AMER. ZOOL., 20:469-476 (1980)
Effects of Barometric Pressure and Abnormal Gas Mixtures on
Gaseous Exchange by the Avian Embryo 1
ALOYSIUS H. J. VISSCHEDIJK
Department of Veterinary Physiology, State University of Utrecht,
Alexander Numankade 93, 3572 KW Utrecht, The Netherlands
SYNOPSIS. Gas moves through the pores of the egg shell by diffusion in the gas phase.
The gas flux is therefore determined by the product of the effective conductance of the
shell and the partial pressure gradient of the gas between the ambient air and the inner
side of the shell. The partial pressure gradient of oxygen is decreased by a reduction of
the oxygen partial pressure in the ambient air. This can be achieved by reducing barometric pressure at normal ambient oxygen concentration or by reducing ambient oxygen
concentration at standard barometric pressure. Both methods are reported to decrease
oxygen consumption of the embryo but to a different degree: At the same ambient oxygen
pressure the reduction is less in eggs exposed to a reduced barometric pressure. In an
attempt to explain this difference, chicken embryos aged 16—19 days were exposed to
various oxygen concentrations and carbon dioxide production was measured. At subnormal oxygen concentrations carbon dioxide output diminished as the oxygen concentration
was lowered and the duration of exposure was prolonged. At oxygen concentrations above
normal a small but significant increase in carbon dioxide production was found. Finally
the results are compared with those in the literature on the diverse effects of a continuous
reduction of barometric pressure and ambient oxygen concentration. This difference is
ascribed to the fact that a reduction of barometric pressure not only decreases oxygen
partial pressure in the ambient air but also increases effective conductance of the egg
shell, the latter being inversely proportional to the barometric pressure.
INTRODUCTION
The notion that developing embryos
were independent of the surrounding air
(Erman, 1818) was disproved by Schwann
(1834) who showed that an adequate supply of oxygen is vital for successful hatching. Since then research has progressed on
the effects of barometric pressure and the
composition of the gas mixture in which
the egg is incubated (Insko, 1949; Francis
etai, 1967; Landauer, 1967; Stephens and
Ploog, 1967; Lundy, 1969; Freeman and
Vince, 1974), particularly concerning the
hatchability of chicken eggs. Lokhorst and
Romijn (1965, 1967) and Erasmus and
Rahn (1976), however, seem to be the only
investigators who studied the effects of
these environmental factors on gaseous exchange.
Gas transport across the egg shell occurs
by diffusion in the gaseous phase (Wangensteen and Rahn, 1970/71; Wangensteen etal., 1970/71; Paganelli etal, 1975).
This implies that the flux of a given gas
1
From the Symposium on Physiology of the Avian
Egg presented at the Annual Meeting of the American Society of Zoologists, 27-30 December 1979, at
Tampa, Florida.
through the shell is determined by the
product of the effective gas conductance
of the shell (that is, the reciprocal of its resistance to diffusion) and the partial pressure gradient of the gas between the ambient air and the inner side of the shell.
We shall now consider how gaseous exchange and hatchability are influenced if
conductance, partial pressure gradient or
both are changed by using different barometric pressures and ambient gas mixtures.
BAROMETRIC PRESSURE
Barometric pressure affects the effective
conductance of the shell, because it is inversely proportional to the barometric
pressure, and the partial pressure gradient
which is the product of the barometric
pressure (minus water vapor pressure at
incubation temperature) and the gas concentration differential across the shell.
Hatchability of eggs depends primarily
on temperature and ambient gas tensions
of oxygen, carbon dioxide and water vapor
(Lundy, 1969). Because of the lack of information on the effect of environmental
factors we assume that hatchability may
serve, in this review, as a gauge for the
470
ALOYSIUS H. J. VISSCHEDIJK
TABLE 1. Relative hatchability and heat production calculated from the data of Francis et al. (1967), Stephens
and Ploog (1967) and Lokhorst and Romijn (1967) al
different altitudes, barometric pressures and effective ambient oxygen pressures.
