GROWTH OF THE CHICK EMBRYO IN RELATION
TO ITS FOOD SUPPLY
BY T. C. BYERLY.
(Physiologist, Bureau of Animal Industry, U.S. Department of Agriculture.)
{Received 27th May, 1931.)
(With Twelve Text-figures.)
INTRODUCTION.
THE author has shown in a previous paper (Byerly, 1930 b) that chick embryos of
different breeds differ little in size when developed in eggs of the same size.
Henderson (1930) found no consistent differences in embryo weights in breeds
normally producing standard-weight eggs as adults. The present paper contains
data on the growth of embryos of breeds producing eggs very different in size and
of embryos in eggs of widely different sizes produced by the same breed.
These data indicate that there is one inherent growth rate for chick embryos of
all breeds, regardless of the size of the egg. This inherent growth rate is modified
in direct proportion to differences in the immediately available food supply. The
immediately available food supply is proportional to a function of the weight of
the yolk sac.
The growth of the embryonic membranes has been measured quantitatively for
the first time, and an estimate of the amount of living material in these membranes
made. When physiological processes, e.g. oxygen consumption and material burned
for maintenance, are calculated per unit weight of the embryo plus the estimated
living material in the membranes, they are found to be of the same order of
magnitude throughout the incubation period. This is directly counter to the
conception of sharply decreasing rates of these processes with time, presented in
the literature.
EXPERIMENTAL PROCEDURE
The basic data are presented in Tables I, III, VI and X. The weights of
2752 embryos and the membranes of most of them were obtained. This material
was obtained from eight sources. The largest group consisted of embryos and
membranes from eggs of standard market size1. These eggs were chiefly from singlecomb Rhode Island Red and single-comb White Leghorn flocks; some eggs from
several other breeds were included. A large portion of the data on embryo weight
1
The term "standard" is used in this paper to designate the eggs of approximate standard size,
average about 60 gm., not the exact standard weight, 56-6 gm.
16
T. C. BYERLY
in eggs secured from this group was included in an earlier paper (Byerly, 1930 b).
The embryos from all eggs of standard size are summarised in the present paper
as a basis for comparison with embryos from smaller and larger eggs from the other
sources. This has been deemed permissible because it was shown in the paper cited
that differences due to breed are small and appear only during the latter half of the
incubation period in eggs of the same size.
The second group of data consists of measurements of embryos and membranes
from small eggs, mostly pullets' eggs, which averaged about 43 gm. in weight.
These eggs were from birds of breeds normally expected to lay standard-weight
eggs as adults, chiefly single-comb Rhode Island Reds and single-comb White
Leghorns.
The third group consists of measurements of Bantam embryos and their
membranes. The Bantam eggs used averaged about 30 gm. The fourth group
consists of measurements of embryos from eggs secured from the mating of F1 individuals from a cross of a Rose-comb Black Bantam male on Barred Plymouth Rock
females. The average weight of the eggs was about 40 gm. The fifth group was
obtained from eggs from F1 birds from the reciprocal cross, Barred Plymouth
Rock male x Rose-comb Black Bantam female. These eggs averaged about 45 gm.
each. The sixth group of data consists of but four embryos. They were developed
in Barred Plymouth Rock eggs fertilised by Bantam sperm. This cross involves
transfer of the sperm in a pipette. Fertility was very low; consequently, the very
small amount of data. The eggs used averaged about 53 gm.
The seventh and eighth groups of data represent measurements of embryos
which developed in double-yolked eggs from birds of breeds normally laying eggs
of standard weight. The former group consists of embryos and membranes from
those eggs in which only one embryo developed, the latter group of twin embryos
and membranes. These double-yolked eggs averaged about 80 gm. in weight.
Errors of measurement must be considered in evaluation of the data. Indeed,
the unavoidable errors in measuring the weight of the embryo during the first
three days of development and in weighing the membranes at any period have
probably deterred other workers from the task. However, even approximately
accurate measurements are infinitely better than guesses. Errors of measurement
are probably greatest in the case of the yolk sac. Two sources of error must be
considered in this connection. Some yolk adheres to the yolk sac. The amount is
relatively greater from the tenth to the eighteenth day of incubation than during
the rest of the period, because the yolk is relatively less hydrated during that
period. The yolk sacs were washed vigorously before they were weighed to remove
as much of the adherent yolk as practicable. The second source of error lies in the
fact that the yolk sac ingests considerable amounts of yolk that no amount of
washing can remove. This yolk is non-living, of course, and must be eliminated in
estimating the amount of living material in the yolk sac. An estimate of the amount
of this ingested yolk is given under the discussion of embryonic metabolism.
Weights of the allantois vary rather widely during the periods of its maximum
weight, which occur at about the ninth to the eleventh and the eighteenth to the
Growth of the Chick Embryo in Relation to its Food Supply
17
twenty-first days. The allantoia are very turgid during these periods and exude
liquid and thus lose weight rapidly on standing for even a short period.
Errors in weighing the embryo arise through the presence of adherent liquid.
This may amount to a relatively large portion of the apparent weight of the embryo
during the first two days of incubation.
Weighings were made to fourth place accuracy. Single specimens or groups
were weighed, depending on embryo age and press of work in the laboratory.
The statistical estimate of error is the probable error. The number of weighings
rather than the number of specimens was used in its determination. All curves
were fitted by method of least squares unless otherwise stated. The coefficient
of deviation, used in comparing goodness offit,is that used by Titus and Hendricks
(1930), and is simply the square root of the mean of the squares of the deviations
of the observed from the calculated values in per cent, of the calculated values1.
All the eggs used were produced and incubated at the U.S. Animal Husbandry
Experiment Farm, Beltsville, Maryland. They were stored at room temperature for
not more than a week and incubated in a Newtown Mammoth incubator. The
temperature of incubation was 39-2 ± 0-2° C , as registered by a-thermometer lying
on the upper surface of the eggs. The temperature of the lower surface of the eggs
is somewhat lower than that of the upper surface in the type of incubator used.
