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

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

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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dynamics of AM fungi within an agricultural context applies only to severaltypes of cropping systems under a limited number of climatic conditions.Based on the information that has been collected over the last decade, theimportance of AM fungi in various cropping systems is being taken moreseriously, particularly as production of some crops moves toward low-inputsustainable systems The importance of AM fungi seems to be more crucialfor 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 irrigationcontinues 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 theinteractions 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 chapterpoint out how much has been learned concerning the impacts of farmingpractices on AM dynamics These same investigations also articulate our lim-itations towards integrating AM fungi within a long-term soil managementprogram that maintains crop yields

Our goal in this chapter is to examine those aspects of annual productionsystems that influence AM dynamics We state at the outset that our workwith AM colonization of cotton in a semi-arid environment does bias some-what the topics we have chosen to examine concerning the ecology of AMfungi in agricultural systems However, given that arid and semi-arid landsconstitute about 40% of the planet’s surface, and that the majority of world-wide cotton production occurs within this climatic zone, we believe thatthere is the need to expand the discussion of mycorrhizae in agriculturebeyond 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 documentedfor a number of species (e.g., Cooper, 1973) There is an optimum tempera-ture for maximum root development for all plant species with the generalpattern of root growth increasing up to the optimum and then decreasing athigher temperatures For example, the optimum temperature for root growth

in cotton plants is between 28 and 35°C (Pearson et al., 1970) while the mum temperature for forage legumes is significantly lower (Brar et al., 1991).Abbas Al-Ani and Hay (1983) showed that root extension rates increased foreach 10°C rise in temperature However, when soil temperatures deviate sig-nificantly from optimum, root branching (Brouwer and Hoagland, 1964 ) and

opti-water uptake (Nielsen, 1974) can be reduced Thus, strategies that wouldenhance 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 aliveand are capable of infecting following soil freezing Working with blocks offield soil, Addy et al (1998) showed that colonization of AM fungi wasgreater in soil that was cooled slowly, allowing for apparent acclimation ofthe AM fungi The exact mechanism for the acclimation and increase in freez-ing tolerance was not determined In general, higher temperatures generallyresult 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 isgenerally inhibited at soil temperatures lower than 15°C Ferguson andWoodhead (1982) showed that periods of cold stress followed by high soiltemperatures increased colonization and sporulation In recent studies undercontrolled 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 tion is very difficult, particularly on a large scale Plastic mulches have beenutilized 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 fieldrow spacings to adjust crop canopy closure to change soil temperatures andgrowth of cotton However the impacts of various field manipulations

coloniza-to control soil temperatures on AM colonization have not been investigated.Another approach to field manipulations of temperature would be toalter root growth characteristics of plants for improved root developmentand AM colonization over a wide range of soil temperatures McMichael(unpublished data) has shown genetic variability in the temperatureresponse of a number of cotton genotypes In a preliminary study, Zak andMcMichael (2000) found that several lines of cotton that differed in cold tol-erance when soil temperatures were kept at 18°C had lower colonization thancotton lines that were rated as highly cold tolerant The mechanisms for theseeffects have not been determined but might reflect differences in root growthand root densities among the cotton genotypes

Soil Moisture

Changes in soil moisture can have a direct influence on the growth ofplant root systems and subsequent AM colonization levels In addition, root-ing depth and density may increase in a drying soil (Taylor, 1983), while root

elongation rates may significantly decrease (Klepper, et al., 1973), affectingcolonization patterns Zak et al (1998) indicated that a decrease in soil mois-ture appeared to impact the extent of mycorrhizal colonization of cottonplants only during the later stages of growth under dry-land conditions inwest 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 lum as a result of severe drought the previous year, rather than a direct impact

inocu-on colinocu-onizatiinocu-on levels Cade-Menun et al (1991) reported that for winterwheat growing in British Columbia, Canada, differences in AM colonizationlevels among winter-wheat fields could have resulted from differences in soilmoisture levels with wet conditions inhibiting AM colonization Soil moisturemay impact colonization levels by decreasing spore germination (e.g., Silvaand 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 geneticallyaltering the root pattern of the crop Research to study the direct interactionsbetween 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 influenceplant growth also influence AM colonization

