A fundamental challenge in conservation is assessing the efficacy of recovery actions to optimize endangered species management. Considerable recent attention has focused on effective measures to counter the endangerment of avian scavengers, which have declined worldwide, primarily due to poisoning. One iconic example is efforts to recover the critically endangered California condor (Gymnogyps californianus), whose leading cause of death is poisoning from ingesting lead-based ammunition in carcasses. Despite enormous resources expended in California, USA, including implementation of public outreach campaigns and two legislative bans on lead ammunition, lead-related mortality of condors has increased. Here we show that two types of behavioral shifts explain the observed increases in condor lead exposure: wilder foraging and ranging by condors and increased shooting of wild pigs (Sus scrofa) by humans. After accounting for these trends, we show that both lead ammunition bans and public outreach efforts have significantly reduced condor blood lead levels in California, lowering mortality. Our analyses uncover a dynamic in which changing ecological conditions mask the true efficacy of legislation and outreach. Given rapid global change, such dynamics are likely operating in many settings, underscoring the importance of comprehensive evaluations of recovery actions, which can be obscured by shifting behaviors and threats.

Procellariiform seabirds are known to have high rates of plastic ingestion. We investigated the bioaccessibility of plastic-associated chemicals [plastic additives and sorbed persistent organic pollutants (POPs)] leached from plastic over time using an in vitro Procellariiform gastric model. High-density polyethylene (HDPE) and polyvinyl chloride (PVC), commonly ingested by Procellariiform seabirds, were manufactured with one additive [decabrominated diphenyl ether (PBDE-209) or bisphenol S (BPS)]. HDPE and PVC added with PBDE-209 were additionally incubated in salt water with 2,4,4'-trichloro-1,1'-biphenyl (PCB-28) and 2,2',3,4,4',5'-hexachlorobiphenyl (PCB-138) to simulate sorption of POPs on plastic in the marine environment. Our results indicate that the type of plastic (nature of polymer and additive), presence of food (i.e., lipids and proteins) and gastric secretions (i.e., pepsin) influence the leaching of chemicals in a seabird. In addition, 100% of the sorbed POPs were leached from the plastic within 100 hours, while only 2-5% of the additives were leached from the matrix within 100 hours, suggesting that the remaining 95% of the additives could continue to be leached. Overall, our study illustrates how plastic type, diet and plastic retention time can influence a Procellariform's exposure risk to plastic-associated chemicals.

California condors (Gymnogyps californianus) are a conservation-reliant species, needing ongoing management to prevent extinction in the wild. The free-flying California population depends on captive releases to achieve population growth, and lead poisoning from ingestion of spent lead ammunition is their primary threat. We used a population viability management approach to assess status and compare management actions to increase population growth and achieve self-sustainability. Specifically, we investigated how to optimize captive-breeding resources by comparing: the replacement of failed wild-laid eggs with captive-laid eggs vs. releases of captivebred juveniles, releases of captive-bred juveniles in concentrated vs. dispersed timeframes, and releases of captive-bred juveniles vs. reductions in lead-related mortality. Releasing captive-bred juveniles bolstered the growth rate more than replacing eggs, and dispersed releases outperformed concentrated releases when population growth rates were lower, such as in current conditions. Importantly, even small, durable reductions in lead mortality outpaced annual releases, and the relative benefit of such reductions increased as the population grew. Further underscoring the importance of reducing adult mortality, we estimated that 2-3 captive-bred juveniles are needed to offset the loss of one free-flying adult. To assess population status and gauge recovery success, we recommend 3-4 years of time-averaged monitoring data. Finally, our analyses showed that recovery will require robustly growing populations to withstand catastrophic events. Overall, we illustrate the key role the captivebreeding program plays in the growth of the free-flying condor population in California and that a selfsustaining population is achievable through reductions in lead-related mortality.

