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in mangrove sediments of Zhujiang (Pearl River) Estuary. LIU Weiqiu1∗ , ZHANG Jielong1, TIAN Guanghong2, XU Hualin3, YAN Xiaohua1. 1 School of Life ...
Acta Oceanol. Sin., 2013, Vol. 32, No. 4, P. 82-88 DOI: 10.1007/s13131-013-0302-8 http://www.hyxb.org.cn E-mail: [email protected]

Temporal and vertical distribution of microphytobenthos biomass in mangrove sediments of Zhujiang (Pearl River) Estuary LIU Weiqiu1∗ , ZHANG Jielong1 , TIAN Guanghong2 , XU Hualin3 , YAN Xiaohua1 1

School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China Management Office of Qi’ao-Dangan Provincial Nature Reserve, Zhuhai 519002, China 3 Guangdong Neilingding-Futian National Nature Reserve, Shenzhen 518040, China

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Received 5 December 2011; accepted 2 November 2012 ©The Chinese Society of Oceanography and Springer-Verlag Berlin Heidelberg 2013

Abstract Being a primary producer, Microphytobenthos (MPB) play an important role in the benthic ecosystem of mangrove swamps. The temporal and vertical distribution of MPB biomass, expressed as chlorophyll a (Chl a), was investigated in mangrove swamps on the Qi’ao island and the Futian Mangrove Nature Reserve, Guangdong Province, South China. Both locations are situated in the Zhujiang (Pearl River) Estuary. For each location, bi-monthly sampling was carried out at four sites during low tide period. Except one site on the Qi’ao Island, which was in Phragmites australis marsh, all sites were in mangrove swamps. The Chl a concentration in surface (0–1 cm) sediment ranged from 0.2 µg/cm3 to 8.3 µg/cm3 in the Qi’ao Island and from 2.1 µg/cm3 to 15.6 µg/cm3 in the Futian Mangrove Reserve. The peak Chl a concentration occurred in winter or early spring, while the lowest Chl a concentration, with a value of about one quarter of the peak, was observed in summer or early autumn. The vertical distribution of Chl a concentration exhibited an exponential decline with depth, which indicated a muddy sediment with high organic matter, and the slope of the curve was positively related to Chl a concentration in the surface sediment. The MPB biomass of the Qi’ao Island was significantly lower than that of the Futian Mangrove Reserve. Our results suggest that the overlaying water quality might influence the MPB biomass in surface sediments. Key words: microphytobenthos, mangrove, biomass, chlorophyll a, vertical distribution Citation: Liu Weiqiu, Zhang Jielong, Tian Guanghong, Xu Hualin, Yan Xiaohua. 2013. Temporal and vertical distribution of microphytobenthos biomass in mangrove sediments of Zhujiang (Pearl River) Estuary. Acta Oceanologica Sinica, 32(4): 82–88, doi: 10.1007/s13131-013-0302-8

exotic mangrove trees were introduced in order to restore the mangrove forest as fast as possible. The ecological risk of exotic species and the function of the restored mangrove should be evaluated successfully in order to manage the mangrove ecosystems in a more rational way (McKee and Faulkner, 2000; Ellison, 2000). Although the difference between benthic animals (especially economic animals) from restored and natural mangrove forests was widely studied (Bosire et al., 2008), no reports that compare MPB from restored and natural mangrove forests or MPB from different types of restored mangrove forests were found. The aim of this study was to: (1) analyze the temporal and spatial pattern of the MPB biomass in different mangrove forests of the Zhujiang (Pearl River) Estuary; (2) assess the effects of mangrove species on the MPB biomass and (3) discuss the environmental factors that affect the MPB of mangrove forests.

1 Introduction Mangrove forests, which are distributed widely on mudflats of tropical and subtropical coastlines, are plant communities dominated by salt- and flood-tolerant trees and shrubs. The high productivity and biodiversity of mangrove forests and their contributions to reduce coastal erosion and provide protection from tropical cylones and tidal waves make it a widely valued coastal ecosystem (Unesco, 1979). As one of the primary producers in mangrove swamps, microphytobenthos (MPB) serve as a common food for certain coastal animals, such as fishes, crabs, prawns and so on (Kang et al., 2007; Choy et al., 2008; Ribeiro and Iribarne, 2011). Although there are some reports about MPB of unvegetated sand and mud flats and salt marshes (MacIntyre et al., 1996; Welker et al., 2002; Mundree et al., 2003; Méléder et al., 2007; Du et al., 2010), few are available that describe the temporal and spatial pattern of MPB in mangrove swamps (Chen et al., 2005; Farooq and Siddiqui, 2011), and this hinders a profound understanding of the functions and processes of the mangrove ecosystem. On the other hand, since the late 1970s, efforts were undertaken to restore and re-create mangrove forests worldwide (Field, 1998; Milano, 1999; Lewis III, 2000). Mangrove trees were always planted in single-species plantations and sometimes,

