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ECOLOGIA BALKANICA 2020, Vol. 12, Issue 2 December 2020 pp. 53-63

Occurences of the Cinereous ( monachus) in the Eastern Rhodopes,

Volen S. Arkumarev1,2*, Dobromir D. Dobrev1,2, Anton A. Stamenov1, Vanya A. Angelova1, Atanas G. Delchev1, Vera A. Dyulgerska1, Sylvia Zakkak3, Eleftherios Kapsalis4, Stoycho A. Stoychev1

1 - Bulgarian Society for Protection of /BirdLife Bulgaria, Yavorov complex, bl. 71, en. 4, 1111 Sofia, BULGARIA 2 – University of Plovdiv “Paisii Hilendarski”, Faculty of Biology, Department of Ecology and Environmental Conservation, 24 Tsar Assen Str., 4000 Plovdiv, BULGARIA 3 - Management Body of Dadia-Lefkimi-Soufli Forest National Park, 68400, Dadia, 4 - WWF-Greece, 68400 Dadia, GREECE *Corresponding author: [email protected]

Abstract. The Cinereous Vulture (Aegypius monachus) is the largest vulture species in Europe. It is currently extinct in Bulgaria, but individuals from the only Balkan population of the species located in northern Greece frequently forage in the Bulgarian side of the Eastern Rhodope Mountains. We studied the patterns of occurrences, numbers and age structure of Cinereous in the Eastern Rhodopes, Bulgaria. During 2016 – 2019 we recorded 215 Cinereous Vulture occurrences. The majority of the observed individuals (72.7%) were immature while adults totaled 23.7%. The highest number of vultures were recorded in spring and summer. Cinereous Vultures visited local supplementary feeding stations singularly or in groups of up to eight individuals. Our study shows that Eastern Rhodopes and specifically SPAs ‘Studen kladenets’, ‘Byala reka’ and ‘’ are important foraging areas and hence high priority conservation areas for the species in Bulgaria.

Key words: Aegypius monachus, foraging, age structure, viewpoint monitoring, feeding station.

Introduction al., 2017). The Cinereous Vulture is The Cinereous Vulture Aegypius considered “Near threatened” according to monachus is a large scavenger with a wide the IUCN Red List (BirdLife International, distribution spanning from to 2020). The only breeding population of the (Ferguson-Lees & Christie, 2001). The species on the Balkan Peninsula occurs in global population of the species is estimated Greece (Skartsi et al., 2008). This population to comprise 7 800 – 10 500 pairs, which was at the edge of extinction with only 4 – 5 equals 15 600 – 21 000 mature individuals breeding pairs and 26 individuals in 1979 (BirdLife International, 2020). Europe holds (Hallman, 1979). Over the next 10 years the 2 536 – 2 838 breeding pairs distributed population started to slowly recover. Two across five countries – , Portugal, decades later the number of breeding pairs , Greece and Ukraine (Andevski et reached 21 (Vlachos et al., 1999) but

