(Life in Extreme Environments 4) Ed. by Steven, Blaire With Contrib. by Antoninka, Anita J. - Babin, Doreen - Bastida, Felipe - Bowker, Matthew A. - Büdel, Burkhard - Cowan, Don A. - de Scally, Storm

Blaire Steven (Ed.
)
The Biology of Arid Soils
Life in Extreme Environments
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Life in Extreme Environments
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Edited by
Dirk Wagner
Volume 4
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The Biology
of Arid Soils
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Editor
Blaire Steven
Department of Environmental Sciences
Connecticut Agricultural Experiment Station
123 Huntington Street
New Haven, CT 06511, USA
blaire.steven@ct.gov
ISBN 978-3-11-041998-6
e-ISBN (PDF) 978-3-11-041904-7
e-ISBN (EPUB) 978-3-11-041914-6
ISSN 2197-9227
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Preface
When Dr. Dirk Wagner asked me to edit an edition in the series “Life in Extreme En-
vironments” on the topic of arid soils, I was a little surprised. Other books in the se-
ries discussed life in the deep ocean, caves, and Earth’s thermal vents. Studies where
scientists require large field campaigns, submersible vehicles, and potential personal
risk to collect samples. In contrast, many people could collect a sample of arid soil
in a brisk walk from wherever they may be reading this. In this regard, arid soils did
not seem to be such an “extreme” of an environment. Yet, arid soils are united by a
common characteristic, namely water scarcity, which limits the diversity and produc-
tivity of these systems. Furthermore, arid ecosystems also occur in both the hottest
and coldest regions of the planet and therefore may experience a multitude of other
severe environmental conditions. So, in many respects arid soils may be as harsh of
an environment as more treacherous locals.
Soil has been described as one of nature’s most complex ecosystems. Thus, any
scientist that takes on the study of soil biology faces a daunting task. By the virtue of
arid soil organisms existing at the low water availability to support life, these commu-
nities tend to be simplified compared to more temperate soils. The collection of papers
in this volume highlight the work of researchers that are employing arid soils to under-
stand the limits of life under low water availability, the functioning of soil ecosystems,
and predicting how these systems will respond to an altered climate.
In putting together this volume I called in favors from collaborators, met new col-
leagues, and learned more about arid soils than I knew before. I was also able to in-
clude photographs taken by my father on his various travels (see Figure 1.1). He has
always been a hobbyist, but can know say he is a published photographer. Congratu-
lations dad. The list of contributing authors to this volume highlights the international
scope of arid land research and the broad disciplines involved. Like any good work of
science I hope this work raises as may questions for future research as it answers for
those with the curiosity to read it.
Blaire Steven
Brought to you by | UCL - University College London

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Volumes published in the series
Volume 1
Jens Kallmeyer, Dirk Wagner (Eds.)
Microbial Life of the Deep Biosphere
ISBN 978-3-11-030009-3
Volume 2
Corien Bakermans (Ed.)
Microbial Evolution under Extreme Conditions
ISBN 978-3-11-033506-4
Volume 3
Annette Summers Engel (Ed.)
Microbial Life of Cave Systems
ISBN 978-3-11-033499-9

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Contents
Preface | V
Contributing authors | XI
Blaire Steven
1 An Introduction to Arid Soils and Their Biology | 1
1.1 The Definition and Extent of Arid Ecosystems | 1
1.2 Characteristics of Arid Soils | 2
1.3 Soil Habitats in Arid Regions | 2
1.3.1 Refugia Sites Associated with Rocks | 3
1.3.2 Shrubs as Islands of Fertility | 3
1.3.3 Biological Soil Crusts | 5
1.4 The Pulse Reserve Paradigm of Arid Ecosystems | 6
1.5 Response of Arid Ecosystems to Disturbance | 7
1.6 Arid Ecosystems as a Model for Soil Biology | 7
1.7 Summary | 7
Carlos Garcia, J.L.Moreno, T. Hernandez, and F. Bastida

2 Soils in Arid and Semiarid Environments: the Importance of Organic Carbon
and Microbial Populations. Facing the Future | 15
2.1 Introduction | 15
2.2 Climate Regulation and Soil Organic Carbon
in Arid-Semiarid Zones | 16
2.3 Land Use and Soil Organic Carbon in Arid-Semiarid Zones | 17
2.4 Soil Restoration in Arid-Semiarid Zones:
Amendments Based on Exogenous Organic Matter | 18
2.5 Microbial Biomass and Enzyme Activity in Arid-Semiarid Zones | 19
2.6 Organic Carbon, Macro and Microaggregates,
and C Sequestration in Arid-Semiarid Zones | 22
2.7 Conclusion | 23
Gary M. King
3 Water Potential as a Master Variable for Atmosphere–Soil Trace Gas
Exchange in Arid and Semiarid Ecosystems | 31
3.2 Water Potential and Water Potential Assays | 32
3.3 Limits of Growth and Metabolic Activity | 35
3.4 Water Potential and Trace Gas Exchanges | 37
3.5 Conclusions | 41
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VIII | Contents
Thulani P. Makhalanyane, Storme Z. de Scally, and Don A. Cowan

4 Microbiology of Antarctic Edaphic and Lithic Habitats | 47
4.2 Classification of Antarctic soils | 48
4.2.1 McMurdo Dry Valley Soils | 49
4.2.2 Antarctic Peninsula Soils | 50
4.3 Bacterial Diversity of Soils in the MDVs and Antarctic Peninsula | 51
4.4 Cryptic Niches in Antarctic Environments | 54
4.4.1 Hypoliths | 55
4.4.2 Epiliths | 56
4.4.3 Endoliths | 57
4.5 Biogeochemical Cycling in Antarctic Environments | 59
4.6 Viruses in Antarctic Edaphic Ecosystems | 59
4.7 Conclusions and Perspectives | 60
Matthew A. Bowker, Burkhard Büdel, Fernando T. Maestre, Anita J. Antoninka, and

David J. Eldridge
5 Bryophyte and Lichen Diversity on Arid Soils: Determinants and
Consequences | 73
5.1 Overview | 73
5.1.1 Moss, Liverwort, and Lichen Biology | 73
5.2 Global Diversity and Characteristic Taxa | 74
5.2.1 Global Species Pool | 74
5.2.2 Global Characteristic Taxa and β Diversity | 75
5.3 Determinants of Moss, Liverwort, and Lichen Diversity
on Arid Soils | 78
5.3.1 Geographic Isolation and Biogeography | 78
5.3.2 Climatic Gradients and Climate Change | 79
5.3.3 Calcicole–Calcifuge Dichotomy and Soil pH Gradients | 80
5.3.4 The Special Case of Gypsiferous Soils | 81
5.4 Consequences of Moss, Liverwort, and Lichen Diversity
on Arid Soils | 82
5.4.1 Contribution of Biocrust Lichens and Bryophytes to Arid Ecosystem
Function | 82
5.4.2 Biodiversity–Ecosystem Functioning Relationship | 83
5.4.3 Effects of Species Richness, Turnover, and Evenness on Ecosystem
Functions | 84
5.4.4 Multifunctionality | 87
5.4.5 Functional Redundancy or Singularity? | 88
5.5 Summary and Conclusions | 89
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Contents | IX
Andrea Porras-Alfaro, Cedric Ndinga Muniania, Paris S. Hamm, Terry J. Torres-Cruz,

and Cheryl R. Kuske
6 Fungal Diversity, Community Structure and Their Functional Roles in Desert
Soils | 97
6.1 Spatial Heterogeneity of Fungal Communities in Arid Lands | 97
6.1.1 Biocrusts | 100
6.1.2 Plant Associated Fungi in Deserts | 103
6.2 Roles in Nutrient Cycling and Effects of Climate Change on Fungal
Communities | 107
6.3 Extremophiles in Deserts | 108
6.3.1 Thermophilic and Thermotolerant Fungi | 109
6.3.2 Rock Varnish and Microcolonial Fungi in Deserts | 109
6.4 Human Pathogenic Fungi in Desert Ecosystems | 111
6.4.1 Coccidioides immitis and C. posadasii | 112
6.4.2 Dematiaceous and Keratinolytic Fungi in Deserts | 112
6.4.3 Eumycetoma | 113
6.4.4 Mycotoxins | 114
6.5 Importance of Fungal Biodiversity in Arid Lands | 115
T.G. Allan Green

7 Limits of Photosynthesis in Arid Environments | 123
7.2 Photosynthetic Responses to Environmental Factors,
a Background | 124
7.2.1 Rates, Chlorophyll and Mass | 124
7.2.2 Response of Net Photosynthesis (NP) to Light (PPFD,
μmol m−2 s−1 ) | 126
7.2.3 Response of Net Photosynthesis to Temperature | 127
7.2.4 Response of Net Photosynthesis to Thallus Water Content (WC) | 127
7.2.5 Response of Net Photosynthesis to CO2 Concentration | 129
7.3 Optimal Versus Real Photosynthetic Rates | 129
7.4 Limits to Photosynthesis in Arid Areas | 131
7.4.1 Length of Active Time | 131
7.4.2 Limits When Active – External Limitation Through Light and
Temperature | 132
7.4.3 Limits When Active – Internal Limitation Through Thallus
Hydration | 132
7.4.4 Catastrophes | 133
7.5 Flexibility – an Often Overlooked Factor | 134
7.6 Summary | 134
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X | Contents
Blaire Steven, Theresa A. McHugh, and Sasha Reed

8 The Response of Arid Soil Communities to Climate Change | 139
8.1 Overview | 139
8.2 Biological Responses to Elevated Atmospheric CO2 | 140
8.3 Biological Responses to Increased Temperature | 142
8.4 Biological Responses to Changes in Precipitation | 143
8.4.1 Natural Precipitation Gradients | 145
8.4.2 Precipitation Manipulation Studies | 147
8.5 Interactions Between Temperature and Soil Moisture | 149
8.6 Conclusion | 150
Doreen Babin, Michael Hemkemeyer, Geertje J. Pronk, Ingrid Kögel-Knabner,

Christoph C. Tebbe, and Kornelia Smalla
9 Artificial Soils as Tools for Microbial Ecology | 159
9.2 Soil Definition | 160
9.3 History of Artificial Soil Experiments | 162
9.4 Methods in Soil Microbial Ecology and Soil Science | 164
9.5 Insights into Microbial Communities from Artificial Soil Studies | 166
9.5.1 Establishment and Structuring of Soil Microbial Communities | 166
9.5.2 Functioning of Soil Microbial Communities | 169
9.6 Artificial Soils for Arid Soil Research | 174
9.7 Concluding Remarks | 175
Index | 181
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Contributing authors
Anita J. Antoninka Storme Z. de Scally

School of Forestry Centre for Microbial Ecology and Genomics
Northern Arizona University Department of Genetics, Natural Sciences 2
Flagstaff, Arizona, 86011, USA University of Pretoria
e-mail: anita.antoninka@nau.edu Hatfield, Pretoria, 0028
e-mail: u12021955@tuks.co.za
Doreen Babin
David J. Eldridge
Julius Kühn-Institut – Federal Research Centre
Centre for Ecosystem Studies
for Cultivated Plants (JKI)
School of Biological, Earth and Environmental
Institute for Epidemiology and Pathogen
Sciences
Diagnostics
University of New South Wales
Braunschweig, Germany
Sydney, Australia
e-mail: doreen.babin@julius-kuehn.de
e-mail: d.eldridge@unsw.edu.au
Felipe Bastida Carlos García

Department of Soil and Water Conservation, Department of Soil and Water Conservation
CEBAS-CSIC CEBAS-CSIC, Campus Universitario de Espinardo
Campus Universitario de Espinardo Murcia, Spain
Murcia, Spain. e-mail: cgarizq@cebas.csic.es
e-mail: fbastida@cebas.csic.es
T. G. Allan Green
Departamento de Vegetal II, Farmacia Facultad
Matthew A. Bowker
Universidad Complutense
School of Forestry
28040, Madrid, Spain
Northern Arizona University
e-mail: thomas.green@waikato.ac.nz
Flagstaff, Arizona, 86011, USA
e-mail: matthew.bowker@nau.edu
Paris S. Hamm
Department of Biological Sciences
Burkhard Büdel Western Illinois University
Plant Ecology & Systematics Macomb, Illinois, USA
Faculty of Biology e-mail: ps-hamm@wiu.edu
University of Kaiserslautern
Kaiserslautern, Germany Michael Hemkemeyer
e-mail: buedel@rhrk.uni-kl.de Thünen Institute of Biodiversity
Federal Research Institute for Rural Areas,
Forestry and Fisheries
Don A. Cowan
Centre for Microbial Ecology and Genomics
Present address: Faculty of Life Sciences
Department of Genetics, Natural Sciences 2
Rhine-Waal University of Applied Sciences
University of Pretoria
Kleve, Germany
Hatfield, Pretoria, USA
e-mail: michael.hemkemeyer@hochschule-
e-mail: don.cowan@up.ac.za
rhein-waal.de

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XII | Contributing authors
Teresa Hernández José Luis Moreno

Department of Soil and Water Conservation Department of Soil and Water Conservation
CEBAS-CSIC, Campus Universitario de Espinardo CEBAS-CSIC, Campus Universitario de Espinardo
Murcia, Spain Murcia, Spain
e-mail: mthernan@cebas.csic.es e-mail: jlmoreno@cebas.csic.es
Gary M. King
Department of Biological Sciences Cedric Ndinga Muniania
Louisiana State University Department of Biological Sciences
Baton Rouge, Louisiana 70803, USA Western Illinois University
e-mail: gkingme@gmail.com Macomb, Illinois, USA
e-mail: c-ndingamuniana@wiu.edu
Ingrid Kögel-Knabner
Lehrstuhl für Bodenkunde, Technische
Universität München Andrea Porras-Alfaro
Freising-Weihenstephan, Germany Department of Biological Sciences
Institute for Advanced Study, Technische Western Illinois University
Universität München Macomb, Illinois, USA
Garching, Germany e-mail: a-porras-alfaro@wiu.edu
e-mail: koegel@wzw.tum.de
Geertje J. Pronk
Cheryl R. Kuske
Lehrstuhl für Bodenkunde, Technische
Bioscience Division
Universität München
Los Alamos National Laboratory
Freising-Weihenstephan, Germany
Los Alamos, New Mexico, USA
Institute for Advanced Study, Technische
e-mail: kuske@lanl.gov
Universität München
Garching, Germany
Fernando T. Maestre
Present address: Ecohydrology Research Group,
Departamento de Biología y Geología, Física y
University of Waterloo
Química Inorgánica
Waterloo, Ontario, Canada
Escuela Superior de Ciencias Experimentales y
e-mail: gpronk@uwaterloo.ca
Tecnología
Universidad Rey Juan Carlos
Móstoles, Spain
Sasha Reed
e-mail: fernando.maestre@urjc.es
Southwest Biological Science Center
U.S. Geological Survey
Thulani P. Makhalanyane Moab, Utah, USA
Centre for Microbial Ecology and Genomics e-mail: screed@usgs.gov
Department of Genetics, Natural Sciences 2
University of Pretoria
Hatfield, Pretoria, USA Kornelia Smalla
e-mail: Thulani.makhalanyane@up.ac.za Julius Kühn-Institut – Federal Research Centre
for Cultivated Plants (JKI)
Theresa A. Mchugh Institute for Epidemiology and Pathogen
Southwest Biological Science Center Diagnostics
U.S. Geological Survey Braunschweig, Germany
Moab, Utah, USA e-mail: kornelia.smalla@julius-kuehn.de
e-mail: tmchugh@coloradomesa.edu

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Contributing authors | XIII
Blaire Steven Terry J. Torres-Cruz

Department of Environmental Sciences Department of Biological Sciences
Connecticut Agricultural Experiment Station Western Illinois University
New Haven, CT, USA Macomb, Illinois, USA
e-mail: blaire.steven@ct.gov e-mail: tj-torrescruz@wiu.edu
Christoph C. Tebbe
Thünen Institute of Biodiversity
Federal Research Institute for Rural Areas,
Forestry and Fisheries
e-mail: christoph.tebbe@thuenen.de

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Authenticated
Blaire Steven
1 An Introduction to Arid Soils and Their Biology
1.1 The Definition and Extent of Arid Ecosystems
When one invokes the terms arid ecosystem or dryland it is often assumed that the
term refers to a desert. However, there are regional differences in the concept of a
“desert” as well as differences in terms for describing and classifying arid lands. The
one characteristic that unites all arid lands is a lack of water availability, generally due
to low precipitation. Yet, lack of precipitation is not the only factor that limits water
availability. Water can be lost from the landscape through evaporation and transpira-
tion, and the evaporative loss of water from plants. Together these processes are re-
ferred to as evapotranspiration [1]. Thus, the “dryness” of a region can be determined
by calculating the net difference between precipitation and water losses through eva-
potranspiration, also referred to as the Aridity Index [2–4]. These metrics have been a
useful tool to generate a standardized method to categorize and define drylands. The
aridity index, as well as other metrics such as the dominant vegetation and climate,
have been used to classify arid lands into three main categories (󳶳 Fig. 1.1):
Hyperarid zone (arid index 0.03 or below): Dryland areas of scant or no veg-
etation. Annual rainfall is low, rarely exceeding 100 mm. Precipitation events are
infrequent and irregular, with dry periods lasting up to several years. Hyperarid re-
gions cover ∼ 8% of the Earth’s surface [5]. Examples: Atacama Desert, South America;
Namib Desert and Sahara Desert, Africa; and Lut Desert, Iran.
Arid zone (arid index 0.03–0.20): Vegetation consists of sparsely distributed
patches of annual or perennial grasses, patchily distributed shrubs, cacti, or small
trees. Maximum precipitation varies from 100–300 mm per year. Arid zones cover
∼ 16% of the planet’s land surface. Examples: Chihuahuan Desert, U.S.A. and Simp-
son Desert, Australia.
(a) (b) (c)
Fig. 1.1: Examples of different arid zone landscapes. (a) Hyperarid zone. Namib Desert, South Africa.
Photo courtesy Don Cowan. (b) Arid zone. Saguaro National Park, Arizona, U.S.A, (c) Semiarid zone.
Witfontein Nature Reserve grassland, South Africa. Photos b and c courtesy Douglas Steven.
DOI 10.1515/9783110419047-001
2 | 1 An Introduction to Arid Soils and Their Biology
Semiarid zone (arid index 0.20–0.50): Vegetation is more diverse and may cover
the surface. For instance, semiarid grasslands or steppes are common. Annual pre-
cipitation can reach 800 mm per year and may occur in distinct dry and wet seasons.
Semiarid zones cover ∼ 18% of the Earth. Examples: Great Plains U.S.A, Kenyan Sa-
vanah, and Mongolian Steppes.
It is important to note that not all arid soils occur in regions classified as drylands.
Isolated patches of arid soils can occur in otherwise temperate regions, for example,
alpine tundra or volcanic cinders [6, 7].
1.2 Characteristics of Arid Soils
Arid soils possess unique characteristics that distinguish them from soils from more
humid regions. Arid systems are generally limited in biological activity and thus con-
tain low levels of organic carbon. This lack of organic carbon is a large driver in the
structuring and function of arid soils and is the focus of Chapter 2. Extended periods
of water deficiencies also slow the elimination or leaching of soluble salts, which are
further accumulated due to high rates of evaporation [8]. Thus, arid soils tend to ac-
cumulate calcium carbonate, gypsum, or silica [9]. Despite similarities in soil genesis,
the different climates, geology, and vegetation of arid lands create unique soil charac-
teristics, so that the morphology and soil characteristics vary between different dry-
lands [10]. The water holding capacity of a soil depends on its physical characteristics,
including texture, structure, and soil depth [11]. This leads to large differences in the
available water for biology between different soils. The critical importance in water
potential is discussed in Chapter 3. So soil characteristics play an integral role in de-
termining the composition and function of arid soil biological communities. In fact,
soil parent material and chemistry have been found to play a large role in shaping arid
soil biology [12, 13]. In this respect, local edaphic factors need to be included in any
study of arid soil biology.
1.3 Soil Habitats in Arid Regions
A characteristic of arid regions is reduced biological diversity. This has been well docu-
mented for vegetation (e.g., [13–16]) and other macro fauna [18]. Similar patterns have
emerged for soil bacterial and fungal communities [19, 20]. In fact, a global survey
of drylands worldwide found that the diversity of soil bacteria and fungi was linearly
correlated to the aridity of the ecosystem [21]. In this regard, aridity is a large predictor
of the diversity of soil communities. However, drylands are not homogenous regions
experiencing low precipitation. Arid regions are patchy at a variety of scales. The veg-
etation is sparse, soil edaphic factors vary, the terrain is uneven, and precipitation
and temperature vary erratically [22–25]. In this respect, not every patch of arid soil
is created equally. Certain niches in drylands differ in their ability to support biologi-
cal communities. For example, aspects of the landscape such as slope or shading that
may alter water retention of the soil have the potential to alter the abundance and di-
versity of the communities the soil can support [26]. This results in distinct ecological
niches, some of which are discussed below.
1.3.1 Refugia Sites Associated with Rocks
In hyperarid deserts, the shelter provided within the shade of a rock can be the dif-
ference between life and death. These lithic associated communities often inhabit re-
gions so devoid of moisture that a significant portion of their water requirements is
met by fog rather than precipitation [27, 28]. Rocks in deserts can support a number
of different communities. These include: hypolithic communities inhabiting the basal
surface of rocks [29, 30], endolithic communities that live inside rocks or pores between
mineral grains [31–34], and chasmolithic communities under rock flakes produced by
weathering [35, 36]. Rocks provide the soil microbiota physical stability, increased
water retention by shading, protection from ultraviolet radiation, and micronutrients
from the mineral components of the rock material [37].
Translucent rocks allow for light transmission to a depth sufficient to support
phototrophs, such as mosses or cyanobacteria. A common cyanobacteria occurring
in hypolithic niches is Chroococcidiopsis sp. [38], which has been detected in deserts
worldwide [39]. These phototrophic populations fix carbon, which can then feed het-
erotrophic populations, resulting in relatively complex ecosystems [35, 40]. Thus,
these communities act as a source of organic carbon, which is a valuable commodity
in otherwise nearly barren soils [41]. Additionally, the presence of active biology can
accelerate the weathering of the rocks. This can occur either by metabolic activity
of the communities, scavenging nitrogen or phosphorous from the rock material,
which has been shown to increase the weathering rate of rock by up to three orders
of magnitude, or by physical infiltration into rock crevices and the mechanical dis-
ruption of porous stones [42–44]. These communities can also increase weathering
by encouraging grazing and the associated scraping of rock surfaces by predatory
invertebrates [45]. So beyond fixing organic carbon, rock associated communities can
also release limiting nutrients supporting the growth of multiple trophic levels. In
this respect, even the interspersed rocks in the desert can act as abiotic oases for soil
biology.
1.3.2 Shrubs as Islands of Fertility
In arid ecosystems where plants are sparse, a shrub is often a conspicuous aspect of
the ecosystem. As wind moves across the landscape the canopy of the shrub can dis-
rupt currents, collecting dust [46]. Later, precipitation moving through the canopy of
the shrub can pick up this deposited dust and other plant litter, transporting this ma-
terial to the under canopy soils [47]. Analyses of fall water have shown that it contains
up to ten times more nutrients than bulk precipitation occurring outside of the shrub
canopy [48]. Thus this material can act to fertilize soils in the canopy zone of the shrub.
Additionally, shrubs supply nest sites, shade, and food resources for animal popula-
tions, which can enrich the local soils through feces, discarded carcasses, and nest
materials [49]. Shrubs are also important in the interception, infiltration, and storage
of water, thereby increasing soil moisture [50]. Finally, the shrub itself contributes
to the enrichment of soil nutrients. In addition, litter production, root exudates, and
deadfall all contribute to enriching the soils in the vicinity of the shrub [51]. Thus
shrubs in drylands are potent collectors of resources and [52, 53] are often referred to as
“islands of fertility” [54]. Shrubs also act as a cradle for biological diversity, protect-
ing the communities from ultraviolet radiation and decreasing evaporation through
shading [55].
Nutrients in the shrub root zone are vertically distributed with the majority of nu-
trients being a few millimeters under the surface [53, 56]. This suggests a low mixing
of the soils and implicates litter production as a large source of the resource accu-
mulation [57]. Shrub canopy zone soils support increased microbial activity, as soil
respiration rates are generally higher in shrub root zone soils than in interspace soils
(e.g., [57–59]). This effect seems to be specific to shrubs as similar increases are not ap-
parent in the vicinity of annual grasses [59]. Despite consistent findings of increased
metabolic activity in under shrub soils, the characteristics of the biologic communi-
ties in shrub zones versus interspace soils are not as uniform. Shrub zone soils tend to
support a higher abundance of macroinvertebrates and nematodes [61–63], although
shrub zone soils may harbor similar or even decreased levels of insect diversity [64].
For soil bacteria and fungi, studies have found an increased [65–67] or no effect [68] on
their abundance, although the composition of the communities between the two habi-
tat types generally differs [69]. More recently, studies employing replicated sequenc-
ing datasets have shown that the differences between the shrub associated communi-
ties and interspaces were primarily due to a difference in the abundance of the species
rather than the membership of the communities (󳶳 Fig. 1.2 [68, 70]). In other words,
shrub canopy soils harbor roughly the same bacteria and fungi as interspace soils,
but the structure of the community differs. This has two important implications. First,
it suggests that the bacteria and fungi that are well adapted to inhabiting arid soils
may be ubiquitous across the landscape, even in habitat patches that show different
characteristics. Secondly, there may be a relatively small number of bacterial and fun-
gal species that need to be accounted for to understand biogeochemical cycles and
functioning of arid soils.
A. Bacterial OTUs B. Fungal OTUs

% of sequence reads % of sequence reads
25 20 15 10 5 0 5 10 30 20 10 0 10 20 30 40 50 60
Shared
Shared
Roots Biocrusts
Roots Biocrusts
Biocrusts Root zones Biocrusts Root zones
Fig. 1.2: Similarity in membership of bacteria and fungi between dryland habitats. Each panel de-
notes the relative abundance of either bacterial of fungal operational taxonomic units (OTUs) in bio-
crusts or the root zones of creosote bushes. The OTUs are split into three categories, OTUs shared
between the habitat patches, those unique to biocrusts, and those unique to the root zones. For
both the bacteria and fungi the most abundant OTUs were shared between the habitats, suggesting
a similar membership for the communities in both habitats, although the abundance of those same
OTUs varied widely between the two habitats. Thus the membership of the communities is similar,
although the structure may vary. Figure adapted from [68].
1.3.3 Biological Soil Crusts
The surface soils between rocks and plants of arid regions are not devoid of life. In
fact, some of the most diverse arid soil communities occur in plant interspaces of arid
and semiarid lands as communities colonizing surface soils. These communities form
a surface crust that has been variously referred to as cryptogamic, microbiotic, crypto-
biotic, or microphytic [71]. More inclusively, the term biological soil crusts (shortened
to biocrusts for this chapter) has been used to refer to the biological crusts that inhabit
a multitude of arid lands [72, 73]. In some arid lands, biocrusts cover up to 60–70% of
the surface soils [74]. Biocrusts have been identified on every continent on Earth and
are a conspicuous feature of drylands worldwide [75].
The keystone species of most biocrusts are cyanobacteria [76–78]. Filamentous
species of cyanobacteria, predominantly in the order Oscillatoriales, such as Micro-
coleus vaginatus form the structural component of the biocrusts [79]. These organ-
isms bind soil particles together and produce fixed carbon for other community mem-
bers [80]. Some of this carbon is in the form of extracellular polymeric substances
that act as the glue to bind the soil together and the matrix to create the surface crust
biofilm [81]. Other cyanobacteria in the biocrusts fix atmospheric nitrogen or produce
pigments, such as scytonemin, that protect the crust organisms from ultraviolet radi-
ation [82–84]. Beyond cyanobacteria, biocrusts harbor mosses, lichens, fungi, algae,
a variety of heterotrophic bacteria, and archaea [85–89]. This also leads to an enrich-
ment of other soil fauna, as nematode populations are more abundant and diverse in
mature biocrusts [88]. Because the dominant species of biocrusts are phototrophic,
the biomass of the crusts is concentrated in the upper few millimeters of soil, but
leaching of these nutrients can enrich surrounding and underlying soils [56]. In this
regard, biocrusts are a complex and diverse ecosystem that support multiple trophic
levels and enrich the surrounding soils.
Biocrusts perform a multitude of ecological services. The pinnacled and rough-
ened surface of biocrusts trap dust, collecting nutrients and aiding in water reten-
tion [90, 91]. The physical binding of soil particles increases aeration and reduces soil
erosion by wind and water [92–95]. Biocrusts are a significant source of fixed carbon
and nitrogen in a landscape where plants are sparse [96]. The presence of well de-
veloped biocrusts can elevate the amount of organic carbon by 3000% compared to
surrounding bare soils [75]. Similarly, biocrusted soils have been found to enrich ni-
trogen by a factor of 200%, the majority of which is rapidly leached into surrounding
soils [97–99]. This nutrient trapping and leaching may also assist in the establishment
and development of desert plants [100–102]. Some evidence even suggests that there
may be fungal nutrient bridges that allow for the passage of nutrients between bio-
crusts and plants [103, 104]. In this respect, biocrusts are not isolated soil patches of
increased soil fertility but are an integral component to dryland ecosystem function.
1.4 The Pulse Reserve Paradigm of Arid Ecosystems
Dryland ecosystems are not just defined by a lack of water; precipitation occurs as
episodic events. Therefore, an essential resource (water) is only available in pulses,
with large intervening periods of limitation. In this respect, it is not enough to con-
sider the amount of available water only but also the size, duration, and periodicity
of precipitation events. In 1973, Noy-Meir [105] proposed the “pulse reserve” model of
production in arid systems. Conceptually the model proposes that a pulse of water,
provided through a precipitation event, stimulates the initiation of biological activ-
ity (generally photosynthesis). After a period of activity the organism builds reserves
of energy to sustain it through the following dry period and to the next pulse. This
model was developed for dryland plants but it has also been shown to be applicable
to mosses [106] and cyanobacteria [107]. A central aspect of this model is that pre-
cipitation events need to be “biologically meaningful,” in that the water needs to of
sufficient amount and duration to stimulate biological activity [108]. This sets up a hi-
erarchical response to precipitation events. Small precipitation events will stimulate
soil cyanobacteria or algae but are inadequate to initiate plant activity [109]. For ex-
ample, it has been estimated that ∼ 2 mm precipitation events are generally adequate
to activate soil cyanobacteria within a few minutes, whereas plants may require in the
range of 3–5 mm of precipitation with soil moisture lasting for at least an hour [11]. In
this respect, understanding dryland ecosystems extends beyond just considering the
limitation of water and must consider the magnitude, duration, and timing of precipi-
1.7 Summary | 7
tation events. The factors in drylands that act to limit photosynthesis, thus constrain-
ing the buildup of reserves, are discussed in Chapter 7.
1.5 Response of Arid Ecosystems to Disturbance
Arid lands are under threat from a variety of sources. Human impact due to agri-
culture, recreation, and mineral extraction all dramatically affect arid lands world-
wide [110, 111]. Changes in climate are warming drylands and changing precipitation
patterns [112]. Because arid soil communities survive at the lower thresholds of wa-
ter availability to support life, even small disturbances have the potential to alter the
composition and function of arid soil communities dramatically. As a consequence of
the low biodiversity of arid soils there are generally lower levels of functional redun-
dancy in the community [113]. Thus the loss of a community member may result in a
tipping point at which the community may not easily recover. Experimental manipu-
lations testing the effects of chronic physical disturbance and climate change pertur-
bations have been conducted in drylands and show that the structure and function-
ing of arid soil communities can be severely altered by even relatively small perturba-
tions [106, 107]. Chapter 8 investigates how dryland communities respond to pertur-
bations, particularly those associated with climate change.
1.6 Arid Ecosystems as a Model for Soil Biology
As mentioned previously, arid soils generally harbor less diverse soil communities
than other soils. Further, arid soils also often show a characteristic of trophic sim-
plicity, the communities of arid soils are generally composed of only a limited number
of trophic levels, and these levels generally become more simple as the environment
becomes more extreme [35]. This relatively low biodiversity and complexity allows re-
searchers to disentangle the biologic, climatic, and environmental factors that drive
the composition and functioning of ecosystems more easily. Thus, arid soil systems
have been proposed as a system to understand biodiversity ecosystem function rela-
tionships better [114]. In Chapter 9 artificial soil microcosms and their contribution to
understanding soil biological processes are discussed.
1.7 Summary
The Earth’s drylands are a diverse patchwork of systems united by a common feature
of limited water availability. While the differences between drylands are numerous,
certain aspects of limited moisture lead to predictable patterns in the diversity, ener-
getics, and composition of soil communities. The purpose of this book is to document
what is known about these patterns and to try to disentangle the biotic and abiotic
factors that shape the distinct, unique, and often overlooked soil communities of arid
lands.
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Carlos Garcia, J.L.Moreno, T. Hernandez, and F. Bastida
2 Soils in Arid and Semiarid Environments:
the Importance of Organic Carbon and Microbial
Populations. Facing the Future
Abstract: Drylands occupy 47% of the Earth’s land area and accumulate 35–42 t car-
bon (C) ha−1 . In comparison to other biomes, the natural depletion of C content in arid
and semiarid lands harbors a high potential for carbon sequestration. We provide a
comprehensive review of carbon biogeochemistry, the associated microbial commu-
nities and strategies for soil restoration in drylands under the scope of global change.
In these areas, the biogeochemistry of organic carbon is governed by climate condi-
tions. Photodegradation, water availability and temperature, overcontrol microbial
activity and hence carbon cycling. Under limited water availability, microbial activ-
ity is diminished and hence the organic matter accumulation in soil increases, but the
development of a sustainable plant cover is not promoted. Soil degradation as a con-
sequence of low carbon content can be avoided by organic amendments consisting of
biosolids (composts, sludges, etc.). Organic amendments promote an increase of soil
organic matter and microbial activity, which are linked to a rise in soil fertility. Ap-
propriate management practices in cropland and shrub lands, which have deep soil
profiles with low organic carbon saturation, seem to be a win–win option for seques-
tering carbon and improving soil productivity. This fundamental research is needed to
balance soil fertility and carbon sequestration, particularly under the global change
scenario.
2.1 Introduction
Drylands occupy 6.31 × 109 ha or 47% of the Earth’s land area (UNEP 1992) and are
distributed among four climate zones: hyperarid (1.0 × 109 ha), arid (1.62 × 109 ha),
semiarid (2.37 × 109 ha), and dry subhumid (1.32 × 109 ha). Arid and semiarid or
subhumid zones are characterized by low and erratic rainfall, periodic droughts, and
different associations of vegetative cover and soils. The annual rainfall varies from up
to 350 mm in arid zones to 700 mm in semiarid areas.
Desertification is the main problem that arid and semiarid lands face. Within the
context of Agenda 21, desertification is defined as “land degradation in arid, semi-arid
and dry subhumid areas resulting from climatic variations and human activities” [1].
Either due to human induced actions or natural conditions, the loss of soil organic
matter (SOM) is strongly linked to soil degradation and desertification in arid and
semiarid areas, and causes a decline in agronomical productivity and failure of soil
ecosystem services. Although arid and semiarid ecosystems have less vegetation and,
DOI 10.1515/9783110419047-002
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16 | 2 Soils in Arid and Semiarid Environments
hence, lower carbon accumulation than boreal or tropical areas, they are estimated to
contain 20% of the global soil C pool (organic plus inorganic) in continental areas [2].
Lal et al. (2004) [3] concluded that the predicted amounts of carbon in drylands are
159–191 billion tons, with a density of 35–42 (t C ha−1 ). If we compare the latter value
with the values estimated for boreal (247–344 t C ha−1 ), tropical (121–113 t C ha−1 ), and
tundra (121–127 t C ha−1 ) ecosystems, it is clear that soils under this climate are de-
pleted in carbon, both for “natural” or “anthropogenic” reasons. The hypothesis is
that these soils still have capacity for carbon sequestration, which would increase soil
quality, ensure food security, and mitigate global change [3].
The organic matter content of soils is subjected to strong and complex physical,
chemical, biochemical, and biological controls that are ultimately responsible for car-
bon stabilization and its mineralization [4, 5]. An alteration of such equilibriums due
to land use (i.e., tillage) [6, 7] and climate pressures may alter the C stocks in soils and
potentially cause soil degradation, hence affecting the sustainability of the planet.
The degradation of soils due to carbon losses in many arid and semiarid areas of the
planet cannot be afforded in the future for two reasons:
1. Many of these areas are located in extensive agricultural zones (i.e., California,
Israel, southeastern Spain, southern Italy, Greece, etc.) and must provide enough
food for a growing population.
2. The need for global change mitigation by C sequestration, where these soils can
play a key role.
Considering that, ultimately, the dynamics of organic carbon are governed by bio-
chemical and microbiological processes, we aim to present the main findings and
trends concerning the biogeochemistry of organic carbon and the intrinsic dynam-
ics of microbial communities in soils developed under arid and semiarid conditions.
The role of organic matter, the significance of the microbial biomass, and the structure
of microbial communities will be highlighted, with special emphasis on soil restora-
tion strategies and the application of methods that provide novel knowledge. Finally,
we reflect on the main gaps in our knowledge that should be addressed in order to
increase the ecological value of soils located in arid and semiarid areas in the future.
2.2 Climate Regulation and Soil Organic Carbon

in Arid-Semiarid Zones
Climate change is a special concern regarding the control of SOM. Variations in tem-
perature and precipitation may alter both biotic and abiotic factors that control car-
bon immobilization in semiarid areas. The positive microbial community feedback in
response to elevated CO2 concentration and warming can accelerate the microbial de-
composition of SOM and potentially lead to soil C losses [8]. However, at the global

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2.3 Land Use and Soil Organic Carbon in Arid-Semiarid Zones | 17
level, the effects of temperature on the decomposition of SOM are less clear [9]. Some
studies have indicated that global emissions of CO2 as a consequence of SOM decom-
position would increase as a response to rising temperatures [10]. In contrast, it has
been suggested that dryland soils would most likely sequester C with a future increase
in precipitation but release C with a decrease in precipitation [11].
Episodic water availability clearly affects element cycling in arid and semiarid
ecosystems [12]. High temperatures and erratic moisture inputs impose a pulsed pat-
tern on biological activities [13], which, in turn, will determine the C and N turnover;
so, organic matter tends to accumulate during dry periods when plant and micro-
bial growth are restricted [14]. Moreover, drought affects the quality and composition
of humic acids, which – biologically and chemically – are the most active fraction
of SOM [15]. Thus, losses of aliphatic and polysaccharide-like structures, secondary
amides, polycondensed aromatic systems of large molecular size, and other unsatu-
rated bond systems such as carbonyl and carboxyl groups were observed in semiarid
soil humic acids after a long drought [14].
Soil processes in arid lands are controlled principally by water availability but
the photodegradation of above ground litter and the overriding importance of spatial
heterogeneity are modulators of the biotic responses to water availability [16]. Micro-
biological soil properties are negatively affected by drought since soil moisture plays
a key role in the survival and activity of soil microorganisms [14]. Mechanisms such as
the retarded diffusion of soluble substrates and/or reduced microbial mobility (and
consequent access to substrates) could explain the low microbial biomass found in
soils with low water content [17]. Liu et al. (2009) [18] suggested that soil water avail-
ability was more important than temperature in regulating the soil microbial respira-
tion and microbial biomass in a semiarid temperate steppe. Accordingly, some authors
have found that organic matter stocks are progressively preserved with the increasing
duration and intensity of droughts [19]. Conversely, an experimental field study about
the impact of climate change on desertification along a Mediterranean arid transect
demonstrated that the SOM content decreased with aridity [20].
2.3 Land Use and Soil Organic Carbon in Arid-Semiarid Zones
Adequate land use management helps to control the global stocks of organic carbon
in drylands and fight against soil desertification [11, 21]. Despite the extensive num-
ber of studies aiming to evaluate the effects of land use on organic C stocks, there
are still some discrepancies. For instance, the conversion of ecosystems from natu-
ral conditions to agricultural use generally results in decreased carbon stocks in arid
and semiarid climates [22, 23]. Disturbance by shrub removal and/or livestock grazing
significantly reduced the amount of organic matter in an Australian semiarid wood-
land [24]. However, other studies did not find any significant effect of land manage-
ment on soil organic carbon (SOC) [22, 25]. As stated by Booker et al. (2013) [26], car-

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bon uptake in arid and semiarid areas is most often controlled by abiotic factors that
are not easily changed by management or vegetation. In this sense, photodegrada-
tion, which is highly intense in arid ecosystems, exerts a dominant control on above
ground litter decomposition [27]. Losses through photochemical reactions may repre-
sent a short circuit in the carbon cycle, with a substantial fraction of the carbon fixed
in plant biomass being lost directly to the atmosphere without cycling through soil
organic matter pools [27]. More studies based on the prevention of photodegradation
should be carried out to promote carbon sequestration in soil and climate change mit-
igation. For instance, the placement of a wide vegetation cover may reduce the effects
of photodegradation and enhance soil moisture.
Reforestation may influence carbon balances, increase soil carbon stocks and
serves for fighting against desertification in many arid and semiarid regions [28, 29].
In general, soils in arid and semiarid conditions depict a positive relationship be-
tween the organic carbon content and plant cover [30, 31]. Nevertheless, the spatial
heterogeneity of plant cover in semiarid shrublands is the principal cause of the spa-
tial heterogeneity of the SOC content, which is associated with the development of
islands of fertility under shrubs [32].
2.4 Soil Restoration in Arid-Semiarid Zones:

