ARTICLE IN PRESS

0038-0717/$ - se

doi:10.1016/j.so

�CorrespondE-mail addr

Soil Biology & Biochemistry 40 (2008) 11–29

www.elsevier.com/locate/soilbio

Review Article

‘Decomposer’ Basidiomycota in Arctic and Antarctic ecosystems

Katherine E. Ludleya,b, Clare H. Robinsonb,�

aCentre for Ecology and Hydrology, Lancaster Environment Centre, Library Avenue, University of Lancaster, Bailrigg, Lancaster LA1 4AP, UKbSchool of Earth, Atmospheric and Environmental Sciences, University of Manchester, Williamson Building, Oxford Road, Manchester M13 9PL, UK

Received 21 April 2007; received in revised form 16 July 2007; accepted 26 July 2007

Available online 29 August 2007

Abstract

Current knowledge concerning ‘decomposer’ Basidiomycota in Arctic and Antarctic ecosystems is based on two sources: (a) collections

and surveys of basidiomata, which have resulted in high-quality catalogues of species, although much of the species’ distribution and

ecology are tentative and (b) isolations from soils and plant litter which typically result in a ‘‘low incidence of basidiomycetes’’ [Dowding,

P., Widden, P., 1974. Some relations between fungi and their environment in tundra regions. In: Holding, A.J., Heal, O.W., MacLean Jr.,

S.F., Flanagan, P.W. (Eds.), Soil Organisms and Decomposition in Tundra. Tundra Biome Steering Committee, Stockholm, Sweden, pp.

123–150], probably because of selectivity in isolation methods. In the few molecular studies carried out in Arctic and Antarctic soils to

date, basidiomycetes, particularly yeasts, have been found. These techniques should give better estimates of the order of magnitude of

fungal species richness in Arctic and Antarctic soils, although caution should be used concerning primer choice and amplification

conditions. From collections in Arctic regions, species of basidiomycetes appear to be circumpolar in distribution with restricted

endemism. Using culture-independent methods, it should be possible to test whether selected Arctic or Antarctic species are truly

cosmopolitan, circumpolar, endemic, or are cryptic phylogenetic species.

Particularly in Arctic ecosystems, potential ‘decomposer’ fungi in soils and roots may be from phylogenetically diverse taxa, and

currently it is unclear whether ‘decomposer’ basidiomycetes are the fungi undertaking the majority of organic matter decomposition in

Arctic and Antarctic ecosystems. For example, in some recent studies, wood decomposition in cold Arctic and Antarctic sites appears to

proceed via ‘soft rot’ by anamorphic ascomycetes (e.g. Cadophora species), rather than by ‘white rot’ or ‘brown rot’ basidiomycete

species. Additionally, it appears basidiomycetes and ascomycetes as ericoid and ectomycorrhizal fungi have the potential to be involved

directly in decomposition.

Given that profound changes are likely to occur in patterns of vegetation (Arctic and Antarctic) and size of soil carbon (C) pools

(particularly in the Arctic) by the end of this century, it is necessary to know more about which species of ‘decomposer’ basidiomycetes

are present and to try to define their potentially pivotal roles in ecosystem C (and N) cycling. One solution to characterise further the

identity and roles of these fungi in a logical way, is to standardise methods of detection and ‘function’ at networks of sites, including

along latitudinal gradients. Results of functional tests should be related to community structure, at least for ‘key’ species.

r 2007 Elsevier Ltd. All rights reserved.

Keywords: Arctic; Antarctic; Basidiomycota; Fungi; Carbon cycling; Climate change; Decomposition; DNA; Ecosystem functioning; Mycorrhizas; RNA;

Saprotrophs; Tundra

1. Introduction

Tundra soils contain ca. 11% of the world’s soil carbon(C) pool (Gorham, 1991), and hold 95% of the organicallybound nutrients in the tundra ecosystem (Jonasson, 1983).Owing to slow decomposition rates in cold, wet or dry soilenvironments, plant growth is often limited by nutrient

e front matter r 2007 Elsevier Ltd. All rights reserved.

ilbio.2007.07.023

ing author. Tel.: +44 161 275 3296; fax: +44 161 306 9361.

ess: clare.robinson@manchester.ac.uk (C.H. Robinson).

availability (e.g. Haag, 1974; Shaver and Chapin, 1980,1995). Decomposition of organic matter in terrestrialecosystems is a process of equivalent status to photosynth-esis (Heal et al., 1997). In temperate ecosystems, sapro-trophic (decomposer) fungi in soil and plant litter arepartly responsible for the breakdown of dead organicmaterial and recycling of plant nutrients (see Read andPerez-Moreno, 2003). Prior to 1964, the role of fungi indecomposition of dead organic matter in tundra had notbeen considered in detail. The review here concentrates on

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–2912

‘decomposer’ basidiomycetes.1 The conventional view isthat ‘decomposers’ strongly influence rates and patterns ofrespiratory C release to the atmosphere, plus mineralisa-tion and immobilisation of the limiting nutrients, N andphosphorus (P). However, research over the last twodecades has suggested that such functional separationbetween decomposer and mycorrhizal basidiomycetesshould not be absolute (Read and Perez-Moreno, 2003).Indeed some basidiomycete ecto- (Hibbett et al., 2000;James et al., 2006) and ericoid (WeiX et al., 2004)mycorrhizal symbionts appear to have evolved repeatedlyfrom saprotrophic precursors.

For Arctic and Antarctic soils and litter, the aims of thisreview are to (1) summarise the current informationconcerning the detection and identification of ‘decomposer’basidiomycetes, particularly with regard to moleculartechniques, (2) determine how much is known about‘decomposer’ basidiomycetes in Arctic and Antarcticenvironments in relation to C cycling, and (3) suggestareas where more research is necessary. Examples fromAlpine ecosystems are included where they are particularlysignificant.

2. Review

2.1. Arctic studies

2.1.1. History of Arctic studies in relation to ‘decomposer’

Basidiomycota

Biologists usually accept the definition of Arctic as thoselands beyond the climatic limit of trees (Bliss andMatveyeva, 1992; Fig. 1). From the years before 1900until the present day, ‘classical’ studies of fungi from Arctictundra regions have provided information on species offungi which either (a) form obvious basidiomata (e.g. forNE Greenland, Ferdinandsen (1910), for Spitsbergen andSvalbard, Dobbs (1942), Gulden and Mohn Jenssen (1988),Watling and Watling (1988), Gulden and Torkelsen (1996),for the archipelagos of Franz Josef Land and SevernayaZemlya, Nezdoiminogo (2002), for Canada and Alaska,Linder (1947), Miller and Murray (1973), Ohenoja andOhenoja (1993), for northern Scandinavia, Lange andSkifte (1967), Kallio (1982), for the Russian Arctic,Nezdoiminogo (2003), and more generally Laursen andAmmirati (1982), Laursen et al. (1987), Petrini and Laursen(1993)), or (b) are either culturable members of theZygomycota and anamorphic ascomycetes associated withhigher plants or soil, or Pucciniomycotina, Ustilaginomy-cotina and anamorphoric/teleomorphic Ascomycota ob-

1Basidiomycetes are members of the phylum Basidiomycota, one of the

four phyla in the kingdom Fungi. According to Blackwell et al. (2006), the

phylum Basidiomycota is generally recognised to include three subphyla:

Pucciniomycotina (rusts and other teliospore producing taxa), Ustilagi-

nomycotina (smuts, Ustilaginales and related taxa) and Agaricomycotina

(equivalent to Hymenomycetes, including Tremellomycetes, Dacrymycetes

and Agaricomycetes). Lichenised fungi are beyond the scope of this

review.

served microscopically in planta (e.g. Lind, 1928; Widdenand Parkinson, 1979; Chlebicki, 1995; Bergero et al., 1999).Historically, the numbers of species recorded in (b) weregreater than those for basidiomata in (a) because collec-tions of higher plants were examined for fungi on theirreturn from the Arctic. For example, Lind (1928)documented ca. 2900 fungi on fragments of 4000 driedplants in museum collections from 24 expeditions toSvalbard, including Bear Island, between 1827 and 1925.A great proportion of the work carried out on the fungal

ecology in soils of Arctic environments was performedduring 1964–1974 in the ‘Tundra Biome’ study of theInternational Biological Programme (IBP; Holding et al.,1974; Bliss et al., 1981). Previous reports gave no idea ofthe biomass or numbers of fungi present in relation toother micro-organisms, or of the relative presence andimportance of major physiological groups in tundrasubstrata. Using isolation-based techniques, some of themajor conclusions of the IBP Tundra Biome network from5 geographical Arctic regions (15 sites) were: (1) taxa founddid not appear very different from those in temperate soils,except two interesting differences between high Arctic andtemperate soils were (i) the lack of any species ofTrichoderma and (ii) the high frequency of occurrence ofsterile mycelium, (2) the majority of fungal isolates werepsychrotophic,2 rather than psychrophilic (Flanagan andScarborough, 1974), (3) there was a ‘‘low incidence ofbasidiomycetes’’ (Dowding and Widden, 1974) using theisolation techniques selected.

2.1.2. Current status of knowledge concerning ‘decomposer’

basidiomycetes present in Arctic ecosystems from (a)

basidiome surveys and (b) isolations from plants and soils

For Svalbard, the current level of detail from collections/surveys of basidiomata is illustrated in Gulden andTorkelsen (1996). Their chapter in A Catalogue of Svalbard

Plants, Fungi, Algae and Cyanobacteria includes 175 spp.of macromycetes belonging to the Basidiomycota, of which145 spp. are Agaricales. The information provided includes‘‘Ecosystem Component Values’’, which are tentativebecause of the fragmentary knowledge of the fungi ofSvalbard. These ‘‘Values’’ include sections for rarity onSvalbard, phytogeographical importance, ecological indi-cator value, local abundance and importance to vertebrateanimals. There is also a comments section for each species,containing habitats and references to previous records.A further high-quality example of the current knowledge

relating to basidiomycete species present in Arctic ecosys-tems comes from Miller (2002). Using collections andsurveys of basidiomata from Arctic tundra in NorthAmerica, more than 32 genera of decomposers containing

2The definitions of psychrophiles and psychrotrophs follow those of

Morita (1975) and Gounot (1986). Both psychrophilic and psychrotrophic

fungi have the ability to grow at 0 1C. Psychrophilic fungi have an

optimum temperature for growth of ca. 15 1C or lower, and a maximum

temperature of growth of 20 1C or below, whereas psychrotrophic fungi

have a maximum temperature for growth above 20 1C.

ARTICLE IN PRESS

Ellesmere I.

Banks I.

Greenland

Svalbard

Severnaya

Zemlya

Russia

Devon I.

Truelove

Lowland

ad Astra

Ice Cap

Toolik Lake

Prince

Patrick I.

Ellef

Ringnes I.

Alaska

Franz Josef

Land

Scandinavia

Canada

Subzone A

Subzone B

Subzone C

Subzone D

Subzone E

Fig. 1. Circumpolar map of the Arctic bioclimatic subzones (after CAVM Team, 2003), and locations of sites mentioned in the current text. Detailed

characteristics of the bioclimatic subzones are given at: http://www.geobotany.uaf.edu/cavm/finalcavm/side2_031016.pdf. Bioclimatic subzones A, B and

C together equate to the High Arctic classification of Bliss (1997)), and subzones D and E together equate to the Low Arctic. The solid black line

represents the North American Arctic Transect from Toolik Lake, Alaska to Isachsen, Ellef Ringnes Island (Kade et al., 2005; Vonlanthen et al., 2007).

K.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–29 13

about 100 species have been found. Twenty-two species inthe genera Galerina, Phaeogalera and Leptoglossum aredecomposers of pleurocarpous bryophytes, and over 60species of decomposers belong to the Coprinaceae,Tricholomataceae, Strophariaceae and Hygrophoraceae.According to Miller (2002), the distribution of tundraspecies appears to be circumpolar with restricted ende-mism.

