Seasonal Adjustment of Solar Heat Gain in A Desert Mammal By Altering Coat Properties Independently of Surface Coloration

The evolution of animal coloration is presumably coerced by sets of selective pressures relating either to visual signalling or to radiative heat gain. A common view is that coat colour, as manifested by surface reflectivity to short-wave radiation, is a prime determinant of solar heat gain (e.g. darker surfaces increase solar heat gain) and that there is a consistent linkage between radiative heat gain and animal coloration (Hamilton, 1973). The degree to which solar heat gain and animal coloration may be independently modified therefore has substantial importance for understanding the costs, benefits and evolutionary limits upon patterns of animal coloration. In the following analysis, we describe a mechanism by which a diurnal desert mammal, the rock squirrel (Spermophilus variegatus Erxleben), substantially modifies solar heat gain independently of environmental factors and surface coloration.

Solar heat gain in animals with fur or feather coats is a complex function of environmental properties such as wind speed and intensity of solar radiation, as I well as a suite of animal properties that are often subtle. The latter include hair optical properties and coat structure (Kovarik, 1964; Hutchinson & Brown, 1969; Øritsland, 1970, 1971; Øritsland & Ronald, 1978; Cena & Monteith, 1975a; Walsberg et al. 1978; Walsberg, 1983, 1988a,b). An example of the possible importance of such complex effects is the reduction of solar heat gain by optimization of coat structure in rock squirrels, diurnal rodents inhabiting rocky canyons and slopes in Mexico and the western United States, including the Sonoran Desert (Hall, 1983). The pelage of S. variegatus consists of two well-defined layers that contrast in their structure and optics: a dense inner coat dominated by fine, dark hairs, and a sparse outer coat dominated by coarse, light hairs that produces the animal ‘s cryptic appearance (greyish-brown in this population). During the summer months, the ratio of inner to outer coat depths characteristic of rock squirrels in the Sonoran Desert is very near that theoretically predicted to minimize radiative heat gain (Walsberg, 1988b). This population therefore illustrates a mechanism by which solar heat gain may be adjusted without affecting coat insulation and surface coloration.

Selection may favour adaptive adjustments of solar heat gain independently of surface coloration, either between populations occupying contrasting environments or within populations exposed to seasonal changes in the thermal environment. There is marked seasonality in the Sonoran Desert. During the midday period, in which these diurnal ground-dwelling squirrels are most active, air temperatures near (5 cm above) the soil surface are typically 20–30 °C in the winter and 40–55°C in the summer (G. E. Walsberg, unpublished data), with clear skies and intense radiation in both summer and winter.

We tested for the existence of adaptive adjustment of solar heat gain by comparing the radiative heat loading characteristics of winter and summer rock squirrel coats. We quantified the radiative heat load transferred to the skin, as well as the optics, structure and thermal insulation of the inner and outer coats. Walsberg’s model (1988b) was then used to explore the role of coat properties in determining observed changes in solar heat gain. Finally, we estimated the consequences of observed adjustments in coat structure upon net heat flow between the animal and the environment.

(All radiation relationships refer to total solar radiation)

 
• α

  absorptivity of individual hairs.

 
• α_c

  absorptivity of coat.

 
• β

  backward scattering coefficient (‘reflectivity’) of individual hairs.

 
• β_c

  reflectivity of coat.

 
• β_s

  reflectivity of skin.

 
• ΔT_e

  temperature gradient from outer coat surface to environment (K).

 
• ΔT_c

  temperature gradient from skin to outer coat surface (K).

 
• ΔT_ic

  temperature gradient across inner coat layer (K).

 
• ΔT_oc

  temperature gradient across outer coat layer (K).

 
• τ

  forward scattering coefficient (‘transmissivity’) of individual hairs.

 
• τ_c

  transmissivity of entire coat

 
• τ_ic

  transmissivity of inner coat

 
• τ_oc

  transmissivity of outer coat

 
• τ_s

  transmissivity of skin

 
• τ_s+c

  transmissivity of skin and entire coat

 
• τ_s+lc

  transmissivity of skin and inner coat

 
• η

  [(l-τ)²-β²]^1/2.

 
• d

  hair diameter (m)

 
• I

  radiation interception function, probability per unit coat depth that a ray will be intercepted by a hair (m⁻¹)

 
• k

  volumetric specific heat of air at 20°C (1200 J m⁻³K⁻¹)

 
• l_c

  coat thickness (m).

 
• l_h

  hair length (m).

 
• n

  hair density per unit skin area (m⁻²)

 
• Q

  net heat flux across skin and fur (Wm⁻²)

 
• Q(Z)

  heat generated by radiation absorption at level z (W m⁻²)

 
• Q_s

  heat load on animal’s skin from solar radiation (W m⁻²)

 
• r_e

  external resistance to convective and radiative heat transfer (sm⁻¹)

 
• r_c

  coat thermal resistance (sm⁻¹)

 
• r_ic

  thermal resistance of the inner coat layer (sm⁻¹)

 
• r_oc

  thermal resistance of the outer coat layer (sm⁻¹).

