The Role of the Biogeochemical Conditions of the Marine Environment on the Trace Element Content in Pacific Salmon

Abstract

The levels of six chemical elements (mercury, arsenic, lead, cadmium, zinc and copper) were examined in two species of Pacific salmon, genus Oncorhynchus , pink salmon (O. gorbuscha ), and chum salmon (O. keta ) that were caught in the Kuril waters in July 2013. Concentrations of toxic elements (Hg, As, Pb, Cd) in both species were shown to be below the maximum concentration limits of these trace elements for seafood. The concentrations of these elements were compared between wild salmon and hatchery salmon of the Pacific and Atlantic oceans.

Keywords

Mercury ; Arsenic ; Lead ; Cadmium ; Zinc ; Copper ; Pink salmon ; Chum salmon ; Kuril waters

Introduction

Despite the apparent uniformity and homogeneity of the water masses in the sea, there are areas similar to terrestrial biogeochemical provinces. Abnormalities or deviations from the background in the environment and biota stipulated by the geochemical features of these zones are not as pronounced as in the sea. They appear not only in the existence of endemic diseases caused by changes in the mineral metabolism of terrestrial organisms but also in distinctive biocenoses and mineral compositions of organisms. In the sea, the difference between the concentrations of elements in a biogeochemical province and beyond it may not be as sharp as on land because of the nature of the environment.

The impact zones of anthropogenic origin, established in coastal areas, are well known. They are caused by technogenic pollution, which creates an abnormal concentration of a number of elements and compounds.

The impact zones of natural-anthropogenic origin are estuarine river zones, which reflect the nature of the drained soils and the character of polluted wastewater in the solid and liquid effluent to the sea.

Natural impact zones of the seas, which have peculiar biogeochemical provinces stipulated by the seepage of highly mineralized undersea brines and are influenced by deep and shallow streams of volcanic products, are understudied. Only upwellings, as highly productive areas of the ocean, have long attracted scientific study. The remaining zones with peculiar biocenoses have been studied for three or four decades. However, although the study and selection of biogeochemical provinces on land has a longer history, it began relatively recently, in the 1930s, by V.I. Vernadsky and A.P. Vinogradov.

The waters of the Kuril Islands and the Kamchatka coastal waters are areas where the effect of upwelling and volcanism is clearly manifested. However, although the high productivity of the Sea of Okhotsk and the Kuril–Kamchatka region and its causes are the subject of the detailed scrutiny of hydrobiologists, hydrochemists, and fishery science, the chemical composition of organisms and the factors that determine the content of micro-elements in organisms are much less studied. During the 1980–1990s, inhabitants of the intertidal and subtidal zones of Kamchatka and Kuril Islands, primarily indicator organisms, such as clams and brown mytilids fucus algae, interestingly showed enrichment by heavy metals — cadmium, zinc, nickel and other elements. Though these benthic organisms characterized the chemical and environmental conditions of their habitat, they did not give an idea of the more open waters of the region inhabited by nekton organisms. The most representative organisms are pelagic fish, and among them, the most important species from an economic point of view are the salmons.

Salmon are large pelagic fish that live primarily in the northern parts of the Pacific and Atlantic oceans, the Arctic Ocean and in the basins of rivers. The two most representative and abundant groups can be distinguished among the fish of the salmon family (Salmonidae ): Atlantic salmon and Pacific salmon. The most distributed representative of Atlantic salmon is Salmo salar . The leading genus of Pacific salmon is Oncorhynchus , which includes pink salmon O. gorbuscha , chum salmon O. keta , sockeye O. nerka , coho O. kisutch , Chinook salmon O. tshawytscha (king salmon), and Sim O. masou . There are several species of the genus Salmo in the Pacific, but they are fewer in number compared with the Pacific salmon genus Oncorhynchus .

