Steroids for free? No metabolic costs of elevated maternal androgen levels in the black-headed gull
1 Dept of Animal Behaviour, University of Groningen, PO Box 14, 9750 AA,
Haren, The Netherlands
2 Centre for Isotope Research, Nijenborgh 4, 9747 AG Groningen, The
Netherlands
* Author for correspondence (e-mail: c.m.eising{at}biol.rug.nl)
Accepted 23 June 2003
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Summary |
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Key words: yolk androgen, maternal hormone, metabolism, energy consumption, daily energy expenditure, sibling competition, parental investment, chick growth, black-headed gull, Larus ridibundus
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Introduction |
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These beneficial effects of yolk androgens have mainly been discussed in
the context of hatching asynchrony. For instance, experimental elevation of
yolk androgen levels decreased the time until hatching by half a day in
black-headed gull chicks [Larus ridibundus;
Eising et al., 2001; but see
Sockman and Schwabl, 2000
for
an opposite effect in American kestrels (Falco sparverius)]. This is
in accordance with the data presented by Lipar and Ketterson
(2000
) and Lipar
(2001
), who showed that
increasing levels of yolk testosterone according to laying order were
associated with an enlarged size of the hatching muscle in European starling
(Sturnus vulgarus) and red-winged blackbird (Agelaius
phoeniceus) chicks. Moreover, since body mass and tarsus length at
hatching of gull chicks from androgen-treated eggs were equal to those of oil
controls, maternal androgens appear to enhance overall embryonic growth.
Growth after hatching can be significantly enhanced by yolk androgens
(Schwabl, 1996
;
Eising et al., 2001
). Also,
long-term enhancing effects of maternal yolk androgens on competitive
behaviour have been reported both in canaries (Serinus canaria;
Schwabl, 1996
) and in gulls
(Eising and Groothuis,
2002
).
However, the occurrence of large within- and between-clutch variation in
the deposition of maternal androgens (e.g.
Schwabl et al., 1997;
Reed and Vleck, 2001
;
Groothuis and Schwabl, 2002
)
begs the question of why not all mothers invest high amounts of hormones into
their eggs, unless there is a cost involved. This cost may either be incurred
by the mother producing the androgens or by the chicks exposed to them.
Steroid hormones can entail immunosuppressive costs (e.g.
Mooradian et al., 1987;
Ketterson and Nolan, 1999
;
Peters, 2000
; but see also
Ros et al., 1997
;
Braude et al., 1999
;
Hasselquist et al., 1999
),
which is also suggested for maternal androgens (T. G. G. Groothuis, C. M.
Eising, C. Dijkstra and W. Müller, manuscript submitted;
Müller et al.
, in press).
High yolk androgens may also induce detrimental levels of sibling competition
or metabolic costs. In the present study, we focus on the latter.
It has often been suggested that testosterone (T) enhances metabolic rate.
Such T-dependent metabolic costs have, for instance, been suggested in gulls
soon after hatching (Ros,
1999). However, data available in the literature are rather
controversial. Studies in the late 1920s showed a reduction of diurnal
metabolic rate in castrated chickens (Gallus gallus) compared with
intact controls (Mitchell et al.,
1927
). Similar results were presented for Japanese quail
(Coturnix coturnix japonica;
Feuerbacher and Prinzinger,
1981
) and for spotted munia (Lonchura punctulata;
Gupta and Thapliyal, 1984
).
Yet, an increase in body mass usually accompanies castration and may have
accounted for the reported differences. Ketterson et al.
(1991
) experimentally showed
in adult male dark-eyed juncos (Junco hyemalis) that, at least prior
to and during the breeding season, high circulating T levels were accompanied
by a reduction in body mass and fat storage, suggesting that high T levels may
be energetically costly. More directly, Buchanan et al.
(2001
) experimentally showed in
male house sparrows (Passer domesticus) that elevated testosterone
levels increased metabolic rate and development of an androgen-dependent
sexual ornament, the bib size, suggesting a metabolic cost of dominance
signalling. By contrast, testosterone implantation in intact birds did not
affect mass-specific basal metabolic rates in captive male white-plumed
honeyeaters (Lichenostomus penicillatus;
Buttemer and Astheimer, 2000
)
and in dark-eyed juncos (Deviche,
1992
). Unfortunately, no data were provided about the activity
levels of the birds in relation to treatment in either study. T-treated
white-crowned sparrows (Zonotrichia leucophrys gambelii) showed
increased activity levels and reduced resting metabolism
(Wikelski et al., 1999
). The
authors suggested that increased activity was compensated by a reduction of
resting metabolic rate (RMR; analogous to
Deerenberg et al., 1998
). The
effect of androgens on metabolism is thus yet far from clear.
