Received: 7 December 2017 | Revised: 15 October 2018 | Accepted: 17 January 2019 DOI: 10.1111/aje.12595

ORIGINAL ARTICLE

Host and edaphic factors influence the distribution and diversity of ectomycorrhizal fungal fruiting bodies within from Tshopo, Democratic

Héritier Milenge Kamalebo1,2 | Hippolyte Nshimba Seya Wa Malale1 | Cephas Masumbuko Ndabaga3 | Léon Nsharwasi Nabahungu4 | Jérôme Degreef5,6 | André De KeseL5

1Faculté des sciences, Université de , Kisangani, D R Congo Abstract 2Centre de Recherches Universitaires du Ectomycorrhizal fungi constitute an important component of forest ecosystems that Kivu (CERUKI)/ISP, Bukavu, D R Congo enhances nutrition and resistance against stresses. Diversity of ectomycorrhi‐ 3Faculté des sciences, Université Officielle de Bukavu, Bukavu, D R Congo zal (EcM) fungi is, however, affected by host plant diversity and soil heterogeneity. 4International Institute of Tropical This study provides information about the influence of host plants and soil resources Agriculture, IITA‐Kalambo, Bukavu, D R on the diversity of ectomycorrhizal fungal fruiting bodies from rainforests of the Congo Democratic Republic of the Congo. Based on the presence of fungal fruiting bodies, 5Meise Botanic Garden, Meise, Belgique 6Fédération Wallonie‐Bruxelles, Service significant differences in the number of ectomycorrhizal fungi species existed be‐ Général de l’Enseignement Supérieur et de tween forest stand types (p < 0.001). The most ectomycorrhizal species‐rich forest la Recherche Scientifique, Brussels, Belgium was the Gilbertiodendron dewevrei‐dominated forest (61 species). Of all 93 species of Correspondence ectomycorrhizal fungi, 19 demonstrated a significant indicator value for particular Héritier Milenge Kamalebo, Faculté des sciences, Université de Kisangani, Kisangani, forest stand types. Of all analysed edaphic factors, the percentage of silt particles D R Congo. was the most important parameter influencing EcM fungi host plant distribution. Email:[email protected] Both host and edaphic factors strongly affected the distribution and diversity Funding information of EcM fungi. EcM fungi may have developed differently their ability to successfully Centre for International Forestry Research; Belgian Federal Science Policy Office colonise root systems in relation to the availability of nutrients. Résumé Dans les forêts, les champignons ectomycorrhiziens sont impliqués dans la nutrition et la protection des plantes hôtes contre les pathogènes. Leur diversité est influencée par la composition floristique et les facteurs édaphiques. Cette étude traite de l’influence des plantes hôtes et des facteurs édaphiques sur la diversité des sporo‐ phores des champignons ectomycorrhiziens dans les forêts denses de la République Démocratique du Congo. Se basant sur la présence de leurs sporophores, on note l’existence des différences significatives entre le nombre d’espèces de champignons ectomycorrhiziens dans les différents types des forêts (P<0.001). La forêt à Gilbertiodendron dewevrei se révèle la plus riche en espèces (61 espèces). Sur un total de 93 espèces de champignons ectomycorrhiziens, 19 sont inféodées aux types particuliers de forêts. La teneur en particules limoneuses est le paramètre édaphique

Afr J Ecol. 2019;57:247–259. wileyonlinelibrary.com/journal/aje © 2019 John Wiley & Sons Ltd | 247 248 | MILENGE KAMALEBO et al.

ayant plus d’influence sur la distribution des arbres hôtes des champignons. Le dével‐ oppement de la forêt à laurentii et les espèces des champignons ecto‐ mycorrhiziens associées étaient principalement influencé par la teneur en phosphore, alors que le développement des forêts dominées par Gilbertiodendron dewevrei, Uapaca guineensis et Julbernardia seretii était influencé par la teneur en particules sablonneuses. L’acidité aluminique, la teneur en particules limoneuses ainsi que la teneur en particules argileuses sont les paramètres ayant plus d’influence sur la présence des sporophores des champignons ectomycorrhiziens associés à Uapaca heudelotii. Les champignons ectomycorrhiziens ont probablement développé des ap‐ titudes particulières lesquelles leur ont permis de coloniser les systèmes racinaires, en relation avec les ressources minérales disponibles.

KEYWORDS Congo basin, Ectomycorrhizal fungi, indicator species, rainforests, soil texture

