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Journal of Ecology 2009, 97, 1139–1150 doi: 10.1111/j.1365-2745.2009.01570.x

SPECIAL FEATURE
FACILITATION IN PLANT COMMUNITIES

Socialism in soil? The importance of mycorrhizal

fungal networks for facilitation in natural ecosystems
Marcel G. A. van der Heijden1* and Thomas R. Horton2
1
Ecological Farming Systems, Agroscope Reckenholz-Tänikon, Research Station ART, Zurich, Switzerland; and
2
Department of Environmental and Forest Biology, SUNY-Environmental Science and Forestry, Syracuse, NY, USA

Summary
1. Almost all plants are engaged in symbiotic relationships with mycorrhizal fungi. These soil fungi
can promote plant growth by supplying limiting nutrients to plant roots in return for plant assimi-
lates.
2. Many mycorrhizal fungi are not host specific and one fungal individual can colonize and inter-
connect a considerable number of plants. The existence of these so-called mycorrhizal networks
implies that fungi have the potential to facilitate growth of other plants and distribute resources
among plants irrespective of their size, status or identity. In this paper, we explore the significance
of mycorrhizal fungal networks for individual plants and for plant communities.
3. We address the following questions: (i) are all plant species benefitting from mycorrhizal net-
works, (ii) is benefit dependent on the size or age of a plant, (iii) is fungal support related to the rela-
tive dominance of plants in a community, (iv) are there host dependent barriers and physiological
constraints for support and (v) what is the impact of mycorrhizal networks on plant–plant interac-
tions and plant community dynamics? Moreover, using a review of published studies, we test
whether mycorrhizal networks facilitate growth of small seedlings that establish between or near
larger plants.
4. We found 60 cases where seedling species were grown together with larger plants with or without
mycorrhizal fungal networks. Mycorrhizal networks promoted seedling growth in 48% of the cases
(for 21 seedling species), while negative effects (25%) and no effects (27%) were also common. Seed-
lings associating with ectomycorrhizal fungi benefitted in the majority of the cases while effects on
seedlings associating with arbuscular mycorrhizal fungi were more variable. Thus, the facilitative
effects of mycorrhizal fungal networks depend on seedling species identity, mycorrhizal identity,
plant species combinations and study system. We present a number of hypothetical scenarios that
can explain the results based on cost–benefit relationship of individual members in a network.
5. Synthesis. Overall, this review shows that mycorrhizal networks play a key role in plant commu-
nities by facilitating and influencing seedling establishment, by altering plant–plant interactions and
by supplying and recycling nutrients.
Key-words: arbuscular mycorrhizal fungi, common mycorrhizal networks, ectomycorrhizal
fungi, facilitation, hyphal links, mutualism, plant competition, positive interactions

tation also play a key role in plant communities (Callaway

Introduction
Plants interact in many ways, both negative and positive. Neg-
ative interactions such as plant competition received much
attention in the 1980s and 90s (Sapp 2004). However, there is
increasing recognition that positive interactions such as facili-
*Correspondence author. E-mail: marcel.vanderheijden@art.admin.ch
et al. 2002; Brooker et al. 2008). Facilitation is defined here as
positive non-trophic interactions that occur between physio-
logically independent plants and that are mediated through
changes in the abiotic environment or through other organ-
isms (Brooker et al. 2008). Examples of facilitation are
the positive effects of nitrogen fixing plants on neighbours and
pollination of multiple plant species by the same insects.

 2009 The Authors. Journal compilation  2009 British Ecological Society


1140 M. G. A. van der Heijden & T. R. Horton
In this paper, we focus on the 400 million-year-old symbiosis
between the majority of land plants and mycorrhizal fungi
(Smith & Read 2008). Such interactions have facilitative effects
when mycorrhizal associations formed or maintained by one
plant are beneficial for other plants. The mycorrhizal symbio-
sis is based on reciprocal exchange of resources: the fungi pro-
vide limiting nutrients to plants in return for plant assimilates
(Smith & Read 2008). In natural ecosystems, plants obtain up
to 80% of their requirement for nitrogen and up to 90% of
phosphorus from mycorrhizal fungi (van der Heijden, Bardgett
& van Straalen 2008). These nutrients are acquired by complex
hyphal networks (Leake et al. 2004; Selosse et al. 2006) which
are specialised to forage for soil nutrients (Olsson, Jakobsen
& Wallander 2002). Moreover, mycorrhizal fungi can also
provide resistance to stress, drought and in some cases to
soil pathogens (Auge 2001; Sikes, Cottenie & Klironomos
2009).
Most mycorrhizal fungi are not host specific and one fungal
individual can simultaneously colonize a large number of
plants from the same but also from different plant species
(Fig. 1). Moreover, both small seedlings and large plants can
be colonized by one mycorrhizal fungal individual (Newman
1988; Horton & van der Heijden 2008). Thus, plants can be
interconnected by mycorrhizal fungal networks in the so-called
‘wood-wide-webs’ (Simard et al. 1997). The existence of these
networks implies that fungi have the ability to distribute
resources among plants irrespective of their size, status (i.e.
their relative dominance in the plant community) or identity.
For clarity, a mycorrhizal fungal network is defined here as an
3 4
4
1
3 zal fungal networks with enhanced growth (Grime et al. 1987;
2
N1
N2
Fig. 1. Resource sharing in mycorrhizal networks. One mycorrhizal
fungal individual colonizes different plant individuals from the same,
but also from different plant species. Carbon and nutrients (N) can
move through this common hyphal network. Different numbers rep-
resent different plant species. For instance, plant species 1, 2 and 3 are
colonized by the same mycorrhizal fungi (dashed line). Nutrients can
be acquired by this fungus from a nutrient patch near plant 1 (N1)
and move to plant 1 or 2. Nutrients of patch N2 could flow to plant 2
or 3. In addition, plant species 1, 2 and 3 are also colonized by another
mycorrhizal fungus (solid line). Some plant species are not colonized
by mycorrhizal fungi (plant 4). Plant size also varies (see plant species
3) showing that plants in different growth stages can be colonized by
the same mycorrhizal fungus.
 2009 The Authors. Journal compilation  2009 British Ecological Society, Journal of Ecology, 97, 1139–1150
13652745, 2009, 6, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2009.01570.x by Test, Wiley Online Library on [09/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
established fungal mycelium that simultaneously colonizes and
interconnects roots of the same or different plant species. The
fungi able to form mycorrhizal fungal networks are those that
form the typical mycorrhizal structures inside plant roots or on
the surface of plant roots after a complex molecular dialogue
between plant and fungus.
In this paper, we explore the significance of mycorrhizal fun-
gal networks as facilitators in plant communities. In particular
we investigate: (i) whether all plants benefit from mycorrhizal
fungi, (ii) whether support is dependent on the size of a plant,
(iii) whether there are host-dependent barriers and physiologi-
cal constraints for support, (iv) whether there is interplant
carbon and nutrient transfer via mycorrhizal networks and
(v) whether mycorrhizal networks influence plant–plant inter-
actions and plant community dynamics. Moreover, using an
analysis of published studies, we test whether mycorrhizal net-
works facilitate growth of small seedlings that establish
between or near larger plants. We end with conclusions and
identify future research priorities.
Do all plant species benefit?
Many plant communities are dominated by mycorrhizal
plants, including most grasslands, savanna, boreal-, temperate-
& tropical forests (Read 1991). In these communities, abun-
dant mycorrhizal fungal networks are formed (Leake et al.
2004) and the majority of plants are usually extensively colo-
nized by these mycorrhizal networks. Pot experiments per-
formed with plants grown under the nutrient-poor conditions
typical for most natural plant communities show that many
plants benefit from the presence of mycorrhizal fungi (Smith &
Read 2008). However, most experiments have been performed
with single plants grown in the absence of competition and
only a few studies have tested the importance of mycorrhizal
networks. Studies that mimicked the field situation using
microcosms simulating nutrient-poor European calcareous
grassland with established mycorrhizal networks showed that
75% of the investigated plant species benefited from mycorrhi-
van der Heijden 2004). Experiments with a number of tree spe-
cies indicate that many of them benefit from mycorrhizal colo-
nization, especially at low soil fertility (Simard, Durall & Jones
2002; Karst et al. 2008). However, the impact of mycorrhizal
fungal networks on tree growth in natural systems is difficult
to study because mycorrhizal fungi are often already present
(but see Nara 2006a; Dickie, Koide & Steiner 2002; see also
below).
Not all interactions with mycorrhizal fungal are positive:
some plant species perceive mycorrhizal fungi as antagonists.
These include some non-mycotrophic plant species (plants that
are unable to form symbiotic associations with mycorrhizal
fungi) and some plant species characteristic of ruderal environ-
ments (Francis & Read 1995; Klironomos 2003). It must be
remembered that approximately 10–15% of all vascular plant
species, including the model plant Arabidopsis thaliana), are
non-mycorrhizal and do not benefit from mycorrhizal fungi
(Wang & Qiu 2006; Brundrett 2009). Hence, the question of

