Functional
Ecology 2003
17, 496 – 503
Average daily metabolic rate, reproduction and energy
allocation during lactation in the Sundevall Jird Meriones
crassus
Blackwell Publishing Ltd.
M. KAM,*† S. COHEN-GROSS,‡ I. S. KHOKHLOVA,* A. A. DEGEN* and
E. GEFFEN‡
*Desert Animal Adaptations and Husbandry, Wyler Department of Dryland Agriculture, Jacob Blaustein Institute
for Desert Research, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel, and ‡Institute for Nature
Conservation Research, Tel Aviv University, Tel Aviv, 69978, Israel
Summary
1. Non-reproducing Sundevall Jird (Meriones crassus) females (body mass = 84 g;
n = 51), with a mean average daily metabolic rate (ADMR) of 88 kJ day−1, were divided
into three groups: high (H), medium (M) and low (L) ADMR. It was hypothesized that
ADMR is related to reproductive rate and predicted that the H group could support a
higher reproductive rate than the L group. It was also hypothesized that allocation of
energy differs with ADMR level and predicted that the H group would use mainly the
reallocation of metabolizable energy to compensate for an increased energy demand for
reproduction whereas the L group would increase their metabolizable energy intake
markedly. To test the hypotheses, the females were mated and, in those that had litters
(n = 32), changes in body mass and metabolizable energy intake were determined and
milk production was estimated during 15 days of lactation. Litter size, offspring mass
and growth rate were determined for pups.
2. Body mass of dams, litter size and body mass of young at birth were similar among
ADMR groups. However, milk production was 42% higher and litter mass at 15 days
was significantly greater in the H than in L group, supporting our first hypothesis. All
females were in negative energy balance during lactation. Mobilization of body energy
reserves increased with litter size but was similar among ADMR groups. In addition,
the increase in metabolizable energy intake of lactating females above that of nonreproducing females was similar among ADMR groups and therefore the second
hypothesis was rejected.
3. ADMR was reduced by 23% during lactation and milk energy was only 30% of total
metabolizable energy invested in milk production in all females. It is concluded that
lactating M. crassus used a combination of reallocation of energy and increased metabolizable energy intake during lactation. The efficiency of offspring production did not
differ among ADMR groups and therefore a high ADMR has an advantage when food
is abundant, whereas a low ADMR has an advantage when food is sparse.
Key-words: Efficiency of lactation, litter size, milk production, offspring growth rate
Functional Ecology (2003) 17, 496 – 503
Introduction
There are a number of reports that metabolic rate is
positively correlated with reproductive rate in mammals
of similar body mass (McNab 1980, 1987), including
several species of rodents (Glazier 1985). It is theorized
that animals with high metabolic rates can increase
their rates of maternal and foetal tissue biosynthesis
© 2003 British
Ecological Society
†Author to whom correspondence should be addressed.
E-mail: [email protected]
and produce milk at a faster rate than mammals with
low metabolic rates and, consequently, can support a
high reproductive rate.
In eutherian mammals, microtine rodents and lagomorphs have a relatively high metabolic rate and large
population growth constants (r; McNab 1980), cricetines have an intermediate rate of metabolism and
intermediate r, whereas heteromyids and fossorial rodents
have a low metabolic rate and a low r. Henneman
(1983) analysed data on BMR and reproductive rate
of mammals and also concluded that the maximal
496
497
ADMR and energy
allocation for
reproduction
Fig. 1. Energy allocation systems during lactation (crossed bar denotes maintenance
level and empty bars denotes the metabolizable energy invested in milk production).
The metabolizable energy requirements (MER) for lactating females (metabolizable
energy intake minus changes in body energy) are compared with MER of nonreproducing females at maintenance. Lactating females could have the same MER as
non-reproducing females but reallocate energy for milk production by reducing
maintenance energy (a). The lactating female can increase MER during lactation: the
increased amount above maintenance level could be invested wholly in milk production
at no change in maintenance level (c); it could be invested wholly in milk production
with reallocation of MER (b) or only partially invested in milk production due to an
increase in maintenance level (d). See text for explanation.
© 2003 British
Ecological Society,
Functional Ecology,
17, 496–503
intrinsic rate of increase in the population of a species
is positively correlated with its basal metabolic rate.
However, Hayssen (1984) found that the correlation
between the intrinsic rate of increase and BMR was
not statistically significant and argued that ‘there is no
theoretical reason to expect a high correlation between
basal metabolic rate and a population’s maximum rate
of increase.’
That a relationship exists between BMR and reproductive rate in mammals was also rejected by Harvey,
Pagel & Rees (1991) who examined the effects of BMR
on 22 life-history variables when the analyses removed
the effects of body mass. They concluded that ‘there is
no empirical evidence for the claim that basal or active
daily metabolic rates contribute to taxonomic variation
in mammalian or eutherian life histories when bodysize effects are controlled for.’ Also, Hayes, Garland &
Dohm (1992) could not find significant correlations
between basal or maximal metabolic rates and litter
size or litter mass in mice (Mus domesticus).
In these studies, either cross-species regression analysis or comparative analysis by independent contrasts
were used. Therefore, these analyses were based on a mean
metabolic rate and mean reproductive rate per species.
In an intraspecific study on cotton rats (Sigmodon
hispidus; Derting 1989), BMR was related to productive rate and the author concluded ‘that if food energy
is unlimited, increases in BMR are associated with
increased production rate, at least on a short-term
basis. Therefore, the hypothesis that increased rates of
basal metabolism are associated with increased rates of
production cannot be rejected at the individual level.’
We hypothesized that average daily metabolic rate
(ADMR), the metabolizable energy required for
maintenance in the non-reproducing animal (Degen
1997; Degen et al. 1998), affects reproduction in small
mammals. We predicted that mammals with a high
ADMR would have a higher reproductive rate than
mammals with a low ADMR. We also hypothesized
that the ADMR of mammals would affect their allocation of energy during lactation. We predicted that
females with high ADMR would use reallocation of
metabolizable energy intake (MEI) (Fig. 1a) to compensate for an increased demand of energy for lactation
whereas females with low ADMR would increase their
MEI markedly (Fig. 1b– d). To test our hypotheses, we
measured ADMR in female Sundevall Jirds (Meriones
crassus) and examined whether a relationship exists
between ADMR and reproductive parameters and calculated an energy budget of lactating females.
Materials and methods
    
