Emir. J. Food Agric ● Vol 31 ● Issue 12 ● 2019 969
Mohamed N. Al-Yahya’ei, Department of Aridland Agriculture, College of Food and Agriculture, United Arab Emirates University, Al Ain 15551,
UAE. E-mail: firstname.lastname@example.org
Received: 14 June 2019; Accepted: 21 November 2019
Organic agriculture is a holistic system characterized by the
strict prohibition of chemical fertilizers, herbicides, and
pesticides, and by managing soil through the use of organic
supplements and crop rotation (IFOAM, 2006). Hence,
the soil fertility, sustainability, and productivity of organic
farming systems mostly rely on biological processes carried
out by soil microorganisms. These organisms represent
key elements in the functionality of agroecosystems, and,
therefore, are critical factors for the success of organic
agriculture (Gosling et al., 2006).
Arbuscular mycorrhizal fungi (AMF) and plants form
perhaps the oldest symbiotic association on earth (Redecker
et al., 2000). It has been estimated that 80–90% of all land
plants form associations with AMF (Parniske, 2008). AMF
act as a living interface between plant roots and soil in
order to acquire water and nutrients for their host plants
(Smith and Read, 2008). In addition, AMF were shown
to protect their plants against biotic and abiotic stresses
(Veresoglou and Rilling, 2012). A role for AMF in the
synthesis of secondary plant metabolites has been reported,
contributing to the production of safe and high-quality
food (Giovannetti et al., 2012).
Organically managed soils were found to harbor higher
AMF diversity (Oehl et al., 2003, 2004; Verbruggen
et al., 2010; Säle et al., 2015; Gottshall et al., 2017), root-
colonization rates (Mäder et al., 2000; Smukler et al., 2008)
Organic farming practices in a desert habitat increased
the abundance, richness, and diversity of arbuscular
Sangeeta Kutty Mullath1, Janusz Błaszkowski2, Byju N. Govindan3, Laila Al Dhaheri1, Sarah Symanczik4,
Mohamed N. Al-Yahya’ei1*
1Department of Aridland Agriculture, College of Food and Agriculture, United Arab Emirates University, Al Ain 15551, UAE, 2Department
of Plant Protection, West Pomeranian University of Technology, Szczecin Slowackiego 17, PL-71434 Szczecin, Poland, 3Department of
Entomology, College of Food Agriculture and Natural Resources, University of Minnesota, Saint Paul, MN 55108, USA, 4Department of Soil
Sciences, Research Institute of Organic Agriculture (FiBL), Ackerstrasse 113, CH-5070 Frick, Switzerland, 5Department of Vegetable Science,
College of Horticulture, Kerala Agricultural University, Thrissur, India.680656
#This paper was presented at the 3rd Conference on Ecology of Soil Microorganisms, Helsinki, Finland in June 2018.
Agricultural practices are known to affect the diversity and efciency of arbuscular mycorrhizal fungi (AMF) in improving overall plant
performance. In the present study we aimed to compare the abundance, richness, and diversity of AMF communities under organic farming
of a desert ecosystem in the Arabian Peninsula with those of an adjacent conventional farming system and native vegetation. In total,
12 sites, including six plant species, were sampled from both farming systems and the native site. Spore morphotyping revealed 24 AMF
species, with 21 species in the organic farming system, compared to 14 species in the conventional site and none from rhizosphere soil
of a native plant (
). The AMF spore abundance, species richness, and Shannon–Weaver diversity index were high
under organic farming. In both systems, the AMF community composition and abundance associated with different crops followed similar
trends, with pomegranates having the highest values followed by limes, grapes, mangoes, and lemons. Our results show that organic
farming in such a desert ecosystem promotes AMF diversity. These data imply that AMF might play an important role in the sustainable
production of food in resource-limited desert habitats.
Keywords: AMF species; Organic farming; Spore abundance; Species richness; Shannon–Weaver index; Desert ecosystem
Emirates Journal of Food and Agriculture. 2019. 31(12): 969-979
Mullath, et al .
970 Emir. J. Food Agric ● Vol 31 ● Issue 12 ● 2019
and spore abundances (Galvez et al., 2001; Oehl et al., 2003,
2004) compared to conventionally managed soils. These
ndings suggest that AMF may play an essential functional
role in the maintenance of soil biological fertility, to
compensate for external inputs such as chemical fertilizers
and pesticides (Lekberg and Koide, 2005; Gosling et al.,
2006). Variations between AMF species in functions such
as colonization rates, growth of extra-radical hyphae, and
phosphorus (P) uptake have been investigated (Hart and
Reader, 2002; Munkvold et al., 2004; Jansa et al., 2005).
It is expected that high AMF diversity is more benecial
for host plants than low AMF diversity (van der Heijden
et al., 1998) due to the potential for greater functional
complementarity (Fitter, 2005).
High-input agricultural practices, such as monocropping,
deep ploughing, chemical fertilization, and pesticide use
are known to negatively affect AMF populations in terms
of biodiversity (Sasvári et al., 2011) and activity, which is
evaluated as the colonization ability (Mozafar et al., 2000;
Ryan et al., 2000).
Vegetation growing in the desert ecosystem of the Arabian
Peninsula (Fisher and Membery, 1998; Glennie and
Singhvi, 2002) must cope with drought, heat, soil salinity,
and low fertility, particularly due to low P availability
(Al-Yahya’ei et al., 2011). Additionally, sandy soils possess
a loose structure with a low water-holding capacity. It is
plausible that the symbiosis between plants and AMF
plays a key role in helping plants to cope with such
harsh environmental conditions. The multiple benets
conveyed by AMF for plant growth and survival under
stressful environments are well known (Smith and Read,
2008). Under arid conditions, for example, mycorrhizal
plants were found to maintain higher drought tolerance
(Augé, 2001) and to have better access to P than non-
mycorrhizal plants (Neumann and George, 2004). AMF
also enhance the soil aggregate stability, a particularly
relevant feature for sandy soils prone to erosion (Rillig
and Mummey, 2006).
Morphological and molecular analyses revealed unique
communities of AMF in the south Arabian Peninsula
(Al-Yahya’ei et al., 2011) that harbor newly reported
AMF species (Symanczik et al., 2014a, b). An assembly
of AMF species isolated from Arabian deserts has shown
complementary abilities in colonizing the root system
under different water regimes (Symanczik et al., 2015).
