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Progress in studies on the diversity and distribution of planktonic ciliates (Protista, Ciliophora) in the South China Sea

  • Corresponding author: Yehui Tan, tanyh@scsio.ac.cn
  • Received Date: 2020-05-28
    Accepted Date: 2020-07-01
    Published online: 2020-11-06
  • Edited by Jiamei Li.
  • As an important component of microzooplankton, ciliates play a key role in matter cycling and energy flow in marine planktonic ecosystems. Studies of planktonic ciliate have been extensive in the South China Sea (SCS) over the last 20 years. Here, we summarize the recent progress on the diversity and distribution of this group in the SCS. This includes that in: (1) the waters covering the intertidal zone of the northern SCS, most studies have focused on taxonomy, with 71 species collected, identified, and described (with ~ 40% new species); (2) neritic waters distribution patterns have been examined at a regional scale, with ciliates displaying significant spatial variations and seasonal dynamics; (3) in oceanic waters, there has been a focus on ciliate distribution in north, centre, and south regions, where mesoscale physical processes play roles in controlling distributions, and noticeable vertical variations occur. More generally, some studies examine the influences of environment variables on ciliates, and indicate that chlorophyll a concentration is commonly positively correlated with ciliates abundance. In addition, some significant findings are summarized, the limitations of past studies are considered, and recommendations are made for future work on planktonic ciliates in SCS.
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Progress in studies on the diversity and distribution of planktonic ciliates (Protista, Ciliophora) in the South China Sea

    Corresponding author: Yehui Tan, tanyh@scsio.ac.cn
  • 1. Key Laboratory of Tropical Marine Bio-Resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
  • 2. Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China
  • 3. Innovation Academy of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences, Guangzhou 510301, China
  • 4. Department of Biological Science, University of Ulsan, Ulsan 680749, South Korea
  • 5. Laboratory of Protozoology, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, School of Life Science, South China Normal University, Guangzhou 510631, China

Abstract: As an important component of microzooplankton, ciliates play a key role in matter cycling and energy flow in marine planktonic ecosystems. Studies of planktonic ciliate have been extensive in the South China Sea (SCS) over the last 20 years. Here, we summarize the recent progress on the diversity and distribution of this group in the SCS. This includes that in: (1) the waters covering the intertidal zone of the northern SCS, most studies have focused on taxonomy, with 71 species collected, identified, and described (with ~ 40% new species); (2) neritic waters distribution patterns have been examined at a regional scale, with ciliates displaying significant spatial variations and seasonal dynamics; (3) in oceanic waters, there has been a focus on ciliate distribution in north, centre, and south regions, where mesoscale physical processes play roles in controlling distributions, and noticeable vertical variations occur. More generally, some studies examine the influences of environment variables on ciliates, and indicate that chlorophyll a concentration is commonly positively correlated with ciliates abundance. In addition, some significant findings are summarized, the limitations of past studies are considered, and recommendations are made for future work on planktonic ciliates in SCS.

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Introduction
  • Planktonic ciliates are common members of microplankton communities, ranging in size from ten to hundreds of micrometres; they are morphologically diverse and usually dominate the microzooplankton community with abundances of tens of thousands per litre (Lynn 2008). In marine food webs, they play a major role by grazing on pico- and nanoplankton while serving as prey for metazoans. Thus, they act as mediators of energy flow (Azam and Malfatti 2007), with 5-60% of primary production gazed by planktonic ciliates and transferred to higher trophic levels (e.g., Montagnes et al. 2010) and inorganic nutrients supplied to biogeochemical recycling (e.g., Dolan 1997). Also, they contribute significantly to heterotrophic biomass and production in the marine ecosystems due to their high growth rates (McManus and Santoferrara 2013; Pierce and Turner 1992).

    Many studies on the diversity and spatial patterns of marine planktonic ciliates have been conducted around the world. For instance, studies have focused on European waters, such as the Baltic (e.g., Mironova et al. 2009) and the Mediterranean Seas (e.g., Bachy et al. 2014; Dolan 2000; Pitta and Giannakourou 2000); waters of North America, in particular the New England Shelf (e.g., Grattepanche et al. 2015; Santoferrara et al. 2014); and across the Southwestern Atlantic Shelf (e.g., Thompson and Alder 2005; Thompson et al. 2001). In addition, some investigations of biogeography at an oceanic scale have been conducted in Atlantic (e.g., Rychert et al. 2014), Pacific (e.g., Gómez 2007; Sohrin et al. 2010) and Indian Oceans (e.g., Zhang et al. 2017). Moreover, the global diversity patterns of ciliates have been studied during the Tara Oceans Voyage (Gimmler et al. 2016). In contrast to studies that examine spatial diversity, ones that focus on the taxonomy of this group have primarily been conducted along the coasts of Europe and China (e.g., Agatha 2011; Song et al. 2009). More recently, molecular methods have been applied to studies of planktonic ciliates. For example, DNA fingerprinting (DGGE) has revealed that the ciliates communities are variable onshore but are more constant in open waters of the Northeast American Shelf (Grattepanche et al. 2016), high-throughput sequencing (HTS) has revealed high spatial variation of ciliates in a tropical estuary (Sun et al. 2017), and DNA barcoding has been used to examine global and local biogeographic patterns of tintinnids (Santoferrara et al. 2018). Despite all of these efforts, we still lack an understanding of several fundamental aspects associated with the diversity and spatial patterns of planktonic ciliates, and the local and global environmental factors governing these remain unresolved (Agatha 2011; Fenchel and Finlay 2004; Fenchel et al. 1997; Foissner et al. 2008). The South China Sea (SCS) may be a useful location to explore these issues.

