Structure and Function in Agroecosystem Design and Management - Chapter 7 doc

CHAPTER 7
Agroecology of Arbuscular
Mycorrhizal Activity
John C. Zak and Bobbie McMichael
CONTENTS
Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145
Factors Impacting Root Growth and AM Symbiosis. . . . . . . . . . . . . . . . . . . 146
Soil Temperature. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
Soil Moisture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147
Nutrient Conditions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 148
Impacts of Management Practices . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149
Tillage. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149
Crop Rotation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 151
Inoculum Dynamics. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152
Herbicide and Pesticide Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 154
Varietal Responses and Breeding Programs . . . . . . . . . . . . . . . . . . . 156
Role of AM Fungi in Soil Stability . . . . . . . . . . . . . . . . . . . . . . . . . . . . 156
Is Management of AM Fungi Practical? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161
INTRODUCTION
Arbuscular mycorrhizal (AM) fungi are recognized as important compo-
nents of agricultural systems as a consequence of their roles in plant mineral
nutrition, root disease dynamics, and soil fertility. While it is generally agreed
that AM fungi are a necessary component of agricultural ecosystems, there is
only limited understanding as to how to integrate and maintain efficient AM
fungi within an annual cropping system. Moreover, our understanding of the
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146 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT

dynamics of AM fungi within an agricultural context applies only to several
types of cropping systems under a limited number of climatic conditions.
Based on the information that has been collected over the last decade, the
importance of AM fungi in various cropping systems is being taken more
seriously, particularly as production of some crops moves toward low-input
sustainable systems. The importance of AM fungi seems to be more crucial
for these low input systems than in the traditional high input production sys-
tems, where breeding has selected for genotypes that respond to high fertil-
izer and water inputs. However, as the cost of chemical inputs and irrigation
continues to increase and as researchers assess the sustainability of tradi-
tional farming practices, the benefits of AM fungi in an overall crop manage-
ment plan become economically important.
There have been increased efforts over the last decade to understand the
interactions among abiotic and biotic factors associated with agricultural sys-
tems and to develop management options that can be used to incorporate
AM fungi into annual cropping systems. The studies detailed in this chapter
point out how much has been learned concerning the impacts of farming
practices on AM dynamics. These same investigations also articulate our lim-
itations towards integrating AM fungi within a long-term soil management
program that maintains crop yields.
Our goal in this chapter is to examine those aspects of annual production
systems that influence AM dynamics. We state at the outset that our work
with AM colonization of cotton in a semi-arid environment does bias some-
what the topics we have chosen to examine concerning the ecology of AM
fungi in agricultural systems. However, given that arid and semi-arid lands
constitute about 40% of the planet’s surface, and that the majority of world-
wide cotton production occurs within this climatic zone, we believe that
there is the need to expand the discussion of mycorrhizae in agriculture
beyond what has been previously discussed for mesic regions.
FACTORS IMPACTING ROOT GROWTH AND AM SYMBIOSIS

Soil Temperature
The influence of soil temperature on root growth has been documented
for a number of species (e.g., Cooper, 1973). There is an optimum tempera-
ture for maximum root development for all plant species with the general
pattern of root growth increasing up to the optimum and then decreasing at
higher temperatures. For example, the optimum temperature for root growth
in cotton plants is between 28 and 35°C (Pearson et al., 1970) while the opti-
mum temperature for forage legumes is significantly lower (Brar et al., 1991).
Abbas Al-Ani and Hay (1983) showed that root extension rates increased for
each 10°C rise in temperature. However, when soil temperatures deviate sig-
nificantly from optimum, root branching (Brouwer and Hoagland, 1964 ) and
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AGROECOLOGY OF ARBUSCULAR-MYCORRHIZAL ACTIVITY 147
water uptake (Nielsen, 1974) can be reduced. Thus, strategies that would
enhance root development may also improve AM colonization.
Research on impact of soil temperature on AM colonization is limited.
Addy et al. (1997) demonstrated that some extraradical hyphae remain alive
and are capable of infecting following soil freezing. Working with blocks of
field soil, Addy et al. (1998) showed that colonization of AM fungi was
greater in soil that was cooled slowly, allowing for apparent acclimation of
the AM fungi. The exact mechanism for the acclimation and increase in freez-
ing tolerance was not determined. In general, higher temperatures generally
result in greater colonization and increased sporulation (Daniels-Hetrick,
1984). Schenck and Schroder (1974) observed that maximum AM develop-
ment in soybean occurred near 30°C. In contrast, Forbes et al. (1996) showed
that in Plantago the highest level of colonization occurred in roots grown at
15°C with the lowest at 27°C. Menge (1984) indicated that AM colonization is
generally inhibited at soil temperatures lower than 15°C. Ferguson and
Woodhead (1982) showed that periods of cold stress followed by high soil
temperatures increased colonization and sporulation. In recent studies under

