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Territorial defence behaviour of Bearded Vulture Gypaetus barbatus against

conspecifics and heterospecifics

Article in Ethology Ecology and Evolution · March 2005

DOI: 10.1080/08927014.2005.9522615

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 Ethology Ecology & Evolution 17: 51-63, 2005

Territorial defence and agonistic behaviour

of breeding bearded vultures Gypaetus barbatus
toward conspecifics and heterospecifics

A. MARGALIDA 1 and J. BERTRAN

Grupo de Estudio y Protección del Quebrantahuesos, Apdo 43, E-25520 El Pont de
Suert, Lleida, Spain

Received 26 August 2004, accepted 12 January 2005

Territoriality and agonistic behaviour against conspecifics and heterospe-

cifics was recorded for nine breeding pairs of bearded vulture Gypaetus barbatus
between 1992 and 1996 in the Pyrenees (NE Spain). For both sexes, the defence
intensity increased from the pre-laying to the chick-rearing period. The intensity
of nest defence was significantly higher in males during the pre-laying period but
no sex differences were found during the incubation and chick-rearing periods.
Competition for nest sites, food and the potential risk of predation may affect
the bearded vulture’s nest defence behaviour towards other species. Most agonis-
tic interactions took place against Eurasian griffon vultures (the most abundant
species and the most important competing for nest sites) and common ravens
(the most likely potential predator and a kleptoparasitic species). Nest defence
against conspecifics mainly took place during the pre-laying period and may be
linked to sperm competition and food resource competition.

KEY WORDS: agonistic behaviour, bearded vulture, Gypaetus barbatus, interspe-

cific interactions, intraspecific interactions, parental investment, Pyr-
enees, territorial defence.

Introduction . . . . . . . . . . . . . . . . . 52
Methods . . . . . . . . . . . . . . . . . . 53
Results . . . . . . . . . . . . . . . . . . 54
Discussion . . . . . . . . . . . . . . . . . 57
Interspecific interactions . . . . . . . . . . . . . 57
Intraspecific interactions . . . . . . . . . . . . . 58
Sexual differences in the intensity of nest defence . . . . . . 59
Intensity of defence in relation to the breeding stage . . . . . 59
Acknowledgements . . . . . . . . . . . . . . . 60
References . . . . . . . . . . . . . . . . . 60

