Pedosphere 25(3): 351–363, 2015

ISSN 1002-0160/CN 32-1315/P

c⃝ 2015 Soil Science Society of China

Published by Elsevier B.V. and Science Press

Cultivable Microfungal Communities Inhabiting Biological SoilCrusts in the Tengger Desert, China

Isabella GRISHKAN1,∗, JIA Rong-Liang2, Giora J. KIDRON3 and LI Xin-Rong2

1Institute of Evolution, University of Haifa, Mount Carmel, Haifa 31905 (Israel)2Shapotou Desert Research and Experiment Station, Cold and Arid Regions Environmental and Engineering Research Institute,

Chinese Academy of Sciences, 320 Donggang West Road, Lanzhou 730000 (China)3Institute of Earth Sciences, The Hebrew University of Jerusalem, Givat Ram Campus, Jerusalem 91904 (Israel)

(Received July 10, 2014; revised December 11, 2014)

ABSTRACT

Biological soil crusts are essential components of arid ecosystems. We examined the variations in microfungal communities in-

habiting different biological crust types in the vicinity of the Shapotou Research Station in the Tengger Desert, China. A total of

134 species from 66 genera were isolated using the soil dilution plate method. The mycobiota of the crusts from the Tengger Desert,

similar to that of the Negev Desert in Israel, was dominated by melanin-containing species with large multicellular spores. Abundance

of these xeric species increased spatially with increasing xeric conditions from moss-dominated to cyanobacterial crusts. Density of

microfungal isolates displayed the opposite trend and was positively correlated with chlorophyll content, indicating the possible sig-

nificant influence of organic matter content and wetness duration on fungal biomass. Within a chronosequence of the localities of

different periods after sand stabilization with revegetation, little variations were revealed in species composition and isolate density

of the crust microfungal communities, while a tendency towards a decrease in the community diversity level with the crust age was

noted Microfungal communities from stabilized localities differed from those of the natural localities in abundance of the dominant

and some frequent species, and in the fluctuations of diversity characteristics between the cyanobacterial and moss-dominated crusts.

The variations in mycobiotic parameters in the soil crusts of the Tengger Desert were apparently associated with the topographically

induced variations in abiotic conditions, while the differences in microfungal community of soil crusts between the Tengger and Negev

deserts, such as the significantly higher abundance of thermotolerant species in the crusts of the Tengger Deserts, were caused by

the principal differences in their precipitation regimes, associated with different rainy seasons, winter and summer in the Negev and

Tengger deserts, respectively.

Key Words: chlorophyll content, community structure, fungal diversity, precipitation regimes, revegetation, sand stabilization,

wetness duration

Citation: Grishkan, I., Jia, R. L., Kidron, G. J. and Li, X. R. 2015. Cultivable microfungal communities inhabiting biological soil

crusts in the Tengger Desert, China. Pedosphere. 25(3): 351–363.

INTRODUCTION

Biological soil crusts (BSCs), widely distributed

in arid and semiarid regions, make a significant con-

tribution to soil surface stabilization, hydrological

processes, and nutrient cycling (e.g., Warren, 1995;

Kidron and Yair, 1997; Kidron, 1999; Belnap and

Lange, 2001). Free-living microfungi, together with

heterotrophic bacteria, cyanobacteria, green algae,

lichens, and mosses, play a remarkable role in the com-

position and functioning of the BSCs. Nevertheless,

fungal diversity in crusts still remains poorly chara-

cterized.

Several studies conducted in the USA desert and

semiarid grasslands, based both on culture-dependent

methods (States and Christensen, 2001; States et al.,

2001) and on culture-independent molecular approa-

ches (Bates and Garcia-Pichel, 2009; Bates et al., 2010,

2012; Porras-Alfaro et al., 2011), revealed rich diver-

sity of crust-inhabiting fungi belonging mainly to the

phylum Ascomycota. A diverse fungal biota was al-

so recovered from the BSCs of the Arabian Desert

(Abed et al., 2013). These studies have characterized

the dominant and frequent taxa of crust fungal com-

munities and some aspects of their association with

different crust types and geographic regions.

In the Negev Desert of Israel, we studied cultivable

crust-inhabiting mycobiota along a precipitation gra-

dient (Grishkan et al., 2006) and within a dune catena

covered by different crust types at the Nizzana Re-

search Site (NRS) in the western Negev (Grishkan and

Kidron, 2013). In both studies, the BSC microfungal

∗Corresponding author. E-mail: grishkan@research.haifa.ac.il.

352 I. GRISHKAN et al.

communities, similar to those of the other Negev re-

gions, were dominated by melanin-containing species

with large multicellular conidia. Abundance of this xe-

ric group increased southward along the precipitation

gradient and towards the more xeric crusts within the

dune catena. Density of microfungal isolates was posi-

tively correlated with the chlorophyll content, indica-

ting the possible significant influence of organic matter

content and wetness duration on fungal biomass (Gri-

shkan and Kidron, 2013). The moss-dominated crusts

differ markedly from the cyanobacterial crusts in the

species relative abundance, diversity level, and isolate

density. There is similarity between the variations in

crust microfungal communities within the dune catena

at NRS (Grishkan and Kidron, 2013) and those along

the precipitation gradient (Grishkan et al., 2006) in the

Negev Desert, implying that microclimatic differences

and regional climatic variability may have a compara-

ble effect on microfungi.

Biological soil crusts occupy also parts of the Teng-

ger Desert in northern China. Although various as-

pects of crust composition, formation, and evolution

have been intensively investigated in this desert (e.g.,

Li et al., 2003, 2004, 2006, 2007, 2010; Jia et al.,

2008, 2012), nothing is known thus far about its crust-

inhabiting microfungal communities. The main goal of

the present research was to examine the composition

and structure of microfungal communities in different

crust types in the Tengger Desert, by analyzing the

species composition, contribution of the major taxo-

nomic and ecological groups to community structure,

the dominant groups of species, density of isolates, and

the diversity level (species richness, heterogeneity, and

evenness). The relationships between the above my-

cobiotic parameters and chlorophyll content was also

estimated following previous work that linked crust

biomass reflected in the chlorophyll content and sur-

face wetness duration (Kidron et al., 2009),

MATERIALS AND METHODS

Site description

This study was conducted in the Shapotou Re-

search Station (SRS) of the Cold and Arid Regions

and Environmental and Engineering Research Insti-

tute, Chinese Academy of Sciences, located in Zhong-

wei County in the Ningxia Hui Autonomous Region,

China, at the southeastern edge of the Tengger Desert

(37◦32′ N, 105◦02′ E, 1 340 m above the sea level). This

area is an ecotone between steppified desert and de-

sertified steppe, being also a transitional zone be-

tween sandy bare and revegetated deserts (Li et al.,

1998). The mean, minimum, and maximum annual

air temperatures reach 10.0, −25.1, and 38.1 ◦C, re-

spectively; the mean, maximum, and minimum an-

nual precipitations are approximately 186, 304, and

88 mm, respectively, 80% of which fall between May

and September (Li et al., 2003). The temperature of

crust surface (the south-exposed cyanobacterial crusts

at midday hours in July 2011) can reach 54 ◦C. Mois-

ture content of the crusts during dry periods is very

low and does not exceed 20 g kg−1. The vegetation

in the region is dominated by psammophytes, such

as Hedysarum scoparium Fisch., Agriophyllum squar-

rosum Moq., Stilpnolepis centiflora Krasch, and Pugio-

nium calcaratum Kom., covering about 1% of the area

(Li et al., 2004). The region consists of huge, dense, and

continuous reticulate barchan dunes with loose, im-

poverished, and mobile blown sand. The non-crusted

dunes (Arenosols, according to the FAO-UNESCO sys-

tem) consist of 99.7% of sand and only 0.3% of fine

particles (silt and clay). However, the BSCs contain

up to 30%–35% of fine particles (Li et al., 2006).

