Distribution and diversity patterns of soil fauna in different salinization habitats of Songnen Grasslands, China

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Applied Field Research Article

Distribution and diversity patterns of soil fauna in different salinization habitats of Songnen Grasslands, China ⁎

Xiuqin Yina,b, , Chen Maa, Hongshi Hec, Zhenhai Wanga, Xiaoqiang Lia, Guanqiang Fua, Jing Liua, Yanmiao Zhenga a b c

School of Geographical Sciences, Northeast Normal University, Changchun, 130024, PR China Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, Changchun, 130024, PR China School of Natural Resources, University of Missouri, Columbia, MO 65211, USA

A R T I C L E I N F O

A B S T R A C T

Keywords: Soil fauna Diversity and distribution Salinization habitat Songnen Grasslands China

The soil fauna communities were studied in the Songnen Grassland, which is located at the easternmost Eurasian steppe of northeast China. We sampled sites from May to October with different alkaline contents to investigate the salinization process on soil fauna. We found that the dominant groups were Prostigmata, Oribatida, and Gamasina mites and the collembolan families Isotomidae and Entomobryidae. Results showed that the composition of the soil fauna communities differed significantly among the habitats with different salinity. Number and density of taxa were lower in communities with high salinity. The highest number of taxa (66) was found on the Artemisia anethifolia sites, the lowest number (47) on the Alkali patches. The Shannon-Wiener index was the lowest on the Alkali patches, whereas the Simpson-dominance index was the highest in these habitats. The number and density of taxa changed during the seasons. The soil fauna tended to gather on soil’s surface. According to the Redundancy analysis, the soil organic matter positively affected the density of the soil fauna and soil fauna decreased with increasing degree of salinization in Songnen Grasslands.

1. Introduction Grassland degradation has the phenomena that grass struggles to grow or can no longer exist on a piece of land due to causes such as overgrazing, climate change and soil salinization (Akiyama and Kawamura, 2007). Soil salinization, one of the major causes of grassland degradation, has received wide attention nowadays. It affects plant growth and distribution by changing the material composition of the ecosystem (Agnieszka, 2003; Cole et al., 2006; Dehaan and Taylor, 2002; Jobbágy and Jackson, 2004), resulting in decrease of biological production. Previous study have revealed that, soil salinization could have a significant impact on belowground systems through changing soil organic matter or base saturation (Wu et al., 2013; Rousk et al., 2011), and these effects should not be neglected. Soil fauna, as an important component in grassland, play a significant role in nutrient cycling and energy flow (Noble et al., 2009; Patricia et al., 2012; Xin et al., 2012), mainly by regulating the composition, distribution, seasonal change of soil microorganisms (Pablo et al., 2013; Song et al., 2008; Yin et al., 2010). Soil fauna is also an important indicator of grassland degradation (Maurizio et al., 2007). Previous studies have been shown that, if soil environmental changes such as moisture or

⁎

nutrients exceeded limitation of the body adaption and regulation, soil fauna’s survival and reproduction could be affected (Yan et al., 2012). Consequently, it is of concern to understand the distribution pattern of soil fauna communities in the grassland. Currently, majority of current studies regarding grassland degradation focus on overgrazing, burrowing of small mammals, and climate change (Arthur, 2007; Li et al., 2012; Xie and Sha, 2012). The studies of soil salinization in grassland degradation are relatively rare. Structure and diversity of soil fauna communities are different by different grassland ecosystems and the same ecosystem of different degrees of degradation (Yeates et al., 1997). Soil fauna, as a crucial indicator of environmental changes, is sensitive to soil salinization. However, few studies regarding the effects of grassland soil salinization on soil fauna distribution have been conducted. To better understand the effects of different salinization on soil fauna distribution and diversity pattern, we selected the salinization habitats of the Songnen Grasslands in this study, where soil salinization was severe (Li and Zheng, 1997). Soil fauna were collected in the different salinization habitats including Chloris virgata, Suaeda corniculata, Puccirrellia tenuiflora, Artemisia anethifolia and Alkali spot habitat. We addresses three questions: for habitats with different degrees of

Corresponding author at: School of Geographical Sciences, Northeast Normal University, 5268 Renmin Street, Changchun, Jilin Province, 130024, PR China. E-mail address: [email protected] (X. Yin).

http://dx.doi.org/10.1016/j.apsoil.2017.09.034 Received 21 December 2016; Received in revised form 21 September 2017; Accepted 23 September 2017 0929-1393/ © 2017 Elsevier B.V. All rights reserved.

