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First published online December 26, 2008
Journal of Experimental Biology 212, 231-237 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.022640
Peak energy turnover in lactating European hares: the role of fat reserves
Research Institute of Wildlife Ecology, University of Veterinary Medicine, Savoyenstrasse 1, A-1160 Vienna, Austria
* Author for correspondence (e-mail: Teresa.Valencak{at}vu-wien.ac.at)
Accepted 18 November 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: energy allocation, parental investment, energetic cost, reproduction, reproductive effort, seasonal shift, allocation strategy, fat depletion, Lepus europaeus
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Hackländer et al.,
2002b). Because young hares start to consume substantial amounts
of solid food only around their third week of life, the major part of their
energy intake until weaning after approximately 4 weeks is obtained from milk,
which causes a high energetic burden for reproducing females
(Hackländer et al.,
2002b).
There are several observations indicating that female hares, similar to
other mammals, might indeed reach an upper limit of energy turnover –
i.e. maximum sustained metabolic rate (SusMR) – during lactation. Food
intake and milk production in hares increase rapidly but then level off after
the second week of lactation. Peak rates of energy assimilation at a high
litter size of three young have been estimated to range around five times
resting metabolic rate (RMR), which is comparable to SusMR in other small
mammals (Hackländer et al.,
2002b; Hammond and Diamond,
1997). Furthermore, as total litter mass increases, energy intake
and milk production of lactating females do not increase proportionally, and
consequently body masses of young at weaning decrease markedly with litter
size (Hackländer et al.,
2002a; Hackländer et al.,
2002b). Together, these findings suggest that female hares, like
other mammals, might face a physiological limit of energy throughput during
peak lactation. These limits have been related to the capacity of `central'
alimentary organs (Koteja,
1996), to peak metabolism in peripheral tissues such as the
mammary glands (Hammond et al.,
1996) or, more recently, to the maximum ability of females to
dissipate excess heat that is generated as a by-product of increased
metabolism (Krol et al.,
2007).
Most previous studies on SusMR during peak lactation have used small
rodents, such as laboratory mice, as animal models. Arguably, in these
species, reproductive performance is determined mainly by the maximum rate of
energy assimilation from food and its conversion to milk, because they lack
sufficient body energy reserves that could be used to supplement milk
production. European hares, however, are well known to build up considerable
fat deposits in autumn and winter (their non-breeding season in central
Europe) (Zörner, 1996)
and might even partly restore fat deposits during the non-reproductive period
or during gestation in the breeding season. Until now, the role of these body
fat reserves for the lactation performance of European hares was unclear,
however. As presented in Drent and Daan
(Drent and Daan, 1980),
breeding females in general might shift between two different strategies of
resource allocation. The `capital breeder' strategy refers to females using
their own body fat reserves to cover the high energetic costs of reproduction,
whereas `income breeders' are considered to raise their energy or food intake
when facing high energy demands. We hypothesized that fat deposits accumulated
over winter could serve lactating hares as an additional milk energy supply,
in particular for the first litters of the year. If that were the case, a
gradual shift from a predominantly `capital' to an `income' strategy over the
breeding season (February to October in central Europe) would give rise to
several possible scenarios of maternal investment during peak lactation: (1)
females could use body fat reserves to supplement milk fat while keeping peak
food intake and energy assimilation (i.e. SusMR) constant; (2) females could
maintain constant energy transfer to young by adjusting/reducing food energy
intake when fat deposits are available; (3) females could adjust both milk
energy transfer and energy assimilation during the breeding season. In all of
these scenarios, it is of interest to determine whether possible seasonal
changes in milk fat content are compensated by adjustments of milk production
(i.e. quantity).
