CMU. Journal (2002) Vol.

1(1) 47

Role of Mycorrhizal Fungi in Ecosystems

Bernie Dell1
1
School of Biological Sciences and Biotechnology, Murdoch University, Perth, Western Australia
6150. E-mail: [email protected]

INTRODUCTION
Most land plants form associations with mycorrhizal fungi. Mycorrhizas are
mutualistic associations between fungi and plant roots. They are described as symbiotic
because the fungus receives photosynthetically derived carbon compounds and the plant
has increased access to mineral nutrients and sometimes water. The two most common
associations are the arbuscular endomycorrhizas (AM) formed by Zygomycete fungi, and
the ectomycorrhizas (ECM) formed by Basidiomycetes, Ascomycetes, and a few
Zygomycetes. Other mycorrhizal associations include the orchid, ericoid, arbutoid,
monotropoid and ectendo- mycorrhizas (Brundrett et al., 1996).
Mycorrhizal associations predominate in most natural terrestrial ecosystems
(Brundrett, 1991). Whereas the AM fungi are widespread geographically and have a very
extensive host range, the ECM fungi are more restricted, forming associations
predominantly with genera of important woody plants. Nevertheless, ECM fungi are
dominant components of the ground-dwelling macro-fungi in ecosystems where members
of the following plant families abound: Betulaceae, Dipterocarpaceae, Fagaceae,
Myrtaceae, Pinaceae, Ulmaceae, Salicaceae. ECM fungi are common in tropical forests of
Asia but are uncommon in many forests in Africa and South America. In Asia, the number
of host species tends to increase with altitude and at higher latitudes.

BENEFITS TO PLANTS
Supply of inorganic mineral nutrients
Many thousands of experiments have shown that mycorrhizal fungi can
overcome nutrient limitation to plant growth by enhancing nutrient acquisition, especially
phosphorus (Marschner and Dell, 1994; Clark and Zeto, 2000). Most studies have
investigated P, but mycorrhizas have been implicated in the uptake of most essential
nutrients. A notable exception is the element boron which is often the main micronutrient
limiting growth in SE Asia (Dell and Malajczuk, 1994).
The main mechanisms for an increase in inorganic nutrient uptake in mycorrhizal
plants are:
• The large surface area for nutrient acquisition provided by the fungal hyphae
external to the root compared to uninfected roots. A high proportion of
ECMs
are located in soil pores (Babel, 1987) from where hyphae radiate out into
soil particles. The aerobic environment of such pores facilitates nutrient
transfer from the fungal sheath to the root (Harley et al., 1953). As the fungal
mycelium grows through soil, it scavenges for mineral nutrients and is able to
48 CMU. Journal (2002) Vol. 1(1)

make contact with uninfected roots, sometimes of different host species. The
ratio of length of hyphae to root length has been measured in the range 300 to
over 8,000 (Read and Boyd, 1986; Jones et al., 1990). Expressed per unit of
soil volume, values of 16 to 2,000 m hyphae/cm3 have been measured in
plantations and forests (Read and Boyd, 1986; Pampolina et al., 2001).
• The small hyphal diameters compared to roots which allows penetration into
some crystalline minerals, aggregates and organic matter, with smaller pores
than could be exploited by roots alone.
• The secretion of enzymes capable of solubilising otherwise unavailable forms
of phosphate (Joner and Johansen, 2000).
Nutrient uptake sites in AM hyphae are discussed by Bago (2000).
There is good evidence that some inorganic and organic nutrients may pass via
the mycelia network from one host plant to another, but the significance of this has not
been adequately quantified in the field.

Supply of organic mineral nutrients

Although many mycorrhizal fungi can access inorganic forms of N (Chalot and
Brun, 1998) and P (Koide and Kabir, 2000), the relative importance of these modes of
nutrition have yet to be quantified in the field. Some litter-inhabiting ECM fungi produce
proteases and distribute soluble amino compounds through hyphal networks into the root
(Read et al., 1989). Recently, Glomus has been shown to transport the amino acids glycine
and glutamine into wheat (Hawkins et al., 2000).

Water
Ectomycorrhizal tree seedlings can often resist drought better than non-
mycorrhizal seedlings (Bowen, 1973). Several studies indicate that Rhizopogon can help
plants to tolerate and recover from water deficits and this can aid seedling establishment.
Plants colonised by AM fungi may have increased tolerance to drought. In flax (Linum
usitatissimum), AM mycorrhizal plants had lowered sensitivity to stress, higher
assimilation combined with lower increase of transpiration, and enhanced root
conductance (Vonreichenbach and Schonbeck, 1995). Unlike for AMs, large mycelial
strands of ECM fungi may increase water flow by bridging the gap between the soil and
the root (Lamhamedi et al., 1992).