2 Materials and methods 2.1 Study site Two locations in the Zhujiang Estuary were selected. One was located on the Qi’ao Island (22◦ 23′ –22◦ 27′ N, 113◦ 36′ –

Foundation item: The National Natural Science Foundation—Joint Founds of Guangdong Province under contract No. U0633002; the National Natural Science Foundation of China (NSFC) under contract No. 31070470; the Project of Science and Technology Bureau of Zhuhai City under contract No. 200901023. *Corresponding author, E-mail: [email protected]

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113◦ 40′ E) and the other in the Futian Mangrove Reserve (22◦ 32′ N, 114◦ 03′ E) (Fig. 1). The study area belongs to the south subtropical monsoon climate zone with plenty of sunlight and rainfall. The annual average temperature is 22–24◦ C, with the lowest monthly average temperature in January (15◦ C) and highest monthly average temperature in July (28◦ C). The annual precipitation is about 1 800 mm. The area of Qi’ao island is 24 km2 . About 600 hm2 of mangrove forests were historically distributed in the tidal land of the island, but only 32.2 hm2 were preserved in the 1990s. Since 1999, Sonneratia caseolaris and S. apetala were introduced to the area from Bengal and the Hainan

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Island of China respectively and now the planted S. caseolaris and S. apetala forests are the main mangrove forests around the island. The area of the Futian Mangrove Reserve is only 368 hm2 , with an area of mangrove forests of about 70 hm2 . About half of the mangrove forests were composed of endemic mangrove species, such as Kandelia candel, Aegiceras corniculatum and Avicennia mariana, and the rest are composed of species introduced to the area from the Hainan Island, Bengal or Australia. The introduced mangrove species include S. caseolaris, S. apetala, Rhizophora stylosa, Bruguiera sexangula, Avicennia marina var. australasica, and so on.

Fig.1. Map of the studied locations with sampling sites. a. The Qi’ao Island and b. the Futian mangrove reserve. Dotted areas indicate intertidal zone. KC represents Kandelia candel, SC Sonneratia caseolaris, SA S. apetala, and PA Phragmites australis on the Qi’ao Island respectively. KCf represents K. candel, AM Avicennia mariana, SKC young K. candel, and SCf S. caseolaris in Futian Mangrove Reserve respectively.

2.2 Sampling From January 2009 to December 2009, samples were collected from the Qi’ao Island about every two months. Sediment samples were collected from four sites, namely, KC, SA, SC and PA. Of these, KC site was in a natural K. candel swamp, which was not impacted by anthropological or natural disturbance; SC site and SA site were located in planted S. caseolaris and S. apetala swamps respectively, which were planted in 2000; while PA site was located in a natural Phragmites australis marsh. Samples were collected from the Futian Mangrove Reserve from December 2009 to September 2010 and four sites (KCf, AM, SKC, SCf ) were selected for sediment sampling. KCf site and AM site were located in naturally revegetated K. candel

and Avicennia mariana swamps respectively, which were about 20 years old. SKC site was in a young K. candel swamp of only 2-years, which had been S. apetala swamp before 2008. SCf site was located in a S. caseolaris swamp planted in 2000. Three sediment cores were collected from each site in a 1 m2 area, using a tailor-made injector with the bottom being cut, and then sectioned into 1 cm slices down to 5 cm depth. The samples were transferred to the laboratory in labeled polythene bottles and analyzed for chlorophyll (Chl a) concentration as soon as possible. After being extracted by 90% ethanol, Chl a concentration was determined spectrophotometrically according to the method of Cong et al. (2007). Chlorophyll a concentration of each 1 cm slice was expressed as µg/cm3 .

