Properties of the setting
Both prey and predator traits crucially predict the outcome of their
non-consumptive interactions. Additionally, the propagation of NCEs
depends also on the setting in which the interaction takes place. During
phase one, changes to the environment may impair prey detection of
predator cues by disrupting acoustic (e.g., owing to anthropogenic
noise; Chan et al . 2010), chemosensory (e.g., because of
pollution; Lürling & Scheffer 2007), or visual (e.g., via increased
turbidity; Abrahams & Kattenfield 1997) systems. These environmental
changes may reduce the likelihood of, or even preclude, anti-predator
behavior. For example, predator avoidance by freshwater snails
(Physa acuta , Helisoma trivolvis ) disappeared when
eutrophication of their outdoor mesocosms led to chemosensory impairment
(Turner & Chislock 2010). Environmental features that impede predator
detection may themselves be recognized as risk cues by prey and thereby
result in elevated defensive investment. For example, Embar et
al . (2011) demonstrated that gerbils (Gerbillus andersoni
allenbyi ) reduced their foraging activity (measured by GUDs) when
landscape features blocked sightlines that were necessary for
anti-predator vigilance. In general, then, environmental heterogeneity
with respect to properties that influence predator detection may mediate
substantial inter-individual and population variation in the degree to
which prey recognize predation danger and subsequently experience and
transmit NCEs.
During phase two, properties of the setting may influence the scope for
prey anti-predator behavior in several ways. First, predator and prey
habitat domains are shaped in part by environmental context (e.g.,
thermal conditions, vegetative structure; Schmitz & Barton 2014).
Accordingly, environmental factors constraining prey movement or the
amount of predator-free space could dictate whether prey manifest
chronic anti-predator vigilance, use refugia, or experience consumptive
effects under the four contingent scenarios described above. Barton &
Schmitz (2009) showed, for example, that experimental warming created
enemy-free space by shifting the environment from one where two spider
predators were spatially complementary to overlapping. This led to a
strictly non-consumptive interaction whereby grasshoppers avoided
predators rather than a composite scenario where they avoided the
sit-and-wait predator but experienced consumptive effects of the active
hunter.
Second, even when predator and prey domains are unaffected by the
setting, landscape features can shape NCEs by modifying the efficacy of
prey escape behavior. The ability of an individual to escape a predator
following an encounter can depend on environmental factors that
influence mobility (e.g., terrain) or visibility (e.g., when the
background affects prey camouflage) (Wirsing et al . 2010). Thus,
areas with properties that render prey escape tactic(s) less effective
are likely to be avoided, at least when predators are present, or to
elicit other countermeasures that enhance the probability of early
predator detection (e.g., vigilance). For instance, reef habitat
complexity enhanced and dampened anti-predator behaviors of large and
small fishes, respectively, likely because large-bodied fish are less
able to flee from predators through obstacle-rich reefscapes than their
smaller counterparts (Catano et al . 2016).
Third, food quantity or quality at the landscape scale can shape NCEs by
influencing the mean energetic state of prey populations (Heithauset al . 2008; Wirsing & Ripple 2011). In depauperate landscapes,
average energetic states will be depressed and the overwhelming
necessity of food should drive foraging decisions (Chesson & Kuang
2008), whereas anti-predator investments should increase when resources
are plentiful and prey have nutritional reserves (Hopcraft et al .
2010; Matassa & Trussell 2014). For example, Matassa et al .
(2016) found that elevated resource (barnacle, Semibalanus
balanoides ) density strengthened anti-predator investment (refuge use)
by sub-adult snails (Nucella lapillus ) exposed to risk cues from
predatory crabs (Carcinus maenas ), presumably by augmenting prey
state.
Fourth, interacting predator-prey pairs are unlikely to do so in
isolation from other species, which may alter the focal prey species’
responses to perceived risk. For instance, dwarf mongooses
(Helogale parvula ) displayed lower rates of anti-predator
vigilance when in the presence of an avian co-forager, the drongo
(Dicrurus adsimilis ) (Sharpe et al . 2010). The presence of
other predators may also affect the transmission of NCEs if prey species
with conflicting predator-specific responses consequently reduce their
investment in defense (Sih et al . 1998). In accord with predator
facilitation (Charnov et al . 1976; Kotler et al . 1992;
Korpimaki et al . 1996), for example, Meadows et al . (2017)
showed that larval mosquitoes (Culex pipiens ) abandoned diving
behavior normally deployed to escape surface-hunting insect
mesopredators when also exposed to a benthic predator (dragonfly naiads,Aeshna spp.).
Lastly, landscape properties may mediate how prey are affected by
temporal variation in predation risk (Box 2 ). Many nocturnal
animals, for example, decrease their activity on moonlit nights because
of their increased exposure to visually-orienting predators, and this
trend is accentuated in areas dominated by open habitats (Prugh &
Golden 2014). Therefore, moonlight exacerbation of NCEs experienced by
nocturnal prey species is likely to be inversely proportional to
landscape cover availability. Landscapes also may influence temporal
patterns of predation risk, and thus NCEs, over longer intervals.
Seasonal variation in snow accumulation, for example, can give prey a
temporary refuge or heighten vulnerability to predation by restricting
mobility (Gorini et al . 2011). Not surprisingly, snow depth has
been linked to prey risk taking (e.g., yarding in deer; Nelson & Mech
1991).
Any of these environmental attributes, alone or in concert, can
influence the kinds of anti-predator behaviors that manifest during
phase two and that precipitate as indirect NCEs during phase three
(Heithaus et al . 2009; Wirsing & Ripple 2011). Thus, direct and
indirect non-consumptive relationships between the same suites of
interacting predator and prey species may differ markedly as a function
of landscape type. Trussell et al . (2006) determined, for
example, that habitat type (availability of refugia) shaped how risk
from crabs (Carcinus maenas ) altered the foraging intensity of a
snail (Nucella lapillus ) and, consequently, the levels of
consumption of the snails’ resource (S. balanoides ).