Turkish Journal of Zoology Turk J Zool (2019) 43: 379-387 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1812-9

Structural characteristics of the soil fauna community in beach wetlands of the region

1 1 1 2 3, 1 4 Ping LU , Nianhua DAI , Guohua ZHANG , Meiwen ZHANG , Derong XU *, Zhuorong LIU , Zhiqiang HUANG  1 Institute of Biological Resources, Academy of Sciences, , P.R. 2 Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, P.R. China 3 Institute of Translational Medicine, Nanchang University, Nanchang, P.R. China 4 Jiangxi Provincial Management Bureau of Wild Fauna and Flora Conservation, Nanchang, P.R. China

Received: 04.12.2018 Accepted/Published Online: 30.05.2019 Final Version: 01.07.2019

Abstract: We examined the soil fauna community composition and structure of Poyang Lake beach wetlands using the modified Tullgren and Baermann methods during September and December 2015. A total of 3755 individuals were obtained from 2 samplings, which were found to belong to 7 classes, 8 orders, 3 suborders, and 17 families. Among these, the Oribatida, Prostigmata, Nematoda, and Onychiuridae were dominant. The functional groups of soil animals included omnivores, saprozoics, predators, and phytophages. Analysis results of the soil fauna composition and diversity showed that the soil animals were mainly concentrated at the 0–10 cm depth, presenting as a significant surface convergence phenomenon. The numbers of individual soil animals differed significantly between sampling sites (P < 0.05), with the beach wetland in Lianhu Township having the highest numbers of individuals and groups. The effect of water level variability on numbers of soil animals was not significant (P > 0.05). Habitat type and sampling time both had highly significant effects on diversity and evenness (P < 0.01), and significant effects on species richness (P < 0.05). During water level changes in Poyang Lake, the individual number, group number, and diversity of the soil animals were closely linked to the sampling site. These results provide basic data for further studies on soil fauna ecology in Poyang Lake beach wetlands.

Key words: Community structure, distribution pattern, functional group, Poyang Lake region

1. Introduction processes of degradation and restoration (Liu et al., 2014), Wetland ecosystems have characteristics of both terrestrial acting as indicators for the maintenance of biodiversity and aquatic ecosystems. Their complex structure enables and ecological balance (Zhang et al., 2013; Chen et al., them to provide a variety of habitats for the growth of 2014). animals and plants (Keddy, 2010). Poyang Lake is the Previously, research on the Poyang Lake wetlands largest river-linking lake in the River Basin and focused mostly on vegetation (Wang et al., 2014; Feng et the largest freshwater lake in China (Wang et al., 2016). al., 2016) and birds (Wu et al., 2014; Yang et al., 2016); As an important freshwater resource pool in China, it is there are only a few reports on soil fauna. The objectives of an ecological conservation library of global significance this study were to investigate the composition, abundance, (Hui et al., 2008). The Poyang Lake wetlands change with distribution, and diversity of soil fauna in typical wetlands seasonal variations in flood levels, and various types of of Poyang Lake; to analyze the structure and diversity habitats form during the process (Liu et al., 2011). These of various habitats; and to provide basic data for soil have developed a variety of wetland soils with abundant biodiversity for further studies in the lake. biodiversity (Liu et al., 2011; Wu et al., 2012; Zhang et al., 2012; Liang et al., 2015; Yang et al., 2015). 2. Materials and methods Soil animals are an important component of wetland 2.1. Overview of the research area ecosystems and are a food source for migratory birds (Wu Poyang Lake is China’s largest freshwater lake, located in et al., 2009). They also participate in the material cycles northern Jiangxi province on the south bank of the middle of wetland ecosystems (Keddy, 2010). Their dynamics and lower Yangtze River (28°24′N to 29°46′N, 115°49′E to can reflect changes in ecological functions during the 116°46′E) in a classic subtropical monsoon climate zone. * Correspondence: [email protected] 379

This work is licensed under a Creative Commons Attribution 4.0 International License. LU et al. / Turk J Zool

