CAPTIVE BREEDING OF THE BEARDED VULTURE AND ITS ASSOCIATED PROBLEMS. Alejandro Llopis* & Hans Frey**

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1 CAPTIVE BREEDING OF THE BEARDED VULTURE AND ITS ASSOCIATED PROBLEMS Alejandro Llopis* & Hans Frey** *Centre de Recuperació de Fauna Vallcalent, Partida de Vallcalent, 63; E Lleida (Spain). **Institut für Parasitologie und Zoologie, Veterinär Medizinische Universität Wien, Josef-Baumanngasse 1, A-1210 Viena (Austria). INTRODUCTION The International Bearded Vulture Captive Breeding Programme was created as a result of the 1978 international reunion in Morges, Switzerland, where essential guidelines for the Bearded Vulture Reintroduction Project in the Alps (FZG 832/78; WWF 1567/78) along with its modus operandi, were established. One of these guidelines was to restrict the programme to the use of bearded vultures that were already in zoological parks, or wild birds which had been injured and were not suitable for release. With this in mind, a reproduction centre was created on the outskirts of Vienna (Vienna Breeding Unit, VBU), which is also the coordinating centre for the programme. In 1985, the first European Threatened Species Conservation Programme (EEP) was established, with one of its objectives being to act as a base for future reintroduction programmes and to create a genetic reserve. Currently, 6 breeding centres and 36 zoological parks all over the world collaborate with the programme and there are 137 bearded vultures in captivity. Until 2005, the programme has worked with 70 founders (44 males y 26 females). The majority of these are from Asia (64), 1 is from Crete, 1 from continental Greece and 4 from the Pyrenees (3 from Spain and 1 from France). Of these, 43 (61.43%) have reproduced (37 leaving offspring, 52.86%) and there are still 10 living birds, of which 8 may still leave offspring. Between 1972 and 2005, 445 clutches were laid (not including 3 females because of a lack of data). Of these, 251 hatched and 216 chicks were successfully reared. In total, 767 eggs have been laid, of which 351 have hatched, resulting in 277 chicks. Of these chicks, 137 have been reintroduced in the Alps over the period Between 1978 and 2005, 77 birds have died, the principal causes of death being aspergillosis (19.48%) aspergillosis as a secondary disease (12.98%), poisoning (12.98%), senility (9.09%) or senility accompanied by illness (11.68%) and trauma (9.09%). Thanks to the experience gained over nearly 30 years of captive breeding of bearded vultures, almost all new pairs now mate and those that don t at least play a role in the breeding process (incubating eggs or rearing the chicks of other pairs). However, it is during the pair forming process that most problems are detected, with birds who have suffered some psychological trauma (having spent too much time without social contact or having been handled excessively during their recovery from illness or accident) or those which have not been reared properly, presenting most problems. The Bearded Vulture Breeding Programme has demonstrated that the size of the cage is not as important as other factors such as the equipment provided and its size (perches, drinking troughs, feeding places and nests), the position of the cage (a quiet site exposed to the sun), the preparation of the staff and the running of the centre (including the handling of the birds and the breeding methods employed). All the birds in captivity, according to the recommendations of the EEP (Frey et al., 1995), have developed

2 behavioural patterns like those of wild birds. The only observed difference has been in the frequency of, for example, copulations per reproductive cycle and pair in some captive birds. The majority of the behavioural patterns of this species that have been observed in captivity (cainism, the colouration of the plumage with mud rich in iron oxide, various aspects of reproductive behaviour etc) have later been confirmed in the wild, thus allowing all information (both in situ and ex situ), to be compared and later applied to the conservation of the species. CAPTIVE BREEDING AND ITS ASSOCIATED PROBLEMS. 1. OBJECTIVES OF THE EEP. In general terms, the objectives of any captive breeding programme are the creation of a breeding stock and genetic reserve, the control of the captive population both genetically and demographically and the production of chicks suitable for release or reinforcement of populations and capable of breeding once they have reached sexual maturity. These objectives have been established by the EEP for bearded vultures. To fulfil these objectives it is necessary to guarantee the maximum genetic variability in the captive population. Obviously, it is impossible that a programme be perfect, with 100% survival probability and complete genetic variation maintained forever within the population. From the statistical point of view, 20 unrelated birds represent 95% of the genetic variation of a extracted population. By including 5 birds from the 3 distinct European populations (Greece, Crete and the Pyrenees) the population of the EEP shows a high level of genetic variability which can be demonstrated in mitochondrial and nuclear DNA tests (Gautschi, 2001; Gautschi et al., 2003; Gautschi et al., 2003a; Negro & Torres, 2000). However, the fall in genetic variability in a reproductive population depends not only on the size of the population, but also on the number of generations. For example, in a population of 30 founding individuals, only 50% genetic variation would have been lost over 50 generations (Boer, 1988). For this reason, to preserve genetic variability over generations, the bearded vulture EEP retains 4 individuals of each pair, which represent 95.6% of the parents genetic variability. Other programmes, like that of the California condor (Gymnogyps californianus) retain 5 individuals (96.7%), (Wallace and Toone, 1992). 2. THE CENTRES Centre location. Although, up until the present moment, the location of the centre does not appear to have any influence on reproductive success, it does influence the lifespan of the birds and, indirectly, the productivity of the programme. Bearded vultures require zones that are sunny in the morning and afternoon and areas which are shaded at midday, especially in the summer. Humidity levels affect them a great deal with aspergillosis being, directly or indirectly, the major cause of death in bearded vultures (32.45%; n=77 of the birds which died between 1978 and 2005). Although the VBU is located in a very humid area, aspergillosis mortality has been maintained at low levels thanks to the method of breeding employed (only 4 birds died as a direct result of aspergillosis, although it was present as a secondary disease in another 8). Keeping all stress factors to an absolute minimum is one of the keys to a long lifespan and is a fundamental requisite for breeding (Fentzloff, 1983; Frey et al., 1995; Schlee, 1994). 2

