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Red deer and Apennine chamois: a difficult coexistence

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Animal Conservation. Print ISSN 1367-9430

Unexpected consequences of reintroductions:

competition between increasing red deer and threatened
Apennine chamois
S. Lovari1,2*, F. Ferretti1,2*, M. Corazza3, I. Minder1,2, N. Troiani3, C. Ferrari3 & A. Saddi1
1 Research Unit of Behavioural Ecology, Ethology and Wildlife Management, Department of Life Sciences, University of Siena, Siena, Italy
2 Biodiversity and Conservation Network (BIOCONNET), Department of Life Sciences, University of Siena, Siena, Italy
3 Department of Biological, Geological and Environmental Sciences, University of Bologna, Bologna, Italy

Keywords Abstract
interspecific interactions; protected areas;
reintroductions; Rupicapra; ungulates; Reintroductions are commonly used to restore the local biological diversity and/or
vegetation change. save threatened taxa. In human-altered landscapes, we may expect that reintro-
duced species affect taxa already present. In Abruzzo, Lazio and Molise National
Correspondence Park (central Apennines, Italy), a 30% decline in the abundance of ‘vulnerable’
Sandro Lovari, Research Unit of Behavioural Apennine chamois (2005: c. 650 individuals, 2010: c. 450 individuals) has been
Ecology, Ethology and Wildlife recorded, whereas red deer (reintroduced in 1972–1987: 81 individuals) have
Management, Department of Life Sciences, greatly increased (2010: > 2500 individuals). We investigated space and diet over-
University of Siena. Via P.A. Mattioli 4, laps between red deer and Apennine chamois, and their effects on foraging behav-
53100, Siena, Italy. iour of the latter. We also compared the composition of grasslands with that
Email: lovari@unisi.it recorded when the former were absent. In 2010–2011, we found out: (1) a great
space (> 75%) and diet (> 90%) overlap between deer and chamois; (2) a significant
*Both authors contributed equally to this increase of unpalatable plant species and a decreasing trend of the nutritious, most
study. grazed species by chamois, in respect to when deer were absent; (3) irrespective
from vegetation type, a significantly reduced bite rate of adult female chamois in
Editor: Iain Gordon
patches used also by deer, compared with areas without deer. Our results suggest
Associate Editor: Kate Searle
a negative effect of red deer on the availability of nutritious plant species in
summer–autumn, possibly because of grazing and physical damage on the grass-
Received 18 July 2013; accepted 06
land caused by trampling. Environmental conditions and access to high-quality
January 2014
forage in the warm season influence the winter survival of offspring of mountain
ungulates. Our results indicate that interspecific overlap in resource use with an
doi:10.1111/acv.12103
increasing, reintroduced population can threaten rare taxa. Reintroductions of
potentially competing species should be avoided in areas where populations of
threatened taxa exist.

Introduction present species. On the other hand, information is not avail-

A reintroduction is the intentional movement and release of
a taxon inside its indigenous range, from which it disap-
peared in historical time (IUCN, 2012). Reintroductions are
commonly used to restore ecosystems and save threatened
taxa (Armstrong & Seddon, 2008; IUCN, 2012). If causes of
extinction or limiting factors have been removed and a fea-
sibility study has been carried out, reintroductions can
enhance the viability and the conservation status of a taxon.
Reintroductions may also have unexpected impacts that
outweigh their benefits: for example the reintroduction of
carnivores could generate cascade effects on other compo-
nents of ecosystems, with potentially negative effects on
some of them (Smith, Peterson & Houston, 2003). Reintro-
duced large herbivores can show sharply increasing popula-
tion dynamics (e.g. Leopold, 1943; Caughley, 1970; Forsyth
& Caley, 2006), which may elicit competition with already
able on the effects of reintroduced populations of large
herbivores on native ones.
Interspecific competition occurs when two species use the
same, limited resource, with negative effects of the superior
competitor on numbers of the inferior one (de Boer & Prins,
1990). Competition occurs through exploitation, when indi-
viduals deplete the amount of resource left available to
others, or through interference, when a resource is actively
disputed (Putman, 1996). In some cases, interspecific
overlap in the use of food resources or habitat, or inverse
numerical trends of populations living in sympatry have
been considered as indirect potential indices of competition
(Putman, 1996; Latham, 1999, for reviews). In these cases,
exploitation of resources has been suspected to affect popu-
lation dynamics, distribution, resource use and phenotypic
quality of wild ungulates (e.g. Sinclair & Northon-Griffiths,
1982; Putman, 1996; Latham, 1999; Focardi et al., 2006;

Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London 359
Competition between reintroduced red deer and Apennine chamois
Richard et al., 2010). Conversely, field data (Ferretti et al.,
2011) and anecdotal observations (Anthony & Smith, 1977;
Forsyth, 1997) have suggested that competition may also
occur through interference. However, few studies have pro-
vided strong evidence of competition among wild ungulates
(Forsyth & Hickling, 1998; Ferretti et al., 2011) and infor-
mation on mechanisms of competition is also scarce (but see
Ferretti et al., 2011).
The availability and quality of food resources in spring–
summer are crucial to improve winter survival of offspring,
which, in turn, influences the population dynamics of wild
ungulates, especially on mountains (e.g. Festa-Bianchet,
1998a; Côté & Festa-Bianchet, 2001a; Pettorelli et al.,
2007). In particular, body size and survival of offspring
depend on environmental variables and body conditions of
mothers, which, in turn, are affected by spring–summer
food resources (Clutton-Brock, Albon & Guinness, 1984,
1986; Festa-Bianchet, 1998a,b; Côté & Festa-Bianchet,
2001a-b; Pettorelli et al., 2005, 2007). In the warm months,
the exploitation of food resources and/or the limitation
of access to them by a competitor, through interference,
could be the ultimate factor affecting the viability of an
ungulate population. We used the Apennine chamois
Rupicapra pyrenaica ornata and the red deer Cervus elaphus
to test the hypothesis that overlap in diet and habitat with a
reintroduced ruminant will alter the foraging efficiency of
another ungulate. High overlap would negatively affect the
latter’s abundance and population persistence.
The Apennine chamois is a ‘vulnerable’ taxon, strictly
protected under national and international legislation, listed
on appendix II of the Bern Convention; annexes II and IV of
the European Union Habitats and Species Directive; appen-
dix II of Convention on International Trade in Endangered
Species of Wild Fauna and Flora; and listed as ‘especially
protected species’ under Italian law n. 157/1992 (Herrero,
Lovari & Berducou, 2008). During the Holocene, the
Apennine chamois was distributed along the Apennine
chain (Masini & Lovari, 1988), surviving only in the
Abruzzo, Lazio and Molise National Park (ALMNP,
central Italy) until 1991 (Dupré, Monaco & Pedrotti, 2001).
Since 1991, there have been many releases of the Apennine
chamois into other protected areas in the central Apennines
(Lovari et al., 2010). Chamois numbers have decreased by at
least 30% within the ALMNP during the last decade (c. 650
individuals in 2005 and c. 450 individuals in 2010; Latini
et al., 2011). Mortality of nearly all kids during winter, espe-
cially in their core range, has determined the population
decline (Latini et al., 2011).
A total of 45 red deer were reintroduced to the ALMNP
in 1972, within the core area of the chamois range (density:
0.5 indviduals per 100 ha; Apollonio & Lovari, 2001).
Thirty-six other individuals were released in small groups
(7–10 individuals per release, in four operations), in the
following 15 years (Apollonio & Lovari, 2001). No data are
available on population dynamics of red deer in ALMNP in
1972–2006, but not surprisingly, recent estimates indicate a
great increase of their densities with respect to the time of
their release (2007: 9.0 individuals per 100 ha; 2010: 14.3
360
S. Lovari et al.
individuals per 100 ha, in the core range of the Apennine
chamois; Latini, 2010). In the last 30 years, chamois density
has about halved in the core area of their range (1984–1985:
c. 38 individuals per 100 ha, Lovari, 1985; 2012: c. 20 indi-
viduals per 100 ha, cf. Latini et al., 2012). In the warm
months, red deer use the alpine grasslands, attended only by
chamois 30 years ago (Lovari, 1984; Bruno & Lovari, 1989).
Because of its flexible food habits (Hofmann, 1989), the red
deer shows a great overlap in diet and habitat use with other
ungulate species (Putman, 1996). A negative effect of red
deer has been suggested for density (Latham et al., 1997)
and body size (fawns: Richard et al., 2010) of roe deer
Capreolus capreolus. A great overlap in the diet of red deer
with that of Northern chamois Rupicapra rupicapra has
been detected (Schröder & Schröder, 1984; Bertolino et al.,
2009), suggesting the potential for competition.
We predicted that: (1) there is a diet/spatial overlap
between Apennine chamois and red deer, both ‘intermediate
feeders’ (Hofmann, 1989), in the warm period, that is
summer to mid-autumn; (2) an increase of the frequency of
unpalatable species and a decrease of that of preferred ones
by chamois has occurred with respect to the time when deer
did not attend the area (cf. Ferrari, Rossi & Cavani, 1988);
(3) the spatial overlap of red deer with adult female chamois
decreases the latter’s foraging efficiency. A decrease in
highly nutritious food resources and an increase in less pal-
atable ones should result in a greater search for food (thus a
greater step rate, cf. Owen-Smith & Novellie, 1982) and a
lower bite rate of chamois in patches attended by both
species, than in those where only chamois graze; (4) red deer
will displace chamois from their feeding grounds, as the
former are much larger than the latter (Boitani et al., 2003;
cf. Ferretti, Sforzi & Lovari, 2011).
Methods
Study area
Our 65-ha experimental area was the core distribution of the
Apennine chamois in ALMNP, upper Val di Rose (prevail-
ing NE-SE aspects), above the treeline (mixed beech Fagus
sylvatica forests, c. 1700–1800 m a.s.l.) up to the top of M.
Sterpi d’Alto and M. Boccanera (1966 and 1982 m a.s.l,
respectively). Up to the late 1990s, our study area and its
neighbourhoods held the densest population of Apennine
chamois (38 individuals per 100 ha, N = c.140 individuals,
Lovari, 1985).
The study area lies in the cold axeric region and cold
temperate subregion (Blasi, 1994), with annual rainfall:
1500 mm; summer rainfall: 260–270 mm; mean annual tem-
perature: 4.7°C; no dry season. Snow cover lasts from late
November to May–June (Bruno & Lovari, 1989).
Vegetation (Fig. 1 and Supporting Information Appen-
dix S1) is a mosaic composed by palatable graminoids
(35.5%), unpalatable grass Brachypodium genuense (24.3%),
clover-dominated Trifolium thalii patches (15.2%) and
rocks/screes with sparse vegetation (25.0%), ungrazed by
livestock since at least 50 years ago.
Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London
S. Lovari et al. Competition between reintroduced red deer and Apennine chamois

