Elemental Composition and Freezing Tolerance in High Arctic Fishes and Invertebrates
1
National Centre for Polar and Ocean Research, Mormugao 403804, India
2
Department of Botany, Banaras Hindu University, Varanasi 221005, India
3
Science and Engineering Research Board, Department of Science and Technology, New Delhi 110016, India
4
Department of Materials Chemistry, Asahikawa College, National Institute of Technology, Asahikawa 071-8142, Japan
5
Department of Pharmaceutical Engineering and Technology, Indian Institute of Technology (IIT) BHU, Varanasi 221005, India
6
National Research Centre for Grapes, Pune 412307, India
*
Author to whom correspondence should be addressed.
Sustainability 2022, 14(18), 11727; https://doi.org/10.3390/su141811727
Submission received: 19 May 2022
/
Revised: 19 July 2022
/
Accepted: 3 August 2022
/
Published: 19 September 2022
(This article belongs to the Special Issue Microbial Diversity in Cold Environments and Their Sustainable Use)
Abstract
:The elemental composition in different Arctic fishes and invertebrates was investigated using Inductively Coupled Plasma Mass Spectrophotometer (ICPMS). Nineteen elements such as Arsenic (As), Barium (Ba), Bismuth (Bi), Cadmium (Cd), Cesium (Cs), Chromium (Cr), Cobalt (Co), Copper (Cu), Iron (Fe), Lead (Pb), Manganese (Mn), Nickel (Ni), Rubidium (Rb), Selinium (Se), Silver (Ag), Strontium (Sr), Uranium (U), Vanadium (V), and Zinc (Zn) were analyzed in six species of fishes (Anarhichas lupus, Gadus ogac, Gadus morhu, Gymnocanthus tricuspis, Liparis sp., Myoxocephalus scorpius) and four benthic invertebrates (Ophiura albida, O. Sarsii, Strongylocentrotus droebachiensis, Polychaete). Elemental data revealed that the invertebrates accumulate higher concentrations of elements than the fishes. The high concentration of elements including Sr, As, and Zn indicated anthropogenic contribution and may affect the fish community in the fragile ecosystem of the High Arctic. The movement of tourists and logistics must be regulated to prevent serious change in Svalbard. Most of the fishes have shown strong antifreeze protein (AFP) activity, and this potential helps fishes to survive in the cold Arctic environment. This is the first study of elemental concentrations and AFPs in fishes and benthic invertebrates filling the knowledge gap from the High Arctic.
1. Introduction
Elements are present at various levels in the geo-spheres (lithosphere, hydrosphere, atmosphere, and biosphere) and are generally classified as lithophiles, chalcophiles, and siderophiles [1]. Among these, some elements are essential components of hormones, enzymes, and enzyme activators [2] and play important roles in physiological and metabolic processes of different life forms [3]. The deficiency and excess intake of elements in different life forms can be detrimental to the health of an ecosystem. Due to the impact of climate change, tourism, and industrialization, the natural habitats have been affected immensely in many parts of the earth’s surface [4]. The contamination of the hydrosphere is one of the most serious concerns that affect the ecological balance in aquatic habitats [5]. Fish act as top predators in the food chain of the aquatic ecosystem and also accumulate higher concentrations of trace elements, causing them to be dangerous to eat [6,7,8,9]. Fish organs (muscles, livers, and gills) are known for their bioaccumulation process [10]. Recently, analyses of essential (copper (Cu), cobalt (Co), selenium (Se), and zinc (Zn)) and nonessential elements (mercury (Hg), lead (Pb), cadmium (Cd), and arsenic (As)) in seven fish species consumed by the indigenous people of the European Russian Arctic were conducted [11].
The Arctic is one of the most pristine regions on earth. The natural processes such as erosion, transportation, and deposition has increased with time since the last glaciation [12]. In order to recognize the effect of such natural processes and/or anthropogenic disturbances, if any, the elemental concentration in different life forms of Kongsfzorden needs to be determined at regular intervals. An unprecedented increase in these elemental values needs to be monitored against the various factors affecting the Kongsfzorden. Environmental monitoring of major, minor, as well as trace elements in the Arctic has been done for aerosols [13,14,15,16], lake sediments [17,18], snow, and cryoconite [1,19]. Biomonitoring of lichens and seabirds has also been conducted [20,21,22] reviewed air pollution in the Arctic through long-range pollutants, while [23] analyzed the element stratigraphy in quaternary sediments of the Arctic Ocean. Hicks and Isaksson [24] assessed the source areas of pollutants in Svalbard snow and ice. Recently, studies on the elemental chemistry of Kongsfjord sediments [25,26], ice cores [27], permafrost [28], lichens [29], and radionuclides [30] have been carried out.
Recently, baseline studies on shallow water fish community determined the abundance and species composition in Kongsfjorden, Svalbard. Among these Myoxocephalus scorpius (shorthorn sculpin) (74.9%), Gadus morhua (Atlantic cod) (17.2%), and Gymnocanthus tricuspis (Arctic staghornsculpin) (3.8%) were identified as the most abundant species across all sampling sites [31]. The diversity and abundance of hard-bottom fauna was recorded at a depth range of 5–10 m [32]. The macro-algal-rich seafloors provide a potential food source and an important habitat for fishes [33]. The resident fish community acts as a secondary producer in the local food web. It prefers shallow water habitats as spawning and nursery grounds [34,35].
Antifreeze proteins (AFPs) are a structurally diverse group of ice-binding proteins that inhibit the growth of ice either by depressing the freezing point (TH activity) or by inhibiting the recrystallization of ice grains [36,37,38]. By this mechanism of control of ice growth, the membranes of the organisms remain protected from damage caused due to freezing, thereby increasing the survival in cold environments. DeVries et al. [39] were the first to isolate AFPs from Antarctic teleost fishes. Since then, a number of AFPs have been discovered in fishes [40,41].
The gap in knowledge of different elements and AFPs in High Arctic fishes and other organisms is an area requiring investigation; therefore, the present study was undertaken on the fishes and benthic invertebrates of the Kongsfzorden, Arctic.
2. Materials and Methods
2.1. Study Area and Sampling
Samples were collected from different locations of Kongsfzorden, Svalbard, Arctic (Figure 1). There are many melting glaciers around, but two are the main sources of water to the Bayelva river finally discharged in Kongsfzorden. In the present study, six different fish species (Anarhichas lupus, Gadus ogac, Gadus morhu, Gymnocanthus tricuspis, Liparis spp., Myoxocephalus scorpius,) were collected using one fyke net (diameter 40 cm, length 90 cm, mesh size 12 mm (bar mesh), deployed in about 3 m water depth with its mouth set perpendicular to the shoreline and one trammel net (inner/outer mesh size 1/15 cm, length 20 m, height 2 m) deployed from about 5 to 12 m water depth [31].