Please cite this article as: Yin, X., Applied Soil Ecology (2017), http://dx.doi.org/10.1016/j.apsoil.2017.09.034

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and 20–30 cm) as well. These samples were taken back to the laboratory and extracted for 24 h at 40 °C. A total of 360 soil mesofauna samples were collected (5 habitat s × 1 plot × 4 quadrats × 3 layers × 6 sampling periods). All of the soil fauna samples were preserved in 75% alcohol. The soil fauna were counted under an OLYMPUS SZX16 stereoscopic microscope (Olympus Co., Tokyo, Japan), and identified by order or family levels. The natural moisture content and soil organic matter are important indexes of the soil physical and chemical properties, and pH is an important index of soil salinity. Therefore, when the soil fauna were sampled, each sample of soil was placed in an aluminum box for determination of soil moisture content (SMC). At the same time, a certain number of soil samples were collected for the determination of soil organic matter (SOC) and pH value. In the laboratory, the aluminum boxes were oven-dried at 105 °C for the determination of soil moisture content (SMC). The soil samples were air-dried, foreign bodies were removed, and then the samples were ground. Soil pH value was determined by potentiometry (PHS – 3B precision pH meter). The potassium dichromate method was chosen for the measurement of SOC. The calculation results are shown in Table 2.

salinization (1) what are the respective composition and diversity of soil fauna? (2) What are the respective spatial and temporal distributions of soil fauna? (3) Which environmental factors impact the soil fauna? 2. Materials and methods 2.1. Study area The study site is located at the Yaojingzi, in the southern Songnen Grasslands, Jilin Province, northeastern China (44°40′–44°44′N, 123°44′–123°47′E). The area has a sub-humid continental monsoon climate, with a mean annual temperate of 4.9 °C and mean annual precipitation of 470 mm, mainly concentrated in June to August. The ≥10 °C accumulated temperature is 3000 °C, with a frost-free period of 136–150 d. The warmest monthly average temperature is 22–25 °C while the coldest month average temperature is −16 to 22 °C. The main soil types in the study area include light chernozem soil, saline meadow soil, alkaline meadow soil, alkaline saline soil and chernozem type sand soil (Zhu et al., 2010). The landscape plant community is Leymus chinensis community. The natural grasslands of the Songnen Grasslands are still given priority to for grazing. However, soil salinization is greatly related to grazing. Due to excessive grazing, the soil salinization degree there has been aggravated. According to the salinization degree and the different dominant species, the main plant communities are the Chloris virgata, Suaeda corniculata, Puccirrellia tenuiflora and Artemisia anethifolia habitats.

2.3. Data analysis The data of soil macrofauna and soil mesofauna were combined, and the results were converted into numbers per square meter (Ind/m2). The determination of soil fauna communities diversity indexes used s

the following formula: Shannon-Wiener index: H ′ = − ∑ Pi ln Pi ;

2.2. Field methods

S−1

To analyze the distribution pattern of on soil fauna in different salinization habitats, five habitats were selected. The salinization degrees from low to high were as follows: Chloris virgata (I), Suaeda corniculata (II), Puccirrellia tenuiflora (III), Artemisia anethifolia (IV), and Alkali spot (V) (Table 1). Soil samples were collected from May to October, which corresponded to the main periods of the soil fauna activity in the study site. Four quadrats were randomly established at 5 m intervals. In each quadrat, soil macrofauna samples were collected from the litter layer (50 × 50 cm) and one soil core (50 × 50 cm), and the soil core was divided into 3 layers (0–10, 10–20 and 20–30 cm) in the each month. All litter and soil cores were thoroughly hand-sorted, and all soil macrofauna were collected into vials. A total of 360 soil macrofauna samples were collected (5 habitats × 1 plot × 4 quadrats × 3 layers × 6 sampling periods). Modified Tullgren funnel extractors were used for collecting the soil mesofauna. The samples extracted were collected from the litter layer (10 × 10 cm) and one soil core (10 × 10 cm), and the soil core was divided into 3 layers (0–10, 10–20 Table 1 Characteristics of different salinization degrees in each habitat. Different salinization habitats

Soil salinity (%) Agrotype

Constructive species Accompanying species

Chloris virgata

Suaeda corniculata

Puccirrellia tenuiflora

Artemisia anethifolia

Alkali spot

0.19%

0.26%

0.47%

0.68%

1.12%

salinized meadow soil Chloris virgata Suaeda corniculata; Puccirrellia tenuiflora

salinized meadow soil Suaeda corniculata Puccirrellia tenuiflora; Artemisia anethifolia

