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Arbuscular-mycorrhizal fungi: Potential roles in weed

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Article  in  Weed Research · October 2000

DOI: 10.1046/j.1365-3180.2000.00207.x

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 Arbuscular-mycorrhizal fungi: potential roles
in weed management
N R JORDAN, J ZHANG & S HUERD
Department of Agronomy and Plant Genetics, University of Minnesota, St Paul MN, USA

Received 15 October 1999

Revised version accepted 5 April 2000

Summary
The importance of interactions between arbuscular-mycorrhizal fungi (AMF) and weeds of agro-
ecosystems is reviewed. Considerable evidence suggests that AMF can a€ect the nature of weed
communities in agro-ecosystems in a variety of ways, including changing the relative abundance
of mycotrophic weed species (hosts of AMF), and non-mycotrophic species (non-hosts). These
e€ects may merely change the composition of weed communities without a€ecting the damage
that these communities cause. However, it is quite plausible that interactions with AMF can
increase the bene®cial e€ects of weeds on the functioning of agro-ecosystems. Through a variety
of mechanisms, weed:AMF interactions may reduce crop yield losses to weeds, limit weed species
shifts, and increase positive e€ects of weeds on soil quality and bene®cial organisms. If bene®cial
e€ects of AMF on the composition and functioning of weed communities can be con®rmed by
more direct evidence, then AMF could provide a new means of ecologically-based weed
management. Intentional management will be required to increase diversity and abundance of
AMF in many cropping systems, but these actions (e.g. conservation tillage and use of cover and
green-manure crops) typically will confer a range of agronomic bene®ts in addition to potential
1 improvements in weed management.

Keywords: weed ecology, biodiversity, biocontrol, integrated weed management.

Introduction
Farmers face very strong pressures to be cost-e€ective in production of food and ®bre, while
reducing the environmental impact of farming. In response, conservation tillage systems have
gained popularity in recent years (Swanton & Weis, 1991). These systems reduce fuel and labour
costs, as well as losses of nutrients and soil (Brown et al., 1989; Hildebrand, 1990). Also, cover
and green-manure crops are being used by a growing number of farmers to improve soil quality
and tilth, reduce fertility and pest-control inputs, and limit soil erosion (Lal et al., 1991; Liebman
& Dyck, 1993). One signi®cant e€ect of increased use of conservation tillage and cover crops is a
substantial increase in diversity and abundance of soil organisms (Doran & Linn, 1994; Neher &
Barbercheck, 1998). Soil organisms are fundamentally important to plant function, and can

Correspondence: N R Jordan, Department of Agronomy and Plant Genetics and, Minnesota Center for Community
Genetics, 1991 Buford Circle, St. Paul MN, 55108, USA. Tel: (+1) 612 625 3754; E-mail: [email protected]

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 398 N R Jordan et al.

strongly a€ect plant population and community dynamics (Watkinson, 1998). In particular, it is
clear that soil biota can a€ect weed biology and management (Boyetchko, 1996). We argue that a
more thorough assessment should be made of the potential value of increased soil biodiversity
for weed management, in order to expand the range of biotic interactions that can be employed
in the service of sustainable approaches to weed management (National Research Council, 1996).
This assessment should certainly encompass interactions between weeds and arbuscular-
mycorrhizal fungi (AMF). Many aspects of plant biology are known to be strongly a€ected by
AMF, which form symbiotic relationships with most vascular plants (Perez-Moreno & Ferrera-
Cerrato, 1997; Smith & Read, 1997). Furthermore, AMF can a€ect the dynamics, diversity and
2,3 productivity of plant communities (Zobel et al., 1997; Van Der Heijden et al., 1998a). It is evident
that increased use of conservation tillage and cover crops will increase the diversity and
abundance of AMF in soils (Johnson & P¯eger, 1992). We propose that agronomic management
to favour AMF may provide a means of directing weed community dynamics (Aldrich, 1984;
Swanton et al., 1993) so as to reduce negative e€ects of weeds, and increase their bene®cial e€ects.
In this review, we brie¯y survey knowledge of AMF in agro-ecosystems, and describe
mechanisms by which AMF might a€ect the functional ecology of weeds (i.e. their functional
biology considered in an ecological context). We then consider the possible in¯uence of AMF on
dynamics and agro-ecological functioning of weed communities, and suggest important research
directions.

