Abstract

In order to clarify the importance of the microbial food chain in relation to the grazing food chain in the Oyashio region, western subarctic Pacific, the biomass of component organisms in the two food chains was investigated during July and October in 1997, and January, March and May in 1998. Carbon flows within the plankton food chains, as established from biomass data combined with published experimental data (Shinada et al., 2000), suggest that primary production is largely channelled through the microbial food chain throughout the year. The grazing food chain is functional along with the microbial food chain only during the spring phytoplankton bloom.

INTRODUCTION

In marine ecosystems, solar energy fixed photosynthetically into organic matter by phytoplankton is channelled to higher trophic levels via two routes. One is the grazing food chain consisting of microphytoplankton (>10 μm) and mesozooplankton (>200 μm). The other is the microbial food chain, which includes components such as pico-, nano- and microphytoplankton, heterotrophic bacteria and protozoans (Fenchel, 1986). Grazing food chains transfer organic matter from surface waters to the interior of the ocean through the production of large, compact and fast-sinking faecal pellets by mesozooplankton (von Bodungen, 1986; Fortier et al, 1994), and the efficient transfer of organic carbon from low to high trophic levels (Fortier et al., 1994 ). On the other hand, phytoplankton production entering the microbial food chain contributes less to vertical particulate fluxes and to high trophic levels because of the smaller faecal pellets in these plankton, which remain in suspension for long periods, and higher metabolic rates of protozooplankton (Nöthig and von Bodungen, 1989; Gonzalez, 1992). Studies of plankton food chains are of great importance in understanding the biological productivity of marine systems in terms of their efficiency and yield to higher trophic levels.

Although the subarctic Pacific has long been known as highly productive, there are some differences in ecological features between the western and eastern parts (Saito et al., 1998; Harrison et al., 1999). A pronounced spring phytoplankton bloom does not occur in the eastern North Pacific (Frost, 1991; Miller, 1993), while spring blooms are a regular annual event in the Oyashio region, the southernmost part of western subarctic Pacific (Kasai et al, 1997; Shinada et al., 1999). High nutrient and low chlorophyll (HNLC) conditions have been found in both areas (Miller et al., 1991; Saito et al., 1998). Two major hypotheses have been proposed to explain the HNLC phenomenon; iron limitation (Martin and Fitzwater, 1988; Boyd et al., 1996) and microzooplankton grazing (Miller et al., 1991; Boyd et al., 1995b). Hence, a clear description of the structure and function of planktonic communities is a step towards a better understanding of production processes in the subarctic Pacific.

The Oyashio current forms the western boundary of the subarctic circulation flowing southwestward along the Kurile Islands (Ohtani, 1970). The Oyashio region is characterized by high primary production (Taniguchi and Kawamura, 1972) and high zooplankton biomass (Hattori, 1991; Odate, K., 1994, and is regarded as one of the most productive fishery areas in the world (FAO, 1997). Taniguchi (Taniguchi, 1991) speculated that the grazing food chain may be the main pathway of primary production, as in the case of upwelling regions. While information about microzooplankton (Dohi, 1982; Odate and Maita,1990) and picophytoplankton (Odate, 1989) is available in Funka Bay, no studies have been made on all components of microbial and grazing food chains in the Oyashio Current.

In this study, we investigated the biomass of planktonic organisms in the Oyashio region, including all major components of microbial and grazing food chains in all seasons of the year. These results, combined with those of dilution experiments (Shinada et al., 2000), are used to establish a carbon-flow model and the relative importance of the two food chains is discussed.

