Climate-Driven Alterations in the Mercury Cycle: Implications for Wildlife Managers Through a One Health Lens

Abstract

Mercury (Hg) is a naturally occurring element, but atmospheric Hg has increased due to human activities since the industrial revolution. When deposited in aquatic environments, atmospheric Hg can be converted to methyl mercury (MeHg), which bioaccumulates in ecosystems and can cause neurologic and endocrine disruption in high quantities. While higher atmospheric Hg levels do not always translate to higher contamination in wildlife, museum specimens over the past 2 centuries have documented an increase in species that feed at higher trophic levels. Increased exposure to pollutants presents an additional threat to fish and wildlife populations already facing habitat loss or degradation due to global change. Additionally, Hg cycling and bioaccumulation are primarily driven by geophysical, ecological, and biogeochemical processes in the environment, all of which may be modulated by climate change. In this review, we begin by describing where, when, and how the Hg cycle may be altered by climate change and how this may impact wildlife exposure to MeHg. Next, we summarize the already observed physiological effects of increased MeHg exposure to wildlife and identify future climate change vulnerabilities. We illustrate the implications for wildlife managers through a case study and conclude by suggesting key areas for management action to mitigate harmful effects and conserve wildlife and habitats amid global change.

1. Introduction

Mercury (Hg) is an element naturally found in the environment, which is released into the atmosphere through processes like volcanic activity, forest fires, and rock weathering. However, since the industrial revolution in the 1890s, there has been a rise in Hg levels in the geologic record as human activities began releasing large quantities of elemental mercury Hg⁰ into the atmosphere [1]. Although increases in atmospheric mercury do not necessarily equate to high mercury contamination of wildlife, museum specimens show a similar increase in methylmercury (MeHg) burden for piscivorous birds and polar bears (Ursus maritimus) over the last 120 years [2,3]. MeHg, the more toxic bioavailable form of mercury, bioaccumulates in organisms, leading to detrimental effects on neurological and endocrine systems [4]. Significant increases in MeHg within these predators during the post-1940s and post-1990s time periods coincide with periods of high anthropogenic Hg⁰ emissions, linking increased emissions to the increased bioaccumulation of MeHg in wildlife [2]. Gaseous elemental mercury (Hg⁰; GEM), gaseous oxidized mercury (HgII), and particulate mercury (PHg) are deposited on the landscape via precipitation and dust particles, which are then integrated into the environment (Figure 1). In the simplest of terms, deposited Hg can undergo four main pathways: (1) it may be methylated and converted to its more toxic form (MeHg) by bacteria in aquatic environments, (2) it may be stored long term in deep reservoirs such as ocean sediments or soils, (3) it may be stored temporarily by accumulating in surface environments such as vegetation, the upper soil layer, or surface waters, (4) it may be volatilized and returned to the atmosphere [4,5]. The fate of deposited Hg depends on environmental factors like temperature, chemical conditions, and biological activity.

There is a long history of studying the human health impacts of Hg exposure, with the first documented account appearing in patient records at Saint Bartholomew’s Hospital in 1865 [6]. Since then, global public health and medical communities have pinpointed the common source of human exposure as the consumption of aquatic species in which bioaccumulation of toxicity had occurred [7]. Effects vary by individual but may include severe neurologic, cardiovascular, and reproductive issues upon exposure [8,9,10]. Similar effects have been observed in wildlife, including neurological issues (e.g., visual impairment), physiological impacts (e.g., inhibited growth), behavioral changes (e.g., lethargy), and decreased reproductive success [11,12]. While convincing evidence indicates that wildlife exposure to Hg has increased since the Industrial Revolution [13,14,15], trends in MeHg accumulation vary, with concentrations rising in populations in some geographic areas while remaining stable or declining in others. The toxicological impacts of Hg to wildlife health have been summarized for several taxa (e.g., birds, fish, and mammals), but questions remain about the complexities of the mercury cycle and the diverse methods used to measure trends. When viewing this widespread challenge through the lens of the interdisciplinary practice of One Health, addressing MeHg accumulation and exposure becomes not only a human health concern but an environmental and wildlife health concern as well.

Although international efforts, such as the Minamata Convention on Mercury, have been implemented to reduce Hg emissions, legacy emissions and delays in the response of global Hg reservoirs to atmospheric inputs continue to pose challenges [16,17]. Even if Hg emissions remain constant, atmospheric and ocean surface Hg concentrations are still expected to increase, as new emissions will accumulate in these reservoirs faster than they can be transferred to deep ocean storage for long-term sequestration [18]. Global Hg levels, particularly in surface reservoirs, are influenced by both climate change and anthropogenic activities [19].

