Distribution and trends of mercury in aquatic and terrestrial biota of New York, USA: a synthesis of 50 years of research and monitoring.

Mercury (Hg) inputs have particularly impacted the northeastern United States due to its proximity to anthropogenic emissions sources and abundant habitats that efficiently convert inorganic Hg into methylmercury. Intensive research and monitoring efforts over the past 50 years in New York State, USA, have informed the assessment of the extent and impacts of Hg exposure on fishes and wildlife. By synthesizing Hg data statewide, this study quantified temporal trends of Hg exposure, spatiotemporal patterns of risk, the role that habitat and Hg deposition play in producing spatial patterns of Hg exposure in fish and other wildlife, and the effectiveness of current monitoring approaches in describing Hg trends. Most temporal trends were stable, but we found significant declines in Hg exposure over time in some long-sampled fish. The Adirondack Mountains and Long Island showed the greatest number of aquatic and terrestrial species with elevated Hg concentrations, reflecting an unequal distribution of exposure risk to fauna across the state. Persistent hotspots were detected for aquatic species in central New York and the Adirondack Mountains. Elevated Hg concentrations were associated with open water, forests, and rural, developed habitats for aquatic species, and open water and forested habitats for terrestrial species. Areas of consistently elevated Hg were found in areas driven by atmospheric and local Hg inputs, and habitat played a significant role in translating those inputs into biotic exposure. Continued long-term monitoring will be important in evaluating how these patterns continue to change in the face of changing land cover, climate, and Hg emissions.

The influence of biotic and abiotic factors on banded common loon (Gavia immer) reproductive success in a remote, mountainous region of the northeastern United States.

Habitat degradation resulting from anthropogenic activities can threaten wildlife populations. Even wildlife existing in seemingly pristine areas are at risk of airborne pollutants and urban development. The common loon (Gavia immer), a top-trophic level predator in freshwater aquatic ecosystems, has previously experienced detrimental changes in reproductive success as a result of anthropogenic activities. However, long-term studies and large sample sizes are necessary to ascertain the impacts of various anthropogenic activities on this long-lived species. Using a multi-year dataset, we investigated the effects of multiple biotic and abiotic factors on the probability of adult male and female common loon hatching and fledging success. From 1998-2017, we banded individual loons, collected blood samples to assess mercury (Hg) exposure of the birds, and monitored their reproductive success. Adult female loon hatching success was negatively associated with the amount of rainfall received in a given year while fledging success was positively associated with the amount of shoreline development. Adult male loon hatching success was positively associated with the amount of shoreline development and fledging success was negatively associated with the number of other loon pairs on a lake.

Spatial patterns and temporal trends in mercury concentrations in common loons (Gavia immer) from 1998 to 2016 in New York's Adirondack Park: has this top predator benefitted from mercury emission controls?

Mercury (Hg), a neurotoxic pollutant, can be transported long distances through the atmosphere and deposited in remote areas, threatening aquatic wildlife through methylation and bioaccumulation. Over the last two decades, air quality management has resulted in decreases in Hg emissions from waste incinerators and coal-fired power plants across North America. The common loon (Gavia immer) is an apex predator of the aquatic food web. Long-term monitoring of Hg in loons can help track biological recovery in response to the declines in atmospheric Hg that have been documented in the northeastern USA. To assess spatial patterns and temporal trends in Hg exposure of the common loon in the Adirondack Park of New York State, we analyzed Hg concentrations in loon blood and egg samples from 116 lakes between 1998 and 2016. We found spatially variable Hg concentrations in adult loon blood and feathers across the Park. Loon Hg concentrations (converted to female loon units) increased 5.7% yr-1 from 1998 to 2010 (p = 0.04), and then stabilized at 1.70 mg kg-1 from 2010 to 2016 (p = 0.91), based on 760 observations. Concentrations of Hg in juvenile loons also increased in the early part of the record, stabilizing 2 years before Hg concentrations stabilized in adults. For 52 individual lakes with samples from at least 4 different years, loon Hg increased in 34 lakes and decreased in 18 lakes. Overall, we found a delayed recovery of Hg concentrations in loons, despite recent declines in atmospheric Hg.