Poyang Lake varies in size dramatically with seasonal water suspension (1:2.5 v:v) was measured with a digital rainfall: during the summer April–September wet season, pH meter, and soil organic carbon (SOC) content was its largest river-linking surface area is 4078 km2, while in determined via dichromate oxidation. Additionally, the the winter dry season from October to March, the average total N (TN) content was measured with an ultraviolet surface area is 1290 km2 (Shao et al., 2014). Hot, humid, spectrophotometer following Kjeldahl digestion (Liu at al., southerly winds prevail during summer and dry, cold, 1996). northerly winds prevail in winter. The average annual 2.4. Data analysis temperature is 17.6 °C, ranging from a mean of 5.1 °C in Group number level is expressed as the relative abundance January to 29.5 °C in July. About 1450–1550 mm of rain of soil animal groups (Lu et al., 2013). A group whose falls annually, mostly between April and June (Dong et number of individual animals accounted for more than al., 2014). During winter, the water subsides and beaches 10% of the total catch was defined as a dominant group, emerge, forming a large number of shallow depressions those accounting for 1%–10% were defined as common 2 and strands. This area of 2698 km accounts for 82% of groups, those consisting of 0.1%–1% were defined as rare the total normal water level area of the lake (Wang et al., groups, and those below 0.1% of the total were defined 2011; Dong et al., 2014); it is an important habitat for as very rare groups. Here, we classified dominant and global winter migratory birds and plays a critical role in common groups as the main groups and rare and very rare maintaining biodiversity (Zhao et al., 2007). groups as other groups. In this study, we selected beaches with the same For community diversity, we used the Shannon–Wiener elevation and habitat but different soil properties at diversity index (H’), Pielou index (Js), and Margalef index Poyang Lake and the grass shoals located at the Henghu (D) (Ma, 1994) as follows: Reclamation Farm in the Xinjian of Nanchang city in Jiangxi province (HH); Jiangxi Poyang Lake Nanji (1) Wetland National Natural Reserve in Nanji township (NJ); Js = Hʹ/LnS (2) and Lianhu township in city in Jiangxi province D = (S - 1)/Ln(S) (3) (LH) (Figure 1; Tables 1 and 2). The three beach sites have where Pi is the ratio of the number of individuals to the similar flood regimes. The soil types are all meadow soil. total number of individuals in the community for the The main dominant plants in the beaches are sedges (Carex number of i species, S is the number of groups, and N is spp.), reeds (Phragmites australis), and triarrhena grass the number of individuals observed. (Triarrhena lutarioriparia). The beaches were flooded in The differences in soil fauna between different wetland summer, but in winter the waters subsided and the beaches communities were analyzed using one-way ANOVA, and were exposed. Soil fauna surveys were conducted during each taxon was analyzed separately. Tukey’s LSD test was the dry season in September and December 2015, when used to compare the significance of differences between the corresponding lake water levels at Xingzi were 13.73 m soil fauna and groups of different wetland communities. and 13.07 m, respectively. All statistical analyses were conducted using Excel 2010, 2.2. Soil fauna sampling and identification SPPSS 19.0, and CANOCA 4.5 software. Fixed sampling plots of 20 × 20 m were marked on the lake beaches or shoals, with three sampling quadrats evenly 3. Results distributed within each sampling plot. Two depth layers 3.1. Composition and characteristics of soil animals in were defined in each quadrat as 0–10 cm and 10–20 cm. Poyang Lake beach wetlands In the first quadrat of 20 × 20 cm, fauna was removed During the study period, 3755 soil animals including manually. In the second quadrat of 10 × 10 cm, fauna was 1 unidentifiable specimen were collected, belonging to removed using a modified Tullgren approach. In the third 7 classes, 8 orders, 3 suborders, and 17 families (Table quadrat of 10 × 10 cm, a 100-mL foil sampler was used 3). A total of 24 species of soil fauna were identified in to remove fauna as per Baermann’s method. Collected soil the Poyang Lake beach wetlands, among which the 4 animals were stored in 70%–75% ethanol. dominant types belonged to the order Oribatida, the Soil animal specimens were all identified to family level suborder Prostigmata, the phylum Nematoda, and the except for members of Nematoda, Araneida, and Acarina family Onychiuridae. Together, these accounted for (Yin, 1998). Functional groups were categorized based on 90.74% of the total individuals. A common group was the their feeding habits and their roles in food decomposition order Mesostigmata, accounting for 6.15% of individuals. (Xu et al., 2013). Rare and very rare species accounted for 3.11% of the total 2.3. Soil property analysis number. Soil moisture was determined by oven-drying fresh The four functional groupings of soil animals included soil at 105 °C to a constant weight. Soil pH of a soil/ omnivores, saprozoics, predators, and phytophages.