These ndings suggest that the diversity of AMF in such
arid regions may play an important role in the tness of
However, to our knowledge, limited studies have been
conducted to examine the effect of organic agricultural
practices on the diversity of AMF in desert ecosystems.
A comparative investigation of such an effect will further
the understanding of the behavior of these symbiotic
fungi and their roles in providing ecological services in
Our aim was to analyze AMF communities associated
with different crops under organic farming in a desert
habitat and to compare them with AMF communities
from adjacent conventionally farmed systems. Spore
morphotyping was used to study the AMF diversity in
both agricultural systems. The results showed that organic
farming in such a desert habitat enhances AMF abundance,
richness, and diversity.
MATERIALS AND METHODS
Study sites and sampling
The study sites are located in a sandy desert in the Emirate
of Abu Dhabi of the United Arab Emirates. The area
consists of two of Al Rawafed Agriculture Farms. One
farm (24º 25’ 07 N, 54º 49’ 40 E) is organically certied,
has an area of 50 hectares, and produces fruits, vegetables,
honey, and mushrooms. The other farm (24º 24’ 36 N, 54º
49’ 44 E) is managed by conventional methods with an
area of 60 hectares. Chemical fertilizers (mainly nitrogen,
phosphorus and potassium) were added according to
recommended fertilizer doses, based on soil test data. The
two farms are separated by approximately 150 m within an
area that is representative of the surrounding desert region,
in terms of soil type and vegetation.
The region has a hot desert climate, with temperatures
ranging from a maximum of 51ºC in July to a minimum
of 5ºC in January. The rainfall is infrequent (total annual
rainfall of approximately 60 mm). The area is 44 m above
sea level with an annual average relative humidity of 50%.
In this study, we selected ve crops grown at different
locations within each farming system with a maximal
distance of 200 m between sampling sites: pomegranate
(Punica granatum), grape (Vitis vinifera), mango (Mangifera
indica), lime (Citrus aurantifolia), and lemon (Citrus limon).
All crops were simultaneously planted in both farms
during the cultivation seasons of 2010 and 2011. In
addition to the ve individual crop plants, an organically
managed pomegranate–cabbage (Brassica oleracea var.
capitata) intercropped plot was included. Soil samples
from the rhizosphere of Tetraena qatarensis, the only native
plant naturally growing in the uncultivated area between
the two farms were also collected. In total, there were
twelve sampling sites (six under organic farming system,
ve under conventional farming system, and one native
Mullath, et al.
Emir. J. Food Agric ● Vol 31 ● Issue 12 ● 2019 971
Soil samples were collected in January 2016. Five replicate
plants in an area of ca. 400 m2 were randomly chosen
at each site. From the rhizosphere of each plant, three
soil samples were collected and pooled using a soil auger
with a diameter of 5 cm and a length of 30 cm. Sixty
pooled soil samples were obtained from 180 original
samples. The soil samples were stored in sealable plastic
bags for transportation and air dried before analysis. Soil
samples for soil-nutrient analysis were collected from the
rhizosphere of ve plants of each species, at each site. The
ve samples from each plant species were pooled to obtain
one composite sample per plant per site and further used
for soil-nutrient analysis.
Soil samples were passed through a 2-mm sieve and
mixed thoroughly to obtain composite samples. Soil
macronutrients (P, K, Ca, Mg, Na, and S) and micronutrients
(Cu, Fe, Mn, Co, and Zn) were measured with an
inductively coupled plasma–optical emission spectrometer
(Model: 710-ES, Manufacturer: Varian, USA).
AMF spore isolation and identication
AMF spores were extracted by wet sieving and sucrose
density-gradient centrifugation, using a modication of
the method of Daniels and Skipper (1982). For each
sample, approximately 15 g of air-dried soil was well
suspended in 20 mL of water in a 50-mL Falcon tube.
Twenty-five ml of sucrose solution (70% v/w) was
injected at the bottom of the tube, forming a stepped
density gradient, and the tube was centrifuged at 900 × g
for 2 min. The supernatant was washed with tap water
for 2 min in a 32-µm sieve and transferred to Petri dishes.
Spores, spore clusters, and sporocarps were collected from
the Petri dish and mounted on slides with polyvinyl-lactic
acid-glycerol (Koske and Tessier, 1983) or polyvinyl-
lactic acid-glycerol mixed 1: 1 (v/v) with Melzer’s
reagent (Brundrett et al., 1994) and examined under a
light microscope (Zeiss; Primostar) at a magnication
of up to ×1000. AMF species identity and abundance
were determined for each sample. Spore abundance was
assessed by counting the total number of AMF spores
extracted from 15 g of eld soil, whereas species richness
was derived from the total number of AMF species found
in the soil samples. T the Shannon–Weaver index was used
to compare the diversity of AMF communities between
farming systems and crops.
Identication was based on original and recent species
descriptions and identication manuals (The International
Culture Collection of Arbuscular and Vesicular-Arbuscular
Endomycorrhizal Fungi, INVAM: https://invam.wvu.
edu/; Arbuscular Mycorrhizal Fungi (Glomeromycota),
Endogone, and Complexipes species deposited in
the Department of Plant Pathology, University of
Agriculture in Szczecin, Poland: http://www.zor.zut.edu.
Analysis of variance (ANOVA) was employed to statistically
compare the AMF species richness, spore density, diversity,
and similarity index at eleven sites representing the six crops
and two farming system combinations.
AMF-abundance data were analyzed after omitting
outlier values to ensure that data met the assumptions of
normality. The resultant unbalanced dataset was handled
using the Kenward and Roger method to approximate
the denominator degrees of freedom and to adjust the
estimated standard errors for xed effects (Littell et al.,
2006). ANOVA was used to compare species richness
across two or more groups, and analysis of similarity
(ANOSIM) was conducted to test whether the AMF
species composition of different crops and farming
system combinations signicantly differed from results
based on the Bray–Curtis dissimilarity measure. ANOVA
was followed by Tukey’s honest signicant difference test
(Tukey’s HSD) with a signicance level of α = 0.05.
The estimation of species richness and diversity indexes
was performed using R software, version 3.2 (vegan and
anosim package), and ANOVA and Tukey’s HSD were
performed using SAS software, version 9.4. Graphical
visualizations were performed using the ggplot2 package
in R, version 3.2 (R Core Team, 2016).