To address these issues, we determined energy intake, milk transfer and
milk energy content throughout lactation in laboratory-housed European hares
at three times during the breeding season: in spring, summer and autumn. To
keep the energetic costs of reproduction comparable between females, litter
sizes were kept constant at three leverets. To minimize external limitations,
all experimental females were given a high-fat diet ad libitum
throughout the experiments. In the wild, hares are very selective on their
diet and pick food plants rich in fat
(Reichlin et al., 2006). Our
laboratory diet, which was arranged to match average stomach contents of
carbohydrate, protein, fat and fibre in free-ranging hares
(Hackländer et al.,
2002b), but with the addition of 10% oil, simulated optimal
provisioning with fat even better than in natural set-asides, where hares can
select preferred food plants. We also determined the growth and solid food
intake of young to assess the possible effects of changes in lactation
performance on the offspring.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). All animals (females and young) were provided with water
and food ad libitum. Food pellets (Raiffeisen, Salzburg, Austria)
were enriched with sunflower oil (12.5 kg oil per 100 kg pellets). The mean
gross energy content of the diet over the whole study period was
19.09±0.03 kJg–1 with 15.3±0.04% protein,
16.1±0.04% fibre and 13.4±0.07% fat. To ensure that the energy
content and particularly the fat content were stable throughout the study
period, we analysed dietary fat content every time the pellets were mixed with
oil. The analyses of the diet were performed as described by Hackländer
and colleagues (Hackländer et al.,
2002b). Data were sampled between February 2004 and October 2007 on a total of 28 mothers and their 50 litters. All experimental animals were aged between 1 and 5 years and were in good health and condition. Hares were exposed to a natural photoperiod and to indoor temperatures in an unheated housing facility that varied between 8°C and 25°C over the study period, but mean ambient temperature varied by less than 2.5°C between the three seasons (see below). During the 9-month yearly reproductive period, the body mass of all animals was determined weekly to the nearest gramme. Food intake was determined over bi-weekly feeding trials (over 3- and 4-day intervals) by weighing offered and uneaten food in all females, resulting in eight data points for each female per 28 d lactation period. Food items spilled from the racks were dried, weighed and subtracted from food consumption. To minimize effects of changes in humidity, food pellets were stored next to the cages before usage.
Total faeces produced by the animals were collected biweekly over 3- and
4-day intervals, dried at 60°C in a drying oven (Heraeus, Germany) for 48
h and then the mass determined to the nearest 0.1 g (Ohaus, Germany). It was
impossible for us to distinguish between old and new faeces, and similarly we
were unable to assess the amount of re-ingested faeces because hares perform
coprophagy by taking up faeces right from the anus and re-digesting it. Gross
energy content was determined for faecal samples by near-infrared spectroscopy
(NIRS). Samples were analyzed using a FT-NIR spectrometer MPA (Bruker Optik
GmbH, Ettlingen, Germany) with an integrating sphere in diffuse reflection.
The samples were measured in a rotating cup with a diameter of 50 mm three to
six times each using a resolution of 8 cm–1 and 64 scans. The
spectrometer was equipped with software OPUS 5.5 with the additional packages
OPUS/LAB and OPUS/QUANT (2005, Bruker, Ettlingen, Germany). The following
parameters were determined: dry matter, protein, fat, ash, acid detergent
fiber (ADF) and lignin. Nitrogen free extracts (NFE) were computed by
subtracting lignin from ADF. For calibration of the NIRS analysis, 80 samples
were chemically analyzed using standardized methods for crude protein, crude
fat, crude ash and dry matter (Nehring,
1960). ADF and lignin were determined by Van Soest detergent
analyses (Otzelberger, 1983).
The NIR calibration results were evaluated by cross validation. Coefficients
of determination for fat, protein, ash, lignin and dry matter were 0.93, 0.93,
0.83, 0.87, 0.87 and 0.96, respectively.
Females were paired with males for two days three times per year –
i.e. in February–March (spring), May–June (summer) and
late-July–August (autumn). To allow litter size manipulations, matings
took place synchronously each time. Immediately after birth of the young
(40.8±0.13 days after mating), litter sizes were manipulated to achieve
a litter size of three for all females investigated. Mean litter size amounted
to 1.3, 1.7 and 1.2 for spring, summer and autumn, respectively, and did not
differ significantly between seasons (F2,71=2.45,
P=0.09). These litter sizes are also comfortably in the range of
litter sizes in free-ranging hares (1–5, average 2–3)
(Zörner, 1996). We did
not fully cross-foster litters, but in most cases we added one or two pups
from another female, which was then left without pups until the next mating.
