INTRODUCTION
Hainan Island (Figure 1) is located in the subtropical northern periphery of the Indo-Pacific Ocean in the South China Sea (18°10′ − 20°9′N108°37′ − 111°1′E). The island has an area of 33.920 km2 and a coastline of more than 1610 km. The annual mean sea surface temperature (SST) is 26°C (1970 − 2002) with an average seasonal range of 12.1°C (Sun et al., Reference Sun, Gagan, Cheng, Scott-Gagan, Dykoski, Edwards and Su2005). The annual SST maximum (30.8°C) and minimum (18.7°C) commonly occur in July and January, respectively. Mean sea surface salinity (SSS) in the South China Sea fluctuates between 33.3 and 34.0 psu. However, SSS is strongly seasonal at Hainan Island, decreasing to a mean value of 26.5 psu owing to freshwater run-off and rain during the summer wet season (Levitus & Boyer, Reference Levitus and Boyer1994). The mean tidal range is generally less than 1.5 m (Zhang et al., Reference Zhang, Xu and Long1996). The rainy season in the southern part of Hainan occurs from May to October and accounts for 95% of the yearly rainfall; the dry season occurs from November to April (Li, Reference Li2011).
Hainan Island (South China Sea, China) and details of the investigation area, Luhuitou reef in Sanya Bay.
The coral reefs of Hainan Island are among the most prominent fringing reefs of China. However, the diversity of coral reef species has been declining. The highest biodiversity was recorded between the 1950s and 1960s (Gurianova, Reference Gurianova1959) but decreased severely during the next 20 years (Hutchings & Wu, Reference Hutchings and Wu1987; Zhang et al., Reference Zhang, Shi, Chen, Fong, Wong, Huang, Wang and Zhao2006). Almost 80% of the fringing reefs along the coastline of Hainan Island (including the coral reef of Luhuitou Peninsula) have been damaged arising from human activities during the 1970 − 1990s (fishing with dynamite, removal of corals for lime and construction). Recently, the eutrophication of Hainan coastal waters, particularly in the shallow gulfs, has increased owing to greater tourist numbers, hotel building along the coast and mariculture in coastal ponds and pools with wastes draining into the sea (Hutchings & Wu, Reference Hutchings and Wu1987; Fiege et al., Reference Fiege, Neumann and Jinhe1994; Zhang et al., Reference Zhang, Xu and Long1996; Hodgson & Yau, Reference Hodgson, Yau, Lessios and Macintyre1997; Zhang et al., Reference Zhang, Que, Liu and Xu2004; Tadashi et al., Reference Tadashi, Dai, Park, Huang, Ang and Wilkinson2008; Titlyanov et al., Reference Titlyanov, Kiyashko, Titlyanova, Pham and Yakovleva2011c).
It is known that degradation processes on coral reefs (especially in eutrophic waters) lead to changes in macroalgal associations (e.g. Smith et al., Reference Smith, Kimmerer, Laws, Brock and Walsh1981; Lapointe et al., Reference Lapointe, Littler and Littler1997; Diaz-Pulido & McCook, Reference Diaz-Pulido and McCook2002; Gartner et al., Reference Gartner, Lavery and Smit2002; Oliveira & Qi, Reference Oliveira and Qi2003; McClanahan et al., Reference McClanahan, Marnane, Cinner and Kiene2006; Sergeeva et al., Reference Sergeeva, Titlyanova and Titlyanov2007; Sfriso & Curiel, Reference Sfriso and Curiel2007; Titlyanov & Titlyanova, Reference Titlyanov and Titlyanova2008; Titlyanov et al., Reference Titlyanov, Titlyanova and Chapman2008, Reference Titlyanov, Kiyashko, Titlyanova, Yakovleva, Li and Huang2011b). Ephemeral fast-growing green algae in the intertidal zone displace slow-growing macroalgae. Frondose and fleshy algae are quickly overgrown by epiphytes, which then become the dominant biomass (Morand & Briand, Reference Morand and Briand1996; Morand & Merceron, Reference Morand, Merceron and Pandatal2004; Lapointe et al., Reference Lapointe, Barile, Littler, Littler, Bedford and Gasque2005a, Reference Lapointe, Barile, Littler and Littlerb; Titlyanov et al., Reference Titlyanov, Kiyashko, Titlyanova, Yakovleva, Li and Huang2011b).
