Assessing the consumptive safety of fish with different mercury content in its muscles (water bodies of Vologda Oblast as a case study)

Mikhail Ya. Borisov; Elena S. Ivanova; Nikolay Yu. Tropin; Anastasia E. Shilova; Elena V. Ugryumova; Darya E. Bazhenova

To cite this article: Borisov, M.Ya. et al., 2023. Assessing the consumptive safety of fish with different mercury content in its muscles (water bodies of Vologda Oblast as a case study). Ecosystem Transformation 6 (4), 97-118. https://doi.org/10.23859/estr-230920

Received: 20.09.2023 Accepted: 26.10.2023 Published online: 13.11.2023

DOI 10.23859/estr-230920 EDN ONTMIZ УДК 574.64+613.2

Научная статья

Оценка безопасности употребления в пищу рыбы из водоемов Вологодской области с различным содержанием ртути в мышечной ткани

М.Я. Борисов1* , Е.С. Иванова2 , Н.Ю. Тропин1 , А.Е. Шилова1 , Е.В. Угрюмова1 , Д.Э. Баженова2

1 Вологодский филиал ФГБНУ «ВНИРО» («ВологодНИРО»), 160012, Россия, г. Вологда, ул. Левичева, д. 5

2 Череповецкий государственный университет, 162600, Россия, Вологодская обл., г. Череповец, пр. Луначарского, д. 5

*myaborisov@mail.ru

Аннотация. Содержание ртути в мышечной ткани рыб водных объектов Вологодской области варьирует в пределах от менее чем 0.001 до 2.492 мкг/г сырой массы. Минимальные средние значения отмечены для радужной форели и снетка (0.025 и 0.066 мкг/г), максимальные средние - для жереха и кильца (0.401 и 0.472 мкг/г). Установлено, что у 12.1% исследованных особей нехищных видов и 9.5% особей хищных видов рыб содержание ртути превышает нормативные уровни, действующие в РФ для этих групп видов (> 0.3 мкг/г и > 0.6 мкг/г соответственно). Доля исследованной рыбы, употребление которой приведет к превышению допустимого еженедельного поступления ртути в организм (RfD согласно US EPA) составляет 50% для детей дошкольного возраста (2-5 лет), 37% для детей младшего школьного возраста (6-10 лет), 24% для детей среднего школьного возраста (11-15 лет) и 18% для взрослого населения.

Ключевые слова: пресные водоемы, нехищные рыбы, хищные рыбы, рекомендации по потреблению, расчет безопасных доз

Финансирование. Работа Е.С. Ивановой выполнена при поддержке Российского научного фонда в рамках гранта № 23-24-00385, https://rscf.ru/project/23-24-00385/

Благодарности. Авторы благодарны всем сотрудникам Вологодского филиала ФГБНУ «ВНИРО», участвовавшим в сборе полевого материала.

ORCID:

М.Я. Борисов, https://orcid.org/0000-0002-0406-0540 Е.С. Иванова, https://orcid.org/0000-0002-6976-1452 Н.Ю. Тропин, https://orcid.org/0000-0002-7152-0543 А.Е. Шилова, https://orcid.org/0009-0006-8255-6863 Е.В. Угрюмова, https://orcid.org/0009-0003-2020-5222

Для цитирования: Борисов, М.Я. и др., 2023. Оценка безопасности употребления в пищу рыбы из водоемов Вологодской области с различным содержанием ртути в мышечной ткани. Трансформация экосистем 6 (4), 97-118. https://doi.org/10.23859/estr-230920

Поступила в редакцию: 20.09.2023 Принята к печати: 26.10.2023 Опубликована онлайн: 13.11.2023

Introduction

Currently, the problem of mercury contamination is of global concern. In 2013, more than 120 countries signed the Minamata Convention to protect human health and the environment from mercury contamination1. The World Health Organization (WHO) considers mercury among ten major chemical elements posing a threat to public health2. In the second half of XX century, WHO developed and recommended safe for human health levels of mercury concentrations in various biosubstrates, the standards for their presence in food, and the reference intake doses3. It is found that fish consumed as food is the main source of mercury intake in the human body (Cottrill et al., 2012). More than 90% of the total mercury in fish muscles is present in the most toxic methylated form (Myers et al., 2007). The majority of methylmercury from the consumed fish (> 95%) is easily absorbed through the gastrointestinal tract (Chouvelon et al., 2009). Its content in the human body increases with the proportion of fish in the weekly diet. The cumulative accumulation of mercury in the human body has neurotoxic effects, negatively affects the cardiovascular system, reproductive function and may bring to disruption of embryonic development (Houston, 2011; Rice et al., 2014). The Food and Agriculture Organization of the United Nations (FAO), the European Food Safety Authority (EFSA) and the US Environmental Protection Agency (EPA) recommend to estimate the safety of fish and seafood products in the diet via the calculation of a safe dose of mercury intake in the human body for a certain time (RfD)4. In the Russian Federation, the regulation of mercury intake in the human body is based on limiting the consumption of fish products with mercury copounds not exceeding MAC5.

Fishing is one of the traditional activities of the population in Vologda Oblast, rich in a variety of water bodies (Borisov et al., 2019). According to official data, the annual fish catch (up to 30 fish species) in the rivers and lakes of the region in the last decade reaches 2 thousand tons. Bream, smelt, roach, sabrefish, perch, and pikeperch play the greatest role in the structure of industrial catches, while perch, pike, and pikeperch, roach, bream and silver bream - in amateur catches. Fish is not only consumed by the local population, but also exported outside Vologda Oblast. Thus, traditionally frequent consumption of fish from local ponds and streams may put the population at risk from mercury exposure.

This study is aimed at assessing the consumptive safety of fish (from water bodies of Vologda Oblast) with different mercury content in its muscles.