All females readily accepted and nursed additional young, independent of
whether they were crossfostered. Note that long-term data from our breeding
colony show that only 10.1% of all females have litters larger than three
leverets (N=813 litters) and very few females are able to wean
successfully more than three young. Thus, by raising three leverets, all
females in our experiment had high (see also
Hackländer et al., 2002b)
and approximately equal energy requirements.
Females were kept separately from their young, except for a short nursing
period in the morning (8–9 am), which simulates the short daily nursing
bouts of free-living hares (Broekhuizen and
Maaskamp, 1980). The milk intake of young was measured daily by
weighing the leverets before and after the 1 h suckling period, with the mass
determined to the nearest 0.1 g. Initial trials showed that mass losses during
the nursing period due to faeces and urine losses in juveniles were negligible
(<2 g per juvenile) in comparison with the milk intake (
60 g).
Therefore, faeces and urine losses during these periods were not determined.
During this period, leverets had no access to other food sources. Otherwise,
the leverets had ad libitum access to the same food as adults, and
the food intake of each litter was determined at weekly intervals. During each
season, small milk samples (<3 ml) from a subsample of females were
collected and chemically analyzed as outlined by Hackländer and
colleagues (Hackländer et al.,
2002b). In one year of our study (2005), we added a saturated
fatty acid, undecanoic acid (C 11:0; Sigma Aldrich, Germany), which does not
naturally occur in the diet of hares, to the pellets (17.66 g undecanoic acid
per litre sunflower oil) and fed it to experimental mothers each time they
were gestating, but not during lactation. This was to see whether undecanoic
acid would be incorporated into fat reserves and later transferred to milk
during lactation. The concentration of undecanoic acid in milk samples was
determined by gas-liquid chromatography (Perkin Elmer Autosystem XL with
Autosampler and FID; Norwalk, CT, USA) using a capillary column (HP INNOWax,
30 mx0.25 mm; Hewlett Packard, USA). Fatty acid methyl esters from milk
were identified by comparing retention times with those of fatty acid methyl
ester standards (Sigma Aldrich, St Louis, MO, USA). Peaks were integrated
using Total Chrom 6.3. software (Perkin Elmer, Norwalk, CT, USA).
For reasons of management of our breeding colony, we had to kill some females at the end of each breeding season in the autumn. From this subsample of animals that were either non-reproducing (N=78), or post-lactating (N=19; on the day of weaning of young), we determined the fresh masses of completely dissected peri-renal white adipose tissue deposits, with masses determined to the nearest 0.1 g.
Computation of energy contents and statistical analyses
The energy content of solid food and faeces was calculated by using
energetic values given in Livesey
(Livesey, 1984) and Livesey
and Marinos (Livesey and Marinos,
1988). Thus, the gross energy content of protein, fat and
fibre/nitrogen-free extract (NFE) was 23.3 kJg–1, 39.6
kJg–1 and 17.5 kJg–1, respectively. Gross
energy intake (GEI) was computed from the amount of food consumed per day
multiplied by its energy content. Metabolizable energy intake (MEI) was
calculated by (i) correcting GEI for urinary energy losses due to nitrogen
excretion by using a metabolizable protein energy content of 19.3
kJg–1 (Livesey,
1984) and (ii) computing the difference between this corrected,
utilizable GEI and the energy content of the daily amount of faeces excreted.
The estimated average urinary energy loss was 3.3% of GEI. Energy assimilation
rates were computed as: (MEI/GEI)x100. The conversion factors above
(using 19.3 kJg–1 for protein), as well as an energetic value
of 16.5 kJg–1 of lactose
(Stubbs et al., 1997), were
also used to compute milk energy content. To allow comparison with published
data from other species, multiples of mass-specific resting metabolic rate
(RMR) were computed by dividing both mass-specific GEI and mass-specific MEI
by 172.3 kJ kg–1 day–1, the RMR of
non-reproducing hares at thermoneutrality (20°C) measured for 4 h with
open-flow respirometry, as outlined elsewhere
(Hackländer et al.,
2002a).
