THE METABOLIC SIGNIFICANCE OF DIFFERENTIAL ABSORPTION OF BY BLACK AND WHITE BIRDS

FRANK HEPPNERl

Department of Zoology University of California Davis, California

The surface color of homeotherms is com- The undyed birds exposed to radiant energy monly thought to have two possible functions: consumed a mean of 2.00 ml OJmin, while concealment (Cott 1957) and communication the dyed birds exposed to radiant energy had ( Lorenz 1935; Tinbergen 1948). Hamilton a mean consumption of 1.44 ml Oz/min. By and Heppner ( 1967) proposed a third possible assuming a thermal quotient of 4.8 Cal/ml 02 function for dark, or black, homeotherm color- (King and Famer 1961), the heat production ation: the reduction of the metabolic cost of of the blackened birds was 6.9 cal/min, and homeothermy by maximization of absorption the heat production of the white birds was of radiant solar energy. This hypothesis pro- 9.6 Cal/mm, a difference of 2.7 cal/min. It is posed that the integument o,f black animals this difference that must be accounted for in absorbs more of the visible and near infrared calculating the difference in the amount of components of solar energy than does the radiant energy absorbed by the blackened and integument of lighter-colored animals, and white birds. that this greater absorption may permit them to reduce their heat 108s~when ambient tem- DETERMINATION OF TOTAL AMOUNT peratures are below their lower critical tem- OF ENERGY FALLING ON SURFACE perature. As reported earlier, the rate of energy falling Hamilton and Heppner reported that black- on the surface of a bird in the metabolism dyed, white Zebra Finches (Poephilu castan- chamber was 1.23 cal/cm2-min, as determined Otis) demonstrated a significant metabolic by a 59junction Eppley pyroheliometer. The economy over undyed birds when both were metabolism chamber, which was made of exposed to artificial sunlight while in a mod- Plexiglas, had a lid fitted with an ultraviolet erately cold (10%) metabolism chamber. I transmitting glass filter. During a metabolism now report the results of experiments relating test, the chamber was submerged in a water the metabolic differences between blackened bath, with 1 cm of water over the top surface and white birds observed by Hamilton and of the chamber lid. Heppner to the difference in amount of radi- The spectrum of the energy that fell on ant energy absorbed by the black and white a bird in the chamber, after passing through the birds in our experiments, and discuss a physi- lid and the water over the lid, was determined cal mechanism whereby dark-colored birds by employing a Beckman DK-2 spectrophoto,m- might achieve a metabolic advantage over eter set up in a spectroradiometry configura- lighter counterparts. tion. A Sylvania DWY “Sun-Gun” lamp, which was the artificial sun in the metabolism experi- DETERMINATION OF DIFFERENCES ment, was mounted over the entrance port of IN ABSORBED ENERGY the spectrophotometer. Spectrum measure- Of paramount importance is the quantitative ments were then made (fig. 1) over the range relationship between the difference in require- 0.359-2.960~ of: (A) the light of the lamp ments for chemical energy of the white and alone, (B ) the light passing through the lid blackened birds, and the different rates of of the metabolism chamber, which was energy absorption from the artificial sun. This mounted between the lamp and the spectro- relationship can be determined by comparing photometer, and (C) the light passing through the difference in heat production, expressed both the lid and a l-cm layer of tap water in calories, between the white and blackened which was created by making a rim of mask- birds, with the difference in the amount of ing tape around the edge of the chamber lid energy absorbed at the surface of birds in the and then pouring water on the lid. The area two color conditions. under the curves can be expressed as the amount of energy falling on‘ a unit of surface 1 Present address: Department of Zoology, University of Rhode Island, Kingston, Rhode Island 02881. per unit of time. The lid had little effect on

