Journal of Animal
Ecology 2003
72, 212– 219
Senescence and age-related reproduction of female
Columbian ground squirrels
Blackwell Science, Ltd
D. R. BROUSSARD*, T. S. RISCH*‡, F. S. DOBSON* and J. O. MURIE†
*Department of Biological Sciences, 331 Funchess Hall, Auburn University, Auburn, AL 36849–5414, USA; and
†Department of Biological Sciences, University of Alberta, Edmonton, Alberta, T6G 2E9, Canada
Summary
1. Three hypotheses have been proposed to explain age-structured patterns of reproductive investment and somatic investment: residual reproductive value, senescence and
evolutionary restraint. We evaluated these hypotheses for female Columbian ground
squirrels (Spermophilus columbianus) by examining age-related patterns of somatic and
reproductive investment. Females were designated as successful (those that weaned
litters) and unsuccessful (those that did not wean litters).
2. Somatic investment varied among both successful and unsuccessful females of
different ages, with yearlings having the highest investment. Considering all females,
reproductive investment varied among age classes with yearlings and the oldest (6–9year-olds) having the lowest investments. However, when only successful females were
considered, reproductive investment was lowest in the yearlings and not significantly
different among older females.
3. The highest proportion of successful females occurred in the middle adult age classes,
while yearlings and the oldest females displayed the lowest proportion of successful
females. During the breeding season, somatic investments of successful and unsuccessful
females differed significantly only in the yearling age class, with unsuccessful females
having the highest investment.
4. Evolutionary restraint or constraint explained patterns of reproduction in the yearling
age class, where both reproductive investment and proportion of reproductive females
were low. There was evidence for senescence of reproduction by some of the oldest females.
Key-words: constraint, restraint, reproductive investment, senescence, somatic investment, Spermophilus columbianus.
Journal of Animal Ecology (2003) 72, 212–219
Introduction
Allocation of resources to reproduction (reproductive
investment) and growth and maintenance (somatic
investment) is an important aspect in an organism’s life
history (Stearns 1976, 1992; Morris 1987; Roff 1992).
Trade-offs occur between these aspects of life histories
because individuals cannot allocate simultaneously
maximal amounts of resources to both producing offspring and to growth and maintenance. Furthermore,
as females age, investment of resources to survival and
maintenance vs. reproduction may change, based
on the expectation of future offspring (Pianka 1988).
© 2003 British
Ecological Society
Correspondence: David Broussard, 331 Funchess Hall, Department of Biological Sciences, Auburn University, Auburn, AL
36849-5414, USA. Tel. (334) 844 9252; Fax: (334) 844 9234;
E-mail: [email protected]
‡Present address: Department of Biological Sciences, Arkansas
State University, State University, AR 72467, USA.
Reproductive output of most birds and mammals
usually increases, and then declines or remains constant over their lifetime (Clutton-Brock 1984, 1988;
Derocher & Stirling 1994; Pärt 1995). Three hypotheses have been proposed to explain these patterns
of lifetime reproduction. They include the residual
reproductive value hypothesis, evolutionary restraint
hypothesis and the senescence hypothesis.
The residual reproductive value hypothesis (Pianka
& Parker 1975) suggests that as females age, reproductive investment in current offspring should increase
as residual reproductive value decreases. Residual
reproductive value is the age-specific expectation of
all future offspring beyond those presently at stake
(Williams 1966). Because survivorship is assumed to
decrease with age, each offspring should become
more valuable to females as they age. Assuming that
individuals have a fixed energy budget throughout
life, an individual with a high probability of future
213
Age-related
reproduction in
ground squirrels
reproductive success should be less likely to invest
highly in current reproduction at a cost to somatic
investment than an organism with a lower probability
of future reproductive success. Therefore, older individuals should display high reproductive investment
compared to younger individuals, and a concomitant
decrease in somatic investment (Pianka 1988).
