Congress on the Sun in the Service of Mankind (1973)
SOLAR RADIATION AND COLOR ADAPTATION
By H. R. Hay
Sky Therm Processes and Engineering 945 Wilshire Boulevard, Los Angeles, California 90017, U.S.A.
In the arctic, a warm white effect, supplemented by UVR reflection to the skin for provitamin activation, may exceed the survival significance of snow color. In the humid tropics, black pigmentation which causes a cool black effect, dehumidification, UVR screening, photodegradation inhibition, and pathogen control may explain Gloger's Rule and lessen the significance of protective coloration.
Pigmentless hair acting with fiber optic effects, including UVR transmission, is postulated to explain vitamin D production in the arctic and some dermatological diseases, such as Lupus erythematosus, in the more equatorial regions.
Increased research emphasis on the physiologic effects of solar radiation on animals is resolving controversy about the theory: In man as in animals and birds, races seem to exist for the principal purpose of accommodating the organism to differences in heat, visible light, and U-V radiation."1 Signification of new studies requires investigators to heed the widest range of postulations concerning animal coloration as a genetic adaptation.
Consideration of some isolated reports relating color and solar radiation effects (and extrapolations therefrom) will be discussed here without attempting a broad account of genetic coloration. A de‑emphasis of protective coloration in its black and white extremes does not diminish its validity in more subtle color patterns. These may be environmentally influenced and, simultaneously, they may be an achievement of remarkable physiologic balance.
Physics and heat transfer texts oriented toward inanimate materials, in addition to our neural responses on hot asphalted streets, condition us to believe, without qualification, that black objects exposed to the sun are hot and that white objects are cooler. Recent investigations have stressed a duality, however, in which "cool black — warm white" has an equal validity that explains some paradoxes.
Prior to life on earth, dual effects from both black and white coloration established such variety of thermal and hydrological balances that earliest life had ample availability of hospitable environments. Volcanic residues ranged in both crystalline and amorphous forms from nonabsorbent to hydrated and hygroscopic minerals; density and particle size varied the thermal conductance and temperature modulation effects; color added reflectance, absorption, and emissivity of radiation; and all affected moisture relationships to produce microclimates of wide range.
Following the volcanic explosion of Sunset Crater, in 1064 A. D., thousands of Indians moved to the Arizona cinder beds to practice agriculture. The area was later abandoned "because the cinders had been stripped from the soil by the winds, and because of the "great drought of 1276-99."2 The likely explanation of these migrations comes from studies on Lanzorote (one of the Canary Islands) where, in 1730-36, similar volcanoes covered portions of the desert island with black basaltic cinders. These still make possible a unique agricultural economy that permits potatoes, onions, and tomatoes to be exported when annual rainfall is about 15 cm. After spreading 10 cm of the blackest cinders over otherwise non-productive clay "hardpan," farmers grow these crops for 10-15 years before low yields cause them to switch to corn. After about 20 years, the cinders are removed to lava beds and are replaced, whereupon watermelons, potatoes, etc., are again grown.
The clean, glassy cinders prevent evaporation from the underlying soil; their insulating porosity is supplemented by a cool black effect which reduces soil temperatures; and the cinders extract some moisture from the air.3 Cinders dirtied through the years seemingly gain capillarity which causes evaporation losses and less dew collection; thus, after corn yields decrease, new cinders must be brought to the fields.
In Greece, for at least 2,000 years, farmers burning their wheat fields after harvest have formed a surface layer of black insulating ash over the fields in early summer. The cool black effect of this ash keeps soil temperatures lower and reduces evaporation during the hot summer months. Fall rains break the ash to a black pigment which warms the soil in winter by a hot black effect. Earlier emergence of seedlings as well as their more rapid growth seems unrelated to any factors other than the duality of cool and hot black.4
The explanation of cool black is found in reports on skin and rectal temperatures of black and white sheep exposed to intense solar radiation, in Australia. Though surface temperatures of 88°C were measured on black sheep, their body temperatures were lower than those of the white animals. Priestley concluded that the reradiation and induced convection, separate from the pronounced effect of wind velocity, acted to dissipate surface heat and to "satisfy the essential conditions for an automatic compensating mechanism."5
Schleger's study of coat color of cattle revealed "... the only significant correlation between colour and temperature is negative, i.e. , darker animals have the lower temperature..."6 Reporting a mathematical analysis, Kovarik stated: "... increasing absorptivity, apart from causing a higher rate of heat generation, also reduces the mean depth at which this heat generation takes place. The resulting flow of heat is divided between the animal body and the surrounding air mass in such proportion that the total thermal load on the animal reaches a maximum at some intermediate value of absorptance rather than for the extremely dark cover." Kovarik concluded: "Therefore, for a sufficiently large value of thermal resistance of the protective layer, an increased density of pigmentation beyond a certain value results in a reduction of the thermal load."7
Other evidence of cool black includes the examples of the Tuareg wearing black clothing over white in the Sahara; desert nomads living under black tents; the predominance of black goats in arid regions; and the prevalance of black hair on humans indigenous to all tropical countries.
