Journal of Arid Environments (2003) 53: 409-417
dei: 10. 1O06/jare.2002. 1046
@
Population
of arbuscular
mycorrhizal
fungi in
semi-arid
environment
of Jordan as influenced by
biotic and abiotic factors
M. Jamil Mohammad**,
S. Rushdi Hamadt & H. Issa Malkawit
* Department of Natural Resources and the Environment, Faculty of
Agriculture, Jordan University of Science and Technology,P.O. Box 3030,
I rbid, Jordan
tFaculty of Science, Jerash University, Jerash, Jordan tDepartment of
Biological Sciences, Yarmouk University, Irbid, Jordan
This study was conducted to evaluate the population of the arbuscular
mycorrhizal fungi (AMF) in the semi-rid agro-ecosystem of North Jordan
and to evaluate the effect of the biotic and abiotic factors on AMF
population. Soil samples were collected from 12 locations where several soil
samples were collected from each location. The collected soil samples were
analysed for chemical and physical properties and spores were separated from
the soil by the floating-adhesion
technique and examined by the dissecting
microscope. The AMF spores densities vary among locations and crops. The
spore density was relatively low, with the highest observed under fruit trees
and the lowest under a fallow system. Eight species were identified. Glomus
mosseae was the most common species among samples, which was found in
85 % of the soil samples collected. G. geosporum was found in 20%, while G.
constrictum and G. clarum were found in 10% of the samples collected. G.
caledomium was found in 8% of the samples. The lowest occurrence was
observed for the G. monosporum and G. clariodum, which were found in only
5% of samples collected. Twenty percent of the samples collected contained
Acaulospora spp. The spore density was not clearly affected neither by the
host plants nor by the location, which suggest the absence of location or plant
specificity for the AMF observed in soils of North Jordan. This may suggest
that other factors could have an effect on mycorrhizal distribution. Therefore,
biotic factors may be relatively less important than abiotic factors for
establishing population patterns. The spore density of AMF had a very weak
correlation with the soil pH and electrical conductivity (EC), and no
significant correlation with the percentages of soil clay and silt particles. The
organic matter (OM) and CaCO3 percentages were significantly positively
correlated with AMF spore density. On the other hand, the AMF spore
density was negatively related to the soil phosphorus. In conclusion, the G.
mosseae was the most common AMF species and no host plant or geographic
location specificity was observed, suggesting the population of AMF species
was affected mainly by a~iotic factors and cropping patterns.
<Q
2002 Elsevier Science Ltd.
Keywords:arbuscular mycorrhizal fungi; population;
*Corresponding
semi-arid environment
author. Fax: 962 2 7095 123. E-mail: [email protected]
0140-1963/02/030409
+ 09 $35.00/0
(g 2002 Elsevier Science Ltd.
410
M. J. MOHAMMAD ET AL.
Introduction
Mutualistic associations of AMF with host plants have been observed in various
natural and agricultural ecosystems (Sylvia & Williams, 1992). They play an essential
role in enhancing
plant growth in semi-arid agro-ecosystem
(Mc Gee, 1989),
particularly for plants grown in eroded soils (Herrera et aI., 1993). Under these
conditions, the AMF populations are usually low (Requena et al., 1996) and therefore,
AMF inoculation and enhancing cultivation practices favoring their activities would
improve soil capacity to support normal plant growth. Mycorrhizal plants have greater
ability to absorb phosphorus (Mohammad et al., 1995), and soil water (Puppi & Bras,
1990), and generally survive better under stressed environmental conditions (Sylvia &
Williams, 1992). AMF have also an aggregating effect, especially on coarse sandy
soils. Soil aggregates above 2 mm were found greater in soils with mycorrhizal plants,
significantly affecting soil stability (Sutton & Sheppard, 1976). It was shown that the
soil mycelium of AMF was coated with a mucilaginous substance that caused soil
particles to adhere together (Mosse, 1986).