It is also known that changes in biomass and species composition in coastal ecosystems occur throughout the year, and that they have seasonal characteristics that appear to be connected to rhythmic changes in abiotic and biotic environmental factors (Fong & Zedler, Reference Fong and Zedler1993; Kennish, Reference Kennish1996; Pedersen & Borum, Reference Pedersen and Borum1996; Kentula & DeWitt, Reference Kentula and DeWitt2003; Su et al., Reference Su, Chung and Lee2009). The greatest seasonal floristic changes are caused by environmental changes in light intensity, temperature, salinity, rainfall, nutrient concentration, and wave action (Costa et al., Reference Costa, Zman, Nimmo and Attrill2000, Reference Costa, Attrilla, Pedrinib and De-Paulab2002; Ateweberhan et al., Reference Ateweberhan, Bruggemann and Breeman2006; Thakur et al., Reference Thakur, Reddy and Jha2008; Su et al., Reference Su, Chung and Lee2009).
This investigation is the first seasonal comparison (during the dry and rainy seasons) of marine algal species diversity and distribution in the upper subtidal zone, and community structure in the coral reefs at Hainan Island. In addition, seasonal changes in the flora of Sanya Bay were examined, the influence of eutrophication on these communities was estimated and the seasonal impact of different environmental factors was determined.
MATERIALS AND METHODS
Study site, time and conditions
Investigations were conducted at Luhuitou reef, Sanya Bay, Hainan Island, China. The algae were collected in front of the Marine Biological Station of the South China Sea Institute of Oceanology during the rainy (October 2008 and November 2010) and dry (April 2009 and February 2012) seasons (Figure 1).
Algal sampling was conducted from 6–15 October 2008, 6–22 April 2009, 15 November–3 December 2010 and 2–28 February 2012. For two months before and one month during sampling (August−October 2008, February−April 2009, September−November 2010 and December 2011–February 2012), climatic characteristics such as surface seawater temperature (SST), number of sunny days (SD), the average concentration of dissolved inorganic nitrogen (DIN) and inorganic orthophosphates (PO4−3) in seawater of the investigated area are presented in Table 1. Climatic characteristics were obtained from the weather station at the Marine Biological Station while nutrient data were obtained at the stations close to Luhuitou reef from the Chinese Ecosystem Research Network (http://www.cern.ac.cn; Huang et al., Reference Huang, Tan, Song, Huang, Wang, Zhang, Dong and Chen2003).
Climatic characteristics of the investigated area.
SST, surface seawater temperature; SD, number of sunny days; DIN: the average concentration of dissolved inorganic nitrogen and orthophosphates (PO4−3). Data source: Li Reference Li2011 and Tropical Marine Biological Research Station in Hainan, Chinese Academy of Sciences.
Collection, conservation and identification of marine plants
Marine plants were collected in the upper subtidal zone (from 0.5 to 3 m depth during low tide). At the sites investigated, the upper subtidal zone consisted of a sloping shore (50 − 200 m wide) composed primarily of dead and live colonies of massive and branched corals interspersed with sand, stones and dead coral fragments of various shapes and sizes (Figure 2). Sampling of the marine plants was carried out via snorkelling and SCUBA diving during low and high tides. Samples were extracted from all substratum types at more than 50 sites. Quadrates in algal turf communities were 100 cm2 while those in the communities of large fleshy or foliose algae were 625 cm2.
Luhuitou coral reef, upper subtidal, 3 m depth at low tide, April 2012.
The collections were preserved as dried herbarium specimens. Freshly collected material was identified using monographic publications, floristic studies and systematic articles by Børgesen, 1913a, b, c, 1914, 1915–1920, 1924, 1940, 1948; Setchell & Gardner, 1930; Yamada, 1934, 1938; Tseng, 1936, 1938, 1942; Tanaka, 1938; Shen & Fan, 1950; Taylor, 1950, 1960, 1966; Egerod, 1952; Dawson, 1954, 1956, 1957, 1961, 1962; Durairatnam, 1961; Chiang, Reference Chiang1962; Womersley, 1967, 1984, 1987, 1994; Zinova, 1967; Hollenberg, 1968a, b; Trono, 1968, 1969, 1997; Pham, 1969; Womersley & Bailey, 1970; Itono, 1972; Abbott & Hollenberg, 1976; Jaasund, 1976; Reyes, 1976; Tseng & Dong, 1978; Vinogradova, 1979; Lu & Tseng, 1980; Perestenko, 1980; Tseng et al., 1980, 1983, 2001, 2005; Trono & Put, 1982; Tseng & Lu, 1983; Dong & Tseng, 1985; Lewis & Norris, Reference Lewis and Norris1987; Trono & Ganzon-Fortes, 1988; Kornmann, 1989; Luan, 1989; Burrows, 1991; Price & Scott, 1992; Luan & Luan, 1995; Wynne, 1993, 1995; Lewis & Mei-Lan, 1996; Draisma et al., 1998; Abbott, 1999; Huang, 1999; Littler & Littler, 2000, 2003; Leliaert & Coppejians, 2003; Skelton, 2003; South & Skelton, 2003; Abbott & Huisman, 2004; Skelton & South, 2004, 2007; Xia et al., 2004; Brodie et al., 2007; Dawes & Mathieson, 2008; Zheng & Li, 2009.
