Planktonic community respiration in the East China Sea: importance of microbial consumption of organic carbon

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Planktonic community respiration in the East China Sea:

importance of microbial consumption of organic carbon

Chung-Chi Chen

a,1

, Fuh-Kwo Shiah

b,

*, Gwo-Ching Gong

c

, Kuo-Ping Chiang

d

a

National Center for Ocean Research, National Science Council, P.O. Box 23-13, Taipei, Taiwan 10617, ROC

b

Institute of Oceanography, National Taiwan University, P.O. Box 23-13, Taipei, Taiwan 10617, ROC

c

Department of Oceanography, National Taiwan Ocean University, Keelung 202-24, Taiwan, ROC

d

Department of Fishery Science, National Taiwan Ocean University, Keelung 202-24, Taiwan, ROC Accepted 18 December 2002

Abstract

Planktonic community respiration (PCR) rates were measured using the oxygen method in autumn 1998 in order to evaluate the respective roles played by microbes (heterotrophic bacteria and ciliates) in organic carbon consumption on the continental shelf of the East China Sea (ECS). For comparative purposes, the ECS shelf was divided into mesotrophic ([NO3

]>0.3 mM) and oligotrophic ([NO3

]p0.3 mM) systems. Bacterial biomass (23.4728.4 mg Cm3) and production (4.976.8 mg Cm3d1) as well as particulate organic carbon concentrations (129.3740.4 mg Cm3) were signiﬁcantly higher in the mesotrophic system, while protozoa (95.6774.9 mg Cm3) were more abundant in the oligotrophic system. PCR rates ranged from 127.6 to 4728.6 mg C m2d1, and the rates were either linearly related to protozoan biomass or multiply regressed with both bacterial and protozoan biomass. Further analysis showed that PCR were dominated by distinct microbial components in different trophic systems, with bacteria and protozoa contributing 72% and 85% of PCR in meso- and oligotrophic systems, respectively. The low primary production to PCR ratio (0.3370.30) suggests that the ECS was net heterotrophic during the study period. Allochthonous supplies of organic carbon, in addition to in situ production, are required to support these high respiration rates. Riverine inputs and/or resuspension from superﬁcial sediments are potential sources of this allochthonous organic carbon.

1. Introduction

The continental shelf is a boundary zone between the land-ocean margins. Although the continental shelf represents less than 20% of the world’s oceanic area, it’s high nutrient input from

riverine run-off has made it one of the most

productive areas in the world (Liu et al., 2000a).

Continental shelf primary production total could be as important as that in the ocean interior (Walsh, 1991). Even though there is a debate as to whether the continental shelf is primarily a carbon source or sink, the carbon ﬂow in this area

to global carbon ﬂux is important. (Liu et al.,

2000a). Understanding the carbon ﬂuxes and cycling processes in the shelf ecosystem is therefore a key step toward estimating the global carbon

*Corresponding author. Fax: +011-886-2-369-5746. E-mail address:fkshiah@ccms.ntu.edu.tw (F.-K. Shiah).

1_{Now at: Deparment of Biology, National Taiwan Normal}

University, 88, Sec. 4, Ting-Chou Rd. Taipei 116, Taiwan, ROC

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budget precisely (Siegenthaler and Sarmiento, 1993).

The East China Sea (ECS) is one of the largest continental shelves in the world. Varieties of water masses have been contributed to, and complicate, this shelf ecosystem, including a large amount of riverine run-off from the west, intrusion and upwelling of the Kuroshio surface and subsurface waters from the east, the Yellow Sea waters from the northern boundary, and the Taiwan Strait

waters from the south (Wong et al., 2000).

Signiﬁcant amounts of allochthonous organic carbon and inorganic nutrients have been supplied to the ECS from riverine run-off and/or from the

upwelling Kuroshio waters (Cauwet and

Mack-enzie, 1993; Chen and Wang, 1996; Wong et al., 1998; Liu et al., 2000b). Enhanced by abundant substrate, high biological productivity with seaso-nal and spatial variation has been observed in the

ECS (Guo, 1991; Gong et al., 2000; Shiah et al.,

2000a).

High primary production tends to enhance the biological pump and draws down the dissolved

CO2concentration. Signiﬁcant CO2sink (ca. 1.2–

2.9 mol m2yr1) was indeed observed in the ECS

shelf using air–sea difference of fCO2(Peng et al.,

1999; Tsunogai et al., 1999; Wang et al., 2000). However, large uncertainty existed when trying to explore carbon cycling process, especially concern-ing how biological production and remineraliza-tion of organic matter contribute to this process.

Based on bacterial production,Shiah et al. (2000a)

estimated that bacteria might consume carbon equivalent to all the in situ particulate primary productivity in the ECS shelf. In addition, other planktonic communities (i.e. protozoa and zoo-plankton) also may consume a large fraction of the organic carbon, which in turn will reduce the

carbon deposition (Rowe et al., 1986;Kemp et al.,

1994). In all cases, it is suggested that biological

activity plays an important role in carbon cycling processes in this shelf ecosystem.

The objective of this study, which is part of the Kuroshio edge exchange processes (KEEP) pro-gram, is to examine the role biological activity plays in carbon cycling within the ECS. Biological carbon productions have been reported previously; however, organic carbon consumption through

biological activities has never been estimated in

this shelf ecosystem (Gong et al., 1999, 2000). To

explore spatial variation, plankton community autumn respiration was measured in the ECS. Respiration was also analyzed with biological variables (i.e. Chlorophyll a (Chl a) and biomass of bacteria and protozoa) to discriminate how carbon consumption was attributed to various components. Furthermore, the relative importance of components (bacteria and protozoa) contribut-ing to respiration was estimated to understand their roles in different designated trophic ecosys-tems. Finally, biological carbon production and consumption (respiration) were compared to delineate the role played by biological activity on carbon balance.

