Spatiotemporal distribution of protozooplankton and ... - Springer Link

Chinese Journal of Oceanology and Limnology Vol. 31 No. 6, P. 1226-1240, 2013 http://dx.doi.org/10.1007/s00343-014-3095-5

Spatiotemporal distribution of protozooplankton and copepod nauplii in relation to the occurrence of giant jellyfish in the Yellow Sea* WANG Lu (王璐)1, 2, XU Kuidong (徐奎栋)1, ** 1

Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China

2

University of Chinese Academy of Sciences, Beijing 100049, China

Received Mar. 13, 2013; accepted in principle Apr. 12, 2013; accepted for publication Aug. 1, 2013 © Chinese Society for Oceanology and Limnology, Science Press, and Springer-Verlag Berlin Heidelberg 2013

Abstract The occurrence of the giant jellyfish, Nemopilema nomurai, has been a frequent phenomenon in the Yellow Sea. However, the relationship between the giant jellyfish and protozoa, in particular ciliates, remains largely unknown. We investigated the distribution of nanoflagellates, ciliates, Noctiluca scintillans, and copepod nauplii along the transect 33°N in the Yellow Sea in June and August, 2012, during an occurrence of the giant jellyfish, and in October of that year when the jellyfish was absent. The organisms studied were mainly concentrated in the surface waters in summer, while in autumn they were evenly distributed in the water column. Nanoflagellate, ciliate, and copepod nauplii biomasses increased from early June to August along with jellyfish growth, the first two decreased in October, while N. scintillans biomass peaked in early June to 3 571 μg C/L and decreased in August and October. In summer, ciliate biomass greatly exceeded that of copepod nauplii (4.61–15.04 μg C/L vs. 0.34–0.89 μg C/L). Ciliate production was even more important than biomass, ranging from 6.59 to 34.19 μg C/(L∙d) in summer. Our data suggest a tight and positive association among the nano-, micro-, and meso-zooplankton in the study area. Statistical analysis revealed that the abundance and total production of ciliate as well as loricate ciliate biomass were positively correlated with giant jellyfish biomass, indicating a possible predator-prey relationship between ciliates and giant jellyfish. This is in contrast to a previous study, which reported a significant reduction in ciliate standing crops due to the mass occurrence of N. nomurai in summer. Our study indicates that, with its high biomass and, in particular, high production ciliates might support the mass occurrence of giant jellyfish. Keyword: Nemopilema nomurai; nanoflagellates; ciliates; Noctiluca scintillans

1 INTRODUCTION Giant jellyfish, in particular Nemopilema nomurai, blooms have been a frequent event in the seas surrounding East Asia (Xian et al., 2005; Dong et al., 2010; Uye, 2011). Jellyfish, as top planktonic predators, can cause drastic changes in the plankton structure of marine ecosystems by feeding directly on mesozooplankton during blooms (Larson, 1987; Stibor and Tokle, 2003; Compte et al., 2010). In pelagic ecosystems, copepods are usually the main components of zooplankton grazing on ciliates. Ciliates then prey on nanoflagellates, which are the main bacteria and picophytoplankton grazers (Fenchel, 2008). Condon et al. (2011) suggested that jellyfish have a bottom-up effect on bacterial

communities by releasing colloidal and dissolved organic matter. Thus, flagellates and ciliates play a key role in transferring primary production to higher trophic levels in the jellyfish-dominated ecosystem. N. nomurai, one of the largest jellyfish, is thought to feed mainly on mesozooplankton such as copepods (Uye, 2011). However, a recent study indicated that mesozooplankton alone might not support mass occurrences of N. nomurai (Zhang, 2008). Feeding relationships have been reported between small jellyfish and ciliates or nanoflagellates. Aurelia adults

* Supported by the National Basic Research Program of China (973 Program) (No. 2011CB403604) ** Corresponding author: [email protected]

