Soil Biology & Biochemistry 40 (2008) 26862695

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Soil Biology & Biochemistry

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

Role of perennial plants in determining the activity of the microbial

community in the Negev Desert ecosystem
Naama Berg, Yosef Steinberger*
The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan 52900, Israel

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 21 January 2008
Received in revised form 14 July 2008
Accepted 20 July 2008
Available online 15 August 2008

Perennial plants are known to be one of the most inuential parameters in desert ecosystems affecting
microbial activity. In this study, we examined the importance of these perennial shrubs and attempted to
determine the most inuential factor that contributes the most to the ecosystem by separating the
physical part and the organic contribution of perennial plants. The study site is located in the northern
Negev Desert, Israel, where 50 Hammada scoparia shrubs and 50 articial plants were randomly marked
to be used as a tool for the above objectives. Soil samples were collected monthly in the vicinity of the
canopies of both shrubs while control samples were collected from the open areas between the shrubs.
All samples were collected from the upper (010 cm) and the deeper (1020 cm) soil layers. The
contribution to microbial activity was measured by evaluation of the microbial community functions in
soil. The results of the research showed a trend of a strong inuence of the perennial H. scoparia shrubs
on microbial community function. The functional aspects of the microbial community that were
measured were CO2 evolution, microbial biomass, microbial functional diversity, and the physiological
prole of the community. High values for all parameters were observed under the vicinity of the H.
scoparia shrubs, while the articial plants were found to have a weaker effect on the community
according to soil depth. The upper-soil layer at both locations (articial plant canopy and control
samples) showed higher values of the functioning parameters than that of the deeper soil layer. The
results indicate the importance of the organic contribution (plant litter) in comparison to the physical
part of desert shrubs.
2008 Elsevier Ltd. All rights reserved.

Keywords:
Islands of fertility
Microbial biomass
Functional diversity
Desert ecosystem

1. Introduction
One of the main limiting factors that largely determine
community functions in desert ecosystems is water availability
(Noy-Meir, 1973, 1974; Evenari et al., 1982; Shmida et al., 1986). The
two main water sources in such ecosystems, where the rain events
are unpredictable in time, amount, intensity, and frequency, are
precipitation and dew formation. In the Negev Desert, rain events
are usually relatively short and scattered over long periods of time
during the winter season (NovemberApril) (Evenari et al., 1982).
Dew formation is an additional and important source of water that
triggers and prolongs biological activity during the long, dry season
(Garner and Steinberger, 1989; West and Skujins, 1978).
In arid ecosystems, primary production is based mainly on
perennial plants, which have access to essential moisture and
nutrients due to their wide range of ecophysiological adaptations
(Evenari et al., 1982; Whitford, 2002). One of the main ecophysiological adaptations of the perennial plants is the regulation of water

* Corresponding author. Tel.: 972 3 5318571; fax: 972 3 7384058.

E-mail address: steinby@mail.biu.ac.il (Y. Steinberger).
0038-0717/$ see front matter 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.soilbio.2008.07.019

loss in order to fulll all their biological functions and protect

themselves against or prevent the dangers of water stress and
drought.
One of the major means used by shrubs, including dwarf shrubs,
to reduce the area of their transpiring surface when soil moisture
becomes limiting is by shedding some of their parts (leaves, stems,
branches, roots, etc.) in order to keep the rest alive and active
(Evenari et al., 1982). Leaf defoliation (litter production) and the
resulting accumulation of leaves in the vicinity of the plant stem
create fertile islands which generate a biological hub of microbial
activity in arid ecosystems. This activity is characterized by
complex trophic interactions between microora and micro-,
meso-, and macrofauna yielding a vigorous nutrient pool as a result
of their activity. Perennial shrubs allow these communities to
increase and prolong their above- and below-ground activities. In
this study, we examined the contribution of perennial shrubs by
testing the differences between the physical and biotic inuence on
the microbial communities (Charley and West, 1975; Santos and
Whitford, 1981; Steinberger and Whitford, 1983; Coleman, 1994;
Sarig et al., 1994; Whitford, 2002).
The contribution of the perennial plants can be divided into two
components: organic and physical. The main, organic component

