Application of a predictive model to detect long-term
changes in nest-site selection in the Bearded Vulture
Gypaetus barbatus: conservation in relation to
territory shrinkage
ANTONI MARGALIDA, 1* JOSÉ ANTONIO DONÁZAR, 2 JAVIER B US TAMANTE, 2
FRANCISCO JOSÉ HERNÁNDEZ 3 & MARILÓ ROMERO-PUJANTE 4
1
Bearded Vulture Study and Protection Group, Apdo. 43, El Pont de Suert, E-25520 Lleida, Spain
2
Department of Applied Biology, Estación Biológica de Doñana, C.S.I.C., Avda Ma Luisa s/n, E-41013 Sevilla, Spain
3
C/La Vega, 24. Salteras. E-41909, Sevilla, Spain
4
Egmasa, Johan Gutenberg, s/n, Isla de la Cartuja. E-41092, Sevilla, Spain
In this study we examined long-term variation in the selection of nesting cliffs for the recovering
population of the Bearded Vulture Gypaetus barbatus inhabiting the Spanish Pyrenees. We
focussed on variables indicating a high probability of cliff occupancy as determined by a
previously published model. Although the breeding population increased from 53 to 93
territories between 1991 and 2002, the breeding range expanded only slightly. New and old
nesting cliffs had similar habitat features in relation to topography, altitude and degree of
human influence, but the distance between occupied cliffs was reduced (from 11.1 to
8.9 km). Thus the probabilities of occupation predicted by the model were lower for newly
colonized locales. Our study shows that territory compression may occur without serious
modification of nesting habitat quality. These results may arise from the lack of strong
territorial behaviour by Bearded Vultures and the availability of high-quality cliffs. The
relatively low quality of sites in adjacent mountains may prevent the expansion of the breeding
range, but conspecific attraction may also play a role. Our study confirms that monitoring
changes in key variables important to habitat selection is useful in determining long-term
trends in settlement patterns in heterogeneous environments. The results also suggest that
the available nest-site selection model may accurately predict cliff occupancy by Bearded
Vultures in those areas where the distance to the nearest neighbour is not a limiting factor.
In particular, the model may be useful in establishing priority areas for reintroduction.
Keywords: cliffs, conspecific attraction, despotic competition, habitat quality, Pyrenees.
Explanatory and predictive models are powerful tools
in the study of spatial distributions of populations
and their use is growing exponentially in animal
ecology (Guisan & Zimmermann 2000, Guisan et al.
2002, Rushton et al. 2004). Models establish statistical
relationships between a response and explanatory
variables that usually quantify environmental characteristics such as climate, landscape features, and degree
of human influence (e.g. Bustamante & Seoane 2004,
Guisan & Thuiller 2005, Gavashelishvili & McGrady
2006). This procedure is increasingly employed in
*Corresponding author.
Email: margalida@inf.entorno.es
wildlife conservation, mainly to determine the
probability of future site occupation for expanding
populations (Mladenoff et al. 1995, Buckland et al.
1996, Jerina et al. 2003, Hirzel et al. 2004) and to
examine habitat suitability for released populations
within reintroduction programs (Bustamante 1998).
The accuracy of predictive models is strongly
dependent on population equilibrium, biotic interactions and stochastic local events. Although such
complexity frequently limits the generality of the
results (Guisan & Zimmermann 2000, Guisan et al.
2002), an increasing number of studies take this into
account (e.g. Fielding & Haworth 1995, Lindenmayer
et al. 1995, Rodriguez & Andrén 1999). Predictive
models are now a potentially valuable tool to detect
long-term trends in those key variables capable of
explaining the distribution of organisms.
Here we use a previously published predictive
model to determine long-term changes in nest-site
selection in an endangered population of the Bearded
Vulture, Gypaetus barbatus. This species is a large
scavenger living in rugged areas where it feeds
mainly on bone remains from wild and domestic
ungulates (Margalida et al. 2007a). It builds large
nests in sheltered caves and ledges of cliffs (see
Hiraldo et al. 1979 for review of general biology).