The evolutionary restraint hypothesis suggests that
the youngest females restrain their reproductive investment to avoid a possible cost to future reproduction
and/or survival (Curio 1983; Marchetti & Price 1989;
Rohwer 1992; Blums et al. 1996). According to this
hypothesis, primiparous females should allocate more
resources to somatic needs and less to reproduction
compared to older females, to avoid this possible cost.
Therefore, primaparous females should have lower
reproductive investments and higher somatic investments compared to older females.
The senescence hypothesis (Williams 1957; Partridge
2001) addresses biological processes underlying the
marked decline in age-specific fitness components,
such as fertility, as an organism ages. Individuals are
senescing if they exhibit a generalized deterioration
of many physiological functions, including declining
reproduction and annual survival. Senescence is based
on an evolutionary trade-off between traits that enhance
reproduction early in life and declining condition of
an organism later in life (Kirkwood & Rose 1984; Rose
1984). Senescence predicts that older individuals will
show an age-specific decline in reproductive investment
and somatic investment and an increase in age-specific
mortality.
The purpose of our study was to evaluate the
residual reproductive value hypothesis, the evolutionary
restraint hypothesis, and the senescence hypothesis with an
extensive data set on a large population of known-aged
Columbian ground squirrels (Spermophilus columbianus,
Ord). We evaluated these hypotheses using litter mass
as a reflection of reproductive investment and change
in female mass from emergence from hibernation to
litter emergence as a reflection of somatic investment
during the breeding season (see Millar 1977; Tuomi
1980; Ebenhard 1990). Thus, we measured reproductive
and somatic investments during the same time period
in a hibernating species with a short active season
(Dobson 1988). The three hypotheses are not mutually
exclusive, but they differ in the age-specific predictions.
We applied these predictions to young, middle-aged
and older female Columbian ground squirrels. Our
goal was to find evidence for the most likely of the
hypotheses, and the most parsimonious explanation of
age-structured reproductive and somatic investments.
Materials and methods
© 2003 British
Ecological Society,
Journal of Animal
Ecology, 72,
212–219
 
Columbian ground squirrels are hibernating, semifossorial rodents whose reproductive ecology and life
history have been well studied. They provide an excellent
model for evaluating hypotheses about life-history
evolution because much is known about their population biology (e.g. Boag & Murie 1981; Zammuto &
Millar 1985a,b). Population size is regulated by food
resources (Dobson & Kjelgaard 1985a; Dobson 1995;
Dobson & Oli 2001) and life histories are extremely
plastic and influenced by individual body condition
(Dobson & Kjelgaard 1985b; Dobson & Murie 1987;
Dobson 1988; King, Festa-Bianchet & Hatfield 1991;
Dobson 1992; Neuhaus 2000). Adult ground squirrels
emerge from their hibernation burrows in spring and
mate. Once the young are weaned in early summer, the
adult females must then prepare for an 8-month period
of hibernation, which begins in late summer (Murie &
Harris 1982). Therefore, Columbian ground squirrels
have a short amount of time in which they must allocate resources to both reproductive and somatic needs
(Dobson, Badry & Geddes 1992). Due to the long
hibernation season and short active season, trade-offs
between reproduction, survival and daily metabolic
maintenance should be pronounced. Additionally,
Columbian ground squirrels are long-lived for rodents,
and senescence is most evident in long-lived mammalian species (Kirkwood & Rose 1984).
 
Field studies were conducted from 1983 to 1990 at the
Turnbull National Wildlife Refuge, 35 km south-west
of Spokane, Washington, USA (47°26′ N, 117°36′ W,
elevation 695 m). The 9-ha study site contains a large
meadow surrounded by an open woodland of Ponderosa pine (Pinus ponderosa) and rocky outcrops. A large
wetland bounded the site on the south, and was an unsuitable habitat for ground squirrels. Ground squirrels
were trapped within a day after emergence from hibernation in early to mid-March Captured individuals were
weighed to the nearest 5 g, examined for reproductive
condition and marked uniquely with numbered metal
ear tags and dye markings on their pelage. New ear tags
and dye markings were reapplied as needed on recapture.