Amendments Based on Exogenous Organic Matter
The scant vegetation of the soils in arid and semiarid zones, which is mainly a result of
low productivity and subsequent abandonment, causes the inputs of organic matter
into the soil to be low. Hence, together with the usual soil erosive processes and high
photodegradation rates, many soils have a low organic matter level, which compro-
mises their functionality and the provision of ecosystem services and can even end in
intense degradation phenomena.
Since the Kyoto Protocol of 1992, which identified soils as a possible sink for car-
bon, there has been much progress. A report on organic matter and biodiversity within
the European Thematic Strategy [33] mentions that exogenous organic matter, that is,
organic materials added to a degraded soil in order to improve harvests or restore it for
subsequent use, constitutes an invaluable source of organic matter and contributes to
the fixation of C in the soil, thus partially diminishing the greenhouse effect derived
from the release of CO2 to the atmosphere.
The application of organic materials enhances the nutrient status of soil by serv-
ing as a source of macro and micronutrients, and improves its physical properties by
increasing soil porosity and water retention because of the presence of humic-like
substances, known as a polycondensed macromolecular structure. In addition, one
of the beneficial effects of humic substances is that soil enzymes bound to humic frac-
tions remain protected in the long term against denaturalization by proteolysis attacks

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in soil. The use of organic amendments to improve soil quality and restore degraded
lands has been widespread [34–36]. Application of organic amendments usually im-
proves soil aggregation [37] and, hence, the physical structure of the soil [38, 39]. Fur-
thermore, organic amendment generates a better nutritional scenario for progressive
plant growth [40, 41]. Plant inputs to soil promote the development of the microbial
biomass and its activity, which raises soil fertility in the long term [36, 42, 43]. Different
types of organic amendments have been applied in arid and semiarid environments:
crop residues, pig slurry, farmyard manure, municipal solid waste, olive mill waste,
sewage sludge, etc. However, the addition of organic amendments to soil has to be
carried out carefully since it does not always lead to an increase in soil quality. For
instance, Tejada et al. (2007) [44] reported that the application of fresh beet vinasse
worsened the physical and biological properties due to its content of sodium ions.
In addition to the carbon inputs arising from the above ground development af-
ter amendment, the organic amendments themselves provide exogenous carbon that
may persist in the soil. The stability and nature of the amendment can determine the
residence time of the added organic carbon [45, 46]. In dryland ecosystems, due to the
high potential for carbon sequestration, the stabilization of SOM is believed to be con-
trolled more by the quantity of the inputs and its interaction with the soil matrix (i.e.,
texture) than by the quality of the organic amendment [47, 48]. It is thought that fine
soil particles have a critical role in C fixation. Some authors observed an increase in
the carbon fixation into fine particles (clay or silt) after organic amendment [48, 49],
while others did not find any variation in the organic carbon content of the fine frac-
tions in the long term [22]. Recent studies based on carbon stable isotope probing have
also suggested a protective role of clays [50, 51], even concluding that there is major
fixation of carbon in clay soils despite the highly labile nature of added carbon (i.e.,
13 C-glucose) [50].
Regardless of the fact that part of the added carbon probably persists in soil phys-
ically linked to soil particles, a clear benefit of organic amendment derives from the
improvement in the nutritional conditions of the soil – which enhances subsequent
plant growth (󳶳 Fig. 2.1). Plant development provides organic matter to the soil, bene-
fits its structure, and avoids soil erosion, a very important issue in sloping areas [36].
2.5 Microbial Biomass and Enzyme Activity in Arid-Semiarid Zones
As stated above, the microbial biomass is largely responsible for soil carbon cycling.
The microbial biomass of semiarid soils is usually constrained by the low amounts
of plant inputs and water availability. The evaluation of microbial biomass by phos-
pholipid fatty acids (PLFAs) analysis revealed that the total PLFAs ranged between 2.2
and 100 nmol fatty acids g−1 soil in arid and semiarid areas [41, 52–55]. Nevertheless,
the interpretation of PLFA patterns in extremely arid ecosystems must be done care-
fully [52]. Water activity below a certain threshold may protect cellular remains from

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18 months after organic

amendment restoration
Fig. 2.1: Field experiment in Spain: soil restoration.
degradation [56]. Hence, the results obtained following treatment might be biased by
the previous viable microbial community.
Generally, the level of biomass correlates well with the amount of organic carbon
and is closely related to the moisture content of dryland soils. For instance, various au-
thors have observed changes in the microbial biomass linked to the organic carbon af-
ter a change in land use [57, 58]. Similarly, the restoration of soil quality by addition of
organic waste byproducts increases the microbial biomass 1.6–3 times [41]. The micro-
bial biomass also responds to plant growth and the parallel increase in SOM [52, 55]. In
detail, Ben-David et al. (2011) [52] found that the fatty acid 16:1w7, indicative of cyano-
bacteria [59], increased in intershrub soils of the Negev Desert (Israel); this suggests
an increase in the relative abundance of cyanobacteria, which are known to be the
primary colonizers of biological crusts in drylands [60].
Dry periods may have a deleterious effect on bacterial communities through star-
vation, induced osmotic stress, and resource competition, which affects the structure
and functioning of soil bacterial communities and leads to a slowing down of N and
C mineralization [14, 61]. For soils that have not received recent organic matter addi-
tions, wet–dry cycles initially stimulate C and net N mineralization and diminish the
microbial biomass during drying but stimulate microbial growth after wetting, and
the wet–dry cycle itself results in higher net N and C mineralization when compared
to continuously moist soils [62, 63]. Accumulation of inorganic N usually occurs dur-
ing dry periods because diffusion of ions is severely restricted in the thin water films
of dry soil and because sinks of inorganic N are limited by reduced microbial growth
and limited plant uptake [14, 64]. A portion of the microbial biomass is killed under
dry conditions [65]; this is readily decomposed by surviving organisms when the soil

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is rewetted. This dead microbial biomass, with its low C:N ratio, becomes available for
microbial activity and leads to high N mineralization, large pulses of CO2 and gaseous
fluxes of N, and a pulse of increased C and N availability.
In principle, as stated by Entry et al. (2004) [57], Gram positive biomarkers would
be expected to increase in desiccated or degraded soils due to their sporulation ca-
pacity under harsh conditions. However, this trend is usually not found [14, 41, 54, 57].
Perhaps, the relatively fast response of soils to nutrient or water pulses might be taken
into consideration, and the measurement of PLFAs at a particular time has to be dis-
cussed carefully. Moreover, only a fraction of the microbial biomass survives both the
dry season in arid environments and the osmotic shock associated with the rapid in-
crease in moisture after the first rainfall [66].
The microbial biomass is responsible for the production of enzymes that are ex-
creted into the extracellular microenvironment, where they can be protected by immo-
bilization in humic and clay colloids [67, 68]. The basic importance of enzyme activity
in soil lies in the fact that ecosystem functioning cannot be totally understood with-
out the participation of enzymatic processes and their catalytic reactions related to
nutrient cycling [69]. Extracellular enzymes are closely related to organic matter de-
composition, and key enzymatic reactions include those involved in the degradation
of cellulose and lignin, those that hydrolyze reservoirs of organic N such as proteins,
chitin, and peptidoglycan, and those that mineralize P from nucleic acids, phospho-
lipids, and other ester phosphates [70]. Extracellular enzyme activity (EEA) mediates
microbial nutrient acquisition from organic matter, and these activities are commonly
interpreted as indicators of microbial nutrient demand and soil quality [69, 71]. In gen-
eral, enzymes are associated with viable, proliferating cells, but they can be excreted
from a living cell or released into the soil solution from dead cells. Once enzymes have
left the shelter of the cell, they are exposed to an inhospitable environment in which
nonbiological denaturalization, adsorption, inactivation, and degradation by prote-
olytic microorganisms all conspire to harm the enzymes, unless they survive due to
the new protection afforded by the mineral and/or humic association, which is more
resistant to proteolysis than the free enzymes.
In arid and semiarid environments, the soil EEA has been used to examine the
functional responses of the soil microbial biomass to factors such as increased nutri-
ent deposition [72], heavy metal contamination [73], organic amendment [36, 41, 74],
soil management [75–77], plant diversity [78], type of agroecosystem [79], and climate
change [80].
More than any other factor, OM dynamics are closely related to the regulation of
enzyme activity. In arid and semiarid areas, the potential activities of enzymes that
decompose proteins (e.g., aminopeptidase) and recalcitrant C compounds such as
lignin and humic substances (e.g., phenol oxidases) exceed those of mesic soils by
more than an order of magnitude in both absolute terms and in relation to the ac-
tivities of enzymes that break down cellulose, which generally dominate the EEA of
mesic soils [81]. The pH is a strong regulator of EEA, with important consequences for

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SOM dynamics. Because of carbonate accumulation, the pH of arid soils can reach 8 or
above, which is optimal for phenol oxidase enzymes [82]. In contrast, the pH optima
of glycosidases (e.g., cellulase, chitinase) generally range from 4 to 6.
Soil texture and moisture also determine the enzyme activity, by influencing the
microbial biomass and by controlling the substrate availability. When the soil mois-
ture is low, the EEA is also low. Prolonged droughts are likely to decrease enzyme pro-
duction, resulting in lower measured activities when moisture returns [83]. Because
rewetting sometime results in a pulse of microbial biomass turnover [84, 85], many
intracellular enzymes may be released into the soil, creating a temporary increase in
EEA. Prolonged precipitation can result in increased EEA in arid or semiarid soils [80],
although this may be at least partially due to enhanced plant growth and rhizodepo-
sition [86].
2.6 Organic Carbon, Macro and Microaggregates,

and C Sequestration in Arid-Semiarid Zones
Converting forest to cultivated areas reduces soil organic carbon mainly through the
reduction of biomass inputs into the soil and the stimulation of soil organic matter
mineralization, thus increasing soil erosion rates [87]. There is evidence that the mag-
nitude of this loss of soil organic carbon through cultivation could be greater in semi-
arid areas than in more humid areas [88]; this impact decreases with depth. The anal-
ysis of environmental control factors suggests a negative effect on soil organic carbon
in a climatic change scenario with increased temperature and a decrease in rainfall,
as is expected in semiarid areas. Some data indicate that this negative impact on soil
organic carbon would be greater in soil surface than in the soil subsurface. For this rea-
son, a strategy for C sequestration should be focused on subsoil sequestration. Appro-
priate management practice in cropland and shrubland, which have deep soil profiles
with low organic carbon saturation, seems to be a win–win option for sequestering
atmospheric organic carbon and improving soil productivity.
Some studies confirm that the potential sequestration of C in semiarid reforested
areas depends largely on the techniques used for reforestation. The C stocks in refor-
ested ecosystems are directly proportional to the amount of biomass produced, which,
in turn, is determined by the productivity of the soil. For this reason, methods that im-
prove the productivity of the soil must be used. The addition of organic amendments
to the soil, prior to planting, could be very effective in terms of C sequestration [87, 89].
In semiarid areas, studies on degraded soil rehabilitation have proved that the
addition of organic amendments to these soils increases the percentage of both soil
macroaggregates and microaggregates within macroaggregates, as well as the concen-
tration of organic C in these soil fractions [90]. This is of great interest since microag-
gregation formation is crucial for the storage and stabilization of soil C in the long

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2.7 Conclusion | 23
term [91, 92]. Other authors have reported an increase of C concentration in fine soli
particles (silt and clay) with the addition of organic amendment to semiarid degraded
soils [49, 93].
In semiarid and arid soils, the chemical stabilization of organic carbon, through
the formation of complexes with silt and clay particles and their physical protection
in microaggregates formed within macroaggregates, could be the main mechanism
of C sequestration in these soils, in both agricultural and forest areas. The physical
protection of soil organic carbon could be promoted by the changes, both qualitative
and quantitative, in plant contributions to soil. In both forested and agricultural ar-
eas in semiarid climates and where a green cover has been incorporated, an increase
in the labile pool of soil organic carbon occur [94]. Fresh plants induce the formation
of macroaggregates both directly, by acting as a binding agent between soil particles,
and indirectly, by activating the production of microbially derived binding agents. The
establishment of these new macroaggregates can increase the formation of microag-
gregates that occlude organic matter inside and make it inaccessible to the microor-
ganisms [90, 95].
In the agricultural soils in semiarid and arid areas, minimum tillage seems nec-
essary, since it promotes the incorporation of plant material into deeper layers, pro-
moting the formation of aggregates and, therefore, organic carbon occlusion within
them [94].
A strong positive correlation between basal soil respiration and the percentage
of microaggregates within macroaggregates has been found in reforested soils, while
this correlation was negative in degraded shrubland [96]. This suggests that the for-
mation of microaggregates, which are rich in organic carbon, could be a self defense
mechanism of the soil to protect organic carbon from increased microbiological activ-
ity [96]; for these reasons, these correlations could serve as indicators of processes of
improvement (positive correlations) or degradation (negative correlation) of the soil.
2.7 Conclusion
Soil degradation due to aggressive human action or passive climate pressure must be
avoided in order to conserve soils that have a high ecological value for the future. The
fragility of these soils contrasts with their intense response to soil restoration pro-
grams, which include the addition of organic matter and their potential capacity for
carbon sequestration. Organic amendments help to preserve and improve the quality
and fertility of the soils in these areas, which could be particularly important under a
global change scenario.
The biogeochemical and microbiological information on arid and semiarid soils
is abundant but perhaps more limited than that for other climates. Nevertheless, such
studies are widespread across the planet and numerous research groups are focused
on the topic. This fact will increase our knowledge of the biogeochemistry of carbon,

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as well as our capacity for managing the cycling of elements and the sustainability of
arid and semiarid soils in the future.
However, if we aim to increase such an “ecological capital,” soil science must nec-
essarily move on and search for answers to new, more focused questions:
1. Which biochemical processes are responsible for carbon fixation and humus forma-
tion?
2. Are we able to “control” the microbial populations and carbon related biochemical
reactions of these soils?
The mutual benefits of microbial activity, carbon sequestration, and plant growth are
clear in terms of sustainability. To enhance the physicochemical protection of soil or-
ganic carbon the stability of microaggregates should be maximized, while ensuring a
suitable rate of macroaggregate turnover that will allow the fixation of new organic
carbon. This could be promoted by minimum tillage, an increase of plant inputs, par-
ticularly root inputs (by modifying residue amount and quality, altering mycorrhizal
associations and vegetal species), etc. It can promote the formation of new macroag-
gregates that can increase the formation of microaggregates that occlude organic mat-
ter inside and make them inaccessible to the microorganisms.
However, fundamental research is needed to balance soil fertility and carbon se-
questration with economic or environmental needs. Managing soil conditions or de-
signing “à la carte” organic amendments, which promote a punctual rise in fertility
when needed (i.e., an increase in agricultural productivity) or foster carbon sequestra-
tion for environmental purposes in abandoned lands at a particular moment, would
definitively increase the ecological value of arid and semiarid soils in the coming era.
Acknowledgment: F. Bastida thanks the Spanish Government for his “Ramón y Ca-
jal” contract (RYC-2012-10666) and FEDER founding. The authors are grateful to the
Fundación Séneca of Murcia Region (19896/GERM/15). The authors thank the Span-
ish Ministry for the CICYT projects AGL2014-55269-R and AGL2014-54636.
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Gary M. King
3 Water Potential as a Master Variable
for Atmosphere–Soil Trace Gas Exchange
in Arid and Semiarid Ecosystems
Abstract: Soil water status strongly affects qualitative and quantitative aspects of soil–
atmosphere trace gas exchange. Soil water status is most often expressed in terms
of gravimetric water contents, which can be particularly useful when translated to
gas filled pore space. Gas filled pore space has predictive value for both gas transport
rates and the types of processes involved in gas production and consumption. How-
ever, water potential offers deeper insights that reflect the physiological responses of
cells, while also providing a basis for comparing activities among different soil types
and across wetting and drying events. Nonetheless, relatively few studies have incor-
porated water potential measurements with analyses of trace gas fluxes. Results for
atmospheric methane uptake suggest similar sensitivities to water potential for arid
soils and forest soils, with strong inhibition below −0.5 MPa. Atmospheric CO uptake
in forest soils shows sensitivities similar to those of methane uptake, but recent ev-
idence suggests that CO oxidizers in arid and saline soils might maintain activity at
remarkably low potentials. Advances in sensor design should facilitate much more ex-
tensive analyses of water potential, more mechanistic models of trace gas exchange,
and a better understanding of the controls trace gas dynamics.
3.1 Introduction
Water plays a profoundly important role in soil–atmosphere gas exchange [1–6]. Wa-
ter shapes plant communities; litter development; the presence and characteristics of
soil horizons; soil organic matter content; microbial community composition, struc-
ture and activity; soil texture, porosity and gas transport [7]. All of these variables
interact with water regimes to determine rates of gas emission to, or uptake from, the
atmosphere.
This is no truer for tropical rainforests than it is for arid ecosystems, the char-
acteristics of which often reflect long term climate change, and not just contemporary
hydrologic regimes. For example, the playa soils of the northwestern United States are
mostly remnants of extensive Pleistocene lakes that disappeared as a consequence of
global climate change (e.g., Lake Bonneville), leaving behind fine grained sediment
beds that progressively evolved in response to sparse plant colonization and strongly
seasonal patterns of temperature and precipitation [8].
Although water limitations often lead to relatively low rates of gas exchange per
m2 , soils in arid and semiarid ecosystems can still play significant roles in some global
DOI 10.1515/9783110419047-003

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32 | 3 Water Potential as a Master Variable for Atmosphere–Soil Trace Gas Exchange
trace gas budgets; this is because they account for roughly one third of the total ter-
restrial surface area [9]. For example, the global soil methane sink is substantially
less than it would be if uptake rates in arid systems were equivalent to those in grass-
lands and forests. Likewise, global uptake of atmospheric carbon monoxide is reduced
by the combination of low uptake rates in some arid soils, and emissions from oth-
ers [10, 11].
Gas exchange in arid and semiarid ecosystems is sensitive to natural and anthro-
pogenic disturbances, many of which affect water regimes and related variables [12–
17]. Climate change, for instance, may result in increased thermal stress and prolonged
periods of drought punctuated by extreme precipitation. Irrigation for agriculture has
resulted in soil salinization, in some cases rendering soils unsuitable for crop produc-
tion, and changing local biogeochemical dynamics [18].
While many variables obviously contribute to rates and patterns of gas exchange
in arid systems, soil water potential is arguably the most important. Water potential,
which is a measure of water availability, affects gas production and consumption at
the level of cells, and elicits immediate responses as it changes through its impact
on cell physiology [19]. However, in spite of its importance, relationships between
trace gas dynamics and water potential have not been characterized extensively. An
overview of these relationships and recent observations are summarized here.
3.2 Water Potential and Water Potential Assays
Although several weight or volume based indices provide convenient measures of soil
water content (e.g., [20]), and are useful in the context of variables such as gas dif-
fusion and advection (e.g., [21, 22]), they provide little insight about the physiologi-
cal responses of microbes to soil water status, and often cannot be directly compared
among systems [23]. In contrast, soil water status can be more completely specified
using physical chemical terms (e.g., [19, 24, 25]). The rationale for using a physical
chemical description of water as an alternative to volumetric measures is simple. The
direction of water movement across cell membranes cannot be predicted on the basis
of weight or volumetric measures of water content, but can be predicted using mea-
sures of the energy status of water, and water potential in particular.
Water potential calculations begin with the mole fraction of water in a solution:
Nw = nw /(nw + n i ) ,
with nw representing number of moles of water kg−1 of solvent (= molality, about

55.51 mol kg−1 or 55.51 m) and n i representing the moles of solute kg−1 of solvent.
Since solutions are often not ideal in a thermodynamic context, an activity coeffi-
cient, γ, specific for a given solute, is applied, yielding a definition for water activity:
aw = γNw .

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3.2 Water Potential and Water Potential Assays | 33
Water activity is often used as a temperature independent measure of water availabil-

ity, and water activity values will be presented below when relevant for specific dis-
cussions. Where appropriate, a water potential equivalent will be presented for a tem-
perature of 25°C. Though there are some advantages to a temperature independent
measure of water status, water activity itself does not necessarily predict directions of
water flow, and it is inadequate for complex, multiphase systems such as soil. Water
potential provides a more complete measure of water availability.
Water potential is defined in energetic terms as the partial molal free energy of
a solution of water under specified conditions of solute composition, temperature,
pressure and gravitational potential:
μw = (∂G/∂nw )n i ,T,P,h ,
where G represents Gibbs free energy, n i is solute concentration, P is pressure, and

h is height (ignored in most biogeochemical contexts [23]). This yields a working ex-
pression for the chemical potential of water:
μw = μ 0w + RT ln aw + Vw P ,
where μ 0w represents the chemical potential of water in a standard reference state; R, T

(in Kelvin) and P represent the gas law constant, temperature, and pressure, respec-
tively, and Vw is the partial molal volume of water (about 1.8×10−5 m3 mol−1 at 25°C).
Rearranging yields:
(μ w − μ 0w )/Vw = RT ln aw /Vw + P ,
where the left hand expression is a chemical potential difference per molal volume
and is designated water potential, ψ:
ψ = RT ln aw /Vw + P .
This expression indicates that water potential in a solution can be subdivided into a
pressure term (taken as a departure from 1 atm) and a solute dependent term. As ap-
plied to soils, the total water potential, Ψ, is typically distributed among three terms:
Ψ = ψs + ψp + ψm ,
where ψs , ψp , ψm are the potentials due to solutes, pressure, and the soil matrix, re-
spectively. The total water potential for any solution is < 0 and is expressed in units
of bars or pascals (N m−2 ). Unlike water activity or other measures of water status, Ψ
provides a complete description that can be compared among systems and used to
predict the direction of water flows, for example into or out of cells.
The matric potential term, ψm , is especially relevant in soils. This potential arises
as a result of the interaction of water at surfaces in a porous matrix, and has been
described by analogy to the behavior of water inside a capillary tube immersed in pure
water. The force associated with the rise of water a distance h in a capillary is related

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to the matric potential within the capillary (= hρg, where ρ is water density [kg m−3 ]
and g is the gravitational constant [m sec−2 ]); the height of capillary rise is inversely
proportional to the capillary radius, r. Soil is essentially a porous matrix in which the
matric potential is related to pore size (i.e., pore radius) and the distribution of water
among pores (a function of water content). When all pores are filled (water saturation),
the matric potential is zero. The matric potential decreases with desaturation due to
the loss of water from larger pores and retention in smaller pores. Progressive loss
leaves the remaining water in smaller pores at progressively lower potentials.
The relationship between water potential and soil pore size distribution has a
number of important consequences, especially for gas exchange. With decreasing wa-
ter content and matric potential, gas transport increases [22, 26, 27], which can accel-
erate some gas transformations as well as exchanges with the atmosphere. However,
water potentials lower than about −0.5 MPa typically inhibit many bacterial activities
due to physiological stresses, physical constraints on substrate transport, cell move-
ment, and the thickness of films available for bacterial immersion. This limitation is
especially relevant for arid soils, which often experience water potentials much less
than −0.5 MPa.
Soil water content can be measured readily using relatively simple gravimetric
methods [28]. Modifications of these methods yield additional indices of soil pore
space, which can aid analyses of soil–atmosphere gas exchange. Several methods and
associated instrumentation are also available for analyses of the water potential. How-
ever, the choice of method depends greatly on the application. Methods suitable for
use in a laboratory context often are unsuited for field use and vice versa. It is also im-
portant to understand whether solute potentials, matric potentials, or both need to be
measured, since this influences method selection. Finally, the range of expected water
potentials must be considered. For arid soils, the range can potentially exceed limits
for any one analytical system, since values can approximate zero during wet seasons
or immediately after precipitation events, but fall below −100 MPa with drying.
For laboratory measurements and water potentials from about −2 kPa to −500 kPa,
a pressure plate apparatus can be used (e.g., [29]). Pressure plates essentially apply
pressure to a soil sample and drive excess water out through a porous ceramic plate.
At equilibrium, the water potential is assumed to equal the applied pressure. The wa-
ter content of the soil sample is then measured. A set of water content determinations
at different pressures is then used to construct a moisture release curve that, in turn,
is used to estimate sample potentials at their initial water contents. Other than its
simplicity, this approach has little to recommend it, since other methods offer greater
accuracy, broader ranges, and more convenience.
Tensiometers, which make direct contact with the soil liquid phase, find use
in both laboratory and field contexts [30]. These instruments use a porous ceramic
reservoir containing pure water (∼ 0 MPa) in contact with a headspace and a pressure
transducer or vacuum gauge. When placed in soil with water at lower potential, water
flowing from the reservoir results in a reduced headspace pressure equivalent to the

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3.3 Limits of Growth and Metabolic Activity | 35
soil water potential. Since flows are reversible, tensiometers can function as piezome-
ters in some configurations. Though inexpensive and typically rugged, their dynamic
range (> −1 kPa to about −100 kPa) substantially limits applications in arid systems.
However, a new microtensiometer might greatly extend these limits [31].
An alternative approach that is well suited for laboratory applications measures
the energy status of water in a vapor phase equilibrated with a soil sample. Dew point
hygrometry has found a wide range of applications, since it is suitable for samples
with water potentials from about −0.1 MPa to < −100 MPa [32, 33]. As implemented
by Decagon Instruments (Pullman, WA) WP4-T, dew point hygrometry covers water
potential values common in arid soils, and does so with good accuracy. However, the
approach and the WP4-T have found limited use in the field due to constraints on tem-
perature control.
In addition to the WP4-T, Decagon Instruments also offers sensors suitable for
field deployment in arid soils [34]. These sensors, e.g., MPS-6, are based on a ceramic
substrate with a known moisture release curve. The sensors can be buried in soil,
where they record both temperature and water potential changes as the water content
of the ceramic substrate varies. The stated measurement range is from −0.01 MPa to
−100 MPa. MPS-6 sensors measure the matric potential and thus are not suitable for
saline soils or other systems with significant solute potentials. In addition, their utility
has not been established for surface soils (e.g., 0–5 cm) that vary substantially over a
diurnal cycle.
3.3 Limits of Growth and Metabolic Activity
The effects of water availability (most often expressed as aw ) on microbial growth have
been given considerable attention in the context of food preservation [35]. Numerous
studies have led to general estimates of lower growth limits for a variety of bacteria
and fungi that commonly occur in processed foods or that contribute to spoilage. In
general, Gram negative bacteria (e.g., Proteobacteria and Bacteroidetes) do not grow
at aw < about 0.95 (−7.06 MPa), while Gram positive bacteria (e.g., Actinobacteria and
Firmicutes) do not grow with aw < about 0.90 (−14.49 MPa) [19]. There are exceptions,
of course. Pontibacillus sp. AS2 and Salinicola sp. LC26 (Firmicutes and Proteobacteria,
respectively) grow at aw = 0.775 (−35.06 MPa), and the actinobacterium Mycobac-
terium parascrofulaceum LAIST_NPS017 grows at aw = 0.800 (−31.93 MPa at 37 °C)
(36). Members of the euryarchaeal Halobacteriaceae, typically grow at aw = 0.755
(−40.60 MPa at 40°C), but limits as low as 0.611 (−67.76 MPa) have been extrapo-
lated from growth data [36]. Many fungi grow at aw = 0.700−0.900 (−49.06 MPa to
−14.49 MPa), but lower limits of 0.611 have also been extrapolated for a few excep-
tional strains [36].
Though studies on water activity collectively represent a reasonably broad survey
of some economically important taxa, they have nonetheless explored relatively few

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species from relatively few phyla (mostly Actinobacteria, Euryarchaea, Firmicutes,

and Proteobacteria), and have been limited by the need to use cultivable isolates.
Thus, water activity limits are essentially unknown for a large percentage of Bacteria,
Archaea, and Eucarya, and for members of soil microbial communities in particular.
Perhaps more importantly, growth limitation by water availability is largely un-
derstood in the context of solute potentials (ψs ), yet matric potentials (ψm ) often de-
termine water availability in soils. While one might propose that the effects of low wa-
ter potential on macromolecules, especially DNA, would be the same regardless of the
mechanism by which water potential is lowered, the ability of cells to respond phys-
iologically to water stress may depend greatly on the relative contribution of solutes
versus pore based capillarity (e.g., [37]). Where solutes dominate total water poten-
tial, Ψ, intracellular water potentials can be adjusted to osmoconformers via solute
transport. When matric potentials dominate Ψ, the ability of cells to adjust may be
constrained by solute availability and by the energy required to synthesize intracel-
lular compatible solutes. This has not been explored systematically, but studies with
isolates have shown differential responses to ψs versus ψm (e.g., [38, 39]). Nonethe-
less, relatively little is known about the growth or activity responses of specific isolates
to matric potential. Addressing this knowledge gap should be a research priority, par-
ticularly since changing precipitation regimes in the future will be accompanied by
changing soil water potential regimes.
Work by Schnell and King [40] with methanotrophs provides an example of the
potential significance of solute versus matric potentials. They used NaCl as a readily
transported solute, and sucrose as an impermeable solute to adjust Ψ in growth me-
dia. While not directly equivalent to a matric potential, a solute potential arising from
an impermeable solute can mimic the effect of matric potentials on cells. Schnell and
King [40] observed that both growth and methane uptake rates were inhibited with
decreasing water potential to a greater degree with sucrose than with NaCl. This sug-
gests that water potential limits for growth might be lower when solutes dominate Ψ.
This is especially relevant for semiarid and arid soils that experience matric potential
extremes well below growth limits due to solute potentials. How do the members of
soil microbial communities cope with such extremes?
While growth certainly provides an exquisitely sensitive index of the ability of
microbes to tolerate extreme conditions, metabolic activity can continue beyond the
limits for growth. Analyses of metabolic activity as a function of temperature have in-
dicated that maintenance and survival metabolism occur at subzero temperatures well
below those at which growth ceases [41]. These results are relevant for understanding
relationships between water availability and metabolism, since bacterial activity in
ice occurs within solutions that have low ψs . However, lower limits for activity have
not been explored systematically as a function of ψs or Ψ for either isolates or mixed
populations in natural systems. This is yet another knowledge gap that should be ad-
dressed. Price and Sowers [41] have suggested that there is no evidence for a minimum
temperature for metabolism, but this might not hold true for water potential.

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3.4 Water Potential and Trace Gas Exchanges
Methane. Water content has a profound and well documented impact on soil–atmos-
phere methane exchanges. At saturation, anoxic conditions can develop, which pro-
mote methanogenesis and methane emission. Numerous variables affect the extent to
which methanogenic activity occurs, including soil organic matter content and elec-
tron acceptor availability. While water potential has not been specifically addressed as
a variable for soil methanogenesis, it is clear that some methylotrophic methanogens
tolerate solute potentials as low as −40 MPa, since they can produce methane in salt
saturated sediments or solutions [42]. Nonetheless, in most cases where methanogens
are active, water potentials are high due to low solute concentrations and the absence
of matric potentials. Furthermore, there are relatively few arid or semiarid soils for
which methanogenesis would have any relevance, since these soils are unsaturated
and methanogenesis is inhibited by molecular oxygen, regardless of water potential
regimes.
Atmospheric methane consumption by methanotrophic bacteria obviously occurs
far more commonly in arid and semiarid soils than does methanogenesis. Due to the
significance of soil methanotrophs for the atmospheric methane budget (e.g., [43]),
numerous studies have addressed the role of variables such as water content, pH, tem-
perature, soil texture, nitrogen content, and land use [6, 44–49]. The effects of water
content have largely been understood in the context of gas transport, with high wa-
ter contents inhibiting uptake from the atmosphere due low diffusion fluxes, and low
water contents inhibiting activity presumably due to undefined water stresses. Water
potential effects per se have been addressed to only a limited extent.
Schnell and King [40] showed that atmospheric methane uptake was very sen-
sitive to water potential in a forest soil. Extreme potentials (e.g., to −10 MPa) in the
“O” and “A” horizons that developed during summer appeared to strongly inhibit up-
take and constrain activity to lower depths, the effect of which was to reduce area
based rates year round. Combined analyses of water content and water potential also
showed that interactions between soil gas exchange, methane concentration, and wa-
ter stress determined uptake rates and responses to water potential. In particular, de-
creasing water content at high water potentials (> −0.2 MPa) increased gas transport
and methane uptake, even though methanotrophs experienced water stress. However,
continued decreases in water content led to increased stress and decreased methane
uptake (󳶳 Fig. 3.1). Addition of exogenous methane to a concentration of 200 ppm min-
imized gas transport limitation and revealed that water stress inhibition developed at
Ψ ≥ −0.2 MPa (󳶳 Fig. 3.1). Isolates were similarly sensitive to water stress, whether it
was imposed as a solute stress or through a mimic of the matric potential.
The patterns observed in Maine forest soils (USA) were confirmed by Bradford et
al. [47] for UK temperate forests, and by Gulledge and Schimel [46] for boreal soils. Wa-
ter stress sensitivity observed for surface soils in these studies likely occurs in surface
soils of arid and semiarid systems, which might explain the subsurface localization of

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0.060 3.0 0.00
Methane uptake rate constant (h–1 gdw–1)
Methane uptake rate (nmol gdw–1 h–1 )

0.055 2.5
–0.20
Water potential (MPa)

0.050 2.0
–0.40
0.045 1.5
–0.60
0.040 1.0
–0.80
0.035 0.5
0.030 0.0 –1.00

–1.0 –0.80 –0.60 –0.40 –0.20 0.0 15 20 25 30 35 40
(a) Water potential (MPa) (b) Water content (%)
Fig. 3.1: (a) Methane uptake rate constants with atmospheric methane and methane uptake rates
at 200 ppm methane versus soil water potential for Maine forest soils. From Schnell and King (40).
(b) Water potential versus water content for the same soils.
a process that depends on an atmospheric substrate (e.g., [44]). If surface soils were
not inhibitory in some manner, they would be the locus of greatest uptake activity,
since the supply of methane is greatest there. However, the lack of parallel, time vary-
ing depth specific water potential and methane uptake data limit extrapolations. Even
so, it is clear that extreme water potentials develop in the surface soils of arid systems,
and that soils most conducive to active methanotrophy occur primarily in deeper hori-
zons (e.g., > 10 cm). Seasonal studies have also shown that the highest methane up-
take rates in arid soils are associated with precipitation events, albeit with a lag, which
indicates that water stress tolerant methanotrophs likely do not occur at substantial
levels.
Though models of climate change impacts on soil methane fluxes include re-
lationships between water potential and inhibition of methane uptake (e.g., [50–
52]), one such relationship predicts significant uptake at water potential values
≪ −10 MPa [50], an outcome that has not been verified empirically for soils in general,
let alone for arid and semiarid soils. Given the lack of spatial coverage by direct studies
of atmospheric methane uptake, simulation models offer a potentially valuable tool
for developing estimates of global uptake rates. However, to be fully useful, the water
potential uptake rate relationship should be established empirically for multiple soil
types and systems and for wetting and drying cycles to evaluate hysteresis effects.
Carbon monoxide. By regulating hydroxyl radical concentrations to a great de-
gree, CO plays a critical role in tropospheric chemistry [53]. Hydroxyl radical is the
primary oxidant in the troposphere, and as such is responsible for chemical oxida-
tion of atmospheric methane and other organic gases. Since it contributes significantly
to atmospheric CO dynamics, uptake by soils has been the focus of multiple studies,
which have addressed rates, controls, and some aspects of CO microbiology [54, 55].
Although CO transformations in soil have been explored much less than methane

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transformations, several studies have established dependencies on soil water con-

tent [56]. Patterns somewhat analogous to those for methane oxidation have emerged,
with lower rates of CO uptake at high water contents, and increasing uptake rates as
gas transport increases with lower water contents; at relatively low water contents,
uptake ceases due to water stress, and net CO emission can sometimes be observed.
Relationships between water potential and atmospheric CO uptake have received
little attention. Weber and King [57] examined controls of CO uptake by unvegetated
and vegetated volcanic cinders on Hawai’i Island (USA). Though not in an arid or semi-
arid climate, water availability oscillated dramatically on a diurnal basis (between 0
and −60 MPa) for unvegetated cinders due to their very limited water retention capac-
ity, which resulted from low organic contents. In contrast, water potential for nearby
cinders at a vegetated site with high organic concentrations varied very little (0 to
−0.1 MPa). During a moderate drying event (from 0 to −1.7 MPa), atmospheric CO
consumption by intact cores from the unvegetated site decreased 2.7-fold, indicating
a strong dependence on water potential. In laboratory assays, maximum potential CO
oxidation rates decreased by 40 and 60%, respectively, when water potentials were
lowered from 0 to −1.5 MPa, confirming sensitivity observed in the field, but also in-
dicating that CO oxidizing communities at the two sites were not differentially adapted
to water stress. Additional analyses revealed that even after desiccation to −150 MPa
for 63 days, CO oxidation by unvegetated cinders resumed within a few hours of rehy-
dration, which indicated that CO oxidizers were able to survive extended water stress.
Samples from both sites that were exposed to multiple wetting–drying cycles (from 0
to −80 MPa) lost significant activity after the first cycle, but uptake quickly stabilized
and was similar after repeated cycles [57]. This suggested that CO oxidizers at both
sites were relatively resistant and resilient to water stress.
CO oxidizers in arid and semiarid soils must be similarly resistant and resilient to
water stress, however empirical studies that establish this point are lacking. Nonethe-
less, pilot studies of atmospheric CO uptake by playa soils from the Alvord Basin (Ore-
gon, USA) during July 2014 and 2015 (GM King, unpublished) revealed activity at water
potentials between approximately −30 MPa to −50 MPa for sites that had experienced
water potentials between −200 MPa and −300 MPa (consistent with ambient relative
humidity). This clearly documents a substantial capacity for tolerance of extreme wa-
ter stress. The possibility that atmospheric CO can be consumed at water potentials
as low as −50 MPa also distinguishes the capabilities of playa soil CO oxidizers from
those of forest soils and cinders, and suggests that arid and semiarid soils might play
a greater role in the global soil methane sink than some have previously assumed [58].
There are, of course, numerous unanswered questions about CO oxidation at such low
water potentials: What organisms are involved? What mechanisms promote their ac-
tivity? How do they respond to diurnal and seasonal variations in water availability?
How does activity in arid and semiarid soils vary among systems and soil types?
Recent results from saline soils near the Bonneville Salt Flats (Utah, USA) have
provided some insights for a few of these questions. King [59] observed atmospheric

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300
250
Core headspace CO (ppb)
200
150
100
50
Thershold, 60.6 parts per billion
0
0 5 10 15 20 25
Time (h)
Fig. 3.2: Atmospheric CO uptake by triplicate intact cores from saline soils adjacent to the Bonneville
Salt Flats; water potentials were approximately −41 MPa. Data are the means of triplicate assays
with 1 standard error indicated. The dashed line indicates the uptake threshold concentration. From
King [59].
CO uptake by intact cores of saline soils with surface water potentials of about
−40 MPa (󳶳 Fig. 3.2). Depth profiles of CO uptake potential and water potential re-
vealed an inverse relationship, with the highest uptake potential at the lowest water
potential. This suggested that a CO oxidizing community was adapted to water stress
regimes dominated by the presence of salts. Additional analyses revealed CO oxidiz-
ing extreme halophiles (Euryarchaeota) that could consume atmospheric CO while
growing in halite saturated brines [59, 60]. These results further established the po-
tential for CO uptake under conditions of low water potential and extended activity to
saline soils. They also indicated that novel euryarchaeotes might be the active agents
when potentials are poised by solutes versus matric stresses. Obviously, a great deal
remains to be learned.
Other gases. Soils are globally important sources and/or sinks for many other
trace gases, few of which have been evaluated in the context of water potential or
water stress [61, 62]. Disregarding CO2 , a trace gas that should be treated separately
(e.g., [5, 48, 63–65]), perhaps the most thoroughly studied gases other than methane
include nitrous oxide and NO. Both play roles in radiative forcing. Nitrous oxide is well
known for its contribution to stratospheric ozone depletion and for its greenhouse
properties [62]. NO is well known as an important reactant in tropospheric chemistry,
and it contributes to formation of tropospheric ozone, which is a potent greenhouse

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3.5 Conclusions | 41
gas that also causes substantial losses of plant production in agriculture and damage
to human health [62].
Nitrous oxide and NO dynamics depend substantially on soil water regimes. High
water contents and low water potentials favor nitrous oxide production from deni-
trification, since it is oxygen sensitive. However, denitrification is often nitrate lim-
ited and dependent on nitrification, an aerobic process [66]. Nitrification is favored
at lower water contents, but it is also very sensitive to water potentials of less than
about −0.1 MPa [67, 68]. In addition, nitrification (ammonia oxidation in particular)
can form both NO and nitrous oxide. The outcome of these relationships is that ni-
trous oxide and NO emissions tend to be maximized at intermediate water contents,
and presumably intermediate water potentials, though the latter have seldom been
measured during flux studies [69–71].
In arid and semiarid soils, nitrogen gas fluxes often depend on water pulses in the
form of episodic precipitation, which can drastically and rapidly alter microbial com-
munity activity, resulting in short term bursts of metabolism that include nitrification
and denitrification, and elevated, but time varying nitrous oxide and NO emissions
(e.g., [1, 4. 17, 72,73,74]). Though water contents have been routinely measured in pre-
cipitation or wetting studies, water potential has not. Given the possibility of hystere-
sis effects in water potential–water content relationships, and different relationships
for different soil types [75], water potential analyses could promote a greater under-
standing of the mechanisms and variables that control nitrogen gas transformations,
while also facilitating comparisons among systems.
Water content and water potential also play important roles in the dynamics of
nitrogen oxide emission from biological soil crusts (BSC), which can represent signif-
icant NOx sources during wetting events (e.g., [70, 76, 77]). Although BSC behavior is
certainly very sensitive to water potential [78], water content has been most commonly
measured in studies of BSC photosynthesis or other activities (e.g., [2]). Nonetheless,
Potts and Friedman [38] showed that matric and solute stresses elicit different re-
sponses from cyanobacteria, and that responses to a given stress differ among cyano-
bacteria. These findings suggest that responses to water stress by BSC may vary across
space or time as community composition varies. Given the global extent and signif-
icance of BSC, and their sensitivity to climate change, a greater emphasis on water
potential and not just water content is essential for an improved mechanistic under-
standing and for model projections of responses to change.
3.5 Conclusions
Soil water potential is a master variable that to a large degree determines the patterns
and rates of trace gas exchanges between soils and the atmosphere. Soil water poten-
tial varies with volumetric water content, but the relationship is nonlinear and varies
among soil types. In addition, water potential, but not water content, offers a mech-

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anistic understanding of trace gas production and consumption at a cellular level.

