Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area of the Black Sea
The results of investigations of tardigrades (2009-2010) in the Bosporus outlet area of the Black Sea are represented. For the first time two species of tardigrades Dipodarctus subterraneus (Renaud-Debyser, 1959) and Tanarctus ramazzottii (Renaud-Mornant, 1975) are recorded for the Black Sea. Tardig...
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Інститут зоології ім. І.І. Шмальгаузена НАН України
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irk-123456789-1097462016-12-13T03:02:17Z Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area of the Black Sea Kharkevych, Kh.O. Sergeeva, N.G. Экология The results of investigations of tardigrades (2009-2010) in the Bosporus outlet area of the Black Sea are represented. For the first time two species of tardigrades Dipodarctus subterraneus (Renaud-Debyser, 1959) and Tanarctus ramazzottii (Renaud-Mornant, 1975) are recorded for the Black Sea. Tardigrades are registered on 4 stations at depths range 88-250 m. Average abundance of tardigrades widely varied from 141 to 11 440 ind./m². The vertical distribution of tardigrades in the sediments was analyzed: most specimens (up to 98 %) found in the top 0-1 cm sediment layer. Приведены результаты исследований тихоходок (2009-2010 гг.) в Прибосфорском районе (Чёрное море). Впервые для Чёрного моря зарегистрированы два вида тихоходок Dipodarctus subterraneus (Renaud-Debyser, 1959) и Tanarctus ramazzottii (Renaud-Mornant, 1975). Тихоходки были зарегистрированы на 4 станциях в диапазоне глубин 88-250 м. Средняя численность тихоходок варьировала в широких пределах от 141 до 11 440 экз./м². Проанализировано вертикальное распределение тихоходок в донных осадках: большинство экземпляров (до 98 %) обнаружены в верхнем 0-1 см слое донных осадков. 2013 Article Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area of the Black Sea / Kh.O. Kharkevych, N.G. Sergeeva // Вестник зоологии. — 2013. — Т. 47, № 3. — С. 219-229. — Бібліогр.: 28 назв. — англ. 0084-5604 DOI 10.2478/vzoo-2013-0021 http://dspace.nbuv.gov.ua/handle/123456789/109746 595.41(262.5) en Вестник зоологии Інститут зоології ім. І.І. Шмальгаузена НАН України |
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Экология Экология |
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Экология Экология Kharkevych, Kh.O. Sergeeva, N.G. Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area of the Black Sea Вестник зоологии |
| description |
The results of investigations of tardigrades (2009-2010) in the Bosporus outlet area of the Black Sea are represented. For the first time two species of tardigrades Dipodarctus subterraneus (Renaud-Debyser, 1959) and Tanarctus ramazzottii (Renaud-Mornant, 1975) are recorded for the Black Sea. Tardigrades are registered on 4 stations at depths range 88-250 m. Average abundance of tardigrades widely varied from 141 to 11 440 ind./m². The vertical distribution of tardigrades in the sediments was analyzed: most specimens (up to 98 %) found in the top 0-1 cm sediment layer. |
| format |
Article |
| author |
Kharkevych, Kh.O. Sergeeva, N.G. |
| author_facet |
Kharkevych, Kh.O. Sergeeva, N.G. |
| author_sort |
Kharkevych, Kh.O. |
| title |
Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area of the Black Sea |
| title_short |
Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area of the Black Sea |
| title_full |
Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area of the Black Sea |
| title_fullStr |
Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area of the Black Sea |
| title_full_unstemmed |
Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area of the Black Sea |
| title_sort |
deep-water tardigrada of the istanbul strait’s (bosporus) outlet area of the black sea |
| publisher |
Інститут зоології ім. І.І. Шмальгаузена НАН України |
| publishDate |
2013 |
| topic_facet |
Экология |
| url |
http://dspace.nbuv.gov.ua/handle/123456789/109746 |
| citation_txt |
Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area of the Black Sea / Kh.O. Kharkevych, N.G. Sergeeva // Вестник зоологии. — 2013. — Т. 47, № 3. — С. 219-229. — Бібліогр.: 28 назв. — англ. |
| series |
Вестник зоологии |
| work_keys_str_mv |
AT kharkevychkho deepwatertardigradaoftheistanbulstraitsbosporusoutletareaoftheblacksea AT sergeevang deepwatertardigradaoftheistanbulstraitsbosporusoutletareaoftheblacksea |
| first_indexed |
2025-07-07T23:36:13Z |
| last_indexed |
2025-07-07T23:36:13Z |
| _version_ |
1837033192167571456 |
| fulltext |
UDC 595.41(262.5)
DEEP-WATER TARDIGRADA OF THE ISTANBUL STRAIT’S
(BOSPORUS) OUTLET AREA OF THE BLACK SEA
Kh. O. Kharkevych, N. G. Sergeeva
A. O. Kovalevsky Institute of Biology of the Southern Seas of NAS of Ukraine
Nakhimov av., 2, Sevastopol, 99011 Ukraine
E-mail: k.kristinna@gmail.com, nserg05@mail.ru
Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area of the Black Sea. Khar -
kevych Kh. O., Sergeeva N. G. – The results of investigations of tardigrades (2009—2010) in the
Bosporus outlet area of the Black Sea are represented. For the first time two species of tardigrades
Dipodarctus subterraneus (Renaud-Debyser, 1959) and Tanarctus ramazzottii (Renaud-Mornant, 1975)
are recorded for the Black Sea. Tardigrades are registered on 4 stations at depths range 88—250 m.