Soil-nutrient analysis of the study sites (Table 1) showed
that soil from the conventional farm had signicantly
higher amounts of Mg, Na, S, Ca, Fe, and Mn than soil
from the organic farm (p < 0.05). No signicant differences
were observed between the organic and conventional farms
with respect to soil P, Cu, Co, and Zn contents.
AMF spore abundance in crops across farming systems
AMF spore abundances differed significantly when
analyzing crops (F5,43 = 45.18, p < 0.0001), the farming
system (F1,43 = 188.01, p < 0.0001), and their interaction
(F4,43 = 10.1, p < 0.0001). With the organic farming
system, the spore abundance was the highest (Fig. 1a)
for the pomegranate–cabbage intercrop (123 spores/15g
dry soil) and the lowest for lemons (48 spores/15 g dry
soil). With the conventional farming system, the highest
spore abundance was recorded for pomegranates (72.25
spores/15 g dry soil) and the lowest was recorded for
mangoes (33.4 spores/15 g dry soil). For each crop, the
Mullath, et al.
972 Emir. J. Food Agric ● Vol 31 ● Issue 12 ● 2019
spore abundance under the organic farming system was
signicantly higher than the corresponding value under
the conventional farming system, with the exception that
lemons had similar spore abundances under both farming
systems. No spores were detected in the case of soil
samples from the native site.
Table 1: Soil-nutrient status of conventional and organic
farming systems. Mean values of the same element followed
by different letters indicate signicant differences between
the two farming systems
Soil nutrients Organic farming Conventional farming
Phosphorus (%) 0.032A0.025A
Potassium (%) 0.125B0.147A
Magnesium (%) 0.596B1.050A
Sodium (%) 0.016B0.356A
Sulphur (%) 0.033B0.075A
Calcium (%) 8.394B14.134B
Iron (%) 0.390B0.490A
Manganese (%) 0.011B0.018A
Copper (ppm) 3.628A7.988A
Cobalt (ppm) 2.755A3.704A
Zinc (ppm) 15.846A27.738A
AMF species richness in crops across farming systems
AMF species richness differed significantly when
analyzing crops (F5,44 = 25.26, p < 0.0001), the farming
system (F1,44 = 62.86, p < 0.0001), and their interaction
(F4,44 = 11.04, p < 0.0001). With the organic farming
system, the species richness was highest (Fig. 1b) for
pomegranates (9–12 species) and lowest for lemons (2–3
species). With the conventional system, the highest species
richness was also recorded in pomegranates (1–8 species)
and the lowest was recorded for mangoes (2–3 species).
The Tukey–Kramer pairwise-comparison test indicated that
the species richness for pomegranates, limes, and grapes
was signicantly higher in the organic farm than in the
conventional farm. In the case of lemons and mangoes,
the species richness was not signicantly different under
the two farming systems.
AMF diversity (Shannon–Weaver index)
The Shannon–Weaver index (H′) was signicantly affected
by the crop species (F5,44 = 10.9, p < 0.0001), farming
system (F1,44 = 20.04, p < 0.0001), and their interaction
(F4,44 = 25.26, p = 0.043). Tukey–Kramer multiple-
Fig 1. (A) AMF spore abundance (per 15 g dry soil), (B) AMF species richness, and (C) AMF Shannon–Weaver Index in the rhizosphere of
pomegranates (Pome), limes, lemons, grapes, mangoes, and the pomegranate–cabbage mixed crop (P + C) grown in conventional (grey bars)
or organic (black bars) farming systems. The letters above the bars indicate signicant differences according to the Tukey–Kramer pairwise-
comparison test with a signicance level of α = 0.05. The data shown represent the means + SE (n = 5).
Mullath, et al .
Emir. J. Food Agric ● Vol 31 ● Issue 12 ● 2019 973
comparison testing (Fig. 1c) revealed that H′ values for
pomegranates, limes, grapes, and the pomegranate–
cabbage intercrop cultivated under organic farming were
signicantly different from those of grapes, mangoes, and
limes cultivated under conventional farming.
Distribution pattern of the AMF species detected
Twenty-four AMF species were identied in this study,
including four previously undescribed species (Table 2,
Fig. 2). Among the 11 species shared by both farming
systems, Rhizoglomus sp. UD-2 and UD-3 (Ambispora-
like) were present in all crops. The organically grown
pomegranates harbored the highest number of species
with a relative spore abundance (RSA) of 21.2% of
Rhizoglomus irregularis spores, followed by a 17.8% RSA for
Rhizoglomus sp. UD-2. Acaulospora excavata and Entrophospora
spp. contributed an RSA of only 1.2%. In contrast, the
rhizosphere of conventionally grown pomegranates was
dominated by Dominikia sp. UD-1, with an RSA of 78.9%.
The species A. excavata, Funneliformis mosseae,
Entrophospora spp., Glomus spp., P. scintillans, Septoglomus
titan, and Septoglomus constrictum were only associated with
pomegranates; Glomus pallidum and P. franciscana were only
associated with limes; and Cetraspora pellucida was only
associated with the pomegranate–cabbage mixed cropping
system. The remaining species were associated with more
than two to four crop plants. For instance, Rhizoglomus
fasciculatum was associated only with limes and lemons,
whereas Dominikia sp. UD.1 was only associated with
pomegranates, grapes, limes, and the mixed pomegranate–
Two major groups of AMF species were primarily recognized.
Group one consisted of species that were present and
generally abundant across most crop and farming-system
combinations like Rhizoglomus sp. UD.2, UD.3 (Ambispora-
like), R. irregularis, and F. coronatum. Group two consisted
of species with a more restricted distribution that were
mainly abundant in either farming system for a given crop.
The abundance of P. scintillans, S. titan, and Dominikia sp.