1 UNEP. Minamata Convention Agreed by Nations. Retrieved 19 January 2013. Web page. URL: https://www.unep.org/news-and-stories/press-release/minamata-convention-agreed-nations (accessed: 04.09.2023).

2 WHO. Mercury and health, 2017. Web page. URL: https://www.who.int/news-room/fact-sheets/detail/mercury-and-health (accessed: 04.09.2023).

3 WHO. IPCS. Environmental health criteria 101: Methylmercury, 1993. World Health Organization, Geneva, 1993-2144.

4 UNEP. Executive summary of the document on guidance for identifying populations at risk from mercury exposure. Chiba, Japan, 24-28 January 2011.

5 SanPiN 2.3.2.1078-01. Hygienic requirements for the safety and nutritional value of food products.

Material and methods

The work summarizes the results of studies of mercury concentrations in muscle tissue of fish from the reservoirs and watercourses of Vologda Oblast for 2007-2023. A total of 98 different types of water bodies (at 112 sites of all 26 municipal districts), including 38 rivers, 50 lakes, 6 reservoirs, 3 ponds and 1 flooded quarry were studied (Fig. 1, Table 1). Fishing was implemented with fixed gill nets, drift nets, seines, fixed traps, trawls, spinning and fishing rods of various designs. Each fish specimen was thoroughly analyzed. Measurements of commercial length and body weight, sex identification, including selection of fish scale, fin arms and otoliths for subsequent age determination were performed. Muscle samples were taken from the midsection of the body between the lateral line and the dorsal fin, placed in plastic bags and stored at -20 °C.

The mercury content was determined in muscles of 10720 specimens of 34 species and ecological forms of fish (Table 1). All the examined fish specimens were the objects of aquaculture, industrial or amateur fishing and consumed by the population as food thereby being a potential source of mercury intake in the human body.

The mercury content in the samples was determined on a PA-915M mercury analyzer with a PIRO (Lumex) device using the atomic absorption pyrolysis method without preliminary sample preparation (Sholupov et al., 2004). Samples of 10-50 mg were placed on a quartz dispenser and transferred to a thermolysis cell to determine the total mercury content with further combustion at a temperature of about 600 °C for 1-2 minutes. Each sample was analyzed in two replications. The accuracy of analytical measurement methods was monitored after 30 measurements using the certified biological material DORM-4 (with a known mercury content of 0.41 ± 0.055 ^g Hg/g) and DOLT-5 (0.44 ± 0.18 ^g Hg/g).

To estimate the patterns of mercury accumulation, its content in individual species and trophic groups of fish was compared. The correlation between mercury concentration, length, weight and age of fish was analyzed. The names of fish species were given according to "Ryby v zapovednikakh Rossii" (2010). In terms of trophic specialization, groups of fish (ichthyophages, planktoichthyophag-es, euryphages, benthophages, phytobenthophages, planktivores) were identified by Yu.V. Slynko and V.G. Tereshchenko (2014) with allowance for specific feeding of fish from the water bodies of Vologda Oblast. During statistical analysis, two types of crucian carp (golden and silver), which did not differ significantly in mercury content, were combined into one group "crucian carp". Because of a significant difference in this indicator, in vendace a large mixed-feeding form "kilets", while in European smelt - a smelt with a short-cycle form and primarily feeding on zooplankton were identified.

Statistical analysis of the results was performed via using the Past 4.0 program (Hammer et al., 2001). For assessing the differences between the mercury content in muscle tissue of fish from different trophic groups, the nonparametric Kruskal-Wallis test (H-test) was applied. Differences were considered significant at a significance level of p < 0.05. The relationship between the mercury concentration in muscles of fish and their size / age parameters was estimated based on the Spearman's rank correlation coefficient (Rs). The relationship was statistically significant at p < 0.05. When Rs is within 0.3-0.5, the relationship is moderate, from 0.5 to 0.7- noticeable, from 0.7 and above - high.

To estimate a safe dose of fish consumption by the population, mercury concentrations in fish muscles were compared with those established by the RF sanitary and epidemiological rules and regulations (MAC for mercury in freshwater non-predatory and predatory fish: 0.3 ^g/g and 0.6 ^g/g wet weight, respectively). A safe dose and the proportion of fish specimens with mercury concentrations exceeding MAC were calculated as well.

Acceptable (safe) weekly fish consumption (CRlim) was defined differentially for each species using the formula (Bloom, 1992):

where CRlim is the permissible weekly consumption of fish (g/week); RfD - the permissible weekly intake of mercury in the human body, BW - a man weight, g; Cm - the concentration of mercury in the consumed fish, ^g/g; the EPA reference dose = 0.0007 ^g/g body weight per week6; the FAO reference

6 Guidance for assessing chemical contaminant data for use in fish advisories. Volume 1: Fish sampling and analysis. Third

Fig. 1. TFishing sites for mercury content measurement.

Table 1. Location, fish species composition and collected material to determine the mercury content in muscle tissue. Types of fish: 1 - sterlet, 2 - zope, 3 - bream, 4 - white-eye, 5 - bleak, 6 - asp, 7 - silver bream, 8 - silver crucian carp, 9 - golden carp, 10 - gudgeon, 11 - chub, 12 - ide, 13 - dace, 14 - sabrefish, 15 - roach, 16 - rudd, 17 - tench, 18 - pike, 19 - European smelt, 20 - smelt, 21 - vendace, 22 - kilets, 23 - whitefish, 24 - whitefish - nelma, 25 - grayling, 26 - rainbow trout, 27 - salmon, 28 -char, 29 - burbot, 30 - ruff, 31 - perch, 32 - pikeperch, 33 - Volga zander, 34 -Amur sleeper.

