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Ann. For. Sci.
Volume 67, Number 3, May 2010
Article Number 301
Number of page(s) 9
Section Review articles
Published online 18 February 2010

© INRA, EDP Sciences, 2010


In tropical Africa, two pedoclimatic zones can be distinguished: humid tropics with dense rainforests or gallery forests, and dry tropics with open bush woodlands, savannas, arid steppes (Garbaye et al., 1988; Le Tacon et al., 1989). In the first ecological zone, where water resources are not a limiting factor for tree growth, forestry is often turned to promote high productivity of timber species by genetic selection, clonal propagation, and use of fast growing exotic species (Khasa and Bousquet, 1995). Therefore high value industrial plantations (e.g. pines, acacias and eucalypts) have been implanted in many humid tropical African areas. In the second ecological zone, where dryness naturally keeps down timber productivity, reforestation is a vital need as the forests are at the basis of population survival, through firewood, non-timber products, soil stabilization. However, the success of reforestation programs required a selection of locally adapted plant species (e.g. fast growing, tolerant of dryness, salinity, heavy metal toxicity) able to face drastic conditions and thus to provide improved environmental situation (Smith and Read, 2008). In this context, exotic trees species belonging to Myrtaceae, Pinaceae, Casuarinaceae and Leguminosae were often used.

Table I

Controlled ectomycorrhization of Pinus caribaea introduced in Central and West Africa.

In their native areas, these exotic tree species are associated with symbiotic microorganisms (mycorrhizal fungi and nitrogen fixing bacteria) which play a significant role in survival and growth of trees. Therefore, the success of tree establishment in a new area involves the availability of functional compatible symbiotic partners. This was convincingly illustrated by the unsuccessful attempts to introduce exotic pines in the tropics until the necessary symbiotic ECM fungi were introduced (Mikola, 1970). Subsequently, seedling inoculation with natural inoculants (soil, crushed fruitbodies or excised ECM roots) has been applied in many tropical African countries to introduce exotic tree species (Garbaye, 1991). However, this practice did not always give best results in growth improvement of exotic tree species in their new habitats, due to the competition between the introduced symbiotic partners and local soil microorganisms (Kabre, 1982; Marx et al., 1985). Hence, to optimize the growth of exotic tree species, use of competitive and effective symbiotic microbial strains was required (Garbaye, 1991; Lamhamedi and Fortin, 1991; Rincón et al., 2007). In this context, the challenge in sylviculture and reforestation was to determine the best compromise between symbiotic compatibility and efficiency of both partners under local soil constraints. This however involves a knowing of symbiotic partners of exotic tree species both in their introduction and native areas.

In this respect, we propose here to review the symbiotic status of exotic tree species useful in reforestation in tropical Africa, and to update reports about their growth improvement through microbial inoculations, specially including ectomycorrhizal ones.


In West Africa, the tropical pine species native of Southeast Asia (e.g. Pinus kesiya), Carribean archipelago (e.g. P. caribaea var. caribaea), Central America (e.g. P. strobus) and North America (e.g. P. radiata) are far the most planted species. These pines are obligate ectotrophs unable to survive or to have a normal growth without symbiotic ECM partners (Delwaulle et al., 1987; Marx et al., 1985; Zhu et al., 2008). Most of their fungal symbionts (Rhizopogon spp., Suillus spp.) are highly host specific, even though some others such as those belonging to the genus Pisolithus may have a broad range of hosts (Bruns et al., 2002; Martin et al., 2002; Marx, 1977; Molina and Trappe, 1994).

