The coupling of oligotrich ciliate populations andhydrography
in the East China Sea: spatial andtemporal variations
Kuo-Ping Chiang
a,*, Chiu-Yi Lin
a, Chung-Hsien Lee
a, Fuh-Kwo Shiah
b,
Jeng Chang
caInstitute of Environmental Biology and Fisheries Science, National Taiwan Ocean University, Keellung 202-204, Taiwan, ROC bInstitute of Oceanography, National Taiwan University, P.O. Box 23-13, Taipei, Taiwan, ROC
cInstitute of Marine Biology, National Taiwan Ocean University, Keellung 202-24, Taiwan, ROC Accepted16 December 2002
Abstract
Variations in the spatial andtemporal distribution of oligotrich ciliate populations in the East China Sea were investigatedduring four cruises of the R/V Ocean Researcher I between December 1997 andOctober 1998. Over the entire continental shelf, a seasonal cycle was foundwith a distinct 3–5-foldincrease in the abundance of oligotrich ciliates in summer. This increase appeared to be induced by the tremendous summertime runoff from the Changjiang. A radial-type spatial distribution pattern also was observed in summer, with population densities higher toward the Changjiang plume but highest of all in the margins of the plume. In spring andfall, the spatial distribution of the oligotrich ciliates was closely correlatedto the abundance of cyanobacterium Synechococcus. In summer in the plume region, mixotrophic ciliates accountedfor over 50% of the total ciliate population, comparedto less than 30% outside the plume or that in other seasons. We propose a model in which these ciliates constitute part of the pathway through which the particulate anddissolvedorganic carbon in the runoff water is incorporatedinto the oceanic foodweb.
r2003 Elsevier Science Ltd. All rights reserved.
1. Introduction
For some years now, researchers have recog-nizedthat bacteria andprotists play essential roles
in marine pelagic ecosystems (Pomeroy, 1974).
Planktonic ciliates are an important component in the microbial foodchain, which is also referredto as the microbial loop (Azam et al., 1983), andthey may help bring about trophic flux andnutrient
cycling (Laybourn-Parry, 1992). In a typical
oligotrophic oceanic ecosystem, organic exudates, or dissolved organic carbon (DOC), from phyto-plankton are usedby bacteria, andthese, in turn,
are consumedby protistan predators, such as
planktonic microflagellates (Fenchel, 1982; Sherr
et al., 1991) andciliates (Sherr andSherr, 1987; Fenchel andJonsson, 1988). Such picoautotrophs as Prochlorococcus and Synechococcous similarly make a significant contribution to phytoplankton
biomass andproductivity in marine ecosystems
(Stockner andAntia, 1986;Shiomoto et al., 1997). Typically, in the subtropical shelf water of the East
*Corresponding author. Fax: +886-2-2462-1016. E-mail address:kpchiang@mail.ntou.edu.tw (K.-P. Chiang).
0967-0645/03/$ - see front matter r 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0967-0645(03)00023-7
China Sea (ECS), picophytoplankton comprise 25–86% of all chlorophyll a and19–72% of
primary production (Chen, 2000; Chiang et al.,
2002). However, picophytoplankton are too small
to be effectively utilizedby metazoan grazers. Picophytoplankton have to be repackedvia the microbial foodchain before their production can
enter the grazing foodchain (Marshall, 1973).
The ECS, the largest marginal sea in the western North Pacific, is a vast area of shallow water into which flows the tremendous river runoff from the
Changjiang (Yangtze River; see Fig. 1). With an
annual mean of about 3 103m3s1, water
discharge reaches its maximum in summer
(Beardsley et al., 1985). The fact that phytoplank-ton productivity is less than likely sufficient to support the demand made by bacteria in the shelf
area of the ECS has led Shiah et al. (2000) to
suggest that the substantial shortfall is made up by
non-phytoplanktonic, allochothonous sources.
The discharged fresh river water, therefore, might, ultimately affect the spatial andtemporal patterns of the ciliate populations and, as a consequence, the microbial foodweb in these shelf waters. New
highly supportive evidence for this theory is presentedin this paper.
