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Seasonal patterns of climate and vegetation growth are expected to be altered by global warming. In alpine environments, the reproduction of birds and mammals is tightly linked to seasonality; therefore such alterations may have strong repercussions on recruitment. We used the normalized difference vegetation index (NDVI), a satellite-based measurement that correlates strongly with aboveground net primary productivity, to explore how annual variations in the timing of vegetation onset and in the rate of change in primary production during green-up affected juvenile growth and survival of bighorn sheep (Ovis canadensis), Alpine ibex (Capra ibex), and mountain goats (Oreamnos americanus) in four different populations in two continents. We indexed timing of onset of vegetation growth by the integrated NDVI (INDVI) in May. The rate of change in primary production during green-up (early May to early July) was estimated as (1) the maximal slope between any two successive bimonthly NDVI values during this period and (2) the slope in NDVI between early May and early July. The maximal slope in NDVI was negatively correlated with lamb growth and survival in both populations of bighorn sheep, growth of mountain goat kids, and survival of Alpine ibex kids, but not with survival of mountain goat kids. There was no effect of INDVI in May and of the slope in NDVI between early May and early July on juvenile growth and survival for any species. Although rapid changes in NDVI during the green-up period could translate into higher plant productivity, they may also lead to a shorter period of availability of high-quality forage over a large spatial scale, decreasing the opportunity for mountain ungulates to exploit high-quality forage. Our results suggest that attempts to forecast how warmer winters and springs will affect animal population dynamics and life histories in alpine environments should consider factors influencing the rate of changes in primary production during green-up and the timing of vegetation onset.
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Ecology, 88(2), 2007, pp. 381–390
Ó2007 by the Ecological Society of America
EARLY ONSET OF VEGETATION GROWTH VS. RAPID GREEN-UP:
IMPACTS ON JUVENILE MOUNTAIN UNGULATES
NATHALIE PETTORELLI,
1
FANIE PELLETIER,
2,3
ACHAZ VON HARDENBERG,
4
MARCO FESTA-BIANCHET,
2
AND STEEVE D. CO
ˆTE
´
1,5
1
De
´partement de Biologie and Centre d’e
´tudes nordiques, Universite
´Laval, Que
´bec G1K 7P4 Canada
2
De
´partement de Biologie, Universite
´de Sherbrooke, 2500 Boul. de l’Universite
´, Sherbrooke, QC J1K 2R1 Canada
3
Division of Biology, Faculty of Life Sciences, Imperial College London, Silwood Park, Ascot, Berkshire SL5 7PY UK
4
Alpine Wildlife Research Centre, Parco Nazionale Gran Paradiso, via della Rocca 47, 10123 Torino, Italy
Abstract. Seasonal patterns of climate and vegetation growth are expected to be altered
by global warming. In alpine environments, the reproduction of birds and mammals is tightly
linked to seasonality; therefore such alterations may have strong repercussions on recruitment.
We used the normalized difference vegetation index (NDVI), a satellite-based measurement
that correlates strongly with aboveground net primary productivity, to explore how annual
variations in the timing of vegetation onset and in the rate of change in primary production
during green-up affected juvenile growth and survival of bighorn sheep (Ovis canadensis),
Alpine ibex (Capra ibex), and mountain goats (Oreamnos americanus) in four different
populations in two continents. We indexed timing of onset of vegetation growth by the
integrated NDVI (INDVI) in May. The rate of change in primary production during green-up
(early May to early July) was estimated as (1) the maximal slope between any two successive
bimonthly NDVI values during this period and (2) the slope in NDVI between early May and
early July. The maximal slope in NDVI was negatively correlated with lamb growth and
survival in both populations of bighorn sheep, growth of mountain goat kids, and survival of
Alpine ibex kids, but not with survival of mountain goat kids. There was no effect of INDVI
in May and of the slope in NDVI between early May and early July on juvenile growth and
survival for any species. Although rapid changes in NDVI during the green-up period could
translate into higher plant productivity, they may also lead to a shorter period of availability
of high-quality forage over a large spatial scale, decreasing the opportunity for mountain
ungulates to exploit high-quality forage. Our results suggest that attempts to forecast how
warmer winters and springs will affect animal population dynamics and life histories in alpine
environments should consider factors influencing the rate of changes in primary production
during green-up and the timing of vegetation onset.
Key words: body mass; green-up; NDVI; plant phenology; population dynamics; resource–animal
interactions; survival.
INTRODUCTION
Predicting the effects of global warming on organisms
of different ecosystems is a major challenge for
ecologists (Walther et al. 2002). In recent decades,
climate change has affected many biological systems
(Crick and Sparks 1999, Post and Stenseth 1999, Inouye
et al. 2000), and much effort is devoted to understand
the consequences of such changes (Hughes 2000, Hulme
2005). Global climate change is altering seasonal
patterns: for example, the average start of the growing
season shifted by eight days from 1989 to 1998 in
Europe (Chmielewski and Ro
¨tzer 2002) and by 5–6 days
from 1959 to 1993 in North America (Schwartz and
Reiter 2000). The life history strategies of species
experiencing seasonal environments have been selected
to match the best environmental conditions. With
seasonal patterns altered, however, the reproduction of
these species may become out of phase with the period
of highest environmental productivity (Thomas et al.
2001, Berteaux et al. 2004). The ultimate consequences
of the timing of birth are expected to depend to a large
extent on the phenology of organisms at other trophic
levels (Visser et al. 2004). In seasonal environments,
large herbivores typically give birth in late spring or
early summer to match the vegetation green-up period
and allow offspring to benefit from the entire vegetation
growing season (Rutberg 1987). By shifting plant
phenology toward an earlier vegetation onset, global
warming could affect juvenile growth and survival of
many species (Inouye et al. 2000, Visser et al. 2004,
Pettorelli et al. 2005a, c). Highly seasonal environments
such as those in arctic or alpine areas are expected to be
strongly affected by climate change (Oechel et al. 1997).
There is much interest in the influence of global
warming in mountainous regions (Diaz and Bradley
Manuscript received 25 May 2006; revised 3 August 2006;
accepted 24 August 2006. Corresponding Editor: C. M.
Herrera.
5
Corresponding author. E-mail: steeve.cote@bio.ulaval.ca
381
1997), where warmer winters are expected to change the
rain/snow ratio. In northern mountains, climate change
may lead to more winter precipitation, resulting in
deeper snowpack at high elevations (Inouye et al. 2000,
Mysterud et al. 2001, Pettorelli et al. 2005a). Increas-
ingly warm winters, however, may augment winter rain
and run-off at the expense of snowpack, as the
rain/snow boundary moves higher in elevation (Beniston
and Fox 1996, Lapp et al. 2005).
The timing of snowmelt should determine the timing
of spring vegetation onset and thereby affect life
histories of alpine ungulates (Rutberg 1987, Kudo
1991). Because plant phenology is the major factor
affecting forage quality (Laycock and Price 1970), it is
frequently described as the driving force in habitat use
by vertebrate herbivores (Fryxell 1991, Albon and
Langvatn 1992). Both plant crude protein content and
digestibility peak early in the growing season, and then
rapidly decline as the vegetation matures: higher forage
quality is thus associated with early phenological stages
where new green leaves dominate biomass (Crawley
1983). Feeding patch choice and forage selection by
ungulates are positively associated with plant quality
(White 1983, Wilmshurst et al. 1995). A shorter period
when high-quality forage is available should thus lower
herbivore performance (Albon and Langvatn 1992,
Langvatn et al. 1996). Because forage quality peaks
during early phenological stages, slow vegetation
growth should prolong access to high-quality forage.
Moreover, spatial heterogeneity in snowmelt may lead
to spatial heterogeneity in the timing of vegetation
green-up onset, which may lengthen the period when
high-quality forage is accessible to herbivores (Mysterud
et al. 2001, Pettorelli et al. 2005a). Rapid temporal
changes in plant productivity might thus correlate both
with fast vegetation growth and reduced spatial
heterogeneity in timing of vegetation onset in alpine
areas, shortening the period of access to high-quality
forage for herbivores.
