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Advances in Clinical Toxicology Research Article 77 min read

Monitoring the Health of Wildlife and their Ecosystems in the Arctic: Hg Toxicology and Stable Isotope

Dainowski BH* and Duffy LK*
* Corresponding author
ISSN: 2577-4328  10.23880/act-16000233  Received: January 28, 2022  Published: February 17, 2022
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Keywords
Toxicology Mercury Stable Isotopes Arctic Climate Change
Abstract

A major survival issue affecting wildlife ecosystems globally is climate change. Climate change fluctuations impact not only atmospheric weather, but also river watersheds and oceans, the health of animal populations, and the health of ecosystems as a whole. Arctic wildlife sentinels can be used as a proxy to monitor both ecosystem health and the health of Arctic subsistence users. In addition to a changing climate, the Arctic is a region of increased activity by the international mining industry. This One Health based literature approach integrates principles of environmental science, forensics, anthropology, physiology and geology, which will focus on toxicology (Hg) and feeding ecology (stable isotopes of δ13C and δ15N) of key terrestrial and marine mammal sentinel species. In the context of climate change, a forensic approach suggests a paleohealth (mercury) and paleodietary (isotopes) indicators in various animal tissues from museum samples as a baseline for future assessments of the impact of metals in food webs.

Introduction

One Health

In the far North, ecosystems and indigenous peoples are impacted by climate change. These impacts include, but are not limited to, significant health problems from the persistent organic pollutants, heavy metal accumulation and significant social and cultural changes related to survival [1].

Understanding this mosaic of processes both globally and locally requires an understanding of the array of toxicological processes for both terrestrial and marine ecosystems as well as the people living in this changing environment [2]. The extraordinary closeness of rural people to their land, which is absent in metropolitan communities, necessitates the interdisciplinary perspective of One Health in which contaminates impact the evolutionary healthy processes between animals, plants and the human social system [2, 3]. This One Health approach focuses on climate change, toxicants, and stable isotope studies for both terrestrial and marine mammals living in the Arctic regions.

As a One Health interdisciplinary approach develops diverse data sets, interpretation becomes essential about the key health interactions between animals, environments and humans. One Health collaborations among experts can improve research design and implement international policies and programs to help insure an optimal future for animals, ecosystems and humans [4, 5, 6, 7, 8, 9].

Climate Change

One of the major global issues affecting ecosystems is climate change. Global warming not only impacts terrestrial and marine populations, but also the physical environment which impacts ecosystem services [1, 10]. One high risk area that is being impacted is the Arctic where ecosystems are experiencing quicker and greater warming occurrences [11, 12, 13, 14, 15, 16, 17, 18]. The Alaskan Arctic and subarctic ecosystems, with their changing weather patterns due to climate changes as well as the increase of industrialization and mining activities release contaminants into the environment. The concentration of mercury (Hg) in animal’s food sources [4, 7, 19, 20, 21, 22] is increasing. These types of changes will have an impact on the health of specific species [23]. For example, mercury bioaccumulation in pristine tundra vegetation would have a significant negative effect on the health of Arctic biota [20]. Whereas, if temporal changes and sudden shifts are observed in stable isotope (δ13C and δ15N) values, this would signify that adaptation behavior is required, such as new locations for foraging or trophic changes [24, 25].

In addition to Alaska, another Arctic region is the Svalbard Archipelago in Norway. This area has become a noteworthy location for contaminants emitted in the Northern Hemisphere [10]. These contaminants arrive in the form of volcanic activities, soil dusts, sea salt aerosols and transport of anthropogenic emissions from lower latitude power plants. The anthropogenic emissions of contaminants seems to account for the greatest amount of pollutants [26, 27]. This is a global problem that threatens the Arctic ecosystems due to long range transportation and accumulation of contaminants [27, 28]. The tundra stores the atmospheric Hg disposition in permafrost and over time it migrates to the Arctic Ocean [29]. It has been found that about 70% of atmospheric Hg disposition occurs through gaseous elemental mercury that is initially taken up by the soil and vegetation [20, 29, 30].

A study conducted on Hg at the Toolik Field Station in Alaska was performed by measuring Hg in the atmosphere, soil pore air, and interstitial snow air, then characterizing the flux of Hg in the tundra ecosystems [29, 31, 32]. This study indicated that the uptake of Hg by ground vegetation of the tundra played the commanding role in the Hg cycling. For example, it was observed that lichen and moss accounts for half of tundra biomass and had high concentrations of Hg [20]. This absorption of Arctic tundra Hg will be continuing due to the ongoing greening trend and the warming associated with climate change [21, 29]. With the soil temperatures rising, leading to permafrost thawing, the Alaskan Arctic has an increased risk of remobilizing higher amounts of stored Hg [33, 34].

MacDonald and colleagues [35] reviewed the ecological effects of global climate change using Hg and persistent organic pollutants (POPs) pathways and their exposure in Arctic marine ecosystems. The exposure pathways of transported chemicals is detrimental to the overall health of terrestrial and marine wildlife in the Arctic. A transportation of this kind can present toxins to an otherwise healthy wildlife and rural human populations [1, 7, 23, 36, 37, 38, 39] as the climate changes, exposure is predicted to increase.

A prediction associated with a warming climate proposes that an increased precipitation at high latitudes will cause sea level rise and seasonal flooding [1, 40]. This fresh water discharge has the potential for the introduction of river- borne pollutants into Arctic marine ecosystems [41].

The appearance of infectious diseases in the polar regions has also been a factor related to climate change [36, 42], indicated by changes in Arctic species composition and the transportation of pathogens [43]. The survival rate of infected animals during warmer temperature winters will increase the risk from pathogens and metals like mercury to marine mammals, with eventual transmission to humans [44, 45, 46, 47].

Sea ice has also been decreasing for several decades (i.e. 1993 to now) in the Arctic Ocean due to climate warming [18, 36, 48, 49, 50, 51, 52, 53, 54, 55]. Because of the receding sea ice, there are direct and indirect impacts on the seasonal distributions of food, the patterns of migration over geographic ranges and the nutritional stress on marine mammals [16, 18, 36, 56, 57]. Climate warming trends also affect the Arctic by decreasing sea ice thickness [53, 54, 58]. This change in sea ice thickness affects species that rely on the presence of sea ice for pupping and molting [59, 60].

River watersheds play a key role in ecosystems as well as providing benefits in human civilizations. These river sheds are intrinsic to physical and biogeochemical cycles of aquatic biota as well as transportation waterways [1]. With the predicted change in climate, riversheds have the potential to change. For example, Hg is distributed across landscapes before it enters the ocean by a rise in river water levels [1, 18, 61]. Understanding the functions of less structured watersheds can be used as a barometer of the health of ecosystems and need an interdisciplinary research approach [1]. One way to monitor the health of watersheds is using wildlife to achieve insights into shifting stresses caused by Hg as well as industrial development [62, 63, 64]. Similarly, in marine ecosystems, the baseline δ13C and δ15N values will vary from offshore to inshore gradients as well as latitudinally [25]. Distinct spatial values will be identified (i.e. isoscape). These isoscapes can then be used to track movements and trophic interactions of species [65, 66, 67, 68].

