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Afr J Ecol. 2019;1–13. wileyonlinelibrary.com/journal/aje
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© 2019 John Wiley & Sons Ltd
Received:7December2017
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Revised:15Octob er2018
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Accepted:17Januar y2019
DOI:10.1111/aje.12595
ORIGINAL ARTICLE
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,Universitéde
Kisangani,Kisangani,DRCongo
2CentredeRecherchesUniversitairesdu
Kivu(CERUKI)/ISP,Bukavu,DRCongo
3Facultédessciences,UniversitéOfficielle
deBukavu,Bukavu,DRCongo
4InternationalInstituteofTropical
Agriculture,IITA‐Kalambo,Bukavu,DR
Congo
5MeiseBot anicGarden,Meise,Belgique
6FédérationWallonie‐Bruxelles,Service
Généraldel’EnseignementSupérieuretde
laRechercheScientifique,Brussels,Belgium
Correspondence
HéritierMilengeKamalebo,Facultédes
sciences,UniversitédeKisangani,Kisangani,
DRCongo.
Email:kamaleboheritier@gmail.com
Funding information
CentreforInternationalForestryResearch;
BelgianFederalSciencePolicyOffice
Abstract
Ectomycorrhizalfungiconstituteanimportantcomponentofforestecosystemsthat
enhancesplantnutritionandresistanceagainststresses.Diversityofectomycorrhi‐
zal(EcM)fungiis,however,affectedbyhostplant diversity andsoilheterogeneity.
Thisstudyprovidesinformationabouttheinfluenceofhostplantsandsoilresources
on the diver sity of ectomycorrhiza l fungal fruiting bo dies from rainforest s of the
DemocraticRepublicoftheCongo.Basedonthepresenceoffungalfruitingbodies,
significantdifferences inthe number ofectomycorrhizal fungi species existed be‐
tweenforeststand types(p<0.001).Themost ectomycorrhizalspecies‐richforest
wastheGilbertiodendron dewevrei‐dominatedforest(61species).Ofall93speciesof
ectomycorrhizal fungi, 19demonstrated a significant indicator value forparticular
forest stand types. Ofallanalysededaphicfactors,the percentageofsilt particles
wasthemostimportantparameterinfluencingEcMfungihostplanttreedistribution.
Bothhosttreesandedaphicfactorsstronglyaffectedthedistributionanddiversity
ofEcMfungi.EcMfungimayhavedevelopeddifferentlytheirabilitytosuccessfully
coloniserootsystemsinrelationtotheavailabilityofnutrients.
Résumé
Danslesforêts,leschampignonsectomycorrhizienssontimpliquésdanslanutrition
etlaprotectiondesplanteshôtescontrelespathogènes.Leurdiversitéestinfluencée
par la composition floristique et les facteurs édaphiques. Cette étude traite de
l’influencedesplanteshôtes et desfacteursédaphiquessurladiversitédessporo‐
phoresdeschampignonsectomycorrhiziensdanslesforêtsdensesdelaRépublique
Démocratique du Congo.Sebasantsurla présence deleurs sporophores,onnote
l’existencedesdifférencessignificativesentrelenombred’espècesdechampignons
ectomycorrhiziens dans les différents types des forêts (P<0.001). La forêt à
Gilbertiodendrondewevreise révèlela plus richeen espèces (61espèces).Sur un
totalde93espècesdechampignonsectomycorrhiziens,19sontinféodéesauxtypes
particuliersdeforêts.Lateneurenparticuleslimoneusesestleparamètreédaphique
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MILENGE KAM ALEBO Et A L.
1 | INTRODUCTION
Mycorrhizae constitute important symbiotic associations be‐
tween pa rticular gr oups of fungi and r oots of some pla nt 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‐
ticrelationbet weenplantsandfungiplaysakeyroleinthefunction‐
ingofnaturalecosystems,especiallyinnutrientcycling(Miyamoto,
Nakano,Hattori,&Nara,2006;Peay,Kennedy,&Bruns,1962;Smith
etal.,2013;Smith,Jakobsen,Grønlund,&Smith,2011;Tedersooet
al.,2014).Mycorrhizaeenhanceplantnutrition(especiallyphospho‐
rusandnitrogen),andincreaseaplants’productivityandresistance
against s tresses (Ker naghan, 20 05; Miyamoto, Naka no, Hattori, &
Nara,2014).Inreturn,themycorrhizalfungibenefitfromphotosyn‐
thetic ally derived ca rbohydrates ma de by the host plant ( Alisson,
Hanso n,&Tre seder,2007;Kernaghan,20 05;Miyamotoetal.,2014).
Plantsdevelopseveraltypesofmycorrhizaewithfungalspecies.
