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Mycorrhizal networks: a review of their extent, function, and importance 1 Suzanne W. Simard and Daniel M. Durall Abstract: It is well known from laboratory studies that a single mycorrhizal fungal isolate can colonize different plant species, form interplant linkages, and provide a conduit for interplant transfer of isotopic carbon, nitrogen, phosphorus, or water. There is increasing laboratory and field evidence that the magnitude and direction of transfer is influenced by physiological source–sink gradients between plants. There is also evidence that mycorrhizal fungi play a role in regu- lating transfer through their own source–sink patterns, frequency of links, and mycorrhizal dependency. Although it is plausible that connections are extensive in nature, field studies have been hampered by our inability to observe them in situ and by belowground complexity. In future, isotopic tracers, morphological observations, microsatellite techniques, and fluorescent dyes will be useful in the study of networks in nature. Mycorrhizal networks have the potential to in- fluence patterns of seedling establishment, interplant competition, plant diversity, and plant community dynamics, but studies in this area are just beginning. Future plant community studies would benefit from concurrent experimental use of fungal network controls, isotopic labeling, direct observation of interplant linkages, and long-term observation in the field. In this paper, we review recent literature on mycorrhizal networks and interplant carbon transfer, suggest future research directions, and highlight promising scientific approaches. Key words: common mycorrhizal network, carbon transfer, source–sink, establishment, competition, diversity. Résumé : Les études conduites en laboratoire démontrent très bien qu’un seul isolat fongique mycorhizien peut coloni- ser différentes espèces de plantes, former des liens interplants et constituer un conduit pour le transfert d’eau ou de carbone isotopique, d’azote et de phosphore entre les plants. Il existe également des preuves, au laboratoire aussi bien que sur le terrain, que l’ordre de grandeur et la direction du transfert sont influencés par les gradients source–puit entre les plants. On a aussi démontré que les champignons mycorhiziens jouent un rôle dans la régulation du transfert via leur propre patron source–puit, la fréquence des liens, et la dépendance mycorhizienne. Bien qu’il soit plausible que les liens soient extensifs en nature, les études aux champs sont rendues difficiles par notre incapacité à les observer in situ, ainsi que par la complexité du milieu hypogé. L’étude des réseaux en nature devra faire appel à des techniques telles que les traceurs isotopiques, les observations morphologiques, l’analyse par microsatellites, et les colorants fluorescents. Les réseaux mycéliens ont le potentiel d’influencer les patrons d’établissement des plantules, la compétition interplant, la diversité végétale, et la dynamique des communautés, mais les études sur ce sujet ne font que commencer. Les nou- velles études sur les communautés végétales gagneraient à utiliser expérimentalement et de façon concomitante le con- trôle des réseaux fongiques, le marquage isotopique, l’observation directe des connections interplants, et les observations à long terme sur le terrain. Cette revue de la littérature récente, sur les réseaux mycorhiziens et le trans- fert interplants de carbone, suggère de nouvelles avenues de recherches et des approches scientifiques prometteuses. Mots clés : réseau mycorhizien commun, transfert de carbone, source–puit, établissement, compétition, diversité. [Traduit par la Rédaction] Simard and Durall 1165 Introduction The terms mycorrhizal network and common mycorrhizal network (CMN) have recently been used by mycor- rhizoligists. A CMN occurs where two or more root systems are interconnected by mycorrhizal fungal hyphae. Mycor- rhizal networks have been shown to function by transferring carbon (C) or nutrients from one plant to another (Finlay and Read 1986a, 1986b), but CMNs can also exist regard- less of whether they are involved with interplant elemental transfer. For example, CMNs may allow movement of nutri- ents or C within the fungal mycelium, but without ever transferring elements into the tissue of plants interconnected by the CMN. Thus, CMNs may or may not function with respect to interplant elemental transfer. The CMN can involve multiple fungal and plant species within a community. One of the simplest mycorrhizal net- works occurs when the mycelium of one fungal individual connects two plants of the same species. The complexity of the network increases with increasing numbers of fungal species, frequency of connections, number of plants within a Can. J. Bot. 82: 1140–1165 (2004) doi: 10.1139/B04-116 © 2004 NRC Canada 1140 Received 22 September 2003. Published on the NRC Research Press Web site at http://canjbot.nrc.ca on 3 September 2004. S.W. Simard. 2 Forest Science Department, University of British Columbia, 2424 Main Mall, Vancouver, BC V6T 1Z4, Canada. D.M. Durall. Biology Department, Okanagan University College, 3333 College Way, Kelowna, BC V1V 1V7, Canada. 1 This article is one of a selection of papers published in the Special Issue on Mycorrhizae and was presented at the Fourth International Conference on Mycorrhizae. 2 Corresponding author (e-mail: [email protected]).

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Page 1: Mycorrhizal networks: a review of their extent, function, and

Mycorrhizal networks: a review of their extent,function, and importance1

Suzanne W. Simard and Daniel M. Durall

Abstract: It is well known from laboratory studies that a single mycorrhizal fungal isolate can colonize different plantspecies, form interplant linkages, and provide a conduit for interplant transfer of isotopic carbon, nitrogen, phosphorus,or water. There is increasing laboratory and field evidence that the magnitude and direction of transfer is influenced byphysiological source–sink gradients between plants. There is also evidence that mycorrhizal fungi play a role in regu-lating transfer through their own source–sink patterns, frequency of links, and mycorrhizal dependency. Although it isplausible that connections are extensive in nature, field studies have been hampered by our inability to observe them insitu and by belowground complexity. In future, isotopic tracers, morphological observations, microsatellite techniques,and fluorescent dyes will be useful in the study of networks in nature. Mycorrhizal networks have the potential to in-fluence patterns of seedling establishment, interplant competition, plant diversity, and plant community dynamics, butstudies in this area are just beginning. Future plant community studies would benefit from concurrent experimental useof fungal network controls, isotopic labeling, direct observation of interplant linkages, and long-term observation in thefield. In this paper, we review recent literature on mycorrhizal networks and interplant carbon transfer, suggest futureresearch directions, and highlight promising scientific approaches.

Key words: common mycorrhizal network, carbon transfer, source–sink, establishment, competition, diversity.

Résumé : Les études conduites en laboratoire démontrent très bien qu’un seul isolat fongique mycorhizien peut coloni-ser différentes espèces de plantes, former des liens interplants et constituer un conduit pour le transfert d’eau ou decarbone isotopique, d’azote et de phosphore entre les plants. Il existe également des preuves, au laboratoire aussi bienque sur le terrain, que l’ordre de grandeur et la direction du transfert sont influencés par les gradients source–puit entreles plants. On a aussi démontré que les champignons mycorhiziens jouent un rôle dans la régulation du transfert vialeur propre patron source–puit, la fréquence des liens, et la dépendance mycorhizienne. Bien qu’il soit plausible que lesliens soient extensifs en nature, les études aux champs sont rendues difficiles par notre incapacité à les observer in situ,ainsi que par la complexité du milieu hypogé. L’étude des réseaux en nature devra faire appel à des techniques tellesque les traceurs isotopiques, les observations morphologiques, l’analyse par microsatellites, et les colorants fluorescents.Les réseaux mycéliens ont le potentiel d’influencer les patrons d’établissement des plantules, la compétition interplant,la diversité végétale, et la dynamique des communautés, mais les études sur ce sujet ne font que commencer. Les nou-velles études sur les communautés végétales gagneraient à utiliser expérimentalement et de façon concomitante le con-trôle des réseaux fongiques, le marquage isotopique, l’observation directe des connections interplants, et lesobservations à long terme sur le terrain. Cette revue de la littérature récente, sur les réseaux mycorhiziens et le trans-fert interplants de carbone, suggère de nouvelles avenues de recherches et des approches scientifiques prometteuses.

Mots clés : réseau mycorhizien commun, transfert de carbone, source–puit, établissement, compétition, diversité.

[Traduit par la Rédaction] Simard and Durall 1165

Introduction

The terms mycorrhizal network and common mycorrhizalnetwork (CMN) have recently been used by mycor-

rhizoligists. A CMN occurs where two or more root systemsare interconnected by mycorrhizal fungal hyphae. Mycor-rhizal networks have been shown to function by transferringcarbon (C) or nutrients from one plant to another (Finlayand Read 1986a, 1986b), but CMNs can also exist regard-less of whether they are involved with interplant elementaltransfer. For example, CMNs may allow movement of nutri-ents or C within the fungal mycelium, but without evertransferring elements into the tissue of plants interconnectedby the CMN. Thus, CMNs may or may not function withrespect to interplant elemental transfer.

The CMN can involve multiple fungal and plant specieswithin a community. One of the simplest mycorrhizal net-works occurs when the mycelium of one fungal individualconnects two plants of the same species. The complexity ofthe network increases with increasing numbers of fungalspecies, frequency of connections, number of plants within a

Can. J. Bot. 82: 1140–1165 (2004) doi: 10.1139/B04-116 © 2004 NRC Canada

1140

Received 22 September 2003. Published on the NRCResearch Press Web site at http://canjbot.nrc.ca on3 September 2004.

S.W. Simard.2 Forest Science Department, University ofBritish Columbia, 2424 Main Mall, Vancouver, BC V6T 1Z4,Canada.D.M. Durall. Biology Department, Okanagan UniversityCollege, 3333 College Way, Kelowna, BC V1V 1V7, Canada.

1This article is one of a selection of papers published in theSpecial Issue on Mycorrhizae and was presented at theFourth International Conference on Mycorrhizae.

2Corresponding author (e-mail: [email protected]).

Page 2: Mycorrhizal networks: a review of their extent, function, and

species, and number of plant species. Complexity of CMNeffects also increases with interactions with other soil organ-isms, such as earthworms, nematodes, or bacteria.

The CMN has the potential to influence plant survival andgrowth by influencing C and nutrient status of individualplants. Research in this area has focused mainly on seedlingestablishment in the neighbourhood of larger trees sharingthe same fungal species. Growth of plants already estab-lished may also be affected to different degrees by the CMN,potentially altering intra- and inter-specific competitive in-teractions among plants within a plant community. Shifts incompetitive interactions could then affect dominance andevenness within a plant community, thereby affecting plantspecies diversity and structure.

In this paper, we review recent advances in the study ofmycorrhizal networks and C transfer, focusing primarily onliterature between 1997 and 2003. We build on earlier re-views by Newman (1988), Miller and Allen (1992), Fitter(2001), and Simard et al. (2002). The review focuses primar-ily on C transfer because it has been the focus of our ownresearch, as well as that of much of the recent literature, andwe refer readers to Simard et al. (2002) for our earlier re-view of nitrogen (N) and phosphorus (P) transfers. Wedevelop our discussion first by reviewing evidence for theexistence and size of CMNs, second by summarizing studiesthat have examined CMN-mediated C transfer betweenplants, and third by providing evidence for plant and fungalfactors that influence transfer. These sections provide back-ground for a more theoretical discussion of potential CMNand transfer influences on feedbacks among plants andmycorrhizal fungi. Finally, we discuss the potential influ-ences that CMNs may have on plant community dynamics(plant establishment, interplant competition, and plant diver-sity) using supporting evidence from the literature. In thecourse of our review, we identify areas in need of furtherstudy and suggest promising scientific approaches for exam-ining mycorrhizal networks.

Evidence for the existence and size of mycorrhizalnetworks

Newman (1988) suggested that many of the mycorrhizalplants growing together in forests or grasslands may be in-terconnected by a CMN and that this could have profoundimplications for ecosystem functioning. Only in laboratorystudies, however, have the concurrent existence of mycor-rhizal networks and transfer of elements from one root sys-tem to another been conclusively demonstrated (McKendricket al. 2000; Wu et al. 2001). Direct physical and functionalevidence of interplant hyphal linkages (listed in Table 1) hasalso been reported in several earlier studies using macro-scopic, microscopic, and autoradiographic tracings withintransparent laboratory microcosms for ectomycorrhizal(ECM) fungi (Reid and Woods 1969; Read et al. 1985; Fin-lay and Read 1986a, 1986b; Arnebrant et al. 1993; Wu et al.2001) and for arbuscular mycorrhizal (AM) fungi (Hirreland Gerdemann 1979; Francis and Read 1984). Some of themost conclusive evidence for ecologically significant levelsof C transfer occurs between conifers and myco-heterotrophic plants in the families Orchidaceae and Montro-paceae. In this relationship, the myco-heterotrophic plantreceives most or all of its C from an ECM fungal symbiont,

which links the myco-heterotrophic plant to a chloro-phyllous plant (Bjorkman 1960; McKendrick et al. 2000).Myco-heterotrophic plants can also be specialists with AMfungi, as shown recently by Bidartondo et al. (2002), butthere currently exists no direct evidence of C transfer facili-tated by AM fungi as it does with ECM fungi. Given that Ccan move from a chlorophyllous plant into a myco-heterotrophic plant via ECM hyphal links, it is our view thatC could also move into the shoot of a chlorophyllous plant,provided there is a strong enough source–sink gradient fororganic compounds. This topic is discussed further in a latersection.

