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Mycorrhizas and tropical soil fertility

Irene M. Cardoso a,*, Thomas W. Kuyper b

aDepartment of Soil Sciences, Federal University of Vicosa, Vicosa 36570-000, Minas Gerais, Brazil

bDepartment of Soil Quality, Wageningen University, P.O. Box 8005, 6700 EC Wageningen, the Netherlands

Available online 24 May 2006

Abstract

Major factors that constrain tropical soil fertility and sustainable agriculture are low nutrient capital, moisture stress, erosion, high Pfixation, high acidity with aluminium toxicity, and low soil biodiversity. The fragility of many tropical soils limits food production in annual

cropping systems. Because some tropical soils under natural conditions have high biological activity, an increased use of the biological

potential of these soils to counter the challenges of food production problems is proposed. Most plant species (including the major crops in the

tropics) form beneficial associations with arbuscular mycorrhizal (AM) fungi. These fungi could be the most important and poorly understood

resource for nutrient acquisition and plant growth in agriculture. This review treats the role of AM fungi in enhancing physical, chemical, and

biological soil quality. It focuses on the roles of AM in maintenance and improvement of soil structure, the uptake of relatively immobile

elements, both macronutrients (phosphorus) and micronutrients (zinc), the alleviation of aluminium and manganese toxicity, the interactions

with other beneficial soil organisms (nitrogen-fixing rhizobia), and improved protection against pathogens. Mycorrhizal associations enable a

better use of sparingly soluble phosphorus pools, thereby increasing the efficiency of added phosphorus fertilizer and of the large relatively

immobile phosphorus pools. Mycorrhizal management through agroforestry, reduced soil disturbance or crop rotation, is often a better option

than mycorrhizal inoculation, considering the problems and costs of large-scale inoculum production. Research directions that are needed to

increase understanding of mycorrhizal associations in tropical cropping systems and to increase mycorrhizal benefit are indicated.

# 2006 Elsevier B.V. All rights reserved.

Keywords: Arbuscular mycorrhizal fungi; Tropical soils; Soil structure; Soil fertility

1. Introduction

Many soils in the tropics are fragile and prone to

degradation. Some characteristics of tropical soils put severe

constraints on food production. Sanchez et al. (2003)

proposed a fertility capability soil classification that

identifies the major attributes that constrain plant produc-

tion. These constraints include soil moisture stress (a dryseason lasting longer than 3 months makes year-round crop

production difficult), low nutrient capital, erosion risks, low

pH with aluminium (Al) toxicity, high phosphorus (P)

fixation, low levels of soil organic matter, and a loss of soil

biodiversity.

In the last century, the so-called Green Revolution

technologies, such as the use of pesticides, synthetic

fertilizers and high-yielding cultivars, were used to over-

come these constraints (Dalgaard et al., 2003). With this

technology the global food supply increased, reducing

hunger and improving nutrition. Nevertheless, a billion

people have no food security and many rural communities in

the tropics and subtropics are persistently affected by adecline in household food production (Stocking, 2003). The

Green Revolution techniques also increased natural resource

degradation, raising questions about the sustainability of

current agricultural practices (Dalgaard et al., 2003). Yields

have stagnated in several regions for 1520 years. The

challenge for the next 50 years is to double food production

in a way that does not compromise environmental integrity

and public health (Tilman et al., 2002). Janssen (2006) states

that the technical discussion has to be focused on the

www.elsevier.com/locate/ageeAgriculture, Ecosystems and Environment 116 (2006) 7284

* Corresponding author.

E-mail address: [email protected] (I.M. Cardoso).

0167-8809/$ see front matter # 2006 Elsevier B.V. All rights reserved.

doi:10.1016/j.agee.2006.03.011
mailto:[email protected]://dx.doi.org/10.1016/j.agee.2006.03.011http://dx.doi.org/10.1016/j.agee.2006.03.011mailto:[email protected]


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efficiency of nutrient use as affected by the proportions of

added nutrients, immobilization processes in the soil and

production capacity of crops, and on site-specificity of

nutrient management. For better nutrient management in the

tropics, an increased use of biological potential is important.

It has been suggested that imitating natural ecosystems

rather than planting monocultures is the best agriculturalstrategy for the tropics. Keys to agricultural success in the

tropics are to use adequate plant species diversity and to use

perennial plants to maintain soil fertility, to guard against

erosion and to fully utilize resources (Altieri, 2004).

Agroforestry systems fulfil these conditions. They mimic

tropical forests, with a diversity of species that tend to be

productive, pest resistant, and maintain soil organic matter

and soil biological activity at levels satisfactory for soil

fertility (Young, 1997; Ewel, 1999; Van Noordwijk and Ong,

1999). Mixtures of plant species usually allow a larger

diversity and/or abundance of mycorrhizal fungi (the subject

of this review) than monocultures.

2. Mycorrhiza

The fungi that are probably most abundant in agricultural

soils are arbuscular mycorrhizal (AM) fungi (phylum

Glomeromycota). They account for 550% of the biomass

of soil microbes (Olsson et al., 1999). Biomass of hyphae of

AM fungi may amount to 54900 kg ha1 (Zhu and Miller,

2003), and some products formed by them may account for

another 3000 kg (Lovelock et al., 2004). Pools of organic

carbon such as glomalin produced by AM fungi may even

exceed soil microbial biomass by a factor of 1020 (Rilliget al., 2001). The external mycelium attains as much as 3%

of root weight (Jakobsen and Rosendahl, 1990). Approxi-

mately 10100 m mycorrhizal mycelium can be found per

cm root (McGonigle and Miller, 1999). Almost all tropical

crops are mycorrhizal, and many, if not most, are strongly

responsive to arbuscular mycorrhizas. A substantial number

are also strongly dependent on arbuscular mycorrhizas.