The systematics and nomenclature followed Guiry & Guiry (AlgaeBase, searched Reference Guiry and Guiry2012). The previously known and newly recorded species for Hainan and China were verified using Algaebase, the Catalogue of Life China (2010 Annual Checklist) and the checklist of marine biota of China seas by Liu (Reference Liu2008).
Analysis of algal communities
The abundance of taxa was determined visually by estimating relative percentage cover. The following codes were used: a single sighting (S); a rare sighting (+); common or 10−30% cover (++); and abundant or 30−50% cover (+++). Algal dominance in the communities was also determined visually and defined as: monodominant if one algal species occupied more than 50% of the surface area; bidominant if two species occupied more than 50%; and polydominant if more species were involved. Calculations of species diversity in the upper subtidal zone included species of marine algae and seagrasses found at Luhuitou reef during all samplings. Rare species found during one of the samplings were not used (in Table 2 these species are marked with asterisks).
Species composition, abundance and distribution of marine plants in subtidal Sanya Bay at Luhuitou coral reef
Annotation: E − epiphyte; En − endophyte; S − single sighting; +− rare sighting; ++ − common; ++ + −abundant, * − rare found only during one sampling
RESULTS
In total, 156 species of marine algae and plants were found in the upper subtidal zone of Luhuitou Peninsula during the investigations. These included 143 taxa of macrophytes (90%), 12 cyanobacterial taxa (Cy) (10%) and the seagrass (Thalassia hemprichii). Among the macrophytes, 79 species (55%) were Rhodophyta (Rh), 38 (25%) were Chlorophyta (Ch) and 26 (20%) were Phaeophyceae (Ph) (Table 2).
Algal communities in the rainy season (October 2008 and December 2010)
In total, during the autumn−winter periods of 2008 and 2010, 96 species of marine macroalgae, one species of blue–green alga (Spirulina subtilissima) and one species of seagrass (Thalassia hemprichii) were collected. The macroalgae included 57% red, 24% green and 19% brown algae (Table 2).
In October 2008, 80 species of macroalgae and one species of blue–green alga were collected. The macroalgae included 57% red, 23% green and 20% brown algae.
In November−December 2010, 90 taxa of macroalgae and one species of blue–green alga were collected. The macroalgae consisted of 60% red, 25% green and 15% brown (Table 2).
ALGAL COMMUNITIES IN OCTOBER 2008
The upper subtidal zone was occupied primarily by polydominant turf algal communities (70−90%, 3−6 cm high) with a mosaic dominance of long-lived articulated calcareous algae (Figure 3) such as Amphiroa fragilissima and Jania capillacea, the fleshy alga Hypnea pannosa (Rh) and coriaceous Lobophora variegata (Ph).
Algal turf community in the upper subtidal zone, Sanya Bay, October 2008. Inserts: predominant species: 1, Lobophora variegata; 2, Jania capillacea; 3, Amphiroa fragilissima.
Turf communities included long-lived species Jania adhaerens, Amphiroa foliacea, Gelidiella acerosa (Rh), Bryopsis pennata, Neomeris annulata, Dictyosphaeria cavernosa, Cladophora vagabunda (Ch), and short-lived Polysiphonia subtilissima, and P. scopulorum var. villum (Rh). Young plants of Sargassum spp. were also common within turf communities as well as outside the communities. Ceratodictyon spongiosum (Rh) and the seagrass, Thalassia hemprichii, were common on sandy bottom areas between patch-reefs and dead coral blocks. Some dead coral blocks were overgrown with calcareous crust-like algae such as Peyssonnelia conchicola, P. inamoena, P. rubra, Lithothamnion sp. Among the epiphytic algae, Stylonema alsidii, Erythrotrichia carnea, Hydrolithon farinosum, Jania capillacea, Gayliella flaccida (Rh) and Sphacelaria tribuloides (Ph) were dominant (Table 2).