The most common and important are thear buscularmycorrhizae
(AM) and t he ectomycorrh izae (EcM) (Piepenb ring, 2015). The ar‐
buscularmycorrhizaepenetraterootcells (Blakcwell, 2011;Berruti
etal.,2011;Fortin,Plenchette,&Piché,2008),whileectomycorrhi‐
zaedevelopwidespreadmycelialnetworkssurroundingroottissues
insoil.IncontrasttoAM, EcM fungidevelop aboveground fruiting
bodies , called sporoc arps, and are ma inly hosted by wood y plant
species (Fortin etal., 2008; Kernaghan, 2005; Piepenbring, 2015).
TheEcMfungalcommunitiesconstituteanimportantcomponentof
many central African forests(Eyi‐Ndonget al.,2011)and play key
roles in biogeochemicalcycles,plant communitydynamicsandthe
maintenanceof soil structure.Furthermore, asEcMfungiincludea
widerangeofediblespecies,theyconstituteanimportantsourceof
foodandincomeforlocalpopulations(Berrutietal.,2011;DeKesel,
Kasongo, & Degreef, 2017; Härkönen et al., 2015; Piepenbring,
2015).
Localenvironmentalfactorsmay also affectEcMfungal diver‐
sity(Berrutietal.,2011;Brundrett,2009;Burke,Lopez‐Gutiérrez,
&Chan,1993;Fortinetal.,2008;Kernaghan,2005).Intropicalfor‐
ests,local‐scalebioticandabioticfactorsincludingsoilproperties
andsoiltypeplayimportantrolesininfluencingthedistributionof
bothplantandfungalcommunities.EcMfungalcommunitiesare
mainlyaffectedbythediversityofhosttreesandtheheterogene‐
ity ofsoil resources (Berrutietal.,2011;Brundrett, 2009; Burke,
Lopez‐Gutiérrez, & Chan, 2009). Moreover,species of EcM fungi
canc olonisediverseho stsandplantspe ciesc anh ostsever alfungal
species.
Several studies (Bâ, Duponnois, Moyersoen, Duponnois,
Moyersoen, & Diédhiou, 2011; Buyck, Buyck, Thoen, & Walting,
1996; Ducousso, Bâ, & Thoen, 2003; Eyi‐Ndong et al., 2011;
Härkönen et al., 2015) have reported that, in tropical Africa, EcM
fungi are mainly distributed throughout the Guineo‐Congolian
basin rainforests,in the ZambezianMiombowoodlandsofEastern
andSouthcentralAfrica,andintheSudaniansavannahwoodlands.
Furthermore, the semi‐deciduousrainforests of the Tshopoprov‐
ince,partof thecentralAfricanCongolesebasin, hostseveral spe‐
ciesofEcMtrees(Bartholomew,Meyer,&Laudelout,1999;White,
1983) and are main ly dominated by Gilbertiodendron dewevrei (De
Wild.)J.Léonard,Brachystegia laurentii (DeWild.)Louis,Julbernardia
seretii (DeWild.) Troupin,Uapaca guineensisMull. Arg. and U. heu‐
delotii Baillon (Lejol y, Ndjel e, & Geerinck , 2010; Vleminck x, 2014;
White, 1983). Several other ectomycorrhizal trees (Afzelia bipin‐
densisHarms,Anthonotha macrophyllaP.Beauv.,Berlinia grandiflora
(Vahl.)Hutch.&Dalz.,etc.)occurinvariousmixedforests(Lejolyet
al.,2010;White,1983).
Despite thewidespread distributionofthis rainforest type and
the roles played by EcM fungi in these forest s, no study on the
ayantplusd’influencesurladistributiondesarbreshôtesdeschampignons.Ledével‐
oppementdelaforêtàBrachystegialaurentiietlesespècesdeschampignonsecto‐
mycorrhiziensassociéesétaientprincipalementinfluencéparlateneurenphosphore,
alors que le développement des forêts dominées par Gilbertiodendron dewevrei,
Uapaca guineensiset Julbernardiaseretii étaitinfluencéparlateneurenparticules
sablonn euses. L’acidité aluminiqu e, la teneur en part icules limoneuses ain si que la
teneur en particules argileuses sont les paramètres ayant plus d’influence sur la
présence de s sporophores des ch ampignons ectomycorr hiziens associés à Uapac a
heudelotii.Leschampignonsectomycorrhiziensontprobablementdéveloppédesap‐
titudesparticulièreslesquellesleurontpermisdecoloniserlessystèmesracinaires,en
relationaveclesressourcesminéralesdisponibles.
KEYWORDS
Congobasin,Ectomycorrhizalfungi,indicatorspecies,rainforests,soiltexture
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MILENGE K AMALEBO Et AL.
rel ationbet weenEcMfu ngifunction,theirhostplantsandsoilp ro p‐
ertiesexist fromthe rainforestsofTshopo. Yet,the assessmentof
ecologicalpatternsofEcMfungi is vital in enhancing conservation
of both fung al communiti es and their hos t plants. T he analysis of
therelationbetweenEcMfungi,hostplanttreesandsoilisalsovital
intheprocess ofassistedcultivationofectomycorrhizalplantsand
EcMfungiinoculation.Thus,thisstudyaimstoanalysetheimpacts
ofsoil resourcesonthediversityanddistributionofEcMfungiand
theirhosttreeswithinrainfores tsoftheYokoandtheYangambibio‐
spherereservefromtheprovinceofTshopo.
