Ecology, 87(10), 2006, pp. 2447–2458
! 2006 by the Ecological Society of America
INDIVIDUALLY VARIABLE ENERGY MANAGEMENT STRATEGIES
IN RELATION TO ENERGETIC COSTS OF EGG PRODUCTION
FRANÇOIS VÉZINA,1,3 JOHN R. SPEAKMAN,2
2
AND
TONY D. WILLIAMS1
1
Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, V5A 1S6, Canada
Aberdeen Center for Energy Regulation and Obesity (ACERO), School of Biological Sciences, University of Aberdeen,
Aberdeen, Scotland, AB24 2TZ, UK
Abstract. Marked interindividual variation in metabolic rate suggests considerable
complexity in energy management strategies, but attempts to further our understanding of
the relationship between resting metabolic rate (RMR), daily energy expenditure (DEE), and
reproductive effort have been hampered by the complexity of studying this system in the field.
Here, we describe energy management strategies in a captive-breeding system, using Zebra
Finches (Taeniopygia guttata), to demonstrate the high level of complexity and interindividual
variability in energy expenditure, food intake, locomotor activity, and reproductive effort. In
particular, we investigated whether the increase in RMR associated with egg production is
additive, resulting in higher DEE and a need for elevated food intake, or whether this cost is
compensated by reduced expenditure in nonreproductive components of the energy budget.
We found high levels of intra-individual variation in energy expenditure associated with egg
production in female Zebra Finches, e.g., comparing nonbreeding stage with the one-egg
stage, change in RMR varied from 4.0% and 41.3%, and change in DEE varied from !33.3%
to þ46.4%. This variation was systematically related to aspects of locomotor activity and
reproductive effort. Females with the largest increase in RMR during egg production
decreased locomotor activity the most but still had increased DEE at the one-egg stage, and
females with high DEE at the one-egg stage produced larger clutches. Our study suggests that
females minimize increases in DEE during egg production through behavioral energy
reallocation (reduced locomotor activity) but that individuals differ in their use of this
strategy, which, in turn, is related to the absolute level of reproductive investment. This
suggests a very complex, individually variable system of energy management to meet the
demands of egg production.
Key words: basal metabolic rate (BMR); daily energy expenditure (DEE); egg production costs;
energy reallocation; reproduction; resting metabolic rate (RMR); Taeniopygia guttata; Zebra Finch.
INTRODUCTION
Energy is widely held to be a universal currency and
biologists are increasingly considering how energy
management affects the fitness of the individual
(Ricklefs 1996). A common assumption is that basal
metabolic rate (BMR) is directly related to an individual’s capacity for sustained levels of high daily energy
expenditure (DEE), i.e., that there is a generalizable
empirical (and functional) relationship between BMR
and DEE (e.g., Daan et al. 1990, Ricklefs 1996).
Nevertheless, there is marked, but largely unexplained,
interindividual variation in both BMR (or resting
metabolic rate, RMR) and DEE in free-living animals
(for reviews, see Bryant and Tatner 1991, Williams and
Vézina 2001, Speakman et al. 2004). Although these
Manuscript received 12 December 2005; revised 29 March
2006; accepted 3 April 2006. Corresponding Editor: S. J.
Simpson.
3 Present address: Department of Marine Ecology and
Evolution, Royal Netherlands Institute for Sea Research
(NIOZ), P.O. Box 59, 1790 AB Den Burg, Texel, The
Netherlands. E-mail: [email protected]
data hint at considerable complexity in energy management strategies, attempts to further our understanding
of the relationship between BMR and DEE, especially in
the context of reproductive effort, have been hampered
by the complexity of studying this system in the field,
e.g., in obtaining comprehensive data on energy intake
and locomotor activity in addition to BMR/DEE in the
same individuals over multiple breeding stages (Williams
and Vézina 2001).
Here, we focus on energy management strategies in a
captive-breeding system, using Zebra Finches (Taeniopygia guttata; see Plate 1), to demonstrate the high level
of complexity and interindividual variability in the
relationship between RMR, DEE, and reproductive
effort. We specifically consider energy management
underlying costs of egg production since numerous
recent studies have shown that females producing extra
eggs do incur fitness costs that are apparent either within
the breeding attempt (Heaney and Monaghan 1995,
Monaghan et al. 1995, 1998, Nager et al. 2000) or in
terms of long-term female survival (Visser and Lessells
2001). The mechanistic link between the cost of egg
production and reproductive success or future survival is
2447
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FRANÇOIS VÉZINA ET AL.
not clear, but increased energy investment required for
the physiological process of egg formation (Williams
1998) may play a significant role. It is therefore
important to understand variation in energy management (measurable through metabolic and behavioral
parameters) in relation to energy intake (food consumption), and both nonreproductive and reproductive
activities; something that would be very difficult in field
studies. Recent empirical studies in both the field and
laboratory have shown that the metabolic cost of egg
production results in a 16–27% increase in resting
metabolic rate (Chappell et al. 1999, Nilsson and Raberg
2001, Vézina and Williams 2002, 2005). Furthermore,
the increased RMR of birds producing eggs is repeatable
between breeding attempts (Vézina and Williams 2005).