The 5th National Climate Assessment (NCA5) provides a snapshot of how climatic shifts have impacted ten distinct regions of the United States and its territories [20]. While each region presents unique challenges and opportunities, there are commonalities across regions, such as compounding extreme events, impacts on social and economic systems, and disproportionate effects on vulnerable communities. Seven regional chapters include a key message related to ecological composition or shifts in biodiversity, while five of the regional chapters include a key message connected to the quality or quantity of water resources. Of note, there are no mentions of MeHg within the NCA5, although Hg is mentioned in two places: the Midwest chapter in reference to fish consumption and toxic chemicals (see Table 24.1 in [21], as well in a reference citation within the Southern Great Plains chapter regarding dispersal of mercury-contaminated sediment during Hurricane Harvey [22]).

Table 1. References to identified effects of changes to mercury (Hg) cycling throughout the regional chapters of the Fifth National Climate Assessment. An X within a cell shows that the topic concept appears within the chapter’s text.

		Northeast	Southeast	Caribbean	Midwest	Northern Great Plains	Southern Great Plains	Northwest	Southwest	Alaska	Hawaii and US-Affiliated Pacific Islands
Effects of increasing global temperatures	Increases in ocean temperatures	X		X				X	X	X	X
	Increases in land temperatures	X	X	X	X	X	X	X	X	X	X
	Increased cryosphere melting				X			X		X
	Increases in temperatures in freshwater systems		X		X		X	X		X
	Changing climate oscillations	X			X		X		X	X	X
	Sea level rise	X	X	X			X	X	X	X	X
	Increase in heavy precipitation and storms	X	X	X	X	X	X	X	X	X	X
Effects of increasing drought conditions	Increase in wildfire intensity		X		X	X	X	X	X	X	X
	Drying of freshwater systems		X	X	X	X	X	X	X	X	X
Other co-factors influencing mercury in wildlife	Human land use change		X	X			X	X			X
	Overfishing	X		X				X			X
	Other pollutants	X		X	X		X	X			X

shows the occurrence of the following mercury-related effects in each of the regional chapters of the NCA5.

Climate change is also predicted to impact many pathways through which Hg is released, taken up, and moved worldwide [4]. Hg cycling and bioaccumulation are primarily driven by geophysical, ecological, and biogeochemical processes in the environment, all of which may be modulated by hydrological or ecological disturbances. For example, climate change may influence Hg cycling and environmental risk via altered wind currents and warmer temperatures affecting patterns of Hg deposition and oxidation; changes in the timing, frequency, type, and amount of precipitation; and altered frequency and intensity of wildfires or melting of permafrost, which may result in increased Hg. Climate change is a global driver that has both direct and indirect effects on the four ecological mechanisms associated with local MeHg bioaccumulation, which are (1) primary productivity, (2) habitat use, (3) bioenergetics, and (4) food web structure [23]. All of these can be directly influenced by climate change through the alteration of the physical environment and indirectly via the human response, such as adaptation in land use [23] or changes in water storage or conveyance [24,25,26]. The broader ecological consequences may vary, resulting in both beneficial and harmful outcomes, yet their precise influence on fish, wildlife, and their habitats is not well understood.

In this review, we first explore the spatial, temporal, and mechanistic alterations of the Hg cycle driven by climate change and their implications for wildlife Hg exposure. Next, we summarize the documented physiological effects of increased Hg exposure to wildlife and highlight future vulnerabilities associated with climate change. We then highlight the implications for wildlife managers using the United States National Wildlife Refuge System as a case study. We conclude by suggesting key strategies for wildlife managers to mitigate Hg exposure and its harmful effects, supporting wildlife conservation amid shifting climate conditions and evolving environmental contamination patterns.

2. Materials and Methods

The last review paper on the interaction between MeHg and wildlife was published in 2020 [27]. Since then, there have been continued publications on mercury exposure in wildlife, and we wanted to expand the assessment to consider climate change more explicitly. While neither a meta-analysis nor a systematic review, we started our literature review process by conducting a Boolean search in Web of Science, a commonly used database with access to 22,000 journals, to understand the current issues at the nexus of these topics and construct the manuscript outline. Specifically, we used the query “climate change” AND “mercury” AND “wildlife” and chose to limit the publication years from 2020, the year of the last major review paper in the field, to 2024, the year this manuscript was written, to capture the most updated literature. One benefit of the Web of Science is the compilation of search results, including authors, abstracts, keywords, and links to the publications so they can be further reviewed. We read through each of the 96 papers that were listed with all three keywords. Some papers were incorrectly labeled or had misleading keywords (for example, a study about climate change and wildlife included “mercury” as a keyword, even though the only mention of mercury was in regard to a mercury thermometer). Some papers were topical but were more focused on describing new methods of measuring mercury in wildlife or developing a new model to predict mercury burdens. Other papers quantified the mercury burden of species, but not specifically how that mercury burden or exposure might be altered in the context of climate change.

