1. Introduction
Metals refer to persistent toxic substances (PTS), as they are stable and persistent in the environment, and do not undergo physical, chemical, and bacteriological degradation. The characteristics of some metals include global transportation (also to the Arctic) with atmospheric fluxes, river, sea, and oceanic currents; bioaccumulation and biomagnification in terrestrial and marine food chains; slow elimination from organisms, including humans; and variable toxicity, which can include adverse human health effects. Some metals cross the placental barrier, where they can affect the fetus during its development, and can be excreted in mother’s milk [
1]. Some metals are referred by the International Agency for Research on Cancer (IARC) to the agents that are carcinogenic to humans; inorganic arsenic, beryllium and cadmium belong to Group 1 (“sufficient evidence of carcinogenicity”), while inorganic lead, nickel, and cobalt belong to Group 2B (“limited evidence of carcinogenicity”) [
2].
Although metals occur naturally in all of the ecosystems and have accumulated and cycled in the environment over geological time periods, significant quantities of metals are now introduced and redistributed in the environment by human activities such as fossil fuel combustion, different industrial processes (e.g., the mining of minerals, metallurgy), agricultural practices, transportation, and waste disposal at local, regional, and global scales. Anthropogenic activities now add metals to surficial environmental compartments at significantly greater rates than natural processes, with the possible exception of volcanic sources [
1]. At the global scale, stationary fossil fuel combustion continues to be a major source of heavy metal emissions. Coal combustion contributes chromium (Cr; 69%), mercury (Hg; 66%), manganese (Mn; 85%), antimony (Sb; 47%), selenium (Se; 89%), tin (Sn; 89%), and thallium (Tl; almost 100%) to atmospheric emissions. The combustion of leaded, low-leaded, and ‘unleaded’ gasoline continues to be the major source of atmospheric lead (Pb) emissions [
3].
Metals are redistributed within the Arctic via atmospheric, marine, freshwater, snow ice permafrost, sediment, and biotic transport mechanisms. The redistribution of metals leads to their presence at concentrations above the naturally occurring levels in locations that are remote from anthropogenic sources, and in forms that are available for biotic uptake. Metals pose a potential risk to the ecosystems and biocenoses of the Arctic [
3]. The diet of Indigenous peoples of the Arctic is based mainly on locally harvested foods; therefore, the dietary exposure of the Arctic population to metals remains a health risk problem.
Metals can accumulate in different organs and tissues of different animals, plants, and fungi. Most metals accumulate in the muscle and parenchymal tissues of fish, birds, and mammals, especially intensively in the liver and kidneys. In the fat of marine mammals, the content of some metals can exceed that of the muscles. The liver of bottom fish species (e.g., freshwater burbot) can accumulate significant levels of certain metals, especially when the water and bottom sediments of the reservoir are highly contaminated by these metals. Seaweed, benthic mollusks (mussels, e.g., bivalves and gastropods), and especially ascidians are able to accumulate extremely high concentrations of metals. The liver and kidneys of reindeer, which feed on lichen “saturated” with metals, also accumulate high levels of metals [
1]. Under conditions of pronounced soil contamination, metals can reach high concentrations in both laminar and tubular mushrooms. Mushrooms are powerful “sorbents” of metals from the Arctic soil, including in the territories where there is permafrost, and can be used as indicators of industrial pollution. Wild berries (cranberries, bilberries, cloudberries, etc) and wild plants (wild onions, garlic, leaves and roots of herbaceous and shrub plants), which are often consumed by Indigenous Arctic people, have the ability (in comparison with fungi) to accumulate metals from the soil. Vegetables and garden berries, which are grown in private gardens, sometimes show significant levels of some metals, especially if the gardens are located near the sources of emissions from industrial enterprises [
4].
Studies on local food contamination by metals (and dietary human exposure to metals) that have been carried out over the last decades in the countries of circumpolar North have always focused on Hg and occasionally Cd (cadmium) and Pb. The summarized results of these multi-national studies are presented in the Reports of the Arctic Monitoring and Assessment Program (AMAP) [
1,
5,
6,
7] and in the Canadian Arctic Contaminants Assessment Reports of the Northern Contaminants Program [
8,
9].
The only metal that has been comprehensively investigated in different biota species at the circumpolar scale is Hg. A meta-analysis was applied in 83 time-series datasets of Hg in Arctic biota with the purpose of determining whether temporal trends exist in the data collected over the past decades (1975–2008). It was shown that nine significantly increasing time series were found for Canada (30% of the Canadian datasets), two significantly increasing time series were found for Greenland (13%), and one significantly increasing time series was found each for the Faroe Islands (14%) and Iceland (7%). Increasing Hg trends were found in marine invertebrates (one; 8% of the significantly increasing datasets), seabirds (two; 15%), marine mammals (five; 38%) and freshwater fish (five; 38%). Only four (5%) of the time series showed a significantly decreasing Hg trend, and one of these also had a significant non-linear trend component. Two of these were for Atlantic cod from the Faroe Islands and Iceland, one was for Arctic char from Canada, and one was for reindeer from Sweden. None of the Arctic marine mammal or seabird datasets showed a significantly declining trend. The remaining 66 Hg time series showed either no trend or a significant non-linear trend component [
7].