The Condor, 72 :50-59, 1970 50 METABOLIC SIGNIFICANCE OF ABSORPTION OF RADIANT ENERGY 51

100 90 1

70- : 2 60- t, YI so- : ; 40-

WAVELENGTH OJ,, 08 I I I I I, - .3 .5 .7 .9 1.1 I.3 1.5 1.7 1.9 2.1 2.3 2.5 FIGURE 1. Spectrum measurements of Sun-Gun WAVELENGTH I/L, artificial sun (A, Sun-Gun; B, Sun-Gun through filter; C, Sun-Gun through filter and water). FIGURE 2. characteristics of the sur- faces of white and black-dyed Zebra Finches (solid line, black bird; dashed line, white bird). the energy passing through it (curve 1B ) over the spectrum range measured, but the water cut off radiation beyond 1.406 p and shifted tions at the five locations were then averaged the energy peak to about 1.050 .U (curve 1C). at 0.100 ,Aintervals and a compo,site curve was This curve represents the spectrum of the hand drawn for each bird (fig. 2). light energy falling on the surface of a bird The shapes of both curves are generally sim- in the metabolism chamber. From the pyro- ilar, both birds tending to be “white” beyond heliometer measurements, it was known that 1.060 p, but there is a sharp difference in the energy falling on the bird had an absolute absorbance from 0.350 to 0.800 p, with the value of 1.23 cal/c&-min. This value is blackened bird absorbing more, as would be equivalent to the area under curve 1C. expected. If the fraction of energy absorbed by the In figure 3 the emission spectrum of the surface is determined for each wavelength, lamp is again shown with the curves produced and this fraction then multiplied by the frac- by multiplying the absorption fractions of the tion of total energy emitted by the source at black and white birds at 0.106 p intervals times that wave-length, a new curve will be ob- the height of the emission curve at the same tained, the area under which will be the wavelength. The area under these curves, energy absorbed by the surface. This area can compared with the area under the curve rep- be measured by a mechanical integrator (pla- resenting the energy falling on the bird, indi- nimeter), and compared with the area under cates what fraction of the energy falling on the curve of the emission spectrum, the ab- the bird is actually absorbed. solute value of which is known ( 1.23 cal/cms- The areas under the three curves were mea- min). The new value obtained will be the sured with a planimeter. It was found that energy absorbed by the surface of the bird. the area under the curve representing the en- The absorption characteristics of the birds ’ ergy absorbed by the black bird was 33.2 per surfaces were determined by setting up the cent of the total energy falling on the bird, Beckman DK-2 spectrophotometer in a spec- and the area under the curve for the white troreflectometer configuration. Live white bird, 16.0 per cent. Zebra Finches and newly dyed, blackened From the pyroheliometer measurements, Zebra Finches were anaesthetized with a gas the area under the curve representing energy anaesthetic and strapped to the sample port falling on the bird is equivalent to 1.23 cal/ of the integrating sphere of the spectrophotom- cm2-min. The black bird absorbed 33.2 per eter. The reflection and absorption charac- cent of this energy, or 0.41 cal/cm2-min, and teristics were compared to a white reference the white bird 16.0 per cent, or 0.20 cal/cm2- block of magnesium carbonate. Because there mm. were slight differences in absorption at differ- Finally, to determine the difference in total ent locations on the back, measurements were energy absorbed by the black and white birds, taken at five locations. The absorption frac- it is necessary to know the area upon which 52 FRANK HEPPNER

100

90 ;;e;;;Sfolling 80 . Energy absorbed 5 70 by black bird. ti Energy absorbed ; 60 by white bird. Ly g 50 f 40 4 / ‘, 1.23 cal/cm2Amin \ ff 30

20

WAVELENGTH (+L’

FIGURE 3. Energy falling on the surface of birds, and energy absorbed by black and white birds.

the radiation is falling. This cannot be mea- conservative. The effective absorbing area sured precisely, because there are reflections of the birds is probably larger than the 14.7 from the bottom of the chamber that will ir- cm2 obtained by projecting the dorsal surface radiate the ventral surface of the bird, postural of the bird on a plane, since there will be some variations, and differences in feather erection reflections in the experimental universe that which will alter the effective area exposed to will impinge on all surfaces of the bird, direct radiation. An estimate can be obtained although the intensity of these reflections is by projecting the dorsal view of the bird on probably small. A larger surface area than a plane surface, and measuring the area of estimated here would increase the absolute this projection. The dorsal projected area of value of the difference in energy absorbed by three birds (excluding the tail) was 13.8, 15.2, black and white birds. Even with a conserva- and 15.2 cm2, or a mean of 14.7 cm2. These tive value, it appears that the difference in areas were obtained by measuring the pro- energy absorbed is sufficient to account for jected area with a planimeter. the metabolic economy demonstrated by the Using 14.7 cm2 as the “absorbing” surface blackened birds. area, it is calculated that the white birds ab- sorbed 2.9 cal/min while the black birds ab- DETERMINATION OF TFMPERATURE sorbed 6.6 cal/min, or 3.1 cal/min more than UNDER THE FEATHERS the white birds. The 3.1 cal/min difference To interpret the results of the metabolism ex- in absorption of energy may be compared with periment and the experiment reported above, the metabolic economy of 2.7 cal/min demon- it was desirable to obtain information about strated by black birds in the metabolism ex- the heat flow from the birds’ skin to the en- periment reported earlier. The value of 3.1 vironment, under conditions that approximated cal/min as the difference in energy absorbed the experimental setup of the metabolism ex- between the black and white birds is probably periments. Temperature measurements can METABOLIC SIGNIFICANCE OF ABSORPTION OF RADIANT ENERGY 53

