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Microplankton and its function in a zone
of shallow hydrothermal activity:
the Craternaya Bay, Kurile Islands
YU. I. SOROKIN1,*, P. YU. SOROKIN1 AND O. YU. ZAKOUSKINA1
INSTITUTE OF MARINE BIOLOGY, RUSSIAN ACADEMY OF SCIENCES, VLADIVOSTOK, RUSSIA
1PRESENT ADDRESS: SHIRSHOV OCEANOLOGY INSTITUTE, RUSSIAN ACADEMY OF SCIENCES (SOUTHERN BRANCH), GELENDZHIK, KRASNODAR DISTRICT
, RUSSIA
*CORRESPONDING AUTHOR: [email protected]
Biomass and productivity of microplankton were measured in the Craternaya Bay (Kurile Islands),
which is influenced by hydrothermal activity and volcanic heating. The hydrothermal fields are situated
around its shores and underwater within the 0–20 m depth. A dense ‘bloom’ of photoautotrophic
microplankton was observed there, dominated by diatoms, phytoflagellates and the symbiont-containing ciliate Mesodinium rubrum. The biomass of these ciliates attained 3–11 g m–3 in the upper
water layer. The total biomass of the phototrophic microplankton reached 30–46 g m–3. The primary
production in the water column was, correspondingly, enormously high: 6–10 g C m–2 day–1. The
depth of the euphotic zone was 7 m. Pelagic photosynthesis was inhibited in the upper 0–1 m by
the spreading of a layer of low-salinity hydrothermal water. The numerical density of bacterioplankton in the upper zone of the water column varied from 1 106 to 2.9 106 cells ml–1, and
its wet biomass from 250 to 750 mg m–3. Its production varied at stations from 70 to 390 mg m–3
day–1. Chemosynthesis contributed up to 30% of this production in the sites neighbouring the
hydrothermal vents. Outside their direct impact however, its share was negligible. The biomass of
heterotrophic planktonic ciliates varied from 30 to 270 mg m–3. The mechanisms of possible influence of shallow volcanic activity on development and function of microplankton in the Craternaya
Bay is discussed.
I N T RO D U C T I O N
The discharge of volcanic hydrothermal vents in the
bottom layer of seas and oceans has a pronounced
impact upon adjacent biological communities. The
hydrothermal waters are warm and of low salinity. They
are enriched with nutrients, with reduced sulphur
compounds, with methane and hydrogen gases, with
gaseous and liquid hydrocarbons, and with heavy metals
as well (Kononov, 1983; Italiano and Nuccio, 1991;
Tarasov et al., 1993; Dando et al., 1995, 1999; Robinson,
2000). In deep oceanic spreading zones, specific benthic
communities are formed, based energetically on the
chemosynthetic bacterial production (Karl et al., 1980;
Tuttle et al., 1982; Cavenaugh, 1983; Grassle, 1986; Gaill
et al., 1987; Gugliandolo and Maungeri, 1993; Van
Dover and Fry, 1994). The shallow oceanic ecosystems
influenced by hydrothermal discharges use both photo-
synthetic and chemosynthetic production as their
primary energy sources. As a result, algo–bacterial mats
are formed on the bottom in areas of sunlit shallow
hydrothermal activity (Tarasov and Zhirmunski, 1989;
Starynin et al., 1989; Namsaraev et al., 1989; Propp et al.,
1989; Tarasov et al., 1990; Sorokin et al., 1998). This type
of ecosystem exists in the Craternaya Bay, situated in the
caldera of the active Yankich volcano. The volcano
belongs to the Ushushir group of middle Kurile Islands
at 47°30N, 152°50W (Gavrilenko et al., 1989; Khristoforova, 1989a). The round-shaped Craternaya Bay is
about 1 km in diameter and has a maximum depth of
60 m. It is connected to the surrounding cold Sea of
Okhotsk by a narrow, shallow strait (Figure 1). Its
morphometric features resemble those of a fjord; its
water exchange with the sea is restricted by the sill uncovering during the ebb. The hydrothermal fields are
situated inside the bay around its shores, and also
Journal of Plankton Research 25(5), © Oxford University Press; all rights reserved
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Fig. 1. Position of stations in the Craternaya Bay; A, zone of hot hydrotherms; B, zone of cold hydrotherms; dotted area, sandy sublittoral near
the pass. The map shows position of the Ushushir Island in the Kurile Island arch.
