Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf

MARSYS-02623; No of Pages 14 Journal of Marine Systems xxx (2014) xxx–xxx

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Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf Cuixia Zhang a,b, Wuchang Zhang b,⁎, Xiaobo Ni c, Yuan Zhao b, Lingfeng Huang d, Tian Xiao b a

Tianjin Key Laboratory of Marine Resource and Chemistry, College of Marine Science and Engineering, Tianjin University of Science and Technology, Tianjin 300457, PR China Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, PR China State Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography, State Oceanic Administration, Hangzhou, 310012, PR China d Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems (Xiamen University), Xiamen, 361102, PR China b c

a r t i c l e

i n f o

Article history: Received 31 August 2013 Received in revised form 8 September 2014 Accepted 9 September 2014 Available online xxxx Keywords: Ciliate Changjiang river estuary Kuroshio water East China Sea

a b s t r a c t In summer 2006 and winter 2007, ciliate abundance and biomass were investigated in the East China Sea in connection with water masses, frontal zones, dissolved oxygen and chlorophyll a concentrations, and picoplankton and nanoflagellate abundances. In addition, tintinnid ciliates were identified to species based on lorica morphology. There was no significant difference of ciliate abundance and biomass between Changjiang diluted water (CDW) and shelf mixing water (SMW) in the Changjiang river estuary and its adjacent sea in summer, or among the coastal water (CoW), the SMW and the Kuroshio water (KW) on the shelf in winter. The influence of water masses on ciliate distribution was slight, except that distinct increases in ciliate abundance were observed in the vicinity of frontal structures. Most tintinnids were neritic species, with no discrimination between two water masses in the Changjiang river estuary. However, cosmopolitan and warm water species were very mainly restricted to SMW and KW; neritic species were essentially present in CoW and SMW on the continental shelf. Total ciliate biomass was closely correlated with picoplankton biomass in the CDW and KW. Picoeukaryotes and Synechococcus were the potential food source of ciliates. In winter, within KW, nanoflagellates would play a major role in the transfer of organic matter from picoplankton to ciliates in the microbial community within KW. In the low-oxygen and hypoxia area adjacent to the Changjiang estuary where relatively high ciliate abundance and biomass occurred, heterotrophic bacteria would appear to exhibit a potential prey effect on the distribution of bacterivorous aloricated ciliates and nanoflagellates acting as intermediates between bacteria and tintinnids. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Planktonic ciliates are one of the most important components of protists in the microbial web where they are major consumers of nano- and picoplankton (Azam et al., 1983). Thus, they are efficiently transferring matter and energy from the primary production level to higher trophic levels. Most planktonic ciliates were oligotrich ciliates, which divided into two groups, tintinnids (loricate ciliates) and oligotrichs (aloricate ciliate). Tintinnids are the best known group of marine ciliates and recognized as indicator species of different water masses due to their hard loricae (Kato and Taniguchi, 1993). In the East China Sea, planktonic ciliates accounted for about 90% of the total protozoan abundance (Chen et al., 2003) and contributed greatly to nutrient regeneration to sustain primary productivity (Ota and Taniguchi, 2003). Plankton distribution is patchy by nature (Haury et al., 1978). Considering spatial scale, patches could be divided into meso (km), fine (m) and micro (cm) scales. A variety of physical and biological processes ⁎ Corresponding author. E-mail address: [email protected] (W. Zhang).

work together to shape the patchiness. At the mesoscale (100 km), physical processes are particularly powerful and, therefore, have a strong influence on plankton variability (Mann and Lazier, 1991). As for other planktons, the distribution of ciliates is patchy at different scales (Montagnes et al., 1999). Due to the limited motility of ciliates, their assemblage distribution and patch size are more influenced by physical factors such as currents and freshwater intrusion than that of the larger and motile zooplankton (Reid and Stewart, 1989). Planktonic ciliates are found in a variety of habitats with marked differences in physical and chemical water-mass features. Ciliate distribution and species varied with water masses and frontal regions in the Southern Ocean (Safi et al., 2007), from the shelf-slope to oceanic waters in the southern Atlantic near Argentina (Santoferrara and Alder, 2009) and between the subtropical gyre and neighboring waters in north-eastern Atlantic Ocean (Quevedo et al., 2003). Continental shelf areas are usually under the influence of both fresh water outflow and oceanic water intrusion. However, the influence of such water masses on the spatial pattern of planktonic ciliates is poorly documented. The East China Sea (ECS), located on the western edge of North Pacific Ocean, is a marginal sea with one of the most extensive continental

http://dx.doi.org/10.1016/j.jmarsys.2014.09.003 0924-7963/© 2014 Elsevier B.V. All rights reserved.

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

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C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

shelves in the world. Among the complex dynamic interactions of several water systems, the nutrient-enriched freshwater of the Changjiang River outflow in the west and the oligotrophic Kuroshio water coming from the equatorial Pacific in the east are two dominant physical factors driving the temporal or spatial variations of phytoplankton biomass, primary production, copepod abundance and assemblage (Gong et al., 1997; Kim et al., 2009; Zuo et al., 2006). In summer, when the maximum Changjiang River flow is maximum, its plume spreads eastwards over the broad ECS. The summer fresh outflow with rich terrestrial inorganic or organic nutrients is known to significantly impact the microbial ecosystem and nanoflagellate community (Jiao et al., 2007; Tsai et al., 2010). In the ECS, summer peaks in ciliate abundance and standing stock were driven by an increased availability of organic carbon utilized by bacteria. Therefore, the input of terrestrial material (i.e., particulate and dissolved organic carbon) through the Changjiang River outflow played an important role in supporting the microbial food web in the shelf water (Chiang et al., 2003; Shiah et al., 2000). In winter, the broad shelf region was characterized by high salinity water resulting from the shelf-ward intrusion of Kuroshio water north of Taiwan, which affected the nutrient budget over the shelf area (Zhang et al., 2007). The Kuroshio water has the lowest primary production with weak seasonal variation in contrast to the upwelling area at the shelf break northeast of Taiwan and Changjiang River mouth (Gong et al., 2000, 2003). Given the marked influence of fresh water outflow in summer and oceanic water in winter on the ECS hydrology features, the impact of both water masses on ciliate distribution remains a matter of concern. Close to the coastline, the encounter of low-salinity water from the Changjiang River outflow with high-salinity water from the sea generates haline fronts. Similarly, in winter, when the warm KW meets the fresher and cold coastal water, a thermohaline front takes place near the continental shelf break (Chen, 2009). Frontal structures are known to enhance phytoplankton development, which should also favor the increase in ciliate abundance. The present study aimed to elucidate the influence of Changjiang River outflow and Kuroshio water (KW) on the ciliate abundance and biomass, on tintinnids species composition. The relationships of ciliate abundance and biomass with environmental factors (e.g., salinity, dissolved oxygen) and picoplankton were also addressed.