The collection and chemical analysis of local foods for Hg, Cd, and Pb were conducted in coastal Chukotka in 2001–2002 along with other Russian Arctic regions within the framework of the Russian Arctic PTS study [
10,
11]. The community-based dietary and lifestyle survey (interviews of 251 indigenous people in Uelen settlement) based on self-reported daily (weekly, monthly) food frequencies were carried out during the same period.
The objective of the present part of the project is to carry out an assessment of 18 environmental metals in subsistence species (including fish, terrestrial, and marine mammals, mushrooms, berries, wild plants, and seafood), compare the results of the three metals with those obtained in coastal Chukotka 15 years ago and during the recent follow-up and with other Arctic regions, and estimate the daily intakes (EDIs) of different metals with different food items by the local Indigenous people. The assessment of numerous metals in seafood (seaweed, mussels, and ascidians) has been carried out for the first time in Chukotka coastal waters. Taking into account that residents of the Russian Arctic, including costal Chukotka Indigenous people, eat seafood (including ascidians), the analysis of metals in this group of local foods is of particular interest.
Another important task is the evaluation of metal content (using the same list of metals as for the food analyses) in the drinking water of each of the studied settlements, as the daily intake of metals is formed both by food and by drinking water. Drinking water in the Arctic sometimes is highly contaminated by metals when the settlement is near the ore mining and processing enterprises, e.g., by aluminum in Kirovsk city or by nickel in the Zapolyarny and Nikel cities of the Murmansk oblast [
12].
2. Materials and Methods
2.1. Field Sampling
Collection of samples of local foods and drinking water were carried out in all three study settlements (Enmelen, Nunligran, and Sireniki). Samples of fish (marine, migratory, freshwater), the meat of terrestrial mammals (reindeer, hare), the meat and blubber of marine mammals (whale, walrus, seals), mushrooms, berries, wild plants, seaweeds, ascidians, and mussels have been collected. Most of the samples have been kindly provided by the local people; several samples were collected by the Northwest Public Health Research Center (NWPHRC) specialists during fieldwork (fish by ice fishing, hare by hunting near Enmelen). Birds (except for one goose sample) and the viscera of marine and terrestrial mammals (e.g., liver and kidneys) were not available in the expedition season, and were absent in the storages of local people.
Samples from multiple specimens of each biological species that were similar in age and size were pooled. Pooled samples accounted for 37% of the total sample number. When pooling the fish species, five to seven specimens were selected, the sizes of which were typical and average for these species; a piece of muscle tissue was cut from the central part of the specimen back (up to the backbone, without affecting it), and packed together with several other pieces that were selected from different specimens of the same species, into one package. Hare meat was taken from the muscles of the lower limbs, while poultry meat was taken from the pectoral muscle, and marine mammal meat (whale, walrus, seal, etc.) was taken from the latissimus dorsi muscle. For the pooling of mushroom samples, seven to 10 caps were used. Wild berries and wild plants were pooled by weight: about 100–150 g. Marine weed and mollusk samples were pooled using five to seven specimens of similar size. After pre-treatment, packing, marking, and freezing, all of the samples were delivered to St. Petersburg in thermocontainers, which helped prevent thawing during transportation. All of the drinking water samples have been collected in each settlement, as well as in Provideniya and Anadyr (for the purpose of conducting the comparison); each 500-mL water sample was put into a plastic container with a screw top.
The total number of samples that was collected and analyzed for metals is 79 (
Table 1); among them were 16 samples of fish, 28 samples of marine mammals, six samples of land mammals, one bird sample, four mushrooms samples, seven berries samples, five wild plants samples, six seafood samples, and six drinking water samples.
2.2. Metals Analyzed in Collected Samples
Eighteen metals (Pb, As (arsenic), Cd, Hg, Cu (copper), Zn (zinc), Ni (nickel), Cr, Al (aluminum), Mn, Ba (barium), Sr (strontium), Co (cobalt), V (vanadium), Be (berillium), Mo (molybdenum), Sn, and Sb have been analyzed in all of the samples of local foods (fauna and flora) and in drinking water.
2.3. Chemical Methods and Laboratory Equipment Used for Metals Analysis
Chemical analyses of metals in all of the samples were performed by the Northwest branch of Research and Production Association "Typhoon" (RPA “Typhoon”), St. Petersburg, Russia, which has international accreditation in the Arctic Monitoring and Assessment Program (AMAP) system. Inductively coupled plasma mass spectrometry (ICP-MS) was applied for the determination of metals, and atomic absorption spectrometry of “cold vapor” (AAS-CV) was applied for the determination of mercury. All of the samples were analyzed on a wet weight (w.w.) basis.
