Journal of Oceanology and Limnology   2021, Vol. 39 issue(6): 2220-2236 PDF
http://dx.doi.org/10.1007/s00343-021-0242-7
Institute of Oceanology, Chinese Academy of Sciences
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#### Article Information

YAN Tao, LIN Mingqing, CAO Wenhao, HAN Shuaishuai, SONG Xikun
Fouling characteristics of cnidarians (Hydrozoa and Anthozoa) along the coast of China
Journal of Oceanology and Limnology, 39(6): 2220-2236
http://dx.doi.org/10.1007/s00343-021-0242-7

### Article History

accepted in principle Jan. 16, 2020
accepted for publication Dec. 27, 2020
Fouling characteristics of cnidarians (Hydrozoa and Anthozoa) along the coast of China
Tao YAN1,2,3, Mingqing LIN1,2, Wenhao CAO1,3, Shuaishuai HAN1,4, Xikun SONG5
1 CAS Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China;
3 CAS Key Laboratory of Marine Environmental Corrosion and Bio-fouling, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
4 Guangzhou CAS Test Technical Services Co., Ltd., Guangzhou 510650, China;
5 State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China
Abstract: Hydrozoans and anthozoans are an important component of a great variety of marine communities, particularly abundant and ubiquitous as part of the fouling assemblages around the globe. Several negative impacts have been associated to their occurrence on artificial substrata. In the coastal waters of China, a total of 76 species of fouling cnidarians were observed and classified. According to the occurrence frequency or biomass, the major species in the Bohai and Yellow Seas were Ectopleura marina, Bougainvillia sp., and Eudendrium capillare; in the East China Sea Anthopleura nigrescens, Diadumene lineata, and Ectopleura crocea; and in the South China Sea Clytia sp., Obelia sp., and Actiniaria spp. The peak period of settlement of most species was mainly in summer and autumn. With the decrease of latitude, species number increased greatly and even cnidarian fouling was observed all year round in the East and South China Seas. Salinity was another factor affecting species distribution. Naturally, immersion time of substrata also directly affects the characteristics of cnidarians in fouling communities.
Keywords: hydrozoan    anthozoan    biofouling    distribution    settlement
1 INTRODUCTION

Cnidarians are common invertebrates in marine environments and only two groups (Hydrozoa and Anthozoa) are concerned in this review. Of them, hydrozoans (anthoathecatans and leptothecatans) usually have an alternation of a benthic colony and a planktonic medusa stage in the life cycle. However, anthozoans (including anemones, corals, and sea fans) have no medusa stage and only the attached polyp stage occurs (Hawkins and Jones, 1992; Levinton, 2001). As sessile organisms, adequate settlement substrata for cnidarians are necessary. In this sense, artificial facilities deployed in seas inevitably become appropriate habitats for them (Connell, 2000, 2001).

Globally, hydroids and sea anemones are important fouling species colonizing buoys, ships, piers, and wharves, as well as offshore platforms (Huang et al., 1981a, 1982b; Gollasch and Riemann-Zürneck, 1996; Farrapeira et al., 2007). Corals usually occur on the submerged part of offshore platforms (Roberts, 2002; Whomersley and Picken, 2003; Sammarco et al., 2004; Yan et al., 2006). Moreover, hydroids can dominate fouling communities on aquaculture nets in temperate waters (Guenther et al., 2009) and even become the sole macro-fouler on deep sea installations (Blanco et al., 2013; Zhang et al., 2015).

Biofouling can substantially increase hydrodynamic loading on nets (Swift et al., 2006). The drag on the hydroid-fouled twines is related to factors such as colony length and growth period, as well as drag coefficient (Lader et al., 2015). Additional evidence showed hydroid colonies can lead to over 10 times more hydrodynamic loading on nets with ~21.4% reduction in flow velocity (Bi et al., 2018). In addition, fouling by hydroids may induce localized corrosion (de Brito et al., 2007). Thus, fouling cnidarians constitute an increasing concern in the marine biofouling field.