per cell; N = 38; cell size: 100 m; cf. Fattorini et al., 2011).
Through a survey in October 2010, we assessed spatial
overlap in the previous months. The presence of pellet
groups of red deer should reflect the use of high-altitude
meadows (c. 1800–2000 m a.s.l.) by this ungulate, in the
previous months.
The faecal accumulation rate technique (Mayle et al.,
1999) was used in 2011. In late June, all pellet groups were
removed from each plot, which were then visited again in
late August to count pellet groups and to estimate overlap in
summer. If pellet groups of red deer/chamois were not found
in August, plots were visited again in late October, to assess
spatial overlap in summer–autumn. We used the index of
Jaccard (1901) to assess spatial overlap in the study area (I)
and in the area used by chamois (ICAM):

I = α (α + β + γ ) ;

I CAM = α (α + β ) ,

where α = number of plots with pellet groups of both

species; β = number of plots with pellet groups of chamois;
γ = number of plots with pellet groups of red deer.

Figure 1 Vegetation map of the study area.

Diet overlap
The diet composition of chamois and red deer were com-
In 2010 and 2011, respectively, 85 (39 adult females) and
pared seasonally through the detection of food remains in
82 (33 adult females) chamois attended our study area (i.e.
faecal samples (Johnson et al., 1983) in spring (April–
the maximum number of individuals observed in separate
May), summer (July–August) and autumn (September–
groups, at the same time in a day, divided by sex/age class;
early November) 2010–2011 (chamois faecal samples, in
40% less than in 1985–1986, S. Lovari, unpubl. data), with a
total: N = 59; red deer faecal samples: N = 54). Only fresh
population structure strongly skewed to mature individuals
samples were collected, after observing defecations
(Latini et al., 2011). Our study area was used also by red
(chamois: n = 8 per season, 2010; n = 10–13 per season,
deer (mean density in ALMNP: 5 deer per 100 ha; mean
2011; red deer: n = 8 per season, 2010; n = 8–11 per season,
density in our study area, the core range of chamois: 14.3
2011) and frozen within several hours, before analyses
deer per 100 ha, in 2010; Latini, 2010: c. 1.3 tons per 100 ha
were carried out. Differences in the seasonal percentage
of deer biomass). Roe deer and wild boar Sus scrofa also live
volume of plant categories were tested by the Mann–
in ALMNP, but they only visit upper grasslands occasion-
Whitney U-test, while frequencies of occurrence were com-
ally (i.e. their faeces were found in only 2% and 1%, of
pared by the chi-square test (Sokal & Rohlf, 1995). We
surveys in sampling plots, respectively, see later). In the last
considered the categories ‘trees/shrubs’, ‘forbs’, ‘grass’ and
50 years, livestock has been absent from this area. The grey
‘fruits’. Seasonal diet overlap (proportional volumes; rela-
wolf Canis lupus, brown bear Ursus arctos and golden eagle
tive frequencies) was estimated through the index of
Aquila chrysaetos visit the area.
Pianka (1973):

M M M
Ov = ∑ oiACoiRD ∑o ∑o 2
iAC
2
iRD
i =1 i =1 i =1
Spatial overlap
In July–October, the extent of spatial overlap of red deer where oi = proportion of food category i in the diet of
and chamois was estimated through pellet group counts Apennine chamois and red deer (0 = no overlap; 1 = max.
(Mayle, Peace & Gill, 1999; Forsyth et al., 2007). Pellets of overlap). In our study area, most plant families have specific
red deer and chamois can be readily told apart through a indigestible features, for example trichomes and glandular
number of morphological differences (Mustoni et al., 2002). cells, which allow detection of their presence in samples.
Presence/absence of pellet groups (>5 pellets, Mayle et al., Overlap in frequency of use of single forb families was inves-
1999) was recorded in circular sampling plots (radius: 5 m), tigated. See Minder (2012) and Supporting Information
randomly placed onto a grid overlain to grasslands (1 plot Appendix S1, for further details.

Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London 361
Competition between reintroduced red deer and Apennine chamois
Vegetation change
Frequency of occurrence (presence/absence) and cover of
plant species were compared between 1982–1984 (red
deer absent) and 2010–2011 (red deer present) through
vegetation surveys in plots (100 m2 per area; n = 34; cf.
Rossi, 1985) using the phytosociological method
(Braun-Blanquet, 1964). We considered the most grazed
species in 1982–1984, according to a scale of monthly
grazing frequency, and three unpalatable species, rare in
1982–1984 (B. genuense, Carduus carlinaefolius, Carlina
acaulis; Rossi, 1985; Ferrari et al., 1988). Presence/absence
of signs of trampling (identified through footprints) by red
deer, absent in 1982–1984 (Rossi, 1985; Ferrari et al.,
1988), were estimated visually.
Presence/absence and frequency/cover of plant species
were compared between 1982–1984, and 2010–2011,
through generalized linear models with binomial (presence/
absence) and Poisson (cover) errors (Crawley, 2007). Statis-
tical analyses were carried out through the R software (R
Development Core Team, 2009).
Effects of red deer on foraging efficiency
of Apennine chamois
The effects of usage of alpine grasslands by red deer on the
foraging efficiency of adult female chamois (> 3 years old;
Lovari, 1985) were assessed through behavioural observa-
tions. Chamois in our study area were habituated to tourists
and could be approached to up to 30 m without eliciting any
alarm response (Cederna & Lovari, 1985). Chamois were
observed from vantage points, at a distance of 30–200 m,
from dawn to dusk (2 days per week; mid-July to early
November; Bruno & Lovari, 1989).
The foraging behaviour of chamois was recorded through
focal animal sampling (Altmann, 1974). Observations were
carried out in 10-min bouts, divided by 1-min sampling
intervals (Ruckstuhl, Festa-Bianchet & Jorgenson, 2003).
Each 1-min focal sample was followed by an interval of 10 s,
to record data on a checksheet (Bruno & Lovari, 1989;
Ruckstuhl et al., 2003). We recorded (1) n. bites to grass per
min (bite rate, an index of food intake rate; Bruno & Lovari,
1989; Ruckstuhl et al., 2003); a bite was identified by a
distinct jerking motion of the head (Bruno & Lovari, 1989);
and (2) number of steps for food searching per min (step
rate: an index of foraging continuity; Bruno & Lovari, 1989;
Neuhaus & Ruckstuhl, 2002); a ‘foraging step’ is defined as
a forward movement of one of the forelegs, with the head
close to the ground (Bruno & Lovari, 1989). When neces-
sary, 10 × 50 binoculars and 20–60× spotting scopes were
used to allow the visibility of the mouth of chamois. At each
sampling event, we estimated the proportion of rock cover
around the focal animal (0–25%, 25.1–50%, > 50% of rock
cover in a radius of five times the body length of an adult
chamois). The geographic location of the focal animal was
recorded after it vacated the area, using a hand-held global
positioning system (GPSMAP 62s, Garmin Ltd., Kansas
City, MO, USA). Locations were overlain on the vegetation
362
S. Lovari et al.
map of our study area (Fig. 1) and on maps of usage of
alpine grasslands by red deer (derived from our pellet group
count surveys), to assess: (1) the type of vegetation (vegeta-
tion with T. thalii; vegetation with graminoids) grazed by
the focal animal; and (2) whether it grazed in a grid cell also
used by red deer. Because of their nocturnal activity, the
observability of red deer was so poor in our study area that
reliable, substantial information on the use of upper
meadows could only be collected through an indirect
method.
We carried out short-term observation bouts (10 min
per individual) on different individuals, to reduce
pseudoreplication of data. Daily movements of female
chamois herds were constant and predictable, allowing us to
follow them during our observation bouts. We recorded
data on individuals who could temporarily be distinguished
by their respective positions on the slope (Frid, 1997). Small
morphological differences (Lovari, 1979) that were visible at
close range decreased the probability of recording data from
the same individual more than once daily.
We recorded 364 sampling bouts (mean: 6.1 bouts per
day; standard deviation: 0.6; 57.5 observation hours).
Observation bouts were discarded when the focal animal
disappeared from sight after < 5 min. The effects of spatial
overlap with red deer on the bite and the step rates of adult
female chamois were estimated through generalized linear
mixed models, with Poisson errors (Crawley, 2007). The
number of bites (or the number of steps) in 1-min sampling
intervals were fitted as response variables. In global models,
explanatory variables were: presence of deer pellet
groups, season (summer: July–August; autumn: September–
November), vegetation (patches with T. thalii; patches with
graminoids), rock cover, year (2010, 2011), time of the day
(morning: 5:00–10:00 h; mid-day: 10:00–15:00 h, summer,
10:00–14:00 h, autumn; afternoon: 15:00–20:00 h, summer,
14:00–18:00 h, autumn) and the two-way interactions
between overlap with red deer and the other variables. In
particular, we included the interaction year × overlap with
red deer to test whether our results have been influenced by
the change of sampling technique of pellet group counts,
between 2010 and 2011. The identity of the focal animal
observed in 10 1-min sampling intervals was fitted as
random factor, to control for the effect of repeated measures
of 1-min sampling intervals taken in the same observation
bout. Minimum adequate models were estimated by remov-
ing the least significant term at each step, starting from the
highest level of interactions, until the elimination of terms
caused a significant increase in the residual deviance
(Crawley, 2007). The significance of changes in residual
deviance was assessed through F-like deletion tests
(Crawley, 2007).
Behavioural interference
We recorded behavioural interspecific interactions when
chamois and red deer where at a mutual distance < 50 m
(Anthony & Smith, 1977; Berger, 1985; Forsyth, 1997;
Ferretti, Sforzi & Lovari, 2008; Ferretti et al., 2011). Inter-
Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London
S. Lovari et al. Competition between reintroduced red deer and Apennine chamois

100 *** *
*
80 **
***
***
% volume

60
Grass
Forbs
40
Trees/shrubs
Other
20

0
AC(n
AC = 18)
(N=18) n = 16)
RD ((N=16) AC n = 20)
AC ((N=20) RD
RD (N=19)
(n = 19) AC n = 21)
AC ((N=21) RD((N=19)
RD n = 19)

Spring Summer Autumn

Figure 2 Seasonal diet composition of Apennine chamois (AP) and red deer (RD) in 2010/2011 in terms of volume (%) of main food categories.
* = P < 0.05; ** = P < 0.01; *** = P < 0.001 (Mann-Whitney U-test).

Table 1 Number of sampling plots (N = 38) with pellet groups of chamois only, red deer only and both species and Jaccard indices of spatial
overlap
Season Only chamois Only red deer Overlap I ICAM
Summer/autumn 2010 7 9 22 0.55 0.76
Summer 2011 4 16 18 0.47 0.82
Summer/autumn 2011 3 12 23 0.61 0.88

I and ICAM: Jaccard indices, indicating spatial overlap in the study area and in the area used by chamois, respectively.

actions were classified following Ferretti et al. (2008; 2011; Table 2 Diet composition and overlap of Apennine chamois and red
see Supporting Information Appendix S1). deer, estimated through micro-hystological analyses of faeces:
seasonal differences (Mann–Whitney U-test) of percentage volumes
of plant categories
Results
Seasonal change: U (P-value)
Species Category Spring–summer Summer–autumn
Spatial overlap
Chamois Grass 35.0 (P < 0.001) 71.5 (P < 0.001)
Both species used a large part of the study area (82–92% and Forbs 45.0 (P < 0.001) 42.5 (P < 0.001)
58–76% of plots for red deer and chamois, respectively; Trees/shrubs 159.5 (P > 0.05) 147.0 (P > 0.05)
Table 1). Spatial overlap in the study area (I) was 0.47–0.61, Fruits 162.0 (P > 0.05) 190.5 (P > 0.05)
depending on season/year (Table 1). Spatial overlap was Red deer Grass 148.0 (P > 0.05) 100.5 (P < 0.05)
1.4–1.7 times greater in the areas grazed by chamois than in Forbs 106.5 (P > 0.05) 10.0 (P < 0.001)
the whole study area, as chamois shared 76–88% of their Trees/shrubs 62.0 (P < 0.01) 59.5 (P < 0.001)
grazing areas with red deer (Table 1). Fruits 128.0 (P > 0.05) 107.0 (P < 0.05)

Diet overlap
Grass was the staple of chamois in spring/autumn and that
of red deer in autumn, whereas grass–forbs were the staple
of both species (summer) and that of deer (spring; Fig. 2).
Trees/shrubs and fruits/ferns/mosses were minor food
items (Fig. 2). The volume of grass in the diet of chamois
decreased significantly in summer and increased in autumn,
while that of forbs showed an opposite pattern (Fig. 2;
Table 2). In the diet of red deer, the volume of grass and
forbs did not change between spring and summer, but in
autumn the volume of the former increased while that of the
latter decreased (Fig. 2; Table 2).
Grass and forbs were found in all faecal samples. The
frequency of trees/shrubs decreased in summer and
increased in autumn in red deer, but not chamois (Fig. 2;
Table 3). Summer food habits of chamois and deer were
not significantly different (Fig. 2; Table 4). In spring and
autumn, grass was eaten significantly more by chamois,
whereas deer ate more trees/shrubs (Fig. 2; Table 4).
Forbs formed the greater proportion of the diet of deer in
spring, whereas in autumn this category was eaten more by
chamois than deer (Fig. 2; Table 4). The frequency of
Labiatae, Fabaceae, Caryophyllaceae, Compositae and
Plantaginaceae was ≥ 50% for both ungulates (Fig. 3).

Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London 363
Competition between reintroduced red deer and Apennine chamois S. Lovari et al.

Table 3 Diet composition and overlap of Apennine chamois and red deer, estimated through micro-hystological analyses of faeces: frequency
of occurrence of plant categories and seasonal differences (chi-square test)
Frequency of occurrence Seasonal change: χ2 (P-value)
Species Category Spring Summer Autumn Spring–summer Summer–autumn
Chamois Trees/shrubs 44% 55% 67% 0.11 (P > 0.05) 0.20 (P > 0.05)
Fruits 0% 10% 19% 0.42 (P > 0.05) 0.14 (P > 0.05)
Red deer Trees/shrubs 100% 63% 95% 5.25 (P < 0.05) 5.88 (P < 0.05)
Fruits 6% 21% 53% 0.58 (P > 0.05) 2.83 (P > 0.05)

Table 4 Diet composition and overlap of Apennine chamois and red value of 2.9 (summer) and 2.8 (autumn) more bites to grass
deer, estimated through micro-hystological analyses of faeces: per min in patches unused by deer than in patches with deer.
interspecific differences (Mann–Whitney U-test) of volumes of plant The bite rate was significantly greater in summer than in
categories in the diets autumn (Table 7; Fig. 4), in clover patches than in other
Interspecific differences: U (P-value) patches, in 2011 than in 2010, and it was significantly lower
Category Spring Summer Autumn in patches with >25% rock cover than in areas with < 25%
Grass 31.5 (P < 0.001) 147.5 (P > 0.05) 111.5 (P < 0.05) rock cover (Table 7).
Forbs 63.0 (P < 0.01) 176.0 (P > 0.05) 110.5 (P < 0.05) The median step rates of female chamois were c. 15%
Trees/shrubs 0.5 (P < 0.001) 148.0 (P > 0.05) 51.5 (P < 0.001) (summer) and c. 7% (autumn) greater in areas attended by
Fruits 135 (P > 0.05) 167.5 (P > 0.05) 116 (P < 0.05) deer than in unattended areas, even if this difference was
not significant (Table 7; Fig. 4). The step rate of chamois
was significantly greater in patches with 25.1–50.0% rock
Table 5 Seasonal diet overlap between Apennine chamois and red
cover than in other patches (Table 7). The interaction
deer, estimated through micro-hystological analyses of faecal
Year × Overlap with red deer influenced significantly
samples and the Pianka index
neither the bite rate nor the step rate of chamois (generalized
Diet overlap (Pianka index) linear mixed models; P > 0.05), suggesting that our results
Scale of analysis Spring Summer Autumn were not influenced by the change of sampling technique of
Large categories (% volume) 0.90 0.99 0.97 pellet group counts, in 2011 (see Methods).
Large categories (relative 0.95 >0.99 0.97
frequencies)
Forb families (relative 0.94 0.97 0.92
Behavioural interference
frequencies) Out of 59.5 observation hours, only one interspecific
‘contact’ was recorded: 1 hind and 2 female chamois grazed
with no apparent interaction. Six ‘contacts’ were seen
outside recording sessions, with no apparent interaction: in
Seasonal diet overlap was high (Ov > 0.90) at all scales of
one case, one adult male chamois uttered an alarm whistle,
analyses (Table 5). Overlap was the greatest in summer
without withdrawing, to a stag.
(Ov = 0.97–0.99) and the lowest in spring (0.90–0.95;
Table 5).
Discussion
Although increasing populations of introduced ungulates
Vegetation change
can affect the density of other ungulates (e.g. fallow deer/roe
Decreases in both the frequency of occurrence and cover deer: Putman & Sharma, 1987; Ferretti et al., 2011; Hima-
proportion of 11 out of the 12 plant species most grazed by layan tahr/Alpine chamois: Forsyth & Hickling, 1998), the
chamois were observed in 2010–2011 in comparison with effects of increasing populations of reintroduced ungulates
1982–1984 (Table 6). Differences between periods were sig- on autochtonous ones have not been assessed. This event
nificant for 5 (frequency) and 8 (cover) species (Table 6). may be especially harmful when local taxa are threatened.
Conversely, frequency and cover of unpalatable species In this paper, we suggest that the recent decline of a vulner-
increased significantly from 1982–1984 to 2010–2011 able ungulate could be related to the increase of a reintro-
(Table 6). Deer trampling was recorded in 60% of sampling duced one, through competition for a scarce food resource.
plots. Mainly vegetation quality and quantity influence body
growth, survival, reproductive success and population
dynamics of ungulates (e.g. Clutton-Brock et al., 1984,
Effects of red deer on foraging efficiency
1986; Côté & Festa-Bianchet, 2001b; Pettorelli et al., 2007).
of Apennine chamois
Among mammals, while body mass can still increase
The bite rate of adult female chamois was significantly after adulthood, skeletal growth is restricted to early life
greater in areas without red deer compared with those with (e.g. Clutton-Brock, Guinness & Albon, 1982; Lindström,
red deer (Table 7; Fig. 4). Female chamois gave a median 1999; Lummaa & Clutton-Brock, 2002; Hewison et al.,

364 Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London
S. Lovari et al. Competition between reintroduced red deer and Apennine chamois
% frequency of occurrence

100 Apennine chamois

80 Red deer

60
40
20
0

Plantaginaceae
Labiatae

Leguminosae

Caryophyllaceae

Compositae

Geraniaceae

Cistaceae

Scrophulariaceae

Rosaceae

Liliaceae
Plumbaginaceae

Umbelliferae

Polygonaceae

Rubiaceae

Ranunculaceae
Figure 3 Frequency of occurrence (%) of
forbs (only families with frequency of
occurrence > 5%) in the diet of Apennine
chamois (N = 59) and red deer (N = 54) in
2010/2011.

Table 6 Variation in frequency of occurrence (FO; %) and cover values [CV; ± standard error (SE)] of the most grazed species by Apennine
chamois when no red deer were present in our study area (1982–1984) and those of unpalatable species, between 1982–1984 and 2010–2011
FO (%) Variation in FO Variation in CV
Species 1982–1984 2010–2011 B SE P B SE P
Palatable Bellis pusilla 29 32 0.14 0.53 n.s 0.07 0.15 n.s
Doronicum columnae 59 32 −1.09 0.51 * −0.46 0.18 **
Festuca spp 74 59 −0.67 0.52 n.s −0.03 0.13 n.s
Heracleum sphondylium orsinii 59 12 −2.37 0.64 *** −0.92 0.26 ***
Plantago atrata 91 82 −0.79 0.75 n.s −0.67 0.22 **
Poa alpina 53 35 −0.72 0.50 n.s −0.31 0.14 **
Ranunculus apenninus 88 74 −0.99 0.66 n.s −0.42 0.17 *
Rumex acetosa 79 26 −2.37 0.58 *** −0.79 0.20 ***
Taraxacum apenninum/Crepis aurea 91 32 −3.07 0.71 *** −1.07 0.23 ***
glabrescens
Taraxacum officinale 35 26 −0.42 0.53 n.s −0.23 0.20 n.s
Trifolium pratense semipurpureum 59 47 −0.47 0.49 n.s −0.24 0.15 n.s
Trifolium thalii 88 62 −1.54 0.64 * −0.44 0.13 ***
Unpalatable Brachypodium genuense 3 62 3.98 1.07 *** 2.30 1.01 *
Carduus carlinaefolius 35 94 3.38 0.81 *** 0.85 0.22 ***
Carlina acaulis 9 29 1.46 0.71 * 0.67 0.37 n.s

Variations in FO and CV of three poorly palatable species were considered as well. Significance of difference was assessed using generalized
linear models with binomial (presence/absence) errors. *** = P < 0.001; ** = P < 0.01; * = P < 0.05. n.s., not significant.

