Anton M. Scheuhammer

Effects of Environmental Methylmercury on the Health of Wild Birds, Mammals, and Fish

Abstract Wild piscivorous fish, mammals, and birds may be at risk for elevated dietary methylmercury intake and toxicity. In controlled feeding studies, the consumption of diets that contained Hg (as methylmercury) at environmentally realistic concentrations resulted in a range of toxic effects in fish, birds, and mammals, including behavioral, neurochemical, hormonal, and reproductive changes. Limited field-based studies, especially with certain wild piscivorous bird species, e.g., the common loon, corroborated laboratory-based results, demonstrating significant relations between methylmercury exposure and various indicators of methylmercury toxicity, including reproductive impairment. Potential population effects in fish and wildlife resulting from dietary methylmercury exposure are expected to vary as a function of species life history, as well as regional differences in fish-Hg concentrations, which, in turn, are influenced by differences in Hg deposition and environmental methylation rates. However, population modeling suggests that reductions in Hg emissions could have substantial benefits for some common loon populations that are currently experiencing elevated methylmercury exposure. Predicted benefits would be mediated primarily through improved hatching success and development of hatchlings to maturity as Hg concentrations in prey fish decline. Other piscivorous species may also benefit from decreased Hg exposure but have not been as extensively studied as the common loon.

The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review.

The toxicity of chronic dietary metal exposure in birds is reviewed. It is concluded that significant physiological and biochemical responses to such exposure conditions occur at dietary metal concentrations insufficient to cause signs of overt toxicity. Particularly important are reproductive effects which include decreased egg production, decreased hatchability, and increased hatchling mortality. Young, growing birds are typically more sensitive to the toxic effects of chronic metal exposure than adults, and altricial species are often more sensitive than precocial species. Factors which modify the absorption and toxicity of heavy metals, such as Se for the case of Hg, and Ca for the case of Pb and Cd, are discussed. Monitoring strategies for assessing environmental metal exposure in birds are evaluated.

Effects of acidification on the availability of toxic metals and calcium to wild birds and mammals

The effects of acidification on wildlife inhabiting aquatic or semi-aquatic environments are reviewed, with particular reference to the possibility for increased dietary exposure to Hg, Cd, Pb and/or Al, and decreased availability of essential dietary minerals such as Ca. It is concluded that: (1) piscivores risk increased exposure to dietary methyl-Hg in acidified habitats, and Hg concentrations in prey may reach levels known to cause reproductive impairment in birds and mammals; (2) piscivores do not risk increased exposure to dietary Cd, Pb or Al because these metals are either not increased in fish due to acidification, or increase are trivial from a toxicological perspective; (3) insectivores and omnivores may, under certain conditions, experience increased exposure to toxic metals in some acidified environments. Exposure levels are likely to be sufficiently low, however, that significant risks to health or reproduction are unlikely. More importantly, these wildlife species may experience a drastic decrease in the availability of dietary Ca due to the pH-related extinction of high-Ca aquatic invertebrate taxa (molluscs, crustaceans). Decreased availability of dietary Ca is known to adversely affect egg laying and eggshell integrity in birds, and the growth of hatchling birds and neonatal mammals. Acidification-related changes in the dietary availability of other essential elements, such as Mg, Se and P, have not been established and require further investigation; (4) herbivores may risk increased exposure to Al and Pb, and perhaps Cd, in acidified environments because certain macrophytes can accumulate high concentrations of these metals under acidic conditions. The relative importance of pH in determining the metal concentrations of major browse species, and the toxicological consequences for herbivores wildlife, is not well established and requires further study. A decreased availability of dietary Ca is also likely for herbivores inhabiting acidified environments.

Common loon eggs as indicators of methylmercury availability in North America.

Increased anthropogenic mercury (Hg) deposition since pre-industrial times, and subsequent transformation of inorganic Hg to methylmercury (MeHg) in aquatic environments, has created areas in North America where Hg poses a relatively high risk to wildlife, especially long-lived, piscivorous species. From 1995 to 2001, we opportunistically collected 577 eggs abandoned by Common Loons from eight states. Egg-Hg concentrations ranged from 0.07 to 4.42 µg/g (ww) or 0.10 to 19.40 µg/g (dw). Mercury was higher in eastern than in western North America. Female blood-Hg concentrations strongly correlated with those of eggs from the same territory even though the mean intraclutch Hg difference was 25%. In New England, egg volume declined significantly as egg-Hg concentrations increased. Fertility was not related to egg-Hg concentrations. Based on existing literature and this studys findings, egg-Hg risk levels were established and applied to our US data set and an existing Canadian data set. Regionally, we found the greatest risk levels in northeastern North America. With few exceptions, loon eggs are suitable indicators of methylmercury availability on lakes with territorial pairs.

