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Turkish Journal of Zoology Turk J Zool (2015) 39: 300-307 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1401-64

Nest-site selection, breeding success, and diet of white-tailed eagles (Haliaeetus albicilla) in the Danube Delta, Romania

1,2, 3 3 3 1,2 3 Attila D. SÁNDOR *, Vasile ALEXE , Mihai MARINOV , Alexandru DOROŞENCU , Cristian DOMȘA , Botond J. KISS 1 Department of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, Romania 2 NaturalNet LTD, Capusu Mare, Cluj, Romania 3 Danube Delta National Institute for Research and Development, Tulcea, Romania

Received: 26.01.2014 Accepted: 01.06.2014 Published Online: 27.02.2015 Printed: 27.03.2015

Abstract: The white-tailed eagle is a flagship of wetland conservation throughout ; thus, general conservation efforts targeting this species can provide effective protection for most species occupying similar habitats. The species’ breeding ecology is well known in northern and western Europe; however, the locally important Danube Delta population has scarcely been studied. Here, the eagles primarily select tall for nesting (mostly willow and white poplar), with most nests built above 15 m. The breeding population is geographically concentrated in the northern and northwestern parts of the delta, most probably because of available nest sites in less- disturbed areas. The population has low breeding success, with nests falling and low productivity of breeding pairs (0.67 fledglings/pair). The diet is diverse, with birds, fish, and mammals being preyed upon. Wildfowl and large cyprinids contribute most to the diet, while corvids and mammals are locally important. Most prey species are common residents, occurring abundantly in the area; thus, food scarcity does not seem to limit the eagle population. To maintain the white-tailed eagle population in the Danube Delta, special effort should be taken for maintaining proper (large) nesting trees or to provide artificial nests in suitable areas.

Key words: White-tailed eagle, Haliaeetus albicilla, nest-site, breeding, diet, Danube Delta, Romania

