Structure and size distribution of plankton communities down to the greater depths in the western North Pacific Ocean

Deep-Sea Research II 49 (2002) 5513–5529

Structure and size distribution of plankton communities down to the greater depths in the western North Pacific Ocean Atsushi Yamaguchia,*, Yuji Watanabea, Hiroshi Ishidaa, Takashi Harimotoa, Kazushi Furusawab, Shinya Suzukib, Joji Ishizakac, Tsutomu Ikedad, Masayuki Mac Takahashie a

Kansai Environmental Engineering Center Co., Ltd., Ocean Environmental Survey Team, Environmental Chemistry Department, 1-3-5 Azuchimachi, Chuo-ku, Osaka 541-0052, Japan b Marine Biological Research Institute of Japan Co., Ltd., 4-3-16 Yutakamachi, Shinagawa-ku, Tokyo 142-0042, Japan c Faculty of Fisheries, Nagasaki University, 1-14 Bunkyo, Nagasaki 852-8521, Japan d Biological Oceanography Laboratory, Faculty of Fisheries, Hokkaido University, 3-1-1 Minato-cho, Hakodate, Hokkaido 041-0821, Japan e Department of Systems Science, Graduate School of Arts and Science, University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan Received 9 January 2001; received in revised form 2 December 2001; accepted 3 March 2002

Abstract As part of the research program ‘‘WEST-COSMIC (Western Pacific Environment Study on CO2 Ocean Sequestration for Mitigation of Climate Change)’’, vertical distribution patterns of community structure and size spectra of plankton organisms were studied at three sites: Station SA at 441N, 1551E (down to 4000 m depth); Station I at 391N, 1471E (2000 m depth); and Station ST at 251N, 1471E (4800 m depth) in the western North Pacific Ocean. The plankton organisms were divided into four major groups (bacteria, phytoplankton, protozooplankton, and mesozooplankton) and their sizes and biomass were quantified. Total plankton biomass in the water column ranged from 8180 (night) to 8630 (day) mg C m
2 at Station ST to 29,800 (day) to 32,800 (night) mg C m
2 at Station SA. The water column-integrated major group compositions (biomass) were different between stations: mesozooplankton were the most dominant group (47–52%) at the two northern stations, while they constituted 9–14% at the southern station. An appreciable contribution of dormant copepods to higher mesozooplankton biomass was noted at the northern station, but there were few copepods at the intermediate station and nil at the southern station. The water columnintegrated size distribution patterns of plankton communities were characterized by three marked peaks [pico-, micro(20 mm), and meso- (2000 mm) size] at Station SA, the same three peaks, but with less marked in the micro- and mesosizes at Station I, and only one peak (pico-size) at Station ST. Biomass each plankton group decreased with increasing depth, and their declining patterns below 100 m depth were well described by a negative power function, with different slopes between groups and also between stations. Within stations, the slope was the greatest for mesozooplankton, followed by phytoplankton and bacteria or protozooplankton. From correlation analyses between the biomass of the four major groups of plankton organisms, a close relation was observed between bacteria and protozooplankton. This bacteria–protozooplankton link, combined with the results of the depth-related changes in the abundance of each major

*Corresponding author. Tel.: +81-138-40-5543; fax: +81-138-40-5542. Present address: Biodiversity Laboratory, Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1, Minatomachi, Hakodate, 041-8611, Japan. E-mail address: a-yama@fish.hokudai.ac.jp (A. Yamaguchi). 0967-0645/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 0 2 ) 0 0 2 0 5 - 9

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group and size spectrum, is discussed in the light of regional and bathymetric differences in the structure and functioning of plankton community contributing to the ‘biological pump’ in the western North Pacific Ocean. r 2002 Elsevier Science Ltd. All rights reserved.

1. Introduction In the oceanic ecosystem, CO2 in seawater is converted to organic matter by photosynthetic activity of phytoplankton, and enters pelagic food webs via a wide variety of heterotrophic organisms. The transport of organic matter to the depth of the ocean is mediated by biological processes called the ‘biological pump’. In the oceanic areas where the biological pump is working actively, seasurface CO2 decreases and promotes the dissolution of CO2 from the atmosphere (ocean is a sink of CO2). The situation may be reversed when the biological pump is weak (ocean a source of CO2) (Longhurst and Harrison, 1989). The function of the biological pump could vary from one oceanic region to another, depending on the structure (size, taxa) of the plankton communities and abundance of the component organisms. Attempts have been made to quantify and size almost all of the entire plankton community, then to analyze the pathway of carbon through planktonic food webs in the eastern North Pacific Ocean (Booth et al., 1993; Boyd et al., 1995), western North Pacific Ocean (Shinada et al., 2000), equatorial Pacific Ocean (Ishizaka et al., 1997), off Bermuda (Roman et al., 1995), North Sea (Nielsen et al., 1993), and Baltic Sea (Uitto et al., 1997). However, all these studies were concerned with plankton communities in the epipelagic zone, and comparable information about the plankton community structure in the mesopelagic and bathypelagic zones is currently lacking. Presently, available information about deep distributions of bacteria and protozooplankton is limited to the work of Nagata et al. (2000) in the various regions in the North Pacific Ocean and that of Patterson et al. (1993) at the single station in the North Atlantic Ocean. No study has been made on phytoplankton. In contrast to the paucity of information for these three plankton groups, mesozooplankton