Seasonal variations in temperature affect somewhat the temperature of the lower
egg surface. This probably accounts for part of the excess in size shown by some
of the embryos from the eggs of Fx matings among the offspring of the Rose-comb
Black Bantam—Barred Plymouth Rock crosses during the first half of the incubation period. These eggs were incubated, for the most part, during May, June
and July. Most of the Bantam data were collected earlier in the spring, the pullets'
egg data in the fall, and the other data in the spring, summer and fall.
GROWTH OF THE YOLK SAC.
Changes in wet weight of the yolk sacs with time are shown in Table I for all
classes of embryos. The growth of the yolk sacs of the first five classes is shown
graphically in Fig. 1. The weights of the yolk sacs in the standard eggs are apparently no heavier than those in any of the other groups of eggs prior to the sixth
day of incubation. From the sixth day on, the weights of the yolk sacs in the
standard eggs become relatively heavier, surpassing all of the others by the middle
of the incubation period.
The curves in Fig. 1 all show two ascending sigmoid segments and a final
descending segment. The first segment extends from the beginning of the incubation
period to the ninth or tenth day. During this period the yolk sac grows peripherally
1
Coefficient of deviation, designated as C. of D. in the graphs, is
Wo
N
in which W = observed value, Wo — calculated value, and N — number of observed values (cf.
Titus and Hendricks, 1930, p. 289).
JBBIX
i8
T. C. BYERLY
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Growth of the Chick Embryo in Relation to its Food Supply
19
until it almost completely surrounds the yolk. The yolk itself increases rapidly in
size during the first four days of incubation due to absorption of water from the
albumen. The yolk sac is of approximately constant thickness during this process
of yolk inclosure. The second segment of the curves extends from the end of the
first segment to the fifteenth or sixteenth day of incubation. The yolk decreases in
size during this period due to the excretion of water into the allantois. Possibly
this fact accounts for the initiation of a new mode of growth of the yolk sac: the
formation of radiating lamellae which invade the yolk. These lamellae are much
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Fig. 1. Wet weight of the yolk sac. The curves connect the points obtained by smoothing according
to the formula b' =
, in which a, b and c are the observed weights on three successive
days and V the smoothed weight for the second day.
deeper in the peripheral portion of the yolk sac than in the central. The third
segment of the curves extends from the fifteenth or sixteenth day to hatching time.
The size of both yolk and yolk sac decreases. The yolk becomes slightly more
hydrated and finally both are drawn into the body1.
The data represented in Table I and Fig. 1 show that yolk-sac weight, at any
point in the incubation period after the first six days, varies directly with egg weight,
except in case of the double-yolked eggs. This is as expected, for yolk-sac weight,
at least the maximum weight, must be a function of yolk weight rather than of the
weight of the entire egg, and the yolks of double-yolked eggs are of only normal
size. Table II gives the approximate mean weight of the yolks in each of the classes
for which there are most data. It seemed at first that the most probable relationship
1
See Romanoff (1930) for detailed account of changes in hydration of the yolk.
2-2
T. C. BYERLY
2O
between the weights of the yolk sacs would be a direct proportion to the two-thirds
power of yolk weight, since this is a measure of yolk surface. This was tried and
found wanting. The probable reason is that the relative thickness of the yolk sac
is similar to that of one of the layers of an onion, thick equatorially and thin at the
poles, especially after the middle of the incubation period. The yolk-sac lamellae
formed during the latter half of the incubation period are limited to the peripheral
portion of the yolk sac. With this fact in mind, the author calculated the circumferences of the yolks and compared their relative values with the relative values for
the yolk sacs. These are presented in Table II. The values are fairly close in the
case of the Bantams and the Ft from the Bantam male x Barred Plymouth Rock
female eggs. The eggs from the Flt from the reciprocal cross, and from the
pullets' eggs show yolk sacs too heavy to fit this relationship, but the amount of
data is relatively small compared with the data for Bantam and for standard eggs.
Values for the Bantam yolk sac calculated from the weights of the standard egg
yolk sac, with the observed values, are given in Fig. 2. The fit, as judged by the
coefficient of deviation, is satisfactory when one takes into account the errors of
measurement involved.
Table I I . Relative weights of the yolk sacs of embryos from different sources
compared with function of yolk size1.
Kinds of eggs
Standard
Bantam
FtB. $ x B.R.?
i^B.R. S x B. ?
Pullet
Circumference of Yolk-sac weight
yolk as % circumas % yolk-sac
ference of yolk in weight of embryos
standard eggs
in standard eggs
100
80-75
89-42
94-09
91-46
100
8i-39
91-46
IOI-OI
107-59
Yolk weight
(gm.)
19
10
13
15
13
Log. egg weight
in gm. as % log.
egg weight of
standard eggs
100
83-07
90-66
93-53
92-43
The values for dry weight of the yolk sac and for per cent, dry weight are given
in Table IX, and Figs. 8 and 9. The curve for dry weight shows the same three
segments described for the wet weight curve. The curve for per cent, dry weight
shows great variability, due at least in part to the washing before weighing. The
per cent, dry weight appears to decrease somewhat during the first three or four
days of incubation. It begins to increase again about the eighth to the tenth day
and is maximum from the eleventh to the fourteenth days, subsequently decreasing
somewhat.
The only previous work found on the growth in weight of the yolk sac is that
of Fangauf (1928) who published data on the weight of the yolk sac from day to
1
The relative values were obtained by solving the equation
Y=AX,
(1)
in which Y — yolk-sac weight on a given day of the incubation period for a given set of data;
X = yolk-sac weight on a given day of the incubation period for the standard egg data; A = a
parameter determined from the data by method of least squares.
This weights the later, heavier values, which was deemed proper because these values should
show the limiting effects of yolk size more than the values during the first days of incubation. They
would be less affected by slight temperature variations also.
Growth of the Chick Embryo in Relation to its Food Supply
21
day as per cent, of egg weight. His data are not comparable to those in this paper,
as obviously they have been greatly smoothed and the original observations were
not published.
The growth of the yolk sac is only partially dependent on the presence of an
embryo. Blastoderms comparable in size with those bearing embryos of two to
three days of incubation are often found with no trace of embryo present. Byerly
(1926, 1930 a) has found that at least a part of the yolk sac, especially the peripheral
growing region, may live and grow several days after the death of the embryo.