Altitude
(acutal or
simulated)
(m)
0
83
145
1000
1204
1500
1951
2000
2194
3200
3292
4953
Barometric
pressure
(torr)
760
753
748
674
657
634
600
596
582
513
507
408
Ambient
oxygen
pressue
(torr)
149
147
146
131
127
122
115
115
112
97
96
75
Relative
hatchability
Francis
(1967)
Stephens
(1967)
Relative
heat production
Lokhorst
(1967)
0.99
1.00
1.00
1.00
0.99
0.87
0.95
0.89
0.92
0.75
TABLE 2. Relative hatchability and heat production calculated from the data of Barott (1937) and Lokhorst and
Romijn (1967) at continuous exposure to different oxygen
concentrations and effective ambient oxygen pressures at a
barometric pressure of 760 torr.
Ambient
oxygen
concentration
(per cent)
Ambient
oxygen
pressure
(torr)
14.3
15
17.0
18
18.6
21.0
30
40
50
102
107
121
128
132
149
213
284
356
Relative
hatchability
Barolt
(1937)
Relative heat
production
Lokhorsl
(1967)
0.61
0.62
0.72
0.86
1.00
0.96
0.80
0.59
0.79
1.00
0.40
0.73
0.50
successful gaseous exchange of the avian
embryo.
Hatchability of eggs laid at or near sea
level has been observed to progressively
decrease when the eggs are incubated at
higher altitudes. The most recent observations were made by Francis et al. (1967)
using the same strains at three altitudes.
Stephens and Ploog (1967) collected eggs
from three breeds at sea level and compared the hatchability of these eggs incubated at sea level, at four simulated altitudes in a compression chamber and at an
altitude of 3200 m. The results of both
groups of investigators are presented in
Table 1, where the hatchability of fertile
eggs is calculated as a fraction of control
at sea level. The same table shows the heat
production of chicken embryos at different simulated altitudes during the 16th—
19th days of incubation expressed as a
fraction of the heat production at sea level.
These data were calculated from the work
of Lokhorst and Romijn (1967). Table 1
illustrates that the basic problem of incubating an egg at high altitude is the reduction in the partial pressure of oxygen in the
ambient air and the lowered oxygen pressure gradient across the egg shell (Freeman and Vince, 1974) as shown by the parallelism between hatchability and metabolic
rate.
Lundy (1969) remarked that additional
detailed experimental information is necessary regarding the effect of other altitude-induced factors on hatchability. The
more rapid weight loss of an egg due to an
enhanced evaporation of water at high altitude is such a factor (Aggazzotti, 1913;
Lokhorst and Romijn, 1967). Paganelli et
al. (1975) have shown that the greater
water loss at high altitude is caused by the
effect of barometric pressure on the water
vapor conductance of the shell, being inversely proportional to ambient pressures
in the range of 0.06 to 8 atmospheres. All
gases are subject to the inverse relationship
between gas conductance and barometric
pressure. This implies that oxygen, though
its partial pressure in the ambient air decreases with increasing altitude, diffuses
more readily into the egg and that carbon
dioxide and water vapor escape more
readily from the egg as the altitude increases.
In an attempt to overcome the effects of
low oxygen partial pressure at high altitude, several investigators introducing
supplementary oxygen into the incubator
during incubation found that there was an
improvement in hatchability (Ells and
Morris, 1947; Meshew, 1949; Stephenson,
1950; Wilgus and Sadler, 1954). Although
it was not appreciated at the time that
there is an increased carbon dioxide conductance at reduced barometric pressure,
Meshew (1949) nevertheless claimed that
the concentration of carbon dioxide as well
as that of oxygen should be increased.
471
GASEOUS EXCHANGE BY THE AVIAN EMBRYO
TABLE 3. Oxygen and carbon dioxide levels (percentages at a barometric pressure of 740 ton) beyond which chicken
embryos did not survive (lower and upper limits) and the ranges where no significant reduction of hatchability was found
during four-day exposure periods (Taylor et al., 1956, 1971; Taylor and Kreutziger, 1965, 1966, 1969).
Period of
exposure (day)
Lower limit
Hatchability
not influenced
(range, %)
Upper limit
Hatchability
not influenced
(range, 7c)
Upper limit
0-4
5-8
9-12
13-16
9-10
<12.5
10-12.5
12.5
16-50
16.5-40
15-60
15-85
99
82
90
absent
0-1.1
0-3
0-5
0-8
7.5
8
15-16
16
17-20
18-21
12.5
16.5-45
absent
0-7
gas
oxygen
Wilgus and Sadler (1954) obtained the best
hatch at an altitude of 1524 m (barometric
pressure 632 torr) with combinations of
20.6% oxygen (120 torr) and 0.2% carbon
dioxide (1 torr) or 23.1% oxygen (135 torr)
and 0.4% carbon dioxide (2 torr). They
suggested that other factors, such as humidity, may also be important.