3 Number Altitude above sea level doesn t appear to influence reproductive success either, although it does influence lifespan. To the present day, centres which are located over 1000m above sea level have not registered a single case of aspergillosis (eg: Guadelentin Breeding Centre, CCG, 1300m above sea level). This makes us suspect that the aspergillosis fungus loses pathogenicity above 1000m and explains the high susceptibility of this species to the disease, since in the wild bearded vultures inhabit elevated areas and therefore have not developed a specific defence mechanism against this disease Centre functions. Before the bearded vulture breeding programme began, very few zoos had obtained successful captive breeding results (Sofia Royal Zoological Park, Alpenzoo Innsbrusk and Almaty Zoo). As soon as the founding birds were gradually grouped together (from 1978 onwards) in the Vienna Breeding Unit, the number of breeding pairs increased (see figure 1). This demonstrates that the experience of the staff and their dedication to the centre is extremely important if the project is to be a success. This conclusion has also been reached in other breeding programmes (white-tailed eagle (Haliaeetus albicilla), bald eagle (Haliaeetus leucocephalus), California condor etc). Only in those centres in which staff are present during all hours of daylight do we have detailed information of the behaviour of individual birds, which allows any anomalies or changes in normal behaviour to be quickly detected. The accidental deaths of bearded vultures in various centres is well recognised (6 from lead poisoning, 2 from poisoning from rat bait, 2 from carbamate poisoning and 7 from trauma). However, similar accidental deaths have never occurred in centres with staff specialised in working with the species, where even disabled birds or individuals that have spent many years isolated from other bearded vultures and have lost their ability to socialise, have bred successfully. What s more, the average age of death varies greatly between specialised and non-specialised centres (28.8 and 14.1 years respectively). 28 1,14 1, ,0 0, ,67 0,63 0,6 0,64 0,55 0,8 0,69 0,74 0,77 0,65 0,71 0,78 0,8 0,6 12 0,5 0,53 0,5 0,47 0,52 0,55 8 0,38 0,45 0,43 0,43 0,41 0,36 0,48 0,4 4 0, , Year breeding success no. of fledglings no. of breeding pairs Figure 1: Number of fledglings, number of breeding pairs and annual breeding success (no. of fledglings / no. of breeding pairs) over the period

4 With regard to these results and because of the danger and complexity involved in pair formation, it was necessary to establish a difference between centres which are dedicated exclusively to breeding (Breeding Centres) and centres which are dedicated to breeding and pair formation (Breeding and Pairing Centres). The function of the former centres is to house already established pairs and to breed chicks. On the other hand, the specialised centres are responsible for establishing pairs, adopting chicks, housing problematic birds and for creating a genetic reserve by receiving examples of all the genetic lineages which make up the EEP. In the latter centres it is important to have specialised staff who are dedicated exclusively to the centre and who are present during all hours of daylight, especially during the breeding season and at the time of pair formation. However, in the breeding centres which receive already established pairs and juvenile birds, it is only necessary to monitor the birds and the reproductive cycle. 3. THE CAGES Dimensions. As previously mentioned, the size of the cages does not have a direct influence on reproductive success, but it does have an indirect effect which depends on the kind of centre. Birds of prey, which are housed in centres that are open to the public need bigger cages to be able to maintain a certain distance from the visitors and consequently maintain the necessary freedom from anxiety which they require to be able to breed. On the other hand, in centres which are closed to the public, the size of the cage can be considerably reduced. For these reasons we can find examples of very small cages like those of the harpy eagle (Harpia harpjya) in Los Angeles Zoo, which measures 3.3 x 5.5m with a height of m (Todd & Meachan, 1974) or enormous cages measuring 27.4 x 13.7m with a height of 15.2m used in the bald eagle breeding programme in the Washington National Zoological Park (Johnson & Gayden, 1975). However, this latter species has also bred successfully in cages measuring only 7.2 x 7.2 x 4.5m in the Fort Worth Zoo (Hancock, 1973). The white-tailed eagle breeding programme at the Bird sof Prey Centre in Burg Guttenberg has used cages measuring from 7 x 8m to 9 x 13m with a height of 5-6m (Fentzloff, 1983) whereas, in Tama Zoo, Tokyo, cages measured up to 25 x 15 x 11.4m (Asakura et al., 1978). Fentzloff (1983) mentions the successful breeding of white-tailed eagles in much smaller cages (4 x 5 x 3.2m). It is also well known that vultures will breed in very small aviaries. A Ruppell s griffon vulture (Gyps rueppellii) has bred successfully in a cage measuring 9.1 x 4.8 x 4.8m, a Himalayan griffon (Gyps himalayensis) in another measuring 7.6 x 8.7 x 5.8m and the king vulture (Sacoramphus papa) in one of only 4.6 x 2.6 x 2.8m in the Menagerie de Paris (Schlee, 1988, 1989, 1994). This has also been observed in the bearded vulture. In 1916 in the Sofia Royal Zoological Park, where the first captive breeding of this species took place, the cage measured only 6 x 7 x 8m and it didn t even have a nest (the egg was laid on the floor and incubated successfully). The same pair mated annually until 1928, raising 9 chicks (Schumann, 1928, 1929). The bearded vulture has also bred in an exhibition cage in Goldau (Switzerland) which measured 600m 2 with a height of 10m. On the other hand, the pair, which bred successfully in Innsbruck, lived in a cage measuring 12 x 6 x 6m. Experience with bearded vultures has shown that a relationship exists between breeding success and the security which pairs are offered. The cages should be long and with sufficient height to provide the distance they need to escape. This distance reduces stress, a factor which has a negative influence on productivity and lifespan. Hancock 4