AMF in agro-ecosystems

Agronomic management can strongly a€ect AMF abundance in agro-ecosystems, although

linkages between particular management factors and speci®c patterns of AMF abundance often
appear to be inconsistent. An increasing number of case studies demonstrate that high AMF
populations will develop in soils where certain conditions are met. These conditions include (i)
avoidance of bare-soil fallow, (ii) low inputs of tillage, synthetic fertilizers, and certain high-
phosphorus animal manures, and (iii) minimal rotation to crops that are poor or non-hosts to
AMF (Baltruschat & Dehne, 1988; Rosemeyer & Gliessman, 1992; Douds et al., 1993; Kurle &
P¯eger, 1994; Glavez, 1995; McGonigle & Miller, 1996; Boswell et al., 1998; Douds & Millner,
1999). Conventional high-input cropping systems often do not meet these conditions, and can
substantially reduce AMF diversity and abundance (Hamel, 1996; Smith & Read, 1997; Douds &
Millner, 1999). Prolonged failure to meet these conditions can result in very low population
4 densities of AMF in some high-input cropping systems (I Charvat, pers. comm.; Johnson et al.,
1992), although some AMF can persist in such situations (Ellis et al., 1992; Khalil et al., 1992;
Hooker & Black, 1995). Moreover, evidence is accumulating that crop monocultures or high-
nutrient inputs may cause a rapid shift in behaviour of AMF species or communities, resulting in
reduction in bene®ts provided to plants by AMF (Johnson, 1993; Johnson et al., 1997; Scullion
et al., 1998; Feldmann & Boyle, 1999). However, as we argue below, when AMF are present in
agro-ecosystems, they may be capable of strongly a€ecting the ecology of weeds.

AMF effects on weed functional ecology: nutrition, seed germination,

pathogen resistance and stress tolerance
AMF colonize roots of `mycotrophic' plant species (`host' species hereafter) and form
mycorrhizae, which are intimate connections between fungus and plant root. Mycorrhizae are

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 Mycorrhizal fungi and weed management 399