Atlantic salmon can be found on both sides of the Atlantic ocean, but its numbers have dropped drastically. By the end of the twentieth and beginning of the twenty-first centuries, wild Atlantic salmon became the object of scientific research and sport fishing. Currently, more than 99% of Atlantic salmon live in fish ponds. Leaders in the production of hatchery salmon are Norway (520–550 thousand tonnes of Atlantic salmon and trout) and Chile (approximately 450 thousand tonnes of Atlantic salmon and trout) (World review…, 2012 ). At the same time, 50% of Pacific salmon reproduce on natural spawning grounds, while a quarter of the livestock population spawns in Kamchatka. However, even if Pacific salmon are reproduced in fish ponds, after their release, they feed in the open sea and ocean waters — in other words, they lead a pascual lifestyle.

As inhabitants of the epipelagic zone (0–200 m), salmon dwell mainly in the upper layer (0–50 m). The pascual area of Pacific salmon in wintertime is located between 40 and 45° N in the Subarctic or Arctic front, marked by high biological and fishery productivity. With the coming of spring, the warming of the upper layers of water and abundant plankton development the zone of active life shifts towards the North and Northeast. Salmon follow it without leaving the eutrophic area, which is the reason for their rapid growth. Masu salmon is the only type of Pacific salmon found only on the Asian shore, mainly in the Sea of Japan. Chum and pink salmon prevail on both sides of the Pacific — from the Peter the Great Bay and San Francisco to the Bering Strait.

Sockeye and Chinook are quite cold-water species, widely prevailing along the American coast. Chinook is the largest species of Pacific salmon, referred to by Americans as King salmon. All Pacific salmon spawn only once during their lifetime, perishing after spawning. This feature is distinctive from the Atlantic salmon, which spawn up to four times (Rukhlov, 1982  ;  Shuntov and Temnykh, 2005 ). Different salmon species spawn at different ages: chum enters the river on the third to fifth years of life; pink salmon, growing and developing faster than chum, returns 18 months after migration into the sea; Sockeye salmon spend from 1 to 5 years (average 2–3 years) in the sea; and Chinook salmon live from 1 to 6 years (average 3–4 years).

All Pacific salmon embed their hard roe in the ground (in a dug hole); therefore, they choose gravel and pebble, without a muck-bottom. After the fertilization of hard roe, the female fills in the hollow with pebbles. The roe develops under the hill, while formed alevin stay in it for the resorption of the vitelline eggs. Fry in some species immediately migrate with the stream (chum, pink salmon), while the others remain in the river for a year or two years (sockeye, chinook, coho, masu salmon). Experiments have proved that salmon find their river by smell, no matter how strong it is.

The main locations of concentrations of Pacific salmon in Russian waters can be divided into several groups that differ in species composition, biomass quantity of salmon and duration of the period of their elevated concentrations. Thus, chum and sockeye salmon dominate in the deep water area of the Bering Sea, while pink and chum salmon dominate the rest of species in the deep water area of Sea of Okhotsk. The Northern Kuril straits are the main migration corridor for spawning schools of the Western Kamchatka sockeye, coho, chinook, chum, and pink salmon fingerlings migrating into the ocean. The Kuril waters and the Sea of Okhotsk are dominated by pink and chum salmon. Northern deep water areas of the Sea of Japan as well as the Kuril waters serve as transit zones for the Western Kamchatka salmon migrations: masu and pink salmon spawn in April and July, autumn chum spawn October–December, while masu and pink salmon juveniles grow through the fall and winter. In the offshore areas of the Far Eastern seas, significant salmon concentrations are observed only when the sire approaches to spawn and during the redistribution of juveniles that migrated down into open waters. This period lasts from June to September (Temnykh, 2004 ).

Pacific salmon represent the largest group, and therefore, it is very important for fishery purposes. Ninety percent of the catches are provided by three major species: pink salmon, chum and sockeye (Table 1 ).

Table 1. Inshore catching of Pacific salmon in the main fishery areas of the Far East in 2011, th. tonnes (Shuntov and Temnykh, 2011 ).

