Impact of the California lead ammunition ban on reducing lead exposure in golden eagles and turkey vultures

Predatory and scavenging birds may be exposed to high levels of lead when they ingest shot or bullet fragments embedded in the tissues of animals injured or killed with lead ammunition. Lead poisoning was a contributing factor in the decline of the endangered California condor population in the 1980s, and remains one of the primary factors threatening species recovery. In response to this threat, a ban on the use of lead ammunition for most hunting activities in the range of the condor in California was implemented in 2008. Monitoring of lead exposure in predatory and scavenging birds is essential for assessing the effectiveness of the lead ammunition ban in reducing lead exposure in these species. In this study, we assessed the effectiveness of the regulation in decreasing blood lead concentration in two avian sentinels, golden eagles and turkey vultures, within the condor range in California. We compared blood lead concentration in golden eagles and turkey vultures prior to the lead ammunition ban and one year following implementation of the ban. Lead exposure in both golden eagles and turkey vultures declined significantly post-ban. Our findings provide evidence that hunter compliance with lead ammunition regulations was sufficient to reduce lead exposure in predatory and scavenging birds at our study sites.     

Exposure of California Condors to Lead From Spent Ammunition

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.     

Seroepidemiologic Survey of Potential Pathogens in Obligate and Facultative Scavenging Avian Species in California

Throughout the world, populations of scavenger birds are declining rapidly with some populations already on the brink of extinction. Much of the current research into the factors contributing to these declines has focused on exposure to drug residues, lead, and other toxins. Despite increased monitoring of these declining populations, little is known about infectious diseases affecting scavenger bird species. To assess potential infectious disease risks to both obligate and facultative scavenger bird species, we performed a serosurvey for eleven potential pathogens in three species of scavenging birds in California: the California condor (Gymnogyps californianus), turkey vulture (Cathartes aura) and golden eagle (Aquila chrysaetos). California condors were seropositive for avian adenovirus, infectious bronchitis virus, Mycoplasma gallisepticum, avian paramyxovirus-2, West Nile virus (WNV) and Toxoplasma gondii. Golden eagles were seropositive for avian adenovirus, Chlamydophila psittaci and Toxoplasma gondii, and turkey vultures were seropositive for avian adenovirus, Chlamydophila psittaci, avian paramyxovirus-1, Toxoplasma gondii and WNV. Risk factor analyses indicated that rearing site and original release location were significantly associated with a positive serologic titer to WNV among free-flying condors. This study provides preliminary baseline data on infectious disease exposure in these populations for aiding in early disease detection and provides potentially critical information for conservation of the endangered California condor as it continues to expand its range and encounter new infectious disease threats.     

Effects of Lead Exposure,Flock Behavior,and Management Actions on the Survival of California Condors (<Emphasis Type="Italic">Gymnogyps californianus</Emphasis>)

Translocation is an increasingly important tool for managing endangered species, but factors influencing the survival of translocated individuals are not well understood. Here we examine intrinsic and extrinsic drivers of survival for critically endangered California condors (Gymnogyps californianus) whose wild population recovery is reliant upon releases of captively bred stock. We used known fate models and information-theoretic methods to compare the ability of hypothesized covariates, most of which serve as proxies for lead exposure risk, to predict survival rates of condors in California. Our best supported model included the following predictors of survival: age of the recovery program, precipitation, proportion of days observed feeding on proffered carcasses, maximum blood lead concentration over the preceding 18 months, and time since release. We found that as flocks have increased in size and age, condors are increasingly likely to range more widely and less likely to be observed feeding on proffered food, and these “wilder” behaviors were associated with lower survival. After accounting for these behaviors, we found a positive survival trend, which we attribute to ongoing improvements in management. Our findings illustrate that the survival of translocated animals, such as highly social California condors, is influenced by behaviors that change through time.     

