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Agriculture, Ecosystems and Environment 116 (2006) 7284 www.elsevier.


Mycorrhizas and tropical soil fertility

Irene M. Cardoso a,*, Thomas W. Kuyper b
b a Department of Soil Sciences, Federal University of Vicosa, Vicosa 36570-000, Minas Gerais, Brazil Department 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 P xation, 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 benecial 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 benecial soil organisms (nitrogen-xing rhizobia), and improved protection against pathogens. Mycorrhizal associations enable a better use of sparingly soluble phosphorus pools, thereby increasing the efciency 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 benet 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 classication that identies the major attributes that constrain plant production. These constraints include soil moisture stress (a dry season lasting longer than 3 months makes year-round crop production difcult), low nutrient capital, erosion risks, low pH with aluminium (Al) toxicity, high phosphorus (P) xation, low levels of soil organic matter, and a loss of soil biodiversity.

* Corresponding author. E-mail address: (I.M. Cardoso). 0167-8809/$ see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2006.03.011

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 overcome 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 a decline 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

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efciency of nutrient use as affected by the proportions of added nutrients, immobilization processes in the soil and production capacity of crops, and on site-specicity 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 agricultural strategy 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 full 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 (Rillig et al., 2001). The external mycelium attains as much as 3% of root weight (Jakobsen and Rosendahl, 1990). Approximately 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 tness (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 benecial effect of mycorrhiza. Rhizosphere interactions occur between AM fungi and other soil micro-organisms with effects on plant nutrient balances, such as nitrogen-xing 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 extraradical hyphae of AM fungi contribute to soil aggregation and structural stability. Therefore, mycorrhizas are multifunctional 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 related reasons: (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-xing 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 deciencies 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. Resourcepoor 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 enhancing 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 inuenced by soil properties, root architecture and management 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 specic 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 by external hyphae of conditions that are conducive for the formation of micro-aggregates; (3) enmeshment of microaggregates by external hyphae and roots to form macroaggregates; and (4) directly tapping carbon resources of the plant to the soils (Miller and Jastrow, 1990, 2000). This direct access will inuence 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 specic soil-protein, whose biochemical nature is still unknown. Glomalin is quantied by measuring several glomalinrelated 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 residence times 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 ow to soil and therefore, effects on soil aggregation are expected. The concentration of glomalin was correlated with stabilization of soil aggregates after a 3years transition of a maize cropping system from conventional tillage to no-tillage (Wright et al., 1999). There are indications 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 benet 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 tness of AM fungi and if so, through what mechanisms. Is glomalin production a mechanism of habitat modication as suggested by Rillig and Steinberg (2002)? Does glomalin make hyphae less palatable to soil fauna? Or does glomalin affect nutrient dynamics by either immobilizing (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 deciency 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 inuence 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 microorganisms.

Fig. 1. General cycle of P in soils (adapted from 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).

The improvement of P nutrition of plants has been the most recognized benecial 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 fungus Glomus 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 Gigaspora 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 afnity (lower Km) or a lower threshold concentration at which inux equals efux (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 benet 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 that mycorrhizal 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 articial medium or articially made P-compounds were added to soil, so doubts remain whether AM fungi can utilize P that is naturally xed 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 signicant 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


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pools even increased. Although these results conrmed 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 conrmed under eld 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 specic 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 this question. A specic 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 mechanisms 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 nonmycorrhizal 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 feedback differently on mycorrhizal functioning. Addition of (triple) superphosphate often reduces mycorrhizal functioning except under conditions of very severe Plimitation, as reported for an annual crop on a poor sandy soil (Bagayoko et al., 2000b) or coffee (Coffea arabica L.)

