Review

Blackwell Science, Ltd

Tansley review Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging

Author for correspondence: Melanie D. Jones Tel. +1 (250) 762 5445 ext. 7553 Fax: +1 (250) 470 6004 or 6005 Email: [email protected]

Melanie D. Jones1, Daniel M. Durall1 and John W. G. Cairney2 1

Biology Department, Okanagan University College, Kelowna, British Columbia V1V 1V7, Canada;

2

Mycorrhiza Research Group, Centre for Horticulture & Plant Science, Parramatta Campus, University

of Western Sydney, Locked Bag 1797, Penrith South DC NSW 1797, Australia

Received: 18 July 2002 Accepted: 22 November 2002

Contents Summary

399

I. Introduction

400

IV. Which is the most important factor driving changes in the ECM fungal community after clearcut logging: inoculum loss or change in the below-ground environment? 406

II. Population biology and inoculum potential of ectomycorrhizal fungi

401

V. Possible consequences for regenerating stands of species shifts in ectomycorrhizal fungi

III. Ectomycorrhiza development on seedlings regenerating after clearcut logging

402

VI. Conclusions

414 416

Summary Key words: clearcut, silviculture, ectomycorrhizal fungal communities, diversity, inoculum, fire.

The effects on the ectomycorrhizal fungal community of clearcut logging, which is used to harvest millions of hectares of ectomycorrhizal forest annually, has been studied for a number of years. Here, we review current knowledge of inoculum sources for ectomycorrhizal fungi in forests and then re-examine earlier studies of ectomycorrhizas on young trees in regenerating stands. We conclude that, taken separately from the effects of site preparation, the major impact of clearcut logging is to change the species composition of the ectomycorrhizal fungal community rather than to reduce the percentage of roots colonized. A thorough examination of site preparation treatments suggests that the changes in fungal species composition are driven by changes in the biology and chemistry of the soil environment after clearcutting as much as they are by loss or change in fungal inoculum. This is an important conclusion because it implies that these new ectomycorrhizal fungal communities are better adapted to the new conditions than the ones in the forest would have been. The shift in fungal species composition and diversity will have implications for seedling establishment and competition. The effects of individual fungi or diverse assemblages of fungi on seedling growth, and effects of changes in the ability of young trees to associate with a common mycelium are discussed. © New Phytologist (2003) 157: 399–422

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I. Introduction Worldwide, millions of hectares of ectomycorrhizal (ECM) forests are at least partially harvested each year, with more than 5 000 000 ha of these being clearcut (Table 1). In clearcut logging (clearfelling), all trees are removed from an area several hectares to tens of hectares in size. A few trees that are too small to harvest or that are of an undesirable species (such as Betula spp. or Populus spp. in stands being harvested for conifers) might be left standing. Small saplings and seedlings that were present in the understory of the forest, and were left behind during harvesting, are referred to as ‘advanced regeneration’ (Helms, 1998). Other types of harvesting remove trees in small groups or result in a thinning of the stand without any areas being totally cleared. In many countries, the majority of logged areas are left to regenerate naturally from the seed bank, but substantial areas are still replanted with seedlings grown in commercial nurseries (Table 1). These seedlings may be of the same species or a subset of the species previously growing on the site. Before planting, especially in wet or cold regions, the organic soil horizons may be removed or displaced by mechanical site preparation or burning. Clearcut logging and subsequent site preparation change the environment of ECM fungi. Consequently we expect to observe differences in colonization or fungal species composition between seedlings growing on clearcuts and those growing in forests. Because ECM fungi differ amongst themselves

in important respects such as their ability to access nutrients of different forms and complexity (Burgess et al., 1993; Turnbull et al., 1995; Wallander, 2000), their affinity for different soil microsites (Bradbury, 1998; Taylor & Bruns, 1999), their tolerance of different abiotic factors (Parke et al., 1983a; Brundrett, 1991), their tendency to colonize fine roots in different regions of the root system (Gibson & Deacon, 1988), and their ability to disperse and colonize from spores (Fox, 1983, 1986a), it is essential to understand the impact of silviculture practices on different ECM fungi. Most previous reviews of the importance of ectomycorrhizas in silviculture have tended to concentrate on inoculation of ECM fungi in nurseries (Mikola, 1973; Trappe, 1977; Marx & Cordell, 1989; Kropp & Langlois, 1990). An exception is the work of Perry and colleagues (Perry & Rose, 1983; Perry et al., 1987). Two recent reviews have discussed the rapid expansion in knowledge of ECM fungal communities brought about by the use of molecular techniques and detailed morphological study of ectomycorrhizas (Dahlberg, 2001; Horton & Bruns, 2001), but these two reviews focused primarily on undisturbed systems. This review will concentrate on ECM fungi in young forest stands regenerating after clearcutting. There are several major changes associated with clearcut logging that are likely to affect ECM fungi. i. Input of carbon to the fungi will decrease. For ECM fungi, their direct supply of carbon via symbiotic roots is gradually removed as the root systems of the harvested trees die. Most ECM fungi seem to rely on supplies of recent photosynthate,

Table 1 Silviculture statistics for selected countries with ectomycorrhizal forests

Country Victoria, Australia

Total forested area (ha)1

Area logged per year (ha)2

% Clearcut

Natural regeneration (ha)

Planted with nursery seedlings (ha)

7 500 000

12 080

19.3

N/A

N/A

Canada Finland

244 571 000 21 934 647

1 025 429 506 480

89.3 23.0

N/A N/A

421 736 N/A

France Sweden USA

15 034 000 27 133 746 225 993 466

100 000 729 400 9 805 0009

64.6 24.5 38.1

59 100 383 0006 7 353 75010

27 800 1 021 0007 2 748 00011

Source of harvesting and regeneration statistics (year of data) Lutze et al. 1999 (1997–98) Statistics Canada3 (1999) Finnish Statistical Yearbook of Forestry4 (1999) Barthod et al. 19995 Swedish NFI8 (2000) USDA Forest Service12

N/A = not readily available. 1Food & Agriculture Organization (FAO). 1999. http://www.fao.org/fo. Accessed May 1999. 2The area logged was subject to different kinds of silviculture including clearcutting, thinning, group selection, and singletree selection (see Lutze et al., 1999 for definitions) depending on the country. 3Natural Resources Canada, Compendium of Canadian Forestry Statistics 2000. http://www.statcan.ca/ start.html. Accessed May 2001. 4Metsätilastollinen vuosikirja. 1999. Ed. Yrö Sevola, Finnish Forest Research Institute, Gummerus Kirjapaino Oy, Jyväskylä. 5Also, Situation des forêts du monde. 2001. FAO. http://www.fao.org/fo and F. Le Tacon (personal communications). 6Naturally regenerated thicket stage forest area, 1997–2001. 7Artificially regenerated thicket stage forest area, 1997–2001. 8Swedish National Forest Inventory (NFI). 2002. http://www-nfi.slu.se. Accessed September 2002. 9Average annual harvest area, 1980 –90. 10Calculated given estimates that 75% of regeneration was natural. 11Average area planted annually from 1986 to 1995. 12A synthesis of information taken from United States Department of Agriculture Forest Service, Forest Inventory and Analysis reports on statewide forest statistics in the United States as provided by W. Brad Smith, National Program Leader, Forest Inventory Association, October 2002.

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at least for fruiting (Last et al., 1979). Litterfall and root turnover, other major sources of carbon, are also reduced following tree removal. ii. The age and species of plants present on site will change. For example, regardless of whether the clearcut is replanted or allowed to regenerate naturally, seedlings and young trees, rather than mature trees, will be the most numerous ECM hosts. Sometimes only a subset of the tree species originally on the site regenerates or is replanted. Changes in the relative abundance of shrubs and herbs can also occur as a result of increases in irradiance. iii. If site preparation is performed, the forest floor is removed or displaced. Because the density of ectomycorrhizas is highest in the organic soil horizons in most forests (Harvey et al., 1986) inoculum levels and habitats for specific ECM fungi will be reduced. iv. The loss of the large overstory trees causes changes in the physical environment of the soil. Fluctuations in soil temperature are greater (Ballard, 2000). Soil moisture can either increase or decrease. Soil porosity can decrease due to vehicle traffic and skidding, and large soil aggregates can become less stable (Perry et al., 1987). v. As a result of the physical and chemical changes described above, populations of soil microflora and fauna will change, as may processes in which these organisms participate, such as decomposition, nitrogen cycling, and production of hydroxymate siderophores (Perry et al., 1984; Forge & Simard, 2000; Prescott et al., 2000; Bradley, 2001). Another potentially important factor is the introduction of exotic ECM fungi on root systems of nursery seedlings. Earlier reviews of this subject often focussed on the negative effects of the above changes on ectomycorrhizas. Common conclusions were: ectomycorrhiza formation is typically reduced following clearcut logging; this is especially likely on sites that are not replanted for many years after logging, have been burned, or have especially demanding environments; and disturbance of the organic soil horizons will reduce the density of ECM fungal inoculum (Harvey et al., 1976; Perry & Rose, 1983; Perry et al., 1987; Perry et al., 1989a; Jurgensen et al., 1997; van Gardingen et al., 1998; Visser & Parkinson, 1999). By contrast, Meyer (1973) concluded that many temperate forests exposed to selective logging or clearcutting are still in a reasonably natural state. He stated ‘in the management of only slightly modified forests, ectomycorrhizae require no more consideration than that given to those in native forests …’ (Meyer, 1973). In this paper, we re-evaluate the evidence for these conclusions. We lay the groundwork for our review by briefly discussing population biology of ECM fungi, including life history strategies and forms of inoculum. Next we thoroughly re-examine the evidence that levels of ectomycorrhiza colonization are reduced by clearcut logging of natural forests, and conclude, instead, that the major impact of conventional forestry practices is on the composition of the ECM fungal

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community. The central core of the paper examines the factors that may underpin for these changes, including inoculum availability, soil environmental factors, and host and nonhost plant communities. We finish by speculating upon the implications of changes for young trees in the regenerating stand. Most of the studies on ectomycorrhizal fungal communities following clearcut logging are from coniferous forests in Canada, the United States and northern Europe and thus this review will be most relevant to these temperate and boreal forests. When available, we have included comparable studies from ectomycorrhizal tropical trees and eucalypt forests. Generally, the results from these studies are similar to those from northern forests, but generalizations should be applied to these forests with caution because they have evolved under different conditions. In this review, we focus our discussion on forests containing native tree species. Our conclusions may not apply to plantations, especially those comprised of nonnative trees.

