Introducing the study area
The study was conducted in Marvast semiarid rangelands in Yazd province,
Iran. The average annual rainfall is 250 mm which is maximum in January
(58.7 mm) and minimum in July and August (without rainfall). The average
annual temperature is 17.5 °C with average annual maximum temperature
28.3 °C and average annual minimum temperature of 0.7 °C. According to
the De Martonne’s classification, the climate is determined as
“semiarid”. Soils are the Brown steppe, predominant soils in Iran.
They have a very weak, often thick, A1 horizon with an
organic matter content of about 1% or more (Dewan and Famouri, 1964).
Shrubs are dominant in the area (Eskandarie, 2012). SE has been
described as an increase in the density of woody plants (e.g. Wiegand et
al., 2005). According to personal observation and communication with
native people and pastorals, the cover and density of shrubs have
increased during the recent years, showing a SE into the rangelands
(Geravand et al., 2016).
Three dominant shrubs were selected with different features and
architectures in the canopy, together with surrounding herbaceous
vegetation (hereafter called control).
- Amygdalus scoparia Spach. (Rosaceae family) is a wild species
of almond which occupies large areas in many parts of central Iran and
its neighboring countries. The oil of the A. scoparia is
extracted and used due to its fatty acid composition which is
comparable to that of olive oil (Sorkheh et al., 2016). The plant is
attractive for grazing animals due to its shade, fruits, and high
palatability of leaves. It is a deciduous large shrub which grows to a
height of up to 6 m, having a single-elongate main stem. It produces
numerous long and green branches. Fruits are drupes and are 1 to 1.5
cm long and 0.5 cm wide. They ripen and dehisce at the end of July
(Fig. 1).
- Ebenus stellata Boiss. (Fabaceae family) is a thorny shrub with
a height of 30-120 cm, with short and oblong-leafy branches and
ternate leaves that are alternate and covered with dense silk flakes.
This species grows in large parts of Iran including Kerman, Yazd,
Esfahan, Fars, and Hormozgan provinces as well as some dry and
semi-dry regions of world (e.g. Oman and India countries). The canopy
structure is open with thorny branches (Fig. 1).
- Daphne mezereum L. (Thymelaeaceae family) is a rounded-upright
deciduous shrub with an erect and bushy habit which typically grows to
1.5 m tall. All parts of this plant are poisonous to humans if
ingested, especially the fruits, sap, and bark. Thus, this shrub is
unpalatable for grazing animals. Nevertheless, fruits are attractive
to birds with no resulting ill effects. This species is found globally
in dry and semi-dry areas as well as in the provinces located in
central Iran (Mozaffarian, 2012) (Fig. 1).
Fifteen sites were randomly selected in the study area. In each site,
all three shrub species were close to each other (see 1 Fig. 1). Thus,
the topographical conditions were equal for growing the three shrubs and
related controls in each site, giving an opportunity for statistical
comparison of sub-canopy soil and vegetation characteristics between
shrubs.
Soil sampling and analyses
Soil sampling was done in April 2018 during the peak of plant biomass
production. According to the previous findings that the main effects of
shrubs would be changes in topsoil properties (e.g. Li et al., 2016;
Zhou et al., 2017), we thus collected soil samples from the topsoil (see
also Hu et al., 2018; Ding et al., 2019). Under the canopy of each
individual shrub, 10 soil cores were randomly collected to a depth of 20
cm, with a 5 cm diameter auger and pooled for each individual. In this
way, three soil samples were collected in each site for three species of
shrubs (totally 45 soil samples) and one for each control (totally 15
soil samples). The locations of control areas were selected according to
the prevailing wind direction in the area. Due to the prevailing
north-western winds in the study area, to eliminate the effects of shrub
litterfall on soil and vegetation in controls, we collected 10 soil
cores in the opposite direction to the prevailing wind (south-eastern)
with respect to the shrubs and at a location beyond the influence area
of any other shrubs at a minimum distance of 100 cm from the shrub
canopies in each site (Casal et al., 2013). Roots, shoots, and pebbles
in each sample were separated by hand and discarded after which the soil
samples were transported to the laboratory. The air-dried samples were
sieved, the smaller roots and coarse gravel (>2mm) were
removed through sieving, and the <2mm soil was used to examine
the effects of shrub species on soil properties. Soil pH was determined
using an Onion Ionalyzer Model 901 pH meter in a 1:2.5, soil: water
solution. Electrical conductivity (EC) was determined from a soil
extract with an EC meter, following the manufacturer’s instructions. The
available K, Ca, and Mg contents (with ammonium acetate extraction at pH
9) were determined by an atomic absorption spectrophotometer (AAS) and
Cation exchange capacity (CEC) with flame photometer (Bower et al.,
1952). The total nitrogen (N) was measured using a semi Micro-Kjeldhal
technique (Bremer and Mulvaney, 1982). The available P was determined
via a spectrophotometer using Olsen method (Homer and Pratt, 1961). Soil
organic matter (OM) was determined through Walkey-Black technique
(Allison, 1975; Erfanzadeh et al., 2014a).
