Wintertime meso-scale horizontal distribution of large tintinnids in the southern Yellow Sea

Chinese Journal of Oceanology and Limnology Vol. 27 No. 1, P. 31-37, 2009 DOI: 10.1007/s00343-009-0031-1

Wintertime meso-scale horizontal distribution of large tintinnids in the southern Yellow Sea*

ZHANG Cuixia (张翠霞)†,††††, ZHANG Wuchang (张武昌)†,†††,**, XIAO Tian (肖天)†, LÜ Ruihua (吕瑞华)††, SUN Song (孙松)†, SONG Weibo (宋微波)†††

† Key Laboratory of Marine Ecology and Environmental Science, Institute of Oceanology, Chinese Academy of Sciences,

Qingdao 266071, China †† Key Laboratory for Science and Engineering of Marine Ecology and Environment, SOA, First Institute of Oceanography, SOA,

Qingdao 266061, China ††† Laboratory of Protozoology, KML, Ocean University of China, Qingdao 266003, China †††† Graduate School of Chinese Academy of Sciences, Beijing100049, China

Received Aug. 21, 2007; revision accepted Jan. 14, 2008

Abstract Spatial distribution of some large tintinnid species (nominally > 76 μm) is investigated on samples vertically towed in the southern Yellow Sea in winters of 2001 to 2004. Nine tintinnid species are recorded: Codonellopsis morchella, Stenosemella pacifica, S. steini, Tintinnopsis schotti, T. radix, T. karajacensis, Eutintinnus tenuis, Parafavella sp., Leprotintinnus neriticus, of which C. morchella and T. radix dominated in the warm tongue-shaped zone of the Yellow Sea Warm Current (YSWC), and S. pacifica is the next in abundance. Our study shows that these tintinnids occur repeatedly in certain special distribution patterns.

Keyword: tintinnid; horizontal distribution; southern Yellow Sea

1 INTRODUCTION

The Yellow Sea (Fig.1A) is located between China and Korea, bounded to the north by the Bohai Sea and to the south by the East China Sea. The maximum depth of the sea is 103 m in average of 44 m, representing one of the western Pacific marginal seas. A deep trough (depth > 90 m) runs through it and can be traced south to the northern end of the Okinawa Trough in the East China Sea.

Tintinnids (Ciliophora: Oligotrichida) are the best known group of marine ciliates for their hard loricae. Although there are several literatures on the tintinnid taxonomy according to the samples taken from nearby Bohai Bay (Wang, 1936) and the Jiaozhou Bay (Yin, 1952; 1957), the study on tintinnid species composition and abundance in the Yellow Sea is scarce (Xu and Su, 1995). In this paper, spatial distribution of some large tintinnids (>76 μm) in southern Yellow Sea during four winter-cruises in 2001 through 2004 is reported.

2 MATERIALS AND METHODS

Four winter-cruises in the southern Yellow Sea were carried out onboard R/V Beidou in November 16 to December 1, 2001 (coded as Cruise 2001);

January 4–19, 2002 (Cruise 2002); January 5–18, 2003 (Cruise 2003); and December 30, 2003 to January 12, 2004 (Cruise 2004). The positions of investigation stations are shown in Fig.1B. Some stations in the south and the southeast part of the study area were not covered in some cruises due to bad weather.

In each station, the surface temperature and salinity were recorded by a SeaBird CTD system placed at 5 m depth. In Cruises 2003 and 2004, water samples of chlorophyll a (Chl a) concentration were taken at different depths using the Rossette Niskin water samplers. 500 ml surface water were filtered with GF/F filter, and then stored in darkness at -20°C until use. Later in the laboratory, the GF/F filters were extracted with 90% acetone in darkness at -20°C for 24 h. The Chl-a concentrations were determined using a Turner Designs (Model II) fluorometer that was calibrated with pure Chl-a from Sigma (Strickland and Parsons, 1972). Chl-a

* Supported by Natural Science Foundation of China (NSFC, No.

40876085), National Key Basic Research Program of China (973 Program,

No. 2006CB400604), Knowledge Innovation Program of CAS (No.

KZCX2-YW-213-3) and NSFC (No. 40821004). This study is also a part

of the postdoctoral research in the Ocean University of China

** Corresponding author: [email protected]

CHIN. J. OCEANOL. LIMNOL., 27(1), 2009 Vol.27 32

Fig.1 The position and isobath (m) of the study area (A) and the investigated stations (B)

concentration was not determined for Cruises 2001 and 2002 samples.

The tintinnid samples were collected by vertical tow net (opening 0.1 m2, mesh size 76 μm) from 2 m above bottom to surface. A flow meter attached at the opening of the net was used to measure the volume of filtered water. The samples were fixed in formalin at final concentration of 5%. In laboratory, the samples were fixed and concentrated to a volume of about 60 ml and well mixed, from which 3–10 ml were sipped into a counting chamber. The lorica of tintinnids in the chamber was identified and counted under a Nikon stereomicroscope at 50 × magnification. Species were determined according to the shape of lorica under Olympus BX50 microscope referring to Wang (1936), Yin (1952) and Yoo et al. (1988). The abundance was measured in the average number of individuals per m3 (ind. m-3).

