Resurgence of Egyptian in western ^ and relationship with Griffon Vultures Jacques Carlon This paper is dedicated to the memory of Bernard Braillon, who died on 26th December 1986, in recognition of his pioneering work on this species on the northern slopes of the Pyrenees. ABSTRACT A long-term study of Egyptian Vultures Neophron percnopterus in southwest showed a marked population recovery from 1985, the species having declined greatly during the previous decade and more. This resurgence was due in part to improved weather during critical periods of the breeding cycle, and also reflected improvements in the fortunes of the Spanish population. The species' relationship with the Griffon fulvus was also studied, and its response to nest-site usurpation by the larger vulture showed interesting adaptations.

Our observations on Egyptian Vultures Neophron percnopterus were carried out in the province of Beam, in the eastern half of the departement of Pyrenees- Atlantiques, situated on the northern slope of the Pyrenees in southwest France (see Carlon 1996b). The study area comprised the valleys of the rivers Baretous, Aspe, Ossau and Ouzom, all in the southern half of the province and covering an area of approximately 860 km2.

[Brit. 91: 409-416, October 1998] © British Birds Ltd 1998 409 410 Carlon: Egyptian and Griffon Vultures in western Pyrenees

During the 12 years 1984-95, a total of 2,366 hours of field observations was made by the author, with an additional 330 hours by colleagues. Altogether, 205 pairs of Egyptian Vultures were monitored at breeding sites over the 12 years, plus ten pairs in 1982 and 1983: making 215 pairs in all. Various findings of this study have already been published in French (Carlon 1989, 1992, 1993, 1996a). The present paper presents a summary in English of the remarkable resurgence of the species in Beam, together with interesting aspects of its relationship with the Gyps fulvus.

Decline and regrowth of the population The population of the in southern France and the Pyrenees underwent a strong decline in the years preceding the 1980s, but has since recovered to a healthier level. This was apparent not only in our study area, but also in the neighbouring regions of Provence, in southeast France (Bergier 1985), and Aragon, on the southern slope of the Pyrenees in (Kostrzewa et al. 1986). During the main period of our study, regular checking of sites that had been abandoned for more than ten years, together with a systematic search of all potential breeding sites, enabled us to record the reoccupation of six sites, the discovery of ten new ones, and successful breeding at a site where a regular pair had taken a seven-year 'sabbatical' during 1977-83. Table 1 summarises the annual development of the Beam population from 1984 to 1995. The years 1982 and 1983, when our fieldwork was less intensive, are also included, to highlight the low point of this population (six pairs in 1984) and the subsequent spectacular recovery and growth (to 21 pairs in 1990). The population stabilised at 20-21 pairs during 1990-95. This apparent stagnation in the 1990s could, we believe, be linked with two factors. First, usurpation of eyries and competition for habitat by the Griffon Vulture represent an appreciable limiting factor (see below); and, secondly, observer effort and efficiency tend, through the process of habituation, to decrease over the course of the years, particularly with regard to searching for potential new breeding sites. It is possible, if not probable, that two or even three sites may have escaped detection in 1994 and 1995, bearing in mind the large extent of suitable breeding habitat available in the study area.

Site fidelity A striking feature of this study was the great fidelity of pairs to breeding sites, so long as they were not subject to heavy disturbance or interspecific parasitism. Apart from instances of nest-site usurpation by Griffon Vultures (see below), we recorded only two definite cases of site desertion out of 205 pairs monitored. The first occurred at the highest site in the study area, at 1,450 m, within the montane and subalpine zone; this was a result of unusual weather conditions, with heavy snowfalls in two years out of three in April, the month when the pair was establishing territory. The second was in Vallee d'Aspe, very probably caused by disturbance from increasingly heavy traffic on the roadway; the pair involved re-established itself at a site 300 m higher up. British Birds, vol. 91, no. 10, October 1998 411

