Seasonal and spatial variation in species diversity, abundance, and element accumulation capacities of macroalgae in mangrove forests of Zhanjiang, China

Seasonal and spatial variation in species diversity, abundance, and element accumulation capacities of macroalgae in man-grove forests of Zhanjiang, ChinaZHANG Yubin1*, LI Yuan1, SHI Fei1, SUN Xingli1, LIN Guanghui2 1 Monitoring Center for Marine Resources and Environments, Guangdong Ocean University, Zhanjiang

524088, China2 Graduate School at Shenzhen, Tsinghua University, Shenzhen 518055, China

Received 20 December 2012; accepted 19 July 2013

©The Chinese Society of Oceanography and Springer-Verlag Berlin Heidelberg 2014

AbstractThe objective of this study was to investigate whether there was distinctive seasonal and zonal variation in the species diversity, biomass, and element accumulation capacities of macroalgae in two major intertidal mangrove stand types (Avicennia marina assemblage and Sonneratia apetala assemblage) in the Zhanjiang region of southern China. Over a year, 31 species in 15 genera were identified in both mangrove assem-blages, of which the dominant species were Cladophoropsis zollingeri and Enteromorpha clathrat. Macroal-gal species were significantly most abundant in spring (p<0.05), followed by summer, winter, and autumn. Variation in the zonal distribution of macroalgal species was conspicuous in both intertidal mangrove as-semblages, with the greatest abundance in the middle zone, and the least in the front zone. Patterns in the seasonal and zonal variation in macroalgal biomass in the S. apetala assemblage were similar to those of macroalgal species diversity in both mangrove assemblages. The seasonal patterns in tissue concentrations of 15 analyzed elements were not uniform among the macroalgae C. zollingeri, E. clathrata, and Gracilaria salicornia in the A. marina assemblage. All three species exhibited variation in their responses to ambient concentrations of different elements, implying their differential ability to absorb and selectively accumulate certain elements.Key words: mangrove macroalgae, seasonal variation, intertidal, biomass, element concentration

Citation: Zhang Yubin, Li Yuan, Shi Fei, Sun Xingli, Lin Guanghui. 2014. Seasonal and spatial variation in species diversity, abun-dance, and element accumulation capacities of macroalgae in mangrove forests of Zhanjiang, China. Acta Oceanologica Sinica, doi: 10.1007/s13131-014-0414-9

1 IntroductionMangroves are tropical and subtropical intertidal woody-

plant communities, representing one of the most biologically important ecosystems in coastal areas (Lin et al., 1997). They are vital to the health of coastal environments, as they provide a source of carbon and nutrients for food chains, generate oxy-gen through photosynthesis, act as nursery grounds for inverte-brate marine fauna (Melville and Pulkownik, 2007a), maintain high regional biodiversity and productivity, and sustain and improve human livelihood (Han and Gao, 2009; Pérez-Estrada et al., 2012). Various species of macroalgae are associated with mangrove forests, where they grow epiphytically on aerial roots (pneumatophores and prop roots), trunks, mud surfaces, and other hard substrata (Lin et al., 1997; Zuccarello et al., 2001; Nedumaran and Perumal, 2009; Pérez-Estrada et al., 2012). Epiphytic macroalgal mats form an important photosynthetic component in many mangroves worldwide (Pérez-Estrada et al., 2012). These macroalgae are exposed to the steep environ-mental gradients associated with estuarine or coastal environ-ments, involving emersion and submersion during tidal cycles, and fluctuating temperature, salinity, light, and nutrient condi-tions (Davey and Woelkerling, 1985; Melville et al., 2005; Mel-ville and Pulkownik, 2007a). As a result, temporal and spatial variations in mangrove macroalgal assemblages have been in-

vestigated extensively, e.g., in Australia (King, 1995; Laursen and King, 2000; Melville et al., 2005; Melville and Pulkownik, 2007a), Japan (Tanaka and Chihara, 1987), Indonesia (Tanaka and Chi-hara, 1988), Kenya (Coppejans and Gallin, 1989), Papua New Guinea (King, 1990), Malaysia (Aikanathan and Sasekumar, 1994), South Africa (Phillips et al., 1994; 1996), Brazil (Yokoya et al., 1999), Egypt (El-Sharouny et al., 2001), South India (Nedu-maran and Perumal, 2009), Mexico (Pérez-Estrada et al., 2012) and China (Lin et al., 1997; Liu et al., 2001). It was found from these investigations that the mangrove macroalgae exhibited significant seasonal and spatial variations affected by the tem-perature, inundation frequency, desiccation tolerance of algal species, and other factors. Macroalgae, including those in man-groves, are capable of absorbing and accumulating elements, including nutrients as well as non-nutrient heavy metals, into their tissues, to well above ambient levels in water and sedi-ment (Zhang et al., 2003; Melville and Pulkownik, 2006, 2007b). Therefore, they have been widely used as bioindicators or bio-monitors to assess metal contamination in coastal or estuarine environments (Melville and Pulkownik, 2006, 2007b).

The Zhanjiang Mangrove National Nature Reserve, with a total area of 7 256×104 m2 (accounting for about 33% of the total mangrove area in China, and 79% of the total mangrove area in Guangdong Province, China), is located on the Leizhou

Acta Oceanol. Sin., 2014

DOI: 10.1007/s13131-014-0414-9

http://www.hyxb.org.cn

E-mail: [email protected]

Foundation item: Public Science and Technology Research Funds Projects of Ocean in China under contract Nos 201305021 and 201105008-E. *Corresponding author, E-mail: [email protected]

ZHANG Yubin et al. Acta Oceanol. Sin., 20142

Peninsula in the extreme south of China Mainland, and is the largest mangrove reserve in China Mainland. Mangroves grow zonally along the coast of this peninsula, which is characterized by the highest abundance, diversity, and density of mangrove plants in China Mainland. In this reserve, true mangrove and semi-mangrove plants together comprise 15 families and 25 species (Han and Gao, 2009). Although ecological researches on mangrove communities, zooplankton, zoobenthos, mollusks, fish, and birds have been conducted in this area (Han and Gao, 2009), no such research record exists for macroalgae. Lin et al. (1997) and Liu et al. (2001) reported macroalgal assemblages in mangrove areas located in Fujian, southeastern China, how-ever, little information is available on mangrove macroalgae in southern China. Accordingly, the aim of this study was to ex-amine seasonal variation and intertidal zonation of macroalgae diversity in Avicennia marina (Forsk) Vierh. and Sonneratia apetala Buch.-Ham assemblages, seasonal and intertidal varia-tion in macroalgal biomass in the latter, and element accumu-lation by dominant macroalgal species in the former. This may contribute to improving our understanding of the biodiversity and ecological functions of macroalgae in mangrove forests.