In the field, direct observations of interplant hyphal link-ages are rare due to the small, hyaline, and interminglingnature of mycorrhizal hyphae (Newman 1988) and due todifficulties in restricting root and fungal growth to two di-mensions for enhanced visibility. Interplant C transfer be-tween plant species pairs sharing ECM (Simard et al. 1997a)and AM fungi (Lerat et al. 2002) has been measured in thefield, with small or negligible transfer to incompatiblemycorrhizal host plants, strongly suggesting that transferoccurred predominantly through a CMN pathway. In thesestudies, however, the mycorrhizal pathway was not visuallyquantified using autoradiography, leaving the identity of thetransfer pathway in question. Notably, all field studies on Ctransfer suffer from this shortcoming.

Additional evidence for mycorrhizal networks exists fromboth lab and field studies, showing low specificity (at leastat the species level) among mycorrhizal fungi and hostplants (van der Heidjden and Sanders 2002; Bruns et al.2002b). There is considerable evidence that many AM fungihave low host specificity (van der Heijden et al. 2003), eventhough a recent study suggests there is more specificityamong AM fungi than originally thought (Helgason et al.2002). ECM conifer and angiosperm hosts are also colo-nized more prevalently by generalist fungi (Horton andBruns 1998; Sakakibara et al. 2002) than by specialists. Oneexample of a specialist association occurs among myco-heterotrophic plant species, which associate with a narrowspecies group of ECM fungi (Bidartondo and Bruns 2002)and AM fungi (Bidartondo et al. 2002). More commonly,however, using morphotyping techniques, ECM fungal spe-cies or genera have been shown to colonize different individ-uals of the same plant species (Kranabetter et al. 1999)or different plant species (Jones et al. 1997; Simard et al.1997b). The use of molecular techniques, such as restrictionfragment length polymorphism (RFLP) and sequencing ofthe polymerase chain reaction (PCR)-amplified internal tran-scribed spacer region, confirm morphotyping studies show-ing that most ECM fungal species associate with multipleplant host species (Horton and Bruns 1998; Horton etal. 1999; Hagerman et al. 2001; Sakakibara et al. 2002;P.G. Kennedy, personal communication). These studies sug-gest there is a high potential for mycorrhizal networks inboth ECM and AM plant communities.

Specificity may also occur below the species level(Vrålstad et al. 2002). Although the same mycorrhizal fun-gal species may be found on different host plants, there maybe different fungal genetic variants specific to different hostplants. Genetic variability within a fungal species may re-duce the possibility of anastomoses between the mycelium

© 2004 NRC Canada

Simard and Durall 1141

Page 3: Mycorrhizal networks: a review of their extent, function, and

© 2004 NRC Canada

1142 Can. J. Bot. Vol. 82, 2004

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Page 4: Mycorrhizal networks: a review of their extent, function, and

© 2004 NRC Canada

Simard and Durall 1143

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chC

MN

can

form

betw

een

diff

eren

tA

Mpl

ants

ofth

esa

me

spec

ies

Med

ium

Gio

vane

tti

etal

.20

01

AM

Gre

enho

use,

pots

Roo

tle

ngth

infe

cted

Spe

cies

Bra

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nell

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naS

uppo

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that

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st

Med

ium

Van

der

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jden

etal

.20

03O

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d(m

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hete

rotr

oph)

,E

CM

Lab

,P

etri

dish

esP

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LP

Sub

spec

ies,

anas

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ose

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ping

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ussy

lves

tris

,G

oody

era

repe

nsna

Des

crib

esa

mec

hani

smby

whi

chC

MN

can

form

be-

twee

nor

chid

san

dE

CM

plan

tsp

ecie

s

Med

ium

Sen

etal

.19

99O

rchi

d(m

yco-

hete

rotr

oph)

,E

CM

Not

e:A

M,

arbu

scul

arm

ycor

rhiz

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,ec

tom

ycor

rhiz

a;SS

R,

sim

ple

sequ

ence

repe

at;

ISSR

,in

ters

impl

ese

quen

cere

peat

;na

,no

tap

plic

able

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igh,

conc

lusi

veev

iden

cefo

rhy

phal

conn

ectio

nsbe

twee

ntw

oor

mor

epl

ants

and

the

CM

Nis

capa

ble

oftr

ansp

ortin

gel

emen

tsfr

omon

ero

otsy

stem

toan

othe

r;m

ediu

m,

high

prob

abili

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nc-

tioni

ngC

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exis

ts,

but

conc

lusi

veev

iden

ceno

tre

port

ed;

low

,lit

tleev

iden

cefo

rth

eex

iste

nce

ofm

ycor

rhiz

alne

twor

ks.

Tab

le1

(con

clud

ed).

Page 5: Mycorrhizal networks: a review of their extent, function, and

of different host plants (Sen et al.1999; Giovannetti et al.2001), reducing the potential for formation of a CMN. Incontrast, finding a single genet on different plant specieswould provide strong evidence for the presence of a CMN,since the fungal hyphae would probably anastomose. Micro-satellite analysis of DNA allows mapping of ECM fungalgenets within a forest. Studies have shown that ECM fungalgenet size ranges from less than 1 m2 to 300 m2 (Bonello etal. 1998; Sawyer et al. 2001). Although microsatellite tech-niques have not been used specifically to demonstrate theexistence of a CMN, ECM fungal genets have been shownto extend over an area encompassing multiple plant hosts ofthe same or different plant species (Zhou et al. 2001; Sawyeret al. 2001; Bergemann and Miller 2002; Dunham et al.2003). Future research is necessary to determine whetherfungal genets occur on different host plants of the same ordifferent species.

Even though microsatellite techniques show promise,genet size may be problematic in estimating the size ofmycorrhizal networks. For example, genet size estimatesmay encompass a series of ramet clumps rather than onecontinuous genet and therefore may not represent a continu-ous mycorrhizal network (Sawyer et al. 2001; Dunham et al.2003). This is especially true when genet size is estimatedfrom sporocarps (Sawyer et al. 2001). In other ECM fungalspecies, however, whose hyphae are thought to extend forlarge distances, there is more chance that genet size wouldbe representative of a CMN (Bonello et al. 1998).

In this section, we reviewed recent evidence for the exis-tence of common mycorrhizal networks. Much more infor-mation is needed to confirm their existence, size,distribution, and function before we can make conclusivestatements about their ecological significance.

Pathways for interplant C transferThe molecular and morphological fungal specificity stud-

ies described above provide evidence that both AM andECM fungal species can associate with multiple plant hostsand that mycorrhizal hyphae emanating from one plant cancolonize the roots of neighboring plants, forming a CMN.Studies using isotopic tracers have suggested that interplanttransfer can occur along several different pathways. Inter-plant transfer can occur directly through an intact CMN(pathway 2a, Fig. 1a) (McKendrick et al. 2000; Wu et al.2001) or a CMN comminuted by soil organisms (pathway2b, Fig. 1a) (Tuffen et al. 2002). Alternatively, transfercan occur along a mycorrhizal–soil pathway (pathway 3,Fig. 1a), where C is exuded or leaked into the soil pool bythe mycorrhizal roots or mycelium of one plant and then ispicked up by the mycorrhizal roots or mycelium of a neigh-bouring plant (Newman et al. 1989), or along anonmycorrhizal–soil pathway (pathway 1, Fig. 1a), wherethere is no movement at any point within fungal hyphae. Inpathways 1, 2b, and 3, C or nutrients exuded into the soilpool are subject to biochemical transformations by soilorganisms, depletion or fixation by physical or chemical pro-cesses, movement as soluble organic compounds, or respira-tion, followed by anapleurotic uptake by neighbour roots.Individual ECM plants can have some root tips that associ-ate with host-specific fungi, others that associate with host-generalist fungi, and some that are nonmycorrhizal (e.g.,

Jones et al. 1997), raising the possibility that multiple path-ways can operate simultaneously within a single plant pair.Empirical evidence for simultaneous multiple pathways co-mes from Simard et al. 1997a, whose data support directtransfer between paper birch and Douglas-fir through theCMN as well as indirect transfer to AM western redcedarthrough the mycorrhizal–soil pathway.

© 2004 NRC Canada

1144 Can. J. Bot. Vol. 82, 2004

Fig. 1. (a) Model pathways for interplant carbon and nutrienttransfer. In pathway 1 (dotted arrow), plants A and B arenonmycorrhizal (NM), and transfer occurs through the soil poolwithout entering mycorrhizal hyphae at any point. In pathway 2a(solid arrows), transfer between plant A and plant B occurs en-tirely within the common mycorrhizal network (CMN) formedby generalist fungus Z. In pathway 2b (broken arrows), transferbetween plant A and plant B is facilitated by soil animals feed-ing on external hyphae produced by mycorrhizal fungi. In path-way 3 (broken–dotted arrow), plant A is colonized with host-specific fungus X and plant B with fungus Y (no CMN), andtransfer occurs partly through fungi X and Y and partly throughthe soil pool. (b) Simple model of interspecific competition be-tween plant A and plant B via the NM–soil pathway (generalinterplant competition for resources). The upper dotted line withend-circle denotes the competitive effect of plant A on plant Band vice versa.

Page 6: Mycorrhizal networks: a review of their extent, function, and

C transfer between plantsAs outlined in the Introduction, our review primarily in-

cludes studies on C transfer published in the past 6 years,but with brief reference to key historical papers. Relevantstudies published between 1997 and 2003 are summarized inTable 2. The earliest evidence for C or nutrient transferthrough a CMN involved movement of 14C from large coni-fer trees in the field to neighbouring myco-heterotrophicplants of the species Monotropa hypopitys Crantz (Bjorkman1960). Since then, using PCR-RFLP techniques, severalmyco-heterotrophic plants have been shown to formendomycorrhizal associations with fungi that simultaneouslyform ECM with surrounding trees (Cullings et al. 1996; Tay-lor and Bruns 1997, 1999; McKendrick et al. 2000; Bidar-tondo and Bruns 2002; Bruns et al. 2002a; Bidartondo et al.2002). In a recent study, McKendrick et al. (2000) providedthe first experimental confirmation that growth of the myco-heterotrophic orchid Corallorhiza trifida Chatelain wassustained by C directly received from a neighbouringautotrophic tree (Betula pendula Roth. or Salix repens L.)through linked fungal mycelia of a shared symbiont. Theylabeled the two tree species with 14C and, using digitalautoradiography and tissue oxidation, found that one-waytransfer to the coralloid rhizome of Corallorhiza trifida wasequivalent to 0.31%–0.38% of label in the donor trees. Theyalso found that Corallorhiza trifida gained 6%–14% of masswhen linked to autotrophs, but lost 13% when not linked,probably resulting from uncompensated maintenance costs.These studies on myco-heterotrophic plants provide conclu-sive evidence that interplant C transport occurs throughhyphal networks.

Interplant transfer of C has also been studied extensivelyin AM and ECM chorophyllous plant systems sinceBjorkman’s original groundbreaking work. In early labora-tory studies, 14C was used to show C transfer from one ECMconifer seedling into the roots and shoots of another via aCMN (Reid and Woods 1969; Finlay and Read 1986a). Sim-ilar work was done in AM systems, but unlike the ECMstudies, transferred label did not move into receiver plant tis-sues (Hirrel and Gerdemann 1979; Francis and Read 1984).In the first field study with ECM plants, Read et al. (1985)showed transfer of 14C to multiple receiver plants, raisingquestions about the existence of bidirectional or net transferand about the ecological significance of the quantities of Ctransferred between plants (Newman 1988; Newman et al.1997).

