The Biology of Arid Soils

Blaire Steven (Ed)The Biology of Arid SoilsLife in Extreme Environments

UnauthenticatedDownload Date | 5119 430 PM

Life in Extreme Environments

|Edited byDirk Wagner

Volume 4


The Biologyof Arid Soils

|


EditorBlaire StevenDepartment of Environmental SciencesConnecticut Agricultural Experiment Station123 Huntington StreetNew Haven CT 06511 USAblairestevenctgov

ISBN 978-3-11-041998-6e-ISBN (PDF) 978-3-11-041904-7e-ISBN (EPUB) 978-3-11-041914-6ISSN 2197-9227

Library of Congress Cataloging-in-Publication DataA CIP catalog record for this book has been applied for at the Library of Congress

Bibliographic information published by the Deutsche NationalbibliothekThe Deutsche Nationalbibliothek lists this publication in the Deutsche Nationalbibliografiedetailed bibliographic data are available on the Internet at httpdnbdnbde

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wwwdegruytercom


Preface

When Dr Dirk Wagner asked me to edit an edition in the series ldquoLife in Extreme En-vironmentsrdquo 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 Earthrsquos thermal vents Studies wherescientists require large field campaigns submersible vehicles and potential personalrisk to collect samples In contrast many people could collect a sample of arid soilin a brisk walk from wherever they may be reading this In this regard arid soils didnot seem to be such an ldquoextremerdquo of an environment Yet arid soils are united by acommon characteristic namely water scarcity which limits the diversity and produc-tivity of these systems Furthermore arid ecosystems also occur in both the hottestand coldest regions of the planet and therefore may experience a multitude of othersevere environmental conditions So in many respects arid soils may be as harsh ofan environment as more treacherous locals

Soil has been described as one of naturersquos most complex ecosystems Thus anyscientist that takes on the study of soil biology faces a daunting task By the virtue ofarid soil organisms existing at the lowwater availability to support life these commu-nities tend to be simplified compared tomore temperate soils The collection of papersin this volume highlight thework of researchers that are employing arid soils to under-stand the limits of life under lowwater availability the functioning of soil ecosystemsand 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 11) He hasalways been a hobbyist but can know say he is a published photographer Congratu-lations dad The list of contributing authors to this volumehighlights the internationalscope of arid land research and the broad disciplines involved Like any good work ofscience I hope this work raises as may questions for future research as it answers forthose with the curiosity to read it

Blaire Steven

Brought to you by | UCL - University College LondonAuthenticated

Download Date | 122517 1143 PM

Volumes published in the seriesVolume 1Jens Kallmeyer Dirk Wagner (Eds)Microbial Life of the Deep BiosphereISBN 978-3-11-030009-3

Volume 2Corien Bakermans (Ed)Microbial Evolution under Extreme ConditionsISBN 978-3-11-033506-4

Volume 3Annette Summers Engel (Ed)Microbial Life of Cave SystemsISBN 978-3-11-033499-9



Contents

Preface | V

Contributing authors | XI

Blaire Steven1 An Introduction to Arid Soils and Their Biology | 111 The Definition and Extent of Arid Ecosystems | 112 Characteristics of Arid Soils | 213 Soil Habitats in Arid Regions | 2131 Refugia Sites Associated with Rocks | 3132 Shrubs as Islands of Fertility | 3133 Biological Soil Crusts | 514 The Pulse Reserve Paradigm of Arid Ecosystems | 615 Response of Arid Ecosystems to Disturbance | 716 Arid Ecosystems as a Model for Soil Biology | 717 Summary | 7

Carlos Garcia JLMoreno T Hernandez and F Bastida2 Soils in Arid and Semiarid Environments the Importance of Organic Carbon

and Microbial Populations Facing the Future | 1521 Introduction | 1522 Climate Regulation and Soil Organic Carbon

in Arid-Semiarid Zones | 1623 Land Use and Soil Organic Carbon in Arid-Semiarid Zones | 1724 Soil Restoration in Arid-Semiarid Zones

Amendments Based on Exogenous Organic Matter | 1825 Microbial Biomass and Enzyme Activity in Arid-Semiarid Zones | 1926 Organic Carbon Macro and Microaggregates

and C Sequestration in Arid-Semiarid Zones | 2227 Conclusion | 23

Gary M King3 Water Potential as a Master Variable for AtmospherendashSoil Trace Gas

Exchange in Arid and Semiarid Ecosystems | 3131 Introduction | 3132 Water Potential and Water Potential Assays | 3233 Limits of Growth and Metabolic Activity | 3534 Water Potential and Trace Gas Exchanges | 3735 Conclusions | 41


VIII | Contents

Thulani P Makhalanyane Storme Z de Scally and Don A Cowan4 Microbiology of Antarctic Edaphic and Lithic Habitats | 4741 Introduction | 4742 Classification of Antarctic soils | 48421 McMurdo Dry Valley Soils | 49422 Antarctic Peninsula Soils | 5043 Bacterial Diversity of Soils in the MDVs and Antarctic Peninsula | 5144 Cryptic Niches in Antarctic Environments | 54441 Hypoliths | 55442 Epiliths | 56443 Endoliths | 5745 Biogeochemical Cycling in Antarctic Environments | 5946 Viruses in Antarctic Edaphic Ecosystems | 5947 Conclusions and Perspectives | 60

Matthew A Bowker Burkhard Buumldel Fernando T Maestre Anita J Antoninka andDavid J Eldridge5 Bryophyte and Lichen Diversity on Arid Soils Determinants and

Consequences | 7351 Overview | 73511 Moss Liverwort and Lichen Biology | 7352 Global Diversity and Characteristic Taxa | 74521 Global Species Pool | 74522 Global Characteristic Taxa and β Diversity | 7553 Determinants of Moss Liverwort and Lichen Diversity

on Arid Soils | 78531 Geographic Isolation and Biogeography | 78532 Climatic Gradients and Climate Change | 79533 CalcicolendashCalcifuge Dichotomy and Soil pH Gradients | 80534 The Special Case of Gypsiferous Soils | 8154 Consequences of Moss Liverwort and Lichen Diversity

on Arid Soils | 82541 Contribution of Biocrust Lichens and Bryophytes to Arid Ecosystem

Function | 82542 BiodiversityndashEcosystem Functioning Relationship | 83543 Effects of Species Richness Turnover and Evenness on Ecosystem

Functions | 84544 Multifunctionality | 87545 Functional Redundancy or Singularity | 8855 Summary and Conclusions | 89


Contents | IX

Andrea Porras-Alfaro Cedric Ndinga Muniania Paris S Hamm Terry J Torres-Cruzand Cheryl R Kuske6 Fungal Diversity Community Structure and Their Functional Roles in Desert

Soils | 9761 Spatial Heterogeneity of Fungal Communities in Arid Lands | 97611 Biocrusts | 100612 Plant Associated Fungi in Deserts | 10362 Roles in Nutrient Cycling and Effects of Climate Change on Fungal

Communities | 10763 Extremophiles in Deserts | 108631 Thermophilic and Thermotolerant Fungi | 109632 Rock Varnish and Microcolonial Fungi in Deserts | 10964 Human Pathogenic Fungi in Desert Ecosystems | 111641 Coccidioides immitis and C posadasii | 112642 Dematiaceous and Keratinolytic Fungi in Deserts | 112643 Eumycetoma | 113644 Mycotoxins | 11465 Importance of Fungal Biodiversity in Arid Lands | 115

TG Allan Green7 Limits of Photosynthesis in Arid Environments | 12371 Introduction | 12372 Photosynthetic Responses to Environmental Factors

a Background | 124721 Rates Chlorophyll and Mass | 124722 Response of Net Photosynthesis (NP) to Light (PPFD

μmol mminus2 sminus1) | 126723 Response of Net Photosynthesis to Temperature | 127724 Response of Net Photosynthesis to Thallus Water Content (WC) | 127725 Response of Net Photosynthesis to CO2 Concentration | 12973 Optimal Versus Real Photosynthetic Rates | 12974 Limits to Photosynthesis in Arid Areas | 131741 Length of Active Time | 131742 Limits When Active ndash External Limitation Through Light and

Temperature | 132743 Limits When Active ndash Internal Limitation Through Thallus

Hydration | 132744 Catastrophes | 13375 Flexibility ndash an Often Overlooked Factor | 13476 Summary | 134


X | Contents

Blaire Steven Theresa A McHugh and Sasha Reed8 The Response of Arid Soil Communities to Climate Change | 13981 Overview | 13982 Biological Responses to Elevated Atmospheric CO2 | 14083 Biological Responses to Increased Temperature | 14284 Biological Responses to Changes in Precipitation | 143841 Natural Precipitation Gradients | 145842 Precipitation Manipulation Studies | 14785 Interactions Between Temperature and Soil Moisture | 14986 Conclusion | 150

Doreen Babin Michael Hemkemeyer Geertje J Pronk Ingrid Koumlgel-KnabnerChristoph C Tebbe and Kornelia Smalla9 Artificial Soils as Tools for Microbial Ecology | 15991 Introduction | 15992 Soil Definition | 16093 History of Artificial Soil Experiments | 16294 Methods in Soil Microbial Ecology and Soil Science | 16495 Insights into Microbial Communities from Artificial Soil Studies | 166951 Establishment and Structuring of Soil Microbial Communities | 166952 Functioning of Soil Microbial Communities | 16996 Artificial Soils for Arid Soil Research | 17497 Concluding Remarks | 175

Index | 181


Contributing authors

Anita J AntoninkaSchool of ForestryNorthern Arizona UniversityFlagstaff Arizona 86011 USAe-mail anitaantoninkanauedu

Doreen BabinJulius Kuumlhn-Institut ndash Federal Research Centrefor Cultivated Plants (JKI)Institute for Epidemiology and PathogenDiagnosticsBraunschweig Germanye-mail doreenbabinjulius-kuehnde

Felipe BastidaDepartment of Soil and Water ConservationCEBAS-CSICCampus Universitario de EspinardoMurcia Spaine-mail fbastidacebascsices

Matthew A BowkerSchool of ForestryNorthern Arizona UniversityFlagstaff Arizona 86011 USAe-mail matthewbowkernauedu

Burkhard BuumldelPlant Ecology amp SystematicsFaculty of BiologyUniversity of KaiserslauternKaiserslautern Germanye-mail buedelrhrkuni-klde

Don A CowanCentre for Microbial Ecology and GenomicsDepartment of Genetics Natural Sciences 2University of PretoriaHatfield Pretoria USAe-mail doncowanupacza

Storme Z de ScallyCentre for Microbial Ecology and GenomicsDepartment of Genetics Natural Sciences 2University of PretoriaHatfield Pretoria 0028e-mail u12021955tukscoza

David J EldridgeCentre for Ecosystem StudiesSchool of Biological Earth and EnvironmentalSciencesUniversity of New South WalesSydney Australiae-mail deldridgeunsweduau

Carlos GarciacuteaDepartment of Soil and Water ConservationCEBAS-CSIC Campus Universitario de EspinardoMurcia Spaine-mail cgarizqcebascsices

T G Allan GreenDepartamento de Vegetal II Farmacia FacultadUniversidad Complutense28040 Madrid Spaine-mail thomasgreenwaikatoacnz

Paris S HammDepartment of Biological SciencesWestern Illinois UniversityMacomb Illinois USAe-mail ps-hammwiuedu

Michael HemkemeyerThuumlnen Institute of BiodiversityFederal Research Institute for Rural AreasForestry and FisheriesBraunschweig GermanyPresent address Faculty of Life SciencesRhine-Waal University of Applied SciencesKleve Germanye-mail michaelhemkemeyerhochschule-rhein-waalde



XII | Contributing authors

Teresa HernaacutendezDepartment of Soil and Water ConservationCEBAS-CSIC Campus Universitario de EspinardoMurcia Spaine-mail mthernancebascsices

Gary M KingDepartment of Biological SciencesLouisiana State UniversityBaton Rouge Louisiana 70803 USAe-mail gkingmegmailcom

Ingrid Koumlgel-KnabnerLehrstuhl fuumlr Bodenkunde TechnischeUniversitaumlt MuumlnchenFreising-Weihenstephan GermanyInstitute for Advanced Study TechnischeUniversitaumlt MuumlnchenGarching Germanye-mail koegelwzwtumde

Cheryl R KuskeBioscience DivisionLos Alamos National LaboratoryLos Alamos New Mexico USAe-mail kuskelanlgov

Fernando T MaestreDepartamento de Biologiacutea y Geologiacutea Fiacutesica yQuiacutemica InorgaacutenicaEscuela Superior de Ciencias Experimentales yTecnologiacuteaUniversidad Rey Juan CarlosMoacutestoles Spaine-mail fernandomaestreurjces

Thulani P MakhalanyaneCentre for Microbial Ecology and GenomicsDepartment of Genetics Natural Sciences 2University of PretoriaHatfield Pretoria USAe-mail Thulanimakhalanyaneupacza

Theresa A MchughSouthwest Biological Science CenterUS Geological SurveyMoab Utah USAe-mail tmchughcoloradomesaedu

Joseacute Luis MorenoDepartment of Soil and Water ConservationCEBAS-CSIC Campus Universitario de EspinardoMurcia Spaine-mail jlmorenocebascsices

Cedric Ndinga MunianiaDepartment of Biological SciencesWestern Illinois UniversityMacomb Illinois USAe-mail c-ndingamunianawiuedu

Andrea Porras-AlfaroDepartment of Biological SciencesWestern Illinois UniversityMacomb Illinois USAe-mail a-porras-alfarowiuedu

Geertje J PronkLehrstuhl fuumlr Bodenkunde TechnischeUniversitaumlt MuumlnchenFreising-Weihenstephan GermanyInstitute for Advanced Study TechnischeUniversitaumlt MuumlnchenGarching GermanyPresent address Ecohydrology Research GroupUniversity of WaterlooWaterloo Ontario Canadae-mail gpronkuwaterlooca

Sasha ReedSouthwest Biological Science CenterUS Geological SurveyMoab Utah USAe-mail screedusgsgov

Kornelia SmallaJulius Kuumlhn-Institut ndash Federal Research Centrefor Cultivated Plants (JKI)Institute for Epidemiology and PathogenDiagnosticsBraunschweig Germanye-mail korneliasmallajulius-kuehnde



Contributing authors | XIII

Blaire StevenDepartment of Environmental SciencesConnecticut Agricultural Experiment StationNew Haven CT USAe-mail blairestevenctgov

Christoph C TebbeThuumlnen Institute of BiodiversityFederal Research Institute for Rural AreasForestry and FisheriesBraunschweig Germanye-mail christophtebbethuenende

Terry J Torres-CruzDepartment of Biological SciencesWestern Illinois UniversityMacomb Illinois USAe-mail tj-torrescruzwiuedu





Blaire Steven1 An Introduction to Arid Soils and Their Biology

11 The Definition and Extent of Arid Ecosystems

When one invokes the terms arid ecosystem or dryland it is often assumed that theterm refers to a desert However there are regional differences in the concept of aldquodesertrdquo as well as differences in terms for describing and classifying arid lands Theone characteristic that unites all arid lands is a lack ofwater availability generally dueto low precipitation Yet lack of precipitation is not the only factor that limits wateravailabilityWater 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 ldquodrynessrdquo of a region can be determinedby calculating the net difference between precipitation and water losses through eva-potranspiration also referred to as the Aridity Index [2ndash4] These metrics have been auseful tool to generate a standardized method to categorize and define drylands Thearidity index as well as other metrics such as the dominant vegetation and climatehave been used to classify arid lands into three main categories (998835 Fig 11)

Hyperarid zone (arid index 003 or below) Dryland areas of scant or no veg-etation Annual rainfall is low rarely exceeding 100mm Precipitation events areinfrequent and irregular with dry periods lasting up to several years Hyperarid re-gions coversim 8of the Earthrsquos surface [5] Examples AtacamaDesert SouthAmericaNamib Desert and Sahara Desert Africa and Lut Desert Iran

Arid zone (arid index 003ndash020) Vegetation consists of sparsely distributedpatches of annual or perennial grasses patchily distributed shrubs cacti or smalltrees Maximum precipitation varies from 100ndash300 mm per year Arid zones coversim16 of the planetrsquos land surface Examples Chihuahuan Desert USA and Simp-son Desert Australia

(a) (b) (c)

Fig 11 Examples of different arid zone landscapes (a) Hyperarid zone Namib Desert South AfricaPhoto courtesy Don Cowan (b) Arid zone Saguaro National Park Arizona USA (c) Semiarid zoneWitfontein Nature Reserve grassland South Africa Photos b and c courtesy Douglas Steven

DOI 1015159783110419047-001

2 | 1 An Introduction to Arid Soils and Their Biology

Semiarid zone (arid index 020ndash050) Vegetation is more diverse andmay coverthe surface For instance semiarid grasslands or steppes are common Annual pre-cipitation can reach 800mm per year and may occur in distinct dry and wet seasonsSemiarid zones cover sim18 of the Earth Examples Great Plains USA Kenyan Sa-vanah and Mongolian Steppes

It is important to note that not all arid soils occur in regions classified as drylandsIsolated patches of arid soils can occur in otherwise temperate regions for examplealpine tundra or volcanic cinders [6 7]

12 Characteristics of Arid Soils

Arid soils possess unique characteristics that distinguish them from soils from morehumid 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 thestructuring and function of arid soils and is the focus of Chapter 2 Extended periodsof water deficiencies also slow the elimination or leaching of soluble salts which arefurther 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 genesisthe 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] Thewater holding capacity of a soil depends on its physical characteristicsincluding texture structure and soil depth [11] This leads to large differences in theavailable water for biology between different soils The critical importance in waterpotential 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 factsoil parentmaterial and chemistry have been found to play a large role in shaping aridsoil biology [12 13] In this respect local edaphic factors need to be included in anystudy of arid soil biology

13 Soil Habitats in Arid Regions

Acharacteristic of arid regions is reduced biological diversity This hasbeenwell docu-mented for vegetation (eg [13ndash16]) and other macro fauna [18] Similar patterns haveemerged for soil bacterial and fungal communities [19 20] In fact a global surveyof drylands worldwide found that the diversity of soil bacteria and fungi was linearlycorrelated to the aridity of the ecosystem [21] In this regard aridity is a large predictorof the diversity of soil communities However drylands are not homogenous regionsexperiencing 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 precipitationand temperature vary erratically [22ndash25] In this respect not every patch of arid soil

13 Soil Habitats in Arid Regions | 3

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 thatmay 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 ecologicalniches some of which are discussed below

131 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 ismet by fog rather than precipitation [27 28] Rocks in deserts can support a numberof different communities These include hypolithic communities inhabiting the basalsurfaceof rocks [29 30] endolithic communities that live inside rocks or poresbetweenmineral grains [31ndash34] and chasmolithic communities under rock flakes produced byweathering [35 36] Rocks provide the soil microbiota physical stability increasedwater retention by shading protection from ultraviolet radiation and micronutrientsfrom the mineral components of the rock material [37]

Translucent rocks allow for light transmission to a depth sufficient to supportphototrophs such as mosses or cyanobacteria A common cyanobacteria occurringin hypolithic niches is Chroococcidiopsis sp [38] which has been detected in desertsworldwide [39] These phototrophic populations fix carbon which can then feed het-erotrophic populations resulting in relatively complex ecosystems [35 40] Thusthese communities act as a source of organic carbon which is a valuable commodityin otherwise nearly barren soils [41] Additionally the presence of active biology canaccelerate the weathering of the rocks This can occur either by metabolic activityof the communities scavenging nitrogen or phosphorous from the rock materialwhich has been shown to increase the weathering rate of rock by up to three ordersof magnitude or by physical infiltration into rock crevices and the mechanical dis-ruption of porous stones [42ndash44] These communities can also increase weatheringby encouraging grazing and the associated scraping of rock surfaces by predatoryinvertebrates [45] So beyond fixing organic carbon rock associated communities canalso release limiting nutrients supporting the growth of multiple trophic levels Inthis respect even the interspersed rocks in the desert can act as abiotic oases for soilbiology

132 Shrubs as Islands of Fertility

In arid ecosystems where plants are sparse a shrub is often a conspicuous aspect ofthe 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 ofthe 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 containsup to ten times more nutrients than bulk precipitation occurring outside of the shrubcanopy [48] Thus thismaterial canact to fertilize soils in the canopy zoneof the shrubAdditionally shrubs supply nest sites shade and food resources for animal popula-tions which can enrich the local soils through feces discarded carcasses and nestmaterials [49] Shrubs are also important in the interception infiltration and storageof water thereby increasing soil moisture [50] Finally the shrub itself contributesto the enrichment of soil nutrients In addition litter production root exudates anddeadfall all contribute to enriching the soils in the vicinity of the shrub [51] Thusshrubs indrylands arepotent collectors of resources and [52 53] are often referred to asldquoislands of fertilityrdquo [54] Shrubs also act as a cradle for biological diversity protect-ing the communities from ultraviolet radiation and decreasing evaporation throughshading [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 mixingof 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 soilrespiration rates are generally higher in shrub root zone soils than in interspace soils(eg [57ndash59]) 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 increasedmetabolic 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 tosupport a higher abundance of macroinvertebrates and nematodes [61ndash63] althoughshrub zone soils may harbor similar or even decreased levels of insect diversity [64]For soil bacteria and fungi studies have found an increased [65ndash67] or no effect [68] ontheir 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 speciesrather than the membership of the communities (998835 Fig 12 [68 70]) In other wordsshrub canopy soils harbor roughly the same bacteria and fungi as interspace soilsbut the structure of the community differs This has two important implications Firstit suggests that the bacteria and fungi that are well adapted to inhabiting arid soilsmay be ubiquitous across the landscape even in habitat patches that show differentcharacteristics Secondly there may be a relatively small number of bacterial and fun-gal species that need to be accounted for to understand biogeochemical cycles andfunctioning of arid soils


A Bacterial OTUs B Fungal OTUs of sequence reads of sequence reads

Root

sBi

ocru

sts

Biocrusts Root zonesBiocrusts Root zones

Shar

ed

Root

sBi

ocru

sts

Shar

ed

25 20 051015 5 10 30 20 2010010 30 40 50 60

Fig 12 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 sharedbetween the habitat patches those unique to biocrusts and those unique to the root zones Forboth the bacteria and fungi the most abundant OTUs were shared between the habitats suggestinga similar membership for the communities in both habitats although the abundance of those sameOTUs varied widely between the two habitats Thus the membership of the communities is similaralthough the structure may vary Figure adapted from [68]

133 Biological Soil Crusts

The surface soils between rocks and plants of arid regions are not devoid of life Infact some of the most diverse arid soil communities occur in plant interspaces of aridand semiarid lands as communities colonizing surface soils These communities forma surface crust that has been variously referred to as cryptogamic microbiotic crypto-biotic or microphytic [71] More inclusively the term biological soil crusts (shortenedto biocrusts for this chapter) has been used to refer to the biological crusts that inhabita multitude of arid lands [72 73] In some arid lands biocrusts cover up to 60ndash70 ofthe surface soils [74] Biocrusts have been identified on every continent on Earth andare a conspicuous feature of drylands worldwide [75]

The keystone species of most biocrusts are cyanobacteria [76ndash78] Filamentousspecies 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 communitymem-bers [80] Some of this carbon is in the form of extracellular polymeric substancesthat act as the glue to bind the soil together and the matrix to create the surface crustbiofilm [81] Other cyanobacteria in the biocrusts fix atmospheric nitrogen or producepigments such as scytonemin that protect the crust organisms from ultraviolet radi-ation [82ndash84] Beyond cyanobacteria biocrusts harbor mosses lichens fungi algaea variety of heterotrophic bacteria and archaea [85ndash89] This also leads to an enrich-ment of other soil fauna as nematode populations are more abundant and diverse inmature biocrusts [88] Because the dominant species of biocrusts are phototrophic


the biomass of the crusts is concentrated in the upper few millimeters of soil butleaching of these nutrients can enrich surrounding and underlying soils [56] In thisregard biocrusts are a complex and diverse ecosystem that support multiple trophiclevels 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 soilerosion by wind and water [92ndash95] Biocrusts are a significant source of fixed carbonand 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 tosurrounding 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 surroundingsoils [97ndash99] This nutrient trapping and leachingmay also assist in the establishmentand development of desert plants [100ndash102] Some evidence even suggests that theremay 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 ofincreased soil fertility but are an integral component to dryland ecosystem function

14 The Pulse Reserve Paradigm of Arid Ecosystems

Dryland ecosystems are not just defined by a lack of water precipitation occurs asepisodic events Therefore an essential resource (water) is only available in pulseswith 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 periodicityof precipitation events In 1973 Noy-Meir [105] proposed the ldquopulse reserverdquo model ofproduction in arid systems Conceptually the model proposes that a pulse of waterprovided through a precipitation event stimulates the initiation of biological activ-ity (generally photosynthesis) After a period of activity the organism builds reservesof energy to sustain it through the following dry period and to the next pulse Thismodel was developed for dryland plants but it has also been shown to be applicableto mosses [106] and cyanobacteria [107] A central aspect of this model is that pre-cipitation events need to be ldquobiologically meaningfulrdquo in that the water needs to ofsufficient amount and duration to stimulate biological activity [108] This sets up a hi-erarchical response to precipitation events Small precipitation events will stimulatesoil cyanobacteria or algae but are inadequate to initiate plant activity [109] For ex-ample it has been estimated that sim2mm precipitation events are generally adequateto activate soil cyanobacteriawithin a fewminutes whereas plants may require in therange of 3ndash5mm of precipitation with soil moisture lasting for at least an hour [11] Inthis respect understanding dryland ecosystems extends beyond just considering thelimitation of water andmust consider the magnitude duration and timing of precipi-

17 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

15 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 precipitationpatterns [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 thecomposition and function of arid soil communities dramatically As a consequence ofthe 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 atipping 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

16 Arid Ecosystems as a Model for Soil Biology

As mentioned previously arid soils generally harbor less diverse soil communitiesthan 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 numberof trophic levels and these levels generally become more simple as the environmentbecomes more extreme [35] This relatively low biodiversity and complexity allows re-searchers to disentangle the biologic climatic and environmental factors that drivethe composition and functioning of ecosystems more easily Thus arid soil systemshave been proposed as a system to understand biodiversity ecosystem function rela-tionships better [114] In Chapter 9 artificial soil microcosms and their contribution tounderstanding soil biological processes are discussed

17 Summary

The Earthrsquos drylands are a diverse patchwork of systems united by a common featureof limited water availability While the differences between drylands are numerouscertain 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 abioticfactors that shape the distinct unique and often overlooked soil communities of aridlands

References

[1] Sellers WD Potential Evapotranspiration in Arid Regions J Appl Meteorol 1964 398ndash104[2] Girvetz EH Zganjar C Dissecting indices of aridity for assessing the impacts of global climate

change Clim Change 2014 126469ndash83[3] Tsakiris G Vangelis H Establishing a drought index incorporating evapotranspiration Eur

Water 2005 93ndash11[4] Levin NE Cerling TE Passey BH Harris JM Ehleringer JR A stable isotope aridity index for

terrestrial environments Proc Natl Acad Sci 2006 10311201ndash5[5] Tucker CJ Newcomb WW Dregne HE AVHRR data sets for determination of desert spatial

extent Int J Remote Sens 1994 153547ndash65[6] Taylor RV Seastedt TR Short- and long-term patterns of soil moisture in alpine tundra Arct

Alp Res 1994 2614[7] Weber CF King GM Distribution and diversity of carbon monoxide-oxidizing bacteria and

bulk bacterial communities across a succession gradient on a Hawaiian volcanic deposit COoxidizer diversity across a succession gradient Environ Microbiol 2010 121855ndash67

[8] Ewing SA Sutter B Owen J et al A threshold in soil formation at Earthrsquos aridndashhyperarid tran-sition Geochim Cosmochim Acta 2006 705293ndash322

[9] Skujins J Genesis and Classification of Arid Region Soils In Semiarid Lands and DesertsSoil Resource and Reclamation CRC Press 1991 33

[10] Bronick CJ Lal R Soil structure and management a review Geoderma 2005 1243ndash22[11] Austin AT Yahdjian L Stark JM et al Water pulses and biogeochemical cycles in arid and

semiarid ecosystems Oecologia 2004 141221ndash35[12] Steven B Gallegos-Graves LV Belnap J Kuske CR Dryland soil microbial communities display

spatial biogeographic patterns associated with soil depth and soil parent material FEMSMicrobiol Ecol 2013 86101ndash13

[13] Deng H Yu Y-J Sun J-E et al Parent materials have stronger effects than land use types onmicrobial biomass activity and diversity in red soil in subtropical China Pedobiologia 20155873ndash9

[14] Qian H Ricklefs RE A latitudinal gradient in large-scale beta diversity for vascular plants inNorth America Ecol Lett 2007 10737ndash44

[15] von Hardenberg J Meron E Shachak M Zarmi Y Diversity of vegetation patterns and desertifi-cation Phys Rev Lett 2001 87198101

[16] Kreft H Jetz W Global patterns and determinants of vascular plant diversity Proc Natl AcadSci 2007 1045925ndash30

[17] Davenport ML Nicholson SE On the relation between rainfall and the Normalized DifferenceVegetation Index for diverse vegetation types in East Africa Int J Remote Sens 1993 142369ndash89

[18] Abramsky Z Rosenzweig ML Tilmanrsquos predicted productivityndashdiversity relationship shown bydesert rodents Nature 1984 309150ndash1

[19] Dunbar J Takala S Barns SM Davis JA Kuske CR Levels of bacterial community diversity infour arid soils compared by cultivation and 16S rRNA gene cloning Appl Environ Microbiol1999 651662ndash9

References | 9

[20] Whitford WG The importance of the biodiversity of soil biota in arid ecosystems BiodiversConserv 1996 5185ndash95

[21] Maestre FT Delgado-Baquerizo M Jeffries TC et al Increasing aridity reduces soil microbialdiversity and abundance in global drylands Proc Natl Acad Sci 2015 11215684ndash89

[22] Huenneke LF Clason D Muldavin E Spatial heterogeneity in Chihuahuan Desert vegetationimplications for sampling methods in semi-arid ecosystems J Arid Environ 2001 47257ndash70

[23] Aguiar MR Sala OE Patch structure dynamics and implications for the functioning of aridecosystems Trends Ecol Evol 1999 14273ndash7

[24] Keacutefi S Rietkerk M Alados CL et al Spatial vegetation patterns and imminent desertificationin Mediterranean arid ecosystems Nature 2007 449213ndash7

[25] Maestre FT Cortina J Spatial patterns of surface soil properties and vegetation in a Mediter-ranean semi-arid steppe Plant Soil 2002 241279ndash91

[26] Burke A Properties of soil pockets on arid Nama Karoo inselbergsndashthe effect of geology andderived landforms J Arid Environ 2002 50219ndash34

[27] Warren-Rhodes KA McKay CP Boyle LN et al Physical ecology of hypolithic communities inthe central Namib Desert The role of fog rain rock habitat and light J Geophys Res Biogeo-sciences 2013 1181451ndash60

[28] Caacuteceres L Goacutemez-Silva B Garroacute X Rodriacuteguez V Monardes V McKay CP Relative humiditypatterns and fog water precipitation in the Atacama Desert and biological implications J Geo-phys Res 2007 112(G4)

[29] Chan Y Lacap DC Lau MCY et al Hypolithic microbial communities between a rock and ahard place Hypolithic microbial communities Environ Microbiol 2012 142272ndash82

[30] Cowan DA Khan N Pointing SB Cary SC Diverse hypolithic refuge communities in the Mc-Murdo Dry Valleys Antarct Sci 2010 22714ndash20

[31] Friedmann EI Endolithic Microorganisms in the Antarctic Cold Desert Science 19822151045ndash53

[32] Friedmann EI Endolithic Microbial Life in Hot and Cold Deserts In Ponnamperuma C Mar-gulis L (eds) Limits of Life Dordrecht Springer Netherlands 1980 33ndash45

[33] Omelon CR Endolithic microbial communities in polar desert habitats Geomicrobiol J 200825404ndash14

[34] Wierzchos J Ascaso C McKay CP Endolithic cyanobacteria in halite rocks from the hyperaridcore of the Atacama Desert Astrobiology 2006 6415ndash22

[35] Cary SC McDonald IR Barrett JE Cowan DA On the rocks the microbiology of Antarctic DryValley soils Nat Rev Microbiol 2010 8129ndash38

[36] Cowan DA Tow LA Endangered Antarctic Environments Annu Rev Microbiol 2004 58649ndash90

[37] Cowan DA Pointing SB Stevens MI Craig Cary S Stomeo F Tuffin IM Distribution and abioticinfluences on hypolithic microbial communities in an Antarctic Dry Valley Polar Biol 201134307ndash11

[38] Grilli Caiola M Ocampo-Friedmann R Friedmann EI Cytology of long-term desiccation in thedesert cyanobacterium Chroococcidiopsis (Chroococcales) Phycologia 1993 32315ndash22

[39] Pointing SB Warren-Rhodes KA Lacap DC Rhodes KL McKay CP Hypolithic community shiftsoccur as a result of liquid water availability along environmental gradients in Chinarsquos hot andcold hyperarid deserts Environ Microbiol 2007 9414ndash24

[40] Lacap DC Warren-Rhodes KA McKay CP Pointing SB Cyanobacteria and chloroflexi-domi-nated hypolithic colonization of quartz at the hyper-arid core of the Atacama Desert ChileExtremophiles 2011 1531ndash8

[41] Cowan DA Sohm JA Makhalanyane TP et al Hypolithic communities important nitrogensources in Antarctic desert soils Environ Microbiol Rep 2011 3581ndash6


[42] Banfield JF Barker WW Welch SA Taunton A Biological impact on mineral dissolution appli-cation of the lichen model to understanding mineral weathering in the rhizosphere Proc NatlAcad Sci 1999 963404ndash11

[43] Viles H Ecological perspectives on rock surface weathering Towards a conceptual modelGeomorphology 1995 1321ndash35

[44] Bennett PC Rogers JR Silicates WJ Silicate weathering and microbial ecology GeomicrobiolJ 2001 183ndash19

[45] Danin A Garty J Distribution of cyanobacteria and lichens on hillsides of the Negev High-lands and their impact on biogenic weathering Flora Israel 1983 27423ndash44

[46] Coppinger KD Reiners WA Burke IC Olson RK Net erosion on a sagebrush steppe landscapeas determined by cesium-137 distribution Soil Sci Soc Am J 1991 55254

[47] Martinez-Meza E Whitford WG Stemflow throughfall and channelization of stemflow byroots in three Chihuahuan desert shrubs J Arid Environ 1996 32271ndash87

[48] Whitford WG Anderson J Rice PM Stemflow contribution to the ldquofertile islandrdquo effect in cre-osotebush Larrea tridentata J Arid Environ 1997 35451ndash7

[49] Dean WRJ Milton SJ Jeltsch F Large trees fertile islands and birds in arid savanna J AridEnviron 1999 4161ndash78

[50] Nulsen RA Bligh KJ Baxter IN Solin EJ Imrie DH The fate of rainfall in a mallee and heathvegetated catchment in southern Western Australia Aust J Ecol 1986 11361ndash71

[51] Butterfield BJ Briggs JM Patch dynamics of soil biotic feedbacks in the Sonoran Desert J AridEnviron 2009 7396ndash102

[52] Garcia-Moya E McKell CM Contribution of shrubs to the nitrogen economy of a desert-washplant community Ecology 1970 5181

[53] Charley JL West NE Plant-induced soil chemical patterns in some shrub-dominated semi-desert ecosystems of Utah J Ecol 1975 63945

[54] Schlesinger WH Reynolds JF Cunningham GL et al Biological feedbacks in global desertifi-cation Science 1990 2471043ndash8

[55] Berg N Steinberger Y Role of perennial plants in determining the activity of the microbialcommunity in the Negev Desert ecosystem Soil Biol Biochem 2008 402686ndash95

[56] Garcia-Pichel F Johnson SL Youngkin D Belnap J Small-scale vertical distribution of bacte-rial biomass and diversity in biological soil crusts from arid lands in the Colorado PlateauMicrob Ecol 2003 46312ndash21

[57] Zaady E Groffman PM Shachak M Litter as a regulator of N and C dynamics in macrophyticpatches in Negev desert soils Soil Biol Biochem 1996 2839ndash46

[58] Conant RT Klopatek JM Malin RC Klopatek CC Carbon pools and fluxes along an environ-mental gradient in northern Arizona Biogeochemistry 1998 4343ndash61

[59] Su Y Zhao H Li Y Cui J Carbon mineralization potential in soils of different habitats in thesemiarid Horqin Sandy Land a laboratory experiment Arid Land Res Manag 2004 1839ndash50

[60] Dossa EL Khouma M Diedhiou I et al Carbon nitrogen and phosphorus mineralization po-tential of semiarid Sahelian soils amended with native shrub residues Geoderma 2009148251ndash60

[61] Liu R Zhao H Zhao X Drake S Facilitative effects of shrubs in shifting sand on soil macro-faunal community in Horqin Sand Land of Inner Mongolia Northern China Eur J Soil Biol2011 47316ndash21

[62] Doblas-Miranda E Saacutenchez-Pintildeero F Gonzaacutelez-Megiacuteas A Different microhabitats affect soilmacroinvertebrate assemblages in a Mediterranean arid ecosystem Appl Soil Ecol 200941329ndash35

References | 11

[63] Yong-zhong S Xue-fen W Rong Y Xiao Y Wen-jie L Soil fertility salinity and nematode diver-sity influenced by Tamarix ramosissima in different habitats in an arid desert oasis EnvironManage 2012 50226ndash36

[64] Yeates GW Schipper LA Smale MC Site condition fertility gradients and soil biological activ-ity in a New Zealand frost-flat heathland Pedobiologia 2004 48129ndash37

[65] Bachar A Soares MIM Gillor O The Effect of resource islands on abundance and diversity ofbacteria in arid Soils Microb Ecol 2012 63694ndash700

[66] Housman DC Yeager CM Darby BJ et al Heterogeneity of soil nutrients and subsurface biotain a dryland ecosystem Soil Biol Biochem 2007 392138ndash49

[67] Ewing SA Southard RJ Macalady JL Hartshorn AS Johnson MJ Soil microbial fingerprintscarbon and nitrogen in a Mojave Desert creosote-bush ecosystem Soil Sci Soc Am J 200771469

[68] Steven B Gallegos-Graves LV Yeager CM Belnap J Kuske CR Common and distinguishingfeatures of the bacterial and fungal communities in biological soil crusts and shrub root zonesoils Soil Biol Biochem 2014 69302ndash12

[69] Kuske CR Ticknor LO Miller ME et al Comparison of soil bacterial communities in rhizo-spheres of three plant species and the interspaces in an arid grassland Appl Environ Micro-biol 2002 681854ndash63

[70] Steven B Gallegos-Graves LV Starkenburg SR Chain PS Kuske CR Targeted and shotgunmetagenomic approaches provide different descriptions of dryland soil microbial communi-ties in a manipulated field study Environ Microbiol Rep 2012 4248ndash56

[71] Belnap J The world at your feet desert biological soil crusts Front Ecol Environ 20031181ndash9

[72] Belnap J Buumldel B Lange OL Biological soil crusts characteristics and distribution Springer2003

[73] Steven B Lionard M Kuske CR Vincent WF High bacterial diversity of biological soil crusts inwater tracks over permafrost in the high Arctic Polar Desert PLoS ONE 2013 8e71489

[74] Ustin SL Valko PG Kefauver SC Santos MJ Zimpfer JF Smith SD Remote sensing of biolog-ical soil crust under simulated climate change manipulations in the Mojave Desert RemoteSens Environ 2009 113317ndash28

[75] Pointing SB Belnap J Microbial colonization and controls in dryland systems Nat Rev Micro-biol 2012 10551ndash62

[76] Garcia-Pichel F Loacutepez-Corteacutes A Nuumlbel U Phylogenetic and morphological diversity ofCyanobacteria in soil desert crusts from the Colorado Plateau Appl Environ Microbiol 2001671902ndash10

[77] Steven B Gallegos-Graves LV Yeager CM Belnap J Evans RD Kuske CR Dryland biologicalsoil crust cyanobacteria show unexpected decreases in abundance under long-term elevatedCO2 Environ Microbiol 2012 143247ndash58

[78] Belnap J Phillips SL Witwicki DL Miller ME Visually assessing the level of development andsoil surface stability of cyanobacterially dominated biological soil crusts J Arid Environ 2008721257ndash64

[79] Langhans TM Storm C Schwabe A Community assembly of biological soil crusts of differentsuccessional stages in a temperate sand ecosystem as assessed by direct determination andenrichment techniques Microb Ecol 2009 58394ndash407

[80] Billings S Schaeffer S Evans R Nitrogen fixation by biological soil crusts and heterotrophicbacteria in an intact Mojave Desert ecosystem with elevated CO2 and added soil carbon SoilBiol Biochem 2003 35643ndash9

[81] Mazor G Kidron GJ Vonshak A Abeliovich A The role of cyanobacterial exopolysaccharidesin structuring desert microbial crusts FEMS Microbiol Ecol 1996 21121ndash30


[82] Bowker MA Reed SC Belnap J Phillips SL Temporal variation in community compositionpigmentation and FvFm of desert cyanobacterial soil crusts Microb Ecol 2002 4313ndash25

[83] Yeager CM Kornosky JL Morgan RE et al Three distinct clades of cultured heterocystouscyanobacteria constitute the dominant N2-fixing members of biological soil crusts of theColorado Plateau USA FEMS Microbiol Ecol 2007 6085ndash97

[84] Gao Q Garcia-Pichel F Microbial ultraviolet sunscreens Nat Rev Microbiol 2011 9791ndash802[85] Nagy ML Peacuterez A Garcia-Pichel F The prokaryotic diversity of biological soil crusts in the

Sonoran Desert (Organ Pipe Cactus National Monument AZ) FEMS Microbiol Ecol 200554233ndash45

[86] Gundlapally SR Garcia-Pichel F The community and phylogenetic diversity of biological soilcrusts in the Colorado Plateau studied by molecular fingerprinting and intensive cultivationMicrob Ecol 2006 52345ndash57

[87] Martiacutenez I Escudero A Maestre FT de la Cruz A Guerrero C Rubio A Small-scale patternsof abundance of mosses and lichens forming biological soil crusts in two semi-arid gypsumenvironments Aust J Bot 2006 54339

[88] Darby BJ Neher DA Belnap J Soil nematode communities are ecologically more maturebeneath late- than early-successional stage biological soil crusts Appl Soil Ecol 200735203ndash12

[89] Bates ST Garcia-Pichel F A culture-independent study of free-living fungi in biological soilcrusts of the Colorado Plateau their diversity and relative contribution to microbial biomassEnviron Microbiol 2009 1156ndash67

[90] Eldridge D Zaady E Shachak M Infiltration through three contrasting biological soil crusts inpatterned landscapes in the Negev Israel Catena 2000 40323ndash6

[91] Bowker MA Belnap J Davidson DW Phillips SL Evidence for micronutrient limitation of bio-logical soil crusts importance to arid-lands restoration Ecol Appl 2005 151941ndash51

[92] Belnap J Gillette DA Vulnerability of desert biological soil crusts to wind erosion the influ-ences of crust development soil texture and disturbance J Arid Environ 1998 39133ndash42

[93] Belnap J Gillette DA Disturbance of biological soil crusts impacts on potential wind erodibil-ity of sandy desert soils in southeastern Utah Land Degrad Dev 1997 8355ndash62

[94] Eldridge DJ Leys JF Exploring some relationships between biological soil crusts soil aggre-gation and wind erosion J Arid Environ 2003 53457ndash66

[95] Bowker MA Belnap J Bala Chaudhary V Johnson NC Revisiting classic water erosion modelsin drylands the strong impact of biological soil crusts Soil Biol Biochem 2008 402309ndash16

[96] Yeager CM Kornosky JL Housman DC Grote EE Belnap J Kuske CR Diazotrophic communitystructure and function in two successional stages of biological soil crusts from the ColoradoPlateau and Chihuahuan Desert Appl Environ Microbiol 2004 70973ndash83

[97] Johnson SL Neuer S Garcia-Pichel F Export of nitrogenous compounds due to incompletecycling within biological soil crusts of arid lands Environ Microbiol 2007 9680ndash9

[98] Evans RD Ehleringer JR A break in the nitrogen cycle in aridlands Evidence from δ15N ofsoils Oecologia 1993 94314ndash7

[99] Johnson SL Budinoff CR Belnap J Garcia-Pichel F Relevance of ammonium oxidation withinbiological soil crust communities Environ Microbiol 2005 71ndash12

[100] Harper KT Belnap J The influence of biological soil crusts on mineral uptake by associatedvascular plants J Arid Environ 2001 47347ndash57

[101] Su Y-G Li X-R Cheng Y-W Tan H-J Jia R-L Effects of biological soil crusts on emergence ofdesert vascular plants in North China Plant Ecol 2007 19111ndash9

[102] Langhans TM Storm C Schwabe A Biological soil crusts and their microenvironment Impacton emergence survival and establishment of seedlings Flora Morphol Distrib Funct EcolPlants 2009 204157ndash68

References | 13

[103] Green LE Porras-Alfaro A Sinsabaugh RL Translocation of nitrogen and carbon integratesbiotic crust and grass production in desert grassland translocation between crust and grassJ Ecol 2008 961076ndash85

[104] Porras-Alfaro A Herrera J Natvig DO Lipinski K Sinsabaugh RL Diversity and distribution ofsoil fungal communities in a semiarid grassland Mycologia 2011 10310ndash21

[105] Noy-Meir I Desert ecosystems environment and producers Annu Rev Ecol Syst 1973 425ndash51

[106] Reed SC Coe KK Sparks JP Housman DC Zelikova TJ Belnap J Changes to dryland rainfallresult in rapid moss mortality and altered soil fertility Nat Clim Change 2012 2752ndash5

[107] Steven B Kuske CR Gallegos-Graves LV Reed SC Belnap J Climate change and physicaldisturbance manipulations result in distinct biological soil crust communities Appl EnvironMicrobiol 2015 817448ndash59

[108] Ogle K Reynolds JF Plant responses to precipitation in desert ecosystems integrating func-tional types pulses thresholds and delays Oecologia 2004 141282ndash94

[109] Schwinning S Sala OE Hierarchy of responses to resource pulses in arid and semi-aridecosystems Oecologia 2004 141211ndash20

[110] Pointing SB Belnap J Disturbance to desert soil ecosystems contributes to dust-mediatedimpacts at regional scales Biodivers Conserv 2014 231659ndash67

[111] Evans J Geerken R Discrimination between climate and human-induced dryland degradationJ Arid Environ 2004 57535ndash54

[112] Dore MHI Climate change and changes in global precipitation patterns what do we knowEnviron Int 2005 311167ndash81

[113] Wall DH Virginia RA Controls on soil biodiversity insights from extreme environments ApplSoil Ecol 1999 13137ndash50

[114] Bowker MA Maestre FT Escolar C Biological crusts as a model system for examin-ing thebiodiversityndashecosystem function relationship in soils Soil Biol Biochem 201042405ndash17

Carlos Garcia JLMoreno T Hernandez and F Bastida2 Soils in Arid and Semiarid Environments

the Importance of Organic Carbon and MicrobialPopulations Facing the Future

Abstract Drylands occupy 47 of the Earthrsquos land area and accumulate 35ndash42 t car-bon (C) haminus1 In comparison to other biomes the natural depletion of C content in aridand semiarid lands harbors a high potential for carbon sequestration We provide acomprehensive review of carbon biogeochemistry the associated microbial commu-nities and strategies for soil restoration in drylands under the scope of global changeIn these areas the biogeochemistry of organic carbon is governed by climate condi-tions Photodegradation water availability and temperature overcontrol microbialactivity and hence carbon cycling Under limited water availability microbial activ-ity is diminished and hence the organic matter accumulation in soil increases but thedevelopment 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 ofbiosolids (composts sludges etc) Organic amendments promote an increase of soilorganic 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 soilprofiles with low organic carbon saturation seem to be a winndashwin option for seques-tering carbon and improving soil productivity This fundamental research is needed tobalance soil fertility and carbon sequestration particularly under the global changescenario

21 Introduction

Drylands occupy 631 times 109 ha or 47 of the Earthrsquos land area (UNEP 1992) and aredistributed among four climate zones hyperarid (10 times 109 ha) arid (162 times 109 ha)semiarid (237 times 109 ha) and dry subhumid (132 times 109 ha) Arid and semiarid orsubhumid zones are characterized by low and erratic rainfall periodic droughts anddifferent associations of vegetative cover and soils The annual rainfall varies from upto 350mm in arid zones to 700mm in semiarid areas

Desertification is the main problem that arid and semiarid lands face Within thecontext of Agenda 21 desertification is defined as ldquolanddegradation in arid semi-aridand dry subhumid areas resulting from climatic variations and human activitiesrdquo [1]Either due to human induced actions or natural conditions the loss of soil organicmatter (SOM) is strongly linked to soil degradation and desertification in arid andsemiarid areas and causes a decline in agronomical productivity and failure of soilecosystem services Although arid and semiarid ecosystems have less vegetation and

DOI 1015159783110419047-002

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Download Date | 9317 857 AM

16 | 2 Soils in Arid and Semiarid Environments

hence lower carbon accumulation than boreal or tropical areas they are estimated tocontain 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 are159ndash191 billion tons with a density of 35ndash42 (t C haminus1) If we compare the latter valuewith the values estimated for boreal (247ndash344 t C haminus1) tropical (121ndash113 t C haminus1) andtundra (121ndash127 t Chaminus1) ecosystems it is clear that soils under this climate are de-pleted in carbon both for ldquonaturalrdquo or ldquoanthropogenicrdquo reasons The hypothesis isthat these soils still have capacity for carbon sequestration whichwould increase soilquality ensure food security and mitigate global change [3]

The organic matter content of soils is subjected to strong and complex physicalchemical biochemical and biological controls that are ultimately responsible for car-bon stabilization and its mineralization [4 5] An alteration of such equilibriums dueto land use (ie tillage) [6 7] and climate pressures may alter the C stocks in soils andpotentially cause soil degradation hence affecting the sustainability of the planetThe degradation of soils due to carbon losses in many arid and semiarid areas of theplanet cannot be afforded in the future for two reasons1 Many of these areas are located in extensive agricultural zones (ie California

Israel southeastern Spain southern Italy Greece etc) andmust provide enoughfood for a growing population

2 The need for global change mitigation by C sequestration where these soils canplay 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 andtrends concerning the biogeochemistry of organic carbon and the intrinsic dynam-ics of microbial communities in soils developed under arid and semiarid conditionsThe role of organicmatter the significance of themicrobial biomass and the structureof microbial communities will be highlighted with special emphasis on soil restora-tion strategies and the application of methods that provide novel knowledge Finallywe reflect on the main gaps in our knowledge that should be addressed in order toincrease the ecological value of soils located in arid and semiarid areas in the future

22 Climate Regulation and Soil Organic Carbonin 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 inresponse to elevated CO2 concentration andwarming can accelerate the microbial de-composition of SOM and potentially lead to soil C losses [8] However at the global



23 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] Somestudies 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 hasbeen suggested that dryland soils wouldmost likely sequester Cwith a future increasein precipitation but release C with a decrease in precipitation [11]

Episodic water availability clearly affects element cycling in arid and semiaridecosystems [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 turnoverso organic matter tends to accumulate during dry periods when plant and micro-bial growth are restricted [14] Moreover drought affects the quality and compositionof humic acids which ndash biologically and chemically ndash are the most active fractionof SOM [15] Thus losses of aliphatic and polysaccharide-like structures secondaryamides polycondensed aromatic systems of large molecular size and other unsatu-rated bond systems such as carbonyl and carboxyl groups were observed in semiaridsoil humic acids after a long drought [14]

Soil processes in arid lands are controlled principally by water availability butthe photodegradation of above ground litter and the overriding importance of spatialheterogeneity are modulators of the biotic responses to water availability [16] Micro-biological soil properties are negatively affected by drought since soil moisture playsa key role in the survival and activity of soil microorganisms [14] Mechanisms such asthe retarded diffusion of soluble substrates andor reduced microbial mobility (andconsequent access to substrates) could explain the low microbial biomass found insoils 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 andmicrobial biomass in a semiarid temperate steppe Accordingly someauthorshave found that organic matter stocks are progressively preserved with the increasingduration and intensity of droughts [19] Conversely an experimental field study aboutthe impact of climate change on desertification along a Mediterranean arid transectdemonstrated that the SOM content decreased with aridity [20]

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

Adequate land use management helps to control the global stocks of organic carbonin 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 thereare still some discrepancies For instance the conversion of ecosystems from natu-ral conditions to agricultural use generally results in decreased carbon stocks in aridand semiarid climates [22 23] Disturbance by shrub removal andor livestock grazingsignificantly 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-




bon uptake in arid and semiarid areas is most often controlled by abiotic factors thatare not easily changed by management or vegetation In this sense photodegrada-tion which is highly intense in arid ecosystems exerts a dominant control on aboveground litter decomposition [27] Losses through photochemical reactions may repre-sent a short circuit in the carbon cycle with a substantial fraction of the carbon fixedin plant biomass being lost directly to the atmosphere without cycling through soilorganic matter pools [27] More studies based on the prevention of photodegradationshould be carried out to promote carbon sequestration in soil and climate changemit-igation For instance the placement of a wide vegetation cover may reduce the effectsof photodegradation and enhance soil moisture

Reforestation may influence carbon balances increase soil carbon stocks andserves 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 spatialheterogeneity 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 ofislands of fertility under shrubs [32]

24 Soil Restoration in Arid-Semiarid ZonesAmendments Based on Exogenous Organic Matter

The scant vegetation of the soils in arid and semiarid zones which ismainly a result oflow productivity and subsequent abandonment causes the inputs of organic matterinto the soil to be low Hence together with the usual soil erosive processes and highphotodegradation rates many soils have a low organic matter level which compro-mises their functionality and the provision of ecosystem services and can even end inintense degradation phenomena

Since the Kyoto Protocol of 1992 which identified soils as a possible sink for car-bon there has beenmuchprogress A report on organicmatter and biodiversitywithinthe European Thematic Strategy [33] mentions that exogenous organic matter that isorganicmaterials added to a degraded soil in order to improve harvests or restore it forsubsequent use constitutes an invaluable source of organic matter and contributes tothe fixation of C in the soil thus partially diminishing the greenhouse effect derivedfrom 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 byincreasing soil porosity and water retention because of the presence of humic-likesubstances known as a polycondensed macromolecular structure In addition oneof the beneficial effects of humic substances is that soil enzymes bound to humic frac-tions remain protected in the long termagainst denaturalization by proteolysis attacks



25 Microbial Biomass and Enzyme Activity in Arid-Semiarid Zones | 19

in soil The use of organic amendments to improve soil quality and restore degradedlands has been widespread [34ndash36] 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 progressiveplant growth [40 41] Plant inputs to soil promote the development of the microbialbiomass and its activity which raises soil fertility in the long term [36 42 43] Differenttypes of organic amendments have been applied in arid and semiarid environmentscrop residues pig slurry farmyard manure municipal solid waste olive mill wastesewage sludge etc However the addition of organic amendments to soil has to becarried out carefully since it does not always lead to an increase in soil quality Forinstance Tejada et al (2007) [44] reported that the application of fresh beet vinasseworsened 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 thatmay persist in the soil The stability and nature of the amendment can determine theresidence time of the added organic carbon [45 46] In dryland ecosystems due to thehigh 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 (ietexture) than by the quality of the organic amendment [47 48] It is thought that finesoil particles have a critical role in C fixation Some authors observed an increase inthe 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 havealso suggested a protective role of clays [50 51] even concluding that there is majorfixation of carbon in clay soils despite the highly labile nature of added carbon (ie13C-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 theimprovement in the nutritional conditions of the soil ndash which enhances subsequentplant growth (998835 Fig 21) Plant development provides organic matter to the soil bene-fits its structure and avoids soil erosion a very important issue in sloping areas [36]

25 Microbial Biomass and Enzyme Activity in Arid-Semiarid Zones

As stated above the microbial biomass is largely responsible for soil carbon cyclingThe microbial biomass of semiarid soils is usually constrained by the low amountsof plant inputs and water availability The evaluation of microbial biomass by phos-pholipid fatty acids (PLFAs) analysis revealed that the total PLFAs ranged between 22and 100 nmol fatty acids gminus1 soil in arid and semiarid areas [41 52ndash55] Neverthelessthe 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




18 months after organic amendment restoration

Fig 21 Field experiment in Spain soil restoration

degradation [56] Hence the results obtained following treatment might be biased bythe previous viable microbial community

Generally the level of biomass correlates well with the amount of organic carbonand is closely related to themoisture content of dryland soils For instance various au-thors have observed changes in themicrobial biomass linked to the organic carbon af-ter a change in land use [57 58] Similarly the restoration of soil quality by addition oforganic waste byproducts increases the microbial biomass 16ndash3 times [41] Themicro-bial biomass also responds to plant growth and the parallel increase in SOM [52 55] Indetail Ben-David et al (2011) [52] found that the fatty acid 161w7 indicative of cyano-bacteria [59] increased in intershrub soils of the Negev Desert (Israel) this suggestsan increase in the relative abundance of cyanobacteria which are known to be theprimary 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 structureand functioning of soil bacterial communities and leads to a slowing down of N andC mineralization [14 61] For soils that have not received recent organic matter addi-tions wetndashdry cycles initially stimulate C and net N mineralization and diminish themicrobial biomass during drying but stimulate microbial growth after wetting andthe wetndashdry cycle itself results in higher net N and C mineralization when comparedto 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 filmsof dry soil and because sinks of inorganic N are limited by reduced microbial growthand limited plant uptake [14 64] A portion of the microbial biomass is killed underdry conditions [65] this is readily decomposed by surviving organisms when the soil




is rewetted This deadmicrobial biomass with its low CN ratio becomes available formicrobial activity and leads to high Nmineralization large pulses of CO2 and gaseousfluxes of N and a pulse of increased C and N availability

In principle as stated by Entry et al (2004) [57] Gram positive biomarkers wouldbe 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 pulsesmight be takeninto 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 thedry 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 extracellularmicroenvironment where they canbeprotected by immo-bilization in humic and clay colloids [67 68] The basic importance of enzyme activityin soil lies in the fact that ecosystem functioning cannot be totally understood with-out the participation of enzymatic processes and their catalytic reactions related tonutrient cycling [69] Extracellular enzymes are closely related to organic matter de-composition and key enzymatic reactions include those involved in the degradationof cellulose and lignin those that hydrolyze reservoirs of organic N such as proteinschitin and peptidoglycan and those that mineralize P from nucleic acids phospho-lipids and other ester phosphates [70] Extracellular enzyme activity (EEA) mediatesmicrobial nutrient acquisition from organic matter and these activities are commonlyinterpreted as indicators ofmicrobialnutrient demand and soil quality [69 71] In gen-eral enzymes are associated with viable proliferating cells but they can be excretedfrom a living cell or released into the soil solution from dead cells Once enzymes haveleft the shelter of the cell they are exposed to an inhospitable environment in whichnonbiological denaturalization adsorption inactivation and degradation by prote-olytic microorganisms all conspire to harm the enzymes unless they survive due tothe new protection afforded by the mineral andor humic association which is moreresistant to proteolysis than the free enzymes