2 Materials and methods

2.1 Study sitesMacroalgal samples were collected from the A. marina as-

semblage (Site 1, named S1; 21°06.38 N, 110°19.25 E) and the S. apetala assemblage (Site 2, named S2; 21°06.69 N, 110°19.02 E) in the vicinity of the Donghai Embankment within the reserve (Fig. 1). These two mangrove assemblages are situated near each other with an intervening distance of less than 2.4 km (Fig. 1). This sampling region has a humid south-subtropical climate accompanied by maritime influences, with annual average air and surface seawater temperatures of 22.5 and 20.9°C, respec-tively. During sampling, the air and surface seawater tempera-tures were measured on the spot with a portable thermometer. Both mangrove assemblages are monodominant, where the Avicennia marina and Sonneratia apetala assemblages repre-sent natural and artificial forests, respectively. In the A. marina assemblage, the plant density was observed to be about 30 per

quadrat of 25 m2 (5 m×5 m), with an average plant height of about 1.6 m, a canopy density of more than 95%, and a large population of seedlings and pneumatophores that together in-terfered with sample collection. The S. apetala assemblage was characterized by a plant density of about 13 per quadrat of 25 m2 (5 m×5 m), with an average plant height of about 5 m, a can-opy density of about 75%–80%, and a large population of pneu-matophores emerging from the surface. The main environ-mental parameters for water and sediment in both mangroves, based on analysis of seasonal samples, are listed in Table 1.

2.2 Sample collectionMacroalgae samples in both mangrove forests were season-

ally collected on April 13 (spring), July 5 (summer), and Octo-ber 22 (autumn) during 2008, and January 29 (winter) in 2009, after ebb tide. Within each site (Fig. 1), three permanent tran-sects were created along the tidal gradient, and different inter-tidal levels (i.e., front, middle, and back intertidal zones from seaward to landward) were marked in each transect according to the methods described by Melville and Pulkownik (2007b). Two replicate stations for sampling in the front and back inter-tidal zones were respectively established at a distance of 2 m into the mangrove stand from the mangrove canopy edge, with the middle intertidal stations (two replicates) halfway between those two in each transect (Melville and Pulkownik, 2007b). In the three different zones of each transect, the macroalgae samples on different substrata, such as aerial roots (pneumato-phores and prop roots), trunks, mud surfaces, shell fragments, and other hard substrata, were collected with small forceps and a knife, placed into labeled plastic bags containing a small quantity of seawater, and immediately transported back to the laboratory on ice for analysis. The frequency of occurrence and distributional zones of each macroalgal species were recorded when sampling.

2.3 Sample analysis

2.3.1 Macroalgae identification and dominance of species Macroalgae samples were washed thoroughly with water to

remove any foreign materials, such as adhering sediment par-ticles and rotten bark, and then temporarily mounted on slides

21°18′N

N

16 km

3 km

109°42′ 109°54′ 110°06′ 110°18′ 110°30′ 110°42′ E 110°18′36″ 110°19′48″ 110°21′00″ E

21°06′

21°06′

21°05′

21°04′

20°54′

20°42′

Zhanjiang BayZhanjiang Bay

Leizhou Bay

Fig.1. Geographical positions of sampling sites.

ZHANG Yubin et al. Acta Oceanol. Sin., 2014 3

for microscope analysis (Nikon Eclipse 80i, Tokyo, Japan). Iden-tities of macroalgal species were assigned based on the existing taxonomic system (Zeng, 1983) and literature (Zeng, 1983; Qian et al., 2005; Consilio Florarum Cryptogamarum Sinicarum Ac-daemiae Sinicae Edita, 1999–2011; Zhao, 2012). The dominance of macroalgal species was defined according to the average rel-ative abundance of species from all stations, namely, rare, com-mon, and dominant species with average relative abundances below 20%, 20%–50%, and above 50%, respectively.

2.3.2 Macroalgal biomassGenerally, mangrove macroalgae grow epiphytically on aer-

ial roots (pneumatophores and prop roots), trunks, and other hard substrates, making it difficult to investigate and determine the macroalgal biomass using the quadrat method, as is per-formed on intertidal mudflats. This was particularly prominent in the A. marina assemblage due to the high canopy density and low plant heights. However, in the S. apetala assemblage, the quadrat method was used successfully. In this assemblage, the macroalgal samples were randomly selected in three 30 cm×30 cm quadrats in each zone, collected seasonally, and placed into plastic bags (after discarding the mud, small twigs, and other impurities), and transported back to the laboratory on ice. The macroalgal samples were then washed thoroughly, placed on small glass Petri dishes, dried in an oven at 80°C until a constant dry weight was achieved, and then weighed to express the mean macroalgal biomass as grams of dry weight per square meter (g/m2).

2.3.2 Elemental analysisIn the A. marina assemblage, the macroalgae tissues of sev-

eral dominant species, including Cladophoropsis zollingeri, Gracilaria salicornia, and Enteromorpha clathrata were avail-able in sufficient amounts for analysis, and were therefore used as representative samples to measure elemental concentra-tions over time. These samples were successively rinsed with tap water and deionized water (Milli-Q grade). Subsequently, the samples were freeze-dried, homogenized, reduced to a fine powder, and passed through a 200-mesh sieve. Subsamples of each sieved sample were digested in two replicates to measure elemental concentrations.

