Effects of environmental methylmercury on the health of wild birds, mammals, and fish

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.     

Total and Methylmercury in Soft Tissues of White-Tailed Eagle (Haliaeetus albicilla) and Osprey (Pandion haliaetus) Collected in Poland

Mercury (Hg) contamination in piscivorous birds, especially methylmercury (MeHg), has been drawing much attention worldwide in regard to its bioaccumulation and biomagnification in food chains. In this study on Hg in the soft tissues of white-tailed eagles (n = 22) and ospreys (n = 2) from Poland, total Hg (THg) range was 0.15–47.6 while MeHg range was 0.11–8.05 mg kg⁻¹ dry weight. In both species, median THg and MeHg concentrations were lower in the muscle and brain than in the liver and kidney. Median nephric residues were just under 3 and 5 mgTHg kg⁻¹ or 0.9 and 3.7 mgMeHg kg⁻¹ for white-tailed eagle and osprey, respectively. In Norwegian data from the 1970s and in our results, MeHg in the muscle of white-tailed eagle was ~60 % THg (%MeHg = MeHg/THg × 100), lower than in other piscivorous birds. A clear similarity in THg tissue levels was found between Polish and German populations of white-tailed eagles.     

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.     

Mortality factors, helminth burden, and contaminant residues in white-tailed sea eagles (Haliaeetus albicilla) from Finland

Eleven white-tailed sea eagles (WSEs) (Haliaeetus albicilla) collected in Finland between 1994 and 2001 were examined for their causes of death, including analyses of ubiquitous environmental contaminants and parasites. Four WSEs died due to electrocution. Two were lead poisoned and another had fragments of a lead bullet in its gizzard. An 11-year-old female drowned entangled in fishing gear, but also had mercury levels in its liver and kidneys known for detrimental physiological effects. One WSE was evidently killed by an intraspecific conflict, which was also assumed to be with another bird. The mortality factors of two WSEs could not be clarified, but one had a lead level of 4.604 microg g(-1) in its liver, indicating high lead exposure at a clinically relevant concentration. All organ levels of chlorinated pesticides, polychlorinated biphenyls, and cadmium were moderate and not harmful for birds of prey. Seven helminth species, but no ectoparasites or coccidians, were found in 8 of 10 WSEs investigated for parasites. The highest prevalence of 40% was found for the liver fluke Metorchis billis, but no severe parasitosis was diagnosed for the eagles. The two acanthocephalan species Corynosoma semerme and Polymorphus meyeri are both new records for WSEs.     

Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries: a review

Using mainly United Kingdom estuaries as examples, various factors governing the bioavailability, bioaccumulation and biological effects of heavy metals in sediment-dominated estuaries are reviewed. Estuaries and metals primarily discussed include the Mersey (Hg, methylmercury; Pb, alkyllead), the Loughor (Cr, Sn), the Severn (Ag, Cd), the Fal (As, Cu, Sn, Zn), Poole Harbour (Cd, Hg, Se, tributyltin) and Southampton Water (tributyltin). Concentrations and bioavailabilities of metals in estuarine sediments depend on many different processes. Examples include (1) mobilisation of metals to the interstitial water and their chemical speciation, (2) transformation (e.g. methylation) of metals including As, Hg, Pb and Sn (3) the control exerted by major sediment components (e.g. oxides of Fe and organics) to which metals are preferentially bound, (4) competition between sediment metals (e.g. Cu and Ag; Zn and Cd) for uptake sites in organisms, and (5) the influence of bioturbation, salinity, redox or pH on these processes. Under field conditions, identification of dominant processes can be achieved by observing the goodness of fit between metal concentrations in ubiquitous deposit-feeding species and levels in various types of sediment extract over a wide spectrum of sediment types. Factors of more local importance are often indicated by the marked deviation of some points from otherwise excellent relationships. For example, points lying above the line relating tissue Sn concentrations in the clam Scrobicularia plana to those in 1 n HCl extracts of sediments were found to reflect the accumulation of tributyltin, a more readily bioavailable form of Sn. In the same species, unexpectedly high tissue-Cu concentrations were characteristic of very anoxic in sediments and tissue And As and Pb concentrations were suppressed in sediments having high concentrations of Fe oxides. Under field conditions, examples of deleterious effects on benthic organisms that can be attributed to specific metallic pollutants are comparatively rare. Effects of tributyltins from antifouling paints on oysters and neogastropods have been documented and their toxicity has undoubtedly led to environmental degradation in many UK estuaries and coastal areas. In estuaries contaminated with metal-mining wastes, the effects of Cu and Zn on species distribution can be observed, but they are generally less obvious than would be predicted from experimental data. Effects are ameliorated by the induction of metal tolerance mechanisms in some species and in others by the appearance of tolerant strains. The induction of metal detoxification systems involving the formation of granules or metal-binding proteins leads in some species to tissue concentrations that are orders of magnitude higher than normal. For example, high concentrations of Cd and Ag have been found in some species from the Severn Estuary, although there is no unequivocal evidence that either metal has caused deleterious effects on benthic populations. On the other hand, experimental studies with Ag, Cd, Cr, Cu, Hg and Zn show that they are toxic to some species at environmentally realistic levels. Since pollutants rarely occur singly, it is likely that in many moderately contaminated estuaries metals contribute to the stress to organisms caused by substances requiring detoxification. There has been much speculation over the years concerning the biomagnification of metals with increasing trophic levels along food chains. Whilst animals having higher metal concentrations than their prey are sometimes found, the only consistent evidence of biomagnification concerns methylmercury. When estuarine birds are considered, there are relatively few instances in which deleterious effects can unequivocally be attributed to metals or their compounds. However, the Mersey bird kill was attributable to alkyllead pollution from industry. Among other organometals, methylmercury has proved toxic to birds but, so far, no evidence for the toxicity of tributyltin has been reported. However, the compound may have affected bird populations through its effects on the abundance of prey organisms, particularly estuarine molluscs. Of the inorganic forms of metals, Pb in the form of shot has caused problems in many areas and Cd, Hg and Se are suspected of causing toxic effects. There is little field evidence that birds have been affected by Ag, As, Cr, Cu or Zn individually. On the other hand, it is difficult to exclude the possibility that, additively, these metals may produce a significant effect. In part, the lack of evidence reflects the fact that relatively little research has been done. There is scope for more work on metals and organometals in estuarine birds, particularly with regard to their metabolism and their effects on juveniles and individuals subjected to stresses such as starvation.     

Persistent organochlorine levels in six prey species of the gyrfalcon Falco rusticolus in Iceland

Our previous investigations have revealed very high levels of organochlorines (OCs) in the Icelandic gyrfalcon Falco rusticolus, a resident top predator. We now examine six potential prey species of birds, both resident and migratory, in order to elucidate the most likely route of the OCs to the gyrfalcon. The ptarmigan Lagopus mutus, the most important prey of the gyrfalcon, contained very low levels of OCs. Bioaccumulation of polychlorinated biphenyls (PCBs) and DDTs in mallards Anas platyrhynchos, tufted ducks Aythya fuligula, golden plovers Pluvialis apricaria, purple sandpipers Calidris maritima, and black guillemots Cepphus grylle reflected their position in the foodchain. The differences in OC-levels seem nevertheless too high just to reflect the different food-chain levels of these species in Iceland. The winter grounds of the migratory golden plovers and tufted ducks appear to be more contaminated than the Icelandic terrestrial habitat of ptarmigans or the freshwater habitat as reflected in mallards, both resident species. However, spending the winter on the coast in Iceland, results in high levels of contaminants in purple sandpipers and black guillemots. Our results indicate OC contamination of the marine ecosystem in Iceland while the terrestrial and freshwater ecosystems are little affected. It is postulated that gyrfalcons receive the major part of the observed contamination from prey other than ptarmigan, especially birds associated with the marine ecosystem and also from migratory birds.     

Effects of methylmercury exposure on glutathione metabolism, oxidative stress, and chromosomal damage in captive-reared common loon (Gavia immer) chicks

We quantified the level of dietary mercury (Hg), delivered as methylmercury chloride (CH₃HgCl), associated with negative effects on organ and plasma biochemistries related to glutathione (GSH) metabolism and oxidative stress, and chromosomal damage in captive-reared common loon (Gavia immer) chicks reared from hatch to 105 days. Mercury-associated effects related to oxidative stress and altered glutathione metabolism occurred at 1.2 μg Hg/g and 0.4 μg Hg/g, an ecologically relevant dietary mercury level, but not at 0.08 μg Hg/g. Among the variables that contributed most to dissimilarities in tissue chemistries between control and treatment groups were increased levels of oxidized glutathione (GSSG), GSH peroxidase, and the ratio of GSSG to GSH in brain tissue; increased levels of hepatic GSH; and decreased levels of hepatic glucose-6-phosphate dehydrogenase (G-6-PDH). Our results also suggest that chronic exposure to environmentally relevant dietary Hg levels did not result in statistically significant somatic chromosomal damage in common loon chicks.     

