Journal of Oceanology and Limnology

Vol. 36 No. 5, P. 1655-1670, 2018

https://doi.org/10.1007/s00343-018-7099-4

Zooplankton community structure, abundance and biovolume

in Jiaozhou Bay and the adjacent coastal Yellow Sea during
summers of 2005–2012: relationships with increasing water
temperature*

WANG Weicheng (王卫成)1, 3, SUN Song (孙松)1, 2, 3, 4, **, ZHANG Fang (张芳)1, 3, 4,
SUN Xiaoxia (孙晓霞)2, 3, 4, ZHANG Guangtao (张光涛)2, 3, 4
1
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences,
Qingdao 266071, China
2
Jiaozhou Bay Marine Ecosystem Research Station, Chinese Academy of Sciences, Qingdao 266071, China
3
University of Chinese Academy of Sciences, Beijing 100049, China
4
Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology,
Qingdao 266071, China

Received Mar. 27, 2017; accepted in principle Jul. 25, 2017; accepted for publication Oct. 26, 2017
© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract Zooplankton abundance, biovolume and taxonomic composition in Jiaozhou Bay and the
adjacent coastal Yellow Sea were evaluated using ZooScan measurement of samples collected by net towing
every August from 2005 to 2012. Zooplankton abundance and biovolume ranged from 1 938.5 to 24 800 ind./
m3 and 70.8 to 1 480.1 mm3/m3 in Jiaozhou Bay and 73.1 to 16 814.3 ind./m3 and 19.6 to 640.7 mm3/m3 in
the coastal Yellow Sea. Copepods were the most abundant group in both regions, followed by Noctiluca
scintillans and appendicularians in Jiaohzou Bay, and chaetognaths and Noctiluca scintillans in adjacent
coastal Yellow Sea. Over the study period, the most conspicuous hydrographic change was an increase in
water temperature. Meanwhile, a general decrease in zooplankton abundance was observed, particularly in
copepod populations. Based on redundancy analysis (RDA), the warming trend was the key environmental
factor influencing to decrease of copepod abundance. The proportion of small-sized copepods increased
while the mean size of all copepods decreased, in significant correlation with water temperature. Our results
indicate that zooplankton, particularly copepods, are highly sensitive to change in water temperature, which
is consistent with predicted impacts of warming on aquatic ectotherms. Due to their dominance in the
zooplankton, the decline in copepod size and abundance could lead to an unfavourable decrease in energy
availability for predators, particularly planktivorous fish.

Keyword: copepod; abundance; body size; ZooScan; temperature; northwestern Yellow Sea

1 INTRODUCTION biogeochemical cycles in the ocean (Dam et al.,

1995). Because zooplankton are ectotherms with
Global warming is considered to be one of the most short life cycles that allow for fast response to
important factors for future changes in marine stressors through phenotypic plasticity or evolutionary
ecosystems (Mackas et al., 2012), and its effects are a
fundamental area of research. Zooplankton are
undoubtedly the most abundant metazoans on Earth, * Supported by the State Key Program of National Natural Science
playing pivotal roles in the transfer of energy from Foundation of China (No. 41230963), the NSFC-Shandong Joint Fund for
Marine Ecology and Environmental Sciences (No. U1606404), and the
primary producers and the microbial food web to Strategic Priority Research Program of the Chinese Academy of Sciences
upper trophic levels (Sherr and Sherr, 2009). (No. XDA11020305) to SUN Song
Zooplankton also play an important role in ** Corresponding author: [email protected]
1656 J. OCEANOL. LIMNOL., 36(5), 2018 Vol. 36

adaptation, they are considered as sentinels for the variability of zooplankton in Jiaohzou Bay are of
response of the oceanic biota to climate change (Hays coarse even fewer and did not allow to evidence
et al., 2005; Dam, 2013). fluctuations at larger time scales. Considering the
In recent decades, scientific knowledge on marine strategic situation of Jiaozhou Bay in northeast
ecosystem responses to global warming has China (Zhang et al., 2015), the lack of long time
significantly increased (Roemmich and McGowan, series of zooplankton in the area motivated the
1995; Wernberg et al., 2011; Lewandowska et al., present study.
2014; Chiba et al., 2015), with many investigators Seawater temperature has a warming rate of
finding that global warming could impact zooplankton 0.023°C/a between the 1960s and 2009 in Jiaozhou
community structure. In the Sevastopol Coast in the Bay, consistent with rising northern hemisphere
Black Sea, species richness of copepods decreased temperature (NHT) (Sun et al., 2012). Similar trends
between 1976 and 1990, and community structure has have also been reported in adjacent coastal seas, such
changed as well due to the increasing of warm-water as the Bohai Sea (Lin et al., 2001; Ning et al., 2010)
species Acartia tonsa and sharp decreasing of the and Yellow Sea (Lin et al., 2005; Kang et al., 2007).
cold-water species Pseudocalanus elongatus In this study, we found that summer water temperature
(Gubanova et al., 2001). In the Northeast Atlantic, the increased from 2005 to 2012 in Jiaozhou Bay and the
diversity of calanoid copepods has significantly adjacent coastal Yellow Sea. Given this trend, we
increased due to increase of sea surface temperature sought to investigate the following objectives: (1) to
(SST) in the western European basin (Beaugrand and study the summer zooplankton community structure
Ibañez, 2002). During this process, zooplankton size in the northwestern Yellow Sea, and (2) to test whether
also changed, with a shift in diversity as small warm- changes observed in copepods are consistent with
water species were gained and larger cool water predictions of the effects of warming on ectotherms
species were lost. Daufresne et al. (2009) proposed (Daufresne et al., 2009).
that long-term warming will result in a general
decrease in the size of marine ectotherms by 2 MATERIAL AND METHOD
decreasing individual mean size and/or increasing
2.1 Zooplankton sampling
abundance of smaller copepods species. Long-term
data series are essential to understand such changes Zooplankton samples were collected using
(Suikkanen et al., 2013). vertical tows of a conical plankton net with total
Jiaozhou Bay is a eutrophic semi-enclosed bay length of 140 cm, ring diameter of 31.6 cm and mesh
situated in the western part of the Shandong size of 160 μm, from the demersal to the surface at
Peninsula, China. It is surrounded by Qingdao City two different sampling points. These included
(population 9×106), with an area of 374 km2 and an Station 5 (36°06′00″N, 120°15′00″E) in Jiaozhou
average water depth of about 7 m. The bay mouth Bay with an average depth of 15.4 m, and Station 10
narrows to 2.5 km and connects the bay with the (35°59′00″N, 120°25′30″E) in the coastal Yellow
South Yellow Sea, which is a traditionally productive Sea in the vicinity of the mouth of Jiaozhou Bay
fishing ground as well as a spawning and nursery with an average depth of 17.4 m. Samples were
area for local fish populations (Jin et al., 2010; Tang collected yearly in mid-August from 2005 to 2012
et al., 2016). Previous studies on zooplankton have (Table 1, Fig.1). After collection, samples were
mainly focused on spatial distribution and population preserved immediately in 5% neutral formaldehyde
dynamics (Zhang et al., 2009; Liu et al., 2011; Sun et seawater solution.
al., 2011a; Wang and Sun, 2015), while their At each station, vertical temperature and salinity
community structure has been studied only rarely. profiles were recorded by a CTD instrument (CTG
Because of individual body size was different across MiniPack CTD-F in 2005–2007, ALEC AAQ 1183-
taxonomic groups and between various life stages of 1F CTD in 2008–2012). Column temperature and
the same species, community composition salinity means were obtained from surface, 5 m, 10 m
assessments may differ between abundance and and bottom measures. Chlorophyll a concentrations
biovolume. Thus, combined consideration of were determined fluorometrically using a Turner
abundance and biovolume together are recommended Designs model-10 fluorometer (Parsons et al., 1984)
for assessing the zooplankton community (Dai et al., for seawater taken with a rosette sampler near the
2016a). Furthermore, studies describing the time surface.
No.5 WANG et al.: Zooplankton community structure, abundance and biovolume 1657

