Biophysical properties of the pelt of a diurnal marsupial, the numbat (Myrmecobius fasciatus), and its role in thermoregulation.

Numbats are unusual marsupials in being exclusively diurnal and termitivorous. They have a sparse (1921 hairs cm(-2)) and shallow (1.19 mm) pelt compared with other marsupials. Coat reflectivity is low (19%) for numbats compared with nocturnal marsupials, but absorptivity is similar to that of diurnal North American ground squirrels (72%), indicating that the coat of the numbat may be adapted for acquisition of solar heat. Numbat coat thermal resistance decreases significantly with wind speed from 45.9 s m(-1) (at 0.5 m s(-1)) to 29.8 s m(-1) (at 3 m s(-1)). Erecting the fur significantly increases pelt depth (6.5 mm) and coat resistance (79.2-64.2 s m(-1)) at wind speeds between 0.5 m s(-1) and 3 m s(-1). Numbat coat resistance is much lower than that of other marsupials, and wind speed has a greater influence on coat resistance for numbats than for other mammals, reflecting the low pelt density and thickness. Solar heat gain by numbats through the pelt to the level of the skin (60-63%) is similar to the highest value measured for any mammal. However the numbat's high solar heat gain is not associated with the same degree of reduction in coat resistance as seen for other mammals, suggesting that its pelt has structural and spectral characteristics that enhance both solar heat acquisition and endogenous heat conservation. Maximum solar heat gain is estimated to be 0.5-3.6 times resting metabolic heat production for the numbat at ambient temperatures of 15-32.5 degrees C, so radiative heat gain is probably an important aspect of thermoregulation for wild numbats.

Absence of aquaporin-4 water channels from kidneys of the desert rodent Dipodomys merriami merriami.

Recently, we found that aquaporin-4 (AQP4) is expressed in the S3 segment of renal proximal tubules of mice but not in rat proximal tubules. Because mice have relatively larger papillae than rats, it was proposed that the renal distribution of AQP4 in various species could be related to their maximum urinary concentrating ability. Therefore, kidneys and other tissues of Merriam's desert kangaroo rat, Dipodomys merriami merriami, which produce extremely concentrated urine (up to 5,000 mosmol/kgH(2)O), were examined for AQP4 expression and localization. Contrary to our expectation, AQP4 immunostaining was undetectable in any region of the kidney, and the absence of AQP4 protein was confirmed by Western blotting. By freeze fracture electron microscopy, orthogonal arrays of intramembraneous particles (OAPs) were not detectable in plasma membranes of principal cells and proximal tubules. However, AQP4 protein was readily detectable in gastric parietal and brain astroglial cells. Northern blotting failed to detect AQP4 mRNA in kangaroo rat kidneys, whereas both in situ hybridization and RT-PCR experiments did reveal AQP4 mRNA in collecting ducts and proximal tubules of the S3 segment. These results suggest that renal expression of AQP4 in the kangaroo rat kidney is regulated at the transcriptional or translational level, and the absence of AQP4 may be critical for the extreme urinary concentration that occurs in this species.

Developmental and acclimatory contributions to water loss in a desert rodent: investigating the time course of adaptive change.

Understanding the evolution of physiological traits requires considering three nonexclusive mechanisms that underlie phenotypes and cause their change over different time scales: acclimation, developmental plasticity, and natural selection for genetically fixed traits. Physiological adjustments to changes in the desiccating potential of the environment were investigated with one subspecies of common desert rodent, Dipodomys merriami merriami (Merriam's kangaroo rat). We raised young whose parents originated from environments that differ in both temperature and humidity. These young were raised under either desiccating or water-abundant conditions, and their water loss was measured at a series of temperatures to determine the effect developmental conditions have on resistance to desiccation. We then determined the contribution of acclimation to desiccation resistance by keeping the differentially raised young in conditions opposite to those during their development and again measuring water loss. We found that developmental plasticity and acclimation can completely account for the existing intraspecific variability in desiccation resistance under certain conditions. In fact, developmental and acclimatory changes can equal genetically based differences of the populations. This phenotypic plasticity can operate relatively quickly and therefore may attenuate the actions of natural selection. Understanding the extent and nature of such flexibility is critical to our understanding intraspecific variability and the consequences of changing climate.

Unappreciated tolerance to high ambient temperatures in a widely distributed desert rodent, Dipodomys merriami.

