Standing crop of planktonic ciliates in the East China Sea and their potential grazing impact and contribution to nutrient regeneration

Deep-Sea Research II 50 (2003) 423–442

Standing crop of planktonic ciliates in the East China Sea and their potential grazing impact and contribution to nutrient regeneration Takashi Ota*, Akira Taniguchi Graduate School of Agriculture, Tohoku University, Sendai 981-8555, Japan

Abstract The spatial distribution and standing crop of the ciliate community were investigated in the East China Sea during February to March 1993, September to October 1993, and July to August 1994. During these three periods, the ciliate community was dominated by aloricate forms, accounting for 50–93% of the total number of ciliates. All aloricate ciliates were assigned to three groups based on their trophic function: autotrophic ciliates (AC), mixotrophic ciliates (MC), and heterotrophic ciliates (HC). Sometimes AC constituted a sizable part of the ciliate community in abundance, but they were always less important in terms of biomass. MC, represented by oligotrichs of the genera Strombidium, Tontonia, and Laboea, were always a significant component in the upper water column and usually dominated during stratified periods in summer and autumn. HC were mainly comprised of oligotrichs of the genera Strombidium, Strobilidium, and Lohmaniella. They were common and most abundant in winter. Tintinnid ciliates (TC) were a minor component of the ciliate community, but they included of a large number of species, i.e. 74 species from 27 genera for all intact loricae in all seasons. The standing crop of total ciliates varied with depth and season from o10 to 4180 cells l
1 and o0:01 to 6:25 mg C l
1 : Integrated values of total ciliates, ranging from 7.9 to 54:3  106 cells m
2 in abundance and from 8.5 to 136:3 mg C m
2 in biomass, were similar to those recorded from tropical and subtropical oligotrophic systems. Based on the results obtained by this first quantitative investigation on planktonic ciliates, their production, ingestion and excretion were calculated. Potential ingestion rates and their impact on reported primary production ranged, respectively, from 14% to 86%, except for the inner shelf where the impact was only 3% in the inner shelf
2
1 waters in winter. NHþ d ; equivalent to 0.1–93.8% 4 excretion rates of ciliates were estimated to be 0.1–63:8 mg N m of the nitrogen requirement by primary producers. These values suggest that the nitrogen excretion by ciliates could be significant contribution to sustainable primary productivity during summer and autumn. r 2002 Elsevier Science Ltd. All rights reserved.

1. Introduction It has long been recognized that the microbial community consisting of bacteria and protists *Corresponding author. Tel.: +81-222-717-8754; fax: +81222-717-8734. E-mail address: [email protected] (T. Ota).

plays an important role in marine pelagic ecosystems (Pomeroy, 1974). An important aspect of the microbial food chain, also termed the microbial loop, is that most of the primary production is respired within the epipelagic zone rather than being exported to depth or to higher trophic levels (Azam et al., 1983; Michaels and Silver, 1988; Sherr and Sherr, 1988). The microbial loop

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 4 6 1 - 7

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T. Ota, A. Taniguchi / Deep-Sea Research II 50 (2003) 423–442

dominates in the oligotrophic oceanic areas such as strongly stratified temperate waters, where organic exudates from phytoplankton are constrained within the euphotic zone, which, in turn, are used by bacteria there (Cushing, 1989). The latter are consumed by protistan predators such as planktonic microflagellates and ciliates (Hass and Webb, 1979; Fenchel, 1982; Davis and Sieburth, 1984; Gast, 1985; Jonsson, 1986; Sherr et al., 1989). On the other hand, the microbial food chain is the only available carbon pathway to consumers at higher trophic levels such as metazoan grazers, when autotrophs o5 mm; which are too small to be efficiently utilized by the metazoan grazers (Marshall, 1973), are responsible for a large proportion of the primary production (Moloney et al., 1991). In this case, the microbial food chain may play the role of exporting the biogenic carbon to higher levels (Legendre and Le Fe" vre, 1995). Planktonic ciliates are ubiquitous, and recently much attention has been focussed on their role as primary consumers of pico- and nano-sized producers (River et al., 1985; Verity, 1985; Sherr and Sherr, 1987; Rassoulzadegan et al., 1988), as well as nutrient regenerators (Ferrier-Page" s and Rassoulzadegan, 1994). It also has been stressed that ciliates are important food sources of metazoan zooplankton and fish larvae (Stoecker and Egloff, 1987; Wiadnyana and Rassoulzadegan, 1989; Jonsson and Tiselius, 1990; Stoecker and Capuzzo, 1990; Pierce and Turner, 1992; Lessard et al., 1996). Therefore, ciliates play a major role in carbon and energy fluxes in pelagic marine systems. It has recently been shown that many marine planktonic ciliates contain active plastids whose photosynthesis can contribute carbon equivalent to 2.5–7.5% body C h
1 (Stoecker and Michaels, 1991). Their photosynthesis contributes a significant part of the primary production in the microplanktonic size fraction (Stoecker et al., 1987, 1989) and is important especially in oligotrophic waters where total primary production is small (Putt, 1990). The abundance of such mixotrophic ciliates has been reported from polar and temperate waters, but little is known in tropical and subtropical waters (Bernard and Rassoulzadegan, 1994).

The East China Sea is characterized by vast but shallow shelf waters in the northwest with relatively low salinity water diluted by riverine input, and by the Okinawa Trough in the east where the subtropical Kuroshio Current flows. Phytoplankton standing crop and primary productivity are generally higher in the shelf waters and tend to decrease offshore toward the basin (Kawarada et al., 1968; Asaoka, 1975; Ning et al., 1988; Furuya et al., 1996; Hama et al., 1997). In these areas, however, no information is available on the standing crop and distribution of the planktonic ciliates. In this study, we examined for the first time the spatial distribution of biomass and species of the planktonic ciliates in the East China Sea.

