Content uploaded by Maksim I. Shapovalov
Author content
All content in this area was uploaded by Maksim I. Shapovalov on Dec 13, 2021
Content may be subject to copyright.
Content uploaded by Maksim I. Shapovalov
Author content
All content in this area was uploaded by Maksim I. Shapovalov on Dec 13, 2021
Content may be subject to copyright.
Available via license: CC BY 4.0
Content may be subject to copyright.
766
ISSN 1995-0829, Inland Water Biology, 2021, Vol. 14, No. 6, pp. 766–776. © The Author(s), 2021. This article is an open access publication.
Russian Text © The Author(s), 2021, published in Biologiya Vnutrennykh Vod, 2021, No. 6, pp. 628–639.
Effects of Polymetallic Ore Occurrences on Mercury Accumulation
by Aquatic Biota in River Ecosystems
M. I. Shapovalova, *, V. A. Gremyachikhb, and V. T. Komovb
a Adyghe State University, Maykop, Russia
b Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences,
Borok Nekouzskii raion, Yaroslavl oblast, Russia
*e-mail: shapmaksim2017@yandex.ru
Received April 20, 2020; revised January 13, 2021; accepted January 28, 2021
Abstract—The study represents the data on metal content in the body of stoneflies Perla pallida Guerin-Men-
eville, 1838 (Plecoptera, Perlidae) and in muscles of the fish family Cyprinidae from the small tributaries of
the Belaya River (Republic of Adygea, Northwest Caucasus) with ore mineralization of various metals includ-
ing mercury. It was found that mercury (Hg) concentrations in stoneflies are corresponds to from the water
basins without local Hg sources. Mercury content in stoneflies depends on season and is more intensive in
early ontogenesis in winter than in the warm season. Mercury concentration in 0.01–0.72 mg/kg dry weight
can cause the pathomorphological changes in the structure of organs and decrease the adaptive potential in
competitive population of stoneflies, in general. The Hg concentration reached 0.09–0.69 mg/kg in the stud-
ied fish species (bleak, gudgeons, and barbels) and was similar to concentrations in stonefly larvae. This can
be related with low size-weight parameters of fishes in samples as wells as with similar feeding patterns of hyd-
robionts.
Keywords: mercury, aquatic biota, river ecosystems, ore occurrences in catchment areas
DOI: 10.1134/S199508292105014X
INTRODUCTION
The global emission of Hg from natural and
anthropogenic sources into the atmosphere, followed
by the migration and deposition to the surface of
aquatic and terrestrial ecosystems, is still the main rea-
son for the increase in its content and negative impact
on biota (Kolka et al., 2011; Eagles-Smith et al., 2016).
Various compounds of this metal, including the most
toxic and bioavailable methylated mercury, form
strong chemical bonds with compounds that make up
the tissues of living organisms and accumulate in con-
centrations hazardous to human health. It has been
experimentally revealed that, in vertebrates, high lev-
els of Hg in tissues lead to chromosomal aberrations
and blood pathologies and negatively affect the ner-
vous system and embryonic development of the fetus
(Topashka-Ancheva et al., 2003; Schеuhammer, 2007;
Tavshunsky et al., 2017). In invertebrates, this relates
to deformations of vital structures, the deceleration of
larval growth, and processes of metamorphosis and
regeneration of damaged organs (Medvedev and
Komov, 2005; Gremyachikh et al., 2006; Jensen et al.,
2007).
Studies of the dependence of the accumulation of
Hg by living organisms on the parameters of the envi-
ronment have been and are still carried out mainly in
aquatic and near-aquatic ecosystems, where the activ-
ity of bacterial methylation is high, contributing to the
inclusion of mercury in food webs (Gilmour et al.,
2013; Tavshunsky et al., 2017). Elevated concentra-
tions of Hg in the muscles of fish from rivers and lakes
in Russia were recorded both when metal was origi-
nated from industrial wastewater (Leonova et al.,
2006) and in the absence of local sources in the catch-
ment area, for example, in acidic (water pH < 5.0)
lakes in the northwest of Russia (Haines et al., 1992,
1995; Stepanova and Komov, 1997). The most signif-
icant concentrations of Hg in the lithosphere are
found the regions of its deposits and ore occurrences,
although they contain only 0.02% of all mercury (Sau-
kov, 1975). The bulk of Hg is in the form of com-
pounds in mercury minerals and as isomorphic or
mechanical impurities in other minerals and often
accompanies metals of the platinum group. Therefore,
in the presence of polymetallic and especially mercury
ores in the catchment area, the probability of Hg in the
trophic webs of aquatic ecosystems increases.
In the foothill regions of the North Caucasus, in
the Belaya River basin, several ore fields with isolated
points of ore occurrences of tungsten, polymetallic
ores, gold ore and placer gold, mercury, and manga-
nese have been identified (Volkodav, 2012). However,
AQUATIC
TOXICOLOGY
INLAND WATER BIOLOGY Vol. 14 No. 6 2021
EFFECTS OF POLYMETALLIC ORE OCCURRENCES ON MERCURY ACCUMULATION 767
studies on the content of mercury in aquatic ecosys-
tems of this region have never been carried out.
The goal of the present paper is to investigate the
effect of polymetallic ore outcrops found in the Belaya
River catchment area on Hg accumulation in repre-
sentatives of amphibiotic invertebrates (Plecoptera
larvae) and fish.
MATERIALS AND METHODS
The Belaya River is the second longest and the
most powerful in terms of the discharge volume of the
left-bank tributary of the Kuban River, located on the
border of the western and northwestern parts of the
Greater Caucasus in the foothill region of the Repub-
lic of Adygea. It originates on the slopes of the Fisht-
Oshten mountain range and flows into the Krasnodar
Reservoir. The river is 277 km in length and the catch-
ment area is 5990 km2 (Mel’nikova and Komlev,
2003).
The river basin is a system within which natural,
inhabited territories, and agricultural lands interact.
The most important components of the natural land-
scape complexes of the Belaya River basin are small
streams which were studied at ten sampling stations
(Fig. 1, Table 1).
In the Belaya River basin, the occurrence of ore
mineralization of various metals, including Hg, is
concentrated. The Khamyshinskoye (Shakhanskoye)
mineralization field occupies most of the interfluve of
the Bzykha and Khamyshinka rivers and the left trib-
utaries of the Belaya River (sampling stations 1–3)
(Volkodav, 2012). Of the five isolated ore occurrences,
the highest Hg content was noted in the Shahanskoye
(0.012% –0.2%). Here, in the transverse vertical
cracks, in the veins of other minerals, cinnabar is
found in the form of inclusions and deposits, which is
often accompanied by native mercury. The Hg content
in other ore occurrences usually does not exceed hun-
dredths of a percent.