The most common species of Kongsfizorden are shown in Figure 2a–d. Invertebrate’s organisms (Ophiura arctica, Ophioceten sericeum, Strongylocentrotus droebachiensis and Polychaetes) were collected using a grab sampler (Figure 2e–h).
The ten collected samples were kept in polystyrene boxes and transported to Kings Bay Marine laboratory at Ny Ålesund to sustain freshness. The fishes were identified on the basis of morphological characteristics [42,43,44,45]. The fishes belonging to family Liparidae showed morphological plasticity and were therefore indented up to genus level. The upper water temperature during the summer was ~5.7 °C to 6.7 °C, while it was ~0 °C during the month of February [31]. Fish samples were measured for length and weight (Table 1).
To avoid metal contamination of the samples, the laboratory wares were soaked in 2 M HNO3 for hours and rinsed with distilled water and deionized water prior to use. The head and gut of the fish samples were removed. The muscles were detached on plastic sheets with a steel knife, packed into plastic bags, and frozen in a −86 °C freezer. Samples were transported to a laboratory via air cargo in insulated boxes with dry ice. Further, muscles tissue was taken for analysis of trace metals and blood samples for AFPs.
2.2. Analytical Procedure
The freeze-dried, powdered, and weighed (0.25 g) samples (fish, Brittle star, Sea Urchin, and Worm sample) were kept in PTFE TFM vessels for microwave digestion following the standard method [1,26,27]. With the completion of the digestion program, the vessels were cooled, and the digested solution transferred into a 25 mL volumetric flask with deionized water. Blank samples were also prepared using the same procedure of samples, and the values obtained were subtracted from the samples. The individual samples were subjected to analysis of elements following the standard method using ICPM [1,26,27]. Elemental concentrations were measured in triplicates and were recorded in mg/kg.
Blood samples from 11 fishes belonging to 6 species (Anashichas lupus F (1738), Gadus morhva A2 (1644), Gadus morhva A1 (1707), Gadus oguc E (1643), Gymnocanthus tricuspis B1 (1763), Gymnocanthus tricuspis B2 (1737), Liparis spp. C2 (1703), Liparis spp. C1 (1770), Myoxocephalus scorpius D1 (1700), Myoxocephalus scorpius D2 (1702), Myoxocephalus scorpius D3 (1704)) were collected through sterile syringe and kept in sterile blood sampling tubes and preserved in a −80 °C deep freezer. A Leica DMLB 100 photomicroscope (Leica Microsystems AG, Wetzlar, Germany) equipped with a Linkam LK600 temperature controller (Linkam, Surrey, UK) was used to examine the antifreeze activity. A total of 5 µL of supernatant of blood sample was taken and observed under a 50× magnifying lens. The blood supernatant was briefly frozen (at about −25 °C) and warmed to 0 °C on the sample stage of the photomicroscope to create several ice crystal seeds in solution. This solution was then cooled to approximately −1 to −5 °C, and the growth of ice crystal seeds was monitored. According to the shape of the ice crystals, the positive and negative activity of the strains were noted. Hexagonal crystals indicated positive activity, while rounded type indicated negative activity.
3. Results and Discussion
The length and weight of Kongsfzorden fishes showed variation (Table 1). Among the fishes studied, Liparis sp. had the least length and weight (12.5–14.5 cm and 36.6 g–71.58 kg, respectively) followed by Myoxocephalus scorpius (11.5–17 cm and 28.76 g–108.9 kg), Gymnocanthus tricuspis (14.5 cm and 65.63 g), Gadus morhua (16.5–37.5 cm and 49.23, 634.7 g), Gadus ozac (30.0 cm and 352.88 g), and Anarhichas lupus (49.0 cm and 1321.07 g) with a higher length and weight. The length of the fishes gradually increased depending on the weight of the fish. Similar findings were also observed in the fish assemblage of a tidal creek in the Niger Delta, Nigeria [46].
The fish element concentration ranged from 0.134 to 0.757 mg/kg for Chromium in Liparis sp. and Myoxocephalus scorpius; 0.165 to 1.311 mg/kg for Manganese in Anarhichas lupus and Myoxocephalus scorpius; 0.000 to 0.051 mg/kg for Cobalt in Gadus ogac and Liparis spp.; 0.255 to 1.74 mg/kg for Copper in Gadus morhu and Gymnocanthus tricuspis; 8.569 to 37.358 mg/kg for Zinc in Gadus morhu and Myoxocephalus scorpius; 2.781 to 35.84 mg/kg for Arsenic in Myoxocephalus scorpius and Gymnocanthus tricuspis; 0.000 to 0.161 mg/kg for Mercury in Liparis sp. and Gymnocanthus tricuspis; and 0.000 to 0.117 mg/kg for Lead and 0.501 to 1.206 mg/kg for Selenium in Gymnocanthus tricuspis and Gadus morhu, respectively. However, these elements in invertebrates ranged from 0.392 to 0.916 mg/kg for Chromium in Ophiura albida (Brittle star) and O. sarsii (Brittle star); 14.13 to 64.834 mg/kg for Manganese in Polychaete (Worm) and O. sarsii (Brittle star); 0.541 to 1.336 mg/kg for Cobalt in O. albida and Polychaete; 0.775 to 10.045 mg/kg for Copper in O. albida and O. Sarsii; 20.178 to 77.622 mg/kg for Zinc in O. albida and Polychaete; 1.221 to 13.458 mg/kg for Arsenic in O. albida and Polychaete; 0.000 to 0.018 mg/kg for Mercury in Strongylocentrotus droebachiensis (Sea Urchin); 0.261 to 5.258 mg/kg for Lead in O. albida and O. sarsii; and 0.395 to 3.978 mg/kg for Selenium in O. albida and Polychaete (Worm), respectively.
Elemental analyses of fish muscles and invertebrates showed the presence of three groups of elements such as lithophiles, chalcophiles, and siderophiles. The lithophiles include Barium (Ba), Chromium (Cr), Cesium (Cs), Rubidium (Rb), Strontium (Sr), Uranium (U), and Vanadium (V); chalcophiles include Arsenic (As), Bismuth (Bi), Cadmium (Cd), Copper (Cu), Lead (Pb), and Zinc (Zn); while siderophiles include Cobalt (Co), Iron (Fe), Manganese (Mn), and Nickel (Ni). The concentration of lithophiles, chalcophiles, siderophiles, and a few others in fish muscles and invertebrates are presented in Table 2, Table 3, Table 4 and Table 5.
