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How and to what degree an animal deals with potential threats is a fascinating topic that has been well-researched, particularly in insects, though usually not with the impact of parasites in mind. A growing body of work is showing how even benign parasites can affect, positively or negatively, their hosts’ physiological or behavioral reaction to threats. With this in mind we conducted an experiment using horned passalus beetles, Odontotaenius disjunctus that were naturally parasitized with a nematode Chondronema passali; we subjected beetles to simulated attacks (resembling rival fighting or predator attacks) and from videos of the encounters we quantified a suite of behaviors (antennae movement, aggressive posturing, threat displays, etc.), plus rates of alarm calls (stridulations) which all correspond to the “fight or flight” reaction. We obtained behavioral and parasite data from 140 beetles from two field collections, of which half had been housed in our lab for three weeks in conditions that would be stressful (little cover for burrowing). We observed a wide range of behaviors during the simulated attack procedure, from beetles offering little resistance to those which were extremely aggressive, though most beetles showed a moderate reaction. Alarm calling rates also varied, but surprisingly, these were not correlated with the magnitude of behavioral reactions. Also surprising was that stressful housing did not heighten the physical resistance during attacks, but did elevate alarm calling rate. Importantly, parasitized beetles had significantly reduced physical reactions to attack than those without nematodes (meaning their resistance to the attack was muted). The results concerning parasitism, coupled with prior work in our lab, indicate that the C. passali nematode depresses the hosts’ acute stress, or fight or flight, reaction (likely from its energetic cost), which may make hosts more susceptible to the very dangers that they are coping with during the stress events.
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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.
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- Award ID(s):
- 1659683
- PAR ID:
- 10406849
- Editor(s):
- Lutermann, Heike
- Date Published:
- Journal Name:
- PLOS ONE
- Volume:
- 18
- Issue:
- 3
- ISSN:
- 1932-6203
- Page Range / eLocation ID:
- e0281149
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pone.0281149