P. radiata was the first pine species introduced in Kenya in 1902. However, its seedlings were scrubby and had hardly survived the nursery stage. This failure was only solved in 1910 when the Royal Botanical garden in Kew suggested importing some soil, bearing fungal propagules, harvested under ancient pine plantations from South Africa. Successfully used in Kenya this practice was then generalized in several other countries such as Tanzania, Uganda, Zimbabwe, Zambia and Malawi (Mikola, 1970). In West Africa, the first successful pine (P. kesiya) plantations were obtained in Dalaba (Guinea) in 1914. Their associated ECM fungus was identified as a Rhizopogon, which thought to be pine-specific (Delwaulle et al., 1987; Molina and Trappe, 1994). Later, the soil inoculation practice was applied to successfully introduce pines in Cameroon, Congo, Nigeria, Liberia, Ivory Coast and Ghana (Delwaulle et al., 1987; Marx, 1980; Momoh and Gbadegesin, 1980). It is still unclear how the original nursery saplings were first inoculated. Three hypotheses, non exclusive, were proposed to explain the inoculum origin: (i) planted pines would have been introduced as ornamentals, by migrants coming from European countries; (ii) pine seeds would have harboured fungal spores; and (iii) planted pines fungi would have contracted symbiotic relationships with local ECM fungi. However, due to the symbiotic incompatibility between introduced pines and some indigenous ECM fungi (Bâ, 1990), the third hypothesis seems unlikely. This could be supported by the failure to introduce P. caribaea in Casamance (South Senegal) where the environmental conditions seemed to be cost attractive to the development of this pine species (Delwaulle, 1978; Kabre, 1982).

Garbaye (1991) reviewed the advantages and disadvantages of the use of natural inoculants (e.g. soil from old plantations, fruitbodies, spores). Indeed, if they are costly attractive compared to the pure strain inoculants, natural inoculants are also a way of parasite dissemination. Therefore, use of pure cultures of selected ECM fungi remains the best practice to optimize the efficiency of inoculums for improvement of tree growth (Lamhamedi and Fortin, 1991; Rincón et al., 2007). This was repeatedly illustrated in pine nurseries and plantations in a range of situations (Tab. I). As an example Momoh and Gbadegesin (1980) and later Delwaulle et al. (1982) reported a better growth response of P. caribeae inoculated with a pure Pisolithus tinctorius strain than those with a soil from pine plantations. Nevertheless, this case did not always occur as instanced by Kabre (1982) and Marx et al. (1985). These authors showed that selected fungal strains were less efficient than natural soil inoculants. According to Kabre (1982), the higher efficiency of natural soil inoculants may result from the presence of antagonistic soil actinomycetes against the introduced Pisolithus strains. However, in many cases Pisolithus was shown as the most efficient genus for tropical pines (Le Tacon et al., 1989).


This family comprises 3000 species gathered in 130 genera. Several genera are known as ectomycorrhizal among which Eucalyptus, Melaleuca and Syzygium. African native species all belong to the genus Syzygium (Aubréville, 1950). Eucalyptus and Melaleuca genera are native from Australia, Indonesia and Papua New Guinea but have been introduced in the whole tropics, particularly in Africa. Eucalyptus which is the most planted tree genus in the world includes five subgenera: Monocalyptus, Symphomyrtus, Corymbia, Eudesmia and Idiogenes (Chilvers, 1972). In their native areas, eucalypts contract both arbuscular and ectomycorrhizal symbioses. Among the different subgenera, Monocalyptus (including E. fastigata and E. radiata) and Symphomyrtus (including E. camaldulensis and E. grandis) contain the most ectotrophic species (Chilvers, 1972). According to Chilvers (1972), the diversity of associated ECM fungi would be greater within the Monocalyptus subgenus than within Symphomyrtus. This higher ECM diversity could explain the ability of Monocalyptus to colonize relatively poorer soils than Symphomyrtus (Pryor and Johnson, 1971).

The ECM fungal partners of eucalypts are highly diversified, including both epigeous fungi (e.g. Laccaria laccata, Scleroderma laeve, P. tinctorius) with a wide host spectrum and hypogeous fungi (e.g. Hymenogaster albellus, Hydnangium carneum) with a narrower host spectrum (Castellano and Bougher, 1994; Chen et al., 2007; Malajczuk et al., 1982; Tedersoo et al., 2007). The ECM fungi associated to eucalypts include numerous taxa native from African hardwoods or from American conifers (Chen et al., 2007; Malajczuk et al., 1982; Tedersoo et al., 2007). However, eucalypts would not be compatible with some fungal genera such as Rhizopogon and Suillus generally specific to pines (Malajczuk et al., 1982; Molina and Trappe, 1994). One of the best known eucalypt-associated fungal genera is Pisolithus and its infra-specific diversity was assessed to identify the most efficient isolates promoting eucalypt growth (Aggangan et al., 1996a; Burgess et al., 1994b). Burgess et al. (1994a) and then Martin et al. (2002) reported a large genotypic diversity among Pisolithus. This genotypic diversity was also established at the functional level through eucalypt growth responses to inoculation with Pisolithus isolates from various geographical origins (Aggangan et al., 1996b; Burgess et al., 1994b). The largest plant growth responses were generally recorded with Pisolithus isolates native from Australia (Burgess et al., 1994b).