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GROWTH OF THE ALLANTOIS.
The data for wet weight of the allantois are given in Table III. The curves in
Fig. 3 show the smoothed values for the five groups for which data were obtained
for the greater part of the incubation period (smoothed as for Fig. 1).
The allantois appears on the fourth day of incubation and increases very
rapidly in wet weight till it reaches a maximum about the tenth day. The wet
weight then decreases till about the fifteenth day and subsequently increases to a
second maximum prior to hatching time. During the periods of maximum wet
weight, ninth to the eleventh and eighteenth to the twentieth days, the allantois
is usually turgid and edematous in appearance.
Table IV gives the ratios between the weights of the allantoia of the Bantam
group and the weights of the allantoia of five of the other groups. Murray (1925 b)
showed egg surface to be proportional to the two-thirds power of egg weight. These
ratios are very close to the ratios between the two-thirds power of the egg weights
except for the "single embryo in double-yolked egg" class. This last ratio is lower
than expected due to the fact, discussed later, that a single embryo developing in
a double-yolked egg is proportional in size to a function of the size of a single yolk
Growth of the Chick Embryo in Relation to its Food Supply
23
to about the eighteenth day of incubation. This leaves a relatively large amount of
water and much of the second yolk to be absorbed through the allantois during the
last three days of incubation. It will be noted in Table III that one allantois in such
an egg reached the relatively enormous weight of 7-7 gm. on the nineteenth day
of incubation. This allantois was extremely turgid and had absorbed most of the
second yolk.
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Fig. 3. Wet weight of the allantois.
Table IV. Allantois weight in relation to egg weight1.
Kinds of eggs
Standard
Pullet
F x B.cJ x B.R.?
Fx B.R. <J x B. ?
Double-yolked,
single embryos
Bantam allantois
weight as % of
weight of allantoia
of each of the
other matings
Two-thirds power of
Bantam egg weight
as % of the twothirds power of egg
weight from each of
the other matings
6741
77-26
8361
76-23
63-07
78-45
8248
77-20
2698
51-88
1
The weight of the allantois is approximately proportional to the two-thirds power of egg
weight. Ratios given were obtained by solving equation (i) in which Y = Bantam allantois weight,
X = allantois weight of each of the other classes, A = parameter determined by method of least
squares.
24
T. C. BYERLY
In the case of the allantois, as with yolk sac, the first few days of its development
gave no indication of limitation by either breed or egg size. The limitations of egg
size become apparent by the eighth day of incubation.
Dry weight of the allantois is shown in Table X and Fig. 8. Changes in per cent,
dry weight are given in Table X and Fig. 9. Only one period of maximum dry
weight exists and this falls on about the fourteenth day, in the interval between the
two periods of maximum wet weight. The per cent, dry weight is about 8 on the
fourth day, drops to less than 5 on the seventh and eighth, rises to a maximum of
about 12 on the thirteenth and fourteenth days, then decreases to about 5 at
hatching time. Thus the maximum per cent, dry weight coincides with maximum
absolute dry weight. About 100 mg. of dry matter are lost in the allantois at
hatching time.
GROWTH OF THE EMBRYO.
The data for wet weight of the embryo for all groups of embryos studied are
given in Table V. The weights for the early days of incubation, especially for the
embryos from standard eggs, are greater than those given by Schmalhausen (1927),
Murray (1925 a) and Romanoff (1929); less than those given by Fiske and Boyden
(1926), and about the same as those given by Lamson and Edmond (1914). These
differences are due, no doubt, to slight differences in temperature during storage
and incubation.
Table V. Comparisons of the values of the parameters of equations (2) and (3)
and of the goodness of fit of the resulting curves.
Kind of eggs
Bantam
FjB. S x B.R. ?
FjB.R. <J x B. °
B.<J x B.R. ?
Pullet
Standard
Coefficient of
deviation (three
days and subsequent values)
Equation
(2) a
(2)
3184
- I-93O7
—
149
(3)
—
— 2-0052
- 1-9031
(3)
3-223
3211
3223
(2)
3-256
- 1-9545
—
15-6
I3-9
I5-4
I2-O
(3)
3223
—
(2)
3367
- 2-2540
— 1-9090
'3-5
67
(3)
3223
- 1-8780
109
—
186
186
(2)
(3) A
-b
—
(2)
3'357
— 2-2115
(3)
3223
3-212
3-223
- 1-8386
(2)
(3)
—
—
( - BR - C)
—
- 1-9347
—
- 1-9187
10-4
- 1-8524
99
Three general opinions as to the nature of the growth curve of the chick embryo
have been expressed and supported during the past few years; perhaps it is more
accurate to say two opinions and a compromise between them. Brody (1927)
plotted the data then available in the literature on arith.-log. paper, so that logarithm
embryo wet weight was plotted against time. The slope of such a curve expresses
the relative rate of growth in this mode of plotting. Brody showed that three or
more straight lines, with fairly sharp breaks between them, gave a goodfitto the
data points, as judged by the eye. Such straight lines indicate that the relative rate
Growth of the Chick Embryo in Relation to its Food Supply
25
of growth is constant during the period covered by each of them. Brody argued
at some length to justify the fact that he used no mathematical test for goodness of
fit, nor any but an inspection method of fitting. It has been stated by Gray (1928 a)
in criticism of Brody's method of plotting that any curve may be fitted by a sufficient
number of sufficiently short straight lines. It may be added that the eye as a judge
of goodness of fit is an inadequate comparator. Brody supposes that the breaks
between successive periods of constant relative rate are caused by metamorphoses
of the embryo.
Murray (1925 a) has expressed an opposing view. He states that the weight
of the embryo, at any time from the fifth to the nineteenth day, the period covered
by his study, can be expressed by a simple exponential equation of the type
(2)
logY = alogX+b,
in which Y equals wet weight of the embryo, X incubation time, and a and b are
the parameters which he determined by the graphic method. He ascribed the
breaks Brody found in the curve to errors of sampling, though his own curve
showed two such breaks.
