sustainability
Article
Relationships between Soil Crust Development and
Soil Properties in the Desert Region of North China
Jiping Niu 1 , Kai Yang 2 , Zejun Tang 1, * and Yitong Wang 1
1
2
*
College of Water Resources and Civil Engineering, China Agricultural University, Beijing 100083, China;
[email protected] (J.N.); [email protected] (Y.W.)
Advanced Materials Institute, Shandong Academy of Sciences, Jinan 250014, China; [email protected]
Correspondence: [email protected]
Academic Editor: Mary J. Thornbush
Received: 2 March 2017; Accepted: 27 April 2017; Published: 3 May 2017
Abstract: This study investigated the effects of soil crust development on the underlying soil properties.
The field sampling work was conducted in June 2016 in the Hobq Desert in Inner Mongolia, North China.
Soil crust samples and 0–6, 6–12, 12–18, 18–24, and 24–30 cm deep underlying soil samples were
taken from five representative areas of different soil crust development stages. All samples were
analyzed for physicochemical properties, including water content, bulk density, aggregate content,
organic matter content, enzyme activities, and microbial biomass carbon and nitrogen. The results
showed that the thickness, water content, macro-aggregate (>250 µm) content, organic matter
content, microbial biomass, and enzyme activities of the soil crusts gradually increased along the
soil crust development gradient, while the bulk density of the soil crusts decreased. Meanwhile,
the physicochemical and biological properties of the soils below the algal and moss crusts were
significantly ameliorated when compared to the physical crust. Moreover, the amelioration effects
were significant in the upper horizons (∼0–12 cm deep) and diminished quickly in the deeper
soil layers.
Keywords: crust type; soil depth; physicochemical properties; enzyme; microbial biomass carbon
and nitrogen
1. Introduction
Soil degradation and desertification control is of great importance to protecting ecological balance
and agricultural development in desert regions. Soil crusts, including physical crusts and biological
crusts, are widely distributed in arid and semi-arid regions. Physical crusts are formed from the action
of water and wind on soil particles on the surface of bare areas [1]. Physical crusts can further develop
into biological crusts which are mainly composed of bacteria, fungi, algae, lichens, mosses, and other
cryptogams [2]. Soil crusts can support surface ecosystems due to their strong ecological adaptability.
The importance of soil crusts in ecosystem lies in the development of soil crust and conversion of
soil nutrition by ameliorating physicochemical and biological properties. Specifically, in the vertical
direction, soil crusts contribute to the regulation of water content and ecological promotion of nutrient
cycle and, therefore, influence soil physicochemical properties, enzyme activities, microbial biomass
carbon and nitrogen [3]. In the horizontal direction, soil crusts improve the resistance to wind erosion of
the underlying soil due to their stable layered structure and, therefore, provide appropriate conditions
for the growth of sand vegetation [4]. The study on soil crusts combining geoscience and biology has
become a research focus and leading edge in arid and semi-arid regions.
In arid and semi-arid desert regions, water content is the dominant factor influencing the sandy
ecosystem restoration. For example, Li et al. [5] found that the spatial variability of rainfall infiltration
depth within the various soil layers significantly influenced the ecological development of soil crusts
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in the Tengger Desert in Inner Mongolia, North China. The authors also found that the soil crusts
influenced the soil water environment by reducing the infiltration and evaporation of precipitation
and, therefore, resulted in a vegetation change from shrubs to herbs. Aggregates and organic matter
are important soil components. Aggregates are the place where organic carbon exists. Organic matter
provides nutrient sources and energy for plant growth and microbial activities. Both aggregates and
organic matter influence the stability of soil structure, as well as soil anti-erodibility and fertility and
plant growth [6,7]. Numerous studies have demonstrated that the development of biological soil crusts
can increases aggregate stability [8], organic matter content [9], and soil fertility [10,11].
Microbial biomass carbon and nitrogen are the most active and variable parts of soil organic
matter [12]. Liang et al. [13] demonstrated that microbial biomass carbon and nitrogen were sensitive to
planting, fertilization and other management measures. Issa et al. [14] reported that the soil crusts with
porous organic bodies increased soil porosity water and nutrient retention. Yu and Steinberger [15]
found that the microbial biomass was recorded relatively higher in the two upper (0–20 cm) layers
than the deeper layers (20–50 cm). Enzymes are the most active biocatalyst in the material cycle
and energy flow of ecosystems, influencing all of the biochemical processes in soil and most organic
carbon species [16,17]. To be specific, alkaline phosphatase can hydrolyze organophosphorus ester
into inorganic phosphate. Urease can promote the hydrolysis of urea into ammonia and, therefore,
supply nitrogen for plant growth and soil microbial activities. Protease can promote the hydrolysis of
proteins into amino acids. Peroxidase is involved in the soil organic carbon cycle and transformation.
The desert region of the Hobq Desert in Inner Mongolia, North China was chosen as the study
area due to the abundant soil crusts and extreme ecological environment. Many studies have examined
the effects of soil crusts on soil hydraulic conductivity [18], soil structure [8], microbial biomass [19],
enzyme activities [20,21], and succession process [1] in this region. However, to our knowledge,
few studies have investigated how different types of soil crusts and vegetation covers influence
the spatial variations in underlying soil properties, which can indicate the soil quality. In addition,
the relationships between soil physicochemical properties, microbial biomass and enzyme activities of
different types of soil crusts remain unknown in the Hobq Desert.
This study explored the effects of different physical and biological crusts on the physicochemical
characteristics, enzyme activities, and microbial biomass of the underlying soils in the Hobq Desert,
aiming at providing a reference for vegetation restoration and soil improvement in the desert region of
North China. In contrast to previous studies where the 0–5 cm deep underlying topsoil was usually
collected, 0–30 cm deep underlying soil samples were collected in this study to investigate the effects
of the organic matter accumulation and microbial activities in the upper soil layers. The sampling
depth was designed according to the root depth (∼30 cm) of Artemisia ordosica which dominates the
study area.
2. Material and Methods
2.1. Study Area
The Hobq Desert is located in Inner Mongolia, North China. It has a desert area of 13,358 km2 ,
ranking as the 7th largest desert in China. The field sampling work was conducted in the southern part
of the desert (40◦ 160 N–40◦ 390 N, 107◦ 450 E–109◦ 500 E, 1020–1097 m asl). The desert is located in a typical
semi-arid temperate continental monsoonal climate zone. According to the Chinese International
Exchange Stations Surface Climate Standard Values Monthly Dataset (1971–2000) (weather station No.:
53463; location: 40◦ 490 N, 111◦ 410 E, 1063 m asl) (National Meteorological Information, 2005), the mean
annual temperature is 6.1 ◦ C, and the lowest and highest monthly mean temperatures are −34.5 ◦ C
and 40.2 ◦ C, respectively. The mean annual precipitation is 250 mm, falling predominantly during
summer, and the mean annual pan evaporation is 2160 mm. The mean annual wind speed is 3.9 m/s,
and there is a wind erosion period often occurring from March to May with a wind speed up to 30
m/s.
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The experimental soil is sandy, weak salt wet cambisol, and arid sandy entisol. A range of
engineering measures such as enclosure and afforestation have been undertaken by the national and
local governments to control the local desertification and restore vegetation cover. The Hobq Desert is
currently covered by drought-tolerant sand vegetation mainly consisting of Agriophyllum squarrosum,
Elymus dahuricus, Salsola collina, Sophora alopecuroides, Astragalus adsurgens, Artemisia ordosica,
and Aneurolepidium chinense. Physical and biological soil crusts have been formed between the bare
sand dune and vegetation. Chen and Duan [22] have recently reported that the local biological soil
crusts include algal crust, lichen crust, algal-lichen mixed crust, and moss crust. The dominant species
composing the local biological soil crusts are Microcoleus vaginatus, Collema tenax, and Byum argenteum.
