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An assessment of the presentability of the biotopes and benthic communities of the northwestern part of the Utrish Nature Reserve marine area for the Caucasian Black Sea coast has been conducted. The literary and original data on the state of benthos in the area from the Kerch Strait to Adler were examined. The studied area of the Utrish Natural Reserve included habitats that are common along the coast (an active cliff, a narrow pebble beach, boulder deposits, rock bench and soft sediments). Only two of the three well-known Black Sea belt macrozoobenthic biocoenoses were observed along the northeastern Black Sea coast: the shallow-water «venus sand» and the deep-water «phaseolina silt». The third biocoenosis («mussel mud») was not noted neither in the reserve's area nor in the studied part of the shelf to the south of Novorossiysk. Of these three belts only «venus sand» was found in the Utrish Nature Reserve's marine area. The absence of the mussel belt in the studied area of the reserve is typical for the southern part of the North Caucasian coast in the current period and thus does not affect the presentability of the reserve's benthic ecosystem. The biocoenosis of the bivalves Pitar rudis – Gouldia minima was common at the muddy sand with shells in both reserve's and reference sites' middle-depths complex instead of the mussel belt which was typical for the 20th century. Its boundary was 10 m deeper in the reserve compared to the reference sites. The absence of the Modiolula phaseolina belt in the area of the reserve could be explained by the insufficient width of the protected marine area (up to 52 m depth); due to this the deep-water complex in the reserve is actually represented by a narrow strip. Extension of the reserve's boundary over the depth of 70 m will include this biocoenosis into the Protected Area, which would significantly increase the presentability of the reserve's marine part for the North Caucasian coast. The biogeographical composition of the reserve's flora, its species diversity and structure in general corresponds to that of the whole region. The macrophyte zone consists of four belts: upper (0–2 m, Dictyota fasciola f. repens + Polysiphonia opaca + Ceramium ciliatum + Ulva compressa), upper mid (2–12 m, Cystoseira crinita + Cystoseira barbata – Cladostephus spongiosus – Ellisolandia elongata), lower mid (12–18 m, Phyllophora crispa, Codium vermilara and Bonnemaisonia hamifera), and the lower belt (below 18 m) formed by a recent invader, B. hamifera. The majority of species found in the reserve's marine area are common species of the Black Sea macrophytobenthos. However, the Utrish Nature Reserve includes more favourable habitats for macrophytes than most of the North Caucasian coast, because the typical macrophyte Cystoseira spp. have been noted at greater depths in the reserve, in comparison to the remaining shelf.
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1
PRESENTABILITY OF THE UTRISH NATURE RESERVE’S BENTHIC
COMMUNITIES FOR THE NORTH CAUCASIAN BLACK SEA COAST
Galina A. Kolyuchkina1,*, Vitaly L. Syomin2,**, Ulyana V. Simakova1, Vadim O. Mokievsky1
1Shirshov Institute of Oceanology, Russian Academy of Sciences, Russia
*e-mail: galka.sio@gmail.com
2Southern Scientic Centre of RAS, Russia
**e-mail: semin@ssc-ras.ru
Received: 01.04.2018
An assessment of the presentability of the biotopes and benthic communities of the northwestern part of the
Utrish Nature Reserve marine area for the Caucasian Black Sea coast has been conducted. The literary and
original data on the state of benthos in the area from the Kerch Strait to Adler were examined. The studied area
of the Utrish Natural Reserve included habitats that are common along the coast (an active cli, a narrow pebble
beach, boulder deposits, rock bench and soft sediments). Only two of the three well-known Black Sea belt
macrozoobenthic biocoenoses were observed along the northeastern Black Sea coast: the shallow-water «venus
sand» and the deep-water «phaseolina silt». The third biocoenosis («mussel mud») was not noted neither in the
reserve’s area nor in the studied part of the shelf to the south of Novorossiysk. Of these three belts only «venus
sand» was found in the Utrish Nature Reserve’s marine area. The absence of the mussel belt in the studied area
of the reserve is typical for the southern part of the North Caucasian coast in the current period and thus does
not aect the presentability of the reserve’s benthic ecosystem. The biocoenosis of the bivalves Pitar rudis –
Gouldia minima was common at the muddy sand with shells in both reserve’s and reference sites’ middle-depths
complex instead of the mussel belt which was typical for the 20th century. Its boundary was 10 m deeper in the
reserve compared to the reference sites. The absence of the Modiolula phaseolina belt in the area of the reserve
could be explained by the insucient width of the protected marine area (up to 52 m depth); due to this the
deep-water complex in the reserve is actually represented by a narrow strip. Extension of the reserve’s boundary
over the depth of 70 m will include this biocoenosis into the Protected Area, which would signicantly increase
the presentability of the reserve’s marine part for the North Caucasian coast. The biogeographical composition
of the reserve’s ora, its species diversity and structure in general corresponds to that of the whole region. The
macrophyte zone consists of four belts: upper (0–2 m, Dictyota fasciola f. repens + Polysiphonia opaca + Cera-
mium ciliatum + Ulva compressa), upper mid (2–12 m, Cystoseira crinita + Cystoseira barbata – Cladostephus
spongiosus – Ellisolandia elongata), lower mid (12–18 m, Phyllophora crispa, Codium vermilara and Bonne-
maisonia hamifera), and the lower belt (below 18 m) formed by a recent invader, B. hamifera. The majority of
species found in the reserve’s marine area are common species of the Black Sea macrophytobenthos. However,
the Utrish Nature Reserve includes more favourable habitats for macrophytes than most of the North Caucasian
coast, because the typical macrophyte Cystoseira spp. have been noted at greater depths in the reserve, in com-
parison to the remaining shelf.
Key words: biocoenoses, biotopes, macrophytobenthos, macrozoobenthos, marine reserve
Introduction
In total, there are about 3000 marine reserves
in the world (Marine Protected Areas, 2011). There
are over 20 Marine Protected Areas (MPAs) of in-
ternational importance along the Black Sea shores
(Alexandrov et al., 2017), and the Utrish Nature
Reserve is the only one situated on the Caucasian
coast. The system of terrestrial Protected Areas ex-
isting at the beginning of the 21st century can be
considered fully representative based on the zonal-
landscape principle (Krever et al., 2009). Contrary
to that, the spatial structure of marine ecosystems
played subordinate role or was just not taken into
account when determining marine reserves’ bound-
aries (Mokievsky et al., 2012a). An assessment of
the species and landscape diversity in the marine
areas of the reserves has not been fully implement-
ed or has not been carried out yet.
The creation of Protected Areas on the Cau-
casian coast is complicated due to a permanent
increase of recreational impact on the coast. The
rst reserve that included a marine area has only
appeared in 2010. It is the Utrish Nature Reserve,
which is situated on the Abrau Peninsula (Chestin,
2009). The main goal of its foundation was to pre-
serve and restore unique natural complexes of dry
subtropics of the Black Sea Caucasian coast (Stat-
ute on the State Nature Reserve Utrish. Approved
Nature Conservation Research. Заповедная наука 2018. 3(4): 1–16 DOI: 10.24189/ncr.2018.065
=============== REVIE W A RT ICLES ===============
2
by the Order of the Ministry of Natural Resources
and Ecology of the Russian Federation No. 145 of
3 March 2011; hereinafter the Statute) whereas
the marine part was created to preserve biological
diversity of the coastal zone of the North Cauca-
sian coast ecosystem, which underwent signicant
changes driven by the climate and anthropogenic
impact at the end of the 20th century – beginning of
the 21st century (Chestin, 2009).