Area	All species	Pink salmon	Chum	Sockeye
Anadyr	2.1	0.4	1.4	0.3
Karaginsky	186.3	177.7	6.4	2.0
Petropavlovsk-Commander	18.1	4.7	2.3	9.3
West Kamchatka	44.7	6.0	14.9	21.0
Magadan region	11.6	9.4	2.1	–
Northern coast of Sea of Okhotsk (Khabarovsky region)	14.5	4.7	9.4	0.1
Amur basin	19.0	4.4	15.6	–
Sakhalin Island (Sea of Okhotsk)	192.3	176.7	15.5	–
South Kuril Islands	11.5	6.2	5.3	–
Northern Kuril Islands	3.0	0.3	1.2	0.9
Tatar Strait (Khabarovsky region)	0.2	0.1	0.1	–
Primorye	0.1	0.01	0.1	–
Southwest Sakhalin	1.2	0.05	1.2	–
All 6 species of the Far Eastern basin	504.6	389.7	75.6	33.6

Pink salmon is the most numerous, smallest and fastest-growing species. It has a leading distributed value in Russian waters (Table 1 ). Although chum is the second most numerous species after pink salmon, it has a higher nutritional value and therefore a higher demand.

We studied the levels of six elements – Zn, Cu, Cd, Pb, As, and Hg – in chum and pink salmon species of Pacific salmon caught in the Kuril waters in July 2013 and compared the concentrations of these elements in the wild salmon and Pacific and Atlantic salmon species grown in fish ponds.

Among the studied trace elements, the first two, copper and zinc, are essential (indispensable) or real bioelements. The last four, cadmium, lead, arsenic, and mercury, are non-essential, but they are almost constantly present in body organs and tissues. In addition to the biological significance, these elements also have distinct physical features. Copper and zinc, if not introduced into the environment from copper–zinc production and use of their alloys and compounds in machinery equipment (ore mining, ore enrichment and smelting, electroplating workshops, anti-corrosion coatings, etc.) are tracers of anthropogenic impact on the environment. Lead, cadmium and mercury, topping all of the “black lists” of heavy metals due to their toxic effect on organisms in 1960–1970s, are tracers of technological environmental impact (Khristoforova, 1989 ).

Materials and Methods

Information on the content of trace elements in fish not only represents a scientific interest indicating the object quality and the quality of their habitat but also has practical importance. It is essential for the population that uses fish directly for food and for the processing industry. In the Russian context, salmons are used almost entirely, with minimum waste. Therefore, the identification of micro-elements was conducted using entire fish carcasses milled for homogeneity. For the purposes of analysis, six units of pink and chum were caught at the end of July 2013 in the northwestern Pacific Ocean relatively close to the Kuril Islands area (46°39′N, 163°38′E) during record expedition of the TINRO Centre.

All of the elements, except mercury were determined in the homogenates of carcasses and organs, which were dried at 85° following the mineralization of samples by concentrated HNO₃ of High Purity grade, according to GOST 26929-94 on the atomic absorption spectrophotometer Shimadzu AA 6800. The element identification accuracy as well as the possible contamination of samples in the analysis were controlled according to the four calibration solutions, including the baseline (zero) solution. Statistical data processing was performed using the standard Excel software. The results were recalculated to wet weight.

Mercury was identified in frozen (− 20°) carcass homogenates after the mineralization of the samples by nitric acid with hydrogen peroxide. The mass concentration of mercury (ppm of wet weight) was found by stripping voltammetry (SV) using the analyzer “Tomanalyt” (TA-4). The element content in the sample solutions was identified using the addition method of certified mixtures with established content of elements.

Results and Discussion

The analysis results are demonstrated in Table 2 .

Table 2. Average concentration of the trace elements (ppm of wet weight) in Pacific salmon (M  ± m , n  = 3) from the north-western Pacific.