2.2. Field Sampling
Vegetation was planted in the study area in the mid-1980s as part of the local desertification control
project. Soil crusts have been widely formed on the top of the sandy soil in the region. According
to our field survey, five types of soil crusts were selected. For each type of soil Crust, a sampling
strip 1 m wide and 20 m long was designed. Along each sampling strip, three sampling points were
selected to determine soil properties based on the same topography and soil type. Our field survey
demonstrated that within the sampling stripes the mean plant height and crown width of the dominant
Artemisia ordosica were 35 and 40 cm, respectively. The mean vegetation cover was estimated to be
∼50%.
At each sampling point, the soil crust sample and 0–6, 6–12, 12–18, 18–24, and 24–30 cm deep
underlying soil samples were collected in June 2016. Briefly, the soil crust was carefully separated
from the underlying soil using a shovel. Next the 30 cm deep undisturbed soil column sample was
collected using an organic glass sampling tube. The soil column sample was then separated into
subsamples of different depths as aforementioned. A total of 75 underlying soil samples were collected.
The characteristics of the five soil crust samples are shown in Table 1.
Table 1. Characteristics of the soil crust samples.
Sample No.
Dominant Vegetation
Crust Type
Color
Thickness (cm)
1
2
3
Artemisia Ordosica
Artemisia Ordosica
Artemisia Ordosica
Artemisia Ordosica and
Eragrostis Poaeoides
Artemisia Ordosica and
Eragrostis Poaeoides
Physical Crust
Algal Crust
Moss Crust
Light-Colored
Dull Gray
Yellow Green
0.41
0.62
1.53
Algal Crust
Brown
0.57
Moss Crust
Yellow Green
1.72
4
5
2.3. Laboratory Analyses
All soil crust samples and underlying soil samples were air-dried and passed through a 2 mm
sieve to remove roots and other debris. Crust thickness was measured using a Vernier caliper. Water
content was determined by the oven-drying method. Bulk density was determined by the cutting ring
method. Each soil sample was separated into three fractions, viz., <53, 53–250 and >250 µm, by the
wet sieving method as described in [23]. Organic matter content was determined by the potassium
dichromate-sulfuric acid oxidation method as described in [24]. Microbial biomass carbon and nitrogen
were determined by the chloroform-fumigation extraction method as described in [25].
Enzymes activities were determined by the methods as described in References [26]. For alkaline
phosphatase, 1 g soil and 0.25 mL toluene were incubated in 1 mL nitro phenolic sodium phosphate
and 4 mL borate buffer at pH = 11 at 37 ◦ C for 1 h. The mixture was then filtered. The amount of
phenol released from the filtrate was estimated based on the color reaction. For urease, 5 g soil was
mixed with 1 mL toluene, 10 mL 10% urea solution and 20 mL citrate solution at pH = 6.7 at 37 ◦ C for
24 h. The amount of released ammonium was colorimetrically determined using a spectrophotometer
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soil was mixed
with
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1 mL toluene, 10 mL 10% urea solution and 20 mL citrate solution at pH = 6.7
4 of at
15
37 °C for 24 h. The amount of released ammonium was colorimetrically determined using a
spectrophotometer at 578 nm. For protease, 5 g soil and 25 mL sodium casein were incubated in 25
at 578 nm. For protease, 5 g soil and 25 mL sodium casein were incubated in 25 mL 50 mol/L tris
mL 50 mol/L tris buffer at pH = 8.1 at 50 °C for 2 h. 5 mL 33% folin solution was then added. The
buffer at pH = 8.1 at 50 ◦ C for 2 h. 5 mL 33% folin solution was then added. The protease activity was
protease activity was colorimetrically quantified using a spectrophotometer at 700 nm. For
colorimetrically quantified using a spectrophotometer at 700 nm. For peroxidase, 2 g soil and 5 mL
peroxidase, 2 g soil and 5 mL 0.3% hydrogen peroxide solution were added to a 100 mL conical flask
0.3% hydrogen peroxide solution were added to a 100 mL conical flask with 40 mL deionized water.
with 40 mL deionized water. After shaking and filtration, the filtrate was titrated to the pink end
After shaking and filtration, the filtrate was titrated to the pink end point with 0.5 mol/L potassium
point with 0.5 mol/L potassium permanganate. The peroxidase activity was then calculated using
permanganate. The peroxidase activity was then calculated using the following formula: (A–B)*T,
the following formula: (A–B)*T, where A is the dosage of potassium permanganate used to titrate
where A is the dosage of potassium permanganate used to titrate the 25 mL original hydrogen peroxide
the 25 mL original hydrogen peroxide solution; B is the dosage of potassium permanganate used to
solution; B is the dosage of potassium permanganate used to titrate the 25 mL soil filtrate solution; and
titrate the 25 mL soil filtrate solution; and T is the correction value.
T is the correction value.
2.4. Data Analyses
2.4. Data Analyses
IBM® SPSS® Statistics 20 (Statistical Product and Service Solutions, IBM Company, USA) was
IBM® SPSS® Statistics 20 (Statistical Product and Service Solutions, IBM Company, USA) was
used to analyze the data. Significant differences among soil physicochemical properties, enzymes
used to analyze the data. Significant differences among soil physicochemical properties, enzymes
activities, microbial biomass carbon and nitrogen were compared by the LSD test at a significance
activities, microbial biomass carbon and nitrogen were compared by the LSD test at a significance
level of 0.05. Results were presented as mean value ± standard deviation. Correlation analysis was
level of 0.05. Results were presented as mean value ± standard deviation. Correlation analysis was
conducted at significance levels of 0.01 and 0.05, respectively.
conducted at significance levels of 0.01 and 0.05, respectively.
3. Results
3.
Results
3.1. Soil Physicochemical Properties
The water
watercontents
contentsofofthe
the
five
crusts
underlying
soil layers
andsample)
layers
five
soilsoil
crusts
andand
theirtheir
underlying
soil layers
(crust (“crust
and layers
sample”)
Except
and
1, thecontents
water contents
crust
and 2,
layers
are
shownare
in shown
Figure in
1. Figure
Except 1.for
crust for
andcrust
layers
1,layers
the water
of crustof
and
layers
3, 4,
2, 3, 54,first
andincreased
5 first increased
with and
depth
and peaked
at the of
depth
6–12
and
then decreased
with
and
with depth
peaked
at the depth
6–12ofcm
andcm
then
decreased
with depth.
depth. Regarding
the Artemisia
the contents
water contents
of crusts
were and
0.9%1.2%,
and
Regarding
the Artemisia
ordosicaordosica
cover, cover,
the water
of crusts
2 and 23 and
were3 0.9%
1.2%, respectively.
The values
up to
2.4%
and
3.0%, respectively,
at the
of and
6–12then
cm
respectively.
The values
reachedreached
up to 2.4%
and
3.0%,
respectively,
at the depth
of depth
6–12 cm
and
then
dropped
to
1.9%
and
1.2%,
respectively,
at
the
depth
of
24–30
cm.
Regarding
the
Artemisia
dropped to 1.9% and 1.2%, respectively, at the depth of 24–30 cm. Regarding the Artemisia ordosica
ordosica
and Eragrostis
waterofcontents
crusts
4 and
were
0.6%
and 2.0%,
and
Eragrostis
poaeoides poaeoides
cover, thecover,
waterthe
contents
crusts 4of
and
5 were
0.6%5and
2.0%,
respectively.
respectively.
The values
up3.2%,
to 0.9%
and 3.2%, respectively,
depth
of 6–12
and then
The
values reached
up toreached
0.9% and
respectively,
at the depth at
of the
6–12
cm and
thencm
dropped
to
dropped
to
0.7%
and
1.4%,
respectively,
at
the
depth
of
24–30
cm.