Even though basidiomata are useful for cataloguingspecies, there are fundamental problems in detecting andenumerating basidiomycetes by these reproductive struc-

tures (Arnolds, 1995; Watling, 1995). The occurrence ofbasidiomata is indicative of the presence of mycelium in thesoil, but the absence of basidiomata does not necessarilymean the mycelium is not there. The numbers ofbasidiomata do not necessarily reflect the abundance ofmycelia. In addition, basidiomata of most species showstrong temporal dynamics because of their limited long-evity and pronounced periodicity.From Section 2.1.1, it is clear that, historically,

basidiomycete mycelium has not been isolated effectivelyby soil/litter washing and plating, the second prevalent

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–2914

method by which data have been obtained about fungalcommunities at Arctic sites. Why are ‘decomposer’basidiomycetes isolated very infrequently or not at allusing soil isolation techniques? Basidiomycete myceliumappears difficult to isolate from soil using conventionaltechniques (e.g. reviews by Frankland et al., 1990; Thorn etal., 1996), although specialist agar media (e.g. Hunt andCobb, 1971) and techniques (Thorn et al., 1996) arehelpful. Despite the apparent absence of basidiomycetemycelium in soil, spores (Johansen, 1991) and mycelium of‘decomposer’ basidiomycetes are likely to be present,especially where basidiomata of such fungi occur. Withoutknowledge of mycelial diversity and distribution in the soilprofile, the roles of individual species cannot be defined.Recently developed molecular biological techniques pro-vide an unrivalled opportunity to attempt to resolve thediversity and distribution of basidiomycete mycelia in soil.

In summary, the current information concerning fungaldiversity in Arctic regions comes from two approaches,which are (a) surveys/collections of basidiomata and(b) isolation in pure culture. From (a) basidiomata,basidiomycete species distribution appears to be circum-polar with restricted endemism, and from (b) IBP-typestudies, culturable fungi are largely cold-adapted isolates ofcosmopolitan species, although these may eventually beshown to be cryptic species (e.g. Geml et al., 2006; Tayloret al., 2006). Arguably, these two approaches, (a) and(b) above, provide a very incomplete and biased view offungal species richness in soil (see Section 2.2).

2.1.3. Other Arctic ‘decomposer’ basidiomycetes

In Arctic ecosystems, basidiomycetes, other than thosetraditionally considered as decomposers occur. These taxaare likely to have some levels of decomposer activity butthey are considered in less detail here. For example, ericoid,and some ectomycorrhizal, fungi have the potential to beinvolved directly in attack both on structural polymers,which may render nutrients inaccessible, and in mobilisa-tion of N and P from the organic polymers in which theyare sequestered (reviews by Read and Perez-Moreno, 2003;Thormann, 2006). Ectomycorrhizal fungal communitiesare documented for Arctic-Alpine ecosystems [e.g. asso-ciated with Dryas octopetala (Vare et al., 1992; Harringtonand Mitchell, 2002; Cripps and Eddington, 2005) oroccurring along chronosequences (e.g. Jumpponen et al.,2002)]. Basidiomycetes also exist as components of ericoidmycorrhizas (e.g. Sebacina spp. in the roots of Gaultheria

shallon, northern Vancouver Island, British Columbia,511N, Allen et al., 2003; WeiX et al., 2004; Selosse et al.,2007). The anamorphic basidiomycete ‘species’ Rhizoctonia

solani, temperate isolates of which form a continuum fromroot endophytes to soil saprotrophs, commonly occurredon roots of 76 plants collected in West Spitsbergen,Svalbard (Vare et al., 1992).

Basidiomycete yeasts are present in Arctic ecosystems,for example, two new species of the basidiomycetousanamorphic genus Rhodotorula were described by Golubev

(1998). A novel Rhodotorula sp., Trichosporon dulcitum,Cryptococcus podzolicus and Rhodotorula mucilaginosa

were isolated from dead leaves of Dryas octopetala

collected from Spitsbergen, Svalbard (791N; E.J. Pryce-Miller and C.H. Robinson, personal observation, 2003). Insub-glacial environments at the same location, basidiomy-cete yeasts, predominantly Cryptococcus liquefaciens, wereisolated in high numbers (Butinar et al., 2007).Basidiomycete snow moulds (Typhula ishikariensis,

T. incarnata, Coprinus psychromorbidus) are poor sapro-trophs in nature, requiring parasitism for their existence.Non-living wheat tissues were colonised in vitro bymultiple isolates of T. ishikariensis and T. incarnata,

showing some putative level of saprotrophic activity bythese fungi. The same isolates could utilise microcrystallinecellulose, bacto-cellulose and glucose as C sources,although indulin AT (a commercial lignin preparation)was inhibitory to T. incarnata (Wu and Hsiang, 1999).Obligate basidiomycete plant parasites in Arctic ecosys-tems are Exobasdium (Nannfeldt, 1981; Ing, 1998) andmembers of the rusts and smuts (e.g. Parmalee, 1989;Elvebakk et al., 1996; Scholler et al., 2003; Tojo andNishitani, 2005).

2.1.4. Other, non-basidiomycete, fungi possibly involved in

decomposition in Arctic ecosystems

Various aspects, including ‘decomposer’ activity, ofecto- and ericoid [e.g. the ascomycete (Helotiales)Hymenoscyphus ericae—Scytalidium vaccinii complex]mycorrhizal colonisation in Arctic and boreal ecosystemshave been reviewed by Gardes and Dahlberg (1996),Read and Perez-Moreno (2003) and Thormann (2006).Several other examples of possible ‘decomposer’ non-basiomycetes present in Arctic ecosystems are mentioned inthis section.Arbuscular mycorrhizal (AM) fungal communities are

reported to occur in Arctic ecosytems (e.g. Dalpe andAiken, 1998; Olsson et al., 2004; Allen et al., 2006),although structures resembling AM fungi were not foundin the roots of 76 plant species collected in WestSpitsbergen, and soil samples screened for AM fungicontained only one spore (Vare et al., 1992). According toRead and Perez-Moreno (2003), there is a single report ofenhanced decomposition and increased N capture by AMfungi from organic necromass, and this was related to atemperate system (Hodge et al., 2001).Dark septate endophytes are ubiquitous in the roots of

Arctic and Alpine plants, yet very little is known abouttheir phylogenetic identities or effects on their host plants(Jumpponen and Trappe, 1998; Schadt et al., 2001; Pierceyet al., 2004). One isolate from Ranunculus adoneus waslikely to be in the Euascomycetes, closely related to theanamorphic taxon Phialophora gigantea (Schadt et al.,2001), and Hambleton and Currah (1997) isolated the non-mycorrhizal Phialocephela fortinii from roots of ericaceousplants. Suggesting significant activity in the decompositionof organic matter, cultures of Cadophora finlandia,

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–29 15

Phialocephala fortinii and five dark septate endophytesfrom Alpine plant communities were able to degradecellulose, laminarin, starch, xylan, gelatin, RNA andTween 80 (a synthetic fatty acid ester), but not analoguesof lignin (Caldwell et al., 2000). Endophytic fungi, unlikelyto be basidiomycetes, in leaves may have weak sapro-trophic activity (e.g. associated with Dryas spp. fromGreenland based on 147 collections, Chlebicki andKnudsen, 2001; isolated from 10 plants of Dryas octopetala

from a polar semi-desert at Ny-Alesund, Svalbard, 791N,Fisher et al., 1995).

Basidiomycete ‘white rot’ and ‘brown rot’ fungi oftencarry out wood decomposition in temperate ecosystems(Rayner and Boddy, 1988). However, there is evidencefrom mummified woods (1.8–65 million years ago) ofBetula, Picea and Pinus found near the ad Astra Ice Cap(811N, 761W), Ellesmere Island, Canada, that this ‘ecosys-tem function’ is being carried out by a ‘soft rot’, Cadophora

species (J.A. Jurgens, R.A. Blanchette, T.R. Filley,personal communication, 2006). Such fungi are anamorphsof the Helotiales and are distinct from the morphologicallysimilar anamorph genus Phialophora in the Chaetothyriales(Harrington and McNew, 2003). Cadophora sp. arecircumpolar, with 3 distinct groups separating into newspecies (Harrington and McNew, 2003). Woody debris isnot usually prevalent in high Arctic ecosystems, perhapsaccounting for the prominent decomposer role of ana-morphic ascomycetes via a soft rot pathway rather than bybasidiomycete ‘white rot’ or ‘brown rot’ fungi. Intemperate ecosystems, ‘soft rot’ fungi only assume promi-nence under circumstances where ‘white’ and ‘brown rot’fungi are inhibited, two important examples being in water-saturated wood and preservative-treated wood (Raynerand Boddy, 1988).

2.2. Culture-independent techniques for fungal community

structure in Arctic and Alpine ecosystems

Molecular biological techniques, developed for fungalmycelia in culture and root tips (e.g. Gardes and Bruns,1993; Kowalchuk et al., 1997) and soil (e.g. Smit et al.,1999; Dickie et al., 2002) over the last 10–15 years, provideexciting opportunities to resolve the diversity and distribu-tion of fungal mycelia in ecosystems. These methods couldbe of particular significance in Arctic soils, given the rarefrequency of occurrence of ‘decomposer’ basidiomycetesnoted in previous isolation studies (Sections 2.1.1 and2.1.2; Thormann, 2006). Currently, there are relatively fewrelevant molecular studies, the findings of which aresummarised below with the aim of highlighting resultsconcerning ‘decomposer’ basidiomycetes. The most inter-esting findings, so far, appear to be concerned with theAscomycota.

The earliest relevant studies are from Alpine environ-ments. Schadt et al. (2003) showed, for soil betweentussocks of Kobresia myosuroides in a dry meadow site atNiwot Ridge, Colorado, USA (401030N, 1051350W), that

fungal biomass comprised most of the annual peak in soilmicrobial biomass under snow. By extraction, andamplification with primers ITS9 and nLSU1221R, ofDNA from soil, 10% of the amplicons were basidomycetespecies and zygomycetes less than 1%. Phylogeneticanalysis revealed a high diversity and three novel cladesthat constituted major new groups of fungi (divergent atthe subphylum or class level) within the Ascomycota. Oneof the same novel phylogenetic lineages, located betweenthe Pezizomycotina and Saccharomycotina, was found byVandenkoornhuyse et al. (2002) using 18S primers (AU2and AU4) on DNA extracted from roots of a temperategrass, Arrenatherum elatius. Using culture-independenttechniques, it appears that fungi in one of the same novelbasal lineages in the Ascomycota as above, distinct fromthe three currently recognised Subphyla of Ascomycota,the Taphrinomycotina, Saccharomycotina and Pezizomy-cotina, are widespread in many diverse habitats worldwideand cluster by geographic region (McLenon et al. 2006).These fungi are more closely related to the Taphrinomy-cotina and Saccharomycotina rather than the Pezizomy-cotina, and are likely to be obligate biotrophs (e.g.intracellular parasites) and live in the active rhizosphere.At the Lyman Glacier, Washington, USA (481110N,

1201540W), clone libraries of partial 18S rRNA genesequences from non-vegetated soils adjacent to the glacierterminus and from similar sites adjacent to the terminalmoraine, contained saprotrophic, mycorrhizal, parasitic orpathogenic ascomycetes and basidiomycetes (Jumpponen,2003). Observations of biotrophic fungi in the younger soilwere attributed to an aerially deposited, dormant sporebank. No definitive zygomycetous sequences were identi-fied. In a later paper, Jumpponen (2007) used a similarcloning technique to characterise fungal, largely ectomy-corrhizal, communities in soil under canopies of Salix

commutata and S. planifolia on the forefront of a recedingglacier.Nemergut et al. (2005) stated that, by contrast with

Alpine ecosystems, molecular microbial diversity in theArctic has been little explored, and that only threepublished studies had used molecular techniques toexamine these soils, and these were related to bacteria.Subsequently, several molecular studies relating to Arcticfungi have been initiated and these are summarised inSection 2.2.1.

2.2.1. Studies by latitudinal transects and vegetation type in

the Arctic

Using clone libraries of partial 18S rRNA genes,basidiomycete sequences (e.g. Cryptococcus, Mrakia, Phle-

bia) have been found in permanently frozen soil in north-western Siberia (Lydolph et al., 2005). Ancient andpreviously unreported fungal DNA was detected fromAscomycota, Basidiomycota and Zygomycota, in totalfrom 12 different classes and 10 different orders.The fungal communities in tussock and especially inter-

tussock soils were dominated by Basidiomycota, using the

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–2916

fungal-specific EF4 and EF3 primers (Smit et al., 1999) forpartial 18S rRNA gene sequences in a study of organic andmineral soils under tussock, intertussock and shrubvegetation at Toolik Lake Long-Term Ecological Researchsite (681380N, 1491340W; Wallenstein et al., 2007). TheBasidiomycota were dominated by Agaricales, and somefungal groups, such as the Cantharellales, were moreabundant in June than in August.

