JUNE2003 SHORTCOMMUNICATIONS 157

detcrnfination of endangered speciesstatus for the Pygmy-Owl( Glaucidiumbrasilianum cactorum) Novem- cactus Ferruginous Pygmy~Owl(Glauddium brasilia- ber 27, 2002. FederalRegister 67(229):71032-71064 num cactorum)in Arizona. Federal Register 62(46): UNITED STATES FISH AND WIEDIJFE SERVICE. 2003. Cactus 10730-10747. Ferruginous Pygmy-Owl ( Glaucidiumbrasilianum cac- UNITED STATES FISH AND WILDEIFE SERVICE. 2002. Pro- torum)draft recovery plan. Albuquerque, NM U.S A posed rule. Endangered and threatened wildlife and plants;designation of critical habitat for the Arizona Received2 May 2002; accepted15 March 2003 distinctpopulation segment of the cactusFerruginous Associate Editor: Clint Boal

j. RaptorRes. 37(2):157-160 ¸ 2003 The Raptor ResearchFoundation, Inc.

INTERSPECIFIC AND INTRASPECIFIC KLEPTOPARASITIC INTERACTIONS OF THE BEARDED ( GYPAETUSBARBATUS) AT NESTINGAREAS

ANTONIMARGALIDA 1 AND JOAN BERT1LhN Groupof Studyand Protectionof theBearded Vulture, Apdo. 43, 12'-25520,El Pontde Suert, Lieida, Spain

KEY WORDS: BeardedVulture, Gypaetus barbatus; inter- In the eastern Pyrenees,the Bearded Vulture popula- spedticinteractions; intraspecific interactions; kleptoparasitism; tion occursin a high population density (Margalida et al. nestinga2•as. 2003) and with an abundant food supply (Margalida et al. 1997). These factorssuggest a low frequency of klep- Kleptoparasitismis the stealingof previouslyprocured toparasitismevents because this feeding strategy is fa- food from heterospecificsor 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- amongbirds, especially among seabirds (Furness 1987). teractionswould be expected as consequenceof low ben- Although kleptoparasiticinteractions in have efits that could be obtained by heterospecificsfrom steal- been reported in the literature (Brockmannand Barnard ing a specializedfood suchas bone remains. 1979,Pascual End Santiago 1991, Bertran and Margalida In this note, we document some interspecific and in- 1996, Margalida and Heredia 2002) information on this traspecific kleptoparasitic interactions of the Bearded behavior at nesting areasis scarce.This may be due to Vulture at nesting areas and we analyze the factors af- the fact that vulture speciesgenerally interact around the fecting this behavior. carcass(,idvarez et al. 1976,K6nig 1983, Blanco et al. MATERIAE 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 difficult. tral Pyrenees(Catalonia, northeastSpain) during a larger studyof the breeding biologyof this species(Margahda The Bearded Vulture (Gypaetusbarbatus) is a solitary and Bertran 2000). Eight focal pairs were studied and we and territorial osteophagousvulture that inhabitsmoun- recorded incidental observationsof another seven pairs tain areas of the southern Palearctic and the Afrotropical during the pre-laying,incubation, and chick-rearingpe- region (del Hoyo et al. 1994). In contrastto the ecology riods (September-July). of other vultures, this speciespresents 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 specms bonesor bone fragmentsthat are visibleto other species, which coexist with the Bearded Vulture and which often (2) the repeated breaking actionsthat take place in the interact with it are the Golden (Aquila chtTsaetos) ossuaries, and (3) the predictability of food sources (10 territories), the (Neophronpercnop- terus) (four territories), the Common Raven (Corvus cor- where prey items accumulate (ossuaries,perches, and 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 intraspecificinteractions with individualsof variousage (Elosegi1989). classes(iramatures, <3 yr; subadults4-5 yr; adults>6 yr) that often visit the nesting areas. Observationswere made using 20-60X telescopesfrom 1 E-mail address:[email protected] vantagepoints that allowed a good view of nesting sites 158 SHORT COMMUNICATIONS VOL. 37, NO. 2

Table 1. Inter- and intrasp½cifickleptoparasitic 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 toparasitisedonly twice, both by Golden Eagleswhich chasedand 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 Bearded Vuhure (immature) 19 0 suffered 16 of the thefts at the nest by ravens and 13 of Bearded Vulture (subadult) 2 0 the thefts at ossuariesby Eurasian Griffons. As occurred Bearded Vulture (adult) 1 1 with intraspecific interactions, interspecific events of kleptoparasitismmostly occurred in those places where 2 0 13 0 food was accumulated/gathered,with kleptoparasitic Common Raven 16 0 chasesin flight being significantlyinfrequent (X2i = 12.44, P < 0.001).

