Oecologia (1999) 121:19±24
Ó Springer-Verlag 1999
Susanne Huber á Eva Millesi á Manfred Walzl
John Dittami á Walter Arnold
Reproductive effort and costs of reproduction
in female European ground squirrels
Received: 22 March 1999 / Accepted: 7 June 1999
Abstract Reproductive e€ort, factors a€ecting reproductive output and costs of reproduction were studied in
primiparous yearling compared to multiparous older
female European ground squirrels (Spermophilus citellus). Yearling females weaned smaller litters than older
ones. Litter size increased with posthibernation body
mass at the expense of slightly lighter young for yearling
but not for older mothers. In older females, on the other
hand, emergence body mass in¯uenced o€spring mass,
whereas litter size was a€ected by oestrus date. High
reproductive e€ort entailed reproductive costs in terms of
reduced subsequent fecundity but not subsequent survival for both yearling and older females. The production
of large litters and long duration of lactation delayed
subsequent oestrus, which, in turn, correlated negatively
with litter size. During the second half of lactation, oestradiol levels were signi®cantly elevated, indicating the
initiation of follicular maturation processes. Oestradiol
levels during that time correlated negatively with current,
but positively with subsequent litter size. We therefore
assume that inhibitory e€ects of lactation on gonadal
development may mediate the negative relationship between reproductive e€ort and subsequent reproductive
timing in adults. This e€ect is absent in yearlings because
they are reproducing for the ®rst time. Reproductive
output in yearlings was in¯uenced by interactions between structural growth and puberty.
Key words Ground squirrel á Female á Reproduction á
Lactation á Gonad development
S. Huber (&)
Research Institute of Wildlife Ecology,
University of Veterinary Medicine of Vienna,
Savoyenstrasse 1,
A-1160 Wien, Austria
e-mail: [email protected]
E. Millesi á M. Walzl á J. Dittami
Institute of Zoology,
University of Vienna,
Althanstrasse 14,
A-1090 Wien, Austria
Introduction
Life history theory predicts a ``trade-o€'' between current reproductive e€ort and subsequent reproduction
and/or survival. This trade-o€ has been termed the costof-reproduction hypothesis (Lack 1966; Williams 1966;
Stearns 1976; Bell 1980; Partridge and Harvey 1985).
Costs of reproduction are separated into survival costs,
where current reproduction decreases an individual's
probability of future survival, and fecundity costs, where
current reproductive e€ort a€ects future reproductive
capacity (Reznick 1992). The mechanisms by which reproductive e€ort is carried over into subsequent reproductive output, however, often remain unclear.
Although most studies in this ®eld have been conducted
in birds, recently reproductive costs have also been analysed in mammals (Mappes et al. 1995; Koskela 1998;
Koskela et al. 1998).
In European ground squirrels (Spermophilus citellus),
reproduction is constrained by hibernation, limiting
both the timing of mating and gonadal development.
Females produce one litter per year and mate within a
few days after emergence from hibernation in order to
maximise the time available for their o€spring to grow
and fatten prior to hibernation (Millesi et al. 1999a).
Gonadal development is limited by hibernation as
maturation processes are suppressed during hypothermia (Barnes et al. 1986). Follicular maturation, however, is known to be a long-term process (reviewed in
Greenwald and Roy 1994). This leads to the assumption
that in European ground squirrels, follicular development may be initiated during summer prior to the hibernation period. As a consequence, interactions with
other activities in one season would a€ect these maturation processes and reproductive output in the next
season. Lactation, for example, is known to depress
luteinising hormone (LH) secretion, thereby suppressing
the LH-dependent processes of gonadal development
(reviewed in Mc Neilly 1994). Hence, physiological
constraints limiting maturation processes possibly me-
20
diate costs of reproduction. Female European ground
squirrels usually breed as yearlings (Millesi et al. 1999a),
but ®rst breeders often produce smaller litters than older
ones (e.g. Festa-Bianchet and King 1991; Dobson and
Michener 1995). While yearlings breed for the ®rst time,
older females have already reproduced during the previous year. Consequently, functional aspects of reproductive decisions may di€er between primiparous
yearling and multiparous older individuals.