Mercury and cadmium in common cormorants (Phalacrocorax carbo)

Mercury (Hg) and cadmium (Cd) in common cormorants (Phalacrocorax carbo) collected in Lake Biwa, Japan and Tokyo, Japan, were investigated to elucidate the biological behaviors of these elements, and to assess exposure to these pollutants of wild, fish-eating birds. Hg and Cd concentrations were highest in the liver and kidneys, respectively. The lowest levels of both elements were observed in chicks. Hg concentrations in all tissues except brain increased significantly with growth from chicks to juveniles (p<0.05, U-test). Cd concentrations in the kidneys and liver also increased significantly during growth from juvenile to adult (p<0.005, U-test). When comparing hepatic Hg and Cd in adult birds between 10 samples from Lake Biwa and nine samples from Tokyo, the Cd concentrations in the Lake Biwa samples (1.4+/-0.37 microg/g dry wt) (mean+/-SD) were significantly higher than those from Tokyo (0.32+/-0.16 microg/g dry wt) (p<0.005, U-test), while no statistically significant difference was found in the Hg concentrations. Possible causes of these differences were discussed in relation to their prey.     

Organochlorine pesticide contamination in grassland-nesting passerines that breed in North America

Organochlorine pesticides and metabolites were measured in grassland-nesting passerines that breed in North America. We also examined testes of male birds for abnormalities that may have resulted from pesticide exposure. Forty-four of 99 individuals contained one or more organochlorine pesticides above the detection limit, representing nine of 10 species. The most prevalent compound detected was p,p'-DDE (minimum-maximum levels: 7.55-285.85 ng/g, carcass concentration). Insectivorous birds had significantly higher levels of p,p'-DDE than both omnivores and granivores. Birds that frequented moist grassland habitats had significantly higher levels of p,p'-DDE than those that frequented drier grassland habitats. No evidence of feminization was observed in any of the testes analyzed, however, other endpoint effects of contamination (e.g. hormone levels and immunological parameters) should be investigated in future studies.     

Large-scale spatial variation in mercury concentrations in cattle in NW Spain

Mercury (Hg) is a highly toxic environmental contaminant and man-made emissions account for between a quarter and a third of total atmospheric levels. Point discharges, particularly coal-burning power stations, are major sources of atmospheric Hg and can result in marked spatial variation in mercury deposition and subsequent uptake by biota. The aims of this study were to quantify the extent to which major point and diffuse sources of atmospheric Hg emissions affected accumulation of Hg by biota throughout Galicia and Asturias, two of the major regions in northwest Spain. We did this by relating renal Hg concentrations in locally reared cattle (n=284) to the proximity of animals to point and diffuse sources of Hg emissions. Mercury residues in calf kidneys ranged between non-detected and 89.4 g/kg wet weight. Point discharges from coal-fired power plants in Galicia had the most dominant impact on Hg accumulation by calves in Galicia, affecting animals throughout the region and explaining some two-thirds of the variation in renal residues between animals located directly downwind from the plants. The effects of more diffuse emission sources on Hg accumulation in calves were not distinguishable in Galicia but were detected in cattle from neighbouring Asturias. The impact of both point and diffuse sources in elevating environmental levels of bioavailable Hg and subsequent accumulation by cattle extended to approximately 140-200 km downwind from source.     

Arsenic residues in predatory birds from an area of Britain with naturally and anthropogenically elevated arsenic levels

Birds of prey forage over large areas and so might be expected to accumulate contaminants which are elevated but heterogeneously distributed in the general environment. The aim of this study was to test the hypothesis that arsenic levels in raptors from a region with elevated environmental arsenic concentrations were higher than those in birds from an uncontaminated part of Britain. Arsenic concentrations in the liver, kidney and muscle of kestrels, Falco tinnunculus, sparrowhawks, Accipiter nisus, and barn owls, Tyto alba, from south-west (SW) England, an area with naturally and anthropogenically (through mining) elevated environmental arsenic concentrations, were compared with those in birds from SW Scotland, where no such geochemical anomaly exists. Arsenic residues in kestrels from SW England were approximately three times greater than those in birds from SW Scotland for the three tissue types analysed. This was not the case for the other species in which arsenic residues were similar in birds from both regions. It is suggested that differences between species in both diet and arsenic metabolism could explain why kestrels have elevated arsenic tissue burdens in response to general environmental contamination but sparrowhawks and barn owls do not.     