For example, decreasing water contents can enhance the physical process of gas ex-
change, but the accompanying decreases in water potential typically inhibit trace gas
production and consumption physiologically. Improved designs for small, relatively
inexpensive systems that can measure in situ water potentials at < −10 MPa, and even
< −100 MPa, offer new possibilities for more extensive water potential monitoring in
semiarid and arid soil systems. More routine application of these technologies will
greatly improve predictive models for trace gas dynamics, especially in the context of
changing climate regimes and increased frequencies of extreme events.
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[77] Abed RM, Lam P, de Beer D, Stief P. High rates of denitrification and nitrous oxide emission in
arid biological soil crusts from the Sultanate of Oman. ISME J 2013, 7:1862–75.
[78] Rajeev L, da Rocha UN, Klitgord N, Luning EG, Fortney J, Axen SD, et al. Dynamic cyanobac-
terial response to hydration and dehydration in a desert biological soil crust. ISME J 2013,
7:2178–91.

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Thulani P. Makhalanyane, Storme Z. de Scally, and Don A. Cowan
4 Microbiology of Antarctic Edaphic
and Lithic Habitats
4.1 Introduction
The Antarctic atmosphere has recently exceeded the nominal barrier of 400 ppm
CO2 [1]. Climate models designed to predict future temperature regimes over the
Antarctic continent are complicated by the interactions between the atmosphere,
ocean, and ice in lower latitude regions [2]. Nevertheless, these models consistently
predict a long term increase in average surface temperatures [3], where southern polar
regions may experience average temperature increases of between 0.3–4.8°C by the
end of the twenty first century [4].
The projected upper range temperature increases are likely to substantially influ-
ence biological community composition and functional processes in a range of non-
marine Antarctic ecosystems, including lakes and ponds [5, 6], permafrost [7, 8], ice
shelves [9, 10], glaciers and meltwater streams [11–13], and soils (and their associated
cryptic and refuge niches) [14–16]. However, feedback of soil ecosystems to climate
change remain unclear, despite the fact that more carbon is stored in these systems
than in plant and atmospheric pools [17, 18]. For instance, carbon stored in Arctic
and Antarctic permafrost alone may significantly intensify climate change through
carbon–climate feedback [19]. We therefore argue, as have others [20–22], that a com-
prehensive understanding of the terrestrial microbiota of the Antarctic continent is
essential in order to appreciate the impacts of projected future climate changes.
The majority of the Antarctic continent is covered by an extensive ice sheet, with
less than 3% of the total land surface comprised of ice free regions [23, 24]. These
regions include mountain ranges, nunataks and coastal arid soils, but are mostly re-
stricted to coastal areas. Ice free soils may only represent a very small fraction of the
total land area of the continent, but they harbor considerable numbers and diversity
of microbial taxa that survive in these extremely challenging environmental condi-
tions [25].
The development of modern metagenomic methods has, as elsewhere, helped to
reveal the true extent of microbial diversity in a diverse range of Antarctic habitats,
including oligotrophic, copiotrophic, psychrophilic, and thermophilic soils. In this
chapter, we review the status of current microbiology research on Antarctic soil com-
munities and the associated cryptic niche habitats (hypoliths, endoliths and epiliths).
We have not focused extensively on permafrost and biological soil crust habitats, both
of which have been the subjects of recent reviews [16, 26].
DOI 10.1515/9783110419047-004

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48 | 4 Microbiology of Antarctic Edaphic and Lithic Habitats
4.2 Classification of Antarctic soils
Studies on Antarctic soils began in the early 1900s and were based on genetic (pedo-
genic processes) and taxonomic (soil properties) classification schemes [27]. Jensen
(1916) was the first to propose that Antarctic soils cannot be classified as “typical” due
to the lack of the organic layer typically associated with soils in other environments
(󳶳 Fig. 4.1a). Loosely arranged unconsolidated Antarctic terrestrial sediments, most of
which lack higher life forms (e.g., plants), also failed to adhere to accepted soil tax-
onomy classification guidelines (󳶳 Fig. 4.1b) [27]. However, studies during the 1960s
led to the recognition of a range of soil forming or pedogenic processes within the ice
free regions of the Antarctic continent [28–31], and the recognition that Antarctic soil
development is influenced by a number of common pedogenic factors including time,
climate and the parent material. The accepted conclusion is that the unconsolidated
gray materials were valid soils [27].
The initial Antarctic soil classification scheme, introduced in 1966, led to the cat-
egorization of six groups [32]. These included the ahumic soils (low organic matter
content), evaporate soils (containing substances left after the evaporation of a body
of water), regosols (weakly developed, loose mineral soils), lithosols (soil containing
mostly weathered rock fragments), protoranker soils (colonized by moss and lichens)
and ornithogenic soils (influenced by birds) [27]. Further soil classifications were in-
troduced by Campbell and Claridge (1977), with the subdivision of the six groups into
zonal, intrazonal and azonal categories. Ahumic soils are considered zonal as they
are strongly influenced by climate and are, therefore, further subdivided on the ba-
sis of moisture availability, soil development and parent material composition [33].
Regosols are considered azonal, whereas evaporate, protoranker and ornithogenic
soils are intrazonal [33].
(a) (b)
Fig. 4.1: (a) Antarctic Dry Valley soils showing the typical pavement structure where mineral soils are
overlain by stones (typically quartz), with the typical organic layer absent. (b) An ice free Antarctic
Dry Valley region showing terrestrial soils that are loosely arranged and lack higher terrestrial life
forms.

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4.2 Classification of Antarctic soils | 49
Early investigations revealed that chemical weathering and ionic migration also
occurred within Antarctic soils, shaping their formation and characteristics [34, 35].
The determination of soil properties, as well as the introduction of the soil classifica-
tion schemes, led to an alternative definition of soil, which was recognized and ap-
proved (Soil Survey Staff, 1999). The new definition described soil as “a natural body
comprised of solids, liquids and gases organized into horizons readily distinguishable
from the initial starting material as a result of addition, losses, transfers and transfor-
mation of energy and matter” [36]. Based on this new definition, Antarctic soils could
be classified according to pedogenic processes affected by factors such as time and
climate, as well as soil properties. Climatic conditions and physiochemical proper-
ties differ markedly across the ice free regions of the Antarctic continent, such as the
McMurdo Dry Valleys (MDVs) and the Antarctic Peninsula, resulting in unique soil
biotopes in each region [27].
4.2.1 McMurdo Dry Valley Soils
The MDVs, occurring within the South Victoria Land zone (roughly from 77° S to 78° S),
represent the largest ice free region of Antarctica [37]. The MDVs are characterized as
cold hyperarid desert regions [38] and are subject to extreme climatic conditions in-
cluding very low temperatures [39, 40], low atmospheric moisture levels and water
availability [41], high levels of UV radiation [37] and strong katabatic winds [42]. The
MDVs have a mean precipitation rate of less than 10 cm yr−1 [43], mostly in the form
of snow that sublimes rather than melts, allowing very little moisture to reach the soil
subsurface [37, 38]. Average annual air temperatures range from −15°C to −30°C [44],
although surface soil temperatures can reach a maximum of around 15°C for short pe-
riods in the summer months [44, 45]. Frequent freeze–thaw cycles occur in MDV soils,
where fluctuations of −15°C to > +20°C have been observed within a single day [39,
40].
The Dry Valleys contain both ephemerally wetted soils from glacial melt exposure
and depauperate mineral soils [46, 47]. The mineral soils within the MDVs are mostly
alkaline, with pH values ranging from 7 to almost 10 in some valley regions [48–51].
MDV soils are often saline and may contain high concentrations of soluble salts such
as calcium, magnesium, sodium, chloride, nitrate and sulfate [37, 41, 50]. Soluble ni-
trogen and phosphorus concentrations vary widely, with ranges of 0–1250 µg g−1 and
0.01–120 µg g−1 , respectively [48]. Organic matter content is typically very low, with a
mean percentage carbon level of less than 0.1% in many soils [52]. The percentage of
sand is markedly higher than the percentage of clay and silt (usually less than 15%
combined) within MDV soils [27].
MDV soils are influenced by both chemical and physical parameters, perhaps
more so than other soils [27]. The predominant pedogenic processes in this region
include salinization and desert pavement formation [53]. These mineral soils contain

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a layer of cemented permafrost, although the depth of this layer may vary [8]. The tax-
onomic classification of MDV soils into two suborders of the order Gelisols, namely
Turbels and Orthels, is based on the characteristics and proximity of permafrost to
the mineral soil surface [27]. Turbels contain ice cemented permafrost within 70 cm
of the soil surface and are generally cryoturbated, indicating that materials from dif-
ferent soil horizons were mixed due to freeze–thaw cycles [27]. Orthels, in contrast,
contain dry permafrost and little cryoturbation [27]. Based on these classifications,
the dominant soil types within the MDVs are Typic Haploturbels, Typic Anhyturbels
and Typic Anhyorthels, where haplo refers to simple and anhy refers to low levels
of moisture or precipitation [54]. The depth of the permafrost layer and the degree
of permafrost melting may be important factors in water availability to surface and
shallow subsurface microbial communities.
4.2.2 Antarctic Peninsula Soils
The Antarctic Peninsula, in contrast to the MDVs, experiences less severe environ-
mental conditions. Nutrient and moisture availability is generally much greater, with
many soils within this region being copiotrophic [24, 55]. The more temperate condi-
tions of the Peninsula support the development of higher life forms, such as plants,
which then sustain other animals, such as birds [56]. The nutrient inputs from these
organisms alter the physiochemical characteristics of the soil, thereby leading to the
alternative, well developed soil biotopes present on the Antarctic Peninsula and sur-
rounding islands [57]. The greater soil taxonomic diversity within the peninsula is due
to the diverse soil characteristics as well as the number of soil forming processes in this
region [58, 59]. The main pedogenic processes occurring within the maritime Antarc-
tic include rubification, carbonation, humification, podsolization, phosphatization
and cryoturbation [53]. The common soil orders within the Antarctic Peninsula, as
classified by soil taxonomy, include the entisols (soils that are extremely underdevel-
oped), inceptisols (soils that are weakly developed) and histosols (soils that contain
organic matter) [54]. Within these, the two suborders, Typic Gelorthents and Typic Ge-
laquents, are the most common, although Turbic Dystrogelepts, Turbic Humigelepts
and Saprists also occur within the peninsula [60].
Ornithogenic soils, which are common on the Antarctic Peninsula, are character-
ized as continuous or historical nutrient inputs from birds, particularly guano (bird
excrement) [27]. As a consequence, ornithogenic soils are highly enriched in nutrients
such as phosphorus, inorganic nitrogen and organic carbon [61]. This external nutri-
ent input also results in high ammonium levels (up to 5% of the dry weight of soil) due
to the conversion of uric acid to ammonia [62]. Ornithogenic soils are typically acidic
(pHs ranging from 3.9 to 5.1) due to the high concentrations of organic acids and am-
monia [61]. Nitrate concentrations are much lower, with ranges of 0–130 µg g−1 pre-
viously reported on Marion Island [63]. Ornithogenic soils also harbor high moisture

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content, with up to 30% water saturation by weight [62]. Despite the high nutrient and
moisture status of these soils, the high percentage of soluble salts limits the growth of
plants, lichens and mosses [62].
Fellfield soils occur mainly within more temperate Antarctic regions, such as the
peninsula and surrounding subantarctic islands, for example Signy and Marion Is-
lands. Fellfield soils are placed in two categories:
(i) moist and nutrient rich, with a high silt content [64],
(ii) dry and nutrient poor, containing high sand content [65].
The first class of fellfield soils contrasts substantially to the desiccated, mostly sandy
soils of the MDVs [66]. For example, fellfield soils on Signy Island may contain as
much as 20% (wt) of soil water content [66]. Maritime Antarctic fellfield soils are prone
to leaching and, therefore, are much less saline than MDV mineral soils [64]. Cryp-
togams, which include mosses and lichens, provide a common but discontinuous veg-
etative distribution within fellfield soils [64]. However, cryptograms are not well an-
chored to the underlying soils and are, therefore, highly unstable habitats. Neverthe-
less, the presence of cryptogams in fellfield soils increases the abundance of key nu-
trients [24]. For example, within coastal Antarctic fellfield soils the soluble phospho-
rus, nitrate and ammonium concentrations range from 4–45 µg g−1 , 1–20 µg g−1 and
15–20 µg g−1 , respectively [34]. Fellfield soils therefore contain substantially higher nu-
trient and organic matter levels than the depauperate MDV mineral soils [34].
The Antarctic continent harbors a wide array of soil biotopes due to its nonho-
mogeneous structure and characteristics, as well as the presence of higher life forms
such as plants and birds in some continental regions. Although the different Antarctic
soil biotopes reflect the diverse nature of the continent, its diversity is also impacted
by the presence of specialized cryptic or refuge niches [67–69].
4.3 Bacterial Diversity of Soils in the MDVs

and Antarctic Peninsula
Studies surveying microbial diversity within Antarctica were originally based on the
determination of bacterial cell densities through ATP, lipid or DNA quantification [70],
the culturing of active microorganisms [71] and microscopic analysis [72]. Microbial
biomass detected within the nutrient rich ornithogenic and fellfield soils of the Penin-
sula are in the range of 107 –1010 prokaryotic cells g−1 [73, 74]. Surprisingly, micro-
bial biomass counts within the MDVs are only slightly lower, with a range of 106 –
108 prokaryotic cells g−1 detected [70]. Microbial cell densities within Antarctic soils
were positively correlated with soil water content and negatively correlated with salin-
ity [75]. Culture dependent studies on Antarctic soils identified the presence of mostly
aerobic heterotrophic microorganisms with limited anaerobic bacteria. The bacterial

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phylotypic diversity was rather limited, consisting mainly of Actinobacteria and Fir-
micutes [76–81].
Culture independent phylogenetic and metagenomic techniques, which are based
on the analysis of total community DNA extracted directly from environmental sam-
ples, avoid any bias induced by the requirement for microbial growth and, therefore,
may provide truer estimates of microbial diversity [81–83]. Phylogenetic fingerprinting
methods, such as terminal restriction fragment length polymorphism (TRFLP), auto-
somal ribosomal intergenic spacer analysis (ARISA) and denaturing gradient gel elec-
trophoresis (DGGE) have provided estimates of the dominant members of microbial
community structures within these regions [81, 84]. However, metagenomic sequenc-
ing, using either large insert libraries, shotgun or amplicon sequencing, identifies the
“entire” microbial community composition within a specific sample [82, 83]. Taken to-
gether, these techniques have resulted in the detection of a much greater microbial di-
versity within Antarctic niches than originally predicted. However, it should be noted
that even with the use of modern phylogenetic marker sequencing technologies, mi-
crobial taxa are typically only identified down to the genus level (in most cases) and
that the true microbial diversity at species and strain levels within Antarctic niches
is, therefore, still largely unclassified [85]. Interestingly, the large number of uncul-
tured microbial representatives commonly detected in surveys of microbial diversity
within Antarctica may also include novel species (particularly members of the family
Actinobacteria) that may have important applications in biotechnology [24].
Overall, studies have shown that bacterial diversity in Antarctic terrestrial en-
vironments is highly heterogeneous, but with some phyla consistently maintained
across many Antarctic soil environments [86–88]. Smith et al. (2006) used DGGE
to analyze the microbial diversity of mineral soils from three different MDV sites.
The samples were dominated by Actinobacteria, Acidobacteria, Cyanobacteria and
Bacteroidetes, and included Verrucomicrobia, Chloroflexi, Alphaproteobacteria and
Betaproteobacteria at lower abundances. Actinobacteria occurred ubiquitously in all
samples, possibly due to the dispersal capabilities and high abundance of this phylum
within soils (󳶳 Tab. 4.1) [79, 89–100]. A similar study on soils within the more north-
ern (and drier) McKelvey Valley identified additional taxa such as Gemmatimonadetes
and the desiccation tolerant Deinococcus–Thermus and Rubrobacter [87]. In contrast,
the more nutrient rich soils of the Peninsula (including both vegetated and fellfield
soils) are dominated by Proteobacteria (including representatives of the Alpha, Beta,
Gamma and Delta Proteobacteria), with lower abundances of Actinobacteria and
Bacteroidetes [39, 76, 88].
Other studies focused on the bacterial diversity of Antarctic soil biotopes have in-
vestigated the factors responsible for driving differences in community structure [50,
76, 101]. Lee et al. (2012) used a combination of pyrosequencing and DGGE to deter-
mine microbial community structure within soils from four geographically isolated
MDVs [50]. Only a limited number of phylotypes were identified at each of the four sites
(typically members of the Actinobacteria and Bacteroidetes), with much of the bacte-

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rial diversity identified being specific to one or more sites. Regional differences were
also observed from other MDV sites: for example, the usually dominant Acidobacteria
were found to occur at very low abundances within the Miers Valley and at Battle-
ship Promontory. These differences were found to be significantly driven by altitude
(specifically, altitude related temperature) and by soil salt content.
Studies on soil biotopes within the Antarctic Peninsula have shown similar com-
munity patterns [88, 101]. Yergeau et al. (2006) assessed the microbial diversity of soils
along an environmental gradient within the Antarctic Peninsula, Falkland Island and
Signy Island using DGGE [101]. This study showed that microbial abundance was sig-
nificantly and positively influenced by vegetation related factors such as nitrogen and
carbon, and soil water content. Microbial community structure was also significantly
correlated with location and latitude, including specific factors such as mean tempera-
ture, nitrate and pH. These communities were influenced by the complex relationship
between vegetation and latitude, where latitude had less of an effect in the presence
of vegetation. Similarly, it has been shown using 16S rRNA gene amplicon sequencing
that bacterial diversity declines with increasing latitude for fellfield but not vegetated
soils within the Antarctic Peninsula [88].
Mineral soil bacterial community structure has also been shown to be markedly
different from ornithogenic soils [58, 76]. Aislabie et al. (2008) used RFLP methods
to analyze microbial diversity in four different mineral soils and one ornithogenic
soil [76]. The mineral soils were found to contain similar bacterial phyla, dominated
by Acidobacteria, Actinobacteria, Firmicutes, Cyanobacteria, Proteobacteria, Bac-
teroidetes and Deinococcus–Thermus. No difference in microbial diversity was found
between soil taxonomic classifications of the mineral soils but was rather found ac-
cording to physiochemical parameters, such as pH. The ornithogenic soils were found
to contain an abundance of endospore formers such as Oceanobacillus, Clostridium
and Sporosarcina, probably reflecting to the high number of Firmicutes found in the
gut and fecal deposits of Antarctic penguins [58].
The microbial diversity within rhizosphere soils of two native vascular plants from
the Antarctic Peninsula was recently assessed [58]. Surprisingly, in contrast to other
peninsula soils [88, 101], the dominant bacterial phylotypes identified were the Firmi-
cutes, Actinobacteria and Proteobacteria, with Acidobacteria, occurring rarely and at
a low abundance. Firmicutes were also identified as the dominant phylum, while Pro-
teobacterial diversity was comparatively low, in contrast to other vegetated and fell-
field peninsula soils [88, 101]. The high abundance of anaerobic spore formers (such
as the Firmicutes) may be due to the higher levels of moisture within the rhizosphere,
or the adaptation of these communities to nutrient (e.g., carbon) limiting conditions
during the winter [58]. This study highlights the importance of local environmental
and physiochemical properties on bacterial community structure within Antarctic soil
biotopes.

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4.4 Cryptic Niches in Antarctic Environments
The ice free regions of the Antarctic continent provide extensive expanses of exposed
rocky substrate. The microbial colonization of rock substrates is a particular feature
of these regions. Lithic associated microhabitats are referred to as lithobiontic niches,
with their communities termed lithobionts [102]. Previous studies have shown that
lithobionts [also referred to as soil rock surface communities (SRSCs)] are ubiquitously
distributed in both hot and cold deserts [103–105]. In the most hyperarid regions,
lithobionts are often the only visible forms of life (󳶳 Fig. 4.2a–d) and are thought to
contribute significantly to the ecology of these regions [51, 68, 105].
The three major lithobiontic niches, which are based largely on the mode of col-
onization of the mineral substrate, are all prevalent in Antarctic ice free regions.
Hypoliths (microbial assemblages found on the ventral surfaces of translucent rocks,
mostly marble and quartz stones) are probably the most studied of the three niches.
Epiliths (organisms populating the surface of stable rock substrata; the subcategory
of chasmoliths inhabits cracks in rocks) occur on various igneous rock surfaces,
while endoliths (communities colonizing the interior of rocks) are usually restricted to
porous sandstones and weathered granitic rocks [67, 68]. In all three niches, micro-
(a) (b)
(c) (d)
Fig. 4.2: Examples of four lithobiont communities/cryptic soil niches, dominated by Cyanobacteria.
(a) A hypolithon with the green biofilm layer, which is distinctive of Cyanobacteria dominated hy-
poliths. (b) An endolithon, which has been exposed, showing microbial colonization within the
green under layer. (c) A cryptoendolith occurring along the crack within the rock, showing visible
Cyanobacteria colonization (thin green line along the crack). (d) Endolithic colonization by Cyano-
bacteria.

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bial colonization is limited by the availability of photosynthetically active radiation

(PAR), which tends to favor the development of photoautotrophs [24, 69].
4.4.1 Hypoliths
Hypolithic microbial communities (hypolithons) have been studied within several of

the MDVs and are present wherever suitable mineral substrates (such as quartz peb-
bles) are available [87, 92, 97, 106]. While these communities are present at most alti-
tudes, colonization of such substrates does not occur at high altitudes (such as Univer-
sity Valley; DA Cowan, personal observation) where little or no seasonal permafrost
melt occurs.
Hypolith communities may be highly similar to, or distinct from, the surround-
ing soil communities, depending on whether they occur in low or high altitude re-
gions, respectively [87, 92]. Microclimate conditions occurring at different altitudes,
such as variations in temperature and moisture availability, which decrease at higher
altitudes, may account for these differences [106]. Where both open soil and hypolithic
communities are found to be similar in composition, it has been suggested that hy-
poliths recruit microbial communities directly from the surrounding soil [107]. Inter-
estingly, hypolithic communities show some variation in gross morphotypic struc-
ture: while most are physically (and visually) dominated by Cyanobacterial biofilms,
a small proportion of quartz hypoliths support moss (Hennendiella spp.) dominated
communities [106].
Hypoliths are thought to be the dominant autotrophic communities in some
Antarctic terrestrial soil environments (i.e., those where suitable translucent mineral
substrates are present in the desert pavement). They are probably the key primary
producers in those Antarctic Dry Valleys that lack high productivity lake systems [97].
A number of recent studies have provided substantial insights into the compo-
sitions and functional diversity of hypolithic microbial communities [108–111]. A
combination of microscopy and culture independent studies showed that Cyanobac-
teria, dominated by filamentous Oscillatorian morphotypes, were prevalent in MDV
hypoliths [38, 112]. Microcoleus, Phormidium and Oscillatoria phylotypes were also
recently identified in MDV hypoliths [111] using 16S rRNA gene pyrosequencing. In
the Vestfold Hills, Oscillatorian Cyanobacterial morphologies were dominant, typi-
cally associated with Lyngbya/Phormidium/Plectonema groups, together with coccoid
cells similar to Chroococcidiopsis [112]. Other dominant bacterial phyla identified in
hypolithic communities include Actinobacteria, α and β Proteobacteria, Plancto-
mycetes, Firmicutes, Acidobacteria and Verrumicrobia [87, 110, 111, 113].
The diversity of fungal phylotypes in Antarctic (particularly Dry Valley) soils is
typically much lower than that of bacteria [114–116], and is dominated by Ascomycetes
lineages [108, 109]. Members of the genera Acremonium, Stromatonectria and Verru-
caria were most commonly identified [108]. Ascomycetes were initially reported as the

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only fungal taxa present in hypolithic communities [97]. However, a recent study re-
ported the presence of Basidiomycetes in hypoliths and soils [117] although they occur
at low abundance. The low moisture availability in desert soils may explain the low
fungal diversity [118].
Other lower eukaryotes, particularly protists, have been identified in Antarctic
Miers Valley hypolithic communities [117]. The relative abundances of Amoebozoa and
Cercozoa phylotypic signals were linked to the sample type (i.e., hypolith type) [106].
Interestingly, the presence of these protists appeared to be unique to the hypolithic en-
vironment, and these organisms have not been identified in nearby open soils. Clearly,
their presence in this habitat has implications for the structure and functioning of food
webs in Antarctic soils and requires further examination.
4.4.2 Epiliths
In Antarctic regions, epilithic colonization is probably the least extensive of all rock
associated habitats. However, studies of the microbial communities present on min-
eral surfaces from other (non-Antarctic) environments [119], particularly rock var-
nishes [120], suggest that Antarctic epilithic microbial communities may be more
widespread and complex than previously considered. A possible role for shallow
subsurface endolithic microbial populations in the genesis of Antarctic rock varnish
layers has been proposed [121].
In Antarctic regions, surface rock communities are limited by the combination of
extremely low temperatures, freeze–thaw cycles, katabatic wind episodes and high
ultraviolet radiation levels [122]. However, in general very little is known regarding
the microbiology of epiliths, in comparison to other lithobionts (endoliths and hy-
poliths) [67]. Early studies suggested that epilithic colonization is primarily associated
with moss and lichen communities [123]. Both lichens and mosses synthesize a wide
range of secondary metabolites, which may act as protectants against some environ-
mental stressors (such as desiccation and UV damage), explaining their dominance in
these niches [124, 125]. Moreover, epiliths are typically found where the rock substrata
have access to moisture [103, 126]. As such, epilithic lichens are widespread across the
coastal regions of Antarctica but decrease toward the interior [126, 127].
Recent studies indicate widespread prevalence of black meristematic fungi in the
coastal northern and southern Victoria Land regions of Antarctica [128]. Black fungi
may be crucial in the hydration or protection of photobionts by dissipating excess sun-
light [129]. In contrast, epiliths from the Princess Elizabeth Land and Mawson Rock re-
gions are dominated by Chroococcidiopsis spp. [130, 131]. Chroococcidiopsis are dom-
inant in both hypolithic and endolithic niches and may support the epilithic “gene-
sis” theory [121]. A comprehensive analysis assessing the dominance of other bacterial
phyla in epiliths may validate this proposal.

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4.4.3 Endoliths
Endolithic microbial communities are defined as those existing inside lithic strata, but
are classified into various subniches [102, 132–134]. Chasmoendoliths (also known as
chasmoliths) are found in interstitial cracks and fissures, while cryptoendoliths are
found in the pores between mineral grains [102, 113, 135, 136]. Like all lithobionts, en-
doliths are dominated by Cyanobacteria [67, 68, 87, 136–138]. Early microscopic anal-
yses of endoliths suggested that the Cyanobacteria co-existed with lichens [91] (mostly
Gloeocapsa, Hormathonema–Gloeocapsa and Chroococcidiopsis communities). More
recent molecular analyses have largely concurred with these studies [126, 139].
Endolithic habitats may impart a degree of species selection; for example, a highly
novel cyanobacterium, a Chloroglea sp., was detected in endoliths from Alexander Is-
land [133], although a range of different Cyanobacterial phylotypes have been identi-
fied in various studies on endolithic microbial communities. Plectonema species have
been identified in 16S rRNA gene clone libraries generated from Dry Valley cryptoen-
dolithic samples [89]. Studies within the Taylor Valley have identified Nostoc, Cyan-
othece, and Chroococcidiopsis species in endoliths [140–142]. Endoliths in McKelvey
Valley have been shown to be dominated by Nostocales and Chroococcidiopsis-like
phylotypes [87]. The drivers for selection of the different cyanobacterial phylotypes in
different endolithic habits are not understood, although community structures have
been shown to vary along a lateral transect within the Miers Valley, which is prob-
ably a result of the different microclimatic conditions of north facing (warmer and
wetter) and south facing (colder and drier) slopes [143]. Although all samples were
dominated by Leptolyngbya, the north facing slopes contained the highest microbial
diversity with a relatively high abundance of Synechococcus-like phylotypes while, in
contrast, the south facing slopes contained Chroococcidiopsis-like phylotypes [143]. It
is tempting to speculate that resistance to extremes, particularly extremes of desicca-
tion, is a factor in the selection of the dominant photoautotroph.
Cyanobacteria in endoliths form consortia with heterotrophic phyla, which vary in
taxonomic composition depending on their location [72]. MDV cryptoendolithic com-
munities, analyzed by microscopy, consisted of heterotrophic assemblages consist-
ing primarily of Alphaproteobacteria (some members of which are potentially capa-
ble of photosynthesis) and Deinococcus–Thermus phylotypes, a group of organisms
with known resistance to desiccation stress. Unlike open soil populations, Actinobac-
teria occur at a comparatively low abundance [89]. In contrast, Acidobacteria and Acti-
nobacteria were the dominant endolithic heterotrophs in samples from the north fac-
ing slopes of the Miers Valley, whereas Deinococcus–Thermus dominated the colder
south facing slopes [143]. Chasmoliths and endoliths from the McKelvey Valley con-
tained high abundances of Bacteroidetes, Actinobacteria, and Gammaproteobacteria,
with Acidobacteria, Deinococcus–Thermus and Alphaproteobacteria at lower abun-
dances [87].

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Hypolith Endolith Open soil
(a) (b) (c)
Cyanobacteria Acidobacteria Cyanobacteria Acidobacteria Cyanobacteria Deinococcus-

Bacteriodetes Proteobacteria Bacteriodetes Proteobacteria Bacteriodetes Thermus
Actinobacteria Verrucomicrobia Actinobacteria Deinococcus- Actinobacteria Chloroflexi
Thermus Acidobacteria Gemmatimonadetes
Proteobacteria Verrucomicrobia
Fig. 4.3: (a) Phylum level classification of bacterial diversity from Antarctic hypolithic communities.
Data is based on the percentage of 16S rRNA gene sequences and tRFLP signatures identified for
each phylum [87, 97], where data was obtained from Pointing et al. (2009) and Khan et al. (2011).
(b) Phylum level classification of bacterial diversity from Antarctic endolithic communities. Data
is based on the percentage of phylum abundances identified from tRFLP fingerprints [87] and was
obtained from Pointing et al. (2009). (c) Phylum level classification of bacterial diversity from Antarc-
tic MDV mineral soils. Data is based on the number of 16S rRNA gene sequences present following
analysis from MDV soil samples [38] as determined by Cary et al. (2010).
In comparison to hypoliths and open soils, endoliths appear to harbor higher

bacterial diversity (󳶳 Fig. 4.3) [87]. In general, all lithobiont microbial communities
are more similar to each other than to those of open soils [87, 113, 143], although sig-
nificant differences in microbial community structures exists between endolithic and
hypolithic communities [87, 142]. Lithobionts are Cyanobacteria dominated, whereas
open soil microbial communities consist of a majority of heterotrophic bacterial phy-
lotypes (󳶳 Fig. 4.3) [87, 143]. Differences between endoliths and hypoliths have been
shown within the McKelvey Valley, where the dominant phylotypes were shown to be
Chroococcidiopsis and Leptolyngbya, respectively [87]. Although both endoliths and
hypoliths are dominated by cyanobacteria, endoliths contain a higher diversity of het-
erotrophic microorganisms relative to hypoliths [87].
Although multiple abiotic factors may drive the differences in bacterial commu-
nity structure in different Antarctic soil biotopes [50, 58, 88], differences are also ob-
served when comparing open soil and cryptic niches [87]. The differences seen be-
tween refuge niches such as hypoliths and endoliths and the open soil are partly due
to the protection that refuge niches provide from environmental stressors [51], and the
increased availability of moisture and nutrients within xeric, nutrient limiting habi-
tats [87]. These factors, and the environmental conditions occurring at different alti-
tudes and latitudes, have been shown to drive the differences in microbial community
structures between cryptic niches and the open soil [87].

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4.6 Viruses in Antarctic Edaphic Ecosystems | 59
4.5 Biogeochemical Cycling in Antarctic Environments
Antarctic soils are generally oligotrophic and have generally low nutrient status
in comparison to those from more temperate biomes [50]. Nonetheless, these soils
demonstrate a high capacity for functional processes [108, 109, 144–146]. For exam-
ple, soils in the Sør Rodane Mountains, located in the Dronning Maud Land (DML)
region of Antarctica, harbored both autotrophic and phototrophic bacteria [146].
Soils in this region contained a high diversity of puf M genes (which encode a sub-
unit of the type 2 photochemical reaction center found in anoxygenic phototrophic
bacteria) and bchL/chlL sequences (genes implicated in bacterio-chlorophyll syn-
thesis). The majority of puf M sequences were related to those previously found in
Proteobacteria, while the origin of the bchL/chlL was linked to Cyanobacteria. An-
other study based on clone libraries of the large subunit of ribulose-1,5-biphosphate
carboxylase/oxygenase (RuBisCO) genes (cbbL, cbbM) and dinitrogenase-reduc-
tase (nif H) genes also identified Cyanobacteria (mostly Nostocales lineages) as the
primary photoautotrophs in DML soils [146]. Surprisingly, these soils lack signa-
tures for alternate energy acquiring processes, such as rhodopsin genes, suggest-
ing that Cyanobacteria in Antarctic regions may have evolved to efficiently cycle C
and N.
In contrast to soils in the DML region, biogeochemical cycling in MDV soils is ap-
parently driven by microbial communities linked to cryptic niche habitats, as indi-
cated by recent GeoChip based analyses [109, 111, 147]. These studies have indicated
that while cryptic niches have higher biomass, with autotrophs being more diverse
in these systems, open soil communities are more diverse in terms of diazotrophic
guilds [147]. In addition, both soils and cryptic niches were highly abundant in func-
tional genes linked to Archaea (mostly Halobacteria). Interestingly, most genes impli-
cated in metabolic pathways linked to carbon transformations in soils were attributed
to fungi [147].
4.6 Viruses in Antarctic Edaphic Ecosystems
Recent metagenomic studies have demonstrated the presence of high levels of viral
diversity in a range of environments [148–151]. In Antarctic environments, the ma-
jority of studies have focused on viruses found in freshwater ponds and lake ecosys-
tems [152–156]. These studies have provided key insights into the influence of environ-
mental extremes on viral diversity, and the role of viruses in biogeochemical cycles.
For instance, a study by Yau and colleagues (2010) highlighted virophages as crucial
regulators of host–virus interactions, a finding that has consequences for carbon flux
dynamics in lake ecosystems [154]. Surprisingly, comparatively little is known of the
role of viruses in Antarctic soil ecosystems. Given the high amount of carbon stored
in these soils, the interactions between viruses and bacteria may be crucial feedback

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mechanisms on carbon cycling. The diversity and ecology of viruses in Antarctic soils
have been reviewed recently [157].
Isolation methods, and analyses using electron microscopy, have shown that
Antarctic soils are dominated by tailed viruses (mostly belonging to the family Myo-
viridae) and spherical viruses (mostly of the family Levividae) [158]. Direct counts
using epifluorescence of extractable and extracellular virus particles suggests that
Antarctic soils may have the highest recorded virus-to-bacteria ratios [159]. A study
by Williamson and colleagues showed that the abundance of viruses increased rel-
ative to bacteria as water and organic content decreased [159]. While the impacts of
climate change and the melting of previously buried ice has not been assessed for
viral communities, this finding does suggests enhanced roles for viral communities
as a consequence of these perturbations.
4.7 Conclusions and Perspectives
In Antarctic microbiology, two of the revelations of the past two decades are that bacte-
rial diversity of Antarctic edaphic niches is much greater than previously thought, and
that specialized cryptic niche communities in cold desert soils may play an important
role in ecosystem processes [24] (󳶳 Tab. 4.1). The presence of substantial populations
of Cyanobacteria, Chloroflexi and Proteobacteria suggests that these organisms con-
tribute to primary productivity in depauperate Antarctica desert soils [87, 106], and
that the presence of diverse heterotrophic organisms (including both bacteria and
fungi) along with viruses [160], macroinvertebrate grazers [161] and predators [162]
suggests the presence of a fully functional trophic hierarchy [24].
However, the global microbial community is familiar with the concept that pre-
dicting organismal or community functions from taxonomic identity is extremely
weak, providing, at best, limited but testable information on functional processes [163].
An assessment of the diversity (and frequency) of key functional genes within a sam-
ple, and relating such data to taxonomic identity, is a step closer to understanding
community function [109], but ultimately should be verified through the determina-
tion of real process rates.
Despite the recent surge of research activity and publications on the structure,
and to some extent, function of Antarctic edaphic microbial communities, we lack
a comprehensive understanding of the finer details: the nature of community inter-
actions in food web structures, the interactive roles of hosts and predators, and the
balance between abiotic and biotic factors in controlling community function. Such
understanding is important for many reasons, not least understanding how changing
climate conditions may impact microbial communities in Antarctic terrestrial environ-
ments.
It is well known that cyanobacteria are essential mediators of biogeochemical pro-
cesses in many habitats, and it is argued that their role in Antarctic soils may be even

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Table 4.1: Microbial diversity from various Antarctic niches.
Domain Identity Niche

Soil Epilith Endolith Hypolith
Archaea Archaea
Crenoarcheota *
Euryarchaeota
Bacteria Acidobacteria
Actinobacteria
Arthrobacter *
Brevibacterium *
Demetria *
Gordonia * *
Janibacter *
Kocuria *
Lapillicoccus *
Leifsonia *
Marisediminicola *
Micromonospora
Mycobacterium *
Nocardiodetes spp. * *
Patulibacter *
Rhodococcus
Unclass. Intrasporangiaceae *
Unclass. Microbacteria *
Uncultured Pseudonocardia * *
Aquificae
Bacteroidetes
Unclass. Flexibacteraceae *
Unclass. Saprospiraceae *
Unclass. Sphingobacteriales *
Cyanobacteria
Acaryochloris spp. *
Anabaena spp. * * *
Chroococcidiopsis spp. * * *
Cylindrospermum spp. *
Gloeocapsa spp. *
Hormathonema spp. *
Leptolyngbya spp. * * *
Lyngbya spp. *
Microcoleus spp. *
Nostoc spp. * * *
Oscillatoria spp. * *
Phormidium spp. * *
Plectonema spp. *
Synechococcus spp. * *

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Table 4.1 (cont.): Microbial diversity from various Antarctic niches.

Chloroflexi * * *
Deinococcus/Thermus
Deinococcus *
Firmicutes
Unclass. Bacillaceae *
Unclass. Clostridiales *
Staphylococcus *
Sporosarcina *
Trichoccus *
Erysipelothrix *
Atopostipes *
Plactomycetes
Proteobacteria * *
Alkanindiges *
Dokdonella *
Lysobacter *
Psychrobacter *
Rhodanobacter *
Lysobacter *
Unclass. Xanthamonadeaceae *
Unclass. Pseudomonadaceae *
Unclass. Rhizobiales *
Verrumicrobia * *
Fungi Ascomycota *
Alternaria *
Antarctomyces *
Cadophora spp. *
Candida spp. *
Cladosporium *
Debaryomyces *
Geomyces spp. *
Leuconeurospora *
Nadsonia *
Nectriaceae *
Onygenales *
Penicillium *
Phaeosphaeria *
Phoma *
Pseudeurotium *
Thelebolus *
Thielavia *
Theobolaceae *

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Table 4.1 (cont.): Microbial diversity from various Antarctic niches.

