Acta Ecologica Sinica 33 (2013) 45–51
Contents lists available at SciVerse ScienceDirect
Acta Ecologica Sinica
journal homepage: www.elsevier.com/locate/chnaes
Abundance and biomass of planktonic ciliates in the sea area around Zhangzi
Island, Northern Yellow Sea
Yu Ying a,c,1, Zhang Wuchang a,⇑, Wang Shiwei b, Xiao Tian a
a
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
Jiaozhou Bay Marine Ecosystem Research Station, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
c
Graduate University of Chinese Academy of Sciences, Beijing 100049, China
b
a r t i c l e
i n f o
Article history:
Received 31 March 2011
Revised 27 July 2011
Accepted 20 March 2012
Keywords:
Planktonic ciliate
Abundance
Biomass
Northern Yellow Sea
Zhangzi Island
a b s t r a c t
We investigated the abundance and biomass of planktonic ciliates in the sea area around Zhangzi Island,
Northern Yellow Sea, from July 2009 to June 2010. Ciliates were sampled monthly from surface to bottom
with a 10 m depth interval at 13 sample stations along three transects. A 1 L sample of water from each
depth was collected with a 2.5 L Niskin water sampler and fixed in 1% acid Lugol’s iodine solution. Water
samples were pre-concentrated using the Utermöhl method and observed using an Olympus IX51
inverted microscope at 100 or 200x. The dimensions of the ciliates were measured and the cell volume
of each species was estimated using appropriate geometric shapes. The carbon:volume ratio used to calculate biomass was 0.19 pg C/lm3. Abundance and biomass of the ciliate in water column were calculated
as the integral of the abundance and biomass from bottom to surface, respectively. The classification of
tintinnids was based on taxonomic literature. The average abundance of non-loricate ciliates was
3066 ± 2805 ind/L, ranging from 165 ind/L (50 m depth of St. B6 in July) to 26,595 ind/L (surface of St.
C1 in September). The average biomass of non-loricate ciliates was 2.88 ± 2.68 lg C/L, ranging from
0.05 lg C/L (10 m depth of St. A6 in July) to 20.51 lg C/L (surface of St. A5 in August). The average tintinnid
abundance was 142 ± 273 ind/L, ranging from 0 ind/L (monthly) to 2756 ind/L (surface of St. A1 in July).
The average tintinnid biomass was 0.84 ± 2.19 lg C/L, ranging from 0.00 lg C/L (every month) to
37.64 lg C/L (20 m depth of St. C5 in July). The results showed that the average abundance of total ciliates
was 3208 ± 2828 ind/L, ranging from 166 ind/L (10 m depth of St. A6 in July) to 26,625 ind/L (surface of St.
C1 in September); the average biomass of total ciliates was 3.73 ± 3.55 lg C/L, ranging from 0.05 lg C/L
(10 m depth of St. A6 in July) to 38.29 lg C/L (20 m depth of St. C5 in July). Abundance and biomass were
vertically homogeneous in February, November and December, but decreased dramatically from the surface down to the bottom in other months. 23 tintinnid species were identified, 12 of which were in genus
Tintinnopsis. Tintinnid species were more abundant in February, July and August. Tintinnids occupied
6.6 ± 10.2% and 19.7 ± 23.3% of the total ciliate abundance and biomass, respectively, which increased during the warm season and at coastal stations, and decreased during the cold season and at offshore stations.
Large non-loricate ciliate species were prevalent in spring, while smaller species dominated in summer
and autumn. The average abundance of total ciliates in water column was 132 ± 72 106 ind/m2, with
increases during spring and autumn. The average biomass of total ciliates in water column was
152.57 ± 93.10 mg C/m2, with increases during spring and summer. The average abundance and biomass
of total ciliates in water column were greater at offshore stations than at coastal stations during spring and
autumn, and were lower during summer and winter. Non-loricate ciliates, tintinnids and total ciliates
showed significant positive correlation with temperature and significant negative correlation with salinity
(p < 0.01). Non-loricate ciliates and total ciliates showed significant positive correlation with Chl a concentration (p < 0.01); however, relationship between Chl a concentration and tintinnids was not significant.
