Behavioral Ecology Vol. 11 No. 6: 633-639
© 2000 International Society for Behavioral Ecology
Early development, adult mass, and reproductive success in bighorn sheep
a Groupe de recherche en écologie, nutrition et énergétique, Département de biologie, Université de Sherbrooke, Sherbrooke, Québec J1K 2R1, Canada b Alberta Department of Environmental Protection, Natural Resources Service, Suite 201, 800 Railway Avenue, Canmore, Alberta T1W 1P1, Canada
Address correspondence to M. Festa-Bianchet, Départment de biologie, Université de Sherbrooke, Sherbrooke, Québec J1K 2R1, Canada. E-mail: mbianche{at}courrier.usherb.ca .
Received 12 August 1999; revised 18 February 2000; accepted 18 April 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Despite considerable empirical and theoretical work on the individual and population consequences of early development, little is known about the correlations between early mass and adult size or lifetime reproductive success of free-ranging mammals. Using a 26-year study of bighorn sheep (Ovis canadensis), we examined how mass as a lamb and mass gain as a yearling affected adult mass for both sexes, horn length of males and lifetime reproductive success of females at different population densities. Mass as a 3-week-old lamb was either weakly or not correlated with adult mass, horn length of adult males, or the number of lambs weaned over a ewe's lifetime. Weaning mass was correlated with most of these variables when the number of ewes in the population was taken into account. When weaning mass was controlled through partial correlation, mass as a yearling was correlated with adult mass of ewes but not with ewe reproductive success or with adult mass or horn length of rams. Lamb mass and number of ewes explained more of the variance in adult characteristics for males than for females. Our results suggest that mass gain during lactation, possibly but not necessarily related to the amount of maternal care received, affects adult mass and reproductive success. Females appear better able than males to compensate for poor early development, likely by postponing their first reproduction. Mass gain over several years and the number of ewes in the population strongly affect adult mass of both sexes and therefore can have profound effects on reproductive success of this long-lived species with a multi-year growth period.
Key words: maternal expenditure, maternal effects, early development, population density, Ovis canadensis, bighorn sheep, lifetime reproduction, body mass, horn size.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Early development is thought to play a key role in affecting individual reproductive success and population ecology of mammals. In ungulates, cohort variations in birth mass or juvenile growth affect life-history traits and population dynamics (Clutton-Brock et al., 1987
,
1992;
Post et al., 1997;
Rose et al., 1998).
Sæther (1997) suggested
that variables affecting early development could affect the reproductive
performance of different cohorts, regardless of whether or not they were
density-dependent. Lindström
(1999) found pervasive effects
of early development on life-history and population dynamics of birds and
mammals.
Despite the apparent importance of early development, most studies of
mammals have been limited to making comparisons among cohorts: little is known
about the consequences of early development for adult mass and reproductive
success of individuals. Large mammals are difficult to capture, and it is
unusual for researchers to weigh individuals repeatedly. Most published
information compares early mass to mass as an older juvenile or as a very
young adult. For 13 captive white-tailed deer (Odocoileus
virginianus) males, Schultz and Johnson
(1995) found a strong
correlation (r=.81) between birth mass and mass at 2.5 years of age,
while Birgersson and Ekvall
(1997) found that weaning mass
of captive fallow deer (Dama dama) was correlated (r
.72)
with mass at 23 months of age. A correlation between birth mass and
first-winter mass (r .72) was also reported by
Pélabon
(1997) for captive fallow
deer. Captivity, however, removes many environmental sources of variation in
growth, and the effects of early development on adult mass for captive animals
may differ from those for wild animals. For wild roe deer (Capreolus
capreolus) in a population with abundant resources, there was no
correlation between birth mass and first-winter mass
(Gaillard et al., 1993). In
feral sheep, birth mass only explained 8% of the variance in mass at 16
months, and 14% at 28 months
(Clutton-Brock et al., 1992).
For 11 red deer (Cervus elaphus) females, Clutton-Brock et al.