From the beginning of the 20th century until
the end of the 1970s, the Black Sea ecosystems
were considered stable (Zenkevich, 1963; Kiseleva
& Slavina, 1966; Kiseleva, 1981, 1992). However,
since the 1970s, species diversity has decreased,
the dominants of communities have changed, the
lower boundary of macrophytobenthos’ habitats
has shifted to shallower depths (Blinova et al.,
1991; Maximova & Luchina, 2002; Maximova &
Moruchkova, 2005; Afanasyev, 2008; Miniche-
va et al., 2008; Simakova & Maximova, 2009;
Kucheruk et al., 2012) and the role of invasive spe-
cies has increased as a result of anthropogenic eu-
trophication, introduction of new non-indigenous
species and climate change (Shushkina & Vinogra-
dov, 1991; Zaitsev & Oztürk, 2001; Chikina, 2009;
Llope et al., 2011) (Fig. 1). In the North Cauca-
sus, these changes mostly aected the coast to the
south of the Abrau Peninsula (Chikina, 2009). In
the northern part, the changes were not so cata-
strophic, although a siltation of vast bottom areas
has been noted in the Kerch Strait area (Chikina,
2009; Terentyev, 2013). The area of the Utrish Na-
ture Reserve, located at the border of these two
zones, remained comparatively understudied dur-
ing these years.
Marine ecosystem studies of the Utrish Nature
Reserve vicinities began in the early 20th century.
Zernov (1913) was the rst to collect macrozoob-
enthos samples in the area. He found «very poor
phaseolina silt» (silt with domination of the bi-
valve Modiolula phaseolina (Philippi, 1844)) at
a 72 m depth (station 127). Later, as reported by
Kiseleva & Slavina (1965), zoobenthos at 59–103
m depths was presented by a community domi-
nated by Modiolula phaseolina. Shallower depths
were not considered. In 1989, within the frame-
work of the study of the Caucasian shelf coast, the
Odessa branch of the Institute of the Biology of the
Southern Seas conducted a survey in the region of
the Abrau Peninsula (Alekseev & Sinegub, 1992).
The presence of common Black Sea communities
with domination of Chamelea gallina (Linnaeus,
1758) (usually referred to as the «venus sand», af-
ter the old name of the species), Mytilus gallopro-
vincialis Lamarck, 1819 and Modiolula phaseolina
has been observed. However, large areas were oc-
cupied by the Terebellides cf. stroemi Sars, 1835
community. Macrophytes in the vicinity of the
Cape Utrish (northern part of the Abrau Peninsula)
was described by several authors (Kalugina-Gut-
nik, 1975; Blinova et al., 1991; Afanasyev, 2005,
2008; Blinova & Saburin, 2005; Vilkova, 2005a;
Teyubova & Milchakova, 2011) since the 1960s.
The three main zones (or belts) of macrophytes
were present in the area, which is typical along the
Caucasian coast from Anapa to Tuapse. A unique
feature of the Utrish Nature Reserve was that Cys-
toseira spp. was found here at unusual depth (up to
32 m) whereas it had never inhabited depths more
than 20 m at the north Caucasian Coast (Kalugina-
Gutnik, 1975). Some authors later noted that the
waters near cape Utrish are clear and the macro-
phytes inhabit deeper biotopes here (Blinova et al.,
1991; Afanasyev, 2005, 2008).
Fig. 1. Diagram of the bottom communities’ dynamics in the Black Sea in the 20th – beginning of the 21st century (adopted
from Kucheruk et al., 2012, extended according to recent data as in Kolyuchkina et al., 2017c).
Nature Conservation Research. Заповедная наука 2018. 3(4): 1–16 DOI: 10.24189/ncr.2018.065
3
In 1999 and 2001, an environmental impact
assessment of the construction of the Caspian
Pipeline Consortium (CPC) structures in the
South Ozereyevka area (Fig. 2) (Lobkovskiy et
al., 2001) was carried out in this area. When jus-
tifying the creation of the Utrish Nature Reserve
(Chestin, 2009), these data were included into
the total dataset used. According to these, two
communities inhabited soft sediments at depths
of 20–35 m: Chamelea gallina and Anadara ka-
goshimensis (Tokunaga, 1906); and Pitar rudis
(Poli, 1795). Their distribution reected local
conditions of sedimentation. Deeper, at 35–50
m the Mytilus galloprovincialis community was
noted. Depths below 50 m were dominated by
Modiolula phaseolina. Three macrophyte zones
were found on hard bottom: shallow (0–2 m),
medium (2–10 m), and lower (10–20 m). Such
vertical distribution of benthos was typical for
the narrow shelf of the Black Sea before the eu-
trophication period of the 1970s.
Compared to the signicantly transformed
southern and northern parts of the Caucasian
coast, the area of the Utrish Nature Reserve
turned out to be one of the least aected by an-
thropogenic impact. Therefore, it has been rec-
ommended as a reference area that preserved the
initial state of coastal biocoenoses of the north-
eastern part of the Black Sea to the greatest ex-
tent (Chestin, 2009). Since the establishment of
the reserve and until 2016 no studies of benthic
biodiversity have been carried out in the marine
part of the reserve. The surveys performed in
the neighbourhood were not so numerous either.
In the course of complex ecological monitoring
conducted by the Research Institute of the Azov
Sea Fishery Problems in 2010–2012, a study of
benthos, zoo- and phytoplankton has been ac-
complished in the coastal regions to the west and
to the east of the Utrish Nature Reserve. Its em-
phasis was on macroalgae; zoobenthos was only
investigated to the depth of 15 m (Afanasyev
et al., 2013). In 2013, a signicant area of the
sea near the Abrau Peninsula in the region of
the River Sukko conuence was described with-
in the framework of the South Stream project
(ESIA Russian Sector, 2014). Studies conducted
in course of this project did not cover the area
of the reserve. In 2016, the Institute of Marine
Biological Research (Sevastopol) carried out a
survey of sh and decapods populations’ state in
the coastal zone of the reserve (Boltachev et al.,
2017). Thus, before the surveys analysed in this
paper (Kolyuchkina et al., 2017a,b) the latest
work concerning the quantitative distribution of
benthos in the area of the reserve dates back to
2001 (Lobkovskiy et al., 2001; Chestin, 2009).
The creation of any reserve, including ma-
rine, involves not only the restriction of use and
ecosystem protection within its borders, but also
the organisation of long-term monitoring. In par-
ticular, according to the Statute, the Utrish Nature
Reserve «ensures the preservation and restora-
tion of unique and typical natural complexes lo-
cated on the territory of the state natural reserve
«Utrish», the organisation and carrying out of
environmental education of public, development
and implementation of scientic methods of na-
ture protection and environmental monitoring».
To fully implement this, it is necessary to con-
duct surveys assigned to obtain an understanding
of the current state of the protected water area;
especially since no studies of quantitative distri-
bution of benthos have been done in the reserve
area after the disastrous transformation of bottom
communities of the Caucasian Black Sea coast at
the beginning of the 21st century.
The aim of the study is to evaluate the present-
ability of the Utrish Nature Reserve for the regional
benthic communities and to estimate the adequacy
of the reserved marine area to main goals of the re-
serve’s organisation (the preservation and restora-
tion of unique and typical biotopes). The main goal
splits into several particular issues: the evaluation
of habitat presentability of the reserve; estimation
of species diversity within the borders; evaluation
of the diversity of communities and their similarity
to adjacent shelf associations in terms of species
composition and quantitative structure. It is critical
to estimate the rate of concordance in communi-
ties’ dynamics inside and outside the reserve for
extrapolation of the results of monitoring to adja-
cent shelf areas. The present study is an analytical
extension of benthic surveys undertaken in 2014–
2017 (Kolyuchkina et al., 2017a,b,c)
Methods
In 2016–2017, a pilot study of the current state
of bottom ecosystems of the northwestern part of
the reserve’s marine area was carried out in the
area of the River Zhemchuzhnaya conuence dur-
ing a coastal marine expedition of the Institute
of Oceanology of RAS «Black Sea 2016–2017».
These studies were performed within the marine
boundaries of the Utrish Nature Reserve, which
are located at the 50 m isobath (Fig. 2).
Nature Conservation Research. Заповедная наука 2018. 3(4): 1–16 DOI: 10.24189/ncr.2018.065
4
Fig. 2. Map of the studied (Utrish Nature Reserve macrozoobenthic transect), reference areas (Golubaya Bay, Inal Bay and
Shepsi macrozoobenthic transects) and historical macrozoobenthic data: 1999–2001 (Lobkovskiy et al., 2001) and 2001
(Chikina, 2009) (adopted from Kolyuchkina et al., 2017c, extended according to historical data).
