Biological Conservation 126 (2005) 582–590
www.elsevier.com/locate/biocon
Application of central-place foraging theory shows the importance
of Mediterranean dehesas for the conservation of
the cinereous vulture, Aegypius monachus
Martina Carrete ¤, José A. Donázar
Department of Applied Biology, Estación Biológica de Doñana (CSIC), Pabellón del Perú, Avda. María Luisa s/n, 41013 Sevilla, Spain
Received 2 January 2005; received in revised form 18 June 2005; accepted 24 June 2005
Available online 22 August 2005
Abstract
The dehesa (oak woodland) is an extensive agro-pastoral ecosystem characteristic of the Western Mediterranean countries which
is suVering a great transformation process since 1950. Although its distribution largely overlaps with several endangered species,
there is scarce information on how they use this human-transformed habitat. We studied the foraging habitat selection of one of
them, the cinereous vulture Aegypius monachus. We radio-tracked 14 cinereous vultures in one of the largest European colonies from
1998 to 2000. Used and available habitats were compared at two scales using compositional analysis. Moreover, we developed a distance-based GLMM for assessing habitat selection in this central-place forager species, by taking into account the spatial distribution of habitat patches in relation to the location of the colony. Home ranges overlapped over a total surface of 592,527 ha around
the colony, and both individual home ranges and travel foraging distances (mean 27.86 km, maximum 86 km) were larger during the
breeding season. All cinereous vultures avoided agricultural lands within their home ranges throughout the year. Habitat use in relation to the distance to the colony pointed out that dehesas were positively selected in spite of being on average far away from the colony than other habitats, a result that was consistent among individuals and seasons. The cinereous vulture thus depends for its
conservation not only on the protection of breeding areas, as has been so far considered, but also on the maintenance of well-conserved dehesas close to the colonies. Preserving the cinereous vultures could contribute to the economic sustainability of dehesas by
attracting PAC funds for their traditional low-intensity exploitation. Although other species may also beneWt from this study since
cinereous vulture could be a “Xagship” for the large-scale conservation of Mediterranean oak woodlands and associated biodiversity, more Wne local management guidelines should be performed on the basis of studies on more sensitive species.
2005 Elsevier Ltd. All rights reserved.
Keywords: Central-place forager; Cinereous vulture; European Common Agricultural Policy; Large-scale conservation; Spain
1. Introduction
European Mediterranean landscapes have been
largely transformed by human activities over the last
10,000 years (Le Honerou, 1981). Agriculture development, grazing, silvicultural practices and natural and
human-induced disturbances such as Wres have been the
*
Corresponding author. Tel.: +34 95 423 23 40; fax: +34 95 462 11
25.
E-mail address: martina@ebd.csic.es (M. Carrete).
0006-3207/$ - see front matter 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2005.06.031
rule in most of the Mediterranean basin and, although
such changes have reduced the extent of the primary biotopes, in many cases they have created new semi-natural
habitats from which many animal species became dependent (e.g., Bignal and McCracken, 1996; Beaufoy, 1998;
Díaz et al., 2003). Oak woodlands, for example, are
mainly found in the Iberian Peninsula (but see
Standiford et al., 2003 for more details on their worldwide distribution). Locally called dehesas (Spain) or
“montados” (Portugal), this habitat type was a wood
mainly composed by Quercus species which has been
M. Carrete, J.A. Donázar / Biological Conservation 126 (2005) 582–590
transformed into a savanna-like habitat, with scattered
trees reaching densities of 40–50 trees/ha, because of
their use for livestock. The soil, sometimes occupied by
small agriculture Welds, is generally covered by herbaceous plants which are proWted by sheep and cows while
tree acorn production is usually consumed by the economically appreciated hairless black pigs.