Abstract Lead (Pb) poisoning is a significant threat to Aotearoa New Zealand's endangered kea (Nestor notabilis), an avian species important to Māori. Historically, exposure was thought to be from lead‐containing building materials; however, recent field observations suggest lead‐based ammunition as an additional source. We used stable lead isotopes to investigate the sources of lead to kea. Comparing 207 Pb/206 Pb ratios in kea blood (n = 91) to both ammunition and building materials, we found approximately one‐third of exposed kea (blood lead > 10 µg/dL) had lead isotope ratios consistent with exposure to lead‐based ammunition. As lead ammunition is still used, including in government‐sponsored culling programs, our data indicate an urgent need to shift toward non‐lead ammunition use to prevent further poisoning and aid conservation efforts. Collaborating with tangata whenua/Māori guardians, we advocate for immediate policy changes to eliminate lead‐based ammunition in kea habitat to safeguard this endangered culturally treasured species from extinction.

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. Lay Summary & BULL; In the first comprehensive assessment of reproduction in California Condors (Gymnogyps californianus) recovering from complete extirpation in the wild, we analyzed 20 years (1999-2018) of data from flocks in southern and central California. & BULL; At the inception of the recovery program, reintroduced flocks of this critically endangered species consisted of young captive-bred individuals without breeding experience. & BULL; We found that California Condor reproductive rates generally increased with age and time spent in the wild. Condors also faced anthropogenic threats that reduced reproductive rates. Hatch success was lower for coastal females, presumably due to DDE exposure from feeding on marine mammals, and fledge success was lower before nests were managed for trash. & BULL; Overall reproductive success should increase over time as the age of California Condors increases if current and emerging threats to reproduction, including the loss of breeders due to lead poisoning, can be addressed.

Microplastic (particle size <5 mm) is considered an emerging threat to the marine environment, yet data are limited for coastal ecosystems. To provide information related to microplastic in a coastal system, we used alkaline tissue digestion and Raman spectroscopy to quantify the prevalence and composition (e.g. fiber, fragment, foam, etc.) of anthropogenic microparticles in the digestive tracts of northern anchovies (Engraulis mordax, anchovy, n = 24), and common murres (Uria aalge, murre, n = 19) from the Monterey Bay, California USA. We also determined microplastic prevalence and composition in seawater (n = 12 17-h sampling periods representing ∼46,000 L sampled) from two Monterey Bay intake systems (Moss Landing, CA and Santa Cruz, CA USA). Microparticles recovered from murre digestive tracts were assessed for estrogenic activity using an in-vitro estrogen receptor activation assay. Suspected anthropogenic microparticles based on visual characteristics were recovered from all sample types with ∼2 particles per 1000 L from the seawater sampling periods, 58% prevalence in anchovies, and 100% prevalence in murres. Across samples of seawater, anchovies, and murres, the most abundant microparticle type found were fibers (78%), followed by fragments (13%), foam (6%), film (2%), and beads (1%). Raman spectroscopy identified 57% of microparticles (excluding dye-prominent and unknown) as plastic (synthetic, semi-synthetic, or blends). Almost one quarter (23%) of the murre digestive tracts contained microparticles that exhibited estrogenic activity. Our study describes the widespread occurrence, composition, and potential estrogenic activity of microplastic in the Monterey Bay and provides important information to aid in the understanding of microplastic contamination in coastal systems.

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.

Lead exposure is a concern in urban ecosystems, with physiological and behavioral effects well documented in humans. Wildlife inhabiting urban ecosystems are also exposed to lead, yet little work has documented the sublethal effects of lead exposure in urban wildlife. We studied northern mockingbirds (Mimus polyglottos) in three neighborhoods of New Orleans, Louisiana, two with high soil lead and one with low soil lead, to better understand how lead exposure may influence mockingbirds' reproductive biology. We monitored nesting attempts, measured lead concentrations in blood and feathers of nestling mockingbirds, documented egg hatching and nesting success, and assessed rates of sexual promiscuity in relation to neighborhood soil lead levels. We found that nestling mockingbirds' blood and feather lead levels reflected the soil lead levels of their neighborhoods and nestling blood lead levels were similar to those of adult mockingbirds in the same neighborhoods. Nest success, as evaluated by daily nest survival rates, was higher in the lower lead neighborhood. Clutch sizes varied substantially across neighborhoods, but rates of unhatched eggs did not covary with neighborhood lead levels, suggesting that other drivers are influencing variation in clutch sizes and hatching success in urban habitats. At least one-third of nestling mockingbirds were sired by an extra-pair male, and there was no relationship between extra-pair paternity rates and neighborhood lead levels. This study provides insight on how lead contamination may influence reproduction in urban-dwelling wildlife and suggests that nestling birds could serve as useful bioindicators of lead levels in urban neighborhoods.

