Elsevier

Environmental Pollution

Volume 157, Issue 2, February 2009, Pages 569-574
Environmental Pollution

Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources

https://doi.org/10.1016/j.envpol.2008.09.015Get rights and content

Abstract

Long-lived species are particularly susceptible to bioaccumulation of lead in bone tissues. In this paper we gain insights into the sublethal effects of lead contamination on Egyptian vultures (Neophron percnopterus). Our approach was done on the comparison of two populations (Canary Islands and Iberian Peninsula) differing in exposures to the ingestion of lead ammunition. Blood lead levels were higher in the island population (Canary Islands range: 5.10–1780 μg L−1 n = 137; Iberian Peninsula range: 5.60–217.30 μg L−1 n = 32) showing clear seasonal trends, peaking during the hunting season. Moreover, males were more susceptible to lead accumulation than females. Bone lead concentration increased with age, reflecting a bioaccumulation effect. The bone composition was significatively altered by this contaminant: the mineralization degree decreased as lead concentration levels increased. These results demonstrate the existence of long-term effects of lead poisoning, which may be of importance in the declines of threatened populations of long-lived species exposed to this contaminant.

Introduction

Lead is a highly toxic heavy metal, which can be released into the environment via numerous routes, but principally by industrial, mining and hunting activities (Fisher et al., 2006). The diffusion into the environment of lead produced by human activities has historically been shown to affect wildlife (Depledge et al., 1993, Eens et al., 1999). Nevertheless, the restrictions implemented over the last few decades have resulted in the current situation where contaminating sources, particularly those from industrial activities in developed countries are very limited. Consequently, the contamination deriving from hunting activities has increased in relative importance in recent decades (Fisher et al., 2006). Ingestion of lead shot and bullet fragments is currently the principal source of lead poisoning for numerous vertebrate species, primarily birds (Bellrose, 1959, Clark and Scheuhammer, 2003, Mateo, 1998, Pain et al., 2005, Pattee and Hennes, 1983, Redig et al., 1980).

Individual effects of lead poisoning in wild vertebrates have been repeatedly highlighted. Acute poisoning (exposure to a high concentration during a short time period) can lead to death (Kenntner et al., 2001, Ramo et al., 1992), while chronic exposure (prolonged exposure at lower concentrations) can have sublethal effects which affect reproductive success (Buerger et al., 1986), behavior (Scheuhammer, 1987), immune response (Redig et al., 1991, Snoeijs et al., 2004) and physiology (Burger, 1995, Fair and Ricklefs, 2002). However, the majority of the studies have limited their scope to descriptive aspects or are based on experimental treatments under controlled laboratory conditions; in consequence, few studies have treated this problem in depth in populations of wild vertebrates (Mateo et al., 1999, Pain et al., 2005).

Bones are a long-term repository for lead, containing approximately 90% of the total body burden in mammals and birds (Ethier et al., 2007). The Pb2+ ion readily replaces the Ca2+ ion (Ehle, 1993, Scheuhammer, 1987) additionally altering the hormonal regulation of the calcium and the osteoblast function (Pounds et al., 1991, Ronis et al., 2001). This leads to long-term detrimental effects, which have regularly been demonstrated in clinical studies on mammals, and fundamentally in humans (Cheng et al., 2001, Latorre et al., 2003, Pounds et al., 1991). Nevertheless, very little information exists on the effects that the substitution of calcium by lead in bone tissue and its consequences in processes such as the mineralization and the alteration of compositional properties and bone mechanics may have (Bjorå et al., 2001, Gruber et al., 1997, Hamilton and O'Flaherty, 1995, Pain et al., 2007). It is foreseeable that these effects could be particularly severe for long-lived vertebrates, whose life-history traits make them prone to lead bioaccumulation over time. Thus, long-term effects of lead poisoning could play an until now unknown role threatening some populations and species of large birds of prey such as the Bald Eagle (Haliaeetus leucocephalus), Steller's Sea Eagle (H. pelagicus), White-tailed Sea Eagle (H. albicilla) and the critically endangered Californian Condor (Gymnogyps californianus) which are all known to be affected by lead ammunition sources (Behrens and Brooks, 2000, Church et al., 2006, Franson, 1996, Kenntner et al., 2001, Meretsky et al., 2000).

