1. The “Coefficient d’Utilisation” or Plastic Efficiency Coefficient (P.E.C.) has been calculated for each day during development. It has a trough which is deepest between the eighth and ninth days; development is therefore most expensive at this point. The correlation between this and the point of greatest intensity of protein combustion is exact.

  2. The “Rendement Energétique brut” or Apparent Energetic Efficiency has been calculated for each day during development. It rises, changing more rapidly towards the end than at the beginning ; thus it resembles the metabolic rate rather than the growth rate. The “Rendement Energétique réel” or Real Energetic Efficiency cannot at present be calculated for the basal metabolism of the embryo is unknown and it is not certain whether the usual conceptions of basal metabolism can be applied to a rapidly growing and changing organism.

In the consideration of embryonic metabolism it is natural to enquire what degree of wastefulness in growth is shown by the developing embryo. Up to the present time this question has only been answered by treating the ontogenetic period as a whole. The efficiency of growth may vary, however, during that period and a knowledge of the variations in this factor with time might throw some light on the chemical events of incubation. The calculations of this paper were made with this end in view. They were possible because of the general balance-sheet of chemical changes in the developing chick which Murray (16-30) and I myself (21-26) have built up.

(A) The Change In The “Coefficient d’Utilisation” Or “Plastic Efficiency Coefficient” During Development

The degree of efficiency with which the transference of yolk and albumen into flesh and blood is effected may most conveniently be expressed by an efficiency coefficient.

The efficiency coefficient as such corresponds to the “Coefficient d’Utilisation “of Terroine and Wurmseriaa), the “Coefficient Économique” of Pfefferu(27), and the “Plastic Equivalent” of Waterman(37). The best name for it would seem to be “Plastic Efficiency Coefficient” (P.E.C. for short) for this shows that it has nothing to do with energy content or expenditure and explains that it is a measure of efficiency of transfer of matter. It may be described as the ratio
and is designed to show the relationship between the substance combusted and the substance stored, or in other words, the relative cost in gm. of solid of building the embryo. The higher the efficiency coefficient, the smaller the amount of burnt substance in relation to stored substance.

Gray (10) in his recent memoir on the chemical embryology of the trout finds that its average Plastic Efficiency Coefficient (P.E.C.) is · 63 which compares very closely with that of the frog, the chick, the silkworm, and Aspergillus. He worked it out for the chick from Murray’s data (18) in a cumulative way, but a more in-stantaneous picture would be given if it were calculated on a daily basis. How expensive is it on each day of development to build what is built on that day? Table I, column 1 gives the day and column 2 the P.E.C. as given by Gray. This would not be appreciably different if it were computed using Murray’s figures for oxygen consumption (20) instead of those for carbon dioxide production, as could now be done.

Column 6 gives the P.E.C. worked out for each day, the incremental P.E.C., and in Fig. 1 it is compared with Gray’s. Both curves fall and then rise, and the lag in the cumulative one is not significant for each day’s point bears, as it were, in itself the effects of the previous days. The incremental P.E.C. shows the instantaneous change.

Fig. 1.

Plastic efficiency coefficient. The vertical dotted line indicates the point of maximum intensity of protein combustion.

Fig. 1.

Plastic efficiency coefficient. The vertical dotted line indicates the point of maximum intensity of protein combustion.

There must be some significance in the deep trough through which the curve passes between the seventh and twelfth days. Evidently at that period development is most expensive ; the amount of burnt substance is greater relatively to the amount of stored substance then than at any other time. This calls to mind the correlation suggested in a previous paper (23) between heat-production and middevelopment, in which it appeared that both for the chick and the toad (Gayda (8) it is most expensive to double the weight of the animal when embryogenesis is half completed. In the chick this is between the seventh and twelfth days. This might be related to the fact that the growth-rate of dry solid is constant during that period, but the fit is not exact for the constancy is hardly established by the seventh day and continues till the fifteenth. There is, moreover, no reason to suppose that an increase of dry substance rather than water should necessarily lead to an increase of catabolism. But the correlation of the intensity of protein combustion is much more exact, in fact, strikingly so, as may be seen from the vertical line in Fig. 1, and the inference that we have here to deal with an effect of Specific Dynamic Action is difficult to resist. Another explanation is also available. It is just at this period that the transference of fat into protein is probably going on, and, as Terroine, Trautman, and Bonnet (35) have shown, such a transference results in an extra energy-loss of 23 per cent. This might lead to an increased expenditure of substance in a given amount of architectural enterprise. Probably more than one factor is responsible.