Our study was aimed (1) at examining reproductive
e€ort ± measured in terms of litter size, weanling mass
and the duration of lactation ± and factors a€ecting
reproductive output in primiparous yearling compared
to multiparous older females and (2) at investigating
costs of reproductive e€ort in terms of reduced survival
and/or fecundity in both age groups.
Materials and methods
The study was carried out in a recreation park near Vienna in 1996
and 1997 and was based on long-term research in this population
(Millesi et al. 1998, 1999a, b). According to Millesi et al. (1999a),
almost all females of the focal population reproduced (94%)
without di€erences between age classes. Consequently, all older
females were multiparous. We monitored the focal population by
daily scans supplemented with all additional sightings not recorded
during scans (Millesi et al. 1999a). We trapped the animals in
Tomahawk live traps baited with peanut butter. Each female (1996:
n = 29; 1997: n = 25) was repeatedly trapped in 3- to 5-day-intervals for 3 weeks after emergence from hibernation in April to
determine oestrus date, and at 2- to 4-week intervals thereafter until
the beginning of hibernation in August with a focus on reproductive phases (gestation, ®rst and second half of lactation, postlactation) and on critical events like parturition, weaning and onset of
prehibernatory fattening. Unfortunately, we did not succeed capturing all individual females at each stage. Therefore, sample sizes
vary for the di€erent parameters.
After ®rst capture, we subcutaneously implanted in the squirrels
a transponder chip (PIT tag, Indexel) for permanent identi®cation.
For distant recognition, the animals were marked with a commercial hair dye in individually recognisable patterns. Body mass
was measured with a laboratory scale, and scull size (maximal
length of scull) was determined by a vernier calliper. We de®ned
spring emergence body mass as the body mass measured within
5 days after emergence from hibernation. Reproductive state was
determined by assessing teat development, milk excretion, and
rapid body mass changes as indicators of littering (Millesi et al.
1999a).
At capture, a 100-ll blood sample was taken from the femural
vein for oestrogen analysis with a minimum interval of 2 weeks
between two successive blood collections. As follicular maturation
is accompanied by elevated oestrogen secretion (Ojeda 1996), oestrogen levels can indicate follicular maturation processes. The
blood samples were centrifugated in the ®eld. Plasma was then
taken into the laboratory and stored at )20°C. Oestradiol levels
were analysed after diethyl ether extraction with a biotin-streptavidin enzyme immunoassay according to Palme and MoÈstl
(1993). Intra- and interassay variation were less than 10%.
We avoided any adverse e€ects on the animals by our procedures. Animals were taken out of the traps immediately after
capture and put into a black bag, where they were always calm. To
avoid stressing the squirrels, we took only the manipulated parts of
the body out of the bag. Together with determination of body mass
and reproductive state, all manipulation procedures lasted less than
5 min. The animals were released immediately afterwards at the
trapping location and resumed their former behaviour either at
once, or after they have hidden in a burrow for a few minutes. We
examined the e€ects of repeated trapping and the manipulations on
body mass, behaviour and reproductive output to rule out capturing e€ects on the results. By comparing these parameters in focal
individuals and females that had been captured rarely without
further manipulations, we did not ®nd any di€erences between the
two groups.
The animals were categorised into three age classes: juvenile
(prior to ®rst hibernation), yearling (after ®rst hibernation) and
older females (at least 2 years old). This was possible since we
know the year of birth of most of the focal individuals. For a few
females for which we did not know the exact year of birth, we
categorised yearling and older females according to scull length, as
yearlings have signi®cantly smaller sculls than older females
(Millesi et al. 1999b). Survival of individual females to the next
breeding season was determined at emergence from hibernation.
We could, however, not di€erentiate between mortality and dispersal in each case, although in many cases we observed kills by
domestic cats.