Based on our reading and the current published literature, we developed the structure of the review paper and the specific focus on implications for wildlife managers. After choosing the topics we wanted to cover in the literature review, we proceeded to flesh out each section without limiting the articles cited to the Boolean results mentioned earlier. In the end, only 38 of the 96 papers from that Boolean search were included, as the key point of the initial search was to guide the determination of which sections to include in the review. Because climate change, mercury, and wildlife are global phenomena, papers cited in this review are intercontinental and cover the Americas, Europe, East Asia, Oceania, and the Artic in general. However, the case study presented in this review is from the United States, based on the physical location of the researchers. Additional articles outside of the literature review (usually from earlier years) were included for context, to further explain an idea or topic, or because a paper from 2020 to 2024 referenced that paper as a source for a specific idea we wanted to include that required further explanation.

3. Results

3.1. Effects of Increasing Global Temperatures

Since 1850, global average temperatures have increased 1.59 ± 0.25 °C on land and 0.88 ± 0.2 °C in the ocean. Despite efforts to curb this warming, the most conservative models (SSP1-1.9) predict that by 2100, the temperature will still be 1.5 °C greater than 1850–1900 levels [28].

3.1.1. Increases in Ocean Temperatures

As ocean temperatures rise, we can expect to see increases in MeHg at all trophic levels. Ocean deoxygenation associated with increased ocean temperatures leads to hypoxic and anoxic conditions that select for Hg-methylating microbes, increasing the amount of MeHg that is bioavailable [29]. Increases in ocean water temperatures were linked to increased MeHg production in marine ecosystems and subsequent increased MeHg uptake in clams (Ruditapes philippinarum), which resulted in higher cellular damage [30]. In predatory fish, ecosystem models investigating the impacts of a 1 °C increase in seawater temperature showed increases in MeHg contamination. Based on historical data, Atlantic cod (Gadus morhua) MeHg is predicted to increase 32%, Spiny dogfish (Squalus acanthias) MeHg is predicted to increase 70%, and Atlantic Bluefin tuna (Thunnus thynnus) MeHg is predicted to increase 56% [31].

3.1.2. Increases in Land Temperatures

Increased plant productivity from warmer environments could help sequester Hg into soils, as Hg deposition from litterfall would increase [1,19,32,33]. In fact, global reforestation on non-cropland and where forests are ecologically possible was modeled to increase Hg sequestration by 98 Mg yr⁻¹ [34]. However, if paired with increases in precipitation and subsequent increased runoff, more Hg will flow into aquatic systems, the primary place of Hg methylation [35]. Additionally, despite potential increases in Hg sequestration in soils, a review of Hg accumulation from the Holocene to the present showed a distinct correlation between Hg accumulation and colder global temperatures, not warmer temperatures [19].

3.1.3. Increased Cryosphere Melting [28]

Permafrost is a long-term reservoir of Hg. As the permafrost thaws, the Hg stored is released back into the biogeochemical mercury cycle [36]. Wetlands (and their downstream freshwaters) associated with permafrost melt had significantly higher concentrations of MeHg than upstream areas and wetlands not created by permafrost melt [36,37].

Glaciers and sea ice are already melting and will continue to melt [28]. Glaciers, sea ice, and snowpack are known sinks of atmospheric Hg [38]. While photochemical reactions often re-emit the Hg stored in ice back into the atmosphere, some remain in the meltwater as MeHg and are transported into nearby environments [1,38]. In the Arctic, melting snowpack leads to high MeHg input to coastal seawaters, which is bioaccumulated in the marine food web [39].

3.1.4. Increases in Temperatures in Freshwater Systems [28]

As land temperatures increase, landlocked freshwater systems will also see increased temperatures. Extended periods of warm temperatures in lakes increased Hg methylation and decreased demethylation rates [40]. Anoxic waters and sediments promote the methylation of Hg, usually via sulfate-reducing microorganisms [41]. Increases in water temperatures generally decreased mixing, increased stratification, or raised the thermocline, increasing the area of anoxic environments in lakes, which leads to increased MeHg production [42].

Additionally, increased productivity in riparian zones can impact MeHg production surrounding freshwater systems. In lakes with low productivity, increasing DOM input stimulated microbial activity, which led to increased MeHg concentrations [43]. In a gradient of lakes with increasing nearshore conifer cover, concentrations of Hg in fish increased with tree cover percent because of increased organic carbon inputs [44].

3.1.5. Changing Climate Oscillations

As temperatures over both the ocean and land increase, climate oscillations will continue to change [45]. In multiple species of arctic biota, yearly variation in the Hg burden was related to time-lagged Arctic and North American Oscillations (AO/NAO), two large-scale climate oscillations that influence climate and weather in North America [46]. These climate and weather patterns impact mercury cycling and bioavailability, as well as influence biotic interactions. For example, they often influence the presence/absence of sea ice during specific seasons, which in turn can influence the trophic level that pagophilic (ice-loving) consumers feed at during that time [47]. As these climate oscillations are projected to change in the coming decades, the cascading effects of these oscillations will likely change Hg bioavailability and burdens in organisms. However, evidence of and the direction of these changes may not be immediately clear, given the time-lag in the relationship between the Hg burden and the AO/NAO, further complicating our understanding of this relationship.