2. Materials and methods 2.1. Study area and sampling

Samples were collected on board R/V Ocean Researcher I between 29 October and 5 November 1998, and a total of 33 stations were occupied (Fig. 1). Using Teﬂon coated Go-Flo bottles

Latitude ( oN) Longitude (o_E) 1000 m 200 m Yangtze River 23 23 24 26 118 119 120 121 122 123 124 125 126 127 128 129 130 24 25 26 27 28 29 30 31 32 33 Taiwan Mainland Chin

Fig. 1. Map of stations (+) in the East China Sea with station number above the mark. Stations conducting protozoa sampling ( ), community respiration incubation (J), and primary production incubation (&) are also indicated. Stations with high surface nitrate concentrations (>0.3 mM) are shaded and deﬁned as mesotrophic, and low surface nitrate concentra-tions (p0.3 mM) are classiﬁed as oligotrophic. Bottom depth contours (dashed lines; 200 and 1000 m) are also shown.

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(20 l, General Oceanics Inc., USA) mounted on a General Oceanic rosette assembly, seawater at each station was sampled at 6–10 water depths, at depth intervals of 3–50 m depending on the depth of each station. Subsamples were taken immedi-ately for further analyses (i.e. nutrients, particulate organic carbon, Chl a, and bacterial and proto-zoan abundance) and on-board incubations (pri-mary and bacterial production, and plankton community respiration).

2.2. Hydrographic and optical measurements Temperature, salinity and density were recorded throughout the water column with a SeaBird CTD (SBE 9/11 puls, SBE Inc., USA). Photosyntheti-cally active radiation (PAR) was measured all through the water column with a biospherical log quantum scalar irradiance sensor (4p; QSP-200L) attached to the rosette frame. Total downwelling scalar irradiance above the sea surface was measured continuously with a separate biosphe-rical quantum scalar irradiance system (QSP 160), equipped with a surface 2p steradian hemispherical scalar irradiance sensor (QSR-240). The depth of

the euphotic zone (ZE) was taken as the depth of

1% surface light penetration.

2.3. Nutrients, Chl a and particulate organic carbon Water subsamples for nutrient analyses were collected from every sampling depth with 100-ml polypropylene bottles and frozen immediately with liquid nitrogen. A custom-made ﬂow injection

analyzer was used for nitrate analysis (Gong,

1992). Chl a concentration was measured with a

Sea Tech fluorometer attached to the SeaBird CTD for a continuous profile of in vivo fluores-cence, with data calibrated by in vitro fluorome-tery (Turner Design 10-AU-005) following acetone

extraction (Strickland and Parsons, 1972). At

selected stations, samples for particulate organic carbon (POC) were ﬁltered through a Whatman 25-mm GF/F ﬁlter, wrapped in aluminum foil

and then stored at 4_{C. Both ﬁlter and aluminum}

foil were pre-combusted at 550Cfor an

hour. After drying and acid-fuming, POCsamples were measured by combustion method using a

HORIBA EMIA-510 analyzer (Shiah et al.,

2000b).

The trapezoidal method was used to estimate

integrated Chl a over ZE; and this method was also

applied to calculate integrated values for POC, bacterial biomass and production, protozoan biomass, primary production, and plankton com-munity respiration. Mean Chl a concentration

over ZE was estimated from the integrated value

divided by ZE; and this calculation also was

adopted with other variables.

2.4. Bacterial abundance and production

Bacterial abundance and production were mea-sured at all stations, and duplicate samples were

taken from several depths within ZE: Bacterial

abundance was determined by acridine orange

epiﬂuorescence microscopy (Hobbie et al., 1977).

To convert to carbon units, bacterial abundance

was used with a conversion factor of 20 1015gC

cell1(Lee and Fuhrman, 1987). Bacterial

produc-tion was estimated by3H-thymidine incorporation

with a thymidine conversion factor of

1.18 1018cell mole1 (Cho and Azam, 1980;

Fuhrman and Azam, 1982;Shiah et al., 1999). 2.5. Protozoan abundance

Samples for protozoan abundance were

col-lected at several depths within ZEfrom 20 stations

(Fig. 1). Samples were ﬁxed with neutralized formalin (2% ﬁnal concentration) and then stored

in the dark at 4Cfor subsequent microscopic

examination. Samples were identiﬁed and counted using an inverted epiﬂuorescence microscope (Nikon-Tmd 300) at 200 or 400 . Cellular carbon was calculated from cell volume using a

conversion factor of 0.14 pg C mm3 (Putt and

Stoecker, 1989).

2.6. Primary productivity

Primary production was measured by the 14C

assimilated method at 12 stations (Fig. 1;Parsons

et al., 1984;Gong et al., 1999). Water samples were

collected from 6 depths within ZE: Samples

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(Spectrum), and inoculated with H14CO3 (ﬁnal

conc. 10 mC i ml1) in 250-ml clean polycarbonate

bottle (Nalgene). Samples were incubated on board for 2–4 h in chambers filled with running surface seawater and illuminated by fluorescent bulbs with a light intensity corresponding to the in situ irradiance level. Following each incubation, samples were filtered on GF/F filters (Whatman, 25 mm) and acidified with 0.5 ml 2N HCl for overnight. After immersion in 10 ml of scintillation cocktail (Ultima Gold, Packard), total activity on the filter was counted in a liquid scintillation counter (Packard 1600). To estimate the euphotic zone-integrated primary production (IP) at sta-tions where incubation was not performed, the following empirical function was used:

½IP ¼ 2:512 ½CS PBopt Kd10:957;

where CS; PBopt and Kd were the surface Chl a

concentration, optimal photosynthetic efﬁciency,

and mean attenuation coefﬁcient within ZE;

respectively (seeGong and Liu, 2003).