UD.1 was highest in conventionally grown pomegranates,
whereas Claroideoglomus claroideum and Cetraspora pellucida were
mainly associated with organically grown grapes and the
Table 2: Relative spore abundance (%) of arbuscular mycorrhizal fungi (AMF) across different crops and farming systems
Farming system Organic Conventional
Crop Pg†Lime Lemon Mango Grape Pg-C‡Pg†Lime Lemon Mango Grape
AMF species present in organic and conventional farming systems
Dominikia sp. §UD-1 - 19.9 - - 9.6 19.5 78.9 12.9 - - -
Rhizoglomus sp. UD-2 17.8 20.9 32.1 37.5 25.3 13.7 7.6 16.9 25.8 28.1 33.8
UD-3 (Ambispora-like) 17.5 23.9 55.4 37.8 13.6 17.9 3.8 30.8 58.4 49.1 38.1
Rhizoglomus irregularis 21.2 10.6 - 12.5 12.5 12.2 3.6 26.8 7.2 15.6 12.1
Diversispora eburna - 2.5 - 3.4 - - - 5.1 - - -
Pacispora scintillans 3.2 - - - - - 1.1 - - - -
Rhizoglomus intraradices - 2.7 12.5 - 3.8 - - - 4.3 - -
Funneliformis coronatum 17.1 4 - 4.5 9 6.8 - - 3.3 7.2 -
Glomus sp. 2.7 - - - - - 0.3 - - - -
Glomus macrocarpum 2.8 2.7 - - - - - - - - 5.2
Diversispora spurca - - - - 21.7 22.6 2.2 - - - 10.8
AMF species present in the organic farming system
Acaulospora excavate 1.2 - - - - - - - - - -
Acaulospora scrobiculata 2.5 1.7 - 4.3 - 2.8 - - - - -
Cetraspora pellucida - - - - - 2.3 - - - - -
Claroideoglomus claroideum 1.8 - - - 4.4 - - - - - -
Entrophospora sp. 1.2 - - - - - - - - - -
Glomus pallidum - 3.6 - - - - - - - - -
Pacispora franciscana - 0.9 - - - - - - - - -
Septoglomus constrictum 4.6 - - - - - - - - - -
Trichispora nevadensis 2.5 1.9 - - - 2.1 - - - - -
UD-4 (Ambispora-like) 3.9 4.7 - - - - - - - - -
AMF species present in the conventional farming system
Funneliformis mosseae - - - - - - 1.9 - - - -
Rhizoglomus fasciculatum - - - - - - - 7.5 1 - -
Septoglomus titan - - - - - - 0.6 - - - -
Total number of AMF
15 12 3 6 8 9 9 7 5 4 5
†Pg, pomegranate; ‡Pg-C, pomegranate–cabbage mixed cropping system; §UD, undescribed
Mullath, et al .
974 Emir. J. Food Agric ● Vol 31 ● Issue 12 ● 2019
grouped in Glomeraceae; three species were grouped in
Diversisporaceae; two each were grouped in Acaulosporaceae,
Pacisporaceae, and Ambisporaceae; and one each was grouped
in Entrophosporaceae, Claroideoglomeraceae, and Gigasporaceae.
The percentage of spores belonging to different families
was calculated separately for each crop and farming system
(Fig. 3a, b). Eight and four AMF families were detected in
the organic and conventional farming system, respectively.
The percentage of spores belonging to Glomeraceae was
highest in all crops under both farming systems except
for lemons, for which the highest percentage of spores
belonged to Ambisporaceae. Under organic farming,
pomegranates were associated with seven AMF families,
whereas lemons were only associated with two families.
Under conventional farming, the number of AMF families
associated with ve crops ranged from two to four.
ANOSIM was employed to assess differences in the
AMF community composition across the two farming
systems. With respect to the farming system, the value of
the ANOSIM was equal to 0.1267 (p = 0.001), using data
related to the presence or absence of different species.
Specifically, neither the species composition between
the conventional and organic farming systems, nor
within either farming system (across all crops) showed
Fig 2. Morphological characteristics of some of the spores detected
in this study. (A) Rhizoglomus sp. UD-2. (B) Tricispora nevadensis.
(C) Rhizoglomus irregulare. (D) Diversispora spurca. (E) Glomus
macrocarpum. (F) Rhizoglomus fasciculatum. (D) Dominikia sp. UD-1. (H)
Rhizoglomus intraradices. (I) Septoglomus constrictum. (J) Cetraspora
pellucida. (K) Acaulospora scrobiculata. (L) Funneliformis coronatum.
pomegranate–cabbage mixed cropping system, respectively.
In contrast, D. spurca was highly abundant in both cropping
systems. The remaining AMF species were mainly associated
with limes, lemons, and mangoes and were identied with
either or both farming systems.
Comparing the RSA across farming systems revealed that
UD-3 (Ambispora-like) was the most abundant species
under organic farming (23.8%) followed by Rhizoglomus sp.
UD-2 (22.6%), while A. excavata, Pacispora franciscana and
Entrophospora sp. occurred only rarely 0.2% (Table 3). In
the conventional system Dominikia sp. UD-1 (45.1%) was
the most abundant species followed by UD-3 (Ambispora-
like) (21.3 %).
AMF families identied in the study
The AMF species identied in this study were grouped
within eight families (Table 4). Twelve species were
Table 3: Relative spore abundance (RSA, %) of arbuscular
mycorrhizal fungi (AMF) across farming systems
AMF species RSA
Acaulospora excavata 0.2 0
Acaulospora scrobiculata 2 0
Cetraspora pellucida 0.5 0
Claroideoglomus claroideum 1.2 0
Diversispora eburna 0.9 0.75
Diversispora spurca 8.9 2.5
Entrophospora sp. 0.2 0
Funneliformis coronatum 7.9 1
Funneliformis mosseae 0 1.1
Glomus macrocarpon 1.1 0.6
Glomus pallidum 0.7 0
Glomus sp. 0.5 0.2
Pacispora franciscana 0.2 0
Pacispora scintillans 0.6 0.6
Rhizoglomus irregularis 12.8 9.4
Rhizoglomus fasciculatum 0 1.2
Rhizoglomus intraradices 2.3 0.5
Septoglomus constrictum 0.9 0
Septoglomus titan 0 0.4
Trichispora nevadensis 1.3 0
Dominikia sp. UD-1 9.8 45.1
Rhizoglomus sp. UD-2 22.6 15.7
UD-3 (Ambispora-like) 23.8 21.3
UD-4 (Ambispora-like) 1.7 0
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Emir. J. Food Agric ● Vol 31 ● Issue 12 ● 2019 975
marked dissimilarities. ANOSIM for individual crops and
either farming system was also performed. The species
compositions between the organic and conventional
farming groups were more dissimilar than the species
compositions within crops under the same farming system,
for pomegranates (R = 0.684, p = 0.005), limes (R = 0.854,
p = 0.011), and grapes (R = 0.824, p = 0.006). In contrast,
with mangoes (R = 0.062, p = 0.313) and lemons (R = 0.18,
p = 0.157), an even distribution of high and low ranks of
dissimilarity was observed within and between the groups,
suggesting that their species compositions between two
farming systems and within a farming system (replicates
of a given crop) were not dissimilar.
