Ramification of Relaxed Thermoregulation Under Climate Change

doi:10.21203/rs.3.rs-5306879/v1

Download PDF

Research Article

Ramification of Relaxed Thermoregulation Under Climate Change

https://doi.org/10.21203/rs.3.rs-5306879/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

How animals respond to climate changes may be limited by their niche dimensions. Animals able to select microhabitats will be less affected than those that physically or behaviorally are unable to change their exposure. Hence the outcome of tick responses to climate change - which may affect transmission of diseases to humans - may not be obvious first-order effects.

Tick species that actively move throughout their habitat searching for hosts may be able to utilize microhabitats that avoid the full effect of rising temperatures. Other tick species are more static since they wait for hosts to come to them. So even if a tick has a low preferred temperature, the need to be present in questing sites optimal for encountering hosts may force exposure to near lethal elevated temperatures.

To further explore the questing behavior of Dermacentor variabilis and D. andersoni, and to test if regional variation is exhibited by adult D. variabilis, we reproduced a study that found that this species is an active hunter that orients and moves towards infrared radiation (IR) by use of Haller’s organs. We also tested if D. andersoni would move towards an exposed human hand, i.e. a host emitting a combination of IR, CO₂, and odors. This tested if the tick species exhibits sit-and-wait or active hunting.

We found strong sit-and-wait behaviors by D. andersoni and D. variabilis. The ticks did not move toward the stationary exposed hand of an observer, and they were not attracted to infrared radiation. Tick may prioritize optimal locations to encounter potential hosts, over enzymatically optimal temperatures. Rather than evolving to detect hosts at a distance, Haller’s organs may have evolved to differentiate warm attachment sites from cooler fur. Our results suggest that Dermacentor questing behavior (remaining on station irregardless of preferred temperature) may make them particularly vulnerable to future rises in temperature.

tick

Dermacentor

thermoregulation

climate change

An organism’s response to climate change is limited by its niche dimensions (Thuiller et al. 2005; Sinervo et al. 2010). Animals able to move within a habitat can ameliorate abiotic shifts, while those that physically or behaviorally are unable to change their exposure may suffer more severe effects (Stevenson 1985). Hence the outcome of tick responses to climate change - which may affect transmission of diseases to humans (Ostfeld and Brunner 2015) - may not be obvious first-order effects.

Tick species that actively move throughout their habitat searching for hosts may be able to utilize microhabitats that avoid the full effect of rising temperatures. Other tick species are more static since they wait for hosts to come to them. So even if a tick has a low preferred temperature, the need to be located in optimal questing sites for encountering hosts may force exposure to near lethal elevated temperatures.

Furthermore, other factors may interface with rising temperatures. Ticks exhibit diverse behavioral patterns when seeking out hosts, and their strategies can vary depending on disease state (Lefcort and Durden 1996), species, population, and abiotic environmental conditions such as humidity, temperature, precipitation, season, and photoperiod (Leal et al. 2020). Ticks generally utilize sit-and-wait tactics for a host to come to them (Parola and Raoult 2001), use environmental cues to actively move towards potential hosts, or use a combination of the two. During questing, sit-and-wait ticks such as Ixodes ricinus climb onto vegetation or other surfaces and extend their forelegs to latch onto passing hosts as they brush by. This passive behavior common in Ixodidae (hard ticks) saves water and energy which is important since many ticks only feed once between molts (Lees 1946). These ticks do not actively move towards hosts but rely on detecting cues such as carbon dioxide, body heat, humidity, vibrations, shadows, movement, and odors to ready themselves for an approaching host. Once on a host they again use these cues to find an appropriate site for attachment. The downside of this static approach is that the tick needs to be contacted by its hosts, for example on the edge of a trail. Even if that location is abiotically or enzymatically unfavorable, the tick has little choice but to be present. On a hot dry day, the heat stress and water loss that is experienced by a 50 kg deer may be bearable for a hydrated deer emerging from shade, but it may be lethal to a tick with its less favorable surface-to-volume ratio.