The Belorechenskoye ore field is located in the
Syuk River valley (sampling station 4), which flows
into the Belaya River (sampling station 5) downstream
the settlement of Nikel’. The leading ore-forming
minerals of the Belorechenskoye barite ore filed are
barite, quartz, calcite, and ankerite, while cinnabar is
a rare mineral. Mercury mineralization is also con-
Fig. 1. Locations of sampling stations in the tributaries to the Belaya River (numbering from the river head to mouth): (1) Lipo-
vaya River; (2) Khamyshinka River; (3) Bzykha River; (4) Syuk River; (5) Belaya River, near the settlement of Nikel’; (6) Dakh
River, downstream of a bridge; (7) Mishoko River; (8) Maykopskaya River; (9) Shuntuk River; and (10) Kurdzhips River, near
the settlement of Krasnyi Most.
N
46
45
44
37 38 39 40 41 E
SEA OF AZOV
BLACK SEA
1
2
3
4
5
6
7
8
9
10
Tabl e 1. Hydrographic characteristics of small rivers inf low-
ing the Belaya River
A dash indicates no data.
River Sampling
station
River
channel
length, km
Height above
sea level
(head/mouth)
Lipovaya 1 8 1340/560
Khamyshinka 2 7 1330/550
Bzykha 3 11 1710/530
Syuk
Belaya
Dakh
4
5
6
14
273
27
990/470
2300/30
–
Mishoko 7 9.4 890/410
Maykopskaya 8 9.5 640/280
Shuntuk 9 12 –/276
Kurdzhips 10 100 2300/224
768
INLAND WATER BIOLOGY Vol. 14 No. 6 2021
SHAPOVALOV et al.
tained in the Triassic strata of the Sakhray River area,
a tributary of the Dakh River (sampling station 6)
(Pekov et al., 2010). The rest of the stations (7–10),
located downstream of the Belaya River, do not have
manifestations of ore mineralization of metals within
their catchment basins.
The studied rivers are typical small watercourses
with rocky bottoms. In the bottom invertebrate com-
munities of the Belaya River and its main tributaries,
238 species of invertebrates have been identified,
87.0% of which are insects. They are dominated by
Caucasian
littoreophilous representatives of zoobenthos: on
biotopes with high water-current velocity, Epeorus–
Simuliidae–Baetis–Blephariceridae; moderate veloc-
ity, Ecdyonurus–Baetis–Rhyacophila–Hydropsich–
Perla-Gammarus; and low velocity, Gammarus–Lime-
philidae (Shapovalov, 2020).
The materials included 326 stonefly larvae Perla
pallida Guerin-Meneville, 1838 (Plecoptera, Perli-
dae), an amphibiotic insect and aquatic organism at
the larval stage. In regards to fish, 35 Kuban spirlin
Alburnoides kubanicus Bănărescu, 1964; 29 minnow
Phoxinus sp.; 9 Caspian gudgeon Gobio cf. holurus
Fowler, 1976; and 3 Kuban barbel Barbus kubanicus
Berg, 1912. Stonefly larvae were sampled in 2012 and
2013 and fish in 2014 and 2015.
The larvae of stoneflies are widespread in all bio-
topes of the Belaya River and its tributaries at height of
no more than 200 m above sea level. They dwell in
cracks on the underside of stones (avoiding a very fast
current) and under large stones, where the layer of
loose pebbles lies. Large species of fam. Perlidae have
a long period of development in a watercourse (up to
3 years) and an active lifestyle. Stoneflies, like the lar-
vae of other insects, may consume detritus of various
origins, mycoflora, unicellular and filamentous algae,
tissues of macrophytes, and mosses, as well as all kinds
of invertebrates (Monakov, 2003). Representatives of
carnivorous stoneflies species, which include Perla
pallida, switch to animal food as they grow, feeding
primarily on dipteran larvae, whose share of the total
number of food components is 68.6–74.3%, and then
on larger organisms: caddisflies larvae and mayflies
(Shapovalov, 2020). The feeding spectra of stonefly
larvae may expand as they grow and develop. Differ-
ences in the composition of food are most often deter-
mined by the composition of the population of the
watercourse in a particular period.
The fish sampled in the tributaries of the Belaya
River are rheophylic cyprinids, whose diet includes
insect larvae to varying degrees (Troitskii and
Tsunikova., 1988; Atlas …, 2003).
The body length and weight of the sampled animals
were measured prior to the processing of samples with
further drying at 36°С (whole insects were used; in
fish, a fragment of dorsal skeletal muscles was dis-
sected). The mercury content was determined in two
or three replicates by the atomic absorption method on
a RA-915+ mercury analyzer with a PIRO (Lumex)
attachment without preliminary sample preparation.
The accuracy of analytical measurement methods was
controlled using DORM-2 and DOLM-2 certified
biological material (Institute of Environmental
Chemistry, Ottawa, Canada).
Data on Hg concentrations are presented as mean
values and their errors (х ± mx) with min–max. Since
the distribution of the data differed from the normal
(Shapiro–Wilk test), the nonparametric Spearman
test was used to identify correlations between the stud-
ied indicators, and the Kruskal–Wallis median was
used to assess the significance of differences between
the samples (the differences are significant at p < 0.05)
(Sokal and Rohlf, 1995).
RESULTS
The body length and weight of stonefly larvae var-
ied widely: length 5.0–32.0 mm and weight 7.0–455.0 mg.
The minimal and maximal concentrations of Hg in the
body of insects reached 0.01 and 0.72, respectively; on
average, over watercourses, it was 0.06–0.38 mg
Hg/kg dry weight (Table 2). The metal content in ani-
mals sampled the closest to the source and located in
the zone of ore occurrences at sampling station 1 was
statistically significantly higher (Fig. 2). The accumu-
lation of Hg by stoneflies at sampling station 2
exceeded that at sampling stations 3–5, 7, and 10; at
sampling station 6, it exceeded that at sampling sta-
tions 4 and 5. For samples from sampling stations 1, 2,
4, 6, and 10, a significant negative relationship
between Hg concentrations in larvae and their body
weight was noted: rs = (–0.56) – (–0.78) at p <0.05;
for samples from sampling stations 2, 4, 6, and 10, it
was also with body length, rs = (–0.55) – (–0.72) at
p< 0.05.
The entire group sample was divided into two sub-
groups: the first included animals from watercourses
located in areas of ore occurrence (sampling stations 1–
6); the second, from watercourses without ore occur-
rence in the catchment (sampling stations 7–10; at
station 9, only fish). The metal concentrations in
stoneflies from the first group were statistically signifi-
cantly higher (Kruskal–Wallis test, H = 21.6, p <
0.000) than from the second: 0.15 ± 0.01 and 0.07 ±
0.004 mg/kg dry weight, respectively. The body length
and body weight of the larvae of the first group were
significantly less than those of the second group:
17.5 ± 0.3 mm and 19.1 ± 0.6 mm (H = 5.9, p <0.02)
and 125.3 ± 6.0 mg and 168.0 ± 13.2 mg (H = 13.9, p<
0.002). With an increase in body length (L), they less
intensively gained body weight (W): in the larvae of the
first group, W = –158.56 + 16.18L and, in the second,
W = –228.52 + 20.75L
In stoneflies from the first group, the same statisti-
cally significant negative relationship between the
INLAND WATER BIOLOGY Vol. 14 No. 6 2021
EFFECTS OF POLYMETALLIC ORE OCCURRENCES ON MERCURY ACCUMULATION 769
Table 2. Content of mercury in stoneflies larvae from the tributaries to the Belaya River
Here and in Table 3: top is the mean and error of mean; bottom is the min–maх, and n is the number of analyzed stonefly larvae; num-
bers of sampling stations are the same as in Fig. 1.