 
• r_z

  thermal resistance from skin to level of ray absorption in coat (sm⁻¹).

 
• S_i

  solar irradiance at the coat surface (W m⁻²).

 
• S⁻

  flux of solar radiation going towards the skin (W m⁻²).

 
• S⁺

  flux of solar radiation going away from the skin (Wm⁻²).

 
• T_a

  air temperature (K).

 
• T_s

  skin temperature (K).

 
• u

  wind speed (ms⁻¹).

 
• z

  depth within coat (m).

Collection and preparation of samples

Nine adult rock squirrels were collected during December and January in the Sonoran Desert, in Maricopa Co., Arizona. An approximately 20cm² square section of skin and attached fur was removed from the mid-dorsal region of each animal and dried in a flat position with the coat normally depressed.

Measurement of heat flow and thermal resistances

Solar heat gain was determined from measurements of heat flow at the skin and calculated as (net heat flux with solar radiation) minus (net heat flux without solar radiation). Consistent with the theoretical model described below, this value equals the portion of the heat generated by insolation that functions as a heat load on the skin.

Simulated solar radiation was generated by a Kratos Analytical Corporation SS1000X solar simulator (see Walsberg, 1988a). Irradiance perpendicular to the beam was measured at the level of the coat using an Oriel Corporation model 7080 pyroelectric radiometer and maintained at 1000 ± 5 W m⁻².

Laminar wind flow was produced by an open-throat wind tunnel with turbulence intensity less than 0·5% (Walsberg, 1988a). Air flowed parallel to the skin, from anterior to posterior portions of the sample. This mimics the condition experienced by an animal oriented with its head directed into the wind. Wind speeds were measured with a Thermonetics HWA-101 thermoanemometer mounted 2 cm above the sample surface. The anemometer was calibrated using the method of Walsberg (1988a).

Total reflectivity of the coat and skin to simulated solar radiation were measured using the techniques of Walsberg (1988a,b). Initially, reflectivity of the outer coat surface was measured, then the outer coat was trimmed off and the reflectivity of the inner coat layer measured. Skin reflectivity was similarly measured after all hair had been trimmed from samples.

Cena & Monteith (1975a) described the relationship between optical properties of individual hairs and bulk coat properties (reflectivity, transmissivity, depth relationships and interception function). Using Walsberg’s (1988a) method, these were used to compute the hair optical properties necessary to produce the measured reflectivity and transmissivity of coats with the depth and interception functions characteristic of individual samples. This was done separately for the inner and outer coats.

This model was applied using numerical integration. The coat was divided mathematically into 200 segments and equations 5–9 were used to estimate S⁻, S⁺, Q(z) and mean r₂ in each increment. Values for Q_s(z) were summed and added to the estimated heat generated at the skin level to obtain the total heat load at the skin produced by solar radiation (Q_s). The coat was assumed to consist of two internally uniform compartments representing the inner and outer layers. Each increment within a layer was assumed to contain equal fractions of that layer ‘s total insulation and coat elements determining radiation interception.

It is remarkable that although rock squirrels did not differ seasonally in their appearance, visible coloration (Fig. 1), or total solar reflectivity (Table 1), solar heat load transferred to the skin was substantially greater in winter coats than previously reported for summer coats (Fig. 2). At wind speeds below 2·0ms⁻¹, heat gain was increased about 20% in winter compared to summer. As in summer coats (Walsberg, 1988b), mean radiative heat gain at the skin beneath winter coats declined from 52 to 38% of short-wave irradiance at the outer coat surface as wind speed increased from 0·5 to 4·0ms⁻¹ and external resistance declined from 54 to 14sm⁻¹ (Figs 2, 3).

Closely conforming to measured values for radiative heat gain in winter coats were those predicted using mean data presented in Tables 1 and 2, and the two-compartment model based on equations 5–9 (Fig. 2). Mean errors ranged from 0 to 5·4% over the range of wind speeds used. Similarly small errors have been found in previous tests of this model and data for summer coats (Walsberg, 1988b).

Unexpectedly, thermal resistance of winter coats was 42–50% lower than the values previously reported for summer coats (Fig. 4). Over the range of wind speeds used, coat thermal resistance (r_c) averaged 33·0 s m⁻¹ and declined 23% as wind speed was increased from 0·5 (r_c = 37·1 sm⁻¹) to 4·0ms⁻¹ (r_c = 28·7 sm⁻¹) (Fig. 4). The lower thermal resistance of winter coats reflects both a 23% decline in the total depth of winter coats compared with summer coats, and a decreased thermal resistance per unit depth in winter coats (calculated from data in Table 1). The decrease in coat depth was not an artefact of increased fur compression during sample preparation as the ratio of total coat depth to the average length of the guard hairs forming the outer fur boundary was similar in winter (0·22) and summer (0·23).

