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1 Bird Study (1999) 46, Nest use, interspecific relationships and competition for nests in the Bearded Vulture Gypaetus barbatus in the Pyrenees: influence on breeding success ANTONI MARGALIDA 1 and DIEGO GARCÍA 2 1 Grup d Estudi i Protecció del Trencalòs (GEPT), Apartat Correus 43, E El Pont de Suert (Lleida), Spain and 2 Generalitat de Catalunya DARP, Direcció General del Medi Natural, Servei de Protecció i Gestió de la Fauna, Gran Via , E Barcelona, Spain Nest use and interspecific relationships were studied in the Bearded Vulture for nest location in the eastern Pyrenees (NE Spain) and their influence on breeding success. A total of 40% (n = 70) of Bearded Vulture nests were usurped (expulsions) by other species, the Griffon Vulture being the species which occupied most nests (81%). Our observations suggest the active selection of nests by usurping species, which for the moment does not seem to influence the breeding success of the Bearded Vulture. The frequency of nest changes, the distance between nests and the productivities obtained do not differ significantly between territories with expulsions (60%) and those which still have all their nests available (40%). Nevertheless, expulsion may have a greater effect on those territories situated at high altitude or with few alternatives for resiting the nest. Since the displacement towards sectors with a greater human presence, or with locations more exposed to unfavourable environmental conditions, may affect breeding success, this may be important for the conservation of the species. The Bearded Vulture Gypaetus barbatus is a threatened cliff-nesting raptor which in the Pyrenees nests in mountainous zones between 700 and 2150 m in altitude. 1,2 Each pair has several nests in its territory, usually between three and five, which it uses each year in rotation; the structure of the nests is maintained in good condition over long periods of time. 3 The nests which are not used during the reproductive cycle may be occupied by other competing species which have similar requirements with regard to the location of the nest, 4 6 as has been documented for different raptors. 7 The Bearded Vulture begins the reconstruction of the nest between three and four months before egg-laying (unpubl. data). 2 This activity entails an important investment in time and energy 7 9 and thus the progressive expulsion of birds from their nests might influence the *Correspondence author. breeding success of the species. The only studies to evaluate the importance and effects of the expropriation of Bearded Vulture nests have been carried out in Navarre (northern Spain). In this area the interspecific overlap and the high density of Griffon Vultures Gyps fulvus 10 make it hard to differentiate between active nest selection by the Griffon Vulture and mere random occupation. 5,6 Nevertheless, the incidence of expulsion of Bearded Vulture nests by Griffon Vultures did not seem to influence the breeding success of the species. 6 This paper provides new data on the increasing occupation of Bearded Vulture nests by other species in the eastern Pyrenees (Catalonia, northeast Spain). The interspecific interactions observed are described; these reinforce the possibility of active selection on the part of the expropriating species. In view of this and the observed increase in expulsions, the effects which these may have on the 1999 British Trust for Ornithology

2 Bearded Vulture competition for nests 225 breeding success of the species and the relationship between the reuse of nests and breeding success are examined. STUDY AREA AND METHODS The study was undertaken in the Catalonian Pyrenees (northeast Spain) in an area of 8750 km 2 which delimits the Bearded Vulture s present range in the region. 11 The average productivity for this breeding area was 0.41 ± sd = 0.14 young/pair (n = 149 breeding attempts) and the average distance to the breeding areas of neighbouring pairs was 12.7 ± 7.4 km (n = 19; see ref. 11). The monitoring of Bearded Vulture nests was carried out exhaustively from 1984 (seven pairs) to 1996 (19 pairs; see ref. 11), and during this period the entire reproductive population of this region was fully monitored. Each year, all known territories were visited monthly. When it was possible to locate the nest exactly, in addition to collecting data on reproduction, we noted from aerial photos and 1:5000 scale maps the characteristics of the nest site, its situation and the distance to the nearest nest of the same pair, with a precision of ±25 m. As the expulsions were detected, the species that had installed themselves in the different nests were noted. The data on interrelations were gathered during the regular surveys of the territories (a minimum of four visits per month from September to July) which have been carried out since Telescopes (20 60 ) were used to undertake the observations from distances of between 400 and 800 m. We considered to what extent the expulsions and their possible influences