Number of
sampling station Data nBody length,
mm Body weight, mg Hg, mg/kg
dry weight
1April, 2012 25
May 4, 2013 20
Jun e 19, 2013 19
Mean
Total for statio n 1 2012–2013 64
2 May 4, 2013 43
June 19, 2013 28
Mean
Total for statio n 2 2013 71
3May 4, 201311
4June 19, 201339
5 October 2012 33
6 October 2012 32
May 4, 2013 20
Mean
Total for station 6 2012–2013 52
7May 201315
8 May 18, 2013 26
10 July 3, 2013 15
Mean
Total for all sta-
tions 2012–2013 326
±
−
15.9 0.9
9.0 27.5
±
−
96.7 16.3
16.0 325.5
±
−
0.38 0.03
0.17 0.72
±
−
19.4 1.4
10.0 29.8
±
−
166.7 28.3
19.0 403.0
±
−
0.24 0.02
0.14 0.42
±
−
13.5 1.5
7.8 31.2
±
−
84.2 28.2
15.0 455.0
±
−
0.26 0.02
0.12 0.38
±
16.3 0.8
7.8–31.2
±
114.9 14.2
15.0–455.0
±
−
0.31 0.02
0.12 0.72
±
−
21.5 0.6
15.0 32.0
±
−
185.2 14.0
69.0 450.0
±
−
0.11 0.02
0.05 0.55
±
−
18.3 1.0
10.8 29.0
±
−
136.1 19.7
26.0 396.0
±
−
0.15 0.01
0.07 0.22
±
20.3 0.6
10.8–32.0
±
165.8 11.8
26.0–450.0
±
−
0.13 0.01
0.05 0.55
±
−
23.1 1.0
18.0 28.6
±
−
192.4 21.9
97.0 314.0
±
−
0.06 0.006
0.03 0.11
±
−
18.2 0.9
8.0 28.1
±
−
139.5 16.6
17.0 376.0
±
−
0.06 0.003
0.03 0.11
±
−
12.1 0.5
5.0 22.5
±
−
54.5 6.3
7.0 212.0
±
−
0.07 0.006
0.02 0.17
±
−
15.7 0.5
10.0 21.0
±
−
77.2 6.1
19.0 163.0
±
−
0.14 0.005
0.08 0.19
±
−
19.5 1.0
13.0 28.2
±
−
144.0 21.2
42.0 363.0
±
−
0.06 0.006
0.03 0.10
±
17.2 0.5
10.6–28.2
±
102.9 9.9
19.0–363.0
±
−
0.11 0.01
0.03 0.19
±
−
16.5 1.2
8.0 24.0
±
−
136.0 25.5
18.0 368.0
±
−
0.06 0.01
0.01 0.09
±
−
19.9 0.7
13.0 30.5
±
−
179.7 19.6
39.0 451.0
±
−
0.09 0.01
0.02 0.16
±
−
20.3 1.2
12.2 28.0
±
−
179.8 24.8
52.0 330.0
±
−
0.07 0.006
0.04 0.13
±
−
17.8 0.3
5.0 32.0
±
−
132.6 5.5
7.0 455.0
±
−
0.13 0.01
0.01 0.72
770
INLAND WATER BIOLOGY Vol. 14 No. 6 2021
SHAPOVALOV et al.
mercury content and length and weight was revealed:
rs = –0.24, p < 0.05. In stoneflies from the second
group, the decrease in metal concentration with the
growth of animals is also significant, but less pro-
nounced: with length rs = –0.17, p < 0.05, weight rs =
‒0.11, p < 0.05. A seasonal (from spring to autumn)
decrease in the average length and weight of stonefly
larvae (in both cases, rs = –0.38, p < 0.05) was noted
at a relatively stable level. accumulation of Hg. In two
groups of different sizes (in the first, the length of
stoneflies is ≤15 mm and, in the second, >15 mm)
sampled in the tributaries of the mineralization zone,
spring individuals were significantly larger than sum-
mer–autumn ones. In the first group (smaller individ-
uals), the metal content decreased from spring to
autumn and, in the second, it did not change signifi-
cantly (Fig. 4).
The minimal and maximal concentrations of Hg in
the muscles of the studied fish species varied within
0.09–0.69 mg/kg dry weight (Table 3, Fig. 5). The
metal content in the muscles of the minnow is statisti-
cally significantly higher than that of the Kuban
spirlin. The accumulation of mercury by minnows at
sampling stations 1 and 2 did not differ; in the spirlin
at sampling station 9, it was higher than that of fish at
sampling stations 2 and 10. The same concerns the fish
body weight. A significant positive relationship
between Hg concentrations in muscles and fish body
weight was noted for the spirlin: rs = 0.53 at p < 0.05.
The content of metal in the muscles of the spirlin from
the stations located in the ore occurrence zones and
outside them did not differ statistically significantly.
Fig. 2. Mercury content in stonefly larvae at sampling stations located in the ore occurrence zone (sampling stations 1–6) and
outside it (sampling stations 7, 8, and 10).
0.2
0
1032
1
Hg, mg/kg dry weight
Sampling stations
0.6
0.4
0.8
87654
Median
Mean
25–75%
Diapason of values
without outcrops
Outcrops
Fig. 3. Correlation between body length and weight at sam-
pling stations located in the ore occurrence zone (1) and
outside it (2).
2
500
400
300
200
100
0
40302010
0
1
Body weight, mg
Body length, mm
INLAND WATER BIOLOGY Vol. 14 No. 6 2021
EFFECTS OF POLYMETALLIC ORE OCCURRENCES ON MERCURY ACCUMULATION 771
DISCUSSION
The input of Hg from catchment areas with out-
crops of polymetallic ore occurrences into waterbodies
and streams is both of a natural and anthropogenic
nature. In the first case, this is due to natural processes
and, in the second, with the more rapid erosion of
mineralization zones as a result of human economic
activities for the extraction, preliminary processing of
minerals, and storage and disposal of waste dumps at
their enrichment (Kocman et al., 2011; Hsu-Kim
et al., 2018). According to recent estimates, artisanal
and small-scale industrial gold mining may be significant
sources of Hg for freshwater ecosystems (880 t/year),
both industrial production and wastewater emissions
(220 t/year); the mobilization of land resources; and
changes in land use, forestry, and frequency and inten-
sity of wildfires (170–300 t/year) (Obrist et al., 2018).
