Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil

Soil Biology & Biochemistry 47 (2012) 198e208

Contents lists available at SciVerse ScienceDirect

Soil Biology & Biochemistry journal homepage: www.elsevier.com/locate/soilbio

Review

Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil John W.G. Cairney Hawkesbury Institute for the Environment, University of Western Sydney, Locked Bag, 1797, Penrith, NSW 2751, Australia

a r t i c l e i n f o

a b s t r a c t

Article history: Received 18 October 2011 Received in revised form 6 December 2011 Accepted 9 December 2011 Available online 13 January 2012

Extramatrical mycelia (EMM) of ectomycorrhizal (ECM) fungi are potentially extensive in soil and receive significant allocations of plant-derived carbon. Although losses from living EMM occur via respiration and exudation, EMM represents a considerable biomass component and potential carbon sink in many forest soils. ECM root tips and rhizomorphs may persist in soil for many months, but interactions between grazing arthropods and decomposers probably facilitate more rapid turnover of diffuse EMM. Elevated atmospheric CO2 concentration [CO2] is likely to increase carbon allocation to ECM fungi by their tree hosts. This will probably increase root colonization by ECM fungi and drive changes in their communities in soil. The likely effects of elevated [CO2] and other climate change factors on the production and turnover of EMM production are difficult to predict from current evidence, and this hampers our understanding of their potential value as future carbon sinks. Responses of grazing soil arthropods to future climate change will have a strong influence on EMM turnover, along with the abilities of ECM fungi to store carbon in below-ground, and this should be seen as a priority area for future research. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: Ectomycorrhizal fungi Soil carbon Extramatrical mycelia Rhizomorphs Climate change

1. Introduction Symbiotic ectomycorrhizal (ECM) associations are ubiquitous in temperate and boreal forests, where they represent key components of mineral nutrient cycling processes (Smith and Read, 2008). The fungi (largely basidiomycetes and ascomycetes) infect short lateral roots of trees, forming a mycelial sheath around individual root tips and penetrating between epidermal cells to form a nutrient and carbon exchange interface (Peterson et al., 2004). Importantly, ECM fungi also produce extramatrical mycelium (EMM) that grows from ECM root tips into surrounding soil to forage for mineral nutrients and seek new root tips for colonisation (Anderson and Cairney, 2007). These mycelial systems are regarded as indeterminate, structurally and physiologically heterogeneous networks that interconnect multiple plant roots (Cairney and Burke, 1996) and may even facilitate inter-plant carbon and nutrient movements (Selosse et al., 2006). Different ECM fungal taxa are known to exhibit different patterns of EMM production that are attributable to their multifarious strategies for foraging in soil (Agerer, 2001). Extramatrical mycelial systems are thus structurally and functionally complex, and variously comprise diffuse

E-mail address: [email protected]. 0038-0717/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2011.12.029

(hyphal) and aggregated (rhizomorphic) components. They are also potentially vast (perhaps extending for up to tens of m through soil), yet we have only begun to understand their importance in ecosystem functioning and likely contributions to carbon cycling at the ecosystem scale (Anderson and Cairney, 2007). Although there is evidence that certain ECM fungi may obtain some carbon saprotrophically from soil organic matter (eg Cairney and Burke, 1994; Talbot et al., 2008; Cullings and Courty, 2009), it is generally accepted that they acquire the bulk of their carbon symbiotically from their host trees (Smith and Read, 2008). This carbon supports maintenance of the established fungal biomass in ECM root tips and EMM, along with generation of new biomass at the advancing mycelial front (Söderström, 1992). EMM is thus recognised as a significant conduit for carbon movement into soil beyond the rhizosphere (Norton et al., 1990; Erland et al., 1991; Finlay and Söderström, 1992). Moreover, it is also viewed as an important pathway for carbon input to below-ground food webs as, for example, a substrate for heterotrophic microorganisms and a food source for soil invertebrates (Söderström, 1992; Heinonsalo et al., 2004; Pollierer et al., 2007). It has been estimated that ca 15% of net primary production may be allocated to ECM fungi in North American and Swedish conifer forests (Vogt et al., 1982; Finlay and Söderström, 1992). Indeed, due to difficulties associated with estimating the carbon requirements of EMM in the field, this is

J.W.G. Cairney / Soil Biology & Biochemistry 47 (2012) 198e208

regarded by some as probably a minimum value (Simard et al., 2002). Moreover, by accessing organic nutrients in soil, ECM fungi can increase plant productivity. Recent modelling suggests that this leads to increased carbon input to soil, and that, rather than entering soil as plant litter, this additional carbon enters soil via ECM fungi (Orwin et al., 2011). It has also been argued that fungal hyphae are not readily decomposed, and that both living and dead ECM mycelia may constitute a considerable below-ground sink for carbon sequestration (Setälä et al., 1999; Treseder and Allen, 2000). Significant questions, however, remain regarding both the spatial and temporal scales over which EMM moderate carbon dynamics in forest soil. This review considers current understanding and knowledge gaps regarding EMM in this context, along with the likely impacts of future climate change. 2. Carbon allocation to ECM fungi by their plant hosts Since the pioneering 14CO2-labelling experiments of Melin and Nilsson (1957), that demonstrated transfer of carbon from host to fungus, it has become increasingly evident that ECM infection strongly influences carbon allocation in trees. Lab-based studies indicate that ECM trees allocate up to a third more carbon belowground than equivalent non-mycorrhizal plants (Reid et al., 1983; Rygiewicz and Andersen, 1994; Durall et al., 1994; Qu et al., 2004). This, however, can be strongly affected by nutrient availability (Bidartondo et al., 2001; Corrêa et al., 2011). Within a root system, ECM root tips generally act as stronger sinks for newly-fixed carbon than uninfected short lateral roots, with up to 42 times more carbon reportedly being allocated to the ECM roots than their uninfected counterparts (Melin and Nilsson, 1957; Nelson, 1964; Bevege et al., 1975; Cairney et al., 1989; Wu et al., 2002). Different ECM fungal taxa present different sink strengths for carbon (Bidartondo et al., 2001), but the sink strength of an ECM root tip appears to be greatest in recently-colonised root tips and to decline as individual root tips age (Cairney et al., 1989; Cairney and Alexander, 1992). EMM is also known to be a significant sink for plant-derived carbon, and translocation to EMM occurs rapidly following accumulation in the root tips (Finlay and Read, 1986). Data from laboratory microcosm experiments indicate that up to 29% of net assimilated carbon from the host can be allocated to the EMM of ECM fungi, however, as with carbon accumulation in ECM root tips, this appears to be strongly influenced by the fungal taxa involved and factors such as nitrogen availability (Rygiewicz and Andersen, 1994; Ek, 1997; Bidartondo et al., 2001). Allocation of carbon within EMM is far from uniform; the growing mycelial front and patches of organic matter or minerals that have recently been colonised by EMM act as particularly strong sinks (Miller et al., 1989; Bending and Read, 1995; Wu et al., 2002; Heinonsalo et al., 2004; Rosling et al., 2004). Indeed, in one study, up to 60% of the carbon in EMM was allocated to the region of mycelium that had colonised organic matter patches (Leake et al., 2001). Sporocarps also represent a major sink for host-derived carbon during their development (Teramoto et al., in press). A major unanswered question is the scale over which movement of host-derived carbon occurs in EMM of ECM fungi in forest soils. Because of their complex indeterminate nature, measurements of carbon translocation within EMM systems in the field are largely lacking. Most investigations of carbon movement in ECM fungi have thus been conducted in laboratory microcosms, with translocation within EMM demonstrated over a scale of only a few cm (Finlay and Read, 1986; Wu et al., 2001, 2002). Using the distribution of genetically identical fruiting bodies of ECM basidiomycetes as a proxy for the distribution of the genetically identical parent mycelium in soil, we know that, while EMM of some taxa are

199

unlikely extend for more than 1 m (eg Gryta et al., 1997; Dunham et al., 2003; Murata et al., 2005), EMM of others may extend for tens of m (eg Dahlberg and Stenlid, 1990; Anderson et al., 1998; Bonello et al., 1998; Sawyer et al., 1999) and infect root tips of multiple trees (Lian et al., 2006; Beiler et al., 2010). On the face of it, there is thus the potential for EMM to act as long-distance distribution systems for carbon in forest soils, but convincing evidence for this is currently lacking for several reasons. Firstly, the presence of identical genotypes of an ECM fungus at multiple locations in soil does not necessarily mean that they are interconnected by a continuous subterranean mycelium. As a result of mycophagy or other disturbances, such EMM may well have fragmented into smaller genetically identical mycelia (Dahlberg and Stenlid, 1995) and, consequently, may not represent an unbroken conduit for carbon movement in soil. Furthermore, even in EMM that is physically uninterrupted, removal of protoplast from older hyphae may lead to areas of functionally ‘inert’ mycelium that physiologically fragments the EMM system and prevents continuous translocation of carbon (Klein and Paschke, 2004; Cairney, 2005). Thus even a physically intact mycelium might, in fact, comprise multiple, physiologically separated regions between which there is no carbon movement (Olsson, 1999). Large EMM systems in the field may thus chiefly comprise multiple local zones that are physically and/or physiologically isolated, and within which host-derived carbon is delivered, utilised, stored and ultimately relinquished. Indeed, while EMM of Rhizopogon spp. has been shown to form continuous connections between trees separated by two m (Beiler et al., 2010), to date, carbon movement in the field that is thought to have been via EMM, has been demonstrated only between plants that were <50 cm apart, and for which the inter-root distance spanned by EMM was likely to be considerably less (Simard et al., 1997; Teste et al., 2010; Deslippe and Simard, 2011). Application of quantum dot labelling in field-based tracer studies, coupled with appropriate imaging technology (Whiteside et al., 2009) offers much potential to help resolve at least some of the current questions regarding the scale of translocation in EMM in the field. 3. Loss of carbon from living EMM Clearly, EMM is a potentially large sink for plant-derived carbon, but residence of some of this carbon within EMM is short-lived. Losses of carbon from functionally viable EMM occur largely via respiration and in the form of hyphal exudates. Respiratory losses from EMM are potentially large, and are regarded as a major contributor to overall forest soil CO2 loss (Högberg and Read, 2006). Combined lab- and field-based observations indicate that carbon acquisition by, and respiration from, EMM is largely dependent on current assimilate supply from the host (Söderström and Read, 1987; Högberg et al., 2001; Steinmann et al., 2004; Körner et al., 2005; Heinemeyer et al., 2007). In laboratory microcosms, as much a 64% of the carbon allocated to the EMM can be respired (Söderström and Read, 1987; Rygiewicz and Andersen, 1994; Ek, 1997; Bidartondo et al., 2001). Field-based measurements also indicate significant respiration from EMM. Using an indirect mass balance approach, Fahey et al. (2005) estimated that ECM fungi contributed around 12% of the overall soil CO2 efflux in a Fagusdominated hardwood forest. Hasselquist et al. (2010) adopted a modelling approach, combined with measurements of soil CO2 and minirhizotron observations of rhizomorph production, and concluded that ca 15% of soil CO2 efflux arose from EMM of ECM fungi in a conifer forest. Indeed, the highest rates of CO2 efflux were correlated with periods of maximum rhizomorph production. The most direct determination of respiration from EMM conducted in the field to date suggests that the ECM contribution to soil CO2 efflux may be even greater. By inserting collars containing mesh of