Norman et al. (1995) treated 12 major food crop genera in

detail, and listed a further 14. All these genera form AM

symbioses. Only a few families and genera of plants do not

generally form arbuscular mycorrhizas; these include

Brassicaceae (their root exudates are possibly even toxic

to AM fungi), Caryophyllaceae, Cyperaceae, Juncaceae,

Chenopodiaceae, and Amaranthaceae (although each of

these families has some representatives that are usually

colonized by AM fungi). Because of the importance of AM

fungi to tropical soil fertility, the focus of this review will be

on the AM symbiosis. The effects of the association will be

reviewed from an agronomists viewpoint. Such an approach

omits a mycocentric view, and is more restricted than a

phytocentric view because it does not include aspects of

plant fitness (for instance plant survival) but only treats

primary production of desirable plant parts (leaves, fruits

and tubers).

The AM association has received attention as part of an

increasingly popular paradigm that considers an active and

diverse soil biological community as essential for increasing

the sustainability of agricultural systems. The ability of AM

fungi to enhance hostplant uptake of relatively immobile

nutrients, in particular P, and several micronutrients, has

been the most recognized beneficial effect of mycorrhiza.Rhizosphere interactions occur between AM fungi and other

soil micro-organisms with effects on plant nutrient balances,

such as nitrogen-fixing bacteria and plant growth-promoting

rhizobacteria (Paula et al., 1993). AM colonization may

furthermore protect plants against pathogens. AM fungi

interact with heavy metals/micronutrients. They can restore

the equilibrium of nutrient uptake that is misbalanced by

heavy metals (Carneiro et al., 2001; Siqueira et al., 1999).

AM fungi can alleviate Al toxicity. AM fungi improve water

relations, especially under nutrient limitation. The extra-

radical hyphae of AM fungi contribute to soil aggregation

and structural stability. Therefore, mycorrhizas are multi-

functional in (agro)ecosystems (Newsham et al., 1995),

potentially improving physical soil quality (through the

external hyphae), chemical soil quality (through enhanced

nutrient uptake), and biological soil quality (through the soil

food web).

Several recent reviews have dealt with the role of

mycorrhizal associations in soil quality and sustainable

agriculture (Dodd, 2000; Barea et al., 2002; Gianinazzi

et al., 2002; Jeffries et al., 2002; Ryan and Graham, 2002;

Harrier and Watson, 2003). These reviews generally focused

on temperate soils. Reviewing the role of mycorrhizas in

tropical soil fertility, more than a decade after the seminal

book by Sieverding (1991), is important for two relatedreasons: (1) soils, major crops and possibly the species

composition of AM fungal communities are different

between the major climatic zones. Because mycorrhizal

functioning depends on the interplay between fungi, plants

and the abiotic environment, different perspectives may

arise from temperate and tropical views; (2) agriculture in

temperate regions is often characterized by conditions of

excess, that in tropical regions by problems of access ( Van

Noordwijk and Cadish, 2002). The latter contrast is evident

for both major macronutrients (phosphorus and nitrogen)

and several micronutrients and heavy metals. The question

whether mining P of saturated soils through mycorrhizal

associations is desirable (Liu et al., 2003a,b) is different

from the question whether mining the unavailable P pools in

P-fixing Oxisols is a useful strategy. Managing mycorrhizal

associations for the remediation of heavy metal pollution in

agricultural soils (Leyval et al., 1997; Entry et al., 2002) is

different from the use of AM associations to prevent

micronutrient deficiencies in crops. Whereas the increased

interest in mycorrhizas in temperate cropping systems has

received an impetus through the transformation towards

organic farming (Mader et al., 2002; Ryan and Graham,

2002), the situation in the tropics is very different. Resource-

poor farmers in the tropics are usually organic by default as a

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consequence of low prices for agricultural products and high

prices for fertilizers and technical equipment. Consequently,

an economic analysis as proposed by Miller et al. (1994),

which includes as main variables prices for agricultural

produce and costs of labor and fertilizers, will result in

different outcomes and hence in different management

recommendations.

3. Physical soil quality (soil structure)

Whereas the role of mycorrhizal associations in enhan-

cing nutrient uptake will mainly be relevant in lower input

agro-ecosystems, the mycorrhizal role in maintaining soil

structure is important in all ecosystems (Ryan and Graham,

2002). Formation and maintenance of soil structure will be

influenced by soil properties, root architecture and manage-

ment practices. Weathered tropical soils, such as Oxisols,

present desirable physical characteristics. However, soil

management can lead to degradation of soil aggregation due

to dispersion of particles, decrease in the size of the

aggregates, increase in the density, movement of clay in the

horizon and decrease in macro-porosity. The use of

machines and fertilizers are considered to be responsible

for soil degradation (Rosa-Junior, 1984; Carpenedo and

Mielniczuk, 1990). The specific adsorption of P by

functional groups can affect the charge balance and cause

dispersion of particles (Novais and Smyth, 1999; Lima et al.,

2000). Soil aggregation is one component of soil structure.

Mycorrhizal fungi contribute to soil structure by (1)

growth of external hyphae into the soil to create a skeletal

structure that holds soil particles together; (2) creation byexternal hyphae of conditions that are conducive for the

formation of micro-aggregates; (3) enmeshment of micro-

aggregates by external hyphae and roots to form macro-

aggregates; and (4) directly tapping carbon resources of the

plant to the soils (Miller and Jastrow, 1990, 2000). This

direct access will influence the formation of soil aggregates,

because soil carbon is crucial to form organic materials

necessary to cement soil particles. Hyphae of AM fungi may

be more important in this regard than hyphae of saprotrophic

fungi due to their longer residence time in soil, because

fungivorous soil fauna prefers hyphae of the latter over those

of AM fungi (Klironomos and Kendrick, 1996; Gange,

2000). In addition, AM fungi produce glomalin, a specific

soil-protein, whose biochemical nature is still unknown.

Glomalin is quantified by measuring several glomalin-

related soil-protein (GRSP) pools (Rillig, 2004). Glomalin

has a longer residence time in soil than hyphae, allowing for

a long persistent contribution to soil aggregate stabilization.