Lead poisoning occurs worldwide in populations of predatory birds, but exposure rates and population impacts are known only from regional studies. We evaluated the lead exposure of 1210 bald and golden eagles from 38 US states across North America, including 620 live eagles. We detected unexpectedly high frequencies of lead poisoning of eagles, both chronic (46 to 47% of bald and golden eagles, as measured in bone) and acute (27 to 33% of bald eagles and 7 to 35% of golden eagles, as measured in liver, blood, and feathers). Frequency of lead poisoning was influenced by age and, for bald eagles, by region and season. Continent-wide demographic modeling suggests that poisoning at this level suppresses population growth rates for bald eagles by 3.8% (95% confidence interval: 2.5%, 5.4%) and for golden eagles by 0.8% (0.7%, 0.9%). Lead poisoning is an underappreciated but important constraint on continent-wide populations of these iconic protected species.

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 identification of modifiers of glucocorticoid release in wild condors. 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 (2300 ± 1400 ng/g dry wt, average ± SD, n = 27) than captive condors (910 ± 490 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 with 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 contaminant-associated 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 need for further investigations into the physiological impacts of sub-lethal contaminant exposures in scavenging species worldwide.

We examined the relationships among tuna consumption, hair mercury levels, and knowledge of mercury exposure risk from tuna consumption in university students that were offered tuna daily at university-run dining halls. Hair total mercury levels in tuna consumers were higher than those in non-tuna consumers (average = 0.466 mu g/g +/- 0.328 standard deviation [SD], n = 20 vs 0.110 mu g/g +/- 0.105 SD, n = 33, respectively; p < 0.0001, Mann-Whitney U test), with tuna eaters exhibiting a positive relationship between self-reported tuna consumption at dining halls and hair mercury levels (R-2 = 0.868, p < 0.0001, n = 17, linear regression). For all tuna eaters surveyed, more than half (54%) self-reported eating >= 3 tuna meals/wk, potentially exceeding the US Environmental Protection Agency's reference dose for methylmercury of 0.1 mu g/kg body weight/d. Seven percent of study participants reported they consumed >20 tuna meals/wk, which was related to hair mercury levels >1 mu g/g, a level of concern. Study participants had an overall lack of knowledge and confidence in their knowledge about mercury exposure risk from tuna consumption, with >99% of participants reporting low knowledge and low confidence in survey answers. Our study highlights the importance of education about the risks of tuna consumption, particularly in institutional settings where individuals have unlimited access to tuna products. Environ Toxicol Chem 2019;00:1-7. (c) 2019 SETAC

Many urban areas have elevated soil lead concentrations due to prior large-scale use of lead in products such as paint and automobile gasoline. This presents a potential problem for the growing numbers of wildlife living in urbanized areas as lead exposure is known to affect multiple physiological systems, including the nervous system, in vertebrate species. In humans and laboratory animals, low-level lead exposure is associated with neurological impairment, but less is known about how lead may affect the behavior of urban wildlife. We focused on the Northern Mockingbird Mimus polyglottos, a common, omnivorous North American songbird, to gain insights into how lead may affect the physiology and behavior of urban wildlife. We predicted that birds living in neighborhoods with high soil lead concentrations would (a) exhibit elevated lead concentrations in their blood and feathers, (b) exhibit lower body condition, (c) exhibit less diverse and consistent vocal repertoires, and (d) behave more aggressively during simulated conspecific territorial intrusions compared to birds living in neighborhoods with lower soil lead concentrations. Controlling for other habitat differences, we found that birds from areas of high soil lead had elevated lead concentrations in blood and feathers, but found no differences in body condition or vocal repertoires. However, birds from high lead areas responded more aggressively during simulated intrusions. These findings indicate that sub-lethal lead exposure may be common among wildlife living in urban areas, and that this exposure is associated with increased aggression. Better understanding of the extent of the relationship between lead exposure and aggression and the consequences this could have for survival and reproduction of wild animals are clear priorities for future work in this and other urban ecosystems.