1 Corresponding author: Antoni Margalida (E-mail: margalid@gauss.entorno.es).

52 A. Margalida and J. Bertran

INTRODUCTION

Generally, territoriality is associated with the defence of resources necessary

for breeding and survival (KREBS 1971, DAVIES 1980). Nest defence may be consid-
ered a form of parental investment because it probably serves to enhance offspring
survival, and involves costs to the parents in terms of future breeding success (TRIV-
ERS 1972, BIERMANN & ROBERTSON 1981). Several models have been developed to
explain variation in this kind of parental investment (MONTGOMERIE & WEATHERHEAD
1988, REDONDO 1989). Parental investment theory predicts an increase in the inten-
sity of defence during the breeding cycle and with increasing brood size (WINKLER
1987, REDONDO 1989). On the other hand, because territorial defence generally
involves an expenditure of energy (GILL & WOLF 1975, CARPENTER & MACMILLEN
1976), the level of investment in territorial defence may be related to other factors
such as competition for nest sites, food or mates (PLESZCYZYNSKA & HANSELL 1980,
GOWATY et al. 1989, GARCÍA & ARROYO 2002).
Nest defence behaviour has been observed in most raptor species (e.g. SPROAT
& RITCHISON 1993, GALEOTTI et al. 2000, CARRILLO & APARICIO 2001, SERGIO &
BOGLIANI 2001), and the intensity of defence is positively associated to offspring
value (number of offspring, their age and their survival prospects, e.g. REGELMANN
& CURIO 1983, REDONDO 1989, HAKKARAINEN & KORPIMÄKI 1994). Sex differences
in the intensity of defence of raptors has often been related to sexual size dimor-
phism (SNYDER & WILEY 1976, ANDERSSON & NORBERG 1981, WIKLUND & STIGH 1983,
ANDERSSON & WIKLUND 1987). Few studies of raptors have documented temporal or
intersexual variation in territorial behaviour against conspecifics and heterospecifics
in a non-simulated natural scenario (FERRER 1990, PANDOLFI & PINO D’ASTORE 1992,
GARCÍA & ARROYO 2002). Particularly absent are detailed studies on such behav-
iour in vultures, a group with moderate differences between males and females.
Although some species of vultures are known to be territorial and to defend the
area around their nest against conspecifics and heterospecifics (MUNDY et al. 1992),
several factors suggest that the territorial behaviour of vultures should differ from
that of other raptors. For example, the low sexual dimorphism in body size and
specialized feeding habits may be responsible for the relatively equal distribution
of parental roles (NEWTON 1979, MUNDY et al. 1992, MARGALIDA & BERTRAN 2000a).
Moreover, the considerably long time that breeding vultures spend at the nest, in
addition to nest inaccessibility, makes their eggs and young less likely to be depre-
dated than those of other raptors. Territorial defence in vultures may be associated
with factors unrelated to predation risk.
The bearded vulture (Gypaetus barbatus) is a long-lived territorial vulture with
a wingspan of 260 cm and weighing 5-6 kg and females are slightly larger than
males (HIRALDO et al. 1979). This species nests on large rocky cliffs and feeds main-
ly on bones. Each breeding pair have several nests within their territory, which are
used in rotation across years (HEREDIA 1991, MARGALIDA & GARCÍA 1999). The pair
displays defensive behaviour around the nest against both conspecifics and heter-
ospecifics (see BERTRAN & MARGALIDA 1996, 2002a).
Although most clutches are of two eggs, only one chick is reared success-
fully and the Pyrenean population is characterized by its low productivity (0.43
fledglings/breeding pair/year; n = 115; MARGALIDA et al. 2003, 2004). Most breed-
ing failures occur during hatching (51%), followed by chick-rearing (28%) and the
incubation period (21%) (MARGALIDA et al. 2003). No nest predation has been docu-
Territorial behaviour of the bearded vulture 53

mented in this species (HEREDIA 1991, MARGALIDA et al. 2003) but more informa-
tion on its behaviour could have important implications in the conservation of this
endangered species.
The aims of this study are to examine sex differences in the intensity of nest
defence in a long-lived and large vulture, the bearded vulture, and to analyse vari-
ations in the intensity of defence in relation to the breeding stage and the species
attacked.

METHODS

Study area

Between 1992 and 1996 we obtained information on inter- and intraspecific agonistic
behaviour) in the course of a study of the bearded vulture’s breeding biology (BERTRAN &
MARGALIDA 1999; MARGALIDA & BERTRAN 2000a, 2000b; MARGALIDA et al. 2003). The study was
carried out on the central Pyrenean population of bearded vultures in a 3750 km2 area in
Catalonia, north-eastern Spain. In this area there is no annual variation in food availability,
and food resources are sufficient to meet the breeding pairs’ annual requirements (MARGALIDA
et al. 1997); therefore, annual variation in behaviour, aside from that imposed by the demands
of reproduction, is not expected (HAKKARAINEN & KORPIMÄKI 1994). In the study area, bearded
vulture nests are situated on rocky cliffs at altitudes between 650 m and 2100 m a.s.l. The
average (± SD) distance between nests belonging to the same pair was 1.7 ± 2.8 km. Other
raptorial species inhabit the same cliff or surrounding area (< 3 km from the bearded vulture
nests): there were six pairs of golden eagles (Aquila chrysaetos) in the same territory (distance
from a bearded vulture nest was 3.10 ± 1.16 km), and eagles were occasionally observed in
nine other territories; eight pairs of ravens (Corvus corax) on the same cliff (distance from
a bearded vulture nest was 0.22 ± 0.01 km), and ravens were regularly observed in nine ter-
ritories; 93 breeding pairs of Eurasian griffon vulture (Gyps fulvus) on the same cliff in six
territories (all the nests placed < 1 km from the bearded vulture nests) and were regularly
observed in nine territories; two pairs of Egyptian vulture (Neophron percnopterus) in the
same territory (average distance of 2.5 ± 1.25 km) and occasionally observed in five territo-
ries. However, the proximity between nesting sites and the movements mean that interactions
can occur with all the species.

