Synthesis of Maternal Transfer of Mercury in Birds: Implications for Altered Toxicity Risk.

Maternal transfer is a predominant route of methylmercury (MeHg) exposure to offspring. We reviewed and synthesized published and unpublished data on maternal transfer of MeHg in birds. Using paired samples of females' blood (n = 564) and their eggs (n = 1814) from 26 bird species in 6 taxonomic orders, we conducted a meta-analysis to evaluate whether maternal transfer of MeHg to eggs differed among species and caused differential toxicity risk to embryos. Total mercury (THg) concentrations in eggs increased with maternal blood THg concentrations; however, the proportion of THg transferred from females to their eggs differed among bird taxa and with maternal THg exposure. Specifically, a smaller proportion of maternal THg was transferred to eggs with increasing female THg concentrations. Additionally, the proportion of THg that was transferred to eggs at the same maternal blood THg concentration differed among taxonomic orders, with waterfowl (Anseriformes) transferring up to 382% more THg into their eggs than songbirds (Passeriformes). We provide equations to predict THg concentrations in eggs using female blood THg concentrations, and vice versa, which may help translate toxicity benchmarks across tissues and life stages. Our results indicate that toxicity risk of MeHg can vary among bird taxa due to differences in maternal transfer of MeHg to offspring.

Mercury correlates with altered corticosterone but not testosterone or estradiol concentrations in common loons.

We investigated the relation between environmental mercury exposure and corticosterone concentrations in free-living adult common loons (Gavia immer). We determined blood and feather mercury concentrations and compared them to testosterone, estradiol, and stress-induced plasma corticosterone concentrations. Although neither testosterone nor estradiol correlated with Hg levels, there was a robust positive relation between blood Hg and stress-induced corticosterone concentrations in males, but not in females. The lack of an effect in females may have been due to overall less contamination in females. There were no significant correlations between feather Hg and stress-induced corticosterone in either sex. To help determine whether Hg had a causal effect on corticosterone, we investigated the impact of experimental Hg intake on the corticosterone stress response in captive juvenile loons. Juveniles were subjected to three different feeding regimes: 0, 0.4 and 1.2µg Hg (as MeHgCL)/g wet weight (ww) fish. We then measured baseline and 30min post-solitary confinement stressor corticosterone concentrations. The Hg fed chicks exhibited a decreased ability to mount a stress response. From these data, we conclude that Hg contamination does appear to alter the corticosterone response to stress, but not in a consistent predictable pattern. Regardless of the direction of change, however, exposure to mercury contamination and the resulting impact on the corticosterone stress response in common loons may substantially impact health, fitness and survival.

Climate change surpasses land-use change in the contracting range boundary of a winter-adapted mammal.

The effects of climate change on biodiversity have emerged as a dominant theme in conservation biology, possibly eclipsing concern over habitat loss in recent years. The extent to which this shifting focus has tracked the most eminent threats to biodiversity is not well documented. We investigated the mechanisms driving shifts in the southern range boundary of a forest and snow cover specialist, the snowshoe hare, to explore how its range boundary has responded to shifting rates of climate and land cover change over time. We found that although both forest and snow cover contributed to the historical range boundary, the current duration of snow cover best explains the most recent northward shift, while forest cover has declined in relative importance. In this respect, the southern range boundary of snowshoe hares has mirrored the focus of conservation research; first habitat loss and fragmentation was the stronger environmental constraint, but climate change has now become the main threat. Projections of future range shifts show that climate change, and associated snow cover loss, will continue to be the major driver of this species' range loss into the future.

Patterns and trends in brominated flame retardants in bald eagle nestlings from the upper midwestern United States.

We report on patterns and trends in polybrominated diphenyl ethers (PBDEs) in the plasma of 284 bald eagle nestlings sampled between 1995 and 2011 at six study areas in the upper Midwestern United States. Geometric mean concentrations of total PBDEs (Σ of nine congeners) ranged from 1.78 ng/mL in the upper St. Croix River watershed to 12.0 ng/mL on the Mississippi River. Lake Superior nestlings fell between these two extremes. Between 2006 and 2011, trends differed among study areas with three declining, two remaining stable, and one increasing. Variation in ΣPBDE trends among study areas was linked to trends in individual congeners. The lower brominated PBDEs (BDE-47, -99, and -100) declined 4-10% while the higher brominated congeners (BDE-153 and -154) increased by about 7.0% annually from 2006 to 2011. This increase was the greatest in nestlings from the St. Croix River and below its confluence with the Mississippi River. Region-wide, our data suggest ΣPBDEs increased in bald eagle nestlings from 1995 through the mid-2000s and then declined by 5.5% annually from 2006 to 2011. These regional trends are consistent with the removal of penta- and octa-PBDEs from the global market.