Other tick species actively search (“hunt”) for hosts. For instance, Ixodes scapularis uses a combination of sit-and-wait and active foraging, allowing it to locate a host within a 50 cm radius (Curtis et al. 2020). This involves using the above cues to first detect hosts and then intentionally moving on the ground in the direction of the host. For example, Haller’s organs on a tick’s front legs precisely detect infrared radiation, CO₂, and odors, so ticks can even measure the signal gradient between their left and right forelegs (Nuttall et al. 1908; Sonenshine and Roe 1991; Leonovich 2013; Carr & Salgado 2019). This gradient provides information on the direction that a potential host is either located or moving.

Environmental conditions such as temperature, humidity, and vegetation type can also influence tick behavior. Only under high humidity levels do Ixodes ricinus nymphs move toward dog odor (Crooks and Randolph, 2006). Additionally, some ticks in warmer climates quest more aggressively, while ticks from cooler climates begin questing at lower temperatures (McClure and Diuk-Wasser 2019).

Confounding the issue of determining which species engage in sit-and-wait versus active hunting is that within species, populations in different geographic regions may display variations in behavior due to local ecological pressures and adaptations. Ticks in certain areas may adjust their host-seeking strategies based on available host species and environmental conditions. For example, Amblyomma americanum ticks from xeric hammocks spend more time questing than those from nearby successional hardwoods (Richardson et al. 2022). Similarly, Amblyomma mixtum quest higher in the vegetation at elevated humidity levels (Beck and Orozco 2015), yet Amblyomma americanum quests lower at elevated humidity levels (Schultze et al. 2001 as reported by Richardson et al. 2022). In Virginia, Atwood and Sonenshine (1967) found a positive correlation between solar radiation levels and daily questing activity of adult Dermacentor variabilis (American dog tick). Contrarily, Harlan and Foster (1990) found that in Ohio ambient temperature was the chief predictor of adult D. variabilis host-seeking behavior, with solar radiation having lessor influence.

It is well understood that tick ranges are expanding poleward as temperatures and rainfall increase under climate change (Leighton et al. 2012; Sagurova et al. 2019). Less studied are the second-order effects such as the possible extirpation of certain tick species due to their static sit-and-wait strategies. Since both D. variabilis and D. andersoni are vectors for Rocky Mountain Spotted Fever (Rickettsia rickettsia) and Rabbit Fever (Francisella tularensis, Lefcort et al. 2020) the outcome of climate change may affect human health.

To further explore the questing behavior of D. variabilis and D. andersoni (Rocky Mountain wood tick), and to test if regional variation is exhibited by adult D. variabilis, we reproduced a study by Carr and Salgado (2019) that found that this species is an active hunter that orients and moves towards infrared radiation (IR). Yet earlier, McEnroe and McEnroe (1973) using a field-collected population determined that D. variabilis in Massachusetts is a sit-and-wait species that climbs or descends vegetation based on internal saturation weight. Carr and Salgado (2019) used a lab-reared colony that originated in Stillwater Oklahoma while we used a field-caught population from Spokane County Washington.

In Eastern Washington State D. variabilis cooccurs with D. andersoni and are known to be most common on the edges of trails (Frady and Magori 2014). Adults share most niche dimensions except we have found that D. andersoni adults are better at resisting desiccation (Lefcort et al. 2020). Larvae of both species also exhibit similar behavior except for diapause activity, and unlike adults, larvae of D. andersoni are more sensitive to water loss than are D. variabilis (Diyes et al. 2023).

In addition to testing if the two species responded to IR, we also tested if D. andersoni would move towards an exposed human hand, i.e. a host emitting a combination of IR, CO₂, and odors. This tested if the tick species exhibits sit-and-wait or active hunting. We predicted that it would actively move toward humans.