In
contrast,
there
was
an
0.7% and 1.4%, respectively, at a depth of 24–30 cm. In contrast, there was an increasing trend in the
increasing
trend
in theand
water
content
ofdepth.
crust and
layers 1atwith
depth.ofMoreover,
the depth
of <24
water
content
of crust
layers
1 with
Moreover,
the depth
<24 cm theatwater
contents
of
cm the
water
contents
and layers
3,corresponding
and 5 were higher
theand
corresponding
value
of
crust
and
layers
2, 3, andof5 crust
were higher
than2,
the
valuethan
of crust
layers 1, while
at the
crust and
layerscm
1, these
while values
at the depth
ofquite
24–30similar.
cm these values became quite similar.
depth
of 24–30
became
Water contents(%)
0.5
1.0
1.5
2.0
2.5
3.0
3.5
Crust
Depth(cm)
0-6
6-12
12-18
18-24
24-30
Crust&layers sample 1
Crust&layers sample 2
Crust&layers sample 3
Crust&layers sample 4
Crust&layers sample 5
Figure 1.
1. The water contents of the five crust and layers samples at different depths.
Figure
The bulk density of the five soil crusts and their underlying
underlying soil
soil layers
layers are
are shown
shown in
in Figure
Figure 2.
2.
3 ) was
3) was
g/cm
higher
thanthan
thosethose
of crusts
2, 3, 4,2,and
The bulk
bulk density
density ofofcrust
crust1 1(1.4
(1.4
g/cm
higher
of crusts
3, 4,5 (range
and 5 0.9–1.3
(range
0.9–1.3 g/cm3 ). Moreover, the bulk density of the algal crust (e.g., crusts 2 and 4) was higher than that
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9, 725
725
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55 of
of 15
15
g/cm3). Moreover, the bulk density of the algal crust (e.g., crusts 2 and 4) was higher than that of the
3). Moreover,
moss
crust (e.g.,the
crusts
and 5).ofThe
abovecrust
trend
was
also 2found
the corresponding
g/cm
bulk 3density
the algal
(e.g.,
crusts
and 4)among
was higher
than that of thesoil
of
the
moss
(e.g.,
3 In
and
5). The
above
was
also
found
among
thecorresponding
corresponding
layers
at crust
the same
depth.
all trend
thetrend
bulk
density
of the
five crust
and layers samples
moss
crust
(e.g.,
crustscrusts
3 and
5).addition,
The
above
was
also
found
among
the
soil
tended
to same
increase
withIndepth.
layers
at
addition,
all the
bulkbulk
density
of theoffive
layers
tended
at the
the
samedepth.
depth.
In
addition,
all the
density
thecrust
five and
crust
and samples
layers samples
to
increase
with depth.
tended
to increase
with depth.
3
0.0
0.0
Crust
Crust
0-6
Depth(cm)
0.4
Bulk density(g/cm )
0.8
1.2
1.6
2.0
2.4
2.8
3.2
3
Bulk density(g/cm )
a
0.8
1.2
1.6
2.0
2.4
2.8
3.2
a
b
0-6
Depth(cm)
0.4
6-12
6-12
12-18
12-18
18-24
18-24
24-30
24-30
a
b
a
a
a
b
b
b
b
c b
c
c
b
c
a
c
a
c
ab
ab
a
b
a
ab
a
ab ab
b
ab
ab
a
b
ab
ab
a
ab a
ab
a
a
b
a
a
a
a
ab
babc
ab
a
b
ab
abc
ab
b
Crust&layers sample 1
Crust&layers sample 2
Crust&layers
sample
1 3
Crust&layers
sample
Crust&layers
sample
2 4
Crust&layers
sample
Crust&layers
sample
3 5
Crust&layers
sample
Crust&layers sample 4
Crust&layers sample 5
Figure 2. The bulk density of the five crust and layers samples at different depths. Data with the
same2.
at
the
same depth
are
not
significantly
different
atdifferent
pat= 0.05
by
thedepths.
LSD
test.
Figure
2.letter
Thebulk
bulk
density
the
five
crust
layers
samples
different
Data
with
the
Figure
The
density
ofofthe
five
crust
andand
layers
samples
at
depths.
Data
with the
same
same
letter
at
the
same
depth
are
not
significantly
different
at
p
=
0.05
by
the
LSD
test.
letter at the same depth are not significantly different at p = 0.05 by the LSD test.
The aggregate contents of the five soil crusts and their underlying soil layers are shown in
Figure
3. The <53 contents
μm aggregate
of crust
(88%)their
was underlying
higher thansoil
those
of crusts
2, 3, 4, and
The aggregate
of thecontent
five soil
crusts1 and
layers
are shown
in 5
The aggregate contents of the five soil crusts and their underlying soil layers are shown in Figure 3.
(range
24%–79%).
both crusts
1 and
2 were
dominated
by those
the <53
μm aggregates
while
Figure
3. The
<53 μm Moreover,
aggregate content
of crust
1 (88%)
was
higher than
of crusts
2, 3, 4, and
5
The <53 µm aggregate content of crust 1 (88%) was higher than those of crusts 2, 3, 4, and 5 (range
crusts
3
and
5
were
dominated
by
the
53–250
and
>250
μm
aggregates,
respectively.
There
was
(range 24%–79%). Moreover, both crusts 1 and 2 were dominated by the <53 μm aggregates while a
24–79%). Moreover, both crusts 1 and 2 were dominated by the <53 µm aggregates, while crusts 3
relatively
of <53
than
theμm
contents
of 53–250
and >250 There
μm aggregates
crusts
3 and higher
5 werecontent
dominated
byμm
theaggregates
53–250 and
>250
aggregates,
respectively.
was a
and 5 were dominated by the 53–250 and >250 µm aggregates, respectively. There was a relatively
presenthigher
in crustcontent
4. Except
for crust
and layers than
4, thethe
<53contents
μm aggregate
content
of theμm
soilaggregates
layers below
relatively
of <53
μm aggregates
of 53–250
and >250
higher content of <53 µm aggregates than the contents of 53–250 and >250 µm aggregates present
crust in
1 was
thanfor
those
the layers
corresponding
below
crustsof
2, the
3, 4,soil
andlayers
5 at the
depth
present
crusthigher
4. Except
crustofand
4, the <53soil
μmlayers
aggregate
content
below
in crust 4. Except for crust and layers 4, the <53 µm aggregate content of the soil layers below crust
of 6–24
In contrast,
the soil
layers
below crustsoil
4 had
the below
highestcrusts
<53 μm
contents
at the
crust
1 wascm.
higher
than those
of the
corresponding
layers
2, 3,aggregate
4, and 5 at
the depth
1 was higher than those of the corresponding soil layers below crusts 2, 3, 4, and 5 at the depth of
depthcm.
of In
0–6contrast,
and 24–30
soil layers
below
crust 1contents
were dominated
of 6–24
thecm,
soil respectively.
layers below Additionally,
crust 4 had thethe
highest
<53 μm
aggregate
at the
6–24 cm. In contrast, the soil layers below crust 4 had the highest <53 µm aggregate contents at the
by the
<53and
μm 24–30
aggregates
at all the depths.
The soil the
layers
and 31 were
depth
of 0–6
cm, respectively.
Additionally,
soilbelow
layerscrusts
below2crust
were dominated
dominated by
depth of 0–6 and 24–30 cm, respectively. Additionally, the soil layers below crust 1 were dominated
depths The
(e.g.,soil
0–12
cm), below
while the
soil2layers
by the
the <53
<53 μm
μmaggregates
aggregatesat
atshallow
all the depths.
layers
crusts
and 3were
weredominated
dominatedby
bythe
by the <53 µm aggregates at all the depths. The soil layers below crusts 2 and 3 were dominated by
depths
(e.g.,
12–30
cm).