2. Materials and methods 2.1. Study area and sampling strategy Two cruises with grid stations were conducted on board R/V Beidou in summer (18 ~ 31 August) 2006 and winter (22 February ~ 11 March) 2007 in the area of the ECS shelf delimited by the coordinates 25–33°N and 121–127°E (Fig. 1). The summer cruise took place in the Changjiang river estuary and its adjacent sea (station depths b100 m) to study the influence of Changjiang River outflow. Seawater samples were collected at all stations to determine dissolved oxygen (DO) and chlorophyll a (Chl a) concentrations and ciliate and picoplankton abundances. Samples were taken at all the stations. The winter cruise was focused on the influence of KW and covered the intermediate part of the continental shelf, extending to the shelf-break area with depth between 100 m and 200 m in the east and close to the Taiwan Strait in the south. Six cross-shelf sections (E1–E6) were investigated and seawater samples were collected at alternate stations (biological stations) to determine Chl a concentration, and ciliate, nanoflagellate and picoplankton concentrations.

2.2. Hydrology and chlorophyll a At every station, vertical profiles of temperature and salinity (from surface down to bottom or 200 m when depth N200 m) were recorded with a Sea-Bird (SEB-25) CTD. At biological stations, seawater samples were collected to determine DO and Chl a concentrations, and ciliate, nanoflagellate and picoplankton abundances at 3 to 7 depths with 5 dm3 Niskin bottles on a rosette equipped with the CTD. Surface sampling was performed at 1 m depth. Immediately after sample collection, DO concentration was determined, both polarographically and using the traditional Winkler titration method (Bryan et al., 1976). For the determination of Chl a concentration, 250 cm3 seawater samples were filtered through Whatman GF/F glass-fiber filters. Chl a was extracted by using 90% aqueous acetone at −20 °C in the dark for 24 h, and its concentration was determined fluorometrically (Parsons et al., 1984) using a Turner Designs fluorometer.

N 34°

33 4 32 31

Section A

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China Zhejiang

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China

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Fujian

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Section E4

Ta

iw a

iw an Ta

122°

2-5

3-1

5-1

120°

1-7

Zhejiang

Fujian

24°

1-5

2-1

124°

126°

128° 120°

122°

124°

126°

E 128°

Fig. 1. Location map of sampling stations. (■) Stations of the summer 2006 cruise in the Changjiang river estuary and its adjacent seas. (●) Physical and biological stations and (○) only physical station of the winter 2007 cruise in the continental shelf of East China Sea The dashed lines indicate bottom depth (m) isolines.

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

3

Fig. 2. Temperature-salinity diagrams for the investigated continental shelf of ECS in summer 2006 and winter 2007. The colour indicates the different salinity. Continuous lines refer to density excess. Dotted lines show limits between different water masses. CDW: Changjiang diluted water; SMW: shelf mixing water; CoW: coastal water; KW: Kuroshio water.

34° N 33°

CDW

CDW 32°

Changjiang R.

Changjiang R.

SMW

31°

SMW

Hangzhou Bay

Hangzhou Bay

30° 29° 28°

T

27°

S

33° Changjiang R.

Changjiang R.

32° 31° Hangzhou Bay

Hangzhou Bay

30° 29° 28°

Chl a 27° 120°

121°

122°

123°

124°

125°

126°

Ciliate abundance 122°

123°

124°

125° E 126°

Fig. 3. Horizontal distribution of surface temperature (T, °C), salinity (S), chlorophyll a concentration (Chl a, μg dm−3) and ciliate abundance (ind. dm−3) in summer 2006 around the Changjiang river estuary. The bold dashed line represents isohaline 32, the boundary between CDW and SMW. CDW: Changjiang diluted water; SMW: shelf mixing water.

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

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C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

32° N 31°

Changjiang R.

Changjiang R.

CoW

h ng z Ha

30°

ou

Ba y

B zhou Ha n g

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ay

29° SMW

28°

SMW

KW

KW

27° 26° 25°

T

Taiwan

32°

Changjiang R.

Changjiang R.

31° Ha

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Taiwan

hou ng z

Bay Han

o gzh

uB

ay

29° 28° 27° 26° 25°

Chl a

Taiwan

24°

120°

122°

124°

126°

Taiwan

120°

122°

Ciliate abundance 124°

126° E

Fig. 4. Horizontal distribution of surface temperature (T, °C), salinity (S), chlorophyll a (Chl a, μg dm−3) and ciliate abundance (ind. dm−3) in winter 2007 on the continental shelf. The dashed isohaline 32 (blue) indicates the boundary of CoW and SMW; the dashed isohaline 34.5 (red) indicates the boundary of SMW and KW. CoW: coastal water; SMW: shelf mixing water; KW: Kuroshio water. (For interpretation of the references to colour in this figure, the reader is referred to the web version of this article.)