Tick collecting and rearing

During June of 2023 and June of 2024, we used cloth drags to collect mixed groups of 400 adult D. variabilis and D. andersoni ticks at James T. Slavin Conservation Area and Palisades Park both in Spokane County, Washington State, USA. Collected ticks were kept in 5-mL vials at 25–28°C. The vials had pinholes to allow airflow and were suspended over water to maintain high humidity levels. Ticks were not fed and were tested in a random order within 2 months of collection. All behavioral experiments (thermal preference in 2023 and the other experiments in 2024) were conducted at our laboratory at Gonzaga University in Spokane, WA. The species identity of ticks was determined using Gregson (1950) as per Lefcort et al. (2020).

Experiment 1: Thermal Preference

Two thermal gradients were created (Fig. 1). Two 40 cm X 2.5 cm clear PETG tubes were divided into 11 temperature zones, with a small hole drilled into the top of each zone to allow access for a thermocouple (Cooper SH66A) and ventilation. The hot end of the tube (zone 11) was occluded with a rubber stopper and warmed by an electric heating pad. For humidity, a piece of water-soaked foam was placed in the cold end (zone 1) of the tube which was cooled by reusable ice packs.

Treatments consisted of cotton make-up rounds that were briefly wiped (face, auxiliary, or saliva) on one of four mixed breed pet dogs. Additionally, there was a control treatment of cotton rounds that did not contact a dog. Cotton rounds were used on the same day that they were swabbed. Gloves were not worn so human scent was also present. The goal was not to test the difference between breeds or the relative attraction of humans versus dogs. The goal was to provide the ticks with a realistic environment that would encourage questing.

After a cotton round was briefly wiped in zone 1 and zone 11, a single tick was breathed upon - CO₂ is known to attract D. variabilis (Carr et al. 2013) - and then inserted through an opening into zone six, and a piece of tape was placed over the hole to prevent escape. The tick remained in the tube for 30 minutes and every three minutes its zonal position was noted. For the control treatment, at 27 minutes the observer once again breathed through the zone six opening. The tick's immediate response to the added CO₂ was recorded. At the 30-minute mark the tick's final location was recorded.

The average zone that the tick occupied was calculated by adding the zones from three minutes to 27 minutes and dividing the result by nine. This was converted into an average temperature estimate using the previously calculated average zone temperatures (Fig. 1). The delta T was calculated by subtracting the final zone temperature from the temperature of the zone occupied by the tick at 27 minutes. 30 D. andersoni ticks were individually tested for each treatment. Between replicates, Zones 1 and 11 were wiped with 70% ethanol to eliminate chemical cues.

Experiment 2: Thermotaxis Assay

To test if ticks were attracted to infrared radiation we reproduced the methods of Carr and Salgado (2019). We used a flat white painted hemlock box − 10 cm (w) x 10 cm (h) x 100 cm (l). The lid was 6mm clear plexiglass. The ends of the arena were 10cm x 10 cm blue anodized aluminum plates (Fig. 2). The arena was marked with faint pencil lines into 10 zones whose temperature could be individually determined through small holes. The external side of the hot end (Zone 11) was heated by an Onilab MS-H380-Pro heater to 40.1 ˚C and the cold plate (zone 1) 13.5 ˚C by ice packs. Hot and cold ends were alternated between replicates. Temperatures were verified by a Cooper SH66A thermocouple. According to the Stephan-Bolzmann law, at 40 ⁰C the plates have an emissivity of 0.94 which is close to human emissivity of 0.98 at 37 ⁰C (Carr and Salgado 2019). The arena was initially misted so humidity varied between 60–75%. A fan gently circulated the air in a closed loop to prevent thermal differences between zones, i.e., the zones (22.1–22.3˚C) mainly only differed in infrared levels. Between replicates, the arena was wiped with 70% ethanol to eliminate chemical cues. This was allowed to evaporate with the lid removed. Ticks in their home vials were left to acclimatize next to the arena for 20 minutes. Tick vials were opened and gently breathed upon to expose the ticks to human odor and carbon dioxide just before testing.

Experiment 2: Thermotaxis Assay - Treatments

T1. Carr and Salgado method: Following Carr and Salgado (2019) we added groups of eight ticks to the center of the arena between zones 5 and 6 and their movements were filmed from above for five minutes. We conducted five replicates without heat and cold applied, and five replicates with the heat and cold.

