Article

Exposure of California Condors to Lead From Spent Ammunition

Authors:
To read the full-text of this research, you can request a copy directly from the author.

Abstract

ABSTRACT The scientific evidence that California condors (Gymnogyps californianus) are frequently sickened and killed by lead poisoning from spent ammunition supports the conclusion that current levels of lead exposure are too high to allow reintroduced condors to develop self-sustaining populations in the wild in Arizona and, by inference, in California. The evidence for lead poisoning and its source comes from the following sorts of data: 1) 18 clinical necropsies revealing high levels of lead in body tissues and (or) presence of lead shotgun pellets and bullet fragments in digestive tracts; 2) moribund condors showing crop paralysis and impending starvation with toxic levels of lead in their blood; 3) widespread lead exposure among free-flying condors, many with clinically exposed or acute levels; 4) temporal and spatial correlations between big game hunting seasons and elevated lead levels in condors; and 5) lead isotope ratios from exposed condors showing close similarity to isotope ratios of ammunition lead but isotope ratios in less exposed condors being similar to environmental background sources, which are different from ammunition lead. Simple population models reveal harmful demographic impacts of unnatural mortality from lead on population trajectories of reintroduced condors. Recent innovations in the manufacture of nonlead shotgun pellets and bullets with superior ballistics now provide for a simple solution to the problem of lead ingestion by condors, many other species of wildlife, and human beings: substitute nontoxic forms of ammunition for traditional lead-based ammunition. The substitution of nontoxic ammunition would be highly efficacious for hunting, economically feasible, and the right thing to do.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the author.

... Unfortunately even as the ecological roles of vultures have become increasingly appreciated, major threats to the survival of vulture species have increased considerably in recent decades, particularly with pesticide poisoning in sub-Saharan Africa, diclofenac use in domestic livestock in South Asia, and lead toxicosis in the western USA (Oaks et al. 2004;Cade 2007;Ogada 2014;. Collision with power lines and increasingly wind farms have also led to high morbidity and mortality in many locations (Meretsky et al. 2000;Lehman et al. 2007;Santangeli et al. 2019). ...
... Though in Africa and North America vultures can have a negative cultural connotation (Cade 2007;Ogada et al. 2012) and can be shot for traditional medicine, bushmeat, or for sport, most anthropogenic causes of trauma in vultures appear to be unintentional rather than intentional. The adaptions which make vultures obligate scavengers also make them more susceptible to traumatic injuries. ...
Article
Vulture species worldwide play a key role in ecosystems as obligate scavengers, and several populations have had precipitous declines. Research on vulture health is critical to conservation efforts including free-living vultures and captive breeding programs, but is limited to date. In this systematic review, we determined the reported causes of free-living vulture species morbidity and mortality worldwide. The most commonly reported cause of mortality was from toxins (60%), especially lead and pesticides, followed by traumatic injury (49%), including collisions with urban infrastructure and gunshot. Neglected areas of research in free-living vulture health include infectious diseases (16%), endocrine and nutritional disorders (6%), and neoplasia (< 1%). Almost half of the studies included in the review were conducted in either Spain or the USA, with a paucity of studies conducted in South America and sub-Saharan Africa. The highest number of studies was on Griffon (Gyps fulvus) (24%) and Egyptian vultures (Neophron percnopterus) (19%), while half of all vulture species had five or fewer studies. Future investigations on free-living vulture health should focus on neglected areas of research, such as infectious diseases, and areas with gaps in the current literature, such as South America, sub-Saharan Africa, and under-studied vulture species.
... Different sources of lead such as pollution (Sriram et al., 2018), fishing sinkers (Haig et al., 2014), mining activities and industries can impact bird species (Plaza et al., 2018). However, the most important source of lead impacting bird populations worldwide is lead ammunition produced from hunting activities (Burger, 1995;Cade, 2007;Fisher et al., 2006;Pain et al., 2009). This may be related to the fact that lead ammunition remains unregulated in many regions of the world (Avery and Watson, 2009;Plaza et al., 2018), unlike other sources of lead such as gasoline and paint, which have been extensively regulated (Stroud, 2015). ...
... In conclusion, most of the reviewed studies only suggest the possible source of lead. This is important given that unclear scientific information is less effective at producing changes in conservation policies intended to mitigate environmental problems (Cade, 2007;Plaza et al., 2018). Future research should use different methods to probe the origin of lead poisoning in vultures. ...
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.
... The propensity of bald eagles to feed on remains of hunterkilled animals also makes them useful for assessing the uptake of contaminants, most notably lead (Pb) from spent Pb ammunition, in terrestrial systems (e.g., Fisher et al. 2006;Cruz et al. 2012;Hunt 2012;Warner et al. 2014). Pb is a particularly toxic pollutant that can enter the environment from multiple sources in addition to spent ammunition, including aircraft, automobiles, metal industries, mining, and refineries (Beyer et al. 1985;Cade 2007;Tsipoura et al. 2011; U.S. Environmental Protection Agency [USEPA] 2013). The use of Pb fishing tackle by anglers also provides a means for bald eagles and other scavengers to ingest Pb directly through consumption of dead or dying fish entangled with Pb sinkers (Scheuhammer and Norris 1996). ...
... Three of the nestlings had blood samples with Pb concentrations ≥16 µg/ dL, which was above the 97.5th percentile of our uncensored data. In comparison with other raptor species, Cade (2007) proposed a threshold for exposure of 10 µg/dL of Pb in blood for California condors (Gymnogyps californianus), and Franson and Pain (2011) adopted subclinical and clinical poisoning ranges of 20-50 and 50-100 µg/dL, respectively, for Pb in blood of adult Falconiforms. More recently, Ecke et al. (2017) proposed a much lower sublethal concentration for golden eagles of 2.5 µg/dL, which they based on the Benchmark Dose Response of a 10% reduction in mean movement rate of radio-telemetered birds. ...
Article
Full-text available
Most studies examining bald eagle (Haliaeetus leucocephalus) exposure to lead (Pb) have focused on adults that ingested spent Pb ammunition during the fall hunting season, often at clinical or lethal levels. We sampled live bald eagle nestlings along waterbodies to quantify Pb concentrations in 3 national park units and 2 nearby study areas in the western Great Lakes region. We collected 367 bald eagle nestling feather samples over 8 years during spring 2006-2015 and 188 whole blood samples over 4 years during spring 2010-2015. We used Tobit regression models to quantify relationships between Pb concentrations in nestling feathers and blood using study area, year, and nestling attributes as covariates. Pb in nestling feather samples decreased from 2006 to 2015, but there was no trend for Pb in blood samples. Pb concentrations in nestling feather and blood samples were significantly higher in study areas located closer to and within urban areas. Pb in feather and blood samples from the same nestling was positively correlated. Pb in feathers increased with nestling age, but this relationship was not observed for blood. Our results reflect how Pb accumulates in tissues as nestlings grow, with Pb in feathers and blood indexing exposure during feather development and before sampling, respectively. Some nestlings had Pb concentrations in blood that suggested a greater risk to sublethal effects from Pb exposure. Our data provides baselines for Pb concentrations in feathers and blood of nestling bald eagles from a variety of waterbody types spanning remote, lightly populated, and human-dominated landscapes.
... Deleterious effects of lead on wildlife prompted a federal ban on hunting waterfowl with lead pellets in 1991, which aided the subsequent recovery of many waterfowl species in North America (Anderson et al. 2000, Samuel andBowers 2000). Given the well-documented susceptibility of scavengers and birds of prey to lead contamination (Tranel and Kimmel 2009), it is not surprising that researchers have identified lead exposure, specifically from ammunition sources, as the primary limiting factor preventing the recovery of the federally endangered California Condor (Gymnogyps californianus), the largest avian scavenger in North America (Church et al. 2006, Cade 2007, Hunt et al. 2007, Rideout et al. 2012, Kelly et al. 2014, 2015. ...
... Such dramatic increases in lead exposure during the hunting season in a facultative scavenger underscore the specter of lead toxicity for a potential propagule of California Condors released into YAT. Although our research did not attempt to determine the source of lead detected in our target species, ingestion of lead ammunition is the most parsimonious explanation for the observed differences in blood lead levels, and other research has directly linked such seasonal differences in avian scavengers to ingestion of ammunition (Church et al. 2006, Cade 2007, Finkelstein et al. 2010. Increased levels of lead during the hunting season is also consistent with findings of previous studies conducted in Mendocino County, California (~300 km south of our study area), where Turkey Vulture blood lead concentrations increased 114% during the hunting season compared with the nonhunting season (Figure 2; . ...
Article
Full-text available
Areas of northern California, USA, have been identified as quality habitat for an expanded California Condor (Gymnogyps californianus) Recovery Program. Nonetheless, lead poisoning continues to complicate California Condor recovery efforts within their current range and threatens the viability of future propagules. Therefore, background levels of lead and other contaminants should be assessed as part of a feasibility analysis to determine the efficacy of expanding the Recovery Program into northern California. A California-wide ban on the use of lead ammunition for hunting, scheduled to go into effect in 2019, coupled with hunter outreach programs aimed at reducing the use of lead ammunition, may present new opportunities for California Condor recovery in this region. As such, we captured and studied 2 surrogate species, Common Ravens (Corvus corax) and Turkey Vultures (Cathartes aura), in coastal and near-coastal habitats of northern California to examine relationships between contaminant (lead, mercury, zinc, and copper) exposure relative to distance from the coast (vultures and ravens), age (vultures and ravens), and hunting season (ravens only). Although blood lead concentrations were relatively low throughout our study area for vultures (median ¼ 5.99 lg dL¹, n ¼ 137), median blood lead concentrations of ravens captured during the hunting season (6.4 lg dL¹, n ¼ 10) were almost 6-fold higher than those of birds captured during the nonhunting season (1.1 lg dL¹, n ¼ 17). In addition, for both species, blood concentrations of mercury decreased with increasing distance from the coast, while blood concentrations of lead increased. Given the significant increase in blood lead concentration in ravens during the hunting season, we believe that pervasive exposure to lead demonstrates a risk facing potential propagules of California Condors throughout the species' historical range.
... While, where compliance is good, this should reduce lead ingestion in waterfowl and their main predators, other avian predators and scavengers, a range of other terrestrial birds continue to be subject to lead exposure and poisoning because of their feeding habits. Lead poisoning in the California condor, which feeds almost exclusively on carrion, is now considered a major obstacle to the recovery of the species (Meretsky et al. 2000, Cade 2007, Snyder 2007. California condors ingest lead fragments from ammunition in carcasses of animals or offal left in the field (Church et al. 2006, Hunt et al. 2006, Cade 2007, and considerable effort is devoted to monitoring and attempts to reduce lead exposure (Hall et al. 2007, Sullivan et al. 2007). ...
... Lead poisoning in the California condor, which feeds almost exclusively on carrion, is now considered a major obstacle to the recovery of the species (Meretsky et al. 2000, Cade 2007, Snyder 2007. California condors ingest lead fragments from ammunition in carcasses of animals or offal left in the field (Church et al. 2006, Hunt et al. 2006, Cade 2007, and considerable effort is devoted to monitoring and attempts to reduce lead exposure (Hall et al. 2007, Sullivan et al. 2007). Lead poisoning of wintering bald eagles and golden eagles (Aquila chrysaetos) was long thought to be primarily due to the ingestion of shotgun pellets in dead or crippled waterfowl, but Kramer and Redig (1997) found that the prevalence of lead poisoning in eagles did not decrease after the implementation of the 1991 nontoxic shot regulations for hunting waterfowl and American coots (Fulica americana) in the United States. ...
Article
Full-text available
Lead is a highly toxic heavy metal that acts as a nonspecific poison affecting all body systems and has no known biological requirement. Absorption of low concentrations may result in a wide range of sublethal effects in animals, and higher concentrations may result in mortality (Demayo et al. 1982). Lead has been mined and smelted by humans for centuries, but the use of lead-based products increased greatly following the Industrial Revolution. Consequently, lead today is ubiquitous in air, water, and soil, in both urban and rural environments (Eisler 2000). Vertebrates are exposed to lead mainly via inhalation and ingestion. A proportion of lead entering the body is absorbed into the bloodstream and subsequently becomes distributed among body tissues, primarily the blood, liver, kidney, and bone. As a result of anthropogenic activities, most animals have higher tissue lead concentrations than in preindustrialized times. Although even very low tissue lead concentrations have some measurable physiological effects, the concentrations usually encountered in the wider environment (i.e., distant from lead emission sources) have not generally been considered to directly affect survival of most wildlife.
... Raptors, both scavengers and predators, are exposed to lead when feeding on the remains of shot animals or when hunting prey injured with lead shot or bullets (Church et al. 2006, Cade 2007. Particularly susceptible to lead toxicosis are scavenger species (Platt et al. 1999, García-Fernandez et al. 1997) like the California Condor (Gymnogyps californianus), a severely endangered species (Snyder and Snyder 2000). ...
... Particularly susceptible to lead toxicosis are scavenger species (Platt et al. 1999, García-Fernandez et al. 1997) like the California Condor (Gymnogyps californianus), a severely endangered species (Snyder and Snyder 2000). Spent lead ammunition appears to be not only the main cause of its decline in the wild during the 20 th Century, but continues to undermine current recovery efforts aimed to establish self-sustaining populations in California, Utah and Arizona (Sorenson et al. 2000, Woods et al. 2006, Cade 2007. Furthermore, lead toxicosis has been reported as an important contributing factor in the population decline of other endangered species, including Steller's Sea Eagles (Haliaetus pelagicus), White-tailed Eagles (Haliaetus albicilla), Red Kites (Milvus milvus), Spanish Imperial Eagles (Aquila adalberti), and Egyptian Vultures (Neophron percnopterus) (Kurosawa 2005, Pain et al. 2005, Saito 2009, Krone et al. 2009, Gangoso et al. 2009, Mateo 2009). ...
... Such biases in our understanding of clinical signs and pathologies are clearly visible from the data (Figs. 2 and 3). Nonetheless, different contaminants disproportionately affect certain taxa more than others, either as a result of specific sensitivity (such as NSAIDs in Old World vultures (Cuthbert et al., 2007)), behavioural ecology (such as lead in California Condors Gymnogyps californianus (Cade, 2007)), or trophic level (such as in Bonelli's Eagles Aquila fasciata exposed to mercury (Badry et al., 2019)) affecting likelihood of exposure, and so a certain level of bias is to be expected. Alternative candidates for experimental contaminant testing, such as wildlife rehabilitation cases, should also be weighed against conservation value, likely post-release welfare, experimental knowledge gained, and individual captive welfare (vs. ...
... A well-studied case of avian mortality due to lead from cervid hunter's bullets is that of the endangered California condor. Condor reintroduction programs have been severely hampered, including the long-delayed reintroduction of the species to much of its original range, by the threat of lead poisoning as the result of consumption of bullet fragments left in carcasses and discarded gut piles (Church et al., 2006;Cade, 2007). Blood lead concentration was significantly higher in turkey vultures during white-tailed deer hunting season when compared to the off-seasons (Kelly and Johnson, 2011). ...
... In White Stork nestlings (Ciconia ciconia) from Spain, Pb blood concentrations were also lower than the 0.2 μg/g threshold found in most birds (N = 54), with only five animals that exceeded this limit (de la Casa-Resino et al., 2014). However, even lower Pb levels such as 0.09 μg/g in blood are considered as subclinical values for California Condor (Gymnogyps californianus) (Cade, 2007) or 0.023 μg/g for adult Golden Eagles (Aquila chrysaetos) (Ecke et al., 2017). These values are 10 times lower than Pb subclinical poisoning concentrations. ...