Socialism in soil? The importance of mycorrhizal fungal networks 1141
whether all plant species benefit from mycorrhizal fungi can be
answered simply with a ‘no’. Finally, the effect of mycorrhizal
fungi on plant growth is context dependent (Johnson, Graham
& Smith 1997; Jonsson et al. 2001). At high soil fertility, there
is often no benefit and plant growth can be slightly reduced in
the presence of mycorrhizal fungi due to their carbon demand
(Smith, Grace & Smith 2009). Further, a mycorrhizal fungus
may be mutualistic with one host plant species, and parasitic
on another host species as Plattner & Hall (1995) report for
Tuber melanosporum.
Is benefit dependent on the size of a plant?
Mycorrhizal fungi usually colonize all plant individuals from
mycotrophic hosts, irrespective of their size or development.
An intriguing question is whether all plant individuals (e.g.
small seedlings and larger plants) receive the same amount of
benefit from mycorrhizal fungi. To test for general patterns,
we performed a literature analysis with studies where seedlings
were grown together with larger ⁄ adult plants in the presence
and absence of mycorrhizal fungi. We made a distinction
between studies where seedlings were grown with adult ⁄ larger
plants from the same species and studies in which seedlings
grew together with different plant species. In addition to this, a
distinction was made between plants hosting arbuscular
mycorrhizal (AM) fungi and ectomycorrhizal (EM) fungi. EM
fungi belong to the Basidiomycetes and Ascomycetes and asso-
ciate with a range of trees, especially those from temperate and
tropical forests. AM fungi belong to the Glomeromycota
(Schüßler, Schwarzott & Walker 2001) and associate with an
estimated 65% of all land plants, including many grasses,
herbs and tropical trees (Wang & Qiu 2006; Brundrett 2009).
The results of the analysis are shown in the next section. This
analysis focuses on experiments where several plants co-occur
in pots, microcosms or in the field. These experiments are eco-
logically more realistic than those where plants are grown
alone in pots with or without mycorrhizal fungi. In pots with
multiple plants (e.g. seedlings and adult plants), interactions
between plants occur (e.g. competition or facilitation) and the
effects of common mycorrhizal networks on plant growth can
be tested, thus better simulating conditions usually observed in
natural communities.
Mycorrhizal networks and seedling
establishment near larger plants
We performed a literature survey and found 20 studies where
seedlings were grown near larger plants in the presence and
absence of mycorrhizal fungal networks (see Appendix S1 in
Supporting Information). In most studies, several seedling spe-
cies were tested and results of 60 cases were included in the
analysis. Thirteen studies were performed with AM fungi, and
seven with EM fungi (Appendix S1). Three categories were
distinguished: cases where seedlings had significantly higher
biomass in the presence of mycorrhizal fungal networks, cases
where seedling biomass was significantly reduced and cases
without significant differences.
 2009 The Authors. Journal compilation  2009 British Ecological Society, Journal of Ecology, 97, 1139–1150
13652745, 2009, 6, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2009.01570.x by Test, Wiley Online Library on [09/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Twenty-one seedling species (48% of cases investigated)
benefited from mycorrhizal networks while 12 species (25% of
cases) responded negatively. The biomass of 15 seedling species
(27% of the cases) was not significantly influenced by the pres-
ence or absence of mycorrhizal fungal networks (Fig. 2;
Appendix S1). The distribution of cases differed significantly
among the three categories (P = 0.05). The average growth
response of all seedlings ⁄ cases was +14% or +20% when
non-mycorrhizal (NM) plants not hosting mycorrhizal fungi
were removed from analysis.
We also performed the analysis separately for plants associ-
ating with AM fungi or with EM fungi. Mycorrhizal networks
formed by EM fungi promoted seedling growth in seven cases
(75% of the cases), while in three cases (25%) seedling growth
did not vary between treatments with or without mycorrhizal
fungi. For AM fungi, 16 out of 37 species (and 42% of the
cases) responded significantly positively, 15 species (33% of
the cases) responded negatively, while growth responses of 12
seedling species (29% of the cases) did not vary significantly in
treatments with or without mycorrhizal fungal networks.
Growth responses of several species (e.g. Plantago lanceolata –
see Appendix S1) were tested repeatedly in different studies.
Hence, the distribution of cases as discussed above and pre-
sented in Fig. 2 does not match precisely to the number of
investigated seedling species. Based on this analysis, it can be
concluded that seedling establishment of plants forming asso-
ciations with EM fungi is more heavily dependent on mycor-
rhizal fungi compared with plants associating with AM fungi.
Note, however, that a much broader range of plant species
(including several non-mycorrhizal hosts) were included in the
analysis with AM fungi, also reflecting the fact that habitats
where AM fungi are abundant probably contain a higher pro-
portion of non-mycorrhizal plants. Moreover, the analysis for
EM fungi is based on only a few cases and the observed effect
35
30
25
Number of cases
20
15
10
5
0
Positive Negative No effect
Seedling mycorrhizal dependency
Fig. 2. Output from literature analysis showing effects of mycorrhizal
fungal networks on seedling growth and establishment. Positive and
negative response indicates the number of cases where seedlings bio-
mass was significantly enhanced or reduced in the presence of mycor-
rhizal fungal networks. ‘No response’ indicates cases where seedling
biomass was not significantly affected by the presence or absence of
mycorrhizal networks. For further information see Appendix S1.
 13652745, 2009, 6, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2009.01570.x by Test, Wiley Online Library on [09/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1142 M. G. A. van der Heijden & T. R. Horton

might change considerably if more studies are included. The
outcome of this analysis is roughly the same if the number of
studies and not the number of seedling species or cases is used
for the analysis (Appendix S1).
An interesting question is whether the benefit seedlings
derive from mycorrhizal fungal networks is higher, lower or
equal compared with coexisting older and larger plants of the
same species. This could be tested for nine studies (Table 1).
Three of these studies indicated that the relative benefit to seed-
lings was similar to that of larger plants (compare the mycor-
rhizal dependencies in Table 1: see Ocampo 1986; Kytoviita,
Vestberg & Tuom 2003; Pietikainen & Kytoviita 2007), two
studies found that seedlings benefited more (van der Heijden
2004; Eissenstat & Newman 1990; although not significantly
so in the latter case) and in two studies adult plants benefited
from mycorrhizal fungi while seedling growth was significantly
reduced (Moora & Zobel 1998; Nakano-Hylander & Olsson
2007). These findings are in line with Moora & Zobel (2009)
who observed that mycorrhizal networks are less beneficial for
seedlings of the same species (intraspecific combinations) com-
pared with seedlings of different plant species (interspecific
combinations). Interestingly, in green orchids cost–benefit
relationships appear to change over a plant’s life cycle. Net
fungus to plant carbon transfer supports seedling establish-
ment of the tiny non-photosynthetic orchid protocorms in the
early growth phases while adult orchids ‘repay’ the carbon to
their mycorrhizal associates when they are older and larger
(Cameron et al. 2008).
We have used a wide range of species and a wide range of
study systems for this analysis. Hence, the experimental condi-
tions (e.g. nutrient availability, soil type, light conditions,
mycorrhizal fungal identity) were highly variable among the
different studies and probably explain the variable results of
the analysis. For instance, the seedling response of Plantago
lanceolata was tested four times in three different studies (see
Appendix S1): in two cases Plantago seedlings benefited
greatly from the presence of mycorrhizal networks (Grime
et al. 1987 & Francis & Read 1995) while in two cases seedling
growth was clearly suppressed (Nakano-Hylander & Olsson
2007). The study by Grime et al. (1987) was performed under
nutrient-poor conditions (as shown by poor overall plant pro-
ductivity), whereas plant nutrient availability in the study by
Nakano-Hylander & Olsson (2007) was much higher as evi-
denced by a higher plant biomass obtained in a shorter growth
period. The effect of mycorrhizal fungi on plant growth is
strongest at low soil fertility (e.g. Smith & Read 2008), perhaps
explaining why the results of the studies by Grime et al. (1987)
and Nakano-Hylander & Olsson (2007) contrasted so much.
We determined the average seedling response to mycorrhizal
fungi in studies where several treatments with mycorrhi-
zal fungi were compared (e.g. treatments with different
mycorrhizal fungal species or communities). In some of these
cases, the seedling response varied greatly depending on
mycorrhizal treatment. For instance, Nara (2006a) inoculated
Salix reinii plants with 11 different EM fungi plus a nonmycor-
rhizal control under glasshouse conditions. After 11 months of
growth, these plants were then planted in the field to establish
individual mycorrhizal networks, and the effect of these
mycorrhizal networks on the growth of nearby seedlings was
tested. A previous study had shown that this field lacked
mycorrhizal inoculum for Salix (Nara & Hogetsu 2004). There
was considerable variation in the effects of adult plants on
nearby seedlings establishment. Mycorrhizal networks of most
of the fungal species improved the growth and nutrient status
of the seedlings over the control except Laccaria amythestina,
where none of the variables were significantly different from
the control. This study clearly shows that established plants
can facilitate seedling establishment. However, it is unclear
whether this is due to direct facilitative effects through mycor-
rhizal networks, or simply because established plants provide

Table 1. Biomass (mg) of seedlings grown together with larger plants from the same plant species in the absence (NM) or presence (M) of hyphal
networks formed by arbuscular mycorrhizal fungi. The Mycorrhizal dependency shows the percentage growth increase or decrease of
mycorrhizal plants relative to non-mycorrhizal plants (calculated after van der Heijden (2002). The summary shows whether seedlings (first
position) and adults (second position) had significantly higher (+), lower ()) or statistically equal biomass (0) in the presence of mycorrhizal
networks

Seedlings Larger plants

Mycorrhizal Mycorrhizal
Plant species NM M dependency NM M dependency Reference Summary

Sorghum vulgare 632a 736b 14.9 1600 2364 32.3 Ocampo 1986 (+; +)
Festuca ovina 24.1 22.0 )8.8 922 609 )51.4 Grime et al. 1987 (); ))
Plantago lanceolata 18.1 28.3 36.0 1980 1430 )38.5 Eissenstat & Newman 1990 (0; 0)
Hypericum perforatum* 1070 800 )25.2 1470 2720 85.0 Moora & Zobel 1998 (); +)
Sibbaldia procumbens* 7 8 12.5 1700 1800 5.5 Kytoviita, Vestberg & Tuom 2003 (0; 0)
Gnaphalium norvegicum 1.5 2.0 26.1 978 1369 28.6 Pietikainen & Kytoviita 2007 (0; +)
Bromus erectus† 8.3 14 40.7 105.6 92.1 )14.7 van der Heijden 2004 (+; 0)
Plantago lanceolata 22 7 )68.2 810 2230 63.7 Nakano-Hylander & Olsson 2007 (); +)
Trifolium subterraneum 60 40 )33.3 260 1810 85.6 Nakano-Hylander & Olsson 2007 (); +)

*The biomass of seedlings grown with or without mycorrhizal fungal networks was estimated from graphs.
†
Seedlings were grown in treatments inoculated with different mycorrhizal fungi. The average seedling response of all mycorrhizal fungal
treatments was taken.