3.1.6. Sea Level Rise

Since 1901, the mean sea level has increased by 0.2 ± 0.05 m, inundating coastal areas, and the mean sea level will continue to increase as more glaciers melt [28]. In coastal Brazil, increased MeHg concentrations are linked to the combined effects of sea level rise and drought. Drought has reduced the flow of freshwater and new sediments through coastal estuaries, while sea level rise has increased seawater intrusion into these estuaries. This traps sediments in estuaries, creating anoxic environments, which methylate Hg. This has resulted in increased MeHg production and increased MeHg concentrations in shrimp, crab, and fish living in the estuary [48]. In tidal marsh songbirds, MeHg contamination can interact with nest flooding probability to reduce songbird survival. Rising sea levels will continue to flood tidal marshes, and if MeHg production in the marsh remains the same or increases, the combined effect will reduce further tidal marsh songbird fitness [49].

3.1.7. Increase in Heavy Precipitation and Storms

Even at the lowest modeled change in global temperatures (+1.5 °C), heavy precipitation, storm frequency and intensity, and associated flooding are predicted to increase [28]. Changes, including climate-induced changes, to hydrologic systems have an incredible ability to moderate MeHg production [23]. In upland boreal and temperate forests, flooding increased net MeHg production in nearby freshwater systems and MeHg bioaccumulation in fish [50,51,52].

3.2. Effects of Increasing Drought Conditions

Increased rates of evapotranspiration resulting from increased land temperatures will lead to increases in drought conditions in some parts of the world [28].

3.2.1. Increase in Wildfire Intensity

Higher temperatures and drought frequency produce favorable conditions for wildfires, and wildfire size and frequency are expected to continue increasing under climate change [28]. In geologic records, elevated mercury input into ecosystems is often linked to increased forest fires [1], likely due to greater Hg and MeHg input into freshwater systems via postfire runoff events [53,54,55]. Not only is MeHg directly introduced into these systems, but also microbial Hg methylation in anaerobic sediments can be stimulated by wildfire runoff inputs [56]. However, fire has also resulted in lower soil, litterfall, throughfall, and stream water Hg due to volatilization and loss of organic soil horizon [57]. Changes to water chemistry, like DOC and pH, from wildfire runoff can mediate or enhance microbial methylation rates [53,58,59]. Additionally, wildfire-related changes in primary and secondary productivity and associated trophic level shifts can impact the bioaccumulation in freshwater wildlife more than total Hg and MeHg inputs into the system do [59].

3.2.2. Drying of Freshwater Systems

Increases in evaporation because of higher temperatures, drought conditions, and altered precipitation regimes will affect the wetting and drying patterns of freshwater [60]. In some scenarios, this will lead to freshwater systems drying at faster rates and for longer time periods than currently experienced. Lower lake levels due to drying events were correlated with increased herring gull (Larus sp.) egg Hg concentrations [61]. The authors speculated that this could be due to warmer, less oxygenated waters that promoted Hg methylation or a correlation with dry weather and increased wildfires in the surrounding areas, which are also known to increase Hg input into the ecosystem [61]. Overall, research suggests that changes in hydrologic systems and sediment sources can impact Hg levels in freshwater [23,62]. While droughts and decreased water flows may reduce point source Hg pollution from nearby anthropogenic sources, it can also increase anoxic environments where inorganic Hg is more readily methylated [62].

3.3. Other Co-Factors Influencing Mercury in Fish and Wildlife

3.3.1. Human Land Use Change

As climate change transforms the landscape around us, humans may have to turn to the intensification of agriculture and resource extraction to meet our needs [63]. Human land use and potential climate-related changes can also impact wildlife exposure to Hg [64]. Forests sequester and store a large amount of unmethylated Hg globally. For example, in the Amazon rainforest, forested soils sequestered 138 µg Hg m⁻²yr⁻¹ and stored 9100 µg Hg m⁻² in the top 5 cm, compared to areas deforested for mining, which only sequestered 8.6 µg Hg m⁻²yr⁻¹ and only stored 7100 µg Hg m⁻² in the top 5 cm [64]. If deforestation of the Amazon continues at the same rate as in 2021, an additional 3.0 Mg Hg yr⁻¹ would be released from soils [65]. Global models estimated that deforestation in 2015 released 217 Mg Hg yr⁻¹, about 10% of all anthropogenic Hg emissions [34]. Deforestation for logging, mining, or agriculture can also emit Hg back into the environment as legacy emissions [66,67]. Research has documented links between deforestation and increased Hg exposure for fish and wildlife, such as a study that found that MeHg burden was higher for northern pike (Esox lucius) in lakes around logged areas than reference lakes [59].

