ESCUELA TÉCNICA SUPERIOR DE INGENIERÍAS AGRARIAS
SUSTAINABLE FOREST MANAGEMENT RESEARCH INSTITUTE
DOCTORAL DISSERTATION / TESIS DOCTORAL
Fungal communi ies associa ed wi h o es s in he
A omon ane egion o E hiopia
Comunidades de hongos asociadas a los bosques en la
egión de A omon ana de E iopía
P esen ada po Demelash Alem Ayana
pa a op a al g ado de doc o po la
Uni e sidad de Valladolid
Di igida po :
D . Pablo Ma ín-Pin o
D . Ta ek Dejene Bekele
Acknowledgemen
i
Acknowledgmen
Fi s o all, I would like o hank he Glo ious God o enabling me o success ully
accomplish my s udy.
I o wa d g ea g a i ude o my Ad iso s, P o . D . Pablo Ma in Pin o and D . Ta ek
Dejene o hei un ese ed echnical suppo h oughou my s udy pe iod. I g ea ly
hank P o esso Pablo Ma in-Pin o o his posi i e a i ude and con inuous mo i a ion
h oughou my s udy pe iod. I hank D . Ta ek Dejene o his dedica ed suppo ,
men o ing, equen ollow-up and p o ision o ele an e e ence ma e ials and da a.
I would like o hank D . Wubalem Tadesse o his suppo and encou agemen
h oughou my s udy pe iod. Wi hou him, my PhD s udy would no ha e happened.
I would like o hank he Uni e si y o Valladolid o accep ance as a PhD s uden and
EEFRI o allowing me o pu sue my s udy.
I hank D . Jozse Geml o men o ing and helping me de elop da a analysis skills
especially in R so wa e while I was in he Ne he lands o such aining.
I would also o wa d g ea g a i ude o M . Sewale Wondimneh and M . An eneh
Yenesew (Bahi Da En i onmen and o es Resea ch Cen e ) o hei suppo in ield
da a collec ion. I hank Banja, Fa a and Libokemkem dis ic o ices expe s and
eligious leade o Ta agedam monas e y o allowing me o conduc he s udies in
hese o es s. I also hank o es gua ds o hei suppo du ing ield da a collec ion.
This esea ch was suppo ed by he p ojec s SUSTIFUNGI_ET (Sus ungi_E h:
2017/ACDE/002094) and MYCOPROED_ET (Mycop oed_E h: 2019/ACDE/000921)
unded by he Spanish Agency o In e na ional De elopmen and Coope a ion. This
s udy was also co- unded by he Spanish Minis y o Educa ion and Cul u e unde a
Sal ado de Mada iaga g an ag eemen , n° PRX17/00315. I would like o hank all
membe s o he Sus ungi_E h p ojec who, in way o ano he , con ibu ed o he
success o my s udy.
Acknowledgemen
ii
I ex end my g a e ul hanks o he s a membe s o E hiopian En i onmen and Fo es
Resea ch Ins i u e (EEFRI) and Bahi Da En i onmen and Fo es Resea ch Cen e o
suppo ing and acili a ing my s udy.
I would like o hank my wi e Zenebech Chekol, o he con inuous mo i a ion and
shoulde ing amily cases while I was busy o my s udy. The smiley aces and laugh e o
my kids (Na nael, Yo danos and Mikias) we e excellen ene gize s o my s udy
especially du ing he pe iod o COVID-19 pandemic.
I hank my colleagues D . Muluge a A na , D . Demeke Mewa, Chalachew Abebe,
Tsehaynesh Gu mu and D . Meha i Alebachew o hei mo al suppo . My b o he s,
sis e s, my b o he s-in-law and my sis e s-in-law a e g ea ly hanked o hei
encou agemen and mo al suppo . I would like o hank my a he , Kes Alem Ayana,
and my mo he , M s. Hibis Yeshu, my a he -in-law, Chekol Gelaw, and my mo he -in-
law, Emawayish Weldelul, o hei p ay and encou agemen . Thanks God o keeping
all o us sa e.
Dedica ion
iii
Dedica ion
Those who los hei li es due o Co ona Vi us (COVID-19) all o e he wo ld and
con lic s in E hiopia
Table o con en s
CONTENTS
Acknowledgmen ............................................................................................................ I
Abs ac ........................................................................................................................ VII
Resumen ....................................................................................................................... XI
Lis o o iginal a icles ............................................................................................... XV
Ou line o he hesis ................................................................................................. XVII
1. In oduc ion ............................................................................................................... 1
1.1. CLIMATE, GEOLOGY AND ECOLOGY OF ETHIOPIA ...................................................................................... 1
1.2. NATURAL FORESTS IN ETHIOPIA ................................................................................................................. 1
1.3. PLANTATION FOREST IN ETHIOPIA .............................................................................................................. 4
1.4. WHAT ARE FUNGAL RESOURCES? .............................................................................................................. 6
1.5. IMPORTANCE OF FUNGI ............................................................................................................................... 6
1.6. FACTORS GOVERNING FUNGAL DISTRIBUTION ............................................................................................ 8
1.7. RESEARCH AND CONSERVATION STATUS OF FUNGI ................................................................................... 9
1.8. OVERVIEW OF MYCOLOGICAL STUDIES IN ETHIOPIA ................................................................................. 11
1.9. WHY THE CURRENT STUDY? ..................................................................................................................... 14
1.10. HYPOTHESES AND RESEARCH QUESTIONS............................................................................................. 16
1.11. SCOPE OF THE STUDY ............................................................................................................................. 17
2. Objec i es o he hesis .......................................................................................... 21
3. Ma e ial and me hods ............................................................................................. 25
3.1. DATA SOURCES ......................................................................................................................................... 25
3.2. THE STUDY AREAS ..................................................................................................................................... 25
3.3. ESTABLISHMENT OF FIELD PLOTS ............................................................................................................. 28
3.3.1. Plo es ablishmen in D y A omon ane o es s o s udy soil ungal communi y
composi ion and di e si y in ela ion o o es i e .................................................. 28
3.3.2. Plo es ablishmen in P. pa ula plan a ion o es o di e en age o s udy he soil
ungal communi ies and succession ....................................................................... 28
3.3.3. Plo es ablishmen o s udy spo oca ps di e si y and p oduc ion and soil ungal
communi y composi ion and di e si y in agmen ed chu ch o es s in D y
A omon ane o es sys ems in No he n E hiopia .................................................. 29
3.4. SAMPLING .................................................................................................................................................. 29
3.4.1. Spo oca p sampling ................................................................................................ 29
3.4.2. Soil sampling o DNA ex ac ion ............................................................................ 29
3.4.3. Soil sampling o physico-chemical analysis ........................................................... 30
3.4.4. Vege a ion and clima e da a collec ion ................................................................... 30
3.5. LABORATORY ANALYSIS AND TAXA IDENTIFICATION ................................................................................. 31
3.5.1 Spo oca p axa iden i ica ion and classi ica ion ....................................................... 31
3.5.2. Molecula analysis .................................................................................................. 32
Table o con en s
i
3.6. DATA ANALYSIS ......................................................................................................................................... 32
3.6.1 Bioin o ma ics analysis ............................................................................................ 32
3.6.2. S a is ical analysis ................................................................................................... 33
4. Resul s ..................................................................................................................... 37
4.1. TAXA COMPOSITION OF SOIL FUNGI ........................................................................................................... 37
4.2. MACROFUNGAL TAXA COMPOSITION ......................................................................................................... 39
4.3. THE EFFECT OF FIRE, STAND AGE AND ABOVEGROUND PLANT DIVERSITY ON FUNGAL RICHNESS,
DIVERSITY AND PRODUCTION..................................................................................................................... 40
5. Discussion ............................................................................................................... 43
5.1. SOIL FUNGAL TAXA COMPOSITION ........................................................................................................... 43
5.2. MACROFUNGAL TAXA COMPOSITION ......................................................................................................... 47
5.3. EFFECT OF FIRE, STAND AGE, AND ABOVEGROUND PLANT DIVERSITY ON FUNGAL RICHNESS, DIVERSITY
AND PRODUCTION ...................................................................................................................................... 50
7. Conclusiones ........................................................................................................... 59
8. Re e ences ............................................................................................................... 61
O iginal a icles ........................................................................................................... 83
Abs ac
ii
Abs ac
The A omon ane egion o E hiopia has na u al and plan a ion o es sys ems ha
p o ide high socioeconomic and ecological alue, including he biodi e si y
conse a ion. Howe e , he na u al o es s in his egion a e acing challenges in which
hei deg ada ion is amed o decades. In esponse o his, exo ic ee species ha e
been in oduced o dec ease he p essu e on he na u al o es s. Thus, he plan a ions
a e managed o maximize he alue o he wood and educe he gap be ween wood
demand and supply in he coun y. Acco dingly, some na u al o es s ha e been
conse ed as p io i y o es s, bu wi hou gene a ing angible bene i s o he local
communi y.
In his con ex , some non- imbe o es p oduc s, no ably mush ooms, a e neglec ed and
no included in E hiopia's o es managemen plans and s a egies o he coun y.
Consequen ly, s udies on he e ec s o o es managemen on he di e si y and
composi ion o ungal communi ies a e e y limi ed. The e o e, ou objec i e was o
gene a e in o ma ion on he composi ion and di e si y o he ungal communi y in he
o es sys ems o he A omon ane egion, including na u al and plan a ion o es s. In
he na u al o es s, he spa ial dis ibu ion o agmen ed chu ch o es s and he ime
a e dis u bance in he o es we e aken in o conside a ion o he s udy. In he
plan a ion o es s, he s and age was aken in o accoun o analysis he exis ing ungal
communi ies and succession in Pinus pa ula plan a ions. We s udied he soil ungal
communi ies in all he o es s sys ems. Speci ically, we also conduc ed he ui body
collec ion in he agmen ed na u al o es s o he No hwes o he coun y, since his
pa icula in o ma ion was al eady a ailable o he es o he sys ems included in his
s udy. In he agmen ed D y A omon ane o es s in No hwes e n E hiopia, h ee o es
ypes we e selec ed. A o al o 27 plo s (2 m × 50 m), nine in each o es ype, we e
es ablished o he collec ion o he spo oca ps and soil ungi. To assess he e ec o
i e on soil ungi, h ee simila plo s we e sampled in each o he h ee o es s ha
di e ed in hei i e his o y (unbu ned, 10-yea s old bu ned and 36-yea s old bu ned
s ands). Likewise, a o al o nine plo s we e es ablished in he plan a ion o es s in h ee
age ca ego ies (5-, 11- o 36- yea old s ands).
Lis o o iginal a icles
x
Lis o o iginal a icles
This hesis is based on ou o iginal wo ks, which a e e e ed in he ex wi h Roman
nume als (I – IV). All excep he o h one a e al eady published. The ou h is a
manusc ip .
Au ho s, coau ho s, and he s age o he publica ion a e p esen ed below:
I. Demelash Alem, Ta ek Dejene, Juan And és O ia-de-Rueda, Józse Geml,
Ca les Cas año, Jane E. Smi h, Pablo Ma ín-Pin o. 2020. Soil ungal
communi ies and succession ollowing wild i e in E hiopian D y A omon ane
o es s, a highly di e se unde explo ed ecosys em. Fo . Ecol. Manage. 474, xx–
xx.(118328) h ps://doi.o g/10.1016/j. o eco.2020.118328
II. Demelash Alem, Ta ek Dejene, Juan And és O ia-de-Rueda, Józse Geml,
Pablo Ma ín-Pin o. 2020. Soil Fungal Communi ies unde Pinus pa ula Schiede
ex Schl dl. & Cham. Plan a ion Fo es s o Di e en Ages in E hiopia. Fo es s
11, 1109. h ps://doi.o g/10.3390/ 11101109
III. Demelash Alem, Ta ek Dejene, Juan And és O ia-de-Rueda, Pablo Ma ín-
Pin o. 2021. Su ey o mac o ungal di e si y and analysis o edaphic ac o s
in luencing he ungal communi y o chu ch o es s in D y A omon ane a eas o
No he n E hiopia. Fo . Ecol. Manage. 496, xx–xx.(119391).
h ps://doi.o g/10.1016/j. o eco.2021.119391
IV. Demelash Alem, Ta ek Dejene, Józse Geml, Juan And és O ia-de-Rueda and
Pablo Ma ín-Pin o. 2021. Soil ungal communi ies in agmen ed D y
A omon ane Chu ch o es s in No he n E hiopia (Manusc ip )
Ou line o he hesis
x ii
Ou line o he hesis
This hesis consis ed o ou s udies impo an o desc ibe he s a us o ungal
communi ies om wo o es sys ems in he D y A omon ane egion o E hiopia. The
i s s udy (S udy I) ocused on he communi y composi ion, di e si y and ichness o
soil ungi unde di e en successional s ages a e i e in he D y A omon ane o es
sys ems o Sou he n E hiopia whe e he ecu en o es i e is common. The second
(S udy II) is on ungal succession in ela ion o s and de elopmen o Pinus pa ula
whe e he e ec s o s and age o P. pa ula on he communi y composi ion, di e si y and
ichness o soil ungi a e discussed. The hi d and he ou h (S udy III and IV) a e
ocused on mac o ungi and soil ungi composi ion o he D y A omon ane chu ch o es
sys ems o No hwes e n E hiopia espec i ely. In he hi d pape , he e ec s o
abo eg ound ege a ion, clima ic, spa ial and edaphic a iables on he communi y
composi ion, di e si y and ichness o o al mac o ungi as well on unc ional g oups a e
discussed. In pape IV, he impac s o he a iables indica ed in pape III on he
communi y composi ion, di e si y and ichness o soil ungi and unc ional guild a e
s udied. The indings ha e implica ions o he sus ainable conse a ion and use o bo h
he na u al and plan a ion o es s in E hiopia h ough mycosil icul u al managemen
app oaches. Also, he conse a ion o biological di e si y o he o es sys em h ough
he p o ision o complemen a y income o he local communi ies h ough spo oca ps
p oduc ion was emphasized. The axa composi ion is also explained in e ms o edaphic
a iables, s and age, ege a ion ypes and clima ic a iables. Concep ual map o he
s udy including he ou s udies is shown below (Fig. 1).
Ou line o he hesis
x iii
Figu e 1: Concep ual map o he hesis including he 4 s udies
In oduc ion
In oduc ion
1
1. In oduc ion
1.1. Clima e, Geology and Ecology o E hiopia
E hiopia is si ua ed in cen al pa o he ho n o A ica and i is a land locked
coun y which spans 30 24' o 140 53'N and 330 00' o 48° 00'E, encompassing
app oxima ely 1270 kms in No h-sou h and 1650 kms in Eas -wes di ec ions. The
coun y has a ied opog aphy anging om 123 m below sea le el o 4533 m abo e
sea le el and majo i y o a ea ha e > 2000 m ele a ion unlike o he coun ies in A ica
(F iis e al., 2010). The mean annual ain all anges om 500 o 2800 mm and
empe a u e 10oC o 30oC (Demissew and No dal, 2010). The highland o he coun y is
dissec ed by he Eas A ican i alley. The oldes ocks in E hiopia a e pa o he
c ys alline basemen , which is p e-Camb ian in o igin. The o iginal igneous and
sedimen a y ocks a e in e blended wi h schis s and gneisses and subsequen igneous
in usions. The whole sys em is e e ed o as he basemen complex (F iis e al., 2010).
Fu he mo e, he coun y is an ecologically di e se coun y owing o he a ied
opog aphic ea u es and al i udinal a ia ions (Geb e sadik, 2016).
1.2. Na u al o es s in E hiopia
Acco ding o F iis e al. (2010), he ege a ion o E hiopia is classi ied in o 12
ypes based on he ele a ion zones in which hey occu ed: (1) Dese and semi-dese
sh ub land, (2) Acacia-Commipho a woodland and bush land, (3) Wooded g assland o
he Wes e n Gambela Region, (4) Comb e um-Te minalia woodland and wooded
g asslands, (5) D y A omon ane o es and g asslands complex, (6) Mois A omon ane
o es , (7) T ansi ion ain o es , (8) E icaceous bel , (9) A oalpine ege a ion, (10)
Ri e ine ege a ion, (11) F esh wa e , lakes, lakes sho es, ma shes, swamps and lood
plain ege a ion and (12) Sal -wa e , lakes, lakes sho es, sal ma shes and plain
ege a ion.
The na u al high-ele a ion o es s (Fig 2), ha include he A omon ane
ege a ion, a e exclusi ely ound in he highland egions o E hiopia be ween 1500 o
In oduc ion
2
3400 m abo e sea le el (Lemenih and Bekele, 2008) ha occupy mo e han 44% o he
coun y’s land a ea (Kidanu, 2004; McCann, 1995). D y A omon ane o es s is a
complex ecosys em cha ac e ized by high humidi y, a a iable ain all pa e n, and a
p olonged d y season (F iis e al., 2010). These o es s p o ide impo an ecosys em
se ices such as wa e shed p o ec ion and ca bon seques a ion (Wassie e al., 2005).
The dominan ee species in hese o es s a e Junipe us p oce a, Podoca pus alca us,
Hagenia abyssinica and Olea a icana, which a e he main sou ce o imbe in he
coun y. These o es s also ha bou a ious ypes o non- imbe o es p oduc s (Fig
2B), including wild edible mush ooms (Dejene e al., 2017b).
Figu e 2: The na u al o es s (A) and he collec ed non imbe o es s p oduc s (B) in
E hiopia
High le els o his o ical human landscape al e a ion and land-use p essu e ha e
esul ed in widesp ead de o es a ion and he deg ada ion o E hiopian o es s (Ae s e
al., 2016; Aynekulu e al., 2016; Da byshi e e al., 2003; Nyssen e al., 2014). A ecen
e iew o o es y in E hiopia e ealed ha de o es a ion is a con inuous p ocess
(Geb u, 2016). When all o es ypes we e included, a de o es a ion a e o 0.93% pe
yea was calcula ed in 2010 (FAO, 2020; Zewdie e al., 2010). The e e -inc easing
demand o wood p oduc s as well as c op and g azing land expansion, s imula ed by
apid popula ion and li es ock g ow h a e he ac o s agg a a ing he deg ada ion o he
D y A omon ane o es s in he coun y (Bekele and Lemenih, 2008). Human-induced
i e is also one o he mos impo an easons o he deple ion and deg ada ion o
na u al esou ces in E hiopia (Lemenih and Bekele, 2008; Wassie e al., 2005). Fi e is
mo e common in he highland a eas, whe e he d y A omon ane o es is ound, and
In oduc ion
3
has a di ec impac on he biodi e si y in he o es ecosys em (Lemenih and Bekele,
2008). As a esul , many physical and biological changes ha e occu ed in hese o es
sys ems in No he n E hiopia. These o es cu en ly a e he mos agmen ed
ecosys ems (Dessie, 2007; Lemenih and Bekele, 2008; Miles e al., 2006; Wassie e al.,
2010). Loss o biodi e si y could also occu in he o es soil, which ha bou s a g ea
di e si y o mic obial o ganisms (Fie e and Jackson, 2006), including ungi. Depending
on he se e i y and equency, i e could di ec ly o indi ec ly a ec edaphic a iables in
he o es ecosys em (Reazin e al., 2016), which in u n could ha e an impac on ungal
communi ies dwelling in he soil (Cai ney and Bas ias, 2007; Dahlbe g e al., 2001;
Rincón and Pueyo, 2010).
Figu e 3: The agmen ed D y A omon ane chu ch o es s in No he n pa o E hiopia
S udies ha e e alua ed he conse a ion alue o agmen ed o es s in he
No he n landscapes o E hiopia (Ae s e al., 2016; Aynekulu e al., 2016; Wassie e al.,
2010, 2005; Nyssen e al., 2014). Mos o hese agmen o es s su i e in he
landscape because o he cul u al o eligious alues held by local communi ies ha a e
ound as o es islands (Aynekulu e al., 2016). These o es s belong o he chu ch o
a e loca ed a ound chu ch o es e i o ies (Ae s e al., 2016; Aynekulu e al., 2016;
Wassie e al., 2009) (Fig 3). Fo es agmen a ion a ec s biodi e si y (Lemenih and
Bonge s, 2011; Wassie e al., 2005) and he popula ion iabili y in he long- e m
(Fe nández e al., 2020). The condi ion p obably e lec ed on he ungal communi ies
cons i u ing he o es s sys ems. Addi ionally, he o es agmen a ion impac s soil
In oduc ion
10
ungal species (56) had been e alua ed o he In e na ional Union o conse a ion o
Na u e (IUCN) Red Lis compa ed o plan s (25,452 species) and animals (68,054)
(Kew, 2018). Despi e ecen ad ances in de e mining he di e si y and composi ion o
o es ungi in a ious biomes, undamen al ques ions ega ding hei dis ibu ion and
unc ion, and he ac o s ha in luence hem emain unanswe ed, pa icula ly in unde -
sampled biomes (Guo e al., 2013; K ashe ska e al., 2015). The majo i y o soil ungi
a e unexplo ed and, he unc ional ela ionship be ween ungi, soil, and plan s emains
unde s udied (B idge and Spoone , 2011; an de Heijden e al., 2008). P e ious
in es iga ions ha e es ima ed ha he e a e abou 5.1 million ungal species wo ldwide
(Taylo e al., 2014). O hese, 2–6% ha e been desc ibed (O’B ien e al., 2005) and
~1200 new species a e desc ibed each yea (Hibbe and Tho n, 2001), indica ing ha
he e a e many mo e ungal species o be explo ed, named, and iden i ied.
Fu he mo e, o da e, mos s udies o soil ungal communi ies ha e ocussed on
empe a e and Medi e anean o es ecosys ems; less conside a ion has been gi en o
soil ungal communi ies in opical o es ecosys ems (Taudiè e e al., 2017). The e o e,
u he s udies a e equi ed o inc ease ou unde s anding o he dynamics o soil ungi
and hei communi y s uc u e (Dh uba e al., 2015) and he impac o a ious
en i onmen al and an h opogenic ac o s. Also, mos s udies o soil ungal communi ies
cu en ly ha e ocussed on empe a e and Medi e anean o es ecosys ems; less
conside a ion has been gi en o soil ungal communi ies in opical o es ecosys ems
(Taudiè e e al., 2017). The e o e, u he s udies a e equi ed o inc ease ou
unde s anding o he dynamics o soil ungi and hei communi y s uc u e (Dh uba e
al., 2015) and he impac o a ious en i onmen al and an h opogenic ac o s.