The residence time for hyphae is considered to vary from

days to months (Langley and Hungate, 2003; Staddon et al.,

2003) and for glomalin from 6 to 42 years (Rillig et al.,

2001). Steinberg and Rillig (2003) demonstrated that even

under relatively favorable conditions for decomposition,

40% of AM fungal hyphae and 75% of total glomalin could

be extracted from the soil 150 days after being separated

from their host. Staddon et al. (2003) reported that

extraradical hyphae turn over in 56 days but mentioned

the possible exception of runner or trunk hyphae that could

have a slower turnover. Hence, different parts of the

extraradical mycelium could have different residence times.

This difference could explain the large variation of residencetimes reported in the literature.

Glomalin is considered to stably glue hyphae to soil

(Wright and Upadhyaya, 1998). The mechanism is the

formation of a sticky string-bag of hyphae (Jastrow and

Miller, 1997; Rillig et al., 2002), which leads to the stability

of aggregates. Glomalin is present in soil in large amounts.

In the top 10 cm of a tropical rain forest in Costa Rica up to

12.5 mg of glomalin cm3 (Lovelock et al., 2004) and in a

chronosequence of Hawaiian soils up to 60 mg of glomalin

cm3 was found (Rillig et al., 2001). Lovelock et al. (2004)

calculated that approximately 3.2% of total soil C and 5% of

soil N in rain forest soil was in the form of glomalin, and

according to Rillig et al. (2001) up to 5% of soil C and 4% of

soil N stocks were derived from glomalin. Miller and

Jastrow (2000) estimated that hyphae and glomalin together

contributed up to 15% of soil organic C in a grassland. The

hydrophobic glycoprotein coating the hyphae and adjacent

soil particles enables the hyphae to survive in gaswater

interfaces and may reduce macroaggregate disruption during

wetting and drying cycles. Moreover, glomalin production

increases carbon flow to soil and therefore, effects on soil

aggregation are expected. The concentration of glomalin

was correlated with stabilization of soil aggregates after a 3-

years transition of a maize cropping system from conven-

tional tillage to no-tillage (Wright et al., 1999). There areindications that some crop rotations favor glomalin

production and aggregate stabilization more than others

(Wright and Anderson, 2000). Thus, management of

cropping systems to enhance soil stability and reduce

erosion may often benefit from consideration of the factors

controlling production and maintenance of extraradical

hyphae and glomalin. Finally, glomalin likely interacts with

elements such as P, Fe, Al, or heavy metals. One question

that is still not answered is whether glomalin production

increases the fitness of AM fungi and if so, through what

mechanisms. Is glomalin production a mechanism of habitat

modification as suggested by Rillig and Steinberg (2002)?

Does glomalin make hyphae less palatable to soil fauna? Or

does glomalin affect nutrient dynamics by either immobiliz-

ing (heavy metals; Fe or Al) or mobilizing (P) nutrients?

4. Chemical soil quality

4.1. Phosphorus uptake

Low P availability limits plant growth in many acid soils

of the tropics. P deficiency is mainly caused by strong

adsorption of H2PO4 to aluminium (Al) and iron (Fe)

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(hydr)oxides, which turns large proportions of total P into

forms that are unavailable to plants. P in soils is present in

pools varying in availability, and pools with the lowest

availability are the largest in Oxisols. The general cycle of P

in soils is depicted in Fig. 1. The link between the organic

and inorganic P-cycle is traditionally conceptualized as

occurring only through the soil solution phase.Total P in the A and B horizons of an Oxisol in Brazil

were about 270 mg kg1 (Cardoso et al., 2004), but the

distribution of P among pools was different. For plants,

readily available Pi (inorganic P, extracted by Resin and

NaHCO3) and the moderately available Pi (extracted by

NaOH), constituted 18% of all P in the A horizon and 14% in

the B horizon, whereas the recalcitrant Pi pool (Pi extracted

by concentrated HCl) was 49 and 67%, with the inert Pi

(extracted by H2SO4H2O2) constituting 9 and 14% in the A

horizon and B horizon, respectively. The readily and

moderately labile Po (organic P) extracted by NaHCO3 and

NaOH was 19% in the A horizon and 5% in the B horizon.

The Po extracted by HCl, which can include the fraction

occluded in the organic matter was 5% in the A horizon and

none in the B horizon. The differences in P availability and

organic pools between the A and B horizon show the

influence of soil biota in P transformations. These

differences demonstrate how much P, which would end

up in fractions that are very hard to recover, has been (and

could further be?) mobilized through plants and micro-

organisms.

The improvement of P nutrition of plants has been the

most recognized beneficial effect of mycorrhizas. The

mechanism that is generally accepted for this mycorrhizal

role consists of a wider physical exploration of the soil by

mycorrhizal fungi than by roots. But AM fungi may be more

than just an extension of the plants root system. Recent

studies suggested that colonization by the AM fungusGlomus intraradices Schenck & Smith downregulated or

even inhibited the phosphate transporters of the plant, as a

consequence of which all the P was taken up by the fungus,

even though there was no increased P-uptake due to

mycorrhizal colonization. However, the AM fungus Giga-

spora rosea Nicol. & Schenck seemed to upregulate plant P

transporters upon colonization (Smith et al., 2003).

Besides hyphae that extend beyond the root depletion

zone, various subsidiary mechanisms have been proposed to

explain P uptake by mycorrhizal fungi, such as (1) the

kinetics of P uptake into hyphae differ from those of roots

either through a higher affinity (lower Km) or a lower

threshold concentration at which influx equals efflux (Cmin);

(2) roots and hyphae explore microsites differently,

especially small patches of organic matter (St John et al.,

1983; Joner and Jakobsen, 1995); (3) plant roots and

mycorrhizal hyphae affect chemical changes and P

solubility in the (mycor)rhizosphere differently. The last

mechanism could lead to access to inorganic and organic P

sources that are unavailable to non-mycorrhizal plants.

It has been suggested that mycorrhizas may benefit plant

growth by increasing the availability of P from non-labile

sources. In many studies, mycorrhizal and non-mycorrhizal

plants appear to use the same labile P sources (Bolan, 1991;

Hernandez et al., 2000), but other studies demonstrated thatmycorrhizal plants obtained P from normally unavailable

sources of Pi and Po (Bolan et al., 1987; Jayachandran et al.,

1989, 1992; Koide and Kabir, 2000; Feng et al., 2003). These

latter studies were executed in artificial medium or

artificially made P-compounds were added to soil, so

doubts remain whether AM fungi can utilize P that is

naturally fixed or organically bound in soil. For example,

added substrates like phytates are readily mineralized,

whereas endogenous soil Po and Po in plant residues are not

(Joner et al., 2000).

