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OFF-HOST PHYSIOLOGICAL
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ECOLOGY OF IXODID TICKS! Glen R. Needham Acarology Laboratory, Department of Entomology, Colleges of Agriculture and Biological Sciences, The Ohio State Universi ty, Columbus, Ohio 43210-1292
Pete D. Teel Department of Entomology, Texas A&M University, College Station, Texas 778432475 KEY WORDS:
water-balance physiology, tick survival, water-vapor sorption, Ixodidae, zoogeographic interpretations
INTRODUCTION Ixodid ticks (Acari: Ixodidae) have notable abilities to imbibe and to con centrate a large volume of vertebrate blood. Through their feeding, they may act as vectors of disease or debilitate by exsanguination or injection of salivary toxin. The brief on-host interval is characterized by rapid metabolism and development while eliminating a water and electrolyte load several times the body weight of the tick as it increases in body size. In contrast, survival between blood meals comprises
>90% of the tick's life and is highly con
servative physiologically. Between blood meals, nutrient reserves must be economically used and body-water content maintained or desiccation and ultimately death results. During off-host periods, ticks experience the rigors of environmental stresses associated with the climate of the immediate habi tat. Susceptibility to injury from temperature extremes and to desiccation varies with tick species, stage, sex, age, and physiological condition. BodyIWe dedicate this review in the memory of deceased Professors of Acarology Manning A. Price and George W. Wharton.
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0066-4170/91/0101-0659$02.00
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water homeostasis is one of the most important processes that influences off-host survival. Researchers have made considerable progress in un derstanding water balance in the Acari (3, 45, 46, 66, 78, 95, 96), but many questions remain unanswered. Some difficulties also exist because in vestigators variously interpret observations of water flow, water potentials, and the influence of humidity and temperature (95). A complete understanding of the impact of environmental stressors on tick water balance, survivorship, and ecological interpretations has not emerged, yet these factors are essential to certain modelling objectives and in terpretations (13). Computers and modelling techniques are tools that have been used to examine complex zoogeographic interrelationships (hosts, vegetation, meteorology, and pathogens) of a few well-known species, in cluding Boophilus microplus (88), Amblyomma americanum (29, 63), Der macentor variabilis (64), and Rhipicephalus appendiculatus (57, 71a). The objectives and interpretations of these models are limited by the degree to which fundamental relationships such as development, population growth, and survival are understood and/or by the extent of available data bases. Prior reviews of water balance by ticks between bloodmeals (45, 46, 6 6, 79) suggested that integumental permeability to water flux and the amount of water in a tick may be of greater value in interpreting survival potential and habitat associations of ixodid ticks than critical equilibrium activity (CEA). Here we address off-host physiological ecology in light of recent findings on active water-vapor uptake and comparative studies of three- and one-host tick survival as a function of whole-body permeability and water content (39, 41, 83, 85; M. D. Sigal & G. R. Needham; P. D. Teel & Needham; Tee!, O. F. Strey, Needham, & M. T. Longnecker, in preparation). We begin with brief overviews on tick biology, water balance, and integument as a preamble to the presentation on water-balance parameters and their correlations with off-host survival. We attempt this assessment to facilitate the application of whole-organism water-balance perspectives to arthropod (tick) survival at the suggestion of Eric Edney, who 15 years ago published his monograph on terrestrial-arthropod water balance (16). For information on other factors that influence survival, the reader is referred to reports on diapause and drop-off rhythms (7), cold hardiness (50), and behavior (8, 30, 52a, 54, 55). Much of the literature concerning water balance of arthropods (including ticks) is found in reviews by Arlian & Veselica (3), Edney (16), Kniille (45), Machin (59), O'Donnell & Machin (71) and Wharton (95). TICKS AS GORGING-FASTING ORGANISMS
An alternate off-host, on-host life-cycle strategy requires ticks to deal with very different natural selection factors in the two situations. Wharton (94)
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refers to animals using this lifestyle as gorging-fasting organisms. Ticks as a group survive longer than any other arthropod without food or drinking water. For example, a typical univoltine ixodid species spends a total of 12-21 days on the host (larvae, 3-5 days; nymphs, 3-5 days, adult females, 6-11 days) for an off-host annual percentage of 94-97. An even higher off-host percent age is possible when adults live for more than one season. This impressive capacity is the product of many adaptive features that conserve energy and water so that life may be extended for months or years (38, 54, 97). When exposed to optimal abiotic conditions in the absence of a host, ticks typically outlive the animals they parasitize (e.g. rodents). Those concerned with animal and human health must be cognizant of this factor when surveying hosts and ticks for the presence of disease organisms or if contemplating a tick or host reduction program. The transformation from a fasting state, adapted for off-host existence in which dramatic abiotic (extrinsic) fluctuations may occur, to a gorging state, in which biotic (intrinsic) and more stable abiotic factors are offered by the host, challenges the tick while it attaches, feeds, and mates (4, 33, 35). The gorging interval is characterized by rapid metabolism and development ac companied by the elimination of excess ions and water back into the host. This intimate association results in the exchange of body fluids between parasite and host, which facilitates infection of the tick by microorganisms or transmission of disease agents to the host (5, 42). Ticks transmit a greater variety of infectious agents than any other group of blood-feeding arthropods (34). Tick saliva maintains the feeding lesion by injecting anti-edema com ponents (76), and the mouth parts of some ixodid ticks are secured in place by an attachment cement that also serves as a gasket (62). The soft integument of the body of immatures and adult females grows, unfolds, and stretches to accommodate the high-volume fluid diet (2, 17, 24, 25). Male metastriate ticks, although attached for extensive periods between matings, take in little host fluid because a nonexpandable sderotized scutum covers most of the dorsum. Mating generally occurs on the host after some interval of feeding by both sexes, and after engorgement the fed immature or adult female detaches and falls to the ground where development is completed or a preoviposition period is followed by egg laying. Most ixodids follow this pattern except for one- and two-host species in which one or both immature stages (larva and nymph) remain on the same animal to continue feeding and development, thus limiting intrastadial exposure to the off-host environment. Off-host fasting is characterized by slow metabolism with lengthy intervals of inactivity, punctuated by movement within the microhabitat to increase water uptake, or to seek a position for detection of a passing blood-meal source (8, 54, 55). Long off-host survival increases the chance of locating a suitable animal. If microenvironmental temperature and relative humidity remain within upper and lower thresholds (without considering numerous
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Annu. Rev. Entomol. 1991.36:659-681. Downloaded from www.annualreviews.org by University of Massachusetts - Amherst on 04/22/13. For personal use only.
negative biotic factors), then survival becomes a function of maintaining the delicate balance between judicious energy use and maintenance of body water content (38, 54, 97). Over the short term, especially when environmental stress is high because of seasonal factors 'and/or if the habitat type is less than optimal, water balance is probably the most critical factor. At the risk of oversimplification, energy depeletion that could result in the inability to maintain water balance may lead to death after long-term survival.
