Comparison of Meiofaunal Abundance in Two Mangrove Wetlands in Tong’an Bay, Xiamen, China

ZHOU Xiping, CAI Lizhe, and FU Sujing

1) Department of Environmental Science and Engineering, Xiamen University Tan Kah Kee College, Zhangzhou 363105, P. R. China

2) Key Laboratory of the Coastal and Wetland Ecosystems, Ministry of Education, Xiamen University, Xiamen 361102, P. R. China

3) Department of Environmental Science and Engineering, College of the Environment and Ecology, Xiamen University, Xiamen 361102, P. R. China

Comparison of Meiofaunal Abundance in Two Mangrove Wetlands in Tong’an Bay, Xiamen, China

ZHOU Xiping1), CAI Lizhe2),3),*, and FU Sujing2),3)

1) Department of Environmental Science and Engineering, Xiamen University Tan Kah Kee College, Zhangzhou 363105, P. R. China

2) Key Laboratory of the Coastal and Wetland Ecosystems, Ministry of Education, Xiamen University, Xiamen 361102, P. R. China

3) Department of Environmental Science and Engineering, College of the Environment and Ecology, Xiamen University, Xiamen 361102, P. R. China

? Ocean University of China, Science Press and Springer-Verlag Berlin Heidelberg 2015

To compare meiofaunal community in the two mangrove wetlands in Tong’an Bay, Xiamen, China, and probe the response of meiofauna to high organic matter, sampling was carried out in Fenglin and Xiang’an mangrove wetlands in the bay. The results showed that the Ne/Co ratio (nematode to benthic copepod) and organic matter in Fenglin mangrove wetland were higher than those in Xiang’an mangrove wetland. The meiofaunal abundance in Fenglin mangrove was all lower than that in Xiang’an mangrove wetland in summer, autumn and spring, while the meiofaunal abundance in Fenglin mangrove was higher than that in Xiang’an mangrove wetland in winter. Two-way ANOVA results showed that the meiofaunal abundance and nematode abundance were significantly different between regions, seasons and region×season. With all the results in the present study, we confirmed that the positive response of meiofaunal and nematode abundance were only detected for medium organic matter contents according to the Xiang’an wetland’s level, and that the distribution of meiofaunal abundance would be influenced by sand content. Higher copepod abundance and lower N/C value usually suggest better environmental quality.

meiofauna; nematodes; copepods; mangrove wetland; Tong’an Bay

1 Introduction

Mangroves are well-known for their diverse, worldwide environmental value (Saenger, 2003). Many of them may be close to coastal cities or areas with large human populations and be affected by anthropogenic disturbance, such as pollution, cutting down trees for wood products, clearing of forests for aquaculture, fishing, and so on (Levings et al., 1994; Rasolofo, 1997; Kairo et al., 2001). Such activities frequently alter the sediment structure in mangroves. Mangroves have a positive effect on the production of detritus and organic matter, the recycling of nutrients, enriching coastal water, and supporting the benthic population of the sea (Shah et al., 2005). Since quite a diversity of benthos living on or in the sediment, it becomes an ideal approach to examine the relationships between fauna and sediments at multiple scales and in multiple habitats (Chapman and Tolhurst, 2007). These habitats are relatively well-studied with regard to the trees themselves and larger fauna such as fish, birds, crabs and mollusks. Less is known about the small invertebrates dwelling in the sediments associated with the mangroves(Erséus, 2002).

Meiofauna, which are smaller benthic organisms, are known to utilize surface-derived material, either directly by feeding on phytodetritus, or indirectly by feeding on decomposing material and the associated bacteria (Hicks and Coull, 1983; Heip et al., 1985), had patchy patterns of distribution that are related to the availability of resources (Pinto et al., 2013). Despite the small body size of the meiofauna, they are considered to be an important link for the energy flow in the benthic food chains (Gallucci et al., 2005; Moens, et al. 2005). Furthermore, their short biological cycles and the high stability of the populations, produce in this community a rapid and unequivocal reaction to environmental changes (Coull and Chandler, 1992). The abundance, distribution, and composition of the meiofauna are sensitive to environmental perturbations, and thus, the meiofauna has become one of the major bio-indicators and is widely applied to monitor the marine environment (Zhang and Zhou, 2004; Balsamo et al., 2010; Moreno et al., 2011).