N. Berg, Y. Steinberger / Soil Biology & Biochemistry 40 (2008) 26862695

includes the litter, fruits, and seeds from the shrub itself and the
below-ground root parts. These products supply the microbial
communities in the soil with a large diversity of carbon sources. The
second component is the physical barrier that protects the belowshrub area from high radiation and decreases wind velocity which,
together, contribute to improve water balance and to increase litter
and seed accumulation below the canopy.
The unique interaction between the plants and the soil biota
enables plant growth, and activity of soil microbial communities.
Such interactions thus increase nutrient availability (Coleman,
1985), which is necessary for primary production and for maintaining the long-term functioning and energy ow of ecosystems
(Grayston and Campbell, 1996; Grayston et al., 1998; Lahav and
Steinberger, 2001a).
Plants and microbial community structure and diversity are
known to be closely correlated (McGrady-Steed et al., 1997)
through utilization of dead cells, root exudates, and litter, which
results in an interwoven interaction between them. Considerable
information is available on the effect of the plant community on the
microbial community. However, the difference between the physical and organic contributions of perennial plants on the microbial
community is not understood.
The aim of this study was to examine the physical and organic
contributions of perennial shrubs to the microbial community on
a monthly basis in the Negev Desert ecosystem, by separating the
two components the physical and biotic parts of the perennial
plants. The functional aspects of the active bacterial community,
such as CO2 evolution, microbial biomass, physiological prole, and
functional diversity, were monitored in the vicinity of Hammada
scoparia and control (articial) shrubs and in an open, betweenshrub site, in order to address these aims. Strong evidence exists
that use of a broad-scale approach to the analysis of microbial
community parameters (Torsvik et al., 1990) will afford results that
will elucidate the inuence of the environmental parameters and
greatly improve our understanding of shrubsoil biotic
interactions.
2. Material and methods
2.1. Study site
The eld study was conducted at the Avdat Farm Research
Station in the Negev Desert Highlands, Israel. Elevation at the site is
about 600 m above sea level. The area has a temperate desert
climate, with hot summers (mean maximum 32  C, mean
minimum 17.7  C, in June) and cool winters (mean maximum
14.8  C, mean minimum 5.4  C, in January). The multi-annual mean
rainfall is 90 mm (Avdat Station), which occurs in scattered
showers only during the winter season (NovemberApril). An
additional source of moisture is dew, which falls heavily during the
autumn months (SeptemberNovember) (Evenari et al., 1982). The
soils are brown, shallow, rocky, desert soils (brown lithosols),
loessial, and grey desert soils (loessian serozems) (Dan et al., 1972).
The vegetation is a mixture of perennial shrub communities with
a large variety of annuals. Predominant perennials in the research
site are H. scoparia, Zygophyllum dumosum, Artemisia sieberi, and
variety of annual plants and geophytes.
2.2. Experimental set-up
Fifty H. scoparia shrubs were randomly marked in the study site
within a 10,000 m2 fenced area. In addition, 50 articial, shrub-like
plants made of plastic were placed randomly in the study area
(there were about 2 m between both shrubs types). The articial
plants were chosen in order to emulate H. scoparias physical
contribution and they looked similar to the natural shrubs in the