(1988) found a correlation of
birth and adult mass (r=.62), but adult mass was not adjusted for
either season or age. Birth mass is often used as an index of early
development (Byers and Hogg,
1995; Clutton-Brock et al.,
1992; Fairbanks,
1993; Smith et al.,
1997), but it does not account for differences in postnatal
maternal care and environmental effects. The frequent use of birth mass may be
due more to its availability than to its suitability as an index of early
development.
Correlations between early development and adult size and reproductive
success are particularly relevant to the study of maternal investment. It is
generally assumed, but seldom quantified, that differences in maternal
expenditure that affect early development also have long-term effects on
off-spring fitness (Clutton-Brock,
1991). Clearly, the strength of the relationship between early
development and lifetime reproductive success has a major effect on the
cost-benefit tradeoffs of alternative strategies of maternal investment. For
example, the theory of parent-offspring conflict
(Trivers, 1974) assumes that
an increase in maternal investment will increase offspring fitness. For
mammals, this theory must assume a correlation between size or condition at
weaning and lifetime reproductive success. A similar assumption is fundamental
to theories of adaptive sex-ratio variation
(Trivers and Willard,
1973).
Here we use long-term data on bighorn sheep (Ovis canadensis) to
investigate correlations between early development and adult mass. Because
most of our study animals were recaptured every year, we could compare mass
for the same individual at different ages. We also investigated the effects of
early development on lifetime reproductive success. For females, we used the
number of lambs weaned during lifetime. Because we had no data on paternity,
for rams we used horn length at five years of age as an indirect measure of
reproduction, assuming that horn size was correlated with reproductive success
(Geist, 1971). Because we
suspected that population density affected individual development, we included
in our analyses the number of adult ewes in the population in the year of
birth. We addressed three specific questions: (1) Is mass during early
development correlated with adult mass and other fitness-related adult traits?
(2) Do these correlations vary with the stage of early development when mass
is measured? (3) Do these relationships differ according to sex?
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study area and population
The study population inhabits Ram Mountain, Alberta, Canada (52°N, 115°W, elevation 1080 to 2170 m). Data used in this article were collected from 1973 to 1998. Sheep were captured in a corral trap from late May to early October and weighed to the nearest 250 g with a Detecto spring scale. Adjustments in body mass of adult ewes, rams aged 2 or 3 years, and lambs and yearlings of both sexes were made using each individual's own rate of mass gain, determined through repeated captures. Most rams 4 years of age and older were only caught from late May to July, and many were only caught once a year. For rams 4 years of age and older, therefore, mass was only adjusted to 5 June using age-specific linear regressions of mass on capture date for all rams combined.
We adjusted mass of individual lambs to 15 June and to 15 September. By 15
June, most lambs are about 3 weeks old
(Festa-Bianchet, 1988a),
therefore we refer to them as "3-week-old lambs." We chose 15 June
because few lambs were weighed before the first week in June. September 15
corresponds approximately to weaning
(Festa-Bianchet, 1988b),
therefore we refer to this age group as "weaned lambs."
Experimental weaning in early September did not affect yearling mass for
females and had a moderate (7-8% mass reduction) effect for males
(Festa-Bianchet et al., 1994).
It is therefore likely that by 15 September lactation is almost over. For
year-lings of both sexes, adult ewes and young rams, we adjusted mass to 5
June and to 15 September. More details about mass adjustment procedures are
reported elsewhere (Festa-Bianchet et al.,
1996). We measured horn length of all sheep captured. Here we
limited our analyses to horn length of 5-year-old males. We chose that age as
a compromise between assessing the effects of early development on horn size
of fullgrown rams [aged eight years and older
(Jorgenson et al., 1998)] and
the strong age-related decrease in sample size, as adult rams are subject to
high natural and hunting mortality
(Jorgenson et al., 1993b;
Loison et al., 1999). We used
the length of the longer horn for each ram, adjusted to 5 June through linear
regression using the slope of horn length on capture date for all
five-year-old rams from 24 May to 15 July. We measured lifetime reproductive
success of ewes as the number of lambs weaned, including only ewes born before
1987 that died of natural causes and a 13-year-old ewe still alive in
September 1999.
