Ectomycorrhizas and Putative Ectomycorrhizal Fungi of Afzelia Africana Sm. and Uapaca Guineensis Mull. Arg. in Southern Senegal

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Ectomycorrhizas and putative ectomycorrhizal fungi of Afxelia africana Sm. and Uapaca guineensis Müll.. Arg. in southern Senegal

BY D. THOEN'i2 AND A. M. BA' 'Laboratoire de Microbiologie des Sols, ORSTOM, B.P. 1386, Dakar, Senegal 'Fondation Universitaire Luxeinbourgeoise (FUL), rue des Diporte's, No. 140, B-6700 Arlon, Belgium (Received 3 April 1989; accepted 18 August 1989)

SUMMARY

Ectomycorrhizas and ectomycorrhizal fungi of Afielia africana Sm. and Uapaca guineensis Müll. Arg. are reported in forests of southern Senegal. Ectomycorrhizas occurred in dry and wet conditions, at different soil contents of available phosphorus (0-17.5 pg g-'). U.guineensis was confined to groundwater forests. Individual trees had both ecto- and endomycorrhizas, A. africana grew scattered in semi-evergreen and riverside forests, whereas in the woodland it formed larger patches and could dominate the canopy. Eighteen putative ectomycorrhizal fungi grew under U..guineensis and thirty-one under A. africana. Only six species were common to both trees, indicating an ecological and/or taxonomical selection. The fungi belonged to the following Orders : Russulales (16), Boletales (2), (2), (1l), Agaricales (9), Cnntharellales Sclerodermatales Hymenogastrales (l), Gnutieriales (l),Aphyllophorales (1). Some of them had a wide Sudano-Zambezian or Guineo-Congolian distribution and reached their northern limit in Senegal.

Key ivords : Ectomycorrhizal fungi, tropical trees, dual symbiosis, ectomycorrhizas, \V. Xfrica.

Afielia bella in Nigeria (Redhead, 19686). A Russula ISTROD L'CT I O S and an unknown member of the Hygrophoraceae During the last decade there has been renewed were recorded under A. bella in Ghana (Alexander, interest in tropics1 mycorrhizas. Field observations 1985). In the Zambian miombo woodland the main have increased the number of tropical tree genera putative ectomycorrhizal fungi belonged to the known to form ectomycorrhizas (ECM) (Newbery genera Amanita, Cantlzarellus, Lactarius and Russula et al., 1988). In tropical Africa, ECM were reported (Högberg & Piearce, 1986). an-rong the follo\ving families (or subfamilies) and In this paper \ve present observations on the genera: Carsalpinioideae (Afielia, Aphanocalys, ectomycorrhizal fungi and the ECM of -4fidia Antltorrotlta. Berlitria, Bracfiystegia, Didelotia, Gil- africana Sm. and L*Tapacaguineensis Müll. Arg. The bert;ocierccfi.orr. lsoberliru'a, Julberizardia, Micro- ectomycorrhizal status of A. africana in Ghana berlinici, 3~[~riopelalaiithlls,Paramacrolobiunt, Tetra- (Jenik & Mensah, 1967) and in Sigeria (Redhead, berlittia), Dipterocarpaceae (Marquesia, Monotes), 1968a) has already been reported. The mycorrhizal Euphorbiaceae (Uapaca), Papilionoideae (Peri- status of U. gubreensis is reported now for the first copsis), Proteaceae (Faurea) (Peyronel & Fassi, 1957. time. 1960; Fassi S; Fontana, 1961, 1962; Jenik & &lensah, 1967; Redheac!, 1968a, 19686,1980. 1982: Hagberg I0.2 ,A .A l'lif< .AS KT 0 115 & Sylund, 1981; Högberg, 1982; Högberg & SI 1 I.< I) \I I{ Sites Pieíírctr, ; Alesander Sr Högberg, 1986 ; Xles- 1980\YS?; , 1985, Newbery et al., 1988). However, The forests rungr from the Guinean to the Sudano- a few putative ectomycorrhizal fungi were Guinean type (Fig. 1 and 'Table 1). -Innual rainfall tified and their host specificity is poorly docu- !varies from an Lnwage of 1200 mm to more than . .4n Inocj& SP. was observed apociated with 1700 n-rm (period 193 1-60). In recent years, these I