The dehesas cover almost 3,000,000 ha of south-western Spain and Portugal (JoVre and Rambal, 1993). Its
value for the conservation of the biodiversity has been
repeatedly remarked. Besides holding a high diversity of
plants (Pineda et al., 1981; Ruiz, 1986), its faunal richness is also considerable. As was stated by the reviews of
Beaufoy (1998) and Díaz et al. (2003), dehesas and spatially related habitats as scrublands and woodlands
maintain the main Western Palearctic and, in some
cases, world populations of species considered as globally threatened or near-threatened such as the Spanish
Imperial eagle Aquila adalberti, the cinereous vulture
Aegypius monachus and the Iberian Lynx Lynx pardina
(The 2004 IUCN Red List of the Threatened Species;
information available at http://www.redlist.org/). These
species, and many other predator vertebrates (see Beaufoy, 1998), prey mainly on wild rabbits Oryctolagus
cuniculus whose densities in these habitats reach up to 15
individuals/ha (I. Fajardo, pers. com.). In addition, avian
scavengers such as vultures and kites Milvus spp. rely on
the carcasses of livestock (sheep, goats and cattle) maintained in these extensive exploitations. Wintering birds
such as common cranes Grus grus, wood pigeons
Columba palumbus or many passerine species use oak
acorns as food source to increase their fat reserves (e.g.,
Herrera, 1977; Díaz et al., 1996, 1997). In spring, when
the annual peak in number and biomass of arthropods
occurs (Herrera, 1980), the bird community of the dehesas includes many near-threatened or vulnerable insectivorous species (e.g., shrikes Lanius meridionalis,
L. senator, rollers Coracias garrulus) and top predators
(e.g., black-shouldered kite Elanus caeruleus, booted
eagle Hieraaetus pennatus, scops Otus scops and tawny
owls Strix aluco Díaz et al., 1997).
Unfortunately, and except for some studies carried
out in protected zones with relatively well-conserved
original habitats as those found in the Doñana National
Park and surrounding lands (see e.g., Heredia et al.,
1991; Revilla et al., 2000), there is scarce information
about the actual use that populations of endangered species, mainly raptors, make of dehesas and other related
human-transformed Mediterranean habitats. This is of
special interest when considering that large predators
and scavengers usually travel long distances during their
foraging trips, going outside the boundaries of protected
areas and potentially exploiting patches with diVerent
degrees of transformation. Thus, a better understanding
of the use of man-made landscapes by these species
would be essential for management and conservation
583
purposes. Moreover, considering that since the 1950s
dehesas are suVering conversion to monocultures of
eucalyptus species and exotic pines (mainly until 1980s),
overgrazing, abandonment of tree management, tree
regeneration failures and conversion to irrigated land
(Díaz et al., 1997; Pulido et al., 2001), this information
could be useful to delineate future European compensation measures based on an optimal habitat design for the
conservation of endangered taxa.
The cinereous vulture could be considered a representative species of this habitat type because its largest European breeding distribution, located in Spain (see below),
largely overlaps with the distribution of dehesas (Fig. 1).
Listed as globally near-threatened (IUCN, 2003; http://
www.redlist.org/) and considered as rare in Europe (BirdLife International, 2004) and vulnerable in Spain (Sánchez-Artés, 2004), the breeding population of this large
scavenger showed a sharply decline through the XIX–
XXth centuries, reaching extinction in most of its former
range (see Cramp and Simmons, 1980). In 2000, and after
a recovering period, European breeding numbers were
estimated in 1435–1977 pairs, of which 1203–1295
(approx. 70–80%) occur in Spain (Donázar, 2002). There,
it is known that local populations are aVected, among
other factors, by illegal poisoning and disturbances in
breeding areas (see Donázar et al., 2002) although no
information exists about how they use the diVerent
human-altered habitats that commonly found during
their foraging activities. In fact, it should be noted that
national and international conservation measures for this
tree-nesting species are addressed to protect breeding
colaonies but nothing is mentioned about the importance
Fig. 1. Distribution of the dehesas (light grey; Standiford et al., 2004) and
the breeding cores of cinereous vultures (dark grey; Martí and del Moral,
2003) in the Iberian Peninsula. The circle shows the study area.
584
M. Carrete, J.A. Donázar / Biological Conservation 126 (2005) 582–590
of maintaining its foraging habitats (Sánchez-Artés,
2004; Poirazidis et al., 2004). Contrarily, actions proposed are linked with the creation of “vulture restaurants” for artiWcial food supply (Sánchez-Artés, 2004)
without a clear understanding of its role in the conservation of the species (but see Vlachos et al., 1999).