On he o he hand, ungi a e acing h ea s ela ed wi h clima e change, pollu ion,
o e -exploi a ion, and habi a des uc ion and agmen a ion (Dahlbe g e al., 2010;
Kew, 2018). Despi e hese, he ungi a e o en neglec ed in conse a ion due o
knowledge gap be ween mycologis s and conse a ionis s in ungal dis ibu ional and
ecological da a. This p oblem is mo e complica ed mainly due o he in isible,
inde e mina e o m and hei endency o swi ch be ween o ms (Dahlbe g and Muelle ,
2011). Al hough he no iceable and abundan spec acles o ui ing s uc u es o ungi
In oduc ion
11
(e.g. mush ooms) p oduced by some ungal species, in gene al ungi a e di icul o
iden i y and coun since, when no ui ing, mos a e composed o no hing mo e
subs an ial han a wispy ne wo k o mycelium. Fungi he e o e con ain a g ea , and ye
la gely obscu ed, p esence wi hin soil and inside o he li ing hings (Kew, 2018). This
makes hem di icul subjec s o cha ac e ize, su ey, and moni o hem. Fo una ely, a
gene al shi owa ds conse ing whole ecosys ems is now unde way due o hei
ecological impo ance in nu ien cycling (Heilmann-Clausen e al., 2015). In gene al,
long- e m and la ge-scale da a, da a om opical, expe imen al da a om ungi
associa ed wi h ees and da a om mul iple simul aneous d i e s o change o ungal
communi y change a e he majo in o ma ion gaps on global ungal esou ces (Kew,
2018).
1.8. O e iew o mycological s udies in E hiopia
Despi e agmen a ion and de o es a ion, s udies ha e e alua ed he
conse a ion alue o di e en o es s in he D y A omon ane egions in E hiopia (Ae s
e al., 2016; Aynekulu e al., 2016; Nyssen e al., 2014; Wassie e al., 2010). Mos o
hese s udies ocused on he abo e s o y componen s o hese o es sys ems and e y
limi ed numbe s o s udies ha e in es iga ed ungal communi ies om he D y
A omon ane egion o E hiopia. These s udies we e ocused on abo e-g ound ungal
communi ies (Dejene e al., 2017a) while he soil ungal communi ies associa ed wi h
he d y A omon ane o es s in E hiopia a e undesc ibed. Fu he mo e, he po en ial
e ec o i e, edaphic, abo eg ound ege a ion, clima e and spa ial a iables on soil
ungal communi ies in hese ecosys ems has no ye been e alua ed. Limi ed ocuses
ha e been gi en o he ecology and conse a ion s a us o he soil ungal and
mac o ungal di e si y o he D y A omon ane o es s sys em despi e hei wide
dis ibu ion in he coun y. Consequen ly, he ungal axonomy and ecology a e e y
poo ly desc ibed and, hence, ungi a e neglec ed when decisions need o be made
ega ding o es managemen and conse a ion ac ions in his egion.
P e ious s udies conduc ed on plan a ion o es esou ces in he D y
A omon ane egions o he coun y ocused on ways o assis he managemen and
In oduc ion
12
de elopmen o hese plan a ions o wood p oduc s. The s udy o soil ungal
communi ies in hese o es sys ems in he D y A omon ane egion is sca ce. Recen ly,
Cas año e al. (2019) in es iga ed he soil ungal communi y and ecological guilds
associa ed wi h Eucalyp us g andis plan a ions in E hiopia. Howe e , cu en ly he e has
been an in e es in su eying ungi in pa icula habi a s (Alem e al., 2020b), o desc ibe
and p edic he ex en o hei di e si y on a la ge scale (Danielsen e al., 2005; Peay,
2014). Howe e , s udies on he soil mic obial communi y, including ungi associa ed
wi h Pinus plan a ions, a e e y limi ed. Spo oca ps associa ed wi h a P. pa ula
plan a ion du ing a single ainy season ha e p e iously been epo ed (A e ill e al.,
2014). Al hough spo oca ps ep esen a unique s ep in he complex li e o ungi (A e ill
e al., 2014), hey do no e lec he en i e soil bio a (O ega-Ma ínez and Ma ínez-
Peña, 2008).
Abo eg ound ege a ion a ec s he communi y composi ion and di e si y o
ungi. The p ac ice o using plan communi ies as su oga es o p edic ungal di e si y
has been epo ed by p e ious s udies (McMullan-Fishe e al., 2010; Rudol e al.,
2013). Despi e agmen a ion, he o es s in he s udy a eas a e sugges ed o be
ela i ely ich in plan species (Ae s e al., 2016; Wassie e al., 2010). The ee species
composi ion o he agmen ed o es s also a ied wi h hei s a us, opog aphy and
al i ude (Bonge s and Tenngkei , 2010), wi h a wide dis ibu ion o e he landscapes
(Ae s e al., 2016). Howe e , he e is no e idence ha he high le el o plan di e si y in
he chu ch D y A omon ane o es s sys em an icipa es co espondingly high
mac o ungal di e si y. Mo eo e , he e is no in o ma ion on how habi a agmen a ion
may a ec ungal communi ies o limi ungal p ocesses is ela i ely limi ed (Edman e
al., 2004; G illi e al., 2012; Mangan e al., 2004). In addi ion, as ye , he en i onmen al
a iables ha go e n ungal communi ies in hese agmen ed o es sys ems ha e no
been iden i ied gi en ha hese o es s a y in hei s a us (size, densi y, species
composi ion e c.), opog aphy and al i ude (Bonge s and Tenngkei , 2010).
P e ious s udies in E hiopia ha e been ocused on e hnomycological knowledge
and mush oom consump ion habi o he local people, di e si y and communi y
composi ion o mac o ungi and soil ungi. Mo e a en ion has been gi en o s udies on
In oduc ion
13
AMF associa ions and edible ungi. Less emphasis was gi en o o al ungal s udies,
bo h abo e g ound and below g ound. In e ms o s udy loca ions, mo e s udies we e
conduc ed in sou he n E hiopia (Alem e al., 2020a; Beenhouwe e al., 2015; Cas año
e al., 2019; Chauhan e al., 2019; Dejene e al., 2017b, 2017a; Dobo e al., 2018b,
2018a, 2016; Hailema iam e al., 2013; Mege sa e al., 2017; Michelsen, 1993; Mule a
e al., 2013, 2008; Sewne and Tuju, 2013; Tuno, 2001; Wube e al., 2009) ollowed by
no h E hiopia (Bi hane e al., 2018b, 2018a, 2017a, 2012, 2010; Delelegn e al., 2018;
Weldeki os e al., 2017; Welema iam e al., 2018). No hwes e n and cen al E hiopia
had been gi en less a en ion in mycological s udies. Since E hiopia has di e si ied
clima ic, ege a ion, opog aphic and edaphic ea u es (F iis e al., 2010; Geb e sadik,
2016) which in u n a ec he ype o ungi ha exis in he a ea (Semwal e al., 2014)
addi ional s udies in unde s udied a eas o he coun y a e equi ed.
Loca ion speci ic s udies ca ied ou in E hiopia showed he exis ence o huge
po en ial o mush ooms (Aba e, 1999; Weldeki os e al., 2017) and high species numeb
pe uni a ea (Dejene e al., 2017a). These s udies also indica ed he po en ial o he
esou ces o he sus ainable managemen o o es esou ces and con ibu ion o ood
secu i y o he local communi y li ing a ound hese o es s in gene al. I was also
indica ed ha mo e numbe o mac o ungal species and new ones can be explo ed i
di e en o es sys ems a e included (Dejene e al., 2017b, 2017d; Mege sa e al.,
2017). In many coun ies, edible wild mush ooms ha e been iden i ied, cul i a ed and
inco po a ed as s aple oods (Boa, 2004) and ex ensi e collec ions and he ba ium da a
ha e also been documen ed (Beluhan and Ranogajec, 2011). Howe e , in E hiopia he
mush oom cul i a ion p ac ices and consump ion is e y low compa ed o o he
coun ies in Eu ope and Asia (Geb elibanos e al., 2016) despi e he coun y possesses
nume ous species o wild mush ooms (Aba e, 1999; Weldeki os e al., 2017). The o es
managemen in he coun y neglec ed such impo an esou ces. The o e all e iew o
he a ailable published da a indica ed ha , s ill he e is a gap in quan i ying he ungal
di e si y o he coun y (Dejene e al., 2017d).
In oduc ion
14
1.9. Why he cu en s udy?
Sus ainable de elopmen hough he conse a ion o na u al esou ces is a majo
challenge o de eloping coun ies like E hiopia. E hiopia is men ioned as one o he
coun ies ich in di e se plan and animal species (Geb e sadik, 2016). Howe e , he
o es esou ce o he coun y a e anishing a an ala ming a e because o a ious
easons such as high human and animal p essu e and unsus ainable use o o es
esou ces (Geb u, 2016). To a e he p oblem, di e en o es de elopmen
app oaches ha e been ied and symbolic achie emen s ha e been eco ded in some
locali ies (Winbe g, 2011). Howe e , many emnan na u al o es s in E hiopia ha e
been closed as “ ese e o es s” o p omo e he conse a ion o he na u al o es s.
Plan a ion o es s especially as g owing ee species ha e been in oduced in he
coun y and plan ed mainly o uelwood and imbe . Howe e , in he managemen o
E hiopian o es s, he alue o o es esou ces o he han imbe ha e been o e looked
(Desalegn and Tadesse, 2004) and he NTFPs such as mush oom a e no included in
o es managemen plan o bo h na u al and plan a ion o es s esou ce o he coun y
despi e hei po en ial con ibu ion o he sus ainable managemen o o es ecosys ems
(Amma e al., 2018) and ensu ing ood secu i y o he na ion. Because o his p oblem
sus ained de o es a ion and deg ada ion has been eco ded in E hiopia (As aw and
E e a, 2017). De ising cheap and e hically widely accep ed inocula p oduc ion me hods
and be e ways o managemen o e ec i e es o a ion o deg aded lands will also
emain o be impo an esea ch a eas (Asmelash e al., 2016). The e o e, al e a i e
o es managemen app oaches ha b ing economic bene i s o he local communi y
and p o ides in e media e income om o es esou ces (Melesse and Ab ew, 2015) a e
impo an o he sus ainable managemen o E hiopian o es esou ces (Yada and
Mekonnen, 2013). One o hese al e na i e o es managemen in e en ions is he use
o NTFPs such as gums and esin, wild honey, medicinal plan s and ungi/mush ooms.
Howe e , he ungal esou ces and he adi ion o mush oom consump ion a e being
disappea ing pa allel wi h he o es esou ce o he coun y (Weldeki os e al., 2017).
These esou ces a e also unde dynamic change due o se e habi a deg ada ion in
he coun y (Dejene e al., 2017d).
In oduc ion
15
Re iew o exis ing li e a u e on ungal s udies o he coun y indica ed ha he
ungal esou ce o he coun y is poo ly s udied, documen ed and no p ope ly u ilized.
This implies he need o conduc ing mo e de ailed and wide scale ungal s udies o
documen he ungal esou ce o he coun y including ungal communi y composi ions,
mush oom p oduc ion and d i ing ac o s o hei dis ibu ion (Dejene e al., 2017d).
Such in o ma ion will help o de ise s a egies o he sus ainable managemen and
u iliza ion (Hailema iam e al., 1990), o mula e e ec i e and in eg a ed policies, p o ide
p io i ized managemen ecommenda ions (Dahlbe g e al., 2010) o hese esou ces.
Conse a ion o biodi e si y depends on eliable in o ma ion abou he kinds o
o ganism p esen , o al numbe o species in each o hese g oup, hei gene ic
di e si y, hei habi a s, dis ibu ion pa e n, ecology, popula ion size, e olu iona y
his o y, and hei ends bo h in ime and space (Bhanda i and Jha, 2018). The
biodi e si y da a o ungi a e use ul indica o s o assess he cu en s a us o an
ecosys em and impo an o main aining and managing he ecosys em o a o es .
I was in he ligh o his backg ound in o ma ion ha he p esen s udy was
conduc ed in di e en ag o-ecologies and di e en o es sys ems o E hiopia so as o
gene a e aluable in o ma ion on o al species ichness, abundance, di e si y, e enness
and composi ion o soil and mac o ungi communi y and ac o s a ec ing hese. Due o
he key ecological ole ha ungi play in ecosys em unc ioning, he in o ma ion abou
how ecological ac o s a ec he ungal communi ies in he chu ch agmen ed o es s
can be c ucial o enable he in eg a ion o hese o es s in o global biodi e si y
conse a ion s a egies and o unde s and wha ac ions mus be unde aken o
conse e hese o es s, and hei biological componen s. In o ma ion gene a ed om
his esea ch is belie ed o help design conse a ion and sus ainable use o ungi in
pa icula and o o es esou ce o E hiopia in gene al. The ou pu o he esea ch will
also add aluable in o ma ion o he local, na ional and global ungal communi y
di e si y. I will also con ibu e o he achie emen o na ional en i onmen al and o es
ela ed goals as well as o he na ional GDP, ood secu i y o he na ion and he
coun y’s ision o become middle income coun y by 2030. This esea ch in line wi h
he in e na ional and na ional de elopmen s a egies o he coun y such as Clima e
In oduc ion
16
Resilien G een Economy o E hiopia, Millennium De elopmen Goals, and Fo es
Sec o de elopmen o E hiopia, G ow h and ans o ma ion plan o E hiopia and o he
o es ela ed na ional and in e na ional con en ions.
Thus, s udy he e ec o a ious en i onmen al a iables soil on he ungal
communi y composi ion and spo oca ps p oduc ion in di e en ecosys ems is o
pa amoun impo ance o ha e a gene al unde s anding o p ocesses in he o es s
ecosys ems (Hanson e al., 2012; Haza d e al., 2013) o se up hei managemen and
conse a ion s a egies. In es iga ing he ungal communi y composi ion and how his
communi y changes ac oss si es in agmen ed o es s should help us o unde s and
di e en aspec s o ungal in e ac ion wi hin hese sys ems and hei unc ion in he
ecosys em (Gene ie e e al., 2019). This in o ma ion would also enable he in eg a ion
o agmen ed o es s in o global biodi e si y conse a ion s a egies (Hunde a e al.,
2013; Ae s e al., 2016; Aynekulu e al., 2016) and o unde s and wha ac ions a e
equi ed o conse e hese o es sys ems hei biological componen s, including ungi
(Bu gess e al., 2006). Fu he mo e, he mac o ungal s udy in agmen ed D y
A omon ane o es s is also a means o unde s and how o imp o e na u al ungal
ichness and spo oca p p oduc ion and help us o acili a e he conse a ion o
economically and ecologically impo an mac o ungal species in hese agmen ed high
p io i y o es sys ems. Such in o ma ion could help o guide managemen and
conse a ion s a egies o hese p io i y o es s and supplemen ou knowledge o
mac o ungal species in E hiopia. Simila ly, he knowledge o ungi and hei communi y
s uc u e in ela ion o di e en age ca ego ies o plan a ion o es s also helps o
de e mine p ope managemen s a egies o plan a ion o es in E hiopia. Fu he mo e,
knowledge o he edible mush ooms p oduced in hese o es s could p o ide an
oppo uni y o ha es ing edible mush ooms o ei he subsis ence o comme cial use.
1.10. Hypo heses and esea ch ques ions
In ou s udy ega ding he e ec o i e on soil ungal communi y composi ion and
di e si y, we hypo hesized ha he ichness and composi ion o he en i e and unc ional
soil ungal communi ies would change subs an ially du ing a pos - i e o es succession
In oduc ion
17
and would di e om hose in unbu ned o es and he communi y u no e would
pa ially be explained by edaphic a iables. As a consequence, we expec ed ude al,
gene alis sap o ophic ungi be mo e abundan and species- ich sho ly a e i e han in
unbu ned o es s. By con as , oo -associa ed symbio ic ungi we e expec ed o be
mo e di e se in olde bu ned o es s and unbu ned o es s.
In ou soil ungal s udy unde P. pa ula plan a ion, we hypo hesized ha
subs an ial change in he composi ion o soil ungal communi ies would be de ec ed
along he ch onosequence o P. pa ula plan a ions. Speci ically, we hypo hesized ha
he e would be changes in he o al and unc ional ungal di e si y and communi y
composi ion along he ch onosequence o he plan a ions.
In ou mac o ungal and soil ungal s udies in he h ee agmen ed chu ch o es s
o he D y A omon ane a eas in No h E hiopia, we hypo hesized ha he ungal
di e si y o he chu ch o es s would be high in e ms o o al ungal species and
unc ional s a us gi en ha ungal di e si y is ela ed posi i ely o plan ichness
(Tede soo e al., 2014b). We also hypo hesized ha he composi ion o mac o ungal
communi ies would di e among he s udied o es s, esul ing in an o e all highe
ichness alue o he s udy si es and hei communi y composi ion is d i en by
ege a ion and si e condi ions such as soil e ili y (Cas año e al., 2018; Vašu o á e al.,
2017), clima ic and spa ial a iabili y (Glassman e al., 2017; Li e al., 2020; Tede soo e
al., 2014a; Tede soo e al., 2014b).
1.11. Scope o he s udy
To ou knowledge, his esea ch is he i s sys ema ic a emp s ocused o
desc ibe he ungal communi ies’ s uc u es and spo oca p p oduc ion in agmen ed
o es s in D y A omon ane egion o E hiopia in ela ion o mul iple en i onmen al
ac o s such as o es i e, ascula plan di e si y, edaphic cha ac e is ics, clima ic and
o he spa ial a iables. This esea ch is also he i s a emp o desc ibe he soil ungal
communi y composi ion in ela ion o s and de elopmen s age o P.pa ula plan a ion
unde E hiopian condi ion. The ield s udies in he D y A omon ane o es s we e based
In oduc ion
18
bo h on soil ungal sampling and spo oca p collec ions. Spo oca p collec ions we e
done du ing he pick ainy season o he yea in he s udied o es s. Howe e , he s udy
was conduc ed du ing he main ainy season o a single yea in he D y A omon ane
o es s and P.pa ula plan a ion in E hiopia. The e o e, i s wide applica ion in o he
o es sys ems o he coun y shall be aken wi h cau ion. Long e m sampling pe iod
and wide scale s udies a e equi ed o know mo e abou he ungal esou ce o he
coun y. Howe e , he esul s p o ide ele an in o ma ion o de eloping sus ainable
managemen s a egies o D y A omon ane o es s in E hiopia by in eg a ing
ungi/mush ooms which in u n help o conse e hese o es sys ems and hei
biological componen s, including ungi. The s udy on spo oca ps including edible
mush ooms in agmen ed chu ch o es s could also p o ide an oppo uni y o
ha es ing edible mush ooms o ei he subsis ence o comme cial use and help o
sus ainable managemen o hese o es sys ems.
Objec i es
Ma e ial and Me hods
26
Wondo Gene na u al o es a ea, whe e he s udy on soil ungal communi y in
ela ion o i e conduc ed, co e s abou 797 ha o na u al o es s land (Ango and
Bewke , 2007; Belaynesh, 2002; Fen a, 2014). The o es is cha ac e ized by emnan
D y A omon ane o es pa ches (Ango and Bewke , 2007; Belaynesh, 2002; Fen a,
2014) and ha bou s impo an auna and lo a (Belaynesh, 2002; Fen a, 2014). The
clima e is cha ac e ized by he Weyna-Dega ag o-clima ic zone, wi h a bimodal ain all
pa e n: he main ainy season is in he summe and a lesse ainy season is in sp ing
(Belay, 2016; Fen a, 2014). Pa o he na i e ege a ion in Wondo Gene s udy si es,
whe e he s udy on e ec o P.pa ula s and age on soil ungal communi y and di e si y
conduc ed (Fig. 6), was des oyed o cul i a ion (Teshome, 2011). In ecen decades, a
mass plan ing scheme o exo ic ee species has been unde aken on hose a eas and
esul ed in app oxima ely 100 ha o non-na i e plan a ions o Cup essus lusi anica,
G e illea obus a and P. pa ula (Bekele e al., 2013; Teshome, 2011).
Figu e 6. Plan a ion o Pinus pa ula whe e soil ungal da a was collec ed (pho o c edi ,
Dejene e al., 2017)
Figu e 7. D y A omon ane o es s (A,Wondo Gene ; B, Ta agedam; C,Alemsaga; D,
Banja) selec ed o ou s udy (pho o c edi :7A, Dejene e al., 2017; 7B-7D, Demelash
Alem)
Ma e ial and Me hods
27
The Ta agedam (Fig. 7C) and Banja (Fig. 7D) o es s we e designa ed as
ese es in 1979 (Zegeye e al., 2011) and 1994 (Abe e e al., 2017), espec i ely, o
p e en any kind o enc oachmen s. The Alemsaga o es (Fig. 7B) was designa ed as a
p io i y o es in 1978 o se e as a seed sou ce, o conse e he emnan na u al o es ,
and o ehabili a e he deg aded a ea in he No he n pa o he coun y (Mas esha e
al., 2015). Desc ip ions o he s udy o es s a e p o ided in Table 1.
Table 1. Cha ac e is ics o he s udy si es
Desc ip ions
Fo es s
Ta agedam
Alemsaga
Banja
Wondo Gene
Geog aphical loca ion
12°06'–12°07'
N 37°46'–
37°47' E
11°54'–11°56'N
37°55'–37°57'E 10°57'–11° 03'N
36°39'– 36°48'E
7°06' –7°07' N
38°37' –38°42' E
Al i ude ange (m asl)
2142–2484
2180–2470
1870–2570
1600-2580
Mean annual p ecipi a ion
(mm)
1098 1926 1884.3
1210
Mean annual empe a u e
(°C)
19.5 15.8 18.7
20
Fo es a ea (ha)
875
814
897
797
Sand (%)
58.89(2.93)
51.78(2.99)
68.67(2.21)
56.55(2.14)
Sil (%)
28.44(2.38)
32.44(2.13)
20.00(1.76)
20.83(1.87)
Clay (%)
12.67(1.37)
15.78(1.93)
11.33(1.33)
23.23(1.81)
pH H2O 1:2.5
7.04(7.03)
5.85(6.59)
5.60(6.24)
6.46(0.12)
EC (dS/m)
0.43(0.05)
0.28(0.03)
0.81(0.14)
0.17(0.03)
Ex.Ca (cmol(+)/kg)
13.95(0.60)
9.19(0.52)
13.55(0.87)
22.03(2.48)
Ex.Mg (cmol(+)/kg)
6.16(0.10)
4.58(0.15)
5.54(0.20)
7.49(0.89)
Ex.Na (cmol(+)/kg)
1.95(0.05)
2.05(0.10)
1.82(0.12)
0.97(0.09)
Ex.K (cmol(+)/kg)
0.73(0.06)
0.61(0.04)
0.77(0.06)
0.60(0.07)
CEC (cmol(+)/kg)
47.21(1.36)
34.89(0.92)
44.51(1.96)
42.8(3.25)
O ganic ma e (%)
4.46(0.60)
3.35(1.34)
4.87(0.10)
9.14(1.03)
Ni ogen (%)
0.23(0.01)
0.17(0.02)
0.26(0.01)
0.49(0.05)
P (ppm)
17.18(5.72)
7.8(0.73)
17.64(6.05)
32.38(2.85)
Dominan species
in each plo s
May enus
obscu a,
Ca issa edulis,
Olea sp.