When we failed to replicate Carr and Salgado’s result (an attraction to infrared radiation) we tried several additional treatments to see if we could reproduce their result:

T2 (control for IR). The arena mimicked the conditions of T1 but no hot plate and no ice pack were used and only a single tick was present. Adult ticks of these species are not gregarious, so using lone ticks more closely simulated what occurs in the field and avoided pseudoreplication. We also directly observed the ticks rather than filming them. A single tick was placed between zones 5 and 6. The trials lasted 10 minutes with zone occupation recorded every two minutes. N = 100 replicates.

T3. The arena mimicked the conditions of T2 but we added a hot and cold end. The hot side (zone 10) was at 40.0 ˚C. and the cold plate (zone 1) was at 13.5 ˚C. N = 50 replicates.

T4 (test for IR versus air temperature). Similar to T3 but we covered the metal plates with aluminum foil (with a thin air gap between the plate and the foil. This allowed heat to transfer but blocked infrared radiation. The aluminum foil was at 37.0 ˚C. The cold plate (zone 1) was at 13.5 ˚C. We measured each tick with and without aluminum foil. N = 50 replicates with foil and 50 replicates without the foil. A month passed between T2 and T4 and we worried about a time effect, so we repeated the control for this treatment.

T5. Same as T4 but zone 10 at 40 ˚C. The cold plate (zone 1) was at 13.4 ˚C. N = 50 replicates with foil and 50 replicates without the foil. A month passed between T2 and T5, so we repeated the control for this treatment.

T6 (test for disturbance by the observer). Same as T3 but we used a remote camera. N = 50 replicates.

T7 (test for disturbance by the observer). Same as T2 but with a remote camera. N = 50 replicates.

Experiment 3A: Distant Approach to a Human

Since we could not get the ticks to move to an IR source, as found by Carr and Salgado (2019) this experiment tested if D. andersoni ticks would move towards a stronger signal, a human emitting IR, CO₂, and odors. We first tested if ticks would move towards a human located at a significant distance, as noted in other species of Ixodes ticks (i.e., Curtis et al. 2020). A table (1.5 m X 0.75 m) was covered by a gently misted white synthetic felt cloth. It was divided into eight radiating zones with zone 8 farthest from the observer. The zones curved so that all areas within a zone were roughly equal distance from the observer (Fig. 3).

A single tick was breathed upon and then placed between Zones 4 and 5, 0.75 m from the edge of the table area where the observer was located. The tick’s location was recorded every minute for 10 minutes. The 10 zonal locations were then averaged into a single number, and this was the score assigned to that tick.

Two treatments (N = 60 ticks each) were used. In the first control treatment, the observer was located one meter away from Zone 1 of the table which is beyond the range that published studies have recorded as a distance that ticks can detect. The second experimental treatment had the observer seated next to Zone 1 with their hand resting on the near edge of Zone 1.

Experiment 3B: Near Approach to a Human

This experiment tested if D. andersoni ticks would move towards a human from a near distance (5 cm and less). A white synthetic felt cloth was placed on a table. A single tick was breathed upon and then placed either 5, 4, 2, 1, or 0.5 cm from the observer’s hand. The tick’s location was recorded every minute for five minutes. Additionally, it was noted if the tick successfully contacted the hand whereupon it was immediately removed. The time to reach the hand was measured. 150 ticks were tested. Note: ticks of this species require over 24 hours of attachment in order to transmit pathogens.

Statistics

We used JMP statistical software (Cary, NC, USA) to perform One-way ANOVAs and Student t-tests. Alpha was set to 0.05.

In this and previous studies we have found no differences in adult male and female behavior of either D. andersoni or D. variabilis (Lefcort et al. 2020; Lefcort et al. 2023).