TABLE 1. Temperatures (“C) in three positions TABLE 2. Temperatures (“C) in two positions under the feathers of a stuffed black and white under the feathers of a live white and black-dyed Yellow-billed Magpie ( ambient temperature, 15&C ). Zebra Finch (ambient temperature, lO.O”C).

Black feathers White feathers Lamp off Lamp on BkWk white Black white Under surface 41.7 37.5 Middle 38.0 35.4 Under surface 26.1 26.1 32.8 28.8 Next to skin 35.0 34.9 Next to skin 37.8 37.8 37.8 37.8 indicate the steepness of the gradient from obtain only readings next to the skin, and the skin of a bird to the environment, and just under the first layers of feathers. Measure- thus furnish an idea of the rate of heat flow. ments were made under both the white and Two experiments were performed which sug- the black feathers with the Sun-Gun on, and gested what the heat flow conditions of the off. The bird was anaesthetized with ether metabolism experiments might have been. and placed on its back with the ventral side exposed to the lamp. The results are recorded STUFFED BLAC,K AND WHITE BIRD in table 2. A cotton-stuffed museum specimen of a Yel- low-billed Magpie (Pica nuttalli) was placed DISCUSSION OF TEMPERATURE EXPERIMENTS ventral side up on a piece of corrugated card- The results of these experiments, although not board. The top of the chamber used in the useful in a quantitative sense because of dif- metabolism experiment was then mounted ferences in experimental conditions between above it and the lamp used in that experiment the metabolism and temperature experiments, placed above the chamber lid, 25 cm from suggest a mechanism by which the heat econ- the ventral surface of the magpie. A layer of omy demonstrated by black birds in the water 1 cm deep was made above the filter metabolism experiment might be accomplished in the chamber lid, to simulate submersion in (fig. 4 ) . For a bird of any color in a cold a water bath. Yellow Springs Instrument Co. environment, in the absence of sunlight (fig. thermister probes were placed at various lo- 4A), the direction of heat flow is from the cations under the feathers and connected to a interior of the bird to the environment, and YSI thermometer. the rate of heat flow, indicated by the length The experimental setup was located in a of the arrow, is governed chiefly by the insu- walk-in controlled temperature room which lative properties of the feathers. was set at 15.6”C. The magpie specimen was In the case of a black bird in the presence allowed to come to ambient temperature; then of sunlight (fig. 4B), the outer layer of feathers the Sun-Gun lamp was turned on, and tem- is warmed by the sun, thereby reducing the perature readings were made after the tem- gradient between the skin of the bird and the perature at the various locations had reached outer layer of feathers, with the result that a state. of equilibrium where the incoming heat produced by radiation was balanced by the heat reradiated, and carried off by con- vection. Temperatures under both the black and the white breast feathers were measured under (1) the first layer of feathers from the sur- face, (2) approximately in the middle of the feathers, and (3) next to the skin of the speci- men. The results are recorded in table 1.

WHITE AND BLACK-DYED LIVE BIRD The feathers on half the breast of a white Zebra Finch were dyed black in the manner of the metabolism experiments. The experi- mental setup was the same as in the stuffed- bird experiment, except that the ambient tem- perature was lO.O”C and the lamp was 3.5 cm SKIN OUTER ENVIRONMENT from the surface of the bird. The plumage of FEATHERS the bird was only slightly thicker than the FIGURE 4. Heat flow in black and white birds under diameter of the probe, so it was possible to different conditions. For explanation see text. 54 FRANK HEPPNER