A non-irrigated vegetation system was initially es-

tablished in 1956 to protect the Baotou-Lanzhou rail-

way line from sand burial. This system, further ex-

panded in 1964, 1981, and 1987, included a com-

bination of windbreaks, straw checkerboard barriers,

and xerophytic shrubs (Duan et al., 2004). Following

surface stabilization, biological (cyanobacterial) soil

crusts began to colonize the dune surfaces. These crusts

were then gradually converted to moss and lichen

crusts (Li et al., 2003). Currently, the BSCs cover more

than 80% of the total revegetated desert sections. The

area is free from either grazing or trampling.

Sampling

Crust samples were collected in July 2011 and Au-

gust 2013 in the vicinity of the SRS. The crusts were

sampled across a chronosequence in accordance with

the years during which the revegetation took place,

1956, 1964, 1981, and 1987, and are hereafter referred

to as the crusts of 1956, 1964 1981, and 1987. The

samples were taken from four different crust types,

cyanobacterial crusts, mixed crusts (lichens, green al-

gae, cyanobacteria, and mosses in similar proportions),

and two moss-dominated types (one with Bryum ar-

genteum Hedw. and the other with Didymodon vinealis

(Brid.) Zand, hereafter referred to as moss-1 and moss-

2, respectively). In the locality of 1987, only the first

two crust types were sampled. The main crust pro-

perties are shown in Table I. A natural crust locality

(in the vicinity of Hongwei) and the south-facing slope

(SFS) and north-facing slope (NFS) of a non-stabilized

MICROFUNGAL COMMUNITIES IN BIOLOGICAL SOIL CRUSTS 353

TABLE I

Selected properties of the biological soil crusts from the locality of sand stabilization with revegetation in 1956 in the Tengger Desert,

China

Crust typea) Thick- pHb) Organic Chlorophyll Photoautotrophic speciesc)

nessb) C a and bCyanobacteriad) Lichense) Mossesf)

mm g kg−1 mg m−2

Cyanobacterial 2–4 7.42±0.26g) 0.6±0.2 40.4±5.4 MIC, PHO, NOS, OSC, SCH

Mixed 5–10 7.41±0.39 1.0±0.5 74.4±14.0 MIC, PHO, NOS, OSC, SCH COL, END BRY

Moss-1 10–15 7.93±0.05 13.2±0.5 108.5±21.5 MIC, PHO, NOS, OSC, SCH BRY, TORb, TORd

Moss-2 15–25 7.99±0.10 13.4±0.8 153.6±44.2 MIC, PHO, NOS, OSC, SCH DID, BAR, BRY

a)Moss-1 and Moss-2 are the two types of moss-dominated crusts.b)After Liu et al. (2006).c)After Li et al. (2010).d)MIC = Microcoleus vaginatus; PHO = Phormidium spp.; NOS = Nostoc sp.; OSC = Oscillatoria sp.; SCH = Schizothrix rupicola.e)COL = Collema tenax; END = Endocarpon pusillum.f)BRY = Bryum argenteum; TORb = Tortula bidentata; TORd = Tortula desertorum; DID = Didymodon vinealis; BAR = Barula

ditrichoides.g)Mean±standard deviation (n = 3–5).

and non-crusted sand dune were also sampled in 2011

as a control.

In 2011, all crusts were collected in accordance with

crust thickness (Table I). In 2013, the samples were

taken from the surface layer of the crusts (0.0–0.4 cm)

and from their subsurface layer (0.4–0.8 cm), except

for the cyanobacterial crusts where only the samples

of the 0.0–0.5 cm layer were collected. From each crust

type in each locality, 3–5 samples were taken. The sam-

ples were processed in the laboratory of the Institute of

Evolution, University of Haifa, Israel, within 2–6 weeks

after the sampling.

Isolation and identification of microfungi

Microfungi were isolated by means of the soil dilu-

tion plate method (Davet and Rouxel, 2000). Despite

certain limitations and biases, this method remains a

useful and valid approach for the initial characteriza-

tion of the ecology of fungal communities (e.g., Bills et

al., 2004). It is especially relevant for desert soils where

fungi may exist for a long period in a dormant (spore)

state.

Ten grams of each soil sample were used in a di-

lution series. Two culture media with different carbon

and nitrogen sources were employed: malt extract agar

(MEA) and Czapek’s agar (CzA) (Sigma-Aldrich Inc.,

St. Louis, USA). Streptomycin (Spectrum Chemical

Mfg. Corp, Gardens, USA) was added to each medi-

um (100 µg mL−1) to suppress bacterial growth. One

mL of soil suspension from the dilutions of 1:10–1:100

(soil:sterile water) was mixed with the agar medium

at 40 ◦C in Petri dishes (90-mm diameter). The plates

were incubated at 25 and 37 ◦C (the samples of 2011)

in darkness for 10–15 d (3 plates for each medium and

temperature).

After incubation, the emerging fungal colonies were

transferred to MEA and CzA for purification and fur-

ther taxonomic identification. In an attempt to in-

duce sporulation, all non-sporulating isolates were also

grown on oatmeal agar (Sigma-Aldrich Inc, St. Louis,

USA) as recommended by Bills et al. (2004) and on

water agar (20 g agar, 1000 mL water). Taxonomic i-

dentification was based on morphological characteris-

tics of fungal isolates. All names of species are cited

according to the database of Kirk et al. (2014).

Data and statistical analyses

Density of fungal isolates was expressed as colony

forming units (CFU) per g dry substrate for sand sam-

ples and crust samples collected in 2013, or per cm2

surface for crust samples collected in 2011 because of

sampling the crusts of various thickness. Analysis of

biodiversity was based on the Shannon-Wiener index

(H) and evenness (J) (J = H/Hmax, where Hmax is

the maximum H possible) (Krebs, 1999).

We analyzed spatial variations in the microfungal

community composition according to the variations in

the major desert group of melanin-containing micro-

fungi and separately of melanized species with large

multicellular spores. The contribution of each group

was estimated as an average of its density (number

of isolates of a particular group in the sample/total

number of all isolates in the sample, i.e., its relative

abundance in total isolate number in the sample) and

its relative abundance in the Shannon index (%) (Gri-

shkan et al., 2008).

Statistical analysis was conducted using the XL-

STAT statistical software (http://www.xlstat.com). We

354 I. GRISHKAN et al.

employed a one-way analysis of variance (ANOVA) fol-

lowed by multiple-comparison tests to compare da-

ta from different crusts on diversity characteristics,

contribution of melanin-containing species, and isolate

density. To evaluate similarity between microfungal

communities from different habitats, the clustering of

the communities based on species relative abundances

was made by the unweighed pair group average method

with the Euclidian distance as the distance coefficient.

The relationship of the characteristics of microfungal

communities with crust chlorophyll content was esti-

mated by linear regression analyses.

RESULTS

Composition and diversity of microfungal communities

The mycobiota isolated from the crusts sampled in

2011 and 2013 was composed of 123 and 67 identified

species, respectively. Altogether 134 species were iso-

lated: 6 of Mucoromycotina, 22 of teleomorphic (mor-

phologically sexual) Ascomycota, and 106 of anamor-

phic (asexual) Ascomycota. These species belonged to

66 genera, with the most common being Aspergillus

(12 species), Penicillium (8 species), Chaetomium (8

species), and Phoma (7 species). Twenty-three types

of microfungal strains remained non-sporulating in cul-

ture.

