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.