Meso-scale spatial distribution of large tintinnids

Chinese Journal of Oceanology and Limnology
Vol. 26 No. 1, P. 81-90, 2008
DOI: 10.1007/s00343-008-0081-9
Meso-scale spatial distribution of large tintinnids in early
summer in 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 Sciences, Institute of Oceanology, Chinese Academy of Sciences,
Qingdao 266071, China)
(††Laboratory of Protozoology, KML, Ocean University of China, 266003 Qingdao, China)
(†††
Key Lab for Science and Engineering of Marine Ecology and Environment, SOA, First Institute of Oceanography, SOA,
Qingdao 266061, China)
Received Feb. 21, 2006; revision accepted
Abstract
The spatial distribution of some large tintinnid species (nominally>76 μm) was investigated
according to samples collected by vertical towing in cruises to the southern Yellow Sea in summer
2000–2002 and 2004. Eight species were identified: Codonellopsis mobilis, Leprotintinnus netritus,
Tintinnopsis karajacensis, T. japonica, T. kiaochowensis, T. butschlii, T. radix, and Parafavella sp. With
maximum abundance of 158.2 ind/L in June 2004, C. mobilis was the dominant species, lasting from May
to July 2004. Tintinnid communities were patchy and distributed mainly in shallow waters along the
shore.
Keywords: tintinnid; abundance; Yellow Sea
1 INTRODUCTION
Tintinnids (Ciliophora: Oligotrichida) are the best
known group of marine ciliates because of their hard
loricae. They are vigorous phytoplankton grazers
and periodically serve as food for mesozooplankton.
Tintinnids have been known since the beginning of
plankton study. However, it was not until the 1980s,
with the introduction of the microbial food loop
(Azam et al., 1983) that seasonal occurrence and
abundance of the species were extensively studied
in several stations in some estuaries, such as Bay of
Mali Ston (Krsinic, 1987a), the Eastern Adriatic
Bays (Krsinic, 1987b), Damariscotta River Estuary
(Sanders, 1987), Narragansett Bay (Verity, 1987),
Bedford Basin (Paranjape, 1987), Bay of Fundy
(Middelbrook et al., 1987), Bahia Blanca Estuary
(Barria de Cao, 1992), Admiralty Bay (Wasik and
Mikolajczyk, 1994), Buzzards Bay (Pierce and
Turner, 1994), Hiroshima Bay (Kamiyama and
Tsujino, 1996), Bay of Villefranche (Cariou et al.,
1999), Chesapeake Bay (Dolan and Gallegos, 2001),
and Nervion River estuary (Urrutxurtu, 2004).
Long-term community changes of tintinnids were
also studied at one or several stations in the coastal
waters of the Mediterranean Sea (Abboud-Abi Saad,
1989; Modigh and Castaldo, 2002) and North Irish
Sea (Graziano, 1989). Studies on the distribution of
tintinnids were also carried out along one or more
transects in neritic areas (Boltovskoy et al., 1989;
Alder and Boltovskoy, 1991a, b; Boltovskoy and
Alder, 1992; Froneman and Perissinotto, 1996;
Thompson et al., 1999, 2001; Dolan, 2000; Modigh
et al., 2003; Thompson and Alder, 2005). However,
studies on spatial distributions in a comparatively
large ocean area were scarce (Cordeiro et al., 1997).
Located between China and the Korean
Peninsula, the Yellow Sea (Fig.1) is a marginal sea
of the western Pacific. Although there have been
several literatures on the taxonomy and ecology of
tintinnid in the Bohai Gulf (Wang, 1936) and the
Jiaozhou Bay (Yin, 1952, 1957; Sun et al., 2004;
Zhang et al., 2005), reports on abundance and
spatial distribution of the species in the Yellow Sea
have remained scarce (Xu and Su, 1995). In this
paper, we report the spatial distribution of some
large tintinnids (nominally > 76 μm) in the southern
Yellow Sea in the early summers of 2000–2002 and
2004.
