Dynamics of leaching of POPs and additives from plastic in a Procellariiform gastric model: Diet- and polymer-dependent effects and implications for long-term exposure.

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.

Lead exposure is correlated with reduced nesting success of an urban songbird.

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.

Microplastic in northern anchovies (Engraulis mordax) and common murres (Uria aalge) from the Monterey Bay, California USA - Insights into prevalence, composition, and estrogenic activity.

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.

Genetically based demographic reconstructions require careful consideration of generation time.

Bakker et al. use Robinson et al.'s reconstruction of three species of vulture to illustrate how incorrect generation time estimates can yield inaccurate results, underscoring the importance of generation time specification for genetically based reconstructions, especially for comparisons and species of conservation concern.

Demographic implications of lead poisoning for eagles across North America.

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.

Foraging behavior, contaminant exposure risk, and the stress response in wild California condors (Gymnogyps californianus).

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 (ß = 53 ± 20 SE) and peak urate GCM levels (ß = 1090 ± 586 SE). Years observed feeding on marine mammals, a variable positively associated with DDE and PCB exposure, positively influenced peak urate GCM (ß = 1100 ± 520 SE) and the magnitude of GCM response (peak GCM - 1st urate GCM) (ß = 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.

Tuna Consumption, Mercury Exposure, and Knowledge about Mercury Exposure Risk from Tuna Consumption in University Students.

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 µg/g ± 0.328 standard deviation [SD], n = 20 vs 0.110 µg/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 (R2 = 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 µg/kg body weight/d. Seven percent of study participants reported they consumed >20 tuna meals/wk, which was related to hair mercury levels >1 µg/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;38:1988-1994. © 2019 SETAC.

Sub-lethal exposure to lead is associated with heightened aggression in an urban songbird.

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.

Glucocorticoid measurement in plasma, urates, and feathers from California condors (Gymnogyps californianus) in response to a human-induced stressor.

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.

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.

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.

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.

Linking cases of illegal shootings of the endangered California condor using stable lead isotope analysis.

Lead poisoning is preventing the recovery of the critically endangered California condor (Gymnogyps californianus) and lead isotope analyses have demonstrated that ingestion of spent lead ammunition is the principal source of lead poisoning in condors. Over an 8 month period in 2009, three lead-poisoned condors were independently presented with birdshot embedded in their tissues, evidencing they had been shot. No information connecting these illegal shooting events existed and the timing of the shooting(s) was unknown. Using lead concentration and stable lead isotope analyses of feathers, blood, and recovered birdshot, we observed that: i) lead isotope ratios of embedded shot from all three birds were measurably indistinguishable from each other, suggesting a common source; ii) lead exposure histories re-constructed from feather analysis suggested that the shooting(s) occurred within the same timeframe; and iii) two of the three condors were lead poisoned from a lead source isotopically indistinguishable from the embedded birdshot, implicating ingestion of this type of birdshot as the source of poisoning. One of the condors was subsequently lead poisoned the following year from ingestion of a lead buckshot (blood lead 556 µg/dL), illustrating that ingested shot possess a substantially greater lead poisoning risk compared to embedded shot retained in tissue (blood lead ~20 µg/dL). To our knowledge, this is the first study to use lead isotopes as a tool to retrospectively link wildlife shooting events.

Assessing mercury exposure and biomarkers in largemouth bass (Micropterus salmoides) from a contaminated river system in California.

We evaluated mercury (Hg) exposure and two biomarkers, metallothionein (MT) gene expression and histopathological alterations in a wild fish species, largemouth bass (Micropterus salmoides), collected from the Sacramento-San Joaquin Delta, CA, a region polluted with Hg from historic mining activities. Hg is highly toxic and can disrupt multiple physiological systems in vertebrate species, including the immune system. Total mercury (THg) concentration in muscle tissue ranged from 0.12 to 0.98 ppm (wet weight) and was not related to body condition (r (2) = 0.005, p = 0.555). Using linear regression analysis, we found a positive relationship between MT gene expression (as determined using quantitative polymerase chain reaction) and copper, zinc, manganese, aluminum, and nickel (decreased to one variable by way of principal component analysis) (r (2) = 0.379, p = 0.044), a negative relationship with selenium (r (2) = 0.487, p = 0.017), and a weak, negative relationship with THg concentrations (r (2) = 0.337, p = 0.061). Juvenile largemouth bass collected from Hg-contaminated areas displayed histopathological features of immunosuppression compared with those collected from less contaminated areas as evidenced by significantly lower macrophage density in kidney and liver tissue (p = 0.018 and 0.020, respectively), greater trematode density in liver tissue (p = 0.014), and a greater number of adult trematodes. Our results suggest that largemouth bass may be experiencing sublethal effects from chronic Hg exposure. Furthermore, our findings illustrate the utility of examining multiple sublethal markers of effect to assess the impacts of contaminant exposure on physiological function in wild species.

Lead poisoning and the deceptive recovery of the critically endangered California condor.

