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Soil Biology & Biochemistry 79 (2014) 68e77

Contents lists available at ScienceDirect

Soil Biology & Biochemistry

journal homepage: www.elsevier.com/locate/soilbio

Relative roles of spatial factors, environmental ltering and biotic

interactions in ne-scale structuring of a soil mite community
Meixiang Gao, Ping He, Xueping Zhang*, Dong Liu, Donghui Wu**
a

Key Laboratory of Wetland Ecology and Environment, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun
130012, China
b
Key Laboratory of Remote Sensing Monitoring of Geographic Environment, College of Heilongjiang Province, Harbin Normal University, Harbin 150025,
China

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 17 April 2014
Received in revised form
31 August 2014
Accepted 2 September 2014
Available online 18 September 2014

Community theories suggest that community structuring depends on dispersal limitation, environmental ltering and biotic interactions. However, the relative roles of these factors at ne scale are less
well understood. In this study, we attempt to determine the relative roles of spatial factors, environmental ltering and biotic interactions in the ne-scale (5 m) structuring of a soil mite community from a
temperate deciduous forest in the Maoershan Ecosystem Research Station in northeastern China. In
August 2012, we established three plots and collected 100 samples from each plot in a 5
5 m2 area
using a spatially delimited sampling design. To quantify the relative contributions of the spatial and
environmental processes, Moran's eigenvector maps (MEMs), variation partitioning analysis and partial
Mantel test were used. Null and neutral models were used to disentangle the effects of biotic interactions. Null mode analyses were conducted for non-random patterns of species co-existence and
signicant species-pairs in the assemblage of soil mites, and to determine whether the observed pattern
was the result of biotic interactions. The neutral model was used to identify whether the community
structure shows divergence, convergence or neutrality. The results indicated that the relatively large and
signicant variance was due to spatial factors in all plots. The contribution of environmental ltering was
relatively low and non-signicant in all plots based on variation partitioning, while it was signicant in
Plot II based on a partial Mantel test. Soil organic matter content, soil pH, and soil and litter water content
explained a signicant part of the variance observed in the distribution of the mite community.
Furthermore, the null model revealed a non-random co-occurrence pattern in the soil mite community,
and the environmental niche overlap indicated a weak contribution of biotic interactions. The observed
mean dissimilarity implied signicant divergence in communities based on neutral model analysis.
Collectively, these results emphasize that both spatial and environmental processes were important
drivers in the ne-scale structuring of soil mite communities in a temperate deciduous forest and that
biotic interactions were less inuential in the observed pattern.

Keywords:
Spatial factors
Environmental ltering
Biotic interactions
Soil mite community
Fine-scale
Temperate deciduous forest

2014 Elsevier Ltd. All rights reserved.

1. Introduction
Many studies have questioned the manner in which species
form assemblages and the rules that govern this process. According
to niche and neutral theories in community ecology, the

* Corresponding author. Tel.: 86 13804576310.

** Corresponding author. Tel.: 86 15904308293.
E-mail addresses: gmx102@hotmail.com (M. Gao), 1545932025@qq.com (P. He),
gmx102@163.com (X. Zhang), liudong@neigae.ac.cn (D. Liu), wudonghui@neigae.ac.
cn (D. Wu).
http://dx.doi.org/10.1016/j.soilbio.2014.09.003
0038-0717/ 2014 Elsevier Ltd. All rights reserved.

composition of species assemblages can be explained by three

processes: dispersal limitation, environmental ltering and biotic
interactions (Drake, 1990; Weiher and Keddy, 2001; Gilbert and
Lechowicz, 2004; Leibold et al., 2004; Tews et al., 2004). Neutral
theories suggest that species are ecologically equivalent and that
community structure relies strongly on stochastic processes and
dispersal limitation (Hubbell, 2001). In contrast, niche theories
emphasize that the appearance of species in a specic habitat is
based on biotic interactions and environmental ltering, the latter
ltering species from the regional species pool (Diamond, 1975;
Chase and Leibold, 2003; Webb et al., 2010). In fact, these

M. Gao et al. / Soil Biology & Biochemistry 79 (2014) 68e77

theories are not mutually exclusive and evidence for both has been
reported for various communities at different spatial scales (Lindo
and Winchester, 2009; Dumbrell et al., 2010; Caruso et al.,
2012b). However, their relative roles are still not well known
(Chase and Myers, 2011; Winegardner et al., 2012).
Indeed, the relative roles of spatial factors, environmental
ltering and biotic interactions in community structuring are hypothesized to be scale-dependent. Environmental heterogeneity is
expected to function at larger scales (Weiher and Keddy, 1995;

n, 2010),
Swenson et al., 2007; Cavender-Bares et al., 2009; Sobero
because the substantial variation in environmental variables allows
species to co-exist. At larger spatial scales, community structuring
may be constrained by spatial factors (dispersal limitation)
(Declerck et al., 2011; Sokol et al., 2013; Tang et al., 2013) and
dispersal limitation might override environmental ltering in
certain habitat types (Bello et al., 2013). In addition, the inuence of
biotic interactions becomes gradually more important as the spatial
scale decreases and they might have no obvious effect at scales
larger than small (101e103 m) or ne (<101 m) (Hortal et al., 2010).
Moreover, in order to describe the underlying mechanisms of
species distribution, it is essential to explicitly consider the variables in multiscales (Hortal et al., 2010). However, processes at the
small scale often have been neglected when recognizing processes
at large scales and it is difcult to infer that variation at the small
scale is regulated by stochastic processes (Anderson et al., 2011).
Disentangling the mechanisms at larger spatial scales might be
challenging, as insufcient considering underlying processes at
relative ne-scales (Anderson et al., 2011; Caruso et al., 2012b).
Soil harbors a large diversity of organisms, which represent
most of the world's terrestrial biodiversity (Wardle, 2002; Bardgett,
ns, 2010). However,
2005; Bardgett and Wardle, 2010; Decae
fundamental questions relating to the causes and maintenance of
this diversity remain only partially answered (Bardgett, 2002;