Antagonism of parasitic organisms

There are many claims that mycorrhizal plants are more resistant to disease from
pathogenic fungi and bacteria than nonmycorrhizal plants. In particular, mycorrhizal fungi
can provide some protection against root invading primary pathogens (Schonbeck, 1979;
Duchesne et al., 1989). Some examples for woody species include [host/pathogen/
mycorrhizal fungus(i)]: Castanea/Phytophthora/Laccaria, Hebeloma, Paxillus (Brazanti
et al., 1999); Picea/ Cylindrocladium/Paxillus (Morin et al., 1999); Pinus/Fusarium/
Paxillus (Chakravarty et al., 1991; Farquhar and Peterson, 1991); Pinus/Phytophthora/
Pisolithus (Marx, 1973; Barham et al., 1974); and Pseudotsuga/Fusarium/Laccaria
(Sylvia and Sinclair, 1983). However, rarely is complete protection provided. Unlike in
pines where the fine roots near the soil surface are usually all ensheathed by ECM fungi,
 CMU. Journal (2002) Vol. 1(1) 49

the feeder root system of many broadleaf trees contains a mixture of nonmycorrhizal and
mycorrhizal short roots. Whilst the mechanisms of disease suppression remain unclear, it
has been surmised that the fungal mantle in ECMs provides a physical barrier to pathogen
ingress. Other proposed mechanisms include the production of antibiotic or antifungal
compounds by mycorrhizal fungi, and the activation of plant defence genes.
Further, mycorrhizal plants may be less impacted by pathogenic nematodes than
nonmycorrhizal plants (Smith, 1987; Pinochet et al., 1996), probably because they are
better able to maintain a water and nutrient absorbing surface in infected soil. However,
further work is needed as Ryan et al., (2000) showed that AM inoculation of potato plants
stimulated production of the potato cyst nematode-selective hatching chemical.

Amelioration of adverse soil conditions

An increasing number of studies indicate the importance of mycorrhizal fungi for
the survival of plants in places with problem soils or regions with extreme climate. The
topic has been reviewed (Haselwandter and Bowen, 1996). Often, growth stimulation
through the supply of essential nutrients dilutes the potential impact of damaging ions in
the shoot.
i. Heavy metals
The capacity of plants to colonise soils containing high levels of heavy metals
(such as Zn, Cu, Mn, Ni, Cr) is enhanced by their colonisation by mycorrhizal fungi (Galli
et al., 1994; Hartley et al., 1997; Leyval et al., 1997). Possible mechanisms by which
mycorrhizas deal with excess metals include the immobilisation of metals in the fungal
hyphae or in root tissue (Hildebrandt et al., 1999). Thus, mycorrhizal plants often show
less toxicity symptoms in the shoot.
ii. Unfavourable pH
ECM plants in alkaline soils may be advantaged by the capacity of fungal hyphae
to access limiting nutrients such as P and Zn. Some ECM fungi produce oxalic acid which
dissolves sparingly soluble calcium phosphates (Lapeyrie et al., 1991). Iron uptake may be
enhanced by the release of siderophores (Marschner, 1995).
iii. Salinity
AM fungi can protect some non-halophytic plants against yield losses in
moderately saline soils. Possible mechanisms include the stimulation of root growth (Ruiz-
Lozano and Azcon, 2000), improved plant nutrition (Al-Karaki, 2000) and increased
synthesis of plant polyols (Juniper and Abbott 1993) in mycorrhizal plants. The incidence
of mycorrhizal halophytes is generally quite low (Brundrett, 1991). Little information is
available for ECM associations (Dixon et al., 1993).

ROLES IN ECOSYSTEMS
The ecology of mycorrhizal fungi is not well documented (Abbott and Gazey,
1994; Francis and Read, 1995). Hence, in the discussion that follows, conclusions are
mostly drawn from short-term studies with a small range of partnerships, often under
experimental conditions. In nature, the situation is far more complex as a single tree may
have fungal partners which can vary in time and space. The study by Moyersoen et al.,
(1998), on the co-occurrence of AM and ECM fungi in rainforest in Cameroon, provides a
50 CMU. Journal (2002) Vol. 1(1)

good example of a field study exploring possible functional roles of mycorrhizal fungi.
More studies of this type are needed to elucidate the dynamics of mycorrhizal fungi in
ecosystems and the impact of disturbance.