The populations of AMF vary greatly and their distribution is affected by various
factors including soil, host plant, environmental conditions and agricultural practices
(Hayman, 1982). Under normal conditions, plant roots are usually colonized by AMF
(McGonigle & Miller, 1996). However, different agricultural practices or different
farming systems could have an effect on AMF activities.
AMF survive in the soil either associated with plant roots or as spores in the soil.
Although spores are not the only structure which can be used as inoculum, spore
density is still the common tool for quantifying mycorrhizal population in the soil
(Moorman & Reeves, 1979). Spore densities tend to increase during the summer after
the period of maximum root growth (Hayman, 1982). G. mosseae, like many other
AMF, occur in a broad range of dissimilar environments (Koske, 1987). For a species
to occur in diverse habitats, it must have physiological and genetic characteristics
which enable the species to survive different environmental
conditions (He slopHarrison, 1964). Even though AMF are sensitive to environment (Mosse et al., 1982),
some individual species are very widely distributed
and can tolerate different
environmental
conditions (Stahl & Christensen,
1991). There is variability due to
variable phenotypic plasticity among populations of G. mosseae in their responses to
different environmental factors, but this is not enough to explain the wide distribution
of this fungi species. In addition, AMF behavior is affected by soil pH (Wang et al.,
1985), nutrient level (Mosse et at., 1981) and interactions with other micro-organisms
(Bagyaraj, 1984).
Jordan is known for its wide and unique diversity of flora and fauna (AI-Eisawi,
1996). Much work has been done on biodiversity of plant and animal life in Jordan.
However, studies about population and biodiversity of soil micro-organism are scanty
and much work is needed to study the distribution, diversity and composition of
microbial populations in Jordan soils (GCEP, 1998). Limited studies have been
conducted on AMF populations in Jordan soils (AI-Momany, 1989); however, the
effect of abiotic factors on AMF population in Jordan soils was not previously
investigated.
Desertification
in the semi-arid region in Jordan is a real threat to the
agro-ecosystem with the soil becoming fragile (susceptible to structure destruction
and further erosion). This may result in reduction of AMF population
in the
soil. In desertified arid and semi-arid regions such as Jordan, AMF are essential
for enhancing plant growth and sustaining vegetation cover. Therefore, it is necessary
first to evaluate the AMF population of the soils. The objective of this study
was to evaluate the AMF population and their spatial and host variations in semiarid North Jordan and to evaluate the effect of the abiotic factors on AMF
populations.
ARBUSCULAR
MYCORRHIZAL
Material
FUNGI
411
IN JORDAN
and methods
The study area is characterized by long dry period in the summer and by scarce and
irregular rainfall in the winter months. The average annual precipitation is 350 mm
and the average minimum
and maximum
temperatures
are 15°C and 35°C,
respectively (Meteorological
Department,
1997). The dominant plants are olive,
stone fruits, grain crops, onions and summer crops, which is a Mediterranean
nonforest vegetation (AI-Eisawi, 1996).
~+
.
,.
25 '" n 1l1li
Km
. Bard1
areaIII
,;
57
..
..
12
81.
1
0
I
81
"
"
2
3
4
..
10
..
9
..
5
..
6
.
25
50 Km
..
7
I
=
"
8
Figure 1. Study area and sampling location: 1 U mmQais; 2 =Malka; 3 =Samer; 4 =Ain
=
6 =KufrJais; 7 =BeitRas; 8 Maru; 9 Kharja; 10 =,Harima; 11 = Eubla;
Trab; 5 Sama;
12 = Rafeed.
=
412
M. J. MOHAMMAD ET AL.
Soil samples were collected from 12 locations in the North of Jordan (Fig. 1). At
each location, several soil samples were taken from the fallow and root zone of the
dominant crops. Soil samples were collected in May 1996 from the top 20 cm using a
spade to collect about 1 kg of soil (the soil auger could not be used because the soils
were dry and stony in several locations). The number of soil samples collected was
based on the number of dominant crops and cropping system. The collected soil
samples were stored in plastic bags and kept in the icebox during the field trip and
then immediately refrigerated at 4 QC when arrived in the laboratory. Spore extraction
started in the following day and lasted about 1 week. A sub-sample, taken from each
sample, was air-dried, ground to pass a 2 mm sieve and was analysed for physical and
chemical characteristics.