ttir et al., 2012; Caruso
Lindo and Winchester, 2009; Ingimarsdo
et al., 2012b, 2013). Environmental variability is known to allow
for the spatial co-existence of competing earthworm species, which

nez
emphasizes the importance of environmental ltering (Jime
et al., 2012). On the other hand, Caruso et al. (2013) reported that
biotic interactions might be a predominant factor in the structuring
of soil metacommunity dynamics. Other publications have also
demonstrated the important contributions of biotic competition,
environmental ltering, or/and spatial factors to the structuring of
ns et al., 2008; Lindo and
soil animal communities (Decae

ttir et al., 2012; Caruso et al.,
Winchester, 2009; Ingimarsdo
2012b). However, the question of the relative roles of these variables at the ne-scale remains little studied.
Soil mite communities represent ideal assemblages to test the
relative roles of the underlying processes in ne-scale community
structuring. According to niche theories, environmental heterogeneity can create varied micro-conditions for co-occurring species,
whereas environmental conditions seem to be more homogeneous
at the ne scale and thus the environmental heterogeneity may be
less important in maintaining diverse species at this level. When
considering the highly spatial connectivity and reachability,
dispersal might be sufcient to allow species to survive in microhabitats with suitable environmental characteristics, in other
words, dispersal might be not limiting (Fuentes, 2002). Thus, it may
be that spatial factors are not important in regulating community
structure at ne scale. Soil mite communities have large diversity at
small spatial scales. Given the highly similar resources at the nescale, the neighboring coexisting species largely share or compete
for limited local resources and spaces (Weiher and Keddy, 1995;
Kraft and Ackerly, 2010). Consequently, the biotic interactions
have the most opportunity to be a major structuring force at the

mez et al., 2010). However, those
ne scale (Wardle, 2006; Go

69

processes may operate simultaneously in a ne-scale community

(Logue et al., 2011; Winegardner et al., 2012) and perhaps different
in intensity.
In this study we addressed the relative contributions of spatial
factors, environmental ltering and biotic interactions on the nescale structuring of soil mite communities in a temperate deciduous forest at the Maoershan Ecosystem Research Station in northeastern China. We tested two hypotheses in this study: 1) spatial
factors and environmental ltering should play relative minor roles
for these communities and 2) biotic interactions should play an
important role in community structuring at the ne scale.
2. Materials and methods
2.1. Study site
The study was performed at the Maoershan Ecosystem Research
Station (127 300 e340 E, 45 200 e250 N) of the Northeast Forestry
University in Heilongjiang Province, China. This area is covered
with typical forests of northeastern China. The region lies within a
continental temperate monsoon climate. The climate is characterized by an average annual temperature of 2.8  C and an average
annual precipitation of 884 mm. The average altitude is approximately 300 m and the average degree of slopes is about 10e15 . The
type of parent material is granite bedrock and the type of soil is a
Hap-Boric Luvisol (Gong et al., 1999). The annual evaporation is
approximately 884 mm. The frost-free days are about 120e140.
Soil mite communities were collected in a temperate deciduous
forest at the Maoershan Ecosystem Research Station. This location
has a 60-yr old secondary forest with an 18 m tall canopy layer. The
main tree species include Fraxinus mandshurica Rupr., Ulmus
davidiana Planch. var. japonica (Rehd.) Nakai, Betula platyphylla
Suk., Populus davidiana Dode, Juglans mandshurica Maxim., Acer
mono Maxim., Tilia amurensis Rupr. and Populus ussuriensis Kom.,
and the main shrub species include Syringa reticulata (Blume) Hara
var. amurensis (Rupr.) Pringle, Padus racemosa (Lam.) Gilib., Acer
ginnala Maxim. and Corylus mandshurica Maxim.
2.2. Soil mite communities and soil sampling
Three experimental plot replicates (5
5 m2) were established
at the study site in August 2012. The distance between each replicate (Plot I, Plot II and Plot III) was more than 60 m. Each plot was
divided into 100 squares of 0.5
0.5 m2. Soil mite samples were
obtained from the left-bottom area of each square. Square soil
samples (15
15 cm2 and 10 cm depth) were collected for the
extraction of mite communities. These communities were removed
from 500 5 g of the square soil samples using the Berlese-Tullgren

rrez-Lo

pez et al., 2010), with mites
method (Krantz, 1978; Gutie
being preserved in a 95% alcohol solution. Adult soil mites were
identied to the species level and then were counted respectively
(Balogh and Balogh, 1992; Yin et al., 1998; Walter and Proctor, 2001;
Krantz and Walter, 2009). Soil mite juveniles were excluded from

ttir et al., 2012).
all analyses (Ingimarsdo
A vegetation-free soil core sample (5
5 cm2 and 10 cm depth)
was taken directly to the right of each square used to sample the
soil mites. These soil samples were air-dried and then sieved to
1 mm. To obtain soil's organic matter content, the colorimetric
method after digestion in H2SO4 was used. The soil water content
was determined gravimetrically. In deionized water with a soil/
solution ratio of 1:5, the soil pH was obtained (Lao, 1988; Pansu and
Gautheyrou, 2003). In addition to the plant species richness (the
number of vascular plant species), the DBH (diameter at breast
height) and basal diameter of vascular plant, the litter dry weight
(10
10 cm2) and the litter water content were measured.