Acacia
abyssinica,
Buddleja
polys achya,
Acacia nilo ica
Albizia
gummi e a,
P unus a icana,
B ucea
an idysen e ica
Junipe us
p oce a,
Podoca pus
alca us, Hagenia
abyssinica Olea
a icana
Re e ences
Gede aw and
So omessa
(2014) Zegeye
e al. (2011)
Ze ihun e al.
(2013)
Bi hane e al.
(2017)
Mas esha e al.
(2015) Wube e
al. (2004)
Abe e e al.
(2017)
(Alem e al.,
2020a;
Belaynesh, 2002;
Cos a e al.,
2014)
No e: Numbe s in pa en heses a e s anda d e o o he mean
Ma e ial and Me hods
28
3.3. Es ablishmen o ield plo s
Plo s in D y A omon ane na u al o es s (s udy I) and plan a ions o P. pa ula
(s udy II) o Wondo Gene s udy a ea we e es ablished by conside ing he simila i y o
he a eas in clima e, al i ude, soil and o he ecological condi ions. We used he
in o ma ion om he Depa men o Fo es Managemen in Wondo Gene College o
Fo es y (WGCF) o ind a eas wi h simila i e his o y in na u al o es s and s and ages
classes in plan a ions. The plo s es ablished in Ta agedam, Alemsaga and Banja
o es s (s udy III and IV) we e based on hei his o y and he composi ion o ascula
plan s. Field obse a ions and published da a sou ces we e used o desc ibe he si es.
Wi hin each o he selec ed a eas in all s udies, plo s we e placed sys ema ically
(Luoma e al., 1991) a enough om each o he in o de o p o ide ela i ely
independen es ima es as possible.
3.3.1. Plo es ablishmen in D y A omon ane o es s o s udy soil ungal
communi y composi ion and di e si y in ela ion o o es i e (s udy I)
Sample plo s we e es ablished in he o es in 2015. The con ol s and o
unbu ned na u al o es (UB) was ep esen a i e o he o iginal na u al o es and had
no been a ec ed by i e o a leas 40 yea s. Bu ned s ands selec ed o he s udy
we e simila in e ms o i e se e i y, i.e., he canopy and unde s o y had bu ned and he
soil o ganic laye had been consumed (Rincón and Pueyo, 2010). In hese bu ned
a eas, wo o es s ands we e selec ed based on i e his o y: (1) one-yea -old bu ned
o es (B1); and (2) en-yea -old bu ned o es (B10). Wi hin each o hese o es s ands,
h ee ansec s (a o al o 9 plo s) we e es ablished abou 250 m apa om each o he .
Each ansec co e ed an a ea o 100 m2, wi h a ec angula shape (2 m × 50 m).
3.3.2. Plo es ablishmen in P. pa ula plan a ion o es o di e en age o s udy he
soil ungal communi ies and succession (s udy II)
In P. pa ula plan a ions, s ands o h ee di e en age g oups (5-, 11- and 36-
yea s-old s ands) we e selec ed and h ee 2 m × 50 m plo s we e es ablished in each
age ca ego y (Gassibe e al., 2011) o soil sampling bo h o molecula wo k and o
Ma e ial and Me hods
29
soil physico-chemical analysis. A minimum dis ance o abou 120 m was used be ween
plo s wi hin a s and (Luoma e al., 1991).
3.3.3. Plo es ablishmen o s udy spo oca ps di e si y and p oduc ion (s udy III)
and soil ungal communi y composi ion and di e si y (s udy IV) in
agmen ed chu ch o es s in D y A omon ane o es sys ems in No he n
E hiopia
In o al, 27 sample plo s we e es ablished, nine in each o he h ee chu ch
o es s, as desc ibed in Gassibe e al. (2011) and (He nández-Rod íguez e al., 2013).
Each plo was ec angula in shape (2 m × 50 m). Wi hin each o he selec ed chu ch
o es s, we s udied h ee di e en si es including h ee plo s pe si e. The plo s we e
es ablished abou a minimum dis ance o 500 m apa .
3.4. Sampling
3.4.1. Spo oca p sampling (s udy III)
All ungal ui bodies ound in each plo we e ha es ed weekly. F esh weigh
measu emen s we e aken in si u o de e mine ui body p oduc ion in kilog ams pe
hec a e pe yea . The numbe o indi iduals o each species in each plo was also
eco ded. Specimens we e pho og aphed in he ield and hei mo phological ea u es
and ecological cha ac e is ics we e no ed o acili a e axonomic iden i ica ion p ocesses
in he labo a o y (Adeniyi e al., 2018). Specimens o each mac o ungus we e aken o
he labo a o y and d ied o p ese e as he ba ia specimens, and hen used o
mo phological axa iden i ica ion.
3.4.2. Soil sampling o DNA ex ac ion (S udy I, II & IV)
Fi e co es we e ex ac ed in each plo using a cylind ical (2 cm adius, 20 cm
deep, 250 cm3) soil bo e (De la Va ga e al., 2012; Taylo , 2002) along he cen e line
o each ansec and 5 m apa o collec spa ial a iabili y and minimize he p obabili y
o sampling he same gene epea edly. Soil sample co es om each plo we e pooled
Ma e ial and Me hods
30
o o m a composi e sample o DNA ex ac ion. Soil co es we e d ied, sie ed h ough a
1 mm mesh and g ounded o a ine powde using a mo a and pes le. A subsample
was s o ed a -20ºC un il submi ed o molecula analysis.
3.4.3. Soil sampling o physico-chemical analysis (S udies I, II, III & IV)
To ela e soil ungal composi ion o edaphic a iables, addi ional soil samples
we e collec ed om each ansec s. Soil samples, om he cen e and om he ou
co ne s o each plo in each s udy, we e ex ac ed o a dep h o 20 cm wi h he aid o an
auge and spade a e clea ing plan ma e and deb is. A composi e soil sample o
app oxima ely 500 g om each plo was placed in a plas ic bag and anspo ed o he
labo a o y o he de e mina ion o edaphic a iables.
A e ai d ying he soil in shade, impo an chemical and physical p ope ies o
he soil we e de e mined using DTPA ex ac ion, KH2PO4 ex ac ion, Olsen, Kjeldahl
diges ion, Walkley–Black, ammonium ace a e and ins umen al me hods espec i ely.
The analysis was conduc ed by Wa e Wo ks Design and Supe ision En e p ises,
labo a o y se ice sub p ocess, soil e ili y sec ion a Addis Ababa, E hiopia (S udies I
and II) and Amha a Design and Supe ision Wo ks En e p ise a Bahi Da , E hiopia
(s udies III & IV). Main edaphic a iables o he na u al o es in Wondo Gene (Table 1
in s udy I), P. pa ula s ands (Table 1 in S udy II) and chu ch o es s o agmen ed
na u al o es s o in No he n E hiopia (Table 1 in s udy III & Table 1 in s udy IV) a e
summa ized.
3.4.4. Vege a ion and clima e da a collec ion (S udies III & IV)
To ela e he ege a ion cha ac e is ics o mac o ungal (s udy III) and soil ungal
(s udy IV) ichness and di e si y, ege a ion in en o ies we e conduc ed in he plo s
es ablished o ungal sampling. Vascula plan iden i ied in each plo s we e eco ded
using hei e nacula names. Fo hose species di icul o iden i y hei scien i ic name
in he ield, specimens we e collec ed and hei axonomic iden i ica ion was conduc ed
using published olume o he lo a o E hiopia and E i ea (Hedbe g and Sue, 1989).
La ge ees g owing ou side he plo s we e included in he su ey i hei c owns
Ma e ial and Me hods
31
o e hung he plo s because ee c own p ojec ion a eas can a ec ungal occu ence
(Collins e al., 2018). Fu he mo e, la ge ees c ea e hei own mic ohabi a and
de elop a la ge oo sys em, p o iding mo e space o ungal associa ions (Schön e al.,
2018). Vascula plan species ichness and di e si y pa ame e s we e de e mined
(Table 3 in s udy III). Plan pa ame e s and hei co ela ions we e also used o u he
in e p e a ion o ungal pa e n om each s udy a eas. The myco hizal s a us o he
ascula ee species ound in each o he s udied plo s we e checked using eely
accessible da abases (Soudzilo skaia e al., 2020).
Since ain all and empe a u e a ec ungal communi y composi ion and di e si y
(Bah am e al., 2012; Djelloul and Sam aoui, 2011), ain all and empe a u e da a o he
nea by me eo ological s a ions we e p ocu ed om he E hiopian Na ional
Me eo ological Agency (NMA), Bahi Da me eo ological se ice cen e . This was done
o ela e clima ic a iables wi h soil ungal species composi ion and di e si y.
3.5. Labo a o y analysis and axa iden i ica ion
3.5.1 Spo oca p axa iden i ica ion and classi ica ion (S udy III)
In he labo a o y, he mo phological ea u es o he ui bodies we e examined
using app op ia e monog aphs, including An onin (2007), Hama e al. (2010),
Heinemann (1956), Hjo s am and Ry a den (1996), Mo is (1990), Pegle (1968, 1969,
1977), Rammeloo and Walleyn (1993), and Singe (1965), o de e mine he genus and
species o he mac o ungal specimens. Up- o-da e ungal axa names and au ho s’
names we e ob ained om he Mycobank da abase (h p://mycobank.o g). Ecological
unc ions a he genus le el we e iden i ied using a FUNGuild (www. unguild.o g) sea ch
and p o ided (Table 2, s udy III). In addi ion, he edibili y o he ui ing bodies collec ed
om he s udy si es was assessed ollowing he c i e ia used by Bone e al. (2004).
Taxa desc ibed in he li e a u e as bo h non-edible and edible in he li e a u e we e
classi ied as non-edible. Taxa desc ibed in he li e a u e as ha ing doub ul edibili y
we e classi ied as non-edible. Only species classi ied as edible by a la ge majo i y o
he li e a u e consul ed we e classi ied as edible ungi (E).
Ma e ial and Me hods
32
3.5.2. Molecula analysis (S udies I, II & IV)
DNA was ex ac ed om 0.25 g o soil pe sample using a Powe Soil™ DNA
Isola ion Ki (MoBio Labo a o ies Inc., Ca lsbad, CA, USA). PCR eac ions we e
pe o med in iplica e o each sample o minimize PCR biases. PCR eac ions we e
pe o med in 20 μl eac ion olumes con aining 11.22 μl o MQ wa e , 1.60 μl o DNA
empla e, 2.00 μl o 10× bu e , 1.40 μl o MgCl2 (50 mM), 1.60 μl dNTPs (10 mM), 0.50
μl BSA (2%), 0.80 μl o e e se and o wa d p ime s (10 μM) and 0.08 μl Pla inum Taq
polyme ase (In i ogen, Ca lsbad, CA, USA). We used he ollowing PCR condi ions: an
ini ial dena u a ion s ep a 94°C o 3 min; hen 35 cycles o 94°C o 45 s, 50°C o 1
min and 72ºC o 1.5 min; and a inal cycle o 72°C o 10 min. The ITS2 DNA egion
was ampli ied using he o wa d p ime ITS7 (Ih ma k e al., 2012) and he ba coded
e e se p ime ITS4 (Whi e e al., 1990). The ITS4 p ime was labelled wi h sample-
speci ic Mul iplex Iden i ica ion DNA- ags. A nega i e con ol consis ing o MQ wa e
ins ead o DNA was included in each PCR un. The absence o bands on gels indica ed
ha nega i e con ols we e amplicon ee. Ion To en sequencing was ca ied ou a he
Na u alis Biodi e si y Cen e . The sequencing Ion 318TMChip was used o allow o he
highes possible sequencing co e age.
3.6. Da a analysis
3.6.1 Bioin o ma ics analysis (S udies I, II & IV)
Raw sequence eads comp ising demul iplexed sample eads we e ob ained
om he Ion To en ou pu . P ime s and poo -quali y ends we e emo ed based on a
0.02 e o p obabili y limi in Geneious P o 8.1.8 (BioMa e s, New Zealand). Nex , all
sequences we e unca ed o 200 bp and hen il e ed wi h USEARCH .8.0 (Edga ,
2010) o disca d sequences wi h an expec ed e o o >1. The emaining sequences
we e collapsed in o unique sequence ypes on a pe -sample basis using USEARCH
.8.0 (Edga , 2010) while p ese ing ead coun s. Fi s , we disca ded single on
sequence ypes be o e g ouping he emaining high-quali y sequences in o ope a ional
axonomic uni s (OTUs) wi h USEARCH a a 97% sequence simila i y le el while
simul aneously excluding OTUs wi h <70% simila i y o <150 bp pai wise alignmen
Ma e ial and Me hods
33
leng h o a ungal sequence. Sequences we e assigned o axonomic g oups based on
pai wise simila i y sea ches agains he cu a ed UNITE+INSD ungal ITS sequence
da abase, which con ains iden i ied ungal sequences wi h assignmen s o species
hypo hesis g oups (Kõljalg e al., 2013). Up- o-da e ungal axa names and au ho s’
names we e ob ained om Mycobank da abase (h p://www. mycobank.o g). The
FUNGuild da abase (h p://www. unguild.o g) was ini ially used o pe o m unc ional
classi ica ion o OTUs a he genus le el and i was manually checked a e wa ds. OTUs
wi h >90% simila i ies o a ungal SH wi h known ecological unc ion we e assigned o
unc ional g oups. Fo gene a ha a e known o comp ise species om mul iple
unc ional guilds, hei ecological unc ion was assigned indi idually based on a ailable
ecological in o ma ion o he ma ching SH in he UNITE da abase.
3.6.2. S a is ical analysis (S udies I-IV)
All explana o y en i onmen al a iables we e subjec ed o app op ia e da a
ans o ma ion when needed o achie e he pa ame ic c i e ia o no mali y and
homoscedas ici y. Shannon’s H’ di e si y indices, H = –Σpi(lnpi) (Shannon and Wea e ,
1949), we e es ima ed, whe e p indica es he ela i e abundance o ungal OTUs
(Ken and Coke , 1993). The Simpson’s di e si y indices, D = 1 – Σ (pi2), whe e pi is
he impo ance p obabili y in elemen i; and he E enness, J = H′/H′max, whe e H′ is
he numbe de i ed om he Shannon di e si y index and he H′ max is he
maximum possible alue o H′ we e also calcula ed (Magu an, 1988). In addi ion, he
ichness alues o all ungal OTUs (S) based on ea men ype we e es ima ed. All
di e si y measu es we e calcula ed using he Biodi e si yR package (Kind and Coe,
2005) in R (R Co e Team, 2020). Fo s udies which ANOVA assump ions we e me ,
di e si y indices and ichness we e compa ed ac oss ea men s using one-way ANOVA
using R (R Co e Team, 2020) and Tukey HSD was used o de e mine significan
di e ences be ween means (P ≤ 0.05) among ea men s. Linea Mixed E ec s models
(LME, Pinhei o e al., 2016) was used o p e en he alse posi i e associa ions due
ela edness s uc u e in he sampling (s udy III). The mos signi ican a iables used o
in e p e a ion o ungal di e si y and communi y composi ion we e selec ed using he
o wa d.sel unc ion o adeg aphics package (Sibe chico e al., 2017) in R. Sepa a e
Ma e ial and Me hods
34
analysis was conduc ed on unc ional g oups o ungi o de e mine whe he hei
abundance and di e si y we e a ec ed by explana o y en i onmen al a iables.
O dina ion echniques based on Hellinge - ans o med ungal abundance da a
we e used o disce n changes in ungal communi y composi ion among ea men and o
iden i y signi ican explana o y a iables ela ed o axa composi ion. The abundance
da a ma ices agains edaphic a iables we e subjec ed o a canonical co espondence
analysis (CCA) using PC-ORD . 6.0 so wa e (McCune and Me o d., 2011) (s udy II).
Non-pa ame ic da a analysis me hods we e used when ans o ma ions did no p o ide
he app op ia e esul s o a clea in e p e a ion (Ág eda e al., 2014). Non-me ic
mul idimensional scaling (NMDS) was conduc ed using me aMDS unc ion o he egan
package in R on Hellinge - ans o med abundance o ungal da a ma ices agains
explana o y a iables (S udy III and IV). Co ela ion o o dina ions axes sco es wi h
edaphic, ege a ion and clima ic a iables we e assessed using linea eg ession. A
mul iple- esponse pe mu a ion p ocedu e (MRPP) and a pe mu a ion-based
nonpa ame ic MANOVA (Pe MANOVA) (Ande son, 2001) we e un using B ay–Cu is
dis ance and adonis unc ion o he egan package (Oksanen e al., 2019) in R (R Co e
Team, 2020) o analyze di e ences in ungal communi ies ac oss o es s o among
ea men s. An analysis o simila i y pe cen ages (SIMPER; Cla ke, 1993) was also
pe o med using he simpe unc ion o he egan package (Oksanen e al., 2019) in R
(R Co e Team, 2020) o iden i y ungal species ha we e mos esponsible o he
obse ed pa e ns and de e mine he pe cen age con ibu ion o ungal axa o
signi ican dissimila i ies be ween he h ee o es s (Pa a icini e al., 2010). Indica o
species analysis was de e mined using he mul ipa unc ion o he indicspecies
package (Cace es and Legend e, 2009) in R.
Fungal species accumula ion cu es and he Rényi di e si y p o ile we e also
gene a ed using a sample-based es ima o o Es ima eS Ve sion 9 (Colwell, 2013) o
compa e ungal ichness and di e si y among di e en ea men s. A Rényi di e si y
p o ile (Tó hmé ész, 1995) was also used o depic he di e si y cu es among
ea men . Unless s a ed, all da a analysis was conduc ed using R So wa e e sion
4.0.3 (R Co e Team, 2020).
Resul s
Discussion
43
5. Discussion
5.1. Soil Fungal Taxa Composi ion (S udies-I,-II, and-IV)
F agmen a ion poses majo h ea s o D y A omon ane o es ecosys ems o
E hiopia. Howe e , hese o es s a e conside ed o be majo ese oi s o biodi e si y
(Ae s e al., 2016; Aynekulu e al., 2016; Da byshi e e al., 2003; Nyssen e al., 2014).
Simila ly, we ound a huge soil ungal di e si y in hese o es sys ems wi h clea
di e ences in communi y composi ion among he h ee s udy a eas loca ed in No he n
E hiopia (S udy IV). The di e se ungal species in such o es sys ems could be mainly
explained by highe ee species di e si y (Chen e al., 2017) and due o he imp o ed
soil e ili y om added nu ien s in he decomposi ion p ocess o wood ma e ials ha
p o ide he equi ed nu ien s o di e se g oups o ungal species (Siciliano e al.,
2014).
In all s udies, he ungal axa we e domina ed by Ascomyco a, which is cong uen
wi h o he s udies in di e en o es ecosys ems (Geml e al., 2014; Reazin e al., 2016;
Smi h e al., 2017; Tede soo e al., 2014). The dominancy o Ascomyco a could be due
o hei highe genomic po en ial o esou ce u iliza ion, compe i ion, and s ess
ole ance (Egidi e al., 2019). In all ou s udies i was obse ed ha signi ican numbe s
o ungal axa we e no iden i ied down o genus and species le el indica ing lack o
da a om unde s udied opical and sub opical o es ecosys ems (Tede soo e al.,
2014) such as he o es sys ems in E hiopia. The la ges p opo ions o iden i ied ungal
species in ou s udies we e sap ophy ic which play a ole in decomposi ion o o ganic
ma e , as a sou ce o human ood (Ki k e al., 2008) and as biocon ol agen in
ag icul u e (Rossman e al., 1999; Samuels, 1996).
Ou s udy on soil ungal communi y unde di e en age g oups o P. pa ula
plan a ion showed ha he unc ional g oups o ungi om he whole s udy plo s we e
sap o ophs (41%) ollowed by plan pa hogenic (7%) and ECM (2%) ungi. The low
p opo ion o ECM ungi de ec ed unde P.pa ula plan a ions migh be due o he
Discussion
44
con e sion o he na i e ege a ion o he a ea o c op cul i a ion many yea s ago
(Teshome, 2011).
S udies indica ed ha he p opo ion o myco hizal ungi in opical egions is low
and he majo i y o plan species in he egion do no o m myco hizal associa ion wi h
ungi (B und e , 2009). Absence o ECM ungi in he d y A omon ane o es s o
E hiopia was also epo ed p e iously (Dejene e al., 2017a). In con as , we
encoun e ed highe ela i e p opo ion o ECM ungi in such o es sys ems (Fig 2B in
s udy-I; Fig 1B in s udy-IV). This associa ion may be due o he di e se ege a ion (F iis
e al., 2010) and he p esence o mo e ees ha hos myco hizal ungi, o may be due
o he dispe sion o myco hizal inocula om nea by plan a ion o es s domina ed by
Eucalyp us and Pinus species (Cas año e al., 2019; Dejene e al., 2017a, 2017b;
U celay e al., 2017). High numbe o ECM species in such o es sys ems could also be
jus i ied by he olde and dense o es s ha main ain empe a u e and adequa e
mois u e (Fe nández-Toi án e al., 2006; Pinna e al., 2010; Toi anen e al., 2012). The
oo sys ems o he old ees also acili a e he occu ence o ECM ungi (Mölde e al.,
2014).