Juvenile ground squirrels were captured within 1–
2 days after emergence from natal burrows (in early
to late May). Emergence date could be anticipated
because date of breeding was known or could be estimated within a few days. Mating dates were determined
by observing above-ground copulations, or if mating
was not observed, from the external appearance of
the female’s genitalia, behavioural evidence of underground copulation (including oral cleaning of the groin
area by both sexes), detection of a copulatory plug or
the presence of sperm in vaginal smears. Dates of litter
emergence were estimated by adding 51 days to the
estimated or observed mating date: 24 days from
mating to parturition and 27 days from parturition
to first emergence of the litter (Shaw 1925; Murie &
Harris 1982; Murie 1992). The site of emergence was
anticipated for most litters. Natal burrows could be
214
D. R. Broussard
et al.
© 2003 British
Ecological Society,
Journal of Animal
Ecology, 72,
212–219
identified from observations of females stocking them
with nesting material before young were born, or by
observing females emerge from or enter them during
the lactation period.
During the period of litter emergence, the study site,
especially the locations of natal burrows, were checked
one to three times daily for newly emerged juveniles.
Juveniles were captured in wire-mesh traps that were
placed over natal burrows, or in live traps that surrounded the burrows. Most juveniles were captured,
weighed to the nearest 5 g and marked within the first
3 days of emergence. The lactating female that associated with a natal burrow was assumed to be the mother
of the litter that emerged from that burrow. Female
Columbian ground squirrels are highly philopatric and
settle as adults near the burrows in which they were
born (Murie & Harris 1984). Therefore, female age was
known from date of birth for most females in our data
set (161 of 229). However, females during the first year
of the study were of unknown age. These females, along
with a few rare females that dispersed into the study
site, were assigned a minimum known age of 2 years
(68 of 229). Exclusion of these females changed none of
the age-structured patterns of reproductive investment
and somatic investment and, hence, changed none of
our interpretations of these patterns. Therefore, these
females were included to accumulate a substantial
sample of the oldest females, for examination of the
proportion of successful individuals in each age group
(see Results). As the age assigned to these females is
the minimum possible, their inclusion in the oldest age
groups is a conservative treatment of the data.
Data on reproductive investment and somatic investment were collected each time a female weaned a litter.
We obtained two measures of investment.
1. Reproductive investment: total litter mass at first
emergence from the natal nest.
2. Somatic investment: change in a female’s mass
between her emergence from hibernation and emergence of her litter.
Total litter mass was calculated as the sum of juvenile mass in each litter near the time of weaning.
Because lactation had virtually subsided at this time,
the majority of direct energetic investment into the offspring was considered complete (Mattingly & McClure
1982; Kenagy, Sharbaugh & Nagy 1989; Michener
1989). We assumed that litter mass at weaning is an
accurate reflection of maternal energy investment, in
part because litter size at weaning was not significantly
different from litter size at conception or birth in
Columbian ground squirrels (Murie, Boag & Kivett
1980). Because this is a wild population of ground
squirrels where rearing of juveniles takes place belowground, we were unable to assess reproductive investment for those females that lost litters during lactation.
Females were designated as successful (those that
weaned litters) and unsuccessful (those that did not
wean litters). Unsuccessful females include those
females known to have mated but did not lactate, those
that mated, subsequently lactated, but lost their litter
some time during lactation, and those that did not
mate. For unsuccessful females, somatic investment
was measured as the mass gained from her emergence
from hibernation to 51 days after mating, the time at
which her litter would have emerged. Some litters were
killed by badgers (Taxidea taxus) and other litters may
have suffered partial predation by badgers during
lactation (Murie 1992). These litters were eliminated
from data analyses (60 litters).
