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.