Many studies have focused on the impact of an early
start of vegetation growth on herbivore performance
(e.g., Portier et al. 1998, Coˆ te
´and Festa-Bianchet 2001a,
Griffith et al. 2002). Few, however, have attempted to
partition the effect of an early start of vegetation growth
from that of a rapid rate of changes in vegetation
phenology, possibly leading to a shorter period of access
to high-quality forage. Here we assess the effects of
annual variations in the timing of vegetation green-up
onset and the rate of change in plant productivity during
green-up on the growth and survival of juvenile
mountain ungulates in North America and Europe.
We indexed vegetation dynamics by the normalized
difference vegetation index (NDVI), a satellite-based
measurement that correlates strongly with aboveground
net primary productivity (Pettorelli et al. 2005b).
Previous studies generally considered climatic variables
as proxies for plant phenology (Portier et al. 1998, Toı
¨go
et al. 1999). The links between weather and vegetation
phenology, however, are complex, involving a number
of climatic variables and depending on location, while
the link between primary productivity and NDVI is
direct and has been shown to be linear, robust,
consistent, and strong in temperate areas (Pettorelli et
al. 2005b). We considered three species of mountain
ungulates: bighorn sheep Ovis canadensis, Alpine ibex
Capra ibex, and mountain goat Oreamnos americanus in
four populations. These species have broadly similar
habitat use, social organization, foraging behavior,
sexual size dimorphism, fertility, and body mass
(Festa-Bianchet 1988a, Festa-Bianchet et al. 1997, Toı
¨go
et al. 1999, Coˆ te
´and Festa-Bianchet 2003). Because
juveniles are the age class most likely to be affected by
both extrinsic and density-dependent processes in
ungulates (Gaillard et al. 2000), we focused on the
relationships between vegetation phenology and juvenile
growth and survival.
Early vegetation onsets positively affect the perfor-
mance of ungulates inhabiting highly seasonal environ-
ments (Giacometti et al. 2002, Pettorelli et al. 2005c). We
consequently expected (H
1
, hypothesis 1) a positive
effect of early vegetation onsets on juvenile growth and
survival. Rapid changes in plant productivity during
green-up should be associated with a reduced period of
access to high-quality forage, either through rapid
vegetation growth or reduced spatial heterogeneity in
the timing of the vegetation onset. We therefore
expected that (H
2
, hypothesis 2) rapid changes in NDVI
during green-up would be negatively related to juvenile
survival and growth. Finally, we expected that late
vegetation onsets or rapid changes in plant productivity
would have stronger effects under harsh environmental
conditions such as at high population density (H
3
,
hypothesis 3).
MATERIALS AND METHODS
Study areas and sample collection
Ram Mountain (528N, 1158W; elevation, 1700–2200
m), Alberta, Canada, is an isolated mountain ;30 km
east of the main Canadian Rockies. The area used by
sheep (;38 km
2
) is characterized by alpine and
subalpine habitat. Each year, sheep are trapped from
the end of May to late September and weighed to within
125 g with a spring scale. All ewes have been marked
since 1976, and .80%of the lambs were caught in most
years. Here we considered the body mass of 332 lambs
weighed between 1982 (when NDVI measurements first
became available) and 2004. We also calculated the
proportion of marked lambs in September (n¼634) that
were reobserved as yearlings the following spring (end of
May) to estimate first-year overwinter survival (see
Festa-Bianchet et al. 1997 for more details on field
methods).
The Sheep River bighorn sheep population (508N,
1148W) is also in Alberta, 160 km south of Ram
Mountain. In winter, the population uses a low-
elevation range (1450–1700 m) in the eastern slopes of
NATHALIE PETTORELLI ET AL.382 Ecology, Vol. 88, No. 2
the Rocky Mountains. In spring, ewes migrate to higher
elevation (1800–2250 m) ;12–15 km west of the winter
range (Festa-Bianchet 1988a). The winter range (14 km
2
)
is characterized by grassy meadows interspersed with
aspen (Populus tremuloides) copses, while the summer
range (;50 km
2
) consists of alpine and subalpine
habitat. Since 1981, .95%of the sheep have been
marked (Festa-Bianchet 1988a, b). Each autumn, lambs
aged 4–6 months are immobilized with a dart gun and
their chest girth is measured. Chest girth is highly
correlated with lamb mass (r¼0.90, Pelletier et al. 2005).
We considered the mean chest girth adjusted for capture
date, per year and per sex, of 428 lambs born between
1982 and 2004. To estimate lamb overwinter survival, we
considered the proportion of lambs marked in Septem-
ber–November (n¼464) that were reobserved as
yearlings the following spring (end of April–May).
Caw Ridge is located in the Rocky Mountains of
west-central Alberta (548N, 1198W). Mountain goats
use ;28 km
2
of alpine tundra and open subalpine forests
from 1750 to 2185 m (Coˆ te
´and Festa-Bianchet 2001a).
Since 1989, the population has fluctuated from 76 to 147
individuals. We considered the sex-specific average mass
of 137 kids weighed between late May and early October
in 1989–2004. No kids were weighed in 1998–2000. We
used the proportion of kids in September (n¼349) that
were reobserved as yearlings the following spring (end of
May–June) to estimate kid overwinter survival, from
1989 to 2004.
The Gran Paradiso National Park (GPNP hereafter)
in northwestern Italy (458N, 78E) is composed entirely
of mountainous terrain. Alpine pastures, moraines,
cliffs, glaciers, and rock account for 59%of its 720
km
2
. Ibex use elevations ranging from ;800 m to
beyond the upper limit of vegetation at ;3200 m. Yearly
autumn counts are conducted in the entire park by ;30
park wardens over two consecutive days in September,
when the number of kids, yearlings, and adult males and
females are determined (Jacobson et al. 2004). We used
the proportion of kids that were seen as yearlings the
following autumn to estimate first-year overwinter
survival in 1982–2004 (number of yearlings in year
t/number of kids in year t1). Because censuses are
done in September, juvenile survival in the GPNP was
from 4 to 16 months of age. Estimates of survival based
on population counts are subject to biases, and their
quality is far lower than estimates based on marked
individuals (Gaillard et al. 2000). However, those biases
should not vary from year to year, making the
comparison of vegetation phenology and survival
estimates possible in GPNP.
Weather data
Alberta.—Data on snowfall (in centimeters), precipi-
tation in water equivalent (in millimeters) and average
temperature (in degrees Celsius) in April and May were
obtained from the Environment Canada meteorological
stations near the study sites (Grande Cache [1255 m] for
Caw Ridge, Nordegg [1326 m] for Ram Mountain, High
River [1219 m] for Sheep River). Those data were
available from 1988 to 2004 for Caw Ridge, and from
1982 to 2004 for Sheep River and Ram Mountain.
GPNP.—Data on snow depth (in centimeters), rain
(in millimeters), and average temperature (in degrees
Celsius) in April and May were obtained from the Serru`
meteorological Station (Azienda Elettrica Municipal-
izzata Torino) located inside the GPNP at an elevation
of 2240 m (1982–2004). The average temperature was
defined as (average maximal temperature þaverage
minimal temperature)/2.
