Respiration and energetics of embryonic development in a large altricial bird, the Australian pelican (Pelecanus conspicillatus)
1 Department of Environmental Biology, University of Adelaide, Adelaide
5005, South Australia
2 Department of Anatomy and Histology, Flinders University, GPO Box 2100,
Adelaide 5001, South Australia
* Author for correspondence at present address: Department of Cardiac Physiology, National Cardiovascular Center Research Institute, 5-7-1 Fujishiro-dai, Suita, Osaka 565-8565, Japan (e-mail: jpearson{at}ri.ncvc.go.jp)
Accepted 6 June 2002
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Summary |
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The embryonic developmental pattern of O2 consumption and CO2 production showed clear plateaus lasting 2-3 days immediately prior to internal pipping, resembling the typical precocial pattern. However, the rate of pre-internal pipping O2 consumption was low in comparison with that of precocial species of similar egg mass. There is no evidence to support the hypothesis that the observed plateau in rates of O2 uptake is due to a diffusion limitation of the eggshell gas conductance in this species. Embryonic metabolic rate nearly doubled during the pipping period, but the mass-independent metabolic rate of the hatchling was low in comparison with that of the resting adult. The total O2 consumed (11 063 ml) is equivalent to 217.3 kJ (or 34% of egg energy) based on indirect calorimetry and the observed respiratory exchange ratio of 0.71. Thus, the cost of development (direct calorimetry) was 0.29 kJ J-1 in the egg (mean egg mass 168 g), which is one of lowest reported values. As a result, the production efficiency of pelican embryonic development was 61.6%, higher than the average for birds in general (56.9%) and, in particular, of seabirds that have prolonged incubation periods on the basis of egg mass. High efficiency in embryonic development in this species was attained as a result of rapid embryonic growth later in incubation, low hatchling energy density (23.6 kJ g-1 dry matter) and dry matter content, low embryonic metabolic rate throughout incubation and a shorter than expected incubation period of 33 days (predicted 36 days).
Key words: respiration, embryo, egg, Australian pelican, Pelecanus conspicillatus, development
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Introduction |
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The eggs of altricial pelecaniforms are a small fraction of the female's
body mass, but nevertheless very large. The dozen species of pelecaniforms
investigated to date have, on average, yolk fractions of 22% and egg energy
densities of 5.1 kJ g-1 wet mass, similar to those of the smallest
altricial passerines (Vleck and Bucher,
1998). Previous investigations of egg composition in Pelecanus
onocrotalus and P. erythrorhynchos found some of the lowest
known egg energy densities among the altricial phyla
(Bugden and Evans, 1997
;
Jones, 1979
;
Williams et al., 1982
), with
the exception of a high energy density for the smaller pelican P.
occidentalis (Lawrence and Schreiber,
1974
) that may be erroneous
(Bugden and Evans, 1997
). The
allometric comparisons of cost of development (total energy consumption per
gram of egg) reported by Bucher and Bartholomew
(1984
) suggest that the
metabolic cost of producing P. occidentalis hatchlings may be lower
than that of precocial species.
Embryos of altricial species, and pelicans in particular, can only achieve
a low cost of development over long incubation periods if they hatch
significantly earlier than predicted on the basis of egg mass, are more
efficient at producing hatchling tissues than more precocial species and/or
hatch with lower than expected tissue energy densities. Precocial hatchlings,
in general, have higher true hatchling energy densities (yolk-free dry mass)
than other developmental modes, in which energy densities appear to vary
little (Ar et al., 1987;
Pearson, 1999
). To date, the
efficiency of egg energy conversion to hatchling tissues, defined as
production efficiency, has not been determined for any pelecaniform or large
altricial species.