Can settlement in natal-like habitat explain maladaptive habitat selection?

The study of habitat selection has long been influenced by the ideal free model, which maintains that young adults settle in habitat according to its inherent quality and the density of conspecifics within it. The model has gained support in recent years from the finding that conspecifics produce cues inadvertently that help prebreeders locate good habitat. Yet abundant evidence shows that animals often fail to occupy habitats that ecologists have identified as those of highest quality, leading to the conclusion that young animals settle on breeding spaces by means not widely understood. Here, we report that a phenomenon virtually unknown in nature, natal habitat preference induction (NHPI), is a strong predictor of territory settlement in both male and female common loons (Gavia immer). NHPI causes young animals to settle on natal-like breeding spaces, but not necessarily those that maximize reproductive success. If widespread, NHPI might explain apparently maladaptive habitat settlement.

Bi-phasic trends in mercury concentrations in blood of Wisconsin common loons during 1992-2010.

We assessed the ecological risk of mercury (Hg) in aquatic systems by monitoring common loon (Gavia immer) population dynamics and blood Hg concentrations. We report temporal trends in blood Hg concentrations based on 334 samples collected from adults recaptured in subsequent years (resampled 2-9 times) and from 421 blood samples of chicks collected at lakes resampled 2-8 times 1992-2010. Temporal trends were identified with generalized additive mixed effects models and mixed effects models to account for the potential lack of independence among observations from the same loon or same lake. Trend analyses indicated that Hg concentrations in the blood of Wisconsin loons declined over the period 1992-2000, and increased during 2002-2010, but not to the level observed in the early 1990s. The best fitting linear mixed effects model included separate trends for the two time periods. The estimated trend in Hg concentration among the adult loon population during 1992-2000 was -2.6% per year, and the estimated trend during 2002-2010 was +1.8% per year; chick blood Hg concentrations decreased -6.5% per year during 1992-2000, but increased 1.8% per year during 2002-2010. This bi-phasic pattern is similar to trends observed for concentrations of methylmercury and SO(4) in lake water of an intensely studied seepage lake (Little Rock Lake, Vilas County) within our study area. A cause-effect relationship between these independent trends is hypothesized.

Effects of injected methylmercury on the hatching of common loon (Gavia immer) eggs.

To determine the level of in ovo methylmercury (MeHg) exposure that results in detrimental effects on fitness and survival of loon embryos and hatched chicks, we conducted a field study in which we injected eggs with various doses of MeHg on day 4 of incubation. Eggs were collected following about 23 days of natural incubation and artificially incubated to observe hatching. Reduced embryo survival was evident in eggs injected at a rate of ≥1.3 µg Hg/g wet-mass. When maternally deposited Hg and injected Hg were considered together, the median lethal concentration of Hg (LC(50)) was estimated to be 1.78 µg Hg/g wet-mass. Organ mass patterns from eggs of chicks injected at a rate of 2.9 µg Hg/g differed from that of controls and chicks from the 0.5 µg Hg/g treatment, largely related to a negative relation between yolk sac mass and egg mercury concentration. Chicks from eggs in the 2.9 µg Hg/g treatment were also less responsive to a frightening stimulus than controls and chicks from the 0.5 µg Hg/g treatment. We also found that the length of incubation period increased with increasing egg mercury concentration. Tissue Hg concentrations were strongly associated (r(2) ≥ 0.80) with egg Hg concentration.

Spatial gradients of methylmercury for breeding common loons in the Laurentian Great Lakes region.