The lithophiles were found in lower concentrations in different fishes than the benthic organisms studied in the present study (Table 2). The concentration of Sr was significantly higher than the values recorded in most of the fishes and invertebrates. Uranium values were below the quantification in all the fishes, while the lowest concentration was detected in invertebrates. The values of lithophiles were much lower than the values reported from the sediments of Kongsfzorden [25,26,27], lichens, and glacier cryoconites [1,29] of Svalbard.
The chalcophile elements were in a higher concentration in the fishes than the lithophiles (Table 3). In the fishes, elements such as As and Zn were present in concentrations higher than the values of Cu and Pb. The concentrations of Bi and Cd values were below the quantification in all the fishes, while in a few invertebrates the lowest concentration was detected. The high concentrations of As in fishes E(1643) and B1(1763), and Zn in B1(1763) and D2(1702) were recorded. The concentration of Zn was comparatively much higher in invertebrates (Brittle star: Ophioceten sericeum and Worm: Polychaetes) than the fishes. The high concentrations of As in fishes E(1643) and B1(1763) is evidence that proves that there is a process of bioaccumulation in fishes which may lead to Arsenic poisoning in the fish population, which is sourced from the Svalbard terrestrial habitats. High concentrations of As have also been reported in sediments from Kongsfzorden [26] and glacier cryoconites [1]. These observations provide a clue that the Svalbard probably holds enriched sources of elements such as As and Zn. A bio-monitoring study by Borgå et al. [20] found elevated levels of Zn and Cu in Arctic seabirds as a consequence of bioaccumulation. In the fish muscles, elements such as Cd and Pb were present in lower concentrations, while for Zn, the concentrations exceeded the values reported from the Red Sea [47,48,49]. In the case of Cu, the concentrations were higher in the present study than the two estimates at the Red Sea [47,49]. Since no previous information is available on the concentration of these elements from Arctic fjords, no comparison could be made.
The siderophiles (Co, Fe, Mn, and Ni) were lower in the Arctic fishes than the invertebrates (Table 4). However, the Fe and Mn values of Arctic fishes were very similar to estimates at the Red Sea and lay in between the reported values [49]. In the case of Ni and Cu, concentrations were lower in the present study than the estimates for the fish muscles at Chascomus lake [50]. Siderophiles from sediments from Kongsfzorden [26] and glacier cryoconite [1] habitats of Svalbard close by corroborate with the present results. A comparison of siderophilic elements from the present study with other habitats of Svalbard showed comparatively lower concentrations of siderophiles [1,26]. Elements such as Ag and Se were also analyzed from Kongsfzorden fishes and invertebrates of the Arctic region (Table 5). The concentration of Ag and Se was higher in invertebrates than fishes.
Determining the exact source of the elements is often difficult as it may arise from multiple sources [51]. We can, however, segregate the sources into two groups: local deposition and long-distance (transboundary) transmission [52]. Pollutants from various sources (natural or anthropogenic) are released into the atmosphere and through wind movement travel long distances [51]. Moreover, the erosive action of glacial ice also deposits sediments with different elements into Kongsfzorden, which is another important contributor. High concentrations of anthropogenic (137Cs, 90Sr) and natural (210Pb) radionuclides and heavy metal (Pb, Cd, Cu, Zn, Fe, and Mn) deposition were reported from glacial cryoconite of Spitsbergen [30]. The glacial cryoconite elements with melt water finally enter into the Kongsfzorden and accumulate in aquatic organisms including fishes and invertebrates.
In the fishes and invertebrates studied, the concentration of most of the elements in the invertebrates were much higher than the fishes present in Kongsfzorden, probably because the invertebrates are benthic and stay on the seafloor where all the sediments are accumulated, brought down by wind and the surrounding glaciers. The high velocity winds, after hitting the mountainous terrain, subside into the valley depositing the dust it carries. The difference in depths of collection sites may also affect the deposition patterns of elements. In the Arctic fishes and invertebrates, the values of elements such as Cd, Cr, Cu, Pb and Zn were different than the values reported in lichens and cryoconites [29], Kongsfjorden sediments [25,26], and ice cores [27] (Table 3).
The observed elemental concentrations in the present study were below the EU maximum concentrations of 0.050 mg/kg for Cd and 0.3 mg/kg for Pb for fish species [53]. The amount of As (2.78–35.84 mg/kg) in the present study exceeds the Russian regulation limit of 5.0 mg/kg (wet-weight) in seawater fish [54]. Recently, Sobolev et al. [11] also recorded higher concentrations of As in the Russian Arctic which were not recommended for human consumption. Further, the comparison of the current study on essential elements such as copper (Cu: 0.255–1.740 mg/kg), cobalt (Co: 0.015–0.051 mg/kg), selenium (Se: 0.501–1.206 mg/kg), and zinc (Zn: 8.569–37.358 mg/kg) showed considerably higher concentrations in fish species of Svalbard, High Arctic, than the fish species of the Russian Arctic [11]. Benthic organisms analyzed during the present study showed significantly higher concentrations than the fish species of Svalbard. Arctic fishes feed primarily on zooplankton, salmon eggs, insects, and benthos [55], which may possibly result in a bioaccumulation process through the food chain in the High Arctic.
Out of eleven blood samples of different fishes screened for AFPs, two species (Gadus morhva and Anashichas lupus) have shown weak activity, while four species (Gadus oguc, Gymnocanthus tricuspis, Liparis spp., Myoxocephalus scorpius) have shown strong AFP activity (Figure 3a–f). AFPs help fishes to survive in the cold Arctic water.
4. Conclusions
An overall comparison between the two sets of data reveals that benthic organisms had a greater concentration of most elements as compared to the fishes. This is the first study on determining the elemental concentration of High Arctic fish and invertebrates. It is assumed that elemental concentrations present in High Arctic organisms are above the normal range. Therefore, it is advised that the human impact must be avoided to protect the fragile ecosystem of the High Arctic. The data of the present study will be useful to the scientific community and public officials involved in the environmental monitoring of Arctic ecosystems.
Author Contributions
Conceptualization, supervision, Sampling, S.M.S.; methodology, formal analysis, writing—original draft preparation: P.S. and R.U.M.; writing—review and editing, S.M.S. and M.T. All authors have read and agreed to the published version of the manuscript.