In experiments at a simulated altitude of
9100 m (225 torr) Weiss and Grimard
(1971) calculated that an atmosphere of
pure oxygen was needed to provide the
necessary oxygen partial pressure. A relative humidity of 85-95% prevented excessive water loss but a hatchability of only
21% of control resulted. Because an increased egg shell conductance should be
correctable by decreasing the diffusion
area, Weiss (1978) covered part of the shell
with paraffin wax and found an interpolated hatch of 90% of controls at 69% shell
coverage if the eggs were incubated at 225
torr pressure in 100% oxygen. Weiss thus
proved that hatchability at altitude depends on oxygen supply and egg shell conductance. The experiments of Weiss and
Grimard (1971) and Weiss (1978), however,
suggest that not only do the partial pressures of oxygen and water vapor in the
ambient air have to be adjusted at high altitude, but also that of carbon dioxide. Until now there is no experimental proof for
this view though air-cell carbon dioxide
tension has been shown to fall from 32 to
22 torr at 0.5 and to increase from 34 to
59 torr at 2 atmospheres (Erasmus and
Rahn, 1976).
17
carbon dioxide
ABNORMAL GAS MIXTURES
Experiments on the effects of abnormal
gas mixtures at sea level pressure can be
divided into those where the oxygen/nitrogen or carbon dioxide/nitrogen ratio is
changed and those where nitrogen is partially or wholly replaced by another inert
gas. The first category components change
the partial pressure gradients of oxygen
and/or carbon dioxide across the egg shell
but have, depending on the magnitude of
the changes, little or no effect on the conductance of the shell. The substitution of nitrogen by another inert gas has no influence on the partial pressure of oxygen or
carbon dioxide in the ambient air but may
have a marked effect on the conductance
of the shell because the diffusion coefficients of oxygen, carbon dioxide, and
water vapor are highly dependent on the
inert background gas present. According
to the Chapman-Enskog equation (Reid
and Sherwood, 1966) oxygen diffuses
3.62, 1.60, 0.95, and 0.46 times more rapidly in helium, neon, argon and sulphurhexafluoride, respectively, than in nitrogen in a binary system.
Changes of the oxygen/nitrogen ratio
Barott (1937) made the first systematic
study of the effect of oxygen concentration
throughout incubation on hatchability and
found an optimum curve for the relationship between both variables. He demonstrated that hatchability is more sensitive
to reduced than to increased oxygen concentration. In Table 2 Barott's results are
472
£
ALOYSIUS H. J. VISSCHEDIJK
1.0
1.0
0.8
0.8
0.6
0.6
,0.4
0.4
0.2
0.2
50
70
90
110
130
150
ir
i70
190
210
230
250
270
290
Ambient oxygen p a r t i a l pressure . torr
FIG. 1. Relative metabolism, measured as carbon dioxide production at short-term exposure and as heat
production at continuous exposure. After Visschedijk et al., 1980. Reprinted with the permission of the editor of
Respiration Physiology.
compared with the metabolic rate during
the 16th—19th days of incubation as calculated from the work of Lokhorst and
Romijn (1967).
Barott's observations were confirmed by
Taylor et al. (1956, 1971) and by Taylor
and Kreutziger (1965, 1966, 1969) who
limited the duration of exposure to abnormal oxygen concentrations to 5 different
four-day periods. Table 3 shows a wide
range of oxygen concentrations in which
the reduction of hatchability is not consistently significant. The lower limit (that is,
the oxygen concentration below which the
embryos did not survive) was similar in all
periods of exposure. The upper limit (that
is, the oxygen concentration above which
the embryos did not survive) appeared to
vary: It was lowest during the 5th-8th and
highest during the 13th—16th days of incubation. The upper limit seems to be
achieved at a greater oxygen concentration
than would be expected by extrapolation
from Barott's experiments (Table 2). The
lower limit, however, could be the same at
four-day exposure (Table 3) and continuous exposure (Table 2) as indicated after
extrapolation of Barott's results.