N Table 1 Water depth and sampling times/dates at the

36.25°
sampling stations
36.20°
Data Time Water Bottom
Station
36.15° Jiaozhou Bay (dd/mm/yyyy) (hh:mm–hh:mm) depth (m) depth (m)

36.10° 5 Qingdao 18/08/2005 10:15–10:45 15.4 13.0

○
16/08/2006 11:10–11:35 17.0 15.0
36.05°
15/08/2007 14:25–14:50 15.8 14.5
36.00° 10
10/08/2008 09:20–09:50 15.0 13.0
35.95° Station 5
Yellow Sea 13/08/2009 13:55–14:11 14.3 13.0
35.90° 14/08/2010 13:18–13:43 13.1 11.0
35.85° 11/08/2011 13:25–14:00 15.7 14.0
16/08/2012 15:00–15:30 16.7 14.5
120.05° 120.15° 120.25° 120.35° 120.45° E 120.55°
16/08/2005 10:20–10:45 16.8 14.0
Fig.1 Location of sampling stations 5 and 10 in Jiaozhou 15/08/2006 10:10–10:30 18.0 16.0
Bay and the coastal Yellow Sea
15/08/2007 09:30–09:55 18.0 16.5
09/08/2008 10:15–10:40 17.0 15.0
2.2 Zooplankton analysis Station 10
13/08/2009 10:00–10:17 17.1 15.0

Preserved zooplankton samples were subjected to 13/08/2010 10:55–11:22 16.0 13.0

image analysis using a semi-automatic ZooScan 10/08/2011 10:50–11:25 16.0 14.0

system (http://www.zooscan.com). In the laboratory, 15/08/2012 12:10–12:40 20.0 18.0
a fraction of each plankton sample was obtained with
Bottom depth was the depth of vertical tows.
a Motoda box splitter (Motoda, 1959). Subsamples,
usually between 1/4 and 1/64 of the original samples, 4 Major Minor 2
( )( )( ) ,
were scanned in a scanning cell with a transparent 3 2 2
frame (11 cm×24 cm) and digitized at 4 800 dpi while for Noctiluca, volume (mm3) was also
following the scanning protocol (Schultes and Lopes, determined assuming that the cells are spherical. This
2009). After processing the samples with ZooProcess, was calculated as
the detected objects were automatically classified
4 ESD 3
according to a learning set, and corrections were ( )( ),
3 2
made manually (Grosjean et al., 2004; Gorsky et al.,
2010). By default, only objects having an equivalent where the net volume can be obtained by multiplying
spherical diameter (ESD) of >300 μm were detected the area of net mouth and the vertical distance that the
and processed. Zooplankton taxonomic groups were net was towed, the Major, Minor and ESD (μm) of
identified through the ZooScan system. Based on this each object were provided by ZooScan.
dataset, we divided total copepods into two different
2.3 Data analysis
ESD-based body sizes, S1 (300–500 μm) and S2
(>500 μm). Yearly differences in environmental variables
Abundance (ind./m3) of total zooplankton in each (temperature, salinity and Chl α) were compared
taxonomic group was calculated using the following using one-way analysis of variance (ANOVA), and
equation: difference in variables between the two sampling
Abundance=number of zooplankton(splitting/net stations were analysed by t-test.
volume). Redundancy analysis (RDA) was used to assess
Zooplankton biovolume (mm3/m3) was calculated relationships between zooplankton abundance and
as follows: environmental variables, and was performed using
Biovolume=volume of zooplankton individuals CANOCO software version 5 (Microcomputer Power,
(splitting/net volume). USA). The zooplankton species data are analysed
Zooplankton volume (mm3) for all taxa except using detrended correspondence analysis (DCA) to
Noctiluca scintillans was approximately equal to identify the ordination methods (Hill and Gauch,
ellipsoidal volume, and was calculated as 1980). If the maximum gradient length of the four
1658 J. OCEANOL. LIMNOL., 36(5), 2018 Vol. 36

a. Temperature (°C) b. Salinity

0 0

32
29
31
28
5 5 29
27

Depth (m)
Depth (m)

27
26

25 26

24 24
10 10
23 23

22
21

2005 2006 2007 2008 2009 2010 2011 2012 2005 2006 2007 2008 2009 2010 2011 2012
Year Year
c. Temperature (°C) d. Salinity
0 0

32
26

25
31
5 24 5
Depth (m)

Depth (m)

23
30
22

21
29
10 20
10
19

18 28

2005 2006 2007 2008 2009 2010 2011 2012 2005 2006 2007 2008 2009 2010 2011 2012
Year Year

Fig.2 Vertical profiles of temperature and salinity at both sampling stations in August 2005–2012
Station 5: (a) and (b); station 10: (c) and (d).

axes is lower than 3, redundancy analysis (RDA) is 3 RESULT

recommended (Peng et al., 2012). Zooplankton
3.1 Hydrography
abundance values and environmental variables were
transformed as log(x+1) to stabilize variance and Between 2005 and 2012, temperature decreased
normalize data distributions. relative to increasing depth at the two sampling
Linear regression was applied to evaluate the stations (Fig.2a, c). Surface temperature fluctuated
relationship between average total volume of between 25.1 and 28.0°C, and 23.9 and 26.5°C at
copepods and water temperature. stations 5 and 10, respectively, and reached low points
No.5 WANG et al.: Zooplankton community structure, abundance and biovolume 1659

27 a 16
Station 5
Station 10
26

Chlorophyll a (μg/L)
12
Temperature (℃)

25
8

24
4

23
0
2005 2006 2007 2008 2009 2010 2011 2012
22 Year
2004 2005 2006 2007 2008 2009 2010 2011 2012
Year Fig.4 Interannual variation in sea surface chlorophyll α
(μg/L) at both sampling stations in August 2005–2012.
32 b
of 22.5 and 18.4°C at bottom depth in 2005. Average
30
water column temperature ranged from 23.3 to 26.4°C
28
(Fig.3a), and 22.1 to 26.2°C (Fig.3c) at stations 5 and
Salinity

