AMER. ZOOL., 20:449-459 (1980)
Adaptation of the Avian Egg to High Altitude1
CYNTHIA CAREY
Department of EPO Biology, University of Colorado,
Boulder, Colorado 80309
SYNOPSIS. Theoretical predictions and experiments on eggs of domesticated birds indicate
that the diffusion coefficient of gases is inversely proportional to barometric pressure.
Therefore, potentially lethal losses of CO2 and water vapor from eggs laid at high altitude
might result if the increased tendency of gases to diffuse at reduced barometric pressure
were not counteracted in some manner. Limited data from two wild populations indicate
that water loss from eggs is independent of altitude over a 3000 m elevational gradient.
Four different possibilities are discussed by which compensation for increased diffusion
of water vapor might be achieved at high elevations: 1) a reduction in eggshell conductance
(GH.^O), 2) an increase in the initial water content of the eggs, 3) an increase in shell
thickness, and 4) alteration of water vapor pressure in the nest microenvironment or
incubation temperature by variation in parental behavior. Mean GH2O of eggs of two
precocial and four altricial species breeding above 2800 m is significantly reduced below
values of related birds breeding at lower elevations, but no change in initial water content
or shell thickness has been observed in such eggs. Observations of parental behavior in
species breeding over wide elevational gradients have not yet been made. Identification
of the mechanisms by which eggshell structure is modified to achieve a reduced GH 2 O,
the environmental cues used by females to determine the elevation of the breeding location, and the rapidity with which shell structure can be modified awaits further research.
INTRODUCTION
Exchange of O 2 , CO 2 , and water vapor
between the avian embryo and its environment occurs by diffusion through microscopic pores in the eggshell and the shell
membranes (Wangensteen and Rahn,
1970/71; Wangensteen et al., 1970/71;
Wangensteen, 1972; Paganelli etal, 1975).
This exchange is governed by a complex
interaction among the eggshell structure,
the gaseous content of the environment,
and certain factors determined by the behavior of the incubating adult. The eggshell structure and parental incubation behavior have evolved together with the
incubation period in a manner that regulates gaseous exchange within limits appropriate for the successful development
of the embryo (Ar and Rahn, 1978). Although considerable effort has been devoted to description of these characteristics, particularly eggshell conductance to
gases, in many species (Rahn and Ar,
1974; Ar et al., 1974; Ar and Rahn, 1978),
little attention has been directed towards
' 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.
describing populational variability in one
or more of these characteristics in species
breeding over broad environmental gradients. Such variability, if present, would
allow examination of the important question concerning how diffusive respiratory
systems can be adjusted to environmental
stress.
The gradual reduction in barometric
pressure with increasing elevation in montane habitats provides an excellent environmental gradient that poses progressively severe problems for gas exchange. The
morphological and physiological adjustments of animals native to high altitudes,
that breathe by convection, such as adult
birds and mammals, have been partially
documented (Hall etal., 1936; Morrison et
al., 1963«, b\ Bullard et al., 1966; Carey
and Morton, 1976; and others). However,
the principles governing gas exchange by
convection and diffusion differ considerably (Dejours, 1975). Therefore, the purpose of this review is to identify the important respiratory problems encountered
by avian embryos at high elevations and to
present the apparent solutions to these
problems in several populations of avian
species.
450
CYNTHIA CAREY
THEORY AND EXPERIMENTAL
CONFIRMATION
The diffusive flux of gases between the
embryo and environment can be described
by a modification of Fick's first law of diffusion (Wangensteen et al., 1970/71; Paganelli et al., 1975):
M = (D/RT)(Ap/L)AP
3
(1)
1
where M = gas flux (cm STPD • sec" ), D =
binary diffusion coefficient (cm2 sec"1),
Ap = effective pore area (cm2), L = length
of diffusion path or shell thickness (cm),
AP = partial pressure difference of gas
across shell (torr), and RT = gas constant
and absolute temperature (cm3 STPDcm- 3 -torr-'). The terms (D/RT)-(Ap/L)
are often combined into the term "G"
(cm"3 • sec"1 • torr"1) representing the conductance, or the diffusive capacity of the
eggshell to each gas (Ar et al., 1974).
Therefore, Eq. 1 can be simplified into:
M = GAP
(2)
Equation 2 states that the diffusion of
these gases between the interior of the
shell and its environment is determined by
the conductance of the eggshell and the
differences in their respective gas tensions
between the inside and outside of the shell.