We determined time of vaginal oestrous from vaginal smears
collected during the ®rst 3 weeks after emergence from hibernation,
following Holmes and Landau (1986). Smears were stained using
the Papanicolaou stain protocol and cytology was classi®ed under a
Polyvar microscope by the ratios and numbers of nucleated epithelial cells, corni®ed cells and leucocytes. Lactation was de®ned as
the period from parturition until the onset of teat regression (when
teats are still large but limp and dried out). Estimates of the end of
lactation were supported by observations of burrow use. Females
stopped using litter burrows after weaning of young.
Litter size was determined when juveniles emerged from natal
burrows for the ®rst time, which never coincided with weaning. As
individual burrows were only used by a single female, litter size was
de®ned as the number of juveniles emerging from a female's burrow. Litter mass was calculated as litter size times mean juvenile
emergence body mass. X-ray analyses on intrauterine litter size
showed that the number of emerging o€spring is determined prenatally and that di€erential postnatal mortality is unlikely to explain litter size variation (Millesi et al. 1999a). We therefore used
emergence litter size as a measure of fecundity.
Statistical analysis was conducted using the SPSS 7.5 for Windows statistical package. In 1996, the onset of reproduction was
delayed due to 10 days of heavy snowfall. To provide comparability of data, we corrected for this delay. If assumptions were met,
we applied parametric tests. For some analyses this was the case
only after square root transformation of the original data. We used
individual means when repeated measurements were available in a
particular phase. Linear regressions and ANCOVA for regression
were used to compare reproductive e€ort and fertility costs between
yearling and older females. Logistic regression was performed to
test survival costs of reproduction. Signi®cance values were obtained from two-tailed statistics. Means are presented ‹1SD.
Results
Reproductive output
Yearling females weaned signi®cantly smaller litters
(5.36 ‹ 1.86 young, range 3±8, n = 14) than older
mothers (6.8 ‹ 1.72 young, range 3±10, n = 26; t-test
for independent samples: t38 = )2.47, P = 0.018).
Mean oestrus date was later in yearling (April 12 ‹ 1.8,
n = 14) than older females (April 7 ‹ 4.7, n = 26;
t-test for independent samples: t38 = 3.474, P = 0.001).
Body mass at emergence from hibernation also di€ered
signi®cantly between yearling (175.1 ‹ 27.42 g,
n = 12) and older females (199.5 ‹ 20.19 g, n = 18;
t-test for independent samples: t28 = )2.813, P =
0.009).
21
In yearling females, emergence body mass correlated
positively with litter size (Fig. 1), suggesting a bodymass-dependent adjustment of reproductive output. In
older females, however, this association was not found
(Fig. 1). An opposite picture emerged from analysing
the relation between litter size and oestrus date. While
litter size decreased with progressing oestrus date in
older females (Fig. 2), this e€ect seemed to be absent in
yearlings (Fig. 2), though the regression slopes did not
di€er signi®cantly.
Yearling and older mothers allocated reproductive
e€ort di€erently into number and weight of o€spring.
Heavier yearling mothers invested in additional but
lighter young (cf. Fig. 1 and Fig. 3). In contrast, heavier
older females did not invest in more, but in heavier
young (cf. Fig. 1 and Fig. 3). Accordingly, female
posthibernation body mass showed a signi®cant positive
correlation with mean o€spring body mass at natal
emergence after correction for litter size for older but
not for yearling females (partial correlation coecient:
mean juvenile body mass at natal emergence versus female emergence body mass, corrected for litter size:
older females, r = 0.5323, n = 15, P = 0.05; yearling
females, r = 0.3845, n = 7, P = 0.452).
Fig. 1 Litter size versus body mass at emergence from hibernation (g)
in older females (closed circles), and yearling females (open squares).