2.3. Ciliate analysis For ciliate abundance determination, 1 dm3 seawater samples were fixed with acid Lugol iodine (1% final concentration) in a plastic bottle and then stored cool in the dark until analysis in the laboratory as early as possible. Samples were settled for at least 24 h. The upper layer water was gently siphoned out, and the remaining (~ 100 cm3) was transferred into a smaller bottle. A 20 cm3 subsample was settled in an Utermöhl chamber (Utermöhl, 1958) and enumerated under an inverted microscope (Olympus IX 51) at 100 or 200 × magnification. For tintinnids, both cells (loricae with protoplast) and empty loricae were counted in order to ensure species richness. Tintinnids were identified according to taxonomic references (Kofoid and Campbell, 1929; Nie and Cheng, 1947; Xu, 2007; Xu et al., 2001). The volume of each cell was determined by measuring cell dimensions with an ocular micrometer, assuming appropriate geometric shapes (ellipsoid, cone, cylinder, ball, semi-ellipsoid and their combinations). The carbon content of each cell was then obtained using the carbon to volume conversion factor 0.19 μg C μm−3 for ciliate (Putt and Stoecker, 1989). Total ciliate abundance and biomass were calculated by excluding tintinnids empty loricae. Integrated (0–30 m) ciliate abundance and biomass were calculated according to the trapezoidal method.

flow cytometer (Becton Dickinson) are reported in the companion papers (Zhao et al., 2013). Conversion factors were used to estimate carbon biomass: 115 fg C cell−1 for Synechococcus (Li and Harrison, 2001), 1500 fg C cell−1 for picoeukaryotes (Zubkov et al., 1998) and 20 fg C cell−1 for heterotrophic bacteria (Lee and Fuhrman, 1987). For nanoflagellate abundance determination, 40 to 100 cm3 samples were preserved in glutaraldehyde (1% final concentration), filtered onto 2 μm pore-size black polycarbonate membrane filters and stained with DAPI (5 μg cm−3 final concentration) for 5 min. The black polycarbonate membrane filters were examined in the laboratory under an epifluorescence microscope (Olympus BX51). 2.5. Statistics Total ciliate abundance and biomass of the surface and inventory between 0 and 30 m depth in the different water masses were tested for significance by t test. Potential relationships between ciliate biomass and environmental factors were tested by SPSS 19. p b 0.05 was considered significant in the statistical analyses. 3. Result 3.1. Water masses

2.4. Flow cytometry and microscopy For flow cytometry analysis, 5 cm3 subsamples were fixed onboard with paraformaldehyde (final concentration 1%), kept at room temperature for 10 to 15 min and then freeze trapped in liquid nitrogen. The samples were stored at −80 °C until their analysis in the laboratory. Detailed methods about flow cytometry analysis using a FACSVantage SE

Salinity in the water column was used to distinguish different water masses that were defined according to Gong et al. (1996) and Chen (2009). Because the 31 isohaline was closer to the mouth of the Changjiang River and few sampling stations were in its plume, seawater with salinity ≤32 were called Changjiang diluted water (CDW) in summer and coastal water (CoW) in winter. In the Kuroshio water (KW)

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

9

1200 1000 800 600 400

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Integrated abundance (106 ind. m-2)

1.4

1000

100 80 60 40 20 0

CoW

SMW

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60 50 40 30 20 10 0

CoW

SMW

KW

Fig. 5. Average surface ciliate abundance (ind. dm−3), biomass (μg C dm−3), average integrated (0–30 m) ciliate abundance (106 ind. m−2) and biomass (mg C m−2) in the different water masses in summer 2006 (A) and winter 2007 (B). Numbers in parentheses indicate number of seawater samples. Error bars represent standard deviation (SD). *p b 0.05, t test. CoW: coastal water; CDW: Changjiang diluted water; SMW: shelf mixing water; KW: Kuroshio water.

with the salinity ≥ 34.5, the Kuroshio surface water was dominant due to the sampling depth (ca. 200 m) in contrast to the weak Kuroshio subsurface water. In summer, temperature and salinity in the water column were in the ranges 10.48–30.08 °C and 24.63–34.62, respectively. Salinity 32 was defined as the boundary between CDW and the shelf mixing water (SMW). In addition, the low temperature, about 10 °C in the St. 5 deep water, resulted from the intruding stretch of summertime Yellow Sea Cold Water (Fig. 2). The fresh CDW was confined to the coastal area and separated into northern and southern branches by the tonguelike SMW, which occupied most of the offshore waters outside of the Changjiang River mouth (Fig. 3). The CDW plume met the SMW along an S-shaped line. In winter, temperature and salinity in the water column were in the ranges 9.88–24.58 °C and 25.95–34.79, respectively. Three water masses, the CoW, the KW and the SMW, were identified. CoW belonged to the coastal area with surface salinity ≤32. The KW with high salinity (34.5–34.79) and high temperature (N 20 °C) intruded from the northeast of Taiwan Island largely running in the southwest direction, and SMW occurred between CoW and KW (Figs. 2 and 4). KW intruded the shelf area in an S-shaped line, with the intrusion especially farthest along section E2.

3.2. Chl a and ciliate distribution In summer, high Chl a concentrations were observed alongshore in surface water, especially outside the Changjiang River mouth and Hangzhou Bay with a maximum value of 16.09 μg dm−3 at St. 11. High ciliate abundances were mainly found in the northern and southern regions of the Changjiang River mouth occupied by CDW. Two maximum ciliate abundance values (2335 ind. dm−3, (St. 32) and 2870 ind. dm−3, (St. 18)) were found near the interface region between CDW and SWM (Fig. 3). In winter, surface Chl a concentration was maximum (1.66 μg dm−3) at St. 3–5, a value 10 times less than summer maximum, and decreased from the coastal-shelf waters (CoW and SMW) to KW. There were two patches of ciliate abundance. One was in the boundary of KW and SMW in the northern section E1 outside of the Changjiang River mouth. The other was in the coastal region of sections E3 and E4. Enhanced ciliate abundance was associated with the intrusion of KW in the northeastern of Taiwan Island (Fig. 4). Average surface ciliate abundance and biomass were higher in CDW (942 ± 697 ind. dm−3 and 3.3 ± 5.57 μg C dm−3, respectively) than those in SMW (403 ± 307 ind. dm−3 and 0.29 ± 0.28 μg C dm−3, respectively) (Fig. 5A). Similarly, average integrated (over 0–30 m depth) ciliate

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

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C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

Table 1 List of tintinnids and number of samples in which this species appeared in the Changjiang river estuary and its adjacent seas in summer, on the continental shelf in winter. Biogeographic distribution patterns of tintinnids genera (cosmopolitan, neritic and warm water ) were referred to Dolan and Pierce (2013). The number in the parentheses indicate sample size in the water masses.