The complex Hg cycle in the Arctic, e.g. remobilization of Hg stored in tundra, which is impacted by climate change, is a model that should be expanded to other toxic metals, including the rare earth elements. An urgency to monitor metal concentrations in precipitation, air, bodies of water, soils and δ13C and δ15N levels in food webs will increase the knowledge of the impact of global industrial activity, such as the production of raw materials. Monitoring will improve studies to determine if the patterns observed in different regions throughout the world, including the Arctic, will be similar across all species as the warming climate continues.

Mercury as a Tracer for Change in Metal Distribution

Some elements are seen as more toxic than other pollutants [69]. This viewpoint brings together diverse and multiple approaches to interpreting how chemicals shape humanity’s future [70]. Such viewpoints include, but are not limited to, the distribution and movement of chemicals related to people, wildlife, and nature, in order to learn and understand our ever changing environment.

One element that is of major concern worldwide is mercury. It is found in the environment in three forms: elemental (metallic), organic (methylmercury (MeHg)) and inorganic (mercury salts), where all three forms are toxic [71, 72, 73]. Globally, mercury is a pollutant that affects both ecosystem and human health [21, 72, 74, 75, 76] and is released into the environment by both anthropogenic and natural sources. The aim of the Minamata Convention on Mercury in August 2017, was for the reduction of global emissions to protect the environment and human health; as a result, it was approved by 91 countries [73]. Because of this convention, Hg needs to be continually monitored in the environment to determine if new measurements set by this treaty will reduce the impact of Hg on marine food webs in the future.

The atmosphere is the most important pathway of mercury deposition for redistribution to both the terrestrial and marine ecosystems [37, 74]. As anthropogenic elemental mercury vapor is transported via air currents from industrial activities, such as gold mining or coal-fired power stations, it accumulates in the animal’s respiratory system and/or on the food they ingest [77, 78]. Whereas natural occurring mercury dwells in the atmosphere for about one year and then is deposited on the Earth’s surface [72, 74, 76, 79]. For example, when permafrost and glaciers thaw in the Arctic, Hg is released into the environment [34, 80, 81]. How Hg is released into the Arctic environment is by a phenomenon called a polar sunrise during the springtime [82]. During this polar sunrise is when Hg in the atmosphere mixes with the lower ozone layer causing the Hg to be deposited onto snow packs at an accelerated rate [82, 83]. Then in the summer, when the snow melts, the Hg is released and found on soil and foliage, which can impact the health of wildlife through trophic level accumulation [1, 71, 82]. In addition, the terrestrial and marine ecosystems often show a higher accumulation of different compounds such as HgCl2, CH3Hg in their food webs [22, 84]. It is these forms of Hg that are a key benchmark for research. By understanding the mechanisms of mercury distribution, we can then address the metals effecting the diets of Arctic wildlife and the local environment in order to keep a healthy Arctic ecosystem [21].

Another effect of global warming is the quick hardening of small snow layers during the winter. This hardening of snow layers, called snow-pack, produces changes in ice properties. This change called ground icing, in turn, effects the vegetation caught under this hard ice layer [85, 86]. These changes in weather can create long term affects that impact the condition of vegetation, which in turn affects wildlife foraging profile and nutritional status [10]. For example, the ungulates in Norway are restricted in their food availability during ground icing which is caused by overgrazing [87]. This overgrazing causes the ungulates to increase their foraging areas, which causes an increase in environmental imprints. By increasing foraging areas, the ungulates ingest more undesirable food sources, e.g. goose droppings or algae from marine sources [88, 89].

In aquatic ecosystems, mercury is directly deposited via snow, rain and by soil runoffs into aquatic ecosystems [72, 73]. It is in these aquatic ecosystems where mercury, Hg, transforms into methylmercury, CH3Hg, biomagnifying through food webs. The marine fish and mammal’s health is impacted by the consumption of CH3Hg contaminated foods, which increases the trophic level transfers [5, 21, 39, 74]. This, in turn, affects the Indigenous Arctic populations, especially those who rely on seafood as a major part of their diet, where they are exposed to CH3Hg impacting their health [1, 22, 52, 74, 90]. These Hg cycles of deposition continues to increase the toxic load on a regional scale.

Hg as a trace element can bioaccumulate and biomagnify along food chains [73, 76, 91, 92]. The mercury methylation is by a natural bacterial process taking place in aquatic sediments [93]. The Arctic fish and marine mammals, specifically those at the top of the food web, will have high Hg burdens [92]. Lamborg and colleagues [94] estimated that the Hg burden in marine environments have tripled since the pre-industrial period. In addition, Dietz and colleagues [95] have estimated a 14-fold increase in Hg concentration in polar bear hair from Greenland between 1300 years ago and present.

Lavoie and colleagues [96] found bio-magnification rates to be approximately 6.0 ± 3.7 times for each trophic level in Arctic marine food webs. The tropical marine food webs were increased only 5.4 times at each trophic level [97]. The MeHg is transferred through the food web chain in fish more than other forms of Hg, similar to the way it is absorbed into fatty tissues [91, 73, 76]. In some tissues, it slowly metabolizes to inorganic Hg (HgCI2) [98]. The MeHg moves to the kidney, liver, spleen and eventually travels to the brain and muscles [99]. However, in the vertebrate gastrointestinal tract, inorganic Hg is weakly absorbed and leaves the body rapidly in urine and feces [100]. Evans and colleagues [101] also reported that MeHg is slowly eliminated from the body with a half-life of 10 to 15 days depending on the organ affected.

Research has shown that the patterns of Alaskan Native diets have shifted from a complete subsistence diet in pre- contact circumpolar populations to it’s current condition that includes more “Western” foods for these indigenous circumpolar populations [102, 103, 104, 105]. Concurrently, terrestrial and marine ecosystems have been measuring the impact of terrestrial ecosystems Hg cycling by toxicants over the last century, which led to the Minamata Convention. This global cycling of Hg affects not only the health of terrestrial and marine biota, but has a negative affect on human health. Monitoring is not only important because of the atmospheric Hg sink strength and it’s impact on Polar ecosystems, but also how quickly Hg is transferred from these ecosystems to Hg found in foods for human consumption. This has been shown in the Polar environment and how it has been impacted by both climate shifts and Asian industrial development [106].

When Hg is recirculated back into the atmosphere [21] via air and ocean currents, it causes the toxins to migrate to the poles. However, most of the remediation focus is on the more populated areas at lower latitudes. Whereas, the toxic effects from Hg circulating in the Arctic environment needs increased monitoring in order to assess the current and future health impacts (e.g. infectious and zoonotic diseases) on terrestrial and marine ecosystem.