salinealkali soil

salinealkali soil

Puccirrellia tenuiflora Artemisia anethifolia

Artemisia anethifolia Puccirrellia tenuiflora

salinealkali soil –

i=1

Margalef richness index: D = ln N ; Pielou evenness index: e = H ′ ln s ; Simpson dominance index: c = ∑(Ni/N)2. Repeated ANOVA measurements were carried out to evaluate the effects of habitat, sampling period and their interactions at the group number and density. One-way analysis of variance was then used to determine the differences in group number, density of soil fauna among habitats, sampling periods and sampling depths, and the difference of diversity indexes among the habitats and sampling periods. Multiple comparisons of means were performed at the 5% probability level using least significant difference (LSD) when the differences were significant. To meet the requirements for normality and homogeneity of variance, all data were ln (x + 1)-transformed. Redundancy analysis (RDA) using CANOCO software for Windows 4.5 was chosen to determine the relative contributions of the measured environmental variables to the communities composition of the soil fauna. To reduce the number of variables, an abundance of 21 orders (sub-orders) of soil fauna, were used to perform the detrended correspondence analysis (DCA) and RDA, which included Prostigmata, Oribatida, Gamasida, Collembola, Coleoptera, Diptera, Homoptera, Hemiptera, Thysanoptera, Araneae, Isopoda, Hymenoptera, Orthoptera, Corrodentia, Symphyla, Plesiopora, Geophilomorpha, Dermaptera, Gastropoda, Lepidoptera, and Opiliones. The data were first analysed by DCA, suggesting that RDA is an appropriate approach (length of gradient < 3). To meet the requirements of DCA and RDA analysis, the data of soil fauna were ln (x + 1) −transformed, and the environment factors were square-root transformed. 3. Results 3.1. Soil fauna communities composition We collected 19,684 individual samples belonging to 3 phyla, 7 classes, 21 orders (suborders) and 108 groups in the five salinization habitats, during six sampling periods. The mean density of soil fauna was 5876.5 individuals/m2, ranging from 4194.5 individuals/m2 in the Alkali spot habitat to 7157.22 individuals/m2 in the Artemisia

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Table 2 Average values of ecological factor in different salinization habitats (Mean ± SE).

pH SOC (%) SMC (%)

I

II

III

IV

V

F

p

10.60 ± 0.06 0.61 ± 0.05AB 14.52 ± 0.96

10.54 ± 0.09 0.73 ± 0.07B 15.80 ± 0.91

10.63 ± 0.04 0.58 ± 0.06A 15.59 ± 1.08

10.54 ± 0.07 0.74 ± 0.05B 13.95 ± 0.89

10.62 ± 0.06 0.47 ± 0.02A 14.39 ± 0.91

0.497 4.858 0.711

0.738 0.005 0.592

I: Chloris virgata habitat, II: Suaeda corniculata habitat, III: Puccirrellia tenuiflora habitat, IV: Artemisia anethifolia habitat, V: Alkali spot habitat. SOC: soil organic matter, SMC: soil moisture content. The same letter(s) indicate no significantly different between each salinization habitat at p < 0.05 by one-way ANOVA.

larvae, Coccinellidae, Anthribidae, Pselaphidae, Tenebrionidae, Chrysomelidae larvae, Scaphidiidae, Cantharidae larvae, Psychodidae, Typhlocybidae, Cicadidae, Pauropdidae and Porcellionidae were captured in more than two salinization habitats, except the Alkali spot habitat. Moreover, the number of specific groups in the Alkali spot habitat (Cupedidae, Helodidae, Chalcidoidea, Miridae) was lower than the other habitats. In May, the Oribatida density (12,350 individuals/ m2) in the Chloris virgata habitat was significantly higher than the other habitats, with density of Gamasida and Prostigmata in the Suaeda corniculata habitat and Artemisia anethifolia habitat being higher in September. The group number and density of the soil fauna showed significant differences among the different sampling periods in the same habitat. The group numbers of the Chloris virgata habitat and Artemisia anethifolia habitat show that the trend first increased and then decreased, with peaks in August (20 per quadrat) and July (23 per quadrat), respectively. There were significant differences in terms of group number in the Artemisia anethifolia habitat among the sampling periods (p < 0.001), while there was almost no change in group number among the different sampling periods. The density of soil fauna was lowest in July or August in each habitat. Significant differences of density were found among the different sampling periods in the Chloris virgata habitat, Puccirrellia tenuiflora habitat, Artemisia anethifolia habitat and Alkali spot habitat (p = 0.003, p < 0.001, p = 0.016, p = 0.001, respectively). The temporal variation of the group numbers differed among the different habitats, but the density was low in summer (July and August), due to the fact that the densities of Prostigmata, Oribatida, Gamasida, Isotomidae and Entomobryidae in spring (May and June) and autumn (September and October) were considerably higher.

