Black kites wintering in Europe: estimated number, subspecies status, and behaviour of a bird wintering on Crete and Turkey

Abstract Black kites of the nominal subspecies Milvus migrans migrans breed in Europe and winter regularly in sub-Saharan Africa and the Middle East. As a new phenomenon, black kites with morphological characteristics of the subspecies Milvus migrans lineatus are observed in Europe. Based on observations of black kites in winter 2020/2021 summarized in this paper, based on other recent reports about wintering black kites in Europe and based on juvenile black kite tagged on Crete and tracked for two years, we conclude that hundreds to thousands of black kites are now regularly wintering in south of Europe, and in smaller numbers in other parts of Europe as well as in northern Africa. The growing number of wintering black kites in Europe is apparently caused by members of the population from a hybrid zone between M. m. migrans and M. m. lineatus breeding east of the Urals, i.e. from the area of the European part of Russia. This is consistent with the hypothesis of the spreading of M. m. lineatus and a subsequent hybridization zone between M. m. migrans and M. m. lineatus in a westerly direction from Siberia across continental Europe. Moreover, two black kites found dead on Crete were attributed to M. m. lineatus and M. m. migrans by cytochrome B gene sequence analyses. The juvenile black kite with lineatus features tagged on Crete and telemetrically tracked during the next two years moved to the south-western part of Russia during the next two summers, but did not breed. It spent the following two winters at the same landfill in south-western Turkey. It seems that an adaptation to food sources provided by municipal waste landfills is important for black kites wintering in Europe, the Middle East and Morocco. Highlights • Hundreds to thousands of black kites are now regularly wintering in Europe. • The growing number of wintering black kites is caused by birds from a hybrid zone between Milvus migrans migrans and M. m. lineatus in eastern Europe. • Municipal waste landfills are important as food sources for black kites wintering in Europe.


Introduction
Black kites of the nominal subspecies Milvus migrans migrans (Boddaert 1783) (western black kite) breed in Europe and winter regularly in sub-Saharan Africa and the Middle East (Ferguson-Lees & Christie 2001;Panuccio et al. 2013;Literák et al. 2020;Ovčiariková et al. 2020 Skyrpan et al. 2021). Firstly, Corso (2002) published observations of black kites with lineatus features (now referred to as eastern black kites) in Italy at the Strait of Messina. Black kites with lineatus features were lately observed in Zagreb, Croatia, and in Zhornyska, Lviv Region, Ukraine (Kralj & Barišić 2013;Skyrpan and Literak 2019). Dozens of black kites with lineatus features were observed wintering on Crete in January 2020 (Panter et al. 2020). Forsman (2016) mentioned that black kites with features of lineatus have increased in Europe during the past two decades. In recent years, there has been a substantial increase in the number of sightings of black kites with lineatus features in the whole Europe (Skyrpan et al. 2021). Furthermore, it appears that the emergence of black kites with lineatus features in Europe coincides with a number of observations of wintering black kites in Georgia, Turkey, and the whole of southern Europe (Sunyer & Viñuela 1996;Tsvelykh & Panyushkin 2002;Sarà 2003;Biricik & Karakaș 2011;Molina et al. 2012;Palomino et al. 2012;Abuladze 2013;Mayordomo et al. 2015;Literák et al. 2017;Panter et al. 2020;Skyrpan et al. 2021).
Hybrids between M. m. migrans and M. m. lineatus are featured in a review of avian hybrids throughout the world (McCarthy 2006) based on weak references from Sibley and Monroe (1990). Forsman (2003Forsman ( , 2016 stated that a typical adult lineatus is easily distinguished from a typical adult migrans; however, a great deal of overlap in morphological characteristics is present between these two subspecies. All black kites with lineatus features in Europe should be considered hybrids between M. m. migrans and M. m. lineatus, as pure M. m. lineatus individuals only occur in east Siberia and Japan (Andreyenkova et al. 2021). Previous research has determined the western Siberian black kite population to more or less comprise migrans × lineatus hybrid birds (Stepanyan 1990;Karyakin 2017). The westward expansion of M. m. lineatus has increased since the 1990s owing to a drop in the numbers of M. m. migrans, with lineatus features apparently rapidly introgressing the European subspecies over the vast territory between Altai and the Urals (Karyakin 2017;Andreyenkova et al. 2021 (Skyrpan et al. 2021).
The aim of this study, following recent works on the increasing number of wintering black kites in Europe (Literák et al. 2017;Panter et al. 2020;Skyrpan et al. 2021), is: (a) to estimate the total number of wintering kites in Europe at present and to define the areas with the highest density of wintering kites; (b) to characterize their subspecies status; and (c) using data from a telemetrically tracked black kite having some features of M. m. lineatus wintering on Crete and in Turkey, to characterize the behavioural ecology of this bird during wintering and during the following summer period.