5 (1973) and Carpenter et al. (1987), working with captive breeding of bald eagles, also mention that the only parameter of the cage dimensions which influences breeding is the height. The same occurs with the black vulture (Aegypius monachus) (Tewes et al., 1998). The ethologist, Dr. Konrad Lorenz, demonstrated in several of his documentaries with geese, their inability to recognise distances; they are always guided by size. Consequently, when the imprinted chicks walked with him they always maintained the same distance. As soon as their adoptive father bent down, the chicks ran towards him, closing the distance. In this way he showed that, by bending down and reducing his size, the chick thought that he was further away and reacted by moving towards him without realising that the distance that separated them from their father hadn t changed. Consequently, having birds housed in cages with high perches means that, because of the angle of vision from the perch, the staff on the ground appear to the bird to be smaller than they actually are and for the birds this signifies that they are further away offering them a prudent escape distance. For this reason, it is important to determine the minimum height that birds require to feel they have an adequate escape distance inside their cage. Thus, in the Guadelentin Breeding Centre, Iberian imperial eagles (Aquila adalberti) which were housed in bearded vulture cages adapted for eagles and with a height of 4m, would often repeatedly fly into the wire mesh of the cage and injure themselves when staff entered the cage. This behaviour was never observed once they were housed in 5m high cages. Other authors have reached the same conclusion whilst working with other species of eagles (Carpenter et al., 1987; Jonson & Gayden 1975; Maestrelli & Wiemeyer, 1975; Wiemeyer, 1981). Nevertheless, this height is limited by the necessity of quickly accessing the nest to handle its contests when required. We now know that with correct handling, the appropriate dimensions for a cage housing a breeding pair of bearded vultures can be reduced to 6 x 12 x 4m and to 6 x 16 x 4m for a communal cage housing 6-8 juveniles Materials. The use of hard materials for the framework and walls of the cage has caused injury to many birds, some of which have even died after hitting the wire mesh or frame. In the bearded vulture, this occurred when a fledgling attacked its mother and she died after hitting the cage. In centres where soft materials are used (wood and welded elastic wire mesh), no birds have ever died in this way. Unlike all other vultures and most eagles, the bearded vulture plays with anything it finds in its cage, chasing butterflies and even nibbling wood. They also have the peculiar behaviour of swallowing anything colourful or shiny or anything that resembles their habitual food (screws, tool handles, brushes and pieces of hosepipe). Three birds have died after swallowing foreign objects left behind in their cages. However, they are also capable of regurgitating small objects-even a dummy egg of the size used with this species. It is important that wood should not be treated with any toxic substances since there is a risk that a bird might swallow splinters of wood while nibbling and poison itself. This playful behaviour has led to one bird escaping from a cage with interwined wire mesh. The bird was able to open a sufficiently large gap in the mesh. For this reason, it is important that the mesh should be welded and held so that it doesn t strain against the framework. This cushions the impact should a bird fly against it. The floor should preferably be made of any natural material and if possible should be covered with grass. Artificial floors require at least an annual disinfection whereas natural floors do not (Carpenter et al., 1987). Furthermore, food does not get 5

6 dirty and birds do not injure themselves when they land, unlike the one housed in a cage with a gravel floor which cut its claw (Llopis, personal observation) Cage Infrastructure. When breeding falcons it is advisable to keep the centre of the cage clear of obstacles to prevent accidents (Cade et al., 1977). In bearded vultures there are 2 documented cases of collision with obstacles, in both cases the obstacle being a tree. One bird was slightly injured when a branch went through its patagium and another bird died. For this reason, it is also advisable to keep the centre of bearded vulture cages clear of obstacles Perches As aforementioned, birds (because of the peculiar fact that they are guided by size and not by distance) feel safer when they have raised perches. However, the perch should never be higher than the nest. Any bird which is observed from above the nest, even by other birds of the same species, feels threatened. When the nest is placed under the perches, incubation can be negatively affected. For the same reason, it is important that the path giving access to the cage should always be under the level of the nest. To respect individual distance, it also helps if perches are installed around the whole cage. This distance defined as the agreed distance at which animals are attracted to members of their own species but repelled by them when this distance is shorter (Wilson, 1980; Drickamer et al., 2002), is vitally important during pairing. In cages with just one nest and one perch, pairing is complicated by the fact that the individual distance must be broken suddenly, often resulting in attacks. When perches are installed around the cage, the birds can move towards each other gradually and little by little break the individual distance. What s more, in non-established pairs, the subordinate bird can escape from attacks by the other and at the same time can stay on a perch where it feels safer. In cages with few perches, the subordinate birds are forced to spend most of their time on the floor where they feel threatened and consequently become more stressed. What