Winter diet and lead poisoning risk of Greater Spotted Eagles Clanga clanga in southeast Spain

ABSTRACT

Capsule: Diet analysis revealed high lead exposure for Greater Spotted Eagles Clanga clanga wintering in southeast Spain.

Aims: To describe the diet composition of the endangered Greater Spotted Eagle in a wintering area located in southeast Spain, and determine lead ammunition exposure through analysis of regurgitated pellets and prey remains.

Methods: Between 2008 and 2018, a total of 26 pellets, 29 prey remains and 10 direct predation observations were collected in El Hondo Natural Park, Spain. All the pellets and 10 prey remains were analysed with X-ray in order to detect metal from ammunition.

Results: Greater Spotted Eagles fed mainly on birds, with 18 different species accounting for 73.1% of prey items and 66.1% of biomass consumed. The most frequent species identified were Common Moorhen Gallinula chloropus (23.1%), rats Rattus spp. (15.4%) and Common Teal Anas crecca (8.9%). Ammunition was detected in 42.3% of regurgitated pellets and in 40.0% of prey remains analysed. Of those containing ammunition, lead shot was found in 63.9% of pellets and 25.0% of prey remains.

Conclusion: High lead shot presence in pellets and prey remains of wintering Greater Spotted Eagles in southeast Spain warns of a high risk of lead poisoning. Factors such as feeding behaviour, the large space–time overlap between the raptor presence and the waterbird hunting season and non-compliance with the ban on the use of lead ammunition are likely contributing to high lead exposure.

Knowledge of behaviour and ecology of migratory raptors along their winter areas is essential to design effective conservation strategies at the global scale (Grande et al. 2009, McClure et al. 2018). Disturbances suffered in winter quarters could compromise the survival and the reproductive success of raptor populations in their breeding areas (Martin et al. 2007, Grande et al. 2009). This could be particularly detrimental to the conservation of endangered species. Raptors are disproportionately more threatened with extinction compared to other avian and non-avian groups, due to their ecology and life-history (McClure et al. 2018). Several factors can cause their populations to decline, including habitat loss, persecution by humans (e.g. shooting and direct poisoning), interactions with human infrastructures (e.g. wind farms, power lines, collision with vehicles), and contamination with toxic chemicals (Donázar et al. 2016).

Poisoning by lead (Pb) is an increasing concern for the conservation of raptors due to negative effects on breeding success (Gil-Sánchez et al. 2018), or direct mortality effects (Mateo et al. 2001, Pain et al. 2019). The most relevant source of lead poisoning in raptors comes from hunting ammunition (García-Fernández 2014). Lead ammunition, as shot or bullet fragments, can be ingested by raptors when they predate or scavenge on game prey that have been shot but not collected by hunters (Fisher et al. 2006). Lead ammunition ingestion has been recorded in many raptor species around the world (see reviews in Pain et al. 2009, 2019) but not all of them are equally exposed to lead. Long-lived species may be critically affected. Deaths attributed to lead poisoning have been recorded in scavenging species such as White-tailed Eagles Haliaeetus albicilla, Steller’s Sea Eagles Haliaeetus pelagicus and Bald Eagles Haliaeetus leucocephalus (Pain et al. 2019).

Both in North America and Europe, hunting of waterfowl during winter is a widespread practice. Estimates provided by the United States Forest and Wildlife Service indicate that 19% of ducks shot by hunters are not recovered (USFWS 1975). Thus, raptors with scavenging habits that winter in wetlands may be highly likely to ingest lead shot present in unrecovered carcasses (Nadjafzadeh et al. 2013). Lead ingestion and poisoning have been documented in several raptor species in Spain (Mateo et al. 1997, 1999, 2001, García-Fernández et al. 2005, Gangoso et al. 2009, Pain et al. 2019, Gil-Sánchez et al. 2018). Regurgitated pellets from Spanish Imperial Eagles Aquila adalberti, Red Kites Milvus milvus and Western Marsh Harriers Circus aeruginosus, which frequently feed on bird carcasses in wetlands during winter, contained a higher presence of lead shot in pellets during the hunting season than outside it (Mateo et al. 1999, 2001, 2007). This was reflected in high blood lead levels, characteristic of clinical lead poisoning (>600 ng/ml) (Pain et al. 1993, 1997, Mateo et al. 1999).