We isolated 72, 69, 80, 58, and 76 species from the

1956, 1964, 1981, and 1987 crusts sampled in 2011,

and from the natural locality, respectively. The com-

munities of the cyanobacterial crusts in each stabi-

lized locality were characterized by the lowest diversi-

ty indices, while the moss-2 crusts contained the most

even microfungal communities, although these diffe-

rences were mainly nonsignificant (Table II). In con-

trast, in the natural locality, the communities of the

moss-dominated crusts were characterized by the least

Shannon and evenness indices. The microfungal com-

munities of the non-stabilized sandy localities were the

most even among all communities studied (Table II). A

tendency towards an increase in the diversity indices

from 1956 to 1987 can be seen in the cyanobacteri-

al and mixed crusts of the stabilized localities. For all

crust types, the least heterogeneous and even micro-

fungal communities were found in the 1956 crusts.

We isolated 50, 46, and 58 species from the 1956,

1964, and 1981 crusts sampled in 2013, respectively.

The spatial tendencies revealed in the crusts sampled

in 2011 were less expressed, with only the Shannon

and evenness indices of the mixed crusts increasing

from 1956 to 1981, while the communities from the up-

permost 0.0–0.4 cm crust layer were significantly less

heterogeneous and even when compared with the com-

munities from the lower 0.4–0.8 cm crust layer (Table

III).

Melanin-containing microfungi super-dominated

TABLE II

Diversity characteristicsa) of microfungal communities in the biological soil crusts sampled in 2011 in localities after sand stabilization

with revegetation in 1956, 1964, 1981, and 1987, in natural crust localities, and on the south-facing slope (SFS) and north-facing slope

(NFS) of non-stabilized and non-crusted sand dunes (bare localities) of the Tengger Desert, China

Habitatb) 1956 1964 1981

S H J S H J S H J

Cyanobacterial crust 26cc) 1.88b 0.58b 36abc 2.22ab 0.62ab 37abc 2.36ab 0.65ab

Mixed crust 38abc 2.18ab 0.60ab 39abc 2.56ab 0.70ab 38abc 2.50ab 0.69ab

Moss-1 crust 44ab 2.42ab 0.64ab 39abc 2.45ab 0.67ab 43ab 2.50ab 0.66ab

Moss-2 crust 38abc 2.41ab 0.66ab 41ab 2.86a 0.77ab 47a 2.88a 0.75ab

SFS – – – – – – – – –

NFS – – – – – – – – –

Habitat 1987 Natural Bare

S H J S H J S H J

Cyanobacterial crust 42ab 2.61ab 0.70ab 43ab 2.87a 0.76ab – – –

Mixed crust 43ab 2.72ab 0.72ab 38abc 2.62ab 0.72ab – – –

Moss-1 crust – – – 32bc 2.33ab 0.64ab – – –

Moss-2 crust – – – 38abc 2.53ab 0.70ab – – –

SFS – – – – – – 43a 2.86a 0.76ab

NFS – – – – – – 37abc 2.92a 0.81a

a)S = number of species, including sterile strains; H = Shannon index; J = evenness.b)See Table I for descriptions of each crust type.c)Values followed by the same letter(s) within each characteristic are not significantly different (a one-way analysis of variance

(ANOVA), at the 5% level of probability).

MICROFUNGAL COMMUNITIES IN BIOLOGICAL SOIL CRUSTS 355

TABLE III

Diversity characteristicsa) of microfungal communities in surface (0.0–0.4 cm) and subsurface (0.4–0.8 cm) layers of the biological soil

crusts sampled in 2013 in localities after sand stabilization with revegetation in 1956, 1964, and 1981 in the Tengger Desert, China

Crust typeb) Layer 1956 1964 1981

S H J S H J S H J

cm

Cyanobacterial 0.0–0.4 21bcdc) 1.88cde 0.62abc 23abc 1.94cde 0.62efg 23abc 1.75de 0.56gh

Mixed 0.0–0.4 18bcd 1.38ef 0.48h 23abc 1.73def 0.55gh 27ab 2.08abc 0.63efg

0.4–0.8 14de 2.19abc 0.82ab 10e 1.66def 0.72bcd 17cde 2.17abc 0.77abc

Moss-1 0.0–0.4 21bcd 1.99bcd 0.65def 24abc 1.99bcd 0.63efg 24abc 2.05bcd 0.65def

0.4–0.8 20bcd 2.51ab 0.84a 20bcd 2.01bcd 0.67def 24abc 2.22abc 0.69cde

Moss-2 0.0–0.4 19bcd 1.98bcd 0.67cde 24abc 2.41ab 0.76abc 22bcd 1.95cde 0.63efg

0.4–0.8 26abc 2.42abc 0.74abc 22bcd 2.01bcd 0.65def 33a 2.44ab 0.70cde

a)S = number of species, including sterile strains; H = Shannon index; J = evenness.b)See Table I for descriptions of each crust type.c)Values followed by the same letter(s) within each characteristic are not significantly different (a one-way analysis of variance

(ANOVA), at the 5% level of probability).

all communities studied (Tables IV and V); they com-

prised 67% of the total species number and 51.4%–94%

of the contribution index (Fig. 1). The main cores of

melanin-containing fungi were represented by species

with large (> 20 µm) multicellular spores such as

Embellisia phragmospora, Alternaria alternata, Ulocla-

Fig. 1 Spatial dynamics of contribution of melanin-containing species and melanized fungi with large multicellular spores in biological

soil crusts in localities after sand stabilization with revegetation in 1956 (a), 1964 (b), 1981 (c), and 1987(d), in natural crust localities

(e), on the south-facing slope (SFS) and north-facing slope (NFS) of non-stabilized and non-crusted sand dunes (bare localities) (f),

and in surface and subsurface crust layers in localities after sand stabilization with revegetation in 1956 (g), 1964 (h), and 1981 (i)

in the Tengger Desert, China. Bars with the same letter(s) within the melanin-containing species or the melanized fungi with large

multicellular spores are not significantly different at the 5% level of probability. CB, MIX, M1, and M2 are the abbreviations of crust

types: cyanobacterial, mixed, moss-1, and moss-2, respectively. See Table I for descriptions of each crust type. Abbreviations with

−0 and −1 indicate surface and subsurface crust layers, respectively.

356 I. GRISHKAN et al.

TABLE IV

Average relative abundance of common microfungal species from different biological soil crust types (cyanobacterial (CB), mixed

(MIX), moss-1 (M1), and moss-2 (M2) crusts)a) in the localities after sand stabilization with revegetation in 1956, 1964, 1981, and

1987, in natural crust localities, and on the south-facing slope (SFS) and north-facing slope (NFS) of non-stabilized and non-crusted

sand dunes (bare localities) in the Tengger Desert, China

Species 1956 1964 1981 1987 Natural Bare

CB MIX M1 M2 CB MIX M1 M2 CB MIX M1 M2 CB MIX CB MIX M1 M2 SFS NFS

%

MucoromycotinaMortierella humilis – – – – 0.2 – 0.2 – – – – – 0.4 – – 0.1 0.1 1.2 – –

Rhizopus oryzaeb) 0.7 0.6 0.4 – 0.2 – 0.5 0.5 0.3 0.7 0.3 0.3 1.0 0.9 – 0.1 0.2 – 2.3 3.8Teleomorphic Ascomycota

Canariomyces nota- 0.6 2.6 0.9 1.6 1.2 2.6 2.8 3.9 1.4 0.2 0.5 0.8 0.3 2.1 4.2 0.9 1.4 3.3 0.1 0.1

bilisb)

Chaetomium atrobru- – 0.3 – – – – – – – 0.3 0.2 0.3 0.4 6.8 – 0.9 – – 1.2 –

nneumb)

Chaetomium globosumb) – – – – – – 0.7 0.3 0.3 0.1 – – – – – – 0.5 – – –Chaetomium struma- 2.3 2.0 1.5 0.4 2.5 5.5 3.1 4.3 2.3 5.6 3.2 1.7 3.4 2.8 4.1 1.8 0.7 1.6 2.3 0.6

riumb)