Such studies therefore raise an important question in
relation to energy management: how does a female cope
with a 16–27% increase in RMR in terms of her overall
energy budget (as measured by DEE)? There are two
likely possibilities: (1) the cost of egg production could
be additive to other expenditures, meaning that daily
energy expenditure (DEE) would also increase in
response to egg production, and require increased food
intake or utilization of stored energy, or (2) the
additional energy demand could be compensated for
by reducing or trading off some other component of the
energy budget.
One proposed mechanism for energy reallocation as a
management strategy involves a reduction in locomotor
activity in reproducing females. This has been demonstrated in free-living gravid lizards (Cooper et al. 1990),
birds (Ettinger and King 1980), and pregnant and
lactating mammals (Poppitt et al. 1993, Speakman et
al. 2001). Captive-breeding Zebra Finches similarly
reduce their level of locomotor activity during egg
production (Houston et al. 1995, Williams and Ternan
1999), suggesting they might use a behavioral strategy
for energy reallocation to direct more ingested energy
toward egg production. However, no studies to date
have combined measures of locomotor activity and food
intake with any direct measurements of energy expenditure. If energy reallocation occurs during egg production
in Zebra Finches, then assuming that compensation is
complete, and all individual utilize this strategy equally,
overall daily energy expenditure for a given female
should be relatively constant between nonbreeding and
egg-producing stages, which would be consistent with
the general lack of difference in average DEE among
breeding stages reported for free-living birds (Williams
and Vézina 2001).
To investigate individual variability in energy management during egg production and the potential for
energy reallocation via behavioral mechanisms, we
measured RMR, DEE, food intake, locomotor activity,
and reproductive effort on the same individual female
Zebra Finches. Our first aim was to compare DEE
estimates of females measured at nonbreeding and
breeding (laying and chick-rearing) stages in controlled
Ecology, Vol. 87, No. 10
captive conditions, thus reducing any confounding
effects of ambient ecological conditions. Second, we
evaluated how egg-producing females manage their
overall energy budgets by comparing their DEE
estimates with previous RMR measurements made at
the same breeding stages for the same individuals. We
examined interindividual variation as this represents the
basis for natural selection and may allow us to better
understand flexibility in how individual birds adjust to
the energy cost of egg production (see Williams and
Vézina 2001). We predicted that if female Zebra Finches
used a behavioral strategy for energy reallocation,
locomotor activity would decrease but food intake and
DEE would not change from nonbreeding to eggproducing stages. Alternatively, if egg production costs
were additive, then DEE should increase when the birds
are forming eggs, due to the increase in RMR.
MATERIAL
AND
METHODS
Animal care
Zebra Finches were maintained in controlled environmental conditions (temperature 19–238C; humidity 35–
55%; constant light schedule, 14L : 10D with lights on at
0800 hours) and all birds were provided with a mixedseed diet (50:50 Panicum and white millet, approximately 12.0% protein, 4.7% lipid; Jamieson’s Pet Food,
Vancouver, British Columbia, Canada), water, grit, and
cuttlefish bone (calcium) ad libitum. The birds also
received a multivitamin supplement in the drinking
water once per week. Between experiments, all birds
were housed in large reserve cages (122 3 46 3 41 cm) in
single-sex groups, and during experiments all pairs
(nonbreeding female/female, and breeding male/female;
see Experimental groups and general protocol) were
housed in separate breeding cages (61 3 46 3 41 cm)
provided with an external nest box (15 3 14.5 3 20 cm).
For experiments with single-sex pairs, access to the box
was blocked by closing the entrance with a piece of
cardboard. During breeding experiments, nest boxes
were checked daily between 1000 and 1200 hours, and all
new eggs were weighed (60.001 g) and numbered. A
clutch was considered complete after two consecutive
days with no new eggs. All experiments and animal
husbandry were carried out under a Simon Fraser
University Animal Care Committee permit (692B-94),
following the guidelines of the Canadian Committee on
Animal Care.
Experimental groups and general protocol
All birds were adult individuals (.3 months of age)
with previous successful breeding experience. Females
were first paired as nonbreeding female/female pairs
(NB) for seven days, food consumption and locomotor
activity were measured on days 5, 6, and 7 of the
nonbreeding period, and DEE was measured from day 6
to day 7 using the doubly labeled water (DLW)
technique. On day 8, all female/female pairs were
separated and each female was paired with a male to
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ENERGY MANAGEMENT IN EGG-PRODUCING BIRDS
form a male/female breeding pair (see Plate 1).
Locomotor activity was monitored in breeding pairs
starting the following day through until clutch completion. Food intake was recorded on day 1 and 2 after
pairing (pre-laying: PL) and again during egg laying
(LY) beginning the day prior to laying of the first egg
and during the four following days. All females had their
DEE measured at the one-egg stage (i.e., on the day they
laid their first egg; LY-1) with DEE estimates encompassing a complete ovulation and laying cycle (second
egg). The birds were then left to incubate their eggs and
raise their chicks (see Plate 1). Ten of the females paired
with males did not produce eggs. We later compared the
activity data from these unsuccessful breeding pairs with
activity patterns of successful breeders (see Williams and
Ternan 1999).