In s udy-II, some ungal species unde he gene a Tomen ella, Rama ia and
Inocybe we e ound associa ed wi h P. pa ula ees a all age s ages o ee
de elopmen . Tomen ella and Inocybe a e cosmopoli an species ha inhabi Eucalyp us
plan a ions in E hiopia (Cas año e al., 2019). Species o Rhizopogon we e also
associa ed mo e wi h younge s ands (5- and 11-yea -old s ands) in his s udy, which
suppo s p e ious indings, ha hey a e ea ly colonize ungal species (Tede soo e al.,
2016b). The Rhizopogon species a e known as spo e bank species ha acili a e he
es ablishmen o ees in o me ly non- o es habi a s. Amani a, which was also ound in
ou s udy si e o P. pa ula plan a ion a e well-known o hei associa ion wi h coni e
o es s as he gene a is cha ac e is ic o la e-s age pine s ands ha a e 30–40 yea s old
(Chu-Chou and G ace, 1982; Visse , 1995).
P e ious s udies indica ed ha he composi ion o ECM ungi in he soil is
co ela ed wi h soil e ili y and he g ow h s a us o he hos ees (Cozzolino e al.,
Discussion
45
2016; Wang and Wang, 2008). Simila ly, we ound ha he 36-yea -old s and and he 5-
yea old s and o P. pa ula had dis inc i e soil ungal communi ies. The dis inc
composi ion o ECM ungi in young and old s ands unde P. pa ula plan a ions (s udy II)
migh be ela ed o si e quali y ac o s, such as soil e ili y and s and age ac o s. Gi en
ha he amoun o OM, a ailable P and he C/N a io o 5- and 11-yea -old s ands we e
no signi ican ly di e en , his may ha e enabled 11-yea -old s ands o de elop an
associa ion wi h only a limi ed numbe o ECM ungi, bu a highe ela i e abundance o
hese ECM ungi, which could indica e inc eased dependence o P. pa ula ees on a
limi ed numbe o dominan symbion s species.
We obse ed di e ences in ungal communi y composi ion and di e si y due o
o es i e. This could be due o a change in ege a ion (Ha e al., 2005) and loss o
hos plan s a e i e (Pa inson e al., 2006; Smi h e al., 2005). Mo e ungal species
we e de ec ed in he bu ned o es a eas whe e he soil e ili y was ela i ely low han in
unbu ned a eas, which could be ela ed o deposi ions o ash a e he i e (Hul e al.,
2015). Ash deposi ions could c ea e emp y niches o apid coloniza ion o he a ea by
ea ly s ages colonize ungi (F i ze e al., 1993). Aga icus campes oides was highly
abundan in one-yea -old bu ned s ands bu much less abundan in en-yea -old bu ned
and unbu ned s ands. The species migh be pa ially esponsible o he di e ences
be ween s ands, sugges ing ha ime a e i e is also p obably esponsible o he
a ia ion in he dominance o some species and hei exclusi e occu ence in ce ain
s ands. This is suppo ed by p e ious indings ha , o a gi en s and, ce ain ungal
species end o be abundan and cha ac e ize i s composi ion (Zhu e al., 2010).
Dis inc ungal communi y composi ion pa e n was also obse ed in ou soil
ungal s udy in he s udied D y A omon ane o es sys ems in No h E hiopia (s udy-IV).
Such di e ences indica e he si e speci ic na u e o ungal assembly such as ecological
g adien s (Egidi e al., 2019) and ege a ion (Egidi e al., 2019; Tede soo e al.,
2016).Vege a ion is known o a ec ungi composi ion along wi h he p ocesses ha
in luence he na u e and quan i y o esou ces en e ing in o he soil (Wa dle e al., 2004)
which u he implies ha ungal communi y is s uc u ed h ough he en i onmen al
Discussion
46
ac o s (Hanson e al., 2012; Haza d e al., 2013) ha egula e he assemblage o
ege a ion.
S udies demons a ed ha ungal communi y composi ion can be go e ned by
a ious en i onmen al a iables and landscape he e ogenei y (Bah am e al., 2015;
Fe a i e al., 2016; Peay e al., 2010; L. Tede soo e al., 2014). Thus, e alua ing he
ungal communi ies in di e en ecosys ems is essen ial o il e ou he ela i e
con ibu ions o en i onmen al ac o s o ungal di e si y and composi ion in an
ecosys em (Tian e al., 2018).
Soil cha ac e is ics s ongly a ec ungal communi y s uc u es (S aa sma e al.,
2001; Zaka ia and Boddy, 2002; Laube e al., 2008; Reazin e al., 2016; Yang e al.,
2017), communi y composi ion (Cas año e al., 2019; Delelegn e al., 2018; Laube e
al., 2008) and dis ibu ion (Cla idge e al., 1993). Speci ic ungal species a e likely o
espond o en i onmen al a iables, mainly edaphic pa ame e s, in di e en ways
(Cozzolino e al., 2016; Koide e al., 2014), and, hus, in u n, he composi ion o he
ungal communi y is di ec ly co ela ed wi h edaphic a iables (Cozzolino e al., 2016).
Ni ogen and Phospho ous signi ican ly a ec ed he communi y composi ion o
en i e soil ungal in ou i e expe imen in D y A omon ane o es sys ems (s udy I).
P e ious epo s also indica ed ha high a ailabili y o N and P could nega i ely a ec
he s uc u e o ungi in he soil, pa icula ly o he myco hizal ungi (Zhao e al., 2018)
by dec easing plan dependency on ungi and educing ca bon alloca ion o ungi (Liu e
al., 2019) which e en ually could cause compe i ion among he ungal species and lead
o he o ma ion o dis inc ungal composi ion (Wang and Wang, 2008; Zhao e al.,
2018). A ailable P also in luenced he composi ion o soil ECM ungi in P. pa ula
plan a ion (Table 4 in s udy-II), which was simila o he indings epo ed by Rosens ock
e al. (2016). Howe e , we no ed posi i e co ela ion be ween N and en i e soil ungal
communi y composi ion in D y A omon ane o es s in E hiopia (s udy-IV). This mos
p obably indica es ha he majo i y o plan species in he s udied o es a e
independen o myco hizal ungi.
Discussion
47
Soil pH is epo ed as impo an ac o s go e ning he ungal composi ion (Ullah
e al., 2019). Ou s udy on soil ungi in he D y A omon ane o es s in No h E hiopia
(s udy-IV) indica ed ha ungal composi ion is main ained a a lowe pH le el. Howe e ,
some ungal axa a e di ec ed owa ds he highe pH le el which could be due o he
abili y and adap abili y o hese axa o g ow in a compa a i ely alkaline soil condi ion
(Ne a ez e al., 2009; Tian e al., 2018).
Ca ions play an impo an ole in many physicochemical p ocesses, such as
pho osyn hesis (He e al., 2017) and, hence, he amoun o ca bon ha is a ailable o
soil ungi (Shi e al., 2014) in o es s soils. Ou s udy showed signi ican e ec o Ca,
Mg, and K on soil ungal communi y composi ion in he D y A omon ane o es s (s udy-
IV).
The clima ic and ege a ion cha ac e is ics a e epo ed o in luence he spa ial
a ia ion and hus, he composi ion o ungal communi ies (Newsham e al., 2016). In
ou soil ungal s udy in he D y A omon ane o es sys ems in No h E hiopia (s udy IV),
we obse ed a s ong associa ion o soil ungi wi h daily empe a u e and annual ain all.
In line wi h ou esul s, o he s udies indica ed ha empe a u e shapes he composi ion
o soil ungal communi ies in o es ecosys ems (Newsham e al., 2016) since ai
empe a u e oge he wi h he mois u e in he soil inc eases he me abolic ac i i y o
ungi, ex ends he pe iod o which ungi a e ac i e each yea , and enables a swi ch
om su i al o g ow h s a egies. Thus, he dis inc soil ungal communi ies ound in
each o he chu ch o es s (S udy-IV) may ollow he a ia ion o he ain all o he h ee
a eas, he plan communi y in each o he o es s, o bo h (Hawkes e al., 2011).
5.2. Mac o ungal Taxa composi ion (S udy-III)
Despi e habi a agmen a ion is epo ed as nega i ely a ec ing he ungi
communi y in o es sys ems (Saps o d e al., 2017), we ound a high numbe o
mac o ungal species in agmen ed chu ch o es s in D y A omon ane egion o
E hiopia. The di e se ungal species in such o es sys ems could be mainly explained
by highe ee species di e si y (Chen e al., 2017) and due o he imp o ed soil e ili y
Discussion
48
om added nu ien s in he decomposi ion p ocess o wood ma e ials ha p o ide he
equi ed nu ien s o di e se g oups o ungal species (Siciliano e al., 2014).
Signi ican numbe s o ungal axa we e no iden i ied down o genus and species
le el indica ing lack o da a om unde s udied opical and sub opical o es
ecosys ems (Tede soo e al., 2014) such as he o es sys ems in E hiopia. The la ges
p opo ions o iden i ied mac o ungal species in ou s udy we e sap ophy ic. Such
unc ional g oups a e impo an o decomposi ion o o ganic ma e and a e aluable
ood sou ces o humans (Ki k e al., 2008). Some o he species a e also impo an in
ag icul u e as biological con ol agen s (Rossman e al., 1999; Samuels, 1996).
The spo oca p p oduc ions ob ained in his s udy we e no high. Al hough u he
esea ch is needed, his could pa ially be explained by he single one species. Some
o he species we e collec ed in a single ime du ing he collec ion pe iod. Mo eo e ,
majo i y o he species we e sap ophy ic ungi which a e cha ac e ized by low biomass
p oduc ions (Gassibe e al., 2011; Media illa e al., 2014). Howe e , aluable edible
mac o ungal species belonging o he Cal a ia, Lae ipo us, Pleu o us, Te mi omyces
sp., and Mac olepio a gene a we e also collec ed in his s udy. Among hese edible
species, Te mi omyces sp. is highly ega ded by local people in sou hwes E hiopia
because o i s good as e and a oma (Aba e, 2014). This also p o ides a s a ing poin
in e ms o b oadening he managemen and conse a ion o agmen ed o es s o he
p oduc ion o non- imbe o es s p oduc s in E hiopia.
Al hough, p e ious s udies indica ed he low p opo ion o ECM species in he
opics (Dejene e al., 2017a; Tede soo e al., 2014), we ound mo e ECM axa (14% o
he o al). This could be a ibu ed o highe ascula plan di e si y (F iis e al., 2010),
a ailabili y o mo e ees ha hos myco hizal ungi (Hailema iam e al., 2013; Wube e
al., 2003) o he dispe sion o myco hizal inocula om he nea by plan a ion o es s.
This inding indica es he impo an implica ion o he indigenous o es sys em o he
main enance o unc ional ungal di e si y in E hiopia (Dejene e al., 2017a).
Discussion
49
Soil pH is known o be he mos c i ical edaphic a iable a ec ing he
composi ion and s uc u e o ungal communi ies (Doche y e al., 2015; Fie e and
Jackson, 2006b; Zhang e al., 2016). Simila ly, in his s udy, soil pH co ela ed wi h
ungal species composi ion and he p esence o g ea e numbe s o mac o ungal
species was associa ed wi h lowe pH alues. This was in line wi h he indings o
Puangsomba e al. (2010) and Zhang e al. (2016) who epo ed nega i e in luence o
highe pH le els on ungal communi y s uc u e, p obably because a highe pH es ains
he expansion o ungi and he p oduc ion o spo oca ps.
O ganic ma e in luences mycelial ou g ow h and ne wo k o ma ion (Zaka ia
and Boddy, 2002) and ungal communi y h ough i s impac on he wa e -holding
capaci y and soil and nu ien a ailabili y (Ha ing on, 2003). Thus, a high le el o
o ganic ma e accumula ion implies a high le el o mac o ungal assembly, pa icula ly
o sap ophy ic species. Simila ly, we ound OM associa ed wi h he composi ion o
mac o ungi in he s udied agmen ed chu ch o es s o D y A omon ane o es s
sys ems (Figu e 6 in s udy III).
We also ound ha CEC associa ed wi h mac o ungal composi ion. C ab ee e
al. (2010) obse ed ha ungal species ichness was low, pa icula ly when he CEC
was high. This is p obably because he CEC in luence nu ien a ailabili y, soil pH, and
soil eac ions o o he amelio an s in he soil (Ogeleka e al., 2017). CEC is i al in many
physicochemical p ocesses, such as pho osyn hesis (He e al., 2017) and he eby
in luence he amoun o ca bon a ailable o ungi in he soil (Shi e al., 2014).
Maximum and minimum empe a u es also a ec ed mac o ungal composi ion.
This may be due o he ac ha he mycelium o he ungal species is mo e eadily
a ec ed by a mosphe ic changes (Sale ni e al., 2002), being mo e supe icial
speci ically o hose sap o ophs species ha cons i u e he majo i y o mac o ungal
axa in ou s udied o es s. Tempe a u e can also play impo an ole in nu ien cycling
p ocess (Geng e al., 2017) which in u n esul s in he o ma ion o dis inc ungal
communi ies, pa icula ly o he ungi ha a e soil dependen as a subs a e (Nicolás e
al., 2019).
Discussion
50
5.3. E ec o i e (s udy-I), s and age (s udy-II), and abo eg ound plan
di e si y (s udy-III and s udy-IV) on ungal ichness, di e si y and
p oduc ion
Ou s udy on he e ec o i e on soil ungal communi y (s udy-I) e ealed ha
highe o al ichness alues we e ound in o es s ands ecen ly a ec ed by i e han
unbu ned s ands. This could be a ibu ed o he new ecological condi ions c ea ed by
di e ences in i e se e i y, which may inci e o suppo spo e ge mina ion o se e al
ungal species in he soil (Heino, 2012) ollowing he i e in he in es iga ed o es s. In
addi ion, he mycelium o ungal species in he hizosphe e may pe sis (Cowan e al.,
2016; Shen e al., 2016) o he ungal communi y may be esilien o he e ec s o i e o
some ex en (Cowan e al., 2016; Jennings e al., 2012).
The s udy also e ealed absence o signi ican di e ence in ungal di e si y
be ween i e a ec ed a eas. This could be due o he less uel consumed and hea
p oduced du ing i e (Reazin e al., 2016; Semeno a-Nelsen e al., 2019). Ra he he
change migh ha e been d i en by indi ec e ec o i e in soil p ope ies o by he
change in he plan communi ies (Oli e e al., 2015; Ponde e al., 2009; T appe e al.,
2009). Also, ungi in a ecu en o es ecosys em may be adap ed o equen i es
(Semeno a-Nelsen e al., 2019) (Dean e al., 2015; Ha e al., 2005) (Semeno a-
Nelsen e al., 2019). Fu he mo e, he in ensi y o he i e migh no ha e been high
enough o a ec he below-g ound ungal communi ies (Bá cenas-Mo eno e al., 2009;
Egidi e al., 2016). Thus, he esponses o soil ungi o ecu ing low-in ensi y i e also
appea o be minimal (Johnson e al., 2013; Oli e e al., 2015) and epheme al (Ha e
al., 2005).
Time since he i e occu ence did no a ec ungal guild di e si y. In ag eemen
wi h ou inding, Egidi e al. (2016) no ed absence o a signi ican change in ungal
di e si y ollowing i e. This migh be due o low uel loads ha esul ed in li le hea
ans e ed o he soil (Lun and Mo gan, 2002)..
Discussion
51
Ou s udy also e ealed ha bo h he ichness and di e si y o ECM ungi we e
highe in in he ecen ly bu ned s ands, which could indica ed an immedia e pos - i e
myco hizal coloniza ion in i e-a ec ed o es s ands (Dahlbe g, 2002; Rincón e al.,
2015). The ECM axa may also ha e es ablished dominance immedia ely a e bu ning
owing o hei ole ance o i e e ec s (Dahlbe g, 2002; Kip e e al., 2010) o hey may
ha e su i ed in a mycelial s a e du ing he i e e en (Hewi e al., 2013). In con as , ,
o he s udies epo ed ha olde s ands suppo g ea e di e si y o ECM ungi
(Fe nández-Toi án e al., 2006; Pinna e al., 2010; Toi anen e al., 2012) and gene ally
ha e highe abundance o ECM (Mölde e al., 2014).
The ela i ely highe di e si y indices o ECM ungi in he 5-yea -old s and han in
he 11-yea -old s and unde P. pa ula may possibly be a ibu ed o he less de eloped
ee canopy a he ea lie s age o s and de elopmen , which may ha e allowed di e se
ECM ungi o in e ac ex ensi ely wi h he oo sys ems o unde s o y plan s (Dang e
al., 2017) and/o he p e ious land use o he plan a ion a ea (ag icul u al c op
p oduc ion). Deacon and Fleming, (1992) demons a ed ha when a o es a ion akes
place on land ini ially used o o he pu poses, he ECM ungal spo es a e he
undamen al inoculum du ing he ea ly s age o ECM succession. The spo e banks
migh ha e also de i ed om o he nea by myco hizal-associa ed plan a ions such as
Eucalyp us plan a ions (Cas año e al., 2019; Dejene e al., 2017d).
The highe di e si y indices o ECM species de ec ed in he 36-yea -old s and
han in he 11-yea -old s and may be due o he hinning ca ied ou in his s and unlike
he o he wo age g oups o P. pa ula (Dejene e al., 2017b). Chen e al. (2015) because
hinning could inc ease he ela i e abundance o myco hizal ungi as i opens up he
o es canopy, which in u n, inc eases soil empe a u e and mois u e (Wang e al.,
2019). Thinning may he e o e ha e a posi i e e ec on mic obial ac i i y (Pang e al.,
2013) because soil empe a u e and mois u e in luence he eac ion o mic obial
enzymes and, hus, shi he mic obial communi y composi ion by al e ing subs a es
and ex acellula enzyme ac i i y (Hasse and Zak, 2005). Do e and Kee on (2015) and
Tomao e al. (2020) sugges ed ha ungal di e si y can be conse ed o e en inc eased
using o es managemen p ac ices ha enhance he s uc u al complexi y o s ands and
Conclusions
58
o aluable wild mush ooms should be inco po a ed in o managemen and
conse a ion s a egies in hese agmen ed o es sys ems.
4. Ou soil ungal and mac o ungal s udies in agmen ed chu ch o es s o he d y
A omon ane o es sys ems indica ed ha he p omo ion o ascula ee
di e si y in hese o es sys ems h ough en ichmen plan ings o assis ed na u al
egene a ion managemen sys ems would o e sui able habi a s wi h a iable
mic oclima es ha should assis ungal species. In addi ion, he e ec s o he
a o emen ioned managemen p ac ices on soil e ili y should be aken in o
conside a ion owing o he impo an ela ionship be ween edaphic a iables and
ungal composi ion in hese o es s.
5. Da a ob ained in all he s udies in his hesis will signi ican ly con ibu e o he
body o knowledge ega ding soil ungal communi ies in E hiopia and p o ided
ele an in o ma ion equi ed o he managemen and conse a ion o hese
o es sys ems and he cen al oles played by ungi in he managemen and
conse a ion o such o es s sys ems including p o ision o ood esou ces o
poo popula ions du ing imes o ood sca ci y.
6. In all ou s udies i was obse ed ha signi ican numbe o ungal axa was no
iden i ied down o genus and species le el. This indica es ha he ungal di e si y
in E hiopian o es sys ems is as ye la gely undesc ibed and likely includes many
axa unknown o science. Thus, we ad ise ha addi ional long e m scien i ic
in es iga ions a e needed o consolida e he E hiopian ungal biodi e si y
da abase.
Conclusions
59
7. Conclusiones
1. El es udio e eló que los bosques eclesiás icos agmen ados de los sis emas
o es ales secos a omon anos en E iopía albe gan muchos hongos
di e si icados impo an es pa a el manejo sos enible de es os sis emas
o es ales. Po lo an o, el esul ado p esen a una isión de la conse ación y el
manejo de g emios uncionales aliosos en los suelos de los sis emas o es ales
agmen ados de la iglesia D y A omon ane de E iopía. La di e sidad de plan as
ascula es se encon ó como un ac o pa a la di e sidad úngica del suelo. Se
encon a on hongos ECM impo an es en es os sis emas o es ales. Sis emas
o es ales e íopes que pod ían espalda la impo ancia de la conse ación de
los hongos en los sis emas o es ales a omon anos secos de E iopía. Es
ine i able que los bosques eclesiás icos agmen ados de los sis emas o es ales
secos a omon anos necesi en una conexión, ya sea median e el es ablecimien o
de un nue o bosque de p o ección adyacen e a los bosques emanen es o el
es ablecimien o de plan aciones o es ales asociadas con mico izas. Es o
ambién p opo ciona ía di e sos nichos pa a el c ecimien o y desa ollo de
di e en es especies de hongos y pe mi i ía un ácil mo imien o de espo as en e
los ipos de bosques.
2. Nues os es udios des aca on que la composición de los hongos di e ía en una
c onosecuencia después de un incendio en los bosques secos agmen ados de
A omon ano, a iaba con la edad del odal en las plan aciones de P. pa ula,
di e ía debido a la composición de especies de á boles de los bosques secos de
A omon ano en E iopía y su composición se explica po ac o es ascula es.
di e sidad a bó ea, a iables edá icas, espaciales y climá icas. Po lo an o, el
e ec o de las p ác icas de manejo o es al como el acla eo y la cosecha debe
ene se en cuen a debido a la impo an e elación en e es os pa áme os
ecológicos y la composición úngica del suelo en los sis emas o es ales de
E iopía.
3. Nues o es udio de mac o ungos e eló la p esencia de aliosas especies de
mac o ungos comes ibles pe enecien es a los géne os T icholoma, Suillus y
Conclusions
60
Te mi omyces, que po encialmen e pod ían come cializa se y, po lo an o,
pod ían p opo ciona ing esos suplemen a ios a la población local y los
adminis ado es o es ales que dependen de los bosques. Po lo an o, la
p oducción de aliosos hongos sil es es debe inco po a se a las es a egias de
manejo y conse ación en es os sis emas o es ales agmen ados.
4. Nues os es udios sob e hongos y mac o úngicos del suelo en bosques
eclesiás icos agmen ados de los sis emas o es ales secos a omon anos
indica on que la p omoción de la di e sidad de á boles ascula es en es os
sis emas o es ales median e plan aciones de en iquecimien o o sis emas de
ges ión de egene ación na u al asis ida o ece ía hábi a s adecuados con
mic oclimas a iables que debe ían ayuda especies. Además, deben ene se en
cuen a los e ec os de las p ác icas de manejo an es mencionadas sob e la
e ilidad del suelo debido a la impo an e elación en e las a iables edá icas y
la composición úngica en es os bosques.