Cosmopolitan

Summer

Water masses

Species

CDW (49)

Amphorellopsis acuta⁎ Codonellopsis mobilis C. ostenfeldi⁎ Eutintinnus tenius Eutintinnus sp. 1

Neritic

Favella taraikaensis Favella sp. 1 Leprotintinnus nordquisti L. simplex⁎ Stenosemella nivalis⁎ S. pacifica S. ventricosa⁎ Tintinnidium spp.⁎ Tintinnopsis amoyensis T. beroidea⁎ T. baltica T. brasiliensis T. butshlii T. digita T. directa T. gracilis⁎

Warm water

6 3 7 3 6

6 6 3 1 3 16 1 4 2 4

SMW (112)

Species

CoW (15)

2 5 5 2 21

Codonellopsis mobilis Dadayiella acutiformis Dadayiella sp. 1 Dictyocysta reticulate Eutintinnus fraknoii Eutintinnus sp. 1 Protorhabdonella curta Salpingella acuminata Salpingella attenuata Leprotintinnus simplex Stenosemella nivalis Tintinnidium spp. Tintinnopsis elongata T. orientalis T. radix T. tubulosoides

20 1 8 14 4 4 1 1 16 27 17 11 2 1 5 1 9 7

7 13 7 4 4 2

Xystonellopsis favata⁎

Water masses

4 4 2 9 3 4

2

T. minuta T. orientalis T. parva T. radix⁎ T. schotti T. tubulosoides Rhabdonella amor Undella ostenfeldi⁎

Winter

5

SMW (57) 5 1

1 1

KW (46) 1 2 2 3 2 5 1

1 1 17 1

1 1 1

5 1 18

2

Epiorella healdi Epiplocyloides reticulata Proplectella claparedei Undella hyalina

9

3 1

1 1 1

1 3

⁎ Recorded by Ota and Taniguchi (2003).

abundance and biomass in CDW (27.59 ± 8.17 × 106 ind. m−2 and 73.21 ± 72.75 mg C m−2, respectively) were larger than those in SMW (19.63 ± 14.31 × 106 ind. m−2 and 59.96 ± 169.95 mg C m−2 ,

35° N 34°

respectively) in the estuary and adjacent sea. Average surface ciliate abundance and biomass were approximately two times higher in SMW (432 ± 616 ind. dm−3 and 0.69 ± 0.77 μg C dm−3, respectively) than

Neritic species Leprotintinnus simplex Stenosemella nivalis Tintinnidium spp. Tintinnopsis elongata T. orientalis T. tubulosoides T. radix

33° 32°

Warm water species Epiorella healdi Epiplocyloides reticulata

Cosmopolitan species

Proplectella claparedei Undella hyalina

Codonellopsis mobilis Dadayiella acutiformis Dadayiella sp.1

Dictyocysta reticulata Eutintinnus fraknoii

Eutintinnus sp.1 Protorhabdonella curta Salpingella acuminata Salpingella attenuata

31° 30° 29° 28° 27° 26° 25° 24°

120°

122°

124°

126°

128°

120°

122°

124°

126° E

128°

Fig. 6. Location of tintinnid species observed in winter 2007. The dashed isohalines indicate the surface boundary of the SMW and KW. SMW: shelf mixing water; KW: Kuroshio water.

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

(A)

Station 20

19

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10

18

16 20

19

18

17

16 20

19

18

17

16

CDW SMW

30 40

60

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T

1-1 CoW

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1-5

1-7

1-9 1-11 1-1

Ciliate abundance

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1-9 1-11 1-1

1-3

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1-9 1-11

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50

KW

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Depth (m)

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4-1 4-3 CoW

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4-10 4-1

Ciliate abundance

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4-7

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4-3

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100 150 Section E4 S

T

Ciliate abundance

200 Fig. 7. Vertical distribution of temperature (T, °C), salinity (S) and ciliate abundance (ind. dm−3) along the section B (A) in summer 2006, section E1 (B) and section E4 (C) in winter 2007. Dots indicate sampling positions. The blue dashed lines indicate the boundary of CDW and SMW, the CoW and SMW; red dashed lines indicate the boundary of the SMW and KW. The colour indicates different background of water masses. CoW: coastal water; CDW: Changjiang diluted water; SMW: shelf mixing water; KW: Kuroshio water.

those in CoW (209 ± 307 ind. dm−3 and 0.19 ± 0.36 μg C dm−3, respectively) and KW (202 ± 193 ind. dm−3 and 0.20 ± 0.18 μg C dm−3, respectively). Average integrated (over 0–30 m depth) ciliate abundance and biomass in SMW (39.01 ± 86.3 × 106 ind. m−2 and 30.91 ± 39.48 mg C m−2, respectively) were much higher than those in KW (16.93 ± 8.75 × 106 ind. m−2 and 14.03 ± 9.22 mg C m−2, respectively) and CoW (1.37 ± 2.15 × 106 ind. m−2 and 1.6 ± 2.61 mg C m−2, respectively) (Fig. 5). There was no significant difference of ciliate abundance

and biomass between the different water masses investigated during both seasons (t test, p N 0.05). 3.3. Tintinnid taxa and distribution In summer, the average tintinnid abundance was 300 ± 333 ind. dm− 3, contributing 40% ± 28% to the total ciliate abundance in all the layers. A total of 30 species (12 genera) was identified. Among

Table 2 Pearson correlations coefficients between total ciliate abundance (TC Ab), total ciliate biomass (TC Bi) in the different layers and environmental and biological factors. T: temperature; S: salinity; Chl a: Chlorophyll a concentration; DO: dissolved oxygen; TF: total nanoflagellate; Syn: Synechococcus; Picoeuk: picoeukaryotes; HB: heterotrophic bacteria; Pico: picoplankton. The numbers in the parentheses indicate sample size in the water masses.