Eucalypt AM symbioses are much less studied than its ECM symbioses. After Asai (1934) and Maeda (1954), it was only in the 1980s that they were really investigated (Malajczuk et al., 1981). Numerous works (Boudarga et al., 1990; Chen et al., 2000a; 2000b; Chilvers et al., 1987; Lapeyrie and Chilvers, 1985) showed that AM and ECM fungi could coexist not only on the same root system but even in the same root apex. The relative implication of each mycorrhizal type in the plant growth response is not clearly established (Chen et al., 2000a; 2000b; 2007; Lapeyrie and Chilvers, 1985). Nevertheless, a distinct plant response to both types of symbioses was observed along the plant development stage: arbuscular mycorrhizae generally are predominant on young saplings and ectomycorrhizae on older trees (de Mendonça Bellei et al., 1992; Oliveira et al., 1997). The biological processes leading to this mycorrhizal succession remain unknown (van der Heijden, 2001).

Outside their native areas, eucalypts are most commonly associated with ECM fungi belonging to the genera Pisolithus and Scleroderma (Bakshi, 1966; Garbaye et al., 1988; Mikola, 1970; Thapar et al., 1967; Thoen and Ducousso, 1989). The question of the origin (indigenous or introduced) of these fungal genera is still under debate (Garbaye et al., 1988; Le Tacon et al., 1989). Hence, when using eucalypts as exotic tree species in a new plantation two strategies are eligible: either introducing selected ECM fungal strain that shared the same evolutionary history with their natural host, from Australia, or selecting efficient fungal strains among the indigenous fungi (Bâ, 1990; Garbaye et al., 1988). In a field trial in Congo, tree productivity of E. urophylla × E. kirtoniana hybrid trees inoculated with a North-American pine-compatible Pisolithus strain was 30% over the uninoculated controls (Garbaye et al., 1988). However, after one year of plantation, the inoculated strain was rapidly replaced by a local Scleroderma species, revealing the low compatibility of this North-American Pisolithus strain to eucalypts under local pedoclimatic conditions. Furthermore, in vitro experiments evidenced that an Australian Pisolithus, isolated from its natural E. urophylla host was much more aggressive in terms of root colonization than the North-American strain used in Congo (Lei et al., 1990; Malajczuk et al., 1990). This result shows the need of preliminary compatibility and efficiency tests with fungal strains isolated from the native area of the host tree, before field inoculations in a new area. For instance, field trials in China and Philippines (where indigenous fungi had poor compatibility with eucalypts) showed that 2 y after inoculation with selected Australian Pisolithus and Scleroderma strains, the growth of eucalypts was improved 2.5 times over the uninoculated trees (Dell and Malajczuk, 1997). Moreover, local Pisolithus and Scleroderma strains were much less efficient than Australian strains, both in nursery and field experiments in China (Chen et al., 2006; Dell et al., 2002). Molecular tracing of Australian Pisolithus strains revealed that they survived and even fructified in the Chinese plantation soils over 3 y plantation (Dell et al., 2002).

It has been shown in axenic conditions that some scleroderma strains (e.g. S. dictyosporum and S. verrucosum) isolated from African native trees were not compatible with E. camaldulensis that is the most planted species in Senegal (Bâ, 1990) whereas fruitbodies of S. verrucosum and S. capense spontaneously occurred in E. camaldulensis plantations (Thoen and Ducousso, 1989). Nevertheless, regarding the intra-specific variation and distribution of African eucalypt-compatible scleroderms (Sanon et al., 1997), it is unclear whether these S. verrucosum constituted the same strain.