Total N and P concentrations were determined after diges-tion with concentrated sulfuric acid/hydrogen peroxide, using colorimetric analysis (Bao, 2005). The concentrations of K, Na, Ca, and Mg were determined with an Atomic Absorption Spec-trophotometer (Varian AA240FS AAS), and the Cr, Mn, Fe, Ni, Cu, Zn, As, Cd, and Pb concentrations were detected using In-

ductively Coupled Plasma Mass Spectrometry (Agilent 7500cx ICP-MS) after digestion with nitric acid/perchloric acid (Bao, 2005). Reagent grade standards, certified reference sediments (shore marine sediment GBW 07314, The Second Institute of Oceanography, State Oceanic Administration of China), certi-fied reference plant material (Laminaria japonica tissue GBW 08517, The Second Institute of Oceanography, State Oceanic Administration of China), and internal reference standards from Agilent company were routinely used as controls for the analytical methods to ascertain the reliability of the methods and results. Recoveries were greater than 80% for all elements. Analyses of element concentrations were similarly performed for eight water samples and 12 sediment samples collected from the corresponding macroalgal habitats.

Element concentration factors in macroalgal tissues were calculated as the ratio of the concentration of an element in the tissue to its concentration in the adjacent substrata (water or sediment). Concentration factors were calculated for individual elements in each algal species to evaluate the algal capacity for element accumulation (Melville and Pulkownik, 2007b).

2.4 Statistical analysisDifferences in species diversity of macroalgae among four

seasons in both mangrove assemblages were examined using a nonparametric Wilcoxon test, and analysis of variance (ANO-VA) was utilized to assess the differences in macroalgal bio-mass among seasons and among three intertidal zones in the S. apetala assemblage. A significant level was accepted when p<0.05 in each statistical analysis performed in SPSS (Ver. 16.0) for Windows.

3 Results

3.1 Seasonal variation in the macroalgae diversity in both mangrove assemblagesIn the four seasonal sampling periods, mean air and water

temperatures were as follows: spring (water 19.3°C, air 17.2°C); summer (water 28.8°C, air 29.2°C); autumn (water 24.8°C, air 25.2°C); winter (water 13.2°C, air 12.5°C). The species diversi-ties of macroalgae in both mangrove assemblages are listed in Tables 2 and 3. In the four seasons, 31 species in 15 genera were recognized in the two mangrove assemblages together, in-cluding 9 species and 4 genera of Cyanophyta, 5 species and 3 genera of Rhodophyta, 16 species and 7 genera of Chlorophyta, and 1 species and 1 genus of Phaeophyta. All these species were present in the A. marina assemblage (Table 2), and most in the S. apetala assemblage as well (Table 3).

Table 1. Main physico-chemical characteristics of seawater and sediment in the two mangrove assemblages studied

Water factorAvicennia marina

assemblage

Sonneratia apetala

assemblageSediment factor

Avicennia marina

assemblage

Sonneratia apetala

assemblage

pH 8.02±0.31 7.96±0.26 ST light clay light clay

Salinity 28.1±2.3 22.3±4.6 pH 4.41±0.08 6.32±0.13

DO/mg·L−1 6.85±0.30 6.56±0.38 Salinity 25.1±3.2 19.0±2.6

DOC/mg·L−1 3.07±0.27 3.40±0.36 OC/mg·g−1 20.3±2.1 17.2±1.8

DIN/mg·L−1 0.432±0.066 0.493±0.072 TN/mg·g−1 1.93±0.24 1.52±0.21

DIP/mg·L−1 0.040±0.006 0.043±0.009 TP/mg·g−1 0.67±0.09 0.58±0.06

TN/mg·L−1 0.907±0.103 0.966±0.128

TP/mg·L−1 0.121±0.020 0.142±0.017

Notes: DO represents dissolved oxygen, OC organic carbon, DOC dissolved organic carbon, DIN dissolved inorganic nitrogen, DIP dis-solved inorganic phosphorus, TN total nitrogen, TP total phosphorus, and ST soil texture.


The seasonal pattern of macroalgae species in the A. marina assemblage was as follows: spring (30 species) > summer (24 species) > winter (14 species) > autumn (12 species). The spe-cies diversity of macroalgae was significantly more abundant in spring than in other seasons (Wilcoxon test, p<0.05), as was summer relative to winter and autumn (Wilcoxon test, p<0.05). The dominant species were Caloglossa leprieurii, Catenella im-pudica, Gracilaria salicornia, and Cladophoropsis zollingeri in spring; G. salicornia, Enteromorpha clathrata, and C. zollingeri in summer; E. clathrata and C. zollingeri in winter; and only C. zollingeri in autumn. During the entire year, C. zollingeri was prevalent as the dominant species, while C. leprieurii, C. impu-dica, G. salicornia, and E. clathrata were seasonally dominant species. Some algae classified as eurythermal species appeared in all four seasons, for example, Lyngbya confervoides, Oscil-latoria amphibian, and O. nigro-viridis in Cyanophyta; and E. prolifera, E. clathrata, Monostroma nitidum, Ulva lactuca, C.

zollingeri, and Rhizoclonium implexum in Chlorophyta. In the S. apetala assemblage, 27 species in 14 genera were

present, including 7 species and 3 genera of Cyanophyta, 5 species and 3 genera of Rhodophyta, 14 species and 7 genera of Chlorophyta, and 1 species/genus of Phaeophyta (Table 3). Seasonal species diversity resembled that in the A. marina as-semblage, namely spring (25 species) > summer (22 species) > winter (5 species) > autumn (2 species), and significantly higher species diversity of macroalgae was found in spring and sum-mer than in winter and autumn (Wilcoxon test, p<0.05). The dominant species were C. leprieurii, C. impudica, G. salicornia, E. clathrata, and C. zollingeri in spring; G. salicornia, E. clath-rata, and C. zollingeri in summer; only E. clathrata in winter; and no dominant species in autumn except the occasional oc-currence of Oscillatoria bonnemaisonii (Cyanophyta) and E. clathrata (Chlorophyta). Most dominant species appeared in the spring and summer, implying that the temperature, mois-

Table 2. Seasonal variation in the composition of macroalgae species in the Avicennia marina assemblageSpecies Spring Summer Autumn Winter