C transfer between ectomycorrhizal plantsTo address the identified need to investigate bidirectional

and net transfer (Newman 1988), Simard et al. (1997a) andSimard et al. (1997d) used dual (13C–14C) pulse-labeling toexamine CMN-mediated transfer between ECM Pseudo-tsuga menziesii Mirb. (Franco) and Betula papyrifera Marsh.seedlings in the laboratory and field. Bidirectional C transferwas balanced between P. menziesii and B. papyrifera in thelaboratory and first-year field experiment, and in the secondfield year, P. menziesii received a net C gain fromB. papyrifera. Net gain by P. menziesii averaged 6% of Cisotope uptake through photosynthesis, with more in deepshade (10%) than in full or partial sun (3%–4%). Label wasdetected in receiver plant shoots in all transfer experiments,

indicating movement of transferred C out of fungal and intoplant tissues (Simard et al. 1997a, 1997d, 1997e). In thefield, equidistant AM Thuja plicata Donn ex D. Don seed-lings absorbed <1% and 18% of transferred isotope in thefirst and second years, respectively, suggesting that most Cwas transferred through the ECM hyphal pathway, but thatsome was also transferred through soil pathways. Based onthe field and lab results, Simard et al. (1997a) and Simard etal. (1997d) concluded that interplant C transfer was a com-plex and variable process that involved hyphal as well assoil pathways. One of the shortcomings of these experimentswas that the presence and functional status of hyphal con-nections were not unequivocally demonstrated (e.g., usingradiography); instead their presence was inferred from ECMshared-compatibility studies, using morphological and mo-lecular techniques (Jones et al. 1997; Simard et al. 1997b;Sakakibara et al. 2002), from observations of hyphal links inlaboratory rootboxes and from measurement of transfer be-tween EM versus AM seedlings.

The experiments of Simard et al. (1997a) and Simard etal. (1997d) were constructively criticized by Fitter et al.(1998), Robinson and Fitter (1999), and Fitter (2001), justi-fiably highlighting some of the limitations of the studies. Weare in agreement with Robinson and Fitter (1999) and Fitteret al. (1999) regarding several of these shortcomings. Theysuggested, instead of AM controls, use of physical barriersto prevent hyphal contact between ECM plants, full reci-procity of all dual-labeling treatments, quantification ofdonor root isotopic-specific activities, identification of trans-ferred C compounds, examination of both plant and fungalregulatory factors, and investigation of the significance oftransfer in a broader array of natural ecosystems and overlonger periods of time. We are addressing several of theselimitations in our current research programs, investigatingbidirectional transfer in mixed and single species forests(L.J. Philip, M.D Jones, and S.W. Simard, unpublished data;F. Teste, S.W. Simard, and D.M. Durall, unpublished data).

We felt that some of the criticisms of Robinson and Fitter(1999) and Fitter et al. (1999), however, were unfounded.We addressed most of these criticisms in the review bySimard et al. (2002), and we expand on them here. Robinsonand Fitter (1999) reiterated that a large amount of C (18%)was absorbed by AM T. plicata, suggesting the occurrenceof a soil-transfer pathway through release and capture ofexudates and possibly negating the primacy of a hyphal-transfer pathway. The significance of a soil-transfer pathwaywas never disputed by Simard et al. (1997a), and the com-mon occurrence of host-general and host-specific fungi on asingle ECM root system (Molina et al. 1992; Simard et al.1997b; Jones et al. 1997) suggests that multiple transferpathways operating simultaneously in a given plant pair areto be expected (see model pathways above). Even so, theoccurrence of pathway 2a (Fig. 1a) is suggested by the ex-periment of Simard et al. (1997a) as well as others (Francisand Read 1984), which show greater transfer when mycor-rhizal links are present. Secondly, Robinson and Fitter(1999) argued that our studies showed one-way rather thanbidirectional transfer, based on the nearly 10-fold larger iso-tope transfer from B. papyrifera to P. menziesii than viceversa in the second-year field experiment and the possibilitythat received isotope lies within the error calculation limits.

© 2004 NRC Canada

Simard and Durall 1145

Page 7: Mycorrhizal networks: a review of their extent, function, and

© 2004 NRC Canada

1146 Can. J. Bot. Vol. 82, 2004

Myc

orrh

izal

type

;st

udy

cond

itio

nsIs

otop

esu

ppli

ed;

anal

ysis

met

hod

Pla

ntsp

ecie

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irs;

fung

alin

ocul

ant

Met

hod

used

tose

para

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ngal

from

soil

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way

Tra

nsfe

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thw

ayfo

und

Fact

orfo

und

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flue

nce

tran

sfer

Type

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ansf

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und

and

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reof

amou

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ence

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C;

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ula

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ttr

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;(i

ii)

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mor

etr

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erin

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full

ligh

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nsis

-te

ntw

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tran

sfer

was

3%–1

0%of

tota

lis

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rs

Roo

tan

dsh

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Sim

ard

etal

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97a

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root

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and

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ayP.

men

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ii,

B.

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dso

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28- µ

mm

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barr

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EC

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guis

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i)no

net

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Two-

way

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5%of

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rs

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root

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sed

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sted

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enzi

esii

(tra

nsfe

rin

reve

rse

dire

ctio

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One

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sfer

was

4.7%

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r

Roo

tan

dsh

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Sim

ard

etal

.19

97c

EC

M;

root

box

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b

Pul

sed

14C

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tora

diog

raph

yP

inus

dens

iflo

rapa

irs;

Pis

olit

hus

tinc

tori

us,

T01

Non

myc

orrh

izal

cont

rol

1°:

EC

MP

rese

nce

ofhy

phal

link

s(i

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ayan

dtw

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fer;

(ii)

isot

ope

mov

emen

tfr

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ycel

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than

apex

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se

Not

dete

rmin

edF

unga

lW

uet

al.

2001

AM

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xin

lab

Nat

ural

abun

danc

e13

C;

bioa

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Pla

ntag

ola

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ynod

onda

ctyl

on;

nativ

ero

otfr

agm

ents

Dif

fere

nt13

Cdi

scri

min

atio

nbe

twee

nC

3an

dC

4pl

ants

;28

- µm

and

0.45

- µm

mes

hba

rrie

rs

1°:

AM

;2°

:so

ilP

rese

nce

ofhy

phal

link

s(i

)O

ne-w

aytr

ans-

fer

toC

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onda

ctyl

on(t

rans

-fe

rin

reve

rse

dire

ctio

nno

tde

term

ined

);(i

i)on

e-w

aytr

ansf

erto

P.la

nceo

lata

Typi

call

y0%

–10%

(up

to41

%)

ofC

inre

ceiv

erro

ots

deri

ved

from

dono

r

Roo

tan

dfu

ngal

ofC

.da

ctyl

on;

root

and

shoo

tof

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nceo

lata

Wat

kins

etal

.19

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;ro

otbo

xin

lab

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sed-

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eted

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tan

dfu

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97

Tab

le2.

Cha

ract

eris

tics

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tran

sfer

inE

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and

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syst

ems

mea

sure

din

rece

ntfi

eld

and

labo

rato

ryst

udie

s.

Page 8: Mycorrhizal networks: a review of their extent, function, and

© 2004 NRC Canada

Simard and Durall 1147

Myc

orrh

izal

type

;st

udy

cond

itio

nsIs

otop

esu

ppli

ed;

anal

ysis

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Pla

ntsp

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soil

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Type

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and

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nttr

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Nat

ural

-ab

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;bi

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twee

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mes

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1°:

AM

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:so

ilS

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and

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thal

tere

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One

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sfer

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5%–1

5%of

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lant

ago

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ter

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sms

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Pul

sed

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Cor

rall

orhi

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etul

ape

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lix

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;fi

eld

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hba

gsan

dno

nmyc

orrh

izal

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rols

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link

s(E

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ophs

)

Pre

senc

eof

hyph

alli

nks

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-way

tran

sfer

toC

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trif

ida

from

both

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pend

ula

and

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,bu

tno

tP

inus

sylv

estr

is

One

-way

tran

sfer

toC

orra

llor

hiza

trif

ida

was

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%–0

.38%

ofis

otop

ein

dono

rs;

itga

ined

6%–1

4%m

ass

ofw

hen

link

edto

auto

trop

hsan

dlo

st13

%w

hen

not

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ket

al.

2000

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infi

eld

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m,

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amer

ican

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Bet

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is(E

CM

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rece

iver

plan

ts

(i)

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-way

tran

s-fe

r;(i

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ansf

erre

vers

edbe

twee

nsp

ring

and

fall

,co

rres

pond

ing

wit

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sour

ce–

sink

patt

erns

info

liat

ion

One

-way

tran

sfer

toA

.sa

ccha

rum

was

1.6%

ofle

afC

dem

and

Roo

tan

dsh

oot

Ler

atet

al.

2002

AM

;sp

lit

Pet

ridi

shin

lab

13C

and

15N

NM

R;

gas

chro

mat

ogra

ph,

mas

ssp

ectr

os-

copy

anal

ysis

ofpr

otei

nex

trac

t

Dau

cus

caro

ta;

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mus

intr

arad

ices

Roo

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mpa

rtm

ent

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-m

aine

din

rece

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whi

le15

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und

inre

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naF

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ffer

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rson

alco

mm

unic

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n

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However, Simard et al. (1997a) showed that isotope re-ceived by both tree species was well above detection andcalculation error limits in all experiments, and Simard et al.(1997a, 1997d, 1997e) showed that large amounts of isotopewere transferred in both directions in both the first-year fieldand laboratory studies, exceeding one-way transfer consid-ered significant in other systems (e.g., Read et al. 1985;Finlay and Read 1986b). Thirdly, Robinson and Fitter(1999) suggested that [13CO2] far exceeded [14CO2] in ourfield labeling chambers, possibly altering C assimilation, al-location, and interplant flux patterns. However, out-plantedB. papyrifera and P. menziesii were pulsed with similar12 + 13CO2 (0.05%) and 12 + 14CO2 (0.03%) concentrations(Simard et al. 1997a), resulting in the same 13C and 14C tis-sue allocation patterns (Simard et al. 1997a). This findingwas supported by another study by Simard et al. (1997e),who found no effect of increasing 12 + 13CO2 concentrationsfrom 0.04% to 0.05% on 13C allocation patterns. Fourthly,Robinson and Fitter (1999) and Fitter (2001) argued thatSimard et al. (1997a) inferred a mutualistic plant–fungus–plant relationship from their results and that they had specu-lated that competition interactions be replaced by mutualismas the dominant interaction shaping plant communities.While these speculations may have been made in otherpapers, Simard et al. (1997a) carefully stated that the netcompetitive effect of one species on another should not bepredicted without an understanding of interplant transferthrough hyphal and soil pathways (i.e., model pathways 1, 2,and 3) and in so doing recognized the primacy of competi-tive interactions in shaping plant community dynamics. Ourstudies were insufficient, however, to determine the impor-tance of C transfer relative to other competitive interactionsin plant community dynamics. Nevertheless, the magnitudeof net transfer we measured was in the range considered suf-ficient to increase survival and growth of interconnectedramets in clonal plants (Alpert et al. 1991). This suggests tous that C transfer has the potential to influence plant interac-tions some time during community development, but longerterm, broader scope field research is needed before we canquantify this effect.

Following the ECM studies of Simard and associates, Wuet al. (2001) carefully examined the pathway, movement,and fate of 14C transferred between ECM-connected Pinusdensiflora Sieb. & Zucc. seedling pairs using time-courseautoradiography in laboratory microcosms. They demon-strated unequivocally that 14C was transferred from ECMdonor plants to the mycelia and ECM of receiver seedlingswithin 3 d. They also found that 14C moved bidirectionallywithin the mycelia, with the greatest transfer through densemycelial fans of one fungal species and hyphal strands ofanother. Hyphal strands of ECM had earlier been hypothe-sized as the most important conduits of transferred C(Cairney and Smith 1992), but this study confirms thathyphae not associated with rhizomorphs can also be an im-portant pathway.

In contrast to many of the earlier C-transfer studies in-volving ectomycorrhizae (Bjorkman 1960; Brownlee et al.1983; Francis and Read 1984; Read et al. 1985; Finlay andRead 1986b; Arnebrant et al. 1993; Simard et al. 1997a;Simard et al. 1997d; Simard et al. 1997e), Wu et al. (2001)found no transfer into root or shoot tissues of receiver

plants. Reasons for the inconsistency in root-to-shoot Ctransfer are not understood, but Wu et al. (2001) differedfrom the earlier studies in that shoots of receiver plants werewrapped in aluminum foil during the chase period to preventrefixation of respired 14CO2, whereas most of the other stud-ies used equidistant control plants to quantify and subtractrefixed 14CO2, leaving receiver plants in an unaltered physi-ological condition. By preventing fixation and respiration ofreceiver shoots, Wu et al. (2001) may have weakened thesink strength of plant tissues for organic compounds. Addi-tionally, the use of radiography to detect C transfer mayhave underestimated C transfer into pine shoots because it isless sensitive than the tissue oxidation method commonlyused by others (e.g., Simard et al. 1997a; Lerat et al. 2002).