2 | MATERIALS AND METHODS
2.1 | Study site
ThestudysitesarelocatedintheTshopoprovinceoftheDemocratic
Republic of Congo. The mycological data were collected within
rainfore sts of the biosph ere reserve of Yangamb i (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 reser ve of Yangambi is
located i n Isangi territor y, more tha n 100km Wes t of Kisangani.
The Yokosite is located in theUbunduterritory 32kmsouth‐east
ofKisangani.Apartfrom thewidespreadmixed forests,the region
is mainly characterised by semi‐deciduous rainforests dominated
by G. dewevrei, Scorodophloeus zenkeri Harms, Prioria balsamifera
(Vermoesen)BretelerandJ. seretii(Lejolyetal.,2010;Vleminckxet
al.,2014;White,1983).
Aspartoftheequatorialregion,theTshopoprovinceischarac‐
terised by a rainyand hot climate,typical of the Af type according
toKöppen(1923).The climateis characterised bymonthlyaverage
temperaturebetween22.4and29.3°C,andannualaverageof25°C.
The annu al rainfall ra nges from 1,60 0 to 2,20 0mm with an aver‐
age of 1828mm (Mohym ont & Demarée, 20 08). Rainfall is irr eg‐
ularly di stributed ye arly with a lit tle precipi tation from D ecember
toFebruary, and along rainyseason interruptedby twosmall dry
seasons, 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 be en collected f rom March to May in 2015 an d 2016,
whichcorrespondtothemainmushroomfruitingseason.Thefungal
inventoryinvolvedsixforeststandtypes(mixedforestsandforests
FIGURE 1 Locationofthestudysite
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MILENGE KAM ALEBO Et A L.
dominated,respectively,byG. dewevrei, B. laurentii, J. serretii, U. heu‐
delotii and U. guineensis).Themixedforestshostseveralectomycor‐
rhizal tr ees such as A. bipindensis, A. macrophylla, Paramacrolobium
coeruleum (Taub.) J. Léonard and Pericopsis elata (Harms) Van
Meeuwen(Table1).
Plots (100×100m each)dividedinto20×20mgrids werede‐
marcatedineachforesttype,exceptinU. heudelotiiforestinwhich
plots were less than 100×100m due to the limited distribution
(20×50m). In each plot, analysed data were exclusively based on
thepresence/absenceofthehar vestedabovegroundectomycorrhi‐
zal fungal fruiting bodies (Table2). In the field, somemacroscopic
features(habitus;stipe,capandhymenophorecharacteristics)were
assessed.
Sporeprintswerepreserved,andsporocarpsweredriedforfur‐
thermicroscopicanalysis.Avoucher collectionandcollectedspore
printsweredepositedattheHerbariumofMeiseBotanicGarden(BR)
inBelgium.Microscopicstudyconsistedinexaminingthepileipellis,
basidia, cystidia and spores (ornamentation and size). Taxonomic
referencestudiesfortropicalAfrica (Buyck,;DeKeselet al., 2017;
Eyi‐Ndong etal., 2011;Heim, 1955;Heinemann,1954;Heinemann
&Rammeloo, 1983,1987, 1989; Verbeken & Walleyn, 2010)have
been used forspecies identification. Names of fungal species and
author 's abbreviation s were annotated us ing the Index Fungor um
database (http://www.indexfungorum.org/Names/Names.asp,
Accessed 12 N ov 2017). All unident ified specie s but identifi ed to
the genuslevel werenumbered and indicated “sp.”Fungalspecies
richnesswas calculated as the number of fungal species collected
fromeachtypeofforest(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
Composi te soil samples h ave been taken wit hin each plot at 0 to
30cmdepthusingabucketsoilauger.Soil sampleswerepackedin
plasticbagsforlaboratoryanalysis.Fromeachsoilsample,pH(H20,
1:2.5), min eral nutrie nt (nitrogen, pho sphorus, pot assium and ca r‐
bon)andexchangeablecations(H+,Al3+,Ca2+andMg2+)weremeas‐
ured. Extractablenitrogen(N)wasassessedbyKjeldahl procedure
while Olsenextract method was usedfor exchangeable potassium
(K) and ex tractable phosphorus (P). The total organic carbon (C)
wasmeasured calorimetrically(Anderson&Ingram,1993).Thesoil
particlesizeanalysiswasmeasuredhygrometrically(Motsara&Roy,
2015).TheKruskal–Wallistestwasusedtoassesst hedifferencebe‐
tweensoilparameters.