Vegetation sampling and analyses
In the growth season (April 2018), the mean density
(number/m2), mean production
(kg/m2), and mean cover (%) of each plant species
growing under the canopy of each shrub and surrounding area (control)
were determined using quadrats 0.5 m×0.5 m. Since no clonal species were
observed in the area, estimation of plant density for all herbaceous
species was feasible. We used the methodology of “clipping and
weighing” for estimating the plant production of each herbaceous
species (Heady and Child, 1994). The herbaceous species in each plot
were clipped using a shear, and then weighed after oven drying, after
which the weight was calculated per m2(gr/m2 for plant productions). The number of
individuals was also counted in the quadrats for each plant species and
transferred into the number per m2. Areal cover
percentages of plants were visually estimated in each quadrat. The
number of quadrats under each shrub individual varied according to the
size of canopy of shrubs between two (for smallest ones) and four (for
largest ones). We also estimated the mean canopy surface of shrubs on
ground and the height of each individual shrub using a meter tape.
In addition, placing a thermometer (Marmonix MST 325 model) on soil, the
mean soil surface temperature was measured in multiple measurements (10
points) beneath each shrub and control. The time of recording the soil
surface temperature was the same for four locations (under three shrubs
and control) in each site.
Plant diversity and richness indices were calculated for each individual
under-shrub using plant cover data. The Shannon index is commonly used
to characterize the diversity of communities; it is sometimes referred
to as the Shannon-Wiener index (Equation 1) (Chernov et al., 2015).
Equation 1 H’ =\(\sum_{i=1}^{s}\text{pi}\text{logpi}\)
Where pi is the relative abundance of the ith taxon, and
S denotes the number of detected taxon.
Another diversity index frequently used in ecology is the Simpson index,
which is commonly determined as the probability of two plant species
belonging to different taxa randomly selected from an indefinitely large
community. The Simpson index is calculated from Equation 2 (Chernov et
al., 2015).
Equation 2 SI\(=\)\(\sum_{i=1}^{s}\frac{ni\ (ni-1)}{N(N-1)}\)
Where ni is the individual number of each plant species
in the taxon, and N denotes the total number of all individuals of all
plant species.
In addition, a large number of species richness indices have been
invented, each providing a value to show richness in a habitat, among
which the Menhinick index was used a simple measure of species richness
(Equation 3) (Hammer et al., 2001).
Equation 3 MI = (S) / \(\sqrt{N}\)
Where, S is the total number of species and N denotes the total number
of individuals in the sample.
All diversity and richness indices were calculated using the Past
software.
Data statistical
analysis
Firstly, normality of data (soil and vegetation characteristics) was
examined using the Kolmogorov-Smirnov test and homogeneity of variance
using Levene’s test. To evaluate the effect of shrub species on soil
properties and, plant diversity and richness, one-way ANOVA and LSD mean
comparison tests were used. All statistical analyses were performed in
SPSS software ver. 16.
Secondly, in order to compare the combination of soil properties under
three shrubs and surrounding area, the non-metric multidimensional
scaling (NMDS) was performed (Kottler Gedan, 2019) using the package
‘vegan’ (Oksanen, 2019) in R (R Core Team, 2018).
In addition, using the cover percentage of plants, the compositions of
vegetation were compared between four locations (three under the canopy
of three shrub species and one in the control) using additional NMDS
performing.
Results Variation of soil properties under the shrubs
The results of one-way ANOVA revealed that with the exception of Ca and
Mg, all soil properties were significantly different (P<0.05)
between four locations (under three shrubs and control) (Table 1).
The pH significantly decreased with shrub canopies with the lowest value
under A. scoparia (7.99) (Fig. 2). The highest pH value
was observed in the control (8.34).