have been well studied. Historically, studies on the biomass of mesozooplankton in meso- and bathypelagic zones before 1990 include those in the North Pacific Ocean (Vinogradov, 1968; Murano et al., 1976; Kikuchi and Omori, 1985; Sameoto, 1986), North Atlantic Ocean (Grice and Hulsemann, . 1965; Angel and de Baker, 1982; Roe, 1988), Indian Ocean (Vinogradov, 1968), Mediterranean Sea (Scotto di Carlo et al., 1984), off Bermuda (Deevey and Brooks, 1971), and Red Sea (Weikert, 1982). In the last two decades, the development of sampling gear such as RMT 1+8 (Roe and Shale, 1979), BIONESS (Sameoto et al., 1980) or MOCNESS (Wiebe et al., 1985) allow easy, precision sampling of mesozooplankton in the meso- and bathypelagic zones, and knowledge has increased rapidly (Weikert and Trinkaus, 1990; Koppelmann and Weikert, 1992, . 1997, 1999; Koppelmann, 1994; Bottger-Schnack, 1996). However, most of the these studies are focused on the systematics of certain zooplankton taxa (such as calanoid or poecilostomatoid copepods, and mysids) or zooplankton biomass, and few attempts have been made on the whole plankton community in terms of systematics, trophic structure or size composition. In the present study, as a basis for quantitative estimation of the biological pump, we investigated biomass of all plankton taxa and their size composition down to 2000–4800 m depth at three stations, which encompass subarctic to subtropical regions in the western North Pacific Ocean. Plankton organisms were divided into four major groups: bacteria, phytoplankton, protozooplankton, mesozooplankton and sized and assembled to create their community size spectrum. All these results are combined and discussed in the light of vertical features of prevailing food chain components and its implications for the effect on carbon cycling in the whole water column in the western North Pacific Ocean.

A. Yamaguchi et al. / Deep-Sea Research II 49 (2002) 5513–5529

2. Methods As part of the research program ‘‘WESTCOSMIC’’ (‘‘Western Pacific Environment Assessment Study on CO2 Ocean Sequestration for Mitigation of Climate Change’’ cf. Harada, 1999; Ishizaka, 1999), deep plankton sampling was conducted at three stations in the western North Pacific Ocean. The three stations included one in the subarctic region (Station SA located at 441N, 1551E ca. 5340 m deep) studied in 19–21 August 1998, one in the subtropical region (Station ST at 251N, 1471E ca. 5710 m deep) sampled 20–21 September 1999, and one in the transitional region (Station I at 391N, 1471E ca. 5320 m deep) sampled in 21 November 1997. Water samples were taken from 0, 10, 25, 40, 50, 75, 100, 125, 150, 200, 300, 400, 500, 750, 1000, 1500, 2000, 3000, 4000, and 5000 m using 12-l rosette-mounted Niskin bottles (General Oceanics) on a CTD system (Seabird SBE-9). Net zooplankton was collected from discrete depths with a modified NORPAC net (mesh size 90 mm, mouth opening 0.16 m2, cf. Motoda, 1957) from 0–100 and 100–200 m, and with VMPS (Vertical Multiple Plankton Sampler, mesh size 90 mm, mouth opening 1.0 m2, cf. Terazaki and Tomatsu, 1997) from 200–500, 500–1000, 1000–1500, 1500–2000, 2000– 3000, and 3000–4000 m at Station SA, and from 200–300, 300–500, 500–1000, and 1000–2000 m at Station I, and from 200–300, 300–500, 500–1000, 1000–2000, 2000–3000, 3000–4000, and 4000– 4800 m at Station ST. Net zooplankton samplings were conducted only at night at Station I, but both day and night at Stations SA and ST. At each station, water samples for chlorophyll a were filtered through Whatman GF/F filters, and measured fluorometrically after the extraction with dimethyl-formamide (Suzuki and Ishimaru, 1990). Nitrate (plus nitrite) in seawater was determined using a Bran and Luebbe Auto Analyzer II, immediately after the collection. Several different methods were used to enumerate and determine the size of plankton over a range of four orders of magnitude (0.2–2000 mm) (cf. Kiyosawa et al., 1995). Pico- and nanoplankton (0.2–20 mm) were analyzed by fluorescent microscopy; water samples were filtered through 0.2-

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and 3-mm Nuclepore filters, preserved with glutaraldehyde or neutralized formalin, and stained with DAPI and FITC (Ishizaka et al., 1994). Neutralized formaldehyde (final concentration, 2%) was used to preserve microplankton and mesoplankton samples. Microplankton (20–200 mm) were counted and sized under a microscope after settling 1 l water samples, or by filtering 5-l water samples through 10-mm mesh netting. Considering the water sample size (1 or 5 l) of this study, most protists were considered as ‘free-living’, not those associated with aggregate particles, which were sparsely distributed in the oceanic water column (Ploug et al., 1999). While we handled water samples as gently as possible, a rapid change in hydrostatic pressure in the course of water collection from depth and preservation may have caused an underestimation of our counts of protists (cf. Patterson et al., 1993). For mesoplankton (200–2000 mm), specimens in net plankton samples were counted and sized. In the course of enumeration and sizing of each size/category of plankton, systematic characteristics of individuals also were recorded. The size data for individual organisms were converted to biovolumes (mm3) then carbon mass assuming appropriate geometric body shapes. The bacterial carbon mass was estimated to be 0.02 pg C per cell assuming a cell diameter of 0.4 mm (Lee and Fuhrman, 1987). The biovolume-carbon factor for Prochlorococcus (cell diameter of 0.6 mm, assumed) and Synechococcus (0.9 mm, measured) was 0.47 pg C mm
3 (Verity et al., 1992). Non-diatom phytoplankton carbon was calculated from the biovolume-carbon equation given by Verity et al. (1992) and the diatom carbon from the equation of Strathmann (1967). The Verity et al. (1992) equation for non-diatom phytoplankton also was used for estimating protozoan carbon. For mesozooplankton, the biovolume-carbon conversion factors were 0.06 pg C mm
3 for non-gelatinous zooplankton, and 0.003 pg C mm
3 for gelatinous zooplankton (Cnidaria, Ctenophora, and Tunicata) (Parsons et al., 1984). In addition to size-based categories, the plankton community was divided into four large trophic groups (bacteria, phytoplankton, protozooplankton, and mesozooplankton, cf.