Much of the Laurentian Great Lakes region is a mercury-sensitive landscape, in which atmospheric deposition and waterborne sources of mercury (Hg) have led to high concentrations of bioavailable methylmercury (MeHg) in predatory fish and piscivorous wildlife. Efforts since the early 1990s have established the common loon (Gavia immer) as the primary avian indicator for evaluating the exposure and effects of MeHg in North America. A regional Hg dataset was compiled from multiple loon tissue types and yellow perch (Perca flavescens), a preferred prey fish species for loons. Hg exposure in loons and perch was modeled to develop male and female loon units (MLU and FLU, respectively), standardized metrics that represent the estimated blood Hg exposure of a male or female loon for a given loon territory or water body. Using this common endpoint approach to assess loon Hg exposure, the authors demonstrate spatial trends in biotic Hg concentrations, examine MeHg availability in aquatic ecosystems of the Great Lakes region in relation to landscape-level characteristics, and identify areas with potentially significant adverse reproductive impacts to loons and other avian piscivores. Based on 8,101 MLUs, seven biological Hg hotspots were identified in the Great Lakes region. Policy-relevant applications are presented.

Patterns and Trends of Polybrominated Diphenyl Ethers in Bald Eagle Nestlings in Minnesota and Wisconsin, USA.

We measured concentrations of up to 17 polybrominated diphenyl ethers (PBDEs) in plasma of 492 bald eagle (Haliaeetus leucocephalus) nestlings between 1995 and 2017 from 12 study areas in Wisconsin and Minnesota, USA. Geometric mean concentrations of the sum of 9 PBDE congeners (∑PBDE) measured across all years ranged from 2.88 to 10.8 µg/L, and nestlings in urban areas had higher concentrations than those in remote locations. Region-wide from 2006 through 2017, we found that ∑PBDEs declined by 3.8% annually and congeners BDE-47, -99, and -100 declined by 5.6 to 6.5%, whereas BDE-153 and -154 had no significant declines. When categorized by waterbody type, nestlings from Great Lakes and river study areas had higher concentrations of ∑PBDEs than those at inland lakes, but river study areas spanned the extremes. From 2006 to 2017, ∑PBDEs declined by 7.3% annually in Great Lakes nestlings and by 3.2% in nestlings along rivers, and increased by 32.7% at inland lakes. Using a longer dataset (1995-2015), we found that ∑PBDEs declined in Lake Superior nestlings by 3.3% annually. Our results show that PBDEs declined in bald eagle nestling plasma in most study areas since PBDE production was reduced, but that concentrations remain high near urban centers and that trends differ by congener, study area, and waterbody type. Environ Toxicol Chem 2021;40:1606-1618. © 2021 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Effects of methylmercury exposure on the behavior of captive-reared common loon (Gavia immer) chicks.

Behavioral effects resulting from exposure to dietary methylmercury (MeHg) have been reported in studies of several wildlife species. However, quantifying the impact of contaminant exposure on wild populations is complicated by the confounding effects of other environmental stressors. We controlled confounding stressors in a laboratory study to quantify the level of dietary MeHg exposure associated with negative effects on the fitness of captive-reared common loon (Gavia immer) chicks. We evaluated the effect of MeHg on loon chick behavior by employing several assays, including measures of righting reflexes, responsiveness to taped parental calls, reaction to frightening stimuli, and estimates of time activity budgets. Evidence suggested that as chicks aged, those exposed to nominal dietary dose levels of 0.4 and 1.2 microg Hg/g wet-weight in food (average estimated delivered dietary level of 0.55 and 1.94 microg Hg/g, respectively) were less likely (p < 0.01) to right themselves after being positioned on their backs during outdoor trials (> or =37 days old) compared to chicks on the control diet. We detected differences (p < 0.05) in several response variables with respect to source of eggs. Chicks from nests on low-pH lakes tended to spend more time on resting platforms, spent less time in the shade, were more likely to walk across a platform upon release and do it quicker, were less responsive to a frightening stimulus, and exhibited less intense response to parental wail calls than did chicks from neutral pH-lakes. Rapid MeHg excretion during feather growth likely provides loon chicks protection from MeHg toxicity and may explain the lack of behavioral differences with dietary intake. Lake source effects suggest that in ovo exposure to MeHg or other factors related to lake pH have consequences on chick behavior.

Distribution and accumulation of mercury in tissues of captive-reared common loon (Gavia immer) chicks.