Data collection

The breeding cycle was divided into three periods: pre-laying, incubation and chick-
rearing. Collectively, the three periods span from October (the start of nest rebuilding) to July
(when the chicks leave the nest, see HEREDIA 1991, MARGALIDA et al. 2003). In total, 612 hr of
observation over 106 days were carried out during the pre-laying period (2 months before lay-
ing to laying onset, n = 8 pairs), 419 hr over 53 days during the incubation period (from first
egg to hatching, n = 7 pairs) and 1443 hr over 187 days during chick rearing (from hatch-
ing to fledging, n = 9 pairs); 20-60 × telescopes were used and observations were carried out
300-600 m from the nest. We defined bearded vulture attacks as any behaviour consisting of
an aerial chase, with or without physical contact, until the intruder was expelled from the
vicinity of the nest. During the observations, notes were made of the sex of the attacking indi-
vidual and the species attacked. Although males and females in this species are considered
sexually monomorphic (HIRALDO et al. 1979), females are slightly larger than males and tend
to be more intensely colored (NEGRO et al. 1999). Variation in moult patterns was also useful
for identifying individuals.
54 A. Margalida and J. Bertran

Statistical analysis

Each observation day was taken as a sampling unit. For each observation day and pair,
an attack rate was calculated as the number of attacks divided by the number of hours of
observation. To avoid pseudoreplication, the average daily frequency was calculated for each
of the pairs. Given that these data did not follow a normal distribution, differences among
periods were tested with the Kruskal-Wallis test and sex differences with the Mann-Whitney
U test. To evaluate the significance of the attacks in relation to breeding periods and how
intersexual variation of defence relates to the various species, the χ2 test was applied (SOKAL
& ROHLF 1981).

RESULTS

A total of 280 territorial defence attacks was observed, of which 141 were
directed to griffon vultures (50.4%), 87 to ravens (31.1%), 32 to other bearded vul-
tures (11.4%) and 20 to golden eagles (7.1%).
Significant differences were found among species and periods during the
nesting cycle (χ62 = 33, P < 0.0001, Fig. 1). The griffon vulture was the species most
often attacked during the three periods (pre-laying: 56.2%, n = 48, incubation: 59%,
n = 39 and chick-rearing: 47.1%, n = 193), while the proportion of attacks on the
remaining species varied. During the pre-laying period, the species that received the
second largest number of attacks was the bearded vulture (22.9%), followed by the
golden eagle during incubation (17.9%) and the raven during chick-rearing (39.9%).
Although both sexes increased the levels of territorial defence as the breeding
cycle progressed, the differences were not significant (males: Kruskal-Wallis H2 =

���
��
��
��
������������

��
��
��
��
��
��
�
��������� ���������� �������������
Fig. 1. — Frequency distributions (%) of the species attacked by bearded vultures during the breed-
ing cycle. Dark grey column: griffon vulture; white column: golden eagle; black column: raven; light
grey column: bearded vulture.
Territorial behaviour of the bearded vulture 55

1.78, P = 0.41; females: Kruskal-Wallis H2 = 2.31, P = 0.31, Fig. 2). Attack rate was
significantly higher in males than females during the pre-laying period (0.07 ± 0.028
vs 0.015 ± 0.016 attacks/hr, respectively, Mann-Whitney U, z = 2.31, P = 0.021), but
not during incubation (0.068 ± 0.03 vs 0.031 ± 0.017 attacks/hr, z = 0.38, P = 0.701),
or chick-rearing (0.098 ± 0.026 vs 0.055 ± 0.015 attacks/hr, z = 1.37, P = 0.17).
During the four months of chick-rearing, no differences in the levels of territorial
defence were found (males: Kruskal-Wallis H3 = 0.55, P = 0.91; females: Kruskal-
Wallis H3 = 1.77, P = 0.62, Fig. 3).