Effectiveness of Action to Reduce Exposure of Free-Ranging California Condors in Arizona and Utah to Lead from Spent Ammunition

California condors (Gymnogyps californianus) released into the wild in Arizona ranged widely in Arizona and Utah. Previous studies have shown that the blood lead concentrations of many of the birds rise because of ingestion of spent lead ammunition. Condors were routinely recaptured and treated to reduce their lead levels as necessary but, even so, several died from lead poisoning. We used tracking data from VHF and satellite tags, together with the results of routine testing of blood lead concentrations, to estimate daily changes in blood lead level in relation to the location of each bird. The mean daily increment in blood lead concentration depended upon both the location of the bird and the time of year. Birds that spent time during the deer hunting season in two areas in which deer were shot with lead ammunition (Kaibab Plateau (Arizona) and Zion (Utah)) were especially likely to have high blood lead levels. The influence upon blood lead level of presence in a particular area declined with time elapsed since the bird was last there. We estimated the daily blood lead level for each bird and its influence upon daily mortality rate from lead poisoning. Condors with high blood lead over a protracted period were much more likely to die than birds with low blood lead or short-term elevation. We simulated the effect of ending the existing lead exposure reduction measures at Kaibab Plateau, which encourage the voluntary use of non-lead ammunition and removal of gut piles of deer and elk killed using lead ammunition. The estimated mortality rate due to lead in the absence of this program was sufficiently high that the condor population would be expected to decline rapidly. The extension of the existing lead reduction program to cover Zion (Utah), as well as the Kaibab plateau, would be expected to reduce mortality caused by lead substantially and allow the condor population to increase.     

Breeding condors in captivity for release into the wild

Recognizing the decline of the South American Condor in some parts of its range and the highly endangered status of the California condor, the New York Zoological Society developed a captive-breeding program for South American condors. This program was designed to produce techniques applicable to hand-rearing of either species of condor. Once condors were successfully reared in captivity, it became imperative to develop techniques to ensure that captive-reared condor chicks could be released into the wild, could survive there, and could interact naturally with other wild condors. Captive-bred hand-reared condor chicks were taken to Northwestern Peru and successfully released into the wild.     

Effects of Lead Exposure,Flock Behavior,and Management Actions on the Survival of California Condors (Gymnogyps californianus)

Translocation is an increasingly important tool for managing endangered species, but factors influencing the survival of translocated individuals are not well understood. Here we examine intrinsic and extrinsic drivers of survival for critically endangered California condors (Gymnogyps californianus) whose wild population recovery is reliant upon releases of captively bred stock. We used known fate models and information-theoretic methods to compare the ability of hypothesized covariates, most of which serve as proxies for lead exposure risk, to predict survival rates of condors in California. Our best supported model included the following predictors of survival: age of the recovery program, precipitation, proportion of days observed feeding on proffered carcasses, maximum blood lead concentration over the preceding 18 months, and time since release. We found that as flocks have increased in size and age, condors are increasingly likely to range more widely and less likely to be observed feeding on proffered food, and these “wilder” behaviors were associated with lower survival. After accounting for these behaviors, we found a positive survival trend, which we attribute to ongoing improvements in management. Our findings illustrate that the survival of translocated animals, such as highly social California condors, is influenced by behaviors that change through time.

     

Andean and California condors possess dissimilar genetic composition but exhibit similar demographic histories

While genetic diversity of threatened species is a major concern of conservation biologists, historic patterns of genetic variation are often unknown. A powerful approach to assess patterns and processes of genetic erosion is via ancient DNA techniques. Herein, we analyzed mtDNA from historical samples (1800s to present) of Andean Condors (Vultur gryphus) to investigate whether contemporary low genetic variability is the result of recent human expansion and persecution, and compared this genetic history to that of California condors (Gymnogyps californianus).We then explored historic demographies for both species via coalescent simulations. We found that Andean condors have lost at least 17% of their genetic variation in the early 20th century. Unlike California condors, however, low mtDNA diversity in the Andean condor was mostly ancient, before European arrival. However, we found that both condor species shared similar demographies in that population bottlenecks were recent and co‐occurred with the introduction of livestock to the Americas and the global collapse of marine mammals. Given the combined information on genetic and demographic processes, we suggest that the protection of key habitats should be targeted for conserving extant genetic diversity and facilitate the natural recolonization of lost territories, while nuclear genomic data should be used to inform translocation plans.     

Experimental lead poisoning in turkey vultures (Cathartes aura)

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.     

