Ghosts of parasites past influence current non-consumptive effects in Drosophila nigrospiracula

Parasites can indirectly impact hosts through non-consumptive effects (NCEs) via changes in behaviour, morphology, and/or physiology. These responses can be understood in terms of the ecology of fear (ectoparasites) or the ecology of disgust (endoparasites) framework. We tested the hypothesis that NCEs of parasite exposure (e.g., parasite avoidance and defense) trade off with other important behaviours such as feeding and resting. We predicted that when exposed to parasites (without infection), hosts will increase their defensive behaviors at the expense of feeding. We also posited that history of exposure (without infection), or previous infection would impact the expression of these NCEs. The study system involves a cactophilic fruit fly (Drosophila nigrospiracula) and a naturally occurring parasitic mite (Macrocheles subbadius). First, we assessed how prior mite exposure affected fly behaviour in response to current parasite exposure. Mite presence resulted in increased grooming and movement, but exposure history did not affect these behaviours. However, the interaction between previous and current exposure influenced host feeding and resting behaviours. We found that previously exposed flies increased feeding and decreased resting upon a secondary mite exposure. In a second experiment, we tested the role of infection history on current parasite exposure. Compared with naïve flies, previously infected flies were expected to increase defensive behaviours upon secondary exposure. Flies increased defensive and ambulatory behaviour in the presence of mites, and consequently less time was spent resting but feeding was unaffected. None of the behaviours measured were affected by previous infection status. In general, current parasite exposure resulted in NCEs. Moreover, our results showed that previous exposure (without infection) to parasites may have an even stronger effect upon secondary exposure than infection history. Our study highlights the importance of the ecology of fear and the role that exposure and infection history plays in generating NCEs of parasitism.