Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes1
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1243
Mycorrhizal fungi as drivers of ecosystem
processes in heathland and boreal forest biomes1
David J. Read, Jonathan R. Leake, and Jesus Perez-Moreno
Abstract: The importance of mycorrhizas in heathland and boreal forest biomes, which together cover much of the
landmass of the Northern Hemisphere and store most of the global stocks of carbon, is reviewed. The taxonomic affini-
ties of the organisms forming these symbiotic partnerships are assessed, and the distinctive structural features of the
ericoid mycorrhizas of heathland dwarf shrubs and the ectomycorrhizas of boreal forest trees are described. It is
stressed that neither in terms of the geographical distribution of the plants nor in terms of the occurrence of their char-
acteristic mycorrhizas in the soil profile should these biomes be considered to be mutually exclusive. What unites them
is their apparent affinity for acidic organic soils of inherently low accessibility of the major nutrients nitrogen (N) and
phosphorus (P). These properties relate directly to the nature of the nutrient-poor recalcitrant litter produced by their
host plants and through positive-feedback mechanisms that are reinforced by selective removal of labile nutrients by the
mycorrhizas. We suggest that coevolution of these plant litter traits with mycorrhizal associations that are adapted to
them has been one of the defining features of these ecosystems. Ericoid and ectomycorrhizal fungi have biochemical
and physiological attributes that make them highly efficient at scavenging for organic sources of N and P in surface
soil horizons. In so doing, they restrict supplies of these elements to the decomposer communities. Case studies involv-
ing exploitation of N and P in defined organic substrates are described. In both biomes the dominant plants depend
upon the abilities of their fungal partners to recover nutrients, so the symbioses control nutrient cycles, productivity,
species composition, and functioning of these ecosystems. It is in this context that the fungal symbionts are here con-
sidered to be drivers of nutritional processes in their respective biomes. Through their influences upon the quality of
carbon residues mycorrhizal fungi must also affect the sink–source balance for this key element in soil. There is an ur-
gent need for the evaluation of the relative contributions of symbiotic and saprotrophic components of the microflora to
the processes of carbon storage and cycling in these biomes, particularly in the context of global climate change and
impacts of anthropogenic pollutant N deposition.
Key words: carbon sequestration, peatlands, C/N ratios, carbon and nutrient cycles.
Résumé : Cette revue porte sur l’importance des mycorhizes dans les biomes des tourbières et des forêts boréales, qui
couvrent ensemble une grande partie des masses continentales de l’hémisphère nord et cumulent une majeure partie des
réserves globales du carbone. Les auteurs évaluent les affinités taxonomiques des organismes qui forment ces partena-
riats symbiotiques, et décrivent les caractéristiques structurales propres aux mycorhizes éricoïdes des arbustes nains des
tourbières, et aux ectomycorhizes des arbres de la forêt boréale. On insiste sur le fait qu’on ne doit en aucune façon
considérer ces deux biomes comme mutuellement exclusifs, que ce soit sur la base de la distribution géographique des
plantes, ou de la présence de leurs mycorhizes caractéristiques dans le profil de sol. Ce qui les unis est leur apparente
affinité pour les sols organiques acides avec leur inaccessibilité inhérente aux nutriments majeurs, l’azote (N) et le
phosphore (P). Ces propriétés sont directement reliées à la nature des litières récalcitrantes pauvres en nutriments pro-
duites par leurs plantes hôtes, laquelle, par des mécanismes de rétroaction positive, est renforcée par l’élimination sé-
lective des nutriments labiles via les mycorhizes. Les auteurs suggèrent que la coévolution de ces caractéristiques des
litières végétales avec des associations symbiotiques qui leurs sont adaptées, a été une des caractéristiques définissant
ces écosystèmes. Les champignons éricoïdes et ectomycorhiziens ont des propriétés biochimiques et physiologiques qui
les rendent hautement efficaces à récupérer les sources organiques de N et de P dans les horizons de surface du sol. Ce
faisant, ils limitent la disponibilité de ces nutriments pour la communauté des décomposeurs. On décrit des cas
d’espèce impliquant l’exploitation du N et du P dans des substrats organiques définis. Dans les deux biomes, les plan-
tes dominantes dépendent de la capacité de leurs partenaires fongiques à récupérer les nutriments, de sortes que les
symbioses contrôlent les cycles nutritifs, la productivité, la composition en espèces et le fonctionnement des écosystè-
mes. Par leurs influences sur la qualité des résidus carbonés, les champignons mycorhiziens doivent également affecter
Received 7 October 2003. Published on the NRC Research Press Web site at http://canjbot.nrc.ca on 9 September 2004.
D.J. Read2 and J.R. Leake. Department of Animal and Plant Sciences, The University of Sheffield, Sheffield S10 2TN, UK.
J. Perez-Moreno. Colegio de Postgraduados, Microbiologia Edafologia-a-Irenat, Montecillo, Texcoco, C.P. 56320, Mexico.
1
This article is one of a selection of papers published in the Special Issue on Mycorrhizae and was presented at the Fourth
International Conference on Mycorrhizae.
2
Corresponding author (e-mail: d.j.read@sheffield.ac.uk).
Can. J. Bot. 82: 1243–1263 (2004) doi: 10.1139/B04-123 © 2004 NRC Canada1244 Can. J. Bot. Vol. 82, 2004
la balance source–puit pour cet élément clé. Il y a un urgent besoin qu’on évalue la contribution relative des compo-
santes saprophytiques et symbiotiques de la microflore aux processus de l’accumulation et du cyclage du carbone dans
ces biomes, surtout dans le contexte du changement global du climat et des impacts liés à la déposition de polluants N
d’origine anthropique.
Mots clés : séquestration du carbone, tourbières, rapports C/N, cycles du carbone et des nutriments.
[Traduit par la Rédaction] Read et al.