Endangered species recovery programs seek to restore populations to self-sustaining levels. Nonetheless, many recovering species require continuing management to compensate for persistent threats in their environment. Judging true recovery in the face of this management is often difficult, impeding thorough analysis of the success of conservation programs. We illustrate these challenges with a multidisciplinary study of one of the world's rarest birds-the California condor (Gymnogyps californianus). California condors were brought to the brink of extinction, in part, because of lead poisoning, and lead poisoning remains a significant threat today. We evaluated individual lead-related health effects, the efficacy of current efforts to prevent lead-caused deaths, and the consequences of any reduction in currently intensive management actions. Our results show that condors in California remain chronically exposed to harmful levels of lead; 30% of the annual blood samples collected from condors indicate lead exposure (blood lead ≥ 200 ng/mL) that causes significant subclinical health effects, measured as >60% inhibition of the heme biosynthetic enzyme δ-aminolevulinic acid dehydratase. Furthermore, each year, ∼20% of free-flying birds have blood lead levels (≥450 ng/mL) that indicate the need for clinical intervention to avert morbidity and mortality. Lead isotopic analysis shows that lead-based ammunition is the principle source of lead poisoning in condors. Finally, population models based on condor demographic data show that the condor's apparent recovery is solely because of intensive ongoing management, with the only hope of achieving true recovery dependent on the elimination or substantial reduction of lead poisoning rates.

Patterns of mortality in free-ranging California Condors (Gymnogyps californianus).

We document causes of death in free-ranging California Condors (Gymnogyps californianus) from the inception of the reintroduction program in 1992 through December 2009 to identify current and historic mortality factors that might interfere with establishment of self-sustaining populations in the wild. A total of 135 deaths occurred from October 1992 (the first post-release death) through December 2009, from a maximum population-at-risk of 352 birds, for a cumulative crude mortality rate of 38%. A definitive cause of death was determined for 76 of the 98 submitted cases, 70% (53/76) of which were attributed to anthropogenic causes. Trash ingestion was the most important mortality factor in nestlings (proportional mortality rate [PMR] 73%; 8/11), while lead toxicosis was the most important factor in juveniles (PMR 26%; 13/50) and adults (PMR 67%; 10/15). These results demonstrate that the leading causes of death at all California Condor release sites are anthropogenic. The mortality factors thought to be important in the decline of the historic California Condor population, particularly lead poisoning, remain the most important documented mortality factors today. Without effective mitigation, these factors can be expected to have the same effects on the sustainability of the wild populations as they have in the past.

Leadership: a new frontier in conservation science.

Leadership is a critical tool for expanding the influence of conservation science, but recent advances in leadership concepts and practice remain underutilized by conservation scientists. Furthermore, an explicit conceptual foundation and definition of leadership in conservation science are not available in the literature. Here we drew on our diverse leadership experiences, our reading of leadership literature, and discussions with selected conservation science leaders to define conservation-science leadership, summarize an exploratory set of leadership principles that are applicable to conservation science, and recommend actions to expand leadership capacity among conservation scientists and practitioners. We define 2 types of conservation-science leadership: shaping conservation science through path-breaking research, and advancing the integration of conservation science into policy, management, and society at large. We focused on the second, integrative type of leadership because we believe it presents the greatest opportunity for improving conservation effectiveness. We identified 8 leadership principles derived mainly from the "adaptive leadership" literature: recognize the social dimension of the problem; cycle frequently through action and reflection; get and maintain attention; combine strengths of multiple leaders; extend your reach through networks of relationships; strategically time your effort; nurture productive conflict; and cultivate diversity. Conservation scientists and practitioners should strive to develop themselves as leaders, and the Society for Conservation Biology, conservation organizations, and academia should support this effort through professional development, mentoring, teaching, and research.

Evaluating the potential effectiveness of compensatory mitigation strategies for marine bycatch.

Conservationists are continually seeking new strategies to reverse population declines and safeguard against species extinctions. Here we evaluate the potential efficacy of a recently proposed approach to offset a major anthropogenic threat to many marine vertebrates: incidental bycatch in commercial fisheries operations. This new approach, compensatory mitigation for marine bycatch (CMMB), is conceived as a way to replace or reduce mandated restrictions on fishing activities with compensatory activities (e.g., removal of introduced predators from islands) funded by levies placed on fishers. While efforts are underway to bring CMMB into policy discussions, to date there has not been a detailed evaluation of CMMB's potential as a conservation tool, and in particular, a list of necessary and sufficient criteria that CMMB must meet to be an effective conservation strategy. Here we present a list of criteria to assess CMMB that are tied to critical ecological aspects of the species targeted for conservation, the range of possible mitigation activities, and the multi-species impact of fisheries bycatch. We conclude that, overall, CMMB has little potential for benefit and a substantial potential for harm if implemented to solve most fisheries bycatch problems. In particular, CMMB is likely to be effective only when applied to short-lived and highly-fecund species (not the characteristics of most bycatch-impacted species) and to fisheries that take few non-target species, and especially few non-seabird species (not the characteristics of most fisheries). Thus, CMMB appears to have limited application and should only be implemented after rigorous appraisal on a case-specific basis; otherwise it has the potential to accelerate declines of marine species currently threatened by fisheries bycatch.