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

Received:7December2017  |  Revised:15October2018  |  Accepted:17January2019DOI:10.1111/aje.12595

O R I G I N A L A R T I C L E

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

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

1Facultédessciences,UniversitédeKisangani,Kisangani,DRCongo2CentredeRecherchesUniversitairesduKivu(CERUKI)/ISP,Bukavu,DRCongo3Facultédessciences,UniversitéOfficielledeBukavu,Bukavu,DRCongo4InternationalInstituteofTropicalAgriculture,IITA‐Kalambo,Bukavu,DRCongo5MeiseBotanicGarden,Meise,Belgique6FédérationWallonie‐Bruxelles,ServiceGénéraldel’EnseignementSupérieuretdelaRechercheScientifique,Brussels,Belgium

CorrespondenceHéritierMilengeKamalebo,Facultédessciences,UniversitédeKisangani,Kisangani,DRCongo.Email:kamaleboheritier@gmail.com

Funding informationCentreforInternationalForestryResearch;BelgianFederalSciencePolicyOffice

AbstractEctomycorrhizalfungiconstituteanimportantcomponentofforestecosystemsthatenhancesplantnutritionandresistanceagainststresses.Diversityofectomycorrhi‐zal(EcM)fungiis,however,affectedbyhostplantdiversityandsoilheterogeneity.Thisstudyprovidesinformationabouttheinfluenceofhostplantsandsoilresourceson the diversity of ectomycorrhizal fungal fruiting bodies from rainforests of theDemocraticRepublicoftheCongo.Basedonthepresenceoffungalfruitingbodies,significantdifferences in thenumberofectomycorrhizal fungi speciesexistedbe‐tweenforeststandtypes(p<0.001).Themostectomycorrhizalspecies‐richforestwastheGilbertiodendron dewevrei‐dominatedforest(61species).Ofall93speciesofectomycorrhizal fungi,19demonstrateda significant indicatorvalue forparticularforeststandtypes.Ofallanalysededaphicfactors,thepercentageofsiltparticleswasthemostimportantparameterinfluencingEcMfungihostplanttreedistribution.BothhosttreesandedaphicfactorsstronglyaffectedthedistributionanddiversityofEcMfungi.EcMfungimayhavedevelopeddifferentlytheirabilitytosuccessfullycoloniserootsystemsinrelationtotheavailabilityofnutrients.

RésuméDanslesforêts,leschampignonsectomycorrhizienssontimpliquésdanslanutritionetlaprotectiondesplanteshôtescontrelespathogènes.Leurdiversitéestinfluencéepar la composition floristique et les facteurs édaphiques. Cette étude traite del’influencedesplanteshôtesetdesfacteursédaphiquessurladiversitédessporo‐phoresdeschampignonsectomycorrhiziensdanslesforêtsdensesdelaRépubliqueDémocratiqueduCongo.Sebasantsur laprésencede leurssporophores,onnotel’existencedesdifférencessignificativesentrelenombred’espècesdechampignonsectomycorrhiziens dans les différents types des forêts (P<0.001). La forêt àGilbertiodendrondewevrei se révèle laplus richeenespèces (61espèces).Suruntotalde93espècesdechampignonsectomycorrhiziens,19sontinféodéesauxtypesparticuliersdeforêts.Lateneurenparticuleslimoneusesestleparamètreédaphique

248  |     MILENGE KAMALEBO Et AL.

1  | INTRODUC TION

Mycorrhizae constitute important symbiotic associations be‐tween particular groups of fungi and roots of some plant species(Leguminosae,Phyllanthaceae,Gnetaceae and Dipterocarpaceaefami‐lies)intropicalAfrica(Bâ,Duponnois,Diabaté,&Dreyfus,2011;Eyi‐Ndong,Degreef,&DeKesel,2011;Härkönen,Niemelä,Kotiranta,&Pierce,2015;Piepenbring,2015;Yorou&Kesel2011).Themutualis‐ticrelationbetweenplantsandfungiplaysakeyroleinthefunction‐ingofnaturalecosystems,especiallyinnutrientcycling(Miyamoto,Nakano,Hattori,&Nara,2006;Peay,Kennedy,&Bruns,1962;Smithetal.,2013;Smith,Jakobsen,Grønlund,&Smith,2011;Tedersooetal.,2014).Mycorrhizaeenhanceplantnutrition(especiallyphospho‐rusandnitrogen),andincreaseaplants’productivityandresistanceagainst stresses (Kernaghan, 2005;Miyamoto,Nakano,Hattori, &Nara,2014).Inreturn,themycorrhizalfungibenefitfromphotosyn‐thetically derived carbohydratesmade by the host plant (Alisson,Hanson,&Treseder,2007;Kernaghan,2005;Miyamotoetal.,2014).