Oligotrich ciliates are known to be a major
component of ciliate community in the ECS (Ota
andTaniguchi, 2003). For the first time, their spatial andtemporal variations are examinedin the study, and the relationships between ciliate population density and surface salinity, particulate organic carbon (POC), andbacterial productivity (BP) in summer were analyzed. Besides these, this study discusses variations in the population of mixotrophic ciliates (MC) andthe standing stock of cyanobacteria.
2. Materials and methods
During four cruises of the R/V Ocean Research-er I in DecembResearch-er (wintResearch-er) 1997, andMarch (spring), June (summer), andOctober (fall) 1998, surface temperatures andsalinity were measured at a total of 31–36 sampling stations along seven cross-shelf transects (Fig. 1). Water samples were collectedat 16–22 sampling stations along four of
Fig. 1. ECS survey stations were locatedalong seven cross-shelf transects (white anddark circles) on the four sampling cruises of 1997 and 1998. Dark circles indicate the stations where water samples were collected for the present study. Dashed lines indicate the Changjiang plume margin.
the cross-shelf transects, indicated as Transects A,
B, C andD (Fig. 1). A Sea Bird-General Oceanic
Rosette assembly with 20 l Go-Flo bottles were then employedto recordtemperature andsalinity as well as to collect water samples from 5 to 11 different depths in the water column (2 m-bottom or 100 m). The seawater samples were subse-quently fixedin neutralizedformalin (2% final concentration). To prevent degradation of the pigments in the plastids that had been ingested intact by the ciliates, the fixedsamples were stored
in a cool (4C), dark place until they could be
examinedunder microscope.
Oligotrich ciliate cells in a 100-ml sample were
concentratedfollowing the Uterm.ohl methodand
were identified and thoroughly counted in each sample using an invertedepifluorescence
micro-scope (Nikon-Tmd300) at 200 or 400 (Hasle,
1978). All of the oligotrich ciliates were classified as heterotrophic ciliates (HC) or MC basedon their autofluorescence. Plastids that had been retainedintact by the mixotrophic oligotrich ciliates were recognizable by redfluorescence they emittedwhen excitedwith light at 450–490 nm (blue light).
Next, water samples (0.5–2.0 l) for POC mea-surements were first filteredthrough a 200 mm mesh to remove zooplankton andthen through a
pre-combusted(550C) 25 mm GF/F filter for 1 h
(pumping pressure o100 mm Hg). The GF/F
filters were then wrappedin pre-combusted aluminum foil in the next stage, andstoredat
4C. After being dried and acid fumed, the POC
concentrations were measuredwith a CHN analyzer (Fisons; NA1500). Finally, a one-way ANOVA was usedfor statistical analysis andthese results were comparedusing the least significant difference (LSD) method.
3. Results
3.1. Ciliate community
In ECS, the cell size of the ciliate community
showeda gradual decrease from inner to outer
shelf in all seasons (Fig. 2). The mean cell size also showedsignificant seasonal variations, especially
WINTER y = -0.1059x + 36.099 R2 = 0.354, p < 0.05 ESD (um) 0 10 20 30 40 50 60 SPRING ESD (um) 0 10 20 30 40 50 60 SUMMER ESD (um) 0 10 20 30 40 50 60 FALL Depth (m) 0 2 0 4 0 6 0 8 0 100 120 140 160 ESD (um) 0 10 20 30 40 50 60 y = -0.1374x + 40.58 R2 = 0.3331, p < 0.05 y = -0.0289x + 28.165 R2 = 0.1959, p < 0.05 y = -0.1764x + 41.746 R2 = 0.7162, p < 0.05
Fig. 2. The cross-shelf distribution of ESD of oligotrich ciliate in all four seasons in the ECS.
in summer. The equivalent spherical diameter
(ESD) in winter, spring, andfall were 29.670.93,
32.171.51, and30.471.21 mm, respectively. In contrast, Summer ciliates hada smaller size at 26.170.52 mm ESD (Po0:05; ANOVA andLSD analysis).
During the fall cruise, extra effort was made to obtain a general picture of species composition. On the basis of morphological characteristics, the
ciliates were classifiedinto three groups (Song
et al., 1999): Strombilidiids, Tontonia in Strobili-diidae, and Strombilidiids species other than Tontonia. The most dominant component was
Strombilidiids, making up 66.6%715.6%,
fol-lowed by other Strombilidiids at 31.2%714.7%,
and Tontonia at 2.1%72.7%.
