Arctic Biodiversity Assessment

Home , Flavocetraria, Graphis scripta, Helotiales, Hygrocybe conica, Melampsora, Pezizales

354 Arctic Biodiversity Assessment

The golden colored blackening waxcap Hygrocybe conica var. aurantiolutea is a colorful member of waxcaps that grows in grasslands in the low and sub-Arctic zones. At appropriate climatic conditions, the cryptically growing long-lived mycelia produce sporocarps in August-September. Waxcaps are sensitive to nitrogen, and their occurrence is strongly reduced in temperate and boreal zones due to anthropogenic deposition of nitrogen and fertilization. Tasiusaq at Qassiarsuk in South Greenland, 1987. Photo: Flemming Rune. 355

Chapter 10 Fungi

Lead Authors Anders Dahlberg and Helga Bültmann

Contributing Authors Cathy L. Cripps, Guðríður Gyða Eyjólfsdóttir, Gro Gulden, Hörður Kristinsson and Mikhail Zhurbenko

Contents

Summary ��356 I want to tell you something I learned about plants from 10.1. Introduction ��356 » the late Kakkik that I tried myself. My sister’s late husband 10.2. Status of knowledge ��356 used to know about nirnait, caribou lichen, the plants that 10.2.1. Fungal life strategies and ecosystem functions ��356 caribou eat. They are long and you pull them out. They 10.2.2. Fungal properties and adaptations to Arctic conditions ��358 tend to grow in swampy areas. I boiled them when all the 10.2.3. Historic and present investigations ��359 people in our camp were sick. I was the only one up and 10.3. The fungi of the Arctic ��361 about when we were living in a fishing camp. My mother 10.3.1. Species richness ��361 10.3.2. Species richness in differentgeographical regions ��363 had been admitted to the hospital and we were waiting 10.3.3. Distribution of species within different Arctic zones ��363 for her return in August. Six of my family members were 10.3.4. Distribution of different life forms and at different sick in bed. I boiled some caribou lichen in a pot for a long substrates ��364 time, following my brother in-law’s advice. He told me to 10.3.5. Specificity to the Arctic and rarity ��364 stop boiling them when the water turned black. I waited 10.4. Trends, causes and prospects ��365 for them to cool down and I gave each sick person some 10.5. Conclusions and recommendations ��366 to drink. The next day, they were all up and about. Acknowledgements ��367 It looked like the cough syrup in a bottle. References ��367 Aalasi Joamie in Joamie et al. 2001. 356 Arctic Biodiversity Assessment

SUMMARY will respond directly to changing composition, abundance and location of the vegetation. Similarly, terricol- Fungi are one of the most species-rich groups of organ- ous6 lichen communities will be affected by increased isms in the Arctic. While the occurrence, distribution competition from vascular plants. The changing veg- and ecology for lichenized fungi (lichens)1 are reason- etation will transform the fungal diversity and thereby ably well known, less is known about non-lichenized affect ecosystem services provided by fungi, such as fungi (normally just called fungi), including lichenicol- plant’s uptake of nutrients, decomposition and long-term ous fungi (fungi living on lichens)2 and in particular, carbon sequestration in soil, although unknown how microfungi3. The known number of fungal species in and to what degree. The conservation status of Arctic the Arctic is presently about 4,350, of which 2,600 are fungi is predicted to scarcely be affected within the next macrofungi4 and 1,750 are lichens, the rest are micro- decades but greatly changed over the long term. fungi. The fungi have largely a cryptic life form and have therefore not been exhaustively inventoried. Hence, total fungal-species richness in the Arctic may exceed 10.1. INTRODUCTION 13,000. Local species richness is typically high and can be very high, e.g. about 50 lichen species on less than 1 Fungi are an extraordinary group of organisms. They m2. Most species appear to be present throughout the constitute a large portion of Arctic biodiversity and are Arctic, and they also occur in alpine habitats outside the essential in the functioning of Arctic terrestrial ecosys- Arctic, particularly in the northern hemisphere. Few tems. A substantial part of the fungi is lichenized and fungi are endemic to the Arctic. Of the lichens, 143 spe- generally termed lichens. The remaining part of the cies are listed as Arctic endemics, but it is likely that the fungi is in general terms just called fungi and will here major part will prove to be synonyms of other species. be referred to as fungi. Given favorable weather conditions, some may produce short-lived, sometimes promi- Fungi are pivotal in Arctic terrestrial food-webs. Mycor- nent, sporocarps (mushrooms), but predominantly, and rhizal, saprotrophic5 and pathogenic fungi drive nutri- for many species exclusively, they exist as cryptic and ent and energy cycling, and lichens are important for hidden mycelia in e.g. soil and in living or dead insect or primary production. Reindeer lichens Cladonia subgenus plant tissues. The most well-known group of fungi in the Cladina spp. form dominant vegetation types in many Arctic is the lichenized fungi (lichens) because they grow areas and function as keystone species. on substrate surfaces and often contribute conspicuously, and colorfully, to Arctic vegetation. This is particularly As for other inconspicuous organism groups, it is obvi- apparent in the high Arctic and in reindeer lichen7-domi- ously desirable to gain a better knowledge of the iden- nated vegetation types in the sub-Arctic. tity, occurrence and functions of fungal species, and particularly the large number of unrecorded species (mainly Here we review the knowledge and status of Arctic microfungi). An evaluation of the conservation status macroscopic fungi, i.e. visible sporocarps of fungi, and of Arctic fungi is feasible, and the mapping of rare and lichens. Microfungi constitute the most species-rich fun- endemic species is necessary. Enhanced monitoring and gal group in the Arctic, but are only briefly mentioned functional research would enable more accurate predic- due to scarcity of knowledge. tion of how fungal diversity and the ecosystem functions of fungi will develop with climate change. 10.2. STATUS OF KNOWLEDGE Effects of climate change on diversity of Arctic fungi are predicted to be gradual but radical over time, due to changes in vascular plant flora and vegetation, especially 10.2.1. Fungal life strategies and ecosystem the expansion of shrubs. Most fungal species associate functions with living or dead parts of specific vascular plants and Fungi are heterotrophic, i.e. they cannot fix carbon but 1 Lichenized fungi live in symbiosis with photosynthetic green need organic carbon for growth and therefore rely on algae or cyanobacteria and form stable structures called photosynthetically derived energy from plants, includ- lichens. ing algae and cyanobacteria. Their strategies to access 2 Lichenicolous fungi live exclusively on lichens, commonly as this energy are to be (1) mutualistic8 (i.e. to associate host-specific parasites, but also as broad-spectrum pathogens, saprotrophs or commensals. 3 Microfungi are defined as fungi either lacking known reproductive structures, with microscopic reproductive structures or small sporocarps, typically less than 2 mm. They consti- 6 Organisms living on or in the soil. tute the majority of known species and likely the overwhelm- 7 Despite being lichens, reindeer lichens are sometimes called ing majority of the yet unknown and undescribed fungi. “reindeer or caribou moss”. 4 Macrofungi are defined as fungi with visible, sporocarps, 8 Mutualism is a relationship between two species of organisms typically larger than 2 mm. in which both benefit from the association, e.g. fungi and 5 Saprotrophic organisms decompose dead plant, animal or plants in mycorrhizae and fungi and green algae or cyanobac- fungal tissues. teria in lichens. Chapter 10 • Fungi 357 with photosynthetic organisms), (2) endophytic9, (3) cetes and yeasts but also macrofungi (Ludley & Robinson saprotrophic (i.e. they decompose dead plant, animal or 2008). Hitherto, the information on microfungi has fungal tissues) or (4) parasitic. largely been restricted to culturable mycelia from soil and plants (Ludley & Robinson 2008). Molecular tools Fungal mutualism may be in the form of lichen or are now providing exciting opportunities to resolve the mycorrhiza. Lichens are an intimate, long-lived and diversity, distribution and function of fungal mycelia in stable association between fungi and green algae and/or the Arctic. The saprophytic macrofungi producing larger cyanobacteria. Each lichen species has a unique fungus sporocarps include puffballs Calvatia, funnels Clitocybe, or mycobiont that determines its appearance and proper- Galerina and Leptoglossum. Pyrenomycetes is a common ties as well as its taxonomy, while the photosynthetic group of saprophytic microfungi mostly apparent as symbionts (photobionts) consist of relatively few species black dots on dead plants that are frequent in the Arctic (148 according to Voytsekhovich et al. 2011), which are (Lind 1934, Savile 1963). globally widespread and sometimes free living (Nash 2008). Lichens are classified and named after their Fungal parasites are normally specialized microfungi at- fungal symbionts. The majority of Arctic vascular plants tacking plants, animals, in particular invertebrates, and species form different types of mycorrhizae (Gardes & sometimes also fungi. They may have large effects on the Dahlberg 1996, Newsham et al. 2009). The complex population sizes of their hosts, but have not been exten- mycorrhizal organ, consisting of plant root and fungal sively studied in the Arctic (but see Savile 1963). Exam- hyphae, enlarge the surface area for absorbing water and ples of Arctic parasites are rust fungi such as Melampsora nutrients from soil, explore for nutrients more exten- that commonly cause mortality of willows (Parmelee sively than vascular-plant roots, and mobilize organically 1989, Smith et al. 2004) and smuts (Ustilaginales), bound nutrients. The fungal association provides the parasitizing plants of Cyperaceae (Scholler et al. 2003). fungus direct access to the plant’s carbohydrates, while Another group of frequent pathogens in the Arctic are the plant gain benefits from improved mineral and water the snow molds that attack mosses and vascular plants absorption through the fungal mycelium. Ectomycorrhi- under snow-cover when plant resistance is lowered (Tojo zal fungi are common in the Arctic where they associ- & Newsham 2012). ate with roots of mountain avens Dryas spp., willows Salix spp., birch Betula spp. and alpine bistort Bistorta Fungi are pivotal for the cycling of carbon and nutrients spp. and in the sub-Arctic with additional species of (including N) in terrestrial ecosystems of the Arctic bushes and trees. Ectomycorrhizal fungi belong mostly (Ludley & Robinson 2008, Newsham et al. 2009). Until to genera forming conspicuous sporocarps, e.g. boletes recently, in ecological studies fungi were lumped with (e.g. Leccinum spp.), amanitas Amanita spp. and milk-caps other microbes into a ‘black box’, and both the identity Lactarius spp. Arbuscular mycorrhizae are widespread in and roles of fungi in Arctic regions were largely un- Arctic species of the true grasses Poaceae, the butter- known (Callaghan et al. 2004). The majority of Arctic cup family Ranunculaceae, the aster family Asteraceae, plants’ nutrient uptake is accomplished by mycorrhizal the saxifrage family Saxifragaceae and the rose family symbioses. Lichens are significant primary producers Rosaceae (e.g. Gardes & Dahlberg 1996, Olsson et al. in the Arctic, and their contribution of biomass ranges 2004, Ormsby et al. 2007, Peters et al. 2010, Walker et from 2% in low Arctic to over 18% in high Arctic al. 2010). Ericoid mycorrhizae are widespread in Arctic tundra and 65% in polar desert habitats (Webber 1974, species of the heather family Ericaeae, e.g. huckleberry Longton 1988). The proportion of Arctic vegetation Vaccinium spp., bell-heather Cassiope spp. and crowberry biomass associated with mycorrhizal fungi has been Empetrum spp. (Walker et al. 2011). The fungal symbionts estimated to range from 17% to 100% (Olsson et al. in arbuscular and ericoid mycorrhizae are microfungi 2004). The cyanobacterial photobionts of Arctic lichens and typically need microscopic root examination to be contribute significantly to nitrogen fixation (Crittenden seen, or molecular tools to be detected and identified. & Kershaw 1978). Note that while the fungal part in lichens constitutes the major part of the lichen biomass, The few studies conducted of Arctic fungal endophytes the mycorrhizal fungi constitute only a minute part of indicate a high species diversity, e.g. in above ground the plant biomass. tissues of mountain avens (Higgins et al. 2007) and associated with Arctic plant roots, as so called dark septate The decomposition of dead organic matter and recy- endophytes (Newsham et al. 2009). Recently, fungal cling of nutrients in Arctic terrestrial systems is mainly endophytes have been found common in lichen thalli conducted by saprotrophic fungi, with contributions (Arnold et al. 2009, U’ren et al. 2010). by mycorrhizal fungi, and to a lesser degree by bacteria (Ludley & Robinson 2008, McMahon et al. 2009). Saprotrophic fungi are characterized by their depend- Fungi have a major advantage over bacteria in this regard ence on dead organic materials as sources of energy and due to their ability to redistribute nutrients and car- nutrients. They consist predominantly of microfungi, in- bohydrates within their extended hyphae and thereby cluding a large number of anamorphic (asexual) ascomy- overcome spatial deficiencies.

