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Loss of body hair, bipedality and thermoregulation. Comments on recent papers in theJournal of Human Evolution
Current events Lia Queiroz do Amaral Department of Applied Physics, Institute of Physics, University of Sa˜o Paulo, C.P. 66318, 05389-970—Sa˜o Paulo, SP, Brazil
Loss of body hair, bipedality and thermoregulation. Comments on recent papers in the Journal of Human Evolution Journal of Human Evolution (1996) 30, 357–366
Introduction A series of papers by Wheeler (1984, 1985, 1990, 1991a,b, 1992a,b, 1993, 1994a) have been published in the Journal of Human Evolution on the subject of the thermoregulatory advantages of hominid bipedalism combined with naked skin and larger body size. The premise of these papers, regarding loss of body hair, is that it occurred only when biped hominids moved to open savanna environments. These papers have already attracted commentary from Dean (1988, 1990), Porter (1993) and very recently Chaplin et al. (1994), with reply by Wheeler (1994b). Although it is widely accepted that naked skin facilitates dissipation of body heat, the circumstances favoring its evolution are quite unclear. The point made in this paper is that although Wheeler’s calculations demonstrate the thermoregulatory advantages of bipedalism over quadrupedalism and of increased body size in savanna environments, the results do not indicate that the initial step in the denudation process occurred in open hot environments, nor that bipedality preceded body-hair reduction. Most of the points analyzed by Wheeler in his detailed calculations had been considered with rougher estimates in an earlier paper by Newman (1970), not mentioned by Wheeler. In his analysis, Newman concluded that ‘‘the obvious time and place where progressive denudation would have been least disadvantageous is the ancient forest habitat’’.
It is argued here that Wheeler’s more detailed calculations give support to such a very early process of denudation and not to its later evolution in equatorial savanna environments. In his first papers (Wheeler, 1984, 1985) Wheeler claimed that ‘‘the lower direct solar radiation fluxes incident upon a biped mammal made possible the reduction of body hair’’.
That is, bipedalism would be pre-adaptive to loss of body hair. But his calculations, regarding estimates of the percentages of total body surface area exposed to direct solar radiation, only showed advantages of bipedalism in relation to quadrupedalism, without any consideration as to the question of denudation. He did not tackle the crucial point: a haired biped could be a better choice regarding thermal stress from direct solar radiation. In later papers (1991a,b, 1992a) arguments supporting the advantages of larger body size and lower water requirements of bipeds are shown in calculations made for haired bipeds and quadrupeds. But no consideration was given to the question of nakedness. It was only in the next paper (1992b) that Wheeler really addressed the question of loss of body hair, making calculations for haired vs. naked bipeds and quadrupeds, crossing the four alternatives. Therefore, focusing on this paper is appropriate. 0047–2484/96/040357+10 $18.00/0
? 1996 Academic Press Limited
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. . Analysis of Wheeler’s (1992b) results
When the thermal budgets of haired and naked hominids in quadrupedal and bipedal postures are compared (Wheeler, 1992b) it is seen that the reduced surface insulation of naked skin increases the rates of both energy gain and loss during respective periods of positive and negative heat load. This means that a naked skin is worse regarding the integral over both day time (it receives more solar energy requiring dissipation) and night time (it requires more endogenous heat production). These results are valid for all ambient temperatures. Wheeler also calculates the thermoregulatory water budgets at increasing levels of metabolic expenditure and states ‘‘It is apparent from the results obtained that there is no simple answer to the question as to whether a naked skin constitutes a net thermoregulatory asset for hominids in savanna conditions . . .’’
He then makes the point that nakedness ‘‘would have both increased the maximum heat load which could be tolerated and, perhaps more importantly, under certain circumstances reduced the drinking water requirements’’.
These two claims regarding advantages of nakedness will be analyzed here in more detail. In Wheeler’s notation (1992b), T200 is the maximum air temperature at a standard height of 200 cm above the ground and Tg is the maximum surface temperature of the 40 cm tall ground vegetation. He considers four T200/Tg regimes (with Tg "T200 =5)C), but here only his results for the two lowest T200 values (30)C and 35)C) will be considered, because nakedness has clear disadvantages when the ambient temperature is higher than body temperature, in open environments. 1. Tolerance of high heat loads The argument of increased tolerance to peak thermal loads by a naked skin in open equatorial conditions is based on the values given by Wheeler for maximum rates of cutaneous evaporative cooling reported for modern haired primates (100 W/m2) in contrast to the maximum rate of heat dissipation of modern humans (in excess of 500 W/m2). The point made here is that the value he takes for haired primates is not adequate for this argument. The maximum known value is the correct value for this comparison: Mahoney (1980) gives for patas monkey running 16 km/h at 53)C an evaporative rate of 0·5 mg H2O/cm2/min, which corresponds to 201 W/m2. Results on both patas monkeys (Mahoney, 1980) and baboons (Rogers et al., 1992) that live in open savanna environment show that heat acclimation and physical fitness are the key points that define the sweating capacity. It is accepted that mechanisms of thermal acclimation to exercise and heat are different (Nadel et al., 1974; Taylor, 1977) and their evolution is still an open question. What comes from results obtained from patas monkeys (Mahoney, 1980) is that the presence of hair is not necessarily such a drawback regarding cutaneous evaporation by sweating. The sweating capacity of these terrestrial open savanna monkeys approaches the sweat rates of humans. Patas are active all day and can run in bright sunlight (Mahoney, 1980). Their sweating capacity at rest is even higher than that of humans (Figure 13 of Mahoney, 1980). They can tolerate heat even at high levels of exercise (three to eight times the resting metabolic rate) and Mahoney (1980) says: ‘‘maximum human sweat rates are about two times higher than patas sweat rates measured in these experiments, which are not necessarily the monkey’s maximum rate’’.
, Table 1
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Integrated peak environmental thermal loads (W.h) of quadrupeds and bipeds for three conditions of skin (naked and fully haired, with thermal conductance of 10 and 5 W/m2/)C) and two ambient temperatures (T200 =30)C and 35)C) Form of locomotion Bipeds
T200 ()C) 30 35
Quadrupeds
30 35
Skin conditions
Integrated peak environmental thermal loads (W.h) and ratio of values for naked and haired 19·9 2·75 118 2·80
36·3 1·50 189 1·75
83·7 2·82 209 2·92
134 1·76 334 1·83
5
10
54·6 330 236 610 Naked
The ratio of values for naked and fully haired are shown in the second lines. Numerical integration (precision 0·5%) from curve values taken from Figures 3 and 4 of Wheeler, 1992b.