So far, no data have been reported on the relationship between maternally derived yolk androgens and metabolism. Are chicks facing a trade-off between beneficial effects of maternal androgens on the one hand and costs in terms of energy expenditure on the other? Therefore, we studied whether metabolic rates and daily energy expenditure of black-headed gull chicks hatching from eggs injected with androgens differ from those of chicks from oil-injected eggs during different stages of development. Since the black-headed gull is a sexually dimorphic species and significant sex differences in growth occur around day 15 after hatching (W. Müller, C. M. Eising, C. Dijkstra and T. G. G. Groothuis, unpublished data), we also included a comparison between the sexes.
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Materials and methods |
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Egg injections
Black-headed gulls lay a modal clutch of three eggs, in which androgen
levels increase significantly with laying order
(Eising et al., 2001;
Groothuis and Schwabl, 2002
).
In all experiments, we used only first-laid eggs, since the eggs of a clutch
not only differ in androgens but also in mass, protein and water content and
vitamins (Heaney et al.,
1998
). This enabled us to elevate the hormone level by injections
to the same as that of normal last-laid eggs, hence within the physiological
range of the species. We used the same procedures to select, calculate the
dose to be injected and inject our eggs as in a previous study
(Eising et al., 2001
).
Androgen treatment consisted of injection of a mixture of 0.12 µg
testosterone and 10.0 µg androstenedione per 50 µl of oil. After
hatching, all chicks were marked with a small, numbered, plastic band for
individual identification.
DEE and resting metabolic rate (RMR) of older chicks
In 2000, we first measured DEE in the field and then RMR in the lab in 29
individuals between day 20 and day 32 after hatching. These 15 Oil and 14 T
chicks were reared in the field by their foster parents and were part of an
experiment focussing on the effect of maternal yolk hormone levels on begging
behaviour (Eising and
Groothuis, in press). For a description of the study site and the
gull breeding system, see Eising et al.
(2001
). For this experiment,
chicks from T- and oil-injected eggs (see below) were matched for age and body
mass in two chick nests. Groups of these nests were located in enclosures
(wire mesh covered with cloth; 60 m2; 4050 cm high) to
facilitate re-capturing of chicks. To measure oxygen consumption, chicks were
caught from their enclosures at around 19.00 h and were transported to the lab
facilities, where the RMR protocol (see below) started at around 21.30 h. This
was conducted on the day that the final blood sample for the DEE measurement
was taken in the afternoon. Chicks were measured overnight and then returned
to the field. Parents readily accepted the chicks and there was no effect on
survival probabilities.
Resting metabolism
In 2001, we measured RMR of young chicks when they were presumably still
consuming yolk and of older chicks under conditions at or below
thermo-neutrality (15°C). Chicks from T- and oil-injected eggs were
brought to the lab around hatching and were subsequently hand reared. During
the first week after hatching, chicks of both treatments were matched for age
and mass and, from then on, were housed in pairs in cages (0.9 mx0.75 m;
0.9 m high). Food and water were provided ad libitum. Between the age
of 2 days and 10 days, oxygen consumption of 29 T and 24 Oil chicks was
measured under thermo-neutral conditions. Another set of chicks was measured
when they were between 20 days and 30 days old, either at thermo-neutral
conditions (25°C; 14 T, 15 Oil) or below thermo-neutral (15°C; 10 T,
16 Oil).
In 2002, we measured metabolic rates just prior to and just after hatching, when chicks are still consuming yolk and are therefore exposed to the manipulated levels of androgens. Freshly laid eggs were brought to the lab, injected there (see below) and hatched in an incubator. Oxygen consumption of eggs was measured on the day aimed to be 2 days prior to hatching (32°C; 23 T, 23 Oil). Subsequently, the oxygen consumption of the chicks was measured on the day of hatching (32°C; 15 T, 19 Oil) or two days after hatching (30°C; 13 T, 11 Oil).
Indirect calorimetry
Oxygen consumption measurements were performed in darkness at temperatures
ranging between 25°C and 32°C, which is thermo-neutral for gulls. In
2001, we also measured oxygen consumption of older chicks at 15°C, which
is below thermo-neutral. In 2000 and 2001, oxygen consumption of chicks was
measured overnight in individual airtight boxes (20 litre) equipped with a
movement detector and a temperature sensor. In 2002, oxygen consumption of
eggs and chicks was measured during the day for at least four hours in smaller
respiration chambers (2 litre). Paper towels provided bedding. Food and water
was not provided during the measurements but always directly thereafter. Just
before and after the measurement, chicks were weighed to the nearest 0.1
g.