Scleractinian corals from the genera Porites, Acropora, Pocillopora, Galaxea, Montipora, Platygyra, Favites, and so forth, were also common in the upper subtidal zone.
ALGAL COMMUNITIES IN NOVEMBER–DECEMBER 2010
In November−December 2010, similar to that observed in October 2008, the upper subtidal hard substratum was mainly occupied by polydominant communities of algal turf (Figure 4). These were dominated by long-lived articulated calcareous species such as Amphiroa fragilissima, A. foliacea, Jania adhaerens and J. capillacea (Rh). Long-lived Hypnea pannosa (fleshy form), Gelidium pusillum, Gelidiella acerosa (caespitose form), Dictyota friabilis (fleshy form) and filamentous ephemeral species, such as Centroceras clavulatum, Polysiphonia japonica var. savatieri and P. subtilissima (Rh), were common. Turbinaria ornata and young thalli of Sargassum spp. were also found on areas of hard substratum not occupied by algal turf. Some dead coral blocks were overgrown by Peyssonnelia conchicola, P. inamoena, P. rubra and Lithothamnion sp. Among the epiphytic algae, Stylonema alsidii, Gayliella flaccida, Herposiphonia secunda f. tenella (Rh), Sphacelaria rigidula (Ph) and Ulvella lens (Ch) were dominant (Table 2).
Algal turf community in the upper subtidal zone, Sanya Bay, November 2010. Inserts: predominant species: 1, Amphiroa foliacea; 2, Jania adhaerens.
Algal communities during the dry seasons (April 2009 and February 2012)
In total, during the winter−spring periods of 2009 and 2012, 114 species of marine algae and plants were found, including 105 taxa (94%) of macroalgae, seven taxa of cyanobacteria and one species of seagrass (Thalassia hemprichii). The macroalgae consisted of 58% red, 24% green and 18% brown algae.
In April 2009, 89 species of marine macroalgae, six species of cyanobacteria and one species of seagrass, Thalassia hemprichii, were found. The macroalgae comprised 56% red, 22% green and 22% brown algae. In February 2012, 97 species of marine macroalgae, three species of blue–green algae and one species of seagrass, Thalassia hemprichii, were found. Macroalgae included 60% red, 20% green and brown 20% algae (Table 2).
ALGAL COMMUNITIES IN APRIL 2009
In April 2009, a bidominant community of brown frondose algae, Sargassum polycystum and S. ilicifolium, was distributed along the foreshore at the border between the low intertidal and upper subtidal zones (Figure 5). Sargassum sanyaense and Sargassum sp. were also found in the community. At the edge of the Sargassum spp. community bed, S. polycystum was densely overgrown by epiphytes such as Acrochaetium robustum, Centroceras clavulatum, Gayliella flaccida, Ceramium comptum, C. borneense, Polysiphonia japonica var. savatieri (Rh), Hincksia mitchelliae and Sphacelaria tribuloides (Ph). Behind the Sargassum spp. bed, the hard substrate, consisting of patch-reef debris and dead coral blocks, was occupied by a polydominant community of turf algae (Figure 6). This community was dominated by Amphiroa foliacea, Acanthophora muscoides, Hypnea pannosa, H. valentiae, Tolypiocladia glomerulata and Jania capillacea (Rh). Within this community Gelidiella acerosa, Acanthophora spicifera (Rh), Dictyota friabilis (Ph), Boodlea composita, Bryopsis pennata, Caulerpa serrulata and Neomeris annulata (Ch) were also common. Turbinaria ornata (Ph) and Halymenia maculata (Rh) were found outside of the algal turf community.
Bidominant community of Sargassum species in the subtidal zone of Sanya Bay, April 2009. Inserts: 1, Sargassum polycystum; 2, Sargassum sanyaense.
Algal turf community in the upper subtidal zone, Sanya Bay, April 2009. Inserts: predominant species: 1, Acanthophora muscoides; 2, Tolypiocladia glomerulata; 3, Hypnea valentiae.