The Greater Spotted Eagle Clanga clanga is a medium-large migratory raptor that breeds in temperate Eurasia and winters in wetlands of south Eurasia and north Africa (Meyburg et al. 2019, Maciorowski et al., 2019). It is listed as an endangered species because it has undergone a moderate decline due to habitat loss and degradation throughout its breeding and wintering ranges, together with the effects of human disturbance and persecution (Våli 2015, BirdLife International 2017). Its hunting behaviour, diet and habitat preferences make it sensitive to lead exposure (Pain et al. 1993), but the evidence is limited to one individual wintering in the Ebro Delta (Spain) that showed a high blood lead concentration of 336 ng/ml (Mateo et al. 2001). Since 2007, El Hondo Natural Park, in southeast Spain, has held a small but stable wintering population of Greater Spotted Eagles (Marco-Tresserras & Pérez-García 2017). In several ponds that are part of this protected area, waterfowl hunting is permitted during winter. Although the use of lead shot in Ramsar sites and other protected wetlands has been banned in Spain since 2001 (Mateo & Kanstrup 2019), verifications of compliance with this regulation have been limited to only a few wetlands (Mateo et al. 2014, Valverde et al. 2019).

This study aims to describe the diet composition of the wintering population of the Greater Spotted Eagle in southeast Spain and analyse the presence of ammunition in regurgitated pellets and prey remains to determine the risk of lead poisoning. This research will allow us to understand the basic ecology and threats faced by this endangered species in one of its wintering areas, in order to improve conservation actions globally. Furthermore, our results will provide an indirect assessment of compliance with the ban on the use of lead shot in wetlands.

Methods

Study area and species

The study was conducted in El Hondo Natural Park, located in the south of Alicante province, Spain (38.17° N 0.75° W). The climate is Mediterranean, with annual mean precipitation of 200–400 mm, mainly in autumn and spring, and average temperatures of 25.5°C in summer (20.4–29.7°C) and 12.6°C in winter (7.4–17.8°C) (State Meteorological Agency AEMET, http://www.aemet.es). El Hondo Natural Park is a protected wetland complex that covers an area of 23.8 km², comprising two main irrigation water reservoirs and several small ponds. The vegetation is composed of sedges, reeds and halophytes. The wetland is surrounded by intensive irrigation crop fields (pomegranates, palms and melons). The two main water reservoirs are exclusively used for water storage, irrigation and wildlife protection, while small water reservoirs are subject to various uses and activities, such as public use for recreation, hunting and fishing activities. Before being a protected area, El Hondo was an important hunting ground for waterfowl, which triggered serious lead poisoning problems in waterfowl in the 1990s (Mateo et al. 1998). Hunting of waterfowl and species control (e.g. Great Cormorant Phalacrocorax carbo) are currently still permitted in some of the small ponds of the park. This protected area is also surrounded by numerous small game grounds, mainly for hunting European Rabbits Oryctolagus cuninculus.

This Natural Park is an important breeding site for endangered species such as Marbled Duck Marmaronetta angustirrostris and White-headed Duck Oxyura leucocephala. In winter, the area is the resting place of thousands of waterbirds such as the Northern Shoveler Spatula clypeata, Common Pochard Aytha ferina, Black-necked Grebe Podiceps nigricollis and Greater Flamingo Phoenicopterus roseus. There is also an important community of wintering raptors including Marsh Harriers, Common Buzzards Buteo buteo, Bonelli's Eagles Aquila fasciata and Booted Eagles Hieraaetus pennatus.