The position of Schmalhausen (1927) is intermediate between that of Brody
and that of Murray. He describes the curve as a parabola but recognises the
presence of systematic deviations corresponding, at least roughly, with the metamorphoses postulated by Brody. He has shown that segments of many growth
curves approach a parabola in form. MacDowell, Allen and MacDowell (1927) have
shown that a betterfitis obtained with this type of curve when the starting-point
used is that time at which the first rudiment of the embryo is discernible. Their
own data were for the growth of the mouse embryo. MacDowell, Gates and
MacDowell (1930) have shown, for the suckling period in the development of the
mouse, that the curve also approaches a parabola as the food supply approaches
ad libitum consumption.
The present data for the first six groups of embryos are plotted in Fig. 4. The
method of plotting is that suggested by MacDowell, Allen and MacDowell (1927).
Logarithm embryo weight in tenth milligrams is plotted against logarithm incubation time in tenths of days minus five-tenths of a day1. It should be understood
that the author does not state that the embryo proper first becomes discernible at
exactly 0-5 day incubation. This is the value used by MacDowell, Allen and
MacDowell for the chick and seems as good as any other as a conventional period.
Two curves are plotted for each of two of the six sets of data. The two curves
for the other sets of data are so nearly identical in each case that but a single curve
could be drawn for each of these sets of data. In each case, the parameters of the
curves for equation (2) were determined by applying the method of least squares
to the set of data for which the curve is given. The parameters of the curves drawn
as continuous lines were determined by applying the same method to all six sets
of data considered as a single set. The equation of these curves is:
logY = A\ogX-BR-C,
(3)
1
These units were used to avoid negative logarithms and for no other reason.
26
T. C. BYERLY
in which Y = embryo weight, measured in tenths of a milligram; X = incubation
time less 0-5 day, measured in tenths of a day; R — the reciprocal of the logarithm
of the egg weight in gm.; A, B and C are the parameters determined in the manner
stated above.
•J33
Fig. 4. Log. embryo wet weight plotted against log. incubation time.
Now, obviously, if the parameters of this equation are determined by using
any one of the six sets of data, the quantity (— BR — C) has the same value as (— b)
in equation (2). If, on the other hand, the parameters of equation (3) are determined
by using all six sets of data, considered as a single set, as good a fit should be
expected as is obtained by determining the parameters of equation (2) for each
Growth of the Chick Embryo in Relation to its Food Supply
27
individual set of data, only if the assumptions implied in formulating equation (3)
are essentially correct. These assumptions are: that the slope of the curve for each
set of data is identical with that for every other set of data and thus that the relative
rates of growth of all classes of embryos are identical, and that the limiting effect
of egg size in each case is proportional to a function of the logarithm of egg weight
in grams. The curves from the two equations very nearly coincide for the four best
sets of data. The coefficients of deviation given in Table V are almost as good for
the curves from equation (3) as those from equation (2).
The values determined for the parameters for each of the equations for each of
the six sets of data are given in Table V. The values of parameter A in equation (2)
vary but little from one set of data to another, whereas the values of b in equation
(2) vary more.
The embryo weights in grams for each of the eight sets of data are given in
Table VI.
The constant b in equation (2) is theoretically equal to logarithm embryo weight
after the lapse of one unit time, in this case at o-6 day incubation, since unit time
is c-i day and zero time is 0-5 day. It is not possible to ascertain whether or not
this is true. The data in Tables I, III and VI for the wet weight of the yolk sac, the
allantois and the embryo, respectively, show a considerable amount of independent
variation during their early development. For example, the standard-egg embryo
is heavier than the Bantam embryo from the fourth to sixth days of incubation,
whereas the reverse is true with respect to the allantoia. The standard-egg embryos
weighed on the third day were heavier than the others weighed on that day; this
has increased importance, since a fair number of embryos was examined in five of
the groups. It should be particularly emphasised that differences between standardegg embryos and those in pullets' eggs are discernible just as early as those between
Bantam and standard-egg embryos. The author (Byerly, 1930 b) probably attached
somewhat too little importance to the effect of egg size on embryo size during the
first days of incubation. Possibly the effect of egg size on embryo size appears as
soon as the circulation is established or soon thereafter, apparently by the third day
of incubation, and certainly by the seventh.
It is entirely possible, of course, that differences are present at 0-6 day incubation,
as required by theory. This would mean that the embryonic anlage was proportional
in size to a function of egg size or that the rate of cell division was proportional to
a function of egg size. The latter seems hardly possible, since differences in embryo
size are apparent as soon in eggs of different size from the same breed as in eggs of
different size from breeds widely different in body size; because for single-comb
Rhode Island Reds and single-comb White Leghorns, Byerly (1930 b) and Henderson
(1930) for Cornish and single-comb White Leghorns, showed that there is little
or no effect of breed on embryo size during the early days of incubation in eggs of
the same size. The data indicate that differences are probably imposed on embryos
of the same size by differences in available food supply. This hypothesis satisfies
the facts now available. It is not certainly proved, but is at least sufficient until
facts inconsistent with it appear.
1 I
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Growth of the Chick Embryo in Relation to its Food Supply
29
It has been pointed out that b in equation (2) is equivalent to the quantity
(— BR — C) in equation (3) when determined from any one set of data. R in this
quantity was assigned the value of the reciprocal of the logarithm of egg weight in
grams simply because it was found by the hoary process of trial and error that this
function of egg weight gave the quantity approximately correct values for all sets
of data. This function has no apparent rational significance, but it will be shown
later that a rational value may be substituted for it.
The constant a in equation (2) is equivalent to A in equation (3); it defines the
slope of the curve and therefore the relative rate of growth, as has been stated.
It was assumed that the slope of all the curves was the same in fitting equation (3)
to the six sets of data considered as one set. The relative rate of growth on successive
days of the incubation period is given for each of the eight sets of data, in Table VII.
Values for relative rate for a particular day are subject to considerable variation
just as is an increment curve. Average relative rates and averages of the relative
rates for successive days in per cent, of the relative rates for embryos in standard
eggs are given for the third to the seventeenth day and eighteenth to the twentieth
day periods at the bottom of Table VII. The average values for the third to seventeenth day period are practically identical; the eighteenth to twentieth day period
show average values roughly proportional to egg size.