The words “a given amount of architectural enterprise” suggest that an alternative way of expressing the P.E.C. might be valuable. Instead of finding out how much material has to be burnt on a given day in order to construct a given amount of embryo, one could calculate how much material would have to be burnt on a given day in order to construct 100 mg. of embryo. Such a value, which would obviously differ from the P.E.C. above described in being high when the development was wasteful and low when it was efficient, and which might be called the percentage P.E.C., is given in column 7 of Table 1. It gives a peak at 8-5 days of development instead of a trough. There can be no doubt of the phenomenon of maximum inefficiency in the middle of the ontogenesis of the chick.

Table 1.
Efficiency Coefficient.
graphic
graphic

We have seen that the average P.E.C. for the whole of development is · 68. It is interesting to enquire which of the foodstuffs contributes principally to this degree of efficiency. Knowing already that fat is the chief foodstuff combusted and that protein is the chief architectural material, it would be natural to predict that the most efficiently stored substance would be protein. The exact figures follow.

Out of 100 gm. of protein in its diet, then, the embryo can store away 98, out of 100 gm. of carbohydrate 82, but out of 100 gm. of fat only 43. This could not have been predicted from the combustion curves alone, but needed a consideration of the constitution of the embryo. The embryo has to thank protein absorption for its average P.E.C. level, and to a lesser degree that of carbohydrate. In the case of animals such as the trout which burn large amounts of protein, the “foodstuff P.E.C.” would be very different.

(B) The Change In The “Rendement Energétique” Or “Energetic Efficiency Coefficient” During Development

The P.E.C. or Plastic Efficiency Coefficient is based on analyses of actual material. Terroine and Wurmser(33) in their classical paper on Growth Energy have argued, following Tangl (32), that a better idea of the fundamental nature of growth and especially embryonic growth can be got by dealing in energy rather than matter. They therefore define the “Rendement Energétique” analogously to the Plastic Efficiency Coefficient as
which is only another way of writing

This can be calculated from the results obtained by the following investigators and works out thus :

They proceed to point out, however, that this “Rendement Energétique brut” contains a fallacy and that to get the “Rendement Energétique réel” the basal metabolism must be taken into account. Tangí’s “Entwicklungsarbeit “(Ea) fails to allow for the fact that all the time the embryo is growing it is also eating and every cell as soon as formed begins a normal metabolic life ; it is thus only a measure of the total embryonic metabolism. In just the same way the “Rendement Energétique brut” fails to allow for the fact that some of the energy absorbed by the embryo is expended in basal metabolism, maintenance energy, “énergie d’entretien,” etc. to which the embryo is committed by the mere circumstance of being alive at all. Thus of the energy in the material combusted only a certain fraction ought really to be included in the calculation of the efficiency, for the rest is earmarked for the upkeep of that part of the building already constructed and cannot be termed in any sense a waste. The “Rendement Energétique brut “does not take into account the fact that every cell embarks upon a basal metabolism as soon as it is completed. A calculation of the true growth energy must therefore allow for this according to the following formula :

The denominator is now the energy absorbed for growth and non-basal metabolism only. The strict correspondence between observed and calculated heat-production found by Bohr and Hasselbalch(2) suggests that the energy not allotted to one or other of the above headings will be very small. There is, however, some doubt whether the usual notions of basal metabolism can be applied to so rapidly changing a system as the embryo. Basal metabolism is that amount of energy used in maintaining a steady state, but can the embryo be considered to be in a steady state even momentarily? Perhaps the conceptions of Terroine and Wurmser are not applicable to the cells of a developing metazoon though they may be quite satisfactory for moulds and bacteria.