anethifolia habitat. The communities were dominated by Prostigmata, Oribatida and Gamasida, which accounted for 50.34%, 17.28% and 16.72% of the total individual density, respectively. The common groups were Isotomidae and Entomobryidae, which made up 6.98% and 1.72% of total individuals, respectively. The remaining taxa only represented 7.04% of the communities. The species diversity of the Artemisia anethifolia and Alkali spot habitats were the highest and lowest in the five salinization habitats, respectively. Prostigmata and Gamasida were the most dominant groups in all habitats. Oribatida and Isotomidae were among the dominant groups in Chloris virgata habitat. Isotomidae and Oribatida were also among the dominant groups in Suaeda corniculata and Puccirrellia tenuiflora habitats, respectively. 3.2. Distribution of soil fauna communities 3.2.1. Horizontal distribution and dynamic There was a difference in the soil fauna diversity among the different habitats, with the highest at 66 groups in the Artemisia anethifolia habitat, followed by 61 groups in the Chloris virgata habitat, 56 groups in the Suaeda corniculata habitat, 50 groups in the Puccirrellia tenuiflora habitat, and 47 groups in the Alkali spot habitat. The repeated ANOVA results (Table 3) show that the responses of group number and density responded significantly to habitat (p < 0.001, p = 0.011, respectively), sampling period (p = 0.002, p < 0.001, respectively), and their interaction (p < 0.001, p = 0.003, respectively) (Fig. 1). The change of group number is more sensitive to habitat than the sampling period, with the density more sensitive than the sampling period. The group number and density of the soil fauna showed significant differences among the different habitats in the same sampling period. The group number of the Alkali spot habitat was lower than that in the other habitats in every sampling period, while the highest was in the Artemisia anethifolia habitat in June, July, September, and in the Chloris virgata habitat in August and October. In addition, there were significant differences among the salinization habitats in May, June, July, August and October (p < 0.001, p < 0.001, p = 0.002, p = 0.010, respectively). The density of soil fauna varied widely among the different habitats. The density was higher in the Chloris virgata habitat than other habitats in May and October, whereas in June, July and August the density in the Artemisia anethifolia habitat was the highest, with the highest density in September occurring in the Suaeda corniculata habitat. The density differed markedly among the habitats in May, July and September (p < 0.001, p < 0.001, p = 0.021, respectively). In addition to the shared group, Staphylinidae

3.2.2. Vertical distribution The group number has a degressive tendency with the increase of soil depth, and the group numbers of the 0–10 cm soil layer are significantly higher than the other two layers in the five habitats (p < 0.001, p < 0.001, p < 0.001, p < 0.001, p < 0.001, respectively) (Fig. 2). The density of the soil fauna in the 0–10 cm layer is highest in the different salinization habitats. The density in the Suaeda corniculata habitat and Artemisia anethifolia habitat exhibit significant differences in three layers (p = 0.009, p = 0.003, respectively). Many soil fauna were found in the 0–10 cm layer, which was located at the top of the soil and exposed to air. Except for mites and Collembolan, there are many types of soil fauna living in the topsoil (Carabidae, Tenebrionidae, Curculionidae, Coccinellidae, Staphylinidae, Elateridae, Carabidae larvae, Silphidae, Curculionidae larvae, Tenebrionidae larvae, Elateridae larvae, Cantharidae larvae, Staphylinidae larvae, Diptera larvae, Formicoidae, Tctrigoidea, Gryllidae, Aphididae, Typhlocybidae, Coccidae, Lygaeidae, Goreidae, Thripidae, Phlaeothripidae, Larvaevoridae, Psocidae, Chironomidae, Araneae, Labiduridae, Miridae, Enchytraeidae, Geophilidae, Pupillidae), which have high density. However, soil fauna, which live in the 10–20 and 20–30 cm layers, are Prostigmata, Oribatida, Gamasida, Isotomidae, Entomobryidae, Pseudachorutidae, Sminthuridae, Onychiuridae, Carabidae larvae, Silphidae, Curculionidae larvae, Tenebrionidae larvae, Elateridae larvae, Cantharidae larvae, Staphylinidae larvae, Diptera larvae, Psocidae,

Table 3 Results of repeated ANOVA measurements of the effects of habitat, sampling period and their interaction on the group number and density of the soil fauna. The statistically significant (p < 0.05) results are in boldface.

Habitat Sampling period Habitat*Sampling period

Group number

Density

F

p

F

p

41.84 4.037 3.018

< 0.001 0.002 < 0.001

3.472 14.318 2.375

0.011 < 0.001 0.003

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Fig. 1. Horizontal distribution of soil fauna in different salinization habitats (Mean ± SE). I: Chloris virgata habitat, II: Suaeda corniculata habitat, III: Puccirrellia tenuiflora habitat, IV: Artemisia anethifolia habitat, V: Alkali spot habitat. Capital letters indicate temporal differences within habitats at the p < 0.05 level, while lowercase letters indicate spatial differences within seasons at the p < 0.05 level.

highly populated; Prostigmata and Gamasida alone account for 88.32%, while Oribatida and Isotomidae make up only 4.57% and 2.33%, respectively. However, the density of soil fauna in the other habitats are relatively homogenous, thus the Alkali spot habitat has a lower Shannon-Wiener index, richness index and evenness index, and higher dominance index. The temporal variations of each diversity index varied among the habitats. The Shannon-Wiener index, richness index and evenness index were higher in July or August, while the dominance index showed the opposite trend. There was a low density of main soil fauna groups (Prostigmata, Oribatida, Gamasida and Isotomidae) in July and August, during which time plants and soil fauna are undergoing the breeding season. In addition to the soil fauna which can survive in all four seasons, Elateridae, Cicindelidae, Cupedidae, Coccinellidae larvae, Jassidae, Miridae, Reduviidae, Thripidae, Scatopsidae, Anthomyiidae, Passalidae, Chrysomelidae larvae, Chrysomelidae, Scarabaeidae larvae, Languriidae, Psychodidae and Aphididae only appeared in July or August, resulting in larger group numbers. Therefore, there are higher Shannon-Wiener indexes and lower dominance indexes in July and August.