3.3.2. Overfishing

The impacts of overfishing are exacerbated by changes in oceans due to climate change, which impact not only fish populations but also fish exposure to pollutants like Hg [59]. Overfishing can induce changes in marine trophic levels, thus affecting MeHg exposure of predatory fish. Historical data and modeling show that the overfishing of herring (Clupea sp.) led to species-specific trophic responses. In Atlantic cod (Gadus morhua), herring overfishing decreased MeHg concentrations as cod switched from consuming large herring with high MeHg body burdens to smaller herring with lower MeHg body burdens. However, the overfishing of herring increased MeHg in Spiny dogfish (Squalus acanthias), as dogfish switched from consuming herring to consuming cephalopods, which have higher concentrations of MeHg [68]. Similarly, a multi-decadal study of sea bird MeHg burden showed that the impact of overfishing and climate change on prey fish species led to a diet shift, causing increased MeHg exposure in birds [31].

3.3.3. Other Pollutants

Other pollutants can interact with landscape characteristics to promote or prevent the deposition and methylation of mercury. For example, sulfate deposition, especially in sulfur-limited environments, can increase the number of sulfur-reducing bacteria, which in turn can methylate mercury into MeHg, increasing the concentration of bioavailable Hg and increasing the levels of Hg accumulated in aquatic invertebrates [69].

4. Discussion

The biomagnification of mercury in wildlife is a culmination of dietary consumption of MeHg and physiological processes that govern the bioaccumulation of MeHg within the body [64,70,71]. In a study on arctic fish and invertebrates, only long-lived predators were at risk for mercury toxicity, highlighting the importance of an organism’s life history for mediating the risk of lethal and sublethal effects of mercury [72]. Wildlife managers will want to pay special attention to the condition and population health of high trophic level predators that feed in aquatic or marine environments since these species are the most likely to be exposed to high levels of mercury through their diet. At the same time, there are fewer studies of some lower trophic level organisms and evidence from broad spatial scale studies (e.g., [73]), which documents the relative importance of other factors such as biogeochemistry, landscape characteristics, and food web characteristics [74], pointing to the value of assessing multiple trophic levels as part of monitoring plans.

4.1. Case Study: The National Wildlife Refuge System

The United States National Wildlife Refuge System (NWRS) is the world’s largest network of lands and waters (~346 million hectares) set aside for the conservation of fish, wildlife, and their habitats [75]. NWRS units can be found in every state and all territories of the United States, from Alaska to the Caribbean, providing a continental scale system of conservation lands throughout North America. The system consists of 573 National Wildlife Refuges, 38 Wetland Management Districts, and 5 Marine National Monuments, which are managed under the purview of the United States Fish and Wildlife Service (USFWS). These areas serve as vital habitats for fish and wildlife that , support high levels of biodiversity and ecological integrity, and provide essential ecosystem services such as water filtration and purification. Many at-risk species rely on these lands, with research indicating that one-third of federally threatened or endangered species inhabit or depend on these areas ([76], Figure 2).

Lands are managed for the continuing benefit of the American people according to the National Wildlife Refuge System Administration Act of 1966 (16 U.S.C. 668dd-668ee) and the National Wildlife Refuge System Improvement Act of 1997 (P.L. 105–57). This legislation identifies conservation as the fundamental mission of the NWRS and ensures that the biological integrity, diversity, and environmental health of these areas are maintained. Additionally, the legislation recognizes compatible wildlife-dependent recreation, including hunting and fishing, as appropriate uses, with some areas designating these activities as priorities.

Although NRWS units are designated as protected areas, pollutants can still infiltrate via airways or waterways beyond their boundaries. While Hg has not been consistently or comprehensively studied across the NWRS, some research has been conducted. At Lostwood National Wildlife Refuge in North Dakota, researchers examined mercury concentrations in the eggs and nestlings of tree swallows (Tachycineta bicolor). Their findings indicated that mercury concentration was higher in eggs collected near seasonal wetlands when compared to semi-permanent wetlands or lakes, but no significant differences were observed in nestlings [77]. Additional research at the same location found that seasonal and semi-permanent wetlands consistently had the highest MeHg concentrations [78]. Meanwhile, a study at the nearby Glacial Ridge National Wildlife Refuge in Minnesota revealed that while wetland sediment samples contained typical total Hg concentrations, MeHg concentration was twice as high as those collected from locations outside the NWRS [79].

Wildlife studies have revealed that alligators (Alligator mississippiensis) with elevated Hg concentrations have lower body condition at Merritt Island National Wildlife Refuge in Florida [80]. Similarly, Hg tissue concentrations for largemouth bass (Micropterus salmoides) were significantly correlated with body condition for fish from Crystal Reservoir at Ash Meadows National Wildlife Refuge in southern Nevada [81]. Some studies have documented Hg decline over time, such as a long-term study on saltmarsh sparrows (Ammodramus caudacutus) at Rachel Carson National Wildlife Refuge in Maine that found blood Hg concentrations decreased from 2000 to 2017 [82].

