Changes in prey physiology/immunity
Prey responses to predator presence extend beyond the behavioral to the
physiological, and these physiological changes can produce additional
non-consumptive effects of predators on parasites. Prey often decrease
foraging behavior in favor of hiding or vigilance in response to
predators (Brown et al. 1988; Jones & Dornhaus 2011; Thaleret al. 2012; Creel et al. 2014). Predator presence also
frequently increases hormonal stress levels in prey organisms (Clinchyet al. 2011, 2013; Middlemis Maher et al. 2013; Cinelet al. 2020). Both decreased nutrition and increased stress have
been shown to have negative effects on organismal immune function which
can in turn increase susceptibility to parasites (Hamilton 1974; Navarroet al. 2004; Martin 2009; Viney & Riley 2014; Strandin et
al. 2018). This results in a functional tradeoff between predator and
parasite response in prey organisms (Navarro et al. 2004; Ottiet al. 2012; Adamo et al. 2017). For example, house
sparrows exposed to barn-owl predators had a reduced T-cell-mediated
immune responses and higher prevalence and intensity ofHaemoproteus malarial infection in separate experiments (Navarroet al. 2004). However, complex immune system interactions are not
required for physiology mediated predator spreading. For example,
predator kairomones induce Daphnia dentifera to grow larger and
mature faster which in turn makes them more susceptible to infection by
their yeast parasite (Duffy et al. 2011; Yin et al. 2011).
We predict that physiologically mediated predator spreading will be most
evident where prey have large physiological or stress responses to
predator presence leading to a diversion of resources away from immune
function. Operationalizing this prediction requires an extensive
understanding of prey physiology in order to identify systems in which
predator stress downregulates immune function. However, there are a few
heuristics that can be applied. In particular, predators with ambush or
sit-and-wait predation strategies tend to be perceived as a larger
threat/stressor than ranging predators, leading to a larger
physiological response (Preisser et al. 2007; Clinchy et
al. 2011, 2013). Additionally prey that are highly energy- and/or
nutrient-limited even in the absence of predators are more likely to
suffer physiological effects from the introduction of predators (Creel
& Christianson 2008).
Ideal systems for the study of physiologically mediated
predator-spreading are those in which physiological effects of predation
are already well characterized and those in which predator presence can
be manipulated without consumptive predation (e.g., by using a caged
predator or a predator that has been rendered incapable of attacking
prey, or by using predator chemical cues; e.g. Schmitz et al.1997; Duffy et al. 2011; Szuroczki & Richardson 2012; Buss &
Hua 2018; Flick et al. 2020). Experiments in particular require
measuring not just the predator effect on a parasite response but also
the effect of predator exposure on at least one physiological
intermediary. Easier to measure non-invasive intermediary metrics
include body condition and fecal stress hormones (Palme et al.2005; Sánchez et al. 2018) but ideally a study would measure both
this type of proximate response to predators and the ultimate effect of
predation stress on immune function. Such experiments are likely to be
expensive and time intensive but hold the key to a potentially
underestimated type of predator spreading.