Article
Young birds at an intensive growth stage are especially vulnerable to the deleterious effects of contaminants such as lead (Pb). This element negatively influences organs, development and even behavior, which can consequently lead to lower survival and reproductive success of thepopulation. There was a suspicion that these mechanisms, along with other factors, retarded population growth of the Black Stork - still a heavily understudied species in respect to pollution, especially Pb. Therefore, we undertook a study concerning Pb concentrations in the down and blood of Black Stork nestlings from breeding grounds in central and southern Poland (Europe). To investigate the effects of Pb exposure on nestling condition, scale mass index and reduced glutathione levels were also studied, but results indicated that Pb did not influence either of these parameters. The highest blood Pb concentration reached 0.247 μg/g, while the highest down Pb concentrations was significantly higher reaching 4.95 μg/g. Concentrations in blood and down were not correlated with each other. Nest location and year of sampling were not influential for blood but were influential for down Pb concentrations. Relationships between Pb concentrations, habitat characteristics and proximity to emitters were not significant. Overall Pb concentrations in Black Stork nestlings were below the toxicity threshold and did not have negative effects on specimens studied. They were probably related to maternal exposure during migration, on stopover and breeding grounds as well as with food provided by parents.
... Although reintroductions were initiated in 1992 (Walters et al. 2010) and at the end of 2022 over 180 birds were in the wild in California, population growth has been reliant on the release of captive-bred juveniles ). Lead toxicosis is the primary cause of death for free-flying juvenile and adult condors (Rideout et al. 2012, Viner et al. 2020, and their principal source of lead exposure is feeding on carcasses of animals shot with lead-based ammunition (Church et al. 2006, Cade 2007. ...
Article
In the first comprehensive assessment of the reproductive rates of critically endangered California Condors (Gymnogyps californianus) recovering from complete extirpation in the wild, we analyzed 20 years (1999–2018) of data from condor flocks in southern and central California. We found that several anthropogenic threats affected reproductive rates: (1) coastal space use by female condors was associated with lower hatch probability, presumably due to foraging on marine mammals and associated DDE exposure; (2) trash ingestion by chicks decreased fledging probability prior to implementation of trash management in 2007; and (3) all parent deaths during rearing resulted in chick or early fledgling deaths, and most parental deaths were due to lead poisoning. We also detected several effects on reproductive rates of the complex individual-based management of condors, which involves ongoing releases of captive-bred individuals and health interventions including treatment of lead poisoning. Recruitment rates were lower for new release sites, which we attribute to a lack of individual- and flock-level experience. In addition, the number of free-flying days in the wild in the year before first breeding and in the 8 weeks before subsequent breeding was positively associated with female and male recruitment and with female rebreeding probabilities, respectively, indicating that removing individuals from the wild may reduce their breeding success. Finally, probabilities of recruitment, rebreeding, and fledging all increased with age, and given the age distribution skew of the recovering flocks towards younger individuals, overall reproductive success was lower than would be expected at the stable age distribution. Thus, reproductive rates should increase over time as the mean age of California Condors increases if current and emerging threats to reproduction, including the loss of breeders due to lead poisoning, can be addressed.
... Threat mapping evidence found on it was heterogeneously distributed and clustered around terrestrial Asia, Africa, and South America, where there is higher reliance of communities on wild meats for sustenance, and presence of illicit wildlife trades [145][146][147]. Nonetheless, hunting and persecution of animals also occurs in Europe and North America [148][149][150][151][152][153] where mapping evidence for this threat was limited. Therefore, this systematic map will be useful for the implementation of targets on terrestrial biological resource use in Asia, Africa, and South America but more evidence is needed elsewhere. ...
Article
Full-text available
Background Human activities are driving accelerating rates of species extinctions that continue to threaten nature’s contribution to people. Yet, the full scope of where and how human activities threaten wild species worldwide remains unclear. Furthermore, the large diversity of approaches and terminology surrounding threats and threat mapping presents a barrier to understanding the state of knowledge and uptake into decision-making. Here, we define ‘threats’ as human activities and direct human-initiated processes, specifically where they co-occur with, and impact the survival of, wild species. Our objectives were to systematically consolidate the threat mapping literature, describe the distribution of available evidence, and produce a publicly available and searchable database of articles for easy uptake of evidence into future decision-making. Methods Four bibliographic databases, one web-based search engine, and thirteen organisational websites were searched for peer-reviewed and grey-literature published in English 2000–2020. A three-stage screening process (title, abstract, and full-text) and coding was undertaken by two reviewers, with consistency tested on 20% of articles at each stage. Articles were coded according to 22 attributes that captured dimensions of the population, threat, and geographic location studied in addition to methodological attributes. The threats studied were classified according to the IUCN Red List threat classification scheme. A range of graphical formats were used to visualise the distribution of evidence according to these attributes and complement the searchable database of articles. Review findings A total of 1069 relevant threat mapping studies were found and included in the systematic map, most conducted at a sub-national or local scale. Evidence was distributed unevenly among taxonomic groups, ecological realms, and geographies. Although articles were found for the full scope of threat categories used, most articles mapped a single threat. The most heavily mapped threats were alien invasive species, aquatic or terrestrial animal exploitation, roads and railways, residential development, and non-timber crop and livestock agriculture. Limitations regarding the English-only search and imperfect ability of the search to identify grey literature could have influenced the findings. Conclusions This systematic map represents a catalogue of threat mapping evidence at any spatial scale available for immediate use in threat reduction activities and policy decisions. The distribution of evidence has implications for devising actions to combat the threats specifically targeted in the post-2020 UN Biodiversity Framework, and for identifying other threats that may benefit from representation in global policy. It also highlights key gaps for further research to aid national and local-scale threat reduction. More knowledge would be particularly beneficial in the areas of managing multiple threats, land-based threats to marine systems, and threats to plant species and threats within the freshwater realm.
... 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). ...
Article
Full-text available
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.
... Despite this increase in numbers, condor populations remain threatened by a variety of anthropogenic factors , Rideout et al. 2012, Finkelstein et al. 2015, Kelly et al. 2015, Kurle et al. 2016. The most important threat to California Condors is lead poisoning from ingestion of spent ammunition in their only food source, carrion (Cade et al. 2007, Hunt et al. 2007, Finkelstein et al. 2015. In addition to lead poisoning, condor reproductive failure has been linked to DDEpoisoned marine mammal food sources (Kurle et al. 2016) and ingestion of microtrash, and direct adult mortality has been linked to shooting by humans and predation while feeding or roosting (Rideout et al. 2012, Kelly et al. 2015. ...
Article
Full-text available
Despite a dramatic recovery from the brink of extinction, California Condors (Gymnogyps californianus) still face significant anthropogenic threats. Although condor movement patterns across large temporal scales are understood, less is known about their movements on a fine temporal scale. We used a trajectory-based analysis of GPS telemetry data gathered from condors during 2013 to 2018 to investigate the relationship between the distances condors travel in a day, demographic characteristics (e.g., age and sex), and time of year. Most (>71.4%) daily travel distances by condors were <100 km, and, on average, condors traveled 70.1 +- 60.9 km/d (¯x +- SD). On two occasions one condor traveled >400 km in a single day (477 km one day and 415 km the following day). The tendency for condors to travel long distances increased with age, and condors traveled longer distances during the summer and when nesting. Traveling such long distances likely exposes birds to threats across a greater variety of landscapes than would be expected for birds that moved shorter distances. Given anticipated condor range expansion and population increase, this work highlights the importance of coordinating condor conservation across the broad spatial scales at which they move.
... Bullets and slugs are the predominant ammunition for large game, whereas shotgun pellets are used for upland small game. Once in the environment, spent lead ammunition can have detrimental effects on wildlife that directly or indirectly consume lead fragments or pellets (Cade 2007;Craighead and Bedrosian 2008;Neumann 2009;Cruz-Martinez et al. 2012). Avian scavengers such as eagles Accipitridae spp. ...
Article
Full-text available
Despite the known deleterious effects lead exposure can have on humans, lead remains the most common type of ammunition used to harvest big game and upland game birds. We sampled wild turkey Meleagris gallopavo breast muscle shot with standard lead and copper-plated lead pellets to quantify lead residue concentrations within the wound channel, and we sampled multiple adjacent locations to measure the extent lead contamination spreads through tissue of harvested turkeys. We found that samples taken from the wound channel contained more lead (mean = 3.76 μg/g dry weight) than both samples taken adjacent to the wound channel (mean = 0.20 μg/g dry weight) and samples taken from >5 cm away (mean = 0.15 μg/g dry weight). Additionally, we found that birds harvested with standard lead ammunition did not differ in lead concentrations from those shot with copper-plated lead, suggesting that copper plating does not aid in reducing lead exposure. Our findings suggest that wild turkeys harvested with either lead or copper-plated lead shot have the potential to expose consumers, especially children due to their lower tolerance, to low levels of lead that could exceed daily consumption limits set by the Food and Drug Administration and Centers for Disease Control. However, elevated lead levels were confined to the wound channel, and thus proper preparation of game to remove tissue surrounding wound channels may eliminate or substantially reduce lead exposure from harvested game birds.
... Longlived raptors are more vulnerable to poisoning, as they might assume a lethal burden of lead before producing enough offspring for the population recruitment (Krone, 2018). In areas of intense hunting, it has been ascertained that lead poisoning may even preclude the conservation of large birds of prey, as in the case of the California condor (Gymnogyps californianus) (Cade, 2007;Finkelstein et al., 2012). ...
Article
Lead poisoning from spent ammunition is known to affect many avian species. Birds of prey ingest lead when feeding on game shot with lead gunshot or bullets. Raptors with scavenging habits are particularly vulnerable to ingesting lead in areas with intensive hunting and are good indicators of the risk of poisoning from lead ammunition. To assess how much facultative and obligate avian scavengers suffer lead contamination in south-central Europe, between 2005 and 2019 we collected and analysed 595 tissue samples from 252 carcasses of 4 species (golden eagle, bearded vulture, griffon vulture, cinereous vulture). Lead concentrations in organs showed a similar pattern across species with long and small bones revealing the highest median values (5.56 and 6.8 mg/kg w.w., respectively), the brain the lowest (0.12), and the liver and kidney the intermediate (0.47 and 0.284). Overall, 111 individuals (44.0%) had lead concentrations above background thresholds in at least one tissue (i.e. >2 mg/kg w.w. in soft tissues, >8.33 in bone) and 66 (26.2%) had values indicating clinical poisoning (>6 mg/kg w.w. in liver, >4 in kidney, >16.6 in bone). Tissue lead concentrations and incidence of clinical and sub-clinical poisoning were higher in golden eagles and griffon vultures than in bearded and cinereous vultures, likely due to different feeding habits. In all species we found a rapid increase in lead values with age, but differences between age classes were significant only in the golden eagle. Birds with lead fragments in their digestive tract, as detected by X-rays, had higher median lead concentrations, suggesting that hunting ammunition is the main source of lead poisoning. Our results imply that lead impacts the demography of these long-lived species with delayed sexual maturity and low reproduction rate. A rapid transition towards lead-free bullets and gunshot is therefore required across Europe.
... For human comparison, the US National Institute for Occupational Safety and Health (NIOSH) defines toxicity for adults at 5 μg/dL. Based on the subclinical Pb concentration for condors of < 10 μg/dL (Cade 2007) and rehabilitation benchmark for wild raptors of > 40 μg/dL (Fallon et al. 2017), chelation therapy began with a single intramuscular injection of CaEDTA (100 mg/kg) in hopes of saving the swan, although it did not live through the night. The body was wrapped in plastic and frozen whole. ...
Article
Full-text available
We utilized lead (Pb) stable isotopes to identify the source of acute Pb poisoning in a Tundra Swan (Cygnus columbianus) and evaluated overall Pb exposure. Upon necropsy, we obtained samples of blood, liver, kidney, heart, thigh, breast, femur, and metallic objects (i.e., fishing sinker, spring and swivels) from the gizzard for Pb isotopic analysis. Pb isotope ratios of blood and soft tissues were essentially identical to the Pb ratios of the sinker, the likely source of acute poisoning. The spring and swivels had lower Pb content and ratios distinct from tissue, suggesting no significant contribution to poisoning. Femur Pb isotopic composition was the most distinct biological sample and indicative of a combination of sources. These results demonstrate isotopic analysis as a viable method for determining the source of acute Pb poisoning, and that Pb isotope ratios in bone most likely record a lifetime-averaged metric of Pb exposure.
... 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, 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. ...