The limit of tolerance to exercise has not yet been defined for these haired non-human primates. To sum up, it is reasonable to accept that the sweating capacity of humans is about twice that of furred mammals (Newman, 1970) and not a factor of five as assumed by Wheeler. In extreme conditions, a factor of three is the limit. To make quantitative estimates of total thermal loads (not given explicitly by Wheeler), curves of Figures 3 and 4 of Wheeler 1992b have been reproduced using a scanner and Microsoft Windows on a PC computer, and the integrated peaks of environment thermal loads have been calculated by numerical integration. Results for two ambient temperatures (T200 =30)C and 35)C) are shown in Table 1 for quadrupeds and bipeds, for three conditions of skin: naked and fully haired with thermal conductance of 10 and 5 W/m2/)C. Results in Table 1 show that the environmental thermal load on a naked skin is almost a factor of three higher than for a quadruped or biped better insulated (fully haired, conductance 5). For better insulation the ratio would be even larger. This shows that nakedness gives no real advantage regarding tolerance to peak thermal loads but that the high-sweating capacity of humans essentially compensates the higher thermal loads absorbed by naked skin. A haired animal (quadruped or biped) in an open hot environment should increase its insulation rather than decrease it! That is precisely the trend followed by savanna monkeys, that have a dense hair coat and are much better insulated than forest primates (Mahoney, 1980). The same point was stressed previously by Newman (1970). Further aspects should still be stressed regarding thermal loads: (1) an important point is that wind favors heat dissipation by a naked skin only if the air temperature is lower than body temperature. At air temperatures higher than body temperature wind increases the heat load, especially for a naked person (Cabot Briggs, 1975). (2) No complete analysis is made by Wheeler of the disadvantages of naked skin during the negative thermal load at night. The disadvantage is great in open savanna, where minimum night temperatures drop to 11)C (Hall, 1965). In fact this is the reason why primates living in savanna habitats (like baboons) have developed a large and dense mantle of hair. Patas monkeys can change their conductance
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by a factor of 11 (Mahoney, 1980) to cope with temperature gradients in a savanna. The problem of negative thermal loads at night is minimized by the milder night temperatures of more forested environments. From this analysis it can be concluded that the biological avenue to cope with heat stress in an open environment is to keep a hair covering, increase sweating capacity and have a variable conductance, and not to have a naked skin. Newman’s (1970) conclusion, therefore, remains valid: ‘‘if nakedness was a disadvantage in a savanna environment which required a compensatory adaptation (sweating), loss of hair must have stemmed from other causes or preceded the occupation of the habitat in question, at least for its inception’’.
Newman (1970) also mentions the thermoregulatory advantages of bipedalism, but he does not ascribe its evolution to such advantages. It should be stressed that the only circumstance in which nakedness really favors tolerance of high heat loads is for heat loads without contribution from sun absorption. That is to say, activity in more closed forest conditions. 2. Thermoregulatory drinking water requirements Wheeler’s claim that under certain circumstances nakedness can actually save water is based on his Figures 5 and 6, where curves of water consumption as a function of diurnal metabolic rate are shown for several ambient temperature ranges. He also considers several conditions of the skin: naked and fully haired—this with two levels of efficiency of heat transfer during sweating (80% and 100%) and two values of thermal conductance (10 and 5 W/m2/)C). What these curves indeed show is that, with regard to water requirements, a naked skin is disadvantageous when the ambient temperature is higher than body temperature, but it can be advantageous if the ambient temperature is lower than body temperature. The advantage is greater for a biped than for a quadruped. His figures show that the environment with T200 =30)C is much more favorable to a denudation process than the environment with T200 =35)C. He does not discriminate between these two temperatures as representing two different habitats, and claims instead that his results favor denudation in the open and hot equatorial savanna just saying that ‘‘days with maximum air temperatures between 29–35)C are some of those most typical of the equatorial African savanna’’.
The point made here is that, although there are habitats that can be represented by the continuum 29–35)C, it is worthwhile to go deeper in the analysis considering T200 =30)C and T200 =35)C as two different habitats. T200 =35)C should be associated with an open environment, as the savanna where nowadays baboons and patas monkeys live (Mahoney, 1980). Daytime air temperatures often exceed 36)C during the dry season and night temperatures may drop to 11)C (Hall, 1965). Shadow is rather scarce and sunshine at midday rather stressing (Faniran & Jeje, 1983). This environment is quite similar to Wheeler’s T200 =35)C (although Tg values in savanna may be higher than Wheeler’s estimate). T200 =30)C should be associated with more forested environments, less equatorial latitudes and higher altitudes (Faniran & Jeje, 1983). Summer maxima at daytime are typically around 30)C and night temperatures are seldom below 18)C. Protection from sunshine may be easily found, but not permanent. This environment is more similar to Wheeler’s T200 =30)C (although, Tg values in a forest ambient may be lower than Wheeler’s estimate).
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There is particular interest in making the analysis for these two T200 values in view of recent finds of early hominid fossils: the most recent view (Ruff, 1991; Wheeler, 1993), resulting from a comparison between Australopithecus and early Homo physiques, shows the advantages of Homo regarding thermoregulation in open environments. Ruff (1991) states that African Homo erectus would most likely have been limited to relatively open/dry environments, whereas Australopithecius could have inhabited either open/dry or closed/wet environments. The most recent view is that australopithecines were in fact living not in open savanna but in an environmental mosaic including sub-tropical forest (Rayner et al., 1993; Kingston et al., 1994). Although the actual environment where Australopithecius emerged is highly controversial, it is important to make a detailed analysis discriminating the habitats represented by T200 =30)C and T200 =35)C. A definition of thermoregulatory requirements of these two habitats may lead to clues into the question of whether nakedness evolved at the emergence of Homo or earlier at the emergence of Australopithecus. For a more detailed and quantitative discussion, the results regarding water consumption obtained by Wheeler for these two temperature regimes and for two levels of metabolic expenditure (2 and 3 basal metabolic rates, BMR) are shown in Table 2. Note that 2 BMR corresponds to activities such as locomotion. The values have been extracted from Figures 5 and 6 of Wheeler (1992b) using a scanner and Microsoft Windows in a PC computer. Table 2 is rather detailed and allows the analysis of several different variables: form of locomotion, level of exercise, ambient temperature, and three conditions for the skin: naked or haired, conductance 10 or 5 and efficiency 100 or 80%. Table 2 shows that naked bipeds are the best option at T200 =30)C. At T200 =35)C a fully-haired biped with efficient heat transfer is better at rest and only slightly less favored in activity. A fully haired biped with a conductance larger than 10 W/m2/)C (about 20 W/m2/ )C) and efficient heat transfer would be a better choice regarding water requirements at T200 =35)C even in activity. Patas monkeys, that live in such hot environments, are able to change their conductance as a function of temperature and level of exercise from a minimum value of 1·9 W/m2/)C for temperatures below 18)C up to a maximum value of 25 W/m2/)C for running at temperatures above 40)C (Figure 12, Mahoney, 1980). It can be infered that in a hot open environment (T200 =35)C) a haired biped (with good heat acclimation) would be a better choice in what regards thermoregulatory water requirements. Wheeler’s results do show that naked bipeds could enter hot open spaces; but they do not indicate that nakedness evolved in such conditions. To extract the maximum information from data in Table 2, analysis of one variable at a time was made. Table 3 shows the effect of change in conductance. There is a cross-over for better values of conductance as a function of both T200 and level of activity. This can also be seen directly in Wheeler’s Figures 5 and 6: there is an inversion in the curves for the two conductance values as T200 increases. Better insulation is favored in higher T200 and lower activity. A variable conductance is essential for thermoregulation, and that seems to be the essential factor for survival in hot environments. Patas monkeys are a typical example of this importance (Mahoney, 1980). The effect of change in T200 is shown in Table 4. Ratios of water consumption show that moving from a habitat with T200 =30)C to a habitat with T200 =35)C means penalties for everybody, but: highest penalties are for naked bipeds at rest (increase of 116% in water consumption); lowest penalties are for haired (bipeds or quadrupeds) at higher activity level, with efficient heat transfer and better insulation (increase of about 20% in water consumption).