White solar radiation collectors are being increasingly investigated in arctic and subarctic regions. The U. S. Army experimented with white arctic uniforms using a translucent, white, synthetic pile on black backing; but the released test results on solar heating were inconclusive.8 In Antarctica, "the Weddell seal actively seeks the warmth of insolation by orienting with the long axis of the body perpendicularly to the sun's rays." Temperatures measured on adult seals immediately after being killed were 8-10°C warmer on the sunny side than on the shaded side; in intense insolation, the skin temperature was found to be higher than body temperature indicating that heat gained "was distributed to other parts of the body through the circulatory system .... Tanned skins under sun show a marked 'greenhouse effect' in which both fur and skin temperatures rise faster and higher than black-bulb temperatures. A possible lenticular effect of the flattened translucent hairs of the adult is indicated in which the adult skin is warmed faster than that of the pup, but also cools faster in the shade."9
Studies on cadavers of the harp seal exposed to the sun showed that skin temperatures rose from 40°C ten minutes after death to 50°C within 25 minutes, while rectal temperature remained constant at 37° with air temperatures between -1 and -5°C.10 The observation that the skin areas covered with bright hairs are heated to higher temperature than areas covered with dark hairs is explained as "probably due mainly to radiation reflected from hair to hair towards the skin." Solar radiation utilization was positively correlated with the spectral reflectance factor of the pelt.11 It was suggested that the harp seal may be able to absorb solar radiation and reduce its consumption of chemical energy proportionately; the degree of utilization being dependent upon the spectral energy distribution of the incident radiation, hence upon the sun's altitude and the atmospheric moisture.10
Significantly, "introducing an infrared lamp in addition to solar radiation. produced higher skin temperature in bright-furred samples than in black-furred samples..." even though "the black hairs were always heated to the highest temperatures."10 Since the experiment showed possible transmittance of infrared through the pelt, the greenhouse effect is discounted and heat trapping under insulation is a more appropriate explanation. This raises questions about the mechanism of infrared entry and about the effectiveness of the same mechanism for losing body heat during strenuous exercise. The harp seal when exercising develops elevated temperatures first in the flippers, then in certain cases warm spots appeared in irregular patterns on the trunk surface."12 There is need for more clarification of the means by which animals spill heat; vasomotor and pilomotor or feather-erection means may be only the more obvious ones.
As a generalized rule for thermal effects of insolation, it is evident that: Under strong insolation black continuous surfaces of high thermal conductance and storage tend to be hot; similar white surfaces tend to be cooler; and corresponding thermal effects exist below the surface. But reverse thermal effects tend to exist below black and white particulate, porous, or translucent insulating materials.
Ultraviolet Radiation Absorption
The high heat load from solar radiation on dark skin is contraindicated for physical comfort in the tropics. Evaporative cooling, which offsets such heat load, can cause excessive water loss in dry areas or higher adjacent humidity in moist regions. Because "The effect of ultraviolet radiation [UVR] upon cells is invariably deleterious," heavy pigmentation protects Negro skin against cell damage and cancer. Urocanic acid in human skin is another UVR modulator in the delicate balance between cell damage and vitamin D activation in epidermal tissue.
Recently, a significant difference in the reflectivity of neonate and adult skin was demonstrated. Though pigmented adults reflect less light than pale ones, Negro skin in the first days after birth "resembles that of white newborns or even white adults more than that of Negro adults."13 In all races, the neonate skin is lighter and is covered with lanugo hairs which are especially prominent when the provitamin concentration is highest in the first weeks of life. During the first two years, when bone development requires more vitamin D, lanugo persists in the changing vellus which gradually darkens and becomes coarse terminal hair. In adults, 15 percent of the hair remains lanugo type — especially on the face. In view of its presence on children, even in the tropics, lanugo possibly has a role in UVR absorption.