Plantsdevelopseveraltypesofmycorrhizaewithfungalspecies.Themost common and important are the arbuscularmycorrhizae(AM) and the ectomycorrhizae (EcM) (Piepenbring, 2015). The ar‐buscularmycorrhizaepenetraterootcells(Blakcwell,2011;Berrutietal.,2011;Fortin,Plenchette,&Piché,2008),whileectomycorrhi‐zaedevelopwidespreadmycelialnetworkssurroundingroottissuesinsoil. IncontrasttoAM,EcMfungidevelopabovegroundfruitingbodies, called sporocarps, and aremainly hosted bywoody plantspecies (Fortinetal.,2008;Kernaghan,2005;Piepenbring,2015).TheEcMfungalcommunitiesconstituteanimportantcomponentofmanycentralAfrican forests (Eyi‐Ndongetal.,2011)andplaykeyrolesinbiogeochemicalcycles,plantcommunitydynamicsandthemaintenanceofsoilstructure.Furthermore,asEcMfungiincludeawiderangeofediblespecies,theyconstituteanimportantsourceoffoodandincomeforlocalpopulations(Berrutietal.,2011;DeKesel,

Kasongo, & Degreef, 2017; Härkönen et al., 2015; Piepenbring,2015).

LocalenvironmentalfactorsmayalsoaffectEcMfungaldiver‐sity(Berrutietal.,2011;Brundrett,2009;Burke,Lopez‐Gutiérrez,&Chan,1993;Fortinetal.,2008;Kernaghan,2005).Intropicalfor‐ests,local‐scalebioticandabioticfactorsincludingsoilpropertiesandsoiltypeplayimportantrolesininfluencingthedistributionofboth plant and fungal communities. EcM fungal communities aremainlyaffectedbythediversityofhosttreesandtheheterogene‐ityofsoil resources (Berrutietal.,2011;Brundrett,2009;Burke,Lopez‐Gutiérrez,&Chan,2009).Moreover, speciesofEcM fungicancolonisediversehostsandplantspeciescanhostseveralfungalspecies.

Several studies (Bâ, Duponnois, Moyersoen, Duponnois,Moyersoen, & Diédhiou, 2011; Buyck, Buyck, Thoen, & Walting,1996; Ducousso, Bâ, & Thoen, 2003; Eyi‐Ndong et al., 2011;Härkönenet al., 2015) have reported that, in tropicalAfrica, EcMfungi are mainly distributed throughout the Guineo‐Congolianbasinrainforests, intheZambezianMiombowoodlandsofEasternandSouthcentralAfrica,andintheSudaniansavannahwoodlands.Furthermore, the semi‐deciduous rainforests of the Tshopo prov‐ince,partofthecentralAfricanCongolesebasin,hostseveralspe‐ciesofEcMtrees(Bartholomew,Meyer,&Laudelout,1999;White,1983) and aremainly dominated byGilbertiodendron dewevrei (De Wild.)J.Léonard,Brachystegia laurentii (DeWild.)Louis,Julbernardia seretii (DeWild.)Troupin,Uapaca guineensisMull.Arg. andU. heu‐delotii Baillon (Lejoly,Ndjele, &Geerinck, 2010; Vleminckx, 2014;White, 1983). Several other ectomycorrhizal trees (Afzelia bipin‐densisHarms,Anthonotha macrophyllaP.Beauv.,Berlinia grandiflora (Vahl.)Hutch.&Dalz.,etc.)occurinvariousmixedforests(Lejolyetal.,2010;White,1983).

Despitethewidespreaddistributionofthisrainforesttypeandthe roles played by EcM fungi in these forests, no study on the

ayantplusd’influencesurladistributiondesarbreshôtesdeschampignons.Ledével‐oppementdelaforêtàBrachystegialaurentiietlesespècesdeschampignonsecto‐mycorrhiziensassociéesétaientprincipalementinfluencéparlateneurenphosphore,alors que le développement des forêts dominées par Gilbertiodendron dewevrei,UapacaguineensisetJulbernardiaseretiiétait influencéparlateneurenparticulessablonneuses. L’acidité aluminique, la teneur en particules limoneuses ainsi que lateneur en particules argileuses sont les paramètres ayant plus d’influence sur laprésence des sporophores des champignons ectomycorrhiziens associés àUapacaheudelotii.Leschampignonsectomycorrhiziensontprobablementdéveloppédesap‐titudesparticulièreslesquellesleurontpermisdecoloniserlessystèmesracinaires,enrelationaveclesressourcesminéralesdisponibles.

K E Y W O R D S

Congobasin,Ectomycorrhizalfungi,indicatorspecies,rainforests,soiltexture

     |  249MILENGE KAMALEBO Et AL.

relationbetweenEcMfungifunction,theirhostplantsandsoilprop‐ertiesexistfromtherainforestsofTshopo.Yet,theassessmentofecologicalpatternsofEcMfungi isvital inenhancingconservationof both fungal communities and their host plants. The analysis oftherelationbetweenEcMfungi,hostplanttreesandsoilisalsovitalintheprocessofassistedcultivationofectomycorrhizalplantsandEcMfungiinoculation.Thus,thisstudyaimstoanalysetheimpactsofsoilresourcesonthediversityanddistributionofEcMfungiandtheirhosttreeswithinrainforestsoftheYokoandtheYangambibio‐spherereservefromtheprovinceofTshopo.

