Landscape of fear in disease ecology: Do parasites have a larger impact than predators?

Prey species modify their distribution, movement, behaviour, or diet to minimize predation risk, while often compromising food intake. These indirect costs are large, may incur fitness costs, and often outweigh the direct costs of predation. Predation risks vary spatially and hence prey adapt to these spatial differences, and live in a so-called landscape of fear. Host-parasite interactions are in many ways similar to predator-prey interactions. Given these similarities, we reviewed to what extent new insights from this concept of the landscape of fear can be applied in disease ecology, as parasitic infections have large indirect costs and fitness consequences for hosts too. Hosts modify their spatial distribution, their activities, and their food intake, in an effort to reduce infection risk. Hosts trade-off foraging, predation risk, and infection risk. For instance, living in groups, a common strategy to decrease predation and increase food intake, increases infection risk. Spatio-temporal changes in distribution and behaviour of host species may shape community structure, and parasitism can thereby trigger cascading effects, affecting species diversity and population dynamics at lower trophic levels. Parasites may even act as ecosystem engineers, similar to predators. These large indirect effects of parasitic infections are species- and scale-dependent, and environmental variables, such as latitude, rainfall, and humidity, strongly influence parasite effects on hosts. We hypothesize that (i) the foraging – predation – infection trade-off is expected to show broad geographical patterns, with more disease risk prone behaviour in areas with a lower parasite risk. Since immune responses are species-specific and correlated with life-history traits such as body size, we also hypothesize that (ii) infection risk has a lower weight in the predation- foraging – infection risk trade-off for larger species, and that (iii) smaller species are strongly affected by spatial and temporal differences in infection risk. Moreover, as parasites influence both predator and prey, and as parasitic infections occur more frequently but are less fatal than predation attempts, we expect that parasites have a larger influence on the landscape than fear for predators (iv). We formulated several other hypotheses on the basis of the principles underlying the foraging – infection – predation trade-off, to test the application of insights from prey-predator theory to disease ecology.