10, respectively. Significant temperature differences

26 among the years were clearly observed at both stations
(ANOVA, station 5: P=0.003; station 10: P=0.05).
24 The period of 2005–2012 exhibited an overall
warming trend despite 2011 as an outlier. The year
22
2004 2005 2006 2007 2008 2009 2010 2011 2012 2012 was the warmest year of the sampling period.
Year Conversely, salinity increased with increasing
depth (Fig.2b, d). Salinity varied from 19.8 to 30.8,
27 c and 29.0 to 31.2 on the surface, and reached 28.1 and
26 29.2 at the bottom depth at stations 5 and 10,
respectively. Average water column salinities ranged
25
Temperature (℃)

from 25.7 to 30.8 (Fig.3b), and from 29.1 to 31.2

24 (Fig.3d) at stations 5 and 10, respectively. Salinity
23 also showed significant interannual variation
(ANOVA, station 5: P=0.001; station 10, P<0.001),
22
with the lowest value in 2007, an increasing trend was
21 only observed at station 5.
20 Chl α concentrations varied among years (Fig.4),
2004 2005 2006 2007 2008 2009 2010 2011 2012
Year
with a maximum in 2008 (station 5: 12.6 μg/L; station
10: 5.2 μg/L) and minima in 2009 at station 5
32 d (0.7 μg/L) and in 2007 at station 10 (0.3 μg/L).

3.2 Zooplankton abundance, biovolume and

31
taxonomic composition
Salinity

30
During the study period, zooplankton abundance
and biovolume ranged from 1 938.5 to 24 800 ind./m3
and 70.8 to 1 480.1 mm3/m3 at station 5 and 73.1 to
29
16 914.3 ind./m3 and 19.6 to 640.7 mm3/m3 at station
10 (Tables 2, 3). Generally, both zooplankton
28 abundance and biovolume at station 5, were higher
2004 2005 2006 2007 2008 2009 2010 2011 2012
Year than at station 10.
Twelve diverse zooplankton taxonomic groups
Fig.3 Interannual variation in water column averaged
temperature and salinity at both sampling stations in were observed in total: appendicularians, bivalve
August 2005–2012 larvae, chaetognaths, cladocerans, copepods, decapod
Station 5: (a) and (b); station 10: (c) and (d). Vertical bars show SE. larvae, echinoderm larvae, medusae, polychaete
1660 J. OCEANOL. LIMNOL., 36(5), 2018 Vol. 36

Table 2 Abundance and biovolume of established zooplankton taxonomic categories averaged across all cruises at station 5
in August 2005–2012
Abundance (ind./m3) Biovolume (mm3/m3)
Category
Range Mean±SE Range Mean±SE
Copepods 1 884.6–13 569.2 4 877.3±1 444.4 40.1–921.6 238.2±105.5
Appendicularians 0–855.2 325.5±128.7 0–21.7 8.1±3.3
Chaetognaths 57.1–373.3 251.8±37.6 17.9–209.7 116.9±24.6
Medusae 0–1 538.5 256.3±186.2 0–65.1 19.2±9.4
Noctiluca scintillans 0–8 400.0 1 170.1±1 036.7 0–264.6 36.2±32.7
Cladocerans 0–123.1 42.6±20.9 0–9.7 2.0±1.2
Nauplius larvae 0–114.3 50.5±13.8 0–2.34 1.0±0.3
Polychaete larvae 0–153.9 72.3±17.5 0–9.2 3.4±1.2
Bivalve larvae 0–90.9 50.5±11.9 0–2.8 1.3±0.3
Echinoderm larvae 0–171.4 60.6±28.3 0–5.6 1.8±0.9
Decapod larvae 30.8–236.4 106.6±25.2 1.1–53.4 26.0±7.0
Other zooplankton 0–110.3 26.1±15.5 0–119.3 16.2±14.8
Total zooplankton 1 938.5–24 800.0 7 290.1±2 669.9 70.8–1 480.1 470.2±162.3

Table 3 Abundance and biovolume of established zooplankton taxonomic categories averaged across all cruises at station 10
in August 2005–2012
Abundance (ind./m3) Biovolume (mm3/m3)
Category
Range Mean±SE Range Mean±SE
Copepods 65.4–1 3171.4 3 774.9±1 468.3 1.7–434.7 120.1±49.11
Appendicularians 0–800.0 193.2±98.1 0–11.3 3.7±1.6
Chaetognaths 7.7–800.0 253.3±90.6 11.8–466.2 84.8±54.9
Medusae 0–285.7 55.9±35.0 0–10.2 2.4±1.4
Noctiluca scintillans 0–1 200.0 221.3±144.2 0–32.6 6.2±3.9
Cladocerans 0–693.3 157.7±94.5 0–22.2 6.0±3.4
Nauplius larvae 0–262.5 77.8±34.5 0–5.3 1.6±0.7
Polychaete larvae 0–213.3 79.6±29.7 0–13.9 3.5±1.7
Bivalve larvae 0–57.1 22.2±9.0 0–1.4 0.5±0.2
Echinoderm larvae 0–114.3 28.1±12.7 0–9.2 1.9±1.1
Decapod larvae 0–228.6 98.7±30.4 0–41.9 19.5±5.9
Other zooplankton 0–100.0 32.2±11.9 0–4.2 1.1±0.5
Total zooplankton 73.1–16 914.3 4 994.9±1 864.4 19.6–640.7 251.4±86.7

larvae, nauplius larvae, Noctiluca scintillans and abundance at stations 5 and 10, respectively. In this
other zooplankton (Figs.5, 6). Copepods were the study, meroplankton comprised bivalve larvae,
most abundant zooplankton group, comprising 66.9% decapod larvae, echinoderm larvae and polychaete
of total abundance at station 5 and 75.6% at station larvae, and accounted for 4.0% and 4.6% of the total
10, followed by N. scintillans (16.1%) at station 5 and abundance at stations 5 and 10. Copepods dominated
chaetognaths (5.1%) at station 10. Appendicularians zooplankton biovolume, making up 50.7% of the total
were the next most abundant group, comprising 4.5% at station 5 and 47.8% of the volume at station 10.
at station 5 and 3.9% at station 10. Gelatinous These were followed by chaetognaths, making up
zooplankton are generally considered to include 24.9% at station 5 and 33.7% at station 10, then N.
appendicularians, chaetognaths and medusae, scintillans at station 5 making up 7.7%, and decapod
together accounting for 11.5% and 10.1% of the total larvae at station 10 making up 7.8%.
No.5 WANG et al.: Zooplankton community structure, abundance and biovolume 1661

0.8% 0.7% 0.4% 3.2%

a 0.7% b 0.6%
1.6% 0.6%
0.6% 1.6%
1.0%
1.5% 0.4% 2.0%

3.5% 1.1%
5.1%
3.5%
4.5% 3.9%

4.4%
16.1%

66.9% 75.6%

Copepods Noctiluca scintillans Appendicularians Chaetognaths

Medusae Decapod larvae Polychaete larvae Echinoderm larvae
Bivalve larvae Nauplius larvae Cladocerans Other zooplankton

Fig.5 Relative abundance of zooplankton taxonomic groups averaged across all cruises at two sampling locations in late
summer 2005–2012
a. station 5; b. station 10.