The Bearded Vulture lived formerly in all the mountain
regions of the Old World from southern Europe to
the Middle East and central Asia, but at present its
distribution has been much reduced, mainly due to
human persecution (Margalida et al. 2008). In
Europe, by far the largest population occupies the
Pyrenean range between France and Spain (Heredia
2005). Because the Bearded Vulture is considered
endangered in Europe (Annex I, EU Wild Birds
Directive 79/409/EEC, Appendix II of the Bern
Convention, Bonn Convention and CITES) with
fewer than 130 breeding territories in the European
Union in 2005, reintroduction projects have been
carried out, for example in Andalucía (Simón et al.
2005) and the Alps (Terrasse 2004), or are in
preparation (e.g. Sardinia, the Balkans).
Nesting habitat selection by Bearded Vultures was
studied in 1991 in the Spanish Pyrenees by assessing
physiography, land use, climate, human disturbance
and intraspecific density (Donázar et al. 1993).
Cliffs having a high probability of occupancy were
those situated in rugged areas (i.e. a high degree of
topographic irregularity), at an average altitude, far
from villages and far from the nearest conspecific
territory (see below for details). Between 1990 and
2000 the Bearded Vulture population of the Spanish
Pyrenees grew annually at a rate of 5% (Heredia &
Margalida 2002). This increasing trend is unusual as
populations of this species are decreasing over most
of their distribution (Del Hoyo et al. 1994). However, the area in which the Pyrenean birds are found
has not increased at the same rate: less than 10% of
their former breeding range has expanded during the
last two decades (Heredia 2005).
In this paper, we have the advantage of the above
mentioned 1991 predictive model to assess whether
nest-site selection patterns of the Bearded Vulture
have changed in parallel with population growth. The
results may contribute to the long-term management
of the most important European population of this
endangered species and, moreover, may help to
determine the validity of nest-site selection models
as a tool for future conservation actions, especially
those involving reintroduction programs.
M E T HO D S
Population trends and cliff
characterization
The basic information on the distribution of territories
and nests of Bearded Vultures in the Pyrenees has
been obtained from two sources: unpublished
databases compiled by R. Heredia from 1977 to
1991 (see Donázar et al. 1993) and monitoring programs established by regional governments (Navarra,
Aragón and Catalunya) from 1991 to the present.
In all the regions, the monitoring has been able to
detect the occupation of new territories thanks to
repeated visits to locations with at least minimum
requirements for the establishment of new pairs
(Margalida et al. 2003c). Each year, breeding sites
known from previous studies, named old cliffs, and
new sites located after 1991, named new cliffs, were
visited at least once a week between the months of
November and August. To locate the nests, observations began in September coinciding with the start of
nest building (Margalida & Bertran 2000) and ended
during fledging (June–August). During each visit, a
pair’s breeding behaviour and whether the birds
were building nests, incubating, or rearing a chick
was recorded. The sampling effort for the two periods
(i.e. 1977 – 91 and 1991– 2002) was similar.
Statistical procedures
Comparisons were done on the basis of four groups
of sampling locations (b and c correspond to those
used by Donázar et al. 1993, see Table 1):
(a) New (n = 36): cliffs with nests occupied between
1991 and 2002. If a territory had more than one nest,
we only considered the one used the first time.
(b) Old (n = 111): all cliffs with nests occupied at
least once between 1977 and 1991.
(c) Random (n = 111): unoccupied cliffs from the
existing range, selected by pseudo-random generation
of co-ordinates and choosing the nearest point on a
cliff without a nest.
(d) Peripheral (n = 40): cliffs without Bearded Vulture
nests selected at random in the former range of the species
and located in zones more than 20 km from the nearest
pair. These cliffs were in the Eastern Pyrenees and the
Table 1. Variables used to characterize Bearded Vulture nesting cliffs and random cliffs. In random cliffs, distances were measured from
a point in the centre of the cliff (modified from Donázar et al. 1993).
Topography
RELIEF: Topographic irregularity index. Total number of 20-m contour lines, cut by four 1-km lines starting from the nest in directions
N, S, E and W.
Cliff local characteristics
ALTITUDE: Altitude of the nest above the sea level (m).
CLIFF: Cliff height, measured as the number of 20-m contour cut by a 50-m line perpendicular to the cliff face at nest level.