* Supported by China’s 863 Program (No.2006AA09Z179) and 973
Program (No.2006CB400604)
** Corresponding author: wuchangzhang@ms.qdio.ac.cn
CHIN. J. OCEANOL. LIMNOL., 26(1), 2007
82
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Fig.1 Position and isobath (m) of the study area (A) and all stations used in May and June cruises (B)
2 MATERIAL AND METHOD
Tintinnids were collected during cruises to the
southern Yellow Sea onboard R/V Beidou. Six
cruises were carried out on 13–28 June 2000, 15–25
May 2001, 11–21 June 2001, 4–10 July 2001, 3–12
June 2002 and 10-19 June 2004. The study area (Fig.
1) was in the coastal shallow waters (11–75 m) of
the southern Yellow Sea. Coastal waters around
Shidao and Subei Bank were shallower (<20 m)
than the offshore area. Stations set up for
investigation were different among the cruises. All
stations of the May and June cruises are shown in
Fig.1, while stations of July 2001 are shown in Fig.5.
Detailed information of scientific content in every
station is indicated in Figs. 2–7.
In every station, vertical temperature and salinity
were profiled by casting a SeaBird CTD system.
Water samples were taken using Rossette Niskin
water samplers. A 500 ml surface water was
processed through a GF/F filter to determine
chlorophyll a (Chl-a) concentration. The filters were
stored in darkness at –20°C. Later in the laboratory,
the GF/F filters were extracted with 90% acetone in
darkness at –20°C for 24 hours. 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).
The tintinnid samples were collected by a vertical
towing net (opening 0.1 m2, mesh size 76 μm) from
2 m above the bottom of the sea to the surface. A
flowmeter was attached at the opening of the net to
estimate filtered water volume. The samples were
fixed by formalin at a final concentration of 5%.
Back in the laboratory, the samples were settled and
concentrated to a volume of about 60 ml. To
examine tintinnids, the samples were thoroughly
mixed and then 3–10 ml was dropped into a count
chamber. Lorica of the tintinnids in the chamber
was examined and counted under a Nikon
stereomicroscope at a magnification of 50×. Species
were identified according to the shape of lorica
under an Olympus BX50 microscope with reference
to Wang (1936), Yin (1952), and Yoo et al. (1988).
3 RESULT
Surface temperature, salinity and Chl-a
concentration fell in the ranges of 13.1–24.6°C,
16.33–33.04 and 0.05–7.37 μg/L, respectively, in
the six cruises (Table 1). Generally, surface water in
deeper waters had high temperature, high salinity
and low Chl-a concentration than in shallower
waters in the cruises of May and June (Figs.2–4 and
6–7).
A total of eight species of tintinnids was
recorded:
Codonellopsis mobilis Wang, 1936
Leprotintinnus netritus Campbell, 1926
Parafavella sp.
Tintinnopsis karajacensis Brandt, 1896
T. japonica Hada, 1932
T. kiaochowensis Yin, 1957
T. butschlii Daday, 1887
T. radix Brandt, 1907
Their occurrence and maximum abundance in the
six cruises are listed in Table 1. C. mobilis was the
dominant species in all cruises. The maximum
abundance of C. mobilis was lowest (3.4 ind/L) in
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ZHANG et al.: Tintinnid spatial distribution in Yellow Sea
83
Table 1 Range of surface temperature (°C), salinity, and Chl-a concentration (μg/L) and maximum abundance (ind/L) of
tintinnids in different cruises
Cruise
T
S
Chl a
C. mobilis
Parafavella sp.
L. netritus
T. karajacensis
T. japonica
T. butschlii
T. radix
T. kiaochowensis
June 2000
18.3–21.5
31.95–32.7
0.19–0.56
34.9 (14/19)
1.2 (11/19)
R (1/19)
N
N
N
N
N
May 2001
13.1–17.9
29.65–33.04
0.05–1.39
3.4 (14/25)
N
N
N
N
N
N
N
June 2001
14.1–22.4
29.17–32.89
0.14–0.84
127.0 (23/24)
N
6.5 (4/24)
14.9 (5/24)
13.3 (5/24)
2.6 (3/24)
R (2/24)
N
July 2001
21.2–24.6
29.88–31.78
0.07–0.83
103.8 (19/19)
N
N
R (2/19)
R (2/19)
N
N
R (3/19)
June 2002
14.7–20.3
16.33–32.55
0.14–6.46
43.4 (26/30)
N
5.9 (1/30)
0.8 (4/30)
5.1 (2/30)
N
N
N
June 2004
16.5–21.2
29.56–32.39
0.10–7.37
158.2 (16/26)
N
R (2/26)
R (3/26)
R (2/26)
N
N
N
R: rarely found (< 0.1 ind/L); N: not found. Data in parentheses are the number of total stations occurred / the number of stations sampled.
