The metabolic cost of avian egg formation: possible impact of yolk precursor production?
Department of Biological Sciences, Simon Fraser University, Burnaby, 8888 University Drive, Burnaby, V5A 1S6, Canada
* Author for correspondence (e-mail: fvezina{at}sfu.ca)
Accepted 2 September 2003
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Summary |
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Key words: egg production, energy cost, resting metabolic rate, RMR, vitellogenin, very-low-density lipoprotein, zebra finch, Taeniopygia guttata, yolk precursor production
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Introduction |
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Another component of egg production that is likely to be energetically
costly is the increased liver activity involved in protein and lipid
production for oogenesis. During the process of egg formation, the
hypothalamus initiates a hormonal cascade by releasing gonadotropin-releasing
hormone (GnRH), which induces the release of follicle-stimulating hormone
(FSH) and luteinizing hormone (LH) from the pituitary gland
(Williams, 1998;
Scanes, 2000
). These hormones
stimulate the ovary to produce estrogens
(Williams, 1998
), which then
trigger the production of the egg-yolk precursors, vitellogenin (VTG) and
yolk-targeted very-low-density lipoprotein (VLDLy), by the liver
(Bergink et al., 1974
;
Deeley et al., 1975
;
Wallace, 1985
;
Walzem, 1996
;
Williams, 1998
), which are
then secreted into the blood. During rapid yolk development, plasma VTG and
VLDLy are taken up by the ovary and are processed within the follicles into
yolk, the nutrient and energy source for the developing avian embryo
(Bernardi and Cook, 1960
;
Stifani et al., 1988
;
Wallace, 1985
). In laying
domestic hens (Gallus gallus domesticus), approximately 50% of the
liver's daily protein synthesis is attributed to VTG production, potentially
tripling the amount of protein in circulation
(Gruber, 1972
). Hepatic lipid
production also increases markedly during this time (from 0.51.5
µmol triglyceride ml-1 plasma in non-breeders to 2050
µmol triglyceride ml-1 plasma in laying hens;
Griffin and Hermier, 1988
), as
VLDL synthesis shifts from the exclusive production of non-laying, generic
VLDL to an increase in the hepatic synthesis of estrogen-dependent VLDLy
(Walzem, 1996
;
Walzem et al., 1999
). The
presence of circulating VLDLy represents a dramatic shift in lipid metabolism
as the structure and function of plasma VLDL particles change from larger,
generic VLDL, which are involved in triglyceride (i.e. energy) transport
within an individual, to smaller VLDLy, which supply the yolk with energy-rich
lipid (Walzem, 1996
;
Walzem et al., 1999
). These
changes in protein and lipid metabolism are likely to be energetically costly
as they are associated with an increase in the activity of the liver and
potentially other organs involved in reproduction, such as the ovary.
However, in female starlings, there is no relationship between laying RMR
and lean dry liver mass or plasma levels of the yolk precursors in individuals
having 15 yolky follicles left to ovulate
(Vézina and Williams,
2003). Nevertheless, this does not mean that yolk precursor
production is not energetically costly. Liver mass per se may not be
representative of the liver's metabolic intensity, i.e. the amount of energy
consumed per unit tissue mass. Furthermore, the elevated RMR reported in
laying starlings was measured during active laying when yolk precursor levels
were already maintained at an elevated level
(Challenger et al., 2001
;
Vézina and Williams,
2003
). It is possible that laying female plasma is saturated with
yolk precursors, with minimal rate of production by the liver and therefore no
relationship with RMR. Alternatively, the elevated precursor levels may be the
result of a balance between high hepatic production and high ovary uptake
rate. Consequently, comparing precursor levels with RMR in active layers may
be problematic and potentially misleading.
To measure the metabolic cost of yolk precursor production accurately, one
has to measure the animal's metabolic rate at a time when the liver is known
to be actively involved in VTG and VLDLy synthesis. In the present study, we
documented the pattern of yolk precursor production in zebra finches
(Taeniopygia guttata) in response to daily injections of
17ß-estradiol (E2) and measured the potential metabolic cost
of VTG and VLDL production by respirometry. Zebra finches represent a very
good model species for this type of study because: (1) ongoing work in our lab
has shown that mass-corrected RMR is 26% higher at the one-egg stage than
at the non-breeding stage (F. Vézina, K. G. Salvante and T. D.