Ó 2012 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
1. Introduction
Marine planktonic ciliates are a major, ubiquitous and diverse
group of protozoa. They range in size from 5 to 200 lm and are
⇑ Corresponding author.
E-mail addresses: yuyingxlf001@163.com (Y. Yu), wuchangzhang@163.com
(W. Zhang).
1
Tel.: +86 532 82898937.
divided into tintinnids and non-loricate ciliates which belong to
subclass Oligotrichia and Choreotrichia in class Spirotrichea [1].
As one of the main components of microzooplankton, ciliates are
trophic link between the microbial food web and traditional food
chain. Planktonic ciliates are consumers of pico- and nanoplankton,
and prey of mesoplankton and fish larvae [2–5]. Reports on ciliate
abundance and biomass in the China Seas could not be found until
1872-2032/$ - see front matter Ó 2012 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.chnaes.2012.12.007
46
Y. Yu et al. / Acta Ecologica Sinica 33 (2013) 45–51
1990s and now investigations have been conducted in Bohai Sea,
Yellow Sea, East China Sea and South China Sea [6]. However, studies on the annual variation of abundance and biomass of planktonic
ciliates are scarce except in the Jiaozhou Bay [7].
Located in the south of Waichangshan Islands in the Northern
Yellow Sea, Zhangzi Island is one of the most important aquaculture bases in Northern China. The average water depth in this area
is 35 m. Year round average water temperature and salinity is
11 °C and 31, respectively. This paper presents preliminary data
on annual variation of ciliate abundance and biomass in the sea
area around Zhangzi Island.
0.19 pg C/lm3 [14]. The plasma of tintinnids was assumed to occupy 30% of the lorica volume [15].
Non-loricate ciliates were divided into three size classes by cell
volume: NCI (103–104 lm3), NCII (104–105 lm3) and NCIII
(>105 lm3) [16]. Ciliate abundance and biomass in water column
were calculated as the integral of the abundance and biomass from
bottom to surface. Univariate correlation analyses were carried out
using the statistical program SPSS v16.0.
3. Results
3.1. Environmental variables
2. Materials and methods
Totally 10 cruises were carried out onboard R/V Liaochangyu Research 19 at approximately monthly interval in the sea area around
Zhangzi Island during July 2009 through June 2010 (except January
and May 2010). 13 Stations along three transects (indicated as
Transects A, B and C in Fig. 1) were visited in every cruise. Water
depth of all the stations is between 32 m and 58 m. The stations
were divided into offshore stations (depth >46 m, A6, B5, B6, C5
and C6) and coastal stations (depth <46 m, rest stations).
At each station, vertical profiles of temperature and salinity
were conducted with an AAQ1183-1F ALEC CTD. Water samples
for chemical and biological studies were collected with 2.5 L Niskin
water sampler at 10 m depth intervals, between surface and 2 m
above bottom.
A sample of 500 mL was filtered onto GF/F filters. The filters
were frozen at 20 °C and later were extracted with 90% acetone
at 20 °C in darkness 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.
Ciliate sample of 1 L from each depth were fixed with 1% acid
Lugol’s iodine solution and stored in a cool dark place until analysis. Each sample was settled for at least 24 h. The supernate was siphoned out and 150 mL sample was left. The concentrated sample
was examined and counted following the Utermöhl method [8]. A
subsample of 20 or 25 mL of the concentrated sample was settled
in Utermöhl counting chamber for 24 h and counted using an inverted microscope (Olympus IX51) at 100 or 200. Tintinnids
were identified based on their morphological characteristics in references [9–13]. The dimensions of about 30 individual cells for
each taxon were measured and average bio-volume of each taxon
was estimated from appropriate geometric shapes. Biomass values
were calculated from bio-volume, applying a conversion factor of
Surface temperature ranged from 0.33 °C (February, St. A1) to
26.13 °C (August, St. C6) with an average of 12.78 ± 8.17 °C. Surface
salinity ranged from 29.80 (June, St. B5) to 32.42 (February, St. B6),
with an average of 31.61 ± 0.57. Surface Chl a concentration ranged
from 0.00 lg/L (September, St. B3; October, St. C6) to 7.32 lg/L
(August, St. B3), with an average of 0.55 ± 0.58 lg/L.
