DOI: 10.5061/dryad.fxpnvx0qf
title: Broadening the ecology of fear: non-lethal effects arise from diverse responses to predation and parasitism

description: The ecology of fear demonstrates how prey responses to avoid predation
 cause non-lethal effects at all ecological scales. Parasites also elicit
 defensive responses in hosts with associated non-lethal effects, which
 raises the longstanding, yet unresolved question of how non-lethal effects
 of parasites compare with those of predators. We developed a framework for
 systematically answering this question for all types of predator and
 parasite systems. Our framework predicts that trait responses and their
 non-lethal effects should be strongest from predators and parasites that
 do not kill individuals to feed on them, but which nevertheless damage
 fitness. Analysing trait response data on amphibians, which have been
 well-studied for this area of research, showed that individuals generally
 responded more directly to short-term predation risks than to parasitism.
 Apart from studies using amphibians, there have been few direct
 comparisons of responses to predation and parasitism, and none have
 incorporated responses to micropredators, parasitoids, or parasitic
 castrators, or examined their long-term consequences. Addressing these and
 other data gaps highlighted by our general framework can advance the field
 toward understanding how non-lethal effects shape real food webs, which
 contain multiple predator and parasite species.
description: Data
 were compiled as part of a systematic review with the aims to (a) assess
 the breath of empirical studies to directly compare trait responses to
 predators and parasites, and (b) seek support for the predictions emerging
 from our general trait response framework.
 We searched for
 literature using Google Scholar and Web of Science, using combinations of
 terms describing consumers (consumer, predat*, parasit*, anti-parasit*,
 anti-predat*, infect*, natural enemy), resources (host, prey, resource),
 traits (behavio*, activity, space use, refuge use, feeding, development),
 and effects (non-lethal, sub-lethal, risk, trait-mediated, trait response,
 indirect).   initiated our search on 10 January 2017 and continued to
 monitor the literature until the time of manuscript submission. 
 considered journal articles that met three criteria:
 measured traits
 associated with defense in an animal exposed to a predator cue. Cues
 included media (e.g. water) used by a predator , a consumed conspecific ,
 a predator kept behind a barrier (e.g. mesh cage), or an unrestrained
 predator. measured the same trait
 response (in the same resource species and life stage, but not necessarily
 the same individuals) to 1) a parasite cue, such as media previously
 containing infected hosts or infective stages or direct exposure to
 parasite infective stages, or 2) in animals infected with
 parasites. 3. had
 a control, wherein defense traits were measured in individuals that were
 not exposed to either a parasite or predator cue. 
 We did
 not include studies of trade-offs between predation and parasitism that
 used infection (in the case of predator effects) or predation (in in the
 case of parasite effects) as response variables because different traits
 were measured between “predator” and “parasite” treatments, and therefore
 were not comparable. We used the
 <i>digitize</i> package in R to extract data from figures. We
 recorded the number of replicates as ll as the mean and variance (SE or
 SD) of the response variables separately for controls, predator
 treatments, and parasite treatments. Studies often included a treatment
 containing both a predator and parasite cue (hereafter referred to as
 ‘combined’). We recorded these treatments as separate entries, with
 independent sample sizes, means, and variances. For studies that measured
 responses in multiple resource species and/or for multiple traits, we
 treated each species and trait as a different entry. When data were
 recorded across multiple days, we pooled data to calculate a single
 response mean and variance. We also pooled data from any additional
 treatments that varied factors such as consumer density or exposure
 frequency, and again calculated the response mean and variance for
 predator, parasite and, when applicable, combined treatments.