Differential reliance on aquatic prey subsidies influences mercury exposure in riparian arachnids and songbirds.

Cross-ecosystem subsidies move substantial amounts of nutrients between ecosystems. Emergent aquatic insects are a particularly important prey source for riparian songbirds but may also move aquatic contaminants, such as mercury (Hg), to riparian food webs. While many studies focus on species that eat primarily emergent aquatic insects, we instead study riparian songbirds with flexible foraging strategies, exploiting both aquatic and terrestrial prey sources. The goal in this study is to trace reliance on aquatic prey sources and correlate it to Hg concentrations in common riparian arachnids (Families Tetragnathidae, Opiliones, and Salticidae) and songbirds (Common Yellowthroat Geothlypis trichas, Spotted Towhee Pipilo maculatus, Swainson's Thrush Catharus ustulatus, Song Sparrow Melospiza melodia, and Yellow Warbler Setophaga petechia). We used stable isotopes of δ13C and δ15N and Bayesian mixing models in MixSIAR to determine the reliance of riparian predators on aquatic prey sources. Using mixed effects models, we found that arachnid families varied in their reliance on aquatic prey sources. While songbird species varied in their reliance on aquatic prey sources, songbirds sampled earlier in the season consistently relied more on aquatic prey sources than those sampled later in the season. For both arachnids and songbirds, we found a positive correlation between the amount of the aquatic prey source in their diet and their Hg concentrations. While the seasonal pulse of aquatic prey to terrestrial ecosystems is an important source of nutrients to riparian species, our results show that aquatic prey sources are linked with higher Hg exposure. For songbirds, reliance on aquatic prey sources early in the breeding season (and subsequent higher Hg exposure) coincides with timing of egg laying and development, both of which may be impacted by Hg exposure.

Correction to: Spatial variation in aquatic invertebrate and riparian songbird mercury exposure across a river-reservoir system with a legacy of mercury contamination.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Historical patterns in mercury exposure for North American songbirds.

Methylmercury (MeHg) is a global environmental contaminant that poses significant risks to the health of humans, wildlife, and ecosystems. Assessing MeHg exposure in biota across the landscape and over time is vital for monitoring MeHg pollution and gauging the effectiveness of regulations intended to reduce new mercury (Hg) releases. We used MeHg concentrations measured in museum specimen feathers (collected between 1869 and 2014) and total Hg concentrations (as a proxy for MeHg) of feathers sampled from wild birds (collected between 2008 and 2017) to investigate temporal patterns in exposure over approximately 150 years for North American songbirds. For individual species, we found greater concentrations for samples collected post-2000 compared to those collected during historic times (pre-1900) for six of seven songbird species. Mean feather concentrations measured in samples collected post-2000 ranged between 1.9 and 17 times (mean 6.6) greater than historic specimens. The proportion of individual songbirds with feather concentrations that exceeded modeled toxicity benchmarks increased in samples collected after 1940. Only 2% of individual songbirds collected prior to 1940 had feather concentrations greater than 2.4 µg/g (a toxicity benchmark related to a 10% decrease in nest success) compared to 35% of individuals collected post-1940. Many species included in this study have a vulnerable or near-threatened conservation status, suggesting recovery actions are needed to address mercury pollution.

Spatial variation in aquatic invertebrate and riparian songbird mercury exposure across a river-reservoir system with a legacy of mercury contamination.

Mercury (Hg) loading and methylation in aquatic systems causes a variety of deleterious effects for fish and wildlife populations. Relatively little research has focused on Hg movement into riparian food webs and how this is modulated by habitat characteristics. This study characterized differences in Hg exposure in aquatic invertebrates and riparian songbirds across a large portion of the Willamette River system in western Oregon, starting at a Hg-contaminated Superfund site in the headwaters (Black Butte Hg Mine) and including a reservoir known to methylate Hg (Cottage Grove Reservoir), all downstream reaches (Coast Fork and Willamette River) and off-channel wetland complexes (Willamette Valley National Wildlife Refuge Complex). After accounting for year, date, and site differences in a mixed effects model, MeHg concentrations in aquatic invertebrates varied spatially among habitat categories and invertebrate orders. Similarly, THg in songbird blood varied by among habitat categories and bird species. The highest Hg concentrations occurred near the Hg mine, but Hg did not decline linearly with distance from the source of contamination. Birds were consistently elevated in Hg in habitats commonly associated with enhanced MeHg production, such as backwater or wetlands. We found a positive but weak correlation between aquatic invertebrate MeHg concentrations and songbird THg concentrations on a site-specific basis. Our findings suggest that Hg risk to riparian songbirds can extend beyond point-source contaminated areas, highlighting the importance of assessing exposure in surrounding habitats where methylmercury production may be elevated, such as reservoirs and wetlands.