Measurements were conducted in an eight-channel open flow system. Dry
outdoor air was passed through each of the eight chambers. Flow rates were
measured and controlled with a mass flow control (Brooks, Model 5850S;
Rosemount Inc., Veenendaal, The Netherlands) set to maintain the oxygen and
carbon dioxide concentrations in the outlet air above 20% and below 1%,
respectively. Oxygen and carbon dioxide concentrations of dried inlet and
outlet air from each chamber were measured every 10 min with a paramagnetic
oxide oxygen analyser (Xentra 4102; Servomex, Zoetermeer, The Netherlands) and
an infrared carbon dioxide gas analyser (1440C1 STD; Servomex). Data points
were collected from each metabolic chamber separately and stored by computer.
Oxygen consumption was calculated according to Hill
(1972) to correct for volume
changes with respiratory quotient below
Energy metabolism and maternal androgens
1 and expressed in standard temperature and pressure. The first hour and
last 30 min of every measurement were excluded from the analyses.
Six measurements were taken from each chick per hour, and 30 min running
means were calculated to determine the lowest average, which was taken as the
measurement of RMR for each individual. To be able to compare DEE and RMR,
oxygen consumption was expressed in kJ h1 using the
gas-exchange conversion factors of Gessaman and Nagy
(1988).
Daily energy expenditure
Rates of DEE of free-living chicks were estimated with the doubly labelled
water method (DLW; Lifson and McClintock,
1966; Speakman,
1997
). During the field season of 2000, 28 chicks were injected
intra-peritoneally with 0.8 ml of a mixture of H218O and
2H2O using calibrated 1-ml insulin syringes. Based on
the principle of isotope dilution (Visser
et al., 2000
), the 2H and 18O concentrations
in the DLW mixture were calculated to be 34.8% and 61.4%, respectively. After
an equilibration period of 1 h (Speakman,
1997
), the chick was weighed with an electronic balance to the
nearest 0.1 g, and a blood sample (`initial') was taken by puncturing the
brachial vein with a sterile needle and subsequently filling 46 glass
capillaries each with 15 µl blood. Capillaries were flame-sealed
immediately and stored at 4°C until further analysis. Thereafter, the
chick was returned to its nest. After 48 h, the chick was recaptured,
reweighed and another blood sample (`final') was taken following the same
procedures as outlined above. Blood samples of six other chicks were taken for
assessment of the natural abundances of 2H (152.3±0.98 atom
percent) and 18O (2000.6±2.27 atom percent).
Blood samples were analysed in triplicate at the Centre for Isotope
Research at the University of Groningen. For each individual, its amount of
body water was determined following the principle of 18O dilution,
using the quantity and 18O enrichment of the dose, the
population-specific 18O background concentration and the
individual-specific 18O concentration of the initial blood sample.
The daily CO2 production was calculated for each animal using
Speakman's (1997) equation
7.17. DEE is expressed as kilojoules spent per day. For a detailed description
of the analytical and calculation procedures, see Visser and Schekkerman
(1999
) and Visser et al.
(2000
).
Statistical analyses
All data on oxygen consumption and DEE were normally distributed for all
age classes and could therefore be tested parametrically using General Linear
Models (GLM) with or without repeated measures or by independent sample
t-tests. The variables of interest treatment, sex and age
and their possible interaction effects were only retained in the full
models when they reached statistical significance (P<0.05). If no
statistical significance was reached, single independent models are presented.
Power analyses were performed using the program GPOWER (shareware;
Erdfelder et al., 1996).
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Results |
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Peri-natal RMR
Before hatching
Table 1A shows the mean egg
mass-specific RMRs per treatment per age class. When tested in a GLM,
including treatment and sex, mass-specific metabolic rates prior to hatching
increased significantly with age (F1,33=37.87,
P<0.001). Since T treatment is known to decrease the time until
hatching (this sample: T, 23.47±0.24 days; Oil, 23.94±0.24 days;
F1,33=2.02, P=0.17) and therefore age at hatching
may not be similar, we also looked at the relationship between mass-specific
RMR and the number of days after egg laying and found there was no such
relationship (F1,44=0.02, P=0.89).
|
In the first model, there was no effect of treatment or sex on the eggs' RMR. Unfortunately, sex was not always known, which diminishes the sample size in the full model. Therefore, the effect of treatment was also determined over the total sample size (N=46) independently of sex. There was again no treatment effect on the mass-specific RMR of the eggs. When RMR was corrected for chick hatching mass instead of egg mass, there was still no significant effect of treatment (F1,37=2.47, P=0.12) or sex (F1,35=0.02, P=0.90). Thus, during embryonic development, androgen treatment did not affect metabolic rates.