We determined the distribution and accumulation of Hg in tissues of common loon (Gavia immer) chicks maintained for up to 15 weeks on either a control diet with no added methylmercury chloride (MeHgCl) or one containing either 0.4 or 1.2 microg Hg (as MeHgCl)/g wet-weight food. Total Hg and MeHg tissue concentrations were strongly positively correlated (r2 > 0.95) with the amount of Hg delivered to individual chicks throughout the course of the experiment. The pattern of differential Hg concentration in internal tissues was consistent within each treatment: Liver > kidney > muscle > carcass > brain. Feather Hg concentrations were consistently higher than those of internal tissues and represented an important route of Hg elimination. Feather mass accounted for 4.3% +/- 0.1% (average +/- standard error) of body mass, yet 27.3% +/- 2.6% of total Hg intake was excreted into feathers. Our calculations indicate that 26.7% +/- 4.9% of ingested Hg was not accounted for and, thus, either was never absorbed or was absorbed and subsequently eliminated in feces. With the additional excretion into feathers, 54% of ingested Hg was excreted. Demethylation was evident in the liver at all treatment levels and in the kidneys of chicks dosed at 1.2 microg Hg/g. Mercury concentrations were strongly positively correlated (r2 > or = 0.95) among internal tissues and with blood Hg concentration. Mercury concentrations of secondary feathers were moderately correlated (r2 = 0.82-0.93) with internal tissues. We supply regression models that may be used to provide perspective and a useful means of interpreting the variety of measures of Hg exposure reported in the literature.

Bioenergetic and pharmacokinetic model for exposure of common loon (Gavia immer) chicks to methylmercury.

A bioenergetics model was used to predict food intake of common loon (Gavia immer) chicks as a function of body mass during development, and a pharmacokinetics model, based on first-order kinetics in a single compartment, was used to predict blood Hg level as a function of food intake rate, food Hg content, body mass, and Hg absorption and elimination. Predictions were tested in captive growing chicks fed trout (Salmo gairdneri) with average MeHg concentrations of 0.02 (control), 0.4, and 1.2 microg/g wet mass (delivered as CH3HgCl). Predicted food intake matched observed intake through 50 d of age but then exceeded observed intake by an amount that grew progressively larger with age, reaching a significant overestimate of 28% by the end of the trial. Respiration in older, nongrowing birds probably was overestimated by using rates measured in younger, growing birds. Close agreement was found between simulations and measured blood Hg, which varied significantly with dietary Hg and age. Although chicks may hatch with different blood Hg levels, their blood level is determined mainly by dietary Hg level beyond approximately two weeks of age. The model also may be useful for predicting Hg levels in adults and in the eggs that they lay, but its accuracy in both chicks and adults needs to be tested in free-living birds.

Effects of methylmercury exposure on the immune function of juvenile common loons (Gavia immer).

We conducted a dose-response laboratory study to quantify the level of exposure to dietary Hg, delivered as methylmercury chloride (CH3HgCl), that is associated with suppressed immune function in captive-reared common loon (Gavia immer) chicks. We used the phytohemagglutinin (PHA) skin test to assess T-lymphocyte function and the sheep red blood cell (SRBC) hemagglutination test to measure antibody-mediated immunity. The PHA stimulation index among chicks receiving dietary Hg treatment did not differ significantly from those of chicks on the control diet (p = 0.15). Total antibody (immunoglobulin [Ig] M [primary antibody] + IgG [secondary response]) production to the SRBC antigen in chicks treated with dietary methylmercury (MeHg), however, was suppressed (p = 0.04) relative to chicks on control diets. Analysis indicated suppression of total Ig production (p = 0.025 with comparisonwise alpha level = 0.017) between control and 0.4 microg Hg/g wet food intake treatment groups. Furthermore, the control group exhibited a higher degree of variability in antibody response compared to the Hg groups, suggesting that in addition to reducing the mean response, Hg treatment reduced the normal variation attributable to other biological factors. We observed bursal lymphoid depletion in chicks receiving the 1.2 microg Hg/g treatment (p = 0.017) and a marginally significant effect (p = 0.025) in chicks receiving the 0.4 microg Hg/g diet. These findings suggest that common loon chick immune systems may be compromised at an ecologically relevant dietary exposure concentration (0.4 microg Hg/g wet wt food intake). We also found that chicks hatched from eggs collected from low-pH lakes exhibited higher levels of lymphoid depletion in bursa tissue relative to chicks hatched from eggs collected from neutral-pH lakes.

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.

Influence of in ovo mercury exposure, lake acidity, and other factors on common loon egg and chick quality in Wisconsin.