70

M. Gao et al. / Soil Biology & Biochemistry 79 (2014) 68e77

2.3. Statistical analysis

Differences in species richness and abundance of the mite
communities between three plots were tested using a one-way
ANOVA (analysis of variance). As the variances were not homogeneous in all plots, the one-way ANOVA and post hoc Tamhane-T2
test were used.

2.3.1. Relative roles of spatial factors and environmental ltering

When considering the co-varying environmental variables in
each plot, a principal component analyses (PCA), grounded on the
correlation matrices, was selected to reduce the multivariate variables to uncorrelated variables. As independent environmental
variables, the principal components (PCs) were used for subsequent

mez et al., 2010).
analyses of each plot (Go
The powerful approach of distance-based Moran's eigenvector
maps (MEMs, formerly named PCNMeprincipal coordinates of
neighbor matrices) (Borcard and Legendre, 2002; Dray et al., 2006;
Legendre and Gauthier, 2014) was used to reveal the effects of
spatial variables on the community assembly. MEMs analysis produces a range of spatial variables derived from the geographic coordinates of each plot (Dray et al., 2006). The MEMs gure spatial
variation across multiple spatial scales and can be served as
explanatory spatial factors of community variation (Diniz-Filho and
Bini, 2005; Peres-Neto and Legendre, 2010). A Hellinger transformation was applied to the species abundance matrices prior to
analysis (Legendre and Gallagher., 2001; Borcard et al., 2011). In
Plot I, Plot II and the Mean Plot, signicant linear trends were found,
so the data of soil mite communities were detrended. The residuals
were then used as input data in later spatial analyses of those plots
and the non-detrended data were used in Plot III. Next, a forward
selection process was performed based on the adjusted R-square to
choose the linear combination of vectors that describes the most
variation in the mite species matrix with the lowest possible
number of vectors (Dray et al., 2006; Borcard et al., 2011). After the
forward selection procedure, 9, 10, 3 and 8 MEMs were chosen in
Plot I, Plot II, Plot III and the Mean Plot, respectively; these
explained 8.91, 13.61, 3.61 and 7.58% of the variation of the soil mite
community (P < 0.05), respectively.
Variation partitioning was then used to infer the relative
contribution of spatial factors and environmental ltering on the
soil mite community matrix of each plot (Legendre and Legendre,
1998; Cottenie, 2005; Blanchet et al., 2014). The chosen environmental variables (PCs) and spatial variables (MEMs) were
analyzed with the powerful, partial redundancy analysis (pRDA)
method. A pRDA allows the total variation of a species matrix in
each plot to be partitioned into fractions that represent the
contribution of the pure environmental fraction [a], the spatially
structured environmental fraction (shared fraction) [b], the pure
spatial fraction [c], and the unexplained fraction [d] (Peres-Neto
et al., 2006; Borcard et al., 2011). The signicance of each
source of variation was tested with a Monte Carlo permutation
test (999 permutations).
In a patchy environmental resource condition, a combination of
spatially explicit analysis and partial Mantel test should be helpful
for revealing the roles of environmental and spatial variables

nez et al., 2011). A partial Mantel test was calculated to exam
(Jime
whether the community dissimilarities depended on spatial distances or environmental distances (as an agent for environmental
ltering) (Kristiansen et al., 2012; Wang et al., 2013). Although a
partial Mantel test might not be suitable for partitioning the variation in community assembly (Legendre et al., 2005, 2008;
Legendre and Fortin, 2010), it can be helpful in recognizing
whether there is obvious distance decay.