Basidiomycota
Bensingtonia *
Bulleromyces *
Cryptococcus spp. *
Leucosporidiella *
Rhodotorula *
Zygomycota
Mortierellaceae *
Mortierella *
Data was compiled from several resources [38, 48, 69, 76, 86, 87, 89, 90, 92–100].
more critical in the absence of higher eukaryotic phototrophs. Modern metagenomics

provides a set of tools that, at least, give ready access to information of an organism’s
potential capacity to respond to change. For instance, a cyanobacterial genome se-
quence provides some insight into the organism’s stress response capacity, which can
be verified using ex situ culture dependent stress experiments. However, the technical
challenges associated with the isolation of slow growing cold active cyanobacterial
cultures have posed a considerable challenge [164, 165]. A novel approach to (par-
tially) overcoming this challenge may be to sequence “mixed” cyanobacterial cultures
and implement genome binning approaches, which are increasingly used in the field
of environmental metagenomics [166–168]. Metagenomic binning approaches have
yielded insights on the ecology of other extreme habitats [169] and have the capacity
to contribute a greater understanding of community interactions in Antarctic soils.
A note of caution, relating specifically to issues of “legacy DNA”, must be added.
Conditions in the driest and coldest soils of the Antarctic continent, particularly the
McMurdo Dry Valleys, are not inconsistent with those used routinely by microbiolo-
gists for the preservation of biological material: i.e., freeze drying [170]. It is, therefore,
instructive to contemplate the impacts on metagenomic DNA dependent phylotypic
surveys of these extreme habitats due to the presence of a legacy of dead cells and
even residual genomic DNA [171]. A recent study by Fierer’s group [172] suggests that
legacy (relic) DNA forms a significant proportion of metagenomic DNA extracted from
temperate soils, suggesting that at least some of the published surveys of Antarctic soil
microbial diversity might reflect both historical and extant community compositions.
It is well accepted by the microbial ecology community that RNA-based phyloge-
netic surveys, which assess the “functioning” fraction of the microbial community, are
more reliable and informative. However, the extreme technical difficulties of extract-
ing usable quantities of RNA from low biomass, low activity environments such as the
cold desert soils of Antarctica makes this an objective rather than a current reality.

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Acknowledgment: The authors wish to thank the University of Pretoria, Antarctica

New Zealand, and the South African National Research Foundation (SANAP program)
for supporting field and laboratory research programs.
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Matthew A. Bowker, Burkhard Büdel, Fernando T. Maestre, Anita J.
Antoninka, and David J. Eldridge
5 Bryophyte and Lichen Diversity on Arid Soils:
Determinants and Consequences
5.1 Overview
Arid regions are distinct from most other biomes in that vascular plant cover is discon-
tinuous, allowing light to reach the soil surface. Thus, a niche exists for the photosyn-
thetic organisms that together comprise biological soil crusts (biocrusts). Biocrusts
are a feature of arid regions worldwide, in both hot and cold climates, where they are
a permanent component of successionally mature ecosystems [1]. Biocrusts are a con-
tinuous soil aggregate of the uppermost millimeters of the soil, distinguishable from
other types of soil crust in that they are engineered by biota [2]. They harbor a wide
variety of organisms (archaea, fungi, and bacteria – notably cyanobacteria [3–5]), in
addition to mosses, liverworts and lichens, the subject of this chapter.
5.1.1 Moss, Liverwort, and Lichen Biology
Mosses and liverworts are often grouped as “bryophytes”, although current under-
standing regards these as a polyphyletic group [6]. We will use the term bryophyte
here for convenience to collectively refer to both mosses and liverworts. Both are true
plants, of the kingdom Plantae, which lack the lignified vascular tissue character-
istic of tracheophytes [7]. Without these tissues, their size is constrained, confining
them to the soil surface, often beneath and in between vascular plants. Bryophytes
are older than vascular plants, and are first encountered on land in the middle Or-
dovician period (∼ 470 mya), prior to the formation and breakup of the supercontinent
Pangea [8]. Perhaps not surprisingly, they are found on all continents. Both mosses
and liverworts may have impressive desiccation tolerance strategies to cope with low
water availability, and are commonly found on arid soils as well [9]. Bryophytes do
not reproduce by seed, but instead produce spores as a result of sex, dispersed by the
sporophyte. Although spores can be dispersed long distances, including from conti-
nent to continent [10], many dominant bryophytes of arid regions produce no or few
sporophytes [11, 12], constraining their dispersal, and possibly generating local adap-
tation. Bryophytes are generally capable of vegetative reproduction from any type of
tissue [13], and may or may not also have specialized asexual propagules [14].
Lichens are a symbiosis of at least two primary bionts, a fungal partner (myco-
biont; generally an ascomycete), and a photosynthetic partner (photobiont; a green
DOI 10.1515/9783110419047-005

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74 | 5 Bryophyte and Lichen Diversity on Arid Soils: Determinants and Consequences
alga or cyanobacterium). Though they are often grouped together with bryophytes as
nonvascular “plants,” they do not belong to the kingdom Plantae; rather they are clas-
sified as fungi and named based upon the mycobiont [15]. Despite lacking taxonomic
relatedness, lichens do share some characteristics with bryophytes, including repro-
duction by spores and the lack of specialized water conductance mechanisms, which
is related to small size and desiccation tolerance. Lichens are apparently younger than
bryophytes, dating to ∼ 415 mya (the Devonian period) [16], but have controversially
been proposed to date over 100 mya earlier [17]. Lichens are found on all continents,
are small in stature and confined near to surfaces such as soils. Spores are the product
of sex in the fungal biont and can be a long-distance dispersal agent [18], but to form a
lichen must encounter a compatible photobiont upon germination [19]. Many lichens
also reproduce vegetatively from propagules that contain both mycobiont fungal cells
and photobiont cells, including specialized propagules such as soredia, isidia, or un-
specialized thallus fragments [20].
Bryophytes and lichens are found throughout the world, from arctic tundra, to
temperate tree trunks, to rock outcrops, to arid zone biocrusts. In drylands, at local
scales, they may comprise a substantial amount of the eukaryotic diversity present [21,
22]. The purpose of this chapter is to summarize the dimensions of their biodiversity on
arid soils, outline some of the major determinants of their biodiversity, and summarize
the effects of bryophyte and lichen biodiversity on arid soil function.
5.2 Global Diversity and Characteristic Taxa
5.2.1 Global Species Pool
The diversity distribution of biocrust organisms around the world is incompletely

known. As a first approach to quantify this, we defined seven geographical regions
spanning arid and semiarid areas, as well as polar deserts and initial soils of the
temperate, boreal, and arctic climatic zones, which are characterized by a very sparse
cover of vascular plants (Asia, Africa, North America, including Central America
and Greenland, South America, Antarctica, Europe, and the Pacific region, i.e., Aus-
tralia and New Zealand). In total 323 bryophyte (68 liverworts, 255 mosses) and 553
lichen species (88 cyanolichens, 465 chlorolichens) have been identified explicitly
as biocrust components all globally presently being unevenly distributed amongst
the different geographical regions (continents and subcontinents) partly due to dif-
fering research effort in different parts of the world [5, 23–35] (󳶳 Fig. 5.1). Among all
geographical regions differentiated here, South America is the least known in terms
of biocrust presence and their diversity and taxonomic composition. Only recently
have research activities emerged, investigating biocrusts of several regions of this
understudied continent [36–38].

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Cyanolichens Chlorolichens Liverworts Mosses

300
7,960,000 km2
250
33,579,000 km2
200
Species number
24,709,000 km2
30,521,532 km2
10,180,000 km2
14,000,000 km2
150
17,840,000 km2
100
50
0
ia
pe
Am orth
er h
a
c
a
An ica
tic
fi
ric
Am t
ic
As
ro
ci
er
So
rc
Af
Pa
N
Eu
ta
Geographical region, decreasing size
Fig. 5.1: Species numbers per geographical region (N-America includes Central America and Green-
land; Pacific includes Australia and New Zealand); regions are arranged according to size.
Biocrust lichens are well known for all regions except South America, while biocrust
bryophytes are well known only for Europe, North America, and the Pacific region
(󳶳 Fig. 5.1). The highest species numbers found so far have been in Europe, followed
by North America and Asia. In Europe and North America there are many scientists
working on this topic, while in Asia this is true for Russia and China only.
5.2.2 Global Characteristic Taxa and β Diversity
No bryophyte or lichen species occurs in biocrusts in all of the seven geographical re-
gions defined here. However, 20 species (17 lichens, 3 mosses) occurred in at least four
out of the seven geographical regions (󳶳 Tab. 5.1). These can be thought of as the more
cosmopolitan, characteristic taxa. Two lichens, but no bryophytes, are documented in
biocrusts of all regions except Antarctica.
While it is notable that a few species are so widely distributed, the wider pat-
tern suggests that most species are confined to only one or a few regions. With 287
bryophyte (60 liverworts, 227 mosses) and 411 lichen species (64 cyanolichens, 347
chlorolichens), the bulk of species from biocrusts is restricted to only one of the seven
geographical regions (󳶳 Fig. 5.2). In two of the seven regions we found 26 bryophytes
and 95 lichens, whereas in three of seven regions the number declined to 7 bryophytes
and 30 lichens. For further details, see 󳶳 Fig. 5.2 and 󳶳 Tab. 5.1. While it is true that a

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Table 5.1: List of the 56 lichen and bryophyte species recorded from at least three out of the seven
geographical regions defined here [23–35]. Species are arranged first according to their frequency
and second alphabetically.
N-America1
S-America
Antarctica
Pacific2
Europe
Africa
Asia
Species
Lichens
Heppia despreauxii (Mont.) Tuck. × × × × × ×
Placidium squamulosum (Ach.) Breuss × × × × × ×
Collema tenax (Sw.) Ach. × × × × ×
Diploschistes diacapsis (Ach.) Lumbsch × × × × ×
Diploschistes muscorum (Scop.) R. Sant. × × × × ×
Endocarpon pusillum Hedw. × × × × ×
Peltula patellata (Bagl.) Swinsc. & Krog × × × × ×
Placidium lacinulatum (Ach.) Breuss × × × × ×
Placidium pilosellum (Breuss) Breuss × × × × ×
Psora decipiens (Hedw.) Hoffm. × × × × ×
Toninia sedifolia (Scop.) Timdal × × × × ×
Cladonia fimbriata (L.) Fr. × × × ×
Cladonia furcata (Huds.) Schrad. × × × ×
Collema coccophorum Tuck. × × × ×
Fulgensia fulgens (Sw.) Elenkin × × × ×
Heppia adglutinata (Kremp.) A. Massal. × × × ×
Heppia lutosa (Ach.) Nyl. × × × ×
Acarospora nodulosa (Dufour) Hue × × ×
Buellia epigaea (Hoffm.) Tuck. × × ×
Buellia punctata (Hoffm.) A. Massal. × × ×
Candelariella vitellina (Hoffm.) Müll. Arg. × × ×
Cetraria islandica (L.) Ach. × × ×
Cladonia cervicornis (Ach.) Flot. × × ×
Cladonia foliacea (Huds.) Willd. (including C. convoluta) × × ×
Cladonia pocillum (Ach.) O. J. Rich. × × ×
Cladonia pyxidata (L.) Hoffm. × × ×
Cladonia verticillata (Hoffm.) Schaer. × × ×
Collema crispum var. crispum (Huds.) Weber ex F. H. Wigg. × × ×
Fulgensia bracteata ssp. bracteata (Hoffm.) Räsänen × × ×
Fulgensia desertorum f. macrospora Llimona × × ×
Fulgensia subbracteata (Nyl.) Poelt × × ×
Gypsoplaca macrophylla (Zahlbr.) Timdal × × ×
Heppia solorinoides (Nyl.) Nyl. × × ×
Peccania fontqueriana P. P. Moreno & Egea × × ×
Peltula obscurans (Nyl.) Gyelnik × × ×
Peltula radicata Nyl. × × ×
Phaeorrhiza nimbosa (Fr.) H. Mayrhofer & Poelt × × ×
Placynthium nigrum (Huds.) Grey × × ×
Psora crenata (Taylor) Reinke × × ×

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Table 5.1 (cont.): List of the 56 lichen and bryophyte species recorded from at least three out of the
seven geographical regions defined here [23–35]. Species are arranged first according to their fre-
quency and second alphabetically.
N-America1
S-America
Antarctica
Pacific2
Europe
Africa
Asia
Species
Psora lurida Ach. × × ×

Rinodina terrestris Tomin × × ×
Squamarina cartilaginea (With.) P. James × × ×
Squamarina lentigera (Weber) Poelt × × ×
Toninia aromatica (Turner) A.Massal × × ×
Toninia lutosa (Ach.) Timdal × × ×
Toninia ruginosa (Tuck.) Herre × × ×
Bryophytes
Bryum argenteum Hedw. × × × × ×
Bryum caespiticium Hedw. × × × ×
Ceratodon purpureus (Hedw.) Brid. × × × ×
Weissia controversa Hedw. × × ×
Crossidium crassinerve (De Not.) Jur. × × ×
Didymodon cf. rigidulus Hedw. × × ×
Riccia lamellosa Raddi × × ×
Riccia sorocarpa Bisch. × × ×
Syntrichia ruralis (Hedw.) F.Weber & D.Mohr × × ×
Trichostomum brachydontium Bruch ex F. Muell. × × ×
1 including Central America and Greenland.
2 Australia, New Zealand
400 Cyanolichens Liverworts

250
Chlorolichens Mosses
Species number
Species number
300 200
200 150
100
100
50
0 0
6 gr. ons
l r ns
6 gr. ons
eg s
4 gr. ons
5 gr. ons
re s
4 gr. ons
5 gr. ons
re s
ns
ns
3 gr. ion
3 gr. ion
Al ion
n
n
o
io
og gio
io
og gio
eg
eg
gi
gi
gi
gi
gi
gi
gi
eg
g
ge re
ge re
ge re
ge re
ge re
ge re
ge re
ge re
ge . r
ge . r
lr
2 ogr
2 ogr
r.
r.
Al
o
o
o
o
e
e
1g
1g
(a) (b)
Fig. 5.2: Frequency of lichen (a) and bryophyte (b) species across seven geographic regions.

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lack of detection does not mean that a taxon is truly absent from a region, these data
suggest a considerable amount of species turnover from continent to continent. More
sampling effort is necessary to fill in current distribution gaps.
5.3 Determinants of Moss, Liverwort, and Lichen Diversity

on Arid Soils
5.3.1 Geographic Isolation and Biogeography
At large scales, dispersal limitations likely shape the bryophyte and lichen β diversity
of major landmasses, the genetic diversity and distinctiveness, and α diversity of arid
soil bryophyte and lichen communities. Bryophytes and lichens can disperse spores
over long distances, e.g., from continent to continent [10, 18]. However, many dryland
species may rely more upon vegetative propagules, e.g., tissue fragments, which are
much more dispersal limited due to their larger size, possibly allowing for geographic
isolation.
At the global scale, we might expect that the mode of reproduction dictates the
distribution of species, and we can hypothesize that this mechanism arranges arid
soil bryophytes and lichens into groups based on dispersal limitation. The less dis-
persal limited group, which might abundantly produce spores, and in the case of
lichens, also associate with a widely distributed photobiont, would be expected to
be widespread or possibly cosmopolitan. An exemplar might be the moss Ceratodon
purpureus, which is a prolific sporophyte producer, present on all continents (though
not always in arid soil biocrusts) [10]. For lichens, long distance dispersal of spores
is not sufficient in and of itself, because the spores must encounter a compatible
photobiont. The lichen Psora decipiens is a broadly distributed lichen, which may
reduce this problem by associating with multiple photobionts [39]. There are limits
to spore distribution, therefore, even among cosmopolitan species. Genetic distance
and floristic dissimilarity among populations may increase as connectivity via wind
or geographic proximity decreases [18].
Other species are dispersal limited, due to a lack of successful reproduction via
spores, and may either be widespread (found on several continents) or restricted in
range (found on one or a few continents). Widespread dispersal limited species may
be hypothesized to be relatively old, predating the breakup of the supercontinents.
Such species might exhibit a strong degree of interspecific variation, and local adap-
tation, for example chemical races of lichens (Culberson 1986). Widespread dispersal
limited species could be either common or rare. Common ones might include species
found in arid regions of multiple land masses, but only rarely reproduce sexually. The
lichen Gypsoplaca macrophylla may be an example of a rare species that falls within
this group. Currently it has a wide distribution on three continents, including arid
gypsiferous soils of southwestern US [22], in addition to Greenland, the Alps, and a

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5.3 Determinants of Moss, Liverwort, and Lichen Diversity on Arid Soils | 79
few localities in Asia [40]. It is always a rare community member. Perhaps this strange
distribution arose through extinction of a formerly widespread taxon.
Geographically restricted and dispersal limited species might be found only
within a single major land mass, or a portion of one. These endemic community
components might be hypothesized to represent evolutionarily younger species that
arose after the breakup of the continents and have remained isolated due to long-
distance dispersal limitation. The lichen genus Xanthoparmelia originated after the
breakup of the continents [41] and has multiple species that have adopted a reliance
on dispersal of vagrant, unattached thalli as propagules [42]. This reliance on local
dispersal may explain the large degree of local endemism in this genus [42].
5.3.2 Climatic Gradients and Climate Change
Climate is a major global driver of biocrust α and β diversity and composition in dry-
lands. Rainfall, potential evapotranspiration and temperature all combine to deter-
mine the type of biocrust communities that can be supported. These effects vary with
spatial scale, from continental and landscape scales, down to the scale of meters or
less.
Simultaneously dry and very cold environments may be at the physiological lim-
its for some species to survive. Water may be scarce due to rarity of precipitation, or
infrequency of thawing temperatures. For example, there are no liverworts or cyano-
lichens known from Antarctica (󳶳 Fig. 5.1). We may hypothesize that chlorolichens and
mosses are more able to survive given the rarity of liquid water or are able to activate
photosynthesis with less water.
Within less extreme climates in the temperate and tropical regions, biocrust lichen
and moss richness is correlated with soil moisture across large precipitation gradi-
ents [43]. Cooler habitats appear to support a large diversity and biomass of lichen
taxa [44], possibly because the balance of photosynthesis and respiration between
the symbiotic partners maximizes the opportunity to form complex thallus structures.
Similarly, higher rainfall has been correlated with increasing richness and changes
in biocrust composition [45]. Rainfall seasonality can also have marked effects on
biocrust composition [27, 46]. In Australia, for example, biocrust lichens are restricted
to winter rainfall dominant areas, where they are able to avoid hydration of the thallus
during extremely hot weather [47]. Despite the preference for winter rainfall, very cold
temperatures are not necessarily preferred. Areas in the northwestern United States (a
winter rainfall region) with warmer winter temperatures have been shown to be more
conducive to crust development than areas with colder winters [48]. Biocrust species
richness and composition are also known to vary with altitude, which is usually a sur-
rogate for increasing precipitation and decreasing temperature [26]. Castillo-Monroy
et al. [37] showed that biocrust species richness in an Ecuadorian dryland increased
with increasing elevation, with clear differences in composition along the elevational

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gradient. These altitudinal differences can be attributed to the redistribution of runoff

and differences in soil texture, which largely drive soil moisture availability, and con-
sequently, competition from vascular plants and available niches for biocrust taxa.
Changes in soil moisture availability at more local scales can also alter biocrust
cover and composition. For example, the two major patch types in drylands (resource
shedding water runoff zones and resource accumulating water runon zones) that re-
sult from the redistribution of water, support different taxa at small scales. Lichens
and cyanobacteria typically dominate resource shedding areas, whereas microsites
where resources accumulate are often dominated by bryophytes [49, 50]. The mech-
anism behind this distribution may relate to the need for bryophytes to access free
water to reproduce but is also related to competition with vascular plants (e.g., 51,52].
At the microsite scale, the distribution of biocrust taxa is strongly dependent on soil
moisture [22, 53–55] and the availability of suitable niches for establishment. These
microsites are often areas that receive slightly more moisture, are cooler and sheltered
from temperature extremes [56, 57].
Biocrusts lichens and mosses have been predicted to mediate any substantial ef-
fects on ecosystem functioning due to climate change [58–60]. However, there are also
likely to be substantial changes in biocrust composition and richness resulting from
a changing climate. For example, Ferrenberg et al. [61] showed that an increase in
small summer rainfall events changed biocrust composition from moss dominated
(Syntrichia caninervis) to cyanobacteria dominated (Microcoleus vaginatus) commu-
nities [61], and Maestre et al. (2015) reported up to a 45% decline in lichen dominated
biocrusts with warming after 4 years [62].
5.3.3 Calcicole–Calcifuge Dichotomy and Soil pH Gradients
Biocrust β diversity, particularly that of lichens, is known to be strongly influenced

by soil pH, which in turn is strongly influenced by the concentrations of calcium (Ca)
carbonate and other carbonates in the soil [27, 28, 48, 63–65]. The relationship be-
tween lichen taxa and soil pH is so pronounced that lichens have been classified into
two broad functional groups according to their response to soil pH. Calciphiles, which
include the majority of soil lichens in drylands, are strongly associated with soils of
high pH. Conversely, calcifuges have a low tolerance to high pH soils [66] and appear to
be more common in mesic soils. This dichotomy recurs in many locations around the
world, dictating both biocrust abundance and community composition. In drylands
in the western USA and Ecuadorian dry mountain shrublands, biocrusts reach their
greatest development on neutral to acidic soils [37, 48]. In other dryland areas of the
USA, Spain, Australia, and Israel, biocrust lichens and bryophytes are more diverse
and occupy a greater cover in areas of high pH (e.g., [17, 47, 63, 67, 68]). Lichens inhab-
iting Ca rich soils are thought to have greater concentrations of Ca oxalate on the outer
surface of the thallus, reducing the concentration of Ca in the immediate area where

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5.3 Determinants of Moss, Liverwort, and Lichen Diversity on Arid Soils | 81
the lichen attaches [69]. Magnesium, manganese, and other nutrients have also been
shown to be highly correlated with crust cover and composition [28, 43, 56, 56, 66, 70],
but the exact mechanisms behind their effects on biocrust taxa are still not fully un-
derstood and may relate to pH or carbonate gradients.
5.3.4 The Special Case of Gypsiferous Soils
Occasionally, dryland soils have high levels of Ca in the form of gypsum [71]. Gyp-
sum content is one of the edaphic factors most influential on taxonomic richness and
species turnover of soil mosses, liverworts, and lichens in a given region [72–74]. For
example, on the Colorado Plateau (USA), out of eight different soil types, gypsifer-
ous soils had the greatest species richness (∼ 21 species per site), supported the sec-
ond greatest species evenness, and supported eight indicator species out of a total of
19 [22]. In this case study, the gypsiferous soils had a disproportionately large effect
on diversity at both local scales and within the entire study area. Higher taxonomic
and functional richness of both mosses and lichens is also reported in Europe and
Australia on gypsum soils [28, 72, 73, 75].
Gypsiferous arid soils of the Northern hemisphere and Australia often appear to
be dominated by well distributed gypsophile lichen taxa such as Diploschistes spp.,
Psora decipiens, Fulgensia spp., Acarospora nodulosa, and Squamarina lentigera,
among others [22, 28, 72, 76–78]. Where gypsum soils are rare in the landscape, these
species may be rare or narrowly distributed within a region, despite local abundance
and wide distribution globally. Gypsiferous soils also appear to harbor a larger num-
ber of endemics compared to other soils, a phenomenon also observed in vascular
plants [79]. Perhaps this is because the specific edaphic preferences of the lichens,
coupled with dispersal limitations, lead to narrow distributions. One example is
Lecanora gypsicola, described in 1998 and known only from sporadically occurring
gypsiferous soils of the western United States [80].
Dominant mosses of gypsiferous arid soils appear to differ more than lichens from
region to region and may be generalist species rather than gypsum specialists [22, 78].
Widespread, but usually subdominant gypsophile species include Aloina bifrons, and
a few Crossidium spp. [22, 73]. There are clear gypsum endemic mosses, however, in-
cluding the North American endemic Didymodon nevadensis, which was only discov-
ered in the 1990s [81]. Guerra et al. [73] list seven rare gypsophile species, known only
from the Iberian Peninsula, including a rare gypsum tolerating liverwort, Riccia crus-
tata.
Why are gypsum soils such a distinct habitat? Bogdanović et al. [82] showed that
two moss species with no reported preference for gypsum were able to tolerate its pres-
ence. Thus, the ability to grow on gypsum might be widespread in mosses, and this
might contribute to high α diversity, but would not explain high species turnover from
gypsiferous habitats to nongypsiferous habitats nearby. Rather, true gypsophiles must

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either derive a benefit from growing in the habitat type, or resist its specific stresses
better than most species. Gypsum contains Ca and sulfur, both essential nutrients. The
fact that some gypsophiles also are found on soil rich in Ca carbonate might suggest
a high demand for, or tolerance of Ca. A recent study of vascular plant endemism de-
tected accumulations of Ca oxalate in plant tissues of gypsophiles, and hypothesized
that this is a mechanism for coping with excess Ca [83]. This may be an intriguing clue,
since lichen pruina are composed of Ca oxalates and most lichens preferentially grow-
ing on gypsum abundantly produce pruina. Nonetheless, soils rich in Ca carbonate but
not gypsum often have different floras [22, 84], suggesting that Ca alone is an unlikely
explanation of unique lichen and bryophyte assemblages on gypsiferous soils.
5.4 Consequences of Moss, Liverwort, and Lichen Diversity

on Arid Soils
5.4.1 Contribution of Biocrust Lichens and Bryophytes to Arid Ecosystem Function
Biocrust mosses and lichens play major roles in nutrient cycling, and in building and
maintaining soil fertility. Lichen and bryophyte dominated biocrusts are an important
part of the global carbon (C) budget, taking up from 1 to 37 g C m−2 yr−1 in arid lands,
depending on the species composition, amount of cover and water availability [85–
87]. This is a substantial contribution to productivity in arid lands, accounting for as
much as 3.7–13.9% of net primary productivity [88]. Likewise, lichens and bryophytes
play key roles in regulating terrestrial nitrogen (N) cycling. N is commonly the most
limiting nutrient in terrestrial ecosystems [89]. Many lichens house N fixing cyanobac-
terial symbionts within their thallus, and, likewise, biocrust mosses, are known to
host N fixing symbionts on their leaves [90, 91]. Enzyme activity is high in lichen and
moss dominated biocrusts, and is dependent on species composition, which is impor-
tant for N, C and phosphorous cycling [92]. Microbial N fixation and N transformation
activity is known to be stimulated within biocrusts [93], and these combined activities
can account for the majority of available N input to arid systems [88, 94]. They also
capture dust, which helps to promote ecosystem productivity by addition of both soil
and nutrients to the ecosystem [95].
Because mosses and lichens bind the soil together with filamentous structures
such as hyphae, rhizines, and rhizoids, they aggregate soil, reducing soil loss due to
wind and water erosion [96, 97]. This is true even during inactivity because lichens
and bryophytes of biocrusts have remarkable desiccation tolerance [98, 99], and the
physical structure of the biocrust persists.
Due to the physical structure of the biocrusts, mosses and lichens have complex
effects on soil hydrology, which are largely dependent on biocrust composition, rain-
fall intensity, ambient temperature, and soil texture [50, 100, 101]. Lichens can have
mixed effects, either generating runoff or promoting infiltration, depending upon the

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5.4 Consequences of Moss, Liverwort, and Lichen Diversity on Arid Soils | 83
surface connectivity of the lichen thallus, whereas mosses have greater surface rough-
ness and high water absorbing capacity, at 100−1000× their dry mass, enhancing
infiltration [101, 102]. Sinuous microtopography of well developed lichen and moss
biocrusts can slow down the movement of water, enhancing infiltration compared to
smoother cyanobacterial biocrusts, but many lichen biocrusts can generate runoff at
high rainfall events [97, 103, 104]. Well developed crusts also influence water retention
by reducing evaporation [104, 105]. All of these factors influence water availability for
vascular plants and the soil food web.
Finally, biocrusts composed of bryophytes and lichens support a vibrant soil
food web in the top millimeters of soil because they leak much of the C and N that
they fix back into the soil [106]. Recent work has demonstrated that microbes spe-
cialize on specific biocrust excretions, allowing the C and N to be recycled and
re-assimilated [107]. Lichens and bryophytes produce a number of secondary com-
pounds that provide protection from harmful ultraviolet radiation [108–110]. Surface
bryophyte and lichen community resilience is critical for protecting biocrust commu-
nity members that lack UV protection (e.g., light cyanobacteria).
5.4.2 Biodiversity–Ecosystem Functioning Relationship
Understanding the links between biodiversity and those processes that determine
the functioning of ecosystems (biodiversity–ecosystem functioning relationship) has
been a major research topic in community and ecosystem ecology over the last two
decades [111–114]. During this period, several hundred biodiversity–ecosystem func-
tioning relationship studies have been conducted with a wide variety of organisms,
such as vascular plants, algae and soil, fauna, and ecosystem processes, including
primary productivity, nutrient cycling, or water quality (see [112, 113] for reviews).
Biocrusts have not been an exception to this, and multiple observational and exper-
imental studies have explored how changes in the diversity of biocrust constituents,
such as lichens and mosses, affect ecosystem functioning [115, 116, 118, 121, 126–128].
Indeed, some attributes of biocrusts, such as small size and the ease of transplant
and/or culturing their constituents, make them particularly suitable for biodiversity
and ecosystem functioning research, and their use by researchers on this topic is
being encouraged [132].
Most studies on the biodiversity–ecosystem function relationship to date have
focused on particular ecosystem processes, such as productivity, and on species rich-
ness as a focal aspect of biodiversity [111, 113]. These studies provide ample evidence
of positive richness function relationships in nature. As an example, Cardinale et
al. [113] found that the relationship between producer diversity and biomass was best
described by some form of a positive but decelerating curve in 79% (of 272) studies,
while linear relationships were found in only 13% of cases. Similar results were found
when looking at functions such as nutrient uptake (89% positive but decelerating

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curve, 9% linear relationship, 47 studies) or decomposition (61% positive but deceler-

ating curve, 19% linear relationship, 36 studies; 113). Biocrusts have proven to be no
exception to the positive relationship between biodiversity and ecosystem functioning
reported with other organisms; however, they more commonly exhibit approximately
linear relationships between the number of macroscopic species (bryophytes and
lichens) and various indicators of nutrient cycling, hydrological, and soil develop-
ment and retention functions. Positive richness function relationships are supported
in multiple observational field studies conducted in drylands [115, 116], although
sometimes negative effects or no effects are reported [117].
Moisture availability also plays a role in determining biodiversity–ecosystem
functioning relationships. Mulder et al. (2001) experimentally tested the relation-
ships between species diversity and productivity using mosses and liverworts [118].
They found that biomass increased with species richness, but only when communities
were subject to experimental drought. Rixen and Mulder [119] exposed arctic tundra
moss communities of varying richness to two drought and density levels, and found
that productivity was increased in the species rich communities, particularly in the
low density plots, but only when plots were watered regularly. They also found that
moisture retention improved at high species richness levels, as a result of the positive
effects that biomass had on moisture conditions.
Other studies have explored how the diversity of microbes associated with bio-
crusts affect ecosystem functioning. For example, Hu et al. (2002) observed that ar-
tificial biocrusts composed of multiple cyanobacterial species aggregated soil more
strongly than biocrusts formed by single species [120]. It would be reasonable to be-
lieve that some apparent effects of bryophyte and lichen diversity are actually medi-
ated by community properties of associated bacteria and fungi. Nonetheless, Castillo-
Monroy et al. [121] found that lichen richness, rather than bacterial richness, was di-
rectly related to multiple ecosystem functions related to nutrient cycling. More studies
on this topic will help partition the relative influence of bryophyte lichen and micro-
bial diversity on ecosystem functions.
5.4.3 Effects of Species Richness, Turnover, and Evenness on Ecosystem Functions
Despite biodiversity encompassing multiple components, most studies on the biodi-

versity–ecosystem functioning relationship conducted to date have targeted species
richness, or α diversity, as the main biodiversity descriptor [113]. However, there is
growing evidence suggesting that other components of biodiversity, such as species
evenness, β diversity (species turnover), trait diversity, functional group diversity,
phylogenetic diversity, and within species genetic diversity, have the potential to in-
fluence ecosystem processes [122–125]. Only some of these elements of biodiversity
have been investigated using biocrusts. In 󳶳 Tab. 5.2, we compile results from the
literature on the frequency of effects of biocrust lichen and bryophyte α diversity,

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Table 5.2: Percentage of cases in which α diversity, evenness, and β diversity of biocrust bryophytes
and/or lichens have a detectable effect on an indicator of ecosystem function. In the case of α diver-
sity and evenness, the proportion of these effects that are positive is also reported. We report main
effects only; in some cases interactive effects are detected. White filled cells indicate no data. Black
filled cells indicate that an effect on multifunctionality was reported. Mean reflects the average pro-
portion of ecosystem function indicators affected per dataset. Frequency reflects the percentage of
datasets in which there are > 0 effects on ecosystem function indicators detected.
β diversity
α diversity
% positive
% positive
evenness
Dataset Function indicators
Single site, Alicante, 0 80 25 bulk density, respiration,
Spain [117] organic C, total N, soil
aggregate stability
Single site, Cuenca, 80 25 0 bulk density, respiration,

Spain [117] organic C, total N, soil
aggregate stability
Many sites, Utah, USA [115] 100 100 100 0 magnetic susceptibility
Many sites, Arizona, 50 100 50 100 surface roughness, soil

USA [115] aggregate stability
Many sites, Utah, USA [115] 100 50 0 magnetic susceptibility,

surface roughness
Single site, Communidad 33 100 0 100 phosphatase,

de Madrid, Spain [36, 115, β-glucosidase, urease
133]
Single site, Communidad de 0 100 Steady state infiltration
Madrid, Spain [50]
Many sites, Central & 83.3 100 16.7 100 66.7a “C cycling”, respiration,
Southern Spain (gypsum phosphatase, total N,
soils) [116, 128] urease, multifunctionality
Many sites, Central & South- 42.9 66.7 14.3 100 33.3a organic C, β-glucosidase,
ern Spain (calcareous respiration, phosphatase,
soils) [116, 128] total N, urease,
multifunctionality
Constructed biocrusts com- 20 0 10 ammonium, nitrate,

position experiment (sur- organic C, total N,
face) [126, 134] β-glucosidase,
phosphatase, urease,
N-fixation,
multifunctionality,
microbial catabolic profile
a Bowker et al. 2013 [116] did not address β diversity. Bowker et al. 2011 [128] analyzed β diversity
effects on individual functions but not on multifunctionality.

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Table 5.2 (cont.): Percentage of cases in which α diversity, evenness, and β diversity of biocrust
bryophytes and/or lichens have a detectable effect on an indicator of ecosystem function. In the
case of α diversity and evenness, the proportion of these effects that are positive is also reported.
We report main effects only; in some cases interactive effects are detected. White filled cells in-
dicate no data. Black filled cells indicate that an effect on multifunctionality was reported. Mean
reflects the average proportion of ecosystem function indicators affected per dataset. Frequency
reflects the percentage of datasets in which there are > 0 effects on ecosystem function indicators
detected.
β diversity
α diversity
% positive
% positive
evenness
Dataset Function indicators
Constructed biocrusts com- 80 80 60 organic C, total N,
position experiment (sub- β-glucosidase,
surface) [126] phosphatase,
multifunctionality
Constructed biocrusts 10 100 0 20 ammonium, nitrate,

evenness experiment (sur- organic C, total N,
face) [126, 134] β-glucosidase,
phosphatase, urease,
N-fixation,
multifunctionality,
microbial catabolic profile
Constructed biocrusts even- 60 33.3 0 40 organic C, total N,

ness experiment (subsur- β-glucosidase,
face) [126] phosphatase,
multifunctionality
Single site, Baja California, 100 CO2 gas exchange

Mexico [129]
Single site, Communidad de 100 organic C, hexoses,
Madrid, Spain [92] phenols, respiration, total
N, microbial biomass N,
amino acids, proteins,
dissolved inorganic p,
phosphatase
Mean 50.7 68.6 26.1 65.0 66.3

Frequency 84.6 90.9 50.0 80.0 100.0
evenness, or β diversity on ecosystem functioning. Our rules for inclusion required

an explicit manipulation or measurement of one of these elements of biodiversity,
a focus on biocrusts of dryland soils, and a measurement of at least one indicator
of ecosystem function. We excluded measurements of activity or physiology of iso-
lated biocrust organisms, focusing instead on the functions of biocrust communities.
Finally, in our consideration of β diversity, we included comparisons of biocrusts

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dominated by a particular species, but excluded comparisons of biocrust types and

effects of turnover among morphological groups, because species compositions were
not explicitly measured.
Overall, available evidence suggests that, as in several other communities, species
richness commonly exerts positive effects on ecosystem functioning in biocrusts. In
85% of cases meeting our inclusion criteria, at least one α diversity relationship was
detected with ecosystem function (󳶳 Tab. 5.2). On average, about half of the ecosystem
function indicators were affected by α diversity, over two thirds of which were positive.
The magnitude and sign of these effects depend on the characteristics of the biocrust
community (abundance, spatial pattern), the ecosystem function considered, envi-
ronmental conditions, and the interactions among these factors. Species richness has
been found to be a better indicator of ecosystem functioning than the richness of a pri-
ori functional groups, perhaps because our limited knowledge of the functional traits
of biocrust constituents does not properly group species according to their impacts
on ecosystem functioning [51, 90]. Alternatively, it may mean that biocrust moss and
lichen species tend to have unique suites of functional traits [84, 115], and perhaps a
trait diversity index would prove to be even more informative than species richness.
Biocrust evenness is less commonly related to ecosystem functioning; at least one
evenness–function relationship occurs in about half of cases, and about a quarter of
functional indicators were influenced by evenness (󳶳 Tab. 5.2). As with α diversity,
most of these relationships were positive. Despite the lower frequency of main effects,
evenness is sometimes influential in interaction with other biocrust properties (e.g.,
spatial patterning) [115, 126, 127].
Beta diversity was most the most consistent influence on ecosystem functioning.
Relationships between β diversity and at least one ecosystem function were detected
in all available studies meeting our criteria, and two thirds of ecosystem function in-
dicators examined were influenced by β diversity (󳶳 Tab. 5.2) These effects extend to
hydrology [50, 115], nutrient cycling [126, 128], and production [129]. While the num-
ber of studies conducted to date precludes us making strong inferences, the mount-
ing available evidence suggests that species richness and β diversity are among the
most influential biocrust attributes driving biodiversity–ecosystem functioning rela-
tionships. These biodiversity effects are as strong as or stronger than those of commu-
nity attributes such as total cover or spatial patterning [117, 126].
5.4.4 Multifunctionality
Increasingly, ecologists are moving beyond considering single ecosystem functions,

such as productivity, to multifunctionality, defined as the simultaneous performance
of multiple ecosystem functions [122]. Delgado-Baquerizo et al. [60] conducted a sur-
vey on three continents to assess how biocrust forming mosses affect multifunction-
ality, as measured with multiple soil variables related to carbon, nitrogen and phos-

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phorus cycling and storage. Compared with soil surfaces lacking biocrusts, biocrust
forming mosses enhanced multifunctionality in semiarid and arid environments, but
not in humid and dry subhumid ones. They also found that the relatively positive ef-
fects of biocrust forming mosses on multifunctionality compared with bare soil in-
creased with increasing aridity. Thus the presence of biocrusts does seem to enhance
ecosystem multifunctionality. The next logical question is whether the diversity of bio-
crusts exerts an effect upon multifunctionality as it does for single ecosystem func-
tions.
Lefcheck et al. [114] conducted a meta-analysis of the effects of species richness
on multifunctionality using a comprehensive database of 94 experiments, manipulat-
ing species richness across a wide variety of taxa, trophic levels, and habitat. Two key
results from this study were: (i) multifunctionality was enhanced as species richness
increased, and (ii) the overall effect of species richness on multifunctionality grew
stronger as more functions were considered. To date, two studies have suggested that
a greater number of biocrust species promotes greater multifunctionality and that a
greater number of species is required to sustain multiple functions than a single func-
tion (󳶳 Tab. 5.2) [116, 126]. The few studies available indicate that diversity of biocrust
mosses and lichens is highly important to maintain ecosystem multifunctionality in
drylands, and that biocrusts follow the general trend exhibited by other communities.
5.4.5 Functional Redundancy or Singularity?
Given that mosses, liverworts, and lichens are all poikilohydric, and desiccation and
stress tolerant primary producers, it would be logical to suspect that they tend to-
ward functional redundancy [130]. Redundant species are essentially interchange-
able, and the loss of one such species would not be expected to reduce ecosystem
function, although it has been suggested that redundancy may bolster an ecosystem’s
ability to maintain function under differing conditions [131]. There are two reasons
why we doubt that biocrust bryophytes and lichens are functionally redundant. First,
if biocrust mosses, liverworts, and lichens were redundant, we would expect ecosys-
tem function or multifunctionality to asymptote at relatively low levels of species rich-
ness; this is not so. Relationships between biocrust richness and their functional-
ity are much closer to linear relationships than asymptotic ones, suggesting that at
least across the range of observed values, an increase in richness leads to an increase
in a given function or in multifunctionality [115, 132]. This observation might relate
to variation in response to environment, for example different ideal combinations of
water and light availability and temperature for maximal photosynthetic rate among
species [129]. A multispecies community with different environmental optima would
be more likely to maintain high productivity, regardless of the conditions at a given
moment. The other reason to believe that individual species are fundamentally dif-
ferent is that individual species abundances can be tied to high values of particu-

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5.5 Summary and Conclusions | 89
lar functional indicators, suggesting distinct ecological roles [128, 133]. For example,
biocrust communities rich in the lichen Squamarina lentigera exhibited higher phos-
phatase activity, when compared to communities dominated by Diploschistes diacap-
sis [128]. Likewise, mosses and lichens exhibit fundamentally different effects on hy-
drology, with mosses often acting as infiltration promoters, but lichens acting to gener-
ate runoff [50]. Different mosses and lichens are also known to have distinct functional
traits. For example, only a subset of lichens is known to have the ability to fix nitrogen
(e.g., Collema, Leptogium, Heppia, Peltula, Peltigera). Lichen and moss species also
have a wide chemical diversity, and many of the chemicals likely affect other commu-
nity members that may impact ecosystem processes [42, 92, 108].
We suggest that the perception of redundancy disappears when more than one
function is considered. Functional profiles of 23 biocrust forming organisms in Spain
were tabulated along with all of their documented effects on ecosystem functions [128].
Over half of them had a unique set of effects, even though many species exerted some
of the same effects. When considering biodiversity loss, this suggests that at low lev-
els of biodiversity, communities may have different functional attributes based on the
particular species present. As more species are added, it becomes more likely that
most functions are being conducted by at least one species, and, therefore, multi-
functionality is more likely to be sustained at higher richness [116, 126].
5.5 Summary and Conclusions
Biocrust lichens and bryophytes shape the landscape in all areas where vascular plant
development is limited, including arid regions, occupying the soil surface and provid-
ing important ecosystem functions. Biocrust lichens and bryophytes are documented
from all continents, and some species are widespread among land masses. The major-
ity of species are restricted to one or a few geographic areas, a pattern that may partly
be determined by dispersal limitations. Within major landmasses, α and β-diversity
are largely determined by climatic gradients such as aridity, or edaphic factors such
as pH or gypsum content of the soil. Depending on these factors, different commu-
nity assemblages are formed, with resulting impacts on ecosystem function. In gen-
eral, ecosystem function increases with higher biocrust species richness, for individ-
ual ecosystem functions as well as for ecosystem multifunctionality. Changes in com-
munity composition have also been linked to differences in ecosystem function or
multifunctionality. Because of this, and evidence that some ecosystem functions are
tied to particular species traits, it is important to consider individual biocrust moss
and bryophyte species as singularly important, rather than functionally redundant.
Climate change and land use practices are already impacting the function and diver-
sity of biocrust communities. Management and conservation efforts should focus on
maintaining viable biocrust habitat (especially that of endemics) aiding dispersal, and
restoring biocrust communities in degraded habitat.