Significant differences of EC, N, and P were observed between four
locations with the highest values under A. scoparia (0.28 Ms/cm,
0.57 % and 67.7 mg/kg, respectively) and the lowest values in control
(0.12Ms/cm, 0.16% and 10.57mg/kg, respectively). Although the values of
K and OM were not significantly different between three shrubs, the
lowest significant values of K and OM were found in the control with
257.9mg/kg and 0.81%, respectively (Fig. 2).
The highest mean soil surface temperature was recorded in control
(32.77°C) and the lowest under A. scoparia and D. mezerum(19.09°C and 17.93°C, respectively).
The NMDS results of soil properties separated and identified groupings
of soil (Fig. 4). Axis 1 clearly separated soil under D. mezerum ,A. scoparia and E. stellata from control. The second axis
of the NMDS showed no separable grouping for the four locations (Fig.
3).
Variation of vegetation characteristics under the shrubs
In general, 65 plant species were recorded in the study area. Astraceae,
Poaceae, and Papilianaceae were the most abundant families with 12, 10
and 7 species, respectively. Bromus tectorum and Galium
aparine were found abundant and common in the four locations. The
number of species beneath three shrubs and control was different with
43, 50, 30 and 31 species under D. mezerum , A. scoparia ,E. stellata and control, respectively (Appendix S1).
The results showed that the highest and lowest values of Shannon-Wiener
diversity index were observed beneath the A. scoparia and control
with 2.07 and 1.10, respectively. In addition, the highest value of
Simpson diversity index was recorded under A. scoparia (0.84)
which was not significantly different from D. mezerum (0.80) and
control (0.80), while the lowest value of Simpson diversity index was
observed under E. stellata (0.55). The highest and lowest values
of Menhinick richness index were observed under A. scoparia(3.43) and E. stellata (1.46), respectively (Table 2).
The greatest herbaceous production was observed under E. stellata(64.76gr/m2) and lowest was found in the control
(16.09gr/m2) (Table 2).
In addition, the mean surface of shrub canopies on ground was ca. 7.5
m2, 5.5 m2, and 4.00
m2 for A. scoparia D. mezerum , andE. stellata , respectively, and amongst three shrubs, A.
scoparia had the highest mean height with ca. 3.5 m compared withD. mezerum and E. stellata with ca. 2.60 m and ca. 1.83 m,
respectively (Table 2).
The NMDS results of vegetation cover identified groupings of species
composition (Fig. 4). Axis 1 separated D. mezerum and A.
scoparia from E. stellata and control. On the other hand, the
second axis of the NMDS showed no separable grouping for the four
locations.
DiscussionThe effect of shrubs on soil nutrients
Comparing the shrubs and control, our results indicated that the
presence of shrubs increased the values of soil nutrition properties
(OM, N, P and K). Many studies have found that shrubs increased soil OM
(Blaser et al., 2014; Liu et al., 2015; Du et al., 2016; Li et al.,
2016; Zeng et al., 2017; Ding et al., 2019), N (Blaser et al., 2014;
Zeng et al., 2017; Ding et al., 2019), P (Hagos et al., 2005; Blaser et
al., 2014; Ding et al., 2019) and K (Hagos et al., 2005; Ding et al.,
2019), where our results supported these findings. Nutrient accumulation
beneath shrubs as fertile islands in drylands is common and can provide
opportunities for C and N enhancement. For instance, McClaran (2008)
found that soil OM and N accumulation was one to eight times greater
beneath Prosopis sp. than in the open grassland. Similarly, many
other researchers reported that soils under shrubs are more fertile than
soils from the surrounding grassland (Abdallah et al., 2012; Noumi,
2015). Xie (2004) stated that soil OM stocks can be enhanced by
increasing the rate of litter addition to the soil. Thus, in our study
area, the augmentation of nutrient properties in soil can be a result of
a high input of plant litter amount by leaves and stems of shrubs and
herbaceous species existing under the shrub canopies.
Among studied soil properties, lower pH levels (less alkaline) were
observed beneath the three shrubs than control, which may be due to
leaching of volatile acids from the foliage of these shrubs (Whitford,
1992). Eldridge (2011) analyzed the data of 244 case studies in 43
ecosystem attributes from different parts of the world and showed that
pH declined with shrub.
