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22.1 Introduction

Tropical forests are important for their diverse bioresources as well as the significance of the carbon pool. Tropical forests are disappearing at the rate of 13.5 million hectares (ha) each year, largely due to logging, burning and clearing for agricultural land, and shifting cultivation (Kobayashi 2004). Timber harvesting has resulted in the transformation of more than five million ha of tropical forest annually into over-logged, poorly managed, and degraded forests. Degraded tropical forests require wide-scale rehabilitation and it is not easy to rehabilitate degraded tropical forests because a major obstacle in the rehabilitation of tropical forests is slow tree growth and high mortality of seedlings in the nursery. It is also necessary to understand the physical, chemical, and biological factors of forest soils, in order to remediate degraded tropical forests. Among these properties, biological properties are least well known. Arbuscular mycorrhizal (AM) fungi affect the maintenance of vegetation in various ecosystems and may play an important role in tropical forests. Most tropical tree species form arbuscular mycorrhizas.

The diversity of AM fungi and the breadth of their associations with plant species in natural environments are crucial to understanding the ecological role of AM fungi in plant coexistence. AM fungal community structures differ significantly between host species and have been reported to increase the growth and survival rate of some tropical tree seedlings (Wubet et al. 2009). Phosphorus (P) limits the productivity of trees in many forests and plantations especially in highly weathered, acidic, or calcareous profiles in the world. Most trees form mycorrhizal associations which are prevalent in the organic and mineral soil horizons. Mycorrhizal tree roots have a greater capacity to take up phosphate (Pi) from the soil solution than non-mycorrhizal roots (Plassard and Dell 2010). Rehabilitation of degraded tropical forests following inoculation of AM fungi has potential to restore important ecosystem functions. The purpose of this chapter is to review the effect of inoculation of AM fungi on growth of native tree species from tropical forests.

22.2 Degraded Tropical Forest and Reforestation

The total world’s forests cover nearly 3.9 billion ha or nearly 30 % of the world’s land area (FAO 2001; Fenning and Gershenzon 2002). The number of tropical forests has been declining owing to illegal logging, fire, conversion into agricultural lands, rubber tree and palm oil plantation, and use of the forest plantation estate as pulp trees. Degraded forests are considered to be low-value resources because they are characterized by the vegetation such as ferns, sedges, and scrub. However, it is not easy to rehabilitate this ecosystem in a short term, because it is necessary to select and produce high-quality tree seedling species that have high survival rates during the rehabilitation process.

Tropical forests contribute considerably in sustaining global biodiversity (Laurence 1999). They are homes to indigenous people, pharmacopeias of natural products, and providers of vital ecosystem services, such as flood amelioration and soil conservation. At regional and global scales, tropical forests also have a major influence on climate and carbon storage. Tropical forestlands have been disappearing at the rate of 13.5 million ha each year. Furthermore, timber harvesting has resulted in the transformation of more than five million ha of tropical forest annually into logged-over, poorly managed, and degraded forests.

One of the most serious world problems affecting tropical rain forest is desertification. This is a complex and dynamic process which is claiming several 100 million ha annually. Tropical forests are particularly affected, resulting in a rapid reduction in area. Human activities can cause or accelerate desertification and the loss of most plant species as well as their associated symbioses. The reduction and degradation caused by anthropological activities affect not only the sustainable production of timber but also the global environment. Accurate scientific information will enable managers to devise silvicultural systems to enhance soil properties and forest resources important for sustainable production and for minimizing deleterious impacts of harvesting and short-rotation plantation. Degraded tropical forested lands require wide-scale rehabilitation and it is necessary to improve the biological diversity of tropical forestlands and to enhance the commercial value of timber.

The rapid production of forest planting stock seedlings of high quality in nurseries is important for replenishing degraded tropical forestlands. Moreover, many soils of tropical forests are nutrient poor (Hattenschwiler et al. 2011). Soil nutrient availability is one of the limiting factors for the early growth of transplanted seedlings in degraded tropical forestlands. Degraded tropical forestlands are recognized as low-value forest resources without successful natural regeneration that are dominated by grasslands including fern, sedges, or scrub. Nowadays, reforestation programs have to prepare millions of seedling stocks annually. The use of vigorous seedlings in reforestation programs is important. However, seedling stocks of tropical forest species are usually weak, often N and P deficient, and have high mortality rates after transplanting in the field. Phosphorus was the most limiting nutrient for plant growth of four woody legume species (Moreira et al. 2010). Ultimately, rehabilitation can increase the area of forest as well as contribute to conservation of the remaining primary forests and environmental quality.