Food intake and locomotor activity were measured
again in successful breeders between days 16 and 18 of
the chick-rearing period (CK; ;2–4 days before fledging) and breeding female DEE was measured from day
17–18 during the chick-rearing stage. If chicks fledged
before day 16 (n ¼ 2 pairs), locomotor activity data were
discarded because of the bias introduced by chicks
hopping on the perches. We used a repeated-measures
approach to compare DEE values of 24 females
measured as nonbreeders, at the one-egg stage and
during chick-rearing (in females that successfully raised
chicks, sample sizes are: NB ¼ 24; LY-1 ¼ 24; CK ¼ 11).
Preliminary experiments showed that we could not
measure RMR and DEE in the same breeding attempt
without causing breeding failure. Therefore, to compare
changes in RMR and DEE we used data on RMR
measured in the same individual females and for the
same breeding stages, but in an earlier breeding experiment using exactly the same protocol as described above
(Vézina and Williams 2005). Since RMR is repeatable
over relatively long periods (months to years) in both
nonbreeding and egg-laying birds (Rønning et al. 2005,
Vézina and Williams 2005) we consider the individual
change in RMR, measured in the first breeding attempt,
a good reflection of the metabolic investment in egg
production specific to a given female. Although we
measured all birds as nonbreeders before their breeding
stages, we do not believe that any time-dependent effects
confounded this study because all birds had already bred
previously. Furthermore, the time intervals between
pairing and laying, as well as egg and clutch mass, are
repeatable between breeding attempts in Zebra Finches
(T. D. Williams, unpublished data) as is reproductive
effort measured as both RMR and DEE at LY-1
(Vézina and Williams 2005; F. Vézina, unpublished data).
Locomotor activity
We monitored locomotor activity at all breeding
stages using a micro-switch system connected to a cage
perch as described and validated by Williams and
Ternan (1999). This system does not discriminate
potential differences between sexes in locomotor activ-
2449
PLATE 1. (Top) A female (front) and a male (back) Zebra
Finch forming an experimental breeding pair. (Bottom) A
brood of fledged Zebra Finch chicks. Photo credit: Andrea Vin.
ity, but validation of the technique using direct
observation via video recording clearly showed that
activity does not differ with sex and that the two birds of
a pair follow the same activity pattern (Williams and
Ternan 1999). Williams and Ternan (1999) also showed
that time spent in the nest box is not dependent on sexes.
Because we could only monitor locomotor activity in 14
cages at a time, the complete data set was gathered over
five identical experimental runs.
Food intake
To obtain a gross estimate of energy intake we
measured food consumption by giving birds 25 g/d of
seeds in an open 946-mL plastic food container placed
on the cage floor. This avoided any spillage and allowed
us to measure seed mass intake by weighing the
remaining seeds and empty husks left in the container
after each 24-h period. Williams and Ternan (1999)
showed that, on average, females eat slightly more food
(4.5%) than males, but this difference was significant
only on the two days before the first egg was laid.
Measuring food intake per pair is therefore a good
indicator of female food intake in our experimental
context, and we report the pair values as representative
of female energy input. During the experiment, the birds
received 6 g of egg food supplement (20.3% protein,
6.6% lipid) daily, which was always completely consumed, by both males and females, by the following day.
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FRANÇOIS VÉZINA ET AL.
Daily energy expenditure (DEE)
We measured DEE in females that successfully laid
eggs, using the doubly labeled water technique (Lifson
and McClintock 1966, Speakman 1997). The injection
solution was made of 4.2182 g H218O (96.1 atom%),
3.9372 g H218O (95 atom%), and 3.8825 g 2H2O (99.8
atom%). Using a high-precision gas tight syringe
(Hamilton, Reno, Nevada, USA), all individuals received 76 lL of labeled water intramuscularly in the
right pectoral muscle. To determine the exact amount of
water injected, the syringe was weighed (60.0001 g)
before and after each injection. The birds were then
returned to their cages for an hour to allow for isotope
equilibration with the body water pool (Williams and
Nagy 1984). After the equilibration period, the birds
were weighed (60.1 g) and blood was sampled by
puncturing the brachial vein of one wing. About 100 lL
of blood was collected per individual into microhematocrit tubes that were immediately flame sealed
after releasing the birds back in their cages. Twenty-four
hours later, a second blood sample was taken from the
other wing following the same procedure. The birds were
then reweighed and released into their cages. Background isotope enrichments can vary significantly over
time, and this may result in significant errors in CO2
production measurements (reviewed in Williams and
Vézina 2001). Because background levels are mainly
affected by the enrichment of the input sources: water,
food, and atmospheric oxygen (Speakman and Racey
1987, Tatner 1988, 1990, Thomas et al. 1994), it is
unlikely that our birds would exhibit marked background enrichment variation in controlled conditions, as
the only variable input source was drinking tap water.
However, we were concerned about changes in body
composition between breeding stages and a possible time
effect (Williams and Vézina 2001). We therefore took
blood samples for background measurements at all
breeding stages and all experimental runs (total background sample size NB ¼ 10, LY-1 ¼ 5, CK ¼ 3). All
samples were stored at 48C until distillation and
analysis.
