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Effects of early horn growth on reproduction and
hunting mortality in female chamois
Marco Rughetti
1,2
* and Marco Festa-Bianchet
2
1
Parco Naturale Alpi Marittime, Piazza Regina Elena 30, 12010 Valdieri (CN), Italy; and
2
De
´partement de Biologie and
Centre d’e
´tudes Nordiques, Universite
´de Sherbrooke, Sherbrooke, QC J1K 2R1, Canada
Summary
1. Environmental conditions during early development can affect the growth patterns of verte-
brates, influencing future survival and reproduction. In long-lived mammals, females that experi-
ence poor environmental conditions early in life may delay primiparity. In female bovids, annual
horn growth increments may provide a record of age-specific reproduction and body growth. Horn
length, however, may also be a criterion used by hunters in selecting animals to harvest, possibly
leading to artificial selection.
2. We studied three populations of chamois (Rupicapra rupicapra) in the western Alps to explore
the relationships between female horn length and early growth, age of primiparity and age-specific
reproduction. We also compared the risk of harvest to reproductive status and horn length.
3. Early horn growth was positively correlated with body mass in pre-reproductive females and
with reproduction in very young and senescent adults. Females with strong early horn growth
attained primiparity at an earlier age than those with weak early growth. Horn lengthdid not affect
hunter selection, but we found a strong hunter preference for nonlactating females.
4. Our research highlights the persistent effects of early development on reproductive performance
in mammals. Moderate sport harvests are unlikely to affect the evolution of phenotypic traits and
reproductive strategies in female chamois. A policy of penalizing hunters that harvest lactating
females, however, may increase the harvest of 2-year-old females, which have high reproductive
potential.
Key-words: horn growth, hunting, primiparity, Rupicapra rupicapra, senescence
Introduction
The evolution of reproductive strategies is of central interest
in ecology. Because many populations are exploited or other-
wise affected by human activities, a simultaneous consider-
ation of natural and artificial selective pressures should
provide novel insights and may be required for most large
mammals (Festa-Bianchet 2003; Proaktor, Coulson & Mil-
ner-Gulland 2007). That approach would be particularly
appropriate in cases where natural and artificial selective
pressures are thought to be opposite, as in the case of trophy
hunting (Coltman et al. 2003). Here, we examine how differ-
ences in morphology and early development may influence
the reproductive success of female chamois (Rupicapra rupic-
apra Linnaeus) exposed to natural and artificial selective
pressures.
Environmental conditions during early development can
affect the growth patterns of vertebrates (Lindstro
¨m 1999).
Harsh weather, high density or scarce resources decrease
juvenile growth rate,reducing bodydevelopment and eventu-
ally future reproductive performance (Madsen & Shine 2000;
Gaillard et al. 2003; Beauplet et al. 2005). Rapid early devel-
opment is typically associated with large mass and high
reproductive success in adults (Lummaa & Clutton-Brock
2002; Beauplet & Guinet 2007; Solberg et al. 2008). In polyg-
ynous and sexually dimorphic ungulates, males with rapid
early growth are typically larger as adults and have higher
reproductive success than males with poor early growth
(Kruuk et al. 1999; Solberg et al. 2008). Rapid growth, how-
ever, is associated with greater mortality of juvenile males
during periods of resource scarcity (Clutton-Brock, Major &
Guinness 1985). On the contrary, when resources are scarce,
females allocate energy to growth and maintenance rather
than to reproduction (Gaillard et al. 2000a; Festa-Bianchet,
Gaillard & Coˆ te
´2003). Females that experience poor envi-
ronmental conditions early in life can delay primiparity
(Festa-Bianchet & Jorgenson 1998; Gaillard et al. 2003) and
may show compensatory growth later in life. Ungulate
females that attain primiparity at an early age are typically
heavier than nonreproducing females of the same age
*Correspondence author. E-mail: marco.rughetti@Usherbrooke.ca
Journal of Animal Ecology 2011, 80, 438–447 doi: 10.1111/j.1365-2656.2010.01773.x
2010 The Authors. Journal compilation 2010 British Ecological Society
(Jorgenson et al. 1993; Garel et al. 2009; Hamel et al. 2009a).
In bighorn sheep (Ovis canadensis Shaw), heavy adult females
live longer than light ones (Gaillard et al. 1998) and have
higher reproductive success at all ages (Be
´rube
´, Festa-Bian-
chet & Jorgenson 1999). In red deer (Cervus elaphus Linna-
eus), Nussey et al. (2007) found that poor environmental
condition early in life decrease the fecundity of senescent
females, while females that enjoy favourable environmental
conditions during early development have high fecundity at
all ages. Good environmental conditions during ontogeny
may lower the costs of early primiparity (McElligott, Altw-
egg & Hayden 2002; Moyes et al. 2006) and allow a strong
reproductive performance during senescence.
In temperate climates, the horns of bovids stop growing in
winter, usually forming a distinct annulus (Bubenik & Bube-
nik 1990). The growth of each annual horn increment can be
affected by environmental conditions (Festa-Bianchet et al.
2004), reproduction (Miura, Kita & Sugimura 1987) and
early development, as some species show compensatory
growth (Pe
´rez-Barberı
´a, Robles & Nores 1996; Festa-Bian-
chet & Coˆ te
´2008). Consequently, horn increments may pro-
vide a permanent indication of age-specific body growth. In
some species, primiparity is associated with reduced horn
growth (Miura, Kita & Sugimura 1987), but we know little
about the relationship between early horn development and
age-specific female reproductive success.