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. Two years later, regulations were passed to require use of nontoxic ammunition for deer hunting (including copper-jacketed lead bullets with low fragmentation rates), and were expanded in 2004 to cover all big-game hunting. As a leading professional society for raptor researchers and raptor conservationists, the RRF is dedicated to the accumulation and dissemination of scientific information about raptors, and to resolving raptor conservation concerns (RRF 2020). Lead poisoning of raptors remains an ongoing conservation concern and presents a global threat to raptor populations, many of which have little to no direct regulatory protection. Based on the science summarized here, reducing the sources and scale of lead poisoning will allow long-term co-occurrence of raptor populations with human populations. Literature Cited 1. Avery, D., and R. T. Watson (2009). Regulation of lead-based ammunition around the world. InIngestion of Lead from Spent Ammunition: Implications for Wildlife and Humans ( R. T. Watson, M. Fuller, M. Pokras, and W. G. Hunt, Editors). The Peregrine Fund, Boise, ID, USA. pp. 161–168. Google Scholar 2. Bedrosian, B., D. Craighead, and R. Crandall (2012). Lead exposure in Bald Eagles from big game hunting, the continental implications and successful mitigation efforts. PLoS ONE 7(12): e51978. https://doi.org/10.1371/journal.pone.0051978 . Google Scholar 3. Berny, P. J., E. Mas, and D. Vey (2017). Embedded lead shots in birds of prey: The hidden threat. European Journal of Wildlife Research 63:101. https://doi.org/10.1007/s10344-017-1160-z . Google Scholar 4. Burger, J. (1995). A risk assessment for lead in birds. Journal of Toxicology and Environmental Health 45:369–396. Google Scholar 5. Cade, T. J. (2007). Exposure of California Condors to lead from spent ammunition. Journal of Wildlife Management 71:2125–2133. Google Scholar 6. Carpenter, J. W., O. H. Pattee, S. H. Fritts, B. A. Rattner, S. N. Wiemeyer, J. A. Royle, and M. R. Smith (2003). Experimental lead poisoning in Turkey Vultures (Cathartes aura). Journal of Wildlife Diseases 39:96–104. Google Scholar 7. Cartró-Sabaté, M., P. Mayor, M. Orta-Martínez, and A. Rosell-Melé (2019). Anthropogenic lead in Amazonian wildlife. Nature Sustainability 2:702–709. Google Scholar 8. Church, M. E., R. Gwiazda, R. W. Risebrough, K. Sorenson, C. P. Chamberlain, S. Farry, W. Heinrich, B. A. Rideout, and D. R. Smith (2006). Ammunition is the principal source of lead accumulated by California Condors reintroduced to the wild. Environmental Science and Technology 40:6143–6150. Google Scholar 9. Crandall, R. H., D. J. Craighead, B. Bedrosian, and V. A. Slabe (2019). Survival estimates and cause of mortality of Golden Eagles in south-central Montana. Journal of Raptor Research 53:38–45. Google Scholar 10. Davies, D. J. A., I. Thornton, J. M. Watt, E. B. Culbard, P. G. Harvey, H. T. Delves, J. C. Sherlock, G. A. Smart, J. F. A. Thomas, and M. J. Quinn (1990). Lead intake and blood lead in two-year-old UK urban children. Science of the Total Environment 90:13–29. Google Scholar 11. Ecke F., N. J. Singh, J. M. Arnemo, A. Bignert, B. Helander, Å. M. M. Berglund, H. Borg, C. Bröjer, K. Holm, M. Lanzone, T. Miller, et al. (2017). Sublethal lead exposure alters movement behavior in free-ranging Golden Eagles. Environmental Science and Technology 51:5729–5736. Google Scholar 12. Feierabend, J. S., and O. Myers (1984). A National Summary of Lead Poisoning in Bald Eagles and Waterfowl. National Wildlife Federation, Washington, DC, USA. Google Scholar 13. Finkelstein, M. E., J. Brandt, E. Sandhaus, J. Grantham, A. Mee, P. J. Schuppert, and D. R. Smith (2015). Lead exposure risk from trash ingestion by the endangered California Condor (Gymnogyps californianus). Journal of Wildlife Diseases 51:901–906. Google Scholar 14. Finkelstein, M. E., D. F. Doak, D. George, J. Burnett, J. Brandt, M. Church, J. Grantham, and D. R. Smith (2012). Lead poisoning and the deceptive recovery of the critically endangered California Condor. Proceedings of the National Academy of Science 109:11449–11454. Google Scholar 15. Finkelstein, M. E., D. George, S. Scherbinski, R. Gwiazda, M. Johnson, J. Burnett, J. Brandt, S. Lawrey, A. P. Pessier, M. Clark, and J. Wynne (2010). Feather lead concentrations and 207Pb/206Pb ratios reveal lead exposure history of California Condors (Gymnogyps californianus). Environmental Science and Technology 44:2639–2647. Google Scholar 16. Fisher, I. J., D. J. Pain, and V. G. Thomas (2006). A review of lead poisoning from ammunition sources in terrestrial birds. Biological Conservation 131:421–432. Google Scholar 17. Franson, J. C., and D. J. Pain (2011). Environmental contaminants in biota: Interpreting tissue concentrations. InLead in Birds, Second Ed. ( W. N. Beyer and J. P. Meador, Editors). CRC Press, Boca Raton, FL, USA. pp. 563–594. Google Scholar 18. Friend, M. (1999). Lead. InField Manual of Wildlife Diseases: General Field Procedures and Diseases of Birds ( M. Friend and J. C. Franson, Editors). US Geological Survey, Biological Resources Division, Madison, WI, USA. pp. 317–334. Google Scholar 19. Gangoso, L., P. Álvarez-Lloret, A. B. Rodríguez-Navarro, R. Mateo, F. Hiraldo, and J. A. Donázar (2009). Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources. Environmental Pollution 157:569–574. Google Scholar 20. Garbett, R., G. Maude, P. Hancock, D. Kenny, R. Reading, and A. Amar (2018). Association between hunting and elevated blood lead levels in the critically endangered African White-backed Vulture Gyps africanus. Science of the Total Environment 630:1654–1665. Google Scholar 21. Gil-Sánchez, J. M., S. Molleda, J. A. Sánchez-Zapata Bautista, I. Navas, R. Godinho, A. J. García-Fernández, and M. Moleón (2018). From sport hunting to breeding success: Patterns of lead ammunition ingestion and its effects on an endangered raptor. Science of the Total Environment 613:483–491. Google Scholar 22. Haig, S. M., J. D'Elia, C. Eagles-Smith, J. M. Fair, J. Gervais, G. Herring, J. W. Rivers, and J. H. Schulz (2014). The persistent problem of lead poisoning in birds from ammunition and fishing tackle. The Condor 116:408–428. Google Scholar 23. Hansen, E., C. Lassen, and A. Elbaek-Jørgensen (2004). Advantages and Drawbacks of Restricting the Marketing and Use of Lead in Ammunition, Fishing Sinkers and Candle Wicks. Enterprise Directorate-General, European Commission, Brussels, Belguim. Google Scholar 24. Helander, B., J. Axelsson, H. Borg, K. Holm, and A. Bignert (2009). Ingestion of lead from ammunition and lead concentrations in White-tailed Sea Eagles (Haliaeetus albicilla) in Sweden. Science of the Total Environment 407:5555–5563. Google Scholar 25. Henny, C. J., L. J. Blus, D. J. Hoffman, R. A. Grove, and J. S. Hatfield (1991). Lead accumulation and Osprey production near a mining site on the Coeur d'Alene River, Idaho. Archives of Environmental Contamination and Toxicology 21:415–424. Google Scholar 26. Ishii, C., S. M. M. Nakayama, Y. Ikenaka, H. Nakata, K. Saito, Y. Watanabe, H. Mizukawa, S. Tanabe, K. Nomiyama, T. Hayashi, and M. Ishizuka (2017). Lead exposure in raptors from Japan and source identification using Pb stable isotope ratios. Chemosphere 186:367–373. Google Scholar 27. Isomursu, M., J. Koivusaari, T. Stjernberg, V. Hirvelä-Koski, and E. R. Venäläinen (2018). Lead poisoning and other human-related factors cause significant mortality in White-tailed Eagles. Ambio 47:858–868. Google Scholar 28. Jørgensen, S. S., and M. Willems (1987). The fate of lead in soils: The transformation of lead pellets in shooting-range soils. Ambio 16:11–15. Google Scholar 29. Katzner, T. E., M. J. Stuber, V. A. Slabe, J. T. Anderson, J. L. Cooper, L. L. Rhea, and B. A. Millsap (2018). Origins of lead in populations of raptors. Animal Conservation 21:232–240. Google Scholar 30. Kitowski, I., D. Jakubas, D. Wiącek, and A. Sujak (2017). Concentrations of lead and other elements in the liver of the White-tailed Eagle (Haliaeetus albicilla), a European flagship species, wintering in Eastern Poland. Ambio 46:825–841. Google Scholar 31. Krone, O. (2018). Lead poisoning in birds of prey. InBirds of Prey ( J. H. Sarasola, J. M. Grande, and J. J. Negro, Editors). Springer International Publishing, Cham, Switzerland. pp. 251–272. Google Scholar 32. Krone, O., N. Kenntner, A. Trinogga, M. Nadjafzadeh, F. Scholz, J. Sulawa, K. Totschek, P. Schuck-Wersig, and R. Zieschank (2009). Lead poisoning in White-tailed Sea Eagles: Causes and approaches to solutions in Germany. InIngestion of Lead from Spent Ammunition: Implications for Wildlife and Humans ( R. T. Watson, M. Fuller, M. Pokras, and W. G. Hunt, Editors). The Peregrine Fund, Boise, ID, USA. pp. 289–301. Google Scholar 33. Lambertucci, S. A., J. A. Donázar, A. D. Huertas, B. Jiménez, M. Sáez, J. A. Sanchez-Zapata, and F. Hiraldo (2011). Widening the problem of lead poisoning to a South-American top scavenger: Lead concentrations in feathers of wild Andean Condors. Biological Conservation 144:1464–1471. Google Scholar 34. Lambertucci, S. A., A. Trejo, S. Di Martino, J. A. Sánchez-Zapata, J. A. Donázar, and F. Hiraldo (2009). Spatial and temporal patterns in the diet of the Andean Condor: Ecological replacement of native fauna by exotic species. Animal Conservation 12:338–345. Google Scholar 35. Langner, H. W., R. Domenech, V. A. Slabe, and S. P. Sullivan (2015). Lead and mercury in fall migrant Golden Eagles from western North America. Archives of Environmental Contamination and Toxicology 69:54–61. Google Scholar 36. Langner, H. W., E. Greene, R. Domenech, and M. F. Staats (2012). Mercury and other mining-related contaminants in Ospreys along the Upper Clark Fork River, Montana, USA. Archives of Environmental Contamination and Toxicology 62:681–695. Google Scholar 37. Lohr, M. T., J. O. Hampton, S. Cherriman, F. Busetti, and C. Lohr (2020). Completing a worldwide picture: preliminary evidence of lead exposure in a scavenging bird from mainland Australia. Science of the Total Environment 715:135913. https://doi.org/10.1016/j.scitotenv.2019.135913 . Google Scholar 38. Madden, K. K., G. C. Rozhon, and J. F. Dwyer (2019). Conservation Letter: Raptor persecution. Journal of Raptor Research 53:230–233. Google Scholar 39. Madry, M. M., T. Kraemer, J. Kupper, H. Naegeli, H. Jenny, L. Jenni, and D. Jenny (2015). Excessive lead burden among Golden Eagles in the Swiss Alps. Environmental Research Letters 10:034003. https://iopscience.iop.org/article/10.1088/1748-9326/10/3/034003 . Google Scholar 40. Mateo, R., and N. Kanstrup (2019). Regulations on lead ammunition adopted in Europe and evidence of compliance. Ambio 48:989–998. Google Scholar 41. Nadjafzadeh, M., H. Hofer, and O. Krone (2013). The link between feeding ecology and lead poisoning in White-tailed Eagles. Journal of Wildlife Management 77:48–57. Google Scholar 42. Naidoo, V., K. Wolter, I. Espie, and A. Kotze (2012). Lead toxicity: Consequences and interventions in an intensively managed vulture colony. Journal of Zoo and Wildlife Medicine 43:573–578. Google Scholar 43. Pain, D. J., I. J. Fisher, and V. G. Thomas (2009). A global update of lead poisoning in terrestrial birds from ammunition sources. The Peregrine Fund, Boise, ID, USA. pp. 99–118. Google Scholar 44. Pain, D. J., R. Mateo, and R. E. Green (2019). Effects of lead from ammunition on birds and other wildlife: A review and update. Ambio 48:935–953. Google Scholar 45. Pain, D. J., J. Sears, and I. Newton (1995). Lead concentrations in birds of prey in Britain. Environmental Pollution 87:173–180. Google Scholar 46. Pattee, O. H., J. W. Carpenter, S. H. Fritts, B. A. Rattner, S. N. Wiemeyer, J. A. Royle, and M. R. Smith (2006). Lead poisoning in captive Andean Condors (Vultur gryphus). Journal of Wildlife Diseases 42:772–779. Google Scholar 47. Plaza, P. I., and S. A. Lambertucci (2019). What do we know about lead contamination in wild vultures and condors? A review of decades of research. Science of the Total Environment 654:409–417. Google Scholar 48. Plaza, P.I., M. Uhart, A. Caselli, G. Wiemeyer, and S. A. Lambertucci (2018). A review of lead contamination in South American birds: The need for more research and policy changes. Perspectives in Ecology and Conservation 16:201–207. Google Scholar 49. Raptor Research Foundation (RRF) (2020). About us. https://raptorresearchfoundation.org/about/history/ . Google Scholar 50. Rattner, B. A., J. C. Franson, S. R. Sheffield, C. I. Goddard, N. J. Leonard, D. Stang, and P. J. Wingate (2008). Sources and Implications of Lead Ammunition and Fishing Tackle on Natural Resources. Wildlife Society Technical Review 08-01. The Wildlife Society, Bethesda, MD, USA. Google Scholar 51. Rideout, B. A., I. Stalis, R. Papendick, A. Pessier, B. Puschner, M. E. Finkelstein, D. R. Smith, M. Johnson, M. Mace, R. Stroud, J. Brandt, et al. (2012). Patterns of mortality in free-ranging California Condors (Gymnogyps californianus). Journal of Wildlife Diseases 48:95–112. Google Scholar 52. Russell, R. E., and J. C. Franson (2014). Causes of mortality in eagles submitted to the National Wildlife Health Center 1975–2013. Wildlife Society Bulletin 38:697–704. Google Scholar 53. Saito, K. (2009). Lead poisoning of Steller's Sea-eagle (Haliaeetus pelagicus) and White-tailed Eagle (Haliaeetus albicilla) caused by the ingestion of lead bullets and slugs, in Hokkaido Japan. InIngestion of Lead from Spent Ammunition: Implications for Wildlife and Humans ( R. T. Watson, M. Fuller, M. Pokras, and W. G. Hunt, Editors). The Peregrine Fund, Boise, ID, USA. pp. 302–309. Google Scholar 54. Scheuhammer, A. M. (1987). The chronic toxicity of aluminium, cadmium, mercury and lead in birds: A review. Environmental Pollution 46:263–295. Google Scholar 55. Scheuhammer, A. M., and S. L. Norris (1996). The ecotoxicology of lead shot and lead fishing weights. Ecotoxicology 5:279–295. Google Scholar 56. Schulz, J. H., J. J. Millspaugh, B. E. Washburn, G. R. Wester, J. T. Lanigan, III , and J. C. Franson (2002). Spent-shot availability and ingestion on areas managed for Mourning Doves. Wildlife Society Bulletin 30:112–120. Google Scholar 57. Sieg, R., K. A. Sullivan, and C. N. Parish (2009). Voluntary lead reduction efforts within the northern Arizona range of the California Condor. InIngestion of Lead from Spent Ammunition: Implications for Wildlife and Humans ( R. T. Watson, M. Fuller, M. Pokras, and W. G. Hunt, Editors). The Peregrine Fund, Boise, ID, USA. pp 341–349. Google Scholar 58. Slabe, V. A., J. T. Anderson, J. Cooper, T. A. Miller, B. Brown, A. Wrona, P. Ortiz, J. Buchweitz, D. McRuer, E. Dominguez-Villegas, and S. Behmke (2020). Feeding ecology drives lead exposure of facultative and obligate avian scavengers in the eastern United States. Environmental Toxicology and Chemistry 39:882–892. Google Scholar 59. Spurling, P., L. Brown, and C. Parish (2018). The North American Non-lead Partnership, Version 1. The Peregrine Fund, Boise, ID, USA. http://www.nonleadpartnership.org . Google Scholar 60. Stroud, D. A. (2015). Regulation of some sources of lead poisoning: A brief review. InProceedings of the Oxford Lead Symposium. Lead Ammunition: Understanding and Minimising the Risks to Human and Environmental Health ( R. J. Delahay and C. J. Spray, Editors). Oxford University, Oxford, UK. pp. 8–26. Google Scholar 61. Thomas, V. G. (2019). Chemical compositional standards for non-lead hunting ammunition and fishing weights. Ambio 48:1072–1078. Google Scholar 62. US Fish and Wildlife Service (2016). Bald and Golden Eagles: Population Demographics and Estimation of Sustainable Take in the United States, 2016 Update. USDI Fish and Wildlife Service, Division of Migratory Bird Management, Washington, DC, USA. Google Scholar 63. Watson, R. T., M. Fuller, M. Pokras, and W. G. Hunt (Editors) (2009). Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, ID, USA. Google Scholar 64. Wayland, M., L. K. Wilson, J. E. Elliott, M. J. R. Miller, T. Bollinger, M. McAdie, K. Lagelier, J. Keating, and J. M. W. Froese (2003). Mortality, morbidity, and lead poisoning of eagles in western Canada, 1986–98. Journal of Raptor Research 37:8–18. Google Scholar 65. Wiemeyer, G. M., M. A. Pérez, L. Torres, L. Sampietro, G. F. Bravo, N. L. Jácome, V. Astore, and S. A. Lambertucci (2016). Repeated conservation threats across the Americas: High levels of blood and bone lead in the Andean Condor widen the problem to a continental scale. Environmental Pollution 220(Part A):672–679. Google Scholar
... California condors (Gymnogyps californianus), one of the world's most endangered species (IUCN, 2019), are frequently exposed to lead via ingestion of spent lead-based ammunition (Cade, 2007;Church et al., 2006;Finkelstein et al., 2012). At least 50% of wild California condors have been exposed to lead at levels high enough to receive clinical treatment (e.g. ...