© Ecologia Balkanica Union of Scientists in Bulgaria – Plovdiv http://eb.bio.uni-plovdiv.bg University of Plovdiv Publishing House Occurences of the Cinereous Vulture (Aegypius monachus) in the Eastern Rhodopes, Bulgaria remained stable over the next decade availability along with long-term (Skartsi et al., 2008). Nowadays, it is implementation of conservation measures confined to a colony of about 30 breeding resulted in the significant increase of the pairs in the Dadia-Lefkimi-Soufli Forest population in the area National Park (Zakkak & Babakas, 2015). (Demerdzhiev et al., 2014; Dobrev et al., However, small populations restricted to 2019) and probably had a positive impact confined areas are fragile and face higher on the Cinereous Vulture population as extinction risk due to persistent threats, well. Through radio tracking and GPS such as poisoning or stochastic events. telemetry it has been confirmed that Despite applied large-scale conservation individuals from the breeding population in measures, the population still suffers Greece are foraging in the Bulgarian side of increased mortality due to poisoning the Eastern Rhodopes (Vasilakis et al., 2008, (Pantovic & Andevski, 2018; Vavylis et al., 2016). Furthermore, a study on the diet of 2020) and other threats, such as collision the species confirms that it is feeding on with energy infrastructure, such as wind carcasses found in Bulgaria (Skartsi et al., turbines (Vasilakis et al., 2016, 2017). 2015). However, there is a lack of In Bulgaria the species had wide knowledge on the phenology and age distribution until the beginning of the 20th structure of the Cinereous Vultures century. In some areas it was considered foraging in Bulgaria. Information on the more abundant than the Griffon Vulture main foraging areas and seasonal dynamics fulvus. It occurred in the Rhodopes, of vulture occurrences is crucial to inform Balkan Mountains, Rila, Pirin, Dobrudzha, species conservation programs and plan the Danubian Plain, Provadia-Royak Plateus implementation of adequate conservation etc. (Farman, 1869; Reiser, 1894). However, actions. in the middle of the 20th century the Here we present data on the pattern of population has undergone a dramatic occurences, numbers, age structure and the decline, mainly due to mass poisoning main foraging areas of the Cinereous campaigns against terrestrial predators Vultures in the Eastern Rhodopes, Bulgaria. (Patev, 1950). Around 1960 it hardly This study aims to contribute to the overall occurred in Bulgaria, although it is possible knowledge on the distribution and that single pairs were breeding in the movements of the last breeding colony of Eastern Rhodopes and the Eastern Balkan the Cinereous Vulture in the Balkan Mountain until the 1980s (Michev, 1985). Peninsula and to inform the running The last confirmed breeding record in conservation programs for the species. Bulgaria dates back to 1993, when a single pair bred near Studen kladenets reservoir in Material and Methods the Eastern Rhodopes (Marin et al., 1998). In Pattern of Cinereous Vulture subsequent years there were numerous occurences in the Eastern Rhodopes, observations of pairs with courtship Bulgaria were studied in 2016 – 2019 with behavior, but breeding was not confirmed visual observations from stationary (Iankov et al., 1998; Tewes et al., 2004). viewpoints and regular observations at two Cinereous Vultures frequently forage far supplementary feeding stations. from their breeding sites and especially Observations from viewpoints over areas with high food availability Visual observations from 19 stationary (Carrete & Donazar, 2005; Moreno-Opo et viewpoints in 7 SPAs (Special Protected al., 2010). The large number of free ranging Areas) forming part of the Natura 2000 livestock (mainly ) and wild ungulates network were conducted twice per month in Bulgaria creates favorable feeding between December and May in 2016 and opportunities for vultures. High food 2017. Observations from the stationary