 
Meriones crassus is a widespread gerbillid rodent that
inhabits a variety of desert habitats with annual precipitation of 30 – 100 mm. It is a burrow-dweller that forages
nocturnally and is primarily granivorous (Khokhlova
et al. 1994). Progenitors of our breeding colony were
trapped at the Ramon crater, located at the Negev
desert Highlands (30°35′N, 34°45′E).
ADMR was measured in 51 non-reproducing
females born in our laboratory. Air temperature was
25 ± 1 °C and photoperiod was 12L : 12D, environmental conditions under which Meriones crassus have
been bred successfully. The rodents were maintained in
individual metabolic cages (20 × 10 × 10 cm) with a
wire-meshed floor that allowed for measurement of
food intake and faecal output. During the experimental
period they were offered 100%, 70%, 60% or 50% of
estimated daily requirements (Kam, Khokhlova &
Degen 1997) of millet seeds and Atriplex halimus ad
libitum in separate food cups attached to the side of the
cages. Each individual received all levels of food offered.
Seeds and pieces of plant material that passed through
the mesh were separated manually from the faeces. The
animals were allowed 3 weeks for adjustment, and
then each food level was offered for 7 days and dry matter
and energy digestibilities were measured over 4 days
(Khokhlova, Degen & Kam 1995). Each animal was
weighed daily to 0·01 g prior to receiving food and
change in body mass was determined as a percentage
of the previous day (Kleiber 1975). Between trials, the
rodents were offered ad libitum millet seeds and Atriplex
halimus for 7 days.
MEI was calculated following Kam et al. (1997).
ADMR was determined for each female from the
498
M. Kam et al.
linear regression of body mass change on MEI at the
point of zero body mass change (Degen 1997; Degen
et al. 1998; Robbins 1993).
metabolizable energy invested in milk production, eqn
1 can be modified to:
MER = k1ADMR + k2 MP,