2.2.3 | Statistical analyses
Toexaminetherelativeinfluenceofsoiltypeandhostplantspecies
onectomycorrhizalfungalspecies assembly,weusedpermANOVA
analysis (10,000 permutations) (Anderson, 2001). The ordination
analysis withRsoftwareinvolvedthenon‐metricmultidimensional
scaling ( NMDS) (Clarke & Gorle y, 2013). The hier archical anal ysis
wasusedtoclusterplotsbasedontheirmycologicalsimilaritywhile
EcM fungal species accumulation curves were performed using
Excel sof tware. The Indicator spe cies analysis (Indval) per formed
withtheindicspeciespackageofRsoftwarewasusedtodetermine
indicatorspeciesforeachforeststandtype(DeCáceres,2002).For
each indicatorspecies, probability of both fidelityand occurrence
werecalculated.Thefidelityconcernstheexclusivemembershipof
fungalspeciestoaparticularforeststandtype,whiletheoccurrence
probabilityindicatesthefrequency or preference offungalspecies
toplotsofagiventypeofforest.
TABLE 1 ListanddistributionofEcMplanttrees(+:present,−:absent),),(P1=Brachystegia laurentii‐dominatedforest,
P2=Gilbertiodendron dewevrei‐dominatedforest,P3=Julbernardia serretiiforest,P4=Mixedforest,P5=Uapaca guineensis‐dominated
forestsandP6=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 − − − − − +
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MILENGE K AMALEBO Et AL.
TABLE 2 ListofrecordedEcMfungiandtheiroccurrencewithinforests(+:present;−:absent),(P1=Gilbertiodendron dewevrei‐dominated
forest,P2=Brachystegia laurentii‐dominatedforest,P3=Mixedforest,P4=Julbernardia serretiiforest,P5=Uapaca guineensis‐dominated
forestsandP6=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 +‐ − − ‐ −
(counnues)
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MILENGE KAM ALEBO Et A L.
3 | RESULTS
Family Species
Forest stand types
P1 P2 P3 P4 P5 P6
Clavariaceae Scytinopogon angulisporus (Pat.)Corner + + + − − −
Cortinariaceae Telam onia 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 +− − − − −
TABLE 2 (Continued)
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MILENGE K AMALEBO Et AL.
3.1 | Diversity and distribution of ectomycorrhizal
(EcM) fungi within forest stand types
3.1.1 | Species richness
Atotal of 93 taxaofEcM fungiwererecorded in six differentfor‐
eststands. Amongthem,54were determinedtospeciesleveland
39to thegenuslevel. Significantdifferenceswereobserved in the
numberofEcMfungibetweenforeststandtypes(Figure2)(p‐value
<0.001).TheShannondiversityindexrevealedthattheG. dewevrei‐
dominatedforestwasthemostspecies‐richforeststand(totalspe‐
cies number=61, Shannon index value=4.11). The second most
species‐richforeststandwastheB. laurentii‐dominatedforest(total
species number=24,Shannonindex value=3.17),followed by the
U. heudelotii‐dominated forest (total species number=7, Shannon
indexvalue=1.94)andthemixedforests(totalspeciesnumber=7,
Shannon index value=1.94). The lowest number of EcM fungal
species was reported in J. seretii‐dominated forest (total species
number=4, Shannon index value=1.38). TheRussulaceaewasthe
most representative family ofEcM fungi (35 species), followed by
Cantharellaceae(18species),Boletaceae(14spec ies)an dAmanitaceae
(13species).
Whereas the number of EcM fungi significantly differed be‐
tweenforesttypes,thespeciescumulativecurve(Figure3)revealed
differentpatternsofspeciesrichness withinplots.Thehighestcu‐
mulative sp ecies richness was demons trated in G. dewevrei‐domi‐
natedforests,followedbyB. laurentii‐dominatedforests.Plotsfrom
mixed forests, J. seretii forests andUapacaspp.‐dominatedforests
exhibitedlowvariationinthenumberofEcMfungi.
3.1.2 | Fungal species assemblages and
indicator species
The composition of vascular plants prominently influenced EcM
fungi species assemblages and composition. Clustering of plots
based on thecomposition inEcMfungi isstronglycorrelated with
forest s tand type s (Figure 4). Apar t from a few common sp ecies,
each fore st stand t ype is charac terised by its own Ec M diversity.
However,oneplotofJ. seretii‐dominatedforestwasclusteredwith
mixedforestsassomecommonspeciesofEcMfungioccurredinthe
twotypesofforeststands.