METHOD

Field samplings

Samplings were carried out at station A3 (40°30′N, 145°E) in the southern part downstream of the Oyashio Current during July and October in 1997 and January, March and May in 1988 (Figure 1). Water samples were collected from depths of 10, 20, 30, 50, 100 and 200 m with Niskin bottles for enumeration of heterotrophic bacteria, cyanobacteria, picophytoplankton, nanoflagellates and microzooplankton. Surface water samples were collected with a plastic bucket. Samples for pico- (<2 μm) and nanoplankton (2–10 μm) were preserved with 1% glutaraldehyde (final concentration). Microplankton (10–200 μm) samples were fixed with a mixture of alkaline Lugol's solution, formalin and sodium thiosulphate (Sherr and Sherr, 1993). Mesozooplankton (>330 μm) was collected with a Bongo-type net (30 cm mouth opening, 3 m long and 330 μm mesh). The nets were towed vertically from the bottom of the mixed layer to the surface. The depth of the bottom of the mixed layer was estimated from CTD records. During winter and early spring, when the mixed layer was indistinguishable, the nets were towed from 50 m depth. The nominal filtering efficiency of the net was 1.0 (Saito et al., 1998). Water column temperature and salinity were recorded from 0 to 200 m using a CTD system (Sea Bird19).

Abundance estimation

Heterotrophic bacteria were stained with 4′, 6-diamidino-2-phenylindole (DAPI) and filtered onto 0.2 μm black Nuclepore filters. At least 400 cells on each filter were counted with an epifluorescence microscope at a magnification of 1000×. Bacterial cell volume was calculated from the length and width of >30 photographed cells. The cell volumes were converted to carbon units using a conversion factor of 0.209 pg C μm–3 (Kogure and Koike, 1987).

Cyanobacteria were filtered onto 0.4 μm black Nuclepore filters. At least 100× autofluorescent cells were counted at a magnification of 1000× on each filter. Cyanobacterial cell volume was calculated from cell diameter measurements on >100 cells per filter made with an ocular micrometer. Cell volumes (V, μm3) were converted to carbon units (C, pg C μm–3) using the formula; log10C = 0.863 log10V – 0.363 (Verity et al., 1992).

Pico- and nanophytoplankton and heterotrophic nanoflagellates (HNF) were counted using epifluorescence microscopy after staining with DAPI and proflavine hemisulphate (Haas, 1982). Samples were filtered onto 1.0 μm black Nuclepore filters. Discrimination between autotrophic algae and HNF was facilitated using green excitation to reveal pure chlorophyll autofluorescence. At least 100 cells were counted on each filter at a magnification of 1000×. Cell volumes were calculated from length and width measurements of >30 cells per filter using an ocular micrometer. The cell volumes were converted to carbon units using the above-mentioned formulae for pico- and nanophytoplankton (Verity et al., 1992) and a conversion factor of 0.22 pg C μm–3 for HNF (Børsheim and Bratvak, 1987).

Microplankton were counted with an inverted microscope after the samples had been left to settle overnight. Autotrophic and heterotrophic flagellates were discriminated by epifluorescence microscopy. Biovolumes were estimated from measurements of lengths and widths of organisms and assuming simple geometrical shapes. Cell volumes (V, μm3) of diatoms were converted to cell carbon (C, pg C) using the formula ; log10C = 0.758 log10V – 0.422 (Strathmann, 1967). The cell volumes of naked ciliates were converted to carbon using a conversion factor of 0.19 pg C μm–3 (Putt and Stoecker, 1989), and those of naked and thecate flagellates were converted using conversion factors of 0.11 and 0.13 pg C μm–3, respectively (Edler, 1979). To convert biovolumes to carbon units, a formula proposed for tintinnids (Verity and Langdon, 1984) and the factor of 0.05 pg C μm–3 proposed for nauplii (Mullin, 1969) were adapted.

Mesozooplankton were sorted to and counted to major systematic groups such as copepods, euphausiids, appendicularians, chaetognaths, amphipods, medusae. Then, wet biomass of each systematic group was determined, and converted to carbon, assuming a carbon to wet volume ratio of 0.05 pg C μm–3 (Mullin, 1969).