Because most mountain ungulate populations are subject
to sport hunting, it is important to consider the potential eco-
logical impacts and artificial selective pressures from human
harvest (Festa-Bianchet 2003). Horn length may be a crite-
rion used by hunters in deciding which animals to harvest,
possibly leading to artificial selection (Festa-Bianchet 2003).
Hunters usually seek specific age or sex classes (Milner, Nil-
sen & Andreassen 2007), decreasing their survival (Bonenfant
et al. 2008). If hunters preferentially remove individuals with
long horns, they may also select against correlated traits, such
as large mass (Coltman et al. 2003) or possibly early repro-
duction. If hunters prefer to harvest females without depen-
dent offspring (Festa-Bianchet 2007), however, hunting may
increase the mortality of nonlactating females, possibly
affecting the evolution of female reproductive strategies
(Proaktor, Coulson & Milner-Gulland 2007). Several studies
have examined the ecological and evolutionary effects of
hunting on males (Femberg & Roy 2008), and simulations
suggest that high harvest rates may favour females that make
a greater reproductive effort early in life (Proaktor, Coulson
& Milner-Gulland 2007). Few studies, however, have empiri-
cally evaluated the potential effects of hunting on female
reproductive strategy (Mysterud, Yoccoz & Langvatn 2009).
We studied three populations of chamois in the western
Alps to explore the relationships between horn increment
length in females and early growth, age of primiparity, age-
specific reproduction and the risk of sport harvest. We tested
six hypotheses (Table 1). We expected that early horn growth
would reflect early body growth and predict adult horn
length but not adult mass, similarly to what we found for
Table 1. Summary of hypotheses, predictions and populations involved, for a study of reproductive success in female chamois in the western
Italian Alps. ‘Park’ refers to a protected population, while VCO2 and CN4 are hunted populations. Regulations imposed a heavy penalty for
harvesting lactating females in VCO2
Hypothesis Predictions Populations
Supported
(yes, no)
(A) Early horn growth is an index of early
rapid development but not of adult
mass.
Early horn growth is positively correlated with
yearling mass but not with adult mass.
CN4, VCO2, Park Yes
(B) Early horn growth predicts adult horn
length.
Early horn growth is positively correlated with
adult horn length.
CN4, VCO2, Park Yes
(C) Females with rapid early growth
reproduce early.
Horn increments grown over the first2 years of
life are correlated with age of primiparity.
CN4, Park
a
Yes
(D) Females with rapid early growth have
greater probability to reproduce when
aged 4 years and older.
Horn increments grown over the first2 years of
life are correlated with probability of reproduction.
CN4, Park
a
No
b
(E) Hunter prefers to harvest nonlactating
females, particularly when heavy
penalties apply to the harvest of
lactating ones.
Lower frequency of lactating females harvested
in VCO2 than in CN4.
In VCO2 but not in CN4, asthe hunting season
progresses, the availability of nonlactating females
should decrease and more lactating females will
be harvested.
In VCO2, the harvest will include more 2-year-old
females compared to CN4, because 2-year-old
females are unlikely to lactate.
CN4, VCO2, Park
c
Yes
(F) Hunters prefer to harvest long-horned
females where penalties for harvesting
lactating females are light.
Length of horn increments grown over the first few
years of life will decrease with ageat harvest in
CN4 but not in VCO2.
CN4, VCO2 No
a
Not tested in VCO2 because of small sample size.
b
Yes for senescent females.
c
Gestation rate inthe Park wasused as an age-specific control unbiased by hunter selectivity.
Early horn growth 439
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of AnimalEcology,80,438–447
males (Rughetti & Festa-Bianchet 2010). We then tested
whether horn length as a yearling was positively correlated
with the probability to reproduce at all ages. In female cham-
ois, horn growth during the first two summers of life accounts
for about 73% of horn length at 5 years (Bassano, Perrone &
von Hardenberg 2003;Fig. 1). We expected that horn growth
over the first 2 years of life would be correlated with age of
primiparity. On the other hand, horn growth in the year of
first reproduction can be reduced by the energy cost of lacta-
tion (Miura, Kita & Sugimura 1987). For females aged
4 years and older, we expected that rapid early horn growth
would be correlated with fecundity.
Finally, we assessed whether horn length and reproductive
status affected hunter selection and consequently female sur-
vival. We monitored two areas with differing hunting regula-
tions and expected that heavier penalties for the harvest of
lactating females would lead to an increase in the proportion
of nonlactating females in the harvest. Harvest should then
be concentrated on very young and old females that are less
likely to lactate than prime-aged females (Crampe et al.
2006). If reproductive status did not strongly affect hunter
choice, hunter selectivity could be mostly based on horn
length, and females with rapid early horn growth could be
harvested at a younger age than those with slow growth.