not formed with non-mycotrophic species (`non-host' species hereafter). The net e€ect of
colonization on plant function and ®tness can vary widely, from strongly bene®cial to strongly
deleterious (Johnson et al., 1997) and evidence is accumulating that these e€ects are typically
speci®c to a particular combination of AMF and plant genotypes (Bever et al., 1996). This more
nuanced view of AMF:plant relations is replacing the notion that the response of a given plant
species to AMF can be described categorically (Van der Heijden et al., 1998a).
For the plant, potential bene®ts of colonization include greatly increased uptake of soil
nutrients, especially phosphorus. Mycorrhizae serve to increase the volume of soil available for
acquisition of mineral nutrients by host plants (Smith & Read, 1997), via the nutrient uptake
capacity of the fungal mycelium in the soil (a network of fungal tissue within the soil). AMF-
facilitated nutrient uptake allows mycorrhizal plants to tolerate wide variation in soil fertility
(Varma, 1995). In addition to P, AMF have been reported to facilitate absorption and
accumulation of ammonium N, K, Ca, Mn, Fe, Cu, Zn, and Ni in various plants (Marschner &
Dell, 1994; Medeiros et al., 1994; Smith & Read, 1997). In a number of cases (e.g. Martensson
et al., 1998; Nasholm et al., 1999) AMF have been shown to play a signi®cant role in N
nutrition.
Among agricultural weeds that are AMF hosts, AMF infection has been shown to improve
growth, seed production and seed quality (Koide et al., 1988; Koide & Lu, 1992; Stanley et al.,
1993; Shumway & Koide, 1994a; Koide & Lu, 1995; Heppell et al., 1998). This e€ect has been
shown to be variable within the growing season, and to decline at higher plant densities (Koide &
Li, 1991; Shumway & Koide, 1994b). Such work has begun to characterize the e€ects of AMF on
the ecological functioning of weeds and weed populations. However, the focus has been on
species that are AMF hosts, and on e€ects on individual plant function or intraspeci®c
interactions. Processes critical to population and community dynamics, e.g. germination and
establishment, interspeci®c interactions, and stress tolerance in both host and non-host species,
have only begun to be examined in agricultural weeds.
There is some indication that germination and early growth of weedy species can be strongly
a€ected by AMF, and that some of these e€ects indicate parasitic or antagonistic behaviour of
AMF towards plants (Johnson et al., 1997). Francis & Read (1995) developed an experimental
system that modelled establishment of ruderal weeds in gaps in grassland ecosystems. A ®ne-
mesh ®lter was used to exclude plant roots from growing into the experimental soil volume, while
allowing development of an AMF mycelium. Very strong AMF e€ects on seed germination,
early growth and survival of target weeds were observed. Non-host species, including several
important agricultural weeds (Chenopodium album L. and Spergula arvensis L.) had germination,
early growth and survival rates sharply reduced by the presence of AMF mycelia. In these
interactions, fungal hyphae penetrated the roots of non-host species. Penetration was associated
with disrupted and distorted morphological development of roots, absence of arbuscules
(presumed sites of plant:fungus nutrient exchange), and a strong stunting e€ect on seedling and
plant growth (Francis & Read, 1995). Host species (e.g. Plantago lanceolata L.) showed the
opposite pattern, bene®ting strongly from mycelium presence.
This experiment is unique in examining seedling:mycelium interaction free of confounding
e€ects of seedling:root interactions. However, several other studies (Grubb, 1986; Allen et al.,
1989; Francis & Read, 1994; Muthukumar et al., 1997; Johnson, 1998) have produced evidence
consistent with this mechanism, in which early growth rates of non-host weedy species were
reduced in the presence of AMF. These studies highlight the capability of some AMF to exert
strongly antagonistic e€ects on some non-host species. There are also indications that non-host

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400 N R Jordan et al.

species may be actively antagonistic to AMF, e.g. via inhibitory compounds released into soil
(Fontenla et al., 1999). Notably, many troublesome agricultural weeds belong to families that
appear to be predominantly non-hosting (Hirrell et al., 1978; Tester et al., 1987; Brundrett,
1991; Francis & Read, 1994), including Amaranthaceae, Brassicaceae, Caryophyllaceae,
Chenopodiaceae, Cyperaceae, and Polygonaceae. Moreover, agricultural weeds that are
members of families that commonly host AMF (e.g. Poaceae, Compositae) have been shown
in some cases to be non-mycorrhizal (Harley & Harley, 1987; Feldmann & Boyle, 1999). It is
clearly premature to delimit the prevalence of hosting behaviour among agricultural weeds.
However, there are good grounds to hypothesize that, when present, AMF may reduce the
prevalence of non-host species in weed communities.
Other e€ects of AMF that are of potential importance to the distribution and abundance of
weeds include e€ects on interactions between weeds and their pathogens and herbivores, and
response of weeds to environmental stresses. Protective e€ects of AMF infection against a range
of pathogens have been documented (Fitter & Garbaye, 1994; Newsham et al., 1995a), in
controlled environments (Linderman, 1992; Fitter & Garbaye, 1994) and ®eld settings (West
et al., 1993; Newsham et al., 1995b; Smith & Read, 1997; Little & Maun, 1996). Similar
protective e€ects against above-ground herbivory by insects have been observed in some but not
all cases (Gange & Bower, 1997).
AMF may a€ect weed responses to a number of forms of environmental stress. For example,
AMF have been found to improve drought tolerance (Bethlenfalvay, 1992). AMF inoculation of
corn increased growth and yield over a range of drought stress treatments (Sylvia & Williams,
1992). Mechanistically, it is clear that many physiological processes that in¯uence plant water
relations and drought tolerance are a€ected by AMF (Bethlenfalvay, 1992). AMF can also
improve plant tolerance of other stresses, including high soil temperature, saline soil, adverse soil
pH, and toxic metals (Mosse et al., 1981; Bagyaraj, 1990; Munyanziza et al., 1997). Also, weed
species that are germinating in the understory of a mycorrhizal crop species may bene®t from
mycorrhizae that are subsidized by energy from other plants connected to the mycelium (Smith &
Read, 1997). This subsidy may permit these species to survive and produce seeds despite low
light levels and perhaps other stress factors.

