Table Of Content.
June 2003 Short Communications 157
determination of endangered species status for the Pygmy-Owl {Glauddium brasilianum cactorum) Novem-
cactus Ferruginous Pygmy-Owl {Glauddium brasilia- ber 27, 2002. Federal Register 67(229):71032-71064
num cactorum) in Arizona. Federal Register 62(46): United States Fish and Wildufe Service. 2003. Cactus
10730-10747. Ferruginous Pygmy-Owl {Glauddium brasilianum cac-
NM A
United States Fish and Wii.dlife Service. 2002. Pro- torum) draft recovery plan. Albuquerque, U.S
posed rule. Endangered and threatened wildlife and
plants; designation of critical habitat for the Arizona Received 2 May 2002; accepted 15 March 2003
distinct population segment ofthe cactus Ferruginous Associate Editor: Clint Boal
RaptorRes. 37(2):157-160
J.
© 2003 The Raptor Research Foundation, Inc.
Interspecific and Intraspecific Ki.eptoparasitic Interactions oe the Bearded Vulture
Gypaetus barbatus) at Nesting Areas
(
Antoni Margalida’ and Joan Bertran
Group ofStudy and Protection of the Bearded Vulture, Apdo. 43, E-25520, El Pont de Suert, Lleida, Spain
Key Words: Bearded Vulture, Gypaetus barbatus; inter- In the eastern Pyrenees, the Bearded Vulture popula-
specific interactions', intraspecific interactions', kleptoparasitism', tion occurs in a high population density (Margalida et al.
nesting areas. 2003) and with an abundant food supply (Margalida et
al. 1997). These factors suggest a low frequency of klep-
Kleptoparasitism is the stealing ofpreviously procured toparasitism events because this feeding strategy is fa-
food from heterospecifics or conspecifics (Brockmann vored when food is less abundant (Stillman et al. 1997).
and Barnard 1979). This behavior is quite widespread On the other hand, a low frequency of interspecific in-
among birds, especially among seabirds (Furness 1987). teractions would be expected as consequence oflow ben-
Although kleptoparasitic interactions in vultures have efits that could be obtained by heterospecifics from steal-
been reported in the literature (Brockmann and Barnard ing a specialized food such as bone remains.
1979, Pascual and Santiago 1991, Bertran and Margalida In this note, we document some interspecific and m-
1996, Margalida and Heredia 2002) information on this traspecific kleptoparasitic interactions of the Bearded
behavior at nesting areas is scarce. This may be due to Vulture at nesting areas and we analyze the factors af-
the fact thatvulture species generally interact around the fecting this behavior.
carcass (vMvarez et al. 1976, Konig 1983, Blanco et al.
Materiai. and Methods
1997, Mundy et al. 1992) and that they deliver food,
which they carry in their crop to the nest, making theft Fieldwork was undertaken between 1991-97 in the cen-
of this food by other birds difficult. tral Pyrenees (Catalonia, northeast Spain) during alarger
study of the breeding biology of this species (Margalida
The Bearded Vulture {Gypaetus barbatus) is a solitary and Bertran 2000). Eight focal pairs were studied and we
and territorial osteophagous vulture that inhabits moun- recorded incidental observations of another seven pairs
tain areas ofthe southern Palearctic and the Afrotropical during the pre-laying, incubation, and chick-rearing pe-
region (del Hoyo et al. 1994). In contrast to the ecology riods (September-July)
of other vultures, this species presents some features that Bearded Vulture nests are situated on rocky cliffs at
may favor kleptoparasitism: (1) the carrying of large altitudes between 650 m and 2100 m. Among the species
bones or bone fragments that are visible to other species, which coexist with the Bearded Vulture and which often
(2) the repeated breaking actions that take place in the interact with it are the Golden Eagle {Aquila chrysaetos)
woshseurareiepsr,eyanidtem(s3)actchuemuplraetdiecta(boislsuiatryieosf, fpeorocdhesso,uracneds t(e1r0us)ter(rfiotuorriteesr)r,ittohreiesE)g,yptthieaCnoVmulmtourne R{aNveeonphr{oGnorpveurscncoopr--
ax) (14 territories), and the Eurasian Griffon {Gypsful-
nests). Nevertheless, kleptoparasitic events involving the
vus) (nine territories). At the same time, there are also
Bearded Vulture have only been reported occasionally
intraspecific interactions with individuals of various age
(Elosegi 1989). classes (immatures, <3 yr; subadults 4—5 yr; adults >6 yr)
that often visit the nesting areas.
