Lead poisoning and heavy metal exposure of golden eagles (Aquila chrysaetos) from the European Alps
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- Kenntner, N., Crettenand, Y., Fünfstück, H. et al. J Ornithol (2007) 148: 173. doi:10.1007/s10336-006-0115-z
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Lead poisoning and organ levels of the non-essential heavy metals lead, cadmium and mercury of seven free-ranging golden eagles (Aquila chrysaetos) from the European Alps, and of one 23-year-old captive golden eagle are reported. All birds were found dead or moribund during the years 2000 and 2001 in Austria, Germany and Switzerland. One golden eagle from Switzerland with extraordinarily high lead residues in its liver and kidney was clearly identified as lethally lead poisoned. Another bird from the same region was found still alive and died in a wildlife rehabilitation center, showing lead residues in its organs known for acute lead poisoning with detrimental physiological effects, such as nervous disorders and the inhibition of the hemoglobine synthesis. Concentrations of cadmium, mercury and lead residues in the organs of the other five free-ranging birds, and in the long-lived captive golden eagle, were low and represent the natural background levels in birds of prey of the terrestrial food web. This is the first published report of lead poisoning in golden eagles from Switzerland. Sources for lead poisoning in golden eagles in the Alpine region are discussed.
KeywordsAquila chrysaetosCadmiumGolden eagleLead poisoningMercury
The golden eagle (Aquila chrysaetos) is a large raptorial bird species of the circumpolar Holarctic. In central Europe, it mainly inhabits the subalpine and alpine regions of the Alps. In the 19th century and early 20th century, the golden eagle became extinct in most non-alpine regions due to severe human persecution and large-scale land use changes of its formerly huge distribution area all over central Europe. The alpine population recovered during the last decades to a stable population of about 1,100–1,200 breeding pairs. This species preys on medium-sized mammals and birds, and also feeds on carrion, the latter especially during the winter season (Haller 1996; Haller and Sackl 1997; Watson 1997). Similar to other scavenging birds, the golden eagle is highly susceptible to lead poisoning through foraging on hunter-crippled prey, and on carcasses or eviscerated animal offal containing embedded lead fragments from bullets or shot pellets (Miller et al. 2002).
Lead poisoning in golden eagles has been reported from North America (Craig et al. 1990; Kramer and Redig 1997; Wayland et al. 1999), but investigations in Europe are rare. Until now, lead levels were published from one golden eagle from Austria (Zechner et al. 2005), five birds from the UK (Pain et al. 1995) and two from Sweden (Borg 1975; Pain et al. 1995; Kendall et al. 1996). Two golden eagles from Germany were judged as lead poisoned by pathological findings (Bezzel and Fünfstück 1995), without toxicological analysis of their organs. Focusing on the occurrence of lead poisoning, we analyzed organ samples of golden eagles for levels of the potentially toxic heavy metals, lead, mercury and cadmium.
Origin, age, sex and concentrations of lead (Pb), cadmium (Cd) and mercury (Hg) in livers and kidneys of seven free-ranging golden eagles (Aquila chrysaetos) from the European Alps
Date of finding
5 May 2001
13 May 2001
1 Apr 2001
31 Dec 2000
23 Jan 2001
All analyses of contaminants were performed at the Research Institute of Wildlife Ecology at the University of Veterinary Medicine Vienna, Austria. Livers and kidneys of eight golden eagles were analyzed for concentrations of lead, mercury and cadmium. However, we did not obtain both organs for each bird. Organ samples were mineralized in nitric acid, and levels of heavy metals were analyzed using atom absorption spectroscopy techniques with graphite-furnace for lead and cadmium, and a cold-vapor technique for mercury. A detailed description of the analytical method has been given previously (Kenntner et al. 2001). In three cases, only the skinned carcasses were submitted for necropsy, which prevented aging by plumage characteristics and, in one case, even the sexing by inspection of the gonads. All levels of heavy metals in golden eagles were calculated in mg* kg−1 (ppm) on a wet weight basis. Statistical analyses were computed with SPSS 11.5 for PC.
Results and discussion
The adult female golden eagle from the Austrian zoo in Feldkirch had levels of 0.093, 0.026, 0.018 ppm for lead, cadmium and mercury in its liver, and 0.066, 0.064, and 0.020 ppm in its kidneys, respectively. These levels were low and may represent the background levels for birds of prey, similar to the concentrations for cadmium and mercury in the seven free-ranging golden eagles (Table 1; Franson 1996; Furness 1996; Thompson 1996). However, the high lead residues in the organs of two golden eagles found in Switzerland were significant for lead poisoning and can produce highly detrimental physiological effects in birds of prey. Bird no. 7 was found alive, but with extreme convulsions, near Ardon, Bolaire on 23 January 2001. It died in a rehabilitation center and was suspected of having lead poisoning. However, the levels of 6.674 and 1.492 ppm in the liver and kidney, respectively, were difficult to judge, because the kidney level was in a range indicating sub-lethal lead exposure, whereas the high liver level was indicative of lethal lead poisoning (Franson 1996). High lead exposure induces mainly organ and nervous disorders, and inhibition of the hemoglobin synthesis (Locke and Thomas 1996). The organs of two other dead golden eagles from the same region in southwest Switzerland (Fig. 1) were obtained for comparison purposes with this suspected lead poisoned eagle. One of them (no. 5) had lead levels of 59.490 and 12.780 ppm in its liver and kidney, respectively,, which are indicative of lethal lead poisoning in birds of prey and other species. This female eagle was found dead near St. Jean in an emaciated condition on 1 April 2001. Radiographs indicated no sign of illegal persecution or lead ammunition in its gizzard, while necropsy revealed a highly viscous greenish content of the intestinal tract. All pathological findings suggested that the bird may have died from starvation. As both symptoms may also occur as a consequence of chronic lead poisoning the general need of toxicological analyses is emphasised—not only in highly suspected cases.
