Feeding Ecology Drives Lead Exposure of Facultative and Obligate Avian Scavengers in the Eastern United States.

Lead poisoning of scavenging birds is a global issue. However, the drivers of lead exposure of avian scavengers have been understood from the perspective of individual species, not cross-taxa assemblages. We analyzed blood (n = 285) and liver (n = 226) lead concentrations of 5 facultative (American crows [Corvus brachyrhynchos], bald eagles [Haliaeetus leucocephalus], golden eagles [Aquila chrysaetos], red-shouldered hawks [Buteo lineatus], and red-tailed hawks [Buteo jamaicensis]) and 2 obligate (black vultures [Coragyps atratus] and turkey vultures [Cathartes aura] avian scavenger species to identify lead exposure patterns. Species and age were significant (α < 0.05) predictors of blood lead exposure of facultative scavengers; species, but not age, was a significant predictor of their liver lead exposure. We detected temporal variations in lead concentrations of facultative scavengers (blood: median = 4.41 µg/dL in spring and summer vs 13.08 µg/dL in autumn and winter; p = <0.001; liver: 0.32 ppm in spring and summer vs median = 4.25 ppm in autumn and winter; p = <0.001). At the species level, we detected between-period differences in blood lead concentrations of bald eagles (p = 0.01) and red-shouldered hawks during the winter (p = 0.001). During summer, obligate scavengers had higher liver lead concentrations than did facultative scavengers (median = 1.76 ppm vs 0.22 ppm; p = <0.001). These data suggest that the feeding ecology of avian scavengers is a determinant of the degree to which they are lead exposed, and they highlight the importance of dietary and behavioral variation in determining lead exposure. Environ Toxicol Chem 2020;39:882-892. © 2020 SETAC.

Parasitaemia data and molecular characterization of Haemoproteus catharti from New World vultures (Cathartidae) reveals a novel clade of Haemosporida.

BACKGROUND: New World vultures (Cathartiformes: Cathartidae) are obligate scavengers comprised of seven species in five genera throughout the Americas. Of these, turkey vultures (Cathartes aura) and black vultures (Coragyps atratus) are the most widespread and, although ecologically similar, have evolved differences in morphology, physiology, and behaviour. Three species of haemosporidians have been reported in New World vultures to date: Haemoproteus catharti, Leucocytozoon toddi and Plasmodium elongatum, although few studies have investigated haemosporidian parasites in this important group of species. In this study, morphological and molecular methods were used to investigate the epidemiology and molecular biology of haemosporidian parasites of New World vultures in North America. METHODS: Blood and/or tissue samples were obtained from 162 turkey vultures and 95 black vultures in six states of the USA. Parasites were identified based on their morphology in blood smears, and sequences of the mitochondrial cytochrome b and nuclear adenylosuccinate lyase genes were obtained for molecular characterization. RESULTS: No parasites were detected in black vultures, whereas 24% of turkey vultures across all sampling locations were positive for H. catharti by blood smear analysis and/or PCR testing. The phylogenetic analysis of cytochrome b gene sequences revealed that H. catharti is closely related to MYCAMH1, a yet unidentified haemosporidian from wood storks (Mycteria americana) in southeastern USA and northern Brazil. Haemoproteus catharti and MYCAMH1 represent a clade that is unmistakably separate from all other Haemoproteus spp., being most closely related to Haemocystidium spp. from reptiles and to Plasmodium spp. from birds and reptiles. CONCLUSIONS: Haemoproteus catharti is a widely-distributed parasite of turkey vultures in North America that is evolutionarily distinct from other haemosporidian parasites. These results reveal that the genetic diversity and evolutionary relationships of avian haemosporidians are still being uncovered, and future studies combining a comprehensive evaluation of morphological and life cycle characteristics with the analysis of multiple nuclear and mitochondrial genes will be useful to redefine the genus boundaries of these parasites and to re-evaluate the relationships amongst haemosporidians of birds, reptiles and mammals.

Assessing multi-tissue lead burdens in free-flying obligate scavengers in eastern North America.

Avian scavengers are regularly exposed to anthropogenic lead. Although many studies evaluate lead concentrations of either blood or tissues of lead-poisoned birds, there is comparatively less research on lead burdens of free-flying, apparently healthy individuals and populations. Here, we address this lack of information by assessing lead levels of multiple tissues (femur, liver, kidney, breast muscle, thigh muscle) in free-flying black vultures (n = 98) and turkey vultures (n = 10) collected outside the hunting season. We found only one individual had a soft tissue lead concentration indicative of acute exposure (6.17 mg/kg wet weight in the liver), while the other 107 vultures showed consistent low-level lead exposure throughout the soft tissues. All vultures, however, had femur lead concentrations indicative of chronic lead exposure (black vultures [Formula: see text]31.80 ± 20.42 mg/kg (±SD); turkey vultures 23.21 ± 18.77 mg/kg). Lead levels were similar in all tissues in both vulture species (in each case, p > 0.05) and were generally highest in the femur, intermediate in the kidney and liver, and lowest in the breast and thigh muscle. Despite the consistency of these patterns, there were few strong correlations between lead levels in different tissues within each species, and those correlations that did exist were not consistent between species. Because these vultures were free flying and apparently healthy, the organism-wide lead distributions and between-species trends we report here provide important insight into the sublethal lead burdens that black vultures and turkey vultures commonly carry. Furthermore, these data offer a framework to better interpret and contextualize lead exposure data collected from these and other species.

Chronic lead exposure is epidemic in obligate scavenger populations in eastern North America.

Lead is a prominent and highly toxic contaminant with important impacts to wildlife. To understand the degree to which wildlife populations are chronically exposed, we quantified lead levels within American black vultures (Coragyps atratus; BLVU) and turkey vultures (Cathartes aura; TUVU), two species that are useful as environmental sentinels in eastern North America. Every individual sampled (n=108) had bone lead levels indicative of chronic exposure to anthropogenic lead (BLVU: x¯=36.99 ± 55.21 mg Pb/kg tissue (±SD); TUVU: x¯=23.02 ± 18.77 mg/kg). Only a few showed evidence of recent lead exposure (BLVU liver: x¯=0.78 ± 0.93 mg/kg; TUVU liver: x¯=0.55 ± 0.34 mg/kg). Isotopic ratios suggested multiple potential sources of lead including ammunition, gasoline, coal-fired power plants, and zinc smelting. Black and turkey vultures range across eastern North America, from Quebec to Florida and individuals may traverse thousands of kilometers annually. The extent to which vultures are exposed suggests that anthropogenic lead permeates eastern North American ecosystems to a previously unrecognized degree. Discovery of an epidemic of chronic lead exposure in such widespread and common species and the failure of soft-tissue sampling to diagnose this pattern has dramatic implications for understanding modern wildlife and human health concerns.