Lokhorst and Romijn (1965) stated that
most of their 6 young embryos died immediately after an exposure to an oxygen
partial pressure of 54 torr, achieved by reducing barometric pressure to 307 torr.
Recently we exposed embryos aged 16-19
days to various oxygen concentrations during some hours and measured carbon
dioxide production (Visschedijk et al.,
1980). The results show that the effects are
more pronounced at a lower oxygen concentration and an extended exposure (Fig.
1). We have extrapolated a zero gaseous
exchange at short-term (our results) as well
as at continuous exposure (data calculated
from Lokhorst and Romijn, 1967) to a
common intercept at an oxygen partial
pressure of 55 torr. This extinction point
473
GASEOUS EXCHANGE BY THE AVIAN EMBRYO
of gaseous exchange seems to be attained
at a lower oxygen tension than that" of
hatchability which in fact is a long-term
effect.
While there is no doubt that reduced
partial pressure of oxygen reduces hatchability and gaseous exchange, there is some
upon the effects of increased oxygen
levels. Continuous exposure reduced
hatchability (Barott, 1937) and a temporary exposure reduced hatchability (Taylor et al., 1956, 1971; Taylor and Kreutziger, 1965, 1966, 1969) or increased it
(Cruz and Romanoff, 1944), whereas our
results show that short-term exposure during the closing stages of incubation increased gaseous exchange by 8-10% (Fig.
1). It seems that hatchability may not serve
as a gauge for gaseous exchange of the
chicken embryo at supranormal ambient
partial pressures of oxygen.
Changes of the carbon dioxide/
nitrogen ratio
Barott (1937) was also the first to study
the effect of various carbon dioxide concentrations, other conditions being kept
constant. Hatchability decreased linearly
with increasing ambient carbon dioxide
levels until it was zero at a concentration
of 5%.
A much higher tolerance to increased
carbon dioxide concentrations, in particular during the second half of the incubation period, was found by Taylor et al.
(1956, 1971) and by Taylor and Kreutziger
(1965, 1966, 1969) who limited the duration of exposure to four-day periods (Table 3). The addition of carbon dioxide,
however, had also resulted in decreasing
the oxygen levels. Restoration of the oxygen level to approximately 21% increased
tolerance to the higher carbon dioxide
concentrations. The carbon dioxide tolerance decreased when high carbon dioxide
concentrations were combined with high
or low oxygen levels.
Though it is generally assumed that carbon dioxide levels below 0.5% during the
entire period of incubation are harmless,
more detailed information is required on
the effect of carbon dioxide concentrations
in the important range between 0-2%
TABLE 4. Relative heat production of chicken embryos al
different barometric pressures (P) and fractional oxygen
concentrations (F), calculatedfrom the data ofLokhorst and
Romijn(1965, 1967).*
Relative heat
product! on at
FracBarometric
pressure
P (torr)
oxygen
concentration
F
Oxygen
partial
pressure
(torr)
Relative
egg shell
conductance
760
760
760
600
760
507
408
0.209
0.186
0.170
0.209
0.143
0.209
0.209
149
132
121
115
102
96
75
1.00
1.00
1.00
1.27
1.00
1.50
1.86
Normal
Reduced
P
P
Reduced
Normal
1.00
0.79
0.72
(0.70)
0.61
(0.49)
(0.27)
1.00
F
F
0.89
0.73
O.50
* The values in parentheses are predicted on the
principle that egg shell conductances differ at normal
and reduced barometric pressure.
(Lundy, 1969). Note that there is a complete lack of knowledge on the effect of
ambient carbon dioxide concentration on
gaseous exchange of the avian embryo.
Replacement of nitrogen
Hatchability of chicken eggs was reduced by about 50% when helium was substituted for nitrogen, even when the temperature and the relative humidity were
elevated to compensate for the greater
heat and weight loss in a helium-oxygen
atmosphere (Weiss et al., 1965; Weiss and
Wright, 1968). Similar results were obtained by subjecting embryos to 100% oxygen at decreased atmospheric pressure
and elevated humidity (Weiss and Grimard, 1971). It was suggested that the reduction of hatchability was caused by the
absence of an inert gas. The evidence for
this hypothesis arose from the fact that
nitrogen, neon and argon produced successful hatching whereas helium did not
(Weiss and Grimard, 1972).