underwater within the depth interval of 0–20 m. Daily
debit of thermal waters is close to 20 000 m3; they have
a temperature between 10 and 30°C and contain
hydrogen sulphide, elemental sulphur, heavy metals,
methane and hydrogen gases (Tchertkova and Guseva,
1986; Gavrilenko et al., 1989; Shulkin, 1989; Propp et al.,
1989). The heating of the bottom by the volcano results
in permanent convective mixing of the water column in
the bay, thus preventing formation of an anoxic
hydrogen sulphide zone, which usually exists in cold
marine fjords. The oxygen is transported into deeper
strata of the bay also with the cold, saline waters of the
Okhotsk Sea, which penetrate into the bay during the
flood tide, spreading over the bottom. Because of the
favourable oxygen conditions, the bottom area of the bay
harbours an abundant and diverse benthic fauna characterized by a biomass of several kg m–2 (Tarasov et al.,
1986). The benthic fauna is dominated by holothurians,
ceriantarians, polychaetes and clams, which feed mostly
on seston and algo–bacterial mats (Tarasov and Zhirmunski, 1989). In accordance with Nesterov et al. and
Starynin et al., the chemosynthetic bacteria, mostly
thiobacilli, contribute significantly to local autotrophic
organic production, which supports rich animal life
(Nesterov et al., 1991; Starynin et al., 1989). However,
Kharlamenko did not find the expected maxima of
bacterial production over the hydrothermal vents of the

bay (Kharlamenko, 1989), where intensive chemosynthesis had been reported by the other authors. Thus, the
problem of a real role for chemosynthesis in the energy
balance of this specific ecosystem remained disputable.
Another problem was the evaluation of the real level of
photosynthetic primary production by phytoplankton in
this bay. Previous attempts to measure it using the oxygen
bottle method failed (Nor, 1991). This method seems to
be unacceptable in conditions of oxygen oversaturation
(Propp et al., 1989). We investigated the problems
described above in the Craternaya Bay, aboard the R/V
‘Alexander Nesmeyanov’ in June 1990.
METHOD
Water samples were taken with a plastic water bottle at
seven basic stations (Figure 1). Station 1 was situated at 28 m
depth opposite the Sulfureta valley over the hot underwater
hydrothermal vents; station 1a was in the same place, close
to the shore at 3 m depth; station 2 was in the southeastern
part of the bay outside the hydrothermal zone; station 3 was
in the deep northwestern part of the bay in an area of cold
water vents at 55 m depth; station 4 was in the southwest of
the bay, near the pass, at 30 m depth; and station 5 was in
the northern part of the bay between two islands. Station 6
was situated in waters of the Okhotsk Sea outside the bay,
opposite the pass at 40 m depth.
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MICROPLANKTON IN THE HYDROTHERMAL CRATERNAYA BAY
The numerical abundance and biomass of phytoplankton and planktonic ciliates were estimated by epifluorescence microscopy on black, 1 µm pore-size Nuclepore
filters, stained with the fluorochrome primuline after
Caron (Caron, 1983). The zooflagellates were counted
similarly on 0.4 µm pore-size Nuclepore filters. The
planktonic bacteria were counted and sized using the
epifluorescence microscopy method of Hobbie et al.
(Hobbie et al., 1977). The biomass of microplankton
groups was expressed in wet biomass (biovolume).
Primary production in the water column was measured
using a radiocarbon method as modified by Sorokin
(Sorokin, 1999). The incubation of subsamples was
carried out in 300 ml bottles. To calculate the integrated
production in the water column, the following measurements were taken:
(i)
the absolute production rate in samples taken from
the surface layer (Cps mg C m–3 day–1),
(ii) the coefficient Kp, describing the dependence of
photosynthetic rate upon the vertical distribution of
active phytoplankton, and
(iii) the coefficient Kt, its dependence upon the light attenuation on vertical profile.
By multiplying these coefficients measured at corresponding depths, the coefficient Ks was found, which
describes the relative rate of photosynthesis in the water
column (Figure 2).
Bacterial production and chemosynthesis rates in
samples of water were measured with the use of a
modified CO2 dark uptake method (Sorokin, 1999). The
dark CO2 uptake (Ad) was measured in 250 ml bottles in
the intact water samples. The samples were kept in the
dark before injecting into them portions of ‘working’
isotope solution. The latter had an estimated radioactivity
of 15 106 counts min–1 (c.p.m.). The bottles thus
injected were incubated in the dark for 10–12 h at the
temperature in situ. After being fixed with diluted Lugol’s
solution, the samples were first prefiltered through 3 µm
Fig. 2. Parameters of stratification, hydrochemistry and water column photosynthesis at station 1; S, salinity, ‰; t°, water temperature, °C; O2,
dissolved oxygen, ml l–1; PO4, µM; Chl, chlorophyll content in water, mg m–3; Pp, photosynthesis rate, mg C m–3 day–1; Kp, distribution of active
phytoplankton (relative values); Kt, dependence of its photosynthesis rate upon light attenuation on vertical profile, both given as relative values; tr,
Secchi disk transparency.