The Belaya River basin in the upstream reaches is
located in the zone of gold-bearing, copper and lead–
zinc mineralization interspersed with mercury-bear-
ing minerals (in particular, cinnabar and native Hg)
(Volkodav, 2012). The development of the Belaya
River gold placers began in 1932 and continued until
1941, although prospecting works in 1934 and 1935 did
not reveal new placers on the river or industrial miner-
alization (Volkodav, 2012).
The small valleys of the Belaya River Basin were
developed by prospectors at the beginning of the last
century and continue to interest local metal miners to
this day. Any economic activity in the catchment of
rivers (mining of polymetallic ores, deforestation, and
regulation of watercourses) may lead to an increase
in the removal of finely dispersed suspension of mer-
cury mineral cinnabar and the accumulation of mer-
cury in bottom sediments within slowly flowing river
sections (Hsu-Kim et al., 2018).
The metal content in the larvae of stoneflies and
muscles of the studied fish species from the Belaya
River and its tributaries in the zone of ore fields and
outside it is comparable to that revealed in larvae of
amphibiontic insects and fish from waterbodies and
watercourses of various regions lacking local sources
of pollution in the catchment area and predominantly
prone to atmospheric pollution. Thus, the concentra-
tion of total Hg in chironomid larvae from lakes in the
Canadian Arctic varies within 0.09–0.50 mg/kg dry
weight (Ganter et al., 2010). In larvae of dragonflies
from subtropical freshwater Lake Caddo (Texas and
Louisiana, United States), it is 0.17–0.31 (Chumchal
et al., 2011); in Losha River (Vologda oblast), Savala
River (Voronezh oblast), and an artificially dug chan-
nel opening in Rybinsk Reservoir and Sunozhka River
(Yaroslavl oblast), it is 0.02–0.07, 0.0 4–0.15, and
0.01–0.38 mg/kg dry weight, respectively (Gremy-
achikh et al., 2013).
The seasonal decrease in the body length and
weight of larvae of Perla pallida Guerin-Meneville,
1838 is due to the fact that in the spring samples a sig-
Fig. 4. Seasonal changes in Hg content in stonefly larvae ≤15 mm in length (a) and >15 mm (b) sampled in tributaries in the ore
occurrence zone.
(a)
0.8
0.6
0
0.4
0.2
Spring Summer Autumn
Hg, mg/kg dry weight
(b)
0.8
0.6
0
0.4
0.2
Spring Summer Autumn
Hg, mg/kg dry weight
772
INLAND WATER BIOLOGY Vol. 14 No. 6 2021
SHAPOVALOV et al.
nificant part of the animals is represented by large
overwintered specimens (the development cycle in
stoneflies from Adygean watercourses is about 3 years).
Later samples contain individuals hatched in spring
(much less often in summer and autumn) at early
stages of development (Cherchesova and Zhiltsova,
2013). Low concentrations of Hg in summer and
autumn larvae in the small-sized group are associated
with seasonal changes in the composition of food: at a
specific time period, animals choose the most numer-
ous and available food items (Monakov, 2003). In
winter and early spring, it is mainly detritus and bacte-
ria that have developed in and on it; from late spring to
autumn, it is algae and invertebrates. According to
de Wit et al. (2012), the consumption with food of the
bacteria transforming inorganic forms of mercury into
organometallic ones more efficiently than algae
explains the increased metal content in aquatic organ-
isms in the winter–spring period. In addition, over-
wintering larvae do not molt, and each molt during the
growing season is accompanied by rapid growth and,
accordingly, dilution of the accumulated Hg (Ross
et al., 1985). In large larvae of stoneflies, the metal
content does not change significantly with the change
of seasons due to obligate zoophagy: detritus and algae
enter the stomachs of predators from the intestines of
eaten prey (Monakov, 2003).
Fish with both low and increased concentrations of
metal in muscles are found in the rivers and lakes of
nature reserves in European Russia remote from
sources of Hg emissions, which is determined by the
biogeochemical (ecological) characteristics of the
waterbodies and their drainage basins. In perch from
the Usman River (the Voronezhsky Nature Reserve),
a content of 0.35–1.30 mg/kg dry weight was
recorded; in the lakes of the Rdeisky Nature Reserve,
0.20–12.00 (Komov et al., 2009); in Darvinsky
Reserve, 0.10–4.95 (Stepanova and Komov, 1997);
and in Oksky Reserve, 0.10–2.50 mg/kg dry weight
(Gremyachikh et al., 2012).
Unlike stoneflies, the levels of metal in the muscles
of the Kuban spirlin from the Belaya River and its trib-
utaries located closer to the river head in the zone of
ore fields (sampling station 2) and outside it (sampling
stations 7, 8, and 10) are low, but upon approaching
the mouth of the river, these values, on the contrary,
increase. However, this is determined by the small size
of fish caught in the upper reaches: for many species,
a correlation was noted between the size and content
of mercury in the internal organs and muscle tissue
(Komov et al., 2009; Gremyachikh et al., 2012). The
metal content in the muscles of predatory fish from
the Tapajos River (Brazil), one of the main tributaries
of the Amazon, from the mid-1980s, where traditional
gold mining takes place, reaches 20 mg/kg dry matter
(Nevado et al., 2010). With an increase in the distance
from the mining sites downstream of the river, it
decreases, as is observed in the Katun and Selenga riv-
ers with numerous mineralization zones in the catch-
ment area (Vasil’ev and Sukhenko, 1993; Komov
et al., 2014), in which the concentrations of Hg in fish
vary in the range of 0.25–0.55 and 0.24–2.33 mg/kg
dry weight, respectively.
In water, Hg is present in small amounts in a mix-
ture of various forms: mainly suspended and colloidal
particles and, to a lesser extent, a true solution (Han
and Gill, 2005; Hsu-Kim and Sedlak, 2005; Balogh
et al., 2008; Schuster et al., 2008; Dittman et al.,
2010). In a study conducted on the Idrijetsa River
(Slovenia), draining the territory of the former mer-
cury mine, it was found that Hg is in the form of a
finely suspended material, including colloids, and
mercury is transported downstream during short but
extreme hydrometeorological events when the metal is
remobilized from the bottom sediments of the river
(Kocman et al., 2011). During such events, the con-
centrations of Hg in water and bottom sediments rap-
idly decrease and, at the same time, bacterial methyl-
ation of the metal occurs, which increases the propor-
Table 3. Content of mercury in the muscle tissues of fish the
Belaya River tributaries
Number
of sampling station nFish body
weight, g
Нg, mg/kg
dry weight
Kuban spirlin
26
87
96
10 16
Mean
Minnow
114
215
Mean
Gudgeon
95
Kuban barbel
93
±
−
0.11 0.02
0.06 0.17
±
−
0.15 0.005
0.15 0.18
±
−
3.1 0.7
1.6 6.6
±
−
0.26 0.03
0.13 0.34
±
−
5.1 1.1
2.9 8.9
±
−
0.51 0.07
0.26 0.69
±
−
3.2 0.7
0.8 13.4
±
−
0.16 0.01
0.09 0.30
±
−
3.0 0.5
0.06 13.4
±
−
0.24 0.03
0.09 0.69
±
−
0.03 0.007
0.02 0.15
±
−
0.27 0.02
0.16 0.40
±
−
0.11 0.009
0.07 0.18
±
−
0.25 0.01
0.17 0.40
±
−
0.07 0.01
0.02 0.18
±
−
0.26 0.01
0.16 0.40
±
−
1.6 0.7
0.4 4.2
±
−
0.20 0.02
0.12 0.24
±
−
2.0 0.8
0.8 3.6
±
−
0.19 0.02
0.15 0.23
INLAND WATER BIOLOGY Vol. 14 No. 6 2021
EFFECTS OF POLYMETALLIC ORE OCCURRENCES ON MERCURY ACCUMULATION 773
tion of methylmercury (M eHg) in the to tal Hg content
and, consequently, the risk of accumulation in biota
(Ullrich et al., 2007; Kocman et al., 2011; Jackson et
al., 2019).