Introduction The mycorrhizal status of heathland and
boreal forest plants: taxonomic and
Together heathland and boreal forest biomes cover ap-
proximately 70% of the terrestrial surface of the Northern structural aspects
Hemisphere (Fig. 1). Since the soils that support them
contain the world’s largest stocks of carbon, the climate of ERM plants in heathlands
the planet, indeed, the future of the planet itself, can be In his analysis of heathlands as one of the major ecosys-
said to depend upon the interactions between the plants tems of the world, Specht (1979) defined them as being
that dominate these biomes, their microbial symbionts, characterized by their extreme nutrient impoverishment and
and the soil organic matter in which the symbiotic sys- by the predominance of dwarf shrubs of the family Eric-
tems proliferate. One of the least widely appreciated aceae and its relatives. In the present treatment, to facilitate
features of the atmosphere–plant–soil continuum in heath- direct comparisons with boreal forests, consideration will be
land and boreal forests has been that plant nutrients are largely restricted to the heaths of the Northern Hemisphere.
supplied through biotic interfaces with soil organic matter Here, the ericaceous genera of most widespread distribution
and minerals that are dominated by the mycelial systems and ecological importance are Calluna, Erica, Gaultheria,
of mycorrhizal fungi rather than by the roots themselves. Rhododendron, and Vaccinium. Representatives of these gen-
Whereas in the dominant plant family of heathland sys- era can form pure stands in areas situated latitudinally or
tems, the Ericaceae, the fungi proliferate within the epi- altitudinally above the forest tree line, where they may also
dermal cells of roots to form ericoid mycorrhiza (ERM) be mixed with shrubby representatives of the families Betu-
(Fig. 2, left panel), in the boreal forests, trees in the domi- laceae and Salicaceae (Fig. 1). These structural units are also
nant family, Pinaceae, are characterized by the possession referred to as “tundra”. Ericaceous plants are also major
of sheathing mantles of fungal tissue over the exterior components of the vascular plant flora of the extensive
of their root surfaces, forming ectomycorrhizas (ECM) northern peatlands and mire complexes. Here they contribute
(Fig. 2, right panel). In both cases the fungi occupy a zone as “ecosystem engineers” to the development of drier hum-
equivalent to the region in nonmycorrhizal or arbuscular mocks between Sphagnum lawns and are amongst a very
mycorrhizal (AM) plant families that is absorptive and restricted range of woody plants to grow on the most
normally produces root hairs. The emerging recognition nutrient-impoverished ombrotrophic raised mires. Some of
that fungal symbionts are critically positioned to exert the less-abundant ericaceous plants such as Andromeda poli-
controls over the exchanges of carbon and nutrients be- folia and Vaccinium oxycoccus are particularly associated
tween the sources and sinks of these biomes brings with it with these kinds of mires. Whilst most peatland ecosystems
an awareness that a better understanding of their func- differ hydrologically and pedologically from true heathlands,
tional capabilities is essential. their physiognomy and species composition share much in
Fortunately, studies of the mycorrhizal status of heathland common with heaths and tundra. In the transition from blan-
and boreal forest plants, which have been carried out with ket bogs to heathlands on peaty soils the distinctions are
increasing intensity over recent years, now place us in a completely blurred. The major ericoid plant species also of-
good position to consider these functional aspects in an eco- ten occur as a more or less continuous ground layer beneath
system context. Functional analysis, if it is to be realistic, the canopy of boreal forest trees in a structural unit termed
must be based upon a firm understanding of the nature of the “taiga”. Given the importance of ericaceous plants as major
symbioses being examined, that is, “what they are”, and but subdominant components in these extensive northern bog
upon their patterns of distribution in nature that determine and forest communities, we include consideration of them
the resources to which they have access, that is, “where they alongside their roles in heathlands.
are”. Armed with this information, one is equipped to begin Plants of the main ericaceous genera are themselves char-
to ask the functional questions, “What do they do and how acterized by a tightly conserved root architecture, the finest
do they do it?” distal elements of which lack root hairs but support inflated
These “What?”, “Where?”, and “How?” questions are ad- epidermal cells occupied by mycorrhizal fungi, the majority
dressed next, and the answers so far available are used to pro- of which are ascomycetes (Read 1996) (Fig. 2, left panel). In
vide some insights into the possible impacts of ERM and the sense that the fungi forming ERM also appear to be rep-
ECM symbioses upon key processes in the two types of resentative of a taxonomically, structurally, and functionally
biome. close grouping, they too can be said to be conserved. Early
© 2004 NRC CanadaRead et al. 1245
Fig. 1. Map showing distribution of boreal forest (black) and heathland-type (grey stipple) communities and the patterns of dominance
of ectomycorrhizal (ECTO) and ericoid mycorrhizal plants within these biomes. AM, arbuscular mycorrhiza.
descriptions of the typical symbionts of ericoid roots as be- still found, at some time in the Mesozoic era (Specht 1979;
ing dark-septate, normally sterile fungi that grew slowly in Kron 1996).
culture (Bain 1937; Burgeff 1961; Pearson and Read 1973) The likelihood that environmental factors, in particular the
were followed by a recognition that they were of ascomy- extremes of acidity, low levels of nutrient availability, and
cetous affinities and that most of them could be ascribed to accumulation of organic matter that typify the heathland
genera in the Helotiales, for example, the Hymenoscyphus– environment, will have contributed to the selection of this
Scytalidium complex (Read 1974, 1996; Egger and Sigler tightly conserved group of mycobionts has been hypothe-
1993; Sharples et al. 2000) or Onygenales Oidiodendron sized (Read and Perez-Moreno 2003). A defining feature
maius (Dalpé 1986; Hambleton et al. 1998). Molecular anal- that tightly links ericaceous plants to environments in which
yses of the fungal occupants of ericoid roots have now indi- rates of nutrient mineralization are very low is the exceed-
cated the presence of a somewhat broader range of fungal ingly low nitrogen (N) and phosphorus (P) concentration in
genera in ERM roots of both Northern (Perotto et al. 1996; their litter. Surveys of relationships between relative growth
Xiao and Berch 1996; Monreal et al. 1999; Allen et al. rates, shoot nutrient status, litter decomposition rates, and
2003) and Southern (Liu et al. 1998; McLean et al. 1999) types of mycorrhizal associations for over 80 species (Corn-
Hemisphere heathlands. Most of those for which, by follow- elissen et al. 2001) confirm the suggestion made by Read
ing Koch’s postulates, evidence of mycorrhizal status has (1991) that plants with ERM have the lowest shoot nutrient
been obtained still cluster in the same phylogenetically re- concentrations, lowest relative growth rates, and the slowest
lated groupings (Cairney and Ashford 2002). These similari- litter-decay rate. Plants with ECM have intermediate nutrient
ties have been used to support the hypothesis that ERM concentrations and growth rates, but their litter is also very
plants had a monophyletic origin (Cullings; 1996), probably recalcitrant, whereas plants with AM have the highest nutri-
in the Southern Hemisphere, where their greatest diversity is ent status and growth rates and their litter decays the fastest.
© 2004 NRC Canada1246 Can. J. Bot. Vol. 82, 2004
Fig. 2. Left panel: transverse section through the distal part of a “hair root” of the typical ericoid mycorrhizal plant Calluna vulgaris.
Note dense occupation of the inflated epidermal cells by hyphal complexes of Hymenoscyphus ericae. (Photo courtesy D.J. Read.)