The three-day values are used as a starting-point because a fairly large number
of embryos was examined in each of five of the classes on that day, because the
earlier values do not show that the embryos in standard eggs were heavier than the
embryos in other classes of eggs before that time, and because the hypothesis that
food supply is responsible for differences in embryo size requires equal size of
embryos of all classes before the circulation is established. The data show a sharp
diminution of relative rate on the eighteenth day of incubation in four of the five
sets of data which show values for that period. This break undoubtedly has a
rational basis. It has been shown that the yolk sac diminishes in size during the
last days of incubation. The changes preparatory to hatching begin at that time.
The most important of these from the present standpoint is the removal of the
amniotic and allantoic fluids. This is accomplished in part by swallowing and
probably in part by absorption through the allantois. The amount of material to
be removed is directly proportional to egg weight, or very close to such a proportion.
During the last three days the embryo changes from a proportionality in size to
logarithm egg size to a direct proportionality to egg size (Jull and Heywang, 1930).
This is especially striking in the case of the single embryos in double-yolked eggs.
These embryos are little or no larger at eighteen days than standard-egg embryos,
but at hatching time they are proportional in size to egg size. One such embryo
weighed 57 gm., without the yolk, at hatching time as compared with an average
weight of about 35-9 for the standard-egg embryos.
Perhaps it should be emphasised once more that a parabola gives only an
approximate fit to the growth curve of the chick embryo. The deviations in Fig. 3
are systematic. The standard-egg data give the best fit to a straight line, plotted
logarithmically against log time. This is probably due to the fact that selection for
(
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r-qb&
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CI
Growth of the Chick Embryo in Relation to its Food Supply
31
large egg size has been carried on through many generations in the breeds which
now produce eggs of standard size. According to Hays (1929), the weight of the
egg of Gallus bankiva, probably ancestral to the domestic fowl, is only about 40 gm.
The increase in egg size would account for the better fit of the data to a straight line
of the logarithms of embryo weight of embryos in standard eggs plotted against
logarithm time for the last three days of the incubation period.
It should be possible to express the growth of the embryo in terms of its
membranes and time if the postulate that the absolute rate of growth of the embryo
is limited by food supply is correct, and if the efficiency of the membranes bears
an approximately constant ratio to some function of membrane weight. This may,
in fact, be done as is shown in Table VIII and Fig. 5.
Fig. 5. Daily increments in embryo wet weight calculated by means of equation (4) — • — and
observed daily increments —O— both plotted against incubation time. Points marked with * not
used in solution of equation nor of coefficient of deviation.
Table VIII. Daily increments in embryo wet weight as a function of daily yolk sac
weight from three to seventeen days' incubation. Values of terms in equation (4) for
each of the four most complete sets of data.
Parameters of equation (4)
Source of data
A
Standard eggs
Fx B. <J x B.R. ? eggs
FtB.R.3 x B.$eggs
Bantam eggs
1-426
1-414
11-354
1I- 4 II»
1-424
B
C. Of D.
(%)
— 1-625
— 1-6031
- 1-543
- 1-649
- 1-643
19-0
13-8
85-0
43-o
25-7
• Corrected for grossly variant thirteen-day observation.
The assumption was made that the daily increments are proportional to a
function of the daily weight of the yolk sac during the period from three to seventeen
32
T. C. BYERLY
days' incubation inclusive. Each of the four sets of data which were the most
nearly complete was used to determine the parameters of an equation of the type
of equation (2):
l o g Y = A logX - B,
(4)
in which Y = daily increment in wet weight of the embryo, X = daily wet weight
of the yolk sac, and A and B are parameters determined by method of least squares.
The values of the parameters A and B determined from each of the sets of data
are given in Table VIII. Three of the four sets yield almost identical values; the
parameters determined from the fourth set are somewhat lower. Table VI shows
that on the thirteenth day a single embryo was weighed in this set and that this
weight was only a trifle heavier than that recorded for the twelfth day. By smoothing
the twelfth and thirteenth day increments to correct for this grossly variant observation, the second values for the parameters A and B given in Table VIII for this
set of data were obtained. These values are practically identical with the values for
the other three sets. This means that the efficiency of the yolk sac is constant
throughout at least the greater portion of the incubation period, and that the
efficiency of the yolk sacs is the same for all classes of embryos considered.
The calculated and observed values of the daily increments in wet weight of the
standard-egg embryos are plotted in Fig. 5 against incubation time. The variations
are rather large, but only become systematic after the eighteenth day when the
embryo is rapidly becoming dependent on other means of food getting, and from
the fifth to the ninth day period during which food material must be supplied for
the rapidly growing allantois. Increment curves are notoriously variable, and it
has already been pointed out that gross errors exist in measurements of the yolk sac.
Equations may be devised which express the cumulative growth curve of the
embryo in terms of the weight of its membranes and of time. These equations may
or may not include the weight of the allantois. Its inclusion assures a fair fit
throughout the incubation period; without it, the deviations after the eighteenth
day become rather large for the reasons noted in connection with the increment
curve. Equation (5)
l o g E = A log YS + BT - C,
(5)
in which E = embryo weight in mg., YS = yolk sac weight in mg., T = incubation
time in days, A, B and C the parameters, was fitted to the Bantam-egg and standardegg data and to the six sets of data plotted in Fig. 3 considered as a single set, by
the method of least squares. The values of the parameters of equation (5), determined as stated, are given in the upper portion of Table IX. The lower portion of
Table IX presents the values of the parameters of equation (6) determined from
each of the four sets of data which are most nearly complete. Equation (6) is
log £ = ,4 log YS + B log Al+CT-D,
(6)
in which E = embryo weight in mg., YS = yolk sac weight in mg., Al = allantois
weight in mg., T = incubation time in days, A, B, C and D are the parameters
determined by method of least squares, using each of the four most complete sets
of data. Comparison of the coefficients of deviation for equations (5) and (6) show
that equation (6) gives a better fit. This is also demonstrated in Fig. 6 for the
Bantam data.
Growth of the Chick Embryo in Relation to its Food Supply
33
Table IX. Values for the parameters of equations (5) and (6) and a comparison
of the goodness of fit of curves given by those equations.
Equation
5
6
Parameters
Kind of eggs
Standard
Bantam
Summary
Standard
FjB. S x B.R. ?