Arsenic and mercury bioaccumulation in the aquatic plant, Vallisneria neotropicalis

Arsenic (As) and mercury (Hg) are among the most toxic metals/metalloids. The overall goal of this study was to investigate the bioaccumulation of these trace elements in Vallisneria neotropicalis, a key trophic species in aquatic environments. For this purpose, As and Hg concentrations were determined in sediments and natural populations of V. neotropicalis in sub-estuaries of Mobile Bay (Alabama, USA), differing with respect to past and present anthropogenic impact. Analyses indicate that the Fish River is the most contaminated among the sub-estuaries investigated; levels of As found in Fish River sediments fall within a range that could potentially cause adverse effects in biota. Sediment As concentrations were only moderately correlated with those in V. neotropicalis; no correlation was found between sediment and plant Hg levels. However, several parameters could have masked such potential relationships (e.g., differences in sediment characteristics and “biological dilution” phenomena). Results presented herein highlight the numerous parameters that can influence metal/metalloids accumulation in aquatic plants as well as species-specific responses to trace element contamination. Finally, this study underscores the need for further investigation into contaminant bioaccumulation in ecologically and economically important coastal environments.     

Application of indicator kriging to the complementary use of bioindicators at three trophic levels

The use of biological indicators is widespread in environmental monitoring, although it has long been recognised that each bioindicator is generally associated with a range of potential limitations and shortcomings. To circumvent this problem, this study adopted the complementary use of bioindicators representing different trophic levels and providing different type of information, in an innovative approach to integrate knowledge and to estimate the overall health state of ecosystems. The approach is illustrated using mercury contamination in primary producers (mosses), primary consumers (domestic pigeons and red-legged partridges) and top predators (Bonelli's eagles) in southern Portugal. Indicator kriging geostatistics was used to identify the areas where mercury concentration was higher than the median for each species, and to produce an index that combines mercury contamination across trophic levels. Spatial patterns of mercury contamination were consistent across species. The combined index provided a new level of information useful in incorporating measures of overall environmental contamination into pollution studies.     

Relationships between metal concentrations in great tit nestlings and their environment and food

Metal concentrations (Ag, As, Cd, Cu, Hg, Ni, Pb, Zn) were determined in the feathers and excreta of nestling great tits (Parus major), in their main invertebrate prey (Lepidoptera larvae) and in vegetation samples, all collected from four sites along a pollution gradient. Metal contamination in vegetation samples increased significantly towards the pollution source. The Ag, As, Hg, Ni and Pb concentrations in food samples were significantly higher at the site closest to the pollution source compared to the other three sites. Great tit nestlings from the site closest to the pollution source had significantly higher concentrations of Ag, As, Hg and Pb in their excreta than did nestlings at the other three sites. For five metals (Ag, As, Cu, Ni and Pb), we found concentrations in caterpillars to be significantly positively correlated with vegetation samples. We also found clear significant positive correlations between excreta and caterpillars for Ag, As, Hg and Pb and between feathers and caterpillars for As and Pb. Our data suggest that excreta are a good monitor for the presence and concentrations of non-essential metals in the food and the environment of passerine birds.     

Monitoring of raptors and their contamination levels in Norway

This article summarizes results from raptor monitoring and contamination studies in Norway of the golden eagle, gyrfalcon, white-tailed sea eagle, osprey, peregrine, and merlin. Golden eagle and gyrfalcon populations have been monitored since 1990 as part of the "Monitoring Programme for Terrestrial Ecosystems" (TOV). No long-term trend in the population size or productivity of golden eagle has been shown in any of the 5 study areas. The reproductive output of gyrfalcon is monitored in 3 areas. It is positively correlated with the populations of its main prey species, the rock ptarmigan and the willow ptarmigan. The white-tailed sea eagle population has been monitored since 1974 by the Norwegian Ornithological Society, and the population is increasing. The levels of pesticides and polychlorinated biphenyls are low in the eggs of both the golden eagle and the gyrfalcon, but elevated levels and effects on reproduction have been indicated for a coastal subpopulation of golden eagle. The pollutant levels in white-tailed sea eagle are lower than in the Baltic population of sea eagles, and shell thinning was never severe overall, but individual eggs have contained pollutant concentrations above critical levels. The levels of pollutants in the bird-eating falcons, peregrine, and merlin were higher than in other species. New emerging pollutants, like brominated diphenylethers and perfluorinated organic compounds, could be detected in all species. By incorporating available published and unpublished data, we were able to produce time trends for pollutants and shell thickness over 4 decades.     

