Elsevier

Journal of Insect Physiology

Volume 101, August 2017, Pages 39-46
Journal of Insect Physiology

Dehydration and starvation yield energetic consequences that affect survival of the American dog tick

https://doi.org/10.1016/j.jinsphys.2017.06.012Get rights and content

Highlights

  • Effects of dehydration and starvation were examined in Dermacentor variabilis.

  • Single and repeated dehydration bouts depleted lipid and protein reserves.

  • Reduced energy levels coincided with increased O2 consumption in dehydrated ticks.

  • Starved ticks had reduced energy reserves and dehydration tolerance.

Abstract

Ticks are obligate hematophagous arthropods, but may have to endure extended time (1–2 years) between feedings. During these off-host periods, ticks must contend with a multitude of environmental stresses including prolonged or repeated exposure to desiccating conditions. In this study, we measured the energetic consequences of single and repeated bouts of dehydration of American dog ticks, Dermacentor variabilis, and examined the impact of energy reserves on tick survival during dehydration. Recently molted ticks exposed to a single period at 0% relative humidity (RH) for 5 d lost ∼26% of their body water and showed 1.3- and 1.7-fold reductions in protein and lipid, respectively. These reduced energy reserves coincided with increased O2 consumption in dehydrated ticks. Exposure to repeated cycles of dehydration (0% RH, 48 h) and rehydration (100% RH, 24 h) also reduced energy reserves; however, ticks were able to fully recover their body water after 12 cycles of dehydration/rehydration and endured >20 cycles. Starvation of ticks, in the absence of dehydration, for 18 or 36 weeks resulted in the loss of ∼20–40% of protein and 60% of lipid reserves. When ticks were exposed to continuous dehydration at 0% RH, their survival after 18 weeks of starvation was only minimally impacted; however, individuals starved for 36 weeks succumbed to dehydration much more rapidly than recently fed ticks. Both single and repeated dehydration exposures resulted in substantial energetic costs and ticks with limited energy reserves were more susceptible to dehydration-induced mortality, indicating that adequate energy reserves are critical for tolerance to dehydration stress and long-term success of ticks.

Introduction

The American dog tick, Dermacentor variabilis, is a hard tick (Ixodidae) that is widely distributed in the United States and acts as an important vector for diseases such as Rocky Mountain spotted fever (de la Fuente et al., 2008). As with other ixodid ticks, D. variabilis has a multi-stage life cycle (larva, nymph, adult) with each stage requiring a blood meal for development and/or reproduction (Sonenshine, 1991). Although ticks are obligate hematophagous arthropods, they spend the majority of their lives off host where they must contend with environmental stressors while relying on energy reserves acquired from blood feeding by the previous stadia (reviewed in Needham and Teel, 1991). The ability to survive these stresses while off host significantly impacts the specific environments where ticks and their pathogens can establish (Goethert and Telford, 2009; Klompen et al., 1996).

During off-host periods, ticks are at risk for dehydration due to their small body size and consequent high surface-area-to-volume ratio (Benoit and Denlinger, 2010), and maintaining water balance is critical for tick survival (Needham and Teel, 1991). Ticks can prevent dehydration through physical and physiological adaptations to conserve water, behavioral mechanisms, and acquisition of exogenous water (Benoit and Denlinger, 2010, Needham and Teel, 1986, Sonenshine, 1991). However, some of these preventative measures come at an energetic cost. Increased movement between humid microhabitats and questing locations, which occurs under desiccating conditions (Crooks and Randolph, 2006, Short et al., 1989), and the active, solute-driven process of water vapor absorption to replenish water content (Gaëde and Knülle, 1997) can reduce lipid reserves (discussed in Randolph, 2008).