In arid and semiarid environments the soil EEA has been used to examine thefunctional 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 [75ndash77] plant diversity [78] type of agroecosystem [79] and climatechange [80]

More than any other factor OM dynamics are closely related to the regulation ofenzyme activity In arid and semiarid areas the potential activities of enzymes thatdecompose proteins (eg aminopeptidase) and recalcitrant C compounds such aslignin and humic substances (eg phenol oxidases) exceed those of mesic soils bymore 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 ofmesic soils [81] The pH is a strong regulator of EEA with important consequences for




SOMdynamics Because of carbonate accumulation the pHof arid soils can reach 8 orabove which is optimal for phenol oxidase enzymes [82] In contrast the pH optimaof glycosidases (eg cellulase chitinase) generally range from 4 to 6

Soil texture and moisture also determine the enzyme activity by influencing themicrobial 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] Becauserewetting sometime results in a pulse of microbial biomass turnover [84 85] manyintracellular enzymes may be released into the soil creating a temporary increase inEEA 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]

26 Organic Carbon Macro and Microaggregatesand C Sequestration in Arid-Semiarid Zones

Converting forest to cultivated areas reduces soil organic carbon mainly through thereduction of biomass inputs into the soil and the stimulation of soil organic mattermineralization 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 carbonin a climatic change scenario with increased temperature and a decrease in rainfallas is expected in semiarid areas Some data indicate that this negative impact on soilorganic carbonwouldbegreater in soil surface than in the soil subsurface For this rea-son a strategy for C sequestration should be focused on subsoil sequestration Appro-priatemanagement practice in cropland and shrubland which have deep soil profileswith low organic carbon saturation seems to be a winndashwin option for sequesteringatmospheric organic carbon and improving soil productivity

Some studies confirm that the potential sequestration of C in semiarid reforestedareas depends largely on the techniques used for reforestation The C stocks in refor-ested ecosystems are directly proportional to the amount of biomass producedwhichin turn is determined by the productivity of the soil For this reasonmethods that im-prove the productivity of the soil must be used The addition of organic amendmentsto 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 theaddition of organic amendments to these soils increases the percentage of both soilmacroaggregates andmicroaggregateswithinmacroaggregates aswell 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



27 Conclusion | 23

term [91 92] Other authors have reported an increase of C concentration in fine soliparticles (silt and clay) with the addition of organic amendment to semiarid degradedsoils [49 93]

In semiarid and arid soils the chemical stabilization of organic carbon throughthe formation of complexes with silt and clay particles and their physical protectionin microaggregates formed within macroaggregates could be the main mechanismof C sequestration in these soils in both agricultural and forest areas The physicalprotection of soil organic carbon could be promoted by the changes both qualitativeand 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 increasein the labile pool of soil organic carbon occur [94] Fresh plants induce the formationof macroaggregates both directly by acting as a binding agent between soil particlesand indirectly by activating the production ofmicrobially derived binding agents Theestablishment 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 withinthem [94]

A strong positive correlation between basal soil respiration and the percentageof microaggregates within macroaggregates has been found in reforested soils whilethis 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 defensemechanism of the soil to protect organic carbon from increased microbiological activ-ity [96] for these reasons these correlations could serve as indicators of processes ofimprovement (positive correlations) or degradation (negative correlation) of the soil

27 Conclusion

Soil degradation due to aggressive human action or passive climate pressure must beavoided in order to conserve soils that have a high ecological value for the future Thefragility of these soils contrasts with their intense response to soil restoration pro-grams which include the addition of organic matter and their potential capacity forcarbon sequestration Organic amendments help to preserve and improve the qualityand fertility of the soils in these areas which could be particularly important under aglobal change scenario

The biogeochemical and microbiological information on arid and semiarid soilsis abundant but perhapsmore limited than that for other climates Nevertheless suchstudies are widespread across the planet and numerous research groups are focusedon the topic This fact will increase our knowledge of the biogeochemistry of carbon




as well as our capacity for managing the cycling of elements and the sustainability ofarid and semiarid soils in the future

However if we aim to increase such an ldquoecological capitalrdquo soil sciencemust nec-essarily move on and search for answers to new more focused questions1 Which biochemical processes are responsible for carbon fixation and humus forma-

tion2 Are we able to ldquocontrolrdquo the microbial populations and carbon related biochemical

reactions of these soils

Themutual benefits of microbial activity carbon sequestration and plant growth areclear in terms of sustainability To enhance the physicochemical protection of soil or-ganic carbon the stability of microaggregates should be maximized while ensuring asuitable rate of macroaggregate turnover that will allow the fixation of new organiccarbon This could be promoted byminimum tillage an increase of plant inputs par-ticularly root inputs (by modifying residue amount and quality altering mycorrhizalassociations 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 ldquoagrave la carterdquo organic amendments which promote a punctual rise in fertilitywhen needed (ie an increase in agricultural productivity) or foster carbon sequestra-tion for environmental purposes in abandoned lands at a particular moment woulddefinitively increase the ecological value of arid and semiarid soils in the coming era

Acknowledgment F Bastida thanks the Spanish Government for his ldquoRamoacuten y Ca-jalrdquo contract (RYC-2012-10666) and FEDER founding The authors are grateful to theFundacioacuten Seacuteneca of Murcia Region (19896GERM15) The authors thank the Span-ish Ministry for the CICYT projects AGL2014-55269-R and AGL2014-54636

References

[1] UNCED Managing fragile ecosystems Combating desertification and drought (Rio de Janeiro3ndash14 June 1992) Report of the United Nations Conference on Environment and DevelopmentGeneral ACONF15126 (Vol II) Chapter 12 (httpwwwunccdch)

[2] Rasmussen C Southard RJ Howarth WR Mineral control of organic carbon mineralization in arange of temperate conifer forest soils Global Change Biol 2006 12834ndash47

[3] Lal R Soil carbon sequestration impacts on global climate change and food security Science2004 3041623ndash26

[4] Six J Conant RT Paul EA Paustian K Stabilization mechanisms of soil organic matter Implica-tions for C-saturation of soils Plant Soil 2002 241155ndash76



References | 25

[5] von Lutzow M Koegel-Knabner I Ekschmitt K Matzner E Guggenberger G Marschner B FlessaH Stabilization of organic matter in temperate soils mechanisms and their relevance underdifferent soil conditions ndash a review Eur J Soil Sci 2006 57426ndash45

[6] Kandeler E Stemmer M Klimanek EM Response of soil microbial biomass urease and xy-lanase within particle size fractions to long-term soil management Soil Biol Biochem 199931261ndash73

[7] Conant RT Six J Paustian K Land use effects on soil carbon fractions in the southeasternUnited States II Changes in soil carbon fractions along a forest to pasture chronosequenceBiol Fertil Soils 2004 40194ndash200

[8] Nie M Pendall E Bell C Gasch CK Raut S Tamang S Wallenstein MD Positive climate feed-backs of soil microbial communities in a semi-arid grassland Ecol Lett 2013 16234ndash41

[9] Giardina CP Ryan MG Evidence that decomposition rates of organic carbon in mineral soil donot vary with temperature Nature 2000 404858ndash61

[10] Jones C McConnell C Coleman K Cox P Fallon P Jenkinson D Powlson Global climate changeand soil carbon stocks predictions from two contrasting models for the turnover of organiccarbon in soil Global Change Biol 2005 11154ndash66

[11] Albaladejo J Ortiz R Garciacutea-Franco N Ruiz-Navarro A Almagro M Garciacutea-Pintado J Martiacutenez-Mena M Land use and climate change impacts on soil organic carbon stocks in semi-aridSpain J Soil Sediment 2013 13265ndash77

[12] Austin AT Yahdjian L Stark JM Belnap J Porporato A Norton U Ravetta DA Schaeffer SMWater pulses and biogeochemical cycles in arid and semiarid ecosystems Oecologia 2004141221ndash35

[13] Collins SL Sinsabaugh RL Crenshaw C Green L Porras-Alfaro A Sutrsova M Zegkin LH Pulsedynamics and microbial processes in aridland ecosystems Journal of Ecology 2008 96413ndash20

[14] Hueso S Garciacutea C Hernaacutendez T Severe drought conditions modify the microbial communitystructure size and activity in amended and unamended soils Soil Biol Biochem 2012 50167ndash73

[15] Buurman P Nierop KGJ Kaal J Senesi N Analytical pyrolysis and thermally assisted hydrolysisand methylation of EUROSOIL humic acid samples ndash A key to their source Geoderma 200915010ndash22

[16] Austin AT Has water limited our imagination for aridland biogeochemistry Trends Ecol Evol2011 26229ndash35

[17] van Meeteren MJM Tietema A van Loon EE Verstraten JM Microbial dynamics and litter de-composition under a changed climate in a Dutch heathland Appl Soil Ecol 2008 38119ndash27

[18] Liu W Zhang Z Wan S Predominant role of water in regulating soil and microbial respirationand their responses to climate change in a semiarid grassland Global Change Biol 200915184ndash95

[19] Borken W Matzner E Reappraisal of drying and wetting effects on C and N mineralization andfluxes in soils Global Change Biol 2009 15808ndash24

[20] Lavee H Imeson AC Sarah P The impact of climate change on geomorphology and desertifica-tion along a Mediterranean-arid transect Land Degrad Dev 1998 9407ndash22

[21] de Baets S Meersmans J Vanacker V Quine TA van Oost K Spatial variability and change insoil organic carbon stocks in response to recovery following land abandonment and erosion inmountainous drylands Soil Use Manage 2012 2965ndash76

[22] Steffens M Koumllbl A Totsche KU Koumlgel-Knabner I Grazing effects on soil chemical and physicalproperties in a semiarid steppe of Inner Mongolia (PR China) Geoderma 2008 14363ndash72

[23] Peacuterez-Quezada JF Delpiano CA Snyder KA Johnson DA Franck N Carbon pools in an aridshrubland in Chile under natural and afforested conditions J Arid Environ 2011 7529ndash37




[24] Daryanto S Eldridge DJ Throop HL Managing semi-arid woodlands for cabon storage Grazingand shrub effects on above- and belowground carbon Agr Ecosyst Environ 2013 1691ndash11

[25] Seddaiu G Porcu G Ledda L Roggero PP Agnelli A Corti G Soil organic matter content andcomposition as influenced by soil management in a semi-arid Mediterranean agro-silvo-pastoral system Agr Ecosyst Environ 2013 1671ndash11

[26] Booker K Huntsinger L Bartolome JW Sayre NF Stewart W What can ecological science tellus about opportunities for carbon sequestration on arid rangelands in the United States GlobEnviron Change 2013 23240ndash51

[27] Austin AT Vivanco Plant litter decomposition in a semi-arid ecosystem controlled by pho-todegradation Nature 2006 442555ndash58

[28] Harper RJ Okom AEA Stilwell AT et al Reforesting degraded agricultural landscapes with Eu-calypts Effects on carbon storage and soil fertility after 26 years Agr Ecosyst Environ 20101633ndash13

[29] Hu YL Zeng DH Chang SX Mao R Dynamics of soil and root C stocks following afforestation ofcroplands with poplars in a semi-arid region in northeast China Plant Soil 2013 368619ndash27

[30] Garciacutea C Hernaacutendez T Roldaacuten A Martiacuten A Effect of plant cover decline on chemical microbio-logical parameters under Mediterranean climate Soil Biol Biochem 2002 34635ndash42

[31] Garciacutea C Roldaacuten A Hernaacutendez T Ability of different plant species to promote microbiologicalprocesses in semiarid soil Geoderma 2005 124193ndash202

[32] Schlesinger WH Raikks JA Hartley AE Cross AF On the spatial pattern of soil nutrients indesert ecosystems Ecology 1996 77364ndash74

[33] van Camp L Bujarrabal B Gentile AR et al Reports of the Technical Working Groups Estab-lished under the Thematic Strategy for Soil Protection EUR 21319 EN3 Luxembourg Office forOfficial Publications of the European Communities 2004 1ndash872

[34] Garciacutea C Hernaacutendez T Costa F Variation in some chemical parameters and organic matter insoils regenerated by the addition of municipal solid-waste Environ Manage 1992 16763ndash68

[35] Tejada M Hernaacutendez MT Garciacutea C Application of two organic amendments on soil restorationEffects on the soil biological properties J Environ Qual 2006 351010ndash17

[36] Bastida F Moreno JL Garcia C Hernandez T Addition of urban waste to semiarid degradedsoil Long-term effect Pedosphere 2007 17557ndash67

[37] Albiach R Canet R Pomares F Ingelmo F Organic matter components and aggregate stabilityafter the application of different amendments to a horticultural soil Bioresour Technol 200176125ndash29

[38] Albaladejo J Castillo V Diacuteaz E Soil loss and runoff on semiarid land as amended with urbansolid refuse Land Degr Develop 2000 16551ndash59

[39] Caravaca F Masciandaro G Ceccanti B Land use in relation to soil chemical and biochemicalproperties in a semiarid Mediterranean environment Soil Tillage Res 2002 6823ndash30

[40] Garciacutea C Hernaacutendez T Albaladejo J Castillo V Roldaacuten A Revegetation in semiarid zones influ-ence of terracing and organic refuse on microbial activity Soil Sci Soc Am J 1998 62670ndash76

[41] Bastida F Kandeler E Moreno JL Ros M Garcia C Hernandez T Application of fresh and com-posted organic wastes modifies structure size and activity of soil microbial community undersemiarid climate Appl Soil Ecol 2008 40318ndash29

[42] Ros M Hernaacutendez MT Garciacutea C Soil microbial activity after restoration of a semiarid soil byorganic amendments Soil Biol Biochem 2003 35463ndash69

[43] Bastida F Hernaacutendez T Albaladejo J Garciacutea C Phylogenetic and functional changes in themicrobial community of long-term restored soils under semiarid climate Soil Biol Biochem2013 6512ndash21



References | 27

[44] Tejada M Moreno JL Hernaacutendez MT Garciacutea C Application of two beet vinasse forms in soilrestoration Effects on soil properties in an and environment in southern Spain Agr EcosystEnviron 2007 119289ndash98

[45] Kiem R Koumlgel-Knabner I Contribution of lignin and polysaccharides to the refractory carbonpool in C-depleted arable soils Soil Biol Biochem 2003 35101ndash18

[46] Abiven S Menasseri S Chenu C The effects of organic inputs over time on soil aggregate sta-bility ndash A literature analysis Soil Biol Biochem 2009 411ndash12

[47] Gentile R Vanlauwe B Six J Litter quality impacts short- but not long-term soil carbon dynam-ics in soil aggregate fractions Ecol Appl 2011 21695ndash703

[48] Nicolaacutes C Hernaacutendez T Garciacutea C Organic amendments as strategy to increase organic matterin particle-size fractions of a semi-arid soil Appl Soil Ecol 2012 5750ndash58

[49] Garciacutea E Garciacutea C Hernaacutendez T Evaluation of the suitability of using large amounts of urbanwastes for degraded arid soil restoration and C fixation Eur J Soil Sci 2012 63650ndash58

[50] Bastida F Torres IF Hernaacutendez T Bombach P Richnow HH Garciacutea C Can the labile carbon con-tribute to carbon immobilization in semiarid soils Priming effects and microbial communitydynamics Soil Biol Biochem 2013 57892ndash902

[51] Helgason BL Gregorich EG Janzen HH Ellert BH Lorenz N Dick RP Long-term microbial reten-tion of residue C is site-specific and depends on residue placement Soil Biol Biochem 201468231ndash40

[52] Ben-David EA Zaady E Sher Y Nejidat A Assessment of the spatial distribution of soil micro-bial communities in patchy arid and semi-arid landscapes of the Negev Desert using combinedPLFA and DGGE analyses FEMS Microbiol Ecol 2011 76492ndash503

[53] Cotton J Acosta-Martiacutenez V Moore-Kucera J Burow G Early changes due to sorghum biofuelcropping systems in soil microbial communities and metabolic functioning Biol Fertil Soils2012 49403ndash13

[54] Drenovsky RE Steenwerth KL Jackson LE Scow KM Land use and climatic factors structureregional patterns in soil microbial communities Glob Ecol Biogeogr 2010 1927ndash39

[55] Hortal S Bastida F Armas C Lozano YM Moreno JL Garciacutea C Pugnaire FI Soil microbial com-munity under a nurse-plant species changes in composition biomass and activity as the nursegrows Soil Biol Biochem 2013 64139ndash46

[56] Lester ED Satomi M Ponce A Microflora of extreme arid Atacama Desert soils Soil BiolBiochem 2007 39704ndash08

[57] Entry JA Fuhrmann JJ Sojka RE Shewmaker GE Influence of irrigated agriculture on soil car-bon and microbial community structure Environ Manage 2004 33363ndash73

[58] Jia GM Zhang PD Wang G Cao J Han JC Huang YP Relationship between microbial communityand soil properties during natural succession of abandoned agricultural land Pedosphere2010 20352ndash60

[59] Potts M Olie JJ Nickels JS Parsons J White DC Variation in Phospholipid Ester-Linked FattyAcids and Carotenoids of Desiccated Nostoc commune (Cyanobacteria) from Different Geo-graphic Locations Appl Environ Microbi 1987 534ndash9

[60] Belnap J Lange OL Biological Soil Crust Structure Function and Management BerlinSpringer-Verlag 2001 5ndash12

[61] Griffiths RI Whiteley AS OrsquoDonnell AG Bailey MJ Physiological and community responsesof established grassland bacterial populations to water stress Appl Environ Microb 2003696961ndash68

[62] Fierer N Schimel JP Effects of drying-rewetting frequency on soil carbon and nitrogen transfor-mations Soil Biology and Biochemistry 2002 34777ndash787

[63] Huxman TE Snyder KA Tissue D et al Precipitation pulses and carbon fluxes in semiarid andarid ecosystems Oecologia 2004 141254ndash68




[64] Stark JM Firestone MK Mechanisms for soil moisture effects on activity of nitrifying bacteriaAppl Environ Microb 1995 61218ndash21

[65] Bottner P Response of microbial biomass to alternate moist and dry conditions in a soil incu-bated with 14C- and 15N-labelled plant material Soil Biol Biochem 1985 17329ndash37

[66] Kieft TL Soroker E Firestone MK Microbial biomass response to a rapid increase in waterpotential when dry soil is wetted Soil Biol Biochem 1987 19119ndash26

[67] Ceccanti B Nannipieri P Cerveli S Sequi P Fractionation of humus-urease complexes Soil BiolBiochem 1978 1039ndash45

[68] Bastida F Jindo K Moreno JL Hernaacutendez T Garciacutea C Effects of organic amendments on soilcarbon fractions enzyme activity and humus-enzyme complexes under semi-arid conditionsEur J Soil Biol 2012 5394ndash102

[69] Nannipieri P Grego S Ceccanti B Ecological significance of the biological activity in soils InBollag JM ed Stotzky G 2nd edn New York Marcel Dekker 1990 293ndash355

[70] Sinsabaugh RL Lauber CL Weintraub MN et al Stoichiometry of soil enzyme activity at globalscale Ecol Lett 2008 111252ndash64

[71] Bastida F Moreno JL Hernaacutendez T Garciacutea C Microbiological degradation index of soils in asemiarid climate Soil Biol Biochem 2006 383463ndash73

[72] Sinsabaugh RL Gallo ME Lauber CL Waldrop M Zak DR Extracellular enzyme activities andsoil carbon dynamics for northern hardwood forests receiving simulated nitrogen depositionBiogeochemistry 2005 75201ndash15

[73] Moreno JL Hernaacutendez T Garciacutea C Effects of a cadmium-contaminated sewage sludge com-post on dynamics of organic matter and microbial activity in an arid soil Biol Fertil Soils 199928230ndash37

[74] Pascual JA Garciacutea C Hernaacutendez T Ayuso M Changes in the microbial activity of an arid soilamended with urban organic wastes Biol Fertil Soils 1997 24429ndash34

[75] Madejon E Moreno F Murillo JM Pelegrin F Soil biochemical response to long-term conserva-tion tillage under semi-arid Mediterranean conditions Soil Till Res 2007 94346ndash52

[76] Moreno B Garciacutea-Rodriacuteguez S Cantildeizares R Castro J Beniacutetez E Rainfed olive farming in south-eastern Spain Long-term effect of soil management on biological indicators of soil quality AgrEcosyst Environ 2009 131333ndash39

[77] Melero S Lopez-Bellido RJ Lopez-Bellido L et al Stratification ratios in a rainfed Mediter-ranean Vertisol in wheat under different tillage rotation and N fertilisation rates Soil Till Res2012 1197ndash12

[78] Gonzaacutelez-Polo M Austin AT Spatial heterogeneity provides organic matter refuges for soilmicrobial activity in the Patagonian steppe Argentina Soil Biol Biochem 2009 411348ndash51

[79] Acosta-Martinez V Acosta-Mercado D Sotomayor-Ramirez D Cruz-Rodriguez L Microbial com-munities and enzymatic activities under different management in semiarid soils Appl Soil Ecol2008 38249ndash60

[80] Henry HAL Soil extracellular enzyme dynamics in a changing climate Soil Biol Biochem 20124753ndash59

[81] Stursova M Sinsabaugh RL Stabilization of oxidative enzymes in desert soil may limit organicmatter accumulation Soil Biol Biochem 2008 40550ndash53

[82] Sinsabaugh RL Carreiro MM Repert DA Allocation of extracellular enzymatic activity in rela-tion to litter composition N deposition and mass loss Biogeochemistry 2002 601ndash24

[83] Burns RG DeForest JL Marxsen J et al Soil enzymes in a changing environment Current knowl-edge and future directions Soil Biol Biochem 2013 58216ndash34

[84] Fierer N Schimel JP A proposed mechanism for the pulse in carbon dioxide production com-monly observed following the rapid rewetting of a dry soil Soil Sci Soc Am J 2003 67798ndash805



References | 29

[85] Schimel J Balser TC Wallenstein M Microbial stress-response physiology and its implicationsfor ecosystem function Ecology 2007 881386ndash94

[86] Bell TH Henry HAL Fine scale variability in soil extracellular enzyme activity is insensitive torain events and temperature in a mesic system Pedobiologia 2011 54141ndash46

[87] Albaladejo J Ortiz R Garcia-Franco N Ruiz-Navarro A Almagto M Garcia-Pintado J Martinez-Mena M Land use and climate change impacts on soil organic carbon stock in semiarid spainJ Soil Sediments 2012 13265ndash277

[88] Martinez-Mena M Lopez J Almagro M Boix-Fayos C Albaladejo J Effect of water erosion andcultivation on the soil carbon stock in a semiarid area of South-East Spain Soil till Res 200899119ndash129

[89] Maestre FT Cortina J Are Pinus halepensis plantations useful as a restoration tool in semiaridMediterranean areas Forest Ecol Manag 2004 198303ndash317

[90] Nicolaacutes C Kennedy JN Hernaacutendez T Garciacutea C Six J Soil aggregation in a semiarid soilamended with composted and non-composted sewage sludge- A field experiment Geoderma2014 219ndash22024ndash31

[91] Six J Elliot ET Paustian K Doran JW Aggregation and soil organic matter accumulation in culti-vated and native grassland soils Soil Sci Soc Am J 1998 621367ndash1377

[92] Gale WJ Cambardella CA Bailey TB Root-derived carbon and the formation and stabilization ofaggregates Soil Sci Soc Am J 2000 64201ndash207

[93] Caravaca F Lax A Albaladejo J Soil aggregate stability and organic matter in clay and fine siltfractions in urban refuse-amended semiarid soils Soil Sci Soc Am J 2001 651235ndash1238

[94] Lopez-Garrido R Madejon E Leon-Camacho M Giron I Moreno F Murillo JM Reduced tillageas an alternative to no tillage under Mediterranean conditions a case study Soil Till Res 201414040ndash47

[95] Six J Bossuyt H Degryze S Denef K A history of research on the link between (micro) aggre-gates soil biota and soil organic matter dynamics Soil Till Res 2004 797ndash31

[96] Garcia-Franco N Carbon sequestration mechanisms in semiarid soils according to lnad useand management practices Doctoral Thesis Murcia University (Spain) 2014 186 pp



Gary M King3 Water Potential as a Master Variable

for AtmospherendashSoil Trace Gas Exchangein Arid and Semiarid Ecosystems

Abstract Soilwater status strongly affects qualitative and quantitative aspects of soilndashatmosphere trace gas exchange Soil water status is most often expressed in termsof gravimetric water contents which can be particularly useful when translated togas filled pore space Gas filled pore space has predictive value for both gas transportrates and the types of processes involved in gas production and consumption How-ever water potential offers deeper insights that reflect the physiological responses ofcells while also providing a basis for comparing activities among different soil typesand across wetting and drying events Nonetheless relatively few studies have incor-porated water potential measurements with analyses of trace gas fluxes Results foratmospheric methane uptake suggest similar sensitivities to water potential for aridsoils and forest soils with strong inhibition below minus05MPa Atmospheric CO uptakein 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 atremarkably low potentials Advances in sensor design should facilitatemuchmore ex-tensive analyses of water potential more mechanistic models of trace gas exchangeand a better understanding of the controls trace gas dynamics

31 Introduction

Water plays a profoundly important role in soilndashatmosphere gas exchange [1ndash6] Wa-ter shapes plant communities litter development the presence and characteristics ofsoil horizons soil organic matter content microbial community composition struc-ture and activity soil texture porosity and gas transport [7] All of these variablesinteract with water regimes to determine rates of gas emission to or uptake from theatmosphere

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 contemporaryhydrologic regimes For example the playa soils of the northwestern United States aremostly remnants of extensive Pleistocene lakes that disappeared as a consequence ofglobal climate change (eg Lake Bonneville) leaving behind fine grained sedimentbeds that progressively evolved in response to sparse plant colonization and stronglyseasonal patterns of temperature and precipitation [8]

Although water limitations often lead to relatively low rates of gas exchange perm2 soils in arid and semiarid ecosystems can still play significant roles in some global

DOI 1015159783110419047-003



32 | 3 Water Potential as a Master Variable for AtmospherendashSoil 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 substantiallyless than it would be if uptake rates in arid systems were equivalent to those in grass-lands and forests Likewise global uptakeof atmospheric carbonmonoxide is reducedby 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 [12ndash17] Climate change for instancemay result in increased thermal stress andprolongedperiods of drought punctuated by extreme precipitation Irrigation for agriculture hasresulted 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 exchangein arid systems soil water potential is arguably the most important Water potentialwhich is a measure of water availability affects gas production and consumption atthe level of cells and elicits immediate responses as it changes through its impacton cell physiology [19] However in spite of its importance relationships betweentrace gas dynamics and water potential have not been characterized extensively Anoverview of these relationships and recent observations are summarized here

32 Water Potential and Water Potential Assays

Although several weight or volume based indices provide convenient measures of soilwater content (eg [20]) and are useful in the context of variables such as gas dif-fusion and advection (eg [21 22]) they provide little insight about the physiologi-cal responses of microbes to soil water status and often cannot be directly comparedamong systems [23] In contrast soil water status can be more completely specifiedusing physical chemical terms (eg [19 24 25]) The rationale for using a physicalchemical description of water as an alternative to volumetric measures is simple Thedirection of water movement across cell membranes cannot be predicted on the basisof 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 + ni)

with nw representing number of moles of water kgminus1 of solvent (= molality about5551mol kgminus1 or 5551m) and ni representing the moles of solute kgminus1 of solventSince 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



32 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 25degC Though there are some advantages to a temperature independentmeasure of water status water activity itself does not necessarily predict directions ofwater flow and it is inadequate for complex multiphase systems such as soil Waterpotential provides a more complete measure of water availability

Water potential is defined in energetic terms as the partial molal free energy ofa solution of water under specified conditions of solute composition temperaturepressure and gravitational potential

μw = (partGpartnw)ni TPh

where G represents Gibbs free energy ni is solute concentration P is pressure andh is height (ignored in most biogeochemical contexts [23]) This yields a working ex-pression for the chemical potential of water

μw = μ0w + RT ln aw + VwP

where μ0w represents the chemicalpotential ofwater 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 partialmolal volume of water (about 18times10minus5 m3 molminus1 at 25degC)Rearranging yields

(μw minus μ0w)Vw = RT ln awVw + P

where the left hand expression is a chemical potential difference per molal volumeand is designated water potential ψ

ψ = RT ln awVw + P

This expression indicates that water potential in a solution can be subdivided into apressure 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 lt 0 and is expressed in unitsof bars or pascals (Nmminus2) Unlike water activity or other measures of water status Ψprovides a complete description that can be compared among systems and used topredict the direction of water flows for example into or out of cells

The matric potential term ψm is especially relevant in soils This potential arisesas a result of the interaction of water at surfaces in a porous matrix and has beendescribed by analogy to the behavior of water inside a capillary tube immersed in purewater The force associated with the rise of water a distance h in a capillary is related




to the matric potential within the capillary (= hρg where ρ is water density [kgmminus3]and g is the gravitational constant [m secminus2]) the height of capillary rise is inverselyproportional to the capillary radius r Soil is essentially a porous matrix in which thematric potential is related to pore size (ie pore radius) and the distribution of wateramongpores (a functionofwater content)Whenall pores are filled (water saturation)the matric potential is zero The matric potential decreases with desaturation due tothe loss of water from larger pores and retention in smaller pores Progressive lossleaves the remaining water in smaller pores at progressively lower potentials

The relationship between water potential and soil pore size distribution has anumber of important consequences especially for gas exchange With decreasingwa-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 Howeverwater potentials lower than about minus05MPa typically inhibit many bacterial activitiesdue to physiological stresses physical constraints on substrate transport cell move-ment and the thickness of films available for bacterial immersion This limitation isespecially relevant for arid soils which often experience water potentials much lessthan minus05MPa

Soil water content can be measured readily using relatively simple gravimetricmethods [28] Modifications of these methods yield additional indices of soil porespacewhich can aid analyses of soilndashatmosphere gas exchange Severalmethods andassociated instrumentation are also available for analyses of thewater potential How-ever the choice of method depends greatly on the application Methods suitable foruse in a laboratory context often are unsuited for field use and vice versa It is also im-portant to understandwhether solute potentials matric potentials or both need to bemeasured since this influencesmethod selection Finally the range of expected waterpotentials must be considered For arid soils the range can potentially exceed limitsfor any one analytical system since values can approximate zero during wet seasonsor immediately after precipitation events but fall below minus100MPa with drying

For laboratorymeasurements andwater potentials fromaboutminus2kPa tominus500kPaa pressure plate apparatus can be used (eg [29]) Pressure plates essentially applypressure to a soil sample and drive excess water out through a porous ceramic plateAt 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 determinationsat different pressures is then used to construct a moisture release curve that in turnis used to estimate sample potentials at their initial water contents Other than itssimplicity this approach has little to recommend it since other methods offer greateraccuracy broader ranges and more convenience

Tensiometers which make direct contact with the soil liquid phase find usein both laboratory and field contexts [30] These instruments use a porous ceramicreservoir containing pure water (sim0MPa) in contact with a headspace and a pressuretransducer or vacuumgauge When placed in soil with water at lower potential waterflowing from the reservoir results in a reduced headspace pressure equivalent to the



33 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 dynamicrange (gt minus1kPa to about minus100kPa) substantially limits applications in arid systemsHowever a new microtensiometer might greatly extend these limits [31]

An alternative approach that is well suited for laboratory applications measuresthe energy status of water in a vapor phase equilibrated with a soil sample Dew pointhygrometry has found a wide range of applications since it is suitable for sampleswith water potentials from about minus01MPa to lt minus100MPa [32 33] As implementedby Decagon Instruments (Pullman WA) WP4-T dew point hygrometry covers waterpotential values common in arid soils and does so with good accuracy However theapproach and theWP4-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 forfield deployment in arid soils [34] These sensors eg MPS-6 are based on a ceramicsubstrate with a known moisture release curve The sensors can be buried in soilwhere they record both temperature andwater potential changes as the water contentof the ceramic substrate varies The stated measurement range is from minus001MPa tominus100MPa MPS-6 sensors measure the matric potential and thus are not suitable forsaline soils or other systemswith significant solute potentials In addition their utilityhas not been established for surface soils (eg 0ndash5 cm) that vary substantially over adiurnal cycle

33 Limits of Growth and Metabolic Activity

The effects ofwater availability (most often expressed as aw) onmicrobial growthhavebeen given considerable attention in the context of food preservation [35] Numerousstudies have led to general estimates of lower growth limits for a variety of bacteriaand fungi that commonly occur in processed foods or that contribute to spoilage Ingeneral Gram negative bacteria (eg Proteobacteria and Bacteroidetes) do not growat aw lt about 095 (minus706MPa) while Grampositive bacteria (eg Actinobacteria andFirmicutes) donot growwith aw lt about 090 (minus1449MPa) [19] There are exceptionsof coursePontibacillus sp AS2and Salinicola sp LC26 (Firmicutes andProteobacteriarespectively) grow at aw = 0775 (minus3506MPa) and the actinobacterium Mycobac-terium parascrofulaceum LAIST_NPS017 grows at aw = 0800 (minus3193MPa at 37 degC)(36) Members of the euryarchaeal Halobacteriaceae typically grow at aw = 0755(minus4060MPa at 40degC) but limits as low as 0611 (minus6776MPa) have been extrapo-lated from growth data [36] Many fungi grow at aw = 0700minus0900 (minus4906MPa tominus1449MPa) but lower limits of 0611 have also been extrapolated for a few excep-tional strains [36]

Though studies on water activity collectively represent a reasonably broad surveyof some economically important taxa they have nonetheless explored relatively few




species from relatively few phyla (mostly Actinobacteria Euryarchaea Firmicutesand Proteobacteria) and have been limited by the need to use cultivable isolatesThus water activity limits are essentially unknown for a large percentage of BacteriaArchaea 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 onemight propose that the effects of lowwa-ter potential onmacromolecules especially DNA would be the same regardless of themechanism 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 solutesversus pore based capillarity (eg [37]) Where solutes dominate total water poten-tial Ψ intracellular water potentials can be adjusted to osmoconformers via solutetransport When matric potentials dominate Ψ the ability of cells to adjust may beconstrained by solute availability and by the energy required to synthesize intracel-lular compatible solutes This has not been explored systematically but studies withisolates have shown differential responses to ψs versus ψm (eg [38 39]) Nonethe-less relatively little is knownabout the growth or activity responses of specific isolatesto matric potential Addressing this knowledge gap should be a research priority par-ticularly since changing precipitation regimes in the future will be accompanied bychanging soil water potential regimes

Work by Schnell and King [40] with methanotrophs provides an example of thepotential significance of solute versus matric potentials They used NaCl as a readilytransported solute and sucrose as an impermeable solute to adjust Ψ in growth me-diaWhile not directly equivalent to a matric potential a solute potential arising froman impermeable solute canmimic the effect of matric potentials on cells Schnell andKing [40] observed that both growth and methane uptake rates were inhibited withdecreasing 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 potentialextremes well below growth limits due to solute potentials How do the members ofsoil microbial communities cope with such extremes

While growth certainly provides an exquisitely sensitive index of the ability ofmicrobes to tolerate extreme conditions metabolic activity can continue beyond thelimits for growth Analyses of metabolic activity as a function of temperature have in-dicated thatmaintenanceand survivalmetabolismoccur at subzero temperatureswellbelow those at which growth ceases [41] These results are relevant for understandingrelationships between water availability and metabolism since bacterial activity inice occurs within solutions that have low ψs However lower limits for activity havenot been explored systematically as a function of ψs or Ψ for either isolates or mixedpopulations 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 aminimumtemperature for metabolism but this might not hold true for water potential



34 Water Potential and Trace Gas Exchanges | 37

34 Water Potential and Trace Gas Exchanges

Methane Water content has a profound and well documented impact on soilndashatmos-phere methane exchanges At saturation anoxic conditions can develop which pro-mote methanogenesis andmethane emission Numerous variables affect the extent towhich methanogenic activity occurs including soil organic matter content and elec-tron acceptor availabilityWhilewater potential has not been specifically addressed asa variable for soil methanogenesis it is clear that some methylotrophic methanogenstolerate solute potentials as low as minus40MPa since they can produce methane in saltsaturated sediments or solutions [42] Nonetheless inmost caseswheremethanogensare active water potentials are high due to low solute concentrations and the absenceof matric potentials Furthermore there are relatively few arid or semiarid soils forwhich methanogenesis would have any relevance since these soils are unsaturatedand methanogenesis is inhibited by molecular oxygen regardless of water potentialregimes

Atmosphericmethane consumption bymethanotrophic bacteria obviously occursfar more commonly in arid and semiarid soils than does methanogenesis Due to thesignificance of soil methanotrophs for the atmospheric methane budget (eg [43])numerous studies have addressed the role of variables such aswater content pH tem-perature soil texture nitrogen content and land use [6 44ndash49] The effects of watercontent 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 lowwater contents inhibiting activity presumably due to undefined water stresses Waterpotential 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 (eg to minus10MPa) in theldquoOrdquo and ldquoArdquo horizons that developed during summer appeared to strongly inhibit up-take and constrain activity to lower depths the effect of which was to reduce areabased rates year round Combined analyses of water content and water potential alsoshowed that interactions between soil gas exchange methane concentration andwa-ter stress determined uptake rates and responses to water potential In particular de-creasing water content at high water potentials (gt minus02MPa) increased gas transportandmethaneuptake even thoughmethanotrophs experiencedwater stress Howevercontinued decreases in water content led to increased stress and decreased methaneuptake (998835 Fig 31) Addition of exogenous methane to a concentration of 200 ppmmin-imized gas transport limitation and revealed that water stress inhibition developed atΨ ge minus02MPa (998835 Fig 31) Isolates were similarly sensitive to water stress whether itwas 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 etal [47] for UK temperate forests and byGulledge and Schimel [46] for boreal soilsWa-ter stress sensitivity observed for surface soils in these studies likely occurs in surfacesoils of arid and semiarid systems whichmight explain the subsurface localization of




ndash10(a) (b)

0030 00 ndash100

ndash080

ndash060

ndash040

ndash020

000

05

10

15

20

25

30

0035

0040

0045

0050

0055

0060

ndash080 ndash060

Water potential (MPa) Water content ()

Met

hane

upt

ake

rate

cons

tant

(hndash1

gdw

ndash1)

Met

hane

upt

ake

rate

(nm

ol g

dwndash1

hndash1 )

Wat

er p

oten

tial (

MPa

)

ndash040 ndash020 00 15 20 25 30 35 40

Fig 31 (a) Methane uptake rate constants with atmospheric methane and methane uptake ratesat 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 (eg [44]) If surface soils werenot inhibitory in some manner they would be the locus of greatest uptake activitysince the supply of methane is greatest there However the lack of parallel time vary-ing depth specificwater potential andmethane uptake data limit extrapolations Evenso it is clear that extreme water potentials develop in the surface soils of arid systemsand that soils most conducive to activemethanotrophy occur primarily in deeper hori-zons (eg gt 10 cm) Seasonal studies have also shown that the highest methane up-take rates in arid soils are associatedwith precipitation events albeitwith a lagwhichindicates that water stress tolerant methanotrophs likely do not occur at substantiallevels

Though models of climate change impacts on soil methane fluxes include re-lationships between water potential and inhibition of methane uptake (eg [50ndash52]) one such relationship predicts significant uptake at water potential values≪ minus10MPa [50] an outcome that has not been verified empirically for soils in generallet alone for arid and semiarid soils Given the lack of spatial coverage by direct studiesof atmospheric methane uptake simulation models offer a potentially valuable toolfor developing estimates of global uptake rates However to be fully useful the waterpotential uptake rate relationship should be established empirically for multiple soiltypes 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 theprimary oxidant in the troposphere and as such is responsible for chemical oxida-tionof atmosphericmethaneandother organic gases Since it contributes significantlyto atmospheric CO dynamics uptake by soils has been the focus of multiple studieswhich have addressed rates controls and some aspects of CO microbiology [54 55]Although CO transformations in soil have been explored much less than methane




transformations several studies have established dependencies on soil water con-tent [56] Patterns somewhat analogous to those formethane oxidation have emergedwith lower rates of CO uptake at high water contents and increasing uptake rates asgas transport increases with lower water contents at relatively low water contentsuptake ceases due to water stress and net CO emission can sometimes be observed

Relationships between water potential and atmospheric CO uptake have receivedlittle attention Weber and King [57] examined controls of CO uptake by unvegetatedand vegetated volcanic cinders onHawairsquoi Island (USA) Thoughnot in an arid or semi-arid climate water availability oscillated dramatically on a diurnal basis (between 0and minus60MPa) for unvegetated cinders due to their very limited water retention capac-ity which resulted from low organic contents In contrast water potential for nearbycinders at a vegetated site with high organic concentrations varied very little (0 tominus01MPa) During a moderate drying event (from 0 to minus17MPa) atmospheric COconsumption by intact cores from the unvegetated site decreased 27-fold indicatinga strong dependence on water potential In laboratory assays maximumpotential COoxidation rates decreased by 40 and 60 respectively when water potentials werelowered from 0 to minus15MPa confirming sensitivity observed in the field but also in-dicating that COoxidizing communities at the two siteswere not differentially adaptedto water stress Additional analyses revealed that even after desiccation to minus150MPafor 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 stressSamples from both sites that were exposed to multiple wettingndashdrying cycles (from 0to minus80MPa) lost significant activity after the first cycle but uptake quickly stabilizedand was similar after repeated cycles [57] This suggested that CO oxidizers at bothsites were relatively resistant and resilient to water stress

CO oxidizers in arid and semiarid soils must be similarly resistant and resilient towater 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 (GMKing unpublished) revealed activity at waterpotentials between approximately minus30MPa to minus50MPa for sites that had experiencedwater potentials between minus200MPa and minus300MPa (consistent with ambient relativehumidity) This clearly documents a substantial capacity for tolerance of extreme wa-ter stress The possibility that atmospheric CO can be consumed at water potentialsas low as minus50MPa also distinguishes the capabilities of playa soil CO oxidizers fromthose of forest soils and cinders and suggests that arid and semiarid soils might playa 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 lowwater potentials What organisms are involved What mechanisms promote their ac-tivity How do they respond to diurnal and seasonal variations in water availabilityHow 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) haveprovided some insights for a few of these questions King [59] observed atmospheric




00

50Thershold 606 parts per billion

100

150

200

250

300

5 10Time (h)

Core

hea

dspa

ce C

O (p

pb)

15 20 25

Fig 32 Atmospheric CO uptake by triplicate intact cores from saline soils adjacent to the BonnevilleSalt Flats water potentials were approximately minus41 MPa Data are the means of triplicate assayswith 1 standard error indicated The dashed line indicates the uptake threshold concentration FromKing [59]

CO uptake by intact cores of saline soils with surface water potentials of aboutminus40MPa (998835 Fig 32) Depth profiles of CO uptake potential and water potential re-vealed an inverse relationship with the highest uptake potential at the lowest waterpotential This suggested that a CO oxidizing community was adapted to water stressregimes dominated by the presence of salts Additional analyses revealed CO oxidiz-ing extreme halophiles (Euryarchaeota) that could consume atmospheric CO whilegrowing in halite saturated brines [59 60] These results further established the po-tential for CO uptake under conditions of lowwater potential and extended activity tosaline soils They also indicated that novel euryarchaeotes might be the active agentswhen potentials are poised by solutes versus matric stresses Obviously a great dealremains to be learned

Other gases Soils are globally important sources andor sinks for many othertrace gases few of which have been evaluated in the context of water potential orwater stress [61 62] Disregarding CO2 a trace gas that should be treated separately(eg [5 48 63ndash65]) perhaps the most thoroughly studied gases other than methaneincludenitrous oxide andNO Both play roles in radiative forcing Nitrous oxide is wellknown for its contribution to stratospheric ozone depletion and for its greenhouseproperties [62] NO is well known as an important reactant in tropospheric chemistryand it contributes to formation of tropospheric ozone which is a potent greenhouse



35 Conclusions | 41

gas that also causes substantial losses of plant production in agriculture and damageto human health [62]

Nitrous oxide and NO dynamics depend substantially on soil water regimes Highwater 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 favoredat lower water contents but it is also very sensitive to water potentials of less thanabout minus01MPa [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 contentsand presumably intermediate water potentials though the latter have seldom beenmeasured during flux studies [69ndash71]

In arid and semiarid soils nitrogen gas fluxes often depend onwater pulses in theform of episodic precipitation which can drastically and rapidly alter microbial com-munity activity resulting in short term bursts of metabolism that include nitrificationand denitrification and elevated but time varying nitrous oxide and NO emissions(eg [1 4 17 727374]) 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 potentialndashwater content relationships and different relationshipsfor different soil types [75] water potential analyses could promote a greater under-standing of the mechanisms and variables that control nitrogen gas transformationswhile also facilitating comparisons among systems

Water content and water potential also play important roles in the dynamics ofnitrogen oxide emission from biological soil crusts (BSC) which can represent signif-icant NOx sources during wetting events (eg [70 76 77]) Although BSC behavior iscertainly very sensitive towater potential [78] water content has beenmost commonlymeasured in studies of BSC photosynthesis or other activities (eg [2]) NonethelessPotts 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 BSCmay vary acrossspace 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 waterpotential and not just water content is essential for an improved mechanistic under-standing and for model projections of responses to change

35 Conclusions

Soil water potential is a master variable that to a large degree determines the patternsand 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 variesamong soil types In addition water potential but not water content offers a mech-




anistic understanding of trace gas production and consumption at a cellular levelFor example decreasing water contents can enhance the physical process of gas ex-change but the accompanying decreases in water potential typically inhibit trace gasproduction and consumption physiologically Improved designs for small relativelyinexpensive systems that canmeasure in situwater potentials at lt minus10MPa and evenlt minus100MPa offer new possibilities for more extensive water potential monitoring insemiarid and arid soil systems More routine application of these technologies willgreatly improve predictive models for trace gas dynamics especially in the context ofchanging climate regimes and increased frequencies of extreme events

References

[1] McLain JET Martens DA Moisture controls on trace gas fluxes in semiarid riparian soils SoilSci Soc Am J 2006 70367

[2] Grote EE Belnap J Housman DC Sparks JP Carbon exchange in biological soil crust commu-nities under differential temperatures and soil water contents implications for global changeGlobal Change Biol 2010 162763ndash74

[3] Wu X Yao Z Bruumlggemann N Shen ZY Wolf B Dannenmann M et al Effects of soil moisture andtemperature on CO2 and CH soilndashatmosphere exchange of various land usecover types in asemi-arid grassland in Inner Mongolia China Soil Biol Biochem 2010 42773ndash87

[4] Harms TK Grimm NB Responses of trace gases to hydrologic pulses in desert floodplainsJournal of Geophysical Research Biogeosci 2012 117doi1010292011JG001775

[5] Moyano FE Vasilyeva N Bouckaert L Cook F Craine J Curiel Yuste J et al The moisture re-sponse of soil heterotrophic respiration interaction with soil properties Biogeosci 201291173ndash82

[6] Luo GJ Kiese R Wolf B Butterbach-Bahl K Effects of soil temperature and moisture onmethane uptake and nitrous oxide emissions across three different ecosystem types Biogeosci2013 103205ndash19

[7] Porporato A Daly E Rodriguez-Iturbe I Soil water balance and ecosystem response to climatechange Am Nat 2004 164625ndash632

[8] Oviatt CG Lake Bonneville fluctuations and global climate change Geol 1997 25155ndash158[9] Galbally IE Kirstine WV Meyer CP Wang YP Soilndashatmosphere trace gas exchange in semiarid

and arid zones J Environ Qual 2008 37599[10] Conrad R Seiler W Arid soils as a source of atmospheric carbon monoxide Geophys Res Lett

1982 91353ndash56[11] Conrad R Seiler W Influence of temperature moisture and organic carbon on the flux of H2

and CO between soil and atmosphere field studies in subtropical regions 1985 905699ndash709[12] Billings SA Schaeffer SM Evans RD Trace N gas losses and N mineralization in Mojave desert

soils exposed to elevated CO2 Soil Biol Biochem 2002 341777ndash84[13] Peacuterez MVA Castantildeeda JG Friacuteas-Hernaacutendez JT Franco-Hernaacutendez O Van Cleemput O Den-

dooven L et al Trace gas emissions from soil of the central highlands of Mexico as affectedby natural vegetation a laboratory study Biol Fertil Soils 2004 40252ndash9

[14] McLain JET Martens DA McClaran MP Soil cycling of trace gases in response to mesquite man-agement in a semiarid grassland J Arid Environ 2008 721654ndash65

[15] Dijkstra FA Morgan JA LeCain DR Follett RF Microbially mediated CH4 consumption and N2Oemission is affected by elevated CO2 soil water content and composition of semi-arid grass-land species Plant Soil 2009 329269ndash81



References | 43

[16] Singh JS Anticipated effects of climate change on methanotrophic methane oxidation ClimateChange Environ Sustain 2013 120

[17] Homyak PM Sickman JO Influence of soil moisture on the seasonality of nitric oxide emissionsfrom chaparral soils Sierra Nevada California USA J Arid Environ 2014 10346ndash52

[18] Ladeiro B Saline agriculture in the 21st century using salt contaminated resources to copewith food requirements J Bot 2012 doi1011552012310705

[19] Brown AD Microbial water stress physiology principles and perspectives 1990 Wiley amp SonsNY

[20] Tate RL III Soil microbiology 2nd edn 2000 Wiley amp Sons NY[21] Castro MS Steudler PA Bowden RD Factors controlling atmospheric methane consumption by

temperate forest soils Glob Biogeochem Cyc 1995 91ndash10[22] Moldrup P et al Predicting the gas diffusion coefficient in undisturbed soil from soil water

characteristics Soil Sci Soc Am J 2000 6494ndash100[23] Fenchel T King GM Blackburn TH Bacterial biogeochemistry the ecophysiology of mineral

cycling 2012Academic Press New York[24] Griffin DM Water and microbial stress Adv Microb Ecol 1981 591ndash136[25] Nobel PS Physiochemical and environmental plant physiology 2nd edition 1999 Academic

Press New York 489 p[26] Skopp J Oxygen uptake and transport in soils analysis of the air-water interfacial area Soil

Sci Soc Am J 1985 491327ndash31[27] Skopp J Jawson MD Doran JW Steady-state aerobic microbial activity as a function of soil

water content Soil Sci Soc Am J 1990 541619ndash25[28] Jarrell WM Armstrong DE Grigal DF Kelly EF Monger HC Wedin DA Soil water and tempera-

ture status In Robertson GP Coleman DC Bledsoe CS Sollins P (eds) Standard soil methodsfor long-term ecological research Oxford Univ Press Oxford 1999 55ndash73

[29] Bittelli M Flury M Errors in water retention curves determined with pressure plates Soil SciSoc Am J 2009 731453ndash60

[30] Whalley WR Ober ES Jenkins M Measurement of the matric potential of soil water in the rhizo-sphere J Exp Bot 2013 64doi101093jxbert044

[31] Pagay V Santiago M Sessoms DA Huber EJ Vincent O Pharkya A Corso TN Lakso AN StroockAD A microtensiometer capable of measuring water potentials below minus10 MPa Lab Chip 201414142806ndash17

[32] Fonteyn PJ Schlesinger WH Marion GM Accuracy of soil thermocouple hygrometer measure-ments in desert ecosystems Ecol 1987 681121ndash24

[33] Mantri S Bulut R Evaluating performance of a chilled mirror device for soil total suction mea-surements Geotechnical Special Publication 2014 doi1010619780784478509008

[34] Nolz R Kammerer G Cepuder P Calibrating water potential sensors integrated into a wirelessnetwork Ag Wat Manage 2013 11612ndash20

[35] Jay JM Modern food microbiology 5th edn 2012 Springer Science amp Business Media[36] Stevenson A Burkhardt J Cockell CS Cray JA Dijksterhuis J Fox-Powell M et al Multiplication

of microbes below 0690 water activity implications for terrestrial and extraterrestrial lifeEnviron Microbiol 2015 17257ndash77

[37] Cytryn EJ Sangurdekar DP Streeter JG Franck WL Chang WS Stacey G et al Transcriptionaland physiological responses of Bradyrhizobium japonicum to desiccation-induced stressJ Bacteriol 2007 1896751ndash62

[38] Potts M Imre-Friedman E Effects of water stress on cryptoendolithic cyanobacteria from hotdesert rocks Arch Microbiol 1981 130267ndash71




[39] Johnson DR Coronado E Moreno-Forero SK Heipieper HJ van der Meer JR Transcriptome andmembrane fatty acid analyses reveal different strategies for responding to permeating andnon-permeating solutes in the bacterium Sphingomonas wittichii BMC Microbiol 2011 11250

[40] Schnell S King GM Responses of methanotrophic activity in soils and cultures to water stressAppl Environ Microbiol 1996 623203ndash09

[41] Price PB Sowers T Temperature dependence of metabolic rates for microbial growth mainte-nance and survival Proc Natl Acad Sci USA 2004 1014631ndash6

[42] Giani D Jannsen D Schostak V Krumbein W Methanogenesis in a saltern in the Bretagne(France) FEMS Microbiol Ecol 1989 62143ndash50

[43] King GM Ecological aspects of methane oxidation a key determinant of global methane dy-namics Adv Microbial Ecol 1992 12431ndash468

[44] Striegl RG McConnaughey TA Thorstenson DC Weeks EP Woodward JC Consumption of atmo-spheric methane by desert soils Nature 1992 357145ndash7

[45] Ball BC Smith KA Klemedtsson L Brumme R Sitaula BK Hansen S et al The influence ofsoil gas transport properties on methane oxidation in a selection of northern European soilsJ Geophys Res 1997 10223309

[46] Gulledge J Schimel JP Moisture control over atmospheric CH4 consumption and CO2 produc-tion in diverse Alaskan soils Soil Biol Biochem 1998 301127ndash32

[47] Bradford MA Wookey PA Ineson P Lappin-Scott HM Controlling factors and effects of chronicnitrogen and sulphur deposition on methane oxidation in a temperate forest soil Soil BiolBiochem 2001 3393ndash102

[48] Davidson EA Ishida FY Nepstad DC Effects of an experimental drought on soil emissions ofcarbon dioxide methane nitrous oxide and nitric oxide in a moist tropical forest Glob ChangeBiol 2004 10718ndash30

[49] Norton U Mosier AR Morgan JA Derner JD Ingram LJ Stahl PD Moisture pulses trace gasemissions and soil C and N in cheatgrass and native grass-dominated sagebrush-steppe inWyoming USA Soil Biol Biochem 2008 401421ndash31

[50] Curry CL Modeling the soil consumption of atmospheric methane at the global scale GlobalBiogeochem Cyc 2007 214

[51] Curry CL The consumption of atmospheric methane by soil in a simulated future climate Bio-geosci 2009 62355ndash67

[52] Nazaries L Murrell JC Millard P Baggs L Singh BK Methane microbes and models funda-mental understanding of the soil methane cycle for future predictions Environ Microbiol 2013152395ndash417

[53] Crutzen PJ Gidel LT A two-dimensional photochemical model of the atmosphere 2 The tropo-spheric budgets of the anthropogenic chlorocarbons CO CH4 CH3Cl and the effect of variousNOx sources on tropospheric ozone J Geophys Res 1983 886641ndash61

[54] Conrad R Soil microorganisms as controlers of atmospheric trace gases (H2 CO2 CH4 OCSN2O NO) Microbiol Rev 1996 60609ndash640

[55] King GM Characteristics and significance of atmospheric carbon monoxide consumption bysoils Chemosphere Global Change Sci 1999 153ndash63

[56] King GM Attributes of atmospheric carbon monoxide oxidation in Maine forest soils ApplEnviron Microbiol 1999 655257ndash64

[57] Weber CF King GM Water stress impacts on bacterial carbon monoxide oxidation on recentvolcanic deposits ISME J 2009 31325ndash34

[58] Potter CS Davidson EA Verchet LV Estimation of global biogeochemical controls and seasonal-ity in soil methane consumption Chemosphere 1996 322219ndash46

[59] King GM Carbon monoxide as a metabolic energy source for extremely halophilic microbesImplications for microbial activity in Mars regolith Proc Natl Acad Sci USA 2015 1124465ndash70



References | 45

[60] McDuff S King GM Neupane S Myers M Isolation and characterization of extremelyhalophilic CO-oxidizing Euryarchaeota from hypersaline cinders sediments and soils and de-scription of a novel CO oxidizer Haloferax namakaokahaiae Mke23T sp nov FEMS MicrobiolEcol 2016 92doi101093femsecfiw028

[61] Mooney HA Vitousek PM Matson PA Exchange of materials between terrestrial ecosystemsand the atmosphere Science 1987 238926ndash32

[62] Monson RK Holland EA Biospheric trace gas fluxes and their control over tropospheric chem-istry Annu Rev Ecol Syst 2001 32547ndash76

[63] Davidson EA Verchot LV Cattanio JH Ackerman IL Carvalho JEM Effects of soil water con-tent on soil respiration in forests and cattle pastures of eastern Amazonia Biogeochem 20004853ndash69


[65] Jassal RS Black TA Novak MD Gaumont-Guay D Nesic Z Effect of soil water stress on soil res-piration and its temperature sensitivity in an 18-year-old temperate Douglas-fir stand GlobalChange Biol 2008 141305ndash18

[66] Bateman EJ Baggs EM Contributions of nitrification and denitrification to N2O emissions fromsoils at different water-filled pore space Biol Fertil Soils 2005 41379ndash88

[67] Stark JM Firestone MK Mechanisms for soil moisture effects on activity of nitrifying bacteriaAppl Environ Microbiol 1995 61218ndash21

[68] Gleeson DB Herrmann AM Livesley SJ Murphy DV Influence of water potential on nitrifica-tion and structure of nitrifying bacterial communities in semiarid soils Appl Soil Ecol 200840189ndash94

[69] Bargsten A Falge E Pritsch K Huwe B Meixner FX Laboratory measurements of nitric oxiderelease from forest soil with a thick organic layer under different understory types Biogeosci2010 71425ndash41

[70] Weber B Wu D Tamm A Ruckteschler N Rodriguez-Caballero E Steinkamp J et al Biologicalsoil crusts accelerate the nitrogen cycle through large NO and HONO emissions in drylandsProc Natl Acad Sci USA 2015 11215384ndash9