2.7. Plankton community respiration

Plankton community respiration was measured

as dissolved oxygen (O2) decreasing in dark

incubation at 22 stations (Fig. 1; Gaarder and

Grann, 1927). Triplicate samples were taken for either initial or treatment from 2 to 6 discrete

depths within ZE: Samples were siphoned into

60-ml biological oxygen-demand bottles (Cat. No. 227494-00, Wheaton, Millville, NJ, USA). The treatment involved bottles incubating for 12 h in a dark chamber ﬁlled with running surface seawater and maximum temperature changes less than

1.3370.85_{C(mean7SD) during each}

incuba-tion. Temperature differences between top and

bottom of ZE in all incubation stations were also

small, with mean7SD values of 0.2070.56_C.

Concentration of O2 was measured by direct

spectrophotometry method with precision of

0.5 mM (Pai et al., 1993). The difference in O2

concentration between initial and dark treatment was used to compute plankton community respira-tion. Since temperature changes were insigniﬁcant between incubation chambers and in situ environ-ments, the rate was not corrected for temperature

effects. To convert respiration from oxygen to carbon units, a respiration quotation (RQ) of 1

was applied (Parsons et al., 1984; Hopkinson,

1985).

3. Results

3.1. Hydrography in the East China Sea

Surface temperature (SST) in the ECS increased

from the inner shelf (21_{C) to the slope (27}_C),

with isotherms parallel to the coastal shoreline (Fig. 2a). Surface salinity contours also showed a similar trend, with values ranging from 27.48 to

34.40 psu (Fig. 2b). Nitrate concentrations in the

surface water were in the range 0–24.3 mM, with high nutrient concentration along the inner shelf and in the northwest of the ECS, near the Yangtze

River (Changjiang) estuary (Fig. 2c). For a more

systematic understanding of this shelf ecosystem, the ECS was categorized into mesotrophic and oligotrophic systems by surface nitrate concentra-tion, >0.3 andp0.3 mM, respectively (Fig. 2c). 3.2. Biological variables in the ECS

To understand spatial variation of different variables in the ECS, biological variables (i.e. biomass and rates) were compared between mesotrophic and oligotrophic systems. In the ECS, mixed-layer depth (MLD) ranged from 4 to 69 m, with a mean7SD value of 39.8721.3 m (Table 1). On average, MLD was signiﬁcantly shallower in the mesotrophic than in the

oligo-trophic systems, with mean7SD values of

33.9722.2 m and 49.7715.4 m, respectively

(p ¼ 0:01). Euphotic depth (ZE) varied from 3 to

66 m in the ECS, with a mean7SD value of

37.7719.0 m (Table 1). Similar to the MLD, ZE

was also shallower in the mesotrophic than in the

oligotrophic systems, with mean7SD values of

27.3718.9 and 49.5710.5 m, respectively

(po0:01). There was however no difference

observed between MLD and ZE in the ECS

(p ¼ 0:68). Since most of biological variables were

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therefore integrated over ZE; instead of MLD, for further comparison.

Integrated Chl a values in mesotrophic and oligotrophic systems were in the ranges 1.5–70.1

and 11.7–74.4 mg Chl m2, respectively (Table 1).

Even though mean values of integrated Chl a

were slightly lower in mesotrophic (28.17

20.4 mg Chl m2) than in oligotrophic systems

(40.3719.6 mg Chl m2

), it was not statistically signiﬁcant (p ¼ 0:10). Integrated values of primary production in mesotrophic and oligotrophic sys-tems were in the ranges 16–797 and 106–

854 mg Cm2d1, respectively. No signiﬁcant

dif-ference (p ¼ 0:14) in integrated primary

produc-tion was evident between the meso- and

oligotrophic systems, with mean7SD values of

2837229 and 4077231 mg Cm2d1,

respec-tively. Signiﬁcant linear regression, however was evident between the integrated values of primary

production and Chl a, with slope and r2 _{values of}

linear regression of 9.8 and 0.75, respectively (po0:01).

Integrated bacterial biomass was relatively

constant and ranged from 222.3 to 426.2 mg Cm2

in the ECS (Table 1). There was no statistical

difference (p ¼ 0:60) in mean values of integrated

bacterial biomass between mesotrophic

(295.3753.1 mg Cm2

) and oligotrophic systems

(305.8758.2 mg Cm2), but, mean bacterial

biomass (mg Cm3) over ZE was signiﬁcantly

higher (po0:001) in the mesotrophic (23.47

28.4 mg Cm3) than in the oligotrophic systems

(6.973.8 mg Cm3). Integrated bacterial

produc-tivity between the systems was not statistically (p ¼ 0:06), although mean values were larger in

mesotrophic (55.9716.7 mg Cm2_d1_{) than in}

oligotrophic (45.2714.2 mg Cm2_d1_{) systems.}

Similar spatial patterns were observed between integrated values of bacterial productivity and biomass in the ECS (data not shown). Therefore, a signiﬁcant relationship between integrated bacter-ial biomass and productivity was indeed evident, with slope and r2values of linear regression of 0.21

and 0.48, respectively (n ¼ 32; po0:01). Similar to

bacterial biomass, a signiﬁcant difference also was

found in mean bacterial production over ZE

between different systems (po0:01), i.e. bacterial

production was higher in mesotrophic (4.97

6.8 mg Cm3d1) than in oligotrophic systems

(1.070.5 mg Cm3d1). A signiﬁcant relationship

also was observed between mean values of

bacterial biomass and production over ZE; with

118 119 120 127 128 129 130 24 25 26 27 28 29 30 31 32 33 118 119 120 127 128 129 130 24 25 26 27 28 29 30 31 32 33 Surface temperature: 21.7 - 27.3 °C 200 m 1000 m psu 200 m 1000 m Latitude ( ° N) Longitude (°E) 200 m 1000 m Taiwan (a) (b) (c) mainland C mainland C mainland C 118 119 120 121 122 123 124 125 126 127 128 129 130 24 25 26 27 28 29 30 31 32 33

Fig. 2. Contour plots for surface (2 m) values of temperature, salinity, and nitrate concentration in the East China Sea, with contour intervals of 1_{C, 0.5 psu, and 3 mM, respectively.}

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slope and r2values of linear regression of 0.24 and 0.99, respectively (n ¼ 32; po0:01).