54 Arkumarev et al. viewpoints were held for a total of 1114 of the observed individuals with hours. Viewpoints were chosen at higher immatures representing 72.7% (n = 123), open spots on hills with wide view in all followed by adults 23.7% (n = 40). directions to improve visibility. Juveniles comprised only 3.6% (n=6) of the Observations were conducted observed individuals. In total, 27 marked simultaneously from 3 – 4 viewpoints with Cinereous Vultures were observed, of constant communication among the which 37% were adults, 59.3% were observers, in order to avoid double- immatures and 3.7% were juveniles. In counting, and follow the movements of the total, 45.5% of tagged vultures were recorded vultures in the area. recorded in Bulgaria more than once Observations at vulture feeding stations (between 2 and 5 times) during the study. Observations were performed during One immature individual was observed on organized supplementary feedings at least 44 occasions. It was recorded during every twice a month between 2016 and 2019, at a month of the year with the highest number supplementary feeding station in SPA of observations in spring and summer. It ‘Studen kladenets’. Observations were also was a regular visitor of the feeding station performed less regularly, at a feeding and frequently roosting nearby. In 2018 station in SPA ‘Most Arda’ due to food and 2019 we observed courtship behavior availability. We observed from a distance with another untagged immature vulture, greater than 500 m from the feeding stations but no breeding attempts were recorded. in order to avoid disturbance. Data The highest numbers of Cinereous collection started right after carcass disposal vultures were recorded in April and May and lasted until darkness, or until the (Fig. 1). In January and February only one carcass was fully consumed. The observed and two vultures were observed, Cinereous Vultures were aged following respectively. Forsman (2003): individuals in first Vultures observed from viewpoints plumage were considered as juveniles, from We conducted 1 114 hours of second to fifth plumage as immatures and observations throughout a period of 68 days from sixth plumage as adults. For every and recorded 47 Cinereous Vultures. marked individual the type of tag (wingtag, Overall, we spotted vultures in 37% of the ring or transmitter), position, colour and days with field observations. The age was inscription were recorded. Observations determined for 72.3% of the observed were made with spotting scopes (20×60) individuals. Immatures were the best and binoculars (10×60) during daytime, represented age class comprising 55.9%, under suitable weather conditions by followed by adults – 38.2%. Only two experienced observers. Data was collected juveniles were observed during the study. using the SmartBirds Pro app (Popgeorgiev The main flight corridor of the species et al., 2015). Spatial data were mapped and between Bulgaria and Greece was defined processed using QGIS software (QGIS by observations from stationary viewpoints Development Team, 2016). located at elevated spots in all SPAs in the area. We observed 34% (n=16) of the Results Cinereous Vultures in SPA ‘Byala reka’. In We observed 215 Cinereous Vulture SPA ‘Krumovitsa’ and SPA ‘Studen occurrences during observations from kladenets’ an equal numbers of vultures stationary viewpoints and regular were recorded – 29.8% (n=14). ‘Dobrostan’ observations at supplementary feeding was the only SPA where no vultures were stations. The age was determined for 78.6% recorded (Fig. 2).

55 Occurences of the Cinereous Vulture (Aegypius monachus) in the Eastern Rhodopes, Bulgaria

Fig. 1. Monthly dynamic of the observations of Cinereous Vultures in the Eastern Rhodopes, Bulgaria presented per age classes.

Fig. 2. Distribution and number of Cinereous Vultures observed per viewpoints.

56 Arkumarev et al.

Vultures observed at supplementary ‘Studen kladenets’ (95.8%), while only 4.2% feeding stations (n = 7) of the birds visited the feeding On 106 occasions, 168 Cinereous station in SPA ‘Most Arda’. The age of Vultures were observed taking advantage 80.4% of the Cinereous Vultures visiting the of the supplementary feedings. The feeding stations was identified. Adults majority of the vultures were observed at comprised only 20% of observed the supplementary feeding station in SPA individuals (Table 1).

Table. 1. Age structure of Cinereous Vultures observed at supplementary feeding stations in Bulgaria during 2016 to 2019.

Number of Number of Number of ind. Age Age class individuals observations per observation class % Adult 27 22 1.22 20% Immature 104 89 1.17 77.1% Juvenile 4 3 1.33 2.9%