Williams, unpublished), which is very similar to reported values for starlings
(Vézina and Williams,
2002
) and great tits (Parus major;
Nilsson and Raberg, 2001
); (2)
the pattern of yolk precursor production during the laying cycle is known and
similar to the one reported in starlings
(Salvante and Williams, 2002
;
Challenger et al., 2001
) and
(3) this species responds in a known manner to E2 injections
(Williams and Martyniuk,
2000
). We used E2 doses adjusted to generate plasma
yolk precursor levels within the normal range for breeding females at the peak
of investment (one-egg stage; Williams and
Ternan, 1999
). We then measured RMR in dosed individuals during
the period of known hepatic activity. In order to evaluate the metabolic cost
of yolk precursor production, we compared this RMR value with the metabolic
rate previously measured in all individuals.
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Materials and methods |
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Estradiol treatment
We know from previous studies that administration of E2 to
female zebra finches triggers partial development of the oviduct
(Williams and Martyniuk,
2000). Because the maintenance and activity costs of the oviduct
have previously been shown to be related to metabolic rate
(Chappell et al., 1999
;
Vézina and Williams,
2003
), we avoided any confounding effects in our results by using
male zebra finches as models for this experiment. Males react to E2
injections by producing yolk precursors in the same fashion as females
(Bergink et al., 1974
;
Follett and Redshaw, 1974
).
Various E2 doses were tested (F. Vézina, K. G. Salvante and
T. D. Williams, unpublished results) in order to generate a response in plasma
yolk precursor levels comparable with normal female breeding values. The final
dose used in this study was 1.5 µg g-1 (assuming a mean mass of
17 g for all birds) of E2 dissolved in corn oil (No Name Pure Corn
Oil, Toronto, Canada).
Experiment 1: pattern of yolk precursor plasma levels in response to
daily E2 injections
In order to determine the best possible timing of RMR measurement in
relation to the estradiol treatment, we had to document the rise in
circulating yolk precursor levels in response to the E2 treatment.
Only VTG was monitored, since both precursors have been reported to respond
similarly to E2 injections in zebra finches
(Williams and Martyniuk,
2000). For this experiment, 32 male zebra finches were used. The
birds were divided into five groups, and all birds received a daily
E2 injection (30 µl, i.m.) over four consecutive days (days
14; Fig. 1A). Starting
from the day following the first injection, one group of birds was blood
sampled each day until two days following the last injection (sample sizes
were 4, 9, 5, 10 and 4 for days 26, respectively;
Fig. 1A). All birds were blood
sampled only once from the brachial vein. We also repeated this experiment
using females (N=23) to confirm that both sexes responded the same
way to the estradiol treatment.
|
Experiment 2: metabolic costs of yolk precursor production
For this experiment, we used 32 males randomly assigned to one of two
groups: E2 (injected with E2 in corn oil; N=16)
and sham (corn oil only; N=16). We used a repeated measures design
where each bird was used as its own control in order to monitor changes in RMR
due to E2 administration within a bird. The experiment lasted 11
days and proceeded as follows (Fig.
1B): on the night preceding day 1, all birds had their RMR
measured by respirometry (protocol described below) and were blood sampled the
following morning (day 1). These data will be referred to as `pre-treatment'.
Estradiol and sham injections (30 µl, i.m.) started the morning of day 7
and lasted four consecutive days until day 10. Results from experiment 1 led
us to measure RMR on the night following the second day of injections, i.e.
day 8 (see justification in the Results section), and all birds were blood
sampled again the following morning (day 9), from here on referred to as
`mid-treatment'. The injections were then continued until day 10 to ensure
that the liver was actively producing yolk precursors at the time of RMR
measurement (i.e. no plateau in precursor levels). This was confirmed by a
final blood sample on day 11, from here on referred to as
`post-treatment'.