The Greater Spotted Eagle was considered a rarity in Spain in the last century (Barrientos & Bolonio 2002), but in the last decade, a stable winter population of 3–5 birds have become established in eastern and southeastern Spain (Pérez-García et al. 2014, Marco-Tresserras & Pérez-García 2017). Greater Spotted Eagles arrive in early October and leave the area in mid-March. This period coincides almost entirely with the waterbird hunting season in the Valencia Region that begins on 12 October and ends in the second week of February.

There are no previous studies on the diet of the Greater Spotted Eagle in Spain, but studies conducted in other areas from Europe show that it is composed mainly of birds and mammals and to a lesser extent amphibians, reptiles, fish and arthropods (Meyburg et al. 2019). In addition to habitat loss and degradation, this species faces an additional threat as it is especially vulnerable to poisoning, not only because it inhabits wetlands, but also because of its scavenging habits. In China, the mortality of this species was evidenced due to the consumption of poisoned Pheasants (Qingxia 1996) and also probably in Thailand and Malaysia (Mallalieu 2007). In Spain, a single case of elevated lead exposure has been detected for this species (Mateo et al. 2001), but so far there has been no study on lead exposure.

Field surveys and diet analysis

The diet of the Greater Spotted Eagle between 2008 and 2018 was determined by the combination of three different methods: analysis of regurgitated pellets, identification of prey remains and direct field observations. Fieldwork was performed from October to March, overlapping with the waterbird hunting season. The pellets and prey remains were collected from usual roost sites located in Eucalyptus trees, Aleppo Pines Pinus halepensis and Date Palms Phoenix dactylifera. These places were located through field observations and information provided by a satellite-tracked bird (Pérez-García et al. 2014). Field observations occurred randomly during field surveys and were carried out with binoculars and telescopes. The pellets and prey remains were analysed, and the elements were separated according to their identification and quantification (Marti et al. 2007). Most prey were identified to species level, except for some few cases which were identified to group e.g. micromammals or passerines. Each prey species identified in one pellet was counted as one individual. For each prey and group consumed, the frequency of occurrence (FO) and biomass consumed (B) were calculated. The frequency of occurrence was calculated as the number of individuals of each group of prey divided by the total number of prey. Biomass consumed (B) was estimated by multiplying the standard mean weight of each prey by the number of total individuals consumed (Orihuela-Torres et al. 2017). Both indices were shown as a percentage to facilitate comparisons.

Ammunition presence analysis

The presence of lead from ammunition was determined following the process described in Gil-Sánchez et al. (2018) for all pellets (n = 26) and a subsample of prey remains (n = 10). We used X-ray photographs obtained by a mobile veterinary radiology unit ‘ISOMEDIC (model PX300 HF)’ registered with the code 03/IRX/1205. The radiology unit was programmed to obtain good contrast in photographs according to Gil-Sánchez et al. (2018). The imaging plates for computer radiology were scanned with a Kodak CR 7400 scanner and processed using the Kodak Dental Imaging Software, version 6.12.11.0-B. The presence, number and type of ammunition used were confirmed after a careful examination of each pellet and prey remain. The diameter of all the shot found was measured using a digital calliper (±0.01 mm). The most widespread alternative to lead use is steel ammunition. A magnet was used to differentiate between steel and lead shot. Finally, we compared the frequency of occurrence of the main prey, mammals and birds, between total pellets analysed and pellets that contained shot (Gil-Sánchez et al. 2018). For this comparison, we used a Chi-squared test.

Results

A total of 26 pellets, 29 prey remains and 10 direct observations were obtained. Seventy-eight prey of four classes were recorded: Birds (18 species), Mammals (3 species), Actinopterygii (1 species) and Malacostraca (1 species). Prey size varied from Greater Flamingo (3030 g) to small passerines (25 g).