3.2. Horizontal distribution
In winter, spring andfall, the distributions
pattern of surface salinity andtemperature in the entire ECS ran roughly parallel to the coastline (Fig. 3), andsalinity rangedbetween 32 and34 psu at almost all stations. By contrast, during summer, a radial distribution pattern appeared in front of the mouth of the Changjiang, andin the center of the radial pattern, salinity was as low as 25 psu. The hydrographic features of the ECS, therefore, appearedto be significantly influencedby summer runoff from the Changjiang. It was also foundthat the extent andlocation of the plume closely approximatedthe typical Changjiang plume, as
determined by Gong et al. (1996) in which they
defined the temperature and salinity of the summer
plume as >23C and o31 psu, respectively. In
the present paper, the plume is defined as
T ¼ 22226C andsalinity aso31 psu.
In the same vein, the horizontal density dis-tribution of total oligotrich ciliates (TC) made
pronouncedseasonal change (Fig. 4). From winter
to spring, relatively few (1–50 104 cells m3)
ciliates existedin the water column. Nevertheless, abundance tended to increase from the inner shelf to the outer shelf, with the maximum population density observed at the northeast outer shelf. Ciliate abundance increased in summer (30– 180 104 cells m3), distributed in a pattern that matchedthat of radial surface salinity, again with
a high density (>60 104 cells m3) area in the
Changjiang plume (o26C; o31 psu). Then, in
the fall, ciliate abundance generally decreased
(o20 104 cells m3 at most sampling stations),
but a high ciliate abundance was still found in the
center of the continental shelf (>70 104
cells m3).
In winter, spring andfall, HC andMC hada similar distribution pattern to that of TC. HC were the most abundant components of the oligotrich ciliates, representing between 70.5% and92.2% of the total number of oligotrich ciliates. In summer, MC abundance was high within the margin of the Changjiang plume (>120 104cells m3), where it accountedfor >50% of the total number
com-paredtoo30% comprisedoutside the plume.
3.3. Vertical distribution
Water column profiles revealedvery different
patterns of vertical distribution of TC and MC between Kuroshio Water (St. 11), Shelf Mixing Water (St. 16), andthe Changjiang plume (St. 19). In Kuroshio Water, the abundance of TC was, for the most part, uniform in the first 100 m andMC was rarely apparent in every season (Fig. 5). In the middle part of the continental shelf (shelf mixing water), a decrease in abundance was observed with depth and a subsurface ciliate maximum layer was observedin the bottom of euphotic zone (euphotic zone=42 m). MC was mostly evident in the euphotic zone in the fall andalso hada maximum abundance at 40 m. In summer, the abundance of TC was significantly higher than in other seasons in the Changjiang plume, andthe vertical distribu-tion pattern of TC differed considerably from that in other seasons. A maximum abundance of TC was observedat 2 m, but TC then decreasedwith depth. A similar vertical profile to that of TC was observedin the case of MC, while the abundance
rangedfrom 40–160 104 cells m3, again being
highest relative to that in other areas or seasons in the ECS.