Comparing three shrubs, significantly higher values of soil N and P and,
and non-significantly higher values of soil OM, Mg and K were observed
under A. scoparia. Taller (3.50m vs. 2.60m and 1.83m) canopy may
be a reason for increasing litter input compared with the two other
shrubs. Thus, a greater shrub litter mass would be likely to promote
higher levels of microbial decomposition, leading to enhanced soil
nutrient properties i.e. OM, N, K, P and Mg (see also McClaran et al.,
2008; Eldridge et al., 2011). In addition, larger shrubs would be
expected to support higher levels of biological activity as they provide
a wider habitat (canopy area) and therefore more resources (e.g. seed,
fruit, sap, flowers) for birds and mammals.
The effect of shrubs on vegetation characteristics
Comparing vegetation characteristics under three shrubs and control,
shrubs generally increased the plant species diversity and richness. The
most conservative explanation is that in semiarid lands, shrub shading
may promote facilitation role due to its effects on reducing
evapotranspiration and improving soil moisture (e.g. Maestre et al.,
2003; Guo et al., 2019). Indeed, higher litter input combined with lower
soil surface temperature under the canopies may create proper conditions
for emergence, growth, and reproduction of a larger number of species
due to increase in available soil moisture and decrease in soil surface
evaporation, resulting in enhanced plant diversity and richness.
Ghemandi (2019) reported that shrubs acted as nurse species increasing
the richness in the non-degraded semiarid grassland and facilitating the
seedling recruitment of important forage species in the degraded sites.
Similarly, Foronda (2019) indicated that plant diversity in semiarid
gypsum communities accumulated in the vicinity of shrubs. Also, Piper
(2019) stated that shrubs facilitated the occurrence of many species in
the plant community.
Among three shrubs, greater plant diversity and richness were found
under A. scoparia . Several traits of shrubs could be important in
relation to their functional outcome. Increases in the stature and size
of A. scoparia may promote a higher diversity of understory
canopies because of the “patch effect” (Erfanzadeh et al., 2014b) and
the increase in habitat heterogeneity under shrub canopies (Maestre and
Cortina 2005; Iyengar et al., 2017). Garner and Steinberger (1989)
reported that a higher shrub height compared with shorter shrubs and
control indicated the potential for shrubs to alter the microclimate,
and capture mobile resources such as airborne sediments, and therefore
their potential to create fertile islands and increasing plant diversity
under the canopy. Further, the shrub produces nests for birds and small
animals and may determine animal use and habitat, and therefore deposits
of exogenous resources such as feces and carcasses (Maestre et al.,
2009) and, deposits seeds through epizoochory and endozoochory (Chuong
et al., 2016), resulting an increase in plant diversity and richness.
Similarly, in semiarid steppes from the Mediterranean Basin, increases
in shrub cover and size were associated with higher species richness and
diversity of vascular plants (Maestre et al., 2009).
Although the diversity and richness of plant species were highest underA. scoparia , the greatest green plant production was found
beneath the canopy of E. stellata . The data showed that some
annual species (e.g. Bromus danthonia and B. tectorum )
consisted to a large part of plant production under E. stellatawhile they were produced in a very smaller amount of biomass under the
two other shrubs.
Finally, a literature review found that the three shrubs are probably
different in negative allelopathic impacts on herbaceous plants under
their canopies. D. mezerum produced a secondary metabolite,
containing various toxic compounds, including daphnetoxin and mezerein
(Chiej, 1984). While, lack of acute toxicity was reported in E.
stellata (e.g. Khodaparast et al., 2012) and A. scoparia (e.g.
Zibaeenezhad et al., 2017)
Grouping of soil properties and vegetation characteristics
by NMDS
The results of NMDS divided the soil properties into recognizable groups
including shrubs and control. This means that the soil under the three
shrubs was completely segregated from control; dissimilarity of the soil
between shrubs and control was greater than between three shrubs. Thus,
any species of shrub is able to change (promote) soil and should be
considered in the conservation projects in semiarid areas. Conversely,
grouping of vegetation characteristics was less pronounced by NMDS.
Thus, it can be concluded that the sensitivity of soil properties to the
shrubs might be higher than of vegetation.
Natural regeneration of herbaceous species in disturbed sites may be
facilitated by increasing the cover of shrub species. Thus, they could
be used as nurse plants during the first stages of restoration project.
We believe that increasing the cover and encroachment of shrub species
should not be a concern for managers. Conversely, recovery of herbs can
also be initiated through conservation and extension of shrubs.
Nevertheless, the extent to which shrubs affect soil and vegetation
characteristics is dependent not only on the presence of shrubs, but
also on the species of shrubs. Thus, different functions of various
species of shrubs on soil and vegetation should be considered in the
restoration projects of degraded rangelands.