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Habitat Requirements of the Seabird Tick, Ixodes Uriae (Acari: Ixodidae

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Habitat Requirements of the Seabird Tick, Ixodes Uriae (Acari: Ixodidae J Comp Physiol B DOI 10.1007/s00360-006-0122-7 ORIGINAL PAPER Habitat requirements of the seabird tick, Ixodes uriae (Acari: Ixodidae), from the Antarctic Peninsula in relation to water balance characteristics of eggs, nonfed and engorged stages J. B. Benoit Æ J. A. Yoder Æ G. Lopez-Martinez Æ M. A. Elnitsky Æ R. E. Lee Jr Æ D. L. Denlinger Received: 25 July 2006 / Revised: 25 August 2006 / Accepted: 27 September 2006 Ó Springer-Verlag 2006 Abstract The seabird tick Ixodes uriae is exposed to strategies. Stages that do not absorb water vapor, eggs, extreme environmental conditions during the off-host fed larvae and fed nymphs, rely on water conservation. phase of its life cycle on the Antarctic Peninsula. To Other noteworthy features include heat sensitivity that investigate how this tick resists desiccation, water promotes water loss in eggs and unfed larvae, an requirements of each developmental stage were inability to drink free water from droplets, and determined. Features of I. uriae water balance include behavioral regulation of water loss by formation of a high percentage body water content, low dehydration clusters. We conclude that I. uriae is adapted for life in tolerance limit, and a high water loss rate, which are a moisture-rich environment, and this requirement is characteristics that classify this tick as hydrophilic. met by clustering in moist, hydrating, microhabitats Like other ticks, I. uriae relies on water vapor uptake under rocks and debris that contain moisture levels as an unfed larva and enhanced water retention in the that are higher than the tick’s critical equilibrium adult, while nymphs are intermediate and exploit both activity. Keywords Water balance Á Dehydration Á Tick Á Communicated by I.D. Hume. Ixodes Á Antarctica J. B. Benoit (&) Á G. Lopez-Martinez Á D. L. Denlinger Department of Entomology, The Ohio State University, Introduction Columbus, OH 43210, USA e-mail: [email protected] Only a single tick species, Ixodes uriae, lives in Ant- G. Lopez-Martinez arctica. On that continent, the tick feeds predomi- e-mail: [email protected] nantly on penguins, but it is distributed at high D. L. Denlinger latitudes in both hemispheres, presumably spread by e-mail: [email protected] migratory seabirds (>48 avian species recorded) that serve as its preferred hosts (Wilson 1970). As a com- J. A. Yoder Department of Biology, Wittenberg University, petent vector of Borrelia spirochetes to birds, I. uriae Springfield, OH 45501, USA has epidemiological significance (Olsen et al. 1993, e-mail: [email protected] 1995). Physiologically, few experiments have probed I. uriae’s remarkable ability to survive in extreme cold M. A. Elnitsky Á R. E. Lee Jr Department of Zoology, Miami University, and dry conditions. Those studies that have been con- Oxford, OH 45056, USA ducted focus primarily on how this tick copes with M. A. Elnitsky extremely low temperature (Lee and Baust 1982, e-mail: [email protected] 1987). Interestingly, no physiological adaptations, i.e., R. E. Lee Jr cold tolerance or desiccation resistance (Lee and Baust e-mail: [email protected] 1987; Dautel and Knu¨ lle 1996), have been described 123 J Comp Physiol B that would make Antarctica a suitable habitat exclu- penguin (Pygoscelis adeliae) rookeries. Ticks were sively for I. uriae, but not other ticks. handled using soft-tipped forceps or an aspirator. In Under field conditions, I. uriae takes approximately the experiments, eggs were used 7–10 days post-ovi- 3 years to develop from larva to adult, annually position, larvae were used 10–14 days after ecdysis in spending more than 11 months off the host, residing in the laboratory at 4°C, but the only age information we aggregations underneath rocks and debris that some- can provide for other stages is that they were acquired times reach thousands of individuals (Eveleigh and at the same time. Eggs were tested for viability by Threlfall 1974). Each of these tick colonies consist of a holding them in groups at 100% relative humidity mixture of ticks in all stages of development both be- (RH) at both 4 and 25°C for 1 month or until emer- fore and after blood feeding, and are typically in close gence. Experiments on engorged stages (larvae and proximity to penguin rookeries. While clustered, these nymphs) were conducted after they had ceased move- ticks remain relatively akinetic, huddling in direct ment in preparation for molting, denoted by extension contact with each other. They leave the aggregation in of the legs and failure by the tick to respond to stimuli the protected, sheltered area only to feed, undoubtedly (Kahl and Knu¨ lle 1988). Temperature (25 and 4 ± 1°C) guided by bird host cues (kairomones; Sonenshine and photoperiod (15:9 h light:dark) were controlled 1991). After each bloodmeal, the ticks immediately using