Right panel: transverse section through an ectomycorrhizal fine root of Picea sitchensis colonized by the fungus Amanita spissa. Note
dense pseudoparenchymatous mantle of fungal mycelium ensheathing the external surface of the root with intercellular intrusions into
the cortical tissues forming a Hartig net. (Photo courtesy A. Taylor.)
The evidence that ericoid fungi represent a distinctive func- is the gymnosperm family Pinaceae, two of the genera of
tional type of mycorrhizal symbiont is discussed in the next which, Pinus and Picea, occupy vast tracts of the northern
section. land mass, often as monospecific stands of trees. As a result,
the boreal zone is sometimes simply referred to as “the
Ectomycorrhizas on plants of boreal forests northern coniferous forest”. Other components of these sys-
The boreal forest, or taiga, is the world’s largest vegeta- tems, which become of increasing importance in a poleward
tion system. It stretches as a continuous 1000–2000 km wide direction, are Larix and the angiosperm genera Betula and
circumpolar belt around the Northern Hemisphere (Fig. 1) Salix, all of which are deciduous.
(Whittaker 1970; Odum 1971). In the characteristically cool While plant diversities of the boreal forest are restricted
climates of this biome both evapotranspiration and decom- relative to those of more temperate biomes, the same cannot
position rates are low, with the result that the organic resi- be said for its flora of ECM fungal symbionts. Earlier stud-
dues of its plants accumulate either as raw humus at the soil ies, largely based upon records of the occurrence of fungal
surface or as peat, sometimes to considerable depths. In the fruit bodies and their patterns of association with particular
latter circumstance it is arguable whether the boreal system trees, suggested that upwards of 6000 species, largely of
should be described as a “forested bog” or as “a boggy for- basidiomycetous, but also of ascomycetous fungi, are likely
est”. to be capable of forming ECM (Molina et al. 1992), a con-
In so far as the soils over much of the boreal forest biome siderable proportion of these being mycorrhizal with boreal
are, like those of heathlands, characterized by low availabil- forest trees. The application of morphological (Agerer 1986–
ity of plant nutrients, particularly N (Tamm 1991), there is 1998; Taylor et al. 2000) and molecular (Gardes and Bruns
little to distinguish the major selective effects that nutritional 1996; Egger 1995; Dahlberg 2001; Horton and Bruns 2001)
limitations have placed upon both types of plant community. methods has largely confirmed the extent of this diversity
Indeed, the two biomes merge to the extent that over much but, more importantly, has revealed that the observed popu-
of its area the ericaceous ground layer of the boreal forest lation of fungal fruit bodies above ground is not representa-
might well be described as a heathland. However, the re- tive of the fungal community structure on the roots
sponses of the boreal forest dominants to nutritional limita- themselves. In nature, a relatively small number of dominant
tion have been different. In particular, this is a biome fungal taxa can form most of the ECM tips present (Gardes
characterized by the prevalence of ECM trees (Fig. 1). Like and Bruns 1996; Erland and Taylor 2002). Clearly, from a
their shrubby counterparts in heathlands, these are represen- functional as opposed to a biodiversity standpoint, it is im-
tative of a small number of genera. Of particular importance portant to determine the identities of these dominant fungi,
© 2004 NRC CanadaRead et al. 1247
some of which, for example, members of the families soil profile. In the case of the peaty soils that cover so much
Corticiaceae and Thelephoraceae, may not be represented at of the boreal zone, anaerobiosis associated with a high water
all in the conspicuous aboveground mycoflora (Taylor and table and permanent or winter freezing of the subsoil, re-
Alexander 1989; Kõljalg et al. 2000). Recognition of the stricts the essentially aerobic mycorrhizal fungi to the super-
predominance of fungi such as these is a prerequisite for ficial layers, as already noted for ericaceous plants. Trees
development of strategies for analysis of their functioning. require a slightly deeper oxic zone than the ericaceous
Until recently such analyses depended on the ability to plants. Although the greater evapotranspiration of trees than
isolate mycorrhizal fungi into pure culture, to enable their the dwarf shrubs permits a greater lowering of the water ta-
functioning alone and in symbiosis with host plants to be de- ble under forest cover, most trees, particularly the conifers,
termined under controlled laboratory conditions. The major are excluded from sites where the water table reaches the
constraint on such approaches is that amongst many genera surface during the growing season. In areas with better
such as Russula that can be dominant on roots (Taylor and drainage and a lower water table, leaching activities prevail
Bruns 1999) most species have proved unculturable, and and a trend towards podzolisation occurs.
there is an urgent requirement to develop methods such as Working in black spruce (Picea mariana) forests on soils
gene-expression analysis that do not require laboratory cul- of the humic type (pergelic cryoquats) of interior Alaska,
turing to establish functional traits. Ruess et al. (2003) found that 84% of fine-root production
occurred within 20 cm of the surface of the overlying moss
cover. In these forests, which constitute one of the largest
The vertical distribution of mycorrhizal continuous vegetation types in North America, almost 100%
roots in heathland and boreal forest of first-order fine roots are ectomycorrhizal. These roots
ecosystems have an estimated life-span of 108 d, and even without con-
sideration of their extensive extararadical mycelial systems,
Distribution of ERM roots they constitute 56% of the total stand production. Calcula-
Analyses of fine-root distribution of plants with ERM tions based upon estimates of turnover rates (Ruess et al.
in heathlands (Gimingham 1972) and as understory compo- 2003) indicate that approximately six times as much N is cy-
nents of coniferous forests (Reiners 1965; Persson 1983) cling through fine roots than through litterfall.
consistently show an accumulation, even to the extent that a The effectiveness with which the ECM symbionts recap-
root “mat” can be formed, in the fermentation (F) and fer- ture this key resource must therefore be a key factor deter-
mentation-humic (FH) horizons at the top of the soil profile. mining stand productivity, and most likely, its fitness (see
The quantitative estimates of Persson (1983) indicate that following text).
in the cases of Calluna vulgaris and Vaccinium vitis-idaea Comparisons between boreal forests and their counter-
growing on a podzolic soil in Central Sweden, not only were parts in more temperate, lower latitudes (Van Cleve et al.
the bulk of the fine roots confined to the upper 22 mm of the 1983; Raich and Nadelhoffer 1989; Ruess et al. 1996;
profile, but the turnover in this FH zone was as much as Gower et al. 2001) indicate that boreal systems are distin-
97% and 87%, respectively, of that in the entire 30 cm of the guishable by the fact that a disproportionately large amount
profile. of the annual nutrient budget and soil CO2 flux appears to be
Such superficial rooting patterns enable ericaceous plants derived from mycorrhizal root processes.
