Macrozoobenthos of the shallow waters of Pechora Bay (SE Barents Sea)

Abstract

Macrozoobenthic communities provide vital ecosystem services including habitats and foraging resources for other species in all marine ecosystems. Although macrozoobenthos of deeper parts of the Pechora Sea (SE Barents Sea) have been studied in more detail, there is a lack of research in shallow waters of the Pechora Bay. The study area lies within the Nenetsky State Nature Reserve, established in 1997, to protect important breeding and moulting grounds of waterfowl. Macrozoobenthos provide key foraging resources for waterfowl in the nature reserve, however, there is a mismatch between ornithological and macrobenthic data. Eight stations were studied along the Russky Zavorot Peninsula in the Pechora Bay on a depth of 1.1–1.8 m within the near-shore zone of the Nenetsky State Nature Reserve in August 2016. A monodominant community of Limecola balthica with a biomass of 21.31 ± 0.32 g/m2 and 14 species in total was recorded across the area. The dominant species of the community correspond to those in the community of L. balthica recently described from the central estuarine part of the Pechora estuary. A low biomass and poor species richness in the L. balthica community support the earlier published results for the northern part of the bay and indicate the dependence of the community characteristics on environmental factors. The paucity of macrozoobenthos in the area is likely attributed to extreme environmental conditions including the following: (1) the water column freezes to the bottom during winter in the shallows of the Pechora estuary or (2) the freshwater flow spreads under the ice, severely impacting salinity. Hence the community is comprised of eurythermal and euryhaline forms and is reduced in biomass. It is unlikely that the shallows of the Russky Zavorot Peninsula play an important role as feeding grounds for benthic predators since a low in biomass barren community of a burrowing mollusc L. balthica does not provide enough foraging resources to feed stocks of waterfowl. The L. balthica-community could be used as an indicator of climate changes in the future – it is predicted that a reduction in sea ice volume will improve conditions for growth of L. balthica and may therefore lead to an increased body size and biomass of bivalves in the shallows.

Full text

Nature Conservation Research. Заповедная наука 2019. 4(4) https://dx.doi.org/10.24189/ncr.2019.058
MACROZOOBENTHOS OF THE SHALLOW WATERS OF PECHORA BAY
(SE BARENTS SEA)
Anna A. Gebruk1,2, Polina B. Borisova3, Milana A. Glebova2, Alexander B. Basin3,
Miloslav I. Simakov3, Nikolay V. Shabalin2, Vadim O. Mokievsky3
1University of Edinburgh, United Kingdom
e-mail: Anna.Gebruk@ed.ac.uk
2Marine Research Centre of Lomonosov Moscow State University, Russia
3Shirshov Institute of Oceanology of RAS, Russia
Received: 16.03.2018. Revised: 01.08.2019. Accepted: 02.08.2019.
========== ОРИГИНАЛЬНЫЕ СТАТЬИ ===========
============= R E S E AR C H A RT I C L ES =============
Macrozoobenthic communities provide vital ecosystem services including habitats and foraging resources for
other species in all marine ecosystems. Although macrozoobenthos of deeper parts of the Pechora Sea (SE Bar-macrozoobenthos of deeper parts of the Pechora Sea (SE Bar-
ents Sea) have been studied in more detail, there is a lack of research in shallow waters of the Pechora Bay. The
study area lies within the Nenetsky State Nature Reserve, established in 1997, to protect important breeding and
moulting grounds of waterfowl. Macrozoobenthos provide key foraging resources for waterfowl in the nature
reserve, however, there is a mismatch between ornithological and macrobenthic data. Eight stations were studied
along the Russky Zavorot Peninsula in the Pechora Bay on a depth of 1.1–1.8 m within the near-shore zone of
the Nenetsky State Nature Reserve in August 2016. A monodominant community of Limecola balthica with a
biomass of 21.31 ± 0.32 g/m2 and 14 species in total was recorded across the area. The dominant species of the
community correspond to those in the community of L. balthica recently described from the central estuarine
part of the Pechora estuary. A low biomass and poor species richness in the L. balthica community support the
earlier published results for the northern part of the bay and indicate the dependence of the community charac-
teristics on environmental factors. The paucity of macrozoobenthos in the area is likely attributed to extreme
environmental conditions including the following: (1) the water column freezes to the bottom during winter in
the shallows of the Pechora estuary or (2) the freshwater ow spreads under the ice, severely impacting salinity.
Hence the community is comprised of eurythermal and euryhaline forms and is reduced in biomass. It is unlikely
that the shallows of the Russky Zavorot Peninsula play an important role as feeding grounds for benthic preda-
tors since a low in biomass barren community of a burrowing mollusc L. balthica does not provide enough forag-
ing resources to feed stocks of waterfowl. The L. balthica-community could be used as an indicator of climate
changes in the future – it is predicted that a reduction in sea ice volume will improve conditions for growth of L.
balthica and may therefore lead to an increased body size and biomass of bivalves in the shallows.
