INFLUENCE OF TEMPERATURE ON METABOLISM AND THE PROBLEM O F ACCLIMATIZATION BY N. R. DHAR
It is well known that the temperature of a warm-blooded animal is maintained a t the normal even though the temperatures of the outside environments vary from zero and lower to 30' or 35'. In cold-blooded animals, on the other hand, the temperature of the body is only slightly higher than that of the environment at the time. The metabolism of such animals varies with the temperatures in such a manner that the respiratory exchange almost always rises with the increase in temperature, but generally irregularly and to a very different degree in different animals. The frog in the mud during the winter a t a temperature of 4' has quite a different metabolism from that which he enjoys during the summer sunshine as it sits on the river bank and snaps a t passing flies. Rohrig and Zuntzl first showed that a curarized warm-blooded animal a t ordinary room temperatures lost the power of maintaining its body temperature and that the intensity of metabolism decreased accordingly. Curare prevents the transmission of motor impulses to voluntary muscles. Krogh2 states that the curve of oxygen absorption as influenced by body temperature is the same in the anesthetized frog and fish as in the curarized dog. In warmblooded animals the temperature is maintained a t a constant level independent of the climatic condition and this level is a favorable one for the activity of nerve and muscle. It would indeed be inconvenient were the active life of a man dependent upon the temperature of the environment. The essential mechanism for the regulation of body temperature is nervous. ,In warm-blooded animals a fall in the surrounding temperatures regularly causes not a decrease but an increase in the respiratory exchange, thanks to the mechanism of chemical heat regulation. The most elaborate study of the chemical heat regulation has been made by Rubner3 who obtained the results given in Table I in the case of a guinea pig. TABLEI Temperature of air "C.
COn per Kg. and Hour
Gr.
O0
2.91
I IO
2.15
2 IO
1.77
2 6'
1.54 I .32
30° 3 so 40'
1.27
1.45
Pfliiger's Archiv, 4, 57 (1871). Internat. Z.physik-chem. Biologie, 1, 492 (1914). a "Die Gesetze des Energieverbrauchs bei der Ernahrung" (1902).
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481
At 3 j " the regulation breaks down and the respiratory exchange rises with increase in temperature of the body as seen in the last experiment of the above series. In the foregoing paper1 we have shown that under standard conditions where the effect of nervous influence is excluded increase in temperature causes greater metabolism in both warm and cold blooded animals. After studying a considerable range of animals, Rubner has found that all animals transform nearly the same total amount of energy per kilogram of body weight in the whole period from the birth to the natural death. The mean value of the constant Rubner finds to be 191600 calories, the values for different species ranging from 141091 and 265500 calories. Small animals with an intensive metabolism live a relatively short time; large animals with more sluggish metabolism live a longer time. Rubner's view is that a definite sum of living action or energy transformation determines the physiological end of life. It is Rubner's law that the metabolism is proportional to the superficial area of an animal. Erwin Voit2has calculated the following results, Table 11, for showing the heat production in resisting animals of various sizes a t medium temperatures of the environment :-
TABLE I1 Weight in Kg.
Horse Pig Man Dog Rabbit Goose Fowl Mouse Rabbit (without ears)
441 I28
Calories produced per Sq. $1. Surface Per Kilo 11.3 948 19.1
1078
68.3
32.1
1042
15.2
51.5
1039
2.3 3.5
75.1 66.7
776 969
2.0
71.0
943
212.0
I 188
75.1
917
0.018 2.3
This table supports the generalization of Rubner. Voit shows that the metabolism of the pigeon may be doubled after removing its feathers. From the experiments of Rubner it appears that the presence of adipose tissue acts in the same way as does a warm fur t o extend the range of the physical regulation and to delay the onset of chemical regulation of body temperature. That the range of physical regulation of temperature of a small dog was due to his long hair, is shown by the change in his metabolism after shaving him. Rubner shows this in Table 111. 1
Dhar: Proc. Akad. Wet. Amsterdam. 23, 44 Z. Biologie, 41, 120 (1907).