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Figure 1. Schematic diagram of soil fauna sampling locations in Poyang Lake beach wetlands. 1: Henghu Reclamation Farm, , Nanchang city (HH); 2: Nanji township, Xinjian district, Nanchang city (Nanji Wetland National Natural Reserve) (NJ); 3: Lianhu township, , Shangrao city (LH).

Among these, omnivores and saprozoics were the most 3.2. Distribution characteristics of soil fauna numerous, accounting for 30.77% of the total number of 3.2.1. Horizontal distribution groups, followed by phytophagous soil animals (20.78%) The number of individuals and number of groups in the and predators (15.38%). wetland of Lianhu Township (LH) were highest, and the

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Table 1. Geographic characteristics of the sampled plots.

Elevation No. Place Location Dominant plant species (m) Henghu Farm, 28°59′27″N, 1 HH 16 Xinjian, Nanchang 116°09′40″E Sedge (Carex spp.) Triarrhena Nanji, Xinjian, 28°57′06″N, 2 NJ 16 (Triarrhena lutarioriparia) Nanchang 116°21′23″E Reed (Phragmites australis) Lianhu,Poyang County, 28°56′15″N, 3 LH 16 Shangrao 116°33′32″E

Table 2. Selected soil properties of the sampled plots.

Soil layer Moisture SOCb TN Site Month pH C/N (cm) (%) (g/kg) (g/kg) HH 9 0–10 5.68 32.38 ± 0.05a 15.30 ± 1.22 1.56 ± 0.01 9.79 ± 0.73 10–20 6.49 31.93 ± 0.06 11.64 ± 1.91 1.18 ± 0.20 9.88 ± 0.23 12 0–10 4.86 30.79 ± 0.02 23.28 ± 2.25 2.12 ± 0.33 11.07 ± 0.76 10–20 5.12 27.84 ± 0.01 13.44 ± 1.76 1.34 ± 0.22 10.09 ± 0.37 NJ 9 0–10 6.37 19.92 ± 0.02 6.00 ± 2.43 0.67 ± 0.30 9.15 ± 1.69 10–20 5.33 18.96 ± 0.02 3.66 ± 0.21 0.46 ± 0.01 8.03 ± 0.59 12 0–10 4.98 24.50 ± 0.07 7.48 ± 1.56 0.71 ± 0.21 10.73 ± 1.74 10–20 5.16 26.26 ± 0.09 8.01 ± 2.65 0.80 ± 0.19 9.88 ± 2.03 LH 9 0–10 7.61 24.06 ± 0.04 14.37 ± 11.19 1.48 ± 0.95 9.22 ± 1.27 10–20 7.71 25.61 ± 0.02 9.90 ± 5.40 1.07 ± 0.40 8.94 ± 1.61 12 0–10 4.81 33.81 ± 0.03 22.38 ± 8.94 1.92 ± 0.43 11.36 ± 2.11 10–20 4.75 30.32 ± 0.02 13.92 ± 0.98 1.43 ± 0.04 9.74 ± 0.97

