Dust and bullets: Stable isotopes and GPS tracking disentangle lead sources for a large avian scavenger
Graphical abstract
Introduction
Lead is a heavy metal whose toxic effects in humans have been known for millennia (Papanikolaou et al., 2005). Its consequences in wildlife, however, were not described until the 19th century (Calvert, 1876). Since then, direct mortality due to lead toxicity has been frequently reported for many avian species (Pain et al., 2019). There are, nonetheless, more subtle and bearly detectable sub-lethal effects that often go unnoticed, such as alterations in behavior, morphology, and breeding success or physiological functions (Espín et al., 2015; Golden et al., 2016; Vallverdú-Coll et al., 2016). Consequently, the study of the impact of lead pollution on wildlife has become an extremely active field in conservation of threatened populations (Pain et al., 2019).
Vultures are one of the bird groups most sensitive to lead intoxication to the extent that it has been noted as a significant conservation problem for many vulture species worldwide (Golden et al., 2016; Plaza & Lambertucci, 2019), threatening entire populations and compromising the success of costly conservation programs (Finkelstein et al., 2012). The obligate scavenging habits of vultures make them very prone to ingesting ammunition from big game hunting remains (Mateo et al., 1997; García-Fernández et al., 2005; Krone, 2018). Carcasses and remains of shot animals are frequently abandoned in nature (Hunt et al., 2006; Legagneux et al., 2014) and can contain up to hundreds of fragments of metallic lead that can be bioavailable for vultures because of the characteristic extremely acidic gastric fluid of these species (Hunt et al., 2006; Hunt et al., 2009; Knott et al., 2010).
Ammunition is not the only source of lead that could affect vultures. Alternative sources of lead such as paint, contaminated water or soils have also been described as possible causes of intoxication in wildlife (Katzner et al., 2018). Some of them, such as lead-based paint, are of little relevance to scavengers because of their low exposure occurrence (Finkelstein et al., 2012). On the contrary, lead in soil is naturally widespread, and mining activities have led to its bioavailability to wildlife. This is relevant because wild and domestic ungulates, whose carcasses are the main food source for vultures, accumulate lead from the soil in their tissues triggering potential trophic transfer processes affecting higher trophic levels (García-Fernández, 2014; Mateo-Tomás et al., 2016; Naidoo et al., 2017).
Starting from this scenario, it is crucial to identify the role that ammunition and topsoil lead play in vulture intoxication, not only to counteract resistance to global regulations on lead hunting ammunition (Cromie et al., 2010), but also to rule out possible underestimates of the risk posed by topsoil lead. Thus far, the most direct approaches have made use of stable isotope signatures (Church et al., 2006; Mateo-Tomás et al., 2016; Naidoo et al., 2017). In addition, the application of stable isotope mixing models goes one step further, allowing a detailed assessment of the contribution of potential lead sources (Longman et al., 2018). This approach alone, however, is incomplete. It is well known that large avian scavengers perform huge long-distance movements (Alarcón & Lambertucci, 2018), which makes it difficult to determine where the individuals may have been exposed to lead in topsoil and/or game carcasses (Binkowski et al., 2016). In addition, from a population point of view, individual foraging decisions are highly variable (Alarcón & Lambertucci, 2018), which implies the possibility that different birds in the same breeding area could be unequally exposed to different lead sources. Recent studies have tried to deal with this but have been based on direct observations (Church et al., 2006; Mateo-Tomás et al., 2016; Naidoo et al., 2017), which can introduce important biases when the home ranges are very large or include poorly accessible areas.
Here, taking advantage of GPS tracking of 58 griffon vultures of two Spanish populations differently exposed to topsoil and ammunition, we aim to identify the contribution of topsoil and ammunition sources to lead concentrations in the blood of the tracked birds. Spain is an excellent place to address this issue because it holds 90% of the European population and shows a high prevalence of abnormal blood lead levels (García-Fernández et al., 2005; Mateo-Tomás et al., 2016; Descalzo and Mateo, 2018). Moreover, Spanish vultures are exposed to both target lead sources. Whereas elevated lead exposure has been reported in wild ungulates, as well as in livestock, because of topsoil contamination in some Spanish regions (Reglero et al., 2009; Taggart et al., 2011; Pareja-Carrera et al., 2014), the populations of these game species are recovering across most of the country, with the number of animals hunted being one of the largest in Europe (Apollonio et al., 2010). Our aim is to estimate for the first time, linkages between sources of lead in the environment and that found in griffon vultures and the spatial scale at which this species may be exposed to lead. We specifically predict that 1) blood lead in individual vultures derives from two different sources, ammunition and topsoil; 2) lead in the blood of vultures differs between populations based on the individual level of exposure to topsoil and ammunition; and 3) exposure to big game hunting is the major driver of high levels of blood lead concentration.