In this study, protozoan abundance was mostly dominated by ciliates (either hetero- or mixo-trophes), which accounted for about 90% of the total abundance, while a small amount was composed by tintinids. Integrated protozoan biomass in the mesotrophic system was fairly low

(289.57410.3 mg Cm2), and higher biomass was

found in the oligotrophic system, ranging from

304.3 to 9894.4 mg Cm2 with a mean7SD value

of 4539.073483.7 mg Cm2

(Table 1). The differ-ence in integrated protozoan biomass between

systems was statistically signiﬁcant (po0:01). A

similar pattern also was observed in mean

proto-zoan biomass over ZE; i.e. mean protozoan

biomass was signiﬁcantly smaller in mesotrophic

(8.979.1 mg Cm3) than in oligotrophic systems

(95.6774.9 mg Cm3; po0:01).

Integrated particulate organic carbon (POC)

was signiﬁcantly higher (po0:05) in oligotrophic

than in mesotrophic systems, with mean7SD

Table 1

Different variables in the mesotrophic (Meso) and oligotrophic (Oligo) systems in the ECS including: water column depth (m), mixed-layer depth (MLD; m), euphotic depth (ZE; m), and integrated values of chlorophyll a (Chl a; mg Chl m2), primary productivity (PP;

mg Cm2d1), bacterial biomass (BB; mg Cm2), protozoan biomass (Prot; mg Cm2), particulate organic carbon (POC; mg C m2), and planktonic community respiration (PCR; mg C m2d1) over ZEat different stations (Sts). MLD was based on a 0.125 unit

potential density criterion (Levitus, 1982). EZwas assumed at depth where light intensity X1% of surface light intensity

System Sts Depth MLD ZE Chl a PP BB Prot POCPCR

Meso 2 82 14a ₃₆ _27.1 ₂₄₈ _222.3 _283.4 _— _190.6 Meso 3 62 41a ₂₆ _10.3 ₉₄ _246.2 _10.0 _— _— Meso 4 31 7a ₃ _1.5 ₁₆ _355.2 _0.5 _— _248.8 Meso 5 31 8a ₆ _5.1 ₈₆ _301.3 _— _559.2 _310.8 Meso 6 26 7a ₆ _4.1 ₃₈ _285.8 _5.2 _— _— Meso 7 77 66a 50 41.8 797 292.9 511.8 — 1100.8 Meso 8 97 50a 48 37.4 434 267.2 1374.9 — 2486.1 Meso 18 26 14a 8 11.7 107 270.2 38.6 — 306.5 Meso 19 26 26a 9 11.1 73 222.3 37.2 1586.5 127.6 Meso 20 44 4a 26 56.7 514 372.3 327.5 4150.3 620.9 Meso 21 40 40a 23 70.1 640 246.2 504.6 3689.6 897.6 Meso 22 51 51a 15 15.9 145 354.3 91.3 1521.5 — Meso 28 51 51a 28 31.5 213 401.1 — 2376.0 — Meso 30 31 12a 19 21.8 204 305.1 — — 839.3 Meso 31 72 62a ₅₆ _37.6 ₃₄₅ _270.0 _— _— _2218.2 Meso 34 91 15a ₆₂ _39.0 ₃₅₄ _265.8 _— _— _— Meso 35 72 58a ₄₂ _55.2 ₅₀₁ _342.2 _— _— _— Oligo 1 201 6a ₂₂ _30.1 ₆₂₃ _426.2 _304.3 _1903.4 _1011.8 Oligo 9 107 39a ₄₄ _32.2 ₄₁₀ _294.2 _3529.0 _3629.2 _— Oligo 10 140 50a ₅₂ _27.9 ₂₁₅ _241.0 _1687.5 _3911.3 _1282.3 Oligo 11 151 35a ₅₂ _11.7 ₁₀₇ _317.0 _— _— _623.9 Oligo 12 91 69a ₆₆ _18.0 ₁₆₅ _234.8 _— _— _2219.2 Oligo 14 92 64a ₅₁ _35.9 ₃₀₈ _339.0 _7552.5 _4235.3 _4728.6 Oligo 15 71 65a ₄₃ _62.6 ₈₅₄ _348.2 _9222.7 _— _2914.9 Oligo 16 61 53a 49 66.4 615 373.8 9894.4 — 3697.5 Oligo 17 61 57a 45 74.4 678 341.0 3239.6 — 1186.7 Oligo 23 66 48a 53 51.2 573 318.9 3692.5 4248.5 — Oligo 24 81 53a 62 30.0 106 300.2 1728.4 3679.6 — Oligo 26 92 49a 47 20.9 186 289.5 — — 396.4 Oligo 27 80 54a 54 51.3 505 222.3 — — — Oligo 29 51 43a 41 63.5 451 318.8 — 3916.4 1267.3 Oligo 32 91 61a 61 28.9 315 222.3 — 4177.1 3076.0

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values of 3712.67768.9 mg Cm2 and

2313.971378.8 mg Cm2, respectively (Table 1).

An inverse pattern, however, was, found in mean

POCconcentrations (i.e., mg Cm3) over ZE

between systems, i.e. mean POCconcentrations

were signiﬁcantly (po0:01) lower in oligotrophic

(81.4713.0 mg Cm3

) than in mesotrophic

sys-tems (129.3740.4 mg Cm3

). To understand how POCstock related to biological variables, inte-grated POCwas analyzed to correlate with measured biological parameters. Among all the analyses, integrated POCwas multiply regressed with integrated stocks of Chl a and protozoa (r2_{¼ 0:73; p ¼ 0:01).}

3.3. Contribution of different components to planktonic community respiration

To understand how planktonic community respiration (PCR) contributed by different com-ponents, linear regression was used to analyze

relationships between mean PCR (mg C m3d1)

versus mean biomasses (mg Cm3) of

bacterio-plankton, phytoplankton and protozoa, and mean bacterial production as well as primary production

over ZE: Of all the analyses, PCR was only

signiﬁcantly related to protozoan biomass (Fig. 3a;

r2_{¼ 0:38; p}_{o0:05). Even though there was a weak}

relation between PCR and bacterial biomass (or bacterial production), it was not statistically

signiﬁcant (Fig. 3b; r2¼ 0:15; p ¼ 0:08). No

sig-niﬁcant relationship was evident between PCR and phytoplankton biomass.