Members of Casuarinaceae family are actinorrhizal trees. They comprise 96 species including 59 Allocasuarina, 17 Casuarina, 2 Ceuthostoma and 18 Gymnostoma (Maggia and Bousquet, 1994). Their native areas range from Australia to South East Asia. Some species of Casuarina and Allocasua-rina have been exported to the whole inter-tropical zone mainly as windbreaks or fuelwood; Casuarina equisetifolia, C. cunninghamiana and C. glauca, being dominant in plantations. In Senegal, thousands of hectares were planted with Casuarinaceae in the Niayes area and all along the littoral between Dakar and Saint-Louis to stabilize sand dunes (Dommergues et al., 1999). Within native area, Casuarinaceae are associated to a wide diversity of ECM fungi, some being common with Eucalypts (Reddell et al., 1991). Allocasuarina is the most ectotrophic genus with a wide diversity of fungal partners: about 20 fungal genera (e.g. Amanita, Elaphomyces, Pisolithus) were registered, while only few species (Scleroderma sp. and Thelephora sp.) were identified below Casuarina trees (Dell et al., 1994; Duponnois et al., 2003; Reddell et al., 1986; Thoen et al., 1990). Moreover, Casuarina does not systematically form ectomycorrhizae (Duponnois et al., 2003; Reddell et al., 1986). Nowadays, few data are available about the AM symbioses among Casuarinaceae, despite that these types of symbioses would be more common in the genus Casuarina (Duponnois et al., 2003; Reddell et al., 1986). A very particular feature of mycorrhizal symbioses has been described within some Neocaledonian species of Gymnostoma as “myconodules”hosting AM fungi belonging to the genus Glomus (Duhoux et al., 2001).

Casuarinaceae are also naturally associated with the nitrogen-fixing actinomycetous Frankia, which has been successfully inoculated to promote the growth of species used for the stabilisation of sand dunes in Senegal (Dommergues et al., 1999). This particular type of symbiosis may be responsible for the success of Casuarinaceae as exotics trees in the forest plantations in many countries. The three types of symbioses (ECM, AM and actinorrhizal symbiosis) have been shown to coexist on the same C. equisetifolia root system (Bâ et al., 1987), but their functional relevance remains unclear. Diem and Gauthier (1982) demonstrated that mycorrhization of C. equisetifolia saplings with Glomus mosseae improved the plant growth, Frankia nodulation and nitrogen fixation. Nevertheless, there is likely no report on mycorrhization of Casuarinaceae species beyond the nursery stage, despite its potential promoting effect on nitrogen fixation and plant growth.


Members of the Dipterocarpaceae are found in the tropics and predominantly in the rain forests of South East Asia. Their economic importance as timber is considerable. In Malaysia, they represent 70% of the timber production (Langenberger, 2006; Maruyama, 1997). Dipterocarpaceae often constitute pure forest stands in South East Asia, where the most common genera are Dipterocarpus, Hopea and Shorea. Some species, belonging to the genera Monotes and Marquesia, are naturally present in African forests, one genus (Pakaraimaeae) in South America, and one genus in the Seychelles (Vateriopsis). Their mycorrhizal status is generally ectotrophic (Moyersoen, 2006; Nataranjan et al., 2005; Rivière et al., 2007; Singh, 1966; Smits, 1992; Tedersoo et al., 2007) and more rarely endotrophic (Aniwat, 1987). Their associated ECM fungi are highly diversified (Hong, 1979; Nataranjan et al., 2005; Watling and Lee, 1995). Six hundred and thirteen fungal species are known to fructify under dipterocarps: 255 of which presumably are ECM fungi (e.g.S. verrucosum, Amanita hemibapha, Lactarius virescens) and 187 constitute new taxa (Watling and Lee, 1995). The genera Amanita, Russula and Phylloporus are among the most frequent both in natural stands and artificial plantations (Nataranjan et al., 2005), while scleroderms are the most represented fruiting taxa in Hopea spp. and Shorea spp. nurseries (Yazid et al., 1996). Recently, Sirikantaramas et al. (2003) using molecular tools evidenced that Thelephoraceae was one of the most common and abundant fungal families found on roots of Dipterocarpaceae.

