1. No category

Research Article
ISSN 2336-9744 (online) | ISSN 2337-0173 (print)
The journal is available on line at www.ecol-mne.com
Deep - water hypoxic meiobenthic Protozoa and Metazoa taxa of the
Istanbul Strait’s (Bosporus) outlet area of the Black Sea
NELLI G. SERGEEVA1* & SOFIA A. MAZLUMYAN2
1
Institute of Marine Biological Research Russian Academy of Sciences, 2, Nakhimov ave., Sevastopol 299011, Russia.
E-mail: [email protected]
2
Institute of Natural & Technical Systems Russian Academy of Sciences, 28, Lenin str., Sevastopol, 299011, Russia.
E-mail: [email protected]
Received 8 May 2015 │ Accepted 22 May 2015 │ Published online 26 May 2015.
Abstract
The purpose of these investigations was to understand the response of different meiobenthos taxa on the oxygen
depletion in the habitat in the deep-water areas of the Black Sea. The results of first study were published in TrJFAS
(Sergeeva et al. 2013) and were devoted to vertical distribution of the deep-sea meiobenthic communities. This article
includes a historical overview of research dedicated to meiobenthos and represents first detailed quantitative analysis of
taxonomic composition and vertical distribution of main taxa of meiobenthos in the Istanbul Strait’s (Bosporus) outlet
area of the Black Sea along the transition from oxic to anoxic conditions, where the sinking water is in contact with the
bottom. Nine stations were carried out in the Istanbul Strait’s outlet area of the Black Sea during 9th–21st November
2009 at the R/V ‘Arar’ cruise from the Istanbul University. The abundance and vertical distribution of main taxa of
Protozoa (Ciliophora, Gromida and Foraminifera) and Metazoa (Nematoda, Polychaeta and Harpacticoida) on the Black
Sea shelf and the upper slope area (75–300 m depth water) were studied. Meiobenthos was present at all investigated
depths and included 21 taxa. Gromiids, hard-shell foraminifera and polychaetes were found at depths between 75–250
m, Ciliophora, soft-shelled foraminifera and nematodes were found at depths between 75–300m. Our data suggest that
some benthic eukaryotes (protozoa and metazoa) can tolerate anoxic and sulfidic conditions of the Black Sea.
Key words: Ciliophora, Gromida, Foraminifera, Nematoda, Polychaeta, Harpacticoida, abundance trends, depth
gradient, sediment layers habitat versatility.
Introduction
This work continues a series of studies on deep-water meiobenthos in the Istanbul Strait’s (Bosporus) outlet
area of the Black Sea, conducted within the framework of the EU 7th FP project HYPOX (In situ monitoring
of oxygen depletion in hypoxic ecosystems of coastal and open seas, and land-locked water bodies) EC Grant
226213. The aim of that study was ambiguous. Firstly, to understand the response of the benthic fauna on
oxygen depletion and secondly, to analyze the taxonomic composition and distribution of the benthic fauna
inhabiting the depth zone where the oxic/anoxic interface zone meets the sea floor.
Previous Studies
Pioneer studies of benthic fauna in the Bosporus outlet area were done in 1890, where new mollusks species
were discovered, previously not described for the Black Sea (Ostroumov 1893, 1894). In subsequent studies
the research interests were focused only on the macrobenthic component of bottom fauna (Zernov 1913;
Ecol. Mont., 2 (3), 2015, 255-270
DEEP-WATER PROTOZOA AND METAZOA OF THE BOSPORUS
Yakubova 1948). Size category of bottom fauna, called meiobenthos has not been studied until the twentieth
century. Meiobenthos embraces a set of microscopic benthic body of 0.1–1 mm size (Mare 1942). Some
authors considered 2 mm, as the upper dimensional criteria of meiobenthos (Chislenko, 1961a, 1961b). The
size composition of meiobenthos includes the permanent meiofauna (eumeiobenthos) and the temporary
meiofauna (pseudomeiobenthos), represented by the juvenile stages of macrobenthos (Chislenko 1961a).
At 1959 for the first time meiobenthic fauna was collected at Bosporus outlet area of the Black Sea.