NDVI data
Data collected by the National Oceanic and Atmo-
spheric Administration satellites and processed by the
GIMMS group (Tucker et al. 2005) are available. From
these, NDVI values have been produced from visible
and near-infrared reflectance measurements (NDVI ¼
[NIR VIS]/[NIR þVIS], where NIR is the near
infrared light reflected by the vegetation, and VIS is the
visible light reflected by the vegetation). We used the
best available corrected NDVI time series for the
number of years considered. The spatial scale of
resolution (pixel size) for that series is 64 km
2
and an
NDVI value is available on a bimonthly basis, from
July 1981 to now (Pettorelli et al. 2005b). Bimonthly
NDVI values are based on 15-d temporal composites
(maximum value compositing) to reduce cloud contam-
ination problems (Pettorelli et al. 2005b). We used
NDVI averages from one pixel for Ram Mountain,
eight pixels for Sheep River, five pixels for Caw Ridge,
and 11 pixels for the GPNP. For Ram Mountain, we
thus used the minimum possible scale, i.e., 64 km
2
. For
the other study areas, we used the total spatial range of
the populations, covering areas likely much larger than
those actually used by the study populations. We used
the minimum number of pixels possible considering the
shape of the study areas and their overlap with NDVI
pixels. We thus traded spatial resolution for data
quality, assuming that the annual phenological signal
captured at the scale of the GIMMS data would be
correlated with vegetation productivity in the different
study sites. We could not, however, test this assump-
tion, because there are no data on the phenology of
forage available for our study sites.
We used NDVI measurements around the mean date
of green-up to distinguish early from late annual onsets
of vegetation growth. The timing of the onset of
vegetation growth was thus indexed using the sum of
the two bimonthly NDVI values in May (vegetation
growth typically starts in May in all study sites; see Fig.
1a), an index that correlates with vegetation biomass
(integrated NDVI [INDVI], Pettorelli et al. 2005b). The
rate of change in plant productivity during green-up,
when indexed using NDVI, is defined as the rate of
increase between two fixed dates (generally between the
estimated date when vegetation starts growing and the
February 2007 383PLANT PHENOLOGY AND ALPINE UNGULATES
estimated date when vegetation biomass reaches a
plateau; Pettorelli et al. 2005b). Because for all sites
vegetation growth reaches a plateau in July (Fig. 1a),
we considered the slope between early May and early
July as an index of the rate of vegetation changes
during green-up. This last index, however, does not
capture any deviation from a linear increase in NDVI
between those two dates and smooths the rate of change
during green-up. For example, a linear and a logarith-
mic increase between the two dates would provide the
same slope. We therefore also indexed the rate of
vegetation changes during green-up as the maximal
slope between any two consecutive bimonthly NDVI
values from early May to early July (Reed et al. 1994,
Kaduk and Heinmann 1996, Fig. 1b). Higher maximal
increases indicate faster changes in vegetation growth
and higher deviations from a linear increase in NDVI
during green-up.
FIG. 1. (a) Average normalized difference vegetation index (NDVI) values (1982–2004) in four study areas: Ram Mountain
(Alberta), Sheep River (Alberta), Caw Ridge (Alberta), and Gran Paradiso National Park (GPNP, Italy). (b) Illustration of the
concept of the maximal increase in NDVI. We present two years (1984 and 1997) in the Gran Paradiso National Park exhibiting
contrasted vegetation dynamics. The x-axis represents each NDVI picture available (two per month, for a total of 24 pictures per
year), ranging from 1 to 24 and starting on 1 January. The period considered in the analyses extended from early May to early July.
In both years (1984 and 1997), the maximal increase in NDVI occurred between 1–15 May and 15–30 May; however the rate of
increase between these two periods in 1997 was double that in 1984.
NATHALIE PETTORELLI ET AL.384 Ecology, Vol. 88, No. 2
Analyses
We expected climatic conditions in April/May to
determine the average and maximal rate of changes in
primary productivity during green-up. Precipitation was
transformed as ‘‘log(precipitation þ4)’’ to stabilize the
variance (Pettorelli et al. 2005a). Because there were no a
priori reasons to believe that different relationships
between climate and phenology should be expected
between Ram Mountain, Sheep River, and Caw Ridge,
climatic data for Alberta were pooled and study site was
considered as a factor. Because temperature and
snowfall in April were correlated in Alberta (R
2
¼
0.11, slope ¼0.05 60.02, mean 6SE, P¼0.01), we
considered the residuals of this regression as an index of
snowfall in April when analyzing the relationships
between phenological measures and weather data.
As lamb chest girth and body mass increased during
the period of capture, both parameters were adjusted
(girth at Sheep River to 20 November; body mass at
Ram Mountain to 15 September; Festa-Bianchet et al.
1997, Pelletier et al. 2005) before determining the yearly
sex-specific means. At Caw Ridge, kid body mass was
adjusted to 30 July (the mean date of capture for the 137
kids considered) using the slope of the linear regression
between mass and date without distinction for sex (Coˆ te
´
and Festa-Bianchet 2001a), before determining the
yearly sex-specific means. Mass and chest girth were
ln-transformed to stabilize the variance (Sokal and
Rohlf 1995). Using linear models weighted for yearly
sample size, we explored the linear and quadratic
relationships between NDVI measures and the chest
girth or body mass of juveniles.
The annual proportion of juveniles that survived the
winter was arcsine square-root transformed (Sokal and
Rohlf 1995). First-year winter survival is not sex-biased
(Festa-Bianchet et al. 1997, Coˆ te
´and Festa-Bianchet
2001a). Lamb survival at Sheep River and Ram
Mountain was affected by cougar (Puma concolor)
predation episodes (Sheep River: one from 1993 to
1995, and one from 1999 to 2004; Ram Mountain: one
from 1997 to 2003; Festa-Bianchet et al. 2006) and a
pneumonia epizootic in Sheep River (1985–1986; Festa-
Bianchet 1988a). To account for such effects, we used a
dummy variable (0/1, with 1 coding for cougar
predation or the occurrence of the epizootic). Using
linear models on arcsine square-root transformed
proportions, we then explored the linear and quadratic
relationships between NDVI measures and survival.
Because density-dependent responses were expected at
Ram Mountain and the GPNP (Portier et al. 1998,
Jacobson et al. 2004), we took into account population
density while modeling the effect of NDVI on body mass
and first-year survival. Density at Ram Mountain was
indexed as the ln-transformed average body mass of
yearling females in June, an index of resource availabil-
ity (Coltman et al. 2003, Festa-Bianchet et al. 2004).
Because the yearly maximal increase in NDVI at time t
correlated with this index of density at time t(R
2
¼0.21,
slope ¼0.63 60.27, P¼0.03), we used the residuals of
this regression to account for changes in density.
Density in the GPNP was indexed using yearly total
population counts (Jacobson et al. 2004). There was no
correlation between this index of density and the yearly
maximum increase in NDVI at the GPNP.
In three out of the four populations, several factors
have been described to influence juvenile survival and
growth such as birth date and age or condition of the
mother (Festa-Bianchet 1988b, Festa-Bianchet et al.
2000, Coˆ te
´and Festa-Bianchet 2001a, b, Gendreau et al.
2005). Here we used yearly averages because we were
interested in the impact of annual variations in
phenology on annual average performance. We also
wanted to explore whether similar patterns could be
observed in Canada and in Europe, in the GPNP, where
individual data are not available.
Model selection was performed using Akaike’s
Information Criterion corrected for small sample sizes
(AIC
c
; Burnham and Anderson 1998). All continuous
variables were standardized when checking for interac-
tions between them. Temporal autocorrelation among
residuals was checked, and was not significant for all
comparisons. All statistical analyses were performed in
the statistical package R (available online).
6
RESULTS
Phenology and local climate
Indicators of warm and wet springs influenced
vegetation phenology as assessed by NDVI in our study
sites. In Alberta (Appendix: Table A1), warmer springs
tended to be associated with rapid changes in plant
productivity: temperatures in April (slope ¼0.006 6
0.003, P¼0.08) and precipitation in May (slope ¼0.03
60.02, P¼0.06) tended to affect positively maximal
increases in NDVI. On the other hand, low snowfall in
April (slope ¼0.11 60.06, P¼0.05) and high
precipitation in May (slope ¼0.14 60.04, P¼0.002)
favored high INDVI values in May. Neither tempera-
ture in April nor snowfall in April or precipitation in
May was significantly related to the average slope of
NDVI from early May to early July (all P.0.13;
Appendix: Table A1). In the GPNP (Appendix: Table
A2), both high temperatures in May and low snow depth
in April appeared to favor both the INDVI in May
(suggesting early onset of vegetation growth) and the
maximum increase in NDVI (suggesting rapid changes
in plant productivity), but these relationships were
nonsignificant (all P.0.09).
