A phylogenetic approach to total evaporative water loss in mammals

Abstract Maintaining appropriate water balance is a constant challenge for terrestrial mammals, and this problem can be exacerbated in desiccating environments. It has been proposed that natural selection has provided desert-dwelling mammals physiological mechanisms to reduce rates of total evaporative water loss. In this study, we evaluated the relationship between total evaporative water loss and body mass in mammals by using a recent phylogenetic hypothesis. We compared total evaporative water loss in 80 species of arid-zone mammals to that in 56 species that inhabit mesic regions, ranging in size from 4 g to 3,500 kg, to test the hypothesis that mammals from arid environments have lower rates of total evaporative water loss than mammals from mesic environments once phylogeny is taken into account. We found that arid species had lower rates of total evaporative water loss than mesic species when using a dichotomous variable to describe habitat (arid or mesic). We also found that total evaporative water loss was negatively correlated with the average maximum and minimum environmental temperature as well as the maximum vapor pressure deficit of the environment. Annual precipitation and the variable Q (a measure of habitat aridity) were positively correlated with total evaporative water loss. These results support the hypothesis that desert-dwelling mammals have lower rates of total evaporative water loss than mesic species after controlling for body mass and evolutionary relatedness regardless of whether categorical or continuous variables are used to describe habitat.     

Participation of book lungs in evaporative water loss in Paraphysa parvula, a migalomorph spider from Chilean Andes

Small animals need efficient water conservation mechanisms for survival and reproduction, which is relevant for the spiders that have large book lungs with large respiratory surface. If lung evaporation is relevant to limit water loss, adjustments of the spiracle opening to metabolic demands should be expected. In this study, we measured the metabolic rate and total evaporative water loss mediated by the opening of the spiracles in the migalomorph spider Paraphysa parvula, a resident of fluctuating Mediterranean environments of the mountains of central Chile. We found that the metabolism of P. parvula was similar to other Theraphosidae and low compared to other arthropods. Carbon dioxide production and evaporative water loss increased with temperature, particularly at 40 °C. The total evaporative water loss at 40 °C increased dramatically to about 10 times that found with the lower temperatures. Thus, 40 °C will be the limit temperature for this species after which evaporative water loss starts to become damaging, so it has to avoid it. The exposition to hypercapnic environments had as a consequence an increase in evaporative water loss and the involvement of the book lungs in this loss was about 60%. The possibility of losing water could condition this species to seek temperate and oxygenated shelters under rocks.     

Is the evaporative water loss of Knot Calidris canutus higher in tropical than in temperate climates?

To test whether Knot Calidris canutus wintering in the tropics suffer higher rates of water loss through evaporation than do Knot wintering at temperate latitudes, we tried to develop a physically realistic model to predict evaporative heat loss from air temperature, wind and humidity. In separate experiments, involving respirometry and double-labelled water, we tried to estimate relevant parameters. In both sets of experiments, we were able to show significant effects of air temperature on evaporative water loss only. Knot which were able to eat and drink had an evaporative water loss three times that of postabsorptive Knot unable to drink when in a metabolic chamber. Water turnover rates of Knot feeding on bivalves under simulated field conditions were high and did not correlate with predicted evaporative water loss. Over 32 experimental bird-days, the average contribution of predicted evaporative water loss to daily water turnover was 20%. A comparison of predicted evaporative water loss in the north-temperate Dutch Wadden Sea and in the tropical Banc d'Arguin in Mauritania in midwinter showed that Knot wintering in the tropics may need only marginally more water for evaporative cooling than Knot wintering in the Dutch Wadden Sea. Knot foraging on intertidal invertebrates are able to maintain high water turnover rates with little need to drink seawater.     