9 Fungal endophytes are microfungi living inside plants with- The presence and diversity of fungal species is largely out causing apparent symptoms. determined by the distribution, diversity and abundance 358 Arctic Biodiversity Assessment of vascular plants and for lichenicolous fungi10 of the Porpidia and a fruticose reindeer lichen, Cladonia arbus- lichens. Fungi parasitizing insects rely on the occurrence cula (Werth 2010). Most Arctic rock-dwelling crustose of their host animals. Some fungal species are confined lichens reproduce sexually and are dispersed by spores to a single plant species, whereas others may associ- (Fahselt et al. 1989). ate with a few or several plant species. The majority of Analyzing the increment of thallus radius over time Arctic lichenicolous fungi are confined to one lichen (Rhizocarpon geographicum is frequently used in lichenom- genus (Zhurbenko 2010a). On the other hand, common etry), large thalli of rock-dwelling crustose lichens have Arctic lichen species or genera may host many lichenicol- been estimated to be up to several thousands years old ous fungi (e.g. about 20 on Stereocaulon spp. or Thamnolia (Matthews & Trenbirth 2011). These estimations are spp.; Zhurbenko 2010b, 2012). Lichens ecologically re- based on circumstantial evidence and linear extrapo- semble bryophytes. Their distribution depends primarily lation of growth rates derived from data for several on habitat conditions (e.g. substrate type: rock-soil-bark, decades or a few centuries. It is possible that exception- pH, microclimate, etc.) and competition by other plant ally large crustose lichen thalli may be formed by the species. coalescence of neighbouring thalli rather than by slow radial growth and are not genetic ‘individuals’, though 10.2.2. Fungal properties and adaptations to this is not probable for R. geographicum (e.g. Clayden 1997). Similar estimates of potential longevity of rein- Arctic conditions deer lichen genotypes are not possible, as the older por- tions at the base of thalli decay after about 30 years (Holt The short growing season and restricted opportunities & Bench 2008). The annual growth of Arctic-alpine for reproduction in the Arctic is thought to have selected lichen thalli is seldom expressed as a change in surface for high longevity in individual fungi, slower population area, thickness or biomass. Usually, it is measured and growth, and hence lower turnover than in more produc- reported as a radial change that ranges from 0-0.5 mm tive biomes (cf. Gardes & Dahlberg 1996). Local spread- per year in some crustose species (e.g. R. geographicum) ing relies primarily on mycelial growth or asexual spores to about 6 mm per year in reindeer lichens (Pegau 1968, rather than sexual reproduction. Population dynamics Werner 1990, Armstrong & Bradwell 2010, Matthews & of fungi have not been studied in the Arctic, but may be Trenbirth 2011, Bültmann & Daniëls 2012). inferred from boreal and temperate biomes (cf. Dahlberg & Mueller 2011). There, soil-inhabiting fungal genotypes Arctic fungi have evolved physiological mechanisms to may potentially, in stable conditions, exist for years, cen- maintain mycelial activity and growth at low tempera- turies or even longer as mycelia. Furthermore, patterns tures and low water potential (Robinson 2001). Even of sporocarp fairy rings and molecular studies reveal that when soils are frozen, microbial processes in the Arctic genotypes of mycorrhizal and other soil-dwelling mac- continue. Fungi contribute 10 times more to Arctic soil rofungi typically extend from a few to several hundred microbial biomass than cohabiting bacteria. Microbial square meters. In contrast, substrate-bound saprotrophic processes, i.e. predominantly of fungal origin, reach and pathogenic fungi are restricted in age and space. their annual peak under snow (e.g. Schadt et al. 2003), However, they may also disperse by asexual spores and take up carbon from the environment and grow in fro- sometimes as mycelia by insects, enabling genotypes to zen soils at least down to -2 °C (McMahon et al. 2009). spread and persist longer than their host substrates. Arctic lichens may have a positive net primary photosynthesis balance at low temperatures (many studies by Many lichen genotypes can most easily disperse by K.A. Kershaw and co-workers, e.g. Larson & Kershaw thalli fragmentation, and subsequently be transported 1975, Kershaw 1985), even under snow and ice, and by wind, water or animals over considerable distances. survive extremely low temperatures and levels of water Some lichens even have specialized organs for frag- content (Kappen et al. 1996, Sommerkorn 2000). mentation composed of fungal hyphae and algal cells, i.e. isidia, small thallus outgrowths that easily break Arctic and alpine ectomycorrhizal mushrooms spe- off, or soredia, smaller powdery propagules. Hence, cies have evolved substantially smaller sporocarps and whereas single genotypes are localized in soil-dwelling a reduced number of gills compared with their forest fungi, they are typically more scattered and dispersed counterparts, probably as a response to restricted as- in lichens (e.g. Scheidegger & Werth 2009, Geml et al. similate accessibility and the dry, harsh environmental 2010). Significant genetic differentiation at the landscape conditions (Knudsen 2006). Similarly, sporocarps of level has been shown in two Arctic lichens, a crustose many microfungi (observed in the pyrenomycete group) tend to be smaller in the Arctic (Savile 1963). The short growing season has also pushed parasitic species of Arctic 10 Lichenicolous fungi constitute a functional non-taxonomic rust and smuts to have simplified lifecycles, e.g. perennial group of mainly ascomycetes and rarely basidiomycetes or other groups that forms obligate associations with lichens, habits which enable growth as soon as the season starts as commensals, parasites or rarely saprotrophs. They are (Lind 1927, Savile 1982). Finally, lichenization is rela- typically included in lichen checklists. Infection of lichens is tively more common in Arctic than in temperate areas. very obvious in some Arctic vegetation types, e.g. snow beds. For example, the number of lichens vs. the number of Thus, lichenicolous fungi could be expected to influence the macrofungi is about 1:1 in Greenland and 1:2 in Great growth of lichens (see Lawrey & Diederich 2003). Britain (Knudsen 2006), and the percentage of lichenized Chapter 10 • Fungi 359 fungi of all known fungi is about 20% at the global level help to increase knowledge of Arctic mycology by and 35% for the Russian Arctic (Zhurbenko 2010a). complementing studies based on sporocarps or mycelial isolations (Fujimura et al. 2008, Bjorbækmo et al. 2010, 10.2.3. Historic and present investigations Fujiyoshi et al. 2011, Walker et al. 2011, Geml et al. 2012, Timling et al. 2012). The first overviews of Arctic fungi were published for Svalbard by Karsten (1872) and for Greenland by The history of lichenological exploration of the Arctic Rostrup (1888) (for an extensive overview, see Elvebakk is long. Lichens are easy to collect and preserve, and & Prestrud 1996, Gulden & Torkelsen 1996, Knud- samples were brought home even by early Arctic expedi- sen 2006). A brief history of the early mycology in the tions. Therefore, the distribution of lichens is reasonably Canadian Arctic is presented by Savile (1962). Due to well known, though crustose microlichens are underrep- the ephemeral and irregular occurrence of sporocarps resented. The distribution of their associated lichenicol- combined with the low accessibility for humans to the ous fungi is much less known (Zhurbenko 2009a). The Arctic, macrofungi are collected with considerably first major work was a lichen flora of Arctic Europe and less frequency than lichens, and hence the knowledge Greenland (Fries 1860). Details of lichen exploration of their distribution and ecology is correspondingly are reported in several checklists and floras (e.g. Lynge lower. Regional species lists are available for Greenland, 1947, Krog 1968, Thomson 1979, 1984, 1990, 1997 for Iceland, Svalbard and the Russian Arctic, but a com- North America, Elvebakk & Hertel 1996 for Svalbard, bined checklist for Arctic fungi has not yet been com- Printzen 2008 for a summary). Greenland is represented piled (Elvebakk & Prestrud 1996, Karatygin et al. 1999, by many floristic studies (e.g. Alstrup 1982, 2005, Hallgrímsson & Eyjólfsdóttir 2004, Borgen et al. 2006, Alstrup et al. 2000, numerous papers by E.S. Hansen, as Hallgrímsson 2010). Unfortunately, regional lists cannot Hansen 2008, Hansen et al. 1987). Recently, a Panarctic easily be combined because of varying taxonomy. There- Lichen Checklist including their associate lichenicolous fore, knowledge of macrofungal distribution is presented fungi was compiled by Kristinsson et al. (2006, 2010). at the level of Arctic Russia, Greenland and Svalbard. The exploration of Arctic lichenicolous fungi is reviewed Iceland is also considered, although most of that country by Zhurbenko (2010a). The diversity of lichenicolous is classified as sub-Arctic. The Russian Arctic fungal fungi is relatively well known for Greenland, Svalbard checklist also includes species from the sub-Arctic and and Russia (Alstrup & Hawksworth 1990, Alstrup & reports the recorded species numbers in the Arctic Elvebakk 1996, Zhurbenko & Santesson 1996, Lawrey proper to be 20-30% less than when the sub-Arctic is in- & Diederich 2003, Alstrup 2005, Zhurbenko 2007, cluded (Karatygin et al. 1999). No comprehensive check- 2009a, 2009b, 2010a). list exists for the main North American Arctic, although the distributions of some Arctic species in Canada are General characteristics of Arctic macrolichen11 com- reported by Redhead (1988). Arctic species tend to have munities have been summarized for lichen-rich vegeta- wide distributions, more or less throughout the Arctic tion in general (Ahti & Oksanen 1990), in Alaska (Holt (experiences by authors and e.g. Lind 1934, Cripps & et al. 2007), on rock in Greenland (Daniëls 1975) and Horak 2006, 2010, Ronkier & Ronkier 2010). for Arctic terricolous lichen communities (e.g. Nimis 1981, 1985, Daniëls 1982, Bültmann 2005, Bültmann & Information on fungal specimens in Arctic herbaria Daniëls 2009). is increasingly accessible through the global biodiversity information facility, GBIF (2012), but is still very Lichens are established bioindicators for air purity (e.g. incomplete. To promote the development of Arctic and Nimis et al. 2002), but effects of air quality on species alpine mycological knowledge, mycologists have co- composition of Arctic lichen have not been reported. operated in the International Symposium of Arcto-alpine Lichens have been used as accumulation indicators for Mycology network (ISAM) since 1980 and have arranged contaminants such as heavy metal cations, radionuclides, nine symposia with more than 100 participants in total nitrogen, sulphur and organic compounds in the Arctic and almost 100 scientific papers presented (Laursen & (e.g. Nash & Gries 1995, Walker et al. 2003). Ammirati 1982, Laursen et al. 1987, Petrini & Laursen 1993, Mukhin & Knudsen 1998, Boertmann & Knudsen Monitoring of fungi has not taken place in the Arctic. 2006, Høiland & Økland 2008, Cripps & Ammirati Two local monitoring studies in Greenland that include 2010). lichens show no trends for any aspect of lichen diversity as yet (Elberling et al. 2008 for 1997-2007 at Zacken- By necessity, Arctic mycological research has been pri- berg, Daniëls et al. 2011 from 1968 to 2007 in Ammas- marily exploratory, focusing on identification, descrip- salik). The site at Zackenberg is continuously monitored tion and recording of fungal taxa. Few analyses of pat- (Hansen 2006, Elberling et al. 2008), and monitoring terns and dynamics of macrofungal communities and of Arctic fungal ecology have been made (e.g. Lange 1957, 11 Macrolichen are defined as foliose (including squamulose) and Petersen 1977). Recent advancements in molecular ap- fruticose lichens, which can mostly be identified macroscopi- proaches enable the detection, genetic characterization cally, while microlichens are crustose lichens, mostly visible and quantification of fungi in environmental samples, to the naked eye, but require microscopical means to be e.g. soil and plant tissues. These data will significantly identified. 360 Arctic Biodiversity Assessment