2. Material and methods 2.1. Sample collection and analysis As part of Japan’s MASFLEX Program, water samples for the quantitative analysis of the ciliate community were collected on three cruises of R.V. Kaiyo, Japan Marine Science and Technology Center, in February to March 1993 (Cruise K92-09), September to October 1993 (Cruise K93-05), and July to August 1994 (Cruise K9404) along the PN line from Okinawa, Japan, to north of Shanghai, China (Fig. 1). In the following sections, the data obtained on these three cruises will be given in the order of season, i.e. winter (K92-09), summer (K94-04) and autumn (K93-05). The samples were taken from 7 to 14 depths in the surface layer down to 200 m or near the bottom with a CTD-RMS comprised of 12 Niskin bottles, and fixed in neutralized formalin seawater (2% final concentration). While significant loss of cells may be possible with this fixative (Gifford, 1985), formaldehyde has the advantage in distinguishing plastidic and non-plastidic cells under the epifluorescence microscope (Stoecker et al., 1987, 1994). The fixed samples were stored in a cool ðB41CÞ dark place for subsequent microscopic examination to avoid possible bleaching of pigments retained by ciliates.

T. Ota, A. Taniguchi / Deep-Sea Research II 50 (2003) 423–442

425

Fig. 1. Map of the East China Sea showing location of stations arranged on line PN in February/March (open circles) in 1993, and July/August (filled triangles) in 1994, and September/October (crosses) in 1993.

A subsample of exactly 100 ml was settled in a settling chamber for ca. 24 h in the dark. The possession of plastids of individual cells and their cell number were examined by autofluorescence under an Olympus IMT-2 inverted epifluorescence microscope at a magnification of 100–400 (Stoecker et al., 1989). The size of the cells also was measured with an eyepiece micrometer, and then the cell volume ðmm3 Þ was calculated by assuming standard geometric forms, which in turn was converted into biomass in terms of weight of carbon using a volume to carbon conversion factor of 0:14 pg C mm
3 (Putt and Stoecker, 1989). Its equivalent spherical diameter (ESD) also was calculated from the cell volume. Because preservation may cause separation of the cell body from the lorica of tintinnid ciliates, or may destroy the fragile cell (Paranjape and Gold, 1982), we took all intact loricae without injury caused by the predator’s attack into account in our estimate of biomass, regardless of presence/absence of the cell body. The species of the ciliates were identified by referring to Kofoid and Campbell (1929, 1939), Marshall (1969), Taniguchi (1997) for tintinnids and Small and Lynn (1985), Maeda

and Carey (1985), Maeda (1986) for aloricate ciliates. Data on temperature and salinity were cited from Kusakabe et al. (1998), those on nitrogenous nutrients from Watanabe et al. (1995) and those on chlorophyll a and primary production from Hama et al. (1997). 2.2. Estimates of ciliate productivity Since no data on in situ growth rates of ciliates are available, their potential productivity ðPc Þ was calculated assuming that all individuals actively grew and their growth rate was determined by their cell size and ambient temperature; i.e. following equation was employed: ln rm ¼ 1:52 ln T
0:27 ln V
1:44; where rm is the intrinsic growth rate ðd
1 Þ; T is the ambient temperature ð1CÞ; and V is the cell volume ðmm3 Þ (Muller . and Geller, 1993). This equation is particularly applicable to Strombidium and Strobilidium species, which dominate in the East China Sea, and gives rather conservative values at temperatures > 201C (Montagnes, 1996) compared to other equations proposed by Fenchel (1974), Finlay (1977), Montagnes et al. (1988), and Nielsen and Ki
rboe (1994).

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426

and usually ranged in size between 20 and 40 mm ESD. The smaller-sized fraction o20 mm ESD was relatively abundant in summer (17–34%), but less abundant in winter (0–16%) and autumn (3–14%). In terms of biomass, their contribution never exceeded 16%, even in summer. At least 20 species or types of aloricate ciliates were recognized by their characteristic outer morphology (Table 1); however, a precise cytological staining technique was not employed. Apart from individual species, all aloricate ciliates were

3. Results 3.1. Ciliate community The ciliate community was dominated by aloricate forms, accounting for 50–93% of the total number of ciliates, which were almost entirely dominated by oligotrichs. Their cell size showed a wide range from 8.6 to 114:2 mm ESD. Among them, ciliates of o50 mm ESD dominated numerically, making up 62–97% of the total cell number

Table 1 List of naked ciliates commonly found in the East China Sea in winter (W), summer (S) and autumn (A) with their cell size ðmean7S:D:Þ in length and width, average seasonal abundance and maximal density. Strombidium sp. A–H, Tontonia sp. A–C and Strobilidium sp. may not all be new species since distinction was made only on outer morphological bases Species or type

Autotrophic Mesodinium rubrum Mixotrophic Strombidium sp. A Strombidium sp. B Strombidium sp. C Strombidium sp. D (cf. conicum) Laboea strobila Tontonia gracilima Tontonia sp. A (cf. poopsia) Tontonia sp. B Tontonia sp. C (cf. simplicidens) Tontonia appendiculariformis Heterotrophic Strombidium sp. E Strombidium sp. F Strombidium sp. G Strombidium sp. H (cf. wulffi) Strombidium constrictum Strobilidium sp. Askenasia sp. Urotrichia sp. Vorticella sp.

n

Mean length ðmmÞ

Mean width ðmmÞ

Season

W

S

A

Maximum density ðcells l
1 Þ

(season, station, depth)

876

2676

1874

þþþ

þþ

þþþ

1670

(W, PN12, 1 m)

897 47 15 19

2574 3174 4178 47718

2074 1973 2575 2677

þþþ

þþ þþ

þþþ

1460 120 30 30

(A, PN12, 10 m) (S, PN10, 10 m) (W, PN6, 5–10 m) (W, PN8, 60 m)

12 474

132757 3076

61720 2775

þ þþ

þ þþ

þ þþþ

40 740

(W, PN5, 10 m) (A, PN8, 10 m)

53

43711

3577

þþ

þþ

þþ

160

(A, PN12, 5 m)

135 269

48711 3177

2876 2174

þþ þþ

þþ þþ

þþ þþ

200 280

(S, PN12, 5 m) (S, PN12, 10 m)