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362 Table 2
Values of diurnal water consumption (kg/12 h) taken from Figures 5 and 6 of Wheeler, 1992b for quadrupeds and bipeds in two ambient temperatures T200 and two levels of metabolic expenditure (Metabolic expenditure—in units of basal metabolic rate (BMR).
Locomotion Quadrupeds
Metabolic T200 expenditure ()C) (in BMR) 30 35
Bipeds
30 35
Diurnal water consumption (kg/12 h)
2·0 3·0 2·0 3·0
1·16 1·61 1·83 2·36
1·11 1·70 1·53 2·19
1·14 1·83 1·45 2·18
1·37 2·10 1·92 2·76
1·42 2·30 1·81 2·73
2·0 3·0 2·0 3·0
0·62 1·02 1·34 1·87
0·82 1·41 1·26 1·93
0·94 1·65 1·26 2·00
1·03 1·79 1·60 2·42
1·19 2·08 1·59 2·50
Skin conditions*
Naked
Fully Fully Fully Fully haired haired haired haired 100% 100% 80% 80% 10 5 10 5
*Five different conditions for the skin are considered: naked and fully haired (H), with two levels of efficiencies of heat transfer during sweating (80% and 100%) and two values of thermal conductance (10 and 5 W/m2/)C).
Table 3
Effect of variation in conductance of haired skin: values for diurnal water consumption for 10 W/m2/)C divided by values for 5 W/m2/)C
Locomotion
T200 ()C)
Quadrupeds
30 35
Bipeds
30 35
Metabolic expenditure (in BMR)
Haired 100%*
Haired 80%†
2·0 3·0 2·0 3·0
0·97 0·93 1·05 1·00
0·96 0·91 1·06 1·01
2·0 3·0 2·0 3·0
0·87 0·85 1·00 0·96
0·86 0·86 1·01 0·97
*Fully haired with 100% efficiency of heat transfer during sweating. †Fully haired with 80% efficiency of heat transfer during sweating. Ratios larger than one favor more insulation, while ratios smaller than one favor less insulation.
This means essentially that it would be easier for an active haired quadruped than for a naked biped to change from a habitat with T200 =30)C to a habitat with T200 =35)C. Another interesting result is obtained considering a transition from quadrupeds at T200 =30)C to bipeds at T200 =35)C. Ratios are given in Table 5, and show that such
, Table 4
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Effect of variation in ambient temperature: values of diurnal water consumption at T200 =35)C divided by values at T200 =30)C Fully haired
Metabolic expenditure (in BMR)
Naked
100%* 10
100%† 5
80%‡ 10
80%§ 5
Quadrupeds
2·0 3·0
1·55 1·47
1·38 1·29
1·27 1·19
1·40 1·31
1·27 1·19
Bipeds
2·0 3·0
2·16 1·83
1·54 1·37
1·34 1·21
1·55 1·35
1·34 1·20
Locomotion
*Fully haired with 100% efficiency of heat transfer during sweating and 10 W/m2/)C thermal conductance. †Fully haired with 100% efficiency of heat transfer and 5 W/m2/)C thermal conductance. ‡Fully haired, 80% efficiency and 10 W/m2/)C thermal conductance. §Fully haired, 80% efficiency and 5 W/m2/)C thermal conductance. Ratios larger than unity express the penalties for a change to a hotter habitat. BMR, basal metabolic rate.
Table 5
Values of diurnal water consumption for bipeds at T200 =35)C divided by values for quadrupeds at T200 =30)C Metabolic expenditure (in BMR) 2·0 3·0
Fully haired Naked
100%* 10
100% 5
80% 10
80% 5
1·15 1·16
1·13 1·13
1·10 1·09
1·17 1·15
1·12 1·09
*For explanation see Table 4. BMR, basal metabolic rate. Ratios larger than unity express the penalties for the transition to a hotter habitat
transition has penalties for all skin options, but that the smallest penalty is for a fully haired animal with better efficiency of heat transfer and better insulation. Again, a haired biped would be a better choice at T200 =35)C even regarding water requirements. The only circumstance in which nakedness is favored is for denudation in the T200 =30)C habitat. The advantage is larger for bipeds, but it also exists for quadrupeds in activity, as can be seen not only from the tables presented here, but also directly from Figure 5 of Wheeler (1992b). For T200 =30)C the curves of water consumption for naked and haired quadrupeds cross slightly above 2 BMR, favoring nakedness at even moderate activity levels. It is also possible to analyze the more probable way for a ‘‘haired quadruped’’ to reach the ‘‘naked biped’’ stage. The intermediate form favored would be the one having more advantages from the initial stage. By dividing the water consumption requirements of a ‘‘naked quadruped’’ by those of a ‘‘haired biped’’, it is possible to measure whether nakedness or bipedality would be the first favored by water requirements, and, therefore, whether nakedness would precede or follow
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364 Table 6
Adaptive advantages of intermediate forms. Values of water requirements of naked quadrupeds divided by those of haired bipeds Fully haired
Metabolic expenditure (in BMR)
100% 10
100% 5
80% 10
80% 5
30
2·0 3·0
1·41 1·14
1·23 0·98
1·13 0·90
0·97 0·77
35
2·0 3·0
1·45 1·22
1·45 1·18
1·14 0·97
1·15 0·94
T200 ()C)
BMR, basal metabolic rate. Ratios smaller than 1 favor nakedness before bipedality while ratios larger than 1 favor bipedality before nakedness.