Materials and methods
STUDY AREA
Our study populations included the Alpi Marittime Natural Park
(280 km
2
), where no hunting is allowed, and the adjacent hunting
area CN4 (595 km
2
), in south-western Piedmont, Italy, near the bor-
der with France (4412¢N, 716¢E). The second hunted area (VCO2,
727 km
2
) is in northern Piedmont near the border with Switzerland
(4612¢N, 829¢E). All study areas have narrow valley and steep
mountains. Chamois use areas mostly between 1000 and 3000 m
a.s.l. As altitude increases, forests of beech (Fagus sylvatica) are
replaced by conifers (Picea abies, Abies alba and Larix decidua), then
alpine pastures at higher elevations. Rocks and moraines cover 47%
of the Park and about 25% of VCO2 and CN4. Ibex (Capra ibex
Linnaeus) is the only other mountain ungulate, abundant in the Park
and small isolated populations in CN4. Roe deer (Capreolus capreo-
lus Linnaeus) and wild boar (Sus scrofa Linnaeus) are present mainly
under 1200 m elevation. Red deer are abundant in CN4 and VCO2.
Wolves (Canis lupus Linnaeus) are permanent residents in the Park
and in CN4. Cattle graze all study areas during summer.
POPULATION DATA
In the Park, 374 females aged 2 years and older were captured by
dart gun in April–May, mostly 2–6 weeks before parturition, from
1991 to 2008 and released elsewhere for reintroduction programmes.
Gestation status was recorded for 319 of these by abdominal palpa-
tion. In CN4 and VCO2 respectively, 552 and 495 females aged
2 years and older were harvested from 2000 to 2008. In CN4, the
hunting season starts in mid-September and normally ends in mid-
December, but 89% of females were harvested in September and
October. In VCO2, hunting starts in early September and normally
ends in early October. Lactation status was noted for 445 females in
CN4 and 380 in VCO2. We included in the analyses data from 11 3-
year-old females harvested in CN4 in 2009. Age and body mass (kg)
(eviscerated mass for harvested animals) were recorded for all
females. Age can be determined precisely by counting the horn annuli
(Schroder & Elsner-Schack 1985). Horn length (cm) was measured
from tip to base along the frontal surface. Because it is not possible
to distinguish the horn increments grown during the first and second
summers, we combined growth over the first 2 summers (L2) for all
analyses (see (Coˆ te
´, Festa-Bianchet & Smith 1998), for a similar
approach in mountain goats Oreamnos americanus De Blainiville).
We measured horn increments for all females captured in the Park,
175 shot in CN4 from 2006 to 2009 and 99 shot in VCO2 in 2007 and
2008. Because horn increments grown after the fourth summer of life
are generally 2 mm or less, we restricted our analyses to either total
horn length or the firstfour increments.
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17
Age (years)
5
10
15
20
25
Horn length (cm)
Fig. 1. Box plot of horn length of 717 female
chamois aged 2 years and older harvested in
autumn in the CN4 hunting area in southern
Piedmont, Italy, 2000–2009.
440 M. Rughetti & M. Festa-Bianchet
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology,80,438–447
HUNTING REGULATIONS
Hunting regulations in Piedmont encourage theharvest of nonlactat-
ing females. In both hunting areas, hunters that harvest a nonlactat-
ing female increase their position on a merit scale that gives access to
permit for adult males, while hunters that harvest a lactating female
cannot harvest an adult male in either the current or the successive
hunting season. In VCO2, however, regulations provide stronger
incentives against shooting lactating females: hunters can have up to
four chamois tags during a season but killing a lactating female limits
them to two and leads to a fine that increases if the hunter harvests a
second lactating female. Consequently, we expected stronger hunter
selection for nonlactating females in VCO2 than in CN4. Harvest
rate in 2002–2007 varied from 0Æ09 to 0Æ13 in CN4 and from 0Æ11 to
0Æ15 in VCO2 with an average, respectively, of 10% and 13% of the
number of chamois seen during annual censuses. The actual harvest
rate, however, was lower, as census counts underestimate population
size (Loison et al. 2006).
STATISTICAL ANALYSIS
We present statistical methods according to the hypotheses listed in
Table 1.
Hypothesis A: To test for a correlation between early horn growth
and adult mass, we fitted a linear regression for each age class using
horn length (cm) as a yearling as the predictor variable. We consid-
ered the following age classes: 2, 3 and 4 years and older in the Park
and 1Æ5, 2Æ5, 3Æ5 and 4Æ5 years and older in CN4 and VCO2. Most
chamois in Piedmont are born in late May; therefore, they were near
their approximate birth dates when captured in the Park and about
6 months older during the hunting season.
Hypothesis B: To test whether total horn length was a function of
horn length as a yearling, we used a multiple linear regression
including population as a covariate. We expected a positive effect of
early horn growth on adult horn length despite compensatory
growth.
Hypothesis C: Because primiparity was mainly at three and
4 years, we used a general linear model with a binomial distribution
to estimate the probability that a 3-year-old female would be lactat-
ing in autumn in CN4 or pregnant in spring in the Park as a function
of early horn growth. Horn increments grown during the third (L3)
and fourth (L4) summers of life (when chamois are aged 2 and
3 years) were negatively correlated with L2 (CN4, r=)0Æ53 for L3,
n= 131 and )0Æ43 for L4, n= 99. Park, r=)0Æ57 for L3, n= 299
and )0Æ37 for L4, n= 256). Therefore, we considered the residuals
of the regressions of L3 and L4 on L2 (RL3 and RL4), which reflect
variation in horn growth in years 3 and 4 that is not explained by L2.