Aspergillus nidulans – 0.6 1.0 – 0.6 0.8 0.9 1.7 – – 0.2 – – – 1.1 0.1 – 1.1 2.3 0.4Aspergillus rugulosus 2.0 0.1 0.8 4.1 0.2 5.6 1.0 2.9 1.1 1.1 1.4 1.3 0.4 0.3 0.3 – – 0.8 – –

Thielavia terricolab) – – – – – – – 0.2 0.6 – – – – – 0.3 – – – – –

Anamorphic Ascomycota

Alternaria alternatab) 12.9 9.9 5.5 6.5 14.1 19.6 3.5 6.6 10.2 15.6 5.2 7.4 19.2 18.7 17.4 20.0 8.0 21.0 18.4 14.2Aspergillus fumigatus 1.4 0.8 1.1 0.1 0.4 0.5 0.8 1.1 1.0 0.4 0.4 1.2 1.4 0.8 0.4 0.2 0.1 0.1 6.1 3.5

Aspergillus nigerb) – 0.1 0.1 0.1 – – – 0.2 – 0.5 – – 0.2 – 0.1 0.1 – – 0.4 0.4

Boeremia exiguab) 10.1 4.2 7.0 8.9 4.4 2.0 2.0 1.5 7.9 2.8 4.4 2.6 9.1 7.9 1.5 4.6 1.7 1.9 2.4 5.3Cladosporium cladospo- 2.4 1.2 0.1 2.7 1.7 1.0 0.6 1.3 1.5 3.7 1.8 5.9 1.9 3.4 1.8 1.9 2.0 3.4 3.3 9.3

rioidesb)

Coleophoma empetrib) 0.5 – – – 0.5 0.4 – 0.8 1.1 0.6 0.4 0.8 0.5 0.4 0.1 – 0.1 0.1 1.6 0.4

Curvularia inaequalesb) 0.9 – 2.2 0.3 – 0.2 0.9 0.3 2.0 3.0 2.9 0.5 1.4 0.2 – – – – – 0.4

Curvularia spiciferab) 0.5 0.4 0.3 0.3 0.7 0.5 0.8 – 0.1 0.5 – 0.4 0.9 0.5 0.5 0.4 – 0.2 0.8 0.4Drechslera demati- – 0.3 0.1 0.1 6.2 0.8 0.5 4.6 0.1 0.4 0.2 1.1 0.3 – 1.1 2.1 2.0 2.4 0.8 –

oideab)

Embellisia phragmos- 52.0 44.0 44.0 33.7 51.6 38.5 47.3 34.0 47.8 35.7 43.4 24.2 26.8 29.4 18.7 27.5 26.2 21.0 14.7 13.4

porab)

Fusarium oxysporum 0.1 7.7 2.9 0.1 1.7 3.6 9.4 7.9 6.1 9.4 15.0 15.6 6.8 10.6 9.0 11.8 29.0 20.0 15.3 9.0Gibberella intricans 2.6 – 9.3 23.1 0.2 – – – – 1.8 0.6 3.0 – – – – – 0.3 – –

Gilmaniella humicolab) 0.5 8.0 0.5 0.7 – – – – – 0.6 – 0.2 0.4 – – – – 0.6 – –

Monodictys fluctuatab) – – – – – 0.2 – – – 1.6 – – 0.5 – 9.9 – 1.2 – – –Myrothecium verrucaria 0.2 – 0.2 0.3 0.9 0.4 1.5 1.8 0.4 0.2 1.1 – 1.7 0.6 – 1.1 0.2 0.7 – –

Papulaspora pannosab) – – – – – 0.4 0.3 0.3 0.2 – 0.4 0.4 0.8 0.2 0.4 – 0.2 0.6 0.8 –Penicillium aurantio- – – – – – 0.2 4.1 2.1 1.2 0.5 1.2 3.4 0.2 0.8 – 0.1 0.1 0.2 – –griseum

Phoma medicaginisb) – 0.8 0.3 0.1 0.2 – – – – – – – – – 3.5 2.4 0.9 3.0 0.4 –

Pyrenochaeta cavab) 1.6 – 1.4 2.2 0.8 1.0 1.7 – 3.3 0.3 1.9 0.6 – 0.5 1.5 2.6 11.0 1.1 0.4 –

Septoria sp.b) – 3.3 – – – – – – – – – – – – 3.0 9.9 – 3.8 – –

Setosphaeria rostratab) 0.7 0.4 1.9 1.6 0.2 2.8 3.3 7.2 1.2 0.7 4.7 10.2 1.6 4.3 0.3 1.0 2.2 1.8 – –Stachybotrys charta- 0.6 0.5 1.5 0.6 0.3 0.9 0.6 1.5 0.4 0.5 0.6 2.0 0.6 1.3 1.3 0.3 0.4 0.9 2.6 4.1

rumb)

Talaromyces variabilis – 0.8 0.2 0.3 – 0.2 0.2 0.3 0.4 0.2 0.1 0.1 – 0.8 0.3 – – – – –Trichoderma koningii – – 0.1 – – 1.2 0.5 – – – 0.3 – 0.3 – – – – – 0.6

Ulocladium atrumb) 3.5 3.2 4.2 3.0 8.5 5.1 7.5 5.1 4.5 5.0 3.2 5.5 10.3 4.7 6.3 5.1 6.3 2.8 1.9 2.5Westerdykella capitu- 0.4 – 6.9 0.3 – – – 0.5 – 1.2 – – – – – 0.1 – – – –

lumb)

Diplodia sp.b) – – – – – – – – 0.8 0.5 – – – – 1.6 1.4 – 0.2 – –

Mycelia sterilia

Dark-colored 1b) – 0.7 – – – – 1.6 5.2 2.4 3.2 1.0 0.8 – 0.6 – – – 0.3 1.2 –

Dark-colored 2b) – – – – 0.2 0.2 1.3 – – – 0.2 0.2 0.3 0.9 3.0 0.2 0.3 0.9 11.1 8.9

a)See Table I for descriptions of each crust type.b)Melanin-containing species.

MICROFUNGAL COMMUNITIES IN BIOLOGICAL SOIL CRUSTS 357

TABLE V

Average relative abundance of common microfungal species from the surface (0.0–0.4 or 0.0–0.5 cm) and subsurface (0.4–0.8 cm) layers

of different biological soil crust types (cyanobacterial (CB), mixed (MIX), moss-1 (M1), and moss-2 (M2) crusts)a) in the localities

after sand stabilization with revegetation in 1956, 1964, 1981, and 1987 in the Tengger Desert, China

Species 1956 1964 1981

CB MIX M1 M2 CB MIX M1 M2 CB MIX M1 M2

0.0– 0.0– 0.4– 0.0– 0.4– 0.0– 0.4– 0.0– 0.0– 0.4– 0.0– 0.4– 0.0– 0.4– 0.0– 0.0– 0.4– 0.0– 0.4– 0.0– 0.4–0.5 0.4 0.8 0.4 0.8 0.4 0.8 0.5 0.4 0.8 0.4 0.8 0.4 0.8 0.5 0.4 0.8 0.4 0.8 0.4 0.8cm cm cm cm cm cm cm cm cm cm cm cm cm cm cm cm cm cm cm cm cm

%Mucoromycotina

Mortierella humilis – 0.9 15.0 – 1.8 – – 3.5 – 36.0 – – – – – 0.3 8.7 – 0.4 – 0.8

Rhizopus oryzaeb) 0.3 0.5 – – – – – 0.2 0.2 – – – 0.4 – – 0.5 10.8 0.2 – – 0.4

Teleomorphic Ascomy-cota

Canariomyces nota- – – – – – 0.2 1.4 0.2 – – 1.4 1.5 0.4 – 1.4 1.0 – – 1.3 – 3.2

bilisb)

Chaetomium artrobru- 1.2 0.4 1.4 – 0.9 – – – – – – 0.5 – – – – 20.0 0.2 – – 0.4

nneumb)