Cinereous Vultures visited the feeding as a main movement corridor by the species stations mostly singularly or in small groups of (Noidoi & Vasilakis, 2011). This finding was up to three individuals. However, larger confirmed by data obtained from 27 groups were also observed. The highest Cinereous Vultures tracked with GPS number observed simultaneously at the feeding transmitters during the same period station in SPA ‘Studen kladenets’ was eight. (authors’ unpublished data) and a study on the feeding pattern and diet of the Griffon Discussion Vulture in the Eastern Rhodopes which Our study confirms that Cinereous revealed that vultures find most of their food Vultures frequently occur in the Bulgarian in SPA ‘Studen kladenets’ and SPA part of the Eastern Rhodopes throughout ‘Krumovitsa’. The density of livestock and most of the year, except for winter. The wild herbivores in this area is high creating observed individuals originated from the favorable feeding conditions for vultures. only breeding colony in the Balkans which is We found that SPAs ‘Madzharovo’ and found in the Dadia-Lefkimi-Soufli Forest ‘Ivaylovgrad’ which are mostly covered by National Park in Greece (Skartsi et al., 2008). forests and dense vegetation were less One Cinereous Vulture released as part of a frequently visited by Cinereous Vultures. reintroduction program in Kotel, Bulgaria The species prefers to forage in open areas was recorded as well in 2019 (Stoynov, 2019, where food detection probability is higher Blagoevgrad, pers. comm.). These (Carrete & Donazar, 2005; Garcia-Baron et observations are in line with results obtained al., 2018) which explains the lower visitation by GPS tracking of Cinereous Vultures from rate recorded for these two SPAs. No the colony in Greece (Vasilakis et al., 2016) vultures were recorded in SPA ‘Dobrostan’, and previous observations of marked which is located farther from Greece. Despite individuals. The majority of vultures were the number of livestock extensively grazing found to fly over SPA ‘Byala reka’ and SPA in this area being high, it is more remote ‘Krumovitsa’ following the valleys of the from the breeding colony and is located at Byala Reka river and Dushundere stream. higher altitudes making the foraging trips This is the shortest route between the more energetically costly therefore vultures breeding colony in Greece and the rarely visit it. supplementary feeding station in SPA The Cinereous Vultures were observed ‘Studen kladenets’ in Bulgaria which is used flying singularly or in small groups of up to

57 Occurences of the Cinereous Vulture (Aegypius monachus) in the Eastern Rhodopes, Bulgaria three individuals, in rare cases in mixed (Ruxton and Houston 2004; Duriez et al. groups with Griffon Vultures. The results 2014). The adverse weather in winter from the viewpoint monitoring indicated impedes thermal creation and determines that Griffon Vultures are using the same suboptimal foraging conditions. Rain or flight corridors during foraging. Both snow may impede flights for entire days, vulture species gained height over the bare especially in winter (Hiraldo and Donazar hills of the Irantepe ridge located in SPA 1990). Furthermore, in this period, the days ‘Krumovitsa’ which is the highest ridge in are shorter and vultures have less time for the area and then glided southeast or foraging. Studies on Cinereous and Griffon northwest. This area is remote and far from Vultures show that in winter they spent settlements, but with significant significantly less time foraging than during numbers of livestock. About 1 000 cattle are the rest of the year (Hiraldo & Donazar, extensively grazed along Irantepe ridge 1990; Xirouchakis & Andreou, 2009). (data obtained from the BFSA Juvenile Cinereous Vultures in Spain also www.babh.government.bg) providing good have larger home ranges in spring and feeding opportunities for vultures which summer but restrict their movements around explains the regular presence of both species. the breeding colony during autumn and At the supplementary feeding stations winter (Castaño et al., 2015). Cinereous Cinereous Vultures were frequently Vultures confine their movements to smaller outnumbered by the Griffon Vultures which areas in winter and avoid long energetically monopolize the carcasses. However, higher expensive foraging trips. In January and numbers of Cinereous Vultures were February 2017, the weather conditions in observed when offal was disposed. The Bulgaria and northern Greece were harsh disposal of offal allows more vultures to feed with heavy snowfalls and low temperatures simultaneously and reduces the competition over a long period. Under such unfavorable within the vulture guild (Cortés-Avizanda et conditions, Cinereous Vultures probably al., 2010; Moreno-Opo et al., 2015, 2020). In preferred to stay closer to the breeding 2017 the proportion of offal disposed at both colony and the supplementary feeding feeding stations in Bulgaria was higher station in the Dadia-Lefkimi-Soufli Forest which might explain the observed increase National Park which was supplied with food in the number of Cinereous Vultures visiting on a weekly basis. In spring, when flight the feeding sites. Thus, in order to increase conditions are improved, vultures make the species visitation rate and the longer foraging trips (Hiraldo & Donazar, attractiveness of the feeding stations in 1990) which can explain the increased Bulgaria we recommend the adoption of number of Cinereous Vultures observed in feeding protocols which envisage regular March and April in the Bulgarian side of the provisions with smaller pieces of meat and Eastern Rhodopes. On the other hand, the bones scattered around (Cortés-Avizanda et winter months coincide with the onset of the al., 2010). breeding season, when pairs are building The highest numbers of Cinereous and defending their nests and start Vultures in our study area were recorded in incubation (Ferguson-Lees & Christie, 2001). spring. The number of vultures observed During this period breeding vultures have from the stationary viewpoints or at the smaller home ranges and exclude long vulture feeding stations was low in winter distance movements (Vasilakis et al. 2008). (December – February) and gradually On the contrary, during the chick rearing increased towards the summer. Large period vultures increase their home ranges vultures, being soaring raptors, heavily rely since they have to satisfy food provisioning on thermal updrafts to travel long daily for their chicks and themselves. This is distances with low energy expenditures confirmed by our observations of a marked