Ofall93recordedtaxa,19speciesofEcMfungidemonstrated
a 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‐domi nated forest (6 spe cies) and the fore st dominated by
G. dewevrei(5species)whereastheU. guineensis‐dominatedforest
and the B. laurentii–G. dewevrei combined forest both have only
oneindicator species.NospeciesofEcMfungiwasdemonstrated
asindicatorforJ. seretiiandothermixedforests.Basedontheiroc‐
currenceandfidelityprobability,allindicatorspeciesof B. lauren‐
tiiforest revealed strongpreference (100% occurrence) whereas
only4ofthem demonstrated 100%fidelity.Theall five indicator
speciesof G. dewevrei‐dominated forestwereexclusively faithful
(100%fidelity)anddemonstratedstrongpreference(100%occur‐
rence). In U. heudelotii forests, all indicator species were faithful
FIGURE 2 Distributionofthenumbers
ofEcMspecieswithinforeststandtypes
(MIX:Mixedforests;GIL,Gilbertiodendron
dewevrei‐dominatedforests;BRA:
Brachystegia laurentii‐dominatedforests;
JUL:Julbernardia seretii‐dominated
forests,Uapaca guineensis‐dominated
forests,Uapaca heudelotii‐dominated
forests)
FIGURE 3 EcMspeciescumulativecurveaccordingtoforest
standtypes(MIX:Mixedforests;GIL:Gilbertiodendron dewevrei‐
dominatedforests;BRA:Brachystegia laurenti‐dominatedforests;
JUL:ForestsdominatedbyJulbernardia seretii;UAPG:Uapaca
guineensis‐dominatedforests;UAPH:Uapaca heudelotii‐dominated
forests)
0
10
20
30
40
50
60
70
0123
EcM species numbe
r
Plots
MIX
GIL
BRA
JUL
UAPG
UAPH
8
|
MILENGE KAM ALEBO Et A L.
whereasonly fourofthemdemonstratedstrong preferencewith
100%occurrence.
Several ot her species of EcM fung i, even reported f aithful to
somespecificforeststands,weredescribedasrarespecies(p‐value
<0.05) occu rring rarely i n single plots. T his is the case of num er‐
ousspeciesofthegenusAmanita and Russulasporadicallyfoundin
G. dewevrei‐ and B. laurentii‐dominatedforests.
3.2 | Variability in soil types and properties within
forest stands
Most of edaphic factorsclearly differed betweenthe forest types
(Table4).Significantdifferencesexistedforextractablephosphorus
content(p‐value=0.005),sandparticlessize(p‐value=0.037),clay
particles (p‐value=0 .024), exchangeable C a (p‐value=0.015), soi l
C(p‐value =0.033)aswellasavailableN(p‐value =0.004).Inaddi‐
tion, theforests dominated byB. laurentii, G. dewevrei and J. seretii
arecharacterisedbyasandyloamsoilwhileU. guineensis and U. heu‐
delotii forests are respectively characterised by loamy sand and
clayeysoils.
Althou gh soil proper ties clear ly differ be tween fores t stands,
the PERMA NOVA analy sis revealed that the s ilt particle size r e‐
mains the m ost import ant soil paramete r that has prominent i n‐
fluence o n the diversity of b oth EcM fungi and hos t plant trees
(Table 5). However, the non‐metric multidimensional scaling
(NMDS) ordination (Figure 5) demonstrated that G. dewevrei‐ and
U. heudelotii‐dominated forests are mostly promoted by particle
sizeof clay andsilt, andthe content in organic C,N and extract‐
able K. Fur thermor e, the hydrogen acid ity, the exchangeab le Ca,
theavailableMg,thepHandthe percentage ofsand particlesare
themostimportantedaphicparametersthatpromoteB. laurentii‐,
J. seretii‐ and U. guineensis‐dominatedforests.Correlationbetween
theedaphicfactorsandforeststandtypes,demonstratedthatthe
soilpropertiesthat are mainly ordinatedwith a giventypeoffor‐
esthadprominentinfluenceonthediversityofbothEcMfungiand
hostplanttrees(Figure5).
Thefirstaxisordinatedforeststandsbasedmainlyonsoiltype.
All ty pes of forest (B. laurentii‐dominated forest, G. dewevrei‐dom‐
inated forest and J. seretii forest) developed on sandy soil were
grouped together while only U. heudelotiionclayeysoilissepa‐
rated.Thesecondaxisordinatedforeststandsbasedmainlyonsoil
acidit y.Fore sts growin g on soil charac terised by hydro gen acidity
wereordinatedtogether,whereasforestsofsoilcharacterisedbyAl
acidityformed separate ordination. However,thediversityofeach
foreststandandassociatedEcMfungalcommunityweredifferently
influencedbysoil properties. The NMDSanalysisshowed thatthe
sustainabilityofB. laurentii‐dominatedforestanditsassociatedEcM
fungi was mainly promoted by the content in extractable P.Fungi
andhost plants fromG. dewevrei,U. guineensis and J. seretiiforests
were influenced primarily by hydrogen acidity, exchangeable Ca,
availableMg,pHandthepercentageofsandparticles.Furthermore,
Alacidity,totalN, C,Kand contentofsiltand claywerethe most
FIGURE 4 Hierarchicalclustering
ofplotsreferringtothemycological
similarity
|
9
MILENGE K AMALEBO Et AL.
important edaphic parameters influencing the presence of EcM
fungiassociatedwithU. heudelotii.