1. Introduction concentrated in the northern part of the continent, with The white-tailed eagle (Haliaeetus albicilla) is an important the largest populations in Norway and Russia, while conservation symbol and umbrella species, being on the populations from central and eastern Europe are much highest level of the trophic pyramid in most wetland smaller, reaching 700 breeding pairs (Bauer and Berthold, ecosystems in Europe. Moreover, it is a good indicator 1996; Horváth, 2007; Probst and Gáborik, 2011). Central species for ecosystem processes occurring in its habitats and eastern Europe, however, are important as wintering (Helander et al., 2008). Hence, general conservation efforts territory for the aforementioned northern populations targeting this species can provide effective protection for (Probst and Gáborik, 2011). In Romania, 37–42 pairs are most species occupying similar habitats. By providing breeding, with the Danube Delta population of 20–22 conservation measures for such an umbrella species, pairs being the most important locally (Munteanu, 2009). species in the whole trophic chain will benefit, together There are 3 main factors governing population with other species sharing the same habitats and ecological dynamics of large-bodied carnivores: access to nest sites, processes therein. food availability, and predation (Newton, 2010). Access to The white-tailed eagle has a wide European distribution proper nest support has been proven to be a main limiting range in northern, central, and eastern Europe, with factor of population size for most large predatory birds a total area covered by 2.76 million km2, while the in general (Katzner et al., 2003; Newton, 2010). This is European population is between 5000 and 6600 breeding especially important for white-tailed eagles, as their nests pairs (BirdLife International, 2004). After a long-lasting are huge structures. A specific situation is the case of re- decline (Cramp, 1980), its population trend turned into colonization efforts in areas where the species became an increase in the last few decades (BirdLife International, scarce or extinct in the past (Horváth, 2007; Rajchard et al., 2004). Most of the European breeding population is 2010); thus, every conservation plan should consider this * Correspondence: [email protected] 300 SÁNDOR et al. / Turk J Zool issue. The white-tailed eagle is a wide-spectrum generalist cover reaching 92%, and less than 5% of the area lacks in terms of food, with fish, waterbirds, and medium- water cover. Forest cover is 6% and a considerable part sized mammals being the main diet components (Cramp, of it is seasonally flooded softwood. Continental-type 1980). However, the shares of these 3 most important hardwood forests are located on Letea and Caraorman components may vary locally (Bezzel, 1985; Bauer and islands, covering less than 1% of the whole delta. The Berthold, 1996; Nadjafzadeh et al., 2013). Food availability climate is continental, with mean temperatures of –1.8 °C is crucial in the period of nestling development, thus in January and 22.2 °C in August. Most lakes and slow- limiting nesting success. Predation (in the case of this flowing branches or channels freeze in winter, but ice cover species, illegal killing/hunting) may limit populations with lasts for short periods. The yearly average precipitation is low reproduction rates, and even low extraction rates of 350–380 mm (mostly in the form of rain in spring and individuals may hinder any conservation effort in a given autumn) and evaporation is about 1000 mm/year, with area (Newton, 2010). spontaneous salinization of humid soils (Gâştescu and The white-tailed eagle is a flagship species of Ştiucă, 2006). wetland conservation all over Europe, with important 2.2. Nest survey numbers of breeding pairs located inside protected areas The area was surveyed from a motorboat in the nonbreeding (Albuquerque et al., 2013). However, as with most large season for the locations of nests (large structures, built carnivores, it is still conservation dependent and protected usually on solitary or the tallest trees, highly visible from in most range states (BirdLife International, 2004). Food a considerable distance). When found, a number of data selection, breeding ecology, and population dynamics are were collected from each nest (nesting species, nest well known in its northern range states—especially for height, clutch status). Nest height was measured with a populations breeding on shores—and in central Europe tape, from the nest-top to the ground or water level, with (Sulkava et al., 1997; Horváth, 2003; van Rijn et al., 2010; 0.5-m accuracy. All known nests were visited several times Whitfield et al., 2013; for a comprehensive summary see to collect data on occupancy, laying dates, and nesting Cramp, 1980, or a more recent account in Nadjafzadeh, success. Close inspection of active nests was performed in 2011). In contrast, there are only a few publications in April or May, to avoid unnecessary disturbance during a southeastern Europe (none specifically from Romania), critical period of nesting. Some of the nests lack nesting with only anecdotal information published for the Danube success data, as after the spring floods retreat (mid-May), Delta population (Dombrowski, 1910; Puşcariu, 1968; access is restricted in several areas of the delta, thus Klemm, 1973; Marinov and Kiss, 1991; Pocora, 2010). As preventing a close inspection of nests in these areas. modern conservation measures targeting such a species 2.3. Diet are impossible without proper knowledge of its population Pellets and prey remains were collected from the nests figures or ecological requirements, there is a current and below the nesting trees. All collections were stored need for information based on locally collected data. Our individually and analyzed separately. The contents of each paper presents new information on population structure, pellet were ascertained if possible, but most pellets were nesting, and food selection, comparing the data with broken, and the number of individuals per pellet was regional information from the past, with a time span of therefore not calculated. For the identification of prey nearly a century. groups we used all available material, while the skulls, mandibles, humeri, and tibiae of mammals, the feathers, 2. Materials and methods humeri, and tarsometatarsi of birds, and species-specific 2.1. Study site bones of fish were used for species-level identification. The study site is the Danube Delta Biosphere Reserve Mammal and bird remains were compared to the reference (DDBR), a wetland complex lying on the western coast of collection of SDA, while fish remains were compared using the Black Sea. It is a protected site, with most of its area identification guides (Radu, 2005; Otel, 2007). Paired covered by freshwater or brackish wetlands dominated elements for each taxon were separated, and the largest by reed (Phragmites australis), being the second largest number of these was considered the minimum number of delta in Europe. Among wetlands there are a number of individuals (MNI) per taxon per sample. Original animal sandbanks, 2 largely covered by forests, while the rest biomass was calculated by multiplying the number of are grasslands. The total area of the DDBR is 5050 km2, individuals of each species found in pellets/remains by bordered by arable lands to the north (Ukraine), the Black the mean body mass of the specific prey group/species Sea to the east, agricultural areas interspersed with steppes collected from the region, or extracted from reference and small rocky hills to the west and southwest, and by works (Cramp (1980) for birds and Otel (2007) for fish). a brackish lagoon system to the south. Most habitats are We estimated the trophic dimensions of the ecological characterized by the presence of freshwater, with wetland niches (niche breadth) by using Levins’ (1968) equation:

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2 D = 1/Σpi , where pi is the proportion of prey in different destruction (27.3%) caused by natural causes (tree fall, categories (mainly species). Diversity of trophic spectrum deterioration caused by snow or windstorms). All nests was estimated using the formula of Shannon and Wiener: were built on trees, with most being built at considerable

H = –Σpi lnpi, where pi is the proportion of any given prey heights, with the average height being 15.67 m (min = 4 m, species (Jankowiak and Tryjanowski, 2013). max = 23 m) and nearly two-thirds were built at heights above 16 m (Table 2). 3. Results White-tailed eagles from the DDBR build their nests 3.1. Nesting ecology mostly on tall trees, thus favoring large willows (Salix spp., The study covers 3 breeding seasons (2009–2011); in this 70.8%), native white poplar ( alba, 20.8%), and period, 72 individual nests were visited at least once (see (white) poplar (Populus spp. X, 4.1%), with the rest the Figure for the study area and nest locations of active being built on common alder (Alnus glutinosa, 4.1%) (see nests during the study period). Most nests were found in also Table 3). The nests were positioned in most cases in a the northern half of the Danube Delta (north to the Sulina fork of the tree trunk (57%), but also on lateral branches or branch). From the visited nests, only 33 individual nests on logs of broken branches. were actively used during the studied period, with 19–20 Breeding started in early January, with the first chicks active nests/year (Table 1). These nests were followed in hatched in February. As some nests were inaccessible the breeding seasons, in the period from egg-laying to due to the fragility of the support trees, we managed to fledging (January–July). collect detailed nesting data only for 59 clutches (HPa) in The nest failure rate is fairly high, with 52% of the 3 years. The overall success rate was JZm = 0.67 (nestlings/ studied nests failing to produce any young, with obvious nest initiating pair), with a productivity of JZm = 1.33– cases known only for 11 nests. The most common cause 1.45 nestling/successful pair (Table 1). There were no for nest desertion was human intrusion (54.5%) or nest differences in reproductive rate among years, this being

Figure. Map of the study area with the locations of actively used white-tailed eagle nests in the years 2009–2011.

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Table 1. Yearly distribution of studied nests and breeding success of white-tailed eagle in the Danube Delta.

Year No. of nests visited Active (HPa) Successful (HPm) Mean nest success (JZm) 2009 34 20 11 1.45 2010 42 20 9 1.33 2011 45 19 9 1.33

Table 2. Height distribution of white-tailed eagle nests in the Danube Delta (n = 36).

Height (m) 4–5 6–7 8–9 10–11 12–13 14–15 16–17 18–19 20–21 22–23 No. nests 2 2 2 1 3 4 6 12 2 2

Table 3. Nest tree selection of white-tailed eagle nests in the Danube Delta (n = 72).