ORIENTATION: Orientation of the cliff face at the level of the nest. Orientations were scored in increasing shelter from cold humid winds
from the NW, which are dominant in the area: 1 = NW, 2 = N or W, 3 = NE or SW, 4 = E or S, 5 = SE.
Environmental characteristics of the surrounding area
FOREST: Extent (%) of forested areas in a 1-km radius around the nest.
DISTANCE VILLAGE: Distance to the nearest inhabited village (km).
INHABITANTS: Number of inhabitants in the nearest village.
Human disturbance
KILOMETRES ROADS: Kilometres of paved and unpaved roads in a 1-km radius of the nest. DISTANCE
PAVED ROAD: Shortest linear distance between the nest and the closest paved road (km). DISTANCE
ROAD: Shortest linear distance between the nest and the closest road, paved or unpaved (km).
HEIGHT PAVED ROAD: Altitudinal difference between the nest and the closest paved road, measured at the point the road is closer to
the nest (m). If the nest is lower than the road, a negative value is obtained.
HEIGHT ROAD: Altitudinal difference (m) between the nest and the closest road (paved or unpaved). If the nest is lower than the road,
a negative value was obtained.
Intraspecific relationships
NEAREST NEIGHBOUR: Linear distance between the nest and the closest nest of the nearest neighbour (km).
Table 2. Descriptive statistics (mean ± sd) and significance of the differences in mean values between some groups obtained with the
Mann–Whitney test of the variables characterizing the new breeding cliffs (n = 36) occupied by the Bearded Vulture in the Spanish
Pyrenees between 1991 and 2002, old cliffs occupied before 1991 (n = 111), randomly selected cliffs (n = 111) and cliffs in peripheral
mountains (n = 40).
Cliffs
Variable
RELIEF
ALTITUDE
CLIFF
ORIENTATION
FOREST
DISTANCE VILLAGE
INHABITANTS
KILOMETRES ROADS
DISTANCE PAVED ROAD
DISTANCE ROAD
HEIGHT PAVED ROAD
HEIGHT ROAD
NEAREST NEIGHBOUR
P (Mann–Whitney U-test)
New
(n = 36)
Old
(n = 111)
Random
(n = 111)
Peripheral
(n = 40)
New–
Old
New–
Random
Peripheral–
Random
77.0 (19.9)
1424.2 (358.9)
321.7 (124.5)
3.3 (1.0)
167.0 (97.0)
2.60 (1.4)
88 (139)
1.5 (1.6)
2.3 (1.7)
1.0 (0.9)
431.4 (267.6)
325.0 (257.8)
8.9 (8.4)
83 (18.0)
1333 (361.2)
367.2 (116.7)
3.1 (1.3)
167.9 (111.5)
3.1 (2.4)
175 (259)
1.5 (2.2)
2.1 (1.6)
1.0 (0.9)
404.7 (252.3)
250.8 (291.0)
11.1 (5.4)
67.8 (15.4)
1316.56 (516.0)
268.8 (94.1)
3.0 (1.2)
155.4 (102.7)
2.8 (2.0)
116 (205)
2.4 (2.9)
2.3 (1.7)
1.0 (1.0)
390.6 (330.3)
254.0 (310.7)
8.1 (6.0)
58.8 (13.0)
1078.7 (955.3)
13.5 (4.7)
3.3 (1.2)
49.5 (32.7)*
2.2 (1.3)
156 (186)
4.6 (3.6)
1.6 (1.2)
0.3 (0.2)
239.2 (247.2)
83.0 (147.6)
53.3 (21.5)
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
0.001
0.003
ns
0.01
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
0.010
< 0.0001
< 0.0001
ns
ns
ns
0.002
< 0.0001
ns
< 0.0001
0.013
0.001
*Calculated on a sample size n = 19 as consequence of limited data available.
Basque Mountains. They are habitually visited by
immature and adult birds during their dispersal stage
(R. Heredia, D. Campión, A. Margalida, unpubl. data).
We first used Wilcoxon Mann–Whitney tests to
check if there were statistical differences in environ-
mental variables comparing peripheral to random
cliffs. Next, we compared the differences in environmental variables between new and old nesting cliffs,
and between new and random cliffs (Table 2).