3 RESULTS

In general, the studied area is characterized with the intrusion of the Yellow Sea Warm Current (YSWC) from southeast to the northwest (Fig. 2). In

the two sides of the YSWC are waters of low temperature and low salinity, colder in the northern side than that in the southern. The salinity of waters in coastal areas of the Haizhou Bay and Subei Bank are the lowest. The Chl a concentration is high in the coastal Subei Bank and low in the central YSWC.

In addition, variations in season and annum are obvious in the YSWC (Table 1). It is warmer in November than in January in overall, and saltier in January (33.77 to 34.45) than in November ((33.24). In November, the YSWC is weak whose 32.4 salinity contour was limited in the south of 33.5°N, while it reached 34.5°N or farther northward in Januaries (Fig.2).

Nine species are recorded: Codonellopsis morchella, Stenosemella pacifica, S. steini, Tintinnopsis schotti, T. radix, T. karajacensis, Eutintinnus tenuis, Parafavella spp. and Leprotintinnus neriticus. Most species are longer than 76 μm, except for S. steini. The abundance varied greatly to 10-fold among these species: from 30 229 for C. morchella to 247 ind. m-3 for Parafavella spp.

Table 1 Ranges of surface temperature (°C), salinity, and Chl a concentration (μg L-1) in the four cruises

T S Chl-a

Cruise 2001 14.20 (St. 7674, 76184)

-18.20 (St. 144194)

31.29 (St. 13094)

-33.24 (St. 144194)

Cruise 2002 8.43 (St. 89194)

-14.25 (St. 14494).

31.55 (St. 10394)

-34.14 (St. 14494)

Cruise 2003 7.24 (St.12994)

-15.17 (St. 152194)

31.73 (St. 8894)

-33.77 (St. 14494)

0.22 (St. 118194)

-2.83 ( St.12294)

Cruise 2004 5.27 ( St. 7994)

-16.89 (St. 144194)

31.33 (St. 14894)

-34.45 (St. 13594)

0.27 (St. 11594)

-1.75 (St. 11394)

St.: the station number

No.1 ZHANG et al.: Wintertime meso-scale horizontal distribution of large tintinnids in southern Yellow Sea 33

Fig.2 Spatial distributions of surface temperature (°C), salinity, and chlorophyll a concentration (Chl-a, μg L-1) during the four cruises (The sampling stations are indicated in dot)

The occurrence and maximum abundance of these species in the cruises varied in season and annum (Table 2). The number of species in the four cruises is 8, 6, 5, and 5, respectively. C. morchella and E. tenuis occurred only in Cruise 2001, while T. radix, S. pacifica, S. steini and T. karajacensis in all four cruises. From November 2001 to January 2002, the abundance of T. radix increased, while that of T.

schotti decreased with C. morchella disappearance. The spatial distribution varies distinctly among

species, which is closely related with YSWC (Figs.3–6). C. morchella and T. radix flocked near the central YSWC shown in Cruise 2001; and T. radix did in all January cruises. S. pacifica occurred just around the tongue-shaped warm part of the YSWC shown in Cruises 2001 and 2003, whereas the

CHIN. J. OCEANOL. LIMNOL., 27(1), 2009 Vol.27 34

Table 2 The maximum abundance (ind. m-3) of tintinnids in the four cruises

Species Cruise 2001 Cruise 2002 Cruise 2003 Cruise 2004

C. morchella 30 229

T. radix 105 1 025 5 457 1 283

S. pacifica 111 1 027 4 235 284

S. steini 11 873 4 025 1 055 386

T. karajacensis 1 737 867 248 69

Parafavella sp. 220 247 15

T. schotti 419 123

E. tenuis 5 117

L. neriticus 963

distribution was limited to the Subei Bank in Cruise 2001 but expanded to the northern cold waters east of Shandongtou in Cruise 2004. T. karajacensis distributed mainly in the Subei Bank in 2002 cruise (Fig.7) while S. steini in all of the four cruises (Fig.8). Their distribution area never spread northward beyond 36°N. Unlike T. karajacensis and S. steini, Parafavella spp. occurred in mainly the northern part of the study area north of 35°N (Fig.9). To the rest, E. tenuis distributed in the Haizhou Bay in Cruise 2001 (Fig.10) and L. neriticus restricted to the Subei Bank in Cruise 2004 (Fig.10).

The special distribution of tintinnids is irregular and often in isolated areas, i.e., a few high abundance areas in just several stations are surrounded by areas of much low abundance. For example, in Cruise 2002, the maximum abundance of T. radix is 1 025 ind.m-3

recorded in St.14194, followed by 499 in St.15294; 441 in St.15094; and 416 ind.m-3 in St. 14394; and below 150 ind.m-3 in other stations. That of S. pacifica is 1 027 ind.m-3 in St. 13094, surrounded by much lower abundance: 440 in St. 13994; 326 in St. 10494; 219 in St. 12994; 182 in St. 15694; 134 in St. 14194; and below 100 ind. m-3 in other stations.