Period of black kite wintering in Europe
Based on data from the autumn and spring migrations of M. m. migrans reviewed in detail by Panuccio et al. (2013) and newly summarized for key flyways of black kites between Europe and Africa in the Strait of Gibraltar, Spain; Batumi, Georgia; and Northern Valleys, Israel, by Onrubia and Martín (2021), we consider all observations of black kites in the period from November until January as observations of wintering birds out of the migration period of M. m. migrans.
Black kites winter in small numbers in the Czech Republic and Slovakia and use communal roosting places with red kites (Milvus milvus) ). In the Czech Republic and Slovakia, a regular census of the number of wintering red kites has been organized at communal roosting places. In our study, black kites observed at communal roosting places of red kites were recorded in the Czech Republic and Slovakia in the period from December 2020 to February 2021.
In some cases, black kite sightings in the surveyed databases were supplemented by photo documentation. In this photo documentation, we evaluated 1272 I. Literák et al. cases of birds in which it was possible to find morphological features of the subspecies lineatus. To create an overview of wintering birds with lineatus features, we used also records of these birds published recently in Skyrpan et al. (2021). Finally, we also used reports of black kites with lineatus features from winter 2019/2020 and 2021/2022, which were sent directly to us by local field ornithologists. All data of black kites wintering in Europe and the northern coast of Africa were processed and visualized using ArcGIS Pro (Esri, Redlands, CA, USA) and QGIS (www.qgis.org) geographic information software packages.

Telemetry tracking
Over a three-day period in January 2020, 157 kites were recorded at the surveyed landfill sites on Crete, Greece (Panter et al. 2020). Some 68 black kites, many of which had features of M. m. lineatus, two red kites (Milvus milvus) and a hybrid red kite × black kite were observed in Arkadi landfill. About two months later, on 2 April 2020, dozens of birds of various species were found to have died suddenly at the Arkadi landfill. They were poisoned by a toxic substance that travelled from the landfill to the birds' water source. The affected birds became immobile and died in convulsions (https://www. rethemnosnews.gr/rethymno/631408_xafnikosthanatos-gia-dekades-agria-poylia-gyro-apo-tonhyta-amarioy, accessed 30 April 2021). Some birds, including one black kite, were rescued. This rescued juvenile black kite (2cy) was fitted with a 20 g OrniTrack-20 (solar powered GPS-GSM/GPRS tracker, Ornitela, Lithuania, www.ornitela.com) on 10 April 2020 and released back in the wild. As this bird had some features of M. m. lineatus (pale/bluish cere and legs, and pronounced dark eye mask), we supposed it to be a black kite originating from a hybrid zone between M. m. migrans and M. m. lineatus (Figure 1). The bird was tracked until 8 January 2022 when the logger apparently failed and no more data were transmitted.
The logger was fitted to the bird's back using wing harnesses consisting of two loops of 6 mm Teflon ribbon that encircled the body around the base of the wings and joined in front of the breastbone (Thaxler et al. 2014). GPS positions were collected usually as one position fixed per 15 min. and sent as text messages by local mobile operators to Ornitela Centre in Lithuania where they were saved and archived. The obtained dataset was then analysed using ArcGIS Pro and QGIS.