Carbon transport
The fungal/plant interface provides a conduit for the movement of carbon from
the plant to the fungus, and for movement between plants linked by mycelia (Francis and
Read, 1984; Simard et al., 1997; Wu et al., 2001). The nature of the interface and its mode
of regulation are still being elucidated (Hall and Williams, 2000). It is generally believed
that mycorrhizal plants direct more of their photosynthates into the soil than
nonmycorrhizal plants. This extra carbon accumulates in patches and at the edge of hyphal
mats (Finlay and Read, 1986), and boosts the energy supply to the detrital food web,
benefiting saprohytic microbes and other soil organisms (Barea, 2000). Because the
chemical (Dieffenbach and Matzner, 2000) and physical environment around mycorrhizas
(the mycorrhizosphere) differs from nonmycorrhizas, presumably it provides microhabitats
for soil biota that are not present in the rhizospere of nonmycorrhizal roots.
Mycorrhizal fungi are estimated to consume from 15 to 50% of net primary
production (Fogel and Hunt, 1979; Vogt et al., 1982).

Nutrient cycling and nutrient conservation

Fungi are crucial components of ecosystems as they transport, store, release and
cycle nutrients. A good example of the potential of mycorrhizal fungi to capture and
deliver nutrients to their host comes from studies using inoculated eucalypts in field trials
in sub-tropical China. Generally, trees in this region grow well below their potential. The
main constraint to productivity appears to be low soil fertility (Dell and Malajczuk, 1994;
Xu and Dell, 1998). Most of the land available for plantation forestry have been degraded
over recent centuries with extensive loss of the A horizon caused by population pressure,
inadequate management and over-harvesting (Xu, 1996). Topsoil crusting is common,
contributing to enhanced erosion, reduced soil water storage, compaction and poor root
development (Xu et al., 2000). Low soil organic matter (SOM) content (<2%) also
restrains productivity. As most soils for plantation eucalypts in southern China have lost
their Ao layer, we need urgently to consider how to recover microbial biodiversity as there
is no doubt that this will be important for improving long-term soil fertility. The capacity
of some ECM fungi to promote both early growth and survival of eucalypts is very
important for commercial plantations on these disturbed and difficult sites. Significant
effects of ECM fungal inoculation on growth of plantation eucalypts were obtained at two
sites in southern China (Xu et al., 2001). Effects were isolate dependent with some
isolates stimulating tree growth and some isolates depressing tree growth. Similar results
were obtained in a trial in the Philippines where two isolates increased survival while one
isolate decreased survival of Eucalyptus urophylla (Aggangan et al., 1999). The
improvement in growth could be attributed to the acquisition of P as other essential
mineral nutrients were supplied at establishment. Generally, inoculation only increased
stand volume under P-limiting soil conditions.
In forests, litter is an important nutrient reservoir. ECM fungi can mobilise P, N
 CMU. Journal (2002) Vol. 1(1) 51

and other nutrients from litter to tree roots (Attiwill and Adams, 1993; Perez-Moreno and
Read, 2000). Fogel (1980) estimated that ECMs account for 43% of the annual turnover
of N in a Pseudotsuga menziesii forest in Oregon. Litter type can affect the diversity and
function of ECMs (Conn and Dighton, 2000). Buscot et al., (2000) propose that the high
diversity of fungal partners that a tree may have allows optimal foraging and mobilisation
of various N and P forms from organic soil layers.

Soil structure
It is obvious from the examination of ECM mycelial mats, that mycorrhizal fungi
have a big impact on soil structure. Yet, there is scant information in the literature
regarding soils in tropical ecosystems. In agricultural soils, AM fungi increase the
formation of soil aggregates (Bethlenfalvay et al., 1999).

Food for animals

Long-distance dispersal of spores from ECM fungi with hypogeal (truffle-like)
sporocarps depends largely on mammal mycophagy (Kotter and Farentinos; Claridge and
May, 1994). Mycophagy is widespread and has been demonstrated in Europe, Australasia
and North America. Mycophagy serves to maintain populations of ECM fungi and
provides nourishment to small mammals (Malajczuk et al., 1987). Sporocarps are good
sources of water, protein, carbohydrates and minerals (Johnson, 1994; Claridge et al.,
1999). The tripartite relationship between truffles/truffle-like fungi, vertebrates such as
squirrels and many ground-dwelling marsupials, and the host trees, are well known. Less
well known is the role that mycorrhizal fungi play as a food source for invertebrates and
the role of invertebrates in dispersal of ECM and AM fungal spores.

