Article

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

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... The Andean Condor is at risk of extinction in the wild and is currently listed as 'Vulnerable' by the IUCN Red List [13], with key threats being chemical contamination (e.g. [14,15]) and human persecution [16,17]. To provide shelter from the elements, humans and other predators, condors use montane caves or rock shelves on large cliffs as isolated nests or communal roosts [18][19][20]. ...
... To ensure a robust chronology, 10 samples of various material types, including vegetation picked from samples, condor nestling down feathers and bulk sediment, were analysed using accelerator mass spectrometry (AMS) 14 C dating at the André E. Lalonde AMS laboratory in Ottawa, Ontario, and Keck Carbon Cycle AMS Facility in Irvine, California. The 14 C data were calibrated using a South Hemisphere calibration (SHCal20) [26] and the chronology and accumulation rate were determined using the package 'rBacon' v.2.5.5 [27] in the R workspace [28]. ...
... The 14 C ages indicate a stratigraphically intact guano profile with no reversals, regardless of material type (figure 2a). The mean basal age of the guano deposit based on the modelled dating profile is 2150 BP (figure 2a). ...
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Understanding how animals respond to large-scale environmental changes is difficult to achieve because monitoring data are rarely available for more than the past few decades, if at all. Here, we demonstrate how a variety of palaeoecological proxies (e.g. isotopes, geochemistry and DNA) from an Andean Condor (Vultur gryphus) guano deposit from Argentina can be used to explore breeding site fidelity and the impacts of environmental changes on avian behaviour. We found that condors used the nesting site since at least approximately 2200 years ago, with an approximately 1000-year nesting frequency slowdown from ca 1650 to 650 years before the present (yr BP). We provide evidence that the nesting slowdown coincided with a period of increased volcanic activity in the nearby Southern Volcanic Zone, which resulted in decreased availability of carrion and deterred scavenging birds. After returning to the nest site ca 650 yr BP, condor diet shifted from the carrion of native species and beached marine animals to the carrion of livestock (e.g. sheep and cattle) and exotic herbivores (e.g. red deer and European hare) introduced by European settlers. Currently, Andean Condors have elevated lead concentrations in their guano compared to the past, which is associated with human persecution linked to the shift in diet.
... domestic dogs Canis lupus familiaris and pumas Puma concolor), as well as other scavenging birds [6,16]. Other anthropogenic threats affecting this species are shooting, lead contamination, electrocution, and the use of condors in traditional celebrations [17][18][19][20]. Despite the increase in available scientific information pertaining to the Andean Condor, few studies have addressed the factors that threaten this species, and the impacts of these threats remain uncertain in some regions of its distribution, such as northern South America [6]. ...
... Lead contamination is a major threat to Andean Condors throughout their range [6,17]. Our data show that lead concentrations in condor blood in Ecuador and Colombia ranged from 2 μg/dL to 31 μg/dL (S1 Table). ...
... Our data show that lead concentrations in condor blood in Ecuador and Colombia ranged from 2 μg/dL to 31 μg/dL (S1 Table). In four condors, we found that these concentrations exceeded the sublethal threshold of 20 μg/dL [17]. Deaths associated with lead contamination are often isolated rather than in massive events, so this impact could be hidden and remain undiagnosed in most sites where the Andean Condor occurs [6]. ...
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Vultures comprise one of the most threatened groups of birds worldwide. With a total population not exceeding 6700 mature individuals, and in rapid decline across its range, the Andean Condor (Vultur gryphus) is listed as a Vulnerable species in the IUCN red list. Local population extinctions and decline are of particular concern in northern South America, where no more than 340 condors may exist at present. Despite this, no quantitative assessments exist in Ecuador, Colombia, and Venezuela regarding the threats affecting Andean Condor populations. To address this, we compiled records of Andean Condors injured, or killed, between 1979 and 2021. We obtained data of 164 condors affected by different causes of injury, of which 83.5% were reported in Ecuador, 15.2% in Colombia, and 1.2% in Venezuela. Of the total number, 84.7% of the injured individuals died. Between 1979 and 2021, in Ecuador, Colombia and Venezuela, at least 103 Andean Condors were presumably poisoned, 22 were shot, and 39 individuals were affected by other causes. The total number of individuals affected by different causes represents between 48% and 72% of the total population estimated in northern South America. Of great concern is the fact that, between 2007 and 2021, poisoning and shooting together caused the loss of 19–31% of the estimated population of condors in Ecuador, and 7–21% of the estimated population in Colombia. Given the important mortality induced by humans, environmental education programs, socio-ecological research, application of environmental laws, and management strategies based on scientific evidence to prevent and mitigate human-wildlife conflicts are urgently required for effective Andean Condor conservation in northern South America.
... Lead concentrations over the threshold accepted levels were reported in feathers, blood and bones of Andean condors from Argentina Plaza et al., 2020b;Wiemeyer et al., 2017) (Fig. 1). For instance, the prevalence of lead concentrations compatible with health alterations was 4.6% in feathers sampled from north-western Patagonia . ...
... For instance, the prevalence of lead concentrations compatible with health alterations was 4.6% in feathers sampled from north-western Patagonia . In addition, the prevalence of individuals with blood concentrations compatible with subclinical and clinical lead contamination was 32% in wild individuals from Patagonia (Plaza et al., 2020b), and 35% in individuals received for rehabilitation from different regions of Argentina (Wiemeyer et al., 2017). Moreover, 32% of individuals admitted for rehabilitation showed bone lead levels compatible with severe chronic exposure (Wiemeyer et al., 2017). ...
... In addition, the prevalence of individuals with blood concentrations compatible with subclinical and clinical lead contamination was 32% in wild individuals from Patagonia (Plaza et al., 2020b), and 35% in individuals received for rehabilitation from different regions of Argentina (Wiemeyer et al., 2017). Moreover, 32% of individuals admitted for rehabilitation showed bone lead levels compatible with severe chronic exposure (Wiemeyer et al., 2017). These studies suggest that many Andean condors from diverse regions could be suffering health problems and even dying by acute, but also chronic lead exposure. ...
Article
While scientific knowledge is consistently increasing for several species of conservation concern, mitigating their population declines continues to be a great challenge globally. This is the case of the Andean condor (Vultur gryphus) in South America. Scientific information on this species has increased steeply in the last years, but their population declines continue. Here, we review and analyze the scientific information available about Andean condors ecology with implications for its conservation. We also evaluate published and unpublished information about the different threats affecting their populations. Finally, we propose conservation actions based on acquired scientific knowledge, which should be of help for conservation managers and policy makers. The increase in scientific information on this species was mainly focused on subject areas as key habitats for roosting and breeding, food sources, intra and interspecific interaction, human-condor relationships, movement ecology, genetic composition, and health information. Worryingly, good demographic information is still lacking (e.g., population density, breeding success, age and sex-specific survival rates) which prevents the assessment of the population viability. The most important threats affecting condor populations that require urgent actions are poisoning with pesticides and lead contamination. Illegal shooting, impacts produced by human infrastructure and cultural threats are other threats affecting this species. There is not much scientific information on the potential effects of veterinary drugs ingestion, impacts of carnivore traps, pathogen microorganisms and disturbances produced by tourism or climbing activities. Importantly, the actual population impacts of most of the mentioned threats are still unknown. Although some basic ecological studies are still needed (e.g., demography), conservation policies should incorporate scientific knowledge acquired in the last years to produce better results and reverse population declines for this species.
... Currently, lead contamination associated with ammunition is an important conservation problem for the threatened Andean Condor Vultur gryphus (Lambertucci et al. 2011, Wiemeyer et al. 2017 (Ballejo et al. 2018). However, compared with Andean Condors, Black Vultures incorporate a higher proportion of some anthropogenic subsidies in their diets, such as discards from fisheries and abattoirs as well as household waste (Ballejo et al. 2018. ...
... For both species we sampled individuals in the Patagonian steppe, while Black Vultures were also sampled at a rubbish dump located more than 60 km away from the steppe site (Villa La Angostura rubbish dump) to evaluate whether lead contamination differed by foraging site. Andean Condors in the steppe forage only on herbivore carcasses but not in rubbish dumps, fisheries or slaughterhouses (Lambertucci et al. 2009a), so carcasses with lead ammunition fragments seem to be the main source of lead for scavenging birds (Lambertucci et al. 2011, Wiemeyer et al. 2017. Therefore, we predicted that Black Vultures trapped in the steppe should have similar blood lead concentrations to Andean Condors, although Black Vultures trapped in the rubbish dump would show lower lead blood concentrations, as their diet at the dump is mainly composed of organic waste rather than carcasses with lead ammunition fragments. ...
... Northern populations are critically endangered, whereas it is considered Threatened in Argentina where populations are larger but showing signs of decline (Lambertucci 2010, Aves Argentinas, 2017. It is negatively affected by several human activities (Speziale et al. 2008, Lambertucci et al. 2009a, Alarc on & Lambertucci 2018), particularly lead contamination (Wiemeyer et al. 2017). The Andean Condor population studied is one of the largest, with around 300 individuals (Lambertucci 2010). ...
Article
Lead contamination is a global problem affecting a large number of bird species around the world. Among the different avian guilds, vultures and facultative scavengers are particularly threatened by this toxic metal. However, little information is available about differences in exposure to this metal for sympatric vulture species that share food resources. We compared blood lead concentrations of two closely related sympatric obligate scavenger species, the abundant Black Vulture Coragyps astratus and the threatened Andean Condor Vultur gryphus in north‐western Patagonia, Argentina. We sampled 28 Andean Condors and 29 Black Vultures trapped foraging in the same area in the steppe. We also sampled 16 Black Vultures foraging in a rubbish dump to determine if there were differences in lead contamination among foraging sites. Andean Condors had significantly higher mean blood lead concentrations than Black Vultures. There was no difference in lead concentrations between Black Vultures trapped in the steppe and in the rubbish dump. The prevalence and probability of lead concentrations above the threshold level (20 µg/dL) was higher for Andean Condors than for Black Vultures, potentially producing different effects on their health. This disparity in lead contamination may be due to differences in their foraging habits or in their susceptibility to this toxic metal. Overall, our results suggest caution in using an abundant surrogate species to infer lead contamination in a closely related but harder to sample species.
... The challenge is particularly great for scavenger birds, since individuals face different types of threats both on the ground and in the air (Lambertucci et al. 2015, Runge et al. 2014. Outside of PAs, endangered species can be exposed to direct threats such as through persecution (Ogada et al. 2012) and poaching (Litchfield 2013), or indirect threats such as habitat fragmentation (Speziale et al. 2008), unintentional poisoning (Ogada et al. 2012, Wiemeyer et al. 2017 and collision with human infrastructure such as buildings, aircraft, drones and powerlines (Lambertucci et al. 2015). Therefore, individuals of species that spend more time in unprotected areas are comparatively less protected and more exposed to threats (Ogada et al. 2012, Thiollay 2006. ...
... on issues not related to the management of livestock in the Steppe or on problems such as pesticide or lead poisoning, which are direct threats for condors , Lambertucci et al. 2011, Wiemeyer et al. 2017. As observed in adults (Lambertucci et al. 2014), immature condors perform long flights, during which they cross protected and unprotected areas, through the Andes Mountains to the Steppe. ...
... This does not mean that there are no threats inside PAs, but they are better controlled. Condors are also exposed to other conservation threats related to human infrastructure (Lambertucci et al. 2009a, Speziale et al. 2008) and lead poisoning (Lambertucci et al. 2011, Wiemeyer et al. 2017. Importantly, most of those problems are associated with foraging areas, which are mainly in private livestock farms. ...
Article
The framing of environmental conservation has been changing, mainly towards a reconciliation between human needs and nature conservation. A major challenge of biosphere reserves (BRs) is the integration of biodiversity conservation and the sustainable development of local communities. Although these areas are large, they are often not large enough to contain the movements of wide-ranging species. We studied immature Andean condor ( Vultur gryphus ) movements to evaluate their habitat use in relation to protected areas (PAs). We particularly aimed to determine whether BRs significantly increase the protection of this wide-ranging species. We analysed the movement overlap of 26 GPS-tagged birds with the PAs of Patagonia, and we evaluated preferences for particular landscape categories with a use–availability design. Condors were mainly located in unprotected areas (56.4%), whereas 26.4% of locations were within International Union for Conservation of Nature (IUCN) PAs and 17.2% of locations were in BRs (not including IUCN PAs). When compared to availability, birds preferred BRs over other areas, highlighting the importance of BRs in protecting species that forage in humanized areas. However, the lack of controls and management policies expose condors to several threats, such as poisoning and persecution, in both private lands and BRs. Implementing strict management practices for BRs will help to conserve wide-ranging scavengers that feed in humanized areas.
... Numerous studies have highlighted the prevalence of lead poisoning among large raptors that are either complete or partial scavengers, including Golden Eagle (Aquila chrysaetos; Wayland et al., 1999;Madry et al., 2015), Bald Eagle (Haliaeetus leucocephalus; Neumann, 2009;Bedrosian et al., 2012), California Condor (Gymnogyps californianus; Gwiazda et al., 2006;Finkelstein et al., 2012), Andean Condor (Vultur gryphus; Lambertucci et al., 2011;Wiemeyer et al., 2017), Steller's Sea Eagle (H. pelagicus; Ishii et al., 2017), White-tailed Sea Eagle (H. ...
... During processing the birds were kept in a recumbent position with their heads covered by a cloth. Using a disposable needle and syringe, a blood sample of at least 0.5 mL was drawn from either the tarsal vein on the leg or the brachial vein on the underside of the wing and transferred to a purple-topped, certified lead-free, 250-500 μl EDTA tube (Kenny et al., 2015;Wiemeyer et al., 2017). The sample was carefully swirled to ensure thorough mixing with the EDTA medium and refrigerated or frozen until such time as it could be couriered (on ice) to the laboratory for testing. ...
... Instead, blood [Pb] displayed a distinctly right-skewed distribution ( Fig. 2A), which is typical of lead poisoning involving exposure to pure, metallic lead particles (Franson and Pain, 2011;Scheuhammer and Norris, 1996). Since it is unlikely that these nest-bound chicks are encountering fragments of Table 1 Interpretation of [Pb] in different tissue types of members of the order Falconiformes, adapted from Wiemeyer et al. (2017) and Franson and Pain (2011). ...
Article
Poisoning, including secondary lead poisoning, is cited as the single most important cause of vulture mortalities in Africa. To evaluate the prevalence of lead poisoning among South Africa's Gyps vultures compared to other, non-scavenging birds, we obtained blood and bone samples from Cape (Gyps coprotheres) and White-backed (G. africanus) vultures. We found that 66% of White-backed Vultures (n = 110, including 85 nest-bound chicks sampled at Dronfield Nature Reserve) and 80% of Cape Vultures (n = 15) had blood [Pb] in excess of 10 μg/dL, the upper limit of background exposure. Average blood [Pb] were 15.4 μg/dL and 29.7 μg/dL for White-backed and Cape vultures, respectively. Bone samples revealed that 12% of White-backed Vultures (n = 18) and 9% of Cape Vultures (n = 75) suffered from subclinical to severe clinical lead poisoning upon their deaths. By contrast, none of the 40 blood, bone or liver samples obtained from non-scavenging bird species were found to exceed background exposure levels. Our results suggest that, unlike non-scavenging birds, the scavenging lifestyle of Gyps vultures subjects them to lead poisoning on a regular basis. Had environmental sources of lead (e.g., dust) been the source of the lead poisoning at the White-backed Vulture breeding colony at Dronfield, all the chicks would have displayed similar blood lead concentrations. Instead the values ranged from barely detectable to very high, leading us to conclude that metallic lead fragments regurgitated by parents during feeding are responsible for the elevated lead levels in some of the chicks at this site. We conclude the likely source of these particles to be fragments of lead ammunition embedded in the carcasses of hunted animals. These results add to a growing body of evidence underscoring the threat posed by the use of lead ammunition and its potential role in the declines of vultures and other scavenging taxa.