Nutrient Conditions

The nutrient status of soil in agroecosystems is modified through izer applications to enhance production These fertilizer applications usu-ally have significant negative effects on AM colonization levels and seasonalpatterns as the N and P status of the soil increases within a growing seasonand between years (e.g., Daniels-Hetrick, 1984; Menge, 1984) In addition tothe direct negative impacts of fertilizer application, Johnson and Pfleger(1992) suggest that an indirect effect of fertilizer application is to alter AMfungal species occurrences Moreover, populations of AM fungi may beadapted to specific fertility levels for a particular crop and region resulting in

fertil-AM fungi that are adapted to a specific level of nutrients responding ently to altered fertilization regimes when crops are rotated through a spe-cific field

differ-In designing fertilizer application rates that not only optimize plantproduction 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 tion Menge (1984) also reported that high levels of micronutrients, such asmanganese and zinc, can also reduce colonization Therefore, in the manage-ment of agricultural soils, maintenance of the proper nutrient balanceappears to be important for optimum performance of plant-mycorrhizalassociations

coloniza-IMPACTS OF MANAGEMENT PRACTICES Tillage

For many agricultural systems, tillage is a necessary management tice that is used to reduce weed competition, reduce soil compaction, enhancewater infiltration, and reduce wind erosion of sandy-loam soils Based onboth 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 asubsequent decline in mycorrhizal infectivity, particularly if fields are notreplanted that year The causal relationships between tillage and reduced AMcolonization 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 growingseason, and on the decreased viability of AM inoculum types (McGonigleand Miller, 1996) The disruption of the AM hyphal network can negativelyinfluence AM-induced enhancement of plant growth (e.g., O’Halloran et al.,1989; Jasper et al., 1989a, b), reduce tissue P concentrations and shoot dryweight (e.g., Fairchild and Miller, 1988; Evans and Miller, 1990), and has beenreported to result in the subsequent decline in AM colonization (Evans andMiller, 1988) In greenhouse pot studies the effects of soil disturbance havevaried 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 noeffects 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

prac-Not only can tillage impact AM infectivity and viability, Kabir et al (1999)reported a direct decrease in metabolically active hyphae associated withmycorrhizal corn following soil disturbance if soils were subsequently left fal-low for one to three months (Figure 7.1) In their greenhouse study, thedestruction of the AM hyphal network also reduced plant phosphorous con-tent and shoot dry weights The decrease in plant P was attributed to theinability of the fragmented network to explore a sufficient soil volume tomaintain adequate plant P levels for optimum plant growth The maintenance

of a continuous AM hyphal network is crucial to supplying the host with 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

suf-to five months before the next crop is planted During this period of time, AMinoculum can either remain intact or be reduced, depending upon soil prepa-ration needs, the previous impacts of tillage practices on the maintenance ofthe AM hyphal network, and the interactions of agricultural practices withclimatic conditions Since tillage practices also affect root distributions, it isreasonable to propose that tillage will also affect the subsequent distribution

80 100

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.

Hamel, C., Soil Biol Biochem., 307 –314, 1999.

of AM propagules that have survived from the previous crop Comparingconventional tillage and No-till systems, Smith (1978) found that AM sporeswere most abundant in the top 10 cm of soil in the No-till system (drilledwheat) when compared to conventional tillage wheat where the majority ofthe 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 ton (Zak et al., 1998), the vertical distribution of AM inoculum becomes anissue that should be considered if one is to manage effectively AM fungi.Tillage may also negatively affect mycorrhizal dynamics by influencing

cot-AM fungal species composition Johnson and Pfleger (1992) speculated thatthrough repeated disruption of the mycorrhizal network and the severing ofhyphae 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

AM fungal species composition to different degrees However, there havebeen 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) previouslypointed out the deficiencies in our understanding of the impacts of tillage on

AM dynamics in agricultural systems, specifically with respect to changes inspecies composition

In addition to the disruption of the AM mycelial network, tillage alsonegatively affects mycorrhizal benefits to crop plants by increasing soil com-paction and through increased decomposition of incorporated plantresidues, which includes mycorrhizal root fragments Intensive tillage exac-erbates soil compaction, requiring annual deep plowing to break up thiscompacted 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 gal assemblages in agroecosystems is lower, sometimes substantially,depending upon the amount of human input into the system (e.g., Siqueira etal., 1989, and Sieverding, 1990) Most annual cropping systems are managed

fun-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 theuse of a single plant species, and cultural practices that are part of the man-agement system (irrigation, tillage, fertilizer and pesticide application) allinteract to select for a specific ensemble of AM species that can tolerate andproliferate 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 aparticular field or production system Schenck and Kinloch (1980) were one

of the first to document that, although AM fungi were considered generalistswith regard to host species, there were differences in the species composi-tions of AM fungal ensembles among six different crops planted in the samesoil 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 thespecies 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

