Lead poisoning of raptors: state of the science and cross-discipline mitigation options for a global problem.

Lead poisoning is an important global conservation problem for many species of wildlife, especially raptors. Despite the increasing number of individual studies and regional reviews of lead poisoning of raptors, it has been over a decade since this information has been compiled into a comprehensive global review. Here, we summarize the state of knowledge of lead poisoning of raptors, we review developments in manufacturing of non-lead ammunition, the use of which can reduce the most pervasive source of lead these birds encounter, and we compile data on voluntary and regulatory mitigation options and their associated sociological context. We support our literature review with case studies of mitigation actions, largely provided by the conservation practitioners who study or manage these efforts. Our review illustrates the growing awareness and understanding of lead exposure of raptors, and it shows that the science underpinning this understanding has expanded considerably in recent years. We also show that the political and social appetite for managing lead ammunition appears to vary substantially across administrative regions, countries, and continents. Improved understanding of the drivers of this variation could support more effective mitigation of lead exposure of wildlife. This review also shows that mitigation strategies are likely to be most effective when they are outcome driven, consider behavioural theory, local cultures, and environmental conditions, effectively monitor participation, compliance, and levels of raptor exposure, and support both environmental and human health.

Portable X-ray fluorescence for bone lead measurements of Australian eagles.

Lead (Pb) toxicity from ammunition has been shown to be a threat to scavenging birds across the globe. Toxic levels of lead have recently been found in Australia's largest bird of prey, the wedge-tailed eagle (Aquila audax), through inductively coupled plasma mass spectrometry (ICP-MS) analysis of liver and bone samples. However, ICP-MS is consumptive (causing damage to archived specimens), time-consuming, and expensive. For these reasons, portable X-ray fluorescence (XRF) devices have been optimized to measure bone lead in North American avian species, humans, and other environmental samples. In this study, we assessed portable XRF for bone lead measurement in Australian raptors in two parts. First, we validated the method using tissues from wedge-tailed eagles from Tasmania (A. a. fleayi), analysing bone samples taken from sites on the femur immediately adjacent to sites for which we had ICP-MS data (n = 89). Second, we measured lead via portable XRF in the skulls of wedge-tailed eagles from south-eastern mainland Australia (A. a. audax) collected during a criminal prosecution (n = 92). Portable XRF bone lead measurement demonstrated an excellent correlation with ICP-MS results using root-transformed regression (R2 = 0.88). Calculated equivalent ICP-MS values revealed that greater than 50% of the eagles from mainland Australia had elevated lead levels (>10 mg/kg) and 13% had severe lead exposure (>20 mg/kg). Our results support previous studies of North American avian species and suggest that portable XRF could be a useful and inexpensive option for measurement of bone lead in Australian scavenger species.

A novel method for captive rearing and translocation of juvenile common loons.

Common loons (Gavia immer) are diving waterbirds that are particularly challenging to keep in captivity due to their specific behavioral and physiologic needs, special housing requirements, and susceptibility to stress-related disease. We report a novel method for housing and captive rearing common loon chicks that was developed as part of the first-ever loon translocation effort in southeast Massachusetts, from 2015 to 2017. Thirteen loon chicks were reared in aquatic pens in a natural lake environment, utilizing noninvasive feeding and monitoring techniques that avoided human habituation. Chicks were reared in aquatic pens for 16-28 days before being released onto the lake. All chicks remained clinically normal and were monitored on the lake for up to 4 months following release. At least four of the chicks were subsequently confirmed to have survived to adulthood when they returned to the area in breeding plumage two to 3 years following release. Two of these confirmed adults displayed prolonged territorial pair behavior together, and this is an encouraging early sign that captive-reared individuals may form successful breeding pairs in the future. Because most immature loons remain on the ocean until at least 3 years of age, we expect additional captive-reared loons to return to the release area in subsequent years. These husbandry techniques could be applied to other loon and diving bird species that are notoriously difficult to house in captivity. The novel feeding techniques described here could also be adapted for loon chicks being reared in pools or other traditional captive settings.

PLASMA BIOCHEMISTRY AND PROTEIN ELECTROPHORESIS REFERENCE INTERVALS OF THE COMMON LOON (GAVIA IMMER).