Regression lines: older females, y = 7.842 ) 0.0056x, R2 = 0.004,
t19 = )0.286, P = 0.78; yearling females: y = )2.671 + 0.0474x,
R2 = 0.584, t8 = 3.351, P = 0.01. Slopes of regression lines are
signi®cantly di€erent between yearling and older females (ANCOVA:
t27 = 2.083, P = 0.047)
Fig. 3 Mean individual body mass in litters at natal emergence (g)
versus female body mass at emergence from hibernation (g) for older
females (closed circles), and yearling females (open squares). Regression lines: older females, y = )34.833 + 0.491x, R2 = 0.301, t13 =
2.364, P = 0.034; yearling females, y = 121.63 ) 0.295x, R2 = 0.30,
t5 = )1.491, P = 0.196. Slopes of regression lines are signi®cantly
di€erent between yearling and older females (ANCOVA: t18 = 2.793,
P = 0.012)
Fig. 2 Litter size versus oestrus date in older females (closed circles),
and yearling females (open squares). Regression lines: older females,
y = 24.602 ) 0.17x, R2 = 0.187, t24 = )2.352, P = 0.027; yearling
females: y = 9.43 ) 0.04x, R2 = 0.002, t12 = )0.169, P = 0.87.
Slopes of regression lines are not signi®cantly di€erent between
yearling and older females (ANCOVA: t36 = 0.817, P = 0.419)
Fig. 4 Oestrus date in 1997 versus litter size in 1996 in older (closed
circles) and yearling (open squares) females. Regression lines: older
females, y = 90.35 + 2.77x, R2 = 0.598, t5 = 2.729, P = 0.041;
yearling females, y = 99.9 + 0.779x, R2 = 0.599, t5 = 2.731, P =
0.041. Slopes of regression lines show a tendency to be di€erent
between yearling and older females (ANCOVA: t10 = 2.082,
P = 0.064)
22
Costs of reproduction
Producing large litters delayed oestrus in the following
year in both yearling and older females (Fig. 4). A
similar relationship was found between litter mass and
subsequent oestrus date (linear regression: R2 = 0.557,
t7 = 2.969, P = 0.021). We pooled yearling and older
females for this and the following analyses because age
classes did not di€er signi®cantly in either case. Duration of lactation in one season a€ected oestrus delay in
the next. Females nursed large litters signi®cantly longer
than smaller ones (Pearson correlation: r = 0.798,
n = 22, P < 0.001). Long-lactating females, in turn,
reproduced later in the subsequent season, i.e. weaning
date was positively correlated with the following oestrus
date (Fig. 5). Lactation duration correlated positively
with subsequent oestrus date as well (Pearson correlation: r = 0.605, n = 14, P = 0.022).
During the second half of lactation, mean oestradiol
levels were signi®cantly elevated (Fig. 6). Females that
nursed smaller litters had higher oestrogen levels during
that time than did mothers lactating larger litters
(Fig. 7a). On the other hand, subsequent litter size correlated positively with oestrogen levels during the second
half of lactation. Females with high oestrogen titres produced larger litters the following year (Fig. 7b).
We did not ®nd any e€ect of reproductive e€ort on
survival. A mother's probability of surviving to the
subsequent breeding period was neither signi®cantly
in¯uenced by litter size (logistic regression: b = )0.078,
SE = 0.177, n = 40, P = 0.66) nor by mean young
emergence body mass (logistic regression: b = 0.0045,
SE = 0.023, n = 26, P = 0.84), litter mass (logistic
regression: b = 0.0008, SE = 0.0052, n = 30, P =
0.88) or lactation duration (logistic regression: b =
)0.0009, SE = 0.1404, n = 22, P = 0.99). As age
classes did not di€er signi®cantly, they were not separated for analysis.