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Andrea Porras-Alfaro, Cedric Ndinga Muniania, Paris S. Hamm,
Terry J. Torres-Cruz, and Cheryl R. Kuske
6 Fungal Diversity, Community Structure and Their
Functional Roles in Desert Soils
Desert ecosystems represent a rich reservoir of unexplored fungal diversity with com-
plex assemblages of microbial communities. Deserts are considered one of the most
hostile habitats for life on Earth [1, 2]. They encompass extreme conditions for life, in-
cluding drastic changes in temperature, high ultra violet and infrared radiation, low
moisture availability, long periods of dryness, low nutrient availability, and osmotic
stress [3, 4]. All these characteristics require organisms with specific adaptations to
survive in this intense and variable environment [5–7].
Fungi in these areas include a high number of taxa with hyaline and melanized
hyphae that inhabit rock surfaces, biocrusts, rhizosphere soils, and plant tissues
(󳶳 Fig. 6.1) [3, 6, 8, 9]. Taxa with melanized hyphae are known as dark septate fungi
(DSF) (󳶳 Fig. 6.2a,b). Dark septate fungi (DSF) are a nonmonophyletic group of fungi
that includes a diverse taxonomic assemblage within Ascomycota. Orders such as
Pleosporales, Sordariales, Capnodiales, Xylariales, Helotiales, and Hypocreales in-
clude a number of DSF commonly isolated from multiple substrates in deserts includ-
ing soils and plants [10]. Dark septate fungi are dominant inside plant tissue as endo-
phytes, on the surface of rocks, and in biocrusts, a microbial community composed
of algae, cyanobacteria or moss together with fungi, bacteria, and archaea [3, 11].
They are also considered as being of special interest in the medical field because they
are allergens and cause pulmonary and skin diseases in immunocompromised and
healthy individuals [12].
A majority of fungi in arid lands grow as asexual forms (mitosporic) or as sterile
mycelia (󳶳 Fig. 6.2) and are thus difficult to characterize, but advances in molecular
techniques and the low cost of sequencing have recently allowed large surveys in these
areas, showing important potential for the description of novel taxa [8, 9, 13–16]. This
chapter focuses on the description of fungal diversity in the different microenviron-
ments characteristic of arid lands. We will discuss their roles as plant and biocrust
symbionts, their function in nutrient cycling, their responses to climate and land use
changes, and their potential as pathogens in humans.
6.1 Spatial Heterogeneity of Fungal Communities in Arid Lands
The sparse distribution of plants and biocrusts in arid ecosystems creates a series
of microenvironments in which fungi can be supported by the photosynthetic prod-
ucts and organic matter in zones where primary producers are present (i.e., islands of
DOI 10.1515/9783110419047-006

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98 | 6 Fungal Diversity, Community Structure and Their Functional Roles in Desert Soils
(a) (b)
(c) (d)
(e)
(f) (g)

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󳶣 Fig. 6.1: Diverse microenvironments for fungal communities in desert ecosystems. (a) Coleogyne
ramosissima (blackbrush) in a lichen dominated biocrust, (b) grasses and cyanobacteria dominated
biocrust, (c) lichen dominated biocrust in gypsum soils, (d) desert varnish, (e) patchy distribution of
plant communities, (f) lichen dominated biocrust, (g) moss dominated biocrust.
(a) (b)
(c) (d)
(e) (f)
Fig. 6.2: Common fungi in arid systems. (a) Dark septate endophyte colonizing a grass root, (b) dark
septate endophyte on root surface, (c) ectomycorrhizal fungi in piñon pine roots, (d) arbuscular
mycorrhizal fungus, (e) microcolonial fungi inside pits on rock surface, scale bar 200 μm [5], (f) ker-
atinophilic bait from soil using sterile snake skin.

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fertility)(󳶳 Fig. 6.1) [17]. Biocrusts and rhizosphere zones account for the highest diver-
sity of fungi in arid lands [8, 9, 15, 18, 19], but other communities are found in more
extreme conditions such as desert varnish and gypsum deposits [5, 20, 21]. Distinct
fungal communities in deserts are supported by the high heterogeneity created by the
combination of seasonal climate, variable distribution of nutrients and water, and a
mosaic of microenvironments [8, 17, 22].
6.1.1 Biocrusts
Biocrusts, also known as biological soil crusts or microbiotic crusts, are prominent fea-
tures of desert ecosystems (󳶳 Fig. 6.1). Biocrusts can cover up to 70% of the ground in
some deserts [23]. This common arid microenvironment supports large microbial com-
munities that involve a photosynthetic component (algae, cyanobacteria, or moss)
combined with a microbial mat of fungi, archaea, and other bacteria; in which the
bacterial biomass is 50–500 fold higher than the biomass of surrounding noncrusted
soils [24, 25]. Biocrusts are classified by their color and texture or by the communities
of microorganisms found in them [24, 26]. The darker crusts are dominated by cyano-
lichens and mosses (󳶳 Fig. 6.1a, c,f-g), and light crusts include cyanobacteria such as
Microcoleus vaginatus (󳶳 Fig. 6.1b). The structure of microfungal communities in bio-
crusts is influenced by the photosynthetic partner and has shown large spatial hetero-
geneity from small areas to large regional scales (󳶳 Fig. 6.3a) [19, 25, 27]. Fungi show
very patchy distributions even at the millimeter scale with high hyphal density areas
while other areas lack hyphal components [24]. The patchy distribution has been con-
firmed using molecular methods in which comparison of biocrusts in close proximity
show high variation and little overlap in terms of their fungal community composition
(󳶳 Fig. 6.3a) [16].
Diversity studies on biocrusts reveal abundance of different fungi that rank
from 40–106 species using a combination of cultured based techniques and molec-
ular markers (mainly based on Sanger sequencing and DGGE bands). The most
abundant genera within Ascomycota, the dominant phylum, include taxa such as
Alternaria, Acremonium, Chaetomium, Phoma, Preussia, Stachybotrys, and Ulocla-
dium [15, 18, 24, 27]. Many species within these genera are considered pathogens
and decomposers that likely benefit from the carbon and nitrogen fixed by the pho-
tosynthetic partners. Steven et al. [15] reported at least 78 unique OTUs (operational
taxonomic units) using cloning and sequencing of the LSU (large subunit) in biocrusts
from Utah, USA. Culture based studies have reported 71 species and 48 genera in the
western Negev Desert in Israel [27]. A recent study using 454 Titanium sequencing
of biocrusts showed a slightly larger diversity than previously reported for biocrusts
(140–228 OTUs for the LSU rRNA region) [16]. Next generation sequencing techniques
facilitate the detection of larger numbers of taxa, the comparison of studies, and the
determination of potential culture based bias toward fast growing fungi.

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A. Sand crusts B. Shale crusts C. Between sand and shale
108 121 88 79 Sand Shale
40 50 46 41
(37%) 22 (41%) (52%) 12 (52%)
18 210 136
25 107
21 24 12 8 (66%) (56%)
45
39 (54%)
(36%)
109 83 317 243
D. Taxonomic composition of conserved OTUs
100
Percent of shared OTUs
80
Unclassified Fungi
60 Chytriomycota
Basidiomycota
40
Unclassified Ascomycota
20 Rare Ascomycota
Dothideomycetes
0
Sand Shale Sand and Shale
(25 OTUs) (18 OTUs) (107 OTUs)
E. Taxonomic distribution of root-associated fungi
CL1–N–64
CL2–N–67
CL3–N–60
CL4–C–50
CL5–C–43
CL6–C–77
CL7–N–22
CL8–N–23
CL9–N–20
CL10–C–17
CL11–C–21
CL12–C–28
CL13–N–26
CL14–N–27
CL15–N–24
CL16–C–22
CL17–C–21
CL18–C–29
0% 20% 40% 60% 80% 100%
Pleosporales Agaricales Xylariales Sordariales
Phallales Hypocreales Glomerales Halosphaseriales
Onygenales Pezizales unknown
Fig. 6.3: Fungal diversity in the biological soil crust of the Colorado Plateau. (a–c) Shared OTUs for
different replicate samples showing little overlap among fungal communities and large spatial het-
erogeneity. (d) Taxonomic composition of shared OTUs showing dominance of Dothideomycetes and
a large number of unclassified fungi at this site. (e) Dominance of Pleosporales (Dothideomycetes) is
also observed in individual plants (each bar) of Bouteloua gracilis in a semiarid grassland. Modified
from [9, 16].

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Dominance by dark septate fungi ranges from 83–98%, including abundant

taxa within the Dothideomycetes, Sordariomycetes, Eurotiomycetes, and the Pezi-
zomycetes (󳶳 Fig. 6.3a) [14, 15, 18, 24, 27]. Dominant taxonomic groups are consistent
across culture based and molecular studies using different techniques such as DGGE,
Sanger sequencing, and 454-Titanium sequencing. Pleosporales is the dominant
fungal order in arid land biocrusts, in some cases representing up to 92% of the se-
quences [16, 18, 19], making this order one of the most important groups in terms of
abundance and diversity in biocrusts. Specific areas, such as the Chihuahuan desert,
report larger numbers of undescribed taxa within this order with little similarity to
known fungi, illustrating how incomplete the fungal diversity from these systems
is represented in curated databases [14, 18]. The large number of undescribed taxa
opens new opportunities for the description and characterization of new species. For
example, Knapp et al. [13] recently described three new genera and five new species
within the order Pleosporales from a semiarid region.
Other fungal phyla such as Basidiomycota and lower lineages of fungi, including
zygomycetes (mainly Mortierellales) and chytridiomycetes, are present in biocrusts in
a smaller proportion (< 1−20%). Agaricomycetes are dominant within Basidiomycota
represented by taxa in the orders Agaricales, Cantharellales, Corticales, Polyporales,
and Tremellales, including several yeast species [19]. Many of these fungal orders in-
clude plant pathogens, decomposers, and important mycorrhizal fungi. Lichenized
fungi are also common in arid soils, even in cases when lichens are hard to distin-
guish from cyanobacterial dominated biocrusts [14, 16, 28]. Lichens are discussed in
detail in Chapter 5 in this book. Within the basal lineages of fungi, Mortierella alpina
seems to be quite common across different types of biocrusts [14, 29], and reports of
chytrids using molecular methods shows great potential for the description of new
species [16, 18].
Dominant fungi in biocrusts have adapted to the harsh conditions on the sur-
face soil, including high UV radiation, high temperatures during the summer, and ex-
tremely limited water. Their melanized hyphae not only protects them against these
conditions, but likely provides protection to cyanobacteria, algae, and other microor-
ganisms in the biocrust [3]. It is possible that hyphal mats may also play a role in sta-
bilizing the soil surface and limiting erosion in arid lands [3].
Fungi associated with different types of biocrusts affect nutrient availability
through decomposition and transfer of nutrients with nearby grasses [30]. Fungal
hyphae have been observed in direct contact with clusters of Microcoleus vaginatus,
the dominant cyanobacteria in biocrusts [24]. Rhizosphere soils and biocrusts share
a great proportion of specific fungal taxa [15, 18], and the overlaping fungal commu-
nities in these different patches are relevant to the support of fungal networks (also
referred to as fungal loops) [17] that facilitate the interchange of nutrients between the
biocrusts and rhizosphere zones. Green et al. [30] showed that grasses and biocrusts
transport N (and C) through fungal networks. In this trace element study, 15 N was
translocated from biocrusts and grasses at rates of up to 100 cm/day [30].

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Microbial communities in the biocrusts are highly sensitive to changes in precip-

itation regimes with dramatic reductions in biocrust cover with altered precipitation
patterns [15, 31, 32], but additional data needs to be collected to determine potential ef-
fects of changing climate on the structure of their fungal communities. Biocrusts show
great potential for conducting simple and low cost manipulations in the field [15, 33].
Their distribution and spatial heterogeneity facilitate the establishment of studies in
microbial diversity, biogeography, and responses to climate change [31].
6.1.2 Plant Associated Fungi in Deserts
In addition to biocrust fungi, plant associated fungal communities (rhizosphere, my-

corrhizal fungi, and endophytes) represent very important habitats for fungal diver-
sity in arid lands (󳶳 Fig. 6.2). Plant associated fungi include taxa in every fungal phy-
lum and represent multiple ecological strategies varying from mutualists, commensal-
ists, pathogens, and saprobes. The fungal colonizers inside roots, stems, leaves, and
seeds include more specialized community of fungi [9, 18, 34, 35], such as mycorrhizal
and nonmycorrhizal species with large colonization rates by endophytic dark septate
fungi [9, 35, 36].
Biocrusts and rhizosphere soils share an important proportion of fungal taxa. The
structure of their fungal communities differs but dominant colonizers are frequently
detected in both microenvironments [15, 18]. As in biocrusts, rhizosphere fungal com-
munities are influenced by the presence of organic matter, nutrients, season, precipi-
tation, and levels of CO2 [15, 37–41].
Ascomycota fungi are dominant (68–88%) in rhizosphere soils with lower and
variable proportions of Chytridiomycota, Blastomycotina, Mucoromycotina, and
Mortierellomycotina (< 1–31%) [15, 18, 22, 37]. Dothideomycetes, Eurotiomycetes, Leo-
tiomycetes, and Sordariomycetes, all classes within Ascomycota, are common [8, 15].
In the shrub Larrea tridentata (creosote) in the Mojave desert, Dothideomycetes within
the order Pleosporales were abundant [15, 40]. Similar proportions of dominant taxa at
the class and order levels are consistent in multiple studies including arid grasslands
in New Mexico, USA [18, 42] and are associated with plants in the family Asteraceae
in a semiarid grassland in Europe [43]. Hudson et al. [22], using a metagenomic ap-
proach for rhizosphere soils in a semiarid grassland in New Mexico, also detected
high proportions of Ascomycota (65%) with important contributions of Basidiomy-
cota (30.9%) and arbuscular mycorrhizal fungi (AMF, 5.4%), which are more difficult
to detect using conventional PCR based approaches [22].
6.1.2.1 Mycorrhizal Fungi

Mycorrhizal colonization in arid lands is not as abundant in comparison to more mesic
environments but is still an important component of arid land fungal diversity [42,

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44, 45]. Mycorrhizal fungi have important roles in the acquisition of nutrients, such
as nitrogen and phosphorus. They facilitate the attachment of plant roots to the soil,
access to water, and other essential nutrients [46, 47]. The stressful conditions of arid
ecosystems favor two main groups of mycorrhizal fungi: arbuscular mycorrhizal fungi
(AMF) and ectomycorrhizal fungi (EMF)(󳶳 Fig. 6.2c,d).
6.1.2.2 Arbuscular Mycorrhizal Fungi

Represented by species in the phylum Glomeromycota, AMF are the most common
plant symbionts found in about 80% of vascular plants (󳶳 Fig. 6.2d) [48, 49]. AMF play
major roles in the establishment of plant communities in low-nutrient arid land soils
by facilitating nutrient absorption, water uptake, and soil stabilization [48, 50, 51].
Though not as diverse and abundant as in other ecosystems, such as temperate
forests, AMF communities in arid ecosystems portray some level of species richness
and varying levels of colonization on plants. For example, general estimates of AMF
biomass abundance in plants range from 4 g m−2 in deserts in comparison to 44 g m−2
in temperate grasslands [52]. In terms of species diversity, AMF taxa defined based on
SSU rRNA analyses revealed lower numbers of AMF (27 taxa) for desert environments
in comparison to temperate broadleaf mixed forests (82 taxa), temperate seminatu-
ral grasslands (90 taxa), and subtropical savannas and grasslands (43 taxa). Diversity
was comparable or higher in deserts with respect to boreal forests (12 taxa), subtropi-
cal dry broadleaf forests (18 taxa), and temperate coniferous forests (12 taxa) [53]. The
differences in diversity may be a result of the low number studies available for deserts
that are poorly represented in molecular curated databases and the techniques used
to detect these fungi in the environment. For example, the use of next generation se-
quencing has helped reveal an abundance of AMF fungi in piñon pine, which was
considered primarily colonized by ectomycorrhizal fungi in juniper-piñon woodland
in New Mexico [54].
The order Glomerales with Glomus group A is the dominant cluster of species [44].
Other dominant genera include Claroideoglomus and Scutellospora [44, 51, 55]. The
orders Archaeosporales and Diversisporales are represented by genera such as Ar-
chaeospora, Diversispora, and Acaulospora but colonization levels are low [51]. In arid
lands, AMF colonization rates vary greatly for different sites. Some fungi unique to
desert ecosystems have relatively high colonization rates varying from 37 to 95% de-
pending on their location, nutrient availability, and environmental conditions [44, 51,
55], while some grasses showed very low colonization rates [35, 45, 56]
AMF nutrient acquisition and survival is highly dictated by water availability at
these sites. The diversity and rates of root colonization by AMF tend to decrease with
dryness but hyphae can survive for long periods under dry conditions [55, 57]. For
some AMF, such as Acacia laevis and Scutellospora calospora, infectivity during the
dry season also depends on the time of sporulation. The hyphae of A. laevis have the

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capacity to infect plants for 11 weeks in dry soils if they did not receive water before
sporulation started [55].
In addition to season, plant diversity and plant ecophysiological adaptations to
stressful conditions create abiotic constraints that dictate the composition and growth
of AMF communities [58]. Plants such as Atriplex halimus, a common plant of arid
and semiarid regions, excretes salt as an adaptation to this stressful environment [59].
Thus, salt tolerant fungi dominate the diversity of AMF in A. halimus. Also, particular
vegetation in areas with a high level of gypsum (gypsophytes) tends to present unique
AMF structures in Glomus species that are specific for these sites [20].
6.1.2.3 Ectomycorrhizal Fungi (EMF)

Represented by species in the phyla Basidiomycota and Ascomycota, EMF are essen-
tial for desert trees and flowering plants [60, 61]. Ectomycorrhizal fungi link plant
roots to the soil and surrounding plant communities, increasing nutrient efficiency
in an environment with low nutrient quality and in some areas with high soil toxi-
city [62]. The most common type of basidiomycetes collected in these areas include
Amanita species such as A. rubescens, A. citrina, and A. muscaria; Hebeloma species
such as H. sinapizans and H. crustuliniforme; Laccaria laccata; Paxillus involutus, and
Russula vesca [62]. Using 454-Titanium sequencing, Dean et al. [54] also reported a
diverse assemblage of genera in piñon-juniper woodlands in New Mexico, including
Cenococcum, Inocybe, Tricholoma, Rhizopogon, and Geopora, showing the potential of
next generation sequencing for the documentation of ectomycorrhizal fungi in these
poorly studied sites (󳶳 Fig. 6.2c) [54].
Mycoheterotrophic plants such as desert orchids are nonphotosynthetic plants
that obtain all their nutrients, including carbon, from fungi rather than photosyn-
thesis [63], They are also dependent on ectomycorrhizal networks for their survival.
Fungi associated with desert mycoheterotrophs belong to the class Agaricomycetes,
with Russulales, Sebacinales, and Boletales being the most common orders and Rhi-
zopogon and Sebacina being the most common genera [64, 65].
Other mycorrhizal communities include desert truffles. They constitute a diverse
group of hypogeous ectomycorrhizal fungi also known as turma [60, 61] and play a
major role in maintaining certain plant communities in arid lands [61]. Desert truffles
include species in the genus Terfezia, Tirmania, Picoa, and Balsamia, and mainly col-
onize the roots of plants in the family Cistaceae, known as rockroses, such as Cistus,
Tuberaria, and Helianthemum [66–68]. Because of their adaptations to stressful con-
ditions in arid ecosystems, they are spread worldwide with a higher number of reports
in well studied sites in the Middle East, the Mediterranean basin, the African Kalahari,
and the Australian desert [7, 60]. In these regions truffles also have economic impor-
tance in the food industry, where they are used as an expensive seasoning. The most
commonly found species are Terfezia leptoderma, T. boudieri, T. claveryi, and Picoa
lefebvrei [60, 61].

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6.1.2.4 Nonmycorrhizal Fungi (Endophytes)

Fungal endophytes have been recovered from leaves, stems, roots, and seeds of many
species of arid plants. The term endophyte refers to fungi that inhabit plant tissues
without causing any damage to their hosts [69, 70]. Root endophytes do not form the
characteristic structures for nutrient transfer commonly observed in mycorrhizal fungi
(i.e., vesicles, arbuscules, Hartig net, mantle). These plant-fungal associations occur
with diverse species across all fungal phyla and are found in every studied plant across
the globe [10, 69, 71]. In arid ecosystems, endophytes are important for nutrient trans-
fer and plant survival because they provide protection against stressful conditions,
such as drought and heat, but also against biotic factors such as herbivory [47, 69, 72].
Compared to other ecosystems, the diversity of fungal endophytes in arid lands
is relatively low, but the rate of plant colonization can vary greatly among plant
species [72–75]. Endophytes are phylogenetically diverse, showing important levels
of novel species even at low colonization rates. An analysis of 22,000 plant segments
from desert trees and shrubs showed colonization rates of 1–3.5% on stems and leaves
with more than 60% of the isolates likely representing novel species [34]. Large num-
bers of potential novel species have also been recovered from roots in piñon-juniper
woodlands [54] and grasses [9, 21, 35, 42, 44].
Root colonization rates in grasses are high (60–90%) with variation among plant
species and tissue types (aboveground vs. belowground communities) [9, 21, 35, 42].
Dominant taxa in roots are similar to those observed in rhizosphere and biocrust soils,
including many Dothideomycetes, Eurotiomycetes, Sordariomycetes, and a propor-
tion of Basidiomycota mainly within Agaricomycetes (󳶳 Fig. 6.3e). Species such as
Alternaria, Fusarium, Aspergillus, Chaetomium, Preussia, Monosporascus, Darksidea,
and Moniliophthora appeared to be generalists, isolated from diverse plant species
and tissues [10, 13, 35]. Other species such as Phoma pomorum show higher levels of
specificity for specific tissues such as stems and leaves [72], resulting in more selective
endophytic communities [13, 34].
Unlike mycorrhizal fungi, the functions of nonmycorrhizal fungi (endophytes
and other rhizosphere associated fungi) are not well defined. Their ecological roles
likely vary based on tissue, environmental factors, and host; ranging from mutualists
to plant pathogens to saprobes [69]. For example, species of the genera Olpidium,
Monosporascus, and Moniliophthora are well known plant pathogens, but are usually
abundant in association with healthy roots of desert plants, mainly from the family
Poaceae (󳶳 Fig. 6.3e) [9, 35, 42, 66]. Coprophilous fungi traditionally found in animal
dung have also been recovered from arid land grasses [9]. Herrera et al. [76] suggested
a potential link between the endophytic and coprophilic life stages in which the fungi
are ingested by animals as plant endophytes and they continue as coprophiles once
excreted.
Among the different types of endophytes in arid lands, dark septate fungi are con-
sidered to be the most dominant, in some cases exceeding the abundance of AMF

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6.2 Roles in Nutrient Cycling and Effects of Climate Change on Fungal Communities | 107
(󳶳 Fig. 6.2a,b) [9, 10, 35, 44]. Melanized septate hyphae are normally observed inside
root tissue with the formation of microsclerotia (󳶳 Fig. 6.2a) and intercellular and in-
tracellular colonization (󳶳 Fig. 6.2b) [9, 42, 56, 77]. Colonization is more common in
the root cortex with extraradical mycelium spreading from the intercellular spaces in
the roots into the soil [56].
Functional roles for the majority of DSF are still unclear, but fungal inoculation
experiments in several plant species reveal the potential to increase plant thermotol-
erance and survival under drought conditions. Some species of Curvularia have been
reported to confer thermotolerance to plants [78, 79]. A Paraphaeosphaeria quadrisep-
tata isolate from a Sonoran desert cactus provides protection to model plants such
as Arabidopsis thaliana to lethal temperatures through regulation of heat shock pro-
teins [47]. This genus is also one of the most common taxa recovered from grasses such
as Bouteloua gracilis, B. eriopoda, among others [9, 74]
More specialized communities of endophytes in desert ecosystems include fungi
in gypsum deposits or very specialized environments, like the Caatinga deserts in
Brazil. With a worldwide coverage over 100 million ha, gypsum soils represent an-
other specialized ecosystem in arid and semiarid regions with low annual precipita-
tion and large numbers of endemic plant species (󳶳 Fig. 6.1) [21, 80]. Gypsum soils are
characterized by high concentrations of calcium sulfate (CaSO4 ), low nutrient content,
and low porosity. Thus, gypsophiles and gypsovags, the most common type of plants
found in gypsums, have unique mycorrhizal and endophytic communities [81, 82].
Colonization rates vary widely among different plant tissues and species endemic to
gypsum soils [21, 80, 83]. The variation of endophytic and mycorrhizal communities
is likely correlated with the physiological and ecological demands of the plants as a
response to stressful conditions of this environment. Commonly isolated genera from
healthy plant tissues include Alternaria, Sporormiella, Phoma, Fusarium, Rhizoctonia,
Epicoccum, Pleospora, and Cladosporium [21, 82].
Other specialized endophytic communities have been identified in the Caatinga
deserts in Brazil. The dominant type of desert vegetation in this area includes cacti,
shrubs and thorny trees, as well as arid grasses [84]. Species of Penicillium and As-
pergillus are, common and unique species for these areas have been described, includ-
ing A. caatingaensis and A. pernambucoensis. Other unique Neosartorya species in-
clude N. indohii, N. paulistensis, N. takakii, N. tatenoi, N. tsurutae, and N. udagawae [84,
85].
6.2 Roles in Nutrient Cycling and Effects of Climate Change

on Fungal Communities
Arid lands are characterized by low soil N content and are more responsive to low N
input as a result of anthropogenic deposition [86]. Fungal interactions and responses

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to N and C additions are diverse and complex. Two decades ago the biotic component
of the global N cycle was attributed only to bacterial metabolism. Today we know that
fungi have a fundamental role in N transformations in arid soils. Fungi are capable
of dissimilatory nitrate reduction with production of NO, N2 O, and N2 [87, 88]. In arid
lands fungi are resilient to N deposition in short and long term N deposition exper-
iments, where little changes in diversity, community structure, and fungal biomass
have been observed with respect to bacterial communities [8, 9, 18, 86].
The main C source for soil fungi is supplied by plants and cyanobacterial crusts [17,
30] and by the rapid turnover of soil proteins in arid lands [89, 90]. During periods
of active growth, plant photosynthate may be translocated to biocrusts, the center of
N-fixation [17]. Fungi account for a substantial fraction, even the majority, of N2 O pro-
duction in arid land soils, since they can operate at low water potentials, and N2 O is
the principal product of fungal mineralization of amino acids through denitrification
via heterotrophic nitrifiers [87, 90].
In addition to their roles in nutrient cycling, fungi play important roles in decom-
position processes that are highly regulated by abiotic factors. Photochemical oxida-
tion (photodegradation) plays a major role facilitating the enzymatic oxidation pro-
cesses carried out by bacteria and fungi [4, 91, 92]. Fungal communities that can tol-
erate high UV radiation and low moisture can quickly respond to the small pulses of
water characteristic of arid environments. Fungi associated with plant litter consist of
filamentous dark septate ascomycetes and yeasts. Gallo et al. [91] reported dominant
communities of Sporiobolales, Coniochaetales, Cystofilobasidiales, and Pleosporales
in litter of juniper and piñon in arid woodlands of New Mexico. In deserts, small mam-
mals contribute to the accumulation of plant litter, allowing fungal communities to ac-
tively grow in a more humid environment with increased amounts of organic carbon.
This higher level and movement of organic matter directly impacts the dispersal and
structure of fungal communities, including specialized coprophilous fungi [76, 93, 94].
6.3 Extremophiles in Deserts
Extremophilic fungi are those that can survive in conditions that are considered stress-
ful or lethal for other organisms. As previously mentioned, fungi in deserts show adap-
tations to high UV radiation and low moisture, but in the mosaic of microenviron-
ments there are even more specialized fungal communities exposed to higher selective
pressures such as very high temperatures (40–70°C), and extremely low organic mat-
ter. We focus on two fairly well studied groups: thermophilic fungi and microcolonial
fungi in rock varnish.

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6.3 Extremophiles in Deserts | 109
6.3.1 Thermophilic and Thermotolerant Fungi
Thermophilic fungi can grow in a range of temperatures between 40–50°C [95],

with optimal growth at 45°C. Thermotolerant fungi include representatives that can
grow between 40–50°C but their optimal growth temperature is at 25°C instead of
45°C [96, 97]. Unlike bacteria, Eukaryotes experience irreversible membrane damage
above 65°C [95]. In desert ecosystems, these fungi can encounter conditions favorable
for growth during the monsoon season, in which high temperatures will hold for long
periods of time [96].
Thermophilic fungi reported in deserts include taxa within two major groups,
the Ascomycota and Zygomycota (Mucoromycotina). Common orders of thermophiles
in deserts include fungi within Sordariales, Eurotiales, and Mucorales [96]. Mucor
miehei, M. thermohyalospora, Rhizomucor tauricus, R. pusillus, Talaromyces, Remer-
sonia thermophila, and Stilbella thermophila are frequently reported in arid grass-
lands, as well as in many microenvironments in hot deserts [96]. Thermophilic fungi
have been isolated from different substrates, including bulk soil, litter, animal dung,
biocrusts, and rhizosphere soils [7, 96]. In Saudi Arabia up to 48 species of ther-
mophilic and thermotolerant fungi were isolated from different types of desert soils,
with two thirds of the species being thermotolerant and one third recognized as ther-
mophiles [98]. Thermophilic fungi have also been studied from desert soils in Egypt,
dominated by taxa such as Chaetomium thermophilum, Malbranchea pulchella var.
sulfurea, Rhizomucor pusillus, Myriococcum albomyces, Talaromyces thermophilus,
and Torula thermophila [99].
Powell et al. [96] showed that thermophiles vary seasonally in an arid grassland
in New Mexico, with the highest number of propagules in summer and spring dur-
ing the highest precipitation period. The amount of records for thermophilic fungi in
desert soils is relatively limited despite their ubiquitous distribution based on recent
reports [96]. This is likely due to the bias on isolation temperatures in culture based
studies and the notion that fungal diversity in deserts is low [7, 98].
6.3.2 Rock Varnish and Microcolonial Fungi in Deserts
In deserts, several organisms, including cyanobacteria, chlorophytes, fungi, mosses,

heterotrophic bacteria, and lichens, can produce rock surface communities that are bi-
ologically active, forming thin and complex layers on the top few centimeters of rock
surfaces [3]. These microcolonies can be found in association with specific mineral de-
posits known as rock varnish (󳶳 Fig. 6.1d, 󳶳 Fig. 6.2e). Rock varnish are present on rock
surfaces [5] and are coatings mainly made of clays, oxides, hydroxides, manganese,
and iron. They are found in deserts and semiarid regions all over the world. These dark
coatings are hard and have a unique chemistry; they are usually black when they are

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rich in iron and manganese, dark brown or pigmented opaline silica when rich in iron
oxides, and can be red when deficient in manganese [5, 6].
The origin of rock varnish is not completely understood; it could be the result of
abiotic processes, but it has also been suggested that their formation could be medi-
ated by microorganisms that are commonly observed on these surfaces [5, 6]. Micro-
colonial fungi are the predominant biological organisms on desert varnish rock coat-
ings; this fact has led researchers to study them as one of the forming agents of desert
varnish (󳶳 Fig. 6.1d, 󳶳 Fig. 6.2e) [5, 6].
6.3.2.1 Characteristics of Microcolonial Fungi

Microcolonial fungi (MCF) have the ability to survive where other organisms are rarely
found. They were first described in the Sonoran Desert by Perry and Adams in 1977, us-
ing scanning electron microscopy and morphological analysis [6]. Microcolonial fungi
are globally distributed and have been reported in the Sonoran, Mojave, Gobi, Namib,
Great Victoria, Gibson, Simpson, Arabian, and Nubian deserts [1, 6, 100], and in semi-
arid areas of the Mediterranean and the USA [7, 101].
These fungi form clusters on desert rocks and rock coatings of approximately
100 μm in diameter and have spheroidal subunits of approximately 5 μm in diam-
eter with black or dark brown pigmentation [1, 6, 100]. These fungi are part of epi
(surface) and endolithic (inside rock or in pores of mineral grains) communities and
they can penetrate sedimentary soft rocks such as limestone, sandstone, and marble,
and hard rocks such as granite and basalt [7]. One of the first reports on microcolo-
nial fungi in deserts was published by Staley et al. [7] in 1982 on rocks collected in
the western United States and Australia. The microcolonial structures were grown in
the laboratory, obtaining slow growing fungal colonies that were mainly composed
of a single isolate. The fungi on these rocks are metabolically active and have been
referred to as blackberries and black globular units due to their color and shape [6].
Even though very limited morphological diversity has been observed, studies using
DNA sequencing have shown high genus and species diversity within several orders
of ascomycetes [7].
6.3.2.2 Adaptations of Microcolonial Fungi

Microcolonial fungi are recognized as one of the most stress tolerant eukaryotic or-
ganisms [7, 102]. Their colony morphology is thought to be a response to the environ-
mental stressful conditions allowing for an optimal surface–volume ratio, decreas-
ing water loss and reducing the fungal surface exposed to sun radiation and different
stressors [7, 102]. Other factors of stress adaptation include the melanization of multi-
layered cell walls and the generation of trehalose to stabilize enzymes under desicca-
tion [7, 101, 102]. It has been suggested that these fungi are chemoorganotrophs, since
they rely on nutrients and carbon from external sources brought to the rock surface
by the wind, like small particles of organic matter (e.g., pollen grains) [1, 6]. Micro-

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colonial fungi do not actively grow during hot periods regardless of the humidity but
can survive for long periods under the severe desert conditions [100]. Pigments such
as melanin, mycosporines, and carotenoids protect them from UV light [6, 101, 103],
and their vegetative cells are highly stress tolerant and long living [6]. Colonies of
these fungi produce large amounts of extracellular polymeric substances (EPS), which
might provide protection from the sun [6, 7, 103], and can absorb water and hold it
against the rocks for longer periods [3].
6.3.2.3 Importance of Microcolonial Fungi

Black microcolonial fungi are responsible for biological deterioration of marble and
limestone monuments and statues, growing as a dark brown or black crust on their
surfaces. They are considered one of the most damaging microorganisms in terms of
the deterioration of monumental stones in all cities worldwide, not just arid lands.
For example, a study by Marvasi et al. [104] characterized Sarcinomyces petricola as
the yeast responsible for the dark spots found on two valuable statues (“Ratto delle
Sabine” and “Copia del David”) located in the Piazza della Signoria in Florence, Italy.
The study of these fungi is important in order to decide on proper procedures to restore
and conserve monuments.
Microcolonial fungi allow us to study the limits of life on Earth, evolution, and
adaptation to extreme environmental conditions by eukaryotic organisms [105]. It is
suspected that rock varnish coatings exist on Mars, and our understanding of how
microcolonial fungi have developed several adaptations against harsh environmental
conditions can provide good models to study rock coatings that can facilitate detection
of life on other planets [6]. Studies of stress resistance by these fungi have provided
promising results on their ability to survive space and Martian conditions [7, 102].
Cryptomyces antarticus (a cold desert microcolonial fungus) has even been shown to
survive simulated Martian conditions and real space exposure [101, 105].
6.4 Human Pathogenic Fungi in Desert Ecosystems
Arid soils are not immune to the ubiquitous distribution of fungal pathogens. In
desert ecosystems, fungi reproduce mainly through asexual reproduction, creating
large amounts of propagules or drought resistant spores that can be easily dispersed
by wind, even at transcontinental distances [3]. Changes in climate and extreme
droughts followed by dust storms and the increase in the number of infectious lung
diseases have brought attention to the study of pathogenic fungi in desert ecosys-
tems [106]. Opportunistic infections may occur in immunocompromised individuals
due to a decreased ability to fight infections, such as those with HIV/AIDS or leukemia,
in organ transplant patients, children, or the elderly.