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Table 1 Major taxonomic accounts of four plankton groups in this study Size (mm)

Pico (0.2–2)

Four major plankton groups Bacteria

Phytoplankton

Protozooplankton

H. Bacteria

Cyanobacteria Prochlorophytes Picoeukaryotes

Nano (2–20)

AMF A. Dinoflagellates Haptophyta Diatoms

HMF H. Dinoflagellates Ciliates

Micro (20–200)

A. Dinoflagellates Diatoms

H. Dinoflagellates Ciliates Foraminiferida Radiolaria

Meso (200–2000)

Macro (2000o)

Metazooplankton

Nauplii

Copepoda Ostracoda Other Crustacea Urochordata Chaetognatha Cnidaria Mollusca

Note: AMF, autotrophic microflagellates; HMF, heterotrophic microflagellates; A., autotrophic; H., heterotrophic.

Table 1) and their carbon biomass was expressed as mg C m
3 or mg C m
2 in this study. Detailed accounts of the systematics and biomass of organisms of this study can be found in Yamaguchi et al. (2000).

3. Results 3.1. Temperature, nutrients, chlorophyll a Over the three sampling stations, the surface temperatures ranged from 13.51C (Station SA) to 29.51C (Station ST) (Fig. 1A). Integrated mean temperature over the upper 200 m was 6.31C at Station SA, 16.71C at Station I, and 23.61C at Station ST. Water temperature decreased with increasing depth, and a subsurface minimum (1.91C) was observed at 150 m at Station SA. Water temperature at 1000 m depth did not differ appreciably between stations (range, 2.4–3.61C) and was almost the same below 2000 m depth

(integrated mean temperature over 2000–5000 m, 1.5–1.61C). Vertical profiles of nitrate concentration at each station corresponded well to those of water temperature of respective stations; high nitrate was associated with low temperature (or weak thermocline) at Station SA, while low nitrate was seen at high temperature (or strong thermocline) at Station ST (Fig. 1B). Station I exhibited intermediate values of temperature and nitrate. Integrated mean nitrate concentration over the upper 200 m was 21.9 mM at Station SA, 10.0 mM at Station I, and 1.3 mM at Station ST. Differences in nitrate concentration between the three stations were seen down to nearly the 1000 m depth, where the concentrations became nearly equal (43.7–44.1 mM). Vertical profiles of chlorophyll a concentration could be divided into two types: one showing a near-surface (30–50 m) peak at Stations SA and I, and another showing a subsurface peak (110 m) at Station ST (Fig. 1C). The near-surface peaks were

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Fig. 1. Vertical profiles of temperature (A), nutrients (NO3+NO2) (B), and chlorophyll a (C) at three stations in the western North Pacific Ocean.

0.71–0.76 mg m
3, while the subsurface peak was 0.25 mg m
3. Integrated mean chlorophyll a concentrations over the upper 200 m were 0.22 mg m
3 at Station SA, 0.21 mg m
3 at Station I, and 0.10 mg m
3 at Station ST. 3.2. Vertical profile of plankton biomass At all three stations, bacterial biomass in the upper 100 m fell into a narrow range (10–15 mg C m
3), and decreased exponentially with increasing depth from 100 to 1000 m (note that the biomass and depth scales of Fig. 2A are both log10 scales). Differences in bacterial biomass in the 0–1000 m water column were not appreciable between stations. Below 1000 m depth, bacterial biomass differed between station, being highest at Station SA (1.2–1.8 mg C m
3), lowest at Station ST (0.2–0.3 mg C m
3), and intermediate at Station I (0.4–1.7 mg C m
3). Phytoplankton biomass in the upper 50 m depth varied greatly between stations; it was highest at Station SA (surface phytoplankton biomass, 114 mg C m
3), followed by Station I (17 mg C m
3), then Station ST (1.3 mg C m
3) (Fig. 2B). Vertical profiles of phytoplankton biomass closely paralleled those of chlorophyll a at each station (cf. Fig. 1C). The subsurface maximum of phytoplankton biomass at 110 m at Station ST corre-