Stable Isotopes

In order to properly assess the effect of global climate changes on diet and movements of terrestrial animals and marine mammals, the ratio of the stable isotopes of carbon and nitrogen values are applied [18, 25, 107, 108, 109, 110, 111, 112, 113]. The stable nitrogen isotope (15N/14N) has been used to identify food web trophic structures, i.e. the relationship of diet type to the ecosystem in which organisms live [1, 52, 112, 114, 115, 116, 117, 118]. Nitrogen isotope values are used to compare trophic levels [107, 112, 119, 120, 121, 122, 123, 124]. These trophic levels are described by Trites [125] as level 1-Algae and phytoplankton, level 2- herbivores and detritivores and levels 3-5 carnivores and omnivores including marine mammals; where each level is determined by what the animal consumes. In a paper by Hoondert and colleagues [113], they state the trophic level characterization of ecological communities should include one of three objectives: 1, to define the trophic patterns associations within an ecosystem’s community, 2, what components are affecting the grouping of these ecosystems, and 3, what are the pathways of nutrients, energy, and contaminants these animals are exposed to in specific ecosystems [126].

Stable isotope studies traditionally trace pathways of organic matter using δ13C and δ15N [127]. Different stable isotope ratios, (i.e.13C/12C), also arise in the photosynthetic pathways of C3 and C4 plants [128, 129, 130]. In Western and Arctic Alaska, the native vegetation is exclusively composed of C3 plants [131, 132]. There are some native C4 plants that are rare in Alaska, which include a few wetland rushes (Juncus), spikerushes (Eleocharis), and beaked sedge (Rhyncospora) as well as some coastal grasses such as saltgrass (Distichlis) [133].

These stable carbon isotopes are reflective of naturally occurring isotope values in animals’ diets and reflective of animals’ movement patterns [134, 135, 136]. This has been established in various studies of stable isotope ratios reflecting dietary sources from coastal, terrestrial, benthic and pelagic environments [137, 138, 139, 140]. For example, with the sea ice shifting due to climate warming, the biodiversity and distribution of marine mammals may shift toward the poles [141]. Also, coastal terrestrial animals that feed on fish can leave a 15N signal in coastal plants [142]. In regard to human movement patterns, distinguishing Arctic wild foods from processed store-bought foods can be established because of the difference in carbon isotopes [112, 122, 136, 143, 144].

In Arctic marine systems a high spatiotemporal intra- species variability in trophic level is exhibited, e.g. a system driven by seasonal fluctuations in light and temperature [145]. Changing peaks in abundance of primary producers and declining prey availability due to loss of sea ice in summer, lead to these changing trophic interactions among species in high-latitude marine environments; thus, affecting the trophic position and contaminant level of species [146, 147]. One such marine mammal that has been used to monitor changes in trophic positions from migration patterns is that of whales [148].

Stable isotopes of δ13C and δ15N can also be connected to toxins such as Hg during climate changes on ecosystems. As this increased warming phenomena continues in the Arctic, the weather will continue to stress the Arctic ecosystems and lead to both vegetation damage and the decline of wildlife health [39, 149]. During climate changes, precipitation moves Hg from the atmosphere cycling it back into the oceans and rivers and to the soils exposing more Arctic organisms to Hg

loads. Then as the climate warms, the sea ice cover decreases, which in turn increases the Hg levels in the atmosphere [39, 150, 151]. This melting of ice and snow releases an increased amount of Hg into the river watersheds which then leads to an uptake in Hg in food webs.

It is these applications of stable isotope values which provide information regarding the impact climate change has in informing or the distribution of species [1, 107, 111, 113, 152]. Additionally, stable isotopes not only informs about animals, but all historical indigenous human movement patterns in search for sustainable food supply [112, 153, 154].

Two Important Tissues Needed In Wildlife Monitoring Studies

As a consequence of climate change over the last three decades in northern latitudes, Alaskan wildlife and their ecosystems are experiencing the impact of global warming [155]. The larger animals in a region, such as moose, muskoxen and caribou, are experiencing conflicts with timing of resource availability and migration patterns, Funck and colleagues [19, 24, 156, 157, 158] have noted changes in caribou migration patterns due to warmer summers and winters. Additionally, elevated amounts of Hg have been observed in Arctic marine mammals such as the polar bear, seals, and whales, where Hg has threatened the health of these ecosystems [22, 91, 159]. Because these factors effect the lifestyle of both terrestrial and marine wildlife, innovative approaches in research need to be used. Specifically, there are two tissues that stand out amongst many others and are lacking in the literature, that is, bone and renal cortex and medulla. The more innovative approaches are used on tissues, the more essential information can be derived. In turn, this information can be beneficial in acquiring a more in-depth knowledge about the health of terrestrial and marine wildlife.

Role of Bone

Bone has not been widely used in research, mainly archival bones, yet provides valuable information [160]. Bone can be easily sampled and cataloged, thus providing a unique way to monitor the pathway of pollutants and diets from museum samples for past historical patterns. In this regard, bone can help to understand changes in the behavioral and health patterns in wildlife due to warming climate changes around the world, specifically the Arctic.

The main components which make up bone are hydroxyapatite (mineral) and collagen (organic) [161]. Bone is unique in the way it remodels itself throughout life [162, 163]. However, the remodeling rate is dependent upon an animal’s physiological factors and their age [164]. The bone collagen is used in stable isotope studies to infer the diet intake during recent years of life [112, 165]. Bone collagen and keratinized tissues are useful tools in under- standing migration patterns during periods of rapid climate changes, in both terrestrial and marine wildlife as each species will consume more than one kind of prey, with each prey uptake energy and nutrients from different sources in their particular ecosystem [52, 148, 166].

Diagenesis is the breakdown of bone and its interaction with the local physical, chemical and biological environment over time [167]. These processes modify the bone’s original structural and chemical properties and can either preserve or destroy the bone. It is the physical factors such as soil and climate, and chemical factors such as deterioration of the organic and mineral phases, as well as biological factors such as alterations that take place on the bone itself (when exposed to elements or in a burial context), that play a important factor in the diagenesis process [168]. Because bones are not in equilibrium with the soil solution of a particular environment, they undergo various chemical deteriorations [167, 169]. When bone is exposed to moist environmental conditions, a key agent of change is diagenesis. It’s altered states are in the proportions of the inorganic components (e.g. calcium, hydroxyapatite, magnesium) with the organic component (e.g. collagen). Other changes in bone take place and need to be considered. This is because various types of soil components are absorbed onto the bone surface and cause the components of the bone to leach out [168, 170].

It has been shown in various studies that bone can also be used to predict toxicant levels in soft tissue from Arctic animals [64, 171, 172, 173]. Also, in bone mineral, toxicants are actively absorbed and then released during bone remodeling [174]. Toxicants, such as Hg has a direct effect on the bone itself as well as an underlying effect on other organ systems when it is released. Bone collagen has a slow turnover rate [175], and was used in stable isotope research to infer the lifetime of a red fox’s diet [64]. We are fortunate to have some studies describing techniques for the preservation of bone, classification of soil environment, and detection of the factors in the environment which affect the preservation of bone [169, 176].