In this paper we gain insights into the sublethal effects of lead contamination on long-lived vertebrates. We studied the Egyptian Vulture (Neophron percnopterus), a small vulture considered as globally endangered (IUCN, 2007) whose most important populations in the Western Palearctic remain in Spain (Donázar, 1993, Donázar, 2004, Perea et al., 1990). Some Spanish populations of this species have been monitored from the eighties until present, providing an adequate data source for the objectives proposed (Donázar, 1993, Donázar et al., 1996, Donázar et al., 2002). Our approach is based on the comparison of two populations, one resident on islands (Canary Islands) and the other a migratory continental one (Iberian Peninsula) which are potentially differentially affected by this contaminant (see Donázar et al., 2002). Our first hypothesis is that the island population, being resident, suffers higher exposure than the migratory continental one to the ingestion of lead shot during the winter hunting season. Consequently we can predict that (a) we should find a higher frequency of lead shot in regurgitated pellets and of acute-type poisoning shown by blood analysis. As a corollary of the former prediction, (b) in the island population we should find a seasonal pattern with higher lead blood levels during the hunting season. Our next hypothesis is that the contamination has long-term effects on individuals. Given that the bone lead level reflects life time exposure, we predict that (c) the Canary Islands Egyptian Vultures will show higher contaminant levels in this tissue, and (d) there will be an effect of bioaccumulation with age. Finally, we expect to find negative effects on the affected individuals, such that (e) a negative relationship will exist between lead concentration and compositional properties of the bone tissue.

Section snippets

Area and study populations

We analyzed samples of Egyptian Vultures from Fuerteventura, Canary Islands (30 breeding pairs; 1662 Km2) and from the Iberian Peninsula. Within the latter area, individuals from Cádiz (30 b.p.; 9500 Km2), the Ebro valley (100 b.p.; 19,000 Km2) and Segovia (25 b.p.; 5000 km2) were included. Throughout its distribution, Egyptian Vultures usually consume livestock carcasses in “vulture restaurants”, but also scavenge heavily on wild prey (mainly rabbit Oryctolagus cuniculus and pigeon Columba spp.

Lead intoxication in relation to geographical and seasonal patterns of hunting activities

We found no lead shot in the continental pellets examined (n = 327), which was significantly different (χ2 = 14.9, DF = 1, p = 0.01) from that found in a previous study carried out in the Canary Islands, where 5% of the pellets examined contained lead shot (n = 424; Donázar et al., 2002).

Although the mean blood lead concentration was significantly higher in the continental population: T test for unequal variances t = 2.50, DF = 66.56, p = 0.01, 95% CI = 0.03–0.30 (Lavene test of variance equality F = 5.43, p = 

Discussion

Our study demonstrates that ingestion of lead ammunition is related to the accumulation of lead in bones of Egyptian Vultures. It ultimately affected the degree of bone mineralization, this being lowest in those birds with highest bone lead concentrations. Numerous studies indicate that heavy metals, and in particular lead, can affect the correct mineralization of the bone (Gruber et al., 1997, Hamilton and O'Flaherty, 1995), directly or indirectly altering the renewal rate by affecting

Conclusions

We analyzed the long-term effects of lead poisoning in two populations of Egyptian vultures (insular vs. mainland). The ecological context of the insular population determined an elevated exposition to lead shot, and consequently, higher levels of blood and bone lead than the mainland one. Moreover, blood lead levels were higher during the hunting season in the island population, especially for males. In addition, we found a clear effect of bioaccumulation of bone lead with age. The main

Acknowledgements

We would like to thank A. Trujillano and M. de la Riva for their helpful assistance during the fieldwork. The Consejería de Medio Ambiente del Cabildo Insular de Fuerteventura, the Viceconsejería de Medio Ambiente del Gobierno de Canarias, and the Projects REN 2000-1556 GLO and CGL2004-00270/BOS funded this research. We also thank financial support from the Spanish government through grant REN2003-07375.

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