# Planktonic ciliates in different water masses in open waters near Prydz Bay (East Antarctica) during austral summer, with an emphasis on tintinnid assemblages

Chen Liang, Haibo Li, Yi Dong, Yuan Zhao, Zhencheng Tao, Chaolun Li, Wuchang Zhang, Gérald Grégori

► To cite this version:

Chen Liang, Haibo Li, Yi Dong, Yuan Zhao, Zhencheng Tao, et al.. Planktonic ciliates in different water masses in open waters near Prydz Bay (East Antarctica) during austral summer, with an emphasis on tintinnid assemblages. Polar Biology, 2018, 41 (11), pp.2355-2371. 10.1007/s00300-018-2375-5. hal-02024248

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# Planktonic ciliates in different water masses in open waters near Prydz Bay (East Antarctica) during austral summer, with an emphasis on tintinnid assemblages

Chen Liang<sup>1,2,3,4</sup> · Haibo Li<sup>1,2,4</sup> · Yi Dong<sup>1,2,4</sup> · Yuan Zhao<sup>1,2,4</sup> · Zhencheng Tao<sup>1,2,4</sup> · Chaolun Li<sup>1,2,4</sup> · Wuchang Zhang<sup>1,2,4</sup> · Gerald Gregori<sup>5</sup>

## Abstract

Planktonic ciliates are important microzooplankton in pelagic ecosystems. Previous studies in Antarctic waters have only investigated ciliate assemblages in different habitats without considering water masses. In this article, we report the charac-teristics of ciliate assemblages in different water masses in open waters near Prydz Bay (East Antarctica) during austral sum-mer. Three water masses were identified according to temperature and salinity: Summer Surface Water (SSW), Winter Water (WW), and Circumpolar Deep Water (CDW). SSW was further divided into $SSW_{Chl a < 3}$ (in vivo Chlorophyll $a > 3$ mg m$^{-3}$) and $SSW_{Chl a < 3}$ (in vivo Chlorophyll $a < 3$ mg m$^{-3}$). Ciliate abundance and biomass in water masses decreased in the order: SSW > WW > CDW. $SSW_{Chl a > 3}$ had a higher proportion (38.2%) of tintinnids to the total ciliate abundance and larger aloricate ciliates (ciliates in the 10–20 µm size class were < 15% of the total aloricate ciliate abundance) than in other water masses. WW had a higher proportion (> 30%) of Southern Ocean endemic tintinnid species in total tintinnid abundance than in other water masses. Each water mass had the following indigenous tintinnid species: SSW, *Salpingella* sp., *Codonellopsis gaussiani*; WW, *Salpingella costata*, *S. faurei*, *Cymatocylis affinis/convallaria* forma *drygalskii*, and *C. vanhoeffeni*. *Laackman-niella naviculaefera* and *C. affinis/convallaria* forma *cristallina* were present at high abundance in both WW and $SSW_{Chl a > 3}$. Upwelling caused discontinuity of the ciliate distribution. Our results will help predict the spatial and temporal variations of ciliate assemblages and other plankton according to the dynamics of water masses in Antarctic waters.

**Keywords** Planktonic ciliates · Abundance · Tintinnid · Water mass · Prydz Bay · Antarctica

**Electronic supplementary material** The online version of this article (https://doi.org/10.1007/s00300-018-2375-5) contains supplementary material, which is available to authorized users.

<figure><img src="image_2.png" /></figure>

Wuchang Zhang
wuchangzhang@qdio.ac.cn

## Introduction

Marine planktonic ciliates constitute a major, ubiquitous, and diverse group of protozoa. These organisms range from 5 to 200 µm in length and can be divided into tintinnids and aloricate ciliates, which belong to the subclasses Oligotrichia and Choreotrichia, respectively, in the class Spirotrichea (Lynn 2008). As one of the main components of microzooplankton, ciliates are a trophic link between the microbial food web and the traditional food chain. Planktonic ciliates feed on nanoplankton (Heinbokel and Beers 1979; Capriulo 1983; Verity 1987) and picoplankton (Bernard and Rassoulzadegan 1993), while they are preyed upon by mesoplankton and fish larvae (Azam et al. 1983; Lavalpeuto et al. 1986; Pierce and Turner 1992, 1994). Thus, they play an important role in the transfer of energy and material through the entire pelagic food web (Beers 1967; Pierce and Turner 1992).

<footnote n="1">1 CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, People's Republic of China</footnote>

<footnote n="2">2 Laboratory for Marine Ecology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, People's Republic of China</footnote>

<footnote n="3">3 University of Chinese Academy of Sciences, Beijing 100049, People's Republic of China</footnote>

<footnote n="4">4 Center for Ocean Mega-Science, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao 266071, People's Republic of China</footnote>

<footnote n="5">5 Aix-Marseille University, Toulon University, CNRS, IRD, Mediterranean Institute of Oceanology UM110, 13288 Marseille, France</footnote>
The various genera of tintinnids have been divided into
several biogeographical types (cosmopolitan, neritic, warm-
water, boreal, and austral) according to their global occur-
rence (Pierce and Turner 1993; Dolan et al. 2013a). There-
fore, different biogeographical areas can be characterized
by different tintinnid assemblages (Li et al. 2016). In the
austral assemblage, Dolan et al. (2012) divided the austral
species (40°S–78°S) into Southern Ocean endemic species
(only found south of 40°S) and widespread species (those
with a geographic range extending into the Southern Ocean).
In Antarctic waters, ciliate abundance was observed in dif-
ferent habitats (oceanic areas, transitional areas, polynyas,
edges of glaciers, and edges of sea ice) in the Amundsen
Sea (e.g., Jiang et al. 2014, 2015, 2016) and the Weddell Sea
(e.g., Heinbokel and Coats 1986; Garrison and Buck 1989;
Garrison et al. 1991; Gowing and Garrison 1992). These
investigations generally evaluated ciliate assemblages at a
horizontal level while providing very little vertical distribu-
tion information. Plankton distribution has been found to
be closely related to water masses (Longhurst 2007), and
previous studies have provided evidence of different phy-
toplankton community structures in various water masses
(e.g., Stoecker et al. 1992; Mura et al. 1995; Zhang et al.
2012). Although water masses are well defined in the South-
ern Ocean (Tomczak and Godfrey 1994), no studies have
investigated the relationship between ciliates and different
water masses in this ocean to date.