125

88725

47712

þþ

þþ

þþ

240

(S, PN12, 10 m)

68 19 272 35

34717 5474 3174 34710

29712 4773 2373 2377

þþ þþ þþ þ

þ þþ þþ

þþ þ

290 90 120 110

(W, PN7, 40 m) (W, PN7, 60 m) (W, PN7, 10 m) (S, PN10, 1 m)

46 53 525

3575 3179 1774

2274 41718 1877

þþ þ þþ

þþ þ þþþ

þþ þ þþ

100 40 690

(S, PN10, 10 m) (A, PN12, 10 m) (S, PN12, 20 m)

54 49

3077 2274

2376 1872

þþ

þþ þþ

þþ þþ

50 150

(S, PN1, 40 m) (S, PN12, 1 m)

þ þ þ: > 500 cells l
1 ; þþ: 50–500 cells l
1 ; þ: o50 cells l
1 :

þ þ

þ þ

T. Ota, A. Taniguchi / Deep-Sea Research II 50 (2003) 423–442

assigned to one of the following three groups in terms of trophic function: autotrophic ciliates (AC), mixotrophic ciliates (MC) and heterotrophic ciliates (HC). Mesodinium rubrum was the only species of AC recognized in this study. While this species occurred in every season and sometime constituted a sizable portion of the ciliate community abundance, it was always less important in terms of biomass because of its small size (26 mm in length). MC, which were always a significant component in the upper water column, were formed by oligotrichs of the genera Strombidium, Tontonia, and Laboea. When large peaks of abundance of MC occurred, a single species usually dominated the community. Large-sized MC, such as Tontonia appendiculariformis (88 mm in length) and Laboea strobila (132 mm in length), were basically minor components in abundance, but their contribution to biomass was not negligible. HC also were comprised of oligotrichs of the genera Strombidium, Strobilidium, and Lohmaniella. They were commonly found in our samples, but no single species dominated. Other species such as Askenasia sp, Uroticha sp and Vorticella sp also were commonly found in our samples. The last species is not truly planktonic but an epibiont on diatom Chaetoceros spp. Tintinnids (TC) were minor components among ciliate community in terms of abundance and biomass, being usually o100 cells l
1 : In spite of their low abundance over three seasons in our study, TC populations were comprised of a great number of species, i.e. 74 species of 27 genera for intact loricae and 59 species of 26 genera for loricae with a cell body inside (Table 2). 3.2. Ciliate distribution 3.2.1. Winter 1993 The vertical distribution of temperature and salinity was homogeneous at every shelf station and in the top 150 m in the Okinawa Trough, but horizontally they decrease from the offshore toward the Changjiang River (11–221C; 33.8–34.8 PSU). The vertical and horizontal distribution of chlorophyll a (chl a) varied over a rather narrow range from 0.34 to 0:73 mg l
1 (see Hama et al.

427

1997). On the other hand, ciliate abundance always peaked within the top 10 m except for PN-1. The population density was high, > 1000 cells l
1 from the shelf edge to the central shelf waters (PN-5, PN-6 and PN-8), but extremely low ðo200 cells l
1 Þ in the inner shelf and the Trough waters. Consequently, there was no significant correlation between chl. a and ciliates (Fig. 2). The average abundance of total ciliates in the water column was calculated from integrated values through the water column, i.e. down to 200 m in the Trough waters and down to nearly the bottom in the shelf waters (Table 3). For this winter period, the average abundance was high at the shelf edge (285–473 cells l
1 ), intermediate in the Trough (123–247 cells l
1 ), and lowest in the inner shelf waters (53–79 cells l
1 ). HC were the most abundant component of the ciliate community, comprising 28–78% of total number of ciliates (Fig. 5A). Although MC was abundant in the top 10 m in central shelf waters, its maximum abundance (ca. 1000 cells l
1 at 10 m at PN-8) was ca. 50% of that in the other two seasons. Their contribution to the total abundance (12–49%) was generally lower than that of HC (Fig. 5A). AC, or Mesodinium rubrum, was widely distributed along the PN line. It was abundant in the central shelf waters with a maximum of 700 cells l
1 at the surface at PN-6, but it was low in the Trough. Although when abundant, its contribution was nearly 50% of the total number of ciliates at a particular depth, integrated over the water column its contribution was low. TC in the central to inner shelf waters were the agglutinated forms, such as Stenosemella nivalis, S. ventricosa and Tintinnopsis gracilis. S. nivalis also occurred in the subsurface layer at PN-4, located beyond the shelf waters. On the other hand, some warm oceanic species such as Acanthostomella conicoides and Dictyocysta elegans were restricted to the Trough and hardly occurred in the shelf waters. Species of the genera Eutintinnus and Salpingella were relatively widely distributed from the Trough to the shelf edge. 3.2.2. Summer 1994 The water column was strongly stratified in the summer with the pycnocline coinciding with the

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428

Table 2 List of tintinnid ciliates found in the East China Sea in winter (W), summer (S) and autumn (A) with their mean cell size in length (L) and width (W) n

Species

L,

W

ðmmÞ Acanthostomella conicoides A. minutissima Amphorellopsis acuta Amphorides minor A. quadrilineata Ascampbelliella armilla A. urceolata Climacocylis sipho Codonella galea C. brevicaudata C. ostenfeldi C. schabi Dadayiella ganymedes Dictyocysta extensa D. duplex D. elegans lepida D. elegans speciosa D. fundlandica D. polygonata Epiplocyloides acuta E. ralumensis E. reticulata Eutintinnus apertus E. fraknoii E. haslae E. lususundae E. pacificus E. stramentus E. tublosus Leprotintinnus simplex

WO WO WO WO WO WO WO N N N N WO WO WO WO WO WO WO WO WO WO WO WO

WO N

7 12 3 13 13 52 9 1 1 1 2 3 23 2 2 5 9 1 1 2 5 1 9 9 3 12 2 15 2 123

27, 26, 151, 89, 113, 27, 33, 275, 75, 235, 106, 78, 87, 48, 56, 57, 50, 53, 57, 73, 65, 65, 62, 186, 48, 221, 75, 139, 143, 82,

