Seasonal Distribution of Meiofaunal Assemblages in the Mangrove Tidal Flat of Futian, Shenzhen, China

SONG Yuanliu, YAN Cunjun, GAO Chunzi, XU Hualin, HUA Er,and LIU Xiaoshou,

Seasonal Distribution of Meiofaunal Assemblages in the Mangrove Tidal Flat of Futian, Shenzhen, China

SONG Yuanliu1), 2), YAN Cunjun1), GAO Chunzi1), XU Hualin3), HUA Er1),and LIU Xiaoshou1), 2),*

1),,,266003,2),,266003,3),518040,

Meiofauna are fundamental components in mangrove ecosystem which play important roles in the energy flow and mat- ter cycling. In order to reveal the spatio-temporal distribution of meiofaunal assemblages in mangrove habitats, sediment samples were collected in July (summer) and October (autumn) of 2013, January (winter) and April (spring) of 2014 in the mangrove tidal flat of Futian, Shenzhen, China. A total of 14 meiofaunal taxa were identified, including free-living marine nematodes, benthic copepods, polychaetes, oligochaetes, ostracods, isopods,. Additionally, there were also undetermined taxa. Results showed that the abun- dance range of meiofauna was (488.35±71.29)–(5136.36±623.38)ind(10cm)−2. Marine nematodes were the most dominant group, with an average abundance of (1869.56±227.92)ind(10cm)−2, accounting for 98.35% of the total abundance of meiofauna. The sea- sonal distribution of meiofauna showed that the abundance was the highest in summer, followed by those in spring, winter, and au- tumn. Vertical distribution showed that meiofauna were mainly distributed in the upper sediment layer (0–5cm), with a proportion of 89.56%. Correlation analysis between meiofauna and environmental factors showed that meiofaunal abundance and biomass had significantly negative correlation with salinity. BIOENV analysis between meiofaunal assemblages and environmental factors show- ed that meiofaunal assemblages were affected by the combined effects of temperature, salinity, sediment median grain size, water content, and chlorophyllcontent.

meiofauna; taxa composition; abundance; mangrove tidal flat; seasonal distribution

1 Introduction

Mangroves are trees and shrubs that grow in saline coas- tal habitats in the tropics and subtropics. Mangrove wet- lands are a special type of wetland ecosystem in the tran- sition zone between terrestrial ecosystems and marine eco- systems (Cao, 2008). As an important ecological type of coastal ecosystem, mangroves are also one of the most productive natural ecosystems on earth (Daza, 2020). Mangroves provide a considerable abundance and diver- sity of living resources, and they play an important role in preventing and controlling pollution of coastal waters and protecting the biodiversity of coastal areas. Mangrove eco- systems are one of the most versatile habitats for micro- organisms with high potentials (Nathan, 2020). Man- groves also function as windbreaks and embankments toprotect coastal areas from erosion (Field, 1998; Lewis, 2005; Pinto, 2013).

Meiofauna are a group of benthic animals that can pass through a 0.5mm mesh but retained by a 0.042mm mesh. Several scholars have suggested the use of 0.031mm mesh screen as the lower limit for meiofauna (Zhang and Zhou, 2004), because there are some mature individuals of meio- fauna can be retained between 0.031mm mesh and 0.042mm mesh. Therefore, in this study, a 0.031mm mesh was used as the lower limit. Meiofauna are key components and an intermediate link in marine food chains. As consumers, they play important roles in matter cycling and energy flow in the mangrove ecosystem. Meiofauna have been widely used in marine environmental monitoring and ecosystem health evaluation systems (McIntyre, 1969; Zhang, 2017; Majdi., 2020; Zhao and Liu, 2021).