Key words: Arctic, biomass, estuary, Limecola balthica, macrobenthic community
Introduction
The Arctic Ocean has one of the most sensi-
tive to environmental changes ecosystems on Earth
(Spiridonov et al., 2012). Declines in sea ice thick-
ness in the Arctic Ocean, along with an increase in air
temperature, ocean acidication and anthropogenic
pressures from oshore industries lead to changes in
the marine ecosystems of the Arctic regions (Kwok
& Rothrock, 2009). The benthic fauna is often used
to observe contemporary changes in the environ-
ment, since various environmental factors including
the availability of organic matter and water temper-
ature, as well as human activities, have direct impact
on biomass and the composition of macrozooben-
thos assemblages (Denisenko et al., 2003; Hinz et
al., 2009). Recent publications revealed that benthic
invertebrates also tend to ingest and accumulate mi-
croplastics from the water column (Courtene-Jones
et al., 2017; La Beur et al., 2019). Hence, there is a
need for expanding the current knowledge on mac-
robenthos, especially in the Arctic regions.
The Pechora Sea in the southeast (SE) basin of
the Barents Sea is characterised by shallowness, a
specic hydrological regime and by an intense o-
shore oil and gas exploration and production (Den-
isenko et al., 2003). The macrozoobenthos of the
Pechora Sea accounts for approximately 35% of the
benthic biodiversity in the Barents Sea and is gener-
ally well-described for the deeper waters; however,
there is a lack of data for the near-shore areas (Dahle
et al., 1998; Denisenko et al., 2003; Kucheruk et al.,
2003; Sukhotin et al., 2008; Denisenko N. et al.,

2019). The macrozoobenthos of the Pechora Sea is
characterised by a high variability in spatial distribu-
tion («mosaic pattern») caused by alterations of sea-
oor topography and sediment types. Presumably
this is also applicable for the Pechora Bay (Dahle et
al., 1998; Denisenko et al., 2003).
The study area is within the Pechora Bay, the
large estuarine ecosystem that assures a huge pro-
portion of continental runo into the Barents Sea
region. The Pechora Sea receives approximately
2.5 million tonnes of terrigenous sediments annu-
ally through the Pechora estuary (Dobrovolsky
& Zalogin, 1982). The Pechora Bay is character-
ised by a broad intertidal zone, with a tide height
of 1.1–1.5 m (Byshev et al., 2003; Denisenko N. et
al., 2019). The ice thickness in winter reaches 1.5
m, freezing to the bottom of the shallow near-shore
areas of the bay. Sediments in the bay are formed
by clayey sands and are inuenced by a continental
runo and permafrost abrasion (Denisenko N. et al.,
2019). The latest review of macrozoobenthos of the
Pechora Bay was by Denisenko N. et al. (2019) and
was based on samples collected in 1995. Twenty-
two sites from a depth range of between 5 m and 18
m were studied in the north-east and central areas
of the bay. Overall, the most common was a typi-
cal estuarial assemblage with a strong dominance of
Limecola balthica Linnaeus, 1758 (occurring at 9 of
22 sites). The L. balthica-community described by
Denisenko N. et al. (2019) had a mean biomass of
130.3 ± 64.8 g/m2 and comprised 34 species in total.
The study area lies within the 1st zone of the
Nenetsky State Nature Reserve named «Pechora
river estuary and a 2 km water territory surround-
ing the Russky Zavorot peninsula». The Nenetsky
State Nature Reserve covers the River Pechora es-
tuary and nearby islands. In total the state nature
reserve covers an area of 3134 km2 of which more
than a half (1819 km2) corresponds to marine areas
(Nenetsky Zapovednik, 2019). To safeguard the
area from rapidly developing industrial activities,
a state nature reserve was established in 1997. The
main aim of establishing the nature reserve was the
protection of important habitats for waterfowl that
stopover in shallow waters of the Pechora Sea dur-
ing their migration from reproduction sites in West
Siberia to variable wintering sites (Sukhotin et al.,
2008). The Nenetsky State Nature Reserve pro-
vides nesting and feeding grounds, and forms part
of the migration routes for 125 species of water-
fowl and coastal birds. This includes species from
the Red Data Book of the Russian Federation and
IUCN Red List of threatened species, such as: the
yellow-billed loon Gavia adamsii Gray, GR, 1859;
Bewick’s swan Cygnus columbianus bewickii Ord,
1815; the lesser white-fronted goose Anser albi-
frons Scopoli, 1769; the red-breasted goose Branta
rucollis Pallas, 1769 (IUCN, 2019).
