Endangered California Condor Research Articles

Bone lead measurements of live condors in field to assess cumulative lead exposure.

Lead poisoning remains the leading cause of diagnosed death for critically endangered California condors, which are annually monitored for lead exposure via blood tests. Blood tests are generally reflective of acute lead exposure. Since condors are victims to both chronic and acute lead exposure, measuring bone, which in humans is reflective of years to decades worth of exposure, is a valuable biomarker. In this study, we measured bone Pb of the tibiotarsus of 64 condors in vivo using a portable x-ray fluorescence device. The average uncertainty for measurements, typically reflective of how effective the device performed, was found to be 3.8 ± 2.2µg/g bone mineral. The average bone lead level was found to be 26.7 ± 24.5µg/g bone mineral. Bone lead correlated significantly with a sum of all blood lead measures over the lifetime of each condor. In the future, bone lead can potentially be used to inform treatment planning and address the chronic health implications of lead in the species.

Bird Flu Shots: The U.S. is vaccinating endangered California Condors for avian flu.

Bird Flu Shots: The U.S. is vaccinating endangered California Condors for avian flu.

Lead, trash, DDE, and young age of breeders linked to lower fertility in the first two decades of reintroduction for critically endangered California Condors in California

Abstract 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 from 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 toward 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.

Policy comparison of lead hunting ammunition bans and voluntary nonlead programs for California condors

AbstractThe endangered California condor (Gymnogyps californianus) is negatively affected by lead poisoning from spent lead‐based hunting ammunition. Because lead poisoning is the primary mortality factor affecting condors, the California Fish and Game Commission banned lead hunting ammunition during 2008 in the southern California condor range followed by a statewide ban implemented in 2019. In contrast, the Arizona Game and Fish Department instituted an outreach and awareness program encouraging voluntary use of nonlead hunting ammunition in the northern portion of the state during 2005 and a similar program was launched in Utah during 2012. The juxtaposition of policy tools provided a unique opportunity to evaluate the intended efforts to mitigate lead exposure in condors and their respective positive and negative effects. Herein we reflect upon the effectiveness of lead policy actions in the 3‐state region on the basis of condor blood‐lead levels, population status, and hunter awareness of the issue and use of nonlead hunting ammunition.

Supervised versus unsupervised approaches to classification of accelerometry data.

Sophisticated animal-borne sensor systems are increasingly providing novel insight into how animals behave and move. Despite their widespread use in ecology, the diversity and expanding quality and quantity of data they produce have created a need for robust analytical methods for biological interpretation. Machine learning tools are often used to meet this need. However, their relative effectiveness is not well known and, in the case of unsupervised tools, given that they do not use validation data, their accuracy can be difficult to assess. We evaluated the effectiveness of supervised (n = 6), semi-supervised (n = 1), and unsupervised (n = 2) approaches to analyzing accelerometry data collected from critically endangered California condors (Gymnogyps californianus). Unsupervised K-means and EM (expectation-maximization) clustering approaches performed poorly, with adequate classification accuracies of <0.8 but very low values for kappa statistics (range: -0.02 to 0.06). The semi-supervised nearest mean classifier was moderately effective at classification, with an overall classification accuracy of 0.61 but effective classification only of two of the four behavioral classes. Supervised random forest (RF) and k-nearest neighbor (kNN) machine learning models were most effective at classification across all behavior types, with overall accuracies >0.81. Kappa statistics were also highest for RF and kNN, in most cases substantially greater than for other modeling approaches. Unsupervised modeling, which is commonly used for the classification of a priori-defined behaviors in telemetry data, can provide useful information but likely is instead better suited to post hoc definition of generalized behavioral states. This work also shows the potential for substantial variation in classification accuracy among different machine learning approaches and among different metrics of accuracy. As such, when analyzing biotelemetry data, best practices appear to call for the evaluation of several machine learning techniques and several measures of accuracy for each dataset under consideration.

Assessing Marine Endocrine-Disrupting Chemicals in the Critically Endangered California Condor: Implications for Reintroduction to Coastal Environments.

Coastal reintroduction sites for California condors (Gymnogyps californianus) can lead to elevated halogenated organic compound (HOC) exposure and potential health impacts due to the consumption of scavenged marine mammals. Using nontargeted analysis based on comprehensive two-dimensional gas chromatography coupled to time-of-flight mass spectrometry (GC×GC/TOF-MS), we compared HOC profiles of plasma from inland and coastal scavenging California condors from the state of California (CA), and marine mammal blubber from CA and the Gulf of California off Baja California (BC), Mexico. We detected more HOCs in coastal condors (32 ± 5, mean number of HOCs ± SD, n = 7) than in inland condors (8 ± 1, n = 10) and in CA marine mammals (136 ± 87, n = 25) than in BC marine mammals (55 ± 46, n = 8). ∑DDT-related compounds, ∑PCBs, and total tris(chlorophenyl)methane (∑TCPM) were, respectively, ∼7, ∼3.5, and ∼148 times more abundant in CA than in BC marine mammals. The endocrine-disrupting potential of selected polychlorinated biphenyls (PCB) congeners, TCPM, and TCPMOH was determined by in vitro California condor estrogen receptor (ER) activation. The higher levels of HOCs in coastal condors compared to those in inland condors and lower levels of HOC contamination in Baja California marine mammals compared to those from the state of California are factors to consider in condor reintroduction efforts.