White poplar Hybrid (white) poplar Common alder Nest support tree species Willow (Salix spp.) (Populus alba) (Populus spp. X) (Alnus glutinosa) No. nests 51 15 3 3 Active nests 30 9 1 1 Nests destroyed 19 3 2 2 constant in the study period. We were not able to find half of the cases, with only 2 species occurring regularly any relationship between nest location (nest supporting in the diet (muskrat, Ondatra zibethicus, and European tree species, nest height, or geographical location) and hare, Lepus europaeus). Their share, however, is important breeding success. We estimate that we managed to find in terms of biomass (7%). The occurrence of raccoon dog the nests of ca. 80% of existing breeding pairs; thus, the (Nyctereutes procyonoides), harbor porpoise (Phocoena estimated breeding population does not exceed 25 pairs (a phocoena), and domestic sheep (Ovis aries) was certainly breeding density of 0.048 pairs/km2). related to scavenging; thus, we excluded them from 3.2. Trophic analysis biomass analyses as there is no certainty that the whole A total of 260 prey items belonging to a minimum of 38 body was consumed. prey species were identified from 21 batches collected from 17 nests (see Table 4.). Diet niche-breadth was D = 4.41, 4. Discussion while prey diversity was H = 0.55. The most important White-tailed eagles breeding in the Danube Delta diet component (in terms of individual numbers, 50%; exclusively used trees for breeding during the study occurrences, 84.7%; biomass, 55.25%) was the group of period. Nesting on soil or rocks was not found in the recent birds. Altogether, 23 bird species were identified in the population, as has been described in the past (Dombrowski, diet, with birds using wetlands as their main habitat being 1910; Klemm, 1973). Nest position showed an increased the most important (41.1% MNI and 51.9% of biomass). mean height compared to data from the early (3–4 m in Other bird species found to be important prey locally were Dombrowski, 1910) or mid-20th (2–3 m in Linția, 1954) crows (Corvus spp.) and the magpie (Pica pica), which century. A more recent survey found similar nest heights were found in only 3 nests, there constituting 30% of prey. in 1971 (Klemm, 1973); thus, this is not a new tendency. Fish remains were found in 76% of the collections (37.7% The practice of building nests in taller trees may have a of biomass consumed), large-sized individuals in most close connection with increased traffic inside the delta, cases. Only 7 species were individually recognizable, with started by aggressive polder creation in the early 1960s, common carp (Cyprinus carpio), Prussian carp (Carassius and continued by uncontrolled tourism development in gibelio), and Northern pike (Esox lucius) being found in the 1990s (Gâştescu and Ştiucă, 2006). This phenomenon most individual batches. Mammals were found in less than is similar to the situation found in most surveys in central

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Table 4. Food composition of white-tailed eagle expressed as frequency of occurrence in remains/pellets, relative frequency of occurrence in all prey, and the percentage of fresh biomass.

Prey species Occurrence (%) Relative frequency (%) Biomass (%) Esox lucius 42.86 6.15 3.41 Carassius gibelio 33.33 8.08 2.68 Cyprinus carpio 57.14 11.54 19.18 Abramis brama 9.52 1.15 0.77 Cyprinidae indet. 42.86 10.00 7.76 Silurus glanis 9.52 0.77 0.21 Sander lucioperca 4.76 0.38 0.17 Perca fluviatilis 4.76 0.38 0.13 Pisces indet. 19.05 6.15 3.41 Pisces Total 76.19 44.62 37.72 Phasianus colchicus 4.76 0.38 0.42 Anser anser 19.05 3.08 11.25 Anser albifrons 9.52 0.77 2.13 Cygnus olor 14.29 1.15 6.39 Anas platyrhynchos 33.33 3.08 3.75 Anas strepera 14.29 2.69 2.28 Aythya ferina 28.57 2.31 2.38 Aythya nyroca 4.76 0.38 0.32 Anatidae indet. 28.57 3.46 3.07 Phalacrocorax carbo 9.52 0.77 1.96 Phalacrocorax pygmeus 28.57 3.08 2.32 Ardea cinerea 14.29 1.15 1.92 Botaurus stellaris 4.76 0.38 0.53 Podiceps nigricollis 9.52 0.77 0.26 Podiceps grisegena 9.52 0.77 0.70 Podiceps cristatus 23.81 3.08 3.24 Tachybaptus ruficollis 23.81 3.46 0.54 Charadriiformes indet. 4.76 0.38 0.05 Gallinula chloropus 9.52 0.77 0.27 Fulica atra 57.14 9.62 8.52 Columba palumbus 14.29 1.92 0.96 Coracias garrulus 4.76 0.38 0.06 Corvus cornix 14.29 1.54 0.87 Corvus frugilegus 14.29 1.15 0.40 Pica pica 23.81 2.31 0.56 Sturnus vulgaris 9.52 1.15 0.10 Aves Total 85.71 50.00 55.25 Ondatra zibethicus 19.05 1.92 3.20 Lepus europaeus 14.29 1.15 3.84 Nyctereutes procyonoides 4.76 0.38 0.00 Phocoena phocoena 4.76 0.77 0.00 Ovis aries 14.29 1.15 0.00 Mammalia Total 47.62 5.38 7.03