After hatching
19 chicks (9 T, 10 Oil) were measured both at hatching and two days later,
and a repeated-measures analysis of variance (ANOVA) shows that there was a
significant positive effect of age (the repeat) on mass-specific RMR
(Fig. 1B;
Table 1B). Treatment and sex
had no effect on RMR.
The data for age 0 days and age 2 days have also been analysed separately in order to have a larger sample size at both ages. At age 0 days, there was no significant difference in RMR between the T and the Oil group or between males and females. Mass-specific RMR was higher at age 2 days than at age 0 days. Again, there was no statistical difference between the RMRs of both treatment groups or an effect of sex. In conclusion, around hatching there were no indications of an effect of treatment or sex on chick metabolic rates.
Early post-hatching metabolism
Early post-hatching RMR under thermo-neutral conditions is presented in
Table 1C. None of the tested
variables (age, treatment and sex) or their interactions contributed
significantly to the explained variance in RMR.
RMR of older chicks at and below thermo-neutral conditions
Metabolic rates of chicks measured below thermo-neutral at 15°C were
significantly higher (F1,53=8.75, P<0.005)
than those of chicks measured at thermo-neutral conditions
(Table 1C). Overall, treatment
had no effect on RMR (F1,53=0.64, P=0.43).
Also, within each temperature range there was no effect of treatment. Overall, we found an almost significant effect of sex (F1,51=3.77, P=0.06) on oxygen consumption. Males (N=30, mean age 23.7 days) consume on average 35.10±0.65 J h1 g1, whereas females (N=25, mean age 23.8 days) consume 37.46±0.90 J h1 g1. However, there was also a significant interaction effect of sex and temperature (F1,51=4.00, P=0.05). In conditions below thermo-neutral, oxygen consumption of females was significantly higher than that of males, whereas in thermo-neutral conditions oxygen consumption of males and females was similar (Table 1C). At this age range, there was also a significant difference in body mass (males, 279.4±4.36 g; females, 246.36±5.04 g; F1,53=24.83, P<0.001) between males and females, which may have caused differences in thermo-regulatory costs (see Discussion).
To increase the power of the test regarding treatment and sex, data measured in older chicks in thermo-neutral conditions were combined for both years (2000 and 2001) in a full factorial GLM. The result confirmed that none of the variables tested significantly affected RMR (treatment: F1,50=0.36, P=0.55; sex: F1,50=1.85, P=0.18; age: F1,50=0.25, P=0.62).
The above results confirm the finding of the previous experiment that exposure to androgens during embryonic development does not affect oxygen consumption post-hatching in thermo-neutral conditions.
RMR of older chicks reared in the field
The mean energy consumption in the T and Oil groups and for males and
females is presented in Table
1D. None of the variables tested (age, treatment, sex or
interactions) using backward GLM contributed significantly to the explained
variance in mass-specific RMR.
Daily energy expenditure
DEE averaged 341.2±14.8 kJ day1 (mean ±
S.E.M., N=15) in the Oil group and 346.2± 4.9 kJ
day1 (N=13) in the T group, which was not
statistically different (F1,23=0.17, P=0.68).
Over the age range studied (2230 days), age did not affect DEE
(F1,26=0.74, P=0.40). There was also no effect of
sex (males, 349.0±7.0 kJ day1, N=8; females,
346.7±10.2 kJ day1, N=19;
F1,23=0.06, P=0.81) nor an interaction effect of
treatment and sex (F1,23=0.34, P=0.56). It is
unlikely that body mass differences obscured an effect of treatment since
there was no significant difference in body mass between treatment groups (T,
204.79±7.19 g; Oil, 207.67±8.74 g; t27=0.25,
P=0.80; males, 206.0±7.79 g; females, 208.9±7.14 g;
t26=0.24, P=0.81).
Activity-related metabolism
Activity-related metabolism (which consists primarily of activity and
thermo-regulatory costs) can be estimated roughly from the combination of DEE
and RMR data. By subtracting the RMR in kJ day1
(Gessaman and Nagy 1988) from
the DEE for each individual, we obtain an estimate for the activity metabolism
of each chick. The effect of treatment on this estimate was far from
significant (T, 184.37±11.88 kJ day1; Oil,
176.94±5.88 kJ day1; F1,26=0.29,
P=0.60) and so was the effect of sex (males, 181.74±10.54 kJ
day1; females, 182.99±8.88 kJ day1;
F1,25=0.01, P=0.94). Also, age did not affect
activity metabolism (F1,26=2.94, P=0.10).