s more, there is less risk that birds, when they are disturbed or become violent (for example during attacks or handling in the cage), will fly against the mesh in cages with a larger number of perches. With very nervous birds it is sometimes necessary to install visual obstacles to avoid these collisions (for example, strips of wood attached to the mesh some 20-25cm apart). To prevent the tail feathers rubbing against the mesh, the perches must be installed at least 60cm away from it. As the species is composed of cliff breeders, the perches should be adapted to the anatomy of their claws to prevent the formation of corns. They should be flat and some 20cm wide so that the claw is completely supported. They also need to be sufficiently rigid to prevent them from bending during copulation, which would provoke insecurity and lead to the birds abandoning the copulation on the perch Ladders Because bearded vultures are soaring birds of prey it is impossible for many of them, especially females and older birds, to get up to the perches by beating their wings. Thanks to the installation of ladders with a minimum width of 20cm and a maximum height of 45-60cm (the height being adapted to the flight ability of the individual bird), it is much easier for the birds to transport material to the nest (important behaviour during the breeding season, which reinforces the relationship between the pair) as well 6

7 as to bring food to the perches (where food can be handled more easily than on the floor) Feeding places For birds to be relaxed in their cages, it is important that they are familiar with the working practices of the centre. For this reason, it is advisable to install a feeding place in each cage measuring 90 x 90cm, which is close to the door and away from the nest and where food can be placed every day at the same time. The familiarisation can become such that some individuals that have been naturally raised will, after some time of being fed by the staff, actually take food from their hand across the mesh. In cages that house a greater number of birds (juvenile cages), the installation of various feeding places made of wood or stones in different parts of the cage will allow each bird to eat above the floor and at a distance from the others, something which is essential for subordinate birds Drinking troughs All birds of prey drink and tend to bathe themselves regularly. During the period of egg formation, females drink large quantities of liquid. Anxiety during the incubation period is one of the main causes of egg loss, a factor that has also been observed in the bald eagle (Carpenter et al., 1987). It must be taken into account that birds become more nervous, aggressive and sensitive during the reproductive cycle; a phenomenon that has been mentioned by various researchers involved in the breeding of other large birds of prey. The most vulnerable days are those during the incubation period and the first days of the chicks life, when even handlers have been attacked (Asakura et al., 1978; Gerrard et al., 1979; Johnson & Gayden, 1975; Maestrelli & Wiemeyer, 1975; Schumann, 1928; Todd & Meachen, 1974; Wiemeyer, 1981; Wylie, 1973). The loss of eggs due to the anxiety caused by the necessity of entering the cage on a daily basis to clean and fill the drinking troughs can be prevented by installing a system providing a continuous supply of drinking water, with a mechanism that allows it to be regulated from outside the cage. The same system is used in the captive breeding of falcons (Cade et al., 1977). The drinking troughs should be big enough to allow the birds to bathe (210 x 130cm and 35cm depth) and should have a sufficiently soft access ramp to allow individuals with physical defects to be able to leave them easily Bowls for mud baths The fact that bearded vultures can develop the peculiar habit of bathing in mud rich in iron oxide is well-documented (Caussimont et al., 1995; Frey & Roth-Callies, 1994; Margalida, 2000; Negro & Margalida 2000; Xirouchakis, 1998). Although the reason for this behaviour is still unknown, various hypotheses exist (Arlettaz et al., 2002; Negro et al., 1999; Negro et al., 2002). One of these hypotheses is that the behaviour is used as a signal of status (Negro et al., 1999). It has been observed that birds in captivity regularly carry out this activity and that the frequency depends on the weather and how often mud is provided. Furthermore, the intensity of the colouration correlates with the age and sex of the bird, with older individuals and females displaying more intense pigmentation (Frey & Roth-Callies, 1994). The baths are only used when the birds do not feel threatened and are interrupted if they are disturbed. Given that birds in a breeding programme spend their whole lives in captivity and that they must be kept in good physical and psychological condition, it is advisable to offer them all available means of allowing them to develop as many innate behavioural 7

8 patterns as possible. For this reason, it is advisable to install a bowl in each cage, preferably made of concrete and measuring approximately 1m in diameter and with a depth of 10cm, where mud rich in iron oxide can be offered every 15 days (except during the breeding season). The mud should be mixed with water until it reaches the consistency of a creamy liquid. Before providing mud from any unknown source it should be analysed to detect any possible toxic substances like heavy metals or other organic contaminants that could affect the health of the birds, since those individuals that are just developing the custom of mud-bathing will test the consistency with their beaks and swallow the mud (Frey & Roth-Callies, 1994). Two birds died of lead poisoning in a zoological park after they were provided with mud with a high lead content Nests The dimensions of nests in successful breeding programmes of birds of prey are extremely varied (Hancock, 1973; Gilbert et al., 1981; Maestrelli & Wiemeyer, 1975; Todd & Meachan, 1974; Wylie, 1973). However, they all emphasize the fact that the nest must be located in the most secure part of the cage. For this reason, it is necessary to install it at the end of the cage which is furthest away from the door. Furthermore, given that they are cliff dwellers, the nest should be closed on all sides except at the front, simulating a cave. At the same time, it is a territorial species