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pore-size Nuclepore filters to eliminate the phytoplankton. Then they were filtered onto 0.4 µm pore-size
membrane filters that were rinsed in the funnel successively with sea water, then with 0.5% and 0.05% HCl
solutions in sea water. Their radioactivity was measured,
and the dark CO2 uptake by bacterioplankton (Ad) was
calculated. The rate of heterotrophic microbial production (Pbh) in the water of the Okhotsk Sea, taken at station
6 outside the influence of the volcano, was calculated as:
Pbh = Ad 12 mg C m–3 day–1, if Ad was expressed as mg
C m–3 day–1. In the samples taken in the Craternaya Bay,
where waters were influenced by the hydrothermal effluents, total microbial production (Pbt) was estimated as the
sum of Pbh and chemosynthesis (Pch): i.e. Ppt = Pbh + Pch
(Sorokin et al., 1998). For its evaluation, we measured dark
CO2 uptake in a series of samples taken through a vertical
profile at the given station (Adb) and also in one sample
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taken at station 6 outside the bay, where chemosynthetic
production was practically absent (Adi). Simultaneously,
the same sample series (plus a sample from station 6) were
taken into sterile 50 ml bottles for measuring relative functional activity of heterotrophic bacteria by estimation of
14C-labelled protein hydrolysate uptake. The value of P
bh
was then calculated:
P bh =
A di xR i x12
mg C m - 3 day - 1,
Ro
where Ri is the radioactivity of 14C-labelled hydrolysate
consumed by bacteria in samples from the Craternaya
Bay, and Ro is the corresponding value measured in the
sample taken outside the bay at station 6. Pch in this case
should be equal to:
Pch = Adb – [(Adb Ri)/Ro] mg C m–3 day–1
Table I: Distribution of phototrophic microplankton in water column; designations
Depth
N
Phytoplankton
(m)
(106 l–1)
Biomass of principal components (g m–3)
Mesodinium rubrum
Whole biomass
–––––––––––––––––––––––––––––––––––––––
––––––––––––––––––––––––––––
microplankton
(g m–3)
of phototrophic
Nanophyto-
Dino-
N
B
Diatoms
flagellates
flagellates
(103 l–1)
(g m–3)
Station 1
0
3.35
26.00
0.003
2
4.02
12.00
0.26
<0.02
3
0.15
26.17
0.20
190
9.50
21.96
4
7.85
12.83
7
5.75
7.90
0.80
0.24
123
6.15
20.02
0.50
<0.02
72
3.60
12.01
25
0.65
1.27
0.003
<0.02
3
0.15
1.43
1
2
6.27
25.10
0.27
0.10
220
11.00
36.47
3.80
2.80
0.53
0.07
60
3.00
6.40
0
13.36
40.26
0.25
0.08
116
5.80
46.39
7
3.83
6.38
0.30
0.13
140
7.00
13.81
12
2.17
3.35
0.15
0.10
9
0.45
4.05
25
1.27
1.00
0.14
<0.02
18
0.90
2.05
0
11.60
35.10
0.67
<0.02
0
0
35.78
5
2.15
11.00
0.15
<0.02
50
2.50
13.66
10
3.03
3.50
0.07
0.09
26
1.30
4.96
20
0.72
1.20
0.04
<0.02
3
0.15
1.40
50
0.45
0.07
0.03
<0.02
3
0.15
0.26
0
0.19
0.07
0.006
0.04
2
0.10
0.27
8
0.10
0.10
0.06
0.06
2
0.10
0.29
Station 1a
Station 2
Station 3
Station 6
N, numerical density; B, biomass.
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MICROPLANKTON IN THE HYDROTHERMAL CRATERNAYA BAY
The relative activity of heterotrophic bacteria on vertical
profiles was calculated as the ratio
P ch = A db -
A db xR i
mg C m - 3 day - 1
Ro
of Ri at the given depth to that measured in the surface
sample. The relative activities of some specific groups of
bacteria, such as the hydrogen and methane-oxidizing
bacteria and the thiobacilli, were evaluated using 14CO2
uptake rates measured in the presence of excess of,
respectively, hydrogen or methane gases, or thiosulphate
added into the samples (Sorokin, 1999). The data on
chlorophyll and nutrient content in the water were shared
by M. Propp.
R E S U LT S
Phytoplankton and primary production
During our observations, a phytoplankton ‘bloom’ was
present in the bay, as usual during the summer (Tarasov
et al., 1986). The upper water layer had a brownish colour
and was oversaturated with oxygen up to 160–180%. The
Secchi disc transparency was only 1.6–1.8 m, while in the
surrounding Okhotsk Sea it was 8 m. The phytoplankton
was dominated by diatoms of the genera Chaetoceros and
Thalassiosira. Their wet biomass in the euphotic zone
attained 20–40 g m–3 (Table I). The second significant
component was represented by small phytoflagellates
8–20 µm; their biomass attained 0.6–0.8 g m–3. It was
rather high also below the euphotic zone. Larger dinoflagellates also occurred with a biomass of 100–240 mg
m–3. Phototrophic microplankton also included the
symbiont-containing ciliate Mesodinium rubrum. This ciliate
is capable of active photosynthesis and functions as a
primary producer in planktonic communities (Taylor,
1971; Sorokin and Kogelshatz, 1979; Stoecker et al.,
1991). The biomass of this ciliate attained a ‘red tide’ level
in the layer of its accumulation between 2 and 7 m depth,
where it ranged from 2.5 to 11 g m–3 (Table I). Mesodinium
was absent from the upper brackish layer at station 1 in
the zone of hot hydrothermal vents, accumulating there
below 2 m depth. The same observation was made at
station 3. However, at station 2, outside the direct influence of hydrothermal activity, its maximal biomass (6 g
m–3) was recorded at the surface. The joint biomass of
phototrophic microplankton in the upper water layer
reached 20–46 g m–3. The chlorophyll concentration in
the layer of phytoplankton maximum reached 15–20 µg
l–1, thus corresponding to its dense bloom (Figures 2 and
4). The integrated biomass in the water column was 210
g m–2 at station 1, 320 g m–2 at station 2 and 237 g m–2
at station 3. At station 6 in the coastal Okhotsk sea water,
integrated biomass was 3.5 g m–2. The biomass of phytoplankton in the upper water layer at this station was
170–190 mg m–3 (Table II). Mesodinium was also found
there in minor amounts, being brought there, presumably,
from the bay with ebb water.