We tested the following models: CN4, Logit (P-lactating) = L2 ·
RL3 ·RL4; Park, Logit (P-pregnancy) = L2 ·RL3. We expected
higher values for RL3 (last increment grown before reproduction)
and lower values for RL4 (increment grown while lactating) for
females primiparous as 3-year-olds compared to nulliparous 3-year-
olds. For the Park, we could not compare RL4 with reproductive
status at age 3, because animals were captured in spring, before L4
had finished growing. We did not estimate the probability of early
reproduction as a function of L2 in VCO2 because of the small
sample of females aged 3 years (n= 19, 2 lactating).
Hypothesis D: To assess the effect of early horn growth on
reproduction of females aged 4 years and older in CN4 and in the
Park, we modelled the probability of reproduction as a function of
age, body mass and length of horn grown as a yearling, using general
linear models with a binomial distribution: CN4, Logit (P-lactat-
ing) = age ·age
2
·mass ·L2; Park, Logit (P-pregnant) = age ·
age
2
·L2. We included a quadratic effect of age to account for
potential senescence. In CN4, harvest date was not included because
it did not affect female mass (Rughetti & Festa-Bianchet unpublished
data). In the Park, we did not consider the effect of mass because we
could not account for foetal mass for pregnant females. We did not
analyse data for VCO2 because we measured only 20 lactating
females. Because some females in CN4 were eviscerated and others
partially eviscerated (with heart, liver and lungs), we first estimated
the age-specific difference in mass in the two groups, then subtracted
it from partially eviscerated mass to estimate eviscerated mass.
Hypothesis E: We examined whether hunter preference for non-
lactating females was stronger in VCO2 than in CN4. We used the
frequency of pregnant females in the Park as a control unbiased by
hunter selectivity. Because of juvenile mortality, lactation rates
should generally be lower than gestation rates, but we assumed that
this decrease would not be affected by female age. To compare age
effects on reproduction, we fitted a general linear model with a bino-
mial distribution and a cubic smoothing spline procedure (Bartels,
Beatty & Barsky 1995). We expected a lower frequency of lactating
females in VCO2 than lactating in CN4 or gestating in the Park. We
then used a general linear model with a binomial distribution to
examine whether the proportion of lactating females in the harvest
increased during the hunting season. If hunters prefer to harvest non-
lactating females, with the advance of the season the availability of
nonlactating females should decrease and more lactating females
should be shot. Finally, we compared the age structure of females
captured in the Park and harvested in CN4 and VCO2 with a Pear-
son’s chi-squared statistic (Snedecor & Cochran 1980). In VCO2, we
expected a greater proportion of young females compared to the Park
and CN4 populations, because young females were unlikely to
lactate.
Hypothesis F: If hunters prefer to harvest long-horned females,
short-horned females should live longer. We fitted a multiple linear
regression model to test for a decrease in length of the yearling horn
increment with increasing age at harvest (Hengeveld & Festa-Bian-
chet in press). Because an apparent decrease of L2 may be due to
horn tip wear, we repeated the same analysis for horn increments
grown during the third and fourth summers of life.
All analyses were conducted in R (R Development Core Team
2009). To select final models, we began with a full model including all
variables of interest and their interactions, then simplified it using a
stepwise procedure based on P-values. To test the fit of logistic
regression models, we performed a goodness of fit test from the
Design packages (Harrell 2009). Large P-values indicate an accept-
able fit.
Results
In the Park, horn growth during the first two summers of life
was correlated with mass for 2-year-old females captured in
April–May; at 3 years the correlation was weak, and for
adults it disappeared (Table 2). We found similar patterns in
CN4 and VCO2: horn length of yearlings in autumn was cor-
related with mass, but for older females, horn growth during
the first two summers of life explained almost no variability
in mass (Table 2).
Total horn length increased rapidly from 2 to 4 years, then
changed little with age (Fig. 1). For females aged 4–10 years,
Early horn growth 441
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of AnimalEcology,80,438–447
horn growth as a yearling explained 26% of the variability in
total horn length (horn length = L2 + population; L2, slo-
pe = 0Æ459, SE = 0Æ043, t
348
=10Æ62, P<0Æ001; popula-
tion (Park), intercept = )0Æ390, SE = 0Æ191, t
348
=)2Æ05,
P=0Æ04; population (VCO2), intercept = )0Æ934,
SE = 0Æ276, t
348
=)3Æ38, P<0Æ001). Population affected
the intercept of the regression of horn growth as a yearling on
total horn length but the slopes were similar
(length = L2 + population vs. length = L2 ·population,
F=2Æ51, P=0Æ5). Total horn length averaged 20Æ0cm
(±1Æ7 SD) in CN4, 19Æ6 cm (±1Æ7 SD) in the Park and
19Æ3 cm (±1Æ3 SD) in VCO2.
From 2000 to 2008, 4 of 74 (5%) and 12 of 105 (11%) 2-
year-old females harvested, respectively, in CN4 and VCO2
were lactating. Of 43 2-year-olds captured in the Park from
1992 to 2008, none was pregnant; therefore, primiparity was
mainly at three and 4 years. Horn length at age 2 was posi-
tively associated with reproductive status at 3 years, explain-
ing, respectively, 17% and 20% of the probability of being
pregnant in the Park or lactating in CN4 (Fig. 2, Table 3).