Discussion
Although yearling female European ground squirrels
reproduced at a similar rate as older females, reproductive performance di€ered markedly between the two
age groups. Yearling females not only produced smaller
litters compared to older ones, their litter size correlated
Fig. 5 Oestrus date in 1997 versus weaning date in 1996 in older
with
posthibernation body mass whereas it did not in
females (closed circles), and yearling females (open squares). Regression line (yearling plus older females): y = 50.66 + 0.248x, R2 = older mothers. Presumably as a result of this correlation,
0.888, t6 = 6.907, P < 0.001
yearling posthibernation body mass had a slightly negative e€ect on neonate mass. Hence, heavy yearlings
invested in additional o€spring at the expense of slightly
Fig. 6 Oestradiol titres (ng/ml) during gestation (G), ®rst half of
lactation (L1, de®ned as the period from the ®rst to the medium day
of lactation in each individual), second half of lactation (L2, de®ned as
the period from the medium to the last day of lactation in each
individual), and postlactation (PL). Means + 1 SD are shown. Phase
di€erences (data were square root transformed for analysis to correct
for non-normality): ANOVA, F3,64 = 2.542, P = 0.064; post-hoc
comparisons (LSD), L2±G: P = 0.032, L2±L1: P = 0.044, L2±PL:
P = 0.011; all others: P > 0.5. Sample sizes: G = 11, L1 = 20,
L2 = 12, PL = 25
Fig. 7 a Oestradiol titres during the second half of lactation in 1996
(ng/ml) versus litter size in 1996 in older (closed circles) and yearling
(open squares) females. Regression line (yearling plus older females):
y = 0.113 ) 0.011x, R2 = 0.242, t11 = )1.873, P = 0.088. b Litter
size in 1997 versus oestradiol titres during the second half of lactation
in 1996 (ng/ml) in older (closed circles) and yearling (open squares)
females. Regression line (yearling plus older females): y = )0.03 +
0.0156x, R2 = 0.476, t6 = 2.337, P = 0.058
23
smaller young. The relationship between body mass and
litter size in yearling females may be due to the fact that
yearlings enter hibernation as juveniles before reaching
maturity. So before breeding they have to pass through
puberty which is known to in¯uence and be in¯uenced
by structural growth (reviewed in Foster 1994): additional development or improved nutrition are translated
to the gonadotropin-releasing hormone-pulse generator
to increase its activity. The resultant increase in LH
pulse frequency drives the pubertal processes by developing follicles (reviewed in Foster 1994). Puberty also
seems to be the main reason for the later mean oestrus
date in yearling compared to older females.
In older females, litter size did not vary with body
mass but with oestrus date. This negative relation between litter size and oestrus date possibly represents
carryover e€ects from previous parental e€ort to subsequent reproduction. We suggest that physiological
e€ects of previous lactation in¯uenced subsequent oestrus date by a€ecting follicular maturation processes (see
below). This is supported by the fact that, in contrast to
yearlings, older females with high posthibernation body
mass produced heavier instead of additional young.
Reproductive output di€ers between yearling and
older females in a number of ground squirrel species
(e.g. Armitage and Downhower 1974; Sherman and
Morton 1984; Festa-Bianchet and King 1991; Dobson
and Michener 1995). In Richardson's ground squirrels,
a similar pattern as seen in our study has been described: litter size and maternal body mass correlated
among yearlings, but not among older females, while
litter size decreased signi®cantly as the breeding season
progressed in older, though not yearling females.
Moreover, in yearling females, body mass in¯uenced
litter size, while in older females, body mass a€ected
neonate mass (Michener 1989; Dobson and Michener
1995). Dobson and Michener (1995) also showed that in
yearling females, di€erences in body mass primarily re¯ected di€erences in structural size, whereas body mass
of older females was strongly associated with condition,
i.e. fat reserves. If a similar principle applies to the
European ground squirrel ± which remains to be examined ± this would support our suggestions that
structural growth in yearling females a€ected reproductive output through an e€ect on litter size, while
body condition in older ones had a minor e€ect on litter
size but was re¯ected in o€spring mass. O€spring body
mass, in turn, may a€ect juvenile survival to the following spring (e.g. Murie and Boag 1984; Michener and
Locklear 1990) and/or subsequent juvenile reproductive
success (e.g. Michener 1989; King et al. 1991; Rieger
1996). In our study, o€spring mass had no e€ect on
juvenile survival but in¯uenced juvenile reproductive
output in the following season (S. Huber, I.E. Ho€mann, E. Millesi, J. Dittami, W. Arnold, unpublished
work). Thus, yearling females ± allocating surplus resources to the production of additional but lighter
young ± had ®tness costs in terms of reduced o€spring
fecundity, while older females ± allocating surplus re-
sources to the production of heavier young ± had ®tness
bene®ts in terms of increased reproductive output of
their o€spring.