[71] Vourlitis GL DeFotis C Kristan W Effects of soil water content temperature and experimentalnitrogen deposition on nitric oxide (NO) efflux from semiarid shrubland soil J Arid Environ2015 11767ndash74

[72] Fierer N Schimel JP Holden PA Influence of drying-rewetting frequency on soil bacterial com-munity structure Microb Ecol 2003 4563ndash71

[73] Austin AT Yahdjian L Stark JM Belnap J Porporato A Norton U et al Water pulses and biogeo-chemical cycles in arid and semiarid ecosystems Oecol 2004 141221ndash35

[74] Steenwerth K Jackson L Calderon F Scow K Rolston D Response of microbial communitycomposition and activity in agricultural and grassland soils after a simulated rainfall Soil BiolBiochem 2005 372249ndash62

[75] Royer JM Vachaud G Field determination of hysteresis in soil-water characteristics Soil SciSoc Am J 1975 39221ndash223

[76] Barger NN Belnap J Ojima DS Mosier A NO Gas loss from biologically crusted soils in Canyon-lands National Park Utah Biogeochem 2005 75373ndash91

[77] Abed RM Lam P de Beer D Stief P High rates of denitrification and nitrous oxide emission inarid biological soil crusts from the Sultanate of Oman ISME J 2013 71862ndash75

[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 201372178ndash91



Thulani P Makhalanyane Storme Z de Scally and Don A Cowan4 Microbiology of Antarctic Edaphic

and Lithic Habitats

41 Introduction

The Antarctic atmosphere has recently exceeded the nominal barrier of 400 ppmCO2 [1] Climate models designed to predict future temperature regimes over theAntarctic continent are complicated by the interactions between the atmosphereocean and ice in lower latitude regions [2] Nevertheless these models consistentlypredict a long term increase in average surface temperatures [3] where southern polarregions may experience average temperature increases of between 03ndash48degC by theend 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] iceshelves [9 10] glaciers andmeltwater streams [11ndash13] and soils (and their associatedcryptic and refuge niches) [14ndash16] However feedback of soil ecosystems to climatechange remain unclear despite the fact that more carbon is stored in these systemsthan in plant and atmospheric pools [17 18] For instance carbon stored in Arcticand Antarctic permafrost alone may significantly intensify climate change throughcarbonndashclimate feedback [19] We therefore argue as have others [20ndash22] that a com-prehensive understanding of the terrestrial microbiota of the Antarctic continent isessential in order to appreciate the impacts of projected future climate changes

The majority of the Antarctic continent is covered by an extensive ice sheet withless than 3 of the total land surface comprised of ice free regions [23 24] Theseregions 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 thetotal land area of the continent but they harbor considerable numbers and diversityof microbial taxa that survive in these extremely challenging environmental condi-tions [25]

The development of modern metagenomic methods has as elsewhere helped toreveal the true extent of microbial diversity in a diverse range of Antarctic habitatsincluding oligotrophic copiotrophic psychrophilic and thermophilic soils In thischapter 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 bothof which have been the subjects of recent reviews [16 26]

DOI 1015159783110419047-004



48 | 4 Microbiology of Antarctic Edaphic and Lithic Habitats

42 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 ldquotypicalrdquo dueto the lack of the organic layer typically associated with soils in other environments(998835 Fig 41a) Loosely arranged unconsolidated Antarctic terrestrial sediments most ofwhich lack higher life forms (eg plants) also failed to adhere to accepted soil tax-onomy classification guidelines (998835 Fig 41b) [27] However studies during the 1960sled to the recognition of a range of soil forming or pedogenic processes within the icefree regions of the Antarctic continent [28ndash31] and the recognition that Antarctic soildevelopment is influenced by a number of common pedogenic factors including timeclimate and the parent material The accepted conclusion is that the unconsolidatedgray 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 mattercontent) evaporate soils (containing substances left after the evaporation of a bodyof water) regosols (weakly developed loose mineral soils) lithosols (soil containingmostly weathered rock fragments) protoranker soils (colonized bymoss 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 intozonal intrazonal and azonal categories Ahumic soils are considered zonal as theyare 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 ornithogenicsoils are intrazonal [33]

(a) (b)

Fig 41 (a) Antarctic Dry Valley soils showing the typical pavement structure where mineral soils areoverlain by stones (typically quartz) with the typical organic layer absent (b) An ice free AntarcticDry Valley region showing terrestrial soils that are loosely arranged and lack higher terrestrial lifeforms



42 Classification of Antarctic soils | 49

Early investigations revealed that chemical weathering and ionic migration alsooccurred 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 ldquoa natural bodycomprised of solids liquids and gases organized into horizons readily distinguishablefrom the initial starting material as a result of addition losses transfers and transfor-mation of energy andmatterrdquo [36] Based on this new definition Antarctic soils couldbe classified according to pedogenic processes affected by factors such as time andclimate as well as soil properties Climatic conditions and physiochemical proper-ties differ markedly across the ice free regions of the Antarctic continent such as theMcMurdo Dry Valleys (MDVs) and the Antarctic Peninsula resulting in unique soilbiotopes in each region [27]

421 McMurdo Dry Valley Soils

TheMDVs occurringwithin the South Victoria Land zone (roughly from 77deg S to 78deg S)represent the largest ice free region of Antarctica [37] The MDVs are characterized ascold hyperarid desert regions [38] and are subject to extreme climatic conditions in-cluding very low temperatures [39 40] low atmospheric moisture levels and wateravailability [41] high levels of UV radiation [37] and strong katabatic winds [42] TheMDVs have a mean precipitation rate of less than 10 cmyrminus1 [43] mostly in the formof snow that sublimes rather thanmelts allowing very little moisture to reach the soilsubsurface [37 38] Average annual air temperatures range from minus15degC to minus30degC [44]although surface soil temperatures can reach amaximum of around 15degC for short pe-riods in the summermonths [44 45] Frequent freezendashthaw cycles occur inMDV soilswhere fluctuations of minus15degC to gt +20degC have been observed within a single day [3940]

The Dry Valleys contain both ephemerally wetted soils from glacialmelt exposureand depauperate mineral soils [46 47] The mineral soils within the MDVs are mostlyalkaline with pH values ranging from 7 to almost 10 in some valley regions [48ndash51]MDV soils are often saline and may contain high concentrations of soluble salts suchas calcium magnesium sodium chloride nitrate and sulfate [37 41 50] Soluble ni-trogen and phosphorus concentrations vary widely with ranges of 0ndash1250 microg gminus1 and001ndash120 microg gminus1 respectively [48] Organic matter content is typically very low with amean percentage carbon level of less than 01 in many soils [52] The percentage ofsand is markedly higher than the percentage of clay and silt (usually less than 15combined) within MDV soils [27]

MDV soils are influenced by both chemical and physical parameters perhapsmore so than other soils [27] The predominant pedogenic processes in this regioninclude salinization and desert pavement formation [53] These mineral soils contain




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 namelyTurbels and Orthels is based on the characteristics and proximity of permafrost tothe mineral soil surface [27] Turbels contain ice cemented permafrost within 70 cmof the soil surface and are generally cryoturbated indicating that materials from dif-ferent soil horizons were mixed due to freezendashthaw cycles [27] Orthels in contrastcontain dry permafrost and little cryoturbation [27] Based on these classificationsthe dominant soil types within the MDVs are Typic Haploturbels Typic Anhyturbelsand Typic Anhyorthels where haplo refers to simple and anhy refers to low levelsof moisture or precipitation [54] The depth of the permafrost layer and the degreeof permafrost melting may be important factors in water availability to surface andshallow subsurface microbial communities

422 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 withmany 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 plantswhich then sustain other animals such as birds [56] The nutrient inputs from theseorganisms alter the physiochemical characteristics of the soil thereby leading to thealternative well developed soil biotopes present on the Antarctic Peninsula and sur-rounding islands [57] The greater soil taxonomic diversity within the peninsula is dueto thediverse soil characteristics aswell as thenumber of soil formingprocesses in thisregion [58 59] The main pedogenic processes occurring within the maritime Antarc-tic include rubification carbonation humification podsolization phosphatizationand cryoturbation [53] The common soil orders within the Antarctic Peninsula asclassified by soil taxonomy include the entisols (soils that are extremely underdevel-oped) inceptisols (soils that are weakly developed) and histosols (soils that containorganicmatter) [54]Within these the two suborders Typic Gelorthents and Typic Ge-laquents are the most common although Turbic Dystrogelepts Turbic Humigeleptsand 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 (birdexcrement) [27] As a consequence ornithogenic soils are highly enriched in nutrientssuch as phosphorus inorganic nitrogen and organic carbon [61] This external nutri-ent input also results in high ammonium levels (up to 5 of the dryweight of soil) dueto the conversion of uric acid to ammonia [62] Ornithogenic soils are typically acidic(pHs ranging from 39 to 51) due to the high concentrations of organic acids and am-monia [61] Nitrate concentrations are much lower with ranges of 0ndash130 microg gminus1 pre-viously reported on Marion Island [63] Ornithogenic soils also harbor high moisture



43 Bacterial Diversity of Soils in the MDVs and Antarctic Peninsula | 51

content with up to 30water saturation byweight [62] Despite the high nutrient andmoisture status of these soils the high percentage of soluble salts limits the growth ofplants lichens and mosses [62]

Fellfield soils occur mainly within more temperate Antarctic regions such as thepeninsula 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 sandysoils of the MDVs [66] For example fellfield soils on Signy Island may contain asmuch as 20 (wt) of soil water content [66]MaritimeAntarctic fellfield soils are proneto leaching and therefore are much less saline than MDV mineral soils [64] Cryp-togams which includemosses 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 4ndash45microg gminus1 1ndash20microg gminus1 and15ndash20 microg gminus1 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 formssuch as plants and birds in some continental regions Although the different Antarcticsoil biotopes reflect the diverse nature of the continent its diversity is also impactedby the presence of specialized cryptic or refuge niches [67ndash69]

43 Bacterial Diversity of Soils in the MDVsand Antarctic Peninsula

Studies surveying microbial diversity within Antarctica were originally based on thedetermination of bacterial cell densities through ATP lipid or DNA quantification [70]the culturing of active microorganisms [71] and microscopic analysis [72] Microbialbiomass detected within the nutrient rich ornithogenic and fellfield soils of the Penin-sula are in the range of 107ndash1010 prokaryotic cells gminus1 [73 74] Surprisingly micro-bial biomass counts within the MDVs are only slightly lower with a range of 106ndash108 prokaryotic cells gminus1 detected [70] Microbial cell densities within Antarctic soilswere positively correlatedwith soil water content and negatively correlatedwith salin-ity [75] Culture dependent studies on Antarctic soils identified the presence of mostlyaerobic heterotrophic microorganisms with limited anaerobic bacteria The bacterial




phylotypic diversity was rather limited consisting mainly of Actinobacteria and Fir-micutes [76ndash81]

Culture independent phylogenetic andmetagenomic techniques which are basedon the analysis of total community DNA extracted directly from environmental sam-ples avoid any bias induced by the requirement for microbial growth and thereforemayprovide truer estimates ofmicrobial diversity [81ndash83] Phylogenetic fingerprintingmethods 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 microbialcommunity structures within these regions [81 84] However metagenomic sequenc-ing using either large insert libraries shotgun or amplicon sequencing identifies theldquoentirerdquomicrobial community composition within a specific sample [82 83] Taken to-gether these techniques have resulted in the detection of amuch greater microbial di-versity within Antarctic niches than originally predicted However it should be notedthat 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) andthat the true microbial diversity at species and strain levels within Antarctic nichesis therefore still largely unclassified [85] Interestingly the large number of uncul-tured microbial representatives commonly detected in surveys of microbial diversitywithin Antarctica may also include novel species (particularly members of the familyActinobacteria) 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 maintainedacross many Antarctic soil environments [86ndash88] Smith et al (2006) used DGGEto analyze the microbial diversity of mineral soils from three different MDV sitesThe samples were dominated by Actinobacteria Acidobacteria Cyanobacteria andBacteroidetes and included Verrucomicrobia Chloroflexi Alphaproteobacteria andBetaproteobacteria at lower abundances Actinobacteria occurred ubiquitously in allsamples possibly due to the dispersal capabilities andhigh abundance of this phylumwithin soils (998835 Tab 41) [79 89ndash100] A similar study on soils within the more north-ern (and drier)McKelvey Valley identified additional taxa such asGemmatimonadetesand the desiccation tolerant DeinococcusndashThermus and Rubrobacter [87] In contrastthe more nutrient rich soils of the Peninsula (including both vegetated and fellfieldsoils) are dominated by Proteobacteria (including representatives of the Alpha BetaGamma and Delta Proteobacteria) with lower abundances of Actinobacteria andBacteroidetes [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 [5076 101] Lee et al (2012) used a combination of pyrosequencing and DGGE to deter-mine microbial community structure within soils from four geographically isolatedMDVs [50] Only a limited number of phylotypeswere identified at each of the four sites(typically members of the Actinobacteria and Bacteroidetes) with much of the bacte-




rial diversity identified being specific to one or more sites Regional differences werealso observed from other MDV sites for example the usually dominant Acidobacteriawere 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 themicrobial diversity of soilsalong an environmental gradient within the Antarctic Peninsula Falkland Island andSigny Island using DGGE [101] This study showed that microbial abundance was sig-nificantly and positively influenced by vegetation related factors such as nitrogen andcarbon and soil water content Microbial community structure was also significantlycorrelatedwith locationand latitude including specific factors suchasmean tempera-ture nitrate and pH These communities were influenced by the complex relationshipbetween vegetation and latitude where latitude had less of an effect in the presenceof vegetation Similarly it has been shown using 16S rRNA gene amplicon sequencingthat bacterial diversity declines with increasing latitude for fellfield but not vegetatedsoils within the Antarctic Peninsula [88]

Mineral soil bacterial community structure has also been shown to be markedlydifferent from ornithogenic soils [58 76] Aislabie et al (2008) used RFLP methodsto analyze microbial diversity in four different mineral soils and one ornithogenicsoil [76] The mineral soils were found to contain similar bacterial phyla dominatedby Acidobacteria Actinobacteria Firmicutes Cyanobacteria Proteobacteria Bac-teroidetes and DeinococcusndashThermus No difference in microbial diversity was foundbetween soil taxonomic classifications of the mineral soils but was rather found ac-cording to physiochemical parameters such as pH The ornithogenic soils were foundto contain an abundance of endospore formers such as Oceanobacillus Clostridiumand Sporosarcina probably reflecting to the high number of Firmicutes found in thegut and fecal deposits of Antarctic penguins [58]

Themicrobial diversitywithin rhizosphere soils of twonative vascular plants fromthe Antarctic Peninsula was recently assessed [58] Surprisingly in contrast to otherpeninsula soils [88 101] the dominant bacterial phylotypes identified were the Firmi-cutes Actinobacteria and Proteobacteria with Acidobacteria occurring rarely and ata 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 (suchas the Firmicutes) may be due to the higher levels of moisture within the rhizosphereor the adaptation of these communities to nutrient (eg carbon) limiting conditionsduring the winter [58] This study highlights the importance of local environmentalandphysiochemical properties on bacterial community structurewithin Antarctic soilbiotopes




44 Cryptic Niches in Antarctic Environments

The ice free regions of the Antarctic continent provide extensive expanses of exposedrocky substrate The microbial colonization of rock substrates is a particular featureof these regions Lithic associatedmicrohabitats are referred to as lithobiontic nicheswith their communities termed lithobionts [102] Previous studies have shown thatlithobionts [also referred to as soil rock surface communities (SRSCs)] are ubiquitouslydistributed in both hot and cold deserts [103ndash105] In the most hyperarid regionslithobionts are often the only visible forms of life (998835 Fig 42andashd) and are thought tocontribute 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 regionsHypoliths (microbial assemblages found on the ventral surfaces of translucent rocksmostly marble and quartz stones) are probably the most studied of the three nichesEpiliths (organisms populating the surface of stable rock substrata the subcategoryof chasmoliths inhabits cracks in rocks) occur on various igneous rock surfaceswhile endoliths (communities colonizing the interior of rocks) are usually restricted toporous sandstones and weathered granitic rocks [67 68] In all three niches micro-

(a) (b)

(c) (d)

Fig 42 Examples of four lithobiont communitiescryptic 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 thegreen under layer (c) A cryptoendolith occurring along the crack within the rock showing visibleCyanobacteria colonization (thin green line along the crack) (d) Endolithic colonization by Cyano-bacteria



44 Cryptic Niches in Antarctic Environments | 55

bial colonization is limited by the availability of photosynthetically active radiation(PAR) which tends to favor the development of photoautotrophs [24 69]

441 Hypoliths

Hypolithic microbial communities (hypolithons) have been studied within several ofthe 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 asUniver-sity Valley DA Cowan personal observation) where little or no seasonal permafrostmelt 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 altitudessuch as variations in temperature and moisture availability which decrease at higheraltitudesmay account for these differences [106]Where both open soil andhypolithiccommunities 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 biofilmsa small proportion of quartz hypoliths support moss (Hennendiella spp) dominatedcommunities [106]

Hypoliths are thought to be the dominant autotrophic communities in someAntarctic terrestrial soil environments (ie those where suitable translucent mineralsubstrates are present in the desert pavement) They are probably the key primaryproducers 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 [108ndash111] Acombination of microscopy and culture independent studies showed that Cyanobac-teria dominated by filamentous Oscillatorian morphotypes were prevalent in MDVhypoliths [38 112] Microcoleus Phormidium and Oscillatoria phylotypes were alsorecently identified in MDV hypoliths [111] using 16S rRNA gene pyrosequencing Inthe Vestfold Hills Oscillatorian Cyanobacterial morphologies were dominant typi-cally associatedwith LyngbyaPhormidiumPlectonema groups together with coccoidcells similar to Chroococcidiopsis [112] Other dominant bacterial phyla identified inhypolithic 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 istypicallymuch lower than that of bacteria [114ndash116] and is dominated byAscomyceteslineages [108 109] Members of the genera Acremonium Stromatonectria and Verru-cariawere most commonly identified [108] Ascomyceteswere initially reported as the




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 occurat low abundance The low moisture availability in desert soils may explain the lowfungal diversity [118]

Other lower eukaryotes particularly protists have been identified in AntarcticMiersValleyhypolithic communities [117] The relative abundances ofAmoebozoa andCercozoa phylotypic signals were linked to the sample type (ie hypolith type) [106]Interestingly the presence of these protists appeared to beunique to the hypolithic en-vironment and these organismshavenot been identified in nearby open soils Clearlytheir presence in this habitat has implications for the structure and functioningof foodwebs in Antarctic soils and requires further examination

442 Epiliths

In Antarctic regions epilithic colonization is probably the least extensive of all rockassociated 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 morewidespread and complex than previously considered A possible role for shallowsubsurface endolithic microbial populations in the genesis of Antarctic rock varnishlayers has been proposed [121]

In Antarctic regions surface rock communities are limited by the combination ofextremely low temperatures freezendashthaw cycles katabatic wind episodes and highultraviolet radiation levels [122] However in general very little is known regardingthe microbiology of epiliths in comparison to other lithobionts (endoliths and hy-poliths) [67] Early studies suggested that epilithic colonization is primarily associatedwith moss and lichen communities [123] Both lichens and mosses synthesize a widerange of secondary metabolites which may act as protectants against some environ-mental stressors (such as desiccation andUV damage) explaining their dominance inthese niches [124 125] Moreover epiliths are typically foundwhere the rock substratahave access tomoisture [103 126] As such epilithic lichens arewidespread across thecoastal regions of Antarctica but decrease toward the interior [126 127]

Recent studies indicate widespread prevalence of blackmeristematic fungi in thecoastal northern and southern Victoria Land regions of Antarctica [128] Black fungimaybe crucial in the hydration or protection of photobionts by dissipating excess sun-light [129] In contrast epiliths from the Princess Elizabeth Land andMawson 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 ldquogene-sisrdquo theory [121] A comprehensive analysis assessing the dominance of other bacterialphyla in epiliths may validate this proposal




443 Endoliths

Endolithicmicrobial communities are defined as those existing inside lithic strata butare classified into various subniches [102 132ndash134] Chasmoendoliths (also known aschasmoliths) are found in interstitial cracks and fissures while cryptoendoliths arefound in the pores between mineral grains [102 113 135 136] Like all lithobionts en-doliths are dominated by Cyanobacteria [67 68 87 136ndash138] Early microscopic anal-yses of endoliths suggested that the Cyanobacteria co-existedwith lichens [91] (mostlyGloeocapsa HormathonemandashGloeocapsa and Chroococcidiopsis communities) Morerecent molecular analyses have largely concurred with these studies [126 139]

Endolithic habitatsmay impart a degreeof species selection for example a highlynovel 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 havebeen 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 [140ndash142] Endoliths in McKelveyValley have been shown to be dominated by Nostocales and Chroococcidiopsis-likephylotypes [87] The drivers for selection of the different cyanobacterial phylotypes indifferent endolithic habits are not understood although community structures havebeen 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 andwetter) and south facing (colder and drier) slopes [143] Although all samples weredominated by Leptolyngbya the north facing slopes contained the highest microbialdiversity with a relatively high abundance of Synechococcus-like phylotypes while incontrast the south facing slopes contained Chroococcidiopsis-like phylotypes [143] Itis 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 formconsortiawithheterotrophic phylawhichvary intaxonomic 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 DeinococcusndashThermus phylotypes a group of organismswith known resistance to desiccation stress Unlike open soil populations Actinobac-teriaoccur at a comparatively lowabundance [89] In contrastAcidobacteria andActi-nobacteria were the dominant endolithic heterotrophs in samples from the north fac-ing slopes of the Miers Valley whereas DeinococcusndashThermus dominated the coldersouth facing slopes [143] Chasmoliths and endoliths from the McKelvey Valley con-tained high abundances of Bacteroidetes Actinobacteria and Gammaproteobacteriawith Acidobacteria DeinococcusndashThermus and Alphaproteobacteria at lower abun-dances [87]




Hypolith

(a) (b) (c)

Endolith Open soil

CyanobacteriaBacteriodetesActinobacteria

AcidobacteriaProteobacteriaVerrucomicrobia


AcidobacteriaProteobacteriaDeinococcus-Thermus

CyanobacteriaBacteriodetesActinobacteriaAcidobacteriaProteobacteria

Deinococcus-ThermusChloroflexiGemmatimonadetesVerrucomicrobia

Fig 43 (a) Phylum level classification of bacterial diversity from Antarctic hypolithic communitiesData is based on the percentage of 16S rRNA gene sequences and tRFLP signatures identified foreach 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 Datais based on the percentage of phylum abundances identified from tRFLP fingerprints [87] and wasobtained 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 followinganalysis from MDV soil samples [38] as determined by Cary et al (2010)

In comparison to hypoliths and open soils endoliths appear to harbor higherbacterial diversity (998835 Fig 43) [87] In general all lithobiont microbial communitiesare 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 andhypolithic communities [87 142] Lithobionts are Cyanobacteria dominated whereasopen soil microbial communities consist of a majority of heterotrophic bacterial phy-lotypes (998835 Fig 43) [87 143] Differences between endoliths and hypoliths have beenshown within the McKelvey Valley where the dominant phylotypes were shown to beChroococcidiopsis and Leptolyngbya respectively [87] Although both endoliths andhypoliths 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 dueto the protection that refuge niches provide from environmental stressors [51] and theincreased 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 inmicrobial communitystructures between cryptic niches and the open soil [87]



46 Viruses in Antarctic Edaphic Ecosystems | 59

45 Biogeochemical Cycling in Antarctic Environments

Antarctic soils are generally oligotrophic and have generally low nutrient statusin comparison to those from more temperate biomes [50] Nonetheless these soilsdemonstrate a high capacity for functional processes [108 109 144ndash146] For exam-ple soils in the Soslashr 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 pufM genes (which encode a sub-unit of the type 2 photochemical reaction center found in anoxygenic phototrophicbacteria) and bchLchlL sequences (genes implicated in bacterio-chlorophyll syn-thesis) The majority of pufM sequences were related to those previously found inProteobacteria while the origin of the bchLchlL was linked to Cyanobacteria An-other study based on clone libraries of the large subunit of ribulose-15-biphosphatecarboxylaseoxygenase (RuBisCO) genes (cbbL cbbM) and dinitrogenase-reduc-tase (nifH) genes also identified Cyanobacteria (mostly Nostocales lineages) as theprimary 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 Cand 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 indicatedthat while cryptic niches have higher biomass with autotrophs being more diversein these systems open soil communities are more diverse in terms of diazotrophicguilds [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 inmetabolic pathways linked to carbon transformations in soils were attributedto fungi [147]

46 Viruses in Antarctic Edaphic Ecosystems

Recent metagenomic studies have demonstrated the presence of high levels of viraldiversity in a range of environments [148ndash151] In Antarctic environments the ma-jority of studies have focused on viruses found in freshwater ponds and lake ecosys-tems [152ndash156] These studies have provided key insights into the influence of environ-mental extremes on viral diversity and the role of viruses in biogeochemical cyclesFor instance a study by Yau and colleagues (2010) highlighted virophages as crucialregulators of hostndashvirus interactions a finding that has consequences for carbon fluxdynamics in lake ecosystems [154] Surprisingly comparatively little is known of therole of viruses in Antarctic soil ecosystems Given the high amount of carbon storedin these soils the interactions between viruses and bacteria may be crucial feedback




mechanisms on carbon cycling The diversity and ecology of viruses in Antarctic soilshave been reviewed recently [157]

Isolation methods and analyses using electron microscopy have shown thatAntarctic soils are dominated by tailed viruses (mostly belonging to the family Myo-viridae) and spherical viruses (mostly of the family Levividae) [158] Direct countsusing epifluorescence of extractable and extracellular virus particles suggests thatAntarctic soils may have the highest recorded virus-to-bacteria ratios [159] A studyby Williamson and colleagues showed that the abundance of viruses increased rel-ative to bacteria as water and organic content decreased [159] While the impacts ofclimate change and the melting of previously buried ice has not been assessed forviral communities this finding does suggests enhanced roles for viral communitiesas a consequence of these perturbations

47 Conclusions and Perspectives

InAntarcticmicrobiology twoof the revelationsof thepast twodecades are that bacte-rial diversity of Antarctic edaphic niches ismuchgreater than previously thought andthat specialized cryptic niche communities in cold desert soils may play an importantrole in ecosystem processes [24] (998835 Tab 41) The presence of substantial populationsof Cyanobacteria Chloroflexi and Proteobacteria suggests that these organisms con-tribute to primary productivity in depauperate Antarctica desert soils [87 106] andthat the presence of diverse heterotrophic organisms (including both bacteria andfungi) 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 extremelyweak providing at best limitedbut testable informationon 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 understandingcommunity 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 structureand to some extent function of Antarctic edaphic microbial communities we lacka comprehensive understanding of the finer details the nature of community inter-actions in food web structures the interactive roles of hosts and predators and thebalance between abiotic and biotic factors in controlling community function Suchunderstanding is important for many reasons not least understanding how changingclimate conditionsmay impactmicrobial communities inAntarctic terrestrial environ-ments

It iswell known that cyanobacteria are essentialmediators of biogeochemical pro-cesses in many habitats and it is argued that their role in Antarctic soils may be even



47 Conclusions and Perspectives | 61

Table 41 Microbial diversity from various Antarctic niches

Domain Identity NicheSoil Epilith Endolith Hypolith

Archaea ArchaeaCrenoarcheota Euryarchaeota

Bacteria Acidobacteria

ActinobacteriaArthrobacter Brevibacterium Demetria Gordonia Janibacter Kocuria Lapillicoccus Leifsonia Marisediminicola MicromonosporaMycobacterium Nocardiodetes spp Patulibacter RhodococcusUnclass Intrasporangiaceae Unclass Microbacteria Uncultured Pseudonocardia

Aquificae

BacteroidetesUnclass Flexibacteraceae Unclass Saprospiraceae Unclass Sphingobacteriales

CyanobacteriaAcaryochloris 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




Table 41 (cont) Microbial diversity from various Antarctic niches


Chloroflexi

DeinococcusThermusDeinococcus

FirmicutesUnclass 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






BasidiomycotaBensingtonia Bulleromyces Cryptococcus spp Leucosporidiella Rhodotorula

ZygomycotaMortierellaceae Mortierella

Data was compiled from several resources [38 48 69 76 86 87 89 90 92ndash100]

more critical in the absence of higher eukaryotic phototrophs Modern metagenomicsprovides a set of tools that at least give ready access to information of an organismrsquospotential capacity to respond to change For instance a cyanobacterial genome se-quence provides some insight into the organismrsquos stress response capacity which canbe verified using ex situ culture dependent stress experiments However the technicalchallenges associated with the isolation of slow growing cold active cyanobacterialcultures have posed a considerable challenge [164 165] A novel approach to (par-tially) overcoming this challengemay be to sequence ldquomixedrdquo cyanobacterial culturesand implement genome binning approaches which are increasingly used in the fieldof environmental metagenomics [166ndash168] Metagenomic binning approaches haveyielded insights on the ecology of other extreme habitats [169] and have the capacityto contribute a greater understanding of community interactions in Antarctic soils

A note of caution relating specifically to issues of ldquolegacy DNArdquo must be addedConditions in the driest and coldest soils of the Antarctic continent particularly theMcMurdo Dry Valleys are not inconsistent with those used routinely by microbiolo-gists for the preservation of biologicalmaterial ie freeze drying [170] It is thereforeinstructive to contemplate the impacts on metagenomic DNA dependent phylotypicsurveys of these extreme habitats due to the presence of a legacy of dead cells andeven residual genomic DNA [171] A recent study by Fiererrsquos group [172] suggests thatlegacy (relic) DNA forms a significant proportion of metagenomic DNA extracted fromtemperate soils suggesting that at least someof the published surveys of Antarctic soilmicrobial 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 ldquofunctioningrdquo fraction of themicrobial community aremore reliable and informative However the extreme technical difficulties of extract-ing usable quantities of RNA from low biomass low activity environments such as thecold desert soils of Antarctica makes this an objective rather than a current reality




Acknowledgment The authors wish to thank the University of Pretoria AntarcticaNew Zealand and the South AfricanNational Research Foundation (SANAP program)for supporting field and laboratory research programs

References

[1] Glikson A Cenozoic mean greenhouse gases and temperature changes with reference to theAnthropocene Glob Chang Biol 2016 223843ndash3858

[2] Flato G Marotzke J Abiodun B et al Evaluation of Climate Models In Stocker TF Qin D Plat-tner GK et al eds Climate Change 2013 The physical science basis Contribution of WorkingGroup I to the Fifth Assessment Report of the Intergovernmental Panel on Climate ChangeCambridge Cambridge University Press 2013 741ndash866

[3] Vaughan DG Marshall GJ Connolley WM et al Recent rapid regional climate warming on theAntarctic Peninsula Clim Change 2003 60243ndash74

[4] Christensen JH Kanikicharla KK Marshall G Turner J Climate phenomena and their relevancefor future regional climate change In Pauline M ed Climate Change 2013 The physical sci-ence basis Contribution of Working Group I to the fifth Assessment of the IntergovernmentalPanel on Climate Change Cambridge Cambridge University Press 2013 1217ndash1308

[5] Spaulding SA Antarctic Lakes Arct Antarc and Alp Res 2015 47401ndash2[6] Cavicchioli R Microbial ecology of Antarctic aquatic systems Nature Rev Microbiol 2015

13691ndash706[7] Gooseff MN McKnight DM Welch KA Lyons WB Stream biogeochemical and suspended sed-

iment responses to permafrost degradation in stream banks in Taylor Valley Antarctica Bio-geosciences 2016 131723

[8] Stomeo F Makhalanyane TP Valverde A et al Abiotic factors influence microbial diversity inpermanently cold soil horizons of a maritime-associated Antarctic Dry Valley FEMS MicrobiolEcol 2012 82326ndash40

[9] Christner BC Priscu JC Achberger AM et al A microbial ecosystem beneath the West Antarcticice sheet Nature 2014 512310ndash3

[10] Boetius A Anesio AM Deming JW Mikucki JA Rapp JZ Microbial ecology of the cryospheresea ice and glacial habitats Nature Rev Microbiol 2015 13677ndash90

[11] Kohler TJ Van Horn DJ Darling JP Takacs-Vesbach CD McKnight DM Nutrient treatments altermicrobial mat colonization in two glacial meltwater streams from the McMurdo Dry ValleysAntarctica FEMS Microbiol Ecol 2016 92fiw049

[12] Stanish LF OrsquoNeill SP Gonzalez A et al Bacteria and diatom co-occurrence patterns in micro-bial mats from polar desert streams Environ Microbiol 2013 151115ndash31

[13] Archer SD McDonald IR Herbold CW Cary SC Characterisation of bacterioplankton commu-nities in the meltwater ponds of Bratina Island Victoria Land Antarctica FEMS Microbiol Ecol2014 89451ndash64

[14] Colesie C Allan Green TG Haferkamp I Budel B Habitat stress initiates changes in compo-sition CO2 gas exchange and C-allocation as life traits in biological soil crusts ISME J 201482104ndash15

[15] Caruso T Chan Y Lacap DC Lau MC McKay CP Pointing SB Stochastic and deterministicprocesses interact in the assembly of desert microbial communities on a global scale ISME J2011 51406ndash13

[16] Makhalanyane TP Van Goethem MW Cowan DA Microbial diversity and functional capacity inpolar soils Curr Opin Biotechnol 2016 38159ndash66



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[18] Scharlemann JP Tanner EV Hiederer R Kapos V Global soil carbon understanding and man-aging the largest terrestrial carbon pool Carbon Manag 2014 581ndash91

[19] Schuur EA Bockheim J Canadell JG et al Vulnerability of permafrost carbon to climatechange Implications for the global carbon cycle BioScience 2008 58701ndash14

[20] Walther G-R Post E Convey P et al Ecological responses to recent climate change Nature2002 416389ndash95

[21] Arneth A Harrison SP Zaehle S et al Terrestrial biogeochemical feedbacks in the climatesystem Nat Geosci 2010 3525ndash32

[22] Convey P Bindschadler R Di Prisco G et al Antarctic climate change and the environmentAntarct Sci 2009 21541ndash63

[23] Convey P Chown SL Clarke A et al The spatial structure of Antarctic biodiversity Ecol Monogr2014 84203ndash44

[24] Cowan DA Makhalanyane TP Dennis PG Hopkins DW Microbial ecology and biogeochemistryof continental Antarctic soils Front Microbiol 2014 5154

[25] Cowan DA Antarctic Terrestrial Microbiology Physical and Biological Properties of AntarcticSoils Heidelberg Berlin Springer-Verlag 2014

[26] Jansson JK Taş N The microbial ecology of permafrost Nature Rev Microbiol 2014 12414ndash25[27] Ugolini FC Bockheim JG Antarctic soils and soil formation in a changing environment a re-

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Foundation New Brunswick NJ Rutgers University 1964[30] Ugolini FC Bull C Soil development and glacial events in Antarctica Ohio State University

Institute of Polar Studies 1965[31] Ugolini F Starkey R Soils and micro-organisms from Mount Erebus Antarctica Nature 1966

211440ndash441[32] Tedrow J Ugolini F Antarctic soils In Tedrow JC ed Antarctic soils and soil forming pro-

cesses Washington DC American Geophysical Union 1966 161ndash77[33] Campbell I Claridge G A classification of frigic soils-the zonal soils of the Antarctic continent

Soil Sci 1969 10775ndash85[34] Ugolini FC Anderson DM Ionic migration and weathering in frozen Antarctic soils Soil Sci

1973 115461ndash70[35] Jackson M Lee S Ugolini F Helmke P Age and uranium content of soil micas from Antarctica

by the fission particle track replica method Soil Sci 1977 123241ndash8[36] Bockheim J Properties of a chronosequence of ultraxerous soils in the Trans-Antarctic Moun-

tains Geoderma 1982 28239ndash55[37] Horowitz N Cameron RE Hubbard JS Microbiology of the dry valleys of Antarctica Science

1972 176242ndash5[38] Cary SC McDonald IR Barrett JE Cowan DA On the rocks the microbiology of Antarctic Dry

Valley soils Nat Rev Micro 2010 8129ndash38[39] Aislabie JM Chhour K-L Saul DJ et al Dominant bacteria in soils of Marble Point and Wright

Valley Victoria Land Antarctica Soil Biol and Biochem 2006 383041ndash56[40] Barrett JE Virginia RA Wall DH Adams BJ Decline in a dominant invertebrate species con-

tributes to altered carbon cycling in a low-diversity soil ecosystem Glob Chang Biol 2008141734ndash44




[41] Witherow RA Lyons WB Bertler NA et al The aeolian flux of calcium chloride and nitrateto the McMurdo Dry Valleys landscape evidence from snow pit analysis Antarct Sci 200618497ndash505

[42] Nylen TH Fountain AG Doran PT Climatology of katabatic winds in the McMurdo Dry ValleysSouthern Victoria Land Antarctica J Geophys Res Atmos 2004 109D03114

[43] Doran PT McKay CP Fountain AG et al Hydrologic response to extreme warm and cold sum-mers in the McMurdo Dry Valleys East Antarctica Antarct Sci 2008 20499ndash509

[44] Doran PT Priscu JC Lyons WB et al Antarctic climate cooling and terrestrial ecosystem re-sponse Nature 2002 415517ndash20

[45] Barrett J Virginia R Wall D et al Persistent effects of a discrete warming event on a polardesert ecosystem Glob Chang Biol 2008 142249ndash61

[46] Niederberger TD Sohm JA Tirindelli J et al Diverse and highly active diazotrophic assem-blages inhabit ephemerally wetted soils of the Antarctic Dry Valleys FEMS Microbiol Ecol2012 82376ndash90

[47] Simmons B Wall D Adams B Ayres E Barrett J Virginia R Long-term experimental warm-ing reduces soil nematode populations in the McMurdo Dry Valleys Antarctica Soil Biol andBiochem 2009 412052ndash60

[48] Cowan DA Ah Tow L Endangered antarctic environments Annu Rev Microbiol 200458649ndash90

[49] Toner JD Sletten RS Prentice ML Soluble salt accumulations in Taylor Valley Antarctica Im-plications for paleolakes and Ross Sea Ice Sheet dynamics J Geophys Res Earth Surf 2013118198ndash215

[50] Lee CK Barbier BA Bottos EM McDonald IR Cary SC The inter-valley soil comparative surveythe ecology of Dry Valley edaphic microbial communities ISME J 2012 61046ndash57

[51] Makhalanyane TP Valverde A Velaacutezquez D et al Ecology and biogeochemistry of cyano-bacteria in soils permafrost aquatic and cryptic polar habitats Biodivers Conserv 2015241ndash22

[52] Matsumoto G Chikazawa K Murayama H Torii T Fukushima H Hanya T Distribution and cor-relation of total organic carbon and mercury in Antarctic dry valley soils sediments and or-ganisms Geochem J 1983 17241ndash6

[53] Bockheim JG Ugolini FC A review of pedogenic zonation in well-drained soils of the southerncircumpolar region Quat Res 1990 3447ndash66

[54] Bockheim J McLeod M Soil distribution in the McMurdo Dry Valleys Antarctica Geoderma2008 14443ndash9

[55] Hopkins D Sparrow A Elberling B et al Carbon nitrogen and temperature controls on micro-bial activity in soils from an Antarctic dry valley Soil Biol and Biochem 2006 383130ndash40

[56] Otero X Fernaacutendez S de Pablo Hernandez M Nizoli E Quesada A Plant communities as a keyfactor in biogeochemical processes involving micronutrients (Fe Mn Co and Cu) in Antarcticsoils (Byers Peninsula maritime Antarctica) Geoderma 2013 195145ndash54

[57] Bokhorst S Huiskes A Convey P Van Bodegom P Aerts R Climate change effects on soilarthropod communities from the Falkland Islands and the Maritime Antarctic Soil Biol andBiochem 2008 401547ndash56

[58] Teixeira LC Peixoto RS Cury JC et al Bacterial diversity in rhizosphere soil from Antarcticvascular plants of Admiralty Bay maritime Antarctica ISME J 2010 4989ndash1001

[59] Niederberger TD McDonald IR Hacker AL et al Microbial community composition in soils ofNorthern Victoria Land Antarctica Environ Microbiol 2008 101713ndash24

[60] Blume H Boumllter M Soils and soil scapes In Beyer L Boumllter M (eds) Geoecology of AntarcticIce-Free Coastal Landscapes Heidelberg Berlin Springer-Verlag 2002 91ndash113



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[62] Speir T Cowling J Ornithogenic soils of the Cape Bird adelie penguin rookeries AntarcticaPolar Biol 1984 2199ndash205

[63] Sanyika TW Stafford W Cowan DA The soil and plant determinants of community structuresof the dominant actinobacteria in Marion Island terrestrial habitats Sub-Antarctica Polar Biol2012 351129ndash41

[64] Wynn-Williams DD Ecological aspects of Antarctic microbiology In Marshall KC ed Advancesin microbial ecology NY Springer US 1990 71ndash146

[65] Block W Lewis Smith R Kennedy A Strategies of survival and resource exploitation in theAntarctic fellfield ecosystem Biol Rev 2009 84449ndash84

[66] Yergeau E Fell-Field Soil Microbiology In Cowan D ed Antarctic Terrestrial MicrobiologyPhysical and Biological Properties of Antarctic Soils Heidelberg Berlin Springer-Verlag2014 115ndash29

[67] Makhalanyane TP Pointing SB Cowan DA Lithobionts Cryptic and Refuge Niches In CowanD ed Antarctic Terrestrial Microbiology Physical and Biological Properties of Antarctic SoilsHeidelberg Berlin Springer-Verlag 2014 163ndash79

[68] Pointing SB Hypolithic Communities In Weber B Buumldel B Belnap J (eds) Biological SoilCrusts An Organizing Principle in Drylands Springer International Publishing 2016 199ndash213

[69] Chan Y Lacap DC Lau MC et al Hypolithic microbial communities between a rock and a hardplace Environm Microbiol 2012 142272ndash82

[70] Cowan D Russell N Mamais A Sheppard D Antarctic Dry Valley mineral soils contain unex-pectedly high levels of microbial biomass Extremophiles 2002 6431ndash6

[71] Vishniac H The microbiology of Antarctic soils In Friedmann EL ed Antarctic microbiologyNY Wiley-Liss 1993 297ndash341

[72] de los Riacuteos A Wierzchos J Sancho LG Ascaso C Exploring the physiological state of continen-tal Antarctic endolithic microorganisms by microscopy FEMS Microbiol Ecol 2004 50143ndash52

[73] Ramsay AJ Stannard RE Numbers and viability of bacteria in ornithogenic soils of AntarcticaPolar Biol 1986 5195ndash8

[74] French D Smith V Bacterial populations in soils of a subantarctic island Polar Biol 1986675ndash82

[75] Cameron RE King J David CN Soil microbial and ecological studies in Southern Victoria LandAntarct J US 1968 3121ndash3

[76] Aislabie JM Jordan S Barker GM Relation between soil classification and bacterial diversity insoils of the Ross Sea region Antarctica Geoderma 2008 1449ndash20

[77] Giudice AL Brilli M Bruni V De Domenico M Fani R Michaud L Bacteriumndashbacterium in-hibitory interactions among psychrotrophic bacteria isolated from Antarctic seawater (TerraNova Bay Ross Sea) FEMS Microbiol Ecol 2007 60383ndash96

[78] Nicolaus B Marsiglia F Esposito E et al Isolation of five strains of thermophilic eubacteria inAntarctica Polar Biol 1991 11425ndash9

[79] Babalola OO Kirby BM Le Roes-Hill M et al Phylogenetic analysis of Actinobacterial popula-tions associated with Antarctic Dry Valley mineral soils Environ Microbiol 2009 11566ndash76

[80] Bottos EM Scarrow JW Archer SD McDonald IR Cary SC Bacterial community structures ofAntarctic soils In Cowan D ed Antarctic Terrestrial Microbiology Physical and BiologicalProperties of Antarctic Soils Heidelberg Berlin Springer-Verlag 2014 9ndash33

[81] Kirk JL Beaudette LA Hart M et al Methods of studying soil microbial diversity J MicrobiolMethods 2004 58169ndash88




[82] Zhou J He Z Yang Y Deng Y Tringe SG Alvarez-Cohen L High-throughput metagenomic tech-nologies for complex microbial community analysis open and closed formats mBio 20156e02288ndash14

[83] Thomas T Gilbert J Meyer F Metagenomicsndasha guide from sampling to data analysis MicrobInform Exp 2012 23

[84] Tytgat B Verleyen E Obbels D et al Bacterial diversity assessment in Antarctic terrestrial andaquatic microbial mats a comparison between bidirectional pyrosequencing and cultivationPloS One 2014 9e97564

[85] Pearce DA Newsham KK Thorne MA et al Metagenomic analysis of a southern maritimeantarctic soil Front Microbiol 2012 3403

[86] Smith JJ Tow LA Stafford W Cary C Cowan DA Bacterial diversity in three different Antarcticcold desert mineral soils Microb Ecol 2006 51413ndash21

[87] Pointing SB Chan Y Lacap DC Lau MC Jurgens JA Farrell RL Highly specialized microbialdiversity in hyper-arid polar desert Proc Natl Acad Sci USA 2009 10619964ndash9

[88] Yergeau E Newsham KK Pearce DA Kowalchuk GA Patterns of bacterial diversity across arange of Antarctic terrestrial habitats Environ Microbiol 2007 92670ndash82

[89] de le Torre J Goebel BM Friedmann EI Pace NR Microbial diversity of cryptoendolithiccommunities from the McMurdo Dry Valleys Antarctica Appl Environ Microbiol 2003693858ndash67

[90] de Scally S Makhalanyane T Frossard A Hogg I Cowan D Antarctic microbial communitiesare functionally redundant adapted and resistant to short term temperature perturbationsSoil Biol and Biochem 2016 103160ndash70

[91] Friedmann EI Hua M Ocampo-Friedmann R Cryptoendolithic lichen and cyanobacterial com-munities of the Ross Desert Antarctica Polarforschung 1988 58251ndash9

[92] Wood SA Rueckert A Cowan DA Cary SC Sources of edaphic cyanobacterial diversity in theDry Valleys of Eastern Antarctica ISME J 2008 2308ndash20

[93] Wood SA Mountfort D Selwood AI Holland PT Puddick J Cary SC Widespread distributionand identification of eight novel microcystins in Antarctic cyanobacterial mats Appl EnvironMicrobiol 2008 747243ndash51

[94] Bahl J Lau MCY Smith GJD et al Ancient origins determine global biogeography of hot andcold desert cyanobacteria Nature Commun 2011 2163


[96] Taton A Grubisic S Brambilla E De Wit R Wilmotte A Cyanobacterial diversity in natural andartificial microbial mats of Lake Fryxell (McMurdo Dry Valleys Antarctica) a morphologicaland molecular approach Appl Environ Microbiol 2003 695157ndash69

[97] Khan N Tuffin M Stafford W et al Hypolithic microbial communities of quartz rocks fromMiers Valley McMurdo Dry Valleys Antarctica Polar Biol 2011 341657ndash68

[98] Wong FK Lacap DC Lau MC Aitchison JC Cowan DA Pointing SB Hypolithic microbial com-munity of quartz pavement in the high-altitude tundra of central Tibet Microb Ecol 201060730ndash9

[99] Jungblut AD Hawes I Mountfort D et al Diversity within cyanobacterial mat communities invariable salinity meltwater ponds of McMurdo ice shelf Antarctica Environ Microbiol 20057519ndash29

[100] Cowan DA Pointing SB Stevens MI Cary SC Stomeo F Tuffin IM Distribution and abioticinfluences on hypolithic microbial communities in an Antarctic Dry Valley Polar Biol 201134307ndash11



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[101] Yergeau E Bokhorst S Huiskes AH Boschker HT Aerts R Kowalchuk GA Size and structure ofbacterial fungal and nematode communities along an Antarctic environmental gradient FEMSMicrobiol Ecol 2006 59436ndash51

[102] Golubic S Friedmann I Schneider J The lithobiontic ecological niche with special referenceto microorganisms J Sediment Res 1981 51475ndash8

[103] Pointing SB Belnap J Microbial colonization and controls in dryland systems Nature RevMicrobiol 2012 10551ndash62


[105] Makhalanyane TP Valverde A Gunnigle E Frossard A Ramond JB Cowan DA Microbial ecol-ogy of hot desert edaphic systems FEMS Microbiol Rev 2015 39203ndash21


[107] Makhalanyane TP Valverde A Birkeland N-K Cary SC Tuffin IM Cowan DA Evidence for suc-cessional development in Antarctic hypolithic bacterial communities ISME J 2013 72080ndash90

[108] Le PT Makhalanyane TP Guerrero LD Vikram S Van de Peer Y Cowan DA Comparativemetagenomic analysis reveals mechanisms for stress response in hypoliths from extremehyperarid deserts Genome Biol Evol 2016 82737ndash47

[109] Chan Y Van Nostrand JD Zhou J Pointing SB Farrell RL Functional ecology of an Antarctic dryvalley Proc Natl Acad Sci USA 2013 1108990ndash5

[110] Gunnigle E Ramond JB Guerrero LD Makhalanyane TP Cowan DA Draft genomic DNA se-quence of the multi-resistant Sphingomonas sp strain AntH11 isolated from an Antarctic hy-polith FEMS Microbiol Lett 2015 362fnv037

[111] Wei STS Lacap-Bugler DC Lau MCY et al Taxonomic and functional diversity of soil and hy-polithic microbial communities in Miers Valley McMurdo Dry Valleys Antarctica Front Micro-biol 2016 71642

[112] Smith MC Bowman JP Scott FJ Line MA Sublithic bacteria associated with Antarctic quartzstones Antarct Sci 2000 12177ndash84

[113] Van Goethem MW Makhalanyane TP Valverde A Cary SC Cowan DA Characterization of bac-terial communities in lithobionts and soil niches from Victoria Valley Antarctica FEMS Micro-biol Ecol 2016 92fiw051

[114] Rao S Chan Y Lacap D Hyde K Pointing S Farrell R Low-diversity fungal assemblage in anAntarctic Dry Valleys soil Polar Biol 2011 35567ndash74

[115] Arenz BE Held BW Jurgens JA Farrell RL Blanchette RA Fungal diversity in soils and historicwood from the Ross Sea Region of Antarctica Soil Biol and Biochem 2006 383057ndash64

[116] Arenz B Blanchette R Distribution and abundance of soil fungi in Antarctica at sites onthe Peninsula Ross Sea Region and McMurdo Dry Valleys Soil Biol and Biochem 201143308ndash15

[117] Gokul J Valverde A Tuffin M Cary S Cowan D Micro-eukaryotic diversity in hypolithons fromMiers Valley Antarctica Biology 2013 2331ndash40

[118] Dreesens LL Lee CK Cary SC The distribution and identity of edaphic fungi in the McMurdoDry Valleys Biology 2014 3466ndash83

[119] Uroz S Kelly LC Turpault M-P Lepleux C Frey-Klett P The mineralosphere concept miner-alogical control of the distribution and function of mineral-associated bacterial communitiesTrends Microbiol 2015 23751ndash62

[120] Kuhlman K Fusco W La Duc M et al Diversity of microorganisms within rock varnish in theWhipple Mountains California Appl Environ Microbiol 2006 721708ndash15




[121] Mergelov N Goryachkin S Shorkunov I Zazovskaya E Cherkinsky A Endolithic pedogene-sis and rock varnish on massive crystalline rocks in East Antarctica Eurasian Soil Sci 201245901ndash17

[122] Edwards HG Newton EM Wynn-Williams DD Coombes SR Molecular spectroscopic studies oflichen substances 1 parietin and emodin J Mol Struct 2003 64849ndash59

[123] Howard-Williams C Vincent WF Microbial communities in southern Victoria Land streams(Antarctica) I Photosynthesis In Vincent WF Ellis-Evans JC (eds) High Latitude LimnologySpringer Netherlands 1989 27ndash38

[124] Grube M Cernava T Soh J et al Exploring functional contexts of symbiotic sustain withinlichen-associated bacteria by comparative omics ISME J 2015 9412ndash24

[125] Erxleben A Gessler A Vervliet-Scheebaum M Reski R Metabolite profiling of the mossPhyscomitrella patens reveals evolutionary conservation of osmoprotective substances PlantCell Rep 2012 31427ndash36

[126] Zucconi L Onofri S Cecchini C et al Mapping the lithic colonization at the boundaries of lifein Northern Victoria Land Antarctica Polar Biol 2016 3991ndash102

[127] Wynn-Williams D Cyanobacteria in Deserts ndash Life at the Limit In Whitton BA Potts M (eds)The Ecology of Cyanobacteria Springer Netherlands 2002 341ndash66

[128] Selbmann L Grube M Onofri S Isola D Zucconi L Antarctic epilithic lichens as niches forblack meristematic fungi Biology 2013 2784ndash97

[129] Selbmann L De Hoog G Mazzaglia A Friedmann E Onofri S Fungi at the edge of life cryp-toendolithic black fungi from Antarctic desert Stud Mycol 2005 511ndash32

[130] Broady PA The ecology of sublithic terrestrial algae at the Vestfold Hills Antarctica BritishPhycological Journal 1981 16231ndash40

[131] Broady PA Ecological and taxonomic observations on subaerial epilithic algae from PrincessElizabeth Land and Mac Robertson Land Antarctica Br Phycol J 1981 16257ndash66

[132] De Los Rios A Wierzchos J Sancho LG Green TA Ascaso C Ecology of endolithic lichens colo-nizing granite in continental Antarctica Lichenol 2005 37383ndash95

[133] Hughes KA Lawley B A novel Antarctic microbial endolithic community within gypsum crustsEnviron Microbiol 2003 5555ndash65

[134] Weber B Buumldel B Endoliths In Reitner J Thiel V (eds) Encyclopedia of Geobiology SpringerNetherlands 2011 348ndash55

[135] Nienow J Friedmann E Ocamp-Friedmann R Endolithic microorganisms in arid regions InEncyclopedia of environmental microbiology NY John Wiley amp Sons Inc 2003 21100ndash12

[136] De Los Riacuteos A Grube M Sancho LG Ascaso C Ultrastructural and genetic characteristics ofendolithic cyanobacterial biofilms colonizing Antarctic granite rocks FEMS Microbiol Ecol2007 59386ndash95

[137] Friedmann EI Endolithic microbial life in hot and cold deserts Orig Life 1980 10223ndash35[138] Pointing SB Warren-Rhodes KA Lacap DC Rhodes KL McKay CP Hypolithic community shifts

occur as a result of liquid water availability along environmental gradients in Chinarsquos hot andcold hyperarid deserts Environ Microbiol 2007 9414ndash24

[139] Archer SD de los Riacuteos A Lee KC et al Endolithic microbial diversity in sandstone and granitefrom the McMurdo Dry Valleys Antarctica Polar Biol 2016 doi101007s00300-016-2024-9

[140] Buumldel B Bendix J Bicker FR Allan Green T Dewfall as a water source frequently activates theendolithic cyanobacterial communities in the granites of Taylor Valley Antarctica J Phycol2008 441415ndash24

[141] Buumldel B Schulz B Reichenberger H Bicker F Green T Cryptoendolithic cyanobacteria fromcalcite marble rock ridges Taylor Valley Antarctica Algol Stud 2009 12961ndash9

[142] Jungblut AD Neilan BA NifH gene diversity and expression in a microbial mat community onthe McMurdo Ice Shelf Antarctica Antarct Sci 2010 22117ndash22



References | 71

[143] Yung CC Chan Y Lacap DC et al Characterization of chasmoendolithic community in MiersValley McMurdo Dry Valleys Antarctica Microb Ecol 2014 68351ndash9

[144] Choi A Cho H Kim S-H Thamdrup B Lee S Hyun J-H Rates of N2 production and diversityand abundance of functional genes associated with denitrification and anaerobic ammoniumoxidation in the sediment of the Amundsen Sea Polynya Antarctica Deep Sea Res Part II TopStud Oceanogr 2016 123113ndash25

[145] Goordial J Davila A Greer C et al Comparative activity and functional ecology of permafrostsoils and lithic niches in a hyper-arid polar desert Environ Microbiol 2016 19443ndash58

[146] Tahon G Tytgat B Stragier P Willems A Analysis of cbbL nifH and puf LM in soils from theSoslashr Rondane Mountains Antarctica reveals a large diversity of autotrophic and phototrophicbacteria Microb Ecol 2016 71131ndash49

[147] Wei ST Fernandez-Martinez M-A Chan Y et al Diverse metabolic and stress-tolerance path-ways in chasmoendolithic and soil communities of Miers Valley McMurdo Dry Valleys Antarc-tica Polar Biol 2015 38433ndash43

[148] Edwards RA Rohwer F Viral metagenomics Nature Rev Microbiol 2005 3504ndash10[149] Dinsdale EA Edwards RA Hall D et al Functional metagenomic profiling of nine biomes

Nature 2008 452629ndash32[150] Schoenfeld T Liles M Wommack KE Polson SW Godiska R Mead D Functional viral metage-

nomics and the next generation of molecular tools Trends Microbiol 2010 1820ndash9[151] Fancello L Trape S Robert C et al Viruses in the desert a metagenomic survey of viral com-

munities in four perennial ponds of the Mauritanian Sahara ISME J 2013 7359ndash69[152] Wilson WH Lane D Pearce DA Ellis-Evans JC Transmission electron microscope analysis

of virus-like particles in the freshwater lakes of Signy Island Antarctica Polar Biol 200023657ndash60

[153] Zawar-Reza P Arguumlello-Astorga GR Kraberger S et al Diverse small circular single-strandedDNA viruses identified in a freshwater pond on the McMurdo Ice Shelf (Antarctica) InfectGenet and Evol 2014 26132ndash8

[154] Yau S Lauro FM DeMaere MZ et al Virophage control of antarctic algal hostndashvirus dynamicsProc Natl Acad Sci USA 2011 1086163ndash8

[155] Laybourn-Parry J Anesio AM Madan N Saumlwstroumlm C Virus dynamics in a large epishelf lake(Beaver Lake Antarctica) Freshwater Biol 2013 581484ndash93

[156] Le Romancer M Gaillard M Geslin C Prieur D Viruses in extreme environments Rev EnvironSci Bio 2007 617ndash31

[157] Zablocki O Adriaenssens EM Cowan D Diversity and ecology of viruses in hyperarid desertsoils Appl Environ Microbiol 2016 82770ndash7

[158] Hopkins D Swanson M Taliansky M What do we know about viruses in terrestrial Antarc-tica In Cowan D ed Antarctic Terrestrial Microbiology Physical and Biological Properties ofAntarctic Soils Heidelberg Berlin Springer-Verlag 2014 79ndash90

[159] Williamson KE Radosevich M Smith DW Wommack KE Incidence of lysogeny within temper-ate and extreme soil environments Environ Microbiol 2007 92563ndash74