There are several vertically divided water masses in
waters near Prydz Bay (East Antarctica) during austral
summer; namely, Summer Surface Water (SSW), Winter
Water (WW), Circumpolar Deep Water (CDW), Antarctic
Bottom Water (ABW) and Antarctic Shelf Water (ASW)
(Smith et al. 1984; Middleton and Humphries 1989; Le
et al. 1996; Vaz and Lennon 1996; Williams et al. 2010;
Shi et al. 2013). Moreover, upwelling occurs sporadically
in Prydz Bay (Lin et al. 2016). Bathymetrically, there is a
basin known as the Amery Depression located at a depth
of about 700 m seaward of the Amery Ice Shelf that shoals
gently to outer shelf banks at a depth of around 200 m (Gao
et al. 2013). Few studies have investigated ciliate assemblage
in Prydz Bay and its surrounding waters. Planktonic ciliates
were investigated at 0 and 5 m below sea ice at two stations
very close (3 km) to shore (Paterson and Laybourn-Parry
2012). In addition, ciliate abundances were determined at
a depth of 15 m in Prydz Bay, 5 km offshore from the Aus-
tralian Antarctic station of Davis (Davidson and Marchant
1992), but there is no record of tintinnid species in this area.
However, there have been studies of phytoplankton, zoo-
plankton, bacteria, and viruses in Prydz Bay and its adja-
cent areas without considering water masses (e.g., Zhu et al.
1994; Waters et al. 2000; Thomson et al. 2010; Liang et al.
2016). Moreover, Zhang et al. (2012) used flow cytometry
to show that the SSC (side scatter, optical parameter) signal

of picophytoplankton increased horizontally from out of the
bay to a coastal station without considering the vertical divi-
sion of water masses in Prydz Bay.

The notion that different water masses contain different indigenous species of plankton is the base of plankton biography (Longhurst 2007; Priede 2014), as well as the base of expatriate species (Angel 1993; Kobari et al. 2008), stray species (Dolan et al. 2012) and indicator species (e.g., Kato and Taniguchi 1993). Most of the biogeographical studies have been conducted in the horizontal division of water masses, however, we hypothesized that different ciliates have different preferred water masses in the vertical direction in Antarctic waters. Therefore, we compared the ciliate assemblages in different vertically divided water masses in open waters near Prydz Bay during austral summer. Our specific objectives were to compare (1) the contributions of aloricate ciliates and tintinnids to total abundance, (2) proportions of different-sized aloricate ciliates in total aloricate ciliate abundance, and (3) tintinnid species distributions in different water masses.

Materials and methods

Sampling was conducted at 34 stations in four South-North
transects (P2, P3, P4, P5) in open waters near Prydz Bay
(65°28′–73°3′E, 65°–68°S) (Fig. 1) onboard the R. V. “Xue-
long”, during the late austral summer (3–27 February) of
2015. The study area was outside of Amery Depression
and free of ice. The minimum and maximum depths of
the stations were 102 m (St. P2-9) and 3991 m (St. P5-2),
respectively. At each station, vertical profiles of temperature,
salinity and in vivo Chlorophyll *a* (Chl *a*) fluorescence were
determined from the sea surface to a depth of 300 m or 2 m
above the bottom when the water depth was <300 m using
the SBE911-conductivity-temperature-depth (CTD) unit.
Water masses were determined according to temperature
and salinity (Smith et al. 1984; Middleton and Humphries
1989; Le et al. 1996; Vaz and Lennon 1996; Williams et al.
2010; Shi et al. 2013).

Water was sampled using 10-L Niskin bottles on a rosette
CTD carrousel. Seawater samples of 1 L were collected
from each sampling point (surface, 25, 50, 75, 100, 150,
200, 300 m at each station), then fixed with Lugol's solution
(1% final concentration, $vv^{-1}$). A total of 264 water samples
were collected.

In the laboratory, each water sample was concentrated
to about 100 mL by gently siphoning out supernatant water
after allowing it to settle for at least 48 h. The settling and
siphoning processes were repeated to concentrate each sam-
ple to a final volume of ~50 mL. The concentrated sample
was then allowed to settle in an Utermöhl counting chamber
<figure><img src="image_3.png" /><figcaption>**Fig. 1** Sampling stations in open waters near Prydz Bay during the late austral summer. Red star Chinese Antarctic station of Zhongshan; Red circle Australian Antarctic station of Davis</figcaption></figure>

for at least 24 h, after which it was examined using an Olym-
pus IX 71 inverted microscope (×100 or ×400).

For each sample, the entire concentrated sample was
counted. A maximum of 25 mL of the concentrated sample
was examined in each count; therefore, at least two counts
were made to complete sample analysis. A smaller volume
was examined for each count when the microscopic view was
blurred because of the high concentration of phytoplankton.
The species present in low abundance (especially Antarctic
endemic species of tintinnids) were counted completely in

every count to ensure accuracy. Highly abundant species
were not counted if a high number was obtained in a pre-
vious count. Because mechanic and chemical disturbances
associated with collection and fixation procedures could
provoke detachment of the protoplasma from the loricae
(Paranjape and Gold 1982; Alder 1999), empty loricae of
tintinnid species were counted as living cells in this study.
In addition, some loricae might be empty when they were
sampled (Kato and Taniguchi 1993; Dolan and Yang 2017),
which might have resulted in overestimated numbers.
For each species, sizes (e.g., length or width, according to shape) of the cell (aloricate ciliate) or lorica (tintinnid, especially length and oral diameter) were measured for at least (if possible) 20 individuals in the entire study area. According to lorica morphology and size, tintinnids were identified to the species level according to references (Laackmann 1910; Kofoid and Campbell 1929, 1939; Hada 1970; Boltovskoy et al. 1990; Alder 1999; Zhang et al. 2012; Dolan et al. 2013b; Kim et al. 2013). Ciliate volumes were then estimated using appropriate geometric shapes (cone, ball, and cylinder). Tintinnid carbon biomass was estimated using the equation: C=lorica volume (µm³) × 0.053 + 444.5 (Verity and Langdon 1984). The conversion factor of carbon biomass for aloricate ciliates used in this study was 0.19 pg C µm⁻³ as defined by Putt and Stoecker (1989). Southern Ocean endemic species were defined according to Dolan et al. (2012).