Determining optimal sampling strategies for monitoring mercury and reproductive success in common loons in the Adirondacks of New York.

The common loon (Gavia immer), a top predator in the freshwater food web, has been recognized as an important bioindicator of aquatic mercury (Hg) pollution. Because capturing loons can be difficult, statistical approaches are needed to evaluate the efficiency of Hg monitoring. Using data from 1998 to 2016 collected in New York's Adirondack Park, we calculated the power to detect temporal changes in loon Hg concentrations and fledging success as a function of sampling intensity. There is a tradeoff between the number of lakes per year and the number of years needed to detect a particular rate of change. For example, a 5% year-1 change in Hg concentration could be detected with a sampling effort of either 15 lakes per year for 10 years, or 5 lakes per year for 15 years, given two loons sampled per lake per year. A 2% year-1 change in fledging success could be detected with a sampling effort of either 40 lakes per year for 15 years, or 30 lakes per year for 20 years. We found that more acidic lakes required greater sampling intensity than less acidic lakes for monitoring Hg concentrations but not for fledging success. Power analysis provides a means to optimize the sampling designs for monitoring loon Hg concentrations and reproductive success. This approach is applicable to other monitoring schemes where cost is an issue.

Ultraviolet-assisted oiling assessment improves detection of oiled birds experiencing clinical signs of hemolytic anemia after exposure to the Deepwater Horizon oil spill.

While large-scale oil spills can cause acute mortality events in birds, there is increasing evidence that sublethal oil exposure can trigger physiological changes that have implications for individual performance and survival. Therefore, improved methods for identifying small amounts of oil on birds are needed. Because ultraviolet (UV) light can be used to identify thin crude oil films in water and on substrate that are not visually apparent under normal lighting conditions, we hypothesized that UV light could be useful for detecting small amounts of oil present on the plumage of birds. We evaluated black skimmers (Rynchops niger), brown pelicans (Pelecanus occidentalis), clapper rails (Rallus crepitans), great egrets (Ardea alba), and seaside sparrows (Ammodramus maritimus) exposed to areas affected by the Deepwater Horizon oil spill in the Gulf of Mexico as well as from reference areas from 20 June, 2010 to 23 February, 2011. When visually assessed without UV light, 19.6% of birds evaluated from areas affected by the spill were determined to be oiled (previously published data), whereas when examined under UV light, 56.3% of the same birds were determined to have oil exposure. Of 705 individuals examined in areas potentially impacted by the spill, we found that fluorescence under UV light assessment identified 259 oiled birds that appeared to be oil-free on visual exam, supporting its utility as a simple tool for improving detection of modestly oiled birds in the field. Further, UV assessment revealed an increase in qualitative severity of oiling (approximate % of body surface oiled) in 40% of birds compared to what was determined on visual exam. Additionally, black skimmers, brown pelicans, and great egrets exposed to oil as determined using UV light experienced oxidative injury to erythrocytes, had decreased numbers of circulating erythrocytes, and showed evidence of a regenerative hematological response in the form of increased reticulocytes. This evidence of adverse effects was similar to changes identified in birds with oil exposure as determined by visual examination without UV light, and is consistent with hemolytic anemia likely caused by oil exposure. Thus, UV assessment proved useful for enhancing detection of birds exposed to oil, but did not increase detection of birds experiencing clinical signs of anemia compared to standard visual oiling assessment. We conclude that UV light evaluation can help identify oil exposure in many birds that would otherwise be identified visually as unexposed during oil spill events.

A novel method for captive rearing and translocation of juvenile common loons.