Birds were the main prey group, both in terms of frequency of occurrence (FO = 73.08%, n = 57) and biomass consumed (B = 66.16%). Mammals were the second most consumed prey group in terms of frequency of occurrence (FO = 20.51%, B = 14.81%, n = 16), while fish were the second most important group by biomass consumed (FO = 5.13%, B = 18.95%, n = 4). Crustaceans were rarely consumed (FO = 1.28%, B = 0.08%, n = 1) (Figure 1). The type of diet analysis partially influenced the importance of each prey group. Birds were the most important prey-group in all three different methods. However, the second most important prey-group varied between methods. Mammals were the second most important prey-group by pellet analysis, but fish were more frequent in field observations and prey remains (Table 1).

Figure 1. Frequency of occurrence (FO) and biomass consumed (B) of mammals, birds and others (including fish and crustaceans) in the winter diet of Greater Spotted Eagle from El Hondo Natural Park, Alicante, Spain. Results are shown separately for each method of analysis used: pellets, prey remains and direct field observations.

Table 1. Diet of the Greater Spotted Eagle in El Hondo Natural Park (Alicante, Spain) between 2008 and 2018 assessed by pellets analysis (Pellets), prey remains (Prey remains) and direct field observations (Direct obs.). FO = frequency of occurrence, B = biomass consumed.

Class/Order/Family/Species	Weight (g)	Pellets			Prey remains			Direct obs.			Total
		n	FO (%)	B (%)	n	FO (%)	B (%)	n	FO (%)	B (%)	n	FO (%)	B (%)
Mammalia		14	35 . 90	37 . 72	1	3 . 45	0 . 21	1	10	2.45	16	20 . 51	14 . 81
Rodentia
Muridae
Rattus rattus	185	6	15.38	7.85	0	0	0	0	0	0	6	7.69	3.01
Rattus sp.	185	5	12.82	6.54	0	0	0	1	10	2.45	6	7.69	2.76
Micromammal unidentified	40	0	0	0	1	3.45	0.21	0	0	0	1	1.28	0.11
Lagomorpha
Leporidae
Oryctolagus cuniculus	1100	3	7.69	23.33	0	0	0	0	0	0	3	3.85	8.94
Aves		23	58 . 97	47 . 93	26	89 . 66	78 . 74	8	80	71.1	57	73 . 08	66 . 16
Anseriformes
Anatidae
Mareca streptera	900	0	0	0	1	3.45	4.74	0	0	0	1	1.28	2.44
Anas crecca	340	4	10.26	9.61	3	10.34	5.37	0	0	0	7	8.97	6.44
Spatula clypeata	610	0	0	0	1	3.45	3.21	0	0	0	1	1.28	1.65
Aythya ferina	820	0	0	0	1	3.45	4.31	0	0	0	1	1.28	2.22
Anas platyrhynchos	840	0	0	0	1	3.45	4.42	0	0	0	1	1.28	2.27
Anas sp.	700	0	0	0	2	6.90	7.37	0	0	0	2	2.56	3.79
Phoenicopteriformes
Phoenicopteridae
Phoenicopterus ruber	3030	0	0	0	0	0	0	1	10	40.08	1	1.28	4.10
Podicipediformes
Podicipedidae
Tachybaptus ruficollis	160	2	5.13	2.26	0	0	0	0	0	0	2	2.56	0.87
Gruiformes
Rallidae
Gallinula chloropus	340	8	20.51	19.23	7	24.14	12.52	3	30	13.49	18	23.08	15.19
Porphyrio porphyrio	770	0	0	0	2	6.90	8.10	0	0	0	2	2.56	4.17
Fulica atra	420	2	5.13	5.94	1	3.45	2.21	0	0	0	3	3.85	3.41
Charadriiformes
Recurvirostridae
Recurvirostra avosetta	300	0	0	0	0	0	0	1	10	3.97	1	1.28	0.41
Charadriidae
Vanellus vanellus	215	1	2.56	1.52	1	3.45	1.13	1	10	2.84	3	3.85	1.46
Shorebird sp.	50	0	0	0	0	0	0	1	10	0.66	1	1.28	0.07
Laridae
Chroicocephalus ridibundus	300	4	10.26	8.48	1	3.45	1.58	0	0	0	5	6.41	4.06
Pelecaniformes
Ardeidae
Ardea cinerea	1440	0	0	0	3	10.34	22.73	0	0	0	3	3.85	11.70
Ixobrychus minutus	100	1	2.56	0.71	2	6.90	1.05	0	0	0	3	3.85	0.81
Accipitriformes
Accipitridae
Buteo buteo	760	0	0	0	0	0	0	1	10	10.05	1	1.28	1.03
Paseriforme
Passerine unidentified	25	1	2.56	0.18	0	0	0	0	0	0	1	1.28	0.07
Actinopterygii		1	2 . 56	14 . 14	2	6 . 90	21 . 05	1	10	26.46	4	5 . 13	18 . 95
Cypriniformes
Cyprinidae
Cyprinus carpio	2000	1	2.56	14.14	2	6.90	21.05	1	10	26.46	4	5.13	18.95
Malacostraca		1	2 . 56	0 . 21	0	0	0	0	0	0	1	1 . 28	0 . 08
Decapoda
Cambaridae
Procambarus clarkii	30	1	2.56	0.21	0	0	0	0	0	0	1	1.28	0.08
Total		39	100	100	29	100	0	10	100	0	78	100	100