to grow on slight hummocks on waterlogged peats, for ex- Detailed studies of mycorrhizal root distribution in boreal
ample, in ombrotrophic mires, despite their roots lacking forests have also been carried out in podzolic systems. In his
aerenchyma. Their dense proliferation of superficial roots, studies of Pinus sylvestris in sandy podzolic soils supporting
which grow upwards into the accumulating litter, forms an pine–heath, Persson (1983) observed a largely superficial
absorptive mat intercepting nutrient inputs in a manner anal- pattern of fine-root proliferation similar to that seen in the
ogous to that of the Sphagnum lawns that dominate the wet- ericoid plants. However, the presence of ericoid understory
ter hollows. They may also make a significant contribution plants could influence their depth profiles. In areas support-
to the accumulation of peat. In contrast with deep-rooted ing patches of C. vulgaris the major zone of proliferation
cyperaceous plants like Eriophorum that have very well- was depressed by a few centimetres to a region closer to the
developed aerenchyma (Malmer et al. 2003), the shallow- FH-mineral soil transition.
rooted Ericaceae lack air channels in their roots and provide In a recent analysis of the distribution of Picea abies roots
no oxygen supply to the anaerobic peat. Their interception across a latitudinal gradient through Europe from the boreal
and uptake of N and P at the surface will restrict the supply (Skogaby, SW Sweden) to temperate zone (Waldstein, Ger-
to the underlying peat of the main nutrients (N and P) that many, and Aubure, France) it was shown (Stober et al. 2000)
limit microbial decomposition in ombrotrophic mires (Aerts that the bulk of the fine roots were located in the top 10 cm
et al. 2001). Furthermore, the organic matter produced by of the soil profile in every stand. However, there was some
ericaceous plants is exceptionally rich in phenolic com- evidence of a greater proliferation (93% as distinct from
pounds (Jalal et al. 1982), many of which are highly fungi- 75% and 78%, respectively) of fine roots in the organic hori-
toxic and are known to inhibit microbial decomposition of zon of the boreal than in the two more southerly sites. Addi-
litter (Leake and Read 1989). tionally, whereas most of the fine roots in the upper 10 cm
of the profile were living, those in the deeper profiles were
Distribution of ECM roots considered to be mostly dead.
The fine roots of ECM genera of boreal forest trees are It is a feature of most previous studies of fine-root popula-
also strongly concentrated in the superficial horizons of the tions that while authors have recognised that roots of the less
© 2004 NRC Canada1248 Can. J. Bot. Vol. 82, 2004
Fig. 3. Average total number of mycorrhizal root tips in each horizon of a boreal forest soil (O, E1, E2, EB, B1, B2, and C) expressed
as the percentage of total number of such tips in the organic horizon (O). Error bars represent SE of the mean (n = 3). (From Rosling
et al. 2003. Reproduced with permission of New Phytol., Vol. 159, p. 779, © 2003 Cambridge University Press).
than 2 mm diameter size category consist almost entirely of Further recent studies, one using DNA analysis of hyphal
ectomycorrhizas, few until recently have taken the desirable fragments recovered from the L, F, H, and B horizons of a
next step to characterize the ECM and describe their distri- pine forest soil (Dickie et al. 2002), another a combination
bution in the soil profile. The advent of molecular tech- of sequencing with morphotyping in boreal forest substrates
niques has made this advance possible. Rosling et al. (2003) of differing quality (Tedersoo et al. 2003) and one using
have analysed the distribution of ECM root tips and charac- morphotyping alone (Koide and Wu 2003), indicate cluster-
terized their fungal associations in a boreal forest podzol ing of distinctive groups of mycorrhizal fungi in specific
supporting Pinus sylvestris and Picea abies in Central Swe- niches in coniferous forest soils. In the study of Tedersoo et
den. While they found, as in previous studies, that the or- al. (2003), a strong preference of resupinate thelephoroid
ganic layer is the most intensively exploited by fine roots and athelioid fungi for coarse woody debris was observed.
(Fig. 3), they also demonstrated that considerable numbers Results of these kinds confirm earlier observations made at
of mycorrhizal roots occur in the mineral horizons. Half of the macroscopic scale, but now add information on the iden-
the fungal taxa identified were associated with the mineral tity of the fungi present. For example, Dimbleby (1953)
soil (Table 1). Of the mineral horizons most heavily ex- examining the factors involved in the invasion of heathland
ploited by ECMs, that located immediately beneath the or- soils by birch, noted that seedling establishment and prolif-
ganic layer, the E1, contained the largest number of fine eration of mycorrhizas occurred exclusively in relict 150-
roots. This is a horizon into which soluble organic residues year-old decaying stumps of pine. The questions raised by
will first leach after rainfall or thawing events, so the pres- such observations at that time are as pertinent, and as much
ence of significant numbers of ECM roots here is perhaps to unresolved, now as they were 50 years ago. Are the ectomy-
be expected. More surprising is that the fungi occupying the corrhizas formed in a particular substrate because inoculum
two types of environment appear to be different (Table 1), has survived there? Are these substrates particularly favour-
although their primary sources of energy (the trees) are able for spore germination or for root and mycorrhiza prolif-
likely to be the same. While Dermocybe spp., Tomen- eration? If so, is the basis of their favourability physical,
tellopsis submollis, and three Piloderma species were found chemical, or the result of less antagonistic interactions with
predominantly in the organic horizon, Suillus luteus, other organisms in the occupied areas? Is it due to combina-
Lactarius utilis, and three further species of Piloderma were tions of these factors? These questions relate to function and
associated with the mineral horizons. are addressed in the following section.
© 2004 NRC CanadaRead et al. 1249
Table 1. Vertical distribution of mycorrhizal taxa on roots sampled throughout a podzol profile showing the highest
recorded abundance of each taxa in the organic (O: 0–3 cm) and mineral horizons E1 (3–18cm), B (18–35 cm), and
C (40–53 cm) (after Rosling et al. 2003).