Soil samples were analysed for pH on 1: 1 soil:water
suspension
(McLean,
1982); soluble salts were determined
by measuring the
electrical conductivity of 1: 1 soil:water extract (Rhoades, 1982); soil texture by the
hydrometer method (Gee & Bauder, 1986); organic matter by the Walkley-Black
method (Nelson & Sommers, 1982); calcium carbonate by acid neutralization method
(Richards, 1954); and NaHCOTextractable
phosphorus by Watanabe & Olsen (1965)
med10d.
The soil moisture was determined so that results could be reported on a dry-soil
basis. Spores were separated from the soil by the floating-adhesion
technique with
slight modification of Sutton & Barron (1972) method. Twenty grams of soil was
suspended in 250 ml of distilled water, thoroughly agitated for 10 min was left for
10 min for the clay to precipitate. The supernatant
was then transferred into a
separatory funnel. After 5 min, the supernatant was released from the funnel at a rate
of 75 drops min -1. The funnel was washed with distilled water to remove and collect
the spores adhering to the funnel sides. The spores were collected using filter paper
(Whatman #1) and then examined with a dissecting microscope. Spore densities were
recorded per 100 g dry soil. Species identifications were performed according to
Schenk & Perez (1990). Spore density for each species in each sample was recorded.
Pearson's correlation coefficients was used to determine the relationship between
spore abundance and abiotic factors using the Systat software statistical program
(Wilkinson, 1990).
Results
and discussion
The AMF species identified in the soil samples taken from the different locations in
North Jordan are presented in Table 1. Spores of eight species were found in the study
area. G. mosseae was the most common species among the samples, being found in
85% of the soil samples collected. These species are typical to arid and semi-arid
environment. It has been reported that G. mosseae has a variable response to different
Table 1. Occurrence of AMF species in the soil samples of North Jordan
Species
Symbol
% of samples
contained the species
Glomus mosseae
Glomus geosporum
Acaulospora spp.
Glomus clarum
Glomus constrictum
Glomus caledonium
Glomus monosporum
Glomus clariodum
G. mos
G. geo
A. spp
G. cIa
G. con
G. cal
G.mon
G. cIr
85
20
20
10
10
8
5
5
ARBUSCULAR
MYCORRHIZAL
FUNGI
IN JORDAN
413
environmental
conditions due to the variable phenotypic plasticity of this species
(Heslop-Harrison,
1964). The Glomus genus was reported to be dominant in arid and
semi-arid climates due to its resistance to high soil temperatures (Al-Raddad, 1993),
which explains the higher frequency of its occurrence in samples. G. geosporum was
found in 20% of the samples. G. constrictum and G. clarum were found in 10% and
G. caledomium in 8% of the samples. The lowest occurrence was observed for the
G. clariodu111~which was found in only 5% of the samples. Twenty percent of the
samples contained Acaulospora spp. The AMF population in the soils of North Jordan,
composed of eigtht species, indicate the variability of the AMF population in the soil
of North Jordan.
There were no obvious patterns in geographic distribution of the AMF species
(Table 2). In general, more than one species were observed in each soil sample
regardless of the geographic location or plant species (Tables 2 & 3). However, the
spore density was not clearly affected either by the host plants or by the location. This
suggests an absence of location or plant specificity for the AMF observed. The
absence of clear-cut trend in spore densities within the samples collected may suggest
that other factors could have an effect on AMF distribution.
Seely (1991) and
Jacobson (1997) reported that biotic factors are relatively less important than abiotic
factors for establishing population patterns and found that the duration of moisture
availability determines the level of AMF colonization. Level of soil fertility is believed
to be an important factor influencing the AM population (Hayman, 1982). Several
researchers reported a reduction in AMF population under high levels of soil P (AIMomany, 1989).