Carbon budget

Total phytoplankton production (PP) in the euphotic layer was calculated as

 

\[\mathbf{PP}{=}\ \mathbf{PB}{[}exp({\mu})\ {-}\ 1{]}\ {\times}\ A\]

where

 

\[A\ {=}\{{[}1\ {-}\ exp({-}\mathit{k}z){]}/\mathit{k}{]}\}/(0.5z)\]

and PB denotes the mean phytoplankton biomass in the euphotic layer (mg C−3, and m is the phytoplankton growth rate (day–1) derived from dilution experiments conducted at ca. 50% of the surface light intensity [cf. (Shinada et al., 2000)]. A is a factor to adjust total phytoplankton production, taking into account the progressive decrease of light intensity with depth; and k is the extinction coefficient calculated from the Secchi disc reading (SD) i.e. k = 1.7/SD (Poole and Atkins, 1929). The primary production of size-fractionated were estimated from size-fraction biomass data assuming that phytoplankton primary production is directly proportional to biomass. The phytoplankton sedimentation flux (PS) was calculated as a function of PP as PS = 0.049PP1.41 (Wassmann, 1990).

Bacterial production (BP) in the euphotic layer was computed from bacterial numbers (BNUMS, cells ml–1); log10 BP = 1.124 log10 BNUMS – 0.608 (Cole et al., 1988).

Nano- and microzooplankton grazing on phytoplankton (MG, mg C m–3 day–1) in the euphotic layer was estimated from the dilution experiments (Shinada et al., 2000) as MG = g{PB[ exp(μ − g) – 1]}/(μ − g) where the g (day–1) is the instantaneous grazing rate.

Protozooplankton respiration (Rp, nl O2 ind.−1 h−1) was calculated from body volume (V, μm3), as log10 Rp = 0.75 log10V – 4.09 (Fenchel and Finlay, 1983). A Q10 of 2.5 was adopted for temperature correction (Caron et al., 1990). Mesozooplankton and naupliar respiration (Rm, μl O2 ind. h−1) were calculated as a function of body mass (CW, mg C ind.–1) and temperature (T, °C), i.e. ln Rm = 0.5254 + 0.8354 ln CW + 0.0601 T (Ikeda, 1985).

Production and food requirement of protozooplankton and mesozooplankton (copepods and euphausiids) were calculated from their respiration rates, assuming the respiratory quotient (RQ) to be 0.97 (Gnaiger, 1983); and net growth efficiencies to be 0.25 for heterotrophic dinoflagellates and 0.5 for ciliates, HNF and the other protozooplankton. Gross growth efficiencies are assumed to be 0.3 for nauplii and mesozooplankton; assimilation efficiencies as 0.8 for all the protozooplankton and nauplii and 0.7 for mesozooplankton (Ikeda, 1985; Witek et al., 1997).

RESULTS

Oceanographic conditions

The surface temperature ranged from 1.5°C in March 1998 to 12.1°C in October 1997 (Figure 2). The thermocline was well developed in October, when the surface water temperature was high, but it was not evident at the other sampling occasions. Surface salinity ranged from 32.7 psu in May 1998 to 33.2 psu in October 1997. A halocline was observed in July 1997, when low salinity was observed above 20 m (32.8 psu). Therefore, a strong pycnoline was established in July and October 1997, mainly due to salinity and temperature gradients, respectively. No pycnoline was evident in January and March 1998. In May 1998, the stability of the water column increased slightly with depth.

Vertical structure of plankton biomass

Over the study period, the depth of the euphotic layer varied from 14 to 43 m (Figure 2). During the stratified period (July, October and May) the euphotic layer was shallower than 30 m, while it was deeper during the mixing period (January and March). An appreciable portion (59–75%) of the total biomass of autotrophs in the 0–200 m water column was distributed in the top 30 m during the stratified period, while the biomass of autotrophs extended below 30 m during the mixing period.

The highest biomass of heterotrophs was observed in the euphotic layer throughout the year, except for May 1998. During the stratified period, 40–62% of total biomass of heterotrophs in the 0–200 m water column was found in the top 30 m of the water column. During the mixing period, the biomass of heterotrophs exhibited broad distribution with depth, as observed for autotrophs.