Average abundance of tardigrades widely varied from 141 to 11 440 ind./m2. The vertical distribution
of tardigrades in the sediments was analyzed: most specimens (up to 98 %) found in the top 0—1 cm
sediment layer.
Ke y wo r d s: deep-water tardigrades, Dipodarctus subterraneus, Tanarctus ramazzottii, abundance, dis-
tribution, Black Sea.
Ãëóáîêîâîäíûå òèõîõîäêè (Tardigrada) â ðàéîíå Áîñôîðà (׸ðíîå ìîðå). Õàðêåâè÷ Õ. Î, Ñåðãå -
åâà Í. Ã. – Ïðèâåäåíû ðåçóëüòàòû èññëåäîâàíèé òèõîõîäîê (2009—2010 ãã.) â Ïðèáîñôîðñêîì
ðàéîíå (׸ðíîå ìîðå). Âïåðâûå äëÿ ׸ðíîãî ìîðÿ çàðåãèñòðèðîâàíû äâà âèäà òèõîõîäîê
Dipodarctus subterraneus (Renaud-Debyser, 1959) è Tanarctus ramazzottii (Renaud-Mornant, 1975).
Òèõîõîäêè áûëè çàðåãèñòðèðîâàíû íà 4 ñòàíöèÿõ â äèàïàçîíå ãëóáèí 88—250 ì. Ñðåäíÿÿ ÷èñ-
ëåííîñòü òèõîõîäîê âàðüèðîâàëà â øèðîêèõ ïðåäåëàõ îò 141 äî 11 440 ýêç./ì2. Ïðîàíàëèçè ðî -
âàíî âåðòèêàëüíîå ðàñïðåäåëåíèå òèõîõîäîê â äîííûõ îñàäêàõ: áîëüøèíñòâî ýêçåìïëÿðîâ (äî
98 %) îáíàðóæåíû â âåðõíåì 0—1 ñì ñëîå äîííûõ îñàäêîâ.
Êëþ÷åâûå ñ ëîâ à: ãëóáîêîâîäíûå òèõîõîäêè, Dipodarctus subterraneus, Tanarctus ramazzottii,
÷èñëåííîñòü, ðàñïðîñòðàíåíèå, ׸ðíîå ìîðå.
Introduction
Among the seas of Mediterranean basin, the Black Sea exhibits a number of features. It is deep marginal
meromictic reservoir that has an oxygenated surface layer overlying a sulfide containing anoxic deep layer. The
combined effect of great depth, considerable desalination of surface waters caused by river discharges, and the
influx of saline deep water from the Marmara Sea, creates a distinct stratification of the water column into an
upper, relatively thin (150—250 m deep) oxic zone with plentiful flora and fauna and a huge anoxic zone (from
150 to 250 m depth down to the deepest point) with high hydrogen sulfide concentrations.
The Black Sea exhibits a number of remarkable oceanographic and hydrographic characteristics
(Murray et al., 1993; Özsoy, Ünlüata, 1997). The combined effect of great depth (> 2000 m), shallow sill
depth (35 m) of the Istanbul Strait (Bosporus) outlet, large amount of river water input, and the inflow of
warm and saline Mediterranean water creates a distinct basin-wide water-column stratification with a chemo-
cline/pycnocline at 100 to 150 m, separating an oxic and an anoxic zone. Between the oxic and anoxic waters
there is a suboxic zone, which is important for biogeochemical and redox reactions.
Long-term monitoring of the distribution of oxygen and sulfide across this boundary indicates that it is
situated at a depth of 80—100 m in the centre and 160—250 m at the periphery (Eremeev, Konovalov, 2006).
