Quantifying fear effects on prey demography in nature

Abstract

In recent years, it has been argued that the effect of predator fear exacts a greater demographic toll on prey populations than the direct killing of prey. However, efforts to quantify the effects of fear have primarily relied on experiments that replace predators with predator cues. Interpretation of these experiments must consider two important caveats: (1) the magnitude of experimenter-induced predator cues may not be realistically comparable to those of the prey's natural sensory environment, and (2) given functional predators are removed from the treatments, the fear effect is measured in the absence of any consumptive effects, a situation which never occurs in nature. We contend that demographic consequences of fear in natural populations may have been overestimated because the intensity of predator cues applied by experimenters in the majority of studies has been unnaturally high, in some instances rarely occurring in nature without consumption. Furthermore, the removal of consumption from the treatments creates the potential situation that individual prey in poor condition (those most likely to contribute strongly to the observed fear effects via starvation or reduced reproductive output) may have been consumed by predators in nature prior to the expression of fear effects, thus confounding consumptive and fear effects. Here, we describe an alternative treatment design that does not utilize predator cues, and in so doing, better quantifies the demographic effect of fear on wild populations. This treatment substitutes the traditional cue experiment where consumptive effects are eliminated and fear is simulated with a design where fear is removed and consumptive effects are simulated through the experimental removal of prey. Comparison to a natural population would give a more robust estimate of the effect of fear in the presence of consumption on the demographic variable of interest. This approach represents a critical advance in quantifying the mechanistic pathways through which predation structures ecological communities. Discussing the merits of both treatments will motivate researchers to go beyond simply describing the existence of fear effects and focus on testing their true magnitude in wild populations and natural communities.

Consumptive and non‐consumptive effects of predators vary with the ontogeny of their prey

“…An important consideration when assessing the effects of fear on prey populations using predator cues is that the magnitude of those cues may be artificially enhanced by the experimental setup, making them difficult to compare with cues in the prey's natural environment (Peers et al. ). Turbulent, high‐flow conditions may rapidly dilute predator cues in aquatic environments, with prey showing low response levels to predator presence in field conditions compared to laboratory trials (Freeman , McKay and Heck , Harding and Scheibling ).…”

“…Chemical cues have been shown to trigger different behavioral responses in several species of sea urchin (Vadas and Elner 2003, Freeman 2006, Matassa 2010, Morishita and Barreto 2011, and seem to play a key role in subtidal ecosystems where invertebrates are important grazers (Haggerty et al 2018). An important consideration when assessing the effects of fear on prey populations using predator cues is that the magnitude of those cues may be artificially enhanced by the experimental setup, making them difficult to compare with cues in the prey's natural environment (Peers et al 2018). Turbulent, high-flow conditions may rapidly dilute predator cues in aquatic environments, with prey showing low response levels to predator presence in field conditions compared to laboratory trials (Freeman 2006, McKay and Heck 2008, Harding and Scheibling 2015.…”

“…Controlled laboratory studies are compelling, but they may overestimate the importance of non‐consumptive effects by artificially enhancing the detection threshold of predator chemical cues (Harding and Scheibling , Peers et al. ). Achieving a more nuanced understanding of the dynamics of predator effects in complex natural settings requires integrating how their strength varies across space and gradients of habitat complexity (Catano et al.…”

Population cycles in voles and lemmings: state of the science and future directions

“…, Peers et al. ), is amenable to experimental testing and should be tested in cyclic rodent populations (see also Appendix ). Results of a modelling study by Radchuk et al. () suggested that both intrinsic and extrinsic factors may be necessary to explain rodent population cycles adequately, yet few attempts have been made to test the multifactorial hypothesis due to logistical difficulties. It is widely accepted that population cycles are accompanied by several life‐history and behavioural traits that vary across cyclic phases.…”

Predation risks suppress lifetime fitness in a wild mammal

“…Untangling risk effects in wild populations requires controlling for bottom–up effects (Vucetich and Peterson , DeWitt et al ), yet individual condition, predation risk, and recruitment are rarely measured over the same spatial or temporal scales for wild mammals (Creel et al , Middleton et al ). Thus, while the nature and consequences of NCEs have been well described in elegant experimental systems (reviewed by Preisser et al 2005, Preisser and Bolnick , Schmitz et al ), few studies have explored how animals allocate resources to growth and reproduction under the risk of predation in natural ecosystems (Creel and Christianson , Peers et al ).…”