Status

Threats

Double clutching

Two captive-bred pairs - one of Griffon and one of Cinereous Vultures, have been included in the breeding programme in the WRBC intended to increase the number of the local population by producing parent-reared chicks which subsequently are released into the wild. Some of the birds in the pairs were replaced over the years; however, all were disabled and incapable of surviving in the wild.

The male Griffon Vulture B58 was caught in the wild in Bulgaria exhausted and in a generally bad condition. At the end of 2006, it was admitted into the breeding programme of the WRBC. Its first partner was the vulture Leshka. In 2014, the pair had their first chick. This was followed by two unsuccessful breeding seasons after which the female laid unfertilised eggs. The couple were separated in 2016. B58 was moved to the visitors’ part of the Centre. The female Griffon Vulture K8X arrived in June 2014 from Spain where it was captured from the wild. In Bulgaria, it was released from the aviary in Kotel. In December 2014, it was found shot in Balabankuru, Turkey and was treated in the Faculty of Veterinary Medicine of Istanbul University. It was operated on to remove the bullet and, as a result, a joint in her left wing was blocked. In December 2015, K8X was admitted in the WRBC to become part of the breeding programme with the male KOJ; however, the male showed aggression and the pair were separated. A new pair was formed - B58 and K8X and their first successful season was in 2019.

The first Cinereous Vulture in the breeding programme of the WRBC was admitted in 2011. It was the female with ring number J2028 which arrived from Spain after being rescued from the wild. It was hatched in 2009. In 2014, a male bird arrived from France with ring number A19, hatched in the wild. The pair were separated at the end of 2018 because they were unsuccessful as they never copulated or had fertile eggs. The female was given a chance with another partner in 2019. The male was replaced with a bird from Ouwehands Dierenpark Zoo in the Netherlands - ring number CS, hatched in 2012. All their eggs were either infertile or died during incubation due to excessive weight loss. In 2023, the female was changed with another disabled bird - ring number K2. K2 was captured in 2017 in Spain and had partial amputation of one wing.

Interior of the cages

The cages of the vultures have been constructed suitable for the purposes of the captive breeding: 12 metres long, 6 metres wide and 4 metres high (Fig. 1). They provided the birds enough space to easily perform short flights and jumps within the cage. The door is on the opposite side of the nesting platforms, preventing the vultures from stress when keepers enter the cage for cleaning, changing water or reconstructions. The cage has two water ponds: one larger oval-shaped (1.8/1.3m) and a smaller spherical one (1/1m) with a tap water system, so the birds have access to fresh water for drinking and bathing. There is a feeding platform on the ground beside the door (1/1m) and also a feeding table installed in the middle of the cage. The two corner nesting platforms (2/2/2.8m) are at 2.7 metres height from the ground, with four stairs for climbing. Two of the walls and the roof are with mesh giving the birds sight to the surroundings. The double-door protection is a crucial safety precaution to prevent the birds from escaping the cage when opening the inner door. Food is provided through a small door in the corridor to keep entrance of the breeders in the cage to a minimum - once a week for cleaning of the cage and water ponds and twice a year for medical examination of the birds. Thorough cleaning and disinfection of the facilities is made twice a year during the regular health examination of the pairs when the birds are taken out to avoid stress. The following was the protocol described in a publication by Huyghe et al. (2023).

Figure 1.  

Measurements of the cages for Griffon and Cinereous Vultures in the WRBC.

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Video surveillance

Behaviour and breeding methods

The data for the first pair are summarised in Table 2,and for the second - in Table 3.

The first Cinereous Vulture pair had their first egg laid on 28/3/2017, but it was infertile as they never had experience or copulations. The female was also not experienced in incubating and she broke it on the next day. Next season, on 9/4/2018 she laid an egg, which again was infertile and she broke it after one day. The pair was separated at the end of 2018 and the female was given a chance with another partner. The second pair started copulating and their first egg was hatched on 31/03/2019. On the next day - 01/04/2019, it was taken to the incubator and artificially incubated for 58 days. It was opened on 29/05/2019 and was found infertile. In season 2020, they started copulating on 19/03/2020. The first egg was laid on 25/03/2020 and immediately taken to the incubator. On 30/03/2020, they started copulating again. Second egg was laid on 15/04/2020 and taken to the incubator on 16/04/2020. The first egg was opened on 22/05/2020 and the second egg was opened on 10/06/2020. Both eggs were found infertile. From 2020, the weight loss of the eggs was monitored (Figs 2, 3, 4, 5, 6, 7, 8).

Figure 2.  

Season 2020 - egg 1 weight loss.

Figure 3.  

Season 2020 - egg 2 weight loss.

Figure 4.  

Season 2021 - egg 1 weight loss.

Figure 5.  

Season 2021 - egg 2 weight loss.

Figure 6.  

Season 2021 - egg 1 weight loss.

Figure 7.  

Season 2023 - egg 1 weight loss.

Figure 8.  

Season 2023 - egg 2 weight loss.

