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 We reviewed and synthesized published and unpublished data on maternal transfer of MeHg in birds.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

Controls of Methylmercury Bioaccumulation in Forest Floor Food Webs.

Compared to the extensive research on aquatic ecosystems, very little is known about the sources and trophic transfer of methylmercury (MeHg) in terrestrial ecosystems. In this study, we examine energy flow and trophic structure using stable carbon (δ13C) and nitrogen (δ15N) isotope ratios, respectively, and MeHg levels in basal resources and terrestrial invertebrates from four temperate forest ecosystems. We show that MeHg levels in biota increased significantly ( p < 0.01) with δ13C and δ15N at all sites, implying the importance of both microbially processed diets (with increased δ13C) and trophic level (with increased δ15N) at which organisms feed, on MeHg levels in forest floor biota. The trophic magnification slopes of MeHg (defined as the slope of log10MeHg vs δ15N) for these forest floor food webs (0.20-0.28) were not significantly different ( p > 0.05) from those observed for diverse temperate freshwater systems (0.24 ± 0.07; n = 78), demonstrating for the first time the nearly equivalent efficiencies with which MeHg moves up the food chain in these contrasting ecosystem types. Our results suggest that in situ production of MeHg within the forest floor and efficient biomagnification both elevate MeHg levels in carnivorous invertebrates in temperate forests, which can contribute to significant bioaccumulation of this neurotoxin in terrestrial apex predators.

Multi-tissue analyses reveal limited inter-annual and seasonal variation in mercury exposure in an Antarctic penguin community.

Inter-annual variation in tissue mercury concentrations in birds can result from annual changes in the bioavailability of mercury or shifts in dietary composition and/or trophic level. We investigated potential annual variability in mercury dynamics in the Antarctic marine food web using Pygoscelis penguins as biomonitors. Eggshell membrane, chick down, and adult feathers were collected from three species of sympatrically breeding Pygoscelis penguins during the austral summers of 2006/2007-2010/2011. To evaluate the hypothesis that mercury concentrations in penguins exhibit significant inter-annual variation and to determine the potential source of such variation (dietary or environmental), we compared tissue mercury concentrations with trophic levels as indicated by δ(15)N values from all species and tissues. Overall, no inter-annual variation in mercury was observed in adult feathers suggesting that mercury exposure, on an annual scale, was consistent for Pygoscelis penguins. However, when examining tissues that reflected more discrete time periods (chick down and eggshell membrane) relative to adult feathers, we found some evidence of inter-annual variation in mercury exposure during penguins' pre-breeding and chick rearing periods. Evidence of inter-annual variation in penguin trophic level was also limited suggesting that foraging ecology and environmental factors related to the bioavailability of mercury may provide more explanatory power for mercury exposure compared to trophic level alone. Even so, the variable strength of relationships observed between trophic level and tissue mercury concentrations across and within Pygoscelis penguin species suggest that caution is required when selecting appropriate species and tissue combinations for environmental biomonitoring studies in Antarctica.

Pattern of mercury allocation into egg components is independent of dietary exposure in Gentoo penguins.

Avian eggs have become one of the most common means of evaluating mercury contamination in aquatic and marine environments and can serve as reliable indicators of dietary mercury exposure. We investigated patterns of mercury deposition into the major components of penguin eggs (shell, membrane, albumen, and yolk) using the Gentoo penguin (Pygoscelis papua) as a model species. Eggs were collected from both wild and captive populations of Gentoo penguins to compare the allocation of mercury into individual egg components of birds feeding at disparate trophic positions as inferred by stable isotope analysis. Mercury concentrations in captive penguins were an order of magnitude higher than in wild birds, presumably because the former were fed only fish at a higher trophic position relative to wild penguins that fed on a diet of 72-93% krill (Euphausia spp.). Similar to previous studies, we found the majority of total egg mercury sequestered in the albumen (92%) followed by the yolk (6.7%) with the lowest amounts in the shell (0.9%) and membrane (0.4%). Regardless of dietary exposure, mercury concentrations in yolk and membrane, and to a lesser degree shell, increased with increasing albumen mercury (used as a proxy for whole-egg mercury), indicating that any component, in the absence of others, may be suitable for monitoring changes in dietary mercury. Because accessibility of egg tissues in the wild varies, the establishment of consistent relationships among egg components will facilitate comparisons with any other study using eggs to assess dietary exposure to mercury.

Mercury exposure driven by geographic and trophic factors in Magellanic penguins from Tierra del Fuego.

Penguins accumulate mercury due to their long-life span together with their high trophic position. We sampled adult and juveniles' feathers from three colonies of Spheniscus magellanicus from Tierra del Fuego along an inshore-offshore corridor. We integrated toxicological information (mercury concentrations) and foraging biomarkers (δ13C, δ15N) into a common data analysis framework (isotopic niche analysis) to evaluate the influence of age, location, and foraging behaviors on mercury concentrations. Adults had higher feather mercury concentrations, δ13C, and δ15N values compared to juveniles. Also, adult and juvenile feather mercury concentrations differed between colonies, with lower mercury concentrations at the nearest inshore colony relative to the farther offshore colonies. Trophic position and the isotopic niche analyses suggest that this geographic gradient in mercury concentrations is due to differences in colonies' foraging areas. Understanding penguins' exposure to mercury derived from local food webs is a crucial first step in evaluating the impacts of this heavy metal on their conservation status.