2  | MATERIAL S AND METHODS

2.1 | Study site

ThestudysitesarelocatedintheTshopoprovinceoftheDemocraticRepublic of Congo. The mycological data were collected withinrainforests of the biosphere reserve of Yangambi (0°51′01.62′′N;24°31′43.53′′E)andwithinrainforestsofYokoreserve(0°17′34.9′′N;25°18′27.4′′E) (Figure 1). The biosphere reserve of Yangambi islocated in Isangi territory, more than 100kmWest of Kisangani.TheYokosite is located intheUbunduterritory32kmsouth‐eastofKisangani.Apartfromthewidespreadmixedforests,theregion

is mainly characterised by semi‐deciduous rainforests dominatedby G. dewevrei, Scorodophloeus zenkeri Harms, Prioria balsamifera (Vermoesen)BretelerandJ. seretii(Lejolyetal.,2010;Vleminckxetal.,2014;White,1983).

Aspartoftheequatorialregion,theTshopoprovinceischarac‐terisedbyarainyandhotclimate,typicaloftheAftypeaccordingtoKöppen(1923).Theclimateischaracterisedbymonthlyaveragetemperaturebetween22.4and29.3°C,andannualaverageof25°C.The annual rainfall ranges from1,600 to 2,200mmwith an aver‐age of 1828mm (Mohymont & Demarée, 2008). Rainfall is irreg‐ularly distributed yearlywith a little precipitation fromDecembertoFebruary,anda long rainyseason interruptedby twosmalldryseasons, from December to January and from June to August(Mohymont&Demarée,2008).

2.2 | Sampling plots, fungal data collection and analysis

2.2.1 | EcM fungi collection and identification

Data have been collected fromMarch toMay in 2015 and 2016,whichcorrespondtothemainmushroomfruitingseason.Thefungalinventoryinvolvedsixforeststandtypes(mixedforestsandforests

F I G U R E 1  Locationofthestudysite[Colourfigurecanbeviewedatwileyonlinelibrary.com]

250  |     MILENGE KAMALEBO Et AL.

dominated,respectively,byG. dewevrei, B. laurentii, J. serretii, U. heu‐delotii and U. guineensis).Themixedforestshostseveralectomycor‐rhizal trees such asA. bipindensis,A. macrophylla,Paramacrolobium coeruleum (Taub.) J. Léonard and Pericopsis elata (Harms) VanMeeuwen(Table1).

Plots(100×100meach)dividedinto20×20mgridswerede‐marcatedineachforesttype,exceptinU. heudelotiiforestinwhichplots were less than 100×100m due to the limited distribution(20×50m). Ineachplot,analyseddatawereexclusivelybasedonthepresence/absenceoftheharvestedabovegroundectomycorrhi‐zal fungal fruitingbodies (Table2). In the field, somemacroscopicfeatures(habitus;stipe,capandhymenophorecharacteristics)wereassessed.

Sporeprintswerepreserved,andsporocarpsweredriedforfur‐thermicroscopicanalysis.AvouchercollectionandcollectedsporeprintsweredepositedattheHerbariumofMeiseBotanicGarden(BR)inBelgium.Microscopicstudyconsistedinexaminingthepileipellis,basidia, cystidia and spores (ornamentation and size). TaxonomicreferencestudiesfortropicalAfrica(Buyck,;DeKeseletal.,2017;Eyi‐Ndongetal.,2011;Heim,1955;Heinemann,1954;Heinemann&Rammeloo,1983,1987,1989;Verbeken&Walleyn,2010)havebeenused for species identification.Namesof fungal speciesandauthor's abbreviationswere annotated using the Index Fungorumdatabase (http://www.indexfungorum.org/Names/Names.asp,Accessed 12Nov 2017). All unidentified species but identified tothegenus levelwerenumberedand indicated “sp.”Fungal speciesrichnesswascalculatedas thenumberof fungal speciescollectedfromeachtypeofforest(Baptista,Martins,&Tavares,1953;Caiafa,Gomez‐Hernandez,Williams‐Linera,&Ramírez‐Cruz,2006;Hueck,1951).Thediversityofectomycorrhizalfungibasedonspeciesrich‐nesswasdeterminedusingtheShannon(H)index(Fisher,Corbet,&Williams,1943).

2.2.2 | Soil sampling and analysis

Composite soil samples have been takenwithin each plot at 0 to30cmdepthusingabucketsoilauger.Soilsampleswerepackedinplasticbagsforlaboratoryanalysis.Fromeachsoilsample,pH(H20,1:2.5),mineral nutrient (nitrogen, phosphorus, potassium and car‐bon)andexchangeablecations(H+,Al3+,Ca2+andMg2+)weremeas‐ured.Extractablenitrogen(N)wasassessedbyKjeldahlprocedurewhileOlsenextractmethodwasusedforexchangeablepotassium(K) and extractable phosphorus (P). The total organic carbon (C)wasmeasuredcalorimetrically(Anderson&Ingram,1993).Thesoilparticlesizeanalysiswasmeasuredhygrometrically(Motsara&Roy,2015).TheKruskal–Wallistestwasusedtoassessthedifferencebe‐tweensoilparameters.