58 Arkumarev et al. adult vulture breeding in Greece, which was However, young vultures from Spain and observed twice feeding in Bulgaria during Greece does not migrate but alternatively the chick rearing period. This shows that make long distance movements far from the under suitable weather conditions some breeding colonies (Vasilakis et al., 2008; breeding adults may undertake long Castaño et al., 2015). Similar to other raptors, distance movements in search of food. immature vultures disperse and explore new Furthermore, food availability in the Eastern areas gaining knowledge on the availability Rhodopes is high due to the large number of of other suitable foraging and breeding sites. extensively grazing livestock and wild This behavior also helps to reduce the ungulates. However, in winter livestock is competition with adults near the breeding kept near the villages or in shelters which colony (Watson 2010; Gil et al., 2014). leads to a reduction in food availability but Vasilakis et al. (2008) did not find significant in spring and summer livestock suffers differences in the home range size of adult increased mortality which creates favorable and immature Cinereous Vultures from the feeding conditions for the vultures. During breeding colony in Greece. Both age classes this period Griffon Vultures in the Eastern had larger home ranges during the non- Rhodopes rely mostly on carcasses found in breeding season with immatures inhabiting the wild rather than the food provided at the slightly larger territories. However, the supplementary feeding stations. The frequency of long distance movements has combination of the unfavorable flight not been studied. Adult vultures need to conditions in winter, the limited food find the balance between parental care for resources available and the start of the the offspring and foraging which affects breeding season with the associated changes daily travelling distances (Moran-Lopez et in vulture behavior probably explain the low al., 2006). They probably spend more time in number of Cinereous Vultures observed in the vicinity of the nesting sites and less the Eastern Rhodopes during this season. frequently undertake long distance The majority of the observed movements compared to immature individuals in our study were immature individuals. This could explain the low individuals. We must note that since not all number of adults observed in the Eastern individuals were marked we were not able Rhodopes but more research is needed to to estimate how many different vultures confirm this hypothesis. were actually observed. Our results However, we recorded some adults indicated that some individuals visit during our observations, including Bulgaria more frequently than others and individuals breeding in Greece which were this could have biased the determination of making one-day foraging trips to Bulgaria. the age structure. However, if we consider The relatively low number of adults only the marked individuals it is still evident permanently present in the area suggests that most of the recorded Cinereous that the presence of breeding pairs in the Vultures were immatures. They wander Bulgarian side of the mountain is unlikely. further away from the breeding colonies The prevalence of immature vultures and compared to adults (Yamaç & Bilgin, 2012), the observed courtship behavior are positive also observed in other vulture species signs for future colonization of the former (Monsarrat et al., 2013; Peshev et al., 2018). breeding grounds. Similar processes were In , and large observed in Portugal where the colonization proportions of juvenile and immature of the border areas with Spain was preceded Cinereous Vultures are migrant and spent by regular occurences of immature and adult the winter in more southern latitudes Cinereous Vultures (Lourenço, 2011; (Gavashelishvili et al., 2012; Yamaç & Bilgin, Lourenço et al., 2013; ICNB, 2017). However, 2012; Kang et al., 2019; Reading et al., 2020). the steady increase of the Spanish