Research concerning fungal diversity is being conductedat recently established and described sites along a biocli-matic gradient (North American Arctic Transect, NAAT,Kade et al., 2005; Vonlanthen et al., 2007; Fig. 1).Ribosomal RNA genes in soil DNA extracts are beingamplified with fungal-specific primers (ITS region; Gardesand Bruns, 1993), followed by the establishment andsequencing of fungal clone libraries. Preliminary data showa reduction in fungal diversity in roots and fungal fruitingbodies with increasing latitude, as well as a decline inectomycorrhizal morphotypes obtained from Salix arctica

(I. Timling, D. L. Taylor, personal communication, 2006).At present, high percentage similarities occur betweensequences from roots, soils and basidiomata from Arcticcollections compared with lower latitudes.

Using direct isolation of small-subunit and ITS rRNAgenes by PCR and high-throughput sequencing of clonedfragments, abundance and diversity of fungi in forest soilsmay be orders of magnitude higher than previouslyhypothesised (O’Brien et al., 2005). Sequencing tens tohundreds of clones, as is typically undertaken, is generallyinsufficient to approach saturation of species accumulationcurves. Collaboration with a genome centre, employingcost-effective high throughput methods, would allow thesequencing of tens of thousands of clones (D.L. Taylor,personal communication). This would give an even moreaccurate estimate of the abundance and diversity of fungiin ecosystems.

2.3. Carbon cycling in Arctic ecosystems in relation to

‘decomposer’ basidiomycetes

‘‘The role of the basidiomycete fungi in the tundra hasnot been studied but hyphae with clamp connections showthat basidiomycetes account for at least one-third of thetotal soil fungal biomass in the autumn’’ (Flanagan andScarborough, 1974). It remains true today that the role inecosystem functioning (e.g. decomposition and C cycling)of ‘decomposer’ (and indeed ectomycorrhizal) basidiomy-cetes in Arctic ecosystems is inadequately characterised.

Profound changes are predicted to occur in Arcticregions by the latter part of this century (examples areshown in Fig. 2), including increases in annual average airtemperatures by ca. 3–5 1C over the land areas, and inannual average precipitation of ca. 20% [Arctic ClimateImpact Assessment (ACIA), 2005]. These changes will haveeffects on ecosystem functions that are difficult to predict,particularly whether positive or negative feedbacks toclimate warming will be apparent. Four key, autocorre-

lated uncertainties are (1) how vegetation patterns willchange, and how these changes will feed back to climate(e.g. ACIA, 2005; Arft et al., 1999; Walker et al., 2006),(2) how soil C pools will change with changing patterns ofpermafrost, soil temperatures and vegetation cover (e.g.Mack et al., 2004; Davidson and Janssens, 2006), (3) howbacterial- vs decomposer fungal- vs mycorrhizal-dominatedprocesses will change in relation to vegetation change (e.g.Lipson et al., 2002; Schadt et al., 2003; Wallenstein et al.,2007), and (4) how important are basidiomycete decom-posers in the ecosystem processes of C (and nutrient)cycling. The outcome of these uncertainties could becritically important to global C cycles and in predictingpositive and negative feedbacks to atmospheric CO2 levelsand climate change. Simultaneously, the abundance,diversity, functions and potential responses to climatechange of fungi, including basidiomycetes, in Arctic tundraare not fully understood.In one recent laboratory study (Zak and Kling, 2006),

analyses of phospholipid fatty acids coupled with com-pound-specific 13C isotope tracing (13C-cellobiose, 13C–N-acetylglucosamine, 13C-vanillin), were used to quantifymicrobial community composition and function in soilsfrom two sites in each of three ecosystems at Toolik Lake,Alaska. The activity of extracellular enzymes involved incellulose, chitin and lignin degradation was also assayed. Inthese laboratory incubations at 2.8 1C, soil from undertussock tundra contained significantly greater relativeabundance and activity of fungi than in soils fromstream-side birch willow and lakeside wet sedge tundra.However, soils were homogenised and the majority ofvisible coarse and fine roots removed by hand, suggestingthat any mycorrhizal contribution to fungal biomass oractivity would not be the same as occurred in the ecosystemin situ. The fraction of biomass and activity contributed by‘decomposer’ basidiomycetes is also unclear from suchstudies.In a meta-analysis of standardised warming experiments

at 11 locations across the tundra biome, warming increasedheight and cover of deciduous shrubs and graminoids,decreased cover of mosses and lichens, and decreased totalspecies diversity and evenness (Walker et al., 2006). Withrelation to increases in shrub cover in response to warming,very little is known about the role of mycorrhizas in the Cbalance of Arctic ecosystems. For example, there ispotential for common mycorrhizal networks to develop(e.g. Simard et al., 1997), and Hobbie and Hobbie (2006)estimated that the plants provided 8–17% of theirphotosynthetic C to mycorrhizal fungi for growth andrespiration in moist, acidic tundra at Toolik Lake.Differences in C particularly, and nitrogen (N), isotope

ratios (d13C and d15N values) among basidiomata ofmycorrhizal and saprotrophic fungi may provide a wayof determining trophic strategies (or ‘function’ in relationto C cycling at the broad-scale) for a broad spectrum offungi whose strategies have been a matter of speculationonly (Hobbie et al., 2001). Mycorrhizal fruit-bodies have

ARTICLE IN PRESS

Present

extent of

sea ice

Projected

summer

sea ice

extentPresent

permafrost

boundary

Projected

permafrost

boundary

Present

tree-line

Projected

tree-line

Fig. 2. A circumpolar map of the Arctic, showing changes in the extent of summer sea ice and tree-line projected to occur by the end of this century. The

change in the permafrost boundary assumes that present areas of discontinuous permafrost will be free of any permafrost in the future and this change is

likely to occur beyond the 21st century (after ACIA, 2005).

K.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–29 17

been found to be consistently enriched in d15N anddepleted in d13C compared with those of saprotrophicfungi (Hobbie et al., 1999, 2001).

Within natural soil fungal communities, differences canbe detected between those species that are present, usingDNA, and those that are present and metabolically active,using RNA (I.C. Herriott and D.L. Taylor, personalcommunication, 2006; Anderson and Parkin, 2007).

In summary, as seen from the scattered informationabove, there is still far to go before decomposition

and C cycling of ‘decomposer’ (and ectomycorrhizal)basidiomycetes in Arctic ecosystems are satisfactorilydescribed and analysed. Model studies using mixturesof decomposer (and mycorrhizal) fungi in relativelyrealistic substrata may help to explain the roles of differentfungi in C cycling. RNA has great potential as an in situindicator of fungal activity. It is necessary to relate resultsof functional tests to community structure, which shouldbe possible for ‘key’ species, if not for the wholecommunity.

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–2918

2.4. Studies concerning ‘decomposer’ fungi in Antarctica

2.4.1. Biogeographical zones

Less than 1% of the Antarctic is free of ice and snow andterrestrial biodiversity is generally low compared withcorresponding latitudes in the Arctic (Kanda and Komar-kova, 1997), and most of the continent is technically desert.The Antarctic can be usefully divided into three zones: thesub-Antarctic, the maritime Antarctic and the continentalAntarctic (Fig. 3; Peck et al., 2006). The sub-Antarctic zone

Signy I.

King

George I.

Alexander I.

Ross I.

Ross Sea

RegionNew

South

Sandwich Is.

30°W

150°W

120°W

90°W

180°

0°

60°W

South Georgia

Falkland Is

SOUTH AMERICA

South

Orkney Is

Polar Frontal Zone

McMurdo

Sound

ANT

Antarctic Peninsula

Fig. 3. Circumpolar map of Antarctica, showing biogeographical zones (afte

mentioned in text. The dotted red line represents the outer boundary of the sub

maritime zone and the green broken line represents the outer boundary of th

transect from Signy Island (maritime) to La Gorce Mountains (continental).

Falkland Islands (cool temperate) to Coal Nunatak, Alexander Island (mariti

lies between 501 and 601 South and includes SouthGeorgia, the Kerguelen Islands, Crozet Islands, HeardIsland, McDonald Island, Prince Edward Island andMacquarie Island. The climates of these islands arestrongly oceanic and the temperature variation over theyear is much smaller than experienced in continentalAntarctica. The sub-Antarctic is the most biologicallydiverse of the Antarctic biogeographical zones, andvegetation consists of both flowering plants and crypto-gams. The vegetation is superficially similar to Arctic

McMurdo

Dry Valleys

Harbor

Victoria

Land

Kerguelen Is.

Windmill Is.

60°S

30°E

60°E

90°E

120°E

40°S

50°S

150°E

ARCTICA

Polar Frontal Zone

80°S

r Kanda and Komarkova, 1997; Peck et al., 2006) and locations of sites

-Antarctic zone, the dotted blue line represents the outer boundary of the

e continental zone. The solid red line represents the Lawley et al. (2004)

The solid pink line represents the Yergeau et al. (2007) transect from the

me).

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–29 19

tundra, although sub-Antarctic soils do not have apermafrost layer (Peck et al., 2006).

The maritime Antarctic comprises the western coastalregions of the Antarctic Peninsula southwards to Alex-ander Island and islands of the Scotia Arc (South Shetland,South Orkney and South Sandwich Islands) at 55–721S.The climate has some oceanic influence but this is muchreduced during winter when extensive sea-ice forms. Thegrowing season is around 5 months, compared with around2 months in continental Antarctica (Wynn-Williams, 1990).The maritime climate is also milder than in continentalAntarctica, with more available water and greater vegeta-tion cover. Bare mineral soil with discontinuous crypto-gamic vegetation, typical in many areas of the maritimeAntarctic, is termed fellfield soil (Wynn-Williams, 1990).This zone contains two vascular plant species, Deschampsia

antarctica and Colobanthus quitensis. Large bryophytecommunities occur in certain regions, and under turf-forming mosses, organic layers can accumulate (Bailey andWynn-Williams, 1982). Some of the coastal areas andislands of both the sub-Antarctic and maritime Antarcticare significantly influenced by colonies of birds or seals,which provide quantities of additional nutrients, particu-larly N and P.

There are large ice-free areas in continental Antarctica,such as the Victoria Land Dry Valleys, plus more isolatedareas comprising exposed rock and soil on nunataks. Thecold desert areas of the inland valleys and mountainregions present extremely harsh environments with low soilmoisture levels (Fell et al., 2006), high soil salt contents,strong winds, extremes of temperature and frequentfreeze–thaw cycles. The vegetation of continental Antarc-tica is dominated by lichens. There are no vascular plantsand bryophyte communities comprise few species.

For the whole Antarctic region, the British AntarcticSurvey (BAS) maintains regularly updated records offungal species that have either been published inthe literature or deposited in major culture collections(Bridge et al., 2007). This is an excellent, detailed onlineresource.

2.4.2. ‘Decomposer’ basidiomycetes in sub-Antarctic

ecosystems

The sections below, synthesised from primary literature,focus on ‘decomposer’ basidiomycetes found in soils,or plant communities, in each of the three biogeogra-phical zones. Table 1 is a summary, with particular regardto the Basidiomycota, of the findings and techniquesused in a number of studies of Antarctic fungi, and inclu-des the longitude and latitude of the sites referred to inthe text.