200

J.W.G. Cairney / Soil Biology & Biochemistry 47 (2012) 198e208

different sizes, that were designed to exclude EMM and/or roots into conifer forest soil, Heinemeyer et al. (2007) estimated that the EMM was responsible for ca 25e35% of soil CO2 efflux. Living mycelia of ECM fungi are also known to excrete a range of carbon-containing compounds into soil that includes sugars, polyols, amino acids, peptides, proteins, hydroxamate siderophores, various low molecular weight organic acids and pigments (Sun et al., 1999; Jones et al., 2004; Johansson et al., 2008, 2009). Much of this exudation occurs at the EMM growing front and, while some of the sugars and other compounds are probably reabsorbed by the hyphae, such exudation is likely to be important in maintaining hyphal homeostasis (Sun et al., 1999). Most is known about organic acid exudation, and it is clear that ECM fungi release a variety of these compounds, including oxalic, citric and malonic acids and that such exudation is likely to vary between different taxa (eg Lapeyrie et al., 1987; Griffiths et al., 1994; Van Schöll et al., 2006; Tuason and Arocena, 2009; Johansson et al., 2009). Notwithstanding the fact that up to 70% of excreted oxalate can be bound to EMM hyphae (Arvieu et al., 2003), the presence of ECM fungi in a root system has been shown to significantly increase exudation of organic acids into tree rhizospheres in some circumstances (Ahonen Jonnarth et al., 2000; Casarin et al., 2003; Johansson et al., 2008, 2009). In other cases, no overall increase in exudation has been observed, but ECM infection has been shown to alter the types of organic acids excreted, with the predominant organic acid varying when different ECM fungal taxa are present (Van Schöll et al., 2006). The quantities of the different organic acids excreted also appear to depend upon the ECM fungal genotypes and can be influenced by edaphic factors that include calcium, nitrogen, magnesium, phosphorus and potassium availability or the presence of toxic metals (Paris et al., 1996; Ahonen Jonnarth et al., 2000; Arvieu et al., 2003; Van Hees et al., 2006; Johansson et al., 2008, 2009; Fransson and Johansson, 2009; Tuason and Arocena, 2009). In axenic culture, exudation of carbon-containing compounds from ECM fungal mycelia can comprise up to 40% of the fungal carbon budget (Fransson et al., 2007b), however this probably overestimates the exudation from EMM of ECM fungi growing in planta. For Hebeloma crustuliniforme growing symbiotically with Pinus sylvestris in a microcosm system, it was tentatively estimated that excretion of oxalate, often the most abundant organic acid produced by ECM seedlings (Fransson and Johansson, 2009), comprised 2e4% of the total fungal carbon budget (Van Hees et al., 2006). While this would constitute ca 0.2% of the carbon assimilated by the host plant, a subsequent study, using the same plant host but different ECM fungal taxa, estimated that the proportion of host-derived carbon exuded by ECM fungi was an order of magnitude lower (Johansson et al., 2009). 4. EMM biomass and carbon storage in forest soils Much of the carbon that enters ECM fungi from their host trees is incorporated into fungal biomass and, in many forests, this constitutes a significant fraction of overall below-ground biomass. Estimates of fungal biomass in ECM root tips in forest stands, for example, range from ca 20e10,000 kg ha
1, depending on forest type, climatic factors and/or the proportion of root tip biomass regarded as fungal for calculation (ranges from ca 2e40%) (Fogel and Hunt, 1979; Vogt et al., 1982; Dahlberg et al., 1997; Satomura et al., 2003; Sims et al., 2007; Helmisaari et al., 2009; Okada et al., 2011). EMM is also a significant below-ground biomass component in many forests, and is generally concentrated in upper layers of the soil profile (Bååth et al., 2004; Wallander et al., 2004; Göransson et al., 2006). In two-dimensional soil microcosms and at

the outer edge of soil-filled tubes, extension of ECM mycelia can be rapid (8 mm d
1), and vary between different taxa (Coutts and Nicholl, 1990; Read, 1992; Donnelly et al., 2004). Rates of growth in the field are less clear, but EMM growth in Swedish coniferous and deciduous forests is known to be seasonal, with growth in winter reduced to <20e30% of the peak autumn growth rates (Wallander et al., 2001; Hagerberg and Wallander, 2002; Nilsson et al., 2007). It also varies considerably between different forest sites and over different years (Wallander et al., 2011). Minirhizotron observations of ECM rhizomorph dynamics indicate that production of these structures also follows a similar seasonal pattern in a mixed conifer forest in California (Hasselquist et al., 2010). An indirect estimate of soil microbial biomass, derived using fumigation-extraction methods, suggested that EMM of ECM fungi may constitute in excess of one third of the total microbial biomass (equivalent to an estimated 58 kg carbon ha
1) in a Swedish conifer forest (Högberg and Högberg, 2002). This is considerably greater than the 8 kg carbon ha
1 estimated by direct observation of hyphal and rhizomorph length (presumed to be largely ECM fungal) in ECM mat soils in North American conifer forests (Ingham et al., 1991). Because it is difficult to discriminate EMM of ECM fungi from mycelia of saprotrophs in soil, the best estimates of ECM mycelial biomass in forest soils have been obtained by ergosterol or phospholipid fatty acid (PLFA) analysis of sand-filled hyphal ingrowth bags (Wallander et al., 2001, 2004). As these bags do not contain organic matter, they select largely for ECM mycelia over those of saprotrophs, a fact that has been confirmed by trenching experiments, along with d13C and DNA analyses that indicate that the bulk (ca 85e90%) of colonisation of such bags in a range of forest soils is by EMM of ECM fungi (Wallander et al., 2001, 2003, 2010; Hagerberg and Wallander, 2002; Nilsson and Wallander, 2003; Bastias et al., 2006; Kjøller, 2006). Although the limitations of this approach must be acknowledged, including the probably erroneous assumption that there is no mycelial turnover during incubation of the bags in soil and that mycelial colonisation of sand approximates that in soil (Wallander et al., 2001; Hendricks et al., 2006), data obtained in this fashion suggest that EMM biomass in coniferous forests can be some 100e600 kg ha
1 (Wallander et al., 2001, 2004; Hagerberg et al., 2003). Assuming that fungal biomass comprises ca 50% carbon (Wallander et al., 2011), this would represent some 50e300 kg carbon ha
1. Where soil has been substituted for sand in hyphal ingrowth bags, estimates of EMM biomass within a similar range have been obtained (Hendricks et al., 2006; Sims et al., 2007). Growth and/or biomass of EMM in soil are strongly affected by edaphic factors such as nutrient status, temperature and moisture (Nilsson and Wallander, 2003; Nilsson et al., 2005, 2007; Clemmensen et al., 2006; Hendricks et al., 2006; Sims et al., 2007; Wallander et al., 2011). In the case of forest fertilization, at least, the effect on EMM was found to be strongly site-specific in Swedish conifer forests, with the addition of a complete fertilizer reducing EMM growth, perhaps indirectly via host tree growth responses (Wallander et al., 2011). It is also evident that EMM production differs in forest stands of different age. By comparing 40 Norway spruce stands of up 130 yrs old, Wallander et al. (2010) demonstrated that EMM production was greatest at ca 10e20 yrs, which coincided with the time of canopy closure, a fact that was further supported by the observations of Wallander et al. (2011). Whether this represents a direct effect of stand age on EMM production per se, or reflects shifts that were observed in ECM fungal community structure (in favour of taxa that produce more EMM) is unclear. Real-time PCR using taxon-specific primers has the potential to facilitate estimation of EMM biomass for individual ECM fungal species in soil. For quantification, this method requires information on the number of copies of the target gene that are present in the

J.W.G. Cairney / Soil Biology & Biochemistry 47 (2012) 198e208

mycelium or standardisation using cultured mycelium (van der Linde et al., 2009), and to date has only been used to estimate EMM biomass in soil for two taxa. Thus it has been estimated that Lactarius deliciosus produces up to 125 mg and Boletus edulis 258 mg EMM kg
1 soil (¼ca 62 and 229 mg carbon respectively) in conifer plantations (Parladé et al., 2007; Hortal et al., 2009; De la Varga et al., 2012). While quantification has not yet been achieved for other taxa, spatial and temporal variation in the relative amounts EMM biomass in soil has been observed for several further taxa using this method (Suz et al., 2008; van der Linde et al., 2009), emphasising its potential value for future investigations. Using a d13C analysis approach, combined with hyphal ingrowth cores to separate EMM from fine roots, Godbold et al. (2006) estimated that EMM may account for as much as 10 tonnes ha
1 over a two-year period (equal to 62% of new carbon added to soil) in a Populus alba plantation. Using a similar approach, Wallander et al. (2011) concluded that carbon input to soil via EMM was somewhat lower (0.3e1.1 tonnes ha
1 annually) in Picea abies plantations. In addition to rhizomorphs and more diffuse hyphae, EMM of ECM fungi also periodically supports sporocarps of various types that can constitute a considerable, but transient, biomass, ranging from a few to several hundred kg ha
1 in some forests (eg. Fogel and Trappe, 1978; Fogel and Hunt, 1979; Vogt et al., 1982; Dahlberg et al., 1997; Sims et al., 2007; De la Varga et al., 2012). Some taxa, also produce other structures, notably sclerotia, that can constitute several thousand kg ha
1 biomass in some forest soils (Fogel and Hunt, 1979; Watanabe et al., 2004) and represent a frequently underestimated ECM fungal biomass component. 5. Turnover of carbon stored in ECM root and mycelial biomass While there is no question that EMM can represent a substantial component of forest soil biomass, its significance in carbon sequestration will depend strongly on rates of turnover.