To address this controversy, Cardoso et al. (2006) used

natural substrates, and analyzed the different P pools

through P fractionation prior to and after a treatment with

mycorrhizas. An Al-resistant maize (Zea mays L.) variety

was grown for 3 months in pots with 200 g of the A horizon

of an Oxisol. No significant changes occurred in the

inorganic and organic P pools with non-mycorrhizal plants.

Mycorrhizal plants, on the other hand, depleted the pools of

ResinPi and NaHCO3Pi completely, and the pool of

NaOHPi by about 20%. Therefore, in the short term,

mycorrhizas did more than simply shortening the distance

that P ions must diffuse to plant roots, because mycorrhizas

took up P that was not available in short terms to plants. In

this study, Po was not used by the mycorrhizas and these


Fig. 1. Generalcycleof P in soils(adaptedfrom Stevenson and Cole, 1999).

The P is apportioned into pools that vary in availability to plants. (IVL)

Inorganic very labile, (IML) inorganic moderately labile, (ISI) inorganic

stable or inert, (OVL) organic very labile and (OML) organic moderately

labile. Very labile can be considered available to the plants in short terms,

for example to annual crops. Moderately labile is available to the plants in

medium terms, for example, to perennial crops. Stable is only available in

long term. Inert pool (Pi or Po occluded in the organic matter) was not

included in the model because this pool may not be available at all. Bold

arrows represent very labile pools and dashed arrows represent the stable or

inert pools (Cardoso, 2002).


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pools even increased. Although these results confirmed

uptake by mycorrhizal fungi from P pools not available to

plants on a short term in a pot experiment, the results have

still to be confirmed under field conditions. A mycorrhizal

role for uptake of Po could be excluded because the Po pool

increased. Amounts of plant available fractions (ResinPi

and NaHCO3Pi) in the A horizon were higher (9 mg P kg1

soil) than the threshold concentration (3 mg P kg1 soil)

reported by Hayman (1983) for Centrosema pubescens

Benth. and Paspalum notatum Flugge. Possibly the specific

maize variety was bred for Al-resistance under relatively

high P-availability, and that the threshold for this cultivar

was higher than 3 mg P. By breeding for Al-resistance under

conditions of high P-availability breeders may have selected

varieties with lower dependence on mycorrhizas (Trindade

et al., 2001). Considering that P limits growth in tropical

acid soils, plant breeders should be aware of this unintended

consequence.

A speculative mechanism to explain P uptake by

mycorrhizal fungi involves the production of glomalin.

Glomalin contains very substantial amounts of iron (up to

5% of the glomalin pool, Rillig et al., 2002; Lovelock

et al., 2004). Assuming 0.5 mg glomalin g1 soil with 1%

iron, and assuming that this iron was derived initially from

unavailable FeP forms in the NaOHPi fraction, the

destabilization of this bond could have released 1.75 mg P

per pot, comparable to the 2.01 mg NaOHPi that was

taken up (Cardoso et al., 2006). Bolan et al. (1987) had

already proposed that mycorrhizal fungi may break the

bond between Fe and P, but they did not suggest a

mechanism. Further research into the physiological and

ecological roles of glomalin is needed to address thisquestion.

A specific role for AM fungi in the uptake of rock

phosphate (RP) has sometimes been postulated, because

mycorrhizal plants are thought to be more effective in

utilizing RP than non-mycorrhizal plants. But the mechan-

isms involved have received little attention. Ness and Vlek

(2000) noted that only mycorrhizal maize took up P from

hydroxy-apatite, and that the P was subsequently transferred

to maize. The question whether AM fungi affected apatite

dissolution was not addressed. Pairunan et al. (1980) warned

that a comparison of P uptake by mycorrhizal and non-

mycorrhizal plants at only one addition level of RP may

falsely suggest a role for AM fungi in RP dissolution. Only a

response curve of RP use at several levels by mycorrhizal

and non-mycorrhizal plants could separate effects through

dissolution of RP (accessing sources that are normally

unavailable for plants) and increased uptake through

extension of the depletion zones.

Adding easily soluble P-fertilizers or RP might feed-

back differently on mycorrhizal functioning. Addition of

(triple) superphosphate often reduces mycorrhizal func-

tioning except under conditions of very severe P-

limitation, as reported for an annual crop on a poor sandy

soil (Bagayoko et al., 2000b) or coffee (Coffea arabica L.)

on P-fixing soils (Siqueira et al., 1998). In contrast,

addition of sparingly soluble P sources such as RP can

even increase mycorrhizal colonization (Vanlauwe et al.,

2000; Alloush and Clark, 2001). The magnitude of the

effect seems to be partly crop species-specific, interacting

with the extent to which rhizosphere changes affect RP

dissolution.

4.2. Mining P from the soil

The main strategy to cope with P deficiency in the tropics

has been the addition of fertilizers, either in the form of

synthetic fertilizer or in the form of RP. The price of

fertilizers in the tropics is often prohibitive because the

income of farmers is lower than that of farmers in temperate

regions while fertilizer prices are higher. In Africa, for

example, fertilizer can cost up to six times as much as in

Europe or North America (Sanchez, 2002). The use of

synthetic fertilizer is relatively inefficient because of P

fixation. Most of the fertilizer phosphate in P-fixing soils

ends up in fixed pools, having a recovery of only

approximately 1020% (Janssen, 2006). The use of RP,

mainly consisting of apatite, has been proposed as

alternative to the use of synthetic fertilizer in view of its

very large deposits in Africa (Mowo, 2006).