No. Water body Municipal district Fish species Number of species Number of specimens

3, 7, 15, 18, 19, 21, 22,

1 Lake Onega Vytegorsky 23, 25, 26, 27, 28, 29, 30, 31, 32 16 495

2 Lake Tudozero Vytegorsky 3, 7, 15, 16, 18, 23, 29, 31, 32 9 113

3 River Megra Vytegorsky 3, 15, 16, 18, 25, 29, 31 7 22

4 Lake Velikoye Vytegorsky 3, 7, 9, 14, 15, 16, 18, 29, 31, 32 10 224

5 Vytegorsk Reservoir Vytegorsky 3, 6, 7, 12, 14, 15, 16, 18, 31, 32, 33 11 104

6 Belousovsk Reservoir Vytegorsky 3, 5, 7, 14, 15, 18, 31, 32, 33 9 161

7 Novinkinsk Reservoir Vytegorsky 2, 3, 4, 6, 7, 12, 14, 15, 18, 30, 31, 32 12 77

8 Lake Kemskoye Vytegorsky 2, 18 2 57

9 Lake Kuzhozero Vytegorsky 3, 15, 31, 32 4 16

10 Kovzha Reservoir Vytegorsky 3, 15, 18, 21, 29, 31, 32 7 148

11 Lake Volotskoye Vashkinsky 3, 8, 15, 16, 30, 31, 32 7 77

12 Lake Borovskoye Vashkinsky 15, 31 2 27

13 Lake Ananino Vashkinsky 3, 15, 18, 19, 29, 30, 31 7 90

14 Lake Svyatozero Vashkinsky 3, 7, 12, 15, 16, 18, 19, 29, 30, 31 10 144

15 Lake Yarbozero Vashkinsky 3, 7, 12, 15, 16, 30, 31 7 51

16 River Kema Vashkinsky 3, 6, 18, 29, 32 5 13

17 Lake Beloye Vashkinsky, Belozersky 2, 3, 4, 6, 7, 9, 10, 12, 14, 15, 16, 17, 18, 20, 21, 29, 30, 31, 32, 33 20 851

18 Lake Andozero Belozersky 3, 7, 14, 15, 16, 18, 31, 32 8 103

19 Lake Kozhino Belozersky 3, 15, 16, 17, 18, 31 6 48

20 Lake Lozskoye Belozersky 3, 7, 12, 15, 16, 18, 31, 32 8 42

21 Lake Motkozero Belozersky 3, 7, 15, 16, 18, 29, 31, 32 8 71

22 Lake Azatskoye Belozersky 3, 7, 9, 15, 16, 18, 26, 31, 32 9 152

23 Lake Serkhlovskoye Babaevsky 18, 31 2 27

24 Lake Sinichye Chagodo-schensky 18, 31 1, 2, 3, 4, 7, 8, 10, 11, 2 49

25 River Mologa Ustyuzhensky 12, 14, 15, 18, 30, 31, 32, 33 16 474

26 River Kolp' Kaduisky 12, 15, 18, 31 4 21

27 River Suda Kaduisky 3, 7, 11, 15, 18, 29, 30, 31 8 153

No. Water body Municipal district Fish species Number of species Number of specimens

28 River Andoga Kaduisky 2, 3, 7, 15, 29, 31 6 19

29 Rybinsk Reservoir Cherepovetsky 3, 7, 8, 12, 15, 18, 21, 29, 30, 31, 32, 33 12 366

30 River Yagorba Cherepovetsky 2, 3, 6, 12, 15, 30, 31, 32 8 52

31 32 River Sheksna (Cherepovets) River Sheksna (village Poteryaevo) Cherepovetsky Sheksninsky 2, 3, 6, 7, 11, 12, 15, 18, 29, 31, 32 2, 3, 6, 7, 12, 14, 15, 18, 31, 32, 33 11 11 224 161

33 Lake Uzbinskoye Kirillovsky 15, 31 2 31

34 Sheksna Reservoir Kirillovsky, Sheksninsky 1, 2, 3, 4, 5, 6, 7, 8, 9, 12, 14, 15, 16, 17, 18, 21, 26, 29, 30, 31, 32, 33 22 848

35 quarries near the village of Kovrizhnovo Kirillovsky 3, 15, 31 3 18

36 Lake Il'inskoye Kirillovsky 3, 9, 18, 31 4 24

37 Lake Spasskoye Kirillovsky 3, 9, 15, 18, 31 5 48

38 Lake Borodaevskoye Kirillovsky 3, 9, 12, 15, 18, 31 6 61

39 Lake Veshchozero Kirillovsky 3, 5, 7, 12, 15, 29, 30, 31 8 173

40 Lake Svyatoye Kirillovsky 3, 5, 7, 15, 18, 19, 21, 29, 30, 31, 32 11 252

41 Lake Vozhe Kirillovsky, 3, 5, 7, 12, 15, 18, 29, 30, 31, 32 10 980

42 Lake Danislovo Vozhegodsky 15, 31 2 18

43 Lake Beketovskoye Vozhegodsky 9 1 58

44 River Ilmenets Vozhegodsky 13, 25 2 16

45 Lake Munskoye Vozhegodsky 9 1 37

46 Lake Orekhovo Vozhegodsky 15, 31 2 39

47 Lake Pertozero Vozhegodsky 3, 9, 15, 18, 26, 30, 31 7 148

48 Lake Sienskoye Vozhegodsky 15, 31 2 29

49 Lake Morenno Vozhegodsky 15 1 11

50 Lake Svyatoye Vozhegodsky 3, 9, 15, 18, 31 5 114

51 Lake Salozero Vozhegodsky 15, 31 2 65

52 River Vozhega Vozhegodsky 3, 7, 12, 13, 15, 18, 25, 29, 30, 31 10 193

53 Lake Gagatrino Vozhegodsky 31 1 25

54 Lake Korgozero Vozhegodsky 3, 15, 31 3 60

55 Lake Monozero Vozhegodsky 31 1 35

56 Lake Chunozero Vozhegodsky 15, 18, 31 3 48

57 Lake Dolgoye Vozhegodsky 3, 15, 18, 30, 31 5 62

58 Lake Tamenskoye Vozhegodsky 31 1 18

59 Lake Bolshoye Yakhrengskoye Vozhegodsky 15, 31 2 20

No. Water body Municipal district Fish species Number of species Number of specimens