The bioavailability of Hg for biota depends in a
complex nonlinear manner on a variety of biological
and ecological factors that affect the patterns and
pathways of metal migration along food webs (Lavoie
et al., 2013; Karimi et al., 2016; Polito et al., 2016;
Eagles-Smith et al., 2018; Hsu-Kim et al., 2018). This
is why bottom sediments of waterbodies and soils in
the catchment areas containing relatively high Hg
concentrations with low bioavailability of metal may
be sources of its accumulation in aquatic organisms
only to low levels. For instance, in the muscles of
bream from Lake Serebry located in the immediate
vicinity of the Karabash copper-smelting plant in
Chelyabinsk oblast, Hg concentrations are several
times lower than in the muscles of bream from Lake
Seliger in Tver oblast, in the vicinity of which there is
practically no industry (Tatsii et al., 2017).
Since the second half of the last century, there has
been no active industrial and artisanal mining of gold
or polymetallic ores in the Belaya River basin. This is
why the input of Hg occurs mainly with atmospheric
precipitation and runoff from the river catchment area
as a result of the erosion (leaching) of rocks, as well as
of mountain, floodplain-meadow, and forest soils
(Volkodav, 2012). The specificity of the river hydro-
logical regime (closer to the source, glacial, snow and
storm water supply the sections closer to river headwa-
ters; there is a high water-current velocity) does not
create favorable conditions for the bacterial methyla-
tion of mercury compounds increasing its bioavail-
ability in either the water column or in bottom sedi-
ments. The accumulation of Hg by animals depends
on many environmental factors: the water pH level,
the area of wetlands in the drainage basin, and the
concentration of dissolved organic matter (Harding
et al., 2006). However, the main mechanism for an
increase in the concentration of metal in each subse-
quent link is its trophic transport along the food web
(Eagles-Smith et al., 2018).
The predatory larvae of stoneflies participate in the
transfer of Hg along the food web of aquatic ecosys-
tems as secondary and tertiary consumers, which are
at the same trophic level with some fish and at the
same time are a food object for omnivorous and pred-
atory fish species. In the bottom fauna of mountain
streams, amphibiontic insects are one of the most
abundant and widespread groups of invertebrates.
Potential food items for predatory stonefly larvae are
>40% of the species composition of benthic inverte-
brates in the studied rivers (Shapovalov, 2011, 2020).
By consuming large insect larvae (in a specific case,
dragonflies), fish in the watercourse limit the Hg f lux
into the terrestrial ecosystem, but do not affect the
mercury flux passing through the small larvae of chi-
ronomids and caddis flies (Tweedy et al., 2013).
The present study revealed that concentrations of
Hg in larvae of stoneflies and muscles of fish from the
small streams of Adygea are low and comparable to
each other: 0.01–0.72 and 0.09–0.69 mg/kg dry
weight, respectively, which may be associated with the
low size and mass parameters of fish in the samples
and, as a result, the similarity of the food spectra of the
aquatic organisms under study. As food items, the lar-
vae of stoneflies (and also adults, even taking into
account the possible increase in metal concentration
as a result of metamorphosis), accumulating Hg
within the established values, cannot significantly
harm the predatory representatives of the aquatic,
near-water, and terrestrial ecosystems in the Belaya
River basin.
As was shown on the chironomids from Arctic
lakes, during metamorphosis, the concentration of
methylated forms of mercury increases two- to three-
fold (Chetelat et al., 2008). Insect imagoes emerging
from waterbodies contribute to the removal of metal
water and its transfer into terrestrial ecosystems (Speir
et al., 2014; Chumchal and Drenner, 2015; Williams
et al., 2017) and, at the same time, pose a threat to rep-
resentatives of the arachno- and avifauna, both near-
water and those unconnected to aquatic ecosystems
(Cristol et al., 2008).
Can Hg at the recorded concentrations be harmful
for the species under study and representatives of near-
water biota? The few experimental and field studies
evaluating the potential toxicity of Hg have been done
on a dose–response basis. The concentrations of
metal in the medium (water, bottom sediments, and
substrate) was revealed to cause lethal (mortality, %
for a certain number of hours), sublethal (slowing
growth, motor and respiratory activity, metamorpho-
sis, reproduction, and having a teratogenic effect), and
an absence of visible effects of the reaction of living
organisms. Thus, the exposure of Chironomus riparius
Fig. 5. Mercury content in the muscles of fish sampled in
Belaya River watercourses.
0.8
0.6
0
MinnowBarbelGudgeon
Kuban spirlin
0.4
0.2
Hg, mg/kg dry weight
774
INLAND WATER BIOLOGY Vol. 14 No. 6 2021
SHAPOVALOV et al.
Meigen, 1804 larvae to a solution of Hg chloride
(1.58 mg/L) resulted in the immobilization of 50% of
the individuals after 48 h (Rodrigues et al., 2013);
keeping these larvae on bottom sediments with total
Hg concentrations of 0.93, 2.42, and 3.84 mg/kg dry
weight leads to a decrease in the survival rate of chi-
ronomids (88, 80, and 26%, respectively) and a sup-
pression of growth and development rate compared to
control (the percentage of individuals hatched from
eggs is 94, 74, and 8%, respectively) (Chibunda,
2009).
However, it is preferable to judge the danger of Hg
for biota (a set of negative deviations in the develop-
ment and functioning of biological systems of all lev-
els) by the concentrations of its inorganic and organic
forms not in abiotic components of the environment,
but in living beings of different levels of the food web,
which reflect the features of biogeochemical transfor-
mations of metal in specific ecosystem conditions
(Jain et al., 2007). In C. riparius larvae reared on mer-
cury-containing food or bottom sediments, the accu-
mulation of 0.6–0.8 mg Hg/kg dry weight slows down
the metamorphosis, and the proportion of individuals
with deformations of the mouth structures of the head
capsule increases to 19–20% (Gremyachikh et al.,
2006; Tomilina and Grebenyuk, 2019). The concen-
trations of Hg (0.01–0.72 mg/kg dry weight) revealed
in the larvae of stoneflies, like in chironomids belong-
ing to the group of amphibiotic insects, may lead to
pathomorphological deviations in the formation of
vital structures and, accordingly, to a decrease in the
competitiveness of animals for food resource, increas-
ing their availability to predators.