[160] Zablocki O van Zyl L Adriaenssens EM et al High diversity of tailed phages eukaryoticviruses and virophage-like elements in the metaviromes of Antarctic soils Appl Environ Mi-crobiol 2014 806888ndash97

[161] Hogg ID Stevens MI Wall DH Invertebrates In Cowan D ed Antarctic Terrestrial Microbiol-ogy Physical and Biological Properties of Antarctic Soils Heidelberg Berlin Springer-Verlag2014 55ndash78

[162] Boveng PL Hiruki LM Schwartz MK Bengtson JL Population growth of Antarctic fur sealslimitation by a top predator the leopard seal Ecology 1998 792863ndash77




[163] Xu Z Malmer D Langille MG Way SF Knight R Which is more important for classifying micro-bial communities whorsquos there or what they can do ISME J 2014 82357ndash9

[164] Rampelotto PH Extremophiles and extreme environments Life 2013 3482ndash5[165] Olsson-Francis K de la Torre R Cockell CS Isolation of novel extreme-tolerant cyanobacteria

from a rock-dwelling microbial community by using exposure to low Earth orbit Appl EnvironMicrobiol 2010 762115ndash21

[166] Sharon I Banfield JF Genomes from metagenomics Science 2013 3421057ndash8[167] Albertsen M Hugenholtz P Skarshewski A Nielsen KL Tyson GW Nielsen PH Genome se-

quences of rare uncultured bacteria obtained by differential coverage binning of multiplemetagenomes Nat Biotechnol 2013 31533ndash8

[168] Chatterji S Yamazaki I Bai Z Eisen JA CompostBin A DNA composition-based algorithmfor binning environmental shotgun reads In Vingron M Wong L (eds) Annual InternationalConference on Research in Computational Molecular Biology Heidelberg Berlin Springer-Verlag 2008 17ndash28

[169] Lewin A Wentzel A Valla S Metagenomics of microbial life in extreme temperature environ-ments Curr Opin Biotechnol 2013 24516ndash25

[170] Cowan DA Chown SL Convey P et al Non-indigenous microorganisms in the Antarctic as-sessing the risks Trends in Microbiol 2011 19540ndash8

[171] Nielsen KM Johnsen PJ Bensasson D Daffonchio D Release and persistence of extracellularDNA in the environment Environ Biosafety Res 2007 637ndash53

[172] Carini P Marsden PJ Leff JW Morgan EE Strickland MS Fierer N Relic DNA is abundant in soiland obscures estimates of soil microbial diversity Nature Microbiol 2016 216242



Matthew A Bowker Burkhard Buumldel Fernando T Maestre Anita JAntoninka and David J Eldridge5 Bryophyte and Lichen Diversity on Arid Soils

Determinants and Consequences

51 Overview

Arid regions are distinct frommost 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) Biocrustsare a feature of arid regions worldwide in both hot and cold climates where they area permanent component of successionally mature ecosystems [1] Biocrusts are a con-tinuous soil aggregate of the uppermost millimeters of the soil distinguishable fromother types of soil crust in that they are engineered by biota [2] They harbor a widevariety of organisms (archaea fungi and bacteria ndash notably cyanobacteria [3ndash5]) inaddition to mosses liverworts and lichens the subject of this chapter

511 Moss Liverwort and Lichen Biology

Mosses and liverworts are often grouped as ldquobryophytesrdquo although current under-standing regards these as a polyphyletic group [6] We will use the term bryophytehere for convenience to collectively refer to both mosses and liverworts Both are trueplants of the kingdom Plantae which lack the lignified vascular tissue character-istic of tracheophytes [7] Without these tissues their size is constrained confiningthem to the soil surface often beneath and in between vascular plants Bryophytesare older than vascular plants and are first encountered on land in the middle Or-dovician period (sim470mya) prior to the formation andbreakup of the supercontinentPangea [8] Perhaps not surprisingly they are found on all continents Both mossesand liverworts may have impressive desiccation tolerance strategies to cope with lowwater availability and are commonly found on arid soils as well [9] Bryophytes donot reproduce by seed but instead produce spores as a result of sex dispersed by thesporophyte Although spores can be dispersed long distances including from conti-nent to continent [10] many dominant bryophytes of arid regions produce no or fewsporophytes [11 12] constraining their dispersal and possibly generating local adap-tation Bryophytes are generally capable of vegetative reproduction from any type oftissue [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 1015159783110419047-005



74 | 5 Bryophyte and Lichen Diversity on Arid Soils Determinants and Consequences

alga or cyanobacterium) Though they are often grouped together with bryophytes asnonvascular ldquoplantsrdquo they do not belong to the kingdomPlantae rather they are clas-sified as fungi and named based upon the mycobiont [15] Despite lacking taxonomicrelatedness lichens do share some characteristics with bryophytes including repro-duction by spores and the lack of specialized water conductance mechanisms whichis related to small size anddesiccation tolerance Lichens are apparently younger thanbryophytes dating to sim415mya (the Devonian period) [16] but have controversiallybeen proposed to date over 100 mya earlier [17] Lichens are found on all continentsare small in stature and confined near to surfaces such as soils Spores are the productof sex in the fungal biont and can be a long-distance dispersal agent [18] but to form alichen must encounter a compatible photobiont upon germination [19] Many lichensalso reproduce vegetatively from propagules that contain both mycobiont fungal cellsand 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 totemperate tree trunks to rock outcrops to arid zone biocrusts In drylands at localscales theymay comprise a substantial amount of the eukaryotic diversity present [2122] The purpose of this chapter is to summarize the dimensions of their biodiversity onarid soils outline someof themajor determinants of their biodiversity and summarizethe effects of bryophyte and lichen biodiversity on arid soil function

52 Global Diversity and Characteristic Taxa

521 Global Species Pool

The diversity distribution of biocrust organisms around the world is incompletelyknown As a first approach to quantify this we defined seven geographical regionsspanning arid and semiarid areas as well as polar deserts and initial soils of thetemperate boreal and arctic climatic zones which are characterized by a very sparsecover of vascular plants (Asia Africa North America including Central Americaand Greenland South America Antarctica Europe and the Pacific region ie Aus-tralia and New Zealand) In total 323 bryophyte (68 liverworts 255 mosses) and 553lichen species (88 cyanolichens 465 chlorolichens) have been identified explicitlyas biocrust components all globally presently being unevenly distributed amongstthe different geographical regions (continents and subcontinents) partly due to dif-fering research effort in different parts of the world [5 23ndash35] (998835 Fig 51) Among allgeographical regions differentiated here South America is the least known in termsof biocrust presence and their diversity and taxonomic composition Only recentlyhave research activities emerged investigating biocrusts of several regions of thisunderstudied continent [36ndash38]



52 Global Diversity and Characteristic Taxa | 75

0

AsiaAfric

aNorth

America

South

America

Antarctica

EuropePacifi

c

Geographical region decreasing size

50

100

150

20033

579

000

km2

305

215

32 km

2

247

090

00 km

2

178

400

00 km

2

140

000

00 km

2

1018

000

0 km

2

7960

000

km2

250

300Cyanolichens Chlorolichens Liverworts Mosses

Spec

ies n

umbe

r

Fig 51 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 biocrustbryophytes are well known only for Europe North America and the Pacific region(998835 Fig 51) The highest species numbers found so far have been in Europe followedby North America and Asia In Europe and North America there are many scientistsworking on this topic while in Asia this is true for Russia and China only

522 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 3mosses) occurred in at least fourout of the seven geographical regions (998835 Tab 51) These can be thought of as the morecosmopolitan characteristic taxa Two lichens but no bryophytes are documented inbiocrusts 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 287bryophyte (60 liverworts 227 mosses) and 411 lichen species (64 cyanolichens 347chlorolichens) the bulk of species from biocrusts is restricted to only one of the sevengeographical regions (998835 Fig 52) In two of the seven regions we found 26 bryophytesand 95 lichens whereas in three of seven regions the number declined to 7 bryophytesand 30 lichens For further details see 998835 Fig 52 and 998835 Tab 51 While it is true that a




Table 51 List of the 56 lichen and bryophyte species recorded from at least three out of the sevengeographical regions defined here [23ndash35] Species are arranged first according to their frequencyand second alphabetically

Species Asia

Afric

a

N-Am

eric

a1

S-Am

eric

a

Anta

rctic

a

Euro

pe

Paci

fic2

LichensHeppia despreauxii (Mont) Tuck times times times times times times

Placidium squamulosum (Ach) Breuss times times times times times times

Collema tenax (Sw) Ach times times times times times

Diploschistes diacapsis (Ach) Lumbsch times times times times times

Diploschistes muscorum (Scop) R Sant times times times times times

Endocarpon pusillum Hedw times times times times times

Peltula patellata (Bagl) Swinsc amp Krog times times times times times

Placidium lacinulatum (Ach) Breuss times times times times times

Placidium pilosellum (Breuss) Breuss times times times times times

Psora decipiens (Hedw) Hoffm times times times times times

Toninia sedifolia (Scop) Timdal times times times times times

Cladonia fimbriata (L) Fr times times times times

Cladonia furcata (Huds) Schrad times times times times

Collema coccophorum Tuck times times times times

Fulgensia fulgens (Sw) Elenkin times times times times

Heppia adglutinata (Kremp) A Massal times times times times

Heppia lutosa (Ach) Nyl times times times times

Acarospora nodulosa (Dufour) Hue times times times

Buellia epigaea (Hoffm) Tuck times times times

Buellia punctata (Hoffm) A Massal times times times

Candelariella vitellina (Hoffm) Muumlll Arg times times times

Cetraria islandica (L) Ach times times times

Cladonia cervicornis (Ach) Flot times times times

Cladonia foliacea (Huds) Willd (including C convoluta) times times times

Cladonia pocillum (Ach) O J Rich times times times

Cladonia pyxidata (L) Hoffm times times times

Cladonia verticillata (Hoffm) Schaer times times times

Collema crispum var crispum (Huds) Weber ex F H Wigg times times times

Fulgensia bracteata ssp bracteata (Hoffm) Raumlsaumlnen times times times

Fulgensia desertorum f macrospora Llimona times times times

Fulgensia subbracteata (Nyl) Poelt times times times

Gypsoplaca macrophylla (Zahlbr) Timdal times times times

Heppia solorinoides (Nyl) Nyl times times times

Peccania fontqueriana P P Moreno amp Egea times times times

Peltula obscurans (Nyl) Gyelnik times times times

Peltula radicata Nyl times times times

Phaeorrhiza nimbosa (Fr) H Mayrhofer amp Poelt times times times

Placynthium nigrum (Huds) Grey times times times

Psora crenata (Taylor) Reinke times times times




Table 51 (cont) List of the 56 lichen and bryophyte species recorded from at least three out of theseven geographical regions defined here [23ndash35] Species are arranged first according to their fre-quency and second alphabetically

Species Asia

Afric

a

N-Am

eric

a1

S-Am

eric

a

Anta

rctic

a

Euro

pe

Paci

fic2

Psora lurida Ach times times times

Rinodina terrestris Tomin times times times

Squamarina cartilaginea (With) P James times times times

Squamarina lentigera (Weber) Poelt times times times

Toninia aromatica (Turner) AMassal times times times

Toninia lutosa (Ach) Timdal times times times

Toninia ruginosa (Tuck) Herre times times times

BryophytesBryum argenteum Hedw times times times times times

Bryum caespiticium Hedw times times times times

Ceratodon purpureus (Hedw) Brid times times times times

Weissia controversa Hedw times times times

Crossidium crassinerve (De Not) Jur times times times

Didymodon cf rigidulus Hedw times times times

Riccia lamellosa Raddi times times times

Riccia sorocarpa Bisch times times times

Syntrichia ruralis (Hedw) FWeber amp DMohr times times times

Trichostomum brachydontium Bruch ex F Muell times times times

1 including Central America and Greenland2 Australia New Zealand

0

(a) (b)

Spec

ies n

umbe

r

100

200

CyanolichensChlorolichens

LiverwortsMosses

300

400

0

Spec

ies n

umbe

r

100

50

150

200

250

1 geogr r

egion

2 geogr regions

3 geogr regions

4 geogr regions

5 geogr regions

6 geogr regions

All regions

1 geogr r

egion

2 geogr regions

3 geogr regions

4 geogr regions

5 geogr regions

6 geogr regions

All regions

Fig 52 Frequency of lichen (a) and bryophyte (b) species across seven geographic regions




lack of detection does not mean that a taxon is truly absent from a region these datasuggest a considerable amount of species turnover from continent to continent Moresampling effort is necessary to fill in current distribution gaps

53 Determinants of Moss Liverwort and Lichen Diversityon Arid Soils

531 Geographic Isolation and Biogeography

At large scales dispersal limitations likely shape the bryophyte and lichen β diversityof major landmasses the genetic diversity and distinctiveness and α diversity of aridsoil bryophyte and lichen communities Bryophytes and lichens can disperse sporesover long distances eg from continent to continent [10 18] However many drylandspecies may rely more upon vegetative propagules eg tissue fragments which aremuchmore dispersal limited due to their larger size possibly allowing for geographicisolation

At the global scale we might expect that the mode of reproduction dictates thedistribution of species and we can hypothesize that this mechanism arranges aridsoil bryophytes and lichens into groups based on dispersal limitation The less dis-persal limited group which might abundantly produce spores and in the case oflichens also associate with a widely distributed photobiont would be expected tobe widespread or possibly cosmopolitan An exemplar might be the moss Ceratodonpurpureus which is a prolific sporophyte producer present on all continents (thoughnot always in arid soil biocrusts) [10] For lichens long distance dispersal of sporesis not sufficient in and of itself because the spores must encounter a compatiblephotobiont The lichen Psora decipiens is a broadly distributed lichen which mayreduce this problem by associating with multiple photobionts [39] There are limitsto spore distribution therefore even among cosmopolitan species Genetic distanceand floristic dissimilarity among populations may increase as connectivity via windor geographic proximity decreases [18]

Other species are dispersal limited due to a lack of successful reproduction viaspores and may either be widespread (found on several continents) or restricted inrange (found on one or a few continents) Widespread dispersal limited species maybe hypothesized to be relatively old predating the breakup of the supercontinentsSuch species might exhibit a strong degree of interspecific variation and local adap-tation for example chemical races of lichens (Culberson 1986) Widespread dispersallimited species could be either common or rare Common ones might include speciesfound in arid regions of multiple landmasses but only rarely reproduce sexually Thelichen Gypsoplaca macrophylla may be an example of a rare species that falls withinthis group Currently it has a wide distribution on three continents including aridgypsiferous soils of southwestern US [22] in addition to Greenland the Alps and a



53 Determinants of Moss Liverwort and Lichen Diversity on Arid Soils | 79

few localities in Asia [40] It is always a rare communitymember Perhaps this strangedistribution arose through extinction of a formerly widespread taxon

Geographically restricted and dispersal limited species might be found onlywithin a single major land mass or a portion of one These endemic communitycomponents might be hypothesized to represent evolutionarily younger species thatarose after the breakup of the continents and have remained isolated due to long-distance dispersal limitation The lichen genus Xanthoparmelia originated after thebreakup of the continents [41] and has multiple species that have adopted a relianceon dispersal of vagrant unattached thalli as propagules [42] This reliance on localdispersal may explain the large degree of local endemism in this genus [42]

532 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 withspatial scale from continental and landscape scales down to the scale of meters orless

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 orinfrequency of thawing temperatures For example there are no liverworts or cyano-lichens known fromAntarctica (998835 Fig 51)Wemayhypothesize that chlorolichens andmosses are more able to survive given the rarity of liquid water or are able to activatephotosynthesis with less water

Within less extremeclimates in the temperate and tropical regions biocrust lichenand moss richness is correlated with soil moisture across large precipitation gradi-ents [43] Cooler habitats appear to support a large diversity and biomass of lichentaxa [44] possibly because the balance of photosynthesis and respiration betweenthe symbiotic partnersmaximizes the opportunity to form complex thallus structuresSimilarly higher rainfall has been correlated with increasing richness and changesin biocrust composition [45] Rainfall seasonality can also have marked effects onbiocrust composition [27 46] In Australia for example biocrust lichens are restrictedto winter rainfall dominant areas where they are able to avoid hydration of the thallusduring extremely hot weather [47] Despite the preference for winter rainfall very coldtemperatures are not necessarily preferred Areas in the northwestern United States (awinter rainfall region) with warmer winter temperatures have been shown to be moreconducive to crust development than areas with colder winters [48] Biocrust speciesrichness and composition are also known to vary with altitude which is usually a sur-rogate for increasing precipitation and decreasing temperature [26] Castillo-Monroyet al [37] showed that biocrust species richness in an Ecuadorian dryland increasedwith increasing elevation with clear differences in composition along the elevational




gradient These altitudinal differences can be attributed to the redistribution of runoffand 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 biocrustcover and composition For example the two major patch types in drylands (resourceshedding water runoff zones and resource accumulating water runon zones) that re-sult from the redistribution of water support different taxa at small scales Lichensand cyanobacteria typically dominate resource shedding areas whereas micrositeswhere resources accumulate are often dominated by bryophytes [49 50] The mech-anism behind this distribution may relate to the need for bryophytes to access freewater to reproduce but is also related to competition with vascular plants (eg 5152]At the microsite scale the distribution of biocrust taxa is strongly dependent on soilmoisture [22 53ndash55] and the availability of suitable niches for establishment Thesemicrosites are often areas that receive slightly moremoisture are cooler and shelteredfrom temperature extremes [56 57]

Biocrusts lichens and mosses have been predicted to mediate any substantial ef-fects on ecosystem functioning due to climate change [58ndash60] However there are alsolikely to be substantial changes in biocrust composition and richness resulting froma changing climate For example Ferrenberg et al [61] showed that an increase insmall 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 dominatedbiocrusts with warming after 4 years [62]

533 CalcicolendashCalcifuge Dichotomy and Soil pH Gradients

Biocrust β diversity particularly that of lichens is known to be strongly influencedby soil pH which in turn is strongly influenced by the concentrations of calcium (Ca)carbonate and other carbonates in the soil [27 28 48 63ndash65] The relationship be-tween lichen taxa and soil pH is so pronounced that lichens have been classified intotwo broad functional groups according to their response to soil pH Calciphiles whichinclude the majority of soil lichens in drylands are strongly associated with soils ofhighpH Conversely calcifugeshavea low tolerance tohighpHsoils [66] andappear tobe more common in mesic soils This dichotomy recurs in many locations around theworld dictating both biocrust abundance and community composition In drylandsin the western USA and Ecuadorian dry mountain shrublands biocrusts reach theirgreatest development on neutral to acidic soils [37 48] In other dryland areas of theUSA Spain Australia and Israel biocrust lichens and bryophytes are more diverseand occupy a greater cover in areas of high pH (eg [17 47 63 67 68]) Lichens inhab-iting Ca rich soils are thought to have greater concentrations of Ca oxalate on the outersurface of the thallus reducing the concentration of Ca in the immediate area where




the lichen attaches [69] Magnesium manganese and other nutrients have also beenshown 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

534 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 andspecies turnover of soil mosses liverworts and lichens in a given region [72ndash74] Forexample on the Colorado Plateau (USA) out of eight different soil types gypsifer-ous soils had the greatest species richness (sim21 species per site) supported the sec-ond greatest species evenness and supported eight indicator species out of a total of19 [22] In this case study the gypsiferous soils had a disproportionately large effecton diversity at both local scales and within the entire study area Higher taxonomicand functional richness of both mosses and lichens is also reported in Europe andAustralia on gypsum soils [28 72 73 75]

Gypsiferous arid soils of the Northern hemisphere and Australia often appear tobe dominated by well distributed gypsophile lichen taxa such as Diploschistes sppPsora decipiens Fulgensia spp Acarospora nodulosa and Squamarina lentigeraamong others [22 28 72 76ndash78] Where gypsum soils are rare in the landscape thesespecies may be rare or narrowly distributed within a region despite local abundanceand wide distribution globally Gypsiferous soils also appear to harbor a larger num-ber of endemics compared to other soils a phenomenon also observed in vascularplants [79] Perhaps this is because the specific edaphic preferences of the lichenscoupled with dispersal limitations lead to narrow distributions One example isLecanora gypsicola described in 1998 and known only from sporadically occurringgypsiferous soils of the western United States [80]

Dominantmosses of gypsiferous arid soils appear to differmore than lichens fromregion to region andmay be generalist species rather than gypsum specialists [22 78]Widespread but usually subdominant gypsophile species includeAloina bifrons anda 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 onlyfrom 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 thattwomoss specieswith no reported preference for gypsumwere able to tolerate its pres-ence Thus the ability to grow on gypsum might be widespread in mosses and thismight contribute to high α diversity butwould not explain high species turnover fromgypsiferous habitats to nongypsiferous habitats nearby Rather true gypsophilesmust




either derive a benefit from growing in the habitat type or resist its specific stressesbetter thanmost species Gypsumcontains Ca and sulfur both essential nutrients Thefact that some gypsophiles also are found on soil rich in Ca carbonate might suggesta 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 hypothesizedthat this is amechanism for copingwith excess Ca [83] Thismay be an intriguing cluesince lichen pruina are composed of Ca oxalates andmost lichens preferentially grow-ingongypsumabundantly producepruinaNonetheless soils rich inCa carbonatebutnot gypsum often have different floras [22 84] suggesting that Ca alone is an unlikelyexplanation of unique lichen and bryophyte assemblages on gypsiferous soils

54 Consequences of Moss Liverwort and Lichen Diversityon Arid Soils

541 Contribution of Biocrust Lichens and Bryophytes to Arid Ecosystem Function

Biocrust mosses and lichens play major roles in nutrient cycling and in building andmaintaining soil fertility Lichen and bryophyte dominated biocrusts are an importantpart of the global carbon (C) budget taking up from 1 to 37 g Cmminus2yrminus1 in arid landsdepending on the species composition amount of cover and water availability [85ndash87] This is a substantial contribution to productivity in arid lands accounting for asmuch as 37ndash139 of net primary productivity [88] Likewise lichens and bryophytesplay key roles in regulating terrestrial nitrogen (N) cycling N is commonly the mostlimiting nutrient in terrestrial ecosystems [89] Many lichens house N fixing cyanobac-terial symbionts within their thallus and likewise biocrust mosses are known tohost N fixing symbionts on their leaves [90 91] Enzyme activity is high in lichen andmoss dominated biocrusts and is dependent on species composition which is impor-tant for N C and phosphorous cycling [92] Microbial N fixation and N transformationactivity is known to be stimulated within biocrusts [93] and these combined activitiescan account for the majority of available N input to arid systems [88 94] They alsocapture dust which helps to promote ecosystem productivity by addition of both soiland nutrients to the ecosystem [95]

Because mosses and lichens bind the soil together with filamentous structuressuch as hyphae rhizines and rhizoids they aggregate soil reducing soil loss due towind and water erosion [96 97] This is true even during inactivity because lichensand bryophytes of biocrusts have remarkable desiccation tolerance [98 99] and thephysical structure of the biocrust persists

Due to the physical structure of the biocrusts mosses and lichens have complexeffects on soil hydrology which are largely dependent on biocrust composition rain-fall intensity ambient temperature and soil texture [50 100 101] Lichens can havemixed effects either generating runoff or promoting infiltration depending upon the



54 Consequences of Moss Liverwort and Lichen Diversity on Arid Soils | 83

surface connectivity of the lichen thallus whereasmosses have greater surface rough-ness and high water absorbing capacity at 100minus1000times their dry mass enhancinginfiltration [101 102] Sinuous microtopography of well developed lichen and mossbiocrusts can slow down the movement of water enhancing infiltration compared tosmoother cyanobacterial biocrusts but many lichen biocrusts can generate runoff athigh rainfall events [97 103 104]Well developed crusts also influencewater retentionby reducing evaporation [104 105] All of these factors influence water availability forvascular plants and the soil food web

Finally biocrusts composed of bryophytes and lichens support a vibrant soilfood web in the top millimeters of soil because they leak much of the C and N thatthey 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 andre-assimilated [107] Lichens and bryophytes produce a number of secondary com-pounds that provide protection from harmful ultraviolet radiation [108ndash110] Surfacebryophyte and lichen community resilience is critical for protecting biocrust commu-nity members that lack UV protection (eg light cyanobacteria)

542 BiodiversityndashEcosystem Functioning Relationship

Understanding the links between biodiversity and those processes that determinethe functioning of ecosystems (biodiversityndashecosystem functioning relationship) hasbeen a major research topic in community and ecosystem ecology over the last twodecades [111ndash114] During this period several hundred biodiversityndashecosystem func-tioning relationship studies have been conducted with a wide variety of organismssuch as vascular plants algae and soil fauna and ecosystem processes includingprimary 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 constituentssuch as lichens and mosses affect ecosystem functioning [115 116 118 121 126ndash128]Indeed some attributes of biocrusts such as small size and the ease of transplantandor culturing their constituents make them particularly suitable for biodiversityand ecosystem functioning research and their use by researchers on this topic isbeing encouraged [132]

Most studies on the biodiversityndashecosystem function relationship to date havefocused on particular ecosystem processes such as productivity and on species rich-ness as a focal aspect of biodiversity [111 113] These studies provide ample evidenceof positive richness function relationships in nature As an example Cardinale etal [113] found that the relationship between producer diversity and biomass was bestdescribed by some form of a positive but decelerating curve in 79 (of 272) studieswhile linear relationships were found in only 13 of cases Similar results were foundwhen looking at functions such as nutrient uptake (89 positive but decelerating




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 noexception to the positive relationship betweenbiodiversity and ecosystem functioningreported with other organisms however they more commonly exhibit approximatelylinear relationships between the number of macroscopic species (bryophytes andlichens) and various indicators of nutrient cycling hydrological and soil develop-ment and retention functions Positive richness function relationships are supportedin multiple observational field studies conducted in drylands [115 116] althoughsometimes negative effects or no effects are reported [117]

Moisture availability also plays a role in determining biodiversityndashecosystemfunctioning relationships Mulder et al (2001) experimentally tested the relation-ships between species diversity and productivity using mosses and liverworts [118]They found that biomass increasedwith species richness but onlywhen communitieswere subject to experimental drought Rixen and Mulder [119] exposed arctic tundramoss communities of varying richness to two drought and density levels and foundthat productivity was increased in the species rich communities particularly in thelow density plots but only when plots were watered regularly They also found thatmoisture retention improved at high species richness levels as a result of the positiveeffects 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 morestrongly 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 tomultiple ecosystem functions related to nutrient cycling More studieson this topic will help partition the relative influence of bryophyte lichen and micro-bial diversity on ecosystem functions

543 Effects of Species Richness Turnover and Evenness on Ecosystem Functions

Despite biodiversity encompassing multiple components most studies on the biodi-versityndashecosystem functioning relationship conducted to date have targeted speciesrichness or α diversity as the main biodiversity descriptor [113] However there isgrowing evidence suggesting that other components of biodiversity such as speciesevenness β diversity (species turnover) trait diversity functional group diversityphylogenetic diversity and within species genetic diversity have the potential to in-fluence ecosystem processes [122ndash125] Only some of these elements of biodiversityhave been investigated using biocrusts In 998835Tab 52 we compile results from theliterature on the frequency of effects of biocrust lichen and bryophyte α diversity




Table 52 Percentage of cases in which α diversity evenness and β diversity of biocrust bryophytesandor 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 maineffects only in some cases interactive effects are detected White filled cells indicate no data Blackfilled 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 ofdatasets in which there are gt 0 effects on ecosystem function indicators detected

Dataset αdi

vers

ity

po

sitiv

e

even

ness

po

sitiv

e

βdi

vers

ity

Function indicators

Single site AlicanteSpain [117]

0 80 25 bulk density respirationorganic C total N soilaggregate stability

Single site CuencaSpain [117]


Many sites Utah USA [115] 100 100 100 0 magnetic susceptibility

Many sites ArizonaUSA [115]

50 100 50 100 surface roughness soilaggregate stability

Many sites Utah USA [115] 100 50 0 magnetic susceptibilitysurface roughness

Single site Communidadde Madrid Spain [36 115133]

33 100 0 100 phosphataseβ-glucosidase urease

Single site Communidad deMadrid Spain [50]

0 100 Steady state infiltration

Many sites Central ampSouthern Spain (gypsumsoils) [116 128]

833 100 167 100 667a ldquoC cyclingrdquo respirationphosphatase total Nurease multifunctionality

Many sites Central amp South-ern Spain (calcareoussoils) [116 128]

429 667 143 100 333a organic C β-glucosidaserespiration phosphatasetotal N ureasemultifunctionality

Constructed biocrusts com-position experiment (sur-face) [126 134]

20 0 10 ammonium nitrateorganic C total Nβ-glucosidasephosphatase ureaseN-fixationmultifunctionalitymicrobial catabolic profile

a Bowker et al 2013 [116] did not address β diversity Bowker et al 2011 [128] analyzed β diversityeffects on individual functions but not on multifunctionality




Table 52 (cont) Percentage of cases in which α diversity evenness and β diversity of biocrustbryophytes andor lichens have a detectable effect on an indicator of ecosystem function In thecase of α diversity and evenness the proportion of these effects that are positive is also reportedWe 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 Meanreflects the average proportion of ecosystem function indicators affected per dataset Frequencyreflects the percentage of datasets in which there are gt 0 effects on ecosystem function indicatorsdetected

Dataset αdi

vers

ity

po

sitiv

e

even

ness

po

sitiv

e

βdi

vers

ity

Function indicators

Constructed biocrusts com-position experiment (sub-surface) [126]

80 80 60 organic C total Nβ-glucosidasephosphatasemultifunctionality

Constructed biocrustsevenness experiment (sur-face) [126 134]

10 100 0 20 ammonium nitrateorganic C total Nβ-glucosidasephosphatase ureaseN-fixationmultifunctionalitymicrobial catabolic profile

Constructed biocrusts even-ness experiment (subsur-face) [126]

60 333 0 40 organic C total Nβ-glucosidasephosphatasemultifunctionality

Single site Baja CaliforniaMexico [129]

100 CO2 gas exchange


100 organic C hexosesphenols respiration totalN microbial biomass Namino acids proteinsdissolved inorganic pphosphatase

Mean 507 686 261 650 663Frequency 846 909 500 800 1000

evenness or β diversity on ecosystem functioning Our rules for inclusion requiredan explicit manipulation or measurement of one of these elements of biodiversitya focus on biocrusts of dryland soils and a measurement of at least one indicatorof ecosystem function We excluded measurements of activity or physiology of iso-lated biocrust organisms focusing instead on the functions of biocrust communitiesFinally in our consideration of β diversity we included comparisons of biocrusts




dominated by a particular species but excluded comparisons of biocrust types andeffects of turnover among morphological groups because species compositions werenot explicitly measured

Overall available evidence suggests that as in several other communities speciesrichness commonly exerts positive effects on ecosystem functioning in biocrusts In85 of cases meeting our inclusion criteria at least one α diversity relationship wasdetected with ecosystem function (998835 Tab 52) On average about half of the ecosystemfunction indicatorswere affected by α diversity over two thirds of whichwere positiveThe magnitude and sign of these effects depend on the characteristics of the biocrustcommunity (abundance spatial pattern) the ecosystem function considered envi-ronmental conditions and the interactions among these factors Species richness hasbeen 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 traitsof biocrust constituents does not properly group species according to their impactson ecosystem functioning [51 90] Alternatively it may mean that biocrust moss andlichen species tend to have unique suites of functional traits [84 115] and perhaps atrait diversity index would prove to be even more informative than species richness

Biocrust evenness is less commonly related to ecosystem functioning at least oneevennessndashfunction relationship occurs in about half of cases and about a quarter offunctional indicators were influenced by evenness (998835 Tab 52) As with α diversitymost of these relationships were positive Despite the lower frequency of main effectsevenness is sometimes influential in interaction with other biocrust properties (egspatial patterning) [115 126 127]

Beta diversity was most the most consistent influence on ecosystem functioningRelationships between β diversity and at least one ecosystem function were detectedin all available studies meeting our criteria and two thirds of ecosystem function in-dicators examined were influenced by β diversity (998835 Tab 52) These effects extend tohydrology [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 themost influential biocrust attributes driving biodiversityndashecosystem 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]

544 Multifunctionality

Increasingly ecologists are moving beyond considering single ecosystem functionssuch as productivity to multifunctionality defined as the simultaneous performanceof 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-




phorus cycling and storage Compared with soil surfaces lacking biocrusts biocrustforming mosses enhanced multifunctionality in semiarid and arid environments butnot 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 enhanceecosystemmultifunctionality Thenext logical question iswhether 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 richnessonmultifunctionality using a comprehensive database of 94 experiments manipulat-ing species richness across a wide variety of taxa trophic levels and habitat Two keyresults from this study were (i) multifunctionality was enhanced as species richnessincreased and (ii) the overall effect of species richness on multifunctionality grewstronger as more functions were considered To date two studies have suggested thata greater number of biocrust species promotes greater multifunctionality and that agreater number of species is required to sustain multiple functions than a single func-tion (998835 Tab 52) [116 126] The few studies available indicate that diversity of biocrustmosses and lichens is highly important to maintain ecosystem multifunctionality indrylands and that biocrusts follow the general trend exhibited by other communities

545 Functional Redundancy or Singularity

Given that mosses liverworts and lichens are all poikilohydric and desiccation andstress 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 ecosystemfunction although it has been suggested that redundancymay bolster an ecosystemrsquosability to maintain function under differing conditions [131] There are two reasonswhy we doubt that biocrust bryophytes and lichens are functionally redundant Firstif biocrust mosses liverworts and lichens were redundant we would expect ecosys-tem function ormultifunctionality 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 atleast across the range of observed values an increase in richness leads to an increasein a given function or in multifunctionality [115 132] This observation might relateto variation in response to environment for example different ideal combinations ofwater and light availability and temperature for maximal photosynthetic rate amongspecies [129] A multispecies community with different environmental optima wouldbe more likely to maintain high productivity regardless of the conditions at a givenmoment 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-



55 Summary and Conclusions | 89

lar functional indicators suggesting distinct ecological roles [128 133] For examplebiocrust communities rich in the lichen Squamarina lentigera exhibited higher phos-phatase activity when compared to communities dominated byDiploschistes diacap-sis [128] Likewise mosses and lichens exhibit fundamentally different effects on hy-drologywithmosses oftenactingas infiltrationpromoters but lichens acting to gener-ate runoff [50] Differentmosses and lichens are also known to have distinct functionaltraits For example only a subset of lichens is known to have the ability to fix nitrogen(eg Collema Leptogium Heppia Peltula Peltigera) Lichen and moss species alsohave a wide chemical diversity andmany 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 onefunction is considered Functional profiles of 23 biocrust forming organisms in Spainwere tabulated alongwithall of their documented effects onecosystem functions [128]Over half of them had a unique set of effects even though many species exerted someof the same effects When considering biodiversity loss this suggests that at low lev-els of biodiversity communities may have different functional attributes based on theparticular species present As more species are added it becomes more likely thatmost functions are being conducted by at least one species and therefore multi-functionality is more likely to be sustained at higher richness [116 126]

55 Summary and Conclusions

Biocrust lichens andbryophytes shape the landscape in all areaswhere vascular plantdevelopment is limited including arid regions occupying the soil surface and provid-ing important ecosystem functions Biocrust lichens and bryophytes are documentedfrom all continents and some species arewidespread among landmasses Themajor-ity of species are restricted to one or a few geographic areas a pattern that may partlybe determined by dispersal limitations Within major landmasses α and β-diversityare largely determined by climatic gradients such as aridity or edaphic factors suchas 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 ormultifunctionality Because of this and evidence that some ecosystem functions aretied to particular species traits it is important to consider individual biocrust mossand bryophyte species as singularly important rather than functionally redundantClimate change and land use practices are already impacting the function and diver-sity of biocrust communities Management and conservation efforts should focus onmaintainingviablebiocrusthabitat (especially that of endemics) aidingdispersal andrestoring biocrust communities in degraded habitat




References

[1] Bowker MA Biological soil crust rehabilitation in theory and practice an underexploited op-portunity Restor Ecol 2007 1513ndash23

[2] Jones CG Lawton JT Shachack M Organisms as ecosystem engineers Oikos 1994 69373ndash86

[3] Garcia-Pichel F Loza V Marusenko Y Mateo P Potrafka R Temperature drives the continentalscale distribution of key microbes in topsoil communities Science 2013 3401574ndash7

[4] Steven B Kuske CR Reed SC Belnap J Climate change and physical disturbance manipula-tions result in distinct biological soil crust communities Appl Env Microbiol 2015 817448ndash59

[5] Bowker MA Belnap J Buumldel B Sannier C Pietrasiak N Eldridge DJ Rivera-Aguilar V Controlson distribution patterns of biological soil crusts at micro- to global scales In Weber B BuumldelB Belnap J (eds) Biological soil crusts an organizing principle in drylands Berlin Springer-Verlag 2016 173ndash97

[6] Mishler BD Lewis LA Buchheim MA Renzaglia KS Garbary DJ Delwiche CF ZechmanFWKantz TS Chapman RL Phylogenetic relationships of the ldquogreen algaerdquo and ldquobryophytesrdquoAnn Mo Bot Gard 1994 81451ndash83

[7] Graham LE Cook ME Busse JS The origin of plants body plan changes contributing to a ma-jor evolutionary radiation Proc Nat Acad Sci USA 2000 974535ndash40

[8] Rubinstein CV Gerrienne P de la Puente GS Astini RA Steemans P Early middle Ordovicianevidence for land plants in Argentina (eastern Gondwana) New Phytol 2010 188365ndash9

[9] Oliver MJ Velten J Mishler BD Desiccation Tolerance in Bryophytes A Reflection of the Primi-tive Strategy for Plant Survival in Dehydrating Habitats Integr Comp Biol 2005 45789ndash99

[10] McDaniel SF Shaw AJ Selective sweeps and intercontinental migration in the cosmopolitanmoss Ceratodon purpureus (Hedw) Brid Mol Ecol 2005 141121ndash32

[11] Stark LR Castetter RC A gradient analysis of bryophyte populations in a desert mountainrange Memoirs of the New York Botanical Garden 1987 45186ndash97

[12] Stark LR Mishler BD McLetchie DN The cost of realized sexual reproduction and sporophyteabortion in a desert moss Am J Bot 2000 871599ndash1608

[13] La Farge C Williams KH England JH (2013) Regeneration of Little Ice Age bryophytes emerg-ing from a polar glacier with implications of totipotency in extreme environments Proc NatAcad Sci USA 2013 1109839ndash44

[14] Glime Janice M 2007 Bryophyte Ecology Volume 1 Physiological Ecology Houghton Michi-gan USA Michigan Technological University and the International Association of Bryologists2007 (ebook accessed on 12 December 2015 at httpwwwbryoecolmtuedu)

[15] Tehler A Systematics phylogeny and classification In Nash III TH ed Lichen Biology Cam-bridge UK Cambridge University Press 1996 217ndash39

[16] Honegger R Edwards D Axe L The earliest records of internally stratified cyanobacte-rial and algal lichens from the lower Devonian of the Welsh borderland New Phytol 2013197264ndash75

[17] Retallack GJ Ediacaran life on land Nature 2013 49389ndash92[18] Muntildeoz J Feliciacutesimo AacuteM Cabezas F Burgaz AR Martiacutenez I Wind as a Long-Distance dispersal

vehicle in the southern hemisphere Science 2004 3041144ndash7[19] Seymour FA Crittenden PD Dyer PS Sex in the extremes lichen forming fungi Mycologist

2005 1951ndash8[20] Fahselt D Individuals and populations of lichens In Nash TH III ed Cambridge University

Press Cambridge 2008 252ndash73



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[21] Rosentreter R Compositional patterns within a rabbitbrush (Chrysothamnus) community ofthe Idaho Snake River Plain In McArthur D Durant E Welch BL (eds) Proceedings Sympo-sium on the biology of Artemisia and Chrysothamnus Ogden Utah US Department of Agricul-ture 1986 273ndash7

[22] Bowker MA Belnap J A simple classification of soil types as habitats of biological soil crustson the Colorado Plateau USA J Veg Sci 2008 19831ndash40

[23] Belnap J Buumldel B Lange OL Biological soil crusts characteristics and distribution In BelnapJ Lange OL ed Biological soil crusts structure function and management Berlin Springer2003 3ndash30

[24] Buumldel B Darienko T Deutschewitz K Dojani S Friedl T Mohr KI Salisch M Reisser W WeberB Southern African biological soil crusts are ubiquitous and highly diverse in drylands beingrestricted by rainfall frequency Microb Ecol 2009 57229ndash47

[25] De los Rios A Raggio J Peacuterez-Ortega S Vivas M Pintado A Green TGA Ascaso C Sancho LGAnatomical morphological and ecophysiological strategies in Placopsis pycnotheca (lich-enized fungi Ascomycota) allowing rapid colonization of recently deglaciated soils Flora2011 206857ndash64

[26] Dettweiler-Robinson E Bakker JD Grace JB Controls of biological soil crust cover and compo-sition shift with succession in sagebrush shrub-steppe J Arid Envir 2013 9496ndash104

[27] Eldridge DJ Distribution and floristics of terricolous lichens in soil crusts in arid and semi-aridNew South Wales Australia Aust J Bot 1996 44581ndash599

[28] Eldridge DJ Tozer ME Environmental factors relating to the distribution of terricolous bryo-phytes and lichens in semi-arid Eastern Australia Bryologist 1997 10028ndash39

[29] Eldridge DJ Koen TB Cover and floristics of microphytic soil crusts in relation to indices oflandscape health Plant Ecol 1998 137101ndash14

[30] Frey W Herrnstadt I Kuumlrschner H Verbreitung und Soziologie terrestrischer Bryophytenge-sellschaften in der Juumldaumlischen Wuumlste Phytocoenologia 1990 19233ndash65

[31] Haarmeyer DH Luther-Mosebach J Dengler J Schmiedel U Finckh M et al (2010) Biodiver-sity in southern Africa Vol 1 Patterns at local scale ndash the BIOTA observatories Goumlttingen ampWindhoek Klaus Hess Publishers 1ndash801

[32] Hawkes CV Flechtner VR Biological soil crusts in a xeric Florida shrubland Compositionabundance and spatial heterogeneity of crusts with different disturbance histories MicrobEcol 2002 431ndash12

[33] Rogers RW Soil surface lichens on a 1500 kilometre climatic gradient in subtropical easternAustralia Lichenologist 2006 38565ndash75

[34] McCune B Rosentreter R Biotic soil crust lichens of the Columbia Basin Corvallis OregonNorthwest Lichenologists 2007 1ndash105

[35] Williams W Buumldel B Species diversity biomass and long-term patterns of biological soilcrusts with special focus on Cyanobacteria of the Acacia aneura Mulga Lands of QueenslandAustralia Algol Studies 2012 14023ndash50

[36] Castillo-Monroy AP Maestre FT La costra bioloacutegica del suelo Avances recientes en elconocimiento de su estructura y funcioacuten ecoloacutegica Revista Chilena de Historia Natural 2011841ndash21

[37] Castillo-Monroy A Beniacutetez A Reyes-Bueno F Donoso D Cueva A Biocrust structure respondsto soil variables along a tropical scrubland elevation gradient J Arid Environ 2016 12431ndash38

[38] Raggio J Green TGA Crittenden PD Pintado A Vivas M Peacuteres-Ortega S De los Rios A San-cho LG Comparative ecophysiology of three Placopsis species pioneer lichens in recentlyexposed Chilean glacial forelands Symbiosis 2012 5655ndash66

[39] Ruprecht U Brunauer G Tuumlrk R High photobiont diversity in the common European soil crustlichen Psora decipiens Biodivers Conserv 2014 231771ndash85




[40] Timdal E Gypsoplacaceae and Gypsoplaca a new family and genus of squamiform lichensBibl Lichenol 1990 38419ndash27

[41] Amo de Paz G Cubas P Divakar PK Lumbsch HT Crespo A Origin and Diversification of MajorClades in Parmelioid Lichens (Parmeliaceae Ascomycota) during the Paleogene Inferred byBayesian Analysis PLoS ONE 2011 6e28161

[42] Galloway DJ Lichen biogeography In Nash III TH ed Lichen biology Cambridge UK Cam-bridge University Press 2008 317ndash37

[43] Bowker MA Belnap J Davidson DW Phillips SL Evidence for micronutrient limitation of bio-logical soil crusts potential to impact aridlands restoration Ecol Appl 2005 151941ndash51

[44] Eversman S Lichens of alpine meadows on the Beartooth Plateau Montana and WyomingUSA Arct Alp Res 1995 27400ndash6

[45] Concostrina-Zubiri L Martiacutenez I Rabasa SG Escudero A The influence of environmental fac-tors on biological soil crust from a community perspective to a species level approach J VegSci 2014 25503ndash13

[46] Zedda L Grongroft A Schultz M Petersen A Mills A Rambold G Distribution patterns of soillichens across the principal biomes of southern Africa J Arid Environ 2011 75215ndash20

[47] Rogers RW Soil surface lichens in arid and subarid southeastern Australia III The relation-ship between distribution and environment Aust J Bot 1972 20301ndash16

[48] Ponzetti J McCune B Biotic soil crusts of Oregonrsquos shrub steppe community composition inrelation to soil chemistry climate and livestock activity Bryologist 2001 104212ndash25

[49] Maestre FT Huesca MT Zaady E Bautista S Cortina J Infiltration penetration resistance andmicrophytic crust composition in contrasted microsites within a Mediterranean semi-aridsteppe Soil Biol Biochem 2002 34895ndash898

[50] Eldridge DJ Bowker MA Maestre FT Alonso P Mau RL Papadopoulos J Escudero A Interac-tive effects of three ecosystem engineers on infiltration in a semi-arid Mediterranean grass-land Ecosystems 2010 13499ndash510

[51] Eldridge DJ Dynamics of moss- and lichen-dominated soil crusts in patterned Callitris glauco-phylla woodlands in eastern Australia Acta Oecol 1999 20159ndash70

[52] Eldridge DJ Biological soil crusts of Australia In Belnap J Lange OJ Berlin Springer-Verlag2003 119ndash132

[53] George DB Davidson DW Schleip KC Patrell-Kim LJ Microtopography of microbiotic crusts onthe Colorado Plateau and the distribution of component organisms Wes Nor Amer Nat 200060343ndash54

[54] Proctor M The bryophyte paradox tolerance of desiccation evasion of drought PlantEcol2000 15141ndash9

[55] Raabe S Muumlller J Manthey M Duumlrhammer O Teuber U Goumlttlein A Foumlrster B et al Drivers ofbryophyte diversity allow implications for forest management with a focus on climate changeFor Ecol Manage 2010 2601956ndash64

[56] Belnap J Lange OL Biological Soil Crusts Structure Function and Management Springer-Verlag Berlin 2003

[57] Maestre FT Bowker MA Canton Y Castillo-Monroy AP Cortina J Escolar C Escudero A LazaroR Martinez I Ecology and functional roles of biological soil crusts in semi-arid ecosystems ofSpain J Arid Environ 2011 751282ndash91


[59] Maestre FT Escolar C de Guevara ML Quero JL Lazaro R Delgado-Baquerizo M Ochoa VBerdugo M Gozalo B Gallardo A Changes in biocrust cover drive carbon cycle responses toclimate change in drylands Global Change Biology 2013 193835ndash47



References | 93

[60] Delgado-Baquerizo M Maestre FT Eldridge DJ Bowker MA Ochoa V Gozalo B Berdugo M ValJ Singh BK Biocrust-forming mosses mitigate the negative impacts of increasing aridity onecosystem multifunctionality in drylands New Phytol 2016 doi101111nph13688

[61] Ferrenberg S Reed SC Belap J Climate change and physical disturbance cause similar com-munity shifts in biological soil crusts Proc Nat Acad of Sci USA 2015 11212116ndash21

[62] Maestre FT Escolar C Bardgett R Dungait JAD Gozalo B Ochoa V Warming reduces the coverand diversity of biocrust-forming mosses and lichens and increases the physiological stressof soil microbial communities in a semi-arid Pinus halepensis plantation Front Microbiol2015 6865

[63] McCune B Rosentreter R Field key to soil lichens of central and eastern Oregon Unpublishedreport 1995 Oregon State University and USDI BLM

[64] Hauck M Juumlrgens S-R Willenbruch K Huneck S Leuschner C Dissociation and metal-bindingcharacteristics of yellow lichen substances suggest a relationship with site preferences oflichens Ann Bot 2009 10313ndash22

[65] Rivera-Aguilar V Godınez-Alvarez H Moreno-Torres R Rodrıguez-Zaragoza S Soil physico-chemical properties affecting the distribution of biological soil crusts along an environmentaltransect at Zapotitlan drylands Mexico J Arid Environ 2009 731023ndash8

[66] Bowker MA Belnap J Davidson DW Goldstein H Correlates of biological soil crust abundanceacross a continuum of spatial scales support for a hierarchical conceptual model J Appl Ecol2006 43152ndash63

[67] Ochoa-Hueso R Hernandez RR Pueyo JJ Manrique E Spatial distribution and physiology ofbiological soil crusts from semi-arid central Spain are related to soil chemistry and shrubcover Soil Biol and Biochem 2011 431894ndash1901

[68] Downing AJ Selkirk PM Bryophytes on the calcareous soils of Mungo National Park and aridarea of southern central Australia Great Basin Naturalist 1993 5313ndash23

[69] Syers JK Iskandar IK The pedogenetic significance of lichens In Ahmadjian V Hale ME (eds)The Lichens Academic Press New York 1973 225ndash48

[70] Thompson DB Walker LR Landau FH Stark LR The influence of elevation shrub species andbiological soil crust on fertile islands in the Mojave Desert USA J Arid Environ2005 61609ndash29

[71] Ullmann I Buumldel B Biological soil crusts on a landscape scale In Belnap J Lange OJ Biologi-cal soil crusts structure function and management Berlin Springer-Verlag 2003 203ndash13

[72] Nimis PL Poelt J Tretiach M Lichens from the gypsum Park of the northern Apennines(N Italy) Cryptogamie Bryol L1996 1723ndash38

[73] Guerra J Ros R Cano M Casares M Gypsiferous outcrops in SE Spain refuges of rare vulner-able and endangered bryophytes and lichens Cryptogamie Bryol L 1995 16125ndash35

[74] Anderson DC Rushforth SR The cryptogam flora of desert soil crusts in southern Utah USANova Hedwig 1976 28691ndash729

[75] Casares-Porcel M Gutieacuterrez-Carretero L Siacutentesis de la vegetacioacuten liqueacutenica gipsiacutecola termo- ymesomediterraacutenea de la Peniacutensula Ibeacuterica Cryptogamie Bryol L 1993 14361ndash88

[76] Jafari M Tavili A Zargham N Heshmati GA Zare Chahouki M Shirzadian S Sohrabi M Com-paring some properties of crusted and uncrusted soils in Alagol Region of Iran Pakistan J Nut2004 3273ndash7

[77] Laacutezaro R Cantoacuten Y Soleacute-Benet A Bevan J Alexander R Sancho LG Puigdefaacutebregas J Theinfluence of competition between lichen colonization and erosion on the evolution of soil sur-faces in the Tabernas badlands (SE Spain) and its landscape effects Geomorphology 2008102252ndash66




[78] Martiacutenez I Escudero A Maestre F Small-scale patterns of abundance of mosses and lichensforming biological soil crusts in two semi-arid gypsum environments Aust J Bot 200654339ndash48

[79] Meyer SE The ecology of gypsophile endemism in the Eastern Mojave Desert Ecology 1986671303ndash13

[80] Rajvanshi F St Clair LL Webb BL Newberry CC The terricolous lichen flora of the San RafaelSwell Emery County Utah USA In Glenn M Cole M Dirig R Harris R (eds) LichenographiaThomsoniana North American lichenology in honor of John W Thomson Ithaca New YorkUSA Mycotaxon LTD 1998 399ndash406

[81] Zander RH Stark LR Marrs-Smith G Didymodon nevadensis a new species for North Americawith comments on phenology Bryologist 1995 98590ndash5

[82] Bogdanović M Sabovljević M Sabovljević A Grubišić D The influence of gypsiferous sub-strata on bryophyte growth are there obligatory gypsophilous bryophytes Botan Serbica2009 3375ndash82

[83] Palacio S Aitkenhead M Escudero A Montserrat-Martiacute G Maestro M Robertson AHJ Gyp-sophile chemistry unveiled Fourier transform infrared (FTIR) spectroscopy provides new in-sight into plant adaptations to gypsum soils PLoS ONE 2014 9e107285

[84] Concostrina-Zubiri L Pescador DS Martiacutenez I Escudero A Climate and small scale factorsdetermine functional diversity shifts of biological soil crusts in Iberian drylands BiodiversConserv 2014 231757ndash70

[85] Belnap J Welter W Grimm NB Barger NN Ludwig JA Linkages between microbial and hydro-logic processes in arid and semiarid watersheds Ecology 2005 86298ndash307

[86] Li XR Zhang P Su YG Jia RL Carbon fixation by biological soil crusts following revegetation ofsand dunes in arid desert regions of China a four-year field study Catena 2012 97119ndash26

[87] Porada P Weber B Elbert W Poscl U Keidon A Estimating impacts of lichens and bryophyteson global biogeochemical cycles Global Biogeochem Cycles 2013 2871ndash85

[88] Elbert W Weber B Burrows S Steinkamp J Budel B Andreae M Poschl U Controbutions ofcryptogamic covers to the global cycles of carbon and nitrogen Nat Geosci 2012 5459ndash462

[89] Vitousek PM Howart RW Nitrogen limitation on land and in the sea how can it occur Biogeo-chemistry 1991 1387ndash115

[90] Bowker MA Belnap J Davidson DW Microclimate and propagule availability are equally im-portant for rehabilitation of dryland N-fixing lichens Restor Ecol 2010 1830ndash33

[91] Rousk J DeLuca TH Rousk J The cyanobacterial role in the resistance of feather mosses todecomposition ndash toward a new hypothesis PLOS One 2013 4e62058

[92] Delgado-Baquerizo M Gallardo A Covelo F Prado-Comesantildea A Ochoa V Maestre FT Differ-ences in thallus chemistry are related to species-specific effects of biocrust-forming lichenson soil nutrients and microbial communities Func Ecol 2015 291087ndash98

[93] Delgado-Baquerizo M Morillas L Maestre FT Gallardo A Biocrusts control the nitrogen dy-namics and microbial functional diversity of semi-arid soils in response to nutrient additionsPlant Soil 2013 372643ndash54

[94] Evans RD Erlinger JR A break in the nitrogen cycle in Aridlands Evidence from δ15N of SoilsOecologia 1993 94314ndash7

[95] Chaudhary VB Bowker MA OrsquoDell TE Grace JB Redman AE Johnson NC Rillig MC Untanglingthe biological controls on soil stability in semi-arid shrublands Ecol Appl 2008 402309ndash2316

[96] Eldridge DJ Leys JF Exploring some relationships between biological soil crusts soil aggrega-tion and wind erosion J Arid Environ 2003 53457ndash66



References | 95

[97] Rodriacuteguez-Caballero E Aguilar MA Castilla YC Chamizo S Aguilar FJ Swelling og bio-crusts upon wetting induces changes in surface microtopography Soil Biol Biochem 201582107ndash11

[98] Stark LR Brinda JC McLetchie DN Oliver MJ Extended periods of hydration do not elicit de-hardening to desiccation tolerance in regeneration trials of the moss Syntrichia caninervis IntJ Plant Sci 2012 173333ndash343

[99] Kranner I Beckett R Hochman A Nash TH Desiccation tolerance in lichens a review Bryolo-gist 2008 111576ndash93

[100] Tighe M Harling RE Flavel RJ Young IM Ecological succession hydrology and carbon acquisi-tion of biological soil crusts measured at the micro-scale PloS One 2012 7e48565

[101] Chamizo S Cantoacuten Y Lazaro R Sole-Benet A Domingo F Crust composition and disturbancedrive infiltration through biological soil crusts in semiarid systems Ecosystems 2012 15148ndash61

[102] Michel P Payton IJ Lee WG During HJ Impact of disturbance on above-ground water storagecapacity of bryophytes in New Zealand indigenous tussock grassland ecosystems N Zeal JEcol 2013 37114ndash36

[103] Belnap J The potential roles of biological soil crusts in dryland hydrologic cycles Hydrol Pro-cess 2006 203159ndash78

[104] Chamizo S Cantoacuten Y Rodriacuteguez-Caballero E Domingo F Biocrusts positively affect the soilwater balance in semiarid ecosystems Ecohydrology 2016 91208ndash21

[105] Kidron GJ Monger HC Vonshak A Conrad W Contrasting effects of microbiotic crusts onrunoff of desert surfaces Geomorphology 2012 139484ndash94

[106] Darby BJ Neher DA Belnap J Impact of biological soil crusts and desert plants on soil micro-faunal community composition Plant Soil 2010 328421ndash31

[107] Baran R Brodie EL Mayberry-Lewis J Hummel E Da Rocha UN Chakraborty R Bowen BPKaraoz U Cadillo-Quiroz H Garcia-Pichel F Northen TR Exometabolite niche partitioningamong sympatric soil bacteria Nat Comm 2015 6doi101038ncomms9289

[108] Xie CF Lou HX Secondary metabolites in bryophytes An ecological aspect Chem Biodiv2009 6303ndash12

[109] Solhaug KA Gauslaa Y Nybakken L Bilger W UV-induction of sunscreen pigments in lichensNew Phytol 2003 15891ndash100

[110] Buumldel B Karsten U Garcia-Pichel F Ultraviolet-absorbing scytonemin and mycosporine-likeamino acid derivates in exposed rock-inhabiting cyanobacterial lichens Oecologia 1997112165ndash72

[111] Hooper DU Chapin FSI Ewel JJ Hector A Inchausti P Lavorel S Lawton JH Lodge DM LoreauM Naeem S Schmid B Setala H Symstad AJ Vandermeer J Wardle DA Effects of biodiversityon ecosystem functioning a consensus of current knowledge Ecol Monogr 2005 753ndash35

[112] Cardinale BJ Duffy JE Gonzalez A Hooper DU Perrings C Venail P Narwani A Mace GMTilman D Wardle DA Kinzig AP Daily GC Loreau M Grace JB Larigauderie A Srivastava DSNaeem S Biodiversity loss and its impact on humanity Nature 2012 48659ndash67

[113] Cardinale BJ Matulich KL Hooper DU Byrnes JE Duffy E Gamfeldt L Balvanera P OrsquoConnor MIGongalez A The functional role of producer diversity in ecosystems Am J Bot 2011 98572ndash92

[114] Lefcheck JS Byrnes JE Isbell F Gamfeldt L Griffin JN Eisenhauer N Hensel MJS Hector ACardinale BJ Duffy JE Biodiversity enhances ecosystem multifunctionality across trophiclevels and habitats Nat Commun 2015 66936