Organic versus conventional farming
AMF spore abundance, species richness, and diversity were
signicantly higher in organically managed soils than in
conventional ones. Similarly, positive effects of organic
farming on AMF communities have been reported in
other ecosystems (Oehl et al., 2004; Lee and Eom, 2009;
Verbruggen et al., 2010; Bedini et al., 2013; Säle et al., 2015).
An enhancement in AMF species richness under organic
farming compared to conventional farming has also been
observed in red peppers (Lee et al., 2008) and maize (Bedini
et al., 2013). Furthermore, it has been reported that AMF
from less intensively managed sites better promote plant
biomass production than AMF from sites with higher
management intensity (Johnson, 1993; Singh et al., 2008).
Hence, this may suggest that AMF-rich communities
from organically managed elds contribute more to plant
productivity and other ecosystem functions than do those
of conventionally managed elds.
The differences observed among the two farming systems
might be partially attributed to the quality and quantity of
the applied fertilizers. The use of mineral fertilizers can
have strong effects on fungal symbionts (Oehl et al., 2004,
Bünemann et al., 2006), further implying a net negative
effect on plant nutrition and growth (Verbruggen et al.,
2010). Indeed, the loss of fungal diversity can disrupt major
ecosystem services such as plant biodiversity, ecosystem
variability, and productivity (van der Heijden et al., 1998;
Wagg et al., 2014). Furthermore, it was observed that
AMF taxa might react differentially to external inuences.
Many of the identied AMF species belonging to the
Acaulospora, Entrophospora, Cetraspora, and Claroideoglomus
genera, appeared to be restricted to plots managed by
organic farming. Similar observations were reported
previously (Oehl et al., 2004). Wetzel et al. (2014) observed
that S. constrictum was more abundant under reduced tillage
and low-input agriculture, which is in line with observations
made in this study. In addition, Oehl et al. (2003) found that
Glomeraceae species were similarly abundant in all farming
systems, whereas Scutellospora species were more abundant
in organic systems than in conventional systems. These
Table 4 : Species of arbuscular mycorrhizal fungi (AMF)
identied within each family
AMF family AMF species
Acaulosporaceae Acaulospora excavata, Acaulospora
Diversisporaceae Diversipsora sp., Diversispora eburne,
Glomeraceae Funneliformis coronatum, Funneliformis
mosseae, Glomus macrocarpum,
Glomus pallidum, Glomus sp.,
Rhizoglomus irregularis, Rhizoglomus
fasciculatum, Rhizoglomus intraradices,
Septoglomus constrictum, Septoglomus
titan, Rhizoglomus sp. UD-2,
Dominikia sp. UD-1
Entrophosporaceae Entrophospora sp.
Pacisporaceae Pacispora scintillans, Pacispora
Ambisporaceae UD-4 (Ambispora-like), UD-3
Claroideoglomeraceae Claroideoglomus claroideum
Gigasporaceae Cetraspora pellucida
Fig 3. Distribution of AMF families (%) in the rhizosphere of different
crops grown (A) under organic farming and (B) under conventional
Mullath, et al .
976 Emir. J. Food Agric ● Vol 31 ● Issue 12 ● 2019
observations suggest that some taxa are more sensitive to
certain agricultural practices like tillage, fertilization, or the
use of fungicides than others. Because AMF species are
functionally important for natural ecosystems and low-input
sustainable farming, their loss under conventional farming
may negatively impact environmental and agronomical
services, and might affect multiple ecosystem functions.
Effect of host plants on AMF communities under
organic and conventional farming systems
AMF species compositions were found to be host
plant-dependent in this study. The rhizosphere of
pomegranates harbored the highest abundance and richness
of AMF species, in contrast to lemons, which had the
lowest values. These observations are in agreement with
results found in other ecosystems (Vandenkoornhuyse
et al., 2002, 2003; Gollotte et al., 2004; Scheublin et al.,
2004; Li et al., 2010; Alguacil et al., 2011). Sýkorovà et al.
(2007) showed that AMF communities differed signicantly
between the two co-existing host plants Gentiana verna
and Gentiana acaulis, but did not differ within the same
host plant at different locations. These observations
indicated the strong impact of host plant identity on the
AMF community composition and might be explained by
differences in the degree of AMF selectivity for certain
plant species. While some plants preferentially associate
with a broad spectrum of AMF species, others might favor
association with only few species, or with more specic and
specialized AMF (Oehl et al. 2003; Scheublin et al. 2004).
In this study, pomegranates harboring the highest AMF
abundance and richness might be considered the best host
for promoting the diversity of AMF communities. Similar
observations have been made by Deyn et al. (2011). They
reported that increased AMF abundance was explained
by plant species identity in the case of the grass species
Effect of agriculture on the natural AMF community
of native plants
Identifying AMF communities associated with various
crops under both farming systems, along with those of
native plant species was meant to shed light on the inuence
of crop introduction on native AMF communities. Any
shift in the AMF community composition would be
attributed to changes in the land-use pattern because the
underlying assumption is that the same AMF community
was present in all the three habitats (i.e., organic and
conventional farming systems, and undisturbed land with
native vegetation). However, no spores were detected
within the rhizosphere soil of the native plants. Potentially
present AMF species could be recovered by trap culturing
(Al-Yahya’ei et al., 2011) or through more intensive
sampling efforts and successive trap-culturing techniques
(Stutz and Morton 1996; Bever et al. 2001). The relatively
rich AMF communities observed within the two cultivated
systems were most likely stimulated by the establishment
of crop plants and the application of agricultural inputs
and irrigation. Such a trend of increasing AMF abundance
and richness upon initiation of agricultural land use is more
pronounced in desert ecosystems. In southern Arabia,
natural undisturbed habitats are directly exposed to harsh
climatic conditions, including pronounced drought (Cui
and Nobel 1992) and heat (Bendavid-Val et al. 1997). Only
a few plant species can withstand such conditions and,
consequently, the landscape is shaped by a scarce vegetation
cover. Thus, AMF lacking appropriate host plants fail
to propagate and hence, propagule numbers in the soil
decrease (Requena et al., 1996). Therefore, introducing
agriculture in such habitats represents a drastic change
in the environmental conditions, and thus a marked shift
in the AMF community is expected. Similar observations
of higher AMF diversity in agricultural sites than in
adjacent natural sites were reported for other hot and arid
ecosystems (Li et al., 2007 and Al-Yahya’ei et al., 2011).