20 22 41 38 44 21 34 50 52 48 34 30 27 31 35 39 34 43 40 50 52 49 28 33 30 47 26 26 30 24

Season W

S

þ

þ þ

þ þ

þ þ þ þ þ

þ þ þ þ

þ þ þ þ þ

þ þ þ þ þ þ þ

þ þ

þ þ þ þ þ þ þ þ

þ þ þ þ

L,

W

ðmmÞ

A

þ

þ

n

Species

Ormosella trachelium Parundella longa Protorhabdonella curta P. simplex Rhabdonella cornucopia R. elegans R. exilis R. poculum R. spirails Salpingella acuminata S. curta S. decurtata S. laminata S. subconica Steenstrupiella gracilis S. steenstrupii Stenosemella avellana S. nivalis S. steini S. ventricosa Tintinnidium spp. Tintinnopsis angusta T. beroidea T. gracilis T. radix Undella ostenfeldi Xystonella clavata Xystonellopsis cymatica X. favata

WO WO WO WO WO WO WO WO WO WO WO WO WO WO WO N N N N N N N N WO WO WO

3 1 29 5 3 5 3 4 1 3 13 8 2 5 1 12 3 8 1 5 1 1 6 11 6 2 2 1 1

50, 157, 41, 50, 116, 123, 61, 83, 400, 255, 73, 112, 65, 122, 85, 103, 33, 35, 70, 51, 300, 55, 35, 120, 229, 48, 385, 213, 208,

Season W

29 30 25 31 48 45 29 47 58 32 15 14 18 18 33 34 26 28 33 47 35 23 23 38 39 24 63 50 50

S þ þ þ þ

þ

þ þ þ þ

þ þ þ

þ þ þ þ þ þ þ þ

þ þ þ þ

A

þ þ þ

þ þ þ þ

þ

þ þ þ þ þ þ

þ

þ: occurrence of intact lorica with organism, WO: warm oceanic species, N: neritic species (see also Fig. 7).

nutricline which was usually formed within the euphotic zone over the entire area. The surface temperature was high (26.9–29:41C) over vast areas (PN-1 to PN-10), but lower at the northernmost station (PN-12) where the salinity was also low (o32:0 PSU). A distinct subsurface chlorophyll maximum (SCM) developed, especially in the inner shelf waters (9:39 mg l
1 at PN-12), which corresponded to the upper limit of the nutricline (see Hama et al., 1997). Density peaks of total ciliates also corresponded to the SCM, and were usually > 1000 cells l
1 in the shelf waters, and 700–900 cells l
1 in the Trough (Fig. 3). The highest density was observed

at 10 m at PN-12 (ca. 3000 cells l
1 ). The average abundance in the water column tended to increase from 191 to 1594 cells l
1 along the transect from the Trough to the inner shelf. MC were very abundant in the upper water column in the inner shelf waters and the highest value > 2000 cells l
1 ; was observed at 10 m at PN12. While its contribution was 72% of the total number of ciliates at this depth, the average contribution of MC through the water column ranged from 17% to 47% over the entire area (Fig. 5B). HC were also abundant. However, the depth of their maximum abundance was usually different from that of MC. Of the HC,

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429

Fig. 2. Vertical profiles of total number of ciliates, chlorophyll a and sigma-t at stations on line PN in winter 1993.

Table 3 Pearson’s correlation coefficients ðrÞ of standing crops four trophic groups of ciliates to chlorophyll a for pooled data obtained at every depth at every station on each cruise Season

Abundance vs. chlorophyll a AC

MC

HC nn

Biomass vs. chlorophyll a TC

Total n

AC

MC

HC nn

TC nn

Total n

0.48nn 119

Winter 1993

0.12 n ¼ 44

0.27 107

0.05 119

0.06 62

0.21 119

0.11 n ¼ 44

0.33 107

Summer 1994

0.00 n¼3

0.81nn 46

0.41nn 54

0.43n 45

0.72nn 54

0.00 n¼4

0.90nn 45

0.43nn 51

0.90nn 44

0.42nn 51

Autumn 1993

0.59 n¼6

0.86nn 44

0.79nn 55

0.25 22

0.81nn 59

0.60 n¼6

0.84nn 44

0.63nn 55

0.16 22

0.85nn 59

n

0.47 119

0.22 62

P % 0:05; P % 0:01: n ¼ number of data sets (sampling depths  stations) AC ¼ autotrophic ciliates; MC ¼ mixotrophic ciliates; HC ¼ heterotrophic ciliates; TC ¼ tintinnid ciliates; TOTAL ¼ total ciliates. nn

430

T. Ota, A. Taniguchi / Deep-Sea Research II 50 (2003) 423–442

Fig. 3. Vertical profiles of total number of ciliates, chlorophyll a and sigma-t at stations on line PN in summer 1994.

the small-sized Askenasia sp was the most abundant component in number, accounting for 11– 20% of the total ciliates. AC rarely occurred along line PN during the summer season. Abundance as well as species diversity of TC was highest in the summer. A maximum of 160 cells l
1 of TC was recorded at 35 m at PN-12. The genera Stenosemella and Tintinnopsis were important components in the central to inner shelf waters. In contrast to winter, warm oceanic genera Acanthostomella and Ascampbelliella were widely distributed from the Trough to the inner shelf waters. Other oceanic species such as Dadayiella ganymedes and Protorhabdonella curta were also important components of the TC community in the upper water column on the shelf. 3.2.3. Autumn Cruise 1993 The surface temperature was high in the Trough waters ð27:41CÞ and decreased toward the inner

shelf ð21:71CÞ: Vertical stratification of the water column became more intense than in summer, and the surface mixed layer tended to be shallow toward the shelf waters. In the shelf waters, ciliates accumulated to 600 to 1200 cells l
1 in the upper water column above the developed pycnocline (Fig. 4), which made up 74–89% of total integrated populations in the entire water column. Below the pycnocline, their abundance rapidly decreased to o50 cells l
1 : At PN-12 in the innermost shelf waters, the maximum abundance of 4180 cells l
1 was observed at the surface. In the Trough waters, however, ciliate abundance was lower than 250 cells l
1 throughout the water column. The average value over entire water column tended to increase from the Trough ð40 cells l
1 Þ to the inner shelf waters ð945 cells l
1 Þ: AC was most abundant in the top 5 m at PN-12 ð> 1500 cells l
1 Þ and comprised ca. 50% of the