The aim of this paper was to examine the foraging
habitat selection pattern of cinereous vultures breeding
in the largest colony of Southern Spain in relation to the
spatial distribution of dehesas. The species, which is at
the “top” of the food web as consumer of carcasses of
livestock and wild animals, may search through enormous land surfaces (see e.g., Mundy et al., 1992; Donázar, 1993) because of its large body-size and energetic
requirements and the spatio-temporal unpredictability
of its food resources. However, breeding birds are tied to
the colony year-round (Donázar, 1993), behaving as central-place foragers (Orians and Pearson, 1979) which are
obliged to return every day to their nest or roost-site at
the colony. Hence, its foraging habitat selection pattern
would be the result of a trade-oV between the quality of
the diVerent patches (food-rich and food-poor habitats)
and the distance at which they are located (low and high
Xight cost;). Information about this subject may be critical for a good design of conservation strategies for this
vulnerable raptor as well as for traditional agro-grazing
systems in broad regions of the Iberian Peninsula.
2. Study area
Sierra Pelada is located at the western end of the
Sierra Morena range, south-western Spain (37°51⬘10⬙N,
7°03⬘30⬙W), occupying around 40,000 ha of low mountains that range up to an altitude of 613 m.a.s.l. Annual
rainfall is around 1000 mm3 and mean temperature is
15 °C. Although the natural vegetation was Mediterranean forest of evergreen, holm, and cork oaks
(Quercusilex and Q. suber) with small patches of other
tree species such as black alders Alnus glutinosa and
strawberry trees Arbutus unedo, the area was deforested
in the past for grazing activities, resulting in an open
landscape dominated by Mediterranean scrubland with
scattered woodland patches and isolated trees. In the
1960s and 1970s, the area underwent extensive transformation, with more than 70% of the land being reforested
with eucalyptus trees (Eucalyptus spp.) and non-native
pines (Pinus pinaster and Pinus pinea). In 1989, 13,000 ha
were declared as “natural area” with the main aim of
conserving the cinereous vulture breeding colony located
in this already degraded place. Currently, in
2,323,527.36 ha around the breeding colony (our study
area, see below), the dominant land-uses are crops (33%,
mainly extensive croplands), dehesas (23%), open lands
(19%, mainly grasslands and shrublands) and exotic forest (17% and 3%, for eucalyptus and pines, respectively).
The cinereous vulture breeding colony has
increased from 45 pairs in the early 1970s (Hiraldo,
1974) to 90–100 pairs in 1993 (Andalus, 1996; authors’
unpublished), decreasing to 72 pairs in 1998 (authors’
unpublished). Causes of decline have been mainly attributed to illegal poisoning and disturbances in breeding
areas (see Donázar et al., 2002).
3. Methods
3.1. Field procedures
During the winters of 1997, 1998 and 1999, we
equipped with battery-operated transmitters (battery
life: 2 years; Ayama, Biotrack and Wagner) 14 cinereous
vultures (6 in 1997, 3 in 1998 and 5 in 1999) breeding in
the Sierra Pelada colony. Birds were captured with
rocket nets close to the breeding colony, by baiting them
with carrions of livestock. Each vulture (10 males and 4
females, sexed though molecular procedures) was radiotracked an average of 44 days (range: 10–104 days) from
March 1998 to June 2000, investing a total of 321 Weldwork days. We used two radio-tracking teams. The Wrst
one was located, in alternative surveys, in a high point at
the north or at the south of the breeding colony. The second team moved by car, intensively searching for birds
in a radius of up to 100 km around the other team. Each
team recorded the exact hour and the direction of each
radio-location to triangulate vulture positions. Triangulation was performed with the programme LOAS (available at http://www.ecostats.com/index.htm). As locations
obtained by biangulations are subject to biases when the
resulting angle diVers from 90° (White and Garrot,
1990), we were conservative selecting radiolocations and
thus we considered only those that corresponded to foraging birds, obtained with two radio-locations within
a period of 10 min and included within the range of
30–150°. Thus, we discarded approximately 40% of
radiolocation data and the resulting dataset for analyses
comprised 711 used points.
3.2. Data analysis
3.2.1. Home range and habitat selection
Home range size was obtained with the RANGES V
package (Kenward and Hodder, 1996), using the 95%
Wxed kernel estimator (Worton, 1989, 1995). When it was
possible (number of radiolocations 710; see below), we
calculated the home ranges of adult birds for both, the
breeding (February–July) and the non-breeding
(August–January) season.