Padina australis (Ph) formed monodominant communities with inclusions of P. minor at the border with the low intertidal zone. Ceratodictyon spongiosum (Rh) and the seagrass, Thalassia hemprichii, were common on sandy bottom areas between dead coral blocks. Crust-like algae of the genera Peyssonnelia, Lithothamnion (Rh) and Neoralfsia (Ph) occupied about 10% of the hard substratum. In cyanobacterial films (often covering algal turf communities), three communities were identified: (1) a monodominant community of Phormidium sp. (bright green colour); (2) a bidominant community (dark brown colour) with a predominance of Coleofasciculus chthonoplastes and Oscillatoria spp. and accompanying species of Spirulina subtilissima, Lyngbya majuscula, Phormidium sp.; and (3) a green colour community with a predominance of Planktothrix agardhii [Oscillatoria agardhii] and L. majuscula. Among the epiphytes growing on the turf algae, Erythrotrichia carnea, Stylonema alsidii, Acrochaetium hypneae, Hydrolithon farinosum, Pneophyllum fragile, Jania capillacea, Centroceras clavulatum, C. minutum, Ceramium marshallense, Gayliella flaccida, Wrangelia argus (Rh), Feldmannia mitchelliae, Sphacelaria novae-hollandiae (Ph), Acrochaete leptochaete (endophyte), Rhizoclonium riparium, R. riparium var. implexum (Ch) and Licmophora sp. (Bacillariophyta) were all common (Table 2).
ALGAL COMMUNITIES FEBRUARY−MARCH 2012
In February−March 2012, in the upper subtidal zone at Luhuitou Peninsula, two main algal communities (bidominant and polydominant) were found. The bidominant community comprised of brown frondose algae, Sargassum polycystum and S. sanyaense, with accompanying species of S. ilicifolium and Sargassum sp. This community was distributed along the border between the upper subtidal zone and the low intertidal zone. Within this community, Sargassum spp. were densely overgrown by epiphytes, such as Chroodactylon ornatum, Erythrotrichia carnea, Acrochaetium robustum, A. hypneae, A. microscopicum, Colaconema gracile, Jania ungulata f. brevior, Gayliella flaccida, Neosiphonia sphaerocarpa (Rh), Kuetzingiella elachistaeformis, Sphacelaria novae-hollandiae, S. rigidula (Ph) and Ulva clathrata (Ch).
The polydominant community occupied the hard substrate, which consisted of the patch-reef debris in-between the Sargassum spp. bed and behind the bed (towards the sea). This community (2−5 cm high with 100% algal cover) comprised long-lived fleshy algae Hypnea pannosa, H. valentiae, Acanthophora muscoides, Spyridia filamentosa (Rh) and ephemeral finely-branched algae Gayliella flaccida and Centroceras clavulatum (Figure 7). Caulerpa serrulata, Bryopsis pennata, Neomeris annulata (Ch), Colpomenia sinuosa, Hydroclathrus tenuis, Dictyota bartayresiana (Ph) and Halymenia maculata (Rh) were common between the turf algae or growing above the turf. Turbinaria ornata, C. sinuosa, Chnoospora implexa, Rosenvingea intricata (Ph), H. maculata (Rh) and Caulerpa racemosa (Ch) were common outside of the community.
Algal turf community in the upper subtidal zone, Sanya Bay, March 2012. Inserts: predominant species: 1, Gayliella flaccida; 2, Hypnea pannosa; 3, Spyridia filamentosa.
Padina australis formed a monodominant community on separate dead coral blocks along the border with the low intertidal zone, often with Padina minor interspersed. On sandy bottom areas with dead coral debris, Ceratodictyon spongiosum and the seagrass, Thalassia hemprichii, were common. Some dead coral blocks were occupied by crust-like algae such as Peyssonnelia conchicola, P. rubra, Lithothamnion sp. and Neoralfsia expansa (Figure 8). A community of blue–green algae dominated by Phormidium nigroviride and with accompanying species of Aphanocapsa litoralis, Oscillatoria margaritifera, Trichocoleus tenerrimus and Oscillatoria limosa was found on the substratum not occupied by algal turf. Stylonema alsidii, Erythrotrichia carnea, Acrochaetium microscopicum, Gayliella flaccida, Polysiphonia japonica var. savatieri (Rh) and Sphacelaria rigidula (Ph) were dominant among the epiphytic algae (Table 2).
Community of crust-like algae in upper subtidal, Sanya Bay, March 2012. Inserts: 1, Peyssonnelia rubra; 2, Neoralfsia expansa; 3, Peyssonnelia conchicola.