1 | INTRODUCTION Kasongo, & Degreef, 2017; Härkönen et al., 2015; Piepenbring, 2015). Mycorrhizae constitute important symbiotic associations be‐ Local environmental factors may also affect EcM fungal diver‐ tween particular groups of fungi and roots of some plant species sity (Berruti et al., 2011; Brundrett, 2009; Burke, Lopez‐Gutiérrez, (Leguminosae, Phyllanthaceae, Gnetaceae and Dipterocarpaceae fami‐ & Chan, 1993; Fortin et al., 2008; Kernaghan, 2005). In tropical for‐ lies) in tropical (Bâ, Duponnois, Diabaté, & Dreyfus, 2011; Eyi‐ ests, local‐scale biotic and abiotic factors including soil properties Ndong, Degreef, & De Kesel, 2011; Härkönen, Niemelä, Kotiranta, & and soil type play important roles in influencing the distribution of Pierce, 2015; Piepenbring, 2015; Yorou & Kesel 2011). The mutualis‐ both plant and fungal communities. EcM fungal communities are tic relation between plants and fungi plays a key role in the function‐ mainly affected by the diversity of host trees and the heterogene‐ ing of natural ecosystems, especially in nutrient cycling (Miyamoto, ity of soil resources (Berruti et al., 2011; Brundrett, 2009; Burke, Nakano, Hattori, & Nara, 2006; Peay, Kennedy, & Bruns, 1962; Smith Lopez‐Gutiérrez, & Chan, 2009). Moreover, species of EcM fungi et al., 2013; Smith, Jakobsen, Grønlund, & Smith, 2011; Tedersoo et can colonise diverse hosts and plant species can host several fungal al., 2014). Mycorrhizae enhance plant nutrition (especially phospho‐ species. rus and nitrogen), and increase a plants’ productivity and resistance Several studies (Bâ, Duponnois, Moyersoen, Duponnois, against stresses (Kernaghan, 2005; Miyamoto, Nakano, Hattori, & Moyersoen, & Diédhiou, 2011; Buyck, Buyck, Thoen, & Walting, Nara, 2014). In return, the mycorrhizal fungi benefit from photosyn‐ 1996; Ducousso, Bâ, & Thoen, 2003; Eyi‐Ndong et al., 2011; thetically derived carbohydrates made by the host plant (Alisson, Härkönen et al., 2015) have reported that, in tropical Africa, EcM Hanson, & Treseder, 2007; Kernaghan, 2005; Miyamoto et al., 2014). fungi are mainly distributed throughout the Guineo‐Congolian Plants develop several types of mycorrhizae with fungal species. basin rainforests, in the Zambezian Miombo woodlands of Eastern The most common and important are the arbuscular mycorrhizae and South central Africa, and in the Sudanian savannah woodlands. (AM) and the ectomycorrhizae (EcM) (Piepenbring, 2015). The ar‐ Furthermore, the semi‐deciduous rainforests of the Tshopo prov‐ buscular mycorrhizae penetrate root cells (Blakcwell, 2011; Berruti ince, part of the central African Congolese basin, host several spe‐ et al., 2011; Fortin, Plenchette, & Piché, 2008), while ectomycorrhi‐ cies of EcM trees (Bartholomew, Meyer, & Laudelout, 1999; White, zae develop widespread mycelial networks surrounding root tissues 1983) and are mainly dominated by Gilbertiodendron dewevrei (De in soil. In contrast to AM, EcM fungi develop aboveground fruiting Wild.) J. Léonard, Brachystegia laurentii (De Wild.) Louis, Julbernardia bodies, called sporocarps, and are mainly hosted by woody plant seretii (De Wild.) Troupin, Uapaca guineensis Mull. Arg. and U. heu‐ species (Fortin et al., 2008; Kernaghan, 2005; Piepenbring, 2015). delotii Baillon (Lejoly, Ndjele, & Geerinck, 2010; Vleminckx, 2014; The EcM fungal communities constitute an important component of White, 1983). Several other ectomycorrhizal trees (Afzelia bipin‐ many central African forests (Eyi‐Ndong et al., 2011) and play key densis Harms, Anthonotha macrophylla P. Beauv., Berlinia grandiflora roles in biogeochemical cycles, plant community dynamics and the (Vahl.) Hutch. & Dalz., etc.) occur in various mixed forests (Lejoly et maintenance of soil structure. Furthermore, as EcM fungi include a al., 2010; White, 1983). wide range of edible species, they constitute an important source of Despite the widespread distribution of this type and food and income for local populations (Berruti et al., 2011; De Kesel, the roles played by EcM fungi in these forests, no study on the MILENGE KAMALEBO et al. | 249 relation between EcM fungi function, their host plants and soil prop‐ is mainly characterised by semi‐deciduous rainforests dominated erties exist from the rainforests of Tshopo. Yet, the assessment of by G. dewevrei, Scorodophloeus zenkeri Harms, balsamifera ecological patterns of EcM fungi is vital in enhancing conservation (Vermoesen) Breteler and J. seretii (Lejoly et al., 2010; Vleminckx et of both fungal communities and their host plants. The analysis of al., 2014; White, 1983). the relation between EcM fungi, host plant trees and soil is also vital As part of the equatorial region, the Tshopo province is charac‐ in the process of assisted cultivation of ectomycorrhizal plants and terised by a rainy and hot climate, typical of the Af type according EcM fungi inoculation. Thus, this study aims to analyse the impacts to Köppen (1923). The climate is characterised by monthly average of soil resources on the diversity and distribution of EcM fungi and temperature between 22.4 and 29.3°C, and annual average of 25°C. their host trees within rainforests of the Yoko and the bio‐ The annual rainfall ranges from 1,600 to 2,200 mm with an aver‐ sphere reserve from the province of Tshopo. age of 1828 mm (Mohymont & Demarée, 2008). Rainfall is irreg‐ ularly distributed yearly with a little precipitation from December to February, and a long rainy season interrupted by two small dry 2 | MATERIALS AND METHODS seasons, from December to January and from June to August (Mohymont & Demarée, 2008). 2.1 | Study site