... Recent studies suggest that lead contamination in vultures is probably a widely distributed conservation problem (Garbett et al., 2018;Plaza et al., 2018;Rajamani and Subramanian, 2015;Wiemeyer et al., 2017). Our results signal an important geographical bias that should be considered, given that this important threat and its consequences at an individual and population level could be undiagnosed in many parts of the world. ...
... Blood can be useful to study acute exposure in live birds, whereas liver and kidney can be useful to study this exposure in dead birds (Espín et al., 2014a(Espín et al., , 2014b. Feathers are very useful as a non-invasive sample in live birds, and bones can be used in living and dead birds to assess chronic lead exposure (Espín et al., 2014a(Espín et al., , 2014bPlaza et al., 2018;Wiemeyer et al., 2017). A combination of samples in live birds allows a temporal screening of the bird, which is desirable since detecting lead in some cases may be difficult (Finkelstein et al., 2010;Wiemeyer et al., 2017). ...
... Feathers are very useful as a non-invasive sample in live birds, and bones can be used in living and dead birds to assess chronic lead exposure (Espín et al., 2014a(Espín et al., , 2014bPlaza et al., 2018;Wiemeyer et al., 2017). A combination of samples in live birds allows a temporal screening of the bird, which is desirable since detecting lead in some cases may be difficult (Finkelstein et al., 2010;Wiemeyer et al., 2017). ...
Article
Vultures and condors (hereafter vultures) make up one the most threatened avian guilds in the world due to a variety of human-mediated impacts and disturbances. In fact, 70% of vulture species are currently suffering impacted by significant conservation threats, with lead contamination being particularly important. Unfortunately, lead contamination in vulture species remains poorly studied in many regions of the world. We reviewed the existing scientific knowledge about this threat to vultures. We found 62 scientific articles studying lead contamination in vultures. Seventy-two percent of these articles were from North America and Europe, with the rest corresponding to Asia (13%), South America (8%), and Africa (7%). Most (92%) were published recently (2001–2018). Published articles included information on 13 vulture species out of a total of 23 from both the Old (9) and New World (4). Eighty-eight percent of the articles showed individuals with lead concentrations above threshold levels in some tissues sampled, with New World (Cathartidae) vultures more affected than Old World vultures (Accipitridae). The most suspected but rarely probed source of lead was lead ammunition, but other sources such as pollution or industry were also reported. It is concerning that lead contamination is considered a major threat for just 8% (2/23) of the vulture species categorized by the IUCN Red list. Our review shows that lead contamination is an important threat for several vulture species worldwide, but remains undiagnosed and not well-recognized in some species and geographical areas. The effect of this contaminant on vulture demography is not well known but merits particular attention since it may be leading to population declines in several species.
... Irrespective of the source, lead becomes soluble when it comes into contact with the acidic gastric fluids (Helander et al. 2009) from where it is absorbed into the bloodstream (Franson and Pain 2011). In raptors, physiological impacts of lead increase substantially in severity at blood [Pb] > 10-20 µg/dL Pain 2011, Finkelstein et al. 2014;Wiemeyer et al. 2017) and are usually attributable to exposure to specific lead sources that elevate circulating levels above background environmental levels. Because raptors are likely exposed to a combination of lead sources, it is important to consider all possible avenues of exposure, as failure to do so may hamper mitigation measures. ...
... Because normality could not be achieved through data transformation, and the homogeneity of variance assumption was violated, the non-parametric Kruskal-Wallace test was employed to test for significant differences between the isotopic ratios of the different lead exposure groups. Graphics were produced using the ggplot2 (Wickham 2016) and ggbreak (Xu et al. 2021) packages. Where possible, statistical analyses and comparisons with previous studies focused on 207 Pb/ 206 Pb and 208 Pb/ 206 Pb only. ...
Article
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Elevated lead levels in scavenging raptors can originate from a variety of environmental and anthropogenic sources, including soil, water, mining activities and legacy lead from leaded fuel, but has mostly been attributed to fragments of lead-based ammunition embedded in the tissues of carcasses. To identify the origins of lead in the tissues of white-backed vulture (Gyps africanus) chicks at Dronfield Nature Reserve, South Africa, we used MC-ICP-MS to compare the isotopic composition of lead in blood samples to those of soil in the chicks’ immediate environment, different mining activities in South Africa and lead ammunition commonly used in hunting and game management practices. The isotopic ratios in vulture blood samples ranged widely (²⁰⁷Pb/²⁰⁶Pb: 0.827–0.911), but fell within those measured for ammunition (0.761–0.938). Dronfield water can be excluded as a significant source, as the lead concentration for water was below detection limits. Uranium, coal, atmospheric Pb, legacy Pb from fuel and Pb mining can also be excluded as significant sources, based on the limited overlap with Pb isotopic ratios measured in vulture blood. Whereas 55% of chicks we sampled displayed isotopic ratios consistent with Dronfield soil, the low local Pb concentration and the low extractable Pb levels in South African soil in general, imply that soil Pb is unlikely the major source of Pb in WBV chicks, especially in birds with elevated blood Pb levels, i.e. > 20 µg/dL. Our results, when considered in the context of vulture feeding ecology and low Pb levels in non-scavenging birds in South Africa, imply the major source of elevated Pb levels in WBV chicks to be fragments of lead-based ammunition embedded in the carrion fed to them by their parents.
... Ongoing and persistent threats that impact Andean Condor populations range from habitat destruction, especially relevant for roosting and nesting sites, to hunting due to perceived and documented human-wildlife conflicts (Naller et al. 2008, Ministerio del Ambiente and The Peregrine Fund 2018). Documented threats (Pavez and Estades 2016) also include collisions with power line infrastructure, an extremely worrying increase in illegal carcass poisoning for predator control (Alarcón and Lambertucci 2018), secondary lead poisoning due to consumption of hunted prey species (Wiemeyer et al. 2017), use of body parts in handicrafts, collisions with vehicles (Speziale et al. 2008), competition for food from feral and domestic dogs, tourism disturbance, and use in folkloric Yawar Fiesta events in Peru, often resulting in serious injury or death (Piana 2019). ...
... Thus, current knowledge suggests that Andean Condors remain present in at least 59% of their historical range, although this increases to around 80% when incorporating eBird knowledge (Fig. 2d). Serious threats, such as large poisoning events with pesticides (Alarcó n and , Estrada Pacheco et al. 2020 and lead (Wiemeyer et al. 2017), in combination with confirmed local extirpations herein, underscore the need for species-specific conservation planning and actions. ...
... Ongoing and persistent threats that impact Andean Condor populations range from habitat destruction, especially relevant for roosting and nesting sites, to hunting due to perceived and documented human-wildlife conflicts (Naller et al. 2008, Ministerio del Ambiente and The Peregrine Fund 2018). Documented threats (Pavez and Estades 2016) also include collisions with power line infrastructure, an extremely worrying increase in illegal carcass poisoning for predator control (Alarcón and Lambertucci 2018), secondary lead poisoning due to consumption of hunted prey species (Wiemeyer et al. 2017), use of body parts in handicrafts, collisions with vehicles (Speziale et al. 2008), competition for food from feral and domestic dogs, tourism disturbance, and use in folkloric Yawar Fiesta events in Peru, often resulting in serious injury or death (Piana 2019). ...
... Thus, current knowledge suggests that Andean Condors remain present in at least 59% of their historical range, although this increases to around 80% when incorporating eBird knowledge (Fig. 2d). Serious threats, such as large poisoning events with pesticides (Alarcó n and , Estrada Pacheco et al. 2020 and lead (Wiemeyer et al. 2017), in combination with confirmed local extirpations herein, underscore the need for species-specific conservation planning and actions. ...
Article
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The Andean Condor (Vultur gryphus) is a culturally iconic wildlife symbol for the South American Andes, but is naturally found at very low population densities, and is increasingly threatened. Using the Range Wide Priority Setting methodology, we (a group of 38 Andean Condor experts) updated the Andean Condor historical range (3,230,061 km2), systematized 9998 Andean Condor distribution points across the range, and identified geographic areas for which there was expert knowledge (66%), including areas where Andean Condors no longer occur (7%), and geographic areas where condors are believed to range, but for which there was not expert knowledge about condor presence (34%). To prioritize conservation action into the future and identify existing Andean Condor population strongholds, we used expert knowledge to identify 21 of the most important areas for the conservation of the species (i.e., Andean Condor Conservation Units [ACCUs]) that cover 37% of the revised historical range, and range in size from 837 km2 to 298,951 km2. In general, ACCUs were relatively small in the northern portion of the range in Venezuela, Colombia, Ecuador, and northern Peru, and significantly larger in the central and southern portion of the range in Peru, Bolivia, Chile, and Argentina, reflecting the reduced and narrower historical range in the northern portion of the range, as well as increased threats. Andean Condors can fly extremely long distances and so the populations of many neighboring ACCUs are probably still functionally connected, although this situation also underlines the need for integrated and large-scale conservation efforts for this species. As a function of the Range Wide Priority Setting results, we make recommendations to ensure population connectivity into the future and engage a wide range of actors in Andean Condor conservation efforts.
... They forage particularly in the Patagonian steppe, avoiding urbanized sites such as roads, slaughterhouses, and rubbish dumps [13,34,35]. This species is facing different threats associated with human activities in Argentina and throughout their entire distribution range [29,36,37]. For instance, intentional poisoning, lead contamination, and collision with power lines, among others, are common threats present in Argentina, producing injuries in some individuals, which have to be admitted for rehabilitation at specialized rehabilitation centers, such as Buenos Aires Zoo [36][37][38] Figure S1). ...
... This species is facing different threats associated with human activities in Argentina and throughout their entire distribution range [29,36,37]. For instance, intentional poisoning, lead contamination, and collision with power lines, among others, are common threats present in Argentina, producing injuries in some individuals, which have to be admitted for rehabilitation at specialized rehabilitation centers, such as Buenos Aires Zoo [36][37][38] Figure S1). This area is a steppe dominated by grasses and shrubs, and it borders the Andean Forest in the west [39]. ...
Article
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Wild bird species have commonly been implicated as potential vectors of pathogens to other species, humans included. However, the habitat where birds live could influence the probability to acquire these pathogens. Here, we evaluated if the characteristics of the environment used by obligate scavenging birds (vultures) influence their colonization by zoonotic pathogens. For this, we particularly focused on Salmonella spp., a zoonotic pathogen commonly present in bird species. The occurrence of this bacteria was evaluated in free ranging Andean condors (Vultur gryphus) using natural environments from Argentina and compared with those obtained from condors under human care. In addition, we compared our results with those reported for other wild vultures using natural and anthropized environments at a global scale. We did not find Salmonella spp. in samples of wild condors. Captive condor samples presented Salmonella spp. with an occurrence of 2.8%, and one isolate of Meticilin Resistant Staphylococcus aureus, among other potential pathogenic microorganisms. Moreover, some species of free ranging vultures from diverse geographical areas using anthropized environments tend to present higher occurrences of Salmonella spp. These results highlight the importance of pristine ecosystems to protect vultures’ health toward pathogenic microorganisms that can produce disease in these birds, but also in other species. We call for more studies evaluating differences in occurrence of zoonotic pathogens in vultures according to the quality of the environment they use. Even when vultures have not been implicated in zoonotic pathogen spread, our results add information to evaluate potential events of pathogen spillover between vultures and from these birds to other species.
... Harmful lead levels have been found in a multitude of scavenging species associated with lead-based ammunition but little attention has been devoted to this issue in Australia (Hampton et al., 2018). This is a worldwide phenomenon, with harmful lead exposure from bullet-derived lead having been reported from numerous scavenging bird species in North America (Bakker et al., 2017;Church et al., 2006), Europe (Ecke et al., 2017;Helander et al., 2009) Asia (Isomursu et al., 2018;Kenny et al., 2015), South America (Lambertucci et al., 2011;Wiemeyer et al., 2017) and Africa (Garbett et al., 2018;van den Heever et al., 2019). We are unaware of any such published studies on wild Australian species. ...
... The lead levels observed in bone samples from adult wedge-tailed eagles were generally low compared to species that specialize in scavenging from elsewhere in the world. For example, mean bone lead levels reported for Andean condors (Vultur gryphus) were 23.08 ppm (Wiemeyer et al., 2017). However, studies from congeneric eagle species from other parts of the world have reported comparable lead levels. ...
Article
Lead toxicity from ammunition has been shown to be a threat to scavenging birds across the globe. Despite decades of research in Europe, North and South America, Asia and Africa, there have been no studies to investigate this phenomenon in Australia despite that continent having many species of scavenging birds and widespread shooting practices. We present preliminary evidence of lead exposure in Australia's largest bird of prey, the wedge-tailed eagles (Aquila audax) through analysis of bone and eggshell samples from south-western Australia. From 11 bone samples, three birds (27%) had lead levels exceeding literature thresholds for elevated levels (>6.75 ppm). From 36 eggshell samples, no samples had lead levels >0.5 ppm, suggesting some limitations for this matrix as an indicator of lead exposure. Isotope ratios suggested ammunition as a likely source of the lead found in bone samples with elevated lead levels but other potential sources of lead require further investigation. Our preliminary results demonstrate that lead exposure is occurring in scavenging birds in Australia, and like the rest of the world, is likely to be derived from ammunition. This study supports an urgent call for further research into this worldwide phenomenon in Australia.
... Lambertucci et al. (2011) found lead levels as high as 21.1 ppm in condor feathers from northern Patagonia. A recent study by Wiemeyer et al. (2017) found blood lead levels ranging from 0.2 to 1400 ppm in a set of 76 free-ranging condors from across Argentina submitted for rehabilitation. Additionally, through X-ray examination they identified 15 of 62 (24.2%) condors with ammunition fragments in their bodies (Wiemeyer et al. 2017). ...
... A recent study by Wiemeyer et al. (2017) found blood lead levels ranging from 0.2 to 1400 ppm in a set of 76 free-ranging condors from across Argentina submitted for rehabilitation. Additionally, through X-ray examination they identified 15 of 62 (24.2%) condors with ammunition fragments in their bodies (Wiemeyer et al. 2017). Whereas secondary lead poisoning has been documented in numerous predator and scavenger bird species, particularly raptors, there are few studies involving other taxonomic groups (Tranel and Kimmel 2009). ...
Article
Waterfowl hunting in Argentina is a profitable industry that attracts hunters from all over the world. Most hunting occurs as high-end hunting tourism, through which registered outfitters service predominantly foreign clients on private lands. Lead pollution from hunting ammunition is increasingly recognized as a significant local problem, impacting wildlife, aquatic and terrestrial habitats, and extending to vulnerable human rural communities. Regulatory frameworks that restrict lead shot use are a budding success story but remain challenged by their constrained geographic range and limited compliance rooted in unavailable nontoxic ammunition. Changes in hunting practices in Argentina are long overdue.