Factors responsible for the resurgence of the population Climatic influences The influence of climatic conditions on population fluctuations and reproduction was discussed by Carlon (1992). Two interesting facts have emerged from this study: the low percentage of breeding failures, and the development of earlier and more successful fledging. In years with 'normal' weather conditions, breeding failures appear to be relatively rare. In Provence, Bergier & Cheylan (1980) recorded only four failures (6.8%) out of 59 breeding attempts. In Beam, of 66 breeding attempts over the five years 1985-88 & 1990, only five failed (7.5%, a figure roughly equivalent to theirs), even though the Mediterranean climate is more favourable to the species. On the other hand, the Provencale region is subject to much greater disturbance, owing to the greater accessibility of nesting sites. Breeding success across the entire northern slope of the Pyrenees in normal years during 1959-85 was shown to be 77% (Braillon 1986). In Beam, during 1985-90, we recorded only ten breeding failures (plus two suspected failures) out of 91 pairs, giving a success rate of 88%. This improvement appears to be due to better weather conditions during the early stages of development of the young. This was borne out in 1991, when six pairs failed out of a total of 21, all but one (which was probably due to human disturbance) at or soon after hatching. In that year, precipitation was 15.1% less than in the three preceding years, but temperature and total sunshine hours were both 14-15% lower, and these last two parameters would appear to be of the greatest importance during the critical period of hatching and early development. Note that cold, wet springs, such as occurred in 1988, do not necessarily lead to failure if hatching takes place after such weather has ceased. During the study period, a distinct advancement in fledging date was noted. Up to 1987, the mean fledging date in Beam was about 20th August; during the two drought years which followed (1989, 1990), it was 12th August, where it remained. Owing to much earlier fledging at some sites in 1994—2nd and 5th August, 25th and 30th July, and an unprecedented 11th July in Vallee d'Aspe (M. & R. Cruse in litt.)—the mean date for fledging has been brought forward to 25th July. We also recorded a small increase in productivity, with a higher number of juveniles reared per pair during 1988-95 (mean 1.26/pair) than during 1959- 85 (1.17/pair) (table 2). Given that 1989 and 1990 were drought years, we demonstrated (Carlon 1992) that higher temperatures, increased total sunshine hours and a drop in total precipitation were determining factors in this increase in fledging rate. As recording fledging success requires an enormous amount of time in the field, it was not possible to determine this throughout the entire 12-year period. Nevertheless, we were able to calculate it for six years (1988-90, 1991- 92 and 1995; table 2). These involved a significant number of breeding attempts (88), and a representative sample of climatic conditions which included two years (1989-90) of dry, hot weather, followed by two years (1991-92) with particularly cold and wet weather throughout the most critical 412 Carlon: Egyptian and Griffon Vultures in western Pyrenees stages (May-June: end of incubation, hatching and first days of life of the chicks), and then by one year of drought (1995). On the basis of these criteria, and a rigorous follow-up during the three periods, we consider our figure of 1.26 young/pair a realistic one, corroborated by and comparable with those published for Provence (1.38-1.40: Bergier & Cheylan 1980; Bergier 1985; Bayle 1990) and for the Spanish slope of the Pyrenees in Catalonia and Navarra (1.29-1.75: Donazar & Ceballos-Ruiz 1988). Note that this increase in fledging rate is due almost solely to the higher percentage of broods of two young in years when weather conditions were very favourable for this sun-loving species. Especially when climatic conditions have been propitious, fieldwork needs to be concentrated during and subsequent to the period when the young leave the nest (about the third week in July to late August); this is particularly true when the brood contains two young.

Other possible influences As weE as these climatic factors that have played a major role on the two sides of the Pyrenean massif, particularly in Beam, there are others, not insignificant, that need to be examined (see Carlon 1989). The resurgence of the population may best be appreciated by dividing the period into two parts. In 1982-85, the combined number of occupied sites was 33 (possibly 35), or an annual mean of eight or nine; in 1986-88, this total rose to 46, or a mean of 15 or 16 per year (table 1). During 1979-83, Bergier (1985) recorded, in Provence, the recolonisation of a territory abandoned since 1965, the occupation of a new site, and the observation of several immatures during the breeding season, while in Aragon, Spain, in 1984-85, a population increase was confirmed for the first time (Kostrzewa et al. 1986).