Biodiversity of macro-organisms has generally beenshown to decrease from the cool temperate zone, throughthe sub-Antarctic, to the interior of continental Antarctic.This appears to be true for fungi on a broad scale, althoughthe variety of habitats and climatic conditions experienced,especially within the maritime Antarctic, mean that this

relationship is not always straightforward (Vishniac, 1996;Lawley et al., 2004; Yergeau et al., 2007).A large number of basidiomycete species has been

recorded in the sub-Antarctic using collections of basidio-mata (Pegler et al., 1980; McKenzie and Foggo, 1989).Several records from Pegler et al. (1980) have been reportedonly on imported substrata and these species are thereforethought likely to have been introduced. For example,Trametes versicolor was collected from the underside oftimber at Grytviken Whaling Station, South Georgia, andDacrymyces stillatus was collected from a wooden foot-bridge, also at Grytviken Whaling Station (Pegler et al.,1980). The naturally occurring ecosystems in the sub-Antarctic nevertheless support diverse communities of‘decomposer’ basidiomycetes, although they are thoughtto be less diverse than in the corresponding latitudes in thenorthern hemisphere.A list of recorded basidiomata was compiled specifically

for South Georgia by Smith (1994) and contains 37basidiomycete taxa. Even though 60% of South Georgiais permanently ice-covered, coastal areas are free of snowand ice for 4–6 months during the summer and consist oflarge areas of tall tussock grassland dominated by Poa

flabellata. The decayed foliage of the grass develops into a‘pedestal’ of peat in which the root system is enveloped.Smith (1994) listed a total of 24 basidiomycetes associatedwith this ecosystem. The most diverse basidiomycetecommunities in South Georgia occur in the grass litterthat accumulates around the base of the tussock pedestals,including, for example, species of Collybia, Galerina andOmphalina, and mycelial networks have been observed inthe decaying litter (Smith, 1994).Other snow-free habitats found on South Georgia

include bogs and mires, stands of the dwarf shrub Acaena

magellanica and areas dominated by mosses such as theturf-forming Polytrichum alpestre. Basidiomata of ‘decom-poser’ species have been recorded from all of thesevegetation types (for example, species of Galerina andCoprinus have been recorded from bryophyte bog, andCoprinus martini has been recorded from areas dominatedby Acaena magellanica), although they were less frequentlyobserved than in the tussock grassland. Grasslandsdominated by Deschampsia antarctica occur on SouthGeorgia and Smith (1994) listed eight basidiomycetespecies associated with litter of this species.A number of basidiomycetes were recorded from the

sub-Antarctic Kerguelen Islands, including various speciesof Coprinus, Galerina and an Agaricus species (Pegler et al.,1980). From 62 sites in the Kerguelen Islands, a variety offungi were isolated from soil, plant and bird/seal faecalmaterial using the Warcup plate method and plating ontomalt extract agar medium (Steiman et al., 1995). However,only two basidiomycete species were detected (Corticium

alutaceum and an unidentified species) and these from onlyfive of the sites. In summary, it is known from collectionsof basidomata that basidiomycetes occur in sub-Antarcticsoils and litter, although the isolation techniques employed

ARTIC

LEIN

PRES

STable 1

Summary, with regard to the Basdiomycota, of the findings and techniques used in a number of studies of Antarctic fungi (ordered by increasing degrees South)

Area studied Study outline Techniques Findings Reference

Falkland Islands, sub-Antarctic

zone and Antarctica. South from

511S

A list compiled of recordings of

macromycetes (Ascomycota and

Basidiomycota) from the Antarctic

region

Collection of basidiomata Contains a list of 44 basidiomycetes that

are known to occur in the Antarctic

region. Most of the collections are

deposited at Kew herbarium

Pegler et al. (1980)

Gradient from Falkland Islands

(cool temperate) to base of

Antarctic peninsula (maritime),

51–721S

Studied size and structure of soil

community (bacteria, fungi and

nematodes) along an environmental

gradient. Comparison between vegetated

and fellfield sites

Fungal abundance assessed using CFU

counts, PLFA and ergosterol analysis

and real-time PCR of fungal 18S rDNA.

CFU counts carried out on PDA and

water agar medium and incubated at 4,

12 and 20 1C

Studied influence of latitude and

vegetation on soil community but did not

identify species. Overall found that

community structure was associated with

latitude and community abundance more

related to factors associated with

vegetation

Yergeau et al. (2007)

PCR-DGGE analysis also carried out

using fungal primer FR1-gc/FF390

Kerguelen Islands, 48–491S (sub-

Antarctic)

Soil, plant and faecal material analysed

from various sites in the Kerguelen

Islands

Warcup plates on malt extract agar

medium (MEA), with 1.5%

chloramphenicol, incubated at 22 1C

2 basidiomycetes found: Corticium

alutaceum (1 sample) and unidentified (4

samples)

Steiman et al. (1995)

Majority of isolated fungi were

anamorphic ascomycetes

South Georgia, 541S (sub-

Antarctic)

Occurrence and distribution of fungi

according to habitat and substratum

preference

Account based on various collections of

basidiomata held at the British Antarctic

Survey, Royal Botanic Gardens, Kew,

and the International Mycological

Institute, Egham

List of 113 taxa, including 37

basidiomycetes and 49 ascomycetes and

listed according to substratum

Smith (1994)

South Georgia, 541S (sub-

Antarctic)

Fungi isolated from new, mature and

senescent leaves and fallen litter of three

plant species (two grasses and a dwarf

shrub). Common isolates were used to

test enzyme activity and effects of

temperature on growth rate (1–30 1C)

Isolated during summer, plated on

cellulose agar medium or potato dextrose

agar medium (PDA) incubated at 5 or

25 1C. Airspora also sampled on same

media and incubated at 25 1C

Sterile mycelium accounted for 41% of

total number of fungi isolated. The

remainder were mostly ascomycetes as

well as the zygomycete Mortierella. No

basidiomycetes were detected

Hurst et al. (1983)

Jane Col, Signy Island, 601S and

Fossil Bluff, Alexander Island,

711S (maritime Antarctica)

Fungal diversity in maritime soils

determined using direct extraction of

DNA from soils and isolation studies

DNA extracted directly from soil and

from isolated colonies. PCR

amplification of 18S rDNA carried out.

Soil culture enrichment used on Fossil

Bluff soils so results for these indicate

‘culturable diversity’

A total of 102 fungal sequences of which

48 were from the Basidiomycota. At

Fossil Bluff the basidiomycete sequences

were all yeasts. Basidiomycete sequences

from Jane Col were closely related to the

Uredinales

Malosso et al. (2006)

Gradient from Signy Island,

(maritime) to coastal mainland,

(maritime) to interior

(continental), 60–871S

Studied eukaryotic diversity in six sites

along an environmental gradient to test

the hypothesis that diversity decreases as

latitude increases. Also considered levels

of endemicity in biota

Clone libraries constructed by extracting

total genomic DNA from soil and

amplifying SSU rRNA gene

Found very few basidiomycete

sequences. Within the maritime Antarctic

there was no decrease in diversity with

increase in latitude, although diversity

was lower in continental Antarctic

Lawley et al. (2004)

Signy Island, South Orkney

Islands, 601S (maritime)

Microbial distribution and seasonal

variation. Six sites with different

environmental conditions. Microbial

Took soil samples in summer and winter 23 fungal isolates found of which 13 were

identified. 50% of isolates were sterile

mycelium. No basidiomycetes detected

Bailey and Wynn-Williams

(1982)Length of fungal mycelium observed by

direct count method

K.E

.L

ud

ley,

C.H

.R

ob

inso

n/

So

ilB

iolo

gy

&B

ioch

emistry

40

(2

00

8)

11

–2

920

ARTIC

LEIN

PRES

Sdistribution examined with respect to soil

variables

Dilution plates on Czapek-Dox agar

medium plus 0.5% Bacto yeast extract

and 0.007% rose Bengal, incubated at 10

and 25 1C

Soil-crumb plates prepared according to

Warcup (1950)

Signy Island, South Orkney

Islands, 601S (maritime)

Compared biota in grassland soils

(Deschampsia antarctica) at Signy Island

with moorland soil in upland UK

Length of fungal mycelium observed by

direct count method

Found mostly dark forms of sterile

mycelia at Signy. Verticillium and

Geomyces spp. common

Heal et al. (1967)

Isolation of fungi on dilution plates and

Warcup plates on Czapek-Dox agar

medium

No basidiomycetes detected, although,

‘‘one species of toadstool observed’’

King George Island, South

Shetland Islands, 621S (maritime)

Microfungi were isolated from mosses,

lichens and vascular plants (54 samples).

Optimal growth temperatures were

determined for isolates. Yeasts were not

considered

Fungi were isolated by placing fragments

of moss, lichen and selected plants on

MEA and incubating at 5 and 10 1C

A total of 490 isolates was obtained from

which 58 taxa were identified. The

majority were anamorphic ascomycetes.

Also isolated were 63 different types of

sterile mycelium. No basidiomycetes

were detected. 44% of tested isolates

were found to be mesophilic, 46%

psychrotolerant and 10% psychrophilic

Moller and Dreyfuss (1996)

Windmill Islands, Wilkes Land,

East Antarctica, 661S

(continental)

Filamentous fungi isolated from soil and

moss samples and the effect of water

content in moss turves on fungal

diversity was assessed

Vertical cores cut through moss turves

with 1 cm cork borer

No relationship found between water

content and diversity for soil or moss.

Majority of isolates were anamorphic

ascomycetes, with species of Phoma the

most frequently occurring

McRae and Seppelt (1999)

Slurry of moss samples spread onto

plates of PDA, Czapek Dox agar and

cornmeal agar media incubated at 5 and

18 1C. Preliminary isolations had been

done with 9 isolation media in order to

optimise isolation method

No basidiomycetes were detected

Windmill Islands, 661S

(continental)

Microfungi were isolated from samples

of soils, mosses, algae, lichens, seal skin

and feathers. Samples were collected in

summer from a variety of habitats

Fungi were isolated using dilution plate

and soil plate methods. A modified

version of Warcup’s soil plate method

was also used (Warcup, 1950). Media

used: PDA, Czapek-Dox, MEA,

Oatmeal agar, V-8 vegetable extract agar,

Sabouraud maltose agar, Cornmeal agar,

and nutrient agar. Plates incubated at 4

and 20 1C

A total of 1,228 isolates from which 22

genera were identified. Mosses and algae

supported the greatest diversity of fungi

and more fungi were isolated from

biotically influenced soils than those with

little or no plant or animal influence. No

basidiomycetes isolated

Azmi and Seppelt (1998)

Victoria Land, 74–761S

(continental)

Isolated yeasts and filamentous fungi

from 8 different moss species at 17

different sites

Aliquots of each moss species plated onto

MEA and PDA and incubated at 15 and

24 1C

A total of 28 fungal taxa isolated and

identified. Most were anamorphic

ascomycetes; the most commonly

isolated species was Phoma herbarum.

Five species of basidiomycetous yeast

were isolated

Tosi et al. (2002)

Also tested growth rates of fungi at 8

different temps (2–451)

Victoria Land, 741S (continental) Soil, bird dung and feather samples (126

samples) collected from nine different

sites in Victoria Land

Hair-bait technique ( for keratinophilic

fungi). Isolation from soil, dung and

feather samples carried out using a moist

chamber technique

From 122 occurrences of fungi, 15 species

were identified, mostly anamorphic

ascomycetes. The basidiomycetous yeast

Del Frate and Caretta

(1990)

K.E

.L

ud

ley,

C.H

.R

ob

inso

n/

So

ilB

iolo

gy

&B

ioch

emistry

40

(2

00

8)

11

–2

921

ARTIC

LEIN

PRES

STable 1 (continued )

Area studied Study outline Techniques Findings Reference

Cryptococcus albidus was isolated from

penguin, petrel and skua dung

Dilution plate technique used for soil and

dung samples using MEA, PDA and

yeast phosphate soluble starch agar

medium. All samples incubated at 8, 15,

25 and 40 1C

Ross Island (continental) and

McMurdo Dry Valleys

(continental) Sites between 76 and

781S

Compared fungi isolated from three

expedition huts and other introduced

materials on Ross Island with

surrounding soils and with more remote

soils in the McMurdo Dry Valleys

Isolations from wood samples and soil

dilution plates carried out on MEA,

acidified MEA and a basidiomycete

selective media and incubated at 8 and

20 1C

A total of 284 fungal ITS sequences were

identified

Arenz et al. (2006)

DNA extracted from cultures and ITS

sequences amplified with ITS1 and ITS4

primers

Most fungi identified were filamentous

ascomycetes (74%) and these were the

most frequently isolated fungi in wood

and maritime soil samples. The most

common fungi in soils from the Dry

Valleys were Cryptococcus and

Epicoccum

DNA extracted from wood and other

artefacts was amplified by PCR with

ITS1F and ITS4, then ITS3 and ITS4

and analysed by DGGE

New Harbor, 771S (continental) Above and below-ground wood samples

taken during summer from a historic hut

brought to Antarctica in 1959

Isolations from wood samples onto MEA

or acidified MEA and incubated at 8 and

20 1C. Isolates identified by morphology

and rDNA ITS sequencing, and tested

for ability to degrade wood.

Dominant fungi were species of

Cadophora and these seemed to be main

wood decomposers causing significant

‘soft rot’.