At six stations in the western part of the Bosporus area Bặcesco & Mặrginneanu (1959) indentified and
described 20 species of meiobenthos that were not only new for the Black Sea, but also new for biological
literature. The presence of nineteen species of benthic foraminifera, three species of harpacticoids, three
species of ostracods has been documented (Bặcesco & Mặrginneanu 1959; Bặcescu 1960). Several ostracods
species specific only to the Bosporus outlet area of the Black Sea were described in the late fifties and early
sixties (Caraion 1959; Marinov 1962; Shornikov 1966).
In the sixties another research was focused on benthic foraminifera in the Bosporus area (depth 80–
100 m). Three main foraminiferan complexes were defined based on the dominant foraminiferan species.
The first complex, where species Streblus beccarii dominated was represented by six species, in the second
set (represented by 10 species) species of genera Ammobaculites are abundant and the third complex
consisted of a mixed thirty two species group (Didkowsky 1969). Subsequently at Bosporus outlet area
seventy nine species of benthic foraminifers have been discovered, comprising thirty nine genera and six
orders. Twenty seven new species were unique for the Bosporus area of the Black Sea (Yanko & Vorobyova
1991).
Additional studies dealing with benthic fauna in the Bosporus outlet area were performed by the
Department of Benthos of IBSS, during 1958, 1960 during RV ‘Academic Kovalevsky’ cruises at the
Bosporus area. By sampling a total of ten benthic stations at water depths of 70–113 m three ecological
communities were distinguished, namely Modiolula phaseolina, located to the north-east of the Bosporus
outlet area, and the ecological communities Sternaspis scutata and Amphiura stepanovi – Terebellides
stroemi located to the north-west of the Strait. In the Modiolula phaseolina community four higher taxa and
six species of meiobenthos were found. In the Amphiura stepanovi-Terebellides stroemi community also four
higher taxa and ten species of meiobenthos were found. In the Sternaspis scutata community seven species
of meiobenthos were found. In general, the meiobenthos included the following taxa: Nematoda,
Kinorhyncha, Polychaeta, Ostracoda, Harpacticoida, Acari. Nematodes as usual were the most numerous
taxa (Kiseleva 1969). The taxonomic analysis of sediment samples revealed 51 species of nematodes belong
to the thirty seven genera. Further on some species from Bosporus region were described as new to science,
among them there are Sabatieria praebosporica Sergeeva 1973, S. asperum Sergeeva 1973, Filoncholaimus
ponticus Sergeeva 1974, Parironus ponticus Sergeeva 1973, Halichoanolaimus lukjanovae Sergeeva 1973,
Mesacanthion heterospiculum Sergeeva1974, Crenopharinx brevicaudatus (Sch. Stekh.), Paramesacanthion
truncus Vitiello, Viscosia minudonta. Four species were found only on the shelf of the Bosporus area and the
two of them later were met in other parts of the Black Sea (Sergeeva 1973a, b, 1974, 1977).
In 1991 U. Luth (2004) presented results of investigations of meiofauna and macrofauna on transect
in the region Inebolu in the depth interval from 50 m to 250 m. Special interest was to set taxonomic
composition and distribution patterns of deep-water benthic communities inhabiting the layer where the
oxic/anoxic interface meets the sea floor. On the Inebolu transect the steep decline in number of taxonomic
groups occurred between 130 m and 150 m depth, already in the suboxic zone. Mobile forms with high
oxygen demands such as crustaceans or fish were restricted to this zone.
Pioneer studies of diversity and abundance of deep-water Tardigrada at the oxic/anoxic interface in
the Bosporus outlet area of the Black Sea were done by Kharkevych & Sergeeva (2013), where new
tardigrades species were discovered, previously not described for the Black Sea.
Brennan et al. (2013) presented first time data about meiobenthos composition on three stations in the
oxic/suboxic/anoxic interface of the Black Sea off Sinop. The highest total abundance of meiobenthos was
found in the oxic sediment core and the lowest in the anoxic core. The total number of individuals in the oxic
zone was approximately 200 times higher than the number of individuals found in the anoxic zone. The taxa
composition of meiobenthos on three sites ranged between 5 and 9 major groups. Meiofauna from the anoxic
sample includes representatives of only Nematoda, Acari, Harpacticoida and hard-shelled Foraminifera.