    The SCS is the largest semi-enclosed basin in the western Pacific Ocean with an area of ~ 3.3 million km2 (Su 2004) and hosts various physical-chemical environments and a diversity of microplankton (Li et al. 2012; Song et al. 2012). Studies on ciliates of the SCS were initiated in 1947 when some costal planktonic ciliates were described morphologically (Nie and Cheng 1947). No further studies were performed until the 1990s when two investigations on marine biodiversity, including ciliates, were conducted in the southern SCS (Xu et al. 1994, 1996). Since 2007, studies on the diversity and distribution of ciliates in the SCS have increased, leading to 55 related papers (Fig. 1a). Among these studies, new ciliates species have been described based on morphological and molecular methods (Liu et al. 2009, 2011b, c, 2012, 2013b, 2015b, c, 2016c, 2019; Shen 2018; Song et al. 2013, 2015a, b, 2018a, b, 2019; Wang et al. 2018b; Xu and Bai 1998b), the temporal and spatial dynamics of ciliate communities have been analysed (Feng et al. 2010; Liu et al. 2010a, 2016a; Tan et al. 2010; Xu et al. 1998a; Yu et al. 2014a, c), and relationships between ciliates and their environment have been examined (Su et al. 2007, 2008; Wang et al. 2013, 2014; Wu et al. 2016a, 2017a). Most of the studies have focused on subdivisional districts of the SCS. For example, the taxonomic studies are mostly limited to waters covering the intertidal zone, and those on community characters of ciliate have been mostly carried out in the neritic and oceanic waters (Fig. 1b). This uneven distribution of studies prevents our overall understanding on the diversity and distribution of ciliates, highlighting the necessity to consider the SCS as a whole.

    Figure 1.  The statistics of existing papers on ciliates in the South China Sea (SCS) in each year (a) and area (b)

    Here, to improve our overall knowledge and understanding of ciliates in the SCS, we summarize recent progress on the diversity and distribution of planktonic ciliates. Considering the wide distribution of studies, we reviewed them based on three geographical regions: the intertidal zone (waters covering the area between the low and high tides), the neritic zone (beyond the intertidal zone and above the continental shelf), and the oceanic zone (from the shelf break to the deep sea). It should be clarified that in this review, the results from previous studies are mostly based on morphological identification. The few studies applying molecular methods are treated independently, recognising that in the future, this approach should be pursued.

Intertidal waters
  • Over the last 10 years, studies on the diversity of planktonic ciliates in the intertidal water of northern SCS have mainly focused on their taxonomy (Table 1). It should be noted that, apparently for pragmatic reasons, samples were collected from waters overlying the intertidal zone. However, planktonic ciliates isolated from these waters undoubtedly also occur in neritic and possibly oceanic waters (see below). Therefore, it should not be assumed that the ciliates are endemic to the waters covering the intertidal zone, and we do not discuss the distribution of endemic intertidal species here, although the extent to which they occur might be an avenue for further investigation.

    No. Longitude and latitude Year of sampling Month of sampling Number of species Number of new reports Location Habitat References
    1 110.03° E, 20.003° N 2017 Oct 1 0 Haikou Reef Bai et al.(2019)
    2 2006–2016 10 0 Zhanjiang/Guangzhou/Shenzhen/Huizhou/Hong Kong Wetland/Estuary/Mariculture/Beach/Reef/Dock/Harbour Liu et al.(2019)
    3 110.40° E, 21.20° N/110.41° E, 21.37° N 2012/2013 Nov/Oct 2 2 Zhanjiang Harbour/Mangrove Song et al.(2019)
    4 2003–2010 10 0 Zhanjiang/Daya Bay Beach/Mariculture Ma et al.(2019)
    5 114.27° E, 22.27° N 2014 Dec 1 1 Hong Kong Dock Shen et al.(2018)
    6 109.5° E, 18.23° N/110.6° E, 20.01° N/110.55° E, 21.23° N/113.98° E, 22.5° N 2013/2014/2018 Apr/Jun/Nov 3 1 Zhuhai/Sanya/Zhanjiang/Haikou Estuary/Harbour/Wetland Song et al.(2018b)
    7 113.98° E, 22.5° N/110.55° E, 20.1° N/110.60° E, 21.23° N 2014/2014/2013 May/Apr/Oct 3 2 Zhuhai/Haikou/Zhanjiang Estuary/Wetland/– Song et al.(2018a)
    8 110.4° E, 21.37° N 2013 Oct 1 1 Zhanjiang Mangrove Wang et al.(2018b)
    9 110.4° E, 21.2° N 2009/2010/2010 Dec/Mar/Mar 3 2 Zhanjiang Harbour Liu et al.(2016c)
    10 114.9° E, 22.7° N/110.7° E, 21.6° N 2009/2010 May/Mar 2 2 Daya Bay/Zhanjiang Littoral zone/Mangrove Liu et al.(2015b)
    11 114.07° E, 22.61° N/113.67° E, 22.67° N/114.53° E, 22.71° N 2008/2009/2009 Apr/Apr/May 3 3 Shenzhen/Guangzhou/Daya Bay Mangrove/Mariculture/– Liu et al.(2015c)
    12 110.43° E, 21.15° N/110.31° E, 21.1° N 2010/2013 Mar/Nov 2 1 Zhanjiang Mangrove Song et al.(2015a)
    13 113.61° E, 22.75° N/110.41° E, 21.38° N/110.4° E, 21.2° N 2013/2013/2013 May/Oct/Nov 3 3 Guangzhou/Zhanjiang/Zhanjiang Estuary/Mangrove/- Song et al.(2015b)
    14 114.53° E, 22.71° N/109.43° E, 21.37° N/109.75° E, 21.51° N 2007/2010/2010 Nov/Mar/Mar 3 3 Daya Bay/Zhanjiang/Zhanjiang Dock/Mangrove/Mangrove Liu et al.(2013b)
    15 114.53° E, 22.71° N/114.07° E, 22.61° N 2007/2008 Aug/Apr 2 0 Daya Bay/Shenzhen –/Mangrove Song et al.(2013)
    16 114.07° E, 22.61° N 2008 Dec 1 0 Shenzhen Jiang et al.(2012)
    17 114.53° E, 22.71° N/113.91° E, 22.49° N/114.53° E, 22.71° N 2007/2008/2007 Apr/Dec/Nov 3 2 Daya Bay/Shenzhen/Daya Bay –/Harbour/– Liu et al.(2012)
    18 2008 Nov–Dec 16 0 Daya Bay Zhang et al.(2012)
    19 114.53° E, 22.71° N 2007 Dec 1 1 Daya Bay Harbour Liu et al.(2011b)
    20 114.07° E, 22.61° N/114.54° E, 22.71° N 2008/2008 Apr/Mar 3 1 Shenzhen/Daya Bay Mangrove/- Liu et al.(2011c)
    21 114.07° E, 22.61° N 2008 Jan/Mar 2 2 Shenzhen Mangrove Liu et al.(2009)
    22 1 1 Daya Bay Xu et al.(1998b)
    23 1933/1934 51 10 Hainan Island Nie and Cheng (1947)
    — data not available