2687

eld (same size and proportions about 45 cm high and 40 cm in

diameter).
Immediately after set-up of the experiment, soil samples were
collected from depths of 010 and 1020 cm between November
2005 and May 2007 during the study period. The samples were
collected monthly (n 4) from three locations/treatments: (1)
under the canopy of H. scoparia; (2) under the canopy of the articial plants; and (3) from the interspace between the shrubs
(control samples). The soil samples were placed in individual
plastic bags and transported in a cooler to the laboratory. All soil
samples were sieved (mesh size 2 mm) in order to remove root
particles and other organic debris, and were kept at 4  C until
biological and chemical analyses were performed.
2.3. Methods
Soil moisture was determined gravimetrically by drying samples
at 105  C for 48 h, and was expressed as percentage of dry weight.
Organic-matter content was determined by igniting samples at
490  C for 8 h.
Total soluble nitrogen (TSN) was determined by chemical
extraction and color reactions using a Skalar-Autoanalyzer (S.F.A.S.,
1995).
Microbial functional diversity and community level physiological
prole (CLPP) were detected using the MicroResp plate (Campbell
et al., 2003). Fifteen different carbon sources of carbohydrates,
carboxylic acids, amino acids, and aromatic carboxylic acids
(Table 1) were added to whole soil samples (0.33 g in each well) in
deep well plates. CO2 evolution was measured by dye plates
a colorimetric reaction with absorbent alkali with the ability to
measure carbon dioxide evolution. The plates were twice read in
a spectrophotometer at 590 nm: just before the plates were placed
on the deep wells containing the soil samples (Time 0) and after 6 h
of soil respiration (Time 1). During that time, the plates were
incubated in the dark at 27  C. The result for each well was calculated in comparison to the 16th well, which contained the same soil
sample and water, measuring the basal respiration with no carbon
source at all.
Microbial functional diversity was determined using the ShanP
nonWeaver index (H0 ): H0  Pi(ln Pi), where Pi is the ratio of the
activity of a particular substrate and the sum of activities of all
substrates (Zak et al., 1994).
CO2 evolution and microbial biomass were measured by dye
plates a colorimetric reaction using absorbent alkali with the
ability to measure carbon dioxide evolution. Water was added to
whole soil samples in deep well plates covered by the dye plates in
order to measure respiration. Glucose was added to determine
microbial biomass according to the substrate-induced respiration
method. CO2 values were measured after 6 h of soil respiration
(Anderson and Domsch, 1978).
These two results were used for calculating the competition
efciency of the soil microbial population under environmental
conditions. The coefcient (qCO2) was calculated according to the
equation:
Table 1
The different carbon sources added to soil in MicroResp divided into chemical
groups
Aromatic carboxylic acids

Carboxylic acids

Carbohydrates

Amino acids

3,4-Dihydroxybenzoic acid
(protocatechuic acid)

L-Alanine

L-Arabinose

Citric acid

Arginine
L-Cysteine HCl
g-Amino butyric acid
L-Lysine
N-Acetyl-glucosamine

D-Fructose

L-Malic acid
Oxalic acid

D-Galactose
D-Glucose
Trehalose

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N. Berg, Y. Steinberger / Soil Biology & Biochemistry 40 (2008) 26862695

57.3

60

Total rainfall = 175.6 mm

Rainfall (mm)

50
40

44.2
Total rainfall = 58.8 mm
26.8

30

25.9

23.2

19.4 19.2

20

6.9

10

1.9

1.1

4.6

3.9

Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07
Fig. 1. Monthly rainfall in the research area during the study period (November 2005June 2007).

qCO2 CO2 production=biomass:

The metabolic index for CO2 is a specic parameter for evaluating
the effects of environmental conditions on soil microbial biomass
(Anderson and Domsch, 1990, 1993).
All the data obtained in the study were subjected to statistical
analysis of variance using the SAS model (ANOVA, Duncans
multiple range test and Pearson correlation coefcient) and were
used to evaluate differences between separate means. Differences
at the P < 0.05 level were considered signicant.

rainy season (October 2006May 2007) were 58.8 and 175.6 mm,
respectively (Fig. 1). The amount of 58.8 mm represents 65% of the
multi-annual average, while 85% fell during 2 months (46 and 39%
in February and April, respectively) out of the four rainy months. In
April 2006, the total rainfall was 23.8 mm that fell during 2 days of
rain. In the second rainy season (October 2007May 2007) the
amount of rainfall was more than three times that of the previous
year, with a total rainfall amount of 175.6 mm. One-third of this
amount fell during 4 days only, during April 2007.
3.2. Soil moisture

3. Results
3.1. Precipitation
The total amounts of rainfall at the study site during the rst
rainy season (November 2005April 2006) and the second season