... Esta medida representa las concentraciones circulantes del plomo ingerido o liberado de tejidos de almacenamiento. Sin embargo, mediante esta metodología no se puede diferenciar entre una exposición aguda o crónica, debido a que existe un continuo movimiento intercompartimental de plomo entre sangre, tejidos blandos y huesos, por lo cual este metal llega a tener una vida media de 28-30 días, 40 días y hasta más de 30 años, respectivamente(22).En el estudio el mayor valor detectado fue 4 µg/dL en un rey gallinazo (S. papa) del zoológico B, que es un valor muy bajo comparado con el umbral establecido por Franson en 1996, ya que menciona el valor 20 µg/dL como el mínimo necesario para considerar efectos fisiológicos(23,24). Sin embargo, Espín et al.(25) reportan que la enzima ácido delta-aminolevulínico deshidratasa (ALA-D), una enzima esencial en la biosíntesis del grupo heme, así como uno de los más sensibles y específicos biomarcadores de baja exposición a plomo, se ve inhibida en más del 15 % con concentraciones mayores a 10 µg/dL en el buitre leonado (Gyps fulvus) y en 10 % con concentraciones de plomo > 1 µg/dL en el búho real (Bubo bubo).En cuanto al promedio por institución zoológica, el mayor promedio lo obtuvo el zoológico B con 2,65 ± 1,00 µg/dL, lo que muestra diferencias significativas de las concentraciones de este metal pesado entre los 3 zoológicos muestreados (p = 0,01), mientras que no se evidenciaron diferencias significativas entre especies (p = 084). ...
... Sin embargo, Espín et al.(25) reportan que la enzima ácido delta-aminolevulínico deshidratasa (ALA-D), una enzima esencial en la biosíntesis del grupo heme, así como uno de los más sensibles y específicos biomarcadores de baja exposición a plomo, se ve inhibida en más del 15 % con concentraciones mayores a 10 µg/dL en el buitre leonado (Gyps fulvus) y en 10 % con concentraciones de plomo > 1 µg/dL en el búho real (Bubo bubo).En cuanto al promedio por institución zoológica, el mayor promedio lo obtuvo el zoológico B con 2,65 ± 1,00 µg/dL, lo que muestra diferencias significativas de las concentraciones de este metal pesado entre los 3 zoológicos muestreados (p = 0,01), mientras que no se evidenciaron diferencias significativas entre especies (p = 084). En Argentina se hallaron concentraciones igualmente bajas en cóndores en cautiverio, con un promedio de 5,63 ± 3,08 µg/dL y un rango de 0,02 a 9,20 µg/ dL(24).No obstante, en la intoxicación por plomo intervienen tres factores: estatus nutricional, predisposición genética y disponibilidad de plomo. La ingestión es la vía primaria de contaminación(18). ...
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El plomo es uno de los metales pesados más tóxicos para los seres vivos, lo cual constituye una problemática a escala global. Este metal se encuentra de manera natural en el medio ambiente. Puede permanecer por largos periodos en tejidos animales y producir alteraciones fisiológicas, comportamentales e incluso la muerte. Uno de los grupos taxonómicos más afectados son las aves, especialmente aquellas especies que se encuentran en la parte superior de la cadena alimenticia, debido a su susceptibilidad a la bioacumulación de metales pesados. Sin embargo, en Suramérica existe escasa información sobre la exposición de plomo en catártidos. El objetivo de esta investigación fue determinar concentraciones basales de plomo en catártidos mantenidos en condiciones de cautiverio en Colombia. Para ello se analizaron muestras sanguíneas de 9 reyes gallinazos (Sarcoramphus papa) y 7 cóndores de los Andes (Vultur gryphus) de tres zoológicos por medio de espectrofotometría de absorción atómica. Los resultados sugieren que 15 de 16 ejemplares contienen concentraciones de plomo. El zoológico B tuvo el mayor promedio (2,65 ± 1,00 μg/dL), seguido del zoológico C (1,87 ± 0,63 μg/dL) y del zoológico A (0,8 ± 0,89 μg/dL). El promedio para S. papa fue de 2,11 ± 0,42 μg/dL, mientras que el de V. gryphus fue de 1,89 ± 1,52 μg/dL. Se concluye que aunque existe una diferencia significativa (p = 0,01) entre los zoológicos muestreados y se detectaron concentraciones de plomo en el 93,75 % de la población, estas son bajas comparadas con las reportadas por los estudios.
... Lead is a highly toxic heavy metal and the most common cause of metal poisoning in raptors, even at concentrations below lethal levels, lead may adversely affect individuals (Berny et al. 2015;Pain et al. 2019). Long-term exposure to lead is known to have caused population declines in the California condor (Finkelstein et al. 2014) and the Andean Condor (Wiemeyer et al. 2017). Cape vultures are known to exhibit signs of osteodystrophy as a result of lead exposure Content courtesy of Springer Nature, terms of use apply. ...
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Vultures struggle to breed owing to increased exposure to toxic materials, reduced nesting sites and changing weather conditions. Breeding success determines the fate of bird populations; thus, understanding the determinants of breeding success is vital, especially for critically endangered species like Gyps species, whose populations have been decimated across Asia due to the rampant use of diclofenac. Despite their declining trend, data on vultures’ breeding are limited. Between 2010 and 2023, monitoring the reproductive performance and the covariates that influence it, we assessed the drivers of breeding success in Long-billed Vultures (LBV) Gyps indicus in the Deccan Plateau, India. Over 14 years, we monitored 23 nests in two breeding colonies and found that 161 occupied pairs of LBV laid 116 eggs, of which 85 fledged successfully. The reproductive performance recorded over 14 years showed a significant declining trend. Inter-annual variations in breeding success compared with corresponding period’s environmental covariates showed that breeding success decreased with the toxic levels in effluent discharge from paper industry and increased with wind speed. Inter-nest variations in nest success compared with corresponding nest and nest-site covariates, revealed that nest success increased with nest depth and was higher in nests with vegetation cover than those without the same, but decreased with distance from the top of the cliff to nest. Overall, our study indicates that effluent discharge into the Peddavagu stream by the Sirpur paper industry is a key negative driver of LBV breeding success. We suggest, measures to filter hazardous substances at the Sirpur paper industry, conducting detailed toxicological studies on vulture carcasses and initiating new studies on LBV breeding ecology in potential areas, as these can provide critical insights.
... Bone size and age could be factors influencing this change, but the previous samples were limited in quantity and scope of analysis. Our study found a significant positive association between age and bone lead similar to the bone lead study in live Andean condors (Wiemeyer et al. 2017). The high lead concentration in the live bone could be deleterious throughout the condor's lifetime as bone resorption and deposition happen in response to physiological and metabolic changes. ...
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Lead poisoning remains the leading cause of diagnosed death for critically endangered California condors, which are annually monitored for lead exposure via blood tests. Blood tests are generally reflective of acute lead exposure. Since condors are victims to both chronic and acute lead exposure, measuring bone, which in humans is reflective of years to decades worth of exposure, is a valuable biomarker. In this study, we measured bone Pb of the tibiotarsus of 64 condors in vivo using a portable x-ray fluorescence device. The average uncertainty for measurements, typically reflective of how effective the device performed, was found to be 3.8 ± 2.2 µg/g bone mineral. The average bone lead level was found to be 26.7 ± 24.5 µg/g bone mineral. Bone lead correlated significantly with a sum of all blood lead measures over the lifetime of each condor. In the future, bone lead can potentially be used to inform treatment planning and address the chronic health implications of lead in the species.
... Spent ammunition in carcasses is thought to be a major avenue of exposure among scavenging birds (Fisher et al., 2006;Franson and Pain, 2011b;Ganz et al., 2018;Naidoo et al., 2017), with high levels of lead exposure frequently reported among vultures (Finkelstein et al., 2012;van den Heever et al., 2019; Abbreviations: EHL, evaporative heat loss; EWL, evaporative water loss; M b, , body mass; MHP, metabolic heat production; T air, , air temperature; T b, , body temperature; RMR, resting metabolic rate. Wiemeyer et al., 2017). Blood lead levels associated with significant subclinical and clinical poisoning in southern African vultures have been reported by several workers (e.g., Garbett et al., 2018;Naidoo et al., 2017;van den Heever et al., 2019), supporting arguments that poisoning in general is a major cause of recent rapid declines in vulture populations in Africa (Ogada et al., 2016;Safford et al., 2019). ...
... Similar methods have been used by the United States Fish and Wildlife Service (USFWS) to collect data on American woodcocks (Scolopax minor) (Myatt and Krementz, 2007). Lead stored in bones is considered the best indicator for evaluating lead exposure over the total lifetime (Franson and Pain, 2011), and has been used for this purpose in several avian groups, including waterbirds (Merendino et al., 2005) and raptors (Wiemeyer et al., 2017). Wings were collected from a total of 77 ducks from nine sites across Victoria (Fig. 2) by government recreational hunting enforcement officers in 2018 (n = 30) and 2021 (n = 47). ...
Article
There is growing worldwide recognition of the threat posed by toxic lead for wildlife and humans. Lead toxicity from ammunition has been shown to be a threat to waterbirds across the globe. Lead shot was banned for all waterfowl hunting in Victoria, Australia, in 2002. However, no assessments of lead exposure in Australian waterfowl have been published since the 1990s. Our aim was to estimate contemporary lead exposure via measuring bone lead concentrations in a harvested dabbling duck, the Pacific black duck (Anas superciliosa). We collected wings from 77 Pacific black ducks, spanning 2018 (n = 30) and 2021 (n = 47), from nine sites with long-term histories of regular waterfowl hunting. We sought to validate portable X-ray fluorescence (XRF) for this purpose by taking a piece of humerus bone from each bird, and measuring lead concentration (mg/kg), first via non-destructive XRF and then via destructive inductively coupled plasma mass spectrometry (ICP-MS) and validated the relationship via regression analysis. Portable XRF bone lead measurement demonstrated a strong correlation with ICP-MS results using root-transformed regression (R2 = 0.85). Greater than 92 % of ducks had only background lead exposure (<10 mg/kg). When compared to historical studies in the same species at similar field sites from the 1990s, lead exposure levels were considerably lower, with mean lead concentrations ~2-fold lower (3.7 c.f. 7.7 mg/kg), and the frequency of birds with severe lead exposure (>20 mg/kg) ~3-fold lower (2.6 c.f. 7.5 %). Our results confirm that portable XRF is a useful option for measurement of bone lead in Australasian waterbird species. Our findings also demonstrate that a ban on the use of lead shot around 20 years ago has been associated with a substantial reduction in lead exposure in at least one species of waterfowl.
... In contrast, when Andean condors forage in natural and semi natural areas in Argentina, within or close to protected areas, the occurrence of plastic is less common (Ballejo et al., 2021). To improve conservation policies for this species and its environment, it is important to know whether Andean condors are exposed to plastic pollution in different parts of their distribution range, as with other threats such as intentional poisoning and lead contamination (Plaza and Lambertucci, 2020;Wiemeyer et al., 2016). Moreover, given that Andean condors are apex scavengers at the top of the trophic chain, this species can serve as an indicator of plastic pollution in the environment and for other species. ...
Article
Plastic pollution is an alarming environmental problem affecting diverse species worldwide. Scavenging birds are currently exposed to plastic due to contamination of their food sources. Here, we evaluated the ingestion of plastic by a threatened top scavenger, the Andean condor (Vultur gryphus), and the potential origin of the plastic. We analyzed the biotic (organic items from the diet) and abiotic (synthetic material) composition of regurgitated pellets in two remote areas of Peru associated with protected areas: a marine-coastal region and an Andean region. Condors consume mainly Pinnipeds and South American camelids in the marine-coastal region, and camelids and livestock in the Andean region. We found different sizes and varieties of plastic debris, with a very high frequency of occurrence (85–100%) of microplastics in pellets of both areas studied. The occurrence of microplastics differed between sites; although very high in general, the rate of occurrence and density were higher in the marine-coastal region. We also confirmed that carcasses consumed by condors in both study areas were contaminated with plastic. Therefore, plastic in Andean condors is most probably acquired through the food web in both the marine and terrestrial environments. Andean condors from Peru are highly contaminated with plastic, which may affect their health, population dynamics, and conservation. Moreover, as condors are apex scavengers, our results highlight the fact that plastic pollution in remote areas of Peru is present at different levels of the food web and in the environment. Urgent Action should be taken to reduce environmental contamination with this hazardous pollutant.
... Long-lived species in particular may be susceptible to bioaccumulation of lead in bone tissue (Gangoso et al., 2009). In addition, long-term effects of lead exposure have been a factor in the decline of the California condor (Cade, 2007;Finkelstein et al., 2012Finkelstein et al., , 2014Green et al., 2008;Hall et al., 2007), the Andean Condor (Wiemeyer et al., 2017), and other long-lived raptors worldwide (Berny et al., 2015;Clark & Scheuhammer, 2003;Hernández & Margalida, 2009;Kenntner et al., 2001;Pain et al., 2005;Rodriguez-Ramos Fernandez et al., 2011). Vultures and other scavengers are particularly susceptible to lead poisoning because they feed on the carcasses or entrails of animals that have been shot with lead-based ammunition (Gangoso et al., 2009;Gorski et al., 2021;Pain et al., 2019). ...
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African wildlife face challenges from many stressors including current and emerging contaminants, habitat and resource loss, poaching, intentional and unintentional poisoning, and climate‐related environmental change. The plight of African vultures exemplifies these challenges due to environmental contaminants and other stressors acting on individuals and populations that are already threatened or endangered. Many of these threats emanate from increasing human population size and settlement density, habitat loss from changing land use for agriculture, residential areas, and industry, and climate‐related changes in resource availability. Environmental chemicals that are hazardous include legacy chemicals, emerging chemicals of concern, and high‐volume‐use chemicals that are employed as weed killers and in other agricultural applications. Furthermore, there are differences in risk for species living in close proximity to humans or in areas affected by habitat loss, climate, and industry. Monitoring programs are essential to track the status of nesting pairs, offspring survival, longevity, and lifetime productivity. This is important for long‐lived birds, such as vultures, that may be especially vulnerable to chronic exposure to chemicals as obligate scavengers. Furthermore, their position in the food web may increase risk due to biomagnification of chemicals. We review the primary chemical hazards to Old World vultures and the interacting stressors affecting these and other birds. Habitat is a major consideration for vultures, with tree‐nesters and cliff‐nesters potentially experiencing different risks of exposure to environmental chemicals. The present review provides information from long‐term monitoring programs and discusses a range of these threats and their effects on vulture populations. Environ Toxicol Chem 2022;00:1–19.
... observation), which the marabou then target for their food content. Plastic consumption is often lethal for many species of birds, particularly freshwater (Wiemeyer et al. 2017;Battisti et al. 2019) and marine birds (Tanaka et al. 2013;Verlis et al. 2013;Lavers et al. 2014;Wilcox et al. 2015;Roman et al. 2016); however, we only saw two marabou corpses (at the Maun landfill) during this study and so their ability to regurgitate may prevent mortality. ...