Cyanophyta

Lyngbya confervoides Ag. + + + +

Lyngbya sp. + + − +

Oscillatoria amphibian C. Ag. + + + +

O. bonnemaisonii Crou. + − + +

O. nigro−viridis Thwaites + + + +

Phormidium fragile Gom. + − − −

P. tenuis Ag. + − − −

P. naveanum Grumow var. marina Tseng. et Hua. + + + −

Trichodesmium erythraeum Her. ++ − − −

Subtotal 9 5 5 5

Rhodophyta

Caloglossa leprieurii (Mont.) J. Ag. +++ ++ − −

Catenella impudica (Mont.) J. Ag. +++ ++ − −

Gracilaria coronompifolia J. Ag. + + − +

G. salicornia (C. Ag.) Dawson. +++ +++ − +

G. tenuisitipitata C. F. ++ ++ − ++

Subtotal 5 5 0 3

Chlorophyta

Chaetomorpha aerea (Dillw.) K tz. + + − −

C. macrotona Sur. + + − −

C. media (Ag.) K tz. + + − −

C. sp. + + − −

Cladophora fascicularis (Mert.) K tz + + − −

Cladophoropsis zollingeri (Kutzing) Reinbold +++ +++ +++ +++

Enteromorpha clathrata (L.) Grev. ++ +++ ++ +++

E. compressa (L.) Grev. + − − −

E. intestinalis (L.) Grev. + + − −

E. linza (L.) J. Ag. + − − −

E. prolifera (M ll.) J. Ag + + + +

Monostroma nitidum Wittr. ++ ++ + ++

Rhizoclonium implexum (Dillw.) K tz. ++ ++ + +

R. riparium (Roth.) K tz. + + − −

Ulva lactuca L. ++ ++ + +

U. pertusa Kjellm + + − −

Subtotal 16 14 6 6

Phaeophyta

Dictyota dichotoma (Huds.) Lamx. − − + −

Subtotal 0 0 1 0

Total 30 24 12 14

Notes: + represents rare species, ++ common species, +++ dominant species, and − no species.


ture, and light influenced their seasonal changes. Similar obser-vations were made by Karsten et al. (1994), Lin et al. (1997), and Liu et al. (2001).

3.2 Zonal variation in the macroalgae diversity of both man-grove assemblagesSince the macroalgae were most abundant in spring, the

zonal variation in their species composition was analyzed in both mangrove assemblages in this season (Table 4). Similar zonal patterns were observed in both assemblages, with the most abundant species growing in the middle zone, including the dominant species C. leprieurii, C. impudica, C. zollingeri, E. clathrata, G. salicornia, M. nitidum, U. lactuca, R. implexum, and Chaetomorpha spp. The back zone contained the second highest proportion of macroalgal species, including E. clathra-ta, M. nitidum, U. lactuca, and R. implexum in both assemblag-es, and C. leprieurii in just the A. marina assemblage. The front zone included C. leprieurii and E. clathrata in both assemblag-es, and M. nitidum and U. lactuca in only the A. marina assem-blage. Generally, C. leprieurii, M. nitidum, E. clathrata, and U.

lactuca were present in all three zones of the A. marina assem-blage while only E. clathrata was ubiquitous over all three zones of the S. apetala assemblage. R. implexum was mainly distrib-uted in the middle and back zones in both assemblages while C. zollingeri and G. salicornia thickly covered the sediment surface in the middle zone of both assemblages. Other macroalgae spe-cies were scattered across the different zones (Table 4).

3.3 Variation in the macroalgal biomass in the Sonneratia apetala assemblageThe highest biomass of macroalgae in all zones was found

in spring, with an annual average of 104.5 g/m2 (Table 5), fol-lowed by summer and then winter in the Sonneratia apetala as-semblage (ANOVA, p<0.05). The intertidal zone was almost bare in autumn in this assemblage despite occasional occurrence of two species (Oscillatoria bonnemaisonii and Enteromorpha clathrata), resulting in the least macroalgal biomass. Except for autumn, the significant difference in macroalgae biomass was found among the three zones (ANOVA, p<0.05), with an annual average of 55.1, 43.0, and 29.8 g/m2 in the middle, back, and

Table 3. Seasonal variation in the composition of macroalgae species in the Sonneratia apetala assemblageSpecies Spring Summer Autumn Winter

Cyanophyta

Lyngbya sp. + + − −

Oscillatoria amphibian C. Ag. + + − −

O. bonnemaisonii Crou. + + + +

O. nigro-viridis Thwaites + + − +

Phormidium tenuis Ag. + − − −

P. fragile Gom. + − − −

P. naveanum Grumow var. marina Tseng. et Hua. − + − −

Subtotal 6 5 1 2

Rhodophyta

Caloglossa leprieurii (Mont.) J. Ag +++ ++ − −

Catenella impudica (Mont.) J. Ag. +++ ++ − −

Gracilaria. coronompifolia J. Ag. + + − −

G. tenuisitipitata C. F. ++ ++ − −

G. salicornia (C. Ag.) Dawson. +++ +++ − −

Subtotal 5 5 0 0

Chlorophyta

Chaetomorpha aerea (Dillw.) K tz. + + − −

C. media (Ag.) K tz. + + − −

Cladophora fascicularis (Mert.) K tz + + − −

Cladophoropsis zollingeri (Kutzing) Reinbold. +++ +++ − −

Enteromorpha clathrata (L.) Grev. +++ +++ + +++

E. compressa (L.) Grev. + − − −

E. intestinalis (L.) Grev. + + − −

E. linza (L.) J. Ag. + − − −

E. prolifera (M ll.) J. Ag + − − −

Monostroma nitidum Wittr. ++ ++ − +

Rhizoclonium implexum (Dillw.) K tz. ++ ++ − −

R. riparium (Roth.) K tz. + + − −

Ulva lactuca L. ++ ++ − +

U. pertusa Kjellm + + − −

Subtotal 14 11 1 3

Phaeophyta

Dictyota dichotoma (Huds.) Lamx. − + − −

Subtotal 0 1 0 0

Total 25 22 2 5

Notes: + represents rare species, ++ common species, +++ dominant species, and − no species.


front zones, respectively.

3.4 Bioaccumulation of elements in the dominant macroal-gae of the Avicennia marina assemblageOwing to the presence of sufficient biomass for analysis, C.

zollingeri, G. salicornia, and E. clathrata were selected as repre-sentative dominant species to investigate variation in the con-centrations of 15 elements (Table 6). On the basis of elemental analysis, the element concentration factors in macroalgal tissue were then calculated (Tables 7 and 8).

The three macroalgal species revealed varying capacities for accumulating elements in different seasons (Table 6). No distinct differences were found among different seasons for the concentrations of the majority of elements in tissues of C. zollingeri. The exceptions included Mn, which was noticeably higher in winter, and P, which was higher in autumn and winter than in spring and summer. The concentrations of K in winter and Cr in summer were obviously lower than in the other sea-sons.