## Data analysis

The occurrence frequency of each tintinnid species was calculated by dividing the total number of sampling points by the number of sampling points where this species occurred. Principal component analysis (PCA) was conducted using Canoco for Windows 4.5 software. For PCA, environmental variables included seawater temperature, salinity, Chl *a* and depth, while biological variables consisted of the abundance of 13 tintinnid species. Cluster analysis was conducted using the Primer 5 software. Group-average linkage based on the Bray–Curtis similarity matrix of the fourth root transformed tintinnid abundances was utilized.

## Results

### Hydrography and water mass division

The water column temperature (Fig. 2) showed obvious sandwich structures, with warm water (T > −1.5 °C) lying on and below a cold water (T < −1.5 °C) layer. We defined the cold-water belt (T < −1.5 °C) in the middle as WW, the warm water upon WW in the upper 50 m as SSW, and the warm water below WW as CDW. Upwelling occurred in transect P3 (Sts. 6, 7), P4 (Sts. 4–6), and P5 (Sts. 3–6). The upwelling in transects P4 and P5 were stronger, with −1.2 °C outcropping to the surface, while the upwelling was comparatively weak in Transect P3 with a temperature of only −0.8 °C outcropping to the surface. WW lied between 50 and 100 m on the offshore side of the transects, whereas it occupied the water column down to 300 m on the coastal side.

The salinity was less than 34 in the upper 50 m (SSW) at most stations, while WW and CDW exhibited higher

salinity (> 34) (Fig. 2). The position of salinity 34 isohaline was similar to that of the −1.5 °C isothermal underlying SSW. The in vivo Chlorophyll *a* (Chl *a*) decreased with depth, and the highest values (> 3 mg m⁻³) were limited to coastal sites in the upper 50 m of SSW, with a maximum value of 19.18 mg m⁻³ being observed at 4.5 m at St. P5-9. According to the spatial distribution of the concentration of Chl *a*, SSW was divided into an area with Chl *a* concentration > 3 mg m⁻³ near the shelf and another area with concentration < 3 mg m⁻³ in the north. The horizontal division of the two sectors overlapped with that of the upwelling, with the exception of transect P2, for which upwelling was not detected in SSW.

### Ciliate abundance and biomass in different water masses

Ciliate abundance and biomass decreased from SSW to CDW (Table 1, Figs. 3, 4, 5a). High ciliate abundance (>1000 ind. L⁻¹) and biomass (>4 µg C L⁻¹) occurred in SSW. The aloricate ciliate proportion accounted for > 57% of the total ciliate abundance in all water masses. Average abundances of aloricate ciliates and total ciliates in SSW<sub>Chl a>3</sub> (SSW, Chl *a* > 3 mg m⁻³) were less than in SSW<sub>Chl a<3</sub>, but their average biomasses were greater than in this fraction of water (Table 1, Fig. 5b). The proportion of tintinnids to the total ciliate abundance in SSW<sub>Chl a>3</sub> (38.2%) was much higher than in any other water masses (<13%), with CDW having the lowest tintinnid proportion (2.2%, Fig. 5b). In addition, SSW<sub>Chl a>3</sub> contained larger sized aloricate ciliates, with those in the 10–20 µm size class compromising <15% of the total aloricate ciliate abundance, while this value was more than 39% in other water masses (Fig. 5c).

Thirteen tintinnid species belonging to five genera were identified (Table 2, Fig. 6), and the occurrence frequencies and abundances of different tintinnids varied greatly. Generally, tintinnids with a higher occurrence frequency also had a higher abundance (both average abundance and maximum abundance, Online Resource 1). *Salpingella* sp. was the most abundant and frequent species, while *Amphorides laackmanni* was the least abundant (Table 2, Fig. 5d, Online Resource 1). Tintinnid total abundance in different water masses was different, with SSW<sub>Chl a>3</sub> having the highest average tintinnid total abundance (209 ind. L⁻¹) among all water masses (Fig. 5d, Table 1). The average abundance of all tintinnid species in CDW was low (<0.9 ind. L⁻¹) (Fig. 5d, Table 2).

There were seven Southern Ocean endemic tintinnid species (*Codonellopsis gaussi*, *Laackmanniella naviculaefera*, *Cymatocylis affinis/convallaria*, *C. antarctica*, *C. affinis/convallaria* forma cristallina, *C. affinis/convallaria* forma drygalskii and *C. vanhoeffeni*). *Laackmanniella naviculaefera*
<figure><img src="image_4.png" /><figcaption>**Fig. 2** Vertical distributions of temperature (T, °C), salinity (S), in vivo Chlorophyll *a* (Chl *a*) fluorescence along the transects (P2, P3, P4, P5) in open waters near Prydz Bay. Dot symbols indicate both the depths at which ciliates were sampled and the water masses where</figcaption></figure>

samples were collected (purple circle SSW; red diamond WW; green square CDW). Blue line: upwelling range at the 0-m depth. SSW: Summer Surface Water, WW: Winter Water, CDW: Circumpolar Deep Water

and *C. affinis/convallaria* forma cristallina were the most abundant endemic species in WW (Table 2). The average abundance of endemic species in SSW<sub>Chl *a* > 3</sub> was highest (Fig. 5d), and the Southern Ocean endemic species abundance in WW (>> 30%) was much higher than in other water masses (Fig. 5e).

## Tintinnid species in different water masses

Cluster analysis divided all tintinnid species into four groups according to their distribution (Online Resource 2). Species in groups I, II and III had higher occurrence frequencies, making it possible to study their distribution