Mangrove habitats possess complex organic detrital food chains, and serve as feeding ground and refuge for sur- rounding microorganisms (Zhu, 2012). In the man- grove ecosystem, several benthic organisms thrive because of the rapid progress of the matter cycle (Ghosh and Man- dal, 2019). Among the benthic metazoans, meiofauna is the most dominant in number (Netto and Gallucci, 2003; Zhao, 2020). Meiofauna play an ecologically important role as a food source for macrofauna and in organic matter re-cycling (Murray, 2002; Danovaro, 2007; Wang, 2019). The Futian Mangrove Reserve is located in the northeast of Shenzhen Bay (22˚30΄N, 113˚56΄E), China. It is distributed in a strip shape with an area of approxi- mately 367.64hm2, comprising of land area of 139.92hm2and tidal area of 227.72hm2. It is the only national nature reserve in the Chinese hinterland (Lu, 2014). Several re- searches have been carried out in the Futian Mangrove ha-bitat of Shenzhen Bay, including environmental pollution (Zheng and Lin, 1996) and ecological (Chen, 1996) studies. Research on macrofauna in the Futian Mangrove in Shenzhen began with the study of macrofauna commu- nities (Gao, 2004), focusing mainly on communitystructure, population ecology, and pollution ecology (Ma, 2003; Cai, 2011). The study of meiofauna in the mangrove of the Futian Mangrove area of ShenzhenBay started in 1997, mainly on the species compositionand seasonal variation of marine nematodes in Futian mud- flats (Cai, 2000). Tan(2017) reported the struc- ture of meiofauna communities in the mangrove area ofFutian. The purpose of this study was to investigate the spa- tio-temporal dynamics of taxa composition, abundance, and biomass of meiofauna in the mangrove tidal flat of Futian, and to examine the influence of environmental factors on meiofauna population and biomass.

2 Materials and Methods

2.1 Field Sampling

Sediment samples for meiofauna and environmental fac- tors analysis were collected in July (summer) and October (autumn) of 2013, January (winter) and April (spring) of 2014 at 10 sites in the Guanniao Pavilion (G), Fengtang Estuary (F), Shazui Wharf (S), and a fishpond (Y) in the mangrove habitat of Futian in the northeast of Shenzhen Bay (Fig.1). Each area was sampled at high (H), middle (M), and low (L) points, except Site Y, and each sampling point was taken three times as a parallel sample. In order to determine the seasonal dynamics, the samples were col- lected in spring (SP), summer (SU), autumn (AU), and win-ter (WI) at the 10 sites, GH, GM, GL, FH, FM, FL, SH, SM,SL, and Y.Due to restrictions in July 2013, the Fengtang Estuary (F) was not sampled at that time.

Fig.1 Sampling sites in the Futian Mangrove tidal flat, Shenzhen, China.

At each sampling site, three undisturbed sediments wererandomly collected as replicate samples using sampling tubes (reformed by plastic syringes) with an inner diame- ter of 2.9cm. The core sample was 11 cm in length. To exa- mine the vertical distribution of meiofauna, cores were sec- tioned into 4 layers (0–2, 2–5, 5–8 and 8–11cm) into a 250mL plastic bottle. All core samples were fixed with 5% buffered formaldehyde. In addition, surface sediment sam- ples were also collected and frozen to −20℃ at each site to determine the grain size, organic matter content, water content, chlorophyll(Chl-), and phaeophorbide (Pha).

A YSI 600XLMMulti-Parameter Water Quality Sonde (YSI Inc., USA) was used to measure the dissolved oxygen, temperature, and salinity of interstitial water at each sam- pling site.

2.2 Laboratory Analysis

Sediment samples for meiofauna were stained with 1‰ Rose Bengal for over 24h, followed by wet sieving with tap water, using 0.5mm and 0.031mm meshes to remove clay and silt. Meiofauna samples were extracted by flota- tion and centrifugation (1800rmin−1, 10min) using a col- loidal silica solution (Ludox™, Aldrich Chemical Com-pany) with a specific gravity of 1.15gcm−3(Liu, 2015),and the process was repeated thrice. Different samples werewashed into different petri dishes and meiofauna were count- ed under a stereomicroscope.

Environmental characteristics of sediments were deter- mined by oceanographic survey (State Quality and Tech- nical Supervision Administration of China, 2007). Briefly, Chl-and Pha were measured using a fluorophotometer.The sediment median grain size was measured using a Mal- vern Mastersizer 3000 particle size analyzer. The sediment organic matter content was measured using the potassium dichromate-sulfuric acid (K2Cr2O7-H2SO4) oxidization me- thod.

2.3 Statistical Analysis

The biomass of meiofauna was determined using trans- formation coefficients. Table 1 lists the coefficients from abundance to biomass of meiofauna taxa. The average dry weight of individuals in different groups of meiofauna was based on Widbom (1984), Zhang(2001) and Liu. (2005, 2018).