Role of Renal Cortex and Medulla

The kidney is widely used to monitor contaminant levels in Arctic animals. In the bulk of the literature, the kidney is digested whole (both cortex and medulla together) [177, 178, 179, 180, 181]. However, one study used an innovation approach of separating the renal cortex from the kidney medulla and analyzing each component of the kidney individually [182]. It is important to note, and to consider in future studies, that different structures in the kidney perform different functions. Therefore, these different structures can accumulate toxicants at different rates and amounts [183, 184].

Terrestrial Wildlife Studies

An important process for the animal community structure and their ecological relationships in an ecosystem is that of competition [10, 185]. Researchers have used the feeding ecology knowledge of Hg concentrations to indicate what small mammals, birds and/or fish as omnivores to know what they are consuming. This diet knowledge leads to an understanding of the overall health of these animal populations [64, 91]. In addition, studies have shown how monitoring the diet differences between trophic levels in wildlife, using δ13C and δ15N diet, can be used as biomarkers for regional availability of foods during climate change fluctuations.

Mercury

In the Arctic, foxes are similar to dogs and coyotes as they are also omnivores [71]. Therefore, red foxes (Vulpes vulpes) were used as a sentinel species to provide information about Hg concentrations and changes in exposure [64, 71]. Working together with local trappers in western Alaska, Dainowski and colleagues [64] evaluated 65 red fox tissues to see if total mercury (THg) concentrations of keratinized tissue, hair, and bone could predict total mercury (THg) concentrations in skeletal muscle, renal medulla, renal cortex, and liver. They reported the keratinized tissue of hair THg concentration had a compelling positive correlation with liver, renal medulla, renal cortex, and muscle. The THg concentration for males and females was reasonably predictive of THg concentration in the renal cortex and liver based on R2 values (R2 = 0.61 and 0.63, respectively). This study also used an innovative approach of separating the renal cortex from the medulla in the kidney, and analyzing the components individually. Their data indicated the cortex had consistently higher THg concentration than the medulla (~3:1). The separation of this tissue is an important consideration for future research. By monitoring the concentration levels in each kidney component, a more precise picture of the potential adverse effects from Hg can be obtained.

In another study of trapped foxes, Hallanger and colleagues [39] from Svalbard, Norway explored temporal trends of Hg in 109 Arctic foxes, over 11 trapping seasons between 1997-2014. The Arctic fox (Vulpes lagopus) from Svalbard, Norway has been shown to have among the highest THg concentration levels of any other apex animal [186]. This is because the Arctic foxes mainly feed from marine carcasses (e.g. seals (Phocidae spp.) in addition to their terrestrial animals (e.g. Svalbard reindeer carcasses (Rangifer tarandus platyrhynchus [187]. When Hallanger and colleagues [39] adjusted their study for sea ice cover, consumption of reindeer carcasses, and differences of δ13C, they found the THg concentration levels in the liver of the Arctic foxes increased by 7.2%. But, Hallanger and colleagues [39] found the THg concentration level increased in the ‘raw annual trend’ by only 3.5%. They also reported the THg levels had up to five-fold variation between trapping seasons. This study suggested how sea ice cover and food webs affect mercury concentration levels in an important organ, the liver.

Caribou (Rangifer tarandus) are also considered one of the main components of the tundra biome [188] in northern latitudes, including, Alaska [189]. Caribou and reindeer (semidomesticated caribou) diets consist of mainly vegetation, which includes lichens, that can accumulate contaminants from the atmosphere. Therefore, when caribou consume these lichens, they accumulate high concentrations of mercury [189]. Duffy and colleagues [189] research investigated the total mercury (THg) in the hair of both caribou and reindeer from the Seward Peninsula, Alaska. The Seward Peninsula is where total mercury (THg) has been defined as the aggregate of different forms of mercury that is found in tissues of terrestrial animals. They compared differences between a free-range diet and a pollock-based fishmeal diet. The freeranging reindeer’s average THg concentrations were 55.3ng/g; whereas, the fishmeal fed reindeer was 19ng/g. This research was able to show that the free-ranging reindeer and caribou feed on a diet of lichen, indicating a greater exposure to Hg. On the other hand, Pacyna and colleagues [10] used hair samples from the Svalbard reindeer (Rangifer tarandus platyrhynchus) to determine Hg concentration levels. Their research found very low levels which agreed with other published literature of lichen and moss in Svalbard. These two studies have clearly shown that different ecosystems in the northern latitude tundra biome’s are affected differently by climate changes.

Research conducted by Kalisinska and colleagues [76] used three mesocarniore species (piscivorous Eurasian otter, feral American mink and the invertebrativorous European badger of NW Poland) in their respective northern ecosystems to determine the THg levels for mercury contamination. Their investigation revealed that all three mesocarniore species were not significantly different in their livers and kidneys for THg. The Hg levels in the liver were non-significant between the American mink and Eurasian otter. However, THg concentrations were significantly higher for roadkill animals than the trapped American minks. Their study also indicated that the European badger, who lives in the floodplains, bioaccumulated Hg at higher concentration levels. Since this badger was from floodplains, Kalisinska and colleagues [76] could use this species as a bioindicator of mercury soil contamination. Therefore, further studies are needed in order to understand how to optimize not only the health of these wildlife animals, but also their specific ecosystem.

Stable Isotopes

Stable isotopes are used to provide trophic levels as well as the feeding ecology of each species. Nitrogen stable isotope (δ15N) analysis is often used for determining relative trophic position using a 3-5% increase in δ15N values with each trophic step [109, 114, 190, 191]. These increases in δ15N values may develop from various diet resources. The increases in δ15N will also depend on the tissue turnover rates [112, 192]. For example, in the liver and plasma of blood, the turnover rate is usually in the range of days, whereas, in muscle and red blood cells the turnover rate is usually several weeks to months [193]. If stomach and scat analysis is used for trophic positions, then the prey that was consumed, as well as the rate at which digestion takes place, should be known [194]. Additionally, the diversity among species, the condition of the ecosystem, and the baseline species [113] needs to be considered when applying tropic positions. The carbon stable isotope analysis (δ13C) is used to determine the source of carbon in a food chain, i.e. the feeding habits of animals [109]. For example, δ13C is used to reconstruct the diets, whether that is animal or plants, of a wildlife species. Something worthy to note, and has been demonstrated by Trites [125], supporting the strength of stable isotope studies is the use of biopsy samples, instead of the stipulation to kill an animal.