Some have argued that C movement to shoots in earlierECM studies may have actually followed transfer betweennonmycorrhizal rather than between mycorrhizal roots (Wuet al. 2001; Fitter et al. 2001). These authors also recog-nized, however, that previous research demonstrated move-ment of isotopically labeled organic N compounds from themycorrhizal fungus to plant tissue in ectomycorrhizal plants(Arnebrant et al. 1993; Cliquet and Stewart 1993; Finlay etal. 1989; Chalot and Brun 1998; Näsholm et al. 1998) andmyco-heterotrophic plants (McKendrick et al. 2000). Amechanism for C transfer into receiver tissue has been pro-posed, where sugar or organic N is transported from the do-nor plant to the fungus, low molecular weight organic Nmoves from the donor to receiver plant through the intercon-necting fungus along a hydrostatic pressure gradient fromhigh to low assimilate and N concentrations, and the organiccompound is then actively transported across the plant–fungal membrane into plant tissues (Smith and Smith 1990;Martin et al. 1997; Chalot and Brun 1998). Whether trans-ferred C moves into receiver plant tissues or remains in fun-gal tissues is still under debate, and this has been proposedas the key piece of evidence that would underscore the func-tional significance of interplant transfer in ecological inter-actions (Fitter et al. 1999; Robinson and Fitter 1999). Weand others argue, however, that C transferred to the ectomy-corrhizal fungi of the receiver plant, even without transferinto plant tissues, is still a subsidy to the nutrient-gatheringsystem of the plant (Perry 1998; Simard et al. 2002) that po-tentially can affect plant community dynamics (Bever 2003).

C transfer between arbuscular mycorrhizal plantsRecent studies in AM systems are providing increasing

evidence that the pattern of interplant C transfer contrastswith that in ECM systems. These differences in part have fu-elled the aforementioned debates. Several laboratory studieshave demonstrated C movement from one AM plant to an-other (Francis and Read 1984; Martins 1993; Watkins et al.1996), but none have demonstrated net transfer (Perry 1999),and most have found little (Francis and Read 1984; Read etal. 1985) or no movement of transferred C from roots toshoots (Waters and Borowicz 1994; Watkins et al. 1996;Graves et al. 1997; Fitter et al. 1998), because it appearedto remain associated with fungal tissue (Fitter et al. 1999;P.E. Pfeffer, personal communication). Watkins et al. (1996)used differences in natural abundance of 13C to quantify Ctransfer between laboratory-grown C3 (Plantago lanceo-lata L.) and C4 (Cynodon dactylon (L.) Pers.) plants, as well

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as different-sized mesh barriers, to distinguish AM fromsoil-transfer pathways and showed that one-way transfer toCynodon dactylon was generally <10% of donor isotopecontent, ranging between 0% and 41%. They also found thattransfer between potentially linked plants far exceeded thatof unlinked plants and most transferred C remained in themycorrhizal tissues of Cynodon dactylon, but that mosttransferred C moved into both roots and shoots of Plantagolanceolata. Fitter et al. (1998) further tested the fate oftransferred C in Cynodon dactylon and Plantago lanceolataby examining the regrowth of clipped receiver plants, con-firming that all transferred C remained in mycorrhizal struc-tures. They also showed that the extent of transfer waspositively correlated with fungal vesicle abundance, nothyphal abundance (Fitter 2001), underscoring differenceswith ECM transfer patterns shown by Wu et al. (2001).These results were corroborated by Graves et al. (1997),who fumigated sections of mycorrhizal and nonmycorrhizalC4 Festuca ovina S. Wats. turf with 13C-depleted air andshowed that 41% of C was transferred from donor roots tolinked neighbours, most transferred C remained in donormycorrhizal structures, and no C was transferred to unlinkedneighbours. The lack of transferred C movement from AMfungal tissues into associated plant tissues is supported bythe recent work of P.E. Pfeffer (personal communication),who showed that 15N substrates supplied in vitro toextraradical mycelium (ERM) of AM carrot-root cultures re-sulted in substantial labeling of root proteins, but that 13Csubstrates supplied to the ERM entered only fungal com-pounds (trehalose and storage lipids) and not host root me-tabolites. Similar to Wu et al. (2001), however, sink strengthof receiver plants may have been substantially altered by ex-cising the carrot shoots and placing the roots in a Petri dish.

A recent field study that investigated interplant C transferin an AM Acer saccharum Marsh. forest in Quebec providesdivergent results to the AM laboratory, greenhouse, and invitro studies described previously. Lerat et al. (2002) grewA. saccharum, Erythronium americanum Ker-Gawl., and, asa control, ECM Betula alleghaniesis Britt. individuals to-gether in fibre pots in the forest understory. In spring, theylabeled fully expanded E. americanum leaves with 14C whileA. saccharum overstory and sapling leaves were still leaf-less, but were bursting bud, and followed this with a falllabeling of fully expanded A. saccharum foliage, afterE. americanum leaves had been shed. In the spring, 0.064%of the fixed label in donor E. americanum was transferredinto A. saccharum, with 13 times less transferred into Betulacontrol plants. Although the amount transferred was small, itwas equivalent to 1.6% of leaf expansion costs for the maplesaplings, which the authors suggest is a conservative esti-mate, considering that maple saplings would be connectedto several E. americanum plants in the undisturbed forest.Autoradiographs clearly showed that 14C had moved intoroots, stems, and leaves of receiver maple seedlings. In thefall labeling, there was evidence that the direction of transferhad reversed, with 14C moving from A. saccharum saplingsto 7 of 22 E. americanum mycorrhizal root systems andnone moving to Betula controls. The lack of radioactivity inbirch indicated that transfer through soil pool pathways wasinsignificant. The pattern of C transfer was consistent withsource–sink relationships between donor and receiver plants

during spring and fall seasons. Fully developed E. ameri-canum were strong sources and newly developing mapleleaves were strong sinks for carbohydrates in spring,whereas defoliated E. americanum roots became sinks fornew maple-leaf assimilate in the fall. This study provides thefirst evidence that the direction and amount of C transfer canchange with season, emphasizing that one-time measure-ments are inadequate for evaluating the significance oftransfer to plant fitness where receivers and donors havenonsynchronous phenologies.

Reasons why transfer patterns in AM systems differ fromthose in EM systems have yet to be fully explored. Severalmorphological, physiological, and genetic factors may be in-volved, including AM and EM differences at the fungus, in-terface, root, plant-species, and ecosystem levels. Some ofthese differences may be controlled by examining transferamong plant species forming both ECM and AM associa-tions within the same ecosystem. A striking difference isalso emerging in some field versus laboratory or greenhousestudies for both ECM (e.g., Simard et al. (1997a) vs. Wu etal.(2001)) and AM systems (e.g., Lerat et al. (2002) vs. Fit-ter et al. (1998)). There are numerous conditions that differbetween the field and laboratory or greenhouse, including al-terations in source–sink patterns in plant combinations andsimplification of the CMN. These factors should be exam-ined to improve our understanding of the mechanisms andsignificance of C transfer in nature.

Factors regulating C transferStudies that have investigated factors influencing the

transfer of C among interconnected plants have focused onthree areas: source–sink relationships between donor and re-ceiver plants, sink patterns of fungi making up the CMN,and perturbations to the CMN. The original pioneering labo-ratory studies by Read and coworkers showed that theamount of C transferred among interconnected AM or ECMplants increased with shading of the receiver, suggesting thatC moved between plants along a source–sink gradient of acurrent C assimilate (Francis and Read 1984; Read et al.1985; Finlay and Read 1986a). These studies were sup-ported by the field study of Simard et al. (1997a), whoshowed that net transfer from ECM B. papyrifera to P. men-ziesii increased twofold when P. menziesii was deeplyshaded. New corroborating evidence for plant-drivensource–sink regulation of transfer comes from Lerat et al.(2002), who showed that seasonal changes in source–sinkgradients driven by shifting plant phenologies affected thedirection of C transfer between AM plants. In another study,Waters and Borowicz (1994) altered sink strength of AM-linked plants by clipping one of the partners and found thatC flowed away from clipped plants toward unclipped plants,the opposite of that expected. They reasoned, however, thatclipping the plants increased labile C concentration in theroots (i.e., turned them into source plants), thereby increas-ing the diffusion gradient for C out of roots into mycorrhizalfungi and into connected, neighbouring, unclipped plants. Incontrast to sink-strength manipulations, Fitter et al. (1998)found that increasing source strength by growing plants inenriched CO2 environments had no effect on the occurrenceor extent of C transfer. Other experiments examined transferbetween plants that naturally differed in C physiology or

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mycorrhizal dependency (Grime et al. 1987; van der Heijden2002).

The form of C transferred between interconnected plantsis important for understanding the mechanism of interplanttransfer and how C compounds are used by receiver plants.Trehalose, mannitol, and arabitol are major carbohydratesassociated with mycelium interconnecting ECM plants(Söderström et al. 1988), and trehalose is important in myce-lium of AM plants (Lammers et al. 2001; P.E. Pfeffer, per-sonal communication). The occurrence and concentration ofthese compounds can differ between extramatrical mycelium(EMM) and fungal tissue of ECM. For example, mannitolis found in free-living mycelium of Pisolithus tinctorius(Mich.: Pers.) Coker & Couch, whereas trehalose tends toaccumulate in Pisolithus tinctorius ECM (Martin et al.1998). Furthermore, trehalose predominates in ECMbasidiomycetes, whereas mannitol is commonly found as asoluble form of C in ECM ascomycete tissue (Martin 1985;Martin et al. 1988; Ceccaroli et al. 2003). Source–sink gradi-ents of these compounds likely play a role in movement ofcarbohydrates within the CMN, but it is unknown whetherthese gradients are important in moving C via the commonmycorrhizal network from one plant to another. Free aminoacids also represent an important sink of assimilated C inectomycorrhizal fungi (Martin et al. 1988; Ceccaroli et al.2003). N source–sink gradients may be as much or more im-portant than C assimilate gradients in moving C from oneplant to another, because there is greater evidence that or-ganic N compounds transfer more readily from fungal toplant tissues than do carbohydrates. Amino acids or low-weight nitrogenous compounds have been shown to passfrom mycorrhizal fungi into host-plant tissues (Finlay 1989;Cliquet and Stewart 1993; Arnebrant et al. 1993; Näsholm etal. 1998). Although slow movement of carbohydrates fromthe fungal mycobiont to the plant symbiont has been demon-strated in excised roots (Lewis and Harley 1965), other stud-ies have failed to demonstrate this (Smith and Smith 1990).In addition to carbohydrates and amino acids, lipids, such astriacylglycerides, may play an important role in the move-ment of C in the ERM of AM plants (Pfeffer et al. 1999).There is a great need to identify compounds that are trans-ferred through the CMN and into mycorrhizal and host-planttissues and to trace their movement using biochemical andmolecular markers. This would help identify the mechanismfor simultaneous C and nutrient exchange between intercon-nected plants and fungi.

There is increasing evidence that mycorrhizal fungi alsoplay a role in controlling the direction, magnitude, and rateof C or nutrient transfer between linked plants, particularlyin AM systems. Although the ability of the fungi to seques-ter and provide nutrients and C to linked plants at differentrates and amounts has largely been unexplored (Miller andAllen 1992), different characteristics of the CMN have re-cently been shown to influence interplant transfer. For exam-ple, Martensson et al. (1998) found great variation in Ntransfer from bean to chicory among different linking iso-lates of Glomus spp., which they suggested reflected differ-ences in the isolates’ capacity to initiate a plant trigger for Ntransfer. In other studies, hyphal links have been shown toenhance herbicide injury to weeds, possibly because AMfungi adjusted their own source–sink relations in favour of

sink-driven fluxes (Bethlenfalvay et al. 1996b; Rejon et al.1997). Several studies provide evidence that magnitudeof transfer is affected by the degree of physical root–rhizosphere overlap or frequency of mycorrhizal links(Johansen and Jensen 1996; Walter et al. 1996; Simard et al.1997a). By contrast, Watkins et al. (1996) and Fitter et al.(1998) found little relationship between C transfer and thedegree or direction of AM colonization and little evidencethat colonization was related to number or functioning oflinks. Additional fungal factors that appear to play a rolein transfer include identity of the fungal species, seasonalor phenological variation in mycorrhizal activity (Frey andSchüepp 1992; Hamel et al. 1992), as well as differentialmycorrhizal dependency of plant species in mixtures (Zhu etal. 2000; van der Heijden 2002).

Factors that may disrupt the CMN and transferSoil animals, such as collembola and earthworms, feed on

the hyphae and spores of mycorrhizal fungi (Finlay 1985;Klironomos and Moutoglis 1999; Tuffen et al. 2002).Collembola can reduce the number of AM spores found insoil and in some cases reduce external hyphal length of AMfungi (Larsen et al. 1996). In cases where collembola havehad no effect or resulted in an increase in AM hyphal length(Klironomos and Kendrick 1995), interconnections betweenAM fungi and plants may still have occurred. For example,collembola have been found to sever hyphal branches with-out shortening hyphal length (Klironomos and Ursic 1998).These studies suggest that soil animals may have a profoundeffect on the presence, size, and function of the CMN.Tuffen et al. (2002), using AM-linked leek plants in a labo-ratory microcosm experiment, showed that increased earth-worm grazing of the AM mycelium led to enhancedavailability of 32P to a receiver plant. Thus, transfer of 32Pfrom one plant to another was greater when earthworms hadcomminuted the CMN (pathway 2b in Fig. 1a) than when anintact CMN was connecting the two plants (pathway 2a inFig. 1a). This lab study demonstrates that soil animals areable to influence the functioning of a CMN, but we awaitfield results to see if similar effects occur in nature.