Finally, we compared average probability of cliff
occupancy predicted by the model between old,
new and random cliffs. We used generalized linear
models (GLMs) to analyze the binary response
variables ‘cliff occupation’, assuming a binomial
distribution of errors and using a logit link function
(see Donázar et al. 1993). The final model included
four variables: relief, distance to the nearest occupied
nest (log-transformed), altitude and distance to the
nearest village (log-transformed): linear predictor =
–33.9 + (0.091*relief ) + (1.644*log distance to the
neighbour territory) + (0.099*altitude) – (4.024*10–6
*altitude 2 ) + (0.945*log distance to the nearest
village). The result was that in 1991 the Bearded
Vulture selected those areas with the most irregular
topography as nesting cliffs, far from other breeding
pairs, at an average altitude, and away from human
habitation.
The predictive ability of a model tends to be
optimistically biased when evaluated with the same
data used to build it. Because of that, and because of
the fact that old nesting cliffs and random cliffs, rather
than new nesting cliffs, have been used to build the
model, the probability of occupancy predicted by
our model on new cliffs cannot be compared with
other cliffs. To avoid the bias, we estimated the
probability of a cliff being occupied by Bearded
Vultures by cross-validation. We divided each sample
(old, new and random cliffs) into five groups with
20% of the observations in each. The first group of
observations in each sample was used as a test and
the remaining four groups of old cliffs and random
cliffs (80% of original model data) were used to fit
new model parameters. This model was used to
predict the probability of occupation in the test
group of observations (20% of data). Each of the
groups of observations was dropped in turn from
model construction and used as test data. The dataset
was reordered 20 times and the whole procedure
repeated, so the probability of cliff occupancy was
estimated 20 times by 20 different predictive models
based on observations before 1991 that did not
contain that particular observation. We estimated
the mean predicted probability for each cliff and
compared samples (old, new and random) with
the Wilcoxon Mann–Whitney test. The predictors
included in all models were the same used in
the model of Donázar et al. (1993); we only estimated new parameters in each case. The whole
procedure was repeated, fitting a model without
distance to the nearest neighbour to estimate the
effect of this variable on the probability of cliff
occupancy.
R E S U LT S
The Bearded Vulture population of the Spanish
Pyrenees grew from 53 territories occupied in 1991
to 93 in 2002. Despite this increase, the distribution
area changed only slightly during this period: two
new territories were located up to 40 km westwards.
The rest of the new territories were found within
the former breeding area, mostly within the central
nucleus of the mountain range. The cliffs located in
peripheral zones, without Bearded Vulture territories,
showed several significant differences from those
existing in occupied breeding areas (Table 2). They
tended to be smaller (mean height) and were usually
located in less steep and lower altitude zones. In
addition, they were nearer, in distance and altitude,
to roads and they had a greater neighbouring human
population.
The new territories occupied from 1991 to 2002
showed similar habitat characteristics to those
occupied before 1991 (Table 2). The only exception
was the variable ‘nearest neighbour’. New territories
were situated at a significantly shorter distance to
other occupied territories than they were before
(mean: 8.9 km vs 11.1 km). In relation to randomly
selected cliffs, new nest sites were in areas that were
more rugged, and in cliffs that were higher than
average. In addition, new nesting cliffs were not
significantly further from the nearest occupied nest
(mean: 8.9 km) than were random cliffs (mean:
8.1 km; Table 2). These results are similar when
comparing old nests with random cliffs (Table 2).
The application of models including the variable
‘nearest neighbour’ determined that newly occupied
cliffs had intermediate probability values between
old nesting cliffs and random cliffs (Fig. 1); the two
comparisons gave significant differences (new vs old
Z = 2.89, P = 0.0038; new vs random Z = −3.16,
P = 0.0016). Previously occupied cliffs had, as
expected, a higher probability of occupancy than
random cliffs (Z = 8.537, P < 0.0001). When probabilities were calculated on the basis of the model
without ‘nearest neighbour’ (Fig. 1), new cliffs did
not differ significantly from old cliffs (Z = 1.11,
P = 0.267), but both old cliffs and new cliffs had
significantly higher occupancy probabilities than
random cliffs (respectively, Z = −3.592, P = 0.0003,
Z = 6.949, P < 0.0001). Therefore, during the last
decade Bearded Vultures have been selecting a
similar kind of cliff as previously chosen in relation
to topography and distance from human habitation,
the main factors affecting cliff selection. The distance
Figure 1. Mean probability (± 95% confidence intervals for the
mean) of a cliff being used by Bearded Vultures for nesting in the
Spanish Pyrenees estimated, with modifications, on the basis of
the GLM model fitted by Donázar et al. (1993). Probabilities are
shown for new cliffs (triangle) occupied after 1991 (n = 36), old
cliffs (square) occupied before 1991 (n = 111) and randomly
selected cliffs (circle) (n = 111). (A) Original model, (B) without
the variable ‘nearest neighbour’.