All analyses were performed using SAS (1990)
statistical software. Analyses of variance (GLM procedure) were performed to test for the effect of age on
reproductive investment and somatic investment.
Data for age groups 6, 7, 8 and 9 were pooled due to low
sample sizes in those age groups. Unless stated otherwise, P-values ≤ 0·05 were considered significant.
Some maternal and reproductive characteristics
varied among years. To control for this variation, a
two-way analysis of variance was used to search for
differences among these variables with age and year as
class variables. No interactions between age and year
were found for any maternal or reproductive variable
(all Ps > 0·05).
Results
- 
Analyses of variance and Duncan’s multiple range
tests were used to search for differences in maternal
and reproductive variables among females of different
age classes (Table 1). Among successful females aged
2 years and older, reproductive and somatic investments did not differ among these age classes. Thus, we
pooled data on older females for some of our analyses.
Successful yearling and older females (aged 2–9 years)
showed different patterns in many maternal and reproductive characteristics. Older females had significantly
higher body masses at spring emergence from hibernation and at litter emergence, lower gain in mass during
the breeding season, larger litter sizes and earlier dates
of litter emergence when compared to yearling females.
To analyse annual survival and frequency of successful and unsuccessful reproduction in all females, age
classes from 1 to 5 and pooled 6–9 were examined
(Table 2). The oldest age classes were pooled because
of low sample sizes among these females. Only half of
yearling females weaned litters, while a vast majority of
females aged 2–5 years were reproductively successful.
In age classes 6–9, however, only 60% of the females
weaned litters. Thus, there was an uneven distribution
of successful vs. unsuccessful females ( χ 22 = 28·85,
P < 0·001). The females in the 2, 3, 4 and 5 age classes
had a significantly higher proportion of success at
weaning litters when compared to the yearling and
older age classes (yearling: χ12 = 40·2, P < 0·001; older:
χ12 = 24·04, P < 0·001). Annual survival did not differ
significantly among age classes ( χ 22 = 0·835, P = 0·66).
Table 1. Reproductive and maternal variables for successful female Columbian ground squirrel by age class ( ± 2 standard errors of the mean). Juvenile
215
mass is average mass of offspring at the end of lactation. Mass at litter emergence is female mass at or near the end of lactation. Data for older females (2–
Age-related
9 years old) are pooled for comparison with yearlings using Student’s t-test
reproduction
in
ground squirrels
Age class (years)
Variable
2
3
4
5
6 –9
Older 2–9
Yearling 1
t
P
Mass at emergence
from hibernation (g)
Mass at litter
emergence (g)
Somatic investment (g)
324 ± 11·8
(43)
417 ± 9·40
(43)
94 ± 5·2
(43)
377 ± 35·1
(43)
3·98 ± 0·38
(43)
29 April ± 2
(40)
98 ± 7·0
(43)
333 ± 13·0
(39)
412 ± 12·0
(39)
79 ± 6·4
(39)
363 ± 35·6
(39)
3·74 ± 0·40
(39)
1 May ± 2
(37)
100 ± 6·1
(39)
334 ± 16·8
(18)
428 ± 9·30
(18)
94 ± 8·6
(18)
400 ± 50·1
(18)
4·53 ± 0·80
(18)
30 April ± 3
(17)
97 ± 12
(18)
357 ± 30·2
(13)
438 ± 25·8
(13)
80 ± 11
(13)
412 ± 55·1
(13)
5·23 ± 1·04
(13)
25 April ± 5
(12)
83 ± 10
(13)
323 ± 22·8
(9)
405 ± 35·4
(9)
82 ± 9·8
(9)
398 ± 55·7
(9)
4·10 ± 0·80
(9)
29 April ± 3
(9)
93 ± 13
(9)
332 ± 3·72
(122)
418 ± 3·49
(122)
87 ± 3·4
(122)
379 ± 9·90
(122)
4·12 ± 0·13
(122)
29 April ± 1
(115)
96 ± 2·0
(122)
251 ± 6·50
(40)
375 ± 5·11
(40)
124 ± 7·37
(40)
284 ± 13·9
(40)
2·95 ± 0·16
(40)
3 May ± 1
(40)
101 ± 3·8
(40)
10·8
0·001
7·0
0·001
4·6
0·001
5·0
0·001
4·7
0·001
3·9
0·001
1·1
0·25
Reproductive
investment (g)
Litter size
Date of litter
emergence*
Juvenile mass (g)
*SE in days.