on P-xing 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-specic, 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 deciency 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 inefcient because of P xation. Most of the fertilizer phosphate in P-xing soils ends up in xed 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 removal rate 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 efcacy 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 efciency 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 mobile than ammonium (uptake is regulated through mass ow), 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 deciencies, especially those of zinc (Zn), are a major concern in developing countries causing especially serious health problems among children, infants and women. Zn deciency in cereals is a well-known problem in parts of Africa and China. Zn deciency 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 specic interactions between the macronutrient P and the micronutrient Zn can occur, because P fertilization increases phytate levels in shoots, thereby reducing Zn bioavailability in cereals. Conversely, Zn deciency leads to upregulation of high afnity 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 that different 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 decient 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 multiora Kunth did not grow in the absence of AM under a range of Al availabilities (including non-toxic levels). The authors observed some variation in Al-resistance among AM fungi as inoculum from acid soils had a stronger benecial 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 nonmycorrhizal 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 efcient when the plants were inoculated with Glomus macrocarpum Tul. & Tul. than with Glomus etunicatum Becker & Gerd., whereas Gigaspora margarita Becker & Hall was not efcient (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. Metaanalysis 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 activation of plant defense systems, changes in exudation patterns and concomitant changes in mycorrhizosphere populations, increased lignication of cell walls, and competition for space for colonization and infection sites. A conceptual separation between nutritional and nonnutritional 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 mycorrhizal effect), inoculation decreased the abundance of both pathogens, suggesting a direct interaction between mutualists 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 (AbdelFattah 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 Rhizoctonia 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 inoculation with the fungus Glomus mosseae increased banana performance and reduced the reproduction of the root-knot nematode Meloidogyne incognita (Kofoid & White) Chitwood. 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) noted that simultaneous inoculation of AM fungi with the rootlesion 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) signicantly improved the tolerance of coffee. In early inoculation the nematode did not affect AM colonization, while in simultaneous inoculation the nematode suppressed mycorrhizal colonization. An experiment involving 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 intraradices annulled differences in nematode species composition as found in the rhizosphere of different Sahelian legumes (Villenave et al., 2003). Mechanisms have not been studied and 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 eld 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 benecial rhizosphere organisms Nodulation and N-xation 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. Insufcient nodulation and xation may be both due to a lack or scarcity of compatible and effective rhizobia, and to nutrient deciencies coupled with an insufciency of AM inoculum. Houngnandan et al. (2000) demonstrated that the rate of N-xation of Mucuna 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 management practices that allow a build up of AM fungal inoculum would alleviate P-deciency and hence increase N-xation. 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 inoculation 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 Psufciency, a situation probably not dissimilar from the selection of Al-resistant maize cultivars from Brazil in conditions of P-sufciency. Cowpea (Vigna unguiculata) breeding lines with higher AM colonization showed higher Nxation 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 (Houngnandan et al., 2001). Marques et al. (2001) observed that AM fungi improved the performance of the woody legume Centrolobium 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 interactions 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 benet from mycorrhizal associations (or more generally benecial 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-sufcient and sustaining agriculture is a better understanding of the nature of agroecosystems and the principles by which they function. The aim is to 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 fertility and 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 speciesspecic. This generally low host specicity 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 agroecology, 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 establishment 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 insufciency after a long bare fallow (especially in climates with an extended dry, vegetationless season) may result in low uptake of P and Zn and in plants with nutrient deciency 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 benecial. Although their data are open to alternative interpretations (build up of plant species-specic pathogens after monocropping), their hypothesis was recently conrmed in a study by Bever (2002). He demonstrated a negative feedback between AM fungi and


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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 preceding crop 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 higher AM colonization in cereals (sorghum, pearl millet (Pennisetum 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 beneted from previously grown soybean plants. Boddington and Dodd (2000a,b) demonstrated benecial agroforestry effects on maize in an Indonesian ultisol. Whereas such benecial agroforestry effects on mycorrhizas may occur in dry savanna regions too (Ingleby et al., 1997; Diagne et al., 2001), it might be more difcult 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 uxes below-ground and the performance of the AM fungal community. Even though AM fungi show only a limited degree of specicity, 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 soil from which nutrients can be taken up efciently. Fagbola et al. (1998) and Salami and Osonubi (2002) proposed agroforestry (alley-cropping) together with mycorrhizal 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 recommended 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 agroecosystems resource-poor farmers who spend money on buying mycorrhizal inoculum could better have spent that money on phosphorus fertilizers. Managing cropping systems for the benet of mycorrhizal associations may be a more direct route towards beneting of mycorrhizal associations, an ubiquitous association.

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 that farmers will choose those that best t 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 inoculation with mycorrhizal fungi in agro-ecosystems is opportune. 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 micropropagation. In both cases, inoculation with mycorrhizas could improve seedling development and plant establishment in the eld (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 eld 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 ows 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

7. Research needs To better benet from mycorrhiza at the farmers level, an increased understanding of mycorrhizal functioning in agro-

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contribution to biological, chemical, and physical soil quality has been acknowledged, although many questions remain how to optimally manage these benecial fungi. More fundamental and strategic studies in this eld 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 through fertilizer programs (Scoones and Toulmin, 1998) and more on management of local biodiversity. Such studies might more rmly 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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