Where the oxic/anoxic interface in the water column impinges on the seafloor, it creates a strong ben-
thic gradient in oxygen and hydrogen sulfide concentrations. This O2/H2S-transition zone is highly dynam-
ic, characterized by varying concentrations of oxygen and hydrogen sulfide in the bottom water, and oscil-
lates above and below its average depth.
The interactions between these oxic and anoxic water masses are of great interest to researchers in dif-
ferent scientific fields. The taxonomic composition and distribution of meiobenthic fauna inhabiting the depth
zone where the oxic/anoxic interface zone meets the sea floor is of special interest.
Vestnik zoologii, 47(3): e-17—e-27, 2013
DOI 10.2478/vzoo-2013-0021
Ýêîëîãèÿ
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Researches give considerable attention to the investigation of meiobenthos of the Black Sea (Sergeeva
et al., 2013). However, data on meiobenthos of Bosporus region and on the meiofauna of the interaction
zone of oxygen and anoxic water masses are scarce (Sergeeva, Gulin, 2007). Specific communities of benth-
ic nematodes, foraminifera, harpacticoides, ostracodes and polychaetes adapted to specific environmental
conditions were recorded to the Bosporus outlet area of the Black Sea (Caraion, 1959; Didkowsky, 1969;
Yanko, Vorobyova, 1991; Karaçuha et al., 2011; Ürkmez et al., 2011; Zaika, Sergeeva, 2012).
The first detailed data of the taxonomic structure, abundance and distribution of the meiobenthos on
the Black Sea shelf and the upper slope area off the Bosporus Strait outlet in the transition zone from oxic
to anoxic conditions along transects from 75 to 300 m water depth were presented of Sergeeva et al. (2013).
The meiobenthos was present at all investigated depths and includes 21 taxa. For the first time in the
Bosporus Strait outlet Tardigrades were found.
The marine tardigrades fauna of the Black Sea is poorly known. From the northwestern Black Sea, near
the Bulgarian and Romania coast, five species, Batillipes mirus Richters, 1909, Stygarctus bradipus Schultz,
1951, Echiniscoides sigismundi Schultz, 1865, Halechiniscus guiteli Richters, 1908 and Hypsibius stenostomus
Richters, 1908 were recorded (Richters, 1909, Rudescu, 1969).
After that, there were found tardigrades species B. mirus, E. sigismundi, H. guiteli and species
Styraconyxinae gen. sp. in the coastal zone of Crimea (Sergeeva et al., 2006). Since then, data about the
Crimean fauna of Tardigrada have successively been obtained from different coastal regions and new for the
Black sea species of tardigrades B. gilmartini McGinty, 1969, B. spinicauda Gallo D’addabbo, Sandulli and
de Zio Grimaldi, 2005, Styraconyx qivitoq Kristensen and Higgins, 1984, S. nanoqsunguak Kristensen and
Higgins, 1984 and Megastygarctides sp. n. were recorded (Khakrevych, 2012). Until now, the marine tardi-
grades of the Bosporus area are entirely unknown.
We adhere to the classification of (Guidetti, Bertolani, 2005; Degma, Guidetti, 2007; Degma et al.,
2013) that the tardigrades form separate phylum Tardigrada, which is divided into 3 classes: Eutardigrada,
Mesotardigrada and Heterotardigrada.
Our main aim is to provide preliminary information concerning diversity and abundance of tardigrades
at the oxic/anoxic interface of the Bosporus region.
This work is the continuation of the series of studies of the deep-water meiobenthos in the Istanbul
Strait’s (Bosporus) outlet area of the Black Sea (Sergeeva et al., 2013), 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.
Material and methods
In the region of the Bosporus Strait (Black Sea), samples were obtained on two occasions: in November
2009 during a cruise of the R/V “Arar” of the Istanbul Technical University (Turkey) and in April 2010 dur-
ing cruise 15/1 of the R/V “Maria S. Merian” (Germany) (fig. 1).
The meiobenthos on the Black Sea shelf and the upper slope area off the Bosporus Strait outlet was for
the first time studied along depth transects from 75 to 300 m water depth, 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.