    Table 1.  Taxonomy studies on ciliate in South China Sea

    From these intertidal waters, 71 species belonging to 24 genera, 12 families, and four orders have been identified (Fig. 2) (Hu et al. 2019). In most of these studies, ciliates morphologies were reported from live and protargol stained specimens, and their phylogenies were analysed based on the SSU rDNA sequences. Moreover, 29 species were recognized as new, based on which new higher-level taxa were established (four genera, one family, and one order) (Liu et al. 2019). Similar taxonomic studies have been conducted in the Bohai and Yellow Seas (Bai et al. 2020b; Song et al. 2009), where 51 species have been found (unpublished data of the authors). The higher species richness of planktonic ciliates in SCS compared with Bohai and Yellow Seas supports the suggestion that the SCS is a diversity hotspot for ciliates (Hu et al. 2019; Jiang et al. 2012; Ma et al. 2019; Zhang et al. 2012). Song et al.(2009) predicted there are 2000 ciliate species in all marine water. However, recent estimation indicated that 83-89% of ciliates are undescribed (Agatha 2011). The high proportion (41%) of new species relative to the total species richness in SCS suggests that there are many unknown species in this area.

    Figure 2.  Some common planktonic ciliate species reported in taxonomy studies in the intertidal zone of SCS. a Antestrombidium wilberti Liu et al., 2015. b Spirostrombidium subtropicum Liu et al., 2013. c Spirostrombidium apourceolare Liu et al., 2013. d Pelagostrobilidium paraepacrum Liu et al., 2012. e Novistrombidium sinicum Liu et al., 2009. f Parallelostrombidium ellipticum Liu et al., 2015. g Spirostrombidium schizostomum (Kahl, 1932) Xu et al., 2006. h Novistrombidium orientale Liu et al., 2009. i Omegastrombidium elegans (Florentin, 1901) Agatha, 2004. j Strombidium pseudostylifer Song et al., 2015. k Strombidium conicum (Lohmann, 1908) Wulff, 1919. l Varistrombidium kielum (Maeda & Carey, 1985) Xu et al., 2011. m Pseudotontonia simplicidens (Lynn, & Gilron, 1993) Agatha, 2004. n Strombidium guangdongense Liu et al., 2016. o Sinistrostrombidium cupiformum Liu et al., 2015. p Apostrombidium orientale Song et al., 2019. q Parallelostrombidium jankowskii (Xu et al., 2009) Song et al., 2017. r Strombidium capitatum (Leegaard, 1915) Kahl, 1932. s Parallelostrombidium conicum Liu et al., 2013. t Strombidium basimorphum Martin & Montagnes, 1993. u Pelagostrobilidium simile Song & Bradbury, 1998. v Strombidium tropicum Liu et al., 2015. w Pelagostrobilidium minutum Liu et al., 2012. x Strombidinopsis minima (Gruber, 1884) Song & Bradbury, 1998. y Parallelostrombidium obesum Liu et al., 2015. z Strombidium cuneiforme Song et al., 2015. aa Cyrtostrombidium paralongisomum Tsai et al., 2015. ab Strombidinopsis cheshiri Montagnes & Taylor, 1994. ac Strombidinopsis minima (Gruber, 1884) Song & Bradbury, 1998. ad Novistrombidium apsheronicum (Alekperov & Asadullayeva, 1997) Agatha, 2003. ae Strombidinopsis elongata Song & Bradbury, 1998. af Lynnella semiglobulosa Liu et al., 2011. ag Strombidinopsis sinicum Liu et al., 2016. ah Novistrombidium testaceum (Anigstein, 1914) Song & Bradbury, 1998. ai Spirotontonia turbinata (Song & Bradbury, 1998) Agatha, 2004. aj Favella campanula (Schmidt, 1901) Jörgensen, 1924. ak Tintinnopsis tubulosa Levander, 1900. al Tintinnopsis acuminata (Daday, 1887) Kofoid & Campbell, 1929. am Amphorellopsis acuta (Schmid, 1901) Kofoid & Campbell, 1929. an Tintinnopsis lohmanni (Jörgensen, 1927) Laackmann, 1906. ao Tintinnopsis tentaculata (Nie & Cheng, 1947). ap Tintinnopsis tocantinensis Kofoid & Campbell, 1929. aq Tintinnopsis cylindrica Daday, 1887. ar Tintinnopsis elongata Daday, 1887. as, at Tintinnopsis beroidea Stein, 1867

    Liu et al.(2019) summarized the results of several diversity and faunal studies on planktonic ciliate in typical habitats of the intertidal zone of northern SCS and found that the order Oligotrichida represents the most abundant taxon, with the highest species richness, and is widely distributed in all habitats. The family Strombidiidae and the genus Strombidium comprise the highest proportion of all planktonic ciliate at family and genus levels, respectively. Similarly, these taxa are also found to dominate the ciliates community in other areas, such as the Yellow Sea, Northwest and South Atlantic Ocean, Baltic Sea, and Mediterranean Sea (Agatha 2011; Dolan and Marrasé 1995; Mironova et al. 2009; Santoferrara and Alder 2009; Song et al. 2009). Given that the family Strombidiidae possesses the highest species number of the planktonic ciliates, its high species richness in these studies is easily explained. Finally, the diversity of planktonic ciliates in five typical intertidal habitats of the northern SCS (mangrove, estuary, mariculture, beach, docks) was compared, indicating that mangrove wetland, with their high environmental heterogeneity, supported the highest species richness (Liu et al. 2019).

