The magnitude of contingency
To quantify strength of contingency in NCEs, we conducted a
meta-analysis of the relationship between four types of prey risk taking
and a key hypothesized driver of context dependence: prey energetic
state (Kotler et al . 2004; Schmitz & Trussell 2016; seeBox 3 for methods). Reduced energetic state resulted in
significantly elevated prey risk taking in each behavioral dimension
(Fig. 4 ). When in a compromised energetic state, prey subjected
to predation risk tended to be more active (d = 0.73, ± 95% CI =
0.32-1.14; lnRR = 0.34, ± 95% CI = 0.17-0.51), spend less time in
refugia (d = 0.95, ± 95% CI = 0.74-1.16; lnRR = 0.58, ± 95% CI
= 0.46-0.71), invest more in foraging versus apprehension (d =
0.84, ± 95% CI = 0.50-1.19; lnRR = 0.49, ± 95% CI = 0.22-0.77), and be
more isolated from other group members (d = 0.86, ± 95% CI =
0.29-1.42; lnRR = 0.42, ± 95% CI = 0.19-0.65) than conspecifics in
better nutritional condition. The mean estimates of d suggest a
medium/strong effect of reduced energetic state on prey activity, and
strong effects on exposure, foraging investment, and isolation. We
detected significant heterogeneity among studies exploring each
risk-taking dimension: activity (d : Q 33 =
178.39, p < 0.001; lnRR: Q 33 = 88.04, p
< 0.001); exposure (d : Q 70 =
213.60, p < 0.001; lnRR: Q 70 = 369.66,
p < 0.001); foraging investment (d :Q 40 = 186.19, p < 0.001; lnRR:Q 40 = 924.42, p < 0.001); isolation
((d : Q 9 = 34.85, p < 0.001;
lnRR: Q 9 = 57.06, p < 0.001).
These results underscore the marked differences that can characterize
risk taking by prey individuals with divergent energetic states, and by
extension the pivotal role that prey condition plays as a mediator of
direct NCEs in communities. Most of the studies included in this
analysis examined small-bodied taxa in laboratory or small-scale
mesocosm settings (Appendix S1 in Supporting Information), and we found
few investigations of the indirect community consequences of
state-mediated variation in prey risk taking. Accordingly, there remains
need for studies quantifying the influence of energetic state on risk
taking under field conditions, especially with larger-bodied species,
and the degree to which disparate responses of prey in divergent
nutritional states shape indirect predator NCEs. Furthermore, prey state
was the only potential driver of contingency in prey anti-predator
behavior subject to enough empirical investigation to support
meta-analysis. Thus, we also encourage further work addressing other
potential drivers of context dependent NCEs.
Our findings also revealed considerable variability in the magnitude and
direction of the effect of prey condition on anti-predator behavior.
Some studies in each of the four behavioral categories showed effects
opposite the majority of studies. In these studies, anti-predator
behavior increased with decreasing body condition or state of the prey
(7 of 34 studies of activity; 7 of 71 for exposure; 5 of 41 for foraging
investment; 1 of 10 for isolation). This variability may, in part, stem
from the myriad means by, and circumstances under, which the experiments
of the meta-analyses were conducted. The variability in results is also
consistent with the idea that, during phase two, anti-predator behavior
and the way it is shaped by context (including prey state) hinge on the
relative safety benefits conferred by different behavioral options
available to the prey species. Either increased or decreased activity,
for example, can serve as effective anti-predator tactics depending on
the hunting mode of the predator against which they are deployed
(Schmitz 2007). Furthermore, if individuals in a low state are more
vulnerable to predation, then they may adopt a higher level of
antipredator investment (Raveh et al . 2011; Makon et al .in press ). It is not surprising, then, that some studies we
assessed found that sated prey exposed to predation risk became more
active, and that food restriction diminished rather than exacerbated
this response (e.g., Hossie & Murray 2011). Though beyond the scope of
this review, meta-regressions with covariates potentially influencing
the efficacy of different anti-predator behaviors (e.g., predator type)
would likely reduce some of the uncertainty characterizing our findings.