The concentrations of N, K, Mg, and Ca in G. salicornia tis-sue were higher in spring than in summer, but not for the other 11 elements. Similarly, the concentrations of N, P, K, Na, Mg, and Ca in E. clathrata tissue were higher in summer than in win-ter, while the reverse was demonstrated for the other nine ele-ments. In other words, the species exhibited differences in their seasonal capacities to bioaccumulate elements, with different seasonal patterns observed for any given element.

Element concentration factors were not uniform across the three macroalgal species, indicating that inter-specific dif-ferences in elemental uptake and accumulation may exist to some extent (Tables 7 and 8). Macroalgae are relatively sensi-

tive to ambient changes in nutrient and heavy metal concen-trations (Brito et al., 2012). Furthermore, they only respond to the soluble elemental fraction, and do not reflect element levels associated with sedimentary or particulate material (Brito et al., 2012). Therefore, we focused on the element concentration factors relative to seawater. In this study, the bioaccumulation capacities for a certain element were not necessarily correlated to its ambient concentration. For example, sodium was the ele-ment present with the highest ambient concentrations, but all three macroalgal species displayed the lowest bioaccumulation capacities for this element among the 15 studied, with the ele-ment concentration factors ranging from 0.7–2.6. Similar pat-terns were observed for other abundant elements, including K, Ca, and Mg. On the other hand, cadmium was the least abun-dant element in seawater (0.13 μg/L), however, the bioaccumu-lation abilities of C. zollingeri, G. salicornia, and E. clathrata for Cd were quite high, with concentration factors of 6 923, 14 615, and 2 308, respectively. The concentration of Fe (4.95 μg/L) was also considerably low in seawater, but its concentration factors in all three macroalgae were more than 1×106. High concentra-tion factors were also observed for Cu, Pb, Zn, Cd, As, Ni, and Cr, with the corresponding element concentration factors vary-ing from 1 502–47 591 (Table 7). The powerful bioaccumulation capacities of these species for the essential nutrients nitrogen and phosphorus resulted in fairly high element concentration factors ranging from 22 418–163 333 (Table 7).

4 Discussion Generally, the majority of mangrove-associated macroal-

gae have a pantropical distribution (King, 1995). In this study, we identified 31 species and 15 genera, many of which were

Table 4. Zonal distribution of macroalgal species in both intertidal mangrove assemblagesMangrove assemblage Back zone Middle zone Front zone

Avicennia marina Caloglossa leprieurii

Enteromorpha clathrata

Monostroma nitidum

Rhizoclonium implexum

Caloglossa leprieurii

Catenella impudica

Chaetomorpha spp.

Cladophoropsis zollingeri


Gracilaria salicornia

Monostroma nitidum


Ulva lactuca



Monostroma nitidum

Ulva lactuca

Sonneratia apetala Enteromorpha clathrata

Monostroma nitidum



Catenella impudica

Chaetomorpha spp.

Cladophoropsis zollingeri


Gracilaria salicornia

Monostroma nitidum


Ulva lactuca



Table 5. Macroalgal biomass in the Sonneratia apetala assemblage (g/m2)Zone Spring Summer Autumn Winter Mean ±SD

Back zone 113.2 33.9 0 24.9 43.0±49.0

Middle zone 125.4 65.8 0 29.1 55.1±54.1

Front zone 74.8 28.6 0 15.9 29.8±32.2

Mean±SD 104.5±26.4 42.8±20.1 0±0 23.3±6.7 42.6±44.8


Tab

le 6

. E

lem

ent c

on

cen

trat

ion

s in

mac

roal

gal t

issu

es, s

edim

ent,

an

d s

eaw

ater

in th

e A

vice

nn

ia m

arin

a as

sem

bla

ge

Sam

ple

s Se

aso

nN

/mg·

g−1

P

/mg·

g−1

Na

/mg·

g−1

K

/mg·

g−1

Mg

/mg·

g−1

Ca

/mg·

g−1

Mn

/mg·

g−1

Fe

/mg·

g−1

Cr

/μg·

g−1

Ni

/μg·

g−1

Cu

/μg·

g−1

Zn

/μg·

g−1

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recognized as hygrophilous and thermophilous or euryther-mal. However, there were large variations in the geographical distribution of macroalgal species in the study area in com-parison with others, such as Sydney, Australia (8 species and 6 genera; Melville and Pulkownik, 2006), Beachwood mangroves of South Africa (18 species; Phillips et al., 1994), Japan (23 spe-cies; Tanaka and Chihara, 1987), Papua New Guinea (25 species; King, 1990), South India (16 species; Nedumaran and Perumal, 2009), Malaysia (10 species; Aikanathan and Sasekumar, 1994), Indonesia (33 species; Tanaka and Chihara, 1988), Brazil (18 taxa; Yokoya et al., 1999), Estero Zacatecas, Mexico (67 species; Pérez-Estrada et al., 2012), and Fujian, China (42 species; Lin et al., 1997). The low species diversity in some of the aforemen-tioned studies can be considered typical of the temperate man-grove areas of the Southern Hemisphere (Phillips et al., 1994; Melville et al., 2005; Melville and Pulkownik, 2007a). It appears to be a trend that the species diversity of mangrove macroalgae increases from temperate to tropical regions. Some studies have suggested that the mean surface water temperature is one of the important physical factors influencing macroalgal growth, abundance, and geographical distribution in different regions (Lin et al., 1997; Nedumaran and Perumal, 2009). Nevertheless, no abundant species of macroalgae were found in mangroves of South India (16 species; Nedumaran and Perumal, 2009) or Malaysia (10 species; Aikanathan and Sasekumar, 1994), both of which are located in the tropics. This suggests that other fac-tors, such as nutrient levels, tidal level, salinity, and substrata of attachment may also play important roles (Lin et al., 1997; Liu et al., 2001; Pérez-Estrada et al., 2012). In other words, the species diversity is related to the unique habitat. In addition, the adaption of species and the degree of shade would influence inter-site variation in species diversity (Lin et al., 1997), given that most species of macroalgae prefer shaded areas (Karsten et al., 1994). In the present study, although both mangrove assem-blages were adjacent to each other, more abundant macroalgae were found in the A. marina assemblage than in the S. apetala assemblage, which was attributed to the high plant and canopy density in the former creating a more suitably shaded envi-ronment, since the removal of a shade-producing canopy can

cause the disappearance of macroalgae from newly exposed pneumatophores and other substrata of attachment (Davey and Woelkerling, 1985).