controlled conditions, McMichael and Zak (unpublished data) showed that
AM colonization of cotton was higher when plants were grown at 28°C than
at 18°C soil temperature.
Managing soil temperature for improved root growth and AM coloniza-
tion is very difficult, particularly on a large scale. Plastic mulches have been
utilized in some crops, for example, to change soil temperature characteris-
tics for improving plant performance (e.g., Ham et al., 1993; Mbagwu, 1991).
Wien et al. (1993) also used mulches to improve field performance of toma-
toes. Burke and Upchurch (personal communication) used different field
row spacings to adjust crop canopy closure to change soil temperatures and
growth of cotton. However the impacts of various field manipulations
to control soil temperatures on AM colonization have not been investigated.
Another approach to field manipulations of temperature would be to
alter root growth characteristics of plants for improved root development
and AM colonization over a wide range of soil temperatures. McMichael
(unpublished data) has shown genetic variability in the temperature
response of a number of cotton genotypes. In a preliminary study, Zak and
McMichael (2000) found that several lines of cotton that differed in cold tol-
erance when soil temperatures were kept at 18°C had lower colonization than
cotton lines that were rated as highly cold tolerant. The mechanisms for these
effects have not been determined but might reflect differences in root growth
and root densities among the cotton genotypes.
Soil Moisture
Changes in soil moisture can have a direct influence on the growth of
plant root systems and subsequent AM colonization levels. In addition, root-
ing depth and density may increase in a drying soil (Taylor, 1983), while root
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148 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
elongation rates may significantly decrease (Klepper, et al., 1973), affecting
colonization patterns. Zak et al. (1998) indicated that a decrease in soil mois-

ture appeared to impact the extent of mycorrhizal colonization of cotton
plants only during the later stages of growth under dry-land conditions in
west Texas. Ryan and Ash (1996) showed that the decline in AM colonization
in wheat in southern New South Wales was due to a reduction in AM inocu-
lum as a result of severe drought the previous year, rather than a direct impact
on colonization levels. Cade-Menun et al. (1991) reported that for winter
wheat growing in British Columbia, Canada, differences in AM colonization
levels among winter-wheat fields could have resulted from differences in soil
moisture levels with wet conditions inhibiting AM colonization. Soil moisture
may impact colonization levels by decreasing spore germination (e.g., Silva
and Schenck, 1983) and altering spore abundance (Anderson et al., 1984).
The alteration of soil moisture characteristics for improved root develop-
ment is less difficult to accomplish on a relatively large scale than genetically
altering the root pattern of the crop. Research to study the direct interactions
between environmental effects on root development and AM colonization,
however, is lacking. Sylvia and Williams (1992), in their review of the impact
of environmental stress on AM activity, indicated that stresses that influence
plant growth also influence AM colonization.
Nutrient Conditions
The nutrient status of soil in agroecosystems is modified through fertil-
izer applications to enhance production. These fertilizer applications usu-
ally have significant negative effects on AM colonization levels and seasonal
patterns as the N and P status of the soil increases within a growing season
and between years (e.g., Daniels-Hetrick, 1984; Menge, 1984). In addition to
the direct negative impacts of fertilizer application, Johnson and Pfleger
(1992) suggest that an indirect effect of fertilizer application is to alter AM
fungal species occurrences. Moreover, populations of AM fungi may be
adapted to specific fertility levels for a particular crop and region resulting in
AM fungi that are adapted to a specific level of nutrients responding differ-
ently to altered fertilization regimes when crops are rotated through a spe-

cific field.
In designing fertilizer application rates that not only optimize plant
production but that enhance AM colonization and maintain more effective
AM species, Johnson and Pfleger (1992) indicated that the ratio of nutrients
is important with a balanced fertilizer providing improved AM coloniza-
tion. Menge (1984) also reported that high levels of micronutrients, such as
manganese and zinc, can also reduce colonization. Therefore, in the manage-
ment of agricultural soils, maintenance of the proper nutrient balance
appears to be important for optimum performance of plant-mycorrhizal
associations.
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AGROECOLOGY OF ARBUSCULAR-MYCORRHIZAL ACTIVITY 149
IMPACTS OF MANAGEMENT PRACTICES
Tillage
For many agricultural systems, tillage is a necessary management prac-
tice that is used to reduce weed competition, reduce soil compaction, enhance
water infiltration, and reduce wind erosion of sandy-loam soils. Based on
both greenhouse and field investigations, the general conclusion of numer-
ous studies is that soil disturbances from tillage result in decreased AM colo-
nization, a decline in AM spore numbers, a change in AM species, and a
subsequent decline in mycorrhizal infectivity, particularly if fields are not
replanted that year. The causal relationships between tillage and reduced AM
colonization and effectiveness center on the impact of this management prac-
tice on the disruption, fragmentation, and destruction of the extensive net-
work of AM extraradical hyphae that develops in soil during the growing
season, and on the decreased viability of AM inoculum types (McGonigle
and Miller, 1996). The disruption of the AM hyphal network can negatively
influence AM-induced enhancement of plant growth (e.g., O’Halloran et al.,
1989; Jasper et al., 1989a, b), reduce tissue P concentrations and shoot dry
weight (e.g., Fairchild and Miller, 1988; Evans and Miller, 1990), and has been