pattern. Three main patterns corresponding to the three groups were identified according to their distribution characteristics (Figs. 7, 8, 9). Pattern 1 was defined by tintinnids that mainly occurred in SSW. These organisms were distributed in the surface or subsurface layer of SSW, but disappeared in the deep water. Tintinnids with this pattern were identified as *Salpingella* sp. and *C. gaussi*. The maximum abundance of *Salpingella* sp. was observed in the upper 25 m, while that of *C. gaussi* was found in the upper 50 m (Fig. 7, Online Resource 3). Pattern 2 was defined as tintinnids that mainly occurred in WW. These species (*Salpingella costata*, *S. faurei*, *C. affinis/convallaria* forma *drygal-skii* and *C. vanhoeffeni*) did not exist in the upper 25 m and
<table><caption>**Table 1** Variations of abundance ± SE (ind. L⁻¹) and biomass ± SE (µg C L⁻¹) of ciliates in different water masses</caption><thead><tr><th rowspan="3">Water masses</th><th colspan="2">Aloricate ciliates</th><th colspan="2">Tintinnids</th><th colspan="2">Total ciliates</th></tr><tr><th colspan="2">Abundance</th><th colspan="2">Abundance</th><th colspan="2">Abundance</th></tr><tr><th>Average</th><th>Range</th><th>Average</th><th>Range</th><th>Average</th><th>Range</th></tr></thead><tbody><tr><td>SSW<sub>Chl a &lt; 3</sub></td><td>584 ± 540</td><td>1–2770</td><td>2.1 ± 2.3</td><td>0.02–11.3</td><td>65 ± 79</td><td>0–346</td><td>0.3 ± 0.6</td><td>0–2.4</td><td>649 ± 559</td><td>22–2822</td><td>2.4 ± 2.4</td><td>0.02–11.5</td></tr><tr><td>SSW<sub>Chl a &gt; 3</sub></td><td>278 ± 196</td><td>2–733</td><td>3.8 ± 4.1</td><td>0.02–15.6</td><td>209 ± 253</td><td>6–1031</td><td>1.2 ± 1.4</td><td>0–7.4</td><td>487 ± 367</td><td>128–1337</td><td>4.9 ± 4.6</td><td>0.2–16.9</td></tr><tr><td>WW</td><td>209 ± 209</td><td>6–974</td><td>0.9 ± 1.0</td><td>0.02–5.3</td><td>19 ± 33</td><td>0–298</td><td>0.3 ± 0.4</td><td>0–1.8</td><td>228 ± 222</td><td>7–1031</td><td>1.2 ± 1.23</td><td>0.02–6.1</td></tr><tr><td>CDW</td><td>90 ± 83</td><td>2–326</td><td>0.3 ± 0.3</td><td>0.003–1.8</td><td>4 ± 11</td><td>0–36</td><td>0.01 ± 0.01</td><td>0–0.1</td><td>94 ± 90</td><td>3–344</td><td>0.3 ± 0.3</td><td>0.003–1.8</td></tr><tr><td>PB</td><td>259 ± 331</td><td>1–2770</td><td>1.28 ± 2.05</td><td>0.003–15.6</td><td>42 ± 107</td><td>0–1031</td><td>0.3 ± 0.7</td><td>0–7.4</td><td>301 ± 371</td><td>3–2822</td><td>1.6 ± 2.4</td><td>0.003–16.9</td></tr></tbody></table>

SSW<sub>Chl a &lt; 3</sub> Summer Surface Water with Chl *a* < 3 mg m⁻³, sampling points *n* = 51, SSW<sub>Chl a &gt; 3</sub> Summer Surface Water with Chl *a* > 3 mg m⁻³, sampling points *n* = 27, WW Winter Water, sampling points *n* = 119, CDW Circumpolar Deep Water, sampling points *n* = 67, PB Prydz Bay, sampling points *n* = 264

mainly occurred in the subsurface and stretched into deep water in WW in the coastal area, with a decreasing trend to the north (Fig. 8, Online Resource 3). Finally, *L. naviculaefera* and *C. affinis/convallaria* forma cristallina formed Pattern 3. These organisms inhabited both SSW<sub>Chl a &gt; 3</sub> and WW, and were distributed from the surface of SSW<sub>Chl a &gt; 3</sub> to deep water in WW (Fig. 9, Online Resource 3). These two species were the most abundant Southern Ocean endemic species in WW (Table 2). Species in group IV (*Codonelopsis glaucialis*, *C. affinis/convallaria*, *C. antarctica*, *Salpingella acuminata*, and *A. laackmanni*) occurred too rarely (occurrence frequency < 8%, Table 2) to show any obvious occurrence pattern (Online Resource 4).

Principal component analysis of the 264 samples and 13 tintinnid species was conducted to examine the contribution of the environmental variables to tintinnid species occurrence (Fig. 10). Two principal components discriminated the environmental conditions in three water masses. These components explained a large proportion (68.1%) of the variance, as well as 44.7 and 23.4% of the tintinnid species variation, respectively (Fig. 10). The first principal component was closely related to seawater depth, Chl *a*, *Salpingella* sp., *C. gaussi* and *C. glaucialis*. These three tintinnid species had a strong positive correlation with Chl *a* but a strong negative correlation with depth. Chl *a* had the greatest influence on *C. gaussi* and *C. glaucialis*. The second principal component was closely related to temperature, *S. costata*, *S. faurei*, *C. affinis/convallaria* forma drygalskii and *C. vanhoeffeni*, *C. affinis/convallaria* forma cristallina and *L. naviculaefera*. These species had a strong negative correlation with temperature (Fig. 10). Different tintinnid groups had different temperatures and Chl *a* preferences: those showing Pattern 1 occurring in warm water in the surface and those showing Pattern 2 being present in cold water. Tintinnid species in Pattern 3 occurred in cold water and warm water with high Chl *a* levels (Online Resource 5).

## Discontinuity of ciliate distribution

Isolines of low abundance of aloricate ciliates, tintinnids, and total ciliates showed upwelling in the corresponding horizontal position of the upwelling. The total ciliate abundance isoline of 200 ind. L⁻¹ upwelled in transects P3, P4 and P5, and even reached the surface in SSW in transect P5. The aloricate ciliate isoline of 200 ind. L⁻¹ was distributed in generally the same pattern as the total ciliate assemblage. The tintinnid abundance isoline of 40 ind. L⁻¹ reached the surface in SSW and defined areas of low abundance in surface water for all transects (Fig. 3). According to the tintinnid distribution (Figs. 7, 8, 9), there was an obvious low-abundance division area that split the tintinnid abundance distribution into two parts. The *Salpingella* sp. abundance distribution in Transect P3 could easily be split into two parts by the 5
<figure><img src="image_5.png" /><figcaption>**Fig. 3** Vertical distributions of abundance (ind. L⁻¹) of aloricate ciliate, tintinnid, and total ciliate along the transects (P2, P3, P4, P5) in open waters near Prydz Bay. Dot symbols indicate both the depths at which ciliates were sampled and the water masses where samples were collected (purple circle SSW; red diamond WW; green square</figcaption></figure>

CDW). Blue line: upwelling range at the 0-m depth. SSW: Summer Surface Water; WW: Winter Water; CDW: Circumpolar Deep Water. Red isotherm of -1.5 °C and green Chl a isoline of 3 mg m⁻³ were attached

ind. L⁻¹ isoline, while the 60 ind. L⁻¹ isoline split Transect P4 and P5 into two parts (Fig. 7). In the case of tintinnids with Patterns 2 and 3 (C. affinis/convallaria forma drygalskii, C. vanhoeffeni, S. costata, S. faurei, L. naviculaefera and C. affinis/convallaria forma cristallina), their distribution area was also divided by low abundance isolines, and their abundance was higher on the coastal side of the cold-water upwelling (Figs. 8, 9).