Measurement of resting metabolic rate
Blem (2000) defines basal
metabolic rate (BMR) as the energy consumed by a post-absorptive bird during
the resting phase of the circadian cycle at a temperature within the
thermoneutral range for the animal. By definition, BMR is the lowest
measurable consumption of oxygen uptake. Because birds in the second part of
experiment 2 were artificially stimulated to produce yolk precursors, we
considered them to be in an `active physiological state' that may induce
elevated levels of energy consumption. Therefore, although the first set of
metabolic rate measurements (i.e. pre-treatment) may fall under Blem's BMR
definition (last meal at least 3 h before beginning of measurements), we use
the term resting metabolic rate throughout the paper for convenience
(note that all of our measurements were taken at thermoneutrality, which is
often not the case for resting metabolism reported in the literature;
Blem, 2000
). All RMR
measurements were completed using a flow-through respirometry system (Sable
Systems International, Henderson, NV, USA). Birds were taken from their cages,
their body mass was measured (±0.1 g) and they were placed randomly in
one of four metabolic chambers (1.5 liter) for one hour prior to the beginning
of RMR measurements. All chambers continuously received approximately 500 ml
min-1 of dry CO2-free air (using DryriteTM and
ascariteTM as scrubbers) and were kept in the dark at 35°C, which is
within the thermoneutral zone for this species (lower critical temperature =
33°C; Meijer et al.,
1996
). RMR measurements were always started at 00:00 h. Our setup
consisted of four metabolic chambers connected to a divided air line with a
valve multiplexer that allowed us to sample air coming from either ambient
baseline air (scrubbed for water and CO2) or from one metabolic
chamber at a time. The air was then passed through a mass flow valve (Sierra
Instruments, Monterey, CA, USA) for proper air flow reading (STP corrected)
and through CO2 and oxygen analyzers (model CA-1 and FC-1,
respectively; Sable Systems International; air was water scrubbed before
CO2 analyzer, and water and CO2 scrubbed before
O2 analyzer). All measurement sequences started by recording 10 min
of baseline air. After baseline recording, the multiplexer switched, and the
out-flowing air from the first chamber was sampled for 55 min. Then the system
switched back to baseline for 10 min before changing again to the second,
third and fourth chambers. Preliminary analysis showed that measuring RMR
using this protocol did not generate a time effect (sensu
Hayes et al., 1992
) on RMR
(F3,15=0.48, P=0.7). The birds stayed in their
chambers for approximately 5 h. After RMR measurement, the birds were weighed
for a second time and the average of first and second masses was used in
subsequent analysis. To calculate RMR, a running mean representing 10 min of
recording was passed through the data for each bird, with the lowest mean
taken as RMR.
Yolk precursor analysis
In order to measure circulating levels of VTG and VLDL, blood samples were
centrifuged at 2200 g for 10 min, and the plasma portion of
each sample was isolated. Plasma samples were then assayed for vitellogenic
zinc (Zinc kit; Wako Chemicals, Richmond, VA, USA) using the method developed
for the domestic hen (Mitchell and
Carlisle, 1991) and validated for passerines
(Williams and Christians,
1997
; Williams and Martiniuk, 2000;
Challenger et al., 2001
;
Salvante and Williams, 2002
).
The concentration of vitellogenic zinc is proportional to circulating levels
of VTG (Mitchell and Carlisle,
1991
). The overall inter-assay coefficient of variation for the
vitellogenic zinc assay (calculated from repeated analyses of a reference
sample) was 14.2% (N=9 assays).
Circulating VLDL was assessed by measuring plasma triglyceride levels
(Triglyceride E kit; Wako Chemicals) according to the method of Mitchell and
Carlisle (1991). Plasma
triglyceride has commonly been measured in non-domesticated birds as an index
of total plasma VLDL, which consists of both the generic and yolk-targeted
forms of VLDL (Williams and Christians,
1997
; Williams and Martyniuk,
2000
; Challenger et al.,
2001
). Despite the marked increase in circulating lipid levels
reported during egg production (Griffin
and Hermier, 1988
; Walzem et al.,
1994
,
1999
;
Walzem, 1996
), in
vivo studies on laying poultry hens have detected only low circulating
levels of intermediate-density and low-density lipoproteins, both by-products
of the metabolism of generic VLDL, suggesting that VLDLy is resistant to
metabolism by laying hens (Hermier et al.,
1989
; Walzem et al.,
1994
; Walzem,
1996
). These studies provide evidence that the marked increase in
total VLDL during avian egg production or following estrogen administration is
the result of increased synthesis of the estrogen-dependent VLDLy component of
total VLDL. The overall inter-assay coefficient of variation for the
triglyceride assay (calculated from repeated analyses of a reference sample)
was 10% (N=5 assays). All assays were run using 96-well microplates
and measured using a Biotek 340i microplate reader (Winooski, VT, USA).