WATER-BALANCE PHYSIOLOGY The water-balance physiology of all terrestrial arthropods serves as the foundation for this review. Maintenance of body water is critical to these animals that have large surface-to-volume ratios. All terrestrial arthropods have a superficial layer of lipid that minimizes water loss from the animal and enables it to survive an otherwise desiccating environment (26, 27). The impediment to water loss offered by this barrier can be illustrated simply by placing a droplet of water about the size of a tick on a nonabsorptive surface and observing how long it takes to evaporate. This remarkable barrier is one of the chief reasons this assemblage of animals dominates the terrestrial environment, yet the integument is one of the least studied organs. Water conservation is the product of many mechanisms, including an internal respiratory system that is guarded from the external environment by a valve and sometimes other specialized structures, excretion of nitrogenous waste in a water-conserving form (uric acid or guanine), and reabsorption of water from fecal material by the rectum. Water is obtained from drinking, eating hydrated food, vapor absorption (from air), and through metabolic processes. Water turnover between the arthropod and the surrounding en vironment may be dramatic, or it may involve the exchange of but a few water molecules per hour; the critical net result is that water balance must be maintained or the animal will perish. The quantity of water in an insect or acarine may be expressed in different ways (3, 95). It is best expressed as the ratio of water weigh! to total weight times 100, or water as a percentage of total weight, and is estimated by subtracting the dry weight from total weight. Hemolymph serves as the main water reserve in ticks (37). Sigal (85) found that adult male and female A. americanum (lone star ticks) can lose as much as 70% of the water mass before losing locomotor ability. This percentage represents one of the highest tolerance levels reported for any arthropod (16), and adult lone star ticks are not considered particularly hardy compared to adults of other ixodid species. Exchange of body water with the environment has been described using a combination of units (e.g. activity, osmotic pressure in millimeters of mer cury, osmolality, freezing point depression, or NaCl equivalents; see 3, 16).
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Because water moves, it seems logical to quantify water using the same measurement both inside and outside the animal, that is, as the ratio of the solution (solvent) to the total number of ions and molecules present. This method has been adopted by Arlian & Veselica (3), Edney (16), and Wharton & Richards (96), and these authors give further rationale for using activity in their studies. The ratio corresponds to the activity aw of the solution (ideal). Activity of liquid water is the same as the activity of water (ay) in air in equilibrium with a plane surface of an aqueous solution at the same tempera ture. The concentration of water in air is generally given in units of percentage RH or relative humidity, which equals the ay times 100. For ticks, the aw (of hemolymph or cytosol) is around 0.99 and that of the surrounding atmospher ic ay is generally less. As water tends to move to sites of lesser activity, ticks generally find themselves in a desiccating circumstance and must rely on other sources of water to make up the deficit. Transpiration The rate at which water leaves (transpiration) is determined by the chemical potential of the body fluids (aw), the total water pool mass, and the permeabil ity of the waterproofing barrier. Diffusion and bulk flow thoroughly mix water pools such that each molecule has the same chance of escaping as every other. This is in fact the definition of a single well-mixed compartment, and includes any separate compartment that operates in parallel (95). Exchange able water then is unbound and is available for participation in transpiration. Sources of water for transpiration (e.g. hemolymph, gut, etc) and the internal exchange of water are discussed elsewhere (37, 66). Transpiration rates can be expressed as a constant percentage loss (% h -\) of this exchangeable water mass. Causes for changes in the rate are discussed below. An instanteous rate equals the product of the rate constant (permeability) and water mass (e.g. mg h-1). The driving force for water movement is the concentration of water molecules in the compartment, and though the water pool is finite, the driving force remains virtually the same, at least while the organism is alive (> 0.98 aw). A doubling of hemolymph osmotic pressure has little impact on the aw• Transpiration is responsible for most water loss, unless the respiration rate is significant (80). Wharton (95) describes the simplification of Crank's (12) equations for solving the problem of evaporation from a surface and justifies not using Pick's law for describing water movement. The conditions that make sim plification possible are: the water pool is well mixed; transpiration rate is slow compared to the rate of mixing and the rate of diffusion away from the surface after a water molecule escapes; and the geometry of one individual is es sentially the same as every other. This latter condition allows for the com-
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parison of ticks as whole organisms without expressing flux rates as a function of surface area. Of concern also is the permeability with respect to symmetry of the integument, that is, does water move out at a different rate than it moves in? Water passes through the same integumental layers during sorption and transpiration except that the order is reversed, and the integument is, for practical purposes, symmetric in its resistance to water movement. Differ ences in rate of movement can be accounted for primarily in the driving forces contributed by the ay outside or aw inside, although Wharton (95) explains that water flow into dry air is somewhat slower than its movement into moist air. His rationale for mentioning this difference is given in his review (95). The integument was thought to be the site of active vapor sorption, and this belief misled some to think that the integument was asymmetric. Specific sites account for all known active uptake mechanisms in arthropods (59, 7 1). Sorption
Sorption is driven by the free energy of water vapor and is proportional to the ay because the source of water is virtually infinite. Any study of sorption must include an analysis of contributions by metabolic water during the ex periment; thus, an estimate of respiratory rate can avoid confusion. When sorption rate (passive and active) equals transpiration rate, the water mass is in a state of equilibrium. Periods when net water loss occur can be com pensated for by active uptake (drinking water, vapor absorption) and doing so greatly extends the life of the organism from days to weeks or months. The critical equilibrium activity is the ay at which equilibrium weight is main tained and is related to whole-animal water balance (47). Water-Vapor Sorption
Water-vapor absorption (WVA) is an energy-dependent process used by arthropods to obtain water directly from unsaturated air (71). WVA provides a source of water separate from all other avenues, including intake of hydrated food (blood), drinking liquid water, or metabolism. This ability is particularly important for organisms that experience long periods of starvation, have slow metabolic rates, have limited abilities to disperse, and drink liquid water infrequently, if at all. Most ticks (immatures and adults) extract water vapor from unsaturated air (39, 44, 46, 48, 51; M. D. Sigal, 1. H. Machin & G. R . Needham, i n preparation). Uptake intervals are intermittant and desiccation thresholds that might initiate the process have not been determined. Adult Amblyomma variegatum weights fluctuate ±2% of their original weight when held at 0.93 av; no specific lower value initiates uptake (79). One measure of WVA ability is the gravimetric determination of a CEA. If a test population of standardized, fasting specimens maintains body weight in an ay below 0. 99,