The survey included a standard habitat map-
ping (Mokievsky et al., 2012b) using a side-scan
sonar (data were collected and provided by the
Marine Research Centre of the Lomonosov Mos-
cow State University); remotely operated under-
water vehicle (ROV) GNOM PRO (12 sites); div-
ing and video transect survey of hard bottom with
macrophytes; a bathymetric survey. Additionally,
aerial photography (using a Fantom 4 drone) of the
coastal zone (from the cli to the depth of 1–2 m)
was performed. Methods and preliminary results
are described in Svasyan et al. (2017) (Fig. 2).
Samples of zoobenthos and bottom sediments
to determine particle size distribution were taken
from the board of the research vessel «Ashamba»
(Institute of Oceanology of RAS) at ve stations.
Material of annual expeditions of the Institute of
Oceanology of RAS «Black Sea 2014–2017» was
used for comparison. These are 32 stations with
depths 10–50 m from the transects on the traverse
of the Golubaya Bay (March 2017), the Inal Bay
(July 2014, 2015, 2016 and 2017) and near Shepsi
settlement (July 2014) (Fig. 2b). The sampling and
analysing procedures were analogous for all the
stations and are described in detail in the work of
Kolyuchkina et al. (2017c). The analysis of grain
size composition was performed in the Analytical
Laboratory of the Institute of Oceanology of RAS
using the wet sieving method (Petelin, 1967). Pre-
liminary results of the work and a list of recorded
species are presented in the works of Kolyuchkina
et al. (2017a,b,с).
We tried to assess the diversity and present-
ability of the macrophyte communities using
very preliminary published and unpublished data:
underwater video surveys together with bottom
vegetation descriptions of ve videos and div-
ing 200–1500 m long, 0–25 m deep transects
(Smirnov, Papunov, Simakova, unpublished);
ROV video analysis (Simakova & Shabalin, un-
published); qualitative (10 samples) and quanti-
tative (15 samples, metal frame 33 × 33 сm or
0.1 m2) collections at depths of 0.5–17 m (Koly-
uchkina et al., 2017b; Simakova et al., 2017; Si-
makova & Smirnov, 2017). Transect survey, ROV
video samples (point, approximately 10 m in di-
ameter or less) and video transects were analysed
by U.V. Simakova; depth, bottom type (pebble,
hard bottom, soft bottom), macrophyte species
list and dominant species were determined at each
point. Continuous video transects were divided in
sections according to depths (2–5 m, 5–10 m, 10
m and more). Species lists and dominant species
were determined for each section.
For comparison, we used previously published
data on macrophytes from other regions of the
North Caucasian coast (Kalugina-Gutnik, 1975;
Lobkovskiy et al., 2001; Mitjaseva et al. 2003; Si-
Nature Conservation Research. Заповедная наука 2018. 3(4): 1–16 DOI: 10.24189/ncr.2018.065
5
makova, 2009, Simakova, 2011; Teyubova & Mil-
chakova, 2011). Biogeographical classication of
algae species and syntaxon names were carried out
in accordance with Kalugina-Gutnik (1975).
Statistical processing of the data was per-
formed using Primer v. 6.1.16. An assessment
of the species number of macrozoobenthos was
carried out using the expected number of species
index – Chao2 (Chao, 1987). For the analysis
of species richness and diversity, the Shannon
biodiversity index (H’), the Margalef’s species
richness (d), the Pielou’s evenness (J’) and tax-
onomic diversity (Delta) (Clarke & Warwick,
2001) were used. The reliability of groupings
was estimated using the ANOSIM method and
the Taxonomic Distinctiveness Test; SIMPER
algorithm was implemented to evaluate the con-
tribution of species to the dierences between
the groups (Clarke & Warwick, 2001).
Results and Discussion
Presentability of biotopes of the Utrish Na-
ture Reserve
The northeastern shelf of the Black Sea can be
divided into two regions: the region of the ancient
River Kuban delta on the North and the Black
Sea Mountain Chain stretching from Anapa to the
border with Georgia (Blagovolin, 1962; Petrov,
1999; Vilkova, 2005b). In the Kuban paleodelta,
the bottom is composed of sand or silted sand;
deeper than 15 m the share of shells in the com-
position of silted sand increases with a maximum
share at a depth of 20–25 m (Petrov, 1999). In the
area of the Black Sea Chain, the shore is mostly
abrasive. It is characterised by active clis, a nar-
row pebbly beach (up to about 2 m deep) bordered
by an inclined bench composed of ysch depos-
its of Upper Cretaceous and Paleogene age (Ze-
nkovich, 1958). The continuous abrasion of rocks
of unequal resistance to destruction in the ysch
leads to the formation of an intersected sculptural
relief of the bottom (Loginov, 1951; Petrov, 1999;
Vilkova, 2005b). At depths of 10 to 30 m, a at
bottom with soft sediments of dierent particle
sizes (Vilkova, 2005b) underlies a complex re-
lief of the bench. The regular belts with dier-
ent types of sediment along the depth gradient
are disturbed by landslides of various ages and
canyons in the river mouths. South of the village
Dzhanhot, the bench narrows and to the south of
Tuapse rocks are found only opposite protruding
capes. The rest of the bottom is occupied by soft
sediments (Kalugina-Gutnik, 1975). The natural
appearance of the shoreline and the distribution
of sediments in the southern part of the region are
transformed by shore protection structures.
The Abrau Peninsula is located in a transition
zone between the narrow southern shelf and shallow
water near the Kerch strait. In the coastal zone of the
reserve, there is an active cli followed by a narrow
pebble beach. Deeper, there is a boulder bench of a
stepped prole with a shallow inclined upper part
and a sharp bend at a depth of more than 7 m. It
passes into a at, slightly inclined bottom, covered
with soft sediments (Vilkova, 2005b). In addition,
unlike most areas of the North Caucasian coast, the
relief is signicantly complicated by landslides of
dierent ages here (Popkov et al., 2015).
In the reserve’s marine area seven main types
of acoustic signal were obtained using the side-
scan sonar. Matching them with the descriptions
of the bottom landscapes made in the 2016–2017
expeditions (Svasyan et al., 2017) allowed to dis-
tinguish between two fundamentally dierent bot-
tom biotopes: soft sediments and bench (Fig. 3A).
The distribution of soft sediments within the inves-
tigated water area ranged from 17 to 52 m. The
bottom sediments at depths of 20–25 m were rep-
resented by pure black terrigenous sand; at depths
of 30–40 m by sand with an admixture of silt;
and at a depth of 50 m and deeper by silt. The
content of silty fractions (less than 0.1 mm) varied
with depth from 31.8% to 99.1%. At the 50 m hori-
zon, the silty fractions were mainly represented by
pelite (less than 0.01 mm, up to 82.7%). Fine sand
fractions dominated at shallow depths where they
comprised up to 84.3%.
The hard bottom biotope of the northern part is
represented by a section of a bench formed by an al-
most undamaged ysch. It forms horizontal, slightly
inclined steps with a few stone blocks on the sur-
face. The eastern part of the area is composed by a
landslide body formed by blocks and boulders, their
roundness decreases with depth. Bulks of coarse
material form a labyrinth of at sites, steep slopes
(20° and more), and sedimentary traps, which are
local depressions lled with sandy and silty sedi-
ments together with rocky material (Fig. 3B).
Based on the analysis of aerial photography of
the coastline sector of the reserve and its vicinities
(from the cli to a depth of 1.5 m, 3979 m in length),
two types of biotopes were identied: boulder and
block areas (total length 1248 m) associated with
capes and pebble and boulder concave sections of
the shore (2731 m). Boulder and pebble deposits ex-
tend to a depth of 2–4 m (Svasyan et al., 2017).