Although the effect of replacement of
nitrogen by another gas was still obscure,
Weiss had thus made a fine start in solving
the questions concerning diffusion through
the shell. His data provided valuable biological support to the physical approach of
Paganelli et al. (1975) who showed that the
effective egg shell conductance increases
at lowered atmospheric pressure and also
474
ALOYSIUS H. J. VISSCHEDIJK
by the substitution of helium for nitrogen.
Weiss (1975) improved hatchability and
decreased egg weight loss to control value
by reducing the diffusion area of the shell
by 50% with paraffin wax in a 79% helium/21% oxygen mixture. He correctly
concluded that the role of inert gases in
incubation is related to their modification
of the rate of gaseous flux through the
shell. The adverse effects of helium were
ascribed to rapid diffusion of other gases
in helium.
This observation was proved by the decrease of the carbon dioxide and the increase of the oxygen partial pressure in the
air space of eggs incubated in a helium environment and by opposite effects in a sulfurhexafluoride atmosphere (Erasmus and
Rahn, 1973, 1976). The simultaneous effects of a replacement of nitrogen by helium and sulphurhexafluoride on carbon
dioxide production and air-cell carbon
dioxide tension were recently studied by
Ar et al. (1980). The elevated rate of diffusion in the helium-oxygen atmosphere
was demonstrated by a decrease of the carbon dioxide partial pressure in the air
space and a temporary increase in carbon
dioxide production. Opposite effects were
found in the sulphurhexafluoride-oxygen
atmosphere. The observed changes of egg
shell conductance agreed closely with
those predicted in multicomponent gas
mixtures according to Wilke (1950). Erasmus and Rahn (1976) showed that oxygen
consumption increases 15% in a helium
and decreases 16% in a sulphurhexafluoride atmosphere. Though the mechanism
for these changes in metabolic rate was
unknown, it was suggested that it was triggered by the changes in carbon dioxide
tension and the concentration of hydrogen
ions.
COMPARISON OF THE EFFECTS OF
BAROMETRIC PRESSURE AND
ABNORMAL GAS MIXTURES ON
GAS EXCHANGE
Data on the effect of reductions in barometric pressure and oxygen concentration on relative heat production during the
final stages of incubation as calculated
from Lokhorst and Romijn (1965, 1967)
are tabulated in Table 4. The results are
listed with decreasing partial pressures of
oxygen computed from the barometric
pressure and fractional oxygen concentration. From the last two columns of Table
4 it is obvious that the relative heat production is higher if the reduction in oxygen partial pressure is achieved by reducing barometric pressure at the normal
fractional oxygen concentration (0.209).
We shall try to reconcile these observations.
Because egg shell conductance is inversely proportional to barometric pressure, the relative shell conductances presented in the fourth column are calculated
as standard atmospheric pressure divided
by the given barometric pressure. At a barometric pressure of 600 torr the relative
conductance is 760/600 or 1.27. This
means that, at the same ambient partial
pressure of oxygen (115 torr), the relative
metabolic rate (heat production) is 1.27
times greater than at normal barometric
pressure. We can also divide the figures
obtained at reduced barometric pressure
(column 6) by the relative conductances
(column 4) to predict metabolic rates at
normal barometric pressure and reduced
oxygen concentration (column 5). The
predicted values, in parentheses, correspond to the observations. We therefore
ascribe the difference in effect of continuous reduction of barometric pressure (at
normal oxygen concentration) and reduction of ambient oxygen concentration (at
normal barometric pressure) to the increase of the effective egg shell conductance at the reduced barometric pressure.
Lokhorst and Romijn (1965, 1967) measured heat production by direct and indirect calorimetry. The latter is performed
by measuring oxygen consumption and
carbon dioxide production; thus the exchange ratio could have been calculated.
Unfortunately these figures were not published so we do not know whether or not
the exchange ratio changes by reduction
of barometric pressure and oxygen concentration. This implies that we can only
translate heat production into oxygen consumption or carbon dioxide production if
we assume that the exchange ratio does
GASEOUS EXCHANGE BY THE AVIAN EMBRYO
not change substantially. With this assumption in mind we have plotted our results obtained at short-term exposure and
those of Lokhorst and Romijn obtained at
continuous exposure as relative metabolic
rates (Fig. 1). It appears that a zero relative
metabolic rate can be extrapolated to a
common intercept at an oxygen partial
pressure of 55 torr. This graphic presentation suggests that the metabolic rate of
the embryo exposed to reduced oxygen
partial pressure slowly decreases until it
levels off towards the rate found at continuous exposure.