Section snippets
Focus species and study area
The European griffon vulture is a large body-sized (up to 12 kg) obligate scavenger. It is the most abundant European vulture (Margalida et al., 2010). The bulk (90%) of the European populations are concentrated in Spain (Margalida et al., 2010) where a 2018 census estimated 30.946 breeding pairs (Del Moral and y Molina, 2018). They nest on cliffs and their main source of food is domestic and wild ungulates (Margalida et al., 2011). They feed over areas covering thousands of square kilometers (
Results
Lead values above the background and toxic levels (>20 μg/dl and >50 g/dl, Pain et al., 2019) appeared in 93.3% and 78.6% of individuals from the southern population and 66.7% and 28.6% of individuals from the northern population, respectively (Table 1). Vultures from the southern population showed significantly higher mean lead concentrations than those from the northern population (mean ± SD respectively: 64.0 ± 29.9 vs. 40.1 ± 25.3 μg/dl; t = −3.324, df = 54.718, p = 0.002). Females tended
Discussion
Our results reveal that both topsoil and ammunition are important sources of lead found in the blood of griffon vultures, but their relative contribution is clearly asymmetric. Most of the vultures were exposed to background lead levels probably derived from both direct topsoil exposure (e.g. contaminated dust inhalation or ingestion) and a transfer between trophic levels. Toxic levels of lead is mainly explained, however, by the ingestion of hunting ammunition. Thus, our study, with the
Further remarks
Topsoil lead can be found naturally (Locutura et al., 2012) but pollution derived from mining activity as occurs in our southern study area is a major problem for wildlife and ecosystems, largely because lead mining activity in Europe has been occurring for millennia (Reglero et al., 2009; Taggart et al., 2011). Although for our target species, no consequences were detected, it is possible to hypothesize that other sensitive threatened species such as Egyptian vultures (Neophron percnopterus),
CRediT authorship contribution statement
Eneko Arrondo: Conceptualization, Methodology, Software, Formal analysis, Writing - original draft. Joan Navarro: Methodology, Software, Formal analysis, Writing - original draft, Writing - review & editing. Juan Manuel Perez-García: Methodology, Software, Formal analysis, Writing - original draft, Writing - review & editing. Rafael Mateo: Conceptualization, Writing - original draft, Writing - review & editing, Supervision, Funding acquisition. Pablo R. Camarero: Resources, Writing - original
Declaration of competing interest
The authors declare no competing interests exist.
Acknowledgements
The research was funded by Comunidad de Bardenas Reales de Navarra the Project RNM-1925 (Junta de Andalucía), Project CGL 2015-66966-C2-1-2-R (Spanish Ministry of Economy and Competitiveness and EU/ERDF) and Project PPII-2014-028-P (Junta de Comunidades de Castilla-La Mancha). EA was supported by La Caixa-Severo Ochoa International PhD Program 2015. JN was funded by the Spanish National Program Ramón y Cajal (RYC-2015-17809). ACA was supported by a PostDoc contract Programa Viçent Mut of Govern
References (68)
- et al.
Spatial distribution of wild boar population abundance: basic information for spatial epidemiology and wildlife management
Ecol. Indicat.
(2014) - et al.
Invisible barriers: differential sanitary regulations constrain vulture movements across country borders
Biol. Conserv.
(2018) - et al.
Rewilding traditional grazing areas affects scavenger assemblages and carcass consumption patterns
Basic Appl. Ecol.
(2019) - et al.
Lead isotope ratio measurements as indicators for the source of lead poisoning in Mute swans (Cygnus olor) wintering in Puck Bay (northern Poland)
Chemosphere
(2016) - et al.
Effects of heavy metals on biomarkers for oxidative stress in Griffon vulture (Gyps fulvus)
Environ. Res.
(2014) - et al.
Delta-aminolevulinic acid dehydratase (δALAD) activity in four free-living bird species exposed to different levels of lead under natural conditions
Environ. Res.
(2015) - et al.
Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources
Environ. Pollut.
(2009) - et al.
Association between hunting and elevated blood lead levels in the critically endangered African white-backed vulture Gyps africanus
Sci. Total Environ.
(2018) Ecotoxicology, avian
- et al.
Implications for wildlife and humans of dietary exposure to lead from fragments of lead rifle bullets in deer shot in the UK
Sci. Total Environ.
(2010)