Soil moisture (%)

20

15

Control
H. scoparia
Artificial

The rainfall pattern of the two rainy seasons was reected in the
soil moisture content on a temporal and spatial basis. The amount
of rainfall led to signicant (P < 0.05) differences between the two
rainy seasons in both soil layers (Fig. 2). The temporal rainfall was
found to increase the soil moisture level to maximal values of 6.9

0 - 10 cm

10

0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07
20

Soil moisture (%)

10 - 20 cm
15

10

0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07
Fig. 2. Changes in mean values of soil moisture (%) at three different locations: under the canopy of Hammada scoparia (diagonal shading), under the canopy of the articial plant
(white), and in the control samples between the shrubs (black). Top part is for the results of soil samples taken from the 0- to 10-cm layer; lower part is for the results of soil samples
taken from the 10- to 20-cm layer.

N. Berg, Y. Steinberger / Soil Biology & Biochemistry 40 (2008) 26862695

2689

Table 2
Correlation coefcient for soil samples collected at the different sites, under the canopy of Hammada scoparia, under the canopy of the articial plants, and in the open area
between the shrubs, during the study period (November 2005May 2007)

SM
OM
TSN
CO2 evolution
MB
qCO2
H0
Carboxylic
Carbohydrates
Amino acids

OM

TSN

CO2 evolution

MB

qCO2

H0

Carboxylic

Carbohydrates

Amino acids

Aromatic

0.17***

0.12*
0.2***

0.14**
NS
0.34***

0.14***
NS
0.41***
0.8***

NS
NS
0.34**
0.4*
0.14**

0.2***
NS
0.41***
0.73***
NS
NS

0.17**
NS
0.3***
0.54***
NS
NS
0.73***

0.13**
NS
0.29***
0.48***
NS
NS
0.58***
0.47***

0.17***
NS
0.32***
0.54***
NS
0.3***
0.68***
0.74***
0.53***

0.17***
NS
0.21***
0.57***
NS
NS
0.73***
0.57***
0.57***
0.46***

SM, soil moisture; OM, organic matter; MB, microbial biomass; qCO2, metabolic quotient; H0 , Shannon index; NS, not signicant B1 (P > 0.05).
*P < 0.05, **P < 0.01, ***P < 0.001.

Organic content (%)

and 15.0% for the 2006 and 2007 rainfall seasons, respectively, in
the 0- to 10-cm soil layer. In the deeper (1020 cm) soil layer, the
maximum values of soil moisture were found to reach higher levels,
such as 8.2 and 16.0% in the rst and second rainy seasons,
respectively. During the rst rainy season, the maximum soil
moisture in both soil layers was found in the vicinity of the articial
plants, whereas in the second rainy season, the highest soil moisture (P < 0.0001) was found in the vicinity of H. scoparia (Fig. 2).
Toward the dry season, in September 2006, the soil moisture
level decreased signicantly (P < 0.05) to 1.9 and 2.2% for the upper
and deeper soil layers (010, 1020 cm), respectively. This trend
was found to change prior to the second rainy season in November
2006, mainly due to the contribution of the dew. A signicant
(P < 0.001) difference on a temporal basis was observed between
the two soil layers and the three sampling sites (H. scoparia shrubs,
articial plants, and control areas). Negative correlation was found
between soil moisture and microbial functional diversity (H0 ) at all
locations (Table 2).

14

Control

12

H. scoparia
Artificial

10

3.3. Soil organic content

Soil organic content was found to be signicantly affected
(P < 0.001) by sampling location and time period (Fig. 3). May 2007
represents the highest levels of all months, with mean values of 4%.
Organic content was the highest under the canopy of the H. scoparia
shrubs at both layers (010 and 1020 cm) (P < 0.0001), with the
upper layer signicantly higher than the lower one (P < 0.05). The
second highest (but not signicant) organic content was found at
both locations under the canopy of the articial plants and in the
control area at the deeper soil layer (1020 cm). The lowest organic
content was found under the canopy of the articial plants and in
the control area in the 0- to 10-cm layer (P < 0.05).
3.4. Total soluble nitrogen (TSN)
The changes in TSN in soil samples collected from the different
sampling sites during the study period are presented in Fig. 4. A