Aquaporins,evaporative water loss and thermoregulation in heat-acclimated Mongolian gerbils (Meriones unguiculatus)

Evaporative water loss is an essential strategy to maintain stable body temperature in heat-exposed rodents. However, the thermoregulatory role and adjustment of evaporative heat loss capacity is unclear during prolonged heat exposure. Here, we studied the role of evaporative water loss in thermoregulation in Mongolian gerbils during heat acclimation. After 3 weeks of heat acclimation, gerbils exhibited a lower body temperature than the controls, and no difference in evaporative losses of water from the lung or saliva spreading compared with the controls. Heat acclimation did not alter the expression of aquaporin-1 and aquaporin-5 in the lungs and the expression of aquaporin-5 in the salivary glands. The expression of aquaporin-2 in the kidneys was kept stable, while the expression of aquaporin-1 in the kidneys was down-regulated. In addition, resting metabolic rate and non-shivering thermogenesis of heat-acclimated gerbils were reduced to 51% and 55% of the control group, respectively. Taken together, heat-acclimated Mongolian gerbils can reduce the metabolic thermogenesis without enhancing the evaporative water loss capacity for thermoregulation.     

The thermal and energetic significance of clustering in the speckled mousebird,Colius striatus

Summary The effect of clustering behaviour on metabolism, body temperature, thermal conductance and evaporative water loss was investigated in speckled mousebirds at temperatures between 5 and 36°C. Within the thermal neutral zone (approximately 30–35 °C) basal metabolic rate of clusters of two birds (32.5 J·g^-1·h^-1) and four birds (28.5 J·g^-1·h^-1) was significantly lower by about 11% and 22%, respectively, than that of individuals (36.4 J·g^-1·h^-1). Similarly, below the lower critical temperature, the metabolism of clusters of two and four birds was about 14% and 31% lower, respectively, than for individual birds as a result of significantly lower total thermal conductance in clustered birds. Body temperature ranged from about 36 to 41°C and was positively correlated with ambient temperature in both individuals and clusters, but was less variable in clusters. Total evaporative water loss was similar in individuals and clusters and averaged 5–6% of body weight per day below 30°C in individuals and below 25°C in clusters. Above these temperatures total evaporative water loss increased and mousebirds could dissipate between 80 and 90% of their metabolic heat production at ambient temperatures between 36 and 39°C. Mousebirds not only clustered to sleep between sunset and sunrise but were also observed to cluster during the day, even at high ambient temperature. Whereas clustering at night and during cold, wet weather serves a thermoregulatory function, in that it allows the brrds to maintain body temperature at a reduced metabolic cost, clustering during the day is probably related to maintenance of social bonds within the flock.Abbreviations BMR basal metabolic rate - bw body weight - C _totab total thermal conductance - EWI evaporative water loss - M metabolism - RH relative humidity - T _a ambient temperature - T _b body temperature - T _ch chamber temperature - T _cl cluster temperature - TEWL total evaporative water loss - LCT lower critical temperature - TNZ thermal neutral zone     

Measurement of fractionated water loss and CO2 production using triply labelled water

The doubly labelled water (DLW) method for measuring CO2 production has recently been the subject of much interest since no other technique gives integrated values for CO2 production over long periods by free-living subjects. The importance of evaporative water loss and fractionation factors to the calculation of CO2 production using this technique is described. Present methods of estimating evaporative water loss and the use of fractionation factors are summarized together with a discussion of their limitations. A novel technique is proposed whereby water labelled with three isotopes can be used to measure evaporative water loss and CO2 production in completely free-living subjects, and the feasibility of the method is tested in simulations using experimental data. This technique has three advantages over existing methods of estimating evaporative water loss: (1) it can be used in completely free-living subjects without any additional experimental procedures (e.g. water-balance studies or physical trapping of water vapour); (2) it gives a direct estimate of fractionated evaporative water loss in each subject, since non-fractionated water lost as vapour is automatically compensated for; and (3) the routes of water loss do not have to be known. The appropriate calculations are presented together with a discussion of the difficulties of measuring oxygen-17 by mass spectrometry. It is estimated that the maximum theoretical error on calculated CO2 production is +/- 0.3%. Practical ways of achieving this theoretical level of accuracy are suggested. We conclude that the proposed technique will allow correction for evaporative water loss to be made more exactly, thereby increasing the accuracy of the heavy water technique for measuring CO2 production in free-living subjects.     