Samples of blood were vacuum distilled into glass
Pasteur pipettes (Nagy 1983) and the water obtained
was used for isotope-ratio mass spectrometric analysis
of 2H and 18O. The 2H analysis was performed on
hydrogen gas, produced by on-line chromium reduction
of water (Morrison et al. 2001). For analysis of 18O
enrichment in blood samples, water distilled from blood
was equilibrated with CO2 gas using the small-sample
equilibration technique (Speakman et al. 1990). For
analysis of 18O : 16O ratios, equilibrated water samples
were admitted to an ISOCHROM lGAS system
(Micromass UK, Waters Corporation, Milford, Massachusetts, USA), which uses a gas chromatograph
column to separate nitrogen and CO2 in a stream of
helium gas before analysis by isotope ratio mass
spectrometry (IRMS). Total body water estimates were
based on the plateau technique (Speakman 1997) and
Ecology, Vol. 87, No. 10
DEE was calculated from CO2 production using Speakman (1997) equation 7.17, taking evaporative water loss
into account and assuming a RQ value of 0.8. All sample
analyses and calculations were performed blind of the
experimental manipulations.
Resting metabolic rate (RMR)
RMR (metabolic rate of birds in post-absorptive
state, measured during the inactive phase of the
circadian cycle at a temperature within the thermoneutral zone) was measured as described in Vézina and
Williams (2005) using a flow-through respirometry
system (Sable Systems International, Las Vegas, Nevada, USA). Since our DEE data are presented in kJ/d, to
obtain RMR values in comparable units we converted
VO2 (mL O2/h) to kJ/d. Average nighttime respiratory
quotient (RQ) was 0.82 and showed a large degree of
variability between individuals (maximal range 0.69 to
0.99), but no differences between breeding stages
(repeated-measures ANOVA, F2,28 ¼ 0.4, P ¼ 0.7; NB
¼ 0.81 6 0.01, LY-1 ¼ 0.83 6 0.01, CK ¼ 0.84 6 0.03
[mean 6 SE]). Daytime RQ was 0.85 (range 0.73 to 1.01,
n ¼ 14; F. Vézina, unpublished data). We cannot consider
that individual RQ remained constant within a 24-h
period because RQ values are not stable through time
(Powers 1991, Walsberg and Wolf 1995, Walsberg and
Hoffman 2005). Therefore, we used an energy equivalent
of 20.38 kJ/L O2, reflecting an averaged RQ value of
0.835 (Weir 1949). Gessaman and Nagy (1988) showed
that using a RQ of 0.8 to convert VO2 values into
kilojoules results in less than 63% error regardless of
the actual protein, fat, or carbohydrate mixture being
catabolized.
Statistical analysis
All data were tested to ensure normality (ShapiroWilk test; Zar 1996). Metabolic rate varies allometrically
with body mass (Schmidt-Nielsen 1984), but using log10transformed values did not change any of the statistical
results compared to untransformed data. We therefore
present results of analysis on untransformed values
(body mass in grams and RMR and DEE in kJ/d). To
compare within-individual changes from the nonbreeding to one-egg and chick-rearing stages, we used
repeated-measures ANOVA and ANCOVA with body
mass as a covariate when appropriate (for RMR and
DEE). This was performed using mixed general linear
models that included individual bird as random factor,
breeding stage as the main fixed effect, and body mass as
covariate if necessary. We removed the interaction term
body mass 3 breeding stage from the ANCOVA when
not significant (i.e., indicating no difference in slopes).
Post hoc comparisons between stages were performed
using Tukey hsd and multiple contrasts (when using a
covariate) corrected with the Bonferroni procedure
(Rice 1989). Within breeding stage, relationships between continuous variables were investigated using
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ENERGY MANAGEMENT IN EGG-PRODUCING BIRDS
2451
Pearson’s correlation analyses. Data are reported as
means 6 SE.
RESULTS
Locomotor activity
We first investigated locomotor activity to confirm the
potential for behaviorally based energy reallocation
(sensu Williams and Ternan 1999). Locomotor activity
(number of perch hops per day) was independent of
male or female body mass at all breeding stages (P $ 0.2
in all cases) but was highly dependent on breeding stage
(F3,48 ¼ 10.5, P , 0.0001; Fig. 1A). Mean activity was
higher at the nonbreeding stage compared to all other
stages, and was 42.1%, 61.1%, and 52.9% lower during
the pre-laying, laying, and chick-rearing stages, respectively. Mean locomotor activity did not differ significantly among these three stages (Fig. 1A) and, during
the laying stage, it was independent of mean egg mass,
clutch mass, and clutch size (P . 0.5 in all cases).
Absolute locomotor activity levels varied considerably
between breeding pairs, so we standardized these data
by calculating the percentage of deviation in daily
activity from mean activity for the whole laying period
for each individual pair (following Williams and Ternan
1999). Locomotor activity in breeding pairs decreased
rapidly between eight and four days before the onset of
laying (Fig. 2A) but thereafter the activity level
remained low and constant until clutch completion
(overall F15, 203 ¼ 6.0, P , 0.0001; independent contrast
day !8 to day !4 F1, 203 ¼ 15.2, P , 0.0001; day !4 to
day 8 F1, 203 ¼1.8, P ¼ 0.2). This pattern of change in
locomotor activity was not apparent in the unsuccessful
male/female pairs that did not produce eggs (F15, 114 ¼
1.2, P ¼ 0.3; Fig. 2B).