Effects of AMF:weed interactions on dynamics

and agro-ecological functioning of weed communities
As would be expected from the manifold e€ects of AMF on plant function at the individual level,
AMF:plant interactions can also a€ect plant communities, particularly by a€ecting regeneration
processes and outcomes of interspeci®c competition (Allen & Allen, 1990). From a
weed-management perspective, we wish to draw attention to two possible e€ects of AMF on
weed communities. First, as noted above, AMF are likely to in¯uence the composition of weed
communities and the relative abundance of species within them. Second, AMF may change the
agro-ecological functioning of weed communities, so that the net e€ect of weeds becomes more
bene®cial.
The composition of plant communities can be strongly a€ected by AMF. Evidence from a
variety of plant communities indicates that host species generally fare more poorly in competitive
interactions with non-hosts when AMF are absent (Watkinson, 1998). Relevant studies have
been conducted on experimental systems ranging from two-species competition experiments in
pots, to studies of the dynamics of experimental plant communities in `microcosms' established

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 Mycorrhizal fungi and weed management 401

in large pots, to ®eld studies in which various treatments were applied to reduce or eliminate
AMF (Fitter, 1977; Hall, 1978; Allen & Allen, 1984; Carey et al., 1992; Hartnett et al., 1994;
West, 1996; Streitwolf-Engel et al., 1997; Marler et al., 1999). For example, the productivity of
host species relative to non-hosts was increased by AMF in controlled-environment studies of
experimental communities of grasses and forbs (Grime et al., 1987; Wilson & Hartnett, 1997).
Grime et al. (1987) found that biomass production of host species was suppressed by certain
dominant non-hosts in the absence of AMF, and this suppression was greatly relieved (over
300% increase in biomass) when AMF were present. AMF can also cause reductions in
performance of non-host weeds. For example, in a ®eld experiment in a non-agricultural setting,
density of the non-host weed Salsola kali L. was reduced 30±50% by AMF inoculation (Allen &
Allen, 1988).
For weeds of agro-ecosystems, AMF e€ects on interactions between host and non-host
species have been assessed in several controlled-environment studies involving pair-wise
interactions (Crowell & Boerner, 1988; Boerner & Harris, 1991; Koide & Li, 1991; Borowicz,
1993). In each case, experimental suppression of AMF resulted in substantial reduction in the
relative performance of the host weed species. In preliminary work extending these comparisons
to a weed community context (N R Jordan, S Huerd & J Zhang, unpubl. obs.), we found that a
multispecies ®eld-collected AMF inoculum signi®cantly increased the overall density and
biomass of host weeds in experimental communities grown in large pots in a greenhouse. In one
experiment, presence of AMF also reduced the total density of non-host weeds. Responses of
host-weeds to AMF were consistent across two soil media, providing a ®rst indication of the
potential e€ect of AMF in shaping weed communities. A single published study has examined
®eld-crop weeds in a ®eld setting (Sanders & Koide, 1994). Survival, growth, seed production and
quality, and P concentration were compared in two host species [Abutilon theophrasti Medic. and
Setaria lutescens (Weigel) F T Hubb] and a non-host species (Amaranthus retro¯exus L.). Soil
fumigation was used to remove AMF, and this treatment was compared with fumigated soil
inoculated with AMF and an unfumigated soil. For most measures of performance,
A. theophrasti bene®ted and A. retro¯exus su€ered when AMF were present, while S.
lutescens responded little. Host species that are strongly responsive to mycorrhizae (i.e. are
strongly bene®ted by AMF colonization, Smith & Read, 1997) would be expected to su€er more
in the absence of AMF than less responsive hosts. In this experiment, S. lutescens, which has
been observed to have little response to AMF infection (Koide & Li, 1991), provides an example
of a less-responsive species.
Many mechanisms may be responsible for the observed bene®cial e€ects of AMF on host
species in mixtures of hosts and non-host species. First, these e€ects may result from antagonistic
e€ects of AMF on non-host species, as described above. In preliminary work, we have found a
consistent pattern of inhibition of non-host species when seedlings of single weed species were
exposed to a multispecies AMF inoculum. Most notably, we found that exposure to the
inoculum caused a 90% reduction in biomass production by A. retro¯exus. Overall, we observed
a mean biomass reduction of 60% for that species and ®ve other non-host species [Chenopodium
album, Polygonum lapathifolium L., Rumex obtusifolium L., Portulaca oleracea L., Brassica kaber
(DC) L C Wheeler; N R Jordan, S Huerd & J Zhang, unpubl. obs.]. If subsequent experiments
con®rm this result, it will suggest that AMF have considerable potential as a broad-spectrum
biocontrol agent of non-host weed species.
Alternatively, any of the various mechanisms by which AMF can bene®t host species may be
at work, e.g. nutrient uptake, or amelioration of e€ects of natural enemies or environmental