Data on female food intake, GEI, MEI, milk production, milk energy
transfer, mass of fat deposits in females, as well as growth of young
(weaning, birth masses) and solid-food intake of litters were analysed with a
repeated measures design, as data within and partly between study years were
sampled from the same animals. We fit linear mixed-effect models, with
separate intercepts for each female included as the random factor. In models
involving juvenile growth and juvenile food intake, we used `litter' as the
random factor. Fixed effects in these multiple-regression models were
lactation week (fitted by a quadratic term owing to the nonlinear time-course
of all variables tested) (e.g. Fig.
1), season (spring, summer, autumn), ambient temperature, female
age (1–5 years) and mean ambient temperature over the measurement
interval. The body masses of females differed slightly between seasons
(3480±42 g, 3402±26 g and 3510±32 g in spring, summer and
autumn respectively). However, the possibly confounding effect of individual
body mass was eliminated by inserting body mass as a covariate in all models
for data obtained from females. In some cases, regression models and ANOVAs
were also computed for the second half of the lactation period, which is
considered to reflect peak lactation (intervals 5–8). Full models
indicated that none of the response variables showed a further significant
increase during this last phase. Residuals from all models were normally
distributed and showed no evidence for heterogeneity of variances. Only for
one response variable – milk undecanoic acid content – were data
non-normally distributed owing to the fact that all values in autumn were
below the detection level and set to zero. Therefore, we used a
Kruskal–Wallis H-test to compare seasonal differences in undecanoic acid
content. We tested for all possible two-way interactions, but none of them
reached significance. All statistical analyses were computed in R (2.7.0.)
(R Development Core Team,
2008), using the package nlme
(Pinheiro et al., 2008). The
data are presented as means ±s.e.m.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Determinants of MEI
Surprisingly, MEI was not constant over the breeding season but increased
significantly in autumn (Fig.
2). This was the case whether the entire lactation period was
considered (F2,314=7.60, P<0.001) or peak
lactation only (F2,178=7.30, P<0.001). This
difference between seasons was not due to differences in mean ambient
temperature, which varied only slightly between spring
(17.14±0.38°C), summer (19.24±0.15°C) and autumn
(17.91±0.29°C). Also, MEI was only slightly affected by the age of
females (F4,314=2.25, P=0.06), owing to an 8.2%
lower MEI in young females (age 1).
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2=9.5337, d.f.=2,
P=0.008). Fat mobilisation during lactation was indeed restricted to
the first and second litters in the year because undecanoic acid could not be
detected in autumn milk samples. In autumn, females had significantly less
retroperitoneal white adipose tissue immediately after the weaning of young
than non-reproducing hares that were sacrificed at the same time
(Fig. 6)
(F1,32=13.03, P=0.001).
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Energy budgets
The energy budgets of females during the three breeding seasons are given
in Table 1. The transfer of
body energy reserves to milk in spring (see above) was estimated from the
difference between mean milk energy transfer during the first (spring) and
later litters (summer and autumn). These budgets indicate that the amount of
energy allocated to milk derived from food consumption was approximately equal
(270 kJ kg–1 day–1) at all seasons.
Also, the resulting amount of energy from MEI used for maintenance and
thermoregulation (MEI–milk energy from food) was not different between
spring and later litters (F1,321=2.18,
P=0.14).
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Growth and energy consumption of young
During all seasons, the costs of growth were predominantly covered by milk
energy. The gross energy used from milk per gramme of body mass increase (day
1–28) was 21.9±0.62 kJ day–1, 15.1±0.36
kJ day–1 and 16.6±0.60 kJ day–1 in
spring, summer and autumn, respectively. Gross energy consumption from solid
food amounted to 1.04±0.12 kJ day–1 (spring),
1.32±kJ day–1 (summer) and 1.47±0.07 kJ
day–1 (autumn).