Few studies have investigated the influence of soil animalson EMM of ECM fungi. Bonkowski et al. (2001) usedPaxillus involutus (Batsch: Fr.) Fr. in a laboratory micro-cosm study to show that ECM hyphal length was reducedwhen protozoa were present compared with when they wereabsent. This study confirms the findings from AM studiesthat soil animals can disrupt the mycelial networks; however,much more evidence under natural conditions is needed. Inaddition to soil animals, other factors that may limit the sizeand function of CMNs include drought, natural disturbances(e.g., fire, flooding), and anthropogenic disturbances (e.g.,ploughing, site preparation, harvesting). These perturbationsform gaps in the plant community and can directly or indi-rectly disrupt the CMN (Jones et al. 2003).

CMN influences on feedbacks among plants and fungiWe have presented evidence that C transferring from one

plant to another may enter the host root or shoot tissue(Watkins et al. 1996; Simard et al. 1997a; Lerat et al. 2002)or, alternatively, remain within the fungal tissues of theirmycorrhizal associations (Graves et al. 1997; Fitter et al.

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1998; Wu et al. 2001; P.E. Pfeffer, personal communica-tion). Even where transferred C remains in mycorrhizal fun-gal tissues and is not transferred into receiver plant tissues,we suggest there may be a net benefit to the plant, becausethe CMN is subsidized, reducing C demand by the plant’sfungal symbionts (Wilkinson 1998; Amaranthus et al. 1999;Fitter 2001; Zabinski et al. 2002; Simard et al. 2002). Withor without C transfer to plant tissues, a CMN is likely tohave important influences on feedback among and betweenplants and mycorrhizal fungi (Bever 2003). Based on theconcept that growth rates and fitness of plants and soil mi-crobes are interdependent, Bever et al. (1997) used a model-ing approach to predict the structure and diversity of plantand microbial communities, later extending the models tofocus specifically on relationships between mycorrhizalfungi and host plants (Bever 2003). These models stronglysuggest that the CMN has the potential to influence structureand diversity of the whole plant–microbe community,whether or not C transfer occurs, or whether transferred Cmoves into receiver plant tissues.

We can use the models developed by Bever (2003) toillustrate potential feedbacks among plants and mycorrhizalfungi resulting from the transfer pathways shown in Fig. 1a.Understanding these feedbacks may help us predict the ef-fects of CMNs and C transfer on plant community dynam-ics, a field of research that we discuss later in this paper. Inour nonmycorrhizal soil pathway (pathway 1), the simplestmodel is where plants compete for resources in the soil pool(Tilman and Pacala 1993). In that case, interspecific differ-ences in nutrient or water demand and uptake, as well as in-trinsic growth rates, would determine which plant specieswere favored in the plant community (Fig. 1b). Even in thesimplest plant systems, however, the additional importanceof facilitative between-plant interactions (e.g., frost protec-tion, sunscald protection, reduced herbivory) in structuringplant communities is being increasingly recognized (Perryet al. 1989; Burton et al. 1992; Callaway 1995; Howe etal. 2002). Facilitative relationships between plants and mi-crobes, such as the mycorrhizal association, are also increas-ingly being recognized as important determinants of plantcommunity dynamics (van der Heijden et al. 1998; Bever etal. 2002; DeLong et al. 2002).

The mycorrhizal–soil-transfer pathway (pathway 3) shownin Fig. 1a, which involves specific mycorrhizal relationshipswith host plants, can have complex effects on plant dynam-ics (see mutualistic models in Bever (2003)). In symmetricrelationships between two plants and their mycorrhizalfungi, in which the host-specific fungus delivers the greatestbenefit to the host plant, there is a positive feedback dy-namic (Fig. 2a). One plant–fungal combination is reinforcedmore than the other in the community, leading to eventuallocal extinction of other types. Dominance of grasslands byexotic invading plants, such as Centaurea L. species that arefavored by native AM fungi, is one example of a positivefeedback (Marler et al. 1999; Klironomos 2002). Asymmet-ric relationships can also occur, however, where an AMfungi that has the greatest benefit to a particular plant mayalso result in a greater growth rate of a second plant species(i.e., cosmopolitan specificity). This results in a sustaineddynamic between the plants and AMF community, where nosingle plant species is able to replace the other, leading to in-

creased plant community diversity. Examples of negativefeedback (Fig. 2b) are numerous (e.g., increasing density-dependent mortality in conspecific patches in tropical forests(Harms et al. 2000)) and are considered more common thanpositive-feedback relationships in nature (Bever 2003). Be-cause mycorrhizal associations range from predominantlylow specificity (e.g., AM) to, less commonly, high specific-ity (e.g., orchid mycorrhizae), with most fungi able to colo-nize and thrive on a number of host-plant species (Molina etal. 1992), there exists a mechanism for negative feedbackwithin mycorrhizal plant communities.

The potential coexistence of the direct CMN transfer path-way (pathway 2a, Fig. 1a) with pathways 1, 2b, and 3 canlead to increasing complexity of potential feedbacks amongplants and fungi and less predictable effects on plant com-munity dynamics. This complexity will increase as the num-ber of fungi and plants involved in the CMN increase and asthe interaction strengths between the plants and shared fungichange as a result of successive feedbacks. Taking a reduc-tionist approach to pathway 2a, however, we can see thatseveral positive- and negative-feedback models are possiblein a simple system containing two plants and one sharedfungus (Fig. 3). In the simplest case (Fig. 3a), there is a con-stant host C / fungal nutrient-exchange ratio between the twoplants, where both plants supply the fungus with the sameamount of C in return for equal benefits from the fungus(e.g., equal amounts of organic nutrients). Feedback betweeneach host and fungus is positive, but both plants coexist be-cause there is no net benefit or net loss (e.g., no net transferbetween plants) to either (i.e., the shared fungus does not al-ter the interaction between the two species). One example ofthis is provided by Simard et al. (1997d), where same-sizedEM paper birch and Douglas-fir grown in laboratory root-boxes exchanged C below ground in equivalent amounts, re-sulting in no net C gain by either species. If we alter themagnitude of host C and fungal nutrient exchange betweenhost plants A and B, but don’t alter the exchange ratio be-tween linked plants, no net effect on the plant communityis also expected (Fig. 3b). This could occur in a self-

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Fig. 2. Two potential consequences of the mutual interdepen-dence of plant and mycorrhiza fungal growth rates. The directionof benefit between the two plant species, A and B, and the twofungal species, X and Y, is depicted with the direction of the ar-rows. Thickness of the arrows represents the degree of the bene-fit received, with a thick line meaning greater benefit than a thinone. (a) The symmetric fitness relation between the plants andfungi results in a positive feedback dynamic. (b) The highlyasymmetric fitness relations between the plants and fungi wouldresult in a negative-feedback dynamic. See text for more detailedexplanation. (From Bever et al. 1997., reproduced with permis-sion of J. Ecol., Vol. 85, p. 568, © 1997 Blackwell ScientificPublications Ltd.)

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regenerating stand of conspecific trees, where trees are ofdifferent sizes but their C physiologies and nutrient demandsare proportionally the same (Jonsson et al. 2001). A net ben-efit to a small tree is still possible, even though there is no Ccost to the adult or C gain by the small tree (i.e., no nettransfer), because it has established within a CMN accessinga large soil-nutrient pool (sensu Zabinski et al. 2002).

However, host C / fungal nutrient-exchange ratios, andhence interactions between host plants and a shared fungus,are not always homogenous. Therefore, feedback from theCMN can be expected to affect growth rates of species Aand B differently. Plant A may have a higher ratio of plantC / fungal organic nutrient exchange than plant B, for exam-ple, resulting in net C transfer from plant A to B (or net“benefit” to B if we consider the more general case of inor-ganic nutrients) (Fig. 3c). When Douglas-fir and paper birch

were grown together for 2 years in the field, for example,there was net C transfer from the more photosyntheticallyactive paper birch to shaded Douglas-fir (Simard et al.1997a). Transfer occurred along a source–sink gradient forC that was driven by plant-species differences in C assimila-tion rates and organic nutrient demands. These source–sinkor interplant C – fungal nutrient relationships can changedramatically over time depending on the phenology of thelinked plants (Fig. 3d). Lerat et al. (2002), for example,found that foliated trout lily was a C source for maple seed-lings in an emerging maple canopy in spring, but that defoli-ated trout-lily corms were a C sink in the fall, when themaple canopy was fully expanded (Lerat et al. 2002). Themost extreme case of direct C transfer occurs from auto-trophic trees to myco-heterotrophic plants through specificshared mycorrhizal symbionts (McKendrick et al. 2000)

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Fig. 3. Feedbacks and direct transfer between plants A and B through the ECM hyphal pathway, where fungus Z represents a CMN.Arrows pointing to the plant represent flow of organic nutrients, whereas arrows pointing to the fungus represent carbon (C) flow. Dif-ferences in size of arrows are explained in the caption for Fig. 3. (a) Plant A and plant B have similar plant C / fungal nutrient-exchange ratios. (b) C / fungal nutrient-exchange ratios of plants A and B are the same, but the magnitude is different, resulting inbenefit to both but no net transfer. In (c) and (d), plant C / fungal nutrient-exchange ratios differ between A and B, resulting in net Ctransfer. (e) The C / fungal nutrient-exchange ratios differ between plants A and B, but C transfer to the myco-heterotrophic plant(plant B) is negligible to plant A.

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(Fig. 3e). Although one-way C transfer from mature trees tothe relatively tiny orchid is an example of positive feedback,theoretically leading to community domination by the re-ceiver plant (i.e., orchids), this does not appear to happen,because of the negligible net cost to the tree (Leake 1994).

Adding more plant and fungal species to the CMN createsa greater array of possible feedbacks and potential effects onplant and fungal community structure and diversity (Bruns etal. 2002b). At the same time, the network can still existwithout all plants being tapped into a common mycorrhizalfungal species and without any direct transfer of C betweenplants. In one relatively simple scenario (Fig. 4), three plants(A, B, C) may be directly and indirectly interconnected bytwo fungi (W, Z). In this example, fungus Z connects plantsA and B; fungus W connects plants B and C. Thus, eventhough plants A and C are not associated with the samemycelium, they still can be considered part of the largermycorrhizal network. At a functional level, the interactionbetween plant C and fungus W may be indirectly affectingplant A through the mutual association with plant B. For ex-ample, plant C could be allocating large amounts of C belowground to fungus W, reducing plant B’s need to allocate C tofungus W and indirectly allowing plant B to contribute tothe C demand imposed by fungus Z, thereby reducing the re-quirement of plant A to provide C to fungus Z (Fig. 4). Thisscenario would occur without any interplant transfer. Al-though there is no evidence supporting the occurrence of thisscenario in nature, it demonstrates the complexity of interac-tions that could exist between different plant species andtheir CMN. It is important to remember that this is a rela-tively simple scenario. In nature, feedbacks among plantsand fungi are much more complex and community effectsmuch less predictable because there exists an enormous po-tential for many plants to be interlinked by many differentshared fungi, all with contrasting and shifting C / nutrient-exchange ratios. These are further affected by additionalfeedbacks generated in pathways 1 and 2.

CMN influences on plant community dynamicsMany studies have discussed the implications of plants

tapping into an existing CMN, and increasing their access toa larger pool of host-derived C or soil nutrients, on plantpopulation or community dynamics. However, almost allstudies suffer from inadequate measurement of C transfer orinclude inadequate controls that separate CMN from soilpathways, leaving unanswered questions about the relativeimportance of CMNs, or of C transfer through alternativepathways, on plant community development. As a result, wefeel the field has great potential for further study. Futurestudies should include (i) demonstration that hyphal linksactually exist in the field, (ii) establishment of adequate con-trols, so that CMN effects can be separated from non-CMNeffects, (iii) measurement of bidirectional or net transfer ofC, nutrients, or water among mycorrhizal plants that arelinked by the CMN, (iv) quantification of changes in themagnitude and duration of CMN effects or transfer overextended periods of time and over critical periods of plantdevelopment, and (v) measurements of CMN and (or) trans-fer effects on plant survival, growth, and fitness. Until theseresearch needs are met, the importance of CMNs and C

transfer to plant population and community dynamics willremain unknown.