2.2.3 | Statistical analyses

Toexaminetherelativeinfluenceofsoiltypeandhostplantspeciesonectomycorrhizalfungalspeciesassembly,weusedpermANOVAanalysis (10,000 permutations) (Anderson, 2001). The ordinationanalysiswithRsoftwareinvolvedthenon‐metricmultidimensionalscaling (NMDS) (Clarke & Gorley, 2013). The hierarchical analysiswasusedtoclusterplotsbasedontheirmycologicalsimilaritywhileEcM fungal species accumulation curves were performed usingExcel software. The Indicator species analysis (Indval) performedwiththeindicspeciespackageofRsoftwarewasusedtodetermineindicatorspeciesforeachforeststandtype(DeCáceres,2002).Foreach indicator species, probabilityofboth fidelity andoccurrencewerecalculated.Thefidelityconcernstheexclusivemembershipoffungalspeciestoaparticularforeststandtype,whiletheoccurrenceprobabilityindicatesthefrequencyorpreferenceoffungalspeciestoplotsofagiventypeofforest.

TA B L E 1  ListanddistributionofEcMplanttrees(+:present,−:absent),),(P1=Brachystegia laurentii‐dominatedforest,P2=Gilbertiodendron dewevrei‐dominatedforest,P3=Julbernardia serretiiforest,P4=Mixedforest,P5=Uapaca guineensis‐dominatedforestsandP6=U. heudelotii‐dominatedforest)

Family EcM Trees

Forest types

P1 P2 P3 P4 P5 P6

Fabaceae Afzelia bipindensisHarms − − − + − −

Anthonotha macrophyllaP.Beauv − − − + − −

Aphanocalyx cynometroidesOliver − + − − − −

Berlinia grandiflora(Vahl)Hutch.&Dalz. − + − − − −

Brachystegia laurentii(DeWild.)Louis + − − − − −

Gilbertiodendron dewevrei(DeWild.)J.Léonard − + − − − −

Julbernardia seretii(DeWild.)Troupin − − + + + −

Paramacrolobium coeruleum(Taub.)J.Léonard − + − + − −

Paramacrolobiumsp. + − − − − −

Pericopsis elata(Harms)VanMeeuwen − − − + − −

Phyllanthaceae Uapaca guineensisMull.Arg − − − + + −

Uapaca heudelotiiBaillon − − − − − +

     |  251MILENGE KAMALEBO Et AL.

TA B L E 2  ListofrecordedEcMfungiandtheiroccurrencewithinforests(+:present;−:absent),(P1=Gilbertiodendron dewevrei‐dominatedforest,P2=Brachystegia laurentii‐dominatedforest,P3=Mixedforest,P4=Julbernardia serretiiforest,P5=Uapaca guineensis‐dominatedforestsandP6=U. heudelotii‐dominatedforest.)

Family Species

Forest stand types

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 − − + − − −

Boletaceae 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.

Family Species

Forest stand types

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 − − + − − −

Russulaceae Lactarius 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.HeimexSinger)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 + − − − − −

TA B L E 2   (Continued)

     |  253MILENGE KAMALEBO Et AL.

3  | RESULTS

3.1 | Diversity and distribution of ectomycorrhizal (EcM) fungi within forest stand types

3.1.1 | Species richness

A total of 93 taxa of EcM fungiwere recorded in six different for‐est stands. Among them, 54were determined to species level and39 to the genus level. Significant differenceswere observed in thenumberofEcMfungibetweenforeststandtypes(Figure2)(p‐value<0.001).TheShannondiversity indexrevealedthat theG. dewevrei‐dominatedforestwasthemostspecies‐richforeststand(totalspeciesnumber=61,Shannonindexvalue=4.11).Thesecondmostspecies‐rich foreststandwas theB. laurentii‐dominated forest (total speciesnumber=24, Shannon index value=3.17), followed by the U. heu‐delotii‐dominated forest (total species number=7, Shannon indexvalue=1.94)andthemixedforests(totalspeciesnumber=7,Shannonindex value=1.94). The lowest number of EcM fungal specieswas

reported in J. seretii‐dominated forest (total species number=4,Shannon index value=1.38). The Russulaceae was themost repre‐sentativefamilyofEcMfungi(35species),followedbyCantharellaceae (18species),Boletaceae(14species)andAmanitaceae(13species).

Whereas the number of EcM fungi significantly differed be‐tweenforesttypes,thespeciescumulativecurve(Figure3)revealeddifferentpatternsofspeciesrichnesswithinplots.Thehighestcu‐mulative species richness was demonstrated inG. dewevrei‐domi‐natedforests,followedbyB. laurentii‐dominatedforests.Plotsfrommixed forests, J. seretii forestsandUapaca spp.‐dominated forestsexhibitedlowvariationinthenumberofEcMfungi.

3.1.2 | Fungal species assemblages and indicator species

The composition of vascular plants prominently influenced EcMfungi species assemblages and composition. Clustering of plotsbasedonthecomposition inEcMfungi isstronglycorrelatedwithforest stand types (Figure 4). Apart from a few common species,each forest stand type is characterised by its own EcM diversity.However,oneplotofJ. seretii‐dominatedforestwasclusteredwithmixedforestsassomecommonspeciesofEcMfungioccurredinthetwotypesofforeststands.