(1920).
482
N . R. DHAR
TABLE I11 Calories per Kilo. Xormal coat of hair
Temperature 20'
55.9
2 5'
54.2 56.2
30'
Shaved 82.3 61.2 j2 .o
It is clearly seen that this dog lost its power of physical regulation between and 30'. As soon as he lost his covering of hair his metabolism became like that of a guinea pig, increasing with a reduction of temperature from 30' downwards, an illustration of chemical regulation. To determine the influence of the protective layer of fat Rubner investigated the influence of temperature on the metabolism of a fasting short haired dog a t a time when he was emaciated and compared it with the fasting metabolism after the same dog had been fattened, Table IV. 20'
TABLE IV Dog (thin) Temperature Cal. per Kilo. 5.1' 121.3 14.4' 100.9 70.7 23.3' 30.6' 62.0
Same dog (fat) Temperature Cal. per Kilo. 7.3' 120.j 15.5' 83 .o 67.0 22.0' 31.0'. 64.5
It appears from this table that the metabolism of the dog was the same at a low temperature in both cases but that the minimum metabolism was almost reached a t a temperature of 22' when the dog had a protective covering of fat which was not the case when he was thin. The physical regulation may be increased by certain voluntary acts, such as are observed when a dog or man exposed to cold lies down and curls himself up in such a way as to offer as small an exposed surface as possible. The contrast to this is offered when on a hot day the dog lies on his back and extends his legs so as to promote loss of heat. In Table V are Voit's results on the effect of temperature on the metabolism of a fasting man (six hour periods.) TABLE V Temperature 4.4' 6 . jo 9.0' 14.3' 16.2'
CO, excreted in grams
Temperature
201.7
23.7'
206.o
24.2'
192 . o
26.7' 30.0'
1j5.1
COg excreted in grams 164.8 166. 5 160.0 170.6
158.3
Voit believed the increase in metabolism to be a reflex stimulus of cold on the skin which raised the power of muscle cells to metabolise.
4
c
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483
Another factor in the heat regulation of man is clothes. Certain savage races living in cool climates do without clothes, as, for example, aborigines of Tierra del Fuego, who according to the reports of travellers, substituted a covering of oil. In such races the process of “hardening” or development of physical regulation must be carried to a maximum. In civilized countries man endeavors to remove all the influence of chemical regulation by keeping his skin covered. Only about 2 0 7 0 of his surface is normally exposed to the air. The most important constituent of clothes is the air, which is a much worse conductor of heat than is fibre. Two experiments cited by Rubner indicate the effect of clothes on metabolism. An individual was kept a t a temperature of between 11’ and 12’ and wore different clothes a t different times. His COz and water excretion are given in Table VI.
TABLE VI Influence of Clothes on Metabolism in Man a t a Temperature of 11° to I 2 O COZin gram. per hour.
Summer clothes Summer clothes and winter overcoat. Summer clothes and fur coats.
Remarks.
28.4
Cold, occasional shivering
26.9
Chilly part of the time.
23.6
Comfortably warm.
When a man was comfortable the chemical regulation of temperature was eliminated. Fat persons have been directly observed to have a smaller respiratory action than lean ones, Benedict and Smith’ have shown by comparing a number of athletes with normal subjects of similar heights and weights that the metabolism of athletes is on the average distinctly greater than that of nonathletes. While it had often been observed that smaller animals had per unit weight a greater respiratory exchange than larger ones, a quantitative study of the influence of size upon metabolism was first made by Rubner on grown dogs weighing from 30.4 to 3.4 kilograms. Rubner found that the metabolism calculated per kilogram increases regularly with decreasing size. When however the surface of the animal is taken into account a practically constant metabolism per sq. surface was found for all. From experiments on guinea pigs of different age and weights Kettnerz finds that the metabolism per kilogram an hour decreases fairly regularly with increasing weight whilst the differences in the results per sq. meter are independent of size. On the other hand, in a recent discussion Benedict3 denies J. Biol. Chem., 20, 243 (1915). Archiv Physiol., 1909, 447. J. Biol. Chem., 20, 263 (1915).