201

Unfortunately, our understanding of the dynamics of ECM biomass, and in particular EMM, remains relatively scant, but several recent studies have provided new insights. The longevity of ECM root tips in soil has been estimated by either direct observation, a biomass-based approach (mean root tip longevity ¼ mean annual root tip biomass divided by annual mortality) or by 14C dating. With such a variety of approaches, and an equally diverse array of criteria, including different visual indictors of root vitality or disappearance, used to signal root tip death, it is perhaps not surprising that the estimates of longevity vary from months to several yrs (Table 1). Most investigations, however, indicate the life-span of an individual ECM root tip as a few months (Orlov, 1960; Vogt et al., 1982, 1986; Downes et al., 1992; Majdi and Nylund, 1996; Rygiewicz et al., 1997; Majdi et al., 2001), although this may vary with factors such as nutrient availability (Alexander and Fairley, 1983; Majdi and Nylund, 1996; Majdi et al., 2001). ECM root tip longevity may also be influenced by soil depth: in a Pinus taeda-dominated plantation, for example, the median life span of an ECM root tip was estimated by minirhizotron observation to be 147 d at 15e30 cm depth, but approximately half of this for equivalent tips in the upper 15 cm of the soil profile (Pritchard et al., 2008). A mean ECM root tip life-span of 159 d and a similar depth-related effect was also observed in a model longleaf pine-wiregrass community (McCormack et al., 2010). While a range of ECM genera, including Boletus, Cenococcum, Cortinarius, Hebeloma, Morchella, Paxillus and Pisolithus form sclerotia (Peterson et al., 2004), relatively little is known about the longevity of these structures (Table 1). Miller et al. (1994) reported that viable sclerotia of Cenococcum geophilum and a Morchella sp. can survive for at least two years, however other studies suggest that, perhaps following forest fires that prevented germination, dead, highly-melanised sclerotia of C. geophilum may have persisted in A horizon soil for up to several thousand years (Watanabe et al., 2007; Benedict, 2011). Turnover of carbon in sporocarp biomass is difficult to assess. While many ECM fungi produce

Table 1 Published estimates of mean, median and maximum longevities of ectomycorrhizal (ECM) roots, sclerotia and mycelia in the field. ECM component Root tips Intact ECM tips Intact ECM tips Intact ECM tips Intact ECM tips Excised ECM tips Intact ECM tips Intact ECM tips Intact ECM tips Intact ECM tips Intact ECM tips Intact ECM tips Excised ECM tips Intact ECM tips Intact ECM tips Intact ECM tips Excised ECM tips Sclerotia Intact sclerotia Sclerotial remains Sclerotial remains Rhizomorphs Intact rhizomorphs Intact rhizomorphs Intact rhizomorphs Diffuse mycelium Hebeloma EMM a b c

mean. median. maximum longevity.

Estimated longevity

Methodology

Reference

>3 yearsc >9 monthsc 14 monthsa 4 monthsa >9 monthsc <12 monthsa <6 monthsa 8 monthsc 8 monthsb <6 monthsb <22 monthsb >2 yearsc 1e6 yearsc 5 monthsb 5 monthsa >6 monthsc

direct observation direct observation biomass method biomass method direct observation biomass method biomass method direct observation direct observation direct observation direct observation direct observation carbon dating direct observation direct observation direct observation

Orlov (1960) Harley (1969) Vogt et al. (1982) Alexander and Fairley (1983) Ferrier and Alexander (1985) Vogt et al. (1986) Santantonio and Santantonio (1987) Downes et al. (1992) Majdi and Nylund (1996) Rygiewicz et al. (1997) Majdi et al. (2001) Langley et al. (2006) Treseder et al. (2004) Pritchard et al. (2008) McCormack et al. (2010) Koide et al. (2011)

>2 yearsc 240 yearsc 4900 yearsc

presence after fire carbon dating carbon dating

Miller et al. (1994) Watanabe et al. (2007) Benedict (2011)

11 monthsa 17 monthsa 15 monthsb

direct observation direct observation direct observation

Treseder et al. (2005) Pritchard et al. (2008) McCormack et al. (2010)

<1 yearc

real time PCR

Guidot et al. (2004)

202

J.W.G. Cairney / Soil Biology & Biochemistry 47 (2012) 198e208

ephemeral epigeous basidiomes for which turnover is effected in a matter of days, the longevity of sporocarps of many, especially hypogeous taxa, is unknown (North et al., 1997; Weber, 2001). Although rates of decomposition of excised roots are unlikely to mirror those of roots that senesce as they remain attached to the plant host, useful observations have been made by burying excised ECM roots in nylon mesh hyphal ingrowth bags in the field (Table 1). Using this approach, Ferrier and Alexander (1985) found that intact ECM root tips persisted for at least nine months. Langley et al. (2006) concluded that ECM root tips of Pinus edulis decomposed 65% slower than uncolonised tips, thus suggesting that ECM infection slows decomposition. In contrast, Koide et al. (2011) found that colonisation of Pinus resinosa roots by Amanita citrina, Amanita muscaria or Tylopilus felleus significantly increased rates of decomposition, and that infection by a range of other ECM fungal taxa had no effect on rates of root decomposition. While this might, to some extent, reflect the different time-spans over which the observations were made (24 and 6 months in the two studies respectively), the latter study clearly indicates that the presence of different ECM fungal taxa on roots affects their susceptibility to decomposition and highlights a difficulty in generalising with regard to persistence and decomposition of ECM roots in the field. Certain ECM fungal taxa do not produce large spreading EMM systems in soil and, for one such fungus (Hebeloma cylindrosporum), a competitive PCR approach suggested that EMM persisted in soil for less than a year (Guidot et al., 2004) (Table 1). Direct observations of Laccaria proxima EMM in soil-filled acrylic tubes also indicated that EMM disappeared within 4e6 months of production (Coutts and Nicholl, 1990). Because single genotypes of some ECM fungal taxa are known to have spread by mycelial growth through soil over tens of metres in some forests (see Section 2 above), and since estimated mycelial growth rates indicate that such expansion occurred over periods of many years, there has perhaps been an erroneous assumption that EMM of these taxa can persist in soil for tens of years (Cairney, 2005). Recent direct observations and experimental evidence suggest that turnover of much of the EMM produced by these taxa may be considerably more rapid. Due to difficulties in visualising diffuse mycelium and individual hyphae in soil, direct assessments of EMM longevity in the field have been few, and limited largely to observations of rhizomorphs via minirhizotrons (Table 1). Although this method does not definitively discriminate ECM rhizomorphs from those of saprotrophs, many of the latter produce rhizomorphs at the soil:litter interface (Thompson, 1984) and it is likely that a substantive proportion of the rhizomorphs in soil are ECM. Mean or median longevities of up to ca 17 months have been predicted in three such studies, however a significant proportion of rhizomorphs may persist for several years (Treseder et al., 2005; Pritchard et al., 2008; McCormack et al., 2010). One study reported that rhizomorph longevity increased with their diameter and was lower in the upper 15 cm of the soil profile than at a depth of 15e30 cm (Pritchard et al., 2008). In contrast, McCormack et al. (2010) found that rhizomorph longevity was negatively correlated with diameter. Direct minirhizotron observations of arbuscular mycorrhizal fungal hyphae, that are larger than those of ECM fungi and so can be observed in such chambers, suggest that some individual hyphae can persist for >5 months in a grassland soil (Treseder et al., 2010). Whether diffuse parts of EMM systems of ECM fungi persist over a similar timescale remains unclear. EMM systems are, however, intrinsically dynamic, and often a diffuse mycelial front will colonise soil, after which much of the diffuse mycelium disappears as aggregated rhizomorphic mycelium forms behind the growing front over a period of tens of d (Donnelly et al., 2004). This undoubtedly reflects some hyphal turnover during that timeframe, and that rhizomorph and/or arbuscular mycorrhizal hyphal

turnover may not be good predictors of rates of turnover a significant component of EMM biomass. Other approaches also suggest that turnover of some EMM may be more rapid than is implied by observations of rhizomorphs (Table 1). Bhupinderpal-Singh et al. (2003) observed an increase in d13C in CO2 respired from soil during the first few weeks following tree girdling and suggested that, at least in part, this might reflect decomposition of EMM that is naturally enriched with 13C. Following insertion of cores into soil in order to sever EMM from roots, Lindahl et al. (2010) observed a sharp decline in ECM fungal DNA sequences inside the cores within 14 d that was taken to reflect a decline in EMM abundance. In addition, dry weight losses from cultured ECM mycelia that were buried in mesh hyphal ingrowth bags in forest soil for 37 d were also considerable, and varied from ca 35e80%, depending on the fungal species (Koide et al., 2011). CO2 efflux from macerated ECM mycelial necromass incubated in soil under laboratory conditions was also found to be rapid, peaking at 14 d, further emphasising rapid decomposition (Wilkinson et al., 2011). Interestingly, these authors also found that CO2 efflux increased with diversity when mycelia of multiple ECM fungal taxa were incorporated into soil, suggesting that care must be applied in extrapolating from rates of decomposition of single fungal isolates to rates of decomposition in complex EMM fungal communities in forest soils. Clearly, such experimental approaches that use macerated, or even intact, hyphal necromass as substrate are unlikely to reflect patterns of decomposition and turnover of EMM that remains functionally integrated with a host. Grazing on EMM by fungivorous arthropods is, however, commonplace in soil (Ek et al., 1994; Setälä, 1995; Pollierer et al., 2007) and may result in severing of hyphal fragments, and perhaps even larger areas of mycelium, from the EMM that is in contact with a tree host. Similarly, other natural disturbances, including digging during foraging by mycophagous mammals (eg. Johnson, 1997; North et al., 1997), may also result in significant disruption of mycelial continuity and effectively sever regions of EMM from the plant host. The relationships between grazers and decomposers in this context requires further clarification, but it is clear that interactive effects of these two groups will be pivotal in determining rates of EMM turnover in soil. The observations outlined above, however, suggest that a significant proportion of EMM may turn over considerably faster than is suggested by observations of rhizomorph longevity. 6. How will climate change influence ECM fungi and their EMM? The concentration of carbon dioxide in the atmosphere ([CO2]) is predicted to exceed 550 ml l
1 by the end of the century, and is likely to be accompanied by an increase in global mean surface temperature of as much as 4.4  C (Solomon et al., 2007). Although the responses of trees to these altered climate parameters have been extensively documented (eg Norby et al., 1999; Lloyd and Farquhar, 2008), the likely impacts on their ECM fungal symbionts are more poorly understood. As a result of enhanced photosynthesis, more carbon is likely to be allocated to root systems under future elevated ([CO2]) scenarios, leading to increased below-ground plant productivity (eg. de Graaff et al., 2006; Iversen, 2010). This could facilitate enhanced transfer of carbon to ECM fungi that might help mitigate the likely increased plant demand for mineral nutrients under elevated [CO2] (Treseder, 2004). Investigations of climate change effects on ECM associations have increased in recent years, but to date most work has focused on the effect of elevated ([CO2]) on infection levels of seedlings in either pots or microcosms in climate-controlled chambers or glasshouses. Although some