bipedality. Results are shown in Table 6. Values smaller than unity favor nakedness before bipedality, whereas values larger than unity favor bipedality first. These results are indeed interesting. Bipedality is favored more for lower activity levels, higher T200 and 100% efficiency of heat transfer, in open environments. However, in such conditions, as shown before, nakedness would not be favored afterwards, and haired bipeds are a better solution. In the only circumstance in which nakedness is clearly favored (T200 =30)C), two possibilities appear from Table 6: (1) At lower levels of activity, bipedality would evolve first (for haired animals with 100% efficiency of heat transfer) and nakedness would follow, as proposed by Wheeler (1992b). However there is a problem with this result. This solution is best for lower levels of activity, whereas all Wheeler’s arguments refer to higher levels of activity. (2) At higher levels of activity, a first step toward naked quadrupeds is favored, particularly for well insulated haired quadrupeds with a lower level of efficiency of heat transfer (23% advantage for nakedness before bipedality). Such lower efficiency would be expected for a haired quadruped not accustomed yet to heat stress, and also for a more humid habitat. This second possibility (not considered by Wheeler) appears even for the open ambient conditions modelled by Wheeler. The advantages for a naked quadruped would be even greater in a more closed habitat, with thermal loads resulting from endogenous metabolism (higher levels of activity) and not to sun absorption. In such, more closed environments, the advantages of bipedality regarding thermoregulation would be much smaller, because they appear only under direct exposure to the sun. This second possibility is the one deserving further exploration, because it corresponds more closely to the initial stage of evolution, as proposed previously by Newman (1970). Results presented here show that the avenue to nakedness was open for active quadrupeds living in a not very hot habitat, before bidedality. Wheeler’s contention that bipedality was the pre-adaptation necessary for nakedness is not supported by his own results. Body hair reduction pre-adaptive to bipedalism was proposed in a previous paper (Amaral, 1989), where the analysis of reproductive success has shown that the evolution of nakedness would result in bipedalism, through a direct impact on fitness, as measured by the number of
,
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progeny. From available data it was estimated that a body-hair reduction responsible for a decrease of 15% in infant survival probability (falls from the mother because of inefficient clinging) in relation to apes would be enough to start favoring bipedalism through the strong selective pressure of infant carrying. This proposal is highly controversial, but it cannot be dismissed and it could explain the inexistence of both naked quadrupeds (favoured in a more forested habitat with T200 =30)C) and haired bipeds (favoured in a more open habitat with T200 =35)C). It should be stressed further that Wheeler’s calculation for ‘‘naked’’ refers in fact to a partial denudation, because his model keeps hair on the upper shoulders, totaling 15% of the body surface, but in a region directly exposed to sun in a naked skin. There is no indication that this was the pattern followed philogenetically. Complete nakedness is more disadvantageous than shown in his results for T200 =35)C and less advantageous than shown in his results for T200 =30)C, in an open ambient. It is also more disadvantageous regarding peaks of environmental thermal loads. In his 1994a paper, Wheeler shows that a naked skin would be most advantageous if hominids retreated to the shade during the hottest hours in open environments. The point to be made here is that these results can be interpreted also favoring evolution of naked skin in a more forested habitat. Conclusions Wheeler’s work did made the point that nakedness has thermoregulatory advantages regarding water comsumption at T200 =30)C. However this is interpreted here as suggesting that nakedness evolved in a more forested environment, and possibly, before or together with bipedality, not after it. It is important to determine with more precision the conditions in which thermoregulatory requirements would allow the evolution of nakedness, even if not being necessarily the drive force for its evolution. Wheeler’s methodology should be extended to focus on the variables ‘‘humidity’’ and ‘‘degree of lightness’’ for complete nakedness, and also allowing Tg
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. . Acknowledgements
I thank Dr Karen Rosenberg for discussions and help in retrieval of pertinent bibliography and, particularly, for bringing Newman’s paper to my attention. The referees and the Editor Professor L. Aiello are also acknowledged for comments that contributed to improve the revised paper. References Amaral, L. Q. (1989). Early hominid physical evolution. Hum. Evol. 4, 33–44. Cabot Briggs, L. (1975). Environment and human adaptation in the Sahara. In (A. Damon, Ed.) Physiological Anthropology, pp. 93–129. New York: Oxford University Press. Chaplin, G., Jablonski, N. G. & Cable, N. T. (1994). Physiology, thermo-regulation and bipedalism. J. hum. Evol. 27, 497–510. Dean, M. C. (1988). Another look at the nose and functional significance of the face and nasal mucous membrane for cooling the brain in fossil hominids. J. hum. Evol. 17, 715–718. Dean, M. C. (1990). More on cool heads. Reply to Wheeler. J. hum. Evol. 19, 323–325. Faniran, A. & Jeje, L. K. (1983). Humid Tropical Geomorphology. London: Longman. Hall, K. R. L. (1965). Behavior and ecology of the wild patas monkey, Erytrocebus patas in Uganda. J. Zool. 148, 15–87. Kingston, J. D., Marino, B. D. & Hill, A. (1994). Isotopic evidence for neogene hominid paleoenvironments in the Kenya Rift valley. Science 264, 955–959. Mahoney, S. (1980). Cost of locomotion and heat balance during rest and running from 0 to 55)C in a patas monkey. J. Appl. Physiol. 49, 789–800. Nadel, E. R., Pandolf, K. B., Roberts, M. F. & Stolwijk, J. A. J. (1974). Mechanisms of thermal acclimation to exercise and heat. J. Appl. Physiol. 37, 515–520. Newman, R. (1970). Why man is such a sweaty and thirsty naked animal: a speculative review. Hum. Biol. 42, 12–27. Porter, A. M. W. (1993). Sweat and thermoregulation in hominids. Comments prompted by the publications of P. E. Wheeler 1984–1993. J. hum. Evol. 25, 417–423. Rayner, R. J., Moon, B. P. & Masters, J. C. (1993). The Makapansgat australopithecine environment. J. hum. Evol. 24, 219–231. Rogers, W. R., Coelho, A. M., Jr., Carey, K. D., Ivy, J. L., Shade, R. E. & Easley, S. P. (1992). Conditioned exercise method for use with nonhuman primates. Am. J. Primatol. 27, 215–224. Ruff, C. B. (1991). Climate and body shape in hominid evolution. J. hum. Evol. 21, 81–105. Taylor, C. R. (1977). Exercise and environmental heat loads: different mechanisms for solving different problems? In (D. Robertshaw, Ed.) International Reviews of Physiology—Environment Physiology II—Vol. 15. Chapter 4. Baltimore: University Park Press, pp. 119–146. Wheeler, P. E. (1984). The evolution of bipedality and loss of functional body hair in hominids. J. hum. Evol. 13, 91–98. Wheeler, P. E. (1985). The loss of functional body hair in man: the influence of thermal environment, body form and bipedality. J. hum. Evol. 14, 23–28. Wheeler, P. E. (1990). The significance of selective brain cooling in hominids. J. hum. Evol. 19, 321–322. Wheeler, P. E. (1991a). The thermoregulatory advantages of hominid bipedalism in open equatorial environments: the contribution of increased convective heat loss and cutaneous evaporative cooling. J. hum. Evol. 21, 107–115. Wheeler, P. E. (1991b). The influence of bipedalism on the energy and water budgets of early hominids. J. hum. Evol. 21, 117–136. Wheeler, P. E. (1992a). The thermoregulatory advantages of large body size for hominids foraging in savanna environments. J. hum. Evol. 23, 351–362. Wheller, P. E. (1992b). The influence of the loss of functional body hair on the water budgets of early hominids. J. hum. Evol. 23, 379–388. Wheeler, P. E. (1993). The influence of stature and body form on hominid energy and water budgets; a comparison of Australopithecus and early Homo physiques. J. hum. Evol. 24, 13–28. Wheeler, P. E. (1994a). The thermoregulatory advantages of heat storage and shade seeking behaviour to hominids foraging in equatorial savanna environments. J. hum. Evol. 26, 339–350. Wheeler, P. E. (1994b). The foraging times of bipedal and quadrupedal hominids in open equatorial environments (a reply to Chaplin, Jablonski & Cable, 1994). J. hum. Evol. 27, 511–517.