Nature Conservation Research. Заповедная наука 2018. 3(4): 1–16 DOI: 10.24189/ncr.2018.065
6
Thus, the northwestern part of the reserve’s ma-
rine area is a biotopical representative of the area of
the Black Sea Mountain Range (from Anapa to Tua-
pse). However, biotopes of accumulative shores and
adjacent underwater slopes with agglomeration of
shells and clay outcrops (widespread south of Cape
Idokopas) are not represented here. The main dier-
ence between the soft sediments of the reserve and
the more southern parts of the coast is the presence
of a sand belt to 30 m depth both in historical and
in recent time (Chestin, 2009; Chikina, 2009; Koly-
uchkina et al., 2017c). According to Kiseleva (1981),
in the mid-20th century, sandy sediments with a very
small admixture of silt (up to 3%) predominated at
depths of 10–30 m along the whole coastline. Thus,
the marine part of the Utrish Nature Reserve is a
unique area that apparently retained siltation at the
mid-20th century level and was not subjected to eutro-
phication at the end of the 20th century. Perhaps this
is due to the general pattern for the Black Sea, when
«opposite large capes with steep slopes of the shelf,
the sands descend to greatest depths» (Barkovskaya,
1961), associated with intense hydrodynamics and
the absence of a constant freshwater outow.
General characteristics of macrozoobenthos
According to our data, 74 species of higher mac-
rozoobenthos taxa were found at the ve stations in
the Utrish Nature Reserve. The expected number of
species calculated using the Chao2 index was 106 ±
21. This value, however, is an underestimation, since
the identication of some organisms was possible
only up to their genus (Rissoa sp.), family (Edwardsi-
idae gen. sp.), class (Oligochaeta gen. sp., Turbellaria
gen. sp.), and type (Nemertea gen. sp.) level (Koly-
uchkina et al., 2017b). With a similar approach, 117
species (130 ± 8 being the expected number of spe-
cies) of invertebrates have been recorded at 32 sta-
tions to the south of the Abrau Peninsula. This is 11%
of the total number of benthic invertebrate species
for the northeastern coast of the Black Sea (Table 1).
Thus, the total number of species found in the reserve
was lower than in the southern part of the coast as a
whole. However, each separate transect in the south-
ern part of the coast had less species than the Utrish
Nature Reserve transect. In addition, a comparison of
macrozoobenthos diversity indices in the Utrish Na-
ture Reserve and the above mentioned regions shows
that, in general, the species richness in the reserve
is higher than in more southern regions (Table 1). It
also turned out to be higher than the average along the
coast found in 2001 (Chikina, 2009).
Presentability of contemporary biocoenoses
Biocoenoses recorded in the area of the Utrish Na-
ture Reserve in 2016 were also found at all transects
south of the Abrau Peninsula in the current period, but
in the area of the reserve they were shifted to greater
depths. Along the coast from the Golubaya Bay to
Shepsi village Chamelea gallina community occurred
Fig. 3. A: Main types of acoustic signal of side-scan sonar and their preliminary interpretation (after Svasyan et al., 2017) for the
western part of the Utrish Nature Reserve marine area: 1 – section of the bench, with an intact structure; 2, 3 – boulder deposits;
4 – boulder deposits, possibly covered by soft sediments; 5 – presumably soft sediments; 6 – gravel/pebble; 7 – sand/silt; 8 – loca-
tion and depth of points of the long-term monitoring transect. B: Map of the slopes of the bottom of the investigated marine area.
The higher the bottom slope value for a pixel (the lighter the pixel), the greater the angle of slope at a given point.
Nature Conservation Research. Заповедная наука 2018. 3(4): 1–16 DOI: 10.24189/ncr.2018.065
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at depths of up to 15 m (shallow-water community),
and Pitar rudis Gouldia minima (Montagu, 1803)
Anadara kagoshimensis – at depths of 20–30 m
(medium-depth community). But in the Utrish Nature
Reserve’s marine area Chamelea gallina was found
to be a dominant at 20–25 m depths, and codominant
in Chamelea gallina Gouldia minima Pitar rudis
community at 30–40 m depths. The coldwater species
communities with a dominance of Parvicardium sim-
ile (Milaschewitsch, 1909) and Modiolula phaseolina
were noted at depths of 40 m and more in the southern
areas (the deep-water complex) (Fig. 4B). In the Utrish
Nature Reserve the P. simile community was found at
50 m depths, and the M. phaseolina community was
not found in the studied area (up to 52 m) (Fig. 4A).
In the shallow-water complex («venus sand»),
28 species were noted in the reserve (about 22 per
station), whereas in the remaining transects this num-
ber ranged from 24 to 46 species (76 in total, 27 per
station, on average). There were 25 species common
between the stations in the reserve and in the southern
part of the coast as a whole (32% of the total num-
ber of species in the community), and 14–21 species
were common between the Utrish Nature Reserve
transect and Golubaya Bay, Inal Bay and Shepsi tran-
sects (southern, or reference, transects, hereinafter)
separately. Thus, in the Utrish Nature Reserve marine
area this community turned out to be relatively poor
compared to other transects. Among the species char-
acteristic of this community at all transects were Ma-
gelona rosea Moore, 1907, Donax semistriatus Poli,
1795 and Mytilus galloprovincialis. The main dier-
ence between macrozoobenthos of the Utrish Nature
Reserve in this zone was the absence of Lentidium
mediterraneum (O.G. Costa, 1830) and Amphibala-
nus improvisus (Darwin, 1854), abundant at all other
transects, and the presence of a characteristic species
Parthenina interstincta (J. Adams, 1797), that was
noted at these depths only in the reserve.
The remaining two communities found in the re-
serve exceeded those of reference transects both in
terms of number of species per sample and species
richness (Table 2). In the medium-depth communi-
ties, 61 species (about 45 species per station) were
recorded from the Utrish Nature Reserve transect,
while the reference transects contained 41–52 species
(79 species in total, about 29 per station). 43 species
(45%) were common between the Utrish Nature Re-
serve and the southern part of the coast as a whole,
31–34 species were common between the reserve and
each reference transect separately. The greatest spe-
cies diversity in the reserve was in this community,
considerably exceeding the diversity of the refer-
ence transects. Prionospio multibranchiata Berkeley,
1927, Apseudopsis ostroumovi Bacescu & Carausu,
1947 and Gouldia minima were characteristic spe-
cies of this complex in general, while the polychaetes
Leiochone leiopygos (Grube, 1860) and Sigambra
tentaculata (Treadwell, 1941) were typical of the ref-
erence transects, not of the reserve.
Table 1. Species diversity of macrozoobenthos in dierent regions of the Black Sea in the 21st century
Character
Caucasian Black
Sea coast species list
(Volovik et al., 2010)
North-Caucasian
Black Sea coast, 2001
(Chikina, 2009)
Golubaya
Bay – Shepsi,
2014–2017
Utrish Nature Reserve,
2016
Number of stations 3032 5
Species number per station 14–35 12–38 22–53
Shannon diversity index 0.1–2.8 1.0–2.6 1.5–2.0
Margalef’s species richness 1.6–5.1 1.69–6.0 4.1–7.6
Species number: total 1032 81 117 74
Anthozoa 11 132
Nemertea 47 1* 1* 1*
Turbellaria 151 1* 1*
Oligochaeta 78 1* 1*
Polychaeta 204 28 54 24
Loricata 3 – – –
Bivalvia 92 17 16 15 (1)
Gastropoda 161 6 16 8 (2)
Crustacea 272 23 27 19 (6)
Ostracoda 117 – 17
Phoronida 31 1 1
Echinodermata 10 2 1 1
Chordata 10 2 1 1
Note: * – organisms were not identied to species level; number of species found in 2016 on rocky substrates are given in
brackets.
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Fig. 4. Scheme of the current location of macrozoobenthos
communities along the northeastern coast of the Black Sea.
A: Utrish Nature Reserve macrozoobenthic transect; B: Inal
Bay, Shepsi and the Golubaya Bay macrozoobenthic tran-
sects (adopted from Kolyuchkina et al., 2017c).