Songbird feathers as indicators of mercury exposure: high variability and low predictive power suggest limitations.

Although feathers are commonly used to monitor mercury (Hg) in avian populations, their reliability as a sampling matrix has not been thoroughly assessed for many avian species, including most songbirds (Order Passeriformes). To better understand relationships between total Hg (THg) concentrations in feathers and other tissues for birds in the thrush and sparrow families, we (1) examined variation in THg concentrations among tissues, including feathers from six different tracts, nails, liver, and muscle; (2) tested relationships between THg concentrations in the various feather tracts and those in internal tissues from the same birds, to assess the predictive power of feather THg, and; (3) compared these relationships to those between THg concentrations in nails and internal tissues, to assess the viability of nails as a non-lethal sampling alternative. THg concentrations in all feather tracts and nails were consistently higher than those in the liver and muscle, and THg was higher in the thrushes than the sparrows. When comparing feather tracts, we observed high variation within some individuals, suggesting that estimates of Hg exposure could vary depending on which feather was sampled. Despite this variation, feather type had little effect on the predictive power of feather THg concentrations, which ranged from extremely weak in the sparrows (0.09 ≤ R2 ≤ 0.16) to moderate (0.29 ≤ R2 ≤ 0.42) in the thrushes. Alternatively, we found that nail samples better predicted internal tissue THg concentrations in both the thrushes (0.44 ≤ R2 ≤ 0.48) and sparrows (0.70 ≤ R2 ≤ 0.78). Nails have been used to monitor Hg in mammals and reptiles, but their reliability as a sampling matrix for monitoring Hg in avian populations has yet to be assessed for most taxa. While nails exhibit stronger relationships to internal tissue THg concentrations, they may not be an effective sampling option for all avian species because the collection of sizable nail samples could harm living birds, particularly small songbirds. However, this method may be reasonable for retrospective museum studies. Overall, our results suggest that, despite their current use in the literature, feathers are not a suitable sampling matrix for Hg monitoring in some songbird species.

Timber harvest alters mercury bioaccumulation and food web structure in headwater streams.

Timber harvest has many effects on aquatic ecosystems, including changes in hydrological, biogeochemical, and ecological processes that can influence mercury (Hg) cycling. Although timber harvest's influence on aqueous Hg transformation and transport are well studied, the effects on Hg bioaccumulation are not. We evaluated Hg bioaccumulation, biomagnification, and food web structure in 10 paired catchments that were either clear-cut in their entirety, clear-cut except for an 8-m wide riparian buffer, or left unharvested. Average mercury concentrations in aquatic biota from clear-cut catchments were 50% higher than in reference catchments and 165% higher than in catchments with a riparian buffer. Mercury concentrations in aquatic invertebrates and salamanders were not correlated with aqueous THg or MeHg concentrations, but rather treatment effects appeared to correspond with differences in the utilization of terrestrial and aquatic basal resources in the stream food webs. Carbon and nitrogen isotope data suggest that a diminished shredder niche in the clear-cut catchments contributed to lower basal resource diversity compared with the reference of buffered treatments, and that elevated Hg concentrations in the clear-cut catchments reflect an increased reliance on aquatic resources in clear-cut catchments. In contrast, catchments with riparian buffers had higher basal resource diversity than the reference catchments, indicative of more balanced utilization of terrestrial and aquatic resources. Further, following timber harvest THg concentrations in riparian songbirds were elevated, suggesting an influence of timber harvest on Hg export to riparian food webs. These data, coupled with comparisons of individual feeding guilds, indicate that changes in organic matter sources and associated effects on stream food web structure are important mechanisms by which timber harvest modifies Hg bioaccumulation in headwater streams and riparian consumers.