## Discussion

### Ciliate abundance and biomass in different water masses

Data concerning ciliate abundance and biomass are scarce in open waters near Prydz Bay. Paterson and Laybourn-Parry (2012) reported a maximum ciliate abundance of 3000 ind.
<figure><img src="image_6.png" /><figcaption>**Fig. 4** Vertical distributions of biomass (µg C L⁻¹) of aloricate, tintinnid, and total ciliate along the transects (P2, P3, P4, P5) in open waters near Prydz Bay. Dot symbols indicate both the depths at which ciliates were sampled and the water masses where samples were collected (purple circle SSW; red diamond WW; green square CDW). Blue line: upwelling range at the 0-m depth. SSW: Summer Surface Water; WW: Winter Water; CDW: Circumpolar Deep Water. Red isotherm of -1.5 °C and green Chl *a* isoline of 3 mg m⁻³ were attached</figcaption></figure>

L⁻¹ in the sea ice area 3 km offshore in April. In addition, higher ciliate abundance of 1.6×10⁵ ind. L⁻¹ was recorded at depth of 15 m at a site 5 km offshore from the Austral-ian Antarctic station of Davis in January (Davidson and Marchant 1992). The close proximity of these stations to the shoreline might explain their higher abundance. The aver-age ciliate abundance (301 ind. L⁻¹) and biomass (1.6 µg C L⁻¹) in this study were higher than during the same season in the Bellingshausen and Amundsen seas, where there were average ciliate abundance of 139 ind. L⁻¹ and a biomass of 0.34 µg C L⁻¹, respectively (Wickham et al. 2011). The tin-tinnid biomass ranged from 0.02 µg C L⁻¹ under the sea-ice

to 1.3 µg C L⁻¹ in the open water column in the Weddell Sea (Buck et al. 1992).

The proportion of tintinnid abundance to total ciliate abundance has been shown to be <20% in oceanic waters (Suzuki and Taniguchi 1998; Gómez 2007; Sohrin et al. 2010; Yu et al. 2016). Yu et al. (2016) found that tintinnid abundance was <10% in stations deeper than 80 m. In the present study, the proportion of tintinnids in SSW<sub>Chl *a*<3</sub> (SSW, in vivo Chlorophyll *a* <3 mg m⁻³) and WW was close to that of oceanic water. A higher tintinnid proportion was found in SSW<sub>Chl *a*>3</sub> than in other water masses. This phenomenon was consistent with the idea that tintinnids may be
<figure><img src="image_7.png" /><figcaption>**Fig. 5** Abundance of ciliate (a) and proportions of aloricate ciliate and tintinnid (b), proportions of different-sized aloricate ciliate in total aloricate ciliate abundance (c), abundances (d) and proportions (e) of different tintinnid species in different water masses. Southern</figcaption></figure>

Ocean endemic species were in red rectangle. SSW<sub>Chl a<3</sub>: Summer Surface Water with Chl *a* < 3 mg m<sup>-3</sup>; SSW<sub>Chl a>3</sub>: Summer Surface Water with Chl *a* > 3 mg m<sup>-3</sup>; WW: Winter Water; CDW: Circumpolar Deep Water

more favored than aloricate ciliates under eutrophic conditions in oceanic waters (Gómez 2007). Suzuki and Taniguchi (1998) also found that tintinnids were adapted to high Chl *a* concentrations.

The size class of aloricate ciliates has rarely been investigated. In our study, the percentages of different size class aloricate ciliates in different layers of a low Chl *a* concentration area was roughly the same as in the tropical Western Pacific (Wang et al. 2016). However, the size class of aloricate ciliates became larger in the higher Chl *a* concentration area. There were no similar results in other studies.

## Tintinnid species composition

This study was the first to investigate tintinnid species communities in open waters near Prydz Bay. A neritic assemblage has also been described in Antarctic waters (Dolan et al. 2013a). However, neritic genera (*Favella*, *Helicostomella*, *Leprotintinnus*, *Metacylis*, *Stenosemella*, *Stylicauda*, *Tintinnidium*, and *Tintinnopsis*) (Dolan et al. 2013a) were not found in the present study. These findings indicate that we did not identify the southernmost limit of the austral assemblage. The tintinnid assemblage might extend further south until it meets the neritic assemblage. However,

there has been only one investigation (Yu et al. 2016) of the expansion of neritic species to offshore areas. That study showed neritic species expanded from the coastal line to the 80-m (distance from bottom) isoline in the East China Sea. If this phenomenon is similar in the Antarctic, neritic species would be found in waters shallower than 80 m. However, the shallowest depth in our study was 102 m; therefore, it is assumed that neritic species did not occur in our study area. Thus, further studies should be conducted in nearshore areas to reveal the mixing between austral assemblage and neritic assemblages in Antarctic waters.