which defends a maximum territory of some m around the nest (Bertran & Margalida 2002, Brown, 1988; Grubac, 1987; Hiraldo et al., 1979). This territorial behaviour may have grave repercussions during pair formation. However, so the incubating bird can remain as undisturbed as possible and dedicate itself exclusively to the incubation, it is important that their mate carry out a territorial defence function. This has also been observed in the bald eagle and in the white-tailed eagle, with males usually defending the territory (Asakura et al., 1978; Fentzloff, 1983; Johnson & Gayden, 1975; Maestrelli & Wiemeyer, 1975). With the construction of a platform measuring 3 x 1.3 x 0.9m in height where the nest (1.3 x 1.3m) is located, there is sufficient space for the bird which is not incubating to be at the side of its mate while it is keeping watch over the territory (the cage). In this way behaviour is clearly distributed. In a comparative study carried out in the Guadalentin breeding centre between a pair and a male that incubated successfully on its own, the male proved to be much more susceptible to any disturbances than the pair (Llopis et al., 1999, 2000, 2001, 2002a, 2002b, 2003, 2004). What s more, this platform also offers shelter for the bird defending its territory in the case of bad weather. At the beginning of the bearded vulture breeding programme, various eggs were lost when the nest got wet and/or because it was defective. Building a roof which projects at least 1m was the solution to the problem. In several cases, especially in pairs with no nest building experience, eggs have been found outside the nest, on the platform after one side of the nest collapsed or lost in the bottom of the nest between branches. These eggs have sometimes been broken when adults walked over the branches. This occurred with a pair of harpy eagles in Los Angeles Zoo (Todd & Meachan, 1974). These kinds of accidents have been prevented by building a wooden frame and covering the bottom with tree bark to provide a firm base and by filling the nest with suitable materials such as wool to line the hollow and placing branches nearby. To avoid conflict originating from the territorial behaviour displayed by pairs of bald eagles housed in different cages, it is advisable to position their nests so that incubating birds have no visual contact with birds other than their own mates (Maestrelli & Wiemeyer, 1975). The same is true of the bearded vulture. Positioning the 8

9 nests towards the South/South East means that, as well as preventing incubating birds from seeing each other, they are also protected from any adverse weather from the north. Sometimes, the high potential aggressiveness of this species (see figure 6.3), especially during the reproductive cycle, can result in attacks between pairs. These attacks are often linked to a change in the physical appearance of one of the birds (there are 7 pairs which display this behaviour). It seems that wet birds (after bathing or being in the rain) are not recognised. Building a platform that runs along the width of the cage (6m) and divided into two parts offers the subordinate bird the possibility of protecting itself in case of bad weather or drying itself without being seen by its mate Access to the cage The access to the cage must be clearly visible to the birds. This means that, if it is necessary to enter the cage, the birds can see the handler approaching in advance and can react without getting nervous. This can be achieved by constructing a single access door located in the part of the cage that is furthest away from the nest. This has also been recommended by other authors (Carpenter et al., 1987) Positioning of equipment in the cage It has been observed that the incubating bird is more relaxed when the drinking trough, mud bowl and feeding platform are placed in parts of the cage which are visible from the nest, because it can maintain visual contact with its mate while he/she is carrying out other activities Cage distribution. When cages are built so that birds can see each other, the relationship between each pair is strengthened because they instinctively protect their territory from the neighbouring birds and can therefore channel some of their potential aggressiveness (which increases at this time) against other birds and not, as has occurred in isolated pairs, against their own mates. Furthermore, it has been observed that, in centres housing several pairs of birds, the younger pairs will begin to reproduce earlier, stimulated by their expert adult neighbours. In the VBU where an average of 30 birds are housed, the average age of a bird when the first egg is laid is 7.56±1.82 years (n=16, 7 males and 9 females). On the other hand, in zoos it is 10.25±3.38 years (n=32, 16 males and 16 females). It has also been observed in California condors that allowing pairs to see each other encourages the development of reproductive behaviour (Arnold, 1993). 4. ORIGINS OF THE BIRDS Advice about the ideal origins and status of a reproductive stock will change depending on the objective of the programme and on the species in question. In the case of the bearded vulture, other captive breeding reintroduction programmes have been used as a guide: peregrine falcon (Falco peregrinus), bald eagle, white-tailed eagle and California condor. Cade et al. (1977) suggest that the ideal age for capturing wild falcons is just before they leave the nest. However, in the bald eagle programme, where individuals of different ages were captured (chicks, juveniles and adults) no correlation between reproductive success and the age of the bird when it was captured was observed. On the other hand, it was observed that, although female bald eagles that couldn t fly did lay eggs, the majority of the disabled males didn t copulate (Carpenter 9