There are no published plasma biochemistry reference intervals for any species within the order Gaviiformes, which includes the common loon (Gavia immer). Because of their unique classification and lack of close taxonomic relatives, species-specific values for clinical data in loons are needed. This study determined reference intervals for plasma biochemical values in adult common loons, and reference intervals for protein electrophoresis values in both adult and juvenile common loons. Healthy, wild adult (n = 148, age >3 yr) and juvenile (n = 31, age 4-12 wk) common loons were sampled on freshwater summer breeding territories at study sites across North America. Plasma biochemical analytes included glucose (Glu), total calcium, phosphorus, sodium, potassium, chloride, blood urea nitrogen (BUN), uric acid, cholesterol, triglycerides, creatine kinase, γ-glutamyl transferase, alkaline phosphatase (ALP), lactate dehydrogenase, aspartate aminotransferase, amylase, and bile acids. Protein electrophoresis data included albumin to globulin ratio (A: G), prealbumin, albumin, α1-globulin, α2-globulin, ß-globulin, and γ-globulin. Adult females had significantly higher Glu, ALP, and BUN than adult males. Juvenile loons had higher ß-globulins than adults, whereas adults had higher α1-globulins. Establishment of complete reference intervals will improve clinical assessment of captive loons, and allow researchers to better understand the health of wild loons in response to the multiple environmental stressors faced by these species.

Lead poisoning from ingestion of fishing gear: A review.

Many publications have investigated the ingestion and toxicity of metallic lead from hunting and the shooting sports. However, there is limited literature on toxicity associated with the ingestion of lead fishing weights, despite our knowledge of damage caused to many species from entanglement in lines, nets, and fish-hooks. This paper surveys current knowledge of species poisoned by ingestion of lead fishing gear and the types of gear that have been implicated. We review the impacts of lead fishing tackle on wildlife species and human health and describe the efficacy of efforts to reduce the use of lead tackle through voluntary, educational, and regulatory approaches to encourage adoption of non-toxic fishing gear. The authors emphasize the need for further research and policy initiatives to deal with this serious problem.

Lead exposure biomarkers in the Common Loon.

Lead in fishing tackle is a significant source of exposure to the environment, wildlife, and potentially humans. Common Loons (Gavia immer) are exposed to lead by eating fish which have lead tackle, or ingesting fishing weights or spent ammunition when they ingest small stones to aid in digestion. Blood lead is traditionally used as a biomarker of exposure in loons, but it only reflects recent exposures. Cumulative exposure measured via bone lead may better reflect the overall health of loons and their aquatic habitat. This study compared a portable x-ray fluorescence (XRF) device for measurement of bone lead with and without tissue overlying the bone on loon cadavers with measurements made by inductively coupled plasma mass spectrometry (ICP-MS) of different tissues from the loons. For this study we had 75 bone samples, 19 body fluid samples, and 17 liver lead samples. We found significant correlations between portable XRF bone lead measurements made with overlying tissue and ICP-MS measures of bone lead (R = 0.88), body fluid lead (R = 0.65), and liver lead (R = 0.71). Bone lead was found to be higher in loons collected from non-coastal regions. In assessing lead-related cause of death, bone lead proved more predictive than liver lead. Future studies should investigate the value of these biomarkers for both aquatic health and loon health to further validate our findings.

Subclinical Lead Exposure Among Backyard Chicken Flocks in Massachusetts.

Ownership of backyard chickens (BYCs) is increasing in urban areas, and BYCs often have access to soil around the home. Exposure to lead-contaminated soil is a known health risk for people; however, the degree to which BYCs are exposed is unknown. We employed a cross-sectional convenience sample to assess blood lead levels (BLLs) in 57 BYCs from 30 flocks in a region with established environmental lead contamination. Over two-thirds (70.2%) had detectable levels of lead in their blood, which averaged 12.5 µg/dL (range: <3.3 µg/dL to ≥65.0 µg/dL). No chickens demonstrated clinical evidence of lead toxicosis. Almost all owners (96.2%) reported that their chickens had free access to soil, and almost three-quarters (69.2%) of the participants reported giving their chickens unrestricted access to the property. Our findings demonstrate that subclinical but elevated BLLs are common in BYCs that live in an environment where lead contamination may be present. Our data support the inclusion of blood lead testing in the routine veterinary care of BYCs, especially in areas where historic use of leaded paint and environmental lead contamination are reported.

Documentation of Malaria Parasite ( Plasmodium spp.) Infection and Associated Mortality in a Common Loon (Gavia immer).

We report malaria parasite infection ( Plasmodium spp.) and associated mortality in a Common Loon (Gavia immer) found dead on Lake Umbagog in New Hampshire, US. Necropsy findings showed the bird to be in good body condition but with pericardial edema and splenomegaly. Histopathological examination of brain and heart revealed intraendothelial and intrahistiocytic proliferation of Plasmodium merozoites with myocarditis. By PCR, the presence of Plasmodium parasites was confirmed from all tissues screened including spleen, muscle, and kidney. Sequencing of nested-PCR products revealed two different Plasmodium lineages, CATUST05 and PADOM11, indicating a mixed malaria parasite infection. Clinical findings strongly support malaria-induced mortality in a Common Loon.