The species composition was characteristic of the majority of Chlorophyta and Rhodophyta in this study. Worldwide, few differences exist with regard to the dominant macroalgae spe-cies in different mangrove areas, although the “Bostrychia–Ca-loglossa” association has been considered globally representa-tive of assemblage composition, including in Australia (Davey and Woelkerling, 1985; King, 1995; Melville et al., 2005; Melville and Pulkownik, 2007a), Asia (Tanaka and Chihara, 1987; 1988; Aikanathan and Sasekumar, 1994; Lin et al., 1997), and Africa (Coppejans and Gallin, 1989; King, 1990; Phillips et al., 1994). However, in the present study, the most abundant species with high occurrence frequency belonged to Chlorophyta and Rho-dophyta in both mangrove assemblages (Tables 2 and 3). Based on our observations of dominant species in the two assem-blages, Chlorophyta species were dominant year-around, while other species in Rhodophyta and Chlorophyta were seasonal. Although Oscillatoria species were present in four seasons, they exhibited a scattered pattern without remarkable seasonal changes, consistent with that observed in the Fujian mangrove areas (Liu et al., 2001). This phenomenon was also observed in other mangroves around the world, such as Rhizoclonium spp. in Jiulongjiang Estuary, China (Liu et al., 2001), Selangor, Malay-sia (Aikanathan and Sasekumar, 1994), Beachwood, South Af-rica (Phillips et al., 1994), and Ilha do Cardoso, Brazil (Yokoya et al., 1999); Enteromorpha and Cladophora in Pichavaram, South India (Nedumaran and Perumal, 2009); Catenalla spp. in Yunx-iao, China (Lin et al., 1997) and Maluku, Indonesia (Tanaka and Chihari, 1988); and Caulerpa sertularioides in Estero Zacatecas, Mexico (Pérez-Estrada et al., 2012).

In our study, the seasonal pattern in macroalgal species di-versity presented the following sequence in both mangrove as-semblages: spring > summer > winter > autumn, as did that of macroalgal biomass in the S. apetala assemblage. In the Fujian mangrove assemblages, the total number of macroalgal spe-cies were highest in spring and summer (Liu et al., 2001), while the total macroalgal biomass was highest in early summer and

Table 8. Element concentration factors of macroalgal tissues relative to sediment in the Avicennia marina assemblageMacroalgal species N P Na K Mg Ca Mn Fe

Cladophoropsis zollingeri 12 15 0.8 16.7 1.8 4.6 13.3 0.7

Gracilaria salicornia 14 29 3.2 19.2 2.8 3.4 6.7 0.3

Enteromorpha clathrata 11 20 1.5 3.9 4.3 2.8 2.0 0.5

Macroalgal species Cr Ni Cu Zn As Cd Pb

Cladophoropsis zollingeri 0.7 1.0 1.2 1.2 1.6 8.2 0.7

Gracilaria salicornia 0.5 0.9 1.2 1.2 1.1 17.3 0.6

Enteromorpha clathrata 0.6 0.5 0.6 0.7 1.1 2.7 0.5

Table 7. Element concentration factors of macroalgal tissues relative to seawater in the Avicennia marina assemblage Macroalgal species N P Na K Mg Ca Mn Fe

Cladophoropsis zollingeri 26 264 85 833 0.7 280 10.5 4.0 6 182 3 696 970

Gracilaria salicornia 29 231 163 333 2.6 322 16.4 2.9 3 091 1 777 778

Enteromorpha clathrata 22 418 110 833 1.2 66 25.2 2.4 927 2 808 081

Macroalgal species Cr Ni Cu Zn As Cd Pb

Cladophoropsis zollingeri 47 591 4 357 3 020 18 404 5 881 6 923 33 933

Gracilaria salicornia 32 117 3 830 3 089 19 618 4 104 14 615 27 303

Enteromorpha clathrata 38 759 2 398 1 502 11 551 4 164 2 308 25 730


lowest in early winter (Lin et al., 1997). This parallels what we observed. A similar seasonal pattern in mangrove macroalgal biomass was elucidated in Hurghada and Safaga, Egypt by El-Sharouny et al. (2001). Distinct summer peaks of macroalgal biomass were also reported in temperate South African man-groves, a finding that was attributed to increased nutrient avail-ability, temperature, and light levels (Steinke and Naidoo, 1990). Furthermore, the higher number of macroalgal species was recorded by Nedumaran and Perumal (2009) in Pichavaram, South India during the pre-monsoon season owing to the fa-vorable physico-chemical parameters. In contrast, the highest number of taxa was observed during the colder, drier months in the mangroves of Ilha do Cardoso, Brazil (Yokoya et al., 1999), coinciding with the highest means of high neap tides and con-tracted periods of continuous emersion (April to August). Yet another pattern was noted in the Estero Zacatecas mangroves in Mexico (Pérez-Estrada et al., 2012): the seasonal species di-versity varied relative to substrata (pneumatophores, aerial roots, and tidal channel bottoms), while the highest macroalgal biomass was recorded in November of the observation year due to effects from a hurricane. Surprisingly, no seasonal variation in macroalgal diversity and abundance (biomass) was detected in mangroves near Sydney, Australia (Laursen and King, 2000; Melville et al., 2005; Melville and Pulkownik, 2007a). Thus, it can be concluded that the seasonal patterns in macroalgal diversity and biomass are highly variable and dependent on the specific physiogeographical and ecological characteristics of specific habitats. In our study conducted in a warm subtropical region, the warmer air and water temperatures and suitable light in-tensity (Karsten et al., 1994), together with the most humid weather in spring, facilitated a vigorous growth of macroalgae that supported higher species diversity and biomass through-out the year. The decrease in these two parameters in summer was likely caused by unfavorably high temperatures and light intensities, and low humidity, a pattern that persisted into au-tumn. In winter, the reversal of this pattern began to rejuvenate macroalgal growth.