The ecotoxicology of lead shot and lead fishing weights

Lead shot ingestion is the primary source of elevated lead exposure and poisoning in waterfowl and most other bird species. For some species (e.g. Common Loons, Gavia immer), lead sinker ingestion is a more frequent cause of lead poisoning. In freshwater environments where recreational angling activity and loon populations co-occur, lead poisoning from ingestion of small (<50 gram) lead sinkers or jigs accounts for 10–50% of recorded adult loon mortality, depending on the locations studied. Lead shot ingestion occurs in waterfowl, and in a wide variety of non-waterfowl species, including upland game birds, shorebirds, raptors, and scavengers. Where it has been explicitly studied in Canada and the US, lead poisoning mortality of bald (Haliacetus leucocephalus) and golden eagles (Aquila chrysactos) from eating prey animals with lead shot embedded in their tissues accounts for an estimated 10–15% of the recorded post-fledging mortality in these raptorial species. In addition to environments that experience hunting with lead shot, clay target shooting ranges, especially those in which the shotfall zones include ponds, marshes, lakes, rivers, beaches, or other aquatic-type environments, create a significant risk of shot ingestion and poisoning for waterbirds. Metallic lead pellets deposited onto soils and aquatic sediments are not chemically or environmentally inert, although tens or hundreds of years may be required for total breakdown and dissolution of pellets. Functional, affordable non-toxic alternatives to lead shot and sinkers are being currently produced, and additional such products are being developed. Several countries have successfully banned the use of small lead sinkers, and of lead shot for waterfowl and other hunting, also for clay target shooting, using a phasing-out process that gives manufactures, sellers, and users adequate time to adjust to the regulations.

Is dietary mercury of neurotoxicological concern to wild polar bears (Ursus maritimus)

Polar bears (Ursus maritimus) are exposed to high concentrations of mercury because they are apex predators in the Arctic ecosystem. Although mercury is a potent neurotoxic heavy metal, it is not known whether current exposures are of neurotoxicological concern to polar bears. We tested the hypotheses that polar bears accumulate levels of mercury in their brains that exceed the estimated lowest observable adverse effect level (20 microg/g dry wt) for mammalian wildlife and that such exposures are associated with subtle neurological damage, as determined by measuring neurochemical biomarkers previously shown to be disrupted by mercury in other high-trophic wildlife. Brain stem (medulla oblongata) tissues from 82 polar bears subsistence hunted in East Greenland were studied. Despite surprisingly low levels of mercury in the brain stem region (total mercury = 0.36 +/- 0.12 microg/g dry wt), a significant negative correlation was measured between N-methyl-D-aspartate (NMDA) receptor levels and both total mercury (r = -0.34, p < 0.01) and methylmercury (r = -0.89, p < 0.05). No relationships were observed among mercury, selenium, and several other neurochemical biomarkers (dopamine-2, gamma-aminobutyric acid type A, muscarinic cholinergic, and nicotinic cholinergic receptors; cholinesterase and monoamine oxidase enzymes). These data show that East Greenland polar bears do not accumulate high levels of mercury in their brain stems. However, decreased levels of NMDA receptors could be one of the most sensitive indicators of mercurys subclinical and early effects.

Lead Poisoning in Upland-foraging Birds of Prey in Canada

We examined the degree of lead exposure, based on tissue-lead concentrations, in 184 raptors of 16 species found dead across Canada. The most prevalent species available for examination were Red-tailed hawks, Great horned owls, and Golden eagles (n=131). The majority of individuals examined had very low lead accumulation, however 3–4% of total mortality in these 3 most commonly encountered species was attributed to lead poisoning. In addition, 1 of 9 Bald Eagles found dead far from aquatic environments was lead poisoned; and a single Turkey Vulture had a highly elevated bone-lead concentration (58 µg/g dry weight). Evidence from our study, along with other published research, indicates that upland-foraging birds of prey and scavengers that typically include game birds and mammals in their diets, are at risk for lead poisoning from the ingestion of lead projectiles from ammunition used in upland hunting. The use of non-lead ammunition for hunting upland game would effectively remove the only serious source of high lead exposure and lead poisoning for upland-foraging raptors.