sponded well with that of chlorophyll a. Below 300 m, the phytoplankton biomass was o0.1 mg C m
3, and decreased slowly with increasing depth. Phytoplankton biomass below 4000 m decreased southward (Station SA>Station I>Station ST), as was the case of bacterial biomass (Fig. 2A). Protozooplankton biomass in the upper 100 m was highest at Station SA (maximum concentration, 63 mg C m
3), while at the two other stations (Stations I and ST) it was nearly the same (2.5–2.7 mg C m
3) (Fig. 2C). Between 100 and 1000 m protozooplankton biomass decreased with increasing depth. Stations I and ST showed close agreement in this variable. The protozooplankton biomass of Station SA was nearly the same as Stations I and ST in the 100–400 m depth range, but showed a much lower value between 500 and 2000 m, where bacterial biomass was also low (Fig. 2A). Below 3000 m, protozooplankton biomass varied between stations in the order of: Station SA>Station I>Station ST, as did bacterial biomass and phytoplankton biomass. Mesozooplankton biomass was highest at Station SA and lowest at Station ST, with that at Station I being intermediate (Fig. 2D). At stations SA and ST, differences in the vertical distribution patterns of mesozooplankton biomass between day and night were not significant (Kolmogorov–

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Fig. 2. Vertical distribution of plankton biomass at three stations in the western North Pacific Ocean: (A) bacteria, (B) phytoplankton, (C) protozooplankton, (D) mesozooplankton. Open and solid symbols in (D) indicate day- and night-time samplings, respectively.

Smirnov two-sample test, p > 0:05). Vertical distribution patterns of mesozooplankton biomass at Station SA and Station ST never overlapped, and the differences at equivalent depths ranged from 2.4- to 103-fold (mean, 33.5). The vertical distribution pattern of mesozooplankton biomass at Station I fell between those at Stations SA and ST, but was characterized by a marked minimum between 100 and 300 m depth (0.3–0.7 mg C m
3). For quantitative expression of the pattern of plankton biomass (B) declining with depth (Z), two models have been used for mesozooplankton, an exponential model B ¼ a0 expð
b0 ZÞ (Vinogradov, 1968) and a power law model B ¼ a Z
b (Koppelmann and Weikert, 1992, 1997), where a and b (a0 and b0 ) are constants. Our preliminary plots show the biomass data for bacteria, phytoplankton, and protozooplankton fit the latter model, while the mesozooplankton data fit the

former model (Fig. 2). To make intercomparisons of the results between these four plankton groups possible, we adopted the power model in this study. Since it is obvious that the data from o100 m depth diverged from the model, regression calculations were made for the data below 100 m depth at each station (using the modified regression model, B ¼ B100 ½Z=100b ; where B100 was the biomass at 100 m depth, Table 2). As judged by correlation coefficients (r2 ), the better fit to the regression model was seen in biomass data from the southern stations over the four trophic groups. As an exception, no significant correlation with depth was observed for the mesozooplankton biomass data from Station I, which may be due to anomalously smaller biomass at 100–500 m depth at that station. Comparison of the slopes of the regression lines revealed that the decrease in biomass with increasing depth was most rapid for

A. Yamaguchi et al. / Deep-Sea Research II 49 (2002) 5513–5529 Table 2 Regression statistics of plankton (bacteria, phytoplankton, protozooplankton or metazooplankton) Taxon and position

n

Regression model B ¼ B100 ðZ=100Þb B100

Bacteria Station ‘‘SA’’ Station ‘‘I’’ Station ‘‘ST’’

Slope b

(95% CI)

r

15

4.71


0.37

(0.12)

0.644**

14

4.39


0.44

(0.06)

0.915***

16

10.02


1.05

(0.06)

0.978***

0.52


0.61

(0.11)

0.833***

0.86


0.88

(0.10)

0.930***

4.05


1.54

(0.15)

0.938***

1.00


0.44

(0.14)

0.668**

1.22


0.43

(0.04)

0.955***

2.39


0.84

(0.00)

0.977***

39.35


1.19

(0.40)

0.799*

36.64


1.19

(0.45)

0.767*

0.48


0.77

(0.64)

0.572 (ns)

13.24


2.26

(0.45)

0.897**

4.90


2.10

(0.42)

0.900**

Phytoplankton Station 15 ‘‘SA’’ Station 14 ‘‘I’’ Station 16 ‘‘ST’’ Protozooplankton Station 15 ‘‘SA’’ Station 14 ‘‘I’’ Station 16 ‘‘ST’’ Metazooplankton Station 7 ‘‘SA’’ (D) Station 7 ‘‘SA’’ (N) Station 5 ‘‘I’’ (N) Station 8 ‘‘ST’’ (D) Station 8 ‘‘ST’’ (N)

Note: Biomass (B; mg C m
3) on depth (Z; m) at three stations (Stations ‘‘SA’’, ‘‘I’’, and ‘‘ST’’) in the western North Pacific Ocean. In this calculation, B shallower than 100 m depth was omitted. B100 is the biomass at 100 m depth. (D) and (N) indicate day- and night-time data. *, po0:05; **, po0:01; ***, po0:001:

mesozooplankton, slowest for bacteria and protozooplankton, with being phytoplankton intermediate. Within each trophic group, the slope became steeper toward the southern stations.