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then a WVA capability is most likely present. CEA values are the net result of many factors, including transpiration, the "pump" threshold ay for active uptake (see below), and loss of water via avenues other than the integument. Each specimen has its own equilibrium ay and weight at that moment in time in this laboratory determination. Published CEA values range from 0.75 to 0 . 94 ay (46). Variability in reported CEA values is not surprising when one factors in age, stage, inherited variability, prior exposure to extrinsic factors, and what host(s) was fed upon (46). For adult A. americanum, values range from 0.80 to > 0.88 ay (31, 81; M. D. Sigal & G. R. Needham, in preparation). These are lower than estimates for adult Amblyomma macula lum, ranging from> 0.86 (M . D. Sigal & G. R. Needham, in preparation) to 0.88-0.90 (51) and 0.92-0.93 (31). The Amblyomma cajennense CEA range was 0.90-0.92 (51). Adult one-host ticks that would normally not experience off-host conditions cannot maintain consistent equilibrium weights below saturation and apparently lack WVA capability (46; M. D. Sigal & G. R. Needham, in preparation). CEA values are useful especially when selecting a humidity for maintaining a laboratory colony or for choosing experimental conditions, but using them as indicators of habitat preference can be mislead ing as we will discuss later. Machin (59) and O'Donnell & Machin (71) have encouraged investigators to determine the pump threshold because it provides more information about WVA. They describe a graphic procedure for estimating the pump threshold from the gain and loss rates above and below the CEA. Use of the term pump means energy was required to transport water against a concentration gra dient. Pump threshold denotes the true physiological point (ay) when uptake commences. The threshold ay may be near the CEA if the integument of the tick is highly waterproofed; however, if the tick is particularly permeable, then the threshold will be lower than the CEA. Theoretically, a tick with a high pump threshold (near saturation) and leaky cuticle might not appear capable of WVA. This possibility is examined below. Pump thresholds for several tick species have been estimated by Machin (59), and values ranged from 74-89% relative humidity for A. americanum adults according to data from Sauer & Hair (81) and Hair et al (31). Factors that characterize a pump site are absorption capacity and absorption conductance ( 1 1). These factors have not been evaluated for ticks. Examination of WVA capabilities reveals the following for different stages and physiological conditions. The egg stage of ticks is not believed to be capable of active uptake, but this condition has not been adequately studied. The unfed stages of most ticks examined thus far have WVA capability, unless that stage spends its unfed period on the host, as do nymphs of two-host species or nymphs and adults of one-host species. Fed larvae and nymphs of three-host Ixodes dammini, Ixodes ricinus, and Haemaphysalis punctata as well as engorged larvae and first-instar nymphs of the multi-host
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(Argasidae) are capable of active uptake (39, 4 1). Active uptake can commence within 1-3 days after feeding. Investigators (39, 41) found that larval Dermacentor marginatus (three-host) and nymphal Hyalom ma anatolicum excavatum (three-host) do not display the capability of water vapor absorption. Active uptake masked by loss via the integument andior tracheal system (nymphs) cannot be ruled out at this time (39). In engorged D. marginatus nymphs, however, active uptake was present but did not lead to substantial net gain at 95% RHl15°C (39). Molting ticks lose uptake capabil ity during the early pharate phase, just after apolysis (separation of cuticle from hypodermal cells of the integument), but I. dammini and I. ricinus regain uptake competence within hours postecdysis (39, 41). Each stage (unfed and engorged) must be examined to determine its WVA capability. Some specimens of adult Dermacentor albipictus intermittantly absorbed water vapor based on weighings, but most individuals were WVA in competent (M. D. Sigal & G. R. Needham, in preparation). Investigations of salivary gland structure at the light microscope level (40) suggest that engorged I. ricinus females may be water-vapor absorption competent until near the end of oviposition. Previously, Kahl (39) observed temporary weight gain in partially engorged preovipositing females but not in fully engorged females. He speculates that water vapor absorption should be impossible during oviposition because the gnathosoma is covered by a viscous secretion beginning a few days before oviposition commences. Partially engorged females, once having entered this phase, never gained weight. Fully engorged females usually lose water in the preoviposition interval, and Kahl notes that active uptake does not occur; however, loss of water via respiration andior transpiration could mask water vapor absorption. To sort out some of this contradictory information, mouth-blocking experiments have been per formed. Engorged preovipositing I. ricinus females with wax-blocked mouth parts did not alter the rate of water loss (39). M. Fahmy, G. R. Needham, & M. D. Sigal (in preparation) obtained the same result with A. americanum. Salivary glands from these females are being examined ultrastructurally to confirm or refute the hypothesis that uptake occurs prior to or during oviposi tion (M. Fahmy, G. R. Needham, & L. B. Coons, in preparation). At least for these two species, WVA apparently does not occur in the preoviposition interval. Rudolph's & Kniille's (46, 78, 79) pioneering work demonstrated that the mouth was the site of uptake in ixodid and argasid ticks. They suggested that the salivary glands were involved in uptake by generating a concentrated hygroscopic salt solution. We (66) also proposed that uptake via hydrophilic cuticle might be responsible, as in the desert burrowing cockroach Arenivaga investigata (70, 71), which has hydrophilic setae. We readdressed the uptake hypothesis because oral fluid from rehydrating ticks had not been examined, and the cheliceral-sheath denticles offer a potentially large surface area for
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Argas reflexus
OFF-HOST ECOLOGY OF TICKS
667
sorption. Oral fluid in ticks either changes the hydrophilic nature of the mouth-part cuticle, as with A. investigata, or serves as a hygroscopic sub stance itself that would support the solute-driven mechanism proposed at the outset. Oral secretions from two rehydrating A. americanum females (as
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determined using a recording electrobalance) have recently been analyzed as
frozen thick sections of the mouth parts (M. D. Sigal, 1. H. Machin, & G. R. Needham, in preparation). Fluid in the lateral salivarium compartment, near where the hypostome and chelicerae converge to form the basis capituli, thawed at between -10 and -12°C (�6.5-5. 4 osmoles). Such a solution would be in eqUilibrium with a humidity near the CEA range for this tick (�90%). This observation confirms earlier suggestions that ticks use a solute driven vapor-uptake mechanism rather than hydrophilic cuticle. The salivary glands are the apparent source of the hygroscopic fluid responsible for uptake (40, 46, 58, 79). Comparative ultrastructural (65, 66) and light-level (40) descriptions of the type I (type A, argasids) salivary gland acini are given elsewhere.