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6.4.1 Coccidioides immitis and C. posadasii
From the family Onygenaceae, containing true human pathogens, the genus Coccid-
ioides is of particular interest in desert ecosystems. This soil borne fungus, which re-
produces using arthrospores, is endemic to arid regions of Mexico, Central and South
America, and the southwestern United States [107]. Coccidioidomycosis, better known
as Valley Fever, starts as a lung infection that can evolve into pneumonia and even
become systemic and spread to other organs such as the skin, brain, and bones, and
particularly endangers immunocompromised populations [108]. Outbreaks often oc-
cur among farmers and construction workers after dust storms [109] or earthquakes
and during other events when the soil is disturbed [110, 111]. The CDC reported one
of the overall highest incidences in 2011 with 42.6 cases per 100,000 people, with the
largest number of cases among 60–79 year olds (69/100,000) in states where Valley
Fever is endemic and has been reported (Arizona, California, Nevada, New Mexico,
and Utah). The number of cases from 1998 to 2014 ranged from 2,271 to 22,641 [112].
The San Joaquin Valley in southern California is one of the most important en-
demic areas in the United States for Coccidioides immitis. The more prevalent Coccid-
ioides posadasii has been detected across the southwestern US and is endemic to Mex-
ico and South America, predominantly Argentina, Venezuela, and Brazil [113]. Tem-
perature and soil texture seem to be the only two factors that regulate the presence
of Coccidioides based on a study of nine sites in California, Utah, and Arizona [114].
Coccidioides-bearing soils are characterized by very fine sand particles and silt, and
its distribution seems to be limited to very specific areas of the planet [114].
Like in the case of other true human pathogens, the detection of Coccidioides in
the environment is very difficult due to its sporadic distribution. Only 0.55% (4 out
of 720) positive soil samples were obtained in California [115]. More sensitive detec-
tion is possible using BALB/c mice as biosensors with 8.9% positive detection in soils
from the Tuscan area in Arizona, which is known for the presence of Coccidioides
posadasii [116]. Intraperitoneal inoculation into mice was also successful in isolating
C. posadasii from 6 out of 24 (25%) soil samples from Brazil [117]. This technique has
facilitated the examination of Coccidioides spp. in endemic areas [117].
6.4.2 Dematiaceous and Keratinolytic Fungi in Deserts
Fungi in the family Arthrodermataceae, as well as other taxa found in desert soils, are
keratinolytic known for their ability to degrade keratin and grow on skin, hair, and
nails of animals. The ability to break down keratin, a stable and resistant cytoskeletal
filament in human and animal cells, is considered a virulence factor of those fungi
known as dermatophytes [118]. Dermatophytes can cause a common skin infection
in humans known as ringworm or tinea. These infections are confined to the dead

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Table 6.1: Percentage of Arthrodermataceae fungi isolated from desert soils.
Bahrain Israel Kuwait India Iran Tunisia

Microsporum gypseum 3.75 4.4 7.5 12.5 22.96 27.4
Trichophyton mentagrophytes 2.5 1.66
Arthroderma curreyi 3.7
T. terrestre 3.5 5.83
Chrysosporium indicum 2.5 17.5 19.16 14.07 11
C. pannicola 15.7 10 7.5
Arthroderma cuniculi 3.7
C. tropicum 2.5 20 10 14
References [120] [121] [122] [123] [125] [141]
superficial regions of the skin and are highly contagious, but in the majority of the
cases they can be treated with the application of antifungal creams [119].
The dermatophytic macroconidial species of Epidermophyton, Microsporum, and
Trichophyton can be found ubiquitously in the environment, including deserts. The
most common desert soil dermatophyte is Microsporum gypseum, isolated from sev-
eral countries, including Bahrain, Israel, Kuwait, India, Egypt, and Iran [120–125]
(󳶳 Tab. 6.1).
In addition to true dermatophytes, other saprophytic fungi can also cause oppor-
tunistic infections in humans. In desert soils, keratinophiles can take advantage of
keratin as a carbon source in a low nutrient environment. Alternaria, a robust ker-
atinophile and a very abundant fungus in deserts, has been reported as the causing
agent of phaeohyphomycotic cysts in immunosuppressed individuals [126]. Fusarium
solani and Fusarium oxysporum, both reported keratinophiles and common in deserts
(󳶳 Fig. 6.2f), are also considered the most common causative agents of Fusarium myco-
sis [127]. Paecilomyces, Geomyces, and Chaetomium keratinophiles and opportunistic
pathogens are also common in arid soils [15, 18, 125].
6.4.3 Eumycetoma
Eumycetoma is a fungal chronic pseudotumorous infection of the skin and subcuta-

neous tissue with high incidence in tropical, subtropical, and arid regions. The infec-
tion progresses with granulomatous lesions and discharge of grains with fungal par-
ticles that spread into adjacent tissue, bone, fascia, and ligaments [128, 129]. Males
between 16–50 years old with agricultural occupations have the highest incidence of
this infection [129, 130]. The most common infection site is the foot that has been ex-
posed to soil or plant material containing a pathogenic fungus [131] after a traumatic
injury. Diagnosis is often accomplished by a biopsy and examination of the grains
produced by the fungus, culture based methods, or DNA sequencing from infected

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tissue. Madurella mycetomatis is the usual etiological agent, but eumycetomas have
also been reported for other common genera including Exophiala jeanselmei, Lep-
tosphaeria senegalensis, Madurella grisea, Fusarium, Aspergillus, Curvularia, Acremo-
nium, and Paecilomyces, among others [129–132], many of which are common taxa in
deserts.
The mycetoma belt includes South America, Sudan, Somalia, Senegal, and south-
ern India [132]. Extensive reports from arid regions include the Republic of Niger, Mex-
ico, Brazil, Iran, India, and Somalia [129, 131, 132]. Sudan shows the highest number
of eumycetoma cases in the world (70% of cases) with Mexico second with an average
of 70 cases per year [131, 132].
6.4.4 Mycotoxins
Mycotoxins are a diverse group of toxic and carcinogenic compounds produced by

fungi. In economically poor arid regions they are not very well documented, but rep-
resent a major problem for human and animal health. Many of the fungi responsi-
ble for the production of mycotoxins are xerophilic (i.e., they can grow in low hu-
midity or low water content) and are abundant in desert soils. The most prominent
species of fungi producing mycotoxins are Penicillium, Aspergillus, and Fusarium; with
the production of significant toxins such as aflatoxin, fumonisins, ochratoxin A, tri-
chothecenes, and zearalenone [133, 134]. Mycotoxins can cause adverse effects that re-
sult in illnesses of animals as well as serious problems for human health. For example,
Fusarium moniliforme, colonizing maize is known to cause leukoencephalomalacia in
horses and has cancer promoting activity due to fumonisins [135]. Ochratoxin A is the
nephrotoxic responsible for human Balkan endemic nephropathy and other urinary
tract tumors [136].
Aflatoxin contamination by Aspergillus is common in arid ecosystems such as the
sub-Saharan Africa. This fungus benefits from high humidity and temperature, but
drought conditions increase the risk of aflatoxin contamination [137]. Aflatoxin is the
most potent naturally occurring carcinogenic substance and is likely responsible for
the highest incidence of hepatocellular cancer in Africa [138]. Kenya reported an acute
outbreak of aflatoxicosis with 317 cases in July 2004, with a fatality rate of 39% caused
by A. flavus contamination and ingestion of contaminated maize [139]. The replace-
ment of millets and sorghum for maize as the preferred cereal for food puts higher
numbers of individuals at risk, since maize seems to have higher colonization rates by
aflatoxin producing Aspergillus strains [137, 140].

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References | 115
6.5 Importance of Fungal Biodiversity in Arid Lands
Plant and biocrust associated fungi comprise a large untapped reservoir of fungal di-
versity. Most studies have focused on specific plant species or sites combining molec-
ular and cultured based methods, but the advent of next generation molecular tech-
niques (e.g., genomics, transcriptomics, metagenomics) is opening new opportunities
to study fungi in arid lands and their response to climate and land use changes [16, 22,
32]. Challenges are still present with the low number of fungal genomes available and
the low number of functional categories that are well annotated. Metagenomic stud-
ies have proved to be of great value even with the disproportionate number of bacteria
(97–99%) vs. fungal (0.5–1.5%) metagenome reads in arid soils. The metabolic poten-
tial and diversity of specific taxa that are difficult to detect using regular PCR based or
culture based techniques have been revealed in current studies [15, 22].
Arid lands in general are considered critical zones of biological interactions [2, 3].
These fragile ecosystems are threatened by environmental changes and their distur-
bance could result in large scale impact on other ecosystems, including marine envi-
ronments, through dust deposition, increase of human infections, among others [2].
Fungi represent a key component of the dynamics of these ecosystems. A better un-
derstanding of the structure and function of fungal communities in deserts will facili-
tate the establishment of practices to ameliorate damage, improve preservation of arid
sites, maximize their potential for discovery of new species, and generate applications
in agriculture and the medical field.
Acknowledgment: AP-A support was provided by National Science Foundation (award

number 1457002) and the Sevilleta Long Term Ecological Research Site. Support for
CRK is from the US Department of Energy, Biological and Environmental Research
Division, through a science focus area grant.
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T.G. Allan Green
7 Limits of Photosynthesis in Arid Environments
Abstract: Soils in arid zones are often covered with biological soil crust (BSC) typ-
ically composed of bacteria, fungi, cyanobacteria, algae, lichens (lichenized fungi)
and bryophytes (mosses and liverworts). BSC have major effects on the stability and
functioning of the soils. All organisms in BSC are poikilohydric, meaning that they
can desiccate and are only active when wet. Photosynthesis of BSC, therefore, shows
response curves to incident light, temperature, CO2 concentration, and thallus water
content (WC). Photosynthesis of BSC is typically optimal at high light, around 15 to
20°C and ambient CO2 above 1000 ppm. Response to WC can be complex, but photo-
synthesis is limited at low WC and often, due to diffusion limitations, at higher WC.
BSC rarely carry out photosynthesis under optimal conditions. Environmental water
status is the major limiter, and in arid areas BSC are active for around 30% of the total
time. In addition, they are active at light intensities and temperatures that are lower
than the habitat means. Further limitations occur from thallus water content effects,
either from low WC when drying or partially hydrated by dew, but also because many
BSC organisms show depressed photosynthesis at high WC. The latter effect can be so
intense that the organisms make little carbon gain from heavy rainfalls. As a result,
overall carbon fixation is probably only around 1% of the theoretical maximum. The
ability of BSC organisms to acclimate to a changing environment has probably been
greatly underestimated and may occur in a few days, so that it might even be fast
enough to influence the results of laboratory studies.
7.1 Introduction
Biological soil crusts (BSC) are a mixture of autotrophic and heterotrophic organisms
that (i) live within or on top the uppermost millimeters of soil creating a consistent
layer and (ii) aggregate soil particles due to their presence and activity [1]. BSC are com-
posed of a wide range of organisms, typically including bacteria, fungi, cyanobacteria,
algae, lichens (lichenized fungi) and bryophytes (mosses and liverworts) of which all
except bacteria (excluding cyanobacteria) and fungi are photosynthetic. Although lo-
cal conditions strongly affect the presence of the different organisms, successional
stages are recognized for BSC with initial colonization by filamentous cyanobacteria
followed by smaller green algae and cyanobacteria and, finally, when the surface has
stabilized, lichens and mosses [1].
BSC organisms cannot be treated as small higher plants but show important dif-
ferences in their physiology and ecology. Firstly, and a physiological trait that links all
BSC organisms, is that they are poikilohydric, meaning that their water status tends to
equilibrate with the surrounding environment; they are wet and active when the envi-
DOI 10.1515/9783110419047-007

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124 | 7 Limits of Photosynthesis in Arid Environments
ronment is wet, and dry and dormant under dry conditions. When dry, BSC organisms
can withstand extremes of light and temperature (both high and low). Poikilohydry,
through water supply and support, also enforces a size limitation on organisms with
the vast majority being less than a centimeter high [2]. This, in turn, means that they
are confined to a two-dimensional habitat in which they are almost always within the
atmospheric boundary layer, bringing important changes to the interactions with the
environment such as in heat exchange [2].
BSC occur throughout the world but, because of competition for light, are best de-
veloped in habitats in which competition by phanerogamous plants is limited. Such
environments are hot, cool and cold semiarid and arid areas, and also polar and alpine
zones. Such habitats are not productive, however their large extent means that they
are estimated to contribute around 1% of global net primary production [3]. Because
of their marginal climates BSC in these areas are also suggested to be more suscep-
tible to future climate changes [4], and this is one important reason to gain a better
understanding of the limits to photosynthesis by BSC.
7.2 Photosynthetic Responses to Environmental Factors,

a Background
7.2.1 Rates, Chlorophyll and Mass
Lange [5] summarizes the then available maximal net photosynthetic rates under op-
timal conditions (NPmax ) for a wide variety of soil crusts, and these span over two or-
ders of magnitude between around 0.1 and 11.5 μmol m−2 s−1 . The majority of NPmax
for BSC lie between 2 and 5 μmol m−2 s−1 (󳶳 Tab. 7.1), which are high rates compared
to the more typical 1 to 2 μmol m−2 s−1 for rain forest lichens [6].
Table 7.1: LMA (mass per unit area), CO2 exchange rates, quantum efficiency and chlorophyll content
for seven BSC lichen species
LMA Maximal net Dark Quantum Chlorophyll

photosynthetic rate respiration efficiency
Species g m−2 μmol m−2 s−1 nmol g−1 s−1 μmol m−2 s−1 mg m−2
Collema cristatuma 310 2.8 9.03 0.95 0.015 43

Fulgensia fulgensb 440 5.2 11.82 1.25 0.026 450
Lecanora muralisc 510 6.5 12.75 1.60 0.025 564
Cladonia convolutad 630 5.4 8.57 1.80 280
Squamarina lentigerae 684 4.0 5.85 1.50 0.024 227
Collema tenax f 1190 3.9 3.28 1.80 0.015 170
Diploschistes diacapsisg 2000 5.0 2.5 1.50 0.011 1350
Source of data: a [7], b [8], c [9], d [10], e [11], f [12], g [13].

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7.2 Photosynthetic Responses to Environmental Factors, a Background | 125
Chlorophyll contents of BSC span a large range and can be comparable with those
of average C3 leaves, which require 500–700 mg chl m−2 to achieve maximal quantum
yield of CO2 uptake [5]. The chlorophyll contents of BSC lichens span a wide range
from a low 42.7 mg chl m−2 for Collema cristatum to an exceptional 1350 mg chl m−2
for D. diacapsis (󳶳 Tab. 7.1) [5]. There are differences between the various BSC types.
Zhao et al. [14] report 20.7, 29.0 and 38.1 mg chl m−2 for algal, mixed and moss domi-
nated BSC from Tengger Desert in China, and Kidron et al. [15] measured 16.7 to 43.4 mg
chl m−2 for cyanobacterial BSC and 53.2 mg chl m−2 for moss dominated BSC in the
Negev Desert. For the Qubqi Desert, Mongolia, Lan et al. [16] found a large increase
in chlorophyll content with BSC development from 30 mg chl m−2 in cyanobacterial
dominated early crusts to 210 mg chl m−2 for fully developed moss dominated crusts.
There appears to be no significant link between BSC chlorophyll content (mg chl m−2 )
−1
and NPmax (μmol m−2 s ) (󳶳 Tab. 7.1).
Although data are limited, lichens forming BSC appear to be “heavy” in compari-
son to those growing in forests, showing a wide range in leaf mass per area (LMA,
g dry weight m−2 ) from 310 gdw m−2 for Collema cristatum, to 2000 gdw m−2 for
Diploschistes diacapsis (󳶳 Tab. 7.1). This compares to mean values of 86 gdw m−2
and 97 gdw m−2 for Lobaria scrobicularia and Lobaria pulmonaria, and 73 gdw m−2
Pseudocyphellaria crocata (Merinero et al. 2014), and 59 to 91 gdw m−2 for Pseudo-
cyphellaria dissimilis from inside a New Zealand rain forest [17]. Similar magnitudes
of LMA are reported for a wide range of lichens summarized in [18]. Data for bryo-
phytes are not as easy to interpret as for lichens. Lichens, albeit a symbiosis, are a
discrete organism and relatively easy to separate from soil crusts. Bryophytes, and
mosses in particular, are known for being intimately bound with the soil crusts and
can contribute to the structural strength of the BSC. As well as not being easy to
separate from the crust, mosses have substantial portions of the plant below ground,
which are not photosynthetic and will always be respiring when active. Studying Grim-
mia laevigata Alpert and Oechel [19] found 85.5 gdw m−2 for green parts of the plant
and 161.5 gdw m−2 for brown parts (total 247 gdw m−2 ). Longton [20] found 241–692
gdw m−2 (100% cover) for Bryum argenteum and 1012–1108 gdw m−2 for B. antarcticum
(= Henediella heimii) with the former growing in sheets and the latter in clumps. In
contrast, Wu et al. [21] report 26.5 gdw m−2 for the desert moss Syntrichia caninervis
in the Gurbantünggüt Desert, China, and Green and Snelgar [22] showed the thalloid
liverworts Monoclea forsteri and Marchantia foliacea, New Zealand rain forest, to have
only 33 and 35 gdw m−2 but still achieve a maximal net photosynthetic rates of 0.81
and 0.99 μmol m−2 s−1 , respectively. There appears to be no relationship between
NPmax (area basis) and LMA, but there is a significant negative relationship between
NPmax (dry weight basis) and LMA [23].

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7.2.2 Response of Net Photosynthesis (NP) to Light (PPFD, μmol m−2 s−1 )
󳶳 Fig. 7.1a shows the typical saturation response of net photosynthesis to light by a
lichen or bryophyte. Marked on the response curve are the so-called cardinal points:
light level or photosynthetic photon flux density (PPFD) required to achieve maximal
NP (PPFDsat ), quantum efficiency of NP to light (QE), which is initial slope of the re-
sponse curve at low light, light level to achieve compensation (i.e. zero NP, PPFDcomp ),
and dark respiration rate (DR), which is NP at zero light. The PPFDsat is typically
around 700 μmol m−2 s−1 for BSC, and as a result they are referred to as sun plants [5].
However, BSC do not achieve the same photosynthetic rates as higher plants, which
have leaves with protected photosynthetic cells and are able to build canopies. The
high PPFDsat of BSC can be interpreted as a protection against the occasional bursts of
high light or maintenance of the ability to benefit from such conditions; these are not
exclusive. The light compensation point is positively correlated with high PPFDsat [24]
and BSC have relatively high values for PPFDcomp, often 60 to 100 μmol m−2 s−1 , which
are also influenced by temperature, being lower at low temperatures. This has the ef-
fect of lowering carbon gain at low light levels, such as might be found after sunrise.
BSC also have low quantum efficiencies, from 0.015 to 0.026 (󳶳 Fig. 7.1a), which are less
than those found for shade lichens and higher plants – 0.05 and 0.06, respectively.
It is not surprising that with their high saturation light level for NP, BSC organ-
isms appear to be well protected against potential damage to photosystems from high
light. The highest light levels for BSC when hydrated and active are found in continen-
Net photosynthesis (μmol CO2 m–2 s–1)
4.0 8.0
Quantum efficiency
CO2 exchange – μmol m–2 s–1
15°C
3.0 6.0
10°C
4.0
2.0
5°C
2.0
1.0
0.0
0.0
Light compensation –2.0
Collema
–1.0 Dark Light –4.0 Diploschistes
respiration rate saturation Psora
–2.0 –6.0
0 200 400 600 800 1000 1200 0 10 20 30 40 50
(a) PPFD (μmol m–2 s–1) (b) Temperature – °C
Fig. 7.1: (a) Typical response curve of net photosynthesis (μmol CO2 m−2 s−1 ) to incident light (PPFD,
μmol m−2 s−1 ) of a soil crust at three temperatures (5, 10 and 15°C), showing the main cardinal
points: light required to obtain maximal NP (PPFDmax ), quantum efficiency, light level to give com-
pensation (no net CO2 exchange, PPFDcomp ), and dark respiration rate (DR). (b) Response of photo-
synthesis to temperature for BSC lichens; the response curves are generated at saturating light and
optimal thallus water content (modified from [12]). Color coding of symbols: black – Collema tenax,
red – Diploschistes diacapsis, blue – Psora cerebriformis: symbol shapes: • – net photosynthesis,
󳵳 – dark respiration, 󳶃 and dashed lines – Gross photosynthesis (NP – DR).

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7.2 Photosynthetic Responses to Environmental Factors, a Background | 127
tal Antarctica where mean PPFD when active can reach around 700 μmol m−2 s−1 [25],
and mosses have constitutive protection against high light with the xanthophyll cycle
components present in similar quantities in both light and shade adapted forms. This
protection of the photosystems is complimented by UV absorbing compounds [26]. It is
now also becoming clear that bryophytes and lichens employ other methods to han-
dle excess light and are physiologically agile in this area. One example is that both
CO2 and O2 can act as interchangeable electron sinks, and the nonsaturating compo-
nent of electron flow is photoreduction of oxygen [27, 28]. Although nonphotochem-
ical quenching (NPQ) is found in both algae and plants, these organisms rely on two
different proteins for its activation, light harvesting complex stress-related protein and
photosystem II subunit S, respectively. In the moss Physcomitrella patens, however,
both proteins are present and active [29].
As a general rule, no negative effects of high light or UV would be expected for
BSC unless levels are applied that have little ecological relevance, e.g., shade adapted
forms being exposed to very high light levels.
7.2.3 Response of Net Photosynthesis to Temperature
In contrast to the rather constant response of NP to PPFD for BSC there seems to be
a wider range of adaptions to temperature. Examples of typical responses of net pho-
tosynthesis to temperature (measured at saturating light and optimal thallus water
content) are shown in 󳶳 Fig. 7.1b, with all three species showing a similar form of re-
sponse. Net photosynthesis has an optimum temperature that is over 30°C for Collema
and lower, around 20°C but with a much broader range with little change in NP, for
the other two species. The decline in NP at higher temperatures is driven by the in-
creasing dark respiration (exponential increase with temperature) up to about 30°C
and at higher temperatures by a fall in photosynthetic capacity (gross photosynthe-
sis, GP), which reaches a maximum at just over 30°C for all three species. A maximal
rate of gross photosynthesis at around 30°C seems to be relatively common in lichens
and mosses and is even found in Antarctic species [30], indicating that the underlying
photosynthetic mechanisms show little change with environment. Differences in op-
timal temperature for NP are also reported for different organisms in the same habitat.
For example, 20–27°C, 15°C and 20°C for cyanobacteria, lichens, and mosses, respec-
tively, in the Mu Us Desert, Ningxia, northwest China (󳶳 Tab. 7.2, from [31]).
7.2.4 Response of Net Photosynthesis to Thallus Water Content (WC)
Thallus water content in BSC is usually expressed as mm rain equivalent (mm, equal
to liters per m2 ) and not, as is routine for lichens and bryophytes as % dry weight,
(% dw = [wet weight − dry weight] ⋅ 100/dry weight), because of the difficulty in sepa-

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Table 7.2: Comparison of photosynthetic rates and light response, and thallus water content (WC)
for BSC dominated by cyanobacteria, lichens and mosses; data from [31].
BSC type NP max Optimal PPFD to PPFD com- Optimal Maximal

tempera- saturate pensation WC for NP WC
ture NP
μmol CO2 (°C) μmol m−2 s−1 μmol m−2 s−1 mm rain mm rain
m−2 s−1 equivalent equivalent
Cyanobacterial 2.67 20–27 900 70 0.38 1.3
Lichen 3.06 15 870 90 0.92 2.5
Moss 6.02 20 1200 50 2.10 3.8
rating BSC organisms from their substrate. At very low thallus water content there is no
CO2 exchange, but as WC rises, so does NP until a maximum is reached (󳶳 Fig. 7.2). At
NPmax the organisms are at, or close to, full turgor (relative water content, RWC, = 1.0)
and at the so-called optimal water content WCopt [2]. Homoiohydric plants do not ex-
ceed RWC of 1.0, but lichens and bryophytes can do this because of variable amounts
of external water held in capillary spaces outside the cells. As a result, maximal RWC
in BSC organisms can be much higher than 1.0, often up to 2.0 or 3.0 for lichens and
substantially higher for bryophytes (see 󳶳 Tab. 7.2 for a comparison of cyanobacteria,
mosses and lichens at a desert site). The change in NP at WC above WCopt is strongly
15 3
Net photosynthesis ( μmol m–2 s–1)
Number of rainfall events
2
10
Number of events
Diploschistes
Psora
Didymodon
1
5
0
0 –1
0 1 2 3 4
Rainfall – mm (0.2 mm categories) or
Thallus water content – mm rain equivalent
−1
Fig. 7.2: Line graph: Response of net photosynthetic rate (right hand axis, μmol m−2 s ) measured
at saturating PFD and 15°C to thallus water content (mm precipitation equivalent) for two lichens,
• – Diploschistes diacapsis and 󳶃 – Psora decipiens, and one moss, 󳵳 – Didymodon rigidulus from
Tabernas Desert, Almeria, Spain. Bar graph: distribution of rainfall occurrence with each bar repre-
senting the number of occurrences of a rainfall event of a particular size; X axis is rainfall event size
in 0.2 mm categories. Note the “plateau” of the moss (󳵳).

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7.3 Optimal Versus Real Photosynthetic Rates | 129
species dependent and can vary from maintenance of NPmax to a strong decline in NP,
sometimes to negative values. The decline in NP at high WC is due to increased CO2
diffusion resistances caused by blockage from capillary water and cell wall expan-
sion [32]. Three examples are shown in 󳶳 Fig. 7.2 and also for two species in 󳶳 Tab. 7.1.
Diploschistes diacapsis has a WCopt of 0.5 mm and a maximal WC of 1.2 mm, whereas
for the second lichen, Psora decipiens, the equivalent values are 1.2 mm and 2.5 mm,
respectively. Both species show a sharp maximum in NP. In contrast, the moss has a
WCopt of 1.2 mm and a maximal WC of 3.9 mm. In addition it shows a relatively small
decline in NP from WCopt to around 3.6 mm. This is a reasonably general difference
with bryophytes having higher WCopt and maximal WC than lichens. Both lichens and
bryophytes show a wide range in their response curves and these appear to be adap-
tive. For example, the very low WCopt and maximal WC values for D. diacapsis appear
to allow the species to benefit from dew fall [23].
7.2.5 Response of Net Photosynthesis to CO2 Concentration
Net photosynthesis typically shows a similar form of saturation response to CO2 con-
centration as shown for light (󳶳 Fig. 7.1a). Most lichens require around 1000 ppm CO2
to saturate NP while mosses and liverworts, despite normally having single-cell thick
leaves require around 1500 ppm CO2 . There is little information available for BSC, but
studies on cyanobacterial dominated BSC show a linear response of NP to 1000 ppm
CO2 [33]. The actual CO2 concentration around and/or within BSC remains enigmatic.
There is evidence from many ecosystems from Antarctic mosses to rain forests that ac-
tual CO2 levels close to the soil surface can be higher than global CO2 concentrations
due to an efflux of CO2 from the soil [34]. CO2 concentrations within the soils covered
with BSC can reach 1200 ppm and are almost always above the ambient atmospheric
levels [33, 35]. Such concentrations indicate a continual efflux of CO2 from the soil
and must include sources in addition to recycling of BSC fixed carbon. Possible major
sources are higher plant roots and associated mycorrhizae. The latter can receive up
to 20% of the carbon fixed by the host plant [36].
7.3 Optimal Versus Real Photosynthetic Rates
According to the response curves presented in 󳶳 Fig. 7.1a,b, 󳶳 Tab. 7.2, BSC at optimal
WC will reach NPmax at a light level ≥ 500 μmol m−2 s−1 and temperatures ≥ 15°C.
Higher light levels will have no effect on NP as most BSC seem to be well protected
against excess light. Higher temperatures will lead to lower NP but not in the under-
lying photosynthetic rate until GPmax is not reached at around 30°C. From these data
it might be expected that the normal habitat of BSC in arid areas is one of high light
and moderate to high temperatures.

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In reality, all BSC photosynthetic organisms are poikilohydric and will only be ac-
tive when hydrated. It is, therefore, necessary to distinguish between conditions when
the organisms are active and when they are inactive. In the latter case they are typically
resistant to extremes of light, desiccation and temperature [23]. With the exception of
the rare example where fruticose lichens become active solely following equilibration
with humid air [37] BSCs in hot arid areas are hydrated either by rain or by dew [38, 39]
and in the cold Antarctic desert by melt water [25].
Dew and rain produce different patterns of activation for mosses and lichens in
BSC. Activation by dew starts for both mosses and lichens during the night and ends in
the morning soon after sunrise as they desiccate. The net result is that the organisms
are active at lower temperatures and light levels than the overall conditions for the
habitat. In particular, dry lichens and mosses become very hot, reaching over 60°C,
because they are good insulators when dry. In contrast, rain can activate the BSC at
any time of day. Both lichens and mosses rapidly activate and can stay so for several
1600 1000
Active Moss 1000
1400
Number of data points
Inactive Didymodon rigidulus 800 Inactive

800
1200 600
Active
1000 600 400

800 200
600 400 0
0 200 400 600 800 1000
400
200
200
0 0
0 10 20 30 40 50 60 0 500 1000 1500 2000 2500 3000
(a) Temperature (b) PPFD (100 μmol m–2 s–1 bands)
1600 1000
Lichen 1000
1400
Psora decipiens 800

800
1200 600
1000 600 400
800 200
600 400 0
0 200 400 600 800 1000
400
200
200
0 0
0 10 20 30 40 50 60 0 500 1000 1500 2000 2500 3000
(c) Temperature (d) PPFD (100 μmol m–2 s–1 bands)
Fig. 7.3: Distribution of active and inactive times (number of data points in year) in relation to tem-
perature (a,c, 5°C bands) and light (b,d, 100 μmol m−2 s−1 bands) for the moss Didymodon rigidulus
(a,b) and the lichen Psora decipiens (c,d) forming BSC at Tabernas Desert, Spain. Left hand panels:
activity (left hand black bars) and inactivity (right hand gray bars); right hand panel: activity (right
hand red bars) and inactivity (left hand black bars). Note: active and inactive bars are reversed in left
and right hand panels.

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days but, once again, both temperature and incident light are lower than optimal val-
ues because of the cloud cover. Net photosynthesis follows the same pattern with a
so-called gulp in the early morning after dew activation [39]. The contrast between
temperature and light levels when active and when inactive is shown in 󳶳 Fig. 7.3. The
data are from continuous monitoring at Tabernas Desert, Almeria [38, 39] for the year
2013 and the lichen P. decipiens and the moss D. rigidulus. Both species behave very
similarly to PPFD when active, concentrated below about 500 μmol m−2 s−1 , although
when inactive levels can reach 2500 μmol m−2 s−1 . For temperature, activity is con-
centrated below 20°C, although both species can reach 60°C, and most activity is at
around 7.5°C for the moss and 12.5°C for the lichen. From August to March the major-
ity of the active time is at night, as one might expect from dew activation lichens and
mosses, while in summer months activity is mainly in the daytime, reflecting rain acti-
vation [39]. The pattern of different, suboptimal conditions when active has also been
well documented by continuous monitoring in Antarctica [25]. Schlensog et al. [40]
showed that mean light levels when active increasingly differ from overall incident
light as the proportion of the time that the organisms are active declines.
7.4 Limits to Photosynthesis in Arid Areas
7.4.1 Length of Active Time
Because of their poikilohydric lifestyle it is no surprise that the greatest limiter of

photosynthesis by BSC in arid zones is water availability. 󳶳 Fig. 7.4a shows the an-
nual run of activity for BSC in the Tabernas Desert, Spain (the annual precipitation
is 230 mm but variable) obtained by continuous chlorophyll fluorescence monitor-
ing [39]. The mean monthly time active for three lichens and one moss over 1 year was
20.7% ± 3.6 with a low of 0.0% in June and high of 74.7% in November (󳶳 Fig. 7.4a).
Activity in the dark typically exceeds that in the light, especially in the high activity
months, so that BSC were active in the light only 8.3% of the total time (󳶳 Fig. 7.4a).
However, carbon gain only occurs at light levels above the photosynthetic compensa-
tion point. Activity in the year 2013 and for the moss D. rigidulus and lichen P. decipi-
ens were 10.3% and 11.4%, respectively, and applying compensation points of 70 and
80 μmol m−2 s−1 gives a carbon gain only for 2.8% and 4.0% of the year, respectively.
Carbon loss through respiration occurs for about twice as long as positive NP, albeit
mainly at lower temperatures at night. A similar pattern is summarized for six lichens
by Evans and Lange [41] and is a further indication that low water availability severely
limits photosynthetic carbon gain by BSC.

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Temperature (°C)
<0 <10 <20 <30
Light/dark ratio
80 1.5 100
Proportion of time active (%)
Cumulative time active (%)

1.0
80
60 0.5
0.0 60
40
40
20
20
0 0
Oct
Nov
Dec
May
Jul
Oct
Sep
Jan
Feb
Mar
Apr
Jun
Aug
Sep
0 <500 <1000 <1500 <2000
Light (μmol m–2 s–1)
2012 2013
(a) Month (b)
Fig. 7.4: (a) Activity pattern through 1 year for BSC at Tabernas Desert, Spain (39 from October 2012
to September 2013). Black lines: annual run of mean monthly time active in light and dark (round
symbols) and only in the light (triangular symbols). Red lines, right hand upper Y axis scale, ratio of
light to dark activity for each month. (b) Plots of accumulated activity (%) for incident light – black
lines and symbols, (lower X axis, PPFD, in 100 μmol m−2 s−1 categories to 1000 (PPFD, μmol m−2 s−1
then 500 (PPFD, μmol m−2 s−1 categories; and for temperature – red lines and symbols (upper X axis
in 5°C categories). Circular symbols – moss D. rigidulus; triangles – lichen P. decipiens.
7.4.2 Limits When Active – External Limitation Through Light and Temperature
BSC are mostly active at lower than normal habitat temperatures and light (󳶳 Fig. 7.3).
󳶳 Fig. 7.4b shows cumulative activity plotted against temperature and incident PPFD
−1
(using only data above 0 μmol m−2 s ). Accepting a PPFD to saturate NP to be around
−2 −1
500 μmol m s , then around 70% of the activity occurs below saturation for the
moss D. rigidulus and lichen P. decipiens. Similarly, if the optimal temperature for NP
lies between 15 and 20°C, then again around 70% of activity is below this temper-
ature. It must be remembered that temperature and light covary significantly but if
PPFD to saturate NP is set at 500 μmol m−2 s−1 , PPFD to compensate CO2 exchange
at 50 μmol m−2 s−1 and optimal temperature for NP at 15°C, then in 2013 at Tabernas
Desert the lichen P. decipiens and the moss D. rigidulus were active above the optimal
light and temperature for photosynthesis for 15.3% and 11.2% of active time, respec-
tively. Over the whole year this is equivalent to 1.8 and 1.1%, respectively. The same
result is found for lichens and mosses with intermittent hydration in Antarctica [40].
7.4.3 Limits When Active – Internal Limitation Through Thallus Hydration
The response of NP to thallus hydration always shows limitation of NP below optimal

WCopt , and this situation will almost always occur when hydration is solely by dew. NP

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can also be depressed at WC higher than WCopt (󳶳 Fig. 7.2), a phenomenon that is more
common in lichens. As a result, carbon gain at the high thallus water contents, which
only occur after rainfall, may be much lower than might be expected. This effect can be
clearly seen in the annual contribution to carbon gain from different hydration sources
for Cladonia convoluta, a lichen showing no depression at high WC, and Lecanora mu-
ralis, with very strong depression (to 2% of maximal NP) at high WC [10]. C. convoluta
gains 78.2% of its annual carbon gain (= 111 mg C m−2 ) on rainy days while L. muralis
gains only 4.2% (= 0.9 mg C m−2 ). The converse is true for activation by dew when L.
muralis obtains 40.0% of annual carbon and C. convoluta only 5.9% (coincidentally
both equal approximately 8.5 mg C m−2 ). A somewhat similar situation can be seen for
BSC organisms in Tabernas desert (󳶳 Fig. 7.2). The lichen D. diacapsis shows a very low
WCopt and strong depression at higher WC and appears to be adapted to utilize dew
events with little carbon gain during rain events. In contrast, the moss D. rigidulus has
a very high WCmax (3.9 mm) with little depression up to a WC of 3.5 mm and is able to
utilize rain events but probably not dew events. Both organisms show similar activity
patterns (󳶳 Fig. 7.3) but carbon gains are probably very different.
7.4.4 Catastrophes
On occasions environmental conditions are such that organisms are unable to survive
or suffer extensive damage. Lichens are known to suffer so-called snow kill when snow
cover remains longer than normal [42]. It has also been suggested that carbon losses
during small intensity rainfall in deserts can cause moss death [43, 44]. The concept
is that of Mishler and Oliver [45], who suggested that in brief wet/dry cycles, such as
produced by a small hydration event like light rainfall, the moss will suffer net carbon
loss because photosynthesis recovers too slowly to counteract the more rapidly recov-
ering respiration. Coe et al. [46] suggest that a series of such rain events will then lead
to carbon starvation and death. Extensive bleaching of moss shoots was found both
in the field and in laboratory simulations. Intuitively this seems reasonable but it is
less so if the probable magnitude of carbon reserves is considered (unfortunately this
information is not given). Although rarely measured, the actual carbon reserves in
mosses can be about 6% of dry weight for small molecular weight sugars and 15% dry
weight for starches [47, 48]. One typical low rain event leads to a maximal net carbon
loss of about 0.24 mgC m−2 [43], which is around 0.02% of carbon reserves (at 36 g m−2
moss dry matter). Carbon starvation, therefore, seems to be an unlikely explanation
for the moss bleaching, and more probably these events represent a desiccation injury
made possible by laboratory pretreatment [49], see also the next section, or, because
of the short duration of the precipitation event the plants become exposed to high
light before protection mechanisms have been fully activated. There is the possibil-
ity that rewetting events can lead to loss of small molecular weight sugars during the
recovery; magnitudes of around 7% loss of soluble pool in lichens are reported [50],

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but even this is not likely to be catastrophic as the starch pool, which is larger, is not
released.
7.5 Flexibility – an Often Overlooked Factor
There is a major difference between gas exchange research on higher plants and that
on BSC (lichens and mosses generally). Typically, higher plants are either studied in
situ or when grown under controlled conditions, whereas BSC are most often brought
into the laboratory and studied there. In the latter case, the BSC are often given a pre-
treatment (several days under controlled light and temperature) before actual mea-
surements are made. Justifications are rarely given for the pretreatment but it is often
an attempt to reduce variability in the following measurements (e.g., [43]). The pos-
sibility that the BSC organisms may actually be changing their physiological perfor-
mance during the pretreatment has been mostly overlooked. Stark et al. [49] have con-
sidered this situation and investigated changes in desiccation tolerance during such
a pretreatment in the laboratory (curiously referred to as deacclimation when it is re-
ally acclimation to the laboratory conditions). Stark et al. [49] found changes were so
rapid that mosses had effectively lost their desiccation tolerance within 8 to 12 days
and performed very differently to immediately after collection. It is possible that this
is the cause of the moss bleaching demonstrated by Coe et al. [43, 46], see Section 7.5.5,
as the mosses were given a 5 day pretreatment in the laboratory before measurements.
Acclimation of respiration to temperature in the field has been clearly demonstrated
by Lange and Green [51]. Mosses in Antarctica were able to re-establish UV protection
within 6 days and to do this by growing new shoots [26].
It appears that acclimation during pretreatment under controlled conditions in
the laboratory could well be fast enough to change lichen and moss responses. Until
now, most BSC researchers have ignored this possibility, but perhaps it needs more
attention in the future.
7.6 Summary
BSC photosynthetic organisms are diverse but, to date, most research has been on
lichen and moss dominated crusts. All show the typical responses of NP to light, tem-
perature, thallus water content and CO2 concentration, although there are consider-
able differences in detail, particularly between lichens and mosses. All are poikilohy-
dric and are active only when hydrated. In arid areas where rainfall is low and also
spasmodic, it is no surprise that desiccation is the main cause of inactivity with an
overall active time of only 20% or less of the year. In summer BSC can be completely
dormant. Activation by dew occurs during periods of low light and temperatures gen-
erally in in the early morning, and activation by rain also usually occurs with low

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References | 135
PPFD due to clouds shading incoming sunlight. As a result BSC are most often (approx-
imately 80% of active time) active at suboptimal light and temperature conditions.
Photosynthesis at maximal rates appear to occur about 1 to 2% of the year. Further
limitations, highly species specific, occur at low hydration and high WC due to lim-
itations to CO2 diffusion and, adding these to previous limitations, suggests overall
activity at optimal rates for about 0.5 to 1% of the year. The ability of the BSC organ-
isms to adapt and acclimate has been greatly underestimated. Although small in size,
BSC organisms are metabolically agile, and this is shown by species specific changes
in the field, and it might also have an effect on laboratory studies where pretreatments
are used. Considerable scope remains for future research on photosynthesis of BSC,
particularly in the area of adaptation and acclimation.
References
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[4] Pointing SB, Belnap J. Microbial colonization and controls in dryland systems. Nature Rev Mi-
crobiol 2012, 10:551–62.
[5] Lange OL. Photosynthesis of soil-crust biota as dependent on environmental factors. In: Belnap
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berg, New York, Springer-Verlag, 2001, 217–40.
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Blaire Steven, Theresa A. McHugh, and Sasha Reed
8 The Response of Arid Soil Communities
to Climate Change
8.1 Overview
Arid and semiarid ecosystems cover approximately 40% of Earth’s terrestrial surface
and are present on each of the planet’s continents [1]. Drylands are characterized
by their aridity, but there is substantial geographic, edaphic, and climatic variability
among these vast ecosystems. For example, drylands vary greatly in their temperature
regimes, encompassing both hot and cold deserts, and such variation plays large roles
in structuring microbial communities [2, 3]. Indeed, the wide range of environmental
variables within and among drylands underscores the substantial variation in dry-
land soil microbial communities, as well as highlights how future climate could drive
additional community change globally. Furthermore, arid ecosystems are commonly
heterogeneous at a variety of spatial scales [4, 5]. Vascular plants are widely inter-
spersed in drylands and bare soil, or soil that is covered with biological soil crusts
(a photosynthetic community of mosses, lichens, and/or cyanobacteria living at the
soil surface), fill these spaces. This biological variability acts to further enhance spa-
tial heterogeneity, as these different zones within dryland ecosystems differ in char-
acteristics such as water retention, albedo, and nutrient cycling [6–8]. Importantly,
the typical soil patches of an arid landscape may be differentially sensitive to climate
change [9]. Soil communities are only active when enough moisture is available [10],
and drylands show large spatial variability in soil moisture, with potentially long dry
periods followed by pulses of moisture. The pulse dynamics associated with this wet-
ting and drying affect the composition, structure, and function of dryland soil com-
munities, and integrate biotic and abiotic processes via pulse driven exchanges, in-
teractions, transitions, and transfers [11, 12]. Climate change will likely alter the size,
frequency, and intensity of future precipitation pulses, as well as influence nonrain-
fall sources of soil moisture, and aridland ecosystems are known to be highly sensitive
to such climate variability [13]. However, despite this great heterogeneity, arid ecosys-
tems are united by a key parameter: a strong limitation by water availability [11]. This
characteristic may help to uncover unifying aspects of dryland soil responses to global
change.
The dryness of an ecosystem can be described by its aridity index (AI). Several
AIs have been proposed, but the most widely used metrics determine the difference
between average precipitation and potential evapotranspiration, where evapotranspi-
ration is the sum of evaporation and plant transpiration, both of which move water
from the ecosystem to the atmosphere [14–16]. Because evapotranspiration can be af-
DOI 10.1515/9783110419047-008