Article
Wild California condors (Gymnogyps californianus) are frequently exposed to lead via lead-based ammunition ingestion, and recent studies indicate significant exposure to organochlorines (e.g. dichlorodiphenyldichloroethylene (DDE) and polychlorinated biphenyls (PCBs)) for condors feeding on beach-cast marine mammals. We investigated the influence of contaminant exposure on condor glucocorticoid response through comparisons between wild and captive populations and identified modifiers of glucocorticoid release. We assessed the glucocorticoid response to routine trapping and handling events through measurement of plasma corticosterone and urate glucocorticoid metabolites (GCM). Comparison of peak urate GCM levels showed wild condors exhibited higher responses to handling-associated stressors (2250 ± 1440 ng/g dry wt, average +/- SD, n=27) than captive condors (907 ± 489 ng/g dry wt., n=6, U = 28, p = 0.003). Multiple linear regression models and an information theoretic approach (AICc) identified several extrinsic variables (e.g., time captive in flight pen before sample collection) that were negatively associated with plasma corticosterone and urate GCM levels in wild condors, which explained ∼25% of glucocorticoid variation. When accounting for these extrinsic variables we found that behavioral variables associated with increased lead and organochlorine exposure risk were positively associated with GCM levels, explaining an additional 15% of glucocorticoid variation among wild condors. Days absent from management area, a variable associated reduced survival attributed to increased lead exposure risk, had a positive influence on plasma corticosterone levels (β = 53 ± 20 SE) and peak urate GCM levels (β = 1090 ± 586 SE). Years observed feeding on marine mammals, a variable positively associated with DDE and PCB exposure, positively influenced peak urate GCM (β = 1100 ± 520 SE) and the magnitude of GCM response (peak GCM – 1st urate GCM) (β = 1050 ± 500 SE). Our findings suggest that individual propensities for these higher risk foraging behaviors predict higher stress-induced glucocorticoid levels in wild condors, and that accounting for variables associated with trapping and handling is essential for assessing the impact of environmental stressors such as contaminants on the condor stress response. As an abnormal glucocorticoid response to stress is associated with reduced reproduction and survival in vertebrates, this work indicates the critical need for further investigations into the physiological impacts of sub-lethal contaminant exposures in scavenging species worldwide.
... In fact, lead is one of the most toxic metals known to affect the health status of different avian guilds, especially vultures (De Francisco et al. 2003, Haig et al. 2014, Plaza & Lambertucci 2019. Today, the main source of lead affecting bird populations is the ingestion of ammunition or bullet fragments produced by hunting activities (Fisher et al. 2006, Cade 2007, Pain et al. 2009, Williams et al. 2018. Depending on the lead concentrations reached in different tissues and organs, the negative impacts of lead vary from subtle sub-clinical changes to serious and lethal effects (De Francisco et al. 2003, Haig et al. 2014, Ferreyra et al. 2015. ...
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.
... Lead is an anthropogenic poison that negatively affects all major systems of the body. A variety of wildlife species are affected by lead, including neotropical migrant songbirds (Lewis et al. 2001), carnivores (Rogers et al. 2012), and the critically endangered California condor (Gymnogyps californianus) (Cade 2007). One of the most common pathways of lead exposure in birds is ingestion of contaminated food sources (Pokras and Kneeland 2008). ...
Article
Full-text available
Lead is toxic to humans and wildlife. Most studies of lead exposure of raptors focus on the winter, non-breeding season when they scavenge heavily. We evaluated blood lead concentrations (BLCs) of red-shouldered hawks (Buteo lineatus) during the non-scavenging season in the eastern United States. BLCs of 53 of 70 hawks were above the limit of detection (x¯ = 9.25 µg/dL ± 19.81; ± SD). Adult hawks had higher BLCs (x¯ = 12.86 µg/dL ± 24.72) than did nestlings (x¯ = 3.25 µg/dL ± 2.62; p ≤ 0.001, χ2 = 13.2). There was no difference in BLCs of adult hawks among physiographic provinces but there were differences between urban and non-urban settings (p = 0.04, χ2 = 4.2). Soils and invertebrate hawk prey also had quantifiable lead concentrations. Our work shows that red-shouldered hawks are exposed to lead when not scavenging, and suggests pathways by which these birds may be exposed.
... Los catártidos, debido a su posición en la red trófica y longevidad, están en riesgo de acumulación de metales pesados en sus tejidos, ya que fungen como bioindicadores de la contaminación ambiental (4,8). Tanto aves de vida libre como en cautiverio están en riesgo de la intoxicación con plomo, pues se reporta toxicosis en especies como el águila calva (Haliaeetus leucocephalus) (9), el pigargo europeo (Haliaeetus albicilla) (10), el cóndor californiano (Gymnogyps californianus) (11,12), el buitre leonado (Gyps fulvus) (1,13), el águila imperial ibérica (Aquila adalberti) (14), el buitre negro americano (Coragyps atratus) (15), entre otras. ...
Article
Full-text available
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.
... Pb from bullet fragments in hunter-killed game ( Herring et al. 2016;Hunt et al. 2006; Knopper et al. 2006), and its potential effects on raptors and other avian species that scavenge carrion has received considerable attention in recent years (Cade 2007; see e.g., Church et al. 2006;Craighead and Bedrosian 2008;Cruz-Martinez et al. 2012;Ecke et al. 2017;Herring et al. 2017, Herring et al. 2016). Golden Eagles (Aquila chrysaetos) are known to feed on carcasses and offal from hunter-killed game (referred to as game carcasses throughout the remainder of the text; Ecke et al. 2017). ...
Chapter
Environmental contaminants like lead (Pb) can pose a threat to wildlife populations, particularly raptors. However, the sources and consequences associated with exposure are often complex and difficult to assess. Machine learning models are suitable for prediction and for gaining biologically meaningful insight into the potential impacts of Pb on wildlife populations. However, despite their potential, they are often under-utilized in the field of ecology. We used TreeNet, a machine learning algorithm, and six variables to investigate the incidence of elevated blood lead levels (eBLL; >0.20 ppm wet weight) in a population of wintering Golden Eagles captured in Idaho (winter 1989–90 through winter 1997–98). Our best model had 76.7% accuracy overall in predicting the presence or absence of eBLL in an independent sample of wintering eagles from the study area. TreeNet results were also corroborated by traditional statistical analyses done in an earlier study and the findings of others, but provided additional information not revealed by those analyses. All six variables were important for predicting the incidence of Pb contamination in eagles and were characterized by multiple complex interactions. Winter of capture had the greatest influence on predicting eagles with eBLL, followed by time of day captured. Month in which an eagle was captured, gender, valley of capture and age class were all about equally important to model prediction. Eagles with eBLL were most likely to be captured later in the day and during the months of December and January. The evidence from our analysis agrees with results from other areas by indicating that the primary source of Pb to the eagles in our study area was most likely related to Pb contaminated carcasses or offal from hunter-killed animals. However, female Golden Eagles, in our study area, and especially adult females, were more likely to have eBLL than males; similar gender differences have been reported for other avian species but not previously for Golden Eagles. Juveniles were least likely of the free-ranging eagles captured during winter to have eBLL and no nestlings and eagles sampled during summer had eBLL. Our results help to identify members of the population most at risk to contaminants, highlighting gender and age related differences that may be of broader geographic and population-level importance. Lastly, our results provide information potentially relevant for informing future population models, conservation efforts and direction for further research.
... ML has been used for decades in investigating the causes of disease in human populations (Collij et al. 2016; see e.g., Cooper et al. 1997;Cruz and Wishart 2006;Moradi et al. 2015;Sriram et al. 2013) and the incidence of contaminants in the environment (see e.g., Hu and Cheng 2013;Wang et al. 2015), but remains under-utilized in ecology (Thessen 2016). Pb from bullet fragments in hunter-killed game (Herring et al. 2016;Hunt et al. 2006;Knopper et al. 2006), and its potential effects on raptors and other avian species that scavenge carrion has received considerable attention in recent years (Cade 2007; see e.g., Church et al. 2006;Craighead and Bedrosian 2008;Cruz-Martinez 244 et al. 2012;Ecke et al. 2017;, Herring et al. 2016. Golden Eagles (Aquila chrysaetos) are known to feed on carcasses and offal from hunter-killed game (referred to as game carcasses throughout the remainder of the text; Ecke et al. 2017). ...
Chapter
Full-text available
Climate change is acting to reallocate biomes and shift the distribution of species in Alaska, where many animals exist near their thermodynamic limits. Machine-learning based ecological niche models that account for landscape characteristics and changes in climate have been effective tools for deciphering patterns in messy, presence-only datasets, and predicting shifts in wildlife distributions over time. Bioclimatic niche models are sometimes criticized for failing to include interspecific interactions into predictions of species distributions. Here I address this shortcoming by including the previously-modeled distributions of 17 species of small mammal prey as well as 36 environmental predictors to develop distribution models for a generalist predator, the American marten (Martes americana) in Alaska. I used TreeNet and a set of public, online, occurrence records as training data in 13 model variations to create the most accurate ecological niche model for marten in 2015. I also used Intergovernmental Panel on Climate Change A2 scenario climate forecasts and future small mammal distributions to forecast marten distribution in 2100. Additionally, I used TreeNet to quantify the magnitude of variable interactions, and network maps to visualize structure in predictor set relationships. I found that (1) sub-models with a reduced set of predictors are capable of achieving higher predicted accuracies than models based on the entire predictor set, (2) top predictors and interaction strengths can be disproportionately influenced by high-level categorical predictors, and (3) a landscape change analysis identified regions of Alaska where the distribution of marten is predicted to expand with climate change over the coming century. Incorporating the interactive influence of prey and other environmental variables in order to improve distribution change projections should aid wildlife and land managers in developing adaptive strategies for conserving dispersal corridors, biodiversity, and ecosystem function into the future.
... Pb has been labeled by the International Agency for Research on Cancer, the National Toxicology Program, and the US Environmental Protection Agency as a carcinogen and endocrine disrupter. The eff ects on condors are crop paralysis and impending starvation (Cade, 2007), and the eff ects on human populations are neurological defects, cardiovascular eff ects, reduced kidney function, and reproductive issues in both sexes (EPA, 2018). ...
... The failure of hunting groups to recognize the compelling science behind threats to scavenging animals posed by lead and the failure to voluntarily switch to lead-free based bullets is threatening the sustainability and social license of hunting (Kanstrup et al. 2018). Despite consistent calls from scientists for a voluntary transition to lead-free bullets for over a decade (Cade 2007), hunting groups have opposed this proposition and have lobbied for reversal of legislation restricting the use of lead-based bullets (Volcovici 2017). Despite the short-term gains achieved by such advocacy, we suggest that the long-term social license of hunting may be threatened by such moves that show little concern for the welfare of unintentionally affected wildlife. ...
... Pb exposure can cause a variety of sub-lethal toxic effects and direct mortality (Kendall et al., 1996). Sub-lethal effects of Pb are exerted on the nervous system, kidney, liver, intestines and circulatory system, resulting in physiological, biological and behavioral changes (Cade, 2007;Fisher et al., 2006;Scheuhammer, 1987). Pb exposure also decrease the activity of d-aminolevulinic acid dehydratase (ALA-d) -an enzyme of the heme biosynthesis pathway (Binkowski and Sawicka-Kapusta, 2015). ...
... Corvid species have also shown harmful Pb exposure (e.g. common ravens; Corvus corax; Table 2; Bedrosian 2008, 2009;West et al. 2017). The best studied bird species to be affected by Pb from bullets is likely to be the California condor (Gymnogyps californianus; Church et al. 2006;Cade 2007;Green et al. 2008;Finkelstein et al. 2012 ; Table 1 West et al. 2017;Specht et al. 2018). This is a worldwide phenomenon, with harmful Pb exposure from bullet-derived Pb having been reported from scavenging bird species in North America, Europe and Asia for decades, and more recent reports from South America (Lambertucci et al. 2011) and Africa (Garbett et al. 2018; Table 2). ...
Article
Full-text available
Lead (Pb) is a toxic element banned from fuel, paint and many other products in most developed countries. Nonetheless, it is still widely used in ammunition, including rifle bullets, and Pb-based bullets are almost universally used in Australia. For decades, poisoning from Pb shot (shotguns) has been recognised as a cause of disease in waterfowl and Pb shot has been subsequently banned for waterfowl hunting in many jurisdictions. However, the risks posed by Pb-based bullets (rifles) have not been similarly recognised in Australia. Pb-based rifle bullets frequently fragment, contaminating the tissue of shot animals. Consuming this Pb-contaminated tissue risks harmful Pb exposure and, thus, the health of wildlife scavengers (carrion eaters) and humans and their companion animals who consume harvested meat (game eaters). In Europe, North America and elsewhere, the environmental and human health risks of Pb-based bullets are widely recognised, and non-toxic alternatives (e.g. copper-based bullets) are increasingly being used. However, Australia has no comparable research despite widespread use of shooting, common scavenging by potentially susceptible wildlife species, and people regularly consuming shot meat. We conclude that Australia has its collective ‘head in the sand’ on this pressing worldwide One Health issue. We present the need for urgent research into this field in Australia.
... This has been proven further by comparing lead isotope signatures from tissue of raptors with isotope ratios from ammunition (Berny et al. 2015;Church et al. 2006;Fisher et al. 2006;Helander et al. 2009;Lambertucci et al. 2011;Madry et al. 2015;Mateo et al. 2001;Pain et al. 2007;Scheuhammer and Templeton 1998) and feeding ecology (Nadjafzadeh et al. 2013). An increase in mortality or blood lead levels in birds of prey and other scavengers such as ravens correlating with hunting seasons has been demonstrated several times (Craighead and Bedrosian 2007;Kelly et al. 2014;Kramer and Redig 1997;Krone et al. 2009a;Cade 2007;Cruz-Martinez et al. 2012;Stauber et al. 2010;Strom et al. 2009). ...
Chapter
Full-text available
Naturally lead (plumbum, Pb) is embedded in the earth’s crust at a concentration of 0.016 g Pb/kg soil, making it a relatively rare metal. From there it is released into the environment by geochemical weathering, igneous processes and radioactive decay (Pattee and Pain 2003). Lead is probably the first metal used by mankind. It was known as opacifier and colourant for glazes and glasses since the fifth millennium B.C. But lead pigment has also been used in cosmetics as long ago as 4000 B.C. due to its softness and low melting point (327.5 °C); it is easily mined and moulded. Formed to coins and figures, lead played an important role in trading more than 4500 years ago in ancient Egypt. As a component of many metallic ores, lead was also considered as a by-product of mining precious metals such as silver. Cooking utensils have been made of lead, and lead piping was the mainstay of the water distribution system in the Roman Empire (Nriagu 1983). Since the Romans did not know sugar, they produced sapa, a syrup made of sweet fruits boiled in lead vessels. Sapa containing lead was used to sweeten drinks and meals. Lead poisoning from all these sources must have been a common disease in ancient Rome. Symptoms included colic, stillbirths, deformities and cases of brain damage. Although controversial (Scarborough 1984), high lead concentrations diagnosed in archaeological Roman bones arguably contributed to the fall of the Roman Empire (Gilfillan 1965). Described in antiquity, lead poisoning was no more mentioned in the literature until the Middle Ages, where it was then mentioned sporadically. Due to the increased use of lead in pottery, piping, shipbuilding, window making, arms industry, pigments and later book printing, lead poisoning reached epidemic dimensions during the period of industrialisation (Hernberg 2000). For millennia the main route of lead exposure was primarily via occupation, but the introduction of leaded paint for residential use in the nineteenth century significantly increased lead accumulation in children (Bellinger 2004). Symptoms in children from lead paint recognised in Australia contributed largely to the understanding of childhood lead poisoning (Henretig 2006). European governments started to ban lead-based paints in the early 1900s, culminating in a ban by the League of Nations in 1922 (Gilbert and Weiss 2006).