CONCLUSIONS
Mercury concentrations in stoneflies from small
tributaries of the Belaya River are comparable to those
in amphibiontic insects from waterbodies and streams
lacking local sources of Hg in the catchment area and
predominantly subject to atmospheric pollution.
Higher levels of metal accumulation were found in the
larvae of stoneflies from watercourses in the
Khamyshinsky field of mineralization (sampling sta-
tions 1 and 2), the runoff from which represents an
additional, albeit insignificant, source of metal input
into the ecosystems of watercourses. The four fish spe-
cies studied (small specimens predominated in the
samples) accumulated Hg in the same concentrations
as the stoneflies. The predatory and large larvae of the
stoneflies are not so much food items for small fish as
their food competitors. In stoneflies accumulating
mercury at concentrations of 0.01–0.72 mg/kg dry
weight, an increase in the proportion of individuals
with pathomorphological deviations in the structure
of the oral apparatus is possible, leading to a decrease
in the viability of the population and, accordingly, the
provision of food for animals of higher trophic levels.
FUNDING
This study was carried out as part of State Task “Physi-
ological, Biochemical, And Immunological Reactions of
Aquatic Organisms under the Influence of Biotic and Abi-
otic Environmental Factors,” no. АААА-А18-
118 01 26 9 01 23 - 4.
OPEN ACCESS
This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, shar-
ing, adaptation, distribution and reproduction in any
medium or format, as long as you give appropriate credit to
the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were
made. The images or other third party material in this article
are included in the article’s Creative Commons license,
unless indicated otherwise in a credit line to the material. If
material is not included in the article’s Creative Commons
license and your intended use is not permitted by statutory
regulation or exceeds the permitted use, you will need to
obtain permission directly from the copyright holder. To
view a copy of this license, visit http://creativecom-
mons.org/licenses/by/4.0/.
COMPLIANCE WITH ETHICAL STANDARDS
Conf lict of interests. The authors declare that they have
no conflicts of interest.
Statement on the welfare of humans or animals. All appli-
cable international, national, and/or institutional guide-
lines for the care and use of animals were followed.
REFERENCES
Atlas presnovodnykh ryb Rossii (Atlas of Freshwater Fishes of
Russia), Moscow: Nauka, 2003, vol. 1.
Balogh, S.J., Swain, E.B., and Nollet, Y.H., Characteristics
of mercury speciation in Minnesota rivers and streams, En-
viron. Pollut., 2008, vol. 154, p. 3.
https://doi.org /10.1016/j.envpol.2007.11.014
Cherchesova, S.K. and Zhiltsova, L.A., Opredelitel’ vesnya-
nok (Plecoptera) Kavkaza (Key to the Caucasian Stoneflies
(Plecoptera)), Moscow: Mosk. S.-Kh. Akad. im. K.A.
Timiryazeva, 2013.
Chetelat, J., Amyot, M., Cloutier, L., and Poulain, A.,
Metamorphosis in chironomids, more than mercury sup-
ply, controls methylmercury transfer to fish in high Arctic
lakes, Environ. Sci. Technol., 2008, vol. 42, no. 24, p. 9110.
https://doi.org /10.1021/es801619h
Chibunda, R.T., Chronic toxicity of mercury (HgCl2) to the
benthic midge Chironomus riparius, Int. J. Environ. Res.,
2009, vol. 3, no. 3, p. 455.
https://doi.org /10.22059/IJER.2010.99
Chumchal, M.M. and Drenner, R.W., An environmental
problem hidden in plain sight? Small human-made ponds,
emergent insects, and mercury contamination of biota in
the great plains, Environ. Toxicol. Chem., 2015, vol. 34,
no. 6, p. 1197.
https://doi.org/10.1002/etc.2954
INLAND WATER BIOLOGY Vol. 14 No. 6 2021
EFFECTS OF POLYMETALLIC ORE OCCURRENCES ON MERCURY ACCUMULATION 775
Chumchal, M.M., Rainwater, T.R., Osborn, S.C., et al.,
Mercury speciation and biomagnification in the food web of
Caddo Lake, Texas and Louisiana, USA, a subtropical
freshwater ecosystem, Environ. Toxicol. Chem., vol. 30,
no. 5, p. 1153.
https://doi.org/10.1002/etc.477
Cristol, D.A., Brasso, R.L., Condon, A.M., et al., The
movement of aquatic mercury through terrestrial food
webs, Science, 2008, vol. 320, p. 335.
https://doi.org/10.1126/science.1154082
Dittman, J.A., Shanley, J.B., Driscoll, C.T., et al., Mercury
dynamics in relation to dissolved organic carbon concentra-
tion and quality during high flow events in three northeast-
ern U.S. streams, Wate r Res., 2010, vol. 46, p. W07522.
https://doi.org/10.1029/2009WR008351
Eagles-Smith, C.A., Wiener, J.G., Eckley, C.S., et al.,
Mercury in western north america: a synthesis of environ-
mental contamination, fluxes, bioaccumulation, and risk to
fish and wildlife, Sci. Total Environ., 2016, vol. 568, p. 1213.
htt ps://doi.org/10.1016/j.scito tenv.2016.05.0 94
Eagles-Smith, C.A., Silbergeld, E.K., Basu, N., et al.,
Modulators of mercury risk to wildlife and humans in the
context of rapid global change, Ambio, 2018, vol. 47, no. 2,
p. 170.
https://doi.org/10.1007/s13280-017-1011-x
Ganter, N., Power, M., Iqaluk, D., et al., Mercury concen-
trations in landlocked arctic char (salvelinus alpines) from
the Canadian Arctic. Part I: Insights from trophic relation-
ships in 18 laces, Environ. Toxicol. Chem., vol. 29, no. 3,
p. 621.
https://doi.org/10.1002/etc.95
Gilmour, C.C., Podar, M., Bullock, A.L., et al., Mercury
methylation by novel microorganisms from new environ-
ments, Environ. Sci. Technol., 2013, vol. 47, p. 11810.
https://doi.org/10.1021/es403075t
Gremyachikh, V.A., Grebenyuk, L.P., Komov, V.T., and
Stepanova, I.K., Accumulation of mercury and its terato-
genic effect on larvae of Chironomus riparius Meigen (Dip-
tera: Chironomidae), Biol. Vnutr. Vod, 2006, no. 1, p. 99.