Statistical analysis
All data were tested to ensure normality (ShapiroWilk test;
Zar, 1996). Plasma yolk
precursor levels violated normality for both the production pattern experiment
and the RMR experiment. Vitellogenin data from the first experiment were log
transformed (adding 0.001 to all data to eliminate zeros) to achieve
normality. Analysis of the precursor production pattern was therefore carried
out on log-transformed data using standard parametric methods (see below). For
clarity, yolk precursor production pattern data are presented non-transformed
in Fig. 2. By contrast, log
transformation of VTG and VLDL data for the RMR experiment did not result in
normally distributed data. Therefore, non-parametric tests were performed (see
below) when the analysis included VTG or VLDL data. For all other analysis,
standard parametric statistics were used since all other variables were found
to be normally distributed.
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Contrary to the results of preliminary testing (see above), there was a
significant time effect on RMR in experiment 2 when controlling for body mass
(pre-treatment: F3,27=2.99, P<0.05;
mid-treatment: F3,26=3.57, P<0.05). This
effect translated into a decreasing RMR over time, but with a difference of
less than 10% between measurements for either the first or last chamber
relative to the mean of all chambers. Overall, pre- and mid-treatment RMR of
birds in the first metabolic chamber was, respectively, 3.04 ml O2
h-1 (7.1%) and 2.10 ml O2 h-1 (4.7%) higher
than the mean for the four chambers (42.57 ml O2 h-1 at
pre-treatment and 44.36 ml O2 h-1 at mid-treatment),
while the RMRs of birds in the fourth metabolic chamber were 3.25 ml
O2 h-1 (7.6%) and 4.21 ml O2 h-1
(9.5%) lower, respectively. The range of maximal differences in the RMR of
birds measured first (chamber 1) compared with birds measured last (chamber 4)
within the same night spanned from -30.0% to +7.7% of RMR associated with
chamber 1 at pre-treatment (mean difference: -15% of mean all-chamber RMR).
For mid-treatment, this range was -26.7% to +32.6% (mean difference: -7% of
mean all-chamber RMR). However, when considering maximal differences in RMR of
birds measured twice in the same chamber throughout the experiment
(N=7), the range spanned from -22.7% to 30.0% of the first RMR
measurement, indicating that the time effect is within the natural individual
variation in RMR measurements. Indeed, this time effect proved to be weak
since post-hoc analysis, using Bonferroni correction for multiple
comparisons (Rice, 1989),
revealed only a marginally significant difference (P=0.0074, with
level of significance corrected to P<0.008) between first and last
chambers at pre-treatment but failed to detect any significant differences in
RMR between birds held in different chambers at mid-treatment. We nevertheless
used a conservative approach and included time in the model when correcting
RMR for the effect of body mass. In order to evaluate changes in RMR within
individual birds throughout the experiment, we used repeated measures analysis
of variance (ANOVA). To control for the effect of body mass in this model we
averaged pre- and mid-treatment masses and included it in the model as a
covariate (body mass was highly repeatable between pre- and mid-treatment;
r2=0.89, N=32, P<0.0001). However,
because we randomized the position of the birds in their metabolic chambers,
we were not able to control for the time effect (i.e. the birds were not
consistently put in the same chambers). We do not believe that this introduced
a systematic bias. As mentioned earlier, the only detectable time effect was
recorded between measurements for chambers 1 and 4 at pre-treatment. However,
only seven of 32 birds were measured in these two chambers over the two
measurement periods. Out of these seven, only four individuals had their RMR
measured in chamber 4 at pre-treatment and in chamber 1 at mid-treatment,
which would artificially increase their RMR. Data are reported as means
± S.E.M.
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Results |
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Experiment 2: metabolic costs of yolk precursor production
Based on the results obtained in the first experiment, we measured RMR
during the night between the second and third day of E2
administration (night of day 8; Fig.
1B). At this point, VTG levels were still lower than normal
one-egg stage values (MannWhitney test, U=137.00,
P<0.005; Salvante and
Williams, 2002), and it is clear that the liver was actively
synthesizing yolk precursors, as plasma VTG increased for at least two more
days (Fig. 2).
There was no difference in body mass between E2-treated and sham birds measured either at pre-treatment or mid-treatment (pre-treatment t-test, t30=0.21, P=0.8; mid-treatment t-test, t30=0.52, P=0.6). Within groups, there was no treatment-related changes in mass in E2-treated individuals (paired t-test, t15=1.41, P=0.2). However, sham birds lost 2% of their mass between the two RMR measurements (paired t-test, t15=2.52, P<0.05), decreasing from 15.0±0.4 g to 14.6±0.4 g.
As in experiment 1, VTG production significantly increased in
E2-treated individuals (Friedman test, 2=27.22,
d.f.=2, P<0.001; Fig.