During the cruise of R/V “Maria S. Merian” samples for biological studies were collected using a multi-
corer (diameter of tubes 9.5 cm) and in the cruise of the R/V “Arar” was used a gravity corer (diameter
7 cm) device that obtain virtually undisturbed sediment samples. The sediment cores were sliced into 1-cm-
thick layers down to a depth of 5—10 cm depth in order to study the vertical distribution of the fauna. All
sediment sections were preserved in 75 % alcohol, which is known to preserve morphological structures of
fauna without distortion. Each layer was washed through two sieves, the upper one with a mesh size of 1 mm,
the lower one with a mesh size of 63 μm, and stained with Rose Bengal solution before being sorted in water
under a microscope for “live” (i. e., stained) and extracted organisms only those specimens that stained
intensely with rose Bengal and showed no signs of morphological damage. All of the isolated organisms were
counted and identified to higher taxa. Tardigrades were picked out using a glass pipette and placed in cavi-
ty slides with a mixture of glycerol (50 %) and water (50 %). Tardigrades specimens were observed and iden-
tificated for species with using of the microscope Nikon Eclipse E200. Photos of the organisms were taken
under different magnification. To compare the data obtained during two cruises, the average abundance of
tardigrades was calculated per square meter.
Oxygen concentrations in the sediment and the overlying water and oxygen penetration depth measured
at 88 m (st. 4), 103 m (st. 5) and 122 m (st. 6) are presented in table 1 (Sergeeva et al., 2013).
Bottom-water oxygen concentrations in the study area range from 0.17 mmol L-1 at 103 m water depth
to 0.12 mmol L-1 at 88 m water depth. The sediment samples in all stations differed by its composition and
structure. In the samples from 88 m (st. 4) the sediment was represented by gray aleuritic mud with frag-
ments of mollusk shells, at a depths of 117 m (st. 283) – black mud with mussel shells, at 122 m deep
(st. 6) – by black mud, and at 250 m (st. 9) – flowing black mud with a strong odor of hydrogen sulfide.
Tardigrada specimens were found on the 3 stations from 9 during a cruise of the R/V “Arar” and only
on the 1 from 18 meiobenthos stations during cruise of the R/V “Maria S. Marian” (table 2).
e-18 Kh. O. Kharkevych, N. G. Sergeeva
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e-19Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area...
Fig. 1. Meiobenthos stations in the region of Bosporus: × – stations 1 – 10 (R/V “Arar”, November, 2009);
î – stations 198 – 302 (R/V “Maria S. Marian”, April, 2010); – stations, where tardigrades were found.
Ðèñ. 1. Ìåéîáåíòîñíûå ñòàíöèè â ðàéîíå Áîñôîðà: × – ñòàíöèè 1 – 10 (ÍÈÑ «Arar», íîÿáðü, 2009);
î – ñòàíöèè 198 – 302 (ÍÈÑ «Maria S. Marian», àïðåëü, 2010); – còàíöèè, ãäå îáíàðóæåíû òèõî-
õîäêè.
Ta b l e 1. Dissolved oxygen concentrations measured in bottom waters above sediments and maximal oxygen
penetration depth in the sediments measured in cores retrieved from the near Bosporus area
Ò à á ëèö à 1. Êîíöåíòðàöèÿ ðàñòâîðåííîãî êèñëîðîäà â ïðèäîííûõ âîäàõ è ìàêñèìàëüíàÿ ãëóáèíà ïðî -
íèê íî âåíèÿ êèñëîðîäà â êîëîíêó äîííîãî îñàäêà â ïðèáîñôîðñêîì ðàéîíå
No t e . Measurings of A. Lichtschlag (Sergeeva et al., 2013).
Station Water depth (m) Oxygen concentration in the
overlying water (mmol L-1)
Maximal oxygen penetration depth (mm) in
bottom sediment
4 88 0.12 1
5 103 0.17 2
6 122 0.16 3
Ta b l e 2. Coordinates of the stations, where tardigrades found
Òà á ëèö à 2. Êîîðäèíàòû ñòàíöèé, íà êîòîðûõ îáíàðóæåíû òèõîõîäêè
Data Coordinates/Cruise Station, N Depth, m
2009.11.15 41°23,29´ N, 29°12,24´ E / R/V “Arar” 4 88
2009.11.15 41°28,68´ N, 29°14,81´ E / R/V “Arar” 6 122
2009.11.15 41°29,93´ N, 29°16,12´ E / R/V “Arar” 9 250
2010.04.16 41°28,54´ N, 29°14,63´ E / R/V “Maria S. Marian” 283 117
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Results
Meiobenthic samples from Bosporus region contain rich fauna of meiobenthic
organisms. The meiobenthos was represented by 21 different taxa. Tardigrades were
associated with the great number of these groups of meiobenthic organisms.