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N . R. DHAR
that there is any close relationship between size and metabolism and deprecates especially the use of the surface as a basis for comparison. His own figures and charts show, however, that such relationships exist that the metabolism per kg. of the body weight decreases fairly regularly with increasing weight. The surface S of an animal is approximately proportional to the square of a linear dimension e.g. length of the body, while the weight is proportional to the third power of a linear dimension. 7;XTehave therefore S = CW8the constant C has been worked out for different species. It does not vary very much even in forms of very different shapes. For man and also for a dog we have C = 12.3 for the rabbit 12.9, the horse 9.0, the rat 9.1 and the guinea pig 8.9. It is quite possible that the surface as at present defined CW’ does not give the very best agreement in comparisons of different individuals. The main point is that metabolism in warm-blooded animals is not proportional to the weight W but to W” where n is certainly not far from 2/3. On the whole, looking at the problem from a broad point of view, it seems pretty certain that the surface law of Rubner is generally proved as far as the metabolism of warm-blooded animals are concerned. In the following pages, I shall try to find out a physical significance of Rubner’s generalization and other facts regarding the influence of temperature on metabolism in both warm and cold blooded animals. We can look at the problem of metabolism of different warm-blooded animals from the following considerations :The body temperature of warm-blooded animals is normally much (I) higher than the surrounding air. In the case of some birds, sparrow, hen, etc., the body temperature is about 42’. In the case of rabbit it is 39O.6 and in the case of dog it is 3gO.2. (2) Experimental results have shown that radiation is the most important factor in the loss of heat from animal body.. Let us assume that a metallic ball of radius r and density of the material p, is placed in air at say To and we are supplying heat to the ball so that the temperature of the ball may be kept constant a t T where T is greater than To. Now in order to maintain this constant temperature a supply of heat has to be given to the ball, otherwise the body loses heat and cools down to the temperature of the surrounding air (To). From Stefan’s law of radiation, we know that the loss of energy from the surface is equal to 4xy2a(T4 - T o ) , where 4 x y 2 is the surface of the body in question and u is Stefan’s constant. Therefore the rate of supply of heat to the body per unit mass in order to keep the body temperature constant to T is equal to
From the foregoing relation it will be seen that the rate of supply of heat per unit mass varies inversely as the radius of the body in question. In other words, a small ball of the same material requires a much larger quantity of heat per unit mass of the body. Let us apply these considerations to the
INFLUENCE O F TEMPERATGRE ON METABOLISM
485
question of metabolism in animals. Ordinarily warm-blooded animals are surrounded by air of a much lower temperature than the temperature of the animal body. In other words, the animal is constantly giving out heat to the outside surroundings mainly by radiation and in order that this phenomenon can take place the metabolism of the system should increase in order to keep the body temperature constant. From the foregoing considerations it will be evident that the amount of heat per unit weight of the body lost by the animal due to this radiation is greater, the smaller the size of the animal. This conclusion is actually corroborated by experiments. Consequently from physical principles it follows that the loss of heat per unit weight of the body and the consequent metabolism in the animal body to keep up this loss of heat is greater the smaller the size of the animal. From the relation already obtained it is seen that the rate of supply of heat per unit mass is proportional to the difference in temperature between the body and the surrounding air; in other words, the greater is the difference in temperature the greater is the rate of supply of energy per unit mass of the substance. Consequently when a warm-blooded animal is surrounded by air which is colder than the air with which it is normally surrounded, his rate of supply of energy and consequently his metabolism should also increase and that is the reason why the metabolism in the case of warm-blooded animals increases with the fall of surrounding temperature. MTehave already shown that the loss of energy from the surface = 4ny2u (T4 - To4), Now if we express this loss per unit surface, the expression becomes u(T4 - To4);in other words, the question of radius or the size of the body does not come into consideration and the loss of energy per unit surface becomes proportional only to the difference between the body temperature and that of the surrounding air. This has been experimentally obtained by Rubner who has obtained the following results with guinea pig: Temperature