Pauropodidae and Enchytracidae, and the density of these groups are lower than the 0–10 cm layer.

3.3. Diversity characteristics The species diversity of soil fauna was highest in the Artemisia anethifolia habitat, followed by the Chloris virgata habitat, with the lowest found in the Alkali spot habitat. The responses of the Shannon-Wiener index, richness index and evenness index responded significantly to habitat (p < 0.001, p < 0.001, p < 0.001, respectively), sampling period (p < 0.001, p < 0.001, p < 0.001, respectively) and their interaction (p = 0.020, p = 0.003, p = 0.021, respectively). The dominance index varied significantly among the habitats (p < 0.001) and sampling periods (p < 0.001). The Shannon-Wiener index and richness index of the Alkali spot habitat are significantly lower than those of the other habitats (p < 0.001, p < 0.001, respectively) (Fig. 3). The evenness index is lowest in the Alkali spot habitat except July and September, while the dominance index is higher in the Alkali spot habitat than the other habitats (p < 0.001). The soil fauna in the Alkali spot habitat are

Fig. 2. Vertical distribution of soil fauna in different salinization habitats (mean ± SE). I: Chloris virgata habitat, II: Suaeda corniculata habitat, III: Puccirrellia tenuiflora habitat, IV: Artemisia anethifolia habitat, V: Alkali spot habitat. Different letters indicate spatial differences within seasons at the p < 0.05 level.

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Fig. 3. Dynamic of soil fauna diversity indexes in different salinization habitats (mean ± SE). I: Chloris virgata habitat, II: Suaeda corniculata habitat, III: Puccirrellia tenuiflora habitat, IV: Artemisia anethifolia habitat, V: Alkali spot habitat. Capital letters indicate temporal differences within habitats at the p < 0.05 level, while lower-case letters indicate spatial differences within seasons at the p < 0.05 level.

3.4. Effects of soil factors on soil fauna communities

4. Discussion

RDA showed that axes 1 and 2 explained 44.9% and 21.6% of the data, respectively (Fig. 4). Different soil variables differed in their influence on the communities composition of soil fauna. The effects of soil organic matter on the soil fauna were significant as shown under the Monte Carlo permutation test (p = 0.046), whereas those of the remaining variables were shown to be not significant under the same test (p > 0.05).

4.1. Spatial distribution and diversity pattern of soil fauna in different salinization habitats Soil salinization can inevitably change the soil micro-environments (Rousk et al., 2011). In this study, we found that there was a significant difference in the taxonomic composition of soil fauna among the 5

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Fig. 4. Redundancy analysis (RDA) showing the relationship between soil fauna composition and soil variables. Five habitats are represented by circles (I: Chloris virgata habitat, II: Suaeda corniculata habitat, III: Puccirrellia tenuiflora habitat, IV: Artemisia anethifolia habitat, V: Alkali spot habitat). Environmental variables (SOC: soil organic matter, SMC: soil moisture content and pH) are represented as arrows and the strength of their impact was directly proportional to the length of the arrow lines.

matter in the Puccirrellia tenuiflora habitat and Alkali spot habitat (higher soil salinizations and pH values), was lower than other habitats (Table 2). In particular, the Alkali spot habitat, due to bare soil, poor nutrients and high pH value, severely limited the growth and reproduction of soil fauna. This further shows that the greater extent of soil salinization leads to lower the density and diversity of the soil fauna.