Concentrated salt on the mouth parts of severely desiccated ticks may serve as temporary storage in water homeostasis. The salt is probably secreted there by the salivary glands (66, 79). As ticks desiccate and body fluids become concentrated, the salivary gland type I acini probably excrete the salt onto the mouth parts until rehydration is possible (40, 65). These salts delequesce at subsaturated humidities near the CEA for the tick (79), and may initiate active
vapor uptake. M. D. Sigal, J. H. Machin, & G. R. Needham (in preparation) stimulated unfed adult A. americanum to produce concentrated oral solutions 8) within minutes of exposure to incandescent (0.43 to 5.11 osmoles, n =
light and to heat. The residue dried immediately at a relatively low humidity.
Behavior-Associated Hydration State and Vapor Absorption
Lees (54) and Camin (8) presented some of the most stimulating thoughts on behavior associated with hydration state. Both recognized the balance be tween hydration state and host seeking as determinants for where a tic k was positioned within the vegetation. It is beyond the scope of this review to discuss off-host behavior, but the reader is referred to reports on Ixodes ricinus
84), A. (31a).
(54, 56), I. persulcatus (16a), Rhipicephalus appendiculatus (72-74, maculatum (18, 19), Dermacentor occidentalis (49), and D. variabilis
IXODID INTEGUMENT Physical Properties of the Cuticle
Ticks have a large surface-to-volume ratio and are prone to desiccation. One of the most important factors that has enabled arthropods in general to be the dominant terrestrial animal form is the ability of the integument to restrict
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water loss. This factor was essential for the transition of arthropods from an aquatic to a terrestrial existence
(27). Lipids associated with the epicuticle are
thought to form the primary barrier to water loss by most terrestrial arthropods and plants
(26). Other specialized integumental features restrict water loss
the spiracles of ixodid nymphs and adults (larvae have no spiracles) are covered by a spiracular plate and ventilation is regulated by a closing mech anism
(80). The oral cavity is formed dorsally by closely opposed paired
chelicerae, ventrally by the hypostome, and laterally by palpi that for many
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species partially enclose the dorso-ventral structures. This arrangement prob ably limits water loss from the mouth unless the palps are splayed. The anus is secured by valves. Hygroreceptors (setae) enable the tick to sense humidity gradients
(32). Only a few investigators beginning with Lees (52) have
studied tick integument. It is quite similar to insect integument, except the cement layer is apparently absent from the epicuticle of ixodids, making the unprotected lipid layer particularly susceptible to damage
(2, 17, 24, 25).
Whole-Body Permeability Integumental permeability, as shown by Lees (51), determines tick water-loss rates. Ticks held below the CEA die from desiccation very quickly if they are particularly permeable, while those that lose water slowly live quite some time by comparison (Table
1). Water-loss rates for ticks measured at 0 av are
actually whole-body permeability estimations that include water loss via the respiratory system, from oral and anal excretions, and any other physiological process that involves the loss of water
(66, 95; M. D . Sigal & G. R.
Needham, in preparation). Freda & Needham (20) suggest that these addition al avenues contribute proportionally much less than does integumentary loss, although an increase in locomotor activity can dramatically increase respira tory water loss
(79).
An understanding of certain principles is critical for studies that estimate the permeability of an organism. First, gravimetric values of permeability must be determined at near
0 avo This determination eliminates any contribu
tion of passive water to the water pool---otherwise permeability will be underestimated. That is not to say that experiments done in the presence of
(3 1 ) report that A. americanum 32% RH showed a difference in permeability, and they
atmospheric water are of no value. Hair et al and A. maculatum at
suggest that this played a key role in habitats each species could occupy. Recent studies demonstrated that A . americanum water-loss rates from the whole-body water pool increased with age
(M. D. Sigal & G. R. Needham, in (51, 52) that
preparation), which supports previous observations by Lees
ixodid CEAs increased with age. The greater rates of water loss probably raise water balance equilibrium thresholds in older ticks, resulting in CEAs at correspondingly higher relative avs.
OFF-HOST ECOLOGY OF TICKS
,,,fl1b
i].Hosl
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669
l
Tick (mesic)
Att;ve ,orption
�� Active sorption
Figure 1
(?)
Whole-body permeability (passive sorption and transpiration) and active-water vapor
uptake capability compared for three hypothetical adult ixodid tick species. Size of arrows indicates relative rate (large - fast. small - slow) of water movement. Limiting barrier represents integument: top figure is a tick that loses water slowly; the bottom figure is a leaky tick; and the middle panel represents a tick of intermediate integumental permeability. Internal eliptical shapes represent internal pools of different sizes from which water may be lost to the atmosphere . The top panel represents a tick that would survive in quite dry microhabitats and would move only occasionally to seek
a
higher humidity for rehydration; while the bottom panel
represents a tick that is leaky, has a small water pool, may not take water from the air actively (via mouth), and would survive only a few days at most in a dry microhabitat. The middle panel diagrams a tick that may have to move daily between microhabitats for rehydration and those where a host may be accessed. Figure provided by M. D. Sigal.