How avian embryos utilise energy during incubation has been the subject of
debate since it was first demonstrated that embryonic respiration and growth
patterns differed among avian species after taking into account egg size
(Hoyt et al., 1978;
Hoyt and Rahn, 1980
; Vleck et
al., 1979
,
1980a
,b
;
Bucher, 1983
;
Bartholomew and Goldstein,
1984
; Bucher and Bartholomew,
1984
; Bucher et al.,
1986
; Hoyt, 1987
;
Vleck and Vleck, 1987
). Rates
of O2 consumption increase rapidly throughout incubation in both
precocial and altricial species, followed by a period when O2
consumption plateaus from approximately 80% of incubation until pipping in
precocial species. There was no evidence for an O2 consumption
plateau in altricial embryos using discontinuous sampling protocols. However,
a few studies subsequently demonstrated, from continuous recordings, that
O2 consumption plateaus in some altricial species, although for a
shorter duration than in precocials
(Prinzinger and Dietz, 1995
;
Prinzinger et al., 1995
,
1997a
).
The physiological meaning of the respiration plateau that predominates in
the development of precocial species has proved controversial. Since
O2 uptake by the embryo is mediated by diffusion through the porous
eggshell and its membranes, gas exchange rates may become limited by the fixed
gas conductance of the eggshell. This might occur after the inner surface of
the eggshell membranes are completely covered by the respiratory
chorioallantoic membranes, at approximately 60% of incubation in precocial
species (galliforms at least). Some researchers consider that the rate of
O2 consumption of precocial embryos approaches this limitation
before internal pipping (IP) because they achieve a significantly greater
amount of their embryonic growth earlier in incubation than in altricial
species and because incubation is prolonged in some species
(Rahn et al., 1974). In
contrast, in galliform species, the plateau metabolic rate of embryos does not
restrict high growth rates because synthetic efficiency probably increases
during late incubation (Dietz et al.,
1998
). Thus, it remains unclear how avian embryos balance their
energy budgets during incubation and whether the plateau in O2
consumption of some avian embryos represents a diffusive limitation to
O2 uptake imposed by the conductance of the eggshell.
The Australian pelican P. conspicillatus, like P.
onocrotalus, lays one of the largest known eggs (140-210 g) with an
altricial mode of development and has one of the longest incubation periods
among pelicans (33-34 days; see Vestjens,
1977). We have determined the changes in material, energy and
water content of fresh eggs and hatchlings of P. conspicillatus to
evaluate production efficiency and hatchling maturity. We have also measured
O2 and CO2 exchange throughout incubation to confirm
production efficiency, establish the respiratory exchange ratio and test for
the occurrence of a plateau in respiration in late development.
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Materials and methods |
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An additional 30 eggs that were found to be actively incubated were
collected and transported to the laboratory for respirometry studies. These
eggs were placed within an artificial incubator (approximately 1 h after
collection). In each case, the collected eggs were replaced with artificial
`transmitter' eggs or fresh abandoned eggs that were presumed to be fertile.
The transmitter eggs were then used to determine incubation temperatures and
nest humidities prior to the respirometry study to ascertain suitable
conditions for artificial incubation (methods described in
Wagner and Seymour, 2001). In
brief, transmitter eggs were prepared from the eggshells that remained after
determination of egg composition and filled with agar to maintain heat
transfer characteristics similar to those of the egg contents according to the
methods of Wagner and Seymour
(2001
). To ensure that at
least one egg was allowed to hatch in each nest, fertile abandoned eggs or
second eggs from other nests were replaced in the nests under investigation
when the original eggs were incubated to hatching in the laboratory and the
embryos later killed.
Mean egg temperature determined by the transmitter eggs in the field was
35.3±0.3°C (mean ± 95% confidence interval; range
32.0-37.6°C, N=88 intermittent recordings from 15 nests, 14
day periods). All eggs were incubated in the laboratory between 35.0 and
36.0°C under 45-55% relative humidity in a still-air incubator with an
automatic turning mechanism. Eggs were removed from the incubator daily for
mass determinations and respirometry measurements described below. After the
final measurements, young embryos were chilled for 3-4 h at 9-10°C to stop
development, whereas hatchlings and late embryos were killed by CO2
and then dissected to remove the residual yolk. After determining the wet mass
of residual yolk, they were oven-dried with the yolk-free hatchlings, and dry
mass was determined as for fresh eggs. Subsamples of dried eggs and hatchlings
were ground in a mill, pressed into pellets (approximately 0.1-0.2 g) and
their energy content determined with a semi-micro oxygen combustion bomb
calorimeter (Parr 1261, IL, USA) calibrated against certified standard benzoic
acid (M & B Laboratory Chemicals, UK). The energy determinations of all
samples were corrected for ash-free mass.