5. Los da os ob enidos en odos los es udios de es a esis con ibui án
signi ica i amen e al cue po de conocimien o sob e las comunidades de hongos
en el suelo en E iopía y p opo ciona on in o mación ele an e eque ida pa a el
manejo y conse ación de es os sis emas o es ales y los oles cen ales que
juegan los hongos en el manejo y conse ación de dichos sis emas o es ales,
incluida la p o isión de ecu sos alimen a ios pa a las poblaciones pob es en
épocas de escasez de alimen os.
6. En odos nues os es udios se obse ó que no se iden i icó un núme o
signi ica i o de axones de hongos has a el ni el de géne o y especie. Es o
indica que la di e sidad de hongos en los sis emas o es ales de E iopía aún no
se ha desc i o en g an medida y p obablemen e incluye muchos axones
desconocidos pa a la ciencia. Po lo an o, ad e imos que se necesi an
in es igaciones cien í icas adicionales a la go plazo pa a consolida la base de
da os de biodi e sidad úngica de E iopía.
Re e ences
61
8. Re e ences
Aba e, D., 2014. Wild Mush ooms and Mush oom Cul i a ion E o s in E hiopia. WSMBMP Bull. 11, 1–3.
Aba e, D., 2008. Wild mush ooms in E hiopia and ou ea ing habi , in: Na ional Mush oom Con e ence.
Facul y o Science, May 14-15, 2008, Addis Ababa.
Aba e, D., 1999. Aga icus campes is in upland E hiopia. Mycologis 13, 28.
h ps://doi.o g/10.1016/S0269-915X(99)80075-5
Abdulla, A.M., 2013. Non- imbe Fo es P oduc s and Food Secu i y: The Case o Yabelo Wo eda,
Bo ana Zone, E hiopia. Food Sci. Qual. Manag. 22, 9–23.
Abe e, F., Bele e, Y., Ke alew, A., So omessa, T., 2017b. Ca bon s ock o Banja o es in Banja dis ic ,
Amha a egion, E hiopia: An implica ion o clima e change mi iga ion. J. Sus ain. Fo . 36, 604–
622. h ps://doi.o g/10.1080/10549811.2017.1332646
Adeniyi, M., Odeyemi, Y., ODEYEMI, O., 2018. Ecology, di e si y and seasonal dis ibu ion o wild
mush ooms in a Nige ian opical o es ese e. Biodi e si as J. Biol. Di e s. 19, 285–295.
h ps://doi.o g/10.13057/biodi /d190139
Ae s, R., Van O e eld, K., No embe , E., Wassie, A., Abiyu, A., Demissew, S., Daye, D.D., Giday, K.,
Haile, M., TewoldeBe han, S., Teke ay, D., Teklehaimano , Z., Binggeli, P., Decke s, J., F iis, I.,
G a ze , G., He my, M., Heyn, M., Honnay, O., Pa is, M., S e ck, F.J., Muys, B., Bonge s, F.,
Healey, J.R., 2016. Conse a ion o he E hiopian chu ch o es s: Th ea s, oppo uni ies and
implica ions o hei managemen . Sci. To al En i on. 551–552, 404–414.
h ps://doi.o g/10.1016/j.sci o en .2016.02.034
Ág eda, T., Cisne os, Ó., Águeda, B., Fe nández-Toi án, L.M., 2014. Age class in luence on he yield o
edible ungi in a managed Medi e anean o es . Myco hiza 24, 143–152.
h ps://doi.o g/10.1007/s00572-013-0522-y
Aklilu, B.M., Bekele, L., Me kineh, M.M., Ba ana, 2019. Is he expansion o Eucalyp us ee a cu se o an
oppo uni y? Implica ions om a dispu e on he ees ecological and economic impac in E hiopia:
A e iew. J. Ecol. Na . En i on. 11, 75–83. h ps://doi.o g/10.5897/jene2019.0765
Alem, D., Dejene, T., O ia-de- ueda, J.A., Geml, J., Cas año, C., Smi h, J.E., Ma ín-pin o, P., 2020a. Soil
ungal communi ies and succession ollowing wild i e in E hiopian d y A omon ane o es s , a
highly di e se unde explo ed ecosys em. Fo . Ecol. Manage. 474, 118328.
h ps://doi.o g/10.1016/j. o eco.2020.118328
Alem, D., Dejene, T., O ia-de-Rueda, J.A., Geml, J., Ma ín-Pin o, P., 2020b. Soil Fungal Communi ies
unde Pinus pa ula Schiede ex Schl dl. & Cham. Plan a ion Fo es s o Di e en Ages in
E hiopia. Fo es s 11, 1109. h ps://doi.o g/10.3390/ 11101109
Alem, S., 2015. In e na ional ade o di e en o es p oduc s in E hiopia.. Volume 4, Issue 4. A ican J.
Econ. Sus ain. De . 4, 353–361.
Amma, S., Toju, H., WaCH in a , Ch., SaTo, H., Tanabe, A.S., A chawakom, T., MKanzaki, A., 2018.
Composi ion and Di e si y o Soil Fungi in Dip e oca paceae-Domina ed Seasonal T opical
Fo es s in Thailand. Mic obes En . 33, 135–143. h ps://doi.o g/10.1264/jsme2.ME17168
Ande son, M.J., 2001. A new me hod o non pa ame ic mul i a ia e analysis o a iance. Aus al Ecol.
26, 32–46. h ps://doi.o g/10.1111/j.1442-9993.2001.01070.pp.x
Ango, T.G., Bewke , W., 2007. Challenges and p ospec s o sus ainable o es managemen in Wondo
Gene a ea, Sou he n E hiopia. E hiop. J. De . Res. 29, 27–64.
h ps://doi.o g/10.4314/ejd . 29i2.42709
An onin, V., 2007. Monog aph o Ma asmius, Gloiocephala, Palaeocephala and Se ulipes in T opical
Re e ences
62
A ica. Fungus Fl T op A 1, 177.
As aw, A., E e a, L., 2017. The con ibu ion o Non-Timbe Fo es P oduc s o he Ru al Li elihood : The
case o yayo dis ic , illu ababo a zone , o omia egional s a e , wes e n. In . J. Appl. Ag ic. Res.
12, 157–169.
Asmelash, F., Bekele, T., Belay, Z., 2019. Compa a i e ield su i al and g ow h o selec ed E hiopian
na i e ee species and he e ec o whole soil a buscula myco hizal ungi inocula ion. J. Ho ic.
Fo . 11, 19–31. h ps://doi.o g/10.5897/JHF2018.0573
Asmelash, F., Bekele, T., Bi hane, E., 2016. The Po en ial Role o A buscula Myco hizal Fungi in he
Res o a ion o Deg aded Lands. F on . Mic obiol. 7, 1–15.
h ps://doi.o g/10.3389/ micb.2016.01095
A e ill, C., Tu ne , B.L., Finzi, A.C., 2014. Myco hiza-media ed compe i ion be ween plan s and
decompose s d i es soil ca bon s o age. Na . Cell Biol 505, 543–545.
Aynekulu, E., Ae s, R., Denich, M., Negussie, A., F iis, I., Demissew, S., Boehme , H.J., 2016. Plan
di e si y and egene a ion in a dis u bed isola ed d y A omon ane o es in no he n E hiopia.
Folia Geobo . 51, 115–127. h ps://doi.o g/10.1007/s12224-016-9247-y
Bahnmann, B., Ma, T., Hal o sen, R., Da ey, M.L., Sedlák, P., Tom, M., Bald ian, P., 2018. E ec s o oak
, beech and sp uce on he dis ibu ion and communi y s uc u e o ungi in li e and soils ac oss a
empe a e o es 119, 162–173. h ps://doi.o g/10.1016/j.soilbio.2018.01.021
Bah am, M., Peay, K.G., Tede soo, L., 2015. Local-scale biogeog aphy and spa io empo al a iabili y in
communi ies o myco hizal ungi. New Phy ol. 205, 1454–1463.
h ps://doi.o g/10.1111/nph.13206
Bah am, M., Põlme, S., Kõljalg, U., Za e, S., Tede soo, L., 2012. Regional and local pa e ns o
ec omyco hizal ungal di e si y and communi y s uc u e along an al i udinal g adien in he
Hy canian o es s o no he n I an. New Phy ol. 193, 465–473. h ps://doi.o g/10.1111/j.1469-
8137.2011.03927.x
Bá cenas-Mo eno, G., a ex backslasha a h, E., Båå h, E., 2009. Bac e ial and ungal g ow h in soil
hea ed a di e en empe a u es o simula e a ange o i e in ensi ies. Soil Biol. Biochem. 41,
2517–2526. h ps://doi.o g/10.1016/j.soilbio.2009.09.010
Ba nes, C.J., Van de Gas , C.J., Bu ns, C.A., McNama a, N.P., Bending, G.D., 2016. Tempo ally a iable
geog aphical dis ance e ec s con ibu e o he assembly o oo -associa ed ungal communi ies.
F on . Mic obiol. 7, 1–13. h ps://doi.o g/10.3389/ micb.2016.00195
Beenhouwe , M. De, Geel, M. Van, Ceulemans, T., Mule a, D., Lie ens, B., Honnay, O., 2015. Soil
Biology & Biochemis y Changing soil cha ac e is ics al e he a buscula myco hizal ungi
communi ies o A abica co ee ( Co ea a abica ) in E hiopia ac oss a managemen in ensi y
g adien . Soil Biol. Biochem. 91, 133–139. h ps://doi.o g/10.1016/j.soilbio.2015.08.037
Bekele, M., 2011. o es plan a ion and woodlo s in E hiopia. A ican Fo es Fo um, Ni obi, Kenya.
Bekele, M., Lemenih, M., 2008. Pa icipa o y Fo es Managemen Bes P ac ices , Lesson Lea n and
Pa icipa o y Fo es Managemen Bes P ac ices , Lesson Lea n and.
Bekele, T., Kassa, K., Mengis u, T., Debele, M., Melka, Y., 2013. Wo king wi h communi ies o add ess
de o es a ion in he Wondo Gene ca chmen A ea , E hiopia : lessons lea n om a pa icipa o y
ac ion esea ch. Res. J. Ag ic. En i on. Manag. 2, 448–456.
Belay, T., 2016. Clima e-g ow h ela ionship o Pinus pa ula Schldl. e Cham. in Wondo Gene , Sou h
Cen al E hiopia. J. Clima ol. Wea he Fo ecas . 04, 1–8. h ps://doi.o g/10.4172/2332-
2594.1000181
Belay, Z., Ves be g, M., Asse a, F., 2013. Di e si y and abundance o a buscula myco hizal ungi
associa ed wi h acacia ees om di e en land use sys ems in E hiopia. A ican J. Mic obiol.
Res. 7, 5503–5515. h ps://doi.o g/10.5897/AJMR2013.6115
Re e ences
63
Belaynesh, Z., 2002. Pe cep ions o o es Resou ce changes in and a ound Wondo Gene Ca chmen
and i s nea u u e impac s. MSc Thesis. Wondo Gene College o Fo es y, Wondo Gene ,
E hiopia.
Beluhan, S., Ranogajec, A., 2011. Chemical composi ion and non- ola ile componen s o C oa ian wild
edible mush ooms. Food Chem. 124, 1076–1082.
h ps://doi.o g/10.1016/j. oodchem.2010.07.081
Be g, A., Ga den o s, U., Hallingback, T., No en, M., 2002. Habi a p e e ences o ed-lis ed ungi and
b yophy es in woodland key habi a s in sou he n Sweden – analyses o da a om a na ional
su ey. Biodi e s. Conse . 11, 1479–1503. h ps://doi.o g/10.1023/A
Bhanda i, B., Jha, S.K., 2018. Compa a i e s udy o mac o ungi in di e en pa ches o Boshan
Communi y Fo es in Ka hmandu, Cen al Nepal. Bo . O ien . J. Plan Sci. 11, 43–48.
h ps://doi.o g/10.3126/bo o . 11i0.21032
Bi hane, E., A egawi, K., Giday, K., 2017a. Changes in a buscula myco hiza ungi spo e densi y and
oo coloniza ion o woody plan s in esponse o exclosu e age and slope posi ion in he highlands
o Tig ay , No he n E hiopia. J. A id En i on. 142, 1–10.
h ps://doi.o g/10.1016/j.ja iden .2017.03.002
Bi hane, E., Fa umah, N., Gidey, K., Zenebe, A., Mohammed, S., 2018a. Vege a ion co e densi y and
dis u bance a ec ed a buscula myco hiza ungi spo e densi y and oo coloniza ion in a d y
A omon ane o es , no he n E hiopia. J. Fo . Res. 29, 675–686. h ps://doi.o g/10.1007/s11676-
017-0493-5
Bi hane, E., Geb emedihin, K.M., Tadesse, T., Hailema iam, M., Solomon, N., 2017b. Exclosu es
es o ed he densi y and oo coloniza ion o a buscula myco hizal ungi in Tig ay, No he n
E hiopia. Ecol. P ocess. 6. h ps://doi.o g/10.1186/s13717-017-0101-9
Bi hane, E., Geb emeskel, K., Taddesse, T., Hailema iam, M., Hadgu, K.M., No g o e, L., Negussie, A.,
2018b. In eg a ing Faidhe bia albida ees in o a so ghum ield educes s iga in es a ion and
imp o es myco hiza spo e densi y and coloniza ion. Ag o o . Sys . 92, 643–653.
h ps://doi.o g/10.1007/s10457-016-0027-8
Bi hane, E., Kuype , T.W., S e ck, F.J., Bonge s, F., 2010. A buscula myco hizal associa ions in
Boswellia papy i e a ( ankincense- ee) domina ed d y deciduous woodlands o No he n
E hiopia. Fo . Ecol. Manage. 260, 2160–2169. h ps://doi.o g/10.1016/j. o eco.2010.09.010
Bi hane, E., S e ck, F.J., Fe ene, M., Bonge s, F., Kuype , T.W., 2012. A buscula myco hizal ungi
enhance pho osyn hesis, wa e use e iciency, and g ow h o ankincense seedlings unde
pulsed wa e a ailabili y condi ions. Oecologia 169, 895–904. h ps://doi.o g/10.1007/s00442-012-
2258-3
Biswas, G., Nandi, S., Kuila, D., Acha ya, K., 2017. A Comp ehensi e Re iew on Food and Medicinal
P ospec s o As aeus hyg ome icus. Pha macogn. J. 9, 799–806.
h ps://doi.o g/10.5530/pj.2017.6.125
Blaalid, R., Ca lsen, T., Kuma , S., Hal o sen, R., Ugland, K.I., Fon ana, G., Kause ud, H., 2012.
Changes in he oo -associa ed ungal communi ies along a p ima y succession g adien
analysed by 454 py osequencing. Mol. Ecol. 21, 1897–1908. h ps://doi.o g/10.1111/j.1365-
294X.2011.05214.x
Blum ield, T.., Xu, Z.., 2003. Impac o ha es esidues on soil mine al ni ogen dynamics ollowing
clea all ha es ing o a hoop pine plan a ion in sub opical Aus alia. Fo . Ecol. Manage. 179, 55–
67. h ps://doi.o g/10.1016/S0378-1127(02)00485-1
Boa, E., 2004. Wild edible ungi: A global o e iew o hei use and impo ance o people, 1s ed, Non-
wood Fo es P oduc s. FAO, Rome. h ps://doi.o g/10.1007/978-3-319-13865-7
Boddy, L., Hynes, J., Bebbe , D.P., F icke , M.D., 2009. Sap o ophic co d sys ems: Dispe sal
mechanisms in space and ime. Mycoscience 50, 9–19. h ps://doi.o g/10.1007/s10267-008-0450-
4
Re e ences
64
Bone , J.A., Fische , C.R., Colinas, C., 2004. The ela ionship be ween o es age and aspec on he
p oduc ion o spo oca ps o ec omyco hizal ungi in Pinus syl es is o es s o he cen al
Py enees. Fo . Ecol. Manage. 203, 157–175. h ps://doi.o g/10.1016/j. o eco.2004.07.063
Bonge s, F., Tenngkei , T., 2010. Deg aded o es s in Eas e n A ica: In oduc ion, in: Bonge s, F.,
Tenningkei , T. (Eds.), Deg aded Fo es s in Eas A ica: Managemen and Res o a ion. Ea hscan
L d., London, UK, pp. 1–18.
B idge, P., Spoone , B., 2011. Soil ungi: di e si y and de ec ion. Plan Soil 232, 147–54.
B und e , M.C., 2009. Myco hizal associa ions and o he means o nu i ion o ascula plan s:
Unde s anding he global di e si y o hos plan s by esol ing con lic ing in o ma ion and
de eloping eliable means o diagnosis. Plan Soil 320, 37–77. h ps://doi.o g/10.1007/s11104-
008-9877-9
Bu gess, N.D., Hales, J.D.A., Ricke s, T.H., Dine s ein, E., 2006. Fac o ing species, non-species alues
and h ea s in o biodi e si y p io i isa ion ac oss he eco egions o A ica and i s islands. Biol.
Conse . 127, 383–401. h ps://doi.o g/10.1016/j.biocon.2005.08.018
Cace es, M. De, Legend e, P., 2009. Associa ions be ween species and g oups o si es: indices and
s a is ical in e ence. Ecology.
Caia a, M. V, Gómez-He nández, M., Williams-Line a, G., Ramí ez-C uz, V., 2017. Func ional di e si y o
mac omyce e communi ies along an en i onmen al g adien in a Mexican seasonally d y opical
o es . Fungal Ecol. 28, 66–75. h ps://doi.o g/10.1016/j. uneco.2017.04.005
Cai ney, J.W.G., Bas ias, B.A., 2007. In luences o i e on o es soil ungal communi ies. Can. J. Fo .
Res. 37, 207–215. h ps://doi.o g/10.1139/x06-190
Cas año, C., Alday, J.G., Lindahl, B.D., Ma ínez de A agón, J., De-Miguel, S., Colinas, C., Pa ladé, J.,
Pe a, J., Bone , J.A., de A agón, J., De-Miguel, S., Colinas, C., Pa ladé, J., Pe a, J., Bone , J.A.,
Ma ínez, J., A agón, D., Colinas, C., Pa ladé, J., Pe a, J., An onio, J., 2018. Lack o hinning
e ec s o e in e -annual changes in soil ungal communi y and di e si y in a Medi e anean pine
o es . Fo . Ecol. Manage. 424, 420–427. h ps://doi.o g/10.1016/j. o eco.2018.05.004
Cas año, C., Dejene, T., Media illa, O., Geml, J., O ia-de-Rueda, J.A., Ma ín-Pin o, P., 2019. Changes in
ungal di e si y and composi ion along a ch onosequence o Eucalyp us g andis plan a ions in
E hiopia. Fungal Ecol. 39, 328–335. h ps://doi.o g/10.1016/j. uneco.2019.02.003
Chauhan, N.M., Gu ama, A.D., Aysa, A., 2019. Endophy ic ungal di e si y isola ed om di e en ag o-
ecosys em o Ense (Ense e en e icosum) in Gedeo zone, SNNPRS, E hiopia. BMC Mic obiol.
19, 1–10. h ps://doi.o g/10.1186/s12866-019-1547-y
Chen, X.-L., Wang, D., Chen, X., Wang, J., Diao, J.-J., Zhang, J., Guan, Q.-W., 2015. Soil mic obial
unc ional di e si y and biomass as a ec ed by di e en hinning in ensi ies in a Chinese i
plan a ion. Appl. Soil Ecol. 92, 35–44. h ps://doi.o g/10.1016/j.apsoil.2015.01.018
Chen, Y.L., Xu, T. Le, Ve esoglou, S.D., Hu, H.W., Hao, Z.P., Hu, Y.J., Liu, L., Deng, Y., Rillig, M.C.,
Chen, B.D., 2017. Plan di e si y ep esen s he p e alen de e minan o soil ungal communi y
s uc u e ac oss empe a e g asslands in no he n China. Soil Biol. Biochem. 110, 12–21.
h ps://doi.o g/10.1016/j.soilbio.2017.02.015
Chu-Chou, M., G ace, L.J., 1982. Myco hizal ungi o Eucalyp us in he No h Island o New Zealand. Soil
Biol. Biochem. 14, 133–137. h ps://doi.o g/10.1016/0038-0717(82)90056-6
Cla idge, A.W., Robinson, A.P., Tan on, M.T., Cunningham, R.B., 1993. Seasonal P oduc ion o
Hypogeal Fungal Spo oca ps in a Mixed-Species Eucalyp Fo es S and in Sou h-eas e n
Aus alia. Aus . J. Bo 41, 145–167.
Cla idge, A.W., T appe, J.M., 2004. Managing habi a o mycophagous ( ungus- eeding) mammals : a
bu ning issue ?, in: Lunney, D. (Ed.), The Conse a ion o Aus alia’s Fo es Fauna. Royal
Zoological Socie y o New Sou h Wales, Mosman ile:///C:/Use s/Demelash/Downloads/s41396-
017-0027-3.pd , pp. 936–946.
Re e ences
65
Cla idge, A.W., T appe, J.M., Mills, D.J., Cla idge, D.L., 2009. Di e si y and habi a ela ionships o
hypogeous ungi. III. Fac o s in luencing he occu ence o i e-adap ed species. Mycol. Res. 113,
792–801. h ps://doi.o g/10.1016/j.myc es.2009.02.014
Cla ke, K.R., 1993. Non-pa ame ic mul i a ia e analyses o changes in communi y s uc u e. Aus al
Ecol. 18, 117–143. h ps://doi.o g/10.1111/j.1442-9993.1993. b00438.x
Clemmensen, K.E., Bah , A., O askainen, O., Dahlbe g, A., Ekblad, A., Wallande , H., S enlid, J., Finlay,
R.D., Wa dle, D.A., Lindahl, B.D., 2013. Roo s and associa ed ungi d i e long- e m ca bon
seques a ion in bo eal o es . Science (80-. ). 340, 1615–1618.
h ps://doi.o g/10.1126/science.1231923
Clemmensen, K.E., Finlay, R.D., Dahlbe g, A., S enlid, J., Wa dle, D.A., 2015. Ca bon seques a ion is
ela ed o myco hizal ungal communi y shi s du ing long- e m succession in bo eal o es s. New
Phy ol. 205, 1525–1536.
Collins, C.G., S ajich, J.E., Webe , S.E., Pombubpa, N., Diez, J.M., 2018. Sh ub ange expansion al e s
di e si y and dis ibu ion o soil ungal communi ies ac oss an alpine ele a ion g adien . Mol. Ecol.