Observationswere made using 20-60X telescopes from
^ E-mail address: [email protected] vantage points that allowed a good view of nesting sites
158 Short Communications VoL. 37, No. 2
Table 1. Inter- and intraspecific kleptoparasitic actions er the prey, which fell into a wooded area from which it
of Bearded Vultures observed in nesting areas in Spain. could not be recovered. In the remaining 31 interactions,
the Bearded Vulture acted as host. In flight it was klep-
Host toparasitised only twice, both by Golden Eagles which
chased and took from the vultures’ talons the prey they
Bearded were carrying. On one of these occasions, the prey was
Vulture Golden dropped and the eagle retrieved it before it touched the
Kleptoparasite (Adult) Eagle ground. Of the other 29 occasions, the Bearded Vulture
suffered 16 of the thefts at the nest by ravens and 13 of
Bearded Vulture (immature) 19 0
the thefts at ossuaries by Eurasian Griffons. As occurred
Bearded Vulture (subadult) 2 0
with intraspecific interactions, interspecific events of
Bearded Vulture (adult) 1 1
kleptoparasitism mostly occurred in those places where
Golden Eagle 2 0
food was accumulated/gathered, with kleptoparasitic
Griffon Vulture 13 0
=
Common Raven 16 0 chasesPi<n flight being significantly infrequent (x^i
12.44, 0.001).
Discussion
(300-600 m). Notes were made of all interactions in
which food was stolen, the species involved, and the sit- Our results suggest that the non-breeding population
uation in which they occurred (in flight, on the nest, at of Bearded Vultures, perhaps due to limited foraging ef-
an ossuary, or on a perch). In all intraspecific interac- ficiency (Brown 1988, Bertran and Margalida 1996), as
tions observed, we recorded the individual’s age, which has been suggested with other species (Fisher 1985, Cal-
was determined following Bertran and Margalida (1996). dow et al. 1999), are making use of the spatial and tem-
poral predictability of food resources by becoming klep-
Results
toparasites. All thefts suffered at the nest by breeding
We observed 54 interactions consisting of food theft, pairs ofBearded Vulture took place during chick-rearing,
26 of which took place at ossuaries, 24 at the nest, 3 in a period when prey items often accumulate at the nest
flight, and 1 on a perch. Twenty-two of all interactions sites. Thefts at ossuaries or in flight occurred duringwin-
were intraspecific, while the remaining 32 were interspe- ter (pre-laying and incubation periods), a time when
cific. No significant difference was observed among the food availability is reduced and weather may greatly limit
situations where the two types of interactions took place the activities offoraging and locating food. For those age
(X^2 “ 1.5, P = 0.47). In 96.3% of all interactions Beard- groups (principally <3 yr) that are more dependent on
ed Vulture adults acted as hosts and only in two did they predictable food sources such as feeding stations (Here-
act as kleptoparasite (Table 1). dia 1991), this might be a foraging strategy used much
Intraspecific Interactions. Thirteen of all intraspecific more regularly. These results are in agreement with the
thefts took place at the ossuaries, eight at the nest, and idea that immature or inexperienced birds may compen-
only one in flight. The frequency of thefts observed was sate for their less-effective foraging abilities by kleptopar-
higher than expected in places where prey remains ac- asitism (Wunderle 1991). To the contrary, kleptoparasi-
cumulated, such as nests or ossuaries. Direct kleptopar- tism by adults could be an opportunistic foraging
asitic actions in flight were avoided (x^i = 9.28, P < behavior. Nevertheless, our observations were mainly
0 001). Twenty-one actions (95.5%) were carried out by done close to the nest and do not include observations
non-breeding individuals. Birds that were less than 3 yr during foraging. This accounts for the fact that breeding
old took part in 19 ofall actions and this age group used adults were the host bird in 96% of all observed events.
this feeding strategy more often than expected (x^g = Nevertheless, the abundant food avalaible and the rela-
13.01, P < 0.001). The only kleptoparasitic action in tively infrequent number ofstolen prey, suggest thatklep-
flight took place between two adult birds in a territory toparasitism amounts to a small cost for the breeding
held by a polyandrous quartet. The parasitic individual pairs, without any measurable impact on breeding suc-
followed insistently a bird that was carrying the bone re- cess (see Margalida et al. 2003).