coz
0'
2.91
I IO
2.15
2 IO
I.77
If we calculate the metabolism according to the relation a(T4- To4),we find that the ratio of the metabolisms at oo and 11' is about 1 . 2 , whilst the observed ratio of the metabolism is about 1.3; the calculated value between 21' and 26' is 1.38 and the observed value is 1 . 2 , taking the average temperature of guinea pig to be 38.2. Hence we get a physical significance of Rubners law. From the foregoing pages, it will be evident that Rubner's generalization would be applicable mainly to warm-blooded animals, because usually they maintain a higher body temperature irrespective of the temperatures of the surroundings and the laws of radiation would be applicable to such cases. In the case of cold-blooded animals the body temperature is only slightly higher than the temperature of the surroundings and the foregoing considera-
486
N. R. DHAR
tions are not applicable in these cases and Rubner’s generalization is not valid for cold-blooded animals. We have already suggested that life principle depends essentially on the activity of the catalyst or the enzymes existing in the body. In the foregoing pages, we have observed that usually smaller animals have more metabolism per unit weight of the body than larger animals; in other words weight for weight, the catalysts or the enzymes in smaller animals are more reactive than the catalysts in larger animals. I t sounds very queer that the activity of the enzymes present in the system of a dog is much greater than the activity of those present in the case of a man or we have to assume that the amount of the catalyst per unit weight of the body is much greater in the case of smaller animals than in large animals. It will be seen in the subsequent discussion that the former proposition is more reasonable than the latter. In other words, we are led to the conclusion that the physical activity and the amount of oxidation per unit weight of the body are much greater in the case of a dog than in the case of a man. Even a most casual observation of the domesticated animals has shown that as a rule, small animals do not live so long as large ones, As a general rule, it may be said that a large animal takes more time than a small one to reach maturity and it has been inferred from this that the length of the period of growth is in proportion to longevity. Hence small animals with intensive metabolism live a relatively short time. Large animals with more sluggish metabolism live a longer time. We have already mentioned that Rubner’s view is that a definite sum of living action or energy transformation determines the physiological end of life. There are chemical analogies to these biological facts. Sabatier and his colleagues have shown that when metallic nickel, which is used as a catalyst in the hydrogenation processes, is prepared under suitable conditions a t as low a temperature as possible, the activity of the catalyst is extremely great but it loses its activity very readily. From our experience with other catalysts, we know that an extremely active catalytic surface deteriorates also very rapidly. In other words, an extremely active catalytic surface is more liable to be poisoned or undergo other changes which would effect its activity as a catalyst than the surface of moderately active catalysts. Consequently it seems probable that in the biological processes of metabolism extremely active catalysts are likely to lose their activity more readily than moderately active catalysts. In other words, the catalysts which accelerate the metabolism or oxidation in the case of dogs induces in an unit time more oxidation than the moderately actiie catalysts present in ,the human system, but the more active catalyst present in smaller animals is more liable to lose their activities by poisoning or other alterations than the moderately active catalysts present in the human body and that is why death is more rapid in the case of animals having more active catalysts than in animals having moderately active ones. In this connection the following experiments of Slonakerl on rats will be of interest. Slonaker kept four albino rats in cages 1
J. Animal Behavior, 2,
20
(1912).