The residuals of the third and fourth horn increments on L2
did not improve the model in either CN4 (RL3: slo-
pe = )0Æ256, SE = 0Æ371, t
31
=)0Æ69, P=0Æ49; RL4: slo-
pe = 0Æ184, SE = 0Æ536, t
30
=0Æ34, P=0Æ73) or the Park
(RL3: slope = 0Æ159, SE = 0Æ493, t
32
=0Æ32, P=0Æ75).
In both the Park and CN4, the probability of reproduction
declined after about 9–11 years of age (Fig. 3, Tables 4 and
5). After accounting for age, horn growth as a yearling did
not affect the probability of gestation for females aged
4 years and older in the Park (slope = 0Æ078, SE = 0Æ080,
t
249
=0Æ97, P=0Æ33). In CN4, horn growth as a yearling
affected lactation in interaction with age; after accounting
for mass, senescent females were more likely to reproduce if
they had grown longer horns as yearlings (Table 4, Fig. 2).
For females aged 11 years and older in CN4, horn growth as
a yearling was 12% longer in 14 lactating than in 13 nonlac-
tating ones (anova F
1,26
=8Æ62, P=0Æ007; lactating
mean = 14Æ8cm±1Æ4 SD; nonlactating mean = 13Æ2±
1Æ6 cm) and was correlated with body mass (slope = 0Æ72,
SE = 0Æ284, t
26
=2Æ52, P=0Æ018, R
2
=0Æ20). Lactating
females were lighter than nonlactating ones, and this differ-
Table 2. Linear regression of body mass as a function of the length of
horn grown during the first 2 years of life (L2) for 294 female
chamois aged 2, 3, and 4 years and older captured in the Alpi
Marittime Natural Park, Italy, from 1991 to 2008, and for 635
females aged 1Æ5, 3Æ5, and 4Æ5 years and older harvested in the
hunting areas of CN4 and VCO2 from 2000 to 2009. Age classes with
sample size less than 20 are not reported. For harvested yearlings, L2
is the total length of the horn
Age Slope SE t-value Pr(>|t|) R
2
d.f.
PARK
20Æ788 0Æ269 2Æ933 0Æ006 0Æ212 32
30Æ615 0Æ296 2Æ081 0Æ045 0Æ110 35
4+ 0Æ050 0Æ116 0Æ434 0Æ664 0Æ001 221
CN4
1Æ51Æ015 0Æ094 10Æ837 0Æ000 0Æ395 180
3Æ50Æ140 0Æ208 0Æ673 0Æ505 0Æ012 38
4Æ5+ 0Æ212 0Æ157 1Æ354 0Æ179 0Æ019 94
VCO2
1Æ50Æ906 0Æ082 11Æ077 0Æ000 0Æ330 249
4Æ5+ 0Æ258 0Æ225 1Æ145 0Æ256 0Æ021 64
Lactation
8
10
12
14
16
Length of horn grown as a yearling (cm)
Yes
No
Pregnancy
8
10
12
14
16
Yes
No
Lactation
8
10
12
14
16
Length of horn grown as a yearling (cm)
Yes
No
Lactation
8
10
12
14
16
Yes
No
(a) (b)
(d)(c)
Fig. 2. Box plot of horn length as a yearling (L2) with respect to
reproductive status for (a) 39 3Æ5-year-old female chamois harvested
in autumn in the CN4 hunting area, 2006–2009 (b) 39 3-year-old
females captured in April–May in the nearby Alpi Marittime Natural
Park, 1991–2008 (c) 77 female chamois aged 4–10 years (d) and 27
female chamois aged 11 years and older harvested in autumn in
CN4, 2006–2008.
Table 3. Logistic regression of the probability of gestation as
function of horn growth during the first two summers of life (L2) for
39 3-year-old females chamois captured in April–May in the Alpi
Marittime Natural Park, 1991–2008, and of lactation for 39 3Æ5-year-
old females harvested in autumn in the nearby CN4 hunting area,
2006–2009
Estimate
Std.
error d.f.
Wald
v2P-value
PARK
Intercept )10Æ387 4Æ231 1 6Æ027 0Æ0141
L2 0Æ822 0Æ330 1 6Æ225 0Æ0126
CN4
Intercept )9Æ301 3Æ320 1 7Æ862 0Æ005
L2 0Æ666 0Æ244 1 7Æ436 0Æ006
Goodness of fit test: Park, Z=1Æ61, P=0Æ11; CN4, Z=)0Æ49,
P=0Æ62.
442 M. Rughetti & M. Festa-Bianchet
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology,80,438–447
ence was greater for prime-aged than for senescent females
(11 years and older, Table 4). Mean eviscerated mass for lac-
tating females aged 4–10 years was 18Æ8 kg (±2Æ9SD)or
10% less than the average of 20Æ8 kg (±2Æ7 SD) for nonlac-
tating ones. Mean eviscerated mass for lactating senescent
females was 18Æ2 kg (±2Æ6 SD), only 4% less than the aver-
age of 18Æ9 kg (±2Æ2 SD) for nonlactating ones. For nonlac-
tating females, mass decreased with age (slope = )0Æ24,
SE = 0Æ10, t
37
=)2Æ29, P=0Æ028), whereas for lactating
ones, it was independent of age (t
60
=0Æ11, P=0Æ9).
For each age class, pregnancy rates in the Park were higher
than lactation rates in hunted populations (Fig. 3, Table 5).