 2009 The Authors. Journal compilation  2009 British Ecological Society, Journal of Ecology, 97, 1139–1150

Socialism in soil? The importance of mycorrhizal fungal networks 1143
an inoculum source (mycorrhizal networks) for nearby seed-
lings. In this respect, it is important to mention that in some
cases seedlings and adult plants are colonized by different
mycorrhizal fungal communities (Aldrich Wolfe 2007), mak-
ing it unclear to what extent resource sharing among seedlings
and larger plants occurs. Overall, the studies discussed above
show that the growth response of seedlings to mycorrhizal fun-
gal networks is variable, depending on factors such as mycor-
rhizal identity, plant species identity, plant species
combinations and nutrient availability (see above).
Seedling establishment is also strongly determined by the
dominant mycorrhizal network in a community. For instance,
Horton, Bruns & Parker (1999) showed that the diverse com-
munity of mycorrhizal fungi associated with Arctostaphylos
supported Pseudotsuga menziesii seedling establishment, while
mycorrhizal communities found near Adenostoma did not.
Pseudotsuga menziesii, associates with EM fungi and the differ-
ence is probably explained by Arctostaphylos shrubs support-
ing well-developed EM networks whereas Adenostoma shrubs
primarily associate with AM fungi. Similarly, Dickie, Koide &
Steiner (2002) reported a positive seedling response when
Quercus seedlings were planted near Quercus trees, but a nega-
tive response when planted near the arbuscular mycorrhizal
Acer even though some EM colonization was observed on
seedlings near Acer. Moreover, a recent study by Collier & Bi-
dartondo (2009) showed that the invasion of EM pines into
heathland (with ericoid mycorrhizal fungi) is limited due to the
absence of EM fungi. The absence of suitable EM inoculum
has also been shown to inhibit Pinaceae invasion into native
Nothofagus communities in Isla Victoria (Nuñez, Horton &
Simberloff 2009).
Is fungal support related to the relative
dominance of a plant in the community
Many ecosystems are dominated by plants forming mycor-
rhizal associations (Read 1991). It is still unclear whether
plants that dominate a specific plant community also
obtain most benefit from mycorrhizal fungi. Studies per-
formed so far gave conflicting results. Hartnett & Wilson
(1999), studying tall grass prairie in North America,
observed that the dominant C4 grasses obtained most ben-
efit from mycorrhizal fungi. They suggested that mycorrhi-
zal fungi reduced plant diversity in these communities by
supporting the dominant plant. Similarly, it is proposed
that in some tropical rainforests EM associations encour-
age dominance of certain tree species (Connell & Lowman
1989). Studies performed with European calcareous grass-
land provide opposite results. Both Grime et al. (1987) and
van der Heijden et al. (1998) show that subordinate plant
species benefited most when mycorrhizal fungi were pres-
ent, while biomass of the dominant grass was not
enhanced, or even reduced in presence of mycorrhizal
fungi. As a consequence, mycorrhizal fungi enhanced plant
diversity in these grassland communities. Note that, in the
study by Grime et al. (1987), field roots were used as inoc-
ulum to establish a fungal network. It is possible that,
 2009 The Authors. Journal compilation  2009 British Ecological Society, Journal of Ecology, 97, 1139–1150
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beside mycorrhizal fungi, pathogenic fungi were also part
of this fungal network. Hence, the negative effects of the
fungal network on the growth of the dominant plant could
also be due to pathogens. Overall, the studies mentioned
above indicate that the ‘status’ and relative dominance of
a plant in the community does not determine how much
benefit it receives. The results appear to depend on the
identity of the dominant plant and its relationship with
mycorrhizal fungi. The observations by Grime et al. (1987)
and van der Heijden et al. (1998) also imply that there are
many factors that determine the dominance of plants in
plant communities: in some cases mycorrhizal fungi are
important, while in other cases other factors such as
growth form, relative growth rate, competitive ability,
resistance to stress or disturbance determine plant abun-
dance.
Free access for everyone? Host specificity &
physiology of mycorrhizal networks
Pot experiments with AM fungi isolated from field soil have
shown that most AM fungal species can colonize most plant
species used as bait plants. This lack of specificity is also
reflected by the fact that some AM fungal species have a world-
wide distribution, associating with a wide range of plant spe-
cies in very different ecosystems (Opik et al. 2006). Despite this
lack of specificity, a considerable number of studies showed
that AM fungi have host preferences and that different plant
species are colonized by different AM fungal communities (e.g.
Vandenkoornhuyse et al. 2003; Opik et al. 2006). Still, in any
given plant community that has been studied to date, it
appears that some of the fungi form extensive networks con-
necting multiple plant species.
The specificity of EM fungi has received more attention than
AM fungi because of the relative ease in finding sporocarps in
the field and of culturing mycorrhizal seedlings in the labora-
tory. It was believed that EM fungi were more host specific
than AM fungi. Many of the examples of EM fungi with nar-
row host ranges fall into the genera Suillus, Leccinum, Gomphi-
dius, Chroogomphus, Brauniellula, and Gomphogaster (Molina,
Massicotte & Trappe 1992), all in the Boletales. This suggests
that the narrow host range of these genera is phylogenetically
determined. There is always a risk of assigning specificity based
on sporocarp appearance or pure culture synthesis experi-
ments. Evidence from field-collected root tips from mixed EM
plant communities suggests that most of the root tips recov-
ered are colonized by fungi associating with multiple host spe-
cies (Horton & Bruns 1998; Horton, Bruns & Parker 1999;
Cullings et al. 2000; Kennedey, Izzo & Bruns 2003; Horton,
Molina & Hood 2005; Dulmer 2006; Ishida, Nara & Hogetsu
2006; Lian et al. 2006; Nara 2006b). While there are some EM
fungi that are relatively host specific, most appear to have
intermediate to broad host ranges and can form networks with
multiple plant species in a mixed stand (Molina, Massicotte &
Trappe 1992).
From the above, it follows that a considerable number of
plant species from a specific community can be colonized by
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1144 M. G. A. van der Heijden & T. R. Horton

the same mycorrhizal fungus and are, thus, connected to the
same network. Important questions that follow are: which
plants maintain this network, which plants receive benefit and
how is this physiologically organised? There are several scenar-
ios (Fig. 3). One option is that carbon investment and plant
benefit are tightly interlinked: the more a plant invests in the
network, the more benefit it receives in return (Fig. 3a). Physi-
ological studies which show that nutrient supply to the plant
increases with enhanced carbohydrate availability for the fun-
gus (Bucking & Shachar-Hill 2005) provide evidence for this
scenario. Studies which show that co-occurring seedlings and
adult plants obtain, per unit of biomass, the same relative ben-
efit from mycorrhizal fungi (e.g. Kytoviita, Vestberg & Tuom
2003; Pietikainen & Kytoviita 2007) also indicate that costs
(carbon investment) and benefit (stimulation of plant growth)
are interlinked (Fig. 3a). Be aware that under this scenario lar-
ger plants obtain more resources in total, because they also
invest more, but the relative benefit is the same. Several studies
also show that plants which obtain large amounts of nutrients
from mycorrhizal fungi also have larger hyphal networks.
Hence, there is evidence that cost–benefit relationships of
plants with mycorrhizal fungi are interlinked for a considerable
number of plant species.
Many plants can, at least partly, control colonization by
mycorrhizal fungi under less beneficial conditions. At high
phosphorus availability, root colonization levels and spore
production by arbuscular mycorrhizal fungi are usually
reduced (Oehl et al. 2003; but see Graham, Duncan & Eissen-
stat 1997). Ectomycorrhizal fungi are also less abundant and
EM fungal communities are less diverse when nitrogen avail-
ability increases (Wallenda & Kottke 1998; Lilleskov et al.
2002), probably because plants suppress colonization (Nehls
et al. 2007). Moreover, plants can repress mycorrhizal phos-
phorus uptake and down-regulate fungal phosphorus trans-
porter genes at high phosphorus availability (e.g. Nagy et al.
2009) when the fungus is not required for nutrient uptake. On
the other hand, plants exude signals to attract mycorrhizal
fungi under nutrient deficiency (Yoneyama et al. 2007). This
suggests that plants have mechanisms to regulate their invest-
ment in mycorrhizal fungi, providing additional evidence that
investment costs and benefits are interlinked. When discussing
this, it is important to remember that mycorrhizal fungi are
independent from plants, aiming to enhance their own fitness.
Hence, the fungi may resist plants when these try to sanction
them under unfavourable conditions.
It is also possible that the relationship between carbon invest-
ment and plant benefit is positive, but with a different angle for
different plant species or different plant individuals (Fig. 3a).
This could explain why, in some cases, seedlings benefit more
from a connection to the mycorrhizal network compared with
adult plants (see above). It also explains why the outcome of
competition between two mycorrhizal plant species is often not
balanced (e.g. Finlay 1989; Perry et al. 1989; Marler et al.,
2004; Scheublin, Van Logtestijn & Van der Heijden 2007).
The second option is that there is no relationship between
carbon investment and plant benefit (Fig. 3b). Every plant
individual has a different relationship, thus resulting in a large
scatter of points (Fig. 3b). This has similarities to the so-called
idiosyncratic relationship between biodiversity and ecosystem
functioning (Johnson et al. 1996) stating that the relationship
is highly variable, depending on factors such as soil type, nutri-
ent availability and plant species identity. This scenario would
mean that some plant individuals obtain much more benefit
from a mycorrhizal network per unit carbon they invest, com-
pared with other plants that receive relatively less benefit per
unit invested carbon. The relationship could also differ with
different mycorrhizal fungal species or for different growth
stages of one plant species (e.g. the relative benefit of seedlings
is much higher compared with adult plants, as shown for a few
plant species in our analysis).
Plant–mycorrhizal network interactions are very hard to
explore in the field because most plants are colonized by multiple
fungal species (networks), each with its own cost–benefit
interaction. In addition, some plant species might, on aver-
age, benefit more from mycorrhizal networks compared
with other plant species. For instance, several studies
showed that mycorrhizal fungi reduce biomass of Festuca
ovina when this grass is coexisting or competing with other
plant species (Grime et al. 1987; van der Heijden et al.
1998; Scheublin, Van Logtestijn & Van der Heijden 2007).