304 SÁNDOR et al. / Turk J Zool or eastern Europe, with low-positioned nests disappearing prey species are organisms related to wetland habitats, totally (Horváth and Pintér, 2005; Radović and Mikuska, with the only exception being the European hare. Bird 2009; Vrezec et al., 2009; Rajchard et al., 2010). prey is diverse, with a minimum of 25 species used, White-tailed eagles select nest sites preferentially and has the highest contribution to the wide trophic on large trees, without a specific tree species preference, niche found herein. Waterbirds make the largest and usually using tree stands at short distances from favorite quantitatively most important component of the diet, feeding areas (Cramp, 1980). In the case of the Danube with Anatidae and Eurasian coot (Fulica atra) being the Delta, there are 3 main types of forested areas, with Salix most important food source in the Danube Delta. All bird spp.-dominated softwood (interspersed with native white species discovered in the diet are commonly occurring in and black poplars, Populus nigra) forests (ca. 75%), followed the area, with all but one species being abundant breeders by commercial plantations of hybrid poplars (ca. 23%). in the delta. The only exception, the greater white-fronted There are 2 hardwood forests inside DDBR, composed goose (Anser albifrons), is a common passage migrant mainly of Quercus spp. (covering less than 1% of forested and wintering species, occurring in 10,000s in autumn territory); however, these stands grow on sandy substrate, and spring (Oţel et al., 2000). This situation is typical for thus most trees do not reach the height of neighboring most white-tailed eagle populations sampled inland, with willows or poplars. Even in these forests, all white-tailed similar results presented for northern (Finland: Sulkava eagle nests are placed in poplars. In consequence, eagles et al., 1997), western (Scotland: Watson et al. 1992; the have no preferences towards selected tree species in our Netherlands: van Rijn et al., 2010), central, and eastern area, similar to populations studied in Hungary (Horváth Europe (: Bauer and Berthold, 1996, Dittberner and Pintér, 2005) or Croatia (Radović and Mikuska, 2009). and Dittberner, 1986; Hungary: Horváth, 2003; Estonia: Placing a nest in a softwood tree poses a risk of short life Randla and Tammur, 1996). Our results are most similar expectancy for the nest. Most nests in our study area last to the situation from Oder Valley (Dittberner and only a few years, with high turnover rate especially in the Dittberner, 1986) and Hungary (Horváth, 2003), as both case of nests in Salix stands. Although our study period of these populations rely principally on Eurasian coot was too short to estimate the average survival period of and wildfowl. Wildfowl are important for other, more nests as structures, most known nests on willows lasted distant populations also, as nearly 80% of eagle prey fewer than 5 years in the Danube Delta. Based on our brought to nests near Lake Baikal consisted of Anatidae survey, there is a continuous lack of suitable, good-quality (Mlíkovský, 2009). There are coastal breeding populations nest sites, proven by the fact that eagles occupy artificial that tend to exploit similar percentages of birds, but in nests very readily if provided (Kiss et al., 2013). their case the importance of colonial seabirds is high (e.g., Nest distribution inside the Danube Delta does not western Scotland, Whitfield et al., 2013) or they rely on show a random distribution; most nests were grouped in one superabundant prey species (e.g., northern Russia, a distinct region in the northwestern part of the DDBR where the main prey was the common eider Somateria (see the Figure). This distribution was not linked to the mollissima (Koryakin and Boyko, 2005)). White-tailed distribution of forested areas in general, but most likely eagles breeding in other coastal areas, however, prefer fish, represents the availability of nesting trees in undisturbed with up to 90% in Greenland (Wille and Kampp, 1983), areas. Most trees holding nests were located in perimeter but fish are also overwhelmingly found in the diets of areas which have constant water cover, and are located at eagles from Lithuania (Dementavičius, 2004), far-eastern considerable distances from roads or navigation routes. Russia (Ganusevich, 1996), Estonia (Tuvi and Vali, 2007), Breeding success of the studied pairs is low, close to the and southern Finland (Sulkava et al., 1997). They usually lowest in comparison to 30 populations from northern prey on large fish species, with most studies presenting or western Europe (see details in Evans et al., 2009), and Cyprinidae as the main prey group (Cramp, 1980). In considerably lower than central European (Randla and the Danube Delta, white-tailed eagles prey preferentially Tammur, 1996;, Horváth and Pintér, 2005; Probst and on medium to large individuals of common and Prussian Gáborik, 2011) or Asian populations (Ganusevich, 1996; carp, followed by medium-sized pikes. These fish species Katzner et al., 2003). However, we are aware that such a are also abundant and compose the bulk of the freshwater short period (3 breeding seasons) may not be enough for fish biomass of the Danube Delta (Oțel, 2007). Mammals wide-reaching conclusions in the case of such a long-lived are preyed upon extensively by certain populations of species. white-tailed eagles, especially in central Europe (Bezzel, The white-tailed eagle is the largest predator in the 1985; Horváth, 2003), but also in the west (Watson et Danube Delta and uses all available food sources. Its al., 1992; van Rijn et al., 2010; Whitfield et al., 2013). We breeding season diet is composed mainly of birds and found 2 species of mammals regularly preyed upon by fish, completed with basically 2 species of mammals. Most eagles. The occurrence of muskrat was expected, as the