Common species, such as the king eiders (So-
materia spectabilis Linnaeus, 1758), form abundant
ocks of up to tens of thousands of individuals to
feed and molt before migrating to wintering grounds
(Krasnov et al., 2002). Marine ducks, including king
eiders, are specialised benthic feeders and their main
prey items are bivalves (Sukhotin et al., 2008). For-
aging macrobenthos were studied near the coasts of
the Dolgy Island (Sukhotin et al., 2008; Denisenko
S. et al., 2019). A mismatch between ornithological
and macrobenthic data for the region was rst noted
by Sukhotin et al. (2008). However, macrobenthic
assemblages have previously never been studied in
the shallows of the continental shore of the Nenet-
sky State Nature Reserve. For the open-sea, sandy
shallows (5–7 m deep) of the Medynsky Zavorot
Peninsula, between the mouth of Pechora Bay and
Dolgy Island, a community dominated by Limecola
balthica (previously known as Macoma balthica
Linnaeus, 1758) was described at several stations
(Kucheruk et al., 2003). The biomass of benthos in
this community was low (ca. 3 g/m2) and species
diversity was scarce (totally16 species and 1–8 spe-
cies per sample), explained by a strong wave action.
Ultimately, there are no macrobenthic data
available for continental shores of the Protected
Area. The present study aimed at fullling the
knowledge gap on shallow-water macrozoobenthos
of the Nenetsky State Nature Reserve by describing
macrozoobenthic assemblages of the Pechora Bay
and comparing them to other Arctic estuarine com-
munities. The results can be used as a baseline data
for further conservation or spatial planning activi-
ties in the area.
Material and Methods
Site description
Benthic samples were collected between 24th
and 30th August 2016 in the Nenetsky State Nature
Reserve from the inner (southern) bay of the Russky
Zavorot peninsula (Fig. 1A). The inner coastline of
the Kuznetskaya inlet forms a shore of the Pechora
Bay and is comprised of wetlands, protected from
the waves and covered by vegetation (Fig. 1C).
Tides on the inner shore are regular, semi-diurnal
with a range of 1–1.5 m. Bottom sediments were
formed of homogeneous sand with silts across the
whole sampling area (Appendix 1).
Nature Conservation Research. Заповедная наука 2019. 4(4) https://dx.doi.org/10.24189/ncr.2019.058

Fig. 1. Map of the study area. A: Study area (black rectangular) and territory under protection of the Nenetsky State Nature
Reserve (green hatching). B: Sampling sites with bathymetry data shown for each site. C: Typical view of the swamped south-
ern shore of the peninsula open to the Kuznetskaya inlet.
Sampling
Samples were taken at 8 stations in 3 replicates
from each site in the depth range between 1.1 m to
1.8 m at low tide from a rubber motorboat with a
hand shovel with capture volume of 0.05 m2. Sedi-
ments were washed over a mesh size of 0.5 mm with
sea water, then pre-xed with 4% formaldehyde.
In the laboratory, pre-xed animals were man-
ually sorted out of the organic debris of the samples
for species identication, studied and re-xed in
70% ethanol solution. Macrobenthic invertebrates
were studied and photographed under a binocu-
lar microscope Leica165C and identied with the
maximum level of certainty. All the species names
were given in accordance to the World Register of
Marine Species (WoRMS). For each sample iden-
tied taxa were counted and weighed on a Jewelry
Scale ML-CF3 to mg, unidentied fragments were
also weighed and recorded as «Varia».
Polychaeta fragments were counted both in an-
terior and posterior fragments and the bigger value
chosen for each species. Bivalve molluscs were
weighed with exoskeleton.
Calculations
Microsoft Excel and software PAST (version
2.17) were used for data analysis (Hammer et al.,
2001; Hammer & Harper, 2006). Non-transformed
data were used.
Standard diversity indices were used to charac-
terise diversity (dominance, Simpson index, Shannon
index, Chao2), all calculations were performed using
PAST software package (Hammer & Harper, 2006).
Species accumulation curve or sample-based
rarefaction was used to assess how samples repre-
sent biodiversity (species richness) predicted in the
area. The predicted species richness ( ) computed
with Chao2-type estimator following Colwell et al.
(2004), species accumulation curve was plotted in
PAST with 95 percent condence intervals (Ham-
mer & Harper, 2006):
where H – samples, Sobs – the total number of
observed species and S1 – the number of species
found in exactly one sample.
Nature Conservation Research. Заповедная наука 2019. 4(4) https://dx.doi.org/10.24189/ncr.2019.058

Mean values ± standard error are given for bio-
mass and abundance.
Determination of macrozoobenthic assem-
blages was based on biomass values. Species with
the largest contribution to biomass at each station
were considered as dominants, second and third
largest – as subdominants.