II. Population biology and inoculum potential of ectomycorrhizal fungi Ectomycorrhizal fungi have different life history strategies. These differences were described first for fungi undergoing primary succession as they colonized birch planted in an agricultural field (Deacon & Fleming, 1992). Some fungi, referred to as ‘early stage fungi’ could fruit in association with very young trees, could colonize seedlings in nonsterile soil from spores or fragmented mycelia and could persist under these conditions, and required low amounts of simple carbohydrates for growth in axenic culture. ‘Late-stage’ fungi fruited slightly later and lacked the other characteristics of early stage fungi. Under field conditions, late-stage fungi were able to compete effectively with early stage fungi for colonization of new roots only if they were already associated with other living roots (Fleming, 1983, 1984). The terms ‘early stage’ and ‘late stage’ have been criticized as confusing and inappropriate (Newton, 1992; Smith & Read, 1997); nevertheless, the differences in life history strategies that they represent will influence the ability of ECM fungi to disperse and re-establish after logging. There are three major sources of ECM fungal inoculum in forests: spores, hyphae and sclerotia (Brundrett, 1991). Spore inoculum includes meiospores, such as ascospores and basidiospores, and asexual spores, such as chlamydospores. Diffuse hyphae or rhizomorphs can extend from living mycorrhizas to colonize new roots (Fleming, 1984; Simard et al., 1997c). Hyphae in the mantle of old, dead or dying mycorrhizas can also act as inoculum (Bâ et al., 1991). Sclerotia and sclerotialike bodies are vegetative balls of hyphae formed by a few species of ECM fungi, including Cenococcum geophilum, Hebeloma sacchariolens, Paxillus involutus, and Phlebopus sudanensis (Fox, 1986c; Thoen & Ducousso, 1989; Ingleby et al., 1990). During afforestation of land that had previously supported

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only nonECM plants, ECM fungi undergo primary succession. Under these conditions, spores are the most important sources of initial inoculum (Deacon & Fleming, 1992) because other inocula, such as hyphae and sclerotia, disappear in the long term absence of ECM plants (Fox, 1986b). Wind is generally considered to be the most important vector for dispersing spores of epigeous sporocarps, while small mammals are important vectors for dispersing spores of hypogeous sporocarps (Kotter & Farentinos, 1984; Miller et al., 1994; Reddell et al., 1997). When trees are harvested from existing stands, and then those sites replanted with seedlings produced in nurseries or allowed to naturally regenerate from seed fall, ECM fungi will undergo secondary succession. Under these situations, the full range of inoculum types would be present. This review will deal only with silvicultural systems that result in secondary succession of ECM fungi. Molecular approaches have begun to provide information on how ECM fungi disperse and establish during secondary succession in natural ecosystems. Based on data derived from above-ground sporocarp material, populations of some ECM fungi are thought to comprise multiple genotypes within a relatively small area (Gryta et al., 1997; Fiore-Donno & Martin, 2001; Redecker et al., 2001). Others appear to be dominated by limited numbers of widely dispersed genotypes that are regarded as large genets (Bonello et al., 1998; Sawyer et al., 1999) while still others may be a mixture of large and small genets (Anderson et al., 2001). The presence of large genets is regarded as indicative of colonization via vegetative growth through soil, whereas dense populations of small genets suggest colonization via meiospore dispersal (Dahlberg & Stenlid, 1990, 1995). Although ECM fungi that produce large genets may thus be expected to be the most important taxa in mature forests (Redecker et al., 2001), this does not appear to be true in all cases. Several studies suggest the presence of multiple small genets of ECM fungi (including Amanita, Laccaria, Lactarius, Russula and Suillus species) in undisturbed mature forest stands (Gherbi et al., 1999; Zhou et al., 1999; Fiore-Donno & Martin, 2001; Redecker et al., 2001). It is thus difficult at present to generalize regarding population structure, even for taxa that are regarded as typical ‘late stage’ or ‘early stage’ fungi. Disturbance can strongly influence patterns of genet distribution and, for some fungi such as Suillus bovinus, genet size can vary according to age of stand (Dahlberg & Stenlid, 1990, 1995). Although the influence of clearcutting on below-ground mycelial genets of ECM fungi has not been investigated to date, clearcutting over relatively large areas (40–100 ha) would be expected to disrupt established genets and, if limited viable vegetative inoculum persists at the site at planting, favour establishment of new mycelia via basidiospores. Bruns and colleagues have used molecular techniques to study ECM fungi on roots of Pinus muricata (bishop pine) before and after a stand-destroying wildfire in California and their results can be used to infer the relative importance spore

vs hyphal inoculum following this type of natural disturbance. Although disturbance from fire differs from that caused by clearcutting, these studies may still be instructive because many ECM forests have evolved with frequent disturbance from fire. Taylor & Bruns (1999) found that effective inoculum of some fungi persisted in the soil even when ectomycorrhizas of those fungi were not present. They referred to these inocula as ‘resistant propagules’, and concluded that it was most likely from spores because roots had been sieved out of the soil and none of the fungi at these sites formed sclerotia. Spatial analysis showed that colonization resulted from randomly distributed, point sources of inoculum (Grogan et al., 2000), a further indication that spores, rather than mycelia were the likely source. In other ecosystems, sclerotia are abundant, increasingly so after fire (Miller et al., 1994; Torres & Honrubia, 1997), so they too could act as resistant propagules during secondary succession. These resistant propagules do not compete effectively with other forms of inocula in forests (Taylor & Bruns, 1999). Ectomycorrhizal hyphae attached to living roots are abundant in forests and may be the major form of inoculum in these settings (Deacon & Fleming, 1992; Read, 1992; Amaranthus & Perry, 1994). As a final caveat, the presence of inoculum of a particular ECM fungus is not enough to ensure colonization by that fungus (Fox, 1986a; Gibson et al., 1988). For example, Rhizopogon spp., formed mycorrhizas in a glasshouse bioassay and in a field bioassay at a shrub site where no other ECM hosts were present, implying that they had active inoculum present in the soil (Horton et al., 1998; Baar et al., 1999). Nevertheless, they did not always form mycorrhizas in the forest. These studies confirm that ECM fungi vary in dispersal characteristics and colonization strategies in ways that are relevant to stands regenerating after logging.

III. Ectomycorrhiza development on seedlings regenerating after clearcut logging (1) Are levels of colonization of seedlings lower in regenerating clearcuts than in forests? We know that total inoculum levels in soil can influence the extent of colonization because when forest soils are diluted with sterile soil in pots, levels of colonization decrease (Baar et al., 1999; Taylor & Bruns, 1999). What evidence do we have that ECM fungal inoculum in clearcuts is lowered to the extent that colonization of roots is reduced (Fig. 1)? Three types of experiments have been performed to address this question: glasshouse bioassays, where soils are removed from clearcuts and adjacent forests and seedlings are grown in these soils under controlled conditions; field bioassays, where seedlings have been planted (nonmycorrhizal at planting) or naturally regenerated in clearcuts and adjacent forests; and soil transfer studies, where soils from clearcuts and forests have been reciprocally transferred. Glasshouse bioassays have

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Fig. 1 A schematic diagram illustrating the two major groups of factors likely to influence the species composition of the ectomycorrhizal fungi communities in regenerating stands after clearcut logging. Interactions amongst factors are not shown.

the disadvantage that collection of soil disrupts the connections between ECM hyphae and living roots or between root tips and their supply of photosynthate. Because living roots are more abundant in forest soils than clearcut soils, this type of assay will underestimate differences in inoculum potential. Field bioassays have the disadvantage that seedlings planted in forests are exposed to much lower irradiance than seedlings growing in clearcuts and the subsequent changes in seedling growth or physiology could affect colonization independently of inoculum potential (Brundrett & Abbott, 1994; Visser, 1995; Zhou & Sharik, 1997). Soil transfer studies can account for differences in aboveground environment, but they still eliminate connections between hyphae and living roots. In any of these studies, size differences amongst seedlings can make differences in colonization difficult to interpret (Perry & Rose, 1983). In Table 2, we re-examine the evidence that clearcutting, in the absence of broadcast burning, has an effect on colonization of seedlings by ECM fungi. We have re-calculated data so that colonization is expressed as a percentage of total root tips. In most of the glasshouse bioassays listed in Table 2, the data were originally presented as numbers of ectomycorrhizas per seedling. This may be the most appropriate variable for expressing colonization when the goal is to infer survival and

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growth of the seedlings because two seedlings with the same number of ECM root tips might be expected to have similar nutrient uptake capacities regardless of the number of nonmycorrhizal roots present. In the present review, however, we are interested in ECM fungal inoculum potential. For that purpose we feel that the percentage of root tips colonized is a better index because it reflects the likelihood that a root will encounter effective inoculum. When data from glasshouse bioassays are expressed in this way, only two of the six studies detected significant reductions in colonization for seedlings planted in clearcuts with intact forest floors (no burning or scalping) compared with those planted in forests (Table 2). In one of these two studies, the authors concluded that inoculum was not limiting (Pilz & Perry, 1984). They reached this conclusion because a glasshouse bioassay found that dilution of the soil with pasteurized soil did not result in a reduction in the number of ectomycorrhizas per seedling. Instead, they suggested that some biological characteristics of clearcut soils reduced root growth (Perry et al., 1982). Evidence from field bioassays for differences in inoculum potential between forests and clearcuts with reasonably undisturbed soils is equivocal. The percentage of roots colonized was higher or lower in clearcuts than in adjacent forests,