Facultative Parthenogenesis in California Condors.

Parthenogenesis is a relatively rare event in birds, documented in unfertilized eggs from columbid, galliform, and passerine females with no access to males. In the critically endangered California condor, parentage analysis conducted utilizing polymorphic microsatellite loci has identified two instances of parthenogenetic development from the eggs of two females in the captive breeding program, each continuously housed with a reproductively capable male with whom they had produced offspring. Paternal genetic contribution to the two chicks was excluded. Both parthenotes possessed the expected male ZZ sex chromosomes and were homozygous for all evaluated markers inherited from their dams. These findings represent the first molecular marker-based identification of facultative parthenogenesis in an avian species, notably of females in regular contact with fertile males, and add to the phylogenetic breadth of vertebrate taxa documented to have reproduced via asexual reproduction.

Arts of Living on a Damaged Planet: Ghosts and Monsters of the AnthropoceneAfter Extinction

Arts of Living on a Damaged Planet: Ghosts and Monsters of the AnthropoceneAfter Extinction

Correcting parentage relationships in the endangered California Condor: Improving mean kinship estimates for conservation management

Abstract Maintaining the existing biodiversity of endangered species is a goal of conservation management programs, and a major component of many collaborative efforts undertaken by zoos, field biologists, and conservation scientists. Over the past 3 decades, the San Diego Zoo has performed long-term genetic studies in support of the recovery program for the critically endangered California Condor (Gymnogyps californianus). This work has included sex determination of hatchlings and parentage confirmation using microsatellite genotyping. This paper describes the genetic work associated with the California Condor recovery program, which aims to provide a highly accurate pedigree for making informed captive pairing and release recommendations. Initial genotyping began after reintroduced California Condors started reproducing, and the focus was on birds hatched from their wild-laid eggs. However, genetic analysis showed discrepancies relative to behavioral observations of wild birds and led to the species-wide testing of all available samples. This genetic study has resolved instances of individual misidentifications and parental misassignments, verified the first cases of extra-pair paternity in this species, identified parentage where chicks were observed being raised by trios, and found 2 apparent de novo mutations in the captive condor population. Correcting the California Condor pedigree according to genetic parental analysis has produced more accurate estimates of mean kinship values among living birds, ranking potential breeders according to their actual breeding value and helping managers to make informed decisions about captive pairing and release of condors in the wild.

The endangered California Condor (Gymnogyps californianus) population is exposed to local haemosporidian parasites

The endangered California Condor (Gymnogyps californianus) is the largest New World Vulture in North America. Despite recovery program success in saving the species from extinction, condors remain compromised by lead poisoning and limited genetic diversity. The latter makes this species especially vulnerable to infectious diseases. Thus, taking advantage of the program of blood lead testing in Arizona, condor blood samples from 2008 to 2018 were screened for haemosporidian parasites using a nested polymerase chain reaction (PCR) protocol that targets the parasite mitochondrial cytochrome b gene. Plasmodium homopolare (Family Plasmodiidae, Order Haemosporida, Phylum Apicomplexa), was detected in condors captured in 2014 and 2017. This is the first report of a haemosporidian species infecting California Condors, and the first evidence of P. homopolare circulating in the Condor population from Arizona. Although no evidence of pathogenicity of P. homopolare in Condors was found, this study showed that the California Condors from Arizona are exposed to haemosporidian parasites that likely are spilling over from other local bird species. Thus, active surveillance should be an essential part of conservation efforts to mitigate the impact of infectious diseases, an increasingly recognized cause of global wildlife extinctions worldwide, particularly in avian populations considered vulnerable or endangered.