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3.3. Vertical profile of taxonomic groups Total plankton biomass in the water column was the greatest at northern Station SA [29,800 (day) and 32,800 (night) mg C m
2] and least at southern Station ST [8180 (night) and 8630 (day) mg C m
2] (Fig. 3). The structure of the entire plankton assemblage as viewed from the composition of the four major groups was also different between these two stations. At Station SA, bacteria and mesozooplankton were the most dominant groups. The contribution of mesozooplankton to the total plankton biomass was greatest in the 200–1000 m depth range (ca. 80%), and decreased with increasing depth. On the other hand, the contribution of bacteria to total plankton biomass increased with increasing depth, reaching its maximum in the deepest layer (3000–4000 m, ca. 80%). In the entire water column, bacteria, phytoplankton, protozooplankton, and mesozooplankton biomass were 8080, 4140, 3640–3660, and 13,900–16,900 mg C m
2, respectively (or 25–27%, 13–14%, 11–12%, and 47–52% of the total plankton biomass, respectively). As at Station SA, bacteria and mesozooplankton were the most important components of plankton biomass at Station I (Fig. 3). However, Station I was different from Station SA in that the ratio of bacteria and mesozooplankton to total plankton biomass did not change much with depth. This may be partly because of the shallower range of sampling depths (o2000 m) at this station. Total plankton biomass in the water column studied was 13,900 mg C m
2. Water column averages of bacteria, phytoplankton, protozooplankton, and mesozooplankton biomass were 4180, 1700, 1140, and 6850 mg C m
2, respectively (or 30%, 12%, 8%, and 49%, respectively, of the total plankton biomass). At Station ST, bacteria and protozooplankton, instead of mesozooplankton, were the most important groups contributing to the total plankton biomass. The relative importance of these two groups did not change greatly with depth. In the entire water column, bacteria and protozooplankton contributed ca. 60% and 20%, respectively, of total plankton biomass. An unique feature

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Fig. 3. Vertical distribution of total plankton biomass and its major taxonomic composition at three stations in the western North Pacific Ocean. The number in the parentheses indicates integrated total plankton biomass (or contribution to the total plankton biomass of each four group).

observed at Station ST is that phytoplankton biomass contributed a significant proportion of total plankton biomass (ca. 5%) down to 4000 m, due to the occurrence of cyanobacteria throughout the water column. These general features remained unchanged both day and night. For the water column, the average biomass of bacteria, phytoplankton, protozooplankton, and mesozooplankton was 4700, 1120, 1620, and 738–1190 mg C m
2, respectively (or 54–57%, 13–14%, 19–20%, and 9– 14%, respectively, of the total plankton biomass).

3.4. Size spectrum of plankton assemblage Over the plankton biomass spectrum from 0.4 to 6000 mm, the pico-size (o2 mm) fraction (mostly bacteria) formed a prominent biomass peak at all the three stations (Fig. 4). In addition to the picosize peak, there were biomass peaks for micro(20 mm) and meso-size fractions (2000 mm) at Station SA. Only a peak for the meso-size fraction was seen at Station I, but neither of these two peaks was recognizable at Station ST. These

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Fig. 4. Water column-integrated plankton size spectrum (ESD, equivalent spherical diameter) and their biomass at three stations in the western North Pacific Ocean. Contribution of plankton biomass living at 8 depth strata to the entire size spectrum is also shown. Note that the horizontal scale (size) is the logarithm (log10).

patterns were unaltered by sampling during dayor night-time (Stations SA and ST). The size-structured plankton biomass spectrum is the sum of all the plankton living at various depths. Common to the results for the three stations, micro-size plankton (20–200 mm, largely autotrophic microflagellates and diatoms) was most concentrated in the 0–100 m depth (Fig. 4).

At the northern stations (Stations SA and I), picosized cyanobacteria were also concentrated in the 0–100 m depth interval. At the southern station (Station ST), cyanobacteria were distributed down to 4000 m depth (in contrast to the northern stations), and they remained major contributors to the peak of the pico-size fraction. The biomass peak of the meso-size fraction at Stations SA and I

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was mainly due to zooplankton living in the 200–1000 m depth interval, regardless of day or night sampling (Station SA).

4. Discussion 4.1. Plankton biomass versus depth The present results at subarctic (Station SA), transitional (Station I) and subtropical (Station ST) stations in the western North Pacific Ocean revealed that the biomass of bacteria, phytoplankton, protozooplankton, and mesozooplankton decreases more or less from subarctic to subtropical stations, reflecting hydrographic/nutrient conditions of the respective regions. This north–south gradient of plankton biomass is most pronounced in mesozooplankton throughout the entire depth range studied, and in the other trophic groups in the top 100 m (Fig. 2). Vertically, the biomass of all four trophic groups decreased rapidly below 100 m. Among the four plankton groups, the biomass distribution of mesozooplankton in the greater depths has been studied most extensively in several regions of the world’s oceans (see Section 1). In the western Pacific Ocean, Vinogradov (1997) analyzed the depth (Z; m)-related reduction in mesozooplankton biomass (B; mg wet weight m
3) by using the exponential regression model, instead of the power regression model used in this study, and resultant b0 (slope) values were 6.5– 8.5  10
4 for the mesozooplankton biomass in the western Pacific Ocean. Our mesozooplankton data, re-fitted to the Vinogradov’s exponential model, yielded b0 -values of 5.2–8.2  10
4, which are close to those of Vinogradov. According to his global synthesis of the vertical distribution of mesozooplankton biomass over depths of several thousands meters in the Pacific, Atlantic, and Indian oceans (Vinogradov, 1968), the slope (b0 ) values are identical in hydrographically identical regions, and the biomass at greater depths was closely related to those of shallow layers in a given oceanic region. A marked between-station difference in mesozooplankton biomass profiles with similar slopes seen in this study (Fig. 2D) supports