Common loons (Gavia immer) are diving waterbirds that are particularly challenging to keep in captivity due to their specific behavioral and physiologic needs, special housing requirements, and susceptibility to stress-related disease. We report a novel method for housing and captive rearing common loon chicks that was developed as part of the first-ever loon translocation effort in southeast Massachusetts, from 2015 to 2017. Thirteen loon chicks were reared in aquatic pens in a natural lake environment, utilizing noninvasive feeding and monitoring techniques that avoided human habituation. Chicks were reared in aquatic pens for 16-28 days before being released onto the lake. All chicks remained clinically normal and were monitored on the lake for up to 4 months following release. At least four of the chicks were subsequently confirmed to have survived to adulthood when they returned to the area in breeding plumage two to 3 years following release. Two of these confirmed adults displayed prolonged territorial pair behavior together, and this is an encouraging early sign that captive-reared individuals may form successful breeding pairs in the future. Because most immature loons remain on the ocean until at least 3 years of age, we expect additional captive-reared loons to return to the release area in subsequent years. These husbandry techniques could be applied to other loon and diving bird species that are notoriously difficult to house in captivity. The novel feeding techniques described here could also be adapted for loon chicks being reared in pools or other traditional captive settings.

PLASMA BIOCHEMISTRY AND PROTEIN ELECTROPHORESIS REFERENCE INTERVALS OF THE COMMON LOON (GAVIA IMMER).

There are no published plasma biochemistry reference intervals for any species within the order Gaviiformes, which includes the common loon (Gavia immer). Because of their unique classification and lack of close taxonomic relatives, species-specific values for clinical data in loons are needed. This study determined reference intervals for plasma biochemical values in adult common loons, and reference intervals for protein electrophoresis values in both adult and juvenile common loons. Healthy, wild adult (n = 148, age >3 yr) and juvenile (n = 31, age 4-12 wk) common loons were sampled on freshwater summer breeding territories at study sites across North America. Plasma biochemical analytes included glucose (Glu), total calcium, phosphorus, sodium, potassium, chloride, blood urea nitrogen (BUN), uric acid, cholesterol, triglycerides, creatine kinase, γ-glutamyl transferase, alkaline phosphatase (ALP), lactate dehydrogenase, aspartate aminotransferase, amylase, and bile acids. Protein electrophoresis data included albumin to globulin ratio (A: G), prealbumin, albumin, α1-globulin, α2-globulin, ß-globulin, and γ-globulin. Adult females had significantly higher Glu, ALP, and BUN than adult males. Juvenile loons had higher ß-globulins than adults, whereas adults had higher α1-globulins. Establishment of complete reference intervals will improve clinical assessment of captive loons, and allow researchers to better understand the health of wild loons in response to the multiple environmental stressors faced by these species.

Spatial patterns of mercury in biota of Adirondack, New York lakes.

We studied the spatial distribution patterns of mercury (Hg) in lake water, littoral sediments, zooplankton, crayfish, fish, and common loons in 44 lakes of the Adirondacks of New York State, USA, a region that has been characterized as a "biological Hg hotspot". Our study confirmed this pattern, finding that a substantial fraction of the lakes studied had fish and loon samples exceeding established criteria for human and wildlife health. Factors accounting for the spatial variability of Hg in lake water and biota were lake chemistry (pH, acid neutralizing capacity (ANC), percent carbon in sediments), biology (taxa presence, trophic status) and landscape characteristics (land cover class, lake elevation). Hg concentrations in zooplankton, fish and common loons were negatively associated with the lake water acid-base status (pH, ANC). Bioaccumulation factors (BAF) for methyl Hg (MeHg) increased from crayfish (mean log(10) BAF = 5.7), to zooplankton (5.9), to prey fish (6.2), to larger fish (6.3), to common loons (7.2). MeHg BAF values in zooplankton, crayfish, and fish (yellow perch equivalent) all increased with increasing lake elevation. Our findings support the hypothesis that bioaccumulation of MeHg at the base of the food chain is an important controller of Hg concentrations in taxa at higher trophic levels. The characteristics of Adirondack lake-watersheds (sensitivity to acidic deposition; significant forest and wetland land cover; and low nutrient inputs) contribute to elevated Hg concentrations in aquatic biota.