Food intake
Food intake was independent of male, female, or
combined (pair) body mass at all breeding stages (P $
0.1 in all cases) but was related to breeding stage (F3,52 ¼
52.3, P , 0.0001; Fig. 1B). However, mean food intake
did not differ among nonbreeding, pre-laying, and
laying stages (average intake; NB ¼ 5.0 6 0.3 g/d, PL
¼ 4.8 6 0.3 g/d, LY ¼ 5.4 6 0.3 g/d) and only increased
markedly during chick-rearing (10.6 6 0.4 g/d) due to
food being consumed by the chicks. None of our
measures of female reproductive effort (clutch size,
clutch mass, mean egg mass) were related to either mean
(four days) food intake during laying (P $ 0.4 in all
cases) or to food intake the day prior to laying of the
first egg (P $ 0.2 in all cases).
DEE in relation to locomotor activity, food intake,
and reproductive effort
DEE was independent of female body mass for all
breeding stage (P $ 0.2 in all cases). At the nonbreeding
stage, DEE was also independent of locomotor activity
recorded between the two blood samples (P ¼ 0.5), and
mean food intake over the three days (5, 6, and 7) prior
FIG. 1. (A) Locomotor activity and (B) food intake in
Zebra Finch pairs at all breeding stages (NB, nonbreeding; PL,
pre-laying; LY, laying; CK, chick-rearing; mean 6 SE). Different lowercase letters indicate significant differences. Note that
food intake during CK is higher because of the amount of food
given to the brood.
to sampling (P ¼ 0.1). However, DEE was positively
correlated with food intake at day 6 (the day of DEE
measurement; r ¼ 0.51, n ¼ 24, F1,22 ¼ 7.7, P , 0.05; Fig.
3). In contrast, DEE at the one-egg stage was positively
correlated with locomotor activity recorded between the
blood samples (r ¼ 0.48, n ¼ 23, F1,21 ¼ 6.1, P , 0.05;
Fig. 4A), i.e., during egg production more active birds
spent more energy on a daily basis. Furthermore,
average food intake per pair, measured either over four
days or on the day of DEE measurement, was
significantly correlated with DEE at the one-egg stage
(mean food intake, r ¼ 0.51, n ¼ 24, F1,22 ¼ 7.7, P , 0.05;
day of LY-1, r ¼ 0.52, n ¼ 24, F1,22 ¼ 8.3, P , 0.01; Fig.
4B). Finally, during chick-rearing, DEE was independent of locomotor activity and food intake (P . 0.5 in
both cases).
On average, females laid 6.0 6 0.4 eggs (range: 4–10
eggs) and mean egg mass was 1.040 6 0.017 g (range:
0.841–1.201 g). DEE at the one-egg stage was positively
correlated with both clutch size (r ¼ 0.49, n ¼ 24, F1,22 ¼
6.9, P , 0.05) and total clutch mass (r ¼ 0.46, n ¼ 24,
F1,22 ¼ 6.1, P , 0.05; Fig. 5A and B); i.e., during egglaying overall energy expenditure was positively related
to reproductive effort. In contrast, during chick-rearing
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FRANÇOIS VÉZINA ET AL.
Ecology, Vol. 87, No. 10
FIG. 2. Standardized locomotor activity in relation to days of the laying cycle in (A) breeding and (B) nonbreeding male/female
Zebra Finch pairs. Values are the mean 6 SE of the percentage deviation from the mean number of hops per day for each individual
pair. The arrow indicates onset of rapid yolk development (RYD). Day 1 in panel (A) is the day the first egg is laid.
DEE was independent of brood size and total brood
mass at 21 days (P $ 0.3 in both cases).
Individual variation in RMR and DEE and relationship
between these traits
For the subset of RMR birds for which we measured
DEE, mean resting metabolic rate varied with breeding
stage, as shown by Vézina and Williams (2005; repeatedmeasures ANCOVA with body mass as a covariate; F2,27
FIG. 3. Relationship between daily energy expenditure
(DEE) in nonbreeding Zebra Finch females and food intake
of the pair on the day of DEE measurement.
¼ 17.0, P , 0.0001, no significant interaction; leastsquare mean NB RMR ¼ 19.8 6 0.4 kJ/d, LY-1 RMR ¼
23.3 6 0.5 kJ/d, CK RMR ¼ 23.1 6 0.9 kJ/d). RMR
increased by 3.5 kJ/d, or 17.6% from the nonbreeding to
the one-egg stage and remained high during chickrearing. However, there was marked interindividual
variation in the change in RMR (DRMR) from the
nonbreeding to the one-egg stage ranging from 4.0% to
41.3%. This individual variability in DRMR was
independent of both nonbreeding and one-egg stage
body mass and was independent of the change in mass
between the two stages (P $ 0.3 in all cases).
Considering the change in RMR in relation to
locomotor activity, only three out of 23 pairs showed
an increase in activity comparing nonbreeding stage
with one-egg stage. One of these pairs represented a
clear outlier with a 97% increase in activity (5.9 times the
standard deviation of the mean difference in activity).
Excluding this pair, there was a significant negative
relationship between the relative change in locomotor
activity (percent difference compared to nonbreeding
level) and RMR at the one-egg stage (r ¼ !0.57, n ¼ 22,
P , 0.01; Fig. 6). Thus, individuals that had the highest
one-egg stage RMR were also the ones showing the
largest reduction in locomotor activity from nonbreeding to one-egg stage, suggesting that the level of
behavioral energy compensation (reduced locomotor
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ENERGY MANAGEMENT IN EGG-PRODUCING BIRDS
2453
FIG. 4. Relationship between daily energy expenditure (DEE) in one-egg stage Zebra Finch females and (A) locomotor activity
of the pair for the 24 hours of DEE measurements and (B) food intake of the pair on the day of laying the first egg (LY-1).
activity) for the cost of producing eggs is a function of
the individual’s initial metabolic investment.