Loss of body hair, bipedality and thermoregulation. Comments on recent papers in the Journal of Human Evolution Journal of Human Evolution (1996) 30, 357–366
Introduction A series of papers by Wheeler (1984, 1985, 1990, 1991a,b, 1992a,b, 1993, 1994a) have been published in the Journal of Human Evolution on the subject of the thermoregulatory advantages of hominid bipedalism combined with naked skin and larger body size. The premise of these papers, regarding loss of body hair, is that it occurred only when biped hominids moved to open savanna environments. These papers have already attracted commentary from Dean (1988, 1990), Porter (1993) and very recently Chaplin et al. (1994), with reply by Wheeler (1994b). Although it is widely accepted that naked skin facilitates dissipation of body heat, the circumstances favoring its evolution are quite unclear. The point made in this paper is that although Wheeler’s calculations demonstrate the thermoregulatory advantages of bipedalism over quadrupedalism and of increased body size in savanna environments, the results do not indicate that the initial step in the denudation process occurred in open hot environments, nor that bipedality preceded body-hair reduction. Most of the points analyzed by Wheeler in his detailed calculations had been considered with rougher estimates in an earlier paper by Newman (1970), not mentioned by Wheeler. In his analysis, Newman concluded that ‘‘the obvious time and place where progressive denudation would have been least disadvantageous is the ancient forest habitat’’.
It is argued here that Wheeler’s more detailed calculations give support to such a very early process of denudation and not to its later evolution in equatorial savanna environments. In his first papers (Wheeler, 1984, 1985) Wheeler claimed that ‘‘the lower direct solar radiation fluxes incident upon a biped mammal made possible the reduction of body hair’’.
That is, bipedalism would be pre-adaptive to loss of body hair. But his calculations, regarding estimates of the percentages of total body surface area exposed to direct solar radiation, only showed advantages of bipedalism in relation to quadrupedalism, without any consideration as to the question of denudation. He did not tackle the crucial point: a haired biped could be a better choice regarding thermal stress from direct solar radiation. In later papers (1991a,b, 1992a) arguments supporting the advantages of larger body size and lower water requirements of bipeds are shown in calculations made for haired bipeds and quadrupeds. But no consideration was given to the question of nakedness. It was only in the next paper (1992b) that Wheeler really addressed the question of loss of body hair, making calculations for haired vs. naked bipeds and quadrupeds, crossing the four alternatives. Therefore, focusing on this paper is appropriate. 0047–2484/96/040357+10 $18.00/0
? 1996 Academic Press Limited
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. . Analysis of Wheeler’s (1992b) results
When the thermal budgets of haired and naked hominids in quadrupedal and bipedal postures are compared (Wheeler, 1992b) it is seen that the reduced surface insulation of naked skin increases the rates of both energy gain and loss during respective periods of positive and negative heat load. This means that a naked skin is worse regarding the integral over both day time (it receives more solar energy requiring dissipation) and night time (it requires more endogenous heat production). These results are valid for all ambient temperatures. Wheeler also calculates the thermoregulatory water budgets at increasing levels of metabolic expenditure and states ‘‘It is apparent from the results obtained that there is no simple answer to the question as to whether a naked skin constitutes a net thermoregulatory asset for hominids in savanna conditions . . .’’
He then makes the point that nakedness ‘‘would have both increased the maximum heat load which could be tolerated and, perhaps more importantly, under certain circumstances reduced the drinking water requirements’’.
These two claims regarding advantages of nakedness will be analyzed here in more detail. In Wheeler’s notation (1992b), T200 is the maximum air temperature at a standard height of 200 cm above the ground and Tg is the maximum surface temperature of the 40 cm tall ground vegetation. He considers four T200/Tg regimes (with Tg "T200 =5)C), but here only his results for the two lowest T200 values (30)C and 35)C) will be considered, because nakedness has clear disadvantages when the ambient temperature is higher than body temperature, in open environments. 1. Tolerance of high heat loads The argument of increased tolerance to peak thermal loads by a naked skin in open equatorial conditions is based on the values given by Wheeler for maximum rates of cutaneous evaporative cooling reported for modern haired primates (100 W/m2) in contrast to the maximum rate of heat dissipation of modern humans (in excess of 500 W/m2). The point made here is that the value he takes for haired primates is not adequate for this argument. The maximum known value is the correct value for this comparison: Mahoney (1980) gives for patas monkey running 16 km/h at 53)C an evaporative rate of 0·5 mg H2O/cm2/min, which corresponds to 201 W/m2. Results on both patas monkeys (Mahoney, 1980) and baboons (Rogers et al., 1992) that live in open savanna environment show that heat acclimation and physical fitness are the key points that define the sweating capacity. It is accepted that mechanisms of thermal acclimation to exercise and heat are different (Nadel et al., 1974; Taylor, 1977) and their evolution is still an open question. What comes from results obtained from patas monkeys (Mahoney, 1980) is that the presence of hair is not necessarily such a drawback regarding cutaneous evaporation by sweating. The sweating capacity of these terrestrial open savanna monkeys approaches the sweat rates of humans. Patas are active all day and can run in bright sunlight (Mahoney, 1980). Their sweating capacity at rest is even higher than that of humans (Figure 13 of Mahoney, 1980). They can tolerate heat even at high levels of exercise (three to eight times the resting metabolic rate) and Mahoney (1980) says: ‘‘maximum human sweat rates are about two times higher than patas sweat rates measured in these experiments, which are not necessarily the monkey’s maximum rate’’.
, Table 1
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Integrated peak environmental thermal loads (W.h) of quadrupeds and bipeds for three conditions of skin (naked and fully haired, with thermal conductance of 10 and 5 W/m2/)C) and two ambient temperatures (T200 =30)C and 35)C) Form of locomotion Bipeds
T200 ()C) 30 35
Quadrupeds
30 35
Skin conditions
Integrated peak environmental thermal loads (W.h) and ratio of values for naked and haired 19·9 2·75 118 2·80
36·3 1·50 189 1·75
83·7 2·82 209 2·92
134 1·76 334 1·83
5
10
54·6 330 236 610 Naked
The ratio of values for naked and fully haired are shown in the second lines. Numerical integration (precision 0·5%) from curve values taken from Figures 3 and 4 of Wheeler, 1992b.