affected breeding success, establishing comparisons between the territories with usurped nests and those which still had all of their nests. The variation in the frequency of nest changes between both groups was analysed as was the possible influence on the breeding success of pairs of the frequency of changes, the number of available nests and the distance between them. The frequency of reuse and nest change in the following year and its influence on breeding success was analysed with regard to 15 pairs studied during 73 consecutive breeding attempts. In order to compare the average productivity (between territories with and without occupied nests), individual productivity (before and after expropriation of a nest) and the relationship of the productivity to the number of available nests, we have used the data from 142 breeding attempts. In this study only Bearded Vulture pairs which made some attempt at breeding (n = 15) were considered, giving a total of 70 nests. Non-parametric tests 12 were used for the statistical analyses. RESULTS Nest loss and interspecific interactions due to nest occupation From 1984 to 1989, a total of nine Bearded Vulture nests was occupied by other species. From 1990 to 1996, 19 more nests were occupied and, at present, only six territories (40%) remain which do not contain usurped nests. There was no case of a usurped nest being reused by a Bearded Vulture. Of the 28 usurped nests (40%, n = 70), 23 were taken over by Griffon Vultures (81.2%), two by Egyptian Vultures Neophron percnopterus (7.1%), two by Peregrine Falcons Falco peregrinus (7.1%) and one by Raven Corvus corax (3.6%). The latter three species occupied Bearded Vulture nests from 1990 to The largest number of expropriations in a single territory occurred in two pairs, with 11 and nine nests respectively, of which nine and five were occupied by Griffon Vultures. The occupation process was monitored regularly in two territories. In one territory a pair of Griffon Vultures was detected settling in a nest at the beginning of July (one month after the Bearded Vulture s breeding failure). Their presence was continuous (they spent the night on the nest), until the start of the breeding season in January. The second case was observed in a territory occupied by a polyandrous quartet. 13 In mid- January a pair of Griffon Vultures took over the nest which was being built by the Bearded Vultures (the former nest of the Griffon Vultures was 17 km away). At the beginning of March the Bearded Vultures were already rebuilding an alternative nest in which no clutch was laid, whilst the Griffon Vultures bred successfully. On the other hand, two Pyrenean Bearded Vulture pairs occupied two Golden Eagle Aquila chrysaetos and two Raven nests. In three of these cases, the expropriation took place

3 226 A. Margalida and D. García during the early breeding years of recently formed Bearded Vulture pairs, coinciding with their settling in the new sector, or else during the second breeding attempt. In one of these cases there were interspecific confrontations, caused by a Bearded Vulture occupying a Golden Eagle s nest. During the Bearded Vulture s incubation in January, the Golden Eagles carried out continuous aggressive, intimidatory flights 14 around the nest, which on several occasions led the Bearded Vultures to abandon the incubatory position. The Golden Eagles perched just a few metres from the nest, attacking the adult when it approached, thus preventing the changeover taking place. In the end the Golden Eagles settled in another nest on the opposite side of the mountain, and no further conflicts were observed. Nest use and influence on breeding success Pairs with a usurped nest have in their territories a greater number of nest structures at their disposal than those pairs without occupied nests (with usurped nests: x = 6 ± sd = 2.6 nests; without usurped nests: x = 2.7 ± sd = 0.7 nests; Mann Whitney test, U = 5, P = 0.02), whilst no relationship exists between the number of nests and the productivity (r s = 0.34, df = 14, ns). The mean distance between nests of the same pair did not differ between groups (with usurped nests: x = 991 ± sd = 2005 m; without usurped nests: x = 1605 ± sd = 3629 m; Mann Whitney test, U = 236, ns). In those territories with an expropriated nest, 91.8% (n = 49) changed nest during the following breeding cycle while in the territories without usurped nests, 83.3% (n = 24) changed. The difference in the frequency of nest change shown by each group was not significant (χ 2 = 0.481, df = 1, ns). Of the eight cases of reuse of the same nest during two consecutive breeding cycles, only in one (1.4%, n = 73) did it take place following successful breeding the previous year. The frequency of nest change did not influence the breeding success or failure (territories with usurped nests: χ 2 = 0.319, df = 1, ns; territories without usurped nests: χ 2 = 2.148, df = 1, P = 0.143; Table 1), nor are there differences between the mean productivity obtained in territories with and without usurped nests (Mann Whitney test, U = 19.5, ns), although at an individual level, two territories showed significant differences (Table 2). DISCUSSION The annual rotation of nests shown by the Bearded Vulture probably has the function of avoiding the infections which might be caused by the accumulation of ectoparasites. 