Conclusions and future directions
In a recent review of context-dependent species relationships,
Chamberlain et al . (2014) called for increased scrutiny of the
factors contributing to, and the ecological and evolutionary
consequences of, variation in interaction outcomes. Focusing on
non-consumptive predator-prey interactions, we address both of these
knowledge gaps. First, we present new insights into NCEs by showing when
and how contingency can arise from properties of the prey, the predator,
and the setting as these effects unfold across three phases (prey risk
perception; prey responses to perceived risk; impacts of these responses
on other species). Second, while recognizing that there is more work to
be done, we help to unravel the consequences of contingency by
quantifying the extent to which prey energetic state drives differences
in anti-predator behavior, and by spotlighting cases where variation in
the outcome of non-consumptive predator-prey interaction has shaped the
indirect NCEs experienced by other community members. Our synthesis also
highlights two knowledge deficiencies – insufficient exploration of
context-dependent indirect NCEs during phase three and the ways in which
direct and indirect NCEs are shaped simultaneously, or even
interactively, by multiple drivers of context dependence – that must be
remedied if we are to develop a coherent framework for predicting NCEs.
Drawing from a broad literature spanning diverse taxa and ecosystems,
our review reveals how contingencies in NCEs can arise as a result of
many factors. It is hardly surprising, then, that studies have revealed
so much variation with respect to whether, and in what way, NCEs
manifest in communities (Moll et al . 2016; Schmitz 2017; Gaynoret al . 2019; Prugh et al . 2019). We clarify these factors
by grouping them into three broad categories: (1) prey properties that
influence detection of and responses to risk; (2) predator properties
shaping their detectability and lethality; and (3) properties of the
setting that influence the prey’s scope for predator detection and
countermeasures. We also emphasize that there is great potential for
interplay among them. For example, divergent responses to predators with
disparate hunting modes could disappear if declining food supply limits
prey capacity for defensive investment. Similarly, because prey often
have multiple defenses whose efficacies are context-specific (Brittonet al . 2007; Wirsing et al . 2010; Wirsing & Ripple 2011;
Schmitz 2017; Creel 2018), sympatric prey may respond divergently to a
shared predator in one setting but similarly in another, depending on
the availability of landscape features that facilitate particular
responses (e.g., refuge space). Moreover, the latter two give rise to an
emergent fourth driver, (4) the timing of predation risk, and prey
properties then determine how individuals respond to this temporal
dimension of danger (Box 2 ). By implication, predictions based
on a single driver of contingency may provide an incomplete picture of
the impacts of predation risk on prey populations and communities.
Rather, examination of NCEs requires thorough consideration of the
functional properties of interacting predator and prey species, as well
as the circumstances under which these interactions occur (Heithauset al . 2009; Wirsing et al . 2010; Creel 2011;
Schmitz 2017). Fortunately, many of these natural history or
environmental details are available or attainable (Wirsing et al .
2010), especially given new approaches (e.g., animal-borne video, camera
traps, drones) that facilitate placing behavioral data in context (Mollet al . 2007; Wirsing & Heithaus 2014).
Our review also highlights the staged manner in which NCE contingencies
can manifest. Namely, prey anti-predator investment may vary intra- and
inter-specifically as a function of differences in sensory perception
(phase one) and the form of any deployed countermeasures (phase two);
contingent outcomes during either of the first two phases then determine
if, and in what way, indirect NCEs emerge during phase three.
Identifying the phase(s) in which context dependence arises is therefore
crucial to predicting how the outcome of non-consumptive predator-prey
interactions will respond to perturbation. For example, landscape
changes that constrain prey habitat domains and raise the frequency of
encounters with predators may elicit increased anti-predator defense
during phase two (Schmitz et al . 2004; 2017a) and thereby elevate
the potential for indirect NCEs in phase three. However, such changes
would be expected to have minimal non-consumptive impact on prey species
lacking the ability to detect risk cues during phase one, unless they
also reshape the sensory environment. Thus, studies exploring the
phase-specific mechanisms by which prey, predator, and landscape
properties shape anti-predator investment will strengthen a general
framework for forecasting NCEs in a changing world.
Recent syntheses have quantified the degree to which NCEs vary as a
function of resource competition (Bolnick & Preisser 2005), predator
hunting mode and habitat domain (Preisser et al . 2007), resource
dynamics (Preisser et al . 2009), and refuge availability (Orrocket al . 2013). The results of our meta-analysis add prey energetic
state to the growing list of drivers whose strong impact on the outcomes
of NCEs has been quantified across systems and taxa. Notably, our
findings differ somewhat from those listed above because we addressed
multiple forms of antipredator behavior and only chose experiments
explicitly contrasting responses of prey individuals with different
energetic states to risk. Hence, we offer novel insights into the
manifold ways in which energetic state can shape patterns of
anti-predator investment under conditions where the potentially
confounding effects of differing environments and other prey traits have
been minimized. Our findings also highlight the varied ways by which
state-dependent variation in anti-predator behaviors might influence the
manifestation of indirect NCEs during phase three – for example via
differences in vigilance or space use – though these hypothetical
scenarios remain to be evaluated empirically.
Our survey revealed two knowledge gaps that represent fruitful
directions for future research. First, whereas there is ample evidence
for context dependence during phases one and two, few studies have
rigorously examined contingency in the propagation of indirect NCEs.
There are notable examples, including the role of predator hunting mode
in shaping indirect NCEs of spiders on plant and soil properties
(Schmitz et al . 2017b), and the impact of the presence or absence
of prey refugia on indirect non-consumptive relationships between crabs
and barnacles (Trussell et al . 2006). These studies offer a
template for expanded scrutiny of contingencies in NCEs during phase
three, which will improve our understanding of when and how predators
initiate indirect effects by altering prey traits.
Second, a growing literature underscores the importance of
simultaneously considering multiple drivers of contingency in NCEs. For
example, anti-predator investment by mud crabs varied with their
personality (bold versus shy) and predator hunting mode (actively
hunting blue crabs versus sit-and-wait toadfish, Opsanus tau )
(Belgrad & Griffen 2016). Working in a large vertebrate system, Thakeret al . (2011) showed that small members of an African ungulate
guild avoided all predators whereas their larger counterparts avoided
sit-and-pursue but not active hunters. More work is needed, however,
particularly on the importance of three-way interactions among factors
drawn from the aforementioned groups.
There are also studies suggesting that interactive impacts of multiple
contingent drivers may act collectively to shape indirect NCEs during
phase three. For example, Murie & Bourdeau (2019) speculated that,
compared to the strong effects initiated by slow-moving sea stars, the
absence of direct and indirect non-consumptive effects of crabs and
octopuses on snail grazing and kelp, respectively, might owe to the
inability of snails to escape these vagile predators. By inference, more
mobile prey species with greater scope for avoidance may have responded
equivalently to all three predators, yielding similar rather than
predator-specific cascades of NCEs. The possibility that interactions
between context dependent factors might modify cascading NCEs has yet to
be tested empirically, however, and thus remains as an exciting research
frontier.