Vegetation dynamics and early performance
Contrary to our first hypothesis (H
1
), high INDVI in
May did not influence the growth of bighorn lambs at
Sheep River or mountain goat kids at Caw Ridge (Table
1; Appendix: Table A3; all P.0.77). At Ram
6
hwww.r-project.orgi
February 2007 385PLANT PHENOLOGY AND ALPINE UNGULATES
Mountain, however, INDVI in May tended to negative-
ly affect lamb mass in mid-September (slope ¼0.19 6
0.11, P¼0.08, Table 1; Appendix: Table A3). We found
no effect in any study area of INDVI in May on first-
year overwinter survival (Table 2; Appendix: Table A4;
all P.0.17).
As expected (H
2
), rapid changes in plant productivity
during green-up negatively influenced the growth of
lambs and kids of both sexes at Ram Mountain, Sheep
River, and Caw Ridge (Table 1, Fig. 2a–c; Appendix:
Table A3). At Sheep River, the yearly average chest
girth differed by up to 2.9 cm for males (3.6%of average
male chest girth) between years with low and high
maximal increases in NDVI, while the yearly average
mass of lambs at Ram Mountain varied by as much as
3.06 kg for males (;11.2%of the average). At Caw
Ridge, yearly average kid mass differed by up to 2.5 kg
for males (15.5%of the average) between years with low
and high maximal increases in NDVI. Similar results
were obtained for female lambs and kids.
The negative effect of the maximal increase in NDVI
on lamb growth was followed by a similar negative effect
on first-year overwinter survival at Ram Mountain and
TABLE 1. Parameter estimates from linear models weighted for
sample sizes for the mean chest girth of bighorn lambs at
Sheep River and the body mass of bighorn lambs at Ram
Mountain and mountain goat kids at Caw Ridge.
Parameter LSM SE TP
A) Sheep River
Intercept 4.43 0.02 317.76 ,0.001
(Females males) 0.04 0.007 5.41 ,0.001
Max. inc. 0.37 0.10 3.50 0.001
B) Ram Mountain
Intercept 3.41 0.04 82.43 ,0.001
(Females males) 0.09 0.02 3.85 ,0.001
Res(BMY) 0.79 0.16 4.81 ,0.001
Max. inc. 0.48 0.17 2.86 0.006
C) Caw Ridge
Intercept 3.03 0.13 23.76 ,0.001
(Females males) 0.07 0.04 1.67 0.11
Max. inc. 1.70 0.82 2.08 0.05
Notes: Model selection procedures are presented in the
Appendix (Table A3). ‘‘Res(BMY)’’ is the residual from the
linear relationship between the maximum increase in NDVI and
the average body mass of yearling females, indexing resource
availability; ‘‘Max. inc.’’ is the maximum increase in NDVI
during green-up.
TABLE 2. Parameter estimates for overwinter survival of
juvenile ungulates at (a) Ram Mountain, (b) Sheep River,
(c) Caw Ridge, and (d) the GPNP, Italy.
Parameter LSM SE TP
A) Ram Mountain
Intercept 1.22 0.14 8.45 ,0.001
Res(BMY) 1.56 0.53 2.94 0.008
Max. inc. 1.64 0.65 2.51 0.02
B) Sheep River
Intercept 1.31 0.17 7.67 ,0.001
Predation 0.27 0.08 3.29 0.004
Max. inc. 2.62 1.36 1.92 0.07
C) Caw Ridge
Intercept 1.07 0.04 26.95 ,0.001
D) Gran Paradiso National Park
Intercept 1.07 0.10 10.63 ,0.001
Max. inc. 2.34 0.73 3.19 0.004
Notes: Model selection procedures are presented in the
Appendix (Table A4). ‘‘Predation’’ is a dummy variable (0,
absence of heavy predation or pneumonia epizootic; 1, heavy
predation or pneumonia); ‘‘Res(BMY)’’ is the residual from the
linear relationship linking the maximum increase in NDVI and
the average body mass of yearling females, indexing resource
availability; ‘‘Max. inc.’’ is the maximum increase in NDVI
during green-up.
FIG. 2. (a) Log-transformed mean body mass (measured in
kg) adjusted for density of male and female bighorn lambs at
Ram Mountain (Alberta) according to the maximal increase in
NDVI. (b) Mean chest girth for male and female bighorn lambs
according to the maximal increase in NDVI at Sheep River
(Alberta). (c) Log-transformed mean body mass (measured in
kg) of male and female mountain goat kids at Caw Ridge
(Alberta) according to the maximal increase in NDVI.
NATHALIE PETTORELLI ET AL.386 Ecology, Vol. 88, No. 2
the GPNP (Table 2, Fig. 3; Appendix: Table A4). The
annual maximal increase in NDVI explained 18%of the
variability in the average first-year overwinter survival
of lambs at Ram Mountain and 33%for kids in the
GPNP. At Sheep River, the effect was in the same
direction and approached significance (slope ¼2.62 6
1.36, P¼0.07). At Caw Ridge, however, the maximal
increase in NDVI was not related to kid survival (Table
2; Appendix, Table A4). The slope in NDVI between
early May and early July did not affect juvenile growth
or survival in any populations (all P.0.10).
Although population density negatively affected
growth and survival of lambs at Ram Mountain (Tables
1 and 2), contrary to (H
3
), density did not interact
significantly with INDVI in May, the NDVI slope
between early May and early July, or the maximal
increase in NDVI in affecting body mass or survival of
juveniles at Ram Mountain or in the GPNP (Appendix:
Tables A3 and A4).
DISCUSSION
As expected, we found a negative effect of rapid
changes in plant productivity during green-up on
juvenile growth in three alpine ungulate populations.
Reduced growth presumably led to a negative effect of
rapid changes in plant productivity on juvenile survival
(Gaillard et al. 1997). However, we found no positive
effect on juvenile growth and survival of either early
vegetation onset as indexed by INDVI in May or
negative effect of steep vegetation onset as indexed by
the slope between NDVI in early May and early July. In
populations where density dependence was previously
reported (Portier et al. 1998, Jacobson et al. 2004), we
did not find any interaction between INDVI in May or
high maximal increase in NDVI and population density
in determining growth or overwinter juvenile survival.
The reported patterns were coherent among the four
populations, three species, and two continents consid-
ered.
The duration of the vegetation growing period when
herbivores can access high-quality forage appears
mainly constrained by spring weather (Pettorelli et al.
2005a). Topographic variability in alpine habitats, on
both meso- and micro-scales, and associated differences
in snowmelt, can result in swards of different phenolog-
ical stages in close proximity, generating spatially
heterogeneous vegetation (Kudo 1991). Warm temper-
atures in spring may reduce this spatial heterogeneity if
they generate rapid snowmelt over the landscape,
reducing the period during which herbivores can access
high-quality forage. Warm temperatures and high
moisture favor rapid plant growth (Defila 1991), which
also shortens the period of high forage quality (Hay and
Heide 1984). In Alberta, we found a positive association
between warm springs and high values of the maximal
increase in NDVI, which allowed us to establish a link
between warm springs and rapid changes in plant
productivity during green-up. Snowfall in April was
positively correlated with the maximum increase in
NDVI but had negative effects on INDVI in May.