FiB.R. (J x B.?
Bantam
A
B
C
1-077
1-106
1-045
0-853
0-778
0914
0827
0-080
0-082
0088
0139
0159
o-ioo
0-156
- 1123
— 0-996
- O-874
0-089
0-088
0-085
0081
D
25-8
195
— 0-614
- 0-438
—0-706
-0531
.zs
o
A
.so
i
92
—
_J
7
•y
/
1o
t
1II
/
<t,so
o
J.0& £*/./OG £O& 4
- .0SZ 7--.99S fry
C.Or P.-/9. S 9&
O OBS-£eV£C> J<yfi.i.
'££•
CO& £-.837 AO/? $
.,se Z.0& JtZ.M.O&S T.ss/fc)
f
.so
.zs
oc7
_-—i
163
X
b
t"*
A
C. of D.
(%)
,
i
'
.
7
•
"
7
•
'
.*
A1
/'
/** A ?
/• '
A - A-
Fig. 6. Log embryo weight as a function of log yolk-sac weight and of time. The solid curve
represents values calculated from equation (5), the broken curve those from equation (6). Bantam
data.
It is possible to obtain a still closer fit to the curve for weight if the growth in
total weight of the embryo and its membranes is considered. This is shown for
the standard-egg data in Fig. 7. The curve in Fig. 7 was calculated from equation (7):
(7)
l o g ^ £ F = ^ l o g YS+ B log Al+ CT,
in which AEY = the combined weight of allantois, embryo and yolk sac in mg.,
YS = weight of the yolk sac in mg., Al = weight of the allantois in mg., T = incubation time in days, A, B and C are the parameters determined by method of least
squares from the standard egg data.
Since material absorbed is used by all these structures, it is reasonable that this
equation should give a better fit than the others. Other equations including the
JEBTXi
3
T. C. BYERLY
34
same terms probably may be devised which would describe the data more accurately
and more rationally. Material absorbed but used for maintenance has been ignored
because of the difficulty of translating from terms of O2 consumed, CO2 produced
or solids disappearing to a basis of wet material absorbed. There is no a priori
reason to expect that the increments are proportional to the product of a power
of yolk-sac weight by a power of allantois weight, as is assumed in equations (6)
and (7). It seems more probable that increments would be proportional to the sum
of a fraction of a power of yolk-sac weight plus a fraction of a power of allantois
weight, since they may have widely differing efficiencies. To devise and fit such
.7S
.SO
(!
.zs
o
.rs
so
C,
h
<
r\
i
2S
O
i
7S
A
A
SO
)
.2S
}
f
1
A
O
• 7S
1f
1
—
t.0& y:>s- +.os#• to
\
SO
Fig. 7. Growth of embryo and its membranes as a function of membrane weight and of time. The
curve represents the values calculated from equation (7); the circles the observed values; "standard"
egg data. AEY is the combined weight of allantois embryo and yolk sac.
equations would involve a very laborious series of approximations. On the other
hand, equation (7) may be the correct form; from an empirical standpoint, it is
reasonably satisfactory (Fig. 7).
It is distinctly realised that the principle of proportional growth advanced by
Robb (1929 b) may also serve as a limiting factor in the growth of the embryonic
membranes, that is, that body size determines membrane size, rather than that
membrane size determines body size. It is perhaps better to avoid that point since
the facts in either case support the assumption that the ultimate limiting factor is
food supply.
There is one striking feature of equations (5), (6) and (7). This is the parameter
B in equation (5) and the parameter C in equations (6) and (7), which is identical
Growth of the Chick Embryo in Relation to its Food Supply
35
with B of equation (5). This parameter multiplied by 100 x s, the natural logarithm
of 10, 2-30259, expresses the rate of growth in per cent, relative to the functions of
membrane weight denned by parameter A of equation (5) and parameters A and B
of equations (6) and (7). It has been demonstrated in Table VIII and Fig. 5, that
the daily increments in weight are proportional to a function of membrane weight,
and that the function and proportionality are probably identical for all the sets of
data. The parameter B of equation (5) and C of equations (6) and (7) express the
same fact. The values of parameter C, equation (6), given in the lower portion of
Table IX, are especially striking when converted to a per cent, basis as the range
is only from 18-6 to 20-2 per cent. The value of the parameter A in equation (5)
and of parameters A and B in equations (6) and (7) are somewhat more variable,
but are probably actually identical from one set of data to another, varying only
because of observational errors in the data for membrane weight.
It has been shown that the chick embryo has an inherent relative rate of growth
which is unaffected by breed or egg size from the time the circulation is established
to the time of changes prior to hatching. The absolute rate of growth is limited by
a function of egg size which is approximately proportional to the reciprocal of the
logarithm of egg size in grams.
The data in Table II for the relative weights of the yolk sacs of embryos from
the several groups show that yolk-sac weight, an approximate measure of the
available food supply, is roughly proportional to yolk circumference. The relative
values for logarithm egg weight in grams are also given in Table II. They are
sufficiently close to identity with the relative values for yolk-sac circumference to
permit the substitution of the latter in equation (3). The substitution has not been
made because of the labour involved and because a better value including an
estimate of the role of the allantois as an absorptive agent, and an estimate of the
amount of wet material used for maintenance may eventually be found. Further,
logarithm egg weight is a vastly more convenient value for the worker who may
care to check these results than yolk-sac circumference, which involves a series of
calculations.
DRY WEIGHT OF THE EMBRYO.
The data for the dry weight and for changes in per cent, dry weight are given
in Table X, and are plotted in Figs. 8 and 9.
The data are very similar to those of Murray (1925 b). The curve for increase
in dry weight is rather flat up to the middle of the incubation period, when it rises
abruptly. During the last day or two of incubation, the slope again diminishes.
This is probably due to the relatively large amount of fluid that must be disposed
of in the standard egg before the chick can hatch. The only measurements of dry
weight are those for standard-egg embryos and their membranes (Fig. 8).
The curve for per cent, dry weight shows an initial value of about 15 per cent,
which drops to less than 7 per cent, with the establishment of the circulation. The
portion of the curve corresponding to the period covered by Murray's data is very
3-2
00
M
I;,
Growth of the Chick Embryo in Relation to its Food Supply
37
similar to his except that the nineteenth day value shows a drop probably due to the
ingestion of amniotic and allantoic fluids (Fig. 9).