At first capture, lambs received numbered Ketchum metal ear tags that held a colored strip of Safeflag plastic. As yearlings, males received color-coded Allflex ear tags, females were fitted with canvas or plastic collars with unique patterns.
From 1973 to 1981, ewe removals maintained the population at an average of
34 adult ewes (Jorgenson et al.,
1993b). After 1981, the population increased, peaking at 104 ewes
in 1992 and declining to 75 ewes in 1997, when a further 11 adult and 3
yearling ewes were removed. Density-dependence was evident through delayed
primiparity (Jorgenson et al.,
1993a), decreased lamb survival
(Portier et al., 1998) and
lower mass gain and horn growth for young sheep
(Festa-Bianchet and Jorgenson,
1998; Jorgenson et al.,
1998).
Data analyses
As in previous publications
(Festa-Bianchet and Jorgenson,
1998), we measured population density as the number of adult ewes
in June in the year of birth. Substituting the average number of ewes during
the first 3 years of life led to very similar results to those reported here.
We previously reported that the number of rams in the population did not
affect horn development of rams (Jorgenson
et al., 1998) possibly because much horn growth occurs before
young rams leave the ewe groups at 2-4 years of age
(Festa-Bianchet, 1991). The
number of adult ewes is therefore a better measure of population density than
the number of rams. All bighorn habitat on Ram Mountain was utilized at all
levels of population size, therefore population size and density are
equivalent.
We used backward stepwise multiple regressions and partial correlations to
assess the relationships between early mass and adult mass, horn length and
lifetime reproductive success. For adult ewes, adult mass was the average mass
adjusted to 15 September at 5 to 7 years of age
(Festa-Bianchet et al., 1996).
For adult rams, we used the average mass at 4 and 5 years of age, adjusted to
5 June. We could not use the same measure of adult mass for both sexes for two
reasons. First, very few males aged 4 years and older were caught after July,
therefore we could not adjust the mass of rams to mid-September. Second, high
male mortality led to a small sample of rams older than 6 years. The measure
we used for ewes (average mid-September mass at 5 to 7 years of age) was
probably a better indicator of adult mass than the measure we used for rams
(average early-June mass at 4 and 5 years of age), because mass in September
is less affected than mass in June by year-to-year changes in weather
(Festa-Bianchet et al., 1996;
Réale et
al., 1999). For both sexes, we found results similar to those
reported here when we repeated univeriate analyses for body mass at each age
from 3 to 6 years for males and from 3 to 8 years for females. We excluded
male lambs orphaned during the early years of the study, because orphaning had
a weak but significant effect on their development
(Festa-Bianchet et al., 1994).
We include orphans, however, in the comparison of adult mass and horn length
with mass gain as a yearling, because we were interested in any factors
(maternal and environmental) that may have caused variation in postweaning
mass gain. Statistical analyses were performed using SPSS for the Macintosh
(SPSS, 1994).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Mass as a 3-week-old lamb
Multiple regressions including the number of adult ewes suggested that mass as a 3-week-old lamb had a weak, positive, and density-dependent effect on adult mass of both ewes and rams. Mass as a 3-week-old lamb was not correlated with ewe lifetime reproductive success and had a weak positive effect on horn length of adult rams through its interaction with number of ewes (see Table 1).
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Weaning mass and mass gain as a yearling
Mass at weaning affected adult mass of sheep of both sexes, reproductive
success of ewes and horn length of rams (see
Table 2, Figures
1 and
2). The number of adult ewes
had negative effects on the same variables. The interaction of weaning mass
and number of ewes was negative when retained in models including weaning mass
as a main effect, and positive in models including number of ewes as a main
effect (see Table 2), because
density had a negative effect on the dependent variables, while weaning mass
had a positive effect. For the sample of lambs included in the analyses, the
number of ewes was not correlated with weaning mass (males: r = -.25,
n = 21, p =.28; females: r =.03, n = 40,
p =.83).