Nematoda dominated all three zones, followed by Harpacticoida in the oxic and suboxic zones.
Meiofauna from the anoxic sample includes representatives of only Nematoda, Acari, Harpacticoida
and hard shelled Foraminifera. The third prevalent group was Polychaeta in the oxic zone and Hydrozoa in
256
SERGEEVA & MAZLUMYAN
the suboxic zone. Kinorhyncha were recruited only from the oxic and suboxic zones. Turbellaria, Ostracoda
and Echinodermata were detected only in the oxic sample (Brennan et al. 2013).
There are significant variations of conditions in the Bosporus area caused by the fluctuation of the
lower flow of the Bosporus. This is reflected in the distribution of benthos, as shown, for example, in the
shift of the peak position in the settlement of the polychaetes Vigtorniella zaikai and Protodrilus sp.
(Sergeeva & Zaika 2013; Zaika & Sergeeva 2012)
There is the first information about the marine filamentous fungi of the deep soft sediments at the
transition zone from oxic to anoxic conditions (117.4–295.7 m water depths) in the Bosporus outlet area of
the Black Sea. The morphologic difference of filamentous mycobiota indicates to species diversity of fungi
in the extreme benthal conditions. Large accumulations of mycelium in the bottom sediments in Black sea
deep-water zone is the evidence of fungi habitation in the hydrogen sulfide zone (Sergeeva & Kopytina,
2014).
Systematic study of fauna from the deeper parts of the Black Sea began since start the EU projects
HERMES (2006–2009) and HYPOX (2009–20012). Two oceanographic expeditions were conducted to
survey fauna at the deep-water part in the outlet area of the Istanbul Strait’s (Bosporus) during cruises of the
RV ‘Arar ‘ (November 2009) and the RV ‘Maria S. Merian’ 15/1 (April–May 2010). During ‘Arar’ cruise
meiobenthos abundance and distribution on the Black Sea shelf and the upper slope area off the Bosporus
Strait outlet area were studied. This study represents the first detailed quantitative analysis of the structure
and distribution of meiobenthos communities in the transition zone from oxic to anoxic conditions.
Meiobenthos was present at all investigated depths and included 21 taxa. (Sergeeva et al. 2013). Our present
study is devoted to the futher description of taxonomic diversity of meiobenthos studied in this cruise.
Material and Methods
A twelve-day cruise was carried out to the Istanbul Strait’s outlet area (Bosporus) of the Black Sea with the
R/V ‘Arar’ from the Istanbul University during 9th–21st November 2009. In this study we sampled and
studied the complete taxa of meiobenthos covering the size range of 63 μm to 1.0 mm in the Istanbul Strait
outlet area of the Black Sea from water depths of 75 m to 300 m, where less saline surface waters of the
Black Sea interact with the saline Mediterranean waters, creating a special ecological system and rapid
transitions from oxic, hypoxic and anoxic water conditions.
The main objectives were, to investigate the distribution patterns of different taxonomic groups of
meiobenthos along different water depths between 75 m and 300 m (i), to determine the maximal sediment
depth of meiobenthos occurrence (ii), to study the quantitative relationships between different taxa and their
settlement levels within the sediment (iii).
Geophysical subbottom profiling and sediment coring along depth transects from 70 m to 300 m were
conducted. Nine benthic stations were chosen along this transect from the oxic to the anoxic zone (Table l).
Table 1. Water depths and coordinates of benthic stations in the Istanbul Strait’s (Bosporus) outlet area of the Black
Sea (RV ’Arar’ cruise, November 2009).
