Elsevier

Environmental Pollution

Volume 220, Part A, January 2017, Pages 672-679
Environmental Pollution

Repeated conservation threats across the Americas: High levels of blood and bone lead in the Andean Condor widen the problem to a continental scale

https://doi.org/10.1016/j.envpol.2016.10.025Get rights and content

Highlights

  • Lead levels in Andean Condor indicate both previous and current exposure in Argentina.

  • X-rays showed that a quarter of birds presented embedded or ingested lead bullets.

  • Bone and blood lead poisoning is a conservation threat for the Andean Condor.

  • Lead exposure was documented throughout most of condor range in South America.

  • Our results widen the problem of scavengers' lead contamination at a continental scale.

Abstract

Wildlife lead exposure is an increasing conservation threat that is being widely investigated. However, for some areas of the world (e.g., South America) and certain species, research on this subject is still scarce or only local information is available. We analyzed the extent and intensity of lead exposure for a widely distributed threatened species, the Andean Condor (Vultur gryphus). We conducted the study at two different scales: 1) sampling of birds received for rehabilitation or necropsy in Argentina, and 2) bibliographic review and extensive survey considering exposure event for the species' distribution in South America. Wild condors from Argentina (n = 76) presented high lead levels consistent with both recent and previous exposure (up to 104 μg/dL blood level, mean 15.47 ± 21.21 μg/dL and up to 148.20 ppm bone level, mean 23.08 ± 31.39 ppm). In contrast, captive bred individuals -not exposed to lead contamination- had much lower lead levels (mean blood level 5.63 ± 3.08 μg/dL, and mean bone level 2.76 ± 3.06 ppm). Condors were exposed to lead throughout their entire range in continental Argentina, which represents almost sixty percent (>4000 km) of their geographical distribution. We also present evidence of lead exposure events in Chile, Ecuador, and Peru. Lead poisoning is a widespread major conservation threat for the Andean Condor, and probably other sympatric carnivores from South America. The high number and wide range of Andean Condors with lead values complement the results for the California Condor and other scavengers in North America suggesting lead poisoning is a continental threat. Urgent actions are needed to reduce this poison in the wild.

Introduction

Lead poisoning related to human activities has been recognized as a threat for both wildlife and human health worldwide (Watson et al., 2009, Lambertucci et al., 2010). It has been extensively documented as a conservation problem by studying selected species (Church et al., 2006, Pain et al., 2005, Pain et al., 2009, Fisher et al., 2006), or potentially contaminated territories (Martínez-López et al., 2004, Gómez-Ramírez et al., 2011, Madry et al., 2015). To estimate the actual impact of lead poisoning as a conservation threat, widely distributed species should be surveyed at different spatial scales. Those species could be useful as indicators of a local or a wide range threat that can affect other sympatric species with similar feeding behavior (Gómez-Ramírez et al., 2014).

Currently the main source of lead available to animals is spent ammunition from hunting activities. (Hunt et al., 2006, Church et al., 2006, Jenni et al., 2015). Among birds, both waterfowl and scavengers are prone to accidental ingestion of lead due to their feeding habits, and therefore much information has been reported from these groups (Guillemain et al., 2007, Friend et al., 2009). Birds of prey have been used as biomonitors for heavy metal exposure since they are at the end of the food chain, and they have large home ranges where they can be exposed to contamination (Dauwe et al., 2003). Lead poisoning, particularly in relation to scavengers, has been poorly studied in South America although hunting has increased in some countries like Argentina during recent decades (Saggese et al., 2009, Lambertucci et al., 2011, Ferreyra et al., 2014). This situation increases the risk of accidental consumption of lead in the form of wounded animals, non-retrieved carcasses or gut piles left in the field (Hunt et al., 2006), creating a dangerous scenario for obligate scavengers.

Many obligate and facultative scavenger populations are experiencing abrupt declines across the globe (Ogada et al., 2012, Ogada et al., 2015). Incidental ingestion of Diclofenac ranks high among main causes for vulture decline (Ogada et al., 2012), but lead poisoning events affecting different vulture species have been documented for North America, Europe and Asia (Fisher et al., 2006, Hernández and Margalida, 2009, Kenny et al., 2015, Nam and Lee, 2009, Pain et al., 2009). In fact, incidental ingestion of spent ammunition from hunted animals is considered the primary factor threatening California Condor (Gymnogyps californianus) survival and recovery in the wild (Church et al., 2006, Parish et al., 2009, Finkelstein et al., 2012).