Table 1 Individual dry weight of different meiofauna taxa

Multivariate analyses were carried out using PRIMER 6 (Clarke and Gorley, 2006) statistical software package, including hierarchical clustering (CLUSTER), principal component analysis (PCA), and BIOENV. SPSS 22 software was used to analyze the variance and correlation of biological data and environmental factors. If the variances were not uniform, the Games-Howell test was carried out.

3 Results

3.1 Environmental Factors

The characteristics of sediments from the 10 sampling sites in the four seasons are shown in Table 2. The highest temperature was 35℃ at the SU-Y sampling site, and the lowest temperature was 13℃ at the WI-Y sampling site. The average salinity was 12.39, which was far below the normal value of 35 in oceanic seawater. Results of one-way ANOVA showed that there were highly significant sea-sonal differences in temperature (=43.322,<0.001) andsalinity (=220.133,<0.001). SPSS bivariate analysis showed a significant negative correlation between tempe- rature and salinity.

There were two types, including clay-silt and sand-silt-clay, of sediment in the sampling area. From analysis, the AU-FL station was sand-silt-clay, but the other stations wereclay-silt. The clay content ranged from 28.01% to 41.96%,and the silt content ranged from 49.00% to 68.74%. The median grain size range was 0.00497–0.00862mm. Therewere no significant differences in sediment types at each station.

In July and October of 2013, January and April of 2014, the highest values of sediment Chl-concentration was ob-served in spring (1.88μgg−1), followed by winter (1.76μgg−1), autumn (1.38μgg−1), and summer (0.53μgg−1). There were significant seasonal differences in Chl-concentra- tion between spring and summer as well as summer and winter (=5.456,=0.004). The highest values of sedi- ment Pha concentration was observed in autumn (7.73μgg−1), followed by spring (7.00μgg−1), summer (6.98μgg−1), and winter (6.62μgg−1). However, there were no signifi- cant seasonal differences in Pha concentration (=1.154,=0.342).

The average organic matter content of the sediments at the 10 sites in the four seasons of Futian Mangrove was 9.2%. The highest value was recorded at the WI-Y site (16.27%), and the lowest value was recorded at the AU-FM site (4.51%). SPSS one-way ANOVA analysis showed that there were no significant seasonal differences in orga-nic matter content (=1.062,=0.378).

Table 2 Environmental factors at the sampling sites in the Futian Mangrove area of the Shenzhen Bay tidal flat, China

()

()

StationT (℃)SMd (mm)W(%)Chl-a(μgg−1)Pha(μgg−1)OM(%)Sand(%)Silt(%)Clay(%)Sediment type SU-SL30.44.60.010.500.426.119.050.3264.3635.32YT SU-Y35.01.900.550.728.2210.31058.0441.96YT AU-FH27.812.10.010.711.257.539.364.0562.4333.52YT AU-FM27.712.70.010.441.5510.864.5121.1149.0029.89YT AU-FL27.912.20.010.451.007.775.5118.3853.6128.01STY AU-GH27.310.50.010.571.826.8110.761.9064.6533.45YT AU-GM27.910.60.010.581.127.696.650.9863.5535.47YT AU-GL27.610.60.010.731.116.7610.350.6864.5334.79YT AU-SH25.310.70.010.541.556.329.192.5266.0131.46YT AU-SM28.111.30.010.602.087.1310.033.2464.8131.95YT AU-SL27.711.30.010.670.887.8711.531.6068.7429.66YT AU-Y27.16.80.010.621.488.5613.198.9655.9035.14YT WI-FH20.020.00.010.581.705.8510.616.4361.6031.98YT WI-FM17.020.00.010.600.906.609.7412.7254.8732.41YT WI-FL16.018.00.010.591.476.728.348.2557.8733.88YT WI-GH21.018.00.010.531.206.749.508.5260.3531.14YT WI-GM23.021.00.010.621.477.159.271.2462.9335.84YT WI-GL21.021.00.010.590.786.028.182.6760.4936.85YT WI-SH22.020.00.010.501.587.808.380.4164.0035.59YT WI-SM21.019.00.010.513.374.379.471.6166.5831.81YT WI-SL20.020.00.010.592.996.0310.701.4566.5831.97YT WI-Y13.019.00.010.632.098.9416.275.4258.8435.74YT

Notes: T,temperature; S,salinity; Md,median grain size; W,water content; Chl-,chlorophyllcontent; Pha,phaeophorbide content; OM,organic matter content; YT,clay-silt; STY, sand-silt-clay.