efficient mutualists In their work on understanding rotation effects on yielddecline and the involvement of AM fungi, Johnson et al (1992) proposed thatcontinuous 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 wheat, may decrease AM inoculum for a succeeding, highly mycorrhizal-dependent crop to the same degree as fallowing (Thompson, 1991) From amanagement perspective, crop rotation decisions should consider the ability

buck-of the current crop to maintain inoculum buck-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 thatcontain hyphae and vesicules The survival and abundance of these propag-ules in an annual cropping system are influenced by a suite of abiotic factorsand management considerations that includes crop rotations, tillage, water-ing schedules, fertilizer type and application rates, and pesticide use Thesefactors either negatively impact AM inoculum production or decrease viabil-ity with the successive crop suffering the greatest adverse affect While AMfungal spores can be found in most agricultural systems, it is unclear to whatextent AM spores maintain colonization levels of annual crops from season

to season (Abbott and Gazey, 1994) In semiarid regions, where spore duction is generally low (Stutz and Morton, 1996), mycorrhizal root frag-ments can be critical sources of inoculum for the succeeding crop (Friese andAllen, 1991) Any management practice or change in climate that acceleratesdecomposition of colonized root fragments can result in a decline in subse-quent AM colonization levels

pro-Changes in AM fungal species and spore densities in annual croppingsystems have been reported to occur in response to tillage practices In a No-

till corn and soybean system, Glomus occultum predominated while in a ventional tillage system, spores of Glomus etunicatum were the most

con-numerous (Douds et al., 1995) The negative effects of tillage on AM fungalspore production and densities have been primarily observed to occur in thetop 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, therebyreducing inoculum densities (Kabir et al., 1999) which in turn may result in adecrease in seedling establishment during the following year

Depending upon the crop, climate, and rainfall patterns for a particularregion, 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

The decisions that are made at this management level can have profoundnegative and positive effects on the production and survival of AM inocu-lum The types of propagules that are present in a production system andtheir 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 producespores (Abbott and Gazey, 1994), the importance of the AM hyphal network

in the soil and the survivability of AM hyphae contained within living anddead roots become critical if one is to develop management strategies of AMfungi in an annual cropping system Walker and Smith (1984) showed thatthe rate of AM colonization was determined primarily by the density of AMpropagules in the soil In the southern parts of Australia, AM fungi appear tosurvive 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 bestsurvives 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 awater management plan The length of time that a suitable AM host is absentfrom a field can result in a significant decline in AM propagules and limitedcolonization of the subsequent crop Long-fallow disorder has now beenattributed to declines in AM propagule densities due to the extended periodswithout 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 fungalspores, 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 todecline 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 thatoccurred 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 thresholdneeded for colonization of cotton in southern Australia

While fallow alone may or may not have a negative impact on quent mycorrhizal colonization, fallowing is usually followed by tillage

subse-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 werecombined, there were substantial declines in AM hyphal infectivity andmetabolic 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 thegrowing season to maintain crop vigor and enhance yield quality In addi-tion, herbicide applications are routinely made either during the growingseason 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 thatRound-Up herbicide will be applied to cotton fields for weed control whenthe genetically altered plant is used The long-term effects of these and othergenetic modifications of cotton (Table 7.1) on mycorrhizal development havenot been examined in detail

Table 7.1 Pesticides Applied to Conventional Cotton Cropping Systems on

the Southern High Plains, Texas Pesticide Target Time of Application

The specific impacts of various fungicides, pesticides, and herbicides on

AM colonization and species occurrences have been reviewed and 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 changedmuch since these reviews were published As would be expected of the vari-ous types of biocides, fungicides have the greatest impact on mycorrhizalsurvival and subsequent colonization However, application rates, time ofapplication, and method of application (foliar sprays versus soil drench) all

summa-in combsumma-ination determsumma-ine the fsumma-inal 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 acrossannual cropping systems, because of the interactive effects of soil influences,species of AM fungi, and indirect effects of the fungicides on soil organismsantagonistic 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 plantcontrol 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) AMinoculum potentials may be reduced when residual effects of pre-emergentherbicides affect root growth during the growing season, as is sometimesobserved in cotton in west Texas

Most insecticides and nematicides have been reported not to have anyimpact on AM colonization When fungivorous nematodes are reduced,increases in AM colonization have been reported (e.g., Sreenivasa andBagyaraj, 1989) However, as mentioned by Kurle and Pfleger (1994), there isstill too little information available to make generalizations