In China, marine fouling investigations have been conducted for many decades and relevant information is quiet abundant (Huang and Yan, 1994). However, there are few studies only dedicated to fouling cnidarians (Lin, 1989). In order to better outline their fouling characteristics, provide the basis for further studies and facilitate the future development of anti-fouling strategies, this paper deals with species composition, distribution, and settlement pattern of sessile fouling cnidarians based on information from marine fouling investigations conducted in China from the 1950s up to the present.

2 DATA SOURCES AND INFORMATION PROCESSING

This paper is a literature review regarding fouling cnidarians and all data come from fouling investigations carried out in the past. According to the geographic location marine fouling along the coast of China, which has been studied, can be regionalized into the 19 sea areas as presented in Fig. 1. Further details on the investigation locations and relevant literature are shown in Table 1. In the literature, all fouling data in the various studies were either obtained from test panels or in situ scrape samples taken from the submerged parts of marine facilities (Liu and Yan, 2006). The details of the species composition and distribution of fouling cnidarians occurring in related waters are listed in Table 2. The nomenclature used for the organisms listed in Table 2 is that found at the website of the World Register of Marine Species (http://marinespecies.org). The settlement period and peak time of the major fouling cnidarians are shown in Fig. 2. Given the heterogeneity of data and the lack of quantitative analysis in (most of) the literature cited, the term major species is used when a species is reported as dominant either due to a high frequency of occurrence, or due to high abundance (biomass or surface covered).

 Fig.1 Investigation locations of marine fouling along the coast of China Map review No. GS(2019)1674.
Table 1 Investigation locations of marine fouling and relevant literature along the coast of China
Table 2 Distribution of fouling cnidarians along the coast of China
 Fig.2 The settlement period and peak time of some fouling cnidarians along the coast of China
3 SPECIES COMPOSITION AND DISTRIBUTION 3.1 Bohai Sea

The Bohai Sea is a semi-enclosed inland sea lined by the coasts of Liaoning, Hebei, Tianjin, and Shandong, connecting with the Yellow Sea through the Bohai Strait. The lowest water temperature in Bohai Sea ranges from -0.5–2.5 ℃ in February and the highest is between 22.5–26.5 ℃ in August; salinity is in the range from 27.0 to 32.0, of course, varies with seasons (Liu et al., 2003). There are 21 fouling cnidarians recorded with the dominant species being Obelia geniculata, Ectopleura marina, Bougainvillia sp., and Eudendrium capillare and common species were Anthopleura nigrescens, Sagartia elegans, and Gonothyraea clarki (Li et al., 1964, 1982c, 1989; Huang et al., 1980a, 1994; Wang et al., 1988).

3.2 Yellow Sea

The Yellow Sea is a semi-enclosed sea lined by Jiangsu Plain, Shandong Peninsula, Liaodong Peninsula, and Korean Peninsula and connects with the Bohai and East China Seas. Its salinity ranges from 29.0 to 33.0 and the mean annual water temperature varies from 12.0 to 15.0 ℃. The water temperature in winter is between 2.0–8.0 ℃ and in summer 24.0–26.0 ℃ (Shen, 2006). 22 species of fouling cnidarians were identified in the Yellow Sea and dominant species being O. geniculata, O. dichotoma, E. capillare and E. marina and common species Ectopleura crocea, G. clarki, and Actiniaria spp. (Li et al., 1964, 1982a, 1990; Zhang et al., 1981; Cao et al., 1999; Sun et al., 2010).

3.3 East China Sea

The East China Sea is a marginal sea and lies between the Yellow Sea and South China Sea. Its average water temperature in winter is 8.0–22.0 ℃ and in summer is 27.0–28.0 ℃ (Shen, 2006). The salinity is usually from 29.0 to 34.5. However, due to the effect of runoff, it could be reduced to 4.0–10.0 in the Changjiang (Yangtze) River estuary (Shen, 2006). There were 42 fouling cnidarians in the East China Sea and the dominant species were E. crocea, A. nigrescens, Bougainvillia sp., O. geniculata, D. lineata and E. capillare, followed by Obelia dichotoma, Pennaria disticha, Eudendrium sp., Clytia gracilis and Actiniaria spp. (Li et al., 1982b; Cai et al., 1994; Wang et al., 1996, 2011, 2012b; Lin et al., 2012).