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Mean annual Site Altitude rainfall (mm) Phytogeographical no. Locality (m) (1931-60) region or domain Soil type

1 Santiaba Manjak 10 1700-1 800 Guinean Hydromorphic soil (12"24'N, 16'35'U') and latosol 600-1 îO0 ,I 13.1:\ ottes i o 1 Guineo-Sudanian Latosol (12"29'N, 16'17'W) III Djibelor 10 1500-1 600 G uineo- Sudanian Latosol (12" 34'N, 16" 17'W) IV Tobor 20 1400-1 500 Sudano-Guinean Latosol (12" 43' N, 16" 14' W) Y Tendouk 20 1400-1500 Sudano-Guinean Latosol (1 2" 46' N, 16" 27' W) I Diegoun 25 1400-1500 Sudano- Guinean Latosol (12" 49' N,16" 19' W) \.' II Kalounayes 30 1300-1400 Sudano-Guinean Latosol (12"50' N,16" 8' W) VI11 Thiara 40 1200-1 300 Sudano-Guinean Grey ferruginous (12" 44' N, 14" 32'W) soil IX Dakateli 80 1200-1 300 Sudano-Guinean Hydromorphic soil (12" 27' N, 12" 40' W)

2) Table 2. Main physico-chemical characteristics of the upper soil layer (site no. as in Table

Site no. Ia* Ib** II* III* IV* V* VI* VII' VIII* 9-8 Clay (Yo) 4.2 12.6 3.7 6.0 4.5 5-3 1-6 12.7 Silt (yo) 26.5 18.6 31-0 9.4 8.9 32-7 368 22.6 23.2 Sand (%I 670 65.0 67.9 83.9 795 61.0 566 74.3 63.1 pH (water) 61 4.0 5-8 49 5.8 6.2 5-5 61 5.1 5.3 PH(KCU 5.6 3.5 5.4 3.8 5-0 5.0 5.5 47 Carbon (Yo) 11-7 31-9 29.4 41 11.7 109 19.6 15.2 25 15.1 Nitrogen (%) 1.0 2-5 03 0.7 1*o 1.7 1-5 1.1 C/N 12 13 12 12 13 11 12 10 14 Total phosphorus 83 148 223 19 24 109 122 135 140 g-7 Available phosphorus 0.0 4.4 13-1 3-9 8.3 4.4 4.4 8.7 17.5 95 9 97 - 85 78 70 83 56