In the Arctic of western Alaska, research of stable isotope ratios of δ15N were used to assess trophic levels and δ13C ratios as indicators of regional variability of marine vs. terrestrial prey of free-ranging red foxes (Vulpes vulpes) [112]. Five tissues (hair, bone, muscle, renal cortex, renal medulla, liver) were used for this stable isotope study. This study found that hair, bone, muscle, liver, renal cortex and medulla tissues of the red fox were isotopically different [112]. In addition, Dainowski and colleagues [112] observed a correlation between δ15N values and THg concentrations of hair. The hair δ15N values varied between 5.00 and 7.00‰, as the THg concentrations varied between 1.00 and 3.00 ppm. This revealed a link between δ15N and THg, by showing when δ15N increases, THg concentrations also increase. Further studies in the correlation between δ15N and THg needs to be addressed during climate warming in order to assess if any health changes of wildlife are taking place in this Arctic region.

In the Arctic of Svalbard, Norway, the soil nitrogen pools and differences in vegetation have been impacted by climate changes and soil moisture during the growing seasons [10]. Pacyna and colleagues [10] investigated if diet variations could be seen in the hairs of the Svalbard reindeer (Rangifer tarandus platyrhynchus), a key species in their region. Their research pointed out a high variability of δ15N, which suggests the reindeers were consuming vegetation with various δ15N values. Because the δ15N values indicated high variations in the isotope signatures, this indicates that the High Arctic tundra does retain the nitrogen signature that has been transported during weather events [195].

Hallanger and colleagues [39], used innovative research with their Hg study, by using δ13C as a substitute for both terrestrial and marine feeding ecology. They found that the δ13C ratios in muscle tissues of Arctic foxes from Svalbard Norway mirrored the fall and winter feeding habits and were produced by a diet of 1-2 months before death [116]. They also found that the δ13C values did explain the increase in THg levels and thus can be used a predictor in feeding habits of sea ice cover and reindeer carcasses in Arctic fox livers. This study also revealed that the Arctic foxes food consumption of a marine diet exposed them to higher levels of THg than those foxes feeding on a terrestrial diet, and was in line with other studies [142, 196, 197].

Marine Mammal Studies

Environmental pollutants, such as Hg, along with a warming climate, threaten marine mammals more so than any other mammals in the world [91, 92]. Because of these impacts on the environment, questions need to be addressed, such as: what impact will climate warming have on marine mammals in the Arctic, and, what impact will the increase in activity of Hg in Arctic waters, where sea ice levels fluctuate, have on the health of these marine populations. Research needs to continue to monitor, heavy metal (Hg) changes, and migration patterns (δ13C and δ15N), in order 1) to observe and maintain terrestrial mammals at a nutritive equalibrium for optimal health and 2) in order to protect the decline of marine populations.

Mercury

A serious issue which impacts both the health of Arctic indigenious populations as well as Arctic ecosystems, on a global scale, is that of mercury contamination. Once mercury leaves the atmosphere and enters a water system it converts to methylmercury by the way of bacterial processes. Once in the waters, methylmercury is one of the most toxiferous admixture that bioaccumulates and biomagnifies at a very high rate along the food chain in marine mammal ecosystems [91, 92]. Therefore, any wildlife animals, fish or birds that consume a marine or sea ice based diet may be at risk from the toxic MeHg levels, as MeHg is known to cause neurochemical, reproductive, and even behavioral changes in fauna [198].

Tilson, Das and colleagues and Roos and colleagues [199, 200, 201] have defined neurotoxicity as “an adverse change in the structure or function of the central and/or peripheral nervous system, following the exposure to a chemical, physical or biological agent”. It is the loss of neurons and gliosis, a variation in the cerebellum, along with, motor and sensory defects, which causes behavior changes from high amounts of MeHg intake [73]. The neurotoxicity caused from MeHg, depends on many factors, such as: 1, the nutritional health of the marine mammal populations; 2, the degree of exposure; and 3, how each mammal metabolizes and excretes the toxin [92].

Another general concern among scientists is that of the transfer of MeHg crossing the placenta [202], and the resulting Hg concentrations in fetal brains [203]. In a systematic study by López-Berenguer [92] MeHg can cross the placental barrier of pregnant marine mammals and accumulate in the fetal bloodstream; in turn, crossing the blood-brain barrier. Their study agreed with Evans and colleagues [101] confirming that inorganic Hg and MeHg can cross the blood-brain barrier, thus resulting in neurotoxic effects in marine mammals. These developmental risks of neurotoxicity can affect the future health of generations of marine mammals and therefore a high priority is needed to study, research and publish on the effects of MeHg in marine mammals and in their ecosystem.

The bioaccumulation of MeHg has also been shown to increase in Northern latitudes as a result of climate change [5, 91]. With climate warming, the lower sea ice levels facilitate dietary changes associated with higher Hg levels in some populations of marine mammals, such as polar bears and ringed seals [35].

The adipose tissue and blood from key marine mammal species such as polar bears and ringed seals have also been analyzed for the purpose of studying spatial and temporal trends and human exposures to contaminants in the Arctic areas of Greenland, Alaska, and Canada [7]. These studies of free-ranging animals suggest high Hg loads in the Arctic, which, in turn, creates an immune suppression in which the body does not have the ability to respond to infectious pathogens [80].

As part of the human exposure of Hg, sea otters (Enhydra lutris) are part of the Native Alaskan hunt for subsistence foods [204]. As scientists, by working in conjunction with these Alaskan hunters, we can use the sea otter to serve as a keystone species for the health of their community structures, as well as, marine ecosystems [205, 206, 207, 208]. Sea otters are a good species to study as they live in small home areas and their prey, for example, clams (Bivalvia sp.), crabs (Dungeness) and sea cucumbers (Holothuroides sp.), is sedentary which mirrors the contamination of their local environment [204, 207, 209, 210, 211, 212]. A group of researchers [204], in Icy Strait, Alaska, worked with the local Alaskan Native subsistence hunters and collected four females and 10 male sea otters. Brown and colleagues [204] analyzed the sea otters liver, gonad, brain and kidney tissues to determine the THg concentration levels. The THg concentration levels in the kidneys and livers were the highest. The average concentration of THg in the kidneys of these sea otters were 30 times greater in comparison to the kidneys of sea otters from South-central Alaska [204, 210].

Stable Isotopes

Hoondert and colleagues [113] studied the trophic levels of Arctic species using pelagic and benthic food webs in four areas of the Arctic, including Alaska. They determined intra-sample, intra-studies, and inter-region variations of trophic levels. A statistically significant difference (P < 0.05) in species trophic levels between these areas was reported. Their findings supported the nitrogen isotopic baselines as established by Carscallen and colleagues [213], where the corrected trophic level is 3.17 ± 0.88 and trophic level estimates are 3.32 ± 0.79 for Arctic areas. However, they did find the variability in trophic levels was higher between region verses within one region for both benthic and pelagic food webs. Since a single region is not suitable as a baseline for the Arctic as a whole, this inter- and intra-study provides valuable information showing how one vast area called the Arctic, actually constitutes different ecosystems with different trophic levels depending on spatial, seasonal and temporal influences [113].