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We compared diets of marabou storks Leptoptilos crumenifer foraging from urban landfills and natural areas in northern Botswana using stable isotope analyses and inductively coupled plasma mass spectrometry on moulted feathers. There were significant differences in the diet of marabous foraging from natural areas compared to urban waste sites, reflected by lower d 13 C and less enriched d 15 N concentrations in those feeding at landfills, suggesting a shift in trophic niche. Feathers from birds foraging at landfills also had significantly higher concentrations of chromium, lead, nickel, and zinc and lower levels of cadmium and potassium than feathers sampled from natural areas. We also analysed marabou regurgitant (42 kg, naturally expelled indigestible food resources) from the Kasane landfill site. More than half was plastic, with single regurgitants weighing up to 125 g. Urban waste stored in open air landfills is altering some marabou diets, affecting their natural trophic niche, resulting in the consumption (and regurgitation) of large amounts of plastic, and exposing marabou to potentially chronic levels of trace metals. Despite the marabou's apparent resilience to this behavioural shift, it could have long-term effects on the population of the marabou stork, particularly considering Botswana has some of the few regular marabou breeding colonies in southern Africa.
... First, Andean Condors can also suffer from lead poisoning caused by incidental ammunition ingestion from hunted animals as well as by direct persecution. In fact, a recent continental-scale study analyzing blood and bone samples of Andean Condors revealed lead values as high as ten times the background reference, with some of the highest values corresponding to samples collected in Patagonia (Wiemeyer et al. 2017). As in the case of pesticide poisoning, there is also experimental evidence linking lead poisoning to altered levels of steroid hormones (Yu et al. 2005). ...
... 1 An estimated 22% of children are born with low birth weight, 2 and 155 million children younger than 5 years were affected by stunting in 2016, most living in Asia and Africa. 3 Many of these children grow up in environments heavily contaminated with fecal pathogens, exposed to environmental lead, 4,5 and experience limited parent-child interaction and stimulation activities, which may result in poor cognitive development and impairment in intellectual function. 6 Several focused interventions improve early child development. ...
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Delivery of interventions through group sessions allows for in-depth discussions and creates opportunities for group members to work together to identify and solve common problems. However, low attendance may limit impact. We explored factors affecting attendance, active participation, and behavior change in an integrated group-based child development and maternal and child health intervention in Bangladesh. Community health workers (CHWs) facilitated two sessions a month including material on child stimulation; water, sanitation, and hygiene; nutrition, maternal depression, and lead exposure prevention. Sessions were conducted with 320 pregnant women and mothers with children younger than 24 months, in 16 villages in Kishoreganj district. After 4 and 9 months of intervention, we conducted focus group discussions and in-depth interviews with mothers (n = 55 and n = 48) to identify determinants of attendance and behavior change, and to examine potential for intervention scale-up. Recruiting family members to assist with childcare resulted in improved attention during sessions. Adopting a storytelling format for presentation of session materials resulted in more engaged participation during courtyard sessions. Session attendance and behavior change, especially purchasing decisions, were difficult for participants without the support of male heads of the household. Selecting a rotating leader from among the group members to remind group members to attend sessions and support CHWs in organizing the sessions was not successful. Facilitating self-appraisals and planning for water and sanitation allowed participants to identify areas for improvement and track their progress. Key determinants of a participant's attendance were identified, and the resulting intervention shows promise for future implementation at scale.
... In this sense, lead (Pb) is a naturally occurring but nonessential element that is highly toxic at elevated concentrations having the potential to affect most body systems and the health of animals. Moreover, this toxic metal is considered one of the most significant threats to several species (Haig et al., 2014;Wiemeyer et al., 2017;Isomurso et al., 2018;Helander et al., 2019;Ecke et al., 2017). ...
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The effects of lead exposure on oxidative stress biomarkers in feral pigeon (Columba livia) from Mitrovicë town (situated in close vicinity of ormer lead and zinc smelter) were studied through the use of blood Pb (PbB) levels, d-aminolevulinic acid dehydratase (δ-ALAD) activity, level of plasma δ-Aminolevulinic acid (ALA), Glutathione (GSH), Malondialdehyde (MDA), Uric acid (UA), Urea (U), and creatinine (CR). Lead levels in pigeons from Mitrovicë were significantly elevated (P<0.001) compared to the control. Elevated PbB in pigeons from Mitrovicë was also accompanied by significantly inhibited (P<0.001) δ-ALAD activity in blood, significantly decreased levels of GSH and MDA (P<0.001; <0.05), and significantly elevated levels of ALA, UA, CR (P< 0.001) compared to the control. Negative correlation was observed between PbB and δ-ALAD activity (r=-0.409; P<0.05) in birds in Mitrovicë. This study provides important evidence about the chronic effects of lead on the analyzed oxidative stress biomarkers. In addition, the study proves that the pigeons in Mitrovicë remain chronically exposed to harmful effects of lead, and that the close vicinity of the former smelter "Trepça" still represents a source of exposure to lead for the health of biota and humans.
... As scientists involved in the whole conservation process, we described lead contamination in condors for the first time in 2011, and even established potential sources of this toxic metal (Lambertucci et al. 2011). Then we evaluated this threat for the entire South America (Wiemeyer et al. 2017) and proposed policy changes to mitigate it. Through these actions, we have obtained a successful result working jointly with different social actors, who have helped to produce a normative to ban lead ammunition in protected areas from Argentina (Resolution 417/2019) and to promote non-toxic alternatives (Fig. 1B). ...
Article
Scientists from different parts of the world have worked on understanding threats affecting vultures. In the case of the threatened Andean condor (Vultur gryphus), their ecology and threats were poorly studied until the last decade. Today, there is not only more information, but there are also several action plans for this species in different parts of their distribution range. Those plans are beginning to be based on scientific evidence and experience of scientists and diverse stakeholders, thus reducing the gap between scientific knowledge and decision-making processes. To illustrate this, we discuss here some successful results obtained by scientists, managers, policy makers and diverse stakeholders working in the conservation of Andean condors. We show some examples of how scientific evidence, and the knowledge and participation of different parties, helped to start promoting regulations for two of the main threats affecting this species, poisoning and lead contamination.
... The change in diet together with the increase in hunting has led to an increase in ingestion of lead ammunition from carcasses, the main source of lead poisoning in Andean Condors (Lambertucci et al. 2011). Although it has been documented that the species is especially susceptible to lead poisoning (Pattee et al. 2006), the impacts on populations are poorly understood (Wiemeyer et al. 2016, Plaza et al. 2018. ...
Article
Lead poisoning of raptors is an ongoing and pervasive global conservation concern with potentially significant impacts for some species and populations. This Conservation Letter provides a scientific review of raptor lead poisoning globally and concludes by highlighting lessons learned and potential solutions. This letter is not intended as an exhaustive literature review. Rather, the intent of the Raptor Research Foundation (RRF) is to provide readers with enough evidence-based examples that they can appreciate the scope and prevalence of lead poisoning, understand the potential effects on raptor species and populations, and gain a basic understanding of the challenges associated with addressing lead poisoning of raptors across regions. Lead is a nonessential metal that has a variety of uses in modern society including ammunition, fuel additives, and storage batteries. The same properties that make lead useful for anthropogenic applications worldwide—resistance to corrosion and low mobility—cause lead to remain in host environments for millennia (Jørgensen and Willems 1987, Davies et al. 1990). The mining, manufacturing, combustion, recycling, and disposal of lead and lead products has resulted in lead concentrations in the atmosphere, soil, and water that are several orders of magnitude higher than naturally occurring concentrations (Franson and Pain 2011). Emissions of lead into the air and water enable lead to be inhaled or ingested, the two most common pathways of exposure to terrestrial vertebrates (Franson and Pain 2011). Exposure to lead, a highly poisonous neurotoxin, has been documented among raptor species worldwide (e.g., Haig et al. 2014, Krone 2018). The primary route of exposure is ingestion, typically through consumption of prey items containing lead fragments (Katzner et al. 2018, Krone 2018). Although lead does not generally appear to bioaccumulate through the food chain, secondary poisoning has been documented in raptors (e.g., Feierabend and Myers 1984). Lead poisoning can also be a secondary effect of shooting (persecution) when the shooting event itself is nonlethal, but lead remains lodged in the body (Berny et al. 2017). For more information on persecution, see the Conservation Letter: Raptor Persecution (Madden et al. 2019). Effects of Lead Poisoning on Raptors. The lethal and sublethal effects of lead on raptors have been well documented (e.g., Watson et al. 2009, Krone 2018). Lead enters the bloodstream after being broken down by stomach acids following ingestion or is absorbed through the lungs after inhalation. After entering the bloodstream, lead is transported to soft tissues such as the kidney and liver and eventually to the skeletal system where lead replaces vital nutrients such as calcium in the bone matrix (Scheuhammer 1987, Gangoso et al. 2009). Blood lead concentrations can be reflective of both recent and past exposure events, as lead can be released from skeletal repositories back into the bloodstream; feathers, kidney, and liver reflect lead exposure over a moderate term, and bones reflect long-term or even life-time exposure (Franson and Pain 2011). Lead in the blood causes anemia even at low levels of exposure, and acute lead poisoning can result in kidney failure, liver lesions and swelling, enlarged gall bladder, brain lesions, and fibrin exudations under the pericardium (as reviewed in Krone 2018). What constitutes lethal concentrations of lead varies by species, with Turkey Vultures (Cathartes aura) and several hawk species being fairly tolerant of repeated lead exposure (Friend 1999, Carpenter et al. 2003) whereas California Condors (Gymnogyps californianus) and Andean Condors (Vultur gryphus) suffer high mortality rates from lead poisoning (Pattee et al. 2006, Finkelstein et al. 2010). Sublethal lead exposure can result in lower fecundity (Pain et al. 2009) as well as indirect mortality. Elevated concentrations of lead can cause increased bone fragility, decreased vision via ocular lesions, and higher susceptibility to infections (as reviewed in Krone 2018), all of which can compromise the ability of a lead-poisoned individual to forage effectively or maneuver in flight (Burger 1995, Ecke et al. 2017). For example, research on Steller's Sea-Eagles (Haliaeetus pelagicus) and White-tailed Eagles (Haliaeetus albicilla) in Japan by Saito (2009) found that victims of vehicle collisions and electrocutions often had high concentrations of lead, and some individuals previously thought to have died of starvation had evidence of lead poisoning. Measuring the concentrations of lead in injured or dead raptors is not routinely performed for most species; thus, the proportion of indirect mortality caused by lead poisoning is likely underestimated (e.g., Wayland et al. 2003). Sources of Lead Poisoning. There is a worldwide consensus that the most important source of lead poisoning in raptors comes from the ingestion of lead pellets and fragments from ammunition, with lead fishing tackle being of next greatest concern (Fisher et al. 2006). A review by Schulz et al. (2002) demonstrated that some areas in Missouri, USA, may have as much as one million lead shot pellets/ha. A recent review of lead poisoning in the northern Peruvian Amazon River basin by Cartró-Sabaté et al. (2019) found significant concentrations of lead in many non-raptor species, due primarily to subsistence hunting, which is permitted only for indigenous communities. Increasing awareness of this issue has led many countries to impose regulations regarding the use of lead ammunition and fishing tackle (e.g., USA, Argentina, see below); however, lead ammunition remains unregulated in many regions of the world (Avery and Watson 2009, Plaza et al. 2018). The amount of lead entering the environment from fishing tackle varies by location. One study estimated that in Poland, 1000–1500 metric tons of lead sinkers were lost annually (Hansen et al. 2004). Areas with exceptionally high fishing pressure may pose an important threat to waterfowl (e.g., Scheuhammer and Norris 1996, Haig et al. 2014). Raptor species that feed on waterfowl (e.g., Bald Eagle [Haliaeetus leucocephalus], White-tailed Eagle) are therefore at risk due to secondary ingestion of lead fishing tackle (Rattner et al. 2008, Ishii et al. 2017). Improvements are still needed to quantify the amount of lead entering aquatic ecosystems (Rattner et al. 2008). Other sources of lead exposure exist but are rarely documented in raptors. Researchers evaluating the effect on Osprey (Pandion haliaetus) of lead exposure from mining found no significant effects of lead from this source (Henny et al. 1991, Langner et al. 2012). However, if there is chronic exposure to low concentrations of lead, the effects could be subtle but significant. Unfortunately, investigating the effects of chronic exposure is challenging due in part to costly postmortem examinations. Microtrash is a known source of lead exposure for raptors, specifically scavengers like condors. However, the degree of lead poisoning risk from ingestion of microtrash and other debris is still unknown (Finkelstein et al. 2015). This research topic needs greater study, especially for raptor species that forage near urban areas and have greater exposure to e-waste. Regardless of the relative contribution of different sources of lead to poisoning in raptors, exposure sources likely act cumulatively, increasing the severity of exposure. Implications to Global Raptor Populations. Worldwide, lead exposure has been documented in at least 42 predatory and scavenging bird species (Fisher et al. 2006, Pain et al. 2019). Feeding ecology is the primary predictor of lead exposure among raptor species, with exposure directly correlated to the extent a species scavenges (Slabe et al. 2020). New and Old World vultures and condors are susceptible year-round due to their ecological role as obligate scavengers. Conversely, facultative scavengers such as Aquila and Haliaeetus eagles are most susceptible during periods when they scavenge rather than periods when they focus on live prey (Slabe et al. 2020). Whereas some obligate scavengers appear to be the most susceptible to population-level impacts from lead, susceptibility varies among both obligate and facultative scavengers. Vultures and condors are particularly susceptible to lead poisoning yet remain poorly studied worldwide with the exception of a few species (Plaza and Lambertucci 2019). The California Condor, a critically endangered species, is the highest profile avian scavenger affected by lead poisoning (Church et al. 2006). Lead exposure in the California Condor lowers reproductive rates and lead toxicosis is the primary cause of death in wild populations of adult individuals (Cade 2007, Finkelstein et al. 2012, Rideout et al. 2012). Andean Condors (near-threatened) are also known to be susceptible to lead poisoning (Pattee et al. 2006); however, studies on free-living individuals have been limited to a few studies conducted in southern Chile and Argentina. Here, introduction of exotic species for hunting purposes (Lambertucci et al. 2011) has led to an increase in the use of lead ammunition. At the same time, the increasing number of exotic animals has also shifted the Andean Condor's diet to almost exclusively introduced wild and domestic animals (Lambertucci et al. 2009). The change in diet together with the increase in hunting has led to an increase in ingestion of lead ammunition from carcasses, the main source of lead poisoning in Andean Condors (Lambertucci et al. 2011). Although it has been documented that the species is especially susceptible to lead poisoning (Pattee et al. 2006), the impacts on populations are poorly understood (Wiemeyer et al. 2016, Plaza et al. 2018). A number of vulture species for which the IUCN conservation status is endangered or critically endangered are susceptible to lead poisoning. For example, lead poisoning is thought to be a major threat to Egyptian Vultures (Neophron percnopterus; endangered), which have elevated lead concentrations in multiple European countries (Gangoso et al. 2009, Plaza and Lambertucci 2019). In Africa, Cape Vultures (Gyps coprotheres; endangered), Lappet-faced Vultures (Torgos tracheliotos; endangered), and White-backed Vultures (Gyps africanus; critically endangered) have high lead concentrations in areas of trophy hunting, an important source of tourism income (Naidoo et al. 2012, Garbett et al. 2018, Plaza and Lambertucci 2019). In Asia, Long-billed Vultures (also known as Indian Vultures; Gyps indicus; critically