When conditions drop below the critical equilibrium humidity (CEH; the relative humidity at which ticks can absorb water vapor), typically 75–95% relative humidity (RH) depending on tick developmental stage and species, ticks begin to dehydrate as water loss exceeds their ability for water vapor uptake (Needham and Teel, 1991, Yoder et al., 2012). To increase survival times at low RH, some ticks rely on energy reserves during dehydration as a source of metabolic water (Dautel, 1999). Additional energetic costs would be incurred during rehydration as dehydration-induced damage is repaired and water balance is restored through active water vapor absorption. When dehydrated ticks are moved to hydrating conditions, there is an increase in observed VCO2 (Fielden and Lighton, 1996), likely as ticks metabolize resources to facilitate water vapor uptake. Another potential source of energy use when arthropods are dehydrated is the variety of molecular mechanisms employed to limit dehydration-induced damage including, expression of proteins such as heat shock proteins, antioxidant enzymes, and aquaporins (Benoit and Denlinger, 2010). D. variabilis upregulates similar pathways in addition to accumulating molecules such as glycerol, which act to prevent damage to cellular components, in various insects and ticks (Rosendale et al., 2016, Yoder et al., 2006). These physiological adjustments that improve tick resistance to dehydration are likely energetically costly.

In addition to the risk of dehydration-induced mortality, ticks must contend with limited nutrient availability during extended off-host periods. Although ticks show a remarkable ability to withstand prolonged starvation, in part through low metabolic rates (Lighton and Fielden, 1995), exhaustion of energy reserves is a major cause of mortality under field conditions (Nieto et al., 2010). In addition to starvation-induced mortality, limited energy reserves can also reduce tolerance of environmental stress. Ticks with high fat reserves survive exposure to low temperatures better than starved ticks with low lipid levels (Herrmann and Gern, 2013). Additionally, older ticks with limited energy stores show a greater susceptability to water loss at low RH as compared to more recently fed ticks (Williams et al., 1986). In several dipterans, dehydration exposure reduces lipid, carbohydrate, and/or protein levels (Benoit et al., 2010, Teets et al., 2012), leading to effects on long-term fitness such as reductions in fecundity (Benoit et al., 2010). These desiccating conditions may be particularly costly for ticks that have been fasting for extended periods and cannot replenish energy reserves until finding a host; however, energetic expenditure during dehydration has received little attention in ticks.

Water balance and starvation are arguably two of the main factors determining the ability of ticks to survive off host (Needham and Teel, 1991); however, little is known about the interaction between these two stresses. Additionally, most studies on tick dehydration have focused on a single dehydration event, although ticks often experience multiple bouts as they move between humid microhabitats and questing locations with less favorable hydric conditions. Therefore, the objectives of this study were to measure the effects of dehydration on energy balance, compare the energetic impacts of a single dehydration event and repeated dehydration/rehydration cycles, and examine the interaction between starvation status and dehydration resistance.

Section snippets

Ticks

Engorged Dermacentor variabilis nymphs were obtained from laboratory colonies at the Oklahoma State University Tick Rearing Facility (Stillwater, OK, USA) where they were fed on sheep (Ovis aries). These colonies are maintained under 14:10 h, light:dark (L:D), 97% relative humidity (RH), and 25 ± 1 °C. Upon arrival, groups of 10 ticks were transferred to 15 cm3 mesh-covered vials and placed in closed chambers containing a supersaturated solution of potassium nitrate, providing 93% RH (Winston and

Water content and survival

Ticks exposed to a single bout of dehydration at 0% RH lost water at ∼0.32% h−1 over the first 5 d. Survival then began to drop as ticks approached a 30% loss in water content (5–6 d), with most ticks succumbing around 40–50% (Fig. 1A). During repeated bouts of dehydration, ticks lost ∼15% of their body water content during 2 d at 0% RH and were able to recover most of that water loss within 1 d at 100% RH for multiple rounds of dehydration/rehydration (Fig. 1B). However, after 25 cycles, water

Discussion

Off-host periods of the tick life cycle are characterized by fluctuations in hydric conditions while the tick is in a fasting state (Needham and Teel, 1991), and both dehydration and starvation can impact tick success in finding hosts and spreading disease (Steele & Randolph, 1985; Randolph and Storey, 1999, Randolph, 2008). This study examined the interaction of dehydration and starvation on the water balance and energetics of an ixodid tick and is the first to consider these in the context of

Acknowledgments

We thank Christopher Holmes and two anonymous reviewers for providing comments that have improved this manuscript. This work was supported by the University of Cincinnati Faculty Development Research Grant to J.B.B. Funding was also provided by the United States Department of Agriculture’s National Institute of Food and Agriculture Grant 2016-67012-24652 to A.J.R.

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