59 Occurences of the Cinereous Vulture (Aegypius monachus) in the Eastern Rhodopes, Bulgaria population has facilitated this process and Segre Foundation. We would like to (Moreno-Opo & Margalida, 2014; ICNB, express our gratitude to Ioannis Tziambazis, 2017) while the population in Greece despite Athanasios Chalivelentzios and Petros Babakas increasing over the past 30 years, suffers from the Management body of Dadia-Lefkimi- high mortality and reduced breeding success Soufli Forest National Park for their (Skartsi et al., 2019), thus, is not expanding contribution in vulture tagging and data outside Dadia-Lefkimi-Soufli Forest collection. We are grateful to Connor Panter for National Park (Zakkak & Babakas, 2015). proofreading the manuscript and to two Our study confirms that the Bulgarian side anonymous reviewers for providing helpful of the Eastern Rhodopes is an important part of comments. the foraging range of the Cinereous Vulture population, hence a high priority conservation References area for the species. Cinereous Vultures Andevski, J., Tavares, J., Williams, N. P., frequently use this area for foraging and Moreno-Opo, R., Botha, A. & Renell, J. feeding throughout most of the year, except in (2017). Flyway Action Plan for the winter. The supplementary feeding site in SPA Conservation of the Cinereous Vulture. ‘Studen kladenets’ is regularly visited by CMS Raptors MOU Technical groups of up to eight individuals and serves as Publication No. 6. Coordinating Unit a safe and predictable food source for the of the CMS Raptors MOU, Abu Dhabi, species. The high number of immature United Arab Emirates. individuals and the observed courtship BirdLife International (2020). Species behavior suggest that if the population in factsheet: Aegypius monachus. Retrieved Greece increases some pairs may settle and from birdlife.org on 03/05/2020. breed in Bulgaria creating a second breeding Carrete, M. & Donazar, J.A. (2005). Application nucleus on the Balkans. The implementation of of central-place foraging theory shows a reintroduction program in this area must also the importance of Mediterranean dehesas be considered for enhancing the recovery of the for the conservation of the cinereous species. Therefore, various conservation vulture, Aegypius monachus. Biological measures should be implemented to improve Conservation, 126, 582-590. doi: the survival of the vultures in the area e.g. 10.1016/j.biocon.2005.06.031. insulation of hazardous powerlines in areas Cortés-Avizanda, A., Carrete, M. & Donazar, frequently visited by vultures, anti-poisoning J. А. (2010). Managing supplementary and anti-poaching activities, use of lead-free feeding for avian scavengers, ammunitions in hunting areas, improvement of guidelines for optimal design using the feeding conditions by increasing the ecological criteria. Biological number of wild and supporting Conservation, 143, 1707-1715. doi: traditional livestock husbandry practices. 10.1016/j.biocon.2010.04.016. Castaño, J.P., Sánchez, J.F. & Díaz-Portero, M.A. Acknowledgements (2015). Dispersal and survival of juvenile This research was financed by the Black Vultures Aegypius monachus in National program "Young scientists and central Spain. Ardeola, 62(2), 351e361. doi: Postdoctoral candidates" funded by the 10.13157/arla.62.2.2015.351. Bulgarian Ministry of Education and Science. Demerdzhiev, D., Hristov, H., Dobrev, D., The fieldwork and data collection were Angelov, I. & Kurtev, M. (2014). Long- conducted in the frame of the LIFE project term population status, breeding “Conservation of Black and Griffon Vultures in parameters and limiting factors of the the cross-border Rhodope Mountains” (LIFE14 Griffon Vulture (Gyps fulvus) population NAT/NL/000901) funded by the European in Eastern Rhodopes, Bulgaria. Acta Union and supported by Rewilding Europe Zoologica Bulgarica, 66(3), 373-384.

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61 Occurences of the Cinereous Vulture (Aegypius monachus) in the Eastern Rhodopes, Bulgaria

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