In contrast to the within-stage analysis, there was a
significant overall effect of body mass on DEE (F1,30 ¼
15.3, P , 0.001) as well as a significant breeding-stage
effect (F2,30 ¼ 6.6, P , 0.01) and interaction term, body
mass 3 breeding stage (F2,30 ¼ 6.1, P , 0.01). The mass
3 stage interaction was due to a slightly higher DEE at
the chick-rearing stage (5.6%) compared with the oneegg stage (no significant difference between nonbreeding
and one-egg stages, independent contrast P ¼ 0.9; mean
NB DEE ¼ 53.6 6 1.0 kJ/d, LY-1 DEE ¼ 51.3 6 1.3 kJ/
d, CK DEE ¼ 54.2 6 1.8 kJ/d). Excluding the chickrearing stage from the analysis resulted in no significant
breeding-stage effect (F1,21 ¼ 0.04, P ¼ 0.8). Again there
was marked individual variation in the change in DEE
(DDEE) comparing nonbreeding and one-egg stage
values, with DDEE varying between !33.3% and
þ46.4%. As a consequence of this individual variation
mean DEE did not change significantly within females
between nonbreeding and one-egg stage (controlling for
body mass). Individual variability in DDEE between
nonbreeding and one-egg stages was independent of the
relative change in locomotor activity for that period (P ¼
0.7), and was independent of body mass at both the
nonbreeding and one-egg stages (P $ 0.1). However,
DDEE was significantly related to the gain in mass
between the two stages (r ¼ 0.63, n ¼ 24, F1,22¼ 14.8, P ,
0.001), which partly reflects the mass of the reproductive
machinery at the one-egg stage (T. D. Williams and C.
E. Ames, unpublished data).
Residual RMR (correcting for body mass) and DEE
were positively correlated at the nonbreeding stage (r ¼
0.59, n ¼ 24, F1,22 ¼ 11.6, P , 0.005; Fig. 7A) but not at
the one-egg stage (P ¼ 0.7; Fig. 7B). Furthermore,
DRMR from the nonbreeding to one-egg stage was
positively correlated with DDEE for the same period (r ¼
0.42, n ¼ 24, F1,22 ¼ 4.7, P , 0.05; Fig. 8). When
corrected for the effect of the gain in body mass on the
change in DEE, the relationship remained significant
(residual DDEE vs. DRMR; r ¼ 0.41, n ¼ 24, F1,22 ¼ 4.6,
P , 0.05).
FIG. 5. Relationship between daily energy expenditure in one-egg stage Zebra Finch females and (A) final clutch size and (B)
clutch mass.
2454
FRANÇOIS VÉZINA ET AL.
FIG. 6. Relationship between the relative change in
locomotor activity from nonbreeding to one-egg stage and
female’s resting metabolic rate (RMR) at the one-egg stage.
Change is presented relative to nonbreeding locomotor activity.
The 3 indicates an outlier that was excluded from the analysis.
Ecology, Vol. 87, No. 10
FIG. 8. Relationship between change in daily energy
expenditure (DEE) and change in resting metabolic rate
(RMR) between nonbreeding and one-egg stage in female
Zebra Finches.
DISCUSSION
FIG. 7. Relationship between daily energy expenditure and
residual resting metabolic rate (RMR; correcting for body
mass) in female Zebra Finches at the (A) nonbreeding and (B)
one-egg stage.
Although we used a captive-breeding species, the
Zebra Finches, in controlled and presumably relatively
benign breeding conditions, we have demonstrated a
high level of complexity and interindividual variability
in energy management strategies, specifically in the
relationship between RMR, DEE, and reproductive
effort. We believe that these results are relevant for freeliving birds and although a comprehensive study of this
nature has so far proved elusive in field studies we hope
our data will inform future experimental fieldwork. Our
study suggests that the metabolic cost of egg production
requires individuals to make behavioral adjustments
that minimize large variations in overall energy
expenditure (DEE): female Zebra Finches reduced
energy expenditure devoted to locomotor activity
during egg production but did not change food intake.
This is in agreement with previous studies (Williams and
Ternan 1999) and supports the hypothesis of behavioral
energy reallocation. On average, RMR increased by
18% in response to egg production but this mean
increase masked a high level of individual variability
(þ4–40%). Similarly, we did not detect a significant
change in average DEE during the same period, and
this was due to even greater individual variability in the
change in DEE (!33% to þ46%). Importantly however,
this variability in RMR and DEE was not random but
was systematically related to aspects of locomotor
activity and reproductive effort. For example, birds
that had high levels of DEE at the one-egg stage
produced large clutches, and individual variation in the
change in RMR associated with egg production was
positively correlated with the change in DEE. Increased
RMR associated with egg production is consistent with
previous observations of elevated RMR during egg
production in Zebra Finches and other passerines
(Chappell et al. 1999, Nilsson and Raberg 2001, Vézina
and Williams 2002, 2005). In our study, we interpret the
October 2006
ENERGY MANAGEMENT IN EGG-PRODUCING BIRDS
individual variability in the change in RMR associated
with egg production as a measure of the metabolic
demands of investment in reproductive tissues. We base
this interpretation on the fact that positive relationships
between RMR and oviduct mass have been demonstrated in three species including Zebra Finches
(Chappell et al. 1999, Vézina and Williams 2003,
2005). The size of the oviduct has been shown to be
related to egg size in European Starlings Sturnus
vulgaris (Ricklefs 1976, Vézina and Williams 2003)
and egg quality may also be related to oviduct size.