AMF species detected in this study
Among all AMF species identied in this study, three out
of four novel species were among the most abundant
species. Hence, it can be assumed that those species
might be especially adapted to withstand and successfully
propagate under such extreme conditions. Adaptations of
AMF species to distinct environmental conditions, such
as drought or extreme temperatures, were already shown
and explained previously (Marulanda et al., 2007; López-
Gutiérrez et al., 2008; Lekberg & Koide, 2008; Antunes
et al., 2011).
In this study, 24 AMF species were detected in both farming
systems. Similar numbers were recorded in previous studies
conducted in southern Arabia (Al-Yahya’ei et al., 2011), the
arid ecosystem of Rajasthan, India (Verma et al., 2016),
and the sand dunes of Morocco (Hibilik et al., 2016).
However, the community composition seems to be quite
unique, with only one species in common with the AMF
community revealed from southern Arabia (Al-Yahya’ei et. al
2011; Symanczik et al., 2014a, b). In this sense, the study
signicantly contributes towards unfolding the mycorrhizal
diversity in the arid habitats of the Arabian Peninsula.
The present study showed that organic farming in desert
ecosystems is a suitable agricultural management strategy
with benecial effects on AMF biodiversity compared
to conventional farming. Therefore, our ndings should
help uncover the role that AMF might play in supporting
sustainable agriculture in desert ecosystems.
Mullath, et al .
Emir. J. Food Agric ● Vol 31 ● Issue 12 ● 2019 977
We thank the supporting team from Al Rawafed Farms. We
also thank Mr.Felix Guiabar from United Arab Emirates
University for his support in the soil chemical analysis.
This work was supported by the United Arab Emirates
University Program for Advanced Research [UPAR fund
No. 31 F043], which is gratefully acknowledged.
Mohamed Al-Yahya’ei initiated the project, collected the
soil samples and supervised all the technical aspects of
the experiments and result interpretations. He revised the
nal version of the manuscript. Sangeeta Kutty Mullath
Sarah Symanczik and Mohamed N. Al-Yahya’ei designed
the experiment. Sangeeta Kutty Mullath conducted the
experiments, collected and tabulated data and wrote the
manuscript. Byju N. Govindan performed the statistical
analysis of the data and helped in interpretation. Laila
Al Dhaheri assisted in taking observations and editing
the manuscript. Janusz Błaszkowski identied the spore
morphologies, helped in designing the experiment and
revising the manuscript. Sarah Symanczik interpreted the
results and revised the manuscript. All authors read and
approved the nal manuscript.
Alguacil, M. M., M. P. Torres, E. Torrecillas, G. Díaz and A. Roldán.
2011. Plant type differently promotes the arbuscular mycorrhizal
fungi biodiversity in their rhizospheres after revegetation of a
degraded, semiarid land. Soil Bio. Biochem. 43: 167-173.
Al-Yahya’ei, M. N., F. Oehl, M. Vallino, E. Lumini, D. Redecker,
A. Wiemken and P. Bonfante. 2011. Unique arbuscular
mycorrhizal fungal communities uncovered in date palm
plantations and surrounding desert habitats of Southern Arabia.
Mycorrhiza. 21: 195-209.
Antunes, P. M., A. M. Koch, K. E. Duneld, M. M. Hart, A. Downing,
M. C. Rillig and J. N. Klironomos. 2008. Inuence of commercial
inoculation with Glomus intraradices on the structure and
functioning of an AM fungal community from an agricultural site.
Plant Soil. 317: 257-266.
Augé, R. M. 2001. Water relations, drought and vesicular-arbuscular
mycorrhizal symbiosis. Mycorrhiza. 11: 3-42.
Bedini, S., L. Avio, C. Sbrana, A. Turrini, P. Migliorini, C. Vazzana and
M. Giovannetti. 2013. Mycorrhizal activity and diversity in a long-
term organic Mediterranean agroecosystem. Biol. Fertil. Soils.
Bendavid-Val, R., H. D. Rabinowitch, J. Katan and Y. Kapulnik. 1997.
Viability of VA-mycorrhizal fungi following soil solarization and
fumigation. Plant Soil. 195: 185-193.
Bever, J. D., P. A. Schultz, A. Pringle and J. B. Morton. 2001.
Arbuscular mycorrhizal fungi: More diverse than meets the eye,
and the ecological tale of why. Bioscience. 51: 923-931.
Brundrett, M., L. Melville and L. Peterson. 1994. Practical Methods in
Mycorrhiza Research. Mycologue Publications, Sydney.
Bünemann, E. K., G. D. Schwenke and L. Van Zwieten. 2006. Impact
of agricultural inputs on soil organisms a review. Aust. J. Soil
Res. 44: 379-406.
Cui, M. and P. S. Nobel. 1992. Nutrient status, water uptake and gas
exchange for three desert succulents infected with mycorrhizal
fungi. New Phytol. 122: 643-649.
Daniels, B. A. and H. D. Skipper. 1982. Methods for the recovery and
quantitative estimation of propagules from soil. In: N. C. Schenck
(Ed.), Methods and Principles of Mycorrhizal Research. The
American Phytopathological Society, St. Paul, pp. 29-35.
De Deyn, G. B., H. Quirk and R. D. Bardgett. 2011. Plant species
richness, identity and productivity differentially inuence key
groups of microbes in grassland soils of contrasting fertility. Biol.
Lett. 7: 75-78.
Fisher, M. and D. A. Membery. 1998. Climate. In: M. Fisher. and
D. A. Membery (Eds.), Geobotany: Vegetation of the Arabian
Peninsula. Kluwer Academic Publishers, Dordrecht, the
Netherlands, pp. 5-38.
Fitter, A. H. 2005. Darkness visible: Reections on underground
ecology. J. Ecol. 93: 231-243.
Galvez, L., D. D. Jr. Douds, L. E. Drinkwater and P. Wagoner.