Seasonal changes in autotrophic plankton

The biomass of autotrophic plankton in the euphotic zone (integrated 0–30 m in July, October 1997 and May 1998; 0–50 m in January and March 1998) varied from 8 mg C m−3 in March to 418 mg C m−3 in May (Figure 3). Biomasses exceeding 100 mg C m−3, as observed in October 1997 and May 1998, were due to the predominance of microphytoplankton (>79%) which consisted mainly of diatoms. On the other occasions, the autotroph biomass was relatively low (<63 mg C m–3), and nanophytoplankton were the major component (>63%). The contribution of picophytoplankton to autotroph biomass was low (<18%) throughout the entire sampling period. The major picophytoplankton taxa, such as cyanobacteria and eukaryotic picophytoplankton, were almost equal in abundance. For microphytoplankton, diatoms were the most important component, followed by naked flagellates and thecate flagellates.

Seasonal changes in heterotrophic plankton

The biomass of heterotrophic plankton in the euphotic zone ranged from 29 mg C m−3 in January 1998 to 246 mg C m−3 in May (Figure 4). Ranges of seasonal variations of each component were 12–51 mg C m−3 for bacteria, 2–40 mg C m−3 for HNF, 4 to 55 mg C m−3 for microzooplankton and 39–150 mg C m−3 for mesozooplankton. Naked ciliates were the most abundant in microzooplankton throughout the year (35–70%), followed by naked flagellates, which were dominant in October 1997 and May 1998 (19–40%). The biomasses of nauplii and thecate flagellates were relatively high in October 1997 and May 1998, when diatom blooms were observed. Mesozooplankton comprised ca. 60% of the total heterotrophic plankton biomass in May 1998. Although copepods were dominant in the total mesozooplankton biomass in July and October 1997 and May 1998, euphausiids became the dominant component of total mesozooplankton biomass in January and March 1998.

Carbon flow diagram

To illustrate seasonal features of the Oyashio region, we divided the year into four seasons based on water column structure and phytoplankton abundance; ‘summer’ – stratified water column and low phytoplankton biomass (July 1997), ‘fall’ – stratified water column with diatom blooms (October 1997), ‘winter’ – well-mixed water column and low phytoplankton biomass (January, March 1998) and ‘spring’ – stratified water column with diatom blooms (May 1998).

During the summer, pico- and nanophytoplankton production contributed 93% of the total phytoplankton production (Figure 5). Bacterial production was also high, about 18 times higher than microphytoplankton production. The nominal food requirement of microzooplankton was about 5.8 times greater than that of mesozooplankton.

In the fall, microphytoplankton production was again high (93% of the total estimated phytoplankton production), about 3.3 times greater than bacterial production. The biomass and food requirement of microzooplankton were about three- and eight-fold higher than those of mesozooplankton, respectively. The grazing of microzooplankton was eight-times the pico- and nanophytoplankton production.

In the winter, pico- and nanophytoplankton production comprised 79% of the total phytoplankton production. Bacterial production was also seven times higher than that of microphytoplankton. The food requirement of microzooplankton was 10 times higher than that of mesozooplankton. The food requirement of mesozooplankton was not met by microphytoplankton production.

As a notable feature in spring, microphytoplankton production was very high (98% of the total phytoplankton production), being eight times higher than the bacterial production, indicating that microphytoplankton was the major primary producer during spring. In contrast to other seasons, mesozooplankton biomass was twice that of the microzooplankton. Food requirements of mesozooplankton exceeded the production of microzooplankton, but were less than that of phytoplankton production. At the same time, microzooplankton grazing on phytoplankton was very high, though the grazing may be overestimated due to the use of the data derived from dilution experiments. The dilution experiments deal with systems in which mesozooplankton was removed, but there is evidence that simultaneous predation by copepods may account for over 50% of daily ciliate production (Atkinson, 1996).

DISCUSSION

Biomass conversion factors and flow calculation

The choice of a conversion factor for converting microbial biovolume to biomass had a major effect on the estimated relative importance of each assemblage to particulate carbon in water. However, it was difficult to select the correct factor because the variability may have been caused by physiological conditions or methodological problems. Therefore, we selected the conversion factors used in roughly similar environmental condition such and/or generally accepted conversion factors.