VALUE TO PEOPLE
In many upland forest regions of SE Asia, sporocarps of fungi, mostly
basidiomycetes, have traditionally been collected for local consumption and trade (Dell et
al., 2000). Many of these fungi, especially members of the Amanitaceae, Boletaceae,
Russulaceae, and Tricholomataceae, form ectomycorrhizal associations with trees in the
families Dipterocarpaceae, Fagaceae and Pinaceae and are important for maintaining
ecosystem function. The highest diversity of edible fungi is collected from mixed forests in
China and the lowest diversity from areas of tropical pine and dipterocarps. In general,
traded fresh sporocarps are 2 to 20 times more valuable, by weight, than local seasonal
fruits and vegetables. International trade in a small number of species is having a major
impact on the quality and sustainability of the mushroom harvest from some collecting
sites.
Forest fungi are also valued for medicine, for their aethetics, as bio-indicators of
environmental quality and for bio-remediation.

LAND MANAGEMENT EFFECTS ON MYCORRHIZAL FUNGI

Any form of land management that involves tillage, timber harvesting, vegetation
clearing, or other forms of disturbance can affect mycorrhizal populations. Severe soil
disturbance, such as fallowing agricultural soils (Thomson, 1987), crop rotation with a
52 CMU. Journal (2002) Vol. 1(1)

non-host species (Gravito and Miller, 1998) or topsoil stripping and storage during mining
(Jasper et al., 1987; Gardner and Malajczuk, 1988; Bellgard, 1993), markedly reduces
populations of mycorrhizal fungi. Unlike AM fungi, ECM fungi may be able to quickly
invade disturbed soils (Jasper, 1994). This is often the case for what have been termed
“early colonising” genera such as Laccaria, Pisolithus, Rhizopogon, Scleroderma and
Thelephora. Recolonisation mostly results from spore dispersal by wind and animal
vectors from sporocarps in adjacent vegetation.
The mycelial network appears to be an important component of the inoculum
potential of an undisturbed soil (Evans and Miller, 1990). Even minor soil disturbance can
impact on the function of mycorrhizas. Severing mycelium reduces the extent of inter-root
and inter-plant connections, thus reducing access to existing and new food bases (Read
and Birch, 1988). The mycelial mats of ECM fungi, mentioned earlier, are vulnerable
because they are easily disrupted by raking litter during the collection of leaves for fuel or
the collection of edible fungi.
Studies in a number of ecosystems (Reeves et al., 1979; Janos, 1980; Allen et al.,
1987; Siqueira et al., 1988) show that in climax communities, normally dominated by
species heavily colonised by mycorrhizal fungi, disturbance leads to a successional
sequence in which re-colonisation is initiated by plant species which are non-mycorrhizal
or little infected (Read and Birch, 1988). Gap-preferring species thus may have lower rates
of mycorrhizal infection than species preferring undisturbed microsites (Onipchenko and
Zobel, 2000). However, Brundrett et al., (1995) found that for parts of tropical Australia,
the activity of mycorrhizal fungi was higher in patches of early-successional vegetation
than in undisturbed habitats. In a study in deciduous tropical forest in Mexico, Allen
(1998) concluded that regrowth of vegetation in small gaps was not limited by mycorrhizal
fungi, since they were still abundant after treefalls. However, recovery in pastures could be
affected by low fungal diversity and dominance of grasses. Jasper et al., (1991) found that
disturbance of forest and heathland soils decreased colonisation of test plants (clover)
compared to disturbance of clover soil. They proposed that a larger number of propagules
in the pasture soil may have allowed the pasture soil to maintain infectivity after
disturbance. There is a suggestion that ecosystems with a high proportion of grasses and
high numbers of AM spores may also be be more tolerant of disturbance (Visser et al.,
1984).
The abandonment of agricultural land in the Italian Alps resulted in succession
from nonmycorrhizal ruderal annuals to AM-colonised perennials and an increase in
floristic richness (Barbi and Siniscalo, 2000). Over time, ECM hosts will increasingly
dominate if old-field succession is allowed to continue.
Use of fertilisers can affect mycorrhizal fungal populations (Baum and
Makeschin, 2000; Pampolina et al., 2001). Increasing soil fertility, especially P and N, can
suppress mycorrhiza formation and/or mycorrhizal diversity but the effects are often host
and fungal dependent. For example, the number of epigeous basidiocarps in an 11-year-old
Pinus taeda stand in north California was reduced to 17 % following the addition of 25 kg
P ha-1 (Menge et al., 1977). In Betula pendula, the addition of 20 kg P ha-1 at 3 and 9
weeks after outplanting reduced ectomycorrhizal root colonization (Newton and Pigott,
1991). By contrast, Fransson et al., (2000) applied repeated balanced additions of
 CMU. Journal (2002) Vol. 1(1) 53