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Three additional sediment cores of the upper 5 cm were sampled from each site using a PVC tube (D=5 cm) with the top equipped with a rubber stopper and the samples from each site were mixed and analyzed as a composite sample for the determination of physico-chemical parameters. After being air-dried and passed through a 2-mm sieve, the sediment samples were analyzed for pH, TOC (total organic carbon), TN (total nitrogen) and TP (total phosphorus). Sediment pH was determined using a pH-meter. TOC, TN and TP were determined using the method introduced by Bao (1999), namely, TOC and TN were determined using the potassium dichromate oxidation-outside heating method and the semi-micro Kjeldahl method respectively, while TP was determined using the molybdenum antimony-ascorbic acid colorimetric method after the samples were digested using the HClO4 -H2 SO4 method. 2.3 Data analysis The variation between sites or locations was analyzed using one-way ANOVA and the LSD test was used to identify differences at alpha equaling 5% significance level. Paired-samples tests were performed to test differences of Chl a concentration in each depth of the sediment as well as the ratio of Chl a concentration in surface (0–1 cm) sediment to that in 1–2 cm depth of the sediment between different sites or different locations. Pearson correlations were calculated to infer relationships between sediment physico-chemical variables and Chl a concentration in surface (0–1 cm) sediment and between Chl a concen-

tration in sediment of different depths, with P levels given in the text. Regression curves of the vertical distribution of Chl a were conducted following the equations of C z = C 0 × exp(−b × z ) (Du et al., 2010), which were inferred from the model of Brotas and Serˆ odio (1995). C z and C 0 represent Chl a concentration at depth z and at the surface depth respectively. b = k /v , where k represents specific degradation rate of Chl a to phaeopigments; v represents mean burial velocy. As k and v were not measured in the study, the parameter b was used instead of k /v as introduced by Du et al. (2010). The equation was applied to each bimonthly data set and the correlation between b and C 0 and the surface Chl a concentration was determined by Pearson correlation analysis. 3 Results 3.1 Sediment physico-chemical characteristics Nitrogen and TOC of KC site were higher than other sites, while pH was lower than other sites (Table 1). TOC of PA and AM site were lower than other sites. In both locations, pH in S. caseolaris swamps was higher than 6, while that in K. candel swamp was lower than 5. The physico-chemical parameters of SC and SCf tend to be more similar than the sites which had different mangrove species. No significant difference was found between the sediment physico-chemical parameters of the Qi’ao Island and Futian Mangrove Reserve (statistical results not shown).

Table 1. Sediment physico-chemical parameters of each site in the Qi’ao Island and the Futian Mangrove Reserve (mean±1 SD) Location Qi’ao Island

Futian Mangrove Reserve

Site

TN/g·kg−1

TP/g·kg−1

TOC/g·kg−1

pH

SA KC SC PA AM SCf KCf SKC

1.72±0.40ab 2.45±0.63c 1.53±0.21ab 1.35±1.23a 1.99±0.26bc 1.45±0.23ab 1.90±0.30abc 1.41±0.17ab

0.55±0.06 0.68±0.11 0.63±0.09 0.53±0.08 0.53±0.16 0.57±0.06 0.65±0.29 0.49±0.04

38.7±7.4d 73.6±23.4e 31.6±4.9bcd 20.7±5.4ab 18.4±8.2a 23.7±6.1abc 34.1±5.8bcd 41.4±9.0d

5.51±1.17ab 4.62±1.71ab 6.58±0.57bc 6.87±1.15c 5.52±0.68ab 6.67±0.82bc 4.77±0.82a 5.56±0.61ab

Notes: KC represents Kandelia candel, SC Sonneratia caseolaris, SA S. apetala, and PA Phragmites australis on Qi’ao Island, respectively. KCf represents K. candel, AM Avicennia mariana, SKC young K. candel, and SCf S. caseolaris in the Futian Mangrove Reserve respectively. Each measure with different letters indicate significant difference between sites.

3.2 Chl a concentration In both locations, biomass of MPB decreased with increasing depth. The fastest decline occurred in surface (0–1 cm) sediment and 1–2 cm depth and became slower at depth lower than 2 cm (Figs 2 and 3). Generally, about 40% of the total Chl a in the upper 5 cm of sediment was distributed in the surface depth. Regression analysis show that the equation C z = C 0 × exp(−b ×z ) fitted the observed data significantly with P0.05). C 0 and b of the regression curves varied largely due to the variable Chl a concentration in surface (0–1 cm) sediment (Chl a1). However, b was significantly related to C 0 and Chl a in the surface (0–1 cm) sediment for data sets of the Futian Mangrove Reserve (P