Respirometry
28 pelican eggs were incubated for the respirometry measurements; however,
some embryos were killed during the last week of incubation for another study
of morphometric analyses of chorioallantoic membranes, heart and lung tissues.
Thus, the sample sizes varied with incubation age. The O2
consumption and CO2 production rates of embryos and hatchlings were
determined by open-flow respirometry at a chamber temperature of 36°C.
Compressed air flowed sequentially through a pressure regulator, a series of
three tubes containing Drierite, soda lime and Drierite (to remove water
vapour, CO2 and water vapour, respectively), and then into one of
three mass-flow controllers (Sierra Instruments Mass-Trak, CA, USA) to flow
separately into three translucent animal chambers (800 ml) held within a
constant-temperature cabinet (±1°C) under dim light. Excurrent air
from the chambers and a fourth channel for dry, CO2-free air passed
through a solenoid gas-flow controller, which directed the samples in turn to
a pump (Charles Austen Pumps, Surrey, UK), a tube of Drierite and, finally, a
combination O2 and CO2 analyser (David Bishop
Instruments 280/0427 Combo, UK) thermostatted to 36°C. Outputs from the
mass-flow controllers and both gas analysers were recorded as voltages on a
personal computer via an A/D converter (Sable Systems Universal
Interface, USA). Sable Systems DATACAN v5.2 data-acquisition software was used
to sample every 0.5 s. Air flow rates used during measurements varied from 100
ml min-1 for early embryos to 350 ml min-1 for
hatchlings.
Calibration of the analysers was routinely achieved by passing dry
compressed air (approx. 21% O2), pure N2 and a precision
gas (0.586% CO2, remainder N2) through the respirometry
system. However, since the response of the CO2 analyser was
non-linear when fractional CO2 changes were less than 1%, a further
post-priori calibration of CO2 production relative to
O2 consumption was made using an alcohol flame
(Young et al., 1984). Pure
ethanol was burnt with a very small flame (using an inflammable asbestos wick)
inside a clean metal paint can outside the cabinet. Compressed air was
supplied at high flow rates to the can, and the majority of the excurrent air
was vented to the outside. A small subsample of the burner gas was diluted
with compressed air from a blank animal chamber before entering the analysers.
Further dilution of the CO2 content of the burner air was made by
increasing the air flow into the burner can and reducing the subsample mixed
with compressed air.
As the respiratory exchange ratio of ethanol combustion is 0.667, the
non-linearity of the CO2 analyser output was corrected over the
range of fractional CO2 changes of 0.05-0.70%, which was similar to
the range for CO2 production rates of pelican embryos and
hatchlings in this study, using a third-order polynomial equation
(y=4101.2x3+29.489x2+0.677x-0.00001,
r2=0.998, where y and x are the
corrected and observed fractional CO2 contents of excurrent air,
respectively). After this correction, the final rates of CO2
production and O2 consumption were calculated according to Withers
(1977) with iterative fitting
assuming an initial respiratory exchange ratio of 0.8.
Artificially incubated embryos were measured once a day for approximately 5
min each after an equilibration period of 40 min, until internal pipping was
observed (candling of the air-cell and vocalisations). Thereafter, embryos
were sometimes measured several times a day until hatching. Hatchling
metabolic rates were recorded for at least 14-15 min to establish minimal
resting values under dim light. Total O2 consumed during incubation
(assuming 33 days of incubation) was estimated from the area under the curve
of mean rate of O2 consumption against incubation age. An energetic
equivalent of 19.64 J ml-1 O2
(Vleck et al., 1980b) was used
to convert total oxygen consumed to total energy consumed during
incubation.
Water vapour conductance of eggs
The water vapour conductance of pelican eggs was measured in the laboratory
to investigate whether O2 uptake becomes limited during late
incubation. Eggs were removed from the routine incubator and placed in sealed
desiccators (containing anhydrous silica gel) maintained at 36°C within a
constant-temperature cabinet. The mass change of the developing eggs was
determined 24 and 48 h later, and the eggs were returned to the routine
incubator (45-55% relative humidity). Water vapour conductance was determined
for individual eggs from the mean water loss rate according to Ar et al.