eqn 4
where 0 < k1 < 1 represents a reduction in ADMR, k1
> 1 represents an increase in ADMR during lactation,
and the reciprocal of k2 represents the proportion of milk
energy of the total metabolizable energy invested in milk
production or the efficiency of use of metabolizable
energy for milk energy (Kam & Degen 1993; Degen 1997).
Following ADMR measurements, each female was mated
by placing a male in her cage. They were offered millet
seeds and Atriplex halimus ad libitum, were checked
daily for vaginal plugs to indicate pregnancy and then
were separated from the males. At parturition, each
female and her offspring were weighed. Growth rate of
the offspring was determined using regression analysis.
MEI of lactating M. crassus was measured for 15 days
after birth, during which time milk was the sole energy
source for the young; change in body energy was taken as
10·9 kJ per g change in body mass (Kam & Degen 1993).
The increase in MEI above ADMR was defined
as reproductive effort (Williams 1966). Metabolizable
energy requirements (MER) were calculated as MEI
plus change in body energy content. To test the effect
of age of the young on the reproductive effort of the
female, we divided the 15 days after birth into three
periods (periods one to three) of 5 days each.
Reproductive effort was calculated as MEI minus ADMR
and as a fraction of ADMR (Tuomi, Hakala & Haukioja
1983; Gittleman & Thompson 1988). Since mobilization
of body energy reserves (BE) of the lactating female
contributes to MER, we also calculated reproductive
effort as MER minus ADMR (Kam & Degen 1993).
A measure of efficiency of offspring production (Ep)
was calculated from the overall energy retention of the
offspring (ERp) and litter size (LS) (Glazier 1990) as:
    
Ep =
In the energy budget of a lactating female, energy
available is from MEI and from mobilization of body
energy reserves (BE) and the output comprises total
heat production from maintenance (ADMRl), heat
increment for milk energy production (HIFmp) and
milk energy (MP). ADMRl is the energy expended by
the lactating female for maintenance extrapolated to
zero energy for milk production. MER of the lactating
females can be presented as (all units as kJ day−1):
   

ER p LS
.
MEI1 − ADMR − BE
eqn 5
We also calculated the index of relative energetic growth
(REGR) as the proportion of average changes in the
litter energy retention during lactation of the energy
content of the litter at birth (Glazier 1990) as follows:
REGR =
ER p LS
,
BE0 LS
eqn 6
where BE0 is the energy content of an offspring at birth.
MER = MEI − BE = ADMRl + (MP + HIFmp).
eqn 1
Milk production was estimated from the growth of the
young and its energy requirements for maintenance.
Energy retention of the young (ERp; kJ day−1), based
on its growth rate (∆mb; g day−1) and body mass (mb; g),
and milk intake MIp (kJ day−1) per offspring, were estimated using relationships established on another desert
gerbillid species of similar body size studied under a
similar controlled environment (Kam & Degen 1993) as:
ER p = 2⋅76 ∆ mb mb0 ⋅23
eqn 2
and
MI p = 1096
⋅ ER p + 0⋅426 m 0b⋅73.
© 2003 British
Ecological Society,
Functional Ecology,
17, 496–503
eqn 3
Total milk production was estimated from MIp and litter
size.
Assuming that ADMRl is linearily correlated with
ADMR and that HIFmp is a fraction of the total
 
In the linear regression analysis of ADMR on body
mass in non-reproducing M. crassus females, values
within the 95% confidence limit of the regression line
were considered as intermediate ADMR (M group),
above the 95% confidence limit as high ADMR (H
group) and below the 95% confidence limit as low
ADMR (L group). This classification of ADMR into
three separate groups accommodated non-linear associations, and allowed finer analyses of factor contribution for each ADMR segment. A one-way  was
used to test for the effect of ADMR and lactation on
parameters of reproduction among groups and a
Scheffe post hoc test was used to separate means, which
differed significantly among groups (Statview 5·0,
SAS Institute Inc., Cary, NC, USA, 1998). In comparing
ADMR and parameters of reproduction among groups,
we controlled for the effects of either litter size, litter
mass or body mass of the lactating female using the
residuals of each variable on the affecting parameter
499
ADMR and energy
allocation for
reproduction
(Ricklefs, Konarzewski & Daan 1996). Values are presented as means ± SD and P < 0·05 was chosen as the
minimal acceptable level of significance; differences of
0·05 > P > 0·10 were considered marginal.
Results
 