the rate of heat flow from the skin of the bird The thermal radiation emitted by the surface to the outer feathers is decreased. At the same is given by time the gradient between the outer feathers R” = eaoAaTa4, (5) and the environment is increased, increasing the heat flow from outer feathers to the en- where E is the infrared emittance of the sur- vironment. However, a portion of the heat face, A, is the surface area, u is a constant that flows from the outer feathers is energy (1.376 X lo-l6 kcal/cm2-set-X4), and T, is that has been reradiated off as a consequence the surface temperature in “K. of the feathers being warmed by sunlight. The Equation ( 1)) written in more specific form, net result is that the outward flow of metabolic where relevant to consideration of the effects heat is reduced in the presence of sunlight. of differential absorption of solar energy, is A double line indicates reradiated heat. The then situation in the white bird is basically the 8kkfk(lb,ro,L)(Tb-T,)’ +Qe same (fig. 4C), but the quantities are differ- k = 8 h,A, ( T, - Tai,) + R,” - R” ent, since the white bird reflects a portion of k the incoming solar energy. + aSDAD + S,“. (6) Birkebak (1966) has derived a set of gen- eral equations for heat exchange in animals An increase in cr, the absorptance of solar which are useful for iIIustrating this proposed energy, might affect the dher terms of equa- mechanism. tion (6) in several ways, one way being to increase the rate of heat loss in infrared emis- Qcond+ Qe= Qconv+ IL” - R” + SD”+ Sd*, (1) sion, as an effect of the heating of the surface, where Qcondis the heat conducted from the while decreasing the rate of conduction of interior of the body to the integument surface, body heat from the interior to the surface, as a Qe is heat lost by evaporation, Qo,, is heat result of the decreased gradient between the lost by convection, R,* is infrared energy ab- interior and the surface. sorbed by the animal from its surroundings, The smaller the gradient is between the R* is infrared’ energy emitted by the animal, skin and the outer feathers, the slower will be SD* is direct solar energy absorbed by the the loss of metabolic heat from the bird. Maxi- animal, and Sd* is diffuse solar energy ab- mizing the amount of solar energy absorbed sorbed by the animal. Q might be expressed by the outer feathers will maximize the heat as Cal/unit time. economy. The heat conducted from the interior of the DISCUSSION body to the integument surface is expressed as The sun radiates energy that potentially could Qeond=~ilkrcfich, ro, L) (Tb- Ta), (2) be used by warm-blooded animals to reduce the energy cost of maintaining a body temper- ature higher than that of its surroundings. The vrhere k is thermal conductivity of the integu- great absorption of short wave-length solar ment, flc( rb, rO, L) is the geometrical form energy by black feathers can serve to decrease factor for a given body’ shape, Tb is the deep the temperature gradient between the skin of body temperature, and T, is the temperature the bird and the outer feathers, thus slolwing at the surface of the body. An increase in the the flow of heat from the bird to its surround- temperature of the body surface might thus ings. In the absence of solar radiation, as in slow the flow of body heat to the environment. the shade and at night, the black bird would Absorbed direct solar energy, the sixth term not necessarily radiate off more heat than a in equation (1) is expressed by Iighter counterpart, because the energy SD* = c&DAD, (3) emitted by a surface at the temperature of the outer feathers of a bird is chiefly in the form where a is the absorptance of the surface, SD of long wavelength infrared. As will be dis- is the direct solar radiation and An is the pro- cussed later, the emissive properties of black jected area of the surface. A similar equation and non-black feathers with respect to these applies to Sd*, the diffuse solar radiation. wavelengths appear to be nearly the same. The heat lost by convection is expressed by Thus it might be possible for a black bird to show a net energy advantage over a similar, Qconv= 8 hk&( Ta- Tair)y (4) but non-black bird, because the black bird where hr is the average heat transfer coeffi- would lose less heat during the day than the cient for the kth part of the body and Al, is its non-black bird, and lose about. the same surface area. amount as its lighter counterpart at night. METABOLIC SIGNIFICANCE OF ABSORPTION OF RADIANT ENERGY 55