Tidal inundation and the related wetting frequency in both mangrove assemblages were found to diminish from the front to back zone. Consequently, there was prominent variation in macroalgal species diversity and biomass among intertidal zones. These observations are in accordance with those from mangroves along the Parramatta River, Australia (Melville et al., 2005). In our study, the occurrence of abundant macroalgal spe-cies diversity and biomass in the middle zone were linked to the moderate emersion and submersion frequencies, high canopy density, and favorable light levels (high shade). Conversely, the long periods of emersion and weak tolerance to desiccation may have resulted in limited macroalgal diversity and biomass in the back zone. The low abundance and diversity of macroal-gae in the front zone can be attributed to the low canopy density and high light levels in spite of relatively long periods of sub-mersion in this study.

E. clathrata and C. leprieurii grew in most zones in the two mangrove assemblages, while M. nitidum and U. lactuca were distributed across all three zones in the A. marina assemblage. These macroalgae possess relatively high tolerance to desicca-tion. Many studies have reported that the horizontal zonation of macroalgal diversity and biomass is present in intertidal mangroves (Coppejans and Gallin, 1989; Aikanathan and Sase-kumar, 1994; Phillips et al., 1994; Yokoya et al., 1999; El-Sharou-

ny et al., 2001; Liu et al., 2001; Melville et al., 2005; Melville and Pulkownik, 2007a). The alternative changes of environmental factors such as water temperature, dissolved oxygen, salin-ity, and in particular, the emersion and submersion frequency based on tidal cycles, create this zonation (Melville et al., 2005; Melville and Pulkownik, 2007a). We hypothesized that the em-ersion and submersion frequency of macroalgae, amount of shading, and tolerance to desiccation were the key factors in determining the zonal distribution and abundance (biomass) of macroalgae in this study.

No apparently seasonal differences were observed regarding element concentrations in Caloglossa zollingeri tissue, with the exception of P, K, Ca, and Mg. However, the concentrations of several elements in the tissues of E clathrata and G salicornia were seasonally variable. This was similar to what was reported in four estuarine mangroves in Australia, where no significant seasonal variations in the concentrations of Cu, Pb, Zn, Cd, Cr, Ni, Mg, and Fe were detected in tissues of Bostrychia sp., Calo-glossa leprieurii, and Catenella nipae (Melville and Pulkownik, 2007b). Zhang et al. (2003) reported apparent seasonal differ-ences in nutrient content in the tissues of C. leprieurii in a Kan-delia candel assemblage, Jiulongjiang Estuary, China, with the highest concentrations of N, P, K, and Na in spring accompany-ing vigorous macroalgal growth. Seasonal differences in metal concentrations in macroalgal tissues were also observed by Ak-cali and Kucuksezgin (2011). There may be a number of reasons for these differences, including the following: environmental factors, such as variations in ambient element concentrations and their interactions, salinity, and pH; and metabolic factors, such as dilution of metal concentrations due to growth (Akcali and Kucuksezgin, 2011). However, concentrations of nutrients such as N and P increased during the period of active growth (Zhang et al., 2003). As a result, there were different seasonal patterns in element concentrations of macroalgal tissues in mangroves located in different regions, which may be explained by the variation in biological properties among these species and their corresponding habitats.

In our study, we measured element concentration factors that indicated relatively low variability in the capacities of dif-ferent macroalgal species to accumulate elements, since three macroalgal species were within the same mangrove assem-blage (Tables 7 and 8). However, other studies have shown that the corresponding concentration factors were highly variable across macroalgal species (Melville and Pulkownik, 2007b; Ak-cali and Kucuksezgin, 2011; Brito et al., 2012). When compar-ing variation among the concentration factors for different el-ements, a high degree of variation was observed in our study, similar to what was noted by Akcali and Kucuksezgin (2011), who analyzed seven macroalgal species, revealing that they possessed extraordinary abilities to accumulate metals to levels several thousand times higher than ambient levels in seawater, with the sole exception of Pb (less than seven times). Among the 15 elements measured in our study, the three macroalgal spe-cies exhibited the highest concentration factors for iron, similar to what was observed in Liusha Bay, Zhanjiang, China (Zhang et al., 2010), where the highest concentration factors were also that of iron, among 11 metals analyzed in 21 species of macroal-gae. This was because the uptake of iron can promote macroal-gae to absorb nitrogen, phosphorus, and other nutrients (Yao, 1987). We also observed relatively high concentration factors for N and P relative to ambient levels in water, implying that they


were able to absorb a large amount of nutrients from seawater during active growth (Zhang et al., 2003). In addition, they were able to accumulate a large amount of heavy metals into their tissues from seawater (Table 7). However, the K, Na, Ca, and Mg were not extensively absorbed into macroalgal tissues despite their high levels in seawater. Therefore, it can be concluded that the macroalgal species examined in our study have the abil-ity to selectively accumulate certain elements, independent of the environmental factors. Nevertheless, other studies have reported the occurrence of a certain degree of inter-specific dif-ferences in elemental uptake and accumulation (Melville and Pulkownik, 2007b; Akcali and Kucuksezgin, 2011; Brito et al., 2012).

In our investigation, Cladophoropsis zollingeri was a pre-dominant species throughout the year, with a high biomass and good capacity to tolerate relatively high metal concentrations. Hence, this macroalgal species is suitable for use as a biomoni-tor in this mangrove area according to the definition and char-acteristics of biomonitors (Melville and Pulkownik, 2007b).

References

Aikanathan S, Sasekumar A. 1994. The community structure of mac-roalgae in a low shore mangrove forest in Selangor, Malaysia. Hydrobiologia, 285(1–3): 131–137

Akcali I, Kucuksezgin F. 2011. A biomonitoring study: Heavy metals in macroalgae from eastern Aegean coastal areas. Marine Pollution Bulletin, 62(3): 637–645

Bao Shidan. 2005. Soil analysis in agricultural chemistry (third edition) (in Chinese). Beijing: China Agricultural Science Press, 21–126

Brito G B, de Souza T L, Bressy F C, et al. 2012. Levels and spatial distri-bution of trace elements in macroalgae species from the Todos os Santos Bay, Bahia, Brazil. Marine Pollution Bulletin, 64(10): 2238–2244

Consilio Florarum Cryptogamarum Sinicarum Acdaemiae Sinicae Edita. 1999–2011. Flora Algarum Marinarum Sinicarum, Tomus II, Rhodophyta; Tomus III, Phaeophyta (in Chinese). Beijing: China Science Press