The limit of tolerance to exercise has not yet been defined for these haired non-human primates. To sum up, it is reasonable to accept that the sweating capacity of humans is about twice that of furred mammals (Newman, 1970) and not a factor of five as assumed by Wheeler. In extreme conditions, a factor of three is the limit. To make quantitative estimates of total thermal loads (not given explicitly by Wheeler), curves of Figures 3 and 4 of Wheeler 1992b have been reproduced using a scanner and Microsoft Windows on a PC computer, and the integrated peaks of environment thermal loads have been calculated by numerical integration. Results for two ambient temperatures (T200 =30)C and 35)C) are shown in Table 1 for quadrupeds and bipeds, for three conditions of skin: naked and fully haired with thermal conductance of 10 and 5 W/m2/)C. Results in Table 1 show that the environmental thermal load on a naked skin is almost a factor of three higher than for a quadruped or biped better insulated (fully haired, conductance 5). For better insulation the ratio would be even larger. This shows that nakedness gives no real advantage regarding tolerance to peak thermal loads but that the high-sweating capacity of humans essentially compensates the higher thermal loads absorbed by naked skin. A haired animal (quadruped or biped) in an open hot environment should increase its insulation rather than decrease it! That is precisely the trend followed by savanna monkeys, that have a dense hair coat and are much better insulated than forest primates (Mahoney, 1980). The same point was stressed previously by Newman (1970). Further aspects should still be stressed regarding thermal loads: (1) an important point is that wind favors heat dissipation by a naked skin only if the air temperature is lower than body temperature. At air temperatures higher than body temperature wind increases the heat load, especially for a naked person (Cabot Briggs, 1975). (2) No complete analysis is made by Wheeler of the disadvantages of naked skin during the negative thermal load at night. The disadvantage is great in open savanna, where minimum night temperatures drop to 11)C (Hall, 1965). In fact this is the reason why primates living in savanna habitats (like baboons) have developed a large and dense mantle of hair. Patas monkeys can change their conductance
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by a factor of 11 (Mahoney, 1980) to cope with temperature gradients in a savanna. The problem of negative thermal loads at night is minimized by the milder night temperatures of more forested environments. From this analysis it can be concluded that the biological avenue to cope with heat stress in an open environment is to keep a hair covering, increase sweating capacity and have a variable conductance, and not to have a naked skin. Newman’s (1970) conclusion, therefore, remains valid: ‘‘if nakedness was a disadvantage in a savanna environment which required a compensatory adaptation (sweating), loss of hair must have stemmed from other causes or preceded the occupation of the habitat in question, at least for its inception’’.
Newman (1970) also mentions the thermoregulatory advantages of bipedalism, but he does not ascribe its evolution to such advantages. It should be stressed that the only circumstance in which nakedness really favors tolerance of high heat loads is for heat loads without contribution from sun absorption. That is to say, activity in more closed forest conditions. 2. Thermoregulatory drinking water requirements Wheeler’s claim that under certain circumstances nakedness can actually save water is based on his Figures 5 and 6, where curves of water consumption as a function of diurnal metabolic rate are shown for several ambient temperature ranges. He also considers several conditions of the skin: naked and fully haired—this with two levels of efficiency of heat transfer during sweating (80% and 100%) and two values of thermal conductance (10 and 5 W/m2/)C). What these curves indeed show is that, with regard to water requirements, a naked skin is disadvantageous when the ambient temperature is higher than body temperature, but it can be advantageous if the ambient temperature is lower than body temperature. The advantage is greater for a biped than for a quadruped. His figures show that the environment with T200 =30)C is much more favorable to a denudation process than the environment with T200 =35)C. He does not discriminate between these two temperatures as representing two different habitats, and claims instead that his results favor denudation in the open and hot equatorial savanna just saying that ‘‘days with maximum air temperatures between 29–35)C are some of those most typical of the equatorial African savanna’’.
The point made here is that, although there are habitats that can be represented by the continuum 29–35)C, it is worthwhile to go deeper in the analysis considering T200 =30)C and T200 =35)C as two different habitats. T200 =35)C should be associated with an open environment, as the savanna where nowadays baboons and patas monkeys live (Mahoney, 1980). Daytime air temperatures often exceed 36)C during the dry season and night temperatures may drop to 11)C (Hall, 1965). Shadow is rather scarce and sunshine at midday rather stressing (Faniran & Jeje, 1983). This environment is quite similar to Wheeler’s T200 =35)C (although Tg values in savanna may be higher than Wheeler’s estimate). T200 =30)C should be associated with more forested environments, less equatorial latitudes and higher altitudes (Faniran & Jeje, 1983). Summer maxima at daytime are typically around 30)C and night temperatures are seldom below 18)C. Protection from sunshine may be easily found, but not permanent. This environment is more similar to Wheeler’s T200 =30)C (although, Tg values in a forest ambient may be lower than Wheeler’s estimate).
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There is particular interest in making the analysis for these two T200 values in view of recent finds of early hominid fossils: the most recent view (Ruff, 1991; Wheeler, 1993), resulting from a comparison between Australopithecus and early Homo physiques, shows the advantages of Homo regarding thermoregulation in open environments. Ruff (1991) states that African Homo erectus would most likely have been limited to relatively open/dry environments, whereas Australopithecius could have inhabited either open/dry or closed/wet environments. The most recent view is that australopithecines were in fact living not in open savanna but in an environmental mosaic including sub-tropical forest (Rayner et al., 1993; Kingston et al., 1994). Although the actual environment where Australopithecius emerged is highly controversial, it is important to make a detailed analysis discriminating the habitats represented by T200 =30)C and T200 =35)C. A definition of thermoregulatory requirements of these two habitats may lead to clues into the question of whether nakedness evolved at the emergence of Homo or earlier at the emergence of Australopithecus. For a more detailed and quantitative discussion, the results regarding water consumption obtained by Wheeler for these two temperature regimes and for two levels of metabolic expenditure (2 and 3 basal metabolic rates, BMR) are shown in Table 2. Note that 2 BMR corresponds to activities such as locomotion. The values have been extracted from Figures 5 and 6 of Wheeler (1992b) using a scanner and Microsoft Windows in a PC computer. Table 2 is rather detailed and allows the analysis of several different variables: form of locomotion, level of exercise, ambient temperature, and three conditions for the skin: naked or haired, conductance 10 or 5 and efficiency 100 or 80%. Table 2 shows that naked bipeds are the best option at T200 =30)C. At T200 =35)C a fully-haired biped with efficient heat transfer is better at rest and only slightly less favored in activity. A fully haired biped with a conductance larger than 10 W/m2/)C (about 20 W/m2/ )C) and efficient heat transfer would be a better choice regarding water requirements at T200 =35)C even in activity. Patas monkeys, that live in such hot environments, are able to change their conductance as a function of temperature and level of exercise from a minimum value of 1·9 W/m2/)C for temperatures below 18)C up to a maximum value of 25 W/m2/)C for running at temperatures above 40)C (Figure 12, Mahoney, 1980). It can be infered that in a hot open environment (T200 =35)C) a haired biped (with good heat acclimation) would be a better choice in what regards thermoregulatory water requirements. Wheeler’s results do show that naked bipeds could enter hot open spaces; but they do not indicate that nakedness evolved in such conditions. To extract the maximum information from data in Table 2, analysis of one variable at a time was made. Table 3 shows the effect of change in conductance. There is a cross-over for better values of conductance as a function of both T200 and level of activity. This can also be seen directly in Wheeler’s Figures 5 and 6: there is an inversion in the curves for the two conductance values as T200 increases. Better insulation is favored in higher T200 and lower activity. A variable conductance is essential for thermoregulation, and that seems to be the essential factor for survival in hot environments. Patas monkeys are a typical example of this importance (Mahoney, 1980). The effect of change in T200 is shown in Table 4. Ratios of water consumption show that moving from a habitat with T200 =30)C to a habitat with T200 =35)C means penalties for everybody, but: highest penalties are for naked bipeds at rest (increase of 116% in water consumption); lowest penalties are for haired (bipeds or quadrupeds) at higher activity level, with efficient heat transfer and better insulation (increase of about 20% in water consumption).