endangered) and White-rumped Vultures (Gyps bengalensis; critically endangered) also have documented lead poisoning (Plaza and Lambertucci 2019). More studies are needed in Africa and Asia, areas experiencing rapid declines in vulture populations, to understand the overall impacts of lead poisoning to vulture species. Multiple species of raptors that are facultative scavengers are also susceptible to lead poisoning, with global studies of lead exposure overwhelmingly focused on Aquila and Haliaeetus eagles. In Europe, researchers found that breeding success in Bonelli's Eagles (Aquila fasciata; endangered) was negatively affected by the ingestion of lead pellets present in small-game prey items (Gil-Sánchez et al. 2018). Lead exposure in Australian raptors is poorly studied; nonetheless, one study revealed that 27% of Wedge-tailed Eagles (Aquila audax; least concern) had elevated lead concentrations (Lohr et al. 2020). Golden Eagles (Aquila chrysaetos; least concern), a circumpolar apex predator, have documented lead exposure in the European Alps (Madry et al. 2015), the United Kingdom (Pain et al. 1995), and North America (Langner et al. 2015). Lead poisoning is estimated to cause between 2.1% and 4.8% of Golden Eagle mortality in the USA (Russell and Franson 2014, US Fish and Wildlife Service 2016) but may be underestimated as a result of reporting bias (e.g., Crandall et al. 2019). Lead exposure in Haliaeetus eagles increases when carcasses and gut piles containing lead fragments from ammunition are used as a food source (Nadjafzadeh et al. 2013, Slabe et al. 2020). In Japan, the discovery of lead poisoning in Steller's Sea Eagle (vulnerable) and White-tailed Eagles resulted in ammunition restrictions for hunting (see below). Studies in Germany, Poland, and Japan revealed lead concentrations consistent with poisoning in the vital organs of White-tailed Eagles (Helander et al. 2009, Krone et al. 2009, Kitowski et al. 2017). Lead poisoning is the most significant source of anthropogenic mortality of this species in Finland (Isomursu et al. 2018). In the USA, lead poisoning accounted for 16.3% of 2980 Bald Eagle (least concern) deaths between 1975 and 2013 (Russell and Franson 2014). Lead Remediation Efforts. Multiple legislative actions have been enacted worldwide to reduce the use of lead ammunition. In total, 33 countries have implemented some level of restriction on lead ammunition, with the majority of these restrictions enacted for the protection of waterfowl and wetlands (Stroud 2015). Australia has a number of hunting regulations, and along with New Zealand imposes restrictions on certain types or uses of lead shot (Avery and Watson 2009). Several African countries also have hunting regulations, with Mauritania setting the example in 1975 by prohibiting the use of lead ammunition for large game and sport hunting (Avery and Watson 2009). South Africa has a regulation prohibiting the use of lead shot for waterfowl hunting (Avery and Watson 2009). The European countries of Denmark, Sweden, and the Netherlands have passed some of the most stringent laws, resulting in countrywide bans on the use of lead ammunition (Mateo and Kanstrup 2019). France, Sweden, and Germany have banned the use of lead ammunition in wetlands and for waterfowl hunting. Countries in South America are increasingly concerned about the use of lead ammunition. For example, two provinces in Argentina have taken pioneering actions to prohibit the use of lead ammunition in wetland ecosystems. In addition, Argentina, Chile, Brazil, Uruguay, Paraguay, Bolivia, Ecuador, and Peru have signed the Convention on Migratory Species, committing to gradually eliminate the use of lead ammunition (Plaza et al. 2018). However, to date, many of these countries have not implemented restrictions. In the USA, California recently enacted a statewide ban on lead ammunition primarily as a result of continued population-level effects of lead on the California Condor. Three other laws have been enacted as a result of concern for a single raptor species: (1) a lead ammunition ban for waterfowl hunting in the USA was passed to protect Bald Eagles, (2) a ban in Germany on lead ammunition was passed due to concern for White-tailed Eagles (Thomas et al. 2019) and, (3) a lead ammunition ban in Hokkaido, Japan was enacted to protect Haliaeetus eagles (Saito 2009, but see voluntary program below). Multiple lead remediation efforts in the USA have utilized on-the-ground communication and education efforts to encourage the voluntary use of non-lead ammunition. Voluntary programs are particularly important because on-the-ground actions can result in immediate behavior changes within the hunting community without the political and cultural divisiveness often associated with legislation. A successful non-lead ammunition outreach and distribution program in northwest Wyoming resulted in >50% voluntary participation in hunters employing non-lead ammunition for elk hunting (Bedrosian et al. 2012). An ongoing multi-year outreach and non-lead ammunition distribution program in the Arizona range of the California Condor by the Arizona Game and Fish Department and The Peregrine Fund has maintained an average annual rate of 87% hunter participation (Sieg et al. 2009; C. Parish, The Peregrine Fund, pers. comm.). A pilot effort by the Oregon Zoo's Non-lead Hunting Education Program, in coordination with The Nature Conservancy, Oregon Hunters Association, and Oregon Department of Fish and Wildlife, increased non-lead ammunition use to 77% of cow elk hunters on the Zumwalt Prairie Preserve over a 4 yr period and is now being adopted statewide (L. Brown, Oregon Zoo, pers. comm.). As of July 2020, the Arizona Game and Fish Department, the Utah Department of Natural Resources, the Oregon Department of Fish and Wildlife, and 25 hunting and conservation organizations, had signed a resolution to partner with the North American Non-lead Partnership (NANP, www.nonleadpartnership.org). Through this partnership, these state agencies and organizations promote the voluntary use of non-lead ammunition to licensed hunters as a form of conservation and stewardship action for scavenging wildlife (Spurling et al. 2018). The NANP promotes the use of non-lead ammunition through communication, education, and incentives, with a focus on both wildlife conservation and hunting heritage within the framework of the North American Model of Wildlife Conservation. The ban of lead ammunition in Hokkaido, Japan, is one example where on-the-ground voluntary efforts effected a regulatory change. A civic group led by veterinarians was established in July 1998 (Saito 2009). They organized activities to prevent lead poisoning of Haliaeetus eagles including bringing in debilitated or dead eagles, patrolling hunting areas, disposing of deer carcasses and offal (as much as 1 ton/d), purchasing nontoxic ammunition for the local hunting association, and creating and publishing educational materials about lead poisoning in raptors. 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While genetic diversity of threatened species is a major concern of conservation biologists, historic patterns of genetic variation are often unknown. A powerful approach to assess patterns and processes of genetic erosion is via ancient DNA techniques. Herein, we analyzed mtDNA from historical samples (1800s to present) of Andean Condors (Vultur gryphus) to investigate whether contemporary low genetic variability is the result of recent human expansion and persecution, and compared this genetic history to that of California condors (Gymnogyps californianus).We then explored historic demographies for both species via coalescent simulations. We found that Andean condors have lost at least 17% of their genetic variation in the early 20th century. Unlike California condors, however, low mtDNA diversity in the Andean condor was mostly ancient, before European arrival. However, we found that both condor species shared similar demographies in that population bottlenecks were recent and co‐occurred with the introduction of livestock to the Americas and the global collapse of marine mammals. Given the combined information on genetic and demographic processes, we suggest that the protection of key habitats should be targeted for conserving extant genetic diversity and facilitate the natural recolonization of lost territories, while nuclear genomic data should be used to inform translocation plans.
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... It is considered Threatened in Argentina, where populations are larger than in other areas, but showing signs of retraction (Aves Argentinas, 2017). It is negatively affected by several human disturbances (Alarcón and Lambertucci, 2018b;Speziale et al., 2008;Wiemeyer et al., 2017). In our study area, there are at least around 300 individuals (Lambertucci, 2010), which mainly feed on large carcasses of sheep, red deer (Cervus elaphus), and cows, but also hares (Lepus europaeus) (Ballejo et al., 2018;Lambertucci et al., 2009b). ...
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Rubbish dumps can become an important environmental source of plastic. Several species feed on organic waste from these sites, but at the same time are exposed to non-organic materials. Species that can gather food in these sites might at the same time disperse waste consumed, but this has rarely been evaluated. We compare the occurrence of plastic debris in regurgitated pellets of three sympatric vultures from northwest Patagonia, Andean condors (Vultur gryphus), black vultures (Coragyps atratus) and turkey vultures (Cathartes aura), foraging in different degrees of humanized sites. We also evaluate the influence of rubbish dumps in the presence of plastic debris in pellets of the studied species and their potential role in spreading plastic to the environment. Most synthetic material present in pellets was plastic. Pellets of Andean condors, which avoid disturbed anthropic sites in this area, showed almost no plastic debris compared with the other sympatric vulture species, suggesting an influence of the foraging habits on plastic ingestion. For black and turkey vultures, we found that dumps may be an important source of plastic. The occurrence of plastic debris in pellets of black vultures sampled in 2010 and 2020 increased, probably associated with the increase in urbanization and waste production in the study area. Avian scavengers were exposed to and are able to transport plastic to distant communal roosts generating "plastic islands". It is necessary to reduce plastic generation and better waste management practices to avoid species and environments to be affected by this pollutant.
... Several studies in recent years have identified signs of Pb poisoning in birds of prey that were found dead or sick, being Pb poisoning identified in some cases as the cause for up to 67% of the recorded mortality events (Rideout et al., 2012;Franson and Russell, 2014;Berny et al., 2015;Jenni et al., 2015;Wiemeyer et al., 2017;Ishii et al., 2017;Kitowski et al., 2017;Ganz et al., 2018;Isomursu et al., 2018;Simon et al., 2020). Most of these studies may have sampling biases related to the method of carcass collection or selection that make it difficult to estimate, from the observed mortality, the actual incidence of Pb poisoning on the populations where the dead animals come from. ...
Article
The ingestion of lead (Pb) ammunition is the most important exposure pathway to this metal in birds and involve negative consequences to their health. We have performed a passive monitoring of Pb poisoning in birds of prey by measuring liver (n = 727) and blood (n = 32) Pb levels in individuals of 16 species found dead or sick in Spain between 2004 and 2020. We also performed an active monitoring by measuring blood Pb levels and biomarkers of haem biosynthesis, phosphorus (P) and calcium (Ca) metabolism, oxidative stress and immune function in individuals (n = 194) of 9 species trapped alive in the field between 2016 and 2017. Passive monitoring results revealed some species with liver Pb levels associated with severe clinical poisoning (>30 μg/g d.w. of Pb): Eurasian griffon vulture (27/257, 10.5%), red kite (1/132, 0.8%), golden eagle (4/38, 10.5%), and Northern goshawk (1/8, 12.5%). The active monitoring results showed that individuals of bearded vulture (1/3, 33.3%), Eurasian griffon vulture (87/118, 73.7%), Spanish imperial eagle (1/6, 16.7%) and red kite (1/18, 5.6%) had abnormal blood Pb levels (>20 μg/dL). Blood Pb levels increased with age, and both monitoring methods showed seasonality in Pb exposure associated with a delayed effect of the hunting season. In Eurasian griffon, blood Pb concentration was associated with lower δ-ALAD activity in blood and P levels in plasma, and with higher blood lipid peroxida-tion and plasma carotenoid levels in agreement with other experimental and field studies in Pb-exposed birds. The study reveals that Pb poisoning is a significant cause of death and sublethal effects on haem biosynthesis, P metabolism and oxidative stress in birds of prey in Spain.
... The Andean condor is the largest New World vulture (weighing up to almost 16 kg, wingspan 3 m; Alarcón et al., 2017;del Hoyo, Elliott, & Sargatal, 1994), and it is classified worldwide by the International Union for Conservation of Nature (IUCN) Red List as Near Threatened (IUCN, 2017). Currently, Andean condors are suffering important conservation problems such as lead contamination, intentional and unintentional poisoning, human persecution, and collision with power lines, causing health alterations that require their rehabilitation (Alarcón & Lambertucci, 2018;Pavez & Estades, 2016;Wiemeyer et al., 2017). The wild population of Andean condors studied is among the largest in their distribution range, with approximately 300 individuals (Lambertucci, 2010). ...
Article
Carotenoids are pigmented compounds acquired through diet that have important functions as antioxidants and immune modulators. We studied the association between immunity and circulating carotenoids in Andean condors (Vultur gryphus ). We evaluated the relationship between α‐, β‐, and γ‐globulin blood concentrations and different circulating carotenoids in two groups of Andean condors that differ in their mean health status, rehabilitating (suffering different pathologies), and wild individuals (trapped when displaying their physiological behavior). In rehabilitating individuals, α‐, β‐, and γ‐globulin concentrations were higher than in wild individuals. This shows that rehabilitating individuals were developing an immune response associated with the pathologies that they were suffering at the time of sampling. In addition, circulating carotenoids were lower in rehabilitating than in wild individuals. We found negative correlations between α‐, β‐, and γ‐globulins and different circulating carotenoids in rehabilitating individuals, but not in wild condors. Xanthophylls were strongly related to α‐, β‐, and γ‐globulin blood concentrations in rehabilitating, but not in wild condors. Our results suggest that there is a potential relationship between circulating carotenoids and immunity in the Andean condor. Given that this species may display a carotenoid‐based pigmentation, our results could suggest that a trade‐off between the immune system and external coloration could operate in this species, which may have implications in their access to food resources and mate selection and, thus, in their conservation. HIGHLIGHTS • Wild and rehabilitating condors differed in their health status. • We found negative correlations between globulins and blood carotenoids in rehabilitating, but not in wild condors. • We suggest a relationship between blood carotenoids and immunity.
... However, according to the International Union for Conservation of Nature (IUCN) Red List, Andean condor populations are globally near-threatened and declining (BirdLife International, 2019), because, besides having very low reproductive rates, they have been threatened by anthropogenic effects such as: poisoning by pesticides, lead ammunition and toxic baits, collisions with power lines, poaching, snare traps and decrease in food (Campbell, 2016;Pavez & Estades, 2016;Wiemeyer et al., 2017). Although vulture species are essential for ecosystem health and functioning, providing a highly effective sanitation service (Monadjem, Kane, Botha, Kelly, & Murn, 2018;Muñoz-Lozano et al., 2019;Ogada, Keesing, & Virani, 2012), they have experienced the most rapid decline in conservation status of any group of birds over the past decade and comprise the most threatened avian group in the world (Buechley & Şekercioğlu, 2016a(Buechley & Şekercioğlu, , 2016bOgada et al., 2012). ...
Article
Critical priority pathogens have globally disseminated beyond clinical settings threatening wildlife. Andean Condors are essentials for ecosystem health and functioning, but their populations are globally near threatened and declining due to anthropogenic activities. During a microbiological and genomic surveillance study of critical priority antibiotic-resistant pathogens we have identified pandemic lineages of multidrug-resistant extended-spectrum β-lactamase (ESBL)-producing Escherichia coli colonizing Andean Condors admitted at two wildlife rehabilitation centres in South America. Genomic analysis revealed presence of genes encoding resistance to hospital and health-care agents among international E. coli clones belonging to sequence types (STs) ST162, ST602, ST1196 and ST1485. In this regard, resistome included genes conferring resistance to clinically important cephalosporins [i.e., CTX-M-14, CTX-M-55 and CTX-M-65 extended-spectrum β-lactamase (ESBL) genes], heavy metals (arsenic, mercury, lead, cadmium, copper, silver), pesticides (glyphosate), and domestic/hospital disinfectants (QACs), suggesting a link with anthropogenic environmental pollution. On other hand, presence of virulence factors, including astA gene associated with outbreak of childhood diarrhoea and extraintestinal disease in animals, were identified, whereas virulent behaviour was confirmed using the Galleria mellonella infection model. E. coli ST162, ST602, ST1196 and ST1485 have been previously identified in humans and food-producing animals worldwide, indicating that a wide resistome could contribute with rapid adaptation and dissemination of these clones at the human-animal-environment interface. Therefore, these results highlight that Andean Condors have been colonized by critical priority pathogens, becoming potential environmental reservoirs and/or vectors for dissemination of virulent and antimicrobial-resistant bacteria and/or their genes, in associated ecosystems and wildlife.