Using the compositional analysis proposed by Aebischer et al. (1993), we compared utilized and available
habitats at two scales: (1) home range selection within
the overall study area and (2) habitat selection within
M. Carrete, J.A. Donázar / Biological Conservation 126 (2005) 582–590
the home range. For the Wrst case, we considered that
the study area was a circle of 86 km of radius (the maximum travel distance recorded during the study period;
see results) centred in the vulture colony. For the
second one, we used the 95% Wxed kernel probability as
an estimator of the home range of each individual. The
compositional analysis, whose main advantage is to
avoid biases due to the non-independence of proportions in habitat use, ranks habitats according to their
relative use. After obtaining the diVerence d between
the log-ratios of availability and use of each habitat,
and taking the data matrix of d values for each individual and habitat as a basis, it calculates the relation
between the determinant of the matrix of mean-corrected sums of squares and cross-products (hypothesis
tested: diVerential habitat use) and the determinant of
the matrix of raw sums of squares and cross products
(hypothesis tested: identical habitat use). The signiWcance of is then tested by means of the expression
¡Nln, where N is the number of animals radiotracked, which follows a chi-square distribution. To
determine where the diVerences lie in habitat use and to
order the habitats according to their use for every individual, a table of relative use of each habitat is constructed, calculating for each comparison between
habitats the proportion in which it is used with respect
to the available proportion. Finally, habitat preference
in each habitat comparison is compared with a random
distribution provided by a computer program (J.F.
Calvo, unpublished).
The use of a habitat patch by a central-place forager
such as the cinereous vulture, that returns to the colony
through the year for breeding and/or roosting, could be
aVected by both the habitat’s quality and proximity to
the central place (see e.g., Rosenberg and McKelvey,
1999; Peach et al., 2004; Franco and Sutherland, 2004).
Thus, we complementarily developed Generalized Linear Mixed Models (link function: logistic, error distribution: binomial; McCullagh and Searle, 2000) to describe
mathematically the probability that a certain point
within the study area was used by birds. The dataset
included radiolocations of individuals (value 1) and an
equal number of randomly selected points not used
(value 0) but included within the study area (see above).
Random points were obtained as independent x,y random coordinates within a uniformly sampled circular
plot.
Circular plots of 2 km of diameter around each radiolocation and random point were used to extract habitat
features, considering that this could be the area that a
vulture could be prospecting when it was located (Donázar, 1993). We used a forward stepwise procedure to
build models in which only signiWcant eVects were
retained (Donázar et al., 1993). There, the proportion of
each habitat was Wrst tested separately, by considering
its linear and quadratic forms and including simulta-
585
neously the distance of each point to the colony (distance) and the interaction between habitat and distance
to the colony (habitat X distance). By this way, we can
test not only for habitat preferences but also for potential constraints imposed by heterogeneity in spatial habitat distribution (Mysterud and Ims, 1998). After
selecting the most important habitat type, we tried to
incorporate the others, as well as their distances to the
colony and the corresponding interactions to build multivariable models. In the construction of models, “individual” was always included as a random factor to
control for the potential non-independence of data as
well as to test for possible inter-individual diVerences in
habitat selection, while “sex” (male and female) and
“season” (breeding and non-breeding season) were considered as Wxed eVects (Serrano et al., 2001). A model
was signiWcant if the probability associated with its
coeYcients was lower than 0.05. For each signiWcant
model, we calculated the percentage of deviance
explained (100 ¤ (100 ¡ deviancemodel)/deviancenull model).
3.2.2. Habitat types
The percentages of the diVerent habitat types for the
compositional analysis as well as for the radiolocations
and the random points were obtained from the
CORINE Land Cover database (CEC, 1991) by using
the XTools extension (available at http://www.odf.state.
or.us/stateforests/sfgis) of ArcView GIS 3.2. Although
this general-purpose land-cover map of Europe has a
relatively coarse resolution (100 m), it has been proved to
be good enough to build broad habitat models of bird
distribution (Seoane et al., 2004). Habitats were grouped
in 4 categories that cover together more than 95% of the
study area: exotic forest of eucalyptus trees (Eucalyptus
spp.) and non-native pines such as P. pinaster and
P. pinea (hereafter, exotic forest), dehesas, agriculture
lands and open areas such as grasslands and scrublands.