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WANG and XU: Protozooplankton and copepod nauplii in relation to giant jellyfish

and polyps can directly prey on ciliates (Malej et al., 2007; Turk et al., 2008; Kamiyama, 2011), and the ephyrae can feed on nanoflagellates (Båmstedt et al., 2001). Indirect cascading effects have been reported between other species of small jellyfish such as Odessia maeotica and ciliates and/or nanoflagellates (Granéli and Turner, 2002; West et al., 2009; Compte et al., 2010). However, despite the frequent occurrence of and disaster caused by the giant jellyfish in East Asia (Sun et al., 2012), there have been no investigations into the relationship between N. nomurai and microzooplankton, in particular ciliated protozoa, to date. In 2012, there was a mass giant jellyfish bloom in the southern Yellow Sea from early June to August, particularly at 33N. The jellyfish rapidly increased in both abundance and biomass in late June, reaching peak biomass in August, and then disappeared in October (S. Sun’s unpubl. data). In May of the same year, an N. scintillans red-tide bloom also occurred along China’s Rizhao coast (35°N). In the present study, we sampled at five stations along the transect 33°N in early June, late June, August, and October 2012. The aims of the study were to reveal (i) protozooplankton (including nanoflagellates, ciliates, and N. scintillans) and copepod nauplii spatiotemporal variation during the N. nomurai bloom, (ii) the relationship between the giant jellyfish and protozooplankton and copepod nauplii, and (iii) the potential role of microzooplankton (ciliates and copepod nauplii) as a giant jellyfish food source.

2 MATERIAL AND METHOD 2.1 Study site and sample collection Water samples were collected from five stations (I1–I5) along the transect 33°N in the southern Yellow Sea in early June (June 8–9), late June (June 24–25), August 14–15, and October 21, 2012 (Fig.1). At each station, sea water was collected with a rosette sampler at different depths (surface, 10, 20, 30, 50 m, and sea floor). A 1-L sample from each depth was transferred to a plastic container and immediately fixed with Lugol’s iodine solution (2% final concentration) (Sherr and Sherr, 1993). All samples were kept in the dark until examination. Vertical profiles of water temperature, depth, and salinity were obtained with a Sea Bird CTD system (conductance temperature depth). Depending on the concentration of the organisms,

34° N

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33° I1 I2 I3 I4 I5 32°

31°

30° 118°

Shanghai

120°

East China Sea

122°

124°

E

126°

Fig.1 Map of the five sampling stations I1–I5 along the transect 33°N in the southern Yellow Sea

each of the fixed samples was settled in a glass column for 48 h in the laboratory, concentrated to 100 mL, and then used for the examination. 2.2 Enumeration of heterotrophic and phototrophic nanoflagellates For enumeration of heterotrophic and phototrophic nanoflagellates, a subsample of 5 mL aliquots of the concentrated sample was added to a small amount of 3% sodium thiosulfate (~100 μL). The sodium thiosulfate bleaches out the iodine color, reducing the darkness of the Lugol’s fixed cells, enhancing fluorescence (Pomroy, 1984; Sherr and Sherr, 1993). The bleached sample was then stained with DAPI (15 μg/mL f.c.), filtered on a black 0.22 μm mixed cellulose ester membrane filter (Porter and Feig, 1980), and counted under epifluorescence microscopy (Zeiss Axioskop 2 plus) with UV excitation at 1 000× magnification. Heterotrophic and phototrophic nanoflagellates in at least 50 fields per filter were counted and the biovolumes of these organisms estimated based on their appropriate geometrical shapes. Heterotrophic and phototrophic nanoflagellate carbon biomasses were calculated using a volumecarbon conversion factor of 220 fg C/μm3 (Borsheim and Bratbak, 1987). 2.3 Enumeration and identification of ciliates, Noctiluca scintillans, and copepod nauplii The 100 mL-concentrated water was settled in a glass column for a further 48 h, and concentrated to 10 mL. A subsample of 1-mL aliquots of the secondary concentrated sample was examined on a 1-mL counting grid under a LEICA DM4500B at 100–200× magnification for ciliates, N. scintillans, and copepod nauplii. Ciliate species identification was based on the published literature (Kofoid and Campbell, 1929,