A long-held assertion has been that nocturnality is an escape mechanism for many nocturnal desert rodents because of limited tolerances to heat. To test this claim, we used a treadmill to examine the tolerances to high ambient temperatures (T(a)'s) of one subspecies of desert rodent, Merriam's kangaroo rat, Dipodomys merriami merriami, from contrasting environments. We simultaneously measured body temperature (T(b)), evaporative water loss, and metabolic rates at an ecologically relevant speed (0.6 km h(-1)) at different ambient temperatures (Ta=25 degrees -42.5 degrees C). We hypothesized that kangaroo rats from a more xeric site would have greater abilities to remain active and maintain stable T(b) than those from a more mesic site, but mesic- and xeric-site animals had comparable tolerances and were active until Tb=42 degrees C. At Ta=42.5 degrees C, however, T(b) of mesic-site animals increased more quickly than in xeric-site animals. Although most animals could not run more than 18 min at Ta=42.5 degrees C, most could run at Ta=40 degrees C for at least 30 min. Benefits of nocturnality for this species may reside more in purposes of water conservation and avoidance of predation and less on the direct regulation of T(b), as T(b) is more labile than commonly thought.

Effect of wind and solar radiation on metabolic heat production in a small desert rodent, Spermophilus tereticaudus.

To understand better how complex interactions between environmental variables affect the energy balance of small diurnal animals, we studied the effects of the absence and presence of 950 W m(-)(2) simulated solar radiation combined with wind speeds ranging from 0. 25 to 1.00 m s(-)(1) on the metabolic rate and body temperature of the round-tailed ground squirrel Spermophilus tereticaudus. As wind speed increased from 0.25 to 1.00 m s(-)(1), metabolic heat production increased by 0.94 W in the absence of solar radiation and by 0.98 W in the presence of 950 W m(-)(2) simulated solar radiation. Exposure to simulated solar radiation reduced metabolic heat production by 0.68 W at a wind speed of 0.25 m s(-)(1), by 0.64 W at 0.50 m s(-)(1) and by 0.64 W at 1.00 m s(-)(1). Body temperature was significantly affected by environmental conditions, ranging from 32. 5 degrees C at a wind speed of 1.0 m s(-)(1) and no irradiance to 35. 6 degrees C at a wind speed of 0.50 m s(-)(1) with 950 W m(-)(2 )short-wave irradiance. In addition, several unusual findings resulted from this study. The coat of S. tereticaudus is very sparse, and the observed heat transfer of 5.68+/-0.37 W m(-)(2 ) degrees C(-)(1) (mean +/- s.e.m., N=11) is much higher than expected from either allometric equations or comparative studies with other rodents of similar mass. Solar heat gain was remarkably low, equalling only 10 % of intercepted radiation and suggesting a remarkably high regional thermal resistance at the tissue level. Animals remained normally active and alert at body temperatures as low as 32.5 degrees C. These findings suggest a unique combination of adaptations that allow S. tereticaudus to exploit a harsh desert environment.

Prevalence of cutaneous evaporation in Merriam's kangaroo rat and its adaptive variation at the subspecific level.

Previous estimates suggested that ventilatory evaporation constitutes the major source of water loss in kangaroo rats (Dipodomys spp.). We quantified rates of water loss in Merriam's kangaroo rat (Dipodomys merriami) and demonstrate the degree to which acclimation to a particular thermal and hydric environment plays a role in the intraspecific variation in water loss evident in this species. We draw the following conclusions: (1) that water loss varies intraspecifically in Merriam's kangaroo rat, in association with habitats of contrasting aridity and temperature; (2) that animals from more xeric locations have lower water loss rates than those from more mesic sites; (3) that most water loss is cutaneous, with ventilatory evaporative water loss contributing, at most, only 44% to total evaporative water loss; and (4) that intraspecific differences in rates of water loss are not acclimatory, but fixed. After acclimating under the same conditions, xeric-site animals still show a 33% lower rate of evaporative water loss than mesic-site animals.

Effects of complex radiative and convective environments on the thermal biology of the white-crowned sparrow (Zonotrichia leucophrys gambelii).