Wintering, migration and stopovers
Spring and autumn migrations are part of annual movements that separate the winter and summer periods. We describe the beginning of those migrations as a day when a bird left the winter/summer area and flew north/south without returning in consecutive days. The end is defined as a day when a bird reached the summer or winter destination without continuing on its migration to the north or south. During both migrations, birds tend to use stopovers, defined as a day with less than 50 km of a directed flight (Literák et al. 2022). Winter home range sizes were calculated using the 95% kernel density estimate (KDE95) from locations obtained during winter period. To analyse the area requirements, we calculated KDE for each winter separately. To visualize the wintering of the tagged bird in Turkey, we used cumulative KDE95 values calculated from positions obtained during the second and third winters, for simplicity, as the bird used the same areas in an identical manner during its second and third winter. In this study, we did not calculate the size of a summer home range. To analyse the location of night roosts, we selected one last recorded location from each day (at 20 -22 h.; UTC+3; Coordinated Universal Time). To compare the latitude of winter and summer areas used by the tagged bird between years of its life span, we defined checkpoints W1, W2, W3 and S1, S2 as night positions where the bird stayed on 31 January and 30 June, respectively, in subsequent years after tagging.

Number of black kites wintering in 2020/2021 in Europe and Morocco
By direct observation or using databases, we registered 1104 observations of black kites in 228 reports in the period from 1 November 2020 to 31 January 2021 (Supplemental material Table S1; Figure 2). The distribution of observations was uneven both geographically and temporally. Most observations related to the Iberian Peninsula. Smaller numbers of observations were made in the south of France, in the Netherlands, in central and south-eastern Europe and in Morocco. Observations were rare in northern Europe (southern Sweden). A total of 400 birds, the largest number recorded at one time in one location, were recorded in Spain near the city of Córdoba on 14 November 2020. Dozens of wintering birds were observed at other Spanish locations in November 2020 and January 2021. Total numbers of observations of black kites in November and December 2020, and January 2021, were 734 (72 reports), 88 (80 reports), and 282 (76 reports), respectively. , and data from a recent paper depicting observations of black kites with lineatus features (Panter et al. 2020;Skyrpan et al. 2021) and four further observations of black kites with lineatus features (see Table I) (green circles). The cluster of circles in Italy does not represent true positions but the occurrence of wintering black kites in Italy, because exact locations were not available in www.ornitho.it.

Telemetry tracking of a tagged black kite
Beside direct observations and data obtained from online databases, we tagged one rescued black kite with features of M. m. lineatus on Crete, which we monitored from 10 April 2020 to 8 January 2022 (Figures 4 and 5). After tagging and release, the bird stayed on Crete where it dwelled and roosted mainly near a landfill and close to a small artificial water reservoir ( Figure 6; Table II). It used a relatively small area of only 3.2 km 2 (kernel density estimate 95%). On 15 May 2020, it began its spring migration to its summer ground in western Russia near Bryansk (Figure 4; Table III).
After the summer period, the tagged bird began its longest autumn migration, lasting 79 days with six stopovers, where it stopped for 46 days (Table  III). In comparison to the previous winter, it changed its destination and flew to winter in south-west Turkey, where it again dwelled and roosted near an area of another landfill, while regularly staying also near Koca Çay River (Figure 7). During wintering in Turkey, it occupied a small area of 3.0 km 2 and roosted exclusively in the vicinity of the landfill (Table II). The next summer, the bird again changed its destination. It flew over 600 km farther north than in the previous year and spent the summer near Volokolamsk, Russia (Figures 4 and 5).
On 3 September 2021, the bird left the summer ground and migrated to Turkey for the winter (Table  II), where it used the same place as the previous winter, in an identical manner. It used an area of 3.6 km 2 and roosted mainly in the vicinity of the landfill while, again, also regularly staying near Koca Çay River. We received the last coordinates on 8 January 2022, while the bird was wintering in Turkey for the second time. The cause of the loss of signal remains unknown.

Growing number of black kites wintering in Europe
Recently, black kites have commonly wintered in Spain, and sometimes dozens to hundreds of black kites have been observed in winter foraging on landfills Palomino 2012;Mayordomo et al. 2015). It seems that wintering