The major problem posed to diffusive
gas exchange in avian eggs laid at high altitude was identified by Rahn and Ar (1974).
Elementary gas kinetics and the ChapmanEnskog equation predict that the diffusion coefficient (D) of gases is inversely
proportional to barometric pressure (PB)
(Reid and Sherwood, 1966; Paganelli etal.,
1975; Paganelli, 1980). Therefore, Eq. 2
can be restated:
(3)
where PB (torr) is the barometric pressure
at a particular elevation.
Equation 3 makes two important predictions. First, oxygen flux into the egg will
increase at reduced PB and the same APo,
across the eggshell. This effect might offset in part the detrimental effects of a reduction of ambient oxygen tensions and
enhance survival. This prediction has re-
cently been evaluated by Visschedijk et al.
(1980). They reanalyzed the data of Lokhorst and Romijn (1965, 1967) who incubated chicken (Gallus domesticus) eggs
either at reduced fractional oxygen concentrations of air (14.3-20.9%) or at reduced PB (408-760 torr). At an equivalent
Po 2 , embryos subjected to low PB had significantly higher metabolic rates than
those of embryos exposed to a reduced
fractional O2 content. Visschedijk et al.
(1980) attributed this significant difference
to the enhanced diffusivity of O2 at low PB.
However, the increase in Do2 will offset
the problems of embryonic oxygen uptake
only to a certain degree. While the flux of
O2 into the egg will be greater at low PB
for the same APo2, ambient Po2 progressively decreases with PB. The APo2 could
be maintained by reduction of aircell and
tissue Po2 or normal tissue Po2 could be
maintained by a reduction of metabolic
rate. The tissue hypoxia or reduced metabolic rate would be expected to restrict
normal growth and hatchability above unspecified altitudes.
Equation 3 also predicts that water vapor and CO2 will diffuse more rapidly
from eggs at high altitude, all other factors
held equal. Experimental evidence also confirms this prediction. Aggazzotti (1913, cited in Paganelli et al., 1975) was the first to
show that chicken eggs incubated at 2900
m lost water more rapidly than similar
eggs incubated near sea level. Additionally, chicken eggs incubated at 0.5 atm lost
twice as much water as at 1 atm and levels
of O2 and CO2 in the air cell increased and
decreased, respectively, close to predicted
levels. Proof that these results were due to
the effect of PB on the diffusion coefficients (D) of these gases was obtained by
measuring water loss from eggs incubated
in atmospheres of inert gases that modify
D in known directions (Paganelli et al.,
1975; Erasmus and Rahn, 1976).
Although eggs typically lose certain
amounts of CO2 and water vapor during
incubation (Rahn et al., 1974; Ar and
Rahn, 1978), the similarities in the fractional water loss during incubation and the
final tensions of O2 and CO2 in the air cell
prior to pipping have led to the assump-
AVIAN EGGS AT HIGH ALTITUDE
don that excessive losses of CO2 and water
vapor, such as observed at low PB, would
disrupt normal growth and reduce hatchability. This assumption has not been fully
tested. The variability in water and CO2
losses tolerated during incubation by embryos of wild birds is unknown and not
well described in embryonic domesticated
birds. Variation in water loss caused by
differences in incubator humidity does
produce pronounced effects on the hatchability of chicken embryos (Landauer,
1967), despite some regulatory abilities in
the latter stages of incubation (Simkiss,
1980). Embryos may cope more effectively
with excess losses of CO2 than water vapor
due to regulatory abilities governing absorption of carbonate from the eggshell
and adjustment of blood buffers (Dawes
and Simkiss, 1971; Crooks and Simkiss,
1974).
Incubation of chicken eggs at high altitudes does diminish hatchability, though
the cause of mortality is not well documented. Acute exposure of chicken embryos to 3800 m resulted in 32.5% mortality by day 18 of incubation (Smith et al.,
1969). Chicken embryos incubated at 9100
m in a normoxic environment suffered excessive losses of CO2 and water vapor that
proved fatal to the embryo unless portions
of the eggshell were covered with paraffin
to restrict gaseous diffusion (Weiss, 1978).
Hatchability was initially quite low (16%)
when a colony of chickens was transported
from a lowland location to 3800 m, but
ultimately it increased to about 60%
(Smith, 1973). Even the highest levels of
hatchability were associated with prolonged incubation periods, reduced metabolic rates, and low hatchling masses relative to sea level values (Wangensteen et al.,
1974).