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Yearlings were captured more frequently than lambs, therefore a mass
estimate for mid-September (that normally requires at least two captures; see
Festa-Bianchet et al., 1996)
was available for almost all yearling sheep. When we repeated the analyses
reported in Table 2 using mass
as a yearling on 15 September, we found very similar results. Weaning mass and
mass as a yearling, however, are not independent (females: r =.47,
n = 62, p <.001; males: r =.69, n = 60,
p <.001; test for equality of correlation coefficients, t
= 1.82, 0.1 > p >.05), therefore correlations of yearling mass
and adult characteristics may be simply an inevitable consequence of their
correlation with weaning mass. To test whether mass gain as a yearling had in
itself any effects on adult mass and reproductive success, we used the
residuals of the regression of yearling mass on weaning mass. For females,
those residuals were correlated with adult mass (r =.43, n =
33, p =.015), but not with lifetime reproductive success
(r=.27, n = 21, p =.24). In both cases, adding the
effects of population size at birth within a multiple regression did not
change the results as population size did not have a significant effect. For
males, however, the residuals of the regression of yearling mass on weaning
mass were not correlated with either adult mass (r=.23, n =
20, p =.35) or with horn length at 5 years (r=.22,
n = 25, p =.31).
Sex differences
Because of differences in capture timing and frequency, we could not use
the same measure of adult body mass for both sexes. However, the results of
multiple regressions including the effects of the number of ewes (see Tables
1 and
2) suggest that the explanatory
power of mass as a 3-week-old lamb and at weaning was much greater for males
(coefficients of multiple determinations of 0.75) than for females
(coefficients of determinations of 0.17 and 0.18), despite the fact that
post-weaning mass gain (relatively and absolutely) is greater for rams than
for ewes (Festa-Bianchet et al.,
1996).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Mass during early development is correlated with adult mass and reproductive success in bighorn sheep. The strength of the correlations between early development and adult mass increased as "early development" was measured at a later age, and lamb mass appeared to be a better predictor of ram adult mass and horn size of males than of ewe adult mass.
Mass as a 3-week-old lamb (on 15 June most lambs are between 15 and 25 days
old) had a marginally significant effect on ewe adult mass through its
interaction with the number of ewes in the population (see
Table 1), suggesting an
increasingly positive effect of mass as a 3-week-old lamb on adult mass as
population size increased. Our data do not suggest that mass at 3 weeks of age
affects ewe reproductive success. Mass as a 3-week-old lamb also affected
adult mass and horn length of males through its interaction with population
density (see Table 1). Both
adult mass and horn length are likely correlated with reproductive success in
bighorn rams (Geist, 1971),
therefore it is possible that mass as a 3-week-old lamb plays a small role in
affecting reproductive success of males.
Mass at 3 weeks of age is presumably affected by a combination of prenatal
and early postnatal maternal care, because at that age lambs are entirely
dependent on milk (Festa-Bianchet,
1988b). At 3 weeks of age, lambs are about one-third their weaning
mass, therefore the measurement error (assuming that our error in reading the
scale was independent of sheep mass) is proportionately greater for lambs at 3
weeks than at weaning. In addition, age differences of a few days may have a
greater effect on lamb mass at 3 weeks of age than at weaning. Compared to
other ungulates, bighorn sheep produce relatively small neonates
(Byers and Hogg, 1995), and
bighorns appear to have a very conservative maternal investment strategy,
postponing primiparity (Jorgenson et al.,
1993a) and decreasing maternal effort in response to increasing
population density (Festa-Bianchet and
Jorgenson, 1998). The results presented here show that the low
level of maternal care provided by some ewes may have a negative effect on
offspring fitness, because larger lambs tend to become larger adults with high
reproductive success. For both sexes, lamb mass at weaning had a stronger
effect on subsequent development than mass at 3 weeks of age. Therefore, our
data suggest that bighorn sheep may experience parent-offspring conflict:
increased maternal investment leads to a fitness cost by reducing fecundity
the following year (Festa-Bianchet et al.,
1998) but it may also increase offspring fitness because larger
lambs at weaning tend to develop into larger adults. Large adult ewes have a
longer life expectancy
(Bérubé
et al., 1999) and experience lower costs of reproduction
(Festa-Bianchet et al., 1998).