reported to result in the subsequent decline in AM colonization (Evans and
Miller, 1988). In greenhouse pot studies the effects of soil disturbance have
varied with impacts depending upon the length of time between the distur-
bance and planting. Jasper et al. (1989a, b) reported a decline in AM colo-
nization following disturbance, while McGonigle et al. (1990) found no
effects of soil disturbance. In a field study using corn under tillage and a No-
till system, Entry et al. (1996) found that tillage had no impact on coloniza-
tion of corn after 7 years.
Not only can tillage impact AM infectivity and viability, Kabir et al. (1999)
reported a direct decrease in metabolically active hyphae associated with
mycorrhizal corn following soil disturbance if soils were subsequently left fal-
low for one to three months (Figure 7.1). In their greenhouse study, the
destruction of the AM hyphal network also reduced plant phosphorous con-
tent and shoot dry weights. The decrease in plant P was attributed to the
inability of the fragmented network to explore a sufficient soil volume to
maintain adequate plant P levels for optimum plant growth. The maintenance
of a continuous AM hyphal network is crucial to supplying the host with suf-
ficient P to meet plant demands and support high yields (Kabir et al., 1999).
For cropping systems in temperate regions there can be an interval of up
to five months before the next crop is planted. During this period of time, AM
inoculum can either remain intact or be reduced, depending upon soil prepa-
ration needs, the previous impacts of tillage practices on the maintenance of
the AM hyphal network, and the interactions of agricultural practices with
climatic conditions. Since tillage practices also affect root distributions, it is
reasonable to propose that tillage will also affect the subsequent distribution
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150 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
80
100
60

40
20
0
0
30 60 90
Fallow Period (Days)
Hyphal Lengths (cm/g)
Parameter and Treatment
Total - Disturbed
Total - Undisturbed
Metabolically Active - Disturbed
Metabolically Active - Undisturbed
Figure 7.1 The interactive effects of disturbance (mixing) and fallow time on lengths
of total and metabolically active AM hyphae associated with Zea mays L.
Values are means Ϯ S.E. Data from Kabir, Z., O’Halloram, I. P., and
Hamel, C., Soil Biol. Biochem., 307–314, 1999.
of AM propagules that have survived from the previous crop. Comparing
conventional tillage and No-till systems, Smith (1978) found that AM spores
were most abundant in the top 10 cm of soil in the No-till system (drilled
wheat) when compared to conventional tillage wheat where the majority of
the spores occurred in soil below 10 cm. If the density of the AM inoculum
is crucial for the successful colonization of annual crop seedlings such as cot-
ton (Zak et al., 1998), the vertical distribution of AM inoculum becomes an
issue that should be considered if one is to manage effectively AM fungi.
Tillage may also negatively affect mycorrhizal dynamics by influencing
AM fungal species composition. Johnson and Pfleger (1992) speculated that
through repeated disruption of the mycorrhizal network and the severing of
hyphae from roots, tillage would be a strong selective influence in determin-
ing AM species composition. Species richness of AM fungi has been shown
to decrease when land is first brought into cultivation (Schenck et al., 1989)

and as the intensity of the agricultural inputs increases (e.g., Sieverding,
1990). Therefore, it is reasonable to speculate that different types of soil man-
agement practices (tillage, minimal tillage, and No-till systems) should affect
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AGROECOLOGY OF ARBUSCULAR-MYCORRHIZAL ACTIVITY 151
AM fungal species composition to different degrees. However, there have
been few long-term evaluations of the effects of different degrees of soil dis-
turbance on AM fungal species richness and species composition. Certain
species of AM fungi (e.g., Glomus mosseae and Glomus aggregatum ) are fre-
quently abundant in highly managed agricultural systems (Schenck et al.,
1989), suggesting that these species may be adapted to highly disturbed sys-
tems. Johnson and Pfleger (1992) and Kurle and Pfleger (1994) previously
pointed out the deficiencies in our understanding of the impacts of tillage on
AM dynamics in agricultural systems, specifically with respect to changes in
species composition.
In addition to the disruption of the AM mycelial network, tillage also
negatively affects mycorrhizal benefits to crop plants by increasing soil com-
paction and through increased decomposition of incorporated plant
residues, which includes mycorrhizal root fragments. Intensive tillage exac-
erbates soil compaction, requiring annual deep plowing to break up this
compacted layer (Soane, 1990), further disrupting the AM fungal network
(Entry et al., 1996) and hastening root decomposition.
Crop Rotation
When compared to undisturbed systems, the species richness of AM fun-
gal assemblages in agroecosystems is lower, sometimes substantially,
depending upon the amount of human input into the system (e.g., Siqueira et
al., 1989, and Sieverding, 1990). Most annual cropping systems are managed
as monocultures that are either rotated through a specific cropping sequence
(e.g., corn—soybean) or that are continuously planted as a single crop some-
times for years. The continuous cropping approach, in conjunction with the