DISCUSSION (300-600 m). Notes were made of all interactions in which food was stolen, the speciesinvolved, and the sit- Our resultssuggest that the non-breedingpopulation 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 intraspecificinterac- ficiency (Brown 1988, Bertran and Margalida 1996), as tions observed,we recorded the individual's age, which has been suggestedwith other species(Fisher 1985, Cal- wasdetermined following Bertran and Margalida (1996). dowet al. 1999), are making use of the spatial and tem- poral predictabilityof food resourcesby becoming klep- RESULTS toparasites.All thefts suffered at the nest by breeding We observed54 interactionsconsisting of food theft, pairs of BeardedVulture 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-twoof all interactions sites.Thefts at ossuariesor in flight occurred during win- were intraspecific,while the remaining 39 were interspe- ter (pre-laying and incubation periods), a time when cific. No significantdifference was observedamong the food availabilityis reduced and weather may greatlylimit situationswhere the two types of interactions took place the activitiesof foraging and locatingfood. For thoseage (X2s= 1.5, P = 0.47). In 96.3% of all interactionsBeard- groups (principally <3 yr) that are more dependent on ed Vulture adults acted as hostsand only in two did they predictable food sourcessuch as feeding stations(Here- act as kleptoparasite (Table 1). dia 1991), this might be a foraging strategyused much Intraspecific Interactions. Thirteen of all intraspecific more regularly. These resultsare 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 observedwas satefor their less-effectiveforaging abilitiesby 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 actionsin flight were avoided (xSi = 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 lessthan 3 yr during foraging. This accountsfor the fact that breeding old took part in 19 of all actionsand this age group used adults were the host in 96% of all observed events. this feeding strategymore often than expected (X22= Nevertheless, the abundant food avalaible and the rela- 13.01, P < 0.001). The only kleptoparasitic action in tivelyinfrequent number of stolenprey, suggest that klep- 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 insistentlya bird that wascarrying the bone re- cess (see Margalida et al. 2003). mains, flapping its wingsvigorously. After an aerial chase As a result of the cost/benefit rate, two factors would of 15 rain, the adult bird that was carrying the remains determine that the speciesthat attempted stealingwould dropped its prey,which the other adult bird collectedon 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 observedin which food wasstolen, in only one case remains in nesting areas.Dominance of adults over ira- was the Bearded Vulture the kleptoparasiticspecies: the matures is a well documented phenomenon in raptors vulture robbed a Golden Eagle of the prey it washolding (Newton 1979), but a reverse-dominancepattern alsohas in its talonswhile perched in the vicinityof its nest.Once been observed (Rodrlguez-Estrellaand Rivera-Rodriguez •n flight, the eagle chasedthe vulture and tried to recov- 1992). In the caseof conspecifics,plumage coloration of JUNE 2003 SHOP,T COMMUNICATIONS 159