The
soil the
layers
were dominated
the>53
<53μm
μmaggregates
aggregatesatatdeep
shallow
depths
(e.g.,
0–12
cm),
while
soilbelow
layerscrust
were4dominated
by the by
the <53 µm aggregates at shallow depths (e.g., 0–12 cm), while the soil layers were dominated by the
μm aggregates
at all the
depths
forsoil
thelayers
depth
of 6–12
where
the dominant
>53the
μm<53
aggregates
at deep depths
(e.g.,
12–30 except
cm). The
below
crustcm
4 were
dominated
by
>53 µm aggregates at deep depths (e.g., 12–30 cm). The soil layers below crust 4 were dominated by the
fell into theatrange
of >53
μm. The
soilfor
layers
5 were
the >53 μm
theaggregates
<53 μm aggregates
all the
depths
except
thebelow
depthcrust
of 6–12
cmdominated
where thebydominant
<53 µm aggregates at all the depths except for the depth of 6–12 cm, where the dominant aggregates
aggregates
all the depths
dominant
of >250crust
μm 5aggregates
at deepby
depths
(e.g.,
aggregates
fellatinto
range ofwith
>53 aμm.
The soilamount
layers below
were dominated
the >53
μm12–
fell into the range of >53 µm. The soil layers below crust 5 were dominated by the >53 µm aggregates
30 cm). at all the depths with a dominant amount of >250 μm aggregates at deep depths (e.g., 12–
aggregates
at all the depths with a dominant amount of >250 µm aggregates at deep depths (e.g., 12–30 cm).
30 cm).
Aggregate content (%)
Aggregate content (%)
100
100
80
80
60
60
40
40
20
20
0
0
(a) Crust
(a) Crust
(b) 0–6 cm
(b) 0–6 cm
(c) 6–12 cm
(c) 6–12 cm
<53 μm
<53 μm
53–250
μm
53–250
μm>250 μm
1 2 3 4 5
1 Crust
2 3sample
4 5No.
Crust sample No.
1 2 3 4 5
1 Layer
2 3sample
4 5No.
Layer sample No.
Figure 3. Cont.
1 2 3 4 5
1 Layer
2 3sample
4 5No.
Layer sample No.
>250 μm
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2017,
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9, 725
66 of
of615
15
of 15
(d) (d)
12–18
cm cm
12–18
(e) (e)
18–24
cm cm
18–24
(f) 24–30
cm cm
(f) 24–30
Aggregate content (%)
Aggregate content (%)
100100
80 80
<53<53
μmμm
60 60
40 40
53–250
53–250
μmμm
20 20
>250
μmμm
>250
0 0
1 12 23 34 45 5
Layer
sample
No.No.
Layer
sample
1 12 23 34 45 5
Layer
sample
No.No.
Layer
sample
1 12 23 34 45 5
Layer
sample
No.No.
Layer
sample
Figure
3. The
The aggregate
aggregatecontents
contentsofofthe
thefive
fivecrust
crustand
andlayers
layerssamples
samples
different
depths.
Crust
Figure
3.
atat
different
depths.
(a)(a)
Crust
(b) (b)
Figure
3. The aggregate
contents of the
five crust
and layers
samples
at different
depths.
(a)
Crust
(b)
0–6
cm
(c)
6–12
cm
(d)
12–18
cm
(e)
18–24
cm
(f)
24–30
cm.
0–60–6
cm cm
(c) 6–12
cm
(d)
12–18
cm
(e)
18–24
cm
(f)
24–30
cm.
(c) 6–12 cm (d) 12–18 cm (e) 18–24 cm (f) 24–30 cm.
TheThe
organic
matter
contents
of the
fivefive
soilsoil
crusts
andand
their
underlying
soilsoil
layers
areare
shown
in in
organic
matter
contents
of the
crusts
their
underlying
layers
shown
organic
matter
contents
increased
with
soilsoil
from
Figure
4. The
crust
development
thethe
physical
crust
Figure
4. The
organic
matter
contents
increased
with
crust
development
from
physical
crust
g/kg
in
crust
1)
to
the
algae
crust
(5.3
g/kg
in
crust
2
and
g/kg
in
crust
4)
and,
finally,
to
(3.4(3.4
g/kg
in
crust
1)
to
the
algal
crust
(5.3
g/kg
in
7.5
g/kg
in
crust
4)
and,
finally,
g/kg in crust 1) to the algae crust (5.3 g/kg in crust 2 and 7.5 g/kg in crust 4) and, finally, the
to the
crust
(9.6(9.6
g/kg
inincrust
33and
17.6
g/kg
inin
crust
5).5).
InIn
contrast,
allall
thethe
organic
matter
contents
of of
moss
g/kg
crust
and
17.6
g/kg
organic
matter
contents
moss
crust
g/kg
in
crust
3 and
17.6
g/kg
incrust
crust
5).
Incontrast,
contrast,
all
the
organic
matter
contents
thethe
five
crust
and
layers
samples
tended
to
decrease
with
depth.
Except
for
crust
and
layers
1,
a1, a
of
five
crust
and
layers
samples
tended
to
decrease
with
depth.
Except
for
crust
and
layers
the five crust and layers samples tended to decrease with depth. Except for crust and layers 1,
conspicuous
decline
was
observed
in
the
organic
matter
contents
of
crust
and
layers
2,
3,
4,
and
5
at
a
conspicuous
decline
was
observed
in
the
organic
matter
contents
of
crust
and
layers
2,
3,
4,
and
5
conspicuous decline was observed in the organic matter contents of crust and layers 2, 3, 4, and 5 at
thethe
depth
of of
0–6
cm,cm,
while
only
a slight
decline
waswas
observed
at the
depth
of 6–30
cmcm
for
all
the
five
at
depth
while
only
a
slight
decline
was
observed
atthe
the
depth
6–30
cmfor
forall
allthe
thefive
the
depth
of 0–6
0–6
cm,
while
only
a slight
decline
observed
at
depth
ofof6–30
crust
and
layers
samples.
five
crust
and
layers
samples.
crust and layers samples.
0
0
2
4
2
Organic
matter(g/kg)
Organic
matter(g/kg)
8
6
8 10 10 12 12 14 14 16 16 18 18 20 20
6
4
a
a
ab
Crust
Crust
a
0-6 0-6
6-126-12
Depth(cm)
Depth(cm)
a
a
12-18
12-18
a
a
a
a
ab
a
a a
a a
a
ab
bc
ab
b ab
a
aa
a
a
a
a
ab
c
c
c
ab
a
a
a
ab
b
a
a
a
ab
c
b
b
a
a
a
a
24-30
24-30
a a
a
bc
a
a
18-24
18-24
a
a
ab
Crust
& layers sample 1
Crust
& layers sample
Crust
& layers sample 2
Crust
& layers sample
Crust
& layers sample 3
Crust
& layers sample
Crust
& layers sample 4
Crust
& layers sample
Crust
& layers sample 5
Crust
& layers sample
1
2
3
4
5
Figure 4. The organic matter contents of the five crust and layers samples at different depths. Data
Figure
4. The
organic
matter contents
of the
fivefive
crust
andand
layers
samples
at different
depths.
Data
Figure
4. The
organic
contents
of the
crust
layers
at different
depths.
Data
with
the same
letter
at thematter
same depth
are not
significantly
different
at samples
p = 0.05 by
the LSD test.
with
the
same
letter
at
the
same
depth
are
not
significantly
different
at
p
=
0.05
by
the
LSD
test.
with the same letter at the same depth are not significantly different at p = 0.05 by the LSD test.
3.2.
Enzyme Activities
Activities
3.2.3.2.
Enzyme
Enzyme Activities
The
activities
of
phosphatase,
urease,
protease,
and
peroxidase
in the
fivefive
soil soil
crusts
and
TheThe
activities
ofalkaline
alkaline
phosphatase,
urease,
protease,
and
peroxidase
in the
crusts
activities
of alkaline
phosphatase,
urease,
protease,
and
peroxidase
in the
five soil
crusts
their
underlying
soil
layers
are
shown
in
Figures
5–8,
respectively.
In
general,
all
the
enzyme
activities
andand
their
underlying
soilsoil
layers
areare
shown
in Figures
5–8,5–8,
respectively.