Even though P is the element that usually limits crop

production in the humid tropics, the amount of total

inorganic P in tropical soils may not be low. In a soil to a

depth of 1 m (which is not much in weathered soils), total

inorganic P can easily amount to 3000 kg ha1, an amount

that will not be quickly depleted by an annual P removalrate of 10 kg ha1 by harvesting crops, assuming two

harvests per year, each of 2.5 t and a biomass P-content of

0.2%; or a removal of 8 kg of P in coffee fruits,

considering 2000 trees of coffee ha1 (Malavolta, 1993;

Cardoso et al., 2006). The use of deep-rooting trees and

shrubs that can take up P from the subsoil (Makumba,

2006) and of plants that can mobilize sparingly soluble

inorganic P sources can be a sustainable strategy because

the depletion due to mining the pools is not likely to

become problematic in the short term. The use of

mycorrhizal plants like Cajanus cajan (L.) Millsp.

(Shibata and Yano, 2003) or Tithonia diversifolia (Hemsl.)

Gray (Jama et al., 2000; Phiri et al., 2003) is based on their

efficacy of mining nutrients.

That mycorrhizas can be used to mine soils for P, should

not be taken as a claim that mycorrhizal fungi are to be

considered as biofertilizers. Contrary to rhizobia, which add

external N to the agroecosystem, AM fungi do not add P. But

their potential to liberate P that otherwise would have ended

up in stable and recalcitrant soils pools, implies that the role

of AM fungi in enhancing uptake and efficiency of internal

plants P pools and externally added P fertilizers, should not

be neglected (Lehmann et al., 2001; Lekberg and Koide,

2005).



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4.3. Nitrogen (N) and potassium (K) uptake

AM plants have been reported to improve nutrition of the

other macronutrients N and K. In acid soils, AM fungi may

be important for the uptake of ammonium (NH4+), which is

less mobile than nitrate (NO3) and where diffusion may

limit its uptake rate. Although nitrate is much more mobilethan ammonium (uptake is regulated through mass flow),

AM fungi may be important in nitrate uptake in

mediterranean and (semi-)desert ecosystems. A similar role

for mycorrhizal fungi may therefore exist for nitrate uptake

in West Africas savanna agro-ecosystems. Because of their

small size, AM fungal hyphae are better able than plant roots

to penetrate decomposing organic material and are therefore

better competitors for recently mineralized N (Hodge,

2003). By capturing simple organic nitrogen compounds,

AM fungi can short-circuit the N-cycle (Hawkins et al.,

2000; Hodge et al., 2001). However, plants seem to be better

than fungi in this regard (Hodge, 2001). It is not clear if this

short-circuit is equally important in tropical as in boreal and

arctic-alpine ecosystems, which are usually dominated by

ectomycorrhizal and ericoid mycorrhizal plants and where

low temperatures may limit N mineralization (Schimel and

Bennett, 2004). Finally, AM fungi can indirectly affect N

availability because enhanced uptake of P is important for

nodulation in legumes.

Concentrations of K were higher in mycorrhizal than in

non-mycorrhizal plants (Bressan et al., 2001; Liu et al.,

2002). Increased K concentrations can be a consequence of

increased P availability on plant growth and the effects of

mycorrhizas on P and K are laborious to disentangle.

4.4. Uptake of micronutrients

Micronutrient deficiencies, especially those of zinc (Zn),

are a major concern in developing countries causing

especially serious health problems among children, infants

and women. Zn deficiency in cereals is a well-known

problem in parts of Africa and China. Zn deficiency in

humans is a consequence of the limited bio-availability of

Zn in tropical soils and hence in plants. Problems may have

been exacerbated as a consequence of increased fertilizer

use. Increased crop production through application of

macronutrient fertilizers can dilute Zn concentrations in

plants. This is the well-known dilution effect, increased

macronutrients availability improve plant growth and

thereby spreads other available nutrients throughout much

issue. More specific interactions between the macronutrient

P and the micronutrient Zn can occur, because P fertilization

increases phytate levels in shoots, thereby reducing Zn bio-

availability in cereals. Conversely, Zn deficiency leads to

upregulation of high affinity P transporters and hence P

accumulation in plants. AM fungi are likely involved in the

interaction between P and Zn. The application of P fertilizer

could reduce mycorrhizal functioning, leading to a lower

uptake of Zn. This effect has been demonstrated by Lambert

et al. (1979). It is not known how general this effect is

because the view of co-uptake and co-transport of P and Zn

might not be correct. Data on P and Zn uptake by

mycorrhizal plants are still contradictory. Jansa et al.

(2003) noted a correlation of P and Zn uptake rates by maize

plants colonized by Glomus intraradices. Conversely, the

study by Mehravaran et al. (2000) provides evidence thatdifferent species of AM fungi differ for the uptake

effectiveness of P and Zn, because uptake of both elements

in mycorrhizal plants was not correlated. A possible

explanation is that AM fungi differently express P and Zn

transporters or differently downregulate the P and Zn

transporters of plants. Recently, Ryan and Angus (2003)

reported the unexpected uncoupling of Zn and P uptake in

mycorrhizal wheat (Triticum aestivum L.) and pea (Pisum

sativum L.) on a P deficient soil in Australia.

4.5. Alleviation of aluminium and manganese toxicity

Whereas the role of ectomycorrhizal and ericoid

mycorrhizal associations in alleviating Al toxicity through

the production of organic acids has been repeatedly

demonstrated, more doubts surround the question whether

AM fungi increase the resistance of plants to Al toxicity or

not. AM fungi may indirectly improve resistance because

mycorrhizal plants can have higher uptake of phosphorus

and of basic cations than plants without mycorrhizas. The

fact that many plants are highly dependent on and responsive

to the AM symbiosis, may give the impression that AM

fungi alleviate Al toxicity. Cuenca et al. (2001) noted that

the tropical plant Clusia multiflora Kunth did not grow in the

absence of AM under a range of Al availabilities (includingnon-toxic levels). The authors observed some variation in

Al-resistance among AM fungi as inoculum from acid soils

had a stronger beneficial effect on plant growth under Al

toxicity than inoculum from neutral soils. Rufyikiri et al.