3.4 South China Sea

The South China Sea is also a marginal sea and its north connects to the East China Sea via the Taiwan Strait. The water temperature is high throughout the year with the annual average temperature above 22.0 ℃. The salinity ranges from 30 to 34.5 (Shen, 2006). 53 fouling cnidarians were recorded. Obelia sp., Clytia sp. and the species of Actiniaria were the dominant species with O. geniculata, O. bidentata, O. dichotoma, Clytia hemisphaerica, C. gracilis, Coryne sp., Hebella sp., Orthopyxis sp. also commonly found (Lin et al., 1989; Zheng et al., 1996b; Yan et al., 1998a, 1999b, 2000, 2009).

4 FOULING CHARACTERISTICS 4.1 Bohai Sea

The Bohai Sea can be divided into five parts, including Liaodong Bay, Bohai Bay, Laizhou Bay, Bohai Strait, and the central waters. Its water temperature changes greatly with seasons and the settlement of most fouling cnidarians mainly took place from June to October.

In Liaodong Bay, the major fouling species were E. marina, Obelia sp., A. nigrescens, O. geniculata, Clytia sp. and Eudendrium rameum which mainly occurred in summer. In the semi-enclosed waters, panels were fouled by A. nigrescens from spring to autumn (Li et al., 1964; Zhang, 2007; Wang, 2010; Wu et al., 2010; Meng et al., 2012).

In Bohai Bay, Bougainvillia sp. heavily colonized test panels deployed at a site more than 18-km offshore from June to September. No fouling cnidarians occurred from December to April and the settlement of G. clarki was observed in May (Huang et al., 1980a). The test panels deployed about 7-km offshore were mainly fouled by E. marina and an unidentified Actiniarian species. Of them, the former settlement began in March and the later only occurred at the depth of 2 m (Zhou et al., 2016). In the harbour location, the panels were mainly fouled by Bougainvillia sp. from June to September, followed by Filellum serratum from May to August. The settlement of selective species of the genera Ectopleura and Obelia began in April (Huang et al., 1980a).

In Laizhou Bay, Obelia sp. could be found on net cages in May (Ren et al., 2000) and the settlement of O. geniculata and E. crocea reached a peak in July (Leng et al., 2012).

In the central Bohai Sea, the fouling cnidarians colonizing the legs of an offshore platform were mainly O. geniculata and S. elegans (Huang et al., 1994).

In the Bohai Strait, the dominant fouling species were C. hemisphaerica, E. capillare, O. dichotoma, E. crocea and E. marina. Of them, C. hemisphaerica and E. marina usually occurred on net cages as well (Hao et al., 1990). On the test panels, C. hemisphaerica and O. dichotoma settled from April to December and the former peak settlement time was from July to October, however, that of the latter was in September. Moreover, E. crocea could be observed from July to December with a settlement peak period in September and October. Concerning E. marina, it mainly occurred on the net cages in June and July (Li et al., 1982c, 1989; Wang et al., 1988; Zhou et al., 2012).

4.2 Yellow Sea

The natural conditions of the Yellow Sea are similar to those of the Bohai Sea. According to the geographical locations, the coastal waters of China include the Liaodong Peninsula waters, the northeastern and southern Shandong Peninsula waters, and the Jiangsu waters. The fouling cnidarians mainly occurred in summer and autumn.

In the waters of Liaodong Peninsula, the test panels and nets were fouled by O. geniculata, E. capillare, E. marina, and Clytia sp. Of them, O. geniculata and E. marina occurred from May to July, with the maximum biomass (4.7 g/m2) of the former in May and the latter in June with the maximum biomass of 31.3 g/m2. The settlement of E. capillare was from July to October, with the maximum biomass in July (Li et al., 1964; Cao et al., 1998). Clytia sp. only occurred in spring (Cao et al., 1999). Additionally, net cages and ropes were fouled by Obelia sp. (Li et al., 2001).

