The metabolic cost of egg production is repeatable
Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, V5A 1S6, Canada
* Author for correspondence at present address: Royal Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1790 AB Den Burg, Texel, The Netherlands (e-mail: fvezina{at}nioz.nl)
Accepted 4 May 2005
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Summary |
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Key words: basal metabolic rate, resting metabolic rate, repeatability, egg production, reproduction, zebra finch, Taeniopygia guttata
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Introduction |
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Here, we show that resting metabolic rate (RMR; our estimator of BMR, see
Materials and methods) is repeatable in relation to physiological state, in
non-breeding and egg-producing zebra finches Taeniopygia guttata. We
have previously shown, in European starlings Sturnus vulgaris, that
egg formation induces a 22% increase in RMR over pre-reproductive values
(Vézina and Williams,
2002), which is comparable to data reported for other free-living
avian species (house sparrows Passer domesticus, 16% over
non-breeding BMR; Chappell et al.,
1999
; great tits Parus major, 27% over-wintering RMR;
Nilsson and Raberg, 2001
).
However, these observations were made on free-living animals where RMR might
be confounded by variation in ecological conditions via effects on
non-reproductive physiological `machinery' (organ mass or metabolic activity),
which might independently contribute to measured variation in RMR
(Vézina and Williams,
2003
). We conducted a study in controlled, laboratory conditions,
allowing for an unbiased estimate of the metabolic cost of egg production,
eliminating the confounding effects of natural variations in ecological
condition. We predicted that there would be a similar state-dependent change
in RMR in laying zebra finches allowing us to (1) estimate the energetic
investment associated with reproductive effort measured as egg production in
zebra finches, (2) determine relationships between RMR in laying birds and
measures of reproductive output (egg and clutch size), (3) estimate
repeatability for non-breeding and laying RMR to evaluate the level of
stability of this trait within individuals and between breeding attempts, and
(4) investigate the effect of time on repeatability of RMR over short (8 days)
and long (10 months) timescales.
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Materials and methods |
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Measurement of resting metabolic rate
Basal metabolic rate is defined as the energy consumed by a resting
post-absorptive animal during the inactive phase of the circadian cycle at a
temperature within the thermoneutral range for the animal
(Commission for Thermal Physiology of the
IUPS, 2001). However, since laying birds are producing eggs, they
have to be considered to be in an `active physiological state'
(Vézina and Williams,
2002
). We therefore consider the term resting metabolic
rate more appropriate in the present study. All resting metabolic rate (RMR)
measurements were completed using a flow-through respirometry set-up (Sable
Systems International; oxygen analyzer model FC-1, CO2 analyser
model CA-1) described elsewhere
(Vézina et al., 2003
).
Birds were taken from their cages within 1015 min after lights were
turned off, their body mass measured (±0.1 g), and were placed randomly
into one of four metabolic chambers (1.5 l) for approximately 1 h prior to the
beginning of RMR measurements. All chambers continuously received 500 ml
min-1 of dry CO2-free air 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 23:00 h. All
measurement sequences started by recording 20 min of ambient baseline air.
After baseline recording, the out-flowing air from the first chamber was
sampled for 33 min before switching to sampling the second chamber for 33 min.
Then the system sampled baseline air for 10 min before changing to the third
and fourth chambers. This cycle was repeated three times over the night (with
ten minutes of baseline in between each set of two chambers), giving 99 min of
recording per chamber over 8 h. After RMR measurement, the birds were
re-weighed and placed back into their cage (approximately 30 min to 1 hbefore
lights were turned on). To calculate RMR, the average of first and second
masses was used and
O2 was
calculated using a running mean representing 10 min of recording, with the
lowest average taken as RMR. This value was always found in the last 5 h of
the night. Preliminary analysis showed that measuring RMR using this protocol
did not generate a time effect (Hayes et
al., 1992
; ANOVA testing for chamber position in the measurement
sequence on mass-corrected RMR: F3,53=0.7,
P=0.5).
Experimental groups
To evaluate the relative increase in resting metabolic rate associated with
egg production in zebra finches, we compared RMR values for a given female
measured as non-breeder (NB; maintained in a single sex group), at laying (LY;
day of first egg laid) and at 17 days into the chick-rearing period (CK;
approximately 4 days before fledging). To estimate repeatability of LY RMR,
females were paired again after a resting period and RMR was measured a second
time at the one-egg stage. Since we could only measure four birds per night,
RMR was recorded for laying birds at the 1-egg (N=38) and two-egg
(N=7) stages to accommodate for days with more than four new layers.