[115] Bowker MA Maestre FT Escolar C Biological crusts as a model system for examining thebiodiversity-function relationship in soils Soil Biol Biochem 2010 42405ndash17




[116] Bowker MA Maestre FT Mau RL Diversity and patch-size distributions of biological soil crustsregulate dryland ecosystem multifunctionality Ecosystems 2013 16923ndash33

[117] Maestre FT Escudero A Martiacutenez I Guerrero C Rubio R Does spatial pattern matter to ecosys-tem functioning Insights from biological soil crusts Func Ecol 2005 19566ndash73

[118] Mulder CP Uliassi DD Doak DF Physical stress and diversity-productivity relationships therole of positive interactions Proc Natl Acad Sci 2001 986704ndash8

[119] Rixen C Mulder CPH Improved water retention links high species richness with increasedproductivity in arctic tundra moss communities Oecologia 2005 146287ndash99

[120] Hu C Liu Y Song L Zhang D Effect of desert soil algae on the stabilization of fine sandsJ Appl Phycol 2002 14281ndash92

[121] Castillo-Monroy AP Bowker MA Maestre FT Rodriacuteguez-Echeverriacutea S Martinez I Barraza-Zepeda CE Escolar C Relationships between biological soil crust bacterial diversity andabundance and ecosystem functioning Insights from a semi-arid Mediterranean environmentJ Veg Sci 2011 1165ndash74

[122] Pasari JR Levi T Zavaleta ES Tilman D Several scales of biodiversity affect ecosystem multi-functionality Proc Nat Acad Sci 2013 11010219ndash22

[123] Tilman D Isbell F Cowles JM Biodiversity and ecosystem functioning Annu Rev Ecol Evol Syst2014 45471ndash93

[124] Venail P Gross K Oakley TH Narwani A Allan E Flombaum P Isbell F Joshi J Reich PB TilmanD van Ruijven J Cardinale BJ Species richness but not phylogenetic diversity influencescommunity biomass production and temporal stability in a re-examination of 16 grasslandbiodiversity studies Funct Ecol 2015 29615ndash26

[125] Wilsey BJ Polley HW Realistically low species evenness does not alter grassland species-richnessndashproductivity relationship Ecology 2004 852693ndash700

[126] Maestre FT Castillo AP Bowker MA Ochoa-Hueso R Species richness and composition aremore important than spatial pattern and evenness as drivers of ecosystem multifunctionalityJ Ecol 2012 100317ndash30

[127] Castillo-Monroy AP Bowker MA Garciacutea-Palacios P Maestre FT Aspects of soil lichen biodi-versity and aggregation interact to influence subsurface microbial function Plant Soil 2015386303ndash16

[128] Bowker MA Mau RL Maestre FT Escolar C Castillo AP Functional profiles reveal unique eco-logical roles of various biological soil crust organisms Funct Ecol 2011 25787ndash95

[129] Buumldel B Vivas M Lange OL Lichen species dominance and the resulting photosynthetic be-haviors of Sonoran Desert soil crust types (Baja California Mexico) Eco Proc 2012 26

[130] Walker BH Biodiversity and functional redundancy Cons Bio 1992 618ndash23[131] Naeem S Species redundancy and ecosystem reliability Cons Bio 1998 1239ndash45[132] Bowker MA Maestre FT Eldridge DJ Belnap J Castillo-Monroy AP Escolar C Soliveres S Bi-

ological soil crusts (biocrusts) as a model system in community landscape and ecosystemecology Biodivers Conserv 2014 231619ndash37

[133] Gotelli NJ Ulrich W Maestre FT Randomization tests for quantifying species importance toecosystem function Methods Ecol Evol 2011 2634ndash642

[134] Cornelissen JHC Lang SI Soudzilovskaia NA During HJ Comparative cryptogam ecologya review of bryophyte and lichen traits that drive biogeochemistry Ann Bot-London 200799987ndash1001

[135] Castillo-Monroy AP Bowker MA Garciacutea-Palacios P Maestre FT Aspects of lichen biodiver-sity and aggregation interact to influence subsurface microbial function Plant Soil 2014386303ndash16



Andrea Porras-Alfaro Cedric Ndinga Muniania Paris S HammTerry J Torres-Cruz and Cheryl R Kuske6 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 mosthostile 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 lowmoisture availability long periods of dryness low nutrient availability and osmoticstress [3 4] All these characteristics require organisms with specific adaptations tosurvive in this intense and variable environment [5ndash7]

Fungi in these areas include a high number of taxa with hyaline and melanizedhyphae that inhabit rock surfaces biocrusts rhizosphere soils and plant tissues(998835 Fig 61) [3 6 8 9] Taxa with melanized hyphae are known as dark septate fungi(DSF) (998835 Fig 62ab) Dark septate fungi (DSF) are a nonmonophyletic group of fungithat includes a diverse taxonomic assemblage within Ascomycota Orders such asPleosporales Sordariales Capnodiales Xylariales Helotiales and Hypocreales in-clude a number of DSF commonly isolated frommultiple 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 composedof 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 theyare allergens and cause pulmonary and skin diseases in immunocompromised andhealthy individuals [12]

A majority of fungi in arid lands grow as asexual forms (mitosporic) or as sterilemycelia (998835 Fig 62) and are thus difficult to characterize but advances in moleculartechniques and the lowcost of sequencinghave recently allowed large surveys in theseareas showing important potential for the description of novel taxa [8 9 13ndash16] Thischapter focuses on the description of fungal diversity in the different microenviron-ments characteristic of arid lands We will discuss their roles as plant and biocrustsymbionts their function in nutrient cycling their responses to climate and land usechanges and their potential as pathogens in humans

61 Spatial Heterogeneity of Fungal Communities in Arid Lands

The sparse distribution of plants and biocrusts in arid ecosystems creates a seriesof microenvironments in which fungi can be supported by the photosynthetic prod-ucts and organic matter in zones where primary producers are present (ie islands of

DOI 1015159783110419047-006



98 | 6 Fungal Diversity Community Structure and Their Functional Roles in Desert Soils

(a) (b)

(c) (d)

(e)

(f) (g)



61 Spatial Heterogeneity of Fungal Communities in Arid Lands | 99

998819 Fig 61 Diverse microenvironments for fungal communities in desert ecosystems (a) Coleogyneramosissima (blackbrush) in a lichen dominated biocrust (b) grasses and cyanobacteria dominatedbiocrust (c) lichen dominated biocrust in gypsum soils (d) desert varnish (e) patchy distribution ofplant communities (f) lichen dominated biocrust (g) moss dominated biocrust

(a) (b)

(c) (d)

(e) (f)

Fig 62 Common fungi in arid systems (a) Dark septate endophyte colonizing a grass root (b) darkseptate endophyte on root surface (c) ectomycorrhizal fungi in pintildeon pine roots (d) arbuscularmycorrhizal fungus (e) microcolonial fungi inside pits on rock surface scale bar 200 μm [5] (f) ker-atinophilic bait from soil using sterile snake skin




fertility)(998835 Fig 61) [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 moreextreme conditions such as desert varnish and gypsum deposits [5 20 21] Distinctfungal communities in deserts are supported by the high heterogeneity created by thecombination of seasonal climate variable distribution of nutrients and water and amosaic of microenvironments [8 17 22]

611 Biocrusts

Biocrusts also knownasbiological soil crusts ormicrobiotic crusts areprominent fea-tures of desert ecosystems (998835 Fig 61) Biocrusts can cover up to 70 of the ground insome deserts [23] This common aridmicroenvironment supports largemicrobial com-munities that involve a photosynthetic component (algae cyanobacteria or moss)combined with a microbial mat of fungi archaea and other bacteria in which thebacterial biomass is 50ndash500 fold higher than the biomass of surrounding noncrustedsoils [24 25] Biocrusts are classified by their color and texture or by the communitiesof microorganisms found in them [24 26] The darker crusts are dominated by cyano-lichens and mosses (998835 Fig 61a cf-g) and light crusts include cyanobacteria such asMicrocoleus vaginatus (998835 Fig 61b) The structure of microfungal communities in bio-crusts is influenced by the photosynthetic partner andhas shown large spatial hetero-geneity from small areas to large regional scales (998835 Fig 63a) [19 25 27] Fungi showvery patchy distributions even at the millimeter scale with high hyphal density areaswhile other areas lack hyphal components [24] The patchy distribution has been con-firmed using molecular methods in which comparison of biocrusts in close proximityshowhigh variation and little overlap in terms of their fungal community composition(998835 Fig 63a) [16]

Diversity studies on biocrusts reveal abundance of different fungi that rankfrom 40ndash106 species using a combination of cultured based techniques and molec-ular markers (mainly based on Sanger sequencing and DGGE bands) The mostabundant genera within Ascomycota the dominant phylum include taxa such asAlternaria Acremonium Chaetomium Phoma Preussia Stachybotrys and Ulocla-dium [15 18 24 27] Many species within these genera are considered pathogensand 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 (operationaltaxonomic units) using cloning and sequencing of the LSU (large subunit) in biocrustsfrom Utah USA Culture based studies have reported 71 species and 48 genera in thewestern Negev Desert in Israel [27] A recent study using 454 Titanium sequencingof biocrusts showed a slightly larger diversity than previously reported for biocrusts(140ndash228 OTUs for the LSU rRNA region) [16] Next generation sequencing techniquesfacilitate the detection of larger numbers of taxa the comparison of studies and thedetermination of potential culture based bias toward fast growing fungi




(25 OTUs)

E Taxonomic distribution of root-associated fungi

CL1ndashNndash64CL2ndashNndash67CL3ndashNndash60CL4ndashCndash50CL5ndashCndash43CL6ndashCndash77CL7ndashNndash22CL8ndashNndash23CL9ndashNndash20CL10ndashCndash17CL11ndashCndash21

CL12ndashCndash28CL13ndashNndash26CL14ndashNndash27CL15ndashNndash24CL16ndashCndash22CL17ndashCndash21CL18ndashCndash29

0Pleosporales Agaricales Xylariales Sordariales

HalosphaserialesGlomeralesunknown

HypocrealesPezizales

PhallalesOnygenales

20 40 60 80 100

Sand Shale Sand and Shale(18 OTUs) (107 OTUs)

Unclassified Fungi

Unclassified Ascomycota

Rare Ascomycota

Dothideomycetes

Chytriomycota

Basidiomycota

A Sand crusts

108 121

402225

242139

50(37)

(36)109

100

80

60

40

20

Perc

ent o

f sha

red

OTUs

0

D Taxonomic composition of conserved OTUs

(41)

88 79 Sand

210 107

317 243

136

Shale46

1218

81245

41(52) (52)

(66) (56)

(54)

83

B Shale crusts C Between sand and shale

Fig 63 Fungal diversity in the biological soil crust of the Colorado Plateau (andashc) Shared OTUs fordifferent replicate samples showing little overlap among fungal communities and large spatial het-erogeneity (d) Taxonomic composition of shared OTUs showing dominance of Dothideomycetes anda large number of unclassified fungi at this site (e) Dominance of Pleosporales (Dothideomycetes) isalso observed in individual plants (each bar) of Bouteloua gracilis in a semiarid grassland Modifiedfrom [9 16]




Dominance by dark septate fungi ranges from 83ndash98 including abundanttaxa within the Dothideomycetes Sordariomycetes Eurotiomycetes and the Pezi-zomycetes (998835 Fig 63a) [14 15 18 24 27] Dominant taxonomic groups are consistentacross culture based andmolecular studies using different techniques such as DGGESanger sequencing and 454-Titanium sequencing Pleosporales is the dominantfungal 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 ofabundance and diversity in biocrusts Specific areas such as the Chihuahuan desertreport larger numbers of undescribed taxa within this order with little similarity toknown fungi illustrating how incomplete the fungal diversity from these systemsis represented in curated databases [14 18] The large number of undescribed taxaopens new opportunities for the description and characterization of new species Forexample Knapp et al [13] recently described three new genera and five new specieswithin the order Pleosporales from a semiarid region

Other fungal phyla such as Basidiomycota and lower lineages of fungi includingzygomycetes (mainly Mortierellales) and chytridiomycetes are present in biocrusts ina smaller proportion (lt 1minus20) Agaricomycetes are dominant within Basidiomycotarepresented by taxa in the orders Agaricales Cantharellales Corticales Polyporalesand Tremellales including several yeast species [19] Many of these fungal orders in-clude plant pathogens decomposers and important mycorrhizal fungi Lichenizedfungi 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 indetail in Chapter 5 in this book Within the basal lineages of fungiMortierella alpinaseems to be quite common across different types of biocrusts [14 29] and reports ofchytrids using molecular methods shows great potential for the description of newspecies [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 theseconditions 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 availabilitythrough decomposition and transfer of nutrients with nearby grasses [30] Fungalhyphae have been observed in direct contact with clusters of Microcoleus vaginatusthe dominant cyanobacteria in biocrusts [24] Rhizosphere soils and biocrusts sharea 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 (alsoreferred to as fungal loops) [17] that facilitate the interchange of nutrients between thebiocrusts and rhizosphere zones Green et al [30] showed that grasses and biocruststransport N (and C) through fungal networks In this trace element study 15N wastranslocated from biocrusts and grasses at rates of up to 100 cmday [30]




Microbial communities in the biocrusts are highly sensitive to changes in precip-itation regimes with dramatic reductions in biocrust cover with altered precipitationpatterns [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 showgreat potential for conducting simple and low cost manipulations in the field [15 33]Their distribution and spatial heterogeneity facilitate the establishment of studies inmicrobial diversity biogeography and responses to climate change [31]

612 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 (998835 Fig 62) Plant associated fungi include taxa in every fungal phy-lumand representmultiple ecological strategies varying frommutualists commensal-ists pathogens and saprobes The fungal colonizers inside roots stems leaves andseeds includemore specialized community of fungi [9 18 34 35] such asmycorrhizaland nonmycorrhizal species with large colonization rates by endophytic dark septatefungi [9 35 36]

Biocrusts and rhizosphere soils share an important proportion of fungal taxa Thestructure of their fungal communities differs but dominant colonizers are frequentlydetected 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 37ndash41]

Ascomycota fungi are dominant (68ndash88) in rhizosphere soils with lower andvariable proportions of Chytridiomycota Blastomycotina Mucoromycotina andMortierellomycotina (lt 1ndash31) [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 theMojave desert Dothideomyceteswithintheorder Pleosporaleswere abundant [15 40] Similar proportions of dominant taxa atthe class and order levels are consistent in multiple studies including arid grasslandsin New Mexico USA [18 42] and are associated with plants in the family Asteraceaein 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 detectedhigh proportions of Ascomycota (65) with important contributions of Basidiomy-cota (309) and arbuscular mycorrhizal fungi (AMF 54) which are more difficultto detect using conventional PCR based approaches [22]

6121 Mycorrhizal FungiMycorrhizal colonization in arid lands is not as abundant in comparison tomoremesicenvironments but is still an important component of arid land fungal diversity [42




44 45] Mycorrhizal fungi have important roles in the acquisition of nutrients suchas nitrogen and phosphorus They facilitate the attachment of plant roots to the soilaccess to water and other essential nutrients [46 47] The stressful conditions of aridecosystems favor twomain groups of mycorrhizal fungi arbuscularmycorrhizal fungi(AMF) and ectomycorrhizal fungi (EMF)(998835 Fig 62cd)

6122 Arbuscular Mycorrhizal FungiRepresented by species in the phylum Glomeromycota AMF are the most commonplant symbionts found in about 80of vascular plants (998835 Fig 62d) [48 49] AMF playmajor roles in the establishment of plant communities in low-nutrient arid land soilsby facilitating nutrient absorption water uptake and soil stabilization [48 50 51]

Though not as diverse and abundant as in other ecosystems such as temperateforests AMF communities in arid ecosystems portray some level of species richnessand varying levels of colonization on plants For example general estimates of AMFbiomass abundance in plants range from4gmminus2 in deserts in comparison to 44 gmminus2

in temperate grasslands [52] In terms of species diversity AMF taxa defined based onSSU rRNA analyses revealed lower numbers of AMF (27 taxa) for desert environmentsin comparison to temperate broadleaf mixed forests (82 taxa) temperate seminatu-ral grasslands (90 taxa) and subtropical savannas and grasslands (43 taxa) Diversitywas 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] Thedifferences in diversity may be a result of the low number studies available for desertsthat are poorly represented in molecular curated databases and the techniques usedto detect these fungi in the environment For example the use of next generation se-quencing has helped reveal an abundance of AMF fungi in pintildeon pine which wasconsidered primarily colonized by ectomycorrhizal fungi in juniper-pintildeon woodlandin New Mexico [54]

The order GlomeraleswithGlomus group A is the dominant cluster of species [44]Other dominant genera include Claroideoglomus and Scutellospora [44 51 55] Theorders Archaeosporales and Diversisporales are represented by genera such as Ar-chaeospora Diversispora andAcaulospora but colonization levels are low [51] In aridlands AMF colonization rates vary greatly for different sites Some fungi unique todesert ecosystems have relatively high colonization rates varying from 37 to 95 de-pending on their location nutrient availability and environmental conditions [44 5155] while some grasses showed very low colonization rates [35 45 56]

AMF nutrient acquisition and survival is highly dictated by water availability atthese sites The diversity and rates of root colonization by AMF tend to decrease withdryness but hyphae can survive for long periods under dry conditions [55 57] Forsome AMF such as Acacia laevis and Scutellospora calospora infectivity during thedry season also depends on the time of sporulation The hyphae of A laevis have the




capacity to infect plants for 11 weeks in dry soils if they did not receive water beforesporulation started [55]

In addition to season plant diversity and plant ecophysiological adaptations tostressful conditions create abiotic constraints that dictate the composition and growthof AMF communities [58] Plants such as Atriplex halimus a common plant of aridand 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 particularvegetation in areaswith a high level of gypsum (gypsophytes) tends to present uniqueAMF structures in Glomus species that are specific for these sites [20]

6123 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 plantroots to the soil and surrounding plant communities increasing nutrient efficiencyin 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 includeAmanita species such as A rubescens A citrina and A muscaria Hebeloma speciessuch asH sinapizans andH crustuliniforme Laccaria laccata Paxillus involutus andRussula vesca [62] Using 454-Titanium sequencing Dean et al [54] also reported adiverse assemblage of genera in pintildeon-juniper woodlands in New Mexico includingCenococcum Inocybe Tricholoma Rhizopogon andGeopora showing the potential ofnext generation sequencing for the documentation of ectomycorrhizal fungi in thesepoorly studied sites (998835 Fig 62c) [54]

Mycoheterotrophic plants such as desert orchids are nonphotosynthetic plantsthat obtain all their nutrients including carbon from fungi rather than photosyn-thesis [63] They are also dependent on ectomycorrhizal networks for their survivalFungi associated with desert mycoheterotrophs belong to the class Agaricomyceteswith 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 diversegroup of hypogeous ectomycorrhizal fungi also known as turma [60 61] and play amajor role in maintaining certain plant communities in arid lands [61] Desert trufflesinclude 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 CistusTuberaria and Helianthemum [66ndash68] Because of their adaptations to stressful con-ditions in arid ecosystems they are spreadworldwide with a higher number of reportsinwell studied sites in theMiddle East theMediterranean basin the AfricanKalahariand 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 mostcommonly found species are Terfezia leptoderma T boudieri T claveryi and Picoalefebvrei [60 61]




6124 Nonmycorrhizal Fungi (Endophytes)Fungal endophytes have been recovered from leaves stems roots and seeds of manyspecies of arid plants The term endophyte refers to fungi that inhabit plant tissueswithout causing any damage to their hosts [69 70] Root endophytes do not form thecharacteristic structures for nutrient transfer commonly observed inmycorrhizal fungi(ie vesicles arbuscules Hartig net mantle) These plant-fungal associations occurwithdiverse species across all fungal phyla andare found in every studiedplant acrossthe globe [10 69 71] In arid ecosystems endophytes are important for nutrient trans-fer and plant survival because they provide protection against stressful conditionssuch 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 landsis relatively low but the rate of plant colonization can vary greatly among plantspecies [72ndash75] Endophytes are phylogenetically diverse showing important levelsof novel species even at low colonization rates An analysis of 22000 plant segmentsfrom desert trees and shrubs showed colonization rates of 1ndash35 on stems and leaveswith 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 pintildeon-juniperwoodlands [54] and grasses [9 21 35 42 44]

Root colonization rates in grasses are high (60ndash90) with variation among plantspecies and tissue types (aboveground vs belowground communities) [9 21 35 42]Dominant taxa in roots are similar to those observed in rhizosphere and biocrust soilsincluding many Dothideomycetes Eurotiomycetes Sordariomycetes and a propor-tion of Basidiomycota mainly within Agaricomycetes (998835 Fig 63e) Species such asAlternaria Fusarium Aspergillus Chaetomium Preussia Monosporascus Darksideaand Moniliophthora appeared to be generalists isolated from diverse plant speciesand tissues [10 13 35] Other species such as Phoma pomorum show higher levels ofspecificity for specific tissues such as stems and leaves [72] resulting inmore selectiveendophytic communities [13 34]

Unlike mycorrhizal fungi the functions of nonmycorrhizal fungi (endophytesand other rhizosphere associated fungi) are not well defined Their ecological roleslikely vary based on tissue environmental factors and host ranging frommutualiststo plant pathogens to saprobes [69] For example species of the genera OlpidiumMonosporascus andMoniliophthora are well known plant pathogens but are usuallyabundant in association with healthy roots of desert plants mainly from the familyPoaceae (998835 Fig 63e) [9 35 42 66] Coprophilous fungi traditionally found in animaldung have also been recovered from arid land grasses [9] Herrera et al [76] suggesteda potential link between the endophytic and coprophilic life stages in which the fungiare ingested by animals as plant endophytes and they continue as coprophiles onceexcreted

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



62 Roles in Nutrient Cycling and Effects of Climate Change on Fungal Communities | 107

(998835 Fig 62ab) [9 10 35 44] Melanized septate hyphae are normally observed insideroot tissue with the formation of microsclerotia (998835 Fig 62a) and intercellular and in-tracellular colonization (998835 Fig 62b) [9 42 56 77] Colonization is more common inthe root cortex with extraradical mycelium spreading from the intercellular spaces inthe roots into the soil [56]

Functional roles for the majority of DSF are still unclear but fungal inoculationexperiments in several plant species reveal the potential to increase plant thermotol-erance and survival under drought conditions Some species of Curvularia have beenreported to confer thermotolerance to plants [78 79] A Paraphaeosphaeria quadrisep-tata isolate from a Sonoran desert cactus provides protection to model plants suchas Arabidopsis thaliana to lethal temperatures through regulation of heat shock pro-teins [47] This genus is also one of themost common taxa recovered fromgrasses suchas Bouteloua gracilis B eriopoda among others [9 74]

More specialized communities of endophytes in desert ecosystems include fungiin gypsum deposits or very specialized environments like the Caatinga deserts inBrazil 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 (998835 Fig 61) [21 80] Gypsum soils arecharacterizedbyhigh concentrationsof calciumsulfate (CaSO4) lownutrient contentand low porosity Thus gypsophiles and gypsovags the most common type of plantsfound in gypsums have unique mycorrhizal and endophytic communities [81 82]Colonization rates vary widely among different plant tissues and species endemic togypsum soils [21 80 83] The variation of endophytic and mycorrhizal communitiesis likely correlated with the physiological and ecological demands of the plants as aresponse to stressful conditions of this environment Commonly isolated genera fromhealthy plant tissues include Alternaria Sporormiella Phoma Fusarium RhizoctoniaEpicoccum Pleospora and Cladosporium [21 82]

Other specialized endophytic communities have been identified in the Caatingadeserts in Brazil The dominant type of desert vegetation in this area includes cactishrubs and thorny trees as well as arid grasses [84] Species of Penicillium and As-pergillus are commonandunique species for these areas have been described includ-ing A caatingaensis and A pernambucoensis Other unique Neosartorya species in-cludeN indohii N paulistensis N takakii N tatenoi N tsurutae andN udagawae [8485]

62 Roles in Nutrient Cycling and Effects of Climate Changeon Fungal Communities

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




to N and C additions are diverse and complex Two decades ago the biotic componentof the global N cycle was attributed only to bacterial metabolism Todaywe know thatfungi have a fundamental role in N transformations in arid soils Fungi are capableof dissimilatory nitrate reduction with production of NO N2O and N2 [87 88] In aridlands fungi are resilient to N deposition in short and long term N deposition exper-iments where little changes in diversity community structure and fungal biomasshave been observed with respect to bacterial communities [8 9 18 86]

ThemainC source for soil fungi is suppliedbyplants and cyanobacterial crusts [1730] and by the rapid turnover of soil proteins in arid lands [89 90] During periodsof active growth plant photosynthate may be translocated to biocrusts the center ofN-fixation [17] Fungi account for a substantial fraction even the majority of N2O pro-duction in arid land soils since they can operate at low water potentials and N2O isthe principal product of fungal mineralization of amino acids through denitrificationvia 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 ofwater characteristic of arid environments Fungi associated with plant litter consist offilamentous dark septate ascomycetes and yeasts Gallo et al [91] reported dominantcommunities of Sporiobolales Coniochaetales Cystofilobasidiales and Pleosporalesin litter of juniper and pintildeon in aridwoodlands of NewMexico 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 carbonThis higher level and movement of organic matter directly impacts the dispersal andstructure of fungal communities including specialized coprophilous fungi [76 93 94]

63 Extremophiles in Deserts

Extremophilic fungi are those that can survive in conditions that are considered stress-ful or lethal for other organismsAspreviouslymentioned fungi indeserts showadap-tations to high UV radiation and low moisture but in the mosaic of microenviron-ments there are evenmore specialized fungal communities exposed to higher selectivepressures such as very high temperatures (40ndash70degC) and extremely low organic mat-ter We focus on two fairly well studied groups thermophilic fungi andmicrocolonialfungi in rock varnish



63 Extremophiles in Deserts | 109

631 Thermophilic and Thermotolerant Fungi

Thermophilic fungi can grow in a range of temperatures between 40ndash50degC [95]with optimal growth at 45degC Thermotolerant fungi include representatives that cangrow between 40ndash50degC but their optimal growth temperature is at 25degC instead of45degC [96 97] Unlike bacteria Eukaryotes experience irreversible membrane damageabove 65degC [95] In desert ecosystems these fungi can encounter conditions favorablefor growth during the monsoon season in which high temperatures will hold for longperiods of time [96]

Thermophilic fungi reported in deserts include taxa within two major groupsthe Ascomycota and Zygomycota (Mucoromycotina) Common orders of thermophilesin deserts include fungi within Sordariales Eurotiales and Mucorales [96] Mucormiehei 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 fungihave been isolated from different substrates including bulk soil litter animal dungbiocrusts 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 soilswith 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 Egyptdominated by taxa such as Chaetomium thermophilum Malbranchea pulchella varsulfurea Rhizomucor pusillus Myriococcum albomyces Talaromyces thermophilusand Torula thermophila [99]

Powell et al [96] showed that thermophiles vary seasonally in an arid grasslandin 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 indesert soils is relatively limited despite their ubiquitous distribution based on recentreports [96] This is likely due to the bias on isolation temperatures in culture basedstudies and the notion that fungal diversity in deserts is low [7 98]

632 Rock Varnish and Microcolonial Fungi in Deserts

In deserts several organisms including cyanobacteria chlorophytes fungi mossesheterotrophic bacteria and lichens canproduce rock surface communities that are bi-ologically active forming thin and complex layers on the top few centimeters of rocksurfaces [3] Thesemicrocolonies canbe found in associationwith specificmineral de-posits known as rock varnish (998835 Fig 61d998835Fig 62e) Rock varnish are present on rocksurfaces [5] and are coatings mainly made of clays oxides hydroxides manganeseand iron They are found in deserts and semiarid regions all over theworld These darkcoatings are hard and have a unique chemistry they are usually black when they are




rich in iron andmanganese dark brown or pigmented opaline silica when rich in ironoxides and can be red when deficient in manganese [5 6]

The origin of rock varnish is not completely understood it could be the result ofabiotic 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 desertvarnish (998835 Fig 61d 998835 Fig 62e) [5 6]

6321 Characteristics of Microcolonial FungiMicrocolonial fungi (MCF) have the ability to survivewhere other organisms are rarelyfound Theywere first described in the SonoranDesert by Perry andAdams in 1977 us-ing scanning electronmicroscopy andmorphological analysis [6]Microcolonial fungiare globally distributed and have been reported in the Sonoran Mojave Gobi NamibGreat Victoria Gibson Simpson Arabian andNubian 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 approximately100 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 andthey can penetrate sedimentary soft rocks such as limestone sandstone andmarbleand 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 inthe western United States and Australia The microcolonial structures were grown inthe laboratory obtaining slow growing fungal colonies that were mainly composedof a single isolate The fungi on these rocks are metabolically active and have beenreferred to as blackberries and black globular units due to their color and shape [6]Even though very limited morphological diversity has been observed studies usingDNA sequencing have shown high genus and species diversity within several ordersof ascomycetes [7]

6322 Adaptations of Microcolonial FungiMicrocolonial 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 surfacendashvolume ratio decreas-ing water loss and reducing the fungal surface exposed to sun radiation and differentstressors [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 sincethey rely on nutrients and carbon from external sources brought to the rock surfaceby the wind like small particles of organic matter (eg pollen grains) [1 6] Micro-



64 Human Pathogenic Fungi in Desert Ecosystems | 111

colonial fungi do not actively grow during hot periods regardless of the humidity butcan survive for long periods under the severe desert conditions [100] Pigments suchas 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 ofthese fungi produce large amounts of extracellular polymeric substances (EPS) whichmight provide protection from the sun [6 7 103] and can absorb water and hold itagainst the rocks for longer periods [3]

6323 Importance of Microcolonial FungiBlack microcolonial fungi are responsible for biological deterioration of marble andlimestone monuments and statues growing as a dark brown or black crust on theirsurfaces They are considered one of the most damaging microorganisms in terms ofthe deterioration of monumental stones in all cities worldwide not just arid landsFor example a study by Marvasi et al [104] characterized Sarcinomyces petricola asthe yeast responsible for the dark spots found on two valuable statues (ldquoRatto delleSabinerdquo and ldquoCopia del Davidrdquo) located in the Piazza della Signoria in Florence ItalyThe study of these fungi is important in order to decide on proper procedures to restoreand conserve monuments

Microcolonial fungi allow us to study the limits of life on Earth evolution andadaptation to extreme environmental conditions by eukaryotic organisms [105] It issuspected that rock varnish coatings exist on Mars and our understanding of howmicrocolonial fungi have developed several adaptations against harsh environmentalconditions canprovidegoodmodels to study rock coatings that can facilitatedetectionof life on other planets [6] Studies of stress resistance by these fungi have providedpromising results on their ability to survive space and Martian conditions [7 102]Cryptomyces antarticus (a cold desert microcolonial fungus) has even been shown tosurvive simulated Martian conditions and real space exposure [101 105]

64 Human Pathogenic Fungi in Desert Ecosystems

Arid soils are not immune to the ubiquitous distribution of fungal pathogens Indesert ecosystems fungi reproduce mainly through asexual reproduction creatinglarge amounts of propagules or drought resistant spores that can be easily dispersedby wind even at transcontinental distances [3] Changes in climate and extremedroughts followed by dust storms and the increase in the number of infectious lungdiseases have brought attention to the study of pathogenic fungi in desert ecosys-tems [106] Opportunistic infections may occur in immunocompromised individualsdue to a decreased ability to fight infections such as thosewithHIVAIDS or leukemiain organ transplant patients children or the elderly




641 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 SouthAmerica and the southwestern United States [107] Coccidioidomycosis better knownas Valley Fever starts as a lung infection that can evolve into pneumonia and evenbecome systemic and spread to other organs such as the skin brain and bones andparticularly endangers immunocompromised populations [108] Outbreaks often oc-cur among farmers and construction workers after dust storms [109] or earthquakesand during other events when the soil is disturbed [110 111] The CDC reported oneof the overall highest incidences in 2011 with 426 cases per 100000 people with thelargest number of cases among 60ndash79 year olds (69100000) in states where ValleyFever is endemic and has been reported (Arizona California Nevada New Mexicoand Utah) The number of cases from 1998 to 2014 ranged from 2271 to 22641 [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 toMex-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 presenceof 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 andits 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 inthe environment is very difficult due to its sporadic distribution Only 055 (4 outof 720) positive soil samples were obtained in California [115] More sensitive detec-tion is possible using BALBc mice as biosensors with 89 positive detection in soilsfrom the Tuscan area in Arizona which is known for the presence of Coccidioidesposadasii [116] Intraperitoneal inoculation into mice was also successful in isolatingC posadasii from 6 out of 24 (25) soil samples from Brazil [117] This technique hasfacilitated the examination of Coccidioides spp in endemic areas [117]

642 Dematiaceous and Keratinolytic Fungi in Deserts

Fungi in the family Arthrodermataceae as well as other taxa found in desert soils arekeratinolytic known for their ability to degrade keratin and grow on skin hair andnails of animals The ability to break down keratin a stable and resistant cytoskeletalfilament in human and animal cells is considered a virulence factor of those fungiknown as dermatophytes [118] Dermatophytes can cause a common skin infectionin humans known as ringworm or tinea These infections are confined to the dead




Table 61 Percentage of Arthrodermataceae fungi isolated from desert soils

Bahrain Israel Kuwait India Iran Tunisia

Microsporum gypseum 375 44 75 125 2296 274Trichophyton mentagrophytes 25 166Arthroderma curreyi 37T terrestre 35 583Chrysosporium indicum 25 175 1916 1407 11C pannicola 157 10 75Arthroderma cuniculi 37C tropicum 25 20 10 14References [120] [121] [122] [123] [125] [141]

superficial regions of the skin and are highly contagious but in the majority of thecases they can be treated with the application of antifungal creams [119]

The dermatophytic macroconidial species of EpidermophytonMicrosporum andTrichophyton can be found ubiquitously in the environment including deserts Themost common desert soil dermatophyte is Microsporum gypseum isolated from sev-eral countries including Bahrain Israel Kuwait India Egypt and Iran [120ndash125](998835 Tab 61)

In addition to true dermatophytes other saprophytic fungi can also cause oppor-tunistic infections in humans In desert soils keratinophiles can take advantage ofkeratin 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 causingagent of phaeohyphomycotic cysts in immunosuppressed individuals [126] Fusariumsolani and Fusarium oxysporum both reported keratinophiles and common in deserts(998835 Fig 62f) are also considered themost common causative agents of Fusariummyco-sis [127] Paecilomyces Geomyces and Chaetomium keratinophiles and opportunisticpathogens are also common in arid soils [15 18 125]

643 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] Malesbetween 16ndash50 years old with agricultural occupations have the highest incidence ofthis 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 traumaticinjury Diagnosis is often accomplished by a biopsy and examination of the grainsproduced by the fungus culture based methods or DNA sequencing from infected




tissue Madurella mycetomatis is the usual etiological agent but eumycetomas havealso been reported for other common genera including Exophiala jeanselmei Lep-tosphaeria senegalensisMadurella grisea Fusarium Aspergillus Curvularia Acremo-nium and Paecilomyces among others [129ndash132] many of which are common taxa indeserts

Themycetoma 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 numberof eumycetoma cases in the world (70 of cases) with Mexico second with an averageof 70 cases per year [131 132]

644 Mycotoxins

Mycotoxins are a diverse group of toxic and carcinogenic compounds produced byfungi 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 (ie they can grow in low hu-midity or low water content) and are abundant in desert soils The most prominentspecies of fungi producingmycotoxins arePenicilliumAspergillus andFusariumwiththe 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 aswell as serious problems for humanhealth For exampleFusariummoniliforme colonizingmaize is known to cause leukoencephalomalacia inhorses and has cancer promoting activity due to fumonisins [135] Ochratoxin A is thenephrotoxic responsible for human Balkan endemic nephropathy and other urinarytract tumors [136]

Aflatoxin contamination by Aspergillus is common in arid ecosystems such as thesub-Saharan Africa This fungus benefits from high humidity and temperature butdrought conditions increase the risk of aflatoxin contamination [137] Aflatoxin is themost potent naturally occurring carcinogenic substance and is likely responsible forthe highest incidence of hepatocellular cancer in Africa [138] Kenya reported an acuteoutbreak of aflatoxicosis with 317 cases in July 2004 with a fatality rate of 39 causedby 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 highernumbers of individuals at risk sincemaize seems to have higher colonization rates byaflatoxin producing Aspergillus strains [137 140]



References | 115

65 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 (eg genomics transcriptomicsmetagenomics) is opening new opportunitiesto study fungi in arid lands and their response to climate and land use changes [16 2232] Challenges are still present with the low number of fungal genomes available andthe low number of functional categories that are well annotated Metagenomic stud-ies have proved to be of great value evenwith the disproportionate number of bacteria(97ndash99) vs fungal (05ndash15) metagenome reads in arid soils The metabolic poten-tial and diversity of specific taxa that are difficult to detect using regular PCR based orculture 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 aridsites maximize their potential for discovery of new species and generate applicationsin agriculture and the medical field

Acknowledgment AP-A supportwasprovidedbyNational ScienceFoundation (awardnumber 1457002) and the Sevilleta Long Term Ecological Research Site Support forCRK is from the US Department of Energy Biological and Environmental ResearchDivision through a science focus area grant

References

[1] Staley JT Palmer F Adams JB Micro colonial fungi common inhabitants on desert rocksScience 1982 2151093ndash5


[3] Pointing SB Belnap J Microbial colonization and controls in drylands systems Nat Rev Micro-biol 2012 10551ndash62

[4] Huxman T Snyder K Tissue D et al Precipitation pulses and carbon fluxes in semiarid andarid ecosystems Oecologia 2004 141254ndash68

[5] Parchert KJ Spilde MN Porras-Alfaro A Nyberg AM Northup DE Fungal Communities As-sociated with Rock Varnish in Black Canyon New Mexico Casual Inhabitants or EssentialPartners Geomicrobiol J 2012 29752ndash66




[6] Perry RS Gorbushina A Engel MH Kolb VM Krumbein WE Staley JT Accumulation and depo-sition of inorganic and organic compounds by microcolonial fungi Proc Third Eur WorkshopExo-Astrobiol 2004 55ndash8

[7] Sterflinger K Tesei D Zakharova K Fungi in hot and cold deserts with particular reference tomicrocolonial fungi Fungal Ecol 2012 5453ndash62

[8] Mueller RC Belnap J Kuske CR Soil bacterial and fungal community responses to nitrogenaddition across soil depth and microhabitat in an arid shrubland Front Microbiol 2015 6891

[9] Porras-Alfaro A Herrera J Sinsabaugh RL Odenbach KJ Lowrey T Natvig DO Novel root fungalconsortium associated with a dominant desert grass Appl Environ Microbiol 2008 742805ndash13

[10] Jumpponen A Trappe JM Dark septate endophytes a review of facultative biotrophic root-colonizing fungi New Phytol 1998 140295ndash310

[11] Belnap J Lange OL Biological Soil Crusts Structure Function and Management Berlin Hei-delberg Springer 2002

[12] Barberaacuten A Ladau J Leff JW et al Continental-scale distributions of dust-associated bacteriaand fungi P Nat Acad Sci 2015 1125756ndash61

[13] Knapp DG Kovaacutecs GM Zajta E Groenewald JZ Crous PW Dark septate endophytic pleospo-ralean genera from semiarid areas Persoonia 2015 3587ndash100

[14] Bates ST Garcia-Pichel F Nash III TH Fungal components of biological soil crusts insightsfrom culture-dependent and culture-independent studies In Nash TH III Geiser L McCune BTriebel D Tomescu AMF Sanders WB (eds) Biology of Lichens ndash Symbiosis Ecology EnvironmMonitoring Systematics Cyber Applications Verlagsbuchhandlung Stuttgart J Cramer inder Gebruumlder Borntraeger 2010 197ndash210

[15] Steven B Gallegos-Graves LV Yeager C Belnap J Kuske CR Common and distinguishing fea-tures of the bacterial and fungal communities in biological soil crusts and shrub root zonesoils Soil Biol Bioch 2014 69302ndash12

[16] Steven B Hesse C Gallegos-Graves LV Belnap J Kuske CR Fungal Diversity in Biological SoilCrusts of the Colorado Plateau Proc 12th Biennial Conf Science Management Colorado Plateau2014in press

[17] Collins SL Sinsabaugh RL Crenshaw C et al Pulse dynamics and microbial processes inaridland ecosystems J Ecol 2008 96413ndash20


[19] Bates ST Nash III TH Garcia-Pichel F Patterns of diversity for fungal assemblages of biologicalsoil crusts from the southwestern United States Mycologia 2012 104353ndash61

[20] Alguacil MM Roldan A Torres MP Complexity of semiarid gypsophilous shrub communitiesmediates the AMF biodiversity at the plant species level Microb Ecol 2009 57718ndash27

[21] Porras-Alfaro A Raghavan S Garcia M Sinsabaugh RL Natvig DO Lowrey TK Endophyticfungal symbionts associated with gypsophilous plants Botany 2014 92295ndash301

[22] Hudson CM Kirton E Hutchinson MI et al Lignin-modifying processes in the rhizosphere ofarid land grasses Environ Microbiol 2015 174965ndash78

[23] Belnap J Some Like It Hot Some Not Science 2013 3401533ndash4[24] Bates ST Garcia-Pichel F A culture-independent study of free-living fungi in biological soil

crusts of the Colorado Plateau their diversity and relative contribution to microbial biomassEnviron Microbiol 2009 1156ndash67

[25] Steven B Gallegos-Graves LV Belnap J Kuske CR Dryland soil microbial communities displayspatial biogeographic patterns associated with soil depth and soil parent material FEMSMicrobiol Ecol 2013 86101ndash13



References | 117

[26] Pietrasiak N Regus JU Johansen JR Lam D Sachs JL Santiago LS Biological soil crust com-munity types differ in key ecological functions Soil Biol and Biochem 2013 65168ndash71

[27] Grishkan I Kidron GJ Biocrust-inhabiting cultured microfungi along a dune catena in the west-ern Negev Desert Israel Eur J Soil Biol 2013 56107ndash14

[28] States JS Christensen M Fungi associated with biological soil crusts in desert grasslands ofUtah and Wyoming Mycologia 2001 93432ndash9

[29] Bates ST Nash TH Sweat KG Garcia-Pichel F Fungal communities of lichen-dominated biolog-ical soil crusts Diversity relative microbial biomass and their relationship to disturbance andcrust cover J Arid Environ 2010 741192ndash9

[30] Green LE Porras-Alfaro A Sinsabaugh RL Translocation of nitrogen and carbon integratesbiotic crust and grass production in desert grassland J Ecol 2008 961076ndash85

[31] Johnson SL Kuske CR Carney TD Housman DC Gallegos-Graves LV Belnap J Increased tem-perature and altered summer precipitation have differential effects on biological soil crusts ina dryland ecosystem Glob Change Biol 2012 182583ndash93

[32] Steven B Kuske CR Reed SC Belnap J Climate change and physical disturbance manip-ulations result in distinct biological soil crust communities Appl Environ Microb 2015817448ndash59

[33] Bowker MA Maestre FT Eldridge D et al Biological soil crusts (biocrusts) as a model systemin community landscape and ecosystem ecology Biodivers Conserv 2014 231619ndash37

[34] Massimo NC Nandi Devan MM Arendt KR et al Fungal endophytes in aboveground tissues ofdesert plants infrequent in culture but highly diverse and distinctive symbionts Microb Ecol2015 7061ndash76

[35] Herrera J Khidir HH Eudy DM Porras-Alfaro A Natvig DO Sinsabaugh RL Shifting fungalendophyte communities colonize Bouteloua gracilis effect of host tissue and geographicaldistribution Mycologia 2010 1021012ndash26

[36] Mandyam K Fox C Jumpponen A Septate endophyte colonization and host responses ofgrasses and forbs native to a tallgrass prairie Mycorrhiza 2012 22109ndash19

[37] Lipson DA Kuske CR Gallegos-Graves LV Oechel WC Elevated atmospheric CO2 stimulatessoil fungal diversity through increased fine root production in a semiarid shrubland ecosys-tem Glob Chang Biol 2014 202555ndash65

[38] Shamir I Steinberger Y Vertical distribution and activity of soil microbial population in asandy desert ecosystem Microb Ecol 2007 53340ndash7

[39] Bell C McIntyre N Cox S Tissue D Zak J Soil microbial responses to temporal variations ofmoisture and temperature in a Chihuahuan desert grassland Microb Ecol 2008 56153ndash67

[40] Nguyen LM Buttner MP Cruz P Smith SD Robleto EA Effects of elevated atmospheric CO2 onrhizosphere soil microbial communities in a Mojave Desert ecosystem J Arid Environ 201175917ndash25

[41] Lipson DA Wilson RF Oechel WC Effects of elevated atmospheric CO2 on soil microbialbiomass activity and diversity in a chaparral ecosystem Appl Environ Microb 2005 718573ndash80

[42] Khidir HH Eudy DM Porras-Alfaro A Herrera J Natvig DO Sinsabaugh RL A general suite offungal endophytes dominate the roots of two dominant grasses in a semiarid grassland J AridEnviron 2010 7435ndash42

[43] Wehner J Powell JR Muller LAH et al Determinants of root-associated fungal communitieswithin Asteraceae in a semi-arid grassland J Ecol 2014 102425ndash36

[44] Porras-Alfaro A Herrera J Natvig DO Sinsabaugh RL Effect of long-term nitrogen fertilizationon mycorrhizal fungi associated with a dominant grass in a semiarid grassland Plant and Soil2007 29665ndash75




[45] Johnson NC Rowland DL Corkidi L Egerton-Warburton LM Allen EB Nitrogen enrich-ment alters mycorrhizal allocation at five mesic to semiarid grasslands Ecology 2003841895ndash908

[46] Tisdall JM Oades JM Organic matter and water-stable aggregates in soils J Soil Science 198233141ndash63

[47] McLellan CA Turbyville TJ Wijeratne EM et al A rhizosphere fungus enhances Arabidopsisthermotolerance through production of an HSP90 inhibitor Plant Physiol 2007 145174ndash82

[48] Brundrett MC Mycorrhizal associations and other means of nutrition of vascular plants un-derstanding the global diversity of host plants by resolving conflicting information and devel-oping reliable means of diagnosis Plant Soil 2009 32037ndash77

[49] Wu Y Jiang J Shen W He X Arbuscular mycorrhiza fungi as an ecology indicator for evaluatingdesert soil conditions Front Agricul China 2010 424ndash30

[50] Johnson D Leake JR Read DJ Novel in-growth core system enables functional studies of grass-land mycorrhizal mycelial networks New Phytol 2001 152555ndash62

[51] Kruger M Teste FP Laliberte E et al The rise and fall of arbuscular mycorrhizal fungal diver-sity during ecosystem retrogression Mol Ecol 2015 244912ndash30

[52] Treseder KK Cross A Global distributions of arbuscular mycorrhizal fungi Ecosystems 20069305ndash16

[53] Oumlpik M Vanatoa A Vanatoa E et al The online database MaarjAM reveals global and ecosys-temic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota) New Phytol2010 188223ndash41

[54] Dean SL Warnock DD Litvak ME Porras-Alfaro A Sinsabaugh R Root-associated fungal com-munity response to drought-associated changes in vegetation community Mycologia 20151071089ndash104

[55] Jasper DA Abbott LK Robson AD The survival of infective hyphae of vesicular-arbuscularmycorrhizal fungi in dry soil an interaction with sporulation New Phytol 1993 124473ndash9

[56] Barrow JR Atypical morphology of dark septate fungal root endophytes of Bouteloua in aridsouthwestern USA rangelands Mycorrhiza 2003 13239ndash47

[57] Symanczik S Courty PE Boller T Wiemken A Al-Yahyarsquoei MN Impact of water regimes onan experimental community of four desert arbuscular mycorrhizal fungal (AMF) species asaffected by the introduction of a non-native AMF species Mycorrhiza 2015 25639ndash47

[58] Barness G Rodriguez Zaragoza S Shmueli I Steinberger Y Vertical distribution of a soil mi-crobial community as affected by plant ecophysiological adaptation in a desert system Mi-crob Ecol 2009 5736ndash49

[59] Walker DJ Lutts S Saacutenchez-Garciacutea M Correal E Atriplex halimus L Its biology and usesJ Arid Environ 2014 100ndash101111ndash21

[60] Gutierrez A Morte A Honrubia M Morphological characterization of the mycorrhiza formed byHelianthemum almeriense Pau with Terfezia claveryi Chatin and Picoa lefebvrei (Pat) MaireMycorrhiza 2003 13299ndash307

[61] Zitouni-Haouar Fel H Fortas Z Chevalier G Morphological characterization of mycorrhizaeformed between three Terfezia species (desert truffles) and several Cistaceae and Aleppo pineMycorrhiza 2014 24397ndash403

[62] Kozdroj J Piotrowska-Seget Z Krupa P Mycorrhizal fungi and ectomycorrhiza associated bac-teria isolated from an industrial desert soil protect pine seedlings against Cd(II) impact Eco-toxicology 2007 16449ndash56

[63] Leake JR The biology of myco-heterotrophic (lsquosaprophyticrsquo) plants New Phytol 1994127171ndash216

[64] Bruns TD Read DJ In vitro germination of nonphotosynthetic myco-heterotrophic plants stim-ulated by fungi isolated from the adult plants New Phytol 2000 148335ndash42



References | 119

[65] Taylor DL Bruns TD Leake JR Read DJ Mycorrhizal specificity and function in myco-het-erotrophic plants Mycorrhizal Ecol 2003 157375ndash413

[66] Bhatnagar A Bhatnagar M Microbial diversity in desert ecosystems Curr Sci 20058991ndash100

[67] Loizides M Hobart C Konstandinides G Yiangou Y Desert Truffles the mysterious jewels ofantiquity Field Mycol 2012 1317ndash21

[68] Jamali S Banihashemi Z Hosts and distribution of desert truffles in Iran based on morpho-logical and molecular criteria J Agric Sci Technol 2012 141379ndash96

[69] Porras-Alfaro A Bayman P Hidden fungi emergent properties endophytes and microbiomesAnnu Rev Phytopathol 2011 49291ndash315

[70] Wilson D Endophyte the evolution of a term and clarification of its use and definition Oikos1995 73274ndash6

[71] Arnold AE Maynard Z Gilbert GS Coley PD Kursar TA Are tropical fungal endophytes hyperdi-verse Ecol Lett 2000 3267ndash74

[72] Sun Y Wang Q Lu X Okane I Kakishima M Endophytic fungal community in stems and leavesof plants from desert areas in China Mycol Prog 2011 11781ndash90

[73] Arnold AE Maynard Z Gilbert GS Fungal endophytes in dicotyledonous neotropical treespatterns of abundance and diversity Mycol Res 2001 1051502ndash7

[74] Herrera J Poudel R Nebel KA Collins SL Precipitation increases the abundance of somegroups of root-associated fungal endophytes in a semiarid grassland Ecosphere 201121ndash14

[75] Loro M Valero-Jimeacutenez CA Nozawa S Maacuterquez LM Diversity and composition of fungal endo-phytes in semiarid Northwest Venezuela J Arid Environ 2012 8546ndash55

[76] Herrera J Poudel R Khidir H Molecular Characterization of Coprophilous Fungal Communi-ties Reveals Sequences Related to Root-Associated Fungal Endophytes Microb Ecol 201161239ndash44

[77] Wu Y Liu T He X Mycorrhizal and dark septate endophytic fungi under the canopies of desertplants in Mu Us Sandy Land of China Front Agr China 2009 3164ndash70

[78] Rodriguez RJ Henson J Van Volkenburgh E et al Stress tolerance in plants via habitat-adapted symbiosis ISME J 2008 2404ndash16

[79] Redman RS Sheehan KB Stout RG Rodriguez RJ Henson JM Thermotolerance generated byplantfungal symbiosis Science 2002 2981581

[80] Alguacil MM Roldan A Torres MP Assessing the diversity of AM fungi in arid gypsophilousplant communities Environ Microbiol 2009 112649ndash59

[81] Palacio S Escudero A Montserrat-Marti G Maestro M Milla R Albert MJ Plants living ongypsum beyond the specialist model Ann Bot 2007 99333ndash43

[82] Pelaacuteez F Collado J Arenal F et al Endophytic fungi from plants living on gypsum soils as asource of secondary metabolites with antimicrobial activity Mycol Res 1998 102755ndash61

[83] Landwehr M Hildebrandt U Wilde P et al The arbuscular mycorrhizal fungusGlomus geospo-rum in European saline sodic and gypsum soils Mycorrhiza 2002 12199ndash211

[84] Oliveira LG Cavalcanti MAQ Fernandes MJS Lima DMM Diversity of filamentous fungi iso-lated from the soil in the semiarid area Pernambuco Brazil J Arid Environ 2013 9549ndash54

[85] Matsuzawa T Campos Takaki GM Yaguchi T Okada K Gonoi T Horie Y Two new species ofAspergillus section Fumigati isolated from caatinga soil in the State of Pernambuco BrazilMycoscience 2014 5579ndash88

[86] Sinsabaugh RL Belnap J Rudgers J Kuske CR Martinez N Sandquist D Soil microbial re-sponses to nitrogen addition in arid ecosystems Front Microbiol 2015 6819

[87] Crenshaw CL Lauber C Sinsabaugh RL Stavely LK Fungal control of nitrous oxide productionin semiarid grassland Biogeochemistry 2008 8717ndash27




[88] Chen H Mothapo NV Shi W Soil moisture and pH control relative contributions of fungi andbacteria to N2O production Microb Ecol 2015 69180ndash91

[89] Stursova M Crenshaw CL Sinsabaugh RL Microbial responses to long-term N deposition in asemiarid grassland Microb Ecol 2006 5190ndash8

[90] McLain JET Martens DA N2O production by heterotrophic N transformations in a semiaridsoil Appl Soil Ecol 2006 32253ndash63

[91] Gallo ME Porras-Alfaro A Odenbach KJ Sinsabaugh RL Photoacceleration of plant litter de-composition in an arid environment Soil Biology and Biochemistry 2009 411433ndash41

[92] Day TA Zhang ET Ruhland CT Exposure to solar UV-B radiation accelerates mass and ligninloss of Larrea tridentata litter in the Sonoran Desert Plant Ecol 2007 193185ndash94

[93] Clarke LJ Weyrich LS Cooper A Reintroduction of locally extinct vertebrates impacts arid soilfungal communities Mol Ecol 2015 243194ndash205

[94] Masunga GS Andresen O Taylor JE Dhillion SS Elephant dung decomposition and co-prophilous fungi in two habitats of semi-arid Botswana Mycol Res 2006 1101214ndash26

[95] Magan N Fungi in extreme environments In Kubicek CP Druzhinina IS (eds) Environmentaland microbial relationships 2nd edn Springer-Verlag Berlin Heidelberg 2007 350

[96] Powell AJ Parchert KJ Bustamante JM Ricken JB Hutchinson MI Natvig DO Thermophilicfungi in an aridland ecosystem Mycologia 2012 104813ndash25

[97] de Oliveira TB Gomes E Rodrigues A Thermophilic fungi in the new age of fungal taxonomyExtremophiles 2015 1931ndash7

[98] Abdel-Hafez SII Thermophilic and thermotolerant fungi in the desert soils of Saudi ArabiaMycopathologia 1982 8015ndash20

[99] Hemida SK Thermophilic and thermotolerant fungi isolated from cultivated and desert soilsexposed continuously to cement dust particles in Egypt Zentralblatt fuumlr Mikrobiologie 1992147277ndash81

[100] Palmer FE Emery DR Stumbler J Staley JT Survival and growth of microcolonial rock fungi asaffected by temperature and humidity 1987 107155ndash62

[101] Marzban G Tesei D Sterflinger K A review beyond the borders Proteomics of microcolonialblack fungi and black yeasts Nat Sci 2013 5640ndash5

[102] Zakharova K Tesei D Marzban G Dijksterhuis J Wyatt T Sterflinger K Microcolonial fungi onrocks a life in constant drought Mycopathologia 2013 175537ndash47

[103] Gorbushina AA Kotlova ER Sherstneva OA Cellular responses of microcolonial rock fungi tolong-term desiccation and subsequent rehydration Stud Mycol 2008 6191ndash7

[104] Marvasi M Donnarumma F Brandi A et al Black microcolonial fungi as deteriogens of twofamous marble statues in Florence Italy I Biodeterior Biodegrad 2012 6836ndash44

[105] Selbmann L Zucconi L Isola D Onofri S Rock black fungi excellence in the extremes fromthe Antarctic to space Curr Genet 2015 61335ndash45

[106] Reid CE Gamble JL Aeroallergens allergic disease and climate change impacts and adapta-tion Ecohealth 2009 6458ndash70

[107] Galgiani JN Ampel NM Blair JE et al Coccidioidomycosis Clin Infect Dis 2005 411217ndash23[108] Dixon DM Coccidioides immitis as a select agent of bioterrorism J Appl Microbiol 2001

91602ndash5[109] Williams JH Phillips TD Jolly PE Stiles JK Jolly CM Aggarwal D Human aflatoxicosis in de-

veloping countries a review of toxicology exposure potential health consequences andinterventions Am J Cli Nutr 2004 801106ndash22

[110] Schneider E Hajjeh RA Spiegel RA et al A coccidioidomycosis outbreak following theNorthridge Calif earthquake JAMA 1997 277904ndash8

[111] Petersen LR Marshall SL Barton-Dickson C et al Coccidioidomycosis among workers at anarcheological site northeastern Utah Emerg Infect Dis 2004 10637ndash42



References | 121

[112] Centers for Disease C Prevention Increase in reported coccidioidomycosisndashUnited States1998ndash2011 MMWR Morbidity and mortality weekly report 2013 62217

[113] Baptista-Rosas RC Catalaacuten-Dibene J Romero-Olivares AL Hinojosa A Cavazos T RiquelmeM Molecular detection of Coccidioides spp from environmental samples in Baja Californialinking Valley Fever to soil and climate conditions Fungal Ecol 2012 5177ndash90

[114] Fisher FS Bultman MW Johnson SM Pappagianis D Zaborsky E Coccidioides niches andhabitat parameters in the southwestern United States a matter of scale Ann N Y Acad Sci2007 111147ndash72

[115] Greene DR Koenig G Fisher MC Taylor JW Soil isolation and molecular identification of Coc-cidioides immitis Mycologia 2000 92406ndash10

[116] Barker BM Tabor JA Shubitz LF Perrill R Orbach MJ Detection and phylogenetic analysis ofCoccidioides posadasii in Arizona soil samples Fungal Ecol 2012 5163ndash76