In the northeastern Shandong Peninsula waters, the dominant fouling cnidarians on the test panels were E. marina and E. capillare. The former occurred in May to August, October, and November with a peak in June and August. The latter presented from June to November and the settlement peak was in August (Li et al., 1990). On net cages, the common fouling species were Bougainvillia sp., Obelia sp., and P. disticha. Among them, Bougainvillia sp. occurred between June to November, particularly in July (Wang and Yue, 2005). During September to November, the test panels were fouled by Obelia sp. and P. disticha (Qi et al., 2010).

In the southern Shandong Peninsula, C. crassa and P. disticha were found in June and July (Li et al., 1964; Qi et al., 2011). Additionally, O. geniculata could be observed in July (Li et al., 1964), and the maximum biomass of E. crocea was also reached in July. The sea anemone Actinothoe qingdaoensis usually occurred on the seasonal, semi-annual, and annual panels (Sun et al., 2010).

In the harbor basin of Lianyungang Port, the northern Jiangsu waters, the settlement of F. serratum was from April to August with a peak time in May and June and that of G. clarki from May to October with its peak time in June (Li et al., 1982a). In the southern waters, common species were E. crocea and A. nigrescens. The settlement of E. crocea was divided into two periods, with peaks between April and June, and then in October. Additionally, E. crocea could grow well on the monthly test panels, however, A. nigrescens and D. lineata were usually found on concrete pillars of a hydrological platform (Zhang et al., 1981).

4.3 East China Sea

The waters where marine fouling investigation has been conducted in the East China Sea can be split into four regions: the northwestern, the southern Zhejiang, the northern Fujian, and the Taiwan Strait.

In the northwestern waters, the dominant fouling cnidarians were hydroids and sea anemones. Of them, the hydroid E. crocea settled from March to November with a peak from May to July (Huang et al., 1979; Wang et al., 2012a, b), but extending to December (Cai et al., 1994) and even January (Huang et al., 1979) in the waters of the Zhoushan Islands. Sea anemones occurred through the year with the maximum biomass of 138.8 g/m2 in July (Li et al., 1964; Xu et al., 2003; Shui and Guo, 2008). The major species was A. nigrescens, followed by D. lineata. A. nigrescens occurred from June to December with a peak from July to September (Huang et al., 1979; Shui and Guo, 2008; Wang et al., 2012b) and D. lineata settled from June to September with its peak in July (Wang et al., 2011). Additionally, the phenomenon that buoys were fouled by A. nigrescens could also be observed (Huang et al., 1981a). Besides, Cordylophora caspia occurred at the sites of tidal reach (Huang et al., 1980b, 1981a) and even became the dominant species with a maximum biomass of 660 g/m2 on the monthly panel in October and 1 326.3 g/m2 on the seasonal panel in autumn (Huang et al., 1980b).

In the southern waters of Zhejiang, except for January to March, the settlement of sea anemones could be observed through the year (Li et al., 1982b) giving maximum biomass on annual panels (Huang et al., 1981b; Li et al., 1982b). The most dominant species was A. nigrescens although its peak settlement time varied with location. For example, in Wenzhou Port located inside the estuary of the Oujiang River, the settlement peak was in February and March (Huang et al., 1981b). However, its peak was in summer (Li et al., 2018) or autumn (Li et al., 1982b; Zhang et al., 1982) outside the estuary. The settlement period of fouling hydroids was variable. Of them, Bougainvillia sp. occurred from June to November reaching a peak in July and E. crocea mainly settled in spring (Huang et al., 1981b; Li et al., 1982b, 2018). O. geniculata settled from June to October with a peak in August (Li et al., 1982b).

In the northern waters of Fujian, the cnidarians fouling test panels were mainly A. nigrescens and E. crocea. The former occurred from May to November and the latter from January to November. In July, the biomass of each reached a peak of 205 g/m2 and 1 000 g/m2, respectively (Li et al., 1994; Lin et al., 2017). However, in the waters of the lagoon connecting to the Luoyuan Bay via sluice gates, the settlement peak of E. crocea was in March and April (Zhou et al., 2001). In the waters of the Minjiang River mouth, which is a macrotidal estuary, buoys and wharves were fouled by Bougainvillia sp., D. lineata, and Anthopleura sp. Meanwhile Bougainvillia sp. also occurred on summer panels (Zheng et al., 1996a).