Planktonic community respiration represents the summation of carbon consumption by all planktonic communities. To see how PCR corre-lated with planktonic communities, forward step-wise multiple linear regression was used to analyze the relationship between PCR versus biomass of phytoplankton, bacteria and protozoa. A signiﬁ-cant relationship was found for PCR versus both

biomass of bacteria and protozoa (r2_{¼ 0:70;}

p ¼ 0:001), and it can be expressed as follows:

PCR ¼ 0:54 BBþ 0:29 BPþ 17:23; ð1Þ

where PCR, BB; and BP are mean values of PCR,

bacterial biomass, and protozoan biomass over

ZE; respectively. Inclusion of phytoplankton

biomass in this analysis, however, did not improve the relationship.

3.4. Respiration and P/R ratio

The contour of integrated PCR (mg C m2d1)

demonstrated how organic carbon was consumed in autumn in the ECS ecosystem. Integrated PCR in the ECS ranged from 127.6 to 4728.6 mg

C m2d1 (i.e., 5.3–92.7 mg Cm3d1), with a

mean7SD value of 1443.371269.2 mg Cm2

d1 (Fig. 4). Signiﬁcant difference was evident in

integrated PCR between trophic systems

(po0:05), and the rates were higher in oligotrophic

than in mesotrophic systems, with mean (7SD)

values of 2036.8 (71396.8) and 849.7

(7810.6) mg Cm2d1, respectively. There was,

however, no difference in mean values of PCR

(i.e., mg Cm3d1) over ZE between these two

systems (p ¼ 0:16). Higher integrated PCR values were found at stations located in both mesotrophic (i.e., Sts. 8 and 31) and oligotrophic (i.e., Sts. 12,

14, 15, 16 and 32) systems (Fig. 4). Respiration at

0 20 40 60 80 100 0 50 100 150 200 250 0 20 40 60 80 100 0 50 100 150 PCR (mg C m-3_d-1₎ Protozoa (mg C m -3) Bacteria (mg C m -3) Y = 1.71X - 19.4 r2_{= 0.38 (p = 0.02, N = 14)} Y = 0.41X + 0.4 r2_{= 0.15 (p = 0.08, N = 22)} (a) (b)

Fig. 3. Relationship between planktonic community respira-tion (mg Cm3d1; PCR) and biomass of (a) protozoa, and (b) bacteria in the euphotic zone. Slopes, r2_{and p values of linear}

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those high rate stations was in the range of 2218.2–

4728.6 mg Cm2d1, and the rates were relatively

low at all other stations (Fig. 4).

The ratio of primary production to respiration (P=R ratio) has been used to examine whether an ecosystem is either autotrophic (i.e., P=R ratio

>1) or heterotrophic (i.e., P=R ratio o1). In this

study, ratio of integrated primary production

(mg Cm2d1) to integrated respiration

(mg Cm2d1) was used to explore carbon

utiliza-tion between producutiliza-tion and consumputiliza-tion in the

ECS. Respiration in the water column below ZE

and from sediment was not included in this estimation; therefore, the estimated P=R ratio will be larger than the theoretical P=R value. In the ECS, the P=R ratio ranged between 0.04 and 1.30, with a mean7SD value of 0.3370.30. The P=R ratio was less than 1 at all stations except St. 2 (Fig. 5). Even though the mean P=R ratio was

slightly higher in mesotrophic (0.4270.34) than in

oligotrophic systems (0.2470.19), it was not

statistically signiﬁcantly (p ¼ 0:12). To explore how primary production affect P=R ratio, the ratios were plotted against integrated primary

productivity (mg Cm2d1). No signiﬁcant linear

relationship was found between ratio of P=R and

integration primary productivity (Fig. 5; r2¼ 0:12; p ¼ 0:07).

4. Discussion

Even though both temperature and salinity in the ECS varies and deviates seasonally and spatially, a general year-round pattern of low temperature and salinity in the inner shelf and high temperature and salinity on the slope has been

observed (Gong et al., 1996; Shiah et al., 1999;

Tseng et al., 2000). Temporal and spatial varia-tions of nutrient concentravaria-tions also have been found in the ECS. Corresponding to temperature and salinity distributions, a general trend in nutrient distribution is also observed in the ECS, i.e. high nutrient concentrations always are re-corded in the inner shelf, and nutrients are usually depleted in surface slope waters except in the Kuroshio upwelling region off north east Taiwan (Liu et al., 1992;Gong et al., 1996, 2000). Similar general patterns in temperature, salinity and nutrient distributions are also evident in this study (Fig. 2).

Previous studies have suggested that riverine discharge from the China coast and upwelling of 118 119 120 121 122 123 124 125 126 127 128 129 130 24 25 26 27 28 29 30 31 32 33 Longitude (°E) Latitude ( ° N) 200 m 1000 m Taiwan Mainla *

Fig. 4. Contour plot of integrated values of planktonic com-munity respiration (mg Cm2d1) in the euphotic zone in the East China Sea. Stations with respiration incubation were labeled with solid (K) circles, and where marked with asterisk (*) respiration was derived from Eq. (1) (see text for details). Respiration quotient (RQ) of 1 was used to convert oxygen to carbon units. Primary productivity (mg C m-2_d-1₎ P/R ratio 0 200 400 600 800 1000 0.0 0.5 1.0 1.5

Fig. 5. Ratio of primary production (mg Cm2d1) to plank-tonic community respiration (mg Cm2d1), i.e., P=R ratio, versus integrated primary productivity (mg Cm2d1) over euphotic zone. Values from meso- and oligotrophic systems are marked with solid (K) and open (J) circles, respectively. Horizontal dashed line represents P=R ratio equal to 1.