Neritic waters
  • In the SCS, the neritic waters are widely impacted by various coastal processes, such as riverine plumes, upwelling, and human activity (Su 2004). These processes play important roles in controlling the distribution of ciliate and are patchily distributed in neritic waters. Therefore, the ciliate communities also show spatial variation (Li et al. 2019; Tan et al. 2010; Wu et al. 2016a).

    Several studies on the spatial variations of ciliates in the SCS neritic waters were conducted in typical bays and estuaries along the south coast of China (Fig. 3a; Table 2). Tan et al.(2010) investigated the ciliates community in Sanya Bay and identified 58 species in 33 genera. They found that a high abundance of ciliates generally appeared in the estuary and associated coastal areas (Fig. 3f). Their results showed the area near coral reefs displayed a low abundance of planktonic ciliates, which was thought to be attributed to the high feeding rate of coral on ciliates (Ferrier et al. 1998). The distributions of ciliates in different aquaculture environments in Nan'ao were compared by Wu et al.(2016a, 2019). The results revealed that the species number and abundance were higher in an oyster-seaweed mixed culture area and non-aquaculture area, and lower in a caged fish culture area (Fig. 3d). Because the water exchange was weak and light transmission was low in the caged fish culture area, the growth of phytoplankton was limited, which apparently led to low ciliate abundance (Wu et al. 2016a). Wu et al.(2016b, 2017b) examined the distributional variation of ciliates in four areas of Daya Bay, and found that the species number was at a maximum at an artificial reef and at a minimum in an aquaculture area, but the abundance at the aquaculture area was significantly higher than three other areas (Fig. 3g). Their results also indicated that species diversity, evenness, and richness were higher in samples from less polluted areas (Fig. 3g), supporting the feasibility of using ciliates as marine environmental indicators (Wu et al. 2016b). The distributions of tintinnid ciliates along Pearl River Estuary were studied by Li et al.(2019), and ~ 43 species in 15 genera were found, in which freshwater, brackish, and marine species occurred in sequence along the salinity gradient. Their results revealed that peak abundance occurred at mesohaline and polyhaline regions (Fig. 3c), while species richness was lowest at oligohaline regions and highest at polyhaline regions (Li et al. 2019).

    Figure 3.  Studies on the distributions of planktonic ciliates in the neritic area of SCS. a Location of research area in SCS. b Distribution of planktonic ciliates abundance in Maowei Sea in January and April (from Liu et al. 2016a). c Distribution of tintinnids abundance along salinity gradient in Pearl River Estuary (from Li et al. 2019). d Distribution of planktonic ciliates abundance in Baisha Bay (from Wu et al. 2016a). e Distribution of tintinnids abundance in Tieshan Harbour in spring and summer (from Yu et al. 2014a, b, c). f Distribution of planktonic ciliates abundance in Sanya Bay (from Tan et al. 2010). g Distribution of planktonic ciliates abundance in Daya Bay as well as their seasonal variation (from Wu et al. 2016b, 2017a). h Seasonal variations of tintinnids abundance in Shantou coastal water (from Liu et al. 2011a, b, c)