Funding
NCAOR: Ministry of Earth Sciences, DST India and Alfred Wegener Institute, Germany.
Institutional Review Board Statement
Study did not require ethical approval. However, Markus Brand has already taken sampling permission under project RIS-ID 2834.
Informed Consent Statement
Not applicable.
Data Availability Statement
We agree MDPI Research Data Policies.
Acknowledgments
We are grateful to the Governor of Svalbard for sampling permission under project RIS-ID 2834. We thank the crew of the AWIPEV Arctic Research Base for their great support of our fieldwork. SMS is thankful to NCAOR and BHU for the support. We are grateful to Sakae Tsuda, National Institute of Advanced Industrial Science & Technology (NIAIST), Japan, for providing AFP analyses facilities, and Yuichi Hanada for the technical help. Authors are thankful to the Norwegian Polar Institute for the map. We thank Markus Brand for helping prepare the samples of Arctic fishes.
Conflicts of Interest
The authors declare no conflict of interest.
References
- Singh, S.M.; Kumar, A.; Sharma, P.; Ravindra, M.; Upadhya, A.K.; Ravindra, R. Elemental variations in glacier cryoconites of Indian Himalaya and Spitsbergen, Arctic. Geosci. Front. 2017, 8, 1339–1347. [Google Scholar] [CrossRef]
- Belitz, H.D.; Grosch, W.; Schieberle, P. Lehrbuch Der Lebensmittelchemie; Springer: Berlin/Heidelberg, Germany, 2001. [Google Scholar]
- Ward, N.T. Trace elements. In Environmental Analytical Chemistry. Blackie Academic and Professional; Fifield, F.W., Haines, P.J., Eds.; Chapman & Hall: London, UK, 1995. [Google Scholar]
- IPCC. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change; Solomon, S., Qin, S., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L., Eds.; Cambridge University Press: Cambridge, UK, 2007. [Google Scholar]
- Kamaruzzaman, C.Y.; Rina, Z.; John, B.A.A.; Jalal, K.C.A. Heavy metal accumulation in commercially importantfishes of South West Malaysian coast. Res. J. Environ. Sci. 2011, 5, 595–602. [Google Scholar] [CrossRef]
- Mansour, S.A.; Sidky, M.M. Ecotoxicological studies. 3. Heavy metals contaminating water and fish from Fayoum Governorate, Egypt. Food Chem. 2002, 78, 15–22. [Google Scholar] [CrossRef]
- Ni, I.H.; Wang, W.X.; Tam, Y.K. Transfer of Cd, Cr and Zn from zooplankton prey to mudskipper Periophthalmus cantonensis and glassy Ambassisurotaenia fishes. Mar. Ecol. Prog. Ser. 2000, 194, 203–210. [Google Scholar] [CrossRef]
- Roméo, M.; Siau, Y.; Sidoumou, Z.; Gnassia-Barelli, M. Heavy metal distribution indifferent fish species from the Mauritania coast. Sci. Total Environ. 1999, 232, 169–175. [Google Scholar] [CrossRef]
- Yilmaz, B. Levels of heavy metals (Fe, Cu, Ni, Cr, Pb, and Zn) in tissue of Mugilcephalus and Trachurus mediterraneusfrom Iskenderun Bay, Turkey. Environ. Res. 2003, 92, 277–281. [Google Scholar] [CrossRef]
- Agusa, T.; Kunito, T.; Sudaryanto, A.; Monirith, I.; Kan-Atireklap, S.; Iwata, H.; Ismail, A.; Sanguansin, J.; Muchtar, M.; Tana, T.S.; et al. Exposure assessment for trace elements from consumption of marine fish in Southeast Asia. Environ. Pollut. 2007, 145, 766–777. [Google Scholar] [CrossRef]
- Sobolev, N.; Aksenov, A.; Sorokina, T.; Chashchin, V.; Ellingsen, E.; Nieboer, D.G.; Varakina, Y.; Veselkina, E.; Kotsur, D.; Thomassen, Y. Essential and non-essential trace elements in fish consumed by indigenous peoples of the European Russian Arctic. Environ. Pollut. 2019, 253, 966e973. [Google Scholar] [CrossRef]
- Darmody, R.G.; Thorn, C.E. Elevation, age, soil development, and chemical weathering at Storbreen, Jotunheimen, Norway. Geogr. Ann. Ser. A Phys Geogr. 1997, 79, 215–222. [Google Scholar] [CrossRef]
- Pacyna, M.; Vitols, V.; Hanssen, J.E. Size distributed composition of the Arctic aerosol at Ny-Alesund, Spitsbergen. Atmos. Environ. 1984, 18, 2447–2459. [Google Scholar] [CrossRef]
- Maenhaut, W.; Cornille, P.; Pacyna, J.M.; Vitols, V. Trace element composition and origin of the atmospheric aerosol in the Norwegian Arctic. Atmos. Environ. 1989, 23, 2551–2569. [Google Scholar] [CrossRef]
- Wadham, J.L.; Hallam, K.R.; Hawkins, J.; O’Connor, A. Enhancement of snowpack inorganic nitrogen by aerosol debris. Tellus 2006, 59, 229–241. [Google Scholar] [CrossRef]
- Eleftheriadis, K.; Vratolis, S.; Nyeki, S. Aerosol black carbon in the European Arctic: Measurements at Zeppelin station, Ny-Ålesund, Svalbard from 1998–2007. Geophys. Res. Lett. 2009, 36, L02809. [Google Scholar] [CrossRef]
- Boyle, J.F.; Rose, N.L.; Appleby, P.G.; Birks, H.J.B. Recent environmental change and human impact on Svalbard: The lake-sediment geochemical record. J. Paleolimnol. 2004, 31, 515–530. [Google Scholar] [CrossRef]
- Rose, N.L.; Rose, C.L.; Boyle, J.F.; Appleby, P.G. Lake-Sediment Evidence for Local and Remote Sources of Atmospherically Deposited Pollutants on Svalbard. J. Paleolimnol. 2004, 31, 499–513. [Google Scholar] [CrossRef]