Held et al. (2006)

Taylor Valley, 771S (continental) Studied fungal distribution and

abundance from 160 sample pits in 20

sample sites including in a range of soil

habitats

Fungi were isolated on a standard yeast

culture medium and incubated at 15 1C

Several of the identified fungi were

basidiomycetous yeasts and a species of

the nematophagous Nematoctonus

(anamorph of Hohenbuelia) was also

identified

Connell et al. (2006)

DNA extracted from colonies and rDNA

from the ITS region amplified and

sequenced

McMurdo Dry Valleys area, 771S

(continental)

Biodiversity of micro-eukaryotes and

their relationship with soil moisture was

studied in the poorly developed soils of

the Dry Valleys

Samples collected in summer from a

variety of sites

Basidiomycetes and ascomycetes were

each found in most of the study sites. The

prevalent basidiomycete species were of

the yeast genus Trichosporon. Other

basidiomycetes identified were species of

Hohenbuehelia (wood-decomposing and

nematophagous fungi), Cryptococcus,

and Malassezia. In the driest soils, an

unidentified clade and species of

Trichosporon were dominant

Fell et al. (2006)

DNA extraction from soil with analysis

of LSU and SSU rDNA

Ross Sea region, 771S

(continental)

The fungi responsible for soft rot of three

huts built by expeditions to Antarctica in

1901, 1908 and 1911 were identified.

Samples of above-ground wood from the

huts, and wooden artefacts were analysed

Wood samples were used for scanning

electron microscopy. Isolations from

wood samples carried out on MEA,

acidified MEA and a basidiomycete-

selective medium

Evidence of ‘soft rot’ decay was found in

two of the huts. No evidence of brown or

white rot was found. The dominant fungi

were species of Cadophora, which are

anamorphic ascomycetes. Evidence

suggests that they are endemic and were

not brought to Antarctica with the huts

Blanchette et al. (2004)

Isolated cultures used for rDNA

extraction. The ITS1, ITS2 and the 5.8S

gene of the ribosomal repeat region were

amplified and sequenced

K.E

.L

ud

ley,

C.H

.R

ob

inso

n/

So

ilB

iolo

gy

&B

ioch

emistry

40

(2

00

8)

11

–2

922

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–29 23

have generally been unable to detect them (e.g. Hurst et al.,1983 in Table 1).

2.4.3. ‘Decomposer’ basidiomycetes in maritime and

continental Antarctic ecosystems

In the maritime Antarctic, fungal diversity was assessedusing a combination of isolation and molecular techniquesat two sites in the maritime Antarctic: Fossil Bluffon Alexander Island and Jane Col on Signy Island(Malosso et al., 2006). Several basidiomycetous yeastsand a group of species closely related to the Uredinaleswere detected.

A variety of relatively recent studies have attempted todescribe the fungal communities in soils, mosses and othersubstrates from Victoria Land in continental Antarctica,using isolation techniques. Species of the basidiomycetousyeast Cryptococcus, as well as Rhodotorula minuta, wereisolated from mosses (Tosi et al., 2002). Cryptococcus

albidus was the only basidiomycete found in the study byDel Frate and Caretta (1990) and was isolated frompenguin, petrel and skua dung [see also Azmi and Seppelt(1998); McRae and Seppelt (1999) in Table 1].

Molecular methods, compared with traditional isolationtechniques, have resulted in different taxa being detected(Table 1), although there are difficulties and biases withboth sets of methods. In the Dry Valleys, basidiomycetes,particularly yeasts, have been detected by moleculartechniques (Table 1). Fell et al. (2006) studied the effectof soil moisture content on micro-eukaryote biodiversityand whether molecular techniques revealed previouslyuncultured, or unculturable, species in Taylor and WrightValleys (McMurdo Dry Valleys). In the lowest moisturecontent soil (0.2–1.3%), Fell et al. (2006) detectedbasidiomycetous yeasts from the genus Trichosporon, andan unidentifiable clade that had high percentage similaritiesto basidiomycetes, including Termitomyces-related fungi,as the most prevalent taxa. Additionally in this study,molecular techniques demonstrated the presence of thebasidiomycete Hohenbuehelia, a genus which containswood decomposers and nematophagous fungi, and thebasidiomycetous yeast Malassezia. The anamorph ofHohenbuehelia, Nematoctonus, was also detected by Con-nell et al. (2006) by amplification and sequencing of rDNAfrom the ITS region in Taylor Valley soils.

Spores or propagules may be transported by the windand may then be preserved in low temperatures and remainviable for long periods, even if unable to colonise thehabitat they find themselves in. It is possible that thesedormant propagules contribute considerably to the de-tected biodiversity in some of the harsher regions(Vishniac, 1996), and it is necessary to identify whichspecies are active and which inactive when assessingdiversity or function. A further confounding factor is thatthe ‘high stress’ and high disturbance conditions inAntarctica are likely to favour fungal species that producelarge numbers of small spores (Tosi et al., 2005) and thiscould influence methods, such as counts of colony-forming

units, of assessing species’ frequency of occurrence(Yergeau et al., 2007).In conclusion: (1) most of the basidiomycetes isolated

from continental Antarctic soils e.g. Dry Valleys, areyeasts, whereas the ‘macro-basidiomycetes’ are mostfrequent in the sub-Antarctic, (2) as concluded for Arcticsystems, the majority of taxa found are psychrotrophicrather than psychrophilic (Heal et al., 1967; Del Frate andCaretta, 1990; Kerry, 1990; Moller and Dreyfuss, 1996;Zucconi et al., 1996; Azmi and Seppelt, 1997; Tosi et al.,2002), (3) a few species of fungi have been shown to beendemic, and such species are psychrophilic, (4) fewbasidiomycetes have been detected in soils and litter usingtraditional isolation techniques, which may be because of anumber of reasons including the selectivity of the methodsemployed, that basidiomycetes may not be frequent inthese soils, and the temporal and spatial variability of thebasidiomycete mycelium, (5) similar to the situationdiscussed for basidiomycetes in Arctic soils (Section 2.3),RNA methods should help to obtain a more accuratedetermination of which basidiomycete species are active inAntarctic ecosystems.

2.4.4. Carbon cycling in Antarctic ecosystems in relation to

‘decomposer’ basidiomycetes

In Antarctic ecosystems, fungal taxonomic diversity isrelatively poorly characterised and even less is knownabout the function of fungal taxa in C cycling. Basidio-mycetous yeasts are capable of using simple sugars. Theyare often found in association with bryophyte communitiesand are thought to exploit the release of dissolved organicC from bryophytes because of damage caused in free-ze–thaw cycles (Wynn-Williams, 1980).Duncan et al. (2006) isolated fungi from ancient wooden

structures and artefacts left behind from the expeditions ofScott and Shackleton (781380S, 1161250E). Seventy-twoisolates of filamentous fungi were cultured on five differentselective media from interior structural wood of the CapeEvans historic hut, 27 screened positive for the ability todegrade carboxymethyl cellulose. Eighteen non-basidiomy-cete isolates produced extracellular endo-1,4-b-glucanasewhen grown at 4 and 15 1C. Two unidentified isolates on‘‘medium 7’’, stated to be preferential for basidiomycetes,were not tested.Again, the information on the role of basidiomycetes in

C cycling is fragmentary, and anamorphic ascomycetes,particularly Cadophora species, are likely to have apredominant role in wood decomposition.Since Antarctic ecosystems are constrained by extreme

environmental conditions, they are likely to be verysensitive to environmental change, including warming(e.g. Vaughan, 2006), greater or smaller amounts ofprecipitation (e.g. Convey and Smith, 2006), and elevatedUV-B (e.g. Hughes et al., 2003). Indirect effects ofenvironmental change on the structure and function of‘decomposer’ basidiomycete communities could includechanges in the dominant plant species (e.g. Smith and

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–2924

Steenkamp, 1990; Robinson et al., 2003; Convey andSmith, 2006) and greater competition from alien species(Convey and Smith, 2006).

3. Conclusions

From the information above, the following two ques-tions arise in relation to ‘decomposer’ basidiomycetes inArctic and Antarctic soils and plant litter.

3.1. Which ‘decomposer’ basidiomycetes are present?

3.1.1. Culture-independent studies

It appears difficult, using traditional culture-basedmethods, to isolate basidiomycete mycelium from Arcticand Antarctic soils, and current knowledge concerningspecies’ identity comes largely from collections and surveysof basidiomata. Are culture-independent, molecular tech-niques useful for detecting, and characterising the diversity,of basidiomycetes in such soils? The number of studies isfew, and the results depend to a certain extent on choice ofprimer and the number of PCR cycles (Jumpponen, 2007).Even so, basidiomycetes have been detected using PCR-based techniques in Alpine, Arctic and Antarctic soils (e.g.Schadt et al., 2003; Fell et al. 2006; Wallenstein et al.,2007). These fungi, so far, are relatively often basidiomy-cete yeasts (e.g. Malosso et al., 2006), especially incontinental Antarctica (e.g. Arenz et al., 2006; Connellet al., 2006; Fell et al., 2006).

Good comparisons of molecular vs traditional techni-ques for detecting and identifying fungi in temperate soilsand wood can be found, respectively, in O’Brien et al.(2005; for fungi in general) and Allmer et al. (2006; forbasidiomycetes only). These critiques are also relevant topotential studies in tundra ecosystems. O’Brien et al. (2005)used large-scale sequencing of DNA, targeting the ITSrRNA gene, for quantifying and characterising soil fungaldiversity in soils from Pinus taeda-dominated and mixedhardwood ecosystems. They recovered 412 unique opera-tional taxonomic units (OTUs) from a total of 863 fungalsequences, a level of richness comparable to that found in a1500m2 forest plot in Switzerland (Straatsma et al., 2001),where 408 species were recovered using surveys ofbasidiomata. The study in Switzerland, however, required21 years of sampling, and identification of 71,222basidiomata, whereas O’Brien et al. (2005) captured thislevel of richness with 863 fungal sequences from only two2000m2 forest plots in a single locale at a single point intime. Given the lack of saturation in their species-effortcurves, these authors would have vastly exceeded their ownrichness estimates if the sampling effort had been compar-able to that of the study of Straatsma et al. (2001). Thus,the true magnitude of fungal diversity could be orders ofmagnitude higher than previously suggested. These authorsalso believed that, using DNA sequences as the primarysampling unit also requires much less processing of eachsample than more labour-intensive methods such as

basidiomata collection and culture-based census-taking,and is therefore amenable to automation of data collectionand analysis, making large-scale biotic surveys conductedover short-time periods feasible.The composition and abundance of wood-inhabiting

fungal communities in 7-year-old slash piles in a 50-year-old Picea abies stand were examined by Allmer et al.(2006), using three methods: counts of basidiomata,mycelial culturing and direct amplification of internaltranscribed spacer terminal restriction fragment length(ITS-T-RFLP) polymorphism from wood combined withsequencing of reference rDNA. Fifty-eight fungal specieswere detected from piled branches and treetops. Morespecies were revealed by basidiome counts and culturingthan by direct amplification from wood. Allmer et al.(2006) concluded that basidiome monitoring poorlyreflected abundance, and that T-RFLP recorded the mostfrequent fungal taxa, but overlooked uncommon taxa.Culturing mycelia from wood gave a bias towards speciesfavoured by the cultural medium.

3.1.2. Degree of endemicity

Largely based on collections from Arctic regions, speciesof basidiomycetes appear circumpolar with restrictedendemism. In relation to Svalbard, temperate/borealspecies comprise ca. 20% of the total known species ofbasidiomycetes, Arctic/Alpine species are in two groups, anorthern group and a group of equally frequent north–south species, which together comprise ca. 75%, and trueArctic species constitute ca. 5% (G. Gulden personalcommunication, 2002). Using culture-independent techni-ques, it should be possible to test whether selected Arctic orAntarctic species are truly cosmopolitan, as was suggestedas a conclusion of the IBP, or are cryptic phylogeneticspecies (e.g. Amanita muscaria in Alaska; Geml et al.,2006). In future molecular studies, careful choices ofprimers and amplification conditions are necessary(O’Brien et al., 2005; Jumpponen, 2007), in order tofacilitate cross-comparison between sites and with previousresults obtained by more traditional methods.

3.2. What are the functions of these ‘decomposer’

basidiomycetes?

3.2.1. Are ‘decomposer’ basidiomycetes the predominant

decomposer fungi in these ecosystems?

Complex basidiomycete and non-basidiomycete fungalcommunities with potential decomposer activity exist insoils and roots in the Arctic (review by Thormann, 2006).More information about C cycling by all such taxa isnecessary to discover whether ‘decomposer’ basidiomycetesare important in decomposition in Arctic and Antarcticecosystems. For example, in some recent studies, wooddecomposition at cold Arctic and Antarctic sites appears toproceed via ‘soft rot’ by anamorphic ascomycetes (e.g.Cadophora species) rather than by ‘white rot’ or ‘brownrot’ basidiomycete species.