... The conservation concerns that affect condors are similar to those that other vultures in the world (Lambertucci and Speziale, 2009). Although lead poisoning is being widely studied (Plaza et al., 2018;Plaza and Lambertucci, 2019;Wiemeyer et al., 2017) poisonings due to the consumption of carrion poisoned by cattle ranchers and the effect that this practice can have on the natural populations of condors, has not yet been addressed. ...
Article
Highlights • Pesticide poisoning is currently the greatest threat to the Andean condor. • Poisonings affect adult condors more than immature ones. • The most commonly used poison is Carbofuran, and to a lesser extent Palation. • Condor poisonings have reached alarming levels that could lead to extinction.
... Lead (Pb) is a naturally occurring but nonessential element that is highly toxic at elevated concentrations and with a potential to affect most body systems in animals. Exposure to Pb and incidences of Pb poisoning have been extensively reported for several diurnal birds of prey around the world, notably eagles and vultures (Wayland and Bollinger 1999;Kurosawa 2000;Church et al. 2006;Pattee et al. 2006;Krone et al. 2009;Franson and Russel 2014;Berny et al. 2015;Mateo-Tomás et al. 2016;Ecke et al. 2017;Wiemeyer et al. 2017;Isomurso et al. 2018), and scarcely for the mainly nocturnal Eurasian eagle owl Bubo bubo (Mateo et al. 2003, Kim andOh 2012) and great horned owl Bubo virginianus (Clark and Scheuhammer 2003). Mortality from Pb poisoning in birds is mostly associated with ingestion of lead-shot or bullet fragments of hunting ammunition and associated with feeding habits occurring mainly in various ducks and raptorial birds (summarized in Franson and Pain 2011). ...
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Patterns of lead and other trace metals were examined in 122 Eurasian eagle owls Bubo bubo found dead in Sweden in the period 1978–2013. Environmental lead (Pb) has decreased over recent decades from reduced anthropogenic emissions but mortality by Pb poisoning is still frequently reported for avian raptors and scavengers exposed to Pb ammunition. One objective here was to determine if Pb concentrations in a nocturnal non-scavenging raptor follow the general decline observed in other biota. Pb concentration in owl liver was significantly correlated with body weight, sex, latitude, longitude and season. Pb showed a significant decreasing trend towards north and west. Starved birds had significantly higher concentrations. Total Pb concentrations in liver averaged 0.179 μg g⁻¹ dry weight (median 0.103) and decreased by 5.6% per year 1978–2013, or 5.3% after adjustment for confounding factors, similar to trends in other species. Among 14 other trace elements only antimony and arsenic showed decreasing trends. Lead isotope ratios ²⁰⁶Pb/²⁰⁷Pb and ²⁰⁸Pb/²⁰⁷Pb increased from 1.138 and 2.408 in 1978–1985 to 1.170 and 2.435 in 2010–2013, respectively, demonstrating that the decreasing Pb concentration in eagle owl is related to the phase-out of leaded gasoline in Europe, where Pb additives had much lower isotope ratios than natural lead in Swedish soils. Only one incidence of suspected Pb poisoning (40.7 μg g⁻¹ in liver) was observed indicating that poisoning from ingestion of metallic lead is rare (< 1%) in eagle owl in Sweden, in contrast to what has been reported for eagles.
... However, one of the main sources of metal contamination there could be volcanic eruptions (e.g. As, Cu, Zn, Cr, Si) (Bubach et al., 2015;Conti et al., 2016;Ruggieri et al., 2012), or lead from hunting (Lambertucci et al., 2011;Wiemeyer et al., 2017). Studies on metal pollution in terrestrial ecosystems represent only 4% (n = 28) (Fig. 5). ...
Article
Emissions of metals and metalloids (Hg; Cd; Cr; Cu; Pb; Ni; Zn; Fe; Mn; As; Se) generated by natural (e.g.,geothermal activity) or anthropic causes (eg., industry or mining) represent a worldwide contamination problem, especially in developing countries. Exposure to high concentrations of these elements is harmful to living beings, including humans. Information on this type of contamination is scarce and fragmented, limiting research which could benefit from these data. To know the state of the research, we reviewed the studies of environmental pollution by metals and metalloids carried out on animal species in Latin America. The use of animals as biomonitors of contamination by metals and metalloids is a continuously expanding practice that allows for early detection of problems. With this work, we were able to identify the most studied areas in Latin America(Amazon, Gulf of California, coastal area between Rio de Janeiro and Florianopolis and River Plate Estuary). Moreover, we provide information on the most studied metals (Hg, Cd, Cu, Pb, Zn) and wild species, which evidence the use of endangered species. The data reviewed should help researchers to direct their efforts towards sparsely researched areas and facilitate bibliographic consultation of scientific information on exposure to metals and metalloids in Latin America.
... com. cited in Wiemeyer et al. 2017). In a study of wild California condors, Finkelstein et al. (2014) found one bird that had been shot and retained embedded birdshot (small sized gunshot) in its tissues. ...
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Poisoning of wild birds following ingestion of lead from ammunition has long been recognised and considerable recent research has focused on terrestrial birds, including raptors and scavengers. This paper builds upon previous reviews and finds that both the number of taxa affected and geographical spread of cases has increased. Some lead may also be absorbed from embedded ammunition fragments in injured birds which risk sub-lethal and welfare effects. Some papers suggest inter-specific differences in sensitivity to lead, although it is difficult to disentangle these from other factors that influence effect severity. Sub-lethal effects have been found at lower blood lead concentrations than previously reported, suggesting that previous effect-level ‘thresholds’ should be abandoned or revised. Lead poisoning is estimated to kill a million wildfowl a year in Europe and cause sub-lethal poisoning in another ≥ 3 million. Modelling and correlative studies have supported the potential for population-level effects of lead poisoning in wildfowl, terrestrial birds, raptors and scavengers.
... Rodriguez-Ramos Fernandez et al. (2011) concluded that the use of lead-free ammunition in upland hunting would reduce potential lead exposure to the Spanish Imperial Eagle and contribute to its recovery. A similar situation exists for the Andean Condor (Vultur gryphus), in which high levels of bone and blood lead indicate that the species is threatened at the continental level across South America (Wiemeyer et al. 2017). Ferreya et al. (2015) indicated that serious sub-clinical effects of lead that may pre-dispose animals (waterfowl) to mortality are equally important to consider as observed mortality in favoring adoption of non-lead ammunition. ...
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This review presents evidence of lead exposure and toxicity to wildlife and humans from spent shotgun and rifle ammunition and fishing weights, and the barriers and bridges to completing the transition to non-lead products. Despite the international availability of effective non-lead substitutes, and that more jurisdictions are adopting suitable policies and regulations, a broader transition to non-lead alternatives is prevented because resolution remains divided among disparate human user constituencies. Progress has occurred only where evidence is most compelling or where a responsible public authority with statutory powers has managed to change mindsets in the wider public interest. Arguments opposing lead bans are shown to lack validity. Differing national regulations impede progress, requiring analysis to achieve better regulation. Evidence that lead bans have reduced wildlife exposure should be used more to promote sustainable hunting and fishing. Evidence of the lead contribution from hunted game to human exposure should shape policy and regulation to end lead ammunition use. The Special Issue presents evidence that a transition to non-lead products is both warranted and feasible.
... 2,6-8 These long-term deleterious effects on individuals can have a negative effect on local populations. 6,9 The reproductive system can also be affected, resulting in decreased reproductive success through abnormal spermatogenesis, decreased fertility in females, fetal development abnormalities, miscarriage, premature membrane rupture and preeclampsia, as well as a delay in fetal growth and postnatal neurotoxic effects. [10][11][12] The Tasmanian devil, Sarcophilus harrisii, is the largest marsupial carnivore remaining in Tasmania since the last thylacine (Thylacinus cynocephalus) died in the 1930s. ...
Article
Background The Tasmanian devil (Sarcophilus harrisii) is the world’s largest extant marsupial carnivore. Since the emergence of devil facial tumour disease in 1996, the species has undergone a severe population decline. The insurance population (IP) was established in 2006 to build a disease‐free captive population to maintain 95% of the wild Tasmanian devil genetic diversity for 50 years. Captive and semi‐wild Tasmanian devils are fed with possum and wallaby meat provided by local hunters, who use lead ammunition. Lead ingestion can cause acute toxicity, including ataxia, coma and death, or chronic subclinical deleterious effects including decreased fertility. Methods We determined blood lead concentrations in 26 captive and 133 wild Tasmanian devils from various sites across Tasmania. Results Captive Tasmanian devils showed significantly higher blood lead concentrations than their conspecifics in the wild. In captivity, older animals had higher blood lead concentrations than young animals, which suggested regular exposure, as lead can accumulate in a living organism in the blood, soft tissues and bones. After a response measure was implemented by removing the heads and wounds containing lead from the diet, blood concentrations significantly decreased in animals at one of the captive study sites, supporting the suspicion of food as the source of lead. Conclusion This study highlights the need to ensure meat fed to captive carnivores is not contaminated by lead, especially in the context of a conservation program breeding individuals in captivity, as for Tasmanian devils.
... The use of lead ammunition and the current lack of regulation in many countries could be inadvertently increasing lead availability for many species in the environment, in particular for scavenger species (Watson et al. 2009, Lambertucci et al. 2010. In fact, hunting activities have been shown to cause accumulation of lead in the environment and in the predators and humans that consume the leporids (Fisher et al. 2006, Wiemeyer et al. 2017. Therefore, leporids may be an important source of this problem for carnivores and humans (which is particularly concerning for children and pregnant women; Watson et al. 2009); however, this relationship has been poorly evaluated in both native and exotic ranges. ...
Article
• Historically, humans have translocated some species of Leporidae (order Lagomorpha) around the world as an introduced food source and as game species. This family is now cosmopolitan and occupies areas where it did not previously exist. With the exception of European rabbits Oryctolagus cuniculus, evidence of the effects of these introduced species is scattered and in many cases anecdotal, though they share many biological traits with Oryctolagus cuniculus, one of the most harmful invasive species worldwide. • We review available studies on the 12 leporid species that have been introduced by humans to areas beyond their native ranges. Our aim is to describe and compare the species’ ecological roles in their native geographic ranges and in their exotic ranges. We review the species’ effects on the ecosystem at different levels of the trophic chain. We also evaluate the consequences of introductions for animal and human health, and their economic consequences, and we consider control measures. • In their native ranges, the 12 leporids are known to provide resources for other species, act as seed dispersers and ecosystem engineers, function as primary prey items for several predator species, and have many other functions. The effects of the leporids in their exotic geographic ranges are also conspicuous, and in many cases strongly negative, due to competition with native fauna and the facilitation of the presence of other invaders. Nonetheless, they constitute a food resource for native and exotic predators. As game species for humans, their hunting may indirectly impact the ecosystems by increasing the amount of lead in the environment. Moreover, they may be carriers of zoonotic diseases. • Conservation biologists should carefully consider the contrasting effects of the introduced leporids species in the ecosystem before developing any management strategy including these species.
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Lead poisoning is an important global conservation problem for many species of wildlife, especially raptors. Despite the increasing number of individual studies and regional reviews of lead poisoning of raptors, it has been over a decade since this information has been compiled into a comprehensive global review. Here, we summarize the state of knowledge of lead poisoning of raptors, we review developments in manufacturing of non‐lead ammunition, the use of which can reduce the most pervasive source of lead these birds encounter, and we compile data on voluntary and regulatory mitigation options and their associated sociological context. We support our literature review with case studies of mitigation actions, largely provided by the conservation practitioners who study or manage these efforts. Our review illustrates the growing awareness and understanding of lead exposure of raptors, and it shows that the science underpinning this understanding has expanded considerably in recent years. We also show that the political and social appetite for managing lead ammunition appears to vary substantially across administrative regions, countries, and continents. Improved understanding of the drivers of this variation could support more effective mitigation of lead exposure of wildlife. This review also shows that mitigation strategies are likely to be most effective when they are outcome driven, consider behavioural theory, local cultures, and environmental conditions, effectively monitor participation, compliance, and levels of raptor exposure, and support both environmental and human health.
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The concentrations of mercury (Hg) and lead (Pb) in feather samples of nine bird’s species (n = 65) were determined from southeastern areas of Iran, Hamun International Wetlands. Hg concentrations were ranged from 0.40 to 3.00 mg/kg dry wt and from 0.38 to 1.76 mg/kg for primary and secondary feathers, respectively. Furthermore, Pb concentrations were ranged from 1.43 to 4.10 mg/kg and from 1.28 to 3.65 mg/kg for primary and secondary feathers, respectively. Deposition of metals varied significantly among the primary and secondary feathers of systematic category (families) for Hg and Pb (p < 0.001). It was found that there is a significant difference in feather Hg and Pb concentrations across species (p < 0.001) with highest concentrations in saker falcon (Falconidae) (Hg = 3.00 mg/kg and Pb = 4.10 mg/kg, primary feather) followed by little owl (Strigidae). Grey francolin (Phasianidae) contained the least amount of Hg (0.40 mg/kg) and Pb (1.43 mg/kg) in primary feather. The results showed that the highest concentrations of heavy metals were related to carnivores. Fish predators, omnivores, and insectivores were examined at the next level of metal concentration, with herbivores having the lowest concentrations of lead (1.43 mg/kg) and mercury (0.40 mg/kg). Birds with an open grasslands feeding strategy had the highest mercury and lead concentration. The average value for Pb was on the border of harmful effects (4 mg/kg). The results of this study indicate that mercury levels are lower than the threshold level for reproductive and behavioral harm (5 mg/kg).
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Bullets from gunshots made of lead are used to kill and arrest criminals, as they are also used by criminals to intimidate or kill innocents for psychosocial gains. So the increased environmental pollution caused by lead from industries, firearms, gasoline, among others is a source of concern for environmental health specialists, clinical toxicologists, experimental toxicologists, industrial toxicologists and ecotoxicologists. Lead can get into body system accidentally via oral, inhalational, epidermal, dermal, intraperitoneal, and intravenous routes. The toxicokinetic data of lead disposition via various routes of administrations are quite inconsistent. Hence the set blood limit concentration has been considered to be incorrect. In view of this, toxicokinetic data analysis of lead was carried out with intent to determine toxic doses of lead in various organs, and its toxicological consequences. Findings have shown that at lower doses, kinetics of lead is linear (first order), and at higher doses the kinetics becomes non-linear (zero-order). Metabolic processes modulated by lead could be either rate limiting or non–rate-limiting causing induction and inhibition of a myriad of metabolizing enzymes in liver, brain, kidney, intestine and lung. The LD50 of lead bullet in human was 450 mg/kg, which caused death in 9.1 days, and penicillamine (18 mg/kg) can be used for treatment. Mean residence time (MRT) and elimination half-life (T12β) were 25.8 and 18 days, respectively.