Further study will be necessary to separate the roles of hypoxia and excessive
losses of CO2 and water vapor in reducing
hatchability of chicken embryos at low PB.
If we accept, in the meantime, the possibility that enhanced diffusion of CO2 and
water vapor could restrict growth and
hatching success in avian embryos, we
must then consider how avian populations
can colonize montane habitats and breed
451
successfully. Twenty-one species of birds
breed between 4300 and 6500 m and many
more between 3000 and 4000 m (see Rahn,
1977, for summary). Since no studies have
yet addressed the problem of excessive
CO, losses from eggs of montane populations, this review will deal solely with water
loss. Such attention is warranted, despite
lack of conclusive evidence that excessive
water loss could prove fatal to avian embryos, since preliminary data indicate this
problem was of sufficient importance that
the increase in DH2O has been successfully
counteracted in montane populations. Daily water loss from naturally incubated eggs
of red-winged blackbirds (Agelaius phoeniceus) and final water content of pipped embryos of red-winged blackbirds and robins
(Turdus migratorius) are independent of PB
over a 3000 m gradient (Carey et al., unpublished data). Therefore, it is important
to examine some potential methods by
which increased diffusivity of gases might
be counteracted in birds breeding at high
elevations.
POSSIBLE MECHANISMS FOR
COMPENSATION OF INCREASED
DIFFUSIVITY OF WATER VAPOR AT
HIGH ALTITUDES
Reduced pore area
Although the shell membranes pose substantial resistance to diffusion of O2 in the
initial stages of incubation (Kutchai and
Steen, 1971; Lomholt, 1976; Tullett and
Board, 1976), the shell provides the principal resistance to gaseous diffusion (Wangensteen et al., 1970/71). A reduction in
pore number and/or size in direct proportion to the reduction in PB would increase
resistance to diffusion and directly offset
the increase in DH2O at a given elevation.
Therefore, water loss from eggs with reduced Ap would be the same at their montane location as from the eggs of the same
species at low elevations.
Estimates of functional pore area (Ap)
are obtained indirectly by measuring the
GH 2 O, the conductance of the eggshell to
water vapor (Ar et al., 1974). The GH 2 O is
a direct correlate of Ap, provided that the
shell thickness (L) does not vary among
452
CYNTHIA CAREY
1132 and 2883 m showed a significant 59%
reduction in GH 2 O for a 17% decrease in
.9PB (Packard et al., 1977) Similarly, mean
GH 2 O of eggs of red-winged blackbirds collected at 2900 m was 74% of the mean of
eggs of the same species collected at 200
m, compared to a PB of 75% of the lowland
• India
O Calif.
value (Rahn et al., 19776). However, eggs
in both studies were of unknown ages. Re.6cent evidence indicates that GH 2 O of small,
600
500
700
400 torr
altricial eggs increases during the initial
.5- 760
stages of incubation (Carey, 1979; Hanka
2000
4000 m
etal, 1979;Sotherland^a/., 1980; Taigen
FIG. 1. Relative conductances to water vapor in eggs et al., 1980; Birchard and Kilgore, 1980).
of the native chicken of India (Gallus gallus) collected
at 3500 m (Rahn el al., 19776) and the domestic chick- Therefore, the conclusions of Packard et
en (Gallus domesticus) studied at 3800 m (VVangensteen al. (1977) and Rahn et al. (19776) that the
et al., 1974). The mean conductance of the lowland reduction in GH 2 O with PB was an adapcontrol was standardized at 1.0 and the average con- tation for compensating for increased
ductances of the montane eggs are plotted at their DH O could be challenged since the same
2
respective altitudes as a fraction of the lowland control. The dark line represents the predicted value at results could be obtained by sampling proeach altitude if the conductance were to be reduced gressively younger eggs at successively
in exact proportion to barometric pressure.
higher elevations.
Two new approaches have been adopted
to control for the effects of age on GH 2 O
populations of the same species. Results in small, altricial eggs. The relation of
for GH 2 O, rather than Ap, will be treated GH 2 O to PB has been evaluated prior to the
in the following summary, since those were development of the chorioallantoic memthe units used in the studies dealing with brane in eggs of cliff swallows {Petrochelidon pyrrhonota) collected between 1268 and
this topic.