Before pregnancy, body mass of 51 M. crassus females
averaged 84 ± 15 g, ranging from 55 to 121 g, and
ADMR averaged 88 ± 18 kJ day− 1, ranging from 57 to
138 kJ day− 1 (Fig. 2).
The linear regression of ADMR on body mass (mb;
r2 = 0·59, F1,49 = 71·75, P < 0·001) (ADMR = 12·03 +
0·907mb), was similar to the regression analysis of the
logarithmic transformation of ADMR on body mass
and therefore the former was used for further analyses.
Twenty values were within the 95% confidence limit
(M group), 14 values above the limit (H group) and 17
values below (L group) (Fig. 2). Of the 51 females, 32
produced litters and were used for further analyses.
Mean ADMRs of the H, M and L groups were 109·8
± 16·9 kJ day− 1 (n = 11), 87·6 ± 12·0 kJ day− 1 (n = 9) and
76·4 ± 13·5 kJ day−1 (n = 12), respectively. Body mass
did not differ among ADMR groups and averaged
87·2 ± 14·8 g.
      
Litter size at birth averaged 4·3 ± 1·3 (range = 2 – 6) and
neither differed among ADMR groups nor was correlated with female body mass before pregnancy. Body
mass of the young at birth, 3·6 ± 0·3 g, did not differ
among ADMR groups and was not affected by litter
size. Litter size at 15 days averaged 4·0 ± 1·4, and did
not differ among ADMR groups (Table 1). Differences
© 2003
British
Fig.
2. The
relationship of average daily metabolic rate (ADMR) to body mass in nonreproductive
Meriones crassus females. The linear regression equation describing the
Ecological Society,
relationship
is ADMR = 12·03 + 0·907mb; the solid lines represent the 95% confidence
Functional Ecology,
limit
of the regression line (dotted).
17, 496–503
in litter mass among ADMR groups were found at day
15 of lactation when the H group was heavier than the
L group (Scheffe, P = 0·048).
A negative correlation between body mass (mb) of
the young and litter size (LS) was found at day 10 (r2 =
0·22, F1,30 = 8·54, P = 0·007) and day 15 of lactation
(r2 = 0·27, F1,30 = 10·95, P = 0·002) when the regression equation took the form: mb (g) at 15 days = 18·9–
1·35 LS. Residuals of body mass (mb) of the young on
litter size among the ADMR groups differed significantly at day 5 (F2,29 = 3·305, P = 0·049) and marginally
at day 15 (F2,29 = 2·979, P = 0·066).
   
Growth rate of young was correlated negatively with
litter size during the first (r2 = 0·19, F1,30 = 6·827, P =
0·014), second (r2 = 0·29, F1,30 = 12·192, P = 0·002)
and third (r2 = 0·31, F1,30 = 13·494, P < 0·001) lactation periods, was similar among groups and averaged
0·65 ± 0·22 g day−1 (Table 1). Residuals of growth rate
of the young on litter size among the ADMR groups
were significantly different (F2,29 = 3·951, P = 0·030)
only at the first lactation period.
   