In total, 53 specimens of tardigrades were found. Two species belonging to one
family of heterotardigrades were recorded from 4 stations from Bosporus region. All
species recorded from Bosporus region belong to the family Halechiniscidae (table 3).
Short diagnosis of found tardigrades species and some aspects of their ecological
and distributional features are given below.
CLASS HETEROTARDIGRADA Marcus, 1927
ORDER ARTHROTARDIGRADA Marcus, 1927
FAMILY HALECHINISCIDAE Thulin, 1928
Genus Dipodarctus Pollock, 1995
Dipodarctus subterraneus (Renaud-Debyser, 1959) (fig. 2)
Ma t e r i a l e x am in ed. 13 adult specimens from Bosporus area of the Black Sea, at 88 and 122 m
deep, from st. 4 and 6, respectively; cruise of R/V “Arar”, November 2009.
D i a gno s i s. All general taxonomic characters according to the original descrip-
tion (Renaud-Debyser, 1959). Length about 100 μm, cuticle smooth, with a slight fold
in correspondence with each pair of legs. A complete set of well-developed cephalic
sense organs is present. Median cirrus (10 μm), unpaired, vertically erected; internal
buccal cirrus (10 μm), paired and in dorsal position; external buccal cirrus (9 μm),
paired and in ventral position; lateral cirrus (13 μm), paired; clava (30 μm), paired.
The median cirrus and the buccal cirri have a well developed basal sheath; the lateral
cirrus and the clavae arise from a common base. Secondary clavae present as cephalic
ridges between internal and external cephalic cirri. Buccal aperture ventral; two stylets
are present.
Long legs, each with 4 digits ending with a claw without spurs. Between third and
fourth legs two long and robust dorsolateral cirri E. Each leg bears short sense organs.
Feet on legs I—III with at least 3 of the 4 toes short and of equal length; these feet
unlike that of the IV leg; foot on leg IV of Tanarctus-type, with 2 short outer toes (toes
1 and 4) with simple crescent claws and 2 long, thin, flexible medial toes (toes 2 and
3) with small crescent claws. Leg IV papilla is like an ovoid base with terminal spine.
As there are no table measurements in original description of the species (Renaud-
Debyser, 1959), so we can only compare the characters that were in the text (table 4).
There is difference in body length between the two localities. According to our
data, Black sea specimens are smaller than that described from Bimini Island. In spite
of this, specimens of this species that were found in other localities (Gallo D’Addabbo
et al., 2001) also have length about 100 μm. Differences in body size and some other
e-20 Kh. O. Kharkevych, N. G. Sergeeva
Ta b l e 3. List of tardigrades species with indication of the stations, where they were found
Òà á ëèö à 3. Ñïèñîê âèäîâ òèõîõîäîê ñ óêàçàíèåì ñòàíöèé, ãäå îíè áûëè îáíàðóæåíû
Species account Sampling station Total
HALECHINISCIDAE
Tanarctinae Renaud-Mornant, 1980
Tanarctus Renaud-Debyser, 1959
Tanarctus ramazzottii Renaud-Mornant, 1975 4, 6, 9, 283 40
Dipodarctinae Pollock, 1995 Dipodarctus Pollock, 1995
Dipodarctus subterraneus Renaud-Debyser, 1959 4, 6 13
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e-21Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area...
Fig. 2. D. subterraneus: 1 – general view (by Gallo D’Addabbo et al., 2001); 2 – photo of ventral view; 3 –
head cephalic appendages with cells glands; 4 – 3rd and 4th legs with different type of digits ending with
claws; 5 – internal, external and lateral cirri and clavaes; 6 – general view of the head.
Ðèñ. 2. D. subterraneus: 1 – îáùèé âèä (ïî: Gallo D’Addabbo et al., 2001); 2 – ôîòî ñ âåíòðàëüíîé ñòî-
ðîíû; 3 – ãîëîâíûå óñèêè è îäíîêëåòî÷íûå ãëàíäû; 4 – 3-àÿ è 4-àÿ íîãà ñ ïàëüöàìè ðàçíûõ òèïîâ
è êîãîòêàìè; 5 – âíåøíèå, âíóòðåííèå, áîêîâûå óñèêè è êëàâà; 6 – îáùèé âèä ãîëîâû.
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features as internal and external cirri could be due to the variation between the two
localities and different environmental conditions.
Species of this genus have specific and unique foot features that simplify the pro-
cess of identification of the species – unequal toe patterns on legs I—III and leg IV.
Feet of this species are a combination of short broad toes of the basic Halechiniscus-
type on the I—III legs, along with the long toes of the Tanarctus-type on the IV legs.