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We studied heavy metal levels in floodplain soils of the Innerste River in northern Germany and in the leaves of wild blackberries (Rubus fruticosus L. agg.) growing within and in adjacent areas outside the river floodplain. Heavy metal contamination of the Innerste floodplain is a legacy of historical metal ore mining, processing, and smelting in the Harz Mountains. The heavy metal (Cd, Pb, Zn, Cu, Ni, and Cr) contents of previously studied soil samples from eleven floodplain sites along the Innerste River were re-analyzed statistically, and the levels of these metals in blackberry leaves were determined at five sites. Mean concentrations in the floodplain soils were elevated by factors of 4.59 to 28.5 for Cd, 13.03 to 158.21 for Pb, 5.66 to 45.83 for Zn, and 1.1–14.81 for Cu relative to the precautionary limits for soils stipulated by the German Federal Soil Protection and Contaminated Sites Ordinance. Cadmium, Pb, Zn, Cu, and Ni levels in floodplain soils decreased markedly downstream, as did the concentrations of Cd, Zn, and Ni in the leaves of blackberries from within the floodplain. Levels of Cd, Pb, and Zn in leaves of blackberries from within the floodplain significantly exceeded those of specimens from outside the floodplain. The findings of our study highlight the potential of wild blackberry as a biomonitor of soil pollution by Cd, Pb, and Zn and corroborate the massive heavy metal contamination of floodplain soils along the Innerste River observed in previous studies.
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Consumption of meat from animals hunted with Pb ammunition can cause toxic accumulation with consequent health risks, even if relatively small amounts are consumed in each exposure. In El Palmar National Park, Argentina, invasive alien mammals, wild boar (Sus scrofa) and axis deer (Axis axis), are culled with Pb ammunition and their meat is consumed. In this study, we evaluated blood Pb concentrations in 58 consumers of culled game and examined Pb exposure risk according to their demographics, duty, and consumption habits. Likewise, the likelihood of exposure was evaluated by quantifying Pb concentrations in meat samples of seven culled axis deer. Twenty-seven participants (46%) had detectable blood Pb levels (limit of detection = 3.3 μg/dL), with an average 4.75 ± 1.35 μg/dL (geometric mean ± geometric S.D.); the average for all participants was 3.25 ± 1.51 μg/dL. Blood Pb concentrations were significantly higher in hunters, in participants who reported consuming game meat more than 5 times per week, and in participants who reported frequently consuming cured game meat (compared to cooked or pickled). Pb concentration varied significantly along the trajectory of the bullet in deer muscle, being highest at mid-point but with detectable Pb levels even in distant tissue samples (control), suggesting potential for dietary intake by consumers. These findings provide evidence of Pb exposure risk in consumers and emphasize the relevance of replacing Pb ammunition with non-toxic alternatives. This change would reduce dietary exposure in frequent consumers and allow the use of game meat as safe food for people whilst eliminating collateral risks to wild animals and the environment.
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In recent decades, there has been a growing interest in integrating the social sciences and conservation studies to inform a more realistic management approach. Indeed, an understanding of people's perception of fauna helps in the evaluation of possible conflicts with humans, and provides tools to solve these conflicts. However, perceptions may change along different parts of a species' geographical distribution. Scavenger birds are not exempt from these conflicts as many farmers blame them for attacking and killing livestock. We evaluated the knowledge, perceptions and attitude of people regarding New World vultures along a migratory path in South America. We conducted 114 interviews with farmers in six different localities between Argentine Patagonia and central Bolivia. About half (48.2%) of the interviewees considered vultures harmful to livestock and a substantial number (24.5%) considered killing these birds as a solution for the conflict. The perception of the damage caused by these birds was worse in vultures' wintering and breeding areas, than along the migration route. People with a higher level of education and greater numbers of livestock exhibited more negative perceptions. However, many people (53%) still believed that scavenger birds are important for the environment. Our results suggest that acknowledgment of services provided by scavengers makes killing of scavengers less likely. Educational strategies are needed to increase levels of appreciation toward the ecosystem services provided by vultures, over those of perceived damages.
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The study of wildlife health greatly contributes to understanding population dynamics and detecting conservation threats. The determination of the different fractions of plasma proteins (proteinogram) is an important laboratory tool to study wildlife health. The aim of this study was to characterize protein electrophoresis in wild Andean condors (Vultur gryphus) from north-western Patagonia and to evaluate differences according to age and sex classes. Once reference values of wild, apparently healthy individuals, were established, we compared these values to those of individuals received at the Buenos Aires Zoo in Argentina for rehabilitation due to various health problems. Reference proteinograms from wild Andean condors differed only in the α 1 and β 2-fractions between sex categories. Males showed higher concentrations of these protein fractions than females. We found clear differences between wild birds and rehabilitating individuals. Total proteins, globulins, α 1-globulins, total α-globulins, β 2-globulins, total β-globulins, and γ-globulins were significantly higher in rehabilitating than in wild individuals, whereas albumin, α 2, and β1-globulins were similar between these groups. The albumin/globulin ratio, as a general indicator of health, was significantly lower in rehabilitating than in wild individuals. The results indicate the effects on different protein fractions of pathologic processes occurring in individuals undergoing rehabilitation. Our results provide useful insights, contributing to improving diagnoses and prognoses in this species. This information may also be useful to assess the health status of Andean condors in studies of wild populations and for comparisons with other bird species.
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Despite irrefutable evidence of its negative impact on animal behaviour and physiology, lethal and sublethal lead poisoning of wildlife is still persistent and widespread. For scavenging birds, ingestion of ammunition, or fragments thereof, is the major exposure route. In this study, we examined the occurrence of lead in four avian scavengers of Switzerland and how it differs between species, regions, and age of the bird. We measured lead concentration in liver and bone of the two main alpine avian scavengers (golden eagle Aquila chrysaetos and bearded vulture Gypaetus barbatus) over the entire area of the Swiss Alps and two of the main avian scavengers occurring in the lowlands of Switzerland (red kite Milvus milvus and common raven Corvus corax). Of those four species, only the bearded vulture is an obligate scavenger. We found that lead burdens in the two alpine avian scavengers were higher than those found for the same species elsewhere in Europe or North America and reached levels compatible with acute poisoning, whereas lead burdens of the two lowland avian scavengers seemed to be lower. Several golden eagles, but only one red kite with abnormally high bone lead concentrations were found. In all four species, a substantial proportion of birds had elevated levels which presumably represent recent (liver lead levels) or past (bone lead levels) uptake of sublethal doses of lead.
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Lead contamination is a worldwide problem that affects the health of several bird species and can cause biodiversity loss. However, in South America there is little information about this problem and the species affected. The aim of this study is to compile existing knowledge about lead contamination in South American bird species and propose actions to mitigate this problem. Through a literature search, we found 39 scientific articles on this topic studying 68 bird species. Most studies came from Argentina and Brazil (71.7%), but also from Chile (7.7%), Venezuela (7.7%), Colombia (5.1%), Bolivia (2.6%), Ecuador (2.6%) and Peru (2.6%). Almost all the articles were published between 2001 and 2017. Waterbirds and birds of prey were the avian guilds more studied. Seventy percent of the studies show individuals with lead concentrations that exceed established thresholds levels. The few available articles suggest that lead contamination may be a continental-scale problem produced by different sources like fuels, mining, industries and hunting ammunition. However, lead ammunition seems to be an underestimated source of lead which is producing the highest toxic levels in bird species from South America. To our knowledge, there are regulations about different lead sources but not for lead ammunition in any country, except for some regions in Argentina. The progressive banning of lead from all sources and particularly from hunting ammunition is the main and most effective way to reduce the risk for wildlife. Current obstacles must be overcome through a combined effort of governments, wildlife managers and local communities. © 2018 Associação Brasileira de Ciência Ecológica e Conservação
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We characterized DNA sequence variation in the mitochondrial control region and 12S ribosomal subunit for a sample of Andean Condors (Vultur gryphus) representing populations distributed throughout the species' extensive geographic range (Colombia to central Argentina and Chile). Domains II and III of the control region along with part of the 12S gene were sequenced from 38 individuals (956 base pairs in 30 individuals and 430–824 base pairs for an additional 8 individuals sampled from museum specimens), and Domain I was sequenced from five of these birds (400 base pairs). We identified a total of five haplotypes based on four variable sites distributed over Domains II and III of the control region and the 12S gene. An additional variable site was identified in Domain I. All changes were transitions and no more than three sites differed between any two individuals. Variation in the control region of condors was lower than for most other birds analyzed for these loci. Although low genetic variability is often associated with endangered megafauna, the condor example is notable because the species still maintains a substantial geographic range. Thus, low genetic variability may occur even in megafauna whose ranges have not been severely reduced over recent centuries. Our results therefore suggest that genetic data from geographically widespread megafauna provide important baseline data for assessing the relationship between genetic variability and its causes in other endangered species. Baja Variabilidad Genética en Poblaciones de Vultur gryphus con Amplia Distribución Geográfica Resumen. Caracterizamos la variación de la secuencia de ADN en la región de control mitocondrial y la subunidad ribosomal 12S en una muestra de Vultur gryphus representativa de poblaciones distribuidas a lo largo del extenso rango geográfico de la especie (Colombia, hasta el centro de Argentina y Chile). Los dominios II y III de la región de control, junto con parte del gen 12S, fueron secuenciados en 38 individuos (956 pares de base en 30 individuos y 430–824 pares de base para una muestra adicional de 8 especímenes de museo), y el dominio I fue secuenciado en 5 de estas aves (400 pares de base). Identificamos un total de cinco haplotipos basados en cuatro sitios variables en los dominios II y III de la región de control y el gen 12S. Un sitio variable adicional fue identificado en el dominio I. Todos los cambios fueron transiciones y entre dos individuos cualesquiera no variaron más de 3 sitios. La variación en la región de control de los cóndores fue más baja que para la mayoría de las aves analizadas para estos mismos loci. Aunque la baja variabilidad genética es a menudo asociada con megafauna en peligro de extinción, el ejemplo del cóndor es notable porque la especie aún mantiene un rango geográfico substancial. Así, la baja variabilidad genética se puede dar incluso en la megafauna cuya dispersión no haya sido sujeta a severas reducciones en los ultimos siglos. Por lo tanto, nuestros resultados sugieren que los datos genéticos de rapaces con amplia distribución geográfica y de otra megafauna proveen de importante información de base para evaluar la relación existente entre la variabilidad genética y sus causas en otra megafauna en peligro.
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Vultures provide critical ecosystem services, yet populations of many species have collapsed worldwide. We present the first estimates of a 30-year Pan- African vulture decline, confirming that declines have occurred on a scale broadly comparable with those seen in Asia, where the ecological, economic, and human costs are already documented. Populations of eight species we assessed had declined by an average of 62%; seven had declined at a rate of 80% or more over three generations. Of these, at least six appear to qualify for uplisting to Critically Endangered. Africa’s vultures are facing a range of specific threats, the most significant of which are poisoning and trade in traditional medicines, which together accounted for 90% of reported deaths. We recommend that national governments urgently enact and enforce legislation to strictly regulate the sale and use of pesticides and poisons, to eliminate the illegal trade in vulture body parts, as food or medicine, and to minimize mortality caused by power lines and wind turbines.
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http://www.peregrinefund.org/subsites/conference-lead/2008PbConf_Proceedings.htm
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The negative consequences of lead shot ingestion have been demonstrated in captive birds, and the prevalence of embedded shot has been measured in wild waterfowl several times. However, the long-term consequences of these two indirect outcomes of hunting on waterfowl survival have merely been investigated. Using data from about 40,000 X-rayed teals (Anas crecca), this study attempts to evaluate these effects. We used multivariate logistic regressions to model the probability of carrying shot in the flesh or in the gizzard while testing for various explanatory variables such as sex, age, time or morphological measures like mass and flattened wing length. Because of technical issues, we used a non-parametric sign test rather than a complete capture-recapture analysis to evaluate the effect of shot on teal survival. This test was applied to the differences in time between ringing and recovery for lead categories (no lead shot, ⩾1 shot in the flesh but none in the gizzard, ⩾1 shot in the gizzard but none in the flesh) compared two by two. We show that, overall, males are more likely to carry embedded shot than females whereas the latter are more likely to carry lead pellets in the gizzard. Similarly, adults are more likely to carry shot in the flesh whereas first year individuals are more likely to have pellets in the gizzard. Embedded shot tend to accumulate in the ducks body over time, i.e. with the number of encounters with hunters, with no significant effect on survival. Conversely, the probability of carrying shot in the gizzard decreases over time, because lead-poisoning quickly leads the individual to death. Several possible biological interpretations are put forward to explain those results. This study demonstrates that negative impacts of ingested lead on teal survival arise after only one single pellet is ingested, advocating the ban of lead ammunition.
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Lead poisoning mortality, through the ingestion of spent shot, is long established in water- fowl, and more recently in raptors and other avian taxa. Raptors (vultures, hawks, falcons, eagles and owls) are exposed to lead from spent ammunition (shot, bullets, or fragments from either) while feeding on game species, and other avian taxa are exposed when feeding in shot-over areas, including shooting ranges. Here we review the published literature on ingestion of and poisoning by lead from ammunition in terrestrial birds. We briefly discuss methods of evaluating exposure to and poisoning from ammunition sources of lead, and the use of lead isotopes for confirming the source of lead. Documented cases include 33 raptor species and 30 species from Gruiformes, Galliformes and various other avian taxa, including ten Globally Threatened or Near Threatened species. Lead poisoning is of particular conservation concern in long-lived slow breeding species, especially those with initially small populations such as the five Globally Threat- ened and one Near Threatened raptor species reported as poisoned by lead ammunition in the wild. Lead poisoning in raptors and other terrestrial species will not be eliminated until all lead gunshot and rifle bul- lets are replaced by non-toxic alternatives. Received 29 May 2008, accepted 24 July 2008. PAIN, D. J., I. J. FISHER, AND V. G. THOMAS. 2009. A global update of lead poisoning in terrestrial birds from ammunition sources. In R. T. Watson, M. Fuller, M. Pokras, and W. G. Hunt (Eds.). Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, Idaho, USA. DOI 10.4080/ilsa.2009.0108
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Lead poisoning remains the leading cause of death among free-ranging California Condors released by The Peregrine Fund in Arizona from 1996 to 2007 in an ongoing effort to establish a self- sustaining population. Daily monitoring of radio-tagged condors by means of VHF and GPS telemetry shows them ranging from the Grand Canyon National Park to the Zion region of southern Utah. Increased proficiency of condors at finding carrion in the wild corresponds with a greater incidence of lead exposure. Periodic testing reveals spikes in blood lead levels during November and December commensurate with the deer hunting seasons and condor movement to deer hunting areas. These data combined with information collected on food types supports the hypothesis that lead ammunition residues in rifle- and shotgun-killed animals are the principle source of lead contamination among these scavengers in northern Arizona and southern Utah. Sustaining the population requires an intensive management regime of testing and treatment for lead exposure. Reducing or eliminating the availability of lead is essential to reestablishment of condors in the wild. Received 15 September 2008, accepted 31 October 2008. PARISH, C. N., W. G. HUNT, E. FELTES, R. SIEG, AND K. ORR. 2009. Lead exposure among a reintroduced population of California Condors in northern Arizona and southern Utah. In R. T. Watson, M. Fuller, M. Pokras, and W. G. Hunt (Eds.). Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, Idaho, USA. DOI 10.4080/ilsa.2009.0217
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Bullet fragments in rifle-killed deer (Odocoileus spp.) carrion have been implicated as agents of lead intoxication and death in bald eagles (Haliaeetus leucocephalus), golden eagles (Aquila chrysaetos), California condors (Gymnogyps californianus), and other avian scavengers. Deer offal piles are present and available to scavengers in autumn, and the degree of exposure depends upon incidence, abundance, and distribution of fragments per offal pile and carcass lost to wounding. In radiographs of selected portions of the remains of 38 deer supplied by cooperating, licensed hunters in 2002–2004, we found metal fragments broadly distributed along wound channels. Ninety-four percent of samples of deer killed with lead-based bullets contained fragments, and 90% of 20 offal piles showed fragments: 5 with 0–9 fragments, 5 with 10–100, 5 with 100–199, and 5 showing >200 fragments. In contrast, we counted a total of only 6 fragments in 4 whole deer killed with copper expanding bullets. These findings suggest a high potential for scavenger exposure to lead.