305 SÁNDOR et al. / Turk J Zool species is abundant in most suitable areas of the delta, but sites, nest destruction, and low breeding success seem to the occurrence of European hare is rare in the delta, as most be the most important population regulation factors in the of the delta’s area is under constant or periodic water cover. area; in addition, the illegal killing of subadults (Sándor All European hare remains were found in the same area, in AD, unpublished) may contribute to the overall low 2 nests some 1.5 km apart. Both mammal species preyed breeding density of the species in the area. To maintain or upon in our study area have been commonly reported from increase the breeding population of white-tailed eagles in a number of studies, forming important diet components the Danube Delta, the management plan of the area should for this species (e.g., Watson et al., 1992; Mlíkovský, 2009). include special requirements for maintaining proper There were 3 other mammal species occurring in the diet of (large) nesting trees or providing artificial nests in suitable the white-tailed eagle in our study. All 3 occurred only at 1 areas. nest each and most probably belong to scavenging events; thus, their importance is reduced at the population level. Acknowledgments White-tailed eagles in the Danube Delta use large This study was in part financed by DANUBEPARKS. We trees for breeding, and the distribution of breeding pairs thank Bandacu Dan, Iacovici Marcel, Leah Victor, Mihalcea is related to the availability of proper breeding sites. Their Marian, and Voicu Mirel; Achimfiev Constantin, Ipati breeding success is low, mostly caused by nest failure. There Iulian, Isacov Nicu, and Lupu Costel (DDBR); Băcescu are no differences in diet selection among the studied pairs Gheorghe, Cîrpăveche Paul, and Gal Anton (DDNRI); apart from locally important mammals; the eagles select Horváth Zoltán and Fenyősi László (Duna-Dráva National their prey from a wide range of species. Lack of proper nest Park) for their help with data collection.

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