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431

Fig. 4. Vertical profiles of total number of ciliates, chlorophyll a and sigma-t at stations on line PN in autumn 1993.

total number of ciliates at this depth, although could not be found at the other stations. Their contribution to the total number of ciliates throughout the water column at PN-12 was 40% (Fig. 5C). MC exceeded 2000 cells l
1 at 1 m at PN-12 but were rarely found below the pycnocline. Their contribution to the total integrated number of ciliates ranged from 27% to 56% over the entire area (Fig. 5C). Abundance and species diversity of TC were extremely low throughout the area. Warm oceanic species were widely distributed from the Trough to the inner shelf in summer, while agglutinated species were restricted in deeper waters in the inner shelf waters. 3.3. Relationships with chlorophyll The Pearson’s correlation was tested between standing crops in abundance and biomass of AC, MC, HC, TC and TOTAL (total ciliates) and standing crops of chl a at individual depths at individual stations on three different cruises

(Table 3). Five significantly positive correlations ðPp0:01; rX0:7Þ were detected on abundance basis: the abundances of MC and TOTAL were correlated with chl a in summer and those of MC, HC and TOTAL with chl a in the autumn. Six significantly positive correlations ðPp0:01; rX0:7Þ on biomass basis: biomasses of MC and TC with chl a in summer and those of MC, HC and TOTAL with chl a in autumn.

3.4. Standing crop Integrated water column biomass at each station in three seasons is shown in Table 4. In winter, the greatest biomass of total ciliates was found in the central shelf waters (56.1–89:8 mg C m
2 ), followed by the Trough (42.9–51:0 mg C m
2 ) and the inner shelf waters (8.5–21:5 mg C m
2 ). The biomass in summer tended to increase from the Trough (39.3–41:5 mg C m
2 ) toward the inner shelf waters (56.1–136:3 mg C m
2 ) and from the

432

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Fig. 5. Percentage composition in terms of abundance (A, B and C) and biomass (D, E and F) of four trophic groups of ciliate populations observed in the East China Sea in winter 1993 (A, D), summer 1994 (B, E) and autumn 1993 (C, F). AC ¼ autotrophic ciliates; MC ¼ mixotrophic ciliates; HC ¼ heterotrophic ciliates; TC ¼ tintinnid ciliates.

Trough (12.2–14:6 mg C m
2 ) to the inner shelf waters (30.2–50:1 mg C m
2 ) in autumn. As a whole, despite the decrease in integrated depth, the ciliate standing crop increased from the Trough to the inner shelf waters in every season, except for a low value in the innermost shelf waters in winter. Seasonal variability in biomass was great (6.4–16-fold) in the inner shelf waters, and it tended to decrease from summer to winter. Biomass variability in the central shelf and Trough waters was small (2.1–3.3 and 3.5–4.2-fold, respectively). Biomass contributions of MC were generally large under vertically stratified conditions, and contributed 21–75% in summer and 20–65% in autumn, to the total ciliate biomass, respectively. Biomass contributions of HC was high in winter (47–87%), except for PN-10 where TC contributed 70% (Fig. 5D–F).

4. Discussion In this study we used the formaldehyde-based fixative. This fixative has an advantage of distinguishing trophic modes of ciliates and of avoiding shrinking of cell size, although known to destroy many ciliate cells (Gifford, 1985; Stoecker et al., 1989; Stoecker et al., 1994). According to Stoecker

et al. (1994), biomass estimated here may have been underestimated by as much as 10–40%. Furthermore, certain species are more sensitive than others to this fixative (Jerome et al., 1993; Stoecker et al., 1994; Ota, unpubl. data). This situation creates another bias in ciliate community structure. Nevertheless, we show the uncorrected data because there are no reliable correcting factors for these underestimation and bias at present. The value reported here for ciliate biomass and then grazing and nutrient regeneration rates which were calculated from the biomass data, therefore, must be minimal estimations. 4.1. Ciliate communities This is the first report of quantitative and qualitative data on planktonic ciliates from the East China Sea. Since we counted empty loricae of tintinnids as live individuals when they were intact, possible underestimation caused by fixation was not the case for tintinnids. While this may lead to potential overestimation of relative abundance of the tintinnids compared to naked forms, tintinnid abundance hardly exceeded 10% of total community in both number and biomass, except at a few winter stations in the inner shelf waters where primary productivity and ciliate abundance were

T. Ota, A. Taniguchi / Deep-Sea Research II 50 (2003) 423–442

433

Table 4 Integrated abundance and biomass of four trophic groups of ciliates and their total abundance and biomass in the column of the East China Sea Station

Integrated depth (m)