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I. Literák et al. of black kites in Spain is now much more common than previously (Franco & Amores 1980;Sunyer & Viñuela 1996). Similarly, in Portugal, the occurrence of black kites in December and January formerly was considered very rare (Catry et al. 2010). Even if black kites were observed to winter in continental Greece in the past (Makatsch 1948), it seems that the dozens of wintering black kites in Greece represent a new phenomenon (Literák et al. 2017). During a study made by car transects in January 2009 and January 2010, a total of eight black kites were reported, one in Sicily and seven in Crete (Panuccio et al. 2019) Winter observations of black kites were rare in the tripoint border area of   (Patev 1950;Kumerloeve 1956;Baumgart 1971;Simeonov et al. 1990;Golemanski et al. 2011). In Ukraine, wintering black kites have been observed since 1998 and their number rose to as many as 70 birds in the Danube Delta and Southern Crimea, where they often use communal landfills for foraging (Tsvelykh and Panjuskhin 2002;Domashevsky 2009). These observations coincided in time with observations of wintering black kites in Hungary, where the birds were seen individually wintering during the period 2010-2016 (László Haraszthy, personal communication). Black kites winter regularly but in small numbers also in the south of the European part of Russia (Melnikov & Sokolov 2020). Based on observations in winter 2020/2021, summarized in this paper, and based on recent reports, which document dozens or hundreds of wintering black kites in Spain and Greece Literák et al. 2017;Panter et al. 2020), and based on further European data referenced above, we can conclude that hundreds to thousands of black kites are now regularly wintering in southern Europe, and a smaller number of black kites winter commonly in other parts of Europe as well as in northern Africa.
These wintering areas now appear to be seamlessly following the wintering areas of black kites in Georgia, Turkey, and Israel, where tens of thousands of black kites winter (Shirihai et al. 2000;Abuladze et al. 2011;Biricik & Karakaș 2011;Abuladze 2013) (Figure 1). Black kites always were by far the most numerous wintering raptor species in Georgia, with 3000 to 12,000 individuals wintering in this country (Abuladze et al. 2011;Abuladze 2013). Formerly, black kites were characterized as sporadically wintering in Turkey, and there were records from all regions of Turkey (Kirwan et al. 2008). Recently, a common wintering of black kites was described in south-eastern Anatolia, Turkey, from 2001 to 2010 (Biricik & Karakaș 2011). Most of them were recorded at landfills where household garbage was deposited, and around slaughterhouses where various parts of slaughtered animals were available. In December 2007, more than 1200 (the highest number counted) black kites wintered near
Gaziantep-Oğuzeli. It was estimated that at least 7500 black kites wintered in the area during 2011. Previously, only exceptionally had wintering black kites been observed in the Middle East including Turkey, Syria, and Lebanon. Common observations of wintering black kites in Israel that are in contrast to the past, and some recent observations of wintering black kites in Egypt as well as in Morocco, lend support to this idea (Kumerloeve 1967;Shirahai et al. 2000;Ciach andKruszyk (2010, 2017).

Subspecies status of black kites wintering in Europe
When observing dozens of wintering black kites in mainland Greece during winters 2002Greece during winters /2003Greece during winters , 2015Greece during winters / 2016Greece during winters and 2016Greece during winters /2017, as no attention was paid to the subspecies status, the observed black kites were considered to belong to the nominal subspecies M. m. migrans (Literák et al. 2017 (Kumar et al. 2020;Literák et al. 2022). The black kite wintering population has increased dramatically in the northern Negev region of Israel over the past two decades, due to using landfills as reliable food source (Berkowitz et al. 2018). Unfortunately, the subspecies status was not determined for many black kites observed at a municipal landfill in Rome (De Giacomo & Guerrieri 2008). A number of black kites apparently belonging to M. m. migrans were tagged in Europe in a breeding season and later tracked to reveal their migration/ dispersal strategy (Sergio et al. 2014;Ovčiariková et al. 2020). We did not find any note/case of these tagged black kites wintering in Europe; rather, they all wintered in sub-Saharan Africa. Some of them stayed in Africa longer in the period of their first or even second year, and they usually bred in Europe when they were 3-6 years old (Sergio et al. 2014;Ovčiariková et al. 2020). We can conclude that the growing number of wintering black kites in Europe is basically caused by members of the population from a hybrid zone between M. m. migrans × M. m. lineatus breeding in eastern Europe east of the Urals, i.e. more or less from the area of the European part of Russia. This conclusion is supported by the finding of a dead black kite on Crete, which we showed to possess the CytB haplotype B6. Haplotype B6 belongs to the haplogroup B, which has been recently attributed to M. m. lineatus (Andreyenkova et al. 2021).
Pure black kites Milvus m. migrans breeding in Europe from the Iberian Peninsula to eastern Ukraine still winter in sub-Saharan Africa (Sergio et al. 2014;Ovčiariková et al. 2020;Literák et al. 2021). Hence, our study does not seem to support a previous idea that a growing number of wintering black kites (considered M. m. migrans) in Europe coincides with climate warming in Europe and with negative changes in sub-Saharan Africa (e.g. an increasing density of human population and extensive use of pesticides in Africa), even if it was reported that the breeding behaviour of black kites (Milvus m. migrans) in Italy responded quickly to climate warming, and despite the fact that aerial and ground spraying of insecticides in Africa often wipes out the food resource of black kites and indirectly kills many individuals (Sergio 2003;Panuccio et al. 2013;Literák et al. 2017).
According to current estimates, 28,000-270,000 pairs of black kites nest in the European part of Russia, which allegedly represents 35-45% of black kites nesting in the whole of Europe (Melnikov & Sokolov 2020). The subspecies status of these birds remains unclear, but it can be expected that from the east (the Urals) to the western border of Russia, the proportion of birds in the hybrid population will decrease (see also Andreyenkova et al. 2021).