Table 1. Sites occupied by Egyptian Vultures Neophron percnopterus in Beam, southwest France, from 1982 to 199S. Totals include 6 reoccupied sites and 10 newly discovered sites. 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995

Total occupied sites 9 7 6 11 13 15 18 19 21 21 20 20 21 20 Sites vacant since 1968 and reoccupied by 1987 ^-6-*- New sites -« m hi Several possible factors may explain these changes. In the western part of the west Pyrenees, the Griffon Vulture population underwent a spectacular growth: from 61 pairs in 1976, to 78 in 1979, and 168 pairs with 122-130 young fledged in 1986 G--J- Lequemeneur, verbally 1986). The numerous local rubbish dumps (for household waste) were amalgamated during the late 1970s and the 1980s into vast refuse tips, most of which were sited at the entrance to large valleys; Egyptian Vultures are frequently observed at these sites. Feeding stations, initially intended for Griffon Vultures, regularly British Birds, vol. 91, no. 10, October 1998 413

Table 2. Mean fledging rate of Egyptian Vultures Neophron percnopterus in Beam, southwest France, 1959-95. Figures refer to number of young per successful pair. Date for 1959-85 are from Braillon (1986). Average 195M5 1988-90 1991-92 1995 1988-95

No. juvs 1.17 1.34 1.08 1.35 1.26 Sample 27 41 20 88 attracted the smaller species, with increasing numbers of adults in June (i.e. at the start of brood-feeding). Pastoralism, a not insignificant source of food, had been maintained at apparently the same level during the period. In addition, Egyptian Vultures regularly foraged along the banks of upland watercourses, which are subject to increasing eutrophication. What was probably a more decisive influence was the fluctuations of the very large Iberian population of Egyptian Vultures. This was estimated at 2,000 pairs in the 1970s (Bijleveld 1974) and was showing worrying signs of decline in most of the provinces (Cramp & Simmons 1980), this being confirmed by a 1985 census which produced a figure of 950-1,100 pairs (Congres international sur les Rapaces mediterraneens, Evora, , 1986). This historical picture enables a better appreciation of a factor which is relevant to the Beam study: namely, the increase, starting in 1984, of the Aragon population, recorded by Kostrzewa et al. (1986), who have also pointed out (in litt.) that poisoned baits aimed at Red Foxes Vulpes vulpes and Carrion Crows Corvus corone were outlawed throughout Spain from 1984. It is also worth bearing in mind the abundance of suitable breeding habitat available in the Pyrenean region. This fourth positive factor (after those of relative food abundance, presence of the large Spanish population on the southern slopes, and increased rate of expansion of the Griffon Vulture population in recent years) throws into particular relief the situation of the Egyptian Vulture in the western Pyrenees, and more particularly in Beam. While the position of the Egyptian Vulture in southwest France remains precarious and of concern, it is nevertheless more favourable than those of the Golden Aquila chrysaetos and the Lammergeier Gypaetus barbatus. It cannot, however, rival the recent dynamism of the smaller predators such as the Red Kite Milvus milvus and especially the Black Kite M. migrans, both clearly increasing, or even more so that of the Common Raven Corvus corax, which has undergone a spectacular expansion during the last decade in the departement of Pyrenees-Atlantiques.