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140 | 8 The Response of Arid Soil Communities to Climate Change
Incident Vegetation/
Precipitation Radiation albedo Transpiration Wind Temperature
Fig. 8.1: Factors affecting an ecosystem’s aridity index. The aridity index is calculated from the dif-
ference in mean annual precipitation and potential evapotranspiration, which results in a loss of
soil moisture. Incident radiation can be blocked by clouds, reducing evaporation and transpiration.
Vegetation or changes in albedo (reflected sunlight) can alter the rate of evaporation at a local scale.
Transpiration is the process through which plants move water from roots to the atmosphere and re-
sults in moisture loss. Wind can act to dry surface soils. Temperature increases are associated with
increased evaporation.
fected by various environmental factors, such as temperature and incident radiation

(󳶳 Fig. 8.1), regions that receive the same average precipitation may have significantly
different AI values [17, 18]. Multiple studies have documented that mean annual pre-
cipitation and AI are highly correlated with biological diversity and net primary pro-
ductivity [19–22]. Accordingly, AI is considered to be a central regulator of the diver-
sity, structure, and productivity of an ecosystem, playing an especially influential role
in arid ecosystems. Thus, the climate parameters that drive alterations in the AI of a
region are likely to play a disproportionate role in shaping the response of arid soil
communities to a changing climate.
In this chapter, we consider climate parameters that have been shown to be al-
tered through climate change, with a focus on how these parameters are likely to affect
dryland soil communities, including microorganisms and invertebrates. In particular,
our goal is to highlight dryland soil community structure and function in the context
of climate change, and we will focus on community relationships with increased at-
mospheric CO2 concentrations (a primary driver of climate change), temperature, and
sources of soil moisture.
8.2 Biological Responses to Elevated Atmospheric CO2
Carbon dioxide (CO2 ) and other greenhouse gases (e.g., nitrous oxide, methane) are
naturally present in the atmosphere but are increasing in concentration due to hu-
man activities. The atmospheric abundance of CO2 was ∼ 400 ppm in 2016, approxi-
mately 40% higher than in 1750 [23]. Beyond being a main driver of climate change,
atmospheric CO2 concentration can directly impact the biology of arid lands. For ex-

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8.2 Biological Responses to Elevated Atmospheric CO2 | 141
ample, increasing atmospheric CO2 concentrations are known to affect both rates of
photosynthesis and water use efficiency [24, 25]. Further, deserts commonly house not
only the vascular plants common in most terrestrial ecosystems, but also the pho-
tosynthetic biocrusts that live in the interspace among vascular plants in drylands
worldwide [26–29]. Multiple free air CO2 enrichment (FACE) experiments have been
established in a variety of biomes to experimentally test the effects of atmospheric
CO2 enrichment (e.g., [24, 25]). In 1997, a FACE experiment was established in the Mo-
jave Desert to evaluate the long term effects of elevated CO2 on an arid shrubland
ecosystem [30]. The vegetation communities, dominated by the shrub Larrea triden-
tata, increased in net primary productivity and biomass in response to elevated CO2 ,
and showed an increased presence of invasive grass [31, 32]. Increased photosynthetic
capacity of biocrusts was also observed [33]. Interestingly, the effect of CO2 on vascu-
lar plants and biocrusts for a given year was dependent upon that year’s precipitation,
with a high enough annual rainfall being necessary to allow for a stimulatory effect
of increased CO2 [31, 33, 34]. Over the course of the experiment, the treatment also
affected the physiology of biocrust communities [33], and soil carbon pools increased
∼ 12% under elevated CO2 , indicating that much of the carbon gains from increased
photosynthesis by the shrubs and/or biocrusts were transferred to belowground com-
munities [32].
Despite observed higher carbon accumulation in the shrubs and larger soil carbon
pools, this did not result in higher biomass of the soil microbial communities under
elevated CO2 [35, 36]. However, the microorganisms tightly associated with the shrub
roots (i.e., the rhizosphere community) showed compositional shifts, with an increase
in Basidiomycota fungi and a decrease in Firmicutes bacteria, suggesting root exu-
dates or other sources of belowground carbon may be altered under elevated CO2 [35].
In contrast, the bacterial and fungal communities in the bulk soil collected beneath
the shrubs (but not associated with roots) showed little compositional change in re-
sponse to CO2 enrichment [36], suggesting that any CO2 induced changes in litter quan-
tity or quality did not impact the composition of the underlying soil microbial commu-
nity. Although the changes in the abundance and composition of the soil communities
under the canopies of the shrubs were relatively subtle, increases in soil respiration,
ammonia loss, and decreased inorganic nitrogen concentrations were all associated
with elevated CO2 [37, 38]. These observations indicate that even in the absence of a
large restructuring of the soil microbial community, elevated CO2 may drive changes
in soil function and nutrient cycling.
While shrub and lichen productivity was stimulated by elevated CO2 at the Mojave
FACE site, the treatment resulted in a small but consistent decrease in cyanobacterial
biomass [39]. Metagenomic sequencing of the community suggested that cyanobac-
teria under elevated CO2 conditions were enriched in genes to counteract oxidative
stress [39], implying that elevated CO2 may induce a stress response in dryland cyano-
bacteria. This stress is possibly due to a disconnect between environmental signals.
Generally, soil wetting results in a pulse of respiration and a diffusion barrier to CO2

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efflux, thereby increasing local CO2 concentrations [40]. Thus, an elevated CO2 signal
could be misinterpreted by cyanobacteria as the presence of soil moisture, leading
to mistimed metabolic activity [39]. In laboratory manipulations, arid soil photosyn-
thetic organisms increased their photosynthetic potential by 20–30% and stored more
carbon under elevated CO2 , but only during wetting pulses [41, 42]. As has been seen
for dryland vascular plants, observations indicate that the functional changes in soil
microbial communities due to elevated atmospheric CO2 concentrations are tightly
correlated with soil moisture and with climate effects on vascular plant processes.
Finally, biological nitrogen fixation rates in the crusted soils were not significantly
different between elevated and ambient CO2 conditions, but the rates of nitrogen fixa-
tion were more spatially variable under enriched CO2 [43]. This suggests that patches
of soil respond differentially to elevated CO2 , further complicating predictions of a
broad scale soil response to a CO2 enriched atmosphere.
In summary, the enrichment of CO2 (and other greenhouse gases) in the atmo-
sphere is a driving force behind climate change [23], but it also has the potential to di-
rectly impact the functioning of arid soil communities. Across a range of ecosystems,
a meta-analysis of the effects of elevated CO2 on soil communities found that a large
portion (40%) of CO2 enrichment experiments do not induce a change in the structure
of the indigenous soil populations [44]. The data synthesized here support this idea:
although the effects of CO2 were notable in vascular plants, they were more subtle in
the soil microbial community, although fewer published studies with a belowground
focus could play a role in this perspective. In this respect, enriched atmospheric CO2
seemed to primarily affect the function of the soils without major shifts in soil mi-
crobial community composition. However, the potential exists for strong interactions
with the availability of water in dryland systems [34, 45]. Thus, the effects of elevated
atmospheric CO2 could become more or less in their extent and magnitude, depending
on the response of factors that affect soil moisture. In particular, predicting the effects
of elevated CO2 enrichment on the status of arid soils will likely require coupled fore-
casting of changes in the dominant precipitation patterns.
8.3 Biological Responses to Increased Temperature
Drylands across the globe are exposed to a wide variation in temperature. The hottest
place on Earth, the Lotus Desert of Iran, is a dryland that experiences surface tem-
peratures above 70°C [46, 47]. In contrast, the mean annual temperatures of the Mc-
Murdo Dry Valleys in Antarctica range from −15 to −30°C [48]. Thus, dryland temper-
atures vary more than any other biome. Data suggest that soil microbial communities
in drylands structure themselves strongly along dryland temperature classes, such as
among hot and cold deserts [2]. Further, the low humidity in drylands results in lower
cloud cover and atmospheric water vapor, which allows heat gained during the day
to be easily lost at night. Therefore, drylands also tend to experience diurnal temper-

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ature shifts larger than those of other ecosystems. For example, the average diurnal
temperature change for arid systems ranges from 12 to 20°C, compared to 4–8°C in
coastal and temperate regions [49]. Climate change has the potential to not only af-
fect average ecosystem temperatures, but also to dictate significant changes to tem-
perature patterns across seasons and within a day. Global surface temperatures have
increased by ∼ 0.2°C per decade for the past 30 years [50] and, in this respect, the
magnitude of the temperature shift due to climate change will likely be relatively small
compared to the normal temperature fluctuations experienced by drylands. That said,
even small changes in temperature have the potential to dramatically affect dryland
systems (e.g., [51]) and, because activity in drylands is constrained to very short time-
lines (i.e., only when soils are wet), seemingly subtle changes to diurnal temperatures
could have dramatic effects at the annual and global scale.
In particular, because of large natural diurnal and seasonal temperature vari-
ations, many arid soil organisms are adapted to growth under large temperature
ranges [52, 53]. This, however, does not necessarily mean soil biota will be resistant or
resilient to increasing temperatures. At a continental scale, arid soils experiencing av-
erage temperature differences of 13 to 15°C showed a shift in the dominant cyanobacte-
rial species, an alteration that could be recapitulated with a similar temperature shift
in the laboratory [3]. Although these temperature increases are significantly larger
than those expected from climate change [50], smaller temperature shifts associated
with experiments in Spain (2.4°C above ambient), the Colorado Plateau (2 to 4°C
above ambient), and South Africa (2 to 4°C above average) induced dramatic changes
to moss and lichen diversity and abundance, but left the dominant cyanobacterial
population relatively unaffected [54–56]. Taken together, these observations suggest
that arid soil communities can be generally resilient to increases in temperature, but
certain community members may exhibit widely different thermal tolerances and re-
sponses to aspects of warming (e.g., the timing of warming). In this way, increases in
mean annual temperature, as well as in seasonal and diurnal temperature alterations,
have the potential to affect state changes in soil communities, particularly through
the relationship between soil moisture and temperature.
8.4 Biological Responses to Changes in Precipitation
With rising temperatures there is an increased capacity of the atmosphere to hold wa-
ter, resulting in altered humidity and precipitation patterns [57, 58]. On average, global
precipitation has increased approximately 2% in the 20th century, although this in-
crease has not been spatially or temporally uniform [59]. A common prediction from
global circulation models is that precipitation is likely to increase at mid and high lati-
tudes while decreasing in the subtropics [60]. Annual precipitation changes predicted
for drylands from a multimodel intercomparison ranged from a net decrease of 30%
to an increase of 25%, depending on the geographical region considered [61, 62]. Spe-

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cific projections include not only changes to absolute annual precipitation volumes
but also more variable precipitation patterns, with increased occurrence of extreme
events in Australian drylands [63], highly variable heavy rain events in arid and semi-
arid northern China (e.g., [64]), and more intense, irregular events delivering less pre-
cipitation in southwestern North America [65]. In general, more extreme precipitation
regimes are expected, with larger individual precipitation events and longer interven-
ing dry periods [66].
A significant challenge to predicting precipitation patterns at local scales is the
influence of topography and other landscape features [60]. Local precipitation is af-
fected by features such as coastlines, lakes, and mountains, making predictions for
topographically complex regions difficult [67, 68]. Consequently, precipitation predic-
tions are often incomplete or highly uncertain [59, 69]. Precipitation occurs as distinct
episodic events, and so it is also temporally variable. Precipitation models produce
predictions in seasonal or monthly time steps, whereas ecosystem components are
often responding to precipitation pulses at smaller temporal scales, with microbial
activity and respiration of invertebrates and shallow rooted plants rapidly stimulated
by changes in soil water potential [70]. Moreover, phenomena such as El Niño and
the Pacific Decadal Oscillation affect regional precipitation in complex and often un-
predictable ways [71]. In arid ecosystems, biological activity is often constrained to
time periods directly following precipitation events [72–75]. Consequently the timing,
duration, and event size may have more significance for soil biota than does average
rainfall amount [76, 77].
Alterations in precipitation patterns, including both size and form of delivery,
can have dramatic effects on sensitive, water limited dryland ecosystems [75]. This
alteration of the timing and size of individual rainfall events has the potential to af-
fect dryland soil communities via the strong responses of soil biota to rewetting and
subsequent drying. As an example, a rainfall experiment on the Colorado Plateau,
USA, showed that increased frequency of small (1.2 mm) rainfall events resulted in
pronounced mortality of the widespread moss Syntrichia caninervis, dramatically re-
ducing moss cover after only one season of treatment (see Section 8.4.2 below for more
details). These results reveal how seemingly subtle modifications to precipitation pat-
terns can affect ecosystem structure and function on unexpectedly short timescales.
Moreover, the soil moss mortality was the result of increased precipitation, underscor-
ing the importance of precipitation event size and timing over absolute amounts of
moisture [51]. As another example of a dramatic response, a modest increase in win-
ter precipitation was associated with a threefold increase in shrub cover, severe reduc-
tions in reptile abundance, and the near local extinction of a keystone rodent in the
Chihuahuan Desert in southwest USA [78].

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8.4.1 Natural Precipitation Gradients
A wealth of research has focused on the response of plant communities to changes

in mean annual precipitation [79–81]. Because this is a difficult parameter to exper-
imentally manipulate, particularly at large scales, rainfall gradient approaches are
often used to describe the effects of different precipitation regimes on ecosystem struc-
ture and function. To a large extent, patterns in vegetation composition and function
across precipitation gradients suggest that decreased water availability is correlated
with a decrease in net primary productivity and biological diversity [60, 82]. However,
patterns for belowground communities have not been as easy to disentangle. Partly,
this is due to the complexity of soil systems and the difficulty in linking changes in
regional parameters to soil community metrics that vary at small spatial scales. For
example, the additional water availability from decreased evaporation in refuge sites
beneath shrubs or rocks is generally a larger predictor for arid soil microbial commu-
nity structure than is mean annual rainfall [83]. Soil microorganisms beneath shrubs
are more abundant, and these communities are compositionally distinct from those
in the soil between plant canopies [84, 85]. Shrubs in arid lands are often referred to
as “islands of fertility”, as the canopy shades the soil, reducing evaporation and pro-
viding carbon and nutrients through the root exudates and litter production [86–89].
Even in drylands that are sparse in vegetation, hypolithic (under rock) soil communi-
ties are more diverse and have higher absolute abundance than exposed soils [90, 91].
Furthermore, soil characteristics also significantly affect the composition of below-
ground communities. For example, the bacterial and archaeal communities in soils of
the Colorado Plateau of Utah were strongly structured based on the parent material
of the soil [26], showing the importance of edaphic conditions in affecting commu-
nity composition. Similarly, the clay content of soils was found to be as large a factor
in structuring microbial communities as average rainfall in sites in South Africa [92].
Thus, the patchy, heterogeneous distribution of soil resources and habitats, as well as
soil characteristics, largely influence indigenous soil communities.
Microbial biomass is the most widely examined soil biotic response to changes
in precipitation [93]. For example, an aridity gradient in the Mongolian Steppe dis-
played the lowest microbial abundance at the driest sites, and a water addition of
30% of the mean annual amount increased the total soil microbial biomass, suggest-
ing that precipitation was a significant factor limiting soil biomass growth and main-
tenance [94]. However, the microbial biomass following this water addition was still
25–40% lower than at a site that naturally received a similar amount of precipitation
as the water addition plots, suggesting the involvement of other environmental pa-
rameters and site characteristics in controlling soil microbial abundance. Similarly,
bacterial biomass significantly declined with decreasing precipitation in the Tibetan
Plateau [95]. In fact, a meta-analysis of microbial biomass across approximately 400
sites consistently found microbial biomass was lowest in the most arid soils [96]. How-
ever, exceptions to this pattern have been observed. In the Negev Desert, microbial

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biomass under shrubs, as assessed by phospholipid fatty acid analysis, was similar
between semiarid and arid sites. These results, indicating aridity did not exert a sig-
nificant effect on soil microbial biomass [97], highlight the importance of refuge sites
and, potentially, edaphic controls in arid soils. Overall, the general trends support
the idea that increased aridity will plausibly lead to decreased soil microbial biomass,
though this remains to be tested experimentally.
While the microbial biomass of soils is susceptible to altered amounts of precip-
itation, the diversity of soil microbial communities often remains unaffected. Several
studies have documented similar diversity of the bacterial and archaeal communities
in the wettest and driest sites along precipitation gradients [87, 98, 99]. It is important
to note that diversity represents species richness and not the composition in terms of
relative abundance. The composition of microbial communities is generally different
between wet and dry sites or in soils with different historical legacies of precipita-
tion [100–102]. Though many studies of dryland soil microbial community response
to variation in soil moisture were conducted with relatively coarse DNA fingerprint-
ing techniques (e.g., terminal restriction fragment length polymorphism), there is a
growing body of research utilizing high throughput sequencing, which allows for a
closer examination of microbial taxa (e.g., [103–105]). At a more global scale, desert
soil communities showed a very high level of stochastic assembly, generally being in-
distinguishable from random, with the only large predictor of desert soil communities
being the high relative abundance of cyanobacteria [106]. Presumably, the high abun-
dance of cyanobacteria is driven by low vegetation cover, which allows cyanobacteria
to act as key primary producers [107, 108]. In contrast to bacteria, cultivable fungi
were less diverse with lower rainfall in Negev Desert sites [109], as well as along a pre-
cipitation gradient in the Northeast of China [110]. Additionally, bacterial and fungal
communities showed a differential response to monsoon precipitation in a semiarid
grassland in northern Arizona [103]. Studies such as these suggest the potential for
different functional groups to be differentially impacted by changes in soil moisture,
and highlight the need to expand our studies to explicitly consider specific soil pop-
ulations and functional groups in an effort to create comprehensive species catalogs
and predictive models. In addition to assessment of how altered precipitation affects
soil community composition and structure, the exploration of how these changes in
soil microbial community composition affect soil ecosystem functioning represents a
critical area of research.
While the data are focused on handful of well studied sites, several studies have
found potential changes in soil function associated with reduced precipitation. For
example, multiple studies have documented soil carbon and nitrogen decreases with
reductions in precipitation [111–113]. However, along a precipitation gradient among
semiarid and arid grasslands in Oklahoma, USA, soil patches in the vicinity of the
grasses had similar carbon and nitrogen levels along the gradient. It was hypothesized
this was at least partially due to slow litter decomposition in the drier sites compensat-
ing for higher productivity in the wetter sites [114]. In this sense, local features may be

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dominant determinants of soil functions and fertility in drylands. In fact, decreased

precipitation has also been associated with increased patchiness in the distribution
of carbon, nitrogen, and other nutrients across dryland landscapes [115]. Thus, while
climate factors such as mean annual precipitation will be altered at regional scales,
understanding the response of arid soil microbial communities will require forecast-
ing those effects at local, habitat specific scales.
8.4.2 Precipitation Manipulation Studies
In contrast to studies utilizing monsoonal moisture or precipitation gradients, sev-

eral field and laboratory studies have employed precipitation manipulation exper-
iments to explore the effects of altered rainfall on dryland soil communities [116].
Laboratory based manipulations designed to maintain an absolute amount of mois-
ture, but delivered in normal periodicity vs. the same amount of water delivered in
50% more events (i.e., small frequent events), tested altered timing of precipitation
on dryland soil communities [117]. Increases in the frequency of precipitation reduced
cyanobacterial abundance, photosynthetic efficiency, and nitrogenase activity [117].
These data support the framework suggesting that, beyond simply considering the
absolute amount of precipitation, predicting the performance of dryland communities
will require considerations of the timing, periodicity, and duration of soil moisture.
A field manipulation experiment on the Colorado Plateau increased the frequency
of small (1.2 mm) summer monsoon rainfall events, and the treatment had strong neg-
ative effects on soil communities [118]. Moss cover in the soils was reduced from ap-
proximately 25% to < 2% in a single year [77], and no recovery has occurred in over
a decade [51, 55]. In the second year of the same experiment, cyanobacterial relative
abundance was also reduced by 75–95% [119]. However, after a decade of consistent
wetting treatment, the cyanobacterial relative abundance had begun to recover. In-
terestingly, the recovering community does not resemble the well-developed crusts
in the control plots [55]. Taken together, these studies support the idea that altering
the frequency of rainfall events, even when the net effect is to increase the amount of
precipitation, can detrimentally affect dryland soil communities.
Soil fauna directly (through consumption) and indirectly (through nutrient dy-
namics) influences microbial activity, abundance, and turnover [120, 121]. Yet, few
studies consider how altered precipitation regimes will impact soil invertebrate com-
munities and associated trophic interactions. Some soil faunas, including nematodes
and collembola, are able capable of anhydrobiosis, a strategy which allows them to
survive in a dehydrated state [122]. In response to simulated rainfall treatments in a
Chihuahua Desert shrubland experiment, a rapid transition from the anhydrobiotic
condition to the active form was observed, and nematode grazing on bacteria and
fungi appeared to be a short lived process stimulated by rainfall [123, 124]. Signifi-
cant increases in both the numbers and diversity of microarthropods in surface litter

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were also documented [123]. A subsequent study showed that soil water amendments
(6 mm and 25 mm monthly events) had no significant effects on nematode density,
though moisture induced activity was greatest in soils experiencing the larger monthly
irrigation [125]. A meta-analysis on the impacts of invertebrate grazers and predators
on plant productivity and microbial biomass found that an increase in the biomass
of soil fauna led to a 35% increase in aboveground productivity across a variety of
ecosystems, and an 8% decrease in microbial biomass [126]. As interactions among
soil communities and abiotic factors such as moisture and temperature have the ca-
pacity to influence nutrient flow and the functioning of ecosystems, future research
addressing how global change factors will affect these interactions would be invalu-
able [127].
The proposed physiological reasons behind the decline in arid soil organisms un-
der small precipitation events, the “pulse reserve” conceptual model, first proposed
by Noy-Meir [11], has been described as “one of the most-cited paradigms in aridland
ecology” [74]. Although the heuristic perspective was developed for vegetation, the
model appears to also relate to responses of soil biota to discrete wetting events [12].
Essentially, the pulse reserve model proposes that each precipitation event triggers a
pulse of growth that generates reserves that carry the organism until the next event
(assuming resources were gained). The response of soil communities to a precipitation
pulse is hierarchically organized by the threshold response of different organisms to
water availability. A small precipitation event will trigger a response in those organ-
isms with lower water requirements, whereas larger precipitation events will stimu-
late a full response of the community. For example, a 2 mm precipitation event may
induce the activity of respiratory soil microorganisms, whereas net carbon fixation
by plants or biological soil crusts generally requires more sustained and/or deeper
wetting [75, 128]. At the highest levels, a pulse of 25 mm may be required for the germi-
nation of plant seeds [129]. There is also a temporal aspect to this response. Microbes
respond to water pulses in the scale of minutes to hours, whereas vascular plants take
hours to days [130]. In this respect, from the microbial perspective there are critical
measures to any precipitation event, and there could be a strong temporal decoupling
between times of vascular plant vs. biological soil crust vs. soil microbial activity. For
each group, precipitation must be in a sufficient amount to initiate a biological re-
sponse and must be present for a suitable time in order to allow for the buildup of ad-
equate reserves, and the source and timing of that precipitation can vary. A schematic
diagram of the pulse reserve paradigm is presented in 󳶳 Fig. 8.2. With this in mind,
it was recently proposed that the traditional pulse reserve framework should be ex-
panded to incorporate the full suite of biotic responses to precipitation [93], and the
paradigm itself could vary across biotic and abiotic gradients.
Experimental evidence for this model has been observed in desert mosses. The
moss Syntrichia caninervis is common and widespread in many drylands [131]. Un-
der laboratory conditions, the carbon balance of the moss was assayed in response to
simulated precipitation events. Rainfall event size was the largest predictor of the car-

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8.5 Interactions Between Temperature and Soil Moisture | 149
Precipitation Precipitation
event event
Photosynthesis > Photosynthesis >

respiration respiration
Soil moisture
Soil moisture
Net carbon uptake
it
e fic
it
ond e fic Net carbon uptake
rb nd
Ca Respiration > rb
o
Ca Respiration >
photosynthesis photosynthesis
(a) Time → (b) Time →
Fig. 8.2: The pulse reserve deficit model of arid soil activity for photosynthetic organisms. (a) pre-
cipitation event results in an increase in soil moisture, which then declines over time (blue line).
After the precipitation event, the photosynthetic soil populations initiate respiration to repair cell
damage and synthesize photosynthesis proteins, and respiration rates are larger than those of pho-
tosynthesis. During this period the cells experience a carbon deficit. If the precipitation event is of
sufficient amount and duration, net photosynthesis occurs (i.e., photosynthesis rates are larger than
those of respiration, and the organisms achieve net carbon uptake; a). If the precipitation event is
not sufficient to initiate net photosynthesis, net carbon deficit occurs (b).
bon balance of the moss, with negative carbon balance developing under the smallest
precipitation events [132]. Negative carbon balances in biocrusted soils were also ob-
served with small wet up events, as seen by an hourly autochamber assessment of
net CO2 exchange for 1 year and 7 months on the Colorado Plateau [133]. The obser-
vation of “puffs” of CO2 loss co-occurring with natural small precipitation events is
consistent with the mechanism of moss death described in Reed et al. [77], in which
mosses repeatedly experienced net carbon loss when subjected to small artificial pre-
cipitation events. Furthermore, a separate S. caninervis study suggested that increas-
ing the length of desiccation periods between wetting events further increased car-
bon losses, indicating a greater energetic cost of building carbon reserves for long dry
periods [132]. Presumably a similar mechanism could also account for the decline of
cyanobacteria in field manipulations [55], although this lacks experimental verifica-
tion.
8.5 Interactions Between Temperature and Soil Moisture
Temperature is a strong driver of evaporation from soils. A 1°C increase in tempera-

ture can be roughly equivalent to a 3–5% reduction in precipitation due to increased
evaporation [134]. Additionally, soil moisture may also be significantly altered if ele-

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vated temperatures shift the composition of winter precipitation from snow to rain or
alter the timing of winter snow melt [75, 135]. Thus, increasing temperatures have the
potential to increase the AI of soils by driving increased evaporation and altering the
form and duration of water pulses on the landscape. In this respect, relatively moder-
ate increases in temperature have the potential to restructure arid soil communities by
altering water availability. This suggests that the interaction between temperature and
soil moisture will likely be key to understanding the response of arid soil ecosystems to
climate warming. To explore the interaction between temperature and precipitation,
multifactorial experiments performed on the Colorado Plateau investigated the effects
of warming (2–4°C surface warming), altered precipitation (additional 1.2 mm addi-
tions), and a combination of warming and altered precipitation [51, 55, 77, 119]. In gen-
eral, warming had little effect on soil bacteria (but see [51]), whereas altered precipita-
tion in combination with warming caused a collapse of the surface soil communities.
Soils under the combinatorial treatment experienced a reduction in moss and lichen
cover of > 80% and a decrease in cyanobacterial relative abundance of > 90% [51, 55].
Clearly, the interaction between warming and altered precipitation drove the soil com-
munities to a state that would not have been predicted from warming alone. These
small water pulses, although increasing the total amount of precipitation, were pre-
sumably offset by increased evaporation induced by the warming. Hence, these obser-
vations support the a framework for an integrated water driven carbon budget and a
pulse reserve model (󳶳 Fig. 8.2; [128]) and join with field data to suggest that small wa-
ter pulses insufficient to induce net carbon fixation can ultimately lead to the collapse
of some arid soil communities [55]. Due to the drying effects of warming and to physio-
logical interactions between temperature and activity during wet phases, these effects
are likely to be amplified in a warmer climate where soil evaporation is heightened.
8.6 Conclusion
Taken together, the studies synthesized here support the idea that the biology of arid
soils is primarily driven by water availability, and that climate factors associated with
controlling soil moisture play the largest role in structuring arid communities. For ex-
ample, the effect of climate change drivers such as elevated atmospheric CO2 is inti-
mately linked to moisture availability, such that CO2 ’s stimulatory effect can be deter-
mined by soil moisture, and CO2 effects on moisture can be a significant indirect con-
trol over arid soil community composition and function. As soils become drier along
a precipitation gradient, there is a generalized reduction in microbial biomass, and
community composition shifts toward desiccation adapted organisms, with cyanobac-
teria often being the dominant source of primary productivity [108, 136]. This reshap-
ing of the soil communities is associated with lowered productivity and rates of nutri-
ent cycling, which can act to reinforce the patchiness of soil resources [37]. In effect,
dryland soil mosses and bacteria respond to reduced moisture in a similar fashion to

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References | 151
plants and macrofauna, with the exception of microbial biodiversity: arid soils may
act as a cradle supporting diverse microbial seed banks [100]. The strong interaction
between warmer temperatures and increased evaporation from the landscape indi-
cates that any precipitation gains from climate change and associated alterations to
the hydrological cycle could be offset by increases in evapotranspiration.
Precipitation in drylands occurs in distinct pulses that are often short with long
dry periods in between, and thus predicting the response of arid soil organisms to cli-
mate change requires accurate forecasts of how these precipitation pulses will man-
ifest. In this context, it may be important to consider precipitation patterns at much
finer temporal scales than mean annual precipitation, as the frequency and size of
pulses can be a strong determinant of ecosystem communities and their physiology
(and changes in function can observed without concomitant changes in community).
The high uncertainty around forecasting precipitation events at the spatial and tem-
poral scales relevant to belowground biota, as well as considerable knowledge gaps
in specific organismal responses to precipitation pulses, severely limits our ability to
predict the fate of arid soil communities. Even so, experimental data suggest that pre-
cipitation and temperature changes within the range predicted to occur over the next
decades should be sufficient to significantly impact soil biology and associated bio-
geochemical cycling [55, 77]. In general, desert lichens and mosses appear to be more
sensitive to these changes than other soil biota, such as cyanobacteria [77]. In this re-
gard, those sensitive community members may be important species to monitor under
a changing climate. Maintenance of dryland soil function will require a collaborative
effort among climate scientists, biologists, and land managers, as well as an improved
understanding of how different biotic and abiotic factors interact to regulate function.
Acknowledgment: The authors are grateful to Anthony Darrouzet-Nardi and Rebecca

Mueller for excellent suggestions on a previous version of the manuscript that im-
proved the chapter. The synthesis provided here was supported by the USDA National
Institute of Food and Agriculture, Hatch project 1006211, the US Department of En-
ergy Office of Science (Award Number DE-SC-0008168), and the US Geological Survey
Ecosystems Mission Area. TAM was supported by a National Science Foundation Post-
doctoral Research Fellowship in Biology under Grant No. 1402451. Any use of trade,
firm, or product names is for descriptive purposes only and does not imply endorse-
ment by the US government.
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Doreen Babin, Michael Hemkemeyer, Geertje J. Pronk,
Ingrid Kögel-Knabner, Christoph C. Tebbe, and Kornelia Smalla
9 Artificial Soils as Tools for Microbial Ecology
9.1 Introduction
Soils are not only regarded as black box due to their opaque nature but also because
they are among the most complex biomaterials on earth [1, 2]. Looking closer into soils
one can find heterogeneous compounds of different origins, various sizes, and proper-
ties. Due to interactions between these compounds, an aggregated three-dimensional
structure arises pervaded by a porous network offering various niches for microbial
colonization. Therefore, it is not surprising that the soil microbiota also exhibits huge
diversity [3]. This soil complexity still challenges soil science and impedes a better
understanding of soil microbial communities and their interactions with the natural
soil environment. From the researcher’s point of view, soils, unfortunately, never only
differ in one single property due to, e.g., different parental rock materials, climatic con-
ditions, or land use. These different factors hinder the comparison of soils and make it
impossible to ultimately clarify causal relationships. Consequently, only carefully de-
signed experiments with reduced natural soil complexity can deliver reliable answers
to soil microbial ecology and go beyond a solely descriptive character [3]. Schreiter
and colleagues recently published a series of experiments running in an experimen-
tal plot system with three soils of different origin (diluvial sand, alluvial loam, loess
loam) stored for 10 years at the same site and with the same cropping history [4–6].
Thereby, the authors could evaluate to which extent soil properties drive the micro-
bial community composition in the bulk soil and rhizosphere under field conditions,
excluding factors like soil management, climate, or cropping history. However, to dis-
entangle the effect of a particular soil parameter, for instance the influence of organic
matter (OM), specific minerals, soil texture, or water potential on the microbiota, it
seems reasonable to focus on model systems rather than on “natural” soils, which
have this immense heterogeneity [3, 7]. 󳶳 Fig. 9.1 shows experimental model systems
used in soil science to enable an understanding of soil processes at different explana-
tory levels by varying the degree of complexity.
In order to gain a mechanistic understanding of interactions between soil miner-
als and microorganisms, highly simplified experimental designs decoupled from the
soil system have been used by numerous studies in the past, providing insights into
the influence of clay minerals, e.g., on microbial growth, metabolism, survival, bio-
chemical activity, and genetic transfer [1, 8–11]. Porous media or so-called transpar-
ent soils offering soil-like physicochemical characteristics are used as a suitable tool
for visualization of colloids within the soil structure [12] or of the rhizosphere and its
DOI 10.1515/9783110419047-009
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160 | 9 Artificial Soils as Tools for Microbial Ecology
Complexity
Simplification
No Soil Porous Media Artificial Soils Arid Soils Non-Arid Soils

Interaction studies Only mineral Soil-like Natural soils Natural soils, e.g.,
between microbiota particles Incubation/ Water-deficient grassland,
and clean soil Soil-like matrix maturation Low OM content forest, mesic,
components and physico- Aggregated tropical soils
Artificial media for chemical properties structure Offer full
cultivation Reproducible complexity
Descriptive
studies
Sterile Soils
Soil-like
Incubation/maturation
Aggregated structure
Fig. 9.1: Schematic diagram of types of soil experiments.
associated microbiome [13]. In contrast, microcosm experiments with sterilized soils

exhibit a much higher soil-like complexity (󳶳 Fig. 9.1). By setting up different matric
potentials in sterilized soils, Wright et al. [14], for instance, showed that pore sizes are
an important determinant for bacterial protection against predators. Soil sterilization
can be also a useful method for soil microbial ecology studies by inoculation of a de-
fined microbial consortium and by tracking its development and activity in an almost
natural soil environment [15–17]. If the focus is, however, to unravel the impact of a
certain parameter within a soil-like system, then artificial soils are regarded as a good
tool allowing us to specifically manipulate the soil composition in a reproducible way
(󳶳 Fig. 9.1). As inferred from the name, artificial or synthetic soils are designed with
known composition. In comparison to commercially available artificial soil products
for gardening, artificial soils for research purposes have the advantage of being cre-
ated under controlled laboratory conditions. The aim of this chapter is to show how
earlier and recent artificial soil experiments contributed to the understanding of soil
microbial communities and how this can be linked to arid soil research.
9.2 Soil Definition
The Soil Science Society of America defines soil as “the unconsolidated mineral or or-
ganic material on the immediate surface of the earth that serves as a natural medium
for the growth of land plants” [18]. The growth of plants in soil is made possible by the
different soil components and their interactions. The principal soil constituents are
minerals, water, gases and soil organic matter (SOM) including the living soil biota.

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9.2 Soil Definition | 161
The portion of each constituent can vary considerably between different soils depend-
ing on, e.g., the soil type, climate, and vegetation. In terms of plant growth, ideal num-
bers were estimated to be 45% (wt/wt) minerals, 25% water, 25% air, and 5% SOM [19].
In contrast to other habitats colonized by microorganisms, soils are dominated by
solid compounds that differ in their chemical composition (mineralogy), depending
on parental rock material and their particle size. Clay-sized particles (< 2 μm) like clay
minerals (e.g., illite, montmorillonite, kaolinite) and metal oxides (e.g., derived from
Fe, Al, Mn), as a product of mineral weathering, might be of special importance for
microorganisms since they offer a high surface area for interaction [20, 21].
Besides inorganic constituents, soils contain residues from plants, animals, de-
caying roots and microorganisms, synthesized biopolymers, humidified substances,
and the living soil biota (edaphon), which together contribute to SOM [22]. Black car-
bon or charcoal is another common component in soils that accumulated over hun-
dreds of years due to pyrolysis of organic materials. The nonliving SOM provides a
matrix for microbial cell attachments and colonization and can also serve as an en-
ergy and nutrient source for the soil microbiota. The metabolic activity of soil bacte-
ria, which are essentially aquatic organisms, is, however, restricted to the water layers
adhering to soil particles or to water filled pores. Instead of living planktonically, most
bacterial cells likely reside in unsaturated soils at the solid–liquid interface embedded
in extracellular polymeric substances (EPS) protected against, e.g., desiccation [3, 23].
Transport of bacterial cells and nutrients as well as gaseous fluxes depends on the
soil water content and, therefore, water-deficiency as present in arid soils is a severe
environmental stress factor for most soil bacteria [23]. An exception are filamentous
bacteria and fungi that are less dependent on the presence of water thanks to their
hyphal growth allowing air-filled pores to be bridged [24]. The soil water content also
influences the connectivity of microbial habitats and the opportunity for microbial in-
teractions and colonization of new surfaces. Therefore, the important role of water
on diversity and structuring of microbial communities must be kept in mind [23, 25–
27].
Soils exhibit a high abundance of microorganisms and a tremendous microbial
diversity [2, 28]. Just 1 g of soil harbors several kilometers of fungal hyphae and pro-
vides space for ca. 1010 bacterial and archaeal cells [29, 30]. However, related to the
surfaces available, soils are still scarcely inhabited, and microorganisms typically oc-
cur concentrated as hotspots (similar to the earth’s colonization by humans). These
hotspots are a direct consequence of the interaction and clustering of different soil
constituents resulting in the formation of soil aggregates with large biogeochemical in-
terfaces (BGIs) [31]. The three-dimensional soil structure is, therefore, a self-organized
system under active contribution of microorganisms due to the gluing properties of
EPS and hyphal growth [2].