Other habitats unsuitable for this species such as urban
areas or seacoast and open sea were not considered in
the analysis.
4. Results
4.1. Home range
The overall home range of the colony, estimated as a
minimum by overlapping the home ranges of the 14 cinereous vultures radio-tracked, reached 592,527 ha. Each
one of the individual home ranges mainly included open
areas (28–31%), dehesas (25–30%) and exotic forest (21–
29%). There were no changes in their relative habitat
composition through the year (p-range D 0.076–0.397) in
spite of their size contraction during the non-breeding
season (breeding season: 135,430 § 61,191 ha, n D 14, and
non-breeding season: 77,775 § 38,365 ha, n D 6; Mann–
586
M. Carrete, J.A. Donázar / Biological Conservation 126 (2005) 582–590
Table 1
Home ranges of cinereous vultures during the breeding (February–
July) and non-breeding (August–January) season in south-western
Spain
of locations for each bird and their home range sizes
were not related (breeding season: r D 0.47, p D 0.094;
non-breeding season: r D 0.24, p D 0.645).
IND SEX Breeding season
4.2. Habitat selection
Non-breeding season
No. of
Home range (ha) No. of
Home range (ha)
locations
locations
102
103
104
105
106
107
109
110
111
112
113
114
115
117
M
F
M
M
M
M
M
M
F
F
M
M
F
M
25
71
49
43
51
61
76
17
25
10
22
20
21
19
126,706.1a
133,197.2a
288,670.9a
162,442.2a
127,512.5a
238,816.1a
109,699.4a
130,269.7
116,260.4
57,700.69
76,145.4
83,736.18
120,357.3
124,506.3
23
16
56
25,482.10
89,771.44
104,413.60
23
20
25
38,215.06
124,259.70
84,507.05
IND, individual code; F, female; M, male.
a
Home ranges with stabilized area (for more details, see text).
Fig. 2. Home ranges of male (M) and female (F) cinereous vultures
during the breeding and the non-breeding seasons. Sample sizes:
Breeding season: M D 10, F D 4; non-breeding season: M D 5, F D 1.
Whitney U-test D 15, p D 0.026), when travel distances
were shorter (breeding season median: 27.86 km, n D 14,
and non-breeding season median: 24.61 km, n D 6;
Mann–Whitney U-test D 40,090, p D 0.002). Males and
females showed similar proportions of each habitat type
within their home ranges (p-range D 0.374–0.945), which
were also similar in size (males: 123,025 § 68,110 ha,
n D 10, and females: 103,457 § 30,062 ha, n D 4; Mann–
Whitney U-test D 33, p D 0.694) even during the
breeding season (males: 146,851 § 67,273 ha, n D 10,
and females: 106,879 § 33,570 ha, n D 4; Mann–Whitney
U-test D 13, p D 0.322). We can assume that these home
range sizes were reasonably estimated with the available
sample size (see Table 1 and Fig. 2) because the number
The compositional analysis indicated that the home
ranges of cinereous vultures were not established at random within the study area during the breeding period
( D 9.34 £ 10¡2, 2 D 33.18, d.f. D 3, p < 0.0001, n D 14
individuals). The ranking matrix (sequence of habitat
types: open lands > exotic forests > dehesas > agriculture
lands) showed that agricultural lands were signiWcantly
less used than any other habitat (p-range D 0.0157–
0.0190), while there were not detectable diVerences in the
intensity of use of the rest (p-range D 0.0938–0.4467).
Within the home ranges, however, habitat use seemed
always proportional to its availability ( D 0.70,
2 D 4.97, d.f. D 3, p D 0.174, n D 14 individuals). Results
were similar during the non-breeding season (Home
range vs. study area: D 0.13, 2 D 12.44, d.f. D 3,
p D 0.006, n D 6 individuals; agriculture lands less used
than open areas: p D 0.047; the other habitat types were
interchangeable: p-range D 0.0654–0.3715. Radiolocations vs. home range: D 0.90, 2 D 0.61, d.f. D 3,
p D 0.893). To avoid potential biases associated with the
number of radiolocations and be conWdent with our estimations of habitat selection, we plotted the percentage
of increase in home range area as a result of increasing
the number of locations for each individual to repeat
analyses with those home ranges that showed a stabilized area. Although we substantially reduced our sample size to 7 individuals during the breeding season
(Table 1), results remained unchanged (Home range vs.
study area: D 0.08, 2 D 18.02, d.f. D 3, p < 0.001, n D 7
individuals; agriculture lands signiWcantly less used than
any other habitat: p-range D 0.022–0.034; the other habitat types were interchangeable: p-range D 0.833–0.431;
Radiolocations vs. home range: D 0.61, 2 D 3.43,
d.f. D 3, p D 0.33).