    
During lactation, M. crassus females increased their
MEI above ADMR and lost body energy. MEI during
lactation was positively correlated with ADMR
(r2 = 0·51, F1,30 = 31·615, P < 0·001) but loss in body
energy was not correlated with ADMR. The regression of MEI (kJ day−1) on ADMR (kJ day−1) took the
form: MEI = −20·3 + 1·53 (± 0·27) ADMR.
During 15 days of lactation, MEI was higher in the
H group than in the M and L groups, but change in body
energy did not differ among groups (Table 1). Mean
change was −7·2 ± 5·9 kJ day−1, which was 6·9 ± 7·5%
of MEI. However, change in body energy (BE; kJ day−1)
was affected by litter size (r2 = 0·20, F1,30 = 7·396; P =
0·011) and the linear regression took the form:
BE = 0·5–2·0 (± 0·7) LS.
MEI of lactating females was marginally correlated
with litter size (r 2 = 0·11, F 1,30 = 3·599; P = 0·067).
However, 63% of the variation in litter growth rate
(∆mbl; g day−1) during lactation was explained by MEI
(kJ day−1) and the regression equation (r2 = 0·63, F1,30 =
51·086, P < 0·001) took the form: ∆mbl = 0·01 + 0·019
(± 0·003) MEI.
Metabolizable energy requirements (MER) of the
lactating females differed significantly among groups
(F2,29 = 3·995, P = 0·029); the H group was greater
than the M and L groups (Table 1). Similarly, most
of the differences in litter growth rate (∆mbl: g day−1)
was explained by differences in MER (kJ day−1) and
the regression equation (r2 = 0·67, F1,30 = 62·001, P <
0·001) took the form: ∆mbl = −0·30 + 0·020 (± 0·003)
MER.
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M. Kam et al.
Table 1. Average body mass of M. crassus before pregnancy (Mbp) and during lactation (Mblac), litter size, body mass (mb), litter
mass (mbl) and growth rate of young (∆mb) and of the whole litter (∆mbl), and components of the energy budget during 15 days
of lactation (see text for explanation). Means are ± SD
ADMR group (sample size)
Mbp (g)
Mblac (g)
ADMR (kJ day−1)
MEI (kJ day−1)
(MEI – ADMR) (kJ day−1)
(% ADMR)
BE (kJ day−1)
MER (kJ day−1)
Litter size at birth
Litter size at 15 days
mb-0 (g)
mb-15 (g)
∆ mb (g day−1)
∆ mbl (g day−1)
mbl-0 (g)
mbl-15 (g)
Low (12)
Medium (9)
High (11)
P
93·6 ± 13·4
90·7 ± 11·5
81·4 ± 11·7
113·1 ± 32·2
31·7 ± 23·7
37·4 ± 27·7
−7·01 ± 5·92
120·1 ± 32·8
4·17 ± 1·27
3·75 ± 1·42
3·48 ± 0·27
12·70 ± 3·99
0·60 ± 0·25
1·92 ± 0·66
14·4 ± 3·9
44·3 ± 12·6
88·8 ± 14·6
90·6 ± 10·6
94·5 ± 9·6
112·5 ± 31·8
17·9 ± 30·7
19·3 ± 33·5
−9·01 ± 8·13
121·5 ± 29·0
4·11 ± 1·36
4·00 ± 1·33
3·59 ± 0·44
13·07 ± 3·59
0·62 ± 0·22
2·27 ± 0·70
14·6 ± 4·9
49·8 ± 14·5
92·0 ± 16·0
92·5 ± 13·0
110·5 ± 12·7
147·9 ± 33·8
37·4 ± 24·8
32·7 ± 22·1
−6·06 ± 3·71
153·9 ± 32·3
4·64 ± 1·43
4·18 ± 1·40
3·60 ± 0·22
14·90 ± 2·77
0·73 ± 0·17
2·86 ± 0·90
16·7 ± 5·5
60·5 ± 18·3
0·759
0·922
< 0·001
0·026
0·259
0·331
0·551
0·029
0·621
0·757
0·637
0·300
0·331
0·021
0·459
0·048
ADMR = average daily metabolic rate; MEI = metabolizable energy intake; BE = body energy changes; MER = metabolizable
energy requirements; mb-0 = average body mass per litter at birth; mb-15 = average body mass per litter at 15 days from birth.
The multiple regression analysis of the MER (kJ g−1
day−1) per offspring during lactation on average offspring mass and growth rate was significant (P < 0·01)
in the first (r2 = 0·33, F2,29 = 7·242), second (r2 = 0·75,
F2,29 = 43·959) and third lactation periods (r2 = 0·77,
F2,29 = 48·956).
   