A field study was conducted in Wisconsin (USA) to characterize in ovo mercury (Hg) exposure in common loons (Gavia immer). Total Hg mass fractions ranged from 0.17 µg/g to 1.23 µg/g wet weight in eggs collected from nests on lakes representing a wide range of pH (5.0-8.1) and were modeled as a function of maternal loon Hg exposure and egg laying order. Blood total Hg mass fractions in a sample of loon chicks ranged from 0.84 µg/g to 3.86 µg/g wet weight at hatch. Factors other than mercury exposure that may have persistent consequences on development of chicks from eggs collected on low-pH lakes (i.e., egg selenium, calcium, and fatty acid mass fractions) do not seem to be contributing to reported differences in loon chick quality as a function of lake pH. However, it was observed that adult male loons holding territories on neutral-pH lakes were larger on average than those occupying territories on low-pH lakes. Differences in adult body size of common loons holding territories on neutral-versus low-pH lakes may have genetic implications for differences in lake-source-related quality (i.e., size) in chicks. The tendency for high in ovo Hg exposure and smaller adult male size to co-occur in low-pH lakes complicates the interpretation of the relative contributions of each to resulting chick quality.

Associations between regional differences in polychlorinated biphenyls and dichlorodiphenyldichloroethylene in blood of nestling bald eagles and reproductive productivity.

The relationship between regional reproduction rates of bald eagles (Haliaeetus leucocephalus) and concentrations of p.p'-dichlorodiphenyldichloroethylene (p,p'-DDE) and total polychlorinated biphenyls (PCBs) in blood plasma from nestling bald eagles was assessed. Blood was analyzed from 309 nestlings from 10 subpopulations of eagles across the Great Lakes region. Geometric mean concentrations of p,p'-DDE and total PCBs were inversely correlated to the productivity and success rates of nesting bald eagles within nine subpopulations. Nestlings eight weeks of age and older had significantly greater geometric mean concentrations of total PCBs and p,p'-DDE than nestlings less than eight weeks of age. The ability to use measurements of p,p'-DDE and total PCBs in nestling blood to determine the potential impact of these contaminants on adult nesting on a regional scale was demonstrated.

Mercury and other element exposure in tree swallows nesting at low pH and neutral pH lakes in northern Wisconsin USA.

The primary objective of this study was to determine whether tree swallows (Tachycineta bicolor) demonstrate similar responses to lake pH and mercury (Hg) contamination in northern Wisconsin as do common loons (Gavia immer). Similar to common loons, Hg concentrations in the blood of tree swallow nestlings were higher, Hg concentrations in eggs tended to be higher, and egg size tended to be smaller at low (<6.2) pH lakes. In contrast to common loons, tree swallow nestling production was not lower at low pH lakes. Based on modeling associations, Hg concentrations in tree swallow eggs and nestling blood can be used to predict Hg concentrations in common loons without the invasive or destructive sampling of loons. Mean concentrations of cadmium, manganese, and mercury in nestling livers were higher at low pH lakes than neutral pH lakes. Concentrations of cadmium, chromium, mercury, selenium, and zinc were not at toxic levels.

Methylmercury exposure associated with reduced productivity in common loons.

Methylmercury can impair the reproduction of fish-eating wildlife. We measured lake pH, mercury (Hg) concentrations in small fish, blood Hg levels in adult male, female and juvenile common loons, and loon productivity from 120 lakes in Wisconsin, USA and New Brunswick and Nova Scotia, Canada (Maritimes). Mean lake pH was higher in Wisconsin than in the Maritimes. Body masses of adult loons and Hg concentrations in the blood of loons and in small fish were greater in the Maritimes. Hg levels in fish increased with lake acidity. Abundance of small fish increased in acidic lakes in the Maritimes. Blood Hg concentrations in adult and juvenile loons decreased with lake pH and increased with Hg levels in fish prey. Hg levels in male, female and juvenile loons were 22, 16 and 2.3 times greater than those in small fish. Loon Hg exposure, measured either as Hg levels in female loon blood or in fish prey, appeared to impose an upper limit on loon productivity. Loon productivity decreased as Hg exposure increased. Quantile regression analysis indicated that maximum observed loon productivity dropped 50% when fish Hg levels were 0.21 ug/g (wet wt), and failed completely when fish Hg concentrations were 0.41 ug/g.

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 microg Hg/g and 0.4 microg Hg/g, an ecologically relevant dietary mercury level, but not at 0.08 microg 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.