~ ~~ * Soil samples taken under Afielia africana: **, soil sample taken under Uapaca guineensis; ***, metallic cations percentage saturation of soil. figures have decreased by an average of approx. (1982) for site I, and Vanden Berghen (1984) for site 100-200 mm. The rainy season extends from June to VIL Site VI11 has a typical woodland structure with October and is followed by a marked dry season. a tree layer and a well developed grass layer. Afielia The Sudano-Guinean tree Afzelia africana has a africana is the dominant tree, accompanied by wide range of habitats. In the semi-evergreen forests Erythrophhum africamm (Welw.) Harms, Daniellia and in the riverside forests it is scattered (Fig. 2a), oliveri (R.) Hutch. & Dalz., Cordyla pinnata (Lepr.) whereas in the woodlands it occurs in small or large Mil.-Red., Pterocarpus erinaceus Poir., Burkea afri- patches and then dominates the canopy. It is present cana Hook., Prosopis africana (G. & Perr.) Taub., in all the sample sites. Uapaca guineensis is a relict Combretum spp. Site IX is a small riverside forest Guinean tree in Senegal, confined to azonal, hydro- where individuàls of U. guineensis arid A. africana morphic soils. In the study area, it is abundant on the grow together. Surrounding vegetation is a degraded border of a wet depression (site i) and scattered in a woodland. Under U. guineensis, the grass layer is riverside forest (site IX). Stilt roots are an adaptation absent and the litter layer is abundant (Fig. 2b), to waterlogging (Fig. 26). whilst under A. africana, the grass layer is well Soils, flora and/or vegetation were described by developed and the little layer is shallow (Fig. 2a). Doumbia (1966)for sites I-VI, Schneider & Sambou Table 2 shows the main characteristics of the upper soil layer (0-20 cm) from sites I to VIlI. ensis. Noteworthy is the great diversity of orders, - . U nde F A. c+ieana-t-h esoi-Is-a reaci d- to- mo-derateIFgenera ~än~-species'tn-'€~êfÜñgärSpeSt~Üm~~t h-K acid ; the metallic cations saturation coefficient (V) africana and U. guineensis. The most represented ranges between 70 !//;o and 97 yo. Under U. guineensis, orders are the Russulales (1 6 species), the Boletales the soil is very acid (pH 4) and poorly saturated (V = (11 species) and the Agaricales (9 species). Several 9 "b). As the water level fluctuates greatly during the fungi, such as Amanita spp. and Russula spp. are still year, leaching occurs causing an important loss of undescribed in Africa and might belong to new nutrients. The content of available phosphorus in species. Xoteworth!. also is the presence of hypo- lo\\ the soil (Olsen method) is \.cry or moderare. The geous fungi. rivo under U. giiiiieeiisis and one under highest availa!)lr phosphorus level (17.5 pg gel) is A. africana. 'These hypogeous species are so far obsrr\.ed in the .qfze/ia nfricnnn woodland of site undescribed. They are the first records of hypogeous !Ir111. fungi in Senegal and perhaps for any tropical forest of West Africa. Only six fungi are common to both A. africana and L'. guineensis. It is, however, Sa?rip ling untimely to assess any host specificity. Sampling was carried out during the rainy season. Table 4 shows that some fungi have a wide Superficial roots were excavated, starting from the distribution in tropical Africa. The fungi of il. trunk and working towards the ultimate fine roots. africana and U.guineensis are, however, not found in Rootlets (1-5 g) were fixed in formaldehyde-acetic the Sudano-Sahelian region, where endomycorrhizal acid (FAA) (Johansen, 1940). For young seedlings trees such as Acacia spp. are dominant. They reach the whole root system was fixed. their northern limit in Senegal in the Sudano- The fine roots were examined under a dissecting Guinean region. microscope. Rootlets covered by a fungal sheath The