J.W.G. Cairney / Soil Biology & Biochemistry 47 (2012) 198e208

studies found no evidence for an effect of elevated [CO2] on ECM infection (Rouhier and Read, 1999; Pérez-Soba et al., 1995; Gorissen and Kuyper, 2000; Weigt et al., 2011), many have reported increased numbers of ECM roots and/or % ECM infection of up to 110% under such conditions (Norby et al., 1987; O’Neill et al., 1987; Ineichen et al., 1995; Bernston et al., 1997; Godbold et al., 1997; Rygiewicz et al., 1997, 2000; Rouhier and Read, 1998; Walker et al., 1998; Lewis et al., 1994; Fransson et al., 2005). These effects, however, seem to be temporary in some cases and are influenced by factors such as ECM fungal taxa, season, nutrient availability, soil moisture and/or the degree to which [CO2] is elevated (Walker et al., 1995, 1998; Rygiewicz et al., 2000; Lewis et al., 1994; Fransson et al., 2005). Nor do they necessarily hold for all host tree taxa: in the case of Tsuga canadensis, which forms both ECM and AM symbioses, elevated [CO2] had no effect on ECM infection, but significantly increased AM infection (Godbold et al., 1997). Root senescence as a result of lengthy growth periods in pot or microcosm systems may also result in temporal differences in the outcomes of such experiments (O’Neill et al., 1987). Field-based assessments from either open-top chamber or freeair CO2 enrichment (FACE) experiments have also provided evidence for increased numbers of ECM roots and % ECM infection under elevated [CO2] conditions (Wiemken et al., 2001; Kasurinen et al., 2005; Garcia et al., 2008). Direct observations via minirhizotrons further indicate that production of ECM root tips in the field can increase considerably (by up to 194%) under conditions of elevated [CO2] (Rygiewicz et al., 1997; Tingey et al., 1997; Pritchard et al., 2008; McCormack et al., 2010), although this effect was found to be more pronounced in soil at a depth of >15 cm than in surface soil (Pritchard et al., 2008; McCormack et al., 2010). Less is known about the likely effects of increased temperature on ECM associations, but two investigations of long term experimental warming of Arctic tundra vegetation reported that it had no effect on ECM colonisation (Clemmensen et al., 2006; Deslippe et al., 2011). Reports of effects of elevated [CO2] on ECM root tip longevity have been more varied. While Rygiewicz et al. (1997) observed no effect of elevated [CO2], others have reported increased longevity of ECM root tips in the upper 15 cm of the soil profile under elevated [CO2] (Pritchard et al., 2008; McCormack et al., 2010). Significantly, two of these studies also concluded that elevated [CO2] led to increased turnover of ECM root tips (ca 25% decrease in longevity) in deeper soil (Pritchard et al., 2008; McCormack et al., 2010). While 19 years of experimental warming was found to increase species richness of ECM fungi associated with Arctic Betula nana (Deslippe et al., 2011), based on investigations conducted under controlled glasshouse conditions or in the field, there appears to be no evidence for a significant effect of elevated [CO2] on species richness of ECM fungal communities in root tips (Godbold and Berntson, 1997; Godbold et al., 1997; Rygiewicz et al., 2000; Fransson et al., 2001; Parrent et al., 2006) or their mycelia in sandfilled hyphal ingrowth bags (Parrent and Vilgalys, 2007). Equally consistent has been the observation that the relative abundance of individual ECM fungal taxa within these communities changes in response to elevated [CO2] (Godbold and Berntson, 1997; Godbold et al., 1997; Rey and Jarvis, 1997; Rygiewicz et al., 2000; Fransson et al., 2001; Kasurinen et al., 2005; Parrent et al., 2006; Parrent and Vilgalys, 2007; Edwards and Zak, 2011). There is also good evidence for altered community composition in response to increased temperature or drought (Gehring et al., 1998; Nilsen et al., 1998; Shi et al., 2002; Cavender-Bares et al., 2009; Deslippe et al., 2011). Interestingly, while Parrent et al. (2006) reported that the abundance of a Tylospora sp. in ECM root tips decreased in response to elevated [CO2] in a FACE experiment, the abundance of its mycelium in sand-filled hyphal ingrowth bags increased (Parrent and Vilgalys, 2007), which was suggested by the authors to

203

reflect altered resource partitioning in response to host demand for additional nutrients. In other studies, shifts in ECM fungal community composition in favour of taxa that produce copious extramatrical hyphae and/or rhizomorphs have been observed under elevated [CO2] (Godbold and Berntson, 1997; Godbold et al., 1997). Long term warming has also been reported to alter ECM fungal community composition in favour of taxa, particularly Cortinariaceae, that produce abundant EMM (Deslippe et al., 2011). Such changes may have implications for carbon allocation beyond EMM biomass, for example an increase in the importance of taxa that exude relatively large quantities of organic acids may result in enhanced release of carbon from EMM (Johansson et al., 2009). It may also facilitate increased EMM-mediated inter-plant carbon movements (Deslippe and Simard, 2011). On the basis of a meta-analysis of published literature, Alberton et al. (2005) concluded that production of EMM by ECM fungi generally responds positively to elevated [CO2]. This is borne out by work using gnotobiotic or non-sterile model laboratory systems, where EMM biomass and surface area have both been shown to increase by up to three fold under elevated [CO2] for several ECM fungal and host combinations (Ineichen et al., 1995; Rouhier and Read, 1998, 1999; Fransson et al., 2005, 2007a). Data from a 14CO2 labelling experiment indicate that this is often associated with increased carbon allocation to the ECM fungi under elevated [CO2], which drives increased EMM biomass production rather than increased carbon accumulation per unit biomass (Gorissen and Kuyper, 2000; Fransson et al., 2007a). The extent of these effects appears, however, to be species-specific, and, importantly, no significant effect of elevated [CO2] on EMM biomass production and/or 14C allocation was observed for several taxa (Gorissen and Kuyper, 2000; Fransson et al., 2007a). Similarly, direct observations of EMM produced by Piloderma croceum and Tomentellopsis submollis in glasshouse rhizotrons provided no evidence for increased production under elevated [CO2] (Weigt et al., 2011). PLFA analysis of sand-filled hyphal ingrowth bags buried in soil at FACE or open-top chamber experiments also indicated that elevated [CO2] did not stimulate increased EMM biomass in the field (Kasurinen et al., 2005; Parrent and Vilgalys, 2007), while Godbold et al. (2006) found no evidence for an effect of elevated [CO2] on ECM-mediated carbon input to forest soil. In contrast, in the only study where it has been investigated in this context, warming resulted in a significant increase in EMM associated with dwarf B. nana in Arctic tundra (Clemmensen et al., 2006). Notwithstanding the fact that minirhizotron observations of rhizomorphs in the field undoubtedly include those of some saprotrophic fungi, this approach has provided some evidence for increased rhizomorph production, but also increased mortality, under elevated [CO2] (Pritchard et al., 2008; McCormack et al., 2010). In general, smaller rhizomorphs were found to have lower survivorship, and larger rhizomorphs greater survivorship under elevated [CO2] (McCormack et al., 2010), while the effects on both production and mortality varied with soil depth (Pritchard et al., 2008; McCormack et al., 2010). Exudation of carbon compounds, including organic acids, amino acids and monosaccharides, from ECM seedlings of P. sylvestris has been reported to increase by up to 270% under elevated [CO2] (Fransson and Johansson, 2009; Johansson et al., 2009), however effects on individual organic acids appear to vary with different ECM fungal taxa (Fransson and Johansson, 2009). Elevated [CO2] also tends to increase below-ground respiration in gnotobiotic ECM plant-soil systems, although this seems to vary with different ECM taxa and, in most cases, may reflect increased EMM production rather than altered carbon use efficiency by the fungi (Gorissen and Kuyper, 2000; Fransson et al., 2007a). In the case of a Laccaria bicolor isolate, however, elevated [CO2] promoted increased

204

J.W.G. Cairney / Soil Biology & Biochemistry 47 (2012) 198e208

respiration with no increase in EMM growth, suggesting that poorer carbon use efficiency occurs in some instances (Gorissen and Kuyper, 2000). Other climate change factors, namely temperature and moisture availability, also appear to affect respiration by ECM fungi. Based on results from a Pinus contorta plantation, Heinemeyer et al. (2007) concluded that soil moisture limitation reduced respiration from EMM, but that changes in soil temperature had no direct effect. Respiratory responses of ECM fungi to temperature in axenic culture are variable, but generally increase with temperature (Hacskaylo et al., 1965; Malcolm et al., 2008). This is consistent with observed temperature-related increases in microbial respiration from soil over the short term that are thought to largely reflect increased maintenance respiration (Schindlbacher et al., 2011). On the face of it, such increased respiratory losses might to some extent offset potential EMM biomass increases that might arise as a result of elevated [CO2]. Some ECM fungal isolates have, however, been shown to rapidly acclimate to increased temperature in axenic culture, such that respiration rates are lower when acclimated at higher rather than lower temperature (Malcolm et al., 2008). Acclimation in this way, particularly over the time scales that environmental warming is likely to occur, may thus have some potential to ameliorate temperature-related increases in carbon loss by respiration. As highlighted by Malcolm et al. (2008), the observed variation in the abilities of different ECM fungi to acclimate to increased temperature means that responses of the belowground ECM fungal community as a whole must be considered to predict likely responses of complex communities in the field. Indeed, differences in carbon use efficiency of individual taxa brought about by differential acclimation to temperature may drive changes in community structure over the longer term in favour of those taxa that are more efficient producers of biomass. This appears to be the case for overall soil microbial respiration where acclimation to temperature over the longer term appears to be related to altered microbial community structure (Bradford et al., 2010). Clearly more research on community level responses of ECM fungi to temperature increases will be required, along with interactions with other trophic levels in soil.

diffuse EMM will be significantly more rapid than has been observed for rhizomorphs. The clear challenge now is to better understand the distribution and dynamics of diffuse EMM in different forest soils, probably via further application of hyphal ingrowth bags or cores (sensu Johnson et al., 2001), and to use manipulative experiments to clarify relationships between EMM turnover and arthropod grazing. Elevated [CO2] is likely to increase carbon allocation to ECM fungi from their tree hosts, resulting in increased root tip colonisation. Changes in the relative abundance of taxa in below-ground ECM fungal communities are also likely, perhaps in favour of taxa that produce significant EMM. Climate change effects on EMM production will be complex and in some circumstances may be confounded by effects on carbon use efficiency. While microcosm experiments suggest that elevated [CO2] can increase EMM production in some ECM taxa, other than increased rhizomorph production (but also mortality), the limited work conducted to date has found no evidence for this in the field. There is, however, some evidence that warming might increase EMM production under some circumstances. Effects of future climate change on turnover of EMM remain difficult to predict but, given the likely importance of interactions between grazing soil arthropods, decomposer microorganisms and EMM turnover, responses of the former groups to climate change will have a strong influence on how EMM turnover is affected. Responses of decomposer microorganisms to climate change, particularly over the longer term remain the subject of debate (Allison et al., 2010). Although the reactions of soil arthropods to climate change are likely to be multifaceted and contextdependent (Lindroth, 2010), there is clear evidence that climate change will have both direct and indirect effects on their communities. Thus warming and soil moisture have been shown to directly affect arthropod richness and or community composition, while elevated [CO2], via its impacts on plant productivity and ECM fungi, affects these indirectly (eg Kardol et al., 2011; Makkonen et al., 2011). Understanding such multitrophic responses to climate change will be pivotal to predicting the significance of ECM fungi in below-ground carbon storage under these conditions, and this should be seen as a priority area for future research.