Chaetomium struma- 0.9 0.7 – 0.9 – – 0.9 – 0.9 – 0.5 3.0 1.5 1.9 – 0.3 – 1.8 0.4 – 2.0

riumb)

Aspergillus nidulans – 0.5 – – – – 0.5 0.5 0.4 8.5 1.0 – – – – 0.3 – 5.8 – – 0.4

Sporormiella minimab) – – – – – – – – – – – – – – – 0.5 0.5 – 0.4 – 0.8

Immature fruit bodiesb) – – – – – – – 0.3 0.4 1.2 – 1.0 – – – – – – 0.9 – –

Anamorphic Ascomycota

Alternaria alternatab) 8.6 5.8 3.5 4.7 – 5.2 3.8 7.5 6.6 – 6.8 3.5 5.9 2.2 5.8 11.5 2.6 6.8 6.0 9.7 5.6Aspergillus fumigatus 1.2 – 10.7 – 12.7 0.2 4.7 0.9 0.5 1.2 – 2.5 – 0.7 – 0.3 23.1 0.6 5.6 0.2 5.2

Aspergillus ustusb) – – 17.7 – 0.9 – – – – – – – – – – – – – – – –

Boeremia exiguab) 4.8 1.1 1.4 9.1 2.7 8.1 5.6 7.0 0.7 – 2.2 0.5 – – 2.0 3.4 0.5 2.2 – 4.7 2.0Cladosporium clados- 1.8 1.4 1.4 – – – 1.4 2.0 1.7 – 2.6 1.0 4.8 – 1.6 2.4 0.5 1.4 – 1.9 1.2

porioidesb)

Coleophoma empetrib) 16.0 3.3 – 0.2 – – 0.9 2.2 3.0 – 4.3 – 1.5 0.4 1.6 – – 2.2 1.7 1.2 2.0Curvularia inaequa- – 0.2 – – – 0.4 – – 0.2 – – – – 0.4 0.8 – – – – – –

les b)

Curvalaria spiciferab) 0.9 0.2 0.4 0.3 0.4 0.5 0.2 2.3 0.4Embellisia phragmos- 41.8 17.7 11.4 37.4 25.5 37.3 42.3 51.3 54.6 37.3 44.3 48.0 37.7 47.0 66.0 47.8 13.9 31.2 37.0 36.0 34.4

porab)

Fusarium oxysporum – – – – – – 2.3 – – – 0.2 – – – – 0.8 – 1.2 1.7 2.1 4.8Gibberella intricans 10.0 0.7 – 9.6 12.7 7.0 1.4 1.7 0.9 3.1 5.0 – 6.6 6.3 9.4 3.2 1.5 0.2 1.3 3.1 2.8Myrothecium verruca- – – – 0.7 – – 0.9 10.0 – – – – 2.9 – – – – – – – –ria

Papulaspora pannosab) 1.2 – – – 0.9 0.4 0.5 – – – – – 0.4 0.7 0.2 – – – – 0.2 0.4Penicillium aurantio- – 0.7 – 0.2 – – 1.9 – – – 0.2 – 1.5 1.1 – – – – – – –griseum

Phoma medicaginisb) – – – – 1.8 6.0 – – – – 0.3 – – 0.4 0.4 – – – – – –

Pyrenochaeta cavab) 2.4 62.5 25.6 27.5 11.0 0.9 – 9.4 21.3 15.7 23.5 15.5 19.3 15.6 3.0 8.6 12.3 1.4 14.7 3.0 0.8

Septoria sp.b) – – – – – 25.2 15.7 – – – – – – – – 0.3 – 33.8 4.3 28.0 6.0

Setosphaeria rostratab) 1.8 1.1 2.1 1.8 0.9 4.0 1.4 1.4 0.7 – 5.1 4.0 2.9 8.5 0.2 2.2 – 4.8 0.4 1.2 2.0Stachybotrys charta- – 0.7 – 0.2 – – 1.9 – – – 0.2 – 1.5 1.1 – – – – – – –

rumb)

Talaromyces variabilis 0.3 0.5 – 0.2 2.7 0.2 – 0.2 0.4 – 0.2 1.0 0.7 0.7 – – 3.6 0.4 0.4 0.2 2.4Trichoderma koningii – – – – – – 0.5 – – – – – – – – 2.9 – 0.2 – – –

Ulocladium atrumb) – – – – – – 0.4 – – – 0.2 – 1.8 0.7 0.2 – – – – 0.4 –Westerdykella capitu- – – – – 6.4 – – 0.5 – – – 7.5 – – 1.8 2.9 – – 3.0 0.5 –

lumb)

Mycelia sterilia

Dark-colored 1b) – – 1.4 1.3 – 0.2 5.2 0.5 – – 0.3 – 3.3 6.3 – – – 0.2 13.3 – 13.2

Dark-colored 2b) – – 1.4 – 0.9 – – – – – 0.2 – – – – – – – 0.4 – 0.4

Dark-colored 3b) – – – – 3.6 – – – – – – – – – 0.6 0.5 – – – – –Light-colored 1.2 – 7.1 – 1.8 – – – – – – – – – 0.4 0.5 – – – – 0.8

a)See Table I for descriptions of each crust type.b)Melanin-containing species.

358 I. GRISHKAN et al.

dium atrum, Setosphaeria rostrata, Drechslera demato-

idea, Curvularia spicifera, and Curvularia inaequales,

with 42.4%–72.3% and 43.1%–49.5% of contribution in

the stabilized and natural localities of 2011, respective-

ly (Fig. 1a–e). In the bare localities, the contribution

of these species was significantly lower (Fig. 1f). Abun-

dance of melanized fungi, especially those with large

multicellular spores, accounted for the remarkable

differences between the surface and subsurface crust

layers, especially in the mixed crusts (Fig. 1g–i). Diffe-

rences in the abundance of melanin-containing species

between crust types (higher in the cyanobacterial

(2011) or mixed (2013) crusts and lower in the moss-

dominated crusts) were much less expressed.

Except for the species mentioned above, the most

abundant and frequently occurring species in the

studied localities are Boeremia exigua, Cladosporium

cladosporioides, Fusarium oxysporum, Gibberella in-

tricans, Stachybotrys chartarum, Coleophoma empe-

tri, Pyrenochaeta cava, Canariomyces notabilis, Chae-

tomium strumarium, Aspergillus nidulans, Aspergillus

fumigatus, and Myrothecium verrucaria. The natural

crusts and bare habitats differed from the crusts of the

stabilized localities with remarkably lower abundance

of the main dominant species, E. phragmospora (Table

IV). In the majority of the natural crusts, some light-

colored fungi, mainly F. oxysporum, were isolated with

higher abundance. In the microfungal communities of

the bare habitats, such species as Rhizopus oryzae, As-

pergillus fumigatus, and Stachybotrys chartarum were

more abundant together with the dark-colored non-

sporulating isolates.

Apart from the lower contribution of melanin-

containing fungi, the 0.4–0.8 cm crust layer had consis-

tently higher abundance of Aspergillus fumigatus than

the 0.0–0.4 cm layer. The main temporal differences

between the microfungal communities of the stabilized

crusts were expressed in lower abundance and frequen-

cy of occurrence of the teleomorphic Canariomyces no-

tabilis, Chaetomium strumarium, and Aspergillus ni-

dulans and in higher abundance of Pyrenochaeta cava

in the localities sampled in 2013 as compared to 2011.

At 37 ◦C, the microfungal community composi-

tion was substantially different from that at 25 ◦C.

The dominant and frequent melanin-containing species

with multicellular spores did not grow at 37 ◦C, and

the teleomorphic species, including Canariomyces no-

tabilis, Chaetomium strumarium, and Aspergillus nidu-

lans, and the anamorphic Aspergillus species, including

Aspergillus fumigatus and Aspergillus niger, as well as

Rhizopus oryzae, were the most abundant fungi.