The study sites are located in the Tshopo province of the Democratic 2.2 | Sampling plots, fungal data Republic of Congo. The mycological data were collected within collection and analysis rainforests of the biosphere reserve of Yangambi (0°51′01.62′′N; 24°31′43.53′′E) and within rainforests of Yoko reserve (0°17′34.9′′N; 2.2.1 | EcM fungi collection and identification 25°18′27.4′′E) (Figure 1). The biosphere reserve of Yangambi is located in territory, more than 100 km West of Kisangani. Data have been collected from March to May in 2015 and 2016, The Yoko site is located in the Ubundu territory 32 km south‐east which correspond to the main mushroom fruiting season. The fungal of Kisangani. Apart from the widespread mixed forests, the region inventory involved six forest stand types (mixed forests and forests

FIGURE 1 Location of the study site [Colour figure can be viewed at wileyonlinelibrary.com] 250 | MILENGE KAMALEBO et al.

TABLE 1 List and distribution of EcM plant trees (+:present, −:absent),), (P1 = Brachystegia laurentii‐dominated forest, P2 = Gilbertiodendron dewevrei‐dominated forest, P3 = Julbernardia serretii forest, P4 = Mixed forest, P5 = Uapaca guineensis‐dominated forests and P6 = U. heudelotii‐dominated forest)

Forest types

Family EcM Trees P1 P2 P3 P4 P5 P6

Fabaceae Afzelia bipindensis Harms − − − + − − Anthonotha macrophylla P. Beauv − − − + − − Aphanocalyx cynometroides Oliver − + − − − − Berlinia grandiflora (Vahl) Hutch. & Dalz. − + − − − − Brachystegia laurentii (De Wild.) Louis + − − − − − Gilbertiodendron dewevrei (De Wild.) J. Léonard − + − − − − Julbernardia seretii (De Wild.) Troupin − − + + + − Paramacrolobium coeruleum (Taub.) J. Léonard − + − + − − Paramacrolobium sp. + − − − − − Pericopsis elata (Harms) Van Meeuwen − − − + − − Phyllanthaceae Uapaca guineensis Mull. Arg − − − + + − Uapaca heudelotii Baillon − − − − − +

dominated, respectively, by G. dewevrei, B. laurentii, J. serretii, U. heu‐ 2.2.2 | Soil sampling and analysis delotii and U. guineensis). The mixed forests host several ectomycor‐ rhizal trees such as A. bipindensis, A. macrophylla, Paramacrolobium Composite soil samples have been taken within each plot at 0 to coeruleum (Taub.) J. Léonard and Pericopsis elata (Harms) Van 30 cm depth using a bucket soil auger. Soil samples were packed in

Meeuwen (Table 1). plastic bags for laboratory analysis. From each soil sample, pH (H20, Plots (100 × 100 m each) divided into 20 × 20 m grids were de‐ 1:2.5), mineral nutrient (nitrogen, phosphorus, potassium and car‐ marcated in each forest type, except in U. heudelotii forest in which bon) and exchangeable cations (H+, Al3+, Ca2+ and Mg2+) were meas‐ plots were less than 100 × 100 m due to the limited distribution ured. Extractable nitrogen (N) was assessed by Kjeldahl procedure (20 × 50 m). In each plot, analysed data were exclusively based on while Olsen extract method was used for exchangeable potassium the presence/absence of the harvested aboveground ectomycorrhi‐ (K) and extractable phosphorus (P). The total organic carbon (C) zal fungal fruiting bodies (Table 2). In the field, some macroscopic was measured calorimetrically (Anderson & Ingram, 1993). The soil features (habitus; stipe, cap and hymenophore characteristics) were particle size analysis was measured hygrometrically (Motsara & Roy, assessed. 2015). The Kruskal–Wallis test was used to assess the difference be‐ Spore prints were preserved, and sporocarps were dried for fur‐ tween soil parameters. ther microscopic analysis. A voucher collection and collected spore prints were deposited at the Herbarium of Meise Botanic Garden (BR) 2.2.3 | Statistical analyses in Belgium. Microscopic study consisted in examining the pileipellis, basidia, cystidia and spores (ornamentation and size). Taxonomic To examine the relative influence of soil type and host plant species reference studies for tropical Africa (Buyck, ; De Kesel et al., 2017; on ectomycorrhizal fungal species assembly, we used permANOVA Eyi‐Ndong et al., 2011; Heim, 1955; Heinemann, 1954; Heinemann analysis (10,000 permutations) (Anderson, 2001). The ordination & Rammeloo, 1983, 1987, 1989; Verbeken & Walleyn, 2010) have analysis with R software involved the non‐metric multidimensional been used for species identification. Names of fungal species and scaling (NMDS) (Clarke & Gorley, 2013). The hierarchical analysis author's abbreviations were annotated using the Index Fungorum was used to cluster plots based on their mycological similarity while database (http://www.indexfungorum.org/Names/Names.asp, EcM fungal species accumulation curves were performed using Accessed 12 Nov 2017). All unidentified species but identified to Excel software. The Indicator species analysis (Indval) performed the genus level were numbered and indicated “sp.” Fungal species with the indicspecies package of R software was used to determine richness was calculated as the number of fungal species collected indicator species for each forest stand type (De Cáceres, 2002). For from each type of forest (Baptista, Martins, & Tavares, 1953; Caiafa, each indicator species, probability of both fidelity and occurrence Gomez‐Hernandez, Williams‐Linera, & Ramírez‐Cruz, 2006; Hueck, were calculated. The fidelity concerns the exclusive membership of 1951). The diversity of ectomycorrhizal fungi based on species rich‐ fungal species to a particular forest stand type, while the occurrence ness was determined using the Shannon (H) index (Fisher, Corbet, & probability indicates the frequency or preference of fungal species Williams, 1943). to plots of a given type of forest. MILENGE KAMALEBO et al. | 251