27, 2461–2476. h ps://doi.o g/10.1111/mec.14694
Colwell, R.K., 2013. Es ima eS: s a is ical es ima ion o species ichness and sha ed species om
samples. Ve sion 9. Use ’s Guide and applica ion published a : h p://pu l.oclc.o g/es ima es.
Cowan, A.D., Smi h, J.E., Fi zge ald, S.A., 2016. Reco e ing los g ound: E ec s o soil bu n in ensi y on
nu ien s and ec omyco hiza communi ies o ponde osa pine seedlings. Fo . Ecol. Manage. 378,
160–172. h ps://doi.o g/10.1016/j. o eco.2016.07.030
Cozzolino, V., Di Meo, V., Monda, H., Spaccini, R., Piccolo, A., 2016. The molecula cha ac e is ics o
compos a ec plan g ow h, a buscula myco hizal ungi, and soil mic obial communi y
composi ion. Biol. Fe il. Soils 52, 15–29. h ps://doi.o g/10.1007/s00374-015-1046-8
C aig, A.J., Woods, S., Hoeksema, J.D., 2016. In luences o hos plan iden i y and dis u bance on spa ial
s uc u e and communi y composi ion o ec omyco hizal ungi in a no he n Mississippi uplands
ecosys em. Fungal Ecol. 24, 7–14. h ps://doi.o g/10.1016/j. uneco.2016.08.007
C ous, P.W., Rong, I.H., Wood, A., Lee, S., Glen, H., Bo ha, W., Slippe s, B., De Bee , W.Z., Wing ield,
M.J., Hawkswo h, D.L., 2006. How many species o ungi a e he e a he ip o A ica? S ud.
Mycol. 55, 13–33. h ps://doi.o g/10.3114/sim.55.1.13
Dahlbe g, A., 2002. E ec s o i e on ec omyco hizal ungi in ennoscandian bo eal o es s. Sil a Fenn.
36, 69–80. h ps://doi.o g/10.14214/s .551
Dahlbe g, A., Genney, D.R., Heilmann-Clausen, J., 2010. De eloping a comp ehensi e s a egy o
ungal conse a ion in Eu ope: cu en s a us and u u e needs. Fungal Ecol. 3, 50–64.
h ps://doi.o g/10.1016/j. uneco.2009.10.004
Dahlbe g, A., Muelle , G.M., 2011. Applying IUCN ed-lis ing c i e ia o assessing and epo ing on he
conse a ion s a us o ungal species. Fungal Ecol. 4, 147–162.
h ps://doi.o g/10.1016/j. uneco.2010.11.001
Dahlbe g, A., Schimmel, J., Taylo , A.F.S.S., Johannesson, H., 2001. Pos - i e legacy o ec omyco hizal
ungal communi ies in he Swedish bo eal o es in ela ion o i e se e i y and logging in ensi y.
Biol. Conse . 100, 151–161. h ps://doi.o g/10.1016/S0006-3207(00)00230-5
Dang, P., Vu, N.H., Shen, Z., Liu, J., Zhao, F., Zhu, H., Yu, X., Zhao, Z., 2018. Changes in soil ungal
communi ies and ege a ion ollowing a o es a ion wi h Pinus abulae o mis on he Loess
Pla eau. Ecosphe e 9. h ps://doi.o g/10.1002/ecs2.2401
Dang, P., Yu, X., Le, H., Liu, J., Shen, Z., Zhao, Z., 2017. E ec s o s and age and soil p ope ies on soil
bac e ial and ungal communi y composi ion in Chinese pine plan a ions on he Loess Pla eau.
PLoS One 12, e0186501. h ps://doi.o g/10.1371/jou nal.pone.0186501
Danielsen, F., Bu gess, N.D., Balm o d, A., 2005. Moni o ing Ma e s: Examining he Po en ial o Locally-
based App oaches. Biodi e s. Conse . 14, 2507–2542. h ps://doi.o g/10.1007/s10531-005-
Re e ences
66
8375-0
Danks, M., Lebel, T., Ve nes, K., And ew, N., 2013. T u le-like ungi spo oca ps in a eucalyp -domina ed
landscape : pa e ns in di e si y and communi y s uc u e. Fungal Di e s. 58, 143–157.
h ps://doi.o g/10.1007/s13225-012-0193-6
Da byshi e, I., Lamb, H., Ume , M., 2003. Fo es clea ance and eg ow h in no he n E hiopia du ing he
las 3000 yea s. The Holocene 13, 537–546. h ps://doi.o g/10.1191/0959683603hl644 p
Day, N.J., Dun ield, K.E., Johns one, J.F., Mack, M.C., Tu e sky, M.R., Walke , X.J., Whi e, A.L., Bal ze ,
J.L., 2019. Wild i e se e i y educes ichness and al e s composi ion o soil ungal communi ies in
bo eal o es s o wes e n Canada. Glob. Chang. Biol. 25, 2310–2324.
h ps://doi.o g/10.1111/gcb.14641
De la Va ga, H., Águeda, B., Ma ínez-Peña, F., Pa ladé, J., Pe a, J., 2012. Quan i ica ion o ex a adical
soil mycelium and ec omyco hizas o Bole us edulis in a Sco s pine o es wi h a iable
spo oca p p oduc i i y. Myco hiza 22.
Deacon, J.W., Fleming, L. V, 1992. In e ac ions o ec omyco hizal ungi, in: Allen, M. (Ed.), Myco hizal
Func ioning an In eg a i e Plan -Fungal P ocess. Chapman and Hall, New Yo k., pp. 249–300.
Dean, S., Fa e , E.C., Menges, E.S., 2015. Fi e E ec s on Soil Biogeochemis y in Flo ida Sc ubby
Fla woods. Am. Midl. Na . 174, 49–64. h ps://doi.o g/10.1674/0003-0031-174.1.49
Deg ee , J., Demuynck, L., Mukande a, A., Nyi andayambaje, G., Nzigidahe a, B., De Kesel, A., 2016.
Wild edible mush ooms, a aluable esou ce o ood secu i y and u al de elopmen in Bu undi
and Rwanda. Bio echnologie 20, 441–452.
Dejene, T., O ia-de-Rueda, J.A., Ma ín-Pin o, P., 2017a. Fungal communi y succession and spo oca p
p oduc ion ollowing i e occu ence in D y A omon ane o es s o E hiopia. Fo . Ecol. Manage.
398, 37–47. h ps://doi.o g/10.1016/j. o eco.2017.05.011
Dejene, T., O ia-de-Rueda, J.A., Ma ín-Pin o, P., 2017b. Fungal di e si y and succession ollowing s and
de elopmen in Pinus pa ula Schiede ex Schl dl. &Cham. plan a ions in E hiopia. Fo . Ecol.
Manage. 395, 9–18. h ps://doi.o g/10.1016/j. o eco.2017.03.032
Dejene, T., O ia-de-Rueda, J.A., Ma ín-Pin o, P., 2017c. Fungal di e si y and succession unde
Eucalyp us g andis plan a ions in E hiopia. Fo . Ecol. Manage. 405, 179–187.
h ps://doi.o g/10.1016/j. o eco.2017.08.050
Dejene, T., O ia-De-Rueda, J.A., Ma ín-Pin o, P., 2017d. Wild mush ooms in E hiopia: A e iew and
syn hesis o u u e pe spec i e. Fo . Sys . 26, 1–7. h ps://doi.o g/10.5424/ s/2017261-10790
Dejene, T., O ia-de-Rueda, J.A., Ma ín-Pin o, P., , 2017e. Edible wild mush ooms o E hiopia: Neglec ed
non- imbe o es p oduc s. Re .Fi o ec. Mex. 40, 391–397.
Delelegn, Y.T., Pu ahong, W., Sandén, H., Yi a e u, B., Godbold, D.L., Wube , T., 2018. T ansi ion o
E hiopian highland o es s o ag icul u e-domina ed landscapes shi s he soil mic obial
communi y composi ion. BMC Ecol. 18, 1–14. h ps://doi.o g/10.1186/s12898-018-0214-8
Demissew, S., No dal, I., 2010. Aloes and Lilies o E hiopia and E i ea. Addis Ababa.
Desalegn, G., Tadesse, W., 2004. Socio-economic Impo ance and Resou ce Po en ial o Non- imbe
Fo es P oduc s o E hiopia Ge achew, in: Tadesse, W., Michael MBogga (Eds.), Conse a ion o
Gene ic Resou ces o Non-Timbe Fo es P oduc s in E hiopia. E hiopian Ag icul u al Resea ch
O ganiza ion and In e na ional Plan Gene ic Resou ces Ins i u e, Addis Ababa, pp. 18–40.
Dessie, G., 2007. Fo es decline in sou h cen al E hiopia: Ex en , his o y and p ocesses. Ph.D. Thesis,
S ockholm Uni e si y, S ockholm.
Dh uba, S., Kuldip, G., Jaysh ee, D., A.K., S., 2015. Fungal di e si y o wel e majo ege a ional zones
o A unachal Hi-malaya, India. J. Fo . Res. 26, 579–586.
Djelloul, R., Sam aoui, B., 2011. Dis ibu ion and ecology o he supe io mush ooms o he Aulnaie o Ain
Re e ences
67
Khia (El Kala Na ional Pa k, No heas e n Alge ia). A ican J. En i on. Sci. Technol. 5, 448–456.
h ps://doi.o g/10.5897/AJEST10.242
Dobo, B., Ase a, F., As aw, Z., 2018a. Di e si y and abundance o a buscula myco hizal ungi unde
di e en plan and soil p ope ies in Sidama, sou he n E hiopia. Ag o o . Sys . 92, 91–101.
h ps://doi.o g/10.1007/s10457-016-0017-x
Dobo, B., Ase a, F., As aw, Z., 2018b. E ec o ee-ense -co ee based ag o- o es y p ac ices on
a buscula myco hizal ungi (AMF) species di e si y and spo e densi y. Ag o o . Sys . 92, 525–
540. h ps://doi.o g/10.1007/s10457-016-0042-9
Dobo, B., Ase a, F., As aw, Z., 2016. Di e si y o A buscula Myco hizal Fungi o Di e en Plan Species
G own in Th ee Land Use Types in Wensho and Shebidino Dis ic s o Sidama in Sou he n
E hiopia. Ad . Biosci. Bioeng. 4, 25. h ps://doi.o g/10.11648/j.abb.20160404.11
Do e, N.C., Kee on, W.S., 2015. S uc u al Complexi y Enhancemen inc eases ungal species ichness
in no he n ha dwood o es s. Fungal Ecol. 13, 181–192.
h ps://doi.o g/10.1016/j. uneco.2014.09.009
D eno sky, R., Vo, D., G aham, K., Scow, K., 2004. Soil wa e con en and o ganic ca bon a ailabili y a e
majo de e minan s o soil mic obial communi y composi ion. Mic ob. Ecol. 48, 424–430.
Edga , R.C, 2010. Sea ch and clus e ing o de s o magni ude as e han BLAST. Bioin o ma ics 26,
2460–2461.
Edman, M., Gus a sson, M., S enlid, J., E icson, L., 2004. Abundance and iabili y o ungal spo es along
a o es y g adien - esponses o habi a loss and isola ion? Oikos 104, 35–42.
h ps://doi.o g/10.1111/j.0030-1299.2004.12454.x
Egidi, E., Delgado-Baque izo, M., Ple , J.M., Wang, J., Eld idge, D.J., Ba dge , R.D., Maes e, F.T.,
Singh, B.K., 2019. A ew Ascomyco a axa domina e soil ungal communi ies wo ldwide. Na .
Commun. 10, 2369. h ps://doi.o g/10.1038/s41467-019-10373-z
Egidi, E., McMullan-Fishe , S., Mo gan, J.W., May, T., Zeeman, B., F anks, A.E., 2016. Fi e egime, no
ime-since- i e, a ec s soil ungal communi y di e si y and composi ion in empe a e g asslands.
FEMS Mic obiol. Le . 363, 1–11. h ps://doi.o g/10.1093/ emsle/ nw196
E hiopian, T., Expe iences, T., 2008. Pa icipa o y Fo es Managemen Bes P ac ices , Lesson Lea n
and Pa icipa o y Fo es Managemen Bes P ac ices , Lesson Lea n and.
FAO, 2020. Global Fo es Resou ces Assessmen . Rome. I aly [WWW Documen ]. URL
h p://www. ao.o g/3/i1757e/i1757e00.h m (accessed 6.20.21).
FAO, 2005. S a e o he Wo ld’s o es s. Food and Ag icul u e O ganiza ion o he Uni ed Na ions, Rome,
I aly.
Fen a, M.M., 2014. Human-wildli e con lic s: case s udy in Wondo Gene dis ic , Sou he n E hiopia. Ag ic.
Fo . Fish. 3, 352–362. h ps://doi.o g/10.1016/j.jneume h.2014.08.006
Fe nández-Toi án, L.M., Ág eda, T., Olano, J.M., 2006. S and age and sampling yea e ec on he ungal
ui body communi y in Pinus pinas e o es s in cen al Spain. Can. J. Bo . 84, 1249–1258.
h ps://doi.o g/10.1139/b06-087
Fe nández, A., Sánchez, S., Ga cía, P., Sánchez, J., 2020. Mac o ungal di e si y in an isola ed and
agmen ed Medi e anean Fo es ecosys em. Plan Biosys . - An In . J. Deal. wi h all Asp. Plan
Biol. 154, 139–148. h ps://doi.o g/10.1080/11263504.2019.1578285
Fe nandez, C.W., Nguyen, N.H., S e anski, A., Han, Y., Hobbie, S.E., Mon gome y, R.A., Reich, P.B.,
Kennedy, P.G., 2016. Ec omyco hizal ungal esponse o wa ming is linked o poo hos
pe o mance a he bo eal‐ empe a e eco one. Glob. Chang. Biol. 23, 1598–1609.
h ps://doi.o g/10.1111/gcb.13510
Fe a i, B.C., Bisse , A., Snape, I., an Do s , J., Palme , A.S., Ji, M., Siciliano, S.D., S a k, J.S., Winsley,
T., B own, M. V., 2016. Geological connec i i y d i es mic obial communi y s uc u e and
Re e ences
74
Pang, X., Bao, W., Zhu, B., Cheng, W., 2013. Responses o soil espi a ion and i s empe a u e sensi i i y
o hinning in a pine plan a ion. Ag ic. Fo . Me eo ol. 171–172, 57–64.
h ps://doi.o g/10.1016/j.ag o me .2012.12.001
Pa a icini, V., Micheli, F., Mon e alcone, M., Villa, E., Mo i, C., Bianchi, C.N., 2010. Rapid assessmen
o epiben hic communi ies: A compa ison be ween wo isual sampling echniques. J. Exp. Ma .
Bio. Ecol. 395, 21–29. h ps://doi.o g/10.1016/j.jembe.2010.08.005
Pa inson, G.S., Hammil, K.A., Su on, B.G., McCGEE, P.., 2006. Simula ed i e educes he densi y o
a buscula myco hizal ungi a he soil su ace. Mycol. Res. 103, 491–496.
Peay, K., Ga belo o, M., B uns, T., 2010. E idence o dispe sal limi a ion in soil mic oo ganisms: isola ion
educes species ichness on myco hizal ee islands. Ecology 91, 3631–3640.
Peay, K.G., 2014. Back o he u u e: na u al his o y and he way o wa d in mode n ungal ecology.
Fungal Ecol. 12, 4–9. h ps://doi.o g/10.1016/j. uneco.2014.06.001
Pegle , D.N., 1977. A p elimina y aga ic lo a o Eas A ica. Kew Bull Add Se 6, 615.
Pegle , D., 1969. S udies on A ican Aga icales: 2. Kew Bull 23, 219–249.
Pegle , D.N., 1968. S udies on A ican Aga icales: 1. Kew Bull 21, 499–533.
Pinhei o, J., Ba es, D., DebRoy, S., Sa ka , D., Team, R.C., 2016. Nlme: Linea and Nonlinea Mixed
E ec s Models. R Package Ve sion 3.1-128. h p://CRAN. R-p ojec . o g/package=nlme.
Pinna, S., Gé y, M.-F., Cô é, M., Si ois, L., 2010. Fac o s in luencing uc i ica ion phenology o edible
mush ooms in a bo eal mixed o es o Eas e n Canada. Fo . Ecol. Manage. 260, 294–301.
h ps://doi.o g/10.1016/j. o eco.2010.04.024
Ponde , F., Tad os, M., Loewens ein, E.F., 2009. Mic obial p ope ies and li e and soil nu ien s a e wo
p esc ibed i es in de eloping sa annas in an upland Missou i Oza k Fo es . Fo . Ecol. Manage.
257, 755–763. h ps://doi.o g/10.1016/j. o eco.2008.10.009
Quo eshi, A.M., 2008. The Use o Myco hizal Bio echnology in Res o a ion o Dis u bed Ecosys em, in:
Siddiqui, Z.A., Akh a , M.S., Fu ai, K. (Eds.), Myco hizae: Sus ainable Ag icul u e and Fo es y.
Sp inge Ne he lands, Do d ech , pp. 303–320. h ps://doi.o g/10.1007/978-1-4020-8770-7_13
R Co e Team, 2020. R: A language and en i onmen o s a is ical compu ing. R Founda ion o S a is ical
Compu ing, Vienna, Aus ia.
Radomi , M., Mesud, A., Žaklina, M., 2018. Conse a ion and ade o wild edible mush ooms o Se bia -
His o y, s a e o he a and pe spec i es. Na . Conse . 25, 31–53.
h ps://doi.o g/10.3897/na u econse a ion.25.21919
Rammeloo, J., Walleyn, R., 1993. The edible ungi o A ica Sou h o he Saha a: a li e a u e su ey. Sc .
Bo Belg 5, 1–62.
Rasche, F., Knapp, D., Kaise , C., Ko anda, M., Ki zle , B., Zechmeis e -Bol ens e n, S., Rich e , A.,
Sessi sch, A., 2011. Seasonali y and esou ce a ailabili y con ol bac e ial and a chaeal
communi ies in soils o a empe a e beech o es . ISME J. 5, 389–402.
h ps://doi.o g/10.1038/ismej.2010.138
Reazin, C., Mo is, S., Smi h, J.E., Cowan, A.D., Jumpponen, A., 2016. Fi es o di e ing in ensi ies apidly
selec dis inc soil ungal communi ies in a No hwes US ponde osa pine o es ecosys em. Fo .
Ecol. Manage. 377, 118–127. h ps://doi.o g/10.1016/j. o eco.2016.07.002
Redondo, M.A., Be lin, A., Bobe g, J., Oli a, J., 2020. Vege a ion ype de e mines spo e deposi ion wi hin
a o es -ag icul u al mosaic landscape. FEMS Mic obiol. Ecol. 96, 1–12.
h ps://doi.o g/10.1093/ emsec/ iaa082
Re e chon, F., Del O ega-La ocea, P.M., Pé ez-Mo eno, J., 2010. Sap ophy ic ungal communi ies
change in di e si y and species composi ion ac oss a olcanic soil ch onosequence a Sie a del
Chichinau zin, Mexico. Ann. Mic obiol. 60, 217–226. h ps://doi.o g/10.1007/s13213-010-0030-7
Re e ences
75
Rich e , A., Schöning, I., Kahl, T., Bauhus, J., Ruess, L., 2018. Fo es Ecology and Managemen
Regional en i onmen al condi ions shape mic obial communi y s uc u e s onge han local o es
managemen in ensi y. Fo . Ecol. Manage. 409, 250–259.
h ps://doi.o g/10.1016/j. o eco.2017.11.027
Rincón, A., Pueyo, J.J., 2010. E ec o i e se e i y and si e slope on di e si y and s uc u e o he
ec omyco hizal ungal communi y associa ed wi h pos - i e egene a ed Pinus pinas e Ai .
seedlings. Fo . Ecol. Manage. 260, 361–369. h ps://doi.o g/10.1016/j. o eco.2010.04.028
Rincón, A., San ama ía-Pé ez, B., Rabasa, S.G., Coince, A., Ma çais, B., Buée, M., 2015.
Compa men alized and con as ed esponse o ec omyco hizal and soil ungal communi ies o
Sco s pine o es s along ele a ion g adien s in F ance and Spain. En i on. Mic obiol. 17, 3009–
3024. h ps://doi.o g/10.1111/1462-2920.12894
Rosens ock, N.P., Be ne , C., Smi s, M.M., K ám, P., Wallande , H., 2016. The ole o phospho us,
magnesium and po assium a ailabili y in soil ungal explo a ion o mine al nu ien sou ces in
No way sp uce o es s. New Phy ol. 211, 542–553. h ps://doi.o g/10.1111/nph.13928
Rossman, A.., Samuel, G.., Roge son, C.., Lowen, R., 1999. Gene a o Bionec iaceae, Hypoc eaceae
and Nec i- aceae (Hypoc eales, Ascomyce es). S ud. Mycol. 42, 1–260.
Rousk, J., Båå h, E., B ookes, P.C., Laube , C.L., Lozupone, C., Capo aso, J.G., Knigh , R., Fie e , N.,
2010. Soil bac e ial and ungal communi ies ac oss a pH g adien in an a able soil. ISME J. 4,
1340–1351. h ps://doi.o g/10.1038/ismej.2010.58
Roy, M., Dubois, M.-P., P o i , M., Vinceno , L., Desma ais, E., Selosse, M.-A., 2008. E idence om
popula ion gene ics ha he ec omyco hizal basidiomyce e Lacca ia ame hys ina is an ac ual
mul ihos symbion . Mol. Ecol. 17, 2825–2838. h ps://doi.o g/10.1111/j.1365-294X.2008.03790.x
Rudol , K., Mo schhause , T., Pál-Fám, F., Bo a-Duká , Z., 2013. Explo ing he ela ionship be ween
mac o ungi di e si y, abundance, and ascula plan di e si y in semi-na u al and managed
o es s in no h-eas Hunga y. Ecol. Res. 28, 543–552. h ps://doi.o g/10.1007/s11284-013-1044-
y
Saha, D., Sund iyal, R.C., 2012. U iliza ion o non- imbe o es p oduc s in humid opics: Implica ions o
managemen and li elihood. Fo . Policy Econ. 14, 28–40.
h ps://doi.o g/10.1016/j. o pol.2011.07.008
Samuels, G., 1996. T ichode ma: A e iew o biology and sys ema ics o he genus. Mycol. Res. 923–
935.