10 et al., 1987; Wiemeyer, 1981). Neither has a correlation between reproductive success and the origins of the founders been mentioned by the California condor project (Meretsky et al., 2000; Wallace & Toone, 1992). This is also true of the bearded vulture. However, it has been observed that the breeding methods and the handling of the bird depending on its origins and physical state, does influence reproductive success. In general, wild birds, especially physically disabled adults, are much more nervous and sensitive to disturbances than those bred in captivity and they must be completely undisturbed if they are to reproduce. Furthermore, birds that have been unsuitably handled before being incorporated into a breeding programme (having been isolated from other birds of the same species for years or having been continuously handled etc) display most behavioural problems (copulating with perches, incorrectly handling their eggs and/or chicks etc) with some of them never forming a pair. However, with correct handling, 2 individuals injured by their own kind (a male BG005 and a female BG015) have reproduced, as well as 2 birds amputees (a male BG002 and a female, BG199) and 2 males that can t fly (BG065 and BG021). Thanks to appropriate handling, a pair of white-tailed eagles in the VBU have copulated perfectly, despite the fact that they are both amputees and are therefore more irritable and nervous. In a private centre, 2 black vultures (also amputees) have reproduced successfully (Frey, personal comment). 5. HOUSING OF THE BIRDS At the beginning of the bearded vulture breeding programme, the founders were housed in various zoological parks. Some of the pairs had reproduced in the parks (Almaty Zoo, Innsbruck, Moscow and Wassenaar), but the majority of them hadn t. Once the birds that hadn t mated and the psychologically and physically conflictive individuals had been transferred to the VBU, 64.18% of the 67 founders reproduced. Currently, all the founders and/or individuals with physical defects are moved to centres with specialised staff where adequate handling and a suitable pair can be determined in advance. Juveniles and established pairs, given that they are easy to handle, are also housed in centres that are only dedicated to breeding. It is well known that pairs of the larger birds of prey defend their territory, especially during the mating period and will attack or even kill birds of the same species or other birds of prey who share the same cage. In the Washington Zoological Park, a pair of bald eagles that were entering the breeding season began to attack another female housed in the same cage. The attacks became so violent that she had to be taken out of the cage (Johnson & Gayden, 1975). Something similar occurred with the king vulture in the Menagerie de Paris and with a lappet-faced vulture (Torgos tracheliotus negevensis) in the Tel Aviv University Zoo. In both cases, it was necessary to remove a third bird from the cage (Schlee, 1994; Mendelssohn & Marder, 1989). For this reason, Carpenter et al. (1987), in their compendium on captive breeding of eagles, recommend that each pair be housed in a separate cage to prevent intra- and interspecific attacks. The white-tailed eagle also displays this same aggressive behaviour during the reproductive period. In the Tama Zoo (Tokyo) a pair of white-tailed eagles shared a cage with 8 kites (5 Haliastur indus and 3 Milvus migrans) of which 2 were killed by the pair during the breeding season (Asakura et al., 1978). In the Schönbrunn Zoo (Vienna), a pair of white-tailed eagles at the beginning of their breeding season forced griffon vultures, black vultures and various species of eagles to remain in one corner of the cage and killed 2 bearded vultures. For fear of losing more bearded vultures during 10

11 the following breeding season, the pair of white-tailed eagles had to be removed from the communal cage (Fiedler, 1970). In the same zoo, Antonius (1933, 1934) had already mentioned the loss of several bearded vultures after they were attacked by white-tailed eagles. In 2002 in the Tierpark Friedrichsfelde (Berlin) a male bearded vulture died after it was attacked by eagles housed in the same cage. Finally, in Dresden Zoo, when a successful pair had to be moved to a communal cage while work was carried out on their own aviary, they immediately stopped laying eggs and within a year the male had died of aspergillosis, a disease related to the physical condition of the animal. Psenner (1976) suggested that one reason why bearded vultures didn t reproduce in zoological parks was because they were kept in communal cages. The griffon vulture and black vulture breed in colonies. For this reason, they can also breed in groups in captivity (Jerez ZooBotánico, Prague Zoo and in acclimatisation cages for reintroduction projects in France and Italy) (Quevedo and Pithart, personal comment; Genero & Perco, 1995; Terrasse, 1995). However, the bearded vulture does not breed in colonies and it defends its territory against other bearded vultures and other birds of prey. This aggressive behaviour means that it should be handled as though it were an eagle and it is necessary to keep pairs separately. Schumann (1928) observed that a pair of bearded vultures in Sofia Zoo didn t begin to breed until they were separated from other bearded vultures (4 from Asia Minor, 1 from Greece, 1 from the Caucasus and 1 from the Spanish Pyrenees). Although the California condor also breeds in colonies, for genetic reasons the pairs are kept separately although they can see each other, which encourages the development of reproductive behaviour (Arnold, 1993). Currently all pairs of bearded vultures are housed separately. Only juveniles up to 3 years of age can be kept in communal cages. When they have formed pairs and start to display territorial behaviour the pair is immediately separated from the others. 6. THE BIOLOGICAL CYCLE AND CAPTIVE BREEDING As far as the technique of captive breeding is concerned, two principle methods must be recognised: natural breeding and artificial insemination. Both methods have their advantages and disadvantages and their use depends on the species, status of the bird and the objective, with artificial insemination being mainly recommended for birds that have imprinted on humans (Grier, 1973; Temple, 1972). In the case of bearded vultures, the objective of the EEP is to maintain a genetic reserve and to produce birds, which can be later released. Because of the low reproductive rate of bearded vultures and the cainism behaviour of the chicks, the natural breeding method has proved to be the most viable with a view to fulfilling the objectives established by the EEP Sexual dimorphism. The bearded vulture, like other vultures, displays an inverse sexual dimorphism with females being slightly larger than males, a difference which is hardly noticed in natural conditions (Margalida & García, 2002). According to Hiraldo et al. (1979), the only significant biometric parameter is the length of the beak, with that of the female being longer. In captivity, although the females are generally slightly larger than the males some inverse examples exist, with females that only weigh 5.5kg and males that weigh over 6kg (not including birds with nutritional deficiencies). In particular, there are 2 males that weigh over 7kg (one of them, BG001, reached 8kg), but both of these birds displayed a female phenotype and never copulated. According to the study being carried out by the VBU and CCG, some small biometric differences between males and 11