    
© 2003 British
Ecological Society,
Journal of Animal
Ecology, 72,
212–219
When all (successful and unsuccessful) females were
considered, somatic investment and reproductive
investment differed among age classes (Fig. 1a; somatic
investment: r2 = 0·27, F5,223 = 16·36, P < 0·001; reproductive investment: r2 = 0·15, F5,223 = 16·30, P < 0·001).
A Duncan’s multiple range test revealed that somatic
investment was highest in the yearlings while litter
mass was highest in the 5-year-olds. On average, yearling females had lower reproductive investment than
females of prime breeding ages (viz. 2–5-year-olds).
Also, on average, among the oldest females (6–9-yearolds), reproductive investment was significantly lower
compared to females of prime breeding age (t120 = 2·07,
P < 0·05). Among successful females, somatic investment and reproductive investment varied among age
classes. Somatic investment was highest in the yearling
age class (Fig. 1b; r2 = 0·17, F5,156 = 6·23, P < 0·001)
while reproductive investment was highest in the 5year-olds and lowest in the yearlings (Fig. 1; r2 = 0·15,
F5,156 = 5·61, P < 0·001).
The effects of maternal mass at emergence from
hibernation on reproductive investment and somatic
investment were analysed. Using residuals of regression, we repeated the above analyses of searching for
differences in reproductive investment and somatic
investment among age classes with both variables
statistically controlled for female spring emergence
mass. Analyses were run first for all females, and then
using only successful females. We found that controlling
for spring emergence mass eliminated the significant
differences among age classes when all females were
considered (somatic investment: r2 = 0·02, F5,223 = 1·09,
P = 0·37; reproductive investment: r2 = 0·06, F5,223 =
2·86, P = 0·02). The value for litter mass was considered
biologically insignificant because age explained only
6% of the variation in litter mass. Controlling for
spring emergence mass eliminated significant differences among age classes when only successful
females were considered (somatic investment: r2 =
0·03, F5,156 = 1·08, P = 0·37; reproductive investment:
r2 = 0·02, F5,156 = 0·86, P = 0·51). Therefore, spring
emergence mass explained 14% of the variation seen
in somatic investment among age classes and 12%
of the variation seen in reproductive investment among
age classes. Additionally, among successful yearling
and older females, mass at emergence from hibernation
was significantly negatively correlated with somatic
investment (yearlings: r = −0·74, n = 41, P < 0·001;
older: r = −0·51, n = 121, P < 0·001). Among older
successful females, reproductive investment was
significantly positively correlated with spring emergence mass (older: r = 0·29, n = 121, P < 0·001).
However, among successful yearling females, reproductive investment was not significantly correlated
Table 2. Percentage of female Columbian ground squirrels
by age class that weaned a litter and percentage of females that
survived to the next year. Sample size for weaning is the
number of females alive at the expected time of litter
emergence for whom weaning status was known and sample
size for survival is the number of females of known age at the
time of litter emergence
Wean
Survive
Age (years)
%
(n)
%
(n)
1
2
3
4
5
6 –9
All
49
83
93
100
100
60
73
(84)
(54)
(44)
(19)
(13)
(15)
(229)
74
83
82
68
69
73
77
(84)
(53)
(43)
(19)
(13)
(15)
(227)
216
D. R. Broussard
et al.