RMR did not differ significantly between egg stages (1-egg RMR=52.0±0.9
ml O2 h-1; 2-egg RMR=50.0±1.7 ml O2
h-1; P=0.8). For repeatability of RMR in non-breeders,
birds and cage availability prevented us from measuring RMR repeatedly in all
females measured as LY. We, therefore, evaluated repeatability of NB RMR using
a group of birds composed of 42% of females that were not used in the breeding
protocol. As we were interested in the effect of time on RMR repeatability, in
a separate experiment, we measured RMR in a group of non-breeding males twice,
with measurements 8 days apart and then a third time 127-249 days later. Mean
RMR and body mass are presented in Table
1 with the respective sample sizes for each group.
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Statistical analysis
All data were tested to ensure normality (Shapiro-Wilk test;
Zar, 1996). To compare within
individual changes in RMR from the non-breeding to one-egg and chick rearing
stages, we used repeated measures analysis of covariance (ANCOVA) using body
mass as a covariate. We used the same method to investigate potential changes
in mean RMR measured twice as LY or NB stages. Repeatability of residual RMR
(effect of body mass factored out by regression analysis) was calculated
following the method proposed by Lessells and Boag
(1987
). Therefore, our
repeatability index reflects the amount of variation in RMR among rather that
within individuals. Post-hoc multiple comparisons between groups
where performed using the Bonferroni procedure to reduce the risk of
committing type I errors (Rice,
1989
). Data are reported as mean ± S.E.M.
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Results |
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In non-breeding females, we measured RMR twice over a period of time spanning 13311 days. Repeatability of residual RMR in these birds was 51.6% (F36,37=3.1, P<0.0005; Fig. 3A). Including the delay between measurements in a multiple regression model showed that the relationship between first and second RMR measurements was still significant when time was taken into account (time effect P<0.05, RMR1 effect on RMR2: P<0.001, no significant interaction term; overall model r2=0.35, N=37, P<0.001). Repeated measures ANCOVA showed a 5.9% increase between first and second RMR measurement when controlling for body mass (F1,37=10.3, P<0.005; Fig. 4). Comparing data on initial NB RMR for males and females, we found that RMR was independent of sex when controlling for body mass (ANCOVA; P=0.3, no significant interaction term between sex and body mass).
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We measured RMR in laying females twice over a period spanning 38 to 254 days. Repeatability of residual RMR was 52.6% (F18,19=3.22, P<0.01; Fig. 3B) and multiple regression showed no effect of delay between measurements in this particular data set (time effect P=0.8). Repeated measures ANCOVA showed no significant differences between the first and second LY RMR measurement when controlling for the effect of body mass (P=0.4, no significant interaction between body mass and measurement sequence; Fig. 4) meaning that absolute mean LY RMR values did not change between breeding attempts.
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Discussion |
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An interesting finding is that zebra finches at the chick-rearing stage
show a 13% higher RMR compared to non-breeding values. This difference is
clearly not the result of partially or non-regressed reproductive organs since
this happens very rapidly, within a day of the final ovulation, in this
(Williams and Ames, 2004) and
other species (Vézina and Williams,
2003
). It appears that resting metabolic rate in chick-rearing
individuals reflects a physiological state that differs from that in both
non-reproductive and egg-producing birds (see also
Vézina and Williams,
2003
).
Although egg production induces a 22% increase in resting metabolic rate,
RMR was repeatable in both non-breeding and laying birds, i.e. individual
variation in RMR was consistent for a given physiological state. This may have
significant evolutionary consequences if the increase in RMR associated with
egg production is consistently posing a constraint on the animal's energy
budget; there is some evidence that this is the case. Williams and Ternan
(1999) showed that egg laying
zebra finches reduce their level of locomotor activity by 46% while food
intake actually decreases by 8%, suggesting that egg production may force
females to reallocate energy through behavioural strategies. Furthermore,
experiments where females have been induced to lay extra eggs and produce
larger clutch sizes showed several fitness consequences visible in lower egg
quality affecting chick survival (Monaghan
et al., 1995
; Nager et al.,
2000
), lower capacity of females to raise their brood
(Heaney and Monaghan, 1995
;
Monaghan et al., 1998
) and
lower female survival between years and reproductive success the year
following the experiment (Nager et al.,
2001
; Visser and Lessells,
2001
).
In contrast to RMR in egg-producing females, for which repeatability was
not affected by time, we found that repeatability of non-breeding RMR
decreased with time in both sexes and even that the average value changed
between measurements (by 5.9%) in females. Similar declines in repeatability
of metabolic rate over time in wild animals have been reported earlier
(measurements of BMR: Bech et
al.,1999;
O2,max:
Chappell et al., 1995
) but this
may not be surprising, given that ecological conditions, and their effects on
physiology, may vary between measurements. However, the reason for the
increase in interindividual variability in RMR over time in our controlled
system is not obvious. There is only one other study that we are aware of that
reported time effects on repeatability of BMR in captive birds. Horak et al.