2001. Effect of tillage and farming system upon VAM fungus
populations and mycorrhizas and nutrient uptake of maize. Plant
Soil. 118: 299-308.
Giovannetti, M., L. Avio, R. Barale, N. Ceccarelli, R. Cristofani,
A. Iezzi, F. Mignolli, P. Picciarelli, B. Pinto, D. Reali, C. Sbrana
and R. Scarpato. 2012. Nutraceutical value and safety of tomato
fruits produced by mycorrhizal plants. Br. J. Nutr. 107: 242-251.
Glennie, K. W. and A. K. Singhvi. 2002. Event stratigraphy,
paleoenvironment and chronology of SE Arabian deserts. Quat.
Sci. Rev. 22: 853-869.
Gollotte, A., D. van Tuinen and D. Atkinson. 2004. Diversity of
arbuscular mycorrhizal fungi colonising roots of the grass species
Agrostis capillaris and Lolium perenne in a eld experiment.
Mycorrhiza. 14: 111-117.
Gosling. P., A. Hodge, G. Goodlass and G. D. Bending. 2006.
Arbuscular mycorrhizal fungi and organic farming. Agric.
Ecosyst. Environ. 113: 17-35.
Gottshall, C. B., M. Cooper and S. M. Emery. 2017. Activity, diversity and
function of arbuscular mycorrhizae vary with changes in agricultural
management intensity. Agric. Ecosyst. Environ. 241: 142-149.
Hart, M. and R. Reader. 2002. Taxonomic basis for variation in the
colonization strategy of arbuscular mycorrhizal fungi. New
Phytol. 153: 335-344.
Hibilik, N., K. Selmaoui, J. Touati, M. Chliyeh, A. O. Touhami,
R. Benkirane and A. Douira. 2016. Mycorrhizal status of
Eryngium maritimum in the mobile dune of Mehdia (Northwest
of Morocco). Int. J. Pure Appl. Biosci. 4: 35-44.
IFOAM. 2006. The IFOAM Basic Standards for Organic Production
and Processing. Version 2005. IFOAM Publications, Germany.
Jansa, J., A. Mozafar and E. Frossard. 2005. Phosphorus acquisition
strategies within arbuscular mycorrhizal fungal community of a
single eld site. Plant Soil. 276: 163-176.
Johnson, N. C. 1993. Can fertilization of soil select less mutualistic
mycorrhizae? Ecol. Appl. 3: 749-757.
Koske, R. E. and B. Tessier. 1983. A convenient permanent slide-
mounting medium. Mycol. Soc. Am. Newsl. 34: 59.
Lee, J. E. and A. H. Eom. 2009. Effect of organic farming on spore
diversity of arbuscular mycorrhizal fungi and glomalin in soil.
Mycobiology. 37: 272-276.
Lee, S. W., E. H. Lee and A. H. Eom. 2008. Effects of organic farming
on communities of arbuscular mycorrhizal fungi. Mycobiology.
Mullath, et al .
978 Emir. J. Food Agric ● Vol 31 ● Issue 12 ● 2019
Lekberg, Y. and R. T. Koide. 2005. Is plant performance limited by
abundance of arbuscular mycorrhizal fungi? A meta-analysis
of studies published between 1988 and 2003. New Phytol.
Lekberg, Y. and R. T. Koide. 2008. Effect of soil moisture and
temperature during fallow on survival of contrasting isolates of
arbuscular mycorrhizal fungi. Botany. 86: 1117-1124.
Li, L., T. Li, Y. Zhang and Z. Zhao. 2010. Molecular diversity of
arbuscular mycorrhizal fungi and their distribution patterns
related to host-plants and habitats in a hot and arid ecosystem,
Southwest China. FEMS Microbiol. Ecol. 71: 418-427.
Li, L. F., T. Li and Z. W. Zhao. 2007. Differences of arbuscular
mycorrhizal fungal diversity and community between a cultivated
land, an old eld, and a never-cultivated eld in a hot and arid
ecosystem of southwest China. Mycorrhiza. 17: 655-665.
Littell, R. C., G. A. Milliken, W. W. Stroup, R. D. Wolnger and
O. Schabenberger. 2006. SAS for Mixed Models. 2nd ed. SAS
Institute Inc., Cary, NC.
López-Gutiérrez, J., G. Malcolm, R. T. Koide and D. Eissenstat. 2008.
Ectomycorrizal fungi from Alaska and Pennsylvania: Adaptation
of mycelial respiratory response to temperature? New Phytol.
Mäder, P., S. Edenhofer, T. Boller, A. Wiemken and U. Niggli. 2000.
Arbuscular mycorrhizae in a long-term eld trial comparing low-
input (organic, biological) and high-input (conventional) farming
systems in a crop rotation. Biol. Fertil. Soils. 31: 150-156.
Marulanda, A., R. Porcel, J. M. Barea and R. Azcón. 2007. Drought
tolerance and antioxidant activities in lavender plants colonized
by native drought-tolerant or drought-sensitive Glomus species.
Microb. Ecol. 54: 543-52.
Mozafar, A., T. Anken, R. Ruh and E. Frossard. 2000. Tillage
intensity, mycorrhizal and non- mycorrhizal fungi, and nutrient
concentrations in maize, wheat, and canola. Agron. J. 92:
Munkvold, L., R. Kjøller, M. Vestberg, S. Rosendahl and I. Jakobsen.
2004. High functional diversity within species of arbuscular
mycorrhizal fungi. New Phytol. 164: 357-364.
Neumann, E. and E. George. 2004. Colonisation with the arbuscular
mycorrhizal fungus Glomus mosseae (Nicol. and Gerd.)
enhanced phosphorus uptake from dry soil in Sorghum bicolor
(L.). Plant Soil. 261: 245-255.
Oehl, F., E. Sieverding, K. Ineichen, P. Mäder, T. Boller and
A. Wiemken. 2003. Impact of land use intensity on the species
diversity of arbuscular mycorrhizal fungi in agroecosystems of
central Europe. Appl. Environ. Microbiol. 69: 2816-2824.
Oehl, F., E. Sieverding, P. Mäder, D. Dubois, K. Ineichen, T. Boller
and A. Wiemken. 2004. Impact of long-term conventional and
organic farming on the diversity or arbuscular mycorrhizal fungi.
Oecologia. 138: 574-583.