The energy budgets of small endotherms are profoundly affected by characteristics of the physical environment such as wind speed, air temperature and solar radiation. Among these, solar radiation represents a potentially very large heat load to small animals and may have an important influence on their thermoregulatory metabolism and heat balance. In this investigation, we examined the interactive effects of wind speed and irradiance on body temperature, thermoregulatory metabolism and heat balance in the white-crowned sparrow (Zonotrichia leucophrys gambelii). We measured changes in metabolic heat production by exposing birds to different wind speeds (0.25, 0.5, 1.0 and 2.0 m s(-1)) and irradiance combinations (<3 W m(-2) and 936+/-11 W m(-2); mean +/- s.d.) at an air temperature of 10 degrees C. Body temperature was not affected by wind speed, but was significantly higher in animals not exposed to simulated solar radiation compared with those exposed at most wind speeds. In the absence of solar radiation, metabolic heat production was strongly affected by wind speed and increased by 30 % from 122 to 159 W m(-2) as wind speed increased from 0.25 to 2.0 m s(-1). Metabolic heat production was even more strongly influenced by wind speed in the presence of simulated solar radiation and increased by 51% from 94 to 142 W m(-2) as wind speed increased from 0.25 to 2. 0 m s(-1). Solar heat gain was negatively correlated with wind speed and declined from 28 to 12 W m(-2) as wind speed increased from 0.25 to 2.0 m s(-1) and, at its maximum, equaled 11% of the radiation intercepted by the animal. The overall thermal impact of the various wind speed and irradiance combinations on the animal's heat balance was examined for each treatment. Under cold conditions, with no solar radiation present, an increase in wind speed from 0.25 to 2.0 m s(-1) was equivalent to a decrease in chamber air temperature of 12.7 degrees C. With simulated solar radiation present, a similar increase in wind speed was equivalent to a decrease in chamber air temperature of 16 degrees C. Overall, shifting environmental conditions from a wind speed of 0.25 m s(-1) and irradiance of 936 W m(-2) to a wind speed of 2.0 m s(-1) with no short-wave radiation present was equivalent to decreasing chamber air temperature by approximately 20 degrees C. The sensitivity to changes in the convective environment, combined with the complex effects of changes in irradiance levels revealed by re-analyzing data published previously, significantly complicates the task of estimating the heat balance of animals in nature.

Do metabolic responses to solar radiation scale directly with intensity of irradiance?

Endotherms exposed to air temperatures below thermal neutrality reduce their metabolic heat production when exposed to sunlight. The physiological effects of this additional source of heat gain from the environment usually are assumed to be proportional to the intensity of irradiance if other factors are held constant. We test this assumption by measuring changes in metabolic heat production produced by exposing a small mammal, the Siberian hamster (Phodopus sungorus) to four intensities of simulated solar radiation (0 W m-2, 317 W m-2, 634 W m-2 and 950 W m-2). In the absence of solar radiation, metabolic heat production is inversely correlated with air temperature over the measured range of 3-27 degrees C. The respiratory quotient varies significantly with ambient temperature, indicating that the catabolic substrate and the thermal equivalent of oxygen consumed or carbon dioxide produced also vary with temperature. The depression of metabolic heat production resulting from exposure to simulated solar radiation is not simply a multiple of the intensity of irradiance. Rather, metabolic responses to higher levels of irradiance are blunted by 14-29% compared with those expected on the basis of the response to less intense irradiance. Because changes in irradiance levels do not have simple linear effects upon the animal's metabolic heat production, even in a simplified situation, significant errors may accumulate in biophysical analyses in which an animal's responses to a restricted set of radiative conditions are measured and the results are extrapolated to a wider range observed in nature.

Seasonal adjustment of solar heat gain independent of coat coloration in a desert mammal.

Despite the apparent importance of solar radiation as a source of heat for free-living animals, there exists no substantial body of empirical data describing physiological responses to solar radiation under the range of convective conditions likely to occur in nature. We therefore quantified effects of simulated solar radiation and wind on metabolic heat production in the rock squirrel, Spermophilus variegatus. This diurnal mammal inhabits the Sonoran Desert and seasonally replaces its pelage in a fashion in which it retains constant external appearance but incorporates optical and structural changes that are thought to significantly alter heat-transfer properties of the coat. At a given wind speed, the presence of 950 W m-2 of simulated solar radiation reduces metabolic heat production by 15% (at a wind speed of 4 m s-1) to 37% (at a wind speed of 0.25 m s-1). Independent of effects of irradiance, metabolic heat production significantly increases with wind speed such that as wind speed is increased from 0.25 m s-1 to 4.0 m s-1, metabolic heat production is elevated by 66% (sunlight absent) or 88% (sunlight present). Previous analyses demonstrated that when exposed to identical radiative and convective environments rock squirrels with summer pelages accrue solar heat loads 33%-71% lower than those experienced by animals with winter coats. This reduction of solar heat gain during the extremely hot Sonoran Desert summer apparently constitutes a previously unappreciated mode of thermal adaptation by seasonal adjustment of radiative heat gain without changes in the animal's appearance.

Effects of solar radiation and wind speed on metabolic heat production by two mammals with contrasting coat colours.