Fig. 5. Funnel plots of taxonomic distinctiveness of the
Utrish Nature Reserve transect’s macrozoobenthos against
that of the reference transects. (A) Delta+, average taxonom-
ic distinctiveness (avTD); (B) Lambda+, variation of avTD.
Table 2. Biodiversity indices of macrozoobenthos communities located at shallow (10–15 m), medium (20–30 m) and deep-
water complexes (40–50 m). For the area of the Utrish Nature Reserve, the ranges of 20–25 m, 30–40 m and 50 m, respec-
tively, are considered
Area S d J’ H’ (loge)Delta
Shallow-water complex
Utrish 22.5 ± 0.7 4.193 ± 0.071 0.5212 ± 0.0079 1.623 ± 0.041 42.65 ± 0.76
Golubaya Bay – Shepsi 26.7 ± 7.9 4.450 ± 1.195 0.4986 ± 0.0992 1.614 ± 0.371 38.74 ± 10.28
Medium depths’ complex
Utrish 45.5 ± 10.67.003 ± 0.875 0.5106 ± 0.0640 1.935 ± 0.124 51.46 ± 0.27
Golubaya Bay – Shepsi 29.3 ± 6.1 4.930 ± 0.659 0.6223 ± 0.0957 2.076 ± 0.257 54.63 ± 7.32
Deep-water complex
Utrish 32 4.955 0.4424 1.533 39.86
Golubaya Bay – Shepsi 20.7 ± 5.0 4.051 ± 1.236 0.6154 ± 0.0715 1.840 ± 0.068 50.09 ± 5.76
Note: S-species number, d – Margalef’s species richness, J’ – Pielou’s evenness, H’ – Shannon Index, Delta – taxonomic diversity.
In the deep-water community, there were 32
species at Utrish (18–23 species per sample),
while the other transects contained 28–38 species
(51 in total, 11–16 species per sample). Nineteen
species (30%) of them were common between
the reserve and the southern part of the coast as a
whole, and 14–15 species were common between
the Utrish Nature Reserve transect and each ref-
erence transect separately. It is likely that the re-
serve’s deep-water complex is considerably less
patchy in comparison, e.g., with that of the Gol-
ubaya Bay. At the Golubaya Bay transect, despite
the lower species number per sample, the total
number of species at 50 m was high due to sig-
nicant dierences between individual samples,
while at the Utrish Nature Reserve transect, with
its high similarity between individual samples,
the number of species per sample was higher. In
the deep-water complex, Terebellides cf. stroemi,
Parvicardium simile, Modiolula phaseolina and
Phtisica marina Slabber, 1769 were typical in the
reserve’s and reference transects.
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9
The only species common between all transects
and all depths is the polychaete Aricidea (Strelzo-
via) claudiae Laubier, 1967. In general, character-
istic species of the reference transects which were
absent or rare in the reserve, mostly included pelo-
philic forms. For example, the taxa Heteromastus
liformis (Claparède, 1864) and Nemertea gen. sp.
were found abundantly throughout the southern
part of the coast, but were absent in the shallow-wa-
ter complex at the Utrish Nature Reserve transect.
Species characteristic for both the shallow and the
medium-depth communities in both reference and
reserve’s transects mostly included bivalves. Be-
sides the dominant Chamelea gallina, they includ-
ed Lucinella divaricata (Linnaeus, 1758), Anadara
kagoshimensis, Fabulina fabula (Gmelin, 1791),
and Spisula subtruncata (da Costa, 1778). In ad-
dition, the polychaete Nephtys cirrosa longicornis
Jakubova, 1930, phoronid Phoronis psammophi-
la Cori, 1889 and amphipod Ampelisca diadema
were characteristic for these horizons. However,
the abundant species Melinna palmata Grube,
1870, that was common in the southern part in the
shallow- and medium-water communities, was
absent at the Utrish Nature Reserve transect. The
polychaete Eunereis longissima (Johnston, 1840)
and bivalve Abra alba (W. Wood, 1802) were typi-
cal in the complexes of medium and large depths
at both reference and reserve’s transects. Oriopsis
armandi (Claparède, 1864) and Pitar rudis were
abundant in these complexes along the southern
part of the coast, but were absent in the deep-water
complex in the Utrish Nature Reserve. The absence
of some abundant species in the Utrish Nature Re-
serve’s macrozoobenthos could be explained by a
low stations’ number sampled here to date.
A comparative analysis of the structure of mac-
rozoobenthos communities showed that, despite the
dierence in depth of the communities in the Utrish
Nature Reserve and the southern part of the coast,
the structure of macrozoobenthos within each com-
plex turned out to be similar. A comparison of the
macrozoobenthos structure in both areas by the den-
sity/biomass using the ANOSIM method has shown
that grouping of stations by region, both between
transects in general and between certain communi-
ties, was unreliable. The Taxonomic Distinctiveness
Test has shown no signicant dierences between
the study areas either (Fig. 5). Although the number
of species per station was signicantly larger in the
reserve compared to the other transects, the average
taxonomic diversity (avTD) and its variation in the
reserve were within the 95% condence interval for
the region. Again, the SIMPER method did not al-
low the identication of species with reliably high
contribution to the dierences between Utrish and
the rest of transects. The average dissimilarity val-
ues did not exceed 4–5, and their ratio to standard
deviation did not exceed 1.5 for the rst 1–3 species.
For most species this ratio was or less than 1. Thus,
the species diversity of the Utrish Nature Reserve
communities is typical for the narrow northeastern
shelf of the Black Sea.
The following feature should be noted for all
transects: higher values of «straight» diversity indi-
ces (S, d) correspond to relatively smaller values of
evenness and indexes that rely on it (J’, H’). For ex-
ample, Utrish is characterised by a smaller number
of species and species richness values in the «venus
sand» community compared to other transects, but
higher values in the medium- and deep-water com-
plexes. On the contrary, Pielou’s evenness and Shan-
non index are higher in the «venus sand» commu-
nity of the Utrish transect, while their values in the
other two Utrish transect’s complexes are relatively
low compared to the southern transects. Another
point to be noted is the low value of the taxonomic
diversity (Delta+) in the deep-water complex, which
indicates a large number of taxonomically related
species or a low number of higher taxa present.
Thus, only two of the three contemporary com-
munities are fully represented in the reserve marine
area, but most of the characteristic macrozooben-
thos species corresponded with species present on
the southern part of the coast. An extension of the
reserve marine boundary over the 70 m isobath in
order to include the Modiolula phaseolina biocoe-
nosis would signicantly increase the presentabil-
ity of the protected sea zone.
Temporal dynamics of the structure of the soft
sediments’ communities
Three communities have been recorded for the re-
serve’s marine zone: (1) sand dominated by the bivalve
Chamelea gallina at 20–25 m, (2) silted sand with
shells dominated by the pelophilic bivalves Pitar rudis
and Gouldia minima and the polychaete Aricidea clau-
diae at 30–40 m, and (3) silt (pelite) dominated by the
bivalve Parvicardium simile at 50 m (Fig. 4A). Only
one of these communities, the «venus sand» biocoe-
nosis, proved to be stable over time: in the 20th century
(Zernov, 1913; Kiseleva & Slavina, 1965; Alekseev
& Sinegub, 1992), at the early 21st century (Chestin,
2009), as well as in 2016, the bivalve Ch. gallina was
dominant here at depths of 20–25 m. The deeper faunal
complexes changed over time. The community of the
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10
silt mussel (Mytilus galloprovincialis) occupied depths
of 30–50 m in the 20th century; it was also noted here
in 2001 (Chestin, 2009). In 2016, the mussel commu-
nity was not observed at any of the investigated depths.
Mytilus galloprovincialis itself was recorded as a sin-
gle juvenile specimen at the depth of 40 m in the P.
rudis – G. minima community. Both of these species
were subdominant in the mussel community in the 20th
century. It should be noted that the mussel zone was
not observed at any of the southern transects in 2014–
2017 either. The problem of the dynamics of the mus-
sel zone in the 21st century has not been suciently
studied, but there is a suggestion that its degradation in
the northern Caucasus may be associated with the silt-
ation of sediments due to the intensive bottom trawling
and the impact of dumping (Zaika et al., 1990). Be-
sides that, the distribution of this community could be
patchy: for example, in the 20th century in the Tuapse-
Shepsi region, the mussel community did not form a
single belt, but was recorded only at part of the 30–50
m depth stations studied (Kiseleva & Slavina, 1972).