Box 10.1. Lichens and reindeer

Reindeer or caribou depend on lichens as winter food (e.g. Large Herbivore Network 2012). The ability of lichens, as of Llano 1956, Inga 2007). Reindeer dig through the snow to other fungi, to accumulate cations of heavy metals including feed on soil lichens. Most important are the reindeer lichens radioactive elements is also problematic. Thus reindeer kept i.e. species of Cladonia, subgenus Cladina, and Stereocaulon for human consumption should not graze in areas subjected spp. (see Box 10.1 Fig. 1). In boreal areas, reindeer also feed to pollution with heavy metals. Especially in the sub-Arctic, on lichens on tree trunks and twigs. Only older forests have the availability of and access to lichens for the reindeer of the enough epiphytic lichen biomass for food. Long-term studies indigenous peoples in the north of Eurasia is a complex and showed a significant decrease of reindeer food lichens in sometimes politically difficult topic. Some state-imposed Alaska (Joly et al. 2009). Higher winter temperatures caused reindeer management systems, such as the Paliskunta- by climate change will cause an increase in ice on top layers system in Finland, have disrupted the traditional knowl- of snow by refreezing or rain making it more difficult for rein- edgeable management of pastures, which has led to severe deer to dig out the lichens (e.g. Putkonen & Roe 2003 and depletion of lichen in some areas (Mustonen et al. 2011).

Box 10.1 Figure 1. Terricolous lichen vegetation is suitable for reindeer with reindeer lichens (here Cladonia mitis & C. rangiferina), Stereocaulon spp. and Flavocetraria cucullata. Photo: Helga Bültmann, Narsarsuaq, S Greenland. Chapter 10 • Fungi 361 results are published regularly in annual reports (e.g. Table 10.1. Known and estimated total species richness of Arctic Hansen 2006). fungi.

Fungal Taxonomic and Known total Estimated Wild mushrooms have rarely been used by indigenous group functional group number of total number Arctic peoples in the past (e.g. as hallucinogen: an species of species Amanita species by Chukchi shamans (M.P. Zhurbenko Lichens 1,7501 ~1,7502 unpubl.), Amanita muscaria and the shelf fungus Polypo- 3 4 5 rus sulphureus in Yakutia (Jakutija 2007) and species of Fungi >2,600 11,000 puffball for the treatment of wounds and cuts (Joamie et Chytridiomycota 83 al. 2001, Cuerrier & the Elders of Kangiqsujuaq 2011). Zygomycota 45 Only during the last decades have interest and use de- Glomeromycota 11 veloped for edible mushrooms, for example in Chukotka Ascomycota 1,245 due to Russian immigration (Yamin-Pasternak 2007). Basidiomycota 837

6 7 In contrast, lichens have historically been used fre- Lichenicolous fungi 373 >440 quently as mild antibiotics (e.g. Cetraria islandica and the Non-lichenized 2,0308 reindeer lichens) in medicine and food preserving, as macrofungi food when half-digested in the stomachs of ruminants Total number of Arctic fungi >4,350 >13,000 and, occasionally undigested, but mostly as famine food 1) The mycobionts of lichens predominantly consist of ascomycetes, but (e.g. ‘rock tripes’ Umbilicaria spp.), as dyes and as fuel or here they are treated as a functional group and not included in the tinder or even soap (Llano 1956, Oswalt 1957, Richard- taxonomic groups (Appendix 10.1). son 1974, Søchting 1990, Joamie et al. 2001, Cuerrier 2) Svalbard and W Greenland are the two best know areas where & the Elders of Kangiqsujuaq 2011). A concise summary macrolichens are considered to be completely sampled, constituting and bibliography of lichen use is compiled by Sharnoff 31% and 37%, respectively, of the known number of lichen species, (2012). Terricolous macrolichens are the main sources of mean 34%. Macrolichens also constitute 34% of the known number of Arctic lichens, and thus we expect the total number of lichens in food for reindeer and caribou with Rangifer tarandus (Box the Arctic not to be much higher than the known number. 10.1) constituting 70-75% of their annual diet, and pe- 3) Fungi refer to non-lichenised fungi. riodically also used by other species including muskoxen 4) Calculated from the highest number of known species for each fun- Ovibos moschatus, lemmings (subfamily Arvicolinae) and gal group in Greenland, Iceland, Svalbard or Arctic Russia. hares Lepus spp. (Llano 1956). Even mushrooms such as 5) Estimated from the suggested relationship between vascular plant bolete species of Leccinum contribute to the summer diet and fungi 1:5(-1:7) (Hawksworth 2001, Schmit & Mueller 2007. of reindeer (Knudsen 2001). 6) Lichenicolous fungi are predominantly ascomycetes, but are here treated as a functional group and not included in the taxonomic groups (Appendix 10.1). 7) Estimated from a relationship of 4:1 between lichens and lichenicol- 10.3. THE FUNGI OF THE ARCTIC ous fungi (after Zhurbenko 2007 and Diederich et al. 2011). 8) Sum based on the species richness of macrofungi of Ascomycota 10.3.1. Species richness (e.g. not anamorphic taxa) and Basidiomycota (cf. Tab. 10.2) and lichenicolous fungi. The total number of known fungal species in the Arctic is > 4,350 (Tab. 10.1). Of these, 1,750 are lichens and about 2,600 are fungi12. Lichens consist almost exclusively of ascomycetes, while in fungi most are ascomycetes and 837 are basidiomycetes. About 2,030 of the fungal ascomycetes and basidiomycetes are macrofungi worth 2007, Blackwell 2011). However, it has been es- (non-systematic group), while the rest are microfungi timated that more than 90% of the global fungal species consisting mainly of ascomycetes but also some Chytridi- remain to be discovered and described, and the current omycota, Zygomycota and Glomeromycota plus rusts working estimate suggests that their number on the and smuts (Tab. 10.2). 373 of the fungi have a lichenicol- Earth is at least 700,000 and likely 1.5 million (Hawks ous life form. worth 2001, Schmit & Mueller 2007). These authors suggest a general relation between numbers of species of These figures correspond to 4% of the globally known fungi to vascular plants to be 5-8:1. The status of lichens total number of fungi (> 99,000), but as much as 10% is rather well known in contrast to that for fungi. Micro- of the globally known lichens and > 20% of the glob- fungi are particularly poorly investigated. In the Arctic, ally known lichenicolous fungi (Tab. 10.1; Hawksworth 2,218 vascular plant species have been recorded, which 2001, Lawrey & Diederich 2003, Feuerer & Hawks- is roughly half as many species as for fungi (cf. Daniëls et al, Chapter 9). With a proportion of 6:1 of fungi:plants, 12 We conservatively estimate the number of (non-lichenized) the number of fungi would amount to ca. 13,000 fungal fungal species in the Arctic to be the highest species number species in the Arctic. recorded for each of the major taxonomic groups in the exist- ing regional checklists. 362 Arctic Biodiversity Assessment

Table 10.2. Compilation of reported number of fungi (non-lichenized fungi) species from different Arctic regions. No compilation exists for the main North America.