Studies on the distribution and biodiversity of meiofauna in mangrove sediments have been conducted in southern African (Dye, 1983), southeast coast of India (Ansar et al., 2014), southeastern Australia (Gwyther, 2000), west coast of Zanbibar (Olafsson et al., 2000),southeast coast of India (Chinnadurai and Fernando, 2007), Vietnam (Xuan et al., 2007), southwestern of Puerto Rico (Torres-Pratts and Schizas, 2007), even in different tropical habitats and oceanic regions such as the Caribbean, Celebes and Red Seas where there are seagrass, mangrove and reef sediments (Pusceddu et al., 2014). Some information on meiofauna in mangrove habitat has also been reported in China. Cai et al. (2000) studied the free-living marine nematodes on the mudflat in Shenzhen estuary and found that nematodes prefer to live and breed in mudflats with high content of organic matter. Guo (2008) studied the number of meiofauna and the community of nematode in Fenglin, which happens to be the place of present study, and revealed that the highest abundance of meiofauna appears at bare mudflat where waste water flows, contributing high organic matter content in the sediment (Guo, 2008). He investigated the community of free-living marine nematodes in different types of mangroves at Fenglin and demonstrated that the abundance of meiofauna in Avicennia marina mangroves is the lowest, while at the bare mudflat, an area with organic discharge, the abundance is the highest.

A field colonization experiment in subtropical Hong Kong was carried out to better understand the relationship of major meiofaunal taxa and nematode species assemblage to the decaying leaf litter of the mangrove Kandelia candel, testifying the important role of meiofauna in the process of detritus decomposition (Zhou, 2001).

However, further proof needs to be provided to confirm the response of meiofauna to mangrove habitat. The aim of the present study is to: 1) understand the distribution of meiofaunal abundance in mangrove wetlands, including nematode and copepod abundance, and 2) compare the meiofaunal abundance in the two mangrove wetlands in Tong’an Bay. A minor purpose of this study is to find if the meiofauna is affected by different organic matter supplies.

2 Materials

2.1 Study Sites

Tong’an Bay is located to the northeast of Xiamen Island, China, with a semi-diurnal tide. It covers an area of 91.7 km2, including 50.4 km2of tidal flat (Zhan et al., 2003). Two sampling sites, Fenglin (FL, 118?06′E, 24?34′N) and Xiang’an (XA, 118?11′E, 24?38′N), are located on the west coast and northeast coast of Tong’an Bay, respectively. A published study was carried out in old Fenglin mangrove area (Guo, 2008), which is near to our sampling station. Fenglin area is also near to a residential district with more freshwater inflow. Additionally, the Jimei Sewage Treatment Plant is located near the Fenglin mangrove area.

At Fenglin, five mangrove species (Kandelia obovata, Sonneratia caseolaria, S. apetala, Acanthus ilicifolius and Rhizophora stylosa) were planted in April 2004, while at Xiang’an, Kandelia obovata was planted in 2005. Five sampling stations were set in Tong’an Bay, three of them (FL1, FL2 and XA-A) were in the mangrove habitat, and the other two (FL3, XA-B) were in the non-mangrove habitat (Fig.1). All these stations were intertidal, and the three mangrove sampling stations were located on the edge of the shoreline with shorter flooding periods due to higher intertidal elevation, while the other two non-mangrove sampling stations were located between the mangrove forest and the aquacultural mudflat. There is a (Jimei) Sewage Treatment Plant and many living quarters surrounding Fenglin mangrove wetland.

Fig.1 Meiofaunal sampling stations at the two mangrove wetlands in Tong’an Bay (FL = Fenglin; XA = Xiang’an).