In rats, "The youngest animals have the least reflectance;" reflection of wavelengths from 350 nm to 700 nm increases through the series shaved; scanty grey fur; fairly thick fur; and thick white fur. Reflectance of this high energy band increases with age much more than does UVR which remains relatively constant at 10-15 percent; shaved skin reflects twice as much UVR. Anomalously, infant Wistar rats were shown to have extraordinarily high UVR reflectance compared with Gunn rats — both being albino.13 An explanation of the difference would reveal much about UVR absorption by skin and hair. Feeding rats a rachitogenic diet, Hess found that white rats remained healthy under conditions of UVR exposure which produced rickets in all black rats.14 This demonstrated the ability of white fur to transmit UVR which is stopped by melanin hair pigment.
Presumably, UVR absorbed on hair tips causes some photodegradation and reradiates energy as infrared heat; the UVR which passes into skin is variously absorbed with 5-10 percent reported as activating the vitamin precursors in the malpighian layer. The precursors exist in sebaceous exudates of birds and of some northern furred animals which preen feathers or lick fur on which vitamin D has been produced by external UVR exposure. The quantity of precursors in human sebaceous glands and follicles needs further investigation — particularly, possible differences in persons having blond and pigmented hair shafts.
Excess pigmentation along with climate change to cold and cloudy weather is said to have caused rickets in Neanderthal man in Europe; it has been theorized that northern man adapted to low-level UVR through decreased skin melanin thus allowing greater vitamin D production for bone development. The adaptive nature of pigmentation seems indicated by neonates and by the lesser amounts of it in the skin of palms and on the soles of the feet where a stratum lucidum under the corneum adds UVR screening in an area of low exposure; pigmentation is lacking in nonexposed tissue. Daniels extended the nordic adaptation hypothesis to include light hair and eye coloration and suggested that pigmentation is also related to wavelengths of light other than that of UVR.15
Hair morphology is immensely complicated for reasons not understood, but it is possibly related, in part, to radiation transmission; insulation and outward reflection may be overrated. Reflection to the skin and perhaps fiber optic transmission within the shaft deserve more consideration.
The exposed hair shaft of humans has scales, overlapping five in the length of one, which conceivably may be receptors for solar radiation conducting it inward to fimbrillated ends of birefrigent cortical cells, which may or may not be pigmented. Without pigment absorption, some "piping" could occur to and through the medulla, which is sometimes hollow, until radiation enters the subcutaneous follicle where cell structure and functions are even more elaborate and less known. Four reasons exist for proposing fiber optics; the major one being that when so little is known about the chemical and physical nature of hair, all mechanisms of light transmission need special study.
If UVR for vitamin D production is conducted, in part, by fiber optics, it is significant that blond hairs are much finer and 30 percent more numerous on a comparable skin area than black hairs. Thus, in addition to better insulation, there are more channels for UVR entry into follicles. Provitamin is reported in the follicle much below the malpighian layer. Postulation has caused fiber optics to be considered as an explanation of Lupus erythematosus — a solar radiation-induced disease with inflammation comparable to sunburn occurring around the follicle at a depth below normal tissue underlying sunburned epidermis.16 This inflammation sandwiching normal tissue nay result from laguno or terminal hair fiber optics or from 'transmission through sebaceous exudate.
No facile argument about UVR absorption by protein can exclude fiber optics in the complicated and little understood hair structure. Recognition is recent of the many unknown aspects of hair growth from anagen through catagen to telogen with shaft depigmentation and concentration of the persistent glassy membrane below the shrinking follicle.17 That Lupus erythematosus may occur in persons with apparently pigmented hair and that Xeroderma pigmentosum is accompanied by UVR sensitivity despite an almost coal-black skin pigmentation may be related to a pigmentless portion, near the skin surface, of a hair in telogen. Fiber optic transmission may be maximum at those scale tips which have recently emerged from the follicle of the pigment-less portion of hair shafts (a value of hair growth?). Fiber optics may not exist in a long length of hair which has undergone photodegradation or other chemical or physical change.
Hair pigmentation varies from diffuse to granular and fixed patterns; it changes with age, and in many animals pigmentation loss seems associated with photodegradation to cause seasonal color patterns. Shaft pigmentation would be a logical mechanism for control of effects of solar irradiation. The towhead nordic child, placed out-of-doors by its mother in winter, and white-furred animals, could be dependent, in part, upon fiber optics for vitamin D. After the bone structure is well developed, nordic hair often becomes moderately pigmented only to lose color again in old age when bone structure becomes a survival factor. The blondest nordic hair is reported inland where the food fish have a low liver content of vitamin D. The Eskimo is presumed to get his vitamin from sea food containing it in abundance rather than through dark and largely covered skin.