In general,
all all
thethe
enzyme
their
underlying
layers
shown
in Figures
respectively.
In general,
enzyme
increased
with soil crust
development
while decreased
with
depth.with
The enzymes
were
more active
activities
increased
with
soilsoil
crust
development
while
decreased
depth.
The
enzymes
were
activities
increased
with
crust
development
while
decreased
with
depth.
The
enzymes
were
in
biological
crusts
than
in
physical
crust.
For
example,
the
alkaline
phosphatase
activity
in
the
algal
more
active
in
biological
crusts
than
in
physical
crust.
For
example,
the
alkaline
phosphatase
more active in biological crusts than in physical crust. For example, the alkaline phosphatase
crust
(crusts
2 and
4)crust
and (crusts
moss crust
(crusts
3 and
5)crust
was 1.1–1.4-times
and
3.4–7.2-times
higher
than
activity
in the
algal
2 and
4) and
moss
(crusts
3 and
5) was
1.1–1.4-times
andand
3.4–3.4–
activity
in the
algal
crust (crusts
2 and
4) and
moss
crust
(crusts
3 and
5) was
1.1–1.4-times
7.2-times
higher
than
in
the
physical
crust
(crust
1).
In
the
0–30
cm
deep
soil
layers,
the
alkaline
7.2-times higher than in the physical crust (crust 1). In the 0–30 cm deep soil layers, the alkaline
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725
7 of 15
77 of
of 15
15
phosphatase
was,
again,
the
following
moss
crust
crust
>>
phosphatase
activity
was,1).
again,
in0–30
thecm
following
decreasing
order:
moss
crust >> algal
algal
crust
in
the physicalactivity
crust (crust
In thein
deep soildecreasing
layers, the order:
alkaline
phosphatase
activity
was,
physical
crust.
physical
crust.
again,
in the
following decreasing order: moss crust > algal crust > physical crust.
00
aa
Crust
Crust
aa
0-6
0-6
cc
aa
aa
aa
aa
6-12
6-12
bb
aa
aa
aa
bb
aa
aa
12-18
12-18
aa
bb
cc
aa
18-24
18-24
aa
Crust
Crust&
&layers
layers sample
sample 11
Crust
Crust&
&layers
layers sample
sample 22
Crust
Crust&
&layers
layers sample
sample 33
Crust
&
layers
sample
Crust & layers sample 44
Crust
&
layers
sample
Crust & layers sample 55
aa
bb
bb
aa
aa
24-30
24-30
25
25
aa
bb
aa
Depth(cm)
Depth(cm)
Alkaline
Alkaline phosphatase
phosphatase activity(mg/g)
activity(mg/g)
1100
15
20
15
20
55
aa
aa
bb
Figure
5.
Figure
Figure5.
5. The
The alkaline
alkaline phosphatase
phosphatase activity
activity of
of the
the five
five crust
crust and
and layers
layers samples
samples at
at different
different depths.
depths.
Data
Data
with
the
same
letter
at
the
same
depth
are
not
significantly
different
0.05
by
the
LSD
test.
Datawith
withthe
thesame
sameletter
letterat
atthe
thesame
samedepth
depthare
arenot
notsignificantly
significantlydifferent
differentatat
atppp===0.05
0.05by
bythe
theLSD
LSDtest.
test.
00
Urease
Urease activity(mg/g)
activity(mg/g)
10
15
10
15
55
20
20
aa
bb
Crust
Crust
bb
aa
bb
Depth(cm)
Depth(cm)
aa
bb
aa
bb
aa
ab
ab
aa
24-30
24-30
aa
bb
aa
bb
aa
bb
aa
18-24
18-24
bb
bb
aa
12-18
12-18
bb
bb
aa
6-12
6-12
bb
cc
aa
0-6
0-6
25
25
aa
bb
Crust
Crust&
&layers
layers sample
sample 11
Crust
Crust&
&layers
layers sample
sample 22
Crust
Crust&
&layers
layers sample
sample 33
Crust
Crust&
&layers
layers sample
sample 44
Crust
Crust&
&layers
layers sample
sample 55
Figure
Figure
6.
The
urease
activity
of
the
five
crust
and
layers
samples
at
different
depths.
Data
with
the
Figure6.
6. The
The urease
urease activity
activity of
of the
thefive
fivecrust
crustand
andlayers
layerssamples
samplesat
atdifferent
differentdepths.
depths. Data
Data with
with the
the
same
same
letter
at
the
same
depth
are
not
significantly
different
at
0.05
by
the
LSD
test.
sameletter
letterat
atthe
thesame
samedepth
depthare
arenot
notsignificantly
significantlydifferent
differentat
atppp===0.05
0.05by
bythe
theLSD
LSDtest.
test.
00
10
10
20
20
Protease
Protease activity(mg/g)
activity(mg/g)
30
40
30
40
aa
Crust
Crust
bb
aa
0-6
0-6
Depth(cm)
Depth(cm)
6-12
6-12
aa
aa
24-30
24-30
aa
aa
aa
ab
ab
aa
aa
aa
aa
aa
70
70
bb
bb
cc
bb
aa
bb
12-18
12-18
60
60
aa
aa
aa
18-24
18-24
aa
50
50
ab
ab
cc
aa
bb
aa
bb
Crust
Crust&
&layers
layers sample
sample 11
Crust
Crust&
&layers
layers sample
sample 22
Crust
Crust&
&layers
layers sample
sample 33
Crust
Crust&
&layers
layers sample
sample 44
Crust
Crust&
&layers
layers sample
sample 55
Figure
Figure
7.
The
protease
activity
of
the
five
crust
and
layers
samples
at
different
depths.
Data
with
the
Figure7.
7.The
Theprotease
proteaseactivity
activityof
ofthe
thefive
fivecrust
crustand
andlayers
layerssamples
samplesat
atdifferent
differentdepths.
depths.Data
Datawith
withthe
the
same
same
letter
at
the
same
depth
are
not
significantly
different
at
0.05
by
the
LSD
test.
sameletter
letterat
atthe
thesame
samedepth
depthare
arenot
notsignificantly
significantlydifferent
differentat
atppp===0.05
0.05by
bythe
theLSD
LSDtest.
test.
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8 of 15
88ofof15
15
0.0
0.0
0.4
0.4
0.8
0.8
Peroxidase
Peroxidaseactivity(mg/g)
activity(mg/g)
1.2
1.6
2.0
2.4
1.2
1.6
2.0
2.4
aa
3.2
3.2
abab
Crust
Crust
abab
aa
0-6
0-6
aa
6-12
6-12
abab
12-18
12-18
aa
abab
bb
abab
abab
bb
bb
aa
24-30
24-30
abab
bb
cc
aa
bb
18-24
18-24
4.0
4.0
bcbc
cc
aa
3.6
3.6
abab
bb
bb
aa
Depth(cm)
Depth(cm)
2.8
2.8
aa
abab
bb
bb
Crust&
layers
Crust&
layerssample
sample1 1
Crust&
layers
Crust&
layerssample
sample2 2
Crust&
layers
Crust&
layerssample
sample3 3
Crust&
layers
Crust&
layerssample
sample4 4
Crust&
layers
Crust&
layerssample
sample5 5
Figure
8.8.The
The
five
crust
and
layers
samples
at at
different
depths.
Data
with
the
Figure
activity
ofofthe
the
five
crust
and
layers
samples
depths.
Data
with
Figure8.
Theperoxidase
peroxidaseactivity
activityof
the
five
crust
and
layers
samples
atdifferent
different
depths.
Data
with
same
letter
at
the
same
depth
are
not
significantly
different
at
p
=
0.05
by
the
LSD
test.
the
same
letter
at
the
same
depth
are
not
significantly
different
at
p
=
0.05
by
the
LSD
test.
the same letter at the same depth are not significantly different at p = 0.05 by the LSD test.
3.3.
3.3.