Cluster analysis based on relative abundances of

species separated the microfungal communities of 2011

into two groups. The first group contained the com-

munities from the majority of stabilized crust loca-

lities. The second group consisted of the communities

from the natural crusts and bare localities, as well as

those from the moss-2 crusts of 1981 and cyanobac-

terial and mixed crusts of 1987 (Fig. 2a). Yet, these

two groups were characterized by comparatively high

similarity (dissimilarity less than 30%, except for the

moss-2 crust community of 1956). Among the commu-

nities from the stabilized crust localities, no distinct

pattern was revealed in grouping either based on the

crust types or localities. Similar absence of a clear pat-

tern was found in clustering the microfungal communi-

ties of 2013 (Fig. 2b). In most cases, the communities

from the 0.0–0.4 cm layer were more similar to each

other than to the communities from the corresponding

0.4–0.8 cm layers.

Density of microfungal isolates

In the crusts sampled in 2011, the CFU numbers

varied from 3 600 to 11 600 (the stabilized localities)

and from 4 400 to 9 800 cm−2 crust surface (the na-

tural localities). In each stabilized locality, the moss-2

crusts contained a significantly higher isolate density

(Fig. 3a–c). In the bare localities, the isolate density

(200–320 per g dry substrate) was 11–58-fold lower

than in the localities of the stabilized crusts.

In the crusts sampled in 2013, significant differen-

ces were found between the 0.0–0.4 and 0.4–0.8 cm lay-

ers: in the 0.0–0.4 cm layers, the CFU numbers were

2.2–4.7-fold higher than those in the 0.4–0.8 cm layers

(Fig. 3f–h). Differences in isolate density between crust

types (higher in the moss-dominated crusts and lower

in the cyanobacterial or mixed crusts) were much less

expressed.

Relationships of mycobiotic characteristics with chloro-

phyll content

A highly significant (P < 0.001) positive linear

relationship was found between isolate density and

chlorophyll content (Fig. 4c). Abundance of melanin-

containing species on a whole, as well as that of

melanized fungi with large multicellular spores, also

displayed a significant (P < 0.05) but negative linear

correlation with chlorophyll content (Fig. 4a, b). None

of the diversity characteristics (species richness, hete-

rogeneity, and evenness) showed any significant rela-

tionship with chlorophyll content.

MICROFUNGAL COMMUNITIES IN BIOLOGICAL SOIL CRUSTS 359

Fig. 2 Clustering of the microfungal communities in the biological soil crusts from localities after sand stabilization with revegetation

in 1956, 1964, 1981, and 1987, in natural crust localities (NAT), and on the south-facing slope (SFS) and north-facing slope (NFS) of

non-stabilized and non-crusted sand dunes (bare localities, BARE) (a), and in the surface and subsurface layers of the crusts in localities

after sand stabilization with revegetation in 1956, 1964, and 1981 (b) in the Tengger Desert, China. CB, MIX, M1, and M2 are the ab-

breviations of crust types: cyanobacterial, mixed, moss-1, and moss-2, respectively. See Table I for descriptions of each crust type.

Abbreviations with −0 and −1 indicate surface and subsurface crust layers, respectively.

Fig. 3 Spatial dynamics of fungal isolate density, expressed as colony forming units (CFU), in the biological soil crusts of localities

after sand stabilization with revegetation in 1956 (a), 1964 (b), 1981 (c), and 1987(d), in natural crust localities (e), and in the surface

and subsurface layers of the crusts in localities after sand stabilization with revegetation in 1956 (f), 1964 (g), and 1981 (h) in the

Tengger Desert, China. Bars with the same letter(s) are not significantly different at the 5% level of probability. CB, MIX, M1, and

M2 are the abbreviations of crust types: cyanobacterial, mixed, moss-1, and moss-2, respectively. See Table I for descriptions of

each crust type. Abbreviations with −0 and −1 indicate surface and subsurface crust layers, respectively.

DISCUSSION

Expectedly, the general picture of fungal species

composition in the crusts from the Tengger Desert is

analogous to that of other deserts. This is mainly due

to the super-dominance of melanin-containing species

both in number and abundance which is considered a

typical attribute for almost all mycologically studied

arid soils (e.g., Ranzoni, 1969; Christensen, 1981; Hal-

wagy et al., 1982; Skujins, 1984; Abdullah et al., 1986;

360 I. GRISHKAN et al.

Fig. 4 Relationships of the abundance of melanin-containing species (a), the abundance of melanized fungi with large multicellular

spores (b), and the density of fungal isolates expressed as colony forming units (CFU) (c) with chlorophyll content in the biological

soil crusts in the Tengger Desert, China.

Hashem, 1991; Ciccarone and Rambelli, 1998; Zak,

2005). This was also found in the Israeli Negev Desert

crusts (Grishkan and Kidron, 2013) as well as in other

Negev soils (Grishkan et al., 2006, 2007; Grishkan and

Nevo, 2010). Similarly, prevalence of melanized fungi

with large multicellular spores revealed in the Teng-

ger crusts was also characteristic of most localities of

the Negev Desert. These fungi, belonging to the order

Pleosporales, were also dominant in the communities

of the crusts sampled on the Colorado Plateau, the

Chihuahuan Desert, the Sonoran Desert, and the semi-

arid grassland in central New Mexico, USA (Bates and

Garcia-Pichel, 2009; Bates et al., 2010, 2012; Porras-

Alfaro et al., 2011). These studies along with our sur-

vey suggest that dark pigmentation together with mul-

ticellular spore morphology is crucial for dispersal and

resting functions in climatically stressful desert habi-

tats.

Distribution of different crust types at the SRS dis-

plays a clear spatial pattern, which apparently influ-

ences the distribution of crust microfungi. With the

cyanobacterial crusts mainly covering the south-facing

slope and the moss-dominated crusts being mostly con-

fined to the north-facing slope and low depressions, the

spatial distribution of these crusts may reflect water

availability at the site. Rainfall is the main source of

water in the area (e.g., Li et al., 2009), but due to

up to 10–15 ◦C higher midday surface temperatures,

much higher evaporation rates characterize the south-

facing slope in comparison with the other positions,

similar to the conditions recorded in the Negev Desert

(Kidron et al., 2000). As a result, a substantially shor-

ter wetness duration (and thus short period of acti-

vity of microorganisms) is typical for the south-facing

slope, which is in agreement with the data obtained

from the NRS (Kidron et al., 2009). Because of the

close link between surface wetness duration and the

crust chlorophyll content, these relatively short hours

of activity may explain the less developed state of the

cyanobacterial crusts and their lowest chlorophyll con-

tent (Table I). Alternatively, longer wetness duration

and subsequently longer hours of activity on the north-

facing slope and some of the depressions may explain

the transition to moss-dominated crusts (Kidron et al.,

2010) with greater crust thickness and higher crust

chlorophyll content, with the mixed crust being sub-

jected to the intermediate abiotic conditions and subse-

quently exhibiting intermediate properties. As for the

crust microfungal communities, the highly significant

positive linear relationship between the isolate densi-

ty and chlorophyll content indicates that the surface

wetness duration not only affects the autotrophic com-

ponent of the crust but, expectedly, also influences the

amount of fungi, taking into account that in the desert

soils, isolate density mainly reflects number of spores

in the crust, i.e., the biomass in its potential, dormant

state. The significant and negative correlation between

the abundance of melanin-containing species, including

melanized fungi with large multicellular spores, and

the chlorophyll content is apparently due to its close

link to both wetness duration and radiation intensity

associated with the topographic position of the crust.