The amount of energy available for absorp- In terms of absolute values, they found that tion depends on many factors, including lati- a nearly nude, resting man saved about 80 kcal/ tude, altitude, season, and atmospheric condi- hr by being in the sunshine as opposed to tions, but under certain conditions represents a being in the shade. This figure represents potentially significant amount to a small ani- 20-25 per cent of the total energy output at mal whose surface/volume ratio is large. Gates that temperature. The posture of the man (1966) presents data for the level of solar appeared to make little, if any, difference in radiation at the earths’ surface under various this figure. conditions. It is not unusual to find levels of Contrary to Blums’ (1945) prediction that a 1.00 Cal/cm*-min at temperate latitudes. A man shaded from sunshine is appreciably in- small bird whose dorsal surface area (exclud- fluenced by radiation from sky and ground, ing tail) is 10 cm* potentially could absorb Adolph and Molnar found no appreciable dif- 600 cal/hr under these conditions. When this ferences in heat production between men who is compared with the approximately 400 cal/hr were shielded from the suns’ rays, but exposed resting metabolic rate of a 30-g passerine bird to ground and sky radiation, and unshielded (Lasiewski and Dawson 1967), it is clear that men outdoors at night, at the same ambient radiant energy absorption represents a poten- air temperature as the daytime measurements. tially important factor in the overall energy This finding does not necessarily mean that balance. The larger the animal, the less im- ground and sky radiation are unimportant to portant absorption of energy should be, owing a smaller animal whose surface/volume ratio to the lessening of the surface/volume ratio, is greater than mans.’ although a 2-kg chicken, whose resting meta- The experiments of Adolph and Molnar bolic rate is 5.5 kcal/hr (Barott and Pringle were chiefly concerned with examining the 1941) and whose dorsal surface area, exclud- effects of solar radiation at low-to-moderate ing the tail, is about 300 cm* has 18 kcal/hr of air temperatures. It might be asked whether solar energy falling on its back under the solar radiation also affects physiology at higher conditions described above. How much of this ambient temperatures. energy is actually absorbed by the feathers Craig and Cummings (1962) examined the will depend on the characteristics of the thermal influence of sunshine and clothing on feathers, and the posture and orientation of men walking in humid heat. They found that the bird relative to the sun. the same physical strain, in terms of heart rate, The physiological effects of sunbathing at blood pressure, and sweating, was found in moderately low temperatures were explored heavily clothed men walking outdoors in an by Adolph and Molnar ( 1946)) who compared ambient temperature of 29.4”C, and a solar various physiological parameters (heart rate, radiant energy level of 1.00 Cal/cm*-min as surface temperature, deep body temperature, was produced indoors at a temperature 5.6” oxygen consumption, urine production, evap- C higher, when the work load was the same. orative water loss, and blood chemistry) of The clothing was a dark olive drab on the nude men under various conditions of ambient outside. This 5.6% increment at 29.4% temperature, cloudiness, humidity, and work- is quite comparable to the values found by ing conditions (at rest, working, etc. ). Their Adolph and Molnar at lower temperatures. most significant measurement with reference Relative to energy metabolism, then, to the present discussion was that of oxygen to sunshine appears to have the same func- consumption, hence energy metabolism, mea- tional effect as raising the ambient tempera- sured under conditions of sun and shade out- ture. The degree to which this effect is pro- doors in the fall at Rochester, New York. They duced will depend on the characteristics of found that lying in sunlight with a radiation the incoming radiation, and the properties of intensity of approximately 1.00 cal/cm*-min, the surface upon which it falls. as opposed to lying in the shade, had the same According to Kirchoffs’ Law, a surface functional effect upon the subjects as raising which is a good absorber is also a good emitter. the ambient air temperature 6°C in the range It is therefore reasonable to ask whether a between 1.1” and 26.7”C. That is, the thresh- black animal that has gained a thermal ad- old of shivering was raised, skin surface tem- vantage during the day by sunbathing might perature was raised, and heat production was not lose that advantage at night by emitting lowered. The difference between sun and more heat than its more lightly colored coun- shade was lessened when work was done, but terpart. the total energy production in both cases was This question was posed, in a different greater than while resting. reference, by Hesse et al. (1937) and Hamil- 56 FRANK HEPPNER ton ( 1939) who speculated