Cold hardening improves larval tick questing under low temperatures at the expense of longevity

Questing in ticks is essential for locating a host, and this behavioral response can occur at regionally specific low temperatures for most tick species. Little is known about the dynamics between tick questing behavior and temperature in ticks, specifically how this may impact other aspects of tick biology. Here, we examine whether cold hardening increases questing in three larval tick species (Ixodes uriae, Dermacentor variabilis, and Amblyomma americanum) at low temperatures and whether cold hardening impacts longevity. Rapid cold hardening and prolonged cold acclimation benefitted ticks by decreasing the temperature of chill coma onset, and increased survival, activity, and questing in ticks at low temperatures. Oxygen consumption increased at low temperatures following acclimation in larvae, suggesting this process has a distinct metabolic expense. This increased metabolism associated with hardening led to a substantial reduction in larval longevity as nutrient reserves are limited and cannot be replenished until a host is located. These studies suggest that tick larvae, and likely other developmental stages, require a delicate balance between the need for questing at low temperatures and survival until the first blood meal. [Display omitted] •Tick larvae undergo the process of rapid cold hardening (RCH) that increases survival under cold temperatures and lower the chill coma temperature.•RCH increases the activity and questing of tick larvae at low temperatures.•Oxygen consumption is increased at low temperatures following cold acclimation, which results in a trade-off in reduced longevity.•Lower temperatures exposures will differentially alter tick questing and longevity, potentially impacting their role as vectors for specific pathogens.