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Interspecific and intraspecific kleptoparasitic interactions of the bearded vulture (Gypaetus barbatus) at nesting areas PDF

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Preview Interspecific and intraspecific kleptoparasitic interactions of the bearded vulture (Gypaetus barbatus) at nesting areas

. 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 make food storages near the nest the least convenientfor Alvarez, E, L. Arias de Reyna, and F. Hiraldo. 1976 stealing. The success in aggressive encounters appears Interactions among avian scavengers in southern determined by the body size and condition, and the pre- Spain. Ornis Scand. 7:215-226. vious possession of the disputed resource (Bautista et al. Bautista, L.M.,J.C. Alonso, andJ.A. Ai.onso. 1998. For- 1998). In contrast, those species with higher aerial ma- aging site displacement in common crane flocks neuverability but with smaller size, such as ravens, would Anim. Behav. 56:1237-1243. have to focus their actions at the nest, where prey re- Bertran, and A. Margalida. 1996. Patron anual de J. mains also accumulate. Obtaining prey remains there observaciones de quebrantahuesos Gypaetus barbatus) may be less costly for those birds because; (1) adults are de diferentes grupos de edad en l(os sectores de ni- gradually less often present at the nest as the breeding dificacion. Alauda 64:171-178. season progresses (Brown 1990, Margalida and Bertran and a. Margalida. 1997. Griffon Vultures {Gyps 2000) and (2) prey items present in the nest have a high- fulvus) ingesting bones at the os.suaries of Bearded er meat content as consequence of differential require- Vultures {Gypaetus barbatus) RaptorRes. 31:287-288 J. ments in nutrients for the chick (Margalida and Bertran AND A. Margaijda. 200,2. Territorial behavior of 1997, Margalida and Bertran 2001). the Bearded Vulture in response to the Griffon Vul- Finally, kleptoparasitism could be a strategy of dem- ture. /. Field Ornithol. 73:86-90. onstrating dominance or competence (Bautista et al. Blanco, G.,J.M. Traverso,J. Marchamalo, and F. Mart- 1998). The fact that in our study area the Bearded Vul- Inez. 1997. Interspecific and intraspecific agression ture density is high (Margalida et al. 2003), heterospe- among Griffon and Cinereous Vultures at nesting and cifics compete by the same nest sites (Margalida and foragings sites./. RaptorRes. 31:77-79. Garcia 1999), and food supply is abundant, suggest that Brockmann, H.J. and C.J. Barnard. 1979. Kleptoparasi- kleptoparasitic actions could be determined by other re- tism in birds. Anim. Behav. 27:487-514. sources than food. For example, demonstrating domi- Brown, C.J. 1988. A study of the Bearded Vulture Gypae- nance or competence by nest sites or in breeding terri- tus barbatus in southern Africa. Ph.D. dissertation, tories may result in social benefits (Caldow et al. 1999, Univ. Natal, Pietermaritzburg, South Africa. Yates et al. 2000). . 1990. Breeding biology of the Bearded Vulture : , . 160 Short Communications VoL. 37, No. 2 in southern Africa, Part II: the nestling period. Ostrich tionship and competition for nests in the Bearded 61:33-42. Vulture Gypaetus barbatus in the Pyrenees: influence Galdow, R.W.G., J.D. Goss-Gustard, R.A. Stillman, on breeding success. Bird Study 46:224-229. S.E.A. LE V. BIT DURELL, R. SwlNFEN, AND T. BrEGN- D. Garcia, Bertran, and R. Heredia. 2003. , J. BALLE. 