(a) (b) (c)

1 3
3
Costs

2
4
4

Benefit

Fig. 3. Three hypothetical relationships between costs (carbon investment) and benefits (assessed as biomass gain) of the mycorrhizal symbiosis.
Cost and benefits are positively correlated (a), are variable, depending on fungus ⁄ plant pair, or environmental conditions (b) or are negatively
correlated (c). Cost and benefit relationships can be positively correlated, but with a different angle for different groups of plant species or for
seedlings compared with adult plants (solid and interrupted line in a). Plant species can invest large amounts of carbon in mycorrhizal fungi and
receive much benefit in return (plant 1), or plants invest small amounts of energy in mycorrhizal networks and receive little in return (plant 2). Some
plant individuals invest much but get not much in return (plant 3) while other plants receive much benefit, without large investments (plant 4).

 2009 The Authors. Journal compilation  2009 British Ecological Society, Journal of Ecology, 97, 1139–1150

Socialism in soil? The importance of mycorrhizal fungal networks 1145
The study by Grime et al. (1987) indicated that there is car-
bon transfer from Festuca ovina to other plant species
through common mycorrhizal fungal networks. The signifi-
cance of this carbon transfer is still under debate. However,
the fact that carbon from Festuca was found in the roots of
other mycorrhizal plant species, and not in non-mycorrhi-
zal plants, suggests that Festuca was at least supplying car-
bon to the hyphal network in this study and that other
plants benefited from the hyphal network. The outcome of
our analysis, which shows that effects of mycorrhizal net-
works on seedling establishment can be positive, neutral
and negative, fits to the scenario shown in Fig. 3b.
It has been proposed that the symbiosis between plants and
mycorrhizal fungi is based on the exchange of luxury goods
(Kiers & van der Heijden 2006). At low soil fertility, plant
growth is limited more by nutrients than by carbon supply,
and carbohydrates accumulate in plant organs (e.g. Poorter &
de Jong 1999; Korner 2003). Under these conditions, it is
advantageous for the plant to allocate assimilates to the fungi
because, by doing so, plants acquire more of the resources they
need, without additional costs. The investment of a luxury
good (carbon) in mycorrhizal fungi by some plants, and the
co-use of mycorrhizal networks by other plants could explain
the variable responses. However, this scenario would only
work if the plant investing a luxury good is not negatively
affected (e.g. by enhanced competitive ability of other plants)
and obtains at least a benefit at some point in its life cycle (e.g.
during seedling establishment).
A third option is that there is a negative relationship
between investment and benefit (Fig. 3c). This implies that
some plant species invest in mycorrhizal networks while others
obtain benefit from them. Generally, this relationship is unli-
kely, because plants would select against mycorrhizal coloniza-
tion if other plants always benefited more and if this resulted in
a reduced competitive ability (but see negative feedback model
in Bever, Westover & Antonovics (1997). This relationship
does fit mycoheterotrophic plants, which lack chlorophyll and
indirectly parasitize other plants by obtaining carbon and
nutrients from mycorrhizal networks. These plants (also called
epiparasites) obtain benefit from mycorrhizal networks of a
single fungal species, while the surrounding vegetation main-
tains the mycorrhizal network. There are about 400 species in
the world with this strategy, distributed in eleven families
including the Orchidacea and Ericaceae, and all of them lack
chlorophyll (Leake 1994; Taylor et al. 2002). Recent studies
indicate that some other plants of these families have a mixed
strategy and acquire carbon both through photosynthesis and
via hyphal links (Julou et al. 2005; Girlanda et al. 2006; Tedersoo
et al. 2007; but see Hynson et al. 2009). It is still unclear whether
these plants also invest in mycorrhizal networks (but see Bidart-
ondo et al. 2000). Experimental studies are required to test this in
more detail.
Socialism or capitalism in soil?
It is tempting to compare mycorrhizal networks with socialist
systems, where all individuals have equal opportunities and
 2009 The Authors. Journal compilation  2009 British Ecological Society, Journal of Ecology, 97, 1139–1150
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where wealth and power are distributed more evenly. On the
contrary, a capitalist mycorrhizal network would be privately
controlled for profit by the plant or plants establishing the net-
work. Our analysis provides both examples of ‘socialist’ and
‘capitalist’ tendencies of mycorrhizal networks. In several cases
small seedlings obtained more benefit (in terms of biomass gain)
compared with the larger plants that established the mycorrhizal
networks (e.g. Eissenstat & Newman 1990; van der Heijden
2004), pointing to socialist tendencies. However, in all studies
performed so far, the actual investments (in terms of car-
bon ⁄ energy input into the network) by small and large plants
were not determined and there is no empirical evidence that
resources are preferentially allocated to small seedlings. It is not
unlikely that in many cases the larger plants facilitated establish-
ment of the small seedlings by (i) providing improved mycorrhi-
zal inoculum potential and (ii) reducing the carbon cost of
establishing a functioning mycorrhizal network around the seed-
lings’ roots. However, there are also several examples which
show that small seedlings receive proportionally the same or even
less benefit from networks as larger plants (Table 1). In terms of
total biomass gains then, the larger plants thus benefit more from
mycorrhizal networks, pointing to capitalist tendencies.
Mycorrhizal networks can also be viewed as part of ‘super-
organisms’ (sensu Clements 1936), with the fungal species in
the network being redundant physical extensions of the roots
that translocate nutrients freely between plants. However, each
fungal species has its own niche and mycorrhizal fungi differ in
many ways including growth rate (Olsson, Jakobsen & Wal-
lander 2002), soil type preference, resistance to stress and dis-
turbance (Oehl et al. 2003), ability to acquire nutrients
(Jakobsen, Smith & Smith 2002), ability to solubilise nutrients
from organic matter and plant host range (Molina, Massicotte
& Trappe 1992). Moreover, mycorrhizal fungi have evolved
mechanisms for recognizing and preventing fusion of non self
tissue. For instance, in AM fungi, hyphal fusions have only
been observed between individuals of the same genotype while
fusion between individuals of different genotypes, species or
families do not occur (Giovannetti, Azzonlini & Citernesi
1999; but see Croll et al. 2009). Soils are, thus, colonized by
several independent networks simultaneously competing for
nutrients and roots. Moreover, in many cases mycorrhizal
plants acquire nutrients not directly from the soil in competi-
tion with other plants, but from their fungal networks. A fun-
gus may compete with other fungi for soil nutrients, and then
deliver those nutrients to the various plants it colonizes. The
distribution of the nutrients to plants in a network are then a
function of variations in compatibility between a fungal indi-
vidual and its colonized plant hosts, and variation in carbon
flow to the fungus among the plants.
Mycorrhizal networks and plant–plant
interactions
The role of mycorrhizal networks in regulating plant–plant
interactions and plant community dynamics is still poorly
understood. From our analysis it follows that seedlings of
several plant species benefit from the presence of mycorrhizal