Evaporative and excretory water loss during free flight in pigeons

Body water conservation is important in flying birds because the very high metabolic demands and heat dissipation requirements during flight depend on plasma-volume integrity. Wind tunnel experiments and theoretical model predictions show that evaporative water loss (EWL) depends on air temperature (T _a) and water vapor density (ρ_a), but these relationships have not been examined in free-flying birds. The contribution of excretory water loss to the total water loss of a flying bird is thought to be negligible but this assumption is untested. To study the dependence of water losses on environmental conditions in free-flying birds and to quantify the contribution of excretory water loss to total water loss, we estimated evaporative and excretory water losses in 16 trained, free-flying tippler pigeons (Columba livia, 250–340 g). We collected excreta by attaching a light latex, water-impermeable receptacle around each bird's vent. By gravimetry, we measured evaporative and excretory water losses of birds for eight flights at different T _as and compared flying to resting (control) birds for two of these flights. EWL was constant with respect to T _a when less than 15 °C, and increased with increasing T _a above 19 °C, indicating that evaporative cooling was invoked when the heat load increased. EWL increased with increasing ρ_a, possibly due to the strong correlation between ρ_a and T _a. Excretory water loss was independent of ρ_a or T _a and averaged almost 10% of the total water loss. Measurements of EWL made on pigeons during wind tunnel experiments and previous free-flight studies are consistent with our free-flight measurements made at similar T _a s. Accepted: 13 April 1999     

Comparative water economy of sympatric rodents in a Chilean semi-arid habitat

1. Water requirements, water balance components and dependence on exogenous water were estimated in four species of sympatric rodents inhabiting a Chilean semi-arid region. 2. A significant increase in free water drinking was observed in all rodents when the diet composition was changed from 14 to 20% protein. 3. Under water balance conditions the cricetid species (Phyllotis darwini, Oryzomys longicaudatus and Akodon olivaceus) showed 1.66 to 1.88 times the weight-specific daily water gain of Octodon degus. 4. In the three cricetid rodents, evaporation was the largest water loss component (2/3 to 3/4 of total loss), while in O. degus evaporative water loss amounted to only 38% of the total. 5. Survival time during water deprivation ranged from 13.4 days in O. degus to only 4 days in O. longicaudatus. 6. All water variables combined indicate that water dependence of O. longicaudatus greater than P. darwini greater than A. olivaceus greater than O. degus.     

The adjustment of avian metabolic rates and water fluxes to desert environments

We tested the hypothesis that birds in arid environments, where primary productivity is low and surface water is scarce, have reduced energy expenditure and water loss compared with their mesic counterparts. Using both conventional least squares regression and regression based on phylogenetically independent contrasts, we showed that birds from desert habitats have reduced basal and field metabolic rates compared with species from mesic areas. Previous work showed that desert birds have reduced rates of total evaporative water loss when exposed to moderate environmental temperatures in the laboratory. We tested whether reduced rates of total evaporative water loss translate into low field water fluxes. Conventional ANCOVA indicated that desert birds have reduced water fluxes, but an analysis based on phylogenetically independent contrasts did not support this finding, despite the wide array of taxonomic affiliations of species in the data set. We conclude that the high ambient temperatures, the low primary productivity, and the water scarcity in desert environments have selected for or resulted in reduced rates of energy expenditure and evaporative water loss in birds that live in these climes.     

Respiratory evaporative water loss during hovering and forward flight in hummingbirds

Hummingbirds represent an end point for small body size and water flux in vertebrates. We explored the role evaporative water loss (EWL) plays in management of their large water pool and its use in dissipating metabolic heat. We measured respiratory evaporative water loss (REWL) in hovering hummingbirds in the field (6 species) and over a range of speeds in a wind tunnel (1 species) using an open-circuit mask respirometry system. Hovering REWL during the active period was positively correlated with operative temperature (T_e) likely due to some combination of an increase in the vapor-pressure deficit, increase in lung ventilation rate, and reduced importance of dry heat transfer at higher T_e. In rufous hummingbirds (Selasphorus rufus; 3.3 g) REWL during forward flight at 6 and 10 m/s was less than half the value for hovering. The proportion of total dissipated heat (TDH) accounted for by REWL during hovering at T_e > 40 °C was < 40% in most species. During forward flight in S. rufus the proportion of TDH accounted for by REWL was ~ 35% less than for hovering. REWL in hummingbirds is a relatively small component of the water budget compared with other bird species (< 20%) so cutaneous evaporative water loss and dry heat transfer must contribute significantly to thermal balance in hummingbirds.     