this hypothesis. Diel vertical migrations of some mesozooplankton components are known to affect day-night biomass profiles in the upper few hundred meters (cf. Vinogradov, 1968), but the present results showed it to be of little importance in the comparisons over greater depth scales (Fig. 2D). Less is known about the vertical distribution of protozooplankton in the ocean. As a notable study, Patterson et al. (1993) enumerated and identified protozooplankton (heterotrophic flagellates and other protists) down to 4000 m depth in the mid-North Atlantic Ocean. They found that the number of species and abundance of protozooplankton declined rapidly with increasing depth, a pattern observed also in this study (Fig. 2C). Patterson et al. (1993) attributed the reduction with depth of number of species and total abundance to reduced food (detritus, bacteria) availability and increased pressure. Nagata et al. (2000) studied bacterial biomass in the water column from the surface to 5000 m depth in the western, eastern and equatorial North Pacific and in the Bering Sea. The results of Nagata et al. (2000) are consistent with ours in that the bacterial biomass in the water column decreased from higher to lower latitudes, and at each station it decreased rapidly at depths >1000 m. According to Nagata et al. (2000), the rapid reduction in bacterial biomass from 1000 to 4900 m was expressed by the power regression model (the same one used in this study) and the resultant slope was
0.90. Since the depth ranges used for the calculation in this study (100–2000, or 4800 m) are different from those of Nagata et al. (1000–3000, or 4900 m), a direct comparison between the two may not be valid. Nevertheless, their slope (
0.90) falls within the range of
0.37 to
1.05 that was found in this study (cf. Table 2). Boyd et al. (1995) reported that >90% of particulate organic carbon (POC) is composed of bacteria in the eastern subarctic Pacific Ocean during winter. On the premise that this is the case in other seasons over the North Pacific Ocean, the vertical profile data of POC may be used to resolve the vertical distribution patterns of bacterial biomass. Our calculations using POC data from the surface down to 6000 m from 501N–401S in the

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Pacific Ocean collected as part of NOPACCS (Northwest Pacific Carbon Cycle Study, cf. Tsubota et al., 1999), and from the surface to 4000 m depth in the North Atlantic Ocean and central Pacific Ocean (Gordon, 1971) yielded a slope of
0.31 to
0.52 (mean,
0.43 for the Pacific Ocean). This is close to the slopes for Stations SA and I, but less than that at Station ST. The existence of living phytoplankton (containing chlorophyll) in the aphotic zone has been reported from various oceans (Wood, 1956; Hamilton et al., 1968; Fournier, 1970), and they retain a photosynthetic response to light resembling that of near-surface populations (Platt et al., 1983). Platt et al. (1983) considered that phytoplankton in the aphotic zone maintains itself through heterotrophic metabolism. 4.2. Taxonomic group composition versus depth Not only total plankton biomass, but the relative importance of each component group changed greatly from subarctic to subtropical stations (Fig. 3). Comparing the results at Station SA in the subarctic region with those at Station ST in the subtropical region, the most important components are bacteria and mesozooplankton in the former, bacteria and protozooplankton in the latter. While the data at Station I were limited to 2000 m depth, the general trophic group structure is close to that at the subarctic Station SA. In terms of trophic functioning, mesozooplankton occupied a large portion of total plankton biomass at Stations SA and I, greater than that at Station ST. This is because mesozooplankton at Stations SA and I includes dormant stages of large grazing copepods (Neocalanus cristatus, N. plumchrus, N. flemingeri, and Eucalanus bungii), all characterized by no feeding, lowered metabolism and a large accumulation of lipids in their body (Miller et al., 1984; Miller and Clemons, 1988; Kobari and Ikeda, 1999). These copepods grow rapidly to pre-adult stages in the upper layers during the productive spring–early summer season and sink to the meso- or bathypelagic zone in midor late summer for molting to adults and reproduction. In the present data, the maximum contribution of these dormant copepods to the

Fig. 5. Vertical distribution of the biomass of dormant calanoid copepods (histograms) and their contribution to the total plankton biomass (lines) at Station SA (upper panel) and Station I (lower panel). No dormant copepods occurred at Station ST.

total plankton biomass was 46% at 1500–2000 m at Station SA, but only 4% at 500–1000 m at Station I, near the southern edge of the distribution of these cold-water copepods (Fig. 5). No dormant copepods were found at Station ST. Dormant copepods do not feed, but they are thought to be major diets for deep-sea pelagic carnivores such as shrimps, chaetognaths, mesopelagic fishes, etc. (for mesopelagic fish, see Beamish et al., 1999). Therefore, it could be a major part of the ‘biological pump’ output in this region. Interrelationships among the biomass of four trophic plankton groups were analyzed using the data from the entire water column at three stations of this study. As a result, a significant correlation was seen only in the bacteria–protozooplankton relationship (Fig. 6A). It is noted that the data sets from 0 to 40 m depth at Station SA deviated from the relationship, and these were omitted in the calculation of regression line (Fig. 6B). The observed close relationship between bacteria

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Fig. 6. Relationship between bacterial biomass and protozoan biomass. (A) All station data are pooled and plotted on log10– log10 scale. Four solid symbols are the data from 0 to 40 m depth at Station SA. (B) Re-plotted data on linear scales, after removing the 0–40 m data at Station SA. Note that the correlation between bacterial biomass and protozoan biomass is highly significant (po0:0001).