Before analysis, solid food samples were thawed, dried, homogenized, and digested. An aliquot of a homogenized sample of approximately 1.5 g was weighed. Digestion was carried out by extra pure nitric acid, which was pre-distilled in a DistillAcid apparatus (Berghof, Eningen, Germany), in Teflon tubes in a MARS-5 microwave digester (“CEM” Corp., Matthews, NC, USA). Samples were exposed at 80 °C for 20 min, and then heated to 120 °C for 75 min with pressure control. The mineralized sample was diluted with high-purity water to a volume of 25 mL. Then, 100 mL of drinking water samples were treated by adding five mL of extra pure nitric acid. Analysis of metals in food and water samples was carried out by ICP-MS on a NexION-300D device (“PerkinElmer”, Chicago, IL, USA). Instrument calibration was performed on multicomponent standard solutions ICP-MESS-4 and ICP-MESS-16 (“Certipur”, Merck Chemicals GmbH, Darmstadt, Germany). An additive of yttrium (89Y), which was obtained by dissolving the metal oxide in extra pure nitric acid, was used as the internal standard. Analysis of metals was carried out in the kinetic energy discrimination, Dynamic Reaction Cell™, and normal modes.
An analysis of mercury was carried out without digestion directly by AAS-CV (cold vapor method) on an RA-915M device with a Universal Mercury Prefix console (“Lumeks”, S.Petersburg, Russia). Limit of detection (LOD values) for the analyzed metals in food and drinking water samples were at least 10 times lower than the corresponding established allowable levels. For quality assurance/control purposes, samples for international intercalibrations under the Canadian Northern Contaminants Program quality assurance/control were used. For the certified reference materials, all of the values were within ±20% of the reference values.
International QA/QC intercalibration standards for metals were used under the aegis of the Canadian Northern Contaminants Program. The obtained results were within ±20% of the reference values.
2.4. Processing, Analysis, and Interpretation of the Data
The analyzed concentrations of metals in local foods were evaluated in terms of comparisons between different species in coastal Chukotka and (as much as possible) in the corresponding species in other circumpolar regions, including the assessment of temporal trends of metals. The exceedances over the established limits were determined using Russian food safety regulation standards for metals in raw foods. Estimated daily intakes (EDIs) of metals by local food consumption were calculated based on the average concentrations of metals in local foods and on the intake frequencies of each food item, as reported by the respondents in the questionnaire. Using the hypothetically assumed one portion size as 150 g/meal of each foodstuff, the average annual EDIs of pollutants were calculated for each food group.
Statistical treatment of the data was carried out using the Microsoft Office 2016 software package.
5. Conclusions
To our knowledge, this is the only study examining multiple metals in the variety of local subsistence foods from the coastal Chukotka since the beginning of the 2000s. For some species of local fauna and flora, the content of metals was demonstrated for the first time.
Levels of metals were very different in various foods. Lead and Hg were low in all of the foods; As levels were up to four mg/kg ww in fish and the blubber of marine mammals. Wild plants (particularly Rhodiola arctica) accumulated Mn (up to 190 mg/kg ww), Al (up to 75 mg/kg ww), Ni, Ba, and Sr. Seafood species were highly contaminated by several metals (As, Cd, Cr, Al, Ba, and Sr); seaweed (Laminaria saccharina) contained very high levels of As (14 mg/kg) and Sr (310 mg/kg); ascidians (particularly Halocynthia aurantium) were contaminated by Cr, Sr, and Al (up to 560 mg/kg); blue mussels accumulated significant levels of Cd (2.9 mg/kg) and Al (140 mg/kg).
The comparison of metals concentrations in different foods with regard to the food safety limits has revealed the following exceedances over the Russian allowable levels: As in marine mammals blubber, land mammals meat, and seaweed; Cd in hare meat, berries, wild plants, and mussels; and Al in whale meat, wild plants, and bearded seal meat. The absence of the established limits for Al and Sr in seafood, and Mn in wild plants and berries, impedes the determination of the excess levels. Concentrations of all of the studied metals in drinking water samples from all of the studied settlements were much lower than the established hygienic limits.
The calculated structure of the estimated daily intakes (EDIs) of metals is formed by multiple food items: Pb, mainly by meat of land mammals and fowl; As by seafood and fish; Hg by fish and sea mammal meat; Cd, Al, Sr, and Ba by seafood; and Ni and Mn by wild plants.
Follow-up analysis of Hg, Pb, and Cd in local foods (conducted 15 years after the first study) has not revealed any increase trend; the slight decrease tendency was noted in arctic char (Hg, Cd and Pb), flounder (Pb and Cd), ringed and spotted seals (Hg), and bearded seal (Hg and Pb).
Geographic comparisons based on the available literature (which is scarce for the Bering Strait region) for Hg, As, Cd, and Pb in the main food items, which are monitored at the circumpolar scale, has not revealed new insight.