7. Conclusions

Acknowledgements

Extramatrical mycelia of ECM fungi are significant sinks for plant-derived carbon. Although EMM systems are thus important facilitators of carbon delivery into soil, our lack of understanding of their physical and physiological continuity in the field means that the scale over which this occurs remains unclear. A significant proportion of the carbon that flows to EMM is respired and, to a lesser extent, some is undoubtedly lost via exudations from living hyphae. Unfortunately, information here is fairly scant, and there is a need to quantify such losses under a broader range of edaphic conditions. Along with ECM root tips, it is clear that EMM constitutes a substantial biomass component in many forest soils, meaning that ECM fungi have the potential to transiently sequester carbon below-ground. The significance of EMM in this context will clearly depend on turnover rates. While fine root dynamics has been highlighted elsewhere as a major gap in understanding carbon cycling processes (Strand et al., 2008), the dynamics of EMM probably merits similar recognition. Although progress in understanding EMM dynamics has been hampered by difficulties in visualising EMM in soil, direct observations indicate that, in common with ECM root tips, rhizomorphs may persist for a few weeks or many months in some circumstances. There is also good evidence that excised mycelia decompose significantly within a few days in soil and, because of the likely interactions between EMM, grazing arthropods and decomposers, it seems likely that turnover of more

Preparation of this review was partly supported by an ARC Linkage International Awards Grant. References Agerer, R., 2001. Exploration types of ectomycorrhizae. A proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11, 107e114. Ahonen Jonnarth, U., van Hees, P.A.W., Lundström, U.S., Finlay, R.D., 2000. Organic acids produced by mycorrhizal Pinus sylvestris exposed to elevated aluminium and heavy metal concentrations. New Phytologist 146, 557e567. Alberton, O., Kuyper, T.W., Gorissen, A., 2005. Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO2. New Phytologist 167, 859e868. Alexander, I.J., Fairley, R.I., 1983. Effects of N fertilisation on populations of fine roots and mycorrhizas in spruce humus. Plant and Soil 71, 49e53. Allison, S.D., Wallenstein, M.D., Bradford, M.A., 2010. Soil-carbon response to warming dependent on microbial physiology. Nature Geoscience 3, 336e340. Anderson, I.C., Cairney, J.W.G., 2007. Ectomycorrhizal fungi: exploring the mycelial frontier. FEMS Microbiology Reviews 31, 388e406. Anderson, I.C., Chambers, S.M., Cairney, J.W.G., 1998. Use of molecular methods to estimate the size and distribution of mycelial individuals of the ectomycorrhizal basidiomycete Pisolithus tinctorius. Mycological Research 102, 295e300. Arvieu, J.-C., Leprince, F., Plassard, C., 2003. Release of oxalate and protons by ectomycorrhizal fungi in response to P-deficiency and calcium carbonate in nutrient solution. Annals of Forest Science 60, 815e821. Bååth, E., Nilsson, L.O., Göransson, H., Wallander, H., 2004. Can the extent of degradation of soil fungal mycelium during soil incubation be used to estimate ectomycorrhizal biomass in soil? Soil Biology and Biochemistry 36, 2105e2109.

J.W.G. Cairney / Soil Biology & Biochemistry 47 (2012) 198e208 Bastias, B.A., Xu, Z., Cairney, J.W.G., 2006. Influence of repeated long-term repeated prescribed burning on mycelial communities of ectomycorrhizal fungi. New Phytologist 172, 149e158. Beiler, K.J., Durall, D.M., Simard, S.W., Maxwell, S.A., Kretzer, A.M., 2010. Architecture of the wood-wide web: Rhizopogon spp. genets link multiple Douglas-fir cohorts. New Phytologist 185, 543e553. Bending, G.D., Read, D.J., 1995. The structure and function of the vegetative mycelium of ectomycorrhizal plants. V. Foraging behaviour and translocation of nutrients from exploited litter. New Phytologist 130, 401e409. Benedict, J.B., 2011. Sclerotia as indicators of mid-Holocene tree-limit altitude, Colorado Front Range, USA. The Holocene 21, 1021e1023. Bernston, G.M., Wayne, P.M., Bazzaz, F.A., 1997. Below-ground architectural and mycorrhizal responses to elevated CO2 in Betula alleghaniensis populations. Functional Ecology 11, 684e695. Bevege, D.I., Bowen, G.D., Skinner, M.F., 1975. Comparative carbohydrate physiology of ecto- and endomycorrhizas. In: Sanders, F.E., Mosse, B., Tinker, P.B. (Eds.), Endomycorhizas. Academic Press, New York, USA, pp. 149e174. Bhupinderpal-Singh, Nordgren, A., Löfvenius, M.O., Högberg, M.N., Mellander, P.-E., Högberg, P., 2003. Tree root and soil heterotrophic respiration as revealed by girdling of boreal Scots pine forest: extending observations beyond the first year. Plant, Cell and Environment 26, 1287e1296. Bidartondo, M.I., Ek, H., Wallander, H., Söderström, B., 2001. Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytologist 151, 543e550. Bonello, P., Bruns, T.D., Gardes, M., 1998. Genetic structure of a natural population of the ectomycorrhizal fungus Suillus pungens. New Phytologist 138, 533e542. Bradford, M.A., Watts, B.W., Davies, C.W., 2010. Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Global Change Biology 16, 1576e1588. Cairney, J.W.G., 2005. Basidiomycete mycelia in forest soils: dimensions, dynamics and roles in nutrient distribution. Mycological Research 109, 7e20. Cairney, J.W.G., Alexander, I.J., 1992. A study of ageing of spruce [Picea sitchensis (Bong.) Carr.] ectomycorrhizas. II. Carbohydrate allocation in ageing Picea sitchensis/Tylospora fibrillosa (Burt.) Donk ectomycorrhizas. New Phytologist 122, 153e158. Cairney, J.W.G., Burke, R.M., 1994. Fungal enzymes degrading plant cell walls: their possible significance in the ectomycorrhizal symbiosis. Mycological Research 98, 1345e1356. Cairney, J.W.G., Burke, R.M., 1996. Physiological heterogeneity within fungal mycelia: an important concept for a functional understanding of the ectomycorrhizal symbiosis. New Phytologist 134, 685e695. Cairney, J.W.G., Ashford, A.E., Allaway, W.G., 1989. Distribution of photosynthetically fixed carbon within root systems of Eucalyptus pilularis ectomycorrhizal with Pisolithus tinctorius. New Phytologist 112, 495e500. Casarin, V., Plassard, C., Souche, G., Arvieu, J.-C., 2003. Quantification of oxalate ions and protons released by ectomycorrhizal fungi in rhizosphere soil. Agronomie 23, 461e469. Cavender-Bares, J., Izzo, A., Robinson, R., Lovelock, C.E., 2009. Changes in ectomycorrhizal community structure on two containerized oak hosts across an experimental hydrological gradient. Mycorrhiza 19, 133e142. Clemmensen, K.E., Michelsen, A., Jonasson, S., Shaver, G.R., 2006. Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytologist 171, 391e404. Corrêa, A., Hampp, R., Magel, E., Martins-Loução, M.-A., 2011. Carbon allocation in ectomycorrhizal plants at limited and optimal N supply: an attempt at unravelling conflicting theories. Mycorrhia 21, 35e51. Coutts, M.P., Nicholl, B.C., 1990. Growth and survival of shoots, roots, and mycorrhizal mycelium in clonal Sitka spruce during the first growing season after planting. Canadian Journal of Forest Research 20, 861e868. Cullings, K., Courty, P.-E., 2009. Saprotrophic capabilities as functional traits to study functional diversity and resilience of ectomycorrhizal community. Oecologia 161, 661e664. Dahlberg, A., Stenlid, J., 1990. Population structure and dynamics in Suillus bovinus as indicated by spatial distribution of fungal clones. New Phytologist 115, 478e493. Dahlberg, A., Stenlid, J., 1995. Spatiotemporal patterns in ectomycorrhizal populations. Canadian Journal of Botany 73 (Suppl. 1), S1222eS1230. Dahlberg, A., Jonsson, L., Nylund, J.E., 1997. Species diversity and distribution of biomass above and below ground among ectomycorrhizal fungi in an oldgrowth Norway spruce forest in south Sweden. Canadian Journal of Botany 75, 1323e1335. de Graaff, M.-A., van Groenigen, K.-J., Six, J., Hungate, B., van Kessel, C., 2006. Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Global Change Biology 12, 2077e2091. De la Varga, H., Águeda, B., Martínez-Peña, F., Parladé, J., Pera, J., 2012. Quantification of extraradical soil mycelium and ectomycorrhizas of Boletus edulisin a Scots pine forest with variable sporocarp productivity. Mycorrhiza 22, 59e68. Deslippe, J.R., Simard, S.W., 2011. Below-ground carbon transfer among Betula nanamay increase with warming in Arctic tundra. New Phytologist 192, 689e698. Deslippe, J.R., Hartmann, M., Mohn, W.W., Simard, S.W., 2011. Long-term experimental manipulation alters the ectomycorrhizal community of Betula nana in Arctic tundra. Global Change Biology 17, 1625e1636. Donnelly, D.P., Boddy, L., Leake, J.R., 2004. Development, persistence and regeneration of foraging ectomycorrhizal mycelial systems in soil microcosms. Mycorrhiza 14, 37e45.