biomass and protozooplankton biomass suggests that microbial food webs are operative throughout greater depths of the western North Pacific Ocean. 4.3. Size spectrum of plankton biomass By the advent of new technology such as fluorescent microscopy and flow-cytometry, widespread distribution of pico-sized phytoplankton in shallow layers of the world’s oceans is becoming widely appreciated among biological oceanographers (Zubkov et al., 1998; Liu et al., 1998; and references therein). The pico-phytoplankton are too small to be utilized by mesozooplankton, and protozooplankton are an essential mediator between the two. The size distribution of plankton biomass will provide insight into possible interactions between component organisms and carbon flow through the communities. In this study, the water column-integrated size distribution of plankton biomass at the three stations (Fig. 4) showed latitudinal variation; i.e. of the three marked size peaks [pico-, micro(20 mm) and meso- (200 mm) sizes] seen at northern station (Station SA), the micro- and meso-size peaks became less marked at the intermediate station (Station I), and virtually disappeared at the southern station (Station ST). The micro-size

organisms that were abundant at the northern station were composed of autotrophic microflagellates and diatoms, most (80%) of which occurred in the 0–100 m depth range (Fig. 4). It has been well documented that these large phytoplankters predominate in high-nutrient regimes (Furuya and Marumo, 1983; Taguchi et al., 1992). Thus, differences in nutrient conditions (NO3+NO2) between the three stations (Fig. 1B) may explain why the micro-size phytoplankton were abundant at Station SA, less abundant at Station I and scarce at Station ST. Lower nutrients at Station ST may be due to the lack of vertical mixing due to the well-established thermocline, as evidenced by the formation of a chlorophyll a peak in the subsurface layer (Fig. 1C) of this station. Subsurface maxima of chlorophyll a at the bottom of the euphotic zone have been reported as characteristic of the oligotrophic subtropical North Pacific Ocean (Takahashi et al., 1985; Furuya, 1990), and its main components are pico-sized phytoplankton (Ishizaka et al., 1994; Suzuki et al., 1997). Almost exclusive predominance of pico-sized primary producers, and greater proportions of bacteria and protozooplankton (Figs. 3 and 4) in the oligotrophic subtropical station indicate that the ‘microbial loop’ (cf. Azam et al., 1983) or ‘microbial food webs’ (Sherr and Sherr, 1988) play the central role for carbon cycling in the epipelagic zone (pico-phytoplankton–protozooplankton link) of this region. At the nutrient-rich subarctic station, the primary producers are pico- and nano/micro-size phytoplankton, thus not only microbial food webs, but traditional grazing food chains (i.e. diatoms/microflagellates–mesozooplankton link) are at work in shallow depths. In the epipelagic zone of the North Pacific Ocean, evidence of the prevalent importance of microbial food webs has been offered by several workers (Booth et al., 1993; Ishizaka et al., 1997; Landry et al., 1997). In the Oyashio Current (western boundary current of the North Pacific Ocean), Shinada et al. (2000) conducted a seasonal survey of biomass and prey–predator relationships among components of the plankton community, concluding that while microbial food webs are major routes in the carbon cycle during most

A. Yamaguchi et al. / Deep-Sea Research II 49 (2002) 5513–5529

seasons, a grazing food chain is activated during the season of spring diatom blooms. In meso- and bathypelagic zones, the only comparable information about the size spectrum of plankton (plus detritus) in the North Pacific Ocean is that of Sheldon et al. (1972). Because of their technical constraints (only bottle sampling of seawater, and particle sizing with Coulter Counter), the size range studied by Sheldon et al. (1972) was limited to only 1–100 mm, as compared with 0.4–6000 mm in this study (Fig. 4). Our results (Fig. 4) show that over the size ranges determined, plankton size groups in meso- and bathypelagic zones contributed to the water column-integrated biomass are pico-, nano- and meso-size fractions over the three stations (little micro-size fraction), which corresponds with results from the epipelagic zone (0–200 m) in the equatorial Pacific (Ishizaka et al., 1997). 4.4. Implications for ‘biological pump’ Studies with sediment traps in the North Pacific Ocean have revealed that only 1% of the POC produced by phytoplankton in the upper layers reaches 3800 m (Wong et al., 1999). Thus, the greater portion of the POC (99%) produced in the euphotic zone enters the carbon cycle of plankton communities of the water column. Our results (Fig. 3) indicated that the total plankton biomass in the whole water column (4000 m or more) at the subarctic station was about 4 times greater than that at the subtropical station, and this betweenstation difference was most pronounced in mesozooplankton biomass (ca. 16 times). The water column-integrated biomass of bacteria, phytoplankton, and protozooplankton was also greater (2–4 times) at the subarctic station than the subtropical station. The sampling depth at the intermediate station was limited to 2000 m, but the biomass of the four plankton groups may fall between those at the subarctic and subtropical stations if the sampling depth is taken into account. Higher total plankton biomass toward the northern stations implies increased activity of the biological pump to the north in the western North Pacific Ocean. Furthermore, differential slopes in the log10 biomass–log10 depth plots