use of a single plant species, and cultural practices that are part of the man-
agement system (irrigation, tillage, fertilizer and pesticide application) all
interact to select for a specific ensemble of AM species that can tolerate and
proliferate under the conditions that are dominant in the production system.
The combination of type of annual crop plant and the length of cultiva-
tion exert a strong influence on the species of AM fungi that are found in a
particular field or production system. Schenck and Kinloch (1980) were one
of the first to document that, although AM fungi were considered generalists
with regard to host species, there were differences in the species composi-
tions of AM fungal ensembles among six different crops planted in the same
soil type and within the same climatic region. Johnson et al. (1992) showed
that three species of Glomus (aggregatum, leptotichum, and occultum) were
dominant in a corn cropping system, while in a soybean cropping system in
the same region only spores of Glomus microcarpum predominated.
Not only can annual crops select certain species of AM fungi from the
species pool that would exist for a given region, the species that can prolifer-
ate under monocultural conditions have been shown not to be the most
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152 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
efficient mutualists. In their work on understanding rotation effects on yield
decline and the involvement of AM fungi, Johnson et al. (1992) proposed that
continuous cropping selects for rapidly growing AM species. As these ineffi-
cient AM fungal species predominate in the soil, crop vigor begins to decline.
Rotations that use either facultatively mycorrhizal crops or species that
do not form arbuscular mycorrhizae, such as rapeseed, sugar beet, or buck-
wheat, may decrease AM inoculum for a succeeding, highly mycorrhizal-
dependent crop to the same degree as fallowing (Thompson, 1991). From a
management perspective, crop rotation decisions should consider the ability
of the current crop to maintain inoculum of effective fungi at high densities
as well as the mycorrhizal dependency of the succeeding crop type

(Thompson, 1994).
Inoculum Dynamics
AM propagules include spores, hyphal fragments, and dead roots that
contain hyphae and vesicules. The survival and abundance of these propag-
ules in an annual cropping system are influenced by a suite of abiotic factors
and management considerations that includes crop rotations, tillage, water-
ing schedules, fertilizer type and application rates, and pesticide use. These
factors either negatively impact AM inoculum production or decrease viabil-
ity with the successive crop suffering the greatest adverse affect. While AM
fungal spores can be found in most agricultural systems, it is unclear to what
extent AM spores maintain colonization levels of annual crops from season
to season (Abbott and Gazey, 1994). In semiarid regions, where spore pro-
duction is generally low (Stutz and Morton, 1996), mycorrhizal root frag-
ments can be critical sources of inoculum for the succeeding crop (Friese and
Allen, 1991). Any management practice or change in climate that accelerates
decomposition of colonized root fragments can result in a decline in subse-
quent AM colonization levels.
Changes in AM fungal species and spore densities in annual cropping
systems have been reported to occur in response to tillage practices. In a No-
till corn and soybean system, Glomus occultum predominated while in a con-
ventional tillage system, spores of Glomus etunicatum were the most
numerous (Douds et al., 1995). The negative effects of tillage on AM fungal
spore production and densities have been primarily observed to occur in the
top 5 cm of soil where the disturbance effects are the most severe. Deep plow-
ing to more than 15 cm will reduce colonization of roots by AM fungi, thereby
reducing inoculum densities (Kabir et al., 1999) which in turn may result in a
decrease in seedling establishment during the following year.
Depending upon the crop, climate, and rainfall patterns for a particular
region, annual cropping systems are either followed by the same cash crop,
rotated with a second cash crop, planted in a winter cover crop, or left fallow.