Mercury exposure and survival in free-living tree swallows (Tachycineta bicolor).

Mercury has become a ubiquitous contaminant in food chains worldwide. A large body of literature detailing bioaccumulation and effects on birds has revealed the potential for mercury to adversely impact avian physiology and reproduction. However, the extent to which these effects impair survival remains poorly understood. The objective of this study was to determine whether mercury exposure was associated with reduced annual survivorship in tree swallows (Tachycineta bicolor) breeding at a site with legacy industrial contamination. From 2005 to 2008, we captured and marked 932 adult swallows. We used Cormack-Jolly-Seber models and an information-theoretic approach to test our hypotheses that adult survival varied by sex, breeding location, and cumulative individual mercury exposure. Blood mercury was significantly elevated on contaminated sites (2005-2007 combined mean ± SE: 2.84 ± 0.09 µg/g; reference: 0.17 ± 0.01 µg/g). Model-averaged estimates of female apparent survival ranged from 0.483 to 0.488 on reference sites and 0.473 to 0.477 on contaminated sites. For males, apparent survival ranged from 0.451 to 0.457 on reference sites and 0.444 to 0.448 on contaminated sites. Thus, we observed approximately a 1% difference in survival between mercury-contaminated and reference sites. Such a small difference is unlikely to impact population viability in this short-lived species; however, some songbirds accumulate mercury to a greater degree than tree swallows and do not possess the migratory behavior that removes swallows to less contaminated areas for the majority of the year. Identifying whether such species are at risk of suffering biologically significant reductions in survival should become a focus of future research.

Relationship between laying sequence and mercury concentration in tree swallow eggs.

When female birds lay eggs, some of their body burden of mercury is eliminated into each egg, potentially leading to declining mercury across the clutch. However, there was no decline in mercury with laying sequence in clutches of tree swallow (Tachycineta bicolor) eggs at a mercury-contaminated site, presumably due to daily replenishment of mercury in females during laying. Sampling just one egg from the nest provided an accurate measure of clutch mercury contamination.

Differing foraging strategies influence mercury (Hg) exposure in an Antarctic penguin community.

Seabirds are ideal model organisms to track mercury (Hg) through marine food webs as they are long-lived, broadly distributed, and are susceptible to biomagnification due to foraging at relatively high trophic levels. However, using these species as biomonitors requires a solid understanding of the degree of species, sexual and age-specific variation in foraging behaviors which act to mediate their dietary exposure to Hg. We combined stomach content analysis along with Hg and stable isotope analyses of blood, feathers and common prey items to help explain inter and intra-specific patterns of dietary Hg exposure across three sympatric Pygoscelis penguin species commonly used as biomonitors of Hg availability in the Antarctic marine ecosystem. We found that penguin tissue Hg concentrations differed across species, between adults and juveniles, but not between sexes. While all three penguins species diets were dominated by Antarctic krill (Euphausia superba) and to a lesser extent fish, stable isotope based proxies of relative trophic level and krill consumption could not by itself sufficiently explain the observed patterns of inter and intra-specific variation in Hg. However, integrating isotopic approaches with stomach content analysis allowed us to identify the relatively higher risk of Hg exposure for penguins foraging on mesopelagic prey relative to congeners targeting epipelagic or benthic prey species. When possible, future seabird biomonitoring studies should seek to combine isotopic approaches with other, independent measures of foraging behavior to better account for the confounding effects of inter and intra-specific variation on dietary Hg exposure.

A comprehensive assessment of mercury exposure in penguin populations throughout the Southern Hemisphere: Using trophic calculations to identify sources of population-level variation.

The wide geographic distribution of penguins (Order Sphenisciformes) throughout the Southern Hemisphere provided a unique opportunity to use a single taxonomic group as biomonitors of mercury among geographically distinct marine ecosystems. Mercury concentrations were compared among ten species of penguins representing 26 geographically distinct breeding populations. Mercury concentrations were relatively low (⩽2.00ppm) in feathers from 18/26 populations considered. Population-level differences in trophic level explained variation in mercury concentrations among Little, King, and Gentoo penguin populations. However, Southern Rockhopper and Magellanic penguins breeding on Staten Island, Tierra del Fuego, had the highest mercury concentrations relative to their conspecifics despite foraging at a lower trophic level. The concurrent use of stable isotope and mercury data allowed us to document penguin populations at the greatest risk of exposure to harmful concentrations of mercury as a result of foraging at a high trophic level or in geographic 'hot spots' of mercury availability.

Trophic calculations reveal the mechanism of population-level variation in mercury concentrations between marine ecosystems: case studies of two polar seabirds.