Studies documenting elevated Hg concentrations on NWRS units have important ramifications for human health, as hunting and fishing are available on over 400 NWRS units. These areas are often known as “duck farms” since many complex water management processes are carried out to enhance resources (e.g., nesting habitats and food) specifically for waterfowl. An estimated 10–12 million waterfowl and migratory birds are harvested annually across North America, with about 3 million originating from NWRS units [83]. Importantly, many of these harvested fish and wildlife are consumed by visitors to these protected lands, creating a direct connection between Hg in these aquatic systems and humans. This reiterates the importance of addressing Hg concerns within a One Health framework, as wildlife managers have opportunities to engage with hunters and anglers on potential risks and ways to minimize contamination. This engagement can also lead to local communities participating in Hg monitoring programs.

4.2. Effects of Mercury on Wildlife Related to Physiology and Behavior

4.2.1. Dosing Studies

Dosing studies have estimated the median lethal dose (LD₅₀24 h) of MeHg over 24 h to be 11.9 mg/kg for rats, 22.4 mg/kg for hamsters (Cricetus cricetus), and over 17 mg/kg for squirrel monkeys [84]. While doses below the LD₅₀ range may not be enough to outright kill animals, there are sublethal effects to wildlife that can harm immune systems, neurologies, endocrine functions, and behaviors that can ultimately cause populations to decline [85,86,87].

4.2.2. Immunosuppression

MeHg exposure is a strong immunosuppressor in wildlife [88,89]. The prevalence of avian flu in various duck species increased with increased exposure to Hg [90]. Northern elephant seal (Mirounga angustirostris) mercury burdens were negatively correlated to the antibody immunoglobulin M levels and inflammatory response regulator cytokine IL-6 levels [91]. In harbor seals (Phoca vitulina), increased MeHg concentration was associated with reduced numbers of lymphocytes. In vitro exposure to MeHg increased cell mortality and decreased DNA, RNA, and protein synthesis [92]. In vitro lymphocyte growth and proliferation were reduced when exposed to HgCl₂ in brown watersnakes (Nerodia taxispilota) [93]. Newborn barnacle goslings (Branta leucopsis) exposed to Hg had reduced levels of natural antibodies and Hg-induced inflammatory effects [94]. Bird embryos with mercury contamination showed potential relationships with four different liver tissues’ gene expression, suggesting that Hg exposure may also impact organisms on an epigenetic level [95].

4.2.3. Endocrine Disruption

Mercury exposure is known to impact endocrine function in wildlife [88]. Thyroid hormones play significant roles in moderating life history events, and disruptions to the endocrine systems in juvenile wildlife can have permanent impacts on individuals as adults [95]. Adrenocortical and thyroid hormone responses to elevated MeHg concentrations have been documented in both tree swallow (Tachycineta bicolor) nestlings and rainbow trout (Oncorhynchus mykiss), although those responses depend on exposure amount, duration, and species [96,97,98]. Responses to exposure may not be linear. In river otters (Lontra canadensis), cortisol production decreases after a specific threshold of Hg is accumulated [99]. In pagophilic (ice-loving) diving sea birds, MeHg blood levels influenced a thyroid hormone associated with underwater foraging duration and depth. When the sea birds were stressed due to early sea-ice breakage, this reduced the time that the sea birds foraged underwater compared to years when sea-ice broke up when expected [100]. This demonstrates that mercury-induced physiological changes occur in the context of environmental change, which can elicit other hormonal changes, like stress hormone production.

4.2.4. Reproduction

Mercury contamination can affect individual-level reproduction. For example, sex hormone production was reduced in brown bullhead (Ameiurus nebulosus) exposed to Hg [98]. Increases in Hg cause decreases in prolactin, a reproductive hormone in common eiders (Somateria mollissima) [101]. When whole populations are exposed, this can cause an entire population to decline. In arctic birds, Hg exposure reduced reproductive output and threatened the entire population of the exposed species [89]. Increased Hg burdens were associated with loon (Gavia immer) and zebra finch (Taeniopygia guttata) reproductive output [102,103]. Without routine monitoring to determine that Hg concentrations were affecting the cause of population decline, this could not be accurately determined, and conservation efforts would continue to be undermined.

4.3. Changes in Mercury Exposure Related to Habitat

4.3.1. Migration

Migrating wildlife both import and export MeHg from systems, such as salmon [104,105] and sea birds [106,107]. Migrating individuals may also experience different exposure rates than their resident counterparts because different spatial locations, even in the same biome, have different mercury concentrations [108]. The Bicknell’s thrush (Catharus bicknelli) is exposed to higher concentrations of MeHg in their wintering location than in their breeding grounds [85]. In migratory birds, mercury exposure changes throughout the year, influenced by changes in diet and trophic position, environmental mercury levels, and energy expenditure [109,110]. In common eiders (Somateria mollissima), mercury concentrations were higher in migratory populations than resident populations, and researchers hypothesized this was because migratory eiders had access to and consumed higher trophic level prey than residents [111]. If patterns of migration change due to climate change (e.g., staying in wintering locations for longer or shorter periods of time or not migrating at all), MeHg exposure for migratory organisms may change.