Bearded Vulture adults could act as statussignal (Negro RESUMEN.--Documentamosinteracciones interespecifi- et al. 1999). This signalcould be usedby territorial adults case intraspecificasde cleptoparasitismoen el quebran- to displaceother immature Bearded Vultures not by at- tahuesos en los sectores de nidificaci6n. De un total de tacking them, but simplyby signallingtheir statuswhile 54 interacciones,26 tuvicron lugar en rompederos,24 approaching them (Bautista et al. 1998). On the other en el nido, tres en vuelo y uno en posaderos.Veinud6s hand, the Bearded Vulture's low wing loading and its de las interaccionesrueton intraspecificasy las 32 restan- large wingspangive this speciesgreat dominancein flight tes interespecificascon cuervos (Corvus corax),bratres (Don•tzar 1993) and make it difficult for an opponent to leonados(Gypsfulvus) y •tguilasreales (Aquilachrysaetos). stealfood successfully.In the caseof conspecifics,the fact La mayoria de las interaccionestuvieron lugar en zonas that younger birds are lessskillful in flight would mean donde el alimento se acumulaba (nidos y rompederos) that they would be lesssuccesslhl in actionsof 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 set una acc•6n be greater than the likely benefits obtained from those oportunistapero para las avesde <3 aftossi podria tra- actions (Fisher 1985). tarse de una estrategiaalimenticia. Puesto que la dispo- Concerningthe interspecificinteractions, the prey re- nibilidad tr6fica es suficiente,la poblaci6n reproductora mains consumedby Bearded Vultures mostlyconsisting esti incrementandosey las especiesheterospecificas com- of bone remains, would be energeticallyinadequate for pitch pot los mismossectores de nidificaci6n, el clepto- many raptor species(e.g., Golden ).In the caseof parasitismopodria estar relacionado con otros fhctores no relacionados con la obtenci6n de alimento. Eurasian Griffons, they would be occasionallymore in- terested in obtaining bone remains at ossuaries(Bertran [Traducci6n de los autores] and Margalida1997) in order to compensatefor a pos- ACKNOWLEDGMENTS sible lack of calcium in their diet (Mundy and Ledger 1976). The dominance of the Eurasian Griftbn on the We would like to thank J.A. Don/tzar, 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 fbr their comments on the manu- bone fragments and splinters at ossuaries,would favor script and C. Carbonerasand S. Hardie fbr translaung the strategyof obtaining calcium at these sites (Bertran the text into English.Funding fbr the researchwas pro- and Margalida 1997). Furthermore, the Bearded Vul- vided by Departament de Medi Ambient of Generahtat ture's attacks of intruders in the vicinity of the nest de Catalunyaand Fundaci6 Territori i Paisatge. throughoutthe breedingseason (Brown 1988, Margalida and Bertran 2000) would act as deterrent and would LITERATURE CITED make food storagesnear the nest the leastconvenient for •tLVAREZ,F., L. ARIASDE REYNA, AND F. HIRALDO.1976 stealing. The successin aggressiveencounters appears Interactions among avian in southern determined by the body sizeand condition,and the pre- Spain. OrnisScan& 7:215-226. vious possessionof the disputed resource (Bautistaet al. BAUTISTA,L.M., J.C. AEONSO,AND J.A. AEONSO.1998. For- 1998). In contrast, those specieswith higher aerial ma- aging site displacement in common crane flocks neuverabilitybut with smaller size,such as ravens,would Anita. Behar. 56:1237-1243. have to focus their actions at the nest, where prey re- BERTRAN,J. AND A. M-ARGALIDA.1996. Patrtn anual de mains also accumulate. Obtaining prey remains there observacionesde quebrantahuesos(Gypaetus barbatus) may be lesscostly for those birds because:(1) adults are de diferentes grupos de edad en los sectoresde m- graduallyless often present at the nest as the breeding dificacitn. Alauda 64:171-178. seasonprogresses (Brown 1990, Margalida and Bertran --AND A. MARGALIDA.1997. Griffon Vultures ( 2000) and (2) prey itemspresent in the nesthave a high- fulvus) ingesting bones at the ossuariesof Bearded er meat content as consequenceof dift•rential require- Vultures ( Gypaetusbarbatus). J. RaptorRes. 31:287-288 ments in nutrients for the chick (Margalida and Bertran --AND A. MARGALIDA. 2002. Territorial behavior of 1997, Margalidaand Bertran 2001). the BeardedVulture in responseto the Griffon Vul- Finally, kleptoparasitismcould be a strategyof dem- ture. J. FieldOrnithol. 