0.7% 0.4% 7.8% 1.4% 0.8%

a 5.5% 0.3% b
4.1% 0.2% 1.0% 0.2% 0.6%
0.4% 2.4%
3.5% 33.7% 0.4%
24.9%

50.7%

1.7%
47.8%

7.7% 1.5%
2.5%

Copepods Noctiluca scintillans Appendicularians Chaetognaths

Medusae Decapod larvae Polychaete larvae Echinoderm larvae
Bivalve larvae Nauplius larvae Cladocerans Other zooplankton

Fig.6 Relative biovolume of different zooplankton taxonomic groups averaged across all cruises at two stations in late
summer 2005–2012
a. station 5; b. station 10.

3.3 Zooplankton variability appendicularians and medusae, which clearly declined

over the course of the study. Large population
We observed year to year variability in the main numbers (>4 900 ind./m3 for copepods, >250 ind./m3
groups of zooplankton (Figs.7, 8), characterised by an for appendicularians and >200 ind./m3 for medusae)
overall decrease in abundance and biovolume for occurring in 2005–2007 did not reappear between
some groups from 2005 to 2012. This decrease was 2008 and 2012 at either sampling station. N. scintillans
particularly evident in the populations of copepods, also exhibited a decreasing trend with the largest cell
1662 J. OCEANOL. LIMNOL., 36(5), 2018 Vol. 36

15000 a Station 5 15000 Station 10

10000 10000

5000 5000

0 0
9000 b 9000

6000 6000

3000 3000

0 0
1000 c 1000

750 750

500 500
Abundance (ind./m3)

250 250

0 0
1000 d 1000

750 750

500 500

250 250

0 0
2000 e 2000

1500 1500

1000 1000

500 500

0 0
600 600
f

400 400

200 200

0 0
05 06 07 08 09 10 11 12 05 06 07 08 09 10 11 12
Time (Year) Time (Year)

Fig.7 Interannual variability in abundance (ind./m3) of zooplankton groups in August 2005–2012

a. copepods; b. Noctiluca scintillans; c. appendicularians; d. chaetognaths; e. medusae; f. meroplankton. Left panel: station 5; right panel: station 10.
No.5 WANG et al.: Zooplankton community structure, abundance and biovolume 1663

1000 a 1000
Station 5 Station 10

750 750

500 500

250 250

0 0
400 400
b

300 300

200 200

100 100

0 0
30 30
c

20 20
Biovolume (mm3/m3)

10 10

0 0
600 600
d

400 400

200 200

0 0
80 e 80

60 60

40 40

20 20

0 0
80 f 80

60 60

40 40

20 20

0 0
05 06 07 08 09 10 11 12 05 06 07 08 09 10 11 12
Time (Year) Time (Year)

Fig.8 Interannual variability in biovolume (mm3/m3) of zooplankton groups in August 2005–2012

a. copepods; b. Noctiluca scintillans; c. appendicularians; d. chaetognaths; e. medusae; f. meroplankton. Left panel: station 5; right panel: station 10.
1664 J. OCEANOL. LIMNOL., 36(5), 2018 Vol. 36

1.0 1.0 Chl a

Chl a 08 08
a b

Poly
Cope
Medu
Echi Poly
12
Echi 11 Naup
06
SAT 11 Appe 07 09 SAS Chae
Deca
Chae
Axis 2

Axis 2
Biva
Noct
05 Cope 05
Clad Appe
Biva Medu
Clad
SAT
SAS Deca Noct
10 06 12 10
Naup
09
07

-1.0 -1.0
-1.0 Axis 1 1.0 -1.0 Axis 1 1.0

Fig.9 Biplot of zooplankton groups (response variables) and environmental factors (explanatory variables) on the space
formed by the two first axis of the RDA for the data set of abundance
Cope: copepods; Appe: appendicularians; Chae: chaetognaths; Medu: medusae; Noct: Noctiluca scintillans; Clad: cladocerans; Naup: nauplius larvae;
Poly: polychaete larvae; Biva: bivalve larvae; Echi: echinoderm larvae; Deca: Decapod larvae; SAT: sea average temperature; SAS: sea average
salinity; Chl α: chlorophyll α. Circles represent years from 2005 to 2012. a. station 5; b. station 10.

10000 a density in 2005. Chaetognaths and meroplankton

S1 S2
showed a fluctuation during the study period, while
8000
an increasing trend was observed in pluteus (53.3 ind./
Abundance (ind./m3)

6000
m3 in 2006, 15.4 ind./m3 in 2008, 85.7 ind./m3 in 2011
and 137.9 ind./m3 in 2012) in Jiaozhou Bay. The
4000 highest abundance (114.3 ind./m3) of pluteus has been
observed in 2011 in coastal Yellow Sea. Biovolume of
2000 each zooplankton group was correlated with its
abundance, and exhibited a similar variability (Fig.8).
0
2005 2006 2007 2008 2009 2010 2011 2012
RDA results are displayed in ordination plots for
Year both stations (Fig.9). At station 5, abundance of
copepods, N. scintillans, bivalve larvae and decapod
12000 b larvae were correlated negatively with water
S1 S2
temperature, while echinoderm larvae were positively
10000
correlated with water temperature and Chl α.
Abundance (ind./m3)

8000 Medusae, appendicularians and polychaete larvae

were negatively correlated with salinity. At station 10,
6000
medusae, appendicularians and N. scintillans were
4000 negatively related with salinity, and copepods,
nauplius larvae, polychaete larvae, bivalve larvae and
2000
decapod larvae negatively associated with
0 temperature.
2005 2006 2007 2008 2009 2010 2011 2012
Year In the case of copepods, the abundance of size rank
Fig.10 Interannual variation in the abundance of two
S1 (300–500 μm) was generally higher than that of
copepod size classes (S1: 300–500 μm and S2: size rank S2 (>500 μm), and the abundances of both
>500 μm) in late summer 2005–2012 size ranks showed a decreasing trend at either station
a. station 5; b. station 10. (Fig.10). In addition, we found that the relative
No.5 WANG et al.: Zooplankton community structure, abundance and biovolume 1665

100 a 0.08 a
S1 S2 V=-0.012T+0.35
05 R²=0.66, P=0.026
Ratio in abundance (%)

80
0.06

Volume (mm3)
06
60
08 07
0.04
11 12
40 ( )
09 10
0.02
20

0.00
0 23 24 25 26 27
2005 2006 2007 2008 2009 2010 2011 2012
Temperature (℃)
Year