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.

Hematological indices of injury to lightly oiled birds from the Deepwater Horizon oil spill.

Avian mortality events are common following large-scale oil spills. However, the sublethal effects of oil on birds exposed to light external oiling are not clearly understood. We found that American oystercatchers (area of potential impact n = 42, reference n = 21), black skimmers (area of potential impact n = 121, reference n = 88), brown pelicans (area of potential impact n = 91, reference n = 48), and great egrets (area of potential impact n = 57, reference n = 47) captured between 20 June 2010 and 23 February 2011 following the Deepwater Horizon oil spill experienced oxidative injury to erythrocytes, had decreased volume of circulating erythrocytes, and showed evidence of a regenerative hematological response in the form of increased reticulocytes compared with reference populations. Erythrocytic inclusions consistent with Heinz bodies were present almost exclusively in birds from sites impacted with oil, a finding pathognomonic for oxidative injury to erythrocytes. Average packed cell volumes were 4 to 19% lower and average reticulocyte counts were 27 to 40% higher in birds with visible external oil than birds from reference sites. These findings provide evidence that small amounts of external oil exposure are associated with hemolytic anemia. Furthermore, we found that some birds captured from the area impacted by the spill but with no visible oiling also had erythrocytic inclusion bodies, increased reticulocytes, and reduced packed cell volumes when compared with birds from reference sites. Thus, birds suffered hematologic injury despite no visible oil at the time of capture. Together, these findings suggest that adverse effects of oil spills on birds may be more widespread than estimates based on avian mortality or severe visible oiling. Environ Toxicol Chem 2018;37:451-461. © 2017 SETAC.

Polycyclic aromatic hydrocarbons in blood related to lower body mass in common loons.

We captured 93 wintering adult and subadult Common Loons (Gavia immer) in coastal Louisiana from 2011 to 2015 following the Deepwater Horizon oil spill. We tested blood samples for exposure to polycyclic aromatic hydrocarbons (PAHs) and measured physiological variables including hematocrit, hemoglobin and total blood protein. PAH concentrations in loon blood differed from year to year and by age class. High PAH concentrations were significantly related to lower body masses in both adult and subadult birds and higher serum protein levels in adults only. PAH concentrations had marginal relations with both hematocrit and hemoglobin levels. The types of PAHs detected also underwent a major shift over time. The PAHs detected in 2011, 2012, and 2015 were primarily low molecular weight (three carbon rings); however, in 2013, most detected PAHs were high molecular weight (four carbon rings). It is unclear what events led to the increase in PAH concentrations and the shift in type of PAHs over time.

Adverse effects from environmental mercury loads on breeding common loons.

Anthropogenic inputs of mercury (Hg) into the environment have significantly increased in the past century. Concurrently, the availability of methylmercury (MeHg) in aquatic systems has increased to levels posing risks to ecological and human health. We use the common loon (Gavia immer) as an upper trophic level bioindicator of aquatic Hg toxicity in freshwater lakes. Multiple endpoints were selected to measure potential negative impacts from MeHg body burdens on behavior, physiology, survival and reproductive success. A robust spatio-temporal dataset was used that included nearly 5,500 loon Hg measurements over an 18-year period. We measured significant changes related to elevated MeHg body burdens, including aberrant incubation behavior, lethargy, and wing area asymmetry. Mercury body burdens in adult loons increased an average of 8.4% per year. Increasing Hg body burdens reduced the number of fledged chicks per territorial pair, with highest risk loons producing 41% fewer fledged young than our reference group. Our multiple endpoints establish adverse effect thresholds for adult loons at 3.0 ug/g (wet weight) in blood and 40.0 ug/g (fresh weight) in feathers. Mercury contamination in parts of Maine and New Hampshire is a driving stressor for creating breeding population sinks. Standardized monitoring programs are needed to determine if population sinks occur elsewhere and to track aquatic ecosystem responses to changes in Hg emissions and deposition.