- Snyder-Conn, E.; Garbarino, J.R.; Hoffman, G.L.; Oelkers, A. Soluble trace elements and total mercury in Arctic Alaskan snow. Arctic 1997, 50, 201–215. [Google Scholar] [CrossRef]
- Borgå, K.; Campbell, L.; Gabrielsen, G.W.; Norstrom, R.J.; Muir, D.C.G.; Fisk, A.T. Regional and species specific bioaccumulation of major and trace elements in Arctic seabirds. Environ. Toxicol Chem. 2006, 25, 2927–2936. [Google Scholar] [CrossRef]
- Barrie, L.A. Arctic air pollution: An overview of current knowledge. Atmos. Environ. 1986, 20, 643–663. [Google Scholar] [CrossRef]
- Pacyna, J.M.; Ottar, B.; Tomza, U.; Maenhaut, W. Long-range transport of trace elements to NyÅlesund, Spitsbergen. Atmos. Environ. 1985, 19, 857–865. [Google Scholar] [CrossRef]
- Aldahan, A.; Possnert, G.; Scherer, R.; Shi, N.; Backman, J.; Boström, K. Trace-element and major-element stratigraphy in quaternary sediments from the Arctic Ocean and implications for glacial termination. J. Sediment Res. 2000, 70, 1095–1106. [Google Scholar] [CrossRef]
- Hicks, S.; Isaksson, E. Assessing source areas of pollutants from studies of fly ash, charcoal, and pollen from Svalbard snow and ice. J. Geophys. Res. 2006, 111, D02113. [Google Scholar] [CrossRef]
- Lu, Z.; Cai, M.; Wang, J.; Yin, Z.; Yang, H. Levels and distribution of trace metals in surface sediments from Kongsfjorden, Svalbard, and Norwegian Arctic. Environ. Geochem. Health 2013, 35, 257–269. [Google Scholar] [CrossRef]
- Singh, S.M.; Naik, S.; Mulik, R.U.; Sharma, J.; Upadhyay, A.K. Elemental composition and bacterial occurrence in sediment samples on two sides of Brøggerhalvøya, Svalbard. Polar Rec. 2015, 51, 680–691. [Google Scholar] [CrossRef]
- Singh, S.M.; Sharma, J.; Gawas-Sakhalkar, P.; Upadhyay, A.K.; Mulik, R.U.; Naik, S.; Bohare, P.; Ravindra, R. Elemental composition and bacterial incidence in firn-cores at Midre Lovénbreen glacier, Svalbard, Arctic. Polar Rec. 2015, 51, 39–48. [Google Scholar] [CrossRef]
- Singh, S.M.; Sharma, J.; Gawas-Sakhalkar, P.; Upadhyay, A.K.; Naik, S.; Bande, D.; Ravindra, R. Chemical and bacteriological analysis of soil from the middle and late Weichselian from Western Spitsbergen, Arctic. Quatern. Int. 2012, 271, 98–105. [Google Scholar] [CrossRef]
- Singh, S.M.; Sharma, J.; Gawas-Sakhalkar, P.; Upadhyay, A.K.; Naik, S.; Pedneker, S.; Ravindra, R. Atmospheric deposition studies of heavy metals in arctic by comparative analysis of lichens and cryoconite. Environ. Monit. Assess. 2012, 185, 1367–1376. [Google Scholar] [CrossRef]
- Łqokas, E.; Zaborska, A.; Kolicka, M.; Ro_zycki, M.; Zawierucha, K. Accumulation of atmospheric radionuclides and heavy metals in cryoconite holes on an Arctic glacier. Chemosphere 2016, 160, 162–172. [Google Scholar] [CrossRef]
- Brand, M.; Fischer, P. Species composition and abundance of the shallow water fish community of Kongsfjorden, Svalbard. Polar Biol. 2016, 39, 2155–2167. [Google Scholar] [CrossRef]
- Voronkov, A.; Hop, H.; Gulliksen, B. Diversity of hard-bottom fauna relative to environmental gradients in Kongsfjorden. Svalbard. Polar Res. 2013, 32, 11208. [Google Scholar] [CrossRef]
- Lippert, H.; Iken, K.; Rachor, E.; Wiencke, C. Macro fauna associated with macroalgae in the Kongsfjord (Spitsbergen). Polar Biol 2001, 24, 512–522. [Google Scholar]
- Werner, E.E. Species packing and niche complementarity in three sunfishes. Am. Nat. 1977, 111, 553–578. [Google Scholar] [CrossRef]
- Keast, A. Thepiscivore feeding guild of fishes in small freshwater ecosystems. Environ. Biol. Fishes. 1985, 12, 119–129. [Google Scholar] [CrossRef]
- Knight, C.A.; Hallett, J.; Devries, A.L. Solute effects on ice recrystallisation: An assessment technique. Cryobiology 1988, 25, 55–60. [Google Scholar] [CrossRef]
- Jia, Z.; Davies, P.L. Antifreeze proteins: An unusual receptor-ligand interaction. Trends Biochem. Sci. 2002, 27, 101–106. [Google Scholar] [CrossRef]
- Duman, J.G.; Olsen, T.M. Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology 1993, 30, 322–328. [Google Scholar] [CrossRef]
- DeVries, A.L.; Komatsu, S.K.; Feeney, R.E. Chemical and physical properties of freezing point-depressing glycoproteins from Antarctic fishes. J. Biol. Chem. 1970, 245, 2901–2908. [Google Scholar] [CrossRef]
- Fletcher, G.L.; Hew, C.L.; Davies, P.L. Antifreeze proteins of teleost fishes. Annu. Rev. Physiol. 2001, 63, 359–390. [Google Scholar] [CrossRef]
- Ewart, K.V.; Hew, C.L. Fish Antifreeze Proteins; World Scientific: Singapore, 2002. [Google Scholar]
- Able, K.W. A revision of Arctic snailfishes of the genus Liparis (Scorpaeniformes: Cyclopteridae). Copeia 1990, 1990, 476–492. [Google Scholar] [CrossRef]
- Węsławski, J.M.; Linkowski, T.B.; Herra, T. Fishes. In Atlas of the Marine Fauna of Southern Spitsbergen; Klekowski, R.Z., Węsławski, J.M., Eds.; Vertebrate University of Gdańsk, Institute of Oceanology: Gdańsk, Poland, 1990; pp. 67–195. [Google Scholar]
- Muus, B.J.; Nielsen, J.G. Sea Fish; Scandinavian Fishing Year Book: Hedehusene, Denmark, 1999; pp. 2551–2569. [Google Scholar]