22.3 Ecology of Arbuscular Mycorrhizal Fungi in Tropical Forests

Tropical rain forest soils often have high P adsorption because of their strong affinity to P to form iron and aluminum oxides and hydroxides, whereas in neutral and alkaline soils, P is adsorbed on the surface of Ca and Mg carbonates (Holford 1997; Whitmore 1989). Soil P concentration of tropical soil is very low (Table 22.1). In most experiment with tropical rain forest plant species, the influence of AM fungi on P nutrition has been evaluated by measuring the growth response of inoculated and non-inoculated plants cultivated in soils with controlled levels of P (Janos 1980). Moyersoen et al. (1998) reported that AM colonization of the tropical tree Oubanguia alata (Scytopetalaceae) was positively correlated with increased P uptake despite low P availability in Korup National Park rain forest, Cameroon.

Table 22.1 Arbuscular mycorrhizal colonization, mycorrhizal dependency (MD) of different tree species grown in tropical forests, and soil phosphorus concentration
Full size table

Early studies focused primarily on mycorrhizas of the temperate forests, but attention turned toward mycorrhizas of the tropical rain forests (Torti et al. 1997). In contrast to the temperate zone, where mycorrhizal associations of trees tend to be formed by ectomycorrhizal fungi, the majority of tropical tree species surveyed thus far are formed by AM fungi (Janos 1980). Notable exceptions of tropical trees forming ectomycorrhizas occur in the families Myrtaceae, Caesalpiniaceae, Euphorbiaceae, Fagaceae, and Dipterocarpaceae (Munyanziza et al. 1997). The highest number of species and spores of AM fungi was observed during the dry season, with a marked decrease during the rainy season in a tropical rain forest in Veracruz, Mexico (Guadarrama and Alvarez-Sanchez 1999). Moyersoen et al. (2001) reported that AM colonization was about 40 % in tree species in heath forests and mixed Dipterocarpaceae forest in Brunei. Tawaraya et al. (2003) showed that 17 of 22 tree species in a tropical peat swamp forest in Kalimantan, Indonesia, had mycorrhizas formed by AM fungi. Of the 142 species of trees and liana surveyed in Guyana, 137 were exclusively formed by AM fungi (McGuire et al. 2008). A light microscopy investigation showed arbuscular mycorrhizas in 112 tree species from 53 families on mineral as well as organic soils in Ecuador (Kottke et al. 2004). In a related study, a segment of fungal 18S rDNA was sequenced from the mycorrhizas of Cedrela montana, Heliocarpus americanus, Juglans neotropica, and Tabebuia chrysantha in reforestation plots from degraded pastures in Ecuador and observed distinct species-rich AM communities (Haug et al. 2010). Dual ectomycorrhizal and AM colonization was observed in 4 of 14 ectomycorrhizal tree species belonging to Caesalpiniaceae and Uapacaceae from rain forest in Cameroon (Moyersoen and Fitter 1999). In total, 193 glomeromycotan sequences were analyzed, 130 of them previously unpublished.

Spores of AM fungi have been isolated from soils of tropical forests and their population and richness were affected by environmental conditions. Spore density and richness based on soil cores were higher in the dry season than in the rainy season in a tropical sclerophyllous shrubland in the Venezuelan Guayana (Cuenca and Lovera 2010). Spore numbers of AM fungi were higher in young secondary forest and pastures and lower in pristine forest in the Amazon region (Sturmer et al. 2009), and AM fungal diversity was high in dry tropical Afromontane forests of Ethiopia (Wubet et al. 2009). AM fungal spores in soil decreased from an early plant succession to mature tropical forest in a Brazilian study (Zangaro et al. 2008). AM fungal types that were dominant in the newly germinated seedlings were almost entirely replaced by previously rare types in the surviving seedlings the following years (Husband et al. 2002a). As the seedlings matured in a tropical forest in the Republic of Panama, the fungal diversity decreased and there was a significant shift (Husband et al. 2002b). Based on spore morphology, 29 species of AM fungi were found in the rhizosphere of Macaranga denticulata (Youpensuk et al. 2004).

22.4 Inoculation of Tropical Tree Species with AM Fungi

AM fungi have been reported to increase growth of some tropical trees (Table 22.1). AM fungi increased seedling growth of 23 of 28 species from a lowland tropical rain forest in Costa Rica under nursery conditions (Janos 1980). AM colonization of the tropical tree Oubanguia alata (Scytopetalaceae) was positively correlated with increased P uptake despite low P availability in a study in Cameroon (Moyersoen et al. 1998). AM fungi improved growth of the Brazilian pine Araucaria angustifolia (Araucariaceae) (Zandavalli et al. 2004). There are also reports of improved growth of non-timber forest product tree species following AM fungal inoculation in tropical forests. For example, Muthukumar et al. (2001) reported that inoculation of Azadirachta indica (Meliaceae) with AM fungi improved seedling growth. Furthermore, the inoculation of AM fungi with phosphate-solubilizing and nitrogen-fixing bacteria increased the growth of A. indica. Conversely, A. excelsa inoculated with AM fungi (without fertilizer) grew more slowly than did the uninoculated plants (Huat et al. 2002). Kashyap et al. (2004) showed that inoculation of Morus alba (Moraceae) with both AM fungi and Azotobacter increased the survival percentage of saplings.