DISCUSSION
According to the floristic analysis conducted in the upper subtidal zone of the Luhuitou reef, marine macroalgae mostly occupied the hard substrate (rocky bottom, carbonate reef, dead coral colonies and their debris), blue–green algae grew commonly on turf algae, and seagrass occupied sandy–silty bottom sites. The average cover by marine plants in the zone was about 60%, and about 22% by live hermatypic corals. Subtidal flora comprised mainly algal turf, calcareous crusts, large brown algal communities and separately growing fleshy, frondose and foliose algae (Table 2).
Species diversity
A total of 436 taxa (macroalgae and blue–green algae) have been recorded from the coastal area of Hainan Island and nearby islets in the last century and the beginning of the present century. Of these, 250 taxa (60% of macroalgae) belong to Rhodophyta, 106 taxa (25%), to Chlorophyta and 65 (15%) to Phaeophyceae (Liu, Reference Liu2008; Titlyanov et al., Reference Titlyanov, Kiyashko, Titlyanova, Yakovleva, Li and Huang2011b). The floristic richness of Hainan Island among the southern provinces of China is second only to Taiwan, where 600 species of macroalgae have been recorded (Lewis & Norris, Reference Lewis and Norris1987). The floristic composition and abundance of the species found around Hainan (among the Chinese provinces) is close to that found around Taiwan (Zhang, Reference Zhang1996). This similarity is probably influenced by both the geographical location of Hainan and the Taiwan Islands and by the intensity of study of their underwater floras.
A total of 156 taxa, including 143 macroalgae (90%), 12 blue–green algae (10%) and one species of seagrass (Thalassia hemprichii), were found in the upper subtidal zone at the Luhuitou reef (Sanya Bay) in front of the Marine Biological Station during this study. Among the macroalgae, 79 red (55%), 38 green (25%) and 26 brown algae (20%) were found. The floristic composition of the marine coastal ecosystem at Hainan Island (Luhuitou coral reef) is similar to that of coral reefs in the Indo-Pacific that are situated in regions with insignificant pollution, where the proportion of benthic macroalgal groups has been shown to be 50−60% red, 20−30% green and 10−20% brown (Lewis & Norris, Reference Lewis and Norris1987; Silva et al., Reference Silva, Basson and Moe1987; Zhang, Reference Zhang1996; Tsuda, Reference Tsuda2003, Reference Tsuda2006; Huisman & Borowitzka, Reference Huisman, Borowitzka, Wells, Walker and Jones2003). In spite of significant pollution with dissolved inorganic nitrogen and phosphorus (Titlyanov et al., Reference Titlyanov, Titlyanova, Bangmei and Bartsch2011a), the subtidal flora of Sanya Bay did not show dramatic changes in macroalgal species composition.
Investigations conducted in other tropical regions of the world have shown that the following changes occur in the marine flora of eutrophicated waters: (1) an increase in species diversity and biomass of ephemeral fast-growing green algae and displacement of slow-growing macroalgae (Burrows, Reference Burrows1971; Barile, Reference Barile2004; Titlyanov et al., Reference Titlyanov, Kiyashko, Titlyanova, Pham and Yakovleva2011c); (2) overgrowth by epiphytes of frondose and fleshy algae (Morand & Briand, Reference Morand and Briand1996; Morand & Merceron, Reference Morand, Merceron and Pandatal2004; Lapointe et al., Reference Lapointe, Barile, Littler, Littler, Bedford and Gasque2005a, Reference Lapointe, Barile, Littler and Littlerb); and (3) ‘blooms’ of local or invasive species (Smith et al., Reference Smith, Kimmerer, Laws, Brock and Walsh1981; Bell, Reference Bell1992; Done, Reference Done1992; Hughes, Reference Hughes1994; Lapointe, Reference Lapointe1997). At Sanya Bay, only the overgrowing of large forms of brown and red algae by epiphytes was observed. In particular, cyanobacterial overgrowth occurred in the low intertidal and upper subtidal zones during the dry season.
Why has eutrophication had no further impact on the flora of Sanya Bay? There are two possible explanations: (1) average concentration of dissolved organic and inorganic compounds of nitrogen and phosphorus in Sanya Bay is not enough for blooms of highly productive green macroalgae that have a high surface to volume ratio; (2) dissolved inorganic matter containing nitrogen and phosphorus is inaccessible to the majority of potentially highly productive macroalgal forms.