different salinization habitats in the Songnen Grasslands, and the diversity of soil fauna was lower than that of non-salinization grasslands (Yin and Li, 1998). Studies revealed that the contents of soil soluble salt could change the soil acidity, and this could indirectly affect the survival and reproduction of soil organism (Schrader et al., 1998; Owojori et al., 2009). Therefore, there was lower diversity of soil fauna in salinization habitats of the Songnen Grasslands. In addition, different soil fauna taxa exhibited various tolerance levels to alkaline environment (Butt and Briones, 2017), thus the group numbers of the dominant group and rare group were lower in the higher salinization habitats of the Songnen Grasslands (Table 1). These findings suggest that soil salinization has an important influence on the taxonomic composition of soil fauna. The study results demonstrate that the diversity of soil fauna communities differs significantly among the different salinization habitats. Some previous studies revealed that the discrepancies of diversity among different habitats closely related to environment factors (Begum et al., 2013; Bardgett and van der Putten, 2014). In this study, the total density and diversity of the soil fauna in the Puccirrellia tenuiflora habitat and Alkali spot habitat (the higher salinization habitats), were lower than those in the other habitats. However, the diversity of soil fauna was lower than that of the non-salinization grasslands (Yin and Li, 1998). The reason for this may be that soil salinization altered the soil properties (Esteban and Robert, 2004) and composition, as well as the diversity of plant species (Ramoliya and Pandey, 2003; Masoud and Koike, 2006; Pichu, 2006) (Table 1), resulting in the decrease in diversity of soil fauna. This study showed that the soil fauna communities significantly correlated with soil organic matter (Fig. 4). Some previous studies revealed that soil provides food and habitat, and soil properties can significantly change the composition of soil fauna (Birkhofer et al., 2012; Carmen et al., 2013; Barros et al., 2004).The content of soil organic

4.2. Temporal distribution and diversity pattern of soil faunal in different salinization habitats The density and diversity of the soil fauna communities exhibited pronounced temporal variations between sampling periods, and different habitats. This was likely to be associated with the temporal variations of environmental factors. Zhu et al. (2010) reported that, environmental factors of different salinization habitats exhibited clear temporal variations in the Songnen Grasslands, and other studies suggested that changes in environmental factors have significant effects on the soil fauna communities (Lavelle et al., 1994; Sharon et al., 2001; Popovici and Ciobanu, 2000; Wiwatwitaya and Takeda, 2005). The Songnen Grasslands have a temperature continental monsoon climate, and the environment factors (e.g. soil organic matter, temperature, precipitation, plant species richness) possess seasonal variations. In addition, soil organic matter in the study area also have seasonal variations (Han et al., 2017), thus affecting the composition and diversity of the soil fauna communities. We showed that the density of soil fauna exhibited significant seasonal change, which is the same as reported by Begum et al. (2013). Precipitation had a remarkable effect on the abundance of Collenbola and mites (Benjamin et al., 2006; Elbadry, 1973), of which the density accounted for 93.05–96.13% of the total density of soil fauna in the Songnen Grasslands. This may be due to the fact that there is a heavy 6

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The habitat salinization affected the diversity of soil fauna. The highest diversity occurred in the Artemisia anethifolia habitat, and the lowest in the Alkali spot habitat. At the same time, the diversity and density exhibited pronounced seasonal variations over six months. Meanwhile, majority of soil fauna living in the topsoil. In particular, the group number has a degressive tendency with the increase of soil depth, and density of the 0–10 cm soil layer were higher than the other two layers (10–20 cm; 20–30 cm). The contents of soil organic matter were relatively lower in the higher salinization habitats. Due to the fact that the soil organic matter could provide the soil fauna with abundant food resource, it played an important role in determining the distribution of soil fauna. The soil salinization decreased the contents of soil organic. Finally, soil salinization had a significant effect on the soil faunal communities composition and diversity.

and concentrated rainfall in July and August, which caused the density of Collenbola and mites to decrease significantly, resulting in the lowest density of soil fauna in this period. In May, June, September and October, the soil organic matter and moisture were more suitable for soil fauna, causing the density of soil fauna to rise. Our study found that the changes of density of the soil fauna communities among the sampling periods were quite large; however, the changes of group number and diversity were larger among the habitats. The reason for this may be that the ecosystems of different salinization habitats are relatively stable; and all groups have relatively stable ecological niches with smaller interspecies competition (Cole et al., 2005). The seasonal dynamic of climate, food resources, and soil properties directly leads to an increase in intraspecies competition or reduction of the density of soil fauna (Benjamin et al., 2006). 5. Conclusions

Acknowledgment

The dominant fauna groups in the Songnen Grasslands are Prostigmata, Oribatida and Gamasida. The composition of soil fauna communities differs significantly among the different salinization habitats.

This work is supported by the National Natural Science Foundation of China (40871120).

Appendix A See Table A1.

Table A1 Mean density (Ind/m2) and percentage (%) of soil fauna in different salinization habitats during the sampling time.