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 402 N R Jordan et al.

stresses. Conversely, given that AMF e€ects on individual plant function and ®tness vary widely
between positive and negative impacts (Johnson et al., 1997; Van der Heijden et al., 1998a), it is
quite possible that AMF could negatively a€ect the relative performance of certain host species
in plant mixtures.
The implication of these studies is that increased diversity and abundance of AMF is likely to
increase the relative abundance of host species in weed communities, although many exceptions
may occur. The question becomes how this e€ect of AMF, and others that may occur, bears
upon the issue of practical concern: the agro-ecological functioning of weed communities. The
functioning of weed communities should be viewed broadly, to include such emergent properties
as dynamic responses to management (e.g. rapidity of weed species shifts) and bene®cial e€ects,
such as those on soil quality, nutrient cycling, and populations of bene®cial organisms, as well as
the harmful e€ects that are the usual focus of investigation. Little direct evidence exists to
indicate how AMF might a€ect the functioning of weed communities, but a variety of indirect
evidence exists. We review what is known regarding AMF e€ects on two potentially signi®cant
attributes of weed communities: species diversity, and interspeci®c facilitative (i.e. bene®cial)
e€ects of weeds (Callaway, 1995) that are mediated by the AMF mycelium.
AMF e€ects on weed species diversity are of interest because agro-ecological e€ects of weeds
may be related to the species diversity of weed communities (Patriquin, 1986; Tilman, 1996;
Tilman et al., 1997), for example, the ability of weeds to maintain populations of desirable
organisms (e.g. bene®cial insects or mycorrhizal fungi) is likely to be related to weed community
diversity (Altieri, 1994; Feldman & Boyle, 1999). For plant communities generally, mechanisms
by which plant:AMF interactions a€ect plant community diversity have been explicitly examined
only in the computer-simulation studies of Bever et al. (1997). Diversity can be promoted when
AMF have a spatially heterogeneous distribution in the soil, or when AMF species and host
species do not provide fully reciprocal bene®ts (Bever et al., 1997). Other mechanisms by which
AMF may a€ect diversity are more speculative. Newsham et al. (1995b) argued that a spectrum
of bene®cial e€ects of AMF association is distributed di€erentially among host species. For
example, AMF may bene®t plant species with poorly branched root systems by enhancing P
uptake, while bene®ting plants with highly branched roots by some other means, e.g. via
protection against fungal pathogens. Their suggestion was that this distribution of bene®ts
promoted plant community diversity. Also, AMF may maintain diversity within weed
communities subjected to frequent environmental stresses, by preventing elimination of less
stress-tolerant species. On the other hand, AMF may decrease community diversity by favouring
a host species that is capable of competitive suppression of other species. As for e€ects of AMF
on performance of individual species, the net e€ects of AMF on diversity may be contingent on
the degree of AMF responsiveness of species that are capable of achieving community
dominance (Hartnett & Wilson, 1999). If these species are highly responsive to the AMF
community present at a particular location, then increased AMF may decrease diversity;
conversely, if these species are less responsive or non-hosts, increased AMF may increase
diversity.
Controlled-environment and ®eld studies (Grime et al., 1987; Streitwolf-Engel et al., 1997;
5 Van Der Heijden et al., 1998b) have provided cases where AMF acted to increase community
diversity. For example, Gange et al. (1993) monitored species richness in ruderal weed
communities for 4 years after establishment and observed a signi®cant positive association
between AMF infection and plant species richness. In contrast, plant diversity in a grassland was
decreased by increasing AMF (Hartnett & Wilson, 1999). In this case, experimental suppression