Average surface temperature and Chl a concentration of all stations peaked in August while average surface salinity showed a
minimum in July (Fig. 2).
3.2. Ciliate abundance and biomass
3.2.1. Annual variation
Range and average of ciliate abundance and biomass during 10
cruises were in Table 1. Average ciliate abundance was
3208 ± 2828 ind/L, with a maximum of 26,625 ind/L in September
at the surface of St. C1 and a minimum of 166 ind/L in July at
10 m depth of St. A6. Average ciliate biomass was
3.73 ± 3.55 lg C/L, with a maximum of 38.29 lg C/L (Parafavella
elongata contributed 98.3% to the total ciliate biomass) in July at
20 m depth of St. C5 and a minimum of 0.05 lg C/L in July at
10 m depth of St. A6.
3.2.2. Vertical distribution
A surface or subsurface maximum of ciliate abundance was observed almost in every month (except November). Ciliate abundance was vertically homogeneous in February, November and
December, but decreased dramatically from the surface or subsurface down to the bottom in other months (Fig. 3).
Ciliate biomass showed a peak value in the surface or subsurface layer in every month. Likewise, ciliate biomass was vertically
homogeneous in February, November and December, but
39.3
Waichangshan Islands
N
43
N
Zhangzi Island
41
39.1
A1
B1
C1
B2
39
Bohai Sea
37
38.9
A3
B3
C3
A5
B5
C5
A6
B6
C6
Yellow Sea
35
117
119
121
123
E 125
38.7
122.4
122.6
Fig. 1. Locations of the sampling stations.
122.8
E
123
47
Y. Yu et al. / Acta Ecologica Sinica 33 (2013) 45–51
32.5
30
4
32
3
20
15
31.5
Chl a
Salinity
Temperature
25
5
2
31
1
10
30.5
5
0
30
0
1 2 3 4 5 6 7 8 9 10 11 12
-1
1 2 3 4 5 6 7 8 9 10 11 12
Month
1 2 3 4 5 6 7 8 9 10 11 12
Month
Month
Fig. 2. Annual variation of surface temperature (°C), salinity and Chl a concentration (lg/L).
Table 1
Variation of the abundance (ind/L) and biomass (lg C/L) of ciliates during 10 cruises.
Month
2
3
4
6
7
8
9
10
11
12
All year
Non-loricate ciliates
Tintinnids
Total ciliates
Abundance (average/
range)
Biomass (average/
range)
Abundance (average/
range)
Biomass (average/
range)
Abundance (average/
range)
Biomass (average/
range)
1676/198–5128
2645/365–15,888
3541/324–25,047
2080/197–7714
3312/165–21,599
2537/291–9179
4261/477–26,595
4438/420–8487
2628/1335–4442
3595/1785–9362
3066/165–26,595
1.82/0.19–10.17
2.88/0.47–12.88
4.24/0.48–15.86
3.04/0.49–11.04
3.07/0.05–13.39
3.51/0.10–20.51
2.51/0.16–11.32
3.71/0.18–13.05
2.11/0.60–3.70
1.96/0.85–5.82
2.88/0.05–20.51
94/0–330
205/0–935
248/0–1064
364/0–2628
194/0–2756
192/0–2049
44/0–237
32/0–278
16/0–90
31/0–97
142/0–2756
0.43/0.00–1.73
0.79/0.00–3.48
1.00/0.00–3.96
0.66/0.00–4.33
3.57/0.00–37.64
1.47/0.00–6.40
0.18/0.00–1.34
0.19/0.00–1.45
0.06/0.00–0.70
0.16/0.00–1.03
0.84/0.00–37.64
1770/380–5192
2849/715–15,888
3789/648–25,105
2444/197–9227
3506/166–24,355
2729/349–9345
4305/507–26,625
4470/525–8522
2644/1354–4442
3626/1785–9409
3208/166–26,625
2.25/0.33–10.79
3.66/0.57–13.17
5.24/0.97–16.18
3.69/0.54–14.42
6.64/0.05–38.29
4.98/0.13–21.86
2.68/0.31–12.55
3.90/0.51–13.05
2.17/0.62–3.91
2.12/0.87–6.01
3.73/0.05–38.29
Abundance
2000
4000
Abundance
6000
8000
0
0
0
-10
-10
-20
Feb.