... The curious nature of pet birds leads them to ingest shiny objects easily. Temporal and spatial patterns of lead intoxication in California condors coinciding with anthropogenic activities such as big game hunting have been recorded (Cade, 2007). ...
Chapter
There are approximately 30 orders of birds in the Aves class, with approximately 2000 genera and 10,000 species. Obviously, such a large class of animals possesses a bewildering array of unique physiologic adaptations, behaviors, and ecologic niches that predispose them to potential intoxication from numerous natural and man-made toxicants in their environment. There is a large body of toxicologic information specific to birds because they occupy a prominent place in natural and altered ecosystems as research animals, as a food source, and as pets. Given the breadth of the topic, this chapter is not an exhaustive treatise but, it is hoped, provides an overview of major avian toxicologic hazards for pet and aviary birds, poultry and other farm-raised birds, and wild birds.
... Food shortages seem to have prompted Bearded Vultures to exploit less predictable food sources, possibly including wild prey species (Oro et al., 2008;Hernández and Margalida, 2008). Our findings show that PCBs values increased with the time suggesting a change in feeding habits that increased their exposure to lead poisoning since wild prey, including carcasses and offal from ungulates killed by hunters, may contain lead shot pellets or bullet fragments (Cade, 2007) and increases the risk of their consuming deliberately poisoned animals (Oro et al., 2008;Hernández and Margalida, 2009). However, the provision of specialized feeding stations obscures the effects of food shortages (Oro et al., 2008;Margalida et al., 2014). ...
Article
The Spanish Bearded Vulture (Gypaetus barbatus) population has suffered from negative trends in a number of reproductive parameters that could jeopardize its long-term viability. From 1989 to 2012, 27 entire eggs and 63 eggshell fragments were collected from nests after breeding failure and/or fledging. Longer-term changes in eggshell thickness were made by examining 69 eggs collected in Spain from 1858 to 1911, and now held in European museums. Low levels of contamination with organochlorine pesticides and polychlorinated biphenyls were found in whole eggs and in conjunction with the high fertility rates observed in the field (66.7%) do not indicate a population suffering from the effects of organochlorine contamination. However, a decrease in the Ratcliffe Index and eggshell thickness were observed in eggs collected since 2001, increasingly so in samples post-2004, indicating an abrupt loss of egg quality. We found no significant relationship between organochlorine residues and eggshell in any of the variables measured. In contrast, we found a positive relationship between food availability and the Ratcliffe Index, eggshell thickness and eggshell surface area. A density-dependent explanation of reduced egg quality could arise from ecological constraints as the decrease of food resources. The impact of sudden changes in food availability due to sanitary regulations between 2006 and 2011 could be related with the loss of Bearded Vulture egg quality.
... The result for the bird may be "choking, poisoning, intestinal obstruction, malnutrition and death," especially for nestlings which cannot regurgitate indigestible items (Ferro, 2000;BirdLife International, 2008). The extremely rare California condor was nearly brought to extinction by lead poisoning among other factors (Cade, 2007). After captive bred birds were introduced into the wild for species recovery, nestlings were recorded with plastic piping, cloth, rubber, glass, metal bottle-tops and even ammunition cartridges in their stomachs; physiological impacts on nestlings include zinc poisoning, malnutrition induced feather retardation, largely due to retarded feather development resulting from obstructed digestive passages. ...
Chapter
This study examines the organizational practices of transportation agencies in the Greater Yellowstone Ecosystem (GYE) to reveal the barriers to wildlife-crossing implementation produced by the culture of these bureaucratic institutions. Through the identification of these cultural barriers and potential measures and practical approaches to surmount these obstacles, this study addresses the critical need to inform and motivate the environmental community to transform the institutional “lack of attention” to crossing structures into a standard approach in which transportation agencies consistently incorporate these structures into their plans and projects. The findings are intended to provide conservation professionals with methods and solutions to effectively facilitate change in the organizational structure and institutional practices of transportation agencies to support human and wildlife safety and connectivity. Specifically, it will (1) inform the environmental community and North American public on the cultural barriers in transportation agencies that obstruct individual agents’ ability and willingness to deviate from or alter their organization’s practices, and (2) ensure that the transportation sector is held accountable for consistently implementing wildlife crossings, thereby ensuring the conservation of ungulates, carnivores, and other large mammals in the GYE and beyond.
... Quantifying population-level effects due to contaminant exposure is exceedingly difficult. The only raptor species in North America for which population effects have been attributed to lead exposure is the California Condor (Cade 2007, Walters et al. 2010, Finkelstein et al. 2012). In other avian groups, such as waterfowl, annual population level losses due to direct lead poisoning from ingesting spent lead pellets were estimated to be 2– 3% of the annual fall migration or in excess of a million birds (Bellrose 1959). ...
Article
Full-text available
Contaminant exposure is among the many threats to Golden Eagle (Aquila chrysaetos) populations throughout North America, particularly lead poisoning and anticoagulant rodenticides (AR). These threats may act in concert with others (e.g., lead poisoning and trauma associated with striking objects) to exacerbate risk. Golden Eagles are skilled hunters but also exploit scavenging opportunities, making them particularly susceptible to contaminant exposure from ingesting tissues of poisoned or shot animals. Lead poisoning has long been recognized as an important source of mortality for Golden Eagles throughout North America. More recently, ARs have been associated with both sublethal and lethal effects in raptor species worldwide. In this review, we examine the current state of knowledge for lead and AR exposure in Golden Eagles, drawing from the broader raptor contaminant ecology literature. We examine lead and AR sources within Golden Eagle habitats, exposure routes and toxicity, effects on individuals and populations, synergistic effects, and data and information needs. Continued research addressing data needs and information gaps will help with Golden Eagle conservation planning.
... Because there is strong selection pressure on birds not to show external signs of illness and these clinical (i.e., recognizable symptoms on examination) signs associated with lead poisoning are nonspecific, diagnosis in the live bird relies on measurement of lead in blood. Background concentrations of lead in the blood of birds have been reported to be <20 mg/dL (<0.2 parts per million [ppm]; Pain et al. 2009, Stauber et al. 2010 although recently some authors have suggested that blood lead concentrations should be considered background only when <10 mg/dL (<0.1 ppm; Church et al. 2006, Cade 2007. There is general consensus that for most raptor species, blood lead concentrations 20 mg/dL (>0.2 ppm) clearly represent elevated blood lead (Kramer and Redig 1997, Pain et al. 2009, Stauber et al. 2010, Harmata 2011. ...
Article
Full-text available
Lead poisoning is a threat to birds, particularly scavenging birds of prey. With the availability of portable lead-testing kits, an increasing number of field researchers are testing wild-caught birds, in situ, for lead poisoning. We describe guidelines for evaluation of lead toxicity in wild raptors by outlining field testing of blood-lead concentrations, presenting criteria for removing a lead-poisoned bird from the wild for treatment, and suggesting strategies for effective treatment of lead intoxicated raptors. Field testing of birds is most commonly accomplished via portable electrochemical analysis of blood; visual observation of condition alone may provide insufficient evidence upon which to make a decision about lead poisoning. Our intended audience is not only the avian research community, but also rehabilitation facilities that may receive apparently uninjured birds. Best practices suggest that birds whose blood-lead levels are <40 μg/dL be released back to the wild as soon as possible after capture. The decision to release or treat birds with blood-lead levels between 40 μg/dL and 60 μg/dL should be made based on the presence of clinical signs of poisoning and relevant biological characteristics (e.g., breeding status). Finally, birds with blood-lead levels >60 μg/dL are potentially lethally poisoned and best served if removed from the wild for appropriate treatment at a licensed rehabilitation facility and later released. We present guidelines for decision-making when treating lead poisoning of wild raptors. Future work based on experimental studies will clarify the role of lead poisoning for specific species and be important to refine these guidelines to improve effectiveness.
... Episodi di saturnismo legati all'utilizzo del piombo nelle munizioni da caccia sono stati documentati per molte specie di uccelli rapaci (Locke e Thomas, 1996;Fisher et al., 2006). Il caso meglio studiato è rappresentato dal Condor della California (Gymnogyps californianus); ricerche accurate hanno dimostrato che l'assunzione del piombo attraverso l'ingestione di carni di ungulati abbattuti è la principale causa di morte per questo grosso avvoltoio e rappresenta il principale ostacolo alla creazione di una popolazione selvatica in grado di autosostenersi senza l'intervento dell'uomo (Snyder e Snyder, 2005;Cade, 2007). In Europa, intossicazioni da piombo sono state riscontrate per diverse specie, tra cui l'Aquila reale e il Gipeto Gypaetus barbatus (Knollseisen et al., 2006;Kenntner et al., 2007). ...
... Avian scavengers that typically include game birds and mammals in their diets are at risk of lead poisoning due to the ingestion of carcasses with residual or fragmented lead ammunition used in hunting. [6][7][8][9] The griffon vulture is a large bird of prey that belongs to the Old World vulture group and can be found over a wide geographic range (northwest Africa, Iberian Peninsula, Balkans, Middle East, and India). 10 Within the Iberian Peninsula, specifically in Portugal, the conservation status of this species is near-threatened. ...
Article
Avian scavengers that typically include game birds and mammals in their diets are at risk of lead poisoning from ingestion of carcasses with fragmented or residual lead ammunition that is used in hunting. Thus, lead may be one of the threats that the griffon vulture (Gyps fulvus) faces in the Iberian Peninsula and particularly in Portugal, where their conservation status is considered to be near-threatened. This is the first report that details 3 cases of lead poisoning, associated with the ingestion of lead shot, in adult female griffon vultures found in the Iberian Peninsula. The birds were found prostrate and immediately transferred to a wildlife rehabilitation center, where they died within 24 hours after supportive treatment. Necropsy and histopathologic examinations were done in 2 birds and metal analyses were done in all birds to determine the birds' causes of death. In one vulture, 9 uneroded lead pellets were recovered from the stomach, and moderate to severe hemosiderosis was seen histologically in the liver, lungs, and kidneys. Diagnosis of lead poisoning was confirmed by results of metal analyses, which revealed extremely high lead concentrations in blood (969-1384 μg/dL), liver (309-1077 μg/g dry weight), and kidneys (36-100 μg/g dry weight) for all 3 vultures. To prevent lead poisoning in vultures and preserve their populations in the Iberian Peninsula, more resources are needed for diagnosis and treatment of wildlife in rehabilitation centers, new regulations enabling the abandonment of fallen stock in the field must be approved, and lead ammunition must be prohibited in big-game hunting.
... Whereas earlier work focused on waterfowl and lead shotgun pellets (e.g., Anderson et al. 2000), most subsequent investigations have focused on avian pred-ators, scavengers, and granivores (Pain and Amiard-Triquet 1993;McBride et al. 2004;Hunt et al. 2006;Craighead and Bedrosian 2008;Helander et al. 2009;Hernández and Margalida 2009;Rogers et al. 2012;Haig et al. 2014;Warner et al. 2014). Lead bullet fragments in carcasses and gut piles from big game hunting are a major source of mortality for California condors (Church et al. 2006;Cade 2007;Stauber et al. 2010;Cruz-Martinez et al. 2012;Finkelstein et al. 2012;Rideout et al. 2012), leading to voluntary restrictions on the use of lead ammunition for hunting in Arizona and Utah (Arizona Game and Fish Department, Condors and Lead summary, Reference S1, http://www.azgfd.gov/w_c/california_ condor_lead.shtml) ...
Article
Full-text available
Lead bullet fragments pose a health risk to scavengers and hunters consuming game meat, but lead or lead-core bullets are still commonly employed for big and small game hunting. Bullet fragmentation has been assessed for modern, high-velocity rifles, but has not been well documented for black-powder cartridge rifles or muzzleloading firearms. We used two established methods to estimate bullet fragmentation. We evaluated a traditional .54 round ball and a modern-designed .54 conical bullet for muzzleloaders, two types of .45-70 black powder rifle cartridges, and a modern lead-core high-velocity bullet (.30-06) as our comparison control. We tested penetration and fragmentation in water (n=12) and ballistics gel (n=2) for each bullet type. We measured lead mass lost to fragmentation and x-rayed ballistic gels to visualize fragmentation patterns. The modern .30-06 bullets we tested (Remington Core-Lokt) retained a mean of only 57.5% of original mass, whereas mean retention by muzzleloader and black powder cartridge bullets ranged 87.8-99.7%. Round balls and .45-70 bullets shed less lead (i.e., 0.04g and 0.19g on average respectively) than the modern conical .54 muzzleloading bullets (3.08g) or the .30-06 control (4.14g). Fragments from round balls and black powder cartridge bullets showed far less lateral spread compared to the high-velocity modern bullet. Our findings suggest that round balls for muzzleloaders and black powder cartridge bullets may leave far fewer lead fragments in game than the conical muzzleloader bullet or modern high-velocity rifle bullet we tested, and thus could pose a lower risk of secondary lead poisoning for humans and wildlife. Artificial tests cannot replicate conditions encountered in the field, but the striking differences we observed in bullet fragmentation even under severe testing conditions suggests that follow-up tests on game animals may be warranted.
... Although the results from this study do not overturn our understanding of the systematic relationships of cathartids, they still provide important information about species phylogenetic relationships that may prove important to help set priorities for management and conservation. For example, high lead levels have been documented in tissue samples obtained from wild caught Black (Behmke et al., 2015) and Turkey Vultures (Martin et al., 2008;Kelly and Johnson, 2011;Behmke et al., 2015) and California Condors (Cade, 2007; see also Golden et al., 2016). In fact, continued exposure to spent lead ammunition has prevented the California Condor from establishing a self sustaining population after near extinction (Finkelstein et al., 2012;Kelly et al., 2014). ...
Chapter
Biogeochemistry, encompassing nearly all the factors for plant and animal ecological, chemical, and physical relations, has a close and even overlapping relation with the conservation sciences. In this relation, both the natural processes and human-constructed systems have severely affected the status of many plant and animal species, including their physiological and ecological dynamics. However, the information on these relations is largely scattered, focusing on the impacts of particular chemicals on particular species, rather than on combined chemical groups on ecosystems, and the possibilities for conservation science and policy. This chapter examines the role of the understanding of biogeochemistry in the development and effective conservation management and policy and how this may inform biogeochemical research. Current research findings indicate a shift in the relevance from global scale chemical flows to smaller scales at the regional, local, and even micro level scenarios. Case studies are taken of the impacts of lead, zinc, mercury, cadmium, arsenic, chromium, copper, and selenium, pesticides (including insecticides and rodenticides), veterinary compounds (such as nonsteroidal anti-inflammatory drugs or NSAIDs and polychlorinated biphenyls or PCBs), and industrial pollutants such as perfluoroalkyl substances on terrestrial, aquatic, and marine life, and the impacts of ameliorative policy actions. Conservation policies have been evolved to remedy these events, but in many cases, more research is required to remedy the impacts of the chemical changes. Significantly, chemical systems are increasingly studied in conjunction with conservation issues, and these actions have contributed to positive results for conservation efforts, and knowledge of conservation issues.
Article
Lead poisoning from feeding on carcasses shot with lead‐based ammunition is a well‐known threat to wildlife. Thus, nonlead (e.g., copper‐based) ammunition is promoted as a safe alternative. We present a unique situation of a male California condor ( Gymnogyps californianus ) discovered with both a lead fragment and a copper bullet in his digestive tract simultaneously. We show that ingestion of a copper bullet did not result in elevated blood copper concentrations, while ingestion of a lead fragment contributed to lead toxicity. Our findings can inform nonlead ammunition outreach efforts by demonstrating that ingestion of a copper‐based bullet did not result in the poisoning of a California condor.