Experiment 1: Thermal Preference

In the control treatment (absent of dog scent) the addition of CO₂ at time 27 minutes increased the thermal preference of the ticks. The mean (+/- SD) temperature from 0–27 minutes was 23.45⁰C (1.15), while after the CO₂ it was 24.39 (3.43) which are significantly different (Paired two-tailed t-test, t = 4.09, d.f. = 143, P < 0.001).

There was a significant difference in the thermal preferences of ticks depending on which dog scent they were exposed to (One Way ANOVA, F = 2.66, d.f. = 7, P = 0.011, Fig. 4) with the ticks exposed to LU’s saliva having a higher thermal preference than ticks in the absence of dog scent (post-hoc Tukey Test). When all the dog treatments were combined and compared to the control (no dog) treatment, the dog treatments increased tick thermal preference from 22.5 ⁰C to 23.9 ⁰C (One-tailed Student’s t-test, t = 2.156, d.f. = 230, P = 0.016).

Experiment 2: Thermotaxis Assay

T1. Following the methods of Carr and Salgado (2019) we found a slight but nonsignificant difference between the distributions of D. andersoni ticks when comparing their location in the arena at room temperature, to the arena when heat was applied to the hot end (zone 10) and ice was applied to the cold end (Zone 1, X² = 3.624, d.f. = 2, P = 0.170, Fig. 5). Ticks did not seem to be attracted to the hot plate (Zone 10) that was emitting higher levels of infrared radiation.

In treatments 2–7 (T2-T7) of D. andersoni, there was no difference in the zones that the ticks were situated in after 10 minutes (One Way ANOVA, F = 0.700, d.f. = 7, P = 0.671, Fig. 6).

In treatments 2–7 (T2-T7) of D. variabilis (the species used by Carr and Salgado 2019) there was no difference in the zones that the ticks were situated in after 10 minutes (One Way ANOVA, F = 0.819, d.f. = 7, P = 0.573, Fig. 7).

Experiment 3A: Distant Approach to a Human

There was a slight but nonsignificant movement towards the observer when the observer’s hand was located in Zone 1 (One-tailed Student’s t-test, t = 1.484, d.f. = 95, P = 0.070, Fig. 8).

Experiment 3B: Near Approach to a Human

From near distances the ticks moved towards the observer’s hand (Fig. 9). Ticks that started closer to the hand were faster to reach the hand (One Way ANOVA, F = 4.77, d.f. = 4, P = 0.001, Fig. 10) with the ticks that started at 0.5 cm being faster than the 5, 4, and the 2 cm ticks (post-hoc Tukey Test).

Understanding the risks posed by disease vectors such as ticks requires information on how vectors encounter human hosts. We found strong sit-and-wait behaviors by D. andersoni and D. variabilis. We wanted to see if ticks would move toward the stationary exposed hand of an observer. We did not. We tried distances from 0.75 m down to 0.5cm. Only starting at 5 cm did we observe over 50% of the ticks moving toward the observer, and only at 1 cm and below did the ticks rapidly climb onto the proffered hand.

Is unclear why we were not able to reproduce the results of Carr and Salgado (2019) who found that D. variabilis was strongly attracted to infrared radiation. Using a copy of their device, we found that neither D. variabilis nor D. andersoni responded to IR. After failing to reproduce Carr and Salgado’s results, we added six more treatments to see if we could somehow detect a response to IR. The only difference between our study and theirs is that although we used groups of eight D. andersoni in Treatment 1, we were short of D. variabilis, so we did not use groups of eight D. variabilis. We did, however, use both D. variabilis and D. andersoni for the other six treatments that attempted to find a response to IR. None saw a reaction to IR. Perhaps there are regional variations in tick behavior. For example, Ixodes ricinus populations from cooler habitats begin questing at colder temperatures than those from warmer habitats (Tomkins et al. 2014). Similarly, southern I. scapularis nymphs do not climb, but northern nymphs do (Arsnoe et al. 2015). Our differences with the Carr and Salgado’s study could also be due to our use of field-caught ticks while they used a multigenerational lab-reared population from a supply house. It is known that laboratory-reared populations of D. andersoni have unique microbiomes (Gall et al. 2017) and microbiomes can affect tick behavior (Bonnet et al. 2017; Chicana et al. 2019). In fairness, D. variabilis moving towards IR is only a small part of Carr and Salgado’s landmark research that elegantly discovered the inner workings of Haller’s organs.