(1974) after correcting to
standard temperature (25°C).
Statistical analyses
Linear regression was used to examine relationships between variables by
the method of least squares. Regression statistics are presented with the
standard error of the regression coefficient (sb). Mean
values are presented with 95% confidence intervals, unless stated otherwise,
and sample size (N). Student's t-tests were performed on
untransformed data. The significance of differences was accepted at the 5%
level.
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Results |
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The composition of freshly laid pelican eggs is presented in
Fig. 1 for 18 eggs ranging in
mass from 140.6 to 190.4 g. Both the wet and dry yolk content of eggs were
independent of fresh egg mass, so most of the variation in egg composition was
attributable to significant increases in water content of albumen, and to a
lesser extent eggshell, with increasing egg mass
(Table 1). Allometric analyses
did not provide a better fit for any of the regression models of egg and
hatchling composition and are therefore omitted. Wet yolk mass accounted for
21% of fresh egg contents in this study. This value is less than the 28%
reported for smaller P. occidentalis eggs
(Lawrence and Schreiber,
1974), but a little higher than the 17.5% found in P.
erythrorhynchos eggs of similar fresh mass
(Bugden and Evans, 1997
).
Further, our mean wet yolk mass is similar to the 22% for pelecaniforms in
general (Vleck and Bucher,
1998
). The total energy content of both the egg contents
(r2=0.043) and the yolk were independent of fresh egg mass
(r2=0.005), while albumen energy content was weakly
correlated with egg mass (r2=0.249, P<0.036).
The mean total egg energy content was 635±26 kJ (N=18) in this
study.
|
|
Yolk-free embryo mass was, on average, 22.3 g (N=3) on day 24, or 72% of the incubation period, and increased in a curvilinear fashion with age (Fig. 2). The wet mass of yolk-free pipped embryos overlapped considerably with that of the yolk-free hatchlings. Whole hatchling masses of pelicans hatched in the laboratory were 68.2±2.7% (N=13) of initial egg mass. Residual yolks represented an average of 17.5% (N=4) of whole embryo mass in externally pipped embryos and 12.6±1.0% (N=14) of whole hatchling mass. The residual yolk of both pipped embryos and hatchlings consisted of 65.9±2.0% (N=18) water, significantly more than found in the fresh yolk (55.2±1.8%), but the water content of whole hatchlings was similar to the total initial egg water content (84.2 versus 87.8±0.8%). The energy contents of yolk-free hatchlings and their residual yolks were 301 kJ and 147 kJ, respectively (Table 1). Energy consumed during incubation (including energy remaining as the meconium and that transferred to the chorioallantois during development) was therefore 635 kJ (egg) minus 448 kJ (whole hatchling), or 187 kJ according to direct calorimetry.
|
Pipping and incubation times
Eggs incubated artificially (>75% incubation) at a mid-egg temperature
of 35°C internally pipped (IP, piercing of inner shell membrane and
breathing in the airspace) on day 32, externally pipped (EP, breaking of the
eggshell and breathing of external air) on day 33 and hatched on day 34. In
contrast, eggs incubated at 36°C pipped and hatched one day earlier. In
the field, embryos from the same colony were internally pipped (vocalizations
heard) on day 30-31, externally pipped on day 31-33 and hatched on most
occasions on day 32 or 33 (87 eggs determined to within ±1 day, mean
32.8±0.2 days, range 31-36 days).
Development of respiration
The rate of O2 consumption of embryos increased in an
approximately exponential fashion with incubation age for the first 25 days,
then increased at a lower rate and plateaued for 2-3 days before IP
(Fig. 3). As the O2
consumption rates of embryos incubated at 35°C were not significantly
different from those incubated at 36°C, the data were combined for the
pre-pipping period (mean Me=171.3±18.9 g). The
greatest increases in rates of O2 consumption to approximately
700-1200 ml day-1 occurred after IP. The development of
O2 consumption during the pipping period was quantitatively similar
at both temperatures; the O2 consumption rates of combined group
means were 1052±266 ml day-1 (N=8) for IP eggs,
1531±170 ml day-1 (N=30) for EP eggs and
1697±176 ml day-1 (N=18) for hatchlings.