a Values are means ± standard error for the sampling plots (n = 3). b SOC, TN, and C/N refer to soil organic carbon, soil total nitrogen, and the ratio of soil organic carbon to soil total nitrogen, respectively. number of individuals and the number of groups of soil (Figure 3). However, the numbers of individual soil animals fauna in Nanji Township (NJ) were lowest (Figure 2a). and the numbers of groups in each layer were different The number of individual soil animals was higher in at various beach wetlands. Among them, the number of December and the number of soil fauna groups was higher groups and number of individuals in the 0–10 cm soil layer in September (Figure 2b). Variance analysis showed that were both ranked as LH > HH > NJ, and only LH and NJ numbers of soil animals differed significantly between sites were significantly different (P < 0.05). The number of soil (F = 4.195, P < 0.05), while the number of groups was not animals in the 10–20 cm soil layer could be ranked as LH significantly different (P > 0.05). The number of individual > HH > NJ (P > 0.05), and the number of groups could be soil animals in the NJ beach wetland was significantly lower ranked as HH > NJ > LH (P > 0.05). than in LH and HH (P < 0.05). There were no significant 3.2.3. Functional group composition differences in the number of individuals and number of Differences among the omnivorous, phytophagous, groups between September and December (P > 0.05). predaceous, and saprophagous groups are shown in 3.2.2. Vertical distribution Table 4. The number of individuals in the omnivorous There were significant differences in the distributions of group was significantly different between sample sites soil fauna and the numbers of groups in different soil cross- (F = 9.296, P = 0.01), and there was no difference in the sections across the three wetland sites (P < 0.05), although number of individuals in the other three groups (P > all showed significant surface convergence phenomena 0.05). Additionally, there was no significant difference

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Table 3. Statistics of soil fauna sampled from the beach wetlands of Poyang Lake in 2015.

No. Name LH HH NJ Total Percentage Deg. Gui. 1 Nematoda 267 827 55 1149 30.60 *** O 2 Mesostigmata 117 58 56 231 6.15 ** S 3 Acarina Prostigmata 388 236 113 737 19.63 *** S 4 Oribatida 717 248 107 1072 28.55 *** S 5 Araneae Pholcidae 1 2 0 3 0.08 Pr 6 Tetramerocerata Pauropodidae 0 2 1 3 0.08 S 7 Onychiuridae 317 98 34 449 11.96 *** O 8 Entomobryidae 0 1 0 1 0.03 O 9 Collembola Sminthuridae 2 0 1 3 0.08 O 10 Neanuridae 3 6 3 12 0.32 O 11 Isotomidae 4 0 0 4 0.11 O 12 Psocoptera Liposcelididae 0 1 1 2 0.05 Ph 13 Carabidae 0 1 0 1 0.03 Pr 14 Staphylinidae 0 3 1 4 0.11 S Coleoptera 15 Tenebrionidae 1 0 0 1 0.03 Ph 16 Nitidulidae 2 0 0 2 0.05 S 17 Ptilodactylidae 4 3 3 10 0.27 Ph 18 Coleoptera larvae Staphylinidae 4 3 11 18 0.48 Ph 19 Nitidulidae 17 1 0 18 0.48 S 20 Dolichopodidae 2 5 3 10 0.27 Pr 21 Clusiidae 1 0 0 1 0.03 S Diptera larvae 22 Ceratopogouidae 9 0 0 9 0.24 O 23 Chironomidae 4 9 1 14 0.37 O 24 Unknown 0 1 0 1 0.03 Total Individuals 1860 1505 390 3755 Groups 18 18 14 24

Deg.: Degree of dominancy, with *** indicating a dominant group and ** indicating a common group. Gui.: Guild, with O indicating omnivores, S indicating saprozoics, Pr indicating predators, and Ph indicating phytophages. in the number of all functional groups across the three 0.05). Among them, the greatest difference in diversity was wetland sites (P > 0.05). The number of individuals in the between the HH and LH sites; additionally, the difference saprophagous group was significantly different between in evenness between these sites was very significant (P September and December (F = 5.932, P = 0.020), but there < 0.01). There was no significant difference in soil fauna were no significant differences in the other 3 groups (P > diversity between September and December (P > 0.05). 0.05). However, the difference in Pielou index was very significant 3.3. The diversity of soil animals in Poyang Lake beach (P < 0.01) (Figure 4b). Two-factor analysis of variance wetlands showed that site and sampling time had significant effects Overall, among the Poyang Lake wetlands, the diversity on the diversity and evenness of soil fauna (P < 0.01). index and Pielou index of soil fauna at NJ were higher The soil fauna richness of the Poyang Lake wetlands than those at LH and HH, which indicated that the soil could be ranked as NJ > LH > HH (Figure 5a). There was fauna of NJ was abundant in composition and more no significant difference in soil fauna richness between evenly distributed (Figure 4a). The differences in soil fauna different sites (P > 0.05). The differences in soil fauna diversity and evenness at various sites were significant (P < richness between September and December was highly

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Individuals Groups a 800 16 1000 Individuals Groups 16 b 14 14 800 600 12 12

s 10 l up s

o s r

l 10

600 G idu a 400 8 up s idu a

8 o r ndi v I

G 6 ndi v I 400 6 200 4 4 200 2 2 0 0 0 0 9 12 9 12 9 12 LH HH NJ LH HH NJ Sample site Sample site/Month Figure 2. Numbers of soil fauna individuals and groups at different sampling sites in Poyang Lake wetlands.