The first copulations for 2021 occurred on 29/01/2021 and the first egg was laid on 31/03/2021. On 01/04/2021, it was taken to the incubator. After three days - on 04/04/2021, the pair started copulating again and the second egg was laid on 24/04/2021. The first egg was opened on 02/06/2021 and the second - on 24/06/2021.

In season 2022, the first copulations occurred on 21/01/2022. The first egg was laid on 04/04/2022 and taken to the incubator on the same day. It was artificially incubated until 31/05/2022. It was infertile, but the embryo had died during incubation after weight loss of 23.2%.

In season 2023, they double-clutched again. The first copulation was spotted on 17/01/2023 and the female laid on 03/01/2023. Two days later - on 03/03/2023, the egg was moved to the incubator and it was opened on 04/05/2023. The second egg was laid on 06/04/2023 and taken to the incubator on the same day. It was opened on 01/06/2023. Both eggs were fertile, but the embryos had died during incubation. All data were systematically entered into a digital database (Table 4).

The days between each step of the process of breeding varied from one year to another. Differences were also observed between the clutching periods of the Griffon and the Cinereous Vulture pairs (Tables 5, 6). For the Griffon Vultures, it took 14 days from the day of copulation to the day of laying the egg of the first clutch in 2020. Meanwhile for the same year, in the Cinereous Vultures’ nest, this period was only 6 days. One year later, that same period took much longer for both of the pairs. The Griffon Vultures laid their egg 65 days after their first copulation was detected and, similarly, 61 days were needed for the Cinereous Vultures. In 2022, this period was shorter for the Griffon Vultures - 38 days, while it took 73 days for the Cinereous Vulture from the first copulation to the laying of the egg. The day gap for the period counted for the second clutch is less variable. In 2020 for the Griffon Vultures pair, it took 25 days and for 2021 - 24 days, likewise for the Cinereous Vultures’ couple in 2020, this period was 16 days and, for 2021, 20 days. For the Griffon Vulture, the first laid egg in 2020 was taken from the pair on the 17^th day after the laying and, in 2021, it was taken on the 14^th day and a second clutch was successful for both in this year. What is interesting is that, in 2022, the egg from the first clutch was taken from the parents on the 13^th day, but the attempt for the second clutch was not successful. The days that were needed for the egg of the Griffon Vulture to stay in the incubator were 42 for 2020 and 40 for 2021. For the second clutch in 2021, the egg stayed in the incubator for 34 days. Meanwhile for the first clutched egg of the Cinereous Vultures, it took much longer- 58 days for 2020 and 63 days for 2021. The second one stayed in the incubator for 55 days for 2020 and 61 days for 2021. The year of 2021 is indicative for the development of the two Griffon Vulture chicks. The first one was raised in the incubator for 6 days and then was given to the parents who took care of it for 68 days. The second chick was raised by the parents for 109 days. Looking back in 2020, this period was 125 days for the chick from the second clutch. The first chick was separated from the parents at the age of 74 days and the second one at the age of 122 days.

Standard protocols regarding breeding the vulture species in captivity were followed (Prakash 2012, Wolter et al. 2015). Our study involved one pair of Griffon Vultures and one pair of Cinereous Vultures - with some changes in the partners through the years, breeding in captivity in the WRBC in Bulgaria. A second clutch was induced on six occasions for the Griffon Vulture pair and on three for the Cinereous Vulture pair. The time between the taking of the first egg and the laying of the second one was approximately 27.5 days for the Griffon and 26.3 days for the Cinereous Vultures in our study. This corresponds to the interval of 20-28 days and results from other studies both of wild and captive vultures (Mendelssohn and Leshem 1983, Martinez et al. 1998). Renesting is often associated with increased breeding success in various bird species (Morrison 1998, Monroe et al. 2008 , Jackson and Cresswell 2017, De la Cruz et al. 2022) at the same time; for Griffon Vultures and others - a lower fledging success has been estimated for hatchlings from second clutches compared to those from the first, due to late fledging dates (Linden and Møller 1989, Brouwer et al. 1995, Martinez et al. 1998, Casas et al. 2009). On the other hand, in facilities where breeding and release happen in a controlled environment, this downside is avoided and, in turn, the second offspring of raptors is positively related to increased re-introduction and conservation success (Wood and Collopy 1993, Khan and Murn 2011, Bowden et al. 2012).

In the WRBC, the overall breeding success for the Griffon Vultures was aided by the renesting - from all the first clutches between 2013 - 2022, there would have been only one reared chick, compared to four reared in total from both clutches for the same period. This showed the positive effect of inducing renesting - even a few individuals can be of great importance to conservation programmes, which justified the efforts. For the Cinereous Vultures, double clutching made no difference to the breeding success due to the lack of successful hatchings from any of the clutches to date - this poses a need for further investigation in order to determine the cause of the problem.

The authors express gratitude to Elena Kmetova-Biro, Ivelin Ivanov, Mirela Kazakova, Simeon Marin and Yana Andonova.