Schmi , J.P., Muelle , G.M., Leacock, P.R., Ma a, J.L., (Flo ence) Wu, Q., Huang, Y., 2005. Assessmen
o ee species ichness as a su oga e o mac o ungal species ichness. Biol. Conse . 121, 99–
110. h ps://doi.o g/10.1016/j.biocon.2004.04.013
Schön, M.E., Niesel , K., Ga nica, S., 2018. Belowg ound ungal communi y di e si y and composi ion
associa ed wi h No way sp uce along an al i udinal g adien . PLoS One 13, e0208493.
h ps://doi.o g/10.1371/jou nal.pone.0208493
Semeno a-Nelsen, T.A., Pla , W.J., Pa e son, T.R., Hu man, J., Sikes, B.A., 2019. F equen i e
eo ganizes ungal communi ies and slows decomposi ion ac oss a he e ogeneous pine sa anna
landscape. New Phy ol. 224, 916–927. h ps://doi.o g/10.1111/nph.16096
Semwal, K.C., Lemma, H., Dhyani, A., Equa , G., Amha e, S., 2014. Mush oom: Na u e’s T easu e in
E hiopia. Momona E hiop. J. Sci. ©CNCS 6, 138–147.
Sewne , T.C., Tuju, F.A., 2013. A buscula myco hizal ungi associa ed wi h shade ees and Co ea
a abica L. in a co ee-based ag o o es y sys em in Bonga, Sou hwes e n E hiopia. A ika Focus
26, 111–131.
Shay, P.-E., Winde , R.S., T o ymow, J.A., 2015. Nu ien -cycling mic obes in coas al Douglas- i o es s:
egional-scale co ela ion be ween communi ies, in si u clima e, and o he ac o s. F on .
Mic obiol. 6. h ps://doi.o g/10.3389/ micb.2015.01097
Re e ences
76
Shen, J., Chen, C.R., Lewis, T., 2016. Long e m epea ed i e dis u bance al e s soil bac e ial di e si y
bu no he abundance in an Aus alian we scle ophyll o es . Sci. Rep. 6, 19639.
h ps://doi.o g/10.1038/s ep19639
Shi, L.-L., Mo ime , P.E., Fe y Slik, J.W., Zou, X.-M., Xu, J., Feng, W.-T., Qiao, L., 2014. Va ia ion in
o es soil ungal di e si y along a la i udinal g adien . Fungal Di e s. 64, 305–315.
h ps://doi.o g/10.1007/s13225-013-0270-5
Sibe chico , A., Julien-La e iè e, A., Du ou , A.-B., Thioulouse, J., D ay, S., 2017. adeg aphics: An S4
La ice-Based Package o he Rep esen a ion o Mul i a ia e Da a. R J. 9, 198–212.
Siciliano, S.D., Palme , A.S., Winsley, T., Lamb, E., Bisse , A., B own, M. V., an Do s , J., Ji, M., Fe a i,
B.C., G ogan, P., Chu, H., Snape, I., 2014. Soil e ili y is associa ed wi h ungal and bac e ial
ichness, whe eas pH is associa ed wi h communi y composi ion in pola soil mic obial
communi ies. Soil Biol. Biochem. 78, 10–20. h ps://doi.o g/10.1016/j.soilbio.2014.07.005
Singe , R., 1965. Ma asmius. Fl. Icon. Champ. Congo 14, 253–278.
Si o aw, R., Lulekal, E., Aba e, D., 2020. E hnomycological s udy o edible and medicinal mush ooms in
Menge Dis ic , Asossa Zone, Benshangul Gumuz Region, E hiopia. J. E hnobiol. E hnomed. 16,
1–14. h ps://doi.o g/10.1186/s13002-020-00361-9
Smi h, J.E., Klube , L.A., Jennings, T.N., McKay, D., B enne , G., Sulzman, E.W., 2017. Does he
p esence o la ge down wood a he ime o a o es i e impac soil eco e y? Fo . Ecol. Manage.
391, 52–62. h ps://doi.o g/10.1016/j. o eco.2017.02.013
Smi h, J.E., McKay, D., B enne , G., McI e , J., Spa a o a, J.W., 2005. Ea ly impac s o o es es o a ion
ea men s on he ec omyco hizal ungal communi y and ine oo biomass in a mixed coni e
o es . J. Appl. Ecol. 42, 526–535. h ps://doi.o g/10.1111/j.1365-2664.2005.01047.x
Smi h, S., Read, D., 2008. Myco hizal symbiosis. Camb idge, UK: Academic P ess.
Solomon, M.M., 2016. Impo ance o non- imbe o es p oduc ion in sus ainable o es managemen , and
i s implica ion on ca bon s o age and biodi e si y conse a ion in E hiopia. In . J. Biodi e s.
Conse . 8, 269–277. h ps://doi.o g/10.5897/ijbc2015.0919
Soudzilo skaia, N.A., Vaessen, S., Ba celo, M., He, J., Rahimlou, S., Aba enko , K., B und e , M.C.,
Gomes, S.I.F., Me ckx, V., Tede soo, L., 2020. FungalRoo : global online da abase o plan
myco hizal associa ions. New Phy ol. 227, 955–966. h ps://doi.o g/10.1111/nph.16569
S aa sma, G., Aye , F., Egli, S., 2001. Species ichness, abundance, and phenology o ungal ui bodies
o e 21 yea s in a Swiss o es plo . Mycol. Res. 105, 515–523.
h ps://doi.o g/10.1017/S0953756201004154
Suggi , A.J., Gillingham, P.K., Hill, J.K., Hun ley, B., Kunin, W.E., Roy, D.B., Thomas, C.D., 2011. Habi a
mic oclima es d i e ine-scale a ia ion in ex eme empe a u es. Oikos 120, 1–8.
h ps://doi.o g/10.1111/j.1600-0706.2010.18270.x
Tadesse, W., Gezahgne, A., Tesema, T., Shibabaw, B., 2019. Plan a ion Fo es s in Amha a Region :
Challenges and Bes Measu es o Fu u e Imp o emen s. Wo ld J. Ag ic. Res. 7, 149–157.
h ps://doi.o g/10.12691/wja -7-4-5
Taudiè e, A., Richa d, F., Ca caille , C., 2017. Re iew on i e e ec s on ec omyco hizal symbiosis , an
unachie ed wo k o a scalding opic. Fo . Ecol. Manage. 391, 446–457.
h ps://doi.o g/10.1016/j. o eco.2017.02.043
Taylo , A.F.S., 2002. Fungal di e si y in ec omyco hizal communi ies. Plan Soil 19–28.
Taylo , D.L., Hollingswo h, T.N., McFa land, J.W., Lennon, N.J., Nusbaum, C., Ruess, R.W., 2014. A i s
comp ehensi e census o ungi in soil e eals bo h hype di e si y and ine-scale niche
pa i ioning. Ecol. Monog . 84, 3–20. h ps://doi.o g/10.1890/12-1693.1
Tede soo, L., Bah am, M., Caj haml, T., Põlme, S., Hiiesalu, I., Anslan, S., Ha end, H., Buegge , F.,
P i sch, K., Ko iche a, J., Aba enko , K., 2016a. T ee di e si y and species iden i y e ec s on soil
Re e ences
77
ungi , p o is s and animals a e con ex dependen 346–362.
h ps://doi.o g/10.1038/ismej.2015.116
Tede soo, Leho, Bah am, M., Dickie, I.A., 2014. Does hos plan ichness explain di e si y o
ec omyco hizal ungi? Re-e alua ion o Gao e al . (2013) da a se s e eals sampling e ec s.
Mol. Ecol. 23, 992–995. h ps://doi.o g/10.1111/mec.12660
Tede soo, L., Bah am, M., Polme, S., Koljalg, U., Yo ou, N.S., Wijesunde a, R., Ruiz, L. V., Vasco-
Palacios, A.M., Thu, P.Q., Suija, A., Smi h, M.E., Sha p, C., Salu ee , E., Sai a, A., Rosas, M.,
Rii , T., Ra kowsky, D., P i sch, K., Poldmaa, K., Piepenb ing, M., Phos i, C., Pe e son, M., Pa s,
K., Pa el, K., O sing, E., Nouh a, E., Njouonkou, A.L., Nilsson, R.H., Mo gado, L.N., Mayo , J.,
May, T.W., Majuakim, L., Lodge, D.J., Lee, S.S., La sson, K.-H., Kohou , P., Hosaka, K., Hiiesalu,
I., Henkel, T.W., Ha end, H., Guo, L. -d., G eslebin, A., G ele , G., Geml, J., Ga es, G., Duns an,
W., Dunk, C., D enkhan, R., Dea naley, J., De Kesel, A., Dang, T., Chen, X., Buegge , F.,
B ea ley, F.Q., Boni o, G., Anslan, S., Abell, S., Aba enko , K., 2014. Global di e si y and
geog aphy o soil ungi. Science (80-. ). 346, 1256688–1256688.
h ps://doi.o g/10.1126/science.1256688
Tede soo, L., Hansen, K., Pe y, B.A., Kjølle , R., Taylo , D.L., Hollingswo h, T.N., McFa land, J.W.,
Lennon, N.J., Nusbaum, C., Ruess, R.W., Lodge, D.J., Ammi a i, J.F., O’dell, T.E., Muelle , G.M.,
Huhndo , S.M., Wang, C.J., S okland, J.N., Schmi , J.P., Ry a den, L., Leacock, P.R., Ma a, M.,
Umaña, L., Wu, Q.F., Czede pil z, D.L., Glassman, S.I., Le ine, C.R., Di occo, A.M., Ba les, J.J.,
B uns, T.D., Hul, S., Minna, S., Jukka, P., Kaja , K., F ank, B., Tommaso, R., A i, J., F ed, O.A.,
Jussi, H., 2016b. Te es ial and Lignicolous Mac o ungi. ISME J. 10, 1228–1239.
h ps://doi.o g/10.1038/ismej.2015.182
Te onen, K., Oldén, A., Halme, P., 2019. Ec omyco hizal ungi in wood-pas u es: {Communi ies} a e
de e mined by ees and soil p ope ies, no by g azing. Ag ic. Ecosys . En i on. 269, 13–21.
h ps://doi.o g/10.1016/j.agee.2018.09.015
Tes aye, M.A., Ga di, O., Anbessa, T.B., Blase , J., 2020. Abo eg ound biomass, g ow h and yield o
some selec ed in oduced ee species, namely Cup essus lusi anica, Eucalyp us saligna, and
Pinus pa ula in Cen al Highlands o E hiopia. J. Ecol. En i on. 44, 1–18.
h ps://doi.o g/10.1186/s41610-019-0146-z
Teshome, T., 2011. Analysis o esin and u pen ine oil cons i uen s o Pinus pa ula g own in E hiopia
Abs ac : 3.
Tian, J., Zhu, D., Wang, J., Wu, B., Hussain, M., Liu, X., 2018. En i onmen al ac o s d i ing ungal
dis ibu ion in eshwa e lake sedimen s ac oss he Headwa e Region o he Yellow Ri e ,
China. Sci. Rep. 8, 4–11. h ps://doi.o g/10.1038/s41598-018-21995-6
Tilman, D., Cassman, K.G., Ma son, P.A., Naylo , R., Polasky, S., 2002. Ag icul u al sus ainabili y and
in ensi e p oduc ion p ac ices. Na u e 418, 671–677. h ps://doi.o g/10.1038/na u e01014
Toi anen, T., Ma kkanen, A., Ko iaho, J.S., Halme, P., 2012. The e ec o o es uel ha es ing on he
ungal di e si y o clea -cu s. Biomass and Bioene gy 39, 84–93.
h ps://doi.o g/10.1016/j.biombioe.2011.11.016
Tomao, A., An onio Bone , J., Cas año, C., De-Miguel, S., 2020. How does o es managemen a ec
ungal di e si y and communi y composi ion? Cu en knowledge and u u e pe spec i es o he
conse a ion o o es ungi. Fo . Ecol. Manage. 457, 117678.
h ps://doi.o g/10.1016/j. o eco.2019.117678
Tó hmé ész, B., 1995. Compa ison o di e en me hods o di e si y o de ing. J. Veg. Sci. 6, 283–290.
h ps://doi.o g/10.2307/3236223
T appe, M.J., C omack, K., T appe, J.M., Pe akis, D.D.B., Caza es-Gonzales, E., Cas ellano, M.A.,
Mille , S.L., 2009. In e ac ions among p esc ibed i e, soil a ibu es, and myco hizal communi y
s uc u e a C a e Lake Na ional Pa k, O egon, USA. Fi e Ecol. 5, 30–50.
h ps://doi.o g/10.4996/ i eecology.0502030
Re e ences
78
T ipa hi, S., Mish a, N.K., T ipa hi, B.P., 2018. Compa a i e s udy on a ie al a ia ion on nu i ional
quali y o mush oom. J. Pha macogn. Phy ochem. 7, 1896–1898.
Tuno, N., 2001. Mush oom u iliza ion by he Majangi , an E hiopian ibe. Mycologis 15, 78–79.
h ps://doi.o g/10.1016/S0269-915X(01)80087-2
Ullah, S., Ai, C., Ding, W., Jiang, R., Zhao, S., Zhang, J., Zhou, W., Hou, Y., He, P., 2019. The esponse
o soil ungal di e si y and communi y composi ion o long- e m e iliza ion. Appl. Soil Ecol. 140,
35–41. h ps://doi.o g/10.1016/j.apsoil.2019.03.025
U celay, C., Longo, S., Geml, J., Tecco, P.A., Nouh a, E., 2017. Co-in asi e exo ic pines and hei
ec omyco hizal symbion s show capabili ies o wide dis ance and al i udinal ange expansion.
Fungal Ecol. 25, 50–58. h ps://doi.o g/10.1016/j. uneco.2016.11.002
an de Heijden, M.G.A., Ba dge , R.D., an S aalen, N.M., 2008. The unseen majo i y: soil mic obes as
d i e s o plan di e si y and p oduc i i y in e es ial ecosys ems. Ecol. Le . 11, 296–310.
h ps://doi.o g/10.1111/j.1461-0248.2007.01139.x
Vašu o á, M., Edwa ds-Jonášo á, M., Bald ian, P., Če mák, M., Cudlín, P., 2017. Dis inc en i onmen al
a iables d i e he communi y composi ion o myco hizal and sap o ophic ungi a he alpine
eeline eco one. Fungal Ecol. 27, 116–124. h ps://doi.o g/10.1016/j. uneco.2016.08.010
Visse , S., 1995. Ec omyco hizal succession in jack pine s ands ollowing wild i e. New Phy ol. 129, 389–
401.
Wald op, M.P., Zak, D.R., Blackwood, C.B., Cu is, C.D., Tilman, D., 2006. Resou ce a ailabili y con ols
ungal di e si y ac oss a plan di e si y g adien : {Resou ce} a ailabili y con ols ungal di e si y.
Ecol. Le . 9, 1127–1135. h ps://doi.o g/10.1111/j.1461-0248.2006.00965.x
Wang, Q.-K., Wang, S.-L., 2008. Soil mic obial p ope ies and nu ien s in pu e and mixed Chinese i
plan a ions. J. Fo . Res. 19, 131–135. h ps://doi.o g/10.1007/s11676-008-0022-7
Wang, Y., Wei, X., del Campo, A.D., Winkle , R., Wu, J., Li, Q., Liu, W., 2019. Ju enile hinning can
e ec i ely mi iga e he e ec s o d ough on ee g ow h and wa e consump ion in a young Pinus
con o a s and in he in e io o B i ish Columbia, Canada. Fo . Ecol. Manage. 454, 117667.
h ps://doi.o g/h ps://doi.o g/10.1016/j. o eco.2019.117667
Wani, B.A., Bodha, R.H., Wani, A.H., 2010. Nu i ional and medicinal impo ance o mush ooms 4, 2598–
2604. h ps://doi.o g/10.5897/JMPR09.565
Wa dle, D.A., Ba dge , R., Kli onomos, J., H, S., an de Pu en, W., Wall, D., 2004. Ecological Linkages
Be ween Abo eg ound and Belowg ound Bio a. Science (80-. ). 304, 1629–1633.
h ps://doi.o g/10.1126/science.1094875
Wassie, A., S e ck, F.J., Bonge s, F., 2010. Species and s uc u al di e si y o chu ch o es s in a
agmen ed E hiopian Highland landscape. J. Veg. Sci. 21, 938–948.
h ps://doi.o g/10.1111/j.1654-1103.2010.01202.x
Wassie, A., S e ck, F.J., Teke ay, D., Bonge s, F., 2009. E ec s o li es ock exclusion on ee
egene a ion in chu ch o es s o E hiopia. Fo . Ecol. Manage. 257, 765–772.
h ps://doi.o g/10.1016/j. o eco.2008.07.032
Wassie, A., Teke ay, D., Powell, N., 2005. Chu ch o es s in No h Gonde Adminis a i e Zone, no he n
E hiopia. Fo . T ees Li elihoods 15, 349–373. h ps://doi.o g/10.1080/14728028.2005.9752536
Weldeki os, M., Bi hane, E., Zeweld, W., Teweldebi han, S., 2017. Cha ac e iza ion, Nu i ional Value and
Consump ion Habi o Wild Mush oom in Tig ay, No he n E hiopia Meha i. ANADOLU, J.o AARI
22, 97–115.
Welema iam, M., Kebede, F., Bedadi, B., Bi hane, E., 2018. E ec o communi y-based soil and wa e
conse a ion p ac ices on a buscula myco hizal ungi ypes, spo e densi ies, oo coloniza ion,
and soil nu ien s in he no he n highlands o {E hiopia}. Chem. Biol. Technol. Ag ic. 5, 9.
h ps://doi.o g/10.1186/s40538-018-0121-4
Re e ences
79
Whi e, T.J., B uns, S., Lee, S., Taylo , J., 1990. Ampli ica ion and di ec sequencing o ungal ibosomal
RNA genes o phylogene ics, in: Innis, M.A., Gel and, D.H., Sninsky, J.J., Whi e, T.J. (Eds.),
PCR P o ocols: A Guide o Me hods and Applica ions. Academic P ess, New Yo k, pp. 315–322.
h ps://doi.o g/ci eulike-a icle-id:671166
Winbe g, E., 2011. Pa icipa o y Fo es Managemen in E hiopia , P ac ices and Expe iences. Addis
Ababa.
Woldegio gis, A.Z., Aba e, D., Haki, G.D., Ziegle , G.R., 2014. An ioxidan p ope y o edible mush ooms
collec ed om E hiopia. Food Chem. 157, 30–36. h ps://doi.o g/10.1016/j. oodchem.2014.02.014
Wu, D., Zhang, M., Peng, M., Sui, X., Li, W., Sun, G., 2019. Va ia ions in Soil Func ional Fungal
Communi y S uc u e Associa ed Wi h Pu e and Mixed Plan a ions in Typical Tempe a e Fo es s
o China. F on . Mic obiol. 10. h ps://doi.o g/10.3389/ micb.2019.01636
Wube , T., Ko ke, I., Teke ay, D., Obe winkle , F., 2009. A buscula myco hizal ungal communi y
s uc u es di e be ween co-occu ing ee species o d y A omon ane opical o es , and hei
seedlings exhibi po en ial o ap isola es sui ed o e o es a ion. Mycol. P og. 8, 317–328.
h ps://doi.o g/10.1007/s11557-009-0602-8
Wube , T., Ko ke, I., Teke ay, D., Obe winkle , F., 2003. Myco hizal s a us o indigenous ees in d y
A omon ane o es s o E hiopia. Fo . Ecol. Manage. 179, 387–399.
h ps://doi.o g/10.1016/S0378-1127(02)00546-7
Wube , T., Weiß, M., Ko ke, I., Teke ay, D., Obe winkle , F., 2004. Molecula di e si y o a buscula
myco hizal ungi in P unus a icana, an endange ed medicinal ee species in d y A omon ane
o es s o E hiopia. New Phy ol. 161, 517–528. h ps://doi.o g/10.1046/j.1469-8137.2003.00924.x
Yada , R.H., Mekonnen, E., 2013. Deg ada ion o P ese ed and Isola ed Chu ch Fo es s in Asebo ,
E hiopia. Eu . Acad. Res. I, 529–534. h ps://doi.o g/10.1108/13555851211218020
Yang, T., Adams, J.M., Shi, Y., He, J., Jing, X., Chen, L., Tede soo, L., Chu, H., 2017. Soil ungal
di e si y in na u al g asslands o he Tibe an Pla eau : associa ions wi h plan di e si y and
p oduc i i y. New Phy ol. 1, 1–10. h ps://doi.o g/10.1111/nph.14606
Zak, D.R., Holmes, W.E., Whi e, D.C., Peacock, A.D., Tilman, D., 2003. Plan di e si y, soil mic obial
communi ies, and ecosys em unc ion: a e he e any links? Ecology 84, 2042–2050.
h ps://doi.o g/10.1890/02-0433
Zaka ia, A.J., Boddy, L., 2002. Mycelial o aging by Resinicium bicolo : In e ac i e e ec s o esou ce
quan i y, quali y and soil composi ion. FEMS Mic obiol. Ecol. 40, 135–142.
h ps://doi.o g/10.1016/S0168-6496(02)00221-0
Zegeye, H., Teke ay, D., Kelbessa, E., 2011. Di e si y and egene a ion s a us o woody species in Ta a
Gedam and Abebaye o es s, no hwes e n E hiopia. J. Fo . Res. 22, 315–328.
h ps://doi.o g/10.1007/s11676-011-0176-6
Zeleke, G., Dejene, T., Tadesse, W., Agúndez, D., Ma ín-Pin o, P., 2020. E hnomycological Knowledge
o Th ee E hnic G oups in E hiopia. Fo es s 11, 875. h ps://doi.o g/10.3390/ 11080875
Zewdie, M., Tes aye, A., Gi ma, Y., 2010. Managemen plan o o es plan a ions o WGCF-NR. In: Final
Documen , Wondo Gene , E hiopia. Wondo Gene , E hiopia.