Summer 2006 CDW (N = 49) SMW (N = 112)

Winter 2007 CoW (N = 15) SMW (N = 57) KW (N = 46)

Depth

T

S

TC Ab TC Bi TC Ab TC Bi

−0.02 0.07 −0.12 −0.05

−0.07 −0.38⁎⁎ −0.08 −0.1

−0.07 0.28 −0.39⁎⁎ −0.36⁎⁎

TC Ab TC Bi TC Ab TC Bi TC Ab TC Bi

−0.32 −0.15 −0.20 −0.28⁎ −0.46⁎⁎ −0.45⁎⁎

0.40 0.28 −0.15 −0.10 0.20 0.26

0.05 0.30 −0.28⁎ −0.28⁎ −0.33⁎ −0.27

Chl a 0.16 0.53⁎⁎ 0.38⁎⁎ 0.46⁎⁎ −0.26 −0.35 0.47⁎⁎ 0.50⁎⁎ 0.51⁎⁎ 0.46⁎⁎

DO

TF

0.04 0.23 −0.17 −0.26⁎⁎

– – – –

– – – – – –

0.30 0.01 0.41⁎⁎ 0.45⁎⁎ 0.37⁎ 0.45⁎⁎

Syn

Picoeuk

HB

Pico

0.20 0.47⁎⁎ 0.31⁎⁎ 0.28⁎⁎

0.25 0.53⁎⁎ −0.09 0.02

0.16 0.52⁎⁎ 0.10 0.17

0.19 0.52⁎⁎ 0.23⁎ 0.28⁎⁎

0.52 0.85⁎⁎ −0.15 −0.06 0.32⁎ 0.42⁎⁎

0.83⁎ 0.85⁎⁎ 0.46⁎⁎ 0.52⁎⁎ 0.35⁎ 0.35⁎

−0.17 −0.04 0.13 0.10 0.42⁎⁎ 0.47⁎⁎

0.45 0.35 0.53⁎⁎ 0.59⁎⁎ 0.43⁎⁎ 0.49⁎⁎

⁎ p b 0.05. ⁎⁎ p b 0.01.

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

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C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

estuary (water depth b 100 m) (Table 1). Most of tintinnids species were simultaneously present in CDW and SMW, although warm water species Rhabdonella amor and Xystonellopsis favata favored the saline SMW. The tintinnid distribution was similar in both water masses (CD and SMW) during summer.

them, the genera Tintinnopsis containing 14 species was an important component of tintinnids in the Changjiang river estuary. Neritic species in the biogeographic distribution patterns were dominant, e.g., the genera Stenosemella, Tintinnidium and Tintinnopsis were frequently found in high abundance within the Changjiang river

(A)

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Fig. 8. Relationships between environmental factors (salinity, temperature, DO, Chl a concentration), picoplankton (Syn: Synechococcus, picoeuk: picoeukaryotes, HB: heterotrophic bacteria) and total ciliate biomass in the each water layer during summer 2006 (A) and winter 2007 (B). (DO data from Zhu et al., 2011). SMW: shelf mixing water; KW: Kuroshio water.

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

(B)

CoW

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2.5

KW

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Fig. 8 (continued).

In winter, the tintinnid had an average abundance (15 ± 25 ind. dm− 3, represented 12% ± 23% of total ciliate abundance. A total of the 20 tintinnid species belonging to 14 genera were recorded, including 9 cosmopolitan species, 7 neritic species and 4 warm water species (Table 1). Neritic species were more frequently present in

CoW and SMW than in KW, of which only four species (Stenosemella nivalis, Tintinnidium spp., Tintinnopsis elongate and Tintinnopsis tubulosoides) were observed in CoW. Cosmopolitan and warm water species were found in SMW and KW, belonging to the offward open water in the continental shelf (Fig. 6).

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

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C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

SMW

TF abundance (103ind. cm-3)

Total ciliate abundance (ind. dm-3)

4000

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Fig. 9. Relationships between total nanoflagellate (TF) and abundance of total ciliate, picoplankton (Syn: Synechococcus, picoeuk: picoeukaryotes, HB: heterotrophic bacteria) in the SMW and KW in winter 2007. SMW: shelf mixing water; KW: Kuroshio water.

3.4. Section distribution In summer, along section B (Fig. 7A), there was stratification between upper warm, fresh water and deep cool, saline water and a weak trend of bottom water upwelling. Salinity front occurred in the shallow coastal area, evidenced by mixing boundary of CDW and SMW at Sts. 18 and 17. There was a significant increase in ciliate abundance between the minimum of 245 ind. dm− 3 at St. 17 and the

maximum of 2870 ind. dm− 3 at St. 18, nearby the coastal salinity front. Additionally, Chl a concentration and ciliate abundance at Sts. 16 and 17 (SMW) were lower than that in CDW along this section. In winter, temperature of the shelf mixed water increased from the coast to the edge of the outer shelf in section E1. There was a shelfbreak front at Sts. 1-9 and 1-10 due to the intrusion of KW. Salinity variation was not obvious in the SMW and KW with the exception of coastal front between Sts. 1-1 and 1-3. Ciliates were mainly found

34° N

34° N

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28°

DO 27° 120°

121°

122°

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125° E

Ciliate abundance 27° 120°

121°

122°

123°

124°

125° E

Fig. 10. DO (mg dm−3) and ciliate abundance (ind. dm−3) distribution of near-bottom waters in August, 2006 (DO data from Zhu et al., 2011).

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

Station

Station

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Fig. 11. Temperature (°C), salinity, DO (mg dm−3), ciliate abundance (ind. dm−3) and biomass (μg C dm−3), HB (heterotrophic bacteria) abundance (105 cells cm−3) distribution along the section A in August 2006 (DO data from Zhu et al., 2011). The dashed lines indicate the boundary of low oxygen (DO = 3 mg dm−3).

in surface and subsurface of SMW, rarely in CoW and SMW. Maximum (1664 ind. dm− 3) ciliate abundance was found at 20 m depth at St. 1-7 on the north-west side of the shelf-break front (Fig. 7B). Along section E4 (Fig. 7C), the encounter of cold and fresh CoW with warm and saline SMW, formed a thermohaline coastal front between Sts. 4-1 and 4-3. Ciliate abundance decreased with depth and exhibited low values low value in KW. An obvious increase of ciliate abundance (2202 ind. dm−3) was found in the surface at St. 4-3, close to the coastal front, about 5 times higher than at the neighboring stations.