INFLUENCE OF TEMPERATURE ON METABOLISM
487
like the old-fashioned revolving squirrel cages, with a properly calibrated odometer attached to the axle, so that the total amount of running which they did in their whole lives could be recorded. It was observed that the amount of exercise taken by these rats was astonishingly large, For a rat to run 5,447 miles in the course of its life is indeed a remarkable performance. Now these four rats attained an average age a t death of 29.5 months, But three control rats confined in stationary cages so that they could only move about to a limited degree, but otherwise under conditions, including temperature, identical with those in the revolving cages, attained an average age a t death of 40.3 months. All were stated to have died of “old age”. From this experiment it clearly appears that the greater the total work done, or total energy output, the shorter the duration of life, and vice versa. We shall now try to explain the possibility of acclimatization of warmblooded animals from this point of view. As we have already mentioned, when there is a fall in the surrounding temperature the metabolism of warmblooded animals is increased; in other words when a warm-blooded animal is brought from a warmer climate to a cooler climate its metabolism and the catalytic activity of the body enzymes are increased. In other words, there is a strain in the system. In the case of human beings this relation should also be valid. We have already mentioned that usually 20% of the body surface is exposed to air in the case of human beings, the remaining 80% is covered by clothes, so that we have to consider only the exposed portion. Kow even for this comparatively small exposed portion the metabolism of the body should increase on lowering the temperature of the surroundings. Consequently the catalyst in the body would be activated; but, as Rubner has shown, the standard metabolism cannot undergo rapid changes as the oxidative energy of the cells is adapted to the usual conditions regarding the loss of heat and is altered very gradually with those conditions; hence the system of a human being or an animal brought from a warmer climate to a cooler climate will be in a state of strain. In the case of cold-blooded animals it is evident that the metabolism is much slower than in the case of warm-blooded animals. Hence the catalytic activity of the enzymes present in cold-blooded animals is not as great as those in the warm-blooded animals of the same size. Consequently the duration of life of a cold-blooded animal is usually greater than that of a warm-blooded animal of the same size and this is corroborated by evidence from biology, because experience show that cold-blooded animals live much longer than warm-blooded animals of the same size. When warm-blooded animals are transported from a warmer climate to a cooler climate, metabolism is increased. The effect of this is that the catalytic activity of the enzymes has to increase in order to produce greater combustion in a unit of time, I have already emphasised that when the catalyst is made to work at a greater speed than the normal one the life period of the catalyst is decreased.
488
N . R. DHAR
Consequently one effect of the transportation of a warm-blooded animal from a warmer climate to a cooler climate will be to activate the enzymes in the body and it will lead to its shortening of the life period. The temperature of a warm-blooded animal remains constant whatever may be the temperature of the surroundings. Consequently the catalyst has to work a t the same temperature irrespective of the temperature of the outside surroundings, Thus, in the case of warm-blooded animals, the question of ageing of the catalyst at a greater rate due to the increase in temperature does not arise, because the catalyst works at a constant temperature which is the body temperature of the animal in question provided the external temperature is less than the body temperature. So the main effect of transporting a warmblooded animal from a warmer country to a colder country is to increase the activity of the body enzymes and to increase the metabolism and t o shorten the life period of the animal in question. ?\Towif the enzymes which were used to generate smaller quantity of heat in a warmer climate are required to produce greater quantity of heat in a cooler climate, they will, by and by, be tired out. In course of time the individual or the animal in question would feel the strain and it seems possible that as years go he will feel the strain more and more. It seems probable thus that an human being transported from a warmer climate to a cooler climate will feel the cold more and more as years go by. On the other hand, if a warm-blooded animal is transported from a cooler climate to a warmer climate, let us see what will be the result on his system by this transportation. As soon as he is surrounded by a warmer atmosphere the amount of metabolism which he was used to produce in a cooler surrounding has to become less because now he is surrounded by a warmer atmosphere. Consequently the catalyst inside the body has to work less in a warmer climate than in a colder climate. Hence the life period of the individual in question is likely to be increased when he is transported from a cooler to a warmer climate provided that the exterior temperature is not greater than his body temperature. I am of the opinion, therefore, that it is more advantageous for a man living in a colder climate to come to a warmer climate than the reverse. When a warm-blooded animal has to live in a country where the outside temperature is usually greater than the body temperature, then the animal will age and grow old and die more readily than an animal living in a cold country; because a t the higher temperature, the body catalysts will age more quickly. Thus this case of an warm-blooded animal will be allied to that of a coldblooded animal. In this discussion, I have all along neglected the consideration of humidity and its influence on human beings and animals. There is another factor that of the color of the skin surface; animals with deeper color are likely to radiate heat more readily than animals with fair complexion.