- Hayward, P.J.; Ryland, J.S. Handbook of the Marine Fauna of North-West Europe; Oxford University Press Inc.: Oxford, UK, 2005. [Google Scholar]
- Oribhabor, B.J.; Ogbeibu, A.E. The ecological impact of anthropogenic activities on the predatory fish assemblage of a tidal creek in the Niger Delta, Nigeria. Res. J. Environ. Sci. 2010, 4, 271–279. [Google Scholar] [CrossRef]
- Emara, H.I.; El-Deek, M.S.; Ahmed, N.S. A comparative study on the levels of trace metals in some Mediterranean and Red Sea fishes. Chem. Ecol. 1993, 8, 119–127. [Google Scholar] [CrossRef]
- Hanna, R.G.M. Levels of heavy metals in some Red Sea fish before Hot Brine pools’ mining. Mar. Pollut. Bull. 1989, 20, 631–635. [Google Scholar] [CrossRef]
- El-Moselhy, K.M.; Othman, A.I.; Abd El-Azem, H.; El-Metwally, M.E.A. Bioaccumulation o heavy metals in some tissues of fish in the Red Sea. Egypt. J. Basic Appl. Sci. 2014, 1, 97–105. [Google Scholar] [CrossRef]
- Schenone, N.F.; Avigliano, E.; Goessler, W.; Cirelli, A.F. Toxic metals, trace and major elements determined by, I.C.PMS in tissues of Parapimelodusvalenciennis and Prochiloduslineatus from Chascomus Lake, Argentina. Microchem. J. 2014, 112, 127–131. [Google Scholar] [CrossRef]
- Marx, S.K.; Kamber, B.S.; McGowan, H.A. Provenance of long-travelled dust determined with ultra-trace-element composition: A pilot study with samples from New Zealand glaciers. Earth Surf. Process. Landf. 2005, 30, 699–716. [Google Scholar] [CrossRef]
- DiGiovanni, F.; Fellin, P. Transboundary Air Pollution. In Encyclopedia of Life Support Systems (EOLSS); Inyang, H.I., Daniels, J.L., Eds.; Springer: Berlin/Heidelberg, Germany, 2006; p. 339. [Google Scholar]
- European Commission. Commission Regulation (EC) No 1881/2006 of 19 December 2006 Setting Maximum Levels for Certain Contaminants in Foodstuffs (Text with EEA Relevance). Off. J. Eur. Union 2006, 364, 5–24. [Google Scholar]
- SanPiN 2.3.2.1078-01 Hygienic Demands of the Safeness and Nutritional Values of Food. Prescript N_ 18, 31.05 [CaнПиH 2.3.2.1078-01 «Gигиеничеcкие требoвaния безoпacнocти и пищевoй ценнocти пищевых прoдуктoв», Пocтaнoвление N_18, 31.05.2002]. Available online: https://www.dia-m.ru/upload/iblock/2b5/567-catalog (accessed on 18 May 2022).
- Lockhart, W.L.; Stern, G.A.; Low, G.; Hendzel, M.; Boila, G.; Roach, P.; Evans, M.S.; Billeck, B.N.; DeLaronde, J.; Friesen, S.; et al. A history of total mercury in edible muscle of fish from lakes in northern Canada. Sci. Total Environ. 2005, 351, 427–463. [Google Scholar] [CrossRef]
Figure 1.
Sampling sites into Kongsfzorden, Svalbard, High Arctic. Map modified from the Norwegian Polar Institute’s map resource (www.toposvalbard.npolar.no, accessed on 18 May 2022).
Figure 1.
Sampling sites into Kongsfzorden, Svalbard, High Arctic. Map modified from the Norwegian Polar Institute’s map resource (www.toposvalbard.npolar.no, accessed on 18 May 2022).
Figure 2.
High Arctic fish and invertebrates. (a) Myoxocephalus scorpius; (b) Gadus ogac; (c) Anarhichas lupus; (d) Liparis sp.; (e) Ophioceten sericeum; (f) Ophiura arctica; (g) Strongylocentrotus droebachiensis; (h) Worm: Polychaetes.
Figure 2.
High Arctic fish and invertebrates. (a) Myoxocephalus scorpius; (b) Gadus ogac; (c) Anarhichas lupus; (d) Liparis sp.; (e) Ophioceten sericeum; (f) Ophiura arctica; (g) Strongylocentrotus droebachiensis; (h) Worm: Polychaetes.
Figure 3.
AFP activity of High Arctic fish. (a). Anashichas lupus; (b). Gadus morhva; (c). Gadus oguc; (d). Gymnocanthus tricuspis; (e). Liparis sp.; (f). Myoxocephalus scorpius.
Figure 3.
AFP activity of High Arctic fish. (a). Anashichas lupus; (b). Gadus morhva; (c). Gadus oguc; (d). Gymnocanthus tricuspis; (e). Liparis sp.; (f). Myoxocephalus scorpius.
Table 1.
Sampling locations and length and weight of Kongsfzorden fishes.
| Fish Code Number | Fjord Side | Location | Catch Device | Depth (m) | Species | Length_Std (cm) | Weight Total | Sex |
|---|---|---|---|---|---|---|---|---|
| F (1738) | North | Hansneset Central | Double Fyke Net | 5 | Anarhichas lupus | 49 | 1321.07 | F |
| E (1643) | North | London | Double Fyke Net | 5 | Gadus ozak | 30 | 352.88 | F |
| A2 (1644) | South | Old Pier Central | Double Fyke Net | 5 | Gadus morhua | 37.5 | 634.7 | F |
| A1 (1707) | North | Hansneset South | Double Fyke Net | 5 | Gadus morhua | 16.5 | 49.23 | U |
| B2 (1737) | South | Gasebu | Double Fyke Net | 5 | Gymnocanthus tricuspis | 14.5 | 65.63 | F |
| C1 (1770) | North | Hansneset South | Double Fyke Net | 5 | Liparis sp. | 12.5 | 36.6 | M |
| C2 (1703) | North | Hansneset South | Fyke Net with Bait | 3 | Liparis sp. | 14.5 | 71.58 | M |
| D1 (1700) | South | Old Pier Central | Double Fyke Net | 5 | Myoxocephalus Scorpius | 13.5 | 53.6 | F |
| D2 (1702) | South | Old Pier Central | Fyke Net with Bait | 3 | Myoxocephalus Scorpius | 11.5 | 28.76 | M |
| D3 (1704) | North | Hansneset South | Fyke Net with Bait | 12 | Myoxocephalus Scorpius | 17 | 108.9 | F |
Table 2.