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Age-dependent skewed sex ratios have been observed in bird populations, with adult males generally outnumbering females. This trend is mainly driven by higher female mortality, sometimes associated with anthropogenic factors. Despite the large amount of work on bird sex ratios, research examining the spatial stability of adult sex ratios is extremely scarce. The Andean condor (Vultur gryphus) is the only bird of prey with strong sexual dimorphism favouring males (males are 30% heavier than females). By examining data from most of its South-American range, we show that while the juvenile sex ratio is balanced, or even female-skewed, the sex ratio becomes increasing male-skewed with age, with adult males outnumbering females by >20%, and, in some cases by four times more. This result is consistent across regions and independent of the nature of field data. Reasons for this are unknown but it can be hypothesized that the progressive disappearance of females may be associated with mortality caused by anthropogenic factors. This idea is supported by the asymmetric habitat use by the two sexes, with females scavenging in more humanized areas. Whatever the cause, male-skewed adult sex ratios imply that populations of this endangered scavenger face higher risks of extinction than previously believed.
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We characterized DNA sequence variation in the mitochondrial control region and 12S ribosomal subunit for a sample of Andean Condors (Vultur gryphus) representing populations distributed throughout the species' extensive geographic range (Colombia to central Argentina and Chile). Domains II and III of the control region along with part of the 12S gene were sequenced from 38 individuals (956 base pairs in 30 individuals and 430–824 base pairs for an additional 8 individuals sampled from museum specimens), and Domain I was sequenced from five of these birds (400 base pairs). We identified a total of five haplotypes based on four variable sites distributed over Domains II and III of the control region and the 12S gene. An additional variable site was identified in Domain I. All changes were transitions and no more than three sites differed between any two individuals. Variation in the control region of condors was lower than for most other birds analyzed for these loci. Although low genetic variability is often associated with endangered megafauna, the condor example is notable because the species still maintains a substantial geographic range. Thus, low genetic variability may occur even in megafauna whose ranges have not been severely reduced over recent centuries. Our results therefore suggest that genetic data from geograph-ically widespread megafauna provide important baseline data for assessing the relationship between genetic variability and its causes in other endangered species.
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Estimations of the population sizes of threatened species are fundamental for conservation. The current estimate of the population of the Andean condor Vultur gryphus is based on limited local counts. Simultaneous censuses of 10 condor communal roosts were therefore conducted during 2006–2008 in north-west Patagonia, Argentina, to obtain a minimum population number, to estimate the size of the local population, and to describe use of the roosts by season and age classes. I fitted the data to two asymptotic models to calculate the population of condors as a function of the number of communal roosts surveyed. In an area of c. 6,300 km 2 I obtained a minimum population size of 246 individuals by direct observation, and a population estimate of 296 condors (range 260–332) by applying the models. This population, the largest known of this species, comprises 68.5% adults and 31.5% imma-tures. Condors had large aggregations in some communal roosts and used the area seasonally, increasing in numbers from autumn to spring and decreasing in summer. Long-term monitoring of communal roosts across the Andean condor's range is essential for the monitoring of this rare and vulnerable species.
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Human disturbance can be a severe problem for some animal species. Behavioural ecology theory predicts that sensitivity to mortality risks, and thereby to disturbance, will be related to life-history characteristics. Long-lived species with low reproductive rates are expected to have a high cost of predation and therefore avoid risks strongly. In this paper we quantify the effect of roads on the Andean condor (Vultur gryphus) using behavioural indicators. We used a pair wise design, offering condors standardized food patches near and far from roads simultaneously. The patches consisted of dead adult sheep. We recorded condors' behaviour when visiting each patch. This study establishes the versatility of behavioural indicators and their usefulness to study conservation problems. We found that, although near and far patches were discovered after similar times and there were similar numbers of condors in the vicinity of near and far patches, the use of patches dif-fered strongly. In the patches far from roads many more condors came to feed, the average time spent per individual was longer, the proportion of time spent vigilant was lower, and the amount of food left uneaten on the carcasses was lower. These results strongly suggest that Andean condors clearly avoid roads, and behave in a way predicted from theory if they trade off safety for energy. This study shows that roads have stronger influence on the hab-itat use of Andean condors, than previously thought, and may be a significant problem for the species in populated areas.
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Endangered species recovery programs seek to restore populations to self-sustaining levels. Nonetheless, many recovering species require continuing management to compensate for persistent threats in their environment. Judging true recovery in the face of this management is often difficult, impeding thorough analysis of the success of conservation programs. We illustrate these challenges with a multidisciplinary study of one of the world's rarest birds-the California condor (Gymnogyps californianus). California condors were brought to the brink of extinction, in part, because of lead poisoning, and lead poisoning remains a significant threat today. We evaluated individual lead-related health effects, the efficacy of current efforts to prevent lead-caused deaths, and the consequences of any reduction in currently intensive management actions. Our results show that condors in California remain chronically exposed to harmful levels of lead; 30% of the annual blood samples collected from condors indicate lead exposure (blood lead ≥ 200 ng/mL) that causes significant subclinical health effects, measured as >60% inhibition of the heme biosynthetic enzyme δ-aminolevulinic acid dehydratase. Furthermore, each year, ∼20% of free-flying birds have blood lead levels (≥450 ng/mL) that indicate the need for clinical intervention to avert morbidity and mortality. Lead isotopic analysis shows that lead-based ammunition is the principle source of lead poisoning in condors. Finally, population models based on condor demographic data show that the condor's apparent recovery is solely because of intensive ongoing management, with the only hope of achieving true recovery dependent on the elimination or substantial reduction of lead poisoning rates.
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Many scavenging bird populations have experienced abrupt declines across the globe, and intensive recovery activities have been necessary to sustain several species, including the critically endangered California condor (Gymnogyps californianus). Exposure to lead from lead-based ammunition is widespread in condors and lead toxicosis presents an immediate threat to condor recovery, accounting for the highest proportion of adult mortality. Lead contamination of carcasses across the landscape remains a serious threat to the health and sustainability of scavenging birds, and here we summarize recent evidence for exposure to lead-based ammunition and health implications across many species. California condors and other scavenging species are sensitive indicators of the occurrence of lead contaminated carcasses in the environment. Transdisciplinary science-based approaches have been critical to managing lead exposure in California condors and paving the way for use of non-lead ammunition in California. Similar transdisciplinary approaches are now needed to translate the science informing on this issue and establish education and outreach efforts that focus on concerns brought forth by key stakeholders.
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The ingestion of spent lead shot was known to cause mortality in wild waterfowl in the US a century before the implementation of nontoxic shot regulations began in 1972. The biological foundation for this transition was strongly supported by both field observations and structured scientific investigations. Despite the overwhelming evidence, various societal factors forestalled the full transition to nontoxic shot for waterfowl hunting until 1991. Now, nearly 20 years later, these same factors weigh heavily in current debates about nontoxic shot requirements for hunting other game birds, requiring nontoxic bullets for big game hunting in California Condor range and for restricting the use of small lead sinkers and jig heads for sport-fishing. As with waterfowl, a strong science-based foundation is requisite for further transitions to nontoxic ammunition and fishing weights. Our experiences have taught us that the societal aspects of this transition are as important as the biological components and must be adequately addressed before alterna- tives to toxic lead ammunition, fishing weights, and other materials will be accepted as an investment in wildlife conservation. Received 16 May 2008, accepted 8 July 2008. FRIEND, M., J.C. FRANSON, AND W.L. ANDERSON. 2009. Biological and societal dimensions of lead poison- ing in birds in the USA. In R. T. Watson, M. Fuller, M. Pokras, and W. G. Hunt (Eds.). Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, Idaho, USA. DOI 10.4080/ilsa.2009.0104
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Lead toxicosis is a problem recognized worldwide in raptors that has seriously impacted the recovery efforts of several endangered species. Vultures, eagles and kites are commonly affected because, as scavengers, they ingest lead ammunition residues when feeding on the remains of gun-killed animals. In South America, lead toxicosis in birds has been scarcely investigated. Raptors have been occasionally re- ported with the presumptive diagnosis of lead poisoning in hunting areas of central Argentina, although no systematic surveys have been conducted. Given the current understanding and knowledge we have on lead toxicosis in raptors in other parts of the world, the intense year-round wildlife hunting activities occurring in central Argentina, and the clinical diagnosis of lead poisoning in some birds presented to rehabilitation centers, we hypothesize that scavenging birds of prey in central Argentina could be systematically exposed to this heavy metal. Recently, we detected lead in the blood and bones of Argentine Solitary Crowned Ea- gles (Harpyhaliaetus coronatus), a severely endangered species from central and northern Argentina. To- gether with recent findings of lead in Andean Condors (Vultur gryphus) and in waterfowl, these studies are a first step to determine the extent of this problem in Argentine birds. Systematic studies of lead toxicity in wild birds in Argentina are needed in order to educate hunters toward a switch to non-lead substitutes. Re- ceived 4 August 2008, accepted 22 October 2008. SAGGESE, M.D., A. QUAGLIA, S. A. LAMBERTUCCI, M. S. BO, J. H. SARASOLA, R. PEREYRA- LOBOS, AND J. J. MACEDA. 2009. Survey of lead toxicosis in free-ranging raptors from central Argentina. In R. T. Watson, M. Fuller, M. Pokras, and W. G. Hunt (Eds.). Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, Idaho, USA. DOI 10.4080/ilsa.2009.0211
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The development of conservation strategies to protect viable populations of scavenging birds requires the existence of adequate and safe food supplies in the wild. Early reports on Andean condors Vultur gryphus diet recorded guanacos and rheas, the dominant herbivores since the Pleistocene, as their main food in Patagonia. However, in the past century, guanaco and rhea populations have notably decreased as a consequence of introduced livestock, and other exotic mammals have colonized the region. We study the spatial and temporal variation of the condors' diet to determine which species are being consumed by condors, and to test whether native herbivores still have a role as a food source. We analysed 371 pellets (517 prey items), collected along 500 km in northwestern Patagonia, Argentina. Our study shows that the Andean condor depends heavily (98.5%) on exotic herbivores. Their diet was made up of c. 51% sheep/goat, 24% hare/rabbit, 17% red deer and 6% cow/horse, with only 2% other mammal species. Samples from locations surveyed after 12–15 years showed a diet shift coincident with the local tendencies in the food source. The diet composition of condors using roosts within the same zone was very similar, which suggests that they may be feeding from the same area. Thus, unhealthy carcasses could impact the entire local populations. Our results show the abundance of the invasive species in northwestern Patagonia and support the idea that native mega-herbivores are ecologically extinct in this area. Exotic species management can have a decisive impact on scavenger's survival. It is necessary to apply a strategy that includes public environmental education about the problems of scavengers (e.g. use of poison, veterinary medicines and lead bullets), and a serious productive plan, including native species as a suitable source of economic development.
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Twelve clutches containing 69 eggs in all, collected from 1874 to 1953, were obtained from a museum. From 1972-1974, 25 unhatched eggs were collected from 11 nests when the birds had stopped brooding. Egg-shell thickness was measured and lead analyses were performed. There was a correlation between lead concentration and shell thickness in both old and recent eggs. Part of the correlation between lead concentration and shell thickness must be explained by an association between lead and PCB's and perhaps other chlorinated hydrocarbons, however, lead is an important confounding factor. Its role as a possible inhibitor of egg-shell production needs further elucidation. (JTE)
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Lead poisoning is not a new threat for wild birds, but it is now playing an important role in shaping raptor populations. Studies have been focused mainly on Europe, North-America, and Japan, but little is known about the situation in South-America. Lead is a serious threat for wildlife, especially for long-lived species. Nevertheless, no information is available for wild Andean condor (Vultur gryphus) populations. This species, which lives throughout the Andes Mountains, is endangered mainly in the north though it is having problems throughout its distribution. We evaluated lead exposure in the Andean condor by a nondestructive method using feathers. We determined lead concentration from 152 feathers, collected in 15 communal roosts distributed throughout almost all condor’s range in Patagonia (ca. 1500 km north–south). We also looked for the origin of this lead through the analysis of lead isotope composition of feathers and ammunition. We present here the first reference data on lead concentration for a raptor population from Argentina. Lead concentrations were generally low, however, some individuals had concentrations several times above the overall mean (up to 21 lg/g). Our results suggest that lead might come from a mix of two types of ammunition sources, one used for big game and another for hare hunting. Andean condors are at the top of the food chain, thus all the other medium-to-large sized scavengers and predators from this area can be also exposed to this threat. We highlight the need to change hunting policies in Argentina, and in other South-American countries, including the banning of lead ammunitions to protect carnivores consuming hunted animals.
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Iron (Fe) deficiency is the most common nutritional problem among children and lead (Pb) toxicity is the most common environmental health threat to children all over the world. The objective of this study was to determine blood lead (BPb) levels and prevalence of Fe deficient anemia among 1 to 5year old children attending day care clinic in pediatric ward of civil hospital Karachi, Pakistan. A total of 340 children of both genders participating in this study, were screened for anemia. Among them 215 were anemic and 125 non-anemic. The anemic group was further divided in two groups on the basis of % hemoglobin (Hb), mild (Hb <10g/dL) and severe anemic group (Hb <8g/dL), while non-anemic as referent children (Hb >10g/dL). The blood samples were analysed for Pb and Fe, along with hematological parameters. The result indicated that anemic children had a higher mean values of Pb in blood than referent children with Hb >10g/dL. The Pb levels <100μg/L were detected in 40% referent children while 60% of them had >10μg/dL. The BPb concentration in severe anemic children (53%) was found in the range of 100-200μg/L, whereas 47% had >200μg/L. The significant negative correlations of BPb level with % Hb (r=-0.514 and r=-0.685) and Fe contents (r=-0.522, r=-0.762, p<0.001) were observed in mild and severe anemic children respectively. While positive correlation was observed between BPb and age of both group and genders (r=0.69, p<0.01). The BPb levels were significantly associated with biochemical indices in the blood which have the potential to be used as biomarkers of Pb intoxication and Fe deficient anemia.