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AGROECOLOGY OF ARBUSCULAR-MYCORRHIZAL ACTIVITY 153
The decisions that are made at this management level can have profound
negative and positive effects on the production and survival of AM inocu-
lum. The types of propagules that are present in a production system and
their rates of survival are crucial pieces of information for subsequently max-
imizing colonization of developing seedlings of annual crops under conven-
tional cropping systems. Since AM fungi differ in their ability to produce
spores (Abbott and Gazey, 1994), the importance of the AM hyphal network
in the soil and the survivability of AM hyphae contained within living and
dead roots become critical if one is to develop management strategies of AM
fungi in an annual cropping system. Walker and Smith (1984) showed that
the rate of AM colonization was determined primarily by the density of AM
propagules in the soil. In the southern parts of Australia, AM fungi appear to
survive as hyphal networks depending on the degree of disturbance (e.g.,
Jasper et al., 1987), hyphae in dried root fragments (Tommerup and Abbott,
1981), and as spores (e.g., McGee et al., 1997). The form of inoculum that best
survives from year to year is highly dependent upon the degree of soil dis-
turbance.
In arid and semiarid regions, fallowing is a necessary component of a
water management plan. The length of time that a suitable AM host is absent
from a field can result in a significant decline in AM propagules and limited
colonization of the subsequent crop. Long-fallow disorder has now been
attributed to declines in AM propagule densities due to the extended periods
without a suitable host (Harinikumar and Bagyaraj, 1988; Thompson, 1987).
Johnson and Pfleger (1992) emphasized that crops that generate large quan-
tities of AM propagules are more effective in alleviating long-fallow disorder
in subsequent crops than do crops that are only facultatively mycorrhizal.
Using a combination of vital staining of AM fungal hyphae and AM fungal
spores, McGee et al. (1997) determined that, for cotton production systems

in southern Australia on a cracking, heavy clay soil, the viability of
AM fungal spores is low and declines during the growing season (Figure
7.2). Furthermore, the infectivity of mycorrhizal propagules appeared to
decline over time (32 wks) for dry soil in the absence of any direct impact on
AM propagules. In addition, when fields were left fallow, any rainfall that
occurred during the fallow resulted in germination of nondormant pro-
pagules further exasperating the decline in AM inoculum (Pattinson and
McGee, 1997). Paradoxically, McGee et al. (1997) reported that while long-
fallow disorder should be a major problem in cotton production systems in
southern Australia, the phenomenon is uncommon. They suggest that either
current methods used to quantify fungal survival do not reflect the ability to
initiate colonization in the field, or that the decline, while substantial during
fallowing, does not reduce the level of AM inoculum below a threshold
needed for colonization of cotton in southern Australia.
While fallow alone may or may not have a negative impact on subse-
quent mycorrhizal colonization, fallowing is usually followed by tillage.
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154 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
Figure 7.2 Changes in viability of AM fungal spores in stored field soils compared
with freshly collected samples. Soil was obtained from a paddock that
had never been cultivated and was used for grazing. Data from McGee,
P. A., Pattinson, G. S., Heath, R. A., Newman, C. A., and Allen, S. J., New
Phytol., 773–780, 1997.
Kabir et al. (1999) were the first to show that when these two practices were
combined, there were substantial declines in AM hyphal infectivity and
metabolic activity leading to subsequent declines in crop growth and nutri-
ent content.
Herbicide and Pesticide Effects
Many annual crops require several applications of pesticides during the
growing season to maintain crop vigor and enhance yield quality. In addi-

tion, herbicide applications are routinely made either during the growing
season or during the fallow periods to ensure effective weed control. For cot-
ton production systems on the Southern High Plains of west Texas, for exam-
ple, cotton is treated with a variety of biocides during the growing season
(Table 7.1) to control weeds and disease organisms. The recent introduction
of Round-Up Ready Cotton to cotton production systems ensures that
Round-Up herbicide will be applied to cotton fields for weed control when
the genetically altered plant is used. The long-term effects of these and other
genetic modifications of cotton (Table 7.1) on mycorrhizal development have
not been examined in detail.
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Table 7.1 Pesticides Applied to Conventional Cotton Cropping Systems on
the Southern High Plains, Texas
Pesticide Target Time of Application
Round-up Weeds Preplanting and early seedling stages
Treflan Weeds Pre-emergent
Prowl Weeds Pre-emergent
Caporal Weeds Pre-emergent
Batan Fungal pathogens Seed treament
Dual Fungal pathogens Seed treatment
Temik Insects Pre-emergent
Aldocarb Thrip Seedling
The specific impacts of various fungicides, pesticides, and herbicides on
AM colonization and species occurrences have been reviewed and summa-
rized in Johnson and Pfleger (1992), Kurle and Pfleger (1994), and Thompson
(1994). Our understanding of the impacts of these compounds on AM devel-
opment and fungal survival in annual cropping systems has not changed
much since these reviews were published. As would be expected of the vari-
ous types of biocides, fungicides have the greatest impact on mycorrhizal