Chapter
Full-text available
Large carnivores such as pumas are often killed in conflicts with humans because they prey on domestic livestock. Habitat loss, partly driven by the increasing use of traditional pasture systems, makes livestock vulneracle to puma attacks. The aim of this study was describe the conflict between local farmers and pumas in a mosais of Protected Areas in southern Brazil. We hypothesized that the farmer's preception, knowledge and attitudes towards the conflict with pumas is affected by socioeconomic variables, such as age, educaton, monthly income and farming experience. Forty-five face-to-face interviews with local farmers were performed in 2011, using a structured questionnaire with 16 open and 26 closed questions focusing on the perception farmers. Our results show that the majority of the local population considered the conflict with pumas a serious problem and thought that attacks by pumas on domestic herds shoud be controlled with the involvement of government authorities. Financial losses caused about pumas attacks on farms did not inflence the attitudes of farmers, and knowledge abou pumas was more inluenced by social variables such as age and educational level. Meetings with the local Rural Consulting Council revelated that conflict with pumas still remains in the region. In this context, a long-term educational program with local farmers is highly recommended, focused on engaging the community in the discussion about possible mitigations tools. Conservation wildlife depends on the ability to provaide decision makers with academic and traditional knowledge which could be build bridges between the commnunity and Environmental Agencies.
Book
INTRODUCTION This book is edited by two environmental scientists with interests in GIS and remote sensing applications, forest, and habitat change, and large animal ecology. It examines the cutting-edge issues related to animal and habitat ecology research and management, with case studies across Asia, the Americas, Africa, and Europe. The topics are based on research and reviews of specific and general topics covering the habitats as well as the species of importance in selected case studies, and the overall general scenarios. The chapters of the book are written by leading academic and field experts, who discuss their skills and research findings. The field covered is vast, so selectivity enters, based on concurrent and relevant subjects, such as field research techniques, nature-society relations, and chemistry in conservation biology and policy. The chapters focus on cases as varied as vultures, storks, waterbirds, pumas or cougars, and elephants, and research techniques such as genetics and GIS. Technological developments, such as GIS and remote sensing, and some genetic methods have altered the nature of ecological research. These include the utility of GIS, and the related techniques of remote sensing, which allow more precise and accurate measurements and consequently more informed and reliable results. Species distribution modeling enables evaluations of habitat suitability and the impacts of habitat alteration and the requirements for the improvement of animal conservation. Integrated research, including the interfacial studies of social and natural sciences, is increasingly important in ecological research, as disciplinary boundaries break down and hybrid disciplines emerge. Simultaneously, chemical and genetic studies are increasing in importance, with applications in the interfaces of the ecological, social, and medical sciences. The topics covered in this book may contribute to the scientific understanding of different, relevant topics on research methods on ecology and conservation biology. This is especially the case, considering the wide selection of research topics in widely varying contexts. Strands may emerge from these selected topics that may inform further research and development in varied areas. These research findings may be replicable in the different contexts to contribute to the objectives of ecological sustainability. The results and conclusions presented, and the strategies recommended in different chapters will help the policymakers and decision implementers, scientists, resource managers, research scholars, and other stakeholders to attain effective and sustainable animal conservation and habitat
Article
Full-text available
This study focuses on heavy metal contamination in soils due to recreational shooting within the Tonto National Forest, Arizona. The main research questions are: (1) Have some soils within the Tonto National Forest (NF) been contaminated with lead (Pb) due to recreational shooting? (2) How far downslope have the soils been contaminated? Soils in permitted shooting areas were tested for lead (Pb), which show statistically significant differences in mean concentration levels when compared to control sites. The dry weight of mean lead concentrations (5125 mg/kg; p value < 0.005) were 152 times greater than that of the respective uncontaminated control site (33.4 mg/kg). Lead contamination ranged from 25,482 to 7185 mg/kg approximately 9.3 m downslope and gradually decreased from there, but was still contaminated over the entire length of the hillslope. To my knowledge, this is the first known study to examine heavy metal contamination in surficial soils within the Tonto NF due to recreational shooting.
Article
Heavy metals affect male reproductive function by impairing reproductive organs, disturbing reproductive hormone levels or directly affecting sperm quality. However, little attention has been given to the effect of environmental heavy metals on reproductive function in wild male birds. The present study investigated the alterations of reproductive function in male tree sparrows (Passer montanus) exposed to environments contaminated by heavy metals in terms of testis parameters, reproductive hormone levels and sperm movement characteristics. Two plots, Baiyin (BY, mainly polluted by copper, zinc, lead and cadmium) and Liujiaxia (LJX, a relatively unpolluted area) were selected as sampling sites. The results showed that tree sparrows from BY (1) accumulated higher levels of cadmium in the testes, (2) showed lower superoxide dismutase (SOD) activity and malondialdehyde level, with higher total antioxidant capacity and apoptosis level in the testes, (3) showed higher plasma levels of estrogen, follicle stimulating hormone and luteinizing hormone (LH), and (4) had better sperm movement performance. Additionally, we found that testis size, SOD activity in testes and LH levels were decisive factors in sperm movement performance in tree sparrows. Heavy metal concentrations in testes negatively correlated with testis size, SOD activity in testes, and estrogen levels in tree sparrows. The present study indicates that heavy metals accumulating in testes of tree sparrows adversely affected some key indicators of male reproductive function. However, testicular function, reproductive hormone levels and sperm quality showed adaptive responses that tended to partially compensate for the negative effects in the heavy metal polluted area. This study further indicated that the regulation of testicular function and reproductive hormone levels was the main factor for better sperm quality in tree sparrows exposed to environments contaminated by heavy metals.
Preprint
Full-text available
A literature synthesis submitted by undergraduate research students in the Department of Natural Sciences and Mathematics at Dominican University of California. The paper discusses the detrimental effects of known toxins on California Condor focusing on physiological impacts of lead poisoning and legislation to control the use of lead ammunition and discussing the impacts of pesticides on the Condor.
Article
Full-text available
We assessed total mercury (THg) concentrations in breast feathers of diurnal North American raptors collected at migration monitoring stations. For 9 species in the Pacific Flyway, we found species and age influenced feather THg concentrations whereas sex did not. Feather THg concentrations µg/g dry weight (dw) averaged (least squares mean ± standard error) higher for raptors that generally consume > 75% avian prey (sharp-shinned hawk Accipiter striatus: n = 113; 4.35 ± 0.45 µg/g dw, peregrine falcon Falco peregrinus: n = 12; 3.93 ± 1.11 µg/g dw, Cooper’s hawk Accipiter cooperii: n = 20; 2.35 ± 0.50 µg/g dw, and merlin Falco columbarius: n = 59; 1.75 ± 0.28 µg/g dw) than for raptors that generally consume < 75% avian prey (northern harrier Circus hudsonius: n = 112; 0.75 ± 0.10 µg/g dw, red-tailed hawk Buteo jamaicensis: n = 109; 0.56 ± 0.06 µg/g dw, American kestrel Falco sparverius: n = 16; 0.57 ± 0.14 µg/g dw, prairie falcon Falco mexicanus: n = 10; 0.41 ± 0.13 µg/g dw) except for red-shouldered hawks Buteo lineatus: n = 10; 1.94 ± 0.61 µg/g dw. Feather THg concentrations spanning 13-years (2002–2014) in the Pacific Flyway differed among 3 species, where THg increased for juvenile northern harrier, decreased for adult red-tailed hawk, and showed no trend for adult sharp-shinned hawk. Mean feather THg concentrations in juvenile merlin were greater in the Mississippi Flyway (n = 56; 2.14 ± 0.18 µg/g dw) than those in the Pacific Flyway (n = 49; 1.15 ± 0.11 µg/g dw) and Intermountain Flyway (n = 23; 1.14 ± 0.16 µg/g dw), and Atlantic Flyway (n = 38; 1.75 ± 0.19 µg/g dw) averaged greater than the Pacific Flyway. Our results indicate that raptor migration monitoring stations provide a cost-effective sampling opportunity for biomonitoring environmental contaminants within and between distinct migration corridors and across time.
Chapter
Scientific Foundations of Zoos and Aquariums - edited by Allison B. Kaufman January 2019
Article
AIMS: To investigate the prevalence of lead exposure in hens and eggs from backyard poultry in a sample of Auckland households, the relationship between concentrations of lead in the blood of the hens and in the shells and yolks of eggs from the same household, and to examine associations with measures of hen health, environment and husbandry factors. METHODS: Thirty households participated in the study from August to November 2016, each providing one adult hen for sampling, an egg from the household if available, and completing a questionnaire on hen husbandry. Concentrations of lead in blood were determined using a portable lead analyser. Eggs were analysed for concentrations of lead in the yolk and shell using inductively coupled plasma mass spectrometry after biological digestion with a mixture of nitric and hydrochloric acid. RESULTS: Twenty three of 30 hens (77%) showed evidence of lead exposure, with median concentrations of lead in blood of 0.77 (min <0.16, max 8.02) μmol/L. All eggs showed evidence of lead exposure, with concentrations of lead in the yolk ranging from 0.003–1.07 mg/kg, and concentrations of lead in the eggshell ranging from <0.1–0.82 mg/kg. A positive correlation existed between concentrations of lead in the blood of a hen and concentrations of lead in egg yolk from the same hen (R²=0.97), and both the yolk (R²=0.58) and shell (R²=0.30) of an egg from her flock. No association was found between concentrations of lead in blood and hen health indices measured in this study. Concentrations of lead in blood were higher in hens from properties with homes built before 1941 than between 1941–1960 (p = 0.03), and in hens from properties with weatherboard homes than brick homes (p = 0.049). CONCLUSIONS AND CLINICAL RELEVANCE:: There was a high prevalence of lead exposure in this sample of Auckland backyard chickens, with the majority of hens being sub-clinically affected. Associations were found between concentrations of lead in the blood of the hens, and properties with homes built before 1940s and clad in weatherboard. Concentrations of lead in over half the egg yolks sampled were at levels sufficient to warrant human health concern. The assessment of concentrations of lead in backyard poultry and eggs intended for human consumption is recommended to protect human and bird health.
Chapter
Successful conservation usually takes a multidisciplinary approach. In Raptor Conservation in Practice I demonstrate how saving raptor species through techniques like captive breeding and release, and others, is effective only with research to solve conservation problems and measure results, and working to develop sustainable solutions with stakeholders using methods drawn from the disciplines of forensic research and social sciences respectively. I use examples from The Peregrine Fund’s experience over nearly 50 years of putting conservation into practice to develop the idea of the multidisciplinary approach and cite examples of recovery of critically endangered species such as the Peregrine Falcon, California Condor and Ridgway’s Hawk, forensic research to discover a new cause of mortality among vultures in South Asia, and community-based conservation solutions with stakeholders in Madagascar and Panama.
Article
Bald Eagles (Haliaeetus leucocephalus) were rare only a few decades ago but have undergone a spectacular recovery range-wide. While their numbers have increased, there is concern about exposure of Bald Eagles to environmental contaminants. We collected excrement from nesting and wintering Bald Eagles in Iowa to examine their exposure to several contaminants and tested for differences as a function of space, time, and breeding status. We detected aluminum, copper, manganese, and zinc at levels above the quantitation limit (QL) in most excrement samples. These elements are all essential micronutrients normally found in living organisms. Arsenic and selenium are essential micronutrients for which fewer samples had levels above the QL. We also detected non-essential elements barium, cadmium, lead, and mercury in excrement samples, although only one sample had a cadmium level above the QL and only 26% of samples had lead levels above the QL. Geometric mean contaminant levels in excrement samples collected from nesting eagles during the spring were higher than for samples collected in the winter for aluminum, barium, copper, manganese, and zinc. The only difference we detected in contaminant levels in excrement samples was in manganese (higher for nest sites along the Mississippi River) and selenium (lower for nest sites along the Mississippi River) versus nest sites not associated with the Mississippi River. We also found that non-breeding eagles had higher levels of barium and manganese than nesting eagles. Our results can serve as a baseline for comparison with future studies investigating exposure of Bald Eagles to environmental contaminants.
Article
Full-text available
Mourning dove (Zenaida macroura) hunting is becoming increasingly popular, especially in managed shooting fields. Given the possible increase in the availability of lead (Pb) shot on these areas, our objective was to estimate availability and ingestion of spent shot at the Eagle Bluffs Conservation Area (EBCA, hunted with nontoxic shot) and the James A. Reed Memorial Wildlife Area (JARWA, hunted with Pb shot) in Missouri. During 1998, we collected soil samples one or 2 weeks prior to the hunting season (prehunt) and after 4 days of dove hunting (posthunt). We also collected information on number of doves harvested, number of shots fired, shotgun gauge, and shotshell size used. Dove carcasses were collected on both areas during 1998-99. At EBCA, 60 hunters deposited an estimated 64,775 pellets/ha of nontoxic shot on or around the managed field. At JARWA, approximately 1,086,275 pellets/ha of Pb shot were deposited by 728 hunters. Our posthunt estimates of spent-shot availability from soil sampling were 0 pellets/ha for EBCA and 6,342 pellets/ha for JARWA. Our findings suggest that existing soil sampling protocols may not provide accurate estimates of spent-shot availability in managed dove shooting fields. During 1998-99, 15 of 310 (4.8%) mourning doves collected from EBCA had ingested nontoxic shot. Of those doves, 6 (40.0%) contained ≥7 shot pellets. In comparison, only 2 of 574 (0.3%) doves collected from JARWA had ingested Pb shot. Because a greater proportion of doves ingested multiple steel pellets compared to Pb pellets, we suggest that doves feeding in fields hunted with Pb shot may succumb to acute Pb toxicosis and thus become unavailable to harvest, resulting in an underestimate of ingestion rates. Although further research is needed to test this hypothesis, our findings may partially explain why previous studies have shown few doves with ingested Pb shot despite their feeding on areas with high Pb shot availability.
Chapter
Full-text available
ABSTRACT.-The primary goal in the recovery of any formerly extirpated taxa is the establishment of a viable, self-sustaining breeding population. Reintroduced populations of the endangered California Condor (Gymnogyps californianus) began breeding in southern California and northern Arizona in 2001. Here, we studied breeding condors in southern California from 2002-2005 to determine nest success and identify limiting factors for nesting condors. Although hatching success (66.7%) was comparable to the historic wild population of the 1980s, fledging success was extremely low (8.3%). Of 10 chicks hatched in the wild since 2001, only one survived to fledge successfully. All post-hatching mortality since 2002 occurred in the mid to late nestling phase. In two cases, heavy metal toxicosis and complications due to the ingestion of foreign material, principally man-made trash, were the cause of death. All but one chick handled since 2002 held such trash (up to 193.5 g). On average, feeding rates were similar to those at historic nests but were more variable. Most nests had lower feeding rates and more prolonged periods of food deprivation than historical nests. Our data suggest that management, principally provisioning at single sites, has significantly altered foraging behavior with detrimental effects on chick survivorship. Whether trash ingestion is related to calcium or other nutritional requirements needs urgent investigation. As a priority, we recommend determining the timing of bone mineralization, and capacity for pellet formation and regurgitation, of nestlings in captivity. In the wild, we recommend the removal of problem birds, closing or cleaning up trash sites and, most importantly, altering current management to reduce dependence on single provisioning sites to promote the development of more natural foraging patterns. However, this is likely to come at a cost of increased exposure to lead contamination. Removal of the threat of lead poisoning would allow more flexible and scientifically driven management of condor populations.