Using trophic levels of stable isotope analysis, feeding relationships can be established; where one species competes for food more than the other species [125]. Trites [125] found that pollock and baleen whales overlap in their diets by 73- 86%. Whereas toothed whales compete for food with beaked whales and seals, and sea lions compete with large flatfish, toothed whales and seals. He found that fish are the largest part of competition among these marine mammals. In his study of trophic levels, Trites [125] found marine mammals to be in the following trophic levels: manatee, level 2, baleen whales, level 3.35, sea otters, level 3.45, seals, level 3.95, sea lions and fur seals, level 4.03, toothed whales, levels 4.23 and at the top of the food chain - polar bears, at level 4.80. His study was useful in understanding how many species, like fish, can occupy the same, or higher, trophic levels of marine mammals, and thus both species are competing with each other for the same foodweb.

Stable isotope ratios are also used as biomarkers to determine the diet differences among ringed (Phoca hispida), bearded (Erignathus barbatus), and harbour (P.

vitulina) seals in the Hudson Bay subarctic marine ecosystem [107]. Their study revealed that adult bearded seals had significantly lower δ15N values in muscle than the pups. Conversely, ringed seals pups had lower δ15N values than the adults suggesting foraging differences in trophic food positions for both species was age specific. On the other hand, δ15N values were not significantly different. The δ13C values were significantly different for different ages of harbor seals. Muscle δ13C values supported the conclusion that bearded seals are benthic feeders and are feeding in a separate food web from harbor and rings seals. For δ15N, harbor seals had the highest levels. This high level indicated their prey came from a higher trophic level relative to ringed and bearded seals. Young and colleagues [107] concluded that the δ13C and δ15N values exhibit the partitioning of resources among, and indicated evidence of separation of life stages within, these three seal species.

Keratinized tissues are widely used in isotope studies due to the non-invasive method in obtaining a sample. Crain and colleagues [55] used the keratinized tissue of claws from bearded (Erignathus barbatus) and ringed (Pusa hispida) seals because their claws can store up to 14 years of sequential data. These claws are two tone in color, where these colors indicate seasonal diets; for example, the light bands are produced in the last spring to last summer and dark bands are from early fall to early spring [214, 215] . In addition, the closer to the tip of the claw represents the age of the seal when they were younger [55]. Stable isotopes in claws can also reflect the stomach content of bearded and ringed seals; and therefore, helpful to evaluate diet and reproduction [55]. Connecting these life history parameters through time adds to an understanding of the overall biology of these marine mammals [55].

Other keratinized tissues used in analyzing nitrogen levels, is that of whiskers and baleen. Whiskers and baleen can provide an insight into the timing of diet shifts in marine mammals, a look into their life history of dietary information [125]. By measuring the carbon ratio’s of baleen from the bowhead whale, Trites and colleagues [125] were able to show that the ocean productivity, and overall carrying capacity, was lower and may have had an affect on the decrease of northern fur seals, harbor seals, and steller sea lions from the Bering Sea in the northern part of the Pacific ocean during the 1970’s through 1990’s. This study was useful in detecting this rearrangement of the ocean’s capacity as well as the diets of marine mammals.

In addition to baleen and whiskers, the whale’s earplugs, a plug of waxy material that forms in the ear canal by the accumulation of cerumen [25], can also give a comparison to the timing of diet from stable isotope analysis. These dark and light growth layers (bands of laminae laid down yearly) are used to age the baleen whales. Mansouri and colleagues [25] reconstructed δ13C and δ15N in earplugs over the lifetime of three species of baleen whales: fin (two Balaenoptera physalus), blue (two Balaenoptera musculus), and humpback (two Megaptera novaeangliae). They reported that the earplugs revealed inter and intraspecies differences. These differences showed that the mean lifetime δ13C values from blues whales was more depleted than fin whales. This dataset did provide a lifetime history of changes in foraging locations or trophic positions as well as ecosystem changes associated with the Suess effect [25]. As the nitrogen levels change in the whiskers, baleen and earplug tissues, it can also provide both an association with climate change and oceanographic occurrences [25, 166]. Furthermore, comparison of time series stable isotope profiles from baleen whale earplugs, with regional and global external datasets such as sea surface temperature and chlorophyll concentration, could provide a proxy for change in marine productivity in association with climate change and oceanographic events [25, 166].

Forensic Studies

Investigating forensic wildlife toxicology plays an important role in providing information about the biological effects of contaminants in the environment worldwide. Contaminants may bioaccumulate and biomagnify, entering into food webs, thus having adverse effects on both wildlife and in many cases, humans. Understanding how contaminants move through food webs is imperative for the health of the ecosystem, wildlife health, and as a variety of terrestrial and marine wildlife serve as subsistence food for indigenous populations in the Arctic.

Forensic science uses analytical techniques and observations to measure data from wildlife remains. The commonly used techniques include toxicology and stable isotope analysis of animal bone [216, 217]. As the impact of mercury (THg) to the environment is continuing, due to climate warming, Hg has the ability to build up in organisms and food webs, causing a significant negative influence on the health of animals. Understanding THg contamination in the environment can help prevent it’s ecological effects on biological diversity which lead to the damage of ecosystems in Arctic regions [1].

Through the study of δ13C and δ15N analysis, time- series datasets from a variety of animal tissues can provide opportunities in reconstructing past ecosystems [218, 219]. The stable isotopic (δ13C and δ15N) composition of animal tissues establish a relationship between diet, geographic location and trophic levels in archaeological and palaeodietary studies [216, 217]. Historical diets and trophic status of animals, relative to their prey, can be seen through current climate changes [67, 220, 221]. For example, how animals, at both the individual and population levels, respond to environmental changes through time [134, 222, 223, 224, 225, 226].

When studying climate change, Polyak and colleagues [227] stated there is a lack of understanding in how Arctic ecosystems respond to long periods of climate change. In response to this, Szpak and colleagues [16] stated that we need to rely on a variety of proxies living in past ecosystems to see how wildlife has responded to those changes. It is the archaeological record that gives the researcher an opportunity to investigate biotic responses, predict a historical baseline for current ecosystem changes, and to develop education and adaptation strategies [16].

Paleo-Health (Mercury)

One forensic approach for assessing THg concentrations over time (millennia) based on museum samples to use this information as a foundation for future assessments of THg in food webs [52, 173], is a study by Dainowski and Duffy [173]. They examined two Arctic foxes and three red foxes of unknown age and origin, and found the Yukon Territory Arctic foxes bone THg concentrations were 0.017 and 0.025 mg/kg; and the red foxes bone THg concentrations were 0.010, 0.036 and 0.073 mg/kg. They concluded that total mercury (THg) concentrations of bone-based tissues will be able to predict the possible THg concentrations in skeletal muscle, renal medulla, renal cortex, and liver of that animal over different time epochs from a previous study with red foxes [64].