Terroine and Wurmser (33) not wishing to place confidence in the law of surfaces, especially as applied to Aspergillus niger, determined their UE or basal metabolism from experiments in which growth was hastened or retarded by adjustments of the pH of the culture medium. Such a procedure is not possible in the case of the chick where the limits within which normal development will proceed are somewhat narrow. In the exploratory calculations of this paper it will therefore unfortunately be necessary to have recourse to the law of surfaces using Meeh’s formula(15) and Rubner’s constant (28). The calculation can evidently not be exact because we do not know how these quantities vary during the embryogeny of the chick, but it is worth while to probe the matter and see what happens. The relevant figures are shown in Tables II and III.

Table II.
graphic
graphic
Table III.
graphic
graphic
In Table II, column 1 gives the day of development, and column 2 the calculated surface of the embryo, obtained according to the formula
where S is the surface, K Rubner’s constant for the chicken, 10· 4, and W the weight taken from Murray’s figures. Column 3 gives the increments of surface each day, the amounts by which the surface is increased in each interdiumal period. Column 4 shows the calories produced in basal metabolism, assuming with Voit(36) that in the chicken this amounts to 0· 943 gm cals. Per Sq mm. surface. This represents the quantity of inevitable loss n the weight of embryo formed each day. In the next column, No. 5, are placed the number of gm. cals. evolved as measured by Bohr and Hasselbalch (2) in each period of 24 hours and if this column is compared with column 9 of Table III where the heat-production calculated from the oxygen consumption is given, it will be seen that the agreement is fair, though the experimental is always rather lower than the calculated value. The fact that the calculated value assumes fat only to be burnt would not entirely account for this. Returning to Table II, however, it can at once be seen that the basal metabolism in column 4 invariably exceeds the total amount of heat put out as given in column 6 which is the incrementation of column 5. Thus there is not enough heat put out to account for the amount that ought to be produced in maintenance energy alone. However, there cannot be much doubt that the basal metabolism as here calculated is absurdly high, for if all the increments are added up the result is 61,000 calories, in other words, about four times as much as the total energy known to be lost by combustion. We must therefore suppose either that the surface formula does not hold in embryonic life or that the high temperature (37°) in which development proceeds leads to a lower basal metabolism than would be expected. Lusk(14..p. 141) says that the minimum requirement for energy is seen to be present when the fasting organism is surrounded by an atmosphere having a temperature of 30° to 35°. Most important of all, however, is the probability that Rubner’s constant for the hen does not hold for the embryonic chick. It is quiescent, its muscles have no tonus or very little, its respiratory muscles are inactive, and its heart alone is requiring constantly a supply of energy. Since the metabolism is proportional to the superficial area of the animal, it may well be asked what is happening in an embryo at the minute stage when its percentage growth-rate is 1400 (Schmalhausen (29)). The large surface in proportion to its weight which the very young embryo must have explains the fall in metabolic rate and rate of heat-production which has been brought to light by so many investigators, e.g. Le Breton and Schaeffer (12), and Shearer (30). Columns 2 and 3 do not begin with nearly such small figures as do columns in which weight is expressed.

Evidently it is not possible at present to calculate the “Rendement Energétique réel” or “Real Energetic Efficiency” (R.E.E.); all that can be done is to calculate the “Rendement Energétique brut” or “Apparent Energetic Efficiency (A.E.E.). This is done in Table III. Column 1 shows the time of development, column 2 the energy stored in the embryo taken from Murray’s table and expressed as gm. cals, per gm. dry weight of embryo, column 3 the same expressed as actual calories present in the embryo each day (cumulative). Column 4 shows the increments of calories, in other words the amounts of potential energy stored in the embryonic body each day. In order to check this and to show that the data balance properly column 5 shows the energy present in the extra-embryonic part of the egg as determined with the bomb calorimeter by Tangí(32). It will be seen that the rest of the egg loses, in addition to combustion losses, 250 gm. cals, between the eighth and the ninth days, while the embryo gains 232; a sufficient agreement. The figure of 34,193 gm. cals, seen at the bottom of column 4 representing the number of cals, contained in the finished embryo agrees sufficiently well with the value given by Tangí of 32,000; the latter was measured directly, the former was obtained by the addition of all the increments.