Abundance ð106 cells m
2 Þ

Biomass ðmg C m
2 Þ

AC

MC

HC

TC

Total

AC

0-200 0-200 0-200 0-200 0-125 0-100 0-90 0-80 0-60 0-40 0-50 0-45

0.2 0.1 0.0 0.3 10.9 12.7 0.5 2.6 2.1 0.1 0.1 1.5

14.9 9.2 5.0 6.5 9.6 5.5 6.6 18.3 5.3 0.4 1.5 0.4

32.4 19.9 16.6 28.9 17.4 28.5 17.9 14.5 3.0 0.8 1.4 1.3

1.6 3.8 2.9 1.4 0.6 0.1 0.4 — 0.5 0.7 0.6 0.2

49.1 33.1 24.5 37.2 38.4 46.8 25.4 35.4 10.8 2.1 3.6 3.5

0.1 0.1 0.0 0.2 10.5 8.7 0.2 2.3 1.3 0.0 0.1 1.1

Summer 1994 PN1 0-200 PN3 0-200 PN5 0-120 PN8 0-80 PN10 0-45 PN12 0-40

0.5 — — — 0.1 0.4

6.5 10.4 24.5 9.9 19.8 29.1

29.1 22.9 27.4 37.4 20.8 29.3

2.8 4.8 2.4 4.7 3.2 3.4

38.9 38.0 54.3 52.0 43.9 62.2

Autumn 1993 PN1 0-200 PN3 0-200 PN5 0-120 PN8 0-80 PN10 0-45 PN12 0-42

— — — — — 15.4

5.4 4.3 5.2 20.1 9.5 14.7

4.6 3.6 12.4 9.6 7.2 8.2

1.4 — 1.6 0.2 0.2 0.4

11.4 7.9 19.2 29.9 16.9 38.8

Winter 1993 PN1 PN2 PN3 PN4 PN5 PN6 PN7 PN8 PN9 PN10 PN11 PN12

MC

HC

TC

Total

12.6 13.9 5.5 6.8 16.8 8.2 5.9 25.4 5.6 1.3 3.1 0.6

36.3 31.7 32.7 34.6 34.1 41.6 48.8 62.1 13.7 1.3 6.5 5.9

1.9 5.2 5.9 1.4 0.6 0.0 1.1 — 0.8 6.1 4.3 0.8

51.0 50.9 44.1 42.9 61.9 58.4 56.1 89.8 21.5 8.7 14.0 8.5

0.3 — — — 0.0 0.1

8.6 14.1 25.3 10.9 32.8 102.9

28.2 24.5 25.2 31.1 23.1 32.8

4.4 0.7 0.3 0.7 0.1 0.6

41.5 39.3 50.7 42.7 56.1 136.3

— — — — — 8.8

3.9 8.4 3.7 30.2 16.5 17.2

6.9 6.2 12.4 16.4 13.3 23.6

1.5 — 2.5 0.2 0.4 0.4

12.2 14.6 18.7 46.8 30.2 50.1

—- not found. AC ¼ autotrophic ciliates; MC ¼ mixotrophic ciliates; HC ¼ heterotrophic ciliates; TC ¼ tintinnid ciliates.

extremely low (Fig. 5). Therefore, possible overestimation of tintinnids seems not to modify largely the structure of the ciliate community. MC were usually dominant in stratified periods, both summer and autumn, and less dominant in winter in the East China Sea. MC have been reported from neritic to oceanic areas of the boreal to tropical oceans (i.e. Stoecker et al., 1987, 1989; Laval-Peuto and Rassoulzadegan, 1988; Putt, 1990; Bernard and Rassoulzadegan, 1994; Sanders, 1995; Suzuki et al., 1998). While variability was observed, these results indicate that MC are relatively important under oligotrophic conditions associated with higher temperatures and higher

light intensities, and relatively unimportant in eutrophic winter and/or conditions. These seasonal changes of relative contribution of MC agree with our results. Furthermore, the relation between absolute biomass and relative contribution of MC (Fig. 6) may indicate that mixotrophy is more important in particular marine systems in such coastal/shelf waters rather than oceanic/ Trough waters. Recently it has been shown that the maximum photosynthetic rate of MC is comparable to that of other phytoplankters (Stoecker et al., 1988, 1991). MC are important not only among ciliate populations, but also among primary producers in

434

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Fig. 6. Relationships between relative biomass contribution of mixotrophic ciliates (MC) to total ciliate biomass and absolute biomass of MC in the shelf and basin waters of the East China Sea in winter 1993, summer 1994 and autumn 1993.

the microplankton ðX20 mmÞ size class (Stoecker et al., 1989). In the Nordic Seas (Iceland, Greenland and Barents Seas), chl a of the MC contributed up to 24% of the total chl a when the latter was as low as 0:2 mg l
1 : To evaluate the contribution of chl a from MC in the East China Sea, literature-based values on their cellular chl a content were multiplied by the observed abundance. Based on this calculation, the amount of chl a attributable to ciliates in the East China Sea was generally low, ranging from 1.2% to 4.1% of the entire water column. However, it was as high as 22% in the upper mixed layer above the pycnocline where MC were dominant. This indicates that MC sometimes contribute significantly to total chl a under oligotrophic conditions as previously demonstrated. Mesodinium rubrum, an AC, occasionally forms non-toxic red tide blooms in neritic waters (McAlice, 1968) and upwelling areas (see Taylor et al., 1971), although it occurs more regularly at lower densities in temperate to subtropical offshore waters. AC abundance reached 1670 cells l
1 in the East China Sea, which is comparable to those values in temperate to subtropical waters.

However, their chl a was only o1:4% of the total chl a: TC in this area comprised smaller fractions of the total ciliate abundance, consistent with previous reports from other areas. However, interesting differences in their distribution were observed. It has been said that particular species of tintinnid ciliates can be a useful indicator of particular water masses (Hada, 1957; Zeitzschel, 1990; Kato and Taniguchi, 1993). Neritic genera of Tintinnopsis and Stenosemella, which were found throughout the water column in the central to inner shelf waters in the winter, tended to be restricted to waters below the pycnocline in the inner shelf waters in summer and autumn (Fig. 7A). On the other hand, warm oceanic species which were found only in the Trough waters in winter were also widely distributed, although less abundant in the surface layer in the shelf waters above the pycnocline in summer and autumn (Fig. 7B, C). These seasonal changes in distribution suggest a separation of ecosystems between the upper and lower water columns when intensified vertical stratification occurs.