100 b S1 S2 0.05 b V=-0.004T+0.13

R²=0.54, P=0.032
Ratio in abundance (%)

80 0.04
05 07
08

Volume (mm3)
60 06
0.03
11
09 10
40 0.02
12
20 0.01

0 0.00
2005 2006 2007 2008 2009 2010 2011 2012 21 22 23 24 25 26 27
Year Temperature (℃)

Fig.11 Interannual variation in the abundance ratio of Fig.12 Average volume (V, mm3) of copepods in relation
two size classes (S1: 300–500 μm and S2: >500 μm) to water column average temperature (T, °C) in
in the abundance of total copepods in late summer August from 2005 to 2012
2005–2012 a. station 5; b. station 10.
a. station 5; b. station 10.

abundance of size rank S1 significantly increased, summer zooplankton community in the northwestern
while that of size rank S2 significantly decreased at Yellow Sea. In both regions, copepods were the most
both sampling stations (Fig.11). At the same time, the abundant group, accounting for a large proportion of
average volume of copepods decreased. A statistically total zooplankton (66.9% and 75.6% at stations 5 and
significant relationship was found between the 10, respectively). Moreover, copepods also comprised
average volume of copepods and water temperature about half of the total biovolume (50.7% and 47.8%
(station 5: R2=0.66, P=0.026; station 10: R2=0.54, at stations 5 and 10), which reflects their community
P=0.032) (Fig.12). dominance in this region. Our results are in the 50%–
80% range reported for copepods in many marine
4 DISCUSSION ecosystems (Wickstead, 1976). N. scintillans also
made up considerable abundance, especially in
4.1 Zooplankton abundance, biovolume and
Jiaozhou Bay (16.1%, Fig.5a). We also found that
taxonomic composition
chaetognaths ranked second in total biovolume, in
The abundance and biovolume of zooplankton in keeping with previous reports by Ishizaka et al.
Jiaozhou Bay and the adjacent Yellow Sea were (1997). In Jiaozhou Bay, copepods, N. scintillans and
calculated in this study. These values were consistently appendicularians were the top three dominant
higher at station 5 than at station 10, and both were taxonomic groups based on abundance, while
within range of the reported abundance and biovolume chaetognaths were a dominant taxonomic group
in the coast of South Yellow Sea (Dai et al., 2016b). based on biovolume. In the adjacent coastal Yellow
The high abundance and low biovolume of Sea, copepods, chaetognaths and meroplankton
zooplankton in the present study area, in comparison dominate the zooplankton based on both abundance
to geographically similar areas in the Northwest and biovolume. As evidenced by this ranking,
Pacific (Sato et al., 2015), indicates a dominance of meroplankton also occupied a very important position
small-sized species in the zooplankton community. in the coastal ecosystem in summer, but have often
Our data provide basic information about the been ignored in prior investigations.
1666 J. OCEANOL. LIMNOL., 36(5), 2018 Vol. 36

4.2 The relationship between zooplankton are recognized as predators feeding mostly on
community and water temperature microzooplankton, mesozooplankton and fish larvae.
By analysing the distribution patterns of zooplankton
A decreasing inter-annual trend was observed in functional groups in the South Yellow Sea, Shi et al.
both zooplankton abundance and biovolume, reflected (2015) found that medusae were mainly distributed in
in the major taxa including copepods. Copepod coastal waters, concurrent with small copepods.
abundance was negatively correlated with water Therefore, a decrease in copepod abundance may
temperature in both regions (Fig.9), suggesting that a cause fluctuation in medusozoan populations. In our
progressive depletion in zooplankton could be a studied regions, Sagitta crassa is the only chaetognaths
response to the warming trend. Similar results were species occurring in summer (Sun et al., 2008; Wang
found during a 30-year study from 1959 to 1992 in et al., 2010), has a wide survival temperature and
the Bohai Sea (Tang et al., 2003). We also found that salinity range (0–28°C and 9.3–48.7, respectively)
the proportion of small-sized copepods increased and (Liu et al., 2007), which includes the range in our
the mean size of all copepods was reduced during our study period. S. crassa mainly feeds on copepods and
study period, in close relationship with temperature zooplankton larvae. In Jiaozhou Bay, the lowest
(Fig.12). Our results were consistent with predictions feeding pressures of S. crassa on zooplankton biomass
of the effects of warming on ectotherms (Daufresne et and production (0.08% and 2.48%) were recorded in
al., 2009). summer (Wang et al., 2010), indicating food items
In Jiaozhou Bay and the adjacent coastal Yellow were abundant for S. crassa. Thus, as shown in our
Sea, the summer copepod community was comprised results chaetognaths exhibited a fluctuation.
mainly of a few species considered to be main Oikopleura dioica is the only appendicularian species
secondary producers, including Paracalanus parvus, that occurred (Sun et al., 2008), and can quickly
Acartia bifilosa, Acartia pacifica, Oithona brevicornis respond to environmental change. For example, the
and Calanus sinicus (Sun et al., 2008). Many studies lowest salinity during our study was observed in the
have found that the embryonic development and summer of 2007 after heavy rains (270 mm in one
survival of C. sinicus are optimised below 20°C day), coincident with a high abundance of
(Huang and Zheng, 1986; Uye, 1988). During our appendicularians (Figs.7c, 8c). Furthermore, we
study, water temperature in August was generally found that the abundance of appendicularians was
higher (Fig.2a, c), likely affecting the growth and negatively correlated with salinity over the course of
population of C. sinicus, Acartia, Oithona and the study (Fig.9). Similar results have previously
Paracalanus. Copepods have also been shown lower reported in other coastal waters. In the Seto Inland
abundance at warmer ambient temperature in Sea, Japan, low salinity and nutrient-rich waters were
laboratory experiments, particularly as adults (Garzke introduced to the surface layer in the aftermath of
et al., 2015). typhoon rains, causing a bloom of appendicularians
Noctiluca scintillans is a large-sized heterotrophic (Nakamura, 1998). Similarly, in southern Kaneohe
and omnivorous dinoflagellate, frequently blooms Bay, Hawaii, appendicularians exhibited the most
massively in spring and early summer in temperate dramatic response to a major runoff event, with
coastal waters (Harrison et al., 2011). Many studies biomass increasing six-fold in one day (Hoover et al.,
have reported that temperature is the limiting factor 2006).
for the growth of N. scintillans in summer, and it was Meroplankton occupied a very important position
probably due to high water temperatures since its in the coastal ecosystem, and was considered to be
growth rate drastically decreased when water more sensitive than holozooplankton in response to
temperature above 25°C (Huang and Qi, 1997; Tada climate change (Edwards and Richardson, 2004;
et al., 2004; Dela-Cruz et al., 2008). N. scintillans in Hays et al., 2005). In North Sea, an increased
this study was negative correlated with water abundance of the larvae of a benthic echinoderm,
temperature (Fig.9a), and the highest abundance was Echinocardium cordatum, was recorded (Lindley and
recorded with the lowest temperature in 2005 (Fig.7b). Batten, 2002). Kirby et al. (2007) proposed that
Gelatinous zooplankton are generally considered warmer conditions in the North Sea after 1987,
to include medusae, chaetognaths and together with increased phytoplankton, may act
appendicularians, comprising more than 10% of the synergistically to increase the reproduction output
total abundance in our studied areas (Fig.5). Medusae and population density of this species. In present
No.5 WANG et al.: Zooplankton community structure, abundance and biovolume 1667