The potential influences of the CMN on plant communitydynamics have been discussed in several earlier review pa-pers (Newman 1988; Miller and Allen 1992; Perry et al.1992; Amaranthus and Perry 1994; Zobel and Moora 1997;Fitter 2001; Simard et al. 2002). In the most recent review,Simard et al. (2002) summarized six possible effects onplant communities and ecosystems that had previously beenproposed in the literature, citing several papers that sup-ported or contradicted the hypotheses. These were that theCMN may (i) assist with seedling establishment near matureplants by allowing seedlings to become colonized more rap-idly or tap into an established CMN supported by otherplants; (ii) assist with recovery of species following distur-bance, which is particularly important where disturbancebehavior is unpredictable; (iii) reduce competition intensityand promote species diversity by allowing C or nutrients todirectly flow from sufficient to deficient plants, resulting ina more even distribution of C or nutrients; (iv) affect fungalnutrient demands, source–sink relationships, foraging anduptake, and therefore fungal ecology; (v) reduce nutrientlosses from ecosystems by keeping more nutrients in livingbiomass; and (vi) increase productivity, stability, and sustain-ability of ecosystems. Most recent research has examinedCMN effects on seedling establishment, competition amongplants, and plant community diversity, and we therefore fo-cus our review of plant community dynamics on those threeareas. In addition, most studies have examined CMN effectson plant communities rather than populations, providing acommunity focus to our review; however, many of the CMNimplications are similar for populations. Recent relevantstudies are summarized in Table 3.

CMN assistance in seedling establishmentIn forests, subalpine parklands, or shrublands, it has been

recognized that seedlings can preferentially establish nearexisting plants of the same or different species, forming is-lands or clumps of regeneration (Perry et al. 1992). Among anumber of hypotheses suggested to explain this phenomenonis one where mycorrhizae of an existing plant communityinfects new seedlings, facilitating their establishment. Theseedlings may benefit in a number of ways: they may be in-

© 2004 NRC Canada

Simard and Durall 1153

Fig. 4. Feedbacks between plants A, B, and C through the ECMhyphal pathway, where fungi Z and W represent a CMN. Thereis no direct interplant C transfer between A and C, but benefit ofplant C to plants A and B still occurs because of benefits to theCMN. Thickness of the arrows represents the degree of the bene-fit received, with a thick line meaning greater benefit than a thinone. See text for detailed explanation.

Page 15: Mycorrhizal networks: a review of their extent, function, and

© 2004 NRC Canada

1154 Can. J. Bot. Vol. 82, 2004

Myc

orrh

izal

type

and

stud

yco

ndit

ions

Pla

ntsp

ecie

san

dpl

anti

ngde

sign

Met

hod

used

tote

stef

fect

ofC

MN

Fun

gal

inoc

ulan

ts

Isot

ope

used

tote

stfo

rtr

ansf

er

Eff

ect

ofC

MN

trea

tmen

ton

fung

alco

mm

unit

y

Eff

ect

ofC

MN

onin

divi

dual

plan

tpe

rfor

man

ceP

lant

com

mun

ity

effe

cts

stud

ied

orsu

gges

ted

Ref

eren

ce

EC

M,

pots

inla

bP

seud

otsu

gam

enzi

esii

and

Pin

uspo

nder

osa

grow

nin

re-

plac

emen

tse

ries

Mix

ture

spl

ante

din

trea

tmen

ts(i

)w

ith

noE

CM

adde

d,(i

i)w

ith

two

EC

Msp

ecie

sad

ded,

and

(ii)

wit

hfo

urE

CM

adde

d

Tre

atm

ents

(i)

The

leph

ora

cont

amin

atio

n,(i

i)R

hizo

pogo

nvi

nico

lor

and

R.

ochr

aceo

rube

nsad

ded,

(iii

)th

etw

oR

hizo

pogo

nspl

usL

acca

ria

lacc

ata

and

Heb

elom

acr

ustu

lini

form

ead

ded

32P

used

toas

sess

pat-

tern

sof

Pup

take

byth

etw

otr

eesp

ecie

s

At

end

ofex

peri

men

t:(i

)in

noE

CM

,>

80%

The

leph

ora

infe

ctio

n;(i

i)in

two

EC

M,

orig

inal

two

fung

ipl

usm

uch

The

leph

ora;

(iii

)in

four

EC

M,

orig

inal

four

fung

i,w

ith

litt

leT

hele

phor

aan

dco

nsid

erab

lecr

oss-

over

ofL

acca

ria

and

Heb

elom

abe

-tw

een

tree

spec

ies

Wit

htw

oor

four

EC

Mad

ded,

P.m

enze

isii

wer

ela

rger

wit

hm

ore

foli

arP

and

N,

and

mor

e32

Pup

take

,in

mix

ture

than

inm

onoc

ultu

re,

but

wit

hout

asso

ciat

edbi

omas

san

dnu

tri-

ent

decr

ease

sin

Pin

uspo

nder

osa;

due

sole

lyto

shar

edL

.la

ccat

a

(i)

Wit

hno

EC

M,

tree

spec

ies

mut

uall

yin

-hi

bite

don

ean

othe

r,(R

YT

<1)

,(i

i)w

ith

two

orfo

urE

CM

adde

d,in

ters

peci

fic

anta

goni

smdi

sap-

pear

ed(R

YT

≥1)

;pl

ant

com

peti

tion

re-

duce

dbe

caus

e(i

)C

MN

may

incr

ease

acce

ssto

mor

enu

tri-

ent

subs

trat

es,

(ii)

CM

Nm

aydi

stri

bute

nutr

ient

sm

ore

even

ly,

or(i

ii)

mor

efu

ngi

ac-

tive

over

wid

erra

nge

ofco

ndit

ions

Per

ryet

al.

1989

EC

M,

fiel

dP.

men

zies

iise

ed-

ling

spl

ante

din

unde

rsto

ryof

Bet

ula

papy

rife

raan

dP.

men

zies

iiad

ults

See

dlin

gspl

ante

dei

ther

inco

ntac

tw

ith

over

stor

ytr

ees

orin

isol

a-ti

onus

ing

1-m

deep

tren

ches

Fie

ldso

ilN

one

See

dlin

gsco

ntac

ting

over

stor

ytr

ees

had

high

erE

CM

rich

-ne

ssan

ddi

vers

ity,

20×

mor

eR

hizo

pogo

n,an

d6×

mor

eT

hele

phor

a

See

dlin

gsin

cont

act

wit

hov

erst

ory

tree

sha

dhi

gher

high

erph

otos

ynth

etic

rate

san

dhe

ight

-to-

diam

eter

rati

o

Aut

hors

sugg

est

that

link

ing

inC

MN

wit

had

ult

tree

sm

ayas

sist

seed

ling

esta

blis

hmen

t

Sim

ard

etal

.19

97d

EC

M,

fiel

dP

inus

sylv

estr

isse

edli

ngs

and

adul

ts

1–10

-yea

r-ol

dP

inus

sylv

estr

isna

tura

lre

gene

rati

onfr

oman

nual

seed

ing

inco

nspe

cifi

cfo

rest

Fie

ldso

il;

upto

10fu

ngal

spec

ies,

acco

unti

ngfo

r74

%–9

2%of

EC

M,

occu

rred

onse

edli

ngs,

old

tree

s

Non

eS

eedl

ings

natu

rall

yre

gene

rate

dw

ith

EC

M,

corr

espo

nd-

ing

wit

hE

CM

onol

dtr

ees

Non

e,ex

cept

that

seed

ling

sha

dsu

c-ce

ssfu

lly

rege

nera

ted

from

seed

Aut

hors

sugg

est

CM

Nis

sign

ific

ant

for

perp

etu-

atio

nof

EC

Msp

ecie

san

dco

mm

unit

ies

inbo

real

fore

sts

dis-

turb

edfr

eque

ntly

bylo

w-i

nten

sity

fire

Jons

son

etal

.19

99b

Tab

le3.

Sum

mar

yof

rece

ntst

udie

sex

amin

ing

pote

ntia

lef

fect

sof

ecto

myc

orrh

izal

(EC

M)

orar

busc

ular

myc

orrh

izal

(AM

)co

mm

onm

ycor

rhiz

alne

twor

ks(C

MN

)on

plan

tpe

r-fo

rman

cean

dpl

ant

com

mun

ity

dyna

mic

s.

Page 16: Mycorrhizal networks: a review of their extent, function, and

© 2004 NRC Canada

Simard and Durall 1155

Myc

orrh

izal

type

and

stud

yco

ndit

ions

Pla

ntsp

ecie

san

dpl

anti

ngde

sign

Met

hod

used

tote

stef

fect

ofC

MN

Fun

gal

inoc

ulan

ts

Isot

ope

used

tote

stfo

rtr

ansf

er

Eff

ect

ofC

MN

trea

tmen

ton

fung

alco

mm

unit

y

Eff

ect

ofC

MN

onin

divi

dual

plan

tpe

rfor

man

ceP

lant

com

mun

ity

effe

cts

stud

ied

orsu

gges

ted

Ref

eren

ce

EC

M,

fiel

dP.

men

zies

iise

ed-

ling

spl

ante

din

shru

bpa

tche

sdo

min

ated

byar

buto

idA

rcto

stap

hylo

sgl

andu

losa

and

AM

Ade

nost

oma

fasc

icul

atum

P.m

enzi

esii

seed

-li

ngs

grow

n4–

10m

onth

sfr

omse

edin

patc

hes

ofA

deno

stom

aan

dA

rcto

stap

hylo

s;li

ght,

soil

,nu

tri-

ents

,an

dal

lelo

path

yw

ere

not

impo

rtan

tto

seed

ling

resp

onse

Fie

ldso

il.

Aft

er10

mon

ths,

17E

CM

spec

ies

colo

-ni

zed

both

P.m

enzi

esii

and

A.

glan

dulo

sain

patc

hes

ofA

rcto

stap

hylo

s;in

sam

eco

re,

85%

ofP.

men

zies

iian

d49

%of

thei

rE

CM

biom

ass

colo

nize

dby

fung

iof

Arc

tost

aphy

los

Non

eA

fter

4m

onth

s,P.

men

zies

iise

ed-

ling

sin

four

offi

veA

rcto

stap

hylo

spa

tche

sw

ere

colo

-ni

zed

bysi

xE

Msp

ecie

sw

here

asse

edli

ngs

intw

oof

five

Ade

nost

oma

patc

hes

wer

eco

lo-

nize

dby

two

EC

Msp

ecie

sof

The

leph

ora

P.m

enzi

esii

seed

ling

mor

tali

tyhi

gher

inA

deno

stom

ath

anA

rcto

stap

hylo

spa

tche

s;no

seed

-li

ngs

surv

ived

inpa

tche

sof

Ade

nost

oma,

whe

reas

20%

sur-

vive

din

the

Arc

tost

aphy

los,

mai

nly

due

toE

CM

inoc

ulum

diff

eren

ces

Sur

viva

lof

esta

blis

hing

seed

ling

sw

asgr

eatl

yin

crea

sed

whe

nas

soci

-at

edw

ith

the

exis

ting

CM

Nin

Arc

tost

aphy

los

patc

hes.

Aut

hors

sugg

est

that

EC

Msp

ecie

ssh

ared

byP.

men

zies

iian

dA

rcto

stap

hylo

sco

n-ne

cted

the

two

host

plan

ts,

crea

ting

cond

i-ti

ons

cond

uciv

efo

rC

tran

sfer

tow

ard

P.m

enzi

esii

Hor

ton

etal

.19

99

EC

M,

fiel

dM

icro

berl

inia

bisu

lcat

a,Te

trab

erli

nia

bifo

liat

a,an

dTe

trab

erli

nia

mor

elia

nase

ed-

ling

spl

ante

din

unde

rsto

ry

Con

spec

ific

seed

-li

ngs

plan

ted

into

fore

sts

wit

hhi

ghan

dlo

wba

sal

area

ofE

CM

adul

ttr

ees

Fie

ldso

ilN

one

Hig

her

myc

orrh

izat

ion

inhi

gh-E

CM

than

inlo

w-E

CM

fore

st;

noef

fect

ofm

ycor

rhiz

atio

non

seed

ling

biom

ass,

but

thos

ew

ith

high

EC

Mha

dhe

avie

rta

proo

ts

Onl

yon

esp

ecie

sin

crea

sed

insu

r-vi

val

orbi

omas

sin

the

high

-EC

Mfo

rest

;su

rviv

ors

oftw

otr

eesp

ecie

sw

ere

heav

ier

inhi

gh-E

CM

fore

sts

Hig

hba

sal

area

ofE

CM

adul

ts,

less

effe

ctiv

ene

twor

kco

nnec

tion

s,or

NM

tran

spla

nts

may

have

mas

ked

the

impo

rtan

ceof

the

CM

Nto

esta

blis

hing

rege

nera

tion

prov

ided

byco

nspe

cifi

cad

ults

New

berr

yet

al.