Comparison between the crust types revealed mi-

nor differences in species composition of the micro-

fungal communities. All crusts exhibited overwhel-

ming prevalence of melanin-containing species accom-

panied with high abundance of melanized fungi with

large multicellular spores. Significantly more expressed

MICROFUNGAL COMMUNITIES IN BIOLOGICAL SOIL CRUSTS 361

differences in these parameters were found between the

0.0–0.4 and 0.4–0.8 cm layers of the studied crusts.

Apparently, ultraviolet (UV) irradiance known to pe-

netrate only up to 100 µm into soil depth (Johnson,

2003) played an important role in the organization

of microfungal communities and might explain the

decrease in abundance of melanized fungi, especially

those with multicellular spores, from the uppermost to

the subsurface crust layers.

Microfungal communities from the same crust

types of the stabilized localities also did not show

significant differences in isolate density within the

chronosequence. This may be attributed to the fact

that all crusts exhibited semi-equilibrium with the

abiotic conditions reaching their final stage of succes-

sion. Given the rapid recovery rates recorded for the

Israeli NRS crusts of < 10 and < 25 years for the

cyanobacterial and moss-dominated crusts, respective-

ly (Kidron et al., 2008), one may assume that the 40–60

years-old SRS crusts already reached their final stage

of development, which may explain in turn the simi-

larity in CFU numbers between the same crust types

in the localities of different periods after sand stabi-

lization and revegetation. A highly significant decline

in isolate density with crust depth might be associated

with a decrease in organic matter content and a possi-

ble reduction in water availability—two main edaphic

factors known to positively influence fungal develop-

ment and activity in soil (e.g., Deacon, 1997).

A general, although nonsignificant, tendency to-

wards a decrease in the community diversity indices (H

and I) with crust age was noted within the chronose-

quence (Table II), which may indicate that with time,

an increase in dominance of one or two prevalent

species could takes place, thus decreasing the hete-

rogeneity and evenness of the microfungal commu-

nities. The highest diversity indices revealed in the

non-crusted sand localities are in accordance with the

above tendency; similarly, the communities of the

sand localities at the NRS were characterized by 1.2–

1.4-fold higher diversity indices than the crust com-

munities. More heterogeneous and even microfungal

communities were recovered also from the subsur-

face crust layer as compared to the uppermost layer

(Table III). Apparently, due to the absence of high

irradiance pressure, the subsurface crust communi-

ties avoid overwhelming dominance of the melanized

species with multicellular spores, thus becoming more

well-balanced.

A comparison between microfungal communities

from the stabilized and natural localities showed some

differences. In the case of species composition, higher

abundance of the main dominant species, E. phrag-

mospora, and lower abundance of one of the frequent

species, F. oxysporum, were found at the stabilized

localities. As for the diversity level, the communities

from the cyanobacterial crusts in the stabilized loca-

lities were characterized by the lowest diversity in-

dices in comparison with those of the moss-dominated

crusts, while in the natural localities, the communities

from the moss-dominated crusts were least heteroge-

neous and even. The pattern of the natural locality is

similar to that found at NRS (Grishkan and Kidron,

2013). This was explained by the fact that an increase

in isolate density, which is characteristic of the moss-

dominated crusts, is often caused by an abundant de-

velopment of one or two species, which decreases both

species richness and diversity level of the microfungal

communities.

Apart from the different dominating microfungal

species in the Tengger and Negev deserts (Embellisia

phragmospora and Ulocladium atrum, respectively), up

to 10-folds more of an abundant presence of the ther-

motolerant fungi (Canariomyces notabilis, Chaetomi-

um strumarium, and Aspergillus nidulans) was recor-

ded in the Tengger crusts as compared to the Negev

crusts. Such a difference might be associated with

the fundamentally dissimilar precipitation regimes that

characterize the Chinese and Israeli deserts. Whereas

the Negev crusts are subjected to winter rains under

comparatively cool temperatures of 5–20 ◦C, the Teng-

ger crusts are adapted to summer rains under warm

and even hot temperatures of 30–35 ◦C. The high tem-

peratures during the rainy season may explain the pre-

dominance of thermotolerant mosses such as Bryum

argenteum (Convey and Lewis Smith, 2006), as well as

the substantially higher abundance of thermotolerant

fungal species in the crusts of the Tengger Desert.

CONCLUSIONS

Species-rich microfungal communities inhabited di-

fferent types of BSCs in the vicinity of the Shapotou

Research Station in the Tengger Desert, which dis-

played little variations within a chronosequence in the

localities of different periods after sand stabilization

and revegetation. The topographically induced differe-

nces in abiotic conditions caused variations in species

composition, isolate densities, and diversity charac-

teristics of the crust microfungal communities in the

Tengger Desert. Similarly to the Negev Desert in Is-

rael, the mycobiota of the crusts in the Tengger Desert

was dominated by melanin-containing fungi with large

multicellular spores, although with different prevailing

362 I. GRISHKAN et al.

species. The substantially higher abundance of ther-

motolerant fungal species in the crusts of the Tengger

Desert in comparison with the Negev Desert was as-

sociated with the principal differences in precipitation

regimes, winter and summer rains which are characte-

ristic of the Negev and Tengger deserts, respectively.

ACKNOWLEDGEMENTS

We thank the Chinese Academy of Sciences Visi-

ting Professorship for Senior International Scientists

(No. 2011T1Z16) and the Israeli Ministry of Absorp-

tion for financial support of this research.

REFERENCES

Abdullah, S. K., Al-Khesraji, T. O. and Al-Edany, T. Y. 1986.

Soil mycoflora of the Southern Desert of Iraq. Sydowia. 39:

8–16.

Abed, R. M. M., Al-Sadi, A. M., Al-Shehi, M., Al-Hinai, S. and

Robinson, M. D. 2013. Diversity of free-living and lichenized

fungal communities in biological soil crusts of the Sultanate

of Oman and their role in improving soil properties. Soil Biol.

Biochem. 57: 695–705.

Bates, S. T. and Garcia-Pichel, F. 2009. A culture independent

study of free-living fungi in biological soil crusts of the Co-

lorado Plateau: their diversity and relative contribution to

microbial biomass. Environ. Microbiol. 11: 56–67.

Bates, S. T., Nash III, T. H. and Garcia-Pichel, F. 2012. Patterns

of diversity for fungal assemblages of biological soil crusts

from the southwestern United States. Mycologia. 104: 353–

361.

Bates, S. T., Nash III, T. H., Sweat, K. G. and Garcia-Pichel,

F. 2010. Fungal communities of lichen-dominated biological

soil crusts: diversity, relative microbial biomass, and their re-

lationship to disturbance and crust cover. J. Arid Environ.

74: 1192–1199.

Belnap, J. and Lange, O. L. 2001. Preface. In Belnap, J. and

Lange, O. L. (eds.) Biological Soil Crusts: Structure, Func-

tion, and Management. Springer-Verlag, Berlin-New York.

pp. V–IX.

Bills, G. F., Christensen, M., Powell, M. and Thorn, G. 2004. Sa-

probic soil fungi. In Mueller, G. M., Bills, G. F. and Foster,

M. S. (eds.) Biodiversity of Fungi: Inventory and Monitoring

Methods. Elsevier Academic Press, San Diego. pp. 271–302.

Christensen, M. 1981. Species diversity and dominance in fun-

gal community. In Carroll, G. W. and Wicklow, D. T. (eds.)

The Fungal Community, Its Organization and Role in the

Ecosystem. Marcell Dekker, New York. pp. 201–232.

Ciccarone, C. and Rambelli, A. 1998. A study on micro-fungi

in arid areas. Notes on stress-tolerant fungi. Plant Biosyst.

132: 17–20.

Convey, P. and Lewis Smith, R. I. 2006. Geothermal bryophyte

habitats in the South Sandwich Islands, maritime Antarctic.

J. Veg. Sci. 17: 529–538.

Davet, P. and Rouxel, F. 2000. Detection and Isolation of Soil

Fungi. Science Publisher Inc., Enfield and Plymouth.