Ewes curtail maternal care at high density, a tactic that allows them to
maintain high survival and high summer mass gain regardless of population
density, but leads to small lambs with low viability at high population
density (Festa-Bianchet et al.,
1998; Festa-Bianchet and
Jorgenson, 1998; Jorgenson et
al., 1997). Parent-offspring conflict in bighorn sheep is likely
more intense at high than at low population density, and likely more intense
for sons than for daughters, as we previously speculated
(Festa-Bianchet et al.,
1994).
Our results give a limited picture of the total fitness effects of early
development because our analysis was restricted to individuals that survived
to adult age. We have reported elsewhere
(Festa-Bianchet et al., 1997)
that mass at weaning affects lamb survival to one year of age, and that the
effects of weaning mass on overwinter survival increase with population
density, similarly to results for feral domestic sheep
(Milner et al., 1999).
Therefore the effects of the density-dependent reduction of maternal care in
bighorn sheep include lower survival of lighter lambs, in addition to the
possible impacts on adult mass and reproductive success reported here.
Bighorn sheep have a complex pattern of mass changes: both sexes gain mass
until at least 7 years of age, and individuals gain 20-35% of their
late-winter mass each summer then lose most of that mass during the following
winter (Festa-Bianchet et al.,
1996). At weaning, females have achieved about 40% of their adult
mass, but males less than 30%; one year later, the corresponding figures are
70% for females and 50% for males. Therefore, during their development
individuals could compensate for poor early mass gain, but may also experience
events that negatively affect their growth, such as harsh weather, low
resource availability due to high population density, injuries, parasites, and
diseases (L'Heureux et al.,
1996).
Males are more strongly affected by early development than females. When
the number of ewes in the population was included in multiple regressions, the
multiple coefficients of determination obtained for rams were generally more
than twice those obtained for ewes (see Tables
1 and
2). Indeed, our results suggest
that over 70% of the variance in adult male mass and horn length is explained
by population density in the year of birth and by weaning mass, while less
than 20% of the variance in adult ewe mass is explained by the same variables.
These results may at first appear counterintuitive, given that postweaning
growth is much greater for rams than for ewes
(Festa-Bianchet et al., 1996),
and therefore the potential for compensatory growth should also be greater for
rams. Differences in plasticity of resource allocation between growth and
reproduction, however, potentially explain this paradox. By varying their age
of primiparity, females can allocate resources to growth or to reproduction,
and affect their mass gain between 2 and 4 years of age
(Jorgenson et al., 1993a).
Males, however, cannot redirect resources to growth from reproduction, even
though young bighorn rams can reproduce
(Hogg and Forbes, 1997).
Energy expenditure during the early-winter rut likely affects the timing of
consumption of fat reserves and possibly over-winter survival, but is unlikely
to affect skeletal growth and mass accumulation over the following summer.
Therefore, young females have greater flexibility than young males in
redistributing resources between somatic growth and reproduction. Compensatory
growth would weaken correlations between mass during early development and
adult mass, and the potential for compensation appeared stronger in ewes than
in rams. Rams are likely selected always to gain as much mass as possible,
because large adult males may enjoy high reproductive success
(Hogg, 1988). Rams that are
small early in life appear generally unable to compensate for their initial
disadvantage by increasing their growth rate later on. This conclusion is
strengthened by our analysis of the residual effects of yearling mass on adult
mass: For rams, it appeared that individual differences in mass accumulation
during the first year after weaning had little or no effect on fitness. For
young ewes, on the other hand, individual differences in mass accumulation as
yearlings had a significant effect on adult mass and suggested a compensatory
pattern of mass gain. Similar results were reported for Alpine ibex (Capra
ibex), where females but not males were able to compensate for poor horn
growth in their first year
(Toïgo et
al., 1999).