© 2003 British
Ecological Society,
Functional Ecology,
17, 496–503
Reproductive effort (MEI – ADMR) did not correlate
with body mass of the lactating females, was not significantly different among ADMR groups (Table 1)
and was only marginally correlated with ADMR
(r2 = 0·11, F1,30 = 3·759, P = 0·062). Also, when corrected for changes in body energy changes, reproductive effort did not differ among ADMR groups and
averaged 37·0 ± 24·3 kJ day−1. Reproductive effort, as
a proportion of ADMR, was similar among ADMR
groups (Table 1).
The regression of reproductive effort on litter size was
not significant. However, reproductive effort was positively
correlated with litter mass at day 15 (r2 = 0·33, F1,30 =
14·554, P < 0·001) and with litter growth rate (r2 = 0·34,
F1,30 = 15·604, P < 0·001). Residuals of the regression
of litter growth rate on reproductive effort differed
significantly (F2,29 = 6·123, P = 0·006) among ADMR
groups and were higher in the H group than in the L
group (Scheffe, P = 0·008). When reproductive effort was
adjusted for body energy changes, the regression analysis of litter growth rate (GRl) on reproductive
effort (RE) improved (r2 = 0·41, F1,30 = 20·491, P < 0·001)
and took the form: GRl = 1·52(± 0·22) + 0·022 (± 0·005)
RE.
Table 2. Estimated milk energy (MP) during lactation and in
the first (MP1; days 1 – 5), second (MP2; days 6 – 10) and third
(MP3; days 11 – 15) lactation periods in M. crassus. Means
are ± SD
ADMR group (sample size)
MP (kJ day−1)
MP1 (kJ day−1)
MP2 (kJ day−1)
MP3 (kJ day−1)
Low (12)
Medium (9) High (11)
P
16·8 ± 4·9
13·0 ± 4·3
18·7 ± 5·8
19·6 ± 4·9
19·3 ± 5·7
16·2 ± 6·2
21·6 ± 6·8
20·5 ± 5·5
0·028
0·084
0·044
0·045
23·8 ± 7·0
18·2 ± 5·8
26·1 ± 7·7
26·3 ± 8·0
˙
 ,   
  
Estimated milk energy was lowest during the first
lactation period and was similar in the second and
third periods (Table 2) in the three ADMR groups.
Milk energy equalled approximately 15% of MER in
all three ADMR groups. Yet, significant differences
were found in milk production among the ADMR
groups and was approximately 42% higher in the H
group than in the L group.
Milk energy (MP; kJ day−1) increased with litter size
(LS) as follows: MP = 7·6(± 2·8) + 3·10(± 0·66) LS (r2 =
0·42, F1,30 = 22·034, P < 0·001). However, milk energy per
offspring (MPp; kJ day−1) decreased with LS as: MPp =
7·6(± 0·7) − 0·59(± 0·18) LS (r2 = 0·28, F1,30 = 11·403, P <
0·001.) As in growth rate, MP (kJ day−1) was positively
affected by reproductive effort (RE) as: MP = 13·6 (± 1·6)
+ 0·17(± 0·04) RE (r2 = 0·41, F1,30 = 20·945, P < 0·001).
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reproduction
Efficiency of offspring production for the whole
litter (Ep; eqn 5) did not differ among ADMR groups
and averaged 34·8 (± 15·7)%. Relative energetic growth
(REGR; eqn 6) was also similar among groups and
averaged 18·1 (± 6·1)%.
The multiple regression analyses of MER during
lactation on ADMR and milk energy (MP) using zerointercept (to fit the model, eqn 4) was significant
(P < 0·001) for all ADMR groups. However, differences
among groups were not significant. The equation including individuals of all ADMR groups took the form:
MER (kJ day−1) = 0·77(± 0·16) ADMR + 2·96(± 0·76)
MP (r2 = 0·75, F2,29 = 44·612, P < 0·001). ADMRl (taken
as MER at zero milk production) was 23% lower than
ADMR, and, milk energy equalled approximately
30% of the metabolizable energy invested in milk
production.
Discussion
Studies relating reproduction and metabolism have used
basal metabolic rate (McNab 1987; Earle & Lavigne 1990)
and resting metabolic rate without (Stephenson & Racey
1995) and with food offered (Speakman & McQueenie
1996; Antinuchi & Busch 2001) as a measure of metabolic rate. These measures do not include heat increment of feeding, which can contribute up to 70% of
energy expenditure in small mammals (Degen, Kam &
Jurgrau 1988; Robbins 1993). In this study, we used
average daily metabolic rate (ADMR), which we defined
as the energy intake needed to maintain constant
body energy content in the non-reproducing animal.
Although ADMR includes BMR, these two variables
do not correlate (based on phylogenetically independent contrasts and factoring out the influence
of body mass; Degen et al. 1998). ADMR is closer to
field metabolic rate (Degen 1997) and therefore more
relevant than BMR when studying reproduction.
ADMR is also a repeatable measurement; it was
8·23 kJ g−0·54 day−1 in M. crassus in a previous study
(Khokhlova et al. 1995) and 8·12 kJ g−0·54 day−1 in this
study.
       