Table X. Dry weight of embryo, allantois and yolk sac in grams on successive
days of the incubation period. Standard eggs only.
Day
1
2
25
3
4
S
6
7
8
9
10
11
12
13
1
5
16
17
18
19
20
Embryo
O-OOOII
000040
000072
000094
00021
00088
00178
0-0382
0-0655
00980
0-140
0-208
0376
0-588
0-993
1-640
2-460
3-170
3-870
4-560
4-890
—
Percentage
dry weight
14-1
147
14-0
7-9
6-4
67
6-7
6-7
6-8
6-8
69
6-6
8-7
9-6
n-8
136
17-0
17-9
183
19-1
17-0
—
Allantois
—
—
—
—
—
000028
000156
000673
00236
0-0490
00923
0134
0-161
0-175
0-170
0-184
0139
0-129
0-106
O-II2
O-O94
Percentage
dry weight
—
—
—
—
—
79
6-7
5-5
4-7
4'7
5-8
7-3
9'S
II-O
12-4
I2-O
10-5
8-5
60
64
5-i
Yolk sac
Percentage
dry weight
0-002
22-5
O-OII
—
311
—
—
0-023
0-071
0-115
O-222
0-293
0-278
0392
0560
0-822
22-1
266
24-1
25-S
284
22-3
287
310
0-912
0-571
0-615
39-1
22-1
28-9
309
2I-O
20-3
22-O
21-5
21-5
0-53°
28-5
0634
0-916
1-136
O-79S
0-814
GENERAL SIGNIFICANCE OF HYPOTHESIS OF LIMITING ROLE
OF FOOD SUPPLY.
MacDowell, Gates and MacDowell (1930), have shown that as the food supply
of the sucking mouse is increased, its growth curve approaches more and more
closely the parabola in form. The same thing is true for the chick embryo. It has
been shown that it is only in the standard and single embryo in double-yolked egg
groups that there is no sharp drop in growth rate during the last three days of the
incubation period. Gray (1928 a) showed that the rate of growth of the embryo of
Salmo fario is proportional to its own size and to the amount of yolk in the yolk sac,
at a particular temperature. He admits the probable advantage of using some
function of the yolk sac as a measure of food supply rather than the total amount
of yolk present. He found it difficult to see a reason for food supply restricting
growth rate, when the amount of food was very great in proportion to the amount
of the material in the embryo. This may be explained by the fact brought out in
the present paper, that the growth of the yolk sac itself is determined by the amount
of food present, but is dependent on diameter (or circumference) rather than on
volume of yolk present. The present data confirms his observation that the specific
growth rate of the embryo decreases because there is a reduction in the rate at which
the tissues are supplied with raw material for building new tissues.
Gray (1928 b) gives a critical review of the requirements of rational growth
curves. The author of this paper believes that he has only shown that the available
38
T.
C.
BYERLY
data do not require a more complex hypothesis than the one presented. Under
standard incubation conditions, the wet weight of the chick embryo from the time
of establishment of the circulation to the changes preparatory to hatching is proportional to a function of time and to available food supply. There is some evidence
that this is also true for mammalian embryos. Bluhm (1929) compiled a great deal
of birth-weight data for the albino mouse and found negative correlation between
litter size and birth weight, positive correlation between maternal body size and
birth weight of young not to be explained by genetic constitution. It would be very
interesting to know whether the efficiency of the digestive tract of the animal after
Fig. 10. Feed consumption and digestive tract weight; curves drawn by inspection.
birth or hatching is also constant. Robb (1929 a) observed that the ratio of the
weight of the gut contents of the rabbit to body weight decreases as the rabbit
matures. Latimer (1924) found that the ratio of digestive tract weight to body
weight decreases with increasing body weight in the chicken. If the efficiency of
the digestive tract is constant, the widening ratio between its weight and that of
the whole body must serve as one of the immediate causes of the decrease in
relative rate of growth with age.
Fig. 10 shows feed consumption plotted against digestive tract weight in the
case of the chicken. This is the only available measure of the efficiency of the
digestive tract at successive ages for the same birds. The interval between each two
successive points of each set of data represents the change in two weeks' time. The
Growth of the Chick Embryo in Relation to its Food Supply
39
amount of food eaten is clearly proportional to the weight of the digestive tract for
the first eight weeks after hatching (Fig. 10).
The data for feed consumption were taken from Titus, McNally and Hilberg
(1930), and Titus and Godfrey (1931). The data for digestive tract weight were
read from the curve given by Latimer (1924) for White Leghorns of weights
corresponding to the observed weights of the birds in the experiments of Titus et al.
Each set of feed consumption data was for ad libitum consumption of a uniform diet.
The first significant deviation from a straight line relationship, for the data
examined, is the next observation after the major inflection in the curve for body
weight plotted against age. This inflection corresponds approximately with the
onset of puberty. It marks the close of the "self-accelerated " phase of growth (cf.
Brody, 1927). Appetite apparently decreases with the beginning of the endocrine
changes of puberty. Whether there is a causal relationship or mere coincidence is
not apparent. It seems reasonable to conclude that the immediately available food
supply, which is controlled by the size of the food-absorbing mechanism, is a factor
causing steady reduction in the relative rate of growth prior to the major inflection
in the growth curve for the chicken. It is of course realised that there may be some
mechanism in the organism itself which controls the growth of the digestive tract
according to Robb's (1929 b) principle of proportional growth.
RATE OF PHYSIOLOGICAL PROCESSES.
The rates of the various metabolic processes of the embryo, as given in the
literature, are based solely on the weight of the embryo. Murray (1926) admits
that an error may be involved in the omission of the embryonic membranes in the
computation of such processes, but assumes that such an error would be constant
or negligible. In order to estimate the error involved by neglect of the embryonic
membranes, estimates have been made of the absolute and relative weights of the
living material in the membranes throughout the incubation period on both dry
and wet basis for the standard-egg data.