The above results, however, did not take into account
the potential constraint that distance from the colony to
diVerent habitat patches could impose on foraging vultures. Accordingly, a distance-based GLMM showed
that the best regression model to predict habitat use only
included the dehesas through its interaction with distance (Table 2). This result was consistent among individuals (Wtted as random term, p D 0.389) independently
of their sex (p D 0.839) and of the season (p D 0.354). The
positive sign of this interaction pointed out that dehesas
were positively selected by birds in spite of being far
away from the colony. In this sense, and considering the
dominant habitat at each radiolocation (coverage
750%), the distance at which cinereous vulture used
dehesas (median D 31.68 km) was signiWcantly higher
than the observed for the other habitat types
M. Carrete, J.A. Donázar / Biological Conservation 126 (2005) 582–590
Table 2
Generalized Linear Mixed Model obtained to predict the foraging
habitat use of cinereous vultures (Aegypius monachus) in south-western Spain (1998–2000) in relation to distance to the colony
Parameter
Estimate
SE
F-test
P
Dehesas
Dist
¡0.88
¡8 £ 10¡5
0.67
5.12 £ 10¡6
1.76
254.28
0.1853
<0.001
6.35
0.0118
Dehesas £ dist
3.8 £ 10¡5
1.5 £ 10¡5
The eVects individual (Wtted as random factor), season and sex (Wtted
as Wxed eVects) did not reach signiWcance into the model (p
range D 0.354–0.839). dehesas: coverage of dehesas in a radius of 2 km,
dist: linear distance to the breeding colony. Deviance explained by the
model: 27.62%.
Degrees of freedom: 1415.
(median D 23.44 km;
p < 0.0001).
Mann–Whitney
U-test D 24,872,
5. Discussion
Cinereous vultures included within their home ranges
similar proportions of dehesas, open areas and exotic
forest, avoiding the use of agricultural lands. However,
choosing the proportion of habitat types within a home
range as a null model of availability involves the implicit
assumption that no factors other than habitat type aVect
its use, which could not be always reasonable (Otis, 1997,
1998; Johst et al., 2001; Peach et al., 2004). The use of a
habitat patch by individuals exhibiting central-place
behaviour as the cinereous vulture may be due to both
the habitat quality and the proximity to the central place
(Franco and Sutherland, 2004). In this sense, when a distance-based model was performed, we Wnd that dehesas
were actively selected compared with the other land uses
in spite of being farther away from the colony. Thus, the
similar preference for exotic forest, open areas and dehesas within the home ranges obtained with the compositional analysis may be a consequence of birds eventually
prospecting these habitats while travelling from their
nests to the dehesas. This is reinforced by our lack of
observations of vultures feeding in exotic forests
(author’s unpublished data).
Foraging habitat selection in most animal species is
commonly assumed to be inXuenced by the availability
and/or accessibility of their main prey species (e.g.,
Newton, 1994; Widen, 1994; Tella et al., 1998; Palomares et al., 2001; Franco and Sutherland, 2004).
Although data to accurately estimate food availability
in our study area is not available, we can infer it
through cattle statistics (cows, sheep, goats, and pigs;
Spanish Institute of Statistics, 1999) and oYcial hunting reports of rabbits (I. Fajardo, unpublished data),
which constitute the main food items of this species
(Hiraldo, 1976). Assuming a positive relationship
between these values and food availability for vultures
587
(i.e., more cattle and more hunted rabbits should imply
more carcases and rabbit corpses in the Weld), the above
mentioned data suggest that dehesas could be an
important foraging habitat for cinereous vulture
because it maintains high relative abundances of rabbits at the same time that they are commonly used for
livestock grazing. Contrarily to what happens in other
regions, however, agricultural lands in the Andalusian
study area are mainly free of grazing animals because
they do not remain uncultivated through long periods
of time (see e.g., Tella et al., 1998). Moreover, although
they hold the highest rabbit abundances (I. Fajardo,
unpublished), the presence of people working in the
Weld as well as car traYc can discourage their use by
cinereous vultures (Donázar et al., 2002; Bautista et al.,
2004).