Because the timing of snowmelt is the main determinant
of vegetation onset in mountainous environments (Kudo
1991), the negative relationship between INDVI in May
and April snowfall was expected. Water from abundant
snowfall in April and heavy precipitation in May,
associated with warm temperatures in April/May, may
lead to a vegetation bloom and fast changes in plant
productivity.
FIG. 3. Winter survival of juveniles according to the maximal increase in NDVI at Ram Mountain (bighorn sheep, Alberta),
Sheep River (bighorn sheep, Alberta), Caw Ridge (mountain goats, Alberta), and the GPNP (ibex, Italy). Survival was adjusted for
density at Ram Mountain and for predation or pneumonia epizootic at Sheep River.
February 2007 387PLANT PHENOLOGY AND ALPINE UNGULATES
Nutritional requirements of animals vary with their
physiological state. For ungulate females, nutritional
demand peaks in late gestation and during lactation
(Clutton-Brock et al. 1989). The daily energetic require-
ment may increase by 150%during peak lactation
compared to maintenance (Loudon 1985). In highly
seasonal environments such as alpine habitats, spring
forage conditions can thus have profound effects on the
energy balance during late gestation and lactation.
Much emphasis has been placed on the importance for
herbivores inhabiting seasonal environments to match
vegetation green-up and birth period to access the
longest possible vegetation growing period (Bunnell
1982, Rutberg 1987). Females with access to high-
quality forage during lactation could provide greater
maternal care than females on a low nutritional plane
and reach sufficient body condition in autumn to
conceive again. Offspring should benefit from greater
maternal care by maximizing growth and overwinter
survival. Indeed, late-born offspring are more likely to
die during winter since they are smaller in autumn
(Festa-Bianchet 1988b). Early vegetation onset mea-
sured by INDVI in May, however, did not affect
juvenile growth or survival in our study.
Contrary to the timing of vegetation onset, little
attention has been paid to the role of the rate of change
in plant productivity during green-up and the possible
variation in the duration of the period of access to high-
quality forage in determining performance of herbivores
(but see Langvatn et al. 1996, Mysterud et al. 2001,
Pettorelli et al. 2005a). Here, we underlined the
relevance of indexing the rate of changes in plant
productivity during green-up using the maximum rate of
change in NDVI, and highlighted the sensitivity of
alpine ungulates to the shape of the vegetation
phenology curve. The only exception was in mountain
goats, where overwinter survival was not related to
vegetation dynamics indexed by NDVI. A previous
study at Caw Ridge reported that fecal crude protein
content in June, an index of forage quality, affected
positively kid mass, but not kid survival (Coˆ te
´and
Festa-Bianchet 2001a). The absence of an effect of fecal
crude protein on survival could be due to an effect on
growth that was not sufficient to lead to a higher
juvenile mortality (Gaillard et al. 1997), consistent with
the results presented here.
The slope between NDVI values in early May and
early July, which describes the steepness of the entire
green-up period, did not correlate with spring weather
or juvenile performance. The rate of changes in plant
productivity during green-up in a particular year would
always be smoothed when considering the slope between
two fixed dates. Therefore, the slope between NDVI
values in early May and early July was less likely than
the maximal increase in NDVI to measure rapid changes
in vegetation productivity influencing the period of
access to high-quality forage by herbivores.
Surprisingly, we did not find any interaction between
density and the maximal increase in NDVI in determin-
ing early growth or survival of alpine ungulates in sites
where density dependence was previously reported. The
interaction of density dependence and climate affects the
early performance of ungulates (e.g., Gaillard et al.
1997, Portier et al. 1998). The absence of interaction in
our study could result from density variations that were
insufficient to exacerbate the effects of rapid changes in
plant productivity during the green-up on early perfor-
mance.
In all study sites, NDVI was assessed at a scale that
was generally higher than the areas used by animals. We
believe that the phenological signal captured at such
large scale is likely to be coherent with vegetation
phenology in the study sites, but it is possible that NDVI
data at a smaller spatial resolution could enhance the
signal we already captured.
Rapid changes in plant productivity during green-up
decreased juvenile performance in all study sites. We
suggest that rapid changes in NDVI during green-up
reduce the period of access to high-quality forage. This
could occur through a faster growth rate of plants, a
reduction in the spatial heterogeneity of snowmelt, or a
change in the plant community accessible to animals. To
test such hypotheses will require independent data on
the spatiotemporal availability and phenology of forage
over many years in the four study sites, data that are not
currently available. However, data on feeding sites of
female mountain goats during two years indicate that
vegetation quality, as measured by protein content of
plants in June, is high when the maximum increase in
NDVI is low (2003, proteins ¼20.1 60.5, maximum
NDVI increase ¼0.118) and low when the maximum
increase in NDVI is high (2002, proteins ¼17.3 60.6,
maximum NDVI increase ¼0.172; comparison of
protein content between years, F
1, 140
¼5.1, P¼0.02).
Further work is required to explain the interannual
variability in the maximal increase in NDVI and to
understand the mechanisms by which rapid changes in
plant productivity (as reflected by NDVI) during the
green-up affect early performance. Considering its
importance in determining growth and survival in all
four populations measured, those studies are critically
needed.
Since we were unable to highlight any consistent effect
of INDVI in May, our results point toward the greater
influence of a measure of the average duration of the
period of access to high-quality forage such as maximal
increase in NDVI, than a measure of the average timing
of vegetation onset (INDVI in May), in determining
growth and survival of juvenile alpine ungulates.
Previous work had shown that in Norway warmer
winters could lead to higher snowfalls and delayed
vegetation onsets at high altitudes, affecting negatively
reindeer performance (Pettorelli et al. 2005c). Our
results highlight another mechanism that could become
more frequent with global climate change (Lapp et al.
NATHALIE PETTORELLI ET AL.388 Ecology, Vol. 88, No. 2
2005): warmer springs could negatively affect alpine
ungulates through a shorter period of access to high-
quality forage. In two of our study areas, the annual
maximal increase in NDVI appeared to increase over
time (Appendix: Fig. A2), possibly reflecting a warming
trend. Finally, our study illustrates how satellite-based
information on vegetation can be useful in investigating
the coupling between vegetation and herbivore perfor-
mance, particularly in highly seasonal environments
where phenological signals are strong.
ACKNOWLEDGMENTS
We are grateful to the many people who helped with field
work. We thank J. Hogg, K. Smith, and J. Jorgenson for their
pivotal contribution to field research in the Alberta sites, and S.
Hamel for data on plant protein content from Caw Ridge.
Special thanks to J.-M. Gaillard, A. Mysterud, T. Coulson, A.
Provenzale, and J. Huot for ideas, comments, and suggestions
on previous drafts of this work. Research at Caw Ridge, Ram
Mountain, and Sheep River was financed by the Alberta Fish
and Wildlife Division, the Natural Sciences and Engineering
Research Council of Canada, the Rocky Mountain Goat
Foundation, the Alberta Conservation Association, the Alberta
Sport, Recreation, Parks and Wildlife Foundation, the Fonds
Que
´becois pour la formation de Chercheurs et l’Aide a
`la
Recherche, the Universite
´de Sherbrooke, and Universite
´Laval.
We are thankful to A. E. M. Torino for providing the weather
data from the Serru` Meteorological Station.
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APPENDIX
Tables showing climatic factors influencing the INDVI in May, the maximum NDVI increase, and the average slope of NDVI
between early May and early July in three study sites in Alberta; climatic factors influencing the INDVI in May, the maximum
NDVI increase, and the average slope in NDVI between early May and early July, and correlation coefficients between climatic
variables for the GPNP (Italy); and model selection procedures. Also included are figures showing interannual variations in NDVI
during the study periods and maximum increase in NDVI from 1982 to 2004 in four study sites in Alberta and Italy (Ecological
Archives E088-023-A1).