nutrients to 36-year-old Picea abies and could find no measurable effect on morphotype
richness (>60 ECM morphotypes) or total number of root tips. However, Cenococcum
was more common in fertilised plots than in the controls. Soil P content is often negatively
correlated with % root colonisation (Maldonado et al., 2000).

MANAGING MYCORRHIZAL FUNGI

Most emphasis on the management of mycorrhizal fungi has focussed on
disturbed habitats such as occur in agriculture and forestry, or in semi-controlled
environments such as in nurseries or in production horticulture. Few studies have
investigated the ecology of mycorrhizal fungal populations in natural systems. We know
relatively little about how perturbations such as fire, flood, drought, volcanism affect the
diversity, function and genetic composition of mycorrhizal fungal populations. Our
knowledge is depauperate concerning seasonal changes in mycorrhizal populations and
fungal succession. However, it is clear from the earlier part of this paper that mycorrhizal
fungi are an integral part of ecosystems (Klironomos et al., 2000) and provide physical
links between the primary producers, the comsumers and the decomposers.
Clearly we need to understand a lot more of the biology and ecology of the
mycorrhizal fungi in their natural habitats. In the meantime, we can undertake the
following:
• maintain populations of host plants and variety of habitats for each species of
host.
• increase activity of target organisms in disturbed habitats by adjusting soil
management strategies, and where necessary, introducing indigenous
organisms.
• document fungal diversity in all areas but initially direct resources to
threatened habitats.
• reduce disturbance to a level that maintains fungal fruiting.
• harvest non-wood forest products sustainably.

FUTURE RESEARCH IN THAILAND

Unlike for the temperate latitudes, where large numbers of taxonomic and
ecological studies have been made on mycorrhizal fungi, there is only a meagre knowledge
of the mycorrhizal fungi associated with many tropical and subtropical ecosystems. A
great deal of taxonomic effort is required, for example, in SE Asia to adequately describe
and delineate the fungal biota and allow ecological studies to proceed on specific
organisms. This is particularly the case for Northern Thailand where the vegetation
changes markedly with topography. There, montane ECM fungal elements occur within
short distances in elevation from lowland species associated with either evergreen or
deciduous Dipterocarps. Researchers working on AM and ECM fungi should ensure that
representative specimens of taxa referred to in their studies are lodged in curated national
or regional fungal herbaria. Over time this will allow definitive names to be applied and
facilitate linkages between the different studies.
54 CMU. Journal (2002) Vol. 1(1)

Furthermore, many fundamental aspects of fungal ecology require intensive

study, such as: seasonal dynamics of fungi, fungal succession, nutrient turn-over, host
range, and fungal resilience/sensitivity to disturbance, to name a few. Such studies are not
facile, as populations must be studied below-ground. It is becoming evident that neither
the diversity nor the abundance of sporocarps above-ground can be used to assess below-
ground ECM fungal diversity or abundance (van der Heijden et al., 1999). Furthermore, in
eucalypt forests in Australia, there is probably a greater diversity of ECM fungi that fruit
below-ground than above-ground (Bougher, 1995). These truffle-like fungi, and many
fungi that produce sporocarps infrequently, or have insignificant fruit bodies, have been
little studied in SE Asia.
Research being undertaken by PhD students at Chiang Mai University on edible
ECM forest fungi and on AM fungi associated with Macaranga denticulata in Swidden
fields of Karen farmers in Mae Hong Son Province, hopefully will be extended by other
researchers in the region in the future. In addition to the types of mycorrhizal fungi
covered in this review, the orchid mycorrhizal fungi also need further attention
(Purshotam-Kaushik, 1998) as issues of orchid conservation and cultivation become more
pressing.

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