We report the first empirical data describing the interactive effects of simultaneous changes in irradiance and convection on energy expenditure by live mammals. Whole-animal rates of solar heat gain and convective heat loss were measured for representatives of two ground squirrel species, Spermophilus lateralis and Spermophilus saturatus, that contrast in coloration. Radiative heat gain was quantified as the decrease in metabolic heat production caused by the animal's exposure to simulated solar radiation. Changes in convective heat loss were quantified as the variation in metabolic heat production caused by changes in wind speed. For both species, exposure to 780 W m-2 of simulated solar radiation significantly reduced metabolic heat production at all wind speeds measured. Reductions were greatest at lower wind speeds, reaching 42% in S. lateralis and 29% in S. saturatus. Solar heat gain, expressed per unit body surface area, did not differ significantly between the two species. This heat gain equalled 14-21% of the radiant energy intercepted by S. lateralis and 18-22% of that intercepted by S. saturatus. Body resistance, an index of animal insulation, declined by only 10% in S. saturatus and 13% in S. lateralis as wind speed increased from 0.5 to 4.0 ms-1. These data demonstrate that solar heat gain can be essentially constant, despite marked differences in animal coloration, and that variable exposure to wind and sunlight can have important consequences for both thermoregulatory stress experienced by animals and their patterns of energy allocation.

Solar heat gain in a desert rodent: unexpected increases with wind speed and implications for estimating the heat balance of free-living animals.

We quantified metabolic power consumption as a function of wind speed in the presence and absence of simulated solar radiation in rock squirrels, Spermophilus variegatus, a diurnal rodent inhabiting arid regions of Mexico and the western United States. In the absence of solar radiation, metabolic rate increased 2.2-fold as wind speed increased from 0.25 to 4.0m.s-1. Whole-body thermal resistance declined 56% as wind speed increased over this range, indicating that body insulation in this species is much more sensitive to wind disruption than in other mammals. In the presence of 950W.m-2 simulated solar radiation, metabolic rate increased 2.3-fold as wind speed was elevated from 0.25 to 4.0m.s-1. Solar heat gain, calculated as the reduction in metabolic heat production associated with the addition of solar radiation, increased with wind speed from 1.26mW.g-1 at 0.25m.s-1 to 2.92mW.g-1 at 4.0m.s-1. This increase is opposite to theoretical expectations. Both the unexpected increase in solar heat gain at elevated wind speeds and the large-scale reduction of coat insulation suggests that assumptions often used in heat-transfer analyses of animals can produce important errors.

The significance of fur structure for solar heat gain in the rock squirrel, Spermophilus variegatus.

The coats of birds and mammals typically vary through their depth in structure, insulation and optical qualities. Physical models predict that such variation can substantially affect the solar heat load acquired by an animal. This study quantifies the consequences of complex coat structure for solar heat gain in the rock squirrel (Spermophilus variegatus (Erxleben, 1777)), a species normally exposed to intense solar radiation. This species' pelage consists of two well-defined layers: a dense inner coat of fine, dark hairs, and a sparse outer coat of coarse, light hairs. The optics, structure and thermal insulation of the inner and outer coats are quantified and used to predict rates of radiative heat gain using a physical model. The radiative heat load measured at the skin compares well with model predictions. The validated model is then used to explore the consequences for solar heat gain of varying the relative proportions of the inner and outer coat layers. Results demonstrate that the ratio of inner to outer coat depths occurring in rock squirrels is very near that theoretically predicted to minimize solar heat gain. This indicates that optimization of fur structure may represent an effective means of adjusting solar heat gain independent of coat insulation and surface coloration.

Consequences of skin color and fur properties for solar heat gain and ultraviolet irradiance in two mammals.

In animals with fur or feather coats, heat gain from solar radiation is a function of coat optical, structural, and insulative characteristics, as well as skin color and the optical properties of individual hairs or feathers. In this analysis, I explore the roles of these factors in determining solar heat gain in two desert rodents (the Harris antelope squirrel, Ammospermophilus harrisi, and the round-tailed ground squirrel, Spermophilus tereticaudus). Both species are characterized by black dorsal skin, though they contrast markedly in their general coat thickness and structure. Results demonstrate that changes in coat structure and hair optics can produce differences of up to 40% in solar heat gain between animals of similar color. This analysis also confirms that the model of Walsberg et al. (1978) accurately predicts radiative heat loads within about 5% in most cases. Simulations using this model indicate that dark skin coloration increases solar heat gain by less than or equal to 5%. However, dark skin significantly reduces ultraviolet transmission to levels about one-sixth of those of the lighter ventral skin.

Individual variation in maximum aerobic capacity: cardiovascular and enzymatic correlates in Rana catesbeiana.

We quantified natural variation in maximum aerobic capacity (V02max) exhibited by a free-living population of bullfrogs (Rana catesbeiana) and examined the degree to which such variation is associated with key parameters of the systemic oxygen transport apparatus and oxidative enzyme (citrate synthase) activity at the tissue level. Regression analysis of these data revealed that only ventricle mass and hemoglobin concentration accounted for significant fractions of the variation in V02max. Neither variation in maximum heart rate nor in citrate synthase activity were significantly correlated with individual variation in maximum aerobic capacity. These results support the contention that, in at least some taxa, maximum aerobic capacity is limited by the ability of the cardiovascular system to deliver oxygen to the tissues.