Indeed, Christians and Williams (2001) have shown a
positive relationship between egg albumen protein
content and oviduct size in European Starlings. Thus,
generating a larger oviduct potentially allows for the
production of larger, better eggs, but this incurs a
higher metabolic cost visible in elevated RMR. Therefore the question remains: how do females adjust their
energy budget relative to their costs of physiological
reproductive investment?
The marked interindividual variation in RMR and
DEE that we have documented clearly confounds the
interpretation of average, population-level changes in
energy expenditure because mean values mask the
particular direction of changes within individuals. Thus,
although mean RMR increased from nonbreeding to
one-egg and chick-rearing stages, mean DEE remained
constant in our study. This was because, at the one-egg
stage, mean DEE was based on measurements of
individuals that had either increased or decreased their
overall energy expenditure, and this variation in change
in DEE cancelled out such that there was no statistical
difference in the mean values. We suggest that females
‘‘manage’’ their energy budget during egg production in
order to minimize potential increases in DEE by
adjusting their behavior, i.e., decreasing locomotor
activity, to compensate for the increase in RMR. In
fact, the individuals showing the largest reproductive
investment in terms of RMR at the one-egg stage were
also members of pair that decreased locomotor activity
the most (down to !86%). Individual variation in
measures of energy expenditure has been reported in
earlier studies (Moreno 1989, Williams 1987) but the
basis of this variation has not been investigated (see
Williams and Vézina 2001). Our results clearly demonstrate that more attention needs to be given to this level
of variability as it may help us to understand adjustments that individual animals have to make to balance
their energy budget.
Reduction of activity as a strategy for energy reallocation
Birds show decreased activity when facing thermoregulatory challenges (Cherel et al. 1988) or the cost of
molting into new feathers (Austin and Fredrickson
1987, Robin et al. 1989). In Zebra Finches, food
limitation also resulted in reduced locomotor activity
(Meijer et al. 1996, Dall and Witter 1998), and egg
production has now been shown in three independent
2455
studies to be associated with reduced activity (Houston
et al. 1995, Williams and Ternan 1999; this study).
Decreases in activity have also been documented in freeliving Willow Flycatchers (Empiodonax traillii) during
egg production (Ettinger and King 1980) and in
mammals such as pregnant female common shrew
(Sorex araneus; Poppitt et al. 1993) and rats (Slonaker
1924), lactating mice (Mus musculus; Speakman et al.
2001) and rats (Slonaker 1924, Wang 1924), as well as
pregnant women (Butte et al. 2004). This suggests that
reducing locomotor activity is a widespread behavioral
mechanism that helps to compensate for temporarily
increased energetic demands from a range of other
physiological processes. In contrast to marked changes
in behavior associated with reproductive investment,
Zebra Finches in our study did not change food (energy)
intake. Energy expenditure in Zebra Finches does not
appear to be limited by their food processing capabilities. Wild Australian Zebra Finches eat 28–76% more
seeds per day than their domesticated counterpart
(Zann 1996) and captive breeding pairs kept in cold
temperatures (78C) consume 72% more seeds per day
than pairs kept in normal conditions (218C; K. G.
Salvante, F. Vézina, and T. D. Williams, unpublished
data). Nevertheless, our experiment demonstrated that
even if these birds are potentially capable of sustaining
higher levels of DEE by increasing food intake during
egg production, egg-laying females appeared to avoid
this strategy.
Additive vs. compensated costs of egg production
At the individual level, it appeared that energy
investment in egg production (increased RMR) generated a wide spectrum of effects on DEE, from overcompensation (decrease in DEE) to additive effects
(increase in DEE). This was shown by the positive
relationship between the change in RMR from the
nonbreeding to the one-egg stage and the change in DEE
during the same period (see Fig. 8). Individuals with
relatively high reproductive effort (large increase in
RMR) appeared to not be able to fully compensate for
this increased energy demand. Even though they showed
the largest decrease in locomotor activity, they still had
an elevation in DEE. Thus, in these birds, there was an
additive effect of the cost of egg production on DEE. In
contrast, individuals with low reproductive effort (small
increase in RMR) were much better at avoiding an
increase in DEE and, in some cases, even overcompensated for the elevated RMR (reduction in DEE during
egg production; see Fig. 8). Therefore, behavioral
adjustments allowed all birds to decrease the total
energy expended, but the level of energy reallocation
appeared to depend on the actual level of reproductive
investment. Ultimately, the females with the highest
DEE at the one-egg stage produced larger clutches,
which suggests that they did benefit from their higher
metabolic investment.
2456
FRANÇOIS VÉZINA ET AL.
Relationship between RMR and DEE
We found a significant positive correlation between
RMR and DEE at the nonbreeding stage, but this
relationship was lost when the birds were actively
producing eggs. A general interpretation for such a
correlation is that increased sustained energy expenditure is supported by enlarged organs which results in
higher maintenance costs and thus elevated RMR
(Peterson et al. 1990, Hammond and Diamond 1997,
Piersma and Lindström 1997, Piersma 2002; but see
Ricklefs et al. 1996, Speakman 2000, Speakman et al.