So far, there is no pure cultivated strain from dipterocarp associated ECM fungi available in the literature (Yazid et al., 1994). This seriously limits the ECM synthesis experiments and controlled ectomycorrhization in nurseries and plantations. However, several features plead for a strong dependency of dipterocarp saplings to ECM fungi. Dipterocarp saplings exhibit a very poor growth without ECM partner, as it has been classically observed with pines (Smits et al., 1988). In addition, inoculations with crushed fruitbodies, excised ECM tips or spores contribute to a significant growth promotion of dipterocarp saplings (Lee, 1991; Lee and Alexander, 1994; Turjaman et al., 2005). Pure ECM fungal cultures would probably be much more beneficial and safer for sapling growth as the crushed fruitbodies and excised ECM tips may also be sources of contaminants (Garbaye, 1991). Furthermore, inoculation experiments in Malaysia using a pure allochtonous strain of P. tinctorius revealed a significant growth response with several Hopea species, but this Pisolithus strain was less competitive than native ECM fungi in plantation (Yazid et al., 1995).

The African dipterocarps are much less diversified than their Asian homologs. Monotes kerstingii is the only Western African dipterocarp which is encountered in association with Isoberlinia forming mixed stands (Aubreville, 1959; Sanon et al., 1997). M. kerstingii forms both AM and ECM symbioses (Sanon et al., 1997). Numerous ECM fruitbodies are detected under this tree species, some of them (e.g. S. verrucosum, Lactarius gymnocarpus) being also associated to Caesalpiniaceae (Sanon et al., 1997). In East Africa, dipterocarps are represented in both Monotes and Marquesia genera with several ECM species, such as Monotes elegans, M. africanus and Marquesia macroura (Alexander and Högberg, 1986; Högberg, 1982). Regarding the economic importance of dipterocarps, more works should be developed to elucidate their mycorrhizal dependency and potential benefits of nursery inoculation practices.


Three subfamilies (Caesalpinioideae, Mimosoideae and Papilionoideae), some containing ECM tree species, constitute the Leguminosae family. In tropical Africa, the most exploited exotic leguminous tree species for their considerable economic interest as multipurpose in traditional agroforestry systems were gathered in Mimosoideae. This subfamily comprises about 2800 species mainly ligneous in semi-arid, subtropical or tropical zones of Africa, America and Australia. The Acacia genus is the most represented with about 1500 species, including three subgenera (Acacia, Aculeiferum, and Phyllodinae) that are distinguished on the molecular phylogeny of the chloroplast DNA sequences (Luckow et al., 2003). Subgenus Acacia contains several important and often emblematic African species (e.g. Acacia nilotica and A. tortilis). As Acacia, the subgenus Aculeiferum includes some important African species such as A. senegal. The third subgenus Phyllodinae contains Australian species of major economical importance as A. mangium, A. auriculiformis and A. crassicarpa. A. mangium is being extensively planted in South East Asia for pulp production (Cossalter, 1986). They are also appreciated in wet African countries as fuel or multipurpose woods (Galiana et al., 1996). In general, all species within Acacia are nodulated with nitrogen – fixing bacteria (Ducousso, 1991; Le Tacon et al., 1989), and are AM mycorrhized (Bâ and Guissou, 1996; Colonna et al., 1991; Duponnois et al., 2002). Generally, species that fit within the subgenus Phyllodinae are also ectomycorrhizal (Ducousso, 1991; Le Tacon et al., 1989). These different types of symbioses are often synergistic, the nitrogen-fixing symbioses having their highest efficiency only after inoculation with AM fungi (Cornet and Diem, 1982). In their native area, Australian acacias are spontaneously associated to the three symbionts (Warcup, 1980), but contrarily to eucalypts there is very few information about the diversity of their associated ECM fungi.

Table II

Field measurements of Acacia holosericea growth parameters in controlled ectomycorrhization trials conducted in Senegal. From Duponnois et al. (2007).