The multivariate analyses and partial Mantel test were implemented using the vegan (Oksanen et al., 2013) and packages in the
R software, version 3.0.1.
2.3.2. Null model and neutral model analysis
To determine whether patterns of species co-occurrence in the
overall matrix showed signs of non-random processes, we performed a formal null model analysis (Gotelli, 2000; Gotelli and
Ulrich, 2012). The commonly used indices of C-score and V-ratio
were used (Gotelli, 2000; Gotelli and McCabe, 2002). The cooccurrence procedures are very sensitive to variation in species
occurrence frequencies, hence row totals were saved as a constraint
in the null model (Gotelli, 2000). Additionally, the V-ratio is
determined by the row and column sums of the matrix (Gotelli,
2000), therefore it is not valid for the FF (xedexed) algorithm.
Thus, the FF, FE (xedeequiprobable) and FP (xedeprobability)
algorithms were used to calculate the C-score, and the FE and FP
algorithms were used to calculate the V-ratio (Gotelli, 2000; Gotelli
and Ulrich, 2010, 2012).
The C-score is an aggregate index that describes the average
behavior of a metric that is calculated on a species-pair basis.
Consequently, important information can be detected by testing for
non-random patterns in species associations on a species-pair basis. Nevertheless, this approach creates the statistical problem that
the amount of possible pairs is high. This problem considerably
increases the risk of Type I errors (Gotelli and Ulrich, 2010). Thus,
this analysis was performed by calculating the C-score for each
species pair and then identifying its signicance using the four
methods suggested by Gotelli and Ulrich (2010). Of these, the CL
(condence limit criterion) is the most liberal and simplest method.
For the CL, when the number of species pairs in a matrix is large,
then 5% of them will fall outside the 95% condence limits simply
by chance (Gotelli and Ulrich, 2010; Krasnov et al., 2011). To address
this problem, the conservative criteria of BY (after sequential
Bonferroni correction) (Benjamini and Yekutieli, 2001), BM
(empirical Bayes mean-based criterion) and BCL (empirical Bayes
condence limits-based criterion) were introduced (Gotelli and
Ulrich, 2010). The steps undertaken to fulll the four criteria can
be found in Gotelli and Ulrich (2010).
Next, the standardized effect size (SES) was calculated to evaluate the direction and extent of deviation from the null model. The
SES evaluates the degree of standard deviations by which the
investigated index is higher or lower than the mean index of the
simulated assemblages (Gotelli and McCabe, 2002). Supposing the
SES values a normal distribution, a 95% condence interval of the
SES values is supposed to occur between 2.0 and 2.0. The C-score
and V-ratio indices were obtained using the Ecosim 7.0 software
(Gotelli and Entsminger, 2009). Signicant species-pairs were obtained based on the PAIRS software (Ulrich, 2008).
The neutral model has suggested as a specic form of more
general null model in community ecology (Gotelli and McGill,
2006). Moreover, the neutral model is a valuable tool for community ecologists with dynamic quantitative expectation in the light of
community dissimilarity (Dornelas, 2010). Thus, a neutral model
was also applied to identify whether the community showed signicant convergence, divergence or just neutrality. Based on the
species abundance distribution (SAD) in each plot and the Mean
plot, the neutral diversity (q) and immigration parameters (Hubbell's m or Etienne's I) (Hubbell, 2001; Etienne, 2007) were evaluated according to a neutral sampling formula for multiple samples,
as introduced by Etienne (Etienne, 2007, 2009). The formula allows
one to gure an exam of q and m (Etienne, 2007, 2009). Fundamental diversity (q) represents the product of the size of the metacommunity and the speciation rate (Etienne, 2007), and the
average immigration parameter (m) calculates the amount of

M. Gao et al. / Soil Biology & Biochemistry 79 (2014) 68e77

dispersal limitation of the local community and can be explained as

the number of potential immigrants competing with local individuals for vacant sites (Etienne and Olff, 2004; Etienne, 2009).
The PARI/GP codes written by Etienne (Etienne, 2007, 2009) were
used to calculate q and m, from which expected SADs were produced. Jaccard indices were then used to identify community dissimilarities based on species abundance for both the observed and
expected communities, which were compared with a bootstrapped
t test (Efron and Tibshirani, 1993; Caruso et al., 2012a, 2012b). Then,
we performed a meta-analysis of the results of calculated and expected community dissimilarities to explore the effects of moderators (i.e. predicted effect). Notionally, the moderators are
partitioned into three models: neutral, divergent and convergent.
Based on a random-effects model, a continuous meta-analysis was
performed. Then a Kendall's rank correlation (Begg and Mazumdar,
1994; Viechtbauer, 2010) was selected to evaluate the funnel plot
asymmetry. All analyses were performed in R platform with
vegan, bootstrape and metafor packages (Viechtbauer, 2010).
2.3.3. Pinka Ojk niche overlap index
To identify whether the pattern obtained was due to interspecic competition or environmental ltering that structured the soil
mite community, Pianka's Ojk (Pianka, 1973), a community-level
niche overlap index, was performed using the mean niche overlap of the total possible pairwise species. The range of the Pianka Ojk
metrices is between 0 and 1. We also gured the values of the SES
ns et al., 2009). A value smaller than expected by chance
(Decae
represents a competitively assemblage, which perhaps resulted
from biotic interactions, especially interspecic competition. A
value above that expected by chance indicates that all species have
similar patterns of resource utilization, which may be caused by
environmental constraints (Albrecht and Gotelli, 2001). The niche
partitioning for environmental variables was calculated from the
individual matrices, in which the rows represented individual
species and the columns represented environmental variables
(PCs). Each entry represented the number of individuals caught in

nez
each plot for a given range of the environmental variables (Jime
ns
et al., 2012). For a detailed description of the method, see Decae

nez et al. (2006, 2012) and Pianka (1973).
et al. (2009), Jime
Calculation and tests of Pinka Ojk niche overlap were carried out
using the niche overlap module of the Ecosim 7.0 software
(Gotelli and Entsminger, 2009).

