Barnett A. Rattner

Algal blooms in water, soils, dusts, and the environment have captured national attention because of concerns associated with exposure to algal toxins for humans and animals. Algal blooms naturally occur in all surface-water types and are important primary producers for aquatic ecosystems. However, excessive algae growth can be associated with many harmful effects ranging from aesthetic to toxicity concerns, so this excessive growth is commonly called a harmful algal bloom (HAB).Ecological imbalances that can lead to excessive algal growth, such as increased nutrient availability to waterbodies from natural and anthropogenic sources, are well documented in scientific literature. On the other hand, fundamental scientific understandings of environmental causes and controls leading to algal toxin production, environmental exposures, and adverse health outcomes for humans and animals could benefit from more attention by U.S. Geological Survey (USGS) scientists. Understanding when, why, and how the toxin is produced by individual algal cells or communities and why the toxin is released to the surrounding waterbody requires fundamental research to determine a toxin’s role, whether it provides competitive advantage or if other potential reasons exist for toxin production and release, such as secretions from otherwise benign biological processes. This research will require groundbreaking scientific discovery about underlying biologic and abiotic (non-living) processes commonly complicated by local variation in land use, microbial species composition, and ecosystem structure of the surrounding watershed.Although underlying processes by which HABs form may be similar from one waterbody to another, individual waterbodies may be controlled by local factors for HAB development and toxin production that are unique to the watershed. Consequently, many fundamental science gaps exist that prevent informed mitigation and prevention of toxic HAB events. There are also gaps in understanding local conditions that control algal growth unique to specific watersheds. Addressing these science gaps is needed to inform evidence-based decisions that protect human and animal health and that reduce recreational and socioeconomic losses.

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.

An important component of assessing the hazards of anticoagulant rodenticides to non-target wildlife is observations in exposed free-ranging individuals. The objective of this study was to determine whether environmentally realistic, sublethal first-generation anticoagulant rodenticide (FGAR) exposures via prey can result in direct or indirect adverse effects to free-flying raptors. We offered black-tailed prairie dogs (Cynomys ludovicianus) that had fed on Rozol® Prairie Dog Bait (Rozol, 0.005% active ingredient chlorophacinone, CPN) to six wild-caught red-tailed hawks (RTHA, Buteo jamaicensis), and also offered black-tailed prairie dogs that were not exposed to Rozol to another two wild-caught RTHAs for 7 days. On day 6, blood was collected to determine CPN’s effects on blood clotting time. On day 7, seven of the eight RTHAs were fitted with VHF radio telemetry transmitters and the RTHAs were released the following day and were monitored for 33 days. Prothrombin time (PT) and Russell’s viper venom time confirmed that the CPN-exposed RTHAs were exposed to and were adversely affected by CPN. Four of the six CPN-exposed RTHAs exhibited ptiloerection, an indication of thermoregulatory dysfunction due to CPN toxicity, but no signs of intoxication were observed in the reference hawk or the remaining two CPN-exposed RTHAs. Of note is that PT values were associated with ptiloerection duration and frequency; therefore, sublethal CPN exposure can directly or indirectly evoke adverse effects in wild birds. Although our sample sizes were small, this study is a first to relate coagulation times to adverse clinical signs in free-ranging birds.

A literature review of bioaccumulation and biotransformation of organic chemicals in birds was undertaken, aiming to support scoping and prioritization of future research. The objectives were to characterize available bioaccumulation/biotransformation data, identify knowledge gaps, determine how extant data can be used, and explore the strategy and steps forward. An intermediate approach balanced between expediency and rigor was taken given the vastness of the literature. Following a critical review of > 500 peer-reviewed studies, > 25,000 data entries and 2 million information bytes were compiled on > 700 organic compounds for ~ 320 wild species and 60 domestic breeds of birds. These data were organized into themed databases on bioaccumulation and biotransformation, field survey, microsomal enzyme activity, metabolic pathway, and bird taxonomy and diet. Significant data gaps were identified in all databases at multiple levels. Biotransformation characterization was largely fragmented over metabolite/pathway identification and characterization of enzyme activity or biotransformation kinetics. Limited biotransformation kinetic data constrained development of an avian biotransformation model. A substantial shortage of in vivo biotransformation kinetics has been observed as most reported rate constants were derived in vitro. No metric comprehensively captured all key contaminant classes or chemical groups to support broad-scope modeling of bioaccumulation or biotransformation. However, metrics such as biota-feed accumulation factor, maximum transfer factor, and total elimination rate constant were more readily usable for modeling or benchmarking than other reviewed parameters. Analysis demonstrated the lack of bioaccumulation/biotransformation characterization of shorebirds, seabirds, and raptors. In the study of bioaccumulation and biotransformation of organic chemicals in birds, this review revealed the need for greater chemical and avian species diversity, chemical measurements in environmental media, basic biometrics and exposure conditions, multiple tissues/matrices sampling, and further exploration on biotransformation. Limitations of classical bioaccumulation metrics and current research strategies used in bird studies were also discussed. Forward-looking research strategies were proposed: adopting a chemical roadmap for future investigations, integrating existing biomonitoring data, gap-filling with non-testing approaches, improving data reporting practices, expanding field sampling scopes, bridging existing models and theories, exploring biotransformation via avian genomics, and establishing an online data repository.

Anticoagulant rodenticides (ARs) are part of the near billion‐dollar rodenticide industry. Numerous studies have documented the presence of ARs in nontarget wildlife, with evidence of repeated exposure to second‐generation ARs. While birds are generally less sensitive to ARs than target rodent species, in some locations predatory and scavenging birds are exposed by consumption of such poisoned prey and, depending on dose and frequency of exposure, exhibit effects of intoxication that can result in death. Evidence of hemorrhage in conjunction with summed hepatic AR residues >0.1–0.2 mg kg⁻¹ liver wet weight are often used as criteria to diagnose ARs as the likely cause of death. In this review focusing on birds of prey and scavengers, we discuss AR potency, coagulopathy, toxicokinetics and long‐lasting effects of residues, and the role of nutrition and vitamin K status on toxicity, and identify some research needs. A more complete understanding of the factors affecting AR toxicity in nontarget wildlife could enable regulators and natural resource managers to better predict and even mitigate risk. Published 2020. This article is a U.S. Government work and is in the public domain in the USA

Pesticides coated to the seed surface potentially pose an ecological risk to granivorous birds that consume incompletely buried or spilled seeds. To assess the toxicokinetics of seeds treated with current-use fungicides, Japanese quail (Coturnix japonica) were orally dosed with commercially coated wheat seeds. Quail were exposed to metalaxyl, tebuconazole, and fludioxonil at either a low (0.0655, 0.0308, and 0.0328 mg/kg body weight, respectively) or high dose (0.196, 0.0925, and 0.0985 mg/kg body weight, respectively). Fungicides were rapidly absorbed and distributed to tissues. Tebuconazole was metabolized into t-butylhydroxy-tebuconazole. All compounds were eliminated to below detection limits within 24 h. The high detection frequencies observed in fecal samples potentially offers a noninvasive matrix to monitor pesticide exposure. Summing total body burden across plasma, tissue, and fecal samples, less than 9% of the administered dose was identified as the parent fungicide, demonstrating the importance to monitor both active ingredients and their metabolites in biological samples.