dependence of the ectomycorrhizal fungi on were gently escised and washed under tap water. host trees is high. Thus, where A. africana or U. Freehand sections were cleared with a 20 yo sodium guineensis are absent, the ectomycorrhizal species hypochlorite solution, rinsed in water, stained with disappear and are replaced by saprophytic genera, as Congo red or toluidine blue and observed with light such Agaricus, Collybia, Coprinus, Lepiota, Leuco- or phase contrast microscopy. Roots were considered coprinus and Psathvrella. On the other hand, ecto- to be ectomycorrhizal when they had a distinctive mycorrhizal fungi are present even when the host sheath and a Hartig net. The ratio of the fungal tree (A. africana or U. guineensis) is isolated and sheath area to the total cross sectional area of root surrounded by endomycorrhizal trees. About fifty was calculated for the ECM of A. africana and of U. tree species were examined and shown to be guineensis. Fine roots were also cleared and stained endomycorrhizal. according to the procedure for VA mycorrhizas of Scleroderma vewucosum, S. dictyosporum and Ino- Phillips & Hayman (1970). Roots were considered to cybe sp. are especially abundant near seedlings of be (VA) mycorrhizal when they had intramatrical regenerating A. africana. These fungi are observed vesicles, endocellular hyphal coils and arbuscules. also under seedlings of A. africana grown in the state Sporocarps of putative ectomycorrhizal genera nursery of Djibelor close to site XII. Such seedlings were collected, dried at 40-45 "C and identified in show abundant ECM suggesting that Scleroderma the laboratory. Voucher material was deposited in verrucosum, S. dictyosporum and Inocybe sp. might be the herbarium of O.R.S.T.O.M. (Bel Air, Dakar) 'early stage' mycorrhizal fungi. and in the herbarium of the National Botanical Garden of Belgium (BR). Ectomycorrhizas Localisation of ectomycorrhizas in the soil. The ECM RESULTS Ectomycorrhizal fungi of U. guineensis are located below the litter layer between 1 and 5 cm depth. This might be correlated During the rainy season (from July to October) there to the fluctuating water level in hydromorphic soils was a great diversity of species and a great abundance and the greater oxygen availability in the topsoil. of sporocarps of putative ectomycorrhizal fungi. The ECM of 'A.africana occur at a depth of 5-20 cm Table 3 shows the species found under A. africana and are located in the mineral soil under the rooting and U.guineensis. Some species fruited after the first zone of the grasses. No Rhizobium root nodules were significant rainfall, others in the middle or at the end found on A. africana. of the rainy season. This suggests the presence of different phenological periods in different species, as Morphology of ectomycorrhizas. Several morphologi- has been observed for fungal fruiting in temperate cal types of ECM are distinguishable in the field by forests (e.g. Thoen, 1971a, b). the sheath colour and texture, pattern of ramification Figures 2 and 3 show some of the main putative and presence or absence of mycelial strands. Figure ectomycorrhizal fungi of A. africana and U. guine- 4 shows some distinctive morphological types of ~ . I* . ,Y f) FIGURE2. Host trees (a. b) and some putative ectomycorrhizal fungi of Afielia africana (c, and Uapaca guineensis (b. d- e. 8). (a) A-aficuna in the semi-deciduous forest of Kalounayes, July 1985. (b) Stilt roots of Uguineensis and Tubasacta bncnneoserosa (N Santiaba Manjak, July 1985. (c) &."a sp. (N Bayottes, July 1986. (d) 7648). 7462). 7581), hanira SP- (N Santiaba Manjak, August 1986. (e above) Mature and (e below) young Lactarius gymnocarpus sp. (N 7646). Santiaba Manjak, August 1986. (0 Russulu sp. (N 7669). Thiara. August 1986. (g) Lacrarius (N 7643). Santiaba Manjak, August 1986.