0.14

0.12

0.1
����������������

0.08

0.06

0.04

0.02

�
��������� ���������� �������������
Fig. 2. — Temporal variation in the average frequency of attacks hr–1 by male (white columns) and
female (black columns) bearded vultures during the breeding cycle.

0.2

0.16
����������������

0.12

0.08

0.04

�
� �� ��� ��
������������������������
Fig. 3. — Variation in average frequency of attacks hr–1 by male (white columns) and female (black
columns) bearded vultures over the chick-rearing period.
 56
Table 1.
Mean ± SD rate of attacks (attacks hr–1) and species attacked by male and female bearded vultures during the breeding cycle. The absolute frequen-
cies are given in brackets.

Male Female

Kruskal- Kruskal-
Prelaying Incubation Chick-rearing Prelaying Incubation Chick-rearing
Wallis Wallis

Griffon
0.028 ± 0.035 (25) 0.036 ± 0.075 (15) 0.053 ± 0.088 (53) P = 0.532 0.002 ± 0.006 (2) 0.019 ± 0.03 (8) 0.036 ± 0.054 (38) P = 0.237
vulture

Golden
0.0007 ± 0.002 (1) 0.012 ± 0.016 (6) 0.007 ± 0.012 (6) P = 0.245 0.0005 ± 0.001 (2) 0.002 ± 0.005 (1) 0.002 ± 0.003 (4) P = 0.824
eagle

Raven 0.008 ± 0.012 (6) 0.009 ± 0.014 (2) 0.039 ± 0.048 (51) P = 0.177 0.0007 ± 0.002 (1) 0.013 ± 0.032 (1) 0.021 ± 0.016 (26) P = 0.023

Bearded
0.024 ± 0.041 (8) 0.005 ± 0.007 (3) 0.006 ± 0.008 (9) P = 0.426 0.008 ± 0.019 (3) 0.005 ± 0.007 (3) 0.003 ± 0.005 (6) P = 0.971
vulture

Table 2.
Territorial defence behaviour (means ± SD attacks hr–1) by male and female bearded vultures that shared and did not share the same cliff with Eura-
sian griffon vultures.

Male Female

With griffon Without griffon Mann-Whitney With griffon Without griffon Mann-Whitney
P P
vultures vultures U-test z vultures vultures U-test z

Pre-laying 0.097 ± 0.039 0.025 ± 0.007 2.24 0.025 0.019 ± 0.023 0.008 ± 0.007 0.74 0.45
Incubation 0.104 ± 0.117 0.02 ± 0.034 1.06 0.29 0.045 ± 0.051 0.001 ± 0.014 0.35 0.72
Chick-rearing 0.129 ± 0.100 0.046 ± 0.038 1.10 0.27 0.084 ± 0.064 0.019 ± 0.021 1.96 0.05
A. Margalida and J. Bertran
Territorial behaviour of the bearded vulture 57

���
��
��
��
�����������

�� ���������������
�����
��
������������
�� ���������������
��
��
��
�
��� ��� �� �� ��� ���
Fig. 4. — Frequency distributions (%) of the species attacked by bearded vultures during the breed-
ing cycle. PLM: pre-laying males; PLF: pre-laying females; IM: incubating males; IF: incubating
females; CRM: chick-rearing males; CRF: chick-rearing females.

We could not detect a difference between the sexes in the proportion of

attacks on the different species (χ23 = 0.31, P = 0.96, Table 1). Across periods, the
only significant differences were found in the higher proportion of attacks by males
on griffon vultures during the pre-laying period (χ22 = 10.95, P = 0.0019, Fig. 4). The
comparison between territories that are found in the same cliff as griffons and
those that are not, revealed that males in the former territories were more aggres-
sive during the pre-laying period, and females attacked more during the chick-
rearing period (Table 2).
The frequency of attacks per hour shows that in both sexes the tendency was
to increase or remain constant as the breeding period progressed, except in the
case of conspecifics where it progressively decreased. The only significant increase
occurred in the females when they increased their aggression towards the ravens
during the chick-rearing period (Kruskal-Wallis H2 = 7.58, P = 0.023, Table 1).