60 Lake Pogorelovo Vozhegodsky 31 1 13

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61 Lake Chernoye Vozhegodsky 9, 15 2 16

62 63 64 65 River Kubena (Kharovsk town) River Uftyuga (Panikha village) River Uftyuga (Bogorodskoye village) River Uftyuga (Tavlash village) Kharovsky Ust-Kubinsky Ust-Kubinsky Ust-Kubinsky 13, 31 11, 13, 15, 18, 30, 31 3, 7, 12, 13, 15, 24, 31 3, 7, 12, 15, 18, 24, 29, 30, 31, 32 2 6 7 10 20 55 45 116

66 Lake Glukhoye Ust-Kubinsky 15, 18 2 9

67 68 River Kubena, (Ustye village) Lake Kubenskoye Ust-Kubinsky Ust-Kubinsky, Vologdsky 3, 5, 7, 12, 15, 18, 30, 31 3, 5, 7, 9, 12, 13, 15, 16, 18, 24, 29, 30, 31, 32 8 14 125 656

69 Lake Dmitrovskoye Vologdsky 15, 18, 30, 31 4 88

70 Lake Koskovskoye Vologdsky 9, 15, 18, 31 4 79

71 River Ema Vologdsky 5, 10, 13, 15, 30, 31 6 25

72 73 Siberian Pond (Vologda) River Vologda Vologdsky Vologdsky 34 3, 7, 12, 15, 18, 30, 31, 32 1 8 15 166

74 pond on R.Sinichka Gryazovetsky 34 1 15

75 River Nurma Gryazovetsky 31 1 10

76 River Lezha Gryazovetsky 5, 15, 31 3 65

77 ponds (Sokol town) Sokolsky 15, 18, 31 3 5

78 Lake Ozerko Sokolsky 9 1 18

79 80 81 River Sukhona (Sokol town) River Sukhona (Shuiskoye village) River Sukhona (Kozhukhovo village) Sokolsky Mezhdure-chensky Mezhdure-chensky 3, 7, 12, 15, 18, 31 3, 6, 7, 12, 15, 18, 30, 31 1, 3, 4, 7, 11, 12, 15, 18, 31, 32 6 8 10 46 110 106

82 River Votcha Sokolsky 25 1 31

83 River Kiyug Syamzhensky 13, 25 2 12

84 River Kostyuga Verkhovazhsky 25 1 25

85 River Vaga Verkhovazhsky 13, 15, 25 3 21

86 Lake Glubokoye Totemsky 3, 12, 15, 18, 31 5 28

87 River Sukhona (Yubileiny settlement) Totemsky 3, 7, 12, 15, 31 5 25

88 River Tiksna Totemsky 13, 25 2 17

89 River Vopra Totemsky 13 1 10

90 River Tsareva Totemsky 13 1 11

No. Water body Municipal district Fish species Number of species Number of specimens

91 River Sukhona (Ustye village) Totemsky 1, 3, 4, 7, 11, 12, 15, 30, 31 9 39

92 River Pechen'zhitsa Totemsky 13 1 20

93 River Sukhona (Tot'ma town) Totemsky 1, 3, 4, 7, 12, 13, 15, 18, 29, 31 10 121

94 River Eden'ga Totemsky 12, 13, 25 3 72

95 River Noren'ga Totemsky 13 1 10

96 River Leden'ga Babushkinsky 13 1 10

97 River Sukhona (Kochen'ga village) Totemsky 3, 4, 7, 12, 15, 31 6 35

98 River Sheben'ga River Sukhona Tarnogsky 25 1 15

99 (Nyuksenitsa village) Nyuksensky 1, 4, 15, 30, 31 5 38

100 River Sukhona (Vostroye village) Nyuksensky 4, 7, 11, 12, 15, 18, 30, 31, 32 9 58

101 River Sukhona (Poldarsa village) Velikoustyugsky 1 1 31

102 River Sukhona (Veliky Ustyug) Velikoustyugsky 4, 11, 12, 13, 15, 31 6 16

103 Lake Babye Babushkinsky 31 1 8

104 River Yurmanga Babushkinsky 25 1 5

105 River Yuza Babushkinsky 13 1 17

106 River Unzha Nikolsky 5, 13, 31 3 20

107 River Lundonga Nikolsky 12, 13, 15, 25, 31 5 47

108 River Bolshoy Karnysh Nikolsky 13, 15 2 20

109 River Pyrnug Nikolsky 25 1 10

110 River Zemtsovka Nikolsky 25 1 50

111 River Yug Nikolsky 31 1 6

112 River Yeontala Kichmengsko-Gorodetsky 25 1 26

dose = 0.0016 ^g/g body weight per week7; the average weight of an adult = 70 kg; the average weight of children of a secondary school age (11-15 years) = 42 kg, of a primary school age (6-10 years) = 26 kg, a preschool age (2-5 years) = 16 kg 8.

MAC of mercury in fish at a given level of consumption (number of servings per week) is calculated using the formula6:

gy _ RfD x BW

edition, 2000. EPA, Washington, DC, USA.

7 Committee on toxicity of chemicals in food consumer products and the environment. Updated COT statement on a survey of mercury in fish and shellfish, 2003.