Need and Seek for Dietary Micronutrients: Endogenous Regulation,External Signalling and Food Sources of Carotenoids in New World Vultures

Among birds, vultures show low concentrations of plasma carotenoids due to the combination of their large size, general dull colouration and a diet based on carrion. We recorded the concentration of each carotenoid type present in plasma of the Andean condor (Vultur gryphus) according to age and sex, that determine colour signalling and dominance hierarchies in the carcasses. We compared the carotenoid profile in wild condors with that of captive condors fed with a controlled diet of flesh to test the hypothesis that wild individuals could acquire extra carotenoids from vegetal matter contained in carcass viscera and fresh vegetation. Wild American black vultures (Coragyps atratus) were also sampled to evaluate the potential influence of colouration in the integument on absorption and accumulation patterns of plasma carotenoids. A remarkably higher concentration of lutein than β-carotene was found in wild condors, while the contrary pattern was recorded in American black vultures and captive condors. We found a consistent decrease in all plasma carotenoids with age, and a lower concentration of most xanthophylls in male compared to female wild condors. Positive correlations of all carotenoids indicated general common absorption and accumulation strategies or a single dietary source containing all pigments found in plasma. The comparatively low total concentration of carotenoids, and especially of lutein rather than β-carotene, found in captive condors fed with a diet restricted to flesh supports the hypothesis that Andean condors can efficiently acquire carotenoids from vegetal matter in the wild. Andean condors seem to be physiologically more competent in the uptake or accumulation of xanthophylls than American black vultures, which agrees with the use of colour-signalling strategies in sexual and competitive contexts in the Andean condor. This study suggests that vultures may use dietary vegetal supplements that provide pigments and micronutrients that are scarce or missing in carrion.     

Spatial and temporal patterns in the diet of the Andean condor: ecological replacement of native fauna by exotic species

The development of conservation strategies to protect viable populations of scavenging birds requires the existence of adequate and safe food supplies in the wild. Early reports on Andean condors Vultur gryphus diet recorded guanacos and rheas, the dominant herbivores since the Pleistocene, as their main food in Patagonia. However, in the past century, guanaco and rhea populations have notably decreased as a consequence of introduced livestock, and other exotic mammals have colonized the region. We study the spatial and temporal variation of the condors' diet to determine which species are being consumed by condors, and to test whether native herbivores still have a role as a food source. We analysed 371 pellets (517 prey items), collected along 500 km in northwestern Patagonia, Argentina. Our study shows that the Andean condor depends heavily (98.5%) on exotic herbivores. Their diet was made up of c . 51% sheep/goat, 24% hare/rabbit, 17% red deer and 6% cow/horse, with only 2% other mammal species. Samples from locations surveyed after 12–15 years showed a diet shift coincident with the local tendencies in the food source. The diet composition of condors using roosts within the same zone was very similar, which suggests that they may be feeding from the same area. Thus, unhealthy carcasses could impact the entire local populations. Our results show the abundance of the invasive species in northwestern Patagonia and support the idea that native mega-herbivores are ecologically extinct in this area. Exotic species management can have a decisive impact on scavenger's survival. It is necessary to apply a strategy that includes public environmental education about the problems of scavengers (e.g. use of poison, veterinary medicines and lead bullets), and a serious productive plan, including native species as a suitable source of economic development.     

The link between feeding ecology and lead poisoning in white-tailed eagles

Lead poisoning affects numerous threatened raptors and is a major cause of death in white-tailed eagles (Haliaeetus albicilla). A major reason for intoxication is assumed to be lead fragments ingested while feeding on game animals killed by lead-based projectiles. However, empirical evidence on the relevance of carrion in raptor diets remains scarce. We therefore investigated the link between raptor feeding ecology and lead poisoning, with white-tailed eagles as a model species for scavenging birds. We collected data on seasonal diet composition and food availability of 7 territorial white-tailed eagle pairs in northeastern Germany. We also analyzed stomach contents (SCs) of 126 eagles found dead from 1996 to 2008 throughout Germany. Multiple regression models revealed that fish were the primary prey for eagles, and waterfowl and carcasses of game mammals comprised a large portion of alternative diet components. Eagles used individual foraging tactics, adjusted to local food supply, to maximize profitability. They showed a type II functional response to fish availability. When fish availability sharply declined, eagles switched to waterfowl and carrion. The consumption of game mammal carrion increased over autumn and winter and was positively correlated with a concomitant seasonal increase in the incidence of lead poisoning in eagles throughout Germany. The stomachs of lead-poisoned eagles predominantly contained game ungulate remains. These results indicate that carcasses of game mammals were the major sources of lead fragments. The link between raptor feeding ecology and lead poisoning is the specific functional response of raptors to changing food availability or poor habitat quality, leading to scavenging on lead-contaminated carrion. This shows that carrion constitutes a considerable threat to white-tailed eagles and other birds with similar feeding habits as long as it contains lead bullet fragments. Conservation management of scavenging birds would be substantially improved if carrion was free of lead bullet fragments. One method to achieve this is the widespread introduction of lead-free ammunition. © 2012 The Wildlife Society.     