4.3.2. Range and/or Diet Shifts

Northward range shifts because of climate change mean consumer-resource patterns are disrupted, which can alter trophic patterns. This may induce changes in an organism’s trophic level (increasing or decreasing it) or switching to a prey source with either higher or lower Hg exposure than the prey usually eaten. It is hard to predict what exactly will occur and how (and if) food webs may be rearranged [47]. However, it is well documented that shifts in diet lead to shifts in MeHg exposure [112]. For example, researchers proposed that changes in food webs in New York State lakes, either from environmental recovery from acid deposition or from stocking and the introduction of invasive species, lead to longer trophic chains and higher Hg concentrations in yellow perch (Perca flavescens; [113]). Similarly, the invasion of dreissenid mussels (Dreissena polymorpha and Dreissena bugensis) and declines in amphipod prey species in the Great Lakes caused predatory fish to switch from consuming zooplankton to small fish, thus feeding at a higher trophic level with higher MeHg concentrations [114].

4.4. Co-Exposure to Mercury and to Other Stressors

4.4.1. Other Contaminants

Organisms will likely be exposed to more than one pollutant, leading to in vivo interactions and complex interactions between contaminants. For example, exposure to both chlorpyrifos and MeHg increased MeHg accumulated in amphipods, as opposed to exposure to just MeHg alone [115]. Exposure to PCBs and MeHg had a synergistic increase on hepatic porphyria (genetic disorders that inhibit liver functioning) in quails (Coturnix japonica; [116]) and a synergistic decrease in dopamine concentrations on rat brain cells [117]. However, some interactions may be more positive and may mediate the effects of Hg. Selenium (Se) reduces the risk of mercury toxicity in organisms by binding to Hg to form the biologically inactive HgSe [118]. For example, leopard seals (Hydrurga leptonyx) with higher Se:Hg molar ratios had lower Hg concentrations than leopard seals with a lower Se:Hg molar ratio, demonstrating the importance of adequate Se in the diet to help counter a high Hg burden [119]. Because of the strong association between Se:Hg molar ratios and the risk of Hg toxicity, measuring levels of both contaminants may be useful for assessing Hg toxicity risk [120]. The Hg burdens of long nosed fur seals (Arctocephalus forsteri) were negatively associated with Se burdens, and Hg levels were strongly correlated with levels of the heavy metals Cadmium (Cd), Vanadium (V), and Silver (Ag), although no physiological effects attributed to those co-occurrences were recorded [121]. A negative relationship between arsenic (As) and mercury levels was recorded in freshwater fish, attributed to differences in the environmental conditions that promote the production of MeHg and the conditions that facilitate the form of As that bioaccumulates. No physiological effects of this interaction were observed [122].

4.4.2. Other Stressors

Beyond interactions between contaminant exposures, wildlife also face interactions among Hg toxicity and other stressors, such as climate change-induced effects on nesting [123], diseases and parasites, climate change-induced physiological stress [99], and changes to migratory habitats [89,106,109,124,125]. These interactions can exacerbate the already sublethal physiological effects of Hg exposure, further harming wildlife [123].

4.5. Management Actions That Could Potentially Alleviate the Effects of Mercury Exposure

We recommend four priorities for consideration when using a One Health framework to help mitigate the effects of Hg on wildlife (Figure 3). The One Health framework recognizes the inherent links between environmental health, wildlife health, and human health. It emphasizes collaboration, communication, and coordination across historically siloed sectors, including medical and public health, agriculture, environmental conservation, and wildlife management [126,127]. Our suggestions include prioritizing the investigating (1), monitoring (2), engagement (3), and prevention (4) of Hg in management actions and plans related to wildlife resources to help maintain and mitigate the harmful effects on the environment, wildlife, and humans (Figure 3). We recognize that wildlife managers are already juggling multiple responsibilities, and our intent is not to add to their workload. Instead, our suggestions build on routine activities to optimize their efforts in conserving fish, wildlife, and their habitats.

4.5.1. Investigating

Investigating dead organisms when feasible, through necropsies or tissue sampling, can provide wildlife managers with a deeper understanding of individual body condition and can help predict population demographics, which are critical for conservation success [128]. Wildlife managers can send tissue samples from carcasses out for contaminant testing, especially high trophic level aquatic predators, since contamination is often sublethal and not observable to the eye. For example, on two separate occasions, managers discovered Hg contamination in river otter (Lutra lutra) individuals through necropsy and tissue testing [128,129]. This can help managers estimate Hg exposure rates and determine if there is cause for concern. Additionally, managers can collaborate with hunters and anglers to identify wildlife carcasses and determine which should be sent out for testing.