Lithophilic elemental composition (in mg/kg) in the Arctic fish and invertebrates.
| Study Site Organism | Sample | Ba | Cr | Cs | Rb | Sr | U | V | |
|---|---|---|---|---|---|---|---|---|---|
| LOQ (mg/kg) | 0.01 | 0.01 | 0.01 | 0.01 | 0.05 | 0.01 | 0.01 | ||
| Kongsfzorden | Fish | F (1738) | BLQ | 0.149 ± 0.00 | 0.028 ± 0.00 | 1.509 ± 0.01 | 0.692 ± 0.01 | BLQ | BLQ |
| E (1643) | 0.129 ± 0.01 | 0.144 ± 0.01 | 0.100 ± 0.00 | 2.16 ± 0.03 | 2.927 ± 0.01 | BLQ | BLQ | ||
| A2 (1644) | 0.026 ± 0.00 | 0.197 ± 0.00 | 0.052 ± 0.00 | 2.171 ± 0.02 | 0.708 ± 0.01 | BLQ | BLQ | ||
| A1 (1707) | 0.056 ± 0.01 | 0.363 ± 0.01 | 0.069 ± 0.00 | 4.046 ± 0.02 | 8.651 ± 0.01 | BLQ | BLQ | ||
| B2 (1737) | 0.032 ± 0.01 | 0.319 ± 0.00 | 0.035 ± 0.00 | 1.665 ± 0.01 | 8.276 ± 0.04 | BLQ | 0.017 ± 0.00 | ||
| B1 (1763) | 0.024 ± 0.01 | 0.442 ± 0.01 | 0.087 ± 0.00 | 2.894 ± 0.02 | 4.094 ± 0.05 | BLQ | BLQ | ||
| C1 (1770) | 0.013 ± 0.00 | 0.235 ± 0.01 | 0.022 ± 0.00 | 1.866 ± 0.01 | 2.989 ± 0.04 | BLQ | 0.020 ± 0.00 | ||
| C2 (1703) | 0.042 ± 0.00 | 0.134 ± 0.01 | 0.031 ± 0.00 | 1.682 ± 0.01 | 5.798 ± 0.05 | BLQ | 0.031 ± 0.00 | ||
| D1 (1700) | 0.073 ± 0.01 | 0.378 ± 0.01 | 0.027 ± 0.00 | 1.619 ± 0.01 | 4.277 ± 0.07 | BLQ | 0.021 ± 0.00 | ||
| D2 (1702) | 0.143 ± 0.01 | 0.757 ± 0.01 | 0.034 ± 0.00 | 1.669 ± 0.02 | 21.903 ± 0.14 | BLQ | 0.051 ± 0.00 | ||
| D3 (1704) | 0.048 ± 0.01 | 0.182 ± 0.01 | 0.044 ± 0.00 | 1.581 ± 0.03 | 7.212 ± 0.06 | BLQ | 0.018 ± 0.00 | ||
| Kongsfzorden | Invertebrates | G (SFS) | 6.823 ± 0.03 | 0.392 ± 0.00 | 0.032 ± 0.00 | 1.048 ± 0.02 | 1116.6 ± 10.69 | 0.169 ± 0.00 | 0.453 ± 0.01 |
| H (SFB) | 27.559 ± 0.28 | 0.916 ± 0.01 | 0.029 ± 0.00 | 1.404 ± 0.01 | 1080.1 ± 3.97 | 0.519 ± 0.01 | 4.849 ± 0.02 | ||
| I (SU) | 16.123 ± 0.08 | 0.914 ± 0.01 | 0.095 ± 0.00 | 1.943 ± 0.01 | 971.53 ± 10.20 | 0.098 ± 0.00 | 1.56 ± 0.01 | ||
| J (WOEM) | 0.880 ± 0.02 | 0.394 ± 0.00 | 0.017 ± 0.00 | 1.171 ± 0.02 | 48.578 ± 0.66 | 0.161 ± 0.00 | 1.418 ± 0.01 | ||
F (1738) = Anarhichas lupus; E (1643) = Gadus ogac; A2 (1644) = Gadus morhu; A1 (1707) = Gadus morhu; B2 (1737) = Gymnocanthus tricuspis; B1 (1763) = Gymnocanthus tricuspis; C1 (1770) = Liparis spp.; C2 (1703) = Liparis spp.; D1 (1700) = Myoxocephalus scorpius; D2 (1702) = Myoxocephalus scorpius; D3 (1704) = Myoxocephalus scorpius; G (SFS) = Brittle star: Ophiura albida; H (SFB) = Brittle star: Ophiura sarsii; I (SU) = Sea Urchin: Strongylocentrotus droebachiensis; J (WOEM) = Worm: Polychaetes. BLQ = Below limit of quantification; LOQ = Limit of quantification.
Table 3.
Chalcophilic elemental composition (in mg/kg) in the Arctic fish and invertebrates.
| Study Site Organism | Sample | As | Bi | Cd | Cu | Pb | Zn | |
|---|---|---|---|---|---|---|---|---|
| LOQ (mg/kg) | 0.01 | 0.05 | 0.02 | 0.05 | 0.01 | 0.1 | ||
| Kongsfzorden | Fish | F (1738) | 14.541 ± 0.11 | BLQ | BLQ | 0.262 ± 0.01 | BLQ | 11.616 ± 0.05 |
| E (1643) | 26.181 ± 0.02 | BLQ | BLQ | 0.594 ± 0.01 | 0.037 ± 0.00 | 13.006 ± 0.13 | ||
| A2 (1644) | 13.212 ± 0.06 | BLQ | BLQ | 0.255 ± 0.01 | 0.117 ± 0.01 | 8.569 ± 0.02 | ||
| A1 (1707) | 6.982 ± 0.12 | BLQ | BLQ | 0.880 ± 0.01 | BLQ | 22.264 ± 0.22 | ||
| B2 (1737) | 9.828 ± 0.07 | BLQ | BLQ | 0.609 ± 0.01 | 0.015 ± 0.00 | 12.811 ± 0.02 | ||
| B1 (1763) | 35.84 ± 0.15 | BLQ | BLQ | 1.740 ± 0.04 | 0.028 ± 0.00 | 27.245 ± 0.54 | ||
| C1 (1770) | 8.694 ± 0.04 | BLQ | BLQ | 0.901 ± 0.01 | 0.029 ± 0.00 | 15.084 ± 0.1 | ||
| C2 (1703) | 16.253 ± 0.10 | BLQ | BLQ | 0.840 ± 0.02 | 0.011 ± 0.00 | 16.326 ± 0.05 | ||
| D1 (1700) | 3.291 ± 0.01 | BLQ | BLQ | 0.946 ± 0.01 | 0.020 ± 0.00 | 16.578 ± 0.1 | ||
| D2 (1702) | 2.781 ± 0.03 | BLQ | BLQ | 0.857 ± 0.02 | 0.029 ± 0.00 | 37.358 ± 0.30 | ||
| D3 (1704) | 4.537 ± 0.09 | BLQ | BLQ | 0.814 ± 0.01 | 0.030 ± 0.00 | 14.544 ± 0.16 | ||
| Kongsfzorden | Invertebrates | G (SFS) | 1.221 ± 0.02 | BLQ | 0.214 ± 0.01 | 0.775 ± 0.02 | 0.261 ± 0.01 | 20.178 ± 0.19 |
| H (SFB) | 4.139 ± 0.04 | 0.652 ± 0.02 | BLQ | 10.045 ± 0.05 | 5.258 ± 0.05 | 40.695 ± 0.20 | ||
| I (SU) | 4.506 ± 0.04 | BLQ | BLQ | 0.918 ± 0.02 | 0.473 ± 0.01 | 23.731 ± 0.02 | ||
| J (WOEM) | 13.458 ± 0.14 | 0.904 ± 0.01 | BLQ | 2.113 ± 0.01 | 0.884 ± 0.01 | 77.622 ± 0.34 | ||
All data are mean of triplicate readings.