[117] de Macecircdo RCL Rosado AS da Mota FF et al Molecular identification of Coccidioides spp insoil samples from Brazil BMC Microbiol 2011 11108ndash16

[118] Scott JA Untereiner WA Determination of keratin degradation by fungi using keratin azureMedical Mycology 2004 42239ndash46

[119] Weitzman I Summerbell RC The dermatophytes Clin Microbiol Rev 1995 8240ndash59[120] Deshmukh SK Mandeel QA Verekar SA Keratinophilic fungi from selected soils of Bahrain

Mycopathol 2008 165143ndash7[121] Feuerman E Alteras I Houmlnig E Lehrer N The isolation of keratinophilic fungi from soils in

Israel A preliminary report Mycopathol 1975 5641ndash6[122] Al-Musallam AA Al-Zarban SS Al-Sanegrave NA Ahmed TM A report on the predominant occur-

rence of a dermatophyte species in cultivated soil from Kuwait Mycopathol 1995 130159ndash61[123] Deshmukh SK Verekar SA Prevalence of keratinophilic fungi in usar soils of Uttar Pradesh

India Microbiol Res 2011 215[124] Bagy MMK Saprophytic and keratinophilic fungi isolated from desert and cultivated soils

continuously exposed to cement dust particles in Egypt ZBL Mikrobiol 1992 147418ndash26[125] Malek E Moosazadeh M Hanafi P et al Isolation of Keratinophilic Fungi and Aerobic Actino-

mycetes From Park Soils in Gorgan North of Iran Jundishapur J Microbiol 2013 61ndash5[126] Boyce RD Deziel PJ Otley CC et al Phaeohyphomycosis due to Alternaria species in trans-

plant recipients Transpl Infect Dis 2010 12242ndash50[127] OrsquoDonnell K Sutton DA Fothergill A et al Molecular phylogenetic diversity multilocus hap-

lotype nomenclature and in vitro antifungal resistance within the Fusarium solani speciescomplex J Clin Microbiol 2008 462477ndash90

[128] Yera H Bougnoux ME Jeanrot C Baixench MT De Pinieux G Dupouy-Camet J Mycetoma ofthe Foot Caused by Fusarium solani Identification of the Etiologic Agent by DNA SequencingJ Clin Microbiol 2003 411805ndash8

[129] Zarei Mahmoudabadi A Zarrin M Mycetomas in Iran a review article Mycopathologia 2008165135ndash41

[130] Loacutepez-Martiacutenez R Meacutendez-Tovar LJ Bonifaz A et al Actualizacioacuten de la epidemiologiacutea delmicetoma en Meacutexico Revisioacuten de 3933 casos Gac Med Mex 2013 149586ndash92

[131] Estrada R Chaacutevez-Loacutepez G Estrada-Chaacutevez G Loacutepez-Martiacutenez R Welsh O Eumycetoma ClinDermatol 2012 30389ndash96

[132] Fahal AH Hassan MA Mycetoma British J Surgery 1992 791138ndash41[133] Bankole S Schollenbeger M Drochner W Mycotoxin contamination in food systems in sub-

Saharan Africa Bydgoszcz Soc Mycotox Res 2006 22163ndash9[134] Fink-Grernmels J Mycotoxins their implications for human and animal health Veterin Quart

1999 21115ndash20




[135] Gelderblom WC Jaskiewicz K Marasas WF et al Fumonisinsndashnovel mycotoxins with can-cer-promoting activity produced by Fusarium moniliforme Appl Environ Microbiol 1988541806ndash11

[136] Pfohl-Leszkowicz A Manderville RA Ochratoxin A An overview on toxicity and carcinogenicityin animals and humans Mol Nutr Food Res 2007 5161ndash99

[137] Hell K Mutegi C Aflatoxin control and prevention strategies in key crops of Sub-SaharanAfrica Afri J Microbiol Res 2011 5459ndash66

[138] Strosnider H Azziz-Baumgartner E Banziger M et al Workgroup report public health strate-gies for reducing aflatoxin exposure in developing countries Environ Health Persp 20061141898ndash903

[139] Probst C Njapau H Cotty PJ Outbreak of an acute aflatoxicosis in Kenya in 2004 identifica-tion of the causal agent Appl Environ Microbiol 2007 732762ndash4

[140] Bandyopadhyay R Kumar M Leslie JF Relative severity of aflatoxin contamination of cerealcrops in West Africa Food Addit Contam 2007 241109ndash14

[141] Anane S Al-Yasiri MYH Normand AC Ranque S Distribution of keratinophilic fungi insoil across Tunisia a descriptive study and review of the literature Mycopathologia 201518061ndash8



TG Allan Green7 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 andfunctioning of the soils All organisms in BSC are poikilohydric meaning that theycan desiccate and are only active when wet Photosynthesis of BSC therefore showsresponse curves to incident light temperature CO2 concentration and thallus watercontent (WC) Photosynthesis of BSC is typically optimal at high light around 15 to20degC 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 WCBSC rarely carry out photosynthesis under optimal conditions Environmental waterstatus is the major limiter and in arid areas BSC are active for around 30 of the totaltime In addition they are active at light intensities and temperatures that are lowerthan the habitat means Further limitations occur from thallus water content effectseither from lowWC when drying or partially hydrated by dew but also because manyBSC organisms show depressed photosynthesis at highWC The latter effect can be sointense that the organisms make little carbon gain from heavy rainfalls As a resultoverall carbon fixation is probably only around 1 of the theoretical maximum Theability of BSC organisms to acclimate to a changing environment has probably beengreatly underestimated and may occur in a few days so that it might even be fastenough to influence the results of laboratory studies

71 Introduction

Biological soil crusts (BSC) are a mixture of autotrophic and heterotrophic organismsthat (i) live within or on top the uppermost millimeters of soil creating a consistentlayer and (ii) aggregate soil particles due to their presenceandactivity [1] BSCare com-posed of awide range of organisms typically includingbacteria fungi cyanobacteriaalgae lichens (lichenized fungi) and bryophytes (mosses and liverworts) of which allexcept bacteria (excluding cyanobacteria) and fungi are photosynthetic Although lo-cal conditions strongly affect the presence of the different organisms successionalstages are recognized for BSC with initial colonization by filamentous cyanobacteriafollowed by smaller green algae and cyanobacteria and finally when the surface hasstabilized 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 allBSC organisms is that they are poikilohydricmeaning that their water status tends toequilibrate with the surrounding environment they are wet and active when the envi-

DOI 1015159783110419047-007



124 | 7 Limits of Photosynthesis in Arid Environments

ronment is wet and dry and dormant under dry conditions When dry BSC organismscan withstand extremes of light and temperature (both high and low) Poikilohydrythrough water supply and support also enforces a size limitation on organisms withthe vast majority being less than a centimeter high [2] This in turn means that theyare confined to a two-dimensional habitat in which they are almost always within theatmospheric boundary layer bringing important changes to the interactions with theenvironment 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 Suchenvironments are hot cool and cold semiarid and arid areas and also polar and alpinezones Such habitats are not productive however their large extent means that theyare estimated to contribute around 1 of global net primary production [3] Becauseof 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 betterunderstanding of the limits to photosynthesis by BSC

72 Photosynthetic Responses to Environmental Factorsa Background

721 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 01 and 115 μmolmminus2 sminus1 The majority of NPmaxfor BSC lie between 2 and 5 μmolmminus2 sminus1 (998835 Tab 71) which are high rates comparedto the more typical 1 to 2 μmolmminus2 sminus1 for rain forest lichens [6]

Table 71 LMA (mass per unit area) CO2 exchange rates quantum efficiency and chlorophyll contentfor seven BSC lichen species

LMA Maximal netphotosynthetic rate

Darkrespiration

Quantumefficiency

Chlorophyll

Species g mminus2 μmol mminus2sminus1 nmol gminus1sminus1 μmol mminus2sminus1 mg mminus2

Collema cristatuma 310 28 903 095 0015 43Fulgensia fulgensb 440 52 1182 125 0026 450Lecanora muralisc 510 65 1275 160 0025 564Cladonia convolutad 630 54 857 180 280Squamarina lentigerae 684 40 585 150 0024 227Collema tenaxf 1190 39 328 180 0015 170Diploschistes diacapsisg 2000 50 25 150 0011 1350

Source of data a [7] b [8] c [9] d [10] e [11] f [12] g [13]



72 Photosynthetic Responses to Environmental Factors a Background | 125

Chlorophyll contents of BSC span a large range and can be comparablewith thoseof average C3 leaves which require 500ndash700mg chlmminus2 to achieve maximal quantumyield of CO2 uptake [5] The chlorophyll contents of BSC lichens span a wide rangefrom a low 427mg chlmminus2 for Collema cristatum to an exceptional 1350mg chlmminus2

for D diacapsis (998835 Tab 71) [5] There are differences between the various BSC typesZhao et al [14] report 207 290 and 381mg chlmminus2 for algal mixed and moss domi-natedBSC fromTengger Desert in China andKidron et al [15]measured 167 to 434mgchlmminus2 for cyanobacterial BSC and 532mg chlmminus2 for moss dominated BSC in theNegev Desert For the Qubqi Desert Mongolia Lan et al [16] found a large increasein chlorophyll content with BSC development from 30mg chlmminus2 in cyanobacterialdominated early crusts to 210mg chlmminus2 for fully developed moss dominated crustsThere appears to be no significant link between BSC chlorophyll content (mg chlmminus2)and NPmax (μmolmminus2 sminus1) (998835 Tab 71)

Although data are limited lichens forming BSC appear to be ldquoheavyrdquo in compari-son to those growing in forests showing a wide range in leaf mass per area (LMAg dry weight mminus2) from 310 gdwmminus2 for Collema cristatum to 2000 gdwmminus2 forDiploschistes diacapsis (998835 Tab 71) This compares to mean values of 86 gdwmminus2

and 97 gdwmminus2 for Lobaria scrobicularia and Lobaria pulmonaria and 73 gdwmminus2

Pseudocyphellaria crocata (Merinero et al 2014) and 59 to 91 gdwmminus2 for Pseudo-cyphellaria dissimilis from inside a New Zealand rain forest [17] Similar magnitudesof 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 adiscrete organism and relatively easy to separate from soil crusts Bryophytes andmosses in particular are known for being intimately bound with the soil crusts andcan contribute to the structural strength of the BSC As well as not being easy toseparate from the crust mosses have substantial portions of the plant below groundwhich are not photosynthetic andwill always be respiringwhen active StudyingGrim-mia laevigata Alpert and Oechel [19] found 855 gdwmminus2 for green parts of the plantand 1615 gdwmminus2 for brown parts (total 247 gdwmminus2) Longton [20] found 241ndash692gdwmminus2 (100 cover) for Bryum argenteum and 1012ndash1108 gdwmminus2 for B antarcticum(= Henediella heimii) with the former growing in sheets and the latter in clumps Incontrast Wu et al [21] report 265 gdwmminus2 for the desert moss Syntrichia caninervisin the Gurbantuumlngguumlt Desert China and Green and Snelgar [22] showed the thalloidliverwortsMonoclea forsteri andMarchantia foliacea New Zealand rain forest to haveonly 33 and 35 gdwmminus2 but still achieve a maximal net photosynthetic rates of 081and 099 μmolmminus2 sminus1 respectively There appears to be no relationship betweenNPmax (area basis) and LMA but there is a significant negative relationship betweenNPmax (dry weight basis) and LMA [23]




722 Response of Net Photosynthesis (NP) to Light (PPFD μmol mminus2 sminus1)

998835Fig 71a shows the typical saturation response of net photosynthesis to light by alichen or bryophyte Marked on the response curve are the so-called cardinal pointslight level or photosynthetic photon flux density (PPFD) required to achieve maximalNP (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 (ie zero NP PPFDcomp)and dark respiration rate (DR) which is NP at zero light The PPFDsat is typicallyaround 700 μmolmminus2 sminus1 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 whichhave leaves with protected photosynthetic cells and are able to build canopies Thehigh PPFDsat of BSC can be interpreted as a protection against the occasional bursts ofhigh light or maintenance of the ability to benefit from such conditions these are notexclusive The light compensation point is positively correlated with high PPFDsat [24]andBSChave relatively high values for PPFDcomp often 60 to 100 μmolmminus2 sminus1 whichare 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 sunriseBSC also have low quantumefficiencies from0015 to 0026 (998835 Fig 71a) which are lessthan those found for shade lichens and higher plants ndash 005 and 006 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 highlight The highest light levels for BSCwhen hydrated and active are found in continen-

0ndash20 ndash60

ndash40CollemaDiploschistesPsora

ndash20

00

20

40

60

80

ndash10

00

10

20

30

40

200 400 600 800PPFD (μmol mndash2 sndash1) Temperature ndash degC (a) (b)

Net p

hoto

synt

hesi

s (μm

ol C

O 2 mndash2

sndash1)

CO2 ex

chan

ge ndash

μm

ol m

ndash2 sndash1

Light saturation

5degC

10degC

15degCQuantum efficiency

Light compensation

Dark respiration rate

1000 1200 0 10 20 30 40 50

Fig 71 (a) Typical response curve of net photosynthesis (μmol CO2 mminus2 sminus1) to incident light (PPFDμmol mminus2 sminus1) of a soil crust at three temperatures (5 10 and 15degC) showing the main cardinalpoints 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 andoptimal thallus water content (modified from [12]) Color coding of symbols black ndash Collema tenaxred ndash Diploschistes diacapsis blue ndash Psora cerebriformis symbol shapes bull ndash net photosynthesis998771 ndash dark respiration 998787 and dashed lines ndash Gross photosynthesis (NP ndash DR)




tal Antarcticawheremean PPFDwhen active can reach around 700 μmolmminus2 sminus1 [25]andmosses have constitutive protection against high light with the xanthophyll cyclecomponents present in similar quantities in both light and shade adapted forms Thisprotectionof thephotosystems is complimentedbyUVabsorbing compounds [26] It isnow 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 bothCO2 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 twodifferent proteins for its activation light harvesting complex stress-related protein andphotosystem II subunit S respectively In the moss Physcomitrella patens howeverboth proteins are present and active [29]

As a general rule no negative effects of high light or UV would be expected forBSC unless levels are applied that have little ecological relevance eg shade adaptedforms being exposed to very high light levels

723 Response of Net Photosynthesis to Temperature

In contrast to the rather constant response of NP to PPFD for BSC there seems to bea wider range of adaptions to temperature Examples of typical responses of net pho-tosynthesis to temperature (measured at saturating light and optimal thallus watercontent) are shown in 998835 Fig 71b with all three species showing a similar form of re-sponse Net photosynthesis has an optimum temperature that is over 30degC for Collemaand lower around 20degC but with a much broader range with little change in NP forthe 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 30degCand at higher temperatures by a fall in photosynthetic capacity (gross photosynthe-sis GP) which reaches a maximum at just over 30degC for all three species A maximalrate of gross photosynthesis at around 30degC seems to be relatively common in lichensandmosses and is even found in Antarctic species [30] indicating that the underlyingphotosynthetic mechanisms show little change with environment Differences in op-timal temperature for NP are also reported for different organisms in the same habitatFor example 20ndash27degC 15degC and 20degC for cyanobacteria lichens and mosses respec-tively in the Mu Us Desert Ningxia northwest China (998835 Tab 72 from [31])

724 Response of Net Photosynthesis to Thallus Water Content (WC)

Thallus water content in BSC is usually expressed as mm rain equivalent (mm equalto liters per m2) and not as is routine for lichens and bryophytes as dry weight(dw = [wet weightminusdry weight] sdot100dry weight) because of the difficulty in sepa-




Table 72 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 Optimaltempera-ture

PPFD tosaturateNP

PPFD com-pensation

OptimalWC for NP

MaximalWC

μmol CO2mminus2 sminus1

(degC) μmol mminus2 sminus1 μmol mminus2 sminus1 mm rainequivalent

mm rainequivalent

Cyanobacterial 267 20ndash27 900 70 038 13Lichen 306 15 870 90 092 25Moss 602 20 1200 50 210 38

ratingBSCorganisms from their substrate At very low thalluswater content there is noCO2 exchange but as WC rises so does NP until a maximum is reached (998835 Fig 72) AtNPmax the organisms are at or close to full turgor (relative water content RWC = 10)and at the so-called optimal water content WCopt [2] Homoiohydric plants do not ex-ceed RWC of 10 but lichens and bryophytes can do this because of variable amountsof external water held in capillary spaces outside the cells As a result maximal RWCin BSC organisms can be much higher than 10 often up to 20 or 30 for lichens andsubstantially higher for bryophytes (see 998835 Tab 72 for a comparison of cyanobacteriamosses and lichens at a desert site) The change in NP at WC above WCopt is strongly

Rainfall ndash mm (02 mm categories) orThallus water content ndash mm rain equivalent

Net p

hoto

synt

hesi

s ( μ

mol

mndash2

sndash1)

Num

ber o

f rai

nfal

l eve

nts

00

5

10

15

1 2 3 4ndash1

0

1

2

3

Number of eventsDiploschistesPsoraDidymodon

Fig 72 Line graph Response of net photosynthetic rate (right hand axis μmol mminus2 sminus1) measuredat saturating PFD and 15degC to thallus water content (mm precipitation equivalent) for two lichensbull ndash Diploschistes diacapsis and 998787 ndash Psora decipiens and one moss 998771 ndash Didymodon rigidulus fromTabernas 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 sizein 02 mm categories Note the ldquoplateaurdquo of the moss (998771)



73 Optimal Versus Real Photosynthetic Rates | 129

species dependent and can vary frommaintenance of NPmax to a strong decline in NPsometimes to negative values The decline in NP at high WC is due to increased CO2diffusion resistances caused by blockage from capillary water and cell wall expan-sion [32] Three examples are shown in 998835 Fig 72 and also for two species in 998835Tab 71Diploschistes diacapsis has a WCopt of 05mm and a maximal WC of 12mm whereasfor the second lichen Psora decipiens the equivalent values are 12mm and 25mmrespectively Both species show a sharp maximum in NP In contrast the moss has aWCopt of 12mm and a maximal WC of 39mm In addition it shows a relatively smalldecline in NP from WCopt to around 36mm This is a reasonably general differencewith bryophytes having higherWCopt andmaximalWC than lichens Both lichens andbryophytes show a wide range in their response curves and these appear to be adap-tive For example the very low WCopt andmaximal WC values for D diacapsis appearto allow the species to benefit from dew fall [23]

725 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 (998835 Fig 71a) Most lichens require around 1000 ppm CO2to saturate NP while mosses and liverworts despite normally having single-cell thickleaves require around 1500 ppm CO2 There is little information available for BSC butstudies on cyanobacterial dominated BSC show a linear response of NP to 1000 ppmCO2 [33] The actual CO2 concentration around andor within BSC remains enigmaticThere is evidence frommany ecosystems fromAntarctic mosses to rain forests that ac-tual CO2 levels close to the soil surface can be higher than global CO2 concentrationsdue to an efflux of CO2 from the soil [34] CO2 concentrations within the soils coveredwith BSC can reach 1200 ppm and are almost always above the ambient atmosphericlevels [33 35] Such concentrations indicate a continual efflux of CO2 from the soiland must include sources in addition to recycling of BSC fixed carbon Possible majorsources are higher plant roots and associated mycorrhizae The latter can receive upto 20 of the carbon fixed by the host plant [36]

73 Optimal Versus Real Photosynthetic Rates

According to the response curves presented in 998835 Fig 71ab 998835 Tab 72 BSC at optimalWC will reach NPmax at a light level ge 500 μmolmminus2 sminus1 and temperatures ge 15degCHigher light levels will have no effect on NP as most BSC seem to be well protectedagainst excess light Higher temperatures will lead to lower NP but not in the under-lying photosynthetic rate until GPmax is not reached at around 30degC From these datait might be expected that the normal habitat of BSC in arid areas is one of high lightand moderate to high temperatures




In reality all BSC photosynthetic organisms are poikilohydric andwill only be ac-tivewhen hydrated It is therefore necessary to distinguish between conditions whentheorganismsare active andwhen they are inactive In the latter case theyare typicallyresistant to extremes of light desiccation and temperature [23] With the exception ofthe rare example where fruticose lichens become active solely following equilibrationwith 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 inBSCActivation by dew starts for bothmosses and lichens during the night and ends inthe morning soon after sunrise as they desiccate The net result is that the organismsare active at lower temperatures and light levels than the overall conditions for thehabitat In particular dry lichens and mosses become very hot reaching over 60degCbecause they are good insulators when dry In contrast rain can activate the BSC atany time of day Both lichens and mosses rapidly activate and can stay so for several

0

(a) (b)

(c) (d)

Num

ber o

f dat

a po

ints

200400600800

1000120014001600

0

Num

ber o

f dat

a po

ints

200

400

600

800

1000

00 200 400 600 800 1000

200400600800

1000MossDidymodon rigidulusActive

Inactive InactiveActive

00 10 20

Temperature30 40 50 60

0 10 20Temperature

30 40 50 60PPFD (100 μmol mndash2 sndash1 bands)

0 500 1000 1500 2000 2500 3000

PPFD (100 μmol mndash2 sndash1 bands)0 500 1000 1500 2000 2500 3000

Num

ber o

f dat

a po

ints

200400600800

1000120014001600

0

Num

ber o

f dat

a po

ints

200

400

600

800

1000

00 200 400 600 800 1000

200400600800

1000LichenPsora decipiens

Fig 73 Distribution of active and inactive times (number of data points in year) in relation to tem-perature (ac 5degC bands) and light (bd 100 μmol mminus2 sminus1 bands) for the moss Didymodon rigidulus(ab) and the lichen Psora decipiens (cd) forming BSC at Tabernas Desert Spain Left hand panelsactivity (left hand black bars) and inactivity (right hand gray bars) right hand panel activity (righthand red bars) and inactivity (left hand black bars) Note active and inactive bars are reversed in leftand right hand panels



74 Limits to Photosynthesis in Arid Areas | 131

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 aso-called gulp in the early morning after dew activation [39] The contrast betweentemperature and light levels when active and when inactive is shown in 998835 Fig 73 Thedata are from continuous monitoring at Tabernas Desert Almeria [38 39] for the year2013 and the lichen P decipiens and the moss D rigidulus Both species behave verysimilarly to PPFDwhen active concentrated below about 500 μmolmminus2 sminus1 althoughwhen inactive levels can reach 2500 μmolmminus2 sminus1 For temperature activity is con-centrated below 20degC although both species can reach 60degC and most activity is ataround 75degC for the moss and 125degC 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 andmosses while in summermonths activity ismainly in the daytime reflecting rain acti-vation [39] The pattern of different suboptimal conditions when active has also beenwell documented by continuous monitoring in Antarctica [25] Schlensog et al [40]showed that mean light levels when active increasingly differ from overall incidentlight as the proportion of the time that the organisms are active declines

74 Limits to Photosynthesis in Arid Areas

741 Length of Active Time

Because of their poikilohydric lifestyle it is no surprise that the greatest limiter ofphotosynthesis by BSC in arid zones is water availability 998835 Fig 74a shows the an-nual run of activity for BSC in the Tabernas Desert Spain (the annual precipitationis 230mm but variable) obtained by continuous chlorophyll fluorescence monitor-ing [39] The meanmonthly time active for three lichens and onemoss over 1 year was207 plusmn 36 with a low of 00 in June and high of 747 in November (998835 Fig 74a)Activity in the dark typically exceeds that in the light especially in the high activitymonths so that BSC were active in the light only 83 of the total time (998835 Fig 74a)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 103 and 114 respectively and applying compensation points of 70 and80 μmolmminus2 sminus1 gives a carbon gain only for 28 and 40 of the year respectivelyCarbon loss through respiration occurs for about twice as long as positive NP albeitmainly at lower temperatures at night A similar pattern is summarized for six lichensby Evans and Lange [41] and is a further indication that lowwater availability severelylimits photosynthetic carbon gain by BSC




Sep

0 0

20

40

60

80

100

2012(a) (b)

2013

0

lt0 lt10 lt20 lt30

lt500 lt1000Light (μmol mndash2 sndash1)

Temperature (degC)

lt1500 lt2000

Month

20

4000051015

Light

dar

k rat

io

Prop

ortio

n of

tim

e act

ive (

)

Cum

ulat

ive ti

me a

ctive

()

60

80

Oct

Nov

Dec

Jan

Feb

Mar Ap

rM

ay Jun Jul

Aug

Sep

Oct

Fig 74 (a) Activity pattern through 1 year for BSC at Tabernas Desert Spain (39 from October 2012to September 2013) Black lines annual run of mean monthly time active in light and dark (roundsymbols) and only in the light (triangular symbols) Red lines right hand upper Y axis scale ratio oflight to dark activity for each month (b) Plots of accumulated activity () for incident light ndash blacklines and symbols (lower X axis PPFD in 100 μmol mminus2 sminus1 categories to 1000 (PPFD μmol mminus2 sminus1

then 500 (PPFD μmol mminus2 sminus1 categories and for temperature ndash red lines and symbols (upper X axisin 5degC categories) Circular symbols ndash moss D rigidulus triangles ndash lichen P decipiens

742 Limits When Active ndash External Limitation Through Light and Temperature

BSC are mostly active at lower than normal habitat temperatures and light (998835 Fig 73)998835Fig 74b shows cumulative activity plotted against temperature and incident PPFD(using only data above 0 μmolmminus2 sminus1) Accepting a PPFD to saturate NP to be around500 μmolmminus2 sminus1 then around 70 of the activity occurs below saturation for themoss D rigidulus and lichen P decipiens Similarly if the optimal temperature for NPlies between 15 and 20degC then again around 70 of activity is below this temper-ature It must be remembered that temperature and light covary significantly but ifPPFD to saturate NP is set at 500 μmolmminus2 sminus1 PPFD to compensate CO2 exchangeat 50 μmolmminus2 sminus1 and optimal temperature for NP at 15degC then in 2013 at TabernasDesert the lichen P decipiens and the moss D rigidulus were active above the optimallight and temperature for photosynthesis for 153 and 112 of active time respec-tively Over the whole year this is equivalent to 18 and 11 respectively The sameresult is found for lichens and mosses with intermittent hydration in Antarctica [40]

743 Limits When Active ndash Internal Limitation Through Thallus Hydration

The response of NP to thallus hydration always shows limitation of NP below optimalWCopt and this situationwill almost alwaysoccurwhen hydration is solely by dew NP




can also be depressed atWC higher thanWCopt (998835 Fig 72) a phenomenon that is morecommon in lichens As a result carbon gain at the high thallus water contents whichonly occur after rainfallmay bemuch lower thanmight be expected This effect can beclearly seen in the annual contribution to carbon gain fromdifferent hydration sourcesfor Cladonia convoluta a lichen showing no depression at highWC and Lecanora mu-ralis with very strong depression (to 2 of maximal NP) at high WC [10] C convolutagains 782 of its annual carbon gain (= 111mgCmminus2) on rainy days while L muralisgains only 42 (= 09mgCmminus2) The converse is true for activation by dew when Lmuralis obtains 400 of annual carbon and C convoluta only 59 (coincidentallyboth equal approximately 85mgCmminus2) A somewhat similar situation can be seen forBSC organisms in Tabernas desert (998835 Fig 72) The lichenD diacapsis shows a very lowWCopt and strong depression at higher WC and appears to be adapted to utilize dewevents with little carbon gain during rain events In contrast the mossD rigidulus hasa very high WCmax (39mm) with little depression up to a WC of 35mm and is able toutilize rain events but probably not dew events Both organisms show similar activitypatterns (998835 Fig 73) but carbon gains are probably very different

744 Catastrophes

On occasions environmental conditions are such that organisms are unable to surviveor suffer extensive damage Lichens are known to suffer so-called snow killwhen snowcover remains longer than normal [42] It has also been suggested that carbon lossesduring small intensity rainfall in deserts can cause moss death [43 44] The conceptis that of Mishler and Oliver [45] who suggested that in brief wetdry cycles such asproduced by a small hydration event like light rainfall the moss will suffer net carbonloss 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 leadto carbon starvation and death Extensive bleaching of moss shoots was found bothin the field and in laboratory simulations Intuitively this seems reasonable but it isless so if the probable magnitude of carbon reserves is considered (unfortunately thisinformation is not given) Although rarely measured the actual carbon reserves inmosses can be about 6 of dry weight for small molecular weight sugars and 15 dryweight for starches [47 48] One typical low rain event leads to a maximal net carbonloss of about 024mgCmminus2 [43] which is around 002 of carbon reserves (at 36 gmminus2

moss dry matter) Carbon starvation therefore seems to be an unlikely explanationfor the moss bleaching andmore probably these events represent a desiccation injurymade possible by laboratory pretreatment [49] see also the next section or becauseof the short duration of the precipitation event the plants become exposed to highlight 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 therecovery magnitudes of around 7 loss of soluble pool in lichens are reported [50]




but even this is not likely to be catastrophic as the starch pool which is larger is notreleased

75 Flexibility ndash an Often Overlooked Factor

There is a major difference between gas exchange research on higher plants and thaton BSC (lichens and mosses generally) Typically higher plants are either studied insitu or when grown under controlled conditions whereas BSC are most often broughtinto 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 oftenan attempt to reduce variability in the following measurements (eg [43]) The pos-sibility that the BSC organisms may actually be changing their physiological perfor-mance during the pretreatment has beenmostly overlooked Stark et al [49] have con-sidered this situation and investigated changes in desiccation tolerance during sucha 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 sorapid that mosses had effectively lost their desiccation tolerance within 8 to 12 daysand performed very differently to immediately after collection It is possible that thisis the cause of themoss bleachingdemonstrated by Coe et al [43 46] see Section 755as themosses were given a 5 day pretreatment in the laboratory beforemeasurementsAcclimation of respiration to temperature in the field has been clearly demonstratedby Lange and Green [51] Mosses in Antarctica were able to re-establish UV protectionwithin 6 days and to do this by growing new shoots [26]

It appears that acclimation during pretreatment under controlled conditions inthe laboratory could well be fast enough to change lichen and moss responses Untilnow most BSC researchers have ignored this possibility but perhaps it needs moreattention in the future

76 Summary

BSC photosynthetic organisms are diverse but to date most research has been onlichen andmoss 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 alsospasmodic it is no surprise that desiccation is the main cause of inactivity with anoverall active time of only 20 or less of the year In summer BSC can be completelydormant 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



References | 135

PPFDdue to clouds shading incoming sunlight As a result BSC aremost often (approx-imately 80 of active time) active at suboptimal light and temperature conditionsPhotosynthesis at maximal rates appear to occur about 1 to 2 of the year Furtherlimitations highly species specific occur at low hydration and high WC due to lim-itations to CO2 diffusion and adding these to previous limitations suggests overallactivity at optimal rates for about 05 to 1 of the year The ability of the BSC organ-isms to adapt and acclimate has been greatly underestimated Although small in sizeBSC organisms are metabolically agile and this is shown by species specific changesin the field and itmight also have an effect on laboratory studieswhere pretreatmentsare used Considerable scope remains for future research on photosynthesis of BSCparticularly in the area of adaptation and acclimation

References

[1] Belnap J Buumldel B Lange OL Biological Soil Crusts Characteristics and Distribution In BelnapJ Lange OL (eds) Biological Soil Crusts Structure Function and Management Berlin Heidel-berg Springer-Verlag GmbH 2001 3ndash30

[2] Proctor MCF Physiological ecology In Goffinet B Shaw AJ (eds) Bryophyte Biology 2nd ednCambridge University Press 2009 237ndash68

[3] Elbert W Weber B Burrows S Steinkamp J Buumldel B Andreae MO Poumlschl U Contribution ofcryptogamic covers to the global cycles of carbon and nitrogen Nature Geosci 2012 5459ndash62

[4] Pointing SB Belnap J Microbial colonization and controls in dryland systems Nature Rev Mi-crobiol 2012 10551ndash62

[5] Lange OL Photosynthesis of soil-crust biota as dependent on environmental factors In BelnapJ Lange OL (eds) Biological Soil Crusts Structure Function and Management Berlin Heidel-berg New York Springer-Verlag 2001 217ndash40

[6] Lange OL Buumldel B Heber U Meyer A Zellner H Green TGAndashTemperate rainforest lichens inNew Zealand High thallus water content can severely limit photosynthetic CO2 exchange Oe-cologia 1993 95303ndash313

[7] Lange OL Photosynthetic performance of a gelatinous lichen under temperate habitat con-ditions long-term monitoring of CO2 exchange of Collema cristatum Biblio Lichen 200075307ndash32

[8] Lange OL Reichenberger H Meyer A High thallus water content and photosynthetic CO2 ex-change of lichens Laboratory experiments with soil crust species from local xerothermicsteppe formations in Franconia Germany In Daniels FJA Schulz M Peine J (eds) FlechtenFollmann Contributions to Lichenology in Honor of Gerhard Follmann Published by the Geob-otanical and Phytotaxonomical Study Group Universitaumlt Koumlln 1995 139ndash53

[9] Lange OL Photosynthetic productivity of the epilithic lichen Lecanora muralis long-term fieldmonitoring of CO2 exchange and its physiological interpretation I Dependence of photosyn-thesis on water content light temperature and CO2 concentration from laboratory measure-ments Flora 2002 197233ndash49

[10] Lange OL Green TGA Photosynthetic performance of a foliose lichen of biological soil crustcommunities long-term monitoring of the CO2 exchange of Cladonia convoluta under temper-ate habitat conditions Biblio Lichenol 2003 86257ndash80




[11] Lange OL Green TGA Photosynthetic performance of the squamulose soil-crust lichen Squa-marina lentigera laboratory measurements and long-term monitoring of CO2 exchange in thefield Biblio Lichenol 2004 88363ndash92

[12] Lange OL Belnap J Reichenberger H Photosynthesis of the cyanobacterial soil-crust lichenCollema tenax from arid lands in southern Utah USA Role of water content on light and tem-perature responses of CO2 exchange Funct Ecol 1998 12195ndash202

[13] Pintado A Sancho LG Green TGA Blanquer JM Laacutezaro R Functional ecology of the biologicalsoil crust in semiarid SE Spain sun and shade populations of Diploschistes diacapsis (Ach)Lumbsch Lichenologist 2005 37425ndash32

[14] Zhao Y Li X Zhang Z Hu Y Chen Y Biological soil crusts influence carbon release responsesfollowing rainfall in a temperate desert northern China Ecol Res 2014 29889ndash96

[15] Kidron GJ Barinova S Vonshak A The effects of heavy winter rains and rare summer rains onbiological soil crusts in the Negev Desert Catena 2012 956ndash11

[16] Lan S Wu L Zhang D Hu C Successional stages of biological soil crusts and their microstruc-ture variability in Shapotou region (China) Envir Earth Sci 2012 6577ndash88

[17] Snelgar WP Green TGA Ecologically-linked variation in morphology acetylene reduction andwater relations in Pseudocyphellaria dissimilis New Phytol 1981 87403ndash11

[18] Green TGA Lange OL Photosynthesis in poikilohydric plants A comparison of lichens andbryophytes In Schulze ED Caldwell MM (eds) Ecophysiology of Photosynthesis Berlin Hei-delberg New York Springer-Verlag 1995 319ndash341

[19] Alpert P Oechel WC Carbon balance limits the microdistribution of Grimmia laevigata a desic-cation-tolerant plant Ecology 1985 66660ndash9

[20] Longton RE Microclimate and biomass in communities of the Bryum association on Ross Is-land continental Antarctica Bryol 1974 77109ndash27

[21] Wu N Zhang YM Downing A Aanderud ZT Tao Y Williams S Rapid adjustment of leaf angleexplains how the desert moss Syntrichia caninervis copes with multiple resource limitationsduring rehydration Funct Plant Biol 2014 41168ndash77

[22] Green TGA Snelgar WP A comparison of photosynthesis in two thalloid liverworts Oecologia1982 54275ndash80

[23] Green TGA Proctor MCF Physiology of photosynthetic organisms within biological soil cruststheir adaptation flexibility and plasticity In Weber B Buumldel B Belnap J (eds) Biological soilcrusts an organizing principle in drylands Heidelberg Berlin Hamburg Springer-VerlagGmbH 2016 347ndash81

[24] Green TGA Buumldel B Meyer A Zellner H Lange OL Temperate rainforest lichens in NewZealand light response of photosynthesis NZ J Bot 1997 35493ndash504

[25] Schroeter B Green TGA Pannewitz S Schlensog M Sancho LG Summer variability winterdormancy lichen activity over 3 years at Botany Bay 77deg S latitude continental AntarcticaPolar Biol 2011 3413ndash22

[26] Green TA Kulle D Pannewitz S Sancho LG Schroeter B UV-A protection in mosses growing incontinental Antarctica Polar Biol 2005 28822ndash7

[27] Proctor MCF Smirnoff N Ecophysiology of photosynthesis in bryophytes major roles for oxy-gen photoreduction and non-photochemical quenching at high irradiance in mosses with unis-tratose leaves Physiol Plant 2011 141130ndash40

[28] Proctor MCF Smirnoff N Photoprotection in bryophytes rate and extent of dark relaxation ofnonphotochemical quenching (NPQ) of chlorophyll fluorescence J Bryol 2015 37171ndash7

[29] Gerotto C Alboresi A Giacometti GM Bassi R Morosinotto T Coexistence of plant and al-gal energy dissipation mechanisms in the moss Physcomitrella patens New Phytol 2012196763ndash73



References | 137

[30] Pannewitz S Green TGA Maysek K Schlensog M Seppelt R Sancho LG Tuumlrk R Schroeter BPhotosynthetic responses of three common mosses from continental Antarctica Antarct Sci2005 17341ndash52

[31] Feng W Zhang Y Wu B Qin S Lai Z Influence of environmental factors on carbon dioxide ex-change in biological soil crusts in desert areas Arid Land Res Man 2014 28186ndash196

[32] Cowan IR Lange OL Green TGA Carbon-dioxide exchange in lichens determination of trans-port and carboxylation characteristics Planta 1992 187282ndash94

[33] Thomas AD Hoon SR Carbon dioxide fluxes from biologically-crusted Kalahari Sands aftersimulated wetting J Arid Envir 2010 74131ndash9

[34] Raven JA Colmer TD Life at the boundary photosynthesis at the soilndashfluid interface A synthe-sis focusing on mosses J Exp Bot 2016 671613ndash23

[35] Thomas AD Hoon SR Dougill AJ Soil respiration at five sites along the Kalahari Transect ef-fects of temperature precipitation pulses and biological soil crust cover Geoderma 2011167284ndash94

[36] Zhu Y Miller RM Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems TrendsPlant Sci 2003 8407ndash9

[37] Lange OL Meyer A Zellner H Heber U Photosynthesis and water relations of lichen soil crustsfield measurements in the coastal fog zone of the Namib Desert Funct Ecol 1994 8253ndash64

[38] Buumldel B Colesie C Green TGA Grube M Suau RL Loewen-Schneider K Maier S Peer T Pin-tado A Raggio J Ruprecht U Improved appreciation of the functioning and importance of bio-logical soil crusts in Europe the Soil Crust International Project (SCIN) Biodiv Conserv 2014231639ndash58

[39] Raggio J Pintado A Vivas M Sancho LG Buumldel B Colesie C Weber B Schroeter B Laacutezaro RGreen TGA Continuous chlorophyll fluorescence gas exchange and microclimate monitoring ina natural soil crust habitat in Tabernas badlands Almeriacutea Spain progressing towards a modelto understand productivity Biodivers Cons 2014 231809ndash1826

[40] Schlensog M Green TGA Schroeter Life form and water source interact to determine activetime and environment in cryptogams an example from the maritime Antarctic Oecologia 201317359ndash72

[41] Evans RD Lange OL Biological soil crusts and ecosystem nitrogen and carbon dynamics InBelnap J Lange OL (eds) Biological Soil Crusts Structure Function and Management BerlinHeidelberg Springer-Verlag GmbH 2001 263ndash79

[42] Benedict JB Lichen mortality due to late-lying snow results of a transplant study Arctic AlpRes 1990 2281ndash9

[43] Coe KK Belnap J Sparks JP Precipitation-driven carbon balance controls survivorship of desertbiocrust mosses Ecology 2012 931626ndash36

[44] Reed SC Coe KK Sparks JP Housman DC Zelikova TJ Belnap J Changes in dryland rainfallresult in rapid moss mortality and altered soil fertility Nat Clim Change 2012 2752ndash5

[45] Mishler BD Oliver MJ Putting Physcomitrella patens on the tree of life the evolution and ecol-ogy of mosses Ann Plant Rev 2009 361ndash15

[46] Coe KK Sparks JP Belnap J Physiological Ecology of Dryland Biocrust Mosses In Hanson DTRice SK (eds) Photosynthesis in Bryophytes and Early Land Plants Netherlands Springer2014 291ndash308

[47] Melick DR Seppelt RD Loss of soluble carbohydrates and changes in freezing point of Antarc-tic bryophytes after leaching and repeated freeze-thaw cycles Antarct Sci 1992 4399ndash404

[48] Sun SQ He G Wu YH Zhou J Yu D Starch and nutrient contents are key for mosses adapting todifferent succession stages along a receding glacier Pol J Ecol 2013 61233ndash9




[49] Stark LR Greenwood JL Brinda JC Oliver MJ Physiological history may mask the inherentinducible desiccation tolerance strategy of the desert moss Crossidium crassinerve Plant Biol2014 16935ndash46

[50] Farrar JF Smith DC Ecological physiology of the lichen Hypogymnia physodes III The impor-tance of the rewetting phase New Phytol 1976 77115ndash25

[51] Lange OL Green TGA Lichens show that fungi can acclimate their respiration to seasonalchanges in temperature Oecologia 2005 14211ndash9



Blaire Steven Theresa A McHugh and Sasha Reed8 The Response of Arid Soil Communities

to Climate Change

81 Overview

Arid and semiarid ecosystems cover approximately 40 of Earthrsquos terrestrial surfaceand are present on each of the planetrsquos continents [1] Drylands are characterizedby their aridity but there is substantial geographic edaphic and climatic variabilityamong these vast ecosystems For example drylands vary greatly in their temperatureregimes encompassing both hot and cold deserts and such variation plays large rolesin structuring microbial communities [2 3] Indeed the wide range of environmentalvariables within and among drylands underscores the substantial variation in dry-land soil microbial communities as well as highlights how future climate could driveadditional community change globally Furthermore arid ecosystems are commonlyheterogeneous 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 andor cyanobacteria living at thesoil 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 [6ndash8] Importantlythe typical soil patches of an arid landscape may be differentially sensitive to climatechange [9] Soil communities are only active when enough moisture is available [10]and drylands show large spatial variability in soil moisture with potentially long dryperiods 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 sizefrequency and intensity of future precipitation pulses as well as influence nonrain-fall sources of soilmoisture and aridland ecosystems are known to be highly sensitiveto 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] Thischaracteristicmayhelp to uncover unifying aspects of dryland soil responses to globalchange

The dryness of an ecosystem can be described by its aridity index (AI) SeveralAIs have been proposed but the most widely used metrics determine the differencebetween average precipitation andpotential evapotranspirationwhere evapotranspi-ration is the sum of evaporation and plant transpiration both of which move waterfrom the ecosystem to the atmosphere [14ndash16] Because evapotranspiration can be af-

DOI 1015159783110419047-008



140 | 8 The Response of Arid Soil Communities to Climate Change

PrecipitationIncidentRadiation

Vegetationalbedo WindTranspiration Temperature

Fig 81 Factors affecting an ecosystemrsquos aridity index The aridity index is calculated from the dif-ference in mean annual precipitation and potential evapotranspiration which results in a loss ofsoil moisture Incident radiation can be blocked by clouds reducing evaporation and transpirationVegetation or changes in albedo (reflected sunlight) can alter the rate of evaporation at a local scaleTranspiration 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 withincreased evaporation

fected by various environmental factors such as temperature and incident radiation(998835 Fig 81) regions that receive the same average precipitationmay have significantlydifferent 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 [19ndash22] Accordingly AI is considered to be a central regulator of the diver-sity structure and productivity of an ecosystem playing an especially influential rolein arid ecosystems Thus the climate parameters that drive alterations in the AI of aregion are likely to play a disproportionate role in shaping the response of arid soilcommunities to a changing climate

In this chapter we consider climate parameters that have been shown to be al-tered through climate changewith a focus on how these parameters are likely to affectdryland soil communities includingmicroorganisms and invertebrates In particularour goal is to highlight dryland soil community structure and function in the contextof climate change and we will focus on community relationships with increased at-mospheric CO2 concentrations (a primary driver of climate change) temperature andsources of soil moisture

82 Biological Responses to Elevated Atmospheric CO2

Carbon dioxide (CO2) and other greenhouse gases (eg nitrous oxide methane) arenaturally present in the atmosphere but are increasing in concentration due to hu-man activities The atmospheric abundance of CO2 was sim400ppm in 2016 approxi-mately 40 higher than in 1750 [23] Beyond being a main driver of climate changeatmospheric CO2 concentration can directly impact the biology of arid lands For ex-



82 Biological Responses to Elevated Atmospheric CO2 | 141

ample increasing atmospheric CO2 concentrations are known to affect both rates ofphotosynthesis andwater use efficiency [24 25] Further deserts commonly house notonly the vascular plants common in most terrestrial ecosystems but also the pho-tosynthetic biocrusts that live in the interspace among vascular plants in drylandsworldwide [26ndash29] Multiple free air CO2 enrichment (FACE) experiments have beenestablished in a variety of biomes to experimentally test the effects of atmosphericCO2 enrichment (eg [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 shrublandecosystem [30] The vegetation communities dominated by the shrub Larrea triden-tata increased in net primary productivity and biomass in response to elevated CO2and showed an increased presence of invasive grass [31 32] Increased photosyntheticcapacity 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 yearrsquos precipitationwith a high enough annual rainfall being necessary to allow for a stimulatory effectof increased CO2 [31 33 34] Over the course of the experiment the treatment alsoaffected the physiology of biocrust communities [33] and soil carbon pools increasedsim12 under elevated CO2 indicating that much of the carbon gains from increasedphotosynthesis by the shrubs andor biocrusts were transferred to belowground com-munities [32]

Despite observed higher carbon accumulation in the shrubs and larger soil carbonpools this did not result in higher biomass of the soil microbial communities underelevated CO2 [35 36] However the microorganisms tightly associated with the shrubroots (ie the rhizosphere community) showed compositional shifts with an increasein Basidiomycota fungi and a decrease in Firmicutes bacteria suggesting root exu-dates or other sources of belowground carbonmay be altered under elevated CO2 [35]In contrast the bacterial and fungal communities in the bulk soil collected beneaththe shrubs (but not associated with roots) showed little compositional change in re-sponse toCO2 enrichment [36] suggesting that anyCO2 induced changes in litter quan-tity or quality did not impact the composition of the underlying soilmicrobial commu-nity Although the changes in the abundance and composition of the soil communitiesunder the canopies of the shrubs were relatively subtle increases in soil respirationammonia loss and decreased inorganic nitrogen concentrations were all associatedwith elevated CO2 [37 38] These observations indicate that even in the absence of alarge restructuring of the soil microbial community elevated CO2 may drive changesin soil function and nutrient cycling

While shrub and lichenproductivitywas stimulated by elevated CO2 at theMojaveFACE site the treatment resulted in a small but consistent decrease in cyanobacterialbiomass [39] Metagenomic sequencing of the community suggested that cyanobac-teria under elevated CO2 conditions were enriched in genes to counteract oxidativestress [39] implying that elevated CO2 may induce a stress response in dryland cyano-bacteria This stress is possibly due to a disconnect between environmental signalsGenerally soil wetting results in a pulse of respiration and a diffusion barrier to CO2




efflux thereby increasing local CO2 concentrations [40] Thus an elevated CO2 signalcould be misinterpreted by cyanobacteria as the presence of soil moisture leadingto mistimed metabolic activity [39] In laboratory manipulations arid soil photosyn-thetic organisms increased their photosynthetic potential by 20ndash30 and storedmorecarbon under elevated CO2 but only during wetting pulses [41 42] As has been seenfor dryland vascular plants observations indicate that the functional changes in soilmicrobial communities due to elevated atmospheric CO2 concentrations are tightlycorrelated with soil moisture and with climate effects on vascular plant processesFinally biological nitrogen fixation rates in the crusted soils were not significantlydifferent between elevated and ambient CO2 conditions but the rates of nitrogen fixa-tion were more spatially variable under enriched CO2 [43] This suggests that patchesof soil respond differentially to elevated CO2 further complicating predictions of abroad 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 ecosystemsa meta-analysis of the effects of elevated CO2 on soil communities found that a largeportion (40) of CO2 enrichment experiments do not induce a change in the structureof the indigenous soil populations [44] The data synthesized here support this ideaalthough the effects of CO2 were notable in vascular plants they were more subtle inthe soil microbial community although fewer published studies with a belowgroundfocus could play a role in this perspective In this respect enriched atmospheric CO2seemed to primarily affect the function of the soils without major shifts in soil mi-crobial community composition However the potential exists for strong interactionswith the availability of water in dryland systems [34 45] Thus the effects of elevatedatmospheric CO2 could becomemore or less in their extent andmagnitude dependingon the response of factors that affect soil moisture In particular predicting the effectsof elevated CO2 enrichment on the status of arid soils will likely require coupled fore-casting of changes in the dominant precipitation patterns

83 Biological Responses to Increased Temperature

Drylands across the globe are exposed to a wide variation in temperature The hottestplace on Earth the Lotus Desert of Iran is a dryland that experiences surface tem-peratures above 70degC [46 47] In contrast the mean annual temperatures of the Mc-Murdo Dry Valleys in Antarctica range from minus15 to minus30degC [48] Thus dryland temper-atures vary more than any other biome Data suggest that soil microbial communitiesin drylands structure themselves strongly along dryland temperature classes such asamong hot and cold deserts [2] Further the low humidity in drylands results in lowercloud cover and atmospheric water vapor which allows heat gained during the dayto be easily lost at night Therefore drylands also tend to experience diurnal temper-



84 Biological Responses to Changes in Precipitation | 143

ature shifts larger than those of other ecosystems For example the average diurnaltemperature change for arid systems ranges from 12 to 20degC compared to 4ndash8degC incoastal 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 haveincreased by sim 02degC per decade for the past 30 years [50] and in this respect themagnitude of the temperature shift due to climate changewill likely be relatively smallcompared to the normal temperature fluctuations experienced by drylands That saideven small changes in temperature have the potential to dramatically affect drylandsystems (eg [51]) and because activity in drylands is constrained to very short time-lines (ie only when soils are wet) seemingly subtle changes to diurnal temperaturescould 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 temperatureranges [52 53] This however does not necessarily mean soil biota will be resistant orresilient to increasing temperatures At a continental scale arid soils experiencing av-erage temperature differences of 13 to 15degC showed a shift in the dominant cyanobacte-rial species an alteration that could be recapitulated with a similar temperature shiftin the laboratory [3] Although these temperature increases are significantly largerthan those expected from climate change [50] smaller temperature shifts associatedwith experiments in Spain (24degC above ambient) the Colorado Plateau (2 to 4degCabove ambient) and South Africa (2 to 4degC above average) induced dramatic changesto moss and lichen diversity and abundance but left the dominant cyanobacterialpopulation relatively unaffected [54ndash56] Taken together these observations suggestthat arid soil communities can be generally resilient to increases in temperature butcertain community members may exhibit widely different thermal tolerances and re-sponses to aspects of warming (eg the timing of warming) In this way increases inmean annual temperature aswell as in seasonal anddiurnal temperature alterationshave the potential to affect state changes in soil communities particularly throughthe relationship between soil moisture and temperature

84 Biological Responses to Changes in Precipitation

With rising temperatures there is an increased capacity of the atmosphere to hold wa-ter resulting inalteredhumidity andprecipitationpatterns [57 58] Onaverage globalprecipitation has increased approximately 2 in the 20th century although this in-crease has not been spatially or temporally uniform [59] A common prediction fromglobal circulationmodels is that precipitation is likely to increase atmid and high lati-tudes while decreasing in the subtropics [60] Annual precipitation changes predictedfor drylands from a multimodel intercomparison ranged from a net decrease of 30to an increase of 25 depending on the geographical region considered [61 62] Spe-




cific projections include not only changes to absolute annual precipitation volumesbut also more variable precipitation patterns with increased occurrence of extremeevents in Australian drylands [63] highly variable heavy rain events in arid and semi-arid northern China (eg [64]) andmore intense irregular events delivering less pre-cipitation in southwestern North America [65] In general more extreme precipitationregimes 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 theinfluence of topography and other landscape features [60] Local precipitation is af-fected by features such as coastlines lakes and mountains making predictions fortopographically complex regions difficult [67 68] Consequently precipitation predic-tions are often incomplete or highly uncertain [59 69] Precipitation occurs as distinctepisodic events and so it is also temporally variable Precipitation models producepredictions in seasonal or monthly time steps whereas ecosystem components areoften responding to precipitation pulses at smaller temporal scales with microbialactivity and respiration of invertebrates and shallow rooted plants rapidly stimulatedby changes in soil water potential [70] Moreover phenomena such as El Nintildeo andthe Pacific Decadal Oscillation affect regional precipitation in complex and often un-predictable ways [71] In arid ecosystems biological activity is often constrained totime periods directly following precipitation events [72ndash75] Consequently the timingduration and event size may have more significance for soil biota than does averagerainfall amount [76 77]

Alterations in precipitation patterns including both size and form of deliverycan have dramatic effects on sensitive water limited dryland ecosystems [75] Thisalteration 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 andsubsequent drying As an example a rainfall experiment on the Colorado PlateauUSA showed that increased frequency of small (12mm) rainfall events resulted inpronounced mortality of the widespread moss Syntrichia caninervis dramatically re-ducingmoss cover after only one season of treatment (see Section 842 below formoredetails) These results reveal how seemingly subtle modifications to precipitation pat-terns can affect ecosystem structure and function on unexpectedly short timescalesMoreover the soilmossmortality was the result of increased precipitation underscor-ing the importance of precipitation event size and timing over absolute amounts ofmoisture [51] As another example of a dramatic response a modest increase in win-ter precipitationwas associatedwith a threefold increase in shrub cover severe reduc-tions in reptile abundance and the near local extinction of a keystone rodent in theChihuahuan Desert in southwest USA [78]




841 Natural Precipitation Gradients

A wealth of research has focused on the response of plant communities to changesin mean annual precipitation [79ndash81] Because this is a difficult parameter to exper-imentally manipulate particularly at large scales rainfall gradient approaches areoften used to describe the effects of different precipitation regimes on ecosystem struc-ture and function To a large extent patterns in vegetation composition and functionacross precipitation gradients suggest that decreased water availability is correlatedwith a decrease in net primary productivity and biological diversity [60 82] Howeverpatterns for belowground communities have not been as easy to disentangle Partlythis is due to the complexity of soil systems and the difficulty in linking changes inregional parameters to soil community metrics that vary at small spatial scales Forexample the additional water availability from decreased evaporation in refuge sitesbeneath shrubs or rocks is generally a larger predictor for arid soil microbial commu-nity structure than is mean annual rainfall [83] Soil microorganisms beneath shrubsare more abundant and these communities are compositionally distinct from thosein the soil between plant canopies [84 85] Shrubs in arid lands are often referred toas ldquoislands of fertilityrdquo as the canopy shades the soil reducing evaporation and pro-viding carbon and nutrients through the root exudates and litter production [86ndash89]Even in drylands that are sparse in vegetation hypolithic (under rock) soil communi-ties aremore 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 ofthe Colorado Plateau of Utah were strongly structured based on the parent materialof 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 factorin structuring microbial communities as average rainfall in sites in South Africa [92]Thus the patchy heterogeneous distribution of soil resources and habitats as well assoil characteristics largely influence indigenous soil communities

Microbial biomass is the most widely examined soil biotic response to changesin 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 of30 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 still25ndash40 lower than at a site that naturally received a similar amount of precipitationas the water addition plots suggesting the involvement of other environmental pa-rameters and site characteristics in controlling soil microbial abundance Similarlybacterial biomass significantly declined with decreasing precipitation in the TibetanPlateau [95] In fact a meta-analysis of microbial biomass across approximately 400sites consistently foundmicrobial biomasswas lowest in themost arid soils [96] How-ever exceptions to this pattern have been observed In the Negev Desert microbial




biomass under shrubs as assessed by phospholipid fatty acid analysis was similarbetween 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 sitesand potentially edaphic controls in arid soils Overall the general trends supportthe idea that increased ariditywill plausibly lead to decreased soil microbial biomassthough 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 Severalstudies have documented similar diversity of the bacterial and archaeal communitiesin the wettest and driest sites along precipitation gradients [87 98 99] It is importantto note that diversity represents species richness and not the composition in terms ofrelative abundance The composition of microbial communities is generally differentbetween wet and dry sites or in soils with different historical legacies of precipita-tion [100ndash102] Though many studies of dryland soil microbial community responseto variation in soil moisture were conducted with relatively coarse DNA fingerprint-ing techniques (eg terminal restriction fragment length polymorphism) there is agrowing body of research utilizing high throughput sequencing which allows for acloser examination of microbial taxa (eg [103ndash105]) At a more global scale desertsoil communities showed a very high level of stochastic assembly generally being in-distinguishable from randomwith the only large predictor of desert soil communitiesbeing the high relative abundance of cyanobacteria [106] Presumably the high abun-dance of cyanobacteria is driven by low vegetation cover which allows cyanobacteriato act as key primary producers [107 108] In contrast to bacteria cultivable fungiwere 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 fungalcommunities showed a differential response to monsoon precipitation in a semiaridgrassland in northern Arizona [103] Studies such as these suggest the potential fordifferent functional groups to be differentially impacted by changes in soil moistureand highlight the need to expand our studies to explicitly consider specific soil pop-ulations and functional groups in an effort to create comprehensive species catalogsand predictive models In addition to assessment of how altered precipitation affectssoil community composition and structure the exploration of how these changes insoil microbial community composition affect soil ecosystem functioning represents acritical area of research

While the data are focused on handful of well studied sites several studies havefound potential changes in soil function associated with reduced precipitation Forexample multiple studies have documented soil carbon and nitrogen decreases withreductions in precipitation [111ndash113] However along a precipitation gradient amongsemiarid and arid grasslands in Oklahoma USA soil patches in the vicinity of thegrasses had similar carbon andnitrogen levels along the gradient Itwas hypothesizedthis 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




dominant determinants of soil functions and fertility in drylands In fact decreasedprecipitation has also been associated with increased patchiness in the distributionof carbon nitrogen and other nutrients across dryland landscapes [115] Thus whileclimate factors such as mean annual precipitation will be altered at regional scalesunderstanding the response of arid soil microbial communities will require forecast-ing those effects at local habitat specific scales