TABLE 2 List of recorded EcM fungi and their occurrence within forests (+: present; −: absent), (P1 = Gilbertiodendron dewevrei‐dominated forest, P2 = Brachystegia laurentii‐dominated forest, P3 = Mixed forest, P4 = Julbernardia serretii forest, P5 = Uapaca guineensis‐dominated forests and P6 = U. heudelotii‐dominated forest.)

Forest stand types

Family Species P1 P2 P3 P4 P5 P6

Amanitaceae Amanita annulatovaginata Beeli + − − − − − Amanita calopus Rammeloo & Walleyn + − − − − − Amanita echinulata Beeli + − − − − − Amanita fibrilosa Beeli + − − − − − Amanita pudica (Beeli) Walleyn + − − − − − Amanita robusta Beeli − + − − − − Amanita sp + − − − − − Amanita sp1 + − − − − − Amanita sp2 + − − − − − Amanita sp3 + − − − − − Amanita sp4 + − − − − − Amanita sp5 + − − − − − Amanita sp6 + − − − − − Aphelaria sp1 − − + − − − Phylloporus ater (Beeli) Heinem − + − − − − Phylloporus sp − + − − − − Phylloporus testaceus Heinem&Gooss.‐Font + − − − − − Pulveroboletus annulatus Heinem + − − − − − Pulveroboletus rufobadius (Bres.) Singer + − − − − − Rubinoboletus luteopurpureus (Beeli) + − − − − − Strobilomyces echinatus Beeli + − − − − − Tylopilus balloui (Peck) Singer − + − − − − Tylopilus beeli Heinem. & Gooss.‐Font + − − − − − Tylopilus niger (Heinem. & Gooss.−Font.) Wolfe + − − − − − Tylopilus sp1 − + − − − − Tylopilus violaceus Heinem + − − − − − Tylopilus virens (W.F. Chiu) Hongo + − − − − − Tylopilus sp2 + − − − − − Cantharellaceae Cantharellus congolensis Beeli + − − − − − Cantharellus conspicuus Eyssart., Buyck & Verbeken + − − − − − Cantharellus densifolius Heinem. + − − − − − Cantharellus incarnatus (Beeli) Heinem. − − − + − − Cantharellus isabellinus Heinem. + − − − − − Cantharellus longisporus Heinem. + − − ‐ − − Cantharellus luteopunctatus (Beeli) Heinem. + − − − − − Cantharellus miniatescens Heinem. + + − − − − Cantharellus pseudofriesii Heinem. − + − − − − Cantharellus ruber Heinem. − + − − − − Cantharellus rufopunctatus (Beeli) Heinem − + − − − − Cantharellus sp 1 − − − + − − Cantharellus sp2 − − − − + − Cantharellus sp3 + − − − − − Cantharellus sp4 + − − + + − Cantharellus sp5 + − − ‐ − − Cantharellus sp6 + ‐ − − ‐ − (countinues) 252 | MILENGE KAMALEBO et al.

TABLE 2 (Continued)

Forest stand types

Family Species P1 P2 P3 P4 P5 P6

Clavariaceae Scytinopogon angulisporus (Pat.) Corner + + + − − − Cortinariaceae Telamonia sp1 + − − − − − Telamonia sp2 + − − − − − Telamonia sp3 + − − − − − Telamonia sp4 + − − − − − Gomphaceae Gomphus brunneus (Heinem.) Corner − + + + + − Inocybaceae Inocybe sp1 − + − − − − Paxillaceae Paxillus brunneotomentosus Heinem. & Rammeloo − − + − − − acutus R. Heim + + − − − − Lactarius saponaceus Verbeken + − − − − − Lactarius sp1 − − − − + − Lactarius sp2 + − − − − − Lactarius sp3 + − − − − − Lactarius sp4 − − − − − + Lactarius sp5 − − − − − + Lactarius sp6 − − − − − + Lactifluus annulatoangustifolius (Beeli) Buyck + − − − − − Lactifluus gymnocarpus (R. Heim ex Singer) Verbeken + − − − + − Lactifluus heimi (Verbeken) Verbeken − − − − − + Lactifluus pelliculatus (Beeli) Buyck + − ‐ − − − Russula annulata R. Heim − + − − − − Russula declinata Buyck + − − − − − Russula inflata Buyck + − − − − − Russula meleagris Buyck − + + − − − Russula porphyrocephala Buyck − + − − − − Russula pruinata Buyck + − − − − − Russula pseudocarmesina Buyck + − − − − − Russula roseostriata Buyck − + − − − − Russula roseovelata Buyck − + − − − − Russula sese Beeli − + + − − − Russula sesemoindu Beeli − − + − − − Russula sp1 + − − − − − Russula sp2 − + − − − − Russula sp3 − + − − − − Russula sp4 + − − − − − Russula sp5 + − − − − − Russula sp6 + − − − − − Russula sp7 + − − − − + Russula sp8 + − − − − + Russula sp9 − − − − − + Russula striatoviridis Buyck + − − − − − Russula testacea Buyck + − − − − − Russula viridrobusta Buyck − + − − − − Thelephoraceae Thelephora palmata (Scop.) Fr. − + − − − − Xerocomaceae Xerocomus sp1 + − − − − − Xerocomus sp2 + − − − − − Xerocomus sp3 + − − − − − Xerocomus spinulosus Heinem. & Gooss.‐Font + − − − − − MILENGE KAMALEBO et al. | 253