In the waters of the Taiwan Strait, the dominant fouling hydroids were E. crocea and Obelia sp. Although E. crocea mainly occurred in winter and spring, it could be found on monthly panels except for August and September with a maximum biomass of 1 300 g/m2 in April (Huang and Cai, 1961, 1962b; Li et al., 1992; Wang et al., 1996; Huang et al., 2007; Lin et al., 2010, 2012, 2014; Qiu et al., 2017). Obelia sp. can be observed almost all year round and its biomass was higher from August to October compared with other months (Zheng et al., 1953; Wang et al., 1996; Huang et al., 2007; Lin et al., 2012, 2014). Sea anemones were A. nigrescens, A. anjunae, and D. lineata (Zheng et al., 1953; Huang et al., 1982c, 2007; Wang et al., 1996; Lin et al., 2012, 2014). Of them, A. nigrescens settled mostly in the summer and autumn with a peak in July (Huang et al., 1982c, 1982d; Qiu et al., 2017) and D. lineata only occurred in July and August (Lin et al., 2012). A. anjunae was found from March to December with maximum biomass of 112 g/m2 in July (Huang and Cai, 1961). Concerning hydroids, Clytia sp. settled through the year (Huang et al., 1982d, 2007) whereas settlement of P. disticha was from summer to winter with a peak in August (Lin et al., 2012). Additionally, Eudendrium generale amoyicum could be found on sub-sea cables in Xiamen waters (Huang and Cai, 1962a).

4.4 South China Sea

The South China Sea extends across subtropical and tropical zones with high water temperatures throughout the year. According to the geographic features, it can be split into the eastern Guangdong, Zhujiang River delta, western Guangdong, Beibu Gulf, Hainan and South China Sea Islands.

In the waters of the eastern Guangdong, A. nigrescens was the dominant species and settled from March to November with the peak in August and September, followed by O. dichotoma which settled from February to November with the peak in September (Li et al., 1996; Zheng et al., 1996b; Lin et al., 2011). In Shantou Port, E. crocea could be found on the tail pipe and chain of navigation buoys while Calyptospadix cerulea heavily colonized the tail pipe inward surface of one of them (Li et al., 1996). Moreover, P. disticha occurred on panels from March to May and then August to November, with a peak in April and May (Lin et al., 2011).

In the waters of the Zhujiang River delta, the common fouling cnidarians were O. bidentata (Yan and Huang, 1990; Zheng and Huang, 1990; Huang et al., 1993), O. geniculata (Zheng et al., 1991; Huang and Lin, 1993; Huang et al., 1993), E. crocea (Huang and Mak, 1982; Huang et al., 1993, 1999b), Eudendrium racemosum (Huang and Mak, 1982; Xu and Gao, 2010), A. nigrescens (Huang and Mak, 1982; Huang et al., 1999b), Anthopleura sp. (Zheng et al., 1991; Huang et al., 1992b), D. lineata (Huang and Mak, 1982; Huang et al., 1992b) and an unidentified species of Actiniaria (Yan and Huang, 1990; Huang et al., 1993; Huang and Lin, 1993). Among them, O. bidentata was the most frequent species fouling net meshes (Zheng and Huang, 1990). It settled from April to August with a peak in May and June (Yan and Huang, 1990; Huang et al., 1993). O. geniculata was observed from March to December with a peak from March to July and E. crocea usually between January and April with a peak in January (Huang et al., 1993). However, E. racemosum was the dominant species in summer and autumn with a peak in June (Xu and Gao, 2010). Moreover, D. lineata could also be observed on pier pilings (Huang et al., 1992b) and Actiniaria spp. only occurred on seasonal, semi-annual, and annual panels (Yan and Huang, 1990). In the adjacent offshore waters, the summer test panels at the depth of 3 m were mainly colonized by Bougainvillia sp., Clytia sp., and Obelia sp.; and the autumn panels were fouled by Coryne sp. Additionally, the Actiniaria species occurred on the surface buoy about 15-km offshore and its biomass reached 2 752.8 g/m2. No sea anemones were found on the buoy approximately 72-km offshore (Yan et al., 1999b).