Deacon, J. W. 1997. Modern Mycology. 3rd Ed. Blackwell Sci-

ence, Oxford.

Duan, Z. H., Xiao, H. L., Li, X. R., Dong, Z. B. and Wang, G.

2004. Evolution of soil properties on stabilized sands in the

Tengger Desert, China. Geomorphology. 59: 237–246.

Grishkan, I., Beharav, A., Kirzhner, V. and Nevo, E. 2007.

Adaptive spatiotemporal distribution of soil microfungi in

“Evolution Canyon” III, Nahal Shaharut, extreme Southern

Negev Desert, Israel. Biol. J. Linn. Soc. 90: 263–277.

Grishkan, I. and Kidron, G. J. 2013. Biocrust-inhabiting cul-

tured microfungi along a dune catena in the western Negev

Desert, Israel. Eur. J. Soil Biol. 56: 107–114.

Grishkan, I. and Nevo, E. 2010. Spatiotemporal distribution of

soil microfungi in the Makhtesh Ramon area, central Negev

desert, Israel. Fungal Ecol. 3: 326–337.

Grishkan, I., Tsatskin, A. and Nevo, E. 2008. Diversity of cul-

tured microfungal communities in surface horizons of soils

on different lithologies in Upper Galilee, Israel. Eur. J. Soil

Biol. 44: 180–190.

Grishkan, I., Zaady, E. and Nevo, E. 2006. Soil crust microfun-

gi along a southward rainfall aridity gradient in the Negev

Desert, Israel. Eur. J. Soil Biol. 42: 33–42.

Halwagy, R., Moustafa, A. F. and Kamel, S. 1982. Ecology of

the soil mycoflora in the desert of Kuwait. J. Arid Environ.

5: 109–125.

Hashem, A. R. 1991. Studies on the fungal flora of Saudi Arabian

soil. Cryptogam. Bot. 2: 179–182.

Jia, R. L., Li, X. R., Liu, L. C., Gao, Y. H. and Li, X. J. 2008.

Responses of biological soil crusts to sand burial in a revege-

tated area of the Tengger Desert, Northern China. Soil Biol.

Biochem. 40: 2827–2834.

Jia, R. L., Li, X. R., Liu, L. C., Gao, Y. H. and Zhang, X. T.

2012. Differential wind tolerance of soil crust mosses explains

their micro-distribution in nature. Soil Biol. Biochem. 45:

31–39.

Johnson, D. 2003. Response of terrestrial microorganisms to

ultraviolet-B radiation in ecosystems. Res. Microbiol. 154:

315–320.

Kidron, G. J. 1999. Differential water distribution over dune

slopes as affected by slope position and microbiotic crust,

Negev Desert, Israel. Hydrol. Process. 13: 1665–1682.

Kidron, G. J., Barzilay, E. and Sachs, E. 2000. Microclimate

control upon sand microbiotic crust, western Negev Desert,

Israel. Geomorphology. 36: 1–18.

Kidron, G. J., Vonshak, A. and Abeliovich, A. 2008. Recovery

rates of microbiotic crusts within a dune ecosystem in the

Negev Desert. Geomorphology. 100: 444–452.

Kidron, G. J., Vonshak, A. and Abeliovich, A. 2009. Microbiotic

crusts as biomarkers for surface stability and wetness dura-

tion in the Negev Desert. Earth Surf. Proc. Land. 34: 1594–

1604.

Kidron, G. J., Vonshak, A., Dor, I., Barinova, S. and Abeliovich,

A. 2010. Properties and spatial distribution of microbiotic

crusts in the Negev Desert, Israel. Catena. 82: 92–101.

Kidron, G. J. and Yair, A. 1997. Rainfall-runoff relationships

over encrusted dune surfaces, Nizzana, western Negev, Is-

rael. Earth Surf. Proc. Land. 22: 1169–1184.

Kirk, P. M. Cannon, P. F., David, J. C. and Stalpers, J. A. 2014.

The CABI bioscience and CBS database of fungal names.

Available online at http://www.indexfungorum.org (verified

on June 24, 2014).

Krebs, C. J. 1999. Ecological Methodology. Addison Wesley

Longman, Menlo Park.

Li, X. R., He, M. Z., Duan, Z. H., Xiao, H. L. and Jia, X. H. 2007.

Recovery of topsoil physicochemical properties in revegeta-

ted sites in the sand-burial ecosystems of the Tengger Desert,

northern China. Geomorphology. 88: 254–265.

Li, X. R., He, M. Z., Zerbe, S., Li, X. J. and Liu, L. C.

2010. Micro-geomorphology determines community struc-

ture of biological soil crusts at small scales. Earth Surf. Proc.

MICROFUNGAL COMMUNITIES IN BIOLOGICAL SOIL CRUSTS 363

Land. 35: 932–940.

Li, X. R., Shi, Q. H. and Zhang, J. G. 1998. Study of plant di-

versity changes during the artificial vegetation evolution pro-

cesses in the Shapotou region. J. Desert Res. (in Chinese).

18: 23–29.

Li, X. R., Zhou, H. Y., Wang, X. P., Zhu, Y. G. and O’Conner,

P. J. 2003. The effects of sand stabilization and revegeta-

tion on cryptogam species diversity and soil fertility in the

Tengger Desert, Northern China. Plant Soil. 251: 237–245.

Li, X. R., Xiao, H. L., He, M. Z. and Zhang, J. G. 2006. Sand

barriers of straw checkerboards for habitat restoration in ex-

tremely arid desert regions. Ecol. Eng. 28: 149–157.

Li, X. R., Xiao, H. L., Zhang, J. G. and Wang, X. P. 2004.

Long-term ecosystem effects of sand-binding vegetation in

the Tengger Desert, northern China. Restor. Ecol. 12: 376–

390.

Li, X. R., Zhang, Z. S., Huang, L., Liu, L. C. and Wang, X. P.

2009. The ecohydrology of the soil-vegetation system restora-

tion in arid zones: a review. Sci. Cold Arid Reg. (in Chinese).

1: 199–206.

Liu, L. C., Li, S. Z., Duan, Z. H., Wang, T., Zhang, Z. S. and Li,

X. R. 2006. Effects of microbiotic crusts on dew deposition in

the restored vegetation area at Shapotou, northwest China.

J. Hydrol. 328: 331–337.

Porras-Alfaro, A., Herrera, J., Natvig, D. O., Lipinski, K. and

Sinsabaugh, R. 2011. Diversity and distribution of soil fungal

communities in a semiarid grassland. Mycologia. 103: 10–21.

Ranzoni, F. V. 1969. Fungi isolated in culture from soils of the

Sonoran Desert. Mycologia. 60: 356–371.

Skujins, J. 1984. Microbial ecology of desert soils. Adv. Microb.

Ecol. 7: 49–91.

States, J. S. and Christensen, M. 2001. Fungi associated with

biological soil crusts in desert grasslands of Utah and Wyo-

ming. Mycologia. 93: 432–439.

States, J. S., Christensen, M. and Kinter, C. K. 2001. Soil fun-

gi as components of biological soil crusts. In Belnap, J. and

Lange, O. (eds.) Biological Soil Crusts: Structure, Function,

and Management. Springer-Verlag, Berlin–New York. pp.

155–166.

Warren, S. D. 1995. Ecological role of microphytic soil crusts

in arid ecosystems. In Allsopp, D., Colwell, R. R. and Hark-

sworth, D. L. (eds.) Microbial Diversity and Ecosystem Func-

tion. CAB International, London. pp. 199–209.

Zak, J. 2005. Fungal communities of desert ecosystems: links to

climate change. In Dighton, J., White, J. F. and Oudemans,

P. (eds.) The Fungal Community, Its Organization and Role

in the Ecosystems. 3rd Ed. CRC Press, Boca Raton. pp. 659–

681.