Abbreviations: DM: Diabetes Mellitus; CVD: Cardiovascular Disease; MeHg: Methylmercury; ROS: Reactive Oxygen Species; Hg: Mercury

Climate change will have an impact on global environmental health and many regard climate change as a major global challenge to reducing disease [1-3]. Disease is part of the concept of health which is broadly defined as a state of dynamic balance in which an individual’s or group’s capacity to cope with the circumstances of living is at an optimal level. The freedom from disease or the risk of contracting one is only part of the modern concept of health, which involves complete physical, mental and social wellbeing [4]. The causes of human disease are varied and result from a combination of environmental, physiological, genetic, lifestyle, and socioeconomic factors acting over the lifetime of an individual. A changing environment is a factor in the initiation or spread of disease [4]. Recent research demonstrates the importance of socioeconomic factors in producing disease, and the recognition that these socioeconomic factors in combination with physical environments (light, temperature, seasonality and pollution) and biological phenomena, like pathogens, need to be understood in a holistic way.

The concept of a complex process is key to understanding environmental health for people inhabiting our planet, which includes marginal and extreme environments. Environmental health focuses on the interrelation between human wellbeing and the health of other species in an ecosystem. Water and air, contaminated with endocrine disruptors, toxic metals, and impacted by both biological terrorism and climate change, pose serious issues in a world in which human systems have become agents of change that affect rural and natural landscapes. Environmental wellbeing refers to the ability of the environment to support all life, including human economic and social systems. The efficiency and sustainability of environmental services, the cycling of materials and the maintenance of organismal balance are needed to reduce the incidence of disease. People have diverse cultural and social systems, but experience common health issues related to living in various environments with nutritional and seasonal stresses. A person or population’s environment can shape the behaviors associated with poor health [5].

An example is Alaska Natives who were essentially free of Diabetes (DM) and Cardiovascular Disease, including stroke (CVD) many years ago [6]. The acculturation since that time involves the increasing consumption of specific store bought foods, often bought without guidance about effects on health. Studies have revealed that some of these foods contain large amounts of saturated and trans fats that are associated with Type 2 Diabetes and Cardiovascular Disease [5-7]. Alaska Natives who consume a diet based on fish and marine mammals are exposed to contaminants such as mercury, thus reducing the safety of their food supply [8]. Environmental change induced alterations in subsistence food consumption may also alter cultural identity. Culture and the environment are closely linked through food and subsistence in terms of how they reflect and represent cultural identity. Contaminants released by climate change affect food security in more than a physical sense. Because climate change, both physical exposure to contaminants and associated mental stress, can lead to an increase behavioral issues in Alaska Natives and other rural populations [4,5].

There is abundant evidence, acquired both via Western science and traditional knowledge, that indigenous peoples and ecosystems throughout the North are experiencing significant health impacts from the accumulation of metals, persistent organic pollutants, and rapid notable ecological, social and cultural impacts from changing climate and industrial development. The issue of climate impacts in the Arctic and sub-arctic raises the question of unequal distribution of burdens and benefits within more developed countries. Developing areas, like the North, stand in the center of two major forms of environmental injustice: 1) exposure to contaminants such as Hg [9,10] and 2) impacts of a changing climate [3,11-14] . These issues share a common feature with each other and with many past instances of environmental injustice, e.g. while negative impacts are experienced locally, the industrial source is distant [15].

This special closeness to the land, which is often lost in urban communities has led to a “One Health” approach to develop an interdisciplinary collaboration that focuses on the interactions between the physical environment, plants and animals and the human social system to understand the disease processes [16,17]. The health and survival of rural populations has traditionally depended on an extensive knowledge of the plant and animal species in their local environment. Seasonal harvest patterns have traditionally been a major community activity and are closely linked to a holistic culture and worldview. The local terrestrial, coastal and marine resources supply natural nutrients and phytochemicals for preventing disease and mitigating metabolic syndromes like diabetes. Understanding the concept of complex processes at both the local and global level is necessary to understanding the many factors in the toxicological process for people living in rural, marginal or polluted environments. One Health emphasizes the unity of an ecosystem [17]. Looking at a map or globe, it is easy to observe that populations living in proximity to marine and river ecosystems are at risk from sea level rise [18] and wet disposition [19,20] with Hg levels ranging from 10.2 to 22.3 ng/g.

River watersheds are among the most complex terrestrial features, performing valuable ecosystem functions and providing services for human society. Rivers are vital to both estuarine and aquatic biota and play important roles in biogeochemical cycles and physical processes. The functions of watersheds have been traditionally used as indicators for ecosystem health. River watersheds have a long history of human activity, but they have not been given the holistic and interdisciplinary research attention of the other ecosystems. Coupling ecosystem assessment with education creates resilience within the community. By monitoring key watershed indicators, for example, using wildlife, we can gain insights into regime shifting stresses such as increasing contaminants like Hg and industrial development [21-24]. Observations of impacts from a changing climate or mineral development can be assessed and inform adaptations to private, state, territorial, tribal and national ecosystem management approaches [25,26].