2005). In particular, the youngest cohorts in a population Table 7 Factors affecting bite and step rates of adult female
require good food in summer to enhance body growth and, Apennine chamois (N = 3389 1-min sampling intervals, out of 364
in turn, winter survival (Lindström, 1999; Lummaa & observation bouts collected in 2010–2011)
Clutton-Brock, 2002). Thus, a reduction of food resources Model Variable Coefficient SE P
(e.g. because of resource exploitation by a superior competi- Bite rate Overlap with red deer (yes) −0.083 0.016 0.000
tor) could have negative effects on winter survival, especially Season (summer) 0.236 0.017 0.000
of young individuals. Rock cover (>50.0%) −0.154 0.022 0.000
Diet overlap was great between chamois and deer. Thus, Rock cover (25.1–50.0%) −0.057 0.018 0.001
one could expect that competition would arise when Year (2011) 0.032 0.015 0.036
resources are limited. No behavioural interference was Vegetation type (patches 0.040 0.017 0.019
recorded during our study. The lack of obvious interference with Trifolium thalii)
between red deer and chamois does not necessarily rule out Intercept 3.204 0.020 0.000
interference competition, in the past 30 years. However, Step rate Rock cover (25.1–50.0%) 0.157 0.079 0.046
Ferretti et al. (2011) reported substantial direct interactions Intercept 0.889 0.084 0.000
between roe deer and fallow deer, with the fallow being the
Effects were estimated through generalized linear mixed models,
superior competitor, in an area where they had been with Poisson errors. The final model for step rate included also the
together for at least 50 years. Our results have shown that non significant effects of overlap with red deer, vegetation type and
the quality of alpine grassland has decreased between 1982– year. SE, standard error.
1984 and 2010–2011, and the most grazed plant species by
chamois (Rossi, 1985; Ferrari et al., 1988) have generally

Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London 365
 Competition between reintroduced red deer and Apennine chamois
Number of bites to grass per min
38
36
34
32
30
28
n = 86
26 10-min
24 intervals n = 91
22
n = 45
20
n = 142
18
Summer Autumn
Patches used by chamois only
Patches used by red deer and chamois
Figure 4 Bite rate and step rate (N of bites/min and N of steps/min, respectively; median ± interquartile range) of adult female Apennine
chamois, in 2010–2011: effects of season and overlap with red deer. For significance, see Table 5.
decreased in frequency and/or cover. The diet of nursing
female chamois depends on the availability of nutritious
vegetation dominated by T. thalii (Ferrari et al., 1988). This
species, whose leaves are rich in proteins and highly digest-
ible (Ferrari et al., 1988), has decreased significantly in
frequency/cover with respect to the time when deer were
absent. Conversely, unpalatable species have increased sig-
nificantly in frequency and/or cover. In particular, the for-
merly rare B. genuense (3% frequency) occurred in more
than 60% of relevés, in 2010–2011, covering more than 24%
of grasslands. The strong vegetative reproduction and the
capacity to alter the ecology of an area make the B. genuense
a greatly competitive plant (Catorci et al., 2011). Because of
the high silica content and the hairs on its leaves, it is not
eaten by chamois and red deer, except accidentally (I.
Minder, unpubl. data). Pasture abandonment promotes the
spread of this plant on calcareous grasslands, as moderate
livestock grazing may control it (Catorci et al., 2013). In our
study area, the heavy grazing selectivity of wild ungulates
could have altered the composition of plant communities,
reducing the fitness of palatable plants and favouring the
spread of scarcely palatable species (Augustine &
McNaughton, 1998; Alm Bergvall et al., 2006). Red deer
have a body mass approximately four times greater than
that of chamois and move in large herds (up to 90 individu-
als in our study area), with a potentially great impact on
vegetation, whereas female Apennine chamois are partial to
T. thalii patches (Ferrari et al., 1988). Accordingly, 60% of
sampling plots showed deer trampling, while trampling was
absent when only chamois grazed in the study area (Rossi,
1985; Ferrari et al., 1988). Red deer may outcompete
chamois not only by feeding over the same preferred food
resources, but also by altering the quality of grassland
through trampling.
The best food patches for chamois (i.e. T. thalii commu-
nities) could not only be depleted by high densities of red
deer, but they may also be influenced by climatic conditions.
Trifolium thalii communities are restricted to sites with a
long-lasting snow cover (Ferrari et al., 1988; Blasi, Di Pietro
& Pelino, 2005). Fluctuations of temperature and snowmelt
366
S. Lovari et al.
5
Number of steps per min
4,5
4
3,5
3
2,5
2
1,5
1
Summer Autumn
affect the viability of snowbed vegetation (Schöb et al.,
2009). Because of climate changes, the reduction of cold-
adapted species and the increase of thermophilous ones have
already been recorded in European alpine ecosystems
(including Apennines; Gottfried et al., 2012). In a nearby
Apennine area (Mt. Greco massif), T. thalii communities
almost disappeared in years with scarce snowfalls (D’Angeli
et al., 2011). In turn, reduction of T. thalii communities
because of climate change could be an alternative reason per
se for the observed decline of chamois, in our study area.
Numbers of Apennines chamois have been increasing stead-
ily in neighbour national parks (Mari & Lovari, 2006), as
well as on mountains relatively close (c. 7–8 km, in a straight
line) to our study area (Lovari, 1977; Latini et al., 2011),
suggesting that potential negative effects of climate change
on the quality of meadows are not yet affecting the viability
of other chamois populations. Because of the rarity and the
fragility of clover communities on the Apennines (Petraglia
& Tomaselli, 2007), and their high nutrient value for
chamois (Ferrari et al., 1988), the alteration or even a reduc-
tion of spatial distribution of this community would inevi-
tably lead to a decrease of nutritious pasture for chamois.
The foraging behaviour of chamois reflects the quality of
pasture in areas with or without red deer presence. We were
compelled to infer the use of grasslands by red deer through
pellet group counts, because of the poor observability of
deer, in our study area. Diet analyses confirmed that deer
fed mainly on species available in the upper grasslands, that
is on feeding grounds of chamois. It has been shown that
bharal Pseudois nayaur increased their diet breadth, when in
sympatry with one to two species of large herbivores, pre-
sumably to include less nutritious food items because of
forage constraints imposed by competitors (Namgail et al.,
2007). On poor feeding grounds, with less opportunities to
select rich food patches, an increased use of less palatable
species may be expected (e.g. Owen-Smith & Neiville, 1982;
Brambilla et al., 2006), presumably leading to both a longer
chewing and a reduction of bite rate (Moquin et al., 2010).
Accordingly, our data show that, for female chamois, the
bite rate was significantly affected by the spatial overlap
Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London
S. Lovari et al.
with red deer, irrespectively from the vegetation type. Thus,
a negative effect of red deer on the food intake rate of
chamois may be suggested.
Movements for food searching depend greatly on pat-
terns of distribution of food resources (e.g. Owen-Smith &
Neiville, 1982; Bunnell & Gillingham, 1985). The step rate
of female chamois increased mildly – not significantly – in
areas attended by red deer, although further data are
required (e.g. through the comparison between study areas
with/without red deer). Our results would also suggest that
the step rate has not increased, and the bite rate has
decreased (by c. 8%, in summer) with respect to 1984–1985,
when deer were not present (Bruno & Lovari, 1989), which
may support the view of a uniformly distributed poor
forage, presently. On the other hand, we showed (1) a great
overlap in diet and space between Apennine chamois and
red deer; (2) a reduction of food resources with respect to the
time when deer were absent; (3) a negative effect of overlap
with red deer on the bite rate of chamois. These results are
strongly suggestive of a negative effect of red deer on food
resources of chamois.
The decrease of chamois in their core range has been
determined by a great winter mortality of kids (Latini et al.,
2011). Mortality determined by inbreeding depression can
be ruled out as released, daughter populations of Apennine
chamois – which should be even more inbred than the
source population, i.e. ALMNP – show a high viability
(Mari & Lovari, 2006). In the last decade, the decrease in the
number of chamois in ALMNP has not been determined by
a density-dependent local decrease of female fecundity, as
birth rates have remained high in the core range of chamois
(median value number of kids : number of adult female
chamois, for 1976–1982: 0.70, Locati & Lovari, 1988; 2010:
0.62, 2011: 0.75, Ferretti & Lovari, unpubl. data). Chamois
numbers were stable during 1972–1987 (Lovari, 1985;
Dupré et al., 2001), but increased during 1993–1999 (up to
600 individuals), because of the protection accorded to
peripheral areas (Dupré et al., 2001). The stability of the
chamois population in its core range, on the last three
decades of the last century, militates strongly against a
recent density-dependent increase of kid mortality. The pre-
dation of bears (Fico, Locati & Lovari, 1984; Di Domenico
et al., 2012), wolves (Patalano & Lovari, 1993; Meriggi &
Lovari, 1996; Grottoli, 2011) and golden eagles (Locati,
1990; Bertolino, 2003) is negligible. No data on parasite
load are available from the 1980s, ruling out comparisons
with 2010–2011 (Latini et al., 2011). However, one should
expect that the parasite load will increase in individuals
weakened by food depletion (Craig et al., 2008; Hughes
et al., 2009).
A parallel decrease of chamois numbers has occurred in
other areas of ALMNP, outside our present study area, with
an intensity that seems approximately related to local deer
presence (Ferretti et al., unpubl. data). If red deer numbers
are the main factor triggering depletion of summer food
resources for Apennine chamois, there may be reason of
concern for the future of this vulnerable taxon. In the last
decades, 80–200 red deer have been reintroduced to each of
Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London
Competition between reintroduced red deer and Apennine chamois
several other Apennine national parks, where Apennine
chamois have also been reintroduced, and their numbers are
increasing. The main reason for deer reintroductions has
been to provide a prey supply for the wolf, to reduce live-
stock damage (e.g. Tassi, 1976; Boscagli, 1985). Most likely,
park size, forest distribution pattern, dispersion and quality