DISCUSSION

Interspecific interactions

Competition for nest sites, food and the potential risk of predation may affect
the bearded vulture’s nest defence behaviour towards heterospecifics. Overall,
although there is no information on the frequency of the intrusions, the level of the
attacks appears to be related to the abundance of species and the frequency with
which the birds fly around the nesting area. Most interactions were observed with
58 A. Margalida and J. Bertran

griffon vultures as consequence that they are the most abundant species and breed
in the same nesting sectors, competing with the bearded vulture for the occupa-
tion of nesting sites (MARGALIDA & GARCÍA 1999) and occasionally for food resources
(MARGALIDA & BERTRAN 2003). If nest sites were being protected, the intensity of
defence during the breeding season would vary little. Because intruder pressure
could affect the intensity of defence (MYERS et al. 1979), the attacks towards grif-
fons throughout the breeding period could function to advertise the occupancy of
the nesting site (BERTRAN & MARGALIDA 2002a).
With regard to ravens, defence could function to prevent predation on off-
spring (BERTRAN & MARGALIDA 2005). Although the density of this species is not
high, most vulture territories have a few pairs of ravens in the surrounding area
(pers. obs). The continuous presence of one of the adults at the nest during the first
weeks of the chick’s life would make it difficult for the ravens to be successful pred-
ators. Nevertheless, the accumulation of prey in the nest that ravens might steal at
a time when ravens start breeding would explain the greater number of interactions
with this species.
In the case of the golden eagle, interactions coincided with this species’
pre-laying period during which it displays greater territorial aggression (BERGO
1987). The lack of interactions with Egyptian vultures would similarly appear to
be due to the scarcity of these birds in the vicinity of bearded vulture nests. The
territorial behaviour defending nesting sites and not the competition for special-
ized food resources (MARGALIDA & BERTRAN 2003) would explain the interspecific
interactions.

Intraspecific interactions

Nest defence against conspecifics mainly took place during the pre-
laying period and could be linked to sperm competition (BIRKHEAD 1988) and food
resource competition (TEMELES 1989). If males are territorial to protect paternity,
the intensity of their defence should peak during the pre-laying period, coincid-
ing with the pair’s sexual activity (BERTRAN & MARGALIDA 1999) and when mate
choice and mate changes may occur (WIKLUND & VILLAGE 1992, MOUGEOT et al.
2001). Aggression towards conspecifics of breeding age can serve to avoid extrapair
copulation attempts, although the risk in this species is low (BERTRAN & MARGALIDA
1999). Nevertheless, in this period the weather might have made it hard to find
food and floaters visited the nesting sectors regularly (ossuaries and perches) where
the remains of food accumulate (BERTRAN & MARGALIDA 1996, MARGALIDA & BERTRAN
2001). The decrease in interactions during incubation and the chick-rearing period
could be explained by two factors (i) the end of the period of sexual activity and (ii)
more favourable weather conditions which would increase the availability of food
resources and thus make them easier to obtain. In this respect, it appears that con-
specifics, and perhaps many heterospecifics, minimize the costs of kleptoparasitic
interactions by avoiding chases in flight and acting in ossuaries, perches and nests,
when adults are not present in the territory (MARGALIDA & BERTRAN 2003). In fact,
the presence of adults perched on spots overlooking the nesting sites would act as
a territorial sign, since the coloration of the ventral region acts as a status signal
(NEGRO et al. 1999). This behaviour would reduce the costs of territorial mainte-
nance (YDENBERG et al. 1988, SEVERINGHAUS 2000).
Territorial behaviour of the bearded vulture 59