Relationships between Egyptian and Griffon Vultures On the outskirts of Griffon Vulture colonies, or sometimes a few kilometres away, it is not unusual to see one or two Egyptian Vultures joining in with the comings and goings, or taking advantage of the larger species' exploratory flights and, being less suspicious, descending before the Griffons when a carcase has been spotted. This behaviour, however, then brings the Griffon Vultures down to the feast, and during this period the Egyptian Vulture, given 414 Carlon: Egyptian and Griffon Vultures in western Pyrenees its subordinate status in the interspecific hierarchy of vultures, demonstrates patience and prudence. Cohabitation with the large vultures is noteworthy and can be observed particularly in those areas where there are many large Griffon colonies, as in the Vallee d'Aspe. The attraction exerted by the Griffon Vulture may be demonstrated by the fact that, in Les Causses, following that species' successful reintroduction in 1982, the Egyptian Vulture appeared almost immediately, after having ceased to nest in that region in 1955; others followed, and a pair established itself from 1984 (C. Bagnolini, J. Bonnet & J.-L. Pinna in litt). The height of Egyptian Vulture eyries in cliff sites seems to be a direct consequence of the marked dominance of the Griffon Vulture. In all but one of the large Griffon colonies in Beam, the nests of Egyptian Vultures occupy the base of these sites, whereas in the years 1965-70, when Griffon numbers were about 80% lower than in 1985, they were higher up the cliffs. This change can probably be attributed to the constant activity of Griffon Vultures at their colonies and the resulting numerous interactions creating permanent disturbance in the close surroundings of the eyries (see below). The immediate departure of an Egyptian Vulture from a tiny cramped ledge as soon as a Griffon Vulture lands is further evidence of the disturbance and the dominance exerted by the latter. On the other hand, adult Egyptian Vultures move around at all levels in these colonies, and make frequent inspections of Griffon nest sites; similar visits by Egyptian Vultures to nest sites of Lammergeiers have been observed (Terrasse & Terrasse 1967). From numerous observations gathered in recent years, I suggest that the term 'mutualism', or commensalism strongly tinged with mutualism, best describes the relationship between the two species. The Egyptian Vulture, as it precedes or often joins the Griffons in searching for carrion, and as it is bolder or more daring at such times, can play a role of 'reconnaissance' and can also 'give the all-clear': in other words, it tends to attract the larger vultures to food more quickly because it is often the first to descend, and, because it is more cautious when on the ground, it thereby indicates that it is safe to feed there. On the other hand, the Griffon parasitises the smaller species in several ways.

Parasitisation by Griffon Vultures In 1986, in the Griffon Vulture colony in Vallee d'Ossau which had experienced an unprecedented growth from 1979 to 1993 (Carlon 1993), an Egyptian Vulture eyrie was taken over by a pair of Griffons. A further nine pairs of Egyptian Vultures in the study area have had their breeding attempts disrupted by loss of their eyries, or have been forced to move to different sites. I have witnessed three instances of food parasitism by Griffon Vultures at two Egyptian Vulture sites. One of these caused the two young to leave the nest prematurely, one young disappearing for good. In 1988, at a large Griffon colony, a breeding attempt failed at the chick stage (approximate age three weeks) following the frequent presence of a Griffon Vulture at the eyrie; although the exact cause of death could not be determined, the Griffon had been seen feeding there on several occasions. Another eyrie, while being British Birds, vol. 91, no. 10, October 1998 415

prepared for nesting, was abandoned following the frequent presence of a Griffon on the nest ledge. These three examples indicate the disturbances and losses suffered by the Egyptian Vulture during the breeding period at sites where it coexists with large colonies of Griffon Vultures. More recently, in spring 1996, in Vallee d'Aspe, a particularly prolific pair of Egyptian Vultures which produced two young every other year, and had occupied a large, very accessible cave for eight years, was forced out when a pair of Griffon Vultures set up breeding territory at the site in January. It is worth noting that, in Spain, Bonelli's Eagle Hieraaetus fasciatus and Lammergeier suffer the same fate, with Griffon Vultures taking over 40% of their breeding sites (Kostrzewa & Galushin 1992). In Beam, the Booted Eagle H. pennatus is victim of a similar exclusion in the Gave de Pau plain by the Black Kite, still expanding in this region and whose pre-breeding arrival is one month earlier than the eagle's (Carlon 1995, 1996b).