Apr.
-30
Jul.
Depth (m)
Depth (m)
0
2000
4000
6000
8000
-20
Mar.
Jun.
-30
Aug.
Nov.
Sep.
Dec.
Oct.
Fig. 3. Vertical distribution of ciliate abundance (ind/L).
decreased dramatically from the surface or subsurface down to the
bottom in other months (Fig. 4).
3.2.3. Tintinnids
Twenty-three tintinnid species were identified, 12 of which
were in genus Tintinnopsis (Table 2). Tintinnid species were more
abundant in February (13 species), July (14 species) and August
(15 species) while less than 10 in other months. There were only
three tintinnid species in June in which Tintinnopsis sp. dominated.
Tintinnids occupied 6.6 ± 10.2% of the total ciliate abundance
with a maximum of 14.0% in June and a minimum of 0.6% in
November. Tintinnids occupied 19.7 ± 23.3% of the total ciliate
biomass with a maximum of 43.1% in July and a minimum of
2.6% in November (Fig. 5).
Percentage of tintinnids in total ciliate abundance and biomass
was higher at coastal stations than offshore stations in spring and
summer and lower in autumn and winter (Fig. 6).
3.2.4. Non-loricate ciliates
Large non-loricate ciliate species were prevalent in spring,
while smaller species dominated in summer and autumn.
NCI were the largest contributors to non-loricate ciliate abundance through the year with an average of 84.0 ± 15.7%. NCII and
48
Y. Yu et al. / Acta Ecologica Sinica 33 (2013) 45–51
Biomass
2
4
6
Biomass
8
10
0
0
0
-10
-10
-20
Feb.
Depth (m)
Depth (m)
0
2
4
Jul.
8
10
12
-20
Mar.
Jun.
Apr.
-30
6
-30
Aug.
Nov.
Sep.
Dec.
Oct.
Fig. 4. Vertical distribution of ciliate biomass (lg C/L).
NCII represented the largest biomass in February, March, April and
June instead of NCI in other months, and a maximum of 60.3% was
observed in April (Fig. 7).
Table 2
Species lists of tintinnids.
Species
Species
Amphorellopsis acuta
Codonellopsis mobilis
Eutintinnus tenuis
Helicostomella longa
Leprotintinnus simplex
Leprotintinnus nordquisti
Parafavella elongata
Ptychocylis obtusa
Ptychocylis acuta
Tintinnidium mucicola
Tintinnidium primitivum
Tintinnopsis beroidea
Tintinnopsis brasiliensis
Tintinnopsis butschlii
Tintinnopsis directa
Tintinnopsis digita
Tintinnopsis gracilis
Tintinnopsis nana
Tintinnopsis nucula
Tintinnopsis radix
Tintinnopsis rapa
Tintinnopsis tocantinensis
Tintinnus tubulosus
Percentage abundance
Percentage biomass
Percentage of tintinnids in total ciliates
abundance and biomass (%)
80
3.3. Abundance and biomass of ciliates in water column
3.3.1. Annual variation
The average abundance of total ciliates in water column was
132 ± 72 106 ind/m2, with a maximum of 180.99 106 ind/m2
in October and a minimum of 73.10 106 ind/m2 in February.
Ciliate abundance showed strong seasonal variations throughout
the year. Two peaks were observed in spring and autumn, respectively, and low values were found in summer and late winter
(Fig. 8).
Average biomass of total ciliates in water column was
152.57 ± 93.10 mg C/m2, with a maximum of 265.06 mg C/m2 in
July and a minimum of 89.25 mg C/m2 in November. Two peaks
were observed in spring and summer respectively while low values
were found in autumn and winter (Fig. 8).