3.4. Seasonal variations
Over the entire ECS, an annual pattern of
24 25 26 27 28 29 30 31 32 33 200 m 1000 m 33 30 127 126 125 124 123 122 121 120 119 118 128 129 130 24 25 26 27 28 29 30 31 32 33 22 200 m 1000 m 24 25 26 27 28 29 30 31 32 33 200 m 1000 m 29 28 27 26 29 30 31 LONGITUDE (οE) LONGITUDE (οE) 24 25 26 27 28 29 30 31 32 33 LATITUDE ( οN) LATITUDE ( οN) 200 m 1000 m 22 24 24 24 24 25 26 27 28 29 30 31 32 33 200 m 1000 m 33 28 33 24 25 26 27 28 29 30 31 32 33 LATITUDE ( οN) 12 20 0 m 10 0 0 m 12 24 25 26 27 28 29 30 31 32 33 200 m 1000 m
LONGITUDE (oE) LONGITUDE (oE)
24 25 26 27 28 29 30 31 32 33 LATITUDE ( οN) LATITUDE ( οN) LATITUDE ( οN) LATITUDE ( οN) LATITUDE ( οN) 16 14 14 16 24 200 m 1000 m WINTER WINTER SPRING FALL SPRING SUMMER SUMMER FALL LONGITUDE (οE) LONGITUDE (οE) LONGITUDE (οE) LONGITUDE (οE) 127 126 125 124 123 122 121 120 119 118 128 129 130 127 126 125 124 123 122 121 120 119 118 128 129 130 118 119 120 121 122 123 124 125 126 127 128 129 130 127 126 125 124 123 122 121 120 119 118 128 129 130 118 119 120 121 122 123 124 125 126 127 128 129 130 127 126 125 124 123 122 121 120 119 118 128 129 130 127 126 125 124 123 122 121 120 119 118 128 129 130 (A) (B)
winter, spring andfall, the average surface salinity was greater than 33.0 psu, unlike that in summer when it was lower than 31.0 psu.
The fluctuations in depth-weighted average TC abundance from surface to bottom or 100 m were
generally parallel to seasonal variations in surface
salinity (Fig. 6A). A low standing stock of TC
(11.41–18.43 104cells m3) was observedduring
seasons of high salinity, namely winter, spring and fall, whereas the standing stock sharply increased
(A) TC HC HC MC MC TC 24 118 119 120 121 122 123 124 125 126 127 128 129 130 25 26 27 28 29 30 31 32 33 LATITUDE ( οN) 5 24 118 119 120 121 122 123 124 125 126 127 128 129 130 25 26 27 28 29 30 31 32 33 5 24 25 26 27 28 29 30 31 32 33 0.1 0.1 0.1 24 25 26 27 28 29 30 31 32 33 15 10 5 1 1 24 25 26 27 28 29 30 31 32 33 10 1 5 25 26 27 28 29 30 31 32 33 0.1 0.1 LATITUDE ( oN) LATITUDE ( oN) LATITUDE ( oN) LATITUDE ( oN) LONGITUDE (οE) LATITUDE ( οN) LONGITUDE (οE) 118 119 120 121 122 123 124 125 126 127 128 129 130 LONGITUDE (οE) 118 119 120 121 122 123 124 125 126 127 128 129 130 LONGITUDE (οE) 118 119 120 121 122 123 124 125 126 127 128 129 130 LONGITUDE (oE) 118 119 120 121 122 123 124 125 126 127 128 129 130 LONGITUDE (οE) (A) (B)
Fig. 4. Horizontal distribution of total ciliate (TC), heterotrophic ciliate (HC) and mixotrophic ciliate (MC) abundance ( 104 cells m3) in the ECS in (A) winter (December 1997); (B) spring (March 1998); (C) summer (June 1998); and(D) fall (October 1998).
to 57.81 104 cells m3, representing a 3–5 fold difference, in the low salinity season (summer). Although similar patterns were also foundfor HC
andMC (Fig. 7A), one-way ANOVA andLSD
showedthat seasonal density fluctuations were
significant only for TC andHC (Po0:05), but not
TC TC HC HC MC MC 24 25 26 27 28 29 30 31 32 33 40 60 20 60 40 24 25 26 27 28 29 30 31 32 33 1 24 25 26 27 28 29 30 31 32 33 24 25 26 27 28 29 30 31 32 33 10 35 35 24 25 26 27 28 29 30 31 32 33 0.1 118 119 120 121 122 123 124 125 126 127 128 129 130 24 25 26 27 28 29 30 31 32 33 30 60 90 120 LONGITUDE (οE) 118 119 120 121 122 123 124 125 126 127 128 129 130 LONGITUDE (οE) LATITUDE ( οN) LATITUDE ( οN) 118 119 120 121 122 123 124 125 126 127 128 129 130 LONGITUDE (οE) 118 119 120 121 122 123 124 125 126 127 128 129 130 LONGITUDE (οE) 118 119 120 121 122 123 124 125 126 127 128 129 130 LONGITUDE (οE) 118 119 120 121 122 123 124 125 126 127 128 129 130 LONGITUDE (οE) LATITUDE ( οN) LATITUDE ( οN) LATITUDE ( οN) LATITUDE ( οN) (C) (D) Fig. 4 (continued).