Columns 6 to 9 give the figures relating to the energy lost in combustion. Column 6 shows Murray’s figures for the mg. of dry solid burnt per gm. dry weight of embryo per day (a measure of the metabolic rate) and column 7 expresses this as actual number of mg. burnt each day. Column 8 translates this into interdiurnal averages, so that the amount of substance combusted in producing the corresponding value of column 4 is there shown for the interdiunal periods. In column 9 this is seen converted into gm. cals., assuming that 100 percent, instead of the true 92 per cent, of the total solid burnt is fat, and that 1 gm. of fat produces on its combustion 9300 gm. cals. The total of this column amounts to 1700 gm. cals., not very far from the 1650 gm. cals., the Ea of Tangl. In column 10 Tangl’s values for column 9 are given, and it may be noticed that they are very close to the newer ones. An error exists here owing to the fact that no account has been taken of the energy left behind in incompletely combusted materials, but as the chief of these is uric acid, and—using the data of Stohmann and Langbeinüi) for the calorific value of uric acid, 2750 gm. cals, per gm.—the cals, locked up in this way only amount to 16 on the nineteenth day or much less than 1 per cent, of the total combusted, this error is negligible. It may also be noticed, by comparing column 7 with Table I, column 4, that the solid combusted calculated from the carbon dioxide output differs very little from that calculated from the oxygen intake. The variations would perhaps be significant for some purposes but not for the present one. Finally column 11 shows the A.E.E. (“Rendement Energétique brut”).

It is diagrammatically represented in Fig. 2. Starting at a low level it slowly rises, gaining in speed till at the fourteenth day it is rising rapidly but soon after-wards it falls off. At the initial stages of development, the efficiency is very low and rises rapidly in the middle of development to attain a constant level by the time of hatching. As can be seen by the value at the base of column 11 the value for the whole of development works out at 66-5, which is exactly what Tangl found. Since the basal metabolism is included in this estimate and since that would naturally be expected to be very high in the early stages when the embryo is very minute and has a large surface in proportion to its size, one would naturally predict that the efficiency, the A.E.E., would be very low then. Its subsequent rise to a constant level might be associated with the decrease in importance of basal metabolism. It is interesting to note that it finishes up very close to the values obtained for the R.E.E., the “Rendement Energétique réel,” of mammalian post-embryonic growth by Kellner and Köhler(11) and Fingerling, Köhler, and Reinhardt(7). But at the present time there is no means of telling what this latter coefficient would show in the ontogenesis of the chick ; it would certainly be much higher than the A.E.E. in the earlier stages but afterwards it might either fall or remain constant. It is difficult to see how the basal metabolism of the embryo could be measured.

Fig. 2.

Apparent energetic efficiency (Rendement Energétique brut).

Fig. 2.

Apparent energetic efficiency (Rendement Energétique brut).

Another way of interpreting Fig. 2 would be by the biogenetic law, for the low efficiency of the early stages may not be due to a high basal metabolism then. As a general rule the “lower” the animal the more wasteful it is: Horace Brown, for example (3), showed that a yeast cell would ferment its own weight of maltose at 30° C. in 2-2 hours and at 40° C. in I· 3 hours, during which time it was not reproducing and as far as could be seen was not doing any work at all. This metabolic level would be about 100 times as high as that of an adult man. The rise in efficiency (A.E.E.) during the development of the chick may perhaps be thought of as a recapitulatory phenomenon.