2.2 Sampling Procedures

Meiofauna was collected in four surveys in summer (July) 2006, autumn (October) 2007, winter (January) 2007 and spring (April) 2007. At each sampling station during each surveys, four replicate sediment sampling were collected using a 0.05 m2box corer. Undisturbed meiofaunal cores were taken using a cut-off syringe (Ф= 2.9 cm) to 10 cm depth, then divided into three layers, 0-2 cm, 2 - 5 cm, and 5 - 10 cm. Each layer was immediately placed in a 250 mL jar, and fixed in a 5% formalin and seawater solution. Back to the laboratory, samples of meiofauna were sieved using 0.5 mm and 0.042 mm mesh size; material retained on the smaller mesh size was collected. Sorting of meiofauna from the sediment was done using a flotation technique in Ludox HS40 solution (Heipet al., 1985). All meiofaunal individuals were sorted into major groups and counted under a stereoscopic microscope.

Samples for sediment analysis were also acquired in spring (April) 2007. In order to analyze the total organic matter (TOM) of the sediment, freeze-dried and homogenized sediment was first acidified with 10% HCl overnight to remove carbonate, then dried at 60℃ and analyzed (Hedges and Stren, 1984) using an EA1110 element analyzer (Carlo-Erba Co., Italy). Finally, the result was converted to TOM content. The grain composition in the sediment was analyzed using a Mastersizer 2000 (Malvern Instruments, UK). Mudflat water salinity was determined using a YS130S-C-T meter at each sampling station during the meiobenthic sampling.

2.3 Data Analysis

Meiofaunal abundance was expressed as inds·10cm-2and calculated for each mangrove wetland during each season. Univariate two-way ANOVA was used to investigate differences between the regions (Fenglin and Xiang’an), and the seasons (summer, autumn, winter and spring) for meiofaunal abundance, Pearson-Correlation analysis was applied to reveal the correlation between the abundance of total meiofauna and nematodes, with the SPSS V.16 statistical software package. The Tukey HSD multiple comparisons test was used in pair-wise comparisons of samples to explore statistically significant differences of meiofaunal abundance. MDS was carried out to analyze the meiofauna assemblages from the five stations in four seasons with PRIMER 5.0 package, the densities of genera were square root transformed based on the Bray-Curtis similarity measure.

3 Results

3.1 The Environmental Factors in Two Mangrove Wetlands

The salinity at the Fenglin was lower than that at the Xiang’an mangrove area. Additionally, the Jimei Sewage Treatment Plant is located near the Fenglin mangrove area. Based on the ‘Evaluation Standard for Sediment Pollutants’ from the ‘Concise Regulations of National Sea Island Resource Comprehensive Survey’, the critical threshold for TOM is 3.4%. Our study showed that TOM values at the three Fenglin sampling stations exceeded the critical threshold, while those of the two Xiang’an sampling stations did not. In addition, the TOM in the mangrove stations was higher than that in the non-mangrove stations (Table 1).

Table 1 The sediment salinity, median particle diameter and TOM at five stations

3.2 The Meiofaunal Community in Two Mangrove Wetlands and MDS Analysis of Meiofauna at Five Stations and in Four Seasons

The annual mean abundance of meiofauna at Fenglin and Xiang’an mangrove wetlands were 1378.4 ± 1712.2 inds·10 cm-2and 1214.1± 682.8 inds·10 cm-2, respectively. The seasonal variations of meiofaunal abundance at these two mangrove wetlands were not the same. The meiofaunal abundance in Fenglin mangrove wetland was the highest in winter, but the meiofaunal abundance in Xiang’an mangrove wetland was the highest in spring. In summer, autumn and spring, the meiofaunal abundance in Fenglin mangrove were all lower than that in Xiang’an mangrove wetland. But in winter, the meiofaunal abundance in Fenglin mangrove was the highest among all the stations (Fig.2).

Two-way ANOVA results showed that the distribution of meiofaunal individuals was significantly influenced by region, season and region×season (Table 2).

Fig.2 Meiofaunal abundance in Fenglin and Xiang’an mangrove wetlands.

Table 2 The F and P values between regions and seasons for meiofaunal abundance in Tong’an Bay

The ordination of samples by MDS analysis showed that the regional and seasonal changes for meiofaunal assemblages were observed in most sampling stations (Fig.3).