nroen and Ba (Facing p. 552) w.

FIGURE3. Some putative ectomycoW fungi of Afilia africano (a, d, e) and of Uapaca guineensis (b, C, Q.(a) Xerocomus subspinulosus (N 7540), Kalounaye~forest, July 1986@) Close-up view of Austrogautienu sp. (N 7873), Santiaba Manjak, September 19¿3%(c) Tubosaeta brunneosetosa (N 7467), Santiaba Manjak, July 1985.(d) Canrharellus pseudofiesii (N 7654). Thiara, August 1986.(e) Amanita hemibapha (N 7658). Thiara, August 1986.(f) Amanita a$rubescens (N7571),Santiaba Manjak, July 1986.

Thoen and Ba Host trees* No. of voucher Orders, species U.g. A.f. material _- -. I~oletnles l~r,l,Y~illlssp. + 7518, 7569, 7596 rld,~,tmp, EUS Heinem. + 7160, 7570 r;, , -_-/2/9, 7729 (;>.r ,do,t ini rmedius (Pat.) Sing. + 4- (;yrr,porlts n~icrosporus(Sing. & Grinl.) Heinem. 8 7613, 7635 I{arnmeloo var. congolensis (Heinem.) Heinem 8 Rammeloo 4- porphyrellus niger Heinem. & Gooss. 7875 pzdveroboletus aff. trinitensis Heinem. - 7461, 7716 Strobilomyces costatispora (Beeli) Gilb. + 7506 Trtbosaetn brunneosetosa (Sing.) Horak - 7462, 7467, 7573, 7714 rocomus om us aff. hypoxanthus Singer - 7491, 7603, 7645 .St,rt~mmusspinulosus Heinem. & Goos. + 7514 .S~,Iocomzts subspinulows Heinem. + 7489, 7493, 7540 Xgaricales Amanita cf. massiconus Bas (nom. prov.) +" 7664, 7882 Amanita hemibopha (Berk. & Br.) Sacc. 7658, 7734 S. +" Amanita aff. rubescens (Pers.: Fr.) F. Gray + 7487, 7566, 7571 Amanita sp. 1 (yellow) 7644 Amanita sp. 2 (grey brown) - 7648 .41nanitn sp. 3 (white with blueish gills) +" 7672 rltnanita sp. 4 (entirely white) +' 7674 Inocybe sp. 1 (leiosporous) +" 7657 Inocybe sp. 2 (gibbosporous) + Russulales Elasmomyces sp. (hypogeous) - 7652 Lactarius gymnocarpus Heim + 7605, 7646, 7881 Lactarius zenkeri P. Henn. . + 7702, 7885 Lactarius sp. 1 (pinkish brown) + 7618, 7643 Lactarius sp. 2 (dark brown) +" 7662 Russula annulata Heim 7606, 7647, 7878 Russula discopus Heim - 7609, 7649, 7872 ,1 Russula aff. foetens Pers. ex Fr. + 7617 Russula aff. pectinata Fr. +" 7669, 7886 Russula sp. 1 (vinaceous brown) 7519 Russula sp. 2 (yellow) + 7581, 7594, 7632 Russut sp. 3 (pinkish red) -. + 7633 Russula sp. 4 (carmin red) + 7509 Russula sp. 5 (red and ocre) + 7507 Russula sp. 6 (pruinous red) + 7580 Russula sp. 7 (cream) +" 7670 Cantharellales Cantharellus congolensis Beeli 7879 Cantharellus @seudofriesii Heinem. 7654 Aphyllophorales Coltricia cinnamomes (Pers.) Murr. -k 7859, 7883 Gautieriales 4- Autrogarieria sp. (hypogeous) 7700, 7873 Hymenogastrales Sch?astm sp. (hypogeous) +a 7660, 7701, 7861 Scleroderrnatales, 2Mm"a dictyosporum Pat. + + 7510, 7526, 7559 +"a VmUCosum Pers. - + 7508, 7522, 7560 Number of species (Total = 43) 18 31 ., Uapaca guineensis; Ad., Afzelia africana gi occurring only in site VI11 (Thiara) - I' b4 Table 4. African cfistnbiitio?r niid habita¿ of some pirtatiee ecto?trvcorrlrizalfiorgifouncf iotder .Afzelia afr

- -- andlor Uapaca guineensis in Senegal _I-^ . - - - - .-- Habitat and Species presumed host tree(*) Country(*)

~ Gantharellus congolensis Rainforest, Macrolobium Zaire Cantharellus pseudofriesii Rainforest, Macrolobium Zaïre Lactarius zenkeri Rainforest( ?) Cameroon Porphyrellus niger Rainforest, Macrolobium, Zaire Dry evergreen forest (muhulu) Strobilomyces costatispora Rainforest, Macrolobium Zaïre Xerocomus spinulosus Rainforest, Macrolobium Zaire Gyroporus microsporus Rainforest, Macrolobium Burundi, ZaTre, Zambia Woodland, Brachystegia Goltricia cinnamomea Deciduous forest Burundi, Kenya, Sierra Leone, South Africa, Zambia 1 Gyrodon cupreus Woodland( ?) Ethiopia, Kenya, Malawi, Uganda Lactarius gymnocarpus Woodland (dry forest) Cameroon, Ivory Coast, Guinea, Tanzania, Zaïre Russula annulata Woodland(**) Tanzania, Zaïre('*) Xerocomus subspinulosus Woodland Tanzania, Zaire

* Source after Heim, 1970; Heinemann, 1954, 1959, 1966; Heinemann & Rammeloo, 1983; Pegler, 1977, 1983; Ryvarden & Johansen (1980). ** Non-published observation, Thoen, 1972.

Table 5. Main characteristics of the ectomycorrhizus of Afzelia africana and Uapaca guineensis

A. africana U. guineensis (n = 10) (n = 13)

~ Range of diameter (,um) 236-466 390-640 Mean diameter (pm) 328 488 SEM* (pm) 88 79 eV** ( % 1 27 16 Range of sheath thickness (pm) 14-85 18-80 Mean sheath thickness (pm) 50 47 SEM* (pn) 24 16 cv** (%I 48 34 Range of sheath area (yo) 20-65 17-54 . Mean sheath area (yo) 50 " 35 SEM* (%I 14 9 cv** (%I 28 26 Range of radial depth of the 18-30 15-68 Hartig net (pm) Range of host tissue diameter (pm) 166-314 304-550 Mean host tissue diameter -@m) 226 393 SEM* (pm) 51 70 CV** (%I 22 18 Number of cortical cells layers 2-3 4-5 Number of protoxylem pales 2 34

* SEM: standard error of the mean; ** Coefficient of variability.