The mean birth masses of young were similar at all seasons (124.4±2.89 g in spring, 123.2±2.37 g in summer and 127.4±3.19 g in autumn). Mean weaning masses at day 28 were 627.7±22.8 g in spring, 690.3±20.5 g in summer and 734.0±30.6 g in autumn. The corresponding slight differences in gain in mass were statistically not significant (F2,16=2.516, P=0.112). The fact that weaning masses remained stable indicates that leverets apparently compensated for the seasonally decreasing milk quality by consuming more solid food and thereby increasing GEI during late lactation in summer and autumn (F6,151=3.83, P=0.0014; weekxseason interaction). This effect was most pronounced in week four of lactation, during which mean solid food intake per litter was 236.4±39.7 kJ day–1 per litter in spring, 277.3±26.8 kJ day–1 in summer and 422.7±37.7 kJ day–1 in autumn.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Hackländer et al., 2002b).
Other precocial mammals, such as the Guinea pig, elevate rates of energy
turnover to only 3.9 times RMR. This is mainly because juvenile Guinea
pigs start to feed on solid food (in addition to milk) even on their first day
of life (Künkele and Trillmich,
1997; Künkele,
2000). Juvenile hares, however, which start to consume substantial
amounts of solid food only in week three, depend to a much higher degree on
their mother's milk, so their early life development is determined by maternal
nutrition and energy allocation (c.f.
Rogowitz and McClure, 1995).
Hence, sustained MEI and GEI in female hares reached up to 6.2 and 9.3 times
RMR, respectively, suggesting that they might reach a metabolic ceiling during
lactation. This is well in the range of SusMR in altricial small rodents where
sustained MEI and GEI were reported to amount to six and eight times RMR,
respectively (Hammond and Diamond,
1997; Johnson et al.,
2001). Contrary to mice, for which assimilation efficiency was
reported to remain constant (at 80%) throughout lactation
(Johnson et al., 2001), hares
showed a 7.5% decrease in digestible energy. Similar changes in digestible
energy have been observed in small rodents when food intake increased in
response to cold exposure (Liu et al.,
2002; Song and Wang,
2006). In hares, which have generally low mean retention times of
digesta in their gastrointestinal tract
(Stott, 2008), the observed
drop in assimilation efficiency during lactation might have resulted from a
further decrease of mean retention time, along with the simultaneous increase
in food intake.
The very high levels of energy intake could suggest that female hares
approached an upper physiological limit during peak lactation, particularly in
autumn. This hypothesis is also corroborated by the strong decrease in weaning
mass with increasing litter size
(Hackländer et al., 2002a;
Hackländer et al., 2002b).
Furthermore, the time-course of increasing GEI and MEI during lactation
(Fig. 1) and the associated
energy assimilation rates indicate that increased food intake was accompanied
by a decline in the efficiency of digestion caused, for instance, by an upper
limit in the capacity of alimentary organs. Thus, based on these observations
alone – without discriminating between seasons – we would conclude
that the observed peak levels of sustained energy turnover in hares were
probably due to physiological constraints, whether they act `centrally' on
energy intake, `peripherally' on energy output or otherwise (for a review, see
Speakman, 2008). However, our
comparison of seasons shows that females in autumn were able to further
increase MEI significantly, compared with spring and summer
(Fig. 2). Our data give no
evidence for seasonal changes in juvenile energy demands that could have
caused these adjustments of MEI in females. Birth and weaning masses of
juveniles did not differ throughout the seasons. Also, mean ambient
temperature, which affects the thermoregulatory costs of juveniles, varied
little between seasons and had no detectable effect on female energy
turnover.