The phytoplankton biomass (Bp) was at its maximum in
the upper 0–3 m layer (see Bp curve, Figure 3). Its main
part was functionally inactive in the subsurface 0–1 m
layer (compare the biomass curve Bp in the same figure
with the Kp curve, which depicts the vertical distribution
of active phototrophic plankton). The daytime M. rubrum
maxima were recorded at a depth of 4–7 m, whereas, in
its massive blooms this maximum is usually situated at the
surface (Sorokin and Kogelshatz, 1979). These data
indicate that the phototrophic plankton is inhibited by
Table II: Pelagic photosynthetic production
Station
PMD
number
(m)
Photosynthetic production per day
–––––––––––––––––––––––––––––––––––––––––––––––––
(mg C m–2)
Specific production per day (µ)
––––––––––––––––––––––––––
In the water
––––––––––––––––––––––––––––––––––––––––––––
At the
At the
column
At the
At the
surface
PMD
(g C m–2)
surface
PMD
1
3
235
2715
6.67
0.15
0.85
2
2
1370
3180
9.80
0.47
1.10
3
3
489
1490
7.07
0.22
1.05
4
3
1300
2150
5.56
–
–
5
3
1530
1710
6.60
–
–
6
5
15
19
0.27
1.50
1.66
PMD, depth of photosynthesis maximum.
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Fig. 3. Phytoplankton biomass, including Mesodinium (Bp, g m–3, wet weight) on vertical profiles at basic stations; for Kp—see Figure 2.
hydrothermal waters spreading just in the upper 0–1.5 m
layer. The latter is evident from the salinity profiles
(Figures 2 and 4).
A significant part (40–80%) of the active phototrophic
microplankton inhabits a dark water layer below the
euphotic zone, e.g. below 6–7 m depth, (Kp curves, Figures
2 and 3). The share of this light-deficient phototrophic
microplankton corresponds to the ratio of the hatched
area of the graph (Figure 2) to its whole area outlined by
the curve Kp. The light deficiency might be escaped by
motile forms, such as Mesodinium and phytoflagellates
(Sorokin and Kogelshatz, 1979). The specific features of
the bay prevent their accumulation at the surface, where
the hydrothermal waters are spreading. The specific
growth rate of phytoplankton (µ) in this layer was two- to
five-fold less than in the layer of the photosynthetic
maximum (Table II). The latter was situated at a depth of
2–3 m, while the illumination optimum for photosynthesis
was situated at the surface (curve Kt), as was the biomass
maximum of phytoplankton. Phytoplankton cells in the
surface layer contained four to 30 times less chlorophyll
relative to cell carbon by comparison with those at 2 m
depth (Figure 4). The effect of an evident inhibition of
phototrophic microplankton in the surface 0–1 m layer
was caused, most probably, by the toxic effect of low
salinity hydrothermal water, containing reduced sulphur
compounds and heavy metals (Shulkin, 1989). Another
sequence of microplankton inhibition in the surface layer
is shown by the PO4-P vertical profile. Its minimum was
recorded at 2 m, where the photosynthesis rate was at its
maximum, but not at the surface (Figures 2 and 4). The
rate of photosynthesis at this depth approached the
record values known in natural marine basins: 1.7–3.2 g
C m–3 day–1. Integrated primary production through the
water column was 6.7–9.8 g C m–2 day–1 in the bay
(Table II). This level was documented earlier in productive areas of the Peruvian coastal upwelling (Sorokin and
Mikheev, 1979). Vigorous phytoplankton development
persists in the bay throughout the whole growth period
(Tarasov et al., 1986). The depth of the euphotic zone in
the Okhotsk Sea at station 6 was 30 m. The rate of photosynthesis in the upper layer at this station was 15–19 mg
C m–3 day–1, e.g. 100–200 times less than in the bay itself
(Table II).
Fig. 4. Same parameters as given in Figure 2, at station 3; NO3,
nitrates, µM.