In the waters of the western Guangdong, the common fouling cnidarians were sea anemones, Anthopleura xanthogrammica (Lin et al., 1989) and the unidentified Actiniaria species (Huang et al., 1982b; Yan et al., 1995) and the hydroids E. crocea (Yan et al., 1995), P. disticha (Lin et al., 1989; Yan et al., 1995) and Obelia sp. (Yan et al., 1995). Among them, the occurrence frequency of A. xanthogrammica on buoys in the Shuidong and the Bohe ports was more than 70% (Lin et al., 1989). In the Zhanjiang port, E. crocea settled from January to April with a peak in March and April, followed by P. disticha with the settlement from March to May with a peak in April and May. Moreover, Obelia sp. occurred through the year with the peak settlement was in September and October (Yan et al., 1995). Besides, Telesto sp. was found on a navigation buoy (Huang et al., 1982b).

In the Beibu Gulf, sea anemones were the dominant foulers including A. nigrescens and Anthopleura sp. (Dong, 1982; Huang et al., 1992a; Wang et al., 1993; Yan et al., 1997, 1998a, 2006; Li et al., 2010a; Tian and Xu, 2015), usually found on seasonal panels, buoys, docks and platform with long immersion times in the sea. Common hydroids on panels were Clytia sp. (Huang et al., 1992a; Wang et al., 1993; Li et al., 2010a), Obelia sp. (Li et al., 2010a, b) and O. bidentata (Wang et al., 1993). Except for March, the settlement of Clytia sp. could be observed throughout the year and its peak occurred in April, July, and August (Huang et al., 1992a; Wang et al., 1993). O. bidentata settled from May to November and the peak was in May and September (Wang et al., 1993). At a buoy station tens of kilometers offshore, the summer panel at a depth of 3–20 m was mainly fouled by the species of Hydractiniidae, while autumn panels at 3 m were fouled by Clytia sp. and Orthopyxis sp. (Yan et al., 1998a).

In the Qiongzhou Strait, as well as the eastern and southern waters of Hainan Island, G. clarki occurred from July to February with a peak in September (Li et al., 1964). Obelia sp. settled throughout most of the year with a peak in March and April (Huang and Cai, 1962b; Li et al., 1964; Huang et al., 1982a; Chen et al., 2018). In Langya Bay, the occurrence frequency of Clytia sp. was over 30% and its settlement peak was from March to May (Zheng et al., 1984). Sea anemones usually could be observed on seasonal (Zheng et al., 1984; Chen et al., 2018), eight-month (Yan et al., 1998b) and annual panels (Huang et al., 1982a), as well as buoys (Huang et al., 1982a, b; Wang et al., 1997; Yan et al., 1999a). Moreover, the settlement of sea anemones also occurred on monthly panels in Qinglan port and Langya bay (Huang et al., 1982a; Zheng et al., 1984). In offshore waters, Clytia sp. and Obelia sp. were the major fouling cnidarians on panels (Yan et al., 1999a, 2000).

In the waters of the South China Sea Islands, the major species of fouling cnidarians were Clytia sp. and Obelia sp. (Zhang et al., 1984; Yan et al., 2003, 2009; Zhang et al., 2015). The summer panels were mainly fouled by Orthopyxis sp. and Clytia sp.; and the autumn panels by Coryne, Clytia, and Obelia spps in the waters northwest of the Dongsha Islands. Moreover, species of Clytia, Obelia, and Hebella could also be found on buoys and their mooring systems (Yan et al., 2003, 2009). In the harbour basin of Yongxingdao, the Xisha Islands, the settlement of hydroids occurred in autumn and winter (Zhang et al., 1984). Moreover, in the northwestern waters of the Xisha Islands, a submersible buoy system at more than 400 m below the sea surface where the overall water depth is 1 667 m, was fouled by Obelia sp. reaching a biomass of 1 286 g/m2 (Zhang et al., 2015).