NATHALIE PETTORELLI ET AL.390 Ecology, Vol. 88, No. 2
... To describe the rate of vegetation green-up, we used the Theil-Sen approach (Fernandes and G. Leblanc, 2005;Theil, 1992) for estimating the rate of change in greenness values during spring. Previous studies have linked vegetation productivity increase during spring to forage quality for large herbivores (Hamel et al., 2009;Pettorelli et al., 2007). As a measure of snow-cover frequency, we divided the number of observations flagged as snow by the number of clear observations for each pixel. ...
... In total, our set of metrics included 14 variables (Table II-2), which we categorized into five groups of habitat metrics: (1) productivity (based on TC greenness), (2) phenology (based on variability in greenness), (3) openness (based on TC brightness), (4) moisture (based on TC wetness), and (5) snow cover. Food availability (Coops et al., 2008;Pettorelli et al., 2005) Phenology Interquartile and interdecile range of TC greenness based on all observations; Theil-Sen estimator for regression of TC greenness against day of year for start-ofseason (3) Food availability, forage quality (Hamel et al., 2009;Pettorelli et al., 2007) Openness Median TC brightness for start-of-season, peak-of-season, and end-of-season (3) Absence of protective cover, food availability (Carroll et al., 2001;Holbrook et al., 2017b) Moisture Median TC wetness for start-of-season, peak-of-season, and end-of-season (3) Forest type and structure, protective cover, vegetation and soil moisture (Cohen et al., 1995;Hansen et al., 2001;Roy and Ravan, 1996) Snow cover Frequency of snow cover (relative to number of clear observations) based on all observations, frequency of snow cover during start-of-season (2) Resource accessibility, movement, predation risk (Macander et al., 2015;Michaud et al., 2014) TOTAL 14 metrics ...
... Likewise, phenology metrics characterizing forage availability and quality were important predictors in our habitat models for red and roe deer. This is in line with previous studies demonstrating the effectiveness of satellite-derived phenology-information for characterizing ungulate habitat (Merkle et al., 2016;Pettorelli et al., 2007), and the finding that habitat selection by roe deer in our study area is largely driven by forage availability . Moreover, metrics calculated from start-of-season observations showed the largest relative importance in our models. ...
Thesis
Die zunehmende Verfügbarkeit von Satellitenfernerkundungs- und Wildtier-Telemetriedaten eröffnet neue Möglichkeiten für eine verbesserte Überwachung von Wildtierhabitaten durch Habitatmodelle, doch fehlt es häufig an geeigneten Ansätzen, um dieses Potenzial voll auszuschöpfen. Das übergeordnete Ziel dieser Arbeit bestand in der Konzipierung und Weiterentwicklung von Ansätzen zur Nutzung des Potenzials großer Satellitenbild- und Telemetriedatensätze in Habitatmodellen. Am Beispiel von drei großen Säugetierarten in Europa (Eurasischer Luchs, Rothirsch und Reh) wurden Ansätze entwickelt, um (1) Habitatmodelle mit dem umfangreichsten global und frei verfügbaren Satellitenbildarchiv der Landsat-Satelliten zu verknüpfen und (2) Wildtier-Telemetriedaten über Wildtierpopulationen hinweg in großflächigen Analysen der Habitateignung und -nutzung zu integrieren. Die Ergebnisse dieser Arbeit belegen das enorme Potenzial von Landsat-basierten Variablen als Prädiktoren in Habitatmodellen, die es ermöglichen von statischen Habitatbeschreibungen zu einem kontinuierlichen Monitoring von Habitatdynamiken über Raum und Zeit überzugehen. Die Ergebnisse meiner Forschung zeigen darüber hinaus, wie wichtig es ist, die Kontextabhängigkeit der Lebensraumnutzung von Wildtieren in Habitatmodellen zu berücksichtigen, insbesondere auch bei der Integration von Telemetriedatensätzen über Wildtierpopulationen hinweg. Die Ergebnisse dieser Dissertation liefern neue ökologische Erkenntnisse, welche zum Management und Schutz großer Säugetiere beitragen können. Darüber hinaus zeigt meine Forschung, dass eine bessere Integration von Satellitenbild- und Telemetriedaten eine neue Generation von Habitatmodellen möglich macht, welche genauere Analysen und ein besseres Verständnis von Lebensraumdynamiken erlaubt und so Bemühungen zum Schutz von Wildtieren unterstützen kann.
... One or more changes in phenophase duration may result in a specific phase not providing favorable conditions for herbivores seeking to maximize nutrition. For example, warmer springs can result in an earlier onset of plant growth, but also shorten the period of highest quality forage, resulting in reduced net energy gain and overall animal performance (Pettorelli et al 2007, Monteith et al 2015. Understanding the phenology of forage resources across multiple phases provides a comprehensive characterization of the current and future nutritional conditions under which herbivores are exposed. ...
... The graminoid functional group included all grasses, sedges, and rushes. (a) Green-up (peak nutritional quality of forage for ungulate herbivores; Pettorelli et al 2007) was classified as the onset of leaf greening, young leaves, and increased leaf size; (b) vegetative (peak forage biomass) was classified as fully green leaves, elongated stems, and the presence of flowers or seeds; and (c) senescent (decline in forage quality and quantity) was classified as total leaf senescence, loss of pigment, leaf drop, and cured plant parts. The phenophase of each plant functional group was described using ocular estimates at the plot level by categories of percentage understory canopy cover (1 = 0%-20%, 2 = 21%-40%, 3 = 41%-60%, 4 = 61%-80%, 5 = 81%-100%). ...
Article
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Consistent with a warming climate, the timing of key phenological phases (i.e. phenophases) for many plant species is shifting, but the direction and extent of these shifts remain unclear. For large herbivores such as ungulates, altered plant phenology can have important nutritional and demographic consequences. We used two multi-year datasets collected during 1992–1996 and 2015–2019 of understory plant phenology in semi-arid forested rangelands in northeastern Oregon, United States, to test whether the duration of phenophases for forage species has changed over time for three plant functional groups (forbs, graminoids, and shrubs). Duration of spring green-up was approximately 2 weeks shorter in the later years for forbs (19 ± 3.8 d) and graminoids (13.2 ± 2.8 d), and senescence was 3 weeks longer for graminoids (25.1 ± 5.1) and shrubs (22.0 ± 4.6). Average peak flowering date was 3.1 ± 0.2 d earlier per decade for understory forage species with approximately 1/3 of the species (35%) exhibiting earlier peak flowering dates over time. Variation in late-winter precipitation had the greatest effect on the duration of understory green-up, whereas variation in summer precipitation had a greater effect on duration of the senescent period. Collectively, these results indicate climate-related progression towards shorter periods of peak plant productivity, and earlier and longer periods of plant senescence, the combination of which substantially reduces the temporal window of forage available in growing forms most usable to herbivores. This work adds a needed component to the climate change literature, by describing links between shifting climate variables, multiple phases of understory plant phenology, and possible nutritional consequences for herbivores under a warming climate.
... Alpine environments are highly seasonal, characterized by relatively cold and short growing seasons and low primary productivity (Pettorelli et al., 2007). Mountain ungulates (subfamily Caprinae) are capital-breeding, alpine species that are expected to exhibit conservative reproductive tactics relative to resource allocation (Toügo et al., 2002). ...
... There are potential nutritional limitations associated with living in alpine ranges. Ungulates inhabiting alpine environments can experience shorter periods of availability of high-quality forage than other temperate ungulates, especially during summers with early and rapid snowmelt (Pettorelli et al., 2007). Further, before giving birth, mountain sheep often migrate to high-elevation summer ranges or parturition sites before spring green-up begins . ...
