Box 1: Space and Time
Predator-prey and parasite-host interactions both require temporal and spatial overlap between the victim and the natural enemy. Hosts must encounter other infected hosts or parasite transmission stages to allow transmission, while predators must encounter their prey to kill and eat them. Predator-prey-parasite interactions can increase parasitism in prey by increasing the spatio-temporal overlap between prey and their parasites. In heterogeneous landscapes where parasites are deposited unequally across space, predator interference can increase the extent to which parasite deposition overlaps with areas of prey space-use through both sloppy predation and parasites passing through predators (Cácereset al. 2009; Strauss et al. 2016; Duffy et al.2019; Lopez & Duffy 2021); facilitation of prey-parasite spatio-temporal overlap by the predator generally requires strong spatio-temporal overlap between that predator and infected prey.
However, the presence of predators can influence parasitism in prey even without regular spatio-temporal overlap between prey and predators (Clinchy et al. 2013). If prey and predators occupy the same areas at different times, then predator cues can have profound behavioral and physiological effects on parasitism in the prey even without any direct interactions. However, the extent of these effects is typically limited by the spatial scale and temporal duration of predator cues and the duration of parasite persistence in the environment. Highly localized predator cues (such as feces in terrestrial systems) may require far finer scale spatial overlap between prey and predator than more diffusible cues (such as predator kairomones in an aquatic system). Likewise, durable predator signals (such as a strong chemical cue) require less temporal overlap between prey and predator than more ephemeral signals (such as auditory cues). These behavioral effects of predators, themselves, may alter the space-use of prey in ways that result in increased spatiotemporal overlap with parasites or infected prey. Similarly, parasites which persist longer in the environment are more likely to be encountered by prey than those with limited environmental viability, making predator spreader effects persist longer for these parasites.
The flexibility in the extent of spatiotemporal overlap required for predator-prey-parasite interactions — as well as the way in which the interaction itself alters spatiotemporal patterns of both prey and parasites — may make detecting patterns and inferring causal mechanisms challenging in some systems. Therefore we recommend careful study of the locations and time periods during which contact between prey and parasites occur both to improve predictions about the potential effect of predators on those spatio-temporal overlaps and to aid in measuring mechanistic intermediary factors between predator presence and parasite outcomes.