survival and subsequent colonization. However, application rates, time of
application, and method of application (foliar sprays versus soil drench) all
in combination determine the final effect of the fungicide on AM fungi.
Moreover, not all application rates are detrimental to mycorrhizal develop-
ment (Johnson and Pfleger, 1992; Kurle and Pfleger, 1994). However, devel-
oping general conclusions of the impacts of fungicides on AM fungi across
annual cropping systems, because of the interactive effects of soil influences,
species of AM fungi, and indirect effects of the fungicides on soil organisms
antagonistic to AM fungi (Fitter and Garbaye, 1994), is impractical. In addi-
tion, the effects of fungicides vary if one is examining colonization levels ver-
sus inoculum production.
The consensus concerning effects of herbicides is that when these plant
control agents are applied at manufacturer-recommended rates under
field conditions, the impacts on AM colonization levels have not been signif-
icant. However, greenhouse studies have shown detrimental impacts of her-
bicides on AM colonization levels (e.g., Nemec and Tucker, 1983). AM
inoculum potentials may be reduced when residual effects of pre-emergent
herbicides affect root growth during the growing season, as is sometimes
observed in cotton in west Texas.
Most insecticides and nematicides have been reported not to have any
impact on AM colonization. When fungivorous nematodes are reduced,
increases in AM colonization have been reported (e.g., Sreenivasa and
Bagyaraj, 1989). However, as mentioned by Kurle and Pfleger (1994), there is
still too little information available to make generalizations.
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156 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
Varietal Responses and Breeding Programs
To date, there have been no breeding programs established whose spe-
cific aims were to increase AM colonization levels of annual crops. Several
studies have reported that various cultivars of pearl millet, wheat, soybean,

and corn differ in the amount of root colonized by AM fungi (Hetrick et al.,
1992; Hetrick et al., 1993; Hetrick et al., 1995; Thompson, 1994) and that these
differences in AM colonization levels among cultivars is a heritable trait
(Krishna et al., 1985; Kesava Rao et al., 1990). When Manske (1990) grew
22-high yield spring wheat varieties and land races under low P conditions,
the highly bred plants did not respond as positively (yield) to the addition of
AM fungi; some even exhibited a negative response when compared to the
land races. As emphasized by Kurle and Pfleger (1994), the results of Manske
(1990) support the hypothesis that current crop breeding programs may be
inadvertently selecting for crop genotypes that are responsive to chemical fer-
tilizers while becoming unresponsive to AM fungi. Toth et al. (1990) showed
that inbred lines of corn with high resistance to a number of fungal diseases
also were not well colonized by AM fungi, indicating that by selecting for
high levels of fungal pathogen resistance these same mechanisms that convey
fungal pathogen resistance may also prevent AM colonization.
Plant species as well as cultivars within species also differ widely in their
mycorrhizal dependency (Planchette et al., 1983; Graham et al., 1997). These
differences in mycorrhizal dependency among genotypes can account for
some of the range in crop response to mycorrhizae and nutrient levels that
have been reported (e.g., Khalil et al., 1999). The management implications of
these results are that in agricultural systems where AM inoculum is low or
has been reduced through tillage practices or fallowing, it may be prudent to
select for high yielding cultivars of low mycorrhizal dependency, at least dur-
ing the early phase of a crop rotation (Thompson, 1994). Likewise, in situa-
tions were AM inoculum is high, managers should select plant genotypes
that can benefit from mycorrhizal colonization.
Ultimately, the merits of either breeding for increased mycorrhizal
dependency or using current genotypes with low AM dependency will be
based upon the cost of phosphate fertilizer, the effects of management prac-
tices on AM inoculum levels, and the benefits in yields that are consistent and

predictable. Moreover, work is ongoing to modify numerous characteristics
of cotton through molecular techniques (Table 7.2). The long-term effects of
these genetic manipulations on AM development have not been examined in
detail, if at all.
Role of AM Fungi in Soil Stability
Much of what has been identified in this chapter as negatively impacting
AM colonization dynamics and inoculum survival has also been mentioned
as controlling the levels of soil organic matter, the amount of microbial
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AGROECOLOGY OF ARBUSCULAR-MYCORRHIZAL ACTIVITY 157
Table 7.2 Current Efforts Being Directed Toward Breeding and Genetic
Manipulation of Cotton That May Impact Arbuscular Mycorrhizae
Colonization of Cotton Growing on the Southern High Plains,
Texas.
Characteristic Projected outcome
Early maturation Increased yields and decreased water use
Inclusion of
Bacillus thuringiensis Increased insect resistance
toxin gene
Herbicide resistance Direct application of herbicide for weed control
Increased cold tolerance Increased growth and yield
Increased drought tolerance Increased stand establishment and yield
Decreased seed gossypol content Increased usage as animal feed supplement
Increased seed size Increased usage as animal feed supplement
Oil quality Oil quality modification
biomass, and the occurrence and maintenance of water-stable soil aggregates
in agroecosystems (Parton et al., 1987). A series of papers described the con-
ceptual model of aggregate formation (Tisdall and Oades, 1982; Oades and
Waters, 1991) in which the physical entanglement by roots and mycorrhizal
hyphae was a major mechanism in the binding of microaggregates into