Outer coat reflectivity was significantly greater than inner coat reflectivity (ANOVA, P < 0·05, N = 9; Table 1). Hair optical properties differed significantly between inner and outer coats (ANOVA, P<0·05), and between the same coat layer in winter and summer pelages (Table 2). Particularly notable were differences in the inner coat, which forms most of the fur depth. Here, forward scattering (τ) by individual hairs was increased by 10% in winter months compared to summer months, absorptivity (α) was decreased by 20%, and backwards scattering (β) was decreased by 63% (Table 1). These changes occurred without seasonal modification of coat reflectivity (Table 1).

Significant seasonal differences were apparent in coat structure. Due mainly to a 34% increase in density of guard hairs during winter months, the radiation interception function was increased by 21% (outer coat) or 28% (inner coat) in winter compared with summer (Table 1).

The increase in radiative heat gain observed in winter coats compared with summer coats is equivalent to that which would be produced by a 20% elevation in the fraction of sunlight absorbed by the animal’s coat (α_c. + τ_c = 1-β_c) if all other fur properties could be held constant. The quantity 1—βis about 0·75 in rock squirrels (Table 1). A 20% increase (1—β = 0·90) would produce a black coat (β_c = 0·10). Thus, the seasonal difference in solar heat gain is equivalent to that which might be produced by a major change in the animal ‘s appearance, if surface coloration could be changed without affecting other coat properties.

Under these conditions, winter coats are predicted to transmit net heat loads averaging 38-126 Wm⁻² greater than summer coats. This 16–22% increase in heat load is 1·0–3·4 times the estimated area-specific basal metabolic heat production of S. variegatus (Walsberg, 1988b), equating to the change in heat load across those portions of the skin directed towards the sun that would be produced by a change in air temperature of 4–14°C (Fig. 5). Such substantial declines in the heat load clearly are advantageous for mammals inhabiting a subtropical desert.

The increased solar heat gain observed in winter coats compared with summer coats results from alterations in a suite of coat and hair properties (Tables 1 & 2). The relative importance of these various seasonal changes can be estimated using simulations incorporating the validated model subsumed in equations 5–9, data represented in Tables 1 and 2, and assuming that wind speed is 1·0ms⁻¹. Radiative heat gain was estimated for a coat resembling the summer pelage except characterized for one variable by the mean value typical of winter fur. Substituted variables were coat depth, the interception function (I), coat thermal resistance per unit depth, and hair optical properties. Factors characteristic of inner and outer coats were used separately. An associated set of hair optical properties (α β τ) was treated as a single variable. Simulation results suggest that the two most important factors producing increased heat gain during winter months are changes in the inner coat in thermal resistance per unit fur depth, and in the optical properties of individual hairs (Fig. 6). The net effect of alterations in hair optical properties in the inner coat during the winter (i.e. increased forward scattering, decreased backward scattering and absorptivity) is to enhance penetration of radiation and consequently elevate solar heat gain. Decreased thermal resistance in the inner coat tends to increase radiative heat gain by reducing the fraction of the total thermal resistance (r_c+r_e) between a point of ray absorption and the skin.

Though illustrative, these simulations provide only a crude approximation of the relative importance of various factors, because interaction effects among the variables were ignored. This lack of interaction effects is reflected by the failure of the sum of the changes predicted to result from altering individual variables to equal the net effect predicted when all factors act in concert. A more sophisticated analysis would require knowledge of the functional relationships between all variables subsumed in the model. Unfortunately, the relationship between hair density and coat thermal resistance is inadequately understood. The complexity of this relationship is illustrated by the association in winter pelages of decreased fur insulation with increased hair density. Although it may initially appear improbable, a negative effect of hair density on coat insulation is explicable in the context of likely effects of fur structure on major avenues of nonevaporative heat flow (radiation, convection, conduction through the air contained in the coat, and conduction along hairs). The relative importance of these transport modes undoubtedly varies with coat structure (see, for example, Davis & Birkebak, 1974; Cena & Monteith, 1975a,b ; Gebremedhin et al. 1983). In general, radiation and convection are most likely to be important in sparse coats. Because the thermal conductivity of hair is much greater than that of air (Davis & Birkebak, 1974), conduction should be maximized in dense coats. If thermal conduction along hairs is sufficiently important, increases in hair density will decrease coat insulation. Unfortunately, estimating the net effect of changes in hair density requires unavailable data describing the thermal conductivity of individual hairs. It is clearly possible, however, that the increased hair density observed in winter coats of rock squirrels may be a mechanism for reducing coat insulation and consequently increasing solar heat gain.

In conclusion, the seasonal alteration in solar heat gain acquired by the pelage of rock squirrels is in a direction expected to be adaptive and is substantial, being equivalent to the change in heat load that would be produced by major changes in air temperature or the animal ‘s surface coloration. Such results suggest the existence of a previously unknown mode of long-term thermoregulation by varying coat optics and structure to alter solar heat gain independently of the animal ‘s coloration. Use of such mechanisms may therefore uncouple the selective pressures related to thermal and social signalling effects of animal coloration.

We thank G. Helseth and H. Berna for aid in collecting specimens. This investigation was supported by a grant from the National Science Foundation (BSR 85-21501).