Among those aged 4–11 years, there were more lactating
females harvested in CN4 (66%) than in VCO2 (54%)
(v
2
=6Æ39, d.f. = 1, P=0Æ011). The proportion of lactat-
ing females in the harvest increased during the hunting sea-
son in VCO2 but not in CN4 (Table 6). The proportion of
females aged 2 years harvested in VCO2 was much greater
(29%) than for Park captures (11%) or in the CN4 harvest
(14%) (v
2
=55Æ74, d.f. = 2, P<0Æ001; Fig. 4). The pro-
portion of females aged 3–11 years was greater in Park cap-
tures (83%) than in CN4 (68%) or VCO2 (63%) harvests
(v
2
=41Æ68, d.f. = 2, P<0Æ001). Correspondingly, the
proportion of females aged 12 years and older also differed
among populations (Park = 6%, VCO2 = 8%, CN4 =
19%).
For both hunted populations, age of harvested females
was independent of either horn growth as a yearling or the
length of horn grown from 2 to 4 years of age (Table 7).
There was no difference between populations in horn growth
as a yearling (Table 7), but for the same growth as yearlings,
females in VCO2 grew shorter increments in the following
2 years than in CN4 [regression model: L2–4 = L2 + pop-
ulation; L2, slope = )0Æ488, SE = 0Æ064, t
143
=)7Æ63,
P<0Æ001; population (VCO2), intercept = )1Æ031, SE =
0Æ221, t
143
=)4Æ67, P<0Æ001]. The difference in horn
growth existed despite yearling females in VCO2 being 7%
heavier (15Æ5Kg±2Æ6 SD, n= 340) than in CN4
(14Æ5kg±3Æ0SD,n= 237), a difference that persisted
among females 4 years and older [20Æ6kg±2Æ8SDin
VCO2 (n= 340) and 19Æ6 kg ± 3 SD in CN4 (n= 237)].
0 2 4 6 8 10 12 14 16
10
30
50
70
90
A
g
e (years)
Percentage of reproductive females
Fig. 3. Percentage of pregnant females
among chamois aged 3 years and older cap-
tured in April–May in the Alpi Marittime
Park (plain dashed line and circles, 319
chamois, 1991–2008,) and of lactating
females among those aged 3 years and older
harvested in two hunting areas, CN4 (bold
solid line and triangles, 455 chamois, 2000–
2008,) and VCO2 (plain solid line and
squares, 380 chamois, 2000–2008). Lines are
cubic smoothed splines.
Table 4. Logistic regression of the probability of lactation for female
chamois aged 4 years and older harvested in CN4 from 2006 to 2008
in relation to age, age
2
, eviscerated mass and the length of horn
grown during the first two summers of life(L2)
Estimate
Std.
error d.f.
Wald
v2P-value
Intercept 49Æ142 18Æ388 1 7Æ140 0Æ007
Age )10Æ236 4Æ390 1 5Æ438 0Æ020
Age
2
0Æ490 0Æ240 1 4Æ170 0Æ041
L2 )0Æ275 0Æ250 1 1Æ201 0Æ273
Mass )2Æ485 0Æ947 1 6Æ875 0Æ009
Age
2
:L2 0Æ006 0Æ003 1 4Æ477 0Æ034
Age : mass 0Æ579 0Æ234 1 6Æ126 0Æ013
Age
2
: mass )0Æ033 0Æ013 1 6Æ007 0Æ014
Goodness of fit test: Z=)0Æ11, P=0Æ91.
Table 5. Logistic regression of the probability of gestation (Park,
1991–2008) and lactation (hunted populations, 2000–2008) of female
chamois aged 4 years and older as a function of age and populations
Estimate
Std.
error d.f.
Wald
v2P-value
Intercept 1Æ655 0Æ204 1 65Æ448 <0Æ0001
Age )0Æ079 0Æ020 1 15Æ109 0Æ0001
Population (CN4) )0Æ588 0Æ178 1 10Æ956 0Æ0009
Population (VCO) )1Æ036 0Æ195 1 28Æ260 <0Æ0001
Goodness of fit test: Z=)1Æ15, P=0Æ25.
Early horn growth 443
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of AnimalEcology,80,438–447
For females aged 4–10 years, the coefficient of variation in
body mass (VCO2 = 0Æ16, CN4 = 0Æ15) was greater than
that for horn length (VCO2 = 0Æ09, CN4 = 0Æ08).
Discussion
Our research produced two key results. First, early develop-
ment affected the reproductive performance of very young
and senescent females, but not of prime-aged adults. Second,
sport harvest did not appear to have strong selective effects
but it did increase the mortality of nonlactating females.
EARLY DEVELOPMENT AND REPRODUCTIVE POTENTIAL
Horn length as a yearling reflected early development
because it was correlated with early body mass. Conse-
quently, horn growth as a yearling provides a permanent
record of early development of female chamois. After
9–11 years of age, the probability of reproduction decreased
with age but a strong early development led to higher proba-
bilities of reproduction in very young and senescent females.
Female chamois with strong early horn growth attained
primiparity at an earlier age than females with lower early
growth and had longer horns as adults, despite compensatory
horn growth. Because of compensatory horn growth, the
length of the third and fourth increments was negatively cor-
related with horn length as a yearling and appeared indepen-
dent of age of primiparity. In the Park, early horn growth did
not affect reproduction during senescence, possibly because
of the limited sample of older females (15, including 12 12-
year-olds).