Influence of reduced dietary calcium on the accumulation and effects of lead, cadmium, and aluminum in birds.

The influence of low dietary calcium on the accumulation and effects of dietary lead, cadmium and aluminum was examined in zebra finches and ring doves. In zebra finches fed a diet containing 0.3% Ca, the hepatic and renal accumulation of lead was enhanced approximately 400% and of cadmium about 150-200%, compared to birds fed a 3.0% Ca diet. Low dietary Ca also caused bones of female finches to lose an average of about 60% of their normal Ca content. Loss of bone-Ca was also observed in male finches, but was less than in females. In reproductively active ring doves, low (0.4%) dietary Ca enhanced the accumulation of lead and cadmium, but not of aluminum, compared with accumulation in doves consuming a 2.0% Ca diet. Enhanced accumulation of lead and cadmium was accompanied by increased synthesis of the metal-binding protein metallothionein and by greater inhibition of delta-aminolevulinic acid dehydratase activity. These results indicate that, under conditions of reduced dietary Ca availability, such as can occur in acid-impacted environments, wild birds risk increased uptake of certain toxic metals and may accumulate toxic concentrations of these metals more rapidly. Researchers should take account of dietary Ca levels when interpreting results of dosing studies in which metals such as lead and cadmium are administered to birds.

Heavy metal and metallothionein concentrations in seabirds from the Pacific coast of Canada

Seabird tissues, collected during the 1990 breeding season from colonies on the Pacific coast of Canada, were analysed for Cd, Hg, Pb and 19 other trace elements. Metallothionein (Mt) was measured in kidneys of three species. Ranges of essential trace metal concentrations were generally narrow, consistent with homeostatic control of these elements in seabird tissues. Cadmium concentrations were always higher in kidney than in liver. Highest mean Cd concentrations (306±78 μg g−1 dry wt) were in kidneys of planktivorous Leachs storm-petrels (Oceanodroma leucorhoa) from Hippa Island in the Queen Charlotte archipelago. Cadmium concentrations in kidneys of both Leachs storm-petrels and rhinoceros auklets (Cerorhinca monocerata) were significantly greater at northern colonies compared to those further south. Cadmium and Mt concentrations were positively correlated in kidneys across the three species for which measurements were made [rhinoceros auklet, Cassins auklet (Ptychoramphus aleuticus), and ancient murrelet (Synthliboramphus antiquus)] with an overall r = 0.82, p < 0.001. Mercury accumulation was not sufficiently great to be of toxicological concern in any of the 5 species. Highest mean Hg concentrations (6.37 μg g−1) were in livers of Leachs storm-petrels from Cleland Island on the west coast of Vancouver Island, and were significantly greater than in birds from further north on Hippa Island. Concentrations of hepatic Hg and Se were not correlated in the three species (rhinoceros auklet, Cassins auklet and ancient murrelet) for which Se was measured. Lead concentrations were consistently greatest in bone, with highest mean concentrations in fork-tailed storm-petrels (Oceanodroma furcata) (6.2 μg g−1 dry wt).

Effects of mercury on neurochemical receptor-binding characteristics in wild mink.

Piscivorous wildlife, such as mink (Mustela vison), routinely are exposed to mercury (Hg) in their natural environment at levels that may cause adverse behavioral outcomes. The purpose of this study was to determine if a correlation exists between neurochemical receptors and concentrations of Hg in the brains of wild mink. Specifically, receptor-binding assays were conducted to characterize the muscarinic cholinergic (mACh) and dopaminergic-2 (D2) systems in brain tissues collected from mink trapped in the Yukon Territory, Ontario, and Nova Scotia (Canada), and values were correlated with total Hg and methyl Hg (MeHg) concentrations in the brains. A significant correlation was found between Hg (total Hg and MeHg) and mACh receptor density (r = 0.546; r = 0.596, respectively) or ligand affinity (r = 0.413; r = 0.474, respectively). A significant negative correlation was found between total Hg and D2 receptor density (r = -0.340) or ligand affinity (r = -0.346). These correlations suggest that environmentally relevant concentrations of Hg may alter neurochemical function in wild mink, and that neurochemical receptor-binding characteristics can be used as a novel biomarker to assess Hgs effects on wildlife. Given the importance of the muscarinic cholinergic and dopaminergic pathways in animal behavior, further studies are required to explore the physiological and ecological significance of these findings.