of food resources differ between these areas, which may
determine different ecological relationships between these
ruminants. Our results indicate that an increase of red deer
has the potential to determine a decline of Apennine
chamois, where they share the same limited food resource,
for example T. thalii communities, rare and extra-zonal in
the Apennines (Ferrari et al., 1988), home of the vulnerable
R. p. ornata. Pay-offs of reintroducing a locally extinct not-
threatened species should be carefully considered, when its
sharp increase may further endanger a threatened taxon,
thus determining an ecological risk rather than a conserva-
tion benefit (IUCN, 2012). In most European protected
areas, pristine habitats have been deeply altered by humans,
making their restoration difficult. Thus, both short- and
long-term consequences of restoring operations (costs and
benefits) have to be very carefully considered beforehand.
Acknowledgements
We are indebted to D. Febbo and G. Rossi for their con-
tinuous support and backing. We thank the wardens M.
Antonucci and M. D’Alessandro for their help in fieldwork,
as well as the ALMNP staff for logistic support. We are
grateful to two anonymous reviewers, the Associate Editor
and, especially, to D.M. Forsyth, who greatly improved
earlier drafts of this paper. We are grateful to D. Ubaldi for
his suggestions on vegetation analyses; to A. Catorci for his
comments on B. genuense ecology; to C. Guacci for infor-
mation on past grazing pressure. Financial support was pro-
vided by the ALMNP Agency (partly within the Project
LIFE09 NAT/IT/000183 Coornata, for some diet analyses).
S.L. planned and supervised the research work, as well as
participated in writing up all drafts; F.F. participated in
research planning and wrote the first draft, conducted most
behavioural observations and pellet group counts, as well as
worked out relevant data; M.C. conducted most vegetation
analyses and participated in writing up all drafts; I.M. con-
ducted food habit analyses and wrote about them; N.T.
participated in vegetation analyses; C.F. supervised vegeta-
tion analyses; A.S. conducted a part of behavioural obser-
vations, in 2010.
References
Alm Bergvall, U., Rautio, P., Kesti, K., Tuomi, J. &
Leimar, O. (2006). Associational effects of plant defences
in relation to within- and between-patch food choice by a
mammalian herbivore: neighbour contrast susceptibility
and defence. Oecologia 147, 253–260.
Altmann, J. (1974). Observational study of behaviour: sam-
pling methods. Behaviour 49, 227–267.
367
Competition between reintroduced red deer and Apennine chamois
Anthony, R.G. & Smith, N.S. (1977). Ecological relation-
ships between mule deer and white-tailed deer in South-
eastern Arizona. Ecol. Monogr. 47, 255–277.
Apollonio, M. & Lovari, S. (2001). Reintroduzioni di cervi
e caprioli nei parchi nazionali, con note sulle
immigrazioni naturali, In Progetto di monitoraggio
dello stato di conservazione di alcuni Mammiferi
particolarmente a rischio della fauna Italiana: 462–475.
Lovari, S. & Sforzi, A. (Eds). Roma: Ministero
dell’Ambiente.
Armstrong, D.P. & Seddon, P.J. (2008). Directions in rein-
troduction biology. Trends Ecol. Evol. 23, 20–25.
Augustine, D.J. & McNaughton, S.J. (1998). Ungulate
effects on the functional species composition of plant
communities: herbivore selectivity and plant tolerance.
J. Wildl. Manage. 62, 1165–1183.
Berger, J. (1985). Interspecific interactions and dominance
among wild great basin ungulates. J. Mammal. 66, 571–
573.
Bertolino, S. (2003). Herd defensive behaviour of chamois,
Rupicapra rupicapra, in response to predation on the
young by a golden eagle, Aquila chrysaetos. Mammalia
49, 233–236.
Bertolino, S., di Montezemolo, N.C. & Bassano, B. (2009).
Food-niche relationships within a guild of Alpine
ungulates including an intriduced species. J. Zool. 277,
63–69.
Blasi, C. (1994). Fitoclimatologia del Lazio. Fitosociologia
27, 151–175.
Blasi, C., Di Pietro, R. & Pelino, G. (2005). The vegetation
of alpine belt karst-tectonic basins in the central
Apennines (Italy). G Bot Ital 139, 357–385.
de Boer, W.F. & Prins, H.H.T. (1990). Large herbivores
that strive mightily but eat and drink as friends.
Oecologia 82, 264–274.
Boitani, L., Lovari, S. & Vigna Taglianti, A. (2003).
Mammalia III: Carnivora – Artiodactyla, In Fauna
d’Italia, Vol. XXXVIII. Bologna: Calderini.
Boscagli, G. (1985). Il lupo: Udine: Lorenzini.
Brambilla, P., Bocci, A., Ferrari, C. & Lovari, S. (2006).
Food patch distribution determines home range size of
adult male chamois only in rich habitats. Ethol. Ecol.
Evol. 18, 185–193.
Braun-Blanquet, J. (1964). Pflanzensoziologie, 3rd edn:
Wien, New York: Springer.
Bruno, E. & Lovari, S. (1989). Foraging behaviour of
adult female Apennine chamois in relation to
seasonal variation in food supply. Acta Theriol. 34, 513–
523.
Bunnell, F.L. & Gillingham, M.P. (1985). Foraging behav-
iour: dynamics of dining out, In Bioenergetics of wild her-
bivores: 53–79. Hudson, R.J. & White, R.G. (Eds). Boca
Raton: CRC Press.
Catorci, A., Ottaviani, G., Vitasović Kosić, I. & Cesaretti,
S. (2011). Effect of spatial and temporal patterns of stress
368
S. Lovari et al.
and disturbance intensities in a sub-Mediterranean grass-
land. Plant Biosyst. 146, 352–367.
Catorci, A., Antolini, E., Tardella, F.M. & Scocco, P.
(2013). Assessment of interaction between sheep and
poorly palatable grass: a key tool for grassland manage-
ment and restoration. J. Plant Interact. http://dx.doi.org/
10.1080/17429145.2013.776706
Caughley, G. (1970). Eruption of ungulate populations,
with emphasis on Himalayan tahr in New Zealand.
Ecology 51, 53–72.
Cederna, A. & Lovari, S. (1985). The impact of tourism on
chamois feeding activities in an area of the Abruzzo
National Park, Italy, In The biology and management of
mountain ungulates: 216–225. Lovari, S. (Ed.). London:
Croom Helm.
Clutton-Brock, T.H., Guinness, F.E. & Albon, S.D. (1982).
Red deer. Behavior and ecology of two sexes: Chicago:
Chicago University Press.
Clutton-Brock, T.H., Albon, S.D. & Guinness, F.E. (1984).
Maternal dominance, breeding success and birth sex
ratios in red deer. Nature 308, 358–360.
Clutton-Brock, T.H., Albon, S.D. & Guinness, F.E. (1986).
Great expectations: dominance, breeding success and off-
spring sex ratios in red deer. Anim. Behav. 34, 460–471.
Côté, S. & Festa-Bianchet, M. (2001b). Reproductive
success in female mountain goats: the influence of age
and social rank. Anim. Behav. 62, 173–181.
Côté, S.D. & Festa-Bianchet, M. (2001a). Birthdate, mass
and survival in mountain goat kids: effects of maternal
characteristics and forage quality. Oecologia 127, 230–
238.
Craig, B.H., Tempest, L.J., Pilkington, J.G. & Pemberton,
J.M. (2008). Metazoan–protozoan parasite co-infections
and host body weight in St Kilda Soay sheep. Parasitol-
ogy 135, 433–441.
Crawley, M.J. (2007). The R Book: Chichester: John Wiley
& Sons, Ltd.
D’Angeli, D., Testi, A., Fanelli, G. & Bianco, P.M. (2011).
A focus on the landscape mosaics: vegetation map of
‘Serra Rocca Chiarano – Monte Greco’ S.C.I (Abruzzo,
Central Apennines).
Di Domenico, G., Tosoni, E., Boitani, L. & Ciucci, P.
(2012). Efficiency of scat-analysis lab procedures for bear
dietary studies: the case of the Apennine brown bear.
Mamm. Biol. 77, 190–195.
Dupré, E., Monaco, A. & Pedrotti, L. (2001). Piano
d’azione nazionale per il Camoscio appenninico
(Rupicapra pyrenaica ornata). Quad Cons. Natura 10,
1–139. Min. Ambiente – Ist. Naz. Fauna Selvatica.
Fattorini, L., Ferretti, F., Pisani, C. & Sforzi, A. (2011).
Two-stage estimation of ungulate abundance in Mediter-
ranean areas using pellet group count. Envir Ecol Stat.
18, 291–314.
Ferrari, C., Rossi, G. & Cavani, C. (1988). Summer food
habits and quality of female, kid and subadult Apennine
Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London
S. Lovari et al.
chamois, Rupicapra pyrenaica ornata Neumann, 1899
(Artiodactyla, Bovidae). Z. Sauegetierk. 53, 170–177.
Ferretti, F., Sforzi, A. & Lovari, S. (2008). Intolerance
amongst deer species at feeding: roe deer are uneasy ban-
queters. Behav. Process. 78, 487–491.
Ferretti, F., Sforzi, A. & Lovari, S. (2011). Behavioural inter-
ference between ungulate species: roe are not on velvet
with fallow deer. Behav. Ecol. Sociobiol. 65, 875–887.
Festa-Bianchet, M. (1998a). Birthdate and survival in
bighorn lambs (Ovis canadensis). J. Zool. 214, 653–661.
Festa-Bianchet, M. (1998b). Condition-dependent reproduc-
tive success in bighorn ewes. Ecol. Lett. 1, 91–94.
Fico, R., Locati, M. & Lovari, S. (1984). A case of brown
bear predation on Abruzzo chamois. Säugetierkd. Mitt.
31, 185–187.
Focardi, S., Aragno, P., Montanaro, P. & Riga, F. (2006).
Inter-specific competition from fallow deer Dama dama
reduces habitat quality for the Italian roe deer Capreolus
capreolus italicus. Ecography 29, 407–417.
Forsyth, D.M. (1997). Ecology and management of Himala-
yan thar and sympatric chamois in the Southern Alps,
New Zealand. Ph.D. Thesis, University of Lincoln.
Forsyth, D.M. & Caley, P. (2006). Testing the irruptive
paradigm of large-herbivore dynamics. Ecology 87, 297–