Correlation of both respiratory and cutaneous water losses of lizards with habitat aridity

Summary Respiratory and cutaneous evaporative water losses were measured in dried air from 5 xantusiid lizard species to determine whether adaptations for water conservation were present in one or both components. These species represent the range of arid to mesic habitats occupied by the Xantusiidae. The respiratory proportion of evaporative water loss ranged from 20–50% and did not show consistent patterns of temperature dependence or interspecific differences. However, respiratory water loss expressed as mg H₂O per ml O₂ consumed and cutaneous water loss (mg H₂O· cm^–2·h^–1) exibited parallel correspondence to habitat aridity. Adaptations for reducing water loss from the skin involved an increased skin resistance to water flux while reduction of respiratory water loss was probably the result of reduced convection requirements for respiratory gas exchange.Abbreviations EWL evaporative water loss - RWL respiratory water loss - CWL cutaneous water loss     

Validation of the doubly labeled water method under low and high humidity to estimate metabolic rate and water flux in a tropical snake (Boiga irregularis).

This study uses indirect calorimetry to assess the effects of humidity on the accuracy of the doubly labeled water (DLW) technique to predict metabolic rate and water flux in brown treesnakes (Boiga irregularis). The DLW technique accurately predicted total water efflux in brown treesnakes under low-humidity conditions and found that the total number of water molecules exchanged with the environment under humid conditions was not significantly different than maximum net total evaporative water loss under low humidity conditions plus fecal water loss. Because of changes of total body water of >12%, the DLW technique overestimated metabolic rate by a factor of 2.2 under low-humidity conditions. Under high-humidity conditions, the DLW technique overestimated metabolic rate in brown treesnakes by a factor of 4.6. Researchers using the DLW technique in humid or moist environments should be cautious because this study indicates that DLW estimates of metabolic rate may be inflated when large amounts of water vapor are exchanged through the skin or respiratory passages.     

Behavioral thermoregulation of the toad, Bufo marinus: effects of air humidity

Two experiments were performed. The first tested the hypothesis that the toad, Bufo marinus, will select a lower ambient temperature under dry environmental conditions. This behavioral response would reduce evaporative water loss and facilitate survival on land. The second experiment measured the effects of temperature on evaporative water loss. In the first experiment, toads were placed in a thermal gradient (11-40 degrees C) for 3 days. On days 1 and 3, water-filled dishes were placed along the temperature gradient and humid air was circulated through the chamber. On day 2, water dishes were removed, and dry air was circulated through the chamber. Body temperature (Tb) was recorded with a cloacal thermistor. Selected Tb was approximately 8.6 degrees C lower during the dry conditions than during the humid conditions. The behavioral hypothermia took about 6 h to develop. In the second experiment, a reduction in Tb from 17.7 to 12 degrees C reduced evaporative water loss by 42%. Consequently, behavioral hypothermia of the toad is an important adaptation to dry environmental conditions.     

Evaporative water loss in seven species of fossorial rodents: Does effect of degree of fossoriality and sociality exist?