Principal component analysis was performed using stan- dardized data of environmental factors. The result showed that the PC1 and PC2 axis accounted for 55.9% of environ- mental variability. On the PC1 axis, there was an increas- ing trend for median grain size, salinity, and Chl-from left to right. On the PC2 axis, Pha increased gradually, while the silt-clay content, water content, and organic matter con-tent gradually decreased from top to bottom (Fig.2).

Fig.2 PCA of environmental factors for the sampling sta- tions in the Futian Mangrove tidal flat, Shenzhen, China.

3.2 Meiofauna

3.2.1 Taxa composition and spatial-temporal distribution of meiofaunal abundance

A total of 14 meiofaunal taxa were identified in the four sampling seasons, including Nematoda, Copepoda, Poly- chaeta, Oligochaeta, Isopoda, Gammarid, Halacaroidea, Nauplia, Ostracoda, Insecta, Bivalvia, Thermosbaenacea,Turbellaria, Tanaidacea. There were also undetermined taxathat fell into others (Table 3). Table 4 shows the average abundance and biomass of main meiofaunal taxa in the Futian Mangrove tidal flat, Shenzhen, China. The results showed that the largest number of taxa 12 was recorded in spring; followed by 8 taxa recorded in summer and autumn;and 6 taxa recorded in winter. Nematodes were the most dominant group, accounting for 97.54%, 99.29%, 96.14%, and 97.26% of the total abundance of meiofauna in the four seasons, respectively.

In terms of seasonal variation, the average abundance of meiofauna was the highest in summer ((5136.35±623.38)ind(10cm)−2), followed by those in spring ((2714.04±869.21)ind(10cm)−2), winter ((581.55±185.48)ind(10cm)−2),and autumn ((488.35±71.29)ind(10cm)−2). In terms of spa-tial distribution, the highest meiofaunal abundance was re- corded at site GH in summer (10828.03ind(10cm)−2), and the lowest was recorded at site FM in winter (30.80ind(10cm)−2).

In terms of seasonal variation, the average biomass of meiofauna was the highest in summer ((2423.10±419.94)μgdwt(10cm)−2), followed by those in spring ((1835.87±312.10)μgdwt(10cm)−2), winter (433.09±93.76μgdwt(10cm)−2), and autumn ((421.56±156.70)μgdwt(10cm)−2). In terms of spatial distribution, the highest value of meio- faunal biomass was recorded at site SH in spring (5591.16μgdwt(10cm)−2) and the lowest value was recorded at site FL in winter (15.55μgdwt(10cm)−2). In terms of biomass, nematodes were the most dominant group, followed by polychaetes.

Table 3a Abundance of each meiofaunal taxon in spring and summer in the Futian Mangrove area of the Shenzhen Bay tidal flat

Table 3b Abundance of each meiofaunal taxon in autumn and winter in the Futian Mangrove area of the Shenzhen Bay tidal flat

Table 4 Average abundance and biomass of main meiofaunal taxa in the Futian Mangrove tidal flat, Shenzhen, China

3.2.2 CLUSTER analysis

Results of the CLUSTER analysis (Fig.3) based on the abundance of meiofauna at all the sampling sites in the four seasons showed that the meiofaunal assemblages could be divided into four groups. Group 1 included the sites in au- tumn (GM, GL) and winter (GM, GL, FM, FL). Group 2 included only a site in summer (Y). Group 3 included the sites in summer (GM, GL), autumn (GH, FH, FM, FL, SH, SM, SL, Y), and winter (SH, SM, SL, FH, GH, Y). Group 4 included the sites in spring (GH, GM, GL, FH, FM, FL, SH, SM, SL, Y) and summer (GH, SH, SM, SL). The re- sults showed that the community structure in spring was similar to that in summer, and the community structure in autumn was similar to that in winter. The community struc- tures of the mid-tidal and the low-tidal areas are similar.

Fig.3 CLUSTER analysis based on meiofaunal abundances in the Futian Mangrove tidal flat, Shenzhen, China.