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MICROPLANKTON IN THE HYDROTHERMAL CRATERNAYA BAY
Bacterioplankton, bacterial production and
chemosynthesis
The numerical density of bacterioplankton in the bay was
1.5 106 to 4.7 106 ml–1 in the upper 20 m layer of
the water column. Its wet biomass there ranged between
176 and 1130 mg m–3 (Table III; Figure 5). The mean
biovolume of bacterial cells was 0.20–0.25 µm3, which
was twice as great as that in the surrounding sea. The
bacterioplankton was distributed fairly evenly in the water
column. Its maximal density (4.73 106 ml–1) was
recorded at station 1a over the hot hydrotherms at 2 m
depth. This level of bacterioplankton density corresponds
to that in eutrophic marine coastal waters. The biomass
of bacteria in the Okhotsk Sea at station 6 was 66 mg m–3,
e.g. four to 10 times less than in the bay.
The most probable cause of high bacterioplankton
density in the bay is the high organic production by
phytoplankton in its waters. The latter conclusion is
supported by data on dissolved organic carbon content.
This attains 8 mg C l–1 in the euphotic zone of the bay
(Khristoforova, 1989b). The share of chemosynthetic
bacterial production in the accumulation of the bacterial
biomass in the water column of the bay was found to be
rather small. It becomes evident if we compare its values
at station 1 over the underwater hydrotherms, where a
significant chemosynthesis rate was recorded, with those
at stations 2 and 3, where it was practically absent
(Table IV). The chemosynthesis rate was almost two
orders of magnitude less than that of the photosynthetic
organic production even at this station. Total dark CO2
assimilation by bacterioplankton, including the chemosynthesis, was 18–30 mg C m–3 day–1 at the same station
(Table IV), in contrast to 1000–2000 mg C m–3 day–1 of
pelagic photosynthetic CO2 assimilation (Figure 5).
Total bacterial production in the upper 20 m of water
Table III: Numerical density (N) and wet biomass (B) of heterotrophic microplankton
Depth
Groups of planktonic microheterotrophs
(m)
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
Total biomass
of micro-
Bacterioplankton
Non-symbiotic ciliates
heterotrophs
(mg m–3)
Zooflagellates
––––––––––––––––––––––––
––––––––––––––––––––––––
––––––––––––––––––––––––
N
B
N
B
N
B
(106 ml–1)
(mg m–3)
(103 l–1)
(mg m–3)
(103 l–1)
(mg m–3)
Station 1
0
2.84
540
100
2
4
30
4
2.77
500
<20
<0.5
6
40
572
546
7
2.75
496
<20
<0.5
<1
<5
500
12
2.51
450
<20
<0.5
<3
20
470
25
1.47
176
<20
<0.5
<1
<5
177
Station 1a
1
3.92
900
30
2
10
80
982
2
4.73
1130
100
4
12
130
1264
0
2.90
760
140
7
3
20
787
7
2.87
746
100
4
14
210
960
12
2.81
731
50
3
6
72
806
25
1.48
237
20
1
2
15
253
661
Station 2
Station 3
0
1.82
387
700
24
26
250
10
2.20
507
60
2
15
120
629
20
1.76
335
80
3
3
24
372
30
1.45
290
210
7
4
28
325
50
1.29
258
400
16
6
35
309
Station 6
0
0.59
67
800
20
2
12
87
25
0.52
68
600
20
3
20
108
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Fig. 5. Bacterial biomass production and chemosynthesis at station 1
(22. 05); S, salinity, ‰; Bb, biomass of bacterioplankton, mg m–3, wet
weight; Ah, relative activity (%) of heterotrophic bacteria; Pbt, Pbh and Pch,
total bacterioplankton production, production of its heterotrophic part
and chemosynthetic production, all given as mg C m–3 day–1.
varied between 70 and 400 mg m–3 day–1 in wet biomass
units (14–80 mg C m–3 day–1). At the deep station 3, below
20 m, it decreased to 9 mg m–3 day–1 at 40–50 m depth
(2 mg m–3 day–1 in carbon units). In the Okhotsk Sea at
station 6 the bacterial production was 10 to 20 times less
compared with that in the bay. Kharlamenko estimated
bacterial production in the bay in August to be 8–19 mg
C m–3 day–1 in the upper layer and 1 mg C m–3 day–1 at
depths over 10 m (Kharlamenko, 1989). We did not detect
any significant difference in bacterial production upon the
presence (stations 1 and 1a) or absence (stations 2 and 3)
of chemosynthesis in the water column. Its share of the
whole bacterial production was 20 to 60% (Table IV;
Figure 6). The major part of this chemosynthesis was
contributed by heterotrophic bacteria in the zone of
shallow hot hydrotherms at station 1a, where chemosynthesis was rather high: 6–30 mg C m–3 day–1 (Table IV).
At station 2, situated some 300 m from station 1a,
detectable chemosynthesis (2 mg C m–3 day–1) was
recorded only in the surface layer, where the low-salinity
hydrothermal waters were spreading. In deeper waters it
was absent. These data indicate that active chemosynthesis is restricted within a narrow coastal zone of the bay
that is directly influenced by the hydrothermal discharge.