Fig.2 Distributions of surface temperature (°C), salinity, Chl a concentration (μg/L) and abundance (ind/L) of
tintinnids (Codonellopsis mobilis and Parafavella sp.) in June 2000 (Dots indicate the position of sampling stations)
84
CHIN. J. OCEANOL. LIMNOL., 26(1), 2007
Vol.26
Fig.3 Distributions of surface temperature (°C), salinity, Chl a concentration (μg/L) and abundance (ind/L)
of C. mobilis in May 2001 (Dots indicate the position of sampling stations)
May 2001, and highest (158.2 ind/L) in June 2004.
Other species were within > 15 ind/L.
Except Parafavella sp. in June 2000, these
species distributed mainly in the shallow waters
along the shore. Hyaline Parafavella sp. was found
only in June 2000 in the eastern part of the study
area with maximum abundance of 1.2 ind/L in Stn.
9794 (Fig.2). There were usually two peaks of C.
mobilis in the Subei Bank and near shore water
around Shidao, respectively. And the maximum
abundance found in Subei Bank was higher than in
the shore around Shidao (Figs.2–4 and 6). Other
species was mainly found in the Subei Bank, for
example, T. karajacensis and T. japonica in June
2001 (Fig.4).
The distribution of tintinnids was patchy in their
distribution region, i.e., they occurred unevenly with
high abundance near several stations as a patch
center surrounded by areas of much lower
abundance. Although C. mobilis occurred in a large
area, the abundance varied in different stations
dramatically. For example, in the Subei Bank, in
June 2000, the maximum abundance of C. mobilis
was 34.9 ind/L in Stn. 11394. However, that in a
nearby station was only 6.9 ind/L (Stn. 9394) or <1
ind/L. In May 2001, the maximum abundance was
3.4 ind/L in Stn. 12294, surrounded by abundance <
0.5 ind/L. In June 2001, abundance center was Stn.
11194 (127.0 ind/L) and Stn. 11294 (90.6 ind/L),
while nearby stations showed less than 10 ind/L. In
June 2002, high abundance was found in Stn. 11151
(43.4 ind/L), 11194 (26.2 ind/L) and 12094 (24.9
ind/L), while other stations had abundance of < 5
ind/L. In June 2004, high abundance was 158.2 and
106.1 ind/L in Stn. 10251 and 10294, respectively.
Other stations had abundance below 60.0 ind/L.
4 DISCUSSION
Different methods have been used in the study on
tintinnid abundance. Some authors concentrated
tintinnids by settling various volumes of fixed
seawater, e.g., Barria de Cao (1992), Kamiyama and
Tsujino (1996), Krsinic (1987a, b), Sanders (1987),
Verity (1987), Paranjape (1987), Modigh and
Castaldo (2002), Sun et al. (2003), and Urrutxurtu
(2004). Some authors filtered large volumes of
water through meshes with different mesh sizes,
including 10 μm (Thompson and Alder, 2005), 15
No.1
ZHANG et al.: Tintinnid spatial distribution in Yellow Sea
85
Fig.4 Distributions of surface temperature (°C), salinity, Chl a concentration (μg/L) and abundance (ind/L) of tintinnids C.
mobilis, T. karajacensis and T. japonica in June 2001 (Dots indicate the position of sampling stations)
μm (Boltovskoy and Alder, 1992), 20 μm
(Bootovskoy et al., 1991; Pierce and Turner, 1994;
Cordeiro et al., 1997; Cariou et al., 1999; Dolan and
Gallegos, 2001), 25 μm (Graziano, 1989), 26 μm
(Boltovskoy et al., 1989; Alder and Boltovskoy,
1991b), and 15-26 μm (Alder and Boltovskoy,
1991a). Others towed nets with different mesh sizes:
30 μm (Middlebrook et al., 1987; Thompson et al.,
2001), 35 μm (Thompson et al., 1999), 50 μm
(Wasik and Mikolajczyk, 1994), 52 μm (AbboudAbi Saab, 1989), 53 μm (Krsinic, 1982; Krsinic and
Grbec, 2002), and 63 μm (Ounissi and Frehi, 1990).