Gre mya chik h , V.A., Kom o v, V.T., Ivanch ev, V.P., e t al.,
The content of mercury in the fish muscles of the Oka Na-
ture Reserve and surrounding areas, Tr. Okskogo Gos. Prir.
Biosfern. Zapov., 2012, no. 27, p. 377.
Gremyachikh, V.A., Komov, V.T., Trankvilevskii, D.V.,
et al., The content of mercury in aquatic and amphibiotic
insects of various reservoirs and watercourses of the Euro-
pean part of Russia, Materialy V Vserossiiskogo simpoziuma
po amfibioticheskim i vodnym nasekomym Gidroentomologiya
v Rossii i sopredel’nykh stranakh (Proc. V All-Russia Symp.
on Amphibiotic and Aquatic Insects “Hydroentomology in
Russia and Adjacent Countries”), Borok, 2013, p. 46.
Haines, T.A., Komov, V.T., and Jagoe, C.H., Lake acidity
and mercury content of fish in Darwin National Reserve,
Russia, Environ. Pollut., 1992, vol. 78, p. 107.
https://doi.org/10.1016/0269-7491(92)90017-5
Haines, T.A., Komov, V.T., Matey, V.E., and Jagoe, C.H.,
Perch mercury content is related to acidity and color of 26
Russian lakes, Water Air Soil Pollut., 1995, vol. 85, p. 823.
Han, S. and Gill, G.A., Determination of mercury com-
plexation in coastal and estuarine waters using competitive
ligand exchange method, Environ. Sci. Technol., 2005,
vol. 39, no. 17, p. 6607.
https://doi.org/10.1021/es048667z
Harding, K.M., Gowland, J.A., and Dillon, P.J., Mercury
concentration in black flies Simulium spp. (Diptera, Simuli-
idae) from soft-water streams in Ontario, Canada, Environ.
Pollut., 2006, vol. 143, p. 529.
https://doi.org /10.1016/j.envpol.2005.11.040
Hsu-Kim, H. and Sedlak, D.L., Similarities between inor-
ganic sulfide and the strong Hg(II)-complexing ligands in
municipal wastewater effluent, Environ. Sci. Technol., 2005,
vol. 39, no. 11, p. 4035.
https://doi.org/10.1021/es050013
Hsu-Kim, H., Eckley, C.S., Achá, D., et al., Challenges
and opportunities for managing quatic mercury pollution in
altered landscapes, Ambio, 2018, vol. 47, p. 141.
https://doi.org/10.1007/s13280-017-1006-7
Jackson, A.K., Eagles-Smith, C.A., and Emery, C., Spatial
variation in aquatic invertebrate and riparian songbird mer-
cury exposure across a river-reservoir system with a legacy
of mercury contamination, Ecotoxicology, 2019, vol. 29,
no. 200, p. 1.
https://doi.org/10.1007/s10646-019-02043-z
Jain, C.K., Malik, D.S., and Rashmi Yadav, Metal fraction-
ation study on bed sediments of Lake Nainital, Uttaranchal,
India, Environ. Monit. Assess., 2007, vol. 130, p. 129.
https://doi.org/10.1007/s10661-006-9383-6
Jensen, P.D., Sorensen, M.A., Walton, W.E., and Trum-
ble, J.T., Lethal and sublethal responses of an aquatic insect
Culex quinquefasciatus (Diptera: Culicidae) challenged with
individual and joint exposure to dissolved sodium selenate
and methylmercury chloride, Environ. Toxicol., 2007,
vol. 22, p. 287.
https://doi.org/10.1002/tox.20254
Karimi, R., Chen, C.Y., and Folt, C.L., Comparing near-
shore benthic and pelagic prey as mercury sources to lake
fish: the importance of prey quality and mercury content,
Sci. Total Environ., vol. 565, p. 211.
https://doi.org /10.1016/j.scitotenv.2016.0 4.162
Kocman, D., Kanduc, T., Ogrinc, N., and Horvat, M.,
Distribution and partitioning of mercury in a river catch-
ment impacted by former mercury mining activity, Biogeo-
chemistry, 2011, vol. 104, p. 183.
https://doi.org/10.1007/s10533-010-9495-5
Kolka, R.K., Sebestyen, S.D., Verry, E.S., and Brooks, K.N.,
Peatland Biogeochemistry and Watershed Hydrology at the
Marcell Experimental Forest, Florida, USA, Boca Raton:
CRC, 2011.
Komov, V.T., Gremyachikh, V.A., Kamshilova, T.B., and
Lobus, N.V., The content of mercury in the muscles of
perch from the lakes of the Polisto-Lovatskii raised bog
massif, Tr. Gos. Prir. Zapov. Rdeiskii, 2009, no. 1, p. 102.
Komov, V.T., Pronin, N.M., and Mendsaikhan, B., The
content of mercury in the muscles of fish of the Selenga
River and lakes of its basin (Russia), Inland Water Biol.,
2014, vol. 7, no. 2, p. 178.
https://doi.org/10.1134/S1995082914020059
Lavoie, R.A., Jardine, T.D., Chumchal, M.M., et al., Bio-
magnification of mercury in aquatic food webs: a worldwide
meta-analysis, Environ. Sci. Technol., 2013, vol. 47,
p. 13385.
https://doi.org/10.1021/es403103t
Leonova, G.A., Kolmychkov, G.V., Geletii, F.G., and An-
drulaitis, L.D., Content and distribution of mercury in abi-
otic and biotic components of the Bratsk Reservoir ecosys-
tem, Biol. Vnutr. Vod, 2006, no. 2, p. 97.
Medvedev, I.V. and Komov, V.T., Regeneration of freshwa-
ter planarians Dugesia tigrina and Polyceli s tenuis under the
influence of methyl mercury compounds of natural origin,
Russ. J. Dev. Biol., 2005, vol. T. 36, no. 1, p. 29.
776
INLAND WATER BIOLOGY Vol. 14 No. 6 2021
SHAPOVALOV et al.
Mel’nikova, T.N. and Komlev, A.M., Vodonosnost’ rek
Severo-Zapadnogo Kavkaza (Water Content of the Rivers of
the North-West Caucasus), Maikop: Kachestvo, 2003.
Monakov, A.V., Feeding of Freshwater Invertebrates, Ghent:
Kenobi Productions, 2003.
Nevado, J.J.B., Martín-Doimeadios, R.C.R., Bernar-
do, F.J.G., et al., Mercury in the Tapajós River basin, Bra-
zilian Amazon: a review, Environ. Int., 2010, p. 593.
htt ps://doi.org/10.1016/j.envint.2 010.03. 011
Obrist, D., Kirk, J.L., Zhang, L., et al., A review of global
environmental mercury processes in response to human and
natural perturbations: changes of emissions, climate, and
land use, Ambio, 2018, vol. 47, p. 116.
https://doi.org/10.1007/s13280-017-1004-9
Pe kov , I.V., L e vit s kii, V. V., an d K rivovic hev, V. G., M i n er -
alogy of the Belorechenskoe field (North Caucasus, Rus-
sia), Belorechensk. Mestorozhd. Mineral. Al’m., 2010, vol. 15,
no. 2, p. 17.