Classical hierarchical clustering based on paired
group (UPGMA) algorithm and non-metric multidi-
mensional scaling (MDS) both based on Bray-Cur-
tis similarity index (Hammer & Harper, 2006) were
used to reveal whether the benthos across the sites
formed distinct communities (groups). The Similar-
ity percentage (SIMPER) was applied to assess taxa
contribution to dierences between the groups. The
one-way analysis of similarities (ANOSIM) with
Bonferroni-corrected p-values following Hammer
& Harper (2006) was used to estimate the signi-
cance of dierences between the groups. The Pear-
son coecient (r) was applied to assess correlations
with environmental variables.
Maps were designed in ESRI ArcMap 10.4.1
using the standard GIS tools provided by the soft-
ware. The reference coordinate system WGS84
and Universal Transverse Mercator projection
(zone 40N) were used.
Results
A total of 14 taxa of benthic invertebrates were
identied in 24 samples from 8 stations, 12 taxa
identied to species level (Table 1). The fauna was
mainly comprised of crustaceans (5 species), poly-
chaetes (4 species) and bivalves (3 species), and with
a single species of Priapulida and Insecta. Bivalves
were the dominant group in both total biomass and
abundance. The mean biomass of the macrobenthic
invertebrates in the area was 21.31 ± 0.32 g/m2 and
the mean abundance was 2131 ± 1825 individuals
per m2 (ind/m2). Primary data on abundance, bio-
mass and number of species per sample are present-
ed in Appendix 1. A taxonomic matrix of species
with images of the specimens is in Appendix 2.
The Shannon diversity was low (H’ = 1.26), mac-
rozoobenthos was represented by a small number of
taxa with a few individuals and astrong dominance
of one species (Table 2). The predicted number of
species was the same as discovered (Chao-2 rich-
ness = 14.19). The biodiversity was represented close
to equally between the stations: four species had
100% occurrence in the study area, and only one spe-
cies had < 20% occurrence (Table 1).
The species accumulation curve approached the
plateau at the level of 7 stations, reaching 14 species
(Fig. 2). The discovered diversity of macrozooben-
thos was therefore fully representative for the area.
The hierarchical clustering and MDS plots
showed three groups of stations in the study area
(Fig. 3). Group A consisted of stations 5, 7 and 8;
group B included stations 2, 3 and 6; and station 1
formed a separate group.
ANOSIM analysis showed statistically signicant
dierence between group A and B (Table 3, p < 0.05).
Table 1. Species composition of macrozoobenthos and mean values of biomass (g/m2) and abundance (ind./m2) of each
species in the study area in 2016
Taxonomic
group Species Mean biomass for the
study area, g/m2
Mean abundance for
the study area, ind./m2
Frequency of oc-
currence across
sites
Habitats*
Bivalvia Cyrtodaria kurriana Dunker, 1861 0.18 ± 0.004 10.83 ± 0.21 0.5 m, b
Bivalvia Limecola balthica L.1758 17.29 ± 0.19 762.50 ± 7.54 1 m
Bivalvia Yoldia hyperborea Gould, 1841 2.87 ± 0.09 595.00 ± 8.05 1 m
Crustacea Saduria entomon Linnaeus, 1758 0.05 ± 0.001 2.500 ± 0.07 0.38 m, b
Crustacea Monoporeia anis Lindstrцm, 1855 0.006 ± 0.001 2.500 ± 0.07 0.25 b, f
Crustacea Pontoporeia femorata Krшyer, 1842 0.001 ± 0.001 0.833 ± 0.04 0.16 m, b
Crustacea Monoculodes sp. Stimpson, 1853 0.003 ± 0.001 4.167 ± 0.13 0.38 m
Crustacea Diastylis sulcata Calman, 1912 0.005 ± 0.001 6.667 ± 0.13 0.75 m, b
Insecta Chironomidae gen.sp. 0.002 ± 0.003 1.667 ± 0.06 0.25 m
Polychaeta Eteone agg. ava Fabricius, 1780 0.09 ± 0.001 31.667 ± 0.32 1 m
Polychaeta Laonice cirrata M. Sars, 1851 0.001 ± 0.001 0.833 ± 0.04 0.13 m, b
Polychaeta Micronephthys minuta Thйel, 1879 0.009 ± 0.007 6.667 ± 0.09 0.63 m
Polychaeta Spio armata Thulin, 1957 0.57 ± 0.007 686.667 ± 7.39 1 m
Priapulida Halicryptus spinulosus von Siebold,
1849 0.17 ± 0.001 1.667 ± 0.06 0.25 m
Note: *Typical habitats are presented according to WoRMS with corrections (Filatova & Zenkevich, 1957; Zhirkov, 2001): m – marine,
b – brackish, f – fresh.