Kuroshio Water (MC, St. 11) Abundance (104 cells m-3) 0 20 40 60 80 100 120 140 160 Depth (m) -160 -140 -120 -100 -80 -60 -40 -20 0 SPRING SUMMER FALL
Shelf Mixing Water (MC, St. 16) Abundance (104 cells m-3) 0 Depth (m) -60 -50 -40 -30 -20 -10 0 SUMMER FALL WINTER Kuroshio Water (TC, St. 11) Abundance (104 cells m-3) 0 50 100 150 200 250 Dept h (m) -160 -140 -120 -100 -80 -60 -40 -20 0 SPRING SUMMER FALL
Changjiang River plume (TC, St. 19) Abundance (104 cells m-3) 0 50 100 150 200 250 Depth (m) -30 -25 -20 -15 -10 -5 0 SPRING SUMMER FALL WINTER
Changjiang River plume (MC, St. 19) Abundance (104 cells m-3) 0 20 40 60 80 100 120 140 160 Depth (m) -30 -25 -20 -15 -10 -5 0 SPRING SUMMER FALL WINTER Shelf Mixing Water (TC, St. 16)
Abundance (104 cells m-3) 0 50 100 150 200 250 Depth (m) -60 -50 -40 -30 -20 -10 0 SUMMER FALL WINTER 20 40 60 80 100 120 140 160
Fig. 5. Vertical distribution of TC and MC abundance ( 104cells m3) in the ECS in Kuroshio Water (St. 11), Shelf Mixing Water (St. 16) andthe Changjiang plume (St. 19) in all four seasons.
for MC (P > 0:05). However, dividing the entire study area into the Coastal Water and Shelf
Mixing Water (respective definitions; see Chiang
et al., 2002) indicated that most of the seasonal fluctuations couldbe attributedto the population
dynamics in the Coastal Water (Figs. 7B andC).
The increases in the summer standing stocks of TC, HC andMC were, in fact, all statistically
significant in the Coastal Water (Po0:05), but was
not true in the Shelf Mixing Water (P > 0:05).
4. Discussion
Ciliate abundance levels reported in the ECS
rangedfrom 0.17 to 183.89 104 cells m3. This
range is similar to ciliate abundance commonly
foundin other oceanic ecosystems (Table 1), but
the degree of variation seems higher compared to the subarctic andsubtropic oceanic waters in western Pacific (Suzuki et al., 1998). Although the formaldehyde-based fixative has been shown to
underestimate ciliate abundance (Leakey et al.,
1994a;Stoecker et al., 1987, 1994), our results are still within the commonly acceptedrange, andour own test indicated similar counts from samples
fixedwith formalin andwith Lugol’s (data not
shown).
4.1. Spatial and temporal distribution
The ciliate distribution pattern showed a distinct variation with season. In spring andfall when Synechococcus abundance was not influenced by runoff from the Changjiang (summer) or the Yellow Sea ColdWater (winter), the ciliate and Synechococcus distributions seemed to match each
other reasonably well (Chiang et al., 2002), anda
positive correction couldbe established(Fig. 8) in the shelf area. This fact is indicative of a close coupling of Synechococcus andoligotrich ciliates in this subtropical shelf ecosystem, andit can be reasonably deduced that the coupling is caused by 0 10 20 30 40 50 60 70 80 90 100 Abundance ( × 10 4 cells m -3) 29 31 33 35 37 39
Surface Salinity (psu)
TC 0 10 20 30 40 50 0 1 2 0 20 40 60 BB BP
WINTER SPRING SUMMER FALL
WINTER SPRING SUMMER FALL
surface salinity Chl. a BB ( mg C m -3) BP ( mg C/ m -3 day -1) Chlarophyll a (10 -3 mg/l) -40 -20 (A) (B)
Fig. 6. Seasonal variations of (A) surface salinity anddepth-weightedaverage TC abundance ( 104 cells m3); and(B) bacterial productivity (BP, mg C m3day1), bacterial biomass (BB, mg C m3) andchlorophyll a (mg m3) (BP andBB data fromShiah et al., 2000).