According to these features and other general taxonomic features we can exactly iden-
tified the specimens.
E co l o g i c a l p a t t e r n a nd g e o g r a ph i c a l d i s t r i b u t i o n. For the first time
it was found from Bimini Island (Bahamas) (Renaud-Debyser, 1959) and later (De Zio
Grimaldi et al., 1999) at various sites in the Mediterranean Sea. Also it was found in
Malta, Faroe Islands, Bahamas and in the Indian ocean near Seychelles in intertidal
and subtidal zones and Maldivian Island at a depth of 58 m (De Zio Grimaldi et al.,
2003; Gallo et al., 2007). The species was a part of the interstitial benthos of the inter-
tidal zone; it was found at a depth of 50-60 cm, in sand composed of detritus of organ-
isms (foraminifera, polyps, spines of echinoderms, mollusks) and of calcareous algae.
Species was recorded from submarine caves in S. Domino Island (Tremiti Island) in
the Mediterranean Sea in intertidal, interstitial coralline sands and subtidal within 20 m
depth (Gallo D’Addabbo, 2001).
It is the first records of this species in the Black Sea, where it was found in deep
water detritus sediment at a depth of 88 and 122 m.
FAMILY HALECHINISCIDAE Thulin, 1928
Genus Tanarctus Renaud-Debyser, 1959
Tanarctus ramazzottii (Renaud-Mornant, 1975) (fig. 3)
Ma t e r i a l e x am in ed. 40 adult specimens from Bosporus area, at 88, 122 and 250 m deep, from st.
4, 6 and 9, respectively of cruise R/V “Arar”, and 1 specimen from st. 283, at 117 m deep, cruise R/V “Maria
S. Marian”.
D i a gno s i s. Diagnostic characteristics and general features in accordance with
the original description of the species (Renaud-Mornant, 1975). Comparative analysis
of the main taxonomic characters of the type-species and Black Sea specimens are given
in the table 5.
Specimens of T. ramazzottii species found in the Black Sea have the similar mor-
phometric characteristics as type-materials of the species. Length about 80 μm, head
width – 35 μm. The Black Sea specimens are of the same sizes (as shown in the table).
The unpaired dorsal median cirrus (11 μm) is present, inserted on an enlarged base.
Paired internal cephalic cirri (20 μm) are inserted on basal peduncle, connected by a
e-22 Kh. O. Kharkevych, N. G. Sergeeva
Ta b l e 4. Morphometrics of the type-materials of the Dipodarctus subterraneus (by Renaud-Debyser, 1959)
and values of characters of specimens (N = 13) found in the Black Sea
Òà á ëèö à 4. Ìîðôîìåòðè÷åñêèå õàðàêòåðèñòèêè òèïîâîãî ìàòåðèàëà âèäà Dipodarctus subterraneus (ïî:
Renaud-Debyser, 1959) è çíà÷åíèÿ ïàðàìåòðîâ ýêçåìïëÿðîâ (N = 13), îáíàðóæåííûõ â ׸ðíîì ìîðå
N o t e. N – number of specimens.
Character, μm Holotype from Bimini island
(Bahamas)
Specimens from the Bosporus region
(Black Sea)
Total body length 133 100—105
Median cirrus 15 8—10
Internal cirri 14—15 10—12
External cirri 7—8 8—9
Lateral cirri “A” 10—13 13—14
Clavae 30—32 30—32
Cirri E — 40
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e-23Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area...
Fig. 3. T. ramazzottii: 1 – general view; 2 – external cirri and secondary clavae; 3 – cuticular membrane;
4 – mouth with subspherical bulb; 5 – clavae between 3rd and 4th legs, digits and claws; 6 – head with
full set of cephalic appendages.
Ðèñ. 3. T. ramazzottii: 1 – îáùèé âèä; 2 – âíåøíèå ãîëîâíûå óñèêè è âòîðè÷íàÿ êëàâà; 3 – êóòèêó-
ëÿðíàÿ ìåìáðàíà; 4 – ñóáñôåðè÷åñêàÿ ðîòîâàÿ ëóêîâèöà; 5 – óñèê ìåæäó 3-é è 4-é íîãîé, ïàëüöû
è êîãîòêè; 6 – ïîëíûé íàáîð ãîëîâíûõ ïðèäàòêîâ.