2003, 2004). Our nonbreeding birds showed the highest
levels of locomotor activity. However, DEE was not
related to activity at this stage, which does not provide
strong support for this interpretation. If the relationship
between RMR and DEE in nonbreeding individuals was
due to a common effect of the underlying physiological
machinery, then its influence on energy expenditure
seems unrelated to locomotor activity as measured by
hopping counts. Speakman et al. (2003) suggested that
RMR and DEE follow independent trajectories that
may or may not correlate in response to direct ecological
conditions that the organism faces and this may be the
case in our egg-laying birds. The lack of relationship
between RMR and DEE in females producing eggs may
have been because these two variables were responding
differently to the demands of egg production. Mean
RMR increased in response to egg production, but mean
DEE remained relatively unchanged because females
individually adjusted their behavior to maintain a
constant overall energy expenditure. The birds that
showed the largest increase in RMR were also the ones
compensating the most. Therefore, they minimized the
impact of an increased RMR on DEE, which resulted in
a correlation between these two variables showing a
slope not significantly different from zero. In other
words, we suggest that reallocation of energy during egg
formation uncoupled the relationship between RMR
and DEE.
DEE and egg production costs
We are aware of only two studies on birds specifically
investigating energy expenditure, using the doubly
labeled water technique, during egg production. Stevenson and Bryant (2000) demonstrated a positive correlation between DEE and egg mass in one of two years in
free-living Great Tits (Parus major), but did not report
nonbreeding or chick-rearing DEE or potential relationships between DEE and clutch size. Consistent with the
present data, Ward (1996) found no significant differences between DEE of wild Barn Swallows (Hirundo
rustica) measured during egg-formation, incubation, or
chick-rearing. Ward (1996) suggested that egg production costs are small relative to routine energy requirements because DEE was not significantly elevated or
correlated with egg energy content. We disagree somewhat with Ward’s (1996) interpretation. The energy
expended in egg formation results from several physio-
Ecology, Vol. 87, No. 10
logical processes that have their own associated energetic costs (reproductive organ development, function
and maintenance, hepatic yolk precursor production
and uptake by the ovary, albumen and shell deposition
in the oviduct). The energy spent in these physiological
activities is not directly comparable to the chemical
energy content of the eggs (see Vézina and Williams
2002). In fact, our data suggest that egg-producing
females compensate for the extra demand associated
with egg formation by decreasing the energy expended in
locomotion in relation to their change in RMR.
Furthermore, this energy compensation strategy appears
to be closely related to the period of follicular growth as
the reduction in activity occurred just before the onset of
rapid yolk development (rapid yolk development begins
four days prior to laying of the first egg in Zebra Finches
[Haywood 1993:Fig. 2a]). Although a 16–27% increase
in RMR (Nilsson and Raberg 2001, Vézina and
Williams 2002, 2005) may represent a relatively small
fraction of DEE, the fact that average DEE does not
increase significantly during egg production may not
mean that the amount of energy invested in egg
production is trivial, but rather that this cost is
demanding enough for the animal to adopt behavioral
strategies to minimize the increase in overall energy
expenditure. That we find no significant differences in
DEE between egg-producing and other life-history
stages, some of which are believed to be energetically
costly (i.e., chick-rearing [Drent and Daan 1980]),
suggests that other expensive activities are also subject
to compensatory adjustments. In agreement with this
idea, Williams and Vézina (2001) compiled absolute
values of DEE (kJ/d) in studies where measurements
were obtained at more than one physiological stage
within species; they found a general tendency for a
constant level of DEE during all phases of reproduction
and perhaps even throughout the year.
In conclusion, our study suggests that females
minimize increases in DEE during egg production
through behavioral energy reallocation (reduced locomotor activity) but that individuals differ in their use of
this strategy which, in turn, is related to the absolute
level of reproductive investment. This suggests a very
complex, individually variable system of energy management to meet the demands of egg production. We
suggest that this complexity might help explain why so
few studies of free-living birds have found support for
positive relationships between energy expenditure and
putative correlated ecological variables (e.g., temperature, food availability, parental provisioning effort;
Williams and Vézina 2001), and why some studies report
contradictory results in different years (e.g., Stevenson
and Bryant 2000).
ACKNOWLEDGMENTS
We are grateful to Oliver P. Love, Katrina G. Salvante,
Julian K. Christians, François Fournier, Piet van den Hout,
Mark A. Chappell, Joseph B. Williams, and Theunis Piersma
for stimulating discussions and comments on earlier versions of
October 2006
ENERGY MANAGEMENT IN EGG-PRODUCING BIRDS
this article. We also thank Dr. Paula Redman and Peter
Thomson for DLW analysis as well as Andréa and JeanBaptiste Vin for their help with bird care and data collection
and processing. A special thanks to Ray Holland, who designed
and built the automated micro-switch monitoring system that
allowed to record hopping activity in Zebra Finches. This
research was funded by an operating NSERC grant to T. D.
Williams, post-graduate funding to F. Vézina from NSERC
and FCAR, and student research grants from SICB, Sigma Xi
and AOU to F. Vézina.
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