Evidence consistent with the first explanation is a local bloom of green macrophytes at a site where seawater runs out of pools used in the cultivation of marine animals (Titlyanov et al., in press). These cultivation pools (1 ha) for crabs, fish and shrimps are situated about 100 m from the Marine Biological Station. Evidence consistent with the second explanation can be seen in the analyses of the molar C:N ratio in the tissues of macroalgae inhabiting the Luhuitou reef. The algae were nitrogen limited even with a high concentration of dissolved inorganic nitrogen in the surrounding seawater. This suggests either a difficulty in nitrogen uptake, caused by the nitrogenous compounds themselves or by the complementary compounds necessary for their absorption, or it may suggest the presence of nitrogen assimilation inhibitors in the polluted waters of Sanya Bay (Titlyanov et al., Reference Titlyanov, Kiyashko, Titlyanova, Yakovleva, Li and Huang2011b).
Seasonal changes in species diversity and algal communities' structure in the subtidal zone
In total, in the subtidal zone during the dry season at Luhuitou Peninsula, 114 species of macroalgae, Cyanobacteria and seagrass were collected; whilst during the rainy season, 98 species were found (15% less).
In the intertidal zone (the same coastal site) during the rainy season, algal species number was 29% less than during the dry season. Species compositions of macroalgae in the intertidal zone during both the dry and rainy seasons were not significantly different: red (58% and 60%), green (22% and 24%) and brown algae (20% and 16%), respectively. During the dry season, blue–green algae were common (seven species) (Titlyanov et al., in press).
In the subtidal zone, 80% of macroalgae recorded were common during both seasons, 15% of macroalgae were found only during the dry season and 2% were found only during the rainy season. In the intertidal zone, 60% of macroalgae were common during both seasons, 30% of macroalgae were found only in the dry season and 10% were found only in the rainy season.
Thus, in the upper subtidal zone of Sanya Bay, changes in species number and their composition were insignificant from season to season. Nevertheless, in the intertidal zone (especially in the upper and middle zones), seasonal changes in flora were significant. The absence of significant changes in the subtidal flora was connected with gradual changes in factors determining species diversity (seawater temperature, light intensity and salinity). In the upper subtidal zone during the transition from the dry to the rainy season, seawater temperature decreases by 4° C to 5° C, salinity decreases by about 2‰ and light intensity decreases by 30% (Li, Reference Li2011; Table 1). Such fluctuations in environmental factors cannot evoke serious changes in the subtidal flora (Lüning, Reference Lüning1990). However, the occurrence of new species (mainly ephemeral and blue–green algae, 15% of all algae found in the subtidal area) during the dry season is likely to be a response to the increased temperature of seawater.
In the intertidal zone, with the change of season, marine plants are exposed to rapid changes in environmental factors (in comparison with subtidal conditions) resulting in partial or complete algal replacement. As has been shown in a previous study (Titlyanov et al., in press), in the intertidal zone at the Luhuitou reef, the greatest species number occurs during the winter−spring (dry) season, which in our opinion relates to optimal conditions for the occurrence and development of ephemeral and epiphytic algae (especially blue–green) and mass occurrence of young plants of annual vegetation. During the rainy season, depletion in species composition was observed, which was most likely related to the decrease in water temperature and salinity (especially in the upper and middle intertidal zones). These conditions do not promote the occurrence and growth of ephemeral algae and the majority of annual species are coming to the end of their vegetative growth period by that time.
Subtidal flora mainly represented by polydominant algal turf communities and to a lesser degree by associations of large foliose, fleshy, articulate and coriaceous algae. During the research period (5 years), species composition of algal communities was relatively constant. Seasonality in the algal turf community was generally characterized by changes in the dominant species, which formed the basis of the algal turf. For example, during the rainy season (October 2008), Amphiroa fragilissima, Jania capillacea, Hypnea pannosa (Rh) and Lobophora variegata (Ph) dominated the turf-forming species. During the dry season (April 2009) at the same site, Hypnea pannosa and Jania capillacea continued to dominate, but new dominants, such as Amphiroa foliacea, Hypnea valentiae, Acanthophora muscoides and Tolypiocladia glomerulata, also appeared. In the rainy season of November 2010, turf communities were dominated by Amphiroa fragilissima, A. foliacea, Jania capillacea and Lobophora variegata as in the previous seasons but Jania adhaerens also became a dominant species. In the dry season of 2012, previous dominants, such as H. pannosa, H. valentiae and A. muscoides, predominated but certain new inhabitants, Spyridia filamentosa, Gayliella flaccida and Centroceras clavulatum (Rh), appeared.