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Table 2 Colonization, diversity of ectomycorrhizal fungi and change in fungal species composition on seedlings planted on clearcuts

Time since harvest (age of % of root tips clearcut) colonized

Type of experiment

Nature of treatment

Pinus contorta, Seeds Pseudotsuga menziesii, Picea engelmannii

Glasshouse bioassay

P. menziesii, Tsuga heterophylla

Seeds

Glasshouse bioassay

Mixed soils 15 years w/o litter from unburned clearcut or forest Sieved soils 1 year w/o litter and humus

P. menziesii

Seeds

Glasshouse bioassay

P. menziesii, Pinus ponderosa

Seeds

Glasshouse bioassay

P. menziesii, P. ponderosa

Seeds

Glasshouse bioassay

P. menziesii

Seeds

Glasshouse bioassay

P. menziesii

Nonmycorrhizal Soil transfer study Unburned clearcuts 1–0 when planted or forests

Pinus sylvestris

Nursery (many Field bioassay were mycorrhizal)

Shorea leprosula, Hopea nervosa

Nonmycorrhizal, 2-month-old at planting

Field bioassay

Quercus rubra

Seeds

Field bioassay

Tree species

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Sieved mineral soil from forest or burned clearcut, with or without litter added Sieved mineral soil from forest or clearcut Sieved mineral soils from unburned clearcuts and forests Unburned clearcuts or forests

Scarified clearcuts vs manually screefed forests Undisturbed forest vs logged area with a few large trees remaining Clearcuts and forests with variable overstory

4 years

Slight increase in mean, but apparently NSD (stats not shown) Site variability greater than treatment effect NSD

1–1.5 years

NSD

1–22 years

Decreased

2–3 years; 3–10 m into forest; > 20 m into clearcut 2–3 years; 3–10 m into forest; > 20 m into clearcut

NSD

Number or diversity of ECM morphotypes† or genotypes* per seedling

Perry et al. (1982)

Yes

NSD

1 year

NSD year 1; decrease year 2 highest in partial cuts

Schoenberger & Perry (1982) Parke et al. (1983b)

Parke et al. (1983b) Not quantified, but differences not obvious

Parke et al. (1984) Pilz & Perry (1984)

Decreased Note nontransferred soil from all sites lower still

1 or 2 years

Change in relative abundance of specific fungi Source

Yes

Pilz & Perry (1984)

†Increased

Yes

Dahlberg & Stenström (1991)

†Variability among sites greater than treatment effect

Yes

Lee et al. (1996)

Zhou et al. (1997)

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Status of seedlings at planting

Yes

Mah et al. (2001) Hagerman et al. (2001) Yes

Yes

†NSD at 16 m or greater into clearcut; increased 2–3 m away from forest †Decreased *no effect †Decreased P. menziesii

Field bioassay Picea hybrid

Picea engelmannii

T. heterophylla

Naturally regenerating Naturally regenerating

Field bioassay

Unburned clearcuts and forests Unburned clearcuts and forests

2 years

NSD at 16 m or greater into clearcut; increased 2–3 m from forest

Yes †Decreased

Ingleby et al. (1998) Kranabetter & Wylie (1998) Hagerman et al. (1999b) Yes †Increased Increased

Intact forest floors of clearcut and forest Intact forest floors of clearcut and forest Undisturbed forest 2 and 3 years floor of clearcuts or forests (≥ 40 m from clearcut) Field bioassay Field bioassay Field bioassay Naturally regenerating Naturally regenerating Nonmycorrhizal, 8-week-old when planted Shorea parvifolia

Tree species

Table 2 Continued.

Status of seedlings at planting

Type of experiment

Nature of treatment

Time since harvest (age of % of root tips clearcut) colonized

Number or diversity of ECM morphotypes† or genotypes* per seedling

Change in relative abundance of specific fungi Source

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depending on the forest type, time since planting, and distance from the forest edge (Table 2). The single soil transfer study (Pilz & Perry, 1984) found that seedlings planted in clearcut soil, regardless of whether it was transplanted within the clearcut or to a forest site, had lower percent colonization. This was because these seedlings had larger root systems, with greater numbers of nonmycorrhizal roots but the same number of mycorrhizal roots, than seedlings planted in transplanted forest soil. Overall, there seems to be no clear evidence that the inoculum potential of ECM fungi is reduced to the point where the percentage of roots colonized is generally decreased. Several authors have recommended that clearcut sites that are to be replanted with conifers should be planted as soon as possible after logging, ideally within 2 yr (Harvey et al., 1980a; Perry et al., 1987; Swift et al., 2000). This recommendation is based primarily on the rapid loss of active ECM roots between 1 and 2 yr after logging on these sites (Harvey et al., 1980a; Hagerman et al., 1999a). Furthermore, clearcuts that regenerate primarily to grasses or nonECM shrubs may have changes in the soil microflora and soil chemistry that make conifer regeneration increasingly more difficult with time (Perry et al., 1989a; Jones et al., 1997). Perry et al. (1987) discussed two major factors that would influence the impact of clearcut age on colonization by ECM fungi: the rate of loss of ECM fungal inoculum through death of ectomycorrhizas, vegetative hyphae and spores, vs the rate of gain through spore input; and the rate of regeneration of ECM hosts on the clearcut. Although most clearcuts classified as ‘difficult to regenerate’ to conifers are older than two-years old (Parke et al., 1984; Amaranthus & Perry, 1987; Jones et al., 1996), this may be an artefact. Conifers might be unable to grow on some sites even immediately after logging, due to steep slopes, thin soils and low rainfall but the sites may be classified as ‘difficult to regenerate’ only after several replanting attempts have failed. By this point some years will inevitably have passed. The only one of the six glasshouse bioassays that showed clear evidence of reduced ECM fungal inoculum was conducted on clearcuts with an average age of 9 yr (Parke et al., 1984). This study is often cited as evidence that older clearcuts are particularly likely to have low inoculum levels (Perry et al., 1987) even though Parke et al. (1984) found no correlation between site age and colonization levels. It is also important to note that clearcuts were selected for this study on the basis that they were difficult to regenerate, and thus their reduced inoculum potential could have correlated with some other variable. Hagerman et al. (1999b) found a slight reduction in both percent colonization and richness of ectomycorrhizas for seedlings planted 3 yr after logging when compared with those planted 2 yr after logging, but this could have been due to year-to-year variation caused by some other factor. Interestingly, Perry et al. (1982) found no reduction in the percentage of roots colonized in glasshouse bioassay seedlings planted in soil from a 15-yr-old-clearcut. Therefore, we

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conclude that a reduction in inoculum potential with age of clearcut has not been established empirically. (2) Changes in fungal species composition following clearcut logging Although there is no conclusive evidence that inoculum levels in clearcuts compromise the percentage of roots colonized, it is apparent from almost every study, especially field bioassays, that different fungi colonize seedlings growing in clearcuts and seedlings growing in forests (Table 2). Interestingly, the diversity of ECM fungi or morphotypes on the root systems of young conifers is not affected in a consistent manner. The diversity can be higher, lower, or unchanged on seedlings growing in clearcuts compared to seedlings growing in nearby forests. We can divide the possible reasons for the change in species composition of the ECM fungal community into two main groups: one that relates to inoculum levels and types, and one that relates to the differences in environment between the two sites (Fig. 1). As discussed in Section II, fungi differ in their ability to colonize effectively from different types of inoculum; therefore, any change in the level or type of inoculum after clearcutting might cause a change in the ECM fungal community. On the other hand, changes in the physical, chemical or biological characteristics of the soil, or in the age or species of ECM host on a site might select for a different community of fungi. Distinguishing between these two possibilities, although difficult, is important. If inoculum of some fungi is lost during tree harvest or site preparation, the pool of ECM fungi available to colonize roots would be reduced. This might warrant adjustments to silvicultural practices. If, on the other hand, the ECM fungi present on clearcuts are ones that are better adapted to absorbing nutrients under these conditions, then forest managers need not be concerned about the change in ECM fungal community. The major goal of Section IV of this paper is to use evidence from the literature to distinguish between these two possibilities. (3) Comparison with natural disturbances Before evaluating the reasons for the changes in fungal communities, it is useful to think about how clearcutting compares with the types of natural disturbances under which ECM forests evolved. Fire is the major natural disturbance under which boreal forests, dry pine forests, and eucalypt forests evolved. Fire may act at a similar scale to clearcut logging, but even so-called ‘stand-destroying’ fires rarely kill all tree stems. In boreal forests, single trees or patches of trees are left alive so that the effect is heterogeneous ( Johnson, 1992). Eucalypt trees are highly resistant to fire and can often regenerate from epicormic shoots or from lignotubers. This means that some ECM roots will remain alive to act as sources of inoculum, even after a major forest fire. Silviculture systems

such as seed tree or green tree retention, where single stems or groups of trees are left after logging may mimic the distribution of trees after fire better than clearcutting, although individual trees of nontarget species may also be left behind in clearcuts. Fire affects the soil differently from clearcut logging. Fire can cause the liberation of nutrients from ash, burning of soil organic matter and increases in soil pH (Mikola et al., 1964; Pietikäinen & Fritze, 1995; Ballard, 2000). Thus, disturbance from fire has some similarities, but some important differences from disturbance by clearcut logging. We are aware of only one study that has compared directly the effects of fire and clearcut logging on ECM fungal communities. In Picea glauca (white spruce)-dominated boreal forest stands, the number of ectomycorrhiza morphotypes per stand was reduced to a similar extent by clearcut logging and by fire (Lazaruk, 2001). Furthermore, the fungal communities in soils from clearcut and burned stands clustered together during detrended correspondance analysis, when compared with communities from unlogged forests or forests cut in long strips. If ECM fungal communities respond to clearcut logging in the same way as they respond to fire, they may show a similar succession as forests grow again on these sites. There have not yet been any studies that follow the succession of ECM fungi after clearcut logging, as there has been for wildfire (Visser, 1995). In wet temperate forests and ECM forests of nonsclerophylous broad-leaved trees, windthrow and insect attack are generally more frequent causes of tree death than fire. Clearcut logging removes trees in a very different pattern from these kinds of disturbances. These disturbances are mimiced better by various kinds of partial cutting than by clearcut logging. In one of the first studies of the effect of partial cutting on ectomycorrhizal fungal communities, Lazaruk (2001) found that the richness and species composition of ectomycorrhiza morphotypes in partially cut stands was intermediate between clearcut and control stands. The comparison between the effects of natural and human-induced disturbance on ECM fungal communities needs to be studied much more extensively in order for us to understand whether ECM fungal communities are adapted to disturbances such as clearcut logging.

