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Research review
Blackwell Science Ltd

Community ecology of ectomycorrhizal

fungi: an advancing interdisciplinary field

Author for correspondence: Anders Dahlberg

Tel: + 46 (0) 18 67 27 94
Department of Forest Mycology and Pathology, PO Box 7026, Swedish University of Agricultural
Fax: + 46 (0) 18 30 92 45
Email: Anders.dahlberg@ mykopat.slu.se Sciences, S-750 07 Uppsala, SWEDEN

Received: 13 December 2000

Accepted: 16 February 2001

Summary

Key words: ectomycorrhizal A long-term goal of community ecology is to identify spatial and temporal factors
community ecology, mycorrhizas, plant that underlie observed community structures. Ultimately, ecologists seek to relate
ecology, ecosystem processes. community patterns to ecosystem processes and functions. Since the mid 1990s,
ectomycorrhizal (ECM) research has been equipped with tools to identify and fully
quantify the taxonomic diversity in below-ground ECM fungal communities in detail
and address such questions. Many of the most important functions of terrestrial ecosystems,
as well as interactions, between plants take place below ground and mycorrhizal fungi
are among the key players in soil ecology. Here the rapidly increasing knowledge of
ECM fungal community ecology is reviewed and the prospects discussed for elucidating
processes that structure ECM fungal communities and the way in which such knowledge
might be integrated with, and advance, the understanding of plant ecology and
ecosystem processes.

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membrane interfaces, within chloroplasts mitochondria

Introduction and root-fungal organs, the mycorrhizas. Effective membrane
Mutualistic associations between organisms, which reciprocally surface area is significantly increased through invagination
increase the fitness of both partners, have been a significant driving and external enlargement, and in the case of the mycorrhizal
force in the course of evolution. The importance of endosymbiotic interface, this has critical implications for efficient root uptake
associations between different procaryotes in the evolution of water and nutrients. Through these symbioses plants have
of eucaryotic cells is now firmly established and there is also succeeded in colonizing all terrestrial biomes (Blackwell, 2000)
increasing recognition that symbiosis at the level of more and consequently, plant-communities are the template for
complex organisms is the rule, rather than the exception (Smith these terrestrial communities of microorganisms. In a strikingly
& Douglas, 1987). An ancient and ecologically important similar manner to the well-being of humans and animals
example is the mycorrhizal symbiosis between vascular plants that is intimately linked to community composition of gut
and soil fungi dating back to the first land plants (Blackwell, bacteria, so also is the functioning of plants closely dependent
2000). However, despite major advances in our understanding upon the composition and activities of their below-ground
of mycorrhizas, the extent and significance of mycorrhizal root mycorrhizal associates.
symbioses remains greatly underrated in plant ecology. In fact, World-wide patterns and regulation of plant species rich-
vascular plants can be regarded as successful entrepreneurs ness and their impacts on ecosystem processes have long been of
that have benefited from symbiotic association with procaryotes interest, but less is known about the diversity, its regulation and
and later fungi to form energy and nutrient transferring biological functional importance of mycorrhizal fungi (Molina et al., 1992).

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While a relatively small number of plants, c. 8000, form ecto-

