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

Abstract

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.

Keywords: Activity; Cold stress; Larvae; Questing; Ticks; Trade-offs.

Figure 1 -. Rapid cold hardening (RCH) and prolonged cold acclimation (Accl.) improve survival.

Left, survival of tick larvae following cold exposure (−14 and −20°C for Amblyomma americanum and −16 and −22°C for Ixodes uriae and Dermacentor variabilis). ✱, indicates significantly different compared to control at the respective temperature. Results and statistical analyses are included in Table S1. Fifteen replicates of ten individuals were conducted for each species. Right, chill coma onset of tick larvae. ✱, indicates significantly different compared to control at the respective temperature. Results and statistical analyses are included in Table S2. Twenty replicates were conducted for each species.

Figure 2 -. Rapid cold hardening (RCH) and prolonged cold acclimation (Accl.) increase activity and questing at lower temperatures.

Top, activity of tick larvae following hardening and acclimation at 5°C and 10°C. ✱, indicates significantly different compared to control at the respective temperature. Results and statistical analyses are included in Table S3. Twenty replicates were conducted for each species and each treatment. Bottom, questing of tick larvae following hardening and acclimation at 5°C and 10°C. ✱, indicates significantly different compared to control at the respective temperature. Results and statistical analyses are included in Table S4. Ten replicates of six individuals were conducted for each species. Relative control levels based on comparison between treatments for each species.

Figure 3 -. Rapid cold hardening (RCH) and prolonged cold acclimation (Accl.) increases oxygen consumption.

Left, oxygen consumption of tick larvae following hardening and acclimation at 5°C and 10°C. ✱, indicates significantly different compared to control at the respective temperature. Results and statistical analyses are included in Table S5. Ten replicates of fifteen individuals were conducted for each species and each treatment.

Figure 4 -. Rapid cold hardening (RCH) and prolonged cold acclimation (Accl.) decreases longevity.

Top, survival of Dermacentor variabilis larvae following hardening and acclimation at 5°C for two weeks and then at 22-24°C. Bottom, survival of I. uriae larvae following hardening and acclimation at 5°C for two weeks and then at 22-24°C. ✱, indicates significantly different compared to control at the respective temperature. Results and statistical analyses are included in Table S6. Ten replicates of ten individuals were conducted for each species.