Soil horizons
Mycorrhizal taxa O E1 E2 EB B1 B2 C
Tylospora spp. 䊉 䊉 䊉 䊉 䊉 䊉䊉䊉
Cortinarius spp. 䊉 䊉䊉䊉䊉 䊉 䊉䊉 䊉䊉 䊉
Piloderma reticulatum 䊉䊉䊉䊉 䊉䊉䊉䊉 䊉䊉 䊉 䊉 䊉
Piloderma sp. 1 䊊 䊊 䊉 䊉
Inocybe spp. 䊉
Piloderma byssinum 䊉
Tomentellopsis submollis 䊉 䊉
Piloderma fallax 䊉 䊉 䊉
Hygrophorus olivaceoalbus 䊉 䊉 䊉
Russula decolorans 䊉䊉䊉䊉 䊉䊉䊉䊉 䊉 䊊
Dermocybe spp. 䊊 䊉 䊉 䊉
Tomentelloid 䊊 䊉
Lactarius utilis 䊉 䊉䊉 䊉䊉
Piloderma sp. 2 䊉 䊉 䊉 䊉䊉
Piloderma sp. 3 䊉 䊉 䊉
Piloderma sp. 4 䊉 䊉 䊉
Suillus luteus 䊉 䊉䊉䊉 䊉䊉䊉 䊉䊉䊉䊉 䊉
Unknown 1 䊉
Unknown 2 䊉
Wilcoxina 䊉
Russula adusta 䊉䊉䊉䊉
Tricholoma portentosum 䊉䊉䊉
Note: The highest relative abundance of taxa in three replicate cores (except for EB horizon, where n = 2) are indicated according
to the following intervals: 䊊1250 Can. J. Bot. Vol. 82, 2004
Table 2. Extracellular enzymes, known to be produced by ericoid mycorrhizal fungi, which would be expected to provide the ability to
degrade structural components of plant litters in heathland and other ericaceous plant communities, thereby affecting decomposition
processes and “unmasking” of nutrients to facilitate attack upon nitrogen- (protein degradation) and phosphorus-containing (organic
phosphorus) polymers.
Process Substrate Enzyme Reference
Plant cell wall degradation Pectin Polygalacturonase Perotto et al. 1997; Peretto et al. 1990
Cellulose Cellulase Varma and Bonfante 1994; Burke and Cairney 1997a
Cellobiose Cellobiohydrolase Bending and Read 1996a; Burke and Cairney 1997a
Hemicellulose Xylanase Burke and Cairney 1998; Cairney and Burke 1998
β-Xylosidase Bending and Read 1996a; Burke and Cairney 1997a, 1997b
β-D-Mannosidase Burke and Cairney 1997a
β-D-Galactosidase Burke and Cairney 1997a
β-L-Arabinosidase Burke and Cairney 1997a
β-1,3-Glucanase Burke and Cairney 1997a
Oxidation of phenolic acids and Polyphenols Polyphenol oxidase Varma and Bonfante 1994
tannins
Laccase Bending and Read 1996b; Bending and Read 1997
Catechol oxidase Bending and Read 1996b; Bending and Read 1997
Hydrolysis of lignin Lignin Lignase Burke and Cairney 1998; Haselwandter et al. 1990*
Protein degradation of nitrogen- Protein Acid proteinase Bajwa et al. 1985; Leake and Read 1990b, 1991; Ryan and
containing polymers Alexander 1992; Chen et al. 1999*; Xiao and Berch 1999*
Organic phosphorus breakdown Acid phosphatase Lemoine et al. 1992
Phosphodiesterase Leake and Miles 1996; Myers and Leake 1996
*Results are based upon indirect method of observation, for example, presence of appropriate gene or growth promotion in test organism supplied with
substrate. For additional results of earlier studies see Leake and Read (1997).
centrations of the structural component of fungal walls, selves express considerable nutrient-mobilizing and
chitin, and that this compound, which contains approxi- decomposer activities in “self” substrates.
mately 40% N, would therefore represent a potentially sig- The importance of litter decomposability as a factor deter-
nificant source of the element in heathland ecosystems. It mining fitness of plants in their natural environments was
was confirmed that chitin did, indeed, represent a major po- recognized in the context of heathlands by Berendse (1994).
tential N source in heathland soils, and comparative analyses However, such studies have not envisaged the possibility that
of the abilities of mycorrhizal and nonmycorrhizal Vac- the fungal mutualists of the plants rather than an ill-defined
cinium plants to mobilize chitin N supplied in the form of group of “saprotrophs” may play a critical role in the partial
fungal cell walls showed that colonization by H. ericae con- decomposition and recycling of nutrients from litter of the
ferred access to the nutrient. Such results suggest that host plants. By facilitating such tightly coupled recovery of
mycorrhizal colonization of ericoid roots proliferating in the key nutrients from the otherwise recalcitrant residues of their
superficial horizons of heathland soils might indeed provide host plants, ERM fungi will contribute significantly to the
for effective recycling of the critical growth-limiting nutrient maintenance of dominance of their hosts in the community.
from fungal biomass. They can thus justifiably be seen as “drivers” in this type of
The residues of the ericaceous plants themselves will in- ecosystem.
evitably form a major component of heathland soil, particu-
larly in what are often pure stands of these dwarf shrubs. Ectomycorrhizas in boreal forest ecosystems
Kerley and Read (1998) investigated the extent to which the The nutrient-mobilizing capabilities of selected ECM
ERM system might be involved directly in mobilization of fungi typical of boreal forest habitats has also been investi-
N from such residues. They grew plants of Vaccinium gated in laboratory studies (Table 3). A major difference in
macrocarpon aseptically and, after killing their tissues by our perspective on this group of fungi compared to the ERM
drying, used the sterile necromass as a substrate containing must, however, arise from the fact that here we are dealing
the sole sources of N for a further set of plants grown in the with a much larger pool of species, most of which have not
mycorrhizal or nonmycorrhizal condition. It was shown that been cultured as of yet. Circumspection is therefore essential
after 60 d, more than 40% of the N contained in the necro- when drawing conclusions. In those species that have been
mass was released and assimilated by mycorrhizal Vaccin- cultured and exposed to analysis, a similar range of extra-
ium plants. Nonmycorrhizal plants, in contrast, recovered cellular enzyme activities as in ERM (Table 2) have been de-
less than 5% of the N from the equivalent substrates. Obvi- tected (Table 3), and the same conclusions might be drawn
ously, litters produced aseptically in this way are not a pre- as to the likely functions of the fungi in the ecosystem.
cise surrogate for those to be found in nature, but such Since, as pointed out previously, the dominant plants of the
experiments do provide evidence that ERM fungi can them- ericoid and boreal forest types of ecosystem often co-occur
© 2004 NRC CanadaRead et al. 1251
Table 3. Extracellular enzymes produced by selected ectomycorrhizal fungi, which would be expected to provide some abilities to
degrade structural components of plant litter, thereby affecting decomposition processes in boreal forest ecosystems processes by
“unmasking” of nutrients to facilitate attack upon nitrogen- (protein degradation) and phosphorus-containing (organic phosphorus)
polymers.