1146 M. G. A. van der Heijden & T. R. Horton
networks. The effect of mycorrhizal networks on interactions
between already established plants is still poorly understood.
In particular it is unclear if there are plant species that maintain
mycorrhizal networks through carbon supply while there are
other species that benefit by acquiring nutrients present in the
network (other than the obvious examples of mycohetero-
trophic plants). Physiological studies such as those by Voets
et al. (2008), performed under sterile in vitro conditions are
necessary to investigate this in detail. Plant competition experi-
ments show that not all plant species receive equal benefit from
mycorrhizal networks (e.g. Finlay 1989; Perry et al. 1989;
Scheublin, Van Logtestijn & Van der Heijden 2007). For
instance, several studies showed that Festuca ovina can benefit
from mycorrhizal fungi when grown alone but, in competition,
its competitive ability is reduced compared with other plants
(van der Heijden et al. 1998; Scheublin, Van Logtestijn & Van
der Heijden 2007). This indicates that the cost–benefit ratio of
plants connected to a mycorrhizal network is not the same for
each plant species. Microcosm studies have also shown that
AM fungi alter plant diversity and plant community structure
(Grime et al. 1987; van der Heijden et al. 1998; Hartnett &
Wilson 1999) because different plant species receive different
amounts of benefit from mycorrhizal network. Moreover, the
composition and number of mycorrhizal fungi present in plant
communities is also important in determining plant productiv-
ity and plant diversity (van der Heijden et al. 1998; Klirono-
mos et al. 2000; Vogelsang, Reynolds & Bever 2006). Studies
with microcosms are of particular interest because the plants
are coexisting and plants can be colonized by the same fungi.
In communities with several mycorrhizal fungi (most EM
communities have tens of species), different plant species can
be colonized by different mycorrhizal fungi and it is even possi-
ble that guilds of plants exist interconnected by the same
mycorrhizal networks (although no proof for this has been
obtained). Molecular techniques that detect specific mycorrhi-
zal fungi, could test whether this is actually happening. More-
over, different mycorrhizal networks are likely to coexist in
mixed forests where trees associate both with AM and EM
fungi, or in EM forests with an understorey of AM herbs
(Newman & Redell 1988). Some mycorrhizal fungi can also
form functional associations with plants with different mycor-
rhizal types as was recently shown for the fungus Piceirhiza
bicolorata (Grelet et al. 2009).
Carbon and mineral nutrient transfer through
mycorrhizal networks
One important consequence of mycorrhizal networks is that
nutrients, carbon and water can be transferred from one plant
to another. The significance of interplant carbon & nutrient
transfer has been widely debated (see reviews by Simard, Dur-
all & Jones 2002 & Selosse et al. 2006). Selosse et al. (2006)
estimated that up to 40% of plant nitrogen in receiver plants
can be derived from donor plants (e.g. nitrogen fixing plants)
and be transferred through mycorrhizal networks. In most sit-
uations this proportion is probably much lower, as nitrogen is
usually limiting plant productivity, making it unlikely that
 2009 The Authors. Journal compilation  2009 British Ecological Society, Journal of Ecology, 97, 1139–1150
13652745, 2009, 6, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2009.01570.x by Test, Wiley Online Library on [09/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
plants give it away for ‘free’. Moreover, nitrogen fixation by
nitrogen fixing plants is energetically expensive, implying that
direct transfer from a nitrogen fixer to a non-nitrogen fixer is
probably low. The significance of interplant carbon transfer
has been unequivocally shown in mycoheterotrophic plants
which parasitize on mycorrhizal networks from which they
obtain carbon and nutrients (see above). In addition, evidence
for carbon movement between green plants comes from Sim-
ard et al. (1997) and Lerat et al. (2002). There is debate about
the ecological significance of C transfer between plants via
mycorrhizal networks (Robinson & Fitter 1999). Graves et al.
(1997) and Wu, Nara & Hogetsu (2001) have shown that C
fixed by one plant and transferred to another remains in the
root system, and presumably the hyphae, of the second plant.
However, C must move out of the root system in mycohetero-
trophs and the studies by Simard and Lerat suggest this can
happen in green plants as well. What is not clear in these stud-
ies is the source of the carbon translocated from the fungi. It is
likely that some of the C atoms are part of amino acids such as
glutamine or glutamate that are transferred as N sources to the
plants from the fungi. How these amino acids influence the
energy budget of these plants, especially those that cannot fix
their own carbon, remains to be determined.
Ecological function of mycorrhizal fungal
networks
Mycorrhizal fungal networks provide a wide range of services
to plants and ecosystems (Table 2). The most important one is
probably nutrient uptake, followed by seedling support (see
analysis). Other functions, such as the prevention of nutrient
leaching, internal cycling of nutrients (e.g. transfer of nutrient
from dying roots and leaf litter) and their ability to facilitate
bacterial dispersion, have been largely overlooked (Table 2).
Moreover, the fact that seedlings in perennial plant communi-
ties become quickly colonized by mycorrhizal fungi (e.g. within
3–6 days after seedling emergence (Read, Koucheki & Hodg-
son 1976; Birch 1986) is probably very important because small
seedlings then have immediate access to a cheap ‘nutrient
adsorption machine’ provided and maintained by the sur-
rounding vegetation (Newman 1988). Plant growth in many
communities (e.g. grassland or savanna) is limited by nutrient
availability and not by light availability. Hence, a connection
to mycorrhizal networks (as a source of inoculum) is extremely
important for plant survival, even if seedlings have to supply
carbon to maintain their own small part of the fungal network.
However, the function of hyphal networks is less clear in eco-
systems where light availability is the main limiting factor for
seedling establishment. For instance, enhanced mycorrhizal
colonization did not improve seedling survival in a tropical forest
(Gehring & Connell 2006). Work by Simard et al. (1997)
showed that tree seedlings in forest obtain carbon from
mycorrhizal networks. This may enhance seedling survival,
although experimental evidence for this is still unclear.
The importance of mycorrhizal networks for seedling estab-
lishment has been known for some time and this is now also
being applied in forestry and agriculture. Moreover, a manage-
 13652745, 2009, 6, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2009.01570.x by Test, Wiley Online Library on [09/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Socialism in soil? The importance of mycorrhizal fungal networks 1147

Table 2. Ecological functions and significance of mycorrhizal fungal networks and of the presence of mycorrhizal fungi

Ecological
Function significance References

Direct effects of mycorrhizal networks

Facilitation of seedling establishment Low to See literature analysis in this paper
very high
Rapid colonization of seedlings Very high Read, Koucheki & Hodgson 1976
Increased mycorrhizal inoculum potential High Newman 1988; Dickie et al. 2005; Dickie & Reich
of soil around established plants 2005; Nara 2006b; Nuñez, Horton & Simberloff
Reduced seedling costs of establishing High Newman 1988
mycorrhizal associations
Prevention of nutrient leaching High* van der Heijden 2009
Transfer of nutrients from dying roots High Ritz & Newman 1985; Mikkelsen, Rosendahl &
Jakobsen 2008
Transport of substances between plants
transfer of carbon Probably low Simard et al. 1997; Robinson & Fitter 1999;
Lerat et al. 2002
transfer of phosphorus Probably low Simard, Durall & Jones 2002; Selosse et al. 2006
transfer of nitrogen Still unclear He et al. 2005; Selosse et al. 2006;
transfer of water Unknown
transfer of plant signals Unknown
Changes in fungal community composition and High Bever, Westover & Antonovics 1997; Collier &
abundance (including plant–soil feedback) Bidartondo 2009; Hubert & Gehring 2008

Ecological functions of the presence of mycorrhizal fungi

Nutrient uptake Very high Summarized in van der Heijden, Bardgett &
van Straalen 2008
Decomposition of litter High Lindahl et al. 2007
Improvement of soil structure by enmeshing soil High Rillig & Mummey 2006
aggregates in stable structures
Carbon transfer to soils High†
Water uptake and hypdraulic lift Variable Auge 2001; Egerton-Warburton, Querejeta &
Allen 2007
Hyphal highways for bacterial dispersion Very low Perotto & Bonfante 1997; Kohlmeier et al. 2005
for plants
Food for other organisms Low for plants‡ Gange 2000

*Considerable amounts of nutrients are lost due to leaching and surface run off: in some areas up to 160 kg N and up to 30 kg of phos-
phorus year)1 hectare)1 are lost in this way (Herzog et al. 2008; Sims, Simard & Joern 1998). The prevention of nutrient leaching is espe-
cially important for non-renewable nutrients (e.g. P or K) and in sandy soils or soils where these nutrients cannot be fixed to soil
particles (Sims, Simard & Joern 1998).
†Plant carbon allocation to mycorrhizal fungi in soil is highly variable, between 0 and 20% of plant carbon is allocated to mycorrhizal
fungi (Hobbie 2006; Jakobsen, Smith & Smith 2002).
‡In forests, mycorrhizal fungi often dominate the microbial biomass, with up to 50% of soil dry weight in areas with particular dense
proliferation of mycelia (Ingham et al. 1991). These hyphae can be consumed by a wide range of organisms. However, some studies indi-
cate that mycorrhizal fungal hyphae are not very palatable and do not belong to the diet of collembola, abundant soil arthropods
(Gange 2000).

ment practice in agriculture that is receiving increased atten-
tion is conservation tillage (Holland 2004). Conservation till-
age minimises the disruption of the soil structure, promotes
soil biodiversity and reduces soil erosion and drought stress.
Several studies reported that mycorrhizal networks increase in
abundance under conservation tillage (e.g. Jansa et al. 2003).
It is likely, although not proven, that the positive effects of con-
servation tillage are, at least in part, mediated by mycorrhizal
networks.
Conclusions and outlook
In this review, we have shown that mycorrhizal fungal net-
works play a key role in natural ecosystems. Mycorrhizal fungi
can facilitate seedling establishment and plant growth by
acquiring limiting nutrients. Many plants benefit from fungal
support, but there are also a considerable number of cases
where there is no, or even a negative effect of mycorrhizal
fungi. The results presented in our analysis clearly reflect this
as we observed significant growth stimulation of small seed-
lings by mycorrhizal fungal networks in only 48% of cases,
while negative effects occurred in 25% of the cases. Mycorrhi-
zal fungal networks have the ability to support co-occurring
plants of different sizes, but effects are highly variable. Thus,
mycorrhizal networks do have some similarities to socialist
systems in that small plants can benefit from networks that are
supported by bigger plants in the community. However,
whether this is actually occurring is highly context dependent,
and varies with study system (e.g. plant species identity, fun-
gal identity, nutrient availability). Beside effects on plant