A fundamental question concerning the water-balance physiology of arthro pods including ticks is the amount of control they have over responding to changing ambient humidity conditions by altering integumental permeability (60, 6 1, 67-69). Integumental permeability control in ticks has not been adequately addressed. Short-term exposure ( 2 weeks) to low humidity did not appear to influence transpiration rates (20). Ticks respond to superficial abrasion by repairing damage (28, 52). As already mentioned, permeability increases with age as indicated by whole-body permeability measurements, but the reason for this increase is unknown. Deposition and removal of lipids also occur during engorgement and molting (14, 15, 28). Evidence for the transition in cuticle permeability from an engorging on-host tick to an en gorged off-host physiological condition emerges from several different stud ies (9, 81). The amount of extractable cuticular lipid per engorged female Boophilus micropius increased threefold over some nine days postdetachment (9), suggesting that the off-host individual is more protected from desiccation than one on the host. Engorged A. americanum females also seem more resistant to desiccation than unfed ticks (81). Alloscutal integument grows �
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Table 1
Comparison of water-balance and survival parameters which characterize adults of
five ixodid spec ie s'
1bree-hosl
speQcs
WhoIo-bodyb pcrmcabili!y (.., h-I)
newly� (mg)
0_2827±.0340 (10) 0.31S6±.0340 (10)
4.30±0.33 (16) 2.3S±O.IS (14)
0.1067±.OOO3 (10) 0.1064±.0004 (10)
� Mortality
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OFF-HOST PHYSIOLOGICAL
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ECOLOGY OF IXODID TICKS! Glen R. Needham Acarology Laboratory, Department of Entomology, Colleges of Agriculture and Biological Sciences, The Ohio State Universi ty, Columbus, Ohio 43210-1292
Pete D. Teel Department of Entomology, Texas A&M University, College Station, Texas 778432475 KEY WORDS:
water-balance physiology, tick survival, water-vapor sorption, Ixodidae, zoogeographic interpretations
INTRODUCTION Ixodid ticks (Acari: Ixodidae) have notable abilities to imbibe and to con centrate a large volume of vertebrate blood. Through their feeding, they may act as vectors of disease or debilitate by exsanguination or injection of salivary toxin. The brief on-host interval is characterized by rapid metabolism and development while eliminating a water and electrolyte load several times the body weight of the tick as it increases in body size. In contrast, survival between blood meals comprises
>90% of the tick's life and is highly con
servative physiologically. Between blood meals, nutrient reserves must be economically used and body-water content maintained or desiccation and ultimately death results. During off-host periods, ticks experience the rigors of environmental stresses associated with the climate of the immediate habi tat. Susceptibility to injury from temperature extremes and to desiccation varies with tick species, stage, sex, age, and physiological condition. BodyIWe dedicate this review in the memory of deceased Professors of Acarology Manning A. Price and George W. Wharton.
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water homeostasis is one of the most important processes that influences off-host survival. Researchers have made considerable progress in un derstanding water balance in the Acari (3, 45, 46, 66, 78, 95, 96), but many questions remain unanswered. Some difficulties also exist because in vestigators variously interpret observations of water flow, water potentials, and the influence of humidity and temperature (95). A complete understanding of the impact of environmental stressors on tick water balance, survivorship, and ecological interpretations has not emerged, yet these factors are essential to certain modelling objectives and in terpretations (13). Computers and modelling techniques are tools that have been used to examine complex zoogeographic interrelationships (hosts, vegetation, meteorology, and pathogens) of a few well-known species, in cluding Boophilus microplus (88), Amblyomma americanum (29, 63), Der macentor variabilis (64), and Rhipicephalus appendiculatus (57, 71a). The objectives and interpretations of these models are limited by the degree to which fundamental relationships such as development, population growth, and survival are understood and/or by the extent of available data bases. Prior reviews of water balance by ticks between bloodmeals (45, 46, 6 6, 79) suggested that integumental permeability to water flux and the amount of water in a tick may be of greater value in interpreting survival potential and habitat associations of ixodid ticks than critical equilibrium activity (CEA). Here we address off-host physiological ecology in light of recent findings on active water-vapor uptake and comparative studies of three- and one-host tick survival as a function of whole-body permeability and water content (39, 41, 83, 85; M. D. Sigal & G. R. Needham; P. D. Teel & Needham; Tee!, O. F. Strey, Needham, & M. T. Longnecker, in preparation). We begin with brief overviews on tick biology, water balance, and integument as a preamble to the presentation on water-balance parameters and their correlations with off-host survival. We attempt this assessment to facilitate the application of whole-organism water-balance perspectives to arthropod (tick) survival at the suggestion of Eric Edney, who 15 years ago published his monograph on terrestrial-arthropod water balance (16). For information on other factors that influence survival, the reader is referred to reports on diapause and drop-off rhythms (7), cold hardiness (50), and behavior (8, 30, 52a, 54, 55). Much of the literature concerning water balance of arthropods (including ticks) is found in reviews by Arlian & Veselica (3), Edney (16), Kniille (45), Machin (59), O'Donnell & Machin (71) and Wharton (95). TICKS AS GORGING-FASTING ORGANISMS
An alternate off-host, on-host life-cycle strategy requires ticks to deal with very different natural selection factors in the two situations. Wharton (94)
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refers to animals using this lifestyle as gorging-fasting organisms. Ticks as a group survive longer than any other arthropod without food or drinking water. For example, a typical univoltine ixodid species spends a total of 12-21 days on the host (larvae, 3-5 days; nymphs, 3-5 days, adult females, 6-11 days) for an off-host annual percentage of 94-97. An even higher off-host percent age is possible when adults live for more than one season. This impressive capacity is the product of many adaptive features that conserve energy and water so that life may be extended for months or years (38, 54, 97). When exposed to optimal abiotic conditions in the absence of a host, ticks typically outlive the animals they parasitize (e.g. rodents). Those concerned with animal and human health must be cognizant of this factor when surveying hosts and ticks for the presence of disease organisms or if contemplating a tick or host reduction program. The transformation from a fasting state, adapted for off-host existence in which dramatic abiotic (extrinsic) fluctuations may occur, to a gorging state, in which biotic (intrinsic) and more stable abiotic factors are offered by the host, challenges the tick while it attaches, feeds, and mates (4, 33, 35). The gorging interval is characterized by rapid metabolism and development ac companied by the elimination of excess ions and water back into the host. This intimate association results in the exchange of body fluids between parasite and host, which facilitates infection of the tick by microorganisms or transmission of disease agents to the host (5, 42). Ticks transmit a greater variety of infectious agents than any other group of blood-feeding arthropods (34). Tick saliva maintains the feeding lesion by injecting anti-edema com ponents (76), and the mouth parts of some ixodid ticks are secured in place by an attachment cement that also serves as a gasket (62). The soft integument of the body of immatures and adult females grows, unfolds, and stretches to accommodate the high-volume fluid diet (2, 17, 24, 25). Male metastriate ticks, although attached for extensive periods between matings, take in little host fluid because a nonexpandable sderotized scutum covers most of the dorsum. Mating generally occurs on the host after some interval of feeding by both sexes, and after engorgement the fed immature or adult female detaches and falls to the ground where development is completed or a preoviposition period is followed by egg laying. Most ixodids follow this pattern except for one- and two-host species in which one or both immature stages (larva and nymph) remain on the same animal to continue feeding and development, thus limiting intrastadial exposure to the off-host environment. Off-host fasting is characterized by slow metabolism with lengthy intervals of inactivity, punctuated by movement within the microhabitat to increase water uptake, or to seek a position for detection of a passing blood-meal source (8, 54, 55). Long off-host survival increases the chance of locating a suitable animal. If microenvironmental temperature and relative humidity remain within upper and lower thresholds (without considering numerous
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negative biotic factors), then survival becomes a function of maintaining the delicate balance between judicious energy use and maintenance of body water content (38, 54, 97). Over the short term, especially when environmental stress is high because of seasonal factors 'and/or if the habitat type is less than optimal, water balance is probably the most critical factor. At the risk of oversimplification, energy depeletion that could result in the inability to maintain water balance may lead to death after long-term survival.