3A), while levels in sham birds remained below the range of VTG
for breeding females (Williams and
Christians, 1997
; Salvante and
Williams, 2002
) and showed no significant change throughout the
experiment (
2=1.97, d.f.=2, P=0.3;
Fig. 3A). Differences between
groups were evident at all periods of the experiment. At pre-treatment, sham
birds had significantly higher levels of plasma VTG than E2-treated
birds (MannWhitney test, U=53.00, P<0.005;
Fig. 3A). However, VTG levels
in both groups were low and representative of typical non-breeding birds
(Williams and Christians,
1997
). Therefore, this difference is not biologically relevant. At
mid- and post-treatment, E2 birds exhibited significantly higher
levels of VTG than sham individuals (MannWhitney test, mid-treatment,
U=34.00, P<0.001; post-treatment, U=22.00,
P<0.0001; Fig. 3A),
with VTG levels averaging 1.59 µg ml-1 at post-treatment. This
is lower than the reported maximum for the first experiment and it is not
clear why the same E2 dose resulted in different precursor levels.
However, plasma VTG levels reported in experiment 2 are much closer to the
natural breeding level of 1.68 µg ml-1
(Williams and Christians,
1997
).
|
Estradiol administration had a similar effect on the pattern of VLDL
production, with plasma levels significantly increasing in
E2-treated individuals (Friedman test, 2=11.38,
d.f.=2, P<0.005; Fig.
3B). One individual had a surprisingly high VLDL level (106 mg
ml-1) at pre-treatment. Taking this individual out of the analysis
made the increase in plasma VLDL in the E2 group more marked
(including outlier: 12.64±6.40 mg ml-1 at pre-treatment to
15.71±3.05 mg ml-1 at post-treatment; excluding outlier:
6.42±1.58 mg ml-1 at pre-treatment to 13.51±2.25 mg
ml-1 at post-treatment) and did not change the overall effect of
estradiol administration on plasma VLDL levels (Friedman test,
2=13.73, d.f.=2, P<0.005). Conversely, sham
individuals showed no change in plasma VLDL (Friedman test,
2=4.88, d.f.=2, P=0.08;
Fig. 3B). These results
translated into no significant difference between groups at pre-treatment
(MannWhitney test, pre-treatment, U=97.00, P=0.4),
61% higher VLDL levels in E2-treated birds at mid-treatment
(MannWhitney test, mid-treatment, U=57.00, P<0.05)
and 109% higher VLDL levels at post-treatment (MannWhitney test,
post-treatment, U=45.00, P<0.005). The maximal VLDL level
reported here (post-treatment levels in E2-treated birds, 13.51 mg
ml-1) is 28% lower than previously reported values for female zebra
finches at the one-egg stage (18.87 mg ml-1;
Williams and Christians, 1997
)
but still within the natural wide range of variation for this
lipoprotein (6.454.5 mg ml-1;
Williams and Christians,
1997
).
Pre-treatment RMR did not differ between the experimental groups (F1,26=0.21, P=0.7) but was positively related to body mass (F1,26=8.76, P<0.01). While mid-treatment RMR was also related to body mass (F1,26=10.50, P<0.005), estradiol injections and increased yolk precursor production did not result in higher RMR in E2-treated birds compared with sham individuals (F1,26=0.34, P=0.6; Fig. 4). Similarly, E2-treated and sham groups did not differ in their RMR response to injections over time (repeated measures ANOVA, treatment x time interaction, F1,29=0.01, P=0.9) Indeed, repeated measures ANOVA revealed no significant changes in RMR between pre- and mid-treatment measurements when controlling for body mass (F1,29=0.24, P=0.6). Mid-treatment RMR was not correlated with circulating VTG or VLDL levels at mid- or post-treatment (Spearman rank correlation, P>0.3 in all cases) in E2-treated birds.
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Discussion |
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Comparing our values of RMR with those from the literature suggests that
our respirometry technique provided robust estimates of BMR. Resting metabolic
rate in pre-treated birds was 42.6 ml O2 h-1, which is
equivalent to 18.821.3 kJ day-1 for energy substrate going
from protein to carbohydrates
(Schmidt-Nielsen, 1990; mean
respiratory quotient was 0.76, which indicates that the birds could be using
energy from mixed sources, which complicates the energetic conversion). This
is almost identical to BMR estimates of 19.7 kJ day-1 for zebra
finches reported by Gavrilov
(1997
). Our estimate of RMR in
pre-treated birds (2.8 ml O2 h-1 when using our mean
body mass of 15.1 g) is also very similar to Vleck's published results for
incubating zebra finches at 35°C (3.0 ml O2 h-1 in
fig. 2 of
Vleck, 1981
).