Clusia minor and Clusia multiflora inoculated with Scutellospora fulgida in acidic soil had greater shoot and root biomass, leaf area, and height in comparison to the biomass of P-fertilized plants and non-mycorrhizal plants (Cáceres and Cuenca 2006). Inoculation with the AM fungus Glomus geosporum improved the growth, nutrient acquisition, and seedling quality of Casuarina equisetifolia seedlings under nursery conditions (Muthukumar and Udaiyan 2010). Seedlings of Araucaria angustifolia inoculated with Glomus clarum had higher shoot biomass; leaf concentrations of P, K, Na, and Cu; and lower concentrations of Ca, Mg, Fe, Mn, and B than controls (Zandavalli et al. 2004). Inoculation with soil-containing AM fungi increased shoot growth nutrient contents when P was limiting but N was applied (Youpensuk et al. 2004). Inoculation with AM fungi Glomus clarum and Gigaspora decipiens increased shoot N and P uptake of non-timber forest product species Dyera polyphylla and Aquilaria filaria under greenhouse conditions, indicating that AM fungi can reduce the application of chemical fertilizer (Turjaman et al. 2006). Other studies have used mycorrhizal roots from individual tree species or from a mixture of the four trap species with resulting improvement in growth of 6-month-old Cedrela montana and Heliocarpus americanus (Urgiles et al. 2009). This latter technique is much easier to handle and has lower costs than spore production for tropical countries with limited facilities for storage of inoculum.

AM fungi increased the growth of Acacia nilotica and Leucaena leucocephala (Leguminosae) 12 weeks after transplantation under greenhouse conditions (Michelsen and Rosendahl 1990), and similar observations were made for three multipurpose fruit-tree species: Parkia biglobosa, Tamarindus indica, and Ziziphus mauritiana 2 months after inoculation (Guissou et al. 1998). The AM fungus Glomus aggregatum stimulated plant growth of 17 leguminous plants (Duponnois et al. 2001), and Glomus macrocarpum increased the growth of two species: Sesbania aegyptiaca and S. grandiflora (Giri et al. 2004). Some studies have successfully used mixed inocula of AM fungi including two (Bá et al. 2000), three (Adjoud et al. 1996), and nine species (Rajan et al. 2000).

Mycorrhizal dependency was calculated to compare the degree of plant growth change associated with AM colonization of 76 species, 25 families (Table 22.1). The average mycorrhizal dependency value of all the plants was 50 % (−69 Min. and 100 Max.). Mycorrhizal dependency was also different among families. It was higher in Ulmaceae and Bignoniaceae. Guissou et al. (1998) reported that mycorrhizal dependency of Parkia biglobosa and Tamarindus indica was similar, reaching no more than 36 %, while Ziziphus mauritiana showed higher mycorrhizal dependency values, reaching up to 78 %. A similar effectiveness of AM fungi for different plant species was also reported by Adjoud et al. (1996). Mycorrhizal dependency is frequently related to the morphological properties of the root of different plant species, and also root systems with only a few, short root hairs are indicative of a high mycorrhizal dependency of the plant species concerned (Baylis 1970). Responses of 12 native woody species to the inoculation of AM fungi were related to root morphological plasticity of the plant (Zangaro et al. 2007).

The survival rate of seedling stocks in the field is vital to reforestation. In one study, the survival rates of AM-inoculated cuttings of Ploiarium alternifolium and Calophyllum hosei were 100 % after 6 months (Turjaman et al. 2008). These values were higher than the survival rates of two tropical tree species from Panama inoculated with AM fungi, which were Ochroma pyramidale (97 %) and Luehea seemannii (52 %), respectively (Kiers et al. 2000). Inoculation with AM fungi can reduce the cost of seedling production for reforesting vast areas of disturbed tropical forests. Despite extensive studies of inoculation of tree species under controlled conditions, there are few reports about the effect of AM fungal inoculation on growth of tropical tree species under field conditions. Recently, Graham et al. (2013) showed that inoculation of Glomus clarum and Gigaspora decipiens increased N and P content of Dyera polyphylla under tropical peat swamp forest in Central Kalimantan, Indonesia.

22.5 Conclusion

Colonization of roots by AM fungi can improve growth of many tree species that occur in tropical forests. Survival rate of seedlings is a key measure of success in reforestation and afforestation. Survival rates of inoculated seedlings can be higher than those of non-inoculated seedlings. Inoculation with AM fungi at the nursery stage is a useful technique to include in large-scale reforestation programs. However, mycorrhizal dependency differs among plant species and with species of AM fungi. Therefore, selection of appropriate combination of plant species and fungal species is also important for reforestation programs.