IV. Which is the most important factor driving changes in the ECM fungal community after clearcut logging: inoculum loss or changes in the below-ground environment? (1) Evidence that inoculum loss drives changes in the ectomycorrhizal fungal community The relative abundance of the different inoculum sources changes after clearcutting. During clearcut logging the stems of most trees are removed and, although they may not be the only hosts for ECM fungi on the site, they will undoubtedly

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be the dominant ones. Numbers of apparently active ectomycorrhizas remain high for at least 1 yr after logging, especially if the logging is done in the late autumn or winter. Sometime between the first and second year after harvest root systems begin to fragment and show signs of decay and the number of ectomycorrhizas per unit volume of soil decreases markedly (Harvey et al., 1980a; Hagerman et al., 1999a). This is true even in stands of Populus tremuloides (trembling aspen), which can regenerate from roots (Visser et al., 1998). After this loss of fine roots from the previous stand, the density of live ectomycorrhizas is highest in the periphery of a clearcut, within a few metres of the surrounding forest (Hagerman et al., 1999a). Parsons et al. (1994) found live roots of Pinus contorta (lodgepole pine) extending up to 15 m into clearcuts, but Harvey et al. (1980a) found no live ectomycorrhizas 5 m or greater away from a forest of P. menziesii and Larix occidentalis (western larch). Thus two major types of inoculum change dramatically after clearcut logging: extramatrical hyphae extending from living roots decrease in abundance because fewer living roots are present, whereas the number of dying mycorrhizas associated with fragmenting root systems increases immediately after logging. These will then subsequently disappear with time. Next we consider the evidence that these two types of inoculum, as well as sclerotia and spores, act as inoculum for seedlings in regenerating stands (Fig. 1). (a) Importance of ectomycorrhizal hyphae associated with living roots There are two types of studies that indicate that loss of ECM hyphae with connections to living roots can influence the species of fungi that colonize seedlings: root isolation experiments and experiments where seedlings are planted within or beyond the rooting zone of mature ECM trees. In the first type of experiment seedlings are planted in plantations or mature forests. The root systems of some of the seedlings are isolated from those of mature trees by coring or trenching (Fleming, 1983, 1984; Alexander et al., 1992; Simard et al., 1997c; Dickie et al., 2002; Onguene & Kuyper, 2002). The number of seedlings and/or the number of fungi forming ectomycorrhizas increased when the roots of seedlings were in contact with the roots of trees in each of these studies. Although differences in soil environment associated with coring or trenching may have contributed to changes in colonization, these results suggest that some ECM fungi colonize most effectively by hyphal extension from a living root system. This is especially likely in situations where mycorrhizas form before seedling leaves become net exporters of carbon (Alexander et al., 1992). If living mycorrhizas and their associated hyphae form an important source of inoculum for some fungi, we would also expect to see more types of ectomycorrhizas or a change in the fungal species composition on seedlings growing in the rooting zone of mature trees. Several studies have found this to be the case for naturally regenerating seedlings and for field

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bioassay seedlings than were nonmycorrhizal at outplanting. Three years after clearcut logging, Hagerman et al. (1999b) found a 65% reduction in colonization and a 55% reduction in the number of ECM morphotypes per Picea engelmannii (Engelmann spruce) seedling planted 16 m or greater into clearcuts compared with seedlings planted 2–3 m away from the forest edge. E.T. Cline (unpublished) found very similar results on P. menziesii seedlings. The number of ECM morphotypes per Tsuga heterophylla (western hemlock) seedling was 50% higher for naturally regenerating seedlings growing in the forest or at the forest/clearcut boundary than for seedlings growing more than 5 m from the forest (Kranabetter & Wylie, 1998). Interestingly, the pattern of lower numbers of types of ectomycorrhizas with distance into the clearcut was much less apparent (Durall et al., 1999) or not present at all (Jones et al., 2002) on seedlings previously colonized by ECM fungi in the nursery. This may be because nursery fungi suppress initial colonization by native fungi (see Section IV.2.c below) and thus, would not reflect a difference in inoculum. Further evidence for the importance of inoculum from living roots comes from studies of seedlings growing at different distances from so-called ‘refuge plants’. This term is used for plant species that are left behind during clearcut logging, but which associate with ECM fungi. This includes tree species that are not always of commercial interest, as well as shrubs that form ectomycorrhizas or arbutoid mycorrhizas (arbutoid mycorrhizas are formed by the same fungi as ectomycorrhizas (Horton et al., 1999; Hagerman et al., 2001)). In an interesting study by Kranabetter (1999) naturally regenerating B. papyrifera seedlings growing in clearcuts within the rooting zone of mature birch trees formed 38% more types of ectomycorrhiza than seedlings growing outside the rooting zone (25–50 m away). The reduction in morphotype richness was less in forests, suggesting that ectomycorrhizas of other trees species could also act as inoculum sources. Betula papyrifera seedlings growing in clearcuts beyond the rooting zone of mature trees also formed a higher proportion of mycorrhizas with a few dominant fungi and had more similar communities than was the case for seedlings growing in rooting zones of mature trees. This suggests that effective inocula for some fungi were present only in rooting zones, presumably associated with live ectomycorrhizas. Only a subset of fungi had effective inoculum in the rest of the clearcut. Other studies in temperate and tropical forests have found that seedlings are colonized more rapidly and /or by a greater diversity of ECM fungi when they are planted in close contact with congeneric adult trees, but this is not observed with all tree species (Newbery et al., 2000; Dickie et al., 2002). Differences other than type and level of inoculum will exist in soils under canopies of trees and these could be responsible for the differences in colonization. Biological and chemical differences, independent of the presence of live roots (Borchers & Perry, 1990) could be generated by litterfall and stemflow, amongst other factors. It is possible that increased foraging by

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small mammals, which may contain ECM fungal spores in their feces, occurs more frequently at the edges than in the middle of clearcuts, but this is unlikely at the sites used by Hagerman et al. (1999b). Red-backed voles are the main mycophagous mammals at these sites, and they avoid clear cuts and the forest immediately adjacent to them (Huggard, 2000). Therefore the studies described above provide evidence that the loss of living mycorrhizas on clearcuts may be one reason that regenerated stands are colonized by different ECM fungi than were present in the previous forest. (b) Importance of sclerotia and dying mycorrhizas: does the removal of forest floor through burning or mechanical site preparation influence colonization? Unless there is extensive cover by refuge plants, most ectomycorrhizas on recent clearcuts will be fragmented root tips of dying root systems. In this section we review the conflicting evidence for importance of these dying mycorrhizas as an inoculum source. Because the supply of carbon to these roots has been reduced by removal of the stem, it is unlikely that there will be vigourous growth of hyphae from these mycorrhizas. Nevertheless, meticulous observations by Bâ et al. (1991) showed that sclerotia, rhizomorphs and isolated ectomycorrhizal root tips of Scleroderma dictyosporum and Scleroderma verrucosum could all act as inocula under laboratory conditions. Sclerotia are infective even after burial in soil for several months (Fox, 1986b,c). When Betula papyrifera (paper birch) and Pseudotsuga menziesii (Douglas-fir) were grown in pots containing soil from a clearcut, they formed the same types of ectomycorrhizas as they did when they were planted directly in the clearcut (Jones et al., 1997). Because mycorrhizas were cut off from the rest of the root system when soil was collected for the pot bioassays, this implies that propagules such as spores, sclerotia or dying ectomycorrhizas were the predominant inoculum in this case. Sclerotia and ECM root tips usually reach their highest densities in the organic soil horizons (forest floor or O horizon and A horizon), although this may not be the case in all forests, such as those with very thin forest floors or those on dry sites (McMinn, 1963; Meyer, 1973; Harvey et al., 1976, 1978, 1979, 1986; Visser, 1995; Jurgensen et al., 1997; Hashimoto & Hyakumachi, 1998). Decayed wood seems to be an especially important source of ECM fungal inoculum (Harvey et al., 1978; Kropp, 1982; Väre, 1989a). Because organic horizons have such high densities of inoculum (Harvey et al., 1986; Vogt et al., 1991; Brundrett & Abbott, 1995), it is often recommended that disturbance to the forest floor be minimized during harvesting (Harvey et al., 1980b; Perry & Rose, 1983; Jones et al., 1996; Visser & Parkinson, 1999). Nevertheless, it is not unusual for the litter, fermentation layer and humus, as well as the A horizon, to be removed or displaced at planting sites in northern or high elevation forests. This reduces competition from herbaceous plants and increases maximum soil temperatures during the growing