|
Similar patterns of CO2 production were also found for both temperature groups as the respiratory exchange ratio (RER) was generally stable throughout the incubation period (Fig. 4). Mean RER was 0.71±0.01 for embryos (N=30) over the whole incubation period and 0.68±0.04 for hatchlings (N=14). Total O2 consumed during incubation was 11063 ml O2 over 33 days. Assuming 19.64 J ml-1 O2 consumed, pelicans consumed 217.3 kJ according to indirect calorimetry. The latter estimate is equivalent to 34.2% of the initial egg energy, or 1.29 kJ g-1 egg. Lack of variability in the egg mass of our sample used for respirometry, however, prevented us from analysing whether the total O2 consumed by individual eggs was related to initial fresh egg mass.
|
Eggshell water vapour conductance determined for respirometry eggs and
fertile eggs temporarily removed from the field was 166.2±7.4 mg
day-1 kPa-1 (N=45, age 1-33 days), after
correcting to 25°C. This conductance is lower than predicted by Ar and
Rahn (1978) on the basis of egg
mass (mean Me=172 g, 95% CI 164.2-222.5 mg
day-1 kPa-1), although not significantly so.
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Discussion |
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All avian eggs necessarily lose water because of the porous eggshell. This
allows the shell membranes to dry and provides a diffusive path for gas
exchange, as well as preventing the accumulation of water that is produced as
a byproduct of embryonic metabolism (Ar and
Rahn, 1980). Not surprisingly, the water content of the P.
conspicillatus hatchling at the end of incubation is a high 84.2%,
similar to the initial egg water fraction. With so few solids in the egg
contents and in the hatchling tissues, it is not surprising that the pelican
hatchling's energy density is a low 23.6 kJ g-1 dry mass. This
value is similar to the average of many other seabird species, although higher
than some extremely low values (three species <22 kJ g-1 and one
exceptional report for Gallus domesticus). All other species
reportedly have higher energy densities (mean for all species 25.3 kJ
g-1, N=34, 95% CI=24.3-26.2 kJ g-1) (from
Ar et al., 1987
;
Pearson, 1999
).
Total production efficiency of converting egg energy (minus residual yolk)
to yolk-free hatchling is 61.6%, higher than the mean of 56.9% for all
hatchling types (data from Ar et al.,
1987; Pearson,
1999
). Thus, P. conspicillatus appears to be as efficient
as columbiform, anseriform and galliform species and significantly more
efficient than the three pelagic-feeding seabird species (44.8-52.5%) that
were reported with low yolk-free hatchling energy densities, which is probably
attributable to the prolonged incubation periods and higher degree of
hatchling physiological maturity of the latter species in terms of mobility
and thermogenic capacity.
Regression analyses of egg and hatchling composition in the present study
suggest that the cost of development in pelicans varies very little,
irrespective of egg size. Jones
(1979) reported that fresh
yolk content increases significantly with egg mass (a 3.4 g yolk increase over
a 74 g increase in egg mass) in P. onocrotalus, although the relative
size of the yolk decreases, as seen in other species (cited in
Jones, 1979
). We found that
P. conspicillatus eggs differing by as much as 50 g in initial mass
contained nearly the same yolk mass (both wet and dry matter), so most of the
mass difference in egg size is attributable to increases in water content of
the albumen fraction with increasing egg mass
(Fig. 1;
Table 1). Precocial species are
commonly reported to invest disproportionately larger yolks and lipid stores
in larger eggs, which generally hatch with higher hatchling energy densities
and yolk reserves (Ricklefs et al.,
1978
; Birkhead,
1984
; Alisauskas,
1986
; Rohwer,
1986
; Arnold,
1989
; Østnes et al.,
1997
). Greater energy reserves in precocial species convey
survival advantages to the mobile hatchlings. In contrast, altricial species
show only weak correlations between yolk content and egg mass and generally no
correlation between lipid content and egg mass
(Ricklefs and Montevecchi,
1979
; Ricklefs,
1984
). An exception is Molothrus ater, which invests more
yolk and energy in larger eggs (Ankney and
Johnson, 1985
).