In a given individual the effect of lead contamination can be evaluated not only by lethal effects (Pattee et al., 2006), but also by sub-lethal detrimental effects on physiological functions (Gangoso et al., 2009, Espín et al., 2015), immune system (Franson and Pain, 2011) and behavior (Burger and Gochfeld, 2000). Beyond death of individuals, sublethal long-term effects could play an important role in shaping populations of long lived scavenging species feeding in frequent hunting or contaminated areas. The Andean Condor (Vultur gryphus) is a good model species to evaluate the impact of lead exposure in South American carnivores because it is a long-lived top scavenger that feeds mainly on medium-to-large herbivores, many species of which are hunted (Lambertucci et al., 2009a, Lambertucci et al., 2011). Moreover, it is widely distributed throughout the South American Andes, has a low reproductive rate, and depends on high adult survival to maintain a stable population (Lambertucci, 2007). Andean Condor poisoning with lead bullets has been reported and studied in captivity (Locke et al., 1969, Pattee et al., 2006). However, there is a lack of information regarding lead poisoning in wild condors. The only report of lead exposure in free ranging individuals comes from Patagonia, Argentina, through feathers collected in three of the thirteen Argentinean provinces that the species inhabits. Lead concentrations in feathers from condors in those areas were generally low but some individuals were clearly exposed to this metal, with an isotopic signature resembling a mixture of two types of ammunition sources used for local hunting (one used for big game and another for hare hunting, Lambertucci et al., 2011).

In this study, we documented lead poisoning events for the Andean Condor populations by integrating two different scales. First, we determined the geographic extent and intensity of lead exposure in Andean Condors in Argentina (over ca. 60% of the area of distribution of condors), analyzing both previous (bone) and recent (blood) exposure events for each location. We then evaluated lead exposure for the species at a global scale by reviewing scientific and technical reports, and collecting unpublished data coming from surveys conducted in different South American countries within the species' range.

Section snippets

Study species

The Andean Condor (Vultur gryphus) is the largest new world vulture. Its sexual dimorphism allows sex determination, and age class can be determined according to feather pattern (del Hoyo et al., 1994). This species inhabits a total North-South distance of ca. 7200 km throughout the Andes Mountains (Ramos, 1999), from northern Venezuela and Colombia to southern Argentina and Chile (del Hoyo et al., 1994, Fig. 1a). Its habitat along the Andes between Argentina and Chile covers ca. 4400 km,

Background and reference levels for Argentina

All captive-reared individuals sampled to obtain reference levels presented detectable lead in both blood and bone tissue (Table S1, Supplementary Material). Blood lead concentrations from those individuals were generally low (mean: 5.63 μg/dL; SD: ±3.08) and ranged from 0.02 to 9.20 μg/dL (i.e., below the 10 μg/dL threshold considered for background exposure in the literature). Bone values ranged from 0.40 to 8.70 ppm with a mean of 2.76 ppm (SD: ±3.06), also below the 10 ppm threshold for

Discussion

We documented recent and previous Andean Condor lead exposure for every Argentine continental province covering more than 4000 km South-North, almost 60% of the species distribution. Considering that condors frequently cross political and geographical borders between Argentina and Chile (Lambertucci et al., 2014), but also between Argentina and Bolivia (De Martino, 2009), lead exposure registered in Argentina might be similar in neighboring countries. Worryingly, even though scientific reports

Funding sources

Financial support for this investigation was provided by Buenos Aires Zoo, The Peregrine Fund, Fundación Bioandina Argentina, and PICT-0725 (2014). See Supplementary Information for full acknowledgments on specific Andean Condor program sponsors.

Acknowledgements

F Barbar helped to collect dead condor carcasses and R Santa Cruz assisted in field necropsies. P Plaza and O Mastrantuoni assisted during field trips. P Alarcón and N Lois provided assistance with maps and imaging. B Uberti and D Anderson revised the English language of the manuscript. We thank H Vargas for catalyzing continued grant support from The Peregrine Fund during the study period. We are indebted to Buenos Aires Zoo keepers, particularly W Gómez and V Cleri for assistance during

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