season (Väre, 1989b; Jurgensen et al., 1997; Ballard, 2000). Mineral soil can be exposed by scraping off the organic layers immediately around the planting hole with a shovel or small mechanical equipment (screefing), by inverting the surface horizons so that mineral soil is on top of a mound or ridge of soil (mounding or ploughing), or by burning the logging debris and upper soil layers after logging and prior to planting (broadcast burning). In Canada in 2000, 240 000 ha were mechanically treated and 12 000 ha burned after harvesting (Canadian Council of Forest Ministers, 2001). By reviewing the effects of these types of mechanical site preparation or broadcast burning on colonization, we can make some inferences about the importance of dying ectomycorrhizas and sclerotia in the forest floor as inoculum sources on recent clearcuts. Broadcast burns vary in intensity, depending on the temperature, moisture level, and thickness of the forest floor. Very hot fires can remove all the organic soil horizons, whereas cooler fires have less impact (Mikola et al., 1964; Harvey et al., 1980b; Grogan et al., 2000). After broadcast burning soils typically have substantially reduced densities or biomass of residual ectomycorrhizas compared to unburned areas (Harvey et al., 1980b; Stendell et al., 1999; Visser & Parkinson, 1999). Chen & Cairney (2002), however, found that while ITS sequences of ECM fungi (taken to reflect total propagule availability) were considerably reduced in the top 15 cm of soil profiles at two eucalypt forest sites following a prescribed burn, this was not the case at a third site. Fire effects may thus be site specific. Since burning generally eliminates so much ectomycorrhiza biomass, it is not surprising that the inoculum potential of burned sites can be lower than unburned sites (Wright & Tarrant, 1958). In a glasshouse bioassay, Parke et al. (1984) found significantly lower colonization rates of P. menziesii or Pinus ponderosa (ponderosa pine) grown in soils from burned than unburned clearcuts. This same kind of reduction in inoculum potential also occurred after 4 yr of annual burning of unlogged eucalypt forests (Brundrett et al., 1996). A year after a broadcast burn hot enough to eliminate the humus, the percentage of Pinus sylvestris (Scots pine) roots colonized was lower than where the fire had not burned the humus (treatment plots not replicated; Mikola et al., 1964). Thus, there is strong evidence that high intensity fires can reduce ectomycorrhiza formation. However, even fires of high intensity do not always reduce percent ECM colonization (Parke et al., 1983a; Herr et al., 1994; Launonen et al., 1999). This may be because some fungi can be triggered to produce hypogeous fruitbodies or sclerotia (e.g. Cenococcum spp.) by fires (Miller et al., 1994; Johnson, 1995). Furthermore, there will always be some ectomycorrhizas in the deeper mineral soil and these will not be exposed to soil temperatures high enough to kill them (Whelan, 1995; Baar et al., 1999; Stendell et al., 1999; Visser & Parkinson, 1999). Poor colonization rates or changes in the ECM fungal community after fire do not appear to

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be due directly to the presence of ash (Grogan et al., 2000; Mahmood et al., 2002) or to the loss of topsoil by erosion (Amaranthus & Trappe, 1993). These results are consistent with a role for sclerotia and dying mycorrhizas in the forest floor and upper soil horizons as inoculum sources, but there are other possible explanations. Fires also cause increases in soil pH and soil temperature, and changes in nutrient availability and soil microbial community (Mikola et al., 1964; Pietikäinen & Fritze, 1995; Ballard, 2000). These changes may be just as important as destruction of inoculum in reducing colonization (Perry & Rose, 1983). Results from experiments on mechanical site preparation do not support the importance as inoculum of sclerotia and dying mycorrhizas in the forest floor. For example, only 4% of the variation in percent colonization of P. sylvestris and P. contorta planted on a ploughed site was explained by whether they were planted in microsites with or without humus (Dahlberg, 1990). Jones et al. (1996) found only a transient (year 2 only) reduction in ectomycorrhiza richness and diversity per P. contorta seedling planted on mechanically screefed microsites (1.5 m × 1.5 m) compared to planting sites with chemical suppression of competition. In an experiment combining three levels of organic matter removal and three levels of soil compaction (one plot only per treatment), Amaranthus et al. (1996) found no effect of forest floor displacement on percent colonization of container-grown P. menziesii or P. monticola seedlings. Removal of litter and humus layers in the Netherlands appeared to increase, rather than reduce, the abundance of ECM fungi on roots (Baar, 1996), regardless of whether or not P. sylvestris seedlings had been previously inoculated with ECM fungi (Baar & de Vries, 1995). Although percent colonization was not presented, the number of ECM root tips of P. monticola and P. menziesii was higher in scalped treatments (mechanical removal of upper organic soil horizons over the entire plot) than in mounded or control treatments even though root weights did not increase with scalping (Harvey et al., 1996). Thus, experiments performed to date suggest that colonization by ECM fungi is much more likely to be reduced following broadcast burning than after mechanical removal of forest floor, a conclusion also reached by Visser & Parkinson (1999). This may be because fire causes more intensive changes to the soil environment, or because mechanical site preparation more often causes displacement of inoculum rather than outright removal. Because fire and mechanical site preparation have inconsistent effects on colonization, it is difficult to conclude about the relative importance of sclerotia and dying mycorrhizas located in the upper organic soil horizons. The lack of a major effect on colonization when the forest floor is removed or displaced mechanically may mean that these inocula are not quantitatively important in clearcuts. By contrast, it could mean that sufficient amounts of these inocula remain deeper in mineral soils (Hashimoto & Hyakumachi, 1998). Certainly roots growing in mineral soils are usually well

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colonized, even at sites where ectomycorrhizas are most dense in organic components of the same soils (Harvey et al., 1976, 1996). Parke et al. (1983b) found no increase in ECM colonization when forest litter and humus were added to P. menziesii growing in mineral soils in a glasshouse bioassay, regardless of whether the mineral soil was from a clearcut or forest. Thus, our major conclusion is that inoculum levels in mineral soils from many coniferous forests or clearcuts do not limit colonization. As with clearcutting, the major impact of forest floor disturbance is likely to be on the composition of the ECM fungal community. The species of ECM fungi on roots is often altered after severe wildfire or moderate broadcast burning (Visser, 1995; Horton & Bruns, 1998; Horton et al., 1998; Launonen et al., 1999; Taylor & Bruns, 1999; Grogan et al., 2000; Mah et al., 2001). This may be because the propagules of different ECM fungi differ in their abilities to withstand very high temperatures (Gibson et al., 1988) or because they are differentially distributed in the horizons most likely to be destroyed by fire (Stendell et al., 1999). It is interesting that E-strain and MRA (Mycelium radicis atrovirens) mycorrhizas seem to comprise a dominant component of the community after either wildfire (Torres & Honrubia, 1997; Horton et al., 1998; Grogan et al., 2000; Mah et al., 2001) or clearcutting (Table 3). Although species composition changes, a reduction in ectomycorrhiza diversity has not been detected in seedlings planted on sites with the forest floor removed (Amaranthus et al., 1996; Baar, 1996; Mah et al., 2001), and low intensity fires may not have an effect on fungal community composition that can be distinguished against the background of high spatial variability (Jonsson et al., 1999a). This change in species composition could be due to differential loss of inoculum of different fungi, but could just as likely be due to the change in habitats available after the forest floor has been removed. Evidence that changes in the environment drive species shifts in the ECM fungal community is discussed below in Section IV.2. (c) Spores We know little about how long ECM fungal spores persist in soil (Fox, 1983, 1986b,c; Miller et al., 1994) and how spore banks change after clearcut logging. Nevertheless, we can deduce that some fungi colonize seedlings in regenerating forest stands from spores. In the interior of British Columbia, E-strain, MRA and Thelephora mycorrhizas increase in relative abundance on seedlings planted beyond the root zone of living trees (Table 3, Durall et al., 1999; Jones et al., 2002). These mycorrhizas are also very common on seedlings growing in sterilized nursery or glasshouse soils (Danielson & Visser, 1990), indicating that the fungi that form them disperse very effectively from spores. Pioneer fungi such as Geastrum, Suillus, and Scleroderma formed the most common ectomycorrhizas on naturally regenerating Shorea parvifolia growing in clearcuts (Ingleby et al., 1998). Spatial and genetic analysis indicated that P. muricata seedlings germinating after a wildfire that consumed the surface

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Table 3 Percentage change in percent colonization of seedlings planted or growing (see Table 2 for details) in clearcuts vs forests, or in the rooting zone of mature trees vs no contact with roots of mature trees Relative abundance of morphotype without contact (clearcut or severing) vs with contact (forest or rooting zone) with roots of mature trees Comparison

Cenococcum

E-strain

MRA

scarified clearcuts vs manually screefed forests

50% increase*

intact forest floors of clearcut vs dipterocarp forest

100% decrease

intact forest floors of forest vs 16 m or greater into clearcut

5.6-fold increase year 2;* 57% decrease year 3 NSD

250% increase year 2; 205-fold increase year 3*

NSD year 2; 7.4-fold increase year 3*

intact forest floor 15 m or greater into forest vs in forest or at forest edge

no difference

no difference

87% increase

28-fold increase

100% decrease

Kranabetter and Wylie (1998)

unburned clearcuts and forests

NSD

99% increase NSD

160% increase NSD

320% increase*

91% decrease

Mah et al. (2001)

intact forest floor of rooting zone (2–3 m) vs 16 m or greater into clearcut

NSD 2 or 3 years after logging

44% decrease year 2; 44% decrease year 3

NSD year 2; 130% increase year 3

rooting zone vs beyond rooting zone, both in clearcuts

no difference†

350% increase

130% increase

340% increase

trenched and untrenched plots in forest

40% increase NSD

111% increase*

NSD

475% increase*

seedling transfer from forest to clearcut

65% reduction

28% increase

no apparent difference

increase from 0% to 16.4% of ECM

Thelephora

Piloderma spp.