that the white color energy falling upon it), and a surface with an of arctic animals is an adaptation for heat con- of 1.0 absorbs all energy falling servation. Two experimental tests of this hy- upon it (and reflects none). Hardy and Mus- pothesis have been made, with differing re- chenheim ( 1934), Hardy ( 1939), and Barnes sults. ( 1963)) using different techniques, report that Stulken and Heistand ( 1953) measured the human skin has an emissivity of 0.98 to 0.99. oxygen consumption of C-57 black mice, Swiss This means that for that region of the spectrum albino mice, and Swiss albino mice which had in which the skin is radiating energy (4-20 P ) , been dyed black with a commercial hair dye. the surface behaves almost like a black body. Oxygen consumption was measured at various Hammel ( 1956) measured the emissivity of temperatures from 30°C to 5°C. They found the pelage of light and dark forms of arctic that in all cases oxygen consumption increased mammals and birds, and found that both had as the temperature decreased, but the rate in- an emissivity of close to 1.00. Hammel con- creased faster in the black mice and the black- cluded that there should be no difference in dyed mice. Their conclusion was that the heat loss between light- and dark-colored forms black mice were radiating off more energy of an animal. than the white mice and thus needed a higher Kelly et al. ( 1954) studied the role of color metabolic rate to maintain a constant body and solar radiation in the thermal environment temperature. of swine. They contrasted the amount of There are several factors that preclude a solar radiant energy absorbed by black and clear interpretation of these results. The C-57 by white pigs and found that black pigs absorb black mouse is a very active strain (Thomp- 90 per cent more than white pigs over the son 1953) and might react differently to cold range 0.4-3 p, which is approximately the than the albino ’ strain. If the C-57 black mice range of direct solar radiation, and 50 per cent became more active as the temperature de- more over the range 0.450 p, which includes creased, they would also show a higher oxygen atmospheric and diffuse sky radiation. Their consumption. In the case of the black-dyed values for the difference in absorption of direct mice, the dye might have produced undetected solar energy between black and white pig skins changes in the insulative characteristics of the compare closely with the value reported here fur, thus permitting a greater loss of heat than for differences in absorption between white in the undyed animals. In the experiment of and black-dyed feathers under similar condi- Hamilton and Heppner ( 1967) there were no tions. significant differences in metabolism between They also reported no differences in absorp- white and black-dyed animals when the arti- tivity or emissivity between black and white ficial sun was off, thus suggesting that the swine in wavelengths beyond 3 p. They con- dye did not affect the insulative properties of cluded that black and white animals in the the feathers. shade would have the same rate of radiative Svihla (1956) measured the food consump- heat exchange, but that black animals would tion of white and black-dyed rats at 25°C and absorb more than white animals when in the 5°C. He found no significant difference be- sun. Their discussion was aimed at consider- tween the two, and concluded that color had ing the problems of heat load upon animals in no effect on heat loss. hot surroundings, but the same physical prin- It is necessary to reexamine Kirchoffs’ Law ciples apply to low ambient temperatures. to clarify the question of the effect of color Thus it is possible that a black animal might on heat loss. Whereas Kirchoffs’ Law states enjoy an advantage over a white animal dur- that a good absorber is also a good emitter, the ing the daytime by absorbing the relatively law applies only for a particular wavelength. short wavelength energy of the sun, without A good absorber of 2 p wavelength energy is losing the advantage at night, since both black not necessarily a good emitter of 3 p energy. and white animals would radiate longer wave- Thus a visual impression of blackness or white- length energy at the same rate. ness furnishes no information about the emis- Buxton ( 1923) was puzzled by the observa- sivity of the surface in other regions of the tion that the only apparent exceptions to the spectrum. In living animals, the radiant en- rule that desert animals were colored to match ergy that is emitted lies principally in the 4- the background were animals that were col- 20 p region, or the infrared (Hammel 1956). ored black. Craig and Cummings ’ (1962) Emissivity is expressed on a scale from 0.0 study of the effect of solar radiation on humans to 1.0; a surface with an emissivity of 0.0 in the presence of high ambient temperatures absorbs or emits no energy (but reflects all does suggest that exposure to solar radiation METABOLIC SIGNIFICANCE OF ABSORPTION OF RADIANT ENERGY 57