0 - 10 cm

8
6
4
2
0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07

Organic content (%)

14

10 - 20 cm

12
10
8
6
4
2
0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07

Fig. 3. Changes in organic content (%) at three different locations: under the canopy of Hammada scoparia (diagonal shading), under the canopy of the articial plant (white), and in
the control samples between the shrubs (black). Top part is for the results of soil samples taken from the 0- to 10-cm layer; lower part is for the results of soil samples taken from the
10- to 20-cm layer.

2690

N. Berg, Y. Steinberger / Soil Biology & Biochemistry 40 (2008) 26862695

I TSN * gr-1 soil

20
16

Control
H. scoparia
Artificial

0 - 10 cm

12
8
4
0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07

10 - 20 cm

I TSN * gr-1 soil

20
16
12
8
4
0

Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07
Fig. 4. Changes in total soluble nitrogen (TSN) at three different locations: under the canopy of Hammada scoparia (diagonal shading), under the canopy of the articial plant
(white), and in the control samples between the shrubs (black). Top part is for the results of soil samples taken from the 0- to 10-cm layer; lower part is for the results of soil samples
taken from the 10- to 20-cm layer.

general trend demonstrated the effect of rainfall seasonality on

TSN. During the rst year, in which the total rainfall was low, TSN
was found to increase signicantly (P < 0.001) compared with the
second rainfall season, and was over threefold higher. The main

g CO2 C (g soil*h)-1

1.2

changes in the TSN on a temporal basis were found in soil samples

collected in the vicinity of H. scoparia shrubs, reaching higher
signicant values (P < 0.001) of 6.11 mg TSN g1 soil compared to
the other sampling sites. Moreover, the deeper soil samples

0 - 10 cm

1.0
0.8

Control
H. scoparia
Artificial

0.6
0.4
0.2
0.0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07

g CO2 C (g soil*h)-1

1.2

10 - 20 cm

1.0
0.8
0.6
0.4
0.2
0.0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07

Fig. 5. Changes in CO2 evolution at three different locations: under the canopy of Hammada scoparia (diagonal shading), under the canopy of the articial plant (white), and in the
control samples between the shrubs (black). Top part is for the results of soil samples taken from the 0- to 10-cm layer; lower part is for the results of soil samples taken from the 10to 20-cm layer.

N. Berg, Y. Steinberger / Soil Biology & Biochemistry 40 (2008) 26862695

100

0 - 10 cm

g C g soil-1

80

2691

Control
H. scoparia
Artificial

60
40
20
0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07

10 - 20 cm

100

g C g soil-1

80
60
40
20
0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07
Fig. 6. Changes in microbial biomass at three different locations: under the canopy of Hammada scoparia (diagonal shading), under the canopy of the articial plant (white), and in
the control samples between the shrubs (black). Top part is for the results of soil samples taken from the 0- to 10-cm layer; lower part is for the results of soil samples taken from the
10- to 20-cm layer.

collected in the vicinity of H. scoparia (1020 cm) were found to be

signicantly higher (P < 0.05) than in the upper (010 cm) soil
layer, with mean values of 6.11 and 5.43 mg TSN g1 soil,
respectively.

g CO2*10-3 C (gCmic*h)-1

30

3.5. CO2 evolution

CO2 evolution during the rst year of rainfall demonstrated
relatively higher activity than during the following periods,

0 - 10 cm

Control
H. scoparia

25

Artificial

20
15
10
5
0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07

g CO2*10-3 C (gCmic*h)-1

30

10 - 20 cm

25
20
15
10
5
0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07

Fig. 7. Changes in qCO2 values (metabolic quotient for CO2) at three different locations: under the canopy of Hammada scoparia (diagonal shading), under the canopy of the articial
plant (white), and in the control samples between the shrubs (black). Top part is for the results of soil samples taken from the 0- to 10-cm layer; lower part is for the results of soil
samples taken from the 10- to 20-cm layer.