macroaggregates. As pointed out by Miller and Jastrow (1990), the model
does not take into account the varying degrees of association between AM
fungi and plant roots of differing morphology. Thus, plant species that
exhibit different root morphologies, by affecting the amount of mycorrhizal
colonization and associated extraradical mycelium, can contribute differ-
ently to aggregate formation. Using path analysis, Miller and Jastrow (1990)
were able to tease apart the interactions between roots and arbuscular myc-
orrhizae to show that AM fungi influence aggregate formation directly
through the amounts of extraradical mycelium produced.
Although the amount of soil carbon is often considered important to
aggregate development, Jastrow et al. (1998) reported that AM hyphae were
the driving factor influencing macroaggregate stabilization in a restored
prairie system. The linkage between aggregate stability and AM fungi was
established when Wright et al. (1996) and Wright and Upadhyaya (1998) re-
ported that (1) AM fungi produce an immunoreactive glycoprotein, glomalin,
and that (2) this glycoprotein is abundant in soils. The glycoprotein is recalci-
trant and has hydrophobic characteristics that indicate that this molecule is
important to aggregate stabilization (Wright and Upadhyaya, 1998). Impor-
tantly, Wright et al. (1996) found that all AM fungi tested produced glomalin.
In a recent survey of aggregate stability and glomalin from 37 sites across the
U.S. and from Scotland subjected to various land-use practices and cropping
sequences, Wright and Upadhyaya (1998) found that aggregate stability was
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158 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
linearly and significantly correlated with two components of total soil glom-
alin. Therefore, any process that disrupts AM hyphal networks or causes
degradation of glomalin will lead to decreased soil aggregate stability.
Jastrow (1987) had shown that the effects of soil disturbance on aggregate sta-
bility in a restored prairie ecosystem would be long term. The cross site com-
parison by Wright and Upadhyaya (1998) also determined that iron

availability could have a significant impact on the production of glomalin,
but the mechanism for this effect is unclear. Calcareous soils from west
Texas, which were deficient in iron, had the lowest glomalin and stability
values of all samples tested.
IS MANAGEMENT OF AM FUNGI PRACTICAL?
Within the last decade numerous book chapters and reviews have exam-
ined the potential for managing arbuscular mycorrhizae in agricultural sys-
tems (e.g., Bethlenfalvay, 1992; Johnson and Pfleger, 1992; Bethlenfalvay and
Schuepp, 1994; Safir, 1994; Robson et al., 1994; Hamel, 1996). The consensus of
these discussions was that the complexity of the plant-AM fungus interac-
tions prevents direct management of selected taxa at this time. The lack of
basic ecological information about the distribution of AM fungi under vari-
ous production systems, the lack of information on temporal patterns with
respect to management practices, the difficulty with species identifications
and obtaining sufficient and appropriate spores for identification, the diffi-
culty in manipulating these fungi without greatly modifying the soil envi-
ronment, and the inability to culture AM fungi substantially impede progress
toward establishing all but the basic approaches for the incorporation of
AM fungi within an annual cropping system. To be sure, as has been stated
in this chapter and elsewhere, we have sufficient evidence to predict what
aspects of annual cropping systems will have negative impacts on AM fungi.
What is lacking is an understanding, in those cases other than direct distur-
bance effects, of the mechanisms that lead to changes in species composition,
colonization rates, and benefits of the AM symbiosis to the crop. Without
understanding the mechanisms that influence AM populations and the
degree of genetic variability that exists within AM assemblages, it becomes
difficult if not impossible to develop strategies that can be used to maintain
or shift the species composition of the endemic AM fungi to the desirable
species, if they are even known for a particular region. For most production
systems, large-scale inoculum additions are not practical and where tried