environmental cabinets. Fed female adults were return to their colony under the rocks where they molt, not analyzed because they die shortly after oviposition and wait until the bird hosts return the following sea- and adult males do not blood feed, thus larvae and son or, in the case of the adult female ticks, mate nymphs were the only fed stages examined. (mating takes place off-host in this tick), lay eggs and In the laboratory, ticks were held individually in 1 cc die (Sonenshine 1991). mesh-covered chambers placed on a perforated por- In this study, dehydration resistance of I. uriae was celain plate within a sealed glass desiccator (8,000 cc) ascertained by determining standard water balance that contained, at its base, a saturated salt solution to characteristics for each stage of the life cycle, from egg maintain RH. Each RH was controlled by saturated to adult. Dehydration tolerance was recorded as an salt solutions containing an excess of solid salt; 33% indicator of the minimum amount of body water re- RH (MgCl2), 75% RH (NaCl), 85% RH (KCl) and quired for function. Water retention was assessed from 93% RH (KNO3) or glycerol–distilled water mixtures water loss rate in relation to temperature. Clustering of of different concentrations (Johnson 1940; Winston this tick was evaluated as a method of water loss sup- and Bates 1960). Additionally, double-distilled water pression. Free water drinking and water vapor was used for 100% RH and CaSO4 was used for 0% absorption were examined as means to replenish losses RH. Each RH was measured daily with a hygrometer and maintain their internal body water mass levels. (SD ± 0.5% RH; Thomas Scientific, Philadelphia, PA) Additionally, all developmental stages of the tick were and varied less than 1% over the course of the exper- compared to determine which periods in the life cycle iments. were most vulnerable to water stress. In particular, we An electrobalance (SD ± 0.2 lg precision and determined percentage body water content; dehydra- ±0.6 lg accuracy, CAHN, Ventron Co., Cerritos, CA) tion tolerance limit; water loss rate; critical transition was used to weigh the ticks without use of anesthesia. temperature (CTT), denoting the temperature where Each specimen was taken from the desiccator, re- water loss increases abruptly; and critical equilibrium moved from its 1 cc enclosure with an aspirator, placed activity (CEA), the lowest amount of ambient moisture or allowed to crawl onto the weighing pan, weighed, that is required for water vapor absorption to occur. picked up with an aspirator, placed back into the enclosure and then returned to the desiccator. This manipulation required approximately 1 min. Materials and methods Measurement of water balance characteristics Tick collection, storage and weighing Temperature used for basic observations was 25°C for Ixodes uriae were collected on the Antarctic Peninsula comparison with previous studies of water balance (64°04¢S, 64°03¢W) from Humble Island near Palmer (Hadley 1994) and 4°C as a temperature that is more Station, Anvers Island in January 2006, and all exper- representative of this tick’s natural environment and iments were conducted at Palmer Station. Male and for comparison with the cold hardiness literature (Lee female adults, nymphs and larvae were found grouped and Baust 1982, 1987; Worland and Block 2003). For together under rocks, typically in sites near Adelie water balance purposes, activity units were used to 123 J Comp Physiol B define water movement into and out of the tick; av is converted to water mass (m). The critical mass (mC), the activity of water as a vapor (av = %RH/100) and aw used to assess dehydration tolerance, was defined as is the activity of water as a liquid, which has been the mass below which the ticks could not be rescued by determined experimentally in terrestrial arthropods to placing them at 1.00av. This value was used to calculate be 0.99aw based on mole fraction (Wharton 1985); thus, the percentage change in mass (dehydration tolerance) the activity of the tick’s body water can be related di- according to Eq. 3, with i serving as the initial mass rectly to the water vapor in the surrounding atmo- sphere. Before experimentation, ticks were placed at percentage change in m = 100(i À mC)/i. ð3Þ 0.33av and monitored until loss of 4–6% body mass so that the ticks were physiologically standardized by removing any residual surface water and to minimize Water loss (mT) the effects of digestion, reproduction and defecation on mass changes; thus, mass measurements reflected only To prevent interference of adsorbed surface water changes in the tick’s body water levels (Arlian and from the atmosphere on mass changes, water loss rate Ekstrand 1975; Wharton 1985). (net transpiration rate = integumental plus respiratory Water balance characteristics were determined water loss) was determined at 0.00av so that mass based on Wharton (1985) with modifications by Benoit changes could be attributed solely to a reduction of the et al.
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