linking-predation-risk-herbivore-physiological-stress-microbial

Linking Predation Risk, Herbivore Physiological Stress and Microbial Decomposition of Plant Litter

The quantity and quality of detritus entering the soil  determines the rate of decomposition by microbial communities as well as  recycle rates of ...

Animal feeding ecology and diet are influenced by the fear of predation. While the mechanistic bases for such changes are well understood, technical difficulties often prevent testing how these mechanisms interact to affect a mesopredator's diet in natural environments. Here, we compared the insectivorous lizard Acanthodactylus beershebensis' feeding ecology and diet between high- and low-risk environments, using focal observations, intensive trapping effort and fecal pellet analysis. To create spatial variation in predation risk, we planted "artificial trees" in a scrubland habitat that lacks natural perches, allowing avian predators to hunt for lizards in patches that were previously unavailable to them. Lizards in elevated-risk environments became less mobile but did not change their microhabitat use or temporal activity. These lizards changed their diet, consuming smaller prey and less plant material. We suggest that diet shifts were mainly because lizards from risky environments consumed prey items that required shorter handling time.

Change your diet or die: predator-induced shifts in insectivorous lizard feeding ecology.

Anthropogenic habitat perturbation is a major cause of population decline. A standard practice managers use to protect populations is to leave portions of natural habitat intact. We describe a case study in which, despite the use of this practice, the critically endangered lizard Acanthodactylus beershebensis was locally extirpated from both manipulated and natural patches within a mosaic landscape of an afforestation project. We hypothesized that increased structural complexity in planted patches favors avian predator activity and makes these patches less suitable for lizards due to a heightened risk of predation. Spatial rarity of natural perches (e.g., trees) in arid scrublands may hinder the ability of desert lizards to associate perches with low-quality habitat, turning planted patches into ecological traps for such species. We erected artificial trees in a structurally simple arid habitat (similar to the way trees were planted in the afforestation project) and compared lizard population dynamics in plots with these structures and without. Survival of lizards in the plots with artificial trees was lower than survival in plots without artificial trees. Hatchlings dispersed into plots with artificial trees in a manner that indicated they perceived the quality of these plots as similar to the surrounding, unmanipulated landscape. Our results showed that local anthropogenic changes in habitat structure that seem relatively harmless may have a considerable negative effect beyond the immediate area of the perturbation because the disturbed habitat may become an ecological trap.

Ecological trap for desert lizards caused by anthropogenic changes in habitat structure that favor predator activity.

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.

Predator control of ecosystem nutrient dynamics.

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.

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

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 herbivoreâ€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 carbohydrateâ€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.

Physiological stress as a fundamental mechanism linking predation to ecosystem functioning.

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.

Fear of predation slows plant-litter decomposition.

It is widely held that herbivore growth and production is limited by dietary nitrogen (N) that in turn constrains ecosystem elemental cycling. Yet, emerging evidence suggests that this conception of limitation may be incomplete, because chronic predation risk heightens herbivore metabolic rate and shifts demand from N-rich proteins to soluble carbohydrate-carbon (C). Because soluble C can be limiting, predation risk may cause ecosystem elemental cycling rates and stoichiometric balance to depend on herbivore physiological plasticity. We report on a stoichiometrically explicit ecosystem model that investigates this problem. The model tracks N, and soluble and recalcitrant C through ecosystem compartments. We evaluate how soluble plant C influences C and N stocks and flows in the presence and absence of predation risk. Without risk, herbivores are limited by N and respire excess C so that plant-soluble C has small effects only on elemental stocks and flows. With predation risk, herbivores are limited by soluble C and release excess N, so plant-soluble C critically influences ecosystem elemental stocks flows. Our results emphasize that expressing ecosystem stoichiometric balance using customary C:N ratios that do not distinguish between soluble and recalcitrant C may not adequately describe limitations on elemental cycling.

Article	Year
Change your diet or die: predator-induced shifts in insectivorous lizard feeding ecology. Oecologia\| PubMed ID: 19466458	2009
Ecological trap for desert lizards caused by anthropogenic changes in habitat structure that favor predator activity. Conservation biology : the journal of the Society for Conservation Biology\| PubMed ID: 20337674	2010
Predator control of ecosystem nutrient dynamics. Ecology letters\| PubMed ID: 20602626	2010
Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proceedings of the National Academy of Sciences of the United States of America\| PubMed ID: 20713698	2010
Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. The American naturalist\| PubMed ID: 20846014	2010
Fear of predation slows plant-litter decomposition. Science (New York, N.Y.)\| PubMed ID: 22700928	2012
Predation risk, stoichiometric plasticity and ecosystem elemental cycling. Proceedings. Biological sciences / The Royal Society\| PubMed ID: 22896643	2012

Dror Hawlena

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