Another characteristic Black Sea community
was not observed in the area of the reserve in 2016:
a belt of pelite dominated by Modiolula phaseo-
lina, recorded in this area in the 20th century. (Zer-
nov, 1913; Kiseleva & Slavina, 1965; Alekseev
& Sinegub, 1992). At a depth of 50 m, where the
deep-water boundary of the reserve is located, the
community of the bivalve Parvicardium simile was
noted in 2016. Modiolula phaseolina was found
only as a minor species. However, it is known that
this community occupies greater depths (70 m and
deeper) in the vicinities of the reserve, as shown
by the South Stream studies (ESIA Russian Sector,
2014) and by the 1999–2001 surveys carried out
directly in the area of the reserve (Chestin, 2009).
Thus, the M. phaseolina community is more likely
to be located deeper than 50 m in the reserve area,
so it is desirable to extend the marine boundaries of
the reserve to at least 70 m isobaths to increase the
presentability of its bottom biocoenoses.
Benthic communities with domination of the in-
vasive species Rapana venosa (Valenciennes, 1846)
and Anadara kagoshimensis, which played an impor-
tant role in the dynamics of macrozoobenthos in the
early 21st century, were not observed in the marine
area of the reserve neither in 2001 nor in 2016 (Ches-
tin, 2009; Chikina, 2009). While A. kagoshimensis
was recorded as a rare species here in 2016, R. ve-
nosa was not found in any sample at all. However, in
2001 A. kagoshimensis was among the dominant spe-
cies at depths of 30–35 m near Southern Ozereyevka,
which is only a little way to the south (Chestin, 2009).
Therefore, it is possible, that these biocoenoses will
be found in the southeastern sector of the marine part
of the reserve, which currently remains unexplored.
General characteristics of macrophyte ora
The preliminary ora of the Utrish Nature Re-
serve includes 33 species (belonging to 12 orders, 17
families, 21 genera) (Kolyuchkina et al., 2017b). In
terms of seaweed biogeography, the ora of the re-
serve contained mainly warm-temperate species (20
species or 71% of total). The cold-temperate group
included only two species (7.14%). The temperate
species made up a more diverse group consisting of
six species (21%). One species was a cosmopolite.
Obviously this rst recent survey performed in
one season contained too low data to access the pre-
sentability of the whole Utrish Nature Reserve ma-
rine area when compared to approximately equal
in size samples from other areas of the coast (Table
3). However, the species ratio mainly reected the
biogeographical composition of the region. Thus,
contemporary data (Kolyuchkina, 2017b) for the
Utrish area were consistent with what has been
previously published (Lobkovskiy et al., 2001).
The new alien species Bonnemaisonia ham-
ifera Hariot was found in the reserve’s marine
area. In all samples, only thalli of the tetrasporo-
phytic phase of B. hamifera were found (Simakova
& Smirnov, 2017). Its native range is the warm
temperate area of the Pacic Ocean (Perestenko,
1994). Since the 19th century it became invasive in
the north Atlantic and the Mediterranean (Boudour-
esque & Verlaque, 2002; Streftaris et al., 2005).
General characteristics of macrophyte vegetation
In general, the macrophyte zone consists of
four belts: upper (0–2 m), upper mid (2–12 m),
lower mid (12–18 m), and the lower belt (below
18 m) formed by the alien species Bonnemaisonia
hamifera (Simakova et al., 2017).
The bottom of the upper macrophyte zone habi-
tat (0–2 m) was composed of boulders and pebbles
of various forms and sizes (from 10 cm to 50–70
cm). Communities found here were formed by an-
nual algae from the association Dictyota fasciola f.
repens + Polysiphonia opaca + Ceramium ciliatum
+ Ulva compressa (according to the classication
of Kalugina-Gutnik, 1975). The oristic composi-
tion of this association was signicantly reduced and
represented by two species: Padina sp. and Dictyota
fasciola (Roth) J.V. Lamouroux. The coverage of the
vegetation varied signicantly from individual thalli
per m2 to 30–50% of surface (Simakova et al., 2017).
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Table 3. Macrophyte oristic composition of the Utrish Nature Reserve compared to other areas of the North Caucasian coast.
The present survey in bold
Region Number of samples
Total number
of macrophyte
species
Species number (% of survey total)
Rhodophyta Ochrophyta Chlorophyta Seagrasses
Cape Utrish vicinity (Lob-
kovskiy et al., 2001)
20 quantitative
+5 qualitative 48 29 (60.4%) 8 (16.7%) 11 (22.9%) 0
Utrish Nature Reserve
(Kolyuchkina et al., 2017b)
15 quantitative
+10 qualitative 33 15 (45.5%) 11 (33.3%) 7 (21.2%) 0
Inal Bay (Maximova,
unpublished)
16 quantitative,
4 qualitative 25 14 (56%) 6 (24%) 5 (20%) 0
Cape Doob (Mitjaseva et
al., 2003)
22 quantitative,
47 qualitative
60 35 (58.3%) 13 (21.7%) 12 (20%) 0
Golubaia Bay (Mitjaseva
et al., 2003) 31 19 (61.3%) 7 (22.6%) 5 (16.1%) 0 (0%)
Gelendjik Bay (Mitjaseva
et al., 2003) 14 6 (40%) 4 (26.7%) 4 (26.7%) 1 (3.8%)
Open coast of Tolstiy Cape
(Simakova, 2009) 12 qualitative 21 13 (61.9%) 5 (23.8%) 3 (14.3%) 0
Maria-Magdalena Bank
(Mitjaseva et al., 2003)
6 qualitative,
8 quantitative 41 19 (44.2%) 11 (25.6%) 11 (25.6%) 2 (7.8%)
Coastal area from Tuapse
to Sochi (Lisovskaya &
Nikitina, 2007)
38 stations 61 30 (49.2%) 6 (9.8%) 23 (37.7%) 2 (5.3%)
North Caucasian coast (re-
gion in general) (Kalugina-
Gutnik, 1975)
About 2000 qualita-
tive and quantitative 135 80 (59.3%) 31 (23%) 22 (16.3%) 2 (12.3%)
Russian + Georgian coasts
(region in general)
(Milchakova, 2007)
183 92 (50.2%) 51 (27.9%) 40 (21.9%) No data
The depth range of 2–12 m was occupied by
communities of the association Cystoseira crinita
+ Cystoseira barbata – Cladostephus spongiosus
– Ellisolandia elongata (according to the classi-
cation of Kalugina-Gutnik, 1975). This syntaxon
is very common along the North Caucasian coast
and forms almost a continuous belt from Anapa
to Cape Idocopas (ca. 100 km) (Afanasyev 2005;
Lisovskaya & Nikitina, 2007; Milchakova, 2007).
Usually Cystoseira spp. communities found along
the North Caucasian coast are formed by four veg-
etation layers, including crustose algae which are
not considered here. The rst layer was 30–50
cm high and was dominated by Cystoseira crinita
and C. barbata. The latter could be codominant or
completely absent. The Cystoseira’s coverage was
high and could exceed 100%. The second layer
was formed mainly by Cladostephus spongiosus.
Its height was less than 20 cm and the coverage
was less than 50%. The third layer included usu-
ally several species, whose height was usually less
than 5 cm, such as coralline algae and Cladopho-
ropsis membranaceae (Simakova et al., 2017). An
important element of the Cystoseira spp. associa-
tions’ structure was the presence of epiphytes with
a high species number and biomass (Kalugina-
Gutnik, 1975; Simakova, 2011).
The coverage of Cystoseira spp. was high in
the reserve during the sampling period (30–80%).