5 DISCUSSION

In the waters along the coast of China, a total of 76 species of fouling cnidarians were found, some of which were widely distributed and some more specific to local environmental conditions. The species number increased from the north to the south. A. nigrescens, E. crocea, C. hemisphaerica, G. clarki, O. dichotoma, and O. geniculata were widely distributed. However, E. rameum occurred only in the Bohai Sea; Metridium senile, A. qingdaoensis, Coryne crassa, and O. longissima in the Yellow Sea; A. anjunae, A. asiatica, C. caspia, E. generale amoyicum, Ectopleura larynx, Gymnangium hians, Hartlaubella gelatinosa, and Thuiaria trilateralis in the East China Sea; Ellisella laevis, Hicksonella guishanensis, Caryophyllia japonica, C. scobinosa, Cladopsammia eguchii, Platygyra sinensis, Oulangia stokesiana, E. racemosum, Ralpharia parasitica, Macrorhynchia nuttingi, M. philippina, Clytia stechowi, Nemalecium lighti, Hebella corrugata, H. scandens, Dynamena crisioides, and Synthecium campylocarpum in the South China Sea.

Water temperature not only plays an important role in limiting the geographical distribution of fouling cnidarians, but also has a significant effect on settlement times. Summer and autumn are the main seasons for the settlement of hydroids and sea anemones in the waters along the Chinese coastline. This may be related to the fact that the reproduction of most hydroids depends on water temperature (McClary, 1959; Ma and Purcell, 2005) and their growth also increases with increasing temperature to the optimum (Fulton, 1962; Nellis and Bourget, 1996; Bettim and Haddad, 2017). For sea anemones, gonad development and binary fission were also favored by increased temperatures (Ford, 1964; Ryan, 2018). Likewise, coral larval development and settlement were enhanced with increasing water temperatures appropriately (Nozawa and Harrison, 2007; Heyward and Negri 2010; Chua et al., 2013; Woolsey et al., 2013).

Salinity is another factor that significantly affects the distribution of fouling cnidarians (Boero, 1984; Gili and Hughes, 1995). With the decrease of salinity, the typical marine species disappear and are substituted by euryhaline species or by those adapted to low salinities. C. hemisphaerica mainly occurred in fully marine environments, such as the waters of Tuoji Island (Wang et al., 1988), Lushun Harbor (Li et al., 1982c) and Zhoushan Islands (Huang et al., 1979; Cai et al., 1994), where the salinity is 30 or above. However, C. caspia was found in waters with low salinity only and even became dominant in the fouling communities at tidal reach sites, such as the Ningbo port and front end of the Changjiang River estuary (Huang et al., 1980b, 1981a).

Substratum heterogeneity may influence the distribution of cnidarians (Gili and Hughes, 1995; Creed and De Paula, 2007; Li and Xu, 2020). Hydroids can grow well on the surface of new substrata. With the further development of the overall fouling communities, their biomass percentage usually decreased (Huang et al., 1980a; Cai et al., 1994). In most conditions, sea anemones were found with a higher occurrence frequency or biomass in samples collected from substrata deployed in the sea for extended periods (Huang et al., 1981b; Li et al., 1982b; Wang et al., 1988; Farrapeira et al., 2007). Corals occurred in long-term fouling communities (Whomersley and Picken, 2003; Yan et al., 2006) and their abundance increased significantly with time (Sammarco et al., 2004).

Some subjective elements in studies, such as investigation method, sampling time and survey location, may also be related to the occurrence or absence of cnidarians in fouling communities. For example, the taxa of cnidarians are important components of benthic communities around Taiwan, China (Tseng et al., 2014; Ribas-Deulofeu, 2016; Lin and Denis, 2019). However, there are no data relating to the field of fouling (see Huang and Chen, 2002; Lin and Shao, 2002) until now. To fill the data gaps and thoroughly understand the fouling characteristics of cnidarians in China, more work is needed particularly in the waters of Taiwan Island, China, and South China Sea Islands.

6 CONCLUSION

According to the data from earlier literature, it can be concluded that a total of 76 species of fouling cnidarians were observed and classified in the coastal waters of China. The species composition and distribution patterns depend mainly on water temperature and salinity, as well as substrata. Moreover, the absence of cnidarians in fouling communities may be related to some subjective factors in studies. To fully understand the fouling characteristics of cnidarians in China, more work should be conducted in the waters where relevant investigations are scarce.

7 DATA AVAILABILITY STATEMENT