    No. Longitude (°E) Latidute (°N) Year of sampling Month of sampling Number of sites Number of species Groups Area Habitat References
    1 108.25–109.88 20.1–21.47 2011 Apr 19 36 All ciliates Beibu Gulf Oceanic Wang et al. (2013)
    2 108.25–109.88 20.1–21.47 2011 Aug 21 101 All ciliates Beibu Gulf Oceanic Wang et al. (2014)
    3 109.4–110.0 21.2–21.6 2010 Apr/Aug 8 8/13 Tintinnids Tieshan Harbour Neritic Yu et al. (2014a)
    4 110–120 18–23.25 2007 Aug 36 44 Tintinnids Northern SCS Oceanic Liu et al. (2010b)
    5 113.5–118 18–23.5 2007 Aug 13 38 All ciliates Northern SCS Oceanic Liu et al. (2010a)
    6 116.6–117.2 23–23.6 2007 Apr/Nov 5 14 Tintinnids Shantou coast Neritic Liu et al. (2011a)
    7 111–115.4 6.9–11 2011 Aug 11 30 All ciliates Southern SCS Oceanic Liu et al. (2016b)
    8 108.45–108.62 21.72–21.88 2012 Jan/Apr 16 18/21 All ciliates Maowei Sea Neritic Liu et al. (2016a)
    9 108.45–108.62 21.72–21.88 2011 Dec 16 19 All ciliates Maowei Sea Neritic Liu et al. (2015a)
    10 109.5–113.5 5–19.5 2010 May 14 22 All ciliates SCS Oceanic Liu et al. (2013a)
    11 114.25–116.77 18.9–20.97 2015 Nov 16 53 Tintinnids Northern SCS Oceanic Wang et al.(2018a, b)
    12 113.4–114.2 21.6–23.2 2014/2015/2017 Oct/Oct/Jun/Jun/Mar/Apr 19/41/36/26/29/35 30/26/16/16/19/22 Tintinnids Pearl River Estuary Neritic Li et al. (2019)
    13 111–117 18.5–22 2009 Jan/Apr 18 −/22 Tintinnids Northern SCS Oceanic Yu et al. (2014b)
    14 109.48–113.23 17.43–21.43 2007 Dec 82 49 Tintinnids Northern SCS Oceanic Zhang et al. (2010)
    15 107.25–109.75 18.75–21.35 2009 Aug 12 20 Tintinnids Beibu Gulf Oceanic Yu et al. (2014c)
    16 109.48–113.23 17.43–21.43 2007 Oct 82 22 Tintinnids Northern SCS Oceanic Feng et al. (2010)
    17 117.06–117.1 23.45–23.48 2014 Apr/Aug 13 19/28 All ciliates Shen'ou Bay Neritic Wu et al. (2019)
    18 114.5–114.8 22.5–22.7 2014 Jan/Apr/Aug/Nov 12 41 All ciliates Daya Bay Neritic Wu et al. (2016b)
    19 114.5–114.83 22.5–22.83 2014 Jan/Apr/Aug/Nov 6 11/21/14/13 All ciliates Dapeng Cove Neritic Wu et al. (2017a)
    20 114.5–114.83 22.5–22.83 1997 Apr 20 9–29 All ciliates Dapeng Cove Neritic Xu et al.(1998a, b)
    21 117.06–117.1 23.45–23.5 2014 Apr 13 19 All ciliates Baisha Bay Neritic Wu et al. (2016a)
    22 109.3–116.5 5.4–11.6 2013 Nov 18 17 All ciliates Southern SCS Oceanic Wu et al. (2016c)
    23 112–118.5 8.5–15 2016 Oct 10 20 All ciliates Central SCS Oceanic Xie et al. (2018)
    24 109.33–109.5 18.18–18.3 2004 Aug 12 58 All ciliates Sanya Bay Neritic Tan et al. (2010)
    25 110.5–120 14–22.25 2004 Sep 5 17 All ciliates Northern SCS Oceanic Su et al. (2007)
    26 116.75–117.9 21.7–22.75 2013/2014 Apr/Jun/Apr/Jul 5 79 All ciliates Northeastern SCS Oceanic Sun et al. (2019)
    27 109.33–109.5 18.2–18.25 2006 Apr 6 102 All ciliates Sanya Bay Neritic Su et al. (2008)
    28 108–118 4.0–12.0 1993/1994 May/Apr 44 All ciliates Nansha Islands Oceanic Xu et al. (1994)
    29 108–118 4.0–12.0 1994 Sep 40 75 All ciliates Nansha Islands Oceanic Xu et al. (1996)
    30 114.5–114.8 22.5–22.7 2014 Jan/Apr/Aug/Nov 12 41 All ciliates Daya Bay Neritic Wu et al. (2017b)
    31 109.45 18.02 2014 Apr 1 79OTU All ciliates Sanya Bay Neritic Wang et al. (2017)
    32 2006–2018 71 All ciliates Coastal area of Guangdong Intertidal Hu et al. (2019)
    33 2015 5 60OTU All ciliates Coastal area of Guangdong Intertidal Lu et al. (2020)
    — data not available

    Table 2.  Community studies on ciliate in South China Sea

    In the SCS neritic zone, environmental (e.g., temperature light) and physical (e.g., river runoff, currents) factors displayed seasonal dynamics, which elsewhere can influence ciliate communities and lead to a seasonal patterns (e.g., Bojanić et al. 2005; Sun et al. 2017). In Daya Bay, the number of ciliate species in the summer was higher than in other seasons, while the highest abundance occurred in spring (Wu et al. 2017a). Moreover, a clear seasonal shift of the taxonomic composition was revealed in this study, i.e., the dominant taxa were oligotrichids in spring but changed to tintinnids in the other three seasons (Wu et al. 2017a) (Fig. 3g). In the Tieshan Harbour, Yu et al.(2014a) found that the ciliate species number, abundance, diversity, and evenness in the summer were higher than in the spring. In the Maowei Bay, the ciliate community also exhibited temporal fluctuations, with higher total abundance and species number in the wet season than in the dry season (Fig. 3b), which was thought to be associated with the seasonal variations of phytoplankton abundance (Liu et al. 2016a). In the Shantou coastal area, tintinnid diversity was higher but their abundance was lower in the fall compared to the spring (Fig. 3h); this was considered to be a response to the seasonal variation of salinity and temperature impacted by river runoff and upwelling (Liu et al. 2011a). Consistent with findings in other seas (e.g., Bojanić et al. 2005; Johansson et al. 2004; Mironova et al. 2012; Urrutxurtu 2004), the high abundance of ciliates usually occurred in summer or wet season in SCS. These high abundances may be explained by the typically warm water temperatures and high Chl-a levels during the summer, i.e., in general, there is often a positive correlation between temperature, Chl-a and ciliates abundance (e.g., Sun et al. 2017; Urrutxurtu 2004).

Oceanic water
  • In oceanic areas of the SCS, a range of mesoscale physical processes occur, such as monsoons, upwelling, and eddies (Chen et al. 2011; Jing et al. 2008; Su 2004). These processes give rise to variation in environmental characters across spatial domains and influence the distributions of planktonic ciliates (Liu et al. 2010a; Wang et al. 2014; Zhang et al. 2010).

    Many studies on the distributions of ciliates have been conducted in the oceanic areas of northern SCS (Fig. 4a; Table 2). Wang et al.(2013, 2014) investigated the ciliate community in the Beibu Gulf, where 36 and 101 species were found in the spring and the summer, respectively. The horizontal distribution patterns showed that abundance and richness were generally high in the areas near the coast (Fig. 4b) (Wang et al. 2014). They also found that the main driver of this pattern was a south-westerly wind, which strengthened the intrusion of water from the south, caused the mixture of water in northern area, and thus produced a high concentration of nutrients and Chl-a as the food for ciliates (Wang et al. 2014). Tintinnid ciliates were investigated in the eastern SCS off Hainan and Leizhou, where 49 and 22 species were found, respectively (Feng et al. 2010; Zhang et al. 2010). Additionally, these studies revealed that the abundance and biomass of tintinnids decreased from nearshore to offshore (Fig. 4c). In the north-eastern SCS, 44 tintinnids were recorded (Liu et al. 2010b). Similar to the findings in eastern SCS off Hainan and Leizhou, the abundance and richness of tintinnids in the north-eastern SCS also displayed a decreasing trend from nearshore to offshore. These findings are consistent with some studies in other seas of the world. For example, mean abundance of ciliates decreased twofold from the shelf-slope to oceanic waters in south-western Atlantic (Santoferrara and Alder 2009), and alpha diversity of planktonic ciliates decreased with increasing distance from shore in New England shelf (Doherty et al. 2010). In nearshore areas, upwelling is common and will introduce nutrients, generating high phytoplankton biomass that may act as food for ciliates, resulting in the high abundance and richness closer to the coast (Wang et al. 2014).