Station Water depth (m)
Latitude, N
Longitude, E
1
75
41°20,33´
29°06,03´
3
82
41º24,02´
29°03,21´
4
88
41°23,29´
29º12.24´
5
103
41°26,86´
29°12,95´
6
122
41°28,68´
29°14,81´
7
160
41°28,99´
29°15,14´
8
190
41°29,36´
29°15,53´
9
250
41°29,93´
29°16,12´
10
300
41°30,14´
29°16,34´
Ecol. Mont., 2 (3), 2015, 255-270
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DEEP-WATER PROTOZOA AND METAZOA OF THE BOSPORUS
Samples for biological studies were collected using a multiple corer and a gravity corer, devices that obtain
virtually undisturbed sediment samples. At each station, the sediment cores were sectioned into the following
horizontal layers: 0–1, 1–2, 2–3, 3–5, 5–7 and 7–9 cm. All sediment sections were preserved in 75% alcohol,
which is known to preserve morphological structures without distortion. We avoided prior fixation in
formalin in order to not damage calcareous taxa. The sediments were washed through sieves with a mesh
size of 1mm and 63μm, and stained with Rose Bengal solution before being sorted in water under a
microscope for “live” (= stained) organisms. We extracted only those specimens that were stained intensely
with Rose Bengal and showed no signs of morphological damage. In this study, we identified ‘live’ protists
and other meiofaunal organisms based on Rose Bengal staining. The fraction that retained in the sieves was
stained with Rose Bengal solution, a dye traditionally used to separate living and dead / decaying organisms
(Grego et al. 2013) and sorted in water under a binocular microscope for ‘live’ (stained) organisms, which
were identified to higher taxa (Bernhard 2000; Bernhard et al. 2006; Danovaro et al. 2010). We extracted
only those specimens that were stained intensely with Rose Bengal and showed no signs of morphological
damage. All isolated macro- and meiobenthos were counted and identified to higher taxa level. All protozoa
and metazoa fauna, larger than 63μm were categorized as meiobenthos. All of the organisms isolated were
counted and identified to higher taxa. Protists were indentified as gromiids based on test characteristics, test
shape and the presence of an oral capsule (Roth et al. 2010). However, because gromiids can be confused
with allogromiid foraminiferans, confirmation of these identification must be await molecular analyses and
an examination of the test-wall ultra structure (Sergeeva et al. 2012)
Oxygen measurements were conducted at three stations (88, 103, and 122 m water depth) as at the
remaining stations pebbles and shells, densely covering the sediment surface, impeded the penetration of the
fragile microsensors (Fig. 1).
-3
-2
Depth (mm)
-1
water column
0
sediment
1
2
3
Station 4, 88m water depth
Station 5, 103m water depth
Station 6, 122m water depth
4
5
0.00
0.05
0.10
0.15
0.20
0.25
0.30
Oxygen (mmol L-1)
Figure 1. Oxygen concentrations in the sediment and the overlying water at Stations 4–6 (by Sergeeva et al 2013).
Results and Discussion
Benthic fauna analyses suggest that the oxic/anoxic transition zone supports a high abundance and rich
protozoan and metazoan life. Altogether, these results confirm our early conclusion about a possible
adaptation of some forms of benthos to hypoxia/anoxia and the hydrogen sulfide environment (Sergeeva et
al. 2012). Our data suggest that some of the organisms (gromiids, allogromiids, ciliophora, hydrozoa,
nematodes, and polychaetes) have indeed adapted to live under hypoxic/anoxic and sulfidic conditions in the
Black Sea. This fauna is indigenous, rather than having been transported from adjacent oxygenated areas.
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SERGEEVA & MAZLUMYAN
1. Protozoa
Protozoa have been defined as single-cell protists with animal-like behavior. Protozoa is the significant
components of the micro- and meiofauna. Protozoa refers to a unicellular heterotrophic protist. As
components of the micro- and meiofauna, protozoa are an important food source for micro-invertebrates.
Thus, the ecological role of protozoa in the transfer of bacterial and algal production to successive trophic
levels is important. As predators, they prey upon unicellular or filamentous algae, bacteria, and marine
filamentous fungi. Protozoa are both herbivores and consumers in the decomposer link of the food chain.
Protozoans from the Istanbul Strait’s (Bosporus) outlet area of the Black Sea comprised Gromida,
Ciliophora and Foraminifera, notably hard-shelled and soft-shelled single-chambered (monothalamous) taxa
(Fig. 2). Gromiids and large allogromiids (soft-shelled) foraminifera may have been disregarded because of
their resemblance to faecal pellets (Nyholm & Gertz 1973). For many years these organisms were difficult
for non-specialists to be classified taxonomically or even recognized as protists (Gooday et al. 2000). These
taxa are also problematic because they are characterized by a small volume of protoplasm, contained within a
large test volume. Representatives of gromiids and soft-shelled foraminiferans in Bulgarian coastal zone are
noticed for the first time A. Valkanov (1970) and V. Golemansky (1974, 1999, 1999a). Then these
protozoans along the shelf and continental slope of the Black Sea with oxygen deficiency were found
(Sergeeva 2003; Sergeeva & Gulin 2007). Gromida was the permanent component of the meiobenthos on all
studied depths. The relative share of Gromida amounts 0–30%. Ciliophora make out main share at the
depths 103, 250, 300 m. The relative share of Ciliophora amounts 15–90 %. The relative share of
Foraminifera amounts 3–88 %. Foraminifera make out main share on the depths 82, 160, 190 m (Fig. 2).