12 females do appear to exist, as well as differences in their general appearance. Females usually have a more pronounced upper curve on their beaks, their heads are wider and the distance between their claws when they are perched is wider. However, these differences, which have also been observed in wild birds (Margalida & Heredia, personal comment) are minimal and should be applied with caution. Differences do exist in reproductive behaviour. It is well known that 2 males in captivity will form a pair and develop all the behavioural patterns of a reproductive pair: nest building, copulation, incubation of dummy eggs and chick rearing. There were several pairs of bearded vultures in various zoological parks in the 1970 s which never laid eggs. Initially it was thought that the females were infertile. However, when the members of a pseudopair died, an autopsy revealed that they were both males. It was then that researchers began to suspect that some pairs were actually made up of 2 males. Psenner (1976), attributed sexual dimorphism as the reason for the low number of reproductive pairs in captivity. At that time, the only way to determine sex was via endoscopy, a method that had given incorrect results in bearded vultures on more than one occasion. Later, sex was determined using cariotypes. This is an expensive method which is also fallible. Currently sex is determined by a DNA test and there hasn t been a single error so far. This is why it was extremely important to determine the sex of individual birds by observing the subtle behavioural differences between a pair of males and a natural pair. Some male pairs will make cloacal contact during copulation, others will not. In the wild, cloacal contact has also been observed between males in polyandrous pairs (Bertran & Margalida, 2003). In general, the dominant male is the one that mounts the other. In pairs where cloacal contact has not been observed during copulation, the subordinate male does not bend down and keeps its body rigid. However, the same bird may request copulation by flapping its wings with its body erect whilst cheeping and stamping its feet around the dominant male and even sometimes jumping on top of it. This behaviour has not been observed amongst females. However, in pairs where cloacal contact has been observed during copulations, the subordinate male bends its body horizontally during the copulation as though it was a female with the result that cloacal contact is achieved. Although individual differences exist, during the mating season all members of male pairs will immediately incubate any dummy eggs which are offered to them. On the other hand, females do not accept dummy eggs immediately and will often throw them out of the nest. They often need weeks before they will accept eggs which have been replaced daily in the nest Sexual maturity. Heredia (1991) and Garcia (1993) mention that several years may pass between the formation of a pair and their first incubation. They estimate that bearded vultures do not incubate until they are approximately 10 years old, although they have already reached sexual maturity. This has also been confirmed in captivity. In captivity, the youngest successful reproductive age was 5 years (1 male and 1 female). Both were paired with an older bird. The oldest age for males was 18 years (n=1) and for females 19 years (n=1). The male was a bird that had been partially hand-reared and the female had been with a male that was also partially hand-reared, until she was 14 years old. The female laid eggs in her second breeding cycle with a male that had been reared naturally and in the third cycle her first chick hatched. However, the average age of the first reproductive cycle in which copulation takes place is 9.62±3.85 (n=21) for males and 7.71±2.74 (n=24) for females. The average age at the arrival of the first eggs is 10.57±3.5 (n=23) for males and 8.70±2.98 (n=27) for females. The average age of reproductive success is 11.26±3.75 (n=19) for males and 9.25±3.29 (n=20) for females. 12

13 If birds that have been partially hand-reared are not included (n=8, 6 males and 2 females) the average age of males goes down considerably (8.13±2.2; 9.24±2.19; 9.79±2.19 respectively). If we only compare the average age of the bird when the first eggs are laid of those individuals that have been naturally reared in the VBU and in zoos, that of the males is 8.43±1.9 (n=7) and 9.80±2.30 (n=10) and that of females is 7.0±1.6 (n=8) and 8.80±2.57 (n=15) respectively. This difference of approximately 1.5 years can be attributed to the aforementioned distribution of the cages, to the advanced detection of incompatibility between individuals in the specialised centres and to the fact that these incompatible pairs are rapidly changed. In this way, the female BG015 reproduced when she was 12 years old and during her third cycle after being transferred to the VBU and paired with BG044 who was 17 years old and in his second cycle at the VBU. On the other hand, with the female BG175 and the males BG105, BG124 and BG223 it was necessary to change the pairings. However, once they were housed in a specialised centre they reproduced earlier (10, 10, 8 and 10 years respectively). The difference in age between males and females can be attributed to the fact that the majority of females are paired with much older males Pair formation. Thanks to the experience gained over 30 years of captive breeding with bearded vultures, currently all new pairs reproduce and those that don t at least carry out a reproductive function (incubating eggs or rearing chicks of other pairs). What s more, in general, birds that have not suffered any psychological trauma and which have been adequately reared in captivity reproduce successfully. However, there