4 | DISCUSSION
4.1 | EcM fungi diversity and distribution within
forest stands
The compo sition and dist ribution of EcM fung al fruiting bo dies var‐
ied significantly with host tree distribution. In all forest types, the
families Russulaceae and Cantharellaceae dominate, as previously re‐
portedbyEyi‐Ndong etal.(2011)fortheCentralAfricanrainforests,
Buyck,Gomez‐Hernandez, Williams‐Linera,andRamírez‐Cruz (2017)
and Bâ, D uponnois, Moye rsoen, and D iédhiou (2010) for t he savan‐
nah woodlands of Western Africa and Buyck(1997),Härkönenet al.
(2015)andDeKeselet al.(2017)fortheMiombowoodlands.Species
ofCantharellaceae and Russulaceae should have developedcapacities
toadapttothelocal edaphicconditionsenablingthemtosuccessfully
coloniseplantrootsthroughouttheseforesttypes(Berrutietal.,2011;
Brundrett,2009;Burkeetal.,2009).Inaddition,theforestsdominated
by G. dewevrei and B. laurentiiwerethemostEcMspecies‐richforest
stands,aspreviouslyrecordedbyEyi‐Ndongetal.(2011)fromlowland
rainforestinGabon. Thiscanbeexplainedbythefact thatB. laurentii
and G. dewevrei fo reststandsar et hemostwid elydist ributedEcMtrees
in the Cong o basin (White, 1983). G. dewevrei and B. laurentii should
havedevelopedcapacities tohostseveralEcMfungi inlocal edaphic
conditions.Aspreviouslyreportedfromdiversetropicalforests(Bâet
al.,2010; Burkeetal.,2009;Eyi‐Ndong etal.,2011;Khasa,Furlan, &
Lumande,199 0;Yorou&Kesel,2011),EcMhosttreesinTsho pobelong
exclusivelytothefamiliesFabaceae and Phyllanthaceae.
Referrin g to the results of i ndicator spe cies analysis, n umer‐
ous species ofEcM fungi have demonstrated strong preference,
evenfidelity,tospecifichabitats. Thisisthe caseofCantharellus
ruber, C. rufopunctatus, Russula roseostriata, Thelephora palmata,
TABLE 3 ValuesoftheindicatorEcM
speciesanalysisforthestudiedforest
stands N°
Indicator EcM
species
Probability Indicator value (Indval)
Fidelity Occurrence Indval p‐value
Brachystegia laurentii‐dominatedforest
1Cantharellus ruber 1.0000 1.000 1.000 **
2Cantharellus
rufopunctatus
1.0000 1.000 1.000 **
3Russula roseostriata 1.0000 1.000 1.000 **
4Thelephora palmata 1.0000 1.000 1.000 **
5Russula meleagris 0.8333 1.000 0.913 **
6Russula sese 0.8333 1.000 0.913 **
7Cantharellus
miniatescens
0.750 0 1.000 0.866 *
Uapaca heudelotii‐dominatedforest
1Lactifluus heimi 1.00 1.00 1.000 **
2Lactarius sp.4 1.00 1.00 1.000 **
3Lactarius sp.5 1.00 1.00 1.000 **
4Lactarius sp.6 1.00 1.00 1.000 **
5Russula sp.7 0.75 1.00 0.866 *
6Russula sp.8 0.75 1.00 0.866 *
Gilbertiodendron dewevrei‐dominatedforest
1Cantharellus
congolensis
1.000 1.000 1.000 **
2Lactarius sp.2 1.000 1.000 1.000 **
3Rubinoboletus
luteopurpureus
1.000 1.000 1.000 **
4Strobilomyces
echinatus
1.000 1.000 1.000 **
5Tylopilus beeli 1.000 1.000 1.000 **
Uapaca guineensis‐dominatedforest
1Cantharellussp.2 1.0000 1.0000 1.000 **
Brachystegia laurentii+Gilbertiodendron dewevrei‐dominatedforests
1Lactarius acutus 1.0000 0.6667 0.816 *
*p‐value<0.05:Significantdifference.**p‐value<0.01:Highlysignificantdifference.
10
|
MILENGE KAM ALEBO Et A L.
TABLE 4 Meanvaluesofedaphicparameters±Standarddeviation(SD)
Edaphic factors
BRA GIL JUL UAPG UAPH Kruskal–Wallis
Mean ±SD Mean ±SD Mean ±SD Mean ±SD Mean ±SD p‐value
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
pH 4,33±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±0,0 0 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 Sandy loam Sandy loam Sandy loam Loamy sand Clay
OM 1,2 1,4 0,8 0,9 2,3
C/Nratio 910 12 9 6
Note.ThetwolastcolumnsindicateP‐valueandthesignificanceleveloftheKruskal–Wallistest.