The calculated weights of the living material in the yolk sac are given in
Table XL
The following scheme was used to obtain an approximation of the amounts of
yolk and protoplasm present. It was assumed that the per cent, dry weight of the
protoplasm in the yolk sac paralleled that in the embryo. The included yolk was
assumed to contain 50 per cent, dry matter, the approximate value for fresh yolk.
The amount of protoplasm in the yolk sacs was then computed from their observed
wet weights and per cent, dry weights. The allantois observed weights were
assumed to consist of living material. The relative amount of the total living
material in the egg comprised by each, the allantois, the embryo, and the yolk sac,
is given in Figs. 11 a and 11 b for the wet and dry basis respectively.
The calculated values for the yolk sac are probably conservative for the period
during which the weight of the yolk sac is greatest relative to embryo weight, i.e.
before the middle of the incubation period. The per cent, dry weight of the yolk-
40
T. C. BYERLY
sac protoplasm is surely not much below the 6 per cent, shown by the embryo
during this period. The living material of the yolk sac comprises a very much
greater portion of the living material in the egg during the first few days of incubation than during the later portion. The allantois is relatively heaviest about the tenth
day of incubation. Prior to the middle of the incubation period, non-inclusion of
the weight of living material in the membranes in computing physiological processes
of the embryo may involve an error of from 50 to 95 per cent. During the latter
half of the incubation period the error involved would gradually decrease to about
10 per cent.
Table X I . Calculated wet and dry weights of the yolk sac in grams on successive days
of the incubation period. Standard eggs only. Calculated weight is the observed
weight less the estimated amount of ingested yolk present. For method of estimation
see text.
Day
Wet weight
Dry weight
1
2
0-006
0-028
0-075
0-157
0-292
0-427
0-525
0-605
O-735
0-805
0994
o-ooi
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
i-55°
2-080
2-385
2-966
3-200
3-204
2-848
2136
1-780
0-006
0-006
0-009
0-015
O-O2I
0-026
0-031
0-036
0-051
0-083
0-139
O-22O
O-286
0-420
O-5I2
0-576
0-504
O-378
0-324
Figs. 11 a and 116 demonstrate Murray's (1926) assumption that to ignore the
embryonic membranes introduced a constant or a negligible error in computations
of physiological processes, is far from correct.
The curve for relative weight of the yolk sac is very similar to the curve for
relative rate of growth of the embryo. It has been shown that the increments in
wet weight are proportional to the wet weight of the yolk sac and that decrease in
relative rate of growth of the embryo were caused by decrease in the available food
supply and need not imply any other limiting factor than food. Before metabolic
processes can be calculated on a correct basis, the relative rates of metabolism of
membranes and embryo must be known. Dr Joseph Needham of Cambridge
informs me that he is undertaking such determinations.
If it is assumed that the rate per unit living material is the same, the published
curves would be greatly modified. Fig. 12 illustrates the type of change that would
be introduced. The curve for oxygen consumption is quite different from that
Growth of the Chick Embryo in Relation to its Food Supply
41
given by Murray (1926) which is shown for comparison. His curve shows a
decreased rate of oxygen consumption with increased incubation time, whereas
essentially equal values are obtained for the entire incubation period if the sum of
all the living material in the egg is used in the calculation. The curve for rate of
metabolism as measured by the amount of solids disappearing during the incubation
period gives a similar picture. The curve shown in Fig. 12 was fitted to equation (8):
(8)
WET MATERIAL
EMBRYO
6
7
a
3
/O II 12 /3 I* IS /S /7
18 13
DRY MATTER
10 // 12 13 14- IS 16 /7 /B
/3
Fig. i i . Per cent, of total protoplasm comprised by each, the allantois, the embryo
and the yolk sac, during the incubation period. A, wet weight. B, dry weight.
in which Y = amount of solids disappearing during one day, W = total wet weight
of living material in the egg at the end of that day, A = a constant, obtained by
solving the equation, A = -=r& in which the several terms are as noted for equation (8). The data for amount of solids disappearing were taken from Murray (1926).
Murray's data for solids disappearing yield a value of about 26 mg. per gm. wet
weight of embryo on the sixth day. The value on the nineteenth day is about
10 mg. per gm., a drop of over 60 per cent. The third process illustrated in Fig. 12
is the rate of absorption of dry matter per unit wet weight of living material in the
42
T. C. BYERLY
egg. The rate is of the same order of magnitude from the third to the seventeenth
days. Murray's (loc. cit.) data yield similar values for this process, calculated in
terms of embryo weight.
The other physiological processes of the embryo would show similar changes
from the published curves if treated in the same manner. Neither those given nor
any other can be accepted as valid until the relative metabolism of embryo and
membranes, respectively, is determined.
/
z
3
6 7 3 S /O // /2 /J /•* /S /S
/NCUB^T/OM T//1EY/V GATS
/7
Fig. 12. Effect of calculating rates of certain metabolic processes on a basis
of total protoplasm in the egg rather than embryo weight.
SUMMARY.
The rate of growth of the chick embryo depends upon an inherent growth rate,
probably identical for all breeds. This rate is modified during incubation in direct
proportion to a function of egg size. The increments in wet weight of the embryo
are proportional to a function of the weight of the yolk sac, from the time of
establishment of the circulation to the time of the changes preparatory to hatching.
Both function and proportionality are probably identical for all breeds of chicken,
regardless of egg size.
The growth in weight of the allantois and the yolk sac have been measured
quantitatively for the first time. The weight of the allantois in eggs of different
sizes is roughly proportional to the two-thirds power of egg weight after the first
three or four days of its growth. During the initial period of its development the
relative size is apparently independent of breed, egg size, or embryo weight. The
yolk-sac weight in eggs of different sizes is roughly proportional to the circumference of the yolk after a similar initial period of independent growth.
Growth of the Chick Embryo in Relation to its Food Supply
43
Inclusion of the living material in the embryonic membranes in calculations of
the rate of physiological processes of the embryo indicates that they are probably
of the same order of magnitude throughout the incubation period rather than of
sharply decreasing magnitude as supposed by some previous workers.
ACKNOWLEDGMENTS.
The author gratefully acknowledges much helpful advice and criticism from
Mr H. W. Titus and Mr W. A. Hendricks.
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