Determination of critical pollutant levels in wild populations, examples from organochlorine insecticides in birds of prey

In assessing effects of pollutants on wild organisms, ecological concern is not so much with the protection of individuals, but with the maintenance of self-sustaining populations. Measures of the toxicity of chemicals made under laboratory conditions are thus of limited use when applied to populations in the field. For wild populations the critical level of any pollutant is that level which will lead to population decline (LPD). Among a range of species, this level may bear no consistent relationship to the LD(50) (or LC(50)). In some British birds of prey, whose numbers had been reduced mainly by HEOD poisoning, it was possible to determine the level of HEOD in the birds below which population recovery occurred. For Sparrowhawk and Kestrel, this was equivalent to a geometric mean HEOD level in livers of birds found dead of about 1.0 microg g(-1) (in wet weight). For Peregrines, it was equivalent to a geometric mean HEOD level in addled eggs of 0.7 microg g(-1) (wet weight).     

Recovery of a marker strain of Salmonella typhimurium in litter and aerosols from isolation rooms containing infected chickens

Screening of poultry flocks for foodborne pathogen Salmonella contamination is critical for Salmonella control in preharvest stages of poultry production. In this study, two sampling methods (litter and air filter) were compared for detection of S. typhimurium from experimentally infected chicks some of which had received either a probiotic competitive exclusion culture or transfer of cecal contents from salmonellae-free adult birds. At 4, 9, and 11 days after inoculation, S. typhimurium samples were enumerated by selective plating. For both types of sampling, the control birds yielded the greatest levels of environmental contamination followed by the samples from the probiotic inoculated birds with the birds receiving the cecal transfer culture having the lowest levels of contamination. Although the two sampling methods responded in a similar fashion, detection sensitivity needs to be increased for air filter sampling.     

Variation of heavy metals within and among feathers of birds of prey: effects of molt and external contamination

In this study we examined the effect of external contamination on the heavy metal (Ag, Al, As, Cd, Co, Cr, Cu, Fe, Hg, Mn, Ni, Pb and Zn) concentration in feathers. We compared the heavy metal content among the 10 primary wing feathers of sparrowhawks (Accipiter nisus), little owls (Athene nocta) and barn owls (Tyto alba) and the variation within the outermost tail feather of sparrowhawks and tawny owls (Strix aluco). The concentration of Hg was significantly higher in feathers molted first, suggesting that levels in feathers reflect levels in the blood during formation. For some other elements (Al, Co, Ni, Pb, Zn) on the other hand, there are strong indications that external contamination may have an important impact on the levels detected in the feathers. This should be taken into account in future monitoring studies.     

Mercury contamination in human hair and fish from Cambodia: levels, specific accumulation and risk assessment

Mercury (Hg) concentrations in human hair and fish samples from Phnom Penh, Kien Svay, Tomnup Rolork and Batrong, Cambodia, collected in November 1999 and December 2000 were determined to understand the status of contamination, and age- and sex-dependent accumulation in humans and to assess the intake of mercury via fish consumption. Mercury concentrations in human hair ranged from 0.54 to 190mug/g dry wt. About 3% of the samples contained Hg levels exceeding the no observed adverse effects level (NOAEL) of WHO (50mug/g) and the levels in some hair samples of women also exceeded the NOAEL (10mug/g) associated with fetus neurotoxicity. A weak but significant positive correlation was observed between age and Hg levels in hair of residents. Mercury concentrations in muscle of marine and freshwater fish from Cambodia ranged from <0.01 to 0.96mug/g wet wt. Mercury intake rates were estimated on the basis of the Hg content in fish and daily fish consumption. Three samples of marine fish including sharp-tooth snapper and obtuse barracuda, and one sample of sharp-tooth snapper exceeded the guidelines by US EPA and by Joint FAO/WHO Expert Committee on Food Additives (JECFA), respectively, which indicates that some fish specimens examined (9% and 3% for US EPA and JECFA guidelines, respectively) were hazardous for consumption at the ingestion rate of Cambodian people (32.6g/day). It is suggested that fish is probably the main source of Hg for Cambodian people. However, extremely high Hg concentrations were observed in some individuals and could not be explained by Hg intake from fish consumption, indicating some other contamination sources of Hg in Cambodia.