 2009 The Authors. Journal compilation  2009 British Ecological Society, Journal of Ecology, 97, 1139–1150

1148 M. G. A. van der Heijden & T. R. Horton
growth, we identified a number of other important ecological
functions of mycorrhizal networks in soil. These include
recycling of nutrients, prevention of nutrient losses, contribu-
tion to soil structure, food for other organisms, and mycorrhi-
zal fungal networks acting as hyphal highways for bacterial
dispersion.
For a better understanding of the impact of mycorrhizal fun-
gal networks on seedling growth and ecosystem functioning,
several key questions need to be answered. First, cost–benefit
relationships of individual plants connected to mycorrhizal
networks are still poorly understood. It is unclear which plants
invest, and how this is related to the amount of benefit received.
The fact that most (if not all) physiological studies are
performed with single plants, grown in highly simplified study
systems, without hyphal interconnections to other plants, does
not contribute to a better understanding of process occurring
in mycorrhizal networks. The use of dual labelling (with 13C;
14C, 15N 33P) as performed by some investigators is impor-
tant. Second, we have shown here that mycorrhizal net-
works are important for seedling establishment in several
cases. However, in order to draw more precise conclusions,
additional studies are required (e.g. studies with EM fungal
networks showed positive effects in 75% of the cases. However,
this conclusion is based on seven independent studies). Fur-
thermore, as far as we know, there are no studies which tested
whether hyphal networks formed by plants with ericoid or
orchid mycorrhizas promote seedling establishment of nearby
plants. Third, the contribution of mycorrhizal networks to
nutrient uptake by plants and nutrient cycling in natural eco-
systems is still poorly understood and mainly based on experi-
ments performed in the laboratory (but see Hobbie & Hobbie
2006). Fourth, there are many other factors that facilitate seed-
ling establishment and plant growth as discussed in this issue of
the Journal of Ecology. The relevance of mycorrhizal networks
compared with these other factors is often poorly understood.
Fifth, most studies have been performed with mycorrhizal
fungi that can be easily cultured. However, molecular tech-
niques have shown that in the case of AM fungi, 60% of envi-
ronmental sequences do not match with AM fungi that have
been brought into culture (van der Heijden, Bardgett & van
Straalen 2008). Hence, it will be extremely important to culti-
vate these fungi and assess their ecological relevance. Sixth, the
spatial distribution and movement of nutrients in mycorrhizal
networks is still poorly understood. Finally, our climate is
changing and periods of drought or heavy rainfall are expected
to increase in many countries. It is important to understand
how these changes influence the stability of mycorrhizal net-
works and their ability in facilitating plant growth.
Acknowledgements
We would like to thank Erik Lilleskov and Mari Moora for discussion and pro-
viding data. Toby Kiers and David Read commented on a very early version of
this paper. We thank the editor and the two referees for helpful and constructive
comments. Financial support was provided to M.G.A.V.D.H by the Swiss Fed-
eral Government and the Swiss National Science Foundation award
31003A_125428 and to T.R.H by the National Science Foundation award DEB-
0614381, the Mianus River Gorge Preserve, and the USDA Forest Service.
 2009 The Authors. Journal compilation  2009 British Ecological Society, Journal of Ecology, 97, 1139–1150
13652745, 2009, 6, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2009.01570.x by Test, Wiley Online Library on [09/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
References
Aldrich Wolfe, L. (2007) Distinct mycorrhizal communities on new and estab-
lished hosts in a transitional tropical plant community. Ecology, 88, 559–
566.
Auge, R.M. (2001) Water relations, drought and vesicular-arbuscular mycor-
rhizal symbiosis. Mycorrhiza, 11, 3–42.
Bever, J.D., Westover, K.M. & Antonovics, J. (1997) Incorporating the soil
community into plant population dynamics: the utility of the feedback
approach. Journal of Ecology, 85, 561–573.
Bidartondo, M.I., Kretzer, A.M., Pine, E.M. & Bruns, T.D. (2000) High root
concentration and uneven ectomycorrhizal diversity near Sarcodes sangui-
nea (Ericaceae): a cheater that stimulates its victims? American Journal of
Botany, 87, 1783–1788.
Birch, C.P.D. (1986) Development of VA mycorrhizal infection in seedlings in
semi-natural grassland turf. Physiological and Genetic Aspects of Mycorrhi-
zae (eds V. Gianinazzi-Pearson & S. Gianinazzi), pp. 233–237. INRA, Paris,
France.
Brooker, R.W., Maestre, F.T., Callaway, R.M., Lortie, C.L., Cavieres, L.A.,
Kunstler, G. et al. (2008) Facilitation in plant communities: the past, the
present, and the future. Journal of Ecology, 96, 18–34.
Brundrett, M.C. (2009) Mycorrhizal associations and other means of nutrition
of vascular plants: understanding the global diversity of host plants by
resolving conflicting information and developing reliable means of diagnosis.
Plant and Soil, 320, 37–77.
Bucking, H. & Shachar-Hill, Y. (2005) Phosphate uptake, transport and
transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimu-
lated by increased carbohydrate availability. New Phytologist, 165, 899–912.
Callaway, R.M., Brooker, R.W., Choler, P., Kikvidze, Z., Lortie, C.J., Micha-
let, R. et al. (2002) Positive interactions among alpine plants increase with
stress. Nature, 417, 844–848.
Cameron, D.D., Johnson, I., Read, D.J. & Leake, J.R. (2008) Giving and
receiving: measuring the carbon cost of mycorrhizas in the green orchid,
Goodyera repens. New Phytologist, 180, 176–184.
Clements, F.E. (1936) Nature and structure of the climax. Journal of Ecology,
24, 252–284.
Collier, F.A. & Bidartondo, M.I. (2009) Waiting for fungi: the ectomycorrhizal
invasion of lowland heathlands. Journal of Ecology, 97, 950–963.
Connell, J.H. & Lowman, M.D. (1989) Low-diversity tropical rain forests – some
possible mechanismsfor their existence.American Naturalist, 134, 88–119.
Croll, D., Giovannetti, M., Koch, A.M., Sbrana, C., Ehinger, M., Lammers,
P.J. & Sanders, I.R. (2009) Nonself vegetative fusion and genetic exchange in
the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist,
181, 924–937.
Cullings, K.W., Parker, V.T., Finley, S.K. & Vogler, D.R. (2000) Ectomycor-
rhizal specificity patterns in a mixed Pinus contorta and Picea engelmannii
forest in Yellowstone National Park. Applied and Environmental Microbiol-
ogy, 66, 4988–4991.
Dickie, I.A., Koide, R.T. & Steiner, K.C. (2002) Influences of established trees
on mycorrhizas, nutrition, and growth of Quercus rubra seedlings. Ecologi-
cal Monographs, 72, 505–521.
Dickie, I.A. & Reich, P.B. (2005) Ectomycorrhizal fungal communities at forest
edges. Journal of Ecology, 93, 244–255.
Dickie, I.A., Schnitzer, S.A., Reich, P.B. & Hobbie, S.E. (2005) Spatially dis-
junct effects of co-occurring competition and facilitation. Ecology Letters, 8,
1191–1200.
Dulmer, K. (2006). Mycorrhizal associations of American chestnut seedlings: a
lab and field bioassay. Environmental and Forest Biology. p. 106. SUNY-
ESF Syracuse, New York, U.S.A.
Egerton-Warburton, L.M., Querejeta, J.I. & Allen, M.F. (2007) Common
mycorrhizal networks provide a potential pathway for the transfer of
hydraulically lifted water between plants. Journal of Experimental Botany,
58, 1473–1483.
Eissenstat, D.M. & Newman, E.I. (1990) Seedling establishment near large
plants – effects of vesicular –arbuscular mycorrhizas on the intensity of plant
competition. Functional Ecology, 4, 95–99.
Finlay, R.D. (1989) Functional aspects of phosphorus uptake and carbon
translocation in incompatible ectomycorrhizal associations between Pinus
sylvestris and Suillus grevillei and Boletinus cavipes. New Phytologist, 112,
185–192.
Francis, R. & Read, D.J. (1995) Mutualism and antagonism in the mycorrhizal
symbiosis, with special reference to impact on plant community structure.
Canadian Journal of Botany, 73(Suppl. 1), 1301–1309.
Gange, A. (2000) Arbuscular mycorrhizal fungi, collembola and plant growth.
Trends in Ecology & Evolution, 15, 369–372.