71

Table 1
Species richness (number of mite species in each plot) and abundance (total number
of individual mites in each plot) of the soil mite communities in a deciduous forest at
Maoershan Mountain Station (northeastern China).
Plot I
Macrocheles sp.
Pachyseius sp.
Epicriidae sp.
Gamasolaelaps sp.
Nanhermannia sp.
Eulohmannia sp.
Belba sp. 1
Scheloribates sp.
Suctobelbella sp.
Geholaspis sp.
Protoribates sp.
Oribatida sp.
Acrotritia ardua (Koch, 1841)
Prostigmata sp.
Ceratozetes sp.
Holaspulus sp.
Belba sp. 2
Hypochthonius sp.
Trombidiidae sp.
Species richness (J)a
Total number of mites (S)a

603 (D)
3302 (E)
530 (D)
NFb
67 (B)
1331 (E)
739 (E)
1 (A)
2671 (E)
184 (C)
182 (C)
1184 (E)
602 (D)
745 (D)
1284 (E)
126 (B)
14 (A)
1321 (E)
2 (A)
18H
14 888H

Plot II

Plot III

Mean plotc

598 (E)
3874 (E)
232 (B)
1 (A)
11 (A)
1701 (E)
126 (C)
2 (A)
2149 (E)
832 (B)
919 (D)
276 (D)
243 (D)
14 (A)
227 (D)
275 (D)
1 (A)
361 (D)
2 (A)
19I
11 844I

575 (E)
3412 (E)
110 (B)
48 (A)
47 (16)
1657 (E)
210 (C)
63 (A)
1965 (E)
397 (70)
1149 (E)
386 (E)
230 (D)
102 (A)
314 (D)
229 (D)
39 (A)
483 (D)
1 (A)
19H
11 417I

592 (E)
3529 (E)
291 (E)
16 (A)
42 (C)
1563 (E)
358 (E)
22 (A)
2262 (E)
471 (E)
750 (E)
615 (E)
358 (E)
287 (D)
608 (E)
210 (E)
18 (A)
722 (E)
2 (A)
19
12 716

a
Different letters indicate signicant differences. J represents community size
and S represents observed richness when estimating the neutral model parameters
for each plot and the Mean plot.
b
NF indicates not found.
c
Data in the Mean plot were the averages of Plots I, II and III combined.
d
Raunkiaer's frequency class. A: 1e20%; B: 21%e40%; C: 41e60%; D: 61e80%;
E: 81e100%.

3.3. Relative contributions of spatial factors and environmental

ltering
The amount of variation accounted for by the pure spatial
fraction [c] was relatively large and signicant in all plots. The
variation explained by the pure environmental fraction [a] and the
spatially structured environmental fraction [b] were relatively
lower and non-obvious in each plot (Fig. 2). Based on the results of
the redundancy analysis, the effects of the specic PCs were
obvious in each plot (Table 2). In plot II, the community dissimilarity exhibited obvious correlation coefcients with the environmental variables after accounting for the effect of spatial variables
(Table 3).

3. Results
3.1. Community assembly
In total, 38 149 soil mites individuals were detected. The most
frequent and abundant soil mite species were Pachyseius sp.,
Eulohmannia sp. and Suctobelbella sp. The species richness of the
soil mite community was obviously different between Plots I and II,
and between Plots II and III. Additionally, the abundance of the soil
mite community was signicantly different between Plots I and II,
and between Plots I and III (Table 1). Overall, the individual-based
rarefaction curves (Gotelli and Colwell, 2001) showed that the
sampling efforts were sufcient to describe the overall richness of
the soil mite communities (Supplementary Material Appendix 1).
3.2. Results of environmental principal components
Eigenvalues of the rst four axes of the PC explained 80.82, 78.84,
79.15 and 73.56% of the total inertia for Plot I, Plot II, Plot III and the
Mean plot, respectively. Four PCs were selected for each plot (Fig. 1).
A summary of the statistics for the environmental variables
analyzed is given in the Supplementary Material Appendix 2.

3.4. Species co-occurrence, signicant species-pairs, niche overlap

and neutral model
According to the C-score with the FF algorithm for Plot II and
Plot III, species co-occurrence showed signicant spatial segregation. The co-occurrence patterns of the other assemblies, which
showed non-randomness based on the C-score or V-ratio with FF or
FE algorithms, all showed signicantly spatial aggregations
(Table 4).
In terms of the pair-based co-occurrence analysis with the FE
algorithm based on the four criteria, there were more signicantly
aggregated species-pairs than segregated species-pairs in all plots.
According to the same analysis with the FF algorithm, for those
plots in which signicant species pairs were identied, there were
more signicantly segregated species-pairs than aggregated
species-pairs, except for the Mean plot based on the CL criterion,
and Plot III based on the BM criterion (Supplementary Material
Appendix 3).
The average values of community Ojk for the environmental
factors were 0.86, 0.81, 0.83 and 0.89 in Plot I, Plot II, Plot III and in

72

M. Gao et al. / Soil Biology & Biochemistry 79 (2014) 68e77

Fig. 1. The rst four axes derived from principal component analysis (PCA) of the environmental variables in each plot. The factor coordinates (arrows) are built from the PC1, PC2,
PC3 and PC4 eigenvector coefcients. LDW-litter dry weight (g), LWC-litter water content (w/w%), SWC-soil water content (w/w%), PR-plant species richness (the number of
vascular plant species), GD-basal diameter of vascular plant (mm), DBH-diameter at breast height (mm), SOM-soil organic matter content (g kg1), pH-soil pH. (a), (b), (c) and (d)
represent Plot I, Plot II, Plot III and the Mean plot.

the Mean plot, respectively. For all environmental variables, the

observed values of the Ojk niche overlap were larger than the
simulated values. Except for PC2 in Plot II, the values of the SES
were obviously larger than 2, which indicates that soil mite communities were not competitively structured (Table 5).
According to the evaluation of the neutral model parameters
and the corresponding test based on observed and simulated mean
dissimilarities, neutrality can be rejected. Obvious funnel plot
asymmetry was not founded (P > 0.05) and signicant heterogeneity was detected (P < 0.001) (Fig. 3).