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489
I have emphasised that the metabolism of cold-blooded animals is much less than in the case of warm-blooded animals under the same conditions; in other words, the enzymes present in cold-blooded animals are not as active as those present in warm-blooded animals. We have also observed that the body temperature of a cold-blooded animal is usually slightly higher than the temperature of the surrounding air and that the metabolism in the case of a coldblooded animal goes on increasing as the surrounding temperature is increased. Let us see what takes place when a cold-blooded animal living in a warmer country is taken to a cooler country. The metabolism in the system will decrease and the animal has to live a life of lesser intensity and possibly with a lesser sense and feeling of well being. The enzymes have to generate lesser quantities of heat in the cool atmosphere and consequently their period of life will be increased and the animal is expected to live a longer life in a cooler surrounding, Moreover, the body catalysts will not age as rapidly in the cooler surroundings as would have been the case in a warmer country. Consequently these two factors will both lead to a greater longevity of the coldblooded animal in question when transported from a warmer to a cooler country. On the other hand, when a cold-blooded animal habituated to a cooler locality, is transported to a warmer country, his metabolism in an unit of time will be increased and the catalysts in the body have to perform more work. Consequently the period of activity of the catalyst will be decreased and the life of the animal is likely to be shortened, though the animal has a more intense and active life in a warm surrounding. Moreover, in a warmer country the body catalyst is likely to age more rapidly than in a cool country. Consequently the effect of both these factors is that old age and death would follow more rapidly in a cold blooded animal transported from a cooler atmosphere to a warmer place. Summary and Conclusion (a) Rubner from his experiments concluded that metabolism in difI. ferent warm-blooded animals was constant when expressed per square metre of the body surface. (b) Experimental results show that smaller animals have greater metabolism in a unit time per kilogram than larger animals. (e) The metabolism of warm-blooded animals increases when there is a fall in the temperature of the surroundings. These biological facts have been explained from Stefan’s law of radiation. 2. The physical activity and amount of oxidation per unit weight of the body are greater in the smaller animals than in the larger ones. In the process of metabolism, extremely active catalysts are likely t o lose their catalytic activity more readily than moderately active catalysts and that is why death is more rapid with smaller animals than with larger ones. 3. The effect of transporting a warm-blooded animal from a warmer country to a colder country is to increase the activity of the body enzymes and to increase the metabolism and to shorten the life of the animal in question.
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N . R. DHAR
If a warm-blooded animal is transported from a cooler climate to a warmer climate, the catalytic activity of the enzymes and the metabolism are decreased. Hence the longevity of the animal in question is likely to be increased. When the warm-blooded animal has to live in a country where the outside temperature is usually greater than the body temperature, then the animal is likely to age and grow old and die more readily than an animal living in a cold country. 4. When a cold-blooded animal is transported from a warmer to a cooler country, the metabolism is decreased and the body enzymes will not age as rapidly as they would do in a warmer country. Consequently both these factors lead to a greater longevity of the cold-blooded animal by this transportation. When a cold-blooded animal is taken from a cooler to a warmer country, the metabolism will be increased and the enzymes will age more rapidly. Hence, the effect of both these factors will be that old age and death will follow more readily, though the animal will live a more intense in a warmer country. Chemical Laboratory, Allahabad University, Allahabad, India.