At station 1, where its rate was significant, it proceeded
throughout the water column with approximately the
same rate of 8–10 mg C m–3 day–1, which was very
unusual (Table IV; Figure 5). In this connection, the
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extremely high rate of dark CO2 uptake by microplankton in the water column of the bay (up to 100 mg C
m–3 day–1) claimed by Nesterov et al. was clearly an
artefact associated with methodological faults (Nesterov
et al., 1991). The principal among them perhaps being the
use of small 30 ml capacity penicillin bottles used for
subsample incubations. Whole dark assimilation thus
measured was related by these authors to the chemosynthesis. The contribution by thiobacilli and nitrifiers to the
total chemosynthesis production was estimated by them
with the use of specific inhibitors: sodium azide for the
thiobacilli and picalinic acid for the nitrifiers. We repeated
these experiments and found the same 80% of CO2 dark
uptake inhibition by sodium azide, and 3–8% by picalinic
acid at station 1 in the zone of hydrotherms where the
chemosynthesis was really present. However, we observed
the same effect of these inhibitors upon dark CO2 uptake
at station 6 in the open waters of the Okhotsk Sea, and
in the waters of the Sea of Japan, where CO2 is incorporated in the dark basically by heterotrophic bacterioplankton. These reagents similarly inhibited uptake of
labelled protein hydrolysate by the bacterioplankton.
Therefore, these inhibitors cannot be used for separating
heterotrophic dark CO2 uptake from chemosynthesis.
The coefficients of specific bacterioplankton production (µ) varied from 0.2 to 0.5 per day in the upper
0–20 m, decreasing to 0.03 – 0.05 in deeper water. This
level of specific production is quite significant if we take
into account the water temperature: 4–9ºC (Sorokin,
1981). The activity of specific groups of bacteria on
vertical profiles was determined at station 1 (Figure 6).
The lithotrophic thiobacilli were most active at 12 m
depth, and the hydrogen-oxidizing bacteria were most
active near the bottom. Active populations of methanotrophs and of heterotrophic bacteria were evenly distributed throughout the vertical profile.
Planktonic protozoa
The following major protozoan groups were quantified
separately: symbiotic ciliate M. rubrum (see Table I),
asymbiotic ciliates and zooflagellates (see Table III).
Mesodinium was dominant among the planktonic ciliates,
especially in the upper 0–10 m. It attained a biomass up
to 10–11 g m–3. The formation of dense populations in
the surface layer is a specific feature of migrating
phototrophic protozoans, ciliates and euglenoids, which
use photosynthetic production of symbiotic, or their
own, chloroplasts. The biomass of asymbiotic protozoans
was two to three orders of magnitude less (Table III). It
varied in the upper water layer from 30 to 270 mg m–3.
Maximal density of zooflagellates (4 105–7 105 cells
l–1) was recorded in the surface layer and near the bottom
at station 3.
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MICROPLANKTON IN THE HYDROTHERMAL CRATERNAYA BAY
Table IV: Relative activity of heterotrophic bacteria (Ha), total dark CO2 uptake by bacteria (At),
chemosynthetic and total bacterial production in water column
Depth
Ha
(m)
%
Ata
Bacterial productionb
Share of-
–––––––––––––––––––––––––––––––––––
chemo
Pbtc
Specific
bacterio-
Chemo-
Hetero-
Total
synthesis
plankton
synthetic
trophic
(Pbt)
in Pbt (%)
production
per dayd
Station 1
0
100
15.0
13.8
27.6
41.4
33
207
0.4
4
176
11.6
7.8
26.8
34.6
23
173
0.3
7
150
14.6
10.8
40.8
51.6
21
258
0.5
18
68
8.2
7.6
18.0
25.6
30
128
0.4
23
56
7.9
6.0
24.0
30.0
20
150
0.9
1
100
18.3
13.2
66.0
79.2
17
396
0.3
2
240
12.4
9.0
41.8
50.8
18
254
0.2
0
100
6.4
1.8
55.2
57.0
3
285
0.4
7
150
5.1
0
61.2
61.2
0
306
0.4
12
220
4.0
0
47.6
47.6
0
238
0.3
25
170
2.1
0
24.4
24.4
0
122
0.5
Station 2
Station 3
Station 4
0
100
2.2
0
26.8
26.8
0
134
0.3
10
144
4.5
3.2
38.4
41.6
8
208
0.4
30
80
0.4
0
2.6
2.6
0
13
0.05
50
120
0.2
0
1.8
1.8
0
9
0.03
Station 5
0
100
0.3
0
3.2
3.2
0
16
0.2
25
130
0.2
0
2.8
2.8
0
14
0.2
Units used are as follows: aAt (mg C m–3 day–1); bbacterial production (mg C m–3 day–1); cPbt (mg m–3 day–1of wet biomass); dproduction per day is µ.