at high temperatures might impose more of a their size ,( crows, vultures, ravens) or because heat load on a black animal than a white ani- of their flocking tendencies (blackbirds, star- mal. This problem might be solved by an lings, mynahs). These factors reduce the ne- examination of the behavior of these animals cessity for a background-matching coloration; under natural conditions. A black animal in and it may be that the energy advantages of- the shade on a very hot day is probably no fered by blackness have resulted in a selection worse off than a white animal, since the radia- for black coloration, rather than grayish or tion component of heat exchange is decreased brownish coloration, in those birds that live in in importance. Also, although the midday climatic conditions where black might be temperatures in desert regions are often so metabolically useful. Where predator pressure hot as to preclude much activity in the open is strong, a neutral, background-matching color sun, the early morning ambient temperatures, will be selected. Cowles (1959) and Cowles when much foraging is often done, especially et al. ( 1967) argue that black is a background by birds, may be below the thermoneutral matching color in dense jungle, but it is diffi- point of the animal, and an advantage might cult to see how black could serve such a func- be gained by maximizing the absorption of tion in more open surroundings, such as the solar energy. typical habitats for blackbirds, crows, and Jaeger (1957) notes that in the Colorado, several other black birds. Desert of North America there is a 16.7”C White birds present different problems with daily difference between maximum and mini- reference to the effects of insolation. A white mum daily temperatures. Cloudsley-Thomp- bird reflects most, although not all, of the son and Chadwick ( 1964) report daily ranges energy in the visible spectrum that falls on of 32.3”C at In Salah, Algeria, and a record it. White or whitish birds would thus be ex- 37.8”C daily range at Bir Mighla, Tripoli. pected to receive a lesser advantage from the Under such conditions, energy expenditure sun than black birds in those cases where might be reduced by adopting a black color to absorption of radiant energy is of value, but capitalize on morning sunlight when the am- also be less subject to high heat loads where bient temperature was below thermoneutrality; insolation is at a high level. then shade could be sought in the middle of Only one experiment has been reported that the day if heat stress became a threat. This relates to the effects of insolation on the en- suggestion might explain the atypical black ergy budget of feral small birds. Morton coloration of desert wheatears and chats noted (1967) observed the feeding behavior of flocks by Buxton. of wild White-crowned Sparrows (Zonatrichia A similar situation may occur in tropical lmc~hys) on sunny and cloudy days in the jungles. Schaller (KM%), in his study on the state of Washington. He noted that on cold, mountain gorilla, notes that the early morning cloudy days there was only a slight decrease temperatures often approached freezing in the in feeding activity during midday, but on highland area, while afternoon temperatures warm sunny days foraging tended to be more were warm. He also states that the black curtailed during midday. Some birds were gorillas are frequent baskers, and, “If gorillas then captured, held in outdoor cages, and their had a religion, they would surely be sun feeding pattern was observed. Their food in- worshippers.” take was significantly less on a sunny morning Black birds in hot non-desert regions do not than on a cloudy morning, although ambient always seek shade during periods of peak temperatures were similar. temperature. I have often seen Brewers’ Black- Finally, Morton compared the feeding pat- birds (Euphagus ~ym~cepha2~~) and Common tern and activity of White-crowned Sparrows Crows (Corvus brachyrhynchos) foraging in irradiated with energy from an infrared sun the sun on days when the ambient tempera- lamp with those which were not. Both groups ture was above 39.4%. Shaded foraging areas were tested under the same ambient tempera- were nearby, but the birds moved from sun to ture conditions, and two test temperatures, shade and back indiscriminately. The birds 20°C and 7°C were used. At 26”C, the were panting, but otherwise showed no ap- feeding pattern of the birds exposed to ’ the parent discomfort. This behavior is a puzzle, infrared was nearly identical to that of the since under those conditions the birds might control birds, and their pattern and total . be expected to be running the risk of a danger- amount of locomotor activity was like that of ously high heat load. the control birds. At 7°C the food intake of Momstblack, or nearly black, birds are rela- the birds exposed to the infrared was relatively tively free from predation, either by virtue of lower than the controls, but again there was 58 FRANK HEPPNER no significant difference in locomotor activity LITERATURE CITED between birds exposed to radiant energy and ADOLPH, E. F., AND G. W. MOLNAR. 1946. Ex- nonirradiated birds. Mortons’ findings indi- changes of heat and tolerances to cold in men cate that insolation can be a significant factor exposed to outdoor weather. Amer. J. Physiol. in the energy metabolism of dark colored, but 146:507-537. non-black, birds. His results are in substantial BARNES, R. B. 1963. Thermography of the human body. Science 1403870-877. agreement with those reported here. BAROTT, H. G., AND E. M. PRINGZE. 