FIGURE 2 Distribution of the numbers of EcM species within forest stand types (MIX: Mixed forests; GIL, Gilbertiodendron dewevrei‐dominated forests; BRA: Brachystegia laurentii‐dominated forests; JUL: Julbernardia seretii‐dominated forests, Uapaca guineensis‐dominated forests, Uapaca heudelotii‐dominated forests)

70 MIX reported in J. seretii‐dominated forest (total species number = 4, GIL 60 Shannon index value = 1.38). The Russulaceae was the most repre‐

r BRA 50 JUL sentative family of EcM fungi (35 species), followed by Cantharellaceae UAPG 40 (18 species), Boletaceae (14 species) and Amanitaceae (13 species). UAPH Whereas the number of EcM fungi significantly differed be‐ 30 tween forest types, the species cumulative curve (Figure 3) revealed 20 different patterns of species richness within plots. The highest cu‐ EcM species numbe 10 mulative species richness was demonstrated in G. dewevrei‐domi‐ 0 nated forests, followed by B. laurentii‐dominated forests. Plots from 0123 Plots mixed forests, J. seretii forests and Uapaca spp.‐dominated forests exhibited low variation in the number of EcM fungi. FIGURE 3 EcM species cumulative curve according to forest stand types (MIX: Mixed forests; GIL: Gilbertiodendron dewevrei‐ dominated forests; BRA: Brachystegia laurenti‐dominated forests; 3.1.2 | Fungal species assemblages and JUL: Forests dominated by Julbernardia seretii; UAPG: Uapaca indicator species guineensis‐dominated forests; UAPH: Uapaca heudelotii‐dominated forests) [Colour figure can be viewed at wileyonlinelibrary.com] The composition of vascular plants prominently influenced EcM fungi species assemblages and composition. Clustering of plots based on the composition in EcM fungi is strongly correlated with 3 | RESULTS forest stand types (Figure 4). Apart from a few common species, each forest stand type is characterised by its own EcM diversity. 3.1 | Diversity and distribution of ectomycorrhizal However, one plot of J. seretii‐dominated forest was clustered with (EcM) fungi within forest stand types mixed forests as some common species of EcM fungi occurred in the two types of forest stands. 3.1.1 | Species richness Of all 93 recorded taxa, 19 species of EcM fungi demonstrated A total of 93 taxa of EcM fungi were recorded in six different for‐ a significant indicator value for a particular forest stand type est stands. Among them, 54 were determined to species level and (Table 3). The highest number of indicator species was demon‐ 39 to the genus level. Significant differences were observed in the strated for the B. laurentii‐dominated forests (7 species), the U. heu‐ number of EcM fungi between forest stand types (Figure 2) (p‐value delotii‐dominated forest (6 species) and the forest dominated by <0.001). The Shannon diversity index revealed that the G. dewevrei‐ G. dewevrei (5 species) whereas the U. guineensis‐dominated forest dominated forest was the most species‐rich forest stand (total species and the B. laurentii–G. dewevrei combined forest both have only number = 61, Shannon index value = 4.11). The second most species‐ one indicator species. No species of EcM fungi was demonstrated rich forest stand was the B. laurentii‐dominated forest (total species as indicator for J. seretii and other mixed forests. Based on their oc‐ number = 24, Shannon index value = 3.17), followed by the U. heu‐ currence and fidelity probability, all indicator species of B. lauren‐ delotii‐dominated forest (total species number = 7, Shannon index tii forest revealed strong preference (100% occurrence) whereas value = 1.94) and the mixed forests (total species number = 7, Shannon only 4 of them demonstrated 100% fidelity. The all five indicator index value = 1.94). The lowest number of EcM fungal species was species of G. dewevrei‐dominated forest were exclusively faithful 254 | MILENGE KAMALEBO et al.