Vertebrates respond to stressful stimuli with the secretion of glucocorticoid (GC) hormones, such as corticosterone (CORT), and measurements of these hormones in wild species can provide insight into physiological responses to environmental and human-induced stressors. California condors (Gymnogyps californianus) are a critically endangered and intensively managed avian species for which information on GC response to stress is lacking. Here we evaluated a commercially available I125 double antibody radioimmunoassay (RIA) and an enzyme-linked immunosorbent assay (ELISA) kit for measurement of CORT and GC metabolites (GCM) in California condor plasma, urate, and feather samples. The precision and accuracy of the RIA assay outperformed the ELISA for CORT and GCM measurements, and CORT and GCM values were not comparable between the two assays for any sample type. RIA measurements of total CORT in condor plasma collected from 41 condors within 15 minutes of a handling stressor were highly variable (median = 70 ng/mL, range = 1-189 ng/mL) and significantly different between wild and captive condors (p = 0.02, two-tailed t-test, n = 10 wild and 11 captive). Urate GCM levels (median = 620 ng/g dry wt., range = 0.74-7200 ng/g dry wt., n = 216) significantly increased within 2 hr of the acute handling stressor (p = 0.032, n = 11 condors, one-tailed paired t-test), while feather section CORT concentrations (median = 18 pg/mm, range = 6.3-68 ng/g, n = 37) also varied widely within and between feathers. Comparison of multiple regression linear models shows condor age as a significant predictors of plasma CORT levels, while age, sex, and plasma CORT levels predicted GCM levels in urates collected within 30 min of the start of handling. Our findings highlight the need for validation when selecting an immunoassay for use with a new species, and suggest that non-invasively collected urates and feathers hold promise for assessing condor responses to acute or chronic environmental and human-induced stressors.

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.

Pelagic predators such as albatross have long been of conservation concern, but assessing their status poses numerous challenges. A standard monitoring method for albatross is colony-based nest counts to track numbers of breeders. However, a variable proportion of the population skips breeding in any given year and cannot be quantified by nest counts, creating several complications to efforts in understanding population dynamics. We used stochastic demographic matrix models for black-footed (Phoebastria nigripes) and Laysan (P. immutabilis) albatross to investigate: i) the potential for the skipping behavior of breeders to create apparent density dependence in nest counts, ii) the limitations to assessing population trends from nest counts and implications for evaluating impacts from fisheries bycatch, including calculating Potential Biological Removal values, and iii) the relative importance of at-sea versus on-island threats to population viability. We found the increased likelihood of these albatrosses skipping breeding following a successful season – a feature common to many seabirds and other taxa – results in substantial negative temporal auto-correlation in the observable population that can be misinterpreted as negative density dependence, with important implications for inferences about population viability. Black-footed albatross appear limited by fisheries bycatch, while Laysan albatross, which have low estimated bycatch mortality, are currently at greater risk from island-based threats. Our results suggest a cautionary approach to managing black-footed and Laysan albatross should be adopted because detecting population declines from nest counts could take decades. Ultimately, we highlight the inherent difficulties in assessing population status and trends in long-lived species such as albatross.

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.

N.D. Holmes,∗ ¶ G.R. Howald,∗ A.S. Wegmann,∗ C.J. Donlan,†‡ M. Finkelstein,§ and B. Keitt∗ ∗Island Conservation, 2161 Delaware Ave Suite A, Santa Cruz, CA 95060, U.S.A. †Advanced Conservation Strategies, Via Agusta 12, Cordoba 14011, Spain ‡Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 15853, U.S.A. §University of California at Santa Cruz, 1156 High Street, Santa Cruz, CA 95064, U.S.A.