2000

EC

M,

fiel

dPa

rabe

rlin

iabi

foli

ata

seed

-li

ngs

plan

ted

unde

rA

fzel

iabi

pind

ensi

s,B

rach

yste

gia

cyno

met

roid

es,

Para

berl

inia

bifo

liat

a,an

dT.

bifo

liat

aad

ults

See

dlin

gspl

ante

d5–

30m

away

from

adul

tsei

ther

inco

ntac

tw

ith

adul

tro

ots

oris

olat

edin

side

aP

VC

tube

Fie

ldso

ilN

one

Num

ber

ofse

edli

ngs

wit

hm

ycor

rhiz

aean

dde

gree

ofin

fect

ion

high

erw

here

seed

ling

sin

cont

act

wit

had

ult

root

sth

anis

olat

ed;

myc

orrh

izat

ion

decl

ined

wit

hdi

s-ta

nce

from

adul

ts

See

dlin

gsu

rviv

alan

dbi

omas

shi

gher

whe

reco

ntac

tw

ith

adul

tro

ots

than

whe

reis

olat

ed;

per-

cent

age

ofE

CM

seed

ling

sde

clin

edw

ith

dist

ance

,bu

tno

tsu

rviv

al,

soE

CM

and

com

peti

-ti

onim

port

ant

CM

Nw

asim

port

ant

inth

ere

gene

rati

onof

EC

Mtr

ees

inan

AM

-do

min

ated

trop

ical

rain

fore

stin

Cam

er-

oon;

diff

eren

tad

ult

tree

spec

ies

had

diff

er-

ent

inoc

ulum

pote

ntia

lsfo

rpl

ante

dse

edli

ngs;

rege

nera

tion

shou

ldbe

carr

ied

out

unde

rco

nspe

cifi

cpa

rent

tree

s

Ong

uene

and

Kuy

per

2002

Tab

le3.

(con

tinu

ed).

Page 17: Mycorrhizal networks: a review of their extent, function, and

© 2004 NRC Canada

1156 Can. J. Bot. Vol. 82, 2004

Myc

orrh

izal

type

and

stud

yco

ndit

ions

Pla

ntsp

ecie

san

dpl

anti

ngde

sign

Met

hod

used

tote

stef

fect

ofC

MN

Fun

gal

inoc

ulan

ts

Isot

ope

used

tote

stfo

rtr

ansf

er

Eff

ect

ofC

MN

trea

tmen

ton

fung

alco

mm

unit

y

Eff

ect

ofC

MN

onin

divi

dual

plan

tpe

rfor

man

ceP

lant

com

mun

ity

effe

cts

stud

ied

orsu

gges

ted

Ref

eren

ce

EC

M,

fiel

dQ

uerc

usru

bra

acor

nspl

ante

dad

jace

ntto

live

EM

Que

rcus

mon

tana

(nea

r-Q

uerc

us),

dead

Q.

mon

tana

(nea

r-de

ad-

Que

rcus

),an

dA

MA

cer

rubr

um(n

ear-

Ace

r)st

ump

spro

uts

EC

Mvs

.A

Mst

ump

spro

uts

test

edE

CM

infl

uenc

ew

itho

utso

ildi

s-tu

rban

ce;

Que

rcus

mon

tana

redu

ced

root

graf

ting

wit

hQ

.ru

brum

;liv

evs

.de

adte

sted

site

alte

rati

onvs

.in

dica

tion

Fie

ldso

ilN

one

Nea

r-Q

uerc

usse

ed-

ling

sin

fect

edby

EC

Mm

ore

rapi

dly

and

toa

grea

ter

exte

nt(4

×)

wit

ha

diff

eren

tan

dm

ore

dive

rse

EM

com

-m

unit

yth

anne

ar-

Ace

ror

near

-dea

d-Q

uerc

usse

edli

ng.

Nea

r-Q

uerc

usse

ed-

ling

sha

dgr

eate

rN

and

Pco

nten

tsth

anin

the

othe

rtr

eat-

men

tsan

dgr

eate

rgr

owth

inth

anth

ene

ar-A

cer

trea

tmen

t

Aut

hors

sugg

est

grea

ter

infe

ctio

nof

seed

ling

sN

ear-

Que

rcus

occu

rred

via

hyph

alli

nks

wit

hliv

ero

ots

ofst

ump

spro

uts;

data

supp

ort

mic

rosi

teal

tera

tion

hypo

thes

isth

atliv

ero

ots

ofQ

.m

onta

nain

crea

sed

qual

ity

and

quan

tity

ofE

CM

,le

adin

gto

incr

ease

dse

edli

nggr

owth

and

nutr

itio

n;in

crea

sing

dens

ity

ofQ

.m

onta

naco

uld

mas

kbe

nefi

ts

Dic

kie

etal

.20

02

AM

,m

icro

-co

sms

inla

b

20he

rbsp

ecie

sin

trod

uced

toea

chm

icro

cosm

whe

regr

azin

g,m

ycor

rhiz

atio

n,an

dhe

tero

geno

ussp

atia

ltr

eat-

men

tsap

plie

d

NM

cont

rols

Glo

mus

cons

tric

tum

used

toin

ocul

ate

seed

ling

sin

myc

orrh

izal

trea

tmen

t

14C

Pla

ntse

edli

ngs

wer

ein

fect

edw

ith

AM

Pla

ntdi

vers

ity

incr

ease

d,w

hile

yiel

dof

dom

inan

tFe

stuc

aov

ina

decr

ease

dan

dA

Msu

bord

inat

esp

ecie

sin

crea

sed;

14C

tran

sfer

red

toA

Mbu

tno

tN

Msu

bord

inat

es

Aut

hors

sugg

est

that

Cm

ovem

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plan

tsvi

aa

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dW

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n19

99

Tab

le3.

(con

tinu

ed).

Page 18: Mycorrhizal networks: a review of their extent, function, and

© 2004 NRC Canada

Simard and Durall 1157

Myc

orrh

izal

type

and

stud

yco

ndit

ions

Pla

ntsp

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NM

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Fest

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ler

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ulum

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fit

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efr

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plan

ts;

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ofC

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mas

ked

byco

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on

Kyt

õvii

taet

al.

2003

Not

e:M

C,

myc

orrh

izal

cont

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NM

,no

nmyc

orrh

izal

.

Tab

le3.

(con

clud

ed).

Page 19: Mycorrhizal networks: a review of their extent, function, and

fected more rapidly with a greater diversity of mycorrhizalfungi; they may tap into an established CMN supported by Cinputs from other plants; they may access a larger pool ofsoil nutrients and water through the CMN; they may receiveC, nutrients, or water transferred directly from other plants;or they may have greater access to available nutrientsthrough CMN interactions with other soil organisms. Thesebenefits may be of life-or-death significance to a plant ifthey come, no matter how briefly, at a particular critical pe-riod during the plant-establishment phase. Once tapped intothe CMN, seedlings may be more likely to survive the criti-cal regeneration period in stressed or harsh environments,such as in deep shade (Simard et al. 1997a; Onguene andKuyper 2002), drought (Borchers and Perry 1990; Marler etal. 1999; Horton et al. 1999), at high elevations (Perry etal. 1989; Jumpponen and Trappe 1998), or on severely orfrequently disturbed sites. The CMN may be particularlysignificant for natural regeneration of temperate and borealforests that are frequently disturbed by wildfire, where itprovides critical linkages through time between the old andnew forests (Perry et al. 1992; Jonsson et al. 1999a).

Potential mycorrhizal network influences on plant estab-lishment have been studied fairly extensively in the field.Studies have used several techniques to separate CMN fromnon-CMN effects, including soil transfers (Perry et al. 1989;Perry et al. 1992), soil trenching (Simard et al. 1997c;Onguene and Kuyper 2002), mycorrhizal versus nonmy-corrhizal or incompatible control plants (Simard et al.1997a; Lerat et al. 2002; Kytoviita et al. 2003), plantingseedlings in mycorrhizal-compatible versus noncompatibleplant communities (Horton et al. 1999), or by seeding orplanting into an existing plant community followed byexamination of mycorrhizae and regeneration patterns(Jumpponen and Trappe 1998; Jonsson et al. 1999b;Newberry et al. 2000; Bidartondo et al. 2000; Dickie et al.2002). None of these studies investigated C or nutrient trans-fers, but rather have quantified general responses of seed-lings and mycorrhizae following association or linkage intothe CMN of established plants. In most cases, seedling bene-fits appear to have resulted from increased mycorrhizal di-versity by association with mature plants. Several of thesestudies are described next.

A number of field studies that support the hypothesis thata CMN can enhance plant establishment and performancehave been conducted in the temperate coniferous forests ofwestern North America. In a series of elegant experimentsin high-elevation Oregon mountains, Perry and associatesfound that regenerating P. menziesii seedlings benefitedgreatly from growing in soils transferred from beneath hard-woods compared with unamended, disturbed soils (Perry etal. 1992). Their work suggested that direct transfer ofmycorrhizal inocula from hardwoods to Douglas-fir was oneof several important factors that helped facilitate establish-ment of Douglas-fir. It corroborated earlier evidence fromDeacon et al. (1983) that seedlings planted close to birchparents formed shared, “late-stage” fungi while those at dis-tance formed different “early-stage” fungi. Since then,Simard et al. (1997c) found that P. menziesii seedlingsplanted in the understory of mature P. menziesii andB. papyrifera forests in British Columbia had higher netphotosynthetic rates, higher ECM diversity and richness, and

a different community of ECM morphotypes (more late-stage and strand-forming ECM) in untrenched (in contactwith root systems of mature trees) than in trenched plots(isolated from mature trees). Access to the higher mycelialinoculum density near the mature trees in the untrenchedtreatment likely accounted for the more diverse and robustECM community on understory P. menziesii seedlings, pos-sibly imposing a greater C drain on the seedlings and there-fore stimulating higher net photosynthetic rates than in thetrenched treatment. In another study that sought to explainpreferential establishment of P. menziesii in Arctostaphylosshrub patches within the California chaparral vegetationtype, Horton et al. (1999) found that P. menziesii seedlingswere colonized more frequently by a greater richness ofECM fungi in Arctostaphylos patches than in Adenostomapatches, corresponding with greater survival rates in theArctostaphylos patches. The authors suggested ECM ino-culum differences between shrub species largely accountedfor the P. menziesii survival differences and that ECM spe-cies shared by P. menziesii and Arctostaphylos connectedthe two host plants, creating conditions conducive for Ctransfer toward P. menziesii. Both the studies of Simard etal. (1997c) and Horton et al. (1999) were able to discountmost environmental factors (e.g., light, available nutrients,or soil water) that could provide an alternative explanationfor seedling performance differences in their treatments.

Similar patterns of tree-seedling establishment have alsobeen found in temperate and tropical forests dominated byhardwood tree species (Newberry et al. 2000; Dickie et al.2002; Onguene and Kuyper 2002). These studies make thefollowing two important contributions: (i) mycorrhizal facili-tation is likely important in secondary succession wheresymbiont populations are potentially limiting, contrastingwith more traditional concepts of facilitation involving pri-mary succession or harsh environmental conditions, and(ii) benefits of mycorrhizal facilitation may be masked bycompetition for resources when tree densities increasebeyond some threshold level. The benefits of mycorrhizalinfection probably happens at relatively low tree densities(Dickie et al. 2002), a suggestion that is corroborated byother studies (Kranabetter 1999; Hagerman et al. 2001).Dickie et al. (2002) found that establishment of ECMQuercus rubrum L. seedlings in a burned and salvage-loggedforest was facilitated by planting the acorns near sproutingstumps of Q. montana Willd. (congeneric was used to elimi-nate possibility of root grafting) but was relatively sup-pressed when planted near sprouting stumps of AM Acerrubrum L. Seedlings planted near Q. montana had a morediverse and different community of ECM fungi, greater Nand P contents, and greater growth relative to seedlingsplanted near A. rubrum, indicating indirect facilitationthrough increased seedling ECM formation. The authorssuggest that with increasing overstory density, mycorrhizalinfection benefits would be overwhelmed by competition forresources, resulting in decreasing Q. rubrum growth. In asimilar study, Onguene and Kuyper (2002) found that 1-month-old seedlings planted into a tropical rainforest hadgreater survival, biomass, and ectomycorrhizal formationwhen they were in contact with conspecific adult roots thanwhen they were isolated. They also found that mycor-rhization declined with distance from parents, while survival

© 2004 NRC Canada

1158 Can. J. Bot. Vol. 82, 2004

Page 20: Mycorrhizal networks: a review of their extent, function, and

did not, suggesting that seedling survival was probably alsopositively influenced by declining competition with distancefrom parents. Corroborating results have been found inclearcut, mixed hardwood – conifer sites in British Colum-bia. Pseudotsuga menziesii planted in a low-density mixturewith B. papyrifera had faster leader growth and higher netphotosynthetic rates in untrenched than in trenched plotsduring the first 3 years after establishment, but this was re-versed in subsequent years after B. papyrifera had outgrownP. menziesii (S.W. Simard, unpublished data). The crossoverfrom positive to negative effects of B. papyrifera neighborson P. menziesii performance happened more quickly in high-than in low-density mixtures.