Dolan et al. (2012) divided tintinnid species reported from locations between 40°S and 78°S into Southern Ocean endemic species (32 species) and widespread species (161 species). In this study, we found seven Southern Ocean endemic species which was only a small part of the total endemic species list. Most endemic species did not emerge in our survey area, which was likely because their abundance was below the detection limit or they inhabited other areas of Antarctic waters. Dolan et al. (2013b) suggested that several species in the genus *Cymatocylis* were different morphotypes of *Cymatocylis affinis/convallaria*. Kim et al. (2013) classified *C. drygalskii* and *C. convallaria* as *C. affinis*, and *C. gaussi* as *Laackmanniella* (*L. naviculaefera* = *L. prolongata*).
<table><caption>**Table 2** Tintinnid species' distribution in different water masses in open waters near Prydz Bay</caption><thead><tr><th rowspan="3">Species</th><th colspan="8">Water masses</th></tr><tr><th colspan="2">SSW<sub>Chl a &lt; 3</sub></th><th colspan="2">SSW<sub>Chl a &gt; 3</sub></th><th colspan="2">WW</th><th colspan="2">CDW</th><th>PB</th></tr><tr><th>Abundance</th><th>OF</th><th>Abundance</th><th>OF</th><th>Abundance</th><th>OF</th><th>Abundance</th><th>OF</th><th>OF</th></tr></thead><tbody><tr><td>Codonellopsis gaussi</td><td>0.53 ± 1.78 (9)</td><td>7.23</td><td>2.76 ± 5.06 (18)</td><td>9.52</td><td>0.58 ± 2.75 (27)</td><td>4.52</td><td>0.05 ± 0.37 (3)</td><td>2.94</td><td>11.36</td></tr><tr><td>C. glacialis</td><td>0.22 ± 0.93 (6)</td><td>4.82</td><td>1.75 ± 5.06 (24)</td><td>5.95</td><td>0.41 ± 2.99 (32)</td><td>3.01</td><td>0.00</td><td>0.00</td><td>7.20</td></tr><tr><td>Cymatocylis affinis/ convallaria forma cristallina</td><td>1.06 ± 3.00 (12)</td><td>8.43</td><td>6.75 ± 12.31 (63)</td><td>17.86</td><td>1.54 ± 3.06 (16)</td><td>12.95</td><td>0.01 ± 0.12 (1)</td><td>2.94</td><td>25.00</td></tr><tr><td>C. affinis/convallaria</td><td>0.08 ± 0.45 (3)</td><td>2.41</td><td>0.11 ± 0.42 (2)</td><td>2.38</td><td>0.02 ± 0.13 (1)</td><td>0.60</td><td>0.01 ± 0.12 (1)</td><td>2.94</td><td>2.65</td></tr><tr><td>C. affinis/convallaria forma drygalskii</td><td>0.45 ± 1.43 (6)</td><td>6.02</td><td>0.41 ± 0.94 (3)</td><td>5.95</td><td>0.92 ± 1.92 (10)</td><td>9.94</td><td>0.01 ± 0.12 (1)</td><td>2.94</td><td>16.67</td></tr><tr><td>C. vanhoeffeni</td><td>0.20 ± 1.40 (10)</td><td>1.20</td><td>0.30 ± 1.55 (8)</td><td>1.19</td><td>0.55 ± 1.42 (8)</td><td>7.23</td><td>0.00</td><td>0.00</td><td>9.85</td></tr><tr><td>C. antarctica</td><td>0.00</td><td>0.00</td><td>0.00</td><td>0.00</td><td>0.11 ± 0.69 (6)</td><td>1.20</td><td>0.03 ± 0.24 (2)</td><td>2.94</td><td>1.89</td></tr><tr><td>Laackmanniella naviculaefera</td><td>4.97 ± 13.00 (72)</td><td>16.87</td><td>21.17 ± 28.88 (131)</td><td>25.00</td><td>3.34 ± 5.35 (32)</td><td>19.58</td><td>0.10 ± 0.55 (4)</td><td>8.82</td><td>39.02</td></tr><tr><td>Salpingella acuminata</td><td>0.00</td><td>0.00</td><td>0.00</td><td>0.00</td><td>0.17 ± 0.73 (6)</td><td>3.01</td><td>0.19 ± 0.74 (4)</td><td>17.65</td><td>6.06</td></tr><tr><td>S. costata</td><td>1.43 ± 8.99 (64)</td><td>3.61</td><td>0.00</td><td>0.00</td><td>3.81 ± 18.71 (201)</td><td>13.55</td><td>0.42 ± 1.69 (10)</td><td>20.59</td><td>20.83</td></tr><tr><td>S. faurei</td><td>0.59 ± 2.42 (16)</td><td>6.02</td><td>0.45 ± 1.83 (9)</td><td>2.38</td><td>2.91 ± 9.99 (79)</td><td>10.54</td><td>0.29 ± 1.88 (15)</td><td>11.76</td><td>17.42</td></tr><tr><td>Salpingella sp.</td><td>55.51 ± 80.26 (346)</td><td>43.37</td><td>174.98 ± 255.15 (1014)</td><td>28.57</td><td>3.88 ± 11.30 (91)</td><td>12.05</td><td>0.87 ± 4.58 (36)</td><td>23.53</td><td>40.91</td></tr><tr><td>Amphorides laackmanni</td><td>0.00</td><td>0.00</td><td>0.34 ± 0.87 (5)</td><td>1.19</td><td>0.55 ± 3.61 (33)</td><td>1.81</td><td>0.01 ± 0.12 (1)</td><td>2.94</td><td>3.03</td></tr></tbody></table>

In each water mass are displayed the average abundance ± SE (ind. L⁻¹) of each tintinnid species with its maximum value (ind. L⁻¹) in parenthesis as well as its occurrence frequency (%)

OF occurrence frequency of each tintinnid species calculated by dividing the total number of sampling points by the number of sampling points where this species occurred, $SSW_{Chl a < 3}$ Summer Surface Water with $Chl a < 3$ mg m⁻³, sampling points $n=51$, $SSW_{Chl a > 3}$ Summer Surface Water with $Chl a > 3$ mg m⁻³, sampling points $n=27$, WW Winter Water, sampling points $n=119$, CDW Circumpolar Deep Water, sampling points $n=67$, PB Prydz Bay, sampling points $n=264$

Therefore, we considered *C. drygalskii*, *C. cristallina* and *C. convallaria* to be polymorphic forms and combined them under the name *C. affinis/convallaria*. However, this was not done for *C. antarctica* and *C. vanhoeffeni* because of their very different morphotypes. In addition, *L. naviculaefera* and *C. gaussi* were treated as different species because they showed distinct morphologies in our study.

In this study, *C. affinis/convallaria* forma cristallina was the dominant morphotype, and *C. affinis/convallaria* forma affinis and convallaria occurred occasionally in Prydz Bay. However, *C. affinis/convallaria* forma convallaria was dominant in Admiralty Bay (King George Island) in austral summer, occupying up to 90% of the total tintinnid proportion, while *C. affinis/convallaria* forma cristallina did not appear (Wasik and Mikolajczy 1994). This distinct difference might reflect geographic differences of tintinnid occurrence.

In the present study, *Salpingella* sp. was the most abundant species, which was consistent with the results of previous studies. For instance, the maximum abundance of *Salpingella* sp. reached 1300 ind. L⁻¹ at a nearshore site in Signy Island (Leakey et al. 1994) and 380 ind. L⁻¹ in the ice-edge zone of the Weddell Sea (Buck et al. 1992).

Based on pictures and the size of lorica observed in previous studies (Heinbokel and Coats 1985; Buck et al. 1992), the *Salpingella* sp. observed in the present study may be the same as that of *Salpingella* sp. #1 observed in the Weddell Sea (Buck et al. 1992).