between neighbouring territories decreased in
parallel with the increase in population density (from
4.4 to 2.5 territories/1000 km2 between 1991 and
2002).
DISCUSSION
Our results show that the selection of nest sites has
not changed with the population increase of the
Pyrenean Bearded Vulture. For those variables
determining the probability of cliff occupancy
(ruggedness, altitude and distance to nearest human
habitation), newly established territories between
1991 and 2002 had similar values to those of traditional
territories occupied previously. These new pairs,
however, occupied cliffs among the existing old
territories so that the distance between neighbours
has reduced by around 20%, which proves territory
shrinkage (Both & Visser 2000, Ridley et al. 2004).
In addition, cliffs remaining unoccupied by Bearded
Vultures after 1991 in the periphery of the Pyrenees
had both lower values in key variables (e.g. relief,
altitude, distance to village) and lower probability of
occupancy than those occupied in the Pyrenean
range during the same period.
These findings seem to contradict what would be
expected from a distribution by despotic competition,
classically described for birds of prey and other
territorial birds (e.g. Ferrer & Donázar 1996, Newton
1998). It could be argued that there is still availability
of good-quality breeding sites in the Pyrenees and
that, consequently, the population has not reached
the saturation threshold necessary to observe the
occupation of marginal territories by newly established
birds. This holds true if the comparison is limited to
the examination of the quality of nesting cliffs where
no long-term changes were evident. A different
picture, however, arises when distance between
neighbouring territories is considered. As this variable
was significant in the model fitted in 1991, we can
deduce that saturation is taking place and that there
is a decrease in territorial quality via reduction in the
distance between breeding pairs. In parallel, it has
been demonstrated that the productivity of the
Pyrenean population has sharply declined during the
last decade as a consequence of the increasing breeding
density (Carrete et al. 2006a), a clear symptom of
population crowding, as is the appearance of unusual
mating systems (Carrete et al. 2006b). Today, the
density attained by Bearded Vultures in the Spanish
Pyrenees (226 km2/one territory) is the highest
recorded for the species in its European breeding
range. Equivalent figures are 333 km2/territory for
the French Pyrenees, 240 km2/territory for Corsica
and 2065 km2/territory for Crete (Xirouchakis &
Nikolakakis 2002, Terrasse 2004). To these numbers
(93 pairs in 2002), a non-breeding population of
around 200 individuals should be added to the
Spanish Pyrenean population (Heredia 2005).
Why do Bearded Vultures tolerate shrinkage of
territories? In territorial birds of prey, an increase in
the density of breeders usually results in a higher
level of agonistic encounters; large territories are
vigorously defended against conspecifics (Newton
1979, 1998, Ridley et al. 2004). Territorial defence
in the Bearded Vulture appears, however, to be
restricted to the areas surrounding the nest (less than
500 m radius according to the majority of authors;
Hiraldo et al. 1979, Brown 1988, Bertran & Margalida
2002, Margalida & Bertran 2005). Outside these limits,
there is habitual tolerance between neighbouring
pairs. Tolerance towards conspecifics may be evolutionarily favoured as a consequence of the large
distances between territories, which would not favour
selection for aggressiveness against intruders (see
also Margalida et al. 2003b). In fact, the strategy for
finding unpredictable food makes it necessary to
forage over extensive areas that overlap neighbouring
pairs (Brown 1988). Human manipulation of the
availability of resources (e.g. feeding stations) may
also be a determining factor explaining this ‘packing’
of the population. During the 1990s, nearly 30 feeding
stations were established in the Spanish Pyrenees.