8 WHO. Weight-for-age (5-10 years), 2007. Web page. URL: https://www.who.int/tools/growth-reference-data-for-5to19-years/ indicators/weight-for-age-5to10-years (accessed: 10.09.2023).

where SV is MAC of mercury in fish at a given level of consumption (jg/g); RfD is the permissible weekly intake of mercury; BW is a man weight, g; CR - a weekly fish consumption (g/week); the EPA reference dose = 0.0007 ^g/g body weight per week. Weekly fish consumption was calculated taking into account a serving weight for a certain age group of the population (for adults - 150 g; for children of 11-15 year old - 110 g, for 6-10 year old - 90 g and 2-5 year old children - 70 g9) and the number of servings per week (1, 2 and 3 pieces).

Results and discussion

The mercury content in muscles of fish from Vologda water bodies varied widely: from 0.001 jg/g wet weight in muscles of roach, silver bream and dace to 2.492 in perch. The minimum average metal concentrations were recorded in rainbow trout and European smelt, whereas the maximum ones - in asp and smelt (Fig.2). In some specimens of rainbow trout and smelt, maximum mercury concentrations reached 0.1 ^g/g; in tench, whitefish, Amur sleeper, grayling, crucian carp they varied as 0.2-0.4^g/g; in sterlet, bleak, vendace, Volga zander, whitefish, gudgeon, rudd, char - from 0.4 to 0.6 ^g/g; blue bream, dace, chub, burbot, ide, salmon and kilets - from 0.6 to 0.8 jg/g; white-eye, sabrefish and smelt - from 0.8 to 1.0 jg/g. Maximum concentrations exceeded 1.0 |jg/g in bream, roach, silver bream, pikeperch, ruff and asp, 1.5 jg/g excess was in pike and 2.0 jg/g - in perch. The average mercury concentrations in muscles of fish from the water bodies of Vologda Oblast were comparable to those in fish from freshwater bodies and watercourses of Russia and the world (Allen-Gil et al., 1997; Arantes et al., 2016; Kalkan et al., 2015; Komov et al., 2014; Li et al., 2015; Milanov et al., 2016; Nemova et al., 2014; Pal and Ghosh, 2013; Siraj et al., 2016). Thus, according to the European Food Safety Authority, freshwater fish species accumulate on average the following concentrations of mercury: roach - 0.12, perch - 0.17, bream - 0.23, and pike - 0.39 jg/g wet weight (Cottrill et al., 2012). Our findings suggest that this indicator for roach caught in Vologda water bodies makes up 0.18, perch - 0.33, bream - 0.13, and pike- 0.38 jg/g.

Fig. 2. Mercury content (jg/g, wet weight) in muscles of different fish species from water bodies of Vologda Oblast.

9 SanPiN 2.3/2.4.3590-20. Sanitary and epidemiological requirements for the organization of public catering for the population.

Trophic specialization is one of the crucial factors determining the mercury content in muscle tissues of fish. Mercury concentrations increase in organs and tissues exponentially with each higher trophic level that is a peculiar feature of this metal migration in the food chain (Bloom, 1992). Hence, the mercury levels in predatory fish can exceed the background concentrations by hundreds of thousands or even millions of times (Croteau et al., 2005).

By feeding habits, Vologda fish can be split in two large groups: peaceful and predatory. Predatory, or ichthyophagous, feed mostly on other fish species; in the early stages of development, their main food is large invertebrates, especially insect larvae. Among the studied fish species, this group includes perch, pike, pikeperch, asp, burbot, salmon, and Volga zander. The second, more numerous group consists of peaceful species. Depending on the predominant feeding component, they are divided into planktivores, benthophages, phytobenthophages, euryphages and species of a mixed feeding type (Slynko and Tereshchenko, 2014). Planktivores (zope, bleak, vendace and smelt) primarily feed on zooplankton, benthophages (white-eye, bream, dace, sterlet, ruff, whitefish) consume benthic organisms, while phytobenthophages (roach, rudd, silver bream, crucian carp, tench) - mainly benthos and plants. Euryphages (ide, grayling, chub, Amur sleeper), which along with various groups of benthic invertebrates also consume fish in large quantities, are distinguished by the greatest diet diversity. A similar position is occupied by planktoichthyophages; adults often feed on juvenile fish (Siberian fish) and are capable of forming ecological groups with a predatory type of feeding (smelt and kilets).

Significant differences in the mercury content were established when comparing trophic groups of fish. The least concentrations (0.025 ± 0.002 ^g/g) were recorded in rainbow trout kept in cages and fed with specialized high-calorie artificial food. No significant differences were noted between ichthy-ophages and planktoichthyophages, as well as benthophages and phytobenthophages, which have similar feeding spectrum. The highest mercury concentrations were observed in planktoichthyophages (0.271 ± 0.009 ^g/g) and predators (0.304 ± 0.004 ^g/g) (Table 2). Thus, predatory fish, as the largest longest-lived and occupying a high position in the food chain, contain more mercury and pose the greatest human health hazard.

Table 2. Mercury content (|jg/g ,wet weight) in fish muscles of different trophic groups from water bodies of Vologda Oblast. N -the sample size, AM - the arithmetic mean, SE - the arithmetic mean error, Min - the minimum concentration, Max - maximum concentration; letters indicate statistically significant differences between mercury concentrations in muscle tissue of fish of different trophic groups (H-test) at a significance level of p < 0.05 (Kruskal-Wallis test).