Shelf Mixing Water
0 30 60 90 150 120
WINTER SPRING SUMMER
Abundance (
×
10
4 cells m
-3) HC MC TC
East China Sea
FALL HC MC TC Coastal Water HC MC TC 0 30 60 90 150 120 Abundance ( × 10 4 cells m -3)
WINTER SPRING SUMMER FALL
WINTER SPRING SUMMER FALL
0 30 60 90 150 120 Abundance ( × 10 4 cells m -3) (A) (B) (C)
Fig. 7. Seasonal variations of the depth-weighted average abundance of HC ( 104 cells m3), MC ( 104 cells m3) andTC ( 104 cells m3) in (A) the entire ECS; (B) Coastal Water; and(C) the Shelf Mixing Water.
a prey–predator relation. This hypothesis is
supportedbyChen (2001), who reportedthat the
grazing rate of oligotrich ciliates was controlledby Synechococcus abundance in the study area, which then hada significant influence on ciliate growth rate. In winter, the Synechococcus–ciliate relation-ship was disturbed when a higher Synechococcus
abundance in Yellow Sea Cold water (>1012
cells m2) was introduced into the study area
(Chiang et al., 2002).
Of particular interest is that in summer, several biological processes other than Synechococcus abundance appeared to have become major con-trolling factors. Strong evidence suggests that the levels of terrestrial substrate hadan effect on the spatial pattern of the ciliate standing stock in that period. A positive correlation between surface
salinity andsurface POC was noted(Fig. 9A),
which strongly implies that the major source of POC was the discharge from the Changjiang. Although DOC data was not available for examination, Chiangjiang showedalso brought significant amount of DOC. Furthermore, there was a goodcorrelation between POC andBP (Fig. 9B). Shiah andDucklow (1994) and Shiah et al. (2000)in fact have arguedthat this is highly indicative of the bottom-up control of bacteria. Finally, there was a positive correlation between
BP andTC (Fig. 9C), suggesting that TC may be
controlledby BP. We conclude from these findings that a very clear relationship exists between ciliate standing stock and the discharge of fresh water
from the Changjiang (cf. Smetacek, 1981;Leakey
et al., 1994b). We agree with Shiah et al. (2000) that this input of terrestrial material (i.e. POC and DOC) is in all likelihoodcrucial in supporting the microbial foodweb in the shelf water.
Ciliate standing stock in the shelf area equally displayed a distinctive temporal pattern (Fig. 6A). In temperate andpolar inshore waters, planktonic ciliate populations also exhibiteda clear seasonal cycle of high abundance during the spring and summer months but low abundance in the winter months, andsince this cycle fully agrees with the fluctuations in chlorophyll a concentration and
bacterial biomass (BB) (Smetacek, 1981;
Mon-tagnes et al., 1988; Leakey et al., 1994b), a tight trophic coupling between ciliates andorganic
Table 1 A comp arision of olig otrich ciliate abunda nce data Ocean ic region Samp ling time Samp ling depth s Remark M ethodAbun d ance (10 4 ce lls/m 3 ) Refe rence Trop ical neritic waters Yea r-roun d5 m 1 st ation Boui n’s 97–393 Ly nn et al. (1 991) Anta rctica ne arshor e water Yea r-roun d10 m 1 st ation Lugo l’s 23–126 Le akey et al. (1994 b) Trop ical oceanic water (No rthwest ern Indian Ocean ) Fall 5–9 depth s 9 st ations Lugo l’s 3.1–82.3 (me an value) Le akey et al. (1996 ) Temperatur e neritic wat er Winte r 1 0 depth s 2 1 stat ions Lugo l’s 16.3–79.2 (we ighted mean ) Jam es andHall (1995) Suba rctic oceanic water (West ern Pacific) Sprin g 6–12 depth s 6 st ations Form aldeh yde 55.73–14 8.88 (me an valu e) Su zuki et al. (1998 ) Suba rctic of oceanic water (West ern Pacific) Fall 6–12 depth s 3 st ations Form aldeh yde 22.38–40 (me an value) Su zuki et al. (1998 ) Subtro pic of ocean ic water (Western Pacific) Fall 6–12 depth s 6 st ations Form aldeh yde 5.38–44.8 8 (me an value) Su zuki et al. (1998 ) Subtro pic of Weste rn Pacific (Eas t Chin a Sea) Thre e seasons 7–14 depth s 7–14 station s Form aldeh yde 3–146 (we ighted mean ) Ot a andTanigu chi (2003 ) Subtro pic of Weste rn Pacific (Eas t Chin a Sea) Four season s 5–11 depth s 16–2 2 station s Form aldeh yde 0.17–183 .89 (weigh ted mean) Th is study