study, an increasing abundance of pluteus (a larva of adult Acartia sp. decreased by 123 μm when raised at
echinoderm) was registered, which was positive with 17.5°C instead of 9.5°C (Garzke et al., 2015).
water temperature and Chl a (Fig.9a). In Jiaozhou Apart from these direct effects, increasing
Bay, increased temperature was reported, particularly temperature may have indirect effects on copepod
in winter and spring (Sun et al., 2012); this would size by affecting the quality of their food. Previous
enhance individual fecundity and reduce mortality mesocosm studies have shown that mean cell size of
during the larval stage of echinoderm (Rumrill, 1990). phytoplankton decreased with temperature (Sommer
In addition, the total abundance of phytoplankton and Lengfellner, 2008). Copepods feed selectively on
increased from 1980s in Jiaozhou Bay (Sun et al., >10 μm food particles, and the degree to which
2011b), which was considered to be important for the herbivorous coastal copepods are food-limited may
growth and development of the planktonic larvae of be strongly dependent on the structure of the
benthic echinoderms (Fenaux et al., 1994). In recent phytoplankton assemblage (Dam and Peterson, 1991).
years, starfish blooms took place to cause severe In our study areas, the proportion of nano-
damage in bivalve aquaculture in Jiaozhou Bay phytoplankton (2–20 μm) compared to micro-
(Zhang et al., 2015). Thus, more attention should be phytoplankton (>20 μm) has increased since the
given to meroplankton, such as echinoderm larvae. 1990s in significant correlation with rising water
It has been suggested that global warming selects temperature, and nano-phytoplankton were dominant
for smaller organisms in marine systems (Daufresne during our study period (Sun and Sun, 2012). This
et al., 2009; Forster et al., 2012; Garzke et al., 2015). change in phytoplankton composition may favour
Decreasing copepod size with increasing temperature, smaller-sized copepods.
as seen in our study, has been previously reported General decreases in zooplankton abundance and
under laboratory conditions (Garzke et al., 2015) and mean size of total copepods and an increase in the
in the field (Suikkanen et al., 2013; Rice et al., 2015), relative abundance of small-sized copepods in
with two possible explanations. First, small copepods Jiaozhou Bay and the adjacent coastal Yellow Sea are
exhibit high fecundity and growth rates when food in line with predictions regarding the impact of global
supply is adequate at warmer temperatures (Turner, warming on marine ecosystems (Daufresne et al.,
2004). Generation time from egg to adult of 2009; Garzke et al., 2015). Because of the southern
Paracalanus sp. would be 21.8 days when raised at an Yellow Sea is a spawning and nursery area for local
average temperature of 15°C, with this duration finfish populations (Jin et al., 2010; Tang et al., 2016),
decreasing as temperature increased (Uye, 1991). By all of the abovementioned changes could disrupt
this mechanism, the higher relative abundance of fisheries by affecting predator-prey dynamics between
small-sized copepods in our study (Fig.11) may be larval fish and their primary copepod prey, particularly
attributed to warmer temperatures in these years. This as most planktivorous fish are visual predators and
is keeping with a study in the South Yellow Sea, select prey based on both type and size. This may, in
which found higher biomass of small copepods during turn, lead to ecological changes affecting community
warmer years (Shi et al., 2015). As an alternative structure and ecosystem function such as secondary
explanation, a rise in temperature could reduce the production and the flux of biogenic materials.
average size of copepods. We found that the average
5 CONCLUSION
volume of total copepods had a clear negative
correlation with water temperature (Fig.10a, b). This The present study provides basic information on
phenomenon can be explained by the temperature- the zooplankton community over an 8-year period in
size rule (TSR), which states that the individual body relation to environmental variables in Jiaozhou Bay
size of ectotherms tends to decrease with increasing and the adjacent coastal Yellow Sea. In both areas,
temperature (Daufresne et al., 2009). It is confirmed copepods were dominant based on both abundance
that rates of growth and development in copepods are and biovolume, followed by chaetognaths. In Jiaozhou
unequally affected by temperature, such that the rate Bay, N. scintillans occupied a more important role
of development increases more quickly with than in the Yellow Sea, where meroplankton were
temperature than does growth rate (Lehman, 1988). more prevalent. We identify a progressive decrease in
Therefore, under warmer conditions, the adult stage is zooplankton abundance over the study period,
reached before the largest potential size is achieved particularly in copepods. In addition, the proportion
(Forster and Hirst, 2012). For example, mean size of of small-sized copepods increased while the mean
1668 J. OCEANOL. LIMNOL., 36(5), 2018 Vol. 36