Because we found that weaning mass affected fitness-related adult
characteristics, a possible interpretation of our results is that variations
in the level of maternal care affect offspring fitness. If that interpretation
is correct, females that curtail maternal care when resources are scarce
(Festa-Bianchet and Jorgenson,
1998) would suffer a fitness cost through reduced offspring
survival or lowered quality of surviving offspring. That cost would presumably
be compensated by an increase in the ewe's survival and future reproductive
potential. Theories of sex-differential maternal investment have been
concerned with whether additional investment leads to different fitness
returns according to offspring sex (Clutton-Brock et al.,
1986, 1991). The apparent
absence of postweaning compensatory growth for males suggests that a reduced
level of maternal care should have a greater impact on the fitness of sons
than of daughters. One could then predict that the density-dependent decrease
in maternal care seen in this population would have a stronger effect on young
males than on young females, yet yearling survival was density-dependent for
females but not for males (Jorgenson et
al., 1997) and we have no evidence of sex-differential effects of
density on lamb survival (Festa-Bianchet
et al., 1997).
The assumption that a correlation between early development and adult
fitness traits is due to differences in maternal expenditure, however, remains
untested. A positive phenotypic correlation between early mass and adult
traits could arise in the absence of maternal effects on adult traits.
Phenotypic correlations of mass at different ages could be due to pleiotropic
genes that influence both traits (Falconer
and Mackay, 1996). For instance, individuals that are genetically
large early in life also tend to be genetically large later in life
(Cheverud et al., 1983). To
quantify the effects of maternal care on adult characteristics, other factors
that affect the relation between early development and adult size must be
accounted for. Cross-fostering experiments are a potential solution
(Lindström,
1999), but they are impractical or impossible with most wild
mammals. Another alternative is a quantitative genetic analysis based on
pedigrees. Because fathers were unknown in the Ram Mountain population,
however, we could not estimate maternal effects on the phenotypic correlation
between early mass and adult traits. Although maternal effects can have
important consequences on offspring fitness, little is known about the
persistence of maternal effects over an offspring's lifetime. Generally,
maternal effects have a strong effect on offspring early traits, but their
influence decreases with offspring age and may become negligible for adult
traits (Cheverud, 1984;
Wolf et al., 1998). Previous
studies of the Ram Mountain population suggest that small mothers may
compensate for potentially negative genetic effects on lamb mass by increasing
maternal expenditure, because the phenotypic relationship between maternal
mass and lamb mass is very weak
(Festa-Bianchet and Jorgenson,
1998;
Réale et
al., 1999). Maternal expenditure likely affects pre-weaning
development and survival, but lamb survival from weaning to one year was
unrelated to maternal mass while increasing with weaning mass (Festa-Bianchet
et al., 1997,
1998). In the study
population, more than 50% of the variability in adult mass appears due to
additive genetic variance
(Réale et
al., 1999), therefore it would not be surprising if only a small
part of the variance in adult mass was caused by differences in maternal
expenditure.
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ACKNOWLEDGEMENTS |
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We thank Bill Wishart for his support of the Ram Mountain project. Our research was generously funded by the Natural Sciences and Engineering Research Council of Canada, the Alberta Recreation, Sports, Parks and Wildlife Foundation, the Alberta Natural Resources Service, the Foundation for North American Wild Sheep, the Fonds pour la Formation de Chercheurs et l'Aide à la Recherche (Québec), and the Université de Sherbrooke. We are grateful for the logistic support of the Alberta Forest Service. Many students, colleagues, volunteers, and assistants contributed to this research and we are grateful to all of them. The manuscript was constructively criticized by Steeve Côté, Jean-Michel Gaillard, Bruno Gallant, Wendy King, and two anonymous reviewers. This is contribution No. 133 of the Groupe de recherches en écologie, nutrition et énergétique.
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