The "warm white effect" and low UVR reflectance of white hair, pelage, and plumage in the arctic are survival factors. In regions of more intense UVR, photo degradation of protein makes pigmentless white quite disadvantageous. Ornithology literature which attributes wear-resistance of black feathers to a stiffening effect ignores the UVR screening action of melanin. Bird feathers with mixed white and black patterns often show the white portions to be worn away, or badly frayed, at the time of molting. Embrittlement by UVR and subsequent breakage of skin‑shading coatings on tropical animals could explain their less frequent white coloration.
One of the least explained rules in science, first stated in 1833, has been expressed as follows: "Races in warm and humid areas are more heavily pigmented than those in cool and dry areas. Black pigments are reduced in warm dry areas and brown pigments in cold humid areas. The rule, called Gloger's rule, seems to have comparatively few exceptions, but its physiological basis is not at all clear .... The precise selective factors responsible for Gloger's rule are still a mystery."18 For lack of better explanation, some writers1 mention a balance between sunlight and vitamin D; other ones consider black as protective coloration among deep forest shadows. This protective theory is applied likewise to black-coated animals living in black lava beds in arid regions where the principle of cool black for both temperature and moisture balance as well as UVR screening may be of greater importance.
Nature appears replete with paradoxes related to dual effects. The cool black of tropical plumage and pelage is the result of hot black at an external zone. Ambient air of this heated zone is dehumidified in the sense that air at 70°C has 10 times the moisture-carrying capacity of air at 20°C. Whereas there would be practically no humidity gradient from moist skin to highly humid air at their normal temperatures in the tropics, a substantial gradient would exist between the skin and the air over a black insulating layer. Pilomotor control or feather fluttering can then regulate entrance of dehumidified air to the skin as needed.
Although hot dehumidified air would add a heat load both to animals with sweat glands and to dry‑skin birds, the amount of heat needed to prevent growth of fungi and bacteria would seem to be tolerable. Another general rule is: "birds with gaudy metallic coloration are more likely to be found in humid tropical regions ...." This dark iridescence may have the effect of reflecting inward of selected shortwave, bacteriostatic and fungistatic radiation which carries little heat load. In the absence of other pathogen control mechanisms, or in combination with them, dessication and UVR reflection could be protective.
There is less conviction that dehumidification or pathogen control would explain color change of the hypodermal cells of Carausius morosus a walking‑stick insect which loses its pale color and becomes black if only a portion of its body is placed within a high humidity chamber.19 Carausius also changes color corresponding to a dark or light background and is black at 15°C and green at 25°C. The subject of relatively rapid, transitory, physiological color change, including diurnal rhythms, has many aspects of adaptation to solar radiation which are not dealt with in this paper. Pertinent to hot black and cool white, however, is this evidence: "The desert lizard Phrynosoma is light at night and during midday and dark during the early morning and late afternoon.
Photodegradation inhibition by black would not be significant for any tropical life remaining in deep shade throughout the day — conditions which would favor pathogens. But the tendency for animals to leave protective shade, to sunbathe, and to migrate makes black coloration in the tropics considerably more than concealment adaptation.
Animals which match desert coloration of oxidized minerals would bear the highest burden according to Kovarik's conclusion that the thermal load may be greatest for pigmentation of less than maximum density. One may surmise that a reddish brown animal absorbs and reradiates most heat and allows optimal daytime penetration to assist evaporative cooling through the thick fur needed as insulation against body heat radiation to the cold night sky. The presence of white and black camels on hot deserts may be a matter of breeder's preference rather than adaptation. Both reddish brown and black goats seem better adapted to hot dry areas than white ones, which are subject to sunscald.
The futility of trying to explain all animal coloration on the basis of presently known facts about solar radiation adaptation is reinforced by the existence of variegated, mottled or striped coatings. Black and white patterns on zebras, skunks, birds, and on many other animals, may provide a desirable solar radiation balance or may indicate dominance of other considerations, especially that of recognition.
In humans as well as in animals color adaptation to solar radiation is a complex phenomenon about which pertinent questions remain unasked or unanswered. Until reasons for the morphological diversity of hair, pelage, and plumage are explained in terms of physiological effects, there is reason to consider the widest range of theories for color adaptation.
Appreciation is owed to Drs. Farrington Daniels, Jr. and Donald R. Steele for discussions, references, and encouragement regarding dermatological postulations.