Process Substrate Enzyme Reference
Cuticle degradation Cutin, lipid, waxes Fatty acid esterase Hutchison 1990b*; Caldwell et al. 1991
Plant cell wall degradation Pectin Polygalacturonase Hutchison 1990b*
Cellulose Cellulase Maijala et al. 1991; Colpaert and van Laere 1996
Cellobiose Cellobiohydrolase Burke and Cairney 1998
Hemicellulose Xylanase Cao and Crawford 1993; Terashita et al. 1995; Cairney
and Burke 1996
Oxidation of phenolic acids Monophenols Tyrosinase Hutchison 1990b*
and tannins
Polyphenols Polyphenol oxidase Bending and Read 1997; Colpaert and van Laere 1996;
Günther et al. 1998
Peroxidase Bending and Read 1997; Cairney and Burke 1994;
Griffiths and Caldwell 1992
Laccase Hutchison 1990b*; Kanunfre and Zancan 1998
Hydrolysis of lignin Lignin Manganese peroxidase Chambers et al. 1999*
Protein degradation Acid proteinase Abuzinadah and Read 1986a, 1986b; El-Badaoui and
Botton 1989; Hutchison 1990a; Zhu et al. 1990;
Maijala et al. 1991 ; Finlay et al. 1992*; Griffiths
and Caldwell 1992; Ryan and Alexander 1992*;
Terashita et al. 1995; Tibbett et al. 1998b, 1999
Organic phosphorus Acid phosphatase Hilger and Krause 1989; Kropp 1990; Sen 1990*;
Kieliszewska-Rokicka 1992; Antibus et al. 1992;
Tibbett et al. 1998a
*Results are based upon indirect methods of observation, for example, gene presence or growth promotion in test organism supplied with substrate. For
additional older literature see Leake and Read (1997).
in the same or juxtaposed soil horizons, it would not be sur- upon autotrophic partners is a reflection of loss rather than
prising if selection had favoured fungal symbionts with sim- gain of the ability to survive in a saprotrophic mode.
ilar nutrient-mobilizing capabilities. As in the case of the ericoid systems, emphasis has re-
The abilities of selected boreal ECM fungi to perform cently been placed upon the ability of specific intact mycor-
decomposer functions should not, however, be exaggerated. rhizal partnerships to explore and exploit natural substrates
When comparisons are made either between this functional containing nutrients. On the basis that, as described before,
group and ericoid fungi (Bending and Read 1996a, 1996b) ECM roots and their extramatrical mycelial systems prolifer-
or saprotrophs (Maijala et al. 1991; Colpaert and van Laere ate preferentially in and immediately below the superficial
1996; Colpaert and van Tichelen 1996), the abilities of ECM organic horizons of boreal forests, Bending and Read
fungi to depolymerize complex carbon sources are invariably (1995a, 1995b) commenced investigations of their nutrient-
lower than those of the other groups. The failure of most mobilizing capabilities with the organic substrate that char-
ECM to penetrate host-plant cells may in part arise from acteristically dominates these horizons, that is, plant leaf
catabolite repression of cellulase production arising from the litter, with its associated microbial biomass. This was col-
large flux of glucose received from their hosts, but almost lected from the FH horizon and supplied as the only major
certainly reflects very limited cellulolytic activity in these potential source of N and P to mycorrhizal plants of the
fungi. Added to this must be the fact that a recent report of boreo-temperate forest tree Betula pendula colonized by
ligninolytic genes in ECM (Chen et al. 2001) has now been Paxillus involutus. This fungus is itself widely distributed in
retracted because of methodological flaws. There is no evi- boreal regions (Laiho,1970). It was subsequently confirmed
dence for expression of these genes in the mycorrhizal fungi (Perez-Moreno and Read 2000) that intensive exploitation of
tested (Cairney et al. 2003). Certainly the preferential the litter (Figs. 4a, 4c) by mycelia of the fungal symbiont
growth of mycorrhizal fungi and regenerating seedlings on, enabled significant reductions of its N and P contents rela-
or in association with, nurse logs (O’HanlonManners and tive to those seen in nonmycorrhizal plants and to concomi-
Kotanen 2004) or humified tree stumps (Dimbleby 1953) in tant increases in growth as well as N and P contents of the
boreal forest environments does not provide such evidence. colonized plants.
There is a remote possibility that some of the so-far un- A feature of the carbon balance of the residues of this at-
culturable species may have ligninolytic potential, but the tack, which is likely to be of significance at the ecosystem
likelihood would seem to be that their greater dependence level (see following text), was that their C/N ratios were sig-
© 2004 NRC Canada1252 Can. J. Bot. Vol. 82, 2004
Fig. 4. Colonization of organic natural substrates by the external ectomycorrhizal mycelium of Paxillus involutus growing from Betula
pendula roots. (a–b) Entire microcosms supporting mycorrhizal Betula plants showing extensive mycelial networks and selective ex-
ploitation of (a) fermentation-horizon materials (in square trays at base of microcosm) collected from birch (left), beech (centre), and
pine (right) forests and (b) necromass of nematodes (in central and right-hand trays only). (c) Close-up of a tray in a microcosm con-
taining birch fermentation-horizon material intensively colonized by ectomycorrhizal mycelium. (d) Close-up of the microcosm in
(b) showing selective mycelial colonization in the tray containing necromass of nematodes. Scale bars = 15 mm.
© 2004 NRC CanadaRead et al. 1253
nificantly increased as a result of the export of N by the col- In these circumstances the inherently large requirement of
onizing fungus. This suggests that the fungus was selectively ECM fungi for N would be expected to drive their scaveng-
exploiting N-containing polymers. The C/N ratios of boreal ing activities in the direction of N sources that are not co-
forest litter are known to decrease in the early stages of polymerized with other carbon-rich polymers. In boreal
decomposition after reaching the L layer, probably as a re- environments, which are so heavily loaded with phenolic
sult of exploitation of their carbon residues by the relatively residues, this essentially means attack upon N-enriched sub-
N-enriched mycelia of saprotrophic fungi (Berg and Staaf strates before their contents enter the immobilization pro-
1981). However, over a period during which the residues de- cesses. It therefore becomes important to ask what, if any,
scend into the FH layer, the saprotrophs will become carbon unprecipitated N sources might be accessible to these fungi.