Ofall93recordedtaxa,19speciesofEcMfungidemonstrateda significant indicator value for a particular forest stand type(Table 3). The highest number of indicator species was demon‐stratedfortheB. laurentii‐dominatedforests(7species),theU. heu‐delotii‐dominated forest (6 species) and the forest dominated byG. dewevrei(5species)whereastheU. guineensis‐dominatedforestand the B. laurentii–G. dewevrei combined forest both have onlyoneindicatorspecies.NospeciesofEcMfungiwasdemonstratedasindicatorforJ. seretiiandothermixedforests.Basedontheiroc‐currenceandfidelityprobability,all indicatorspeciesofB. lauren‐tii forest revealed strong preference (100%occurrence)whereasonly4ofthemdemonstrated100%fidelity.Theall five indicatorspecies ofG. dewevrei‐dominated forestwere exclusively faithful

F I G U R E 2  DistributionofthenumbersofEcMspecieswithinforeststandtypes(MIX:Mixedforests;GIL,Gilbertiodendron dewevrei‐dominatedforests;BRA:Brachystegia laurentii‐dominatedforests;JUL:Julbernardia seretii‐dominatedforests,Uapaca guineensis‐dominatedforests,Uapaca heudelotii‐dominatedforests)

F I G U R E 3  EcMspeciescumulativecurveaccordingtoforeststandtypes(MIX:Mixedforests;GIL:Gilbertiodendron dewevrei‐dominatedforests;BRA:Brachystegia laurenti‐dominatedforests;JUL:ForestsdominatedbyJulbernardia seretii;UAPG:Uapaca guineensis‐dominatedforests;UAPH:Uapaca heudelotii‐dominatedforests)[Colourfigurecanbeviewedatwileyonlinelibrary.com]

0

10

20

30

40

50

60

70

0 1 2 3

EcM

spec

ies n

umbe

r

Plots

MIX

GIL

BRA

JUL

UAPG

UAPH

254  |     MILENGE KAMALEBO Et AL.

(100%fidelity)anddemonstratedstrongpreference(100%occur‐rence). InU. heudelotii forests, all indicator species were faithfulwhereasonly fourof themdemonstratedstrongpreferencewith100%occurrence.

Several other species of EcM fungi, even reported faithful tosomespecificforeststands,weredescribedasrarespecies(p‐value<0.05) occurring rarely in single plots. This is the case of numer‐ousspeciesofthegenusAmanita and RussulasporadicallyfoundinG. dewevrei‐ and B. laurentii‐dominatedforests.

3.2 | Variability in soil types and properties within forest stands

Mostofedaphic factorsclearlydifferedbetweenthe forest types(Table4).Significantdifferencesexistedforextractablephosphoruscontent(p‐value=0.005),sandparticlessize(p‐value=0.037),clayparticles (p‐value=0.024), exchangeable Ca (p‐value=0.015), soilC(p‐value =0.033)aswellasavailableN(p‐value =0.004).Inaddi‐tion, the forestsdominatedbyB. laurentii, G. dewevrei and J. seretii arecharacterisedbyasandyloamsoilwhileU. guineensis and U. heu‐delotii forests are respectively characterised by loamy sand andclayeysoils.

Although soil properties clearly differ between forest stands,the PERMANOVA analysis revealed that the silt particle size re‐mains the most important soil parameter that has prominent in‐fluence on the diversity of both EcM fungi and host plant trees(Table 5). However, the non‐metric multidimensional scaling

(NMDS) ordination (Figure 5) demonstrated thatG. dewevrei‐ and U. heudelotii‐dominated forests are mostly promoted by particlesizeof clayandsilt, and thecontent inorganicC,Nandextract‐able K. Furthermore, the hydrogen acidity, the exchangeable Ca,theavailableMg,thepHandthepercentageofsandparticlesarethemost importantedaphicparametersthatpromoteB. laurentii‐,J. seretii‐ and U. guineensis‐dominatedforests.Correlationbetweentheedaphicfactorsandforeststandtypes,demonstratedthatthesoilpropertiesthataremainlyordinatedwithagiventypeoffor‐esthadprominentinfluenceonthediversityofbothEcMfungiandhostplanttrees(Figure5).

Thefirstaxisordinatedforeststandsbasedmainlyonsoiltype.All types of forest (B. laurentii‐dominated forest,G. dewevrei‐dom‐inated forest and J. seretii forest) developed on sandy soil weregrouped together while only U. heudelotii on clayey soil is sepa‐rated.Thesecondaxisordinatedforeststandsbasedmainlyonsoilacidity. Forests growingon soil characterised by hydrogen aciditywereordinatedtogether,whereasforestsofsoilcharacterisedbyAlacidityformedseparateordination.However,thediversityofeachforeststandandassociatedEcMfungalcommunityweredifferentlyinfluencedbysoilproperties.TheNMDSanalysisshowedthatthesustainabilityofB. laurentii‐dominatedforestanditsassociatedEcMfungiwasmainlypromotedby thecontent inextractableP.FungiandhostplantsfromG. dewevrei,U. guineensis and J. seretii forestswere influenced primarily by hydrogen acidity, exchangeable Ca,availableMg,pHandthepercentageofsandparticles.Furthermore,Alacidity,totalN,C,Kandcontentofsiltandclaywerethemost

F I G U R E 4  Hierarchicalclusteringofplotsreferringtothemycologicalsimilarity[Colourfigurecanbeviewedatwileyonlinelibrary.com]

     |  255MILENGE KAMALEBO Et AL.

important edaphic parameters influencing the presence of EcMfungiassociatedwithU. heudelotii.