Source

57% decrease*

Dahlberg & Stenström (1991) Ingleby et al. (1998) Hagerman et al. (1999b)

Hagerman et al. (1999b)

100% decrease

Kranabetter et al. (1999)

Simard et al. (1997c) 84% decrease

Kranabetter & Friesen (2002)

*denotes a significance difference according to ANOVA; no asterix means no statistics performed. †‘no difference’ means that differences between mean values were less than 25% but no statistical analyses were performed.

organic horizons were colonized by spore inoculum (Grogan et al., 2000; Bruns et al., 2002). Thus, many of the fungi that initially colonize seedlings in clearcuts appear to disperse primarily by spores. They may dominate ECM fungal communities in clearcuts because living ectomycorrhizal inoculum is not abundant. In conclusion, there is evidence that loss of inoculum or changes in the type of inoculum influence which fungal species colonize seedlings regenerating on clearcuts. Nevertheless, every study providing this evidence has also caused changes in the soil environment that may have contributed to the observed species shifts. In the next section, we review evidence that changes in the physical and biological environment

associated with clearcutting and seedling regeneration drive some of the changes in the ECM fungal community. (2) Evidence that changes in the environment drive species shifts in the ectomycorrhizal fungal community Two experiments provide clear evidence that some factor other than inoculum availability determines ECM fungal species composition on seedlings in clearcuts. Hagerman et al. (2001) compared ECM morphotypes on P. menziesii seedlings regenerating naturally in forests with similar seedlings in adjacent clearcuts. The clearcut seedlings had been present in the understory when clear-cut logging

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Pinus sylvestris1 Pinus contorta2

Seedlings Trees Seedlings Trees

Review

Total number of ectomycorrhizal fungi

Number of fungi in common

% of ectomycorrhizas formed by fungi in common

17 17 14 20

10 10 12 12

93% 72% 97% 75%

1

Jonsson et al. (1999b). 2Bradbury (1998); Bradbury et al. (1998).

occurred (advanced regeneration). Three and four growing seasons after harvest, morphotype richness was significantly lower on seedlings in clearcuts than seedlings in the forest. Similar results were observed when naturally regenerated T. heterophylla seedlings were transplanted from forests to small clearcuts (Kranabetter & Friesen, 2002). After transplantion, an estimated 45% of ECM morphotypes were lost from seedlings, with increases in fungi typical of clearcuts (Table 3). Only one morphotype that was unique to forest seedlings survived transplantion into gaps; the rest had disappeared within 2 yr. In both of these studies, all seedlings would have been exposed to the same inoculum because they all initially developed in the forest understory. The results suggest that many forest ECM fungi cannot survive under conditions in the clear-cut, even if they are already present on root systems. This may be due to changes in the soil after clearcutting or, alternatively, these fungi may require associations with larger trees in order to survive. These two studies provide strong evidence that physical, chemical or biological factors (Fig. 1) other than inoculum type and level are responsible for at least some of the differences in ECM communities on clearcuts, a conclusion that was also reached by Perry & Rose (1983). Even in the absence of physical disturbance to the forest floor, physical, chemical and biological characteristics of the soil will change following clearcutting (Perry & Rose, 1983). For example, maximum soil temperatures in clearcuts can be 2–5°C higher, even in regions with short growing seasons (Zhou et al., 1997; Huggard & Vyse, 2002). Soil moisture can be higher (Zhou et al., 1997), as a result of reduced transpiration, or lower (Huggard & Vyse, 2002), as a result of higher soil temperatures and therefore greater evaporation. Populations of microflora will change in response to the changes in carbon supply (reduced litter inputs) and microclimate. It is very difficult to determine the relative influence of chemical, physical and biological soil characteristics on the ECM fungal community because they are interrelated. For example, changes in the microflora can affect ectomycorrhiza formation directly (Garbaye & Bowen, 1987; Summerbell, 1987; Friedman et al., 1989) or indirectly via changes in decomposition and nitrogen mineralisation rates (Jurgensen et al., 1997; Forge & Simard, 2000; Prescott et al., 2000). In one of the few studies specifically targeted at chemical or physical factors, Parke et al. (1983a) found a significant effect of soil temperature on the relative abundance of specific ECM fungi

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on P. menziesii. By contrast, soil pH had no effect on colonization of Pn. banksiana by indigenous ECM fungi (McAfee & Fortin, 1987). From the point of view of an ECM fungus, the plant community that regenerates after logging can differ in several important ways from the previous one. First, the age of the major ECM hosts will be different: seedlings or young trees will replace most mature trees. Second, the tree species in the regenerating stand may differ from the previous stand. This will happen if the new stand is at an earlier seral stage or if the site is replanted with a subset of the original tree species. Third, the density and species composition of nonECM hosts may differ. Irradiance is higher in clearcuts and this will result in the suppression of shade-adapted species. The growth of some tree seedlings may increase, depending on their shade tolerance (Zhou et al., 1997; Ingleby et al., 1998). Sometimes clearcuts are seeded with grasses and forbs for grazing of domesticated animals. Each one of these changes might drive a change in the ECM fungal community on a site. We will consider each in turn. (a) Effect of host age There has long been a perception that some ECM fungi are incapable of colonizing seedlings and instead are restricted to mature trees. Certainly the number of types of ectomycorrhiza associated with seedlings increases as they develop into young trees (Mason et al., 1987; Danielson, 1991; Richter & Bruhn, 1993; Bradbury et al., 1998; Bradbury, 1998). Two recent studies also seem to support this idea. In one study seedlings were present in the understory of a well-established forest (Jonsson et al., 1999b), and in the other seedlings naturally regenerating in a clearcut, at least 4 m away from possible refuge plants, were compared with mature trees in the adjacent stand (Bradbury et al., 1998; Bradbury, 1998). Both papers emphasize the substantial overlap in ECM fungal communities between seedlings and mature trees; however, in both studies 40% of the ECM fungi or morphotypes on mature trees were not present on the seedlings (Table 4). Furthermore, approx. 25% of the roots of the mature trees were formed by fungi absent from the root systems of seedlings. These results indicate that most, but not all, ECM fungi in mature forests can colonize very young seedlings. Some may be able to colonize seedlings but cannot persist in the absence of connections with mature trees (Kranabetter & Friesen, 2002). Thus age of the tree might play a minor

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role in the differences in ECM fungal communities between mature stands and stands regenerating after logging. (b) Effect of host species Many ECM fungi have broad host ranges, but some are restricted to specific families, genera, or species of host (Molina et al., 1992; Newton & Haigh, 1998). Although host specificity can broaden when roots of a secondary host grow in the vicinity of a primary host (Massicotte et al., 1994), roots of different tree species will be colonized with different ECM fungi, even in very close proximity to each other (G. Kernaghan et al. unpublished; Kranabetter et al., 1999). Therefore, if a site is replanted with a different species than was previously present (Richter & Bruhn, 1993), one would expect at least a transient reduction in the number of ECM fungi present. Only those fungi that could associate with both the previous and the newly planted species would be present initially, although other fungi could subsequently disperse into the site. We are not aware of any controlled studies investigating this phenomenon. The only evidence is for exotic host species. These are often introduced with a subset of their native ECM fungi, resulting in low ECM fungal diversity in stands of these trees (Chu-Chou & Grace, 1981; Swart & Theron, 1990; Dell & Malajczuk, 1997). A common occurrence in North American silviculture is to plant only one tree species on a site where a mixed forest had been present prior to logging. In partially cut stands, secondgrowth stands or plantations there is usually (Bills et al., 1986; Heslin et al., 1992; Ferris et al., 2000; Kranabetter & Kroeger, 2001), but not always (D.M. Durall et al. unpublished) greater species richness of epigeous ECM fruitbodies in mixed than single-species plots. This tells us little about diversity of ectomycorrhizas below-ground because of the poor correlation with fruitbody diversity ( Jonsson et al., 1999b). The very few comparisons of below-ground ECM fungal diversity in singlespecies or mixed-species plantations have found only minor effects (Heslin et al., 1992; Jones et al., 1997). It is possible, however, that no treatment effects were detected in these cases because the trees were exotics (Heslin et al., 1992) or quite young (Jones et al., 1997) and ECM fungal diversity would be expected to be low under these conditions. Nevertheless, this does suggest that broadening of host specificity onto secondary hosts may not be important in young stands, where most ectomycorrhizas are formed by pioneer fungi. These fungi often have broad host ranges (Deacon & Fleming, 1992). In older (approx. 100 yr) naturally regenerating mixed stands of Abies, Betula, Picea, Pinus, and Populus species, G. Kernaghan et al. (unpublished) found a significant positive correlation between ECM morphotype diversity and tree species diversity. Interestingly, however, the correlation was not with the species diversity of roots (as determined by wood anatomy), but with overstory tree diversity (the roots of some tree species entered the plots from stems that did not directly overhang the plots). They attribute this surprising result to greater resource heterogeneity in plots with mixed leaf litter

(G. Kernaghan, pers. comm.). Others have also found that litter type can influence the ECM fungal community that develops on roots (Conn & Dighton, 2000). These results are important reminders that, although ECM fungi gain most of their carbon from a plant symbiont, they have evolved from saprotrophic fungi and still colonize and extract nutrients from soil organic matter (Bending & Read, 1995). The major conclusion from the Kernaghan study is that more diverse communities of ECM fungi are expected in mixed than pure stands of mature trees as a result of both resource heterogeneity and fungus-host specificity. (c) Effect of nonectomycorrhizal plants After clearcut logging, it is not unusual for growth of planted tree seedlings to be suppressed by competition from shrubs and herbs (Amaranthus & Perry, 1994; Titus et al., 1995). If these plants do not form ecto- or arbutoid mycorrhizas, they can suppress ectomycorrhiza formation. For example, Pinus lambertianna formed fewer ectomycorrhizas when planted on a site seeded with grasses than on an adjacent, unseeded site (Amaranthus & Perry, 1994). Both Jones et al. (1997) and Richter & Bruhn (1993) observed that Wilcoxina and Thelephora mycorrhizas were not replaced as rapidly by indigenous ECM fungi on sites where AM hosts were prevalent. Furthermore, the species richness of ECM fruitbodies in a Thuja plicata – T. heterophylla forest was weakly negatively correlated with the basal area of T. plicata, an AM tree (Kranabetter & Kroeger, 2001). Ectomycorrhiza development or diversity per seedling was increased when competition from grasses was removed by chemical or mechanical means, but this was a transient effect only (Harvey et al., 1996; Jones et al., 1996). In most of the above cases, seedling growth was also reduced in the presence of high density of AM plants, and this may have been more important than a direct effect of AM roots on the development of ectomycorrhizas. Zhou et al. (1997) found no effect of an understory of fern and maple seedlings on ECM fungal colonization of Quercus rubra (red oak). There has been much interest in the difficulty in regenerating conifers on sites in northern Europe or Canada that become dominated by ericoid mycorrhizal (ErM) plants after clearcut logging (Robinson, 1972; Titus et al., 1995; Prescott & Blevins, 1999). Conifer seedlings are often nutrient stressed on these sites and ECM colonization may be reduced (Handley, 1963). For example, planting Picea mariana (black spruce) seedlings within 1 m of Kalmia angustifolia plants reduced ECM colonization by 50% (Yamasaki et al., 1998). Mycorrhizal colonization of hemlock seedlings that were nonmycorrhizal at planting was reduced in thickets of Rhododendron maximum (Walker et al., 1999). Extracts of tissues of K. angustifolia and Calluna vulgaris inhibited growth of ECM fungi and suppressed mycorrhiza formation by some fungi in vitro (Robinson, 1972; Mallik & Zhu, 1995). Thus, these ErM plants appear to have a direct negative effect on ECM fungi. Interestingly, litter of Banksia grandis, a nonmycorrhizal