Coppejans E, Gallin E. 1989. Macroalgae associated with the man-grove vegetation of Gazi Bay (Kenya). Belgium Journal of Botany, 122(1): 47–60

Davey A, Woelkerling W J. 1985. Studies on Australian mangrove algae: I. Victorian communities: composition and geographic distribu-tion. Proceedings of the Royal Society of Victoria, 91: 53–66

El-Sharouny H M, El-Tayeb M A, Ismail M S. 2001. Macroalgae asso-ciated with mangroves at Hurghada and Safaga of the Egyptian Red Sea Coast. Journal of KAU: Marine Science, 12(Special Issue): 241–251

Han Weidong, Gao Xiumei. 2009. Mangrove Ecosystem and Protection Strategy on Leizhou Peninsula (in Chinese). Guangzhou: South China University of Technology Press, 1–10

Karsten U, Koch S, West J A, et al. 1994. The intertidal red alga Bostry-chia simpliciuscula Harvey ex J. Agardh from a mangrove swamp in Singapore: acclimation to light and salinity. Aquatic Botany, 48(3–4): 313–323

King R J. 1990. Macroalgae associated with the mangrove vegetation of Papua New Guinea. Botanica Marina, 33(1): 55–62

King R J. 1995. Mangrove macroalgae: a review of Australian studies. Proceedings of Linnean Society of New South Wales, 115: 151–161

Laursen W J, King R J. 2000. The distribution and abundance of man-grove macroalgae in Woolooware Bay, New South Wales, Austra-lia. Botanica Marina, 43(4): 377–384

Lin Peng, Chen Zhenfen, Liu Weigang. 1997. Ecological researches on

macroalgae in Fujian mangrove areas. Acta Botanica Sinica (in Chinese), 39(2): 176–180

Liu Weigang, Lin Yiming, Chen Zhenfen, et al. 2001. Distribution and seasonal change of algae in Fujian mangrove areas. Acta Ocean-ologica Sinica (in Chinese), 23(3): 78–86

Melville F, Pulkownik A. 2006. Investigation of mangrove macroalgae as bioindicators of estuarine contamination. Marine Pollution Bul-letin, 52(10): 1260–1269

Melville F, Pulkownik A. 2007a. Seasonal and spatial variation in the distribution of mangrove macroalgae in the Clyde River, Aus-tralia Macroalgae in the Parramatte River, Australia. Estuarine, Coastal and Shelf Science, 71(3–4): 683–690

Melville F, Pulkownik A. 2007b. Investigation of mangrove macroalgae as biomonitors of estuarine metal contamination. Science of the Total Environment, 387(1–3): 301–309

Melville F, Pulkownik A, Burchett M. 2005. Zonal and seasonal variation in the distribution and abundance of mangrove macroalgae in the Parramatta River, Australia. Estuarine, Coastal and Shelf Sci-ence, 64(2–3): 267–276

Nedumaran T, Perumal P. 2009. Temporal and spatial variations in the structure of macroalgal communities associated with man-groves of Pichavaram (South India). Botany Research Interna-tional, 2(3): 198–205

Pérez-Estrada C J, León-Tejera H, Serviere-Zaragoza E. 2012. Cyano-bacteria and macroalgae from an arid environment mangrove on the east coast of the Baja California Peninsula. Botanica Ma-rina, 55(2): 187–196

Phillips A, Lambert G, Granger J E, et al. 1994. Horizontal zonation of epiphytic algae associated with Avicennia marina (Forssk.) Vi-erh. pneumatophores at Beachwood Mangroves Nature Reserve, Durban, South Africa. Botanica Marina, 37(6): 567–576

Phillips A, Lambert G, Granger J E, et al. 1996. Vertical zonation of epi-phytic algae associated with Avicennia marina (Forssk.) Vierh. pneumatophores at Beachwood Mangroves Nature Reserve, Durban, South Africa. Botanica Marina, 39(1–6): 167–175

Qian Shuben, Liu Dongyan, Sun Jun. 2005. Marine Phycology (in Chi-nese). Qingdao: China Ocean University Press, 42–208

Steinke T D, Naidoo Y. 1990. Biomass of algae epiphytic on pneumato-phores of the mangrove Avicennia marina, in the St Lucia estu-ary. South Africa Journal of Botany, 56(2): 226–232

Tanaka J, Chihara M. 1987. Species composition and vertical distribu-tion of macroalgae in brackish water of Japanese mangrove for-ests. Bull Natn Sci Mus, Tokyo, Ser B, 13(4): 141–150

Tanaka J, Chihara M. 1988. Macroalgae in Indonesian mangrove for-ests. Bull Natn Sci Mus, Tokyo, Ser B, 14(3): 93–106

Yao Nanyu. 1987. Algological Physiology (in Chinese). Dalian: Dalian University of Technology Press, 151–267

Yokoya N S, Plastino E M, Braga M D R A, et al. 1999. Temporal and spatial variations in the structure of macroalgal communities as-sociated with mangrove trees of Ilha do Cardoso, São Paulo state, Brazil. Revista Brasileira de Botânica, 22(2): 195–204

Zeng Chengkui. 1983. Common Seaweeds of China (in Chinese). Bei-jing: Science Press, 13–165, 249–301

Zhang Caixue, Bai Fujin, Sun Xingli, et al. 2010. Trace elements of spring and winter macroalgae in Liusha Bay. Oceanologia et Limnologia Sinica , 41(1): 154–160

Zhang Yubin, Lin Peng, Deng Aiying, et al. 2003. Seasonal variation of several nutrient elements of red alga Caloglossa leprieurii in Kandelia candel forest in Jiulongjiang Estuary, Fujian of China. Marine Science (in Chinese), 27(10): 46–49, 78

Zhao Sufen. 2012. Marine Algae and Algal Culture Science (in Chinese). Beijing: China National Defense Industry Press, 21–94

Zuccarello G C, Yeates P H, Wright J T, et al. 2001. Population structure and physiological differentiation of haplotypes of Caloglossa leprieurii (Rhodophyta) in a mangrove intertidal zone. Journal of Phycology, 37(2): 235–244

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Seasonal and spatial variation in species diversity, abundance, and element accumulation capacities of macroalgae in mangrove forests of Zhanjiang, China