4  | DISCUSSION

4.1 | EcM fungi diversity and distribution within forest stands

The composition and distribution of EcM fungal fruiting bodies var‐ied significantly with host tree distribution. In all forest types, thefamiliesRussulaceae and Cantharellaceae dominate, as previously re‐portedbyEyi‐Ndongetal. (2011)fortheCentralAfricanrainforests,Buyck,Gomez‐Hernandez,Williams‐Linera,andRamírez‐Cruz (2017)andBâ,Duponnois,Moyersoen, andDiédhiou (2010) for the savan‐nahwoodlandsofWesternAfricaandBuyck (1997),Härkönenetal.(2015)andDeKeseletal.(2017)fortheMiombowoodlands.SpeciesofCantharellaceae and Russulaceaeshouldhavedevelopedcapacities

toadapttothelocaledaphicconditionsenablingthemtosuccessfullycoloniseplantrootsthroughouttheseforesttypes(Berrutietal.,2011;Brundrett,2009;Burkeetal.,2009).Inaddition,theforestsdominatedby G. dewevrei and B. laurentiiwerethemostEcMspecies‐richforeststands,aspreviouslyrecordedbyEyi‐Ndongetal.(2011)fromlowlandrainforestinGabon.ThiscanbeexplainedbythefactthatB. laurentii and G. dewevrei foreststandsarethemostwidelydistributedEcMtreesin theCongobasin (White, 1983).G. dewevrei and B. laurentii shouldhavedevelopedcapacitiestohostseveralEcMfungiinlocaledaphicconditions.Aspreviouslyreportedfromdiversetropicalforests(Bâetal.,2010;Burkeetal.,2009;Eyi‐Ndongetal.,2011;Khasa,Furlan,&Lumande,1990;Yorou&Kesel,2011),EcMhosttreesinTshopobelongexclusivelytothefamiliesFabaceae and Phyllanthaceae.

Referring to the results of indicator species analysis, numer‐ous species of EcM fungi have demonstrated strong preference,evenfidelity, tospecifichabitats.This is thecaseofCantharellus ruber, C. rufopunctatus, Russula roseostriata, Thelephora palmata,

TA B L E 3  ValuesoftheindicatorEcMspeciesanalysisforthestudiedforeststands N°

Indicator EcM species

Probability Indicator value (Indval)

Fidelity Occurrence Indval p‐value

Brachystegia laurentii‐dominatedforest

1 Cantharellus ruber 1.0000 1.000 1.000 ** 

2 Cantharellus rufopunctatus

1.0000 1.000 1.000 ** 

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 miniatescens

0.7500 1.000 0.866 * 

Uapaca heudelotii‐dominatedforest

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‐dominatedforest

1 Cantharellus congolensis

1.000 1.000 1.000 ** 

2 Lactarius sp.2 1.000 1.000 1.000 ** 

3 Rubinoboletus luteopurpureus

1.000 1.000 1.000 ** 

4 Strobilomyces echinatus

1.000 1.000 1.000 ** 

5 Tylopilus beeli 1.000 1.000 1.000 ** 

Uapaca guineensis‐dominatedforest

1 Cantharellussp.2 1.0000 1.0000 1.000 ** 

Brachystegia laurentii+Gilbertiodendron dewevrei‐dominatedforests

1 Lactarius acutus 1.0000 0.6667 0.816 * 

*p‐value<0.05:Significantdifference.**p‐value<0.01:Highlysignificantdifference.

256  |     MILENGE KAMALEBO Et AL.

TAB

LE 4

 Meanvaluesofedaphicparameters±Standarddeviation(S

D)

Edap

hic

fact

ors

BRA

GIL

JUL

UA

PGU

APH

Kru

skal

–Wal

lis

Mea

n ±S

DM

ean

±SD

Mea

n ±S

DM

ean

±SD

Mea

n ±S

Dp‐

valu

e

Al3+(cmol/kg)

1,07±0,12

0,96±0,26

0,63±0,12

1,00±0,08

12,62±3,12

* 

H+ (cmol/kg)

0,51±0,08

0,57±0,10

0,67±0,08

0,52±0,18

0,46±0,03

NS

pH4,33±0,13

4,13±0,15

4,31±0,09

4,40±0,09

4,36±0,21

NS

N(µg/g)

0,08±0,03

0,08±0,01

0,04±0,02

0,06±0,04

0,22±0,02

** 

C(µg/g)

0,71±0,12

0,81±0,19

0,47±0,10

0,52±0,20

1,32±0,32

* 

Ca(cmol/kg)

1,41±0,36

2,32±0,65

3,11±0,44

2,39±0,18

1,58±0,40

* 

Mg(cmol/kg)

0,67±0,14

0,59±0,21

0,69±0,09

0,58±0,11

0,59±0,02

NS

Clay(%)

18,21±2,31

15,88±1,67

15,54±1,15

13,54±1,16

43,87±9,91

* 

Sand(%)

79,07±2,31

80,73±2,66

81,07±1,15

83,07±1,15

45,42±12,74

* 

Silt(%)

2,72±0,00

3,39±1,63

3,39±1,15

3,39±1,15

10,72±2,84

NS

K(µg/g)

0,13±0,06

0,10±0,00

0,10±0,00

0,07±0,06

0,15±0,07

NS

P(µg/g)

30,37±7,05

9,10±0,57

16,98±1,33

9,60±0,05

8,03±0,47

** 

Soil

type

Sand

y lo

amSa

ndy

loam

Sand

y lo

amLo

amy

sand

Clay

OM

1,2

1,4

0,8

0,9

2,3

C/Nratio

910

129

6

Not

e.ThetwolastcolumnsindicateP‐valueandthesignificanceleveloftheKruskal–Wallistest.