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 Mycorrhizal fungi and weed management 403

of indigenous AMF by soil fungicide applications reduced the dominance of a strongly AMF-
dependent grass species, while a variety of less-responsive or non-mycorrhizal species became
more abundant.
A second avenue by which AMF may a€ect agro-ecological functioning of weed communities
involves interspeci®c facilitative e€ects mediated by the mycelial network. Mycelial
interconnections among host species in a weed:crop mixture may cause patterns of resource
uptake and distribution among host species that di€er qualitatively from those occurring in plant
communities where AMF are absent (Fitter et al., 1998; Perry, 1998). Speci®cally, dying host
species may release nutrients into the AMF mycelium (Newman & Eason, 1993; Smith & Read,
1997; Bethlenfalvay et al., 1996; Rejon et al., 1997), which then may be redistributed among
other host species. This phenomenon may enable facilitative e€ects in crop:weed mixtures. For
example, after selective weed control, nutrients acquired by host weeds may be transferred to
host crop or cover crop via the mycelium (Bethlenfalvay et al., 1996). Such processes may result
in tighter nutrient cycling (Swift & Anderson, 1993) and reduced competitive e€ects of non-host
weeds (Rejon et al., 1997). If such phenomena occur and are qualitatively important, then AMF
may be capable of signi®cantly altering the agro-ecological functioning of weeds. For example,
properly timed control operations ± such as sublethal post-emergence herbicide applications ±
might be used to transfer nutrients from weeds to crops. In this scenario, the weeds would
function in e€ect as a temporary nutrient sink, reducing pre-emption of nutrients by non-host
weeds and leaching and other nutrient losses.
Also, facilitative e€ects may occur when one host species supports populations of mycorrhizal
fungi that are bene®cial to another species (Bethlenfalvay, 1992; Perry, 1995; Bever et al., 1996;
Feldmann & Boyle, 1999). Host species may release carbon into the mycelium which may
support formation of mycorrhizae with other hosts. In e€ect, host plants provide energy that
serves, directly or indirectly, to subsidize formation of mycorrhizae with newly germinating hosts
(Moora & Zobel, 1996; Smith & Read, 1997). This subsidy allows these seedlings to receive
nutrients or other mycorrhizal bene®ts while minimizing the energetic costs of mycorrhizal
establishment to seedlings. For example, weed communities in several cropping systems have
recently been shown to enhance mycorrhizal colonization and growth of subsequent crops
(Feldmann & Boyle, 1999; Kabir & Koide, 2000). However, this e€ect will be bene®cial only if
growth of the species that receives the subsidy is desirable. A counter-example is provided by a
recent demonstration of a substantial carbon subsidy to an invasive rangeland weed (Centaurea
6 maculatalam) via mycelial connections to desirable rangeland grasses (Marler et al., 1999).
It is also possible that AMF may have negative e€ects on agro-ecological functioning of weed
communities, simply by increasing abundance of problematic host weeds. A variety of such
7 weeds appear to be host species, such as Ambrosia artemisiifolia L., Avena fatua L., Abutilon
theophrasti, or Setaria lutescens (Crowell & Boerner, 1988; Koide & Li, 1991; Koide & Lu, 1992;
Koide et al., 1994). The challenge is to determine the balance of bene®cial and negative e€ects of
AMF on agro-ecological functions of weed communities.
The use of AMF to shape weed agro-ecological functioning of weed communities may o€er a
novel avenue of weed management. As demonstrated above, AMF are clearly capable of
powerfully inhibiting growth of certain non-host weed species. If this e€ect is common, then
AMF might serve as a broad-spectrum, self-sustaining biocontrol agent wherever agronomic
management can maintain populations of e€ective AMF. Similarly, if mutually-bene®cial
interactions between AMF and ecologically useful host weeds are commonplace, then AMF may
help to maintain these species in weed communities.