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362 Table 2
Values of diurnal water consumption (kg/12 h) taken from Figures 5 and 6 of Wheeler, 1992b for quadrupeds and bipeds in two ambient temperatures T200 and two levels of metabolic expenditure (Metabolic expenditure—in units of basal metabolic rate (BMR).
Locomotion Quadrupeds
Metabolic T200 expenditure ()C) (in BMR) 30 35
Bipeds
30 35
Diurnal water consumption (kg/12 h)
2·0 3·0 2·0 3·0
1·16 1·61 1·83 2·36
1·11 1·70 1·53 2·19
1·14 1·83 1·45 2·18
1·37 2·10 1·92 2·76
1·42 2·30 1·81 2·73
2·0 3·0 2·0 3·0
0·62 1·02 1·34 1·87
0·82 1·41 1·26 1·93
0·94 1·65 1·26 2·00
1·03 1·79 1·60 2·42
1·19 2·08 1·59 2·50
Skin conditions*
Naked
Fully Fully Fully Fully haired haired haired haired 100% 100% 80% 80% 10 5 10 5
*Five different conditions for the skin are considered: naked and fully haired (H), with two levels of efficiencies of heat transfer during sweating (80% and 100%) and two values of thermal conductance (10 and 5 W/m2/)C).
Table 3
Effect of variation in conductance of haired skin: values for diurnal water consumption for 10 W/m2/)C divided by values for 5 W/m2/)C
Locomotion
T200 ()C)
Quadrupeds
30 35
Bipeds
30 35
Metabolic expenditure (in BMR)
Haired 100%*
Haired 80%†
2·0 3·0 2·0 3·0
0·97 0·93 1·05 1·00
0·96 0·91 1·06 1·01
2·0 3·0 2·0 3·0
0·87 0·85 1·00 0·96
0·86 0·86 1·01 0·97
*Fully haired with 100% efficiency of heat transfer during sweating. †Fully haired with 80% efficiency of heat transfer during sweating. Ratios larger than one favor more insulation, while ratios smaller than one favor less insulation.
This means essentially that it would be easier for an active haired quadruped than for a naked biped to change from a habitat with T200 =30)C to a habitat with T200 =35)C. Another interesting result is obtained considering a transition from quadrupeds at T200 =30)C to bipeds at T200 =35)C. Ratios are given in Table 5, and show that such
, Table 4
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Effect of variation in ambient temperature: values of diurnal water consumption at T200 =35)C divided by values at T200 =30)C Fully haired
Metabolic expenditure (in BMR)
Naked
100%* 10
100%† 5
80%‡ 10
80%§ 5
Quadrupeds
2·0 3·0
1·55 1·47
1·38 1·29
1·27 1·19
1·40 1·31
1·27 1·19
Bipeds
2·0 3·0
2·16 1·83
1·54 1·37
1·34 1·21
1·55 1·35
1·34 1·20
Locomotion
*Fully haired with 100% efficiency of heat transfer during sweating and 10 W/m2/)C thermal conductance. †Fully haired with 100% efficiency of heat transfer and 5 W/m2/)C thermal conductance. ‡Fully haired, 80% efficiency and 10 W/m2/)C thermal conductance. §Fully haired, 80% efficiency and 5 W/m2/)C thermal conductance. Ratios larger than unity express the penalties for a change to a hotter habitat. BMR, basal metabolic rate.
Table 5
Values of diurnal water consumption for bipeds at T200 =35)C divided by values for quadrupeds at T200 =30)C Metabolic expenditure (in BMR) 2·0 3·0
Fully haired Naked
100%* 10
100% 5
80% 10
80% 5
1·15 1·16
1·13 1·13
1·10 1·09
1·17 1·15
1·12 1·09
*For explanation see Table 4. BMR, basal metabolic rate. Ratios larger than unity express the penalties for the transition to a hotter habitat
transition has penalties for all skin options, but that the smallest penalty is for a fully haired animal with better efficiency of heat transfer and better insulation. Again, a haired biped would be a better choice at T200 =35)C even regarding water requirements. The only circumstance in which nakedness is favored is for denudation in the T200 =30)C habitat. The advantage is larger for bipeds, but it also exists for quadrupeds in activity, as can be seen not only from the tables presented here, but also directly from Figure 5 of Wheeler (1992b). For T200 =30)C the curves of water consumption for naked and haired quadrupeds cross slightly above 2 BMR, favoring nakedness at even moderate activity levels. It is also possible to analyze the more probable way for a ‘‘haired quadruped’’ to reach the ‘‘naked biped’’ stage. The intermediate form favored would be the one having more advantages from the initial stage. By dividing the water consumption requirements of a ‘‘naked quadruped’’ by those of a ‘‘haired biped’’, it is possible to measure whether nakedness or bipedality would be the first favored by water requirements, and, therefore, whether nakedness would precede or follow
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364 Table 6
Adaptive advantages of intermediate forms. Values of water requirements of naked quadrupeds divided by those of haired bipeds Fully haired
Metabolic expenditure (in BMR)
100% 10
100% 5
80% 10
80% 5
30
2·0 3·0
1·41 1·14
1·23 0·98
1·13 0·90
0·97 0·77
35
2·0 3·0
1·45 1·22
1·45 1·18
1·14 0·97
1·15 0·94
T200 ()C)
BMR, basal metabolic rate. Ratios smaller than 1 favor nakedness before bipedality while ratios larger than 1 favor bipedality before nakedness.