The age of first reproduction is an important trait in the
reproductive strategy of female mammals (Clutton-Brock
et al. 1987; Lindstro
¨m 1999; Festa-Bianchet, Jorgenson &
Re
´ale 2000). Typically, early primiparity is associated with
large mass, rapid early development, longer life expectancy
and greater fitness (Beauplet & Guinet 2007; Descamps et al.
2008; Hamel et al. 2009b; Pistorius et al. 2008). Good envi-
ronmental condition in early life and large mass positively
affected reproduction at all ages (Be
´rube
´, Festa-Bianchet &
Table 6. Logistic regression of the probability of lactation as a
function of date of harvest (days since the start of the hunting season)
for female chamois aged 2 years and older in the VCO2 and CN4
hunting areas from 2000 to 2008
Estimate Std. error d.f. Wald v2P-values
VCO2
Intercept )3Æ460 0Æ725 1 22Æ753 <0Æ0001
Date 0Æ300 0Æ079 1 14Æ288 0Æ0002
Date
2
)0Æ009 0Æ003 1 10Æ693 0Æ001
Date
3
0Æ00007 0Æ00003 1 8Æ410 0Æ004
CN4
Intercept 0Æ037 0Æ181 1 0Æ042 0Æ84
Date )0Æ003 0Æ005 1 0Æ452 0Æ50
Goodness of fit test: VCO2, Z=0Æ012, P=0Æ99; CN4, Z=1Æ5,
P=0Æ13.
2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Age
0
5
10
15
20
25
30
Percentage
Fig. 4. Age distribution of female chamois
captured in the Alpi Marittime Park (dark
bars, 374 chamois, 1991–2008) or harvested
in CN4 (grey bars, 552 chamois, 2000–2008)
and in VCO2 (white bars, 495 chamois,
2000–2008).
Table 7. Multiple linear regression of horn length as yearling (L2;
d.f. = 244) and horn increment from yearling to 4 years old (L2–4;
d.f. = 145) as a function of age of harvest and population (VCO2
and CN4) for females chamois
Value Std. error t-value P-value
L2
Intercept 13Æ306 0Æ202 65Æ925 0Æ0000
Age 0Æ010 0Æ025 0Æ418 0Æ68
Population (VCO2) 0Æ236 0Æ210 1Æ123 0Æ26
L2–4
Intercept 5Æ569 0Æ305 18Æ255 0Æ0000
Age )0Æ043 0Æ032 )1Æ342 0Æ18
Population (VCO2) )0Æ983 0Æ257 )3Æ825 0Æ0002
444 M. Rughetti & M. Festa-Bianchet
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology,80,438–447
Jorgenson 1999; Nussey et al. 2007). Adult female chamois
with strong early horn growth were apparently able to
acquire substantial amounts of resources to allocate to both
body growth and reproduction. Strong early horn growth
was correlated with a delayed positive fitness consequence by
increasing reproduction during senescence, probably because
early growth in horn and mass were correlated. Therefore,
our data suggest that horn length as a yearling is a reliable
index of reproductive potential in young and senescent
female chamois. Although early horn growth was not corre-
lated with mass of prime-aged adults, it was associated with
the mass of senescent females.
In CN4, female body mass during the hunting season
revealed an energetic cost of lactation. Lactating females
were lighter than nonlactating ones, as reported for other un-
gulates (Sæther & Haagenrud 1985; Clutton-Brock et al.
1996; Reimers, Holmengen & Mysterud 2005). Prime-aged
females therefore faced a trade-off between summer mass
gain and lactation. Autumn mass of senescent females, how-
ever, appeared independent of lactation status. We suggest
that the apparent lower cost of reproduction among older
female chamois arises through two mechanisms: first, females
that survive to the senescent phase are likely those with a
greater reproductive potential as prime-aged adults, as previ-
ously reported for bighorn sheep (Be
´rube
´, Festa-Bianchet &
Jorgenson 1999) and for roe deer (Gaillard et al. 2000b).Sec-
ond, older females may adopt a conservative reproductive
strategy, so that only those in good condition reproduce.
Lactating senescent and prime-aged females had similar
mass, but nonlactating senescent females were about 10%
lighter than nonlactating prime-aged females. Our conten-
tion is supported by the positive effect of early horn growth
on reproduction among senescent females. Females with
rapid horn growth early in life did not reproduce at a greater
rate than other females through the prime-aged years, but
maintained a high reproductive rate into their later years
(Fig. 2).
HUNTER SELECTION
Our results confirmed a strong hunter preference to harvest
nonlactating females where harvest of lactating females car-
ries strong penalties. In contrast to our expectations, how-
ever, horn length did not appear to affect harvest probability
in either hunting area, because the length of horn grown as a
yearling did not decline with harvest age, in contrast with
recent results for bighorn sheep males (Hengeveld & Festa-
Bianchet in press). Therefore, we found no evidence that
either hunting regulations or hunter selection favour the
survival of females with short horns. We suggest that the
relatively low hunting pressure, strong compensatory horn
growth and limited variability in horn length among adult
females weaken the effects of any hunter selection for long
horns, as we reported for males of the same species (Rughetti
& Festa-Bianchet 2010). Despite the limited evidence for hun-
ter selection for horn length, however, horn growth trajecto-
ries differed between the two hunted populations. In VCO2,
horn increments in the third and fourth summer of life were
shorter than in CN4 for the same length of horn grown as
yearling. That difference occurred despite heavier mass in
VCO2 than in CN4 and may suggest a selective pressure for
shorter horns in VCO2. It is unclear whether that pressure is
caused by hunting or is due to differences in environmental
conditions, but it is in the direction predicted by the appar-
ently stronger hunting pressure in VCO2 than in CN4.