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(Table 2) suggest that the mode of food (organic carbon) supply to each major plankton group living at >100 m differs between regions. Our results on the relative abundance of bacteria, phytoplankton, protozooplankton, and mesozooplankton in epi-, meso- and bathypelagic zones in the western North Pacific Ocean show the dominance of bacteria and protozooplankton throughout the water column in the subtropical station and between 3000 and 4000 m in the subarctic station. Sinking POC– DOC–bacteria have been proposed as the main scheme of the carbon cycle in meso- and bathypelagic realm (Cho and Azam, 1988; Nagata et al., 2000). Our results showing high abundance of protozooplankton in meso- and bathypelagic plankton communities advances the scheme as POC–DOC–bacteria–protozooplankton in deep oceans. Sinking POC (phytoplankton cells, fecal pellets, dead zooplankton, detritus) and its subsequent decomposition has been considered as the major source of DOC in meso- and bathypelagic zones in the ocean (Menzel, 1974). In addition, Steinberg et al. (2000) suggested from a recent study in the Sargasso Sea that vertically migrating zooplankton transfer biomass downward, some of which is eaten and stays down, some of which is excreted at depth as DOC. From this view, not only diel vertical migrators but seasonal migration of large, grazing copepods are of particular importance in the subarctic sector of the North Pacific (Vinogradov, 1968). The deep resting stocks of Neocalanus spp., which are endemic in the region, have substantial mortality rates (Miller and Clemons, 1988). Most mortality must be due to predation and thus represents a permanent downward transfer of organic matter. Post-reproductive corpses are another small transfer. However, there was no obvious effect of these seasonal downward transfers in the vertical profiles of bacteria or protozooplankton between 100 and 1500 m (Fig. 2A and C), where the data from the three stations are overlapping. Below 1500 m, both bacteria and protozooplankton biomass are higher at the northern stations, which may reflect the seasonal transfer of organic matter by resting copepod stocks.

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The overlapping vertical profiles of bacteria and protozooplankton biomass from 100 to 1500 m at the three stations and the clear latitudinal separation of the vertical profiles of mesozooplankton biomass (higher biomass at northern stations as mentioned above) raises a question: whether the hypothesized POC–DOC–bacteria–protozooplankton food chain provides enough food for mesozooplankton to form a greater biomass in that depth stratum of the subarctic station? Greater mesozooplankton biomass at the subarctic station than the more southern two stations is unaltered, even if the high proportion of dormant copepods is taken into account. As an alternative food source for mesozooplankton in that depth stratum, sinking phytoplankton POC may be considered (cf. Takahashi, 1986; Michaels and Silver, 1988). However, the vertical flux of phytoplankton POC, as judged by the position and the slope of its biomass–depth regression lines in this study, does not differ appreciably across the three stations (Fig. 2B). Since mesozooplankton biomass in meso- and bathypelagic zones is correlated with those of the epipelagic zone across the world’s oceans (cf. Vinogradov, 1968), sinking fecal pellets egested by mesozooplankton from the upper layers may be a possible food source. While sinking, fecal pellets are ingested and egested as new fecal pellets by other mesozooplankton, and this process may occur in various depth strata (Lampitt et al., 1990). This process, so-called ‘repackaging’, has been evaluated down to 2000 m depth in the western North Pacific Ocean (Sasaki et al., 1988; Sasaki and Nishizawa, 1989). Vinogradov (1968) considered cascading prey– predator relationships between mesozooplankton and micronekton living at various depths of the ocean (‘ladder-migration’ hypothesis) to be the major mechanism of food supply to great depths. More or less, all these potential food sources have been substantiated, as Harding (1974) observed various diatoms, ciliates, other protozoans, parts of copepods and other metazoans, and detrital remains in the guts of meso- and bathypelagic copepods (the main component of mesozooplankton) from the North Atlantic Ocean. For analyzing carbon pathways within epipelagic plankton communities at selected re-

gions, abundance of trophically grouped organisms and their sizes have been used, together with empirical physiological rate data for the organisms expressed as a function of organism size (see Section 4.3). Compared with epipelagic planktonic organisms, physiological data presently available for those living in meso- and bathypelagic zones are scarce, so that the validity of the direct application of epipelagic data to deep-sea plankton organisms is questionable. The metabolism of most mesozooplankton and other animals living in the deep sea appears to be greatly reduced compared with shallow-living counterparts (see review of Childress, 1995). For the paucity of physiological data for bacteria and protozooplankton living at greater depths of the ocean, see Nagata et al. (2000) and Turley et al. (1988), respectively. For deep-sea mesozooplankton, extensive information is now available for the metabolism of copepods (Thuesen et al., 1998), but such information is limited for the other mesozooplankton taxa. Clearly, there is an urgent need for the collection of appropriate biological and physiological data, together with biomass data over various time scales (seasonal, annual), on planktonic organisms living at greater depths in the world’s oceans to deepen our understanding about nature and functions of the biological pump operating at global scales.

Acknowledgements WEST-COSMIC (Western Pacific Environment Assessment Study on CO2 Ocean Sequestration for Mitigation of Climate Change) was supported by New Energy Industry Development Organization (NEDO). We are grateful to Prof. C.B. Miller for comments which improved the manuscript. We thank captains and crews of R.V. Hakurei-Maru II for their great effort during the field sampling. We also thank M. Toyota and Y. Sekido of the Marine Biological Research Institute of Japan for cooperation during the field sampling and identification and enumeration the plankton samples.

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