Socialism in soil? The importance of mycorrhizal fungal networks 1149
Gehring, C.A. & Connell, J.H. (2006) Arbuscular mycorrhizal fungi in the tree
seedlings of two Australian rain forests: occurrence, colonization, and rela-
tionships with plant performance. Mycorrhiza, 16, 89–98.
Giovannetti, M., Azzonlini, D. & Citernesi, A.S. (1999) Anastomosis forma-
tion and nuclear and protoplasmic exchange in arbuscular mycorrhizal
fungi. Applied and Environmental Microbiology, 65, 5571–5575.
Girlanda, M., Selosse, M.-A., Cafasso, D., Brilli, F., Delfine, S., Fabian, R.,
Ghignone, S., Pinelli, P., Segreto, R., Loreto, F., Cozzolino, S. & Perotto, S.
(2006) Inefficient photosynthesis in the Mediterranean orchid Limodorum
abortivum is mirrored by specific association to ectomycorrhizal Russula-
ceae. Molecular Ecology, 15, 491–504.
Graham, J.H., Duncan, L.W. & Eissenstat, D.M. (1997) Carbohydrate
allocation patterns in citrus genotypes as affected by phosphorus nutrition,
mycorrhizal colonization and mycorrhizal dependency. New Phytologist,
135, 335–343.
Graves, J.D., Watkins, N.K., Fitter, A.H., Robinson, D. & Scrimgeour, C.
(1997) Intraspecific transfer of carbon between plants linked by a common
mycorrhizal network. Plant and Soil, 192, 153–159.
Grelet, G.A., Johnson, D., Paterson, E., Anderson, I.C. & Alexander, I.J.
(2009) Reciprocal carbon and nitrogen transfer between an ericaceous dwarf
shrub and fungi isolated from Piceirhiza bicolorata ectomycorrhizas. New
Phytologist, 182, 359–366.
Grime, J.P., Mackey, J.M.L., Hillier, S.H. & Read, D.J. (1987) Floristic diversity
in a model system using experimental microcosms. Nature, 328, 420–422.
Hartnett, D.C. & Wilson, W.T. (1999) Mycorrhizae influence plant community
structure and diversity in tall grass prairie. Ecology, 80, 1187–1195.
He, X.Y., Critchley, C., Ng, H. & Bledsoe, C. (2005) Nodulated N2-fixing Casu-
arina cunninghamiana is the sink for net N transfer from non-N2-fixing Euca-
lyptus maculata via an ectomycorrhizal fungus Pisolithus sp. using 15NH4+
or 15NO3- supplied as ammonium nitrate. New Phytologist, 167, 897–912.
van der Heijden, M.G.A. (2002). Arbuscular mycorrhizal fungi as a determinant
of plant diversity: in search for underlying mechanisms and general princi-
ples. Ecological Studies 157: Mycorrhizal Ecology (eds M.G.A. van der Heij-
den & I.R. Sanders), pp. 243–263. Springer Verlag, Heidelberg, Germany.
van der Heijden, M.G.A. (2004) Arbuscular mycorrhizal fungi as support sys-
tems for seedling establishment in grassland. Ecology Letters, 7, 293.
van der Heijden, M.G.A. (2009) Mycorrhizal fungi reduce nutrient loss from
model grassland ecosystems. Ecology (in press).
van der Heijden, M.G.A., Bardgett, R.D. & van Straalen, N.M. (2008) The
unseen majority: soil microbes as drivers of plant diversity and productivity
in terrestrial ecosystems. Ecology Letters, 11, 296–310.
van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streit-
wolf-Engel, R., Boller, T., Wiemken, A. & Sanders, I.R. (1998) Mycorrhizal
fungal diversity determines plant biodiversity, ecosystem variability and pro-
ductivity. Nature, 396, 72–75.
Herzog, F., Prasuhn, V., Spiess, E. & Richner, T. (2008) Environmental cross-
compliance mitigatees nitrogen and phosphorus pollution from Swiss agri-
culture. Environmental Science & Policy, 11, 655–668.
Hobbie, E.A. (2006) Carbon allocation to ectomycorrhizal fungi correlates
with belowground allocation in culture studies. Ecology, 87, 563–569.
Hobbie, J.E. & Hobbie, E.A. (2006) 15N in symbiotic fungi and plants esti-
mates nitrogen and carbon flux rates in arctic tundra. Ecology, 87, 816–822.
Holland, J.M. (2004) The environmental consequences of adopting conserva-
tion tillage in Europe: reviewing the evidence. Agriculture Ecosystems &
Environment, 103, 1–25.
Horton, T.R. & Bruns, T.D. (1998) Multiple-host fungi are the most frequent
and abundant ectomycorrhizal types in a mixed stand of Douglas fir (Pseu-
dostuga menziesii) and bishop pine (Pinus muricata). New Phytologist, 139,
331–339.
Horton, T.R., Bruns, T.D. & Parker, T. (1999) Ectomycorrhizal fungi associ-
ated with Arctostaphylos contribute to Pseudotsuga menziesii establish-
ment. Canadian Journal of Botany, 77, 93–102.
Horton, T.R., Molina, R. & Hood, K. (2005) Douglas-fir ectomycorrhizae in
40- and 400- year-old stands: mycobiont availability to later succession wes-
tern hemlock. Mycorrhiza, 15, 393–403.
Horton, T.R. & van der Heijden, M.G.A. (2008) The role of symbiosis in seed-
ling establishment and survival. Seedling Ecology and Evolution (eds M.A.
Leck, V.T. Parker & R.L. Simpson). pp. 189–214, Cambridge University
Press, Cambridge, UK.
Hubert, N.A. & Gehring, C.A. (2008) Neighbouring trees affect ectomycorrhi-
zal fungal community composition in a woodland-forest ecotone. Mycor-
rhiza, 18, 363–374.
Hynson, N.A., Preiss, K., Gebauer, G. & Bruns, T.D. (2009) Isotopic evidence
of full and partial myco-heterotrophy in the plant tribe Pyroleae (Ericaceae).
New Phytologist, 182, 719–726.
 2009 The Authors. Journal compilation  2009 British Ecological Society, Journal of Ecology, 97, 1139–1150
13652745, 2009, 6, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2009.01570.x by Test, Wiley Online Library on [09/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Ingham, E.R., Griffiths, R.P., Cromack, W. & Entry, J.A. (1991) Comparison of
direct vs fumigation incubation microbial biomass estimates from ecto-
mycorrhizal mat and non-mat soils. Soil Biology & Biochemistry, 23, 465–472.
Ishida, T.A., Nara, K. & Hogetsu, T. (2006) Host effects on ectomycorrhizal
fungal communities: insight from eight host species in mixed conifer-broad-
leaf forests. New Phytologist, 174, 430–440.
Jakobsen, I., Smith, S.E. & Smith, F.A. (2002) Function and diversity of arbus-
cular mycorrhizae in carbon and mineral nutrition. Mycorrhizal Ecology
(eds M.G.A. van der Heijden & I.R. Sanders). pp. 75–92, Springer Verlag,
Heidelberg, Germany.
Jansa, J., Mozafar, A., Kuhn, G., Anken, T., Ruh, R., Sanders, I.R. & Fros-
sard, E. (2003) Soil tillage affects the community structure of mycorrhizal
fungi in maize roots. Ecological Applications, 13, 1164–1176.
Johnson, N.C., Graham, J.H. & Smith, F.A. (1997) Functioning of mycorrhi-
zal associations along the mutualism-parasitism continuum. New Phytolo-
gist, 135, 575–585.
Johnson, K.H., Vogt, K.A., Clark, H.J., Schmitz, O.J. & Vogt, D.J. (1996)
Biodiversity and and the productivity and stability of ecosystems. Trends
in Ecology and Evolution, 11, 372–377.
Jonsson, L.M., Nilsson, M.C., Wardle, D.A. & Zackrisson, O. (2001) Context
dependent effects of ectomycorrhizal species richness on tree seedling pro-
ductivity. Oikos, 93, 353–364.
Julou, T., Burghardt, B., Gebauer, G., Berveiller, D., Damesin, C. & Selosse,
M.A. (2005) Mixotrophy in orchids: insights from a comparative study of
green individuals and nonphotosynthetic individuals of Cephalanthera
damasonium. New Phytologist, 166, 639–653.
Karst, J., Marczak, L., Jones, M.D. & Turkington, R. (2008) The mutualism-
parasitism continuum in ectomycorrhizas: a quantitative assessment using
meta-analysis. Ecology, 89, 1032–1042.
Kennedey, P.G., Izzo, A.D. & Bruns, T.D. (2003) There is high potential for
the formation of common mycorrhizal networks between understorey and
canopy trees in a mixed evergreen forest. Journal of Ecology, 91, 1071–1080.
Kiers, E.T. & van der Heijden, M.G.A. (2006) Mutualistic stability in the
arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary
cooperation. Ecology, 87, 1627–1636.
Klironomos, J.N. (2003) Variation in plant response to native and exotic arbus-
cular mycorrhizal fungi. Ecology, 84, 2292–2301.
Klironomos, J.N., McCune, J., Hart, M. & Neville, J. (2000) The influence of
arbuscular mycorrhizae on the relationship between plant diversity and pro-
ductivity. Ecology Letters, 3, 137–141.
Kohlmeier, S., Smits, T.H.M., Ford, R.M., Keel, C., Harms, H. & Wick, L.Y.
(2005) Taking the fungal highway, Mobilization of pollutant-degrading bac-
teria by fungi. Environment. Science & Technology, 39, 4640–4646.
Korner, C. (2003) Carbon limitation in trees. Journal of Ecology, 91, 4–17.
Kytoviita, M.M., Vestberg, M. & Tuom, J. (2003) A test of mutual aid in com-
mon mycorrhizal networks: established vegetation negates benefit in seed-
lings. Ecology, 84, 898–906.
Leake, J.R. (1994) The biology of myco-heterotrophic (‘saprophytic’) plants.
New Phytologist, 127, 171–216.
Leake, J.R., Johnson, D., Donnelly, D.P., Muckle, G.E., Boddy, L. & Read,
D.J. (2004) Networks of power and influence: the role of mycorrhizal myce-
lium in controlling plant communities and agroecosystem functioning.
Canadian Journal of Botany, 82, 1016–1045.
Lerat, S., Rachel, R., Catford, J.G., Vierheilig, H., Piché, Y. & Lepointe, L.
(2002) 14C transfer between the spring ephemeral Erythronium ameicanum
and sugar maple saplings via arbuscular mycorrhizal fungi in natural stands.
Oecologia, 132, 181–187.
Lian, C.L., Narimatsu, M., Nara, K. & Hogetsu, T. (2006) Tricholoma matsu-
take in a natural Pinus densiflora forest: correspondence between above- and
below-ground genets, association with multiple host trees and alteration of
existing ectomycorrhizal communities. New Phytologist, 171, 825–836.
Lilleskov, E.A., Fahey, T.J., Horton, T.R. & Lovett, G.M. (2002) Below-
ground ectomycorrhizal fungal community change over a nitrogen deposi-
tion gradient in Alaska. Ecology, 83, 104–115.
Lindahl, B.D., Ihrmark, K., Boberg, J., Trumbore, S.E., Hogberg, P., Stenlid,
J. & Finlay, R.D. (2007) Spatial separation of litter decomposition and
mycorrhizal nitrogen uptake in a boreal forest. New Phytogist, 173, 611–620.
Marler, M.J., Zabinski, C.A. & Callaway, R.M. (2004) Mycorrhizae indirectly
enhance competitive effects of an invasive forb on a native bunchgrass. Ecol-
ogy, 80, 1180–1186.
Mikkelsen, B.L., Rosendahl, S. & Jakobsen, I. (2008) Underground resource
allocation between individual networks of mycorrhizal fungi. New Phytolo-
gist, 180, 890–898.
Molina, R., Massicotte, H. & Trappe, J.M. (1992) Specificity phenomena in
mycorrhizal symbioses: community-Ecological consequences and practical