mycorrhiza (ECM), their global importance is greatly increased
Standing mass and identification of mycorrhizas
by their disproportionate occupancy of terrestrial ecosystems. Within days of emergence, almost every fine root of an
Many trees, such as those in the Betulaceae, Pinaceae, Fagaceae, ectomycorrhizal plant is colonized by mycorrhizal fungi
and Dipterocaraceae are important and obligate ECM plants, (Smith & Read, 1997; Taylor et al., 2000). The number of the
forming vast boreal, temperate and subtropical forests (Smith mycorrhizal tips, commonly a few mm in length, is often very
& Read, 1997). A conservative estimate of the number of ECM high; in boreal forests the numbers typically range between
fungal species in the world is approaching 6000 (Molina et al., 104 and 5 × 105 m–2 forest floor, a figure that in Norway spruce
1992). Beside the diversity of known taxa, there are other ECM forests roughly corresponds to the number of green needles
fungi which do not produce conspicuous reproductive structures, (Dahlberg et al., 1997). Mycorrhizas are short-lived structures,
a feature that precludes their inclusion in known listings, and still being regenerated on a yearly basis. Regeneration may occur
further, a huge number of fungal taxa remain to be discovered. throughout the growing season, but peaks at certain periods.
Until the middle of the 1990s, knowledge of ECM fungal Mycorrhizas are vertically distributed to depths occupied by
community structure, and the degree to which species assem- host tree roots (i.e. down to several meters). However, the
blages show predictable colonization patterns in space and overwhelming majority are located in surface soil layers (e.g.
time, was almost exclusively based on sporocarp surveys. A at the interface of organic matter and mineral soil) where
major advantage of such surveys is the potential to record and mineralization processes are most active. In dry forest eco-
identify all fruiting ECM fungi within an area with relatively systems, mycorrhizas are located deeper in the mineral soil
little work load. However, because of the importance of than their mesic counterparts (Visser, 1995; Taylor & Bruns,
exogenous environmental factors in triggering fruiting, and the 1999). Typically up to 90% of the mycorrhizas are located
consequent irregularity of reproduction, such characterization within the upper 10 cm of the soil profile in boreal soils,
requires long-term monitoring. Moreover, even after decades mainly associated with the thick organic humus or mor layer.
of surveying, additional fungal species may still appear. Even Fungal tissue in mycorrhizal roots have fungal biomass that
more alarmingly, recent demonstrations of the poor corres- is 10–100 times higher than that in the sporocarps, even
pondence between the species composition of sporocarps and without considering the often extensive extramatrical mycelia
fungi colonizing roots raises some concern about the validity (Dahlberg et al., 1997).
of sporocarp survey data. It was, for example, observed that One well-developed approach to identify ECM fungi
whereas the most common sporocarps in a jack pine stand colonizing roots involves detailed morphological and struct-
were those of Suillus tomentosum, the mycorrhizas identified ural descriptions of mycorrhizas – morphotyping (Agerer,
by distinct morphology rarely constituted more than 5% of 1987–1999). In certain cases, morphology of mycorrhizas is
the total mycorrhizas (Danielson, 1984). species-specific and allows unambiguous identification of
During the past decade major advances in molecular biology mycorrhizas collected in the field (e.g. Smith et al., 2000). More
and morphotyping have made it possible to identify myco- generally, this approach only allows grouping into mycor-
bionts from single mm-sized mycorrhizas, enabling monitoring rhizal morphotypes, which do not represent single species.
and spatiotemporal analysis of below-ground ECM fungal However, the most significant methodological advance has
communities (Horton & Bruns, 2001). Thereby, many diversity been the application of high-resolution molecular tools that
and functional properties of ECM communities be integrated allow identification of individual mycorrhizas (Gardes &
and their key contributions related to the overall diversity and Bruns, 1993; Horton & Bruns, 2001). These methods offer
ecosystem processes, an area of growing interest in terrestrial three advantages over morphological methods: they can be
ecology (Copley, 2000). Examples of such recent break-through directed at any taxonomic level or to detect genotypes; they
achievements are demonstrations of significant net transfer of require less time to learn, and are clearly described; and they
nutrients and carbon between different plant taxa through are fully reproducible in time and space. Fungal, or plant
common mycorrhizal mycelia (Simard et al., 1997) and the DNA can be selectively amplified from mixtures of plant and
implication that richness and composition of arbuscular fungal DNA from single mycorrhizas and, with subsequent
mycorrhizal fungi affect diversity and growth of plants (van analysis, species identified (Gardes & Bruns, 1993; Horton &
der Heijden et al., 1998). Bruns, 1998). The internal transcribed spacer (ITS) region in
Here, I briefly discuss the current potential for terrestrial the nuclear ribosomal unit is frequently sequenced, digested
ecologists to identify and quantify ECM fungal communities. with restriction enzymes and resulting restriction fragment
In doing this I provide: an overview of mycorrhizal distribu- length polymorphism analysed (Gardes & Bruns, 1996; Kårén
tions in soils and methods to identify mycobionts in single et al., 1997; Peter et al., 2000). ITS nucleotide databases are
mycorrhizas; a description of recent findings in spatiotemporal also being constructed for certain ECM fungal groups for
characteristics of ECM fungal communities; and a discussion identification and phylogenetic purposes allowing for direct
of how such an appreciation may advance the understanding sequence comparison; particularly informative is the 5′ end of
of plant ecology and ecosystem processes. the LSU gene (Kõljalg et al., 2000; Moncalvo et al., 2000).