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–29 25

3.2.2. Fragmentary knowledge of ‘decomposer’

basidiomycete function, e.g. roles in the C cycle

A possible solution to help characterise the roles of‘decomposer’ basidiomycetes is to use a combination oftechniques to measure the function of basidiomycete myceliain situ in the field or in ecologically relevant substrata in thelaboratory. Examples of methods of measuring ‘function’ insitu are: quantitation of mRNA (e.g. Lamar et al., 1995),addition of 13C- labelled substrates followed by stable-isotopeprobing coupled with isotope ratio mass spectrometry ofnucleic acids or fungal membrane lipids (e.g. Lueders et al.,2004; Rangel-Castro et al., 2005), assessment of laccasesequences from DNA (Luis et al., 2004, 2005), anddegradation of fluorogenic enzyme substrates (Miller et al.1998; Courty et al., 2005; Lindahl and Finlay, 2006). It isnecessary to relate results of functional tests to communitystructure, at least for ‘key’ species.

3.2.3. The importance of organic nitrogen

Organic N sources are likely to be of greater importance tofungi in most high-latitude ecosystems than inorganic Nsources (Lindahl et al., 2002), because low soil temperatures,high or low soil moisture and poor resource quality inhibit Nmineralisation. In boreal forests, for example, it is likely thatN-acetylglucosamine and amino acids replace ammoniumand nitrate as the principal sources of N for ECM plants(Lindahl and Taylor, 2004). However, significant functionalvariability occurs among species of boreal/temperate ECMfungi in their ability to utilise complex organic sources of N,particularly protein. A greater capability to use protein inpure culture is correlated with low availability of inorganicsoil N (Lilleskov et al., 2002; Read and Perez-Moreno, 2003),and/or cold environments (Tibbett et al., 1998), at the sitesfrom where the fungi were isolated. Of the species and generaof ‘decomposer’ basidiomycetes mentioned in the currentreview, there is little information about whether these speciesor isolates produce extracellular proteinases or chitinases.More research is necessary to characterise the roles of‘decomposer’ basidiomycetes in degrading various sources oforganic N in high-latitude soils.

In Arctic and Antarctic ecosystems, the potential responsesof ‘decomposer’ basidiomycetes and their roles in C (and N)cycling to environmental change are largely unknown (but seeGange et al., 2007 for a temperate example). Suchuncertainties add further ambiguities to the effects ofenvironmental changes on functioning in these ecosystemsand on further feedbacks to climate change. Furtherinformation concerning the identity and roles of ‘decomposer’basidiomycetes in Arctic and Antarctic ecosystems could begained by standardising detection and ‘function’ methods atnetworks of sites, including along latitudinal gradients.

Acknowledgements

This work was carried out during the tenure of a NaturalEnvironment Research CASE Studentship (KEL) and with

assistance from the Abisko Transnational Access Pro-gramme (CHR).

References

ACIA, 2005. Impacts of a Warming Arctic. Cambridge University Press,

Cambridge, UK.

Allen, N., Nordlander, M., McGonigle, T., Basinger, J., Kaminskyj, S.,

2006. Arbuscular mycorrhizae on Axel Heiberg Island (801N) and at

Saskatoon (521N) Canada. Canadian Journal of Botany 84,

1094–1100.

Allen, T.R., Millar, T., Berch, S.M., Berbee, M.L., 2003. Culturing and

direct DNA extraction find different fungi from the same ericoid

mycorrhizal roots. New Phytologist 160, 255–272.

Allmer, J., Vasiliauskas, R., Ihrmark, K., Stenlid, J., Dahlberg, A., 2006.

Wood-inhabiting fungal communities in woody debris of Norway

spruce (Picea abies (L.) Karst.) as reflected by sporocarps, mycelial

isolations and T-RFLP identification. FEMS Microbiology Ecology

55, 57–67.

Anderson, I.C., Parkin, P.I., 2007. Detection of active soil fungi by RT-

PCR amplification of precursor rRNA molecules. Journal of Micro-

biological Methods 68, 248–253.

Arenz, B.E., Held, B.W., Jurgens, J.A., Farrell, R.L., Blanchette, R.A.,

2006. Fungal diversity in soils and historic wood from the

Ross sea region of Antarctica. Soil Biology & Biochemistry 38,

3057–3064.

Arft, A.M., Walker, M.D., Gurevitch, J., Alatalo, J.M., Bret-Hart, S.D.,

Dale, M., Diemer, M., Gugerli, F., Henry, G., Jones, M., Hollister, R.,

Jonsdottir, I., Laine, K., Levesque, E., Marion, G., Molau, U.,

Molgard, P., Nordenhall, U., Raszhivin, V., Robinson, C.H.,

Starr, G., Stenstrom, A., Stenstrom, M., Totland, Ø., Turner, L.,

Walker, L., Webber, P., Welker, J., Wookey, P.A., 1999. Response

patterns of arctic plant species to experimental warming: a meta-

analysis of the International Tundra Experiment. Ecological Mono-

graphs 69, 491–511.

Arnolds, E., 1995. Problems in measurements of species diversity of

macrofungi. In: Allsopp, D., Colwell, R.R., Hawksworth, D.L. (Eds.),

Microbial Diversity and Ecosystem Function. CAB International,

Wallingford, UK, pp. 337–353.

Azmi, O.R., Seppelt, R.D., 1997. Fungi of the Windmill Islands,

continental Antarctica. Effect of temperature, pH and culture media

on the growth of selected microfungi. Polar Biology 18, 128–134.

Azmi, O.R., Seppelt, R.D., 1998. The broad-scale distribution of

microfungi in the Windmill Islands region, continental Antarctica.

Polar Biology 19, 92–100.

Bailey, A.D., Wynn-Williams, D.D., 1982. Soil microbiological studies at

Signy Island, South Orkney Islands. British Antarctic Survey Bulletin

51, 167–191.

Bergero, R., Girlanda, M., Varese, G.C., Intilli, D., Luppi, A.M., 1999.

Psychrooligotrophic fungi from Arctic soils of Franz Joseph Land.

Polar Biology 21, 361–368.

Blackwell, M., Hibbett, D.S., Taylor, J.W., Spatafora, J.W., 2006.

Research coordination networks: a phylogeny for kingdom Fungi

(Deep Hypha). Mycologia 98, 829–837.

Blanchette, R.A., Held, B.W., Jurgens, J.A., McNew, D.L., Harrington, T.C.,

Duncan, S.M., Farrell, R.L., 2004. Wood-destroying soft rot fungi in the

historic expedition huts of Antarctica. Applied and Environmental

Microbiology 70, 1328–1335.

Bliss, L.C., 1997. Arctic ecosystems of North America. In: Wielgolaski,

F.E. (Ed.), Polar and Alpine Tundra, vol. 3. Elsevier, Amsterdam,

USA.

Bliss, L.C., Matveyeva, N.V., 1992. Circumpolar arctic vegetation. In:

Chapin, F.S., Jefferies, R.L., Reynolds, J.F., Shaver, G.R., Svoboda, J.

(Eds.), Arctic Ecosystems in a Changing Climate: An Ecophysiological

Perspective. Academic Press, San Diego, USA, pp. 59–89.

Bliss, L.C., Heal, O.W., Moore, J.J. (Eds.), 1981. Tundra Ecosystems: A

Comparative Analysis. Cambridge University Press, Cambridge, UK.

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–2926

Bridge, P., Spooner, B.M., Roberts, P., 2007. List of non-lichenized fungi

from the Antarctic region (version 2.1.4) /http://www.antarctica.

ac.uk/Resources/BSD/Fungi/S.

Butinar, L., Spencer-Martins, I., Gunde-Cimerman, N., 2007. Yeasts in

high Arctic glaciers: the discovery of a new habitat for eukaryotic

microorganisms. Antonie van Leeuwenhoek 91, 277–289.

Caldwell, B.A., Jumpponen, A., Trappe, J.M., 2000. Utilisation of major

detrital substrates by dark-septate root endophytes. Mycologia 92,

230–232.

CAVM Team, 2003. Circumpolar Arctic Vegetation Map. Scale

1:7,500,000. Conservation of Arctic Flora and Fauna (CAFF). Map

No. 1, US Fish and Wildlife Service, Anchorage, Alaska, USA.

Chlebicki, A., 1995. Microfungi on Dryas extracted from Polish

phanerogam herbaria. Acta Societatis Botanicorum Poloniae 64,

393–407.

Chlebicki, A., Knudsen, H., 2001. Dryadicolous microfungi from Green-

land I. List of species. Acta Societatis Botanicorum Poloniae 70,

291–301.

Connell, L., Redman, R., Craig, S., Rodriguez, R., 2006. Distribution and

abundance of fungi in the soils of Taylor Valley, Antarctica. Soil

Biology & Biochemistry 38, 3083–3094.

Convey, P., Smith, R.I.L., 2006. Responses of terrestrial Antarctic

ecosystems to climate change. Plant Ecology 182, 1–10.

Courty, P.E., Pritsch, K., Schloter, M., Hartmann, A., Garbaye, J., 2005.

Activity profiling of ectomycorrhiza communities in two forest soils

using multiple enzymatic tests. New Phytologist 167, 309–319.

Cripps, C.L., Eddington, L.H., 2005. Distribution of mycorrhizal types

among alpine vascular plant families on the Beartooth Plateau, Rocky

Mountains, USA, in reference to large-scale patterns in arctic-alpine

habitats. Arctic, Antarctic and Alpine Research 37, 177–188.

Dalpe, Y., Aiken, S.G., 1998. Arbuscular mycorrhizal fungi associated

with Festuca species in the Canadian High Arctic. Canadian Journal of

Botany 76, 1930–1938.

Davidson, E.A., Janssens, I.A., 2006. Temperature sensitivity of soil

carbon decomposition and feedbacks to climate change. Nature 440,

165–173.

Del Frate, G., Caretta, G., 1990. Fungi isolated from Antarctic material.

Polar Biology 11, 1–7.

Dickie, I.A., Xu, B., Koide, R.T., 2002. Vertical niche differentiation of

ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New

Phytologist 156, 527–535.

Dobbs, C.G., 1942. Note on the larger fungi of Spitsbergen. Journal of

Botany London 80, 94–102.

Dowding, P., Widden, P., 1974. Some relations between fungi and their

environment in tundra regions. In: Holding, A.J., Heal, O.W.,

MacLean, Jr., S.F., Flanagan, P.W. (Eds.), Soil Organisms and

Decomposition in Tundra. Tundra Biome Steering Committee,

Stockholm, Sweden, pp. 123–150.

Duncan, S.M., Farrell, R.L., Thwaites, J.M., Held, B.W., Arenz, B.E.,

Jurgens, J.A., Blanchette, R.A., 2006. Endoglucanase-producing fungi

isolated from Cape Evans historic expedition on Ross Island,

Antarctica. Environmental Microbiology 8, 1212–1219.

Elvebakk, A., Gjærum, H.B., Sivertsen, S., 1996. Part 4. Fungi II.

Myxomycota, Oomycota, Chytridiomycota, Zygomycota, Ascomyco-

ta, Deuteromycota, Basidiomycota: Uredinales and Ustilaginales. In:

Elvebakk, A., Prestrud, P. (Eds.), A Catalogue of Svalbard Plants,

Fungi, Algae and Cyanobacteria, vol. 198. Norsk Polarinstitutt,

pp. 207–259.

Fell, J.W., Scorzetti, G., Connell, L., Craig, S., 2006. Biodiversity of

micro-eukaryotes in Antarctic dry valley soils witho5% soil moisture.

Soil Biology & Biochemistry 38, 3107–3119.

Ferdinandsen, C., 1910. Fungi terrestres from North-East Greenland.

Meddelser om Grønland 43, 137–145.

Fisher, P.J., Graff, F., Petrini, L.E., Sutton, B.C., Wookey, P.A., 1995.

Fungal endophytes of Dryas octopetala from a high arctic polar

semidesert and from the Swiss Alps. Mycologia 87, 319–323.

Flanagan, P.W., Scarborough, A.M., 1974. Physiological groups of

decomposer fungi on tundra plant remains. In: Holding, A.J.,

Heal, O.W., MacLean, Jr., S.F., Flanagan, P.W. (Eds.), Soil

Organisms and Decomposition in Tundra. Tundra Biome Steering

Committee, Stockholm, Sweden, pp. 159–181.

Frankland, J.C., Dighton, J., Boddy, L., 1990. Methods for studying fungi

in soil and forest litter. In: Grigorova, R., Norris, J.R. (Eds.), Methods

in Microbiology, vol. 22. Academic Press, London, UK, pp. 343–404.