Prostigmata Oribatida Gamasida Isotomidae Entomobryidae Diptera larvae Pseudachorutidae Curculionidae larvae Carabidae Sminthuridae Staphylinidae Formicoidae Languriidae larvae Onychiuridae Pauropdidae Porcellionidae Araneae Chironomidae Carabidae larvae Tenebrionidae larvae Nabidae Sciaridae Coccidae Typhlocybidae Tenebrionidae Psocidae Pupillidae Pselaphidae Scaphidiidae Ceratothripidae Geophilidae Tachinoidea Gryllotalpidae Phlaeothripidae Psychodidae Curculionidae Cecidomyiidae Languriidae

Chloris virgata habiatat

Suaeda corniculata habitat

Puccirrellia tenuiflora habitat

Artemisia anethifolia habitat

Alkali spot habitat

Mean

Ind/m2

%

Ind/m2

%

Ind/m2

%

Ind/m2

%

Ind/m2

%

Ind/m2

2911.67 1837.5 922.92 762.75 76.75 63.42 52.08 12.83 28.75 70.83 27.25 4.58 8.33 10.42 6.25 10.58 12.42 29.17 10.83

41.58 26.24 13.18 10.89 1.09 0.91 0.74 0.18 0.41 1.01 0.39 0.07 0.12 0.15 0.09 0.15 0.18 0.42 0.15

2758.42 314.58 1112.5 689.83 81.25 70 56.25 32.33 17.25 8.33 10.75 26.33 18.75 52.08 10.42 15.58 11.33

51.08 5.83 20.60 12.77 1.50 1.30 1.04 0.60 0.32 0.15 0.20 0.49 0.35 0.96 0.19 0.29 0.21

60.48 8.99 14.86 4.39 3.14 0.73 0.79 1.36 0.28 0.41 0.20 0.51 0.03

3090.08 191.67 614.58 97.97 27.14 10.42 8.33 6.67 40.67 4.5 26.75 2.58 20.83 2.08

73.67 4.57 14.65 2.33 0.65 0.25 0.20 0.16 0.97 0.11 0.64 0.06 0.50 0.05

41.67 35 20.17

0.58 0.49 0.28

3.42

0.08

0.21 0.15

30.21 37.131 21.29 3.30 1.66 1.50 0.74 0.45 0.88 0.05 0.33 0.05 0.37 0.04 0.15 0.02 0.17 0.37 0.16 0.04

4332.75 643.75 1064.58 314.75 225 52.25 56.25 97.08 20.17 29.17 14.08 36.58 2.08

11.08 8.33

1699.92 2089.58 1197.92 185.75 93.84 84.33 41.67 25.33 49.58 2.67 18.67 2.83 20.83 2.08 8.33 1 9.58 20.83 8.92 2.17

0.07 0.05

0.21 0.27 0.12 0.33 0.07

0.11 0.001

2.08 4.17 2.08

0.05 0.10 0.05

10.67

0.19

0.001 0.006 0.09 0.15 0.004 0.18 0.05 0.03 0.12 0.01 0.03

0.04 0.12 0.04 0.01 0.15 0.35 0.19 0.15

6.25 0.08

0.08 0.42 6.33 10.42 0.25 12.5 3.83 2.17 8.33 0.83 2.08

2.08 6.25 2.08 0.58 8.33 18.83 10 8.33

0.20 0.48 0.32 0.09 0.17 0.001 0.12 0.17

2.75 2.08

14.67 18.75 8.33 23.08 4.92

14.33 34.67 22.92 6.33 12.5 0.08 8.25 12.5

0.05 0.02

6.5 2.08

0.09 0.03

0.08

0.009 0.04 0.001 0.07 0.14

2.08 0.67

4.08

0.5 2.08 0.08 4.17 7.75

2.75

0.04

1.5 4.17 2.08 0.25 2.17 8.33

0.03 0.08 0.04 0.005 0.04 0.15

1 4.17

0.02 0.07

5.42

0.08

2.08 0.17 2.08 0.83 2.08

0.05 0.004 0.05 0.02 0.05

6.17 0.08

0.11 0.001

2.08 1 2.42

0.03 0.01 0.03

1.17 2.08

0.03 0.05

7

2958.57 1015.42 982.5 410.2 100.78 56.08 42.92 34.85 31.28 23.1 19.5 14.58 14.17 13.33 13.33 12.43 11.38 10 9.58 9.45 7.52 7.1 6.27 5.47 4.88 4.58 4.02 3.8 3.37 3.33 3 2.92 2.52 2.52 2.5 1.88 1.77 1.67 (continued on

% 50.335 17.276 16.716 6.979 1.715 0.954 0.730 0.593 0.532 0.393 0.332 0.248 0.241 0.227 0.227 0.212 0.194 0.170 0.163 0.161 0.128 0.121 0.107 0.093 0.083 0.078 0.068 0.064 0.057 0.057 0.051 0.050 0.043 0.043 0.043 0.032 0.030 0.028 next page)

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Table A1 (continued)