205

Downes, G.M., Alexander, I.J., Cairney, J.W.G., 1992. A study of ageing of spruce [Picea sitchensis (Bong.) Carr.] ectomycorrhizas. I. Morphological and cellular changes in mycorrhizas formed by Tylospora fibrillosa (Burt.) Donk and Paxillus involutus (Batsch. Ex Fr.) Fr. New Phytologist 122, 141e152. Dunham, S.M., Kretzer, A., Pfrender, M.E., 2003. Characterization of Pacific golden chanterelle (Cantharellus formosus) genet size using co-dominant microsatellite markers. Molecular Ecology 12, 1607e1618. Durall, D.M., Jones, M.D., Tinker, P.B., 1994. Allocation of 14C-carbon in ectomycorrhizal willow. New Phytologist 128, 109e114. Edwards, I.P., Zak, D.R., 2011. Fungal community composition and function after long-term exposure of northern forests to elevated atmospheric CO2 and tropospheric O3. Global Change Biology 17, 2184e2195. Ek, H., 1997. The influence of nitrogen fertilization on the carbon economy of Paxillus involutus in ectomycorrhizal association with Betula pendula. New Phytologist 135, 133e142. Ek, H., Sjögren, M., Arnebrant, K., Söderström, B., 1994. Extramatrical mycelial growth, biomass allocation and nitrogen uptake in ectomycorrhizal systems in response to collembolan grazing. Applied Soil Ecology 1, 155e169. Erland, S., Finlay, R., Söderström, B., 1991. The influence of substrate pH on carbon translocation in ectomycorrhizal and non-mycorrhizal pine seedlings. New Phytologist 119, 235e242. Fahey, T.J., Tierney, G.L., Fitzhugh, R.D., Wilson, G.F., Siccama, T.G., 2005. Soil respiration and soil carbon balance in a northern hardwood forest ecosystem. Canadian Journal of Forest Research 35, 244e253. Ferrier, R.C., Alexander, I.J., 1985. Persistence under field conditions of excised fine roots and mycorrhizas of spruce. In: Fitter, A.H., Atkinson, D., Read, D.J., Busher, M. (Eds.), Ecological Interactions in Soil. Blackwell Scientific Publications, Oxford, United Kingdom, pp. 175e179. Finlay, R.D., Read, D.J., 1986. The structure and function of the vegetative mycelium of ectomycorrhizal plants. I. Translocation of 14C-labelled carbon between plants interconnected by a common mycelium. New Phytologist 103, 143e156. Finlay, R., Söderström, B., 1992. Mycorrhiza and carbon flow to the soil. In: Allen, M.F. (Ed.), Mycorrhizal Functioning: an Integrative Plant-Fungal Process. Chapman & Hall, New York, USA, pp. 134e160. Fogel, R., Hunt, G., 1979. Fungal and arboreal biomass in a western Oregon Douglasfir ecosystem: distribution patterns and turnover. Canadian Journal of Forest Research 9, 245e256. Fogel, R., Trappe, J.M., 1978. Fungus consumption (mycophagy) by small animals. Northwest Science 52, 1e31. Fransson, P.M.A., Johansson, E.M., 2009. Elevated CO2 and nitrogen influence exudation of soluble organic compounds by ectomycorrhizal root systems. FEMS Microbiology Ecology 71, 186e196. Fransson, P.M.A., Taylor, A.F.S., Finlay, R.D., 2001. Elevated atmospheric CO2 alters root symbiont community structure in forest trees. New Phytologist 152, 431e442. Fransson, P.M.A., Taylor, A.F.S., Finlay, R.D., 2005. Mycelial production, spread and root colonisation by the ectomycorrhizal fungi Hebeloma crustuliniforme and Paxillus involutus under elevated atmospheric CO2. Mycorrhiza 15, 25e31. Fransson, P.M.A., Anderson, I.C., Alexander, I.J., 2007a. Does carbon partitioning in ectomycorrhizal pine seedlings under elevated CO2 vary with fungal species? Plant and Soil 291, 323e333. Fransson, P.M.A., Anderson, I.C., Alexander, I.J., 2007b. Ectomycorrhizal fungal isolates respond differently to increased carbon availability. FEMS Microbiology Ecology 61, 246e257. Garcia, M.O., Ovasapyan, T., Greas, M., Treseder, K.K., 2008. Mycorrhizal dynamics under elevated CO2 and nitrogen fertilization in a warm temperate forest. Plant and Soil 303, 301e310. Gehring, C.A., Theimer, T.C., Whitham, T.G., Keim, P., 1998. Ectomycorrhizal fungal community structure of Pinyon pines growing in two environmental extremes. Ecology 79, 1562e1572. Godbold, D.L., Berntson, G.M., 1997. Elevated atmospheric CO2 concentration changes ectomycorrhizal morphotype assemblages in Betula papyrifera. Tree Physiology 17, 347e350. Godbold, D.L., Berntson, G.M., Bazzaz, F.A., 1997. Growth and mycorrhizal colonization of three North American tree species under elevated atmospheric CO2. New Phytologist 137, 433e440. Godbold, D.L., Hoosbeek, M.R., Lukac, M., Cotrufo, M.F., Janssens, I.A., Ceulemans, R., Polle, A., Velthorst, E.J., Scarascia-Mugnozza, G., de Angelis, P., Miglietta, F., Peressotti, A., 2006. Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant and Soil 281, 15e24. Göransson, H., Wallander, H., Ingerslev, M., Rosengren, U., 2006. Estimating the relative nutrient uptake from different soil depths in Quercus robur, Fagus sylvatica and Picea abies. Plant and Soil 286, 87e97. Gorissen, A., Kuyper, T.W., 2000. Fungal species-specific responses of ectomycorrhizal Scots pine (Pinus sylvestris) to elevated [CO2]. New Phytologist 146, 163e168. Griffiths, R.P., Baham, J.E., Caldwell, B.A., 1994. Soil solution chemistry of ectomycorrhizal mats in forest soil. Soil Biology and Biochemistry 26, 331e337. Gryta, H., Debaud, J.-C., Effosse, A., Gay, G., Marmeisse, R., 1997. Fine-scale structure of polulations of the ectomycorrhizal fungus Hebeloma cylindrosporum in coastal sand dune forest ecosystems. Molecular Ecology 6, 353e364. Guidot, A., Debaud, J.-C., Effosse, A., Marmeisse, R., 2004. Below-ground distribution and persistence of an ectomycorrhizal fungus. New Phytologist 161, 539e548. Hacskaylo, E., Palmer, J.G., Vozzo, J.A., 1965. Effects of temperature on growth and respiration of ectotrophic mycorrhizal fungi. Mycologia 57, 748e756.

206

J.W.G. Cairney / Soil Biology & Biochemistry 47 (2012) 198e208

Hagerberg, D., Wallander, H., 2002. The impact of forest residue removal and wood ash amendment on the growth of the ectomycorrhizal external mycelium. FEMS Microbiology Ecology 39, 139e146. Hagerberg, D., Thelin, G., Wallander, H., 2003. The production of ectomycorrhizal mycelium in forests: relation between forest nutrient status and local mineral sources. Plant and Soil 252, 279e290. Harley, J.L., 1969. Ecology of ectotrophic mycorrhizas. In: Polunin, N. (Ed.), The Biology of Mycorrhiza. Leonard Hill, London, United Kingdom, pp. 150e162. Hasselquist, N.J., Vargos, R., Allen, M.F., 2010. Using soil sensing technology to examine interactions and controls between ectomycorrhizal growth and environmental factors on soil CO2 dynamics. Plant and Soil 331, 17e29. Heinemeyer, A., Hartley, I.P., Evans, S.P., De la Fuente, J.A.C., Ineson, P., 2007. Forest soil CO2 flux: uncovering the contribution and environmental responses of ectomycorrhizas. Global Change Biology 13, 1786e1797. Heinonsalo, J., Hurme, K.-R., Sen, R., 2004. Recent 14C-labelled assimilate allocation to Scots pine seedling root and mycorrhizosphere compartments developed on reconstructed podzol humus, E- and B- mineral horizons. Plant and Soil 259, 111e121. Helmisaari, H.S., Ostonen, I., Lõhmus, K., Derome, J., Lindroos, A.J., Merilä, P., Nöjd, P., 2009. Ectomycorrhizal root tips in relation to site and stand characteristics in Norway spruce and Scots pine stands in boreal forests. Tree Physiology 29, 445e456. Hendricks, J.J., Mitchell, R.J., Kuehn, K.A., Pecot, S.D., Sims, S.E., 2006. Measuring external mycelia production of ectomycorrhizal fungi in the field: the soil matrix matters. New Phytologist 171, 179e186. Högberg, M.N., Högberg, P., 2002. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytologist 154, 791e795. Högberg, P., Read, D.J., 2006. Towards a more plant physiological perspective on soil ecology. Trends in Ecology and Evolution 21, 548e554. Högberg, P., Nordgren, A., Buchmann, N., Taylor, A.F.S., Ekblad, A., Högberg, M.N., Nyberg, G., Ottosson-Löfvenius, M., Read, D.J., 2001. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411, 789e792. Hortal, S., Pera, J., Parladé, J., 2009. Field persistence of the edible ectomycorrhizal fungus Lactarius deliciosus: effects of inoculation strain, initial colonization level, and site characteristics. Mycorrhiza 19, 167e177. Ineichen, K., Wiemken, V., Wiemken, A., 1995. Shoots, roots and ectomycorrhiza formation of pine seedlings at elevated atmospheric carbon dioxide. Plant, Cell and Environment 18, 703e707. Ingham, E.R., Griffiths, R.P., Cromack, K., Entry, J.A., 1991. Comparison of direct vs. fumigation incubation microbial biomass estimates from ectomycorrhizal mat and non-mat soils. Soil Biology and Biochemistry 23, 465e471. Iversen, C.M., 2010. Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems. New Phytologist 186, 346e357. Johansson, E.M., Fransson, P.M.A., Finlay, R.D., van Hees, P.A.W., 2008. Quantitative analysis of root and ectomycorrhizal exudates as a response to Pb, Cd and As stress. Plant and Soil 313, 39e54. Johansson, E.M., Fransson, P.M.A., Finlay, R.D., van Hees, P.A.W., 2009. Quantitative analysis of soluble exudates produced by ectomycorrhizal roots as a response to ambient and elevated CO2. Soil Biology and Biochemistry 41, 1111e1116. Johnson, C.N., 1997. Fire and habitat management for a mycophagous marsupial, the Tasmanian bettong Bettongia gaimardi. Australian Journal of Ecology 22, 101e105. Johnson, D., Leake, J.R., Read, D.J., 2001. Novel in-growth core system enables functional studies of grassland mycorrhizal mycelial networks. New Phytologist 152, 555e562. Jones, D.L., Hodge, A., Kuzyakov, Y., 2004. Plant and mycorrhizal regulation of rhizodeposition. New Phytologist 163, 459e480. Kardol, P., Reynolds, W.N., Norby, R.J., Classen, A.T., 2011. Climate change effects on soil microarthropod abundance and community structure. Applied Soil Ecology 47, 37e44. Kasurinen, A., Keinanen, M.M., Kaipainen, S., Nilsson, L.O., Vapaavuori, E., Kontro, M.H., Holopainen, T., 2005. Belowground responses of silver birch trees exposed to elevated CO2 and O-3 levels during three growing seasons. Global Change Biology 11, 1167e1179. Kjøller, R., 2006. Disproportionate abundance between ectomycorrhizal root tips and their associated mycelia. FEMS Microbiology Ecology 58, 214e224. Klein, D.A., Paschke, M.W., 2004. Filamentous fungi: the indeterminate lifestyle and microbial ecology. Microbial Ecology 47, 224e235. Koide, R.T., Fernandez, C.W., Peoples, M.S., 2011. Can ectomycorrhizal colonization of Pinus resinosa roots affect their decomposition? New Phytologist 191, 508e514. Körner, C., Asshoff, R., Bignucolo, O., Hättenschwiler, S., Keel, S.G., Pelaez-Riedl, S., Pepin, S., Siegwolf, R.T.W., Zotz, G., 2005. Carbon flux and growth in mature deciduous forest trees exposed to elevated CO2. Science 309, 1360e1362. Langley, J.A., Chapman, S.K., Hungate, B.A., 2006. Ectomycorrhizal colonization slows root decomposition: the post-mortem fungal legacy. Ecology Letters 9, 955e959. Lapeyrie, F., Chilvers, G.A., Bhem, C.A., 1987. Oxalic acid synthesis by the ectomycorrhizal fungus Paxillus involutus. New Phytologist 106, 139e146. Leake, J.R., Donnelly, D.P., Saunders, E.M., Boddy, L., Read, D.J., 2001. Rates and quantities of carbon flux to ectomycorrhizal mycelium following 14C pulse labeling of Pinus sylvestris seedlings: effects of litter patches and interaction with a wood-decomposer fungus. Tree Physiology 21, 71e82.