Microbial
Biomass
Carbon
and
Nitrogen
Contents
3.3.Microbial
MicrobialBiomass
BiomassCarbon
Carbonand
andNitrogen
NitrogenContents
Contents
Soil
Soil
microbial
biomass,
defined
as
the
living
microbial
component
of
the
soil
by
[27],
is
the
Soil microbial
microbial biomass,
biomass, defined
defined as
as the
the living
living microbial
microbial component
component of
of the
the soil
soil by
by [27],
[27], is
is the
the
nutrients
nutrients
and
energy
pool
that
provides
the
conditions
for
soil
biochemical
processes,
thus
being
nutrientsand
andenergy
energypool
poolthat
thatprovides
providesthe
theconditions
conditionsfor
forsoil
soilbiochemical
biochemicalprocesses,
processes,thus
thusbeing
being
frequently
soil
fertility
and
biological
activity.
frequently
proposedas
asan
anindicator
indicatorto
toevaluate
evaluate
soil
fertility
and
biological
activity. The microbial
frequentlyproposed
indicator
to
evaluate
soil
fertility
and
biological
activity.
The
microbial
and
contents
the
five
soil
biomass
andbiomass
nitrogencarbon
contents
ofnitrogen
the five soil
crustsof
and
their
soil
layers
are shown
Thecarbon
microbial
biomass
carbon
and
nitrogen
contents
of
the
fiveunderlying
soilcrusts
crustsand
andtheir
theirunderlying
underlying
soil
layers
shown
in
99and
10,
The
biomass
carbon
nitrogen
in
Figures
and
10, respectively.
microbial
biomass carbon
and nitrogen
contents
of and
the
soil
layers9are
are
shown
inFigures
FiguresThe
and
10,respectively.
respectively.
Themicrobial
microbial
biomass
carbon
andbiological
nitrogen
contents
of
the
biological
crusts
(crusts
2,
3,
4,
and
5)
were
higher
than
those
of
the
physical
crust
crusts
(crusts
2, 3,biological
4, and 5) were
higher
than
of the
crust than
(crustthose
1). There
was
a decreasing
contents
of the
crusts
(crusts
2, those
3, 4, and
5)physical
were higher
of the
physical
crust
(crust
There
was
in
microbial
biomass
carbon
contents
of
trend
in
the microbial
biomasstrend
carbon
and
nitrogen
contents
of the
five and
crust
and layers
samples
(crust1).
1).all
There
wasaadecreasing
decreasing
trend
inall
allthe
the
microbial
biomass
carbon
andnitrogen
nitrogen
contents
of
the
crust
layers
samples
with
(p(pcover,
<< 0.05).
the
Artemisia
ordosica
cover,
the
with
depth
(p <and
0.05).
Under
the Artemisia
ordosica
theUnder
microbial
and
nitrogen
the five
five
crust
and
layers
samples
with depth
depth
0.05).
Under
the biomass
Artemisiacarbon
ordosica
cover,
the
microbial
biomass
carbon
contents
the
moss
and
underlying
soil
contents
the moss
crust and
(crust
3) and underlying
were
higher
than
those
of the algal
microbialof
biomass
carbon
and nitrogen
nitrogen
contents of
ofsoil
thelayers
moss crust
crust (crust
(crust 3)3)
and
underlying
soil
layers
were
higher
than
of
algal
(crust
2)2) and
underlying
soil
layers
atat the
same
crust
and underlying
layers
at crust
the
same
depth.
Similarly,
under
the
Artemisia
ordosica
layers(crust
were2)
higher
than those
thosesoil
of the
the
algal
crust
(crust
and
underlying
soil
layers
the
same
depth.
Similarly,
under
the
ordosica
and
poaeoides
cover,
the
biomass
and
Eragrostis
poaeoides
the microbial
biomass
carbon and
nitrogen
contents
of the moss
crust
depth.
Similarly,
undercover,
theArtemisia
Artemisia
ordosica
andEragrostis
Eragrostis
poaeoides
cover,
themicrobial
microbial
biomass
carbon
contents
of
moss
crust
5)5)and
soil
layers
were
than
(crust
andnitrogen
underlying
soil layers
than those
ofunderlying
the algal crust
andhigher
underlying
carbon5)and
and
nitrogen
contents
ofthe
thewere
mosshigher
crust(crust
(crust
and
underlying
soil(crust
layers4)
were
higher
than
those
of
crust
(crust
soil
layers
atalgal
the same
those
ofthe
the
algal
crustdepth.
(crust4)4)and
andunderlying
underlyingsoil
soillayers
layersatatthe
thesame
samedepth.
depth.
00
5050
100
100
MMicrobial
icrobialbiom
biomass
asscarbon(m
carbon(mg/kg)
g/kg)
150
200
250
300
150
200
250
300
aa
bb
Crust
Crust
cc
aa
aa
Depth(cm)
Depth(cm)
0-6
0-6
6-12
6-12
12-18
12-18
18-24
18-24
24-30
24-30
bc
b bc
b
dc dc
cc
aa
aa
aa
bb
bb
aa
abab
abab
bcbc
aa
aa
aa
aa
400
400
aa
bb
aa
abab
bb
bb
350
350
cc
cc
bb
Crust
&&
layers
Crust
layerssample
sample1 1
Crust
&&
layers
Crust
layerssample
sample2 2
Crust
&&
layers
Crust
layerssample
sample3 3
Crust
&&
layers
Crust
layerssample
sample4 4
Crust
&&
layers
Crust
layerssample
sample5 5
Figure
The
microbial
biomass
carbon
contents
ofofthe
and
samples
atatdifferent
Figure9.
Themicrobial
microbial
biomass
carbon
contents
thefive
fivecrust
crust
andlayers
layers
samples
different
Figure
9.9.The
biomass
carbon
contents
of the
five
crust
and layers
samples
at different
depths.
depths.
Data
with
the
same
letter
at
the
same
depth
are
not
significantly
different
at
p
=
0.05
by
the
depths.
Data
same
letter
at the
same
are not significantly
= 0.05
by
the
Data
with
the with
samethe
letter
at the
same
depth
are depth
not significantly
different atdifferent
p = 0.05 at
bypthe
LSD
test.
LSD
LSDtest.
test.
Sustainability 2017, 9, 725
Sustainability 2017, 9, 725
9 of 15
9 of 15
0
M icrobial biomass nitrogen(mg /kg)
40
60
20
a
ab
Crust
c
a
a
Depth(cm)
0-6
18-24
b
a
b
Crust& layers
Crust& layers
Crust& layers
Crust& layers
Crust& layers
a
a
b
a
24-30
b
a
b
a
c
b
a
12-18
b
a
b
a
100
a
a
a
a
6-12
80
b
a
b
sample
sample
sample
sample
sample
1
2
3
4
5
Figure 10. The microbial biomass nitrogen contents of the five crust and layers samples at different
Data with
with the
the same
same letter
letter at the same depth are not significantly different at p = 0.05 by the
depths. Data
LSD test.
3.4. Relationships between Physicochemical Properties and Microbial Parameters
Parameters of
of Soil
Soil Crusts
Crusts
The relationships
relationshipsbetween
between
water
content,
density,
organic
water
content,
bulkbulk
density,
organic
matter matter
content,content,
microbialmicrobial
biomass
biomass
carbon microbial
content, microbial
biomass content,
nitrogenand
content,
andactivities
enzyme of
activities
thecrusts
five soil
carbon content,
biomass nitrogen
enzyme
the fiveofsoil
are
2
crusts
are
listed
in
Table
2.
The
water
content
was
strongly
related
to
the
alkaline
phosphatase
listed in Table 2. The water content was strongly related to the alkaline phosphatase activity (R = 0.96,
2 = 0.96, p < 0.01). Negative correlations were found between the bulk density and other
activity
p < 0.01).(R
Negative
correlations were found between the bulk density and other parameters. The organic
parameters.