© 2003 British
Ecological Society,
Functional Ecology,
17, 496–503
Litter size and body mass of the young at birth were
not affected by ADMR. Also, body mass of each
young at birth was not affected by litter size. Although
similar results were found for Peromyscus leucopus in
litter sizes between one and six (Derrickson 1988), this
is usually not the case (Mendl 1988). In a previous
study on Peromyscus leucopus, mass of the young at
birth decreased with an increase in litter size (Millar
1978) and this was also reported in a number of rodent
species, namely, Rattus norvegicus (Leon & Woodside
1983), Mus musculus (König, Riester & Markl 1988),
Peromyscus polionotus (Kaufman & Kaufman 1987)
and Psammomys obesus (Kam & Degen 1994).
  
All lactating females mobilized body energy reserves
and were in negative energy balance. The loss in body
energy was only 7% of MEI, which was similar to the
8% in Common Spiny Mice (Degen et al. 2002) but less
than the 14% in lactating Hispid Cotton Rats (Rogowitz
1998). MEI of the lactating dam increased by only 30%
above ADMR, which is very low compared with other
rodents. The increase in MEI by the lactating females
usually ranges between 65 and 200% (Randolph
et al. 1977; Millar 1978; Gittleman & Thompson 1988;
Poppitt, Speakman & Racey 1994). In small rodents
and other small mammals, it may be higher and can
reach 400% in the House Mouse, Mus musculus (König
& Markl 1987), and even 800% in a small shrew, Sorex
coronatus (Genoud & Vogel 1990).
There are indications that MEI increases with litter
size during lactation in small rodents (Millar 1978;
Kam & Degen 1993; Veloso & Bozinovic 2000). This
was not found in this study, and was also not found in
a study on Acomys cahirinus (Degen et al. 2002). Change
in body energy of the lactating M. crassus was affected
by litter size but not by ADMR. Lactating M. crassus
mobilized more body energy reserves with an increase
in litter size. However, studies in other small rodents
(Weiner 1987; Rogowitz 1998) or insectivores (Mover,
Ar & Helwing 1989) did not find such a relationship.
MEI explained 63% of the variation in growth rate of
the pups but body energy change had little effect in
explaining growth rate of pups. MER, which includes
MEI and body energy mobilization explained 67% of
the variation. This is unlike what was found in the
Common Spiny Mouse, Acomys cahirinus, where either
MEI or changes in body energy each explained about
50% of the variation in growth rate of the pups and
MEI and body energy changes combined (MER)
explained 76% of the variation (Degen et al. 2002).
    