However, despite an 80-fold increase in circulating VTG and a 2-fold
increase in plasma VLDL in E2-treated birds, RMR, when measured
during active hepatic yolk precursor production, did not increase
significantly in E2-treated individuals compared with pre-treatment
measurements or sham individuals. This is consistent with the findings of
Vézina and Williams
(2003), which showed no
relationships between RMR and plasma VTG and VLDL in laying European
starlings. There is no other study that we are aware of that has specifically
investigated the metabolic cost of producing the yolk precursors.
Our results may be interpreted as a low energy investment in VTG and VLDL
synthesis. However, this would be surprising given the marked charges in
protein and lipid metabolism associated with rapid yolk formation
(Gruber, 1972;
Griffin and Hermier, 1988
). We
suggest that there might be an alternative explanation. There is accumulating
evidence that birds can adjust their energy consumption in a compensatory
manner when challenged by multiple, and perhaps competing, high-energy
demands. For example, a decrease in locomotor activity has been suggested to
compensate for the cost of molting (Austin
and Fredrickson, 1987
), for the reduced energy availability in
fasting birds (Cherel et al.,
1988
) and for the cost of egg formation
(Houston et al., 1995
;
Williams and Ternan, 1999
).
Similarly, the heat generated by feeding
(Masman et al., 1989
) or
foraging activity (Webster and Weathers,
1990
; Bruinzeel and Piersma,
1998
) has been shown to partially compensate for thermoregulatory
costs. It is clear that changes occurring in physiological systems and organs
within an individual may also result in compensatory effects leading to energy
reallocation with no net increase in overall energy consumption. For example,
Geluso and Hayes (1999
)
measured BMR and organ composition of starlings under high- and low-quality
diets. They found significant differences in the mass of the gastrointestinal
tract, gizzard, liver and breast muscle but no differences in BMR, indicating
that upregulation of certain organs or systems may be coincident with
downregulation of other systems or organs in order to maintain a constant
maintenance energy cost. The question of whether the higher hepatic activity
involved in VTG and VLDL production results in the downregulation of other
physiological systems remains to be resolved. Clearly, studies investigating
energy expenditure at the organ level are needed to elucidate this hypothesis.
We know from previous work in our laboratory that liver structural size does
not systematically increase in association with high levels of endogenous
plasma yolk precursor production in European starlings and zebra finches
(Christians and Williams,
1999a
; Williams and Martyniuk,
2000
; Vézina and
Williams, 2003
) or even in response to administration of exogenous
estradiol (Christians and Williams,
1999b
; Williams and Martyniuk,
2000
). If energy reallocation does take place during precursor
production, the metabolic intensity of the liver (i.e. energy consumption per
unit mass) may still be high during VTG and VLDL production even though
mass-corrected RMR was independent of plasma yolk precursor levels in our
study. A possible mechanism for this could be that the regulation of other
physiological systems is also triggered by a rise in plasma E2. For
example, immune function, which has been shown to have a measurable metabolic
cost (Demas et al., 1997
;
Raberg et al., 2001
;
Martin et al., 2002
), can be
inhibited by certain doses of estradiol in chickens
(al-Afalek and Homeida, 1998
;
Landsman et al., 2001
).
Therefore, a reduction in the activity of the immune system could potentially
lead to energy savings that can be reallocated to other functions.
This experiment was specifically designed to measure the potential costs of
yolk precursor production. However, the influence of other aspects of egg
formation on overall energy expenditure should also be examined. For example,
egg yolk mass is related to the rate of yolk precursor uptake at the ovary and
is potentially limited by the number of VTG/VLDL receptors and their rate of
recycling (Christians and Williams,
2001). Therefore, the very active process of rapid yolk
development may also result in substantial energy investment. These aspects of
egg formation cannot be assessed using males or even non-breeding females due
to the lack of developing ovarian follicles. Thus, more investigation is
needed to explain the remaining variation in elevated laying RMR
(Nilsson and Raberg, 2001
;
Vézina and Williams,
2002
) not accounted for by the maintenance and activity costs of
the oviduct (Vézina and Williams,
2003
).
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Acknowledgments |
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References |
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