Gromida
Ciliophora
Foraminifera
100%
Share
80%
60%
40%
20%
0%
75
82
88
103
122
162
190
250
300
Depth, m
Figure 2. Proportion of main protozoan taxa inhabiting along the depth gradient at the Bosporus outlet area of the Black
Sea
1.1. Gromida
The genus Gromia Claparède & Lachman 1859 was referred to large bottom protozoans (the size of some of
them make more than 1cm), living in small and large depths. On the basis of the General morphology
Gromia was considered to be one of the classes of Foraminifera, with similar life cycle. Gromia differ by
absence of the anastomosis on the pseudopodia and meiosis gametes at other stages of the cycle. There is a
hypothesis that the morphological resemblance between Gromia and Foraminifera may be due to a common
ancestor. But molecular phylogeny showed that Foraminifera and Gromia are separate branches of Rizaria
(Burki et al. 2002; Piña-Ochoa 2010; Rothe et al. 2011). Like soft-shelled foraminifera, representatives of
the genus Gromia have been mentioned only in the works on the Black Sea. (Golemansky 1999a, 2007)
Ecol. Mont., 2 (3), 2015, 255-270
259
DEEP-WATER PROTOZOA AND METAZOA OF THE BOSPORUS
N, indiv.
These protozoans were found at different depths in the Black sea, down to the depths of permanent hypoxia.
Usually they registered in the top inch of the bottom sediment. Preliminary studies showed the presence of at
least five, maybe new to science.
We presume that these organisms are gromiids because they have a clear, transparent test wall, a
well-developed oral capsule, and are filled with stercomata. In our collections in the Bosporus outlet area the
discovered gromiids had spherical and ellipsoidal forms of size from a few μm to more than 1.5 mm. These
organisms were found in the range 75–250 m water depths. The abundance maximum was at 75 m (Fig. 3).
Gromida vertical distribution marked some characteristics. The peaks in abundance of Gromida occurred at
the depth 75, 88, 122, 250 m. At the point of maximum
Gromiida observable abundance (75, 88, 250 m) most of
individuals settled upper layer of the bottom sediment, only at 122 m depth deeper layer (7–9 cm) was
inhabited by Gromia. That is (Fig. 4) notable that the middle layer (3–5 cm) of the investigated bottom
sediment was uninhabited by Gromia.
12500
10000
7500
5000
2500
0
75
82
88
103
122
162
190
250
300
Depth, m
Figure 3. Trends in the abundance of gromiids (indiv.*m-2) along depth gradient at the Bosporus outlet area of the
Black Sea.
0-1cm
1-2 cm
2-3 cm
3-4 cm
5-7 cm
100%
Share
80%
60%
40%
20%
0%
75
82
88
103
122
162
190
250
Depth (m)
Figure 4. Proportion of gromiids inhabiting different sediment layers along the depth gradient.
1.2. Ciliophora
Three species of commensal ciliates Cothurnia maritima Ehrenberg 1838 on oligochaete Tubificoides sp.;
Paracineta livadiana (Mereschkowsky 1881) and Corynophrya lyngbyi (Ehrenberg 1834) on harpacticoid
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SERGEEVA & MAZLUMYAN
N, indiv.*10 3
copepods Amphiascella subdebilis (Willey 1935), Haloschizopera pontarchis Por 1959, Cletodes tenuipes
Scott 1896 and Enhydrosoma longifurcatum (Sars 1909) were found in the Bosporus region of the Black Sea
deep-water (200 and 248 m depths) under hypoxic/anoxic conditions (Sergeeva & Dovgal 2014).