Article
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Food quality and availability, when combined with energetic demands in seasonal environments, shape resource acquisition and allocation by animals and hold consequences for life‐history strategies. In long‐lived species with extensive maternal care, regulation of somatic reserves of energy and protein can occur in a risk‐sensitive manner, wherein resources are preferentially allocated to support survival at the cost of investment in reproduction. We investigated how Rocky Mountain bighorn sheep (Ovis canadensis), an alpine mammal in a highly seasonal environment, allocates somatic reserves across seasons. In accordance with the hypothesis of risk‐sensitive resource allocation, we expected accretion and catabolism of somatic reserves to be regulated relative to preseason nutritional state, reproductive state, and variation among populations in accordance with local environmental conditions. To test that hypothesis, we monitored seasonal changes in percent ingesta‐free body fat (IFBFat) and ingesta‐free, fat‐free body mass (IFFFBMass) in three populations of bighorn sheep in northwest Wyoming between 2015 and 2019 through repeated captures of female sheep in December and March of each year in a longitudinal study design. Regulation of somatic reserves was risk‐sensitive and varied relative to the amount of somatic reserves an animal had at the beginning of the season. Regulation of fat reserves was sensitive to reproductive state and differed by population, particularly over the summer. In one population with low rates of recruitment of young, sheep that recruited offspring lost fat over the summer in contrast to the other two populations where sheep that recruited gained fat. And yet, all populations exhibited similar changes in fat catabolism and risk sensitivity over winter. The magnitude of body fat and mass change across seasons may be indicative of sufficiency of seasonal ranges to meet energetic demands of survival and reproduction. Risk‐sensitive allocation of resources was pervasive, suggesting nutritional underpinnings are foundational to behavior, vital rates, and, ultimately, population dynamics. For species living in alpine environments, risk‐sensitive resource allocation may be essential to balance investment in reproduction with ensuring survival.
... In particular, we considered the environmental features of the corresponding HMU: chamois density, elevation, slope, aspect, proportion of open areas, the vegetation green-up corresponding to the pregnancy period as well as to the seasons during which horns grew. The latter was estimated by using the Normalised Difference Vegetation Index (NDVI), which is widely used to depict vegetation green-up in mountain ungulates (Bischof et al., 2012;Brivio et al., 2019;Hamel et al., 2009;Mason et al., 2014Mason et al., , 2017Pettorelli et al., 2007). NDVI was acquired by the Moderate-resolution Imaging Spectroradiometer (MODIS) on board of the AQUA satellite (16-day composites from daily data recorded at a 250 9 250 m pixel size). ...
... NDVI was acquired by the Moderate-resolution Imaging Spectroradiometer (MODIS) on board of the AQUA satellite (16-day composites from daily data recorded at a 250 9 250 m pixel size). Following Pettorelli et al. (2007), we calculated 4 different NDVI measures: the average NDVI values during May, the average NDVI values throughout summer, the NDVI slope between early May and early July, and the maximal slope between any two consecutive bimonthly NDVI values from early May to early July. ...
Article
Animal weapons are one of the most studied morphological traits, particularly in Artiodactyla. Since in polygynous species males with larger weapons tend to be more successful in gaining access to females, researchers have traditionally focused on horn size. However, in species with limited horn size, weapon size has been assumed to have a reduced or null effect on life history traits. We examined the effect of intrinsic and extrinsic factors on the length of the second and third segments of Alpine chamois horns (Rupicapra rupicapra) in a population living in a poor environment. Our aim was to test how environmental conditions affected weapon growth and whether compensatory growth occurred. We showed that horn length was isometric to body size, although male horns grew more quickly. Ecological factors such as snow and forage availability affected weapon length, though mildly. No sign of compensatory growth was detected. We inferred that chamois mainly use horns as armament in intrasexual interactions. However, horn length was not a key element since horn growth remained isometric, at least under suboptimal ecological conditions. In species without extreme weapons, the handicap caused by longer horns is likely not compensated by an increase in individual fitness. Studies on species with weapons that are not extreme have analysed intrinsic and extrinsic factors affecting weapon growth. However, they have often failed to provide full understanding of the actual benefits associated with larger weapons in these species. In Alpine chamois, we found that some environmental factors significantly affected horn length, however the magnitude of such influence was negligible from biological point of view, the actual weapon size being only mildly influenced. The linearity of the relationship between the horns and body weight and the absence of compensatory growth indicate that these biometric measures are isometric during the first years of life. Our findings, on a monomorphic species without extreme weapons, suggest focusing not only on weapon size but also on their use, shape and the different drivers affecting their ontogenesis.
... The rise in temperature will likely cause Siberian ibex and other alpine ungulates to show behavioral and physiological responses, such as heat avoidance and heat stress, leading them to move to higher elevations or seek shade in the short term [16]. Furthermore, the precipitation of the wettest months may affect the distribution of ibex via the change in the phenology and richness of plants [17,74]. In addition, we found that Siberian ibex prefer to inhabit areas with high NDVI, i.e., where there is high vegetation cover allowing species to acquire food without moving too far [29,75]. ...
Article
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Climate change has led to shifts in species distribution and become a crucial factor in the extinction of species. Increasing average temperatures, temperature extremes, and unpredictable weather events have all become a part of a perfect storm that is threatening ecosystems. Higher altitude habitats are disproportionately affected by climate change, and habitats for already threatened specialist species are shrinking. The Siberian ibex, Capra sibirica, is distributed across Central Asia and Southern Siberia and is the dominant ungulate in the Pamir plateau. To understand how climate change could affect the habitat of Siberian ibex in the Taxkorgan Nature Reserve (TNR), an ensemble species distribution model was built using 109 occurrence points from a four-year field survey. Fifteen environmental variables were used to simulate suitable habitat distribution under different climate change scenarios. Our results demonstrated that a stable, suitable habitat for Siberian ibex was mostly distributed in the northwest and northeast of the TNR. We found that climate change will further reduce the area of suitable habitat for this species. In the scenarios of RCP2.6 to 2070 and RCP8.5 to 2050, habitat loss would exceed 30%. In addition, suitable habitats for Siberian ibex will shift to higher latitudes under climate change. As a result, timely prediction of the distribution of endangered animals is conducive to the conservation of the biodiversity of mountain ecosystems, particularly in arid areas.
... For the considered territory, there are very long data series for some species such as the Alpine ibex (Capra ibex), in the Gran Paradiso National Park with 45-year time series of annual censuses [48,49]. Analyses have been carried out of the effects of climate change on the local distribution and fitness of many species, also combining an empirical population modelling approach and stochastic simulations of the population dynamics [50,51]. ...
Article
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Since climate change impacts are already occurring, urgent adaptive actions are necessary to avoid the worst damages. Regional authorities play an important role in adaptation, but they have few binding guidelines to carry out strategies and plans. Sectoral impacts and adaptive measures strongly differ between regions; therefore, specific results for each territory are needed. Impacts are often not exhaustively reported by literature, dataset and models, thus making it impossible to objectively identify specific adaptive measures. Usual expert elicitation helps to fill this gap but shows some issues. For the Piedmont Strategy, an innovative approach has been proposed, involving experts of private and public bodies (regional authorities, academia, research institutes, parks, associations, NGOs, etc.). They collaborated in two work group, first to identify current and future impacts on biodiversity and ecosystems, and secondly to elaborate and prioritize measures. Involving 143 experts of 46 affiliations, it was possible to quickly edit a cross-validated list of impacts (110) and measures (92) with limited costs. Lastly, a public return of results took place. This approach proved to be effective, efficient and influenced the policymakers, overcoming the tendency to enact long-term actions to face climate change. It could be used internationally by subnational authorities also in other sectors.
... Both survival and growth varied with population density and food availability in interaction with rainfall and temperature, with relatively minor effects of maternal condition and date of birth. These results are comparable to those obtained for northern temperate ungulates (Fowler 1987;Garel et al. 2004;Pettorelli et al. 2007;Feder et al. 2008), further supporting the idea that kangaroos are ecological analogs of ungulates (Fisher et al. 2002). Our study highlights the importance of monitoring population density and food availability in long-term studies of large herbivores, particularly in relatively unpredictable environments. ...