303.
Forsyth, D.M. & Hickling, G.J. (1998). Increasing Himala-
yan tahr and decreasing chamois densities in the eastern
Southern Alps, New Zealand: evidence for interspecific
competition. Oecologia 113, 377–382.
Forsyth, D.M., Barker, R.J., Morriss, G. & Scroggie, M.P.
(2007). Modeling the relationship between fecal pellet
indices and deer density. J. Wildl. Manage. 71, 964–970.
Frid, A. (1997). Vigilance by Dall’s sheep: interactions
between predation risk factors. Anim. Behav. 53, 799–808.
Gottfried, M., Pauli, H., Futschik, A. et al. (2012).
Continent-wide response of mountain vegetation to
climate change. Nature Climate Change 2, 111–115.
Grottoli, L. (2011). Assetto territoriale ed ecologia
alimentare del lupo (Canis lupus) nel Parco Nazionale
d’Abruzzo, Lazio e Molise. PhD Thesis. Università di
Roma La Sapienza.
Herrero, J., Lovari, S. & Berducou, C. (2008). Rupicapra
rupicapra. IUCN 2010. IUCN Red List of Threatened
Species. Version 2010 (www.iucnredlist.org).
Hewison, A., Gaillard, J., Kjellander, P., Toïgo, C., Liberg,
O. & Delorme, D. (2005). Big mothers invest more in
daughters: reversed sex allocation in a weakly
polygynous mammal. Ecol. Lett. 8, 430–437.
Hofmann, R.R. (1989). Evolutionary steps of
ecophysiological adaptation and diversification of rumi-
nants: a comparative view of their digestive system.
Oecologia 78, 443–457.
Hughes, J., Albon, S.D., Irvine, R.J. & Woodin, S. (2009).
Is there a cost of parasites to caribou? Parasitology 136,
253–265.
Animal Conservation 17 (2014) 359–370 © 2014 The Zoological Society of London
Competition between reintroduced red deer and Apennine chamois
IUCN (2012). IUCN Guidelines for Reintroductions and
other conservation translocations: Gland: SSC/
Reintroduction Specialist Group.
Jaccard, P. (1901). Étude comparative de la distribution
florale dans une portion des Alpes et des Jura. Bull. Soc.
Vaud. Sci. Nat. 37, 547–579.
Johnson, M.K., Wofford, H. & Pearson, H.A. (1983).
Microhistological techniques for food habits analyses. Res.
Pap. SO-199, Department of Agriculture Forest Service
Southern Forest Experiment Station, New Orleans.
Latham, J. (1999). Interspecific interactions of ungulates in
European forests: an overview. For. Ecol. Manage. 120,
13–21.
Latham, J., Staines, B.W. & Gorman, M.L. (1997). Correla-
tions of red (Cervus elaphus) and roe (Capreolus
capreolus) deer densities in Scottish forests with environ-
mental variables. J. Zool. 242, 681–704.
Latini, R. (2010). Relazione dell’attività di pellet group
count. Monitoraggio ungulati selvatici – ANNO 2010.
Ente Parco Nazionale d’Abruzzo, Lazio, Molise, unpub-
lished report.
Latini, R., Gentile, L., Asprea, A., Pagliaroli, D., Argenio,
A. & Di Pirro, V. (2011). Stato dell’arte delle azioni A4 e
C2 – Dicembre 2011. Ente Parco Nazionale d’Abruzzo,
Lazio e Molise, unpublished report.
Latini, R., Asprea, A. & Pagliaroli, D. (2012). Conteggi in
simultanea e monitoraggio della popolazione di
Camoscio appenninico nel PNALM: nota sintetica dei
risultati estivi 2012. Ente Parco Nazionale d’Abruzzo,
Lazio, Molise, unpublished report.
Leopold, A. (1943). Deer irruptions. Wis. Cons. Bull. 8,
3–11.
Lindström, J. (1999). Early development and fitness in birds
and mammals. Trends Ecol. Evol. 14, 343–348.
Locati, M. (1990). Female chamois defends kids from eagle
attacks. Mammalia 54, 155–156.
Locati, M. & Lovari, S. (1988). La socialità nel camoscio
appenninico Rupicapra pyrenaica ornata (Neumann,
1899): confronto tra i sessi e suggerimenti di gestione.
Atti I Convegno Nazionale di Biologia della Selvaggina,
Bologna: 561.
Lovari, S. (1977). The Abruzzo chamois. Oryx 14, 47–50.
Lovari, S. (1979). Etologia di campagna: Torino: Bollati
Boringhieri.
Lovari, S. (1984). Il popolo delle rocce: Torino: Rizzoli.
Lovari, S. (1985). Behavioural repertoire of the Abruzzo
chamois, Rupicapra pyrenaica ornata Neumann,
1899 (Artiodactyla: Bovidae). Säugetierkd. Mitt. 32, 113–
136.
Lovari, S., Artese, C., Damiani, G. & Mari, F. (2010).
Re-introduction of Apennine chamois to the Gran Sasso-
Laga National Park, Abruzzo, Italy, In Global
re-introduction perspectives: additional case-studies from
around the globe: 281–284. Soorae, P.S. (Ed.). Abu
Dhabi: IUCN/SSC Re-introduction Specialist Group.
369
 Competition between reintroduced red deer and Apennine chamois
Lummaa, V. & Clutton-Brock, T. (2002). Early develop-
ment, survival and reproduction in humans. Trends Ecol.
Evol. 17, 141–147.
Mari, F. & Lovari, S. (2006). Il camoscio appenninico: un
ritorno in corso, In Salvati dall’arca: 131–142. Fraissinet,
M. & Petretti, F. (Eds). Udine: Perdisa.
Masini, F. & Lovari, S. (1988). Systematics, phylogenetic
relationships and dispersal of the chamois Rupicapra spp.
Quat. Res. 30, 339–349.
Mayle, B.A., Peace, A.J. & Gill, R.M.A. (1999). How many
deer? A field guide to estimating deer population size:
Edinburgh: Forestry Commission Field Book 18.
Meriggi, A. & Lovari, S. (1996). A review of wolf predation
in Southern Europe: does the wolf prefer wild prey to
wildstock? J. Appl. Ecol. 33, 1561–1571.
Minder, I. (2012). Local and seasonal variations of roe deer
diet in relation to food resource availability in a Mediter-
ranean environment. Eur. J. Wildl. Res. 58, 215–225.
Moquin, P., Curry, B., Pelletier, F. & Ruckstuhl, K.E.
(2010). Plasticity in the rumination behaviour of bighorn
sheep: contrasting strategies between the sexes? Anim.
Behav. 79, 1047–1053.
Mustoni, A., Pedrotti, L., Tosi, G. & Zanon, E. (2002).
Ungulati delle Alpi: biologia, riconoscimento, gestione:
Trento: Nitida Immagine.
Namgail, T., Mishra, C., de Jong, C.B., van Wieren, S.E. &
Prins, H.H.T. (2007). Effects of herbivore species richness
on the niche dynamics and distribution of blue sheep in
the Trans-Himalaya. Divers. Distrib. 15, 940–947.
Neuhaus, P. & Ruckstuhl, K.E. (2002). Foraging behaviour
in Alpine ibex (Capra ibex): conseguences of reproductive
status, body size, age and sex. Ethol. Ecol. Evol. 14, 373–
381.
Owen-Smith, N. & Neiville, P. (1982). What should a clever
ungulate eat? Am. Nat. 119, 151–178.
Patalano, M. & Lovari, S. (1993). Food habits and trophic
niche overlap of the wolf (Canis lupus, L. 1758) and the
red fox Vulpes vulpes (L. 1758) in a Mediterranean
mountain area. Rev. Ecol. 48, 279–294.
Petraglia, A. & Tomaselli, M. (2007). Phytosociological
study of the snowbed vegetation in the Northern
Apennines (Northern Italy). Phytocoenologia 37, 67–98.
Pettorelli, N., Gaillard, J.M., Yoccoz, N.G., Duncan, P.,
Maillard, D., Delorme, D., Van Laere, G. & Toïgo, C.
(2005). The response of fawn survival to changes in
habitat quality varies according to cohort quality and
spatial scale. J. Anim. Ecol. 74, 972–981.
Pettorelli, N., Pelletier, F., von Hardenberg, A.,
Festa-Bianchet, M. & Côté, S.D. (2007). Early onset of
370
View publication stats
S. Lovari et al.
vegetation growth vs. rapid green-up: impacts on juvenile
mountain ungulates. Ecology 88, 381–390.
Pianka, E.R. (1973). The structure of lizard communities.
Ann. Rev. Ecol. Syst. 4, 53–74.
Putman, R.J. (1996). Competition and resource partitioning
in temperate ungulate assemblies: London: Chapman &
Hall.
Putman, R.J. & Sharma, S.K. (1987). Long term changes in
New Forest deer populations and correlated environmen-
tal change. Symp. Zool. Soc. Lond. 58, 167–179.
R Development Core Team (2009). R: a language and envi-
ronment for statistical computing: Vienna: R Foundation
for Statistical Computing.
Richard, E., Gaillard, J.M., Saïd, S., Hamann, J.L. &
Klein, F. (2010). High red deer density depresses body
mass of roe deer fawns. Oecologia 163, 91–97.
Rossi, G. (1985). Osservazioni sull’alimentazione del
camoscio appenninico (Rupicapra pyrenaica ornata).
Primo contributo. MSc Thesis, Università di Bologna.
Ruckstuhl, K.E., Festa-Bianchet, M. & Jorgenson, J.T.
(2003). Bite rates in Rocky Mountain bighorn sheep
(Ovis canadensis): effects of season, age, sex and repro-
ductive status. Behav. Ecol. Sociobiol. 54, 167–173.
Schöb, C., Kammer, P.M., Choler, P. & Veit, H. (2009).
Small-scale plant species distribution in snowbeds and its
sensitivity to climate change. Plant Ecol. 200, 91–104.
Schröder, J. & Schröder, W. (1984). Niche breadth and
overlap in red deer Cervus elaphus, roe deer Capreolus
capreolus and chamois Rupicapra rupicapra. A. Zool.
Fenn. 172, 85–86.
Sinclair, A.R.E. & Northon-Griffiths, M. (1982). Does com-
petition or facilitation regulate migrant ungulate popula-
tions in the Serengeti? A test of hypotheses. Oecologia 53,
364–369.
Smith, D.W., Peterson, R.O. & Houston, D.B. (2003).
Yellowstone after wolves. Bioscience 53, 330–340.
Sokal, R.R. & Rohlf, F.J. (1995). Biometry: the principles
and practice of statistics in biological research, 3rd edn:
New York: W. H. Freeman.
Tassi, F. (1976). La reintroduzione degli ungulati nell’-
Appennino Centrale. Camerino and Roma: SOS Fauna:
Animali in Pericolo Di Estinzione.
Supporting information
Additional Supporting Information may be found in the
online version of this article at the publisher’s web-site:
Appendix S1. Supplementary online material.
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