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Fig. 2 Relative abundance of ectomycorrhizal morphotypes on roots in subalpine clearcuts in the summer of 1997. Soil cores contained roots of mature Picea engelmannii and Abies lasiocarpa, which had been harvested 30 months earlier. Field bioassay seedlings were P. engelmannii seedlings grown in the same clearcuts for one growing season (13 wk) and which were nonmycorrhizal at planting. Nursery-grown seedlings were of the same seedlot of P. engelmannii, but had ectomycorrhizas matching the descriptions of Mycelium radicis atrovirens (MRA), E-strain, Thelephora and Amphinema mycorrhizas on their roots at planting 14 months before sampling.

species, suppressed ectomycorrhiza formation by Eucalyptus marginata, whereas litter from Acacia pulchella, a mycorrhizal species, did not (Reddell & Malajczuk, 1984). These studies indicate that nonECM plants, especially ErM plants, can have a negative effect on formation of ectomycorrhizas on clearcuts. Too few studies designed specificially to test for these effects have been performed to make firm conclusions however. (d) Effects of soil microflora and fauna Communities of soil macro-, meso- and microfauna and microflora change after logging (Huhta et al., 1967; Perry & Rose, 1983; Bird & Chatarpaul, 1986; Forge & Simard, 2000; Battigelli & Berch, 2002). Although it is clear that soil microflora and fauna influence the colonization ability and function of ECM fungi (Slankis, 1974; Bowen & Theodorou, 1979; Chakraborty et al., 1985; Fitter & Garbaye, 1994; Dunstan et al., 1998; Perez-Moreno & Read, 2001), we know of only one major study on these interactions in clearcuts. Colinas et al. (1994) applied biocides specific for different groups of organisms to investigate which organisms were responsible for an increase in ECM formation when forest soil was added to planting holes in clearcuts. These authors had previously concluded that poor ectomycorrhiza formation on their clearcut sites was not due to low ECM fungal inoculum, but rather that some biological or chemical factor in the clearcut soil prevented ectomycorrhiza formation (Amaranthus & Perry, 1987). Although none of the specific biocides significantly stimulated numbers of ectomycorrhizas formed on P. menziesii, both pasteurization and tyndallization did (Colinas et al., 1994). Thus, the authors concluded that the clearcut soil contained some deleterious organism that prevented colonization by ECM fungi. (e) Effect of introduced ectomycorrhizal fungi Tree seedlings often become ectomycorrhizal with fungi in the nursery prior to being planted on logged sites. Although these nursery fungi typically decrease in abundance after outplanting

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(Dixon et al., 1981; Bledsoe et al., 1982; Browning & Whitney, 1992; Richter & Bruhn, 1993; Chang et al., 1996; Jones et al., 1997), they can persist for at least 1–2 yr (Castellano & Trappe, 1985; Browning & Whitney, 1992; Roth & Berch, 1992; Jones et al., 1997) and even up to 8 yr (Garbaye & Churin, 1997). These introduced fungi can sometimes colonize other trees. Fungi already present on a root system can have a competitive advantage over other ECM fungi in colonizing newly produced roots (Parladé et al., 1999); thus, in some cases, the nursery fungi suppress colonization by indigenous fungi (McAfee & Fortin, 1986; Dahlberg & Stenström, 1991; Berch & Roth, 1993; Jones et al., 2002). This means that the ECM fungal community on roots of seedlings produced in a nursery and subsequently planted on a clearcut will differ, at least initially, from seedlings that regenerate naturally on the site. Jones et al. (2002) found that 98% of new roots produced by nursery-grown P. engelmannii during the first three growing seasons after planting formed the same four ECM morphotypes present on the root systems at outplanting (Fig. 2). By contrast, dominant fungi from the previous stand formed 40% of ectomycorrhizas formed on P. engelmannii seedlings that had been nonmycorrhizal at planting (Hagerman et al., 1999a,b). The nursery seedlings were planted on mounds created by mechanical site preparation, whereas the nonmycorrhizal seedlings were planted in sites between the mounds. We cannot determine the relative importance of the competition by ECM fungi from the nursery vs the differences in planting microsite, but this example again illustrates the complexity of factors that can influence which ECM fungi colonize young seedlings in clearcuts. (3) Conclusions about the factors that influence colonization by ectomycorrhizal fungi in clearcuts The fungi that dominate the ECM fungal community after clearcutting often can disperse primarily from spores or

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propagules other than living mycorrhizas. However, there is strong evidence that changes in the soil environment are just as important as changes in inoculum in determining which fungi colonize roots in the regenerating stand. Reduction in host age probably has only a minor effect, but a change in host species will have a larger impact, especially as the stand ages. Part of this effect may be through a change in litter and associated soil microflora and fauna. Nonhost plants and ECM fungi introduced from nurseries may also have an impact. Overall we can conclude that some of the shift in ECM fungal community is towards fungi that are better adapted to disperse and survive in the conditions produced by clearcut logging.

V. Possible consequences for regenerating stands of species shifts in ectomycorrhizal fungi In this final section, we discuss how changes in ECM fungal community induced by silviculture treatments might affect the productivity and composition of the regenerating stand. We discuss this at three levels: how colonization by specific ECM fungi might affect the growth of individual seedlings in regenerating stands; how colonization by a number of ECM fungi might affect seedling growth differently than colonization by one fungus; and how the species composition of the ECM fungal community might influence the species composition of the plant community. (1) Will the loss or gain of specific ectomycorrhizal fungi influence seedling productivity in the regenerating stand? If the species of ECM fungi available to colonize young seedlings is changed by clearcut logging, this could influence the regenerating stand by directly affecting the growth of individual tree seedlings. Most of the relevant research comes from inoculation trials for plantation forestry using a small number of fungal isolates. In the field, tree seedlings respond to inoculation with different single ECM fungi with increased growth, decreased growth or no change in growth relative to nonmycorrhizal plants, depending on the fungal isolate and on the site (Bledsoe et al., 1982; Beckjord & McIntosh, 1984; Ekwebelam & Odeyinde, 1984; Shaw et al., 1987; Loopstra et al., 1988; Browning & Whitney, 1992; Parladé et al., 1997). In some cases, inoculation stimulates or inhibits growth in the nursery relative to uninoculated plants and these growth differences are carried over into the field (Shaw et al., 1987; Stenström, 1990; Burgess et al., 1994). Inoculation effects can last up to 7–10 yr (Marx et al., 1988; Garbaye & Churin, 1997; Selosse et al., 2000), sometimes persisting even after the inoculated fungi have disappeared from the root systems (Garbaye et al., 1988). In other cases, differences in size persist for only 1 or 2 yr after outplanting and then

disappear (Hatchell & Marx, 1987; Loopstra et al., 1988; Cram et al., 1999). Inoculation effects may disappear when indigenous fungi rapidly replace inoculated fungi (Sidle & Shaw, 1987, see Section IId above). A second type of response is for inoculation to cause decreased growth rates or no differences in growth rate in the nursery, but increased relative growth rates following outplanting (Beckjord & McIntosh, 1983, 1984; Castellano & Trappe, 1985; Marx et al., 1985; Villeneuve et al., 1991; Quoreshi & Timmer, 2000). This can happen when inoculated seedlings grow faster than uninoculated seedlings only during periods of drought (Marx et al., 1985, 1988; Garbaye & Churin, 1997); such conditions would not normally occur in the nursery. Furthermore, Quoreshi & Timmer (2000) have found that ECM seedlings may be the same size or smaller than uninoculated seedlings in the nursery, but may have higher nutrient contents (mg nutrient per seedling). These nutrient reserves may allow higher relative growth rates by these seedlings after outplanting. In most of the trials cited, uninoculated seedlings formed ectomycorrhizas in the nursery so these were really comparisons of seedlings colonized by different fungi. These observations indicate that seedling establishment and growth on a site can be influenced by colonization with specific ECM fungi, especially if neighbouring seedlings are mycorrhizal with other fungi. Certainly ECM fungal inoculum is patchy in forests (Brundrett & Abbott, 1994; Taylor & Bruns, 1999; Grogan et al., 2000) and the distribution of ectomycorrhizas formed by different fungi is heterogeneous (Horton & Bruns, 2001). After one growing season on clearcuts most nonmycorrhizal Picea engelmannii seedlings had become colonized by only one fungus, and that fungus often differed amongst adjacent seedlings (Hagerman et al., 1999b). These early differences in colonization could be important enough to influence competitive outcomes between adjacent trees even though their ECM fungal associates would be expected to become more similar with time as their root systems grew and overlapped. (2) Will increases or decreases in the diversity of ectomycorrhizal fungi affect growth of individual trees or productivity of the entire stand? Whether considered at the level of a forest stand, or a small, localized volume of soil, communities of ECM fungi are typically species rich (Gardes & Bruns, 1996; Kranabetter & Wylie, 1998; Jonsson et al., 1999a; Taylor et al., 2000). Despite our increasing understanding of ECM community structure and dynamics, knowledge of diversity in ECM functioning within those communities is generally rather poor. This constrains our ability to interpret data from studies such as those in Table 2 in a functional context and predict the likely functional consequences of changes to community structure induced by silvicultural practices.