2692

N. Berg, Y. Steinberger / Soil Biology & Biochemistry 40 (2008) 26862695

0 - 10 cm

Control
H. scoparia
Artificial

H'

3
2
1
0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07
5

10 - 20 cm

H'

3
2
1
0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07
Fig. 8. Changes in soil microbial functional diversity (H0 ) at three different locations: under the canopy of Hammada scoparia (diagonal shading), under the canopy of the articial
plant (white), and in the control samples between the shrubs (black). Top part is for the results of soil samples taken from the 0- to 10-cm layer; lower part is for the results of soil
samples taken from the 10- to 20-cm layer.

including the second rainy season. The levels in soil samples

collected from the bare soil and beneath the canopy of the articial
plants at the 10- to 20-cm layer were found to be signicantly
(P < 0.0001) lower than at the other sampling sites (Fig. 5). The
highest CO2 evolution levels (P < 0.05) were obtained in the soil
samples collected under the canopy of H. scoparia shrubs in the
upper-soil layer, with mean values of 0.10 mg CO2-C g1 dry soil h1.
On a temporal basis, the highest mean values (0.59 mg CO2-C g1
dry soil h1) of CO2 evolution were found in January 2006
(P < 0.05), compared to the summer sampling values (0.003 mg
CO2-C g1 dry soil h1) found in July 2006.
3.6. Microbial biomass
Microbial biomass exhibited a pattern similar to CO2 evolution,
with highest values (P < 0.001) recorded during January 2006
(54.3 mg C g1 dry soil), and then decreasing during the dry period
and the 2007 rainy season, reaching a minimum in July 2006 and
April 2007 with values of 0.52 and 1.57 mg C g1 dry soil, respectively (Fig. 6). A negative correlation was found between the
percentage of soil moisture and microbial biomass (Table 2). The
microbial biomass was largest (P < 0.001) in soil samples collected
in the vicinity of the H. scoparia shrubs. However, it was signicantly higher (P < 0.001) in the upper-soil layer than in the deeper
soil layer (11.27 and 9.01 mg C g1 dry soil, respectively). The values
measured in samples collected from the control sites and under the
canopy of the articial plants at the 10- to 20-cm layer exhibited
signicantly lower (P < 0.001) values of 5.2 mg C g1 dry soil.
3.7. The metabolic quotient (qCO2)
The metabolic quotient (qCO2) is a measure of the ecophysiological status of the soil microbial population and it was found to be
similar at all three sampling sites (Fig. 7). However, signicant

differences (P < 0.05) were found between the two soil layers.
Negative correlation was found between qCO2 levels and the
microbial biomass (Table 2).
3.8. Microbial functional diversity (H0 )
The Shannon index was used to determine the microbial functional diversity (H0 ) of substrate utilization (MicroResp). Signicant
differences (P < 0.001) were found between months and sampling
sites. The highest mean value was found during January 2006
(H0 2.7) and the lowest in July 2006 (H0 0.04) and April 2007
(H0 0.15) (Fig. 8). The sampling sites with the highest mean value
of H0 0.8 were found under the canopy of H. scoparia shrubs, in
both layers (P < 0.001), followed by the control and articial plants
in the upper-soil layer (0.61 and 0.58, respectively). The lowest
values were found in soil samples collected from the deeper layer in
the control site and under the articial plants (P < 0.001) (0.48 and
0.43, respectively). Microbial functional diversity was found to be
strongly associated (r 0.78) with microbial biomass (Table 2).
3.9. Community level physiological prole (CLPP)
All detected carbon groups (aromatic acids, carboxylic acids,
amino acids, and carbohydrates) were found to exhibit signicant
(P < 0.001) differences on a temporal basis (Figs. 9 and 10). The
highest utilization level was found in January 2006, reaching levels
of 1.22 mg CO2-C g1 dry soil h1, whereas the lowest utilization
values (P < 0.05) were measured in July 2006 and April 2007, with
values of 0.0047 and 0.058 mg CO2-C g1 dry soil h1, respectively.
Soil samples collected under H. scoparia shrubs exhibited a relatively higher utilization rate than those from the other sampling sites.
The highest carbon utilization rate (P < 0.05) was found for
aromatic carboxylic acids, with a mean value of 0.482 mg CO2-C g1
dry soil h1, compared to amino acids which were found to be