Regression analysis showed that the efficiency of offspring production was related positively to the relative
energetic growth rate of offspring in 11 rodent species
(Glazier 1990). The relatively high efficiency of offspring production and low relative energetic growth rate
in M. crassus, as was also found in Sigmodon hispidus,
placed both species above the 99% confidence interval
of that regression analysis. It was suggested (Randolph
et al. 1977; Glazier 1990) that the high efficiency of offspring production in S. hispidus was due to the low
maintenance costs of the offspring before weaning.
This explanation could apply for altricial M. crassus as
well. Altricial rodents develop slower than precocial
ones, in particular in temperature regulation (Webb &
McClure 1989), and consequently require less energy
in body temperature maintenance and have more
energy for growth (McClure & Randolph 1980; Kam
& Degen 1993).
502
M. Kam et al.
In large litters, demand for milk could be greater
than the dams could produce and in small litters, dams
could possibly produce more milk than sucked. In
lactating M. crassus, milk production did not appear to
reach a maximum level since it increased with litter
size, as was also found for other rodent species (König
et al. 1988; Kam & Degen 1993; Rogowitz 1998). In
this study, metabolizable energy intake of the dam did
not change with litter size but rather with ADMR. We
conclude that limits of food consumption limited milk
production in lactating M. crassus, favouring females
with high ADMR to those with low ADMR.
We hypothesized that ADMR is positively correlated with reproductive parameters. Females with
higher ADMR had higher milk production and heavier
offspring at 15 days than females with lower ADMR,
which supported our hypothesis. We also hypothesized
that the ADMR level would affect energy allocation
(increased demand vs reallocation of energy) during
lactation. This hypothesis was not supported as lactating females of all ADMR levels were in negative energy
balance and were mobilizing similar body energy
reserves and had similar increases in MEI above
ADMR.
Most studies on energy balance during lactation do
not separate energy expenditure for maintenance and
for milk production. Usually, two components of the
energy requirements of the lactating female are considered: total energy expenditure (Kenagy et al. 1990;
Rogowitz 1998) and an estimate of milk energy production. In this study we differentiated between energy
requirements of lactating M. crassus for maintenance
and for milk production and parental care following
the concept of resource partitioning by Kam & Degen
(1993). Such an approach is important in determining
the energy allocation system (Tuomi et al. 1983).
We defined the allocation system used by lactating M. crassus using a two-parameter model (eqn 4).
Lactating M. crassus lowered their maintenance energy
level measured for non-reproducing females by approximately 23% and used this saved energy, in addition to
the increased metabolizable energy intake and mobilization of body energy reserves, for milk production.
A similar reduction of energy expenditure for maintenance during lactation to compensate for increased
energy requirements was suggested in lactating bats
(Kunz 1987). Milk energy was approximately 30% of
the metabolizable energy invested in milk production.
This low efficiency may be due, in part, to the fact that
the metabolizable energy available for milk production in our model included energy costs of maternal
care.
  
© 2003 British
Ecological Society,
Functional Ecology,
17, 496–503
Lactating M. crassus with high ADMR produced more
milk and, as a result, heavier offspring at 15 days than
females with low ADMR. Larger offspring at weaning
may have higher survivorship and fecundity rates than
smaller offspring. However, females with high ADMR
may not always have an advantage in respect to offspring production. In drought years, which commonly
occur in arid zones, constraints on food availability
and quality may limit MEI. Females with low ADMR
could still survive and reproduce whereas females with
high ADMR could not. We propose that in the field a
trade-off exists between energy expenditure and reproductive rate. In a year of abundant food, females with
high ADMR have an advantage by producing more
milk and larger offspring than females with low energy
expenditure; in a year of sparse food, females with low
energy expenditure have an advantage for they can
possibly reproduce when females with high energy
expenditure could not. We predict that the proportion
of females in a population with high or low energy expenditure varies greatly between years and is dependent on
metabolizable energy availability.
Acknowledgements
We thank Abdullah Abou-Rachbah and Natan Mann
for taking care of the animals, Marina Tzvilikhovsky
and Michal Abba for technical assistance and two
anonymous referees for helpful comments. We also
thank Boris Krasnov for use of his facilities (Ramon
Science Center). This research was supported by grant
no. 97–00077 from the United States–Israel Science
Foundation (BSF), Jerusalem, Israel.
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Received 21 November 2002; revised 27 February 2003; accepted
3 March 2003