Precocial birds. The mean GH 2 O of eggs 2895 m (Sotherland etal., 1980) and magof the native chicken of India {Gallus gal- pies {Pica pica) gathered between 1486 and
lus) collected at 3500 m in the Himalayas 2869 m (Taigen et al., 1980). The regreswas 72% of the mean value of eggs laid at sion line describing the relation between
220 m (Rahn et al., 19776). The PB at the GH 2 O of cliff swallow eggs to PB indicated
montane location was about 69% of the a significant reduction in GH 2 O over the
value at the lowland site (Fig. 1). These 1627 m elevational gradient (Fig. 2). The
chickens were presumed to have been decrease in GH 2 O was considerably greater
breeding at this elevation for at least 40 than that required to compensate for the
increase in DH2O (Fig. 3). For a 19% reyears (Rahn, 1977).
A colony of domestic chickens {Gallus duction in PB, GH 2 O declined approxidomesticus) had been laying eggs for at least mately 39%. The relation between GH 2 O of
15 years at 3800 m in the White Mountains magpie eggs and PB was not significant
of California when the GH 2 O was mea- (Taigen et al., 1980) after the effect of
sured. Mean GH 2 O was 68% of the lowland number of eggs was removed (Fig. 2). The
value (Fig. 1); the PB at that elevation was number of eggs in each clutch at the time
approximately 63% of the PB at the low- of egg collection was a statistically significant factor in both studies, suggesting that
land site (VVangensteen et al., 1974).
the values of GH O may have been influAltricial birds. The first two studies com- enced by the age 2of the egg.
paring eggs of altricial species breeding
An alternate approach has been used to
over elevational gradients documented significant reductions in GH 2 O of the eggs of determine if a significant relation exists
montane populations. Eggs of barn swal- between GH 2 O and PB in small, altricial
lows {Hirundo rustica) collected between eggs (Carey et al., unpublished data). Eggs
1.0-
Gallus
7
I-
453
AVIAN EGGS AT HIGH ALTITUDE
2.0-1
.9-
Pica
u
u
gAgeloius
<
z
1.0-
.8-
Q
z
o
Petrochelidon
u
.7-
Petrochelidon
760
I
1000
Turdus
600
700
1500
3000
ALTITUDE
500
torr
3000
FIG. 3. Relative conductance to water vapor in eggs
of red-winged blackbirds (Agelaius phoeniceus), robins
FIG. 2. Relation of conductance to water vapor (Turdus migratorius), and cliff swallows (Petrochelidon
(mg-day"1 • torr"1) to altitude (m) in cliff swallows pyrrhonota) is shown in relation to the predicted value
(Petrochelidon pyrrhonota) (Sotherland et al., 1980) and if conductance were reduced in exact proportion to
magpies (Pica pica) (Taigen et al., 1980). Each point the reduction in PB at high altitude (thick line). The
represents the populational mean at each location. mean values for conductance of lowland populations
The dark lines represent least squares regression of red-winged blackbirds and robins have been stanlines: G = 0.67 + 0.00027A for Pica, where G = con- dardized to 1.0. Regression lines defining the relation
ductance and A = altitude. This line was calculated between conductance (G in nig-day"1-torr"1) and altifrom mean values of G and collecting altitudes listed tude (A in m): G = 1.46 - 0.00011A and G = 1.85 by Taigen et al. (1980). Mean values for eggs of Petro- 0.00016A for Agelaius and Turdus, respectively, were
chelidon are calculated with a regression line: G = used to calculate the approximate conductance at each
10.14PB + 55.76Ne - 541.54PB, where G = conduc- elevation as a fraction of the sea level control. The line
tance, PB is in kpascals, and Ne = the number of eggs describing Petrochelidon eggs was constructed using
in a nest (2.69). The resulting values for G predicted the regression line provided by Sotherland et al.
by this line were plotted according to the altitude cor- (1980). Values for this species were standardized as a
responding to the PB at the collecting sites listed in fraction of the predicted value at the lowest elevation
Sotherland et al. (1980).
at which eggs were collected (1268 m).
of two species breeding between sea level
and over 3000 m were gathered after day
4 of incubation when GH 2 O is independent
of age (Carey, 1979). The regressions defining the relation of GH,O of eggs of redwinged blackbirds and robins to PB were
statistically significant and suggest a slight
undercompensation for the increase in
DH 2 O at higher elevations (Fig. 3). For instance, PB at 3000 m is approximately 68%
of the sea level value. The GH 2 O predicted
by these equations for eggs laid at that elevation is 74% and 76% for robin eggs and
red-winged blackbird eggs, respectively.