Regarding species, the Common Moorhen Gallinula chloropus was the main prey consumed (FO = 23.08%) followed by rats Rattus spp. (FO = 15.38%), Common Teal Anas crecca (FO = 8.97%) and Black-headed Gulls Chroicocephalus ridibundus (FO = 6.41%). In terms of biomass consumed, Common Carp Cyprinus carpio contributed the most to the diet (B = 18.95%), followed by Common Moorhen (B = 15.19%) and Grey Heron Ardea cinerea (B = 11.7%) (Table 1).

Ammunition was detected in 11 of 26 pellets (42.3%) and in four of 10 prey remains analysed (40.0%). We found only one shot in each of the pellets and prey remain items that contained ammunition. Lead ammunition was found in 63.6% of pellets with shot (n = 7), with steel ammunition in 36.4% (n = 4). Lead ammunition was found in pellets with remains of Common Teal, Common Coot Fulica atra, Common Moorhen, Northern Lapwing Vanellus vanellus, rat species and European Rabbit, while steel ammunition was found in pellets with remains of Common Teal, Little Grebe Tachybaptus ruficollis, Common Moorhen, Black-headed Gull and rat species. All pellets with shot contained one prey species, except in the case of rats that always appeared with other species (Northern Lapwing and Common Moorhen). In both cases we assigned the source of the shot to waterbirds. In prey remains with shot, lead ammunition was detected in 25% (n = 1) and steel in 75% (n = 3). Lead ammunition was found in Common Moorhen and steel in Mallard, Common Pochard and Grey Heron. The mean (±se) diameter of lead shot found in pellets and prey remains of waterbirds was 2.24 ± 0.02 mm (n = 9), while lead shot in the pellet containing rabbit remains was 2.6 mm (n = 1). By contrast, the diameter of steel shot found in pellets and prey remains of birds was 3.35 ± 0.02 mm (n = 5). These diameters correspond to the Spanish shot sizes 8, 7 and 4 respectively, which are used for hunting small game species such as rabbits and waterfowl. Birds were more frequent in pellets containing shot than expected by chance, whereas mammals showed the opposite pattern (χ² = 22.64, df = 1, P < 0.001, Figure 2).

