Effects of lead exposure on birds breeding in the Southeast Missouri Lead Mining District

Lead mining in the Southeast Missouri Lead Mining District began in the 1700s and continued for nearly 300 years; the waste piles associated with smelting, mining, and milling of lead ores have released metal residues that have contaminated soil and water in the region. Previous studies in the district have indicated potential harm to wildlife, including birds, because of elevated lead concentrations associated with mining. Exposure to soil-borne lead was correlated with elevated lead concentrations in tissues, inhibition of δ-aminolevulinic acid dehydratase (δALAD), and renal lesions in birds foraging on ground-dwelling invertebrates at contaminated sites (compared to reference sites) in the Southeast Missouri Lead Mining District.

This study assessed reproductive outcomes for songbirds exposed to soil-borne lead in the district, examined the relation between lead concentrations in soils and in tissues of ground-feeding birds and prey species, and compared the results to literature-based toxicity thresholds for lead that are associated with negative effects in birds. Three lead-contaminated sites and three reference sites (with background concentrations of lead and no known mining inputs) were compared in two ways: individually to all other sites or by site type. Additional effects of lead exposure were evaluated by examining concentrations of biomarkers (oxidative stress, lipid peroxidation, and deoxyribonucleic acid damage) in liver tissues, δALAD inhibition, and renal and hepatic microscopic lesions in birds from lead-contaminated and reference sites.

Lead concentrations in soil were site-dependent and were also generally heterogeneous within the lead-contaminated sites. Between 17 and 74 percent of all soil samples at contaminated sites had lead concentrations that exceeded a threshold (1,000 milligrams per kilogram [mg/kg] lead in soil) previously associated with adverse physiological effects in birds in the Southeast Missouri Lead Mining District. Lead concentrations in mixed invertebrates from lead-contaminated sites (282 to 2,230 mg/kg dry weight [dw]) indicated that consuming soil-dwelling prey species is a potential exposure pathway for adult birds and their broods. At lead-contaminated sites, lead concentrations in 40.5 percent of blood samples (adults and their broods) were within a subclinical effects range (0.9 to 2.3 mg/kg dw), and 18.7 percent of samples had lead concentrations that exceeded clinical effects criteria (greater than 2.3 mg/kg dw). In contrast, only 2.6 percent of blood samples from reference sites were within the subclinical effects range for lead; all other blood samples from the reference sites had lead concentrations representative of background concentrations (less than 0.9 mg/kg dw). Subclinical and clinical threshold exceedances for lead concentrations in livers and kidneys were similarly more prevalent at the contaminated sites compared to the reference sites.

Lead concentrations in blood were positively correlated with lead concentrations in soil, livers, and kidneys. Lead concentrations in blood were negatively correlated with δALAD activity; greater than 50 percent of the birds collected at lead-contaminated sites exhibited injury via greater than 50 percent inhibition of δALAD in blood compared to birds at reference sites. Birds with elevated lead concentrations in tissues also exhibited enhanced oxidative stress. Microscopic lesions in the livers and kidneys of birds had similar rates of occurrence at the contaminated and reference sites, and lesion prevalence could not be directly linked to lead exposure. Reproductive success was monitored at 585 nests, and 3 out of 5 species had reduced nest success associated with elevated lead concentrations in soil; habitat measures did not help explain nest success. Reduced nest success may have resulted from greater nest predation resulting from neurological and behavioral effects of lead exposure. Ultimately, these lines of evidence indicate that bird health and reproduction have been negatively affected by exposure to lead-contaminated soils in the Southeast Missouri Lead Mining District.