size of total copepods decreased, with the concurrent Dela-Cruz J, Middleton J H, Suthers I M. 2008. The influence
increase in water temperature likely driving these of upwelling, coastal currents and water temperature on
changes. Phenological change is also very common the distribution of the red tide dinoflagellate, Noctiluca
scintillans, along the east coast of Australia.
for zooplankton, such as copepods, is there any
Hydrobiologia, 598(1): 59-75.
phenological change in our studied regions, and how
Edwards M, Richardson A J. 2004. Impact of climate change
long the species can adapt to global warming need on marine pelagic phenology and trophic mismatch.
more studies. Considering the limitations of time Nature, 430(7002): 881-884.
scales in this study, further long-term monitoring Fenaux L, Strathmann M F, Strathmann R R. 1994. Five tests
survey is recommended. of food-limited growth of larvae in coastal waters by
comparisons of rates of development and form of
6 ACKNOWLEDGEMENT echinoplutei. Limnology and Oceanography, 39(1): 84-
98.
We sincerely thank Dr. CHENG Fangping for help Forster J, Hirst A G, Atkinson D. 2012. Warming-induced
in identifying zooplankton of the training set, and reductions in body size are greater in aquatic than
ZHU Mingliang for helping with the ZooScan data terrestrial species. Proceedings of the National Academy
analyses. We would like also to thank Dr. ZHOU of Sciences of the United States of America, 109(47):
Konglin for constructive comments on an earlier 19 310-19 314.
Forster J, Hirst A G. 2012. The temperature-size rule emerges
version of the manuscript. We are grateful for all the
from ontogenetic differences between growth and
staff at the Jiaozhou Bay Marine Ecosystem Research development rates. Functional Ecology, 26(2): 483-492.
Station for their valuable help with field work and Garzke J, Ismar S M H, Sommer U. 2015. Climate change
collecting the samples. affects low trophic level marine consumers: warming
decreases copepod size and abundance. Oecologia,
References
177(3): 849-860.
Beaugrand G, Ibañez F. 2002. Spatial dependence of calanoid Gorsky G, Ohman M D, Picheral M, Gasparini S, Stemmann
copepod diversity in the North Atlantic Ocean. Marine L, Romagnan J B, Cawood A, Pesant S, García-Comas C,
Ecology Progress Series, 232: 197-211. Prejger F. 2010. Digital zooplankton image analysis using
Chiba S, Batten S D, Yoshiki T, Sasaki Y, Sasaoka K, Sugisaki the ZooScan integrated system. Journal of Plankton
H, Ichikawa T. 2015. Temperature and zooplankton size Research, 32(3): 285-303.
structure: climate control and basin-scale comparison in Grosjean P, Picheral M, Warembourg C, Gorsky G. 2004.
the North Pacific. Ecology and Evolution, 5(4): 968-978. Enumeration, measurement, and identification of net
Dai L P, Li C L, Wang S W, Wang Y Q, Zhang F. 2016b. zooplankton samples using the ZOOSCAN digital
Analysis of community structure of zooplankton in south imaging system. ICES Journal of Marine Science, 61(4):
Yellow Sea in summer with ZooScan. Oceanologia et 518-525.
Limnologia Sinica, 47(4): 764-773. (in Chinese with Gubanova A D, Prusova I Y, Niermann U, Shadrin N V,
English abstract) Polikarpov I G. 2001. Dramatic change in the copepod
Dai L P, Li C L, Yang G, Sun X X. 2016a. Zooplankton community in Sevastopol Bay (Black Sea) during two
abundance, biovolume and size spectra at western decades (1976-1996). Senckenbergiana Maritima, 31(1):
boundary currents in the subtropical North Pacific during 17-27.
winter 2012. Journal of Marine Systems, 155: 73-83. Harrison P J, Furuya K, Glibert P M, Xu J, Liu H B, Yin K, Lee
Dam H G, Peterson W T. 1991. In situ feeding behavior of the J H W, Anderson D M, Gowen R, Al-Azri A R, Ho A Y T.
copepod Temora longicornis: effects of seasonal changes 2011. Geographical distribution of red and green
in chlorophyll size fractions and female size. Marine Noctiluca scintillans. Chinese Journal of Oceanology and
Ecology Progress Series, 71: 113-123. Limnology, 29(4): 807-831.
Dam H G, Roman M R, Youngbluth M J. 1995. Downward Hays G C, Richardson A J, Robinson C. 2005. Climate change
export of respiratory carbon and dissolved inorganic and marine plankton. Trends in Ecology & Evolution,
nitrogen by diel-migrant mesozooplankton at the JGOFS 20(6): 337-344.
Bermuda time-series station. Deep Sea Research Part I: Hill M O, Gauch Jr H G. 1980. Detrended correspondence
Oceanographic Research Papers, 42(7): 1 187-1 197. analysis: an improved ordination technique. Vegetatio,
Dam H G. 2013. Evolutionary adaptation of marine 42(1-3): 47-58.
zooplankton to global change. Annual Review of Marine Hoover R S, Hoover D, Miller M, Landry M R, DeCarlo E H,
Science, 5: 349-370. Mackenzie F T. 2006. Zooplankton response to storm
Daufresne M, Lengfellner K, Sommer U. 2009. Global runoff in a tropical estuary: bottom-up and top-down
warming benefits the small in aquatic ecosystems. controls. Marine Ecology Progress Series, 318: 187-
Proceedings of the National Academy of Sciences of the 201.
United States of America, 106(31): 12 788-12 793. Huang C, Qi Y. 1997. The abundance cycle and influence
No.5 WANG et al.: Zooplankton community structure, abundance and biovolume 1669

factors on red tide phenomena of Noctiluca scintillans time series of zooplankton phenology. Progress in
(Dinophyceae) in Dapeng Bay, the South China Sea. Oceanography, 97-100: 31-62.
Journal of Plankton Research, 19(3): 303-318. Motoda S. 1959. Devices of simple plankton apparatus.
Huang J Q, Zheng Z. 1986. The effects of temperature and Memoirs of the Faculty of Fisheries, Hokkaido University,
salinity on the survival of some copepods from Xiamen 7(1-2): 73-94.
Harbour. Oceanologia et Limnologia Sinica, 17(2): 161- Nakamura Y. 1998. Blooms of tunicates Oikopleura spp. and
167. (in Chinese with English abstract) Dolioletta gegenbauri in the Seto Inland Sea, Japan,
Ishizaka J, Harada K, Ishikawa K, Kiyosawa H, Furusawa H, during summer. Hydrobiologia, 385(1-3): 183-192.
Watanabe Y, Ishida H, Suzuki K, Handa N, Takahashi M. Ning X R, Lin C L, Su J L, Liu C G, Hao Q, Le F F, Tang Q S.
1997. Size and taxonomic plankton community structure 2010. Long-term environmental changes and the
and carbon flow at the equator, 175°E during 1990-1994. responses of the ecosystems in the Bohai Sea during
Deep Sea Research Part II: Topical Studies in 1960–1996. Deep Sea Research Part II: Topical Studies in
Oceanography, 44(9-10): 1 927-1 949. Oceanography, 57(11-12): 1 079-1 091.
Jin X S, Zhang B, Xue Y. 2010. The response of the diets of Parson T R, Maita Y, Lalli C M. 1984. A Manual of Chemical
four carnivorous fishes to variations in the Yellow Sea and Biological Methods for Seawater Analysis. Pergamon
ecosystem. Deep Sea Research Part II: Topical Studies in Press, New York. p.3-122.
Oceanography, 57(11-12): 996-1000. Peng S T, Qin X B, Shi H H, Zhou R, Dai M X, Ding D W.
Kang J H, Kim W S, Jeong H J, Shin K, Chang M. 2007. Why 2012. Distribution and controlling factors of phytoplankton
did the copepod Calanus sinicus increase during the assemblages in a semi-enclosed bay during spring and
1990s in the Yellow Sea? Marine Environmental Research, summer. Marine Pollution Bulletin, 64(5): 941-948.
63(1): 82-90. Rice E, Dam H G, Stewart G. 2015. Impact of climate change
Kirby R R, Beaugrand B, Lindley J A, Richardson A J, Edwards on estuarine zooplankton: surface water warming in long
M, Reid P C. 2007. Climate effects and benthic-pelagic island sound is associated with changes in copepod size
coupling in the North Sea. Marine Ecology Progress and community structure. Estuaries and Coasts, 38(1):
Series, 330: 31-38. 13-23.
Lehman J T. 1988. Ecological principles affecting community Roemmich D, McGowan J. 1995. Climatic warming and the
structure and secondary production by zooplankton in decline of zooplankton in the california current. Science,
marine and freshwater environments. Limnology and 267(5202): 1 324-1 326.
Oceanography, 33(4): 931-945. Rumrill S S. 1990. Natural mortality of marine invertebrate
Lewandowska A M, Boyce D G, Hofmann M, Matthiessen B, larvae. Ophelia, 32(1-2): 163-198.
Sommer U, Worm B. 2014. Effects of sea surface warming Sato K, Matsuno K, Arima D, Abe Y, Yamaguchi A. 2015.
on marine plankton. Ecology Letters, 17(5): 614-623. Spatial and temporal changes in zooplankton abundance,
Lin C L, Su J L, Xu B R, Tang Q S. 2001. Long-term variations biovolume, and size spectra in the neighboring waters of
of temperature and salinity of the Bohai Sea and their Japan: analyses using an optical plankton counter.
influence on its ecosystem. Progress in Oceanography, Zoological Studies, 54(1): 18.
49(1-4): 7-19. Schultes S, Lopes R M. 2009. Laser Optical Plankton Counter
Lin C, Ning X, Su J, Lin Y, Xu B. 2005. Environmental and Zooscan intercomparison in tropical and subtropical
changes and the responses of the ecosystems of the Yellow marine ecosystems. Limnology and Oceanography:
Sea during 1976-2000. Journal of Marine Systems, 55(3- Methods, 7(11): 771-784.
4): 223-234. Sherr E, Sherr B. 2009. Understanding roles of microbes in
Lindley J A, Batten S D. 2002. Long-term variability in the marine pelagic food webs: a brief history. In: Kirchman D
diversity of North Sea zooplankton. Journal of the Marine L ed. Microbial Ecology of the Oceans. 2nd edn. John
Biological Association of the United Kingdom, 82(1): 31- Wiley & Sons Inc., New York. p.27-44.
40. Shi Y Q, Sun S, Zhang G T, Wang S W, Li C L. 2015.
Liu M T, Li C L, Sun S. 2011. Seasonal variation in fatty acid Distribution pattern of zooplankton functional groups in
composition of seston and the copepod Calanus sinicus the Yellow Sea in June: a possible cause for geographical
(Brodsky, 1962) in Jiaozhou Bay and its trophic separation of giant jellyfish species. Hydrobiologia,
implications. Chinese Journal of Oceanology and 754(1): 43-58.
Limnology, 29(6): 1 164-1 173. Sommer U, Lengfellner K. 2008. Climate change and the
Liu Q, Qu H, Zhang S. 2007. Preliminary studies on the timing, magnitude, and composition of the phytoplankton
tolerance to temperature and salinity in Sagitta crassa. spring bloom. Global Change Biology, 14(6): 1 199-
Transactions of Oceanology and Limnology, (1): 111-116. 1 208.
(in Chinese with English abstract) Suikkanen S, Pulina S, Engström-Öst J, Lehtiniemi M,
Mackas D L, Greve W, Edwards M, Chiba S, Tadokoro K, Lehtinen S, Brutemark A. 2013. Climate change and
Eloire D, Mazzocchi M G, Batten S, Richardson A J, eutrophication induced shifts in northern summer
Johnson C, Head E, Conversi A, Peluso T. 2012. Changing plankton communities. PLoS One, 8(6): e66475.
zooplankton seasonality in a changing ocean: Comparing Sun S, Li Y H, Sun X X. 2012. Changes in the small-jellyfish
1670 J. OCEANOL. LIMNOL., 36(5), 2018 Vol. 36