Fungal group Iceland1 Greenland2 Svalbard3 Arctic Highest number used to Russia4 infer known number of Arctic species Chytridiomycota 83 3 3 83 Zygomycota 45 15 27 45 Glomeromycota 11 11 Ascomycota 620 680 226 800 Pyrenomycetes (180) (470) 470 Leotiales (200) (100) 200 Pezizales (150) (50) 150 Anamorphic 425 200 103 300 425 Basidiomycota 716 837 201 650 837 Lichenicolous fungi5 14 231 75 1406 3737 Total number of known non-lichenized fungi 1,903 1,947 635 1,890 2,594 Known number of macrofungi 1,350 1,579 502 1,410 2,030

1) Hallgrímsson & Eyjólfsdóttir 2004, Hallgrímsson 2010. Lichenicolous fungi refers to low Arctic in Iceland, other fungal groups refer to all of Iceland (low and sub-Arctic). 2) Borgen et al. 2006, Knudsen 2006. 3) Elvebakk & Prestrud 1996. 4) Karatygin et al. 1999. 5) Consists mainly of ascomycetes, but includes also basidiomycetes (Appendix 10.1). 6) Zhurbenko 2010a reports 250 species for the Russian Arctic, however including areas not corresponding with the Arctic as defined here (e.g. with Kola Peninsula). 7) Known Arctic species richness (Appendix 10.1).

a) b)

239 160 Beringia 559 669 1,039 337 662 369 223 Eastern 247 Siberia 376 791 701 Canada 941 490 342 624 457 173 299 European 476 Russia & 383 551 366 western 778 Siberia 253 North Atlantic 791 1,038 491 1,382 650 156 613 375

Figure 10.1. Species richness of lichens in Arctic (a) sectors and (b) floristic provinces. Provinces are shown with different colors (n = 1,750). Continental species richness: North America 1,026, Greenland 1,136, Europe 1,075 and Asia 1,178. Chapter 10 • Fungi 363

10.3.2. Species richness in different Table 10.3. Species richness of lichens in sub-, low and high Arctic geographical regions Greenland on different substrates (n = 1,694 species, distribution unknown for 56 species). All sub- Bark Wood Soil Rock The distributions of Arctic lichens and lichenicolous fungi strates are known in greater detail than those of other fungi (Fig. High Arctic 1,230 101 33 358 738 10.1 and 10.2). The two best investigated areas concern- Low Arctic 1,450 215 53 413 769 ing fungal diversity are Greenland and Svalbard with high Sub-Arctic 671 88 25 211 347 documented species richness for fungi, lichens and their Greenland associated lichenicolous fungi (Tab. 10.2, Fig. 10.1 and Exclusively sub-Arctic Greenland: 32 species, low Arctic: 432 species; 10.2). W Greenland is accessible from the coast and has high Arctic: 204, in low & high Arctic: 1,018 species, sub- & high Arctic: been intensively studied historically and in recent years. It 8 species. includes a small area with sub-Arctic birch forests in the very south, but only about 30 lichen species and 200 fungi are exclusively found in this sub-Arctic enclave (Jensen 2003). Svalbard is rather small and consists exclusively of high Arctic habitats. It has attracted many lichenologi- 10.3.3. Distribution of species within cal and mycological studies (e.g. Øvstedal et al. 2009, different Arctic zones Bjorbækmo et al. 2010, Geml et al. 2012). No compilation of fungi is available from the main American Arctic, Knowledge of the distribution of fungal species in the but a molecular study of ectomycorrhizal roots from 326 low and the high Arctic, respectively, is fragmentary and plants of Arctic willow Salix arctica and mountain avens has not yet been compiled and analyzed. However, these Dryas octopetala collected along a gradient from the low to species are largely dependent on the occurrence and the high Arctic in north America identified 242 different abundance of plants, and hence their distribution may ectomycorrhizal fungal species and no decline in species be inferred from the distribution of plants. Plant species richness (Timling et al. 2012). richness and abundance decline from the low to the high Arctic, which support 2,183 and 111 species of vascu- The difference in the number of recorded species among lar plants, respectively (Daniëls et al., Chapter 9). The regions is due to several factors, including area size, the occurrence of specific plant species determines which diversity and number of different habitats, and rela- species may be present, and different plant species are tive survey effort. The relatively lower species richness associated with different numbers of fungi. High Arctic in many of the vast Arctic areas in North America and root-associated fungal communities are reported to be Russia, for example, is probably caused by fewer surveys quite distinct for six plant species (Fujimura & Egger having been conducted there. 2012). In contrast, the two principal ectomycorrhizal Arctic plants, mountain avens and arctic willow, form ectomycorrhizae with more than 250 fungal species that they largely share (Bjorbækmo et al. 2010, Timling et al. 2012). 5 56 24 84 The distribution of Arctic lichens is better known than 41 that of fungal species. Almost 60% of the lichen species 28 44 occur in both the low and the high Arctic (Tab. 10.3). 18 On average, lichen species richness declines by 15% 15 from low to high Arctic in contrast to species richness 83 34 in vascular plants, which declines by 95% (Tab. 10.3; Daniëls et al., Chapter 9). Most of the decline in lichens 5 67 140 is among species growing on bark and wood and there is 32 some decline among species growing on soil and rocks. 43 16 54 In some high Arctic areas, e.g. in Canada and Svalbard, 0 20 49 lichen species richness can be higher than in the low 75 Arctic (Appendix 10.2). 40 212 16 31 1 52 Arctic fungal diversity hotspots on a landscape scale are 14 not known, but compared with the low plant diversity in Arctic communities, the species richness and hetero- Figure 10.2. Species richness of lichenicolous fungi in Arctic geneity of lichen communities is high (e.g. Lünterbusch floristic provinces. Species richness in Arctic sectors: Beringia 157, & Daniëls 2004, Bültmann 2005, Bjorbækmo et al. Canada 89, North Atlantic 256, European Russia & western Siberia 2010, Geml et al. 2012, Timling et al. 2012), as high as 90 and eastern Siberia 176 (see Fig. 10.1 for delimitation). Continen- in species-rich communities outside the Arctic such as tal species richness: North America 80, Greenland 231, Europe 111 calcareous grasslands (Bültmann 2011). and Asia 243. 364 Arctic Biodiversity Assessment

Table 10.4. Examples of Arctic studies documenting high small-scale species richness of lichens in relation to vascular plants and bryophytes within study plots of different size in homogeneous vegetation (Greenland: all low Arctic, Canada: high Arctic).

Country Total species richness Number of species thereof Reference within plot Lichens Vascular plants Bryophytes Greenland 70/0.16 m2 38 11 21 Lünterbusch & Daniëls 2004 Greenland 71/0.25 m2 47 9 15 Bültmann 2005 Greenland 83/4 m2 48 11 24 Lünterbusch & Daniëls 2004 Greenland 90/9 m2 56 18 16 Sieg et al. 2009 Canada 95/25 m2 40 17 38 Vonlanthen et al. 2008

Species richness of 700 lichens and of 100 lichenicol- (Bültmann 2010). In the Arctic, as in the other biomes, a ous fungi is documented for hotspots in mountain areas larger portion of lichen species grows on acidic substrates in the boreal zone, adjacent to Arctic areas (Elvebakk rather than on calcareous substrates (Appendix 10.2; see & Bjerke 2006: 709 lichens, 94 lichenicolous fungi in also Bültmann 2010). Most species of lichenicolous fungi N Norway, and Spribille et al. 2010: 668 lichens, 98 are found on lichens with soil or plant debris as substrate lichenicolous fungi in Alaska). Species richness in po- (for the Russian Arctic: 63%; Zhurbenko 2010a). Fewer tential Arctic hotspots could be expected to be slightly are associated with rock-dweller (33%) and bark/wood- lower because of the decline in the number of epiphytic dweller species (4%). Most Arctic lichens (66%) are lichens. However small-scale diversity in vegetation crustose, i.e. microlichens, while 34% are macrolichens study plots in the Arctic has been shown to be very high, (7% of squamulose, 13% of leaf-like (foliose) and 14% of in most cases due to a large number of lichens; up to small-shrubby (fruticose); Appendix 10.2). 50 species on less than 1 m2 (Tab. 10.4). For soil fungi, a molecular study detected 332 fungal taxa in 600 soil 10.3.5. Specificity to the Arctic and rarity cores in Svalbard (Geml et al. 2012). Few species if any, of fungi are exclusively confined to 10.3.4. Distribution of different life forms and the Arctic. The potential degree of endemism is probably less than 2% in fungi (H. Knudsen pers. com.). Some at different substrates genera and several species are predominately Arctic- alpine circumpolar in their distribution, while the re- The most well-known fungal life form in the Arctic is maining species also may occur in boreal and temperate lichens, comprising 40% of the known species, while habitats (Gulden & Torkelsen 1996, Knudsen 2006). The ectomycorrhizal fungi constitute at least 6% and licheni- distribution of 422 circumpolar Arctic microfungi was colous fungi about 9% of known species. The remain- reported and discussed by Lind (1927). More recently, ing known species are predominantly saprotrophic, circumpolar distribution has been examined and report- the majority litter- and soil-dwelling with a few wood- ed for a few species of Arctic macrofungi (Knudsen & inhabiting species, and only a few are parasitic species Mukhin 1998, Cripps & Horak 2006, Cripps et al. 2010, (e.g. rust and smuts). Most Arctic lichen species are rock Ronkier & Ronkier 2010, E. Larsson pers. com.). DNA dwellers (56%), followed by lichens on soil (26%), bark sequence analyses of the identity of Arctic ectomycor- (14%) and wood (4%; Appendix 10.2. The proportions rhizal fungi in mycorrhizal host roots imply that many of lichen species growing on these substrates are similar may be distributed globally and are found also in boreal, in boreal and temperate biomes, except for the propor- temperate and Mediterranean biomes (Geml et al. 2012, tion of ‘bark’ species which is higher there, about 30% Timling et al. 2012).

Increasing commonness in the Arctic Figure 10.3. The commonness of lichen species in the Arctic in four categories: very rare, rare, scattered and common. The sizes of the pie Very rare (834) Rare (261)Scattered (237) Common (357) Global occurrence charts correspond to the species number. The estimated global oc- currences of these species within Unknown (143) each category are shown within each pie chart (see Appendix 10.1; Rare (215) n = 1,691, insufficient data for 59 of the 1,750 known species in the Scattered - Arctic). common (1,333) Chapter 10 • Fungi 365

Table 10.5. Numbers of potentially endemic lichens in the Arctic together with lichen species that are rare outside the Arctic, distributed by low and high Arctic, province or sector and their life form. Only species with known distribution are included (n = 358; endemic: 143, rare: 215). For explanation of province and sector, see Fig. 10.1. Low High Only low Only high Only in Only in Microlichens Macrolichens 1 sector 1 province Endemic 83 103 36 56 84 72 125 18 Rare 152 138 41 48 98 80 174 41

Microlichens: crustose, Macrolichens: squamulose, foliose and fruticose

The majority of Arctic lichen species have more limited tundra, similar to related changes occurring in mid- distributions. About 25% are known from the entire latitude alpine regions (Wookey et al. 2009; see also Ims Arctic, a further 25% from three or four sectors (delimi- & Ehrich, Chapter 12). Altered vegetation drives fungal tations of sectors see Fig. 10.1), while 49% are known communities to change. Increasing productivity and in- from only one or two sectors. This is a wider distribu- creasing biomass in the low and the high Arctic – includ- tion than reported for vascular plants, for which about ing increasing shrub cover in the low Arctic – will result 70% of the taxa are found in one or two sectors and in increased fungal activity and biomass, alter composi- 10% in all five (Elven 2007 onwards). The lichen species tion of fungal communities and may subsequently affect known only from one geographic region are mostly very fungal ecosystem processes (e.g. Wallenstein et al. 2007, rare in the Arctic. Overall, 48% of the Arctic lichens Deslippe et al. 2011). These changes will mainly be a are classified as very rare in the Arctic (Appendix 10.2). response to altered composition of plants and increased The majority of those (64%) are common or scattered photosynthesis levels, but other biotic and abiotic factors outside the Arctic (Fig. 10.3). may also play roles.