3.5. Relationship between ciliate biomass and environmental and, biological factors During summer 2006, total ciliate biomass in the different layers showed a significant and negative correlation with temperature in CDW (Spearman coefficient, p b 0.01, N = 49) and salinity in SMW (p b 0.01, N = 112). Negative correlations were found between total ciliate biomass with DO in SMW (Table 2, Fig. 8A). In both water masses of Changjiang Estuary, there were significantly positive correlations

between total ciliate biomass and both Chl a concentration and picoplankton biomass (Table 2). In winter, almost all sampling stations were located in SMW and KW. Salinity was negatively linked to ciliate biomass in SMW (Spearman coefficient, p b 0.05, N = 57). Significant positive covariations were found between ciliate biomass and both picoeukaryotes and Synechococcus within CoW (p b 0.05, N = 15) and KW (p b 0.05, N = 46) (Table 2). Total ciliate biomass within SMW and KW was significantly and positively correlated with Chl a concentration, and picoplankton biomass (Fig. 8B), while total ciliate biomass was significantly and positively correlated with total nanoflagellate abundance (Fig. 9).

4. Discussion 4.1. Zone of tintinnid species For tintinnids counts, some studies include empty loricae (Leakey et al., 1992), although most do not. Sometimes, tintinnid protoplast

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

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C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

can be separated from the loricae during sample handling or agglomerated loricae may be confused with detritus, so counting empty loricae would lead to overestimates of their abundance. However, it is unrealistic to identify species only from the protoplast, without loricae. Part of tintinnids species richness and abundance may be underestimated by excluding counts of empty loricae. In both cruises, the percentage of tintinnid abundance in the whole ciliate abundance was lower than in the estuaries (40% vs. 42%) and in the open shelf (12% vs. 32%) (McManus and Santoferrara, 2013). The neritic genera Stenosemella and Tintinnopsis more frequently appeared in CDW and CoW than in the other water masses so as to form agglutinated loricae, which was affected by the arenaceous and muddy outflow from the Changjiang River according to Reid and Stewart (1989). In winter, tintinnids recorded on the continental shelf were characterized by pronounced distribution zones of species. Cosmopolitan and warm water species were very largely restricted to SMW and KW; neritic species were more present in CoW and SMW than in KW. Particular species of tintinnids were recognized as reliable indicator because their loricae outside of the soft cell body can remain in suspension in a particular water masses for a fairly long times (Kato and Taniguchi, 1993; Zeitzschel, 1990). Epiplocyloides reticulata, Eutintinnus fraknoii, Salpingella acuminata, Salpingella attenuata and Undella hyalina were present in the Kuroshio Current along the meridian 138 °E in the south of Japan (Gomez, 2007). In this study, E. fraknoii and S. acuminata were observed in the KW, but E. reticulata and S. attenuata were found in SMW, and U. hyaline in both water masses (SMW and KW). Five oceanic tintinnid species (Gomez, 2007) would be indicators of the Kuroshio Current. Therefore, these species might indicate the intrusion route of KW from the slope to shelf. In addition, E. reticulata, S. attenuata and U. hyalina belonging to the Kuroshio Current were also found in SMW, which might indicate that KW could be one source of SMW in the East China Sea. 4.2. Water masses and ciliate abundance increase In winter, ciliate abundance (0–30 m) decreased from SMW to CoW and the oceanic KW by factors ca. 40 and 2.5, respectively. These results are in agreement with the wintertime depth-weighted average abundance higher in SMW than in coastal water reported by Chiang et al. (2003) and with the 2-fold reduction of total ciliate abundance from the shelf-slope to oceanic waters in the south-western Atlantic found by Santoferrara and Alder (2009). However, in this study, there was no significant difference in ciliate abundance and biomass between both water masses in summer and the three water masses in winter, which may indicate a slight influence of water masses on the ciliate distribution. The nature of oceanic fronts as boundaries between water masses with different properties (temperature, salinity, etc.) and the enhancement of vertical and horizontal mixing along them leads to increased productivity (Pingree et al., 1981). The elevated primary production associated to frontal structures was largely investigated (Belkin et al., 2009; Holligan, 1981; Le Fevre, 1986). Frontal structures were also shown to enhance ciliate abundance (Santoferrara and Alder, 2009; Simpson et al., 1979). Mesoscale (km) frontal structures were suggested to be more relevant to describe plankton (including ciliates) distribution than hydrographic variable per se (Zarauz et al., 2008). In summer, the coastal salinity front was dominant in the Changjiang river estuary (Tang and Zheng, 1990). The thermohaline front that is formed in winter along the Fujian-Zhejiang Coast between southward flowing cold, fresh CoW and warm, saline offshore SMW flowing northward via the Taiwan Strait was previously established by Belkin et al. (2009) and Chen (2009). Tenfold increase in ciliate abundance was reported in the Islay front (Simpson et al., 1979), and fronts in the south-western Atlantic were