Mercury correlates with altered corticosterone but not testosterone or estradiol concentrations in common loons.

We investigated the relation between environmental mercury exposure and corticosterone concentrations in free-living adult common loons (Gavia immer). We determined blood and feather mercury concentrations and compared them to testosterone, estradiol, and stress-induced plasma corticosterone concentrations. Although neither testosterone nor estradiol correlated with Hg levels, there was a robust positive relation between blood Hg and stress-induced corticosterone concentrations in males, but not in females. The lack of an effect in females may have been due to overall less contamination in females. There were no significant correlations between feather Hg and stress-induced corticosterone in either sex. To help determine whether Hg had a causal effect on corticosterone, we investigated the impact of experimental Hg intake on the corticosterone stress response in captive juvenile loons. Juveniles were subjected to three different feeding regimes: 0, 0.4 and 1.2µg Hg (as MeHgCL)/g wet weight (ww) fish. We then measured baseline and 30min post-solitary confinement stressor corticosterone concentrations. The Hg fed chicks exhibited a decreased ability to mount a stress response. From these data, we conclude that Hg contamination does appear to alter the corticosterone response to stress, but not in a consistent predictable pattern. Regardless of the direction of change, however, exposure to mercury contamination and the resulting impact on the corticosterone stress response in common loons may substantially impact health, fitness and survival.

GM1-gangliosidosis in American black bears: clinical, pathological, biochemical and molecular genetic characterization.

G(M1)-gangliosidosis is a rare progressive neurodegenerative disorder due to an autosomal recessively inherited deficiency of lysosomal ß-galactosidase. We have identified seven American black bears (Ursus americanus) found in the Northeast United States suffering from G(M1)-gangliosidosis. This report describes the clinical features, brain MRI, and morphologic, biochemical and molecular genetic findings in the affected bears. Brain lipids were compared with those in the brain of a G(M1)-mouse. The bears presented at ages 10-14 months in poor clinical condition, lethargic, tremulous and ataxic. They continued to decline and were humanely euthanized. The T(2)-weighted MR images of the brain of one bear disclosed white matter hyperintensity. Morphological studies of the brain from five of the bears revealed enlarged neurons with foamy cytoplasm containing granules. Axonal spheroids were present in white matter. Electron microscopic examination revealed lamellated membrane structures within neurons. Cytoplasmic vacuoles were found in the liver, kidneys and chondrocytes and foamy macrophages within the lungs. Acid ß-galactosidase activity in cultured skin fibroblasts was only 1-2% of control values. In the brain, ganglioside-bound sialic acid was increased more than 2-fold with G(M1)-ganglioside predominating. G(A1) content was also increased whereas cerebrosides and sulfatides were markedly decreased. The distribution of gangliosides was similar to that in the G(M1)-mouse brain, but the loss of myelin lipids was greater in the brain of the affected bear than in the brain of the G(M1) mouse. Isolated full-length cDNA of the black bear GLB1 gene revealed 86% homology to its human counterpart in nucleotide sequence and 82% in amino acid sequence. GLB1 cDNA from liver tissue of an affected bear contained a homozygous recessive T(1042) to C transition inducing a Tyr348 to His mutation (Y348H) within a highly conserved region of the GLB1 gene. The coincidence of several black bears with G(M1)-gangliosidosis in the same geographic area suggests increased frequency of a founder mutation in this animal population.

A rapid postmortem screening test for lead toxicosis in common loons (Gavia immer) and bald eagles (Haliaeetus leucocephalus).

In live animals, lead poisoning can be diagnosed by analyzing blood samples. For postmortem testing, blood samples are not available and analysis of liver or kidney is often used for diagnosis. Liver and kidney analysis is relatively expensive and results might not be quickly available. We examined an inexpensive, rapid method to screen animals for lead toxicosis postmortem by testing the mixture of body fluids (termed "tissue fluids") that pool in the body cavity at necropsy for lead. At necropsy we collected body fluid and liver samples from Common Loon (Gavia immer) and Bald Eagle (Haliaeetus leucocephalus) carcasses and determined concentrations of lead in tissue fluid using a desk-top blood lead analyzer. Concentrations of lead in liver were determined by inductively coupled plasma mass spectroscopy. There was strong correlation between tissue fluid and liver tissue lead concentrations, and receiver-operating characteristic analysis gave an area under the curve of 0.91, indicating that postmortem measurements of lead in tissue fluids can be utilized as a screening method for lead toxicosis.

Hematology and absence of hemoparasites in breeding common terns (Sterna hirundo) from Cape Cod, Massachusetts.