4. Discussion
4.1. Relative roles of spatial factors and environmental ltering
Our analyses suggest that pure spatial pattern had a signicant
inuence on the ne-scale structuring of each mite community. The
analysis based on MEMs allowed us to identify spatial factors
(dispersal limitation and demographic stochasticity) in mite communities. The spatial pattern might result from dispersal-related
processes, such as physical barriers or dispersal ability (Cottenie,

Fig. 2. Variation partitioning for soil mite community in each plot tested by partial redundancy analysis (pRDA). Pure environmental [a], pure spatial [c] and shared fractions [b] are
provided. Negative values are not shown. (a), (b), (c) and (d) represent Plot I, Plot II, Plot III and the Mean plot. **P < 0.01.

M. Gao et al. / Soil Biology & Biochemistry 79 (2014) 68e77

Table 2
The effect of environmental factors on the soil mite community structures analyzed
by redundancy analysis and Monte Carlo permutation test (999 permutations).
Factor

Plot I

PC1a
PC2
PC3
PC4

P
P
P
P

Plot II

0.11
0.07
< 0.001
0.03

P
P
P
P

Plot III

0.06
< 0.001
0.12
0.03

P
P
P
P

Mean plot

< 0.01
0.11
0.03
0.02

P
P
P
P

0.96
< 0.001
< 0.001
0.36

a
PC indicates each of the factors that were obtained from the PCA for each of the
data sets.

Table 3
Partial Mantel test of soil mite community dissimilarity against spatial distance and
environmental distance for each plot (999 permutations).
Plot I

EnvironmentjSpacea
SpacejEnvironmentb

Plot II

Plot III

Mean plot

0.01
0.06

0.38
0.90

0.10
0.01

0.01
0.40

0.07
0.01

0.11
0.57

0.04
0.03

0.18
0.76

a
Soil mite community dissimilarity with environmental distance, controlling for
spatial distance.
b
Soil mite community dissimilarity with spatial distance, controlling for environmental distance.

nroos et al., 2013),

2005; Soininen et al., 2007; Soininen, 2012; Gro
and it is more important when considering the lower active disnroos et al.,
persers (Cottenie, 2005; Soininen et al., 2007; Gro
2013). Active dispersal is the primary means of reaching different
locations for most soil mite species. Terrestrial oribatid mite assemblages are restricted by low dispersal activities at the local scale
nroos et al., 2013). Fine-scale
(Lindo and Winchester, 2009; Gro
dispersers show signicant spatial limitation, perhaps because
their limited dispersal capabilities prevent them from tracking
nroos et al., 2013). Unenvironmental micro-heterogeneity (Gro
fortunately, information on the dispersal abilities of the soil mite
species found in the study area are still lacking and this aspect
needs further investigation.

73

According to neutral theory, community structure can be

explained by spatial factors independent of environmental variables. However, observed community dissimilarity of each plot and
the Mean plot were obviously greater than those predicted using a
neutral model. A quantitative neutral model based on community
dissimilarity (Dornelas et al., 2006; Etienne, 2007) can be used to
recognize the sign of the deterministic regulator of assembly
(Caruso et al., 2012b), nevertheless the underlying mechanisms
accounting for this sign still indistinct (Gotelli and McGill, 2006;
Caruso et al., 2012b). It can be inferred that community structuring can be controlled not only by spatial factors but also by other
processes, such as environmental ltering. The signicant heterogeneity and divergence of each community based on neutral model
analysis suggest that environmental variables might lter species
into local communities (Dornelas et al., 2006). Although a much
smaller and non-signicant fraction of variation was accounted for
by the spatially structured environmental factors and the pure
environmental factors, we cannot simply exclude the effect of
environmental ltering on soil mite assemblages. The soil environmental factors (soil organic matter content, soil pH value, soil
water content and litter water content) were important for the soil
mite communities in Plots I and II. The above-ground vegetation
factors (basal diameter, plant species richness and DBH) were
important in Plot III. It is difcult to conclude that above-ground
plant variables govern soil mite community assemblages. The
food resources of soil mite communities include litter ingredient
and soil fungi (Siepel and Ruiter-Dijkman, 1993; Schneider and
Maraun, 2005). Therefore, the driver of soil mite community assemblies is most likely not the plants themselves. Instead, their
inuence is probably indirect: plant litter affects soil organic matter
and soil water content, which in turn affect the soil microorganisms

ttir et al., 2012). In
on which mite communities feed (Ingimarsdo

nez et al.,
this research, an environmental regulating structure (Jime
2012) was detected in each plot according to the analysis of the
environmental niche partitioning. Moreover, the results of the
partial Mantel test indicated a signicant contribution of environmental fractions in Plot II. In addition, according to Raunkiaer's

Table 4
Species co-occurrence analysis for testing whether species distributions can be approximated by random distributions generated by statistical models (null model analysis).
Plot

Index

Null model

Observed indexa

Mean of simulated indexb

SESc

Initial P valued

Corrected Pe

Plot I

C-score

FE
FF
FP
FE
FP
FE
FF
FP
FE
FP
FE
FF
FP
FE
FP
FE
FF
FP
FE
FP

110
110
110
1.45
1.45
130
130
130
1.93
1.93
112
112
112
2.46
2.46
18.7
18.7
18.7
1.33
1.33