Modification of breeding behaviour A direct consequence of this parasitisation of eyries by Griffon Vultures was the emergence of two new adaptations by the Egyptian Vulture. The first was the selection of a breeding place in cliff sites of smaller size, on sheltered or camouflaged narrow ledges or equivalent caves, but where Griffon Vultures were not present. The second was to breed, when the possibility still remained, at the heart of the Griffon colony, this time not on narrow ledges or even in big caves, but in small cavities without reception ledges, thus preventing access by Griffons; or else to select sites at the base of these same cliffs, little visited by and even inaccessible to the Griffons.

Acknowledgments A number of observers have participated in this study, on a regular or occasional basis and for varying periods, and their assistance is most gratefully acknowledged: Jean-Louis Bonneville, Laurent Brun, Josephine Carlon, Maurita & Richard Cruse, Pascal & Jean-Luc Dunoguiez, the late Robert Etchegorry, Jean-Louis Grange, Robert Houert, Georges Lopez, Henri Navarre, Nicolas Pinczon-du-Sel, Serge Raoult, Jean Tischmacher, and Catherine & Olivier Trioullier. I also thank David A. Christie for translating and adapting my earlier writings on this subject.

References BAYLE, P. 1990. Bilan couple par couple de la reproduction du Vautour percnoptere en Provence en 1988 et 1989. Centre d'Etude sur les ecosystemes de Provence. BERGIER, P. 1985. La reproduction du Vautour percnoptere en Provence de 1979 a 1983. Bulletin no. 2 du Groupe de Travail Mondial sur les Rapaces. [WWGBP] —— & CHEYLAN, G. 1980. Status, succes de reproduction et alimentation du Vautour percnoptere en France mediterraneenne. Alauda 48: 75-97. BIJLEVELD, M. 1974. Birds of Prey in . London. BRAILLON, B. 1986. Nidification du Vautour percnoptere sur le versant Nord des Pyrenees. Un suivi de l'ensemble commence il y a 27 ans. In: Oiseaux des Pyrenees. Acta Biologica Montana 7. Pau. CARLON, J. 1989. Contribution a l'etude du Vautour percnoptere en periode de reproduction. Nos Oiseaux 40: 87-100. —— 1992, Contribution a 1'eco-ethologie du Vautour percnoptere Neophron percnopterus. 416 Carlon: Egyptian and Griffon Vultures in western Pyrenees

Phenologie de la reproduction en Beam. Marie-Blanque 1. 1993. Contribution a l'eco-ethologie du Vautour percnoptere Neophron percnopterus en Beam. Versant Nord des Pyrenees Occidentals. Marie-Blanque 2. 1995. Special Aigle botte Hieraaetus pennatus. Marie-Blanque 4. 1996a. Synthese duodecimal (1984-1995) de la nidification du Vautour percnoptere Neophron percnopterus, en province de Beam, versant nord des Pyrenees Occidentals. Marie-Blanque 5: 1-11. 1996b. Response of Booted to human disturbance. Brit. Birds 89: 267-274. CRAMP, S., & SIMMONS, K. E. L. (eds.) 1980. The Birds of the Western Palearctk. vol. 2. Oxford. DONAZAR, J. A., & CEBALLOS-RUIZ, O. 1988. Alimentacion y tasas reproductoras del Alimoche Neophron percnopterus en Navarra. Ardeola 35: 3-14. KOSTRZEWA, A., & GALUSHM, V. 1992. Premiere session sur l'etude des populations chez les rapaces. In circular of the GTMR, no. 16-17. Paris. [WWGBP] , FERRER-LERTN, E., & KOSTRZEWA, R. 1986. Abundance, status and vulnerability of raptors and owls in parts of the Spanish Pyrenees. Birds of Prey no. 3. Paris. TERRASSE, J.-F., & TERRASSE, M. 1967. Les Vautours en France. Le Courrier de la Nature, no. 86 (special issue).

Jacques Carlon, 12 rue Rabelais, 64000 Pau, France