CONCLUSIONS
The effects of barometric pressure and
abnormal gas mixtures have often been
studied on hatchability of chicken eggs,
occasionally on gaseous exchange of chicken embryos and not, as yet, on that of other avian species.
Though the knowledge of the mechanisms involved in the diffusion of gases
through the egg shell has increased during
the past decade, many problems remain to
be solved. A practical one is whether or not
artificial incubation of sea level eggs can be
performed successfully at any altitude by
an adjustment of relative humidity, oxygen concentration and carbon dioxide concentration. This problem necessitates a
fundamental approach. As hatchability appears to be correlated to metabolic rate at
a reduced partial pressure of oxygen in the
ambient air, further studies are necessary
on the effects of barometric pressure and
abnormal gas mixtures on oxygen consumption and carbon dioxide production.
ACKNOWLEDGMENTS
I am grateful to Dr. H. Rahn for his critical share in this work and to Dr. C. Carey
for correcting the manuscript.
REFERENCES
Aggazzotti, A. 1913. Influenza dell'aria rarefatta
sull'ontogenesi. Nota 1. La perspirazione delle
ova di gallina durante lo svillupo in alta montagna. Wilhelm Roux Arch. Entwicklungsmech.
Org. 36:633-648.
Ar, A., A. H. J. Visschedijk, H. Rahn, and J. Piiper.
1980. Carbon dioxide in the chick embryo to-
475
wards end of development: Effects of He and
SF6 in breathing mixture. Respir. Physiol. 40:
293-307.
Barott, H. G. 1937. Effect of temperature, humidity
and other factors on hatch of hen's eggs and on
energy metabolism of chick embryos. Tech. Bull.
U.S. Dep. Agric. 553:1-45.
Cruz, S. R. and L. A. Romanoff. 1944. Effect of
oxygen concentration on the development of the
chick embryo. Physiol. Zool. 17:184-187.
Ells, J. B. and L. Morris. 1947. Factors involved in
hatching chicken and turkey eggs at high elevations. Poultry Sci. 26:635-638.
Erasmus, B. D. and H. Rahn. 1973. Effects of inert
gases upon the O2 and CO2 gradient across the
eggshell of the incubating hen's egg. Physiologist
16:307.
Erasmus, B. D. and H. Rahn. 1976. Effects of ambient pressures, He and SF6 on O2 and CO2
transport in the avian egg. Respir. Physiol.
27:53-64.
Erman. 1818. (letter to Oken). Isis oder Encyclopadische Zeitung von Oken. 1:122-124.
Francis, D. W., P. E. Bernier, and D. C. Hutto.
1967. The effect of altitude on the hatchability
of chicken eggs. Poultry Sci. 46:1384-1389.
Freeman, B. F. and M. A. Vince. 1974. Development
of the avian embryo. Chapman and Hall, London.
Insko, W. M. 1949. Physical conditions in incubation. In L. W. Taylor (ed.), Fertility and hatchability
of chicken and turkey eggs, pp. 209-243. John Wiley & Sons, Inc., New York.
Landauer, W. 1967. The hatchability of chicken eggs as
influenced by environment and heredity. Storrs agric.
Exp. Stn. Monogr., 1 (revised).
Lokhorst, W. and C. Romijn. 1965. Some preliminary observations on barometric pressure and
incubation. In K. L. Blaxter (ed.), Energy metabolism, pp. 419^124. Academic Press, London.
Lokhorst, W. and C. Romijn. 1967. Energy metabolism of eggs incubated in air with a low oxygen
content. In K. L. Blaxter, J. Kielanowski, G.
Thorbek (eds.), Energy metabolism of farm animals,
pp. 331-338. Oriel Press Ltd., Newcastle upon
Tyne.
Lundy, H. 1969. A review of the effects of temperature, humidity, turning and gaseous environment in the incubator on the hatchability of the
hen's egg. In F. C. Carter and B. M. Freeman
(eds.), The fertility and hatchability of the hen's egg,
pp. 143—176. Oliver and Boyd, Edinburgh.
Meshew, M. H. 1949. The use of oxygen in the
hatching of chicken and turkey eggs at high altitudes. Poultry Sci. 28:87-97.