Zhang, N., Li, Y., Wube , T., B uelheide, H., Liang, Y., Pu ahong, W., Busco , F., Ma, K., 2018. T ee
species ichness and ungi in eshly allen lea li e : Unique pa e ns o ungal species
composi ion and hei implica ions o enzyma ic decomposi ion. Soil Biol. Biochem. 127, 120–
126. h ps://doi.o g/10.1016/j.soilbio.2018.09.023
Zhao, A., Liu, L., Xu, T., Shi, L., Xie, W., Zhang, W., Fu, S., Feng, H., Chen, B., 2018. In luences o
Canopy Ni ogen and Wa e Addi ion on AM Fungal Biodi e si y and Communi y Composi ion in a
Mixed Deciduous Fo es o China. F on . Plan Sci. 9. h ps://doi.o g/10.3389/ pls.2018.01842
Zhu, W., Cai, X., Liu, X., Wang, J., Cheng, S., Zhang, X., Li, D., Li, M., 2010. Soil mic obial popula ion
dynamics along a ch onosequence o mois e e g een b oad-lea ed o es succession in
Re e ences
80
sou hwes e n China. J. M . Sci. 7, 327–338. h ps://doi.o g/10.1007/s11629-010-1098-z
O iginal a icles
O iginal a icles
83
O iginal a icle I
Comunidades de hongos del suelo y sucesión después de los
incendios o es ales en los bosques secos A omon anos de
E iopía, un ecosis ema muy di e so y poco explo ado
Demelash Alema,b,
Ta ek
Dejeneb,
Juan And és
O ia-de-Ruedaa,
Józse
Gemlc,,
Ca les
Cas año
a
,
,
Jane E. Smi hd, Pablo
Ma ín-Pin o
a
,
*
aSus ainable
Fo es
Managemen
Resea ch
Ins i u e,
Uni e si y o
Valladolid,
A da. Mad id 44,
34071
Palencia, Spain
bE hiopian En i onmen
and Fo es Resea ch
Ins i u e,
Addis Ababa,
E hiopia
c
MTA-EKE Lendüle
En i onmen al
Mic obiome Resea ch G oup,
Esz e házy
Ká oly Uni e si y, Leányka u. 6,
H-3300
Ege ,
Hunga y
d
USDA Fo es Se ice Pacific No hwes Resea ch
S a ion,
Fo es y Sciences
Labo a o y, 3200
SW
Je e son
Way, Co allis, OR
97331,
USA
Fo . Ecol. Manage. 474(118328) h ps://doi.o g/10.1016/j. o eco.2020.118328
Resumen
Los bosques secos a omon anos de E iopía son ecosis emas complejos que ienen
impo an es unciones económicas y ecológicas. Sin emba go, los incendios
ecu en es han sido una uen e de pe u bación pa a es os bosques. E aluamos el
e ec o del uego en las comunidades de hongos del suelo en un bosque a omon ano
seco emanen e en Wondo Gene , en el su de E iopía, median e el análisis de
mues as de suelo ecolec adas de odales no quemados y de odales uno y diez años
después del incendio u ilizando me aba coding de ADN del ADN ITS2. El análisis
indicó que la comunidad de hongos del suelo e a más di e sa poco después de una
pe u bación po incendio y disminuyó con el iempo. La composición de la comunidad
úngica ambién di i ió en e los odales. Nues os esul ados ambién indica on que las
di e encias en la di e sidad de hongos dependían del odal y no de la c onología de la
his o ia de los incendios en es e sis ema o es al. Encon amos un mayo núme o de
especies de mico izas en odales quemados, lo que sugie e que es os simbion es de
hongos pod ían compensa los e ec os del es és nu icional causado po el uego en
es as á eas. La composición de la comunidad úngica ambién se co elacionó
signi ica i amen e con el con enido de ma e ia o gánica, po asio y magnesio en el
suelo. Es e abajo pod ía conside a se como un es udio de caso ya que las pa celas
se es ablecie on en un solo odal pa a cada a amien o en los bosques secos
a omon anos de E iopía. Po lo an o, ecomendamos es udios adicionales y las
conclusiones con espec o a o os odales deben oma se con p ecaución.
Palab as cla e: Va iable edá ica, E iopía, Incendio o es al, g upos uncionales de
hongos, secuenciación de o en e de iones, ópicos.
ungi in his o de can also be sap o ophic, en omopa hogenic, and
mycopa asi ic (Rossman e al., 1999). In addi ion o hei ecological
and economic impo ance, he Hypoc eales a e also conside ed o be
he mos impo an egula o s o insec and ungal popula ions and,
he e o e, a e used in ag icul u e as biocon ol agen s (Ca u he s and
Hu al, 1990; Esse and El-Gholl, 1993; Rossman e al., 1999; Samuels,
1996). The second la ges o de o Ascomyco a de ec ed in his s udy
was he Pleospo ales. This o de comp ises sap o ophs o ungi ha a e
pa asi es o ascula plan s (K uys e al., 2006). Some species om his
o de a e also ound on animal dung (K uys e al., 2006), a small
numbe occu as lichens (Semeno a-Nelsen e al., 2019) and as ock-
inhabi ing ungi (Ruibal e al., 2009). The epiphy ic o endophy ic ungi
o he Pleospo ales a e mainly sap o ophic bu also play a key ole in
causing plan diseases such as s em canke (Zhang e al., 2009). A
conside able numbe o ungi belonging o he o de Chae o hy iales
we e also de ec ed in his s udy. This o de includes ungi ha a e
known o be epiphy es, colonizing he lea es and he ba k o ees in
opical o es ecosys ems (A nold e al., 2000; Ba is a and Ci e i,
1962).
The o de Aga icales was he la ges o de o Basidiomyco a de-
ec ed in his s udy: membe s o his o de p oduce he amilia gilled
mush oom (Binde e al., 2005; Hibbe and Tho n, 2001; S ajich,
2015). Aga icales a e widesp ead in di e se ecosys ems (Ki k e al.,
2008) and many o m ec omyco hizae by engaging in mu ualis ic
symbioses wi h ascula plan s (Alexopoulos e al., 1996). Some
Aga icales a e known o be e mi e symbion s, some a e aluable as a
Fig. 3. Numbe s and p opo ional dis ibu ion o ungal ope a ional axonomic uni s (OTUs) ep esen ing all axonomic phyla and o de s ound in soil samples
collec ed om he d y A omon ane o es o Wondo Gene , E hiopia.
D. Alem, e al. Fo es Ecology and Managemen 474 (2020) 118328
6
sou ce o ood o animals, including humans (Ki k e al., 2008),
whe eas o he s ha e hallucinogenic p ope ies o p oduce oxins le hal
o humans (Nichols, 2003). Mos o he species o Aga icales de ec ed in
his s udy a e well known soil sap o ophs, such as hose belonging o
he gene a Aga icus,Cal a ia,Cop inellus,Gymnopilus,Leucoaga icus,
Lycope don,Ma asmius,Psa hy ella and Psilocybe, ha e been epo ed
p e iously as ui bodies om ou s udy a ea (Dejene e al., 2017b)
p o iding alida ion o ou molecula echniques.
4.2. Fungal ichness and di e si y changes a e fi e
Ou esul s om he pos -fi e successional ch onosequence showed
ha soil ungal ichness was ela ed o fi e. In his s udy, we ound
highe o al ichness and di e si y alues in he o es s ands ecen ly
affec ed by fi e han unbu ned s ands. This may be a ibu ed o he
new ecological condi ions c ea ed owing o diffe ences in fi e se e i y,
which may inci e o suppo spo e ge mina ion o se e al ungal species
in he soil (Heino, 2012) ollowing he fi e in he in es iga ed o es s. In
addi ion, he mycelium o ungal species in he hizosphe e may pe sis
(Cowan e al., 2016; Shen e al., 2016) o he ungal communi y may be
esilien o he effec s o fi e o some ex en (Cowan e al., 2016;
Jennings e al., 2012). Fu he mo e, he in ensi y o he fi e migh no
ha e been high enough o affec he below-g ound ungal communi ies
gi en ha low-in ensi y fi es may ha e li le effec on below-g ound
ungal communi ies (Bá cenas-Mo eno e al., 2009; Egidi e al., 2016).
Thus, he esponses o soil ungi o eoccu ing low-in ensi y fi e also
appea o be minimal (Johnson e al., 2013; Oli e e al., 2015) and
epheme al (Ha e al., 2005). Con a y o ou expec a ions, we ound
ha he amoun o ime since he fi e did no seem o affec ungal guild
Fig. 4. Mean o al ungal communi y ichness alues in a d y A omon ane
o es o Wondo Gene , E hiopia, ollowing fi e. Abb e ia ions: UB, unbu ned
s and; B1, one-yea -old bu ned s and; B10, en-yea -old bu ned s and. Ba s
deno e s anda d de ia ion. Diffe en le e s abo e he ba s indica e a significan
diffe ence in ichness be ween s and ypes (P < 0.01, n = 3 ansec s pe
s and).
Fig. 5. Mean soil ungal communi y di e si y and e enness es ima ed o unc ional guilds de ec ed in h ee ypes o o es s and wi h diffe en fi e his o ies.
Abb e ia ions: UB, unbu ned s and; B1, one-yea -old bu ned s and; B10, en-yea -old bu ned s and; Key: Shannon = Shannon di e si y alues; Simpson = Simpson
di e si y alues; E enness = e enness alues. Ba s deno e s anda d de ia ion, n = 3 ansec s pe s and.
Fig. 6. Rela i e p opo ions o ungal ope a ional axonomic uni s (OTUs) in
diffe en ecological guilds in unbu ned s ands (UB), one-yea -old bu ned s ands
(B1) and en-yea -old bu ned s ands (B10). Ba s deno e s anda d de ia ion.
D. Alem, e al. Fo es Ecology and Managemen 474 (2020) 118328
7
di e si y. These esul s ag ee wi h he findings o a me a-analysis o fi e
effec s on soil ungi (Egidi e al., 2016), which highligh ed he absence
o a significan change in ungal di e si y ollowing fi e. This migh be
because li le hea is ans e ed o he soil because uel loads a e low
(Lun and Mo gan, 2002) o migh indica e ha he ungal guild com-
muni ies in bu ned and unbu ned o es s ands sha ed simila gene
p ofiles, which may p omo e unc ional simila i ies among ungal
communi ies wi h diffe ing composi ions (Mund a, 2015). On he o he
hand, he absence o significan diffe ence in ungal ichness and di-
e si y in fi e affec ed a eas migh be due o he ac ha ecu en fi es
consume less uel and p oduce less hea , which does no pene a e in o
soil as deeply as du ing high-in ensi y fi es (Reazin e al., 2016;
Semeno a-Nelsen e al., 2019). Acco dingly, ungal communi y shi s in
such ecu en fi e ecosys ems, like ha o he d y A omon ane o es ,
may be ela i ely modes (Cho omanska and DeLuca, 2001; Ko b e al.,
2004) and he change may be d i en by indi ec fi e-induced changes in
soil p ope ies o by he change in he plan communi ies (Ha e al.,
2005; Oli e e al., 2015; Ponde e al., 2009; T appe e al., 2009). Also,
ungi in a ecu en o es ecosys em may be adap ed o equen fi es.
Some ungi p oduce hea - and smoke-ac i a ed spo es (Semeno a-
Nelsen e al., 2019) and some may benefi om pos fi e ash deposi s
(Dean e al., 2015; Ha e al., 2005) o educed compe i ion om o he
species (Semeno a-Nelsen e al., 2019). Howe e , ac o s o he han
fi e migh ha e a g ea e effec on he ichness and di e si y o soil
ungal communi ies. The e o e, u he esea ch is needed o be e
unde s and he dynamics and cha ac e is ics o soil ungal commu-
ni ies.
A p e ious s udy epo ed he absence o ec omyco hizal ungi in
he d y A omon ane o es s o E hiopia (Dejene e al., 2017a). This
finding was no excep ional as he majo i y o opical woody ee
species a e unable o o m associa ions wi h ec omyco hizal ungi
(B und e , 2009). Howe e , in his s udy, we obse ed diffe en g oups
o myco hizal ungi and hey we e iden ified and classified as ec o-
myco hizal and a buscula myco hizal (Fig. 2). This associa ion may
be due o he di e se ege a ion (F iis e al., 2010) and, hence, he e
may be mo e ees p esen ha can ac as hos s o myco hizal ungi, o
may be due o he dispe sion o myco hizal inocula om nea by
plan a ion o es s, which a e domina ed by Eucalyp us and Pinus species
(Cas año e al., 2019; Dejene e al., 2017a; U celay e al., 2017). Thus,
he findings p esen ed he e may ha e impo an implifica ions o he
indigenous o es sys em o he main enance o unc ional guild di-
e si y in E hiopia gi en ha myco hizal ungi ha e p e iously only
been epo ed om exo ic ee plan a ions (Dejene e al., 2017a).
Howe e , he impo ance o ec omyco hizae and a buscula myco -
hizae in indigenous o es sys ems in E hiopia needs empi ical da a o
confi m. In addi ion, he coexis ence o hese ungi has many p ac ical
ad an ages, such as he exchange o wa e and nu ien s h ough my-
co hizal hyphal ne wo ks (B und e , 2002, 2004). Thus, ou analysis
o he ungal communi ies in hese o es soils p esen s an insigh in o
he conse a ion o unc ional guilds in he o es sys em in he s udy
a ea.
The ege a ion changes a e a fi e may affec he soil mic obial
communi y (Ha e al., 2005). P e ious s udies ha e epo ed ha he
loss o hos plan s a e fi e dec eases myco hizal ungal di e si y
(Pa inson e al., 2006; Smi h e al., 2005). In ou s udy, bo h he
ichness and di e si y o ec omyco hizal ungi inc eased in he e-
cen ly bu ned s ands, which could indica ed an immedia e pos -fi e
myco hizal coloniza ion in fi e-affec ed o es s ands (Dahlbe g, 2002;
Rincón e al., 2015), while he sap o ophic ungi mine alize nu ien s
and s abilize he soil mois u e a e he fi e (Digh on e al., 1986). The
ec omyco hizal axa may also ha e es ablished dominance im-
media ely a e bu ning owing o hei ole ance o fi e effec s
(Dahlbe g, 2002; Kip e e al., 2010) o hey may ha e su i ed in a
mycelial s a e du ing he fi e e en (Hewi e al., 2013). Howe e , he
Fig. 7. . De ended Co espondence Analysis o dina ion plo o soil ungal
communi ies de ec ed in he h ee ea men g oups: B1, plo s in one-yea -old
bu ned s ands; B10, en-yea -old bu ned s ands; UB, unbu ned s ands. Plo s
wi h he same symbol a e in he same ea men g oup.
Table 2
Canonical co espondence analysis showing he significance (P < 0.05) o
edaphic a iables based on simple e m effec s on he myco hizal ungal spe-
cies.
Va iable Simple e m effec s
Explains % pseudo-F P
Mg 22.6 1.71 0.032
K 19.7 1.63 0.036
OM 17.0 1.40 0.047
Fig. 8. . Canonical Co espondence Analysis (CCA) o he species le el com-
muni y composi ion o ec omyco hizal ungi in a d y A omon ane o es in
E hiopia. Abb e ia ions: OM, o ganic ma e ; Mg, magnesium; K, po assium.
Species names a e abb e ia ed ( he ull names o he ec omyco hizal species
used in he o dina ion a e p o ided in supplemen a y Table S2).
D. Alem, e al. Fo es Ecology and Managemen 474 (2020) 118328
8
coloniza ion o myco hizal ungi could also be go e ned by bu n se-
e i y and by he dep h o bu ning in he soil p ofile (Hewi e al.,
2013). Thus, he effec o fi e on myco hizae could be educed when
he fi e only occu s a he soil su ace, and he effec o he fi e educes
wi h soil dep h (Danielson, 1984; Pa inson e al., 2006; Visse , 1995).
Thus, he fi e ha occu ed in ou o es s udy a ea migh no ha e been
s ong enough o affec he myco hizal ungi o may ha e only affec ed
ungi on he soil su ace. I may also be influenced by he hos plan 's
esponse o fi e. Howe e , in E hiopia he myco hizal-associa ions o
mos plan s a e no ye well known. Thus, his should be in es iga ed in
u u e s udies, including ec omyco hizal oo - ip samples, o lea n
mo e abou he di e si y o ec omyco hizal hos ee species and hei
associa ed ungi in d y A omon ane o es s.
4.3. Soil ungal communi ies and en i onmen al a iables
The DCA indica ed ha he ungal communi ies de ec ed in he
h ee s and ypes we e diffe en . The SIMPER analysis also dis-
inguished he o al dissimila i y be ween s ands and he ela i e con-
ibu ion o each ungal species o he obse ed dissimila i y. The
species making he highes con ibu ions o he dissimila i y be ween
he one- and en-yea -old bu ned s ands (10.95%) and he one-yea -old
bu ned s ands and he unbu ned s ands (10.92%) was Aga icus cam-
pes oides. This species was highly abundan (N ~ 14916) in one-yea -
old bu ned s ands bu much less abundan in en-yea -old bu ned and
unbu ned s ands (N = 2 and N = 386, espec i ely). The con ibu ion
o he species migh be pa ially esponsible o he diffe ences be ween
s ands, sugges ing ha ime a e fi e is also p obably esponsible o
he a ia ion in he dominance o some species and hei exclusi e
occu ence in ce ain s ands. This is suppo ed by p e ious findings
ha , o a gi en s and, ce ain ungal species end o be abundan and
cha ac e ize i s composi ion (Zhu e al., 2010). Thus, a species wi h a
consis en ly high con ibu ion o he dissimila i y is a good dis-
c imina ing species (Cla ke, 1993).
Soil mic oo ganisms, including ungi, a e influenced by edaphic
pa ame e s (D eno sky e al., 2004; Laube e al., 2009, 2008). Ou
edaphic da a om he d y A omon ane o es showed ha mo e ungal
species we e de ec ed in he bu ned o es a eas (B1 and B10) whe e he
soil e ili y was ela i ely low han in unbu ned a eas, which could be
ela ed o deposi ions o ash a e he fi e (Hul e al., 2015). Ash de-
posi ions could c ea e emp y niches ha p o ide oppo uni ies o he
a ea o be apidly colonized by ungal species a he ea ly s ages o
succession (F i ze e al., 1993). Howe e , he d y A omon ane o es
a ea has suffe ed e osion caused by hea y ain all soon a e he fi e
e en s. As a esul , he e is a po en ial o sedimen anspo a ion om
fi e-affec ed a eas and, hus, changes in soil e ili y le els among
s ands. Fo ins ance, pH was assumed o be inc eased in newly bu ned
a eas, owing o he p oduc ion o oxides and hyd oxides (Hul e al.,
2015). Howe e , in ou s udy o es s, we eco ded sligh ly high soil pH
alues in unbu ned o es s ands. We ound also a significan influence
o he N, C/N a ion and P on he en i e ungal communi y in his s udy.
Fo example, N and P epo ed could affec he s uc u e o ungi in he
soil, pa icula ly o he myco hizal ungi (Zhao e al., 2018). The
highe a ailabili y o hese elemen s could dec ease plan dependency
on myco hizal ungi. This condi ion could also educe he ca bon al-
loca ion o ungi (Liu e al., 2019), which could inc ease compe i ion
and affec communi y composi ion (Wang and Wang, 2008; Zhao e al.,
2018). Ou esul also confi med ha he ungal ichness is low in
s ands whe e he soil C/N a io is highe .
P e ious s udies ha e epo ed ha a e fi e, he abundance o
ec omyco hizal ungi is educed owing o he loss o hos plan s (Ha
e al., 2005). Howe e , in ou s udy, he o al ungal OTU ichness in
fi e-affec ed s ands, which had poo soil e ili y, was high compa ed
wi h ha o unbu ned s ands (Fig. 4), al hough such condi ions emain
o be in e p e ed. Howe e , Cas año e al. (2019), epo ed high le els
o ec omyco hizal ungi in s ands wi h poo soil quali y. The
occu ence o myco hizal species in poo quali y soils sugges s ha he
nu ien s ess c ea ed in he fi e-affec ed a ea could be compensa ed
o by he inc eased dependency o ees on ungal symbion s (Read and
Pe ez-Mo eno, 2003). In his ega d, he myco hizal ude al guild in
he spo e bank would play an impo an ole by quickly colonizing oo s
o plan s, and will likely aid he su i al o ees a e he fi e (Glassman
e al., 2016). Species o Wilcoxina,Tomen ella,T icholoma and Lacca ia
we e among he ec omyco hizal species ep esen ed in he fi e-affec ed
s ands, whe e soil e ili y was low. Some o hese gene a such as Lac-
ca ia a e conside ed ude al species (Ishida e al., 2007) and a e known
o o m an ec omyco hizal associa ion wi h se e al hos ee species
(Glassman e al., 2016; Hul e al., 2015).
4.4. Conclusions
This pionee s udy is he fi s a emp o desc ibe he soil ungal
communi y in a d y A omon ane o es sys em o E hiopia using nex -
gene a ion sequencing and o in es iga e he effec o fi e dis u bance
on hese ungal communi ies. Da a ob ained in his s udy will sig-
nifican ly con ibu e o he body o knowledge ega ding soil ungal
communi ies in E hiopia; howe e , he axonomy o hese ungi emains
challenging and abou 20% o he ungal species de ec ed ha e no been
desc ibed e en a he phylum le el. We conclude ha , in gene al, he
ungal di e si y in E hiopian o es sys ems is as ye la gely undesc ibed
and likely includes many axa unknown o science. Thus, we ad ise ha
addi ional scien ific in es iga ions o his highly di e se bu unexplo ed
o es ecosys em a e needed o consolida e he E hiopian ungal bio-
di e si y da abase. Also in his s udy, he soil ungal communi ies ex-
pec ed o be changed subs an ially along a pos -fi e o es succession
and in compa ison o hose in unbu ned o es . Howe e , we ound ha
fi e did no ha e a significan nega i e effec on ungal ichness and
di e si y in he bu ned s ands. Ou s udy also highligh ed ha soil
ungal composi ion diffe ed ac oss a ch onosequence a e fi e and was
co ela ed wi h soil e ili y condi ions and he changes would be ex-
plained pa ially by he edaphic condi ions. Con a y o ou expec a-
ion, oo -associa ed symbio ic ungi like ha o he myco hizal ungi
we e no lacking in fi e-affec ed s ands. We assume ha myco hizal
ungi p esen in he spo e bank we e able o colonize he oo s o plan s
ha su i ed he fi e. In he fi e-affec ed o es s, we also ound ungi
ha a e known o o m ec omyco hizal associa ions wi h se e al hos
ee species. This key ecological ole could p o ide suppo o he
impo ance o ungal conse a ion in he d y A omon ane o es sys-
ems in E hiopia. Simila ly, i al edaphic a iables such as OM and K
also appea o be impo an in shaping he composi ion o myco hizal
soil ungi in diffe en ways. Thus, he effec o o es managemen
p ac ices such as hinning and ha es ing on soil e ili y should be
aken in o conside a ion owing o he impo an ela ionship be ween
hese ecological pa ame e s and he soil ungal composi ion in