WATER-BALANCE PHYSIOLOGY The water-balance physiology of all terrestrial arthropods serves as the foundation for this review. Maintenance of body water is critical to these animals that have large surface-to-volume ratios. All terrestrial arthropods have a superficial layer of lipid that minimizes water loss from the animal and enables it to survive an otherwise desiccating environment (26, 27). The impediment to water loss offered by this barrier can be illustrated simply by placing a droplet of water about the size of a tick on a nonabsorptive surface and observing how long it takes to evaporate. This remarkable barrier is one of the chief reasons this assemblage of animals dominates the terrestrial environment, yet the integument is one of the least studied organs. Water conservation is the product of many mechanisms, including an internal respiratory system that is guarded from the external environment by a valve and sometimes other specialized structures, excretion of nitrogenous waste in a water-conserving form (uric acid or guanine), and reabsorption of water from fecal material by the rectum. Water is obtained from drinking, eating hydrated food, vapor absorption (from air), and through metabolic processes. Water turnover between the arthropod and the surrounding en vironment may be dramatic, or it may involve the exchange of but a few water molecules per hour; the critical net result is that water balance must be maintained or the animal will perish. The quantity of water in an insect or acarine may be expressed in different ways (3, 95). It is best expressed as the ratio of water weigh! to total weight times 100, or water as a percentage of total weight, and is estimated by subtracting the dry weight from total weight. Hemolymph serves as the main water reserve in ticks (37). Sigal (85) found that adult male and female A. americanum (lone star ticks) can lose as much as 70% of the water mass before losing locomotor ability. This percentage represents one of the highest tolerance levels reported for any arthropod (16), and adult lone star ticks are not considered particularly hardy compared to adults of other ixodid species. Exchange of body water with the environment has been described using a combination of units (e.g. activity, osmotic pressure in millimeters of mer cury, osmolality, freezing point depression, or NaCl equivalents; see 3, 16).
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Because water moves, it seems logical to quantify water using the same measurement both inside and outside the animal, that is, as the ratio of the solution (solvent) to the total number of ions and molecules present. This method has been adopted by Arlian & Veselica (3), Edney (16), and Wharton & Richards (96), and these authors give further rationale for using activity in their studies. The ratio corresponds to the activity aw of the solution (ideal). Activity of liquid water is the same as the activity of water (ay) in air in equilibrium with a plane surface of an aqueous solution at the same tempera ture. The concentration of water in air is generally given in units of percentage RH or relative humidity, which equals the ay times 100. For ticks, the aw (of hemolymph or cytosol) is around 0.99 and that of the surrounding atmospher ic ay is generally less. As water tends to move to sites of lesser activity, ticks generally find themselves in a desiccating circumstance and must rely on other sources of water to make up the deficit. Transpiration The rate at which water leaves (transpiration) is determined by the chemical potential of the body fluids (aw), the total water pool mass, and the permeabil ity of the waterproofing barrier. Diffusion and bulk flow thoroughly mix water pools such that each molecule has the same chance of escaping as every other. This is in fact the definition of a single well-mixed compartment, and includes any separate compartment that operates in parallel (95). Exchange able water then is unbound and is available for participation in transpiration. Sources of water for transpiration (e.g. hemolymph, gut, etc) and the internal exchange of water are discussed elsewhere (37, 66). Transpiration rates can be expressed as a constant percentage loss (% h -\) of this exchangeable water mass. Causes for changes in the rate are discussed below. An instanteous rate equals the product of the rate constant (permeability) and water mass (e.g. mg h-1). The driving force for water movement is the concentration of water molecules in the compartment, and though the water pool is finite, the driving force remains virtually the same, at least while the organism is alive (> 0.98 aw). A doubling of hemolymph osmotic pressure has little impact on the aw• Transpiration is responsible for most water loss, unless the respiration rate is significant (80). Wharton (95) describes the simplification of Crank's (12) equations for solving the problem of evaporation from a surface and justifies not using Pick's law for describing water movement. The conditions that make sim plification possible are: the water pool is well mixed; transpiration rate is slow compared to the rate of mixing and the rate of diffusion away from the surface after a water molecule escapes; and the geometry of one individual is es sentially the same as every other. This latter condition allows for the com-
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parison of ticks as whole organisms without expressing flux rates as a function of surface area. Of concern also is the permeability with respect to symmetry of the integument, that is, does water move out at a different rate than it moves in? Water passes through the same integumental layers during sorption and transpiration except that the order is reversed, and the integument is, for practical purposes, symmetric in its resistance to water movement. Differ ences in rate of movement can be accounted for primarily in the driving forces contributed by the ay outside or aw inside, although Wharton (95) explains that water flow into dry air is somewhat slower than its movement into moist air. His rationale for mentioning this difference is given in his review (95). The integument was thought to be the site of active vapor sorption, and this belief misled some to think that the integument was asymmetric. Specific sites account for all known active uptake mechanisms in arthropods (59, 7 1). Sorption
Sorption is driven by the free energy of water vapor and is proportional to the ay because the source of water is virtually infinite. Any study of sorption must include an analysis of contributions by metabolic water during the ex periment; thus, an estimate of respiratory rate can avoid confusion. When sorption rate (passive and active) equals transpiration rate, the water mass is in a state of equilibrium. Periods when net water loss occur can be com pensated for by active uptake (drinking water, vapor absorption) and doing so greatly extends the life of the organism from days to weeks or months. The critical equilibrium activity is the ay at which equilibrium weight is main tained and is related to whole-animal water balance (47). Water-Vapor Sorption
Water-vapor absorption (WVA) is an energy-dependent process used by arthropods to obtain water directly from unsaturated air (71). WVA provides a source of water separate from all other avenues, including intake of hydrated food (blood), drinking liquid water, or metabolism. This ability is particularly important for organisms that experience long periods of starvation, have slow metabolic rates, have limited abilities to disperse, and drink liquid water infrequently, if at all. Most ticks (immatures and adults) extract water vapor from unsaturated air (39, 44, 46, 48, 51; M. D. Sigal, 1. H. Machin & G. R . Needham, i n preparation). Uptake intervals are intermittant and desiccation thresholds that might initiate the process have not been determined. Adult Amblyomma variegatum weights fluctuate ±2% of their original weight when held at 0.93 av; no specific lower value initiates uptake (79). One measure of WVA ability is the gravimetric determination of a CEA. If a test population of standardized, fasting specimens maintains body weight in an ay below 0. 99,
