbon fixation and storage (3-5). Moreover, herbivory can trigger physiological adjustments in the remaining damaged plants, including reduction in photosynthetic rates and increased respiration (6-8). Accordingly, we hypothesized that carnivores should increase plant community carbon fixation and reduce respiration, thereby increasing carbon retention, by causing herbivores to reduce their foraging impacts on plants. We tested this hypothesis with a 13 CO 2 pulse-chase field experiment in a grassland ecosystem in northeastern Connecticut.Using established methods to discern indirect effects of carnivores on plants in ecosystems (9), we applied three experimental treatments in replicated 0.25-m 2 fine-mesh enclosures (Fig. S1): (i) plants only (control), (ii) plants and herbivores (+ herbivore), and (iii) plants, herbivores, and carnivores (+ carnivore). The first treatment served as a control for animal effects, the + he...
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