At the moment, 143 lichen species are listed as Arctic It is obvious that the occurrence and abundance of fungi endemics (Appendix 10.1). Five of these are widely will track those of their associated plants, but so far distributed within the Arctic while the majority is the fungal consequences of climatically induced vegeta- classified as very rare (Appendix 10.1 and 10.2). These tion changes have only been studied to a limited extent Arctic endemics are mainly rock-dwelling microlichens (Pickles et al. 2012, Timling & Tayler 2012). One of the occurring in the high Arctic (Tab. 10.5). However, a few studies of vegetational changes and fungal diversity taxonomic revision is needed for many of these lichens in reports large effects on the composition and functions of order to settle their taxonomic status (Kristinsson et al. ectomycorrhizal fungi in an 18-year long-term experi- 2010). A recent critical reexamination of 52 rare lichen mental greenhouse warming of dwarf birch Betula nana taxa reported in Norway concluded that only 30% of (Deslippe et al. 2011). This experiment resulted in higher them were appropriately identified to the species level mycelia biomass in ectomycorrhizal fungi characterized and that the remaining were probably synonyms to more by mycelia of long distance exploration types and capac- common species (Jørgensen & Nordin 2009). ity to mobilize organic nitrogen (e.g. in webcaps Corti- narius spp.). At the same time, there was a reduction of Most lichens with scattered or common distribution fungi with mycelia of the contact exploration type, like in the Arctic are also scattered or common outside the brittle gills Russula spp.; these have an affinity to labile Arctic (Fig. 10.3). The 215 Arctic lichen species that are inorganic nitrogen. The authors infer that warming may rare outside the Arctic are predominantly rock-dwelling profoundly enhance decomposition of soil organic mat- crustose microlichens (Tab. 10.5). ter and increase the connectivity of dwarf birch through mycorrhizal networks of larger size. These changes may further facilitate shrub expansion by enhancing nitrogen 10.4. TRENDS, CAUSES AND acquisition and nutrient redistribution to dwarf birch. The reports of earlier spring and later autumn fruiting PROSPECTS behavior of macrofungi in Europe due to current climatic warming (Kauserud et al. 2008, 2010, 2012) reflect in- Arctic climate and vegetation, including fungal commu- creased fungal activities below ground; such changes are nities, have undergone major changes during past glacial also likely to take place in the Arctic. and interglacial periods (Lydolph et al. 2005, de Vernal & Hillaire-Marcel 2008). Fungal species have repeatedly The predicted profound influence of increased average disappeared and re-colonized the present Arctic, the air temperature and annual average precipitation in the fungi following their associated plants, and the lichens Arctic will have effects on ecosystem functions that are responding to availability of suitable habitats. There is difficult to predict (ACIA 2005). The effects on global growing evidence that the advance of flowering plant carbon cycling and atmospheric CO2 levels will signifi- vegetation is speeding up as is the ‘greening’ of Arctic cantly depend on how the diversity and functions of 366 Arctic Biodiversity Assessment fungal communities are affected due to their key roles al. 2009), but this is not yet apparent in the high Arctic in terrestrial carbon cycling (e.g. Ludley & Robinson (Cornelissen et al. 2001). 2008, Pickles et al. 2012). The uncertainty of how the large Arctic soil pool of carbon will change with chang- It is possible to infer potential future distribution of ing vegetation, soil temperature and permafrost will also fungi by combining predicted changes in habitat types or depend on (1) how vegetation patterns will change and vegetation cover in the Arctic with their ecology. Hence, feed back to climate, (2) how diversity of fungal and bac- it would be feasible to initiate monitoring programs for terial communities will change in relation to vegetation any of these fungal groups. Lichens would best be moni- change, and (3) how the subsequent fungal and bacterial tored through visual surveys (e.g. Elberling et al. 2008) carbon-cycling processes will be affected. It has recently and fungi through a combination of sporocarp observa- been reported that a major portion of stored carbon in tions and molecular analyses of environmental samples. boreal forests derives from roots and root-associated Recent advances in molecular methods, e.g. pyrose- microorganisms, probably with ectomycorrhizal fungi as quencing, efficient bioinformatics and increasing sizes of key-players (Clemmensen et al. 2013). As fungi similarly databases of fungal reference sequences are promising in may be important for the carbon flux in Arctic soils, this regard (e.g. Buee 2009, Geml et al. 2012, Timling et changing vegetation and fungal communities may affect al. 2012). Soil animals are increasingly being monitored the amount of stored carbon. Yet, the abundance, diver- using such methods (Heger et al. 2012). sity, functions and potential reactions to climate change of fungi in the Arctic are not well understood. The conservation status of macrofungi and lichens has not been evaluated for any fungal group at the circum- Lichens are autotrophic and less dependent on vascular polar level, for Arctic-alpine environments or at the plants, though some may compete with plants and some global level (IUCN 2012). None of the three globally ad grow on bark. The majority of lichen species, including hoc red-listed fungal species (two lichens and one fungal most endemic and rare species, grows on rock surfaces species) occurs in the Arctic (IUCN 2012). Given the and do not compete with vascular plants. Neverthe- relatively large distributional and ecological knowledge less, changes in temperature and moisture regime will of Arctic lichens (Kristinsson et al. 2010), a red-list gradually cause changes in the species composition of evaluation and the conservation status of Arctic lichens lichen communities. The Arctic epiphytic lichens may could be established. It is a challenge that many rare be favored by the spreading of shrubs and trees to the lichens are known only from ancient collections. The north, while terricolous lichens can be expected to face evaluation of conservation status should include detailed increasing competition from vascular plants. information about the distribution of rare and endemic Arctic lichens to avoid unintentional destruction of rare The recently established local long-term monitoring of lichens by e.g. construction works, such as reported by lichen communities at Greenland has not detected any Thomson (1997) as a possibility for a type locality in effects of climate change. In the Netherlands, long-term Alaska. Similarly, the conservation status of Arctic mac- monitoring of lichen communities has revealed changes rofungi, although based on substantially less knowledge, that are suggested to be partly due to warming since may for a large share of the species be evaluated based on 1990 with a rather rapid increase in some and a decrease published and anecdotal knowledge in combination with in other species (van Herk et al. 2002, Aptroot 2009). data on habitat trends (Dahlberg & Mueller 2011). However, these findings are only partly applicable to the Arctic. In the Netherlands, the increase in (sub-) Field surveys, monitoring programs and research are tropical species concerns mainly species recovering from needed to maintain and develop knowledge of Arctic the losses by former SO2-pollution, and the decrease in fungi. However, today’s knowledge of Arctic fungi relies boreo-montane/Arctic-alpine species concerns mainly on a very small number of experienced and skilled peo- terricolous species suffering from changes in land man- ple. There is a general concern that universities and gov- agement of semi-natural grassland and heath-land and is ernment agencies rarely hire field-experienced scientists fuelled by anthropogenic emissions of nitrogen com- with a broad taxonomic knowledge. This is particularly pounds (primarily NO3 and NH3; e.g. Hauck 2009). true for Arctic fungal specialists. Without opportunities for such positions, Arctic fungal biodiversity will Increasing nitrogen input to ecosystems has large attract little attention and loss of fungal diversity may direct and indirect effects on species diversity of both go unnoticed and undocumented resulting in causes for ectomycorrhizal fungi (e.g. Lilleskov et al. 2002) and changing fungal-dependent ecosystem processes be less lichens. Atmospheric nitrogen deposition in the Arctic understood. is expected to increase in the future (Callaghan 2005). Such input of nitrogen will increase vascular plant growth and competition with a negative effect for the 10.5. CONCLUSIONS AND Arctic terricolous lichen, including the lichens essential as reindeer food. Field experiments document that RECOMMENDATIONS increased vascular plant vegetation results in a decline in soil-inhabitating macrolichen abundance in the sub- Fungi is a key group of organisms with high species rich- and low Arctic, including reindeer food lichens (Joly et ness and large significance for ecosystem processes in the Chapter 10 • Fungi 367