The incorporation of quantitative trophic level analysis in ecotoxicological studies provides explanatory power to identify the factors, trophic or environmental, driving population-level variation in mercury exposure at large geographic scales. In the Antarctic marine ecosystem, mercury concentrations and stable isotope values in Adélie penguins (Pygoscelis adeliae) were compared between the Antarctic Peninsula and the Ross Sea. Correcting tissue δ(15)N values for baseline δ(15)N values revealed population-level differences in trophic position which contributes to differences in mercury. Data from Thick-billed murres (Uria lomvia) were synthesized from published values from Baffin Bay and Svalbard to demonstrate the utility of baseline δ(15)N values in identifying differences in environmental mercury exposure independent of diet. Here, we demonstrate the importance of calculating population-specific trophic level data to uncover the source of variation in mercury concentrations between geographically distinct populations of marine predators.

Unique pattern of molt leads to low intraindividual variation in feather mercury concentrations in penguins.

The authors hypothesized that the catastrophic annual molt of penguins (Sphenisciformes) would lead to reduced intraindividual variation of mercury concentrations in body feathers. While mean mercury concentrations varied significantly among 8 penguin species, intraindividual variability did not differ among species and was 3 times lower than values observed in other seabirds. The findings of the present study suggest that a single body feather collected at random per individual can be adequate to estimate mercury exposure at the population level in penguins.

Penguin eggshell membranes reflect homogeneity of mercury in the marine food web surrounding the Antarctic Peninsula.

Remote regions such as the Antarctic have become increasingly important for investigations into far-reaching anthropogenic impacts on the environment, most recently in regard to the global mercury cycle. Spatial patterns of mercury availability in four regions of the Antarctic Peninsula were investigated using three species of sympatrically breeding Pygoscelis penguins as biomonitors. Eggshells with intact membranes from Adélie, Gentoo, and Chinstrap penguins were collected at 24 breeding colonies in the South Orkney Islands, South Shetland Islands, eastern Antarctic Peninsula, and western Antarctic Peninsula during the 2006/2007 austral summer. In addition, we compared eggshell membrane mercury concentrations with eggshell stable isotope values (δ(15)N and δ(13)C) to determine if species-specific trophic or foraging habitat preferences influenced female mercury exposure prior to breeding. With few exceptions, mercury concentrations were found to be fairly homogeneous throughout the Antarctic Peninsula suggesting little spatial variation in the risk of exposure to dietary mercury in this food web. Mercury concentrations in Gentoo and Adélie penguins were similar while Chinstrap penguins tended to have higher eggshell membrane mercury concentrations than their congeners. However, inter and intra-specific differences in eggshell membrane mercury concentration were not related to eggshell δ(15)N or δ(13)C values, a likely result of all three species foraging at similar trophic positions. The lack of regional-scale differences in mercury availability in this marine ecosystem may be a reflection of generally uniform atmospheric deposition and upwelling of regionally homogeneous deep water rather than from geographically distinct point sources.

Effects of mercury exposure on the reproductive success of tree swallows (Tachycineta bicolor).

An experimental tree swallow population was established in the headwaters of the Shenandoah River, Virginia, USA to assess the accumulation and effects of mercury contamination on birds that eat emergent aquatic insects. One tributary, the South River, was contaminated with mercury before 1950. Reproductive success of swallows nesting within 50 m of this river was compared to that of three uncontaminated reference tributaries in 2005 and 2006. Female swallows on the contaminated stretch of river had significantly elevated blood and feather total mercury (blood: 3.56 +/- 2.41 ppm ww vs. 0.17 +/- 0.15 ppm reference; feather: 13.55 +/- 6.94 ppm vs. 2.34 +/- 0.87 ppm reference), possibly the highest ever reported for an insectivorous songbird. Insects collected by the swallows to be fed to nestlings averaged 0.97 +/- 1.11 ppm dw total mercury, significantly higher than on reference sites. Swallows in the contaminated area produced fewer fledglings than those in reference areas. The effect of mercury contamination on productivity was detectable only for young females in the contaminated area that were breeding for the first time in 2006, a segment of the population that may already have been stressed by inexperience. Tree swallows served as practical and effective biomonitors for mercury levels and effects and have great potential as proxy biomonitors for more logistically challenging birds such as loons or eagles.

The movement of aquatic mercury through terrestrial food webs.

Mercury has contaminated rivers worldwide, with health consequences for aquatic organisms and humans who consume them. Researchers have focused on aquatic birds as sentinels for mercury. However, trophic transfer between adjacent ecosystems could lead to the export of aquatic mercury to terrestrial habitats. Along a mercury-contaminated river in Virginia, United States, terrestrial birds had significantly elevated levels of mercury in their blood, similar to their aquatic-feeding counterparts. Diet analysis revealed that spiders delivered much of the dietary mercury. We conclude that aquatic mercury pollution can move into terrestrial habitats, where it biomagnifies to levels in songbirds that may cause adverse effects. Rivers contaminated with mercury may pose a threat to the many bird species that feed on predatory invertebrates in adjacent riparian habitats.