The mesh size (76 μm) in this study, as well as Xu
and Su (1995), is the largest among all previous
investigations on tintinnid abundance. It should be
noted that the data in this paper did not cover an
entire community, but some large species. Water
settling method or smaller meshes will be used in
future studies.
The abundance of tintinnids was a vertically
integrated value in this study. Therefore, their
vertical distribution was ignored despite uneven
patterns revealed in some studies (Krsinic, 1982,
1987a; Verity, 1987; Paranjape, 1987; Abboud-Abi
Saab, 1989; Boltovskoy and Alder, 1992; Thompson
et al., 1999, 2001).
86
CHIN. J. OCEANOL. LIMNOL., 26(1), 2007
C. mobilis was first found in 1936 in the Bohai
Gulf, which connects the Yellow Sea and Bohai Sea
(Wang, 1936). Later, this species was found in the
Jiaozhou Bay (Yin, 1952) and Haizhou Bay (Xu and
Su, 1995). However, no abundance data were given.
The maximum abundance of C. mobilis was 11
ind/L in the Bohai Sea in April 1999 (Zhang et al.,
2004) and 800 ind/L in the Jiaozhou Bay in May
2003 (Zhang et al., 2005). At present, there is no
report on this species in other regions of world
oceans.
C. mobilis occurred in the shallow waters in the
Subei Bank and in the coastal area off Shidao. This
distribution pattern might be due to the tidal front in
the area - a transitional area between stratified water
off the coast and the mixed coastal water in summer.
Zhao (1987) determined the positions of tidal fronts
Vol.26
of the Yellow Sea in summer as shown in Fig.8.
Wei et al. (2003) and Liu et al. (2003) have
confirmed the existence of tidal fronts and studied
their role in distributing anchovy eggs, zooplankton,
and phytoplankton in several cruises in this study
region in 2000 and 2002. In this study, C. mobilis
distributed in the inshore side of the tidal front,
which might have kept C. mobilis from moving into
deep water.
C. mobilis were found in May, June, and July
2001. Lower abundance was found in May, which
may imply the beginning period of occurrence of
this species. In June, the maximum abundance was
boosted to 127.0 ind/L and stayed high at 103.8
ind/L in July. Therefore, this species stayed in the
Subei Bank for over two months and maybe even
much later after July.
Fig.5 Distributions of surface temperature (°C), salinity, Chl a concentration (μg/L) and abundance (ind/L) of C.
mobilis in July 2001 (Dots indicate the position of sampling stations)
No.1
ZHANG et al.: Tintinnid spatial distribution in Yellow Sea
Fig.6 Distributions of surface temperature (°C), salinity, Chl a concentration (μg/L) and abundance (ind/L)
of tintinnid C. mobilis in June 2002 (Dots indicate the position of sampling stations)
Fig.7 Distributions of surface temperature (°C), salinity, Chl a concentration (μg/L) and abundance (ind/L)
of tintinnid C. mobilis in June 2004 (Dots indicate the position of sampling stations)
87
88
CHIN. J. OCEANOL. LIMNOL., 26(1), 2007
Vol.26
2001) contended that tintinnid abundance is
probably related to abiotic factors rather than food
availability.
5 ACKNOWLEDGEMENT
We thank all the crew members of R/V Beidou
and Mr. H. Wang for sample collection. We are
grateful to the colleagues for sharing hydrographic
data.
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Fig. 8. Tidal fronts (zigzag lines) in the Yellow Sea in summer
(Courtesy of Zhao, 1987)
Despite the consistent occurrence and distribution
pattern of C. mobilis in the June cruises, its
maximum abundance varied significantly: 34.9,
127.0, 43.4 and 158.2 ind/L in the four June- cruises
in 2000, 2001, 2002, and 2004, respectively. A
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Other tintinnid species have been found in other
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