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1939; Song et al., 2009). For each taxon, the average dimensions were based on the measurements of at least 20 individuals (fewer individuals were used in the case of rare taxa) and biovolumes (lorica volume in the case of tintinnids) were estimated by geometric approximation (Hillebrand et al., 1999). The same method was applied to N. scintillans and copepod nauplii. Dominant ciliates species were based on either their average abundance or average biomass contributions exceeding 10% of the total average abundance or biomass in all samples collected in each period. Individual species cell volume was transformed into carbon biomass using the conversion factor 0.19 pg C/μm3 for ciliates (Putt and Stoecker, 1989). Tintinnid carbon biomass was assumed to occupy 30% of the lorica volume (Gilron and Lynn, 1989). The carbon biomass estimation for N. scintillans followed the formula: C (pg C/ind.)=0.216×cell volume (μm3)0.939 (Menden-Deuer and Lessard, 2000). For copepod nauplii, the conversion factor 0.07 pg C/μm3 was used (Moloney and Field, 1991). Ciliate, N. scintillans, and copepod nauplii production (μg C/(L·d)) was calculated by multiplying biomass (μg C/L) by growth rate (/d). Ciliate growth rates were estimated using the equation: lng=1.52lnt 0.27lnCV1.44 (CV is cell volume of ciliates; t is water temperature; Müller and Geller, 1993). N. scintillans growth rates were taken as 0.2/d (Nakamura, 1998), and that of copepod nauplii was calculated according to g=0.057e0.069t (t is water temperature) (Uye et al., 1996). The average abundance, biomass, and production of individual groups in the water column (CA) at each station were calculated using the formula (Ke et al., 2011):  n1 A +A  C A =  i i 1  Di 1  Di   /D ,  i 1 2  where Ai= the abundance (or biomass or production) in the “i-th” water layer; n=the total number of water layers sampled; Di=the depth of the “i-th” water layer; D=the total sampling depth. The total abundance, biomass, and production in the water column were calculated by multiplying CA by D. Giant jellyfish feeding pressure on ciliate biomass and production (or copepod nauplii) was estimated by dividing jellyfish feeding rates (Zhang unpubl.) by ciliate (or copepod nauplii) biomass and production, assuming that they only consumed ciliates (or copepod nauplii) (Zhang, 2008).

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2.4 Graphics and statistical analysis The distribution maps of environmental and biological variables were constructed using Golden Software Surfer (Version 10.0, Golden Software Inc., USA). Spearman correlation analysis was calculated for the relationships between the biotic and abiotic factors as well as between biotic factors. Data were log-transformed to fit the assumptions of normality and homogeneity of variances. Ciliate community structure was analyzed in PRIMER 6 (Plymouth Marine Laboratory, UK). CLUSTER analysis was used to clarify the characteristics of ciliate community spatiotemporal distributions (species-abundance) at the five stations (I15) on different sampling dates. Analysis of similarity percentages (SIMPER) was used to determine the dominant ciliate species in the groups formed from CLUSTER analysis. One-way analysis of similarity (ANOSIM) was performed to test differences between the ciliate community compositions in different groups. The multivariate biota-environment (BIOENV) procedure was applied to explore the potential relationships between the biotic assemblage biomasses (nanoflagellates, ciliates, N. scintillans, and copepod nauplii) and the jellyfish carbon weight by maximizing a rank correlation between their respective similarity matrices (BrayCurtis similarity).

3 RESULT 3.1 Environmental factors Water temperature decreased, while salinity increased with increasing water depth. The average water temperature was 16.23±3.27°C in early June, 17.62±3.77°C in late June, 21.31±5.98°C in August, and 21.16±0.33°C in October, 2012. Average salinity was 30.16±1.88, 29.77±2.76, 31.42±2.27, and 30.68±0.13, respectively. The highest temperature and salinity values were recorded in August (Fig.2). A thermocline was found at a depth of about 20 m from early June to August, and disappeared in October, 2012. The vertical salinity gradient disappeared at stations I1 and I2 in August and along the entire transect in October (Fig.2). 3.2 Phototrophic (PNFs) nanoflagellates (HNFs)

and

heterotrophic

HNF and PNF abundance and biomass were mostly patchy. HNF abundance was mainly concentrated near the thermocline, while PNFs were most abundant

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Fig.2 Water temperature (a–d) and salinity (e–h) profiles along the transect 33°N from early June to October, 2012

was in the surface layer to a depth of 10 m from early June to August. The distribution of HNF and PNF biomass was less heterogeneous than that of abundance, but generally followed a similar pattern (Figs.3 and 4). Nanoflagellate abundance and biomass decreased

from the coastal to the offshore area (Fig.7). The average HNF abundance over the whole transect varied from 164±142 ind./mL to 374±224 ind./mL, and increased from early June to October, except for a slight fall in late June (Table 1). The average HNF biomass ranged from 4.37±4.04 μg C/L to

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Fig.3 HNF abundance and biomass along the transect 33°N from early June to October, 2012

12.42±11.58 μg C/L, and increased continuously from early June to August, then decreased in October. PNF abundance was 2–3 times that of HNFs. The PNF biomass was 3–5 times that of HNFs. Both PNF abundance and biomass exhibited the same temporal and spatial changes as those of the HNFs (Table 1).