P. erythrorhynchos lays significantly larger first eggs than
second eggs, when present, and hatchlings from first eggs are larger than
those from second eggs (Evans,
1997). In this species, which is an obligate brood-reducing
species, there is considerable evidence that the reduced investment in the
second young conserves reproductive effort whilst providing viable insurance
against the loss of the first young during incubation or the early nestling
period. In contrast, the first-laid eggs of P. conspicillatus (not
necessarily a brood-reducing species) in this study were slightly larger than
the second-laid eggs (P<0.0016), but it is uncertain whether the 3
g difference confers any advantage to first-hatched chicks since initial yolk
energy is independent of egg mass in first and second eggs.
Development of respiration
The development of a clear plateau in O2 consumption after the
period of exponential increase during early incubation in the Australian
pelican resembles the pattern usually reported for large precocial species
(Hoyt et al., 1978; Vleck et
al., 1979
,
1980b
;
Ancel and Visschedijk, 1993
;
Booth and Sotherland, 1991
;
Prinzinger et al., 1997b
). The
2-3 day plateau in metabolic rate of P. conspicillatus is the longest
reported so far for an altricial species
(Fig. 3). Similar metabolic
plateaus have been reported for some semi-altricial penguin species
(Bucher et al., 1986
), but the
results appear inconclusive for other penguin species
(Adams, 1992
;
Brown, 1988
) and the only
other pelican species investigated, P. occidentalis
(Bartholomew and Goldstein,
1984
). The results for very large altricial species lend further
support to the hypothesis that the development of embryonic metabolism is not
inherently different between hatchling maturity types
(Prinzinger and Dietz, 1995
;
Prinzinger et al., 1995
,
1997b
), as first believed
during the period of the pioneering comparative studies
(Hoyt et al., 1978
; Vleck et
al., 1979
,
1980a
,b
).
The most noticeable divergence in the developmental patterns of metabolism
between phyletic groups is the level of metabolic rate attained immediately
before IP and the initiation of pulmonary respiration. To normalise
interspecific comparisons of O2 consumption, 80% of incubation time
is routinely used to provide the pre-internal pipping rate. On this basis, the
729 ml day-1 at 26.5 days in P. conspicillatus is only 71%
of the predicted uptake rate (95% CI=851-1220 ml day-1) according
to the allometric relationship for all hatchling types
(Rahn and Paganelli, 1990).
Even on day 30, the last day of pre-pipping incubation, the rate is only 907
ml day-1 or 89% of the predicted rate. Since both altricial and
precocial taxa appear to be represented by species with less than predicted
prepipping rates as frequently as by species with higher than predicted rates
(Ackerman et al., 1980
; Pettit
et al.,
1982a
,b
;
Rahn and Paganelli, 1990
),
pre-pipping O2 consumption rate appears not to be strictly related
to the degree of cellular differentiation and maturation of tissue function
that varies between developmental modes.
The most suitable convention for analysing the physiological maturity of
avian embryos and hatchlings is to compare the mass-independent metabolic rate
(MIM) of the young of any species with that of an adult of the same species or
genus (Bucher, 1986,
1987
). We assume a similar
metabolic rate for adult P. conspicillatus and P.
onocrotalus of similar body mass
(Shmueli et al., 2000
). The
hatchling-to-adult MIM ratio of P. conspicillatus is 0.348 [mean
minimal RMR (resting metabolic rate) of hatchling 3.23 ml g-0.67
day-1 divided by adult BMR (basal metabolic rate) of 9.27 ml
g-0.67 day-1], which suggests that P.
conspicillatus hatches with a very low degree of physiological maturity,
like most other altricial species and in contrast to more precocial
developmental modes (range of ratios 0.2-0.6 versus 0.4-1.0; see
Bucher, 1987
). This is not
unexpected considering the high hatchling water content (84.2%), similar to
the mean of 83.8% reported for many small altricial species
(Ar and Rahn, 1980
). As in
other avian species, a high hatchling water content correlates with a low
metabolic activity (total rate of O2 uptake). Although large
hatchling size confers the advantage of lower heat loss per gram body mass in
precocial species, the acquisition of a high metabolic rate in pelican species
at hatching would be energetically disadvantageous since the parents do not
construct insulative nests and hatchlings have essentially no insulative down
to minimise the rate of heat loss when not parentally brooded. However, high
hatchling water content and the more immature (proliferative) state of tissues
might benefit pelicans that achieve more rapid postnatal growth than in
precocial species, since there is a trade-off between mature function and
growth rate in birds (for a review, see
Ricklefs et al., 1998
).