In this study, the phytoplankton sedimentation and bacterial production were calculated using the formulae from the literature (Wassmann, 1990; Cole et al., 1988). For phytoplankon sedimentation, we selected the formula designed for roughly similar environmental conditions. While the bacterial production was compared with survey value taken off Esan near to Oyashio region (Shinada, 2000). Consequently, while a good relationship was observed in spring and fall, the calculation values were two or three times underestimated in summer and overestimated in winter compared with the survey values, respectively.

Plankton food chain structure in the Oyashio region

The present results revealed both similarities and dissimilarities in the features of the planktonic community in the Oyashio region as compared to other regions. The occurrence of two phytoplankton blooms (spring and fall) in the Oyashio region has been reported previously (Saito et al., 1998). Throughout the subarctic Pacific, phytoplankton blooms are limited to areas off Washington/California and the Oyashio. The vast deep water central region is a High Nutrient/Low Chlorophyll (HNLC) zone (Banse and English, 1999). Spring and fall phytoplankton blooms are also observed in the North Atlantic (Parsons and Lalli, 1988), but are dominated by different phytoplankton species. Diatoms are prominent in the Oyashio region [(Shinada et al., 1999) and this study], while prymnesiophytes dominated in the North Atlantic (Sieracki et al., 1993). The onset of the Atlantic spring bloom, results in a rapid decrease of silicate (to 0.5 mM) (Sieracki et al., 1993), while high silicate concentrations (5.2–40.8 mM) remain throughout the Oyashio phytoplankton bloom (Saito et al., 1998). Thus, high silicate concentrations during the spring bloom may be one of the key factors in the continual diatom dominance in the Oyashio.

In summer, the low contribution of picophytoplankton to total phytoplankton biomass (Figure 3), contrasts with the results of previous studies in various regions in the subarctic Pacific. In Funka Bay, southwestern Hokkaido, cyanobacteria are the major picophytoplankton component (Odate et al., 1993). The same was reported from the northern North Pacific Ocean (Odate, 1994) and in the northeast subarctic Pacific (Booth et al., 1993). Correlations have been noted between the cyanobacterial abundance and temperature (Murphy and Haugen, 1985), but temperatures in the Oyashio region and these other regions do not differ appreciably (ca. <12°C), except for Funka Bay (ca. >20°C). Clearly, the other factors, such as nutrients or microzooplankton grazing, must be responsible for the lower contribution of cyanobacteria to picophytoplankton biomass in the Oyashio region. In the other seasons, nanophytoplankton dominated the biomass in Oyashio, similar to the seasonal pattern in the northeast subarctic Pacific (Booth et al., 1993) and the North Atlantic (Joint et al., 1993; Sieracki et al., 1993).

The bacterial biomass in the Oyashio region was high in July 1997 and May 1998, and low in October 1997, January and March 1998 (Figure 4). The bacterial growth rate is known to increase with temperatures and concentrations of dissolved organic matter (DOM) (Kirchman et al., 1993). In January and March 1998, the water temperatures of the present study site were low (<5°C, at the surface). DOM concentrations were not determined in this study but were considered to be lower when phytoplankton production was light-limited. Higher DOM concentrations could be expected in July, October 1997 and May 1998 since these samplings were during, or just after, the diatom blooms. These favourable sets of environmental conditions may explain why bacterial biomass increased in July 1997 and May 1998. The bacterial biomass in October 1997 was low despite suitable environmental conditions. Although HNF are considered to play an important role in regulating bacterial abundance (Azam et al., 1983; Sherr et al., 1986), HNF biomass was relatively low in October 1997 (Figure 5). Recent studies have shown that appendicularians can graze on a large size-range of particles, from colloidal (ca. 0.2 mm) to 54 mm (Alldredge, 1976; Flood et al., 1992), and exhibit extremely high growth potential (Paffenhöfer, 1973; Nakamura et al., 1997). A relatively high appendicularian biomass was observed in the Oyashio region in fall (Shichinohe, 2000). These results suggest that appendicularians grazing on bacteria, instead of HNF, could be a possible cause for the lower bacterial biomass in October in the Oyashio region.

