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 We reviewed and synthesized published and unpublished data on maternal transfer of MeHg in birds.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.

Patterns of mercury and selenium exposure in minnesota common loons.

Common loons (Gavia immer) are at risk of elevated dietary mercury (Hg) exposure in portions of their breeding range. To assess the level of risk among loons in Minnesota (USA), we investigated loon blood Hg concentrations in breeding lakes across Minnesota. Loon blood Hg concentrations were regressed on predicted Hg concentrations in standardized 12-cm whole-organism yellow perch (Perca flavescens), based on fish Hg records from Minnesota lakes, using the US Geological Survey National Descriptive Model for Mercury in Fish. A linear model, incorporating common loon sex, age, body mass, and log-transformed standardized perch Hg concentration representative of each study lake, was associated with 83% of the variability in observed common loon blood Hg concentrations. Loon blood Hg concentration was positively related to standardized perch Hg concentrations; juvenile loons had lower blood Hg concentrations than adult females, and blood Hg concentrations of juveniles increased with body mass. Blood Hg concentrations of all adult common loons and associated standardized prey Hg for all loon capture lakes included in the study were well below proposed thresholds for adverse effects on loon behavior, physiology, survival, and reproductive success. The fish Hg modeling approach provided insights into spatial patterns of dietary Hg exposure risk to common loons across Minnesota. We also determined that loon blood selenium (Se) concentrations were positively correlated with Hg concentration. Average common loon blood Se concentrations exceeded the published provisional threshold. Environ Toxicol Chem 2019;38:524-532. Published 2018 Wiley Periodicals Inc. on behalf of SETAC. This article is a US government work and, as such, is in the public domain in the United States of America.

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.

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.

Hand­rearing, growth, and development of common loon (Gavia immer) chicks.

Common loon chicks were reared in captivity in association with studies to evaluate the effects of radiotransmitter implants and to assess the ecological risk of dietary methylmercury. Here we report on hatching and rearing methods used to successfully raise chicks to 105 days of age. We experienced a 91.5% hatch rate, and 89.6% of loon chicks survived to the end of the study at 105 days. Baseline information on observed rates of fish consumption, behavioral development, and growth patterns are provided. Husbandry techniques are provided that should prove valuable to wildlife rehabilitators caring for abandoned or injured loons, and biologists contemplating methods for restoring loons to areas within their former breeding range.

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.

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.

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.

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.

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.

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 methyl mercury exposure on the growth of juvenile common loons.

We conducted a dose-response laboratory study to quantify the level of mercury exposure associated with negative effects on the development of common loon chicks reared in captivity from hatch to 105 days. A dose regimen was implemented that provided exposure levels that bracketed relevant exposure levels of methyl mercury found in loon chicks across North America. We observed no overt signs of mercury toxicosis and detected no significant effect of dietary mercury exposure on growth or food consumption. However, asymptotic mass was lower in chicks that hatched from eggs collected from nests on low pH lakes relative to eggs from neutral pH lakes. Rapid excretion of methyl mercury during feather growth likely provides loon chicks protection from methyl mercury toxicity and may explain the lack of convincing toxicological findings in this study. Lake-source effects suggest that in ovo exposure to methyl mercury or other factors related to lake pH have consequences on chick development.

The oral bioavailability and toxicokinetics of methylmercury in common loon (Gavia immer) chicks.

We compared the toxicokinetics of methylmercury in captive common loon chicks during two time intervals to assess the impact of feather growth on the kinetics of mercury. We also determined the oral bioavailability of methylmercury during these trials to test for age-related changes. The blood concentration-time curves for individuals dosed during feather development (initiated 35 days post hatch) were best described by a one-compartment toxicokinetic model with an elimination half-life of 3 days. The data for birds dosed following completion of feather growth (84 days post hatch) were best fitted by a two-compartment elimination model that includes an initial rapid distribution phase with a half-life of 0.9 days, followed by a slow elimination phase with a half-life of 116 days. We determined the oral bioavailability of methylmercury during the first dosing interval by comparing the ratios of the area under the blood concentration-time curves (AUC(0--> infinity )) for orally and intravenously dosed chicks. The oral bioavailability of methylmercury during the first dosing period was 0.83. We also determined bioavailability during both dosing periods using a second measure because of irregularities with intravenous results in the second period. This second bioavailability measure estimated the percentage of the dose that was deposited in the blood volume (f), and the results show that there was no difference in bioavailability among dosing periods. The results of this study highlight the importance of feather growth on the toxicokinetics of methylmercury.