Paganelli, C. V., A. Ar, H. Rahn, and O. D. Wangensteen. 1975. Diffusion in the gas phase: The effects of ambient pressure and gas composition.
Respir. Physiol. 25:247-258.
Reid, R. C, J. M. Prausnitz, and T. K. Sherwood.
1977. The properties of gases and liquids. McGraw,
New York.
Schwann, T. 1834. De necessitate aeris atmospherici
ad evolutionem pulli in ovo incubito. Diss. Berlin.
Stephens, B. F. and H. P. Ploog. 1967. Incubation
of chicken eggs at high altitudes, 10,500 ft.
476
ALOYSIUS H. J. VISSCHEDIJK
(3,200 m). 1967. World's Poultry Sci. Ass. J.
23:346-354.
Stephenson, A. B. 1950. Supplemental oxygen increases the hatchability of eggs at high altitudes.
Fm Home Sci. 11:65, 95-96.
Taylor, L. W. and G. O. Kreutziger. 1965. The gaseous environment of the chick embryo in relation
to its development and hatchability. (2) Effect of
carbon dioxide and oxygen levels during the period of the fifth through the eighth days of incubation. Poultry Sci. 44:98-106.
Taylor, L. W. and G. O. Kreutziger. 1966. The gaseous environment of the chick embryo in relation
to its development and hatchability. (3) Effect of
carbon dioxide and oxygen levels during the period of the ninth through the twelfth days of
incubation. Poultry Sci. 45:867-884.
Taylor, L. W. and G. O. Kreutziger. 1969. The gaseous environment of the chick embryo in relation
to its development and hatchability. (4) Effect of
carbon dioxide and oxygen levels during the period of the thirteenth through the sixteenth days
of incubation. Poultry Sci. 48:871-877.
Taylor, L. W., G. O. Kreutziger, and G. L. Abercrombie. 1971. The gaseous environment of the
chick embryo in relation to its development and
hatchability. (5) Effect of carbon dioxide and
oxygen levels during the terminal stages of incubation. Poultry Sci. 50:66-78.
Taylor, L. W., R. A. Sjodin, and C. A. Gunns.
1956. The gaseous environment of the chick embryo in relation to its development and hatchability. (1) Effect of carbon dioxide and oxygen
levels during the first four days of incubation
upon hatchability. Poultry Sci. 35:1206-1215.
Visschedijk, A. H. J., A. Ar, H. Rahn, and J. Piiper.
1980. The independent effects of atmospheric
pressure and oxygen partial pressure on gas exchange of the chicken embryo. Respir. Physiol.
39:33-44.
Wangensteen, O. D. and H. Rahn. 1970/71. Respiratory exchange by the avian embryo. Respir.
Physiol. 11:31-45.
Wangensteen, O. D., D. Wilson, and H. Rahn. 1970/
71. Diffusion of gases across the shell of the
hen's egg. Respir. Physiol. 11:16-30.
Weiss, H. S. 1975. Improved hatch rate in heliumoxygen by reducing shell diffusion area. Proc.
Soc. Exptl. Biol. Med. 148:937-941.
Weiss, H. S. 1978. Role of shell diffusion area in
incubating eggs at simulated high altitude. J.
Appl. Physiol.: Respirat. Environ. Exercise Physiol. 45:551-556.
Weiss, H. S. and M. Grimard. 1971. Embryogenesis
in 100% O2 at reduced pressure. Space Life Sci.
3:118-124.
Weiss, H. S. and M. Grimard. 1972. Inert gas effects
on embryonic development. J. Appl. Physiol.
33:375-380.
Weiss, H. S. and R. A. Wright. 1968. Environmental
factors in the adverse effects of helium on embryonic development. J. Appl. Physiol. 24:330335.
Weiss, H. S., R. A. Wright, and E. P. Hiatt. 1965.
Embryo development and chick growth in a helium-oxygen atmosphere. Aerospace Med.
36:201-206.
Wilgus, H. S. and W. W. Sadler. 1954. Incubation
factors affecting hatchability of poultry eggs. (1)
Levels of oxygen and carbon dioxide at high altitude. Poultry Sci. 33:460-471.
Wilke, C. R. 1950. Diffusional properties of multicomponent gases. Chem. Eng. Prog. 46:95-104.