mains, flapping its wings vigorously. After an aerial chase As a result of the cost/benefit rate, two factors would
of 15 min, the adult bird that was carrying the remains determine that the species that attempted stealing would
dropped its prey, which the other adult bird collected on resort to this indirect strategy: the territorial behavior of
the ground. the Bearded Vulture (Margalida and Bertran 2000, Ber-
Interspecific Interactions. Of 32 interspecific interac- tran and Margalida 2002) and the accumulation of prey
tions observed in which food was stolen, in only one case remains in nesting areas. Dominance of adults over im-
was the Bearded Vulture the kleptoparasitic species: the matures is a well documented phenomenon in raptors
vulture robbed a Golden Eagle of the prey itwas holding (Newton 1979), but a reverse-dominance pattern also has
m
Its talons while perched in the vicinity ofits nest. Once been observed (Rodriguez-Estrella and Rivera-Rodriguez
m
flight, the eagle chased the vulture and tried to recov- 1992). In the case of conspecifics, plumage coloration of
June 2003 Short Communications 159
—
Bearded Vulture adults could act as status signal (Negro Resumen. Documentamos interacciones interespecifi-
et al. 1999). This signal could be used by territorial adults cas e intraspecificas de cleptoparasitismo en el quebran-
to displace other immature Bearded Vultures not by at- tahuesos en los sectores de nidificacion. De un total de
tacking them, but simply by signalling their status while 54 interacciones, 26 tuvieron lugar en rompederos, 24
approaching them (Bautista et al. 1998). On the other en el nido, tres en vuelo y uno en posaderos. Veintidos
hand, the Bearded Vulture’s low wing loading and its de las interacciones fueron intraspecificas y las 32 restan-
large wingspan give this species great dominance in flight tes interespecificas con cuervos {Corvus corax), buitres
(Donazar 1993) and make it difficult for an opponent to leonados {Gypsfulvus) y aguilas reales {Aquila chrysaetos).
steal food successfully. In the case ofconspecifics, the fact La mayoria de las interacciones tuvieron lugar en zonas
that younger birds are less skillful in flight would mean donde el aliraento se acumulaba (nidos y rompederos)
that they would be less successful in actions of direct pi- evitando las acciones directas en vuelo. En el caso de los
racy, so that the energetic cost of those attempts might adultos, este comportamiento podria ser una accion
be greater than the likely benefits obtained from those oportunista pero para las aves de <3 anos si podria tra-
actions (Fisher 1985). tarse de una estrategia alimenticia. Puesto que la dispo-
Concerning the interspecific interactions, the prey re- nibilidad trofica es suficiente, la poblacion reproductora
mains consumed by Bearded Vultures mostly consisting esta incrementandose y las especies heterospecificas com-
of bone remains, would be energetically inadequate for piten por los mismos sectores de nidificacion, el clepto-
many raptor species (e.g., Golden Eagles). In the case of parasitismo podria estar relacionado con otros factores
Eurasian Griffons, they would be occasionally more in- no relacionados con la obtencion de alimento.
terested in obtaining bone remains at ossuaries (Bertran [Traduccion de los autores]
and Margalida 1997) in order to compensate for a pos-
Acknowi.edgments
sible lack of calcium in their diet (Mundy and Ledger
1976). The dominance of the Eurasian Griffon on the We would like to thank J.A. Donazar, P.J. Mundy, JJ.
ground, given its larger size and the accumulation of Negro, J.R. Garrido, J.M. Arcos, S. Xirouchakis, and an
anonymous reviewer for their comments on the manu-
bone fragments and splinters at ossuaries, would favor
script and C. Carboneras and S. Hardie for translating
the strategy of obtaining calcium at these sites (Bertran the text into English. Funding for the research was pro-
and Margalida 1997). Eurthermore, the Bearded Vul- vided by Departament de Medi Ambient of Generalitat
ture’s attacks of intruders in the vicinity of the nest de Catalunya and Fundacio Territori Paisatge.
i
throughout the breeding season (Brown 1988, Margalida
and Bertran 2000) would act as deterrent and would Literature Cited
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118:785-789. Received 18 April 2002; accepted 30 December 2002
AND D. GarciA. 1999. Nest use, interspecific rela- Associate Editor:Juan Jose Negro