shown to increase ciliate abundance by 50% (N 2 × 103 ind. dm− 3) (Santoferrara and Alder, 2009). In the present study, the peak of ciliate abundance (N2 × 103 ind. dm−3) represented a 10 times increase in the salinity front at St. 18 on section B (Fig. 7A). Chiang et al. (2003) also reported high ciliate abundance increase in the margins of the Changjiang plume induced by the front between CDW and SMW. In winter, a threefold increase in ciliate abundance (1664 ind. dm− 3) was observed on the western side of shelf-break front on section E1 and a fivefold enhancement of ciliate abundance (2202 ind. dm− 3) was observed in the coastal frontal area on section E4 (Fig. 7B and C). By comparison, our high ciliate abundance ciliate values are slightly lower than those reported in previous studies. In addition to mesoscale distribution of ciliate abundance, the concerned phenomenon in this study was documented by distinct finescale patches of ciliate abundance that were associated with fronts or pycnoclines (Montagnes et al., 1999). The upwelling observed in section B at Sts. 18 and 19, where ciliate abundance increased by factor of 2 at 45 m depth (Fig. 7A), is reminiscent of the upwelling front reported by (Tang and Zheng, 1990) in summer in the Zhejiang coast. 4.3. Picoplankton, nanoflagellate and ciliate distribution When considering the complex ciliate grazing selection, correlation analysis provides information on direct or indirect relationships among biological variables. Total ciliate biomass exhibited close correlation with Chl a concentration and picoplankton biomass within most of water masses, except for CoW. On the shelf, Chl a concentration and picoplankton biomass were higher in summer than in winter (Fig. 8), which helped to explain that ciliate biomass in the Changjiang Estuary and its adjacent sea was larger in summer than in winter. In the CDW, ciliate biomass showed significant positive correlations with biomasses of Synechococcus, picoeukaryotes and heterotrophic bacteria (Table 2). According to the estimated ratio C:chl a 67.4 g g−1 in CDW (Chang et al., 2003), the average contribution of Synechococcus and picoeukaryotes to phytoplankton carbon biomass were 4.7% and 0.7%, respectively. Many evidences supporting the coupling between Synechococcus and ciliate stem from a prey–predator relationship (Chen, 2001). Picoeukaryote grazing by oligotrich ciliates and tintinnids was previously reported both in the northeast Atlantic Ocean (Karayanni et al., 2005) and in laboratory experiments (Bernard and Rassoulzadegan, 1990; Verity, 1988). Picoeukaryotes are the most competitive among picophytoplankton in near-shore waters with abundant river-borne nutrients (Pan et al., 2007). Accordingly, the tight trophic relationship between picoeukaryotes and ciliates was quite apparent in CDW and CoW but not significant in SMW off the Changjiang River mouth or weaker than the relationship between Synechococcus and ciliates in the oligotrophic KW. In winter, ciliate biomass showed a close linear correlation with picoeukaryote biomass, but not with Synechococcus biomass (Fig. 8B ). It seems that picoeukaryotes were relatively more important than Synechococcus in influencing the winter ciliate distribution on the continental shelf. Nanoflagellates, including mixotrophic pigmented and nonpigmented forms, are ascribed primary consumers of bacteria and picophytoplankton (Hahn and Höfle, 2001; Tsai et al., 2007). They are also potential major food source for ciliates (Sanders and Wickham, 1993). Thus, the indirect or direct trophic coupling among pico-, nano- and micro- plankton groups realizes the transfer of their carbon and energy to higher trophic level through the microbial food web. Although flagellate data in the Changjiang Estuary were not available for examination, the tight connection during winter between picoplankton, total nanoflagellates and ciliates would support our hypothesis that nanoflagellates acted as an intermediary in the carbon flow from picoplankton to ciliates (Fig. 9). Total flagellate abundance correlated with components of picoplankton in KW, in a better way with picoeukaryotes and heterotrophic bacteria than with Synechococcus. Our Results are in agreement with (Tsai et al., 2008), who reported

Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003

C. Zhang et al. / Journal of Marine Systems xxx (2014) xxx–xxx

that heterotrophic bacteria contribute more to nanoflagellate carbon than does Synechococcus during the cold season. Furthermore, total ciliate abundance showed a positive and significant linear relationship with flagellate abundance. Tsai et al. (2013) also reported that nanoflagellate grazing was responsible for most of bacterial mortality during the summer in ECS. It can be deduced that under the influence of KW, picoplankton–nanoflagellate–ciliate was an effective pathway of material transfer in the microbial web during winter. 4.4. Environmental factor with ciliate abundance Water masses with different hydrographic features support provide a living environment for planktonic ciliates. In this study, salinity was a more important factor than temperature in regulating total ciliate distribution according to negative correlation between ciliate biomass and salinity in SMW (Fig. 8A and B). Although most oligotrich species were found in waters with salinity b35 (Lei et al., 2009), ciliate would likely tend to develop in waters of optimal salinity depending on seasonal change. Thompson et al. (2001) reported that stable temperature and salinity gradients would probably govern tintinnid specific abundance ranges on the mesoscale. During both investigated seasons, there was more tintinnids in SMW characterized by a well-marked salinity gradient than in other water masses. The tintinnid distribution within water masses was more clearly influenced by temperature when considering species composition. In the recent years, the areas adjacent to the Changjiang estuary in the ECS were shown to belong to the largest coastal low-oxygen zones (2 mg dm−3 b DO b 3 mg dm−3), and a dramatic increase in of hypoxia (DO b 2 mg dm−3) driven by organic matter decomposition and stratification was observed too (Chen et al., 2007; Zhu et al., 2011). The phenomenon of hypoxia occurred both in CDW and SMW (Fig. 8A), which was not a known feature of these water masses (Wei et al., 2007). In this study, the impact of DO concentration on ciliate abundance and biomass was not obvious, except in SMW where ciliate biomass was negatively and significantly correlated with DO. Ciliate community was largely restricted to waters containing at least 2 mg DO dm−3, in agreement with the work of (Dolan and Coats, 1991), reporting marked decreases in ciliate densities linked with oxygen depletion in deep water. What is noteworthy in our results is that ciliate abundance was relatively high within the near-bottom hypoxia zone (Fig. 10), slightly decreasing with the reduction in DO concentration in the vertical distribution. This would suggest that anaerobic ciliates or nanoflagellates were bacterivorous, which was reflected by heterotrophic bacteria abundance in the anoxic zone (Fig. 11). Many aloricated ciliate (e.g., scuticociliates) and heterotrophic flagellates that were reported bacterivores below the oxycline and in the anoxic zone (Fenchel et al., 1990; Rocke and Liu, 2014) weakly contributed to total ciliate abundance and biomass. However, alive tintinnids without empty loricae such as Leprotintinnus simplex, Eutintinnus tenius, Tintinnopsis parva, Tintinnidium spp. and Stenosemella nivalis found in the bottom hypoxia zone represented 41%–99% of total biomass, whereas they were not reported as anaerobic protozoan in previous researches. Although there is lack of nanoflagellate data, it could be inferred that tintinnids were nondirect predators of heterotrophic bacteria, grazing on nanoflagellates that are predators of heterotrophic bacteria. Fenchel et al. (1990) proposed that anaerobic protozoan are largely dependent on bacteria, using fermentative processed for their energy metabolism. Significant and positive correlation between ciliate and heterotrophic bacteria biomass in CDW also provided evidence for potential effect of heterotrophic bacteria on ciliate distribution (Fig. 8A). This is consistent with the transition zone characterized by high levels of labile dissolved organic matter and increasing bacteria activity reported in the Chesapeake Bay (Dolan and Coats, 1990) and Danish eutrophic fjords (Fenchel et al., 1990). Ciliate abundance and biomass showed a marked increase or reached maximum values in conenction with the high heterotrophic bacteria abundance in the anoxic/oxic interfaces or oxycline (Fig. 11).