T. Ota, A. Taniguchi / Deep-Sea Research II 50 (2003) 423–442

Fig. 7. Distribution of tintinnid indicator species in the East China Sea in winter 1993 (A), summer 1994 (B) and autumn 1993 (C). Open and filled circles denote respectively warm oceanic species and neritic species. Solid lines are contour of sigma-t:

4.2. Ciliate distribution The vertical distribution of ciliates was comparatively deeper in winter, whereas the bulk of ciliates was in the upper mixed layer in summer and autumn (Figs. 2–4). Although this is consistent with most previous reports (Beers and Stewart, 1969; Revelante and Gilmartin, 1983;

435

Taniguchi, 1984; Middlebrook et al., 1987), there is no clear explanation of the persistence of such a concentrated distribution in the upper layer (Jonsson, 1989; Fenchel et al., 1990; Dolan and Coats, 1991). Fenchel et al. (1990) and Dolan and Coats (1991) have suggested that oxygen concentration plays a direct role in the vertical distribution of planktonic oligotrichs, which is restricted to a well-oxygenated layer of the water column. Jonsson (1989) reported that planktonic oligotrichs have negative geotaxis and swim upwards in stratified water, and as a result they concentrate in the upper layer. In the stratified water columns in summer and autumn in the East China Sea, oligotrichs were abundant in the upper mixed layer, but occurred in extremely low numbers below the pycnocline where the dissolved oxygen concentration was low (1.2–3:6 ml l
1 ). However, some oligotrichs also were distributed in the underlying layer, indicating that the vertical distribution of the ciliates was determined not only by zonation of dissolved oxygen concentration and physical factors that affect ciliate motility, but also by other factors affecting ciliate growth and/or mortality. One of the possible factors is the vertical distribution of chl a; because the vertical profile of ciliate abundance was generally the same as that of chl a; showing positive correlations in abundance and biomass (Table 3). During stratified periods, the nitrate concentration above the pycnocline was nearly undetectable at most stations (Watanabe et al., 1995). Under such oligotrophic conditions, small-sized phytoplankters usually predominate (Sieburth et al., 1978). In this study, oligotrich ciliates o30 mm ESD, which may consume small particles o10 mm (cf. Jonsson, 1987; Rassoulzadegan et al., 1988), comprised a substantial portion of the total assemblage. These observations suggest that most ciliates in summer and autumn are closely linked to the small-sized phytoplankters dominating in the upper layer. If this is the case, higher temperatures in the upper layer also may enhance the ciliate growth rate there. A slight difference in such environmental factors may selectively enhance the growth of a particular species of ciliates and result in a concentrated distribution of a particular species.

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T. Ota, A. Taniguchi / Deep-Sea Research II 50 (2003) 423–442

In fact, one or a few species of mixotrophic ciliates usually dominated at the depths where total ciliates were abundant. 4.3. Ciliate standing crop The standing crop of ciliates varied with depth and season from o10 to 4180 cells l
1 in abundance and from o0:01 to 6:25 mg C l
1 in biomass. In the Trough waters, seasonal changes in abundance and vertical distribution pattern of ciliates were small compared to those in the shelf water. The average abundance of total ciliates in the Trough waters ranged from 40 to 250 cells l
1 and were similar to those recorded from tropical and subtropical oligotrophic systems. For example, values of 120–720 cells l
1 for ciliates other than tintinnids were reported from the eastern subtropical Pacific by the formalin-fixation method of Beers and Stewart (1969, 1971), and 110–150 cells l
1 for total ciliates from the western subtropical Pacific in autumn by the same method (Suzuki et al., 1998). The biomass of the ciliates ranged from 0.06 to 0:26 mg C l
1 in the Trough waters of the East China Sea, and was comparable to the reported values of 0.06–0:35 mg C l
1 by the same method from the eastern subtropical Pacific (Beers and Stewart, 1971), 0.01–0:52 mg C l
1 by direct counting method from the central tropical Indian Ocean (Sorokin et al., 1985) and 0.1– 1:2 mg C l
1 by Lugol’s fixation method from the northwestern Indian Ocean (Leakey et al., 1996). The abundance of total ciliates in the shelf waters showed marked spatial and temporal variations compared to the Trough waters. The cyclic variation in abundance of ciliates with seasons is commonly observed in neritic waters from tropical to temperate areas (Verity, 1987; Gilron et al., 1991; Lynn et al., 1991; Bernard and Rassoulzadegan, 1994). Unfortunately, we have no data during the phytoplankton spring bloom. However, the results observed in three different seasons indicate a possible seasonal cycle, whose magnitude tends to be greater from the central shelf toward the inner shelf waters. In the latter waters, the discharge from the Changjiang should

greatly affect the turbidity and the vertical stability of the water column, which in turn affect primary productivity. As a result, the seasonal difference of ciliate abundance at PN-12 in this water was as large as 17.8-fold compared to 1.7–2.8-fold for the central shelf waters. Apart from the areal difference in seasonal variability, the annual ranges of abundance and biomass of total ciliates over the shelf were 50–160 cells l
1 and 0.16–3:50 mg C l
1 ; respectively. Generally, these values fall within the reported values from tropical and subtropical oligotrophic waters, while the latters were obtained by different authors by different methods, i.e. by Lugol’s fixation method by Revelante and Gilmartin (1983) and by glutaraldehyde method by Rassoulzadegan et al. (1988) in the Mediterranean Sea, and by quantitative protargol staining method by Lynn et al. (1991) in the Caribbean Sea. The winter minimum recorded in the inner shelf water, however, was smaller than the minimum reported value. Primary productivity was also surprisingly low (Hama et al., 1997), probably due to increased turbidity of the water as a result of the riverine input and vertical mixing in winter (Ning et al., 1988). The phytoplankton community was actually dominated by a benthic diatom Pararia sulcata with thick frustules (Furuya et al., 1996), indicating vertical mixing of the water column. Such diatoms might be not available for planktonic ciliates. 4.4. Grazing impact and contribution to nutrient regeneration The calculated daily production of the ciliate populations in the water column ðmg C m
2 d
1 Þ ranged from 4.8 to 115:9 mg C m
2 d
1 ; from 86.2 to 436:0 mg C m
2 d
1 ; and from 33.4 to 98:4 mg C m
2 d
1 over the entire area in winter, summer and autumn, respectively (Fig. 8). In winter, the production was the highest in the Trough waters, reflecting the highest temperature (21–221C), but extremely low in the inner shelf waters where temperatures were low (101C at PN12). On the other hand, the production in summer and autumn, when the areal difference in temperature was small, tended to be high toward the