In terrestrial endotherms, evaporation is a significant mechanism of water loss in hot environments. Although water is passively lost by evaporation, individuals can regulate it at different levels. Inhabiting a relatively stable environment characterized by mild ambient temperature (T_a) and high humidity can ensure a balanced water budget. Many fossorial rodents are well adapted to live in such conditions. In this study, evaporative water loss (EWL) of fossorial rodent species with different degree of adaptations to underground life (from strictly subterranean to those with regular surface activity) was evaluated. By measuring EWL, the specific contribution of either evaporative or non-evaporative components of heat loss can be determined. With the exception of the silvery mole-rat (Heliophobius argenteocinereus), in all tested rodents EWL is relatively stable below and within the thermoneutral zone (TNZ). As T_as increase above TNZ, EWL increases as does total thermal conductance, but conductance increases several times more than EWL. In addition, non-evaporative routes seem to be more important than evaporative heat loss in the analyzed species. No clear pattern of EWL in relation to a species degree of fossoriality or sociality was detected. In this context, atmosphere of burrows could affect EWL, since the high humidity found inside tunnels can establish limits on evaporation to favor water rather than thermal balance.     

Experimental determination of coefficient of evaporative heat loss in still air (author's transl)]

The authors have determined the coefficient of evaporative heat loss of the human body (he) by means of humidity steps in low air movement (Va less than or equal to 0,2 m/s). Such a determination requires a fully wetted skin and this implies therefore some loss of dripping sweat. The collection of this dripping sweat allows the determination of the total evaporation: this evaporation exists on the skin surface and around the drops during their fall from the skin to the oil pan where dripping sweat is collected. An estimation of this dripping sweat evaporation allows to assess the skin evaporation and, consequently, the evaporative coefficient he. In these experimental conditions: E = S - SNE - 0,0005 SNE (PsH2O - PaH2O) where E is the skin evaporative rate (g/h);S = total sweat rate (g/h);SNE = the nonevaporative sweat rate (g/h);PaH2O = the partial pressure of saturated water (at Ts) on skin (mb) and PaH2O the partial pressure of water vapor in ambient air (mb). The coefficient of evaporative heat loss in low air movement thus found, is 5,18 +/- 0,22 W/m2-mb.     

Validation of the doubly labeled water method in growing precocial birds: the importance of assumptions concerning evaporative water loss

The doubly labeled water (DLW) method was validated against respiration gas analysis in growing precocial chicks of the black-tailed godwit (Limosa limosa) and the northern lapwing (Vanellus vanellus). To calculate the rate of CO2 production from DLW measurements, Lifson and McClintock's equations (6) and (35) were employed, as well as Speakman's equation (7.17) (all single-pool models). The average errors obtained with the first two equations (+7.2% and -11.6%, respectively) differed significantly from zero but not the error obtained with Speakman's equation (average: -2.9%). The latter error could be reduced by taking a fractional evaporative water loss of 0.13, instead of the value of 0. 25 recommended by Speakman. Application of different two-pool models resulted in relative errors of the DLW method of -15.9% or more. After employing the single-pool model with a fractional evaporative water loss value of 0.13, it was found that there was no relationship between the relative growth rate of the chick and the relative error of the DLW method. Recalculation of previously published results on Arctic tern (Sterna paradisaea) chicks revealed that the fit of the validation experiment could be considerably improved by employing a single-pool model and assuming a fractional evaporative water loss of 0.20 instead of the value of 0.50 taken originally. After employing the value of 0.20, it was found that there was no relationship between the relative growth rate of the chick and the relative error of the DLW method. This suggests that isotope incorporation into new body substances does not cause a detectable error. Thus, the DLW method seems to be applicable in young birds growing as fast as 20% d-1, after making adjustments for the fractional evaporative water loss. We recommend Speakman's equation (7.17) for general use in growing birds when evaporation is unknown.     