Lead exposure in free-flying turkey vultures is associated with big game hunting in California

Predatory and scavenging birds are at risk of lead exposure when they feed on animals injured or killed by lead ammunition. While lead ammunition has been banned from waterfowl hunting in North America for almost two decades, lead ammunition is still widely used for hunting big game and small game animals. In this study, we evaluated the association between big game hunting and blood lead concentration in an avian scavenger species that feeds regularly on large mammals in California. We compared blood lead concentration in turkey vultures within and outside of the deer hunting season, and in areas with varying wild pig hunting intensity. Lead exposure in turkey vultures was significantly higher during the deer hunting season compared to the off-season, and blood lead concentration was positively correlated with increasing wild pig hunting intensity. Our results link lead exposure in turkey vultures to deer and wild pig hunting activity at these study sites, and we provide evidence that spent lead ammunition in carrion poses a significant risk of lead exposure to scavengers.     

Nuisance Ecology: Do Scavenging Condors Exact Foraging Costs on Pumas in Patagonia?

Predation risk describes the energetic cost an animal suffers when making a trade off between maximizing energy intake and minimizing threats to its survival. We tested whether Andean condors (Vultur gryphus) influenced the foraging behaviors of a top predator in Patagonia, the puma (Puma concolor), in ways comparable to direct risks of predation for prey to address three questions: 1) Do condors exact a foraging cost on pumas?; 2) If so, do pumas exhibit behaviors indicative of these risks?; and 3) Do pumas display predictable behaviors associated with prey species foraging in risky environments? Using GPS location data, we located 433 kill sites of 9 pumas and quantified their kill rates. Based upon time pumas spent at a carcass, we quantified handling time. Pumas abandoned >10% of edible meat at 133 of 266 large carcasses after a single night, and did so most often in open grasslands where their carcasses were easily detected by condors. Our data suggested that condors exacted foraging costs on pumas by significantly decreasing puma handling times at carcasses, and that pumas increased their kill rates by 50% relative to those reported for North America to compensate for these losses. Finally, we determined that the relative risks of detection and associated harassment by condors, rather than prey densities, explained puma “giving up times” (GUTs) across structurally variable risk classes in the study area, and that, like many prey species, pumas disproportionately hunted in high-risk, high-resource reward areas.     

Lead Bullet Fragments in Venison from Rifle-Killed Deer: Potential for Human Dietary Exposure

Human consumers of wildlife killed with lead ammunition may be exposed to health risks associated with lead ingestion. This hypothesis is based on published studies showing elevated blood lead concentrations in subsistence hunter populations, retention of ammunition residues in the tissues of hunter-killed animals, and systemic, cognitive, and behavioral disorders associated with human lead body burdens once considered safe. Our objective was to determine the incidence and bioavailability of lead bullet fragments in hunter-killed venison, a widely-eaten food among hunters and their families. We radiographed 30 eviscerated carcasses of White-tailed Deer (Odocoileus virginianus) shot by hunters with standard lead-core, copper-jacketed bullets under normal hunting conditions. All carcasses showed metal fragments (geometric mean = 136 fragments, range = 15–409) and widespread fragment dispersion. We took each carcass to a separate meat processor and fluoroscopically scanned the resulting meat packages; fluoroscopy revealed metal fragments in the ground meat packages of 24 (80%) of the 30 deer; 32% of 234 ground meat packages contained at least one fragment. Fragments were identified as lead by ICP in 93% of 27 samples. Isotope ratios of lead in meat matched the ratios of bullets, and differed from background lead in bone. We fed fragment-containing venison to four pigs to test bioavailability; four controls received venison without fragments from the same deer. Mean blood lead concentrations in pigs peaked at 2.29 µg/dL (maximum 3.8 µg/dL) 2 days following ingestion of fragment-containing venison, significantly higher than the 0.63 µg/dL averaged by controls. We conclude that people risk exposure to bioavailable lead from bullet fragments when they eat venison from deer killed with standard lead-based rifle bullets and processed under normal procedures. At risk in the U.S. are some ten million hunters, their families, and low-income beneficiaries of venison donations.     