Fig. 1. Reproductive investment (black) and somatic
investment (white) of female Columbian ground squirrels (a)
all females (successful and unsuccessful); (b) only successful
females. Data are presented as mean ±2 standard errors.
Sample sizes appear above each bar. Age group 6 + represents
age groups 6 –9.
with spring emergence mass (yearlings: r = 0·06, n =
41, P = 0·71).
Among yearling Columbian ground squirrels,
female mass at emergence from hibernation differed
between successful females (mean = 252 g ± 6·2) and
unsuccessful females (mean = 229 g ± 5·6) (t-test:
t82 = 2·67, P = 0·009). Among older females, there was
no difference in mass at emergence from hibernation
for successful (mean = 330 ± 3·6) and unsuccessful
females (mean = 322 ± 8·4) (t-test: t143 = 0·80, P = 0·43).
Somatic investment was compared using t-tests. Somatic
investment of successful and unsuccessful females
differed significantly only for yearlings (Fig. 2; t82 = 2·42,
P = 0·02). However, when this analysis was repeated,
controlling for mass at emergence from hibernation, successful and unsuccessful yearling females did
not differ with respect to somatic investment (t82 = 0·73,
P = 0·50). Among females older than yearlings there
was no significant difference in somatic investment
(Fig. 2; t143 = 0·25, P = 0·80).
investment should decrease with age. The lower values
of litter mass and litter size observed in the yearling age
class seem consistent with the residual reproductive
value hypothesis (Pianka & Parker 1975). However, the
lack of increased reproductive investment by the oldest
females allows us to reject the residual reproductive
value hypothesis as an explanation of reproductive
patterns seen in our study. Also, investment in body
mass during reproduction did not decrease with age
for reproductive females older than yearlings as the
residual reproductive value hypothesis predicted.
The evolutionary restraint hypothesis states that
reproductive investment of the youngest females is
restrained by a cost to future reproduction and /or
survival (Williams 1966; Curio 1983; Marchetti & Price
1989; Rohwer 1992; Hepp & Kennamer 1993; Blums
et al. 1996). Consistent with this hypothesis was a
lower proportion of yearling females producing a litter
as compared to older females and higher somatic
investments of yearling females compared to older
females. In our study, a yearling females’ ability to
successfully wean a litter appeared limited by low
mass at emergence from hibernation. Therefore, a high
proportion of these individuals might have refrained
from attempting to raise a litter compared to older
adult females. This appeared to be due to yearling
females completing growth, as unsuccessful yearling
females weighed significantly less at spring emergence
than successful yearling females. Additionally, unsuccessful yearling females also gained significantly more
mass during the reproductive period than successful
females.
Evolutionary restraint provides an adaptive alternative to the hypothesis of developmental constraint. If
growth to full adult size was not possible during the
first year of life, then lowered reproductive investment
might be constrained by the need for structural growth.
Ground squirrels have deterministic structural growth
(Dobson 1992; Dobson & Michener 1995), and thus
restraint and constraint both seem reasonable explanations for lower reproductive investment in younger
female Columbian ground squirrels. However, both
Discussion
© 2003 British
Ecological Society,
Journal of Animal
Ecology, 72,
212–219
We used our estimates of reproductive and somatic
investments to evaluate three hypotheses that have
been proposed to explain age specific patterns of
resource investment during reproduction of female
Columbian ground squirrels. The residual reproductive value hypothesis predicted that reproductive
investment should increase with age, while somatic
Fig. 2. Somatic investment of successful (black) and unsuccessful (white) female Columbian ground squirrels. Data
are presented as mean ±2 standard errors. Sample sizes appear
above each bar. Age group 6 + represents age groups 6–9.