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Table 1 A compilation of the three most abundant or frequent ectomycorrhizal (ECM fungal taxa, as recorded from mycorrhizas, in 49 ECM
fungal community studies published so far. Only studies where the taxonomic identity of at least one of the three most abundant taxa was
certified are included. Figures indicate at how many studies certain taxa dominated. The data from Canada includes four assessments of ECM
communities on seedlings. Besides 21 papers referred to in the present review paper, 28 additional studies are included

Number of studies with dominance of the following taxa

Sporocarps lacking or Sporocarps lacking

nonconspiceous Conspicous sporocarps or nonconspiceous

Total no Cenococcum Corticea- Thelephor- Suilloid (incl Cortinaria- MRA

Forest type Country of studies geophilum ceae aceae Rhizopogon) Russulales ceae E-strain Risseia

Coniferous forest
Boreal Canada 15 10 7 3 4 4 1 9
Sweden 12 6 12 3 2 2 1 1

Temperate Switzerland 3 1 3 3 1
& Germany
USA 15 4 7 8 7

Deciduous forests
USA 1 1
Germany 1 1
Netherlands 1 1

Rainforest
Indonesia 1 1

In total: 49 22 22 17 14 14 3 10 1

Sequence data in the ML5/ML6 region of the mitochondrial ground mycorrhizal networks. Thelephoraceae, Russulaceae and,
LrDNA representing all major ECM basidiomycete genera is at least in post fire settings, also suilloid fungi repeatedly emerge
established (Bruns et al., 1998). Thus, any single mycorrhiza as the most frequent or abundant mycorrhizas in forests of
can potentially be identified to species either by ITS-RFLP western USA, whereas Corticeaceous fungi and Cenococcum
comparison with reference material or by sequence comparison geophilum, followed by Russulaceae and Thelephoraceae appear
narrowed down to smaller subsets of putative species affinity as the most common in boreal forests (Table 1).
that ultimately, with supplementation of appropriate references, The general rule is that a few fungal ECM taxa account for the
will be identified. most, (> 50%), of the mycorrhizal abundance and are widely
Slightly more than 50 such ECM community studies have spread whereas the majority of species are only rarely encoun-
been published in the period between 1996 and late 2000, few tered (Gehring et al., 1998; Jonsson et al., 1999a,b; Peter et al.,
before (cf. Horton & Bruns, 2001; cf. Table 1). Two thirds of 2000; Stendell et al., 1999; Grogan et al., 2000). In two
these have been based on morphotyping and one third on stands of Douglas-fir, 69 morphotypes were recognized from
molecular methods, sometimes with morphotyping-based 17 500 assessed mycorrhizas; most types were rare, 19 types
stratification as a powerful approach (Jonsson et al., 1999a). colonized > 1% of the mycorrhizas and 9 types colonized
together 67% (Goodman & Trofymow, 1998a). This pattern
of dominance of a few species and rarity of most others is a com-
Characteristics of ECM communities
mon community pattern of any taxonomic group of organisms.
Studies from North America and Europe unanimously confirm Major determinants of the composition of ECM fungal
that fungi that do not form obvious fruiting structures form the community are host plant composition ( Molina et al., 1992)
major mycorrhizal abundance. Fruiting species merely constitute and edaphic factors (Gehring et al., 1998; Kernaghan & Harper,
20–30% of the mycorrhizas (e.g. Gardes & Bruns, 1996; Jonsson 2001). Within local forests, the spatial variation of ECM fungi
et al., 1999a; Fig. 1). Apparently, carbon budget or resource alloca- is very high and most species show aggregated distributions
tion to production of sporocarps vs mycorrhizas and mycelial (Gardes & Bruns, 1996; Kranabetter & Wylie, 1998; Bidartondo
growth vary among species, as discussed in Gardes & Bruns et al., 2000). A study of pinyon trees showed one or a few ECM
(1996) seminal community paper. Typically, certain species fungal taxa to dominate single trees, and the dominant fungi
that commonly form mycorrhizas are poorly or nonrepresented varied between trees (Gehring et al., 1998). Spatial variation
in the above-ground fruiting record, and commonly fruiting spe- was concluded to have a larger effect on ECM fungal species
cies may conversely have only a limited representation in below- composition, than that caused by low intensity wildfire, the