The reduced GH 2 O in eggs of these two
species was correlated with, and probably
contributed to, values of daily water loss
from naturally incubated eggs and water
content of pipped embryos that were independent of variation in PB over a 3000
m elevational gradient (Carey et al., unpublished data).
In summary, mean GH 2 O of montane
populations of two precocial species and
four altricial species (barn swallow, cliff
swallow, red-winged blackbird, and robin)
declined significantly below values of lowland relatives, assuming that the results
from barn swallows were not influenced by
the age of the eggs. The reduced GH 2 O of
eggs of two precocial and two altricial
species fairly closely matched the reduction in PB and should contribute toward
compensation for the increase in DH 2 O in
montane locations. Reduction in GH 2 O of
the other two species (cliff swallow and
barn swallow) greatly overcompensated
for the decrease in PB. These results raise
questions concerning how these eggs take
up sufficient O2 for normal development
454
CYNTHIA CAREY
due to increased DH 2 O. Shell thickness
does not vary significantly with PB in eggs
of red-winged blackbirds and robins (Carey et al., unpublished data), cliff swallows
Increase in initial water content
(Sotherland et al., 1980), magpies (Taigen
If water loss is regulated during incu- et al., 1980), native chickens of India
bation to achieve a prescribed level of hy- (Rahn et al., 19776) or domestic chickens
dration in the pipped embryo (see Ar and
Rahn, 1980), the final water content of the (Wangensteen et al., 1974). There may
egg contents typical of a given species have been no selection for this method of
could be attained at high elevations despite dealing with increased DH2O since thickgreater water losses if the montane eggs ening the shell might have restricted sucwere provided with additional water at lay- cessful pipping and hatching.
ing. This adaptation would require a larg- Alteration in adult nest attentiveness
er egg with a greater initial relative water
The difference in water vapor tension
content than similar eggs of the same
(APH
2 O) across the eggshell provides the
species laid at lower elevations.
driving force for diffusion of water vapor
This particular method of counteracting from the egg. The interior of the egg is
increased diffusivity of water vapor at low assumed to be fully saturated with water
PB does not appear to have been adopted vapor, the exact pressure depending on
by montane populations. Egg mass does the incubation temperature (Rahn et al.,
not vary with elevation in cliff swallows 1976). The water vapor pressure of the
(Sotherland et al., 1980), barn swallows microenvironment of the nest is deter(Packard et al., 1977), magpies (Taigen et mined by numerous factors, such as paal., 1980), or native chickens of India rental attentiveness and nest construction
(Rahn etai, 1977ft). The masses of chicken and location (Rahn et al., 1976). Adult beeggs collected from the colony at 3800 m havior during incubation sets the temperaveraged 22% smaller than those of low- ature of the egg, and therefore, the water
land chickens (Wangensteen et al., 1974). vapor pressure of the egg's interior. The
Egg mass of red-winged blackbirds and water vapor pressure of the nest environrobins does significantly increase with el- ment has also been suggested to be a funcevation, but the initial relative water con- tion of the degree of adult attentiveness
tent does not vary significantly among the during incubation (Rahn et al., 1976,
populations of both species (Carey et al., 1977a).
unpublished data). Therefore, enlargeExcessive water loss from eggs laid at
ment of egg size in these two species does
not appear to provide a supplemental wa- high elevations could be restricted by reter supply for the montane eggs. Adult duction of the magnitude of APH 2 O. Such
red-winged blackbirds breeding in the reduction could be accomplished by demountains are larger than their lowland creasing the internal water vapor pressure
counterparts (K. C. Parkes, personal com- by lowering incubation temperature or by
munication) and may lay larger eggs as a increasing the humidity of the ambient air.
direct result of larger body size. However, The former would require shorter duramontane robins are not significantly larger tions of adult attentiveness or restriction of
than their lowland conspecifics (Carey and heat exchange between the brood patch
and the eggs. The latter would necessitate
Morton, 1976).
greater retention of the water lost from the
eggs, brood patch, and moist nesting maIncrease in shell thickness
terials by increasing the length of bouts of
Since the rate of gaseous diffusion varies attentiveness. These possibilities are clearinversely with the distance, L, over which ly in opposition to one another. Unfortugases must travel (Eq. 1), a thicker shell in nately, no data on nest humidity, incubaeggs laid at high elevations could help re- tion temperatures, or patterns of adult
duce the rate of diffusion of water vapor attentiveness are yet available for species
and lose adequate amounts of water at high
elevations.