Life history of the tracked black kite with lineatus features
We tagged the black kite with features of M. m. lineatus that was rescued while wintering in Crete. Here, the bird dwelled most of the time in the vicinity of a landfill and water body, where it roosted and foraged. Identical behaviour was observed even when the bird changed its destination, wintering in Turkey in following two winters. Such behaviour has been recently observed in many black kites with morphological features of M. m. lineatus (Literák et al. 2017;Panter et al. 2020).
An adult black kite with lineatus features was captured, ringed, and tagged at the Dudaim landfill near Be'er Sheva in southern Israel (Daniel Berkowitz, personal communication). This bird was later observed at a landfill near the village of Nema in the Kirov Region (the European part of Russia west of the Urals) (Karyakin et al. 2018). These findings underline the role of landfills as roosting and foraging places for black kites with features of lineatus. Six recoveries of ringed black kites published recently show a connection between black kites originating from the European part of Russia and those wintering in Israel (Franks et al. 2022). We suppose these ringed black kites originated from the same hybrid zone between M. m. migrans × M. m. lineatus as did our tagged bird.
Black kites breeding in Europe, supposedly pure M. m. migrans, migrate through different corridors to reach their winter ground in sub-Saharan Africa (Sergio et al. 2014;Ovčiariková et al. 2020;Literák et al. 2021). Birds from Spain migrate though the Strait of Gibraltar to winter in north-west Africa (Sergio et al. 2014). Birds from central Europe migrate through various corridors and some birds cross through Greek islands or Turkey on their autumn migration, but do not stop there and continue south to winter in Africa (Lucia et al. 2011;Ovčiariková et al. 2020). Our bird chose the corridor following the west coast of the Black Sea during all its migrations to and from Turkey.
During the first year of monitoring it spent a summer in lower latitudes then in the following summer. A similar movement pattern was observed in black kites M. m. migrants originating from the population in central Europe, where young birds left their natal area and flew to winter in Africa . In subsequent years, birds tended to spend summer closer to the natal area until they reached maturity and spent the summer period back in their natal area. Such behaviour has also been described in other raptors, such as the short-toed snake eagle Circaetus gallicus and the European honey buzzard Pernis apivorus, migrating from Europe to Africa and back Vansteelant 2019). Interestingly, different behaviour was observed in black kites originating from Siberia, where the birds tend to spend each summer period at a similar latitude to their natal area (Literák et al. 2022).
Based on the ecology of black kites from different areas, and the tagged bird's choice of migration corridor, to reach the winter and summer destination, we can assume it originated in the area of western Russia near Volokolamsk or possibly even from farther north near Cherepovets, as the bird visited this area on its last spring migration before spending the summer in Volokolamsk. Since black kites rarely migrate alone during autumn migration, we can assume that more birds from those areas are choosing Crete or Turkey as their winter destination (Panuccio et al. 2013). In contrast, black kites that migrate through Georgia around the eastern coast of the Black Sea to winter in Israel might originate from more eastern parts of European Russia (Panuccio et al. 2013;Karyakin et al. 2018). Such findings may reveal the origin of the increasing numbers of black kites wintering in southern Europe and present further evidence of the westward shift and expansion of the hybridization zone between M. m. migrans × M. m. lineatus (Skyrpan et al. 2021).