Mercury and lead exposure in avian scavengers from the Pacific Northwest suggest risks to California condors: Implications for reintroduction and recovery

Mercury (Hg) and lead (Pb) are widespread contaminants that pose risks to avian scavengers. In fact, Pb exposure is the primary factor limiting population recovery in the endangered California condor (Gymnogyps californianus) and Hg can impair avian reproduction at environmentally relevant exposures. The Pacific Northwest region of the US was historically part of the condor's native range, and efforts are underway to expand recovery into this area. To identify potential threats to reintroduced condors we assessed foraging habitats, Hg and Pb exposure, and physiological responses in two surrogate avian scavenger species (common ravens [Corvus corax] and turkey vultures [Cathartes aura] across the region between 2012 and 2016. Mercury exposure near the Pacific coast was 17–27-fold higher than in inland areas, and stable carbon and sulfur isotopes ratios indicated that coastal scavengers were highly reliant on marine prey. In contrast, Pb concentrations were uniformly elevated across the region, with 18% of the birds exposed to subclinical poisoning levels. Elevated Pb concentrations were associated with lower delta-aminolevulinic acid dehydratase (δ-ALAD) activity, and in ravens there was an interactive effect between Hg and Pb on fecal corticosterone concentrations. This interaction indicated that the effects of Hg and Pb exposure on the stress axis are bidirectional, and depend on the magnitude of simultaneous exposure to the other contaminant. Our results suggest that condors released to the Pacific Northwest may be exposed to both elevated Hg and Pb, posing challenges to management of future condor populations in the Pacific Northwest. Developing a robust monitoring program for reintroduced condors and surrogate scavengers will help both better understand the drivers of exposure and predict the likelihood of impaired health. These findings provide a strong foundation for such an effort, providing resource managers with valuable information to help mitigate potential risks.

Flight response to spatial and temporal correlates informs risk from wind turbines to the California Condor

ABSTRACT Wind power is a fast-growing energy resource, but wind turbines can kill volant wildlife, and the flight behavior of obligate soaring birds can place them at risk of collision with these structures. We analyzed altitudinal data from GPS telemetry of critically endangered California Condors (Gymnogyps californianus) to assess the circumstances under which their flight behavior may place them at risk from collision with wind turbines. Condor flight behavior was strongly influenced by topography and land cover, and birds flew at lower altitudes and closer to the rotor-swept zone of wind turbines when over ridgelines and steep slopes and over forested and grassland cover types. Condor flight behavior was temporally predictable, and birds flew lower and closer to the rotor-swept zone during early morning and evening hours and during the winter months, when thermal updrafts were weakest. Although condors only occasionally flew at altitudes that placed them in the rotor-swept zone of turbines, they regu...

Meteorological and environmental variables affect flight behaviour and decision‐making of an obligate soaring bird, the California Condor Gymnogyps californianus

The movements of animals are limited by evolutionary constraints and ecological processes and are strongly influenced by the medium through which they travel. For flying animals, variation in atmospheric conditions is critically influential in movement. Obligate soaring birds depend on external sources of updraft more than do other flying species, as without that updraft they are unable to sustain flight for extended periods. These species are therefore good models for understanding how the environment can influence decisions about movement. We used meteorological and topographic variables to understand the environmental influences on the decision to engage in flight by obligate soaring and critically endangered California Condors Gymnogyps californianus. Condors were more likely to fly, soared at higher altitudes and flew over smoother terrain when weather conditions promoted either thermal or orographic updrafts, for example when turbulence and solar radiation were higher and when winds from the east and north were stronger. However, increased atmospheric stability, which is inconsistent with thermal development but may be associated with orographic updrafts, was correlated with a somewhat higher probability of being in flight at lower altitudes and over rougher terrain. The close and previously undescribed linkages between Condor flight and conditions that support development of thermal and orographic updrafts provide important insight into the behaviour of obligate soaring birds and into the environmental parameters that may define the currently expanding distribution of Condors within and outside the state of California.

Feasibility of a portable X-ray fluorescence device for bone lead measurements of condor bones

Lead based ammunition is a primary source of lead exposure, especially for scavenging wildlife. Lead poisoning remains the leading cause of diagnosed death for the critically endangered California condors, which are annually monitored via blood tests for lead exposure. The results of these tests are helpful in determining recent exposure in condors and in defining the potential for exposure to other species including humans. Since condors are victim to acute and chronic lead exposure, being able to measure both would lend valuable information on the rates of exposure and accumulation through time. A commercial portable X-ray fluorescence (XRF) device has been optimized to measure bone lead in vivo in humans, but this device could also be valuable for field measurements of bone lead in avian species. In this study, we performed measurements of bone Pb in excised, bare condor bones using inductively coupled plasma mass spectrometry (ICP-MS), a cadmium 109 (Cd-109) K-shell X-ray fluorescence (KXRF) system, and a portable XRF system. Both KXRF and portable XRF bone Pb measurement techniques demonstrated good correlations with ICP-MS results (r=0.93 and r=0.92 respectively), even with increasing skin thickness (r=0.86 between ICP-MS and portable XRF at 1.54mm of soft tissue). In conclusion, our results suggest that a portable XRF could be a useful option for measurement of bone Pb in avian species in the field.

Terrestrial Scavenging of Marine Mammals: Cross-Ecosystem Contaminant Transfer and Potential Risks to Endangered California Condors (Gymnogyps californianus).