800 Individuals Groups 14 groups. Our results indicated that these dominant groups play an important role in the formation and accumulation 700 12 of soil nutrients. The dominant soil fauna species in 600 10 Dongting Lake Wetland (Han et al., 2007) and Taihu s

l 500

Lake Wetland (Li et al., 2013) included Nematoda and 8 up s idu a

400 o Acarina, similar to the results of this study. This indicates r G

ndi v 6 some homology in the dominant species of animals within I 300 similar soil types. In this study, there were differences in 4 200 physical and chemical soil properties among the three 100 2 sites (Table 2), and the fauna differed significantly between them (P < 0.05). However, the number of functional groups 0 0 I II I II I II was stable and was not significantly affected (P > 0.05). We LH HH NJ believe that the functional groups were stable in the same habitat, but the soil fauna community was affected by soil Sampling site/Soil lay er properties (Scheunemann et al., 2010; Sylvain et al., 2014; Figure 3. Distribution of soil fauna in the 0–20 cm soil layer at Yin et al., 2015; Korboulewsky et al., 2016). different sampling sites in the Poyang Lake region. The dominance of the Acarina in the wetland environment and the ratio of Acari to Collembola (A/C > 1) are characteristics of wetlands (Wu et al., 2008). In this significant (P < 0.01) (Figure 5b). Two-factor analysis of study, the A/C values of the Poyang Lake beach wetlands in variance showed that habitat type and sampling time had Lianhu Township (LH), Nanji Township (NJ), and Henghu significant effect on soil fauna richness (P < 0.05). Farm (HH) were 3.93, 7.26, and 5.16, respectively. In this study, the soil animal functional groups in typical 4. Discussion Poyang Lake beach wetlands were mainly saprozoics and Physical and chemical properties of soil, such as omnivores, followed by predatory and phytophagous temperature, water content, pH, organic carbon content, soil animals. The functional groups in typical wetlands total nitrogen content, and vegetation coverage constitute of Sanjiang Plain soil mainly consisted of saprozoics, the soil habitat. These factors affect the composition of the predators, and phytophagous animals, with the saprozoics soil fauna community and can be responsible for uneven occurring in the greatest number, followed by predators distribution (Murray et al., 2006; Lu et al., 2013; Zhu and and phytophagous soil animals (Wu et al., 2008). Similar Zhu, 2015). In this study, the numbers of individuals in results could be seen in Poyang Lake wetlands. Our results the orders Oribatida and Prostigmata of Acarina, the showed that saprozoics and omnivores were dominant in Nematoda, and the family Onychiuridae of Collembola Poyang Lake wetlands, similar to the results of a study of were high, with these animals constituting the dominant Sanjiang Plain wetlands (Wu et al., 2008).

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Table 4. The number of individuals and functional groups across the different sample sites.

Functional groups LH HH NJ Omnivorous 202.00 ± 104.73 a 313.67 ± 3.79 a 28.00 ± 13.00 b Number of Phytophagous 1.67 ± 2.89 NS 1.33 ± 1.15 1.33 ± 1.53 individuals Predaceous 1.00 ± 1.00 NS 2.67 ± 2.08 1.00 ± 1.00 Saprophagous 415.33 ± 189.51 a 183.67 ± 49.57 ab 95.67 ± 61.52 b Omnivorous 4.67 ± 1.53 NS 4.00 ± 1.00 3.67 ± 0.58 Number of Phytophagous 1.67 ± 1.15 NS 1.33 ± 1.53 1.33 ± 0.58 groups Predaceous 1.00 ± 1.00 NS 1.33 ± 0.58 0.67 ± 0.58 Saprophagous 4.67 ± 1.53 NS 4.00 ± 0.00 3.67 ± 1.15