limited and in this condition increasingly disadvantaged in A new generation of experiments has investigated the abil-
competing for N and P with the ECM fungi inhabiting this ity of selected ECM plant–fungal associations to mobilize
horizon. Bending and Read (1995a) proposed the progres- the N contained in defined substrates of low phenolic con-
sive N enrichment of FH residues as the key quality change tent that are likely to be of quantitative significance in boreal
that enabled them to become potentially important sources forest soils. Bearing in mind the disproportionately large
of N for the ECM fungi. amounts of N that are cycled through the ECM systems of
Koide and Wu (2003) buried residues of the L and F hori- boreal forests (Ruess et al. 2003; see preceding text), these
zons in a Pinus resinosa plantation and observed that the de- experiments have the potential to throw much light on a soil
crease of C/N ratio was still evident after 16 months of nutritional process that is fundamental to the success of
incubation. Clearly, the duration of the C/N shift pattern and these ecosystems. Ecologically relevant substrates used to
the stage at which the potential for N release is reached will date include residues of the ECM fungal mycelium itself
be influenced by local environmental factors. In their study, (Andersson et al. 1997), pollen (Perez-Moreno and Read
Koide and Wu emphasised the need to consider the poten- 2001a), and some quantitatively important representatives of
tially confounding effects of the removal of water from the the boreal forest soil mesofauna, namely nematodes (Perez-
substrates by mycorrhizal roots and mycelium. In the boreal Moreno and Read 2001b) and collembolans (Klironomos
forest context, it is indeed likely that the dynamics of de- and Hart 2001). In these experiments, N resources have been
composition and nutrient-abstraction processes will be dif- shown to be intensively exploited by the fungal symbionts,
ferent in potentially surface-dry, sandy podzols as compared with significant quantities of the critical element being
to those of wet, peaty soils. Whatever the local variations passed on to the host plant (Table 4).
may be, the fact remains that N removal from these residues The rapidity and effectiveness with which some ECM
does take place, as evidenced not only by microcosm studies fungi physically dominate and selectively exploit these nutri-
of the kinds described above but also by the extremely small tionally enriched organic resources is striking (Figs. 4b, 4d).
residual quantities of the element associated with the older The strategy of intensive early occupation of resources and
carbon of the humic and fulvic compounds that dominate the the localization of its expression in the superficial horizons
H horizons of boreal forest systems. of the soil may both have been selected as a result of the rel-
These observations leave us open to question the identities atively weak capability of these organisms to liberate N once
of the N-enriched substrates that are exploited by ECM it has been sequestered with phenolic compounds.
fungi in and around the FH layer. In view of the accumu- While a proteolytic capability can provide the key to ac-
lated evidence that organic N released into environments cessing primary sources of N, the rapid absorption of the
with boreal forest type soil is rapidly coprecipitated with products of proteolysis, which are amino acids or small pep-
polyphenolic materials (Handley 1954; Northup et al. 1995), tides (Read et al. 1989), remains a necessity if these are not
the issue of the extent to which these are accessible to ECM to be lost to assimilation and immobilization by saprobes.
fungi becomes important. All the laboratory observations Kinetic data have shown that both fungi (Chalot et al. 1994,
quoted above suggest that those symbionts that have so far 1995) and mycorrhizal roots (Kielland 1994; Wallenda and
been cultured do not, in contrast to their ERM counterparts, Read 1999; Wallenda et al. 2000) typical of those occurring
have access these resources. Recent studies by Wu et al. in boreal forest environments are able to take up amino acids
(2003) support those of Bending and Read (1996b) by indi- at rates significantly higher than those observed for NH4 and
cating that ECM fungi have a low ability to release N and P NO3. The uptake capacities (Vmax) and substrate affinities
from protein–tannin complexes, relative to those of sapro- (Km) observed in these studies indicate the potential for a
trophs. The dynamic interactions between the mycorrhizal substantial uptake of organic N from sites of mobilization.
and saprotrophic communities may therefore be crucial in When these kinetic data are considered in the light of the
forming nutrient cycling cascades of resource quality, since immense biomass and absorptive surface areas of ECM
nutrients acquired by saprotrophic fungal mycelium and bac- mycelium present in boreal and temperate forest soils (see
terial cells from the more recalcitrant sources may subse- Leake et al. 2004), then the full potential of the ECM system
quently become available to mycorrhizal fungi on the death to recover and recycle N in these environments can be ap-
of these other organisms. Direct antagonist effects of mycor- preciated.
rhizal mycelia on contact with saprotrophic mycelial sys- The validity of these laboratory-based observations was
tems (Leake et al. 2002) and transfers of nutrients acquired supported by Näsholm et al. (1998), who injected dual la-
by saprotrophic fungi into mycorrhizal mycelia (Lindahl et belled [13C, 15N]-glycine and 15N-labelled NH4 into the su-
al. 1999) suggest these kinds of interactions can directly af- perficial horizons of a boreal forest soil. Ratios of 13C/15N in
fect both the longevity and functioning of the saprotrophic the roots demonstrated that at least 40% of the N was ab-
communities. sorbed as intact glycine molecules in ECM roots of pine and
© 2004 NRC Canada1254 Can. J. Bot. Vol. 82, 2004
Table 4. Nutrient mobilization expressed as percent loss of nitrogen (N) and phosphorus (P) from different organic natural substrates
by ectomycorrhizal fungi grown in association with different host plants (bold characters) and in parallel controls with mycorrhizal
mycelium absent or very weakly developed.
Nutrient
mobilization
(%)
Type of substrate N P Time (d) Host plant – ectomycorrhizal fungus combination Reference
Plant detrital materials
Douglas-fir litter 32 33 365 Pseudotsuga menziesii – mats of Hysterangium Entry et al. 1991
setchellii
Douglas-fir litter 16 19 365 Control (no host plant) – mycorrhizal hyphal
mats absent
Pine FHM 23 22 120 Pinus sylvestris – Suillus bovinus Bending and Read 1995
Pine FHM 13 3 120 Pinus sylvestris – Thelephora terrestris
Pine FHM 5 0 120 Control (no host plant) – mycorrhizal fungus
absent
Birch FHM 0 40 90 Betula pendula – Paxillus involutus Perez-Moreno and Read 2000
Pine FHM 1 35 90 Betula pendula – Paxillus involutus
Beech FHM 14 37 90 Betula pendula – Paxillus involutus
Pine FHM 25 63 90 Betula pendula – Pinus sylvestris linked by J. Perez-Moreno and D.J. Read
Paxillus involutus (unpublished data)
Pine FHM 25 54 90 Betula pendula – Pinus sylvestris linked by
Paxillus involutus
Pollen
Pine pollen 76 97 115 Betula pendula – Paxillus involutus Perez-Moreno and Read 2001
Pine pollen 42 35 115 Control (nonmycorrhizal plant) – mycorrhizal
fungus absent
Soil animals
Nematodes 68 65 150 Betula pendula – Paxillus involutus Perez-Moreno and Read 2001
Nematodes 37 25 150 Control (nonmycorrhizal plant) – mycorrhizal Perez-Moreno and Read 2001
fungus absent
Note: FMH, fermentation-horizon material.