Article
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A central goal of ecology is to understand how environmental variation affects populations. Long-term studies of marked individuals can quantify the effects of environmental variation on key life-history traits. We monitored the survival and growth of 336 individually marked juvenile eastern grey kangaroos (Macropus giganteus), a large herbivore living in a seasonal but unpredictable environment. During our 12-year study, the population experienced substantial variation in rainfall, forage biomass, and density. We used structural equation modeling to determine how variation in temperature and rainfall affected juvenile survival and growth through its effect on forage biomass and population density. Independently of population density, forage biomass had strong positive effects on survival from 10 to 21 months. At low population density, forage biomass also had a positive effect on skeletal growth to 26 months. Increasing maternal body condition improved rearing success for daughters but not for sons. High population density reduced skeletal growth to 26 months for both sexes. Rainfall had an increasingly positive effect on forage biomass at high temperatures, indicating a seasonal effect on food availability. Our study reveals interacting effects of environmental variation on juvenile survival and growth for a large mammal with a conservative reproductive strategy that experiences substantial stochasticity in food availability.
Chapter
This comprehensive species‑specific chapter covers all aspects of the biology of Alpine ibex Capra ibex, including paleontology, physiology, genetics, life history, ecology, habitat, diet, and behavior. The economic significance and management of Alpine ibex and future challenges for research and conservation are addressed as well. The chapter includes a distribution map, a photograph of the animal, and a list of key literature.
Article
Consistent with a warming climate, the timing of key phenological phases (i.e., phenophases) for many plant species is shifting, but the direction and extent of these shifts remain unclear. For large herbivores such as ungulates, altered plant phenology can have important nutritional and demographic consequences. We used two multi-year datasets collected during 1992-1996 and 2015-2019 of understory plant phenology in semi-arid forested rangelands in northeastern Oregon, United States, to test whether the duration of phenophases for forage species has changed over time for three plant functional groups (forbs, graminoids, and shrubs). Duration of spring green-up was approximately two weeks shorter in the later years for forbs (19 ± 3.8 d) and graminoids (13.2 ± 2.8 d), and senescence was three weeks longer for graminoids (25.1 ± 5.1) and shrubs (22.0 ± 4.6). Average peak flowering date was 3.1 ± 0.2 d earlier per decade for understory forage species with approximately 1/3 of the species (35%) exhibiting earlier peak flowering dates over time. Variation in late-winter precipitation had the greatest effect on the duration of understory green-up, whereas variation in summer precipitation had a greater effect on duration of the senescent period. Collectively, these results indicate climate-related progression towards shorter periods of peak plant productivity, and earlier and longer periods of plant senescence, the combination of which substantially reduces the temporal window of forage available in growing forms most usable to herbivores. This work adds a needed component to the climate change literature, by describing links between shifting climate variables, multiple phases of understory plant phenology, and possible nutritional consequences for herbivores under a warming climate.
Article
A study was carried out at the University of Zimbabwe Farm, to assess and quantify the correlation between plant canopy height and biomass in the rangelands of Zimbabwe. Two range sites, bush grassland and grassland, were selected and three paddocks within each range site were sampled. Four 25 m long transects were drawn in the four cardinal directions from the paddock center. Five 0.25 m2 quadrants were located at 5 m intervals on each transect line. Common plant species in both bush grassland and grassland range sites were Sporobolus pyramidalis, Hyparrhenia filipendula, Cynodon dactylon, and Eragrostis curvula. There was a significant (P<0.05) linear relationship between plant height and biomass for both range sites. There was a significant (P>0.05) quadratic relationship between plant height and biomass for grassland but not for the bush grassland. Pearson Correlation Coefficient (r) was 0.929 for grassland and 0.717 for bush grassland. The regression equation was y = 15.82x – 0.02x2 for bush grassland and y = 15.88x – 0.27x2 for grassland. The coefficient of determination (r2) for grassland was 0.863 and 0.514 for bush grassland. Variation in plant height explained 86.3% of the variation in biomass for grassland and 51.4% for bush grassland accordingly.
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Differential temperature changes with altitude can shed light on the relative importance of natural versus anthropogenic climatic change. There has been heightened interest in this subject recently due to the finding that high-elevation tropical glaciers have been retreating and that significant melting from even the highest alpine regions has occurred in some areas during the past 20 years or so, as recorded in ice core records, which do not reveal any similar period during previous centuries to millennia. In this paper we find evidence for appreciable differences in mean temperature changes with elevation during the last several decades of instrumental records. The signal appears to be more closely related to increases in daily minimum temperature than changes in the daily maximum. The changes in surface temperature vary spatially, with Europe (particularly western Europe), and parts of Asia displaying the strongest high altitude warming during the period of record. High-elevation climate records of long standing taken at a number ofmountain tops throughout the world, but primarily inEurope, are available froma number of countries. In some cases,meteorological observations at these unique mountain sites have been discontinued for a variety of reasons, usually budgetary. It is hoped that the papers published in this special issue of Climatic Change can contribute to a reassessment of the value of continuing climate measurements at these mountain observatories by the appropriate entities, so that we may continue to have access to climate information from the ‘tops of the world’.
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In large-herbivore populations, environmental variation and density dependence co-occur and have similar effects on various fitness components. Our review aims to quantify the temporal variability of fitness components and examine how that variability affects changes in population growth rates. Regardless of the source of variation, adult female survival shows little year-to-year variation [coefficient of variation (CV<10%)], fecundity of prime-aged females and yearling survival rates show moderate year-to-year variation (CV<20%), and juvenile survival and fecundity of young females show strong variation (CV>30%). Old females show senescence in both survival and reproduction. These patterns of variation are independent of differences in body mass, taxonomic group, and ecological conditions. Differences in levels of maternal care may fine-tune the temporal variation of early survival. The immature stage, despite a low relative impact on population growth rate compared with the adult stage, may be the critical component of population dynamics of large herbivores. Observed differences in temporal variation may be more important than estimated relative sensitivity or elasticity in determining the relative demographic impact of various fitness components.
Book
Global warming is likely to have the greatest impact at high latitudes, making the Arctic an important region both for detecting global climate change and for studying its effects on terrestrial ecosystems. The chapters in this volume address current and anticipated impacts of global climate change on Arctic organisms, populations, ecosystem structure and function, biological diversity, and the atmosphere.
Article
Onset of the growing season in mid-latitudes is a period of rapid transition, which includes heightened interaction between living organisms and the lower atmosphere. Phenological events (seasonal plant and animal activity driven by environmental factors), such as first leaf appearance or flower bloom in plants, can serve as convenient markers to monitor the progression of this yearly shift, and assess longer-term change resulting from climate variations. We examined spring seasons across North America over the 1900–1997 period using modelled and actual lilac phenological data. Regional differences were detected, as well as an average 5–6 day advance toward earlier springs, over a 35-year period from 1959–1993. Driven by seasonally warmer temperatures, this modification agrees with earlier bird nesting times, and corresponds to a comparable advance of spring plant phenology described in Europe. These results also align with trends towards longer growing seasons, reported by recent carbon dioxide and satellite studies. North American spring warming is strongest regionally in the northwest and northeast portions. Meanwhile, slight autumn cooling is apparent in the central USA. Copyright © 2000 Royal Meteorological Society
Chapter
Model building and data analysis in the biological sciences somewhat presupposes that the person has some advanced education in the quantitative sciences, and statistics in particular. This requirement also implies that a person has substantial knowledge of statistical hypothesis-testing approaches. Such people, including ourselves over the past several years, often find it difficult to understand the information-theoretic approach, only because it is conceptually so very different from the testing approach that is so familiar. Relatively speaking, the concepts and practical use of the information-theoretic approach are much simpler than those of statistical hypothesis testing, and very much simpler than some of the various Bayesian approaches to data analysis (e.g., Laud and Ibrahim 1995 and Carlin and Chib 1995).