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).
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).