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then a WVA capability is most likely present. CEA values are the net result of many factors, including transpiration, the "pump" threshold ay for active uptake (see below), and loss of water via avenues other than the integument. Each specimen has its own equilibrium ay and weight at that moment in time in this laboratory determination. Published CEA values range from 0.75 to 0 . 94 ay (46). Variability in reported CEA values is not surprising when one factors in age, stage, inherited variability, prior exposure to extrinsic factors, and what host(s) was fed upon (46). For adult A. americanum, values range from 0.80 to > 0.88 ay (31, 81; M. D. Sigal & G. R. Needham, in preparation). These are lower than estimates for adult Amblyomma macula lum, ranging from> 0.86 (M . D. Sigal & G. R. Needham, in preparation) to 0.88-0.90 (51) and 0.92-0.93 (31). The Amblyomma cajennense CEA range was 0.90-0.92 (51). Adult one-host ticks that would normally not experience off-host conditions cannot maintain consistent equilibrium weights below saturation and apparently lack WVA capability (46; M. D. Sigal & G. R. Needham, in preparation). CEA values are useful especially when selecting a humidity for maintaining a laboratory colony or for choosing experimental conditions, but using them as indicators of habitat preference can be mislead ing as we will discuss later. Machin (59) and O'Donnell & Machin (71) have encouraged investigators to determine the pump threshold because it provides more information about WVA. They describe a graphic procedure for estimating the pump threshold from the gain and loss rates above and below the CEA. Use of the term pump means energy was required to transport water against a concentration gra dient. Pump threshold denotes the true physiological point (ay) when uptake commences. The threshold ay may be near the CEA if the integument of the tick is highly waterproofed; however, if the tick is particularly permeable, then the threshold will be lower than the CEA. Theoretically, a tick with a high pump threshold (near saturation) and leaky cuticle might not appear capable of WVA. This possibility is examined below. Pump thresholds for several tick species have been estimated by Machin (59), and values ranged from 74-89% relative humidity for A. americanum adults according to data from Sauer & Hair (81) and Hair et al (31). Factors that characterize a pump site are absorption capacity and absorption conductance ( 1 1). These factors have not been evaluated for ticks. Examination of WVA capabilities reveals the following for different stages and physiological conditions. The egg stage of ticks is not believed to be capable of active uptake, but this condition has not been adequately studied. The unfed stages of most ticks examined thus far have WVA capability, unless that stage spends its unfed period on the host, as do nymphs of two-host species or nymphs and adults of one-host species. Fed larvae and nymphs of three-host Ixodes dammini, Ixodes ricinus, and Haemaphysalis punctata as well as engorged larvae and first-instar nymphs of the multi-host
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(Argasidae) are capable of active uptake (39, 4 1). Active uptake can commence within 1-3 days after feeding. Investigators (39, 41) found that larval Dermacentor marginatus (three-host) and nymphal Hyalom ma anatolicum excavatum (three-host) do not display the capability of water vapor absorption. Active uptake masked by loss via the integument andior tracheal system (nymphs) cannot be ruled out at this time (39). In engorged D. marginatus nymphs, however, active uptake was present but did not lead to substantial net gain at 95% RHl15°C (39). Molting ticks lose uptake capabil ity during the early pharate phase, just after apolysis (separation of cuticle from hypodermal cells of the integument), but I. dammini and I. ricinus regain uptake competence within hours postecdysis (39, 41). Each stage (unfed and engorged) must be examined to determine its WVA capability. Some specimens of adult Dermacentor albipictus intermittantly absorbed water vapor based on weighings, but most individuals were WVA in competent (M. D. Sigal & G. R. Needham, in preparation). Investigations of salivary gland structure at the light microscope level (40) suggest that engorged I. ricinus females may be water-vapor absorption competent until near the end of oviposition. Previously, Kahl (39) observed temporary weight gain in partially engorged preovipositing females but not in fully engorged females. He speculates that water vapor absorption should be impossible during oviposition because the gnathosoma is covered by a viscous secretion beginning a few days before oviposition commences. Partially engorged females, once having entered this phase, never gained weight. Fully engorged females usually lose water in the preoviposition interval, and Kahl notes that active uptake does not occur; however, loss of water via respiration andior transpiration could mask water vapor absorption. To sort out some of this contradictory information, mouth-blocking experiments have been per formed. Engorged preovipositing I. ricinus females with wax-blocked mouth parts did not alter the rate of water loss (39). M. Fahmy, G. R. Needham, & M. D. Sigal (in preparation) obtained the same result with A. americanum. Salivary glands from these females are being examined ultrastructurally to confirm or refute the hypothesis that uptake occurs prior to or during oviposi tion (M. Fahmy, G. R. Needham, & L. B. Coons, in preparation). At least for these two species, WVA apparently does not occur in the preoviposition interval. Rudolph's & Kniille's (46, 78, 79) pioneering work demonstrated that the mouth was the site of uptake in ixodid and argasid ticks. They suggested that the salivary glands were involved in uptake by generating a concentrated hygroscopic salt solution. We (66) also proposed that uptake via hydrophilic cuticle might be responsible, as in the desert burrowing cockroach Arenivaga investigata (70, 71), which has hydrophilic setae. We readdressed the uptake hypothesis because oral fluid from rehydrating ticks had not been examined, and the cheliceral-sheath denticles offer a potentially large surface area for
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Argas reflexus
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sorption. Oral fluid in ticks either changes the hydrophilic nature of the mouth-part cuticle, as with A. investigata, or serves as a hygroscopic sub stance itself that would support the solute-driven mechanism proposed at the outset. Oral secretions from two rehydrating A. americanum females (as
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determined using a recording electrobalance) have recently been analyzed as
frozen thick sections of the mouth parts (M. D. Sigal, 1. H. Machin, & G. R. Needham, in preparation). Fluid in the lateral salivarium compartment, near where the hypostome and chelicerae converge to form the basis capituli, thawed at between -10 and -12°C (�6.5-5. 4 osmoles). Such a solution would be in eqUilibrium with a humidity near the CEA range for this tick (�90%). This observation confirms earlier suggestions that ticks use a solute driven vapor-uptake mechanism rather than hydrophilic cuticle. The salivary glands are the apparent source of the hygroscopic fluid responsible for uptake (40, 46, 58, 79). Comparative ultrastructural (65, 66) and light-level (40) descriptions of the type I (type A, argasids) salivary gland acini are given elsewhere.