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Ectomycorrhizal fungi vary in their abilities to absorb nutrients in culture (Abuzinadah & Read, 1986; Jongbloed et al., 1991; Finlay et al., 1992; Keller, 1996; Anderson et al., 1999) and to transfer these nutrients to their plant hosts (Abuzinadah & Read, 1989; Bougher et al., 1990; Finlay et al., 1992; Van Tichelen & Colpaert, 2000). While functional variation appears implicit in these data, it must be stressed that such studies have been undertaken using only a handful of easily culturable fungal taxa that produce conspicuous fruiting structures in the field (Smith & Read, 1997; Cairney, 1999; Taylor et al., 2000). Genera that are difficult or impossible to culture or that form inconspicuous fruiting structures in the field can be important components of ECM communities (Kõljalg et al., 2000; Taylor et al., 2000). In other words, the fungi for which we know most regarding functioning may not necessarily be the most important ecologically, and their physiological attributes may represent only a subset of the potential activities of ECM fungi in natural and managed forest stands. Appreciating the extent of interspecific variation in ECM communities is further confounded by the fact that populations of individual ECM fungi display considerable intraspecific physiological variation and, for most taxa investigated, only single or a few isolates have been considered (Cairney, 1999). Where multiple isolates have been investigated, extensive variation has been reported (Meyselle et al., 1991; Finlay et al., 1992; Kieliszewska-Rokicka, 1992; Keller, 1996; Tibbett et al., 1998; Anderson et al., 1999), but extrapolation of this information to the field context is difficult, largely because of our rather limited understanding of the population biology of most ECM fungi (see Section II). It has been argued that, because forest soils are so heterogeneous, association with several ECM fungi should enhance the productivity of young seedlings (Perry et al., 1987; Jones et al., 1997). If different fungi are better adapted to different soil horizons or substrates (Reddell & Malajczuk, 1984; Dahlberg, 1990), they may be able to extract nutrients more efficiently from those substrates. Several studies have attempted to address the effect of multiple ECM taxa on host productivity and/or nutrition. Colonization of Pinus patula seedlings with two ECM fungi, for example, enhanced productivity compared to seedlings inoculated with either fungus individually (Reddy & Natarajan, 1997). Interpretation of these data in terms of the effect of increasing ECM diversity is, however, difficult since ECM root tip number increased when both fungi were inoculated together. Similarly, Parladé & Alvarez (1993) reported that different pairs of ECM fungi had different effects on growth of P. menziesii seedlings. Interpretation of their data in terms of potential functional differences between the fungal taxa is compromised by their use of only single isolates of each and observed differences in short lateral root production and colonization levels. When P. menziesii and P. ponderosa competed in mixture with each other, Perry et al. (1989b) found that yield, along with nitrogen and phosphorus nutrition was enhanced in the presence of certain

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ECM fungal combinations. In these experiments, the effect of the individual fungi upon the system was not determined, making it difficult to separate effects of increasing ECM fungal species richness from ‘sampling’ effects (Wardle, 1999). Indeed, the authors were careful to point out that their observations probably reflected more the effect of the presence of particular ECM fungi (Laccaria laccata had a very large effect on P. menziesii) than an effect of different numbers of ECM fungi. More recent experiments have incorporated single ECM fungal treatments, so as to avoid potential ‘sampling’ effects. Jonsson et al. (2001) investigated the influence of inoculated ECM fungal species richness on growth of P. sylvestris and Betula pendula in soils of ‘high’ or ‘low’ fertility. Only in the case of B. pendula in the ‘low’ fertility soil did fungal species richness significantly enhance seedling growth. Indeed, for P. sylvestris in ‘high’ fertility soil, increasing fungal diversity was associated with decreased growth of the host. Using a rather artificial peat: vermiculite growth substrate of high fertility, Baxter & Dighton (2001) found that, while ECM fungal diversity had no effect on whole plant biomass, it was associated with increased root, but decreased shoot, biomass. Moreover, ECM fungal diversity significantly enhanced plant phosphorus (but not nitrogen) content. One criticism of the studies cited here is that the plants were grown in uniform environments. A stimulatory effect of fungal diversity is more likely in heterogeneous environments that, in turn, more realistically mimic natural forest soils. Clearly, many more experiments that more accurately reflect the soil environment will need to be conducted before general conclusions on diversity effects, including those caused by silviculture, can be inferred. (3) How will changes in the potential for hyphal linkages between plants affect seedling establishment and competition? A common feature of the species changes in the fungal community following clearcut logging is a shift to ECM fungi that are host generalists (Dahlberg & Stenström, 1991; Jones et al., 1997; Bradbury, 1998; Hagerman et al., 1999b; Jones et al., 2002). This means that there will be increased opportunities for adjacent trees of different species to associate with the same mycelium. This has the potential to influence below-ground interactions between these trees (Newman, 1988; Miller & Allen, 1992; Amaranthus & Perry, 1994; Fitter, 2001; Simard et al., 2002). These hyphal connections may take longer to develop in clearcuts, where seedlings are planted 1–3 m apart than they would for a seedling developing in the understory of an existing stand. In this section we discuss the evidence that adjacent trees can be associated with the same fungal mycelium and speculate upon the implications of this. Autoradiography and microscopy tracings of transparent laboratory containers have provided direct evidence of ECM

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(Reid & Woods, 1969; Read et al., 1985; Finlay & Read, 1986; Arnebrant et al., 1993; Wu et al., 2001) and AM (Hirrel & Gerdemann, 1979) hyphal linkages between plants. Similar direct observations of interplant hyphal linkages have not been made in the field, due to the small, hyaline nature of ECM hyphae and the three-dimensional nature of the mycelia (Newman, 1988). Recent molecular approaches demonstrate that genets of some ECM fungi extend far enough to encompass the root systems of several trees (Sawyer et al., 2001; Zhou et al., 2001), but these results are for sporocarps, not root tips. Examination of root tips by morphotyping or molecular techniques indicates that one fungal species commonly colonizes adjacent trees and shrubs in the field (Dahlberg & Stenström, 1991; Jones et al., 1997; Simard et al., 1997a; Horton et al., 1999; Kranabetter et al., 1999; Byrd et al., 2000; Hagerman et al., 2001). We must await results from techniques, such as microsattelite analysis of DNA (Kretzer et al., 2000), to confirm that single genets of ECM fungi colonize root systems of different plants. Although this information will not demonstrate how hyphal linkages function, it could certainly test the hypothesis of Newman (1988); that most mycorrhizal plants are interconnected by a common mycorrhizal network. There are three major ways that ECM fungal linkages might influence fungal or plant ecology in regenerating forest stands: as a source of inoculum for seedlings (see Section IV.1.a); to allow the carbon demands of a mycelium to be met by more than one host (Wu et al., 2001); or to facilitate the transfer of carbon and mineral nutrients between neighbouring trees (Simard et al., 1997b; see Fitter et al., 1998, 1999; Robinson & Fitter, 1999; Simard et al., 2002). Wu et al. (2001) showed convincingly that photosynthate from one plant can supply carbon to an ECM fungus on the roots of an adjacent plant, in the lab. Furthermore, carbon can be transferred below-ground between plants, with net below-ground carbon transfer increasing toward shaded plants (Simard et al., 1997c). If the carbon demands of their ECM symbionts were partially met by another tree in the field, or if seedlings in the understory were the net recipients of carbon from another plant, the carbon balance of these seedlings could be improved. We have no empirical data, however, to determine how the carbon demands of a fungus are partitioned amongst several plants associated with that single mycelium in the field. Evidence for reduction of competition through ECM fungal linkages is limited. Perry et al. (1989b) showed that competition between P. ponderosa and P. menziesii in pots was reduced by the presence of specific ECM fungal types colonizing both plant species. Reasons given for the reduction of competition included: the ability of mycorrhizal fungal networks to access nutrients from different substrates (e.g. organic vs inorganic), the ability of fungal networks to distribute nutrients relatively evenly between the different plant species, and the ability of fungi to be active over a wide range of moisture and temperature conditions.

VI. Conclusions We draw several conclusions about the effects of clearcut logging on the interactions between ECM fungi and seedlings. 1 There is no clear evidence that inoculum of ECM fungi is disrupted to the extent that total colonization of roots is affected. 2 There are clear changes in the species composition of the ECM fungal community. Further work is required to determine if these changes are similar to those caused by natural disturbances. 3 Biological, chemical and physical changes in the soil environment are probably as important as alterations in inoculum in causing changes in the ECM fungal community. This implies that the fungi that colonize after clearcut logging are better adapted to disperse into or persist under these conditions. 4 The consequences of changes in the ECM fungal community need to be evaluated in terms of fungal physiology and ecology. Comparisons of the abilities of clearcut fungi and forest fungi to take up nutrients and transfer them to their hosts will allow us to determine how these shifts in fungal species might influence the growth of young trees in the regenerating stand.

Acknowledgements We started work on this manuscript while Melanie Jones and Dan Durall were on sabbatical leave at the University of Western Sydney. We are grateful to Lauren Bennett, Mona Högberg, François Le Tacon, Robin Sen, and Brad Smith for providing us with silviculture statistics for Table 1 or directing us to appropriate sources. We thank Frann Antignano for preparing Table 1.

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