Arctic. Except for macrolichens, however, their presence ACKNOWLEDGEMENTS and significance has often been overlooked and poorly appreciated in the Arctic, despite being species rich, We gratefully acknowledge Henning Knudsen for abundant and pivotal in carbon and nutrient cycling. Dis- suggestions and providing data from Greenland, Greg tributional and ecological knowledge is reasonably good Mueller for contributing to the estimate of the poten- for macrolichens but sparser for fungi and microlichens. tial number of Arctic fungal species, and Ellen Larsson, Sveta Yamin-Pasternak, Tero Mustonen and Violet Ford Even with these caveats, present knowledge largely for other information. The work was partly sponsored enables us to predict the future of Arctic fungi. The by the Swedish Environmental Protection Board. unavoidable greening of the Arctic will steadily and significantly affect the distribution and abundance of fungi, as habitat conditions gradually transform the distribu- REFERENCES tion and abundance of plants. This change is in progress already, but studies of Arctic soil fungal communities ACIA 2005. Arctic Climate Impact Assessment. Cambridge Uni- imply that the response as yet is relatively slow (Timling versity Press. & Taylor 2012). Therefore, we judge that these changes Ahti, T. & Oksanen, J. 1990. Epigeic lichen communities of taiga and tundra regions. Vegetatio 86: 39-70. will only rarely affect their conservation status in the Alstrup, V. 1982. The epiphytic lichens of Greenland. The Bryolo- immediate future. However, over time the effects of gist 85: 64-73. climate change and subsequently transformed vegetation Alstrup, V. 2005. Checklist of the lichenicolous fungi of Green- will have profound effects on the distribution and com- land. Prepared for the NLF excursion to Greenland 2005. position of fungi and consequently also their ecosystem www.nhm.uio.no/lichens/nordiclichensociety/excursions/ LIFU_Greenland.pdf [accessed 16 Nov. 2011] functions. Most of the species are circumpolar and also Alstrup, V. & Elvebakk, A. 1996. A catalogue of Svalbard plants, distributed outside the Arctic. However, a large propor- fungi, algae, and cyanobacteria. Part 5: Lichenicolous fungi. tion of them are confined to Arctic-alpine habitats of Norsk Polarinstitutt Skrifter 198: 261-270. which the greater part is located within the Arctic and Alstrup, V. & Hawksworth, D.L. 1990. The lichenicolous fungi of few are true Arctic endemics. Greenland. Medd. Grønland, Biosci. 31: 1-90. Alstrup, V., Hansen, E.S. & Daniels, F.J.A. 2000. Lichenized, lichenicolous and other fungi from North and North-East The following actions would enable a more thorough Greenland. Folia Cryptog. Estonica 37: 1-20. analysis of the status and trends of Arctic fungi. Aptroot, A. 2009. Lichens as an indicator of climate and global • Long-term funding is necessary to maintain and train change. In: T.M. Letcher (ed.). Climate Change: Observed Arctic specialists in mycology and lichenology and to Impacts on Planet Earth, pp 401-408. Elsevier, Amsterdam. Armstrong, R.A. & Bradwell, T. 2010. Growth of crustose ensure research and monitoring to take place. lichens: a review. Geografiska Annaler, Series A: Physical Ge- • The identity and taxonomy of species with unclear ography 92: 3-17. status (e.g. poorly known fungi and potentially Arnold, A.-E., Miadlikowska, J., Higgins, K.L., Sarvate, S.D., endemic lichens) should be critically examined. The Gugger, P., Way, A. et al. 2009. A phylogenetic estimation of large potential of fungal analysis of deep sequenced trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Systematic environmental samples will largely benefit by clarified Biology 58: 283-297. fungal taxonomy. Bjorbækmo, M.F.M., Carlsen, T., Brysting, A., Vralstad, T., • A check-list for Arctic fungi should be compiled. Høiland, K., Ugland, K.I. et al. 2010. High diversity of root • The knowledge of distribution and ecology for all associated fungi in both alpine and arctic Dryas octopetala. BMC fungi, but in particularly for non-lichenized fungi, Plant Biology 10(244): 1-12. Blackwell, M. 2011. The fungi: 1, 2, 3 ... 5.1 million species? should be improved. American Journal of Botany 98: 426-438. • Conservation status should be assessed for Arctic Boertmann, D. & Knudsen, H. (eds.) 2006. Arctic and alpine lichens and fungi, preferentially at both the Arctic and fungi 6. Medd. Grønland, Biosci. 56: 1-161. global scales. Borgen, T., Elborne, S.A. & Knudsen, H. 2006. A checklist of the • Long-term monitoring within representative Arctic Greenland basidiomycetes. In: D. Boertmann & H. Knudsen (eds.). Arctic and Alpine Micology 6, pp 37-59. Medd. Grøn- habitats would enable us to document and follow fun- land, Biosci. 56: 1-161. gal species shifts over time. Buee, M., Reich, M., Murat, C., Morin, E., Nilsson, R.H., Uroz, • Analyses of how vegetation changes may, based on S. & Martin, F. 2009. 454 Pyrosequencing analyses of forest knowledge of fungal ecology, predict potential habi- soils reveal an unexpectedly high fungal diversity. New Phy- tats for fungi in space and time. tologist. 184: 449-456. Bültmann, H. 2005. Syntaxonomy of arctic terricolous lichen • Efforts to analyze the effects of slowly shifting fungal vegetation, including a case study from Southeast Greenland. communities on ecosystem processes such as nutrient Phytocoenologia 35: 909-949. cycling and carbon fluxes are needed. Bültmann, H. 2010. Diversity and similarity of lichen floras of • Analyses of how the supply of reindeer food lichen countries along a south-north gradient from Italy to Green- communities will alter due to vegetation change land. Ann. Bot. (Roma) 1: 1-10. Bültmann, H. 2011. Liegt der Hotspot der Phyto-Diversität jen- should be conducted in order to better predict future seits der polaren Baumgrenze? Norden 20: 103-109. conditions for populations of reindeer/caribou. Bültmann, H. & Daniëls, F.J.A. 2009. Lichens and vegetation – a case study of Thamnolietum vermicularis. Bibl. Lichenol. 100: 31-47. 368 Arctic Biodiversity Assessment

Bültmann, H. & Daniëls, F.J.A. 2012. Net photosynthesis as an Rasch (eds.). High-Arctic Ecosystem Dynamics in a Changing alternative for relative growth rate in classifying lichens in Climate. Ten years of monitoring and research at Zackenberg Grime’s plant strategy types. Bibl. Lichenol. 108: 21-44. Research Station, Northeast Greenland, pp 223-248. Advances Callaghan, T.V. 2005. Arctic tundra and polar desert ecosystems. in Ecological Research 40, Academic Press. In: Arctic Climate Impact Assessment, pp 243-352. Cambridge Elvebakk, A. & Bjerke, J.W. 2006. The Skibotn area in North University Press. Norway. An example of very high lichen species richness far Callaghan, T.V., Bjorn, L.O., Chernov, Y. Chapin, T., Christensen, to the north: A supplement with an annotated list of species. T.R., Huntley, B. et al. 2004. Biodiversity, distributions and Mycotaxon 96: 141-146. adaptations of arctic species in the context of environmental Elvebakk, A. & Hertel, H. 1996. A catalogue of Svalbard plants, change. Ambio 33: 404-417. fungi, algae, and cyanobacteria. Part 6: Lichens. Norsk Polar- CAVM-Team 2003. Circumpolar Arctic Vegetation Map. Scale institutt Skrifter 198: 271-359. 1: 7,500000. Conservation of Arctic Flora and Fauna (CAFF) Elvebakk, A. & Prestrud, P. 1996. A catalogue of Svalbard plants, Map No.1. U.S. Fish and Wildlife Service, Anchorage. fungi, algae and cyanobacteria. Norwegian Polar Institute. Clayden, S.A. 1997. Intraspecific interactions and parasitism in Elven, R. (ed.) 2007 onwards. Checklist of the Panarctic Flora an association of Rhizocarpon lecanorinum and R. geographicum. (PAF) Vascular Plants. Version: May 2007. www.binran.ru/ Lichenologist 29: 533-545. infsys/paflist/index_old.htm Clemmensen, K.E., Bahr, A., Ovaskainen, O., Dahlberg, A., Ek- Fahselt, D., Maycock, P.F. & Wong, P.Y. 1989. Reproductive blad, A., Wallander, H. et al. 2013. Roots and associated fungi modes of lichens in stressful environments in central Ellesmere drive long-term carbon sequestration in boreal forest. Science Island, Canadian High arctic. Lichenologist 21: 343-353. 339: 1615-1618. Feuerer, T. & Hawksworth, D.L. 2007. Biodiversity of lichens, Cornelissen, J.H.C., Callaghan, T.V., Alatalo, J.M., Michelsen, A., including a world-wide analysis of checklist data based on Graglia, E., Hartley, A.E. et al. 2001. Global change and arctic Takhtajan’s floristic regions. Biodivers. Conserv. 16: 85-98. ecosystems: is lichen decline a function of increase in vascular Fries, T.M. 1860. Lichenes Arctoi Europae Groenlandiaeque plant biomass? J. Ecol. 89: 984-994. hactenus cogniti. Uppsala. Cripps, C.L. & Ammirati, J.F. (eds.) 2010. Eighth International Fujimura, K.E. & Egger, K.N. 2012. Host plant and environment Symposium on Arctic-Alpine Mycology (ISAM 8), Beartooth influence community assembly of High Arctic root-associated Plateau, Rocky Mountains, USA 2008. North American Fungi fungal communities. Fungal Ecology 5: 409-418. 5: 1-220. Fujimura, K.E., Egger, K.N. & Henry, G.H. 2008. The effect of Cripps, C.L. & Horak, E. 2006. Arrhenia auriscalpum in arctic- experimental warming on the root-associated fungal commu- alpine habitats: world distribution, ecology, new reports from nity of Salix arctica. ISME journal 2: 105-114. the southern Rocky Mountains, USA. In: D. Boertmann & Fujiyoshi, M., Yoshitake, S., Watanabe, K., Murota, K., Tsuchiya, H. Knudsen (eds.): Arctic and Alpine Micology 6, pp 17-24. Y., Uchida, M. & Nakatsubo, T. 2011. Successional changes in Medd. Grønland, Biosci. 56: 1-161. ectomycorrhizal fungi associated with the polar willow Salix Cripps, C.L. & Horak, E. 2010. Amanita in the Rocky Mountain polaris in a deglaciated area in the High Arctic, Svalbard. Polar alpine zone, USA; new records for A. nivalis and A. groenlandica. Biology 34: 667-673. North American Fungi 5: 9-21. Gardes, M. & Dahlberg, A. 1996. Mycorrhizal diversity in arctic Cripps, C.L., Larsson, E. & Horak, E. 2010. Subgenus Mallocybe and alpine tundra: An open question. New Phytologist 133: (Inocybe) in the Rocky Mountain alpine zone with molecular 147-157. reference to European arctic-alpine material. North American GBIF 2012. Global Biodiversity Information Facility. www.gbif. Fungi 5: 97-126. org [accessed September 2012] Crittenden, P.D. & Kershaw, K.A. 1978. Discovering the role of Geml, J., Kauff, F., Brochmann, C. & Taylor, D.L. 2010. Surviving lichens in the nitrogen cycle in boreal-arctic ecosystems. The climate changes: high genetic diversity and transoceanic gene Bryologist 81: 258-267. flow in two arctic-alpine lichens, Flavocetraria cucullata and F. Cuerrier, A. & the Elders of Kangiqsujuaq 2011. The Botanical nivalis (Parmeliaceae, Ascomycota). Journal of Biogeography Knowledge of the Inuit of Kangiqsujuaq, Nunavik. Avataq 37: 1529-1542. Cultural Institute. Geml, J., Timling, I., Robinson, C.H., Clare H., Lennon, N., Dahlberg, A. & Mueller, G.M. 2011. Applying IUCN red-listing Nusbaum, H.C. et al. 2012. An arctic community of symbiotic criteria for assessing and reporting on the conservation status fungi assembled by long-distance dispersers: phylogenetic of fungal species. Fungal Ecology 4: 147-162. diversity of ectomycorrhizal basidiomycetes in Svalbard based Daniëls, F.J.A. 1975. Vegetation of the Angmagssalik District on soil and sporocarp DNA. J. Biogeography 39: 74-88. Southeast Greenland. III. Epilithic macrolichen communities. Gulden, G. & Torkelsen, A.-E. 1996. Part 3. Fungi 1. Basidiomy- Medd. Grønland 198(3): 1-32. cota: Agaricales, Gastromycetales, Aphyllophorales, Exoba- Daniëls, F.J.A. 1982. Vegetation of the Ammassalik district, South- sidiales, Dacrymycetales and Tremellales. In: A. Elvebakk & P. east Greenland. IV. Shrub, dwarf shrub and terricolous lichens. Prestrud (eds.). A catalogue of Svalbard plants, fungi, algae and Medd. Grønland, Biosci. 10: 1-78. cyanobacteria, pp 173-206. Norsk Polarinstitutt Skrifter 198. Daniëls, F.J.A., de Molenaar, J.G., Chytry, M. & Tichy, L. 2011. Hallgrímsson, H. 2010. Sveppabókin. Íslenskir sveppir og svep- Vegetation change in Southeast Greenland? Tasiilaq revisited pafræði. Skrudda, Reykjavík. after 40 years. Appl. Veg. Sci. 14: 230-241. Hallgrímsson, H. & Eyjólfsdóttir, G.G. 2004. Checklist of Ice- de Vernal, A. & Hillaire-Marcel, C. 2008. Natural variability of landic Fungi I. Microfungi. Fjölrit Náttúrfræðistofnunar 45: Greenland climate, vegetation, and ice volume during the past 1-189. [in Icelandic with English abstract and introduction] million years. Science 320: 1622-1625. Hansen, E.S. 2006. Lichens. In: A.B. Klitgaard, M. Rasch & K. Deslippe, J.R., Hartmann, M., Mohn, W.W. & Simard, S.W. 2011. Caning (eds.). ZERO 11th Annual Report 2005, pp 44-53. Long-term experimental manipulation of climate alters the Danish Polar Centre. ectomycorrhizal community of Betula nana in Arctic tundra. Hansen, E.S. 2008. The lichen flora of Kuhn Ø and Blåbærdalen, Global Change Biology 17: 1625-1636. easternmost Th. Thomsen Land, North East Greenland. Cryp- Diederich, P., Ertz, D., Stapper, N., Sérusiaux, E., van den togamie, Mycologie 29: 397-411. Broeck, D., van den Boom, P. & Ries, C. 2011. The lichens and Hansen, E.S., Poelt, J. & Søchting, U. 1987. Die Flechtengattung lichenicolous fungi of Belgium, Luxembourg and northern Caloplaca in Grönland. Medd. Grønland, Biosci. 25: 1-52. France. www.lichenology.info [accessed 12 May 2011]. Hauck, M. 2009. Global warming and alternative causes of Elberling, B., Tamstorf, M.P., Michelsen, A., Arndal, M.F., decline in arctic-alpine and boreal-montane lichens in North- Sigsgaard, C., Illeris, L. et al. 2008. Soil and plant community- Western Central Europe. Global Change Biology 15: 2653- characteristics and dynamics at Zackenberg. In: H. Meltofte, 2661. T.R. Christensen, B. Elberling, M.C. Forchhammer & M. Chapter 10 • Fungi 369