Spatial extent of mercury contamination in birds and their prey on the floodplain of a contaminated river.

Mercury (Hg) exposure has been extensively studied in aquatic and piscivorous wildlife, but, historically, less attention has been directed towards terrestrial species. However, it has become apparent that aquatic Hg crosses ecosystem boundaries along with beneficial subsidies, thereby entering the terrestrial food chain. It is still not known how far from contaminated waterways Hg exposure remains a risk. We examined the spatial extent of exposure in terrestrial songbirds breeding in the floodplain along a 40-km stretch of Hg-contaminated river in Virginia, USA. Four songbird species were chosen that readily occupied artificial nest cavities placed at known distances from the river; Carolina chickadees (Poecile carolinensis), Carolina wrens (Thryothorus ludovicianus), eastern bluebirds (Sialia sialis), and house wrens (Troglodytes aedon). We examined Hg exposure at varying distances from the edge of the river for three endpoints: 1) adult bird blood, 2) nestling bird feather and 3) spider whole body (collected in pitfall traps and directly from the mouths of nestling birds). We used mixed effects models to understand 1) how total Hg (i.e., inorganic and organic, THg) concentrations differed between contaminated and reference sites and 2) how THg concentrations declined with distance away from the river on contaminated sites. Adult bird blood THg indicated that a species-by-distance interaction was significant, after accounting for site and year. Importantly, despite the decline with distance, we found that THg levels in some songbird species and their invertebrate prey remained elevated above reference levels for up to 400m away from the river. Our results predict a spatial extent of contamination that is an order of magnitude greater than similar studies investigating the lateral impact of other aquatically derived contaminants. To our knowledge, this study is the first to indicate that exposure to legacy aquatic Hg is possible for terrestrial wildlife across the entire floodplain, rather than being confined to narrow riparian corridors.

Understanding sources of methylmercury in songbirds with stable mercury isotopes: Challenges and future directions.

Mercury (Hg) stable isotope analysis is an emerging technique that has contributed to a better understanding of many aspects of the biogeochemical cycling of Hg in the environment. However, no study has yet evaluated its usefulness in elucidating the sources of methylmercury (MeHg) in songbird species, a common organism for biomonitoring of Hg in forested ecosystems. In the present pilot study, we examined stable mercury isotope ratios in blood of 4 species of songbirds and the invertebrates they are likely foraging on in multiple habitats in a small watershed of mixed forest and wetlands in Acadia National Park in Maine (USA). We found distinct isotopic signatures of MeHg in invertebrates (both mass-dependent fractionation [as δ202 Hg] and mass-independent fractionation [as Δ199 Hg]) among 3 interconnected aquatic habitats. It appears that the Hg isotopic compositions in bird blood cannot be fully accounted for by the isotopic compositions of MeHg in lower trophic levels in each of the habitats examined. Furthermore, the bird blood isotope results cannot be simply explained by an isotopic offset as a result of metabolic fractionation of δ202 Hg (e.g., internal demethylation). Our results suggest that many of the birds sampled obtain MeHg from sources outside the habitat they were captured in. Our findings also indicate that mass-independent fractionation is a more reliable and conservative tracer than mass-dependent fractionation for identifying sources of MeHg in bird blood. The results demonstrate the feasibility of Hg isotope studies of songbirds but suggest that larger numbers of samples and an expanded geographic area of study may be required for conclusive interpretation. Environ Toxicol Chem 2018;37:166-174. © 2017 SETAC.

Mercury in western North America: A synthesis of environmental contamination, fluxes, bioaccumulation, and risk to fish and wildlife.