carbon from phytoplankton andbacteria seems quite apparent. In the ECS, it may well be that the peak ciliate population densities observed in summer were also driven by an increased avail-ability of organic carbon, which in this case probably means bacteria rather than chlorophyll a sources in light of the absence of a chlorophyll a
peak in summer (Fig. 6B) in the ECS. In a
contemporaneous study of the ECS continental
shelf area, we foundthat while depth-weighted
average BP also did peak in summer, but the depth-weighted average BB reached its peak in
spring (Fig. 6B), i.e. several months earlier. To
explain the absence of a BB peak in summer, we suggest that a considerable amount of bacteria may have been consumedby phagoflagellates or phagociliates. This hypothesis is clearly consistent with, andhelps to explain, the high summertime ciliate standing stock that was found in the present study.
4.2. Relationship between MC and phytoplankton in the Changjiang plume
Following Gong et al. (1996) who determined
salinity in the plume as o31 psu, the summer
surface salinity data along the northern transect
(Transect D in Fig. 1) suggest that the center is
locatedaroundat St. 20 with Sts. 19, 21 and22 in
the plume margins (Fig. 10A).Fig. 10Aalso shows
that the abundance of total ciliates was higher within the plume region than outside it, although ciliate abundance was relatively low at the central station (St. 20). Within the plume region (but not outside it), mixotrophs made up the greatest share
of the oligotrich ciliate population (Fig. 10B).
Conversely, along the same transect at the same time, while the total BB remainedconstant, the standing stock of Synechococcous was low within the plume but it grew with increasing distance.
Chang et al. (2003) also reportedthat the
Synechococcus growth rate was 4–5 times higher
within the plume than that outside it (Fig. 10D).
The most likely explanation for these observations is that increasednutrient input from the Chang-jiang leads to an increase in Synechococcus productivity, but any increase in the abundance of these cyanobacteria is offset since Synechococ-cus are consumedby MC within the plume. The net result is, therefore, an increase in the number of MC. This hypothetical account is supported strongly by the tight relationship between MC and
WINTER 0 5 10 15 20 25 30 35 0 2 4 6 8 10 12 14 Syn. ( × 1011 cells m-2) Syn. ( × 1011 cells m-2) Syn. ( × 1011 cells m-2) TC ( × 10 4cells m -3) TC ( × 10 4cells m -3 ) TC ( × 10 4cells m -3) SPRING y = 4.6792x - 1.0982 R2 = 0.3877, p < 0.05 0 10 20 30 40 50 60 0 1 2 3 4 5 6 SUMMER 0 20 40 60 80 100 0 10 20 30 40 50 60 70 Syn. ( × 1011 cells m-2) 0 10 20 30 40 50 60 70 80 FALL y = 0.4664x + 1.2209 R2 = 0.3837, p < 0.05 0 20 40 60 TC ( × 10 4cells m -3)
Fig. 8. Relationships between integrated Synechococcus abundance ( 1011cells m2) and the depth-weighted average abundance of TC ( 104cells m3) in winter, spring, summer andfall.
Synechococcus abundance within the plume (but not outside it) (Fig. 11).
Some independent external evidence is available to indicate that MC and Synechococcus have a predatory/prey relationship because
phycoery-thrin, a pigment unique to Synechococcus (
Water-bury et al., 1979), has previously been identified in
some mixotrophs (McManus andFuhrman, 1986).