Concentrated salt on the mouth parts of severely desiccated ticks may serve as temporary storage in water homeostasis. The salt is probably secreted there by the salivary glands (66, 79). As ticks desiccate and body fluids become concentrated, the salivary gland type I acini probably excrete the salt onto the mouth parts until rehydration is possible (40, 65). These salts delequesce at subsaturated humidities near the CEA for the tick (79), and may initiate active
vapor uptake. M. D. Sigal, J. H. Machin, & G. R. Needham (in preparation) stimulated unfed adult A. americanum to produce concentrated oral solutions 8) within minutes of exposure to incandescent (0.43 to 5.11 osmoles, n =
light and to heat. The residue dried immediately at a relatively low humidity.
Behavior-Associated Hydration State and Vapor Absorption
Lees (54) and Camin (8) presented some of the most stimulating thoughts on behavior associated with hydration state. Both recognized the balance be tween hydration state and host seeking as determinants for where a tic k was positioned within the vegetation. It is beyond the scope of this review to discuss off-host behavior, but the reader is referred to reports on Ixodes ricinus
84), A. (31a).
(54, 56), I. persulcatus (16a), Rhipicephalus appendiculatus (72-74, maculatum (18, 19), Dermacentor occidentalis (49), and D. variabilis
IXODID INTEGUMENT Physical Properties of the Cuticle
Ticks have a large surface-to-volume ratio and are prone to desiccation. One of the most important factors that has enabled arthropods in general to be the dominant terrestrial animal form is the ability of the integument to restrict
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water loss. This factor was essential for the transition of arthropods from an aquatic to a terrestrial existence
(27). Lipids associated with the epicuticle are
thought to form the primary barrier to water loss by most terrestrial arthropods and plants
(26). Other specialized integumental features restrict water loss
the spiracles of ixodid nymphs and adults (larvae have no spiracles) are covered by a spiracular plate and ventilation is regulated by a closing mech anism
(80). The oral cavity is formed dorsally by closely opposed paired
chelicerae, ventrally by the hypostome, and laterally by palpi that for many
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species partially enclose the dorso-ventral structures. This arrangement prob ably limits water loss from the mouth unless the palps are splayed. The anus is secured by valves. Hygroreceptors (setae) enable the tick to sense humidity gradients
(32). Only a few investigators beginning with Lees (52) have
studied tick integument. It is quite similar to insect integument, except the cement layer is apparently absent from the epicuticle of ixodids, making the unprotected lipid layer particularly susceptible to damage
(2, 17, 24, 25).
Whole-Body Permeability Integumental permeability, as shown by Lees (51), determines tick water-loss rates. Ticks held below the CEA die from desiccation very quickly if they are particularly permeable, while those that lose water slowly live quite some time by comparison (Table
1). Water-loss rates for ticks measured at 0 av are
actually whole-body permeability estimations that include water loss via the respiratory system, from oral and anal excretions, and any other physiological process that involves the loss of water
(66, 95; M. D . Sigal & G. R.
Needham, in preparation). Freda & Needham (20) suggest that these addition al avenues contribute proportionally much less than does integumentary loss, although an increase in locomotor activity can dramatically increase respira tory water loss
(79).
An understanding of certain principles is critical for studies that estimate the permeability of an organism. First, gravimetric values of permeability must be determined at near
0 avo This determination eliminates any contribu
tion of passive water to the water pool---otherwise permeability will be underestimated. That is not to say that experiments done in the presence of
(3 1 ) report that A. americanum 32% RH showed a difference in permeability, and they
atmospheric water are of no value. Hair et al and A. maculatum at
suggest that this played a key role in habitats each species could occupy. Recent studies demonstrated that A . americanum water-loss rates from the whole-body water pool increased with age
(M. D. Sigal & G. R. Needham, in (51, 52) that
preparation), which supports previous observations by Lees
ixodid CEAs increased with age. The greater rates of water loss probably raise water balance equilibrium thresholds in older ticks, resulting in CEAs at correspondingly higher relative avs.
OFF-HOST ECOLOGY OF TICKS
,,,fl1b
i].Hosl
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669
l
Tick (mesic)
Att;ve ,orption
�� Active sorption
Figure 1
(?)
Whole-body permeability (passive sorption and transpiration) and active-water vapor
uptake capability compared for three hypothetical adult ixodid tick species. Size of arrows indicates relative rate (large - fast. small - slow) of water movement. Limiting barrier represents integument: top figure is a tick that loses water slowly; the bottom figure is a leaky tick; and the middle panel represents a tick of intermediate integumental permeability. Internal eliptical shapes represent internal pools of different sizes from which water may be lost to the atmosphere . The top panel represents a tick that would survive in quite dry microhabitats and would move only occasionally to seek
a
higher humidity for rehydration; while the bottom panel
represents a tick that is leaky, has a small water pool, may not take water from the air actively (via mouth), and would survive only a few days at most in a dry microhabitat. The middle panel diagrams a tick that may have to move daily between microhabitats for rehydration and those where a host may be accessed. Figure provided by M. D. Sigal.
A fundamental question concerning the water-balance physiology of arthro pods including ticks is the amount of control they have over responding to changing ambient humidity conditions by altering integumental permeability (60, 6 1, 67-69). Integumental permeability control in ticks has not been adequately addressed. Short-term exposure ( 2 weeks) to low humidity did not appear to influence transpiration rates (20). Ticks respond to superficial abrasion by repairing damage (28, 52). As already mentioned, permeability increases with age as indicated by whole-body permeability measurements, but the reason for this increase is unknown. Deposition and removal of lipids also occur during engorgement and molting (14, 15, 28). Evidence for the transition in cuticle permeability from an engorging on-host tick to an en gorged off-host physiological condition emerges from several different stud ies (9, 81). The amount of extractable cuticular lipid per engorged female Boophilus micropius increased threefold over some nine days postdetachment (9), suggesting that the off-host individual is more protected from desiccation than one on the host. Engorged A. americanum females also seem more resistant to desiccation than unfed ticks (81). Alloscutal integument grows �
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Table 1
Comparison of water-balance and survival parameters which characterize adults of
five ixodid spec ie s'
1bree-hosl
speQcs
WhoIo-bodyb pcrmcabili!y (.., h-I)
newly� (mg)
0_2827±.0340 (10) 0.31S6±.0340 (10)
4.30±0.33 (16) 2.3S±O.IS (14)
0.1067±.OOO3 (10) 0.1064±.0004 (10)
� Mortality