It may be noted also that if the embryo continued to behave as wastefully all through incubation as it does in the beginning there would not be enough energy in the egg to provide for it : unless the egg were increased to about one and a half times its present size. Even then there would be no reserve yolk at hatching. Is the increase in efficiency due to change of substrate or increasing complexity of embryonic machinery? This is a problem which much future work in chemical embryology will be required to solve. Apparently no conclusions about the substance combusted can be drawn from the A.E.E. For the R.E.E., on the other hand, Terroine, Trautman, Bonnet, and Jacquot (34) have obtained a value of 38 when protein was the principal foodstuff and 58 in the case of sugar. Terroine, Trautman and Bonnet (35) give further a value of 44 for fat. It is true that these figures were all derived from experiments with moulds, Sterigmatocytis nigra and Aspergillus orhizae, so that it is doubtful whether they can be directly compared with such as may be found to hold for homoiothermic organisms. If, however, they do form a valid series there, one might predict, bearing in mind the fact that protein, though combusted in greatest amount at the mid-point of incubation, never preponderates absolutely in the solid burnt, that the R.E.E., if it ever becomes possible to plot it, will fall markedly as development proceeds.

Since the A.E.E. rises with age it resembles the percentage of total solids, the percentage of fat, the latent period of growth in tissue cultured fragments, the total metabolism and the rate of the heart-beat; a miscellaneous collection of factors. But, having in mind the valuable generalisation of Murray (17) that embryonic development is symmetrically diphasic in character, we may enquire whether it moves rapidly at first, then slowly, like the growth rate, or slowly at first, then rapidly, like the metabolic rate. This question can only be answered by the statement that the rise in A.E.E. resembles the fall in metabolic rate. It is slow at first and later more rapid. Thus it would seem as if the furious intensity of combustion with which the embryo begins its life was associated with great wastefulness, while later on greater economy would accompany greater frugality. It may be noted that there is no trough on the A.E.E. curve and that it attains an adult value shortly before the end of development. The calorific value of the embryonic tissue also rises during development, and Murray’s graph (17. P. 421) shows that it goes up in a curve shaped rather like that for the A.E.E., as in Fig. 2. The two may be related, for the richer in potential energy the embryonic body becomes per unit weight, the more efficient the transfer of energy from the yolk and white might be expected to be. The increasing calorific value of the substance transferred would tend to nullify this tendency but might not abolish it altogether.

Though the curves for P.E.C. and A.E.E. are different, it is interesting to find that the average P.E.C. for all development is-68 while the average A.E.E. is 66 per cent. Out of 100 gm. of solid presented to it, the embryo can store 68 ; out of 100 gm. calories presented to it, the embryo can store 66.

Finally, the embryo can be compared with other engines. Its business is to store as much energy as is given it with as little loss as possible. The object of the steam-engine is to produce as much mechanical work from the energy given it with as little loss as possible. The efficiency of this process is not great: in the locomotive engine, which is notoriously wasteful, it may not exceed 15 per cent, and Wimperis (38) gives a value of 22 per cent, for the internal combustion engine working on producer-gas. However, a much better comparison is between the embryo and the boiler or the electric battery for these machines do not alter the form of the energy passing through them. According to Low (13), a Lancashire boiler presented with 100 calories in the form of coal only wastes 28 : an efficiency of 72 per cent., and, according to Cooper (4), an average electric battery will give back 74 per cent, of the electrical energy put into it. The average A.E.E. of the chick, the silkworm, the minnow, and the frog embryo is 77 per cent, but the R.E.E. would be somewhat higher. It is interesting that the efficiency of the embryo should be of the same order as that of other machines.

My thanks are due to Professor Sir Frederick G. Hopkins, F.R.S. for his encouragement and to Miss M. Stephenson, Mr J. T. Mason, Mr H. W. Phear, and Mr J. P. Moyle for various interesting suggestions. I am also indebted to Dr Dorothy Needham for valuable help and to the Government Grant Committee of the Royal Society for a grant towards the cost of these researches.

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