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Kuroshio subsurface water were the two major

nutrient sources into the ECS (Wong et al., 1998;

Liu et al., 2000b). To understand these compli-cated shelf ecosystems, previous studies divided the ECS into separated regions according to their physical properties (Gong et al., 1996, 2000). Since biological activities are more directly associated with nutrients, the ECS was therefore categorized into mesotrophic and oligotrophic systems based on nutrient concentrations in this and previous studies (Shiah et al., 2001).

Seasonal and spatial variations in phytoplank-ton biomass and primary production have been

reported in the ECS (Gong et al., 1996, 2000), and

their study also found large spatial variations of

Chl a (1.5–74.4 mg Chl m2) and primary

produc-tion (16–854 mg Cm2d1) (Table 1). Averaged

primary productivity is low in autumn

(341.37234.6 mg Cm2

d1) compared to the

summer (>1000 mg Cm2d1 in inner shelf;

Shiah et al., 2001) in the same study area. To regulate phytoplankton growth in the ECS, nutrients and light (especially in the inner shelf) have been suggested as the two most important

factors (Gong et al., 1996). Even though nutrient

concentrations were signiﬁcantly higher in

mesotrophic than in oligotrophic system, no differences were evident in Chl a values and primary production between these two systems (Fig. 2c,Table 1). Previous studies have suggested that growth of phytoplankton might be

phos-phate-limited in the ECS (Gong et al., 1996), But

this seems not to be the case here since the measured ratio of inorganic nitrogen to phosphate (i.e., N=P ratio; ca 1778) was close to the Redﬁeld ratio (Shiah et al., 2001). This implies that growth of phytoplankton in the mesotrophic system might be limited by other factors. Even though no direct evidence indicates that light might be the regulat-ing factor for phytoplankton growth in the mesotrophic system, light intensity is indeed lower

in the autumn than in summer (Gong et al., 2003).

In addition, light limitation can be indirectly supported by shallow euphotic zone (ca 27.3 m) in the mesotrophic system, which was about 50% shallower than that in oligotrophic system (ca

49.5 m; Table 1). In the oligotrophic system,

growth of phytoplankton was likely controlled

by nutrients, which were depleted in surface water in most regions of the ECS.

Planktonic community respiration (PCR) repre-sents integrated carbon consumption by compo-nents including bacterioplankton, phytoplankton,

planktonic protozoa, and zooplankton (Rowe

et al., 1986; Hopkinson et al., 1989; Kemp et al., 1994; Liu et al., 2000a). Respiration rates ranged

from 5.3–92.7 mg Cm3d1 in this study, which

are at the lower end of reported values of 3–647 mg O2dm3d1(i.e. 2.3–485.3 mg Cm3d1if assum-ing RQ=1) from the coastal, shelf and slope

regions (Williams, 1984; Biddanda et al., 1994).

Previous studies have shown that PCR was positively correlated to primary production in some occasions in estuary or coastal regions (Jensen et al., 1990a; Smith and Kemp, 1995). There was, however, no signiﬁcant relationship observed between PCR versus either Chl a or primary production in this study, and similar

results have been reported previously (e.g.,

Ro-binson and Williams, 1999). This suggests that PCR in the ECS was dominated by planktonic communities other than phytoplankton or was supported by other organic carbon sources rather

than in situ primary production (Turner, 1978;

Van Es, 1982).

Indeed, PCR was linearly regressed with proto-zoan biomass or multiple regressed with bacterial

and protozoan biomass (Fig. 3a, Eq. (1)). This

implies that organic carbon consumption by planktonic communities was more attributed to bacterial and protozoan communities. In aquatic ecosystems, it has been suggested that microbial communities, especially bacteria, play important

roles in organic carbon consumption (Rowe et al.,

1986;del Giorgio et al., 1997).Shiah et al. (2000a)

estimated that heterotrophic bacteria completely consume biogenic particulate organic carbon in the ECS, and our results show that bacterioplank-ton account for a large fraction of PCR (Eq. 1).

Even though bacterial respiration (RB) was not

measured directly, RB can be estimated from

bacterial production (PB) and bacterial growth

efﬁciency, which is equivalent to (PB=RBþ PB). A wide range of bacterial growth efﬁciency (5%– 60%;del Giorgio et al., 1997) has been reported, and it could vary along substrate gradient

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(Biddanda et al., 1994;del Giorgio et al., 1997). To estimate bacterial respiration, bacterial growth efﬁciency of 20% was assumed in this study. Estimated values of bacterial respiration contri-bute more than 39.2% of the PCR in the ECS, and this contribution fraction (i.e., 39.2%) is within

reported values from different shelves (Williams,

1984; Grifﬁth et al., 1990; Chin-Leo and Benner,

1992). Even though bacterioplankton contributed

a large fraction of PCR in this study, no signiﬁcant correlation was observed between PCR versus biomass or production of bacterial community (Fig. 3b). Weak correlation between bacterial production and community respiration also has

been found in other continental shelves (Chin-Leo

and Benner, 1992; Biddanda et al., 1994). This implies that larger organisms, in addition to bacterioplankton, may play an important role in PCR in the ECS.

In aquatic ecosystems, planktonic protozoa also could serve as another important organic carbon

consumer (Kemp et al., 1994). This also holds true

in the ECS where a signiﬁcant amount of PCR was

contributed by the protozoan community (Fig. 3a,

Eq. (1)), and this is especially obvious in regions with high respiration rates where protozoan

biomass also peaked simultaneously (Table 1,

Fig. 4). Carbon consumption rate for ciliates has been estimated and ranged within 28.8–67.2% of

cell Cd1 for hetero- and mixotrophic ciliates

using single species measurement (Stoecker and

Michaels, 1991). High respiration rate therefore, can be expected in regions with high protozoan biomass, and this was indeed observed in this

study (Table 1, Fig. 4). Although protozoan

biomass was about 10-fold different, ciliates dominated the mixotrophy found at stations located outside of the Yangtze River (i.e., Sts. 18, 19, 20, 21, and 22) in the mesotrophic system and at stations with high respiration rate in oligotrophic system (i.e., St. 14, 15, and 16) (data not shown). This implies that there must have been a large quantity of other substrates, in addition to bacterioplankton, to support high protozoan growth in the oligotrophic system.