4.5.2. Monitoring

Wildlife managers can engage in Hg monitoring as part of other routine management activities, regularly testing either invertebrates or fish for Hg concentrations when feasible and making sure these assessments include standardization for body size and species [130,131]. Time series data from monitoring combined with experimental analyses can shed light on how Hg and its interactions with other stressors impact wildlife populations [87]. Moreover, investigating spatial patterns of Hg contamination can help determine potential point sources for Hg pollution that may be affecting nearby wildlife [132], and this information can be used to help limit pollution in the future. Monitoring how Hg concentrations change over time and across space can help researchers determine the relationship between different biological, physical, and climate factors and Hg exposure in ecosystems, with the intent to help predict where and what wildlife and humans may be at risk for Hg toxicity [119,133,134].

One example is the Dragonfly Mercury Project (DMP), a national-scale program that uses dragonfly larvae as bio sentinels for Hg relative risk in national parks, wildlife refuges, forests, and other public lands [73]. More easily collected and analyzed than fish, immature aquatic dragonflies provide site-specific impairment indices developed by relating dragonfly Hg to other aquatic and amphibian biota, which provide long-term assessment of changes in Hg using a simple, standardized sampling protocol [73]. By monitoring these interactions across space and time through a One Health lens, we can utilize historically siloed surveillance programs to proactively understand where future increases in Hg levels might appear, thereby resulting in a predictable impact on environment, wildlife, and human health [135]. It may be that a local medical community could be the first to notice an unusual uptick in Hg-related conditions among patients, prompting cross-sector collaboration to identify a potential source and collaborate on solutions.

4.5.3. Engagement

Wildlife managers regularly engage with local hunters and anglers and can leverage these relationships to ask about the observed health and behavior of individuals, especially high trophic level predators that primarily feed in aquatic systems [136]. Additionally, wildlife managers can continue advising hunters and anglers on mercury levels to help prevent human exposure to Hg. Mercury advisory signage and outreach are commonly found near bodies of water that may expose fish-consumers to MeHg by consuming contaminated fish species (Figure 4). Assessing the effectiveness of these outreach efforts is paramount as we invest time and resources in public health education and prevention. Such studies have found, however, that Hg advisories can fall short of reaching their intended audience or desired goal [137,138,139]. Further, these advisories often focus on the impacts of MeHg exposure on human health and rarely speak to the health of wildlife itself.

One Health-oriented messaging can help to remind audiences about the interconnections between human health, environmental health, and wildlife health. For some audiences across the United States, this uplifting of the value and rights of wildlife informs individual decisions (see mutualist, [140]). There is further evidence that emphasizing moral norms and a responsibility to steward the landscape in outreach materials can positively influence recreationists’ behavior [141]. Cross-disciplinary collaborations with landscape ecologists and the public health sector, for example, can aid wildlife managers in designing effectively tailored messaging to reach a variety of audiences. Investment in building relationships with local hunters and anglers can broaden understanding of the impact of wildlife health and disease, which in turn can inform outreach efforts.

4.5.4. Prevention

Finally, wildlife managers can help prevent future Hg exposure by collaborating with partners to mitigate exposure at the source when feasible. Managers often partner with local regulatory agencies to re-evaluate permitting of high Hg emitting industries, even when the source is beyond their direct authority, to prevent point source Hg pollution. Additionally, wildlife managers and their governing agencies can choose to invest in non-Hg creating energy sources when these options are available. Coal-based power plants are the largest atmospheric Hg emitters in the United States [142]. Moving away from coal-based power sources and choosing to power any infrastructure with non-Hg emitting energy can reduce the Hg footprint of areas under the jurisdiction of a wildlife manager (e.g., wildlife refuges or habitat management areas).

5. Conclusions

Climate change will invariably influence the mercury cycle, which in turn affects the exposure of wildlife to Hg through a combination of abiotic and biotic interactions. The direction and magnitude of this change will be dependent on the degree to which climate change progresses, the climatic regime in each location, biogeochemical impacts on the Hg cycle, the species affected, and the ecosystem in which this plays out. Additionally, Hg exposure is mediated by human activities, like land use change and overfishing, other contaminants, and other stressors that may change under a changing climate. At the highest risk for increased Hg exposure are long-lived, high trophic level predators that feed in marine and freshwater systems. Wildlife managers, who play a vital role in conserving these organisms, can proactively plan and adapt to address these emerging challenges. We suggest that managers continue to engage with local hunters and anglers to track changes in populations, monitor mercury levels, investigate deaths of these high trophic level predators, and engage in preventative measures. Wildlife managers can mediate Hg exposure in wildlife by understanding the current pattern of Hg trends and making strategic decisions to prevent further Hg contamination in the face of climate change.