(2002
) found a decreasing
level of repeatability in greenfinches Carduelis chloris going from
87% at 8 days between measurements to 63% at 4 months between measurements
(table 1 in Horak et al.,
2002
). In their case, however, the birds were maintained in
semi-natural conditions between the two sets of measurements (natural changing
photoperiod) which could explain part of the decrease in repeatability. A
potential explanation for our finding is that our non-breeding individuals
were kept in reserve cages forming large groups (1020 birds) between
measurements. Zebra finches are social birds and will form social hierarchies
when maintained in groups (Zann,
1996
). It is thus possible that social interactions and access to
food when birds are kept in non-breeding same-sex groups, affects some aspects
of individual physiology, such as fat content known for its potential
diluting effect on the body mass metabolic rate relationships
(Scott and Evans, 1992
) or
hormonal state, which may influence behaviour and thus energy expenditure
(Ramenofsky, 1984
; Wikelski et
al.,
1999a
,b
).
Therefore, changing group composition between RMR measurements may explain the
decrease in RMR repeatability and the change in mean non-breeding values over
time, a condition that was not encountered by breeding females. Alternatively,
but not exclusively, sex-specific effects of ageing could play a role since
mass-specific metabolic rate is known to decline in older individuals
(Rolfe and Brown, 1997
).
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Acknowledgments |
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References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Battley, P. F., Dietz, M. W., Piersma, T., Dekinga, A., Tang, S. and Hulsman, K. (2001). Is long distance bird flight equivalent to a high-energy fast? Body composition changes in migrated and fasted great knots. Physiol. Biochem. Zool. 74,435 -449.[CrossRef][Medline]
Battley, P. F., Piersma, T., Dietz, M. W., Tang, S., Dekinga, A. and Hulsman, K. (2000). Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc. R. Soc. Lond. B 267,191 -195.[CrossRef][Medline]
Bech, C., Langseth, I. and Gabrielsen, G. W. (1999). Repeatability of basal metabolism in breeding female kittiwake Rissa tridactyla. Proc. R. Soc. Lond. B 266,2161 -2167.[CrossRef]
Bennett, A. F. (1987). Interindividual variability: an underutilised resource. In New Directions in Ecological Physiology (ed. M. E. Feder, A. F. Bennett, W. W. Burggren and R. B. Huey), pp. 147-188. Cambridge, UK: Cambridge University Press.
Chappell, M. A., Bachman, G. C. and Odell, J. P. (1995). Repeatability of maximal aerobic performance in Belding's ground squirrels, Spermophilus beldingi. Funct. Ecol. 9, 498-504.
Chappell, M. A., Bech, C. and Buttemer, W. A.
(1999). The relationship of central and peripheral organ masses
to aerobic performance variation in house sparrows. J. Exp.
Biol. 202,2269
-2279.
Commission for thermal physiology of the International Union of Physiological Sciences (2001). Glossary of terms for thermal physiology. J. Therm. Biol. 28, 75-106.
Dohm, M. R. (2002). Repeatability estimates do not always set an upper limit to heritability. Funct. Ecol. 165,273 -280.[CrossRef]
Drobney, R. D. (1984). Effect of diet on visceral morphology of breeding wood ducks. Auk 101, 93-98.
Falconer, D. S. and Mackay, T. F. C. (1996). Introduction to quantitative genetics. Harlow: Prentice Hall.
Geluso, K. and Hayes, J. P. (1999). Effects of dietary quality on basal metabolic rate and internal morphology of European starlings (Sturnus vulgaris). Physiol. Biochem. Zool. 72,189 -197.[CrossRef][Medline]
Hammond, K., Szewczak, J. and Krol, E. (2001).
Effects of altitude and temperature on organ phenotypic plasticity along an
altitudinal gradient. J. Exp. Biol.
204,1991
-2000.
Hayes, J. P., Speakman, J. R. and Racey, P. A. (1992). Sampling bias in respirometry. Physiol. Zool. 65,604 -619.
Heaney, V. and Monaghan, P. (1995). A within-clutch trade-off between egg production and rearing in birds.Proc. R. Soc. Lond. B 261,361 -365.
Heitmeyer, M. E. (1988). Changes in the visceral morphology of wintering female mallards (Anas platyrhynchose). Can. J. Zool. 66,2015 -2018.
Hilton, G. M., Lilliendahl, K., Solmundsson, J., Houston, D. C. and Furness, R. W. (2000). Geographical variation in the size of body organs in seabirds. Funct. Ecol. 14,369 -379.[CrossRef]
Horak, P., Saks, L., Ots, I. and Kollist, H. (2002). Repeatability of conditions indices in captive greenfinches (Carduelis chloris). Can. J. Zool. 80,636 -643.[CrossRef]
Lessells, C. M. and Boag, P. (1987). Unrepeatable repeatabilities: a common mistake. Auk 104,116 -121.