Water and heat balance during flight in the rose-colored starling (Sturnus roseus)

Water imbalance during flight is considered to be a potentially limiting factor for flight ranges in migrating birds, but empirical data are scarce. We studied flights under controlled ambient conditions with rose-colored starlings in a wind tunnel. In one experiment, we measured water fluxes with stable isotopes at a range of flight speeds (9-14 m s(-1)) at constant temperature (15 degrees C). In a second experiment, we measured evaporation rates at variable ambient temperatures (Ta = 5 deg -27 deg C) but constant speed (12 m s(-1)). During all flights, the birds experienced a net water loss. On average, water influx was 0.98 g h(-1) (SD = 0.16; n = 8), and water efflux was 1.29 g h(-1) (SD = 0.14; n = 8), irrespective of flight speed. Evaporation was related to temperature in a biphasic pattern. At temperatures below 18.2 degrees C, net evaporation was constant at 0.36 g h(-1) (SD = 0.18; n = 10), rising at higher temperatures with a slope of 0.11 per degree to about 1.5 g h(-1) at 27 degrees C. We calculated the relative proportion of dry and evaporative heat loss during flight. Evaporative heat loss at Ta < 18.2 deg C was 14% of total heat production during flight, and dry heat loss accounted for 84%. At higher temperatures, evaporative heat loss increased linearly with T(a) to about 25% at 27 degrees C. Our data suggest that for prolonged flights, rose-colored starlings should adopt behavioral water-saving strategies and that they cannot complete their annual migration without stopovers to replenish their water reserves.     

Temperature regulation and basal metabolic rate in the spotted skunk, Spilogale putorius

1. Metabolic rate, body temperature, and evaporative water loss of six spotted skunks were measured at air temperatures between 8 and 40 degrees C. 2. The mean metabolic rate of spotted skunks at thermoneutral air temperatures was 30.5% below that predicted by body mass. 3. Thermal conductance, body temperature, and rates of evaporative water loss were like those of similar sized mammals. 4. The non-elongate body form, omnivorous diet, and low level of activity of spotted skunks distinguish them from other mustelids and may account for their lower-than-expected basal metabolism.     

Water relations of the tos1 tomato mutant at contrasting evaporative demand

The tos1 (tomato osmotically sensitive) mutant, isolated from an in vitro screen of root growth during osmotic stress, was less sensitive to exogenous ABA, but accumulated more ABA under osmotic stress than WT plants. We assessed growth and water relations characteristics of hydroponically grown tos1 seedlings (in the absence of osmotic stress) at low and high evaporative demands. Growth of tos1 was severely inhibited at both high and low evaporative demands. Twenty DAS, WT and tos1 genotypes had a similar leaf water and turgor potential, but mature tos1 plants (45 day old) showed a significant diurnal loss of leaf turgor, with recovery overnight. Increased evaporative demand increased turgor loss of tos1 plants. High evaporative demand at the beginning of the day decreased stomatal conductance of tos1, without diurnal recovery, thus whole plant transpiration was decreased. De-topped tos1 seedlings showed decreased root hydraulic conductance and had a 1.4-fold increase in root ABA concentration. Impaired root function of tos1 plants failed to meet transpirational water demand and resulted in shoot turgor loss, stomatal closure and growth inhibition.     

Cocoon and epidermis of Australian Cyclorana frogs differ in composition of lipid classes that affect water loss

For amphibians to survive in environments that experience annual droughts, they must minimize evaporative water loss. One genus of Australian hylid frogs, Cyclorana, prevents desiccation by burrowing in the soil and forming cocoons composed of alternating layers of shed epidermis and glandular secretions. Previous data are inconclusive about the role that lipids play in reducing evaporative water loss through skin (cutaneous water loss [CWL]) when Cyclorana spp. are within cocoons. In this study, we measured CWL and lipids in the epidermis and in cocoons of five species of Cyclorana. CWL was significantly lower in frogs within cocoons than in frogs without cocoons. Surface-area-specific CWL for the three small species was significantly higher than that of the two larger species of Cyclorana, but this difference was not apparent in frogs within cocoons. Although lipids were responsible for more of the dry mass of the epidermis (approximately 20%) than of the cocoons (approximately 7%) we found that cerebrosides and ceramides, two polar lipid classes, were almost exclusively found in cocoons. This suggests that these lipid classes are in the glandular secretions rather than in the epidermis. Because these polar lipids are the types that reduce water loss in birds (cerebrosides and ceramides) and mammals (ceramides), we conclude that they are important not only for holding together the shed layers of skin but also for contributing to the barrier against water loss.