AMF spores were found in all samples and the numbers vary greatly among the
samples collected. The densities of AMF spores recovered from the soil samples
ranged from 5 to 70 spores 100 g-l of dry soil even for the same crop, namely Table 4.
The spore density is relatively low, which is common for arid and semi-arid lands
(Requena et al., 1996). In addition, most spores found did not look viable and some
were empty. The density of viable spores in arid and semi-arid soils was reported to be
relatively low (Mc Gee, 1989). Generally, fruit trees showed a higher spore density
compared to the annual crops (Table 4). This agrees with the findings of AI-Raddad
(1993), who attributed these differences to the length of the growing season and the
Table 2. Geographic distribution of AMP species in 39 samples in North Jordan
Site
BeitRas
KufrJais
Sama
AinTrab
Malka
UmmQais
Samer
Rafeed
Eubla
Harima
Kharja
Maru
Total
Species *
Sample
#
2
2
6
2
4
7
4
1
1
2
2
6
39
* Given species were found in at least one sample.
G.
G.
G.
G.
G.
G.
G.
G.
G.
G.
G.
G.
mos;
mos;
mos;
mos;
mos;
mos;
mos;
mos;
mos;
mos;
mos;
mos;
G.
G.
G.
G.
G.
G.
G.
G.
G.
G.
A.
G.
geo
geo; G. cla; A. spp
geo; G. cla; A. spp; G. mon
geo; G. clr
cla; A. spp
geo; A. spp; G. clr
mon; G. con
con
con
cal
spp
clr; G. con; G. cal
414
M. J. MOHAMMAD ET AL.
Table 3. Plant host distribution of AMP species in North Jordan
Plant
Sample
#
Grape
Peach
Almond
Olive
3
3
1
9
Loquat
Cherry
Pomegranate
Apricot
Tobacco
Okra
Onion
Wheat
Broom corn
Fallow
2
1
2
2
3
1
2
2
1
7
Species *
-
G.
G.
G.
G.
G.
G.
G.
G.
G.
G.
G.
G.
G.
G.
G.
mos; G. geo; G. cIa; G. elr
geo; A. spp;
geo; A. spp
mos; G. cIa; G. mon; G. cal;
con; A. spp
mos; G. cIa; G. con
mos; G. geo
mos; G. geo
mos; A. spp
mos; G. geo
mos; G. mon
mos; G. cIa; G. con
mos
mos; A. spp
mos; G. geo; G. cIa; A. spp
* Given species were found in at least one sample.
Table 4. AMP sporedensitiesin soil samplesfrom North Jordan.
Site
UmmQais
UmmQais
Maru
Kharja
Harima
Sama
Samer
UmmQais
Malka
Maru
Maru
UmmQais
UmmQais
UmmQais
UmmQais
Malka
Rafeed
Malka
Eubla
Harima
Plant
host
Spore
#
Site
Plant host
Spore
#
Fallow
Fallow
Fallow
Fallow
Fallow
Fallow
Fallow
Wheat
Wheat
Onion
Onion
Corn
Tobacco
Tobacco
Tobacco
Okra
0 live
0 live
0 live
0 live
5
7
8
5
8
7
6
19
5
40
8
46
15
27
70
38
41
30
64
16
Samer
Maru
Samer
Samer
.Maru
Sama
Kharja
Sama
Maru
Sama
AinTrab
AinTrab
BeitRas
BeitRas
Sama
Sama
Malka
KufrJ ais
KufrJ ais
Olive
Olive
Olive
0 live
Olive
Peach
Peach
Apricot
Loquat
Loquat
Almond
Pomegranate
Pomegranate
Cherry
Plums
Nectareen
Grape
Grape
Grape
41
18
30
27
18
43
12
10
44
41
32
15
35
17
37
18
52
13
14
type of the root systems of fruit trees, which make the rhizosphere more favorable to
spore propagation and AMF colonization.
The lowest spore densities were found in samples taken from fallow soils (Table 4).
