Parasites reduce host fitness via perturbations to host energy allocation, growth, survival, and reproduction. Here, we investigate the independent effects of parasite exposure and infection on host metabolic rate. Our study focuses on Drosophila hydei and a naturally occurring ectoparasitic mite, Macrocheles muscaedomesticae. We use flow-through respirometry to measure the metabolic rate of flies during the period of exposure (preinfection) and during mite attachment. Flies were exposed to mites either indirectly (through a mesh screen) or directly, allowing for physical contact between the fly and the mite. We predicted that fly metabolic rate would increase with the level of parasite exposure: unexposed flies < flies with indirect exposure to mites < flies with direct contact with mites < flies actively infected with mites. As expected, flies indirectly exposed to but not in direct contact with mites produced 70% more CO than unexposed flies. Flies in direct contact with mites produced 35% more CO than flies with indirect contact, and this was more than double the amount of CO produced by unexposed flies. However, infected flies-those actually carrying mites-did not produce significantly more CO than uninfected flies. Our results show that simply being exposed to mites, either indirectly or directly, was sufficient to elicit a response from the host in terms of elevated CO production. Our results show that the costs of parasitism can potentially extend beyond the physiological costs of infection per se to include the energetic costs associated with parasite avoidance. Although studies have shown energetic costs associate with predator-avoidance behaviors, no study to our knowledge has measured the metabolic cost of parasite avoidance.

1. Dispersal is essential for locating mates, new resources, and to escape unfavourable conditions. Parasitism can impact a host's ability to perform energetically demanding activities such as long-distance flight, with important consequences for gene flow and meta-population dynamics.2. Ectoparasites, in particular, can adversely affect host flight performance by diminishing flight aerodynamics and/or by inflicting physiological damage while feeding on host tissue.3. Experimental flight assays were conducted using two fruit fly-mite systems: Drosophila nigrospiracula (Patterson and Wheeler) -Macrocheles subbadius (Berlese) and D. hydei (Sturtevan) -M. muscaedomesticae (Scopoli). Flies that are burdened by mites are expected to exhibit lower flight endurance compared to uninfected flies.4. The results show that the presence of mites (attached) significantly decreased flight endurance by 57% and 78% compared to uninfected D. nigrospiracula and D. hydei, respectively. The physiological damage caused by M. subbadius was revealed through a 53% decline in flight time among previously infected flies (mites removed just prior to flight assay). Surprisingly, the presumably phoretic M. muscaedomesticae also caused a 62% reduction in flight endurance among previously infected D. hydei.5. These results suggest a strong deleterious effect of ectoparasitic mites on host flight performance, mediated by a reduction in flight aerodynamics and damage to host physiology. Adverse effects on host flight and/or dispersal may have broad implications for gene flow, population genetic structure, and local adaptation in both host and parasite meta-populations.

Habitat avoidance is an anti-parasite behaviour exhibited by at-risk hosts that can minimize exposure to parasites. Because environments are often heterogeneous, host decision-making with regards to habitat use may be affected by the presence of parasites and habitat quality simultaneously. In this study we examine how the ovipositing behaviour of a cactiphilic fruit fly, Drosophila nigrospiracula, is affected by the presence of an ectoparasitic mite, Macrocheles subbadius, in conjunction with other environmental factors – specifically the presence or absence of conspecific eggs and host plant tissue. We hypothesized that the trade-off between site quality and parasite avoidance should favour ovipositing at mite-free sites even if it is of inferior quality. We found that although flies avoided mites in homogeneous environments (86% of eggs at mite-free sites), site quality overwhelmed mite avoidance. Both conspecific eggs (65% of eggs at infested sites with other Drosophila eggs) and host plant tissue (78% of eggs at infested sites with cactus) overpowered mite avoidance. Our results elucidate the context-dependent decision-making of hosts in response to the presence of parasites in variable environments, and suggest how the ecology of fear and associated trade-offs may influence the relative investment in anti-parasite behaviour in susceptible hosts.

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Parasites are known to have direct negative effects on host fitness; however, the indirect effects of parasitism on host fitness sans infection are less well understood. Hosts undergo behavioural and physiological changes when in proximity to parasites. Yet, there is little experimental evidence showing that these changes lead to long-term decreases in host fitness. We aimed to determine if parasite exposure affects host fitness independent of contact, because current approaches to parasite ecology may underestimate the effect of parasites on host populations. We assayed the longevity and reproductive output of Drosophila nigrospiracula exposed or not exposed to ectoparasitic Macrocheles subbadius. In order to preclude contact and infection, mites and flies were permanently separated with a mesh screen. Exposed flies had shorter lives and lower fecundity relative to unexposed flies. Recent work in parasite ecology has argued that parasite-host systems show similar processes as predator-prey systems. Our findings mirror the non-consumptive effects observed in predator-prey systems, in which prey species suffer reduced fitness even if they never come into direct contact with predators. Our results support the perspective that there are analogous effects in parasite-host systems, and suggest new directions for research in both parasite ecology and the ecology of fear.