BRA:Brachystegia laurentii‐dominatedforest;GIL:Gilbertiodendron dewevrei‐dominatedforest,JUL:Julbernardia serretiiforest;OM:OrganicMatter;UAPG:Uapaca guineensis‐dominatedfor‐
ests;UAPH:U. heudelotii‐dominatedforest;NS:Notsignificant.
*p‐value<0.05:significantdifference.**p‐value<0.01:Highlysignificantdifference.
|
11
MILENGE K AMALEBO 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 sp ecies for G. dewevrei‐dominated forest while Lactifluus
heimi characterised the U. heudelotii forests. Furthermore,
Lactarius acutuscharacterisedboththeG. dewevrei‐ and B. lauren‐
tii‐dominatedforests.
AsreportedbyYorouandDeKesel(2011),thegreatest danger
facing EcM fungirelatetothethreat;facing theirhabitatandtheir
hostplanttrees.Furthermore,therarityexpressedinthenumberof
fungal locationsand their habitat areasare themain criteria to be
used for EcM fungi‐basedIUCN status classification. Thereby,due
totherapidlossofbiodiversityinnaturalecosystems,theestablish‐
mentofIUCNstatusofvariousrareandendangeredspeciesofEcM
fungifromrainforestsofTshopoisofgreatimportance.
4.2 | Edaphic factors promoting both EcM fungi and
host trees sustainability
Theanalysisofedaphic factorsindicatedmanydifferencesexisting
betweensoil characteristics of the investigated forests.Three dif‐
ferentsoiltypeswerecharacterisedbasedonthesoilparticlessize.
TheG. dewevrei,B. laurentii and J. seretiiforests occurred on sandy
loamsoil,whileU. guineensis and U. heudelotiideveloponloamysand
andclayey soil.Furthermore, thesoil nutrient contentand proper‐
tiesvarysignificantlyamongforests.And,ofthese,availablePwas
alsonegativelycorrelatedtoAlcontent.Moreover,theforestsde‐
velopedonasandysoil(characterisedbyhighlevelofhydrogenacid‐
ityandhighPcontent)(G. dewevrei and B. laurentiiforests)hosteda
higher number of EcM fungi thanthe U. heudelotiiforest found on
clayeysoil(wheretheacidityisbasedonAlcontent).
The s e f i n d i n g sarein l i n ewithsev e r a l otherstudie s ( B u r keeta l . ,
1993;Hazelton & Murphy,20 07;Neffar,Beddiar,&Chenghouni,
2008) thatreported thathighconcentrationsofexchangeableAl
reducetheavailabilityofPinsoilandshouldnegativelyaffectthe
developmentofEcMfungi(Burkeetal.,2009;Neffaretal.,2008).
Furthermore,thehighcontentofavailablePin B. laurentiiforests
mightexplainthattreerootsarestronglyinvolvedintheminerali‐
sa tionofPalo ngw itht heNcoll ectedfro mthe atmo sphe re(B errut i
etal.,2011;Brundrett,2009;Burkeetal.,2009).Nevertheless,it
shouldbenotedthat,althoughthesurveyoffruitingbodiesgives
informationabouttheEcMfungalcompositionanddiversity,such
studiesdonotnecessarilyreflec tt heoverallEcMfungicomm unit y
composition.SomeofEcMfungidonotorrarelyproducefruiting
bodiesduetoincompatiblecombinationsthatdonotenabletheir
mycelialnetworktoproducefruitingstructure(Berrutietal.,2011;
Brundrett,2009;Kernaghan,2005).Furthermore,thenaturalpro‐
ductionofabovegroundfruitingbodiesrequiresmuchmorebio‐
logical energy by hostplantsand depends onavailablenutrients
andfungalbiologicalcapacities (Berrutietal.,2011;Neffaretal.,
2008).
Incomparisonwiththenon‐mycorrhizalmountainforestsfrom
theAlbertineriftcharacterisedbyvolcanicsoilrichinmineralnu‐
trient(Bernaert,2014;Pécrotetal.,1962),rainforestsinYangambi
and Yoko develope d mainly on poor san dy soil (Alongo, V isser,
Kombele, Colinet, & Bogaer t, 2013; Bartholomew et al., 1999;
Gilson, Wambeke, & Gutzwiller, 1956). Previous studies(Berruti
et al., 2011; Brun drett, 20 09; Neff ar et al., 200 8) revealed th at
mycorrhizae occur mainly in poor soils, such as soils from EcM‐
dominated forest s of Yangambi and Yoko (Alongo et al., 2013;
Bartholomew etal.,1999;Gilson etal., 1956).EcMfungi,there‐
fore, enh ance the biologic al fixation of at mospheric nit rogen in
soil andcontrolthe mineralisation ofother nutrients along with
theavailablenitrogen.