No.⁎	Trace elements, ppm of wet weight⁎⁎
	Zn	Cu	Cd	Pb	As	Hg
1	2.24 ± 0.64	0.12 ± 0.04	0.07 ± 0.01	0.54 ± 0.18	0.92 ± 0.28	0.07 ± 0.01
2	2.48 ± 0.74	0.11 ± 0.03	0.08 ± 0.01	0.68 ± 0.20	0.94 ± 0.28	0.09 ± 0.02
3	3.15 ± 0.87	0.17 ± 0.08	0.11 ± 0.03	0.77 ± 0.23	1.27 ± 0.37	0.12 ± 0.04
4	3.34 ± 0.93	0.16 ± 0.07	0.12 ± 0.04	0.95 ± 0.28	1.32 ± 0.39	0.15 ± 0.04

⁎. 1 — pink salmon, ♂, weight (g) — 1208–1459; 2 — pink salmon, ♀, weight (g) — 1168–1272; 3 — chum, ♂, weight (g) — 1564–1609; 4 — chum, ♀, weight (g) — 1670–1982.

⁎⁎. MPC of toxic elements in fish and fish products in Russia: Pb — 1.0; As — 5.0; Cd — 0.2; Hg — 0.2 ppm of wet weight (in Canada: Hg — 0.5; in the United States: Cd — 3; Pb — 1.5; As — 86 ppm of wet weight).

As can be seen in male and female pink salmon of similar mass, the concentrations of elements have few differences. At the level of trends, only the content of Zn, Pb and Hg are slightly higher in female individuals. In chum salmon, in which all of the samples were much larger than pink salmon, the identified elements were present in larger quantities. Among the fish that were caught, chum females were larger than males, and the concentrations of all of the elements, except copper, were higher than in male individuals. Therefore, in wild fish that gained weight in the ocean, a direct relationship between the weight (and size) of individuals and the content of trace elements is observed. This consistency is disrupted when fish are grown in stocking ponds, where the growth runs in a short period of 12 to 23 months (depending on species) compared with the 2- to 5-year-long life of wild salmon. In a period of rapid and extensive growth, the accumulated contaminants are “diluted” by macronutrients, such as proteins or lipids. Canadian researchers Kelly et al. (2008) found a significant correlation between the concentration of total mercury in fish fillets and its size (kg) for wild chinook: the mercury content varied from approx. 0.01 ppm for 2 kg fish to 0.1 ppm for 8 kg fish.

Assessing the overall concentrations of toxic elements found in chum specimens that were caught in the ocean, it is important to emphasize that they are below the MPC levels determined in Russia and are also lower than in the standards adopted by Canada and the United States.

The same authors (Kelly et al., 2008 ) identified a broad range of trace elements in bred and wild salmon, including the wild chum from the inshore waters of British Columbia. They demonstrated that the concentrations of non-essential elements ranged from 0.001 ppm for Cd to 1 ppm for As. Pb and Hg concentrations ranged between 0.01 ppm and 0.05 ppm. The content of the essential elements Cu and Zn fluctuated between 1 and 5 ppm. While the concentrations of zinc in local chum and pink salmon (2.24–3.34 ppm of wet weight) were the same as in the salmon of the Canadian Pacific coast, the concentration of copper was significantly lower than in the British Columbia salmon. Hg concentrations in local salmon varied from 0.07 to 0.15 ppm, and lead concentrations ranged from 0.30 to 0.95 ppm — that is, they were more than an order of magnitude higher. Concentrations of As in local and Canadian samples were almost identical, while the content of Cd was significantly higher in local salmon.

It is important to emphasize that foreign authors, provide data on the content of trace elements in fish fillets. However, in discussing the results of Table 2 , we consider the entire fish carcass.

For a correct comparison of our results with the data reported in the works of foreign authors, we also determined the concentrations of elements in the muscles of Pacific salmon and compared them with the published data for Atlantic salmon — salmon reared in cages (Table 3  ;  Table 4 ).

Table 3. The average content of trace elements in the muscles of Pacific salmon (M  ± m , n  = 3) (July, 2013).

