Current parasite resistance trades off with future defenses and flight performance

Many animals use behavioral defenses such as grooming to avoid or mitigate the negative effects of infection by ectoparasites. Grooming can be energetically costly and may trade off with other host activities. We hypothesize that self-grooming comes at a cost and, therefore, compromises future parasite resistance and other energetically expensive activities, namely flight. We measured the rates of CO2 production (respiration is a proxy for energetic costs) in Drosophila nigrospiracula induced to groom with a non-pathogenic irritant (volcanic ash), allowing us to disentangle the cost of grooming from the cost of infection. The respiration rate of flies induced to groom was significantly higher compared to flies at rest. Results show that flies that spent time grooming, induced by an irritant, had higher average infection intensities upon subsequent exposure to the ectoparasitic mite Macrocheles subbadius. Additionally, flies induced to groom with an irritant suffered a similar to 30% reduction in flight performance compared to flies previously at rest, suggesting reduced ability to escape infested habitats. Lastly, we compared the behavioral response of flies to ectoparasites and irritants, as flies may be specific in their response to different types of threats. Behavioral observations revealed that flies exposed to an irritant increased self-grooming behavior and decreased movement (potentially suggesting reduced escape behavior), whereas flies exposed to mites exhibited increased ambulatory movement as well as increased grooming behavior. Overall, time spent grooming made flies more vulnerable to future infection and decreased flight endurance, a metric of dispersal capability. Significance statement Behavioral defenses are a major method by which animals defend themselves against ectoparasites. However, these defenses, such as rapid movement and intensive grooming, are often energetically costly. This study measures the energetic cost of grooming in Drosophila nigrospiracula and the knock-on effects on future parasite resistance and flight endurance. We measured the energetic cost of grooming using respirometry and observed that flies induced to groom with a non-pathogenic irritant were less able to defend themselves against future mite attack and had reduced flight endurance, likely due to energetic trade-offs. Our results suggest grooming reduces energy available for other energetically demanding activities. As dispersal can limit the long-term impacts of parasites, these trade-offs may indicate a broader trade-off between current and future parasite defense.