No. Trophic group Fish species N AM Hg, |ig/g SE Min Max H-test

1 Artificial food rainbow trout 13 0.025 0.002 0.010 0.036 a

2 Planktivores vendace, zope, bleak, smelt 650 0.150 0.003 0.027 0.638 b

3 Benthophages whitefish, ruff, bream, dace, white-eye, sterlet, whitefish-nelma, gudgeon 2434 0.168 0.003 0.001 1.184 c

4 Phytobentho-phages silver bream, golden crucian carp, silver crucian carp, rudd, tench, roach 2564 0.172 0.003 0.001 1.184 c

5 Euryphages ide, grayling, Amur sleeper, chub 626 0.188 0.005 0.002 0.749 d

6 Planktoichthyophages saberfish, smelt, kilets 336 0.271 0.009 0.045 0.992 e

7 Ichthyophages pike, pikeperch, Volga zander, salmon, asp, burbot, perch, char 4097 0.302 0.004 0.003 2.492 e

Table 3. Size-age dependence of mercury content in fish muscles. N - the sample size, Rs - the Spearman's rank correlation coefficient. A significant correlation (Rs > 0.3 at p < 0.05) between the mercury content in muscles and size/age of fish is shown in bold.

Species

N

mercury/age of fish Rs P

mercury/mass of fish Rs p

mercury/length of fish Rs p

Rainbow trout 13 - - 0.283 0.347 0.072 0.813

Smelt 30 - - 0.412 0.023 0.388 0.033

Crucian carp (gold and silver) 171 0.491 0.000 0.035 0.646 0.032 0.674

Whitefish 69 0.425 0.000 0.134 0.270 0.202 0.094

Amur sleeper 34 0.171 0.332 0.323 0.062 0.198 0.261

Grayling 214 0.396 0.000 0.288 0.000 0.345 0.000

Rudd 169 0.173 0.032 0.003 0.959 0.001 0.985

Bream 1305 0.358 0.000 0.347 0.000 0.351 0.000

Sterlet 297 0.371 0.000 0.292 0.000 0.278 0.000

Tench 33 0.107 0.572 0.106 0.554 0.122 0.498

Volga zander 150 0.043 0.625 0.148 0.069 0.156 0.055

Zope 318 0.566 0.000 0.380 0.000 0.418 0.000

Vendace 164 0.211 0.089 0.520 0.000 0.427 0.000

Roach 1554 0.255 0.000 0.117 0.000 0.197 0.000

White-eye 135 0.219 0.010 0.162 0.052 0.183 0.032

Bleak 138 0.277 0.006 0.135 0.112 0.050 0.555

Dace 322 0.547 0.000 0.473 0.000 0.480 0.000

Chub 16 0.482 0.006 0.800 0.000 0.803 0.000

Silver bream 637 0.326 0.000 0.361 0.000 0.398 0.000

Sabrefish 220 0.283 0.000 0.329 0.000 0.406 0.000

Zander 721 0.434 0.000 0.473 0.000 0.478 0.000

Ruff 258 0.404 0.000 0.132 0.033 0.139 0.524

Gudgeon 14 0.442 0.017 0.654 0.028 0.646 0.031

Whitefish 34 0.126 0.308 0.153 0.384 0.024 0.891

Burbot 231 0.530 0.000 0.472 0.000 0.479 0.000

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Ide 362 0.407 0.000 0.429 0.000 0.447 0.000

Perch 2339 0.576 0.000 0.564 0.000 0.587 0.000

Salmon 21 0.174 0.430 0.266 0.149 0.256 0.338

Char 15 0.130 0.641 0.242 0.383 0.403 0.135

Pike 543 0.504 0.000 0.461 0.000 0.476 0.000

Smelt 99 0.481 0.013 0.451 0.000 0.477 0.000

Asp 77 0.872 0.000 0.772 0.000 0.822 0.000

Kilets 17 0.445 0.007 0.385 0.030 0.637 0.005

Age and life expectancy also affect mercury levels in fish. Mercury concentrations in organs and tissues are generally higher in long- than in short-lived species. They are higher in slow-growing than in fast-growing species, as well as in larger and older fish than in young ones (Ivanova et al., 2023; Soltani et al., 2021; Sonesten, 2003; Stepanova and Komov, 1997). The reliable correlations between the mercury content in muscle tissue and age were established for 19 studied species, while with body length for 18 and with body weight - for 17 species (Table 3). A significant positive relationship between mercury content and age was noted for crucian carp, whitefish, grayling, bream, sterlet, blue bream, dace, chub, silver bream, pikeperch, ruff, gudgeon, burbot, ide, perch, pike, smelt, carp, and asp. The best correlation was found for ichthyophages. Thus, the Spearman's rank correlation coefficient (Rs) between mercury concentrations and size-age indicators (age, weight, length) for pikeperch was 0.4340.478, pike - 0.461-0.504, burbot - 0.472-0.530, perch - 0.564-0.587, asp - 0.722-0.872. At the same time, in most peaceful species (rudd, tench, roach, vendace, white-eye, bleak) and euryphages (Amur sleeper, sabrefish) such a correlation was absent or weakly expressed.

The comparison of mercury concentrations in fish muscles with those established by the RF hygienic rules and regulations for food products safety indicated that mercury concentrations exceeded MAC (< 0.6 ig/g) in 4.5% of predatory fish species from water bodies of Vologda Oblast. Most often high concentrations were found in kilets (29.4%), asp (20.8%), pike (12.9%) and perch (11.9%), not so often - in smelt, char, chub, ruff, salmon, white bream, sabrefish, pikeperch and sporadically - in ide, burbot, dace, roach, white-eye and bream (Table 4) had mercury concentrations corresponding to the recommended levels for non-predatory freshwater fish (0.3 ig/g). Only three species (rainbow trout, smelt, tench) demonstrated the recommended metal content (within 0.3 |jg/g). In 3% of whitefish, sterlet, grayling, Amur sleeper and in 10% of rudd, Volga zander, vendace, bream, blue bream, gudgeon, and white-eye this indicator was above 0.3 jg/g. In other peaceful fish species (i.e. bleak, roach, bream, sabrefish, silver bream), the proportion of specimens with a high mercury content was 10-20%, and in whitefish, ruff, chub and ide it even exceeded 20%. In general, MAC excess was revealed in 12.1% of specimens of peaceful species and in 9.5% of predatory ones.