Fig.3 MDS analysis of meiofaunal assemblages based on square root transformed data of numbers of genera from the five stations and four seasons.

3.3 The Nematode Abundance in Two Mangrove Wetlands

The annual average abundance of nematodes at Fenglin and Xiang’an mangrove wetlands were 1289.7±565.3 inds·10cm-2and 1138.5±346.7 inds·10cm-2, respectively.

Fig.4 Nematode abundance in Fenglin and Xiang’an mangrove wetlands.

The seasonal variations of nematode abundance in two mangrove wetlands were not the same. The nematode abundance in Fenglin mangrove wetland was the highest in winter, but the nematode abundance in Xiang’an mangrove wetland was the highest in spring. In summer, autumn and spring, the nematode abundance in Fenglin mangrove was all lower than those in Xiang’an mangrove wetland. But in winter, the nematode abundance in Fenglin mangrove was higher than that in Xiang’an mangrove wetland (Fig.4).

Pearson-Correlation analysis showed a very significant positive correlation between the abundance of total meiofauna and nematodes (R=0.988, P＜0.01). Two-way ANOVA results showed that there were very significant seasonal variation (ANOVA, F3,68=50.321, P＜0.01) and significant temporal variation (ANOVA, F4,68= 2.948, P＜0.05) in the density of nematodes. In addition, a significant interaction effect between region×season was detected (ANOVA, F12,68= 15.242, P＜0.01) (Table 2).

3.4 The Benthic Copepod Abundance in Two Mangrove Wetlands

The annual average benthic copepod abundance at Fenglin and Xiang’an mangrove wetlands were 25.3 ± 9.4 inds·10cm-2and 66.0 ± 7.0 inds·10cm-2, respectively (Fig.5). Pearson-Correlation analysis showed no significant correlation between the abundance of the total meiofauna and the benthic copepod (R = -0.542, P=0.345＞0.05). Two-way ANOVA results showed that there was no significant seasonal variation (ANOVA, F3,68=2.490, P＞0.05) but there was a significant spatial variation (ANOVA, F4,68= 3.986, P＜0.01) in benthic copepod abundance. In addition, no significant interaction effect between region×season was detected (ANOVA, F12,68=0.736, P＞0.05) (Table 2).

Fig.5 Benthic copepod abundance in Fenglin and Xiang’an mangrove wetlands.

3.5 The Ne/Co Ratio (Nematode to Benthic Copepod) in Two Mangrove Wetlands

The seasonal mean Ne/Co ratio in the present study ranged from 9.00 to 154.13. Fenglin mangrove generally showed the higher values of the Ne/Co ratio, with the only exception of the summer. It is interesting that the Ne/Co ratio is higher than 100 in the winter and spring at Fenglin.

Table 3 Ratio of nematodes to benthic copepods (Ne/Co)

4 Discussion

In general, meiobenthic abundance may be impacted by several factors, such as salinity, sediment particle size, organic matter content, chlorophyll content, water temperature, water depth, and self-propagation (Danovaroand Fabiano, 1995; Mirto et al., 2000; Liu, 2005; Khan et al., 2012). Organic pollution may significantly affect the meiofaunal community (Carman et al., 1997; Cai et al., 2000; Guo, 2008). In present study, the meiofaunal abundance in Fenglin mangrove in summer, autumn and spring was all lower than those in Xiang’an mangrove wetland in the same season. The factor affecting the distribution of meiofauna in present study may relate to organic matter content. By adding extra organic matter to the mud from estuary, Schratzberger and Warwick (1998a) found that low organic matter inflow did not affect the marine nematode abundance, while medium and high amount of organic matter inflow made the abundance of marine nematodes drastically reduced. This phenomenon is not only found at mangrove wetland, but also found in intertidal zone and subtidal zone. The persistently high sediment nutrient levels might limit the colonization of meiofauna leading to lower abundance (Liu et al., 2011). Also, a higher density of nematodes has been found in sediments of sandy nature, whereas there is lower total organic carbon compared to silt/clay composition (Ansari et al., 2014).