122
108
118
1.00
1.15
161
127
151
1.00
1.28
148
104
137
1.00
1.39
21.3
17.9
21.1
1.00
1.02

2.76
1.00
1.63
3.33
1.92
6.03
3.04
3.44
6.86
3.93
7.94
6.95
4.39
10.7
5.95
1.33
1.23
1.22
2.50
2.35

<0.01
0.84
0.06
<0.01
0.04
<0.001
<0.01
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
0.09
0.11
0.11
0.01
0.02

0.01
0.84
0.06
<0.01
0.06
<0.001
<0.01
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
0.27
0.17
0.11
0.02
0.02

V-ratio
Plot II

C-score

V-ratio
Plot III

C-score

V-ratio
Mean plot

C-score

V-ratio
a

The observed indices are those values that were calculated from the observed assemblages.
Mean of simulated indices were values after 50 000 randomizations.
c
A SES (standardized effect size) is calculated as [(observed value-mean of simulated value)/standard deviation of simulated value]. For the C-score, a SES >2 indicates
signicant species segregation, and a SES <2 indicates signicant species aggregation. For the V-ratio, a SES >2 indicates signicant species aggregation, and a SES <2 indicates
signicant species segregation.
d
Initial tail probability of observed indices that were obtained by random permutations.
e
The corrected P-associated tailed probability (P < 0.05) is indicated after the false discovery rate (FDR) procedure (Benjamini and Yekutieli, 2001).
b

74

M. Gao et al. / Soil Biology & Biochemistry 79 (2014) 68e77

Table 5
Community niche analysis for selected environmental principal components.
Plot

Environmental variableb

Observed index

Mean of simulated index

SES

Initial Pc

Corrected Pd

Plot Ia

PC1
PC2
PC3
PC4
PC1
PC2
PC3
PC4
PC1
PC2
PC3
PC4
PC1
PC2
PC3
PC4

0.96
0.83
0.80
0.85
0.96
0.70
0.82
0.74
0.95
0.79
0.81
0.84
0.95
0.89
0.86
0.88

0.48
0.77
0.75
0.80
0.44
0.68
0.59
0.72
0.16
0.71
0.63
0.74
0.73
0.72
0.80
0.79

20.4
6.63
4.68
5.96
20.0
1.49
12.5
2.20
22.5
7.09
11.6
9.54
19.7
14.3
6.96
11.4

<0.001
<0.001
<0.01
<0.001
<0.001
0.92
<0.001
0.04
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001

<0.001
<0.001
<0.01
<0.001
<0.001
0.92
<0.001
0.05
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001

Plot IIa

Plot IIIa

Mean plota

a
Average niche overlap for each plot was calculated for multidimensional environmental principal components by averaging the single Ojk values for each resource that was

nez et al., 2012).
exploited in the environmental principal components by the community and compared with a null model (30 000 simulations) (Jime
b
PC indicates each of the factors that was obtained from the PCA for each of the data sets.
c
The initial P value indicates the probability that the standardized effect size (SES) differed from zero.
d
The corrected P value indicates the probability at P < 0.05, after the FDR procedure correction.

frequency class distribution in all plots, more than 50% of the

species belong to classes D and E (Table 1), meaning that over half
the species are distributed broadly in each plot. Therefore, we can
infer that the mite species were widely distributed in different
micro-habitats, indicating the important governing abilities of the

nez et al., 2012).
micro-environmental spatial heterogeneity (Jime
4.2. Relative role of biotic interactions
The co-occurrence patterns of the soil mite communities
showed signicantly non-random for all plots. According to the
results of our null model analysis on the overall species matrix, a
signicantly aggregated spatial co-occurrence pattern was found in
all plots taking into account the C-score and V-ratio with the FE and
FP algorithms, whereas a signicantly segregated spatial cooccurrence pattern was only detected in Plots II and III according
to the C-score with the FF algorithm. Based on the pairwise null
model analysis, when the soil mite assemblage was segregated
according to the C-score with the FF algorithm (Plots II and III),
there were more segregated species pairs than aggregated species
pairs. Additionally, when the soil mite assemblages were aggregated according to the C-score with the FE algorithm, there were
more aggregated species pairs than segregated species pairs. The
co-occurring distribution of the observed signicant species pairs
was in line with the overall matrix based on the same null model

algorithm. However, few signicant negative species pairs were

detected based on the pairwise null model analysis using the
conservative criterion. The contribution of these negative species
pairs to the non-random community structure may be insignicant
due to dilution effects (Gotelli and Ulrich, 2010; Krasnov et al.,
2011). Moreover, the analysis of neutral model also implies a little
possible function of biotic interactions in community structuring.
What is more, the results of the environmental niche partitioning
suggested a common environmental structuring constraint rather

ttir et al.,
than interspecic competition (Leibold, 1998; Ingimarsdo

nez et al., 2012). Greater micro-variations in the envi2012; Jime
ronment allow for species co-existence, hence environmental
process might predominate over the contribution of biotic interactions. Actually, oribatid mite species are belong to three or four
trophic levels (Schneider et al., 2004; Maraun et al., 2011). Within
the same mite assemblages, true decomposers and predators have
been demonstrated and others occupy intermediate positions
(Schneider et al., 2004; Maraun et al., 2011; Caruso et al., 2012b).
Additionally, predators also control community structures (Wardle,
2002, 2006). Thus we suggest that the stable-isotope method
should be performed in the future (Schneider et al., 2004; Maraun
et al., 2011). We also suggest that a functional trait-based approach
(Bello et al., 2013; Liu et al., 2013; Algarte et al., 2014; Michel and
Knouft, 2014) and a phylogenetic method (Cavender-Bares et al.,
2009) should also be carried out.