Polito, M.J., Brasso, R.L., Trivelpiece, W.Z., et al., Differ-
ing foraging strategies influence mercury (Hg) exposure in
an Antarctic penguin community, Environ. Pollut., 2016,
vol. 218, p. 196.
htt ps://doi.org/10.1016/j.envpol.2016.0 4.097
Rodrigues, A.C.M., Jesus, F.T., Fernandes, M.A.F., et al.,
Mercur y toxicity to freshwater organisms: extrapolation us-
ing species sensitivity distribution, Bull. Environ. Contam.
Tox i col . , 2013, vol. 91, p. 191.
https://doi.org/10.1007/s00128-013-1029-0
Ross, H.H., Ross, C.A., and Ross, J.R.P., A Textbook of En-
tomology, New York: Wiley, 1982.
Saukov, A.A., Geokhimiya (Geochemistry), Moscow: Nau-
ka, 1975.
Scheuhammer, A.M., Meyer, M.W., Sandheinrich, M.B.,
and Murray, M.W., Effects of environmental methylmer-
cury on the health of wild birds, mammals, and fish, Ambio,
2007, vol. 36, p. 12.
https://doi.org/10.1579/0044-7447(2007)36[12:EOE-
MOT]2.0.CO;2
Schuster, P.F., Shanley, J.B., Marvin-Dipasquale, M.,
et al., Mercury and organic carbon dynamics during runoff
episodes from a northeastern USA watershed, Water Air Soil
Poll ut., 2008, vol. 187, p. 89.
https://doi.org/10.1007/s11270-007-9500-3
Shapovalov, M.I., Insects in zoobenthos communities of
mountain rivers of the North-West Caucasus, in Sbornik
materialov VI Mezhdunarodnoi nauchnoi konferentsii “Vul-
kanizm, biosfera i ekologicheskie problemy” (Proc. VI Int.
Sci. Conf. “Volcanism, Biosphere, and Environmental
Problems”), Maikop: Adygeisk. Gos. Univ., 2011, p. 296.
Shapovalov, M.I., Aquatic and amphibiotic insects (Ple-
coptera, Ephemeroptera, Trichoptera, Odonata, Coleop-
tera, Heteroptera) of the Northwestern Caucasus: fauna,
ecology, and bioresource potential, Extended Abstract of
Doctoral (Biol.) Dissertation, Vladikavkaz, 2020.
Sokal, R.R. and Rohlf, F.J., Biometry: the Principals and
Practice of Statistics in Biological Research, New York: Free-
man, 1995.
Speir, S.L., Chumchal, M.M., Drenner, R.W., et al.,
Methyl mercury and stable isotopes of nitrogen reveal that a
terrestrial spider has a diet of emergent aquatic insects, En-
viron. Toxicol. Chem., 2014, vol. 33, p. 2506.
https://doi.org/10.1002/etc.2700
Stepanova, I.K. and Komov, V.T., Mercury accumulation
in fish from water bodies of the Vologodskaya oblast, Russ.
J. Ecol., 1997, vol. 28, no. 4, p. 260.
Tatsii, Y.G., Udachin, V.N., and Aminov, P.G., Environ-
mental geochemistry of mercury in the area of emissions of
the Karabashmed Copper Smelter, Geochem. Int., 2017,
vol. 55, no. 10, p. 935.
https://doi.org /10.1134/S0016702917100093
Tavshunsky, I., Eggert, S.L., and Mitchell, C.P.J., Accu-
mulation of methylmercury in invertebrates and masked
shrews (Sorex cinereus) at an upland forest–peatland inter-
face in Northern Minnesota, USA, Bull. Environ. Contam.
Tox i col., 2017, vol. 99, no. 6, p. 673.
https://doi.org /10.1007/s00128-017-2198-z
Tomilina, I.I. and Grebenjuk, L.P., Induction of deformi-
ties of the hard-chitinized mouthpart structures of larvae
Chironomus riparius Meigen under various contents of per-
sistent organic substances in bottom sediments, Inland Wa-
ter Biol., 2019, vol. 12, no. 3, p. 346.
https://doi.org/10.1134/S1995082919030167
Topashka-Ancheva, M., Metcheva, R., and Teodorova, S.,
A comparative analysis of the heavy metal loading of small
mammals in different regions of Bulgaria II: Chromosomal
aberrations and blood pathology, Ecotoxicol. Environ. Saf.,
2003, vol. 54, p. 188.
https://doi.org /10.1016/S0147-6 513(02 )0005 2-0
Troitskii, S.K. and Tsunikova, E.P., Ryby basseinov Nizhne-
go Dona i Kubani: rukovodstvo po opredeleniyu vidov (Fishes
of the Lower Don and Kuban Basins: Species Identification
Guide), Rostov-on-Don: Knizhn. Izd., 1988.
Tweedy, B.N., Drenner, R.W., Chumchal, M.M., and
Kennedy, J.H., Effects of fish on emergent insect-mediated
flux of methyl mercury across a gradient of contamination,
Environ. Sci. Technol., 2013, vol. 47, p. 1614.
https://doi.org/10.1021/es303330m
Ullrich, S.M., Ilyushchenko, M.A., Kamberov, I.M., and
Tanton, T.W., Mercury contamination in the vicinity of a
derelict chlor-alkali plant. part i: sediment and water con-
tamination of Lake Balkyldak and the River Irtysh, Sci. To-
tal Environ., 2007, vol. 381, nos. 1–3.
https://doi.org /10.1016/j.scitotenv.2007.02 .033
Vasil’ev, O.F. and Sukhenko, S.A., Ecology and hydraulic
engineering ecological risk in creating the Katun Reservoir
in connection with the presence of mercury anomalies on
the drainage basin area, Hydrotech. Constr., 1993, vol. 27,
no. 10, p. 563.
https://doi.org/10.1007/BF01545063
Volkodav, I.G., Noble metals in ores and placers of Adygea,
Vestn. Adygeisk. Gos. Univ., Ser. 4: Estestv.-Mat. Tekhn.
Nauki, 2012, no. 4 (110), p. 163.
Williams, E.B., Chumchal, M.M., Drenner, R.W., and
Kennedy, J.H., Seasonality of odonate-mediated methyl-
mercury flux from permanent and semipermanent ponds
and potential risk to red-winged blackbirds (Agelaius phoe-
niceus), Environ. Toxicol. Chem., 2017, vol. 36, no. 10,
p. 2833.
https://doi.org/10.1002/etc.3844
de Wit, H.A., Kainz, M.J., and Lindholm, M., Methylmer-
cury bioaccumulation in invertebrates of boreal streams in
Norway: effects of aqueous methylmercury and diet reten-
tion, Environ. Pollut., 2012, vol. 164, p. 235.
https://doi.org /10.1016/j.envpol.2012.01.041
Translated by D. Pavlov