There, more than 50 000 kg of bones per year are
left for the Vultures (Regional Governments,
unpubl. data). Consequently, it could be that this
increase in the availability of resources has resulted
in the reduction of territorial behaviour and facilitated
the compression of territories. Monitoring of feeding
stations reveals a predominant use by immature
birds (70%; Heredia 1991), but it is not possible to
disregard the fact that these feeding stations are
important factors for adult birds at specific times of
the breeding cycle. Feeding stations can strengthen
conspecific attraction, reducing the probability that
new breeding birds will occupy territories in areas
distant to the central zone of the mountain range
(Serrano & Tella 2003).
Finally, the packing process could be also motivated
by the scarcity of suitable breeding sites in mountain
areas surrounding the Pyrenees. As our analyses
demonstrate, potential nesting cliffs in those regions
are of lower quality (in terms of altitude, topography
and human influence) than those existing within the
main mountain range. Human presence is known to
affect strongly the distribution patterns of Bearded
Vultures and other large raptors, not only in relation
to the safety of breeding nest sites (Donázar et al.
2002, Margalida et al. 2007b), but also in relation to
foraging grounds (Bautista et al. 2004, Gavashelishvili
& McGrady 2006). Previous analyses have shown
that the breeding success of Pyrenean Bearded
Vultures is affected by human activities and infrastructures (Donázar et al. 1993, Arroyo & Razin
2006). Therefore, it is reasonable to think that the
low probability of cliff occupancy outside the Pyrenees
is determined, at least partially, by the intense
human influence on these peripheral mountain
regions. In this sense, the Pyrenees could progressively
become more of an ecological island for the Bearded
Vulture surrounded by areas that are inadequate due
to the increasingly intense human influence on the
environment. Consequently, the risk of extinction in
this population will remain high as a consequence of
stochastic demographic and environmental phenomena
and of the scarce genetic variability (Godoy et al. 2004).
The conservation efforts for the population of
Pyrenean Bearded Vultures should facilitate the
geographic expansion of the species towards other
mountainous zones of the Iberian Peninsula. Two
complementary actions, the creation of new populations
through reintroduction plans, and the promotion of
the dispersion of non-breeding individuals using
changes in the availability of food, could favour the
maintenance of a metapopulation structure permitting
genetic exchange and, fundamentally, determining
unequal probability of extinction for different
sub-populations. To determine the suitability of the
areas of reintroduction, where constraints linked to
territoriality do not exist, a model such as that
determined in 1991, without the distance to nearest
neighbour variable, seems particularly relevant. In
fact, the aforementioned model has been used to
predict nesting probability in areas where the
Bearded Vulture is being reintroduced, such as the
Alps and Andalucía (e.g. Bustamante 1996). In a
broader sense, our study shows that the probability
of presence determined by predictive models may be
sensitive to social behaviour, in this case flexibility in
territoriality. This shows the necessity for modelling
procedures to take into account variables quantifying intraspecific relationships between individuals
(Alexander et al. 2006).
The basic information about the recent distribution
(1991– 2002) of the Bearded Vulture comes from databases
generated by the Ministry of Environment, Organization of
Land and Housing of the Autonomous Region of Navarra,
the Department of Environment of the General Council of
Aragon and the Department of Environment and Habitat
of the Autonomous Government of Catalonia. Our
thanks to all the people who have directly or indirectly
participated in different phases of this work: I. Afonso,
I. Anton, R. Antor, M. Arilla, J. Bertran, J. Bolado, A. Bonada,
D. Campión, J. Canut, D. García, D. Gómez, R. Heredia,
J. Jové, J. Martín, J.M. Miranda and A. Senosiain. B.E. Arroyo,
G.R. Bortolotti, M. Carrete, F. Hiraldo, A. López-Sepulcre
and two anonymous reviewers contributed suggestions
which improved the manuscript. This work was financed
by the Ministry of Environment of the Autonomous
Government of Andalusía, within the Project ‘Studies of
viability for the reintroduction of the Bearded Vulture in
Andalusía’. Support was also obtained from the BBVA
Foundation through its award for scientific research in
Conservation Biology (2004).
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Received 23 January 2007; revision accepted 6 September 2007.