Figure 2. Percentage of occurrence of birds and mammals in total pellets analysed (n = 26) and in pellets containing ammunition (n = 11) in Greater Spotted Eagle from El Hondo Natural Park, Alicante, Spain (**P < 0.001).

Discussion

The diet of the Greater Spotted Eagle in southeast Spain was similar to other wintering areas in Greece (Alivizatos et al. 2004) or Thailand (Mallalieu 2007); mostly dominated by waterfowl, while mammals and fish contributed secondarily. This result contrasts with the diet in breeding areas, where mammals, and particularly rodents, were generally the most consumed prey-group (Graszynski et al. 2002, Våli & Lõhmus 2002, Dombrovski 2010). El Hondo is an important wintering area in Spain for waterbirds, where concentrations of 12,000–15,000 birds, mainly Northern Shovelers, Common Teals and Common Coots, are recorded annually (GVA 2012), which may explain why waterbirds were the most consumed group of prey. It is uncertain whether Greater Spotted Eagles actively capture them or behave opportunistically and consume dead and injured animals. Scavenging behaviour has previously been described in the species (Alivizatos et al. 2004, Mallalieu 2007, Dombrovski 2010) and in our case, we recorded direct observations of eagles scavenging on Common Carp and Greater Flamingos, so we cannot rule this out with other prey. The high presence of ammunition found in pellets (42.3%) and prey remains (40.0%) suggests that the species scavenge on unrecovered shot game, such as wildfowl and rabbits. We also observed kleptoparasitic behaviour (Mallalieu 2007, Dombrovski 2010), as Greater Spotted Eagles tried to steal the prey of smaller raptors (e.g. Marsh Harriers, Common Buzzards and Booted Eagles). Lethal attacks on Common Buzzards and Booted Eagles were also recorded in the area, though we were unable to determine whether this behaviour was related to intraguild predation, prey-stealing aggression or active predation. It is probably due to this behaviour that other wintering raptors tend to be very aggressive towards Greater Spotted Eagles.

A consequence of scavenging behaviour may be the overestimation of percentage of biomass consumed (Orihuela-Torres et al. 2017), especially for larger prey (e.g. Common Carp, Grey Heron or Greater Flamingo). This may explain the mismatch between the values of biomass consumed and the frequency of occurrence for some prey, such as carp. Besides the difficulty in accurately estimating the percentage of biomass consumed, the methodology used influenced the contribution to the diet of each group. In our study, although birds were the most commonly identified prey by all three methods, mammals were more often recorded in pellets than in prey remains and field observations, in which more fish were recorded. These findings are consistent with previous literature that confirms that pellets can over-represent mammalian prey and under-represent avian prey, while prey remains over-represent large prey and under-represent small prey (Real 1996, Sánchez-Zapata & Calvo 1998, Redpath et al. 2001, Votier et al. 2001). By using these complementary methods, we can provide results for  a clearer comparison to other studies (Simmons et al. 1991, Redpath et al. 2001).

The high frequency of lead detected, 26.9% and 10.0% of the total pellets and prey remains analysed respectively, warns of a high risk of lead exposure. This value is eight times higher than the lead shot percentage found in pellets in other wintering areas such as Greece (Alivizatos et al. 2004). Furthermore, this value was much higher than those recorded for other raptor species wintering in Spanish wetlands: Marsh Harrier in the Ebro Delta 10.7% (Mateo et al. 1999) and in Doñana 1.8–4.3% (González 1991, Mateo et al. 2007), Red Kite in Doñana 5.5% (Mateo et al. 2001), and Spanish Imperial Eagle pellets from Doñana collected during the hunting season, which reached a value of 14.7% (Mateo et al. 2001). A relationship between the ingestion of lead shot and the hunting pressure exerted on waterbirds has also been found, which in turn varies depending on the water level in the protected areas (Mateo et al. 2007). High rates of lead ammunition in pellets were associated with high lead levels in blood in Marsh Harriers from the Ebro Delta (Mateo et al. 1999), so we might expect high lead levels in blood in our studied Greater Spotted Eagle population. Similar blood lead concentrations have been associated with adverse health effects or reduced reproductive capacity of birds (Pain et al. 2019, Vallverdú-Coll et al. 2019).

