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03 sorokin fbg021 (ds) 23/4/03 9:30 pm Page 495 JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒ 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 03 sorokin fbg021 (ds) 23/4/03 9:30 pm Page 496 JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒ 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. 03 sorokin fbg021 (ds) 23/4/03 9:30 pm Page 497 YU. I. SOROKIN, P. YU. SOROKIN AND O. YU. ZAKOUSKINA 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. 03 sorokin fbg021 (ds) 23/4/03 9:30 pm Page 498 JOURNAL OF PLANKTON RESEARCH VOLUME 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 NUMBER PAGES ‒ 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. 03 sorokin fbg021 (ds) 23/4/03 9:30 pm Page 499 YU. I. SOROKIN, P. YU. SOROKIN AND O. YU. ZAKOUSKINA 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. 03 sorokin fbg021 (ds) 23/4/03 9:30 pm Page 500 JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒ 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. 03 sorokin fbg021 (ds) 23/4/03 9:30 pm Page 501 YU. I. SOROKIN, P. YU. SOROKIN AND O. YU. ZAKOUSKINA 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 03 sorokin fbg021 (ds) 23/4/03 9:30 pm Page 502 JOURNAL OF PLANKTON RESEARCH VOLUME 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 NUMBER PAGES ‒ 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. 03 sorokin fbg021 (ds) 23/4/03 9:30 pm Page 503 YU. I. SOROKIN, P. YU. SOROKIN AND O. YU. ZAKOUSKINA 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 03 sorokin fbg021 (ds) 23/4/03 9:30 pm Page 504 JOURNAL OF PLANKTON RESEARCH VOLUME 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., NUMBER PAGES ‒ 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 03 sorokin fbg021 (ds) 23/4/03 9:30 pm Page 505 YU. I. SOROKIN, P. YU. SOROKIN AND O. YU. ZAKOUSKINA 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. 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