All Southern Ocean endemic tintinnid species except for *C. gaussi* were limited to the onshore side of the transects from 65°S to 67.51°S in the present study. Similarly, *C. affinis/convallaria* forma drygalskii was defined as most abundant in the ice-covered coastal zone in the Belling-shausen Sea (Alder and Boltovskoy 1991), while it was dominant in the Amundsen Sea, where it tended to be distributed near the shore (Jiang et al. 2014). In another study, *C. affinis/convallaria* forma drygalskii was almost entirely restricted to the region between 74°S and the Filchner Ice-shelf (Boltovskoy et al. 1989).

## Indigenous tintinnid species in water masses determined their vertical distribution

Because some tintinnid species had higher abundance in a certain water mass than in other water masses, we took them
<figure><img src="image_8.png" /><figcaption>**Fig. 6** Photos of some tintinnid species in open waters near Prydz Bay. **a** *Laackmanniella naviculaefera*, **b** *Salpingella* sp., **c** *S. faurei*, **d** *Codonellopsis glacialis*, **e** *C. gaussi*, **f** *Cymatocylis affinis/conval-***</figcaption></figure>

laria, **g** *C. affinis/convallaria* forma *drygalskii*, **h** *C. affinis/conval-***
laria forma cristallina, **i** *C. vanhoeffeni*

to be indigenous species of this water mass. All the indig-
enous species form indigenous assemblages of this certain
water mass. In this study, SSW indigenous assemblage was
composed of *Salpingella* sp. and *C. gaussi*, WW indigenous

assemblage included *S. costata*, *S. faurei*, *C. affinis/conval-
laria* forma *drygalskii* and *C. vanhoeffeni*, and there was
no indigenous assemblage in CDW. The tintinnid assem-
blage in one certain water mass was a mixture of indigenous
<figure><img src="image_9.png" /><figcaption>**Fig. 7** Vertical distribution of abundance (ind. L⁻¹) of tintinnid species (Pattern 1) in open waters near Prydz Bay. Dot symbols indicate both the depth at which ciliates were sampled and the water masses where samples were collected (purple circle SSW; red diamond WW;</figcaption></figure>

green square CDW). Blue line: upwelling range at the 0-m depth. SSW: Summer Surface Water; WW: Winter Water; CDW: Circumpolar Deep Water. Tintinnid pictures were attached

tintinnids of this water mass and those indigenous to other water masses in addition to some occasional species. Our results supported the hypothesis that different ciliates have different preferred water masses.

Although previous studies of tintinnids in Antarctic waters did not define any tintinnid species–water mass relationship, some studies have investigated their vertical distribution (e.g., Boltovskoy and Alder 1992; Kivi and Kuosa 1994; Christaki et al. 2008). Since water masses were vertically divided in our study area, we were able to compare our results with these previous studies. In our study, *Salpingella* sp. and *C. gaussi* mainly inhabited SSW, which was consistent with the results of previous studies that showed they were present in higher abundance in surface waters. For example, the abundance of *Salpingella* sp. was higher in the upper 50 m than in deeper waters in the ice-edge zone of the Weddell Sea (Buck et al. 1992). *C. gaussi* (maximum 40.3 ind. L⁻¹) mainly existed in the upper 50 m of the ice-edge zone in the Weddell Sea (Boltovskoy and Alder 1992).

Four species (*S. fauri*, *S. costata*, *C. affinis/convallaria* forma *drygalskii* and *C. vanhoeffeni*) were mainly found in WW in this study. No specific vertical distribution pattern of these species was reported in previous studies.

Boltovskoy and Alder (1992) reported that *Salpingella* sp. was mainly distributed in deep water (> 100 m) in the Weddell Sea. This species distribution pattern was similar to that of *S. fauri* and *S. costata* observed in the present study. Because there was no concrete species information about *Salpingella* sp. reported in Boltovskoy and Alder (1992), we suggest that the *Salpingella* sp. observed in their study might be the *S. fauri* or *S. costata* found in the present study.

In the present study, *C. affinis/convallaria* forma *crystalina* and *L. naviculaefera* were found in high abundance in SSW<sub>Chl a>3</sub> and WW. *L. naviculaefera* is a surface species for which the maximum abundance (131 ind. L⁻¹) was observed at 25 m in our study. This species has previously been reported to be present in maximum abundance (40.2 ind. L⁻¹) at 50 m in the Weddell Sea (Boltovskoy and Alder 1992). To the best of our knowledge, there is no vertical distribution data for *C. affinis/convallaria* forma *cristalina* in the available literature. Other species like *A. laackmanni* and *C. antarctic* with no concrete pattern were rare in our study and we did not find any previous distribution data regarding these species.
<figure><img src="image_10.png" /><figcaption>**Fig. 8** Vertical distribution of abundance (ind. L⁻¹) of tintinnid species (Pattern 2) in open waters near Prydz Bay. Dot symbols indicate both the depth at which ciliates were sampled and the water masses where samples were collected (purple circle SSW; red diamond WW;</figcaption></figure>

green square CDW). Blue line: upwelling range at the 0-m depth. SSW: Summer Surface Water; WW: Winter Water; CDW: Circumpolar Deep Water. Tintinnid pictures were attached

## Influences of upwelling on ciliate distribution

Another characteristic of the distribution pattern is the influence of upwelling. Although this upwelling has long been

recognized (Middleton and Humphries 1989), its influence on plankton distribution has not been investigated to date. The combined effects of the coast and upwelling could be responsible for Chl *a* intensification in surface waters at
<figure><img src="image_11.png" /><figcaption>**Fig. 9** Vertical distribution of abundance (ind. L⁻¹) of tintinnid species (Pattern 3) in open waters near Prydz Bay. Dot symbols indicate both the depth at which ciliates were sampled and the water masses where samples were collected (purple circle SSW; red diamond WW;</figcaption></figure>

green square CDW). Blue line: upwelling range at the 0-m depth. SSW: Summer Surface Water; WW: Winter Water; CDW: Circumpolar Deep Water. Tintinnid pictures were attached

the coastal ends of the transects. Upwelling occurred in the same location in which low abundance of surface ciliates and some tintinnid species occurred. Because deep water had low ciliate abundance, we propose that this upwelling was responsible for the low abundance areas. *L. naviculaefera* and *C. affinis/convallaria* forma cristallina occurred in WW, and were the most abundant Southern Ocean endemic species in WW. Therefore, these two species might be more adaptive than other endemic species in WW. We speculate that these two species might be the original inhabitants in WW. When WW was brought to the surface by upwelling, these two species were able to survive and prosper, while others perished. Because the upwelling moved both upward and coastward, these two species occurred in $SSW_{Chl a>3}$ but not in $SSW_{Chl a<3}$.