    Figure 4.  Studies on the distributions of planktonic ciliates in the oceanic area of SCS. a Location of sampling sites in SCS. b Distribution of planktonic ciliates abundance in Beibu Gulf (from Wang et al. 2014). c Distribution of tintinnids abundance in northwestern SCS (from Feng et al. 2010). d Distribution of planktonic ciliates abundance in southern SCS (from Wu et al. 2016c). e Abundance of planktonic ciliates in each sampling site in central SCS (from Xie et al. 2018). f Spatial changes of planktonic ciliates abundance and species number along the latitude gradient in SCS (from Liu et al. 2013a, b). g Abundance of planktonic ciliates in each sampling site in northern SCS (from Liu et al. 2010a). h Spatial variations of planktonic ciliates abundance in 0 m and 75 m depth water of southern SCS (from Liu et al. 2016b)

    Compared with the extensive studies in the northern SCS above, investigations of ciliates in the central and southern SCS are less common. Xie et al.(2018) identified 20 planktonic ciliates species in the central SCS, and found that the tintinnids were richest in terms of species number, while the aloricate ciliates dominated the community in terms of abundance (Fig. 4e). In the southern SCS, 30 and 17 ciliate species were recorded by Liu et al.(2016b) and Wu et al.(2016c), respectively. Similar to that in the central area, the species richness of tintinnids was distinctively higher than that of aloricated species, in both studies. These findings differ from most studies in other seas, where aloricates usually represented most of the ciliates species (Gimmler et al. 2016; Mironova et al. 2009; Pitta and Giannakourou 2000). Given that the central and southern SCS are located in a tropical, oligotrophic area (Su 2004), the particular hydrological environment may shape unique planktonic ciliate communities there. In terms of spatial distribution, ciliates abundance was patchy in the southern SCS (Fig. 4d, h), where nutrient levels and Chl-a concentration were considered as the most important factors affecting the spatial pattern of ciliates (Wu et al. 2016c). On a larger scale, the distribution of ciliates along a latitudinal gradient in the SCS was examined by Liu et al.(2013a), who identified 22 ciliates, and found that abundance and species richness increased from the equator to 16° N (Fig. 4f). This observation agrees with the general latitudinal trends that both abundance and species richness increase away from the equator, reaching a peak at ~ 15-20° (Dolan and Pierce 2013; Rychert et al. 2014).

    The oceanic waters of the SCS present remarkable biochemical and physical depth-gradients, to a maximum depth of > 5000 m (Shaw and Chao 1994). These provide a structured environment and generate different ecological layers, leading to substantial dispersal limitation and environmental selection among layers for ciliates. Sun et al.(2019) found that the mesopelagic zone exhibited comparable alpha diversity to surface waters, with high diversity occurring at the interface with the euphotic zone (Fig. 5e-g). In this study, vertical variations of ciliate composition were mainly present in the relative abundances of the classes Spirotrichea and Oligohymenophorea (Fig. 5h). Moreover, bacterivorous and commensal/parasitic ciliates were considered to be an important component of the food web in the mesopelagic zone, due to their high abundance (Sun et al. 2019). Wang et al.(2018a) explored the vertical distribution of ciliate in the northern SCS slope and found that ciliates abundance displayed a surface peak (Fig. 5a, b). This pattern is similar to the results in the Bay of Fundy (Middlebrook et al. 1987), but different from most findings in other seas where peak abundances appear in the deep chlorophyll maximum (DCM) (Dolan 2000; Sohrin et al. 2010). One possible explanation for this surface peak in the SCS slope is that the DCM might be upwelled to the surface, which commonly happened in slope areas (Wang et al. 2018a). In addition, the seasonal dynamics of the vertical distribution of ciliates were investigated in northern SCS (Yu et al. 2014b). In this study, abundance and biomass usually showed high values in the surface or intermediate layers in the summer, while in the winter, ciliates tended to accumulate in the sub-surface layers (Fig. 5c, d).

    Figure 5.  Studies on the vertical distributions of planktonic ciliates in the oceanic area of SCS. a, b Location of sampling sites (a) and vertical distribution of tintinnids abundance in four transects (b) in slope areas of northern SCS (from Wang et al. 2018a, b). c, d Location of sampling sites (c) and the seasonal variations of vertical distribution of tintinnids abundance along two transects (d) in northern SCS (from Yu et al. 2014a, b, c). e-h Ciliate community in mesopelagic waters in northern SCS (from Sun et al. 2019), showing the location of sampling sites (e), the ciliates species richness in different depths (f), the vertical variation of ciliate community revealed by PCoA (g), and the vertical variation of ciliates compositions (h)

Application of molecular methods
  • Molecular methods, such as high-throughput sequencing (HTS), have been widely used in ecological studies of ciliates in recent decades (Bachy et al. 2013; Grattepanche et al. 2016; Santoferrara et al. 2018; Stock et al. 2013). For ciliates in the SCS, only three studies have applied molecular methods. Using HTS, Lu et al.(2020) examined species diversity in the subclass Oligotrichia in the intertidal zone of five cities of Guangdong, recognising 60 operational taxonomic units (OTUs). In this study, the city of Shenzhen had the highest OTUs and sequences among the five sampling sites (Fig. 6a), and Strombidium was the most abundant and widely distributed genus in this area, as revealed in other studies with morphology methods (Liu et al. 2019). During a one-day time-series study in Sanya Bay, the species diversity and community structure of oligotrich ciliates were analysed using a DNA clone library (Wang et al. 2017). In their results, 79 OTUs were detected, and the species diversity decreased from morning to midday but increased from nightfall to midnight (Fig. 6c). Sun et al.(2019) compared the morphology and HTS methods in their study on the diversity of ciliates in mesopelagic waters of the SCS (Fig. 6d). They found HTS can reveal a more diverse assemblage of ciliates than microscopic examination (575 OTUs vs. 79 morphospecies) (Fig. 6b), but both approaches captured similar vertical distribution patterns of ciliate communities. Additionally, HTS revealed that the species of the classes Spirotrichea and Oligohymenophorea dominated the ciliate communities in their study. This agrees with finding obtained using the same method in the circumglobal Tara Oceans expedition (Gimmler et al. 2016), in which these two classes accounted for 73% of the total ciliate species richness.