Fig. 3. Results based on the meta-analysis evaluating deviations from predictions of the neutral model. The null hypothesis is that mean observed dissimilarities (Jaccard
dissimilarity index) between any two samples are the same as those expected under ecological neutrality. Thus, a positive effect size (observed mean dissimilarity e expected mean
dissimilarity) indicates that dissimilarity is higher than predicted (divergence), while a negative effect size indicates that dissimilarity is lower than predicted (convergence). The
null hypothesis corresponds to the vertical line at zero (neutrality). Error bars are 95% condence limits. q is neutral diversity (Hubbell, 2001). m is the average immigration
parameters in terms of migration rate (calculated by averaging the parameter estimate obtained for each local community, after Etienne, 2009). For the two other neutral model
parameters (J-community size; S-observed richness), please see Table 1. ***P < 0.001. (a) e Plots I, II, III and the Mean plot were considered during meta-analysis process. (b) e Plots
I, II and III were considered during meta-analysis process.

M. Gao et al. / Soil Biology & Biochemistry 79 (2014) 68e77

The relative contributions of spatial factors, environmental

ltering and biotic interactions in soil animal community structuring vary depending upon the spatial scales and study objects. At
the landscale scale (104  2
105 m) (Hortal et al., 2010),

ttir et al. (2012) found collembolan and oribatid species
Ingimarsdo
avoid each other, but emphasized the contribution of spatial and
environmental ltering. At the local scale (103e104 m) (Hortal et al.,
2010), spatial patterns and environmental factors (Caruso et al.,
2012b) and biotic interactions (especially interspecic competition) (Caruso et al., 2013) are important drivers for micro-soil animal communities. At the small scale (101e103 m) (Hortal et al.,

nez et al., 2011, 2012) and
2010), soil environmental ltering (Jime
biotic interactions (Nachman and Borregaard, 2010) permit species
to co-exist. At the ne scale (<101 m) (Ettema and Wardle, 2002;
Hortal et al., 2010), our study showed that both spatial and environmental processes govern co-existence assemblages, with little
evidence being found for the contribution of biotic interactions.
According to our results, the underlying processes at ne scale
seem complicated and signicant. During the processes of identifying the rules of community structuring at regional or local scales,
the underlying processes at the ne scales should not be ignored.
Despite a density sampling strategy and an above/below-ground
environmental factors collecting design, most (about 90% on
average) of the community composition remained unexplained.
Performing comparisons and interpreting results should therefore
be made with care, since pure spatial and environmental variables
can be confused by different sources of errors (Smith and
Lundholm, 2010). For example, pure spatial patterns explained by
dispersal limitation might simply result from unmeasured environmental variables (Smith and Lundholm, 2010; Anderson et al.,
2011). The effects of pure environmental patterns are also related
to niche-mediated competition (Caruso et al., 2012b) and the extent
of measured variables (Jones et al., 2008). Although there are critiques about the ability of variation partitioning to identify the
relative roles of environmental and spatial variables (Tuomisto and
Ruokolainen, 2008; Gilbert and Bennett, 2010), it is helpful for
uncovering community pattern (Anderson et al., 2011). Some
publications have shown that it can be efciently applied (DinizFilho et al., 2012) and it has been widely performed for this purpose (Caruso et al., 2013; Sokol et al., 2013; Michel and Knouft,
2014). At the ne-scale, the unexplained variation might result
from those unmeasured and important environmental factors
(Borcard et al., 2004), such as vertical distributions (soil depth and
structure) (Anderson and Hall, 1977), through its threedimensional structure variability, which may provide high niche
differentiation and the opportunity to segment resources (Wardle,

nez et al., 2006). The unexplained variation might also
2002; Jime
arise from unconsidered temporal variations, which could also
provide important information for identifying underlying mechanisms. Opportunities for species co-existence in a community may
be increased by temporal segregation (Chase and Leibold, 2003;
Dumbrell et al., 2011). We therefore suggest that future studies of
community structuring should better consider both spatial and
temporal variations in environmental factors.
Collectively, these results suggest that both spatial factors and
environmental ltering were important drivers in the ne-scale
(5 m) structuring of a soil mite community in the temperate deciduous forest in northeastern China, whereas biotic interactions
were less inuential in the observed pattern.
Acknowledgments
We thank Pierre Legendre, Jiangshan Lai and Xiangcheng Mi for
their assistance in the MEMs and variation partitioning analysis.

Jime

nez for his assistance with the
We thank Juan-Jose

75

environmental niche overlap analysis. We thank Xiaoguang Du for

his assistance with neutral model analysis. We thank Judson Mark
for his assistance in English polishing. We thank managers of the
Maoershan Ecosystem Research Station for the convenience they
provided. We also thank the anonymous reviewers. This study was
supported by the National Natural Sciences Foundation of China
(grant nos. 41101049, 41471037, 40601047, 41371072, 41430857 and
31200331) and by the China Postdoctoral Science Foundation
(grant no. 2012M511361).

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.soilbio.2014.09.003.

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