No.⁎	Defining elements, ppm of wet weight
	Zn	Cu	Cd	Pb	As	Hg
1	1.24 ± 0.31	0.10 ± 0.04	0.03 ± 0.02	0.45 ± 0.10	0.89 ± 0.32	0.02 ± 0.01
2	1.33 ± 0.25	0.11 ± 0.05	0.04 ± 0.01	0.55 ± 0.10	0.97 ± 0.42	0.04 ± 0.01
3	1.74 ± 0.40	0.15 ± 0.06	0.05 ± 0.03	0.63 ± 0.15	1.25 ± 0.44	0.06 ± 0.01
4	1.88 ± 0.36	0.16 ± 0.07	0.06 ± 0.02	0.78 ± 0.10	1.36 ± 0.57	0.08 ± 0.01

⁎. 1 — pink salmon, ♂, weight (g) — 1208–1459; 2 — pink salmon, ♀, weight (g) — 1168–1272; 3 — chum, ♂, weight (g) — 1564–1609; 4 — chum, ♀, weight (g) — 1670–1982.

Table 4. The concentration of trace elements in the muscles of Salmo salar bred in a rearing channel.

Country	Year	The concentration of toxic elements, ppm wet weight						Source
		Zn	Cu	Cd	Pb	As	Hg
Iceland	2004	–	–	0.08	0.15	0.80	0.073	Ásmundsdottir et al., 2005
Norway	2002	–	–	0.03	0.02	2.33	0.072	Easton et al., 2002
Norway	2003	18.50	1.11	0.00	0.10	0.53	0.09	Liaset et al., 2003
Norway	2007	5.48	0.49	0.11	0.09	0.45	0.129	Sivakumar et al., 2007
Norway	2010	17.25	1.13	0.01	0.08	1.13	0.09	Malde et al., 2010

As can be seen by comparing the data of Table 2  ;  Table 3 , the content of trace elements in salmon muscle is significantly lower than in the entire carcass. It is two times lower for mercury, which is found primarily in adipose tissue; about one and a half times lower for lead, which is concentrated mainly in the bones of fish; two times lower for cadmium, which accumulates mainly in the liver; and almost two times lower for zinc, which primary sedimentates in the gills and the gonads. Only the concentrations of the copper and arsenic remain the same both in the entire carcass and the muscles.

Although, due to the adjustment for several muscles, the contrast of trace element levels in the salmon of the Kuril and Canadian waters was reduced, and it is clear that the fish of the Western Pacific contain greater cadmium and lead concentrations and lower concentrations of copper than the fish of the Eastern Pacific.

A comparison of trace element composition of the two groups of salmon (Table 3  ;  Table 4 ) reveals that the mercury in Western Pacific salmon is about the same as in Atlantic salmon, although the concentration of this strictly regulated element is the lowest in the muscle of Pacific pink salmon. Arsenic is distributed more uniformly in the wild Pacific salmon samples, ranging from 0.89 ppm in pink salmon to 1.36 ppm in chum salmon. The greatest variability among the Atlantic salmon bred in the rearing channels is observed in the Norwegian fish fillets. It ranges from 0.45 to 2.33 ppm, while the average arsenic concentrations are quite similar in both groups of salmon. Cadmium concentrations in the Norwegian samples that were measured in different years differ by an order of magnitude, ranging from undetectable traces to 0.11 ppm. In cadmium content, Pacific salmon stands between the Norwegian and Canadian fish.

While the distribution of three elements – Hg, As, and Cd – in fillets of Pacific and Atlantic salmon appears to be more or less similar, the content of the other three elements in different groups of fish differs significantly and requires a deeper analysis of the causes.

A comparison of the data in Table 3  ;  Table 4 indicates that the fillets of salmon grown in fish ponds contains 5–10 times more zinc and copper than the wild Pacific salmon muscle. As was noted above, Zn and Cu are the tracers of anthropogenic impact on the environment and biota. There is no doubt that salmon bred in the inshore zone will be affected by higher contamination of shallow water compared to the open ocean. Additionally, there is an impact of feed prepared by man, sometimes containing freshwater fish. Finally, regardless of the manufacturers' endeavors, Norwegian fish will be affected by the influence of the Gulf Stream, a powerful stream of starting off the American coast that collects the coastal effluents and discharges them on the Scandinavian shore.