Heat stress, water cycle and quality and food security are other issues impacting human health [4]. Chemical exposure interferes with metabolic functions and homeostasis by interfering with enzymes or receptors [27]. Increased industrial development at low latitudes and global transport of air pollutants will lead to an increase in contaminant deposition. Legacy chemicals from early development efforts such as gold and silver mining and processing have been reported in the rural regions and their populations [25]. Industrial accidents related to development have led to immediate loss of wildlife and fish where populations remained depressed for over a decade [26,27]. Human psychological impacts were often reported.

Methylmercury (MeHg) is an organic form of mercury that creates a lipophilic environmental contaminant that migrates up the food chain [26]. Bioaccumulation MeHg has been increasing in Northern latitudes due to global processes and climate change [26,28]. Studies have shown that MeHg causes cytotoxicity [9,27,29] in various cells and induced both apoptosis and the formation of reactive oxygen species (ROS) such as the superoxide anion and hydroxyl radicals [29,30]. Pancreatic islet cells are damaged by MeHg and high blood glucose levels can be induced by repeated doses. Toxic effects of methylmercury were also seen in 3T3-L1 adipocytes at exposures as low as 100ng/ml during stages of differentiation. Results also showed that VEGF secretion was elevated in adipocytes exposed to MeHg after differentiating into mature, fat-storing cells [31].

Sentinel species, i.e. bioindicators, are usually animals that are higher trophic level predators and are keystone species in an ecosystem, which can be used to monitor risks to the ecosystem or humans [32,23]. Plants, fish [33,34] and lichens [15] with Hg in the range 20 ppb or greater have also been used as indicator species. As Burger reported, Pacific cod currently range around 0.25- .5 ppm Hg, while in the past its bone Hg ranged around 300 ppb to 500 ppb [33]. Sentinel species are useful in following the biomagnification process of mercury in both terrestrial and marine ecosystems [10,26,28,34-36].

Knowledge of the past can inform us on how bioindicator species might respond. An increase in mobility of mercury has the potential to be one of the impacts of climate change. Sea level changes and flooding events in high latitude coastal ecosystems could increase the bioavailability of contaminants such as mercury. Mercury concentrations have been used as an indicator of past exposure to heavy metals in ancient fish and animal samples [33]. Sea otters (Enhydra lutris) are common to the Gulf of Alaska’s coastal areas and paleontological deposits of their bones have been identified as far back as the early Holocene [37]. In sea otters [37], current bone Hg levels are in the low (10 to 50 ppb) down from 200 to 400 ppm several thousands of years ago. Stable isotope ratios are used to reconstruct ancient food webs and help identify sea otter prey, which may have bioaccumulated high concentrations of the metal. Modern sea otters have δ¹³ C, δ¹⁵N, and mercury values likely corresponding largely to a benthic diet. Conversely, higher δ¹⁵N and mercury levels were found in ancient sea otter bones which may not only demonstrate higher trophic level foraging but also a large increase in the bioavailability of mercury in the coastal ecosystem. These large increases may be associated with rising sea level following the glacial maximum [38]. Paleontological remains of sea otters have been used to associate present day predicted climactic perturbations with past events like flooding of Beringia during the Holocene [33,37].

Red foxes can be used as a bioindicator species to monitor variation in mercury concentrations both within a species and between different species living in the local geophysical region or ecosystem [23,39]. Foxes can provide information on Hg biomagnification patterns and changes in exposure. Since foxes are omnivores like dogs [10], examining concentrations of Hg also provides feeding ecology data on the contaminant concentrations in other small mammals, birds and fish which they eat [34]. Fox bones and hair can also be used in forensic investigations [40]. Dogs along the Yukon River, Alaska, have Hg levels which varied from 2000ppb to 16000 ppb [32]. Foxes on the Kuskokwim River ranged around 1200 ppb [23,40].

Watersheds are closely linked ecosystems that are natural units of analysis and management [11], within which Hg can be mobilized and dispersed across the landscape, eventually entering the ocean. Rivers are a major component of socio-ecological systems which, in turn, have the potential to change because of chronic disturbances, i.e. the adaptive cycle [11]. Seven percent of the human population lives below the estimated future sea level, so coastal populations will be impacted by Hg when sea levels rise [18]. Some of the damage from sea level rise can be mitigated if there is a coordinated investment in developing a framework to monitor and understand the local cultural and environmental risks [41,42]. Importantly, Hg needs to be monitored in many locations throughout the world due to its impact on human health [8].

The structural organization of food webs and their sensitivity to disturbances are relevant to our ability to predict the fate of Hg bioavailability related to sea level rise on ecosystems. Climate change and movement of Hg by flooding can impact food systems. Hg needs to be monitored across many ecosystems due to its impact not only on human health, but also the health of the plants and animals that provide ecosystem services. Monitoring studies are needed to confirm preliminary observations related to the anthropological induced climate change leading to increased precipitation and sea level rise that will result increased mercury mobility into the coastal food web.

We appreciate the stimulating discussions and assistance from the following colleagues: Phil Loring, Peter McCroy, Maribeth Murray, S. Craig Gerlach, Arleigh Reynolds, Joanna Burger and Mary van Muelken. This research was supported in part by NSF DUE 0632397 and Alzheimer’s Resource of Alaska.