community in recent decades in Jiaozhou Bay, China. Uye S I. 1988. Temperature-dependent development and
Chinese Journal of Oceanology and Limnology, 30(4): growth of Calanus sinicus (Copepoda: Calanoida) in the
507-518. laboratory. In: Boxshall G A, Schminke H K eds. Biology
Sun S, Zhou K, Yang B, Zhang Y S, Ji P. 2008. Ecology of of Copepods. Springer, Dordrecht, Netherlands. p.285-
zooplankton in the Jiaozhoubay I. species composition. 293.
Oceanologia et Limnologia Sinica, 39(1): 1-7. (in Chinese Uye S. 1991. Temperature-dependent development and growth
with English abstract) of the planktonic copepod Paracalanus sp. in the
Sun X H, Sun S, Li C L, Zhang G T. 2011a. Seasonal and laboratory. Bulletin of the Plankton Society of Japan,
spatial variability in egg production, abundance and Special Volume: 627-636.
production of small copepods in and near Jiaozhou Bay, Wang Q, Sun S, Huo Y Z, Yang B. 2010. The ecology of
China. Journal of Plankton Research, 33(5): 741-750. chaetognaths in Jiaozhou Bay. Oceanologia et Limnologia
Sun X X, Sun S, Wu Y L, Zhang Y S, Zheng S. 2011b. Long- Sinica, 41(4): 639-644. (in Chinese with English abstract)
term changes of phytoplankton community structure in Wang Y T, Sun S. 2015. Population dynamics of Aurelia sp.1
the Jiaozhou Bay. Oceanologia et Limnologia Sinica, ephyrae and medusae in Jiaozhou Bay, China.
42(5): 639-646. (in Chinese with English abstract) Hydrobiologia, 754(1): 147-155.
Sun X X, Sun S. 2012. Phytoplankton size structure and its Wernberg T, Russell B D, Moore P J, Ling S D, Smale D A,
temporal and spatial changes in Jiaozhou Bay. Campbell A, Coleman M A, Steinberg P D, Kendrick G A,
Oceanologia et Limnologia Sinica, 43(3): 411-418. (in Connell S D. 2011. Impacts of climate change in a global
Chinese with English abstract) hotspot for temperate marine biodiversity and ocean
Tada K, Pithakpol S, Montani S. 2004. Seasonal variation in warming. Journal of Experimental Marine Biology and
the abundance of Noctiluca scintillans in the Seto Inland Ecology, 400(1-2): 7-16.
Sea, Japan. Plankton Biology & Ecology, 51(1): 7-14. Wickstead J H. 1976. Marine Zooplankton. The Institute of
Tang Q S, Jin X S, Wang J, Zhuang Z M, Cui Y, Meng T X. Biology's Studies in Biology No. 62. Edward Arnold,
2003. Decadal-scale variations of ecosystem productivity London.
and control mechanisms in the Bohai Sea. Fisheries Zhang T W, Zhu L Y, Xu P P, Zhou H, Qi B J. 2009. Seasonal
Oceanography, 12(4-5): 223-233. variation and distribution characteristics of Noctiluca
Tang Q S, Ying Y P, Wu Q. 2016. The biomass yields and scintillans in Jiaozhou Bay. Periodical of Ocean
management challenges for the Yellow sea large marine University of China, 39(S): 89-93. (in Chinese with
ecosystem. Environmental Development, 17(S1): 175- English abstract)
181. Zhang Z H, Zhang X L, Xu Z J, Yao H Y, Li G, Liu X J. 2015.
Turner J T. 2004. The importance of small planktonic copepods Emergency countermeasures against marine disasters in
and their roles in pelagic marine food webs. Zoological Qingdao City on the basis of scenario analysis. Natural
Studies, 43(2): 255-266. Hazards, 75(S2): S233-S255.