It can be noted that unlike bred Atlantic salmon, the wild Pacific chum and pink salmon caught in the Kuril waters have high concentrations of lead. While the lead content in the bred salmon fillets from both the Atlantic and Eastern Pacific (Canada) ranges between 0.02 and 0.15 ppm, it increases in the muscles of Kuril Western Pacific salmon from 0.45 ppm in male pink salmon to 0.78 ppm in female chum.

As was previously mentioned (Kelly et al., 2008 ), the concentrations in wild salmons may reflect geographic variations in the environment. They are reflected not only in salmon and other fish but also in all aquatic and terraneous organisms. Despite the apparent homogeneity of the water masses in the sea, there are biogeochemical provinces, as on land, that manifest in the original mineral composition of organisms (Khristoforova et al ., 1979  ;  Khristoforova and Bogdanova, 1981 ). The Pacific Ring of Fire starting from the volcanoes of Kamchatka continuing with volcanos of Kuril islands, Japanese islands and southern Western Pacific island arcs is a powerful source of geochemical impacts on the marine environment. The supplier of chemical elements in the environment is underwater and above-water volcanism. For example, on a small uninhabited coral island, Bio (Solomon Islands), the reason for a particular geochemical environment in coastal waters that caused an increase in the metal content in Caulerpa and Halimedales algae was the ash falls from the volcano Mbanya, located 100 km away from the island (Khristoforova and Bogdanova, 1980 ). As a result of post-volcanic processes, kilograms of Fe, Mn, Ag, Cu, and other metals are ejected daily from deep layers and, after dissolution in the thermal waters, are carried by streams (Markhinin, 1985 ).

Kuril–Kamchatka Trench, which delivers nutrients (Propp and Propp, 1988 ) and other elements through upwelling (Malinowskaya and Khristoforova, 1997 ) in the upper layers of the water, is also a source of the formation of impact geochemical zones in the Northwestern Pacific. The study of the metal content (Fe, Mn, Zn, Cu, Cd, Pb, Ni, Cr) in brown algae, bivalves and gastropods that inhabit the Kuril Islands and foul the navigation buoys along the Northwestern Pacific coast repeatedly demonstrates the existence of biogeochemical provinces in the sea, identified by elevated concentrations of elements in organisms (Khristoforova and Kavun, 1988 ; Kavun et al ., 1989  ; Kavun et al ., 2002  ; Kavun and Khristoforova, 1991  ;  Malinowskaya and Khristoforova, 1997 ).

In contrast to Zn and Cu, which are active migrant elements that are present in the marine environment in a soluble form and are easily spread by currents, Pb in saltwater is found predominantly in a suspended form that is less mobile and more localized (Yeats, 1988 ; Khristoforova et al ., 1993  ;  Khristoforova, 1994 ). It appears that this weak migrant is more easily fixed by organisms for this reason. First, it is fixed by plankton and then by its consumer nekton, including the mass fish of the upper pelagic and the studied Pacific pink and chum salmon.

Conclusion

Withal, the wild Pacific pink and chum salmon caught in the Kuril waters, meets the requirements for seafood for the content of the regulated toxic elements Cd, Pb, As and Hg. The content of each element does not exceed the maximum permitted concentrations approved by the Russian standards. Differences in the content of elements in wild Pacific salmon and Atlantic salmon bred in ponds represent a great scientific and practical interest. Higher concentrations of Zn and Cu in farmed salmon and of Pb in pink and chum salmon from the Kuril waters are caused by the same factor — the geochemical conditions of the environment. However, the impact conditions of the coastal waters evaluated by such tracers as zinc and copper are caused by anthropogenic activity, while the impact zones in the waters of the Western Pacific are formed under the influence of natural factors of modern volcanism and upwelling.

Acknowledgments

The research was supported by RFBR grant (no. 12-04-32043 ) and the Scientific Fund of FEFU (no. 12-04-13000-33/13 ).

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