Hawksworth, D.L. 2001. The magnitude of fungal diversity: the Knudsen, H. & Mukhin, V. 1998. The arctic-alpine agaric element 1.5 million species estimate revisited. Mycological Research in the Polar Urals and Yamal, Western Siberia. In: V. Mukhin & 105: 1422-1432. H. Knudsen (eds.). Arctic and Alpine Mycology 5: 152-162. Heger, T.J., Imfeld, G. & Mitchell, E.A.D. 2012. Special issue on Kristinsson, H., Hansen, E.S. & Zhurbenko, M. 2006. Panarctic “Bioindication in soil ecosystems”: Editorial note. European lichen checklist. library.arcticportal.org/276/1/Panarctic_li- Journal of Soil Biology 49: 1-4. chen_checklist.pdf Higgins, K.L., Arnold, A.E., Miadlikowska, J., Sarvate, S.D. & Kristinsson, H., Zhurbenko, M. & Hansen, E.S. 2010. Panarctic Lutzoni, F. 2007. Phylogenetic relationships, host affinity, and checklist of lichens and lichenicolous fungi. CAFF Technical geographic structure of boreal and arctic endophytes from Report No. 20. three major plant lineages. Molecular Phylogenetics and Evo- Krog, H. 1968. The macrolichens of Alaska. Norsk Polarinstitutt lution 42: 543-555. Skrifter 144: 1-180. Holt, E.-A. & Bench, G. 2008. 14C/C measurements support Lange, M. 1957. Macromycetes, part III. Greenland Agaricales. Andreev’s internode method to determine lichen growth rates Ecological and plant geographical studies. Medd. Grønland in Cladonia stygia (Fr.) Ruoss. Lichenologist 40: 559-565. 148(2): 1-125. Holt, E.-A., McCune, B. & Neitlich, P. 2007. Succession and Large Herbivore Network 2012. www.largeherbivore.org/rein- community gradients of arctic macrolichens and their relation deer [accessed September 2012] to substrate, topography, and rockiness. Pacific Northwest Larson, D.W. & Kershaw, K.A. 1975. Acclimation in arctic li- Fungi 2(2): 1-21. chens. Nature 254: 421-423. Høiland, K. & Økland, R.H. (eds.) 2008. Arctic and alpine my- Laursen, G.A. & Ammirati, J.F. (eds.) 1982. Arctic and alpine mycology VII. Sommerfeltia 31. cology – The First International Symposiumon Arcto-Alpine Inga, B. 2007. Reindeer (Rangifer tarandus tarandus) feeding on Mycology. University of Washington Press, Seattle. lichens and mushrooms: traditional ecological knowledge Laursen, G.A., Ammirati, J.F. & Redhead, S.A. 1987. Arctic among reindeer-herding Sami in northern Sweden. Rangifer and alpine mycology 1I. Environmental Science Research 34, 27: 93-106. Plenum Press, New York. IUCN 2012. IUCN Red List of Threatened Species. Version Lawrey, J.D. & Diederich, P. 2003. Lichenicolous fungi: Interac- 2012.2. www.iucnredlist.org [accessed 12 November 2012] tions, Evolution, and Biodiversity. The Bryologist 106: 80-120. Jakutija 2007. Istoriko-kul’turnyj atlas: priroda, istorija, e˙tno Lilleskov, E.A., Fahey, T.J., Horton, T.R. & Lovett, G.M. 2002. grafija, sovremennost’/Pravitel’stvo Respubliki Sacha Belowground ectomycorrhizal fungal community change over (Jakutija). Institut Gumanitarnych Issledovanij AN, Respubliki a nitrogen deposition gradient in Alaska. Ecology 83: 104-115. Sacha (Jakutija). Izdat, Feorija, Moskva. Lind, J. 1927. The geographical distribution of some arctic micro- Jensen, D.B. (ed.) 2003. The Biodiversity of Greenland – a coun- mycetes. Kong. Dan. Vidensk. Selsk. Biol. Medd. 6: 1-45. try study. Technical Report No. 55, Grønlands Naturinstitut. Lind, J. 1934. Studies on the geographical distribution of arctic Joamie, A., Joamie, A., Pitseolak, J., Papatsie, M., Ootoova, E. & circumpolar micromycetes. Kong. Dan. Vidensk. Selsk. Biol. Attagutsiak, T. 2001. Interviewing Inuit Elders 5: Perspectives Medd. 11: 1-152. on Traditional Health. Nunavut Arctic College. Llano, G.A. 1956. Utilization of lichens in the arctic and subarc- Joly, K., Jandt, R.R. & Klein, D.R. 2009. Decrease of lichens in tic. Economic Botany 10: 367-392. Arctic ecosystems: the role of wildfire, caribou, reindeer, com- Longton, R.E. 1988. Biology of polar bryophytes and lichens. petition and climate in north-western Alaska. Polar Research Cambridge University Press. 28: 433-442. Ludley, K.E. & Robinson, C.H. 2008. Decomposer Basidiomycota Jørgensen, P.M. & Nordin, A. 2009. Lichens in Scandinavia in Arctic and Antarctic ecosystems. Soil Biology & Biochemis- known mainly from Norwegian type-specimens. Graphis try 40: 11-29. Scripta 21: 1-20. Lünterbusch, C. & Daniëls, F.J.A. 2004. Phytosociology of Dryas Kappen, L., Schroeter, B., Scheidegger, C., Sommerkorn, M. & integrifolia vegetation in Northwest Greenland on moist-wet Hestmark, G. 1996. Cold resistance and metabolic activity of soil. Phytocoenologia 34: 241-270. lichens below 0°C. Adv. Space Res. 12: 119-128. Lydolph, M.C., Jacobsen, J., Arctander, P., Gilbert, M.T.P., Gili- Karatygin, I.V., Nezdoiminogo, E.L., Novozhilov, Y.K. & Zhur- chinsky, D.A., Hansen, A.J. et al. 2005. Beringian paleoecology benko, M.P. 1999. Russian Arctic fungi. St. Petersburg. [in inferred from permafrost-preserved fungal DNA. Applied and Russian] Environmental Microbiology 71: 1012-1017. Karsten, P.A. 1872. Fungi in insulis Spetsbergen et Beeren Eiland Lynge, B. 1947. Botany of the Canadian Eastern Arctic, part II. collecti. Examinat, enumerat. Öfversigt af Kongl. Vetenskaps- Thallophyta and Bryophyta. Lichenes. Nat. Mus. Canada Bull. Akademiens Förhandlingar 1871 (2). Stockholm. 97: 298-369. Kauserud, H., Stige, L.C., Vik, J.O., Økland, R.H., Høiland, Matthews, J.A. & Trenbirth, H.E. 2011. Growth rate of very large K. & Stenseth, N.C. 2008. Mushroom fruiting and climate crustose lichen (Rhizocarpon subgenus) and its implications for change. Proceedings of the National Academy of Sciences of lichenometry. Geografiska annaler series A – Physical geogra- the USA 105: 3811-3814. phy 93A: 27-39. Kauserud, H., Heegaard, E., Semenov, M.A., Boddy, L., McMahon, S.K., Wallenstein, M.D. & Schimel, J.P. 2009. Mi- Halvorsen, R., Stige, L.C. et al. 2010. Climate change and crobial growth in Arctic tundra soil at -2°C. Environmental spring-fruiting fungi. Proceedings of the Royal Society B. 277: Microbiology Reports 1: 162-166. 1169-1177. Mukhin, V.A. & Knudsen, H. (eds) 1998. Arctic and alpine mycol- Kauserud, H., Heegaard, E., Buntgen, U., Halvorsen, R., Egli, S., ogy V. Yekaterinburg Publishers, Yekaterinburg. Senn-Irlet, B. et al. 2012. Warming-induced shift in European Mustonen, K., Mustonen, T., Aikio, P. & Aikio, A. 2011. Drown- mushroom fruiting phenology. Proceeding of the National ing Reindeer, Drowning Homes – Indigenous Sámi and Hy- Academy of Sciences of the United States of America 109: droelectricity Development in Sompio, Finland. Snowchange 14488-14493. Cooperative, Kontiolahti, Second Print. Kershaw, K.A. 1985. Physiological Ecology of Lichens. Cam- Nash, T.H. (ed.) 2008. Lichen Biology. Cambridge University bridge University Press. Press. 2nd ed. Knudsen, H. 2001. Fungi. In: E.W. Born & J. Böcher (eds.). The Nash, T.H. & Gries, C. 1995. The use of lichens in atmospheric Ecology of Greenland, pp 264-270. Atúakkiorfik, Nuuk. deposition studies with an emphasis on the Arctic. Science of Knudsen, H. 2006. Mycology in Greenland, an introduction. In: the Total Environment 160/161: 729-736. D. Boertmann & H. Knudsen (eds.): Arctic and Alpine Micol- Newsham, K.K., Upson, R. & Read, D.J. 2009. Mycorrhizas and ogy 6, pp 7-16. Medd. Grønland, Biosci. 56: 1-161. dark septate root endophytes in polar regions. Fungal Ecology 2: 10-20. 370 Arctic Biodiversity Assessment