Other researchers found that AMF colonization and AMF spores density declined as a
result of fallow (Black & Tinker, 1979; Kucey & Paul, 1983). Fallow was reported to
415
ARBUSCULAR MYCORRHIZAL FUNGI IN JORDAN
decrease the organic matter content and microbial activities in general (Black &
Tinker, 1979). Fallow in many semi-arid regions is frequently employed to increase
soil moisture storage for successive crops. Therefore, fallow cannot be eliminated from
the cropping systems in these regions. Fortunately, however, the decline in AMF
population in the soil due to long fallow can be ameliorated by AMF inoculation
(Thompson,
1987; Thomson et al., 1991).
It has been reported that population and diversity of AMF tends to increase under
natural ecosystems compared to that under agro-ecosystems (Sieverding, 1990). This
was attributed to the higher diversity of plant communities and to the management
practices in agro-ecosystems that would exert negative effects on the AMF population
(Rabatin & Stinner, 1989).
Impact
of soil fertility
on AMF populations
The spore densities of AMF had a very weak correlation with the soil pH and electrical
conductivity (EC) and no significant correlation with the percentage of soil clay silt
particles (Table 5). The organic matter (OM) and CaC03 percentages
were
significantly positively correlated with the spore densities of the AMF. On the other
hand, the AMF spore densities were negatively related to the soil phosphorus (Table
5). Further evaluation of the relationship between the soil P and spore density of the
AMF under various conditions indicates that the relationships were significantly
negative with fallow, annual crops and fruit trees and non-significant
with olives
(Table 6). Jacobson (1997), in a study of the AMF distribution
in an arid
environment, found that soil moisture availability significantly influenced the AMF
population and colonization levels. Both organic matter and CaC03 contents in the
Table 5. RegresszonequationsrelatingAMP sporedensitiesper 100 g of dry soil
(Y) with different soilproperties(X)
y
Spore
Spore
Spore
Spore
Spore
Spore
Spore
#
#
#
#
#
#
#
X
Linear regression
R
n
PH
EC (dSm-I)
OM (%)
CaC03 (%)
Silt (%)
Clay (%)
P (mg kg-I)
y= 44.62 - 02-43 X
Y=-57-4+09'07
X
Y=01.91 +21.29 X
Y=-17.18 + 02.14 X
Y= -30-59 + 00.22 X
¥= 28.32 + 00,05 X
Y= 34.12 - 00,54 X
0.20
0.17
0-52**
0-47**
0-03
0,03
0.42 **
39
39
39
39
39
39
39
R =correlation coefficient; n =number of observations.
* and ** refer to significance at p<0'05
and <0'01,
respectively.
Table 6. Regression equations relating AMP spore densities per 100 g of dry soil
(Y) with sodium bicarbonate extractable- P (X) under different cropping systems
Crops
Fallow
Annual crops
Fruit trees
Olives
Linear regression
R
N
Y= 06,39 + 00-01 X
0.10
0'58*
0,58 **
0'49*
7
9
23
9
Y= 40,49 - 00.71 X
Y= 40,64 - 00,64 X
Y= 45.61 - 00,78 X
R =correlation coefficient; n =number of observations.
* and ** refer to significance atp<0'05
andp<O'Ol,
respectively.
416
M. J. MOHAMMAD
ET AL.
soil increase the water-holding capacity of the soil (Brady & Weil, 1996) and therefore
may facilitate a more favorable soil moisture conditions for the AMF population.
Conclusions
In conclusion, populations of AMF present in all soils of semi-arid lands of North
Jordan are relatively low. There was no host plant specificity and no obvious patterns
associated with any geographic location, suggesting that the distribution of AMF
species is affected mainly by abiotic factors and cropping patterns. The study was
conducted only in northern Jordan; therefore, further investigation is recommended in
other regions of Jordan, where the climatic condition, cropping pattern and soil
properties are quite different.
This project was funded by the Higher Council of Science and Technology-The
Badia Development Project. Biodiversity of Soil Organisms in Jordan Soil
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