Values are means ± standard error for the sampling site (n = 3). Means followed by different letters are significantly different by multiple comparisons in rows, while NS indicates no significant difference (LSD test or Tamhane’s T2 test), α = 0.05.

a b Shannon-Weiner index (H') 2 Shannon-Weiner index (H') 2 Pielou index（Js） Pielou index（Js） 1.6 1.6

1.2 1.2

0.8 0.8 0.4 0.4 0 0 9 12 9 12 9 12 LH HH NJ LH HH NJ

Sample site Sample site/ Month Figure 4. Shannon–Weiner index (H’) and Pielou index (Js) of soil fauna community at different sampling sites in the Poyang Lake region.

The soil animals showed surface convergence (Xu et al., 2013). September is the end of the Poyang Lake distribution, indicating that the quality of the wetland wet season, when the water level begins to subside, while environment has not been significantly disturbed (Liu et al., December falls in the dry season when water levels are 2014). Notably, the number of soil animals and the number low. The number of soil animals in December (2444) was of groups at Lianhu Township (LH) were the highest. This higher than that in September (1311), and the number result indicates that the soil environment has not been of fauna groups in September (20) was higher than that significantly disturbed in the wetlands of Lianhu Township. in December (13). This was likely because the water In the sampling, we found that the wetlands of Nanji level began to decline in September, when the soil fauna Township (NJ), which belong to Nanji Wetland National community had not yet been restored and the number Natural Reserve, have been significantly disturbed by winter of individuals was small but the number of groups was birds and many birdwatchers, and Henghu Reclamation relatively higher. In December, the soil fauna community Farm (HH) has been significantly disturbed by some human became stable, and the number of individuals increased activities, such as grazing. The number of individuals and and the number of groups decreased. groups of soil animals being highest at LH may also be The diversity index is an important indicator of correlated with the soil properties; this needs further study. the functional organization of flora and fauna. A large Variations in the number of individuals and groups of biodiversity index indicates that the community is soil fauna can also be related to seasonal climatic factors abundant in species, complex in structure, and even in

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b 2.5 a 2.5

） 2

（ D ） 2 x D

e 1.5 （ x in d 1.5 f e

l 1 ind e

a f r g e

l 1 a a

M 0.5 r g a

M 0.5 0 0 9 12 9 12 9 12 LH HH NJ LH HH NJ Sample site Sample site/ Month

Figure 5. Margalef index (D) of soil fauna community at different sampling sites. distribution of the population (Zhang et al., 2014). The beach wetland soil fauna are mainly concentrated in the results of this study showed that the diversity, evenness, 0–10 cm layer, showing a significant surface convergence and richness of beach wetland soil fauna communities at phenomenon. The numbers of individuals and groups of the three Poyang Lake sampling sites were significantly soil animals in the beach wetlands of Lianhu Township different (P < 0.05). While the diversity and evenness (LH) were the highest, which indicated that the soil of soil fauna were not significantly different between environment of the beach wetlands of LH had positive sampling months (P > 0.05), the differences in evenness effects on the soil fauna community. The effects of site and were significant (P < 0.05), indicating that different sites in sampling date on the diversity and evenness of soil fauna the Poyang Lake region had significant effects on soil fauna were both highly significant, and also had significant diversity, while the date of sampling only significantly effects on soil fauna richness. The water level variation of impacted soil fauna evenness. Previous studies have Poyang Lake had no significant impact on the numbers shown that soil fauna composition is also related to the of individuals and groups of soil animals. These results complexity of soil ecosystems and is strongly influenced provide basic data for further studies on soil fauna ecology by soil environmental factors (Lu et al., 2013; Yin et al., in Poyang Lake beach wetlands. 2015). This study only explored the relationship between the structure and diversity of soil fauna at different Acknowledgments locations of Poyang Lake beach wetlands; the reasons for This study was financially supported by the National the changes should be further studied in combination with Natural Science Foundation of China (41561056), the Sci- soil environmental factors. Tech Support Plan of Jiangxi Province (20151BBG70065), In conclusion, the structure and diversity of soil and the Jiangxi Academy of Sciences (2014-YYB-05; 2014- fauna differ geographically. In this study, Poyang Lake XTPH1-05).

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