Brenthidae Larvaevoridae Phoridae Aphididae Silphidae Elateridae larvae Staphylinidae larvae Tctrigoidea Tomoceridae Enchytraeidae Lepidoptera larvae Chrysomelidae larvae Lygaeidae Scarabaeidae larvae Scarabaeidae Chrysomelidae Dasytidae larvae Cyphodridae Cupedidae larvae Lagriidae Hydrophilidae larvae Dermestidae Anobiidae larvae Passalidae Nitidulidae Helodidae Chalcidoidea Scatopsidae Anthomyiidae Tipulidae Urothripidae Aeolothripoidea Thripidae Opiliones Coccinellidae Cucujidae larvae Coccinellidae larvae Labiduridae Histeridae Cupedidae Cicindelidae larvae Cantharoidea Mycetophagidae Ichneumonoidea Anthribidae Cucujidae Cicindelidae Elateridae Lucanidae Cantharidae larvae Drosophilidae Cicadidae Jassidae Goreidae Cydnidae Pentatomidae Scydmaeaidae Bruchidae Cerambycidae larvae Meloidae larvae Tortricidae Elasmidae Gryllidae Bradybaenidae Ceratopogonidae Trypetidae Culicidae Ceratocombidae Reduviidae Miridae Total Group numbers

Chloris virgata habiatat

Suaeda corniculata habitat

Puccirrellia tenuiflora habitat

Artemisia anethifolia habitat

Alkali spot habitat

Mean

Ind/m2

%

Ind/m2

%

Ind/m2

%

Ind/m2

%

Ind/m2

Ind/m2

%

2.08

0.04

6.25

0.09

6.25

0.09

2.08

0.04

2.17

0.03

0.42

0.007

0.08 2.08 1 4.17 2.08 0.08 0.08 0.17 0.75

0.001 0.03 0.01 0.06 0.03 0.001 0.001 0.002 0.01

0.10 0.05 0.10 0.002

0.004

0.03 0.01 0.006 0.06 0.002 0.005

4.17 2.17 4.17 0.08

0.25

2.08 0.92 0.42 4.42 0.17 0.3

0.08

0.002

2.08 0.25 1.08

0.04 0.004 0.02

2.25 2.08 0.75 2.33 0.08

0.03 0.03 0.01 0.03 0.001

0.5

0.01

2.08

0.05

0.08

0.002

2.08

0.05

2.08 2.08

0.05 0.05

0.25

0.006

0.08

0.002

0.08 0.17

0.002 0.004

0.17

0.004

0.08

0.002

0.08 4194.5 47

0.002

1.67 1.67 1.25 1.15 0.93 0.92 0.87 0.85 0.83 0.83 0.77 0.65 0.63 0.62 0.45 0.43 0.43 0.42 0.42 0.42 0.42 0.42 0.42 0.42 0.42 0.42 0.42 0.42 0.42 0.42 0.42 0.42 0.42 0.3 0.28 0.23 0.22 0.17 0.13 0.12 0.07 0.07 0.05 0.05 0.033 0.033 0.033 0.033 0.033 0.033 0.033 0.033 0.033 0.033 0.033 0.033 0.017 0.017 0.017 0.017 0.017 0.017 0.017 0.017 0.017 0.017 0.017 0.017 0.017 0.017 5876.5 108

0.028 0.028 0.021 0.020 0.016 0.016 0.015 0.014 0.014 0.014 0.013 0.011 0.011 0.010 0.008 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.005 0.005 0.004 0.004 0.003 0.002 0.002 0.001 0.001 0.0009 0.0009 0.0006 0.0006 0.0006 0.0006 0.0006 0.0006 0.0006 0.0006 0.0006 0.0006 0.0006 0.0006 0.0003 0.0003 0.0003 0.0003 0.0003 0.0003 0.0003 0.0003 0.0003 0.0003 0.0003 0.0003 0.0003 0.0003

0.08 0.08

0.002 0.002

2.08 2.58

0.04 0.05

0.75

0.01

0.17

0.003

2.17 2.08

2.08 2.17

0.04 0.04

2.08 2.08

0.04 0.04

0.04

0.03

2.08

0.04 2.08

2.08

2.08

0.04

2.08 2.08

0.03 0.03

2.08 2.08

0.03 0.03

1.17 0.92

0.02 0.01

1.08 0.25 0.67

0.02 0.003 0.009

0.04

0.03

0.25

0.004

0.25

0.004

0.17

0.002

0.08 0.08

0.001 0.001

0.08 0.42

0.002 0.008

0.17

0.003

0.08 1.17

0.001 0.02

0.08

0.001

0.25 0.17 0.17

0.004 0.003 0.003 0.25

0.17 0.08

0.08

0.08 0.08 0.08

0.08 7003 61

0.03

0.03 2.08

2.08

%

0.08

0.002

0.002 0.001

0.001

0.003

0.08 0.17 0.08 0.08 0.08 0.08

0.003 0.002 0.002 0.002 0.002

0.08

0.002

0.08

0.002

0.08

0.002

0.17 0.17 0.17

0.002 0.002 0.002

0.08

0.001

0.08 0.17 0.08 0.08 0.08

0.001 0.002 0.001 0.001 0.001

0.08 0.08

0.001 0.001

0.08

0.001

0.001

0.001 0.001 0.001

0.001 5400.17 56

5627.5 50

7157.22 66

8

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