842 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 in50 more events (ie small frequent events) tested altered timing of precipitationon dryland soil communities [117] Increases in the frequency of precipitation reducedcyanobacterial abundance photosynthetic efficiency and nitrogenase activity [117]These data support the framework suggesting that beyond simply considering theabsolute amount of precipitation predicting the performance of dryland communitieswill require considerations of the timing periodicity and duration of soil moisture

A fieldmanipulation experiment on the ColoradoPlateau increased the frequencyof small (12mm) summermonsoon 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 lt 2 in a single year [77] and no recovery has occurred in overa decade [51 55] In the second year of the same experiment cyanobacterial relativeabundance was also reduced by 75ndash95 [119] However after a decade of consistentwetting treatment the cyanobacterial relative abundance had begun to recover In-terestingly the recovering community does not resemble the well-developed crustsin the control plots [55] Taken together these studies support the idea that alteringthe frequency of rainfall events even when the net effect is to increase the amount ofprecipitation 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 fewstudies consider how altered precipitation regimes will impact soil invertebrate com-munities and associated trophic interactions Some soil faunas including nematodesand collembola are able capable of anhydrobiosis a strategy which allows them tosurvive in a dehydrated state [122] In response to simulated rainfall treatments in aChihuahua Desert shrubland experiment a rapid transition from the anhydrobioticcondition to the active form was observed and nematode grazing on bacteria andfungi 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




were also documented [123] A subsequent study showed that soil water amendments(6mm and 25mm monthly events) had no significant effects on nematode densitythoughmoisture induced activitywas greatest in soils experiencing the largermonthlyirrigation [125] A meta-analysis on the impacts of invertebrate grazers and predatorson plant productivity and microbial biomass found that an increase in the biomassof soil fauna led to a 35 increase in aboveground productivity across a variety ofecosystems and an 8 decrease in microbial biomass [126] As interactions amongsoil communities and abiotic factors such as moisture and temperature have the ca-pacity to influence nutrient flow and the functioning of ecosystems future researchaddressing 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 ldquopulse reserverdquo conceptual model first proposedby Noy-Meir [11] has been described as ldquoone of the most-cited paradigms in aridlandecologyrdquo [74] Although the heuristic perspective was developed for vegetation themodel 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 apulse of growth that generates reserves that carry the organism until the next event(assuming resourceswere gained) The response of soil communities to a precipitationpulse is hierarchically organized by the threshold response of different organisms towater 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 2mm precipitation event mayinduce the activity of respiratory soil microorganisms whereas net carbon fixationby plants or biological soil crusts generally requires more sustained andor deeperwetting [75 128] At the highest levels a pulse of 25mmmay be required for the germi-nation of plant seeds [129] There is also a temporal aspect to this response Microbesrespond to water pulses in the scale of minutes to hours whereas vascular plants takehours to days [130] In this respect from the microbial perspective there are criticalmeasures to any precipitation event and there could be a strong temporal decouplingbetween times of vascular plant vs biological soil crust vs soil microbial activity Foreach group precipitation must be in a sufficient amount to initiate a biological re-sponse andmust 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 schematicdiagram of the pulse reserve paradigm is presented in 998835 Fig 82 With this in mindit 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 theparadigm itself could vary across biotic and abiotic gradients

Experimental evidence for this model has been observed in desert mosses Themoss Syntrichia caninervis is common and widespread in many drylands [131] Un-der laboratory conditions the carbon balance of the moss was assayed in response tosimulated precipitation events Rainfall event size was the largest predictor of the car-



85 Interactions Between Temperature and Soil Moisture | 149

Soil

moi

stur

eTime rarr

Precipitationevent

Precipitationevent

Soil

moi

stur

e

Time rarr(a) (b)

Respiration gtphotosynthesis


Net carbon uptake

Carbon deficit

Carbon deficit

Photosynthesis gtrespiration


Net carbon uptake

Fig 82 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 celldamage 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 ofsufficient amount and duration net photosynthesis occurs (ie photosynthesis rates are larger thanthose of respiration and the organisms achieve net carbon uptake a) If the precipitation event isnot sufficient to initiate net photosynthesis net carbon deficit occurs (b)

bon balance of the moss with negative carbon balance developing under the smallestprecipitation events [132] Negative carbon balances in biocrusted soils were also ob-served with small wet up events as seen by an hourly autochamber assessment ofnet CO2 exchange for 1 year and 7 months on the Colorado Plateau [133] The obser-vation of ldquopuffsrdquo of CO2 loss co-occurring with natural small precipitation events isconsistent with the mechanism of moss death described in Reed et al [77] in whichmosses 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 dryperiods [132] Presumably a similar mechanism could also account for the decline ofcyanobacteria in field manipulations [55] although this lacks experimental verifica-tion

85 Interactions Between Temperature and Soil Moisture

Temperature is a strong driver of evaporation from soils A 1degC increase in tempera-ture can be roughly equivalent to a 3ndash5 reduction in precipitation due to increasedevaporation [134] Additionally soil moisture may also be significantly altered if ele-




vated temperatures shift the composition of winter precipitation from snow to rain oralter the timing of winter snow melt [75 135] Thus increasing temperatures have thepotential to increase the AI of soils by driving increased evaporation and altering theform 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 byalteringwater availability This suggests that the interaction between temperature andsoilmoisturewill likely bekey tounderstanding the response of arid soil ecosystems toclimate warming To explore the interaction between temperature and precipitationmultifactorial experiments performed on the ColoradoPlateau investigated the effectsof warming (2ndash4degC surface warming) altered precipitation (additional 12mm 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 communitiesSoils under the combinatorial treatment experienced a reduction in moss and lichencover of gt80 and a decrease in cyanobacterial relative abundance of gt90 [51 55]Clearly the interaction betweenwarming and altered precipitation drove the soil com-munities to a state that would not have been predicted from warming alone Thesesmall 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 apulse reserve model (998835 Fig 82 [128]) and join with field data to suggest that small wa-ter pulses insufficient to induce net carbon fixation can ultimately lead to the collapseof some arid soil communities [55] Due to the drying effects of warming and to physio-logical interactions between temperature and activity duringwet phases these effectsare likely to be amplified in a warmer climate where soil evaporation is heightened

86 Conclusion

Taken together the studies synthesized here support the idea that the biology of aridsoils is primarily driven by water availability and that climate factors associated withcontrolling 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 CO2rsquos 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 alonga precipitation gradient there is a generalized reduction in microbial biomass andcommunity composition shifts towarddesiccationadaptedorganismswith 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 effectdryland soil mosses and bacteria respond to reduced moisture in a similar fashion to



References | 151

plants and macrofauna with the exception of microbial biodiversity arid soils mayact as a cradle supporting diverse microbial seed banks [100] The strong interactionbetween warmer temperatures and increased evaporation from the landscape indi-cates that any precipitation gains from climate change and associated alterations tothe hydrological cycle could be offset by increases in evapotranspiration

Precipitation in drylands occurs in distinct pulses that are often short with longdry 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 muchfiner temporal scales than mean annual precipitation as the frequency and size ofpulses 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 gapsin specific organismal responses to precipitation pulses severely limits our ability topredict 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 nextdecades should be sufficient to significantly impact soil biology and associated bio-geochemical cycling [55 77] In general desert lichens andmosses appear to be moresensitive to these changes than other soil biota such as cyanobacteria [77] In this re-gard those sensitive communitymembersmaybe important species tomonitor undera changing climate Maintenance of dryland soil function will require a collaborativeeffort among climate scientists biologists and landmanagers aswell as an improvedunderstanding of how different biotic and abiotic factors interact to regulate function

Acknowledgment The authors are grateful to Anthony Darrouzet-Nardi and RebeccaMueller for excellent suggestions on a previous version of the manuscript that im-proved the chapter The synthesis provided here was supported by the USDA NationalInstitute 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 SurveyEcosystemsMission Area TAMwas supported by a National Science Foundation Post-doctoral Research Fellowship in Biology under Grant No 1402451 Any use of tradefirm or product names is for descriptive purposes only and does not imply endorse-ment by the US government

References

[1] Thomas DSG Arid Environments Their Nature and Extent In Thomas DSG (ed) Arid ZoneGeomorphology Chichester UK John Wiley amp Sons 2011 1ndash16

[2] Bahl J Lau MCY Smith GJD et al Ancient origins determine global biogeography of hot andcold desert cyanobacteria Nat Commun 2011 2163




[3] Garcia-Pichel F Loza V Marusenko Y Mateo P Potrafka RM Temperature drives thecontinental-scale distribution of key microbes in topsoil communities Science 2013340(6140)1574ndash7

[4] Li X-Y Lin H Levia DF Coupling ecohydrology and hydropedology at different spatio-temporalscales in water-limited ecosystems In Hydropedology Elsevier 2012 737ndash58

[5] Pueyo Y Moret-Fernaacutendez D Saiz H Bueno CG Alados CL Relationships between plantspatial patterns water infiltration capacity and plant community composition in semi-aridMediterranean ecosystems along stress gradients Ecosystems 2013 16452ndash66

[6] Rodriacuteguez-Caballero E Cantoacuten Y Chamizo S Afana A Soleacute-Benet A Effects of biological soilcrusts on surface roughness and implications for runoff and erosion Geomorphology 20124581ndash9

[7] Bowker MA Maestre FT Inferring local competition intensity from patch size distributions atest using biological soil crusts Oikos 2012 1211914ndash22

[8] Bowker MA Maestre FT Mau RL Diversity and Patch-Size Distributions of Biological SoilCrusts Regulate Dryland Ecosystem Multifunctionality Ecosystems 2013 16(6)923ndash33

[9] Delgado-Baquerizo M Maestre FT Escolar C et al Direct and indirect impacts of climatechange on microbial and biocrust communities alter the resistance of the N cycle in a semi-arid grassland J Ecol 2014 102(6)1592ndash605

[10] Proctor MCF Tuba Z Poikilohydry and homoihydry antithesis or spectrum of possibilitiesNew Phytol 2002 156(3)327ndash49

[11] Noy-Meir I Desert ecosystems environment and producers Annu Rev Ecol Syst 1973 425ndash51[12] Collins SL Belnap J Grimm NB et al A Multiscale Hierarchical Model of Pulse Dynamics in

Arid-Land Ecosystems Annu Rev Ecol Evol Syst 2014 45(1)397ndash419[13] McHugh TA Morrissey EM Reed SC Hungate BA Schwartz E Water from air an overlooked

source of moisture in arid and semiarid regions Sci Rep 2015 513767[14] Thomas DSG Science and the desertification debate J Arid Environ 1997 37599ndash608[15] Kassas M Desertification a general review J Arid Environ 1995 30(2)115ndash28[16] Tsakiris G Vangelis H Establishing a drought index incorporating evapotranspiration Eur

Water 2005 9(10)3ndash11[17] Dai A Trenberth KE Qian T A global dataset of Palmer Drought Severity Index for 1870ndash

2002 Relationship with soil moisture and effects of surface warming J Hydrometeorol 20045(6)1117ndash1130

[18] Vicente-Serrano SM Begueriacutea S Loacutepez-Moreno JI A Multiscalar Drought Index Sensitiveto Global Warming The Standardized Precipitation Evapotranspiration Index J Clim 201023(7)1696ndash718

[19] Webb WL Lauenroth WK Szarek SR Kinerson RS Primary Production and Abiotic Controls inForests Grasslands and Desert Ecosystems in the United States Ecology 1983 64(1)134

[20] Lieth H Modeling the primary productivity of the world In Primary productivity of the bio-sphere Springer 1975 237ndash263

[21] Churkina G Running SW Contrasting climatic controls on the estimated productivity of globalterrestrial biomes Ecosystems 1998 1(2)206ndash215

[22] Huxman TE Smith MD Fay PA et al Convergence across biomes to a common rain-use effi-ciency Nature 2004 429(6992)651ndash4

[23] IPCC Climate change 2013 The physical science basis Contribution of working group I to thefifth assesment report of the intergovernmental panel on climate change 2013 1535

[24] Hendry GR Kimball BA The FACE program Agric For Meterology 1994 703ndash14[25] Norby RJ Zak DR Ecological Lessons from Free-Air CO2 Enrichment (FACE) Experiments Annu

Rev Ecol Evol Syst 2011 42(1)181ndash203



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[26] Steven B Gallegos-Graves LV Belnap J Kuske CR Dryland soil microbial communities displayspatial biogeographic patterns associated with soil depth and soil parent material FEMSMicrobiol Ecol 2013 86(1)101ndash13

[27] Belnap J Buumldel B Lange OL Biological soil crusts characteristics and distribution [Internet]Springer 2003 [cited 20 Oct 2015] Available from httplinkspringercomchapter101007978-3-642-56475-8_1

[28] Belnap J The world at your feet desert biological soil crusts Front Ecol Environ 20031(4)181ndash9

[29] Garcia-Pichel F Johnson SL Youngkin D Belnap J Small-Scale Vertical Distribution of Bacte-rial Biomass and Diversity in Biological Soil Crusts from Arid Lands in the Colorado PlateauMicrob Ecol 2003 46(3)312ndash21

[30] Jordan DN Zitzer SF Hendrey GR et al Biotic abiotic and performance aspects of the NevadaDesert Free-Air CO2 Enrichment (FACE) Facility Glob Change Biol 1999 5(6)659ndash68

[31] Smith SD Huxman TE Zitzer SF et al Elevated CO2 increases productivity and invasivespecies success in an arid ecosystem Nature 2000 408(6808)79ndash82

[32] Evans RD Koyama A Sonderegger DL et al Greater ecosystem carbon in the Mojave Desertafter ten years exposure to elevated CO2 Nat Clim Change 2014 4(5)394ndash7

[33] Wertin TM Phillips SL Reed SC Belnap J Elevated CO2 did not mitigate the effect of a short-term drought on biological soil crusts Biol Fertil Soils 2012 48(7)797ndash805

[34] Huxman TE Hamerlynck EP Moore BD et al Photosynthetic down-regulation in Larrea triden-tata exposed to elevated atmospheric CO2 interaction with drought under glasshouse andfield (FACE) exposure Plant Cell Environ 1998 21(11)1153ndash61

[35] Nguyen LM Buttner MP Cruz P Smith SD Robleto EA Effects of elevated atmospheric CO2 onrhizosphere soil microbial communities in a Mojave Desert ecosystem J Arid Environ 201175(10)917ndash25


[37] Schaeffer S Billings S Evans RD Responses of soil nitrogen dynamics in a Mojave Desertecosystem to manipulations in soil carbon and nitrogen availability Oecologia 2003134547ndash53

[38] Soil microbial activity and N availability with elevated CO2 in Mojave Desert soils ndash Billings ndash2004 ndash Global Biogeochemical Cycles ndash Wiley Online Library [Internet] Wiley 2004 [cited 15Oct 2015] Available from httponlinelibrarywileycomdoi1010292003GB002137pdf

[39] Steven B Gallegos-Graves LV Yeager CM Belnap J Evans RD Kuske CR Dryland biologicalsoil crust cyanobacteria show unexpected decreases in abundance under long-term elevatedCO2 Soil cyanobacteria response to elevated CO2 Environ Microbiol 2012 14(12)3247ndash58

[40] Raven JA Colmer TD Life at the boundary photosynthesis at the soilndashfluid interface A synthe-sis focusing on mosses J Exp Bot 2016 erw012

[41] Lane RW Menon M McQuaid JB et al Laboratory analysis of the effects of elevated atmo-spheric carbon dioxide on respiration in biological soil crusts J Arid Environ 2013 9852ndash9

[42] Lange OL Green TGA Reichenberger H The Response of Lichen Photosynthesis to Exter-nal CO2 Concentration and its Interaction with Thallus Water-status J Plant Physiol 1999154(2)157ndash66

[43] Billings S Schaeffer S Evans R Nitrogen fixation by biological soil crusts and heterotrophicbacteria in an intact Mojave Desert ecosystem with elevated CO2 and added soil carbon SoilBiol Biochem 2003 35(5)643ndash9

[44] Allison SD Martiny JB Resistance resilience and redundancy in microbial communities ProcNatl Acad Sci 2008 10511512ndash11519




[45] Dijkstra FA Morgan JA von Fischer JC Follett RF Elevated CO2 and warming effects on CH4uptake in a semiarid grassland below optimum soil moisture J Geophys Res Biogeosciences2011 116(G1)G01007

[46] Mohseni M Abbaszadeh J Nasrollahi Omran A Radiation resistant of native Deinococcus sppisolated from the Lout desert of Iran ldquothe hottest place on Earthrdquo Int J Environ Sci Technol2014 11(7)1939ndash46

[47] Mildrexler DJ Zhao M Running SW Satellite Finds Highest Land Skin Temperatures on EarthBull Am Meteorol Soc 2011 92(7)855ndash60

[48] Doran PT Valley floor climate observations from the McMurdo dry valleys Antarctica 1986ndash2000 J Geophys Res [Internet] 2002 107(D24) [cited 16 Oct 2015] Available from httpdoiwileycom1010292001JD002045

[49] Dai A Trenberth KE Karl TR Effects of clouds soil moisture precipitation and water vapor ondiurnal temperature range J Clim 1999 12(8)2451ndash2473

[50] Hansen J Sato M Ruedy R Lo K Lea DW Medina-Elizade M Global temperature change ProcNatl Acad Sci 2006 103(39)14288ndash14293

[51] Ferrenberg S Reed SC Belnap J Climate change and physical disturbance cause similar com-munity shifts in biological soil crusts Proc Natl Acad Sci 2015 112(39)12116ndash21

[52] Rainey FA Ray K Ferreira M et al Extensive Diversity of Ionizing-Radiation-Resistant Bacte-ria Recovered from Sonoran Desert Soil and Description of Nine New Species of the GenusDeinococcus Obtained from a Single Soil Sample Appl Environ Microbiol 2005 71(9)5225ndash35

[53] Rippka R Waterbury JB Stanier RY Isolation and purification of cyanobacteria some generalprinciples [Internet] In The prokaryotes Springer 1981 212ndash220 [cited 20 Oct 2015] Avail-able from httplinkspringercomchapter101007978-3-662-13187-9_8

[54] Escolar C Martinez I Bowker MA Maestre FT Warming reduces the growth and diversity ofbiological soil crusts in a semi-arid environment implications for ecosystem structure andfunctioning Philos Trans R Soc B Biol Sci 2012 367(1606)3087ndash99

[55] Steven B Kuske CR Gallegos-Graves LV Reed SC Belnap J Climate Change and Physical Dis-turbance Manipulations Result in Distinct Biological Soil Crust Communities Appl EnvironMicrobiol 2015 81(21)7448ndash59

[56] Maphangwa KW Musil CF Raitt L Zedda L Experimental climate warming decreases pho-tosynthetic efficiency of lichens in an arid South African ecosystem Oecologia 2012169(1)257ndash68

[57] Held IM Soden BJ Robust responses of the hydrological cycle to global warming J Clim 200619(21)5686ndash5699

[58] Manabe S Stouffer RJ Sensitivity of a global climate model to an increase of CO2 concentra-tion in the atmosphere J Geophys Res 1980 855529ndash54

[59] Dore MHI Climate change and changes in global precipitation patterns What do we knowEnviron Int 2005 31(8)1167ndash81

[60] Weltzin JF Loik ME Schwinning S et al Assessing the Response of Terrestrial Ecosystems toPotential Changes in Precipitation BioScience 2003 53941ndash52

[61] Bates B Kundzewicz ZW (eds) Intergovernmental Panel on Climate Change Climate changeand water Technical paper of the intergovernmental panel on climate change IPCC Secre-tariat Geneva 2008 pp 210

[62] Maestre FT Salguero-Gomez R Quero JL It is getting hotter in here determining and project-ing the impacts of global environmental change on drylands Philos Trans R Soc B Biol Sci2012 367(1606)3062ndash75

[63] Garnaut R The Garnaut review 2011 Australia in the global response to climate change Cam-bridge University Press 2011



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[65] Seager R Ting M Held I et al Model Projections of an Imminent Transition to a More AridClimate in Southwestern North America Science 2007 316(5828)1181ndash4

[66] Knapp AK Beier C Briske DD et al Consequences of more extreme precipitation regimes forterrestrial ecosystems Bioscience 2008 58(9)811ndash821

[67] Basist A Bell GD Statistical relationships between topography and precipitation patternsJ Clim 1994 71305ndash15

[68] Daly C Neilson RP Phillips DL A statistical-topographic model for mapping climatologicalprecipitation over mountainous terrain J Appl Meteorol 1994 33140ndash58

[69] Xie P Arkin A Analyses of global monthly precipitation using gauge observations satelliteestimates and numerical model predictions J Clim 1996 9840ndash58

[70] Birch HF The effect of soil drying on humus decomposition and nitrogen availability Plant Soil1958 10(1)9ndash31

[71] Trenberth KE The definition of El Nino Bull Am Meteorol Soc 1997 782771ndash7[72] Sponseller RA Precipitation pulses and soil CO2 flux in a Sonoran Desert ecosystem Glob

Change Biol 2007 13(2)426ndash36[73] Huxman TE Snyder KA Tissue D et al Precipitation pulses and carbon fluxes in semiarid and

arid ecosystems Oecologia 2004 141(2)254ndash68[74] Reynolds JF Kemp PR Ogle K Fernaacutendez RJ Modifying the ldquopulsendashreserverdquo paradigm for

deserts of North America precipitation pulses soil water and plant responses Oecologia2004 141(2)194ndash210

[75] Austin AT Yahdjian L Stark JM et al Water pulses and biogeochemical cycles in arid andsemiarid ecosystems Oecologia 2004 141(2)221ndash35

[76] Schwinning S Sala OE Loik ME Ehleringer JR Thresholds memory and seasonality under-standing pulse dynamics in aridsemi-arid ecosystems Oecologia 2004 141(2)191ndash3

[77] Reed SC Coe KK Sparks JP Housman DC Zelikova TJ Belnap J Changes to dryland rainfallresult in rapid moss mortality and altered soil fertility Nat Clim Change 2012 2(10)752ndash5

[78] Brown JH Valone TJ Curtin CG Reorganization of an arid ecosystem in response to recentclimate change Proc Natl Acad Sci 1997 94(18)9729ndash9733

[79] Adler PB Levine JM Contrasting relationships between precipitation and species richness inspace and time Oikos 2007 116(2)221ndash32

[80] Kreft H Jetz W Global patterns and determinants of vascular plant diversity Proc Natl AcadSci 2007 104(14)5925ndash5930

[81] Davenport ML Nicholson SE On the relation between rainfall and the Normalized Differ-ence Vegetation Index for diverse vegetation types in East Africa Int J Remote Sens 199314(12)2369ndash89

[82] Heisler-White JL Knapp AK Kelly EF Increasing precipitation event size increases above-ground net primary productivity in a semi-arid grassland Oecologia 2008 158(1)129ndash40

[83] Pointing SB Warren-Rhodes KA Lacap DC Rhodes KL McKay CP Hypolithic community shiftsoccur as a result of liquid water availability along environmental gradients in Chinarsquos hot andcold hyperarid deserts Environ Microbiol 2007 9(2)414ndash24

[84] Titus JH Nowak RS Smith SD Soil resource heterogeneity in the Mojave Desert J Arid Environ2002 52(3)269ndash92

[85] Kuske CR Ticknor LO Miller ME et al Comparison of Soil Bacterial Communities in Rhizo-spheres of Three Plant Species and the Interspaces in an Arid Grassland Appl Environ Micro-biol 2002 68(4)1854ndash63

[86] Kidron GJ The effect of shrub canopy upon surface temperatures and evaporation in the NegevDesert Earth Surf Process Landf 2009 34(1)123ndash32




[87] Bachar A Soares MIM Gillor O The Effect of Resource Islands on Abundance and Diversity ofBacteria in Arid Soils Microb Ecol 2012 63(3)694ndash700

[88] Wezel A Rajot J-L Herbrig C Influence of shrubs on soil characteristics and their function inSahelian agro-ecosystems in semi-arid Niger J Arid Environ 2000 44(4)383ndash98

[89] Schlesinger WH Raikes JA Hartley AE Cross AF On the Spatial Pattern of Soil Nutrients inDesert Ecosystems Ecology 1996 77(2)364

[90] Chan Y Lacap DC Lau MCY et al Hypolithic microbial communities between a rock and ahard place Hypolithic microbial communities Environ Microbiol 2012 14(9)2272ndash82

[91] Cowan DA Khan N Pointing SB Cary SC Diverse hypolithic refuge communities in the Mc-Murdo Dry Valleys Antarct Sci 2010 22(06)714ndash20

[92] Wichern F Joergensen RG Soil Microbial Properties Along a Precipitation Transect in SouthernAfrica Arid Land Res Manag 2009 23(2)115ndash26

[93] Nielsen UN Ball BA Impacts of altered precipitation regimes on soil communities and biogeo-chemistry in arid and semi-arid ecosystems Glob Change Biol 2015 21(4)1407ndash21

[94] Chen D Mi J Chu P et al Patterns and drivers of soil microbial communities along a precipita-tion gradient on the Mongolian Plateau Landsc Ecol 2015 30(9)1669ndash82

[95] Si G Lei T Xia Y Yuan Y Zhang G Microbial Nonlinear Response to a Precipitation Gradient inthe Northeastern Tibetan Plateau Geomicrobiol J 2015 3385ndash97

[96] Fierer N Strickland MS Liptzin D Bradford MA Cleveland CC Global patterns in belowgroundcommunities Ecol Lett 2009 12(11)1238ndash49

[97] Ben-David EA Zaady E Sher Y Nejidat A Assessment of the spatial distribution of soil mi-crobial communities in patchy arid and semi-arid landscapes of the Negev Desert using com-bined PLFA and DGGE analyses Microbial community structure in patchy desert landscapesFEMS Microbiol Ecol 2011 76(3)492ndash503

[98] Angel R Soares MIM Ungar ED Gillor O Biogeography of soil archaea and bacteria along asteep precipitation gradient ISME J 2010 4(4)553ndash563

[99] Pasternak Z Al-Ashhab A Gatica J et al Spatial and Temporal Biogeography of Soil MicrobialCommunities in Arid and Semiarid Regions PLoS ONE 2013 8(7)e69705


[101] Evans SE Wallenstein MD Soil microbial community response to drying and rewetting stressdoes historical precipitation regime matter Biogeochemistry 2012 109(1ndash3)101ndash16

[102] Castro HF Classen AT Austin EE Norby RJ Schadt CW Soil Microbial Community Responses toMultiple Experimental Climate Change Drivers Appl Environ Microbiol 2010 76(4)999ndash1007

[103] McHugh TA Koch GW Schwartz E Minor Changes in Soil Bacterial and Fungal CommunityComposition Occur in Response to Monsoon Precipitation in a Semiarid Grassland MicrobEcol 2014 68(2)370ndash8

[104] Steven B Gallegos-Graves LV Starkenburg SR Chain PS Kuske CR Targeted and shotgunmetagenomic approaches provide different descriptions of dryland soil microbial communi-ties in a manipulated field study Environ Microbiol Rep 2012 4(2)248ndash56

[105] Steven B Lionard M Kuske CR Vincent WF High bacterial diversity of biological soil crusts inwater tracks over permafrost in the high Arctic polar desert PLoS ONE 2013 8(8)e71489

[106] Caruso T Chan Y Lacap DC Lau MC McKay CP Pointing SB Stochastic and deterministicprocesses interact in the assembly of desert microbial communities on a global scale ISME J2011 5(9)1406ndash1413

[107] Vincent WF Cyanobacterial Dominance in the Polar Regions [Internet] In Whitton BAPotts M editors The Ecology of Cyanobacteria Dordrecht Kluwer Academic Publishers 2002321ndash40



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[108] Wynn-Williams DD Cyanobacteria in Deserts ndash Life at the Limit In Whitton BA Potts M edi-tors The Ecology of Cyanobacteria Dordrecht Kluwer Academic Publishers 2002 341ndash66

[109] Grishkan I Zaady E Nevo E Soil crust microfungi along a southward rainfall gradient indesert ecosystems Eur J Soil Biol 2006 42(1)33ndash42

[110] Yang H Yuan Y Zhang Q Tang J Liu Y Chen X Changes in soil organic carbon total nitrogenand abundance of arbuscular mycorrhizal fungi along a large-scale aridity gradient Catena2011 87(1)70ndash7

[111] Aranibar JN Otter L Macko SA et al Nitrogen cycling in the soil-plat system along a precipita-tion gradient in the Kalahari sands Glob Change Biol 2004 10359ndash73

[112] Wardle DA A comparative assessment of factors which influence microbial biomass carbonand nitrogen levels in soil Biol Rev 1992 67(3)321ndash358

[113] Batjes NH Total carbon and nitrogen in the soils of the world Eur J Soil Sci 2014 65(1)10ndash21[114] Zhou X Talley M Luo Y Biomass Litter and Soil Respiration Along a Precipitation Gradient in

Southern Great Plains USA Ecosystems 2009 12(8)1369ndash80[115] Thompson TL Zaady E Huancheng P Wilson TB Martens DA Soil C and N pools in patchy

shrublands of the Negev and Chihuahuan Deserts Soil Biol Biochem 2006 38(7)1943ndash55[116] Vicca S Bahn M Estiarte M et al Can current moisture responses predict soil CO2 efflux un-

der altered precipitation regimes A synthesis of manipulation experiments Biogeosciences2014 11(11)2991ndash3013

[117] Belnap J Phillips SL Miller ME Response of desert biological soil crusts to alterations inprecipitation frequency Oecologia 2003 141(2)306ndash16

[118] Zelikova TJ Housman DC Grote EE Neher DA Belnap J Warming and increased precipitationfrequency on the Colorado Plateau implications for biological soil crusts and soil processesPlant Soil 2012 355(1ndash2)265ndash82

[119] Johnson SL Kuske CR Carney TD Housman DC Gallegos-Graves LV Belnap J Increased tem-perature and altered summer precipitation have differential effects on biological soil crusts ina dryland ecosystem Glob Change Biol 2012 18(8)2583ndash93

[120] Griffiths BS Ritz K Wheatley RE Nematodes as indicators of enhanced microbiological activ-ity in a Scottish organic farming system Soil Use Manag 1994 10(1)20ndash24

[121] Cole L Dromph KM Boaglio V Bardgett RD Effect of density and species richness of soilmesofauna on nutrient mineralisation and plant growth Biol Fertil Soils 2003 1(1)1ndash1

[122] Demeure Y Freckman DW Van Gundy SD Anhydrobiotic coiling of nematodes in soil J Nema-tol 1979 11(2)189

[123] Whitford WG Freckman DW Elkins NZ et al Diurnal migration and responses to sim-ulated rainfall in desert soil microarthropods and nematodes Soil Biol Biochem 198113(5)417ndash425

[124] Reeves JL Blumenthal DM Kray JA Derner JD Increased seed consumption by biological con-trol weevil tempers positive CO2 effect on invasive plant (Centaurea diffusa) fitness Biol Con-trol 2015 8436ndash43

[125] Freckman DW Whitford WG Steinberger Y Effect of irrigation on nematode population dynam-ics and activity in desert soils Biol Fertil Soils 1987 3(1ndash2)3ndash10

[126] Sackett TE Classen AT Sanders NJ Linking soil food web structure to above- and below-ground ecosystem processes a meta-analysis Oikos 2010 119(12)1984ndash92

[127] Van der Putten WH Vet LE Harvey JA Waumlckers FL Linking above- and belowground multi-trophic interactions of plants herbivores pathogens and their antagonists Trends Ecol Evol2001 16(10)547ndash554

[128] Schwinning S Sala OE Hierarchy of responses to resource pulses in arid and semi-aridecosystems Oecologia 2004 141(2)211ndash20




[129] Beatley JC Phenological Events and Their Environmental Triggers in Mojave Desert Ecosys-tems Ecology 1974 55(4)856

[130] Potts DL Huxman TE Enquist BJ Weltzin JF Williams DG Resilience and resistance of ecosys-tem functional response to a precipitation pulse in a semi-arid grassland J Ecol 200694(1)23ndash30

[131] Stark LR Phenology and Reproductive Biology of Syntrichia inermis (Bryopsida Pottiaceae) inthe Mojave Desert The Bryologist 1997 100(1)13

[132] Coe KK Belnap J Sparks JP Precipitation-driven carbon balance controls survivorship ofdesert biocrust mosses Ecology 2012 93(7)1626ndash36

[133] Darrouzet-Nardi A Reed SC Grote EE Belnap J Observations of net soil exchange of CO2 in adryland show experimental warming increases carbon losses in biocrust soils Biogeochem-istry 2015 126(3)363ndash78

[134] Le Houeacuterou HN Climate change drought and desertification J Arid Environ 1996 34(2)133ndash185

[135] Amundson R Franco-Vizcaiacuteno E Graham RC DeNiro M The relationship of precipitation sea-sonality to the flora and stable isotope chemistry of soils in the Vizcaino desert Baja Califor-nia Mexico J Arid Environ 1994 28(4)265ndash279

[136] Oliver MJ Velten J Wood AJ Bryophytes as experimental models for the study of environ-mental stress tolerance Tortula ruralis and desiccation-tolerance in mosses Plant Ecol 2000151(1)73ndash84



Doreen Babin Michael Hemkemeyer Geertje J PronkIngrid Koumlgel-Knabner Christoph C Tebbe and Kornelia Smalla9 Artificial Soils as Tools for Microbial Ecology

91 Introduction

Soils are not only regarded as black box due to their opaque nature but also becausethey are among themost complex biomaterials on earth [1 2] Looking closer into soilsone canfind heterogeneous compounds of different origins various sizes and proper-ties Due to interactions between these compounds an aggregated three-dimensionalstructure arises pervaded by a porous network offering various niches for microbialcolonization Therefore it is not surprising that the soil microbiota also exhibits hugediversity [3] This soil complexity still challenges soil science and impedes a betterunderstanding of soil microbial communities and their interactions with the naturalsoil environment From the researcherrsquos point of view soils unfortunately never onlydiffer inone singleproperty due to eg differentparental rockmaterials climatic con-ditions or land use These different factors hinder the comparison of soils andmake itimpossible to ultimately clarify causal relationships Consequently only carefully de-signed experiments with reduced natural soil complexity can deliver reliable answersto soil microbial ecology and go beyond a solely descriptive character [3] Schreiterand colleagues recently published a series of experiments running in an experimen-tal plot system with three soils of different origin (diluvial sand alluvial loam loessloam) stored for 10 years at the same site and with the same cropping history [4ndash6]Thereby the authors could evaluate to which extent soil properties drive the micro-bial community composition in the bulk soil and rhizosphere under field conditionsexcluding factors like soil management climate or cropping history However to dis-entangle the effect of a particular soil parameter for instance the influence of organicmatter (OM) specific minerals soil texture or water potential on the microbiota itseems reasonable to focus on model systems rather than on ldquonaturalrdquo soils whichhave this immense heterogeneity [3 7] 998835 Fig 91 shows experimental model systemsused 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 thesoil system have been used by numerous studies in the past providing insights intothe influence of clay minerals eg on microbial growth metabolism survival bio-chemical activity and genetic transfer [1 8ndash11] Porous media or so-called transpar-ent soils offering soil-like physicochemical characteristics are used as a suitable toolfor visualization of colloids within the soil structure [12] or of the rhizosphere and its

DOI 1015159783110419047-009

Brought to you by | University of Sydney LibraryAuthenticated


160 | 9 Artificial Soils as Tools for Microbial Ecology

SimplificationComplexity

Non-Arid SoilsNatural soils eggrasslandforest mesictropical soilsOffer full complexityDescriptivestudies

No SoilInteraction studiesbetween microbiota and clean soilcomponentsArtificial media forcultivation

Porous MediaOnly mineral particlesSoil-like matrix and physico-chemical properties

Artificial SoilsSoil-likeIncubationmaturationAggregated structureReproducible

Arid SoilsNatural soilsWater-deficientLow OM content

Sterile SoilsSoil-likeIncubationmaturationAggregated structure

Fig 91 Schematic diagram of types of soil experiments

associated microbiome [13] In contrast microcosm experiments with sterilized soilsexhibit a much higher soil-like complexity (998835 Fig 91) By setting up different matricpotentials in sterilized soils Wright et al [14] for instance showed that pore sizes arean important determinant for bacterial protection against predators Soil sterilizationcan be also a useful method for soil microbial ecology studies by inoculation of a de-finedmicrobial consortium and by tracking its development and activity in an almostnatural soil environment [15ndash17] If the focus is however to unravel the impact of acertain parameter within a soil-like system then artificial soils are regarded as a goodtool allowing us to specifically manipulate the soil composition in a reproducible way(998835 Fig 91) As inferred from the name artificial or synthetic soils are designed withknown composition In comparison to commercially available artificial soil productsfor 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 howearlier and recent artificial soil experiments contributed to the understanding of soilmicrobial communities and how this can be linked to arid soil research

92 Soil Definition

The Soil Science Society of America defines soil as ldquothe unconsolidated mineral or or-ganic material on the immediate surface of the earth that serves as a natural mediumfor the growth of land plantsrdquo [18] The growth of plants in soil is made possible by thedifferent soil components and their interactions The principal soil constituents areminerals water gases and soil organic matter (SOM) including the living soil biota



92 Soil Definition | 161

The portion of each constituent can vary considerably between different soils depend-ing on eg the soil type climate and vegetation In terms of plant growth ideal num-bers were estimated to be 45 (wtwt) minerals 25water 25 air and 5SOM [19]In contrast to other habitats colonized by microorganisms soils are dominated bysolid compounds that differ in their chemical composition (mineralogy) dependingon parental rockmaterial and their particle size Clay-sizedparticles (lt 2 μm) like clayminerals (eg illite montmorillonite kaolinite) and metal oxides (eg derived fromFe Al Mn) as a product of mineral weathering might be of special importance formicroorganisms 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 substancesand 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 amatrix 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 layersadhering to soil particles or to water filled pores Instead of living planktonically mostbacterial cells likely reside in unsaturated soils at the solidndashliquid interface embeddedin extracellular polymeric substances (EPS) protected against eg desiccation [3 23]Transport of bacterial cells and nutrients as well as gaseous fluxes depends on thesoil water content and therefore water-deficiency as present in arid soils is a severeenvironmental stress factor for most soil bacteria [23] An exception are filamentousbacteria and fungi that are less dependent on the presence of water thanks to theirhyphal growth allowing air-filled pores to be bridged [24] The soil water content alsoinfluences the connectivity of microbial habitats and the opportunity for microbial in-teractions and colonization of new surfaces Therefore the important role of wateron diversity and structuring of microbial communities must be kept in mind [23 25ndash27]

Soils exhibit a high abundance of microorganisms and a tremendous microbialdiversity [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 thesurfaces available soils are still scarcely inhabited andmicroorganisms typically oc-cur concentrated as hotspots (similar to the earthrsquos colonization by humans) Thesehotspots are a direct consequence of the interaction and clustering of different soilconstituents resulting in the formationof soil aggregateswith largebiogeochemical in-terfaces (BGIs) [31] The three-dimensional soil structure is therefore a self-organizedsystem under active contribution of microorganisms due to the gluing properties ofEPS and hyphal growth [2]




93 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 [32ndash35] Thus the hitherto common practice of performing experiments with soil microor-ganisms after growing them on artificial media to cell concentrations much abovethose that would be present in a soil seemed to fully ignore the structural nutritionaland 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 insand aeration and thickness of the moisture film around soil particles are all criti-cal factors influencing bacterial activity Soumlhngen [34] pointed out the importance ofsoil colloids that absorb mineral nutrients and condense surface gases [36] These re-sults demonstrated the pitfalls of cultivation-dependent studies and cleared the wayto looking for new methods for studying soil bacteria and their processes The soilprocess mediated by microorganisms that received the main focus at that time wasthe cycling of nitrogen While Loumlhnis and Green [37] used nutrient solutions basedon soil extracts for physiological tests others tried to study nitrification directly bysoil incubation studies [33] According to Allen and Bonazzi [36] both methods hadtheir limitations These authors worked with soils of reduced complexity in which theOM was destroyed by ignition and concluded that ldquosoil as a medium possesses theproperty of supporting nitrification better than sandrdquo [36] However the reason at thattime remained obscure The authors in fact suggested that probably only buildingup a close-to-natural soil environment ie a synthetic soil would give detailed in-sights into soil processes However the first attempt of Stevens and Withers [33] toconstruct a universal standardized artificial soil medium of high nitrifying capacityfailed There were also early attempts to reduce soil complexity by adding a definedinoculant to previously sterilized soils to subsequently monitor the decomposition ofan 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 [39ndash41] but the success waslimited and the understanding of interactions between microorganisms and the soilmatrix was still barely possible In 1937 Madhok [42 43] again proposed the designof defined synthetic soil compositions under laboratory conditions for studying mi-crobiological soil processes (eg cellulose decomposition nitrification and nitrogenfixation) These first synthetic soils were composed of different mixtures of sand ben-tonite andhumus inoculatedwitha suspensionobtained fromaldquogoodfield soilrdquo [42]Martin and Waksman [44] used the artificial soil media proposed by Madhok [42] tostudy the binding and aggregating effects of microorganisms on soil particles Theirstudies with sand-bentonite and sand-clay mixtures inoculated with different pureand 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-



93 History of Artificial Soil Experiments | 163

gestions byMadhok [42] and composed a synthetic soil of sand and different mixturesvarying in type and amount of colloids in order to create a suitable culture mediumfor soil bacteria They found that colloids (eg bentonite) improved sand as a growthmedium 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 carrierof eg Mg2+ Ca2+ and K+ and as a sorbent of harmful byproducts [45]

In the 1950s and 1960s experimental pedology became popular which is definedas the realization of controlled experiments to study pedogenic processes [46] In thisrespect 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 bacterialmovements in soil using simplified porous media [48ndash50]

Recently artificial soils becamean important tool for analyzing the establishmentand functioningof soilmicrobial communities Ellis [51] developedaprotocol for anar-tificial soilwith essential components of a natural soil butwith reducedheterogeneityThis protocol was later improved byGuenet et al [7] who proposed it as a suitable toolfor studying soil microbial processes Zhang et al [52] used artificial soils incubatedfor several months to understand the temperature sensitivity of SOM decompositionfocusing therein on the effect of its chemical recalcitrance and the soil clay mineralcomposition Based on the assumption that the supply of a mineral phase a sourceof OM and a microbial community provides all the essential ingredients to form asoil-like material Pronk et al [53] designed eight different artificial soils (998835 Fig 92)These were composed of differentmixtures of theminerals illite montmorillonite fer-rihydrite and boehmite and charcoal Sand- and silt-sized quartz were used to providetexture sterilizedmanurewas added as a substrate and themixtureswere inoculatedwith an extract from a natural arable soil

These artificial soils were analyzed in a multidisciplinary approach in order tostudy the initial formation of BGIs in soil as a function of the type of particle surfacespresent The artificial soil mixtures differed in complexity and mineral compositionand were incubated over 18 months in the dark at 20degC on average and a constant wa-ter content of 60 of the maximumwater holding capacity Pronk et al [53] detecteda fast development of these artificial soils to soil-like aggregated systems and showedthe importance of clay mineral presence for macroaggregate formation In contrast totheir expectations microaggregation was similar among soils independently of thepresence and type of clay minerals metal oxides or charcoal The authors suggestedthat development of their artificial soils was not fully completed after 18 months ofincubation and that the stability of the systems declined as a consequence of missingfresh OM input [53] Therefore Vogel et al [54] started a follow-up experiment withfive of these artificial soil mixtures and incubated them for 842 days after they hadreceived 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-




Fig 92 Dry model minerals and sterile manure usedby Pronk et al [53] to compose artificial soils

gates These results demonstrated the importance of a continuous OM supply for theformation of soil macroaggregates and indicated their dynamic nature in the absenceof 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 arethe 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 ofthe Priority ProgramSPP1315 of the Deutsche Forschungsgemeinschaft (DFG)were ac-companied by various microbiological analyses (998835 Tab 91) These recent results andthe results from other microbial ecology studies using artificial soils or simplified soilmicrocosms as a tool to better understand soil microbial communities and their shap-ing factors are reported below (998835 Tab 92)

94 Methods in Soil Microbial Ecology and Soil Science

New insights into soil science and soil microbiology depend on technical progresswhich increases our capacity to handle the opaque nature of soil its complicated



94 Methods in Soil Microbial Ecology and Soil Science | 165

three-dimensional arrangement and the microbial inhabitants that are not visible tothe naked eye The beginnings of soil microbiology were solely based on cultivationtechniques and as outlined above many different attempts were made to mimic thenatural soil environment in the laboratory However even with improved growth me-dia and cultivation conditions only a small fraction of the soil microbial communitycan be cultivated (approximately 03) [55] The advent of molecular techniques inmicrobial ecology promoted the understanding of the structural and functional di-versity of soil microbial communities The extraction of nucleic acids directly fromthe soil matrix or after obtaining the microbial fraction opened new opportunities tostudy soil microorganisms independently of cultivation [56] Possessing highly con-served and variable regions that allow drawing conclusions on taxonomy the 16SrRNA gene coding for the small subunit of the ribosomal RNA was established asbroad phylogenetic marker for bacteria and archaea [57] Over the years a large refer-ence database emerged that to date contains more than 43 million rRNA sequences(wwwarb-silvade) [58] The internal transcribed spacer (ITS) region between the 18SrRNA and 28S rRNA genes was found to be more useful for studying fungal diversityand abundance [59] Quantitative real time PCR (qPCR) allows estimating the amountof soil microorganisms based onmarker gene copy numbers per gram of soil Alterna-tively the analysis of phospholipid fatty acids (PLFA) presents a well established toolto quantify bacterial and fungal biomass in soil [60] The soil microbial communitystructure can be profiled (molecular fingerprint) by different techniques such as ter-minal restriction fragment length polymorphism (T-RFLP) or denaturing gradient gelelectrophoresis (DGGE) based on amplified 16S rRNA gene or ITS fragments [59 61]All these techniques are based on the electrophoretic separation of the marker geneamplicons according to differences in their DNA sequence They brought about greatprogress since for the first time a relatively large dataset could be profiledwithin a fewdays allowing the detection and preliminary identification of microbial responders totreatments and also by the use of an appropriate number of independent replicates asubsequent statistical analysis of microbial community changes The effect of a bettertaxonomic information content associated with constantly falling sequencing costs isthat high-throughput next-generation sequencing techniques are nowadays preferredto nonsequencingmethods for studying soil microbial community compositions egpyrosequencing or Illumina MiSeq Besides the usage of these phylogenetic markersthe detection of functional genes can showpotential metabolic pathways of a commu-nity and indicatemicrobial guilds while enzymeactivity assays are a tool to determineactive 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 inthe beginning of this book chapter soils provide various niches for microbial colo-nization In most ecological studies soil samples are randomly collected and mixedresulting in the destruction of soil aggregates and therefore in an immense loss of




information on microbial habitats Attention is no longer paid to distances for mi-crobial interaction nutrient accessibility or protective habitats [64] As thoroughlyreviewed 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 tostudy 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 smallsize fractions (lt 20 μm) and Sessitsch et al [67] additionally found that different par-ticle size classes exhibit differences in community composition Furthermore by mildultrasonication 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 ofmicroscopic and spectroscopic techniques that are capable of characterizingsoil particles at the submicron scale may allow for the characterization of habitats atscales directly relevant for microbes For example secondary ion mass spectrometryat the nanoscale (NanoSIMS) is promising in terms of giving new insights into thesmall-scale soil component arrangement With NanoSIMS it is possible to analyze theelemental 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] Heisteret al [70] found a patchy arrangement of organic material in incubated artificial soilson clay mineral surfaces The method also allowed differentiating between charcoaland SOM [70] By applying NanoSIMS in soil ecology studies new insights into OMturnover and spatial distribution as well asmicrobial residue formation can be gainedand will be presented among others hereafter

95 Insights into Microbial Communities from Artificial SoilStudies

951 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 analysisof the microbial community development (998835 Tab 91) The artificial soils received aninoculant obtained by water extraction from a natural soil It is probable that not allsoil microorganisms could be detached from the soil matrix by this extractionmethodand thus the inoculantmight have exhibited a lowermicrobial diversity and richnesscompared to the natural soil microbial community Certainly compared to the naturalcolonization of developing soils which is driven by biocolloid transports in soil or airthe colonizationof artificial soils by inoculationwith amicrobial community extracted



95 Insights into Microbial Communities from Artificial Soil Studies | 167

from soil is different Furthermore the mineral surfaces provided mimicked alreadyphysically and chemically weathered material and the added OM provided as sterilemanure represented a partially degraded litter which differs from conditions in na-ture The approach by Pronk et al [53] however allowed the comparison of microbialcommunity developments between soils of differentmineral compositions as all soilsreceived an aliquot of the same inoculant Ding et al [71] studied the early bacterialcommunity establishment in these artificial soils By DGGE and pyrosequencing anal-ysis of bacterial 16S rRNA gene fragments amplified from total community-DNA theauthors showed that bacterial community complexity increased with increasing incu-bation time Artificial soils of differentmineral composition exhibited similar bacterialabundances and diversity However the bacterial diversity in artificial soils incubatedfor 90 days was significantly lower than in the inoculant added to the mixtures at theincubation start [71] Obviously not all bacteria could adapt similarly to the condi-tions that prevailed at initial BGIs These findings therefore provide insights into theadaptation and establishment of soil microorganisms at new pristine surfaces

Molecular fingerprinting techniques were used to compare the structure of thebacterial communities established between these different artificial soils After 90days of incubation a strong effect of charcoal and to a lesser extent of clay mineralson the structure of the bacterial community was observed Metal oxides appeared tohave a weak influence on the betaproteobacterial community By pyrosequencingresponders to minerals or charcoal could be identified and a putative taxonomicaffiliation was possible among others Devosia Rhizobium and Sphingomonas wereenriched in artificial soils containing charcoal Positive responders showing an in-creased relative abundance in the presence of montmorillonite were mainly affiliatedtoGammaproteobacteria andBacteroideteswhereas responders to illitewere found tobelong to distantly related taxa [71] Although the resolution level of the 16S rRNAgenefor bacterial identification is limited information on the phylogenetic and taxonomicaffiliation of responders is still helpful for gaining new insights into the ecologicalrole of certain bacterial taxa

Numerous studies carried out previously with clean particles single bacterialstrains or addition of minerals to soils reported on direct and indirect influences ofminerals on microbes [1 8ndash10 72] In a recent review Uroz et al [73] even proposedthe term ldquomineralosphererdquo emphasizing that minerals represent a specific micro-bial habitat These might be underlying interactions leading to the enrichment orinhibition of bacterial taxa by minerals and charcoal as observed in artificial soilstudies [71 74 75] Results from the artificial soil incubation experiment mentionedabove showed for the first time that these microbe-mineral interactions are also im-portant during early BGI formation and influence the development of soils Artificialsoils from this study [53] were further incubated and after 1 year the effect of metaloxides on Bacteria increased while the influence of charcoal declined probably dueto occlusion of surfaces by OM [74 76] A pronounced influence of clay minerals onBacteria and Fungi was still observed [74] By particle size fractionation Hemkemeyer




et al [77] were able to demonstrate differences between prokaryotic communities liv-ing attached to the quartz-dominated coarser fractions (20ndash63 and 63minus2000 μm) andthe clay-dominatedfinest fraction (lt 20 μm) In the latter case the influence of the ar-tificial soilmineral compositionwasmost pronounced and resulted in different bacte-rial and archaeal communities However Fungi were sensitive to artificial soil mineralcompositions across all particle size fractions These microbial responses to artificialsoil 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 discreteniches for microbial colonization This development was suggested to contribute tomicrobial divergence in soil [76] and helps to understand the tremendous microbialdiversity in soil In addition the analysis of abundances of specific bacterial taxaand activity of enzymes involved in nutrient cycling in those artificial soils indicateda succession in the microbial community from copiotrophic to oligotrophic lifestylelikely due to nutrient limitations [78]

Pronk et al [53] suggested that these artificial soils were still developing even after15 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 anadditional 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 muchstronger and lasted for a longer time in established systems as observed by the CO2respiration rates and the microbial gene abundances measured This was attributedto 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 ofclay mineral exhibited significantly different amounts of macroaggregates In addi-tion the microbial community structure differed significantly between soils with illitefrom those with montmorillonite [54 75] Moreover clay minerals could be identifiedas key drivers of the soilmicrobiota in the long term in comparison to charcoal and fer-rihydrite The effect of charcoal and ferrihydrite was still pronounced after 842 days ofincubation but seemed to be more important for the early microbial community de-velopment [75] After long-term incubation of more than 2 years new discriminativetaxa among artificial soils were found by pyrosequencing analysis compared to theanalysis after 90 days of incubation [71] supporting the concept of dynamicmicrobialcommunity establishment [79] For instance the actinobacterial genus Rhodococcusand the alphaproteobacterial genus Filomicrobium were enriched in soils containingillite whereas in montmorillonite containing soils a higher relative abundance of Fir-micutes (eg 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 randomprocess since highly similarmicrobial communitieswere established among indepen-dent replicates of artificial soil mixtures [71 74 75] Furthermore the experimentalsetup of an independent artificial soil experiment with extended incubation time and




a different microbial inoculant [54] showed reproducible results in terms of microbialcommunity establishment CO2 respiration and OM development

Insights into microbial community establishment and structuring by means ofartificial soils that were gained within the framework of the DFG Priority ProgramSPP1315 are summarized in 998835 Tab 91

An independent study with simplified soils was conducted byWolf et al [26] whoaimed at understanding soil microbial interactions and diversity development Theauthors 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 hydraulicproperties were inoculated with a nonfilamentous (Bacillus weihenstephanensis) anda filamentous bacterial strain (Streptomyces atratus) These simplified artificial soilsrevealed 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 isolationcreated by varied moisture content on competitive dynamics of two bacterial speciesgrowing on a single nutrient source (24-dichlorophenoxyacetic acid) in a uniformsand 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 ofstructuring microbial communities [27] (998835 Tab 92)

952 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 microbialcommunities [71 74ndash77] However microorganisms in these systems were not onlypassive responders to the soil mineral composition since soils were incubated allow-ing bacteria and fungi to actively colonize and structure the soil system The highermacroaggregation in artificial soils containing montmorillonite was explained by Vo-gel et al [54] by the presence of a different bacterial community compared to that insoils containing illite These bacteria might have differed in their potential to producegluing 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 reportedby Ditterich et al [78] showing that enzyme activities in artificial soils incubated for 6months depended on the soil composition Furthermore by pyrosequencing analysisof 16S rRNA gene fragments amplified from total community-DNA of artificial soilsincubated for more than 2 years less taxa affiliated to Bacteroidetes were detectedin montmorillonite containing soils that can usually be found in more nutrient-richenvironments due to their copiotrophic lifestyle [79] In contrast no differences wereobserved 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 productionof OM in the fine fraction (lt 20 μm) which supports the concept of functional re-dundancy among phylogenetically distant related microbial taxa The laboratory




Tabl

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1Ar

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also

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udie

sw

ithin

the

fram

ewor

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the

DFG

Prio

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Prog

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chem

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Inte

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Soil

(SPP

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Dete

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Soil

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days

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Ding

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Deve

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zym

eac

tivity

36

121

8m

onth

sPr

onk

etal

[53

]

Pron

ket

al

[80

83]

Unde

rsta

ndin

gOM

turn

over

and

deve

lopm

ent

over

soil

incu

batio

ntim

eSo

ilm

iner

alco

mpo

-si

tion

and

pres

ence

ofch

arco

al

OMch

arac

teriz

a-tio

nfra

ctio

natio

n3

612

18

mon

ths

Pron

ket

al[

54]

Voge

leta

l[8

5]Un

ders

tand

ing

OMtu

rnov

eran

dfo

rmat

ion

ofor

gano

-min

eral

asso

ciat

ions

atlo

ng-te

rmm

atur

edBG

Is

Soil

min

eral

com

po-

sitio

nan

dpr

esen

ceof

char

coal

Fum

igat

ion-

extra

c-tio

nOM

char

acte

ri-za

tion

fract

iona

tion

842

days

+63

days

13C

15N

labe

led

plan

tlitt

er

Voge

leta

l[5

4]




Table 92 Other artificial soil studies or simplified microcosm experiments focusing on soil micro-bial communities

Publication Aim of Study Factor(s) ofVariance

Detection Methods IncubationTime

Wolf et al[26]

Understanding bacterialgrowth dynamics andmicrobial interactions insoil

Hydraulic con-nectivity ofmicrohabitats

Bacterial platingmotility rate waterretention curve

12 days

Treves et al[27]

Determining the role ofspatial isolation for soilmicrobial communitystructure

Moisture con-tent

Bacterial plating 7 days

Heckmanet al [8196]

Understandingorgano-mineral-microberelationships

Oxide surface Nutrient analysispyrosequencingsoil fractionationX-ray diffractionSEMEDSa

5 10 2030 60 90154 days

Wei et al[84]

Understanding OMdecomposition

Clay contenttemperature

Microbial biomasscarbon PLFA pro-file enzyme activi-ties

2 months

Wei et al[86]

Understanding the roleof microbial communitiesin thermal acclimation ofSOM decomposition

Temperature Microbial biomasscarbon PLFA pro-file enzyme activi-ties

11 days

Lamparteret al [87]

Development of sandparticle wettabilityduring initial BGIformation

pH microbialactivity

C and N measure-ments contactangle determination

10 days

a SEMEDS scanning electron microscopyenergy dispersive spectroscopy

experiment by Heckman et al [81] represents a further simplified artificial soil studythat aimed at understanding the effect of minerals on soluble nutrient dynamics andthe composition of soil microbial communities (998835 Tab 92) After inoculation withits native microbial community forest floor material was incubated with goethiteand quartz or gibbsite and quartz The treatments with oxide surfaces exhibited adifferent microbiota as observed by pyrosequencing of 16S rRNA gene fragmentsamplified from total community-DNA and influenced nutrient content and physico-chemical properties of water-extractable OM compared to the control that receivedonly quartz sand However on a functional level (OM decomposition) no differenceswere observed [81 82] This corresponds to the findings of Pronk et al [80] and Vogelet 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




among different artificial soils might be biased by the detection limit of the methodused The more advanced analysis of microbial residues (an important componentof SOM) using amino sugars as indicator revealed differences among artificial soilswith different clayminerals present [83] These differences in OM turnover were likelycaused by the microbial community dynamics over the incubation time rather thanby direct interactions with the minerals [83] In a different artificial soil experimentlasting for only 2 months Wei et al [84] also observed an effect of clay content on theOM decomposition rate microbial biomass and microbial community composition(998835 Tab 92) Furthermore after several OM additions to matured artificial soils [54] dif-ferences in the decomposition rate of labeled litter and microbial biomass were alsoobserved between soils containing montmorillonite or illite which was explained bythe different structural development with ongoing soil formation This indicated OMstabilization in the fraction of smaller particle size [85] Additional insights into SOMdynamics originated from an artificial forest soil study byWei et al [86] In this studyartificial soilswere used to simulate the acclimation of SOMdecompositionunder 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 daysof preincubation) The authors were able to show that temperature-related shifts inthe 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 soilpercolation experiment conducted by Lamparter et al [87] In this study quartz sandof different sizes was percolated with a dissolved OM solution of varying pH and withor without the addition of sodium azide in order to analyze the effect of OM sorptionand microbial activity on particle wettability By measuring the solid-water contactangle at the three-phase boundary the authors suggested a microbial contribution toa reduction of surfacewettability which directly affects BGI formation [87] (998835 Tab 92)