bipedality. Results are shown in Table 6. Values smaller than unity favor nakedness before bipedality, whereas values larger than unity favor bipedality first. These results are indeed interesting. Bipedality is favored more for lower activity levels, higher T200 and 100% efficiency of heat transfer, in open environments. However, in such conditions, as shown before, nakedness would not be favored afterwards, and haired bipeds are a better solution. In the only circumstance in which nakedness is clearly favored (T200 =30)C), two possibilities appear from Table 6: (1) At lower levels of activity, bipedality would evolve first (for haired animals with 100% efficiency of heat transfer) and nakedness would follow, as proposed by Wheeler (1992b). However there is a problem with this result. This solution is best for lower levels of activity, whereas all Wheeler’s arguments refer to higher levels of activity. (2) At higher levels of activity, a first step toward naked quadrupeds is favored, particularly for well insulated haired quadrupeds with a lower level of efficiency of heat transfer (23% advantage for nakedness before bipedality). Such lower efficiency would be expected for a haired quadruped not accustomed yet to heat stress, and also for a more humid habitat. This second possibility (not considered by Wheeler) appears even for the open ambient conditions modelled by Wheeler. The advantages for a naked quadruped would be even greater in a more closed habitat, with thermal loads resulting from endogenous metabolism (higher levels of activity) and not to sun absorption. In such, more closed environments, the advantages of bipedality regarding thermoregulation would be much smaller, because they appear only under direct exposure to the sun. This second possibility is the one deserving further exploration, because it corresponds more closely to the initial stage of evolution, as proposed previously by Newman (1970). Results presented here show that the avenue to nakedness was open for active quadrupeds living in a not very hot habitat, before bidedality. Wheeler’s contention that bipedality was the pre-adaptation necessary for nakedness is not supported by his own results. Body hair reduction pre-adaptive to bipedalism was proposed in a previous paper (Amaral, 1989), where the analysis of reproductive success has shown that the evolution of nakedness would result in bipedalism, through a direct impact on fitness, as measured by the number of
,
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progeny. From available data it was estimated that a body-hair reduction responsible for a decrease of 15% in infant survival probability (falls from the mother because of inefficient clinging) in relation to apes would be enough to start favoring bipedalism through the strong selective pressure of infant carrying. This proposal is highly controversial, but it cannot be dismissed and it could explain the inexistence of both naked quadrupeds (favoured in a more forested habitat with T200 =30)C) and haired bipeds (favoured in a more open habitat with T200 =35)C). It should be stressed further that Wheeler’s calculation for ‘‘naked’’ refers in fact to a partial denudation, because his model keeps hair on the upper shoulders, totaling 15% of the body surface, but in a region directly exposed to sun in a naked skin. There is no indication that this was the pattern followed philogenetically. Complete nakedness is more disadvantageous than shown in his results for T200 =35)C and less advantageous than shown in his results for T200 =30)C, in an open ambient. It is also more disadvantageous regarding peaks of environmental thermal loads. In his 1994a paper, Wheeler shows that a naked skin would be most advantageous if hominids retreated to the shade during the hottest hours in open environments. The point to be made here is that these results can be interpreted also favoring evolution of naked skin in a more forested habitat. Conclusions Wheeler’s work did made the point that nakedness has thermoregulatory advantages regarding water comsumption at T200 =30)C. However this is interpreted here as suggesting that nakedness evolved in a more forested environment, and possibly, before or together with bipedality, not after it. It is important to determine with more precision the conditions in which thermoregulatory requirements would allow the evolution of nakedness, even if not being necessarily the drive force for its evolution. Wheeler’s methodology should be extended to focus on the variables ‘‘humidity’’ and ‘‘degree of lightness’’ for complete nakedness, and also allowing Tg
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. . Acknowledgements
I thank Dr Karen Rosenberg for discussions and help in retrieval of pertinent bibliography and, particularly, for bringing Newman’s paper to my attention. The referees and the Editor Professor L. Aiello are also acknowledged for comments that contributed to improve the revised paper. References Amaral, L. Q. (1989). Early hominid physical evolution. Hum. Evol. 4, 33–44. Cabot Briggs, L. (1975). Environment and human adaptation in the Sahara. In (A. Damon, Ed.) Physiological Anthropology, pp. 93–129. New York: Oxford University Press. Chaplin, G., Jablonski, N. G. & Cable, N. T. (1994). Physiology, thermo-regulation and bipedalism. J. hum. Evol. 27, 497–510. Dean, M. C. (1988). Another look at the nose and functional significance of the face and nasal mucous membrane for cooling the brain in fossil hominids. J. hum. Evol. 17, 715–718. Dean, M. C. (1990). More on cool heads. Reply to Wheeler. J. hum. Evol. 19, 323–325. Faniran, A. & Jeje, L. K. (1983). Humid Tropical Geomorphology. London: Longman. Hall, K. R. L. (1965). Behavior and ecology of the wild patas monkey, Erytrocebus patas in Uganda. J. Zool. 148, 15–87. Kingston, J. D., Marino, B. D. & Hill, A. (1994). Isotopic evidence for neogene hominid paleoenvironments in the Kenya Rift valley. Science 264, 955–959. Mahoney, S. (1980). Cost of locomotion and heat balance during rest and running from 0 to 55)C in a patas monkey. J. Appl. Physiol. 49, 789–800. Nadel, E. R., Pandolf, K. B., Roberts, M. F. & Stolwijk, J. A. J. (1974). Mechanisms of thermal acclimation to exercise and heat. J. Appl. Physiol. 37, 515–520. Newman, R. (1970). Why man is such a sweaty and thirsty naked animal: a speculative review. Hum. Biol. 42, 12–27. Porter, A. M. W. (1993). Sweat and thermoregulation in hominids. Comments prompted by the publications of P. E. Wheeler 1984–1993. J. hum. Evol. 25, 417–423. Rayner, R. J., Moon, B. P. & Masters, J. C. (1993). The Makapansgat australopithecine environment. J. hum. Evol. 24, 219–231. Rogers, W. R., Coelho, A. M., Jr., Carey, K. D., Ivy, J. L., Shade, R. E. & Easley, S. P. (1992). Conditioned exercise method for use with nonhuman primates. Am. J. Primatol. 27, 215–224. Ruff, C. B. (1991). Climate and body shape in hominid evolution. J. hum. Evol. 21, 81–105. Taylor, C. R. (1977). Exercise and environmental heat loads: different mechanisms for solving different problems? In (D. Robertshaw, Ed.) International Reviews of Physiology—Environment Physiology II—Vol. 15. Chapter 4. Baltimore: University Park Press, pp. 119–146. Wheeler, P. E. (1984). The evolution of bipedality and loss of functional body hair in hominids. J. hum. Evol. 13, 91–98. Wheeler, P. E. (1985). The loss of functional body hair in man: the influence of thermal environment, body form and bipedality. J. hum. Evol. 14, 23–28. Wheeler, P. E. (1990). The significance of selective brain cooling in hominids. J. hum. Evol. 19, 321–322. Wheeler, P. E. (1991a). The thermoregulatory advantages of hominid bipedalism in open equatorial environments: the contribution of increased convective heat loss and cutaneous evaporative cooling. J. hum. Evol. 21, 107–115. Wheeler, P. E. (1991b). The influence of bipedalism on the energy and water budgets of early hominids. J. hum. Evol. 21, 117–136. Wheeler, P. E. (1992a). The thermoregulatory advantages of large body size for hominids foraging in savanna environments. J. hum. Evol. 23, 351–362. Wheller, P. E. (1992b). The influence of the loss of functional body hair on the water budgets of early hominids. J. hum. Evol. 23, 379–388. Wheeler, P. E. (1993). The influence of stature and body form on hominid energy and water budgets; a comparison of Australopithecus and early Homo physiques. J. hum. Evol. 24, 13–28. Wheeler, P. E. (1994a). The thermoregulatory advantages of heat storage and shade seeking behaviour to hominids foraging in equatorial savanna environments. J. hum. Evol. 26, 339–350. Wheeler, P. E. (1994b). The foraging times of bipedal and quadrupedal hominids in open equatorial environments (a reply to Chaplin, Jablonski & Cable, 1994). J. hum. Evol. 27, 511–517.