FIGURE 4 Hierarchical clustering of plots referring to the mycological similarity [Colour figure can be viewed at wileyonlinelibrary.com]

(100% fidelity) and demonstrated strong preference (100% occur‐ (NMDS) ordination (Figure 5) demonstrated that G. dewevrei‐ and rence). In U. heudelotii forests, all indicator species were faithful U. heudelotii‐dominated forests are mostly promoted by particle whereas only four of them demonstrated strong preference with size of clay and silt, and the content in organic C, N and extract‐ 100% occurrence. able K. Furthermore, the hydrogen acidity, the exchangeable Ca, Several other species of EcM fungi, even reported faithful to the available Mg, the pH and the percentage of sand particles are some specific forest stands, were described as rare species (p‐value the most important edaphic parameters that promote B. laurentii‐, <0.05) occurring rarely in single plots. This is the case of numer‐ J. seretii‐ and U. guineensis‐dominated forests. Correlation between ous species of the genus Amanita and Russula sporadically found in the edaphic factors and forest stand types, demonstrated that the G. dewevrei‐ and B. laurentii‐dominated forests. soil properties that are mainly ordinated with a given type of for‐ est had prominent influence on the diversity of both EcM fungi and host plant trees (Figure 5). 3.2 | Variability in soil types and properties within The first axis ordinated forest stands based mainly on soil type. forest stands All types of forest (B. laurentii‐dominated forest, G. dewevrei‐dom‐ Most of edaphic factors clearly differed between the forest types inated forest and J. seretii forest) developed on sandy soil were (Table 4). Significant differences existed for extractable phosphorus grouped together while only U. heudelotii on clayey soil is sepa‐ content (p‐value = 0.005), sand particles size (p‐value = 0.037), clay rated. The second axis ordinated forest stands based mainly on soil particles (p‐value = 0.024), exchangeable Ca (p‐value = 0.015), soil acidity. Forests growing on soil characterised by hydrogen acidity C (p‐value = 0.033) as well as available N (p‐value = 0.004). In addi‐ were ordinated together, whereas forests of soil characterised by Al tion, the forests dominated by B. laurentii, G. dewevrei and J. seretii acidity formed separate ordination. However, the diversity of each are characterised by a sandy loam soil while U. guineensis and U. heu‐ forest stand and associated EcM fungal community were differently delotii forests are respectively characterised by loamy sand and influenced by soil properties. The NMDS analysis showed that the clayey soils. sustainability of B. laurentii‐dominated forest and its associated EcM Although soil properties clearly differ between forest stands, fungi was mainly promoted by the content in extractable P. Fungi the PERMANOVA analysis revealed that the silt particle size re‐ and host plants from G. dewevrei, U. guineensis and J. seretii forests mains the most important soil parameter that has prominent in‐ were influenced primarily by hydrogen acidity, exchangeable Ca, fluence on the diversity of both EcM fungi and host plant trees available Mg, pH and the percentage of sand particles. Furthermore, (Table 5). However, the non‐metric multidimensional scaling Al acidity, total N, C, K and content of silt and clay were the most MILENGE KAMALEBO et al. | 255

TABLE 3 Values of the indicator EcM Probability Indicator value (Indval) species analysis for the studied forest Indicator EcM stands N° species Fidelity Occurrence Indval p‐value

Brachystegia laurentii‐dominated forest 1 Cantharellus ruber 1.0000 1.000 1.000 ** 2 Cantharellus 1.0000 1.000 1.000 ** rufopunctatus 3 Russula roseostriata 1.0000 1.000 1.000 ** 4 Thelephora palmata 1.0000 1.000 1.000 ** 5 Russula meleagris 0.8333 1.000 0.913 ** 6 Russula sese 0.8333 1.000 0.913 ** 7 Cantharellus 0.7500 1.000 0.866 * miniatescens Uapaca heudelotii‐dominated forest 1 Lactifluus heimi 1.00 1.00 1.000 ** 2 Lactarius sp.4 1.00 1.00 1.000 ** 3 Lactarius sp.5 1.00 1.00 1.000 ** 4 Lactarius sp.6 1.00 1.00 1.000 ** 5 Russula sp.7 0.75 1.00 0.866 * 6 Russula sp.8 0.75 1.00 0.866 * Gilbertiodendron dewevrei‐dominated forest 1 Cantharellus 1.000 1.000 1.000 ** congolensis 2 Lactarius sp.2 1.000 1.000 1.000 ** 3 Rubinoboletus 1.000 1.000 1.000 ** luteopurpureus 4 Strobilomyces 1.000 1.000 1.000 ** echinatus 5 Tylopilus beeli 1.000 1.000 1.000 ** Uapaca guineensis‐dominated forest 1 Cantharellus sp.2 1.0000 1.0000 1.000 ** Brachystegia laurentii+Gilbertiodendron dewevrei‐dominated forests 1 Lactarius acutus 1.0000 0.6667 0.816 * *p‐value <0.05: Significant difference. **p‐value <0.01: Highly significant difference. important edaphic parameters influencing the presence of EcM to adapt to the local edaphic conditions enabling them to successfully fungi associated with U. heudelotii. colonise plant roots throughout these forest types (Berruti et al., 2011; Brundrett, 2009; Burke et al., 2009). In addition, the forests dominated by G. dewevrei and B. laurentii were the most EcM species‐rich forest 4 | DISCUSSION stands, as previously recorded by Eyi‐Ndong et al. (2011) from lowland rainforest in . This can be explained by the fact that B. laurentii 4.1 | EcM fungi diversity and distribution within and G. dewevrei forest stands are the most widely distributed EcM trees forest stands in the Congo basin (White, 1983). G. dewevrei and B. laurentii should The composition and distribution of EcM fungal fruiting bodies var‐ have developed capacities to host several EcM fungi in local edaphic ied significantly with host tree distribution. In all forest types, the conditions. As previously reported from diverse tropical forests (Bâ et families Russulaceae and Cantharellaceae dominate, as previously re‐ al., 2010; Burke et al., 2009; Eyi‐Ndong et al., 2011; Khasa, Furlan, & ported by Eyi‐Ndong et al. (2011) for the Central African rainforests, Lumande, 1990; Yorou & Kesel, 2011), EcM host trees in Tshopo belong Buyck, Gomez‐Hernandez, Williams‐Linera, and Ramírez‐Cruz (2017) exclusively to the families and Phyllanthaceae. and Bâ, Duponnois, Moyersoen, and Diédhiou (2010) for the savan‐ Referring to the results of indicator species analysis, numer‐ nah woodlands of Western Africa and Buyck (1997), Härkönen et al. ous species of EcM fungi have demonstrated strong preference, (2015) and De Kesel et al. (2017) for the Miombo woodlands. Species even fidelity, to specific habitats. This is the case of Cantharellus of Cantharellaceae and Russulaceae should have developed capacities ruber, C. rufopunctatus, Russula roseostriata, Thelephora palmata, 256 | MILENGE KAMALEBO et al. ‐ for