Nature Conservation Research. Заповедная наука 2019. 4(4) https://dx.doi.org/10.24189/ncr.2019.058

Fig. 2. Sample rarefaction (Mao’s tau): red line – accumulat-red line – accumulat-
ed number of species, blue line – 95% condential interval,
black dotted line – number of species found in the samples.
Table 2. Key characteristics of macrozoobenthic diversity in
the study area: number of taxa, number of individuals, domi-
nance, Simpson diversity, Shannon diversity, estimated spe-
cies richness (Chao-2 metric)
Diversity indices Values of diversity
indices
Taxa_S 14
Individuals 2537
Dominance_D 0.3151
Simpson_1-D 0.6849
Shannon_H 1.262
Chao-2 14.19
Fig. 3. Groups of stations in the study area determined by the hierarchical clustering (carried out on macrozoobenthic biomass
data) (A) and MDS (B). Three groups can be seen: A – stations 5, 7 and 8, (purple shading); B – stations 2, 3, 4 and 6 (green
shading); C – station 1.
Table 3. Pairwise comparison of groups of stations with
ANOSIM analysis, Bonferroni-corrected p-values and R-
values shown
Group B
Group A p = 0.0283; R = 1
The variation in biomass of three species of bi-
valves (Limecola balthica, Yoldia hyperborea Gould,
1841 and Spio armata Thulin, 1957) assured dierence
between the stations as shown by SIMPER analysis (Ta-
ble 4). The biomass of the bivalve L. balthica accounted
for 83.7% contribution to the dissimilarity between the
groups. Despite the statistical dierence between the
groups of stations, L. balthica remained the dominant
species for all of the stations in the study area and dif-
ferences were likely caused by natural variation in spa-were likely caused by natural variation in spa-
tial distribution of the biomass of the common species.
The macrozoobenthos in the study area was therefore
formed by a monodominant community of L. balthica.
The species composition of each station and
spatial distribution of the macrozoobenthos biomass
(g/m2) across the study area are shown in Fig. 4. The
biomass of macrozoobenthos per station had no cor-
relation with the depth range (r = -0.45, p = 0.2).
Discussion
The macrozoobenthos of the Pechora Sea has
been studied over nearly a hundred years (Zenk-
evich, 1927; Dahle et al., 1998; Denisenko S. et
al., 2003, 2019; Kucheruk et al., 2003; Sukhotin
et al., 2008; Denisenko N. et al., 2019). However,
the vast majority of benthic surveys in this region
were conducted on-board large research vessels
at depths greater ~10 m. Hence there is a lack of
macrozoobenthic data for near-shore and estua-
rine zones. This is also true for most of the Arc-
tic zones, where shallow estuarine ecosystems are
usually out of focus of big surveys.
Nature Conservation Research. Заповедная наука 2019. 4(4) https://dx.doi.org/10.24189/ncr.2019.058

Table 4. Species contribution to dissimilarity between groups of stations produced by SIMPER analysis (only taxa with >1%
contribution shown)
Taxon Average dissimilarity Contribution % Cumulative % Group A Group B
Limecola balthica 78.56 83.7 83.7 0.091 4.65
Yoldia hyperborea 11.38 12.13 95.83 0.073 0.793
Spio armata 1.902 2.027 97.85 0.005 0.113
Fig. 4. Biomass (g/m2) and dominant species of invertebrates on the sampling sites.
The present study provides the rst detailed
report on macrozoobenthos of the continental shal-
lows of the Nenetsky State Nature Reserve, al-
though macrozoobenthos of the central and north-
ern parts of the Pechora estuary were discussed in
a recent publication by Denisenko N. et al. (2019).
The authors sampled twenty estuarine sites in the
Pechora Bay during the RV Geophysic cruise in
spring 1995 and compared the Pechora Bay macro-
zoobenthos with that of the Ob bay in the Kara Sea
(Denisenko et al., 1999). Recently Denisenko N. et
al. (2019) reviewed their data.
Despite the small number of species found in
the present study, the biodiversity of the macrozoo-
benthos was representative for the study area since
it matched the predicted species richness (Chao-
2 = 14.19, n = 14). Estuaries are typically character-
ised by lower biodiversity of macrobenthic inver-
tebrates compared to marine environments. Ratios
between marine, estuarine and freshwater species
in the composition of estuarine macrozoobenthos
typically depend on the salinity of a particular site
(Whiteld et al., 2012). The River Pechora estuary
is characterised as a mesohaline zone with low spe-
Nature Conservation Research. Заповедная наука 2019. 4(4) https://dx.doi.org/10.24189/ncr.2019.058

cies richness (Denisenko N. et al., 2019). The spe-
cies richness is aected more by the granulometric
sediment structure than organic matter content of
sediments or water salinity variations within the
Pechora estuary (Denisenko N. et al., 2019). In the
present study the fauna was comprised of marine
species with a few brackish crustaceans. At least
one brackish species was present at each station.