N. Berg, Y. Steinberger / Soil Biology & Biochemistry 40 (2008) 26862695

Carbo. Acids

1.6

g CO2 C (g soil*h)-1

2693

H. scoparia
1.2

Amino Acids
Carbohydrates
Arom. Carbox. Acid

0.8

0.4

0.0

g CO2 C (g soil*h)-1

1.6

Artificial plant
1.2

0.8

0.4

0.0

g CO2 C (g soil*h)-1

1.6

Control
1.2
0.8
0.4
0
Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07

Fig. 9. Changes in utilization ability of four carbon groups: carbohydrates,

; amino acids,
; carboxylic acids,
; and aromatic carboxylic acids
. Soil samples
collected from the 0- to 10-cm soil layer at three different locations: under the canopy of Hammada scoparia, under the canopy of the articial plant, and in the control samples
between the shrubs.

threefold lower (0.162 mg CO2-C g1 dry soil h1). This group
demonstrated signicant (P < 0.001) differences between the two
soil layers, with the lower values in the deeper layer.
4. Discussion
4.1. Impact of abiotic parameters
Organisms living in desert ecosystems have been found to cope
with the harsh environment by using behavioral, phonological, and
physiological adaptations. One of the most important triggers of
microbial activity that determines the success of these adaptations
is moisture availability, which is unpredictable in time and space.
Evenari et al. (1982), Noy-Meir (1985), Whitford (2002), and Coleman and Crossley (1996) emphasized the importance of moisture
availability to soil biota activity and its contribution to nutrient
accessibility for primary production.
Vegetation cover plays a major role in providing organic matter
and physical protection, thus contributing to fertile islands, biological hub formation, and prolonging of biological activity by
losing soil moisture and increasing seed accumulation.
The results elucidated the importance of the interplay
between rainfall variability and the plant covers contribution of

physical and organic matter as one of the main triggers of soil

microbial community parameters. In our investigation, we were
able to identify a signicant decrease in biological parameters,
yielding four distinct alternatives: (1) low moisture and high
organic matter causing a decrease in microbial functional
diversity (represented in JuneJuly 2006); (2) intermediate
moisture and organic matter inuencing microbial activity
(CO2 evolution, microbial biomass, and microbial functional
diversity) observed during March 2006; (3) high moisture and
low organic matter affecting microbial biomass during the
second wet season; and (4) high moisture and high organic
matter responsible for a decrease in CO2 evolution (represented in AprilMay 2007). The conclusions of the above alternatives are supported by studies conducted in different
ecosystems (e.g., desert) (Coleman et al., 1990; Steinberger, 1995;
Coleman and Hendrix, 2000; Whitford, 2002). Although water is
critical for all biological activities, high rain events and intensity
during short periods may act as inhibitors of soil biota function
(McMahon and Schimpf, 1981). Soil organic-matter values were
found to be signicantly different between the three sampling
sites, with the highest values found in the vicinity of the H.
scoparia shrubs, followed by samples collected in the vicinity of
the articial plants and control samples.

2694

N. Berg, Y. Steinberger / Soil Biology & Biochemistry 40 (2008) 26862695

Carbo. Acids

g CO2 C (g soil*h)-1

1.6

H. scoparia

Amino Acids
Carbohydrates
Arom. Carbox. Acid

1.2

0.8

0.4

0.0

g CO2 C (g soil*h)-1

1.6

Artificial plant
1.2

0.8

0.4

0.0

g CO2 C (g soil*h)-1

1.6

Control

1.2
0.8
0.4
0.0

Nov. Dec. Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
05
06
07
Fig. 10. Changes in utilization ability of four carbon groups: carbohydrates,
; amino acids,
; carboxylic acids,
; and aromatic carboxylic acids
. Soil samples
collected from the 10- to 20-cm soil layer at three different locations: under the canopy of Hammada scoparia, under the canopy of the articial plant, and in the control samples
between the shrubs.