3.3 Ciliates A total of 56 ciliate species belonging to 22 genera were identified, comprising 18 species of aloricate ciliates and 38 species of tintinnids over the four sampling periods. Strombidium was the most diverse

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Fig.4 PNF abundance and biomass along the transect 33°N from early June to October, 2012

group of aloricate ciliates, and Tintinnopsis the most diverse tintinnid group. The species composition varied temporally. Total ciliate species richness increased from early (26 species) through late June (33 species) to August (41 species), and subsequently decreased in October (27 species). Tintinnid species richness followed the same pattern, with 13, 18, 26,

and 16 species observed, respectively. Ciliate species body length fell within the range of 25–265 μm, with the small-sized aloricate ones (~25– 85 μm long) being dominant in both abundance and biomass. The dominant species composition also varied temporally. Strombidium sp.1 (~28×20 m), sp.2 (47×26 m), sp.3 (38×25 m), Laboea strobila

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Table 1 Average abundance and biomass of HNFs, PNFs, ciliates, Noctiluca scintillans, and copepod nauplii, and average ciliate, Noctiluca scintillans, and copepod nauplii production in all samples collected in early June, late June, August, and October, 2012

Abundance (ind./mL)

Abundance (ind./L)

Biomass (μg C/L)

Production (μg C/(L∙d))

HNFs

June 8–9

June 24–25

August 14–15

October 21

206±133

164±142

279±199

374±224

a

PNFs

501±174

478±231

548±260

815±141

Ciliates

2 018±3096

4 557±5639

6 656±6439

2 300±795

Noctiluca scintillans

194±494

92±155

136±255

2±5

Copepod nauplii

23±48

48±98

62±42

62±38

HNFs

4.37±4.04

7.39±9.02

12.42±11.58

7.29±7.44

PNFs

21.47±9.36

26.86±19.46

38.18±28.67

32.20±7.01

Ciliates

4.61±6.97

9.67±11.00

15.04±15.34

4.34±1.38


379.36±967.31

180.65±302.46

266.39±499.91

4.12±9.90

Copepod nauplii

0.34±0.70

0.70±1.41

0.89±0.60

0.89±0.55

Ciliates

6.59±11.27

15.35±18.95

34.19±39.93

8.47±2.79


75.87±193.46

36.13±60.49

53.28±99.98

0.82±1.98

Copepod nauplii

0.071±0.17

0.17±0.38

0.28±0.24

0.22±0.13

: Mean±SD

a

(~85×40 m), Lohmanniella sp.(~37×34 m), and Mesodinium rubrum (~25×20 m) were the most dominant species in early June. Strombidium sp.1 and sp.3, Lohmanniella sp., and Mesodinium rubrum dominated in late June. Strombidium sp.1, Lohmanniella sp., and Mesodinium rubrum were the most dominant species in August and October. The dominant species accounted for 89.3%, 81.0%, 79.1%, and 80.7% of the total ciliate abundance, respectively, and 80.7%, 69.7%, 52.4%, and 73.5% of the total ciliate biomass, respectively. The aloricate ciliates contributed approximately 96.1% of total ciliate abundance in early June and approximately 92.1% in October. Although tintinnids accounted for a mere 6.8% of total ciliate abundance in August and 7.9% in October, they accounted for 20.1% and 11.5% of the total biomass in those months, respectively. Ciliate abundance and biomass exhibited similar spatial and temporal distribution patterns. The average ciliate abundance ranged from 2 018±224 ind./L to 6 656±6 439 ind./L, and the biomass ranged from 4.34±1.38 μg C/L to 15.04±2.24 μg C/L, increasing from early June to August, and decreasing sharply in October (Table 1). Horizontally, ciliate abundance and biomass increased from the coastal to the offshore area in early June, peaked at both the coastal station I1 and the offshore station I4 in late June, decreased from the coastal to the offshore stations in August, but remained stable in October (Fig.7). During summer, the high ciliate density shifted from the surface layer