3.3.2. Spatial distribution
The average abundance and biomass of total ciliates in water
column were greater at offshore stations than at coastal stations
during spring and autumn, and were lower during summer and
winter (Fig. 9).
60
40
3.4. Relationship between ciliates and environmental variables
Non-loricate ciliates, tintinnids and total ciliates showed significant positive correlation with temperature and significant negative correlation with salinity (p < 0.01). Non-loricate ciliates and
total ciliates showed significant positive correlation with Chl a concentration (p < 0.01); however, relationship between Chl a concentration and tintinnids was not significant (Table 3).
20
0
1
2
3
4
5
6
7
8
9
10
11
12
4. Discussion
Month
4.1. Annual variation
Fig. 5. Annual variation of the percentage of tintinnids in total ciliate abundance
and biomass.
NCIII contributed smaller to non-loricate ciliate abundance, with
an average of 13.7 ± 14.0% and 2.3 ± 5.8%, respectively (Fig. 7).
Percentage biomass of NCI, NCII and NCIII of non-loricate ciliates were 40.3 ± 24.8%, 38.5 ± 23.0% and 21.2 ± 25.3% respectively.
Ciliate abundance and biomass in the sea area around Zhangzi
Island were in the range of reports in other regions [17]. In the
present study, ciliate abundance showed strong seasonal variations
throughout the year with two peaks in spring and autumn, respectively. Likewise, two peaks were observed in some temperate
coastal waters, such as the Kaštela Bay [18,19], the Gulf of Maine
49
Y. Yu et al. / Acta Ecologica Sinica 33 (2013) 45–51
Offshore stations
Percentage of tintinnid biomass in total
ciliate biomass (%)
Percentage of tintinnid abundance in total
ciliate abundance (%)
Coastal stations
30
20
10
0
-10
1
2
3
4
5
6
7
8
100
80
60
40
20
0
-20
9 10 11 12
1
2
3
4
5
Month
6
7
8
9 10 11 12
Month
Fig. 6. Annual variation of the percentage of tintinnids in total ciliate abundance and biomass at costal and offshore stations.
NCII
100
100
80
80
Percentage biomass (%)
Percentage abundance (%)
NCIII
60
40
20
NCI
60
40
20
0
0
1
2
3
4
5
6
7
8
1
9 10 11 12
2
3
4
5
6
Month
7
8
9 10 11 12
Month
Fig. 7. Annual variation of percentage abundance and biomass of three different size classes of non-loricate ciliates.
450
400
250
Water column biomass
Water column abundance
300
200
150
100
350
300
250
200
150
100
50
50
0
0
1
2
3
4
5
6
7
8
9 10 11 12
Month
1
2
3
4
5
6
7
8
9 10 11 12
Month
Fig. 8. Annual variation of ciliate abundance (106 ind/m2) and biomass (mg C/m2) in water column.
[16] and the Gdańsk Basin [20]. However, in some other waters
such as the Bay of Biscay [21], Bay of Blanes [22], Chesapeake
Bay [23] and Southampton Water [24], only one peak was
observed.
In the present study, ciliate biomass showed strong seasonal
variations throughout the year with peaks in spring and summer.
Similar changes were observed in other temperate coastal waters,
such as the Gulf of Maine [16], Southampton Water [25] and the
50
Y. Yu et al. / Acta Ecologica Sinica 33 (2013) 45–51
Coastal stations
Offshore stations
500
Water column biomass
Water column abundance
400
300
200
100
0
400
300
200
100
0
1
2
3
4
5
6
7
8
9 10 11 12
Month
1
2
3
4
5
6
7
8
9 10 11 12
Month
Fig. 9. Average ciliate abundance (106 ind/m2) and biomass (mg C/m2) in water column at costal and offshore stations.
Table 3
Relationships between ciliate abundance and biomass and temperature, salinity and
Chl a concentration.
Temperature
Non-loricate ciliate
abundance
Tintinnid abundance
Total ciliate abundance
Non-loricate ciliate biomass
Tintinnid biomass
Total ciliate biomass
a
Salinity
Chl a
concentration
0.254a
0.245a
0.125a
0.043
0.247a
0.194a
0.117a
0.218a
0.293a
0.272a
0.283a
0.196a
0.334a
0.033
0.127a
0.173a
0.064
0.170a
Highly significant difference at the 0.01 level.