The use of lead shot in Spanish Ramsar and other protected wetlands was banned in 2001 (Mateo & Kanstrup 2019). We suggest three hypotheses that may explain the source of the lead ammunition consumed by the eagles despite the ban. The first, and most parsimonious one, is that eagles consume waterbirds hunted but not collected inside the Natural Park, with the implication that hunters continue to use lead shot. Official inspections by rangers have not detected any lead shot (J.L. Echevarrías com pers), however, the inspections are limited and unreliable. Additionally, illegal hunting is common in parts of the Natural Park and is likely to involve lead shot and night hunting, when a large proportion of the hunted birds are not retrieved and may be non-game birds such as Grey Herons or Common Moorhen. Unretrieved or wounded birds are more likely to be taken by scavengers such as the Greater Spotted Eagle.

The second hypothesis is that eagles could be feeding outside the Natural Park, where lead ammunition can be used legally. The fields outside El Hondo Natural Park are mainly active hunting grounds for rabbits. This could explain the presence of lead shot in pellets of the sizes used in rabbit hunting which is not permitted inside the Natural Park. However, continuous tracking of a bird since 2007, using global positioning system devices, has revealed up to 86% of movements were concentrated within the Natural Park, suggesting these birds prefer to feed within the protected wetland (Pérez-García et al. 2014). Additionally, whilst waterbirds may feed in the unprotected fields around El Hondo (Mateo et al. 2014), they are unlikely to be the source of lead shot in the eagle diet given that suitable areas for waterbirds (e.g. rice fields) outside the Natural Park are very scarce.

The third hypothesis is that lead intake is the result of consuming gizzards of waterbirds, which ingest lead ammunition as grit for their gizzards (Pain et al. 1990, 2019). In El Hondo Natural Park, ducks have had serious problems with lead poisoning (Mateo et al. 1997), and although lead shot cleaning work has been done, they are still found in gizzards (pers. obs.). However, in most cases, raptors and specifically spotted eagles, consume the birds’ pectoral muscles, avoiding the digestive organs. Besides, X-ray images taken of the prey remains showed that pieces of shot were randomly lodged in the body, as a product of being shot. In addition, ammunition was also found in species that do not consume grit, such as Little Grebes or Black-headed Gulls.

The European populations of the Greater Spotted Eagle are still declining, so, despite being a small population, the conservation implications of our work are important. Examination of eagle diet suggests not only that the ban on the use of lead ammunition is not fulfilled, with the consequent risk of lead poisoning for waterbirds and raptors, but that hunting of non-game species is occurring inside a protected area. Likewise, the consequences of the intake of lead shot in this wintering area could compromise the Greater Spotted Eagle breeding population. For this reason, urgent regulatory reform of hunting activities, especially in wetlands, is needed. Wetlands are particularly sensitive habitats due to large concentrations of birds, including game and non-game species, in small areas (Kirby et al. 2008), and the presence of many species completely overlaps with the waterbird hunting season. This increases the risk of adverse interactions. We suggest basic measures such as the prohibition of the use of lead ammunition in a buffer area around the protected wetland, the prohibition of night hunting or increased surveillance against poaching, would be essential. Finally, we want to remark that, for complete protection of migratory species, it is necessary to coordinate protection efforts in breeding and wintering areas (Grande et al. 2009).

Acknowledgments

We thank El Hondo Natural Park and Riegos de Levante for the access permissions to the protected area. We are also grateful to Marcos Ferrández, Francisco Botella and Pablo Perales Pacheco for their help with the pellet recollection and observations. We are very grateful to Roberto Rodríguez-Caro for helping with radiographs.