Lead poisoning in captive Andean condors (Vultur gryphus)

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.     

Recovery rates of bottlenose dolphin (Tursiops truncatus) carcasses estimated from stranding and survival rate data

Recovery of cetacean carcasses provides data on levels of human‐caused mortality, but represents only a minimum count of impacts. Counts of stranded carcasses are negatively biased by factors that include at‐sea scavenging, sinking, drift away from land, stranding in locations where detection is unlikely, and natural removal from beaches due to wave and tidal action prior to detection. We estimate the fraction of carcasses recovered for a population of coastal bottlenose dolphins (Tursiops truncatus), using abundance and survival rate data to estimate annual deaths in the population. Observed stranding numbers are compared to expected deaths to estimate the fraction of carcasses recovered. For the California coastal population of bottlenose dolphins, we estimate the fraction of carcasses recovered to be 0.25 (95% CI = 0.20–0.33). During a 12 yr period, 327 animals (95% CI = 253–413) were expected to have died and been available for recovery, but only 83 carcasses attributed to this population were documented. Given the coastal habits of California coastal bottlenose dolphins, it is likely that carcass recovery rates of this population greatly exceed recovery rates of more pelagic dolphin species in the region.     

Biography of a "Feathered Pig": The California Condor Conservation Controversy

In the early 20th century, after hundreds of years of gradual decline, the California condor emerged as an object of intensive scientific study, an important conservation target, and a cultural icon of the American wilderness preservation movement. Early condor researchers generally believed that the species' survival depended upon the preservation of its wilderness habitat. However, beginning in the 1970s, a new generation of scientists argued that no amount of wilderness could prevent the condor's decline and that only intensive scientific management - including captive breeding - could save the species from certain extinction. A bitter and highly politicized battle soon developed over how to best preserve the condor. For 5years the condor was extinct in the wild; however, by the time that officials released the first captive-bred birds the condor recovery program had garnered widespread public support, even among its former critics. Today, condor advocates from the scientific and activist communities work together to manage the species and protect its habitat. The condor's story illustrates some of the tensions, problems, and successes that have accompanied the rise of conservation biology as a scientific field and environmental movement in the United States.     

The effects of rearing method on social behaviors of mentored,captive‐reared juvenile California condors

Puppet‐reared and parent‐reared captive‐bred California condor (Gymnogyps californianus) juveniles were studied before their release into the wild. Behavioral data were collected during social interactions within two cohorts of juveniles (N = 11) and their adult mentors (N = 5). The purposes of this study were to (1) document the social behaviors of mentored juvenile California condors, and (2) compare social behaviors for two different rearing methods (puppet‐reared versus parent‐reared) during two phases of the mentoring process (San Diego Wild Animal Park versus release sites). Of the 17 behaviors examined by 2 × 2 analyses of variance (ANOVAs), two significant interactions between the rearing method and mentoring phase were found: pulls feathers and feeds alone. For both behaviors, parent‐reared condors engaged in these activities more often at the zoo and less often at the release pens than did the puppet‐reared condors. The main effect of rearing was also significant for two behaviors: near others, and receives contact aggression from other. Parent‐reared birds were more likely to be near another bird and receive contact aggression, regardless of mentoring phase, than puppet‐reared birds. The effect size for 16 of the 17 behaviors was greater for the rearing method than for mentoring phase. Rearing method differences may persist long‐term, as parent‐reared adult mentors were significantly more aggressive than puppet‐reared adult mentors. Dominance relations were examined for both cohorts, with the first cohort exhibiting a strong linear relationship (h′ = 0.86, P = 0.018), whereas the second cohort exhibited a moderate but non‐significant linear hierarchy (h′ = 0.63, P = 0.21). The rearing method had no effect on dominance among the juveniles, but adults were probably dominant to juveniles (P = 0.052; the difference was nearly significant). Although social behaviors between the two rearing groups were similar in most respects, this study is the first to document measurable differences between puppet‐ and parent‐reared captive‐bred California condor juveniles. Zoo Biol 27:1–18, 2008. © 2007 Wiley‐Liss, Inc.