BRA:B

rach

yste

gia

laur

entii‐dominatedforest;GIL:G

ilber

tiode

ndro

n de

wev

rei‐dominatedforest,JUL:J

ulbe

rnar

dia

serr

etiiforest;OM:OrganicMatter;UAPG:U

apac

a gu

inee

nsis‐dominatedfor‐

ests;UAPH:U

. heu

delo

tii‐dominatedforest;NS:Notsignificant.

*p‐value<0.05:significantdifference.**p‐value<0.01:Highlysignificantdifference.

     |  257MILENGE KAMALEBO Et AL.

R. meleagris, R. sese and C. miniatescensexclusivelyfoundinB. lau‐rentii‐dominated forests. Likewise, C. congolensis, Rubinoboletus luteopurpureus, Strobilomyces echinatus and Tylopilus beeli were in‐dicator species forG. dewevrei‐dominated forest while Lactifluus heimi characterised the U. heudelotii forests. Furthermore,Lactarius acutuscharacterisedboththeG. dewevrei‐ and B. lauren‐tii‐dominatedforests.

AsreportedbyYorouandDeKesel(2011),thegreatestdangerfacingEcMfungirelatetothethreat;facingtheirhabitatandtheirhostplanttrees.Furthermore,therarityexpressedinthenumberoffungal locationsandtheirhabitatareasarethemaincriteria tobeusedforEcMfungi‐basedIUCNstatusclassification.Thereby,duetotherapidlossofbiodiversityinnaturalecosystems,theestablish‐mentofIUCNstatusofvariousrareandendangeredspeciesofEcMfungifromrainforestsofTshopoisofgreatimportance.

4.2 | Edaphic factors promoting both EcM fungi and host trees sustainability

Theanalysisofedaphicfactorsindicatedmanydifferencesexistingbetweensoilcharacteristicsof the investigated forests.Threedif‐ferentsoiltypeswerecharacterisedbasedonthesoilparticlessize.TheG. dewevrei,B. laurentii and J. seretii forestsoccurredonsandyloamsoil,whileU. guineensis and U. heudelotiideveloponloamysandandclayeysoil.Furthermore,thesoilnutrientcontentandproper‐tiesvarysignificantlyamongforests.And,ofthese,availablePwasalsonegativelycorrelatedtoAlcontent.Moreover,theforestsde‐velopedonasandysoil(characterisedbyhighlevelofhydrogenacid‐ityandhighPcontent)(G. dewevrei and B. laurentiiforests)hostedahighernumberofEcMfungithantheU. heudelotii forestfoundonclayeysoil(wheretheacidityisbasedonAlcontent).

Thesefindingsareinlinewithseveralotherstudies(Burkeetal.,1993;Hazelton&Murphy,2007;Neffar,Beddiar,&Chenghouni,

2008)thatreportedthathighconcentrationsofexchangeableAlreducetheavailabilityofPinsoilandshouldnegativelyaffectthedevelopmentofEcMfungi(Burkeetal.,2009;Neffaretal.,2008).Furthermore,thehighcontentofavailablePinB. laurentiiforestsmightexplainthattreerootsarestronglyinvolvedintheminerali‐sationofPalongwiththeNcollectedfromtheatmosphere(Berrutietal.,2011;Brundrett,2009;Burkeetal.,2009).Nevertheless,itshouldbenotedthat,althoughthesurveyoffruitingbodiesgivesinformationabouttheEcMfungalcompositionanddiversity,suchstudiesdonotnecessarilyreflecttheoverallEcMfungicommunitycomposition.SomeofEcMfungidonotorrarelyproducefruitingbodiesduetoincompatiblecombinationsthatdonotenabletheirmycelialnetworktoproducefruitingstructure(Berrutietal.,2011;Brundrett,2009;Kernaghan,2005).Furthermore,thenaturalpro‐ductionofaboveground fruitingbodies requiresmuchmorebio‐logicalenergybyhostplantsanddependsonavailablenutrientsandfungalbiologicalcapacities(Berrutietal.,2011;Neffaretal.,2008).

Incomparisonwiththenon‐mycorrhizalmountainforestsfromtheAlbertineriftcharacterisedbyvolcanicsoilrichinmineralnu‐trient(Bernaert,2014;Pécrotetal.,1962),rainforestsinYangambiand Yoko developed mainly on poor sandy soil (Alongo, Visser,Kombele, Colinet, & Bogaert, 2013; Bartholomew et al., 1999;Gilson,Wambeke,&Gutzwiller, 1956). Previous studies (Berrutiet al., 2011; Brundrett, 2009;Neffar et al., 2008) revealed thatmycorrhizae occurmainly in poor soils, such as soils fromEcM‐dominated forests of Yangambi and Yoko (Alongo et al., 2013;Bartholomewetal.,1999;Gilsonetal.,1956).EcMfungi, there‐fore, enhance the biological fixation of atmospheric nitrogen insoil and control themineralisationof other nutrients alongwiththeavailablenitrogen.