(2000) provided evidence that the AM fungus Glomus

mosseae (Nicol. & Gerd.) Gerd. & Trappe reduced Al

toxicity in banana (Musa spp.). Most likely the high

mycorrhizal responsiveness and increased uptake of

phosphorus and divalent cations were responsible for

alleviating Al toxicity symptoms in banana leaves.

The concentration of manganese (Mn) in shoots and roots

of mycorrhizal plants is often lower than in non-mycorrhizal

plants (Kothari et al., 1991; Nogueira and Cardoso, 2000;

Nogueira et al., 2004). Nogueira and Cardoso (2000) showed

in greenhouse experiments that mycorrhizal soybeans

(Glycine max (L.) Merr.) grew better and had a lower

concentration of Fe and Mn in the shoots than non-

mycorrhizal soybeans. In the roots, the results were the same

for Mn and inverse for Fe. The decrease of Mn in the shoots

was attributed to reduced availability, whilst the decrease of

Fe in the shoots was attributed to its retention in the roots. In

excess, both Mn and Fe can be toxic to plants, thus

mycorrhizas can protect the plants to their toxicity. The

protection from Mn varied with the species of AM fungi. For



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soybean, this protection was more efficient when the plants

were inoculated with Glomus macrocarpum Tul. & Tul. than

with Glomus etunicatum Becker & Gerd., whereas Giga-

spora margarita Becker & Hall was not efficient (Cardoso

et al., 2003a).

5. Biological soil quality

5.1. Crop protection

AM fungi have the potential to reduce damage caused by

soil-borne pathogenic fungi, nematodes, and bacteria. Meta-

analysis showed that AM fungi generally decreased the

effects of fungal pathogens. Effects on nematodes were more

variable and a general pattern was not evident and the pattern

needs to be tested over a wider range of plants and nematodes

of different feeding strategies (Borowicz, 2001). Interactions

between AM fungi and above-ground pathogens and

herbivores have been noted, but without a consistent pattern.

A variety of mechanisms have been proposed to explain

the protective role of mycorrhizal fungi. A major mechanism

is nutritional, because plants with a good phosphorus status

are less sensitive to pathogen damage. Non-nutritional

mechanisms are also important, because mycorrhizal and

non-mycorrhizal plants with the same internal phosphorus

concentration may still be differentially affected by

pathogens. Such non-nutritional mechanisms include acti-

vation of plant defense systems, changes in exudation

patterns and concomitant changes in mycorrhizosphere

populations, increased lignification of cell walls, and

competition for space for colonization and infection sites.A conceptual separation between nutritional and non-

nutritional mechanisms for pathogen control, even if they

will often interact, is imperative for the application of

mycorrhizal technologies, because nutritional mechanisms

might under certain circumstances more cheaply and/or

more effectively be mimicked by application of mineral

fertilizers or organic amendments.

The fungus Glomus mosseae provided some protection of

peanut ( Arachis hypogaea L.) against pod rot caused by

Rhizoctonia solani Kuhn and Fusarium solani (Mart.) Sacc.

Besides increasing peanut biomass (a nutritional mycor-

rhizal effect), inoculation decreased the abundance of both

pathogens, suggesting a direct interaction between mutu-

alists and pathogens (Abdalla and Abdel-Fattah, 2000). The

pathogens had some negative impact on colonization levels

of the AM fungus. Cowpea (Vigna unguiculata (L.) Wallp.),

colonized by Glomus clarum Nicol. & Schenck, was

protected against the root pathogen Rhizoctonia solani.

Again, the effect was both due to an improved nutritional

status and the direct interaction between AM fungus and

pathogen, possibly competition for infection sites (Abdel-

Fattah and Shabanam, 2002). In a study of mungbean (Vigna

radiata (L.) R. Wilczek) and two pathogens of the genus

Rhizoctonia, Kasiamdari et al. (2002) concluded that

nutritional effects were not important in reducing the

effects of both pathogens, but that the direct interaction

between Glomus coronatum Giovannetti and both Rhizoc-

tonia spp. was responsible for the low incidence of disease.

Interactions between AM fungi and nematodes have been

studied in banana. Jaizme-Vega et al. (1997) stated that

inoculationwith thefungusGlomusmosseae increasedbananaperformance and reduced the reproduction of the root-knot

nematode Meloidogyne incognita (Kofoid & White) Chit-

wood. There was no effect of the nematode on mycorrhizal

development. The interaction between mycorrhizal banana

and the nematode M. javanica (Treub) Chitwood did not

reduce the reproduction of the nematode, but again a positive

growth response of banana was observed (Pinochet et al.,

1997). Timing of the interactions between the AM fungus and

the nematode can be of prime importance. Vaast et al. (1998)

notedthatsimultaneousinoculationofAMfungiwiththeroot-

lesion nematode Pratylenchus coffeae Goodey on coffee did

not enhance tolerance of coffee, but early inoculation (4

months before coffee plants were challenged with the

nematode) significantly improved the tolerance of coffee. In

early inoculation the nematode did not affect AM coloniza-

tion, while in simultaneous inoculation the nematode

suppressed mycorrhizal colonization. An experiment invol-

ving banana and two nematode species (Pratylenchus coffeae

and Radopholus similis Cobb) showed that if the AM fungus

Glomus mosseae was added 2 months before the nematodes,

the nematodes negatively affected mycorrhizal colonization

while the mycorrhizal fungus affected the nematodes

negatively. The effects were to a large extent due to the

improvement of the nutritional status of banana (Elsen et al.,

2003). Finally, the AM symbiosis with Glomus intraradicesannulled differences in nematode species composition as

found in the rhizosphere of different Sahelian legumes

(Villenaveetal.,2003).Mechanismshavenotbeenstudiedand

a general mycorrhizosphere effect was assumed to occur.

AM fungi affected the interaction between sorghum

(Sorghum bicolor (L.) Moench) and witchweed (the

parasitic plant Striga hermonthica (Del.) Benth.). In pot

experiments, AM fungi both compensated for the damage

caused by witchweed and had a negative impact on the

performance of witchweed (Lendzemo and Kuyper, 2001;

Gworgwor and Weber, 2003), whereas in the field AM

fungal inoculation did not have an impact on sorghum,

although it again reduced the performance of witchweed

(Lendzemo et al., 2005). Laboratory experiments showed

that mycorrhizal colonization changed root exudation by

sorghum which resulted in an inhibition of germination of

preconditioned witchweed seeds and this effect could not be

mimicked by phosphorus application (Lendzemo, 2004).