ECM. The texture of the sheath varies from entirely and the lateral roots are common (Fig. 4u). Pinnate smooth to rugose, felty, hairy-or bristly, with dull, (Fig. 4b) and monopodial ectomycorrhizas (Fig. 4c, glossy or waxy aspect. Although the cblour of the e) are also observed. Mycelial strands are present on sheath may change in ageing ECM, we have more than 60% of the ECM (Fig. 4a, c, 4. distinguished white, yellow, pink, beige, brown and In some 'cases it is possible to trace mycelial maroon ECM on U. guineensis and white, yellow, strands and 'extensive masses of loose hyphae from greyish blue, beige, brown and dark brown ECM on the base of sporocarps to the most characteristic A. africana. Both trees may bear two or more ECM. In this way, we have established for Uupuca 44. mycorrhizal types on a single root portion (Fig. guineensis connections between yellow ECM and the Racemose ECM with a sheath covering the mother hypogeous sporocarps of Austrogautieria sp. (Fig. 3 b Figure 4. Stereomicrographsof ectomycorrhizas of Uapaca guineensis (a, b) and Afzefia africana (c, d, e). (a) Cluster of bright yellow ECM formed by Austrogautieria sp., (b) Pinnate, beige ECM formed by Lactarius gymnocarfius.(c) White monopodial or poorly branched ECM. (d) White and dark brown ECM on a single root portion. (e) Close-up view of a dark brown ECM showing hairy sheath. Bar = 1mm. and Fig. 4a), pinnate, beige ECM and Lactarius Anatomy of ectomycorrhizas. Table 5 shows the main gymnocarpus (Fig. 4b), pink ECM and Amanita aff. anatomical characteristics of the ECM. The diameter rubescens, brown, bristly ECM and Coltricia cinna- of the ECM of U.guineensis is greater than that of A. a tnomea (Fig. 4e), and whitish ECM with sclero- africana. The mean value of the sheath thickness is dermic smell and Scleroderma verrucosum. Connec- the same for both species. However, as the host tions between sporocarps and the deeper located ECM tissue diameter is smaller for A. africana, its ratio of of Afdeelia africana were more difficult to establish sheath to host tissue area is greater than that of U.