Parniske, M. 2008. Arbuscular mycorrhiza: The mother of plant root
endosymbiosis. Nat. Rev. Microbiol. 6: 763-775.
Redecker, D., J. B. Morton and T. D. Bruns. 2000. Ancestral lineages
of arbuscular mycorrhizal fungi (Glomales). Mol. Phylogenet.
Evol. 14: 276-284.
Requena, N., P. Jeffries and J. M. Barea. 1996. Assessment of natural
mycorrhizal potential in a desertied semiarid ecosystem. Appl.
Environ. Microbiol. 62: 842-847.
Rillig, M. C. and D. L. Mummey. 2006. Mycorrhizas and soil structure.
New Phytol. 171: 41-53.
R Core Team. 2016. R. A Language and Environment for Statistical
Computing. R Foundation for Statistical Computing, Vienna,
Ryan, M. H., D. R. Small and J. E. Ash. 2000. Phosphorus controls
the level of colonisation by arbuscular mycorrhizal fungi in
conventional and biodynamic irrigated dairy pastures. Austr. J.
Exp. Agric. 40: 663-670.
Säle, V., P. Aguilera, E. Laczko, P. Mäder, A. Berner, U. Zihlmann,
M. G. A. van der Heijden and F. Oehl. 2015. Impact of
conservation tillage and organic farming on the diversity of
arbuscular mycorrhizal fungi. Soil Biol. Biochem. 84: 38-52.
Sasvári, Z., L. Hornok and K. Posta. 2011. The community structure
of arbuscular mycorrhizal fungi in roots of maize grown in a
50- year monoculture. Biol. Fertil. Soils. 47: 167-176.
Scheublin, T. R., K. P. Ridgway, J. P. W. Young and M. G. A. van der
Heijden. 2004. Nonlegumes, legumes, and root nodules harbor
different arbuscular mycorrhizal fungal communities. Appl.
Environ. Microbiol. 70: 6240-6246.
Singh, S., A. Pandey and L. M. S. Palni. 2008. Screening of arbuscular
mycorrhizal fungal consortia developed from the rhizospheres
of natural and cultivated tea plants for growth promotion in tea
[Camellia sinensis (L.) O. Kuntze]. Pedobiologia. 52: 119-125.
Smith, S. E. and D. J. Read. 2008. Mycorrhizal Symbiosis. Academic
Smukler, S. M., L. E. Jackson, L. Murphree, R. Yokota, S. T. Koike and
R. F. Smith. 2008. Transition to large-scale organic vegetable
production in the Salinas Valley, California. Agric. Ecosyst.
Environ. 126: 168-188.
Stutz, J. C. and J. B. Morton. 1996. Successive pot cultures reveal
high species richness of arbuscular endomycorrhizal fungi in
arid ecosystems. Can. J. Bot. 74: 1883-1889.
Sýkorovà, Z., A. Wiemken and D. Redecker. 2007. Co-occurring
Gentiana verna and Gentiana acaulis and their neighboring
plants in two Swiss upper montane meadows harbour distinct
arbuscular mycorrhizal fungal communities. Appl. Environ.
Microbiol. 73: 5426-5434.
Symanczik, S., J. Błaszkowski, G. Chwat, T. Boller, A. Wiemken and
M. N. Al-Yahya’ei. 2014a. Three new species of arbuscular
mycorrhizal fungi discovered at one location in a desert of
Oman: Diversispora omaniana, Septoglomus nakheelum and
Rhizophagus arabicus. Mycologia. 106: 243-259.
Symanczik, S., J. Błaszkowski, S. Koegel, T. Boller, A. Wiemken and
M. N. Al-Yahya’ei. 2014b. Isolation and identication of desert
habituated arbuscular mycorrhizal fungi newly reported from the
Arabian Peninsula. J. Arid Land. 8: 488-497.
Symanczik, S., P. E. Courty, T. Boller, A. Wiemken and M. N. Al-Yahya’ei.
2015. Impact of water regimes on an experimental community
of four desert arbuscular mycorrhizal fungal (AMF) species,
as affected by the introduction of a non-native AMF species.
Mycorrhiza. 25: 639-647.
van der Heijden, M. G. A., J. N. Klironomos, M. Ursic, P. Moutoglis,
R. Streitwolf-Engel, T. Boller, A. Wiemken and I. R. Sanders.
1998. Mycorrhizal fungal diversity determines plant biodiversity,
ecosystem variability and productivity. Nature. 396: 69-72.
Vandenkoornhuyse, P., R. Husband, T. J. Daniell, I. J. Watson
and J. M. Duck. 2002. Arbuscular mycorrhizal community
composition associated with two plant species in a grassland
ecosystem. Mol. Ecol. 11: 1555-1564.
Vandenkoornhuyse, P., K. Ridgway, I. J. Watson, A. H. Fitter and
J. P. W. Young. 2003. Co-existing grass species have distinctive
arbuscular mycorrhizal communities. Mol. Ecol. 12: 3085-3095.
Verbruggen, E., W. F. M. Roling, H. A. Gamper, G. A. Kowalchuk,
H. A. Verhoef and M. G. A. van der Heijden. 2010. Positive effects
of organic farming on below-ground mutualists: Large-scale
comparison of mycorrhizal fungal communities in agricultural
soils. New Phytol. 186: 968-979.
Emir. J. Food Agric ● Vol 31 ● Issue 12 ● 2019 979
Veresoglou, S. and M. Rillig. 2012. Suppression of fungal and
nematode plant pathogens through arbuscular mycorrhizal
fungi. Biol. Lett. 8: 214-217.
Verma, N., J. C. Tarafdar, K. K. Srivastava and B. Sharma. 2016.
Arbuscular mycorrhizal (AM) diversity in Acacia nilotica subsp.
indica (Benth.) Brenan under arid agroecosystems of western
Rajasthan. Int. J. Adv. Res. Biol. Sci. 3: 134-143.
Wagg, C., S. F. Bender, F. Widmer and M. G. A. van der Heijden.
2014. Soil biodiversity and soil community composition
determine ecosystem multifunctionality. Proc. Natl. Acad. Sci. U.
S. A. 111: 5266-5270.
Wetzel, K., G. Silva, U. Matczinski, F. Oehl and T. Fester. 2014.
Superior differentiation of arbuscular mycorrhizal fungal
communities from till and no-till plots by morphological spore
identication when compared to T-RFLP. Soil Biol. Biochem.