Vanhove (1992) compared meiofauna of five mangrove vegetation types in Gazi Bay and concluded that particle size and oxygen conditions are major factors influencing meiobenthic distribution. Lower meiofaunal abundance in Fenglin mangrove in three seasons compared to Xiang’an mangrove wetland might also relate to different sand contents. Raffaelli (1987) pointed out that nematodes could be expected to increase in abundance in both coarse and fine sediment habitats. The sediment in Xiang’an mangrove wetland is finer than in Fenglin mangrove wetland (Table 1), which might help to increase the nematodes abundance in Xiang’an mangrove wetland.

But in winter, meiofauna abundance in Fenglin mangrove bloomed and reached the peak in the year. As nematode is the most dominant meiofaunal group in the present study, the change of nematode abundance has the most important effect on total meiofaunal structure. Nematodes have been suggested to become opportunistic species because of their potential rapid reproduction which allows them to dominate the initial stages of faunal succession after a disturbance or adverse condition (Schratzberger and Warwick, 1998b). In general, recolonization of populations of smaller and short-lived organisms is expected to be more rapid than longer lived species (Driskell et al., 1996). As Schratzberger and Warwick (1998b) pointed out, medium frequency of disturbance help marine nematodes reach high abundance, and low frequency and high frequency disturbance results in the decrease of abundance. Following an adverse condition for most invertebrate in winter, nematodes in Fenglin mangrove wetland got medium disturbance and became dominated. Therefore, nematode communities have increasingly been used to assess the effects of environmental perturbations (Gyedu-Ababio et al., 1999; Dye, 2006), even used as indicators of pollution (Moore and Bett, 1989; Essink and Keidel, 1998; Boyd et al., 2000; Moreno, 2011).

The state of meiofaunal assemblages may better reflect the overall health of the marine benthos, especially for detecting early response to environmental changes (Kennedy and Jacoby, 1999). Different sediment qualities will result in different meiobenthic community composition and different meiobenthic abundance. Whether considering numbers or biomass, benthic copepods is the second commonest dominant group in the meiobenthic community in present study. Compared to some nematodes that are used as indicator species for organic pollution, benthic copepod is more sensitive to environmental pollution than other meiofaunal group (Findlay, 1981; Raffaelli and Mason, 1981; Semprucci et al., 2010; Frontalini et al., 2011). Also, much research has focused on whether the ratio of nematode density to copepod density (the N/C or R ratio) can be an index to the organic pollution status. Raffaelli and Mason (1981) and Warwick (1981) believed that the R ratio can be such an index, but the range of R ratio which indicates the pollution status is still controversial. Anyway, the accuracy and applicability of the Nematode/Copepod index (N/C) in monitoring the effects of environmental disturbances is controversial (Sun et al., 2014).

Benthic copepod abundance in Xiang’an were higher than those in Fenglin mangrove wetland all the four seasons. Higher abundance of benthic copepod and lower N/C value in Xiang’an mangrove in the present study, corresponded with the sediment characteristics, especially with the organic matter. With all the results in the present study, we confirmed the positive response of meiofaunal and nematode abundance to medium organic matter contents (organic matter contents in Xiang’an area was medium, while in Fenglin, the organic matter contents were considered to be high), and showed that the distribution of meiofaunal abundance would be influenced by sand content. Higher copepod abundance and lower R/C value usually suggest better environmental quality.

Acknowledgements

The present project is supported by the National Natural Science Foundation of China (Grant No. 41176089), and also supported by WEL (abbreviation of Key Laboratory of the Coastal and Wetland Ecosystems, Ministry of Education) Visiting Fellowship Program from Xiamen University. The authors would like to thank the staff and students in the benthic ecology laboratory in Xiamen University for their assistance in the field work and for their help with sampling procedures.

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(Edited by Ji Dechun)

(Received April 8, 2014; revised February 12, 2015; accepted March 8, 2015)

J. Ocean Univ. China (Oceanic and Coastal Sea Research)

DOI 10.1007/s11802-015-2642-9

ISSN 1672-5182, 2015 14 (5): 816-822

http://www.ouc.edu.cn/xbywb/

E-mail:xbywb@ouc.edu.cn

* Corresponding author. E-mail: cailizhe@xmu.edu.cn