in June to the 10 m layer, particularly at station I1, in August (Fig.5). Compared with biomass, ciliate production was more important, with average values continuously increasing from early June and peaking in August at 34.19±39.93 μg C/(L∙d), and then decreasing sharply to approximately 8.47±2.79 μg C/(L∙d) in October (Table 1). CLUSTER analysis based on the ciliate communities in the surface layer classified the samples into three groups: group 1 was mainly comprised of the samples obtained in October, group 2 was mainly comprised of those collected in August, and group 3 was mainly comprised of those collected in June. Groups 2 and 3 formed a cluster with an average similarity of 61.1%, and group 1 had only an average similarity of 48.3% and 58.2% with groups 2 and 3, respectively (Fig.8). SIMPER analysis revealed that the small-sized dominant species, Strombidium sp.1, Lohmanniella sp., Mesodinium rubrum and Tontonia simplicidens and the medium-sized species Strombidium sp.2 (~47×26 μm), gave rise to the differences among the three groups. ANOSIM analysis revealed significant differences between the three groups (R=0.904, P=0.001). The CLUSTER analysis exhibited a different pattern of ciliate communities in the 10-m layer. While three main groups could be distinguished, group I was comprised only samples obtained in August, group II was only comprised of those

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Fig.5 Ciliate abundance and biomass along the transect 33°N from early June to October, 2012

collected in October, and group III comprised samples collected in June and clustered with group II. Group I had an average similarity of 53.0% with group II and 48.1% with group III (Fig.8). SIMPER analysis identified that Strombidium sp.1, Lohmanniella sp., and Mesodinium rubrum gave rise to the difference

among the three groups. ANOSIM analysis revealed significant differences between the three groups (R=0.875, P=0.001). 3.4 Noctiluca scintillans N. scintillans, the most predominant plankton

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h. October 21 40 Biomass (μg C/L) 50

Fig.6 Noctiluca scintillans (a–d) and copepod nauplii (e–h) biomass along the transect 33°N from early June to October, 2012

analyzed, was mainly concentrated near the surface layer during the sampling period, numbers decreased with increasing water depth (Fig.6). The average N. scintillans abundance ranged from 2±5 ind./L to 194±494 ind./L and biomass from 4.12±9.90 μg C/L to 379.36±967.31 μg C/L along the entire transect during the sampling period (Table 1). Peaks in

abundance of 1 824 ind./L and biomass of 3 571.00 μg C/L were observed in the surface layer at station I3 in early June, and had decreased by late June. In August N. scintillans abundance and biomass increased 1.5 times those in late June, and then dramatically decreased to the lowest observed values in October (Fig.6; Table 1).

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70 60

20

PNFs (μg C/L)

HNFs (μg C/L)

25

15 10 5

40 30 20 0

I1

I2

I1 I3

I4

Noctiluca scintillans (μg C/L)

25 20 15 10 5 0 I1

I2

I3

I3

I5

2.5

I4

I5

600 500 400 300 200 100 0 I1

I4

I2

I5

30 Ciliates (μg C/L)

50

10

0

Copepod nauplii (μg C/L)

1235

I2

I3

I4

I5

June 8–9

2

June 24–25

1.5

August 14–15

1

October 21

0.5 0 I1

I2

I3

I4

I5

Fig.7 The average HNF, PNF, ciliate, Noctiluca scintillans, and copepod nauplii biomasses in the water columns at stations I1 to I5 along the transect 33°N from early June to October, 2012

N. scintillans maximum average production was observed in early June, with an average of 75.87±193.46 μg C/(L∙d). Production decreased to 36.13±60.49 μg C/(L∙d) in late June, increased to 53.28±99.98 μg C/(L∙d) in August, and then sharply decreased to 0.82±1.98 μg C/(L∙d) in October. 3.5 Copepod nauplii Copepod nauplii abundance and biomass were mainly distributed in the surface layer in June and

August, but became less heterogeneous in October (Fig.6). The copepod nauplii biomass was concentrated in the furthest offshore site in early June, while in late June accumulation occurred in the site closest to the coast (Fig.7). The average copepod nauplii abundance increased from 23±48 ind./L in early June to 48±98 ind./L in late June, and peaked at approximately 62 ind./L both in August and October. Biomass followed the same pattern and peaked at approximately 0.89 μg C/L in both August and October (Table 1).