TABLE 5 Resultsofthecorrelationbetweenedaphicfactors
withthePERMANOVAanalysis
NMDS1 NMDS2 r2p‐value
Al 0.960 97 0.27665 0.7859 NS
H−0.79070 0.612 21 0.2814 NS
pH −0.06851 0.99765 0.5112 NS
N0.99233 −0.12361 0.7778 NS
C0.87 762 −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 .714 6 NS
Sand −0.98303 −0.18345 0 .74 4 6 NS
Silt 0.92701 0.37503 0.8495 *
K0.59450 −0.80 410 0.3661 NS
P−0 .74 898 −0.66259 0.6262 NS
Note.NS:Notsignificant.
*p‐value<0.05:Significantdifference. FIGURE 5 Thenon‐metricmultidimensionalscaling(NMDS)
ordinationshowingtherelativeinfluenceofedaphicfactorsonEcM
fungihostplanttreesmaintenance
–0.4 –0.2 0.00.2 0.
40
.6
–0.4 –0.2 0.00.2 0.4
NMDS1
NMDS2
BRA
GIL
JUL
UAPG
UAPH
Al
H
pH
N
C
Ca
Mg Clay
Sand
Silt
K
P
12
|
MILENGE KAM ALEBO Et A L.
5 | CONCLUSION
Thisstudy givesbasicinformationonthediversityanddistribution
patternof EcM fungalfruitingbodies withinthebiospherereserve
ofYangambiandtheforestreserveofYoko.Atotalof93ectomyc‐
orrhizalfungaltaxawererecorded,amongwhich19speciesshowed
preferenceforparticularforeststands.Regardingtheimpactofsoil,
itwasshownthatedaphicfactorsdifferentlyaffectthedistribution
anddiversityofEcMfungi.TheB. laurentiiplanttreeanditsassoci‐
atedEcMfungiweremainlypromotedbythecontentinextractable
phosphoruswhileG. dewevrei,U. guineensis and J. seretii forests are
mainlysustainedbysandparticlesize.Aluminiumacidityandthesilt
andclayparticleswerethemostimportantedaphicparametersin‐
fluencingthepresenceofEcMfungalfruitingbodiesassociatedwith
U. heudelotii.
Since these rainforest stands are characterised by poor soil
referring to mineral nutrients availability (Alongo et al., 2013;
Bartholomewetal.,1999;Bernaert,2014),EcMfungiplayimport‐
antrolesinnutrientcyclingandmineralisationbyhostplants.EcM
fungi enh ance biologica l fixation of atmos pheric nitroge n in soil,
whichisinvolvedin severalorganiccombinationsand contributes
tomakenitrogenavailableforassimilationbyplants(Berrutietal.,
2011;Neffaret al., 2008). However,both hosttreesand edaphic
factor s strongly af fect the dis tribution an d sustainabil ity of EcM
fungal di versity. EcM fungi may h ave developed dif ferently the ir
abilitytosuccessfullycoloniserootsystemsinrelationtotheavail‐
abilityofnutrients.Forestsmightbecharacterisedbypatchynutri‐
entdistributioninsoilthat inreturnaffectsEcMdistribution. Yet,
furtherstudiesanalysingthedistributionpat te rnofroot‐associated
fungi at finespatialscale arerequiredin ordertogetmuch infor‐
mationabouttheoverallEcMfungaldiversityandtherelationwith
theirhostplants.
ACKNOWLEDGEMENTS
WethanktheEuropeanUnion,theCentreforInternationalForestry
Re s e a rch(C I FOR)a n d t heUni v e r sityof K i s anganif o rtheP h . D.fina n ‐
cialsupportgrantedtothefirst authorthroughtheproject“Forêts
etChangementsClimatiquesauCongo.”Thetaxonomicanalysisfor
speciesidentificationhasbeencarriedoutatMeiseBotanicGarden
in Belgium and was supported by three grants from the Belgian
GlobalTaxonomyInitiativeoftheCEBioSprogram.Thefieldworkof
A.DeKeselinYangambiwasfinancedbyBELSPO(BelgianFederal
Science PolicyOffice)through the COBIMFOproject(Congobasin
integratedmonitoringforforestcarbonmitigationandbiodiversity).
The first author is also grateful tothe IDEA WILD foundation for
theresearchequipmentgrantedtohim.Inaddition,wethankPapa
ELAS I, Mr. RISASI Ratos , Jules BOMBILE , Antoine MOTOSIA an d
MichelMBASIforguidingsamplingexpeditions.
CONFLICT OF INTEREST
Theauthorsdeclarethattheyhavenocompetinginterests.
ORCID
Héritier Milenge Kamalebo https://orcid.
org/0000‐0002‐9232‐9801
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MalaleHN,MasumbukoNdabagaC,NabahunguLN,Degreef
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