Vertical distribution of the free-living benthic Ciliophora in the Bosporus area at the depths from 120
to 300 m was characterized by two peaks of abundance at 103 and 250 m water depth (Fig. 5).
In the Bosporus area Ciliophora was registered in all layers of the bottom sediment. The most
inhibited are the upper layers (0–2 cm) of sediment (Fig. 6). Ciliates abundance peaks can be connected with
food accumulations. Different forms were present, including moving and attached forms, totally more than
Ciliophora
30 species (morphotypes).
50
40
30
20
10
0
75
82
88
103
122
162
190
250
300
Depth, m
Figure 5. Trends in the abundance (103indiv.m-2) of Ciliophora along depth gradient at the Bosporus outlet area of the
Black Sea.
It is known that the top peak of ciliates abundance usually was located in the region of the hydrogen sulfide
border. The most number of benthic ciliates morphotypes was registered at the 250 m depth, in the region of
lower peak of abundance.
0-1cm
1-2 cm
2-3 cm
3-4 cm
4-5 cm
5-7 cm
100%
Share
80%
60%
40%
20%
0%
75
82
88
103
122
162
190
250
300
Depth (m)
Figure 6. Proportion of the Ciliophora inhabiting different sediment layers along the depth gradient at the Bosporus
outlet area of the Black Sea.
Earlier the bathymetric distribution of the benthic ciliates at depths from 120 to 2075 m near the Dnieper
Canyon and the Sorokin Trough (eastern part of the Black Sea) was described from samples of near bottom
Ecol. Mont., 2 (3), 2015, 255-270
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DEEP-WATER PROTOZOA AND METAZOA OF THE BOSPORUS
water, sediment surface detritus, and the upper layer (0–1 cm) of sediment. Hydrogen sulfide was registered
beginning from 160–170 m. The ciliates found in mentioned samples were the representatives of genera
Chilodonella Strand 1928, Trachelocerca Ehrenberg 1834, Tracheloraphis Dragesco 1960 and Loxophyllum
Dujardin 1841. At the same time more than 30 morphological species were recognized among mentioned
materials (Sergeeva & Zaika 2008). The peaks of ciliate abundances were registered at depths of 120, 160–
190, and 240 m in the same region (Sergeeva et al. 2008). Average abundance peak coincides with the
depths of hydrogen sulfide appearance. Besides, according to the data available, at the same depths there are
pelagic peaks of intensity of bacterial chemosynthesis and bacteria production. Therefore ciliates abundance
peaks can be connected with food accumulations. The most number of ciliates morphotypes (8) was at the
240 m depth, in the region of the lower peak of abundance.
1.3. Foraminifera
Foraminifers consist of calcareous (hard-shelled) and soft-shelled forms. Distribution of foraminifera in the
depths was uneven. The maximum abundance of hard-shelled foraminifera corresponds to the 82 m peak
(Fig. 7).
soft-shelled
hard-shelled
total
N,103ind*m-2
50
40
30
20
10
0
75
82
88
103
122
160
depth (m)
190
250
300
Figure 7. Distribution of the Foraminifera (hard-shelled and soft-shelled) abundance (N) along depth gradient at the
Bosporus outlet area of the Black Sea.
Specimens were found in all layers (0–5 cm) of the bottom sediment at the point of maximum observable
abundance (Fig. 8). The most numerous were specimens of Hyperammina sp., which has a fragile sandy
shell. Hyperammina sp was the dominant among the other foraminifera. The largest of its individuals can be
included in the category of macrobenthos. Other most numerous species were Ammonia compacta (Hofker)
and Eggerella scabra (William). Hard-shelled foraminifera in contrast to the soft-walled were more
numerous at lower depths (75–160 m). Soft-shelled foraminiferas were observed in conditions of acute
hypoxia / anoxia (250–300 m). At a depth of 88 m peak of the soft-shelled foraminifera was marked. Most
specimens were found in the top layer (0–2 cm) or in the overlying surface detritus (Figs. 8, 9). Soft-shelled
forms were found at all studied depths. At these depths we can identify representatives of the soft-shelled
forms Goodayia rostellatum Sergeeva & Anikeeva, 2008 and Tinogulmia sp. (Gooday 1990; Sergeeva et al.