73:86-90. onstrating dominance or competence (Bautista et al. BLANCO,G.,J.M. TP,AVEP, SO,J. MA•CnAMALO,AND F. MART- 1998). The fact that in our studyarea the Bearded Vul- [NEZ.1997. Interspecificand intraspecificagression ture densityis high (Margalida et al. 2003), heterospe- among Griffon and CinereousVultures at nesting and cifics compete by the same nest sites (Margalida and foragingssites. J. RaptorRes. 31:77-79. Garcia 1999), and food supplyis abundant,suggest that BROCKMANN,H.J. ANDC.J. BARNARD.1979. Kleptoparasi- kleptoparasiticactions could be determined by other re- fism in birds. Anita. Behar. 27:487-514. sourcesthan fbod. For example, demonstratingdomi- BP,OWN, C.J. 1988. A studyof the BeardedVulture Gypae- nance or competence by nest sitesor in breeding terri- tus barbatus in southern Africa. Ph.D. dissertanon, tories may result in social benefits (Caldow et al. 1999, Univ. Natal, Pietermaritzburg, . 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 Gypaetusbarbatus in the Pyrenees:influence COmDOW,R.W.G., J.D. GOss-CuSTAm),R.A. STILLMAN, on breeding success.Bird Study46:224-229. S.E.A. LE V. DIT DUP,ELL, R. SWINFEN, AND T. BREGN- --, D. GARCIA,J. BERTRAN,AND R. HEREDIA.2003. BALLE.1999. Individual variation in the competitive Breeding biology and successof the Bearded Vulture ability of interference-proneforagers: the relative im- (Gypaetusbarbatus) in northeastern Spain. Ibis 145: portance of foraging efficiency and susceptibilityto 244-252. •nterference.J. Anita. Ecol.68:869-878. --, D. GARCIA,AND R. HERED1A.1997. Estimaci6n de DELHoYo, J., A. ELLIO2T,ANDJ. SA•GATAL.(EDS.). 1994. la disponibilidad tr6fica para el Quebrantahuesos Handbook of the birds of the world. Vol. 2, New world (Gypaetusbarbatus) en Gatalufia (NE Espafia)e impli- vultures to guineafowl.Lynx Ed., Barcelona, Spain. cacions sobre su conservaci6n. Do•ana Acta Vert. 24: DONJ,ZAR, J.A. 1993. Los buRres ibfricos: biologia y con- 235-243. servaci6n.J.M. Reyero [ED.], Madrid, Spain. --AND R. HEREDIA.2002. Interspecific interaction ELOSEGI,I. 1989. Vautour fauve (Gypsfulvus), Gypa•te between Lammergeier Gypaetusbarbatus and Black barbu (Gypaetusbarbatus), Percnoptare d'Egypte Vulture Aegypiusmonachus: predation or kleptoparasi- (Neophronpercnopterus): synthase bibliographique et tism? Sandgrouse24:138-139. recherches.Acta BiologicaMontana. S6rie documents MUNDY,P., D. BUTGHART,J. LEDGER,AND S. PIPER.1992. de travail, 3. CBEA, Pau, France. The vultures of Africa. 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. votes,and bones. S. AfzJ. Sci.72:106-110. FURNESS,R.W. 1987. Kleptoparasitismin seabirds.Pages NEGRO,JJ., A. MARGALIDA,F. HIRALDO,AND R. HEREDIA. 77-101 in j.P. Croxall [ED.], Seabirds:feeding ecology 1999. The function of cosmetic colouration of Beard- and role in marine ecosystems.Cambridge Univ. ed Vultures: when art imitates life. Anita. Behav. 58: Press,Cambridge, MA U.S.A. F14-F17. HEREDIA,R. 1991. Alimentaci6n y recursosalimenticios. NEWTON,I. 1979.Population ecology of raptors.T. & A.D. Pages79-89 in R. Heredia and B. Heredia [EDS.], E1 Poyser,Berkhamsted, U.K. Quebrantahuesos(Gypaetus barbatus) en los Pirineos. PASCUAL,j. ANDJ.M. SANTIAGO.1991. EgyptianVultures ICONA, Colecci6n T6cnica, Madrid, Spain. stealfood from nestlingGriffon Vultures.J. RaptorRes. KONIG,C. 1983. Interspecificand intraspecificcompeti- 25:96-97. tion for food among old world vultures. Pages 153- RODRiGUEZ-ESTRELLA,R. AND L. PdVERA-RODRiGUEZ.1992. 171 in S.R. Wilbur and J.A. Jackson lEDS.I, Vulture Kleptoparasitismand other interactions of Crested biology and management. Univ. California Press, Caracarain the Cape Region,Baja California,Mexico. Berkeley and Los Angeles, CA U.S.A. J. Field Ornithol.63:177-180. MARGALIDA,A. ANDJ. BERTRAN.1997. Dieta y selecci6n STmLM_•N,R.A., J.D. GOss-CuSTAm),AND R.W.G. CALDOW. de alimento de una pareja de Quebrantahuesos 1997. Modelling interferencefrom basicforaging be- (Gypaetusbarbatus) en los Pirineosdurante la crianza. haviour.J. Anita. 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. Curt. Ornithol.8:273-324. BeardedVulture Gypaetusbarbatus: minimal sexualdif- YATES,M.G., R.A. STn.I.MAN,AND J.D. GOss-CuSTAm). ferences in parental activities.Ibis 142:225-234. 2000. Contrastinginterference functionsand foraging -- ANDJ. BERTRAN.2001. Function and temporal var- dispersionin two speciesof shorebird (Charadrii).J. iation in the use of ossuariesby Bearded Vultures Anita. Ecol. 69:314-322. (Gypaetusbarbatus) during the nestling period. Auk 118:785-789. Received18 April 2002; accepted30 December 2002 --AND D. GARGiA.1999. Nest use, interspecificrela- AssociateEditor: Juan Jos6 Negro