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9.3 History of Artificial Soil Experiments
Research in the early 20th century already indicated that soil microorganisms essen-
tially depend on the conditions provided by their immediate natural environment [32–
35]. Thus, the hitherto common practice of performing experiments with soil microor-
ganisms after growing them on artificial media to cell concentrations much above
those that would be present in a soil seemed to fully ignore the structural, nutritional,
and compositional complexity present in natural soils. Rahn [32] compared the bac-
terial activity in solution, in soil, and in sand, and found that nutrient absorption in
sand, aeration, and thickness of the moisture film around soil particles are all criti-
cal factors influencing bacterial activity. Söhngen [34] pointed out the importance of
soil colloids that absorb mineral nutrients and condense surface gases [36]. These re-
sults demonstrated the pitfalls of cultivation-dependent studies and cleared the way
to looking for new methods for studying soil bacteria and their processes. The soil
process mediated by microorganisms that received the main focus at that time was
the cycling of nitrogen. While Löhnis and Green [37] used nutrient solutions based
on soil extracts for physiological tests, others tried to study nitrification directly by
soil incubation studies [33]. According to Allen and Bonazzi [36], both methods had
their limitations. These authors worked with soils of reduced complexity in which the
OM was destroyed by ignition and concluded that “soil as a medium possesses the
property of supporting nitrification better than sand” [36]. However, the reason at that
time remained obscure. The authors, in fact, suggested that probably only building
up a close-to-natural soil environment, i.e., a synthetic soil, would give detailed in-
sights into soil processes. However, the first attempt of Stevens and Withers [33] to
construct a universal standardized artificial soil medium of high nitrifying capacity
failed. There were also early attempts to reduce soil complexity by adding a defined
inoculant to previously sterilized soils to subsequently monitor the decomposition of
an added substrate [33, 38].
Several years elapsed in which tremendous work was done to visualize soil bac-
teria in situ by applying different staining techniques [39–41], but the success was
limited and the understanding of interactions between microorganisms and the soil
matrix was still barely possible. In 1937, Madhok [42, 43] again proposed the design
of defined synthetic soil compositions under laboratory conditions for studying mi-
crobiological soil processes (e.g., cellulose decomposition, nitrification, and nitrogen
fixation). These first synthetic soils were composed of different mixtures of sand, ben-
tonite, and humus, inoculated with a suspension obtained from a “good field soil” [42].
Martin and Waksman [44] used the artificial soil media proposed by Madhok [42] to
study the binding and aggregating effects of microorganisms on soil particles. Their
studies with sand-bentonite and sand-clay mixtures inoculated with different pure
and mixed cultures of microorganisms and addition of different types of OM in com-
parison to similarly treated natural soils contributed considerably to the understand-
ing of the soil aggregation process. Likewise, Conn and Conn [45] followed the sug-

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9.3 History of Artificial Soil Experiments | 163
gestions by Madhok [42] and composed a synthetic soil of sand and different mixtures
varying in type and amount of colloids in order to create a suitable culture medium
for soil bacteria. They found that colloids (e.g., bentonite) improved sand as a growth
medium for different inoculated bacterial strains and developed a recipe for a syn-
thetic soil. Due to the use of defined soil compositions, these authors came to the con-
clusion that colloids are important for soil bacteria, probably by serving as a carrier
of, e.g., Mg2+ , Ca2+ , and K+ and as a sorbent of harmful byproducts [45].
In the 1950s and 1960s, experimental pedology became popular, which is defined
as the realization of controlled experiments to study pedogenic processes [46]. In this
respect, microcosm experiments with artificial soils were also used, but most exper-
iments at that time focused on the study of abiotic soil forming processes (this is re-
viewed in [47]). Exceptions were studies of the role of the water content on bacterial
movements in soil using simplified porous media [48–50].
Recently, artificial soils became an important tool for analyzing the establishment
and functioning of soil microbial communities. Ellis [51] developed a protocol for an ar-
tificial soil with essential components of a natural soil but with reduced heterogeneity.
This protocol was later improved by Guenet et al. [7], who proposed it as a suitable tool
for studying soil microbial processes. Zhang et al. [52] used artificial soils incubated
for several months to understand the temperature sensitivity of SOM decomposition,
focusing therein on the effect of its chemical recalcitrance and the soil clay mineral
composition. Based on the assumption that the supply of a mineral phase, a source
of OM, and a microbial community provides all the essential ingredients to form a
soil-like material, Pronk et al. [53] designed eight different artificial soils (󳶳 Fig. 9.2).
These were composed of different mixtures of the minerals illite, montmorillonite, fer-
rihydrite and boehmite, and charcoal. Sand- and silt-sized quartz were used to provide
texture, sterilized manure was added as a substrate, and the mixtures were inoculated
with an extract from a natural arable soil.
These artificial soils were analyzed in a multidisciplinary approach in order to
study the initial formation of BGIs in soil as a function of the type of particle surfaces
present. The artificial soil mixtures differed in complexity and mineral composition
and were incubated over 18 months in the dark at 20°C on average and a constant wa-
ter content of 60% of the maximum water holding capacity. Pronk et al. [53] detected
a fast development of these artificial soils to soil-like, aggregated systems and showed
the importance of clay mineral presence for macroaggregate formation. In contrast to
their expectations, microaggregation was similar among soils independently of the
presence and type of clay minerals, metal oxides, or charcoal. The authors suggested
that development of their artificial soils was not fully completed after 18 months of
incubation and that the stability of the systems declined as a consequence of missing
fresh OM input [53]. Therefore, Vogel et al. [54] started a follow-up experiment with
five of these artificial soil mixtures and incubated them for 842 days after they had
received a fresh sterile manure addition 562 days after inoculation. The fresh OM sup-
plied allowed reactivation of the system, resulting in a re-formation of macroaggre-

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Fig. 9.2: Dry model minerals and sterile manure used

by Pronk et al. [53] to compose artificial soils.
gates. These results demonstrated the importance of a continuous OM supply for the
formation of soil macroaggregates and indicated their dynamic nature in the absence
of protective roots [54]. By a 16S rRNA gene based analysis of the microbial commu-
nity structure and OM turnover, the authors concluded that mainly clay minerals are
the long-term driver of the soil microbiota and its microhabitats. The artificial soil ex-
periments carried out by Pronk et al. [53] and Vogel et al. [54] within the framework of
the Priority Program SPP1315 of the Deutsche Forschungsgemeinschaft (DFG) were ac-
companied by various microbiological analyses (󳶳 Tab. 9.1). These recent results and
the results from other microbial ecology studies using artificial soils or simplified soil
microcosms as a tool to better understand soil microbial communities and their shap-
ing factors are reported below (󳶳 Tab. 9.2).
9.4 Methods in Soil Microbial Ecology and Soil Science
New insights into soil science and soil microbiology depend on technical progress,
which increases our capacity to handle the opaque nature of soil, its complicated

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9.4 Methods in Soil Microbial Ecology and Soil Science | 165
three-dimensional arrangement, and the microbial inhabitants that are not visible to
the naked eye. The beginnings of soil microbiology were solely based on cultivation
techniques and, as outlined above, many different attempts were made to mimic the
natural soil environment in the laboratory. However, even with improved growth me-
dia and cultivation conditions, only a small fraction of the soil microbial community
can be cultivated (approximately 0.3%) [55]. The advent of molecular techniques in
microbial ecology promoted the understanding of the structural and functional di-
versity of soil microbial communities. The extraction of nucleic acids directly from
the soil matrix or after obtaining the microbial fraction opened new opportunities to
study soil microorganisms independently of cultivation [56]. Possessing highly con-
served and variable regions that allow drawing conclusions on taxonomy, the 16S
rRNA gene coding for the small subunit of the ribosomal RNA was established as
broad phylogenetic marker for bacteria and archaea [57]. Over the years, a large refer-
ence database emerged that to date contains more than 4.3 million rRNA sequences
(www.arb-silva.de) [58]. The internal transcribed spacer (ITS) region between the 18S
rRNA and 28S rRNA genes was found to be more useful for studying fungal diversity
and abundance [59]. Quantitative real time PCR (qPCR) allows estimating the amount
of soil microorganisms based on marker gene copy numbers per gram of soil. Alterna-
tively, the analysis of phospholipid fatty acids (PLFA) presents a well established tool
to quantify bacterial and fungal biomass in soil [60]. The soil microbial community
structure can be profiled (molecular fingerprint) by different techniques, such as ter-
minal restriction fragment length polymorphism (T-RFLP), or denaturing gradient gel
electrophoresis (DGGE) based on amplified 16S rRNA gene or ITS fragments [59, 61].
All these techniques are based on the electrophoretic separation of the marker gene
amplicons according to differences in their DNA sequence. They brought about great
progress, since for the first time a relatively large dataset could be profiled within a few
days, allowing the detection and preliminary identification of microbial responders to
treatments and also, by the use of an appropriate number of independent replicates, a
subsequent statistical analysis of microbial community changes. The effect of a better
taxonomic information content associated with constantly falling sequencing costs is
that high-throughput next-generation sequencing techniques are nowadays preferred
to nonsequencing methods for studying soil microbial community compositions, e.g.,
pyrosequencing or Illumina MiSeq. Besides the usage of these phylogenetic markers,
the detection of functional genes can show potential metabolic pathways of a commu-
nity and indicate microbial guilds, while enzyme activity assays are a tool to determine
active functions [62, 63].
Soil microbial ecology aims at studying the interactions between soil microorgan-
isms and their soil environment. Apart from the selection of tools to study soil micro-
bial communities, the soil sampling procedure is also of importance. As outlined in
the beginning of this book chapter, soils provide various niches for microbial colo-
nization. In most ecological studies, soil samples are randomly collected and mixed,
resulting in the destruction of soil aggregates and, therefore, in an immense loss of

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information on microbial habitats. Attention is no longer paid to distances for mi-

crobial interaction, nutrient accessibility, or protective habitats [64]. As thoroughly
reviewed by Vos et al. [3], a greater effort should be made to look at soils as a habi-
tat from the perspective of single bacterial cells. Separating soils into different parti-
cle size fractions before total community-DNA extraction can be a suitable method to
study the diversity and metabolic activity of particle associated microbial communi-
ties and thus to better understand soil functioning [3, 65]. Using particle size fraction-
ation, Jocteur Monrozier et al. [66] showed highest microbial biomass carbon in small
size fractions (< 20 μm), and Sessitsch et al. [67] additionally found that different par-
ticle size classes exhibit differences in community composition. Furthermore, by mild
ultrasonication and wet-sieving Neumann et al. [68] showed particle size-specific re-
sponses of microbial communities to long-term fertilization, including input of OM.
New ecological insights are also coupled with the progress in soil science. Ad-
vances of microscopic and spectroscopic techniques that are capable of characterizing
soil particles at the submicron scale may allow for the characterization of habitats at
scales directly relevant for microbes. For example, secondary ion mass spectrometry
at the nanoscale (NanoSIMS) is promising in terms of giving new insights into the
small-scale soil component arrangement. With NanoSIMS it is possible to analyze the
elemental and isotopic composition of a solid sample with high sensitivity at a sub-
micron scale in situ, meaning without disturbing the soil structure [69, 70]. Heister
et al. [70] found a patchy arrangement of organic material in incubated artificial soils
on clay mineral surfaces. The method also allowed differentiating between charcoal
and SOM [70]. By applying NanoSIMS in soil ecology studies, new insights into OM
turnover and spatial distribution as well as microbial residue formation can be gained
and will be presented, among others, hereafter.
9.5 Insights into Microbial Communities from Artificial Soil

Studies
9.5.1 Establishment and Structuring of Soil Microbial Communities
Soil microorganisms are assumed to be architects and actors of BGIs shaping their im-
mediate soil surroundings [31]. Therefore, the study of interface formation from pris-
tine materials in artificial soils by Pronk et al. [53] was accompanied by an analysis
of the microbial community development (󳶳 Tab. 9.1). The artificial soils received an
inoculant obtained by water extraction from a natural soil. It is probable that not all
soil microorganisms could be detached from the soil matrix by this extraction method
and, thus, the inoculant might have exhibited a lower microbial diversity and richness
compared to the natural soil microbial community. Certainly, compared to the natural
colonization of developing soils, which is driven by biocolloid transports in soil or air,
the colonization of artificial soils by inoculation with a microbial community extracted

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from soil is different. Furthermore, the mineral surfaces provided mimicked already
physically and chemically weathered material, and the added OM provided as sterile
manure represented a partially degraded litter, which differs from conditions in na-
ture. The approach by Pronk et al. [53], however, allowed the comparison of microbial
community developments between soils of different mineral compositions, as all soils
received an aliquot of the same inoculant. Ding et al. [71] studied the early bacterial
community establishment in these artificial soils. By DGGE and pyrosequencing anal-
ysis of bacterial 16S rRNA gene fragments amplified from total community-DNA, the
authors showed that bacterial community complexity increased with increasing incu-
bation time. Artificial soils of different mineral composition exhibited similar bacterial
abundances and diversity. However, the bacterial diversity in artificial soils incubated
for 90 days was significantly lower than in the inoculant added to the mixtures at the
incubation start [71]. Obviously, not all bacteria could adapt similarly to the condi-
tions that prevailed at initial BGIs. These findings, therefore, provide insights into the
adaptation and establishment of soil microorganisms at new, pristine surfaces.
Molecular fingerprinting techniques were used to compare the structure of the
bacterial communities established between these different artificial soils. After 90
days of incubation, a strong effect of charcoal and, to a lesser extent, of clay minerals
on the structure of the bacterial community was observed. Metal oxides appeared to
have a weak influence on the betaproteobacterial community. By pyrosequencing,
responders to minerals or charcoal could be identified, and a putative taxonomic
affiliation was possible; among others, Devosia, Rhizobium, and Sphingomonas were
enriched in artificial soils containing charcoal. Positive responders showing an in-
creased relative abundance in the presence of montmorillonite were mainly affiliated
to Gammaproteobacteria and Bacteroidetes, whereas responders to illite were found to
belong to distantly related taxa [71]. Although the resolution level of the 16S rRNA gene
for bacterial identification is limited, information on the phylogenetic and taxonomic
affiliation of responders is still helpful for gaining new insights into the ecological
role of certain bacterial taxa.
Numerous studies carried out previously with clean particles, single bacterial
strains, or addition of minerals to soils reported on direct and indirect influences of
minerals on microbes [1, 8–10, 72]. In a recent review, Uroz et al. [73] even proposed
the term “mineralosphere,” emphasizing that minerals represent a specific micro-
bial habitat. These might be underlying interactions leading to the enrichment or
inhibition of bacterial taxa by minerals and charcoal, as observed in artificial soil
studies [71, 74, 75]. Results from the artificial soil incubation experiment mentioned
above showed for the first time that these microbe-mineral interactions are also im-
portant during early BGI formation and influence the development of soils. Artificial
soils from this study [53] were further incubated, and after 1 year the effect of metal
oxides on Bacteria increased while the influence of charcoal declined, probably due
to occlusion of surfaces by OM [74, 76]. A pronounced influence of clay minerals on
Bacteria and Fungi was still observed [74]. By particle size fractionation, Hemkemeyer

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et al. [77] were able to demonstrate differences between prokaryotic communities liv-
ing attached to the quartz-dominated coarser fractions (20–63 and 63−2000 μm) and
the clay-dominated finest fraction (< 20 μm). In the latter case, the influence of the ar-
tificial soil mineral composition was most pronounced and resulted in different bacte-
rial and archaeal communities. However, Fungi were sensitive to artificial soil mineral
compositions across all particle size fractions. These microbial responses to artificial
soil components were not stable and changed over the incubation time [71, 74, 76, 77],
suggesting changing environmental conditions during ongoing soil formation. Cer-
tainly, soil complexity increases with incubation time, thus offering more discrete
niches for microbial colonization. This development was suggested to contribute to
microbial divergence in soil [76] and helps to understand the tremendous microbial
diversity in soil. In addition, the analysis of abundances of specific bacterial taxa
and activity of enzymes involved in nutrient cycling in those artificial soils indicated
a succession in the microbial community from copiotrophic to oligotrophic lifestyle
likely due to nutrient limitations [78].
Pronk et al. [53] suggested that these artificial soils were still developing even after
1.5 years of incubation. Therefore, Vogel et al. [54] set up another artificial soil exper-
iment based on that by Pronk et al. [53] but with prolonged incubation time and an
additional fresh OM input after 562 days. In comparison to the incubation start, the re-
sponse of microorganisms to the new nutrient source added after 562 days was much
stronger and lasted for a longer time in established systems, as observed by the CO2
respiration rates and the microbial gene abundances measured. This was attributed
to the adaption and establishment of microorganisms in their microhabitat [54]. Af-
ter more than 2 years (842 days) of incubation, artificial soils differing in the type of
clay mineral exhibited significantly different amounts of macroaggregates. In addi-
tion, the microbial community structure differed significantly between soils with illite
from those with montmorillonite [54, 75]. Moreover, clay minerals could be identified
as key drivers of the soil microbiota in the long term in comparison to charcoal and fer-
rihydrite. The effect of charcoal and ferrihydrite was still pronounced after 842 days of
incubation but seemed to be more important for the early microbial community de-
velopment [75]. After long-term incubation of more than 2 years, new discriminative
taxa among artificial soils were found by pyrosequencing analysis compared to the
analysis after 90 days of incubation [71], supporting the concept of dynamic microbial
community establishment [79]. For instance, the actinobacterial genus Rhodococcus
and the alphaproteobacterial genus Filomicrobium were enriched in soils, containing
illite whereas in montmorillonite containing soils a higher relative abundance of Fir-
micutes (e.g., Bacillus, Paenibacillus, Lysinibacillus) was found [79].
The artificial soil studies by Pronk et al. [53] and Vogel et al. [54] showed that mi-
crobial community establishment as a function of surfaces present is not a random
process since highly similar microbial communities were established among indepen-
dent replicates of artificial soil mixtures [71, 74, 75]. Furthermore, the experimental
setup of an independent artificial soil experiment with extended incubation time and

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a different microbial inoculant [54] showed reproducible results in terms of microbial

community establishment, CO2 respiration, and OM development.
Insights into microbial community establishment and structuring by means of
artificial soils that were gained within the framework of the DFG Priority Program
SPP1315 are summarized in 󳶳 Tab. 9.1.
An independent study with simplified soils was conducted by Wolf et al. [26], who
aimed at understanding soil microbial interactions and diversity development. The
authors focused on the effect of the matric potential and pore size distribution on bac-
terial growth in soil. Therefore, quartz sand microcosms differing in their hydraulic
properties were inoculated with a nonfilamentous (Bacillus weihenstephanensis) and
a filamentous bacterial strain (Streptomyces atratus). These simplified artificial soils
revealed that filamentous bacteria had a selective advantage in soils with low connec-
tivity [26]. In a similar study, Treves et al. [27] explored the effect of spatial isolation
created by varied moisture content on competitive dynamics of two bacterial species
growing on a single nutrient source (2,4-dichlorophenoxyacetic acid) in a uniform
sand matrix. A low moisture content (high spatial isolation) allowed the less com-
petitive strain to establish, suggesting that the water level in soil matters in terms of
structuring microbial communities [27] (󳶳 Tab. 9.2).
9.5.2 Functioning of Soil Microbial Communities
The analyses of artificial soils composed by Pronk et al. [53] and Vogel et al. [54]
showed the influence of soil minerals and charcoal on the establishment of microbial
communities [71, 74–77]. However, microorganisms in these systems were not only
passive responders to the soil mineral composition since soils were incubated allow-
ing bacteria and fungi to actively colonize and structure the soil system. The higher
macroaggregation in artificial soils containing montmorillonite was explained by Vo-
gel et al. [54] by the presence of a different bacterial community compared to that in
soils containing illite. These bacteria might have differed in their potential to produce
gluing agents such as EPS or in their access to decomposable OM as an indirect con-
sequence of the artificial soil composition [54]. This is supported by results reported
by Ditterich et al. [78] showing that enzyme activities in artificial soils incubated for 6
months depended on the soil composition. Furthermore, by pyrosequencing analysis
of 16S rRNA gene fragments amplified from total community-DNA of artificial soils
incubated for more than 2 years less taxa affiliated to Bacteroidetes were detected
in montmorillonite containing soils that can usually be found in more nutrient-rich
environments due to their copiotrophic lifestyle [79]. In contrast, no differences were
observed in the amount or quality of OM present in soils incubated for 18 months [80]
and artificial soils matured for more than 2 years [54], as well as in the production
of OM in the fine fraction (< 20 μm), which supports the concept of functional re-
dundancy among phylogenetically distant related microbial taxa. The laboratory

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Table 9.1: Artificial soil studies within the framework of the DFG Priority Program on Biogeochemical Interfaces in Soil (SPP1315) focusing on soil microbial
communities.
Publication Aim of Study Factor(s) of Variance Detection Methods Incubation Time Further Information
on Artificial Soils
Vogel et al. Interdisciplinary study of microbial Soil mineral compo- DGGE, qPCR, frac- 842 days (with Vogel et al. [54]
[54] communities, OM decomposition and soil sition and presence tionation, OM char- additional OM input
structure development at matured BGIs of charcoal acterization after 562 days)
Ding et al. Early establishment of soil bacterial Soil mineral compo- 16S DGGE, pyrose- 1, 9, 31, 90 days Pronk et al. [53]
[71] communities at young BGIs sition and presence quencing
of charcoal
Babin et al. Development of soil microbial communities Soil mineral compo- 16S/ITS DGGE, 1 year + 70 days Pronk et al. [53]
[74] and response to phenanthrene at matured sition and presence Southern Blot- phenanthrene
BGIs of charcoal hybridization for
catabolic genes
Babin et al. Development of soil microbial communities Soil mineral compo- 16S/ITS DGGE, 842 days +7, 21, 63 Vogel et al. [54]
[75] and response to phenanthrene at long-term sition and presence qPCR, pyrosequenc- days phenanthrene
matured BGIs of charcoal ing +/- plant litter
Steinbach Establishment of functional soil microbial Soil mineral compo- qPCR, T-RFLP 3 months, Pronk et al. [53]
et al. [76] guilds over maturation time (here: alkane sition and presence 12 months (each
degradation) of charcoal + 2 weeks plant
litter)
Hemkemeyer Establishment of soil microbial diversity in Soil mineral compo- qPCR, T-RFLP, frac- 6 months, Pronk et al. [53]
et al. [77] particle size fractions over maturation time sition tionation 18 months
Ditterich Microbial colonization of soil minerals and Soil mineral compo- qPCR, PLFA, enzyme 3, 6, 12, 18 months Pronk et al. [53]
et al. [78] succession over maturation time sition activity
Pronk et al. Understanding OM turnover and development Soil mineral compo- OM characteriza- 3, 6, 12, 18 months Pronk et al. [54]
[80, 83] over soil incubation time sition and presence tion, fractionation
of charcoal

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Vogel et al. Understanding OM turnover and formation of Soil mineral compo- Fumigation-extrac- 842 days + 63 days Vogel et al. [54]
[85] organo-mineral associations at long-term sition and presence tion, OM characteri- 13 C/15 N labeled
matured BGIs of charcoal zation, fractionation plant litter

Table 9.2: Other artificial soil studies or simplified microcosm experiments focusing on soil micro-
bial communities.
Publication Aim of Study Factor(s) of Detection Methods Incubation

Variance Time
Wolf et al. Understanding bacterial Hydraulic con- Bacterial plating, 12 days

[26] growth dynamics and nectivity of motility rate, water
microbial interactions in microhabitats retention curve
soil
Treves et al. Determining the role of Moisture con- Bacterial plating 7 days
[27] spatial isolation for soil tent
microbial community
structure
Heckman Understanding Oxide surface Nutrient analysis, 5, 10, 20,
et al. [81, organo-mineral-microbe pyrosequencing, 30, 60, 90,
96] relationships soil fractionation, 154 days
X-ray diffraction,
SEM/EDSa
Wei et al. Understanding OM Clay content, Microbial biomass 2 months
[84] decomposition temperature carbon, PLFA pro-
file, enzyme activi-
ties
Wei et al. Understanding the role Temperature Microbial biomass 11 days
[86] of microbial communities carbon, PLFA pro-
in thermal acclimation of file, enzyme activi-
SOM decomposition ties
Lamparter Development of sand pH, microbial C and N measure- 10 days
et al. [87] particle wettability activity ments, contact
during initial BGI angle determination
formation
a
SEM/EDS: scanning electron microscopy/energy dispersive spectroscopy
experiment by Heckman et al. [81] represents a further simplified, artificial soil study
that aimed at understanding the effect of minerals on soluble nutrient dynamics and
the composition of soil microbial communities (󳶳 Tab. 9.2). After inoculation with
its native microbial community, forest floor material was incubated with goethite
and quartz or gibbsite and quartz. The treatments with oxide surfaces exhibited a
different microbiota as observed by pyrosequencing of 16S rRNA gene fragments
amplified from total community-DNA and influenced nutrient content and physico-
chemical properties of water-extractable OM compared to the control that received
only quartz sand. However, on a functional level (OM decomposition) no differences
were observed [81, 82]. This corresponds to the findings of Pronk et al. [80] and Vogel
et al. [54].
As mentioned above, new findings in soil science and microbial ecology are of-
ten driven by technical progress. Thus, the observation of similar OM decomposition

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among different artificial soils might be biased by the detection limit of the method
used. The more advanced analysis of microbial residues (an important component
of SOM) using amino sugars as indicator revealed differences among artificial soils
with different clay minerals present [83]. These differences in OM turnover were likely
caused by the microbial community dynamics over the incubation time rather than
by direct interactions with the minerals [83]. In a different artificial soil experiment
lasting for only 2 months, Wei et al. [84] also observed an effect of clay content on the
OM decomposition rate, microbial biomass, and microbial community composition
(󳶳 Tab. 9.2). Furthermore, after several OM additions to matured artificial soils [54] dif-
ferences in the decomposition rate of labeled litter and microbial biomass were also
observed between soils containing montmorillonite or illite, which was explained by
the different structural development with ongoing soil formation. This indicated OM
stabilization in the fraction of smaller particle size [85]. Additional insights into SOM
dynamics originated from an artificial forest soil study by Wei et al. [86]. In this study,
artificial soils were used to simulate the acclimation of SOM decomposition under con-
trolled laboratory conditions. Therefore, clay, sand, and OM (also a source of microor-
ganisms) were mixed and incubated at different temperatures for 11 days (after 3 days
of preincubation). The authors were able to show that temperature-related shifts in
the structural and functional microbial community composition influenced SOM de-
composition.
These results indicated the active role of soil microorganisms driving nutrient cy-
cling and the structuring of BGIs. The latter fact is supported by a recent artificial soil
percolation experiment conducted by Lamparter et al. [87]. In this study, quartz sand
of different sizes was percolated with a dissolved OM solution of varying pH and with
or without the addition of sodium azide in order to analyze the effect of OM sorption
and microbial activity on particle wettability. By measuring the solid-water contact
angle at the three-phase boundary, the authors suggested a microbial contribution to
a reduction of surface wettability, which directly affects BGI formation [87] (󳶳 Tab. 9.2).
The artificial soil studies by Pronk et al. [53] and Vogel et al. [54] allowed fur-
thermore studying the response of microbial communities and soil interfaces that
established as a function of the soil composition to added compounds (󳶳 Tab. 9.1,
󳶳 Fig. 9.3). This showed that microbial communities thriving in a nutrient-limited
environment with mainly recalcitrant organic compounds left [78] can still rapidly
respond to changing conditions by the selection of specific phenanthrene or litter
degraders after incubation with these amendments [74–76]. The response to phenan-
threne was observed, although the microbial communities that were used to inoculate
the artificial soils of Pronk et al. [53] and Vogel et al. [54] originated from soils with-
out any history of organic contamination. With artificial soil maturation time, the
microbial communities increasingly diverged, but a similar response to the addition
of plant litter in terms of microbial guilds was observed in artificial soils matured for
3 and 12 months. Therefore, the authors concluded that the alkane degrader commu-
nity can be reactivated under favorable conditions [76]. Altogether, this supports the

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Fig. 9.3: Spiking experiment conducted by Babin et al. [75] on artificial soils matured for more than
2 years.
idea of “everything is everywhere but the environment selects”, and thus by artificial
soil studies new arguments can be brought into the ongoing debate of the ecological
concept [88]. These artificial soil studies provide an explanation for the resilience of
soil functions under changing environmental conditions by allowing the existence of
microorganisms with specific metabolic capacities at low densities.
Various spiking experiments on differently matured artificial soils [74–76] further-
more showed that the soil composition controlled the microbial response to spikes
and, therefore, likely the functionality of established interfaces and microbial com-
munities. Less response of bacterial communities to phenanthrene was observed in
soils containing charcoal and montmorillonite, which was explained by the different
bioavailability of phenanthrene among artificial soils [74, 75, 89] (󳶳 Fig. 9.3). By pyrose-
quencing analysis of 16S rRNA gene fragments amplified from total community-DNA,
discriminative bacterial responders to phenanthrene and litter addition were identi-
fied. For instance, an increase of sequences affiliated to the so far poorly described
genus Kocuria in response to phenanthrene was found in all artificial soils except for
the montmorillonite mixture, giving new insights into habitat preferences and ecolog-
ical functions [79]. The response of fungal communities to combined spikes of plant
litter and phenanthrene was influenced by the presence of charcoal as well. The spik-
ing of artificial soils matured for different periods also allowed consideration of the
time factor as an additional parameter. Hence, it was observed that spiking of phenan-
threne even increased the dissimilarity between bacterial communities from artificial
soils with different clay minerals present after more than 2 years of maturation [75].
The artificial soil experiments of the DFG Priority Program (󳶳 Tab. 9.1) aimed at
studying the effect of mineral or charcoal surfaces on soil interface formation, micro-
bial community establishment, and soil functioning. The results from these multidis-
ciplinary analyses of those artificial soils suggest that the mineral composition is a crit-
ical variable in determining the functionality and response of microbial communities.
However, the underlying mechanisms and interactions still remain unclear. As dis-

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cussed above, the response of microorganisms to soil components might be based on

a direct surface interaction. Otherwise, it might be an indirect consequence of the incu-
bation, which allowed the reaction of soil components and, thus, interface formation
and development of complexity. The same applies to the observed soil composition-
dependent responses to spiked compounds: they might be caused by different micro-
bial communities established before the spiking was conducted, by the different in-
terfaces established, or by a complex interplay of all of those factors, respectively [75].
9.6 Artificial Soils for Arid Soil Research
More than one third of Earth’s land area is drylands. Only animal and plant life forms
that are adapted to the extreme conditions (e.g., limited and pulsed nutrient input,
low OM content, water deficiency, temperature variation, alkaline pH) can establish
in arid soils [90]. Most of the soil experiments are carried out with soils from mesic
environments and, therefore, our knowledge of the biology of arid soils is still limited.
Due to the different water regimes affecting microbial activity, but also general interac-
tions between SOM and minerals, it is questionable to which extent information from
temperate soils is also relevant for arid soils. However, the importance and ecological
significance of arid soils that are regarded as especially vulnerable to the global cli-
mate change will likely rise in future [91]. It was previously reported that arid soils offer
certain heterogeneity due to, e.g., nutrient depth stratification and patchy vegetation
distribution [90, 91]. However, one might postulate that the complexity of arid soils is
less compared to that of grassland, forest, or tropical soils due to the lower amounts of
water and SOM (󳶳 Fig. 9.1). Therefore, artificial soils, which are restricted in complex-
ity as well, can be regarded as suitable model systems to study microbial communities
and microbe-mediated processes in arid soils. As mentioned above, simplified soil ex-
periments were already used to study the impact of water content on microbial interac-
tions and community establishment [26, 27]. The artificial soils composed within the
framework of the DFG Priority Program [53, 54] did not focus on water as a parameter.
These artificial soils were incubated at a constant water content of 60% of the water
holding capacity, which likely did not trigger drought stress for most microorganisms.
Furthermore, it was assumed that surfaces were mostly wettable [89]. It may be possi-
ble that water availability differed slightly among these artificial soils due to different
properties of the soil minerals and charcoal, as water tension was not measured di-
rectly. There is no doubt that water is an important covariable shaping the microbial
community establishment in artificial soils during maturation. For following studies,
the compositions of these artificial soils could be varied in order to specifically study
the influence of water on structuring soil microbial communities. For instance, the ef-
fect of the soil mineral composition and pore space geometry could become more im-
portant at low water contents which would, in turn, also affect BGI formation. Given
the appropriate experimental design, incubation of artificial soils will also allow to

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9.7 Concluding Remarks | 175
study the effect of EPS on soil structure and whether it contributes to water retention
or water repellency [23, 92]. These results would certainly provide new insights into
the role of microorganisms as soil architects.
Due to their restricted complexity, arid soils themselves could be regarded as a
simplified soil model. Thus, concepts or hypotheses proposed, based on results from
simplified experimental designs (e.g., artificial soils) could be tested with arid soils.
9.7 Concluding Remarks
A long-standing history and recent research results demonstrate that artificial soils
have become a well-established and useful tool to simulate processes in natural soils
and especially to understand microbial community establishment and functioning.
By their controlled composition, artificial soils exclude factors other than the factor of
interest [7] and still provide conditions similar to natural soils. Vogel et al. [85] showed
that matured artificial soils exhibited similar OM dynamics as a natural soil. Further-
more, the qualitative response of microbial communities that established in artificial
soils to spiked compounds was similar to that of natural soils [75, 76]. Due to their
reproducibility, artificial soils with exact component specifications are established as
a standard medium and reference material for ecotoxicological tests [93–95]. The re-
duced complexity of artificial soils, however, at the same time indicates their limita-
tions. This must be kept in mind before extrapolation of results to natural soils [94]. For
instance, in the case of the artificial soil studies of Pronk et al. [53] and Vogel et al. [54],
a regular and complex OM input as it occurs in nature was excluded. Therefore, a re-
duced microbial diversity was found, and the artificial soils responded more strongly
to external perturbations compared to microorganisms in native soils [75].
Due to the immense interactions of different soil components and the opaque na-
ture of soil in addition, soil microbial ecology remains still a challenging research
discipline. Only continuous methodological improvement and multidisciplinary ap-
proaches can advance our understanding of the ecological role of soil microorgan-
isms and their contribution to soil formation and functioning. In contrast to other
approaches with the goal to model the nature in the lab (e.g., artificial intelligence,
bionics, biotechnology), artificial soil research should aim to get back to nature. A
step-by-step integration of additional variables into the established artificial soil sys-
tems, or the progress from artificial soils to natural arid soils seems necessary in order
to unravel the soil interaction network.
Acknowledgment: The authors acknowledge the Deutsche Forschungsgemeinschaft

(DFG) for funding this work within the framework of the Priority Program SPP1315
“Biogeochemical Interfaces in Soil”.

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Index
16S rRNA gene 165, 167, 169 Coccidioidomycosis see Coccidioides
Collema cristatum 125
A colonization 106
activity 15, 17, 19, 21, 22, 25–29 connectivity 161, 169, 171
Aflatoxin 114 contamination 21
Agaricomycetes 102, 105 Coprophilous fungi 106
agricultural use 17 crusts 20
algae 100 cultivation 162, 165
Alternaria 100, 106, 107, 113 Curvularia 107
AMF 103, see arbuscular mycorrhizal fungi cyanobacteria 20, 97
arbuscular mycorrhizal fungi 103, 104
arid soil 160, 174 D
arid zone 1 D. rigidulus 131
arthrospores 112 dark respiration 126
Ascomycota 97, 100, 103, 105, 109 dark septate fungi 97
Aspergillus 114 dermatophytes 112
Desert 97
B desertification 15, 17, 18, 24, 25
Basidiomycota 102, 103, 105, 106 DGGE 165, 167, 170
biocrusts 5, 6, 73–75, 78, 80, 82–88, 95–97, Diploschistes diacapsis 125
100, 108, 109 diversity 21, 159, 161, 165, 166, 168–170, 175
biodiversity 18 β-diversity 75, 78–81, 84–87, 89
biogeochemical interfaces (BGIs) 161 Dothideomycetes 102
biological soil crusts 41, see biocrusts; BSC droughts 15, 17, 22
Blastomycotina 103 Drylands 15
bryophytes dust storms 111
– definition 73
Bryum argenteum 125 E
BSC 123–127, 129–134 ecosystem functioning 83
ectomycorrhizal 104
C endemic 112
Caatinga 107 endolithic 3
calcium carbonate 80, 82 endophytes 103, 106, 107
carbon monoxide see CO enzyme activity 21
carbon sequestration 15, 16, 18, 19, 23, 24, 26 eumycetoma 113
cellulose 21 Eurotiomycetes 102
charcoal 161, 163, 166–170, 173 evapotranspiration 1
chasmolithic 3 evenness 81, 84–87, 96
Chihuahuan desert 102 experimental pedology 163
chlorophyll 124, 125, 131, 136, 137 extracellular enzymes 21
Chytridiomycota 103 extracellular polymeric substances (EPS) 111,
Cladonia convoluta 133 161
clay minerals 159, 161, 163, 167, 168, 172, 173 Extremophiles 108
climate change 17, 18, 21, 24, 25
CO 31, 38–40, 42, 44, 45 F
CO2 123, 125–129, 132, 134–136 fertility 15, 18, 19, 23, 24, 26
Coccidioides 112 functional redundancy 88, 96, 169

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182 | Index
functional traits 87 M
fungal network 102 matric potential 33–37, 43
fungi 97 maximal net photosynthetic see NPmax
Fusarium 113 melanin 107, 111
metagenomic 103
G metal oxides 161, 163, 167
global change 15, 16, 24 Methane 37, 38, 44
Global diversity and characteristic taxa 77 methanotroph 36, 38
Glomerales see Glomeromycota microbial activity 15, 21, 24, 26, 28
Glomeromycota 104 microbial biomass 16, 17, 19–22, 25, 28
glucose 19 microbial communities 15, 16, 25, 27
glycosidases 22 microbial ecology 159, 160, 164, 165, 171, 175
Gram positive 21 microbiota 159, 161, 164, 168, 171
grasses 106 Microcoleus vaginatus 100
grassland 103, 104, 109 microcolonies 109
Grimmia laevigata 125 microcosm 160, 163
gypsophiles 81 microenvironments 97, 103
gypsum 105, 107 microsclerotia 107
mineralization 16, 20, 24, 25
H mitosporic 97
heterogeneity 159, 163, 174 moisture 17, 18, 20–22, 28
humic acids 17 Mortierellales 102
humic substances 18, 21 Mortierellomycotina 103
hyperarid zone 1 moss 100
hyphae 97 Mucoromycotina 103
hypolithic 3 multifunctionality 87
mycetoma 114
I Mycohetetrophic 105
immunocompromised 112 mycorrhiza 103
incubation 159, 162, 163, 167, 168, 170, 172, 174 mycosis 113
inoculant 162, 166, 169 Mycotoxins 114
internal transcribed spacer (ITS) 165
islands of fertility 3 N
N deposition 108
K NanoSIMS 166
keratinolytic 112 nitrous oxide 40
NPmax 124, 125, 128, 129
L nutrient cycling 82–84, 87
land degradation 15
land use 16, 17, 20 O
leaf mass per area 125 Onygenaceae 112
Lecanora muralis 133 organic amendments 15, 19, 21, 24, 26, 28
lichen 99, 102 organic carbon 2, 15–20, 24, 25
lichens organic matter 15–21, 23–28
– definition 74 osmoconformers 36
lignin 21, 27
litter 167, 170, 172, 173 P
Lobaria pulmonaria 125 P. decipiens 131
Lobaria scrobicularia 125 Paraphaeosphaeria 107

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Index | 183
particle size fractionation 166, 167 soil formation 168, 172, 175
pathogen 97, 106, 111 soil microorganisms 17
pH 21, 80, 89 soil restoration 15, 16, 23, 26, 27
phenanthrene 170, 172, 173 solute potential 36
phenol oxidases 21 SOM 15–17, 19, 20, 22
Phoma 100 Sordariomycetes 102
photodegradation 15, 17, 18, 26 species richness 79, 81, 83, 84, 87–89, 96
photosynthetic photon flux density 126 specificity 106
Physcomitrella patens 127, 136, 137 spiking 173, 174
plant cover 15, 18, 26 stable isotope probing 19
plant pathogens 102 sustainability 16, 24
PLFA 19, 21, 27, 165, 170, 171 synthetic soil 162
poikilohydric 123, 130, 131, 134, 136 Syntrichia caninervis 125
porous media 159, 163
PPFD 126, 127, 131, 132, 135, see PPFD T
precipitation 16, 22, 140 Tensiometer 34
productivity 15, 18, 24 Thallus water content 127
Pseudocyphellaria crocata 125 thermotolerance 107
Pseudocyphellaria dissimilis 125 T-RFLP 165, 170
pyrosequencing 165, 167–171, 173 truffles 105
Q
W
quantitative real-time PCR (qPCR) 165
warming 16
water 159–161, 163, 166, 169, 171, 172, 174
R
water availability 15, 17, 19
respiration 17, 25
water potential 2, 31–41, 43, 45
rhizosphere 97, 100, 102, 103
rock varnish 109
X
S xerophilic 114
semiarid zone 2
shrubs 18 Y
soil erosion 19 yeast 108

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(Life in Extreme Environments 4) Ed. by Steven, Blaire With Contrib. by Antoninka, Anita J. - Babin, Doreen - Bastida, Felipe - Bowker, Matthew A. - Büdel, Burkhard - Cowan, Don A. - de Scally, Storm

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(Life in Extreme Environments 4) Ed. by Steven, Blaire With Contrib. by Antoninka, Anita J. - Babin, Doreen - Bastida, Felipe - Bowker, Matthew A. - Büdel, Burkhard - Cowan, Don A. - de Scally, Storm

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© 2017 Walter de Gruyter GmbH, Berlin/Boston

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Carlos Garcia, J.L.Moreno, T. Hernandez, and F. Bastida

Thulani P. Makhalanyane, Storme Z. de Scally, and Don A. Cowan

Matthew A. Bowker, Burkhard Büdel, Fernando T. Maestre, Anita J. Antoninka, and

Andrea Porras-Alfaro, Cedric Ndinga Muniania, Paris S. Hamm, Terry J. Torres-Cruz,

T.G. Allan Green

Blaire Steven, Theresa A. McHugh, and Sasha Reed

Doreen Babin, Michael Hemkemeyer, Geertje J. Pronk, Ingrid Kögel-Knabner,

Anita J. Antoninka Storme Z. de Scally

Felipe Bastida Carlos García

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Teresa Hernández José Luis Moreno

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Blaire Steven Terry J. Torres-Cruz

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1.1 The Deﬁnition and Extent of Arid Ecosystems

(a) (b) (c)

1.2 Characteristics of Arid Soils

1.3 Soil Habitats in Arid Regions

1.3.1 Refugia Sites Associated with Rocks

1.3.2 Shrubs as Islands of Fertility

A. Bacterial OTUs B. Fungal OTUs

1.3.3 Biological Soil Crusts

1.4 The Pulse Reserve Paradigm of Arid Ecosystems

1.5 Response of Arid Ecosystems to Disturbance

1.6 Arid Ecosystems as a Model for Soil Biology

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2.2 Climate Regulation and Soil Organic Carbon

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2.3 Land Use and Soil Organic Carbon in Arid-Semiarid Zones

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2.4 Soil Restoration in Arid-Semiarid Zones:

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2.5 Microbial Biomass and Enzyme Activity in Arid-Semiarid Zones

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18 months after organic

Fig. 2.1: Field experiment in Spain: soil restoration.

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2.6 Organic Carbon, Macro and Microaggregates,

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[5] von Lutzow M, Koegel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa

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3.2 Water Potential and Water Potential Assays

with nw representing number of moles of water kg−1 of solvent (= molality, about

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Water activity is often used as a temperature independent measure of water availabil-

where G represents Gibbs free energy, n i is solute concentration, P is pressure, and

where μ 0w represents the chemical potential of water in a standard reference state; R, T

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