    Figure 6.  Application of molecular methods in studies of planktonic ciliates in SCS. a Numbers of OTUs and sequences of planktonic ciliates revealed by high-throughput sequencing (HTS) at five sites along the coast of Guangdong (from Lu et al. 2019). b Vertical distribution of alpha diversity (OTU richness and number of species) of ciliate in northern SCS revealed by HTS-V4 amplicon and morphological methods (from Sun et al. 2019). c Rarefaction curves of OTU diversity of ciliates revealed by clone library at different sampling time in Sanya Bay (from Wang et al. 2017). d Molecular (HTS) and morphology (QPS) examination of ciliate composition at class, order, family and genus levels in northern SCS (from Sun et al. 2019)

Relationships between ciliates and environment
  • It is well known that the distribution of ciliates is affected by the environment (Dolan and Pierce 2013; Jiang et al. 2011). In the SCS, the relationships between the ciliate community and environmental variables have also been investigated. Both biotic (e.g., phytoplankton, bacteria, predators) and abiotic factors (e.g., temperature, salinity, nutrients) have been found to play roles in controlling ciliate communities, with the main drivers varying spatially and temporally (Wu et al. 2016a, 2017a).

    Consistent with studies in other locations, such as the Mediterranean Sea (Dolan and Marrase 1995), Southwest Atlantic Ocean (Santoferrara and Alder 2012), and Irish Sea (Montagnes et al. 1999), Chl-a concentration was revealed to have a strong positive relationship with ciliates abundance in the SCS (Feng et al. 2010; Liu et al. 2010a, b; Tan et al. 2010; Yu et al. 2014a). The correlation with Chl-a concentration, on the one hand, indicates the response of ciliates to food availability. On the other hand, it may result from high relative abundance of ciliates containing chloroplasts or endosymbionts, such as Mesodium, which can contribute significantly to the Chl-a (Dierssen et al. 2015; Montagnes et al. 1999). Further studies have investigated the relationships between ciliates and different size fractions of Chl-a in the SCS and have revealed that the ciliate abundance and species number were positively correlated to micro-sized and nano-sized phytoplankton Chl-a concentrations (Liu et al. 2010a, b).

    Predators also may play a role in controlling ciliate communities by top-down interactions (Gómez 2007; Sinistro 2010). In Maowei Bay of the SCS, both positive and negative correlations among the dominant groups of mesozooplankton and ciliates were observed, suggesting that the different ciliates were preferred by selected mesozooplankton species and the predation effects of mesozooplankton on ciliates were taxon-specific (Liu et al. 2015a).

    Temperature and salinity have been identified as significant physical factors impacting ciliate communities in different ecosystems (Forster et al. 2012; Gimmler et al. 2016; Weisse et al. 2001). In the SCS, ciliate abundances were positively correlated with sea surface temperature in Maowei Bay (Liu et al. 2016a), possibly as growth of ciliates is strongly correlated with temperature (Beaver and Crisman 1990; Mieczan 2008). The effects of salinity on ciliates have been studied in estuaries of the SCS, where ciliate species number and abundance both showed negative relationship with salinity (Liu et al. 2010a; Yu et al. 2014b). This inverse relationships may be explained by that the low-salinity water from river discharge providing more food for ciliates (Liu et al. 2010a; Rakshit et al. 2016; Yu et al. 2014b).

    Studies in the SCS have also suggested that the ciliates are affected by nutrients (e.g., NO3-, NO2-, soluble reactive phosphorus). For example, ciliate communities in the northern Beibu Gulf were more closely related to the level of nitrogen (total, nitrate, and nitrite) and phosphorus (total and active), in which nitrogen played a crucial role, followed by phosphorus (Wang et al. 2014). In Tieshan Harbour, total nitrogen was considered as one of the key factors correlated to the tintinnids community (Yu et al. 2014a). The significant effect of nitrite on ciliates was also observed in a global investigation on the correlations between environment and ciliates during the Tara Oceans voyage (Gimmler et al. 2016). The reasons for these associations between nutrients and ciliate are twofold: nutrients can enhance phytoplankton growth and, thus, indirectly influence heterotrophic ciliates that feed on phytoplankton, and nutrients can be directly taken up by autotrophic ciliates (Wang et al. 2014; Wichham et al. 2015).

    In addition, the response of different ciliate species to environmental factors was discussed in some studies in the SCS. In Nan'ao, Mesodinium rubrum and Tintinnopsis beroidea, were significantly positively correlated with Chl-a (Wu et al. 2019). Strombidium globosaneum, Tintinnopsis minuta, and Strombidium conicum, showed more sensitivity to dissolved oxygen, pH, and chemical oxygen demand, whereas Tintinnopsis parvula and Tintinnopsis chinglanensis were significantly related to NO2- (Wu et al. 2019). In Daya Bay, some tintinnids were significantly, positively correlated with nutrients, particularly with nitrogenous nutrients, whereas aloricate ciliate species showed more sensitivity to salinity and temperature (Wu et al. 2016b).

    These findings, above, indicated that planktonic ciliate can reflect the environmental status, and support the notion that they can be considered as favourable bioindicator of marine water quality, as commonly applied in previous studies (e.g., Jiang et al. 2011; Xu et al. 2008). Moreover, considering the variation in responses of different species to environmental factors, the application of ciliates in environmental assessment should consider their specific indicative roles to each environmental factor at a species level.