‐dominated

NS NS * ** * NS * Kruskal–Wallis NS * * NS ** p‐value Uapaca guineensis Uapaca

UAPG: SD Matter; 0,15 ± 0,07 0,59 ± 0,02 1,32 ± 0,32 4,36 ± 0,21 1,58 ± 0,40 0,46 ± 0,03 8,03 ± 0,47 0,22 ± 0,02 10,72 ± 2,84 45,42 ± 12,74 12,62 ± 3,12 43,87 ± 9,91 UAPH Mean ± Mean Clay 2,3 6 Organic OM: forest;

SD ± 0,059,60 0,52 ± 0,18 0,52 ± 0,20 0,07 ± 0,06 2,39 ± 0,18 3,39 ± 1,15 0,58 ± 0,11 0,06 ± 0,04 4,40 ± 0,09 1,00 ± 0,08 83,07 ± 1,15 13,54 ± 1,16 UAPG Mean ± Mean Loamy sand Loamy 0,9 9 Julbernardia serretii Julbernardia

JUL:

SD forest,

± 0,443,11 ± 0,000,10 0,47 ± 0,10 0,67 ± 0,08 0,69 ± 0,09 4,31 ± 0,09 3,39 ± 1,15 0,63 ± 0,12 0,04 ± 0,02 ± 1,3316,98 81,07 ± 1,15 JUL 15,54 ± 1,15 Mean ± Mean Sandy loam Sandy 0,8 12 ‐dominated ) SD SD ± 0,57 9,10 ± 0,000,10 ± 0,154,13 ± 0,260,96 0,59 ± 0,21 0,81 ± 0,19 0,57 ± 0,10 2,32 ± 0,65 3,39 ± 1,63 0,08 ± 0,01 80,73 ± 2,66 15,88 ± 1,67 GIL Mean ± Mean Sandy loam Sandy 1,4 10 Gilbertiodendrondewevrei

GIL:

‐value <0.01: Highly significant difference. p forest;

SD ± 0,361,41 ± 0,060,13 0,51 ± 0,08 0,71 ± 0,12 0,67 ± 0,14 2,72 ± 0,00 1,07 ± 0,12 4,33 ± 0,13 0,08 ± 0,03 ± 2,3179,07 18,21 ± 2,31 Mean ± Mean BRA Sandy loam Sandy 30,37 ± 7,05 1,2 9 ‐dominated ‐dominated forest; NS: Not significant. heudelotii Brachystegia laurentii Brachystegia (cmol/kg) (cmol/kg) . The two last columns indicate P‐value and the significance level of the Kruskal–Wallis test.

3+ + ‐value <0.05: significant difference. ** pH N (µg/g) Ca (cmol/kg) C (µg/g) Mg (cmol/kg) Clay (%) H Edaphic factors Edaphic type Soil P (µg/g) Sand (%) Silt (%) K (µg/g) OM Al C/N ratio p TABLE 4 MeanTABLE values of edaphic parameters ±Standard deviation ( Note BRA: ests; UAPH: U. * MILENGE KAMALEBO et al. | 257

TABLE 5 Results of the correlation between edaphic factors 4 with the PERMANOVA analysis 0.

NMDS1 NMDS2 r2 p‐value pH Ca Al 0.96097 0.27665 0.7859 NS .2 UAPG JUL H −0.79070 0.61221 0.2814 NS H Silt Al pH −0.06851 0.99765 0.5112 NS 2 Clay UAPH 00 DS Mg

N 0.99233 −0.12361 0.7778 NS 0.