Embryonic growth and production efficiency
The pattern of embryo growth in P. conspicillatus conforms well to
the results described for P. occidentalis
(Bartholomew and Goldstein,
1984). On day 24 of the 33 day incubation, yolk-free embryo wet
mass is approximately 20% (22.3/102.6) of the final hatchling wet mass
(Fig. 2). More than 40% of
embryo growth occurs between the 85th and 95th
percentiles of incubation, at the end of pre-pipping development, which
suggests that in pelicans growth is very rapid over the shorter than expected
incubation period (predicted 36 days according to
Rahn et al., 1974
) and, more
importantly, that most of growth is relatively later in incubation. Rapid cell
proliferation during the pipping phase of incubation is apparent from the
increases in wet embryo mass; however, we do not know how the rate of solid
accumulation in embryonic tissues changes during incubation. We can therefore
only speculate that the high total production efficiency of P.
conspicillatus hatchlings; at 61.6%, might be achieved by a low rate of
increase in tissue energy density per gram dry matter, since the hatchling
energy density is low. Further, Ricklefs
(1987
) found that the rate of
dry matter accumulation itself is low in P. occidentalis and other
altricial species.
The average cost of development in P. conspicillatus is 1.11 kJ
g-1 egg mass according to direct calorimetry (mean
Me=170 g), but 1.29 kJ g-1 according to
respirometry (mean Me=171 g). Both estimates are among the
lowest costs of development reported to date in birds
(Bucher and Bartholomew,
1984). However, if the same amount of energy is invested in all
P. conspicillatus eggs, then a larger egg might produce a larger
hatchling at a lower cost of development per gram of egg than a smaller egg,
unless there is intraspecific variability in production efficiency.
Unfortunately, our sample of eggs for respirometry is not sufficiently
variable in egg mass to be able to determine whether the total O2
consumed is related to fresh egg mass.
Is O2 uptake limited during late incubation?
Most of embryonic growth in P. conspicillatus occurs during the
last 25% of incubation (Fig.
2), resulting in a significant reduction in available yolk energy.
Embryonic metabolic rate plateaus before IP, during the period of greatest
embryonic growth and increasing maintenance energy requirements, as in
precocial species (Vleck et al.,
1979). The present study supports the view of Bucher et al.
(1986
) and suggests several
reasons why an O2 uptake limitation imposed by the fixed eggshell
gas conductance is unlikely to cause the plateau in metabolic rate observed in
P. conspicillatus. Soon after IP, when pulmonary and chorioallantoic
respiration modes are functional, there is no significant increase in
O2 uptake rate in spite of the removal of the diffusion limitation.
The calculated O2 partial pressure gradient across the eggshell at
pre-IP is 5.46 kPa (41 mmHg), identical to the average gradient of avian
embryos in general (Rahn et al.,
1974
). Therefore, gas conditions within the air-cell of P.
conspicillatus eggs are not exceptionally hypoxic. Both P.
conspicillatus and semi-altricial Pygoscelis adeliae eggs have a
lower than expected water vapour conductance on the basis of egg mass, but the
plateau rate of O2 uptake prior to IP in the former is much lower
(80% of predicted, 95% CI 540-1542 ml day-1) than is predicted by
water vapour conductance (Rahn et al.,
1974
) and in the latter species much higher (829 ml
day-1=123% of predicted, 95% CI 340-809 ml day-1; see
Bucher et al., 1986
) than
predicted. It remains to be determined whether the synthetic efficiency of
embryonic tissue production increases during late incubation in altricial
species, as reported for galliforms (Dietz
et al., 1998
), which is an alternative explanation for the plateau
in metabolic rate.
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Acknowledgments |
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References |
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