Kattegat [26]. However, in some other waters such as the Disko Bay
[26] and open northern Baltic Sea [27], only one peak was
observed.
In this study, peaks of ciliate abundance and biomass did not
match in time completely. Ciliate abundance was lower while ciliate biomass was higher in summer than in autumn. The higher
percentage of tintinnids in total ciliates could be responsible for
the disagreement. Since tintinnids had larger cell volume than
non-loricate ciliates, higher percentage of tintinnids could contribute higher biomass to total ciliate biomass which gave rise to higher biomass in summer than autumn.
4.2. Vertical distribution
In the present study, abundance and biomass decreased dramatically from the surface down to the bottom in most months.
This vertical variation pattern was similar to that of other temperate coastal waters, such as the Chesapeake Bay [28], Bohai Sea [29],
Ise Bay [30] and Jiaozhou Bay [31]. Such a pattern may be due to
lower water temperature and declining food availability in deeper
water [31]. Furthermore, negative geotaxis of ciliates and water
turbulence may be possible reasons [32].
4.3. Tintinnids
Twenty-three tintinnid species were identified in the present
study. Tintinnid species richness was smaller in the sea area
around Zhangzi Island than in other temperate waters, such as
the Hiroshima Bay (32 species) [33], the Kaštela Bay (35 species)
[19] and the eutrophicated part of Kaštela Bay (36 species) [18].
Tintinnids contributed to the ciliate abundance and biomass
with an average of 6.5% and 19.7%, respectively. The percentages
were smaller than other temperate waters. In the East China Sea,
tintinnids occupied <9% of the total ciliate abundance [34]. In the
open Pacific Ocean, tintinnids occupied 9–17% of the total ciliate
abundance [35]. In the Kaštela Bay, tintinnids occupied 40% and
60% of the total ciliate abundance and biomass, respectively [18].
In the present study, the percentage of tintinnids in total ciliate
abundance and biomass were higher in summer and lower in autumn. This strong seasonal variation was consistent with other
waters. Generally tintinnids dominated in total ciliates in summer
or autumn in coastal waters [36]. In the Kaštela Bay, tintinnids
occupied 65% of the total ciliate abundance in October [37]. In
the coastal waters near Antarctica, tintinnids contributed more
than half to abundance in austral summer [36].
4.4. Non-loricate ciliates
In the present study, larger species were prevalent in spring,
while smaller species dominated in summer and autumn. The seasonal change agreed with most waters, such as the Gulf of Maine
[16], the Kaštela Bay [18] and the open northern Baltic Sea [27].
However, small species dominated in spring while larger species
were prevalent in summer [37] or autumn [19] in the Kaštela Bay.
4.5. Relationship between ciliates and environmental variables
In the present study, ciliates showed significant positive correlation with temperature and significant negative correlation with
salinity, which indicated temperature and salinity may play an
important role in ciliate distribution. Such conclusion was similar
to that in other waters. In the Damariscotta River estuary, temperature was an important factor correlating with total tintinnid density. In the Kaštela Bay, salinity was more important than
temperature in affecting ciliate distribution [19].
In the present study, ciliates showed significant positive correlation with Chl a concentration. Such relationship has been observed in Southampton Water [25] and the Gulf of Naples [38].
However, in Hiroshima Bay, tintinnid abundance was associated
with the <20 lm, but not with the >20 lm size fraction of Chl a
concentration [33]. Chl a concentration was probably a poor indicator of potential ciliate food levels because ciliates are likely to
consume a limited range of phytoplankton in natural systems
[28]. Nonetheless, Chl a concentration was important in affecting
ciliate distribution in the sea area around Zhangzi Island.
Y. Yu et al. / Acta Ecologica Sinica 33 (2013) 45–51
Acknowledgements
We are grateful to Jianhong Xu and staff of R/V Liaochangyu Research 19 for help with sampling.
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