The critically endangered California condor (Gymnogyps californianus) has relied intermittently on dead-stranded marine mammals since the Pleistocene, and this food source is considered important for their current recovery. However, contemporary marine mammals contain persistent organic pollutants that could threaten condor health. We used stable carbon and nitrogen isotope, contaminant, and behavioral data in coastal versus noncoastal condors to quantify contaminant transfer from marine mammals and created simulation models to predict the risk of reproductive impairment for condors from exposure to DDE (p,p'-DDE), a major metabolite of the chlorinated pesticide DDT. Coastal condors had higher whole blood isotope values and mean concentrations of contaminants associated with marine mammals, including mercury (whole blood), sum chlorinated pesticides (comprised of ∼95% DDE) (plasma), sum polychlorinated biphenyls (PCBs) (plasma), and sum polybrominated diphenyl ethers (PBDEs) (plasma), 12-100-fold greater than those of noncoastal condors. The mean plasma DDE concentration for coastal condors was 500 ± 670 (standard deviation) (n = 22) versus 24 ± 24 (standard deviation) (n = 8) ng/g of wet weight for noncoastal condors, and simulations predicted ∼40% of breeding-age coastal condors have DDE levels associated with eggshell thinning in other avian species. Our analyses demonstrate potentially harmful levels of marine contaminant transfer to California condors, which could hinder the recovery of this terrestrial species.

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 18months, 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.

Ancient DNA reveals substantial genetic diversity in the California Condor (Gymnogyps californianus) prior to a population bottleneck

ABSTRACT Critically endangered species that have undergone severe population bottlenecks often have little remaining genetic variation, making it difficult to reconstruct population histories to apply in reintroduction and recovery strategies. By using ancient DNA techniques, it is possible to combine genetic evidence from the historical population with contemporary samples to provide a more complete picture of a species' genetic variation across its historical range and through time. Applying this approach, we examined changes in the mitochondrial DNA (mtDNA) control region (526 base pairs) of the endangered California Condor (Gymnogyps californianus). Results showed a >80% reduction in unique haplotypes over the past 2 centuries. We found no spatial sorting of haplotypes in the historical population; the periphery of the range contained haplotypes that were common throughout the historical range. Direct examination of mtDNA from California Condor museum specimens provided a new window into historical po...

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.

Lead Exposure Risk from Trash Ingestion by the Endangered California Condor (Gymnogyps californianus).

Lead poisoning from ingestion of spent lead ammunition is one of the greatest threats to the recovery of California Condors (Gymnogyps californianus) in the wild. Trash ingestion by condors is well documented, yet the extent that trash presents a lead exposure risk is unknown. We evaluated 1,413 trash items collected from condor nest areas and nestlings in the Transverse Range of Ventura County, California, US, from 2002 to 2008, for their potential as a lead exposure risk to condors. We visually identified 71 items suspected to contain sufficient lead to be of toxicologic concern. These items were leached with weak acid and analyzed for lead. Twenty-seven of the 71 leached items (~2% of the 1,413 items) were "lead containing" based on criteria of a leachate lead concentration >1 μg/mL, with the majority of these items (22; 81% of the 27 lead items) being ammunition related (e.g., spent bullet casings and jacketed bullets). Only three of the 1,413 items collected were lead containing but were clearly not ammunition related; the other two lead-containing items were unidentified. Our results suggest that trash ingestion of nonammunition items does not pose a significant lead exposure risk to the California Condor population in California.

Two decades of cumulative impacts to survivorship of endangered California condors in California

We investigated threats to the California condor (Gymnogyps californianus), a flagship endangered species, using individual data on survival during a 20year period of intensive recovery efforts. Over the two decades of reintroductions, condors in California had an estimated median survival time of 7.8years suggesting that 50% of condors are expected to survive in the wild long enough to contribute to recruitment. In general, annual mortality rates exceeded levels necessary for a stable population; however, mortality declined, reaching levels needed for population stability, during the second decade of re-establishment. Intensive management practices, including utility pole aversion training and clinical interventions to prevent lead-related deaths likely contributed to the decrease in mortality rates. Utility line collision and/or electrocution was an important factor causing mortality over the two decades; though, this threat has largely been mitigated through management and targeted efforts in high-risk areas. In the past, wildfires were not considered a major threat to survival of free-flying condors. However, our analyses suggest that forest fires are significantly linked to the hazard of death, and increased wildfire activity in California highlights this population's vulnerability to catastrophic losses from forest fire. Lead poisoning, which was a major driver in the population's decline, was a leading cause of death accounting for the greatest adult mortality, and lead exposure remains the most significant threat. Recent lead ammunition reduction efforts in the condor range in California hold promise for improving the recovery potential for this population.