Lewis, J.D., Thomas, R.B., Strain, B.R., 1994. Effect of elevated CO2 on mycorrhizal colonization of loblolly pine (Pinus taeda L.) seedlings. Plant and Soil 165, 81e88. Lian, C., Narimatsu, M., Nara, K., Hogetsu, T., 2006. Tricholoma matsutake in a natural Pinus densiflora forest: correspondence between above- and below-ground genets, association with multiple host trees and alteration of existing ectomycorrhizal communities. New Phytologist 171, 825e836. Lindahl, B.D., de Boer, W., Finlay, R.D., 2010. Disruption of root carbon transport into forest humus stimulates fungal opportunists at the expense of mycorrhizal fungi. ISME Journal 4, 872e881. Lindroth, R.L., 2010. Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. Journal of Chemical Ecology 36, 2e21. Lloyd, J., Farquhar, G.D., 2008. Effects of rising temperatures and [CO2] on the physiology of tropical forest trees. Philosophical Transactions of the Royal Society B-Biological Sciences 363, 1811e1817. Majdi, H., Nylund, J.-E., 1996. Does liquid fertilization affect fine root dynamics and lifespan of mycorrhizal short roots? Plant and Soil 185, 305e309. Majdi, H., Damm, E., Nylund, J.E., 2001. Longevity of mycorrhizal roots depends on branching order and nutrient availability. New Phytologist 150, 195e202. Makkonen, M., Berg, M.P., van Hal, J.R., Callaghan, T.V., Press, M.C., Aerts, R., 2011. Traits explain the responses of a sub-arctic Collembola community to climate manipulation. Soil Biology and Biochemistry 43, 377e384. Malcolm, G.A., López-Gutiérrez, J.C., Koide, R.T., Eissenstat, D.M., 2008. Acclimation to temperature and temperature sensitivity of metabolism by ectomycorrhizal fungi. Global Change Biology 14, 1169e1180. McCormack, M.L., Pritchard, S.G., Breland, S., Davis, M.A., Prior, S.A., Runion, B., Mitchell, R.J., Rogers, H.H., 2010. Soil fungi respond more strongly than fine roots to elevated CO2 in a model regenerating longleaf pine-wiregrass ecosystem. Ecosystems 13, 901e916. Melin, E., Nilsson, H., 1957. Transport of C14-labelled photosynthate to the fungal associate of pine mycorrhiza. Svensk Botanisk Tidskrift 51, 166e186. Miller, S.L., Torres, P., McClean, T.M., 1994. Persistence of basidiospored and sclerotia of ectomycorrhizal fungi and Morchella in soil. Mycologia 86, 89e95. Miller, S.L., Durall, D.M., Rygiewicz, P.T., 1989. Temporal allocation of 14C to extramatrical hyphae of ectomycorrhizal ponderosa pine seedlings. Tree Physiology 5, 239e249. Murata, H., Ohta, A., Yamada, A., Narimatsu, M., Futamura, N., 2005. Genetic mosaics in the massive persisting rhizosphere colony “shiro” of the ectomycorrhizal basidiomycete Tricholoma matsutake. Mycorrhiza 15, 505e512. Nelson, C.D., 1964. The production and translocation of photosynthate C-14 in conifers. In: Zimmernan, M.H. (Ed.), Formation of Wood in Forest Trees. Maria Mons Cabot Foundation, New York, USA, pp. 235e257. Nilsen, P., Børja, I., Knutsen, H., Brean, R., 1998. Nitrogen and drought effects on ectomycorrhizae of Norway spruce [Picea abuse L. (Karst.)]. Plant and Soil 198, 179e184. Nilsson, L.O., Wallander, H., 2003. Production of external mycelium by ectomycorrhizal fungi in a Norway spruce forest was reduced in response to nitrogen fertilization. New Phytologist 158, 409e416. Nilsson, L.O., Giesler, R., Bååth, E., Wallander, H., 2005. Growth and biomass of mycorrhizal mycelia in coniferous forests along short natural nutrient gradients. New Phytologist 165, 613e622. Nilsson, L.O., Bååth, E., Falkengren-Grerup, U., Wallander, H., 2007. Growth of ectomycorrhizal mycelia and composition of soil microbial communities in oak forest soils along a nitrogen deposition gradient. Oecologia 153, 375e384. Norby, R.J., O’Neill, E.G., Hood, W.G., Luxmore, R.J., 1987. Carbon allocation, root exudation and mycorrhizal colonization of Pinus echinata seedlings grown under CO2 enrichment. Tree Physiology 3, 203e210. Norby, R.J., Wullschleger, S.D., Gunderson, C.A., Johnson, D.W., Ceulemans, R., 1999. Tree responses to rising CO2 in field experiments: implications for the future forest. Plant Cell, and Environment 22, 683e714. North, M., Trappe, J., Frankin, J., 1997. Standing crop and animal consumption of fungal sporocarps in Pacific Northwest forests. Ecology 78, 1543e1554. Norton, J.M., Smith, J.L., Firestone, M.K., 1990. Carbon flow in the rhizosphere of ponderosa pine seedlings. Soil Biology and Biochemistry 22, 449e455. Okada, K., Okada, S., Yasue, K., Fukuda, M., Yamada, A., 2011. Six-year monitoring of pine ectomycorrhizal biomass under a temperate monsoon climate indicates significant annual fluctuations in relation to climatic factors. Ecological Research 26, 411e419. Olsson, S., 1999. Nutrient translocation and electrical signalling in mycelia. In: Gow, N.A.R., Robson, G.D., Gadd, G.M. (Eds.), The Fungal Colony. Cambridge University Press, Cambridge, United Kingdom, pp. 25e48. Orlov, A., 1960. Growth and changes with age of feeder roots of Picea excelsa Link. Botanicheskii Zhurnal 45, 888e896. Orwin, K.H., Kirschbaum, M.U.F., St John, M.G., Dickie, I.A., 2011. Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a modelbased assessment. Ecology Letters 14, 493e502. O’Neill, E.G., Luxmoore, R.J., Norby, R.J., 1987. Increases in mycorrhizal colonization and seedling growth in Pinus echinata and Quercus alba in an enriched CO2 atmosphere. Canadian Journal of Forest Research 17, 878e883. Paris, F., Botton, B., Lapeyrie, F., 1996. In vitro weathering of phlogopite by ectomycorrhizal fungi II. The effect of Kþ and Mg2þ deficiency and N sources on accumulation of oxalate and Hþ. Plant and Soil 179, 141e150. Parladé, J., Hortal, S., Pera, J., Galipienso, L., 2007. Quantitative detection of Lactarius deliciosus extraradical soil mycelium by real-time PCR and its application in the

J.W.G. Cairney / Soil Biology & Biochemistry 47 (2012) 198e208 study of fungal persistence and interspecific competition. Journal of Biotechnology 128, 14e23. Parrent, J.L., Vilgalys, R., 2007. Biomass and compositional responses of ectomycorrhizal fungal hyphae to elevated CO2 and nitrogen fertilization. New Phytologist 176, 164e174. Parrent, J.L., Morris, W.F., Vilgalys, R., 2006. CO2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87, 2278e2287. Pérez-Soba, M., Dueck, T.A., Puppi, G., Kuiper, P.J.C., 1995. Interactions of elevated CO2, NH3 and O3 on mycorrhizal infection, gas exchange and N metabolism in saplings of Scots pine. Plant and Soil 176, 107e116. Peterson, R.L., Massicotte, H.B., Melville, L.H., 2004. Mycorrhizas: Anatomy and Cell Biology. CABI Publishing, Wallingford, United Kingdom. Pollierer, M.M., Langel, R., Körner, C., Maraun, M., Scheu, S., 2007. The underestimated importance of belowground carbon input for forest soil animal food webs. Ecology Letters 10, 729e736. Pritchard, S.G., Strand, A.E., McCormack, M.L., Davis, M.A., Oren, R., 2008. Mycorrhizal and rhizomorph dynamics in a loblolly pine forest during 5 years of freeair-CO2-enrichment. Global Change Biology 14, 1e13. Qu, L.Y., Shinano, T., Quoreshi, A.M., Tamai, Y., Osaki, M., Koike, T., 2004. Allocation of 14C carbon in two species of larch seedlings infected with ectomycorrhizal fungi. Tree Physiology 24, 1369e1376. Read, D.J., 1992. The mycorrhizal mycelium. In: Allen, M.J. (Ed.), Mycorrhizal Functioning: an Integrative Plant-Fungal Process. Chapman & Hall, New York, USA, pp. 102e133. Reid, C.P.P., Kidd, F.A., Ekwebelam, S.A., 1983. Nitrogen nutrition, photosynthesis and carbon allocation in ectomycorrhizal pine. Plant and Soil 71, 415e432. Rey, A., Jarvis, P.G., 1997. Growth responses of young birch trees (Betula pendula Roth.) after four and a half years of CO2 exposure. Annals of Botany 80, 809e816. Rosling, A., Lindahl, B.D., Finlay, R.D., 2004. Carbon allocation to ectomycorrhizal roots and mycelium colonising different mineral substrates. New Phytologist 162, 795e802. Rouhier, H., Read, D.J., 1998. Plant and fungal responses to elevated atmospheric carbon dioxide in mycorrhizal seedlings of Pinus sylvestris. Environmental and Experimental Botany 40, 237e246. Rouhier, H., Read, D.J., 1999. Plant and fungal responses to elevated atmospheric CO2 in mycorrhizal seedlings of Betula pendula. Environmental and Experimental Botany 42, 231e241. Rygiewicz, P.T., Andersen, C.P., 1994. Mycorrhizae alter quality and quantity of carbon allocated below ground. Nature 369, 58e60. Rygiewicz, P.T., Johnson, M.G., Ganio, L.M., Tingey, D.T., Storm, M.J., 1997. Lifetime and temporal occurrence of ectomycorrhizae on Ponderosa pine (Pinus ponderosa Laws) seedlings grown under varied atmospheric CO2 and nitrogen levels. Plant and Soil 189, 275e287. Rygiewicz, P.T., Martin, K.J., Tuininga, A.R., 2000. Morphotype community structure of ectomycorrhizas on Douglas fir (Pseudotsuga menziesii Mirb. Franco) seedlings grown under elevated atmospheric CO2 and temperature. Oecologia 124, 299e308. Santantonio, D., Santantonio, E., 1987. Effect of thinning on production and mortality of fine roots in a Pinus radiata plantation on a fertile site in New Zealand. Canadian Journal of Forest Research 17, 919e928. Satomura, T., Nakatsubo, T., Horikoshi, T., 2003. Estimation of the biomass of fine roots and mycorrhizal fungi: a case study in a Japanese red pine (Pinus densiflora) stand. Journal of Forest Research 8, 221e225. Sawyer, N.A., Chambers, S.M., Cairney, J.W.G., 1999. Molecular investigation of genet distribution and genetic variation of Cortinarius rotundisporus. New Phytologist 142, 561e568. Schindlbacher, A., Rodler, A., Kuffner, M., Ktzler, B., Sessitch, A., ZechmeisterBoltenstern, S., 2011. Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biology and Biochemistry 43, 1417e1425. Selosse, M.A., Richard, F., He, X., Simard, S.W., 2006. Mycorrhizal networks: des liaisons dangereuses? Trends in Ecology and Evolution 21, 621e628. Setälä, H., 1995. Growth of birch and pine seedlings in relation to grazing by soil fauna on ectomycorrhizal fungi. Ecology 76, 1844e1851. Setälä, H., Kulmala, P., Mikola, J., Markkola, A.M., 1999. Influence of ectomycorrhiza on the structure of detrital food webs in pine rhizosphere. Oikos 87, 113e122. Shi, L., Guttenberger, M., Kottke, I., Hampp, R., 2002. The effect of drought on mycorrhizas of beech (Fagus sylvatica L.): changes in community and nitrogen storage bodies of the fungi. Mycorrhiza 12, 303e311. 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, 579e582. Simard, S.W., Jones, M.D., Durall, D.M., 2002. Carbon and nutrient fluxes within and between mycorrhizal plants. In: van der Heijden, M.G.A., Sanders, I.R. (Eds.), Mycorrhizal Ecology. Springer, Berlin, Germany, pp. 33e74. Sims, S.E., Hendricks, J.J., Mitchell, R.J., Kuehn, K.A., Pecot, S.D., 2007. Nitrogen decreases and precipitation increases ectomycorrhizal extrametrical mycelia production in a longleaf pine forest. Mycorrhiza 17, 299e309. Smith, S.E., Read, D.J., 2008. Mycorrhizal Symbiosis. Academic Press, New York, USA. Söderström, B., 1992. The ecological potential of the ectomycorrhizal mycelium. In: Read, D.J., Lewis, D.H., Fitter, A.H., Alexander, I.J. (Eds.), Mycorrhizas in Ecosystems. CAB International, Wallingford, United Kingdom, pp. 77e83. Söderström, B., Read, D.J., 1987. Respiratory activity of intact and excised ectomycorrhizal mycelial systems growing in unsterilized soil. Soil Biology and Biochemistry 19, 231e236.