Chapter
Full-text available
Lead toxicity, perhaps the principal factor in the decline of the recent historic population of California Condors (Gymnogyps californianus) is still prevalent today. Ingestion of this contaminant, principally via bullet fragments and shotgun pellets in hunter-shot carcasses and gut-piles, poses a serious threat to the re-establishment of condor populations. Beginning in 1992, condors were released annually in southern California and lead exposure was assessed by blood sampling and analysis. Our data-set consisted of 214 samples from 44 individual condors, all but four samples of which were collected between 1997 and 2004. Ninety-fi ve samples (44.4%) had blood-lead levels above background (>20 µg dL –1), 18 (8.4%) were clinically affected (60–99 µg dL –1), and 7 (3.3%) were in the acute toxicity range (>100 µg dL –1). Of 44 individual condors, 34 (77.3%) had blood-lead levels above background, 14 (31.8%) were clinically affected and six (13.6%) had levels indicative of acute toxicity at least once during the sampling period. Twenty-three individuals (52.3%) were exposed to lead on multiple (2–7) occasions. Lead levels differed signifi cantly between years and were related to a switch of release and provisioning sites between the Sierra Madre Mountains (1997–2000) and Hopper Mountain National Wildlife Refuge (2001–2004). Lead levels differed signifi cantly between age-classes with exposure being highest among sub-adults (years 4–5). Blood-lead levels were signifi cantly higher during the months of the deer-hunting season (31.8 vs. 22.4 µg dL –1). Since releases began, three documented deaths have resulted from lead toxicity. Eight condors with chronic or acute lead levels have been chelated to prevent mortality and one condor was chelated twice in two consecutive years. Assuming that without treatment some of these would have been mortalities, lead poisoning was the 8 139
Article
Full-text available
The present paper is devoted primarily to the evaluation of losses resulting from lead poisoning in wild waterfowl populations. Two reports have been published which presented preliminary findings on this subject. Efforts to develop a nontoxic shot were treated in a paper dealing with the value of various shot alloys in relation to lead poisoning; additional data on this subject are presented herein. The approach toward evaluating the importance of lead poisoning in wild waterfowl was threefold: (1) appraisal of the incidence and magnitude of waterfowl die-offs resulting from lead poisoning, (2) appraisal of the incidence of ingested lead shot among waterfowl populations in fall and early winter, and (3) appraisal of waterfowl losses resulting from the ingestion of various quantities of lead shot per bird. 38 references, 9 figures, 31 tables.
Article
Full-text available
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.
Article
Full-text available
Mining and smelting at Kellogg-Smelterville, Idaho, resulted in high concentrations of lead in Coeur d'Alene (CDA) River sediments 15–65 km downstream, where ospreys (Pandion haliaetus) nested. Adult and nestling ospreys living along the CDA River had significantly higher blood lead concentrations than those at Lake Coeur d'Alene (intermediate area) or Pend Oreille and Flathead Lakes (reference areas). Lead concentrations in fish collected from the study areas paralleled those found in ospreys. Inhibition of blood -aminolevulinic acid dehydratase (ALAD) activity and elevation of protoporphyrin concentration provided evidence of lead exposure. In adult ospreys, ALAD activity was negatively correlated with lead in blood (r=–0.57), whereas protoporphyrin was positively correlated with lead in blood (r=+0.40). Neither hemoglobin nor hematocrit was adversely affected by the relatively modest lead concentrations found in the blood. Pronounced accumulation of lead by adults or young could ultimately result in behavioral abnormalities or death, both of which would reduce productivity of the nesting osprey population. We did not observe death related to lead, behavioral abnormalities, or reduced productivity during this 1986–87 study. Despite some lead-induced biochemical changes in blood parameters, ospreys produced young at nearly identical rates in the three study areas; these rates were among the highest ever reported in the western United States. Post-fledging survival of ospreys exposed to lead early in life remains an unknown. Lead does not biomagnify in the food chain as do organochlorine pesticides and mercury and several osprey behavior traits reduce the potential for the species to accumulate critical levels of lead. Swans, which feed at a lower trophic level, continue to die from environmental lead in the region.
Article
Full-text available
Poisoning from lead shot in waterbirds has been well documented globally and, in some countries, legislation exists to combat lead toxicosis at wetlands and/or in waterbirds. However, poisoning of terrestrial species such as raptors and upland game birds, while of potential conservation concern, remains largely to be addressed. For several species, shot are not the only ammunition source of lead, as bullet fragments can be ingested from hunter-killed animal carcasses and gut piles left in the field. This review collates the current knowledge of lead poisoning from ammunition in non-waterbirds. Fifty-nine terrestrial bird species have so far been documented to have ingested lead or suffered lead poisoning from ammunition sources, including nine Globally Threatened or Near Threatened species. We discuss the conservation significance of continued lead use, and detail measures needed to combat lead poisoning.
Article
Full-text available
This paper reports the results of postmortem examinations of four swans from Barney Lake that were suspected of dying of lead poisoning.
Article
Full-text available
Lead-induced mortality appears to have been a major factor in the decline of the California condor (Gymnogyps californianus). We orally dosed turkey vultures (Cathartes aura) with BB-sized lead shot from January 1988 through July 1988 to determine physiologic response (delta-aminolevulinic acid dehydratase inhibition, erythrocyte protoporphyrin levels, anemia), diagnostic tissue lead concentrations (blood, liver, and kidney), and comparative sensitivity of this species. Two turkey vultures died and two became so intoxicated they were euthanized. Overall, responses of measured parameters were comparable to other species exposed to lead although there was considerable individual variation. Survival time (143-211 days), even with the large numbers of shot and constant redosing, was much longer than reported for other species of birds, suggesting considerable tolerance by turkey vultures to the deleterious effects of lead ingestion. Based on these observations, turkey vultures appear to be poor models for assessing the risk of lead poisoning to California condors or predicting their physiologic response.
Article
Full-text available
Despite dramatic declines in children's blood lead concentrations and a lowering of the Centers for Disease Control and Prevention's level of concern to 10 microg per deciliter (0.483 micromol per liter), little is known about children's neurobehavioral functioning at lead concentrations below this level. We measured blood lead concentrations in 172 children at 6, 12, 18, 24, 36, 48, and 60 months of age and administered the Stanford-Binet Intelligence Scale at the ages of 3 and 5 years. The relation between IQ and blood lead concentration was estimated with the use of linear and nonlinear mixed models, with adjustment for maternal IQ, quality of the home environment, and other potential confounders. The blood lead concentration was inversely and significantly associated with IQ. In the linear model, each increase of 10 microg per deciliter in the lifetime average blood lead concentration was associated with a 4.6-point decrease in IQ (P=0.004), whereas for the subsample of 101 children whose maximal lead concentrations remained below 10 microg per deciliter, the change in IQ associated with a given change in lead concentration was greater. When estimated in a nonlinear model with the full sample, IQ declined by 7.4 points as lifetime average blood lead concentrations increased from 1 to 10 microg per deciliter. Blood lead concentrations, even those below 10 microg per deciliter, are inversely associated with children's IQ scores at three and five years of age, and associated declines in IQ are greater at these concentrations than at higher concentrations. These findings suggest that more U.S. children may be adversely affected by environmental lead than previously estimated.
Article
Full-text available
Analyses completed on samples collected between 1993 and 1996 showed that about 7% of 475 Inuit newborns from northern Quebec (Canada) had a cord blood lead concentration equal to or greater than 0.48 micromol/l, an intervention level adopted by many governmental agencies. A comparison between the cord blood lead isotope ratios of Inuit and southern Quebec newborns showed that lead sources for these populations were different. Our investigation suggests that lead shots used for game hunting were an important source of lead exposure in the Inuit population. A cohort study conducted in three Inuit communities shows a significant decrease of cord blood lead concentrations after a public health intervention to reduce the use of lead shot. Lead shot ammunition can be a major and preventable source of human exposure to lead.
Article
Full-text available
The blood lead of 23 griffon vultures (Gyps fulvus) trapped in 2003 was analyzed in order to evaluate exposure to lead in the vulture population of Cazorla Natural Park (in southern Spain). In 2001 the use of leaded gasoline in vehicles was banned in the European Union; however, lead ammunition is still used in Spain in big-game hunting for red deer, fallow deer, mouflon, and wild boar, which are ingested by vultures from September to March. The mean concentration of lead in blood was 43.07 +/- 31.96 microg/dL with a range of 17.39-144.80 microg/dL. Only two vultures had lead levels below 20 microg/dL, and two others had blood lead concentrations close to 150 microg/dL. In view of the results, we think the population of vultures from Cazorla Natural Park is suffering subclinical exposure to lead, with some individuals exposed to high toxicity risk. We concluded that ingestion of lead in the metallic form alone is sufficient to produce these blood lead concentrations, and we recommend the prohibition of lead ammunition for big-game hunting in order to preserve the vulture population.
Article
Full-text available
The endangered California Condor (Gymnogyps californianus) was reduced to a total population of 22 birds by the end of 1982. Their captive-bred descendants are now being released back into the wild in California, Arizona, and Baja California, where monitoring indicates they may accumulate lead to toxic levels. Fragments of ammunition in the carcasses of game animals such as deer, elk, and feral pigs not retrieved by hunters or in gut piles left in the field have been considered a plausible source of the lead, though little direct evidence is available to support this hypothesis. Here, we measured lead concentrations and isotope ratios in blood from 18 condors living in the wild in central California, in 8 pre-release birds, and in diet and ammunition samples to determine the importance of ammunition as a source of exposure. Blood lead levels in pre-release condors were low (average 27.7 ng/mL, SD 4.9 ng/ mL) and isotopically similar to dietary and background environmental lead in California. In contrast, blood lead levels in free-flying condors were substantially higher (average 246 ng/mL, SD 229 ng/mL) with lead isotopic compositions that approached or matched those of the lead ammunition. A two-endmember mixing model defined by the background 207Pb/206Pb ratio of representative condor diet samples (0.8346) and the upper 207Pb/206Pb ratio of the ammunition samples (0.8184) was able to account for the blood lead isotopic compositions in 20 out of the 26 live condors sampled in this study (i.e., 77%). Finally, lead in tissues and in a serially sampled growing feather recovered postmortem from a lead-poisoned condor in Arizona evidence acute exposure from an isotopically distinct lead source. Together, these data indicate that incidental ingestion of ammunition in carcasses of animals killed by hunters is the principal source of elevated lead exposure that threatens the recovery in the wild of this endangered species.
Article
Blood lead levels in children have declined, and the level of concern specified by the Centers for Disease Control and Prevention now is 10 μg/dL. It is not clear, however, whether cognitive deficits consequent to lead exposure are a problem at blood lead levels less than 10 μg/dL. This study estimated blood lead concentrations in 172 children at ages 6, 12, 18, 24, 36, 48, and 60 months. At ages 3 and 5 years, the children were tested with the Stanford-Binet Intelligence Scale, an instrument that evaluates vocabulary, spatial pattern analysis, quantitative ability, and memory. Intelligence quotient (IQ) was related to blood lead levels after adjusting for maternal IQ, quality of the home environment, and other potentially confounding factors. Mean blood lead levels were lowest at age 6 months (3.4 μg/dL) and maximal at age 2 years (9.7 μg/dL). By age 5, the mean level was 6 μg/dL. The lifetime average blood lead level was 7.7 μg/dL at age 3 years and 7.4 μg/dL at age 5. The proportions of children with peak lead levels below 10 μg/dL were 57.0% and 55.8% at ages 3 and 5 years, respectively. At both these ages, the mean IQ (composite score) was approximately 90. After adjusting for numerous covariates, IQ correlated inversely and significantly with blood lead concentration. An increase in the lifetime average blood lead level of 1 μg/dL correlated with a change in IQ of -0.46. The estimated overall difference in IQ for each 1-μg/dL increase in lifetime average lead level was -1.37 points. Other significant predictors of IQ included maternal IQ, material income, and the child's birth weight. These findings suggest that substantially more children in the United States undergo adverse cognitive change from environmental exposure to lead than was previously thought. Primary prevention is essential in view of the lack of effective treatment for children with moderate blood lead elevations.
Article
On Easter Sunday of 1987, the last California Condor (Gymnogyps californianus) known to exist in the wild was trapped for captive breeding, joining 26 others of his species at the San Diego and Los Angeles Zoos. A young male adult, he was a bird whose life had been followed closely for a number of years. His movements and interactions with other condors, his molting patterns and changes in coloration with age, as well as his pairing with an old female in late 1985, and his first breeding attempts in 1986 had all been documented in considerable detail. Like every other bird in the remnant population, he was known and had been studied as an individual. With his capture, an era of intensive investigations of condor natural history and ecology had come to a close.
Article
A 16-yr (1980-95) retrospective study was conducted to assess differences in the prevalence of lead poisoning in Bald (Haliaeetus leucocephalus) and Golden (Aquila chrysaetos) Eagles admitted to The Raptor Center at the University of Minnesota. These years encompass the period before and after federal legislation was enacted restricting the use of lead shot for hunting waterfowl on federal lands (1991). Of 654 eagle admissions reviewed, 138 cases of lead-poisoned eagles were evaluated for the following: recovery location, blood lead concentration, month of admission, radiographic evidence of lead in the ventriculus and primary cause of admission. The prevalence of lead poisoning in eagles did not change after 1991, but mean blood concentrations of lead in the same population decreased. These findings call into question current theories regarding the sources of lead for eagles and the actual mechanisms by which eagles are poisoned. Lead poisoning is a continuing problem both regionally and internationally, and many variables related to this toxicity have yet to be conclusively defined.
Article
The prevalence of lead in Golden Eagles (Aquila chrysaetos) occurring within the recent historical range of the California Condor (Gymnogyps californianus) was determined by analyzing blood samples from 162 Golden Eagles captured between June 1985 and December 1986 at three sites. We found no significant differences between sex and age classes in blood lead levels nor were there differences between residents and migrants. Significant differences were found between months with the highest blood lead levels occurring during the fall/winter period. Approximately one-third (35.8%) of the Golden Eagle population sampled had elevated blood lead levels, values similar to those reported for free-flying California Condors. Given this rate of exposure, if the proposed releases of California Condors back to the wild are to succeed, whether in their former range or elsewhere, any potential for lead poisoning must be reduced. It is essential that we identify the sources of the lead, the seasonal and geographic distribution of these sources, and develop management strategies to reduce or eliminate the hazard.
Article
Five wild California condors (Gymnogyps californianus) that died in 1980-86 were necropsied and tissues were analyzed for environmental contaminants. Three died of lead (Pb) poisoning, 1 presumably of cyanide (CN) poisoning, and 1 nestling of handling shock. Organochlorine concentrations were low in 4 condors that were analyzed for these contaminants. Blood samples from 14 wild and 14 captive condors were analyzed primarily for Pb. Five of 14 wild condors sampled had elevated (>0.70 ppm) concentrations of Pb in blood whereas Pb concentrations in all captive condors were low. Lead levels in individual birds often fluctuated over time. Lead exposure, especially poisoning, was a major factor affecting the wild California condor population during 1982-86. The probable source of Pb was bullet fragments in carrion on which condors were feeding.