Maximum permissible concentrations for food products reflect just average statistical values being often ineffective in assessing the risks to public health associated with alimentary intake of toxic elements and their compounds in food. Therefore, when calculating and making recommendations, it is better to use the criterion of a safe dose of mercury intake in the human body, or RfD (a reference dose), which takes into account the coefficients of absorption and excretion of mercury in the body, the amount of mercury intake with the minimal negative effect on health 10.

The FAO Joint Expert Committee, which assesses contaminants in food, has established a safe weekly intake of methylmercury at 0.0016 ig/g body weight per week. The most stringent guidelines have been currently set by EPA: a safe daily dose is 0.0007 ig/g body weight per week. WHO recommendations are aimed at preserving the adults health, while US regulations (EPA) - to prevent the negative effects of mercury on the nervous system of a developing fetus (Bell, 2017; Grandjean and Budtz-J0rgensen, 2007).

With allowance for the EPA recommendations, the safe permissible weekly consumption of rainbow trout (artificially grown in the reservoirs of Vologda Oblast) for adults is about 2000 g per week, for children of a secondary school age - 1200 g, a primary school age - 700 g and a preschool age - almost 500 g. Wild fish eating is less safe. Depending on a fish type, it varies within 104-740 g for adults, 62-444 g for children of a secondary and 39-275 g of a primary as well as 24-169 g for preschool children. According to FAO recommendations, the calculated levels of safe weekly consumption of fish from Vologda water bodies are almost 2.3 times higher, amounting to 237-1692 g per week for adults, 142-1015 g for children of 11-15 years, 88-628 g of 6-10 year olds and 54-387 g for 2-5 year old children (Table 5).

Based on the calculated number of servings per week of fish with different mercury levels (not

10 UNEP. Executive summary of the document on guidance for identifying populations at risk from mercury exposure. Chiba, Japan, 24-28 January 2011.

Table 4. The ratio of mercury content in peaceful and predatory fish of water bodies of the Vologda region with sanitary and hygienic standards of the Russian Federation.

Fish species N Number of individuals with Hg content < 0.299 |jg/g Number of individuals with Hg content = 0.3-0.599 jg/g Number of individuals with Hg content > 0.6 jg/g

ind. % ind. % ind. %

Artificial feed

Rainbow trout 13 13 100.0 0 0.0 0 0.0

Peaceful views

Smelt 30 30 100.0 0 0.0 0 0.0

Tench 33 33 100.0 0 0.0 0 0.0

Whitefish 69 68 98.6 1 1.4 0 0.0

Grayling 214 210 98.1 4 1.9 0 0.0

Sterlet 297 291 98.0 6 2.0 0 0.0

Crucian carp 171 167 97.7 4 2.3 0 0.0

Rotan 34 33 97.1 1 2.9 0 0.0

Rudd 169 162 95.9 7 4.1 0 0.0

Vendace 164 155 94.5 9 5.5 0 0.0

Bream 1305 1215 93.1 81 6.2 9 0.7

Sinets 318 296 93.1 20 6.3 2 0.6

Gudgeon 14 13 92.9 1 7.1 0 0.0

White-eye 135 122 90.4 12 8.9 1 0.7

Bleak 138 124 89.9 14 10.1 0 0.0

Roach 1554 1367 88.0 168 10.8 19 1.2

Dace 322 277 86.0 40 12.4 5 1.6

Chekhon 220 189 85.9 26 11.8 5 2.3

Gustera 637 534 83.8 84 13.2 19 3.0

Whitefish 34 25 73.5 9 26.5 0 0.0

Ruff 258 195 75.6 50 19.4 13 5.0

Chub 16 12 75.0 3 18.8 1 6.3

Ide 362 258 71.3 98 27.1 6 1.7

Smelt 99 30 30.3 62 62.6 7 7.1

Kilets 17 3 17.6 9 52.9 5 29.4

Total 6610 5809 87.9 709 10.7 92 1.4

Predatory species

Bersh 150 143 95.3 7 4.7 0 0.0

Zander 721 608 84.3 95 13.2 18 2.5

Burbot 231 187 81.0 41 17.7 3 1.3

Salmon 21 12 57.1 8 38.1 1 4.8

Perch 2339 1329 56.8 731 31.3 279 11.9

Pike 543 234 43.1 239 44.0 70 12.9

Asp 77 32 41.6 29 37.7 16 20.8

Palia 15 4 26.7 10 66.7 1 6.7

Total 4097 2549 62.2 1160 28.3 388 9.5

TOTAL 10720 8371 78.1 1869 17.4 480 4.5

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Table 5. Consumptive safety offish from water bodies of Vologda Oblast, g/week.

Fish species N Average mercury content in fish, |jg/g Children of 2-5 years old EPA FAO Children of 6-10 years old EPA FAO Children of 11-15 years old EPA FAO EPA Adults FAO

Rainbow trout 13 0.025 455 1040 739 1690 1194 2730 1991 4550

Smelt 30 0.066 169 387 275 628 444 1015 740 1692

Carp 171 0.083 135 309 220 502 355 811 592 1352

Common whitefish 69 0.085 131 300 213 488 345 788 575 1313

Amur sleeper 34 0.092 122 280 199 455 321 734 536 1224

Grayling 214 0.122 92 209 149 340 240 549 401 915

Rudd 169 0.124 90 206 147 335 237 541 395 902

Bream 1305 0.130 86 197 140 320 226 517 377 861

Sterlet 297 0.136 82 187 133 304 215 491 358 819

Tench 33 0.141 80 182 129 296 209 478 349 797

Volga zander 150 0.152 73 167 119 272 192 439 320 732

Zope 318 0.168 67 152 108 248 175 400 292 667

Vendace 164 0.174 64 147 105 239 169 386 282 644

Roach 1554 0.177 64 145 103 236 167 382 278 636

White-eye 135 0.178 63 144 102 234 165 378 275 629

Bleak 138 0.181 62 141 100 229 162 370 270 617

Dace 322 0.189 59 135 96 220 155 355 259 591

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Fish species N Average mercury content in fish, |jg/g Children of 2-5 years old EPA FAO Children of 6-10 years old EPA FAO Children of 11-15 years old EPA FAO Adults EPA FAO