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 404 N R Jordan et al.

Research directions
First the mycorrhizal responsiveness of agricultural weeds is poorly known. Present notions of
the host/non-host status of weeds are generally based on ®eld surveys of root colonization
(Newman & Reddell, 1987; Boyetchko, 1996), but such indications of colonization do not resolve
parasitic or antagonistic interactions from mutualisms (Francis & Read, 1995). Mycorrhizal
responsiveness has been determined in terms of AMF e€ects on germination, growth and
reproduction for only a few major weed species, most of which are AMF hosts. Therefore,
further examination of mycorrhizal responsiveness of weeds is needed, focusing upon AMF
e€ects on weed germination, growth, stress tolerance, and interspeci®c interactions with other
plants, herbivores and pathogens. Particularly needed are characterizations of AMF e€ects on
these aspects of plant function in weeds from putative non-host families. Additional important
questions include the speci®city of interactions between particular weed species and particular
AMF taxa, and geographic and ecotypic variation in AMF:weed interactions. Such speci®city
and variation are to be expected ± genetic variation a€ecting the plant:AMF relationship is well
documented both within and among plant and AMF species (Koide et al., 1988; Bryla & Koide,
1990; Hetrick et al., 1993; Sanders et al., 1996; Smith & Read, 1997; Van der Heijden et al.,
1998a).
8 Second, to assess the impacts of AMF on weed communities, manipulative ®eld experiments
are needed in which some perturbation technique is used to suppress AMF fungi. Applications of
broad-spectrum fungicides have been used for this purpose in other plant communities (see
Gange et al., 1993; Newsham et al., 1995a; Hartnett & Wilson, 1999). Other perturbation
techniques ± e.g. tillage that disrupts the soil mycelial network ± might also be suitable (Johnson
et al., 1997). All available perturbation techniques, including fungicides (Pedersen & Sylvia,
1997) and soil fumigation, have multiple agro-ecological e€ects and require careful
interpretation. Methodological improvements are needed to improve our ability to resolve
e€ects on AMF from other e€ects of perturbation. Ideally, a series of studies should be
conducted on weed communities that provide model systems in several di€erent cropping
systems.
Third, if direct evidence con®rms the importance of AMF e€ects on weeds in conservation
tillage systems, then pertinent questions will arise about the community and evolutionary
ecology of weed:AMF interactions. Recent work suggests that diversi®ed AMF communities
have the strongest e€ects on plant communities (Van Der Heijden et al., 1998b; Klironomos,
1999). Studies are needed to determine if this is true of AMF:weed interactions. If so, then a
process of community assembly will be required to develop diverse AMF communities from the
depauperate communities that are apparently present in many high-input agro-ecosystems (Ellis
et al., 1992; Helgason et al., 1998). Important issues may include the temporal dynamics of AMF
diversity and e€ects on community assembly of environmental factors, disturbance events, and
landscape-level factors, such as availability of AMF propagules to colonize ®elds.
Development of AMF communities that bene®cially a€ect weed communities may involve
evolutionary change in AMF or weed species. Relevant evolutionary changes may include
increased capacity for mutualism by plant or fungus and adaptation to edaphic and disturbance
factors. Conversely, cropping systems that include factors that are inimical to the AMF:plant
mutualism, such as situations with high synthetic fertility inputs, appear to select for AMF species
or genotypes that provide substantially reduced bene®ts to crops (Johnson, 1993; Johnson et al.,
1997; Scullion et al., 1998; Feldmann & Boyle, 1999). It is conceivable that antagonistic behaviour