Table 4.
Siderophilic elemental composition (in mg/kg) in Arctic fish and invertebrates.
| Study Site Organism | Sample | Co | Fe | Mn | Ni | |
|---|---|---|---|---|---|---|
| LOQ (mg/kg) | 0.01 | 0.5 | 0.05 | 0.1 | ||
| Kongsfzorden | Fish | F (1738) | BLQ | 0.799 ± 0.01 | 0.165 ± 0.00 | 0.124 ± 0.02 |
| E (1643) | BLQ | 2.91 ± 0.02 | 0.344 ± 0.00 | 0.165 ± 0.03 | ||
| A2 (1644) | BLQ | 0.907 ± 0.01 | 0.262 ± 0.01 | 0.249 ± 0.04 | ||
| A1 (1707) | 0.024 ± 0.00 | 5.479 ± 0.06 | 1.094 ± 0.01 | 0.225 ± 0.07 | ||
| B2 (1737) | 0.021 ± 0.00 | 3.179 ± 0.01 | 0.626 ± 0.01 | 0.273 ± 0.05 | ||
| B1 (1763) | 0.029 ± 0.00 | 8.141 ± 0.12 | 1.168 ± 0.01 | 0.177 ± 0.05 | ||
| C1 (1770) | 0.038 ± 0.00 | 3.395 ± 0.04 | 0.407 ± 0.00 | 0.257 ± 0.04 | ||
| C2 (1703) | 0.051 ± 0.00 | 4.573 ± 0.04 | 0.554 ± 0.01 | 0.24 ± 0.03 | ||
| D1 (1700) | 0.028 ± 0.00 | 4.401 ± 0.05 | 0.517 ± 0.01 | 0.246 ± 0.03 | ||
| D2 (1702) | 0.041 ± 0.00 | 7.248 ± 0.06 | 1.311 ± 0.01 | 0.439 ± 0.04 | ||
| D3 (1704) | 0.015 ± 0.00 | 3.533 ± 0.06 | 0.656 ± 0.01 | 0.364 ± 0.06 | ||
| Kongsfzorden | Invertebrates | G (SFS) | 0.541 ± 0.01 | 83.72 ± 0.14 | 19.848 ± 0.21 | 2.668 ± 0.05 |
| H (SFB) | 0.774 ± 0.01 | 438.34 ± 1.95 | 64.834 ± 0.20 | 3.778 ± 0.08 | ||
| I (SU) | 0.733 ± 0.01 | 240.95 ± 2.08 | 19.491 ± 0.21 | 2.616 ± 0.07 | ||
| J (WOEM) | 1.336 ± 0.01 | 129.50 ± 1.09 | 14.13 ± 0.06 | 1.686 ± 0.02 | ||
All data are mean of triplicate readings.
Table 5.
Other elemental composition (in mg/kg) in the Arctic fish and invertebrates.
| Study Site Organism | Sample | Se | Ag | |
|---|---|---|---|---|
| LOQ (mg/kg) | 0.05 | 0.05 | ||
| Kongsfzorden | Fish | F (1738) | 0.816 ± 0.04 | BLQ |
| E (1643) | 0.663 ± 0.03 | BLQ | ||
| A2 (1644) | 0.501 ± 0.02 | BLQ | ||
| A1 (1707) | 0.829 ± 0.08 | BLQ | ||
| B2 (1737) | 0.654 ± 0.03 | BLQ | ||
| B1 (1763) | 1.206 ± 0.05 | BLQ | ||
| C1 (1770) | 0.643 ± 0.01 | BLQ | ||
| C2 (1703) | 1.034 ± 0.01 | BLQ | ||
| D1 (1700) | 0.804 ± 0.02 | BLQ | ||
| D2 (1702) | 0.663 ± 0.05 | BLQ | ||
| D3 (1704) | 0.697 ± 0.02 | BLQ | ||
| Kongsfzorden | Invertebrates | G (SFS) | 0.395 ± 0.03 | 1.143 ± 0.01 |
| H (SFB) | 1.171 ± 0.05 | 1.189 ± 0.02 | ||
| I (SU) | 1.063 ± 0.10 | 0.367 ± 0.01 | ||
| J (WOEM) | 3.978 ± 0.02 | 0.330 ± 0.01 | ||
All data are mean of triplicate readings.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
MDPI and ACS Style
Singh, S.M.; Tsuji, M.; Singh, P.; Mulik, R.U. Elemental Composition and Freezing Tolerance in High Arctic Fishes and Invertebrates. Sustainability 2022, 14, 11727. https://doi.org/10.3390/su141811727
AMA Style
Singh SM, Tsuji M, Singh P, Mulik RU. Elemental Composition and Freezing Tolerance in High Arctic Fishes and Invertebrates. Sustainability. 2022; 14(18):11727. https://doi.org/10.3390/su141811727
Chicago/Turabian StyleSingh, Shiv Mohan, Masaharu Tsuji, Purnima Singh, and Ravindra Uttam Mulik. 2022. "Elemental Composition and Freezing Tolerance in High Arctic Fishes and Invertebrates" Sustainability 14, no. 18: 11727. https://doi.org/10.3390/su141811727
Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.