"with certainty. However the link between whitish guineensis. I M of A. africana and Scleroderma verrucosum has In cross sections, Hartig net penetration is ahvays n proved. limited to epidermal cells that are in direct contact Figure 5. Ectomycorrhkas of Afielia africuna (a, b. c, d, e), endomycorrhiza (f) and ectomycorrhizas of Uupacuguineensis (g, h, i, j). (a)Transverse section through a dark brown ECM. (b)Transverse section through a yellowish ECM. (c) Transverse section through a yellow ECM. (d)Transverse section through a light brown cf) ECM. (e) Transverse section through a white ECM. Endomycorrhizal vesicle and intramatrical hyphae. (s) Transverse section through a maroon brown ECM formed by Coltriciu cinnutnomeu. (h)Transverse section through a pink ECM formed by Amunita ufl. rubescens. (i) Transverse section through a white EChl showing layering and superficial incrustations of the sheath. 6) Transverse section and longitudinal section of an emerging root showing overlapping of Hartig nets H1 and H2; same ECM as (i) Key: S, fungal sheath; Si, sheath incrustations; H, Hartig net; C, clamp connection on emerging hypha; Ep, epidermis of root; o, outer cortex of root I, inner cortex of root: E. endodermis of root; P, primary sylem of root; V. endomycorrhizal =sicle ; N, endomycorrhizal interceilular hypha. Bar = 20 pm. in temperate forests, are absent in southern Senegal. Justaposition of Hartig nets occurs when a new Several of the ectomycorrhizal fungi found under A. lateral root emerges (Fig. 513. Enlarged hyphae are africana and U. guineensis have a wide range in observed at the transition zone benveen the sheath tropical Africa. These fungi are known from miombo and the Hartig net (Fig. 5d, e, g). On Uapaca ECM, woodlands belonging to the Sudano-Zambezian epidermal cells are strikingly elongated, forming a element or rain forests belonging to the Guineo- palisade laycr. :ind are filled with brown phenolics. Congolian element (tVhite. 1965). These two forest . i,,!:dicì l.:Cl I xhrn\ less cpiclcrmal clongation (Fig. t\-pes are kno\vii to cont;iin cctoiiiycorrhizal trees So. h, l.Jand phenolics are rare or absent. Layering of (Peyronel & Fassi, 1957. 19bO: Fass¡ &I Fontana, the sheath is present in ECl[ of both tree species 1961, 1962; Högberg & Nylund, 1081; Hiigberg, (Fig. jc, i). The outer layer of the sheath is 1982; Högberg & Piearce, 1986; Alesander, 1985, sometimes incrusted with pigments (Fig. 5 i. i.). 1987; Ne\vbery et al., 1988), namely Berlinia spp., * Brnchystegia spp. and Cilbertiode?rdrr)rr spp., all trees Etitlnni~~c.nrrhic us absent in Senegal. Some fungi of .4. ofrirana and Lr. pineensis might thus be ;iblc. ro forni ECAI ivith Sr)n-ectoi.nyc.i,rrhizal roots of adult -4. ofriccina and lo\\. other tree genera. sho~viii: ii host specificity. U. griineriisis \vert. esaniined for endomycorrhizas In our plots, -4. njrirarrtr is the only Caesalpinioi (\-AM). It \vas found that U{~pacagiiirieerisis has ideae to have ECM. Other genera of this subfamily VAR4 whereas .-f. africana has not. Thus, mature (Cordyln, Daniellia, Detariuni, Eq*throphleum) that trees of Capncn guineensis may have a dual pattern of we have examined are all endomycorrhizal. Afzelia symbiosis. africana is ectomycorrhizal in all our sites, whatever the available phosphorus level of the soil and the Seed gerrtiiritrtiorl and seedling infection diversity of surrounding endomycorrhizal trees Seeds of o'. guineensis are small (10.5-14 x 7-9 mm), might be. This is consistent with previous observa- whereas those of A. africano are big (20- tions of -4lesander (1975) : ' those species [of Caesal- 29.7 x 9.3 -14.5 mm) and contain, presumably, larger pinioidene] \\.hich form ectomycorrhizas do so even amounts OF food reserves. Seeds of L;. guineensis on soils of higher P status and \\;hen they occur as germinatt. in July, at the beginning of the rainy isolated individuals in a matrix of \:.A [mycorrhizas] season, as soon as they reach the soil. Seeds of A. forming species '. africana fall in February, in the middle of the dry Fundamental questions arise as to how the ecto- season, and dormancy occurs until the rainy season. mycorrhizal propagules reach isolated individuals of Mycorrhizal infection of both species occurs very host trees and how they compete with the ubiquitous soon, even before the emergence of the first leaves. endomycorrhizal fungi ? In A. africana, translocation However, A africana is initially infected by ECM, of reserves, such as carbohydrates, from the big and whereas U.guineensis is infected by VAM. The stage fleshy cotyledbns to the roots probably allows early of development at which U. guineensis becomes ECM infection. Precocious infection might prevent ectomycorrhizal is unknown. colonization of the roots by VAM. In U. guineensis In one site, which was partially reclaimed and the seeds and the cotyledons are smaller than those converted to a pluvial rice field after burning, only a of Afielia. Endomycorrhizal fungi, requiring a lower few adult trees of A. africana remained, yet seeds carbohydrate level than the ECM (Janos, 1984) germinated and sporocarps of Scleroderma verru- colonize the roots first. Ectomycorrhizas (present on ~OSU?