The coverage maximum has been found at depths
of 6–10 m at dierent sites. The structure of com-
munity layers was reduced. Plants of the second and
the third layers were sparse. Only at a depth more
than 6–7 m, the invasive Bonnemaisonia hamifera
(a low plant of up to 2–3 cm high) formed spots
with a high percentage of coverage. At depths of 10
m and more the proportion of plants of the second
layer increased due to the deep-water Rhodophyta
species Phyllophora crispa. The most abundant
epiphytes were red algae: Polysiphonia subulifera
and Bonnemaisonia hamifera (Simakova et al.,
2017). The other ve epiphyte species were rare.
The third deeper belt of bottom vegetation
was formed mainly by three species: Phyllopho-
ra crispa, Codium vermilara and Bonnemaisonia
hamifera. The rst two species might form not
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12
only mixed beds but monodominant communities
as well. It seems that these algae are being over-
grown by B. hamifera. This may lead to signicant
changes in the distribution of native species.
Tetrasporophytes of Bonnemaisonia hamifera
were found for the rst time as mass aggregations
of unattached thalli over an area with soft bottom at
17–40 m depths (Simakova et al., 2017; Simakova
& Smirnov, 2017). Later it was found that this spe-
cies was not only present in native communities as
epilithic vegetation or epiphyte, but also occupied
any vacant substrate especially in the zone deeper
than 6–7 m. It was one of the dominant species (in
terms of % coverage) in the lower zone. In addition
to that, it fully covered hard bottom substrates at
depths more than 18 m which became bare after the
reduction and shift of native vegetation (Maximova
& Luchina, 2002; Simakova & Maximova, 2009).
Presentability of contemporary macrophyte
communities
Preliminary data on the oristic composition
in the reserve’s marine area indicate that it is in-
habited by macrophyte species common for the
North Caucasian coast. The species list comprises
only 24% of regional ora. However, this number
will probably increase with further research.
The majority of species found in the reserve’s
marine area were common species of the Black Sea
macrophytobenthos; on the other hand, some spe-
cies, which are widely distributed along the Cau-
casus coast, were not found here. For example, El-
lisolandia elongata (J. Ellis & Solander) K.R. Hind
& G.W. Saunders, Ceramium ciliatum (J. Ellis) Du-
cluzeau, Gelidium crinale (Hare ex Turner) Gaillon,
Polysiphonia elongata (Hudson) Sprengel and some
others were not found in the Utrish Natural Reserve.
Another very important group, which was not
present in the reserve’s marine area, is the sea-
grasses. Both species of Zostera are not very com-
mon in the North Caucasian region. Zostera noltei
Hornem. meadows are found on sandy shallows in
the inner part of the Gelendjikskaya Bay. Zostera
marina L. forms meadows to the north of Anapa.
Both species are also known from the south of
Tuapse (Milchakova & Phillips, 2003). Zostera is
a genus of ecosystem engineer species that plays
a key role in many regions around the globe. The
habitats that they require (sandy and muddy shal-
lows) are absent in the studied area.
Since the marine area of the reserve is situ-
ated on an open coast, its waters are quite clean.
During the surveys in 2016–2017 no evidence
of anthropogenic suppression of dominant algae
populations, in comparison to other regions, could
be found. At the same time, a reduced structure of
layers of the Cystoseira spp. community and a less
epiphyte diversity, compared to the descriptions of
a typical community of this kind, was found. Such
reduction is typical for areas where a large amount
of soft sediments cover hard bottom substrates. It
usually occurs to the south of Tuapse (Kalugina-
Gutnik, 1975). The same reduction of the com-
munity structure appears in areas where the hard
bottom relief is not very diverse (such as along the
open coast of the Cape Tolstiy) (Simakova, 2009).
The vicinity of the Cape Utrish is traditionally
considered to be an area of the clearest water and
least aected communities of macrophytobenthos.
According to the published data, Cystoseira barbata
occurred here in the 20th century up to a depth of 32
m (Kalugina-Gutnik, 1975). Such depth distribution
was considered to be an absolute record for the So-
viet sector of the Black Sea. To date, normal thalli
of Cystoseira crinita and C. barbata are found in the
reserve’s marine area down to 12 m and, apparently,
deeper. This exceeds the recent depth range of these
species along the coast to the south of the Abrau
Peninsula which has a similar to Ultrish depth dis-
tribution of hard bottom. For example, only dwarf
thalli of C. crinita are found at 10 m depth near the
Golubaya Bay (Simakova, 2011). The other species,
С. barbata, occurs there slightly deeper (12 m) but
also in a form of dwarf thalli. The same pattern was
observed by other authors (Blinova et al., 1991; Af-
anasyev, 2008). This proves that the Utrish Nature
Reserve includes more favourable habitats for mac-
rophytes compared to other areas. In contrast, no na-
tive macrophytes were found at depths greater than
18 m (Simakova & Smirnov unpublished), which
corresponds to earlier data (Lobkovskiy et al., 2001).
That is smaller depth compared to the other areas of
the Caucasian coast such as mentioned above (23
m) (Simakova, 2011). This indicates the result of the
Black Sea ecosystem’s anthropogenic transforma-
tion, which has a signicant eect on macrophytes
even in such a clear area.
Conclusions
It is apparent that such a small marine area
cannot contain all the diversity of the Black Sea
biotopes and associated benthic species. However,
currently the biocoenoses of the reserve can be la-
beled as typical for the northeastern coast of the
Black Sea. The area under study includes habitats
that are common along the whole coast (an active
Nature Conservation Research. Заповедная наука 2018. 3(4): 1–16 DOI: 10.24189/ncr.2018.065
13
cli, a narrow pebble beach, a boulder bench and
soft sediments). Of the most typical ones, only
biotopes of accumulative banks, shells, clays and
near-estuarine bottom landscapes have not been re-
corded. Unlike most areas of the North Caucasian
coast, the relief in the reserve is signicantly com-
plicated by landslide structures of dierent ages.
High species diversity of benthos on soft and rocky
bottom makes it possible to consider the ecosystem
of the reserve as a source of macrozoobenthos spe-
cies for the northeastern coast of the Black Sea.
The macrozoobenthic species diversity of the
reserve was equal to or higher than the other inves-
tigated sites of the North Caucasian coast. The mac-
rozoobenthic communities present within the Pro-
tected Area on soft and rocky bottoms had a similar
structure to those of the southern part of the North
Caucasian coast. Presently, three types of macrozoo-
benthos biocoenoses with dominant bivalve mollusks
were found on soft sediments in the reserve: (1) sand
with dominance of Chamelea gallina, (2) silted sand
dominated by Pitar rudis and Gouldia minima, (3)
silt dominated by Parvicardium simile. The low silt-
ation level of sediments at depths of 20-25 m and the
small role of macrozoobenthic invasive species make
the faunistic complex of these depths within the re-
serve area unique, preserving nearly unchanged from
the middle of the 20th century. Some of the known
biocoenoses were not found in the Protected Area:
Mytilus galloprovincialis silt and Modiolula phaseo-
lina silt. The former was not found due to the absence
of appropriate biotopes, but the rst one was not
noted at any site along the North Caucasian coast in
recent time; this could be a consequence of the whole
Black Sea ecosystem’s transformation in the late 20th
– early 21st century. Thus, only two of the three con-
temporary communities are fully represented in the
reserve marine area, but most of the characteristic
macrozoobenthos species correspond with species
present in the southern part of the coast. An extension
of the reserve’s marine boundary over the 70 m iso-
bath, thus including the M. phaseolina biocoenosis,
would signicantly increase the presentability of the
protected marine territory. Further studies are needed
to conrm this observation.
The rocky biotope was dominated by macroal-
gae Cystoseira spp., which are the common spe-
cies throughout the Black Sea coast of the Cauca-
sus. The species number recorded to date was not
very high. The species diversity of the ora in the
reserve was close to that of the other areas of the
coast (Table 3), taking into account the sampling
eort. However, as further research improves the
reserve’s macrophyte species list, it will obviously
reach values typical for the region or possibly ex-
ceed them. This is supported by the fact that in the
area of the reserve, the lower boundary of the main
macrophyte dominant species’ (Cystoseira spp.)
habitat descends signicantly lower than in the
southern regions of the coast. The vegetation of the
reserve turns out to be representative of the North
Caucasian Coast in terms of communities’ diver-
sity. At the same time, Zostera spp. were not repre-
sented here. These very important macrophytes are
very sparse along the Caucasian coast.