5.2. Interactions between AM fungi and beneficial

rhizosphere organisms

Nodulation and N-fixation by legumes in tropical

cropping systems show wide variation. This could imply



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that such legumes may either deplete soil nitrogen or add

nitrogen. Insufficient nodulation andfixation may be both due

to a lack or scarcity of compatible and effective rhizobia, and

to nutrient deficiencies coupled with an insufficiency of AM

inoculum. Houngnandan et al. (2000) demonstrated that the

rate of N-fixation ofMucuna pruriens (L.) DC., a fallow plant

to restore soil fertility and to control the invasive grass Imperata cylindrica (L.) Beauv. in the derived savanna of

Benin, was often limited by low numbers of effective rhizobia

and could be boosted by rhizobial inoculation, except in very

P-poor soils. The authors concluded that farmers manage-

ment practices that allow a build up of AM fungal inoculum

would alleviate P-deficiency and hence increase N-fixation.

Similar interactions between AM fungi and rhizobia have

been demonstrated for soybean (Glycine max) in low-P soils

of the savanna in Nigeria (Nwoko and Sanginga, 1999;

Sanginga et al., 1999). It was shown that there was a large

variation in mycorrhizal responsiveness to soybean inocula-

tion with AM fungi and that this variability should be

exploited for selecting legumes for growth on marginal soils.

This may be especially relevant because improved soybean

cultivars have often been selected under conditions of P-

sufficiency, a situation probably not dissimilar from the

selection of Al-resistant maize cultivars from Brazil in

conditions of P-sufficiency. Cowpea (Vigna unguiculata)

breedinglines withhigher AM colonizationshowed higher N-

fixation in a low P-soil (Sanginga et al., 2000).

AM fungal and rhizobial responses might show positive

feedback. Rhizobial inoculation increased AM colonization

in soybean (Sanginga et al., 2000) and mucuna (Houng-

nandan et al., 2001). Marques et al. (2001) observed that AM

fungi improved the performance of the woody legumeCentrolobium tomentosum Benth. Ingleby et al. (2001)

demonstrated that AM improved nodulation of Calliandra

calothyrsus Meissn., an agroforestry tree. In a follow-up,

both rhizobia and AM fungi were selected from the trees

native range in Central America and from parts of Africa

where the tree was successfully introduced. In both areas,

effective microsymbionts were obtained. But the interac-

tions between effective rhizobia and effective AM fungi (and

between plant provenances) have not yet been studied

(Lesueur et al., 2001). This may be important because

interactions between AM fungi and rhizobia cannot be

predicted from the behavior of both symbionts individually.

It is still not known when the interaction is additive or

synergistic, both in terms of costs of the symbioses and in

terms of nutrient gains.

6. Management strategies

To benefit from mycorrhizal associations (or more

generally beneficial biological processes in the rhizosphere),

emphasis has to be on agricultural practices that promote the

occurrence and functioning of soil organisms, including AM

fungi. It has been shown that in fragile tropical agro-

ecosystems conventional agriculture, relying on tillage and

external inputs (mineral fertilizers, biocides) for increase of

productivity, may result in large ecological disturbances, and

may be not sustainable in the long term. A key point for the

development of a more self-sufficient and sustaining

agriculture is a better understanding of the nature of agroeco-

systems and the principles by which they function. The aim isto develop agro-ecosystems with minimal dependence on

agrochemical and energy inputs, in which ecological

interactions and synergy among biological components

provide the mechanisms for the systems to sponsor their

own soil fertilityand crop production functions(Altieri, 2002,

2004). In fragile environments, such as the ones discussed by

Janssen (2006) and Giller (2006), these technologies could

offer solutions where other options may fail.

AM fungal species do not seem to be plant species-

specific. This generally low host specificity may allow

mycelial networks of a particular fungus in the soil to be

connected directly to roots of plants of different species,

forming hyphal links between their mycorrhizal roots. These

links provide a pathway that mediates the inter-plant transfer

of nutrients directly through the fungal mycelium, which has

been demonstrated for N (He et al., 2003). Inter-plant

transfer of carbon has been a more contentious issue,

although on balance the present evidence suggests that this is

not of major ecological importance (Fitter, 2001). In

relatively undisturbed agro-ecosystems promoted by agroe-

cology, especially those that include perennial plants and

involve minimal tillage, the mycorrhizal mycelium network

is kept intact. In regularly disturbed agro-ecosystems

dominated by annual crops, where an annual life cycle is

imposed upon the mycorrhizal fungi, the delayed establish-ment of mycorrhizas relative to plants could limit growth

(Kuyper et al., 2004). This could result in limited

phosphorus uptake by seedlings (unless large doses of

fertilizer P are added at the start), as demonstrated for maize

seedlings (Miller, 2000) or low nodulation as demonstrated

for soybean (Goss and De Varennes, 2002).

Crop rotation effects on mycorrhizal functioning have

repeatedly been observed. Harinikumar and Bagyaraj (1988)

observed a 13% reduction in mycorrhizal colonization after 1

year cropping with a non-mycorrhizal crop and a 40%

reduction after fallowing. Lack of inoculum or inoculum

insufficiency after a long bare fallow (especially in climates

with an extended dry, vegetationlessseason) may result in low

uptake of P and Zn and in plants with nutrient deficiency

symptoms that have been described as long-fallow disorder.

The use of mycorrhizal cover crops can overcome this

disorder (Thompson, 1996). Johnson et al. (1992) observed

yield reduction after continuous cropping of soybean and

maize and contributed this decline through monocrops

selecting for AM fungi that are not most beneficial. Although

their data are open to alternative interpretations (build up of

plant species-specific pathogens after monocropping), their

hypothesis was recently confirmed in a study by Bever(2002).