4.2. Microbial community functional aspects

All functional aspects of the microbial community that were
measured in this study (CO2 evolution, microbial biomass, functional diversity, and CLPP) exhibited the same pattern, with high
values in the vicinity of H. scoparia > articial canopy > control in
the 0- to 10-cm upper-soil layer, while no difference was found
between the articial and control samples in the deeper (10
20 cm) soil layer. Our results suggest that the presence of live
shrubs and their broad contribution (physical and biotic) are the
main factors that affect microbial activity in desert soil as reported
by Insam and Haselwandter (1989). Findings similar to ours that
elucidated the importance of soil organic substances in determining biological activity were reported by Campbell et al. (1997),
Priha et al. (1999), and Grayston et al. (1998), emphasizing the fact
that carbon resources from different part of the plants regulate
microbial activity.
The importance of the microbial community in holistically
orchestrating between trophic relations, substrate utilization, and
nutrient recycling was partly elucidated in this study. Microbial
biomass, CO2 evolution and its functional diversity, which reect
microbial activity, were to found to be strongly reduced by highly
intense rainfalls, as also reported by Whitford (2002). Moreover, we
found that low and scattered rainfall intensity, which does not
cause runoff and the removal of nutrients and organic matter,

increases soil microbial activity. This is similar to ndings reported

by Buyanovsky et al. (1982), Coleman (1985), Kaffe-Abramovich
and Steinberger (2006), Lahav and Steinberger (2001b), and Waldrop and Firestone (2004). The metabolic quotient (qCO2) values,
which indicate the ecophysiological status of the soil microbial
population, as reported by Anderson and Domsch (1978), elucidated the importance of the differences between the two soil
layers, indicating the stress conditions undergone by the microbial
community in the deeper (1020 cm) soil layer due to the continuous, stable moisture availability and organic-matter accessibility.
Furthermore, organic-matter availability due to long-term input, as
indicated by the broad contribution of perennial shrubs, yielded
a distinctive continuous difference in relation to the articial plant
along the study period. These differences between the two shrubs
raise a temporal question, which necessitates a long-term followup study.
The microbial populations physiological proles (CLPP) were
found to support the concept of the role of fertile islands in
increasing organic-matter content in the vicinity of perennial
shrubs. The relatively high abundance of aromatic carboxylic acid
utilizers which are known to be compound-stimulating lignins in
the soil microbial community in the vicinity of H. scoparia was
justied by the presence of plant litter accumulation containing
a relatively high lignin content. An increase in CLPP substrate
utilization was found toward the end of the spring seasons (May

N. Berg, Y. Steinberger / Soil Biology & Biochemistry 40 (2008) 26862695

2006 and 2007), triggered by annual plant availability. This trend

was found to decline with the depletion in organic-matter availability toward the winter period, similar to results found by
Medeiros et al. (2006) and Strobel (2001). A follow-up of changes in
plant phenology and seasonal primary productivity throughout the
study period indicated a change in soil total soluble nitrogen, which
is known to be one of the limiting factors for plant productivity in
desert systems (Elkins and Whitford, 1982; Steinberger et al., 1990;
Zaady, 2005).
5. Conclusions
Our data suggest that by creating an island of fertility, perennial
plants form a biological hub which determines soil microbial
activity and community composition, thus determining nutrient
availability for primary producers. The results of this study support
the hypothesis that perennial plants play an important role as
suppliers of organic matter and as moderators of abiotic variables,
e.g., as a physical barrier against wind and radiation. The importance of the microbial community in holistically orchestrating
between trophic relations, substrate utilization, and nutrient pool
supply was partly elucidated in this study.
Acknowledgements
This study was partly supported by a contribution from Mrs.
Renata Steccati Krandel and Mr. and Mrs. Nissim and Giannina
Pontremoli via Keren Kayemeth Leisrael.
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