Article
Home range and survival were determined for cottontail rabbits (Sylvilagus floridanus) living in woodlots in southwestern Wisconsin. Home ranges were determined for 25 radio-tagged cottontail rabbits in a 14-acre (5.7-ha) woodlot where fall densities were 3.6 rabbits per acre (0.4 ha). Home range size varied by season, sex, and individual. Adult male home ranges increased from a mean of 6.8 acres (2.8 ha) in spring to a mean of 9.9 acres (4.0 ha) in early summer, then decreased significantly to a mean of 3.8 acres (1.5 ha) in late summer. This decrease coincided with testes regression. Adult female home ranges were largest (mean = 4.3 acres [1.7 ha]) in spring, then decreased significantly to a mean of 2.1 acres (0.8 ha) in early summer and remained about this size until mid-January. Female home ranges did not overlap in late summer. Between mid-September and mid-November the home ranges of four juveniles did not differ in size from 10 adults which showed no difference according to sex. Retreats (holes, woodpiles, junkpiles) were used as daytime resting locations mostly during periods of snow cover. Less than 8 percent of daytime resting locations occurred in agricultural land. Bimonthly survival rates determined radiotelemetrically for 51 cottontails were 0.77, 0.79, 0.94, 0.80, 0.68, and 0.63 for 2-month periods beginning in March, May, July, September, November, and January, respectively. Annual survival calculated from the bimonthly rates was 0.20; mean annual survival determined demographically was 0.15. Cottontail survival appeared to be related to exposure in insecure cover.
Article
Ecological and toxicological aspects of lead (Pb) in the environment are briefly reviewed, with emphasis on fish and wildlife, their predators, and prey. Subtopics include sources and uses, chemical properties, mode of action, background concentrations, lethal and sublethal effects, and current recommendations for the protection of sensitive living resources. Resources that are at increased risk from Pb include migratory waterfowl that congregate at heavily hunted staging areas and ingest shot, avian predators that consume hunter-wounded game, domestic livestock near smelters and Pb battery recycling plants, zoo animals and livestock held in enclosures coated with Pb-based paints, wildlife that forage near heavily traveled roads, and aquatic life near mining activities.
Article
Although lead uptake by plants takes place, it is limited by the low availability of lead from soils. Plants do not appear to be as effected by lead as by other metals, e.g., zinc, copper. Detrimental effects seem to appear only at total concentrations of several hundred mg Pb/kg of soil. An important concern from a health point of view is the lead levels in the edible parts of the plants. It seems, however, that the edible parts of plants do not have the tendency to concentrate lead with the exception of some leafy vegetables, such as lettuce. In some cases the parts of vegetables not used for human consumption are used for livestock feeding, and because of this, the lead levels in these parts are also important.
Article
There is increasing concern that birds in terrestrial ecosystems may be exposed to spent lead shot. Evidence exists that upland birds, particularly mourning doves (Zenaida macroura), ingest spent lead shot and that raptors ingest lead shot by consuming wounded game. Mortality, neurological dysfunction, immune suppression, and reproductive impairment are documented effects of exposure to lead in birds. An ecological risk assessment on the impact of lead shot exposure in upland birds was conducted and is presented in the context of the new United States Environmental Protection Agency's Ecological Risk Assessment Paradigm. A considerable amount of spent lead shot is released into the environment each year from shooting and hunting. Doves collected from fields that are cultivated to attract mourning doves for hunting activities show evidence of ingestion of spent lead shot. Because lead can cause both acute and chronic toxicity if ingested by birds, and because there is evidence of widespread deposition of lead shot in terrestrial ecosystems, concern for impacts on upland game birds and raptors seems warranted. Although this ecological risk assessment does not clearly define a significant risk of lead shot exposure to upland game birds, this issue merits continued scrutiny to protect our upland game bird and raptor resources.
Article
The remnant wild population of California Condors (Gymnogyps californianus) of the 1980s exhibited a rapid population decline caused by high mortality rates among adult and immature birds. The most prominent mortality factor was lead poisoning resulting from ingestion of bullet fragments in carcasses. Successful captive breeding has allowed many birds to be released to the wild since 1992, based originally on an assumption that exposure to lead could be prevented by food subsidy. The mortality of released birds, however, has generally exceeded levels needed for population stability calculated from simple population models. Collision with overhead wires was the most frequent cause of death in releases before 1994. Lead poisoning again surfaced as a problem starting in 1997 as older birds began feeding on carcasses outside the subsidy program. Although poisonings have been treated successfully by chelation therapy in recaptured birds, food subsidy is proving an ineffective solution to lead exposure. The best long-term solution appears to be either the creation of large reserves where hunting is prohibited or the restriction of hunting to nontoxic ammunition in release areas. Until sources of lead contamination are effectively countered, releases cannot be expected to result in viable populations. In addition, problems involving human-oriented behavior have resulted in the permanent removal of many released birds from the wild. The most promising reduction in human-oriented behavior has been achieved in one release of aversively conditioned, parent-reared birds. Rigorous evaluation of the factors reducing attraction to humans and human structures has been hampered by confounding of techniques in releases. Behavioral problems could be more quickly overcome by adoption of a comprehensive experimental approach.
Article
Previous research has suggested that free-ranging mourning doves (Zenaida macroura) may ingest spent lead pellets, succumb to lead toxicosis, and die in a relatively short time (i.e., an acute lead toxicosis hypothesis). We tested this hypothesis by administering 157 captive mourning doves 2–24 lead pellets, monitoring pellet retention and short-term survival, and measuring related physiological characteristics. During the 19- to 21-day posttreatment period, 104 doves that received lead pellets died (deceased doves) and 53 survived (survivors); all 22 birds in a control group survived. Within 24-hr of treatment, blood lead levels increased almost twice as fast for deceased doves compared to survivors (F1,208 = 55.49; P < 0.001). During the first week, heterophil:lymphocyte (H:L) ratios increased twice as fast for deceased doves than with survivors (F1,198 = 23.14, P , 0.001). Posttreatment survival differed (X2 = 37.4, P < 0.001) among the 5 groups of doves that retained different numbers of pellets, and survival ranged from 0.57 (95% CI: 0.44–0.74) for doves that retained �2 lead pellets 2 days posttreatment compared to 0.08 (95% CI: 0.022–0.31) for those doves that retained 13–19 lead pellets on 2 days posttreatment; significant differences existed among the 5 groups. After controlling for dove pretreatment body mass, each additional lead pellet increased the hazard of death by 18.0% (95% CI: 1.132–1.230, P < 0.001) and 25.7% (95% CI: 1.175–1.345, P < 0.001) for males and females, respectively. For each 1-g increase in pretreatment body mass, the hazard of death decreased 2.5% (P ¼ 0.04) for males and 3.8% (P ¼ 0.02) for females. Deceased doves had the highest lead levels in liver (49.20 6 3.23 ppm) and kidney (258.16 6 21.85 ppm) tissues, whereas controls showed the lowest levels (liver, 0.08 ppm; kidney, 0.17 ppm). For doves dosed with pellets, we observed simultaneous increases in blood lead levels and H:L ratios, whereas packed-cell volume (PCV) values declined. Our results support an acute lead toxicosis hypothesis. Although further research is necessary to investigate the magnitude of lead shot ingestion and toxicosis in mourning doves, we recommend that management agencies initiate development of a long-term strategic plan aimed at implementing a nontoxic shot regulation for mourning dove hunting. (JOURNAL OF WILDLIFE MANAGEMENT 70(2):413–421; 2006)
Article
The authors conducted a survey during 1992 to evaluate blood levels of lead and mercury in Inuit adults of Nunavik (Arctic Quebec, Canada). Blood samples obtained from 492 participants (209 males and 283 females; mean age = 35 yr) were analyzed for lead and total mercury; mean (geometric) concentrations were 0.42 micromol/l (range = 0.04-2.28 micromol/l) and 79.6 nmol/l (range = 4-560 nmol/l), respectively. Concentrations of omega-3 fatty acid in plasma phospholipids--a biomarker of marine food consumption--were correlated with mercury (r = .56, p < .001) and, to a lesser extent, with blood lead levels (r = .31, p < .001). Analyses of variance further revealed that smoking, age, and consumption of waterfowl were associated with lead concentrations (r2 = .30, p < .001), whereas age and consumption of seal and beluga whale were related to total mercury levels (r2 = .30, p < .001). A significant proportion of reproductive-age women had lead and mercury concentrations that exceeded those that have been reportedly associated with subtle neurodevelopmental deficits in other populations.
Article
Elevated lead in the tissues of raptors, especially those that scavenge, is a common occurrence, and lead poisoning appears to be a significant problem in the ongoing recovery effort for California condors (Gymnogyps californianus). Elevated blood lead levels have been found in released birds, and a number of birds have died of lead poisoning. In earlier work, we dosed turkey vultures (Cathartes aura) with lead shot but found them to be a poor model for lead poisoning. In this study, we dosed four Andean condors (Vultur gryphus) with lead shot and found them to be quite sensitive, as two of the birds died and the other two exhibit signs of lead poisoning within 50 days. All lead-responsive parameters were affected, and regurgitation of dosed shot occurred only once. The response of the Andean condors appeared to mimic California condors, suggesting that once exposed to lead, the possibility of survival is poor. This is consistent with observations in the wild, where otherwise healthy birds exposed to metallic lead quickly succumb. At the very least, the release program has to maintain constant surveillance and an active lead monitoring program.
Article
To provide proper medical evaluation and care for the endangered California condor (Gymnogyps californianus), veterinarians need accurate hematologic and biochemical reference ranges. A retrospective study of blood samples from captive California condors housed at the San Diego Wild Animal Park assessed the samples by sex and age of condor to determine serum biochemical and hematologic reference ranges, including lead and zinc levels. Condors were grouped by age as follows: group 1 included birds less than 30 days of age; group 2 included birds between 30 days and 6 mo of age; group 3 included birds between 6 mo and 5 yr of age; group 4 included all birds greater than 5 yr of age. Significant differences between sexes included higher chloride, cholesterol, and total plasma protein concentration in males as compared to females (P < 0.05). Significant differences between age groups were identified in glucose, potassium, phosphorus, calcium, albumin, total plasma protein, globulin, cholesterol, bile acid, and zinc concentrations, as well as aspartate aminotransferase, alkaline phosphatase, lactate dehydrogenase, and creatine phosphokinase activities (P < 0.05). Additionally, significant differences between age groups were noted in white blood cell count, hematocrit, heterophils, lymphocytes, and eosinophils (P < 0.05). A steady increase in glucose and a decrease in alkaline phosphatase and lactate dehydrogenase activities, as well as cholesterol, bile acid, calcium, and phosphorus concentrations, were correlated with age (P < 0.05). Following application of statistical analysis, condors less than 6 mo of age were identified as unique compared to older cohorts; therefore, two reference ranges are proposed by calculating a 90% confidence interval. Reference ranges obtained from other published avian data, including those for psittaciformes, ratites, galliformes, anseriformes, and raptors, were similar to condors in this study.
Review of the second five years of the California condor reintroduction program in the Southwest. U.S. Fish and Wildlife Service, Arizona Ecological Services Office Lead poisoning as a mortality factor in waterfowl populations
  • W Literature Cited Austin
  • K Day
  • S Franklin
  • J Humphrey
  • W G Hunt
  • C Parish
  • R Sieg
  • K Sullivan
LITERATURE CITED Austin, W., K. Day, S. Franklin, J. Humphrey, W. G. Hunt, C. Parish, R. Sieg, and K. Sullivan. 2007. Review of the second five years of the California condor reintroduction program in the Southwest. U.S. Fish and Wildlife Service, Arizona Ecological Services Office, Phoenix, USA. Bellrose, F. C. 1959. Lead poisoning as a mortality factor in waterfowl populations. Illinois Natural History Survey Bulletin 27:235–288.
Before the Fish and Game Commission State of California. Supple-mental information regarding the urgent need for action by the commission Governor's response to request for immediate action
  • D Glenden
  • A Pierto
Center for Biological Diversity, Natural Resources Defense Council, Wishtoyo Foundation, Public Employees for Environmental Responsi-bility, Ventana Wilderness Alliance, D. Glenden, and A. Pierto. 2005. Before the Fish and Game Commission State of California. Supple-mental information regarding the urgent need for action by the commission.,http://www.biologicaldiversity.org/swcbd/species/condor/ Supplement.pdf.. Accessed 15 Oct 2006. Center for Biological Diversity. 2006. Governor's response to request for immediate action.,www.biologicaldiversity.org/swcbd/species/condor/ DFG-Governor-response.pdf.. Accessed 15 Oct 2006.
California condor (Gymnogyps californianus) Account 610 in The birds of North America. The Birds of North America Biology and conservation of the California condor
  • Nuttall Club
  • American Ornithologists
  • Union
  • Cambridge
  • Usa Massachusetts
  • N F R Snyder
  • J Schmitt
  • N F R Snyder
  • H A Snyder
Nuttall Ornithological Club and American Ornithologists' Union, Cambridge, Massachusetts, USA. Snyder, N. F. R., and J. Schmitt. 2002. California condor (Gymnogyps californianus). In A. Poole and F. Gill, editors. Account 610 in The birds of North America. The Birds of North America, Inc., Philadelphia, Pennsylvania, USA. Snyder, N. F. R., and H. A. Snyder. 1989. Biology and conservation of the California condor. Current Ornithology 6:175–267.
Assessment of lead contamination sources exposing California condors. Final Report. California Department of Fish and Game, Habitat Conservation Planning Branch High levels of blood lead in griffon vultures (Gyps fulvus) from Cazorla Natural Park (southern Spain)
  • D M Fry
  • Usa
  • A J Garcia-Fernandez
  • E Martinez-Lopez
  • D Romero
  • P Maria-Mojica
  • A Godino
  • P Jimenez
Fry, D. M. 2003. Assessment of lead contamination sources exposing California condors. Final Report. California Department of Fish and Game, Habitat Conservation Planning Branch, Sacramento, USA. Garcia-Fernandez, A. J., E. Martinez-Lopez, D. Romero, P. Maria-Mojica, A. Godino, and P. Jimenez. 2005. High levels of blood lead in griffon vultures (Gyps fulvus) from Cazorla Natural Park (southern Spain). Environmental Toxicology 20:459–463.
Status of the California condor and mortality factors affecting recovery
  • K. J. Sorenson
  • L. Burnett
  • J. R. Davis
Sorenson, K. J., L. Burnett, and J. R. Davis. 2001. Status of the California condor and mortality factors affecting recovery. Endangered Species Update 18:120–123.
Lead poisoning of waterfowl and raptors. Pages 108–117 in
  • L N Locke
  • N J Thomas
Locke, L. N., and N. J. Thomas. 1996. Lead poisoning of waterfowl and raptors. Pages 108–117 in A. Fairbrother, L. N. Locke, and G. L. Huff, editors. Noninfectious diseases of wildlife. Second edition. Iowa State University Press, Ames, USA.
Report to the California Fish and Game Commission on condor mortality issues, actions, and recommen-dations. U.S. Fish and Wildlife Service and California Department of Fish and Game Limiting factors for wild California condors
  • J M Scott
  • R M Jurek
Scott, J. M., and R. M. Jurek. 1985. Report to the California Fish and Game Commission on condor mortality issues, actions, and recommen-dations. U.S. Fish and Wildlife Service and California Department of Fish and Game, Sacramento, USA. Snyder, N. 2007. Limiting factors for wild California condors. Pages 9–34 in A. Mee and L. S. Hall, editors. California condors in the 21st century. Series in Ornithology no.
Reintroduction of California condors into their historic range: the recovery program in California. Pages 123–138 in
  • J Grantham
Grantham, J. 2007. Reintroduction of California condors into their historic range: the recovery program in California. Pages 123–138 in A. Mee and L. S. Hall, editors. California condors in the 21st century. Series in Ornithology no.
The California condor: a saga of natural history and conservation
  • N. F. R. Snyder
  • H. Snyder
Snyder, N. F. R., and H. Snyder. 2000. The California condor: a saga of natural history and conservation. Academic Press, San Diego, California, USA.