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 Mycorrhizal fungi and weed management 405

towards non-host weeds, or other AMF behaviours that a€ect the agro-ecological functioning of
weed communities, might also be degraded by whatever processes of selection occur in these
cropping systems. As noted above, it is clear that abundant genetic variation a€ecting AMF:plant
interactions is available for evolutionary mechanisms to act upon. Molecular methods for
characterizing AMF variation (e.g. Helgason et al., 1998) are likely to be indispensable to
resolving this variation and characterizing the evolutionary processes that act upon it.
Lastly, many events in agricultural ecosystems that are harmful to AMF can be regarded as
disturbances to AMF communities. Events that may have such an e€ect include crop harvest,
grazing, tillage, rotation to non-host crops, application of biocides, large nutrient inputs,
seasonal extremes of environmental factors, and fallow periods. In several plant communities,
there are indications of mechanisms that serve to maintain AMF communities in settings where
frequent or strong disturbance occurs (Perry et al., 1990). Among these are the so-called
`biological legacies' identi®ed by Perry (1995): structures that provide protection for AMF from
harmful disturbances. For example, in forest systems, large fallen trees appear to provide
physical protection for AMF that are essential to forest regeneration after extensive logging or
®re. Analogous provisions may be needed to maintain e€ective AMF communities in the
disturbance regime of an agro-ecosystem. For example, `zone' tillage, in which tillage is con®ned
to 20±30-cm bands in which crop seeds are sown, may serve to preserve AMF mycelial networks.
Host weeds and self-sowing cover crops may also function as biological legacies in cropping
systems (Perez-Moreno & Ferrera-Cerrato, 1997; Feldmann & Boyle, 1999; Fontenla et al., 1999;
Kabir & Koide, 2000).

Conclusions
In our view, there are two fundamental goals of weed management. The ®rst goal is e€ective
control of weed species that cause major yield losses or other serious problems. The second goal
is to maximize the agro-ecological bene®ts provided by the weed community of an agro-
ecosystem. In some cases, these goals may con¯ict, requiring a careful weighing of costs and
bene®ts of weeds present in a given cropping system. In recent decades, weed control e€orts have
focused on the ®rst goal, perhaps in support of a predominant management objective of high
crop yield. Now, the range of management objectives in agronomy is broadening. Increasing the
eciency of input use, maintaining soil and water resources, and reducing environmental impacts
of farming are global imperatives. In response, management actions have shifted in pursuit of
these goals, in addition to that of high yield. For example, farmers are seeking to enhance levels
of soil quality and bene®cial biodiversity in agro-ecosystems, and to reduce levels of o€-farm
movement of soil sediment and agrochemicals. Present evidence permits the hypotheses that
certain weed species can play bene®cial roles by helping to achieve these objectives, and that
AMF:weed interactions may be critically important to realizing these bene®cial roles of weeds.
We recommend an expanded research e€ort to test these hypotheses. Through this e€ort, weed
science will help to answer a fundamentally important scienti®c question: how can biological
diversity be used to increase the productivity and sustainability of farming (CAST, 1999)?

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