Monoporeia anis Lindstrцm, 1855 and Saduria
entomon Linnaeus, 1758, occurred with the fre-
quency of 0.38 (recorded for stations 7 and 8) and
0.25 (stations 1, 2 and 8) respectively.
Macrobenthos communities in the study area
were dominated by Limecola balthica with the
mean biomass of 21.31 ± 0.32 g/m2 (varying from
1.33 g/m2 on station 1 to 43.17 g/m2 on station 2),
and a total of 14 species. The observed dierences
in biomass between the stations were presumably
a statistical artefact caused by natural variation in
spatial distribution of biomass across the bay since
the structure of dominance remained the same
across the study area. Sediments also were the
same across the study area supporting consistency
of the benthic community. However, we acknowl-
edge that an increasing research area would give a
better understanding of the consistent patterns of
species distribution across the bay.
In 1995, Denisenko N. et al. (2019) revealed
ve types of macrobenthic communities in the
central and northern parts of the bay, as opposed
to the only one observed in the present study. Of
these ve types, the community dominated by L.
balthica was the most common overall and was
characterised by the authors as typical for muddy-
sand bottoms at depths of 5–10 m in the central
part of the bay, with a strong dominance of L. bal-
thica, a total of 34 species, moderate abundance
and a biomass of 130.3 ± 64.8 g/m2 (Denisenko N.
et al., 2019). As for diversity, the majority of spe-
cies found in the present study were also present in
Denisenko’s L. balthica-community, except for the
following: Chironomidae gen.sp., Laonice cirrata
M. Sars, 1851, Spio armata and Yoldia hyperbo-
rea. All these species are typical for shallow water
and often found in terrigenous coastal muds. The
closest to our study area site sampled in 1995 was
site 24 characterised by the L. balthica-community
with a biomass of 21.9 ± 1.8 g/m2.
The study area is characterised by extreme
environmental conditions for macrozoobenthos,
e.g. an ice thickness up to 1.5 m with most habi-
tats at depths 1–2 m freezing to the bottom. The
inner shore of Russky Zavorot Peninsula is isolat-
ed from wind-drift convection and is most prob-
ably impacted by the River Pechora run o. Fur-
thermore, in semi-isolated near-shore areas in the
Arctic, continental stock in winter forms a fresh-
water outow that spreads under the ice, forming
a layer of fresh water, forcing marine macrozoo-
benthos to move deeper into sublittoral zones, as
was also described for the Canadian Arctic (Ellis,
1995). Therefore, the macrobenthic richness in
the area is limited by ice thickness and freshwa-
ter impact and is comprised of eurythermal and
euryhaline forms, tolerant to uctuations in both
temperature and salinity. The sea ice thickness
and under-ice freshwater impact are common
limitation factors for intertidal and upper sublit-
toral zones in the Arctic shallows (Mokievsky et
al., 2016). Ultimately the community in the study
area corresponds to the community with a domi-
nance of L. balthica determined by Denisenko N.
et al. (2019), though with lower richness and a
biomass due to extreme conditions.
A further reduction of the Limecola-commu-
nity was reported from the open shores of the Pe-
chora Sea (Kucheruk et al., 2003). Biomass values
in this area were even lower than in the present
study, whilst among driving factors of macroben-
thic distribution authors emphasised not the ice
thickness or freshwater input, but wind waves that
disturb sea bottom down to several meters depth
as it has been shown for shallowness near Dolgy
Island (Denisenko S. et al. 2019). As in the present
study, the dominant species were also represented
by abundant juveniles only (up to 1000 ind/m2)
with a complete lack of adults.
Limecola balthica is an infaunal bivalve mol-
lusc with a circumpolar distribution, common in
the intertidal zones and estuaries, often dominant
in soft bottom communities (Väinölä & Varvio,
1989). In the Arctic region, L. balthica is dominant
within the Pechora Bay as a relict species. A com-
munity with dominance of L. balthica and Cyrto-
daria kurriana Dunker, 1861 was also described
from the shallows of Baydara Bay (Kucheruk et al.,
1998), but it was absent in typical Arctic estuaries,
such as the Ob Bay in the Kara Sea in 1995 (Den-
isenko et al., 1999). Limecola balthica is evidently
sensitive to the climate change, as was shown for
stock from the western Wadden (North) Sea where
an increase in water temperature resulted in a lower
reproductive output and an earlier spawning period
(Philippart et al., 2003).