On the other hand, picophtoplankton is also a major foodsource for mixotrophic nanoflgellate (Craon, 2000). Thus, we also argue that another hypothesis may be that the great part of picophy-plankton was consumedby nanoflagellate. Then
these pigment-containing nanoflagellates were
transportedto the ciliate community. It has been
proposedelsewhere that the retainedplastids in
MC may come from cyanobacteria (Bernardand
Rassoulzadegan, 1994) or photosynthesis nano-flagellate (Craon, 2000). All of the above observa-tions support the conclusion that the discharged fresh water of the Changjiang plume significantly affects the microbial foodweb in the region. 4.3. Photosynthesis rate of MC and the production of TC
Putt (1990)has reportedthat the concentration
of chlorophyll a rangedfrom 21 to 99 pg cell1in
y = -1.6839x + 65.352 R2 = 0.5442 p < 0.05 0 5 10 15 20 25 30 22 24 26 28 30 32 34 36
Surface Salinity ( psu )
POC ( M) R2 = 0.3663 p < 0.05 0 20 40 60 80 160 140 120 100 0 5 10 15 20 25 30 BP (mg C m -3) R2 = 0.3206 0 0 10 20 40 60 80 20 30 40 50 60 70 80 90 100 200 180 160 140 120 100 BP (mgC m-3 day-1) TC ( × 10 4 cells m -3) y = 2.9159x + 21.932 POC (M) y = 0.2205x + 24.24 p < 0.05 (A) (B) (C)
Fig. 9. Relationships between (A) surface salinity andPOC; (B) POC; andBP and(C) BP andTC in summer (BP andBB data from Shiah et al., 2000).
mixotrphic oligotrich ciliates. Basedon this figure, the maximum average contribution rate of MC to total chlorophyll a in winter, spring, summer and fall are 0.3%, 1.0%, 2.8% and0.7%, respectively. From these results, we are confident that ciliate photosynthesis is likely negligible in the general continental shelf ecosystem of the ECS but that it does have relative importance in the Changjiang plume, where the average contribution rate is 7.7% with the highest value (24.2%) occurring in the margin, just as seen in the high contribution rate observedin the Nordic Sea in summer (24%,
Putt, 1990). On the other hand, according toLee (2000), the average seasonal ciliate production is 29.2 (winter), 8.8 (spring), 80.6 (summer), and
25.7 mg C m2d1 (fall), andthe rate of ciliate
carbon demand for primary production is respec-tively 17.8%, 6.5%, 109.7%, and25% in the ECS. From these results, we are reasonably sure that primary production cannot be sufficient to support the growth of the ciliate community in summer. It follows then that in summer, organic carbon from non-phytoplankton andallochotho-nous sources might play a very important role in 0 50 100 150 200 250 Abundance ( × 10 4 cells m -3) 23 25 27 29 31 33 35 37 39
Surface salinity (psu)
TC 0 10 20 30 40 50 60 70 80 90 100 MC / TC (%) 23 25 27 29 31 33 35 37 39
Surface salinity (psu)
MC / TC (%) Surface salinity Surface salinity 0 800 1000 1200 1400 1600 600 400 200 Biomass (mg C m -2) BB ST. 19 ST. 20 ST. 21 ST. 22 ST. 23 ST. 24 ST. 19 ST. 20 ST. 21 ST. 22 ST. 23 ST. 24 ST. 19 ST. 20 ST. 21 ST. 22 ST. 23 ST. 24 Syn-B 0 0.8 0.6 0.4 0.2 1 1.2 Syn
-growth rate (day
-1) (ND) (ND) ST. 19 ST. 20 ST. 21 ST. 22 ST. 23 ST. 24 (A) (B) (C) (D)
Fig. 10. Variations of (A) surface salinity (psu) and depth-weighted average abundance of TC ( 104cells m3); (B) MC/TC ratio (%); (C) Synechococcous biomass (mg C m2) BB (mg C m2); and(D) intrinsic growth rate of Synechococcous (day1) along the northern transect (Synechococcous andBB data fromShiah et al. (2000)andChang et al. (2000), respectively).
the microbial carbon cycle in the shelf area of the ECS.
Acknowledgements
We are grateful to Dr. K.-K. Liu of National Taiwan University andDr. G.-C. Gong of National Taiwan Ocean University for their constructive comments on this work. We also thank the officers andcrewmembers of the R.V. ‘Ocean Research I’. This study was supported by grants from the National Science Council, ROC, NSC 89-2611-M-019-007-K2.
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