TA B L E 5  ResultsofthecorrelationbetweenedaphicfactorswiththePERMANOVAanalysis

NMDS1 NMDS2 r2 p‐value

Al 0.96097 0.27665 0.7859 NS

H −0.79070 0.61221 0.2814 NS

pH −0.06851 0.99765 0.5112 NS

N 0.99233 −0.12361 0.7778 NS

C 0.87762 −0.47935 0.8560 NS

Ca −0.28578 0.95830 0.3388 NS

Mg −0.99890 0.04687 0.4112 NS

Clay 0.99231 0.12382 0.7146 NS

Sand −0.98303 −0.18345 0.7446 NS

Silt 0.92701 0.37503 0.8495 * 

K 0.59450 −0.80410 0.3661 NS

P −0.74898 −0.66259 0.6262 NS

Note.NS:Notsignificant.*p‐value<0.05:Significantdifference. F I G U R E 5  Thenon‐metricmultidimensionalscaling(NMDS)

ordinationshowingtherelativeinfluenceofedaphicfactorsonEcMfungihostplanttreesmaintenance[Colourfigurecanbeviewedatwileyonlinelibrary.com]

–0.4 –0.2 0.0 0.2 0.4 0.6

–0.4

–0.2

0.0

0.2

0.4

NMDS1

NMDS2

BRA

GIL

JULUAPG

UAPHAl

H

pH

N

C

Ca

MgClay

Sand

Silt

KP

258  |     MILENGE KAMALEBO Et AL.

5  | CONCLUSION

ThisstudygivesbasicinformationonthediversityanddistributionpatternofEcMfungalfruitingbodieswithinthebiospherereserveofYangambiandtheforestreserveofYoko.Atotalof93ectomyc‐orrhizalfungaltaxawererecorded,amongwhich19speciesshowedpreferenceforparticularforeststands.Regardingtheimpactofsoil,itwasshownthatedaphicfactorsdifferentlyaffectthedistributionanddiversityofEcMfungi.TheB. laurentiiplanttreeanditsassoci‐atedEcMfungiweremainlypromotedbythecontentinextractablephosphoruswhileG. dewevrei,U. guineensis and J. seretiiforestsaremainlysustainedbysandparticlesize.Aluminiumacidityandthesiltandclayparticleswerethemostimportantedaphicparametersin‐fluencingthepresenceofEcMfungalfruitingbodiesassociatedwithU. heudelotii.

Since these rainforest stands are characterised by poor soilreferring to mineral nutrients availability (Alongo et al., 2013;Bartholomewetal.,1999;Bernaert,2014),EcMfungiplayimport‐antrolesinnutrientcyclingandmineralisationbyhostplants.EcMfungi enhance biological fixation of atmospheric nitrogen in soil,which is involved inseveralorganiccombinationsandcontributestomakenitrogenavailableforassimilationbyplants(Berrutietal.,2011;Neffaretal.,2008).However,bothhost treesandedaphicfactors strongly affect the distribution and sustainability of EcMfungal diversity. EcM fungimay have developed differently theirabilitytosuccessfullycoloniserootsystemsinrelationtotheavail‐abilityofnutrients.Forestsmightbecharacterisedbypatchynutri‐entdistributioninsoilthatinreturnaffectsEcMdistribution.Yet,furtherstudiesanalysingthedistributionpatternofroot‐associatedfungiat finespatialscalearerequired inordertogetmuch infor‐mationabouttheoverallEcMfungaldiversityandtherelationwiththeirhostplants.

ACKNOWLEDG EMENTS

WethanktheEuropeanUnion,theCentreforInternationalForestryResearch(CIFOR)andtheUniversityofKisanganiforthePh.D.finan‐cialsupportgrantedtothefirstauthorthroughtheproject“ForêtsetChangementsClimatiquesauCongo.”ThetaxonomicanalysisforspeciesidentificationhasbeencarriedoutatMeiseBotanicGardenin Belgium and was supported by three grants from the BelgianGlobalTaxonomyInitiativeoftheCEBioSprogram.ThefieldworkofA.DeKeselinYangambiwasfinancedbyBELSPO(BelgianFederalSciencePolicyOffice)throughtheCOBIMFOproject(Congobasinintegratedmonitoringforforestcarbonmitigationandbiodiversity).The first author is alsograteful to the IDEAWILD foundation fortheresearchequipmentgrantedtohim.Inaddition,wethankPapaELASI,Mr. RISASI Ratos, Jules BOMBILE, AntoineMOTOSIA andMichelMBASIforguidingsamplingexpeditions.

CONFLIC T OF INTERE S T

Theauthorsdeclarethattheyhavenocompetinginterests.

ORCID

Héritier Milenge Kamalebo https://orcid.org/0000‐0002‐9232‐9801

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How to cite this article:MilengeKamaleboH,SeyaWaMalaleHN,MasumbukoNdabagaC,NabahunguLN,DegreefJ,DeKeselA.HostplantsandedaphicfactorsinfluencethedistributionanddiversityofectomycorrhizalfungalfruitingbodieswithinrainforestsfromTshopo,DemocraticRepublicoftheCongo.Afr J Ecol. 2019;57:247–259. https://doi.org/10.1111/aje.12595