Sexual differences in the intensity of nest defence

As a whole, male bearded vultures defended nest sites more vigorously against
conspecifics and heterospecifics than did females, although the only significant
differences occurred during the pre-laying period. In many territorial birds, males
and females react to intruders of their own sex but do not co-operate in territorial
defence when the intruders are of the opposite sex (ARCESE 1989). Because polyan-
dry occurs in the bearded vulture (HEREDIA & DONÁZAR 1990, BERTRAN & MARGALIDA
2002b), one would expect males to react more aggressively. On the other hand, the
males’ greatest investment in nest defence and nest building during the pre-laying
period has been linked to the costs and benefits of these activities (MARGALIDA &
BERTRAN 2000a, 2000b). Males may be interested in having their females avoid
expending excessive energy, which affects their physical condition or the decision to
breed. In addition, females may be able to assess a male’s breeding capacity throu-
gh his activity in building and defending the nest, as has been suggested for other
species (CURIO et al. 1985, SOLER et al. 1998).
In the bearded vulture the division of aggressiveness appears to be related to
the cost of breeding and the balance in the reproductive effort between the sexes
(TRIVERS 1972). Nevertheless, the optimal defence level may also be affected by
parental age and experience (TOLONEN & KORPIMÄKI 1995). In terms of parental
investment, the greater contribution by males in nest defence may be considered
to balance out the greater investment the females in other parental activities (MAR-
GALIDA & BERTRAN 2000a).

Intensity of defence in relation to the breeding stage

In the bearded vulture, for both sexes, the intensity of defence increased from
pre-laying through fledging consistent with parental investment theory. Several
hypotheses have been put forward to explain the temporal change in defence and
our results suggest an increase in nest defence during the nesting cycle consistent
with all the hypotheses:
(a) With respect to the age-investment hypothesis based on cumulative past
parental investment or current/future expected reproductive success (ANDERSSON et
al. 1980, CURIO et al. 1985, REDONDO & CARRANZA 1989), the bearded vulture’s paren-
tal investment in reproduction is significant. The spatial and temporal unpredict-
ability of food resources implies the necessary collaboration of both sexes and only
one chick is reared successfully (BROWN 1990, MARGALIDA & BERTRAN 2000a). More-
over, breeding failures during hatching and chick-rearing are frequent (MARGALIDA
et al. 2003). The increase in nest defence from incubation to the chick-rearing
period could be explained by the increase in the reproductive value of the offspring
(VIÑUELA et al. 1995).
(b) According to the predation risk hypothesis based on the vulnerability and
conspicuousness of older nestlings to predators (HARVEY & GREENWOOD 1978, GREIG-
SMITH 1980, BRUNTON 1990), the intensity of defensive behaviour against ravens (the
most likely potential predator) should increase during the chick-rearing period.
During this period, the bearded vultures’ defensive behaviour was significantly grea-
ter during hatching and the first weeks of the chick’s life, coinciding with the most
critical period because small chicks may be predated by ravens (BERTRAN & MARGA-
LIDA 2005).
60 A. Margalida and J. Bertran

(c) Regarding the renesting potential hypothesis based on the opportunities to

renest during that breeding season (BARASH 1975), in the bearded vulture replace-
ment clutches are unusual as a consequence of a long breeding period that implies
that, in this long-lived species, natural selection may favour a low reproductive
effort in any one season in the interest of improving the probability of breeding in
future seasons (MARGALIDA & BERTRAN 2002).
(d) In accordance with the revisitation hypotheses or habituation hypothesis
based on greater or lesser aggression, respectively, as a consequence of the repeated
visits of the potential predator (KNIGHT & TEMPLE 1986, MONTGOMERIE & WEATH-
ERHEAD 1988, respectively), adapted to heterospecifics, the continual interspecific
interactions with griffon vultures or ravens over the nest site or food (MARGALIDA
& GARCÍA 1999, MARGALIDA & BERTRAN 2003) may have conditioned the adults’ pro-
gressive learning. The results suggest that nest defence against griffons was more
intense in the pairs proximate to numbers of griffons and, therefore, where there
were more intruders regularly flying in the area (BERTRAN & MARGALIDA 2002a).

ACKNOWLEDGEMENTS

We thank G.R. Bortolotti, J. Faaborg, M. Pandolfi and J. Viñuela for valuable comments
on the manuscript. S. Hardie translated the text into English. Financial support was received
from Departament de Medi Ambient of Generalitat de Catalunya.

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