Sex-specific effects of a parasite on stress-induced freezing behavior in a natural beetle-nematode system

Some animals react to predation threats or other stressors by adopting a freezing posture in an attempt to avoid detection, and the duration of this behavior usually corresponds with individual personality, such that timid individuals freeze longer. Despite decades of research on this or related behaviors (thanatosis), never has the impact of parasitism been considered. Parasites could prolong the duration, if hosts are less motivated to move (i.e. lethargic), or they could reduce it, if hosts are motivated to forage more to compensate for energy drain. We examined this behavior within a natural beetle-nematode system, where hosts (horned passalus beetles, Odontotaenius disjunctus) are parasitized by a nematode, Chondronema passali. We exposed beetles (n = 238) to four stressors in our lab, including noise, vibration, light and inversion, and recorded how long they adopt a frozen stance. Afterward, we determined nematode burdens, which can range from dozens to hundreds of worms. Beetles tended to freeze for 20 seconds on average, with some variation between stressors. We detected no effect of beetle mass on the duration of freezing, and this behavior did not differ in beetles collected during the breeding or non-breeding season. There was a surprising sex-based difference in the impact of nematodes; unparasitized females remained frozen twice as long as unparasitized males, but for beetles with heavy nematode burdens, the opposite was true. From this we infer that heavily parasitized females are more bold, while males with heavy burdens would be more timid. The explanation for this finding remains elusive, though we can rule out many possibilities based on prior work on this host-parasite system.