AVIAN EGGS AT HIGH ALTITUDE
455
gland might deposit fewer seeding sites.
The crystals would therefore spread farther before contacting other crystals and
would thus produce fewer pore sites. FewMODIFICATION OF EGGSHELL
er pores might also be created by originatCONDUCTANCE
Only one of the four potential methods ing egg production with a greater volume
outlined in the preceding section has yet of albumen already present within the
been identified as a possibility for control- shell membranes. Less fluid would be takling the increase in gaseous diffusion at en up during the plumping process and
high elevations. Certainly, other methods would result in maintenance of fewer open
will be discovered in the future. Mean- pore channels.
Preliminary information indicates that
while, if we assume that the reduction in
GH 2 O in montane eggs does represent an reduction in GH 2 O in montane eggs is coradaptation to prevent excessive dehydra- related with variation in shell structure.
tion at low PB, it is appropriate to raise Eggshells of red-winged blackbirds collectseveral questions that must be answered ed at 2900 m have crystalline projections
before the complexity of this process can into areas between seeding sites that make
visualization of pores difficult (Fig. 4). Adbe fully understood.
ditionally, the numbers of seeding sites on
the inner surface of the montane eggshells
How is eggshell conductance decreased?
are slightly lower than on lowland ones
The conductance of the eggshell is a (Carey et ai, unpublished data). Resolufunction of Ap and L (Eq. 1). Since shell tion of the exact method by which pore
thickness does not vary significantly in area is varied in montane populations will
these species over elevational gradients require much additional information on
(see above), it is anticipated that variation the basic mechanisms of avian eggshell forin the numbers or sizes of pores in the egg- mation.
shell results in the observed changes in
of birds breeding over wide elevational
gradients.
GH 2 O.
The mechanism by which pore number
and size are manufactured in the shell
gland is not known, even for eggs of domesticated birds. Small calcium clusters
are deposited on the outer shell membrane
and serve as seeding sites for crystallization
of CaCO3. Crystals grow both vertically to
form the shell thickness and horizontally
to complete the structure of the shell.
Eventually, the expanding crystals come
into contact and pores can occur at some
of these junctions (Tullett, 1975). Pores
might be created by the process of "plumping," in which fluid flows through the developing shell at particular crystal junctions and maintains the pore openings
(Tullett, 1978). The numbers of seeding
sites and the plumping process may work
separately or in collaboration to determine
the number, and perhaps the sizes, of
pores.
If it were important to construct an eggshell with fewer numbers of pores to increase the resistance to water loss, the shell
How fast can adjustments in conductance
be accomplished?
Certain features of the avian egg appear
to be heritable characteristics. Shell thickness (Tyler, 1969), egg size and shape
(Kendeigh et al., 1956), patterns of daily
water loss (Quinn et ah, 1945), and GH2O
are more similar in eggs of the same clutch
than when compared between clutches of
the same species. It is unclear in these instances whether these characters are genetically fixed or if they can be modified
by environmental influences.
If GH 2 O is a genetically fixed trait, then
avian populations could invade new montane habitats or descend to lowland areas
for breeding only if sufficient variability
were present in the population that some
females could produce eggs with pore architecture appropriate for optimal gas exchange at the new elevation. The young
hatching from these eggs would pass on
these genes and establish a new breeding
population at this elevation. Therefore, females would conceivably be limited to
456
CYNTHIA CAREY
FIG. 4. Scanning electron micrographs (X597) of the inside of eggshells of red-winged blackbirds collected
at 87 m (top) and 2900 m (bottom). The shell fragments originated from the portion of shell covering the air
cell.
457
AVIAN EGGS AT HIGH ALTITUDE
breed in a narrow range of elevations for
maximal reproductive success.