Thus, changes in the predominant species composition of long-living and ephemeral algae occur annually in subtidal algal turf communities. It seems likely that these changes in predominant and accompanying species reflect the natural process of species succession in the community. Algal community succession begins immediately on newly formed substratum after detachment of old macroalgae. Detached algae are annually found cast ashore in Sanya Bay from February to April.
The subtidal community structure can be changed by the appearance of ephemeral species (especially Cyanobacteria growing abundantly on larger algae) with increasing seawater temperature in the dry season.
In the upper intertidal zone, changes in dominant species occur more than once during the year not only because of the detachment of thalli from the substratum and the subsequent community succession in the newly formed space, but also because of frequent changes in ephemeral dominant species.
Studies of seasonal changes in macroalgal species composition in other tropical and subtropical regions of the World Ocean do not contradict the results found here or the conclusions drawn regarding the factors promoting these changes. For example, investigations in Nanwan Bay (southern Taiwan) showed insignificant seasonal variations in species diversity and evenness on the reef slope (upper subtidal). However, species diversity on the upper reef flat (intertidal) decreased in August−October (Tsai et al., Reference Tsai, Wong, Chang, Hwang, Dai, Yu, Shyu, Sheu and Lee2004). Seasonal changes in species diversity and composition at shallow sites were found in Brazilian coral reefs (Costa et al., Reference Costa, Zman, Nimmo and Attrill2000). On the rocky intertidal shores in the Colombian Caribbean, the macroalgal community was most diverse (23 taxa) in October, which historically has been the rainiest and calmest month of the year (García & Díaz-Pulido, Reference Garcia and Diaz-Pulido2006). Extensive ephemeral blooms of smaller, fleshy brown macroalgae, such as Chnoospora and Hydroclathrus, have been observed on shallow reef (Great Barrier Reef of Australia) predominantly during winter and early spring; large seaweeds, such as Sargassum, have peaks in biomass and reproduction during the summer and lowest biomass during the winter (Diaz-Pulido et al., Reference Diaz-Pulido, McCook, Larkum, Lotze, Raven, Schaffelke, Smith, Steneck, Johnson and Marshall2007).
The above mentioned authors consider that changes in algal communities at shallow sites are evoked by sharp changes in climatic factors occurring from season to season. However, Thakur et al. (Reference Thakur, Reddy and Jha2008) found that seasonal variation in species composition of stranded seaweeds on the north-west coast of India (Port Okha) was correlated with species succession in the natural seaweed habitat of the coast. The seaweed growth season on the Okha coast is spread over seven months, from November to May. During this period, the coast witnesses extensive growth and succession of seaweeds.
In summary, in the subtidal zone along the Luhuitou coast during October 2008, April 2009, November−December 2010 and March 2012, 156 species of marine algae and plants were collected in total, including 143 taxa (90%) of macroalgae, 12 (10%) of Cyanobacteria and one species of seagrass, Thalassia hemprichii. The macroalgae comprised 79 red (55%), 38 green (25%) and 26 brown (20%) algal species. According to species number and composition of algal communities, benthic subtidal flora in Sanya Bay (polluted with urban and mariculture waste) is close to that of relatively unpolluted regions of the Indo-Pacific. Species number and composition varied insignificantly depending on season (dry, rainy). The upper subtidal communities were characterized by a mosaic polydominant algal turf community and by a bidominant community of Sargassum species. In the polydominant community, changes in dominant species occurred mainly among annual fleshy, calcareous articulated and leathery forms. It is considered that these changes were caused by periodic annual changes in the community due to thalli detachment from hard substratum and formation and succession of new algal communities on the available substratum.
ACKNOWLEDGEMENTS
We are grateful to all members of the Marine Biological Station of the Chinese Academy of Sciences in Sanya City for use of the facilities, technical help and hospitality during the course of this research.
FINANCIAL SUPPORT
This study was partially supported by the grants ‘Succession of algal communities in the seas of tropical and temperate regions’ (2007–2009), ‘Physiological and biochemical mechanisms of benthic autotrophic organisms response on climatic and anthropogenic changes in natural habitat (ontogenetic aspects) (2012−2014)’ from the Russian Foundation for Basic Research and the National Natural Science Foundation of China (41106141 and 40830850) and the grant ‘China–Russia special funds 2009’ from the Chinese Academy of Sciences.