All of this indicates that community respiration was dominated by both bacterial and protozoan communities in the ECS (Eq. (1)). To elucidate

how components contributing to PCR varied in different trophic systems, relative contributions were estimated by assuming dominance by only

bacterial and protozoan communities (Table 2).

Results show no signiﬁcant difference in measured PCR and estimated PCR (p ¼ 0:24), and the relative difference i.e. (measured PCR–estimated PCE)/measured PCR*100%) between measured and estimated PCR was only about 6.8%748.0%

(mean7SD) (Table 2). This indicates that PCR in

Table 2

Relative contribution to planktonic community respiration by bacteria and protozoa in the mesotrophic (Meso) and oligotrophic (Oligo) systems in the ECS. Bacterial respiration (RB) over ZE was estimated using bacterial production (PB;

mg Cm3d1) and assuming 20% growth efﬁciency (del

Giorgio et al., 1997) where bacterial growth efﬁciency is

equivalent to (PB=RBþ PB). Respiration by protozoa (RP)

over ZE was estimated using protozoan biomass (mg Cm3)

and assuming respiration rate of 45.6% of cell Cd1 (i.e., average rate of heter- and mixotrophic ciliate from Stoecker

and Michaels, 1991). Planktonic community respiration (PCR*;

mg Cm3d1) was therefore estimated using RB plus RP:

Relative contribution of respiration by bacteria (%RB) and

protozoa (%RP) were calculated using RB or RP divided by

(RBþ RP), respectively. Planktonic community respiration

(PCR; mg C m3_d1_{) measured from incubation was included}

for comparison Regions Sts PCR PCR* %RB %RP Meso 2 5.3 8.1 55.8 44.2 Meso 3 — 5.1 96.6 3.4 Meso 4 82.9 112.9 99.9 0.1 Meso 6 — 40.3 99.0 1.0 Meso 7 22.0 8.3 44.0 56.0 Meso 8 51.8 16.0 18.5 81.5 Meso 18 38.3 30.1 92.7 7.3 Meso 19 14.2 20.3 90.7 9.3 Meso 20 23.9 17.3 66.8 33.2 Meso 21 39.0 17.8 43.8 56.2 Meso 22 — 18.5 85.0 15.0 Oligo 1 46.0 15.1 58.2 41.8 Oligo 9 — 40.1 8.9 91.1 Oligo 10 24.7 16.9 12.2 87.8 Oligo 14 92.7 71.7 5.8 94.2 Oligo 15 67.8 103.1 5.1 94.9 Oligo 16 75.5 97.8 5.9 94.1 Oligo 17 26.4 38.8 15.4 84.6 Oligo 23 — 35.2 9.7 90.3 Oligo 24 — 15.2 16.3 83.7 (—) No data measured.

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the ECS could be estimated reasonably from bacterial and protozoan communities. Results showed that bacteria contributed more than 72.1% of PCR, while respiration by protozoa represented less than 27.9% of PCR in the

mesotrophic system (Table 2). Respiration

domi-nated by the bacterial community has been observed in estuaries and coastal ecosystems (Grifﬁth et al., 1990; Findlay et al., 1992; Kemp et al., 1994). Bacterial biomass and production

(both expressed per m3 unit) were higher in

the mesotrophic than in the oligotrophic system in this study, and similar results have been

observed previously in the ECS (Shiah et al.,

2000a). High bacterial respiration therefore can be expected in areas with high bacterial biomass and production. The opposite pattern was observed in the oligotrophic system where the protozoan community accounted for more than 84.7% of PCR, and the relative contribution could even reach 94.4% at stations with high

respiration rates (Fig. 4, Table 2). Bacterial

respiration was relatively unimportant in the oligotrophic system.

To explore whether the ecosystem is auto- or

heterotrophic, the P=R ratio was applied (Odum,

1956). Overall the ECS ecosystem was net

hetero-trophic during the study period, as evidenced by

the small P=R ratio (ca 0.33; Fig. 5). Between

trophic systems, the mean value of P=R ratio was slightly higher in mesotrophic than in oligotrophic

systems, but not signiﬁcantly different (Fig. 5).

Several reasons might accounted for higher P=R ratio in our case, it might be attributed mostly to the relatively lower respiration in the mesotrophic system. Since no signiﬁcant difference in

respira-tion rate (per m3) was evident between the two

systems, lower integrated rates in the mesotrophic system was simply due to the rates integrated over

shallower ZE (Table 1). To support high

respira-tion rate by organisms in a heterotrophic

ecosys-tem, besides in situ carbon production,

allochthonous organic carbon must be supplied either from outside of the system and/or resus-pended or remobilized from superﬁcial sedimenta-tion. In the ECS, allochthonous DOC has been enriched by riverine discharge and remobilization

of superﬁcial sedimentation (Cauwet and

Mack-enzie, 1993). It also has been observed that organic carbon is heavily subsidized from land and wet-land ecosystems into coastal and shelf ecosystems (Hopkinson, 1985; Moran et al., 1991; Findlay et al., 1992). Even though there was no direct evidence to prove this hypothesis in this study, it could be indirectly supported by the low primary production and high bacterial production found in coastal regions (Table 1).