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5. Conclusion The distribution of ciliate abundance and biomass was slightly influenced by different water masses on the continental shelf of the East China Sea. The enhancement of ciliate abundance occurred nearby frontal structures. In summer, most species were neritic in CDW and SMW, whereas in winter, there was few neritic species in CoW and SMW, but Cosmopolitan and warm water species were present in KW. Results suggest close trophic coupling between ciliates and picoplankton within water masses around Changjiang river estuary. However, ciliate abundance in KW was related to nanoflagellate and heterotrophic bacteria abundances. Further studies involving grazing experiments and ecological models are needed to document those trophic relationships within the microbial web on the continent shelf. Acknowledgments We thank the scientists, officers and crews of R/V “Beidou” for their guidance and assistance during the cruises. We also thank Cheng-Gang Liu for helping with chlorophyll a data, Jing Zhang for providing the DO data and Michel Denis for improving the manuscript. This study was funded by Natural Science Foundation of China U1406403, 973 Project 2011CB409804, Natural Science Foundation of China (NSFC) No. 41306119, the Foundation of Tianjin Key Laboratory of Marine Resources and Chemistry (grant no. 201301) (Tianjin University of Science & Technology), PR China. References Azam, F., Fenchel, T., Field, J.G., Gray, J.S., Meyer-Reil, L.A., Thingstad, F., 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263. Belkin, I.M., Cornillon, P.C., Sherman, K., 2009. Fronts in large marine ecosystems. Prog. Oceanogr. 81, 223–236. Bernard, C., Rassoulzadegan, F., 1990. Bacteria or microflagellates as a major food source for marine ciliates: possible implications for the microzooplankton. Mar. Ecol. Prog. Ser. 64, 147–155. Bryan, J., Rlley, J., Williams, P.l., 1976. A Winkler procedure for making precise measurements of oxygen concentration for productivity and related studies. J. Exp. Mar. Biol. Ecol. 21, 191–197. Chang, J., Shiah, F.K., Gong, G.C., Chiang, K.P., 2003. Cross-shelf variation in carbon-tochlorophyll a ratios in the East China Sea, summer 1998. Deep-Sea Res. II 50, 1237–1247. Chen, K.M., 2001. Ciliate grazing on Synechococcus in a coastal andshelf marine ecosystem: spatial-temporal variations andimportanc e to biological carbon cycling. National Taiwan Ocean University. Chen, C., 2009. Chemical and physical fronts in the Bohai, Yellow and East China seas. J. Mar. Syst. 78, 394–410. Chen, C.C., Gong, G.C., Shiah, F.K., 2007. Hypoxia in the East China Sea: one of the largest coastal low-oxygen areas in the world. Mar. Environ. Res. 64, 399–408. Chen, C.C., Shiah, F.K., Gong, G.C., Chiang, K.P., 2003. Planktonic community respiration in the East China Sea: importance of microbial consumption of organic carbon. DeepSea Res. II 50, 1311–1325. Chiang, K., Lin, C., Lee, C., Shiah, F.K., Chang, J., 2003. The coupling of oligotrich ciliate populations and hydrography in the East China Sea: spatial and temporal variations. Deep-Sea Res. II 50, 1279–1293. Dolan, J.R., Coats, D.W., 1990. Seasonal abundances of planktonic ciliates and microflagellates in mesohaline Chesapeake Bay waters. Estuar. Coast. Shelf Sci. 31, 157–175. Dolan, J.R., Coats, D., 1991. Changes in fine-scale vertical distributions of ciliate microzooplankton related to anoxia in Chesapeake Bay waters. Mar. Microb. Food Webs 5. Dolan, J.R., Pierce, R.W., 2013. Diversity and distributions of tintinnids. In: Dolan, J.R., Montagnes, D.J.S., Agatha, S., Coats, D.W., Stoecker, D.K. (Eds.), The biological and ecology of tintinnid ciliates. Wiley-blackwell, p. 216. Fenchel, T., Kristensen, L.D., Rasmussen, L., 1990. Water column anoxia: vertical zonation of planktonic protozoa. Mar. Ecol. Prog. Ser. 62, 1–10. Gomez, F., 2007. Trends on the distribution of ciliates in the open Pacific Ocean. Acta Oecol. Int. J. Ecol. 32, 188–202. Gong, G.C., Lee Chen, Y., Liu, K., 1996. Chemical hydrography and chlorophyll a distribution in the East China Sea in summer: implications in nutrient dynamics. Cont. Shelf Res. 16, 1561–1590. Gong, G.C., Shiah, F.K., Liu, K., Chuang, W.S., Chang, J., 1997. Effect of the Kuroshio intrusion on the chlorophyll distribution in the southern East China Sea during spring 1993. Cont. Shelf Res. 17, 79–94. Gong, G.C., Shiah, F.K., Liu, K.K., Wen, Y.H., Liang, M.H., 2000. Spatial and temporal variation of chlorophyll a, primary productivity and chemical hydrography in the southern East China Sea. Cont. Shelf Res. 20, 411–436.

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Please cite this article as: Zhang, C., et al., Influence of different water masses on planktonic ciliate distribution on the East China Sea shelf, J. Mar. Syst. (2014), http://dx.doi.org/10.1016/j.jmarsys.2014.09.003