The
organic
matter
content
was positively
stronglyphosphatase
correlated activity
with the(R2alkaline
matter content
was
positively
strongly
correlated
with the alkaline
= 0.98,
2
2 = 0.98, p
2 = 0.96, p < 0.01), respectively. The
phosphatase
activity
(R
<
0.01)
and
protease
activity
(R
p < 0.01) and protease activity (R = 0.96, p < 0.01), respectively. The microbial biomass carbon content
2 =microbial
microbial
biomass
carbon
content
was
correlated
with (R
the
biomass
was
positively
strongly
correlated
with
thepositively
microbial strongly
biomass nitrogen
content
0.99, p < 0.01)
and
2 =2 =
nitrogen
content
0.99,p p< <0.01),
0.01)respectively.
and urease activity (R2 = 0.97, p < 0.01), respectively.
urease activity
(R(R
0.97,
The statistical analysis of the enzyme activities showed that all
all the
the alkaline
alkaline phosphatase,
phosphatase, urease,
urease,
protease and peroxidase activities were strongly related to crust type (p <
< 0.05).
0.05). As
As shown
shown in
in Table
Table 3,
3,
vegetation cover also had aa significant
significant influence
influence on
on enzyme
enzyme activities.
activities. Moreover, the interaction
between crust type and vegetation cover was obvious.
obvious.
Table
microbial parameters
parameters of
of soil
soil crusts.
crusts.
Table 2. Correlation coefficients between physicochemical and microbial
SWC a
SWCb a
SBD
SBD bc
SOMC
SOMCd c
SMBC d
SMBC
SMBN e e
SMBN
Alkaline
Alkaline
Phosphatase
Phosphatase
Urease
Urease
Protease
Protease
Peroxidase
Peroxidase
SWC
SWC
1.000
1.000
SBD
SBD
−0.801
−
0.801
1.000
1.000
SOMC
SOMC
0.916 *
0.916 *
−0.813
−
0.813
1.000
1.000
a
SMBC
SMBC
0.956 *
0.956 *
−0.854
−0.854
0.926
*
0.926 *
1.000
1.000
Alkaline
SMBN
Alkaline
SMBN Phosphatase
Phosphatase
0.935 *
0.959 **
0.935
0.959 **
−0.918
* *
−0.828
−0.918
−0.828
0.911
* *
0.977
**
0.911 *
0.977 **
0.989 **
0.917 *
0.989 **
0.917 *
1.000
0.906 *
1.000
0.906 *
1.000
1.000
Urease
Protease
Urease
Protease
0.872
0.914 *
0.872
0.914 *
−0.775
−0.694
−0.775 0.959
−0.694
0.855
**
0.855
0.959 **
0.972 **
0.942 *
0.972 **
0.942 *
0.953 *
0.895 *
0.953 *
0.895 *
0.809
0.919
0.809
0.919**
1.000
1.000
0.920
0.920**
1.000
1.000
Peroxidase
Peroxidase
0.540
0.540
−0.868
−0.732
0.868
0.732
0.700
0.700
0.768
0.768
0.646
0.646
0.694
0.694
0.616
0.616
1.000
1.000
b SBD–soil
c SOMC–soil
d SMBC–soil
b SBD–soil
c SOMC–soil
d SMBC–soil
SWC–soil water
bulkbulk
density;
organic
matter content;
microbial
SWC–soil
watercontent;
content;
density;
organic
matter content;
e SMBN–soil microbial biomass nitrogen; * and ** indicate significance at p < 0.05 and p < 0.01
biomass
carbon;
e
microbial biomass carbon; SMBN–soil microbial biomass nitrogen; * and ** indicate significance at p
levels, respectively.
< 0.05 and p < 0.01 levels, respectively.
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Table 3. Statistical analysis of enzyme activities.
Source of Variation
Enzymes
Alkaline Phosphatase
Urease
Protease
Peroxidase
Crust Type ×
Vegetation Cover
Vegetation
Cover
F
Sig.
F
Sig.
F
Sig.
F
Sig.
F
Sig.
F
Sig.
F
Sig.
205
174
119
83
0.000
0.000
0.000
0.000
59
114
51
9.3
0.000
0.000
0.000
0.005
78
46
308
15
0.000
0.000
0.000
0.000
79
22
82
5.5
0.000
0.000
0.000
0.026
16
2.7
11
0.3
0.000
0.016
0.000
0.982
9.3
6.9
12
1.7
0.000
0.000
0.000
0.162
7.6
6.5
17
2.6
0.000
0.000
0.000
0.044
Depth
Crust
Type × Depth
Vegetation
Cover × Depth
Crust Type × Vegetation
Cover × Depth
Crust Type
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4. Discussion
4.1. Relationships between Soil Crust Development and Soil Properties
In the Hobq Desert of North China the physical crust has been formed at the surface of the bare
area through the accumulation and subsidence of deposited atmospheric dust. The deposition process
and plant roots can compact the physical crust. The fertility of the subsoil layer can be improved after
long-term migration and leaching of humus and mineral elements. By this time, the microorganisms
will have begun to accumulate organic matter, leading to the development of biological soil crust
from algal crust to moss crust, as the biological soil crust is mainly composed of bacteria, fungi, algae,
lichens, mosses, and other cryptogams [2].
The results showed that the water retention, macro-aggregate content, organic matter content,
enzyme activities, and microbial biomass carbon and nitrogen contents of the soils below the biological
crusts (algal crusts 2 and 4, and moss crusts 3 and 5) were significantly higher than the corresponding
values of the soil below the physical crust (crust 1) (p < 0.05). This finding indicated that the soil
crusts significantly improved the properties of the sandy soil, and the well-developed moss crust had
a more significant amelioration effect when compared to the physical crust and other less-developed
biological crusts. Moreover, the crust thickness was in the following increasing order: physical crust
< algal crust < moss crust. Similarly, Guo et al. [1] observed that the succession process of biological
crust was from algal crust to moss crust with an increase in thickness from 0.68 to 1.79 cm.
Due to the dry and windy climate, and sandy land in the Hobq Desert, soil fertility and structure have
been subjected to severe long-term degradation. The structure of small aggregates can be easily broken up,
and the organic carbon content is low (∼6 mg/kg) [22]. In this study, the establishment and development
of soil crust reduced the bulk density and micro-aggregate content. For example, the amount of <53 µm
aggregates in crust 1 was 88%, indicating a potentially poor surface structure. In contrast, the aggregate
size was significantly increased in well-developed crusts 2, 3, 4, and 5, contributing to increasing
aggregate stability against wind erosion. Moreover, soil crust development can stabilize the loose
desert surface and improve its resistance to wind erosion. This may be attributed to the accumulation
and deposit of atmospheric dust and microbial activities. This finding is in accordance with Chamizo
et al. [2], who found that the aggregate stability was higher under well-developed moss crust than
under physical crust. Biological crust can improve aggregate stability, which contributes to a more
stable soil structure by wrapping loose particles through rhizoid and plant [6,28].
The development of soil crust resulted in an increase in the water contents of the crusts and their
underlying soils in the upper horizons. In the 0–12 cm deep soil layer, for example, the dense root of
vascular plant and microbial secretion could increase the water content [29]. In addition, the reduction
in the surface evapotranspiration can contribute to the increase in the underlying water content.
The water content decreased in the 18–30 cm deep soil layer, possibly because after the interception of
precipitation by soil crusts, precipitation was consumed by the shallow (0–30 cm deep) roots of the
dominant Artemisia ordosica and evaporation of the crusts, instead of recharging to deeper soil. Yu and
Steinberger [15] observed that the water content slightly increased in the 10–20 cm deep soil layer and
then decreased in the 20–40 cm deep soil layer under Hammada scoparia, in the Negev Desert in Israel.