Fig.3 Spatial distribution of C. morchella abundance (ind. m-3) in Cruise 2001 (Sampling stations are indicated in dot)

Fig.4 Spatial distribution of T. radix abundance (ind. m-3) in the four cruises (Sampling stations are indicated in dot)

Fig.5 Spatial distribution of S. pacifica abundance (ind. m-3) in the four cruises (Sampling stations are indicated in dot)

Fig.6 Spatial distribution of T. schotti abundance (ind. m-3) in Cruises 2001 and 2002 (Sampling stations are indicated in dot)

No.1 ZHANG et al.: Wintertime meso-scale horizontal distribution of large tintinnids in southern Yellow Sea 35

Fig.7 Spatial distribution of T. karajacensis abundance (ind. m-3) in the four cruises

Sampling stations are indicated in dot

Fig.8 Spatial distribution of S. steini abundance (ind. m-3) in the four cruises

Sampling stations are indicated in dot

Fig.9 Spatial distribution of Parafavella spp. abundance (ind. m-3) in Cruises 2001, 2002 and 2003 Sampling stations are indicated in dot

Fig.10 Spatial distribution of abundance (ind. m-3) of E. tenuis in Cruise 2001 and L. neriticus in Cruise 2004 Sampling stations are indicated in dot

CHIN. J. OCEANOL. LIMNOL., 27(1), 2009 Vol.27 36

4 DISCUSSION

Changes in species number and the abundance indicate possible seasonal succession in the study area in the four cruises, of which Cruise 2004 is special with the decrease in abundance for all species and with the appearance of L. neriticus who is not seen in Cruises 2002 and 2003. This annual variation can be due to fluctuation in timing of the peak abundance, which may vary within approximately a month (Verity, 1987; Abboud-Abi Saab, 1989; Modigh and Castaldo, 2002).

The distribution areas of C. morchella and T. radix are not parallel to but shift westward off the Yellow Sea trough (Figs.3, 4), which is consistent with the westward shift of the YSWC from the trough axis (Huang et al., 2005).

In November 2001, C. morchella distributed also in the west of the YSWC core (Fig.3); and similar was T. radix but went further beyond the YSWC core to the Haizhou Bay area shown in Cruises 2001 and 2003 (Fig.4), which might be due to the sporadic nature of the YSWC. The distribution of C. morchella and T. radix could extend into the Subei Bank and remain stable there for some period of time.

Often, the distributions of C. morchella and T. radix do not match the salinity maximum. For example, in November 2001, the salinity maximum was in St. 144194 (Fig.2), and the maximum abundance of C. morchella appeared in St. 13594 (Fig.3). In January 2002, the salinity maximum centered in St. 14494 (Fig. 2), and the abundance of T. radix maximized in St. 14194 (Fig.4). Similarly, in January 2003, St. 14494 was the maximum center of salinity (Fig.2), while the abundance of T. radix peaked in St. 13594 (Fig.4); in January 2004, both salinity and abundance of T. radix maximized in St. 13594.

The above-mentioned inconsistency between the maximum tintinnid abundance and the center of warm salty tongue-shaped zone is probably resulted from two aspects. First, the vertical distributions of the YSWC and tintinnids were not considered. Wang and Zuo (2004) noted that the YSWC might intrude in the middle depth. Therefore, the data at 5 m deep might not represent correctly those of the YSWC core. Second, additional unknown factors might complicate the tintinnid distribution.

As both C. morchella and T. radix were seen in all the four cruises during winter between November and January, the two species can be used to trace the

YSWC. Some species can occur in the same season and same station in both coastal and open ocean cases (Modigh and Castaldo, 2002 and references therein). Hydrography related tintinnid biogeographic distributions have been studied in certain areas (Kato and Taniguchi, 1993; Pierce and Turner, 1993; Cordeiro, 1997; Thompson, 1999, 2001), and used to track the upwelling in the North Sea (Balech, 1972), showing certain relationship to water mass circulation. Thompson (1999) used tintinnids as tracers to oceanic currents, taking tintinnids Dictyocysta californiensis and Ormosella acantharus for tracking the Cape Horn Current (Thompson, 2001). Recently, Modigh and Castaldo (2002) suggested that the recurrent pattern of the most abundant tintinnid species could be specific “fingerprints” for that area.

In general, no relationship exists between tintinnids abundance and Chl a concentration in this study. Although T. radix could occur in the YSWC area of low Chl a concentration, the distribution of T. radix may dependent on physical oceanography. The coincidence between high tintinnid abundance and high Chl a concentration in some cases is just as a special case when the physical environment favored both tintinnid and phytoplankton to bloom. As Thompson et al. (1999, 2001) previously stated that, the range of tintinnid specific abundance is probably decided by abiotic factors rather than food availability.

5 ACKNOWLEDGEMENTS

We thank the crew of R/V Beidou and Mr. H. WANG for sample collection, and the colleagues of this program for sharing the hydrographic data of the study area.

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