1999. Individual variation in the competitive Breeding biology and success of the Bearded Vulture ability of interference-prone foragers: the relative im- (Gypaetus barbatus) in northeastern Spain. Ibis 145: portance of foraging efficiency and susceptibility to 244-252. interference./. Anim. Ecol. 68:869-878. D. GarcIa, and R. Heredia. 1997. Estimacion de , DEL Hoyo, A. Ellioit, andJ. Sargatal. (Eds.). 1994. la disponibilidad trofica para el Quebrantahuesos J., Handbook ofthe birds ofthe world. Vol. 2, Newworld (Gypaetus barbatus) en Gataluna (NE Espana) e impli- vultures to guineafowl. Lynx Ed., Barcelona, Spain. cacions sobre su conservacion. Dohana Acta Vert. 24: Donazar, J.A. 1993. Los buitres ibericos: biologia y con- 235-243. servacion. J.M. Reyero [Ed.], Madrid, Spain. and R. Heredia. 2002. Interspecific interaction Elosegi, I. 1989. Vautour fauve {Gyps fulvus), Gypaete between Lammergeier Gypaetus barbatus and Black barbu {Gypaetus barbatus) Percnoptere d’Egypte Vulture Aegypius monachux predation or kleptoparasi- (Neophron percnopterus) synthese bibliographique et tism? Sandgrouse 24:138-139 recherches. Acta Biologica Montana. Serie documents Mundy, R, D. Butchart, J. Ledger, and S. Piper. 1992. de travail, 3. GBEA, Pau, France. The vultures ofAfrica. Academic Press, London, U.K. Fisher, D.L. 1985. Piracy behavior of wintering Bald Ea- AND J.A. Ledger. 1976. Griffon vultures, carni- gles. Condor87:246-251. vores, and bones. S'. Afr.J. Sci. 72:106-110. Furness, R.W. 1987. Kleptoparasitism in seabirds. Pages Negro, JJ-. A. Margalida, F. Hiraldo, and R. Heredia. 77-101 mJ.P. Groxall [Ed.], Seabirds: feeding ecology 1999. The function of cosmetic colouration ofBeard- and role in marine ecosystems. Gambridge Univ. ed Vultures: when art imitates life. Anim. Behav. 58: MA Press, Gambridge, U.S.A. F14-F17. Heredia, R. 1991. Alimentacion y recursos alimenticios. Newton, I. 1979. Population ecology ofraptors. T. &A.D. Pages 79-89 in R. Heredia and B. Heredia [Eds.], El Poyser, Berkhamsted, U.K. Quebrantahuesos (Gypaetus barbatus) en los Pirineos. Pascual, and J.M. Santiago. 1991. Egyptian Vultures J. IGONA, Goleccion Tecnica, Madrid, Spain. steal food from nestling Griffon Vultures./. RaptorRes. Konig, G. 1983. Interspecific and intraspecific competi- 25:96-97. tion for food among old world vultures. Pages 153- RodrIguez-Estrella, R. and L. Rivera-Rodriguez. 1992. 171 in S.R. Wilbur and J.A. Jackson [Eds.], Vulture Kleptoparasitism and other interactions of Grested biology and management. Univ. Galifornia Press, Garacara in the Gape Region, Baja Galifornia, Mexico. Berkeley and Los Angeles, GA U.S.A. /. Field Ornithol. 63:177-180. Margalida, a. and j. Bertran. 1997. Dieta y seleccion Stillman, R.A.,J.D. Goss-Gustard, and R.W.G. Galdow. de alimento de una pareja de Quebrantahuesos 1997. Modelling interference from basic foraging be- (Gypaetus barbatus) en los Pirineos durante la crianza. haviour. / Anim. Ecol 66:692-703. Ardeola 44:191-197. Wunderle,J.M.,Jr. 1991. Age-specific foraging proficien- and j. Bertran. 2000. Breeding biology of the cy in birds. Curr. Ornithol. 8:273—324. Bearded Vulture Gypaetus barbatus:. minimal sexual dif- Yates, M.G., R.A. Stili.man, and J.D. Goss-Gustard. ferences in parental activities. Ibis 142:225-234. 2000. Gontrasting interference functions andforaging AND Bertran. 2001. Function and temporal var- dispersion in two species of shorebird (Gharadrii)./ J. iation in the use of ossuaries by Bearded Vultures Anim. Ecol. 69:314—322. (Gypaetus barbatus) during the nestling period. Auk 118:785-789. Received 18 April 2002; accepted 30 December 2002 AND D. GarciA. 1999. Nest use, interspecific rela- Associate Editor:Juan Jose Negro

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