Microzooplankton assemblages in the Oyashio region were dominated by naked ciliates (Figure 4). This is consistent with the results from the northeast subarctic Pacific (Booth et al., 1993), the North Atlantic (Verity et al., 1993) and the Southern Ocean (Froneman et al., 1997). Microzooplankton biomass was highest during the diatom blooms. This close association between high microzooplankton and phytoplankton biomass has been observed in the North Atlantic (Verity et al., 1993) and in the Baltic Sea (Smetacek, 1981; Hansen, 1991). No clear seasonal trends of microzooplankton biomass have been reported in the northeast subarctic Pacific which lacks phytoplankton blooms (Booth et al., 1993; Strom et al., 1993; Boyd et al., 1995a).

Pico- and nano-size prey have been considered as the most suitable food for microzooplankton (Hansen et al., 1994; Peters, 1994). This prey–predator relationship does not explain the higher microzooplankton biomass, although microphytoplankton (diatoms) was dominant during the observed phytoplankton blooms in spring and fall in the Oyashio region (Figure 3). In addition to the nanophytoplankton–microzooplankton link, microzooplankton (flagellates and naked ciliates) also graze on microphytoplankton (Smetacek, 1981; Gifford, 1985; Capriulo et al., 1988; Hansen, 1992; Strom and Strom, 1996). It is quite likely that the observed high microzooplankton biomass in the Oyashio reflects their grazing on not only nano- but also microphytoplankton (diatoms).

The maximum biomass of mesozooplankton in the Oyashio coincided with the spring diatom bloom (Figure 4). The coincidence of mesozooplankton and phytoplankton blooms differs from the seasonal pattern observed in the North Atlantic. In the North Atlantic, the biomass of mesozooplankton peaks 1 month after the phytoplankton bloom (Parsons and Lalli, 1988). Copepods are the major component of mesozooplankton in both the Oyashio region and the North Atlantic [Figure 4 (Parsons and Lalli, 1988)]. In the Oyashio region, Neocalanus is the dominant copepod genus, while Calanus is the most important component of the copepod biomass in the North Atlantic (Parsons and Lalli, 1988; Colebrook, 1982). There are significant differences in the life cycle of Neocalanus and Calanus copepods (Parsons and Lalli, 1988). Spawning of Neocalanus takes place by utilizing energy (lipids) accumulated during pre-adult copepodite stages in the previous year and their new generation (early copepodites) are ready to utilize phytoplankton blooms of the next year. On the other hand, female Calanus needs to feed on phytoplankton before spawning (Parsons and Lalli, 1988). Because of this, there is a time lag in the population growth response of Calanus to the spring phytoplankton bloom.

The carbon-flow diagrams (Figure 5) lead us to conclude that the microbial food chain channels carbon flow throughout the season in the Oyashio region. As an exception, the grazing food chain is functional along with the microbial food chain only in the spring phytoplankton bloom period. In the northeast subarctic Pacific, because of iron limitation on the microphytoplankton, pico- and nanophytoplankton are the major primary producers throughout the year (Boyd et al., 1996). As a consequence, microzooplankton is the major grazer on phytoplankton (Landry et al., 1993; Boyd et al., 1995b), and mesozooplankton (Neocalanus spp.) graze on microzooplankton (Gifford and Dagg, 1991; Gifford, 1993). In the North Atlantic, a nanophytoplankton (prymnesiophytes) bloom has been observed (Sieracki et al., 1993) and a large part of the nanophytoplankton biomass is grazed by microzooplankton (Verity et al 1993). Therefore, the grazing food chain would not be dominant in this region throughout the year. Finally, the microbial food chain could be dominant throughout the year in the northeast subarctic Pacific and the North Atlantic. From these comparisons, it is clear that the planktonic food chain structure in the Oyashio region is different due to a temporal activation of the grazing food chain. This implies that carbon transfer efficiencies from primary producers to mesozooplankton may be higher in the Oyashio region as compared to the northeast subarctic Pacific and North Atlantic.