Gange, A.C., Gange, E.G., Sparks, T.H., Boddy, L., 2007. Rapid and

recent changes in fungal fruiting patterns. Science 316, 71.

Gardes, M., Bruns, T.D., 1993. ITS primers with enhanced specificity for

basidiomycetes: application to the identification of mycorrhizae and

rusts. Molecular Ecology 2, 113–118.

Gardes, M., Dahlberg, A., 1996. Mycorrhizal diversity in arctic and alpine

tundra: an open question. New Phytologist 133, 147–157.

Geml, J., Laursen, G.A., O’Neill, K., Nusbaum, H.C., Taylor, D.L., 2006.

Beringian origins and cryptic speciation events in the fly agaric

(Amanita muscaria). Molecular Ecology 15, 225–239.

Golubev, V.I., 1998. Rhodotorula creatinovora and R. yakutica—new

species of basidiomycetous yeasts, extracted from permafrost soils of

Eastern Siberian Arctic. Mikologiya I Fitopatologiya 32, 8–13.

Gorham, E., 1991. Northern peatlands: role in the carbon cycle and

probable response to climatic warming. Ecological Applications 1,

182–195.

Gounot, A.-M., 1986. Psychrophilic and psychrotrophic microorganisms.

Experientia 42, 1192–1197.

Gulden, G., Mohn Jenssen, K., 1988. Arctic and Alpine Fungi—2.

Soppkonsulenten, Oslo.

Gulden, G., Torkelsen, A.-E., 1996. Part 3. Fungi I. Basidiomycota:

Agaricales, Gasteromycetales, Aphyllophorales, Exobasidiales, Dacry-

mycetales and Tremellales. In: Elvebakk, A., Prestrud, P. (Eds.), A

Catalogue of Svalbard Plants, Fungi, Algae and Cyanobacteria, vol.

198. Norsk Polarinstitutt, pp. 173–206.

Haag, R.W., 1974. Nutrient limitations to plant production in two tundra

communities. Canadian Journal of Botany 52, 103–116.

Hambleton, S., Currah, R.S., 1997. Fungal endophytes from the roots of

alpine and boreal Ericaceae. Canadian Journal of Botany 75,

1570–1581.

Harrington, T.C., McNew, D.L., 2003. Phylogenetic analysis places the

Phialophora-like anamorph genus Cadophora in the Helotiales.

Mycotaxon 87, 141–151.

Harrington, T.J., Mitchell, D.T., 2002. Characterization of Dryas

octopetala ectomycorrhizas from limestone karst vegetation, western

Ireland. Canadian Journal of Botany 80, 970–982.

Heal, O.W., Bailey, A.D., Latter, P.M., 1967. Bacteria, fungi and

protozoa in Signy Island soils compared with those from a temperate

moorland. Philosophical Transactions of the Royal Society of London

Series B, Biological Sciences 252, 191–197.

Heal, O.W., Anderson, J.M., Swift, M.J., 1997. Plant litter quality and

decomposition: an historical overview. In: Cadisch, G., Giller, K.E.

(Eds.), Driven by Nature. CAB International, Wallingford, UK, pp.

2–30.

Held, B.W., Jurgens, J.A., Duncan, S.M., Farrell, R.L., Blanchette, R.A.,

2006. Assessment of fungal diversity and deterioration in a wooden

structure at New Harbor, Antarctica. Polar Biology 29, 526–531.

Hibbett, D.S., Gilbert, L.-B., Donoghue, M.J., 2000. Evolutionary

instability of ectomycorrhizal symbioses in basidiomycetes. Nature

407, 506–508.

Hobbie, E.A., Macko, S.A., Shugart, H.H., 1999. Insights into nitrogen

and carbon dynamics of ectomycorrhizal and saprotrophic fungi from

isotopic evidence. Oecologia 118, 353–360.

Hobbie, E.A., Weber, N.S., Trappe, J.M., 2001. Mycorrhizal vs

saprotrophic status of fungi: the isotopic evidence. New Phytologist

150, 601–610.

Hobbie, J.E., Hobbie, E.A., 2006. 15N in symbiotic fungi and plants

estimates nitrogen and carbon flux rates in arctic tundra. Ecology 87,

816–822.

Hodge, A., Campbell, C.D., Fitter, A.H., 2001. An arbuscular mycor-

rhizal fungus accelerates decomposition and acquires nitrogen directly

from organic material. Nature 413, 297–299.

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–29 27

Holding, A.J., Heal, O.W., MacLean, Jr., S.F., Flanagan, P.W. (Eds.),

1974. Soil Organisms and Decomposition in Tundra. Tundra Biome

Steering Committee, Stockholm, Sweden.

Hughes, K.A., Lawley, B., Newsham, K.K., 2003. Solar UV-B radiation

inhibits the growth of Antarctic terrestrial fungi. Applied and

Environmental Microbiology 69, 1488–1491.

Hunt, R.S., Cobb Jr., F.W., 1971. Selective medium for the isolation of

wood-rotting basidiomycetes. Canadian Journal of Botany 49,

2064–2065.

Hurst, J.L., Pugh, G.J.F., Walton, D.W.H., 1983. Fungal succession and

substrate utilization on the leaves of three South Georgia phaner-

ogams. British Antarctic Survey Bulletin 58, 89–100.

Ing, B., 1998. Exobasidium in the British Isles. Mycologist 12, 80–82.

James, T.Y., Kauff, F., Schoch, C.L., Matheny, P.B., Hofstetter, V., Cox,

C.J., Celio, G., Guiedan, C., Fraker, E., Miadlikowska, J., Lumbsch,

H.T., et al., 2006. Reconstructing the early evolution of Fungi using a

six-gene phylogeny. Nature 443, 818–822.

Johansen, S., 1991. Airborne pollen and spores on the Arctic island of Jan

Mayen. Grana 30, 373–379.

Jonasson, S., 1983. Nutrient content and dynamics in north Swedish shrub

tundra areas. Holarctic Ecology 6, 295–304.

Jumpponen, A., 2003. Soil fungal community assembly in a primary

successional glacier forefront ecosystem as inferred from rDNA

sequence analyses. New Phytologist 158, 569–578.

Jumpponen, A., 2007. Soil fungal communities underneath willow

canopies on a primary successional glacier forefront: rDNA sequence

results can be affected by primer selection and chimeric data.

Microbial Ecology 53, 233–246.

Jumpponen, A., Trappe, J.M., 1998. Dark septate endophytes: a review of

facultative biotrophic root-colonising fungi. New Phytologist 140,

295–310.

Jumpponen, A., Trappe, J.M., Cazares, E., 2002. Occurrence of

ectomycorrhizal fungi on the forefront of retreating Lyman Glacier

(Washington, USA) in relation to time since deglaciation. Mycorrhiza

12, 43–49.

Kade, A., Walker, D.A., Raynolds, M.K., 2005. Plant communities and

soils in cryoturbated tundra along a bioclimate gradient in the Low

Arctic, Alaska. Phytocoenologia 35, 761–820.

Kallio, P., 1982. Aspects of northern Finnish macromycology. In:

Laursen, G.A., Ammirati, J.F. (Eds.), Arctic and Alpine Mycology.

University of Washington Press, Seattle, USA, pp. 410–431.

Kanda, H., Komarkova, V., 1997. Antarctic terrestrial ecosystems. In:

Wielgolaski, F.E. (Ed.), Ecosystems of the World 3—Polar and Alpine

Tundra. Elsevier, Amsterdam, The Netherlands, pp. 721–761.

Kerry, E., 1990. Effects of temperature on growth-rates of fungi from sub-

Antarctic Macquarie Island and Casey, Antarctica. Polar Biology 10,

293–299.

Kowalchuk, G.A., Gerards, S., Woldendorp, J.W., 1997. Detection and

characterization of fungal infections of Ammophila arenaria (marram

grass) roots by denaturing gradient gel electrophoresis of specifically

amplified DNA. Applied and Environmental Microbiology 63,

3858–3865.

Lamar, R.T., Schoenike, B., Vanden Wymelenberg, A., Stewart, P.,

Dietrich, D.M., Cullen, D., 1995. Quantitation of fungal mRNAs in

complex substrates by reverse transcription PCR and its application to

Phanerochaete chrysosporium-colonised soil. Applied and Environ-

mental Microbiology 61, 2122–2126.

Lange, M., Skifte, O., 1967. Notes on the macromycetes of northern

Norway. Acta Scientia 23.

Laursen, G.A., Ammirati, J.F. (Eds.), 1982. Arctic and Alpine Mycology.

University of Washington Press, Seattle, USA.

Laursen, G.A., Ammirati, J.F., Redhead, S.A. (Eds.), 1987. Arctic and

Alpine Mycology II. Plenum Press, New York, USA.

Lawley, B., Ripley, S., Bridge, P., Convey, P., 2004. Molecular analysis of

geographic patterns of eukaryotic diversity in Antarctic soils. Applied

and Environmental Microbiology 70, 5963–5972.

Lilleskov, E.A., Hobbie, E.A., Fahey, T.J., 2002. Ectomycorrhizal fungal

taxa differing in response to nitrogen deposition also differ in pure

culture organic nitrogen use and natural abundance of nitrogen

isotopes. New Phytologist 154, 219–231.

Lind, J., 1928. The micromycetes of Svalbard. Skrifter om Svalbard og

Ishavet 13.

Lindahl, B.D., Finlay, R.D., 2006. Activities of chitinolytic enzymes

during primary and secondary colonisation of wood by basidiomyce-

tous fungi. New Phytologist 169, 389–397.

Lindahl, B.D., Taylor, A.F.S., 2004. Occurrence of N-acetylhexosamini-

dase-encoding genes in ectomycorrhizal basidiomycetes. New Phytol-

ogist 164, 193–199.

Lindahl, B.D., Taylor, A.F.S., Finlay, R.D., 2002. Defining nutritional

constraints on carbon cycling in boreal forests—towards a less

‘phytocentric’ perspective. Plant and Soil 242, 123–135.

Linder, D.H., 1947. Fungi. In: Polunin, N. (Ed.), Botany of the Canadian

Eastern Arctic, Part 2. Thallophyta and Bryophyta. National Museum

of Canada Bulletin, vol. 97, pp. 234–297.

Lipson, D.A., Schadt, C.W., Schmidt, S.K., 2002. Changes in soil

microbial structure and function in an alpine dry meadow following

spring snow melt. Microbial Ecology 43, 307–314.

Lueders, T., Wagner, B., Claus, P., Friedrich, M.W., 2004. Stable isotope

probing of rRNA and DNA reveals a dynamic methylotroph

community and trophic interactions with fungi and protozoa in oxic

rice soil. Environmental Microbiology 6, 60–72.

Luis, P., Walther, G., Kellner, H., Martin, F., Buscot, F., 2004. Diversity

of laccase genes from basidiomycetes in a forest soil. Soil Biology &

Biochemistry 36, 1025–1036.

Luis, P., Kellner, H., Zimdars, B., Langer, U., Martin, F., Buscot, F.,

2005. Patchiness and spatial distribution of laccase genes of

ectomycorrhizal, saprotrophic and unknown basidiomycetes in the

upper horizons of a mixed forest cambisol. Microbial Ecology 50,

570–579.

Lydolph, M.C., Jacobsen, J., Arctander, P., Gilbert, M.T.P., Gilichinsky,

D.A., Hansen, A.J., Willerslev, E., Lange, L., 2005. Beringian

paleocology inferred from permafrost-preserved fungal DNA. Applied

and Environmental Microbiology 71, 1012–1017.

Mack, M.C., Schuur, E.A.G., Bret-Harte, M.S., Shaver, G.R., Chapin

III., F.S., 2004. Ecosystem carbon storage in arctic tundra reduced by

long-term nutrient fertilisation. Nature 431, 440–443.

Malosso, E., Waite, I.S., English, L., Hopkins, D.W., O’Donnell, A.G.,

2006. Fungal diversity in maritime Antarctic soils determined using a

combination of culture isolation, molecular fingerprinting and cloning

techniques. Polar Biology 29, 552–561.

McKenzie, E.H.C., Foggo, M.N., 1989. Fungi of New Zealand

subantarctic islands. New Zealand Journal of Botany 27, 91–100.

McLenon, T.M., Schadt, C.W., Rizvil, L., Martin, A.P., Schmidt, S.K.,

Vilgalys, R., Moncalvo, J.M., 2006. A novel widespread subphylum of

Ascomycota unravelled from soil rDNA sampling. In: Abstract in

Eighth International Mycological Congress Proceedings, p. 407.