spruce. In their study, Näsholm et al. (1998) observed that Over much of the boreal zone, release of “available N” is so
glycine was also taken up by the putatively AM grass restricted as to be undetectable (Persson et al. 2000). Under
Deschampsia flexuosa and cautioned against making rigid these circumstances the abilities of significant numbers
separation between ECM and AM as functional groups on of ECM fungi to depolymerize complex N sources and to
the basis of their differing abilities to use organic N. Previ- efficiently capture the released products will be of key
ous studies of the nonmycorrhizal arctic sedge Eriophorum importance in what are otherwise typically N-starved envi-
vaginatum (Chapin et al. 1993) had also revealed an ability ronments. By facilitating access to the key fitness-limiting
to use simple organic N sources. However, as pointed out element this group of fungi can, as in the case of their ERM
elsewhere (Read and Perez-Moreno 2003), the crucial dis- counterparts, be regarded as drivers of a pivotal ecosystem
tinction between these functional groups lies in the fact that process.
plants that are associated with ECM (and ERM) fungi will
alone have direct access to the primary sources of the amino Experiments on N source preferences of ERM
acids through the proteolytic activities of their fungal part- (Vaccinium macrocarpon) and ECM (Betula pendula)
ners. The propensity of would-be competitors to assimilate While organic sources of N are quantitatively the most
the products of proteolysis may have been one of the factors important potential source of the element over much of the
that has driven the strategy of intensive substrate occupation tundra, taiga, and boreal zones, mineral forms may be pres-
by ECM fungi revealed in microcosm studies and also seen ent, even if only at low concentrations, particularly in more
in mycelial-mat formation in the FH horizons of boreal for- southerly latitudes (Fig. 7). In pristine northern habitats,
est soils. mineral N, where present, occurs almost exclusively in the
It can be concluded from studies of ECM fungi carried form of ammonium ions (NH4+). In some areas, particularly
out so far that this group is likely to be less active in soil those subject to anthropogenic pollution, NO3– ions can also
decomposition processes than is their ERM counterpart. be present. While the propensity of ammonium and nitrate
However, it may be wrong to conclude, as did Schimel and ions to inhibit uptake of amino compounds by ECM fungi
Bennett (2004) in a recent review, that “in non-ericaceous (Chalot et al. 1994, 1995) and ECM roots (Wallenda et al.
systems, direct decomposition and nutrient uptake may be a 2000) has been found to be low, these studies considered
secondary function to competition for already available N”. only the impacts of one ion upon the uptake of another and
© 2004 NRC CanadaRead et al. 1255
did not address the issue of preference. The occurrence of Fig. 5. Residual nitrogen (N) concentrations in media supporting
selective patterns of N uptake would be of significance not the growth of mycorrhizal (top) and nonmycorrhizal (bottom)
only for mycorrhizal plants themselves, but also, because of plants of Vaccinium macrocarpon supplied at time zero with ni-
their impact upon the availability of substrates for mineral- trate (KNO3) and glutamic acid as a mixture of the two sources,
ization, they would influence the N-cycling dynamics of the equimolar for N, each at a concentration of 15 µg N/mL.
ecosystem as a whole. Subsamples of medium were removed from each of four repli-
Experiments have now been carried out in which plants cate cultures at 4-d intervals over 20 d for analysis. Vertical bars
representative of heathland and boreal forest biomes, Vac- represent SE of the means. Asterisks indicate significant differ-
cinium macrocarpon and Betula pendula, respectively, have ence between treatments at p = 0.05.
been exposed in the mycorrhizal and nonmycorrhizal condi-
tions to simple mixtures of mineral and amino N, with a
view to determining patterns of uptake.
In the first study (J. Perez-Moreno, A. Moghadem, and
D.J. Read, unpublished data), plants of V. macrocarpon were
grown either in the mycorrhizal condition with H. ericae or
axenically in mixtures, equimolar for N, of nitrate (KNO3)
and the amino compound glutamic acid (GA). In the second
(J. Perez-Moreno and D.J. Read, unpublished data),
B. pendula was grown either ectomycorrhizal with Paxillus
involutus as the fungal symbiont or axenically and was ex-
posed to mixtures of ammonium (NH4)2SO4 and GA. The
former design was selected to simulate the impacts upon
organic N assimilation of anthropogenic mineral N deposi-
tions, which occur mostly in the form of NO3 and have dev-
astated heathlands in lowland Europe (Aerts 2002), while
the latter was considered to represent the more pristine bo-
real environments in which, where mineralization occurs,
NH4 is the predominant form of N. Studies of the “free”
amino acid composition of heathland (Abuarghub and Read
1988) and shrub tundra (Kielland 1995) soils indicate that
GA is consistently present as a major component of the sim-
ple organic N pool.
Vaccinium macrocarpon failed to assimilate NO3 when
grown in either the mycorrhizal or nonmycorrhizal condition
(Fig. 5). In contrast, when in the mycorrhizal as distinct
from the nonmycorrhizal condition these plants were able
readily to assimilate GA, irrespective of the presence of the
NO3 ion. These results confirm the preference of this ERM
plant for simple organic N forms and indicate that the NO3
ion, whether occurring in soil solution as a result of natural
processes of nitrification, or through anthropogenic deposi-
tion, is likely, in an organic soil environment, to be relatively
little used by these plants. The consequence, in the event of
either scenario, would be N potentially becoming available
to plants that readily use NO3–-N and which are normally
excluded from heathlands by the absence of available min-
eral N.
The pattern observed in the case of B. pendula was essen-
tially similar with respect to the strong preference being
shown for GA over the mineral-N source in the mycorrhizal
condition (Fig. 6). ECM colonization by Paxillus involutus organic forms of N, they can readily switch to NH4+-N use if
facilitated a rapid assimilation of GA, while the NH4+ ion the former become exhausted (Read et al. 1989).
was not utilized. In the nonmycorrhizal condition, except at The results of the preference experiments are likely to be
the final harvest, assimilation rates of both ions were slow, of broader significance for the N cycle in these types of eco-
and there were no significant differences in utilization be- system. If, as seems likely from studies of the kinetics of up-
tween the sources. take of amino compounds in excised ECM roots of boreal
It cannot be concluded from either of these experiments forest plants (Kielland 1994; Wallenda and Read 1999), the
that the plants will necessarily fail to use the mineral ions rapid and selective uptake of GA indicates a constitutive
when they are present as sole N sources. Indeed, studies of preference and affinity for amino-acid N sources, the effect
ECM fungi growing in pure culture over longer time inter- will strongly be to reduce the flow of organic N substrates
vals indicate that while they preferentially assimilate simple into the mineralization process, a feature that will perpetuate
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