NM N C 0.87762 −0.47935 0.8560 NS Sand Ca −0.28578 0.95830 0.3388 NS C

.2 BRA Mg −0.99890 0.04687 0.4112 NS P K –0 GIL Clay 0.99231 0.12382 0.7146 NS Sand −0.98303 −0.18345 0.7446 NS .4

Silt 0.92701 0.37503 0.8495 * –0 K 0.59450 −0.80410 0.3661 NS –0.4 –0.2 0.00.2 0.40.6 P −0.74898 −0.66259 0.6262 NS NMDS1 Note. NS: Not significant. *p‐value <0.05: Significant difference. FIGURE 5 The non‐metric multidimensional scaling (NMDS) ordination showing the relative influence of edaphic factors on EcM fungi host plant trees maintenance [Colour figure can be viewed at R. meleagris, R. sese and C. miniatescens exclusively found in B. lau‐ wileyonlinelibrary.com] rentii‐dominated forests. Likewise, C. congolensis, Rubinoboletus luteopurpureus, Strobilomyces echinatus and Tylopilus beeli were in‐ 2008) that reported that high concentrations of exchangeable Al dicator species for G. dewevrei‐dominated forest while Lactifluus reduce the availability of P in soil and should negatively affect the heimi characterised the U. heudelotii forests. Furthermore, development of EcM fungi (Burke et al., 2009; Neffar et al., 2008). Lactarius acutus characterised both the G. dewevrei‐ and B. lauren‐ Furthermore, the high content of available P in B. laurentii forests tii‐dominated forests. might explain that tree roots are strongly involved in the minerali‐ As reported by Yorou and De Kesel (2011), the greatest danger sation of P along with the N collected from the atmosphere (Berruti facing EcM fungi relate to the threat; facing their habitat and their et al., 2011; Brundrett, 2009; Burke et al., 2009). Nevertheless, it host plant trees. Furthermore, the rarity expressed in the number of should be noted that, although the survey of fruiting bodies gives fungal locations and their habitat areas are the main criteria to be information about the EcM fungal composition and diversity, such used for EcM fungi‐based IUCN status classification. Thereby, due studies do not necessarily reflect the overall EcM fungi community to the rapid loss of biodiversity in natural ecosystems, the establish‐ composition. Some of EcM fungi do not or rarely produce fruiting ment of IUCN status of various rare and endangered species of EcM bodies due to incompatible combinations that do not enable their fungi from rainforests of Tshopo is of great importance. mycelial network to produce fruiting structure (Berruti et al., 2011; Brundrett, 2009; Kernaghan, 2005). Furthermore, the natural pro‐ duction of aboveground fruiting bodies requires much more bio‐ 4.2 | Edaphic factors promoting both EcM fungi and logical energy by host plants and depends on available nutrients host trees sustainability and fungal biological capacities (Berruti et al., 2011; Neffar et al., The analysis of edaphic factors indicated many differences existing 2008). between soil characteristics of the investigated forests. Three dif‐ In comparison with the non‐mycorrhizal mountain forests from ferent soil types were characterised based on the soil particles size. the Albertine rift characterised by volcanic soil rich in mineral nu‐ The G. dewevrei, B. laurentii and J. seretii forests occurred on sandy trient (Bernaert, 2014; Pécrot et al., 1962), rainforests in Yangambi loam soil, while U. guineensis and U. heudelotii develop on loamy sand and Yoko developed mainly on poor sandy soil (Alongo, Visser, and clayey soil. Furthermore, the soil nutrient content and proper‐ Kombele, Colinet, & Bogaert, 2013; Bartholomew et al., 1999; ties vary significantly among forests. And, of these, available P was Gilson, Wambeke, & Gutzwiller, 1956). Previous studies (Berruti also negatively correlated to Al content. Moreover, the forests de‐ et al., 2011; Brundrett, 2009; Neffar et al., 2008) revealed that veloped on a sandy soil (characterised by high level of hydrogen acid‐ mycorrhizae occur mainly in poor soils, such as soils from EcM‐ ity and high P content) (G. dewevrei and B. laurentii forests) hosted a dominated forests of Yangambi and Yoko (Alongo et al., 2013; higher number of EcM fungi than the U. heudelotii forest found on Bartholomew et al., 1999; Gilson et al., 1956). EcM fungi, there‐ clayey soil (where the acidity is based on Al content). fore, enhance the biological fixation of atmospheric nitrogen in These findings are in line with several other studies (Burke et al., soil and control the mineralisation of other nutrients along with 1993; Hazelton & Murphy, 2007; Neffar, Beddiar, & Chenghouni, the available nitrogen. 258 | MILENGE KAMALEBO et al.

5 | CONCLUSION ORCID

Héritier Milenge Kamalebo https://orcid. This study gives basic information on the diversity and distribution org/0000-0002-9232-9801 pattern of EcM fungal fruiting bodies within the biosphere reserve of Yangambi and the forest reserve of Yoko. A total of 93 ectomyc‐ orrhizal fungal taxa were recorded, among which 19 species showed REFERENCES preference for particular forest stands. Regarding the impact of soil, Alisson, S. D., Hanson, C. A., & Treseder, K. K. (2007). Nitrogen fertiliza‐ it was shown that edaphic factors differently affect the distribution tion reduces diversity and alters community structure of active fungi and diversity of EcM fungi. The B. laurentii plant tree and its associ‐ in boreal ecosystems. 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