McRae, C.F., Seppelt, R.D., 1999. Filamentous fungi of the Windmill

Islands, continental Antarctica. Effect of water content in moss turves

on fungal diversity. Polar Biology 22, 389–394.

Miller, M., Palojarvi, A., Rangger, A., Reeslev, M., Kjøller, A., 1998. The

use of fluorogenic substrates to measure fungal presence and activity in

soil. Applied and Environmental Microbiology 64, 613–617.

Miller Jr., O.K., 2002. Basidiomycetes in arctic tundra in North America.

In: Abstract in Seventh International Mycological Congress Proceed-

ings, p. 18.

Miller Jr., O.K., Murray, B.M., 1973. Arctic and alpine agarics from

Alaska and Canada. Canadian Journal of Botany 51, 43–49.

Moller, C., Dreyfuss, M.M., 1996. Microfungi from Antarctic lichens,

mosses and vascular plants. Mycologia 88, 922–933.

Morita, R.Y., 1975. Psychrophilic bacteria. Bacterial Reviews 39,

144–167.

Nannfeldt, J.A., 1981. Exobasidium, a taxonomic re-assessment applied to

the European species. Symbolae Botanicae Upsalienses 23, 1–72.

Nemergut, D.R., Costello, E.K., Meyer, A.F., Pescador, M.Y., Wein-

traub, M.N., Schmidt, S.K., 2005. Structure and function of alpine and

arctic microbial communities. Research in Microbiology 156, 775–784.

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–2928

Nezdoiminogo, E.L., 2002. Agaricoid macromycetes of the archipelagoes

of Franz-Josef Land and Severnaya Zemlya. Mikologiya I Fitopato-

logiya 36, 35–42.

Nezdoiminogo, E.L., 2003. Biogeographical review of agaricoid fungi

from Russian Arctic. Mikologiya I Fitopatologiya 37, 28–35.

O’Brien, H.E., Parrent, J.L., Jackson, J.A., Moncalvo, J.-M., Vilgalys, R.,

2005. Fungal community analysis by large-scale sequencing of

environmental samples. Applied and Environmental Microbiology

71, 5544–5550.

Ohenoja, E., Ohenoja, M., 1993. Lactarii of the Franklin and Keewatin

Districts of the Northwest Territories, Arctic Canada. Bibliotheca

Mycologica 150, 179–192.

Olsson, P.A., Eriksen, B., Dahlberg, A., 2004. Colonisation by arbuscular

mycorrhizal and fine endophytic fungi in herbaceous vegetation in the

Canadian High Arctic. Canadian Journal of Botany 82, 1547–1556.

Parmalee, J.A., 1989. The rusts (Uredinales) of Arctic Canada. Canadian

Journal of Botany 67, 3315–3365.

Peck, L.S., Convey, P., Barnes, D.K.A., 2006. Environmental constraints

on life histories in Antarctic ecosystems: tempos, timings and

predictability. Biological Reviews 81, 75–109.

Pegler, D.N., Spooner, B.M., Smith, R.I.L., 1980. Higher fungi of

Antarctica, the sub-Antarctic zone and Falkland Islands. Kew Bulletin

35, 499–561.

Petrini, O., Laursen, G.A. (Eds.), 1993. Arctic and Alpine Mycology 3–4.

Bibliotheca Mycologica 150.

Piercey, M.M., Graham, S.W., Currah, R.S., 2004. Patterns of genetic

variation in Phialocephela fortinii across a broad latitudinal gradient in

Canada. Mycological Research 108, 955–964.

Rangel-Castro, J.I., Killham, K., Ostle, N., Nicol, G.W., Anderson, I.C.,

Scrimgeour, C.M., Ineson, P., Meharg, A., Prosser, J.I., 2005. Stable

isotope probing analysis of the influence of liming on root exudate

utilization by soil microorganisms. Environmental Microbiology 7,

828–838.

Rayner, A.D.M., Boddy, L., 1988. Fungal Decomposition of Wood: Its

Biology and Ecology. Wiley, New York, pp. 122–125.

Read, D.J., Perez-Moreno, J., 2003. Mycorrhizas and nutrient cycling in

ecosystems—a journey towards relevance? New Phytologist 157,

475–492.

Robinson, S.A., Wasley, J., Tobin, A.K., 2003. Living on the edge—plants

and global change in continental and maritime Antarctica. Global

Change Biology 9, 1681–1717.

Schadt, C.W., Mullen, R.B., Schmidt, S.K., 2001. Isolation and

phylogenetic identification of a dark-septate fungus associated with

the alpine plant Ranunculus adoneus. New Phytologist 150,

747–755.

Schadt, C.W., Martin, A.P., Lipson, D.A., Schmidt, S.K., 2003. Seasonal

dynamics of previously unknown fungal lineages in tundra soils.

Science 301, 1359–1361.

Scholler, M., Schnittler, M., Piepenbring, M., 2003. Species of Anthra-

coidea (Ustilaginales, Basidiomycota) on Cyperaceae in Arctic Europe.

Nova Hedwigia 76, 415–428.

Selosse, M.-A., Setaro, S., Glatard, F., Richard, F., Urcelay, C., WeiX, M.,

2007. Sebacinales are common mycorrhizal associates of Ericaceae.

New Phytologist 174, 864–878.

Shaver, G.R., Chapin III., F.S., 1980. Response to fertilization by various

plant growth forms in an Alaskan tundra: nutrient accumulation and

growth. Ecology 61, 662–675.

Shaver, G.R., Chapin III., F.S., 1995. Long-term responses to factorial

NPK fertilizer treatment by Alaskan wet and moist tundra sedge

species. Ecography 18, 259–275.

Simard, S.W., Perry, D.A., Jones, M.D., Myrold, D.D., Durall, D.M.,

Molina, R., 1997. Net transfer of carbon between ectomycorrhizal tree

species in the field. Nature 388, 579–582.

Smit, E., Leeflang, P., Glandorf, B., van Elsas, D.J., Wernars, K., 1999.

Analysis of fungal diversity in the wheat rhizosphere by sequencing of

cloned PCR-amplified genes encoding 18S rRNA and temperature

gradient gel electrophoresis. Applied and Environmental Microbiology

65, 2614–2621.

Smith, R.I.L., 1994. Species-diversity and resource relationships of South

Georgian fungi. Antarctic Science 6, 45–52.

Smith, V.R., Steenkamp, M., 1990. Climatic change and its ecological

implications at a subantarctic island. Oecologia 85, 14–24.

Steiman, R., Frenot, Y., Sage, L., SeigleMurandi, F., Guiraud, P., 1995.

Contribution to the knowledge of the mycoflora of Kerguelen Islands.

Cryptogamie Mycologie 16, 277–291.

Straatsma, G., Ayer, F., Egli, S., 2001. Species richness, abundance and

phenology of fungal fruit bodies over 21 years in a Swiss forest plot.

Mycological Research 105, 515–523.

Taylor, J.W., Turner, E., Townsend, J.P., Dettman, J.R., Jacobson, D.,

2006. Eukaryotic microbes, species recognition and the geographic

limits of species: examples from the kingdom Fungi. Philosophical

Transactions of the Royal Society B 361, 1947–1963.

Thormann, M.N., 2006. Diversity and function of fungi in peatlands: a

carbon cycling perspective. Canadian Journal of Soil Science 86,

281–293.

Thorn, R., Reddy, C., Harris, D., Paul, E., 1996. Isolation of saprophytic

basidiomycetes from soil. Applied and Environmental Microbiology

62, 4288–4292.

Tibbett, M., Sanders, F.E., Minto, S.J., Dowell, M., Cairney, J.W.G.,

1998. Utilisation of organic nitrogen by ectomycorrhizal fungi

(Hebeloma spp.) of arctic and temperate origin. Mycological Research

102, 1525–1532.

Tojo, M., Nishitani, S., 2005. The effects of the smut fungus

Microbotryum bistortarum on survival and growth of Polygonum

viviparum in Svalbard, Norway. Canadian Journal of Botany 83,

1513–1517.

Tosi, S., Casado, B., Gerdol, R., Caretta, G., 2002. Fungi isolated from

Antarctic mosses. Polar Biology 25, 262–268.

Tosi, S., Onofri, S., Brusoni, M., Zucconi, L., Vishniac, H., 2005.

Response of Antarctic soil fungal assemblages to experimental

warming and reduction of UV radiation. Polar Biology 28, 470–482.

Vandenkoornhuyse, P., Baldauf, S.L., Leyval, C., Straczek, J., Young,

J.P.W., 2002. Extensive fungal diversity in plant roots. Science 295,

2051.

Vare, H., Vestberg, M., Eurola, S., 1992. Mycorrhiza and root-associated

fungi in Spitsbergen. Mycorrhiza 1, 93–104.

Vaughan, D.G., 2006. Recent trends in melting conditions on the

Antarctic Peninsula and their implications for ice-sheet mass

balance and sea level. Arctic, Antarctic and Alpine Research 38,

147–152.

Vishniac, H.S., 1996. Biodiversity of yeasts and filamentous microfungi in

terrestrial Antarctic ecosystems. Biodiversity and Conservation 5,

1365–1378.

Vonlanthen, C.M., Walker, D.A., Raynolds, M.K., Kade, A., Kuss, P.,

Daniels, F.J.A., Matveyeva, N.V., 2007. Patterned-ground plant

communities along a bioclimate gradient in the High Arctic, Canada.

Phytocoenologia, in press.

Walker, M.D., Wahren, C.H., Hollister, R.D., Ahlquist, L., Alatalo, J.M.,

Bret-Harte, M.S., Calef, M.P., Callaghan, T.V., Carroll, A., Copass,

C., Epstein, H.E., Henry, G.H.R., Jonsdottir, I.S., Klein, J.,

Magnusson, B., Molau, U., Oberbauer, S.F., Rewa, S.P., Robinson,

C.H., Shaver, G.R., Suding, K.N., Tolvanen, A., Totland, Ø., Turner,

P.L., Tweedie, C.E., Webber, P.J., Wookey, P.A., 2006. Plant

community responses to experimental warming across the Tundra

Biome. Proceedings of the National Academy of Sciences, USA 103,

1342–1346.

Wallenstein, M.D., McMahon, S., Schimel, J., 2007. Bacterial and fungal

community structure in Arctic tundra tussock and shrub soils. FEMS

Microbiology Ecology 59, 428–435.

Warcup, J.H., 1950. The soil plate method for isolation of fungi from soil.

Nature 166, 117–118.

Watling, R., 1995. Assessment of fungal diversity: macromycetes, the

problems. Canadian Journal of Botany 73, S15–S24.

Watling, C., Watling, R., 1988. Svalbard Fungi. The British Schools’

Exploring Society Report 1987–1988. Royal Geographical Society,

Kensington Gore, UK.

ARTICLE IN PRESSK.E. Ludley, C.H. Robinson / Soil Biology & Biochemistry 40 (2008) 11–29 29

WeiX, M., Selosse, M.-A., Rexer, K.H., Urban, A., Oberwinkler, F., 2004.

Sebacinales: a hithero overlooked cosm of heterobasidiomycetes with a

broad mycorrhizal potential. Mycological Research 108, 1003–1010.

Widden, P., Parkinson, D., 1979. Populations of fungi in a high arctic

ecosystem. Canadian Journal of Botany 57, 2408–2417.

Wu, C., Hsiang, T., 1999. Mycelial growth, sclerotial production and

carbon utilization of three Typhula species. Canadian Journal of

Botany 77, 312–317.

Wynn-Williams, D.D., 1980. Seasonal fluctuations in microbial activity in

Antarctic moss peat. Biological Journal of the Linnean Society 14,

11–28.

Wynn-Williams, D.D., 1990. Ecological aspects of Antarctic microbiol-

ogy. Advances in Microbial Ecology 11, 71–146.

Yergeau, E., Bokhorst, S., Huiskes, A.H.L., Boschker, H.T.S., Aerts, R.,

Kowalchuk, G.A., 2007. Size and structure of bacterial, fungal and

nematode communities along an Antarctic environmental gradient.

FEMS Microbiology Ecology 59, 436–451.

Zak, D.R., Kling, G.W., 2006. Microbial community composition and

function across an arctic tundra landscape. Ecology 87, 1659–1670.

Zucconi, L., Pagano, S., Fenice, M., Selbmann, L., Tosi, S., Onofri, S.,

1996. Growth temperature preferences of fungal strains from Victoria

Land, Antarctica. Polar Biology 16, 53–61.