217
Age-related
reproduction in
ground squirrels
© 2003 British
Ecological Society,
Journal of Animal
Ecology, 72,
212–219
hypotheses make similar qualitative predictions concerning patterns of reproductive and somatic investments, as well as the influence of spring emergence
body mass. Both restraint and constraint predicted
that lighter, primiparous female Columbian ground
squirrels would forego or limit their first reproduction
to complete growth and invest resources into themselves. Thus, we could not distinguish between these
two possibilities.
We examined the senescence hypothesis (Williams
1957; Kirkwood & Rose 1984) by examining patterns
of reproductive and somatic investment over the lifetimes of females, by quantifying the proportions of
successful vs. unsuccessful females in each age class
(Berube, Festa-Bianchet & Jorgenson 1999), and by
examining survival of females by age class. When all
females (successful and unsuccessful) were considered,
reproductive investment declined significantly in the
oldest females, because the oldest females (aged 6–9
years) contained the largest proportion of unsuccessful
individuals among females older than yearlings. Senescence of reproduction in the some of the older females
is similar to senescence of reproduction in older bighorn
ewes (Berube et al. 1999), where the oldest age class
of ewes had a relatively lower reproductive output
compared to other adult age classes. Examinations of
somatic investment between successful and unsuccessful older adults show that, unlike unsuccessful yearlings, the oldest (aged 6–9 years) unsuccessful females
were not able to increase somatic investment. Millar
(1994) and Morris (1996) found evidence of senescence
in Peromyscus maniculatus and P. leucopus, respectively,
where declining body condition of older females resulted
in decreased reproductive success. In our study, senescence was evident primarily when examining the proportion of successful females in the oldest age group.
Studies that investigate reduced reproductive investment, measured by decreased litter size and/or litter
mass, may fail to detect senescence, as would studies
that attempt to demonstrate senescence from a lower
survival rate for older age classes (Slade 1995). Some of
the oldest females showed senescence by the failure to
wean a litter, but other older females showed similar
reproductive and somatic investments as compared to
younger females. Some older females exhibited reproductive senescence, while others did not.
Identification of senescent declines in reproductive
and somatic investments, and survival, are difficult to
identify. Although declines in reproduction and
survival have generally been interpreted as evidence
for senescence, Blarer, Dobeli & Stearns (1995)
demonstrated that such patterns may be produced by
optimal life histories, without physiological deterioration of individuals at advancing age. In addition, interspecific studies of senescence have assumed that
evidence of senescence should begin at or near the age
when individuals first reproduce (e.g. Promislow 1991;
Gaillard et al. 1994). Columbian ground squirrels did
not exhibit patterns of investments and survival that
would indicate agreement with the above works, as we
discuss below. Thus, we feel that the most reasonable
conclusion is that our population actually exhibited
senescent declines in reproductive investment by adult
females at relatively old ages.
Blarer et al. (1995) showed that if survival declined
due to continued growth throughout life and sizedependent mortality, then decreasing fecundity and
survival could be produced by an optimal life history,
in the absence of senescence. Columbian ground
squirrels did not fit this scenario. First, structural
growth, although continuing throughout life, occurs
at an extremely low rate, around 1% per year, so that
growth to adult size appears deterministic (Dobson
1992; Dobson, Risch, & Murie 1999). In our study,
spring body mass, which probably reflects stored
resources that females have at the start of the year, did
not increase significantly in the oldest females, but
instead exhibited a non-significant decline. Finally,
the decline in mean reproductive investment through
failure to produce litters occurred only in the oldest
age class of adult females, rather than gradually as
trade-off models generally predict. Thus, the basic
conditions for applying Blarer et al.’s (1995) model to
Columbian ground squirrels were not evident.