The organic matter content of crust 1 which is physical crust was below 5 g/kg, indicating the
depletion of soil fertility. The organic matter content of the well-developed moss crust was 5.1-times
greater than that in the physical crust. The establishment and development of soil crust enhanced the
accumulation of organic matter through extracellular polysaccharides [30]. This finding is consistent
with the results of Guo et al. [1] who found that the contents of organic matter, total nitrogen, and total
phosphorus in the bare Horqin Sand Land in Inner Mongolia ranged from 6.64 to 31.91, 0.48 to 1.33,
and 0.13 to 0.23 g/kg, respectively, indicating the inherent infertility after long-term migration and
leaching of humus and mineral elements.
The activities of alkaline phosphatase, urease, protease, peroxidase, and the microbial biomass
carbon and nitrogen contents increased simultaneously with the development of soil crust from the
Sustainability 2017, 9, 725
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physical crust to the algal crust to the moss crust. This finding indicated that the moss crust was
desirable for microbial growth and reproduction, as well as enzyme activities due to its higher contents
of water and organic matter, when compared to algal and physical crusts. Enzyme activities can
accelerate the enzymatic reaction of organic matter, promote the circulation of organic compounds and,
therefore, improve soil properties benefiting plant growth, and enhance biological soil crust formation.
Yang et al. [31] and Pajares et al. [32] reported that soil enzymes and microbes promoted soil nutrient
transformation and cycling, and can be used as indicators of quality changes of soils. The results
of this study also suggested that soil crust formation is mainly accompanied by microbial activities.
Additionally, the results supported previous studies that demonstrated that the development of soil
crust can increase water availability, improve soil stability, and increase contents of organic matter,
carbon, and nitrogen. These properties are the factors that are significantly affecting soil enzyme
activities and microbial biomass in arid and semi-arid areas.
The properties of the 0–30 cm deep soils below the algal and moss crusts were significantly
improved when compared to those of the soil below the physical crust. Moreover, the moss crust had
the most significant amelioration effect on the underlying soil. However, the influence of vegetation
coverage and vegetation litter appeared to be limited as the amelioration effect decreased with depth.
Furthermore, water content varied dramatically with depth. Organic matter content, microbial biomass
carbon and nitrogen contents, and enzyme activities all decreased with depth. These findings are in
accordance with Chamizo et al. [2], who reported that the underlying soil properties (e.g., aggregate
stability, water content, organic carbon and nitrogen content) were higher under the moss crust
than the physical crust. Similarly, Bolton et al. [33] indicated that soil microbial biomass carbon and
nitrogen contents and soil enzyme activity were 2–15 times higher in the top 5 cm of soil than at the
5–15 cm depth regardless of plant type. In this study, at the depth of 0–6 cm, the underlying soil
physicochemical and biological characteristics were significantly (except for organic matter content,
alkaline phosphatase activity, peroxidase activity) improved from physical crust to moss crust (p < 0.05).
Moreover, the amelioration effect mainly occurred under the well-developed moss crust rather than
under the less-developed algal crust and physical crust. Guo et al. [1] demonstrated that biological
crusts pose a significant influence on the properties (e.g., bulk density, organic matter content, nitrogen
content, phosphorus content, electrical conductivity, pH and CaCO3 content) of the 0–5 cm deep layer
underlying topsoil.
Under the Artemisia ordosica cover, for example, the highest contents of organic matter, microbial
biomass carbon and nitrogen, and enzyme activities in the crusts and 0–30 cm deep layers underlying
soils were found in Crust and layers sample 3 (moss crust). Crust and layers sample 3 was dominated
by the 53–250 µm aggregates. In contrast, under the Artemisia ordosica and Eragrostis poaeoides cover,
Crust and layers sample 5 was dominated by the >250 µm aggregates, exhibiting an increasing trend
in organic matter content with increasing aggregate size. Similarly, Jastrow et al. [34] demonstrated
that organic matter content was greater in macro-aggregates (>212 µm) than in micro-aggregates
(53–212 µm). This can be attributed to the different carbon sequestration ways between large aggregates
and micro-aggregates. Large aggregates derived most of their organic matter from the decomposition
of roots and hyphae which are easily affected by the environment and transformation, while
micro-aggregates sequestrate carbon through the combination of organic and inorganic colloids [35].
Therefore, the organic carbon in micro-aggregates mainly consists of stable humus carbon, which is
not easy to be mineralized. The contents of >250 µm aggregates and organic matter, microbial biomass
carbon and nitrogen and enzyme activities under Artemisia ordosica and Eragrostis poaeoides cover were
greater than those under Artemisia ordosica cover. Franzluebbers and Arshad [36] also observed that
the microbial content and activity were greater in large aggregates in the Canadian Prairies.
4.2. Relationships between Vegetation Types and Soil Properties
Regarding the same type of soil crust, the water retention, aggregate stability, organic matter
content, enzyme activities, and microbial biomass carbon and nitrogen contents of the soil under
Sustainability 2017, 9, 725
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the Artemisia ordosica and Eragrostis poaeoides cover (algal crust 4 and moss crust 5) were significantly
higher than the corresponding values of the soil under the Artemisia ordosica cover (algal crust 2 and
moss crust 3) (p < 0.05). Thus, the complex crust-soil-vegetation system interaction has affected the
physicochemical and biological properties of crusts and their underlying soils. The vegetation effects
are dominated by the vegetation litter and root system.
On the one hand, shrub can intercept and deposit atmospheric dust, and then the vegetation litter
intercepts rainfall and suppresses transpiration [37]. In the current study, the cover of Artemisia ordosica
helps the desert surface to resist wind erosion and promote crust development. Therefore, it is easy to
form a feedback mechanism among vegetation litter, soil structure, and soil nutrients. Schlesinger and
Pilmanis [38] found a high infiltration rate below desert shrubs as a result of better soil crumb structure
and lower impact energy of raindrops. Read et al. [39] confirmed that biological crusts are generally
developed from shrub vegetation as it can increase the surface roughness and surface clay content by
capturing aeolian dust through dense foliage. On the other hand, vegetation roots provide effective
carbon and nitrogen contents for microbial and enzyme activities by secreting metabolites into the
rhizosphere during growth [40]. The herbaceous vegetation Eragrostis poaeoides is more conducive
to nutrient accumulation and soil properties improvement due to its very large root system, and the
decomposition of dead roots can gradually improve the underlying soil properties [5].
The type of vegetation cover is also of great importance to soil quality. It is a contributing factor
for the better soil properties found in, for example, algal crust and layers sample 4 than crust and
layers sample 2, and moss crust and layers sample 5 than crust and layers sample 3.
5. Conclusions
The influence of the soil crust development on a range of properties of crust and layer samples
collected from the Hobq Desert was investigated. The results demonstrated that organic matter,
microbial biomass carbon and nitrogen contents, and enzyme activities of the crusts were significantly
different at different soil crust development stages. The thickness, water content, and aggregate
stability of the soil crusts increased with soil crust development, while the bulk density of the soil
crusts decreased with soil crust development. The findings also indicated that soil crusts significantly
improved the soil properties. In addition, moss crust had a more significant amelioration effect
when compared to other less-developed crusts. The physicochemical and biological properties
of the soils below the algal and moss crusts were significantly improved when compared to the
physical crust. However, the effect of the soil crust development on the underlying soil quality
was significant at shallow depths (∼0–12 cm deep) and decreased quickly with depth. The results
suggested that the development of soil crust played a crucial role in improving the physicochemical
and biological properties of the underlying soil. The development of soil crust can promote the growth
of microorganisms and, ultimately, improve the soil microenvironment and ecological restoration in
the desert region.
Acknowledgments: This work was supported by the National Natural Science Foundation of China (No. 51379211).
Author Contributions: Jiping Niu, Kai Yang, Zejun Tang, and Yitong Wang conceived and designed the experiments.
Jiping Niu, Zejun Tang and Yitong Wang performed the experiments. Jiping Niu analyzed the data. Jiping Niu
and Kai Yang wrote the paper.
Conflicts of Interest: The authors declare no conflict of interest.
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