In June and July 1995, 98 breeding common terns (Sterna hirundo) were captured, weighed, and bled as a part of ongoing research on the population health and reproductive biology of this species of special concern. Packed cell volume, total and differential white blood cell counts, and blood smears were obtained. Blood smears from 75 terns were examined. No hemoparasites were found. There were some significant differences among hematologic parameters in birds from different islands, and between birds nesting earlier versus later in the season, but there were no significant differences associated with body mass, sex, or age. The absence of hemoparasites in the blood smears of these terns is noteworthy, especially because other studies of seabirds (including Charadriiformes) have revealed low prevalences of hematozoa.

Adverse effects from environmental mercury loads on breeding common loons.

Anthropogenic inputs of mercury (Hg) into the environment have significantly increased in the past century. Concurrently, the availability of methylmercury (MeHg) in aquatic systems has increased to levels posing risks to ecological and human health. We use the common loon (Gavia immer) as an upper trophic level bioindicator of aquatic Hg toxicity in freshwater lakes. Multiple endpoints were selected to measure potential negative impacts from MeHg body burdens on behavior, physiology, survival and reproductive success. A robust spatio-temporal dataset was used that included nearly 5,500 loon Hg measurements over an 18-year period. We measured significant changes related to elevated MeHg body burdens, including aberrant incubation behavior, lethargy, and wing area asymmetry. Mercury body burdens in adult loons increased an average of 8.4% per year. Increasing Hg body burdens reduced the number of fledged chicks per territorial pair, with highest risk loons producing 41% fewer fledged young than our reference group. Our multiple endpoints establish adverse effect thresholds for adult loons at 3.0 ug/g (wet weight) in blood and 40.0 ug/g (fresh weight) in feathers. Mercury contamination in parts of Maine and New Hampshire is a driving stressor for creating breeding population sinks. Standardized monitoring programs are needed to determine if population sinks occur elsewhere and to track aquatic ecosystem responses to changes in Hg emissions and deposition.

Lead poisoning: using transdisciplinary approaches to solve an ancient problem.

Conservation medicine examines the linkages among the health of people, animals, and the environment. Few issues illustrate this approach better than an examination of lead (Pb) toxicity. Lead is cheap and there is a long tradition of its use. But the toxic effects of Pb have also been recognized for many years. As a result, western societies have eliminated or greatly reduced many traditional uses of Pb, including many paints, gasoline, and solders because of threats to the health of humans and the environment. Legislation in several countries has eliminated the use of lead shot for hunting waterfowl. Despite these advances, a great many Pb products continue to be readily available. For example, wildlife agencies recognize that angling and shooting sports deposit thousands of tons of Pb into the environment each year. In recent years, our knowledge of the lethal and sublethal effects of Pb has grown dramatically. This discussion reviews the effects of lead on wildlife, humans, and domestic animals. It also discusses the importance of bringing together all interest groups to find safe alternatives, to develop new educational and policy initiatives, to eliminate many current uses of Pb, and to clean up existing problems.

Hematologic and physiologic reference ranges for free-ranging adult and young common loons (Gavia immer).

Wild common loons (Gavia immer) were captured across much of their southern North American range. Hematologic and physiologic data were collected to establish reference ranges for adults and chicks from four geographic areas: New England, Canadian Maritimes, south-central Quebec, and the Upper Great Lakes. Mean body mass and blood-glucose levels of adult loons varied among geographic regions. Chicks had lower PCV and total solids than adult loons, and also had faster heart rates and higher blood glucose levels. Although mean body mass in males was consistently greater than in females, hematologic and physiologic reference ranges between sexes were not significantly different. Geographic and age-related differences exist in common loon hematologic and physiologic reference ranges and should be considered when assessing such parameters.

Mortality of common loons in New England, 1987 to 2000.

Diagnostic findings are presented on 522 common loons (Gavia immer) found dead or moribund in New England (Connecticut, Maine, Massachusetts, New Hampshire, Rhode Island, and Vermont, USA) between 1987 and 2000. Common loon numbers and range in New England have decreased from historic levels over the last century due to a number of proposed factors. Goals of this study were to identify and categorize causes of mortality and quantify natural versus anthropogenic causes. The majority of identifiable mortality in chicks was from intraspecific aggression (25%) and other causes of trauma (32%). Death in immature loons was primarily from fungal respiratory disease (20%) and trauma (18%). Causes of adult loon mortality differed significantly in breeding and wintering habitats. Wintering adults primarily died of trauma (17%) and infection (11%) and had significantly poorer body condition than breeding loons. In breeding adults, confirmed and suspected lead toxicosis from ingested fishing weights accounted for almost half of all mortality. Direct anthropogenic factors accounted for 52% of loon mortality in this study. Because of high carcass recovery rates, we believe these data are a good representation of loon mortality in New England. Results highlight the importance of human influences on conservation and management of the common loon in New England.