To support high bacterial metabolism in this low-productivity shelf, allochthonous organic car-bon supplied from outside of the system is suggested. Based on chemical and physical proper-ties (Fig. 2), it is likely that organic carbon from riverine input was the primary source. Previous studies also have shown that signiﬁcant amounts of organic carbon are transported from Chinese

rivers onto the shelf (Cauwet and Mackenzie,

1993; Chen and Wang, 1996). Resuspension of organic-rich sediment can be another extraneous carbon supply into the ECS water column. The ECS is a highly productive continental shelf, with an annual mean productivity of about

550 mg Cm2d1 (Gong et al., 2000). Seasonally,

primary productivity can reach more than

1000–1900 mg Cm2d1in the inner shelf

ecosys-tem or within the upwelling region, especially

during summer (Guo, 1991; Gong et al., 2000;

Gong and Liu, 2003). Signiﬁcant deposition of particulate organic carbon on superﬁcial sedimen-tation has been found during blooms or highly

productive periods in estuaries and coastal

regions (Malone et al., 1988; Jensen et al.,

1990b). In shallow aquatic ecosystems, forcing

by strong physical events (e.g., monsoons,

tropical depressions, and typhoons), organic-rich sediment can be easily re-suspended into the water

column and utilized by organisms (Ritzrau and

Graf, 1992; Dickey et al., 1998; Shiah et al., 2000b).

Although sedimentation rates in the ECS are high, the organic carbon content in the sedimenta-tion was not as high as expected and varied

between 0.3 and 0.6 wt% (Lin et al., 2000). Even

though an important portion of the organic carbon in sediment was utilized either by sulfate

reduction or burial,Lin et al. (2000)estimated that

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missing. Organic carbon resuspended from sedi-ment and respired by planktonic communities therefore may serve as an important link for the missing carbon. Strong physical disturbance on the sediment surface could easily occur in the shallow continental shelf of ECS, which has water

depth between 50 and 100 m (Wang et al., 2000).

Resuspension of organic carbon from sediment is suggested by the high POCvalues observed in bottom water (data not shown). Strong resuspen-sion might have been caused by super Typhoon Zeb, which passed along outer shelf of the ECS

about 2 weeks prior to the study (http://

www.weather.unisys.com/hurricane/). That more than 50% of stations had MLD deeper than 70% of the water column depth can be evidenced as

other persisting typhoon effect (Table 1). In

addition, intrusion of the Kuroshio waters with high DOCconcentrations may be another poten-tial allochthonous source, although the magnitude

varies temporally (Hung and Lin, 1995; Hung

et al., 2000).

The low P=R ratio suggests that continental shelf of the ECS was the main carbon source

during the study periods (Fig. 4); however, it is

difﬁcult to predict or conclude whether the ECS is a net carbon sink or source based on a single survey. In coastal regions, a low P=R ratio (i.e., o1) is usually observed in systems with low

primary production (Duarte and Agust!ı, 1998

and their Fig. 3). In this study, low primary

production was measured, with a mean value of

341.3 mg Cm2d1 which was lower than the

annual mean value (ca, 550 mg Cm2d1; Gong

et al., 2000). Based on air–sea difference of fCO2, several studies have concluded that the ECS is a

CO2sink, which is contrary with the present study

(Peng et al., 1999; Tsunogai et al., 1999; Wang et al., 2000). Those studies were either conducted

in the area north of the present study (Tsunogai

et al., 1999; Wang et al., 2000) or in different

seasons (Peng et al., 1999). Besides, high fCO2

value has been measured in the surface water in a limited area of the continental shelf,

especially after a storm event (Tsunogai et al.,

1999). Storm-induced and enhanced

phyto-plankton growth and/or primary production have been measured about week after events in

or nearby the study area (Chang et al., 1996;

Shiah et al., 2000b). Resuspension of organic-rich sediment and elevated bacterial growth rates also have been found after the passage of storms

in various coastal zones (e.g., Ritzrau and Graf,

1992; Dickey et al., 1998). All this suggests

that planktonic community respiration rate

will be enhanced following high production, subsequent high growth rates of micro-organisms, and/or resuspension of organic-rich sediment induced by storm events. Typhoon Zeb passed along the outer shelf of the ECS about 2 weeks before the present study, which may explain why respiration rates, protozoan biomass, and POCconcentrations were high, but primary

productivity was relatively low (Table 1, Fig. 4).

Episodic storm events therefore may have impor-tant impact on carbon consumption in shallow continental shelf, such as the ECS. To comprehen-sively understand carbon budget in the ECS, the impact and function of strong physical distur-bances effect carbon consumption merit further study.

In summary, high bacterial biomass and pro-duction and low protozoan abundance were found in the mesotrophic part of the ECS. The opposite pattern was observed in oligotrophic system, which had low bacterial biomass and production and high protozoan abundance. Integrated

re-spiration rates ranged from 127.6 to

4728.6 mg Cm2d1, and respiration was linearly

related to protozoan biomass or multiply regressed to both bacterial and protozoan biomasses. In the mesotrophic system, bacterial respiration ac-counted for more than 72.1% of PCR, whereas in the oligotrophic system, respiration was domi-nated by protozoa, contributing more than 84.7%

to the total rates. Low ratio of P=R (i.e., o1)

suggested that the ECS was a net heterotrophic system. This implies that in situ organic carbon production could not sustain consumption by respiration. To support high rates of respiration, allochthonous organic carbon supplied from outside of this ecosystem is suggested. Allochtho-nous organic carbon supplied from riverine input along the China coast and resuspension of

superﬁcial sediment are two most potential

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Acknowledgements

This research was supported by the National Science Council of the Republic of China under grant NSC-87-2811-M002-003 and NSC-91-2611-M003-003-OP3. The work of C.-C. Chen was performed while the recipient of a grant from NSC, ROC (Grand no. NSC-88-2811-M002-0033). We thank Y.-H. Wen, B.-W. Wang, and K.-J. Liu for assistance with the analyses of nutrients, Chl a and primary productivity mea-surement. POCanalysis was aided by Mr. J.-Y. Chen. Thanks also go to two anonymous reviewers for their valuable comments. We are also grateful to the ofﬁcers and crew of the Ocean Researcher I for their assistance. This article is NCOR (Na-tional Center for Ocean Research, ROC) contri-bution #43.

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