There were also some evidences for seasonal changes
in home range. Contrary to what happens in other raptor species which are tied to a nesting place during the
breeding season but then (i.e., during the non-breeding
season) move through larger areas (MarzluV et al., 1996;
Burton and Olsen, 2000; Dykstra et al., 2001; Sunde
et al., 2001), home range of cinereous vultures were bigger during the breeding period. This could be because
daylight time is shorter in winter, thus decreasing the
number of hours available for Xight and, consequently,
the surface prospected by cinereous vultures (Hiraldo
and Donázar, 1990). Moreover, the higher food requirements associated with reproduction can force vultures to
prospect across larger surfaces, looking for the unpredictable location of carrions to satisfy food provisioning
for oVspring and themselves. Here, it should be noted
that although the straight-line travel foraging distances
previously estimated for this vulture through the eventual observations of Xying birds (around 30 km, Mundy
et al., 1992; Donázar, 1993) were markedly smaller than
those obtained in this study by tracking birds, since more
than 40% of our data correspond to larger distances
(reaching up to 86 km). This increase, likely resulting
from biases in evaluating movements without radiotracking methods (since the probability of visually
detecting birds decays at higher distances to the nest due
to the area increase), might reinforce the selection of
dehesas as foraging habitat, which in the study area are
at a median distance of 50 km (range D 15–85 km).
Moreover, as central-place foragers are expected to
depress resources unevenly across their home range (Orians and Pearson, 1979), mainly in the case of colonial
species (Fernández et al., 1998; Lewis et al., 2001; Forero
et al., 2002) such as this vulture, foraging distances could
increase in the future if conservation measures to maintain the traditional exploitation of dehesas as well as to
restore the degraded areas are not taken into account.
As was observed in other colonial species, increments in
food-searching distances can have Wtness consequences
in terms or reducing oVspring quantity and/or quality
588
M. Carrete, J.A. Donázar / Biological Conservation 126 (2005) 582–590
(Tella et al., 1998, 2001; Forero et al., 2002), even aVecting large-scale population trends (e.g., Tella et al., 1998).
5.1. Management implications
QuantiWcation of wildlife resource selection is critically
important for impact assessment and management planning. The conservation of cinereous vulture, contrarily to
many other species, has been primary focused on breeding
cores (Donázar et al., 2002; Poirazidis et al., 2004) taking
less attention to foraging habitat requirements, perhaps
because nesting failures are obvious when they are related
with direct disturbances but less apparent when they are
linked to prey depression through habitat degradation or
management away from nesting sites (Tella et al., 1998;
Rodríguez, 2004). In this sense, our results point out that
protecting “breeding islands” within severely transformed
landscapes, as it is the case of our studied colony, is not
useful enough for a large vertebrate such as the cinereous
vulture that needs to prospected large surfaces for obtaining food resources. Breeding cinereous vultures require,
apart from mature trees for nesting, the existence of adequate foraging habitat such as the dehesas in the neighbourhood which could not be easily replaced by the
creation of supplementary food points (commonly called
“vulture restaurants”) supplied with just carcasses of large
livestock. These feeding stations could have been beneWcial
for the species in some regions (Vlachos et al., 1999), but in
Spain they are scarcely used by cinereous vultures probably because they are overexploited by larger numbers of
the commonest GriVon vulture Gyps fulvus (Authors,
unpublished data). Although the large home range of cinereous vultures allow nesting and foraging habitats to be
not so close, birds would beneWt from the maintenance
and, if it is necessary as in the study area, restoration of
these habitat types close around the colony because they
would reduce the costs associated with long travel distances as those detected in our study (see above).
Changes in dehesas since the 1950s were strong and
have included their conversion to exotic forests of eucalyptus and pines, as happened in the study area and in
many other parts of the Iberian Peninsula (e.g., Algarve,
in Portugal, or Monfragüe, in Spain, holding other of the
larger cinereous vulture colony), local increases in livestock density, abandonment of tree management, tree
regeneration failures, and conversion to irrigated land.