Therefore, it seems that seasonal changes in reproductive investments were
driven by the availability of fat stores that allowed females to downregulate
energy intake and expenditure in the early breeding season. Late-season
breeding then forced females to elevate their energy intake in order to
compensate for the lack of body fat reserves at that time of the year. It
remains to be seen whether this peak rate of energy turnover in autumn
actually represents a physiologically constrained upper limit of SusMR in
hares or whether still-higher levels might be reached under other conditions
– i.e. additional cold load. However, our findings that females (i)
downregulated energy turnover in spring and summer and (ii) did not fully
compensate in terms of total milk energy output for the lack of body reserves
in autumn both point to adverse effects of very high energy turnover, and
hence to trade-offs between current and future reproduction. Generally, there
appears to be a trade-off between reproduction and survival and between
current and future reproduction (Williams,
1966; Stearns,
1989). Thus, limiting the upper level of energy turnover early
might well represent a `prudent parent' strategy
(Drent and Daan, 1980) in hares
that serves to maximise lifetime reproductive success.
Currently, we can only speculate about the nature of the potential fitness
costs associated with intense levels of energy throughput in hares. Two
mutually compatible consequences of high rates of SusMR could be: (i)
increased rates of aging and (ii) increased predation risk. High levels of
metabolic rate are known to cause mitochondrial lipid peroxidation that leads
to deleterious products such as reactive aldehydes, which cause damage to
membranes as well as enzymes and inhibits DNA and protein synthesis
(Hulbert, 2005). Although
there is probably no simple relationship between metabolism and longevity
(Speakman, 2005), it has been
argued that rapid changes between lower and peak rates of energy turnover, as
occur in the time-course of lactation, are particularly damaging and might
impair life span. This could be because such fluctuations lead to a temporal
imbalance between deleterious metabolic products and anti-oxidant defence
systems (Demetrius, 2004;
Demetrius, 2005). A second,
simpler explanation for the costs of high SusMR is that increased food intake
and hence foraging is probably associated with increased locomotion,
conspicuousness and thus predation risk
(Jönsson, 1997;
Kraus et al., 2008).
Consequently, limiting risky foraging, whenever body energy reserves allow
this strategy, should increase longevity and fitness. A prerequisite for this
tactic is resource allocation to energy stores before, and their use during,
the breeding season (Speakman,
2008). This was clearly the case in the females studied here. Our
feeding trials using undecanoic acid as a marker for mobilization of fat
reserves demonstrated that, early in the breeding season, mothers transferred
fatty acids to milk that had been stored previously. Also, the observed
decrease of milk fat and energy content over the reproductive season
(Fig. 3) suggests that body
energy reserves stored during the previous winter served as an important
resource for provisioning the first litters of the year. Thus, lactating hares
might use stored fat reserves to reduce predation risk caused by high energy
needs.
During the peak of their seasonal body fat cycle (approximately 2 months
before the onset of the breeding season), captive female hares can have total
body lipid stores of 8% of body mass, amounting to 280 g in a 3.5 kg animal
(F. Tataruch, unpublished observations from total carcass analysis). The
difference in milk fat content between spring and later litters in the present
study showed that, during the spring lactation period, mothers on average
transferred 195 g of body fat reserves to milk. Thus, it seems at least
possible that females during spring could mobilize further – albeit
limited – fat reserves to also sustain their own maintenance costs and
metabolic rate, in addition to the transfer of fat to milk. If this were the
case, it should be reflected by a significantly lower proportion of MEI
allocated to maintenance costs in spring. However, our estimates of energy
budgets (Table 1) indicated
that the amount of energy from MEI used for maintenance remained almost
constant throughout all seasons. Thus, there was no evidence for a sizeable
role of energy reserves in supporting metabolic rate, which also means that
the seasonal time-course of sustained metabolizable energy intake (SusMEI)
most probably mirrored that of SusMR.