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cuticular membrane; paired external cephalic cirri (12 μm), also with peduncle bases,
are ventrally inserted; both the pair of cirri consists of a larger basal part and a slender
terminal part. The lateral cirri are inserted on an enlarged base, are (11 μm) long. The
primary clavae, 60—65 μm long, shorter that body length, flattened and end with a
rounded apex. Secondary clavae (10 μm) exist as short oval shape, not inserted on a
common base with lateral cirri A, but in a position more ventral and median, very near
to the bases of the external cephalic cirri.
The mouth is ventral with subspherical bulb, stylets are present. Specimens are with
long, slender and telescopic legs. The first three pairs possess long appendages. The
III leg appendages are slightly longer. The cirrus E (35 μm) is situated dorsally, above
the insertion of the 4th legs. The leg IV appendages are 150 μm long, simple without
any projections and branching. The legs bear four digits of different length, having the
internals longer (12 μm) than the externals (9 μm). They insert on a base joined to the
telescopic part of the leg by a strip of cuticle. Cuticular bar supports the lateral digits.
The claws are simple and attached to the digits by a basal spur. The cuticle is punctu-
ated with visible pores on the dorsal side, uniformly distributed.
In the description of the type specimen of this species is said that there is an
important ventral cephalic papillae and long simple IV leg appendages without sec-
ondary branches or projections. The Black Sea specimens of the species have all these
important taxonomic features.
E co l o g i c a l p a t t e r n a nd g e o g r a ph i c a l d i s t r i b u t i o n. This is the first
record of the species in the Black Sea at a depth of 88—250 m. For the first time the
species was found and identified by (Renaud-Mornant, 1975) from the abyssal mud in
the Bay of Biscay at a depth of 3039 meters, as well as in infralittoral fine sand on the
coast of northwestern Britain at a depth of 20 m. Also species were found in different
localities in the Mediterranean and other seas (De Zio Grimaldi et al., 2003).
Average abundance of tardigrades in meiobenthic communities widely varied. In
samples collected during the cruises, average abundance of tardigrades varies at differ-
ent stations from 141 ind./m2 (117 m deep) and 260 ind./m2 (250 m deep) at the 283
and 9 stations of cruise R/V “Maria S. Merian” and R/V “Arar”, respectively, to
1820 ind./m2 (88 m deep) and 11440 ind./m2 (122 m deep) at the 4 and 6 station of
cruise R/V “Arar” (fig. 4).
e-24 Kh. O. Kharkevych, N. G. Sergeeva
Ta b l e 5. Morphometrics of the type-materials of the Tanarctus ramazzottii (by Renaud-Mornant, 1975) and
values of characters of specimens (N = 40) found in the Black Sea
Òà á ëèö à 5. Ìîðôîìåòðè÷åñêèå õàðàêòåðèñòèêè òèïîâîãî ìàòåðèàëà âèäà Tanarctus ramazzottii (ïî
Renaud-Mornant, 1975) è çíà÷åíèÿ ïàðàìåòðîâ ýêçåìïëÿðîâ (N = 40), îáíàðóæåííûõ â ׸ðíîì ìîðå
N o t e. N – number of specimens.
Character, μm Holotype from Bay of Biscay Paratype from Brittany
Specimens from the Bosporus
region (Black Sea)
Total body length 80 82 80—83
Head width 35 32 33—35
Median cirrus 11 10 10—11
Internal cirri 21 22 20—22
External cirri 14 13 12—14
Lateral cirri “A” 11 11 10—11
Clavae 60 65 60—65
Secondary clavae 10 10 10—11
Cirri E 35 33 33—35
IV leg appendage 150 148 148—150
Median digit 13 12 11—12
Lateral digit 9 9 8—9
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New data about vertical distribution of tardigrades within the sediment column
have been obtained in Bosporus study area. Vertical stratification of tardigrades in
0—5 cm upper layer of benthic sediment was investigated. Most tardigrades specimens
were found in the top layer (0—1cm) or in the overlying surface detritus, and only at
st. 6 one specimen of Tardigrada species T. ramazzottii were recorded from 1—2 cm
layer. Our data suggest that near to 98 % of the studied tardigrades are confined to the
top layer (0—1 cm) of the sediments, supposedly to get access to available limited oxy-
gen and food in the bottom water. Studies supplement data about vertical distribution
of species individuals within the sediments.
Discussion
Heterotardigrada have a large geographical and ecological distribution. Taking into
account the new information and all the previous data from the literature, it can be
seen that two tardigrades species T. ramazzottii and D. subterraneus are highly distribut-
ed in different marine waters throughout the world.