The lack of consistent directional changes in reproductive and somatic variables was also inconsistent
with the way that senescence has been identified in
interspecific comparisons. Promislow (1991) and
Gaillard et al. (1994), for example, used the rate at which
survival declines as evidence of how rapidly senescence
occurs. In our study, survival was slightly higher in
2- and 3-year-old females, but variations among age
classes were slight and not significant. Changes in
somatic investment during the reproductive period
were also essentially constant among females older
than yearlings. The proportion of females that produced litters successfully was extremely high through
5 years of age, and then fell dramatically. Thus, the
abrupt decline in mean reproductive investment among
the oldest females appeared out of context with the rest
of the age-structured life history, even taking trade-offs
into account. Senescence appears to provide the best
explanation for the reproductive decline.
Female mass at emergence from hibernation affected
patterns of age-specific reproductive and somatic
investment. Previous work has shown that maternal
mass can influence litter size, average mass of offspring,
or both (McClure 1981; Dobson & Myers 1989;
Michener 1989; Hoogland 1995; Derocher & Stirling
1998; Festa-Bianchet & Jorgensen 1998; Millesi et al.
1999). Older adult females that emerged from hibernation at a heavy mass were able to invest more resources
into reproduction while investing less into themselves
(see also Dobson et al. 1999). Yearling females that
emerged at a relatively high mass were able to wean
litters, while those that emerged at a lighter mass
completed growth instead of investing resources into
producing a litter.
218
D. R. Broussard
et al.
Reduced reproductive output of primiparous (firsttime breeding) females (smaller litters and/or reduced
proportion of individuals reproducing successfully)
compared to multiparous females, as observed in this
study, is consistent with other studies of vertebrates (e.g.
Festa-Bianchet & King 1991; Dobson & Michener 1995;
Risch, Dobson & Murie. 1995; Becker, Boutin & Larsen
1998; Huber et al. 1999; Millesi et al. 1999). The cessation
of reproduction by older females has also been shown in
other vertebrate species (e.g. Promislow 1991; Derocher
& Stirling 1994; Gaillard et al. 1994; Packer, Tater &
Collins 1998). The oldest females of these species show
either reduced reproductive output or stop reproducing
altogether. In our study, older females either reproduced
at a ‘normal’ level or were more likely to fail completely.
On average, the oldest female Columbian ground squirrels showed a significant decline in reproductive output
compared to younger females because they were less
likely to wean a litter compared to middle-aged females.
In conclusion, we found that some young female
Columbian ground squirrels were limited by low spring
emergence masses and therefore were constrained
or restrained in their energetic investment by delaying
production of litters, while completing growth during
their first full year after birth. We also found that the
oldest female age classes exhibited evidence of senescence of reproduction, and were the least likely to give
birth to litters among adults older than yearlings.
We concluded that evolutionary restraint or constraint
best explained patterns of reproduction seen in the
yearling females, while the senescence hypothesis best
explained reproductive patterns seen in the oldest
females. Due to the lack of increased reproductive
investment by the older females, we found no support
for the residual reproductive value hypothesis.
Acknowledgements
For assistance with fieldwork, we thank M.J. Badry,
C. Cassady-St Clair, I. Cote, C. DeVries, H. Dundas, J.
Hare, S. Hatfield, J. Hines, W.J. King, A. Knight,
R. Lewis, B. MacWhirter, M. Ramsay, J. Rieger, J.
Waterman, J.D. Wigginton and P. Young. We appreciate access to the study area granted by personnel of the
Turnbull National Wildlife Refuge and thank R. Carr
and D. Nichols for use of facilities at the Turnbull
Laboratory for Ecological Research. A. Badyaev, S.
Boback, C. Guyer, G.R. Hepp, D. Morris, P. Neuhaus,
C. Osenberg and J. Styrsky made very helpful comments on the manuscript. Fieldwork was funded by a
Natural Sciences and Engineering Research Council
of Canada grant to J.O.M. Data analysis and manuscript preparation was funded by a National Science
Foundation grant to F.S.D. (no. DEB-0089473).
© 2003 British
Ecological Society,
Journal of Animal
Ecology, 72,
212–219
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Received 9 April 2002; accepted 29 September 2002