The above results show that there was no effect of androgen treatment or sex on metabolic rates of black-headed gull chicks during the third and fourth week after hatching under natural conditions. Since the mean metabolic rates were very similar for both treatments and sexes throughout the age ranges over which we performed our measurements, we would have needed huge sample sizes (1304350) to obtain any statistically significant differences, which are then likely to be biologically irrelevant. Thus, we have obtained no indications that energy expenditure differs between chicks from eggs with low or high androgen content.
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Discussion |
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Pre-hatching RMR
Mass-specific metabolic rates increased towards hatching. In birds,
metabolism increases steeply during the last few days prior to hatching
(Prinzinger et al., 1995),
presumably associated with increased pre-hatching activity levels and
accompanying maintenance cost or changes in the water balance
(Vleck et al., 1980
).
In the present study, oxygen consumption did not differ between the T and
Oil eggs during the last days before hatching. Chicks from T-treated eggs
hatched slightly sooner but were not smaller at hatching, indicating that
testosterone stimulates pre-natal growth. This suggests we either measured
metabolic rates during the plateau phase
(Vleck et al., 1980;
Prinzinger and Dietz, 1995
;
Prinzinger et al., 1995
;
Dietz et al., 1998
), when
growth had already levelled off, or the differences in growth are so small
that they are not detectable in our RMR measurements.
Post-hatching RMR
Post-hatching RMR increased for the first few days after hatching and then
gradually decreased. This steep increase shortly after hatching is a common
phenomenon in both precocial and altricial species and is associated with the
development of mature function, including thermoregulation
(Klaassen et al., 1994).
We found no indication that metabolic rates differed between T and Oil
chicks after hatching. We expected to find such differences since T chicks are
more active than Oil chicks (Eising et al., in press) even when maternal
hormones are no longer present and such activity can be energetically costly
(e.g. Ricklefs, 1974;
Vehrencamp et al., 1989
).
Desai and Hales (1997
) also
suggested that maternal effects (nutritional status) play an important role in
`programming' the offspring's metabolism in later life. Moreover, testosterone
stimulates muscle growth, and muscles are a relatively energetically demanding
tissue (Piersma et al.,
1996
).
However, females had higher RMR than males below thermo-neutral conditions. Although RMR was expressed mass specifically, correcting for the significantly larger body mass in males relative to females (asymptotic body mass for males 261.4 g; females, 220.3 g; W. Müller, C. M. Eising, C. Dijkstra and T. G. G. Groothuis, unpublished data), this size difference may still account for the observed interaction effect of sex and temperature on RMR. Since heat conductance and insulating properties depend on surface-to-volume ratio, females might have to expend more energy to maintain body temperature.
Post-hatching DEE
We did not find an effect of treatment on daily energy expenditure nor on
activity metabolism. This suggests that the higher activity and begging
frequencies in T chicks (Eising and
Groothuis, in press) do not entail a detectable energetic cost or
result in a compensation mechanism. McCarthy
(1996
) and Bachman and
Chappell (1998
) already
suggested that the amount of energy allocated to begging behaviour in birds is
slight compared with the amount of energy needed for growth. Similarly, Lynn
et al. (2000
) showed in adult
dark-eyed juncos that testosterone increased activity but not daily energy
expenditure. In that study, testosterone did increase locomotion and foraging
behaviour whereas it decreased sleeping and preening. Lynn et al. proposed
that this differential allocation suggests that there may be long-term costs
associated with maintenance of elevated testosterone levels.
Overall, we have found no evidence that maternal androgens affect metabolism pre- or post-natally directly or indirectly via behaviour. There was neither an effect on RMR nor on DEE. This suggests that the behavioural changes evoked by maternal androgens are energetically cheap. There is no indication of an androgen-mediated trade-off between enhanced growth and begging behaviour on the one hand and metabolic costs in these chicks on the other.
The fact that we did not find differences in metabolic rates between T and
Oil chicks is unlikely to be due to failure of the treatment. The technique of
injecting androgens into eggs to mimic maternal variation has proven
successful in earlier studies, inducing faster growth and increased begging in
gull chicks living in natural conditions
(Eising et al., 2001;
Eising and Groothuis
, in
press). Although most analyses show a very low power, it may be clear from the
presented means that there is little scope for any statistical differences.
The minimum required sample size to obtain a significant treatment effect with
a power of 0.80 was 130, but most tests required close to 1000 individuals.
Similarly, to obtain a significant sex difference we would need, at a minimum,
sample sizes ranging between 580 and 4350, which suggests that there really
are no biologically relevant differences in energy turnover.
Next, potential effects of yolk androgens on metabolism should be measured earlier in the ontogeny.
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Acknowledgments |
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