1941. Energy Black coloration in birds appears to be a and gaseous metabolism of the hen as affected specialized adaptation that functions to reduce by temperature. J. Nutr. 22:273-286. the energy cost of homeothermy in those situa- BIRKEBAK, R. C. 1966. Heat transfer in biological tions where there is low predator pressure, systems. In W. J. L. Felts and R. J. Harrison [eds.] International review of general and experi- daytime ambient temperatures below thermo- mental zoology. Vol. 2. Academic Press, New neutrality, and sufficient insolation to signifi- York. cantly alter the heat exchange between the BL~, H. F. 1945. The solar heat load: its rela- bird and its environment. Black coloration tionship to total heat load and its relative impor- might also serve a concealing function in cer- tance in the design of clothing. J. Clin. Invest. 24:712-721. tain situations, such as in dense foliage, but BUXTON, P. A. 1923. Animal life in deserts, a study the determination of which of these factors of the fauna in relation to the environment. has guided selection for blackness can only Arnold, London. be made by studying the ecology of a species CLOVDSLEY-THCXMPSON,J. L., AND M. J. CHA~~~K. in question. 1964. Life in deserts. Foulis and Co., London. COTT, H. B. 1957. Adaptive coloration in animals. Methuen and Co., London. SUMMARY COUZES, R. B. 1959. Some ecological factors bear- Hamilton and Heppner (1967) found that ing on the origin and evolution of pigment in black-dyed, white Zebra Finches (Poqhilu the human skin. Amer. Naturalist 93:283-293. COWLES, R. B., W. J. H~TON III, AND F. HEPPNER. mstanotis) demonstrated a 23 per cent meta- 1967. Black pigmentation: adaptation for con- bolic economy over undyed’ birds when both cealment or heat conservation? Science 158: were exposed to artificial sunlight at 10°C. 1340-1341. It is here reported that the difference in ra- CRAIG, F. N., AND E. G. GTJMMINGS.196% Ther- diant energy absorbed between the blackened ma1 influence of sunshine and clothing on men walking in humid heat. J. Appl. Physiol. 17: and white birds in the previous experiment 311318. was sufficient to account for their observed 'GATES, D. M. 1966. Spectral distribution of solar metabolic differences. Spectrum and radio- radiation at the earths surface. Science 151: metric analysis of the light energy absorbed 523-529. HAMILTON, W. J., JR. 1939. American mammals. by the surface of the birds showed that the McGraw-Hill, New York. black birds absorbed 3.1 cal/min more than HAMILTON, W. J. III, AND F. H. HEPPNER. 1967. the white birds while the white birds had a Radiant solar energy and the function of black metabolic heat production 2.7 cal/min greater homeotherm pigmentation: an hypothesis. Sci- ence 155: 196-197. than the black birds. HEEL, J. T. 1956. Infrared of some Temperature measurements made under arctic fauna. J. Mammal. 37:375-378. blackened and undyed white feathers of a live HARDY, J. D. 1939. The radiating power of human skin in the infrared. Amer. J. Physiol. 127:454- Zebra Finch exposed to artificial sunlight sug- 462. gest that the warming of the outer feathers of HARDY, J. D., AND C. MU~CHENHEXM. 1934. The the black bird reduces the temperature gra- radiation of heat from the human body. IV. The dient from the skin of the bird to the surface emission, reflection, and transmission of infra- red radiation bv the human skin. J. Clin. Invest. feathers, and thus slows the loss of metabolic 13:817-831. - heat to cold surroundings. HESSE,R., W. C. ALLEE, AND K. P. SCHMIDT. 1937. Ecological animal geography. J. Wiley and Sons, ACKNOWLEDGMENTS New York. JAEGER, E. C. 1957. The North American deserts. Financial assistance was provided by a National Stanford Univ. Press, Stanford. Science Foundation pre-doctoral fellowship to the KELLY, C. F., T. E. Born,, AND H. HEITMAN. 1954. author. I am indebted to W. J. Hamilton III for The role of thermal radiation in animal ecology. guidance and assistance through the project and to G. Salt for valuable suggestions on temperature mea- Ecology 35:562-568. surement. D. S. Farner provided a critical reading KING, J. R., AND D. S. FARNER. 1961. Energy of the manuscript. This paper is taken in part from metabolism, thermoregulation and body tempera- a dissertation presented to the University of California ture. In A. J, Marshall [ea.] Biology and com- at Davis in partial fulfillment of the requirements for parative physiology of birds. Vol. 2. Academic the Ph.D. Press, New York. METABOLIC SIGNIFICANCE OF ABSORPTION OF RADIANT ENERGY 59

LASIJIWSKI,R. C., AND W. R. DAWSON. 1967. A re- pigmentation on metabolic rate and its possible examination of the relations between standard relationship to body temperature control and metabolic rate and body. weight- in birds. Condor ecological distribution. Ecology 34:610-613. 69: 13-23. SVIHLA, A. 1956. The relation of coloration in LOIIENZ, K. Z. 1935. Der Kumpan in der Umwelt z~~ls to low temperature. J. Mamm. 37: des Vogels. J. Omithol. 83:137-213. MORTON, M. L. 1967. The effects of insolation on TINBERGEN, N. 1948. Social releasers and the ex- the diurnal feeding pattern of White-crowned perimental method required for their study. Wil- Sparrows (Zonotrichia kwmph ys gandelii). son Bull. 60:6-51. Ecology 48: 690-694. THOMPSON, W. R. 1953. The inheritance of be- SCHALLER, G. 1964. The year of the gorilla. Univ. havior; behavioral differences in fifteen mouse of Chicago Press, Chicago. strains. Can. J. Psychol. 7:145-155. STIJLKEN, D. E., AND W. A. HEISTAND. 1953. An experimental study of the influence of pelage Accepted for publication 24 September 1968.