The above mentioned case represents the first proven lead poisoning of golden eagles from Switzerland. Lead poisoning of golden eagles from the Alps have been published from Germany (Bezzel and Fünfstück 1995) and Austria (Zechner et al. 2005). The lead poisoning of two male golden eagles from Germany in 1990 and 1994 was diagnosed by lead particles in their gizzards accompanied by further necropsy findings, though without toxicological residue analysis. Lead levels of 28.2 and 7.6 ppm wet weight in liver and kidneys, together with pathological findings for lead poisoning, were found in one adult female golden eagle collected in 2004 in Eastern Austria (Zechner et al. 2005). All these birds were found in the field during winter. Pain et al. (1995) published the lead concentrations in the livers of five golden eagles from Britain without any incident of lead poisoning. Borg (1975) reported liver lead concentrations of 10 and 36 ppm wet weight in two golden eagles with lethal lead poisoning from Sweden (cited in Kendall et al. 1996). There are numerous investigations on captive and free-ranging birds, and even experimental studies, which clearly identify that lead poisoning in birds of prey results exclusively through ingestion of lead ammunition, in the form of lead shot or fragments of lead bullets. There is only one case report, of a bald eagle (Haliaeetus leucocephalus) from Canada, involving lead poisoned by the uptake of fishing weights through its prey (Scheuhammer and Norris 1995). Because golden eagles depend on carrion during the winter season, and lead shot is of minor importance in the Alpine region, we assume that fragments of lead bullets in carrion or viscera is the source of lead poisoning in golden eagles. Secondary lead poisoning through ingestion of lead shot from the gizzards of lead-poisoned waterfowl should be excluded in the Alps, because hunting of waterfowl is insignificant. Furthermore, the use of lead shot for hunting waterfowl in shallow water and wetlands was banned in Switzerland in April 1998 (Beintema 2001; Schweizer Bundesrat 2003).
Bezzel and Fünfstück (1995) suggested the uptake of eviscerated offal from chamois (Rupicapra rupicapra) as the source of the lead poisoning, because local hunters were advised to leave the intestines of the shot game in the field to support the scavenging golden eagles during winter. Following the diagnosis of lead poisoning in at least two golden eagles, and the retrospective assumption as a mortality factor in more eagles showing similar symptoms during the last years, the local hunters were informed to hide the offal to avoid access by golden eagles.
There is an increasing international concern about lead poisoning in birds of prey due to ingestion of lead ammunition other than lead shot (Fisher et al. 2006; Hunt et al. 2006). Because of the high percentage of lead poisoning in white-tailed sea eagles (Haliaeetus albicilla) found dead or moribund in northeast Germany (Kenntner et al. 2001, 2004), the federal state of Brandenburg prohibited the usage of lead bullets for game hunting in the federal forests in the year 2005, and also instructed the hunters to bury the offal in the field to avoid further lead poisoning of scavengers. Similar species protection measures were conducted on Hoikkaido/Japan to avoid further lethal lead poisoning of wintering Steller’s sea eagles (Haliaeetus pelagicus) and white-tailed sea eagles due to scavenging on shot sika deer (Cervus nippon) or its viscera left in the field (Iwata et al. 2000; Kurosawa 2000; Kim et al. 1999).
Bleivergiftung und Schwermetallexposition von Steinadlern (Aquila chrysaetos) aus den Alpen
Bleivergiftungen und Organwerte für die nichtessentiellen Schwermetalle Blei, Cadmium und Quecksilber von sieben freilebenden Steinadlern (Aquila chrysaetos) aus den europäischen Alpen und von einem 23 jährigen Steinadler aus einem Zoo in Österreich werden dargestellt. Alle Steinadler wurden in den Jahren 2000/2001 in Österreich, Deutschland und der Schweiz tot oder sterbend aufgefunden. Bei einem Steinadler aus der Schweiz konnte anhand der sehr hohen Bleiwerte in Leber und Niere eindeutig eine letale Bleiintoxikation diagnostiziert werden. Ein anderer Vogel wurde in derselben Region noch lebend aufgefunden und verendete in einer Pflegestation. Dieser Steinadler hatte Bleiwerte in Leber und Niere, welche eine akute Bleivergiftung mit zentralnervösen Störungen und Beeinträchtigung der Hämoglobin-Synthese anzeigen. Alle Cadmium- und Quecksilberwerte, und alle weiteren Bleiwerte in den Organen der Steinadler waren niedrig und repräsentieren die natürliche Kontamination von Greifvögeln der terrestrischen Nahrungskette, bzw. die Hintergrundbelastung bei Zoovögeln. Dies ist die erste Beschreibung von einer letalen Bleivergiftung eines Steinadlers aus der Schweiz. Potentielle Ursachen einer Bleiexposition für Steinadler der alpinen Region werden diskutiert.
This study was financed by a grant for the Ph.D. thesis of N.K. by the Nachwuchsförderung Berlin (NaföG) and of the German Academic Exchange Service (DAAD). We wish to thank all people, which found the golden eagles in the fields or conducted the necropsy of the birds and providing of detailed data and information about each specimen. Furthermore we are grateful two anonymous referees for their comments and suggestions on the manuscript.