Both yearling and older females weaning large litters
had reproductive costs in terms of reduced subsequent
fecundity. The subsequent oestrus of females producing
large and heavy litters was delayed. Subsequent oestrus
date, in turn, was negatively correlated with litter size in
multiparous females. Direct e€ects of current reproductive output on future litter size were less evident in
our study. During a former study on the same population (J. Dittami, E. Millesi, S. Huber, E. MoÈstl,
M. Walzl, unpublished data), however, a signi®cant inverse relationship between sequential litter sizes was
found. Hence, following Trivers (1972), high parental
investment in terms of long-lactating large litters reduced the residual reproductive value, representing a
``trade-o€'' between current and subsequent reproduction. On the other hand, females did not pay reproductive costs in terms of reduced survival. Females
weaning large or heavy litters were as likely to survive to
the subsequent mating period as mothers of smaller litters and young. Correspondingly, in Richardson's and
Columbian ground squirrels, large litters did not impose
higher survival costs on the mother than smaller ones
(Murie and Dobson 1987; Michener and Locklear 1990;
Risch et al. 1995). In contrast to our ®ndings, however,
ground squirrel studies to date have not described fecundity costs, as no e€ects of successful reproduction on
future reproductive performance were found (Michener
and Locklear 1990; Hare and Murie 1992; Risch et al.
1995). In other small mammals like the bank vole
(Clethrionomys glareolus) also, high reproductive e€ort
caused by litter size manipulation had no e€ect on future
maternal survival or reproduction (Mappes et al. 1995;
Koskela 1998).
The relationship between reproductive e€ort and
timing of subsequent oestrus in our study may be mediated by the reproductive physiology of these animals.
Large litters were nursed longer than smaller ones, and
lactation in one season a€ected oestrus delay in the next.
Both late weaning date and long duration of lactation
postponed oestrus date in the subsequent season. During
late lactation, oestradiol levels were signi®cantly elevated, indicating initiation of follicular maturation processes during that time. Preliminary histological data
support this suggestion, as Graa®an follicles were present
in late summer ovaries (J. Dittami, E. Millesi, S. Huber,
E. MoÈstl, M. Walzl, unpublished data). In addition, high
oestradiol levels during the second half of lactation were
negatively related to current, but positively related to
subsequent litter size. We assume that follicular development may be impaired due to a higher investment in
large litters by long (and probably more intense) lactation, which would lead to an oestrus delay in the following mating period. Follicular development is a longterm process characterised by changes in follicle size and
morphology as well as by ¯uctuations in sex hormone
levels (reviewed in Greenwald and Roy 1994). Interac-
24
tions between follicular maturation and other activities
can have profound e€ects on developmental processes.
LH secretion, for example, is highly depressed during
lactation, suppressing the LH-dependent processes of
follicular development (reviewed in Mc Neilly 1994).
This LH de®ciency decreases steroid production by the
follicle (reviewed in Greenwald and Roy 1994). In animals kept in the laboratory, suppression of follicular
maturation during lactation has been clearly demonstrated. Moreover, the di€erences in suckling stimulus
between small and large litters in¯uenced the degree of
follicular inhibition in the rat. This inhibition was also
re¯ected in low levels of oestrogen (reviewed in Mc Neilly
1994). Thus, it seems reasonable to assume that in European ground squirrels, follicular maturation is impaired by long and intense lactation, resulting in low
oestrogen levels and a delay in subsequent reproduction.
Acknowledgments This work was supported by the Austrian National Bank (JubilaÈumsfonds 6264). We thank I.E. Ho€mann and
S. Hanslick for their help in collecting ®eld data as well as the
referees for their helpful comments on the manuscript. We declare
that the experiments comply with the current laws of Austria.
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