The seasonal decline of milk fat content
(Fig. 3) and the extremely low
mass of fat deposits after lactation in autumn
(Fig. 6) indicate that fat
reserves were gradually depleted over the breeding season. Females in autumn
increased energy intake apparently to raise successfully their last litters of
the season. Thus, in the course of the breeding season, females gradually
switched from a `capital breeding' to an `income breeding' strategy of
resource allocation (Drent and Daan,
1980; Jönsson,
1997). Again, the major benefit of the early `capital breeding'
phase might be the reduction of predation risk by avoiding intensive foraging
(Jönsson, 1997). The
compensatory increase of energy intake during the `income breeding' phase in
autumn was not accompanied, however, by an increase in milk volume transferred
to young. One might be tempted to attribute this constancy of milk volume to
the peculiar, once-a-day, nursing bouts in hares, during which young consume
the entire daily milk supply (Broekhuizen
and Maaskamp, 1980). Milk intake of free-living young takes place
during a daily period shorter than 5 min
(Broekhuizen and Maaskamp,
1980; Hackländer et al.,
2002a; Hackländer et al.,
2002b) and can amount to up to 200 g per mother. Conceivably then,
there might be an upper limit to milk intake due to the capacity of the
gastrointestinal tract of juveniles. However, this was certainly not the
limiting factor in the present experiments in which litter size was kept
constant at three leverets because it has been shown that juveniles in smaller
litters, when competition among leverets is lower, have a significantly
(>50%) higher milk intake
(Hackländer et al.,
2002a).
As a result of constant milk volume but declining milk energy content, the
energy intake of litters obtained from milk significantly decreased in summer
and autumn. In our experimental setting (with high caloric food available
ad libitum), this did not result in an actual impairment of the
growth of young during lactation. Juveniles in autumn clearly compensated for
lower milk quality by increasing solid food intake in the last phase of
lactation (week 3–4). In free-living leverets, this compensatory
increase in energy intake would arguably be limited by the quality or quantity
of natural food sources, as well as increased predation risk. Therefore, in
natural populations, litters born late in the season do in fact experience
disadvantages due to impaired milk energy uptake. Vice versa, these
observations support previous views that leverets born early in the year have
a higher reproductive value (Marboutin et
al., 2003). However, while this conclusion was based on the time
of birth only, which might allow early-born young to start reproducing already
in the same year, our present results show that these early litters also
benefit from the higher energy reserves of females and increased total
maternal investments. Together, these data point to important ecological
consequences of the accumulation of body energy reserves in females before the
breeding season. Compared with the wild, where stomach contents of
free-ranging hares have been reported to contain 11 kJg–1
(Hackländer et al.,
2002b), our lab diet with an energy content of 19
kJg–1 certainly enhanced the capability of hares to deposit
fat stores. However, our females were incapable of building up considerable
fat reserves during periods of pregnancy but instead used fat reserves
accumulated during the preceding late-autumn period. Previous studies have
focused largely on the digestibility and energy content of natural diets of
hares during the breeding season alone
(Hackländer et al., 2002b;
Smith et al., 2004;
Reichlin et al., 2006) but
paid little attention to previously accumulated fat reserves. Future
programmes for conservation measures in this species, which has been severely
declining across Europe over the past few decades
(Mitchell-Jones et al., 1999),
should therefore focus more on environmental conditions during the late
autumn/early winter fattening phase of European hares.
Conclusions
Our study demonstrates that SusMR during peak lactation varies within the
breeding season according to the availability of body fat reserves (c.f.
Speakman and Krol, 2005).
Also, our data indicate that SusMR in lactating hares, when energy reserves
are high, is downregulated below physiologically possible levels, which points
to a trade-off between the cost and benefits of maximum energy turnover. We
argue that this view of limitations on energy throughput during lactation as a
variable of reproductive life-history tactics has received too little
attention in the past. Research on SusMR over the past few decades has largely
focused on various physiological constraints that might explain peak energy
throughput (Weiner, 1992;
Hammond and Diamond, 1997;
Bacigalupe and Bozinovic, 2002;
Speakman and Krol, 2005;
Speakman, 2008). This focus
was probably due to a bias towards models utilising very small mammals in
which limitation by physiological capacities seems more likely and has, in
fact, been convincingly demonstrated (e.g.
Krol et al., 2007). However,
it seems that more studies, especially on medium-sized and larger mammals that
are able to build-up fat reserves during gestation or the non-reproductive
period, are needed to see how frequently peak energy turnover during lactation
is dominated by these physiological ceilings, rather than by an active
restriction of reproductive investments.
LIST OF ABBREVIATIONS
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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