Concerning Tanarctus, currently only 12 species have been described worldwide
(Jorgansen, Kristensen, 2001). Moreover, most found species of the genus Tanarctus are
from the Atlantic and very scare data from the Pacific. Also very little is known about
the worldwide zonation patterns of tanarctid tardigrades (Jorgansen, Kristensen, 2001).
For the first time T. ramazzottii was found in the sediments of Biscay Bay at a
depth of 3039 m. The species was found in the 2-cm-deep sediment. The sand was
heavily compacted and the oxidation of the sediment attains low values from the depth
of 6 to 7 cm (Renaud-Mornant, 1975). In the Mediterranean Sea, where the samples
were collected at different depths and in different sediments, tardigrades species
T. ramazzottii was found in substratum of coralligenous detritus at a depth between
21—40 m and 61—80 m (Grimaldi de Zio, Gallo D’Addabbo, 2001).
We can suppose that the Black Sea specimens were found in the similar environ-
mental conditions of the oxygen regime of Biscay Bay, where it was found at first time.
We recorded T. ramazzottii at 0—1 and 1—2 cm layer of the sediment. Oxygen concen-
tration in the overlying water was 0.12—0.16 mmol L-1 at the stations where specimens
were found. The maximal oxygen penetration depth in bottom sediment was 1 and
3 mm at the 88 and 122 m depth, respectively.
Only 3 species of the genus Dipodarctus is known (Degma et al., 2013; Pollock,
1995; Renaud-Debyser, 1959). D. subterraneus were found in sand, sand with Posidonia
meadow, in shell gravel and coralligenous detritus at all depth between 0 and over 80 m
(Grimaldi de Zio, Gallo D’Addabbo, 2001). Also it was found in the Indian Ocean and
e-25Deep-Water Tardigrada of the Istanbul Strait’s (Bosporus) Outlet Area...
Fig. 4. Average abundance of tardigrades along the depth on the Bosporus region (R/V “Arar”, November,
2009, R/V “Maria S. Marian”, April 2010).
Ðèñ. 4. Ðàñïðåäåëåíèå ÷èñëåííîñòè òèõîõîäîê ïî ãëóáèíå â ðàéîíå Áîñôîðà (ÍÈÑ «Arar», íîÿáðü,
2009; ÍÈÑ «Maria S. Marian», àïðåëü 2010).
0 2000 4000 6000 8000 10000 12000 14000
250
123
117
88
ind/m2
D
ep
th
,
m
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in other water basins (Gallo et al., 2007). In the Black Sea D. subterraneus was found
in deep water detritus sediment at a depth of 88 and 122 m.
Black Sea specimens of D. subterraneus species are smaller than the type-material
of the species. We suppose that it can probably be explained by the fact that it could
be juveniles of the species, because they are proportionately similar to adults in most
features with the exception of disproportionately longer lateral cirri “A”. Also the dif-
ferences in sizes of the specimens from one species D. subterraneus but from different
localities can be explained by different environmental conditions, such factors as spe-
cific hypoxic conditions.
Some authors considered that the kind of the substratum is the most important
ecological factor, whereas the depth has less influence (Grimaldi de Zio, Gallo
D’Addabbo, 2001), at that time the others confirm that physical-chemical characteris-
tics may be more influential in the distribution of meiofauna than the depth or water
temperature (Kristensen, 1992). It is interesting, that in Bosporus region tardigrades
were found in the mud, while in different localities of the Mediterranean Sea no tardi-
grades of these species were found in mud samples. Comparing the distribution of tardi-
grades in different sediments at different depths in the Black Sea, the highest number
of specimens reach a depth of 122 m, where the substratum is black mud.
Scarcity of data about tardigrades biology and distribution is due to the difficulties
of finding them by the minimal size of the specimens.
Agreeing with the statement that the majority of marine Tardigrada show a geo-
graphical distribution highly correlated with that of Tardigrada-workers, it can be
assumed that in future we will not only review the available data concerning the distri-
bution of marine tardigrades in the other seas, but also we will find different species in
the Black sea.
A part of this work was funded by the EU 7th FP project HYPOX (In situ monitoring of oxygen dep-
letion in hypoxic ecosystems of coastal and open seas, and land-locked water bodies) EC Grant 226216. The
authors are grateful to colleagues of Ecology Benthos Department of IBSS, Dr. S. A. Mazlumyan and
Dr. I. P. Bondarev for taking part in benthic sampling during the scientific cruises and also to the leading
technician L. F. Lukyanova for primary treatment of the bottom sediments.
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Received 10 December 2012
Accepted 20 May 2013
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