In some ecosystems, the competitive effects of neighborsmay completely mask facilitative effects of the CMN, evenat low densities and very early during plant establishment. Ina pot study using subarctic herbs, Kytoviita et al. (2003)found that biomass growth of solitary seedlings improvedwith AM inoculation, but these benefits were completelylost when the AM seedlings were linked to adult Sibbaldiaprocumbens L. plants via the CMN. In the absence ofmycorrhizal fungi, by contrast, nonmycorrhizal seedlingsgrew equally well alone or in the presence of a non-mycorrhizal Sibbaldia adult. The authors suggested that theCMN vectored competition between established plants andseedlings, masking any benefits that may have been con-ferred by the CMN. These studies show that the effectsof mycorrhizal symbioses and the CMN on seedling-establishment patterns can vary considerably, depending onthe plant species, fungal species, growing environment, andlife stage of the different plants within a community.

In summary, studies examining CMN effects on plant es-tablishment have found that association with a mature plantresults in seedlings infected with a greater richness or diver-sity of mycorrhizal fungi, a greater proportion of fungishared in common with the mature plant, or a greater pro-portion of strand-, cord-, or rhizomorph-forming fungi. Inmany cases, this has been associated with greater plant per-formance, as measured by increased survival, growth, photo-synthetic rate, or tissue nutrient contents. In none of thesestudies, however, is there convincing evidence that these ef-fects have resulted from C or nutrient transfer from matureplants, even though it is commonly suggested as one of sev-eral potential facilitative mechanisms. Conversely, there ismore evidence that the benefits arise simply from increasedmycorrhization, which may or may not require CMN forma-tion. The beneficial effects of mature plants have beenshown to decrease with increasing neighbour density, prox-imity, or size, suggesting there may be threshold levels atwhich competition for resources outweighs the beneficial ef-fects of CMN inoculation. Future studies in this area need toseparate the effects of C or nutrient transfer from simplemycorrhization and to identify plant community factors thatregulate seedling facilitation by the CMN.

CMN effects on plant competition and diversitySeveral studies have examined the potential effects of a

CMN on inter- and intra-specific competition among plants,even though all suffered from inadequacies in clearly dem-onstrating the existence of a functional CMN. These studiessuggest, however, that the CMN has the potential to decrease

(Grime et al. 1987; Perry et al. 1989; Gange et al. 1993;Moora and Zobel 1996) or increase interplant competition(Eissenstat and Newman 1990; Eason et al. 1991; Hartnett etal. 1993; Bethlenfalvay et al. 1996a; Rejon et al. 1997).Grime et al. (1987) suggested that competitive intensity maybe reduced by the direct flow of C or nutrients from suffi-cient to deficient plants, resulting in greater growth of subor-dinate relative to dominant plants, and greater plantcommunity diversity. On the other hand, there is some evi-dence that competitive dominance may increase, becauselarger plants acquire greater resources from the CMN be-cause of their higher nutrient demand (Zabinski et al. 2002).In some cases, competitive intensity within plant communi-ties may simply be affected by greater, faster, more diverse,or different mycorrhization of plants tapping into the CMN,resulting in increased nutrient access for some plant species.

In one of the first studies that found evidence for CMN ef-fects on interspecific competition, Perry et al. (1989) exam-ined interactions between P. menziesii and Pinus ponderosaDougl. ex P. Laws. & C. Laws. in a replacement-series de-sign with none, two, or four common ECM species added.They found that the two tree species mutually inhibited eachother with no ECM added (but with a Thelphora contami-nant), but that this antagonism disappeared with added ECMspecies, particularly with added generalist Laccaria laccata(Scop.: Fr.) Cooke, resulting in larger P. menziesii seedlingswith more foliar N and P content. The benefits to P. men-ziesii came at no expense to growth or nutrient content ofPinus ponderosa. The authors suggested that competitionwas reduced because a CMN increased access to nutrients, aCMN distributed nutrients more evenly, or more simply thatthe greater diversity of fungi was active over a broader rangeof environmental conditions. Perry et al. (1989) were veryeffective in separating inter- and intra-specific competitiveeffects as well as eliminating the confounding effects ofcompetitor density through the use of a replacement-seriesdesign (Harper 1977). In their experiment, however, contam-ination of the “no-ECM” control by Thelephora may havemasked some of the CMN effects. In addition, the designmade it difficult to separate CMN effects from fungal diver-sity effects on competitive interactions. Some of the prob-lems with this experimental design may be avoided in futureexperiments by use of growth chambers to reduce contami-nation, mesh barrier controls that prevent formation ofhyphal connections, and isotopic tracers to confirm the pres-ence of links and interplant nutrient transfer.

A similar replacement-series approach was also used inthe field by Jones et al. (1997) to examine the effects of treespecies composition and density on the ECM communitiesof P. menziesii and B. papyrifera. Evenness of the ECMcommunity on P. menziesii was higher when grown in mix-ture with B. papyrifera than when grown alone because ofincreases in minor types, and this may have resulted from ei-ther coinoculation from neighboring birch hosts (Massicotteet al. 1994; Simard et al. 1997b) or modification of soilsby birch favoring different mycorrhizal fungi. Jones et al.(1997) found that 91% of B. papyrifera and 56% of P. men-ziesii mycorrhizae were types common to the two tree spe-cies, and they hypothesized that the resulting CMN mayreduce the negative effects of competition between the twotree species. This hypothesis was supported by Simard et al.

© 2004 NRC Canada

Simard and Durall 1159

Page 21: Mycorrhizal networks: a review of their extent, function, and

(1997a), who showed on the same sites that net C transferfrom B. papyrifera to P. menziesii increased with increasingshading of P. menziesii.

In studies seeking to explain why AM fungi increased thecompetitive dominance of the exotic invasive Centaureamaculosa auct. non Lam over native Festuca idahoensisElmer in Montana grasslands, Marler et al. (1999) andZabinski et al. (2002) used 13C to test whether the CMN hadmediated a parasitic drain by Centaurea maculosa fromF. idahoensis or whether it simply enhanced the competitiveability of Centaurea maculosa for soil resources. Zabinski etal. (2002) found that the CMN did not facilitate C transferfrom F. idahoensis to Centaurea maculosa, but rather thatit increased P uptake by Centaurea maculosa, particularlywhen paired with grasses rather than forbs. Forming a CMNwith grass increased access of AM Centaurea maculosa to Pover a wider soil pool covering the neighbor’s rooting zone,resulting in greater plant biomass and luxury consumption ofP. While the CMN in this study did not appear to serve as aconduit of resource transfer, it may have benefited plants inthe community by increasing hyphal development with mul-tiple hosts over a larger soil pool of resources. Either mecha-nism can result in changes in the plant community.

Changes in competitive interactions among plants result-ing from a CMN have been suggested to affect plant com-munity diversity. Reduced interspecific competition, forexample, can reduce the abundance of canopy dominants,increase abundance of subordinates, and result in a moreevenly distributed and diverse plant community. Grime et al.(1987) observed apparent one-way 14C transfer from canopy-dominant F. ovina to understory herbs and grasses, whichthey suggested occurred through a CMN along a naturalsource–sink gradient for assimilate and may have accountedfor increased diversity and more even biomass distributionamong plants. This work was later criticized, because nettransfer and the transfer pathway were not examined (Fitteret al. 1999), and interplant variation in C physiology andAM dependency was not adequately demonstrated. van derHeijden (2002) subsequently reanalysed the data of Grime etal. (1987) and found that subordinate plant species with thehighest mycorrhizal dependency obtained the most 14C fromF. ovina, thus benefiting the most from the CMN. He sug-gested that the number and relative abundance ofmycorrhizal-dependent plant species may help explain thedifferences in how AM fungi, the CMN, and interplant Ctransfer affect different plant communities. It may explain,for example, why Hartnett and Wilson (1999) found thatplant diversity increased when AM mycorrhization declinedfollowing benomyl treatments in a tallgrass prairie, the op-posite result of Grime et al. (1987). Suppression of AMmycorrhizae decreased abundance of the dominant, obli-gately mycotrophic C4 tallgrasses and increased abundanceof subordinate facultatively mycotrophic C3 plants. However,Walter et al. (1996) earlier showed that more 32P was trans-ferred to facultatively mycorrhizal plants than to obligatelymycorrhizal plants in a similar prairie, leading Hartnett andWilson (1999) to conclude that changes in plant diversity intheir experiment resulted more from differences in host re-sponses to AM than to alteration in resource distributionamong neighbors via the CMN.

Evidence for CMN or C transfer effects on competitive

interactions and plant community diversity is inadequate.Several studies above have used isotopes to trace transferthrough a CMN, but most suffer from lack of adequate non-CMN controls (e.g., Grime et al. 1987; Perry et al. 1989;Walter et al. 1996), and few have been conducted underfield conditions. Most studies suggest that non-CMN mecha-nisms, such as changes in soil chemistry or mycorrhizalinfection patterns, are just as likely to explain plant commu-nity competition or diversity changes as CMN or transfermechanisms. Although laboratory and greenhouse studiesprovide greater opportunity for precisely examining theCMN, they provide an unrealistic picture of how the CMNaffects plant communities in nature (Read 2002). More re-search is needed to improve our understanding of whether,where, and how the CMN affects competition and commu-nity diversity in nature. We also need to research those fac-tors that may alter CMN effects on plant communities,including different attributes of site quality (nutrient, water,and light limitations), plant species composition (source–sink patterns, mycorrhizal dependency), fungal species com-position, and stage of plant community development.

Conclusions

Recent field studies have increased our knowledge of theextent, function, and implications of CMNs, but only labstudies have unequivocally demonstrated the existence ofCMNs and their specific role in transferring C from one rootsystem to another. Field evidence for CMNs is supported byboth functional- and taxonomic-level data. The general lackof specificity, at least at the species level, of both AM andECM fungi to their host suggests that CMNs within grass-lands and forests are abundant and extensive. Whether speci-ficity to different host species occurs at a level lower thanspecies is still not well understood. Further research usingmolecular and microsatellite techniques will help to deter-mine whether this specificity occurs and whether it affectsCMN potential. C transfer between plants has been observedin both ECM and AM field studies (Simard et al. 1997a;Lerat et al. 2002), but the transfer mechanism has yet to befully investigated.

Newman (1988) emphasized the need to know whether(i) interplant C transfer in the field is one-way or bidirec-tional, (ii) transfer occurs through a CMN, (iii) transferred Centers the receiver shoot, and (iv) receiver plants benefit sig-nificantly from the CMN. Since this pivotal review, there isfield evidence of bidirectional and net transfer (Simard et al.1997a) and transfer to the receiver shoot in both ECM andAM plants (Simard et al. 1997a; Lerat et al. 2002). Thesestudies did not conclusively show whether the CMN acted asa conduit for C transfer, but they did clearly demonstratethat mycorrhizae facilitated transfer. These studies also pro-vided evidence that the direction and magnitude of C trans-fer was highly dependent on source–sink relations betweenlinked plants. Further field research is needed on plant andfungal source–sink relationships, how they affect magnitudeand direction of transfer, and the mechanisms by which theyinfluence transfer in nature.

Several studies have suggested that the CMN may play arole in improving seedling establishment, reducing or in-creasing plant competition, and reducing or increasing plant

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community diversity. The strongest evidence for CMN ef-fects on plant communities exists for seedling establishment.There is a need to examine CMN effects on plant competi-tion and diversity in nature with adequate controls for theCMN, adequate designs for addressing the confoundingeffects of density, composition, and diversity of plant andfungal communities, direct observation of the functionalCMN, and concurrent isotopic labeling to quantify bidi-rectional and net transfer. Once we have this information,we will be better able to understand the ecological signifi-cance of mycorrhizal networks.

Acknowledgements

We are grateful to the Organizing Committee for the invi-tation to present this review paper at the Fourth InternationalConference on Mycorrhizae in Montréal, Canada, in August2003. We thank Melanie D. Jones for providing valuablecomments on the manuscript.

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