Among the most common waterfowl of the
Nenetsky State Nature Reserve is the king eider
Nature Conservation Research. Заповедная наука 2019. 4(4) https://dx.doi.org/10.24189/ncr.2019.058

that feeds on macrobenthic invertebrates, often
molluscs (Brun, 1971; Lovvorn et al., 2003; Mer-
kel et al., 2007). It was shown for Dolgy Island in
the Pechora Sea that marine ducks including the
king eider were predominantly feeding on mussels
Mytilus edulis Linnaeus, 1758, that were unreach-
able for traditional techniques of benthic research
and therefore often underestimated (Sukhotin et
al., 2008). Unlike the Dolgy Island research area,
in the Russky Zavorot Peninsula any rock outcrops
or fragments of mussel shells were not recorded
during the present study. It is unlikely that the
Limecola balthica-community in the shallows of
Russky Zavorot peninsula provides enough forag-
ing resources to sustain big stocks of waterfowl.
It has been repeatedly predicted in the lit-
erature that increasing temperatures in the Arctic
will aect benthic communities, which could lead
to changes in species distribution and interaction,
allow the introduction of new species, and en-
able a decrease of arctic species alongside with
an increase of boreal species in the composition
of benthic fauna (Lambert et al., 2010; Josefson
et al., 2013; Renaud et al., 2015). The Barents Sea
has been identied as a hotspot for «atlantica-
tion» of seawater and the expansion of boreal spe-
cies (Renaud et al., 2015; Vihtakari et al., 2018).
It is likely that eects of climate change on the
macrozoobenthos of the Pechora Bay will appear
in the foreseeable future. In the study area, the
thickness of sea ice is a key limitation factor for
macrozoobenthos, therefore reduction of the sea
ice volume would likely improve conditions and
habitat availability for the L. balthica-community
which leads to increasing the body size and bio-
mass of molluscs inhabiting shallows. To achieve
a broader understanding of the biomass trends of
L. balthica stock in Nenetsky State Nature Re-
serve near-shore areas, the present study can be
considered as a baseline with further regular ob-
servations required.
Conclusions
A сommunity of macrobenthic invertebrates
with a mean biomass of 21.31 ± 0.3 g/m2, strongly
dominated by L. balthica, and comprising a total
of 14 species, was described based on 8 stations
in the shallows of the Russky Zavorot Peninsula
at a depth of 1.1–1.8 m in August 2016. This is the
rst study of the benthos of the continental shal-
lows of the Nenetsky State Nature Reserve. All
studied sites were characterised by a muddy-sand
substrate. The observed community represents a
form reduced in richness and biomass of the L.
balthica-community, described by Denisenko N.
et al. (2019) from the central and northern parts of
the River Pechora estuary. At the periphery of its
distribution, the community is attributed to sea ice
thickness and freshwater impact and is therefore
comprised of eurythermal and euryhaline forms.
Species occurring in the shallows but absent in
deeper habitats described by Denisenko N. et al.
(2019) included Chironomidae gen.sp., Laonice
cirrata, Spio armata, and Yoldia hyperborea.
It is unlikely that the shallows of Russky Za-
vorot Peninsula play an important role as feeding
grounds for benthic predators since a barren com-
munity of L. balthica does not produce enough for-
aging biomass. The state of the L. balthica-commu-
nity can be used as an indicator of climate change
in the future. We suggest that with a reduction in
the volume of sea ice it is likely that conditions and
habitat availability for the L. balthica-community
will improve in the shallow waters, and this could
lead to an increased size and biomass of bivalves.
However, to gain a better understanding of L. bal-
thica biomass dynamics in the Pechora Bay, more
regular observations are required in both near-
shore and open water areas.
The studies undertaken up until now within the
marine borders of the Nenetsky Reserve are still
rather scarce and do not cover the whole range of
shallow water habitats. As for many other marine
reserves in the Arctic, there is an urgent need for
detailed habitat mapping and diversity estimations.
Acknowledgements
The authors express their gratitude to the adminis-
tration and sta of the Nenetsky State Nature Reserve
for enabling data collection. We gratefully acknowledge
all involved in eldwork (Evgeniy Snytnikov, Michael
Borovskiy, Evgeniy Ezhelya – all are from Lomonosov
Moscow State University) and processing of the samples
(Milena Khutoryanskaya). We also thank Lea-Anne Henry
and Nadia Jogee (Changing Oceans Group, University of
Geosciences), Dr. Andrey Gebruk (Shirshov Institute of
Oceanology of RAS) and anonymous reviewers for giv-
ing helpful feedback. The study is partly supported by the
RFBR grant 18-05-60053.
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Appendix 1. Primary data on abundance, biomass and number of species of macrozoobenthos collected in the Pechora Bay in 2016.