However, if females could rapidly modify shell gland physiology, resulting in a
modified GH 2 O suitable for a new breeding
elevation, they could breed successfully
over a wide range of elevations and populational movements would not be restricted by this mechanism. Such flexibility
would be advantageous since most avian
groups breeding at high elevations are seasonal residents that migrate from lower
elevations each spring. The time interval
between arrival on the breeding ground
and laying is compressed in montane populations (Morton, 1976). If a population
were forced to breed at different elevation
due to prolonged snow cover, etc. on its
traditional breeding grounds, adjustments
in pore geometry must be made rapidly
for maximal reproductive success. Ideally,
these issues should be addressed with tests
on wild birds, but such studies are presently hampered by the problems that most
wild birds will not breed if captured and
then released at different locations or held
in captivity, the effects of captivity and
food content on pore geometry are not
known, and data collection would be extremely slow due to the periodical nature
of breeding in wild birds.
18-,
3800
| 16
114a
12108-
15
30
60
DAYS
FIG. 5. Conductance to water vapor in chicken eggs
laid at 3800 m and following transport of the hens to
1200 m. Each point represents an egg laid by a specific female. Stars, squares, and circles represent eggs
from hens #9274, 325, and 262, respectively (Ledoux, Paganelli, and Rahn, unpublished data).
predicted directions within a fairly short
time period, even in birds that are not well
known for their migratory ability. More
work on other species is clearly needed.
What environmental cues are used to determine
the appropriate conductance?
If the pore geometry of the eggshell can
One experiment has measured the be varied in response to a change in elechange in GH 2 O in chicken eggs following vation, it would be instructive to learn what
transportation of the hens from one alti- environmental cue is used by the female
tude to another. Thirteen chickens that and how this cue varies the physiological
had been held at 3800 m were moved to sequences resulting in production of an
1200 m. The GH 2 O of the eggs of each in- egg with a pore geometry appropriate for
dividual was measured for 10 days prior the breeding location. One logical candito and 6 weeks following transport. During date is barometric pressure, since it apthe time at the lower elevation, the GH 2 O pears to be a factor influencing gaseous
increased an average of 34%, correspond- flux in avian eggs. Homing pigeons, Coing to an increase of 37% in PB (Ledoux, lumba livia, can detect variation in PB
1977). Individual response to the change in equivalent to a change in altitude of 10 m
PB .differed considerably. The change in (Kreithen and Keeton, 1974). Since levels
GH 2 O from control values for each hen of the other gases in air, particularly O2,
measured before transport ranged from also vary with PB, changes in blood oxygen
5% to 70% (Ledoux, Paganelli, and Rahn, levels may act as a cue. If birds hypervenunpublished data). Generally, GH 2 O in- tilate at high elevations, variations in blood
creased sharply in the first few days at the pH or Pco2 might also initiate changes in
lower altitude and then continued to rise shell construction. Resolution of this issue
gradually for the duration of the test pe- will require laboratory studies in which
riod (Fig. 5). These data suggest that en- various components of the environment
vironmental change can modify GH 2 O in can be varied independently.
458
CYNTHIA CAREY
CONCLUSIONS
Physiological characteristics of organisms often correlate with environmental
variation and are interpreted as adaptations to particular environmental stresses.
It is sometimes difficult, however, to conclusively identify the manner by which environmental stress has selected for particular characteristics or to isolate the facet of
the environment that is the selecting factor. The progressive decline in PB with increased elevation poses distinct problems
for respiratory systems, though adaptations of convective respiratory systems appear to be primarily to hypoxia rather than
hypobaria itself. The decline in GH 2 O with
PB in eggs of montane birds can be attributed to the effects of PB on gaseous diffusion. This is one of the few adaptations
to PB that have been described.
Major issues remain unresolved, starting
with the fundamental assumption that excessive water loss could be detrimental to
avian embryos. The variability in GH2O
present within avian populations suggests
that embryonic regulation of body water
content may be of considerable importance and that attributing the regulation of
water loss to modification of GH 2 O alone
may be quite simplistic. Finally, the problems of birds breeding at the very highest
elevations where severe hypoxia becomes
a problem that may require enlargement
of pore area have yet to be addressed.
ACKNOWLEDGMENTS
Research resulting in the unpublished
data of CC cited here was supported by
the Penrose Fund of the American Philosophical Society, the Gilkie Fund of the
American Alpine Club, the Colorado
Heart Association, the Chapman Fund of
the American Museum of Natural History,
and the CRCW of the University of Colorado. Edward Thompson, Steven Garber,
Frances James, Kevin Cook, and Ken Balmas assisted in these studies. I thank T.
Ledoux, C. V. Paganelli, and H. Rahn for
providing access to unpublished data on
chicken eggs.
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