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major natural disturbance in Swedish boreal forests (Jonsson and the mycorrhizas, and the temperature and humidity of
et al., 1999a). One exception is reported in a study of 1000- the soil. This certainly affects the patterns of fruiting. However,
yr-old bristlecone pine stands at high elevation in California; a detailed molecular study of mycorrhizas in a Swiss Norway
here one ECM Pyronemataceae sp. was consistently present as spruce forest conducted over three years showed a striking
inoculum in soil at all forest sites (Bidartondo et al., 2001). similarity in abundance of the 10 most abundant taxa (Peter
Commonly, small volumes of soil contain several ECM species, et al., 2001).
for example single four year old seedlings were colonized by Processes in ECM fungal populations underlie ECM fungal
up to 11 ECM fungi (Kranabetter & Wylie, 1998). Certain community patterns and thus, a knowledge of the ability of
taxa also appear to grow better in either the organic or mineral individual ECM fungal species to bridge distances in time and
layer (cf. Goodman & Trofymow, 1998). space is central to the understanding of ECM community
A significant step forward in understanding ECM fungal structure. However, little is known about the relative impor-
community structure is to establish studies that allow estimation tance of mycelial spread and longevity vs novel colonization
of the relative importance of different mechanisms that create from spores for any ECM fungal species. From the nearly 20
this diversity, and take into consideration spatial and temporal studies of ECM fungal population structures conducted so far
scales. Hypotheses to explore can be placed in two categories: (cf Redecker et al., 2001), it is apparent that genets in some
those based on niche differentiation between coexisting species; species are numerous, short-lived (1–2 yr) and small (< few
and, paradoxically, those based on similarities in competitive m, i.e. Hebeloma cylindrosporum, Laccaria amethystina, Amanita
ability, that is nonequilibrium models. An example of the franchetii, Russula cremoricolor). Other species may have few
former is the intermediate disturbance hypothesis stating that and due to persistence (decades to centuries) and mycelial
a disturbance leads to a predictable sequence of species repla- spread, relatively large genets (20–40 m in diameter, i.e.
cing each other. An intermediate range of disturbance would Suillus spp. and Cortinarius. Small genets may suggest colon-
allow a range of species traits, early to late successional species, ization from recent meiospores, whereas fewer, larger genets
to coexist and lead to a high species richness. The latter assumes indicate old mycelial structures, that have grown from a point
elements of stochasticity which enhance coexistence: so called source over decades. The latter are often found in old forests
lottery models state that due to poor dispersal ability, low (Fig. 1). Some studies suggest mycelial colonization as the
local abundance and chance events, species may be absent in primary avenue of ECM fungal colonization in mature un-
a neighbourhood and their abundance recruitment may thus disturbed forests, i.e. that clonal traits are of higher fitness
be limited. Therefore the best competitor that happens to than sexual traits under undisturbed conditions (e.g. Jonsson
colonize a particular local site may well be inferior on a larger et al., 1999b; Kranabetter et al., 1999). Resistant ECM fungal
scale. Potentially, this can lead to unlimited species richness. propagules also persist, probably in the mineral soil, after major
disturbances such as stand replacing wildfires (Baar et al., 1999).
Exceptions do occur, for example L. amethystina appear to
Temporal dynamics of ECM communities
be short-lived in old beech forests (Gherbi et al., 1999).
Successional changes in primary vegetation successions, and Demographic patterns in ECM fungi, or any soil dwelling
thus of primary ECM fungal colonization, are described from fungus, have still not been explored.
glacial retreats and farmlands. Such questions have been studied There is a need to launch studies of regional scale dynamics
in the course of natural secondary forest succession in a few of ECM fungal populations, and communities, to elucidate
cases. It must be remembered that forest management procedures, important population processes. There is also a need to deter-
such as clearcutting, impose novel selection pressure upon ECM mine which models are most applicable for different ECM fungi:
fungi. Marked changes in ECM community composition occur theories of remnant population dynamics with discontinuous,
after intense, stand replacing fire that totally consumes the nonequalibrium conditions and a pervasive impact of ‘accidents
organic layer, a natural occurrence in certain forest ecosystems of history’ or, on the other hand, meta-population models
( Visser, 1995; Grogan et al., 2000). However, in low intensity with continuous, equilibrium conditions and without historic
fires, where part of the organic layer remains unburnt and a dimensions (cf. Eriksson, 1996).
large proportion of trees survive the fire, the legacy of ECM
fungi appears large (Jonsson et al., 1999a). Short-term variation
in abundance of certain taxa of mycorrhizas may occur, but as
Interactions with plant communities
yet has been poorly investigated, as weather conditions affect Most ECM fungal species typically have broad, but differing,
photosynthesis and thereby allocation of assimilates to the roots, plant host ranges. They may form mycorrhizas with any ECM

Fig. 1 (opposite) Late successional Scots pine stands, in northern Sweden, where both ectomycorrhizal fungal community structure from
sporocarps and mycorrhizas, and fungal population structure of Suillus variegatus have been analysed. The last major disturbance was a forest
fire in 1647. The relative proportion of mass in sporocarps (open red bars, 34 taxa) and of mycorrhizal abundance (closed blue bars, 24 taxa,
distinguished by ITS-RFLP) is shown (Jonsson et al., 1999b). At the same site the spatial distribution Suillus variegatus genets was monitored
from sporocarps analysed by somatic incompatibility reactions (from Dahlberg (1997), with permission).