So why would ticks evolve Haller’s organs, with their exquisite sensitivity to IR (Carr and Salgado 2019), if ticks are not using them to find hosts? The answer may lie less in finding hosts, and more in finding attachment sites. Once a tick has grappled onto a host it is presented with the problem of finding an appropriate attachment site. The area needs to be humid, relatively undisturbed, with exposed skin. Many mammals have thick fur, so ticks need a method of finding optimal sites. On a cool day, the surface of thick fur may be tens of degrees colder than mammal skin, with a reduced IR signature. Human clothes have similarly low radiance. Using a Haller’s organ as an IR meter would solve this quandary.

Consistent with other studies of Ixodes ticks (i.e., Fieler et al. 2021) we found ticks thermoregulated at cool temperatures and with a large variance in mean preferred temperature. Since the lifestyle of sit-and-wait ticks requires them to choose a location that intersects with a host - rather than an abiotically optimal environment - it is not surprising that ticks may show little evidence of tight thermoregulation. Going up to a year between feeding may select for cool energy-conserving and water-conserving temperatures rather than the enzymatically optimal temperature, with a tight variance, preferred by many ectotherms. Hence Fieler et al. (2021) reported that the larvae of several ixodid tick species have a preferred temperature of only about 20 ⁰C. This is close to what we found and also may explain why we observed such a wide variance around mean selected temperatures. Similarly, El Nabbout et al. (2017) found that D. variabilis from throughout Nova Scotia Canada have extremely broad temperature preferences.

The above also explains the statistically significant, but weak change of thermal preference, when we exposed the ticks to dog odor. Rather than using the dog smell as a cue to move toward high IR, we observed only a slight increase in tick thermal preference. Conlon and Rockett (1982) found that D. variabilis in Lucas County, Ohio did not move toward rodent odor; our lab in Spokane County Washington found the same for D. variabilis and D. andersoni exposed to mouse and human odor (Lefcort et al. 2020). In the present study we found that dog odor increased the ticks’ thermal preference, but only from 22.5 to a still low 23.9 ⁰C. Dogs have a much greater average core temperature of between 38.3 and 39.2 ⁰C so a tick choosing 23.9 ⁰C is unlikely to orient towards a dog. However, a tick questing on the edge of a trail needs to optimize location, rather than temperature (see Huey and Slatkin, 1976), so having a low preferred temperature may not be the deciding factor in choosing a questing location.

An interesting ramification of our finding concerns climate change. For a few hours during July of 2021 our field sites reached 43 ⁰C which is near the thermal maximum of Dermacentor ticks (Fieler et al. 2021). Although ticks will descend vegetation to rehydrate, our results suggest that Dermacentor questing behavior (remaining on station irregardless of preferred temperature) may make them particularly vulnerable to future rises in temperature. While few people would mourn a decline of ticks, they are important ecosystem components, and their decrease may mirror the decline of less-studied organisms. One caveat to this prediction is that climate models predict not only a warmer world, but also a wetter world (IPCC 2014). Maintaining saturation may allow ticks to lessen the impact of higher temperatures.

Author Contribution

HL conceived of the study, obtained funding, wrote the manuscript, and helped with the testing. SMB, JWH, and SMS did most of the tick collecting and conducted most of the experiments. SMB and JWH also helped with two of the figures.

Acknowledgement

We thank the Gonzaga Science Research Program.