7,9,10,15 This hypothesis is supported by the fact that, in general, the reuse of the same nest structure during two consecutive years is preceded by failure during incubation (an absence of prey items in the nest and hence an absence of ectoparasites) but not during rearing (a single case in a larger cave). In the Pyrenees, the expropriation of the alternative nests as a consequence of their temporary abandonment would be facilitated by the considerable distance between nests of the same pair (an average of 1605 m in territories without expropriation), which is considerably further than estimated in South Africa (an average of 230 m). 3 Active selection of alien nests can be advantageous for the usurping species, 5,6 and moreover, the presence of old nest structures could have an influence on the usurping Table 1. Breeding success and failure in Bearded Vulture territories with and without usurped nests, in relation to change or reuse of the nest. Without usurped nests With usurped nests Successful breeding Breeding failure Successful breeding Breeding failure Nest change Nest reuse Total

4 Bearded Vulture competition for nests 227 Table 2. Number of nests, productivity and nest-change frequency in territories with and without occupied nests for the Bearded Vulture pairs studied. Productivity Nest change Pair Number of nests x n % n Without usurped nests A B C D E F With usurped nests G 7 1 a /0.4 b 3 a /10 b H /0.75 6/ I /0.4 4/ J /1 11/ K 6 1/1 3/ L* /0 11/ M 4 0/1 3/ N 4 0/0 10/ O* 5 1/0 11/ For productivity: x = average, n = sample size; a before expropriation of a nest; b following expropriation. *Territories with significant differences (P 0.05). The Fisher test was applied. species becoming established. 7 Although it is difficult to differentiate between active selection and random choice with regard to occupation of nests, 5 the observations suggest the possibility that there is an active selection on the part of the expropriating species: the interspecific interactions observed, the numerical increase of the usurping species and the fact that their densities are not high, as well as the observed opportunism of usurping species, leads one to the conclusion that active nest selection does exist. The Griffon Vulture is the main usurping species, probably because in the study area it has a distribution and nesting site requirements similar to those of the Bearded Vulture (pers. obs.). In the eastern Pyrenean zone, it was virtually the only usurping species and the expropriation process seemed to be facilitated by the large body size and the early breeding of this species. 5 On the other hand, the increase in nest expropriation by Griffon Vultures parallels the demographic rise in this species, 6,11,17 a fact which agrees with the observations made in the study area, where the annual rate of increase in the last ten years was 14% (unpubl. data). Faced with the expropriation of its alternative nests, the Bearded Vulture might adopt the strategy of reusing more regularly the nests which are still available, a behaviour observed in another territorial species, the Golden Eagle. 18 Nevertheless, the results show that the species seems to construct new nest structures, moving to alternative areas 11 not very far from the original nesting area. For this reason, the pairs which have usurped nests have significantly more nests with a shorter distance between them. This would also indicate that in the neighbourhood of the original nest site the species has at its disposal sufficient alternative sites nearby. On the other hand, the greater distances observed between nests in territories without expropriation occurs as a consequence of the recent formation of some of the pairs studied, which make continuous changes in nesting territory before their final installation in a specific cliff (pers. obs.). The tendency towards the progressive expropriation of the nests might have consequences for the breeding success of the species in the long term. 6 Although the results show that significant differences in productivity do not