Labocha, M. K., Sadowska, E. T., Baliga, K., Semer, A. K. and Koteja, P. (2004). Individual variation and repeatability in the bank vole, Clethrionomys glareolus. Proc. R. Soc. Lond. B 271,367 -372.[CrossRef][Medline]
Meijer, T., Rozman, J., Schulte, M. and Stach-Dreesmann, C. (1996). New findings in body mass regulation in zebra finches (Taeniopygia guttata) in response to photoperiod and temperature. J. Zool. Lond. 240,717 -734.
Monaghan, P., Bolton, M. and Houston, D. C. (1995). Egg production constraints and the evolution of avian clutch size. Proc. R. Soc. Lond. B 259,189 -191.
Monaghan, P., Nager, R. G. and Houston, D. C. (1998). The price of eggs: increased investment in egg production reduces the offspring rearing capacity of parents. Proc. R. Soc. Lond. B 265,1731 -1735.[CrossRef]
Nager, R. G., Monaghan, P. and Houston, D. C. (2000). Within-clutch trade-offs between the number and quality of eggs: experimental manipulations in gulls. Ecology 81,1339 -1350.
Nager, R. G., Monaghan, P. and Houston, D. C. (2001). The cost of egg production: increased egg production reduces future fitness in gulls. J. Avian Biol. 32,159 -166.[CrossRef]
Nilsson, J-A. and Raberg, L. (2001). The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia 128,187 -192.[CrossRef]
Piersma, T. (2002). Energetic bottlenecks and other design constraints in avian annual cycles. Integ. Comp. Biol. 42,51 -67.
Ramenofsky, M. (1984). Agonistic behaviour and endogenous plasma hormones in male Japanese quail. Anim. Behav. 32,698 -708.
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43,223 -225.
Rogers, C. M., Ramenofsky, M., Ketterson, E. D., Nolan, V. Jr and Wingfield. J. C. (1993). Plasma corticosterone, adrenal mass, winter weather, and season in nonbreeding populations of dark-eyed juncos (Junco hyemalis). Auk 110,279 -285.
Rolfe, D. F. S. and Brown, G. C. (1997).
Cellular energy utilization and molecular origin of standard metabolic rate in
mammals. Physiol. Rev.
77,731
-758.
Scott, I. and Evans, P. R. (1992). The metabolic output of avian (Sturnus vulgaris, Calidris alpina) adipose tissue liver and skeletal muscle: implications for BMR/body mass relationship. Comp. Biochem. Physiol. 103,329 -332.[CrossRef]
Silverin, B. (1981). Reproductive effort, as expressed in body and organ weights, in the pied flycatcher. Ornis Scand. 12,133 -139.
Vézina, F. and Williams, T. D. (2002). Metabolic costs of egg production in the European starling (Sturnus vulgaris). Physiol. Biochem. Zool. 75,377 -385.[CrossRef][Medline]
Vézina, F. and Williams T. D. (2003). Plasticity in body composition in breeding birds: what drives the metabolic costs of egg production? Physiol. Biochem. Zool. 76,716 -730.[CrossRef][Medline]
Vézina, F., Salvante, K. G. and Williams, T. D.
(2003). The metabolic cost of avian egg formation: possible
impact of yolk precursor production? J. Exp. Biol.
206,4443
-4451.
Visser, M. E. and Lessells, C. M. (2001). The costs of egg production and incubation in great tits (Parus major). Proc. R. Soc. Lond. B 268,1271 -1277.[CrossRef][Medline]
Wikelski, M., Hau, M. and Wingfield, J. C. (1999a). Social instability increases plasma testosterone in a year-round territorial neotropical bird. Proc. R. Soc. Lond. B 266,551 -556.[CrossRef]
Wikelski, M., Lynn, S., Breuner, S., Wingfield, J. C. and Kenagy, G. J. (1999b). Energy metabolism, testosterone and corticosterone in white-crowned sparrows. J. Comp. Physiol. A 185,463 -470.
Williams, T. D. (1998). Avian reproduction, overview. In Encyclopedia of Reproduction Vol.I (ed. E. Knobil and J. D. Neil), pp.325 -336. New York: Academic Press.
Williams, T. D. and Ames, C. E. (2004).
Top-down regression of the avian oviduct during late oviposition in a small
passerine bird. J. Exp. Biol.
207,263
-268.
Williams, T. D. and Ternan, S. P. (1999). Food intake, locomotor activity, and egg laying in zebra finches: contributions to reproductive energy demand? Physiol. Zool. 72, 19-27.[CrossRef]
Zann, R. A. (1996). The Zebra Finch: A Synthesis of Field and Laboratory Studies. Oxford: Oxford University Press.
Zar, J. H. (1996). Biostatistical Analysis. London: Prentice Hall.