3.3 Vertical Distribution of Meiofauna

The vertical distribution of meiofauna (Fig.4) showed that the proportions of meiofauna distributed at 0–2, 2–5, 5–8, and 8–11cm were 61.36%, 28.20%, 7.22%, and 3.67%,respectively. Meiofauna were mainly distributed in the up-per and middle sediment layers (0–5cm), accounting for 89.56% of the total meiofauna, while the remaining 10.44%of meiofauna were distributed in 5–11cm. The proportion of nematodes distributed in 0–2, 2–5, 5–8, and 8–11cm was 61.36%, 28.24%, 7.18%, and 3.67%, respectively. It showed a similar trend to the distribution of meiofauna.

Fig.4 Vertical distribution of the abundance of total meiofauna and nematodes.

3.4 Relationship Between Meiofauna and Environmental Factors

The results of the correlation analysis showed that me- iofaunal and nematode abundance, and meiofaunal biomasswere significantly negatively correlated to salinity. This in-dicated that salinity was the most important environmen- tal factor determining meiofaunal distribution.

BIOENV analysis showed that meiofauna community was affected by a variety of environmental factors (Table 5). This explains why the best combination of environmen- tal factors was temperature and salinity, and the correla- tion coefficient was 0.221. Temperature showed the high- est influence among the environmental factors considered, with a correlation coefficient of 0.187.

Table 5 Results of BIOENV analysis between meiofaunal assemblage and environmental variables

Notes: T,temperature; S,salinity; Md,median grain size; W,water content; Chl-,chlorophyllcontent.

4 Discussion

4.1 Comparison with Other Mangrove Regions

Mangroves are rich in tannic acid and organic matter, hence, there are significant differences between meiofau- na in mangrove and non-mangrove habitats (Gee and So- merfield, 1997; Sahoo, 2013). Benthic biologists world- wide have carried out several studies on meiofauna in dif- ferent mangrove areas. In the present study, there weredif- ferences in the assemblages and abundance of meiofauna in different mangrove sites examined (Table 6).

In the present study, a total of 14 meiofaunal taxa were identified during the four sampling seasons. A total of 7meiofaunal taxa were found and the abundance of meio-fauna was (1572±389)ind(10cm)−2in the mangrove area in Futian, Shenzhen Bay by Tan(2017). In this study, the sampling sediment depth was 9cm, and the upper and lower limits of mesh sizes were 0.5mm and 0.042mm, respectively. Zhu(2020) studied the meiofauna in the mangrove area of Futian, Shenzhen Bay in winter with5cm sampling sediment depth. Only 5 meiofaunal taxa, in- cluding nematodes, copepods, polychaetes, oligochaetes and unidentified groups, were found and the meiofaunal abundance was (490.73±465.09)ind(10cm)−2. Therefore, differences insampling seasons, sediment depth (11cm in the present study) and the upper and lower limits of mesh sizes (0.5mm/0.031mm in the present study) may be re- sponsible for the higher taxa number recorded in the pre- sent study compared with the abovementioned studies.

Although the numbers of taxa reported in different stud- ies vary largely between mangrove habitats, nematodes constitute a large percentage of taxa in most reports. Con- sistent with most studies on mangrove habitats, nematodes accounted for 98.35% in the present study. On the con- trary, nematode population was relatively low in the man- grove habitat on the west coast of Zanzibar (Ólafsson,2000),which was because foraminifera constituted the do- minant group in that habitat.

Alongi (1987) reported that meiofauna abundance on sandy beaches can reach 1000–8000ind(10cm)−2, and can be lower than 500ind(10cm)−2in mangrove areas. How- ever, most studies have shown that meiofauna abundance in mangrove areas is higher than 500ind(10cm)−2. The meiofauna abundance in the present study was much high- er than 500ind(10cm)−2, indicating that the Futian man- grove habitat had high productivity. The higher meiofau- na abundance in the present study may also be as a result of the differences in sampling depth and mesh size used in this study compared to previous studies.

Table 6 Comparison of meiofauna studies in different mangrove areas

Notes: For meiofaunal study in Sethukuda Mangrove area, foraminifera were included and the percentages were 52%–97% while other studies only included metazoan meiofauna.