In Africa, the spontaneous ECM partners of Australian acacias would be restricted to the genus Pisolithus (Ducousso, 1990; Duponnois and Bâ, 1999). The origin of these compatible Pisolithus is still unclear, maybe fortuitously introduced. Nonetheless, several authors (Bâ, 1990; Bâ et al., 1994; Duponnois and Plenchette, 2003) detected true ectomycorrhizas between Australian acacias and native African ECM fungi in axenic conditions. For instance, ectomycorrhizal syntheses were obtained between A. holosericea and Scleroderma dictyosporum in axenic and glasshouse conditions (Bâ, 1990; Duponnois and Plenchette, 2003). Duponnois et al. (2005, 2007) observed in several experimental sites in Senegal, through inoculation trials with Pisolithus albus (strain IR100) (Tab. II), a significant growth promotion of A. holosericea and a reduction of negative effects during field transfer. P. albus was even able to develop its full life cycle as fruitbodies within the stand, 2 y after inoculation. In addition, P. albus was found to promote the efficiency of Bradyrhizobium inoculation and therefore growth response of A. holosericea (André et al., 2005). Some temperate ECM fungi such as Boletus and Suillus were also reported to colonize and promote the growth of A. auriculiformis, in Nigeria (Osonubi et al., 1991). In Madagascar, P. microcarpus strain 441 was found to persist on the roots of A. crassicarpa, another Australian species locally appreciated by farmers, while P. albus strain COI 007 was no longer detected after 19 months in the field (Ducousso et al., 2004).

Outside its native area, A. mangium inoculated with native Australian Bradyrhizobium strains generally gave excellent growth responses compared to the local spontaneous bacterial strains (Galiana et al., 1991; 1996). This was observed in African (Galiana et al., 1998; Prin et al., 2003) and Asian countries (Frémont et al., 1999; Martin-Laurent et al., 1999). Inoculation of A. mangium with AM fungi was less convincing probably due to the presence of native efficient strains (de la Cruz and Yantasath, 1993). Concerning ECM symbioses few data are available on spontaneous fungal associates of A. mangium. Only Thelephora ramarioides and Clavaria spp. were reported on A. mangium in Malaysia (Lee, 1990) and Philippines (Anino 1992), respectively. In West Africa, Pisolithus was reported in Australian acacias plantations (Ducousso, 1990; Duponnois et al., 2000). Several studies (Duponnois and Bâ, 1999; Duponnois and Plenchette, 2003) showed that the efficiency of the associations between Acacias and Pisolithus generally depends on soluble P contents in soil.


The works reported in this review pointed out the importance of root symbionts (mycorrhizal fungi and nitrogen fixing bacteria) in establishment and growth of exotic tree species in tropical Africa. Indeed, it was initially observed that exotic pines were unable to establish in the tropics unless symbiotic compatible ECM fungi were introduced (Hacskaylo, 1971). These tropical pines are in fact mostly associated with Rhizopogon spp., and Suillus spp., members of the suilloid group, a monophyletic lineage which includes ECM fungi that exhibit high host specificity (Bruns et al., 2002) and are rarely encountered in tropical Africa (Rivière et al., 2007). Unlike tropical pines, eucalypts are associated with highly diversified ECM fungi. Different growth responses of eucalypts to Pisolithus inoculation were obtained depending on the origins of fungal isolates, the best results being generally observed with isolates sharing the same evolutionary history with their host. This illustrates the importance of taking into account the co-evolution of symbiotic partners in the selection of good symbionts for improvement of timber productivity.

The exotic tree species surveyed for their response to inoculation with selected fungal strains displayed significant mycorrhizal dependencies. Nevertheless, in a new habitat, competition may occur between introduced fungal strains and local soil microorganisms and therefore cuts down the beneficial effect of inoculation on growth of these exotic tree species. In this context, it appears difficult to predict the response of exotic tree species to inoculation in a new habitat without testing the efficiency and competitiveness of selected symbiotic partners under local soil constraints.

On the other hand, exclude Pinaceae which were colonized by only ECM fungi, all exotic tree species presented here are associated with either both ECM and AM fungi (e.g. Eucalyptus), or sometimes with three coexisting symbionts (e.g. Casuarina, Acacia) that are well adapted to the abiotic and biotic factors of their natural habitats. Nevertheless, little is known about the interaction of these different symbionts on their host trees and how they benefit its growth. Hence, the new challenge is to elucidate the relative implication of each symbiont in their host growth promotion for their better exploitation in sylviculture and reforestation.


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All Tables

Table I

Controlled ectomycorrhization of Pinus caribaea introduced in Central and West Africa.

Table II

Field measurements of Acacia holosericea growth parameters in controlled ectomycorrhization trials conducted in Senegal. From Duponnois et al. (2007).