Upwelling in Prydz Bay is a part of the “Antarctic divergence” which generally occurs at 60°S–65°S, although it shows great variations with time (Mann and Lazier 2006; Lin et al. 2016). Thus, the influence of upwelling on ciliate distribution in our study might have occurred in other Antarctic waters in which upwelling was found.

## Prediction of spatial and temporal variations of austral tintinnid assemblage

Because different water masses inhabited different indigenous assemblages, we predicted tintinnid assemblages in other areas and times according to the spatial and temporal variations of water masses in the Southern Ocean. The sandwich structures of SSW, WW, and CDW stretched from waters near Prydz Bay northward until Antarctic Circumpolar Current (ACC) mixed the water layers. Therefore, we speculate that the distributions of austral tintinnid assemblages were similar in waters from our study area to those of ACC.

According to data recorded at the Chinese Antarctic Station of Zhongshan, air temperature was the highest in January (http://polar.chinare.gov.cn/meteo/). Our study was conducted at the end of austral summer, when WW was at its minimum range. As time went on, SSW gradually disappeared and was replaced by WW; thus, WW occupied more of the surface water. Therefore, in winter, the abundance of the dominant species, *Salpingella* sp.
<figure><img src="image_12.png" /><figcaption>**Fig. 10** Principal component analysis (PCA) of tintinnid ciliate abundance and different seawater samples associated with environmental variables. The x-axis is the first PCA axis, and the y-axis is the second PCA axis.</figcaption></figure>

Environmental variables and tintinnid species are indicated by red arrows and black arrows, respectively

(which was indigenous in SSW), will decrease. Tintinnid species indigenous in WW might move northward and upward to the surface waters, resulting in the increase of their proportion.

We do not have species information regarding aloricate ciliates; however, the aloricate assemblage might utilize the same mechanism as tintinnid species because of their close phylogenetic relationship. Although there have been no reports on other plankton differences in different water masses in the Antarctic, this mechanism might also exist in phytoplankton and zooplankton.

In summary, the results of this study supported our hypothesis that different water masses had ciliate assemblages with different characteristics and indigenous tintinnids. Tintinnid vertical distribution could be determined by whether they were indigenous to water masses. Our results will help predict the spatial and temporal variations in assemblages of ciliates and other plankton according to the dynamics of water masses in Antarctic waters.

**Acknowledgements** We thank the 31st CHINARE Antarctic expedition for providing logistical support and environmental data. We thank Jeremy Kamen, MSc, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of a previous version of this manuscript. This study was supported by the National Natural

Science Foundation of China (NSFC 41576164); Chinese Polar Environment Comprehensive Investigation & Assessment Programmes (CHINARE2015-01-06 and CHINARE2015-01-05); the Scientific and Technological Innovation Project by Qingdao National Laboratory for Marine Science and Technology (No. 2015ASKJ02); and the CNRS-NSFC Joint Research Projects Program (NSFC 41711530149).

## Compliance with ethical standards

**Conflict of interest** The authors declare that they have no conflicts of interest.

**Ethical standards** All procedures involving animals were performed in accordance with the ethical standards of the institutions at which the studies were conducted

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<figure><img src="image_13.png" /></figure>

**Online Resource 1** Relationship between occurrence frequency and maximum abundance (●), and average abundance (▲) of each tintinnid species. (1) *Salpingella* sp.; (2) *Laackmanniella naviculaefera*; (3) *Cymatocylis affinis/convallaria* forma cristallina; (4) *Salpingella costata*; (5) *Salpingella faurei*; (6) *Cymatocylis affinis/convallaria* forma drygalskii; (7) *Codonellopsis gaussi*; (8) *Cymatocylis vanhoeffeni*; (9) *Codonellopsis glacialis*; (10) *Salpingella acuminata*; (11) *Amphorides laackmanni*; (12) *Cymatocylis affinis/convallaria*; (13) *Cymatocylis antarctica*
<figure><img src="image_14.png" /></figure>

**Online Resource 2** Cluster analysis using group-average linkage based on the Bray-Curtis similarity matrix of fourth root transformed tintinnid abundances in all sampling points. (group I) tintinnid species in Pattern 1; (group II) tintinnid species in Pattern 2; (group III) tintinnid species in Pattern 3; (group IV) tintinnid species with no distribution pattern
<figure><img src="image_15.png" /></figure>

**Online Resource 3** Vertical scatter distribution of typical tintinnid species in three patterns. (a) Pattern 1: tintinnid mainly occurred in SSW; (b) Pattern 2: tintinnid mainly occurred in WW; (c) Pattern 3: tintinnid occurred in both SSW<sub>Chl a>3</sub> and WW. SSW: Summer Surface Water; WW: Winter Water; SSW<sub>Chl a>3</sub>: Summer Surface Water with Chl a>3 mg m<sup>-3</sup>
<figure><img src="image_16.png" /><figcaption>**Online Resource 4** Vertical distribution of abundance (ind. L⁻¹) of tintinnid species with no distribution pattern in open waters near Prydz Bay. Dot symbols indicate both the depth at which ciliates were sampled and the water masses where samples were collected (● SSW; ◆ WW; ■ CDW). SSW: Summer Surface Water; WW: Winter Water; CDW: Circumpolar Deep Water</figcaption></figure>
<figure><img src="image_17.png" /></figure>

**Online Resource 5** Seawater temperature T (°C) and Chl *a* in the sampling points in open waters near Prydz Bay. Different sizes of red circles indicate different abundances (ind. L⁻¹) of typical tintinnid species in three patterns in the sampling points. Solid blue dots mean sampling points where this species did not occur. (a) Pattern 1: tintinnids mainly occurred in SSW; (b) Pattern 2: tintinnids mainly occurred in WW; (c) Pattern 3: tintinnids occurred in both SSW<sub>Chl a>3</sub> and WW. SSW: Summer Surface Water; WW: Winter Water; SSW<sub>Chl a>3</sub>: Summer Surface Water with Chl *a*>3 mg m⁻³. Horizontal and vertical dashed line indicate Chl *a* value of 3 mg m⁻³ and temperature of -1.5 °C, respectively