5 228 A. Margalida and D. García exist between groups, the individual analyses reflect the existence of differences in two of them. These results must be interpreted with reservation given the limitations of the sample and the possible influence of other factors not related to the expropriation itself, 19 and given that there is a general tendency towards a reduction in productivity in the population studied, 11 as has been confirmed in other populations of the species. 16 Nevertheless, some breeding failures of the Bearded Vulture in the Pyrenees have been attributed to interactions with Griffon Vultures. 11,17 If any relationship is to be observed between the increase in expropriations of Bearded Vulture nests and breeding success, it will be most evident in those territories with fewer available rock faces and suitable nesting sites, 3 as has been shown in the Golden Eagle. 20 The lack of adequate nesting sites would cause the move to alternative areas which may be exposed to greater human pressure (the latter being the cause of, and influencing the majority of, breeding failures of Bearded Vulture s in the Pyrenees 2,19 ); this is the main problem derived from the interspecific conflict for nesting sites. The problem would be most pronounced in those territories with nests located at high altitude and exposed to rigorous climatic conditions in winter. The absence of safeguard locations for nesting may represent important disadvantages during breeding, given that the microclimate of the nest may be fundamental during incubation 21 and for the health of the young. 9,22 The tendency towards an increase in expulsions is evident and these may have implications for the conservation of the species in the near future. ACKNOWLEDGEMENTS We thank J. Bertran, J. Canut, A. Carulla, J. Feixa, R. Heredia and X. Parellada for their valuable help in the field and D.C. Houston and B. Etheridge for comments on the manuscript. We also thank J.A. Donázar and O.J. Arribas for helpful suggestions on a previous draft of the manuscript. S. Cahill, S. Hardie and J. Orta translated the text into English. This study was supported by DARP of the Generalitat de Catalunya, Minuartia Estudis Ambientals, S.L. and a Life Project (94/E/ A221/01126/ASJ) of the European Union. REFERENCES 1. Hiraldo, F., Delibes, M. & Calderón, J. (1979) El Quebrantahuesos Gypaetus barbatus (L.). Monografía 22, ICONA, Madrid. 2. Heredia, R. (1991) Biología de la reproducción. In El Quebrantahuesos (Gypaetus barbatus) en los Pirineos (eds R. Heredia & B. Heredia), pp ICONA, Colección Técnica, Madrid. 3. Brown, C.J., Brown, S.E. & Guy, J.J. (1988) Some physical parameters of Bearded Vulture Gypaetus barbatus nest sites in southern Africa. In Proceedings of the Sixth Pan-African Ornithological Congress (ed. G.C. Backhurst), pp Nairobi, Kenya. 4. Elosegi, I. (1989) Vautour fauve (Gyps fulvus), Gypaète barbu (Gypaetus barbatus), Percnoptère d Egypte (Neophron percnopterus): Synthèse bibliographique et recherches. Acta Biol. Mont. 3. Serie documents de travail. 5. Fernández, C. & Donázar, J.A. (1991) Griffon Vultures Gyps fulvus occupying eyries of other cliff-nesting raptors. Bird Study, 38, Donázar, J.A., Bustamante, J. & Hiraldo, F. (1993) Evaluación del impacto del crecimiento de la población de Buitre leonado (Gyps fulvus) sobre el Quebrantahuesos (Gypaetus barbatus) en Navarra. Estación Biológica de Doñana (CSIC). Government of Navarra. Unpublished report. 7. Newton, I. (1979) Population Ecology of Raptors. T & A.D. Poyser, Calton. 8. Collias, N.E. & Collias, E.C. (1984) Nest Building and Bird Behavior. Princeton University Press, New Jersey. 9. Brown, C.J. (1988) A study of the Bearded Vulture Gypaetus barbatus in southern Africa. PhD Thesis, University of Natal, Pietermaritzburg. 10. Donázar, J.A. & Fernández, C. (1990) Population trends of the Griffon Vulture Gyps fulvus in northern Spain between 1969 and 1989 in relation to conservation measures. Biol. Conserv., 53, García, D., Margalida, A., Parellada, X. & Canut, J. (1996) Evolución y parámetros reproductores del Quebrantahuesos (Gypaetus barbatus) en Catalunya (NE España). Alauda, 64, Sokal, R.R. & Rohlf, F.J. (1981) Biometry, 2nd edn. W.H. Freeman & Co., San Francisco. 13. Margalida, A., García, D. & Bertran, J. (1997) A possible case of a polyandrous quartet in the Bearded Vulture (Gypaetus barbatus). Ardeola, 44, Bergo, G. (1987) Territorial behaviour of Golden Eagles in western Norway. Br. Birds, 80, Wimberger, P.H. (1984) The use of green plant material in bird nests to avoid ectoparasites. Auk,

6 Bearded Vulture competition for nests , Donázar, J.A. (1993) Los buitres ibéricos: biología y conservación. J.M. Reyero, Madrid. 17. Razin, M. (in press) Interactions entre Vautour Fauve Gyps fulvus et Gypaète barbu Gypaetus barbatus dans les Pyrénées-Atlantiques. II Congreso Internacional sobre Aves Carroñeras, Cuenca. 18. Fernández, C. & Azkona, P. (1993) Influencia del éxito reproductor en la reutilización de los nidos por el Águila Real (Aquila chrysætos L.). Ardeola, 40, Donázar, J.A., Hiraldo, F. & Bustamante, J. (1993) Factors influencing nest site selection, breeding density and breeding success in the Bearded Vulture (Gypaetus barbatus). J. Appl. Ecol., 30, Boeker, E.L. & Ray, T.D. (1971) Golden eagle population studies in the Southwest. Condor, 73, Margalida, A., Bertran, J., García, D. & Heredia, R. (1997) Observaciones sobre el periodo de incubación del Quebrantahuesos (Gypaetus barbatus) en los Pirineos. Ecología, 11, Gill, F.B. (1990) Ornithology. W.H. Freeman and Company, New York. (MS received 13 March 1998; revised MS accepted 6 August 1998)

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