Chub 16 0.192 58 134 95 217 153 351 256 585

Silver bream 637 0.198 56 129 92 210 148 339 247 565

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Sabrefish 220 0.202 56 127 90 206 146 334 243 556

Zander 721 0.203 55 126 90 205 145 331 242 552

Ruff 258 0.213 53 120 85 195 138 315 230 526

Gudgeon 14 0.217 52 118 84 192 135 309 226 516

Whitefish 34 0.218 51 117 84 191 135 308 225 514

Burbot 231 0.226 49 113 80 184 130 297 217 495

Ide 362 0.236 47 108 77 176 125 285 208 474

Salmon 21 0.308 36 83 59 135 95 218 159 363

Perch 2339 0.331 34 78 55 127 90 205 149 341

Char 15 0.344 33 74 53 121 86 195 143 326

Pike 543 0.378 30 68 48 110 78 178 130 296

Smelt 99 0.392 29 65 46 106 75 171 125 286

Asp 77 0.401 28 64 45 104 73 167 122 279

Kilets 17 0.472 24 54 39 88 62 142 104 237

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rainbow trout snetok amur sleeper whitefish crucian carp rudd grayling sterlet bream tench volga zander white-eye roach zope silver bream dace bleak pike perch chub gudgeon saberfish vendace ruff

nelmushka ide burbot perch asp pike salmon smelt kllets lake char

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rainbow trout snetok amur sleeper white fish crucian carp rudd grayling sterlet bream tench volga zander white-eye roach

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Can consume up to three servings per week Can consume up to two servings per week Can consume up to one serving per week ■ Exclude from use

Fig. 3. The ratio of different categories of weekly fish consumption by certain age groups of the population: A -preschool children (2-5 years), a serving is 70 g; B -primary school children (6-10 years) - 90 g; C - secondary school children (11-15 years) -110 g, D -adults - 150 g.

Table 6. MAC of mercury in fish (|jg/g, wet weight) for different age groups with regard for recommended servings per week.

Age group

Consumption level Children of 2-5 years Children of 6-10 years Children of 11-15 years Adults

up to 3 servings per week < 0.05 < 0.07 < 0.09 < 0.11

up to 2 servings per week < 0.08 < 0.10 < 0.14 < 0.16

no more than 1 serving per week < 0.17 < 0.21 < 0.28 < 0.33

to exclude from diet > 0.17 > 0.21 > 0.28 > 0.33

exceeding EPA RfD standards), fish from local reservoirs was categorized in 4 groups: "can be consumed up to 3 servings per week", "up to 2 servings per week", "no more than 1 serving per week", "must be excluded from a diet" (Table 6).

A comparison of our results with EPA recommendations (Table 6) shows that at a mercury content of > 0.33 jg/g in Vologda fish, the adult population should completely exclude fish from the diet or eat no more than one serving per week (0.16-0.33 |jg/g or 18 and 34%). For children of different age, these indicators are the following: for 2-5 years - 50 and 34%, for 6-10 years - 37 and 38%, for 11-15 years -24 and 35%, respectively.

A comparison of fish species suggests that 20-40% of perch, salmon and ide, 40-60% of pike and asp, and 60-80% of kilets, char and smelt contain hazardous mercury concentrations to adult health (Fig. 3). Dangerous for preschool children mercury content was detected in 60-80% of pike, asp, perch, burbot, ide, whitefish and in 40-60% of pikeperch, bleak, dace, silver bream, blue bream and roach. In this regard, the local population should limit a regular consumption of these types of fish. Kilets, char, salmon and smelt must be completely excluded from the diet of preschoolers. Eating of rainbow trout and smelt is the safest for all categories of the population.

Conclusion

Mercury concentrations in fish from water bodies of Vologda Oblast varied widely. For instance, the range between the minimum and maximum values made up three orders of magnitude. The lowest concentrations (0.001 ig/g wet weight) were found in muscles of roach, silver bream and dace, whereas the highest (> 1.5 ig/g) - in pike and perch. The maximum average concentrations were noted in typical predatory species (pike, perch, asp, salmon, char) and predatory forms (kilets, smelt) of peaceful species. Rainbow trout (grown in cage farms on artificial feed) and smelt, a typical planktivore, had the least average concentrations of mercury. It is known that mercury accumulation in fish muscles depends on the trophic specialization of individual species, fish age and size. Being the largest long-lived and occupying top levels in the food chain, predatory fish contain more mercury, and thereby at regular consumption in food they are most dangerous to human health.

An important point is that estimation results of a consumptive safety of fish depend on the applied calculation method based on either a safe dose of mercury intake in the human body for a certain time or a safe mercury concentration in fish. The excess in MAC of mercury in muscles has been revealed in 9.5% of the studied predatory and in 12.1% of peaceful fish caught in different reservoirs of Vologda Oblast. In terms of a safe dose of mercury intake in the human body, the amount of unsafe fish consumed by adults in the region under study is 1.5 times (23%) greater of the RF standards for mercury. For adults, it is recommended to exclude up to 18% of fish from the diet, for children of a secondary school age - up to 24%, for primary school - 37% and preschool age children - almost 50%.

Thus, the federal rationing system is relevant only for limiting the peaceful fish consumed by adults. The standards adopted in the Russian Federation do not actually limit the consumption of fish harmful to the health of children.

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