Data Availability

Data files are available at https://www.gonzaga.edu/academics/faculty-listing/detail/hugh-lefcort-phd-623e50ce

Arsnoe IM, Hickling GJ, Ginsberg HS, McElreath R, Tsao JI (2015) Different populations of blacklegged tick nymphs exhibit differences in questing behavior that have implications for human Lyme disease risk. PLoS ONE 10:5e0127450
Atwood EL, Sonenshine DE (1967) Activity of the American Dog Tick, Dermacentor variabilis (Acarina: Ixodidae), in Relation to Solar Energy Changes. Ann Entomol Soc Am 60:354–362
Beck DL, Orozco JP (2015) Diurnal questing behavior of Amblyomma mixtum (Acari: Ixodidae). Exp Appl Acarol 66:613–620
Bonnet SI, Binetruy F, Hernández-Jarguín AM, Duron O (2017) The tick microbiome: why non-pathogenic microorganisms matter in tick biology and pathogen transmission. Front Cell Infect Microbiol 7:236
Carr AL, Roe RM, Arellano C, Sonenshine DE, Schal C, Apperson CS (2013) Responses of Amblyomma americanum and Dermacentor variabilis to odorants that attract haematophagous insects. Med Vet Entomol 27:86–95
Carr AL, Salgado VL (2019) Ticks home in on body heat: A new understanding of Haller’s organ and repellent action. PLoS ONE 14:e0221659
Chicana B, Couper LI, Kwan JY, Tahiraj E, Swei A (2019) Comparative microbiome profiles of sympatric tick species from the far-western United States. Insects 10:353
Conlon JM, Rockett CL (1982) Ecological investigations of the American dog tick, Dermacentor variabilis (Say), in northwest Ohio (Acari: Ixodidae). Int J Acarol 8:125–131
Crooks E, Randolph SE (2006) Walking by Ixodes ricinus ticks: intrinsic and extrinsic factors determine the attraction of moisture or host odour. J Exp Biol 209:2138–2142
Curtis TR, Shi M, Qiao X (2020) Patience is not always a virtue: effects of terrain complexity on the host-seeking behaviour of adult blacklegged ticks, Ixodes scapularis, in the presence of a stationary host. Med Vet Entomol 34:309–315
Diyes CP, Dergousoff SJ, Chilton NB (2023) Interspecific differences in the questing behaviour of Dermacentor andersoni and Dermacentor variabilis (Acari: Ixodidae) larvae. Can Entomol 155:e36
El Nabbout A, Kho J, Lloyd V, Rossolimo T (2017) Rickettsia spp. and its effects on the physiology and behaviour of Dermacentor variabilis. Int J Biology 9:39–46
Fieler AM, Rosendale AJ, Farrow DW, Dunlevy MD, Davies B, Oyen K, Xiao Y, Benoit JB (2021) Larval thermal characteristics of multiple ixodid ticks. Comp Biochem Physiol A: Mol Integr Physiol 257:110939
Frady H, Magori K (2014) Dermacentor tick exposure risk assessment and host variability on four types of recreational trails. Entomological Society of America 2014 Annual Meeting
Gall CA, Scoles GA, Magori K, Mason KL, Brayton KA (2017) Laboratory colonization stabilizes the naturally dynamic microbiome composition of field collected Dermacentor andersoni ticks. Microbiome 5:1–10
Gregson JD (1950) The Ixodidae of Canada. Canada department of agriculture. Ott Can Number 90:92
Harlan HJ, Foster WA (1990) Micrometeorologic factors affecting field host-seeking activity of adult Dermacentor variabilis (Acari: Ixodidae). J Med Entomol 27:471–479
Huey RB, Slatkin M (1976) Cost and benefits of lizard thermoregulation. Q Rev Biol 51:363–384
IPCC (2014) In: Pachauri RK, Meyer LA (eds) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team. IPCC, Geneva, Switzerland, p 151
Leal B, Zamora E, Fuentes A, Thomas DB, Dearth RK (2020) Questing by tick larvae (Acari: Ixodidae): a review of the influences that affect off-host survival. Ann Entomol Soc Am 113:425–438
Lees AD (1946) The water balance in Ixodes ricinus L. and certain other species of ticks Parasitology. 37:1–20