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 thatestablished as a function of the soil composition to added compounds (998835 Tab 91998835Fig 93) This showed that microbial communities thriving in a nutrient-limitedenvironment with mainly recalcitrant organic compounds left [78] can still rapidlyrespond to changing conditions by the selection of specific phenanthrene or litterdegraders after incubation with these amendments [74ndash76] The response to phenan-threnewas observed although themicrobial communities that were used to inoculatethe 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 themicrobial communities increasingly diverged but a similar response to the additionof plant litter in terms of microbial guilds was observed in artificial soils matured for3 and 12 months Therefore the authors concluded that the alkane degrader commu-nity can be reactivated under favorable conditions [76] Altogether this supports the




Fig 93 Spiking experiment conducted by Babin et al [75] on artificial soils matured for more than2 years

idea of ldquoeverything is everywhere but the environment selectsrdquo and thus by artificialsoil studies new arguments can be brought into the ongoing debate of the ecologicalconcept [88] These artificial soil studies provide an explanation for the resilience ofsoil functions under changing environmental conditions by allowing the existence ofmicroorganisms with specific metabolic capacities at low densities

Various spiking experiments on differently matured artificial soils [74ndash76] further-more showed that the soil composition controlled the microbial response to spikesand therefore likely the functionality of established interfaces and microbial com-munities Less response of bacterial communities to phenanthrene was observed insoils containing charcoal and montmorillonite which was explained by the differentbioavailability of phenanthreneamongartificial soils [74 75 89] (998835 Fig 93) Bypyrose-quencing analysis of 16S rRNA gene fragments amplified from total community-DNAdiscriminative bacterial responders to phenanthrene and litter addition were identi-fied For instance an increase of sequences affiliated to the so far poorly describedgenus Kocuria in response to phenanthrene was found in all artificial soils except forthe montmorillonite mixture giving new insights into habitat preferences and ecolog-ical functions [79] The response of fungal communities to combined spikes of plantlitter 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 thetime factor as an additional parameter Hence it was observed that spiking of phenan-threne even increased the dissimilarity between bacterial communities from artificialsoils with different clay minerals present after more than 2 years of maturation [75]

The artificial soil experiments of the DFG Priority Program (998835 Tab 91) aimed atstudying 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 themineral composition is a crit-ical variable in determining the functionality and response of microbial communitiesHowever the underlying mechanisms and interactions still remain unclear As dis-




cussed above the response of microorganisms to soil components might be based onadirect surface interactionOtherwise itmightbean indirect consequenceof the incu-bation which allowed the reaction of soil components and thus interface formationand 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]

96 Artificial Soils for Arid Soil Research

More than one third of Earthrsquos land area is drylands Only animal and plant life formsthat are adapted to the extreme conditions (eg limited and pulsed nutrient inputlow OM content water deficiency temperature variation alkaline pH) can establishin arid soils [90] Most of the soil experiments are carried out with soils from mesicenvironments and therefore our knowledge of the biology of arid soils is still limitedDue to the differentwater regimes affectingmicrobial activity but also general interac-tions between SOM and minerals it is questionable to which extent information fromtemperate soils is also relevant for arid soils However the importance and ecologicalsignificance of arid soils that are regarded as especially vulnerable to the global cli-mate changewill likely rise in future [91] Itwas previously reported that arid soils offercertain heterogeneity due to eg nutrient depth stratification and patchy vegetationdistribution [90 91] However one might postulate that the complexity of arid soils isless compared to that of grassland forest or tropical soils due to the lower amounts ofwater and SOM (998835 Fig 91) Therefore artificial soils which are restricted in complex-ity aswell can be regarded as suitablemodel systems to studymicrobial communitiesandmicrobe-mediated processes in arid soils As mentioned above simplified soil ex-perimentswere already used to study the impact ofwater content onmicrobial interac-tions and community establishment [26 27] The artificial soils composed within theframework of the DFG Priority Program [53 54] did not focus on water as a parameterThese artificial soils were incubated at a constant water content of 60 of the waterholding capacity which likely did not trigger drought stress for most microorganismsFurthermore 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 differentproperties 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 microbialcommunity establishment in artificial soils during maturation For following studiesthe compositions of these artificial soils could be varied in order to specifically studythe 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 Giventhe appropriate experimental design incubation of artificial soils will also allow to



97 Concluding Remarks | 175

study the effect of EPS on soil structure and whether it contributes to water retentionor water repellency [23 92] These results would certainly provide new insights intothe role of microorganisms as soil architects

Due to their restricted complexity arid soils themselves could be regarded as asimplified soil model Thus concepts or hypotheses proposed based on results fromsimplified experimental designs (eg artificial soils) could be tested with arid soils

97 Concluding Remarks

A long-standing history and recent research results demonstrate that artificial soilshave become a well-established and useful tool to simulate processes in natural soilsand especially to understand microbial community establishment and functioningBy their controlled composition artificial soils exclude factors other than the factor ofinterest [7] and still provide conditions similar to natural soils Vogel et al [85] showedthat matured artificial soils exhibited similar OM dynamics as a natural soil Further-more the qualitative response of microbial communities that established in artificialsoils to spiked compounds was similar to that of natural soils [75 76] Due to theirreproducibility artificial soils with exact component specifications are established asa standard medium and reference material for ecotoxicological tests [93ndash95] The re-duced complexity of artificial soils however at the same time indicates their limita-tions Thismust bekept inmindbefore extrapolationof results tonatural soils [94] Forinstance in the case of the artificial soil studies of Pronk et al [53] andVogel 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 stronglyto 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 researchdiscipline 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 otherapproaches with the goal to model the nature in the lab (eg artificial intelligencebionics biotechnology) artificial soil research should aim to get back to nature Astep-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 orderto unravel the soil interaction network

Acknowledgment The authors acknowledge the Deutsche Forschungsgemeinschaft(DFG) for funding this work within the framework of the Priority Program SPP1315ldquoBiogeochemical Interfaces in Soilrdquo




References

[1] Stotzky G Influence of soil mineral colloids on metabolic processes growth adhesion andecology of microbes and viruses In Huang PM Schnitzer M (eds) Interactions of soil mineralswith natural organics and microbes ndash SSSA Special Publication 17 Madison WI USA SoilScience Society of America 1986 305ndash428

[2] Young IM Crawford JW Interactions and self-organization in the soil-microbe complex Science2004 3041634ndash7

[3] Vos M Wolf AB Jennings SJ Kowalchuk GA Micro-scale determinants of bacterial diversity insoil FEMS Microbiol Rev 2013 37936ndash54

[4] Schreiter S Ding GC Heuer H et al Effect of the soil type on the microbiome in the rhizo-sphere of field-grown lettuce Front Microbiol 2014 5144

[5] Schreiter S Ding GC Grosch R Kropf S Antweiler K Smalla K Soil type-dependent effects ofa potential biocontrol inoculant on indigenous bacterial communities in the rhizosphere offield-grown lettuce FEMS Microbiol Ecol 2014 90718ndash30

[6] Schreiter S Sandmann M Smalla K Grosch R Soil type dependent rhizosphere competenceand biocontrol of two bacterial inoculant strains and their effects on the rhizosphere microbialcommunity of field-grown lettuce Plos One 2014 9e103726

[7] Guenet B Leloup J Hartmann C Barot S Abbadie L A new protocol for an artificial soil to anal-yse soil microbiological processes Appl Soil Ecol 2011 48243ndash6

[8] Chenu C Stotzky G Interactions between Microorganisms and Soil Particles An OverviewIn Huang PM Bollag JM Senesi N (eds) Interactions between Soil Particles and Microorgan-isms ndash Impact on the Terrestrial Ecosystem IUPAC Series of Applied Chemistry West SussexEngland John Wiley amp Sons 2002 3ndash40

[9] Marshall KC Clay Mineralogy in Relation to Survival of Soil Bacteria Annu Rev Phytopathol1975 13357ndash73

[10] Filip Z Wechselwirkungen von Mikroorganismen und Tonmineralen ndash eine Uumlbersicht Z PflanzBodenkunde 1979 142375ndash86

[11] Stotzky G Soil as an Environment for Microbial Life In Van Elsas JD Trevors JT Wellington EM(eds) Modern Soil Microbiology New York NY USA Marcel Dekker 1997 1ndash20

[12] Ochiai N Dragila MI Parke JL Three-Dimensional Tracking of Colloids at the Pore Scale UsingEpifluorescence Microscopy Vadose Zone J 2010 9576ndash87

[13] Downie H Holden N Otten W Spiers AJ Valentine TA Dupuy LX Transparent Soil for Imagingthe Rhizosphere Plos One 2012 7e44276

[14] Wright DA Killham K Glover LA Prosser JI Role of Pore-Size Location in Determining BacterialActivity during Predation by Protozoa in Soil Appl Environ Microbiol 1995 613537ndash43

[15] Salonius PO Metabolic Capabilities of Forest Soil Microbial Populations with Reduced Species-Diversity Soil Biol Biochem 1981 131ndash10

[16] Nazir R Semenov AV Sarigul N Van Elsas JD Bacterial community establishment in native andnon-native soils and the effect of fungal colonization Microbiology Discovery 2013 11ndash8

[17] Delmont TO Francioli D Jacquesson S et al Microbial community development and unseendiversity recovery in inoculated sterile soil Biol Fert Soils 2014 501069ndash76

[18] Glossary of Soil Science Terms Madison WI USA Soil Science Society of America 2016 [cited24 Feb 2016] Available from httpswwwsoilsorgpublicationssoils-glossary

[19] Soil Composition and Formation South Carolina SCDNR Land Water and Conservation Divi-sion [cited 11 Oct 2014] Available from httpwwwnerrsnoaagovdocsiteprofileacebasinhtmlenvicondsoilslformhtm



References | 177

[20] Basile-Doelsch I Balesdent J Rose J Are Interactions between Organic Compounds andNanoscale Weathering Minerals the Key Drivers of Carbon Storage in Soils Environ Sci Technol2015 493997ndash8

[21] Churchman GJ Is the geological concept of clay minerals appropriate for soil science A litera-ture-based and philosophical analysis Phys Chem Earth 2010 35927ndash40

[22] Baldock JA Interactions of Organic Materials and Microorganisms with Minerals in the Stabi-lization of Soil Structure In Huang PM Bollag JM Senesi N (eds) Interactions between soilParticles and Microorganisms ndash Impact on the Terrestrial Ecosystem West Sussex EnglandJohn Wiley amp Sons 2002 85ndash132

[23] Or D Smets BF Wraith JM Dechesne A Friedman SP Physical constraints affecting bacte-rial habitats and activity in unsaturated porous media ndash a review Adv Water Resour 2007301505ndash27

[24] Young IM Crawford JW Nunan N Otten W Spiers A Donald LS Chapter 4 Microbial Distribu-tion in Soils Physics and Scaling In Sparks DL (ed) Advances in Agronomy San Diego CAUSA Academic Press 2008 81ndash121

[25] Carson JK Gonzalez-Quinones V Murphy DV Hinz C Shaw JA Gleeson DB Low pore connectiv-ity increases bacterial diversity in soil Appl Environ Microbiol 2010 763936ndash42

[26] Wolf AB Vos M de Boer W Kowalchuk GA Impact of Matric Potential and Pore Size Distribu-tion on Growth Dynamics of Filamentous and Non-Filamentous Soil Bacteria Plos One 20138e83661

[27] Treves DS Xia B Zhou J Tiedje JM A two-species test of the hypothesis that spatial isolationinfluences microbial diversity in soil Microb Ecol 2003 4520ndash8

[28] Tiedje JM Cho JC Murray A Treves D Xia B Zhou J Soil Teeming with Life New Frontiers forSoil Science In Rees RM Ball BC Campbell CD Watson CA (eds) Sustainable Management ofSoil Organic Matter Wallingford UK CAB International 2001 393ndash426

[29] Finlay RD Fungi in Soil In Van Elsas JD Jansson J Trevors JT (eds) Modern Soil Microbiology2nd edn Boca Raton FL USA CRC Press 2007

[30] Van Elsas JD Torsvik V Hartmann A Oslashvrearings L Jansson J The Bacteria and Archaea in Soil InVan Elsas JD Jansson J Trevors JT (eds) Modern Soil Microbiology 2nd edn Boca Raton FLUSA CRC Press 2007

[31] Totsche KU Rennert T Gerzabek MH et al Biogeochemical interfaces in soil The interdisci-plinary challenge for soil science J Plant Nutr Soil Sci 2010 17388ndash99

[32] Rahn O Bacterial activity in soil as a function of grain size and moisture content Mich Agr ExpSta Techn Bul 1912 16

[33] Stevens FL Withers WA Studies in Soil Bacteriology III Concerning methods for determina-tion of nitrifying and ammonifying powers Zentbl Bakteriolog P (II) 1910 2564ndash80

[34] Soumlhngen NL Einfluss von Kolloiden auf microbiologische Prozesse Zentbl Bakteriolog P (II)1913 38621ndash47

[35] Conn HJ The Most Abundant Groups of Bacteria in Soil Bacteriol Rev 1948 12257ndash73[36] Allen ER Bonazzi A On Nitrification I Preliminary Observations B Oh Agr Expt Sta 1915 71ndash

42[37] Loumlhnis F Green HH Methods in soil bacteriology VII Ammonification and nitrification in soil

and in solution Zentbl Bakteriolog P (II) 1914 40457[38] Fraps GS Studies in nitrification N Carolina Agr Expt Sta 1903 33ndash54[39] Conn HJ The microscopic study of bacteria and fungi in soil N Y State Agr Expt Sta Tech Bull

1918 643ndash20[40] Winogradsky S Eacutetudes sur la microbiologie du sol I Sur la meacutethode Ann Inst Pasteur 1925

39299ndash354




[41] Cholodny NG A soil chamber as a method for the microscopic study of the soil microflora ArchMikrobiol 1934 5148ndash56

[42] Madhok MR Synthetic Soil As A Medium for the Study of Certain Microbiological ProcessesSoil Sci 1937 44319ndash22

[43] Madhok MR Cellulose decomposition in synthetic and natural soils Soil Sci 1937 44385ndash98[44] Martin JP Waksman SA Influence of microorganisms on soil aggregation and erosion Soil Sci

1940 5029ndash47[45] Conn HJ Conn JE Synthetic soil as a bacteriological culture medium Soil Sci 1941 52121ndash36[46] Hallsworth EG Crawford DV Experimental Pedology Proceedings of the 11th Easter School in

Agricultural Science London UK Butterworths 1965[47] Bockheim JG Gennadiyev AN The value of controlled experiments in studying soil-forming

processes A review Geoderma 2009 152208ndash17[48] Hamdi YA Soil-water tension and the movement of rhizobia Soil Biol Biochem 1971 3121ndash6[49] Griffin DM Quail G Movement of Bacteria in Moist Particulate Systems Aust J Biol Sci 1968

21579ndash82[50] Wong PTW Griffin DM Bacterial Movement at High Matric Potentials 1 Artificial and Natural

Soils Soil Biol Biochem 1976 8215ndash8[51] Ellis RJ Artificial soil microcosms a tool for studying microbial autecology under controlled

conditions J Microbiol Methods 2004 56287ndash90[52] Zhang J Loynachan TE Raich JW Artificial soils to assess temperature sensitivity of the de-

composition of model organic compounds effects of chemical recalcitrance and clay-mineralcomposition Eur J Soil Sci 2011 62863ndash73

[53] Pronk GJ Heister K Ding G-C Smalla K Koumlgel-Knabner I Development of biogeochemicalinterfaces in an artificial soil incubation experiment aggregation and formation of organo-mineral associations Geoderma 2012 189ndash190585ndash94

[54] Vogel C Babin D Pronk GJ Heister K Smalla K Koumlgel-Knabner I Establishment of macro-ag-gregates and organic matter turnover by microbial communities in long-term incubated artifi-cial soils Soil Biol Biochem 2014 7957ndash67

[55] Amann RI Ludwig W Schleifer KH Phylogenetic Identification and In Situ Detection of Individ-ual Microbial Cells without Cultivation Microbiol Rev 1995 59143ndash69

[56] Smalla K Van Elsas JD The soil environment In Liu WT Jansson JK (eds) EnvironmentalMolecular Microbiology Norfolk UK Caister Academic Press 2010 111ndash30

[57] Woese CR Bacterial Evolution Microbiol Rev 1987 51221ndash71[58] Quast C Pruesse E Yilmaz P et al The SILVA ribosomal RNA gene database project improved

data processing and web-based tools Nucleic Acids Res 2013 41D590ndash6[59] Anderson IC Cairney JWG Diversity and ecology of soil fungal communities increased under-

standing through the application of molecular techniques Environ Microbiol 2004 6769ndash79[60] Frostegaringrd A Baringaringth E The use of phospholipid fatty acid analysis to estimate bacterial and

fungal biomass in soil Biol Fert Soils 1996 2259ndash65[61] Smalla K Oros-Sichler M Milling A et al Bacterial diversity of soils assessed by DGGE T-RFLP

and SSCP fingerprints of PCR-amplified 16S rRNA gene fragments Do the different methodsprovide similar results J Microbiol Methods 2007 69470ndash9

[62] Torsvik V Oslashvrearings L Microbial diversity and function in soil from genes to ecosystems CurrOpin Microbiol 2002 5240ndash5

[63] Nannipieri P Giagnoni L Renella G et al Soil enzymology classical and molecular ap-proaches Biol Fert Soils 2012 48743ndash62

[64] Raynaud X Nunan N Spatial Ecology of Bacteria at the Microscale in Soil Plos One 20149e87217



References | 179

[65] Hemkemeyer M Christensen BT Martens R Tebbe CC Soil particle size fractions harbour dis-tinct microbial communities and differ in potential for microbial mineralisation of organic pol-lutants Soil Biol Biochem 2015 90255ndash65

[66] Jocteur Monrozier L Ladd JN Fitzpatrick RW Foster RC Raupach M Components and MicrobialBiomass Content of Size Fractions in Soils of Contrasting Aggregation Geoderma 1991 5037ndash62

[67] Sessitsch A Weilharter A Gerzabek MH Kirchmann H Kandeler E Microbial population struc-tures in soil particle size fractions of a long-term fertilizer field experiment Appl Environ Micro-biol 2001 674215ndash24

[68] Neumann D Heuer A Hemkemeyer M Martens R Tebbe CC Response of microbial commu-nities to long-term fertilization depends on their microhabitat FEMS Microbiol Ecol 20138671ndash84

[69] Herrmann AM Ritz K Nunan N et al Nano-scale secondary ion mass spectrometry ndash A newanalytical tool in biogeochemistry and soil ecology A review article Soil Biol Biochem 2007391835ndash50

[70] Heister K Houmlschen C Pronk GJ Mueller CW Koumlgel-Knabner I NanoSIMS as a tool for charac-terizing soil model compounds and organomineral associations in artificial soils J Soils Sed2012 1235ndash47

[71] Ding GC Pronk GJ Babin D et al Mineral composition and charcoal determine the bacterialcommunity structure in artificial soils FEMS Microbiol Ecol 2013 8615ndash25

[72] Filip Z Clay Minerals as a Factor Influencing Biochemical Activity of Soil Microorganisms FoliaMicrobiol 1973 1856ndash74

[73] Uroz S Kelly LC Turpault MP Lepleux C Frey-Klett P The Mineralosphere Concept Mineralog-ical Control of the Distribution and Function of Mineral-associated Bacterial CommunitiesTrends Microbiol 2015 23751ndash62

[74] Babin D Ding GC Pronk GJ Heister K Koumlgel-Knabner I Smalla K Metal oxides clay mineralsand charcoal determine the composition of microbial communities in matured artificial soilsand their response to phenanthrene FEMS Microbiol Ecol 2013 863ndash14

[75] Babin D Vogel C Zuumlhlke S et al Soil Mineral Composition Matters Response of MicrobialCommunities to Phenanthrene and Plant Litter Addition in Long-Term Matured Artificial SoilsPlos One 2014 9e106865

[76] Steinbach A Schulz S Giebler J et al Clay minerals and metal oxides strongly influence thestructure of alkane-degrading microbial communities during soil maturation ISME J 201591687ndash91

[77] Hemkemeyer M Pronk GJ Heister K Koumlgel-Knabner I Martens R Tebbe CC Artificial soil stud-ies reveal domain-specific preferences of microorganisms for the colonisation of different soilminerals and particle size fractions FEMS Microbiol Ecol 2014 90770ndash82

[78] Ditterich F Poll C Pronk GJ et al Succession of soil microbial communities and enzyme activi-ties in artificial soils Pedobiologia 2016 5993ndash104

[79] Babin D Ding GC Vogel C et al Pyrosequencing-based analysis of matured artificial soilsreveals the driving influence of the soil composition on the response of bacterial communitiesto added phenanthrene and litter In preparation

[80] Pronk GJ Heister K Koumlgel-Knabner I Is turnover and development of organic matter controlledby mineral composition Soil Biol Biochem 2013 67235ndash44

[81] Heckman K Welty-Bernard A Vazquez-Ortega A Schwartz E Chorover J Rasmussen C Theinfluence of goethite and gibbsite on soluble nutrient dynamics and microbial community com-position Biogeochemistry 2013 112179ndash95




[82] Heckman K Vazquez-Ortega A Gao XD Chorover J Rasmussen C Changes in water extractableorganic matter during incubation of forest floor material in the presence of quartz goethiteand gibbsite surfaces Geochim Cosmochim Acta 2011 754295ndash309

[83] Pronk GJ Heister K Koumlgel-Knabner I Amino sugars reflect microbial residues as affected byclay mineral composition of artificial soils Org Geochem 2015 83ndash84109ndash13

[84] Wei H Guenet B Vicca S et al High clay content accelerates the decomposition of fresh or-ganic matter in artificial soils Soil Biol Biochem 2014 77100ndash8

[85] Vogel C Heister K Buegger F et al Clay mineral composition modifies decomposition andsequestration of organic carbon and nitrogen in fine soil fractions Biol Fert Soils 201551427ndash42

[86] Wei H Guenet B Vicca S et al Thermal acclimation of organic matter decomposition in anartificial forest soil is related to shifts in microbial community structure Soil Biol Biochem2014 711ndash12

[87] Lamparter A Bachmann J Woche SK Goebel MO Biogeochemical Interface Formation Wet-tability Affected by Organic Matter Sorption and Microbial Activity Vadose Zone J 201413doi102136vzj2013100175

[88] OrsquoMalley MA lsquoEverything is everywhere but the environment selectsrsquo ubiquitous distributionand ecological determinism in microbial biogeography Studies in History and Philosophy ofScience Part C Studies in History and Philosophy of Biological and Biomedical Sciences 200839314ndash25

[89] Pronk GJ Heister K Vogel C et al Interaction of minerals organic matter and microorganismsduring biogeochemical interface formation as shown by a series of artificial soil experimentsBiol Fertil Soils 2017 539ndash22


[91] Collins SL Sinsabaugh RL Crenshaw C et al Pulse dynamics and microbial processes in arid-land ecosystems J Ecol 2008 96413ndash20

[92] Or D Phutane S Dechesne A Extracellular polymeric substances affecting pore-scale hydro-logic conditions for bacterial activity in unsaturated soils Vadose Zone J 2007 6298ndash305

[93] OECD Test No 207 Earthworm Acute Toxicity Tests OECD Publishing 1984[94] Hofman J Rhodes A Semple KT Fate and behaviour of phenanthrene in the natural and artifi-

cial soils Environ Pollut 2008 152468ndash75[95] OECD Test No 222 Earthworm Reproduction Test (Eisenia fetidaEisenia andrei) OECD Pub-

lishing 2004[96] Heckman K Grandy AS Gao X et al Sorptive fractionation of organic matter and formation of

organo-hydroxy-aluminum complexes during litter biodegradation in the presence of gibbsiteGeochim Cosmochim Acta 2013 121667ndash83



Index16S rRNA gene 165 167 169

Aactivity 15 17 19 21 22 25ndash29Aflatoxin 114Agaricomycetes 102 105agricultural use 17algae 100Alternaria 100 106 107 113AMF 103 see arbuscular mycorrhizal fungiarbuscular mycorrhizal fungi 103 104arid soil 160 174arid zone 1arthrospores 112Ascomycota 97 100 103 105 109Aspergillus 114

BBasidiomycota 102 103 105 106biocrusts 5 6 73ndash75 78 80 82ndash88 95ndash97

100 108 109biodiversity 18biogeochemical interfaces (BGIs) 161biological soil crusts 41 see biocrusts BSCBlastomycotina 103bryophytesndash definition 73Bryum argenteum 125BSC 123ndash127 129ndash134

CCaatinga 107calcium carbonate 80 82carbon monoxide see COcarbon sequestration 15 16 18 19 23 24 26cellulose 21charcoal 161 163 166ndash170 173chasmolithic 3Chihuahuan desert 102chlorophyll 124 125 131 136 137Chytridiomycota 103Cladonia convoluta 133clay minerals 159 161 163 167 168 172 173climate change 17 18 21 24 25CO 31 38ndash40 42 44 45CO2 123 125ndash129 132 134ndash136Coccidioides 112

Coccidioidomycosis see CoccidioidesCollema cristatum 125colonization 106connectivity 161 169 171contamination 21Coprophilous fungi 106crusts 20cultivation 162 165Curvularia 107cyanobacteria 20 97

DD rigidulus 131dark respiration 126dark septate fungi 97dermatophytes 112Desert 97desertification 15 17 18 24 25DGGE 165 167 170Diploschistes diacapsis 125diversity 21 159 161 165 166 168ndash170 175β-diversity 75 78ndash81 84ndash87 89Dothideomycetes 102droughts 15 17 22Drylands 15dust storms 111

Eecosystem functioning 83ectomycorrhizal 104endemic 112endolithic 3endophytes 103 106 107enzyme activity 21eumycetoma 113Eurotiomycetes 102evapotranspiration 1evenness 81 84ndash87 96experimental pedology 163extracellular enzymes 21extracellular polymeric substances (EPS) 111

161Extremophiles 108

Ffertility 15 18 19 23 24 26functional redundancy 88 96 169



182 | Index

functional traits 87fungal network 102fungi 97Fusarium 113

Gglobal change 15 16 24Global diversity and characteristic taxa 77Glomerales see GlomeromycotaGlomeromycota 104glucose 19glycosidases 22Gram positive 21grasses 106grassland 103 104 109Grimmia laevigata 125gypsophiles 81gypsum 105 107

Hheterogeneity 159 163 174humic acids 17humic substances 18 21hyperarid zone 1hyphae 97hypolithic 3

Iimmunocompromised 112incubation 159 162 163 167 168 170 172 174inoculant 162 166 169internal transcribed spacer (ITS) 165islands of fertility 3

Kkeratinolytic 112

Lland degradation 15land use 16 17 20leaf mass per area 125Lecanora muralis 133lichen 99 102lichensndash definition 74lignin 21 27litter 167 170 172 173Lobaria pulmonaria 125Lobaria scrobicularia 125

Mmatric potential 33ndash37 43maximal net photosynthetic see NPmaxmelanin 107 111metagenomic 103metal oxides 161 163 167Methane 37 38 44methanotroph 36 38microbial activity 15 21 24 26 28microbial biomass 16 17 19ndash22 25 28microbial communities 15 16 25 27microbial ecology 159 160 164 165 171 175microbiota 159 161 164 168 171Microcoleus vaginatus 100microcolonies 109microcosm 160 163microenvironments 97 103microsclerotia 107mineralization 16 20 24 25mitosporic 97moisture 17 18 20ndash22 28Mortierellales 102Mortierellomycotina 103moss 100Mucoromycotina 103multifunctionality 87mycetoma 114Mycohetetrophic 105mycorrhiza 103mycosis 113Mycotoxins 114

NN deposition 108NanoSIMS 166nitrous oxide 40NPmax 124 125 128 129nutrient cycling 82ndash84 87

OOnygenaceae 112organic amendments 15 19 21 24 26 28organic carbon 2 15ndash20 24 25organic matter 15ndash21 23ndash28osmoconformers 36

PP decipiens 131Paraphaeosphaeria 107



Index | 183

particle size fractionation 166 167pathogen 97 106 111pH 21 80 89phenanthrene 170 172 173phenol oxidases 21Phoma 100photodegradation 15 17 18 26photosynthetic photon flux density 126Physcomitrella patens 127 136 137plant cover 15 18 26plant pathogens 102PLFA 19 21 27 165 170 171poikilohydric 123 130 131 134 136porous media 159 163PPFD 126 127 131 132 135 see PPFDprecipitation 16 22 140productivity 15 18 24Pseudocyphellaria crocata 125Pseudocyphellaria dissimilis 125pyrosequencing 165 167ndash171 173

Qquantitative real-time PCR (qPCR) 165

Rrespiration 17 25rhizosphere 97 100 102 103rock varnish 109

Ssemiarid zone 2shrubs 18soil erosion 19

soil formation 168 172 175soil microorganisms 17soil restoration 15 16 23 26 27solute potential 36SOM 15ndash17 19 20 22Sordariomycetes 102species richness 79 81 83 84 87ndash89 96specificity 106spiking 173 174stable isotope probing 19sustainability 16 24synthetic soil 162Syntrichia caninervis 125

TTensiometer 34Thallus water content 127thermotolerance 107T-RFLP 165 170truffles 105

Wwarming 16water 159ndash161 163 166 169 171 172 174water availability 15 17 19water potential 2 31ndash41 43 45

Xxerophilic 114

Yyeast 108





the_biol_of_arid_soils_front_cover

The _Biol_arid_soils _frontmatter_ppI-IV

The _Biol_arid_soils _preface_ppV-VI

The _Biol_arid_soils _contents_ppVII-X

The _Biol_arid_soils _authors_ppXI-XIV

The_Biol_arid_soils_chapter_1-intro_pp1-14

The _Biol_arid_soils _chapter_2_soils_pp15-30

The _Biol_arid_soils _chapter_3_water_potential_pp31-46

The _Biol_arid_soils _chapter_4_microbiol_antarctic_pp47-72

The _Biol_arid_soils _chapter_5_bryos_lichens_pp73-96

The _Biol_arid_soils _chapter_6_fungi_pp97-122

The _Biol_arid_soils _chapter_7_limits_of_photosynthesis_pp123-138

The _Biol_arid_soils _chapter_8_the_response_of_communities_pp139-158

The _Biol_arid_soils _chapter_9_artif_soils_as_tools_for_microb_ecol_pp159-180

The _Biol_arid_soils _chapter_10_index_pp181-184

the_biol_of_arid_soils_back_cover

Life in Extreme Environments

|Edited byDirk Wagner

Volume 4



|







wwwdegruytercom


Preface




Blaire Steven








Contents

Preface | V











VIII | Contents









Contents | IX










X | Contents



Index | 181














































(a) (b) (c)


DOI 1015159783110419047-001




















Root

sBi

ocru

sts


Shar

ed

Root

sBi

ocru

sts

Shar

ed

25 20 051015 5 10 30 20 2010010 30 40 50 60










17 Summary | 7






17 Summary




References




















References | 9













































References | 11










































References | 13
















21 Introduction



DOI 1015159783110419047-002































































27 Conclusion | 23





27 Conclusion













References







References | 25













































References | 27















































References | 29


















31 Introduction




DOI 1015159783110419047-003










Nw = nw(nw + ni)


aw = γNw












ψ = RT ln awVw + P








































ndash10(a) (b)

0030 00 ndash100

ndash080

ndash060

ndash040

ndash020

000

05

10

15

20

25

30

0035

0040

0045

0050

0055

0060

ndash080 ndash060


Met

hane

upt

ake

rate

cons

tant

(hndash1

gdw

ndash1)

Met

hane

upt

ake

rate

(nm

ol g

dwndash1

hndash1 )

Wat

er p

oten

tial (

MPa

)

ndash040 ndash020 00 15 20 25 30 35 40















00


100

150

200

250

300

5 10Time (h)

Core

hea

dspa

ce C

O (p

pb)

15 20 25






35 Conclusions | 41





35 Conclusions






References


















References | 43

















































References | 45























and Lithic Habitats

41 Introduction





DOI 1015159783110419047-004







(a) (b)














































(a) (b)

(c) (d)






441 Hypoliths











442 Epiliths







443 Endoliths







Hypolith

(a) (b) (c)

Endolith Open soil




































Aquificae








Chloroflexi



Plactomycetes


Verrumicrobia

















References



















References | 65


















































References | 67














































References | 69
















































References | 71






































51 Overview





DOI 1015159783110419047-005












0

AsiaAfric

aNorth

America

South

America

Antarctica

EuropePacifi

c


50

100

150

20033

579

000

km2

305

215

32 km

2

247

090

00 km

2

178

400

00 km

2

140

000

00 km

2

1018

000

0 km

2

7960

000

km2

250


Spec

ies n

umbe

r










Species Asia

Afric

a

N-Am

eric

a1

S-Am

eric

a

Anta

rctic

a

Euro

pe

Paci

fic2












































Species Asia

Afric

a

N-Am

eric

a1

S-Am

eric

a

Anta

rctic

a

Euro

pe

Paci

fic2



















0

(a) (b)

Spec

ies n

umbe

r

100

200


LiverwortsMosses

300

400

0

Spec

ies n

umbe

r

100

50

150

200

250

1 geogr r

egion

2 geogr regions

3 geogr regions

4 geogr regions

5 geogr regions

6 geogr regions

All regions

1 geogr r

egion

2 geogr regions

3 geogr regions

4 geogr regions

5 geogr regions

6 geogr regions

All regions


































































Dataset αdi

vers

ity

po

sitiv

e

even

ness

po

sitiv

e

βdi

vers

ity

Function indicators
























Dataset αdi

vers

ity

po

sitiv

e

even

ness

po

sitiv

e

βdi

vers

ity

Function indicators











Mean 507 686 261 650 663Frequency 846 909 500 800 1000




























References























References | 91













































References | 93











































References | 95



















































DOI 1015159783110419047-006




(a) (b)

(c) (d)

(e)

(f) (g)





(a) (b)

(c) (d)

(e) (f)






611 Biocrusts






(25 OTUs)







PhallalesOnygenales

20 40 60 80 100


Unclassified Fungi


Rare Ascomycota

Dothideomycetes

Chytriomycota

Basidiomycota

A Sand crusts

108 121

402225

242139

50(37)

(36)109

100

80

60

40

20

Perc

ent o

f sha

red

OTUs

0


(41)

88 79 Sand

210 107

317 243

136

Shale46

1218

81245

41(52) (52)

(66) (56)

(54)

83








































































































643 Eumycetoma







644 Mycotoxins





References | 115





References































References | 117













































References | 119





















































References | 121























1999 21115ndash20















71 Introduction



DOI 1015159783110419047-007











Darkrespiration

Quantumefficiency

Chlorophyll


















0ndash20 ndash60


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Light compensation


1000 1200 0 10 20 30 40 50
















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Nov

Dec

Jan

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Mar Ap

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Aug

Sep

Oct











744 Catastrophes










76 Summary




References | 135


References



































References | 137





























to Climate Change

81 Overview



DOI 1015159783110419047-008


































































Soil

moi

stur

eTime rarr

Precipitationevent

Precipitationevent

Soil

moi

stur

e

Time rarr(a) (b)



Net carbon uptake

Carbon deficit

Carbon deficit



Net carbon uptake









86 Conclusion




References | 151




References





























References | 153












































References | 155


















































References | 157




































91 Introduction



DOI 1015159783110419047-009













92 Soil Definition
































































Tabl

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Wolf et al[26]




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5 10 2030 60 90154 days

Wei et al[84]




2 months

Wei et al[86]



11 days

Lamparteret al [87]




10 days



































References






















References | 177




















39299ndash354




























References | 179


















































182 | Index





Kkeratinolytic 112








Index | 183








Xxerophilic 114

Yyeast 108






















|







wwwdegruytercom


Preface




Blaire Steven








Contents

Preface | V











VIII | Contents









Contents | IX










X | Contents



Index | 181














































(a) (b) (c)


DOI 1015159783110419047-001




















Root

sBi

ocru

sts


Shar

ed

Root

sBi

ocru

sts

Shar

ed

25 20 051015 5 10 30 20 2010010 30 40 50 60










17 Summary | 7






17 Summary




References




















References | 9













































References | 11










































References | 13
















21 Introduction



DOI 1015159783110419047-002































































27 Conclusion | 23





27 Conclusion













References







References | 25













































References | 27















































References | 29


















31 Introduction




DOI 1015159783110419047-003










Nw = nw(nw + ni)


aw = γNw












ψ = RT ln awVw + P








































ndash10(a) (b)

0030 00 ndash100

ndash080

ndash060

ndash040

ndash020

000

05

10

15

20

25

30

0035

0040

0045

0050

0055

0060

ndash080 ndash060


Met

hane

upt

ake

rate

cons

tant

(hndash1

gdw

ndash1)

Met

hane

upt

ake

rate

(nm

ol g

dwndash1

hndash1 )

Wat

er p

oten

tial (

MPa

)

ndash040 ndash020 00 15 20 25 30 35 40















00


100

150

200

250

300

5 10Time (h)

Core

hea

dspa

ce C

O (p

pb)

15 20 25






35 Conclusions | 41





35 Conclusions






References


















References | 43

















































References | 45























and Lithic Habitats

41 Introduction





DOI 1015159783110419047-004







(a) (b)














































(a) (b)

(c) (d)






441 Hypoliths











442 Epiliths







443 Endoliths







Hypolith

(a) (b) (c)

Endolith Open soil




































Aquificae








Chloroflexi



Plactomycetes


Verrumicrobia

















References



















References | 65


















































References | 67














































References | 69
















































References | 71






































51 Overview





DOI 1015159783110419047-005












0

AsiaAfric

aNorth

America

South

America

Antarctica

EuropePacifi

c


50

100

150

20033

579

000

km2

305

215

32 km

2

247

090

00 km

2

178

400

00 km

2

140

000

00 km

2

1018

000

0 km

2

7960

000

km2

250


Spec

ies n

umbe

r










Species Asia

Afric

a

N-Am

eric

a1

S-Am

eric

a

Anta

rctic

a

Euro

pe

Paci

fic2












































Species Asia

Afric

a

N-Am

eric

a1

S-Am

eric

a

Anta

rctic

a

Euro

pe

Paci

fic2



















0

(a) (b)

Spec

ies n

umbe

r

100

200


LiverwortsMosses

300

400

0

Spec

ies n

umbe

r

100

50

150

200

250

1 geogr r

egion

2 geogr regions

3 geogr regions

4 geogr regions

5 geogr regions

6 geogr regions

All regions

1 geogr r

egion

2 geogr regions

3 geogr regions

4 geogr regions

5 geogr regions

6 geogr regions

All regions


































































Dataset αdi

vers

ity

po

sitiv

e

even

ness

po

sitiv

e

βdi

vers

ity

Function indicators
























Dataset αdi

vers

ity

po

sitiv

e

even

ness

po

sitiv

e

βdi

vers

ity

Function indicators











Mean 507 686 261 650 663Frequency 846 909 500 800 1000




























References























References | 91













































References | 93











































References | 95



















































DOI 1015159783110419047-006




(a) (b)

(c) (d)

(e)

(f) (g)





(a) (b)

(c) (d)

(e) (f)






611 Biocrusts






(25 OTUs)







PhallalesOnygenales

20 40 60 80 100


Unclassified Fungi


Rare Ascomycota

Dothideomycetes

Chytriomycota

Basidiomycota

A Sand crusts

108 121

402225

242139

50(37)

(36)109

100

80

60

40

20

Perc

ent o

f sha

red

OTUs

0


(41)

88 79 Sand

210 107

317 243

136

Shale46

1218

81245

41(52) (52)

(66) (56)

(54)

83








































































































643 Eumycetoma







644 Mycotoxins





References | 115





References































References | 117













































References | 119





















































References | 121























1999 21115ndash20















71 Introduction



DOI 1015159783110419047-007











Darkrespiration

Quantumefficiency

Chlorophyll


















0ndash20 ndash60


ndash20

00

20

40

60

80

ndash10

00

10

20

30

40


Net p

hoto

synt

hesi

s (μm

ol C

O 2 mndash2

sndash1)

CO2 ex

chan

ge ndash

μm

ol m

ndash2 sndash1

Light saturation

5degC

10degC


Light compensation


1000 1200 0 10 20 30 40 50
















PPFD tosaturateNP

PPFD com-pensation

OptimalWC for NP

MaximalWC



mm rainequivalent




Net p

hoto

synt

hesi

s ( μ

mol

mndash2

sndash1)

Num

ber o

f rai

nfal

l eve

nts

00

5

10

15

1 2 3 4ndash1

0

1

2

3
















0

(a) (b)

(c) (d)

Num

ber o

f dat

a po

ints

200400600800

1000120014001600

0

Num

ber o

f dat

a po

ints

200

400

600

800

1000

00 200 400 600 800 1000

200400600800



00 10 20


0 10 20Temperature


0 500 1000 1500 2000 2500 3000


Num

ber o

f dat

a po

ints

200400600800

1000120014001600

0

Num

ber o

f dat

a po

ints

200

400

600

800

1000

00 200 400 600 800 1000

200400600800













Sep

0 0

20

40

60

80

100

2012(a) (b)

2013

0

lt0 lt10 lt20 lt30


Temperature (degC)

lt1500 lt2000

Month

20

4000051015

Light

dar

k rat

io

Prop

ortio

n of

tim

e act

ive (

)

Cum

ulat

ive ti

me a

ctive

()

60

80

Oct

Nov

Dec

Jan

Feb

Mar Ap

rM

ay Jun Jul

Aug

Sep

Oct











744 Catastrophes










76 Summary




References | 135


References



































References | 137





























to Climate Change

81 Overview



DOI 1015159783110419047-008


































































Soil

moi

stur

eTime rarr

Precipitationevent

Precipitationevent

Soil

moi

stur

e

Time rarr(a) (b)



Net carbon uptake

Carbon deficit

Carbon deficit



Net carbon uptake









86 Conclusion




References | 151




References





























References | 153












































References | 155


















































References | 157




































91 Introduction



DOI 1015159783110419047-009













92 Soil Definition
































































Tabl

e9

1Ar

tifici

also

ilst

udie

sw

ithin

the

fram

ewor

kof

the

DFG

Prio

rity

Prog

ram

onBi

ogeo

chem

ical

Inte

rface

sin

Soil

(SPP

1315

)foc

usin

gon

soil

mic

robi

alco

mm

uniti

es

Publ

icat

ion

Aim

ofSt

udy

Fact

or(s

)ofV

aria

nce

Dete

ctio

nM

etho

dsIn

cuba

tion

Tim

eFu

rthe

rInf

orm

atio

non

Artifi

cial

Soils

Voge

leta

l[5

4]In

terd

isci

plin

ary

stud

yof

mic

robi

alco

mm

uniti

esO

Mde

com

posi

tion

and

soil

stru

ctur

ede

velo

pmen

tatm

atur

edBG

Is

Soil

min

eral

com

po-

sitio

nan

dpr

esen

ceof

char

coal

DGGE

qPC

Rfra

c-tio

natio

nOM

char

-ac

teriz

atio

n

842

days

(with

addi

tiona

lOM

inpu

taf

ter5

62da

ys)

Voge

leta

l[5

4]

Ding

etal

[7

1]Ea

rlyes

tabl

ishm

ento

fsoi

lbac

teria

lco

mm

uniti

esat

youn

gBG

IsSo

ilm

iner

alco

mpo

-si

tion

and

pres

ence

ofch

arco

al

16S

DGGE

pyr

ose-

quen

cing

19

319

0da

ysPr

onk

etal

[53

]

Babi

net

al

[74]

Deve

lopm

ento

fsoi

lmic

robi

alco

mm

uniti

esan

dre

spon

seto

phen

anth

rene

atm

atur

edBG

Is

Soil

min

eral

com

po-

sitio

nan

dpr

esen

ceof

char

coal

16S

ITS

DGGE

So

uthe

rnBl

ot-

hybr

idiz

atio

nfo

rca

tabo

licge

nes

1ye

ar+

70da

ysph

enan

thre

nePr

onk

etal

[53

]

Babi

net

al

[75]

Deve

lopm

ento

fsoi

lmic

robi

alco

mm

uniti

esan

dre

spon

seto

phen

anth

rene

atlo

ng-te

rmm

atur

edBG

Is

Soil

min

eral

com

po-

sitio

nan

dpr

esen

ceof

char

coal

16S

ITS

DGGE

qP

CRp

yros

eque

nc-

ing

842

days

+72

163

days

phen

anth

rene

+-p

lant

litte

r

Voge

leta

l[5

4]

Stei

nbac

het

al[

76]

Esta

blis

hmen

toff

unct

iona

lsoi

lmic

robi

algu

ilds

over

mat

urat

ion

time

(her

eal

kane

degr

adat

ion)

Soil

min

eral

com

po-

sitio

nan

dpr

esen

ceof

char

coal

qPCR

T-R

FLP

3m

onth

s12

mon

ths

(eac

h+

2w

eeks

plan

tlit

ter)

Pron

ket

al[

53]

Hem

kem

eyer

etal

[77

]Es

tabl

ishm

ento

fsoi

lmic

robi

aldi

vers

ityin

part

icle

size

fract

ions

over

mat

urat

ion

time

Soil

min

eral

com

po-

sitio

nqP

CRT

-RFL

Pfra

c-tio

natio

n6

mon

ths

18m

onth

sPr

onk

etal

[53

]

Ditte

rich

etal

[78

]M

icro

bial

colo

niza

tion

ofso

ilm

iner

als

and

succ

essi

onov

erm

atur

atio

ntim

eSo

ilm

iner

alco

mpo

-si

tion

qPCR

PLF

Aen

zym

eac

tivity

36

121

8m

onth

sPr

onk

etal

[53

]

Pron

ket

al

[80

83]

Unde

rsta

ndin

gOM

turn

over

and

deve

lopm

ent

over

soil

incu

batio

ntim

eSo

ilm

iner

alco

mpo

-si

tion

and

pres

ence

ofch

arco

al

OMch

arac

teriz

a-tio

nfra

ctio

natio

n3

612

18

mon

ths

Pron

ket

al[

54]

Voge

leta

l[8

5]Un

ders

tand

ing

OMtu

rnov

eran

dfo

rmat

ion

ofor

gano

-min

eral

asso

ciat

ions

atlo

ng-te

rmm

atur

edBG

Is

Soil

min

eral

com

po-

sitio

nan

dpr

esen

ceof

char

coal

Fum

igat

ion-

extra

c-tio

nOM

char

acte

ri-za

tion

fract

iona

tion

842

days

+63

days

13C

15N

labe

led

plan

tlitt

er

Voge

leta

l[5

4]







Wolf et al[26]




12 days

Treves et al[27]


Moisture con-tent


Heckmanet al [8196]



5 10 2030 60 90154 days

Wei et al[84]




2 months

Wei et al[86]



11 days

Lamparteret al [87]




10 days



































References






















References | 177




















39299ndash354




























References | 179


















































182 | Index





Kkeratinolytic 112








Index | 183








Xxerophilic 114

Yyeast 108


























wwwdegruytercom


Preface




Blaire Steven








Contents

Preface | V











VIII | Contents









Contents | IX










X | Contents



Index | 181














































(a) (b) (c)


DOI 1015159783110419047-001




















Root

sBi

ocru

sts


Shar

ed

Root

sBi

ocru

sts

Shar

ed

25 20 051015 5 10 30 20 2010010 30 40 50 60










17 Summary | 7






17 Summary




References




















References | 9













































References | 11










































References | 13
















21 Introduction



DOI 1015159783110419047-002































































27 Conclusion | 23





27 Conclusion













References







References | 25













































References | 27















































References | 29


















31 Introduction




DOI 1015159783110419047-003










Nw = nw(nw + ni)


aw = γNw












ψ = RT ln awVw + P








































ndash10(a) (b)

0030 00 ndash100

ndash080

ndash060

ndash040

ndash020

000

05

10

15

20

25

30

0035

0040

0045

0050

0055

0060

ndash080 ndash060


Met

hane

upt

ake

rate

cons

tant

(hndash1

gdw

ndash1)

Met

hane

upt

ake

rate

(nm

ol g

dwndash1

hndash1 )

Wat

er p

oten

tial (

MPa

)

ndash040 ndash020 00 15 20 25 30 35 40















00


100

150

200

250

300

5 10Time (h)

Core

hea

dspa

ce C

O (p

pb)

15 20 25






35 Conclusions | 41





35 Conclusions






References


















References | 43

















































References | 45























and Lithic Habitats

41 Introduction





DOI 1015159783110419047-004







(a) (b)














































(a) (b)

(c) (d)






441 Hypoliths











442 Epiliths







443 Endoliths







Hypolith

(a) (b) (c)

Endolith Open soil




































Aquificae








Chloroflexi



Plactomycetes


Verrumicrobia

















References



















References | 65


















































References | 67














































References | 69
















































References | 71






































51 Overview





DOI 1015159783110419047-005












0

AsiaAfric

aNorth

America

South

America

Antarctica

EuropePacifi

c


50

100

150

20033

579

000

km2

305

215

32 km

2

247

090

00 km

2

178

400

00 km

2

140

000

00 km

2

1018

000

0 km

2

7960

000

km2

250


Spec

ies n

umbe

r










Species Asia

Afric

a

N-Am

eric

a1

S-Am

eric

a

Anta

rctic

a

Euro

pe

Paci

fic2












































Species Asia

Afric

a

N-Am

eric

a1

S-Am

eric

a

Anta

rctic

a

Euro

pe

Paci

fic2



















0

(a) (b)

Spec

ies n

umbe

r

100

200


LiverwortsMosses

300

400

0

Spec

ies n

umbe

r

100

50

150

200

250

1 geogr r

egion

2 geogr regions

3 geogr regions

4 geogr regions

5 geogr regions

6 geogr regions

All regions

1 geogr r

egion

2 geogr regions

3 geogr regions

4 geogr regions

5 geogr regions

6 geogr regions

All regions


































































Dataset αdi

vers

ity

po

sitiv

e

even

ness

po

sitiv

e

βdi

vers

ity

Function indicators
























Dataset αdi

vers

ity

po

sitiv

e

even

ness

po

sitiv

e

βdi

vers

ity

Function indicators











Mean 507 686 261 650 663Frequency 846 909 500 800 1000




























References























References | 91













































References | 93











































References | 95



















































DOI 1015159783110419047-006




(a) (b)

(c) (d)

(e)

(f) (g)





(a) (b)

(c) (d)

(e) (f)






611 Biocrusts






(25 OTUs)







PhallalesOnygenales

20 40 60 80 100


Unclassified Fungi


Rare Ascomycota

Dothideomycetes

Chytriomycota

Basidiomycota

A Sand crusts

108 121

402225

242139

50(37)

(36)109

100

80

60

40

20

Perc

ent o

f sha

red

OTUs

0


(41)

88 79 Sand

210 107

317 243

136

Shale46

1218

81245

41(52) (52)

(66) (56)

(54)

83








































































































643 Eumycetoma







644 Mycotoxins





References | 115





References































References | 117













































References | 119





















































References | 121























1999 21115ndash20















71 Introduction



DOI 1015159783110419047-007











Darkrespiration

Quantumefficiency

Chlorophyll


















0ndash20 ndash60


ndash20

00

20

40

60

80

ndash10

00

10

20

30

40


Net p

hoto

synt

hesi

s (μm

ol C

O 2 mndash2

sndash1)

CO2 ex

chan

ge ndash

μm

ol m

ndash2 sndash1

Light saturation

5degC

10degC


Light compensation


1000 1200 0 10 20 30 40 50
















PPFD tosaturateNP

PPFD com-pensation

OptimalWC for NP

MaximalWC



mm rainequivalent




Net p

hoto

synt

hesi

s ( μ

mol

mndash2

sndash1)

Num

ber o

f rai

nfal

l eve

nts

00

5

10

15

1 2 3 4ndash1

0

1

2

3
















0

(a) (b)

(c) (d)

Num

ber o

f dat

a po

ints

200400600800

1000120014001600

0

Num

ber o

f dat

a po

ints

200

400

600

800

1000

00 200 400 600 800 1000

200400600800



00 10 20


0 10 20Temperature


0 500 1000 1500 2000 2500 3000


Num

ber o

f dat

a po

ints

200400600800

1000120014001600

0

Num

ber o

f dat

a po

ints

200

400

600

800

1000

00 200 400 600 800 1000

200400600800













Sep

0 0

20

40

60

80

100

2012(a) (b)

2013

0

lt0 lt10 lt20 lt30


Temperature (degC)

lt1500 lt2000

Month

20

4000051015

Light

dar

k rat

io

Prop

ortio

n of

tim

e act

ive (

)

Cum

ulat

ive ti

me a

ctive

()

60

80

Oct

Nov

Dec

Jan

Feb

Mar Ap

rM

ay Jun Jul

Aug

Sep

Oct











744 Catastrophes










76 Summary




References | 135


References



































References | 137





























to Climate Change

81 Overview



DOI 1015159783110419047-008


































































Soil

moi

stur

eTime rarr

Precipitationevent

Precipitationevent

Soil

moi

stur

e

Time rarr(a) (b)



Net carbon uptake

Carbon deficit

Carbon deficit



Net carbon uptake









86 Conclusion




References | 151




References





























References | 153












































References | 155


















































References | 157




































91 Introduction



DOI 1015159783110419047-009













92 Soil Definition
































































Tabl

e9

1Ar

tifici

also

ilst

udie

sw

ithin

the

fram

ewor

kof

the

DFG

Prio

rity

Prog

ram

onBi

ogeo

chem

ical

Inte

rface

sin

Soil

(SPP

1315

)foc

usin

gon

soil

mic

robi

alco

mm

uniti

es

Publ

icat

ion

Aim

ofSt

udy

Fact

or(s

)ofV

aria

nce

Dete

ctio

nM

etho

dsIn

cuba

tion

Tim

eFu

rthe

rInf

orm

atio

non

Artifi

cial

Soils

Voge

leta

l[5

4]In

terd

isci

plin

ary

stud

yof

mic

robi

alco

mm

uniti

esO

Mde

com

posi

tion

and

soil

stru

ctur

ede

velo

pmen

tatm

atur

edBG

Is

Soil

min

eral

com

po-

sitio

nan

dpr

esen

ceof

char

coal

DGGE

qPC

Rfra

c-tio

natio

nOM

char

-ac

teriz

atio

n

842

days

(with

addi

tiona

lOM

inpu

taf

ter5

62da

ys)

Voge

leta

l[5

4]

Ding

etal

[7

1]Ea

rlyes

tabl

ishm

ento

fsoi

lbac

teria

lco

mm

uniti

esat

youn

gBG

IsSo

ilm

iner

alco

mpo

-si

tion

and

pres

ence

ofch

arco

al

16S

DGGE

pyr

ose-

quen

cing

19

319

0da

ysPr

onk

etal

[53

]

Babi

net

al

[74]

Deve

lopm

ento

fsoi

lmic

robi

alco

mm

uniti

esan

dre

spon

seto

phen

anth

rene

atm

atur

edBG

Is

Soil

min

eral

com

po-

sitio

nan

dpr

esen

ceof

char

coal

16S

ITS

DGGE

So

uthe

rnBl

ot-

hybr

idiz

atio

nfo

rca

tabo

licge

nes

1ye

ar+

70da

ysph

enan

thre

nePr

onk

etal

[53

]

Babi

net

al

[75]

Deve

lopm

ento

fsoi

lmic

robi

alco

mm

uniti

esan

dre

spon

seto

phen

anth

rene

atlo

ng-te

rmm

atur

edBG

Is

Soil

min

eral

com

po-

sitio

nan

dpr

esen

ceof

char

coal

16S

ITS

DGGE

qP

CRp

yros

eque

nc-

ing

842

days

+72

163

days

phen

anth

rene

+-p

lant

litte

r

Voge

leta

l[5

4]

Stei

nbac

het

al[

76]

Esta

blis

hmen

toff

unct

iona

lsoi

lmic

robi

algu

ilds

over

mat

urat

ion

time

(her

eal

kane

degr

adat

ion)

Soil

min

eral

com

po-

sitio

nan

dpr

esen

ceof

char

coal

qPCR

T-R

FLP

3m

onth

s12

mon

ths

(eac

h+

2w

eeks

plan

tlit

ter)

Pron

ket

al[

53]

Hem

kem

eyer

etal

[77

]Es

tabl

ishm

ento

fsoi

lmic

robi

aldi

vers

ityin

part

icle

size

fract

ions

over

mat

urat

ion

time

Soil

min

eral

com

po-

sitio

nqP

CRT

-RFL

Pfra

c-tio

natio

n6

mon

ths

18m

onth

sPr

onk

etal

[53

]

Ditte

rich

etal

[78

]M

icro

bial

colo

niza

tion

ofso

ilm

iner

als

and

succ

essi

onov

erm

atur

atio

ntim

eSo

ilm

iner

alco

mpo

-si

tion

qPCR

PLF

Aen

zym

eac

tivity

36

121

8m

onth

sPr

onk

etal

[53

]

Pron

ket

al

[80

83]

Unde

rsta

ndin

gOM

turn

over

and

deve

lopm

ent

over

soil

incu

batio

ntim

eSo

ilm

iner

alco

mpo

-si

tion

and

pres

ence

ofch

arco

al

OMch

arac

teriz

a-tio

nfra

ctio

natio

n3

612

18

mon

ths

Pron

ket

al[

54]

Voge

leta

l[8

5]Un

ders

tand

ing

OMtu

rnov

eran

dfo

rmat

ion

ofor

gano

-min

eral

asso

ciat

ions

atlo

ng-te

rmm

atur

edBG

Is

Soil

min

eral

com

po-

sitio

nan

dpr

esen

ceof

char

coal

Fum

igat

ion-

extra

c-tio

nOM

char

acte

ri-za

tion

fract

iona

tion

842

days

+63

days

13C

15N

labe

led

plan

tlitt

er

Voge

leta

l[5

4]







Wolf et al[26]




12 days

Treves et al[27]


Moisture con-tent


Heckmanet al [8196]



5 10 2030 60 90154 days

Wei et al[84]




2 months

Wei et al[86]



11 days

Lamparteret al [87]




10 days



































References






















References | 177




















39299ndash354




























References | 179


















































182 | Index





Kkeratinolytic 112








Index | 183








Xxerophilic 114

Yyeast 108





















The Biology of Arid Soils

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Transcript of The Biology of Arid Soils