1150 M. G. A. van der Heijden & T. R. Horton
implications. Mycorrhizal Functioning an Integrative Plant–Fungal Process
(ed M.F. Allen). pp. 357–423, Chapman and Hall, New York.
Moora, M. & Zobel, M. (1998) Can arbuscular mycorrhiza change the effect of
root competition between conspecific plants of different ages? Canadian
Journal of Botany, 76, 613–619.
Moora, M. & Zobel, M. (2009) Arbuscular mycorrhiza and plant-plant interac-
tions – impact of invisible world on visible patterns. Positive Interactions and
Plant Community Dynamics (ed. F.I. Pugnaire). CRC Press, Boca Ration,
FL, USA (in press).
Nagy, R., Drissner, D., Amrhein, N., Jakobsen, I. & Bucher, M. (2009) Mycor-
rhizal phosphate uptake pathway in tomato is phosphorus-repressible and
transcriptionally regulated. New Phytologist, 181, 950–959.
Nakano-Hylander, A. & Olsson, P.A. (2007) Carbon allocation in mycelia of
arbuscular mycorrhizal fungi during colonisation of plant seedlings. Soil
Biology & Biochemistry, 39, 1450–1458.
Nara, K. (2006a) Ectomycorrhizal networks and seedling establishment during
early primary succession. New Phytologist, 169, 169–178.
Nara, K. (2006b) Pioneer dwarf willow may facilitate tree succession by provid-
ing late colonizers with compatible ectomycorrhizal fungi in a primary suc-
cessional volcanic dessert. New Phytologist, 171, 187–198.
Nara, K. & Hogetsu, T. (2004) Ectomycorrhizal fungi on established shrubs
facilitate subsequent seedling establishment of successional plant species.
Ecology, 85, 1700–1707.
Nehls, U., Grunze, N., Willmann, M., Reich, M. & Kuster, H. (2007) Sugar for
my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. Phyto-
chemistry, 68, 82–91.
Newman, E.I. (1988) Mycorrhizal links between plants: their functioning and
ecological significance. Advances in Ecological Research, 18, 243–270.
Newman, E.I. & Redell, P. (1988) Relationship between mycorrhizal infection
and diversity in vegetation: evidence from the Great Smoky Mountains.
Functional Ecology, 2, 259–262.
Nuñez, M.A., Horton, T.R. & Simberloff, D. Lack of belowground mutual-
isms hinders Pinaceae invasions. Ecology, 90, 2352–2359.
Ocampo, J.A. (1986) Vesicular arbuscular mycorrhizal infection of host and
nonhost plants – effect on the growth-response of the plants and competition
between them. Soil Biology & Biochemistry, 18, 607–610.
Oehl, F., Sieverding, E., Ineichen, K., Mäder, P., Boller, T. & Wiemken, A.
(2003) Impact of land use intensity on the species diversity of arbuscular
mycorrhizal fungi in agroecosystems of Central Europe. Applied and Envi-
ronmental Microbiology, 69, 2816–2824.
Olsson, P.A., Jakobsen, I. & Wallander, H. (2002) Foraging and resource allo-
cation strategies of mycorrhizal fungi in a patchy environment. Mycorrhizal
Ecology (eds M.G.A. van der Heijden & I.R. Sanders). pp. 93–115, Springer-
Verlag Berlin, Germany.
Opik, M., Moora, M., Liira, J. & Zobel, M. (2006) Composition of root-colo-
nizing arbuscular mycorrhizal fungal communities in different ecosystems
around the globe. Journal of Ecology, 94, 778–790.
Perotto, S. & Bonfante, P. (1997) Bacterial associations with mycorrhizal fungi:
close and distant friends in the rhizosphere. Trends in Microbiology, 5, 496–
501.
Perry, D.A., Margolis, H., Choquette, C., Molina, R. & Trappe, J.M. (1989)
Ectomycorrhizal mediation of competition between coniferous tree species.
New Phytologist, 112, 501–511.
Pietikainen, A. & Kytoviita, M.M. (2007) Defoliation changes mycorrhizal
benefit and competitive interactions between seedlings and adult plants.
Journal of Ecology, 95, 639–647.
Plattner, I. & Hall, I.R. (1995) Parasitism of non-host plants by the mycorrhizal
fungus Tuber melanosporum. Mycological Research, 99, 1367–1370.
Poorter, H. & de Jong, R. (1999) A comparison of specific leaf area, chemical
composition and leaf construction costs of field plants from 15 habitats dif-
fering in productivity. New Phytologist, 143, 163–176.
Read, D.J. (1991) Mycorrhizas in ecosystems. Experientia, 47, 376–391.
Read, D.J., Koucheki, H.K. & Hodgson, J. (1976) Vesicular-arbuscular mycor-
rhiza in natural vegation systems. I. The occurrence of infection. New Phytol-
ogist, 77, 641–654.
Rillig, M.C. & Mummey, D.L. (2006) Mycorrhizas and soils structure. New
Phytologist, 171, 41–53.
Ritz, K. & Newman, E.I. (1985) Evidence for rapid recycling of phosphorus
from dying roots to living plants. Oikos, 45, 174–180.
Robinson, D. & Fitter, A.H. (1999) The magnitude and control of carbon
transfer between plants linked by a common mycorrhizal network. Journal
of Experimental Botany, 50, 9–13.
Sapp, J. (2004) The dynamics of symbiosis: an historical overview. Canadian
Journal of Botany, 82, 1046–1056.
 2009 The Authors. Journal compilation  2009 British Ecological Society, Journal of Ecology, 97, 1139–1150
13652745, 2009, 6, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2009.01570.x by Test, Wiley Online Library on [09/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Scheublin, T.R., Van Logtestijn, R.S.P. & Van der Heijden, M.G.A. (2007)
Presence and identity of arbuscular mycorrhizal fungi influence competitive
interactions between plant species. Journal of Ecology, 95, 631–638.
Schüßler, A., Schwarzott, D. & Walker, C. (2001) A new fungal phylum, the
Glomeromycota: phylogeny and evolution. Mycological Research, 105,
1413–1421.
Selosse, M.-A., Richard, R., He, X. & Simard, S.W. (2006) Mycorrhizal networks:
des liaisons dangereuses. Trends in Ecology and Evolution, 21, 621–628.
Sikes, B.A., Cottenie, K. & Klironomos, J.N. (2009) Plant and fungal identity
determines pathogen protection of plant roots by arbuscular mycorrhizas.
Journal of Ecology, DOI: 10.1111/j.1365-2745.2009.01557.x.
Simard, S.W., Durall, D. & Jones, M. (2002) Carbon and nutrient fluxes within
and between mycorrhizal plants. Mycorrhizal Ecology (eds M.G.A. van der
Heijden & I.R. Sanders). pp. 33–74, Springer-Verlag Berline, Germany.
Simard, S.W., Perry, D.A., Smith, J.E. & Molina, R. (1997) Effects of soil
trenching on occurrence of ectomycorrhizas on Pseudotsuga menziesii seed-
lings grown in mature forests of Betula papyrifera and Pseudotsuga menziesii.
New Phytologist., 136, 327–340.
Sims, J.T., Simard, R.R. & Joern, B.C. (1998) Phosphorus loss in agricultural
drainage: historical perspective and current research. Journal of Environmen-
tal Quality, 27, 277–293.
Smith, F.A., Grace, E.J. & Smith, S.E. (2009) More than a carbon economy:
nutrient trade and ecological sustainability in facultative arbuscular mycor-
rhizal symbiosis. New Phytologist, 182, 347–358.
Smith, S.E. & Read, D.J. (2008) Mycorrhizal Symbiosis, 3rd edn. Academic
Press, London, UK.
Taylor, D.L., Bruns, T.D., Leake, J.R. & Read, D.J. (2002) Mycorrhizal speci-
ficity and function in myco-heterotrophic plants. Ecological Studies 157:
Mycorrhizal Ecology (eds M.G.A. van der Heijden & I. Sanders). pp. 375–
413, Springer Verlag, Heidelberg, Germany.
Tedersoo, L., Pellet, P., Koljag, U. & Selosse, M.E. (2007) Parallel evolutionary
paths to mycoheterotrophy in understorey Ericaceae and Orchidaceae: eco-
logical evidence for mixotrophy in Pyroleae. Oecologia, 151, 206–217.
Vandenkoornhuyse, P., Ridgway, K.P., Watson, I.J., Fitter, A.H. & Young,
J.P.W. (2003) Co-existing grass species have distinctive arbuscular mycorrhi-
zal communities. Molecular Ecology, 12, 3085–3095.
Voets, L., Goubau, I., Olsson, P.A., Merckx, R. & Declerck, S. (2008) Absence
of carbon transfer between Medicago truncatula plants linked by a mycor-
rhizal network, demonstrated in an experimental microcosm. FEMS Micro-
biology Ecology, 65, 350–360.
Vogelsang, K.M., Reynolds, H.L. & Bever, J.D. (2006) Mycorrhizal fungal
identity and richness determine the diversity and productivity of a tallgrass
prairie system. New Phytogist, 172, 554–562.
Wallenda, T. & Kottke, I. (1998) Nitrogen deposition and ectomycorrhizas.
New Phytologist, 139, 169–187.
Wang, B. & Qiu, Y.L. (2006) Phylogenetic distribution and evolution of mycor-
rhizas in land plants. Mycorrhiza, 16, 299–363.
Wu, B., Nara, K. & Hogetsu, T. (2001) Can 14C-labelled photosynthetic prod-
ucts move between Pinus densiflora seedlings linked by ectomycorrhizal myc-
elia? New Phytologist, 149, 137–146.
Yoneyama, K., Yoneyama, K., Takeuchi, Y. & Sekimoto, H. (2007) Phospho-
rus deficiency in red clover promotes exudation of orobanchol, the signal for
mycorrhizal symbionts and germination stimulant for root parasites. Planta,
225, 1031–1038.
Received 8 May 2009; accepted 13 August 2009
Handling Editor: Rob Brooker
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