2005) as the most tolerant to oxygen deficiency (Sergeeva & Mazlumyan 2013).
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SERGEEVA & MAZLUMYAN
0-1cm
1-2 cm
2-3 cm
3-4 cm
100%
Share
80%
60%
40%
20%
0%
75
82
88
103
122
162
190
250
300
Depth (m)
Figure 8. Proportion of hard-shelled foraminifera inhabiting different sediment layers along the depth gradient.
0-1cm
1-2 cm
2-3 cm
3-4 cm
4-5 cm
100%
Share
80%
60%
40%
20%
0%
75
82
88
103
122
162
190
250
300
Depth (m)
Figure 9. Proportion of soft-shelled foraminifera inhabiting different sediment layers along the depth gradient.
2. Metazoa
The Metatozoa present between 75 and 300 m included the following taxa: Coelenterata (Hydrozoa),
Turbellaria, Nematoda, Oligochaeta, Polychaeta, Nemertini, Kinorhyncha, Bivalvia, Gastropoda,
Ophiuroidea, Harpacticoida, Ostracoda, Amphipoda, Cumacea, Tanaidacea, Acari, Tardigrada and Tunicata.
Among Metazoa Free-living Nematoda, Polychaeta and Harpacticoida are key components of the deep-water
meiobenthic communities (Fig. 10). Nematoda was dominating component of the communities at all studied
depths. The relative share of Nematoda amounts 60–98 %. Harpacticoida make out its main share at the 82
m. The relative share of Harpacticoida amounts 8–40 %. The relative share of Polychaeta amounts 0–1.3 %.
Ecol. Mont., 2 (3), 2015, 255-270
263
DEEP-WATER PROTOZOA AND METAZOA OF THE BOSPORUS
Nematoda
Polychaeta
Harpacticoida
100%
Share
80%
60%
40%
20%
0%
75
82
88
103
122
162
190
250
300
Depth (m)
Figure 10. Proportion of the main Metazoa taxa inhabiting along depth gradient at the Bosporus outlet area of the Black
Sea.
2.1. Free-living Nematoda
Nematoda was dominating taxon among meiobenthos along the depth transect. In the distribution of
Nematoda some peaks were marked, occurring at the depth 75, 88–103, 162 and 250 m. Maximal abundance
value of Nematoda reaches up 1.514 th. ind.*m-2 at the depth of 75 m. The share of the Nematoda in its
maximum point corresponded to 82 % of all meiobenthos abundance at that depth.
At the depth of 88–103 m abundance, becomes practically even with 700.0–650.0 th. ind.*m-2. At
the depths of 250 m Nematoda peak of abundance with 400.0 th.ind.*m-2.was observed (Fig. 11).
N, indiv.*10 3
1750
1500
1250
1000
750
500
250
0
75
82
88
103
122
162
190
250
300
350
De pth, m
Figure 11. Trends in the abundance (103indiv.*m-2) of nematodes along depth gradient at the Bosporus outlet area of
the Black Sea.
Nematodes inhabited mostly the top layer (0–2 cm) of bottom sediment. The share of the habitation in that
layer amounts 60-96 % along the depth transect (Fig. 12).
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SERGEEVA & MAZLUMYAN
0-1 cm
1-2 cm
2-3 cm
3-4 cm
4-5 cm
5-7 cm
7-9 cm
100%
Share
80%
60%
40%
20%
0%
75
82
88
103
122
162
190
250
300
Depth (m)
Figure 12. Proportion of nematodes inhabiting different sediment layers along the depth gradient.
2.2. Polychaeta
The distribution of Polychaeta abundance in the depth range 75–250 m is very uneven. In the distribution of
Polychaeta marked peaks occurred at the depth 88, 162 and 250 m. Maximal abundance value of Polychaeta
reached up to 9360 indiv.*m-2 at the depth of 88 m, the second largest peak of polychaetes inhabitation (7280
indiv.*m-2) occurred at the depth 250 m (Fig. 13). At the depth 162 m polychaetes almost entirely were
represented by young individuals of species Vigtorniella zaikai Kiseleva and Protodrilus sp. Usually, these
species inhabited suboxic layer and upper border of the hydrogen sulfide (Zaika et al. 1999, Zaika &
Sergeeva 2008). At the depth 250 m of polychaetes only species V. zaika was found, whereas in other parts
of the Black Sea this species had its maximum of abundance at a shallower depth (150–170 m) (Zaika &
Polychaeta
Sergeeva 2012). The planktonic larvae of V. zaikai
dwell in layer with certain physical and chemical
characteristics. They occurred in all studied samples of near bottom water, sediment surface detritus and in
the upper layer (0–3 cm) of sediment (Fig. 14).