DISCUSSION
The extremely high biological productivity of Craternaya Bay is shown both by its high pelagic primary
production (Table I), and by its dense benthic communities (Tarasov et al., 1986; Propp et al., 1989). It should be
related to the volcanic activity in the caldera in which the
bay is situated. However, how could volcanic activity
influence the productivity of the bay? One method seems
to be obvious—by analogy with the ecosystems of deep
oceanic vents. It is the chemosynthetic production of
organic matter by lithotrophic bacteria in the water
column, in bacterial mats, in upper layer of sediments
and in the bodies of symbiotrophic animals, which
harbour chemosynthetic bacteria. The hydrothermal
effluents contain reduced sulphur compounds and
methane and hydrogen gases, which are used as energy
sources for chemosynthesis by lithotrophic bacteria
(Sorokin, 1972; Bright et al., 1980; Jannasch, 1985;
Sorokin et al., 1998). The first data on the chemosynthesis rate in the Craternaya Bay were reported by Starynin
et al. (Starynin et al., 1989) and Namsaraev et al.
(Namsaraev et al., 1989). They suggested chemosynthesis
as an important trophic source in this bay but Kharlamenko failed to prove any significant role of chemosynthesis in the water column of Craternaya Bay
(Kharlamenko, 1989). The total microbial production
measured using the thymidine method varied in his
experiments from 8 to 19 mg C m–3 day–1, independently
of the location of sampling sites in relation to
hydrotherms. Our measurements (Table IV) demonstrate
a maximal dark CO2 uptake rate (Ad) of 18 mg C m–3

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Fig. 6. Relative activity (%) of specific physiological groups of water
column bacteria at station 1; Ah, Am, Ahg, and At, heterotrophic, methaneoxidizing bacteria, hydrogen-oxidizing bacteria and thiobacilli, respectively.
day–1 at station 1a in the zone of hot shore hydrotherms.
However, roughly 60% of this uptake was heterotrophic,
but not chemosynthetic. The level of total bacterial
production did not depend closely upon the chemosynthesis. Its maximal value (60 mg C m3 day–1) was
recorded at station 3, where the latter was practically
absent. The share of chemosynthesis in total bacterial
production was only 20–50%, even in areas where it was
most intense. The rates of chemosynthesis in the
hydrothermal area at stations 1 and 1a did not show any
maxima in the vertical profiles (Table IV; Figure 5). In
this, the Craternaya Bay differs from other water bodies,
where chemosynthesis in the water column is recorded
and has its maxima in the redox-zone (Sorokin, 1972,
1981). The cause of this difference is the geothermal
mixing of the water column in the bay.
In sunlit shallow zones of seas and oceans influenced
by volcanic activity, the bottom is usually covered with
algo–bacterial mats, formed by mixed algal–bacterial
communities. The main producers of organic matter in
these mats are mostly cyanobacteria and photosynthetic
sulphur
bacteria,
together
with
filamentous
chemolithotrophic sulphur bacteria. In the Craternaya
Bay such mats occupy the bottom in the zone of hot
hydrothermal vents in its eastern part around stations 1
and 1a between the depths of 2 to 20 m (Starynin et al.,
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1989; Namsaraev et al., 1989). These authors report
extremely high values of dark CO2 uptake in the mats: up
to 20–29 g C m–2 day–1. They attributed this uptake to
chemoautotrophic bacteria. These conclusions also seem
to be an artefact. Indeed, the microbial community would
have to use 200–300 g m–2 of oxygen per day to support
such a high autotrophic CO2 uptake. It would then result
in the formation of zero oxygen zones in the bottom water
layer within several hours. However, oxygen deficiency
was never observed in the water column of the bay, even
in the areas of most abundant mats around station 1
[(Propp et al., 1989); see Figure 2]. The real chemosynthesis rates in mats cannot be more than 0.05–0.1 g C m–2
day–1 in accordance with our estimates of bacterial
biomass in the mats and their specific production rates. In
the bay, mats occupy only a restricted zone around the
hydrothermal zone near station 1 (Propp et al., 1989). The
water column chemosynthesis, being located also in the
same area, is practically absent from the larger part of the
bay (Table IV). Therefore the share of chemosynthesis in
total autotrophic production in the bay cannot be more
than 2–3%. Basic primary organic production (over 90%)
is created there by the planktonic phototrophs, and some
3–5% by benthic microalgae in the mats. Thus, the
proposed dominant role of chemosynthesis in the
ecosystem of the Craternaya Bay, suggested by the
researchers above, cannot be accepted.
An alternative explanation for the stimulating effect of
volcanic activity upon the productivity in this bay might
be the acceleration of photosynthetic planktonic production. Its rate in the euphotic zone was about 100 times
greater than that of the chemosynthesis: 1000–2000 mg
C m–3 day–1 compared with 8–30 mg C m–3 day–1 (Tables
II and IV). Bacterial biomass up to 200 mg C m–3
accumulated in the water column basically as a result of
heterotrophic microflora using pelagic photosynthetic
production (Table IV). The content of dissolved organic
matter in the bay was 5–8 mg C l–1, i.e. three to four times
greater than in the surrounding sea (Khristoforova,
1989b). The volcanic activity creates conditions for an
almost permanent bloom of planktonic phototrophs in
the bay. Furthermore, there is acceleration of nutrient
fluxes up to the euphotic zone because of the geothermal
mixing combined with the support of water column
stratification within the euphotic zone at 3–5 m depth.