~occurred among the rice shoots. Germinants adult individuals) must appear later, presumably were shown to be early ectomycorrhizal. This when enough photosynthetates are transferred to the demonstrates the ability of fungal propagules to roots. Primary infection by VAM followed by ECM survive in disturbed sites or to spread from the is reported in the unrelated genera Helianthemum ectomycorrhizal mother trees. (Read, Kianmehr & Malibari, 1977), Alnus (Beddiar, 1984) and Eucalyptus (Lapeyrie & Chilvers, 1985; DISCUSSION Chilvers, Lapeyrie & Horan, 1987). It is noteworthy that these three genera all have small seeds. Adult The diversity of the putative ectomycorrhizal fungi individuals of U. guineensis bear both ECM and of Uapaca guineensis and Afzelia africana is high. It VAM, showing that dual symbiosis may be stable. is comparable to the diversity of temperate ecto- Other dual symbioses are reported for Uapaca mycorrhizal trees such as Fagus sylvatica (Thoen. staudtii, Afzelia pachyloba and Gilbertiodendron de- 1971 a, b). Among the Agarics, the mycorrhizal wevrei by Newbery et al. (1988). Dual symbiosis era Uelong to the boletes, Russula, Lactarius, might be more comm0.n than once believed and nanita and Inocybe. The same genera were re- examination of roots of only young seedlings might orded in East African forests by Pegler (1977). lead to erronous conclusions regarding the mycor- ome important mycorrhizal genera, namely Cortirr- rhizal status of a tree species. staztdtii being the other (Newbery et al., 1988). Four (Boletineae). Flore illustrée des Champignons de l'Afrique other ectomycorrhizal Uapaca spp. grow in the Centrale, Fasc. 10, 183-198, pl. 32-35. miombo woodland which has a drier environment HÖCBERC,P. (1982). Mycorrhizal associations in some woodlands and forest trees and shrubs in Tanzania. New Phytologist 92, (Redhead, 1974; Högberg, 1982; Högberg & Piearce, 407-415. 1956). H~GBERG.P. & NYLUND,J.-E. (1981). Ectomycorrhizae in coastal Some fungi such as Scleroderma z'erriicosum, miombo woodland of Tanzania. Plant and Soil 63, 283-289. S. HÖG~ERG.P. & PIEARCE,G. D. (1986). Mycorrhizas in Zambian tiict-iwporuin and Inocxbe sp. were especially com- trees in relation to host tasonomy, vegetation type and successional patterns. Journal Ecology nion under regenerating individuals of A. africana or of 74, 775-785. JANOS, P. Mycorrhizal fungi: agents or symptoms of under seedlings grown in a nursery. They belong D. (1984). tropical community composition i In: Proceedings of the 6th likely to the 'early stage fungi' (Mason et al., 1982) iYorth .4merican Conference on Mycorrhizae (Ed. by R. Molina), \\.hich are of great practical importance for nursery pp. 98-103. Forest Research Laboratory, Bend, Oregon. JESIK. J. & MENSAH,K. O. A. (1967). Root system of tropical inoculation trials. trees. I. Ectotrophic mycorrhizae of Afzelia africana Sm. iVhereas root nodules were once found on Afzelia Preslia 39. 59-65. qutitzzensis (Högberg & Nylund, 1981), they were IOHANSEN, D.A. (1940). Plant ilficrotechnique. 3IcGraw-Hill. lacking on A. africana. This is consistent with earlier Sew York. LAPEYRIE,F. F. & CHILVERS,G. A. (1385). An endomycorrhiza- observations on the same species by Jenik & Mensah ectomycorrhiza succession associated with enhanced growth of ( 1967). Eucalyptus dumosa seedlings planted in calcareous soil. New Phytologist 100, 93-104. J. MASON. P. A., LAST,F. T., PELHABI, 8E. INGLEBY, K. (1982). Ecology of some fungi associated with and ageing stand of .\ C K N O W LED G M ENTS Birches (Betula pendula and Betula pubescens). Forest Ecology \Ve are grateful to Dr P. Heinemann (National Botanical and Management 4, 19-39. XEWBERY,D. M., ALEXANDER,I. J., THOMAS,D. W. & GARTWN, Garden of Belgium, Meise) for help in identifying several S. J. (1988). Ectomycorrhizal rain-forest legumes and soil fungi and to Samboudian Dedhiou (Ziguinchor, Senegal) phosphorus in Korup National Park, Cameroon. New Phy- for help during field investigations. tologisf 109, 433-450. 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