N, indiv.
10000
8000
6000
4000
2000
0
75
82
88
103
122
162
190
250
300
Depth, m
Figure 13. Trends in the abundance (indiv.*m-2) of Polychaeta along depth gradient at the Bosporus outlet area of the
Black Sea.
Ecol. Mont., 2 (3), 2015, 255-270
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DEEP-WATER PROTOZOA AND METAZOA OF THE BOSPORUS
0-1 cm
1-2 cm
2-3 cm
3-4 cm
4-5 cm
5-7 cm
100%
80%
Share
60%
40%
20%
0%
75
82
88
103
122
162
190
250
300
Depth (m)
Figure 14. Proportion of polychaetes inhabiting different sediment layers along the depth gradient.
2.3. Harpacticoida
In the near-Bosporus area on the 82 m water depth there was new record of the species. Among
harpacticoides from this region, there were several eurybathic species, known for the Black Sea, widespread
on sandy and silty-sandy soils in the depth range of 10–150 m off the coast of the Caucasus, the Crimea and
the coast of Bulgaria and Romania (Kolesnikova 2003, 2010). An the Bosporus outlet area at the 82 m water
depth new species Sarsameira parva (Boeck) and Tachidiella minuta (Sars) were found in the Black Sea
(Kolesnikova & Sergeeva 2011).
The abundance of Harpacticoida rapidly decreased from >200 000 ind *m-2 at a depth of 75 m to 520
-2
ind *m at a depth of 190 m, however again slightly increased at 250 m (Fig. 15).
N, indiv.*10 3
200
150
100
50
0
75
82
88
103
122
162
190
250
300
350
Depth, m
Figure 15. Trends in the abundance (indiv.*m-2) of harpacticoides (including nauplia) along depth gradient at the
Bosporus outlet area of the Black Sea.
In the Bosporus area Harpacticoida were registered from 0–1 to 4–5 cm layers in the column of the bottom
sediment. The upper layers (0–2 cm) of sediments are the most habitable at all depths up to 300 m (Fig. 16).
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SERGEEVA & MAZLUMYAN
0-1 cm
1-2 cm
2-3 cm
3-4 cm
4-5 cm
100%
Share
80%
60%
40%
20%
0%
75
82
88
103
122
162
190
250
300
Depth (m)
Figure 16. Proportion of the harpacticoids inhabiting different sediment layers along the depth gradient.
Conclusion
Under hypoxia, many aerobic organisms have difficulties in their life, so it leads to changes of the structure
of benthic communities and reduced biological diversity and in the extreme conditions it leads to the
disappearance of a number of aerobic benthic forms. At Bosporus outlet area the vertical distribution of some
macrobenthic fauna (Annelida) was noted up to 300 m water depth. Although in columns of multiple cores
(160-300 m) representatives of the macrobenthos taxa: Annelida, Bivalvia and Gastropoda were marked
(Sergeeva et al. 2011). Our data suggest that the oxic/anoxic transition zone supports diversity and density of
some meiofauna Metazoan taxa (Nematoda and Harpacticoida) and Protozoan taxa (Cromida, Ciliophora and
Foraminifera), the most abundant representatives of the eumeiobenthos in samples from deeper,
anoxic/sulfidic areas.
Acknowledgements
A part of this work was funded by the EU 7 th FP project HYPOX (In situ monitoring of oxygen depletion in hypoxic
ecosystems of coastal and open seas, and land-locked water bodies) EC Grant 226213. We are grateful to Dr. Igor
Bondarev of IBSS for taking part in benthic sampling campaign. We are grateful to Professor Namik Çagatay for
providing an opportunity to participate in RV ‘Arar’ cruise and Anna Lichtschlag and Moritz Holtappels (Max Planck
Institute for Marine Microbiology, Germany) for cooperation.
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