Summary of some significant findings in SCS
  • Arising from this review are some notable findings on the diversity and distribution of planktonic ciliates in the SCS, as a contribution to our knowledge of ciliates in global marine waters.

    1.Similar to the findings in other seas, such as the Yellow Sea, the northwest Atlantic Ocean, the Baltic Sea, and the Mediterranean Sea (Agatha 2011; Mironova et al. 2009; Song et al. 2009), in terms of species richness, the order Oligotrichida dominates planktonic ciliate communities in the SCS. This supports the global dominance of oligotrichs and their typically high richness (Agatha 2011).

    2.In neritic waters of the SCS, high diversity and abundance of ciliates usually occurred in the summer or wet season, reflecting seasonal trends in other areas of the world (Bojanić et al. 2005; Johansson et al. 2004; Mironova et al. 2012; Urrutxurtu 2004). These trends may be explained by the significant and positive correlations between temperature, Chl-a, and ciliates abundance (Urrutxurtu 2004).

    3.The abundance and diversity of ciliates in the oceanic waters of the SCS display a decreasing trend from onshore to offshore area. This finding is consistent with most studies in other seas of the world (e.g., Doherty et al. 2010; Santoferrara and Alder 2009). Monsoons and upwellings were thought to play a main role in structuring the ciliate community in the oceanic waters (Wang et al. 2014). Moreover, in the central and southern SCS, ciliate abundance displayed a patchy pattern, which may be explained by the patchiness of their prey (Wu et al. 2016c).

    4.The mesopelagic zone of the SCS exhibited comparable alpha diversity to surface water. Based on their abundance, bacterivorous and commensal/parasitic ciliates species were identified as an important component of the food web in the mesopelagic zone (Sun et al. 2019). In the northern SCS slope, ciliate abundance displayed a surface peak in vertical direction (Wang et al. 2018a), which differs from most findings in other seas where peak abundances appeared in DCM (Dolan 2000; Sohrin et al. 2010). One possible explanation for this surface peak is that the DCM might upwell to the surface (Wang et al. 2018a).

Limitation and prospect
  • Although studies on planktonic ciliates in the SCS have increased in the last 20 years, their diversity and distribution remain poorly appreciated, and some gaps exist.

    1.There remains a need for taxonomy work. Although many new planktonic ciliate taxa have been reported in the SCS, the species number continues to increase, demonstrating that the diversity of these ciliates is higher than previously supposed (Bai et al. 2020a; Hu et al. 2019; Liu et al. 2017; Song et al. 2018a). Moreover, due to the lack of necessary taxonomy data, such as morphological and molecular markers, for many rare species, an accurate species-level identification cannot be achieved in most community studies. To solve this problem, comprehensive and detailed taxonomy data should be obtained, based on more extensive taxonomy studies. Furthermore, past studies may have misidentified species (due to poor resources for identification), resulting in low reliability when comparing the ciliate communities from different studies. For example, species number and abundance sometimes distinctively differ between studies, even from the same area. Therefore, professional background or training in ciliate taxonomy should be encouraged for researchers to increase the accuracy of results (Agatha 2011; Song et al. 2009).

    2.The community coverage of ciliates has been low. Many studies in the SCS have investigated the community of planktonic ciliate by only focusing on several common taxonomic groups (e.g., the loricated tintinnids). However, in terms of abundance and species number, tintinnids account for less than 20% of all ciliates in most waters (e.g., Wang et al. 2013; Yu et al. 2014b; Zhang et al. 2010). To understand ciliate ecology, a more rigorous assessment of their diversity should be included in future studies.

    3.The coverage of the SCS is uneven. Most studies have been conducted in the coastal and north SCS, and some have been confined to intertidal zone waters. In contrast, work conducted in centre and south of the SCS is limited. However, the central and southern areas comprise the main part of the SCS and are characterized by the tropical and deep-sea environments, which may play an important role in shaping a unique ciliate community. To provide a comprehensive understanding of the distribution of ciliates in the SCS, more attention could be paid to the central and southern areas.

    4.Molecular techniques, such as HTS, transcriptomics, and genomics, have rarely been applied in the SCS (Lu et al. 2020; Sun et al. 2019; Wang et al. 2017). Compared with traditional microscope observation, molecular techniques do not rely on taxonomy knowledge but can provide objective results. Moreover, some studies have indicated that molecular methods can reveal higher diversity of ciliates than morphological identification, as they recognise rare and atypical taxa (Santoferrara and McManus 2017). Therefore, molecular techniques should be used in the future to explore the diversity and distribution of ciliates in the SCS.

    5.Although the influences of several factors on ciliates community have been widely examined, most of the studies in the SCS have focused on correlations between abiotic environmental variables and ciliates. Rarely have they estimated the roles of biotic factors in their community structuring. As an intermediate link in energy transfer within the microbial food web, the ciliate community can also be effected by their preys and predators (Li et al. 2016; Liu et al. 2015a). To reveal the driving mechanism of distribution of ciliate in the SCS, studies should be conducted that combine the effects of the abiotic and biotic factors on ciliates.

  • Acknowledgements

  • This work was supported by the Science and Technology Planning Project of Guangzhou (No. 202002030489), Guangdong MEPP Fund [No. GDOE (2019) A23], Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0405), and Natural Science Foundation of China (No. 32070517, 41576124, 31772440, 31761133001). Many thanks are given to Dr. David Montagnes (University of Liverpool) for his kind suggestions to improve the manuscript.

  • Author contributions

  • WWL wrote the manuscript. MKS, ZZY and YHT discussed the results and revised the manuscript. WWL and YHT developed the concept and designed the outline. All authors read and approved the final version of the manuscript.

Compliance with ethical standards

    Conflict of interes

  • The authors declare that they have no conflict of interest.

  • Animal and human rights statement

  • This article does not contain any studies with human participants or animals performed by any of the authors.

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