Acknowledgments
This study was conducted with the permission and assis-
tance of the Utrish Nature Reserve administration. The authors
are grateful to the heads of the Utrish Nature Reserve for the
opportunity to work in the protected water area, as well as to
colleagues from the Centre for Marine Studies of the Lomono-
sov Moscow State University for sonar photography and aerial
photography. We are also thankful to I.A. Smirnov and V.G.
Papunov for the organisation of diving work and to the chil-
dren of school №171 G.O. Babich, A.I. Rokova, I.V. Mironen-
ko for the assistance in the collection and analysis of algae.
The work was supported by the Program of the Presidium of
the Russian Academy of Sciences I.49 «Interaction of physi-
cal, chemical and biological processes in the World Ocean»,
topic 0149-2018-0033 / 6 (IO RAS) and by the research topic
of the SSC RAS «The current state and long-term variability
of the coastal ecosystems of the southern seas of Russia», state
reg. 01201363187.
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РЕПРЕЗЕНТАТИВНОСТЬ БЕНТОСНЫХ СООБЩЕСТВ
ПРИРОДНОГО ЗАПОВЕДНИКА УТРИШ
ДЛЯ СЕВЕРО-КАВКАЗСКОГО ШЕЛЬФА ЧЕРНОГО МОРЯ
Г. А. Колючкина1,*, В. Л. Семин2,**, У. В. Симакова1, В. О. Мокиевский1
1Институт океанологии имени П.П. Ширшова РАН, Россия
*e-mail: galka.sio@gmail.com
2Федеральный исследовательский центр Южный научный центр РАН, Россия
**e-mail: semin@ssc-ras.ru
Была проведена оценка репрезентативности биотопов и бентосных сообществ северо-западного участ-
ка природного заповедника Утриш для северокавказского побережья Черного моря. Для осуществления
поставленной цели были привлечены как собственные, так и литературные данные по состоянию бенто-
са. Изученный район природного заповедника Утриш включает местообитания, обычные для побережья
в целом (активный клиф, узкий галечный пляж, валунно-глыбовые навалы, бенч и рыхлые осадки). Из
трех широко известных черноморских поясных макрозообентосных биоценозов на северо-восточном
побережье Черного моря было отмечено только два: мелководный «венусовый песок» и глубоководный
«фазеолиновый ил». Третий биоценоз («мидиевый ил») не был отмечен ни на акватории заповедника,
ни на обследованной части шельфа южнее Новороссийска. Из этих трех поясов только «венусовый пе-
сок» был отмечен на акватории природного заповедника Утриш. Отсутствие мидиевого пояса на иссле-
дованной акватории заповедника было типичным явлением для южной части северокавказского побере-
жья в современный период, и, таким образом, не оказывало влияния на репрезентативность бентосных
экосистем заповедника. Биоценоз двустворчатых моллюсков Pitar rudisGouldia minima был обычен
на заиленных песках с ракушью как в заповеднике, так и на контрольных участках комплекса средних
глубин, замещая мидиевый пояс, который был типичным в 20 в. Его граница проходила на 10 м глубже
в заповеднике по сравнению с контрольными районами. Отсутствие пояса Modiolula phaseolina на ак-
ватории заповедника может объясняться недостаточной протяженностью охраняемой морской террито-
рии (только до 52 м по глубине); из-за этого глубоководный комплекс в заповеднике в настоящее время
представлен только узкой зоной. Расширение границ заповедника до глубин 70 м позволит включить в
охранную зону и этот биоценоз, что значительно повысит репрезентативность морской зоны заповед-
ника для северокавказского побережья Черного моря. Биогеографический состав флоры заповедника, ее
видовое разнообразие и структура в целом соответствуют таковым для региона. Зона макрофитов состо-
ит из четырех поясов: верхний пояс (0–2 м, Dictyota fasciola f. repens + Polysiphonia opaca + Ceramium
ciliatum + Ulva compressa), верхний горизонт среднего пояса (2–12 м, Cystoseira crinita + Cystoseira
barbata – Cladostephus spongiosus – Ellisolandia elongata), нижний горизонт среднего пояса (12–18 м,
Phyllophora crispa, Codium vermilara and Bonnemaisonia hamifera) и нижний пояс (глубже 18 м), образо-
ванный недавним вселенцем B. hamifera. Большинство видов, найденных в морской части заповедника,
были обычными видами черноморского макрофитобентоса. Однако природный заповедник Утриш яв-
ляется более благоприятным местообитанием для макрофитов, чем другие районы северокавказского
побережья, поскольку обычный для побережья макрофит Cystoseira spp. был отмечен в заповеднике на
больших глубинах, чем на остальном шельфе.
Ключевые слова: биотопы, биоценозы, макрозообентос, макрофитобентос, морской заповедник
Nature Conservation Research. Заповедная наука 2018. 3(4): 1–16 DOI: 10.24189/ncr.2018.065
... До Чорного моря, де гаметофіти досі не виявлені, вид проник на початку 2010-х років (Spiridonov et al., 2020), а в середині десятиліття вже зареєстровано спалах його розвитку біля кавказького узбережжя (Simakova, Smirnov, 2017;Kolyuchkina et al., 2018). З 2017 р. спостерігається масова інвазія в природні фітоценози біля ПБК . ...
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As a result of the monitoring studies based on the materials from 2019, six new species of macroalgae were identified for the marine area of the Nature Reserve «Cape Martyan», located on the Southern Coast of Crimea (SCC): Bolbocoleon piliferum Pringsh., Giraudia sphacelarioides Derbès et Solier, Myrionema balticum (Reinke) Foslie, Lithophyllum cystoseirae (Hauck) Heydr., Bonnemaisonia hamifera Har., Choreonema thuretii (Bornet) F.Schmitz (the latter two species were recorded for the hydrobotanical region «Southern Coast of Crimea» for the first time). As a result, the list of marine macrophytes within the boundaries of the Nature Reserve now includes 160 species and intraspecific taxa at the species rank, which consist about 36% of the total number of macrophytes identified in the Black Sea. Thus, the protected water area near the Cape Martyan continues to function as one of the key refugia for natural phytodiversity in the region. At the same time, B. hamifera is an invasive transforming species that has recently invaded the SCC region. This is a threat to the ecosystem of the Nature Reserve, and in the nearest future the invasion may cover the entire Northern Black Sea region. Thus, on the one hand, the results of the study expand the understanding of the level of natural phytodiversity of the reserve, the hydrobotanical region and the region as a whole, but on the other hand – they indicate the problem of developing biological invasion, which, under the conditions of the isolated Azov-Black Sea basin, can have catastrophic consequences.
... In the Black Sea, there are approximately 63 MPAs (Milchakova et al., 2015;Alexandrov et al., 2017;Begun et al., 2012Begun et al., , 2022. Phyllophora crispa was found within 30 of them situated in Bulgaria, Romania, Russia, and Ukraine; moreover, some MPAs have been established specifically to protect this species (Tkachenko & Maslov, 2002;Tkachenko & Kovtun, 2014;Milchakova et al., 2015;Skrebovska & Shaposhnikova, 2016;Kolyuchkina et al., 2018;Abaza et al., 2019). The effectiveness of MPAs in the conservation of P. crispa has been assessed to date along the Bulgarian coast only, based solely on the data of their connectivity (Berov et al., 2018). ...
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... However, the first objective gets much more attention and number of studies (e.g. Martinez et al. 2006;Pawar et al. 2007;Ruchin & Egorov 2017;Kolyuchkina et al. 2018), although estimation of qualitative biodiversity patterns is not less important in the line of nature conservation. In most cases, the studies resulted in conclusions about inefficiency of protected area networks in different regions worldwide (e.g. ...
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