Gerlach and colleagues [19] examined THg in caribou hair from two houses in a Western Thule archaeological settlement in Alaska. The settlement was the Alaskan Native community of Derring, which was dated ca. AD 1150 [19]. They found it yielded information about the temporal trends of human subsistence users exposure to mercury through caribou harvest times [19]. The caribou hair THg average value was 86ng/g, the same range as indicted in modern caribou and reindeer (Rangifer sp.) [19]. The caribou hair found in the first home had a THg level of 99.6 ng/g; whereas, the caribou hair from the second home had THg levels of 64.2ng/g. Since lichen is a normal diet for caribou; Gerlach and colleagues [19] suggests that the compositional changes in the lichen, THg, could account for the variations found in the hair mercury values. This type of data gives a good overall picture of a historical ecosystem [19].

Bones from marine mammals can be used in stable isotope studies to reconstruct ancient food webs by identifying the prey in a study of the sea otter’s diet [1, 228]. Since the habitat of sea otters (Enhydra Lutris) in the Arctic waters of Alaska encompasses a long stretch of the Gulf of Alaska, Duffy and colleagues [228] compared modern sea otter bones for mercury concentrations to that of sea otter bones from the early Holocene period. By using both mercury and stable isotope studies, they found the diet of these mid- trophic level modern sea otter bones comprised mainly of a benthic diet. However, the ancient bones had higher levels of mercury and δ15N values indicating a rising sea level, followed by a period in which ice sheets covered large parts of the earth [228]. Brinkmann and Rasmussen [229] suggested that these sizable increases may be associated with the sea levels rising. This rising sea level shifted the mid- trophic level sea otter to one of an upper-trophic level during the Holocene epoch. Studies like this can then be applied to present day climate change concerns in order to maximize the potential for a healthy ecosystem and wildlife community.

Paleodiet (Isotopes)

Stable carbon and nitrogen isotope ratios of bone collagen are used to establish foraging and movements of wildlife and human populations [64, 111, 112, 173, 230, 231]. Assessment of parameters such as collagen yield and composition is important to assure the quality of stable isotopic data [232]. Measurement of these parameters is particularly important for analyses of specimens from zooarchaeological assemblages, as poor preservation and diagenesis may degrade collagen and impact stable isotope ratios [232, 233]. Additionally, C/N ratios provide information about whether lipids were effectively removed from a sample during collagen extraction. Failure to remove lipids from bone will result in more negative δ13C values and may cause an underestimation of the dietary contributions of C4 plants or marine foods [232]. Understanding these differences is important as this information might allow researchers to exclude any bones from analysis that are unlikely to be representative of the whole skeleton.

It is important to note that the skeleton of animals who have lived a long life, will only reflect differences in stable isotope ratios if their feeding location or diet changes considerably [111, 114]. Whereas animals having a repetitive diet, their stable isotope ratios will stay the same, regardless of the turnover rates in bone [115]. The faster or slower turnover rates in bone only show differences in stable isotopic ratios of the bone collagen if the food consumed by the animal changed during their lifetime; either by movement, geography or diet [222].

Funck and colleagues [158] examined a steppe bison (Bison priscus) skeleton that was excavated in Alaska’s Northern Arctic region. Using radiocarbon dating on the keratin tissue of the horn, the age was determined to be ~46,000 ± 1000 cal yr BP. They also employed δ13C and δ15N analyses of the same horn keratin to establish a seasonal cycle, and found these values: δ13C - 20.0‰ (±0.6) and δ15N - 4.2‰ (±0.1). They concluded that the high δ15N values were consistent with that of modern day bison, however, as the ecosystem changed, the bison began dispersal and faced significant nutritional stress. Whereas, the δ13C value was consistent with the bison continuing a diet of C3 plants. Funck and colleagues [158] came to the conclusion that the past bison might have lived in an interstadial period and possibly under stress in harsher winters than what is seen today in Northern Alaska’s Arctic. Since this study is signifies that climate changes have taken place in the Arctic landscape overtime, more forensic studies need to be conducted in order to monitor the impact climate change is having on current wildlife and food sources for Native Alaskan communities.

Goude and Fontugne [24] studied δ13C and δ15N levels in bone collagen of carnivores, omnivores and wild herbivores from Liguria in NW Italy and France during the Neolithic period. They found significant correlations between latitude and δ13C for all groups and latitude and δ15N for wild herbivores. The wild herbivores in northern France had lower δ13C values and higher δ15N; whereas, the omnivores had just the lower δ13C values. Their study added new data for the Mediterranean and Western Europe, and the prospect of nitrogen to be used in environmental studies during the Neolithic period.

Another forensic research approach looked at the paleo- dietary (isotopes) indicators in preserved museum bone collagen of the red (Vulpes vulpes) and Arctic fox (Vulpes lagopus), from a Yukon watershed [173]. This study was designed to 1, establish information on reconstructing a diet using carbon stable isotopes and 2, establish a trophic level using nitrogen stable isotopes, for these sentinel species [64, 112]. Because of the small sample sizes, two red fox bones, and three Arctic fox bones, as well as different bones (i.e. femur, tibia, mandible) being analyzed, and no indication of the sex of the foxes, it had no statistical analysis value. Stable isotopes means and standard deviations only gave a visual perspective on what a diet might look like. The δ13C levels were -21.13 and -21.36‰ for Arctic foxes and -20.05, -20.08, and -23.12‰ for red foxes. Their δ15N levels were 5.59 and 7.22‰ for the Arctic foxes and 6.10, 6.57 and 6.66‰ for red foxes. The diet of the two Arctic foxes and two of the red foxes from the Yukon Territory Fossil Collection tend toward a salmon diet, while the third red fox showed a terrestrial mammal diet [173]. The trophic levels indicate these red and Arctic foxes from the Yukon Territory are similar to other red foxes in the watershed, tending toward a slight salmon diet [173].

The NW Coast of Canada was an important area of glacials in Late Pleistocene times [118]. Refugia locations identified for the survival of species were on the outside limits of the Cordilleran Ice Sheet during the Wisconsin glaciation period MIS 4-2. The refugee is now NW Canada and SE Alaska [234]. Kubiak and colleagues [118] reported on collagen samples from an antler fragment dating to the Fraser Glaciation (MIS 3). The collagen isotope values revealed Rangier were consuming a large amount of seaweed, indicating little foraging opportunities during the time period of antler growth [118]. The findings of seaweed consumption further indicated that Caribou herds were unable to break through ice or deep snow drifts to access the resources, especially terrestrial resources, needed for their diets [235]. Events taking place, like MIS 3, indicate climatic change impacts such as hard snow packs due to extreme winds which would delay springtime growth [236, 237].