The latter keeps the phytoplankton population (and
especially heavy diatoms) in the illuminated layer. These
processes oppose each other because the stratification
slows down the turbulent mixing, which itself drives
upward turbulent nutrient flux. Optimal conditions for
phytoplankton growth appear when upwelling supports a
pycnocline in the middle part of the euphotic zone, where
light is still available. When upwelling decreases, the
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MICROPLANKTON IN THE HYDROTHERMAL CRATERNAYA BAY
pycnocline boundary is driven down under the influence
of solar heating. In the upwelling areas of the world
ocean, where these optimal conditions exist for rather
long periods, massive phytoplankton blooms develop. In
such zones of quasipermanent blooming, the thermocline
is situated at 8–15 m depth, while the PO4-P content in
the blooming water is often maintained at the lower limit
for phytoplankton growth (0.1–0.2 µM). However, the
phosphate upward flux to the euphotic zone is fast enough
to support primary production in the water column at the
level of 7–9 g C m–2 day–1 (Sorokin and Mikheev, 1979;
Eppley, 1981). The situation, when the pycnocline
descends to the boundary of the euphotic zone in
upwelling areas, often provokes red tide blooms of large
dinoflagellates, such as Gymnodinium, or of the symbiontcontaining ciliate M. rubrum, which accomplish long
diurnal vertical migrations (Sorokin and Kogelshatz,
1979; Crawford, 1989). These fast-moving protozoa
migrate by day up to the surface for light. At night their
populations migrate down below the thermocline for
nutrients.
In the Craternaya Bay the pycnocline is situated within
the euphotic zone between 2 and 6 m depth (Figures 2
and 4). Therefore, the above-mentioned conditions of
stratification and hydrodynamics characteristic of
productive coastal upwelling areas, also exist there, being
supported by the energy of volcanic heat. This warms the
bottom water, thus inducing upward flow and vertical
convection, resulting in elevation of the pycnocline
boundary up to the euphotic zone. Another factor is the
spreading of low-salinity warm hydrothermal waters from
coastal vents across its surface (Figures 2 and 4). The
shallow pycnocline supported by the volcanic heating is
the principal factor that provides this remarkably high
pelagic and benthic production in the semi-closed and
rather deep Craternaya Bay. This mechanism cannot
work in most open sunlit shallow coastal areas of
hydrothermal venting because of hydrodynamic turbulence. The stimulating effect of venting upon the phytoplankton density and on its photosynthetic production is
less pronounced, or not detectable at all, in such habitats
(Lucila et al., 1996; Sorokin et al., 1998; Robinson, 2000).
The nutrient influx into coastal waters of venting areas
from hydrothermal waters is well-documented (Dando et
al., 1999). Indeed, the nutrient content in waters of the
bay was significantly greater than in the surrounding
Okhotsk Sea (Propp et al., 1989). Concerning the sources
of nutrients in the bay, both the hydrothermal waters and
the terrigenous drainage from the volcanic rocks were
indicated (Propp et al., 1989). Besides, the existence of
some biological mechanisms might be supposed, which
stimulate accumulation of nutrients in a similar way as
occurs in fjord-like bays with a shallow sill at their
entrances. Nutrients in their inorganic and organic
dissolved and particulate forms are driven into the bay
from the surrounding sea with the tide waters. The highly
dynamic microplankton community rapidly consumes
them. Being incorporated into the food web, these nutrients then accumulate in the biomass of pelagic and
benthic filtering fauna, and in detritus and faeces, which
sediment down to the bottom. This process results in
accumulation of organic nitrogen and phosphorus in the
deeper water layers and in bottom sediments. The ebb
outflow drives out from the bay mostly the upper waters,
poor with nutrients (Figures 2 and 4). It results in an
inward nutrient flux during the tidal water exchange
between such bays and the surrounding sea. The stock of
organic nutrients accumulating in them, being mineralized via the food web, gradually enters the productivity
cycle again. A semi-closed turnover of nutrients, together
with the above-mentioned external sources of their
supply, create the situation in which nutrient limitation in
the euphotic zone of the bay is absent despite the highest
possible rate of autotrophic organic production. The
stock of particulate food in the form of microplankton
biomass, and the rate of its production in waters of the
bay, are extremely high (Tables I to IV). They support an
abundant and diverse benthic fauna dominated by filterers and sediment-feeding animals (Tarasov et al., 1990,
1993). The chemical composition of hydrothermal waters
is drastically variable in different shallow venting areas.
Similarly variable are their stimulating or inhibiting
effects upon the pelagic communities (Sorokin et al., 1998;
Dando et al., 1999; Robinson, 2000).
AC K N O W L E D G E M E N T S
The authors thank V. Tarasov for various help and support
of this study, L. Propp and M. Propp for sharing hydrochemical data and P. Gellespie for sharing equipment.
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Received on March 13, 2002; accepted on January 16, 2003