Nonlactating females had a higher probability of being
harvested than lactating females. The low age-specific per-
centage of lactating females in VCO2 (Fig. 3) was likely due
to strong hunter preference for nonlactating females rather
than to a lower frequency of lactation than in the other two
populations. Harvest of lactating females increased with the
advance of the hunting season in VCO2 but not in CN4, pre-
sumably because as many nonlactating females were har-
vested early in the season, later on it became difficult for
hunters to find females without kids. Hunting culture in Pied-
mont and generally in Europe tends to frown upon shooting
lactating females (Festa-Bianchet 2007). Therefore, in hunted
populations, nonlactating females likely suffer greater mor-
tality than lactating females. If this trend was strong, it could
select for a strategy of early primiparity and high maternal
investment each year, even at a cost of reduced longevity,
opposite to the conservative strategy normally favoured by
natural selection in long-lived species (Solberg et al. 2000;
Festa-Bianchet 2003; Proaktor, Coulson & Milner-Gulland
2007). Recent research on Norwegian red deer, however,
found no evidence that sport harvests led to earlier primipari-
ty, possibly because much of the harvest focussed on pre-
reproductive females and on males (Mysterud, Yoccoz &
Langvatn 2009).
The harvest (Fig. 4) of many old animals in both CN4 and
VCO2, compared to heavily harvested populations of other
species such as Norwegian moose (Alces alces Linnaeus)
(Mysterud, Solberg & Yoccoz 2005), suggests a relatively
weak hunting pressure, as older females are rare in heavily
hunted populations (Langvatn & Loison 1999; Solberg et al.
2000; Festa-Bianchet 2003). It may also indicate hunter selec-
tivity for old females that have long horns and are unlikely to
be lactating (Figs 1 and 3). The scarcity of senescent females
captured in the Park could be partly because of a tendency to
avoid females that appear very old, as younger females are
more useful for reintroduction. We suggest, however, that
wardens capturing live females in the Park were more likely
to obtain a random sample of the population than hunters in
autumn. Although wardens may have avoided females that
appeared frail or very small, they were not influenced by lac-
tation status because captures were done before females gave
birth.
Because of their low reproductive value, high harvest mor-
tality of old nonlactating females is unlikely to have strong
ecological or evolutionary consequences (Festa-Bianchet
2003). Strong hunter selection for nonlactating females in
VCO2, however, increased the mortality of 2-year-old
females (Fig. 4), an age class with a very high residual repro-
ductive value (Gaillard et al. 2000a). Hunting regulations
Early horn growth 445
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of AnimalEcology,80,438–447
discouraging the harvest of lactating females seek to reduce
the impact of female harvests on population growth, partly
based on the assumption that if a lactating female is har-
vested her kid would likely die. Our results suggest instead
that this regulation may increase the impact of female har-
vests in comparison with a random harvest of lactating and
nonlactating females. Because most 2-year-old females are
nonlactating, they suffer a disproportionately heavy harvest
pressure. Hunters harvest young females with a very high
probability to survive to the following year, when they will
begin their productive lifespan.
Conclusion
Our research highlights the fundamental importance of early
development on reproductive performance in mammals, not
only for young adults (Descamps et al. 2008; Pistorius et al.
2008; Hamel et al. 2009b) but also during senescence (Be
´r-
ube
´, Festa-Bianchet & Jorgenson 1999; Nussey et al. 2007).
We found no evidence that early development affected hunter
selectivity. Although some types of selective hunting can lead
to evolutionary pressures on morphological traits (Coltman
et al. 2003; Garel et al. 2007), not all forms of sport hunting
should be expected to have evolutionary impacts. Hunter
selectivity can vary according to many factors (Martinez
et al. 2005; Mysterud, Trjanowski & Panek 2006), and some
sport harvests may not be selective (Bischof et al. 2009).
Sport harvest did not appear to have strong impacts on the
evolution of phenotypic traits and reproductive strategies of
female chamois, likely because of a low harvest rate and weak
selection for long-horned females. Our research points to two
avenues for further investigation on the effects of regulations
that protect lactating females. First, the high hunting mortal-
ity of nonlactating females creates a fitness cost of nonrepro-
duction and may favour a higher lactation rate (Proaktor,
Coulson & Milner-Gulland 2007). Second, the high mortality
of pre-reproductive females may decrease population growth
more than alternative strategies of female harvest.
Acknowledgements
Funding was provided by the Piemonte Region, the Alpi Marittime Natural
Park and the Natural Sciences and Engineering Research Council of Canada.
We thank the Park Rangers for logistic support and help with fieldwork.
Special thanks are extended to Giuseppe Canavese for his support of our
research and to the managers of the Comprensorio Alpino Cuneo 4 and
Verbano Cusio-Ossola 2 for their collaboration in collecting data. An earlier
draft of the manuscript benefited from critical comments by S. Hamel and
F. Pelletier. Special thanks to J. Martin for help in statisticalanalysis.
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