Currently, lack of natural regeneration due to overgrazing by livestock or big game in some places, and abandonment in others, is the main conservation problem for
the dehesas system (Pulido et al., 2001). These changes
may have been detrimental for many other species
besides of the cinereous vulture. A further conservation
problem associated with changes in dehesas is their
inclusion into intensive hunting areas where the illegal
use of poison for predator control is usual. Rabbit diseases have lead to an increase in the number of poison-
ing events in Spain (Villafuerte et al., 1998), resulting in a
high raptor mortality (Cano, unpublished). In fact, for
the cinereous vulture, adult mortality reaches 20% in the
studied colony mainly due to poisoning of birds during
foraging activities (Donázar et al., 2002).
Dehesas are included in the Annex. 1 of the EU Habitat Directive to be considered during the designation of
Special Areas of Conservation within the Natura 2000
network. However, Natura 2000 is not intended to
include all areas where a habitat type is present, but
rather a selection of the most representative and bestconserved areas. Besides, dehesas are a biotope which
has been created and need to be maintained by people,
but it is needed to ensure that the intensity of management and exploitation is appropriated (Bignal and
McCracken, 1996; Beaufoy, 1998; Plieninger and Wilbrand, 2001; Díaz et al., 2003). As management decisions
on these lands are in private hands and determined primarily by the European Common Agricultural Policy,
agri-environment payments for the traditional lowintensity exploitation of dehesas, taking into account
nature conservation, could play a mayor role in their
long-term permanence as well as in the conservation of
the species that depend on them (Díaz et al., 1997). This
payment to compensate commercial losses may encourage the maintenance of this traditional low intensity
land use in large areas of Spain and Portugal.
Finally, we want to remark that, although the idea of
carrying out conservation actions at large scales has long
been recognized, the focus had tended to be on individual reserve size, connection between reserves and buVering of anthropogenic impacts on core conservation areas
(e.g., Diamond, 1975; SimberloV, 1986; Hobbs, 1992;
Groom et al., 1999). Cinereous vultures, as many other
large vertebrates, require large home ranges for foraging
activities, reXecting its potential “umbrella species” role
for the conservation of dehesas. However, beyond the
Wnding that this species requires large habitat extensions
for persistence (the total colony home range is at least
592,000 ha) we did not test if this is an eVective umbrella
species for Wne-scale management of dehesas (Roberge
and Anglestam, 2004). Thus, we propose the use of this
charismatic bird as a “Xagship” species for the largescale maintenance of dehesas while more Wne local management guidelines are performed on the basis of studies
on smaller, maybe more sensitive species such as small
mammals or birds, lizards and invertebrates (Pulido and
Díaz, 1998; RubinoV, 2001; Martín and López, 2002;
Roberge and Anglestam, 2004).
Acknowledgements
We thank M. de la Riva very much for his decisive
and careful work at all stages of the research. J. Blas, J.
Bustamante, M. Cabaco, J. Caballero, S. Cabezas, A.
M. Carrete, J.A. Donázar / Biological Conservation 126 (2005) 582–590
Fernández, V. Fiscal, M.G. Forero, L. Gangoso, G. García, H. Garrido, M. Gómez, J. M. Hornero, F. Ibáñez, L.
Infante, E. Luque, I. Luque, J. Martín, F. Martínez, F.
Molino, J.J, Negro, M. Pérez, M.A. Pineda, J. Rengel, M.
Rico, G. de la Riva, R. Rodríguez, M. Ruiz, C. San Segundo, J.M. Sayago, A. Sierra, J.R. Súnico, and J.L. Tella
helped with the Weld tasks. I. Fajardo provided data on
rabbit abundance. J.F. Calvo and J.D. Anadón helped
with the compositional analysis. J.L. Tella, J.A. SánchezZapata, F. Hiraldo, J.M. Grande, M. Díaz, and two
anonymous referees made many constructive comments
on the earlier versions of the manuscript. The study was
Wnanced by the Consejería de Medio Ambiente, Junta de
Andalucía. When writing up the paper, M.C. was supported by a postdoctoral grant from Fundación Séneca
(Murcia, Spain).
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