207

Solomon, S., Qin, D., Manning, M., Alley, R.B., Berntsen, T., Bindoff, N.L., Chen, Z., Chidthaisong, A., Gregory, J.M., Hegerl, G.C., Heimann, M., Hewitson, B., Hoskins, B.J., Joos, F., Jouzel, J., Kattsov, V., Lohmann, U., Matsuno, T., Molina, M., Nicholls, N., Overpeck, J., Raga, G., Ramaswamy, V., Ren, J., Rusticucci, M., Somerville, R., Stocker, T.F., Whetton, P., Wood, R.A., Wratt, D., 2007. Technical summary. In: Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L. (Eds.), Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom, pp. 21e87. Steinmann, K.T.W., Siegwolf, R., Saurer, M., Körner, C., 2004. Carbon fluxes to the soil in a mature temperate forest assessed by C-13 isotope tracing. Oecologia 141, 489e550. Strand, A.E., Pritchard, S.G., McCormack, M.L., Davis, M.A., Oren, R., 2008. Irreconcilible differences: fine-root life spans and soil carbon persistence. Science 319, 456e458. Sun, Y.-P., Unestam, T., Lucas, S.D., Johanson, K.J., Kenne, L., Finlay, R.D., 1999. Exudation-reabsorption in mycorrhizal fungi, the dynamic interface for interaction with soil and other microorganisms. Mycorrhiza 9, 137e144. Suz, L.M., Martin, M.P., Oliach, D., Fischer, C.R., Colinas, C., 2008. Mycelial abundance and other factors related to truffle productivity in Tuber melanosporumeQuercus ilex orchards. FEMS Microbiology Letters 285, 72e78. Talbot, J.M., Allison, S.D., Treseder, K.K., 2008. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Functional Ecology 22, 955e963. Teramoto, M., Wu, B., Hogetsu, T., Transfer of 14C-photosynthate to the sporocarp of an ectomycorrhizal fungus Laccaria amethystina. Mycorrhiza, in press. Teste, F.P., Simard, S.W., Durall, D.M., Guy, R.D., Berch, S.M., 2010. Net carbon transfer between Pseudotsuga menziesii var. glauca seedlings in the field is influenced by soil disturbance. Journal of Ecology 98, 429e439. Thompson, W., 1984. Distribution, development and functioning of mycelial cord systems of decomposer basidiomycetes of the deciduous woodland floor. In: Jennings, D.H., Rayner, A.D.M. (Eds.), The Ecology and Physiology of the Fungal Mycelium. Cambridge University Press, Cambridge, United Kingdom, pp. 185e215. Tingey, D.T., Phillips, D.L., Johnson, M.G., Strom, M.J., Ball, J.T., 1997. Effects of elevated CO2 and N fertilization on fine root dynamics and fungal growth in seedling Pinus ponderosa. Environmental and Experimental Botany 37, 73e83. Treseder, K.K., 2004. A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytologist 164, 347e355. Treseder, K.K., Allen, M.F., 2000. Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytologist 147, 189e200. Treseder, K.K., Masiello, C.A., Lansing, J.L., Allen, M.F., 2004. Species-specific measurements of ectomycorrhizal turnover under N-fertilization: combining isotopic and genetic approaches. Oecologia 138, 419e425. Treseder, K.K., Allen, M.F., Ruess, R.W., Pregitzer, K.S., Hendrick, R.L., 2005. Lifespans of fungal rhizomorphs under nitrogen fertilization in a pinyon-juniper woodland. Plant and Soil 270, 249e255. Treseder, K.K., Schimel, J.P., Garcia, M.O., Whiteside, M.D., 2010. Slow turnover and production of fungal hyphae during a Californian dry season. Soil Biology and Biochemistry 42, 1657e1660. Tuason, M.M.S., Arocena, J.M., 2009. Calcium oxalate biomineralization by Piloderma fallax in response to various levels of calcium and phosphorus. Applied and Environmental Microbiology 75, 7079e7085. van der Linde, S., Alexander, I.J., Anderson, I.C., 2009. Spatial distribution of sporocarps of stiptate hydnoid fungi and their belowground mycelium. FEMS Microbiology Ecology 69, 344e352. Van Hees, P.A.W., Rosling, A., Essén, S., Godbold, D.L., Jones, D.L., Finlay, R.D., 2006. Oxalate and ferricrocin exudation by the extramatrical mycelium of an ectomycorrhizal fungus in symbiosis with Pinus sylvestris. New Phytologist 169, 367e378. Van Schöll, L., Hoffland, E., van Breenan, N., 2006. Organic acid exudation by ectomycorrhizal fungi and Pinus sylvestris in response to nutrient deficiencies. New Phytologist 170, 153e163. Vogt, K.A., Grier, C.C., Edmonds, R.L., Meier, C.E., 1982. Mycorrhizal role in net primary production and nutrient cycling in Abies amabilis (Dougl.) Forbes ecosystems in western Washington. Ecology 63, 370e380. Vogt, K.A., Grier, C.C., Vogt, D.J., 1986. Production, turnover and nutrient dynamics of above- and belowground detritus of world forests. Advances in Ecological Research 15, 303e377. Walker, R.F., Geisinger, D.R., Johnson, D.W., Ball, J.T., 1995. Enriched atmospheric CO2 and soil P effects on growth and ectomycorrhizal colonization of juvenile ponderosa pine. Forest Ecology and Management 78, 207e215. Walker, R.F., Johnson, D.W., Geisinger, D.R., Ball, J.T., 1998. Growth and ectomycorrhizal colonization of ponderosa pine seedlings supplied with different levels of atmospheric CO2 and soil N and P. Forest Ecology and Management 109, 9e20. Wallander, H., Nilsson, L.-O., Hagerberg, D., Bååth, E., 2001. Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytologist 151, 753e760. Wallander, H., Mahmood, S., Hagerberg, D., Johansson, L., Pallon, J., 2003. Elemental composition of ectomycorrhizal mycelia identified by PCR-RFLP analysis and growth in contact with apatite or wood ash in forest soil. FEMS Microbiology Ecology 44, 57e65.

208

J.W.G. Cairney / Soil Biology & Biochemistry 47 (2012) 198e208

Wallander, H., Göransson, H., Rosengren, U., 2004. Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia 139, 89e97. Wallander, H., Johansson, U., Sterkenburg, E., Duling, M.B., Lindahl, B.D., 2010. Production of ectomycorrhizal mycelium peaks during canopy closure in Norway spruce forests. New Phytologist 187, 1124e1134. Wallander, H., Ekblad, A., Bergh, J., 2011. Growth and carbon sequestration by ectomycorrhizal fungi in intensively fertilized Norway spruce forests. Forest Ecology and Management 262, 999e1007. Watanabe, M., Ohishi, S., Pott, A., Hardenbicker, U., Aoki, K., Sakagami, N., Ohta, H., Fujitake, N., 2004. Morphology, chemical properties and distribution of sclerotium grains found in forest soils, Harz Mts., Germany. Soil Science and Plant Nutrition 50, 863e870. Watanabe, M., Sato, H., Matsuzaki, H., Kobayashi, T., Sakagami, N., Maejima, Y., Ohta, H., Fujitake, N., Hiradate, S., 2007. 14C ages and d13C of sclerotium grains found in forest soils. Soil Science and Plant Nutrition 53, 125e131. Weber, N.S., 2001. Musings on mushrooming. McIlvainea 15, 63e76. Weigt, R.B., Raidl, S., Verma, R., Rodenkirchen, H., Göttlein, A., Agerer, R., 2011. Effects of twice-ambient carbon dioxide and nitrogen amendment on biomass,

nutrient contents and carbon costs of Norway spruce seedlings as influenced by mycorrhization with Piloderma croceum and Tomentellopsis submollis. Mycorrhiza 21, 375e391. Whiteside, M.D., Treseder, K.K., Atsatt, P.R., 2009. The brighter side of soils: quantum dots track organic nitrogen through fungi and plants. Ecology 90, 100e108. Wiemken, V., Ineichen, K., Boller, T., 2001. Development of ectomycorrhizas in model beechespruce ecosystems on siliceous and calcareous soil: a 4-year experiment with atmospheric CO2 enrichment and nitrogen fertilization. Plant and Soil 234, 99e108. Wilkinson, A., Alexander, I.J., Johnson, D., 2011. Species richness of ectomycorrhizal hyphal necromass stimulates soil CO2 efflux. Soil Biology and Biochemistry 43, 1350e1355. Wu, B., Nara, K., Hogetsu, T., 2001. Can 14C-labelled photosynthesis products move between Pinus densiflora seedlings linked by ectomycorrhizal mycelia? New Phytologist 149, 137e146. Wu, B., Nara, K., Hogetsu, T., 2002. Spatiotemporal transfer of carbon-14-labelled photosynthate from ectomycorrhizal Pinus densiflora seedlings to extraradical mycelia. Mycorrhiza 12, 83e88.