Western North America is a region defined by extreme gradients in geomorphology and climate, which support a diverse array of ecological communities and natural resources. The region also has extreme gradients in mercury (Hg) contamination due to a broad distribution of inorganic Hg sources. These diverse Hg sources and a varied landscape create a unique and complex mosaic of ecological risk from Hg impairment associated with differential methylmercury (MeHg) production and bioaccumulation. Understanding the landscape-scale variation in the magnitude and relative importance of processes associated with Hg transport, methylation, and MeHg bioaccumulation requires a multidisciplinary synthesis that transcends small-scale variability. The Western North America Mercury Synthesis compiled, analyzed, and interpreted spatial and temporal patterns and drivers of Hg and MeHg in air, soil, vegetation, sediments, fish, and wildlife across western North America. This collaboration evaluated the potential risk from Hg to fish, and wildlife health, human exposure, and examined resource management activities that influenced the risk of Hg contamination. This paper integrates the key information presented across the individual papers that comprise the synthesis. The compiled information indicates that Hg contamination is widespread, but heterogeneous, across western North America. The storage and transport of inorganic Hg across landscape gradients are largely regulated by climate and land-cover factors such as plant productivity and precipitation. Importantly, there was a striking lack of concordance between pools and sources of inorganic Hg, and MeHg in aquatic food webs. Additionally, water management had a widespread influence on MeHg bioaccumulation in aquatic ecosystems, whereas mining impacts where relatively localized. These results highlight the decoupling of inorganic Hg sources with MeHg production and bioaccumulation. Together the findings indicate that developing efforts to control MeHg production in the West may be particularly beneficial for reducing food web exposure instead of efforts to simply control inorganic Hg sources.

Assessing potential health risks to fish and humans using mercury concentrations in inland fish from across western Canada and the United States.

Fish represent high quality protein and nutrient sources, but Hg contamination is ubiquitous in aquatic ecosystems and can pose health risks to fish and their consumers. Potential health risks posed to fish and humans by Hg contamination in fish were assessed in western Canada and the United States. A large compilation of inland fish Hg concentrations was evaluated in terms of potential health risk to the fish themselves, health risk to predatory fish that consume Hg contaminated fish, and to humans that consume Hg contaminated fish. The probability that a fish collected from a given location would exceed a Hg concentration benchmark relevant to a health risk was calculated. These exceedance probabilities and their associated uncertainties were characterized for fish of multiple size classes at multiple health-relevant benchmarks. The approach was novel and allowed for the assessment of the potential for deleterious health effects in fish and humans associated with Hg contamination in fish across this broad study area. Exceedance probabilities were relatively common at low Hg concentration benchmarks, particularly for fish in larger size classes. Specifically, median exceedances for the largest size classes of fish evaluated at the lowest Hg concentration benchmarks were 0.73 (potential health risks to fish themselves), 0.90 (potential health risk to predatory fish that consume Hg contaminated fish), and 0.97 (potential for restricted fish consumption by humans), but diminished to essentially zero at the highest benchmarks and smallest fish size classes. Exceedances of benchmarks are likely to have deleterious health effects on fish and limit recommended amounts of fish humans consume in western Canada and the United States. Results presented here are not intended to subvert or replace local fish Hg data or consumption advice, but provide a basis for identifying areas of potential health risk and developing more focused future research and monitoring efforts.

Avian mercury exposure and toxicological risk across western North America: A synthesis.

Methylmercury contamination of the environment is an important issue globally, and birds are useful bioindicators for mercury monitoring programs. The available data on mercury contamination of birds in western North America were synthesized. Original data from multiple databases were obtained and a literature review was conducted to obtain additional mercury concentrations. In total, 29219 original bird mercury concentrations from 225 species were compiled, and an additional 1712 mean mercury concentrations, representing 19998 individuals and 176 species, from 200 publications were obtained. To make mercury data comparable across bird tissues, published equations of tissue mercury correlations were used to convert all mercury concentrations into blood-equivalent mercury concentrations. Blood-equivalent mercury concentrations differed among species, foraging guilds, habitat types, locations, and ecoregions. Piscivores and carnivores exhibited the greatest mercury concentrations, whereas herbivores and granivores exhibited the lowest mercury concentrations. Bird mercury concentrations were greatest in ocean and salt marsh habitats and lowest in terrestrial habitats. Bird mercury concentrations were above toxicity benchmarks in many areas throughout western North America, and multiple hotspots were identified. Additionally, published toxicity benchmarks established in multiple tissues were summarized and translated into a common blood-equivalent mercury concentration. Overall, 66% of birds sampled in western North American exceeded a blood-equivalent mercury concentration of 0.2 µg/g wet weight (ww; above background levels), which is the lowest-observed effect level, 28% exceeded 1.0 µg/g ww (moderate risk), 8% exceeded 3.0 µg/g ww (high risk), and 4% exceeded 4.0 µg/g ww (severe risk). Mercury monitoring programs should sample bird tissues, such as adult blood and eggs, that are most-easily translated into tissues with well-developed toxicity benchmarks and that are directly relevant to bird reproduction. Results indicate that mercury contamination of birds is prevalent in many areas throughout western North America, and large-scale ecological attributes are important factors influencing bird mercury concentrations.