4.2 Relationships Between Meiofauna and Environmental Factors

Li. (2012) studied the distribution and seasonal va-riation of meiofauna in the intertidal zone of Qingdao san- dy beach. Studies have shown that there are significant sea- sonal changes in the vertical distribution of meiofauna. In winter, due to the low temperature, meiofauna migrates fromthe surface sediment layer to deeper sediment layer.In sum-mer, due to the increased temperature and increased avail- ability of food in the surface sediment layer, they migrate back to the surface. The Futian mangrove habitat is located at lower latitudes and has higher temperatures throughout the year. Unlike the vertical distribution of meiofauna ob- served in the intertidal zone of Qingdao sandy beach (Li, 2012), there were no significant seasonal variations in the vertical distribution of meiofauna in mangroves. Se- veral factors, including biotic and abiotic factors, affect the vertical distribution of meiofauna. Biotic factors, such as food (Rysgaard, 1994) and human activities, and abio- tic factors, such as organic matter, water content, tempera-ture, and salinity, affect the vertical distribution of meio- fauna (Warwick and Buchanan, 1970; Heip, 1985). Additionally, fauna distribution differs with intertidal zones, and is also affected by seasonal changes. However, most research results indicate that meiofauna are mainly distri- buted in surface sediments (Alongi, 1986).

The reason for the significant seasonal changes in the taxa composition and abundance of meiofauna in the Futian mangroves may be due to the effects of seasonal changes of environmental variables, such as interstitial wa-ter temperature and salinity. In the present study, the ma- jor influencing factors are temperature and salinity based on BIOENV analysis. Moreover, salinity and abundance are significantly negatively correlated based on Correlation ana-lysis. According to the Shenzhen Meteorological Bureau data, rainfall in Shenzhen is mainly in spring (March toMay), summer (June to August), and early autumn (Septem- ber). SPSS bivariate analyses show that temperature and precipitation are significantly positively correlated;sali-nity and precipitation are significantly negatively corre-lated; and precipitation is positively correlated with meio- faunal abundance and biomass. However, few studies have shown that in the northern intertidal zone or shallow seahabitats, meiofaunal abundance and salinity are significant- ly related(Zhang, 2001; Li, 2012). This can be attributed to the lesser rainfall and larger temperature dif- ference in the north, which results in more obvious tem-perature effects. However, in the south, during the rainyseason, large amount of fresh water flushes the intertidal zone, resulting in decreased salinity. Therefore, salinity is an important seasonal environmental variable in the pre-sent study.

Results of one-way ANOVA showed no significant dif- ferences in meiofaunal abundance between autumn and win- ter; however, there were significant differences betweenother seasons. This study is consistent with the conclusions of Palmer and Coull (1980). Cai (2000) reported that nema- tode density was highest in spring, followed by those in win- ter, summer, and lowest in autumn. This shows that tem- perature is an important seasonal environmental variable; however, the changes in meiofaunal abundance cannot be attributed solely to its effect. Zou(2020) reported that sediment type was the most important factor for the dif- ferences of meiofaunal abundance in Dongwan mangrovewetland of Fangchenggang, Guangxi, China. Hua(2020) also found that the differences in nematode abun- dance were mainly due to the seasonal dynamic changes of sedimentary environmental factors and the seasonal dyna- mic changes of sediment type.

Seawater has a strong transportation capacity; hence, pe-riodic scouring will change the clay content, silt content,and sand content of sediments. Meiofauna living in the in-tertidal sediments of mangroves are affected not onlyby changes in environmental factors, but also by the activities of other animals and humans (Ingole and Parulekar, 1998). Therefore, the reasons for the differences in the structure and abundance of meiofauna communities in different man-grove areas are complex and diverse. The effect of sea-sonal variables, such as temperature and salinity, on the dis-tribution of meiofauna needs further study.

The present study provides basic information for sea- sonal distribution of meiofauna in the Futian Mangrove Re- serve. However, in order to reflect the annual fluctuation of meiofauna, continuous studies of meiofauna should be carried out. Additionally, meiofaunal distribution in various mangrove habitats should also be studied to reveal the ge- neral patterns. Moreover, species composition of marine nematodes, which are the most dominant group generally in meiofauna, should also be studied to understand the more precise species diversity in mangrove ecosystem.

Acknowledgements

This study was jointly supported by the Fundamental Research Funds for the Central Universities (Nos. 201964024 and 201362018) and the Biodiversity Investigation, Observation and Assessment Program (2019–2023) of Mi- nistry of Ecology and Environment of China. We appreciate Dr. Qinghe Liu and Mr. Deming Huang for their help in the field sampling. We are also very grateful to Dr. Zihao Yuan, Mr. Shan Cai and Ms. Xiaomeng Liu for their help in the laboratory analysis.

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