Station-
sample
Co-ordinates Depth, m Abundance,
ind./m2
Biomass,
g/m2Number of species Sediments
N E
1-1
68.897778 53.634167 1.6
60 1.06 2 Muddy sands
1-2 1080 2.02 8 Muddy sands
1-3 640 0.92 2 Muddy sands
2-1
68.896111 53.659444 1.1
1160 0.92 4 Muddy sands
2-2 4500 98.6 7 Muddy sands
2-3 3940 29.98 6 Muddy sands
3-1
68.896667 53.695556 1.3
8400 10.68 5 Muddy sands
3-2 2100 34.16 8 Muddy sands
3-3 3140 43.82 6 Muddy sands
4-1
68.898611 53.736944 1.2
1760 44.84 6 Muddy sands
4-2 3380 33.78 8 Muddy sands
4-3 3860 38.54 7 Muddy sands
5-1
68.905278 53.755278 1.1
1580 5.3 5 Muddy sands
5-2 2900 13.52 5 Muddy sands
5-3 2860 7.78 6 Muddy sands
6-1
68.915833 53.782778 1.4
1600 18.56 7 Muddy sands
6-2 1960 62.44 7 Muddy sands
6-3 1960 37.2 5 Muddy sands
7-1
68.920278 53.799167 1.2
560 2.86 3 Muddy sands
7-1 680 3.4 6 Muddy sands
7-3 1140 5.86 5 Muddy sands
8-1
68.914444 53.820000 1.8
840 5.58 5 Muddy sands
8-2 620 2.84 5 Muddy sands
8-3 420 6.56 3 Muddy sands
Nature Conservation Research. Заповедная наука 2019. 4(4) https://dx.doi.org/10.24189/ncr.2019.058

Appendix 2. Taxonomic matrix of species with images taken under the binocular microscope.
МАКРОЗООБЕНТОС МЕЛКОВОДИЙ ПЕЧОРСКОЙ ГУБЫ
(ЮГО-ЗАПАД БАРЕНЦЕВА МОРЯ)
А. А. Гебрук1,2, П. Б. Борисова3, М. А. Глебова2, А. Б. Басин3,
М. И. Симаков3, Н. В. Шабалин2, В. О. Мокиевский3
1Университет Эдинбурга, Великобритания
e-mail: Anna.Gebruk@ed.ac.uk
2Цетр морских исследований МГУ им. М.В. Ломоносова, Россия
3Институт океанологии им. П.П. Ширшова РАН, Россия
Сообщества макрозообентоса выполняют жизненно важные функции во всех морских экосистемах,
в том числе формируя местообитания и пищевые ресурсы для других видов. Несмотря на то, что ма-
крозообентос более глубоких участков Печорского моря (юго-западная часть Баренцева моря) в целом
изучен достаточно детально, мелководные участки, в частности Печорская губа, изучены значительно
хуже. Район исследований данной работы находился на территории Ненецкого государственного запо-
ведника, основанного в 1997 г. с целью охраны ключевых районов кормления и линьки для морских
птиц. Макрозообентос формирует основу пищевых ресурсов для морских птиц на территории Ненецкого
заповедника, но в литературе наблюдается явный дисбаланс между количеством опубликованных орни-
тологических и гидробиологических данных. В данной работе был исследован макрозообентос восьми
станций, собранный в августе 2016 г. вдоль побережья полуострова Русский Заворот внутри охраняемых
вод Ненецкого заповедника на глубине 1.1–1.8 м. Для всех станций описано монодоминантное сообще-
ство Limecola balthica со средней биомассой 21.31 ± 0.32 г/м2 и 14 видами макрозообентоса. Доминант-
ные виды описанного сообщества совпадают с сообществом L. balthica, недавно описанным в литературе
для центральной части Печорской губы. Низкая биомасса и видовое разнообразие сообщества L. balthica
в исследуемом районе соответствуют ранее полученным данным для северной части эстуария. Они под-
тверждают гипотезу зависимости состояния сообщества от условий среды. Бедность макрозообентоса в
районе работ вероятно связана с экстремальными условиями обитания, включающими (1) промерзание
грунта на этих глубинах зимой или (2) подледное распреснение за счет континентального стока. В связи
с этим макрозообентос сформирован эвритермальными и эврихалинными видами и характеризуется по-
ниженной биомассой. Маловероятно, что континентальные мелководья полуострова Русский Заворот
играют значимую роль как кормовые угодья для бентосных хищников, поскольку бедное по видовому
составу и биомассе сообщество L. balthica не формирует достаточной для морских птиц кормовой био-
массы. Сообщество L. balthica может быть использовано в качестве индикатора дальнейших климатиче-
ских изменений в акватории, поскольку можно предположить, что уменьшение толщины морского льда
улучшит условия обитания и приведет к увеличению размеров и биомассы мелководных моллюсков.
Ключевые слова: Limecola balthica, Арктика, биомасса, макробентосные сообщества, эстуарий
Nature Conservation Research. Заповедная наука 2019. 4(4) https://dx.doi.org/10.24189/ncr.2019.058