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Vol.31

50

Similarity (%)

60

70

80

Group 2

I2-Jun.24–25

I3-Jun.8–9

I4-Jun.24–25

I3-Jun.24–25

I5-Jun.8–9

{

Group 1

I5-Jun.24–25

I3-Aug.

I1-Jun.24–25

I4-Aug.

I2-Aug.

I5-Aug.

I4-Jun.8–9

I1-Aug.

I4-Oct.

I3-Oct.

I2-Jun.8–9

{ {

I4-Jun.8–9

I5-Oct.

I2-Oct.

100

I1-Oct.

90

Group 3

20

Similarity (%)

40

60

I2-Jun.24–25

I2-Jun.8–9

I1-Jun.8–9

I5-Jun.24–25

I4-Jun.24–25

I5-Jun.8–9

I3-Jun.8–9

I3-Jun.24–25

I4-Jun.8–9

I1-Jun.24–25

I4-Oct.

I1-Oct.

I3-Oct.

I2-Oct.

I5-Oct.

I4-Aug.

I3-Aug.

{ { {

I5-Aug.

I2-Aug.

100

I1-Aug.

80

Group I

Group II

Group III

Fig.8 Cluster analysis based on ciliate species-abundance in the surface (upper) and 10-m water layers (lower) at the five stations (I1–5) from June (early June 8–9 and late June 24–25) through August to October, 2012

Compared with the biomass, copepod nauplii production was less important. Similar to the pattern seen in ciliates, the average copepod nauplii production continuously increased from 0.071±0.17 μg C/(L∙d) in early June to 0.17±0.38 μg C/(L∙d) in late June, peaked at 0.28±0.24 μg C/(L∙d) in August, and then decreased slightly to 0.22±0.13 μg C/(L∙d) in October.

3.6 Relationship between biotic and abiotic factor The Spearman correlation analysis results indicate similar relationships between abundance and biomass in the abiotic and biotic factors. Therefore, only the biomass relationships are shown in Table 2. Most biotic factors were significantly, positively correlated with water temperature (Table 2). PNFs were

No.6


1237

Table 2 Spearman correlation coefficients among water temperature, salinity and depth, the biomass of the giant jellyfish Nemopilema nomurai, HNFs, PNFs, ciliates (both aloricate ciliates and tintinnids), tintinnids, Noctiluca scintillans and copepod nauplii, and ciliate abundance and production HNF biomass

PNF biomass

Ciliate biomass

Tintinnid biomass

Noctiluca scintillans biomass

Copepod nauplii biomass

Ciliate abundance

Ciliate production

Water temperature (°C)

0.25**

0.66**

0.68**

0.12

0.52**

0.57**

0.74**

0.82**

Water salinity

0.067

-0.29*

-0.28*

0.45**

-0.27*

-0.19

-0.32**

-0.38**

Water depth (m)

-0.23

-0.46

-0.52

0.30

**

-0.50

-0.30

-0.60

-0.59**

Giant jellyfish biomass

0.49

0.26

0.48

0.61*

0.18

0.33

0.60*

0.62*

0.060

0.38**

0.26*

0.14

0.27*

0.33**

0.37**

0.55

0.17

0.43

0.49

0.60

**

0.62**

0.30**

0.61**

0.60**

0.95**

0.97**

0.03

0.26*

0.21

0.25*

0.27

**

0.64

0.61**

0.65**

0.69**

*

HNF biomass PNF biomass Ciliate biomass

*

**

**

Tintinnid biomass Noctiluca scintillans biomass Copepod nauplii biomass

*

**

**

**

*

**

Levels of significance are *P0.05, **P0.01

significantly, positively correlated with N. scintillans. Ciliates and copepod nauplii were significantly, positively correlated with water temperature and almost all of the biotic factors (Table 2). The giant jellyfish, N. nomurai, biomass (Zhang et al., unpubl. data, obtained by fishery trawl-net) had no significant relationship with any abiotic or biotic factor, except for a positive correlation with ciliate abundance (ρ=0.60, P