are 2 factors which have a very important influence on pair formation: aggressiveness and the method of rearing. As aforementioned, bearded vultures, like eagles, are extremely aggressive when defending their territory against other species of vultures and even against their handlers. To compensate for the fact that this potential aggressiveness is not used up in captivity, it can be channelled against the pair. In some cases it is necessary to temporarily separate the pair. These attacks may take place unexpectedly after several years or on a regular basis. Attacks sometimes take place after one of the pair has been bathing and is not recognised by its pair because of its wet plumage and these attacks, have also been observed in other species in captivity: in the San Clemente loggerhead shrike (Lanius ludovicianus mearnsi) and in the goshawk (Accipiter gentilis) (Littlefeather and Derek, personal comment). Similar attacks can be extremely dangerous and the pair can be injured, disabled (1 male, BG005, and 1 female, BG015) or even killed (2 males, BG048 and BG077, and 1 female, BG032). Only continuous observation of the pairs, especially during the breeding season, can prevent similar accidents. The continuous threatening behaviour of one of the pair (swelling of the red sclera, raised feathers on the head and nape of the neck, head held high and moved brusquely from side to side and use of threatening calls), the use of displeasure calls similar to those used by young birds and observing that birds start sleeping or resting in unusual parts of the cage are all signals of a problem between the pair. Cheeping, which is used to encourage birds to prepare and present food to the other member of the pair (Immelmann, 1982), can also be emitted by adult captive birds when they are attacked by another bird to encourage the dominant bird to immediately display a reflex behaviour directed towards food (Stegmann, 1959, 1965). Consequently, the emission of this infantile sound (the cheep), is a peacemaking behaviour. Eibl-Eibesfeld (1987) points out that these infantile behavioural patterns displayed between adults are aimed at 13

14 diffusing aggressions. This infantile behaviour has never been observed in wild birds, since they are able to avoid any such attacks. This has been documented in birds which have been reintroduced into the wild. As soon as the birds can fly and ward off aerial attacks, they stop cheeping (Llopis, 1996). On the other hand, when the behavioural patterns of this species are not fully understood, some attacks have been mistaken for copulatory behaviour when the dominant bird jumped onto the subordinate bird s back. However, it is normal that small disagreements between pairing birds are observed and it is necessary to wait at least 2 breeding seasons before any changes are carried out. Generally, the level of compatibility in a new pair of adults with reproductive experience will become clear during their first breeding cycle together. However, pairing aggressive adults can be extremely complicated. Furthermore, the continuous presence of visitors to zoological parks can have a negative influence on pair formation and can sometimes lead to attacks which are redirected towards the mate. It has also been observed that the presence of visitors also has a negative effect on the pairing of white-tailed eagles (Fentzloff, 1983). However, various techniques exist to facilitate pairing in difficult cases. In a study carried out with birds reintroduced into the Alps, in 88% of the intraspecific interactions which took place between juveniles and older birds on the floor, the juveniles always won (n=233). In feeding areas, the juveniles were 100% dominant. On the other hand, older birds were dominant in 96.7% of aerial attacks (n=60) (Llopis, 1996). Because of this, putting a juvenile bird in a cage with a new pair will automatically reduce their aggressiveness because the juvenile will be dominant from the outset. But, as soon as the adults form a pair, the juvenile must be immediately removed from the cage because the adults will recognise the cage as their territory and will defend it by attacking the juvenile. This method has been used with the white-tailed eagle and the bald eagle (Fentzloff, 1983; Johnson & Gayden, 1975). Sometimes pairing the juvenile with the aggressive adult will also work. However, it must also be taken into account that juveniles of one year and under are also very aggressive and express this aggressiveness in a different way to older birds. Both display swollen scleras, emit threatening calls and raise their plumage, but only juveniles in the first months after leaving the nest will incline their heads parallel with the floor (a time when the head and neck feathers are still growing). On the other hand, an older bird (once the head and neck feathers are completely grown) will raise its head, move it brusquely from side to side (whilst always looking at its rival) and will ripple the feathers on the nape of the neck (Llopis, 1996). Another method, which has already been mentioned, is allowing visual contact between neighbouring pairs. Aggressiveness is redirected towards the neighbouring pair (territorial behaviour) and, in the case of a lack of social contact, the reproductive behaviour of a neighbouring pair (nest reconstruction, copulations etc) stimulates the formation of pairs. In this way, the founder male BG031 that had previously been housed in a centre where it had killed a female and injured another, reproduced successfully in the VBU. As soon as it was housed with a female in a cage positioned between 2 others (one of juveniles and the other of a reproductive pair) it dedicated itself to defending its territory from the other birds and never attacked the female. However, the neighbouring reproductive pair began incubating rather carelessly because they were more concerned with defending their territory than with their eggs. Finally, it was necessary to close the contact wall between the 2 pairs. Offering the cage to the subordinate bird a few weeks in advance is another effective technique. Carpenter et al. (1987) and Fentzloff (1983) also recommend this method for bald eagles and whitetailed eagles. This allows the subordinate bird to become familiar with the cage which reduces its stress levels. Sometimes, just changing the cage can be enough to prevent 14