T. Ota, A. Taniguchi / Deep-Sea Research II 50 (2003) 423–442

Fig. 8. Calculated production of total ciliate populations in the East China Sea in winter 1993 (A), summer 1994 (B) and autumn 1993 (C).

inner shelf waters where the integrated biomass through the water column was high, compared to the Trough waters. The potential ingestion rate of ciliates was computed from the above-mentioned productivity

437

by assuming that mean gross growth efficiency is 50% for ciliates (Verity, 1991 and also cf. Taniguchi and Kawakami, 1985). Then, their grazing impact was estimated by referring to the primary production determined on the same cruises (Hama et al., 1997). In the latter case, the grazing impact was calculated for the euphotic zone (Table 5). Their impact on the primary production was 16–59% in winter, 31–86% in summer and 14–36% in autumn throughout the Trough and central shelf waters, while their impact was only 3% in the inner shelf waters in winter (Table 5). Another important role of ciliates is as nutrient regenerators in the epipelagic zone. It now seems clear that most of the nitrogen excreted by ciliates is released as NHþ 4 (Caron and Goldman, 1990). NHþ 4 excretion rates of ciliates can roughly be estimated from their growth rate by the reported relationships between excretion and growth rates. If we assume that the carbon to nitrogen ratio of ciliates is 4.4 and the specific excretion rate (E; h
1 ) is a function of growth rate (G; h
1 ), i.e., E ¼ 3:91 G1:42 (Verity, 1985), nitrogen excretion was calculated to be 0.1– 63:8 mg N m
2 d
1 (see Table 6). This amount is equivalent to 0.1–93.8% of nitrogen requirement by primary producers when the uptake ratio of carbon and nitrogen is 106:16 (see Fig. 9). In this study, we employed some crude assumptions, such as weight/volume ratio of the ciliate cells and C/N ratio of excreta, along with the reported growth and excretion equations as well as uncorrected biomass data observed, which are only available figures at present time. Therefore, we must interpret these values with great caution. However, it is most likely that these values are of conservative estimates of the role of the ciliates in the East China Sea. If so, ciliate populations in the East China Sea may control the primary producers through intensive grazing and also act as important nutrient regenerators. Grazing is more significant in vertically stratified waters in summer and autumn and less significant in winter. In the innermost shelf waters in winter where vertical mixing and input of riverine water are extensive, ciliates are of little importance.

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438

Table 5 Calculated ciliate production ðPc Þ and ingestion ðIÞ through the euphotic zone in relation to primary production ðPp Þ cited from Hama et al. (1997) Station

Euphotic zone (m)

Pp ðmg C m
2 d
1 Þ

Pc ðmg C m
2 d
1 Þ

Pc =Pp (%)

I ðmg C m
2 d
1 Þ

I=Pp (%)

Winter 1993 SST2 80 PN5 80 PN8 45 PN12 7

270 220 570 68

45.5 64.8 46.7 0.9

16.8 29.4 8.2 1.3

90.9 129.6 93.3 1.7

33.7 58.9 16.4 2.6

Summer 1994 PN3 97 PN5 80 PN8 62 PN10 44 PN12 18

350 300 710 710 1500

80.9 128.9 111.6 125.7 352.0

23.1 43.0 15.7 17.7 23.5

161.7 257.8 223.2 251.3 704.0

46.2 85.9 31.4 35.4 46.9

Autumn 1993 PN1 70 PN3 70 PN5 65 PN8 32 PN10 30 PN12 23

290 220 510 1100 320 1000

25.1 15.4 43.6 88.3 57.3 69.8

8.7 7.0 8.6 8.0 17.9 7.0

50.2 30.9 87.2 176.6 114.6 139.5

17.3 14.0 17.1 16.1 35.8 14.0

Table 6 Calculated nitrogen excretion by ciliates ðNec Þ and daily nitrogen requirement by primary producers ðNpp Þ through the euphotic zone Station

Euphotic zone (m)

Npp ðmg N m
2 d
1 Þ

Nec ðmg N m
2 d
1 Þ

Nec =Npp (%)

Winter 1993 SST2 PN5 PN8 PN12

80 80 45 7

47.5 38.7 100.4 12.0

7.8 11.7 1.4 0.1

16.4 30.1 1.4 1.0

Summer 1994 PN3 PN5 PN8 PN10 PN12

97 80 62 44 18

61.6 52.8 125.0 125.0 264.2

27.6 49.6 42.9 45.8 63.8

44.7 93.8 34.3 36.6 24.2

Autumn 1993 PN1 PN3 PN5 PN8 PN10 PN12

70 70 65 32 30 23

51.1 38.7 89.8 193.7 56.4 150.9

9.3 5.7 15.9 29.3 18.3 21.3

18.2 14.7 17.7 15.1 32.4 14.1

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439

Fig. 9. Relationship between calculated daily nitrogen excretion by ciliates ðNec Þ and daily nitrogen requirement by primary producers ðNpp Þ in the East China Sea. Both variables were standardized by stocks of nitrogenous nutrients ðNO2 þ NO3 þ NHþ 4 Þ ðNstocks Þ and grouped by depth and season. Winter ¼ 1993; summer ¼ 1994; autumn ¼ 1993; M ¼ surface mixed-layer samples; U ¼ samples below the pycnocline.

Acknowledgements We are grateful to the following colleagues for collaboration in sampling on three cruises: A. Murase, Hiroshima University, T. Oshima, Tohoku University and other research staff as well as the crew of the R.V. Kaiyo. We also thank Dr. P.J. Harrison for his critical reading and correcting of our English manuscript. This work was partially supported by the grants ‘‘MASFLEX’’ of the Science and Technology Agency of Japan and ‘‘Ocean-Flux’’ of the Ministry of Education, Science and Culture, Japan.

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