have provided mixed results.
Most studies that have examined the roles of AM fungi in annual crop-
ping systems have made the assumption that by enhancing P uptake, AM col-
onization will increase plant growth and subsequent yields. Zak et al. (1998)
reported that early and rapid colonization of cotton on the Southern High
Plains of the U.S. was essential for growth and survival if seedlings were
subjected to cool and wet soil conditions. However, Zak and McMichael
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AGROECOLOGY OF ARBUSCULAR-MYCORRHIZAL ACTIVITY 159
(unpublished data) have found that when environmental conditions were
not stressful (cool and wet) during the early part of the growing season for
cotton, they were unable to detect yield differences in cotton fields with high
levels of AM colonization as compared to cotton with low levels of AM colo-
nization. Under nonstressful conditions, there appears to be little benefit to
cotton becoming mycorrhizal. Unfortunately, the farmer cannot predict from
year to year when soil conditions will become less than optimum for the
growth and maximal yield development of a crop. Therefore, the mainte-
nance of crop-specific AM inoculum densities to ensure rapid colonization
during the seedling stage, and the maintenance of AM fungal species that are
efficient in nutrient uptake and that enhance seedling survival and growth,
are potential yield costs that must be incurred.
The frustration with this simple statement about the roles and benefits of
AM fungi in annual cropping systems is that (1) crops differ in their mycor-
rhizal dependency, (2) AM fungi that rapidly and aggressively colonize roots
may not be the most efficient symbiont, and (3) tillage and fertilization prac-
tices may select for AM fungi that are more parasitic. Graham (1999) has pro-
posed that if the annual crop is one that has a low mycorrhizal dependency,
it might be advantageous actually to reduce the early rates of AM coloniza-
tion so as to reduce initial carbon costs. As long as phosphorous demand can
be met with fertilizer applications, yields will be unaffected by the lack or low

levels of AM colonization.
The challenge in determining how best to incorporate AM fungi in an
annual cropping system will hinge on our understanding of the abiotic and
biotic conditions that make AM fungi a necessity for plant growth and for
maximizing yields in annual crops. From our experiences in annual cropping
systems with cotton, weather has the controlling effect on whether a positive
response to AM colonization is detected in cotton on the Southern High Plains
of the U.S. In those years when growing conditions are nominal the lack of
AM fungi due to tillage or other manipulations discussed above may not
result in significant yield reductions if early season plant loss is minimal.
However, deleterious weather events are often random and unpredictable,
thus necessitating the continued occurrence of beneficial AM fungi at levels
that ensure sufficient root colonization of seedlings before stressful condi-
tions occur.
The value of AM fungi to annual cropping systems will depend upon the
complex interactions that are likely to occur in response to plant genotype,
soil nutrient status, climatic conditions, historical events that have impacted
AM fungal species pools, management practices, the AM dependency of the
crop, climate, and, in some cases, political and economic decisions that affect
crop rotations and fertilizer use. While this complexity seems daunting, the
understanding of abiotic and biotic interactions that have been observed to
influence AM colonization in annual cropping systems suggests that multi-
ple approaches can be developed for managing or incorporating AM fungi
within an annual cropping system that are cost effective over the long term.
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160 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
We have found that for cotton production systems in west Texas, cotton
planted into terminated winter wheat (Zak et al., 1998) is one approach that
can be economically used to maintain AM inoculum levels in annual crops
(Figure 7.3). Isobe and Tsuboki (1999) observed an increase in AM coloniza-

tion of kidney bean when the crop was preceded with a winter crop of barley
or broad beans. For those systems in which companion planting is a viable
Terminated Wheat
Conventional Cotton
Corn as Host
Cotton as Host
50
40
30
20
10
0
JF
M
A
M
J
J
AS
ON
D
50
40
30
20
10
0
JF
M
A

M
J
J
AS
O
N
D
% AM Colonization
% AM Colonization
Month (1995)
Figure 7.3 The influence of companion planting of winter wheat on seasonal
dynamics of AM fungi associated with cotton on the Southern High Plains,
Texas using corn (top graph) and cotton (HS-26) as hosts (bottom
graph). Plants were grown in the greenhouse for two weeks and per-
centage AM colonization of each host determined. Values are means
(N ϭ 5) Ϯ S.E. Data from Zak and McMichael, 2000 (in preparation).
920103_CRC20_0904_CH07 1/13/01 10:54 AM Page 160
AGROECOLOGY OF ARBUSCULAR-MYCORRHIZAL ACTIVITY 161
option, studies should be conducted that examine which companion crops
are most effective at maintaining efficient levels of AM inoculum. In regions
where companion planting may not be profitable or may be unlikely due to
temperature or water restrictions, the planting of low-mycorrhizal depen-
dent annual crops may be the most prudent approach.
As the cost of fertilizer continues to increase, the global climate changes,
and water becomes more costly, there will be greater need to begin to reex-
amine our reliance on high input agriculture methods (Swift and Anderson
1993) and to expand upon our understanding of the roles and ecology of AM
fungi in a greater variety of agriculture systems. To incorporate effectively
AM fungi within an annual cropping system, there is still much to discover
concerning the complexities of the interactions among the soil microflora and

fauna of which AM fungi are one component.
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