Lefcort H, Durden LA (1996) The effect of infection with Lyme disease spirochetes (Borrelia burgdorferi) on the phototaxis, activity, and questing height of the tick vector Ixodes scapularis. Parasitology 113:97–103
Lefcort H, Hovancsek ML, Bell LA, Ellinwood EK, Freisinger EM, Herrmann KG, Lau JR (2023) Do ticks exhibit repeatable individual behaviors? Exp Appl Acarol 91:629–644
Lefcort H, Tsybulnik DY, Browning RJ, Eagle HP, Eggleston TE, Magori K, Andrade CC (2020) Behavioral characteristics and endosymbionts of two potential tularemia and Rocky Mountain spotted fever tick vectors. J Vector Ecol 45:321–332
Leighton PA, Koffi JK, Pelcat Y, Lindsay LR, Ogden NH (2012) Predicting the speed of tick invasion: an empirical model of range expansion for the Lyme disease vector Ixodes scapularis in Canada. J Appl Ecol 49:457–464
Leonovich SA (2013) The main evolutionary trends in sensory organs and questing behavior of Parasitiform ticks and mites Entomol. Rev 93:1190–1191
McEnroe WD, McEnroe MA (1973) Questing behavior in the adult American dog tick Dermacentor variabilis Say (Acarina: Ixodidae). Acarologia 15:38–42
McClure M, Diuk-Wasser MA (2019) Climate impacts on blacklegged tick host-seeking behavior. Int J Parasitol 49:37–47
Nuttall GHF, Cooper WF, Robinson LE (1908) On the structure of ‘Haller’s organ’. Ixodoidea Parasitol 1:238–242
Ostfeld RS, Brunner JL (2015) Climate change and Ixodes tick-borne diseases of humans. Philosophical Trans Royal Soc B: Biol Sci 370:20140051
Parola P, Raoult D (2001) Ticks and tickborne bacterial diseases in humans: an emerging infectious threat Clin. Infect Dis 32:897–928
Richardson EA, Taylor CE, Jabot B, Martin E, Keiser CN (2022) The effects of habitat type and pathogen infection on tick host-seeking behaviour. Parasitology 149:59–64
Sagurova I, Ludwig A, Ogden NH, Pelcat Y, Dueymes G, Gachon P (2019) Predicted northward expansion of the geographic range of the tick vector Amblyomma americanum in North America under future climate conditions. Environ Health Perspect 127:107014
Schulze TL, Jordan RA, Hung RW (2001) Effects of selected meteorological factors on diurnal questing of Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae). J Med Entomol 38:318–324
Sinervo B, Mendez-De-La-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagrán-Santa Cruz M, Lara-Resendiz R, Martínez-Méndez N, Calderón-Espinosa ML, Meza-Lázaro RN, Gadsden H (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899
Sonenshine DE, Roe MR (1991) Biology of ticks, 2nd edn. Oxford University Press, New York
Stevenson RD (1985) The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. Am Nat 126:362–386
Thuiller W, Lavorel S, Araújo MB (2005) Niche properties and geographical extent as predictors of species sensitivity to climate change. Glob Ecol Biogeogr 14:347–357
Tomkins JL, Aungier J, Hazel W, Gilbert L (2014) Towards an evolutionary understanding of questing behaviour in the tick Ixodes ricinus. PLoS ONE 9:e110028

No competing interests reported.

Download PDF

Version 1

posted

You are reading this latest preprint version

Ramification of Relaxed Thermoregulation Under Climate Change

Status:

Version 1

Abstract

Figures

Introduction

Methods

Tick collecting and rearing

Experiment 1: Thermal Preference

Experiment 2: Thermotaxis Assay

Experiment 2: Thermotaxis Assay - Treatments

Experiment 3A: Distant Approach to a Human

Experiment 3B: Near Approach to a Human

Statistics

Results

Experiment 1: Thermal Preference

Experiment 2: Thermotaxis Assay

Experiment 3A: Distant Approach to a Human

Experiment 3B: Near Approach to a Human

Discussion

Declarations

Author Contribution

Acknowledgement

Data Availability

References

Additional Declarations

Status:

Version 1