Fig. 1.

Location of a sampling site (station A3) in the Oyashio Current (arrow), western subarctic Pacific Ocean. Bathymetric contours (200, 1000 and 3000 m) are superimposed.

Fig. 1.

Location of a sampling site (station A3) in the Oyashio Current (arrow), western subarctic Pacific Ocean. Bathymetric contours (200, 1000 and 3000 m) are superimposed.

Fig. 2.

Vertical profiles at Station A3 of temperature, salinity and sigma-t., and the bottom of the euphotic zone (horizontal bars) (top), and vertical distribution of the biomass of autotrophic (middle) and heterotrophic plankton components (bottom).

Fig. 2.

Vertical profiles at Station A3 of temperature, salinity and sigma-t., and the bottom of the euphotic zone (horizontal bars) (top), and vertical distribution of the biomass of autotrophic (middle) and heterotrophic plankton components (bottom).

Fig. 3.

Seasonal changes at Station A3 in pico-, nano- and microphyto-plankton biomass (top), relative abundance of two picophytoplankton (middle) and three microphytoplankton components (bottom) in the euphotic zone.

Fig. 3.

Seasonal changes at Station A3 in pico-, nano- and microphyto-plankton biomass (top), relative abundance of two picophytoplankton (middle) and three microphytoplankton components (bottom) in the euphotic zone.

Fig. 4.

Seasonal changes at Station A3 in heterotrophic plankton biomass (bacteria, HNF, microzooplankton and mesozooplankton) (top), the composition of microzooplankton (middle), and mesozooplankton components (bottom) in the euphotic zone.

Fig. 4.

Seasonal changes at Station A3 in heterotrophic plankton biomass (bacteria, HNF, microzooplankton and mesozooplankton) (top), the composition of microzooplankton (middle), and mesozooplankton components (bottom) in the euphotic zone.

Fig. 5.

Schematic carbon-flow diagrams in the euphotic zone during four seasons of the year at Station A3 in the Oyashio region. Paired figures in each plankton compartment are production rates/standing stock. Figures associated with upward arrows directed to ‘Mesozoo’ and ‘Microzoo’ are their ingestion rates. Sedimentation rates of phytoplankton and faeces production rates of mesozooplankton are indicated by figures along downward arrows of respective compartment. Figures in bold face are measured and those in normal face are calculated rates. Units are mg C m–3 d–1 for the rates, and mg C m–3 for the standing stocks. Phyto = phytoplankton; Zoo = zooplankton; Microzoo includes HNF.

Fig. 5.

Schematic carbon-flow diagrams in the euphotic zone during four seasons of the year at Station A3 in the Oyashio region. Paired figures in each plankton compartment are production rates/standing stock. Figures associated with upward arrows directed to ‘Mesozoo’ and ‘Microzoo’ are their ingestion rates. Sedimentation rates of phytoplankton and faeces production rates of mesozooplankton are indicated by figures along downward arrows of respective compartment. Figures in bold face are measured and those in normal face are calculated rates. Units are mg C m–3 d–1 for the rates, and mg C m–3 for the standing stocks. Phyto = phytoplankton; Zoo = zooplankton; Microzoo includes HNF.

3
Present Address: Seiun-Sou 14, 3-4-1 Washibetsu-Cho, Noboribetsu, Hokkaido 059-0034, Japan

We are grateful to Drs H. Saito, H. Kasai, Y. Kawasaki and T. Kono and Mr K. Nakatsuji for their assistance in sampling at sea and valuable discussions in the course of this study. Thanks are extended to the captains and crew members of R/V ‘Tankai Maru’ and R/V ‘Hokkou Maru’ for their co-operation at sea. We thank Dr G. Padmavati for reading the English text.

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