Clark, et al. [111] studied the variability of δ13C and δ15N in skeletons of Alaska marine mammals to regulate if there were any methodical differences in stable isotope ratios among the skeletal elements. They used the crania and mandibles from 11 Pacific walruses (Odobenus rosmarus divergent), 10 adult ringed seals (Pusa hispida), 9 juvenile seals (Phoca), and 8 adult sea otters (Enhydra lutris). They found no significant differences among the walrus cranium/mandible pairs. They did find a greater variability, exceeding 1.0‰, across seal and sea otter skeletons. Clark and colleagues [111] did remove distal appendicular bones (calaneus, metatarsal, and phalanx) as well as the scapula and vertebra from the rest of the bones in the sea otter. They found by removing these, ‘extra’ sea otter bones from their analysis, the overall variability was greatly reduced in all three animals. This indicates that individual skeletal bones from individual animals can result in different δ13C and δ15N levels, which could be based upon bone turnover rates [112] and thus should be reported separately. This innovative study confirms the study conducted by Newsome and colleagues [222] in that turnover rates in bone will reveal different stable isotopic ratios in bone collagen as the animal changes environments and consuming a different diet during their lifetime. This change in diet could confer a change in climate during this time causing the marine mammals to change their movement patterns.

Szpak and colleagues [16] reported δ13C and δ15N values for bone collagen from marine mammals at different archaeological sites on Kotzebue Sound, Alaska, dating around A.D. 1170-1813. They compared modern mammal bone collagen samples from the same areas to determine trends over time for sea ice productivity and foraging ecology [16]. Between the 19th and 21st centuries, they observed significant changes in δ13C and δ15N values of ringed seals. The large decline in δ13C suggests a reduction of ice algae and organic matter to the benthos in the recent warming trend in the Arctic. These events influence the foraging ecology of these marine mammals [16], and in other areas, such as the Bering Sea to the south, and where climate changes are moving more towards subarctic conditions [16].

Ecosystems

With climate changes currently affecting ecosystems in the Arctic, it is important to establish a baseline for toxicants and stable isotopes in order to identify any future changes that may affect not only wildlife health but that of the indigenous populations. A focused forensic science approach which uses observations and analytical techniques provide data for One Health programs. The One Health techniques should include both toxicology and stable isotope analysis of wildlife tissues and the environment. Since the impact of metals on the environment is increasing, a significant influence on the health of organisms can be expected. Understanding THg and other metal contamination in the environment can help reduce ecological effects on biological diversity in Arctic ecosystems. Stable isotopic studies have shown that the δ13C and δ15N composition in animal tissues establishes the relationship between diet, geographic location and trophic levels in archaeological and palaeodietary studies.

In a study of the Hudson Bay area, a subarctic ecosystem that has seen changes in the environment due to the warming climate, Young and colleagues [107] noted that some species of marine mammals may consume different foods, or compete for the same foods, or change their feeding areas completely [36]. Their study noted that Hudson Bay ice cover is receding. They suggested that the ringed (Phoca hispida) and beard seals (Erignathus barbatus), who have adapted to the presence of ice cover, may decline in numbers. In contrast, the harp (P. groenlandica) and harbour seal (P. vitulina) populations would increase [238].

Murray and colleagues [52] conducted a study of THg concentrations in marine fish off the Gulf of Alaska that spanned the Holocene period. This study related the increasing sea level and associated this increase with coastal flooding and with Hg bioaccumulation in the marine food webs. This suggested the early human coastal populations would have been exposed to higher levels of mercury in their subsistence food during the Holocene when mercury was not linked to industrial mining activities. This increase in mercury mobilization was caused by a rise in sea levels due to glacial melting which eventually submerged Beringia [52].

Mercury has also been observed in high apex marine mammals of the Arctic, the polar bear (Ursus maritimus). The potential for long-term accumulation of contaminates can be found in their lipids, in the subcutaneous layer (known as blubber layer) [91, 239, 240]. Other marine mammals affected are the beluga whales (Delphinapterus leucas), hooded seals (Cystophora cristata), pilot whales (Globicephala melas), and the toothed whale [91], where they also accumulate contaminants like Hg. However, the baleen whales (Mysticeti), like the bowhead whale (B. mysticetus) which feed at lower trophic levels, do not show the same degree of a high climatic imprint [104, 148].

Conclusion

Changes continue to occur in the Arctic and is a reality, as it has been witnessed by many studies on the wildlife populations. The Arctic is changing more rapidly than other parts of the world. The warming of the Arctic will have consequences worldwide, through precipitation patterns causing low changes in sea levels. We expect changes in movement patterns and/or loss of wildlife and marine mammals. These changes of migration patterns and movements, or loss of animals entirely will impact the Alaskan Natives who rely on these animals for survival. We strongly support that wildlife and marine mammals can be used as models to understand the effect of diet changes over time. The association between diet (δ13C and δ15N) and contaminants (THg) to monitor climate change (temporal and regional) can inform on the health of wildlife and marine mammals and their ecosystems. Since bone usually survives in archaeological and paleontological sites world wide, bone has an important role as another valuable tool for monitoring metals, while stable isotope applications can reconstruct health patterns over time. A One Health approach allows scientists, veterinarians, medical professionals, or local hunters and fishermen to collaborate together in order to develop common goals that will benefit our world. Wildlife managers can then move this beyond “monitoring” to data based adaptive system management.

Data Availability

Data is available. The authors used published, peer- reviewed articles for this review.

Conflicts of Interest

The authors declare the absence of any competing personal relationships or financial interests that could be construed as potential conflicts of interest in this paper.

Funding Statement

This work was supported by the Alaska INBRE program, National Institute of General Medical Sciences of the National Institutes of Health under Award Number [P20GM103395].

Acknowledgements

The authors would like to thank the trappers that submitted carcasses to ADF&G, Dr. K. Beckman of ADF&G, Dr. S. Long of NIST, Dr. Julie McIntyre, Dr. Paul Layer, Dr. Kriya Dunlap, Mary Van Muelken, and Bournemouth University Forensic Department - England.

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@article{dainowski2022,
  title   = {Monitoring the Health of Wildlife and their Ecosystems in the Arctic: Hg Toxicology and Stable Isotope},
  author  = {Dainowski BH* and Duffy LK},
  journal = {Advances in Clinical Toxicology},
  year    = {2022},
  volume  = {7},
  number  = {1},
  doi     = {10.23880/act-16000233}
}
Dainowski BH* and Duffy LK (2022). Monitoring the Health of Wildlife and their Ecosystems in the Arctic: Hg Toxicology and Stable Isotope. Advances in Clinical Toxicology, 7(1). https://doi.org/10.23880/act-16000233
TY  - JOUR
TI  - Monitoring the Health of Wildlife and their Ecosystems in the Arctic: Hg Toxicology and Stable Isotope
AU  - Dainowski BH* and Duffy LK
JO  - Advances in Clinical Toxicology
PY  - 2022
VL  - 7
IS  - 1
DO  - 10.23880/act-16000233
ER  -