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angiosperm or gymnosperm or only with angiosperms or gym-

nosperms, or a single family of hosts. This potentially extensive,
but importantly sometimes also limited, linking of ECM plants
via intra- and interspecific ECM mycelia, within and between
species, may have major consequences for our understanding
of plant community characteristics, plant competitive interac-
tions and performance ( Molina et al., 1992). These linkages
potentially allow for nutrient and carbon transfer between
tree species, but their significance in nature remains to be
settled. Evidence for the potential of such mycelial linkages is
accumulating. Field and laboratory soil bioassays showed
Douglas fir to share ECM fungi and potentially form hyphal
links with several other plant species (Massicotte et al., 1999).
Jones et al. (1997) found that 91% of paper birch and 56%
of Douglas fir intermingled mycorrhizal roots examined were
colonized by the same mycorrhizal fungi. In these tree species,
Fig. 2 Diversity and ecosystem function have no direct relationships
a 4–7% net transfer of isotopically labelled carbon from to each other, but are both functions of the presence and activities
birch to Douglas fir has been demonstrated, which may be of individual species or functional groups and their interactions. The
ecologically significant (Simard et al., 1997). If net transfer is environment affects species, and the outcome of their interactions,
predominantly from pioneer plant species to late successional but not diversity or ecosystem processes directly. The question mark
species, ECM fungi may be an important contributing factor indicates the question as to whether diversity and ecosystem
processes are related (redrawn from Bengtsson, 1998).
determining plant community development.
In a mixed stand of bishop pine and Douglas fir the majority
of identified mycobionts were associated with both hosts, even
within small soil volumes, suggesting that individual fungal dynamics, and implications for ecological functions, have
genotypes linked the putatively competing tree hosts (Horton rarely been addressed under controlled experimental conditions
& Bruns, 1998). One study in the Canadian Rockies recorded (Lilleskov & Bruns, 2001). It is likely that many ECM fungi
all present ECM fungi to form mycorrhizas with both Dryas and may fulfil similar ecological functions and that a degree of
Salix (Kernaghan & Harper, 2001). In a comparison between functional redundancy exists in ECM fungal communities. In
seedlings of lodgepole pine, white spruce and subalpine fir an experiment on the effect of plant litter composition, there
seedlings, 43 of 74 mycorrhizal morphotypes were shared was no evidence that the composition of the present ECM fungi
by all conifers, constituting 52% of the total mycorrhizal affected the performance of seedlings (Nilsson et al., 1999).
abundance (Kranabetter et al., 1999). However, it is also Given their taxonomic diversity, communities are still likely
important to appreciate certain ECM fungi, for example to retain vast amounts of functional heterogeneity. Yet it is
suilloid fungi, as rigidly restricted to certain plant taxa and difficult to generalize about the ecological functionality of ECM
thus only potentially linking intraspecific plants. communities because relatively few investigations of ECM
Ericoid and ectomycorrhizal plants often coexist in boreal and fungal physiology have been conducted with more than a few
Mediterranean forests and are normally considered as separate isolates, and those typically include only a handful of taxa that
mycorrhizal systems with mycobionts of different taxonomic typically occur in low abundance (Cairney, 1999). The potential
affinity. However, recently an ericoid mycorrhizal fungus was relationship between ECM fungal species richness and ecosystem
shown to associate with Quercus roots (Bergero et al., 2000). The productivity has once been explored without finding any
possibility that some sharing may occur between ericaceous correlation (Gehring et al., 1998). As debated at length, there
plants and ECM trees has been discussed, but questions concerning is no mechanistic relationship between species richness, or any
whether it occurs and what possible ecological significance it diversity measure, and ecosystem function (Bengtsson, 1998).
may have still need to be answered in appropriate, controlled Probably, it is more vital to understand linkages between the
studies. The results of such experiments may have important actions of key species or functional groups and ecological
implications for our understanding of interactions between functions, as diversity is an abstract aggregated property of
trees and the understorey. species in the context of communities or ecosystems (Fig. 2).
The functioning of terrestrial ecosystems seems to depend heavily
on soil biodiversity. We now have the potential to address and
Effects on ecosystem function
experimentally test questions of ecological significance, as
To date, ECM fungal community studies have been mainly of abundant ECM fungi, potentially being key species, can be
a descriptive or correlative nature and few experimental studies identified. One approach could be to use A set of ECM fungi
have been performed. Causal mechanisms underlying the from selected environmental settings, and to investigate whether

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the abilities of these ECM fungal communities differ for fungi in an old Norway spruce forest in south Sweden. Canadian Journal
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Danielson RM. 1984. Ectomycorrhizal associations in jack pine stands in
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