From tails to toes: developing nonlethal tissue indicators of mercury exposure in five amphibian species.

Exposure to environmental contaminants has been implicated as a factor in global amphibian decline. Mercury (Hg) is a particularly widespread contaminant that biomagnifies in amphibians and can cause a suite of deleterious effects. However, monitoring contaminant exposure in amphibian tissues may conflict with conservation goals if lethal take is required. Thus, there is a need to develop non-lethal tissue sampling techniques to quantify contaminant exposure in amphibians. Some minimally invasive sampling techniques, such as toe-clipping, are common in population-genetic research, but it is unclear if these methods can adequately characterize contaminant exposure. We examined the relationships between mercury (Hg) concentrations in non-lethally sampled tissues and paired whole-bodies in five amphibian species. Specifically, we examined the utility of three different tail-clip sections from four salamander species and toe-clips from one anuran species. Both tail and toe-clips accurately predicted whole-body THg concentrations, but the relationships differed among species and the specific tail-clip section or toe that was used. Tail-clips comprised of the distal 0-2 cm segment performed the best across all salamander species, explaining between 82 and 92% of the variation in paired whole-body THg concentrations. Toe-clips were less effective predictors of frog THg concentrations, but THg concentrations in outer rear toes accounted for up to 79% of the variability in frog whole-body THg concentrations. These findings suggest non-lethal sampling of tails and toes has potential applications for monitoring contaminant exposure and risk in amphibians, but care must be taken to ensure consistent collection and interpretation of samples.

Songbirds as sentinels of mercury in terrestrial habitats of eastern North America.

Mercury (Hg) is a globally distributed environmental contaminant with a variety of deleterious effects in fish, wildlife, and humans. Breeding songbirds may be useful sentinels for Hg across diverse habitats because they can be effectively sampled, have well-defined and small territories, and can integrate pollutant exposure over time and space. We analyzed blood total Hg concentrations from 8,446 individuals of 102 species of songbirds, sampled on their breeding territories across 161 sites in eastern North America [geometric mean Hg concentration = 0.25 µg/g wet weight (ww), range <0.01-14.60 µg/g ww]. Our records span an important time period-the decade leading up to implementation of the USEPA Mercury and Air Toxics Standards, which will reduce Hg emissions from coal-fired power plants by over 90 %. Mixed-effects modeling indicated that habitat, foraging guild, and age were important predictors of blood Hg concentrations across species and sites. Blood Hg concentrations in adult invertebrate-eating songbirds were consistently higher in wetland habitats (freshwater or estuarine) than upland forests. Generally, adults exhibited higher blood Hg concentrations than juveniles within each habitat type. We used model results to examine species-specific differences in blood Hg concentrations during this time period, identifying potential Hg sentinels in each region and habitat type. Our results present the most comprehensive assessment of blood Hg concentrations in eastern songbirds to date, and thereby provide a valuable framework for designing and evaluating risk assessment schemes using sentinel songbird species in the time after implementation of the new atmospheric Hg standards.

Mercury exposure in terrestrial birds far downstream of an historical point source.

Mercury (Hg) is a persistent environmental contaminant found in many freshwater and marine ecosystems. Historical Hg contamination in rivers can impact the surrounding terrestrial ecosystem, but there is little known about how far downstream this contamination persists. In 2009, we sampled terrestrial forest songbirds at five floodplain sites up to 137 km downstream of an historical source of Hg along the South and South Fork Shenandoah Rivers (Virginia, USA). We found that blood total Hg concentrations remained elevated over the entire sampling area and there was little evidence of decline with distance. While it is well known that Hg is a pervasive and long-lasting aquatic contaminant, it has only been recently recognized that it also biomagnifies effectively in floodplain forest food webs. This study extends the area of concern for terrestrial habitats near contaminated rivers for more than 100 km downstream from a waterborne Hg point source.