Nimis, P.L. 1981. Epigaeous lichen synusiae in the Yukon Terri- Smith, J.A., Blanchette, R.A. & Newcombe, G. 2004. Molecular tory. Cryptogamie, Bryol. Lichénol. 2: 127-151. and morphological characterization of the willow rust fungus, Nimis, P.L. 1985. Structure and floristic composition of a high Melampsora epitea, from arctic and temperate hosts in North arctic tundra: Ny Ålesund (Svalbard Archipelago). Inter-Nord America. Mycologia 96: 1330-1338. 17: 47-58. Sommerkorn, M. 2000. The ability of lichens to benefit from Nimis, P.L., Scheidegger, C. & Wolseley, P.A. (eds.) 2002. Moni- natural CO2 enrichment under a spring snow-cover: a study toring with lichens – monitoring lichens. NATO Science series with two arctic-alpine species from contrasting habitats. Bib- IV. Earth and Environmental Sciences 7: 1-408. liotheca Lichenologica 75: 365-380. Olsson, P.-A., Eriksen, B. & Dahlberg, A. 2004. Colonisation by Søchting, U. 1990. Cetraria islandica as health diet in 19th century arbuscular mycorrhizal and fine endophytic fungi in herba- Greenland. Graphis Scripta 3: 24. ceous vegetation in Canadian High Arctic. Can. J. Botany 82: Spribille, T., Perez-Ortega, S., Tønsberg, T. & Schirokauer, D. 1547-1556. 2010. Lichens and lichenicolous fungi of the Klondike Gold Ormsby, A., Hodson, E., Li, Y., Basinger, J. & Kaminskyj, S. 2007. Rush Natrional Historic Park, Alaska, in a global biodiversity Arbuscular mycorrhizae associated with Asteraceae in the Ca- context. The Bryologist 113: 439-515. nadian High Arctic: the value of herbarium archives. Canadian Thomson, J.W. 1979. Lichens of the Alaskan Arctic Slope. Univer- Journal of Botany 85: 599-606. sity of Toronto Press. Oswalt, W.H. 1957. A Western Eskimo ethnobotany. Anthropo- Thomson, J.W. 1984. American Arctic Lichens. 1. The macroli- logical Papers of the Univ. of Alaska 6: 16-36. chens. Columbia University Press. Øvstedal, D.O., Tønsberg, T. & Elvebakk, A. 2009. The lichen Thomson, J.W. 1990. Lichens in the Canadian Arctic Islands. In: flora of Svalbard. Sommerfeltia 33: 1-393. C.R. Harington (ed.). Canada’s Missing Dimension. Volume 1: Parmelee, J.A. 1989. The rusts (Uredinales) of arctic Canada. 385-420. Canadian Museum of Nature, Ottawa. Canadian Journal of Botany 67: 3315-3365. Thomson, J.W. 1997. American Arctic Lichens 2. The microli- Pegau, R.E. 1968. Growth rates of important reindeer forage chens. The University of Wisconsin Press. lichens on the Seaward Peninsula, Alaska. Arctic 21: 255-259. Timling, I. & Taylor, D.L. 2012. Peeking through a frosty window: Peters, C., Basinger, J.F. & Kaminskyj, S.G.W. 2010. Endorhizal molecular insights into the ecology of Arctic soil fungi. Fungal fungi associated with vascular plants on Truelove Lowland, Ecology 5: 419-429. Devon Island, Nunavut, Canadian High Arctic. Arctic, Antarc- Timling, I., Dahlberg, A., Walker, D.A., Gardes, M., Charcosset, tic, and Alpine Research 43: 73-81. J-Y., Welker, J.M. & Taylor, L. 2012. Distribution and driv- Petersen, P.M. 1977. Investigation on the ecology and phenology ers of ectomycorrhizal fungal communities across the North of the macromycetes in the Arctic. Medd. Grønland 199(5): American Arctic. Ecosphere 3:art111. dx.doi.org/10.1890/ 1-72. ES12-00217.1 Petrini, O. & Laursen, G.A. (eds). 1993 Arctic and alpine mycol- Tojo, M. & Newsham, K.K. 2012. Snow moulds in polar environ- ogy, Vols. 3-4. J. Cramer, Berlin. ments. Fungal Ecology 5: 395-402. Pickles, B.J., Egger, K.N., Massicotte, H.B. & Green D.S. 2012. U’Ren, J.M., Lutzoni, F., Miadlikowska, J. & Arnold, A-E. 2010. Ectomycorrhizas and climate change. Fungal Ecology 5: 73-84. Community analysis reveals close affinities between endo- Printzen, C. 2008. Uncharted terrain: the phylogeography of arc- phytic and endolichenic fungi in mosses and lichens. Microbial tic and boreal lichens. Plant Ecology & Diversity 1: 265-271. Ecology 60: 340-353. Putkonen, J. & Roe, G. 2003. Rain-on-snow events impact soil van Herk, C.M., Aptroot, A. & H.F. van Dobben 2002. Long- temperatures and affect ungulate survival. Geophysical Re- term monitoring in the Netherlands suggests that lichens search Letters 30(4), 1188, doi:10.1029/2002GL016326. respond to global warming. Lichenologist 34: 141-154. Redhead, S.A. 1988. A biogeographical overview of the Canadian Vonlanthen, C.M., Walker, D.A., Raynolds, M.K., Kade, A., Kuss, mushroom flora. Can. J. Bot. 67: 3003-3062. P., Daniëls, F.J.A. & Matveyeva, N.V. 2008. Patterned-ground Richardson, D.H.S. 1974: The vanishing lichens. Their History, plant communities along a bioclimate gradient in the High Arc- Biology and Importance. Hafner Press, New York. tic, Canada. Phytocoenologia 38: 23-63. Robinson, C.H. 2001. Cold adaptation in Arctic and Antarctic Voytsekhovich, A.O., Mikhailyuk, T.I. & Darienko, T.M. 2011. fungi. New Phytologist 151: 341-353. Lichen photobionts 1: biodiversity, ecophysiology and co- Ronkier, A. & Ronkier, M. 2010. Biogeographical patterns in evolution with the mycobiont. Algologia 21: 3-26. [in Russian] arctic-alpine fungi: distribution and analysis in Marasmius Walker, T.R., Crittenden, P.D. & Young, S.D. 2003. Regional epidryas. A typical cirumpolar species of cold environments. variation in the chemical composition of winter snow pack and North American Fungi 5: 23-50. terricolous lichens in relation to sources of acid emissions in Rostrup, E. 1888. Fungi Groenlandiae. Medd. Grønland 3: 517- the Usa River basin, northeast European Russia. Environmen- 590. tal Pollution 125: 401-412. Savile, D.B.O. 1963. Mycology in the Canadian Arctic. Arctic Walker, X., Basinger, J. & Kaminskyj, S. 2010. Endorhizal fungi 16:17-25. associated with Ranunculus in the Canadian Arctic and Prairies. Savile, D. 1982. Adaptions of fungi to arctic and subarctic condi- The Open Mycology Journal 4: 1-9. tions. In: G.A. Laursen & J.F. Ammirati (eds.). Arctic & Alpine Walker, J.F., Aldrich-Wolfe, L., Riffel, A., Barbare, H., Simp- Mycology 1, pp 357-370. University of Washington Press. son, N.B., Trowbridge, J. & Jumpponen, A. 2011. Diverse Schadt, C.W., Martin, A.P., Lipson, D.A. & Schmidt, S.K. 2003. Helotiales associated with the roots of three species of Arctic Seasonal Dynamics of Previously Unknown Fungal Lineages in Ericaceae provide no evidence for host specificity. New Phy- Tundra Soils. Science 301: 1359-1361. tologist 191: 515-527. Scheidegger, C. & Werth, S. 2009. Conservation strategies for Wallenstein, M.D., McMahon, S. & Schimel, J. 2007. Bacterial lichens: insights from population biology. Fungal Biological and fungal community structure in Arctic tundra tussock and Reviews 23: 55-66. shrub soils. FEMS 320: 428-435. Schmit, J.P. & Mueller, G.M. 2007. An estimate of the lower limit Webber, P.J. 1974. Tundra primary productivity. In: J.P. Ives & of global fungal diversity. Biodiversity and Conservation 16: R.G. Barry (eds.). Arctic and Alpine Environments, pp 445- 99-111. 473. Methuen, London. Scholler, M., Schnittler, M. & Piepenbring, M. 2003. Species of Werner, A. 1990. Lichen growth rates for the northwest coast of Anthracoidea (Ustilaginales, Basidiomycota) on Cyperaceae in Spitsbergen, Svalbard. Arctic and Alpine Research 22: 129- Arctic Europe. Nova Hedwig 76: 415-428 140. Sharnoff, S. 2012. www.lichen.com/usetype.html [accessed Werth, S. 2010. Population genetics of lichen-forming fungi – a September 2012] review. Lichenologist 42: 499-519. Sieg, B., Drees, B. & Hasse, T. 2009. High-altitude vegetation of Wookey, P.A., Aerts, R., Bardgett, R.D., Baptist, F., Brathen, continental West Greenland. Phytocoenologia 39: 27-50. K.A., Cornelissen, J.H.C. et al. 2009. Ecosystem feedbacks Chapter 10 • Fungi 371

and cascade processes: understanding their role in the respons- es of Arctic and alpine ecosystems to environmental change. Global Change Biology 15: 1153-1172. Yamin-Pasternak, S. 2007. An ethnomycological approach to land use values in Chukotka. Etudes Inuit Studies 31: 121-141. Zhurbenko, M.P. 2007. The lichenicolous fungi of Russia: geographical overview and a first checklist. Mycologia Balcanica 4: 105-124. Zhurbenko, M.P. 2009a. Lichenicolous fungi and some lichens from the Holarctic. Opuscula Philolichenum 6: 87-120. Zhurbenko M.P. 2009b. Lichenicolous fungi and lichens from the Holarctic. Part II. Opuscula Philolichenum 7: 121-186. Zhurbenko M.P. 2010a. Lichenicolous fungi of the Russian Arctic. Doctor of Biological Sciences thesis, Komarov Botanical Insti- tute, St.-Petersburg. [in Russian] Zhurbenko, M.P. 2010b. Lichenicolous fungi and lichens growing on Stereocaulon from the Holarctic, with a key to the known species. Opuscula Philolichenum 8: 9-39. Zhurbenko, M. 2012. Lichenicolous fungi growing on Thamnolia, mainly from the Holarctic, with a worldwide key to the known species. Lichenologist 44: 147-177. Zhurbenko, M.P. & Santesson, R. 1996. Lichenicolous fungi from the Russian Arctic. Herzogia. 12: 147-161. Appendix 10: www.abds.is/aba-2013-appendix-10