He demonstrated a negative feedback between AM fungi and



9/13

plants, with plants showing a lower performance with fungi

that preferentially associate with that plant.

Sanginga et al. (1999) found evidence for increased

mycorrhizal colonization of soybean if the precedingcrop was

maize, and increased colonization of maize if the preceding

crop was bradyrhizobium-inoculated soybean in the savanna

of Nigeria. Similarly, Bagayoko et al. (2000a) reported higherAM colonization in cereals (sorghum, pearl millet (Pennise-

tum glaucum (L.) R. Br.)) in rotation with legumes (cowpea,

peanut) than in continuous cropping. Nematode densities on

cereals also were decreased in rotation with legumes. Osunde

et al. (2003) reported that AM colonization in maize benefited

from previously grown soybean plants. Boddington and Dodd

(2000a,b) demonstrated beneficial agroforestry effects on

maize in an Indonesian ultisol. Whereas such beneficial

agroforestry effects on mycorrhizas may occur in dry savanna

regions too (Ingleby et al., 1997; Diagne et al., 2001), it might

be more difficult to manage the competition between the

agroforestry trees and crops for water. Such tree crops need

then regular pruning but it is not known how regular pruning

would affect carbon fluxes below-groundand the performance

of the AM fungal community.

Even though AM fungi show only a limited degree of

specificity, different plant species stimulate the amount and

occurrence of different species of AM fungi, thus through

the management of plants it is possible to modify

mycorrhizal populations in the soil (Colozzi and Cardoso,

2000; Hart et al., 2001). A mixture of plants, especially a

mixture of crops and trees such as occurring in agroforestry

systems, may root deeply, resulting in a more equitable

occurrence of mycorrhizas throughout the root zone

(Cardoso et al., 2003b). This increases the volume of soilfrom which nutrients can be taken up efficiently.

Fagbola et al. (1998) and Salami and Osonubi (2002)

proposed agroforestry (alley-cropping) together with mycor-

rhizal inoculation of cassava (Manihot esculenta Crantz) as a

sustainable strategy of land use. But they furthermore noted

that it is still impractical to produce and transport the large

inoculum quantities required for this strategy and recom-

mended research on the potential for on-farm acquisition

and multiplication of mycorrhizal inoculum. Unfortunately,

a discussion on the relative merits of inoculation versus

management of mycorrhizal fungi was lacking in their

papers. We subscribe to the view that in most tropical agro-

ecosystems resource-poor farmers who spend money on

buying mycorrhizal inoculum could better have spent that

money on phosphorus fertilizers. Managing cropping

systems for the benefit of mycorrhizal associations may

be a more direct route towards benefiting of mycorrhizal

associations, an ubiquitous association.

7. Research needs

To better benefit from mycorrhiza at the farmers level, an

increased understanding of mycorrhizal functioning in agro-

ecosystems, especially in multispecies agro-ecosystems, is

necessary. To begin with, screenings can be done to assess

which native plants, including spontaneous vegetation

(weed), trees and shrubs, are mycorrhizal. These plants

could then be used as cover crop in agro-ecosystems or

agroforestry systems. But it should be kept in mind that plant

species in the agroecosystem have several functions and thatfarmers will choose those that best fit their needs, even if

they are non-mycorrhizal. Thus, the association with

mycorrhizal fungi is only one aspect to be considered.

Research should assess under what conditions inocula-

tion with mycorrhizal fungi in agro-ecosystems is oppor-

tune. If mycorrhizal inoculum quantity or quality at a certain

site is limiting productivity in agro-ecosystems, as is often

the case of mined areas (Moreira and Siqueira, 2002;

Lekberg and Koide, 2005), inoculation should become an

option. Several authors have considered inoculation as

important in the seedling phase. These authors argue that the

substrate is normally fumigated to have fewer problems with

pathogens or the seedling is produced through micropro-

pagation. In both cases, inoculation with mycorrhizas could

improve seedling development and plant establishment in

the field (Siqueira et al., 1993; Chu et al., 2001; Cavalcante

et al., 2002; Da Silveira et al., 2002; Soares and Martins,

2000; Trindade et al., 2000, 2001; Locatelli and Lovato,

2002; Locatelli et al., 2002).

In the soil, the P transformation and redistribution into

different forms is the net result of transformations in a highly

dynamic cycle, where micro-organisms play a major role.

The understanding of the role of AM fungi in the

transformation rates from recalcitrant forms to more

available forms of Pi is crucial (Fig. 1). The origin of P(inorganic or organic) that is taken up by the vegetation, as

well as conversion rates of soil organic pools in the field has

to be included in models of P dynamics in more realistic

way. Furthermore, an assessment of the role of Al-bound and

Fe-bound phosphorus and its rate of release is important. To

improve the general understanding of these transformation

rates, models of plant nutrient and water uptake must

explicitly include the role of AM fungi in the P flows among

pools. Such models will yield new insight into nutrient

balance in the tropics. Parameters related to sub-soil

exploitation by trees and other perennial crops (Deugd

et al., 1998) that are normally included in models to study

nutrient budgets can best be understood when the roles of the

AM symbiosis are better known.

8. Conclusions

Sustainable production of food crops in the tropics is

often severely constrained by the fragility of soils, being

prone to several forms of degradation. Making better use of

the biological resources in these soils can contribute to

enhanced sustainability. Mycorrhizal fungi constitute an

important biological resource in this respect. Their



10/13

contribution to biological, chemical, and physical soil

quality has been acknowledged, although many questions

remain how to optimally manage these beneficial fungi.

More fundamental and strategic studies in this field are

therefore needed. With such studies, the policy to support

improvement of soil fertility by small farmers in the tropics

may be less based on increasing nutrients input throughfertilizer programs (Scoones and Toulmin, 1998) and more

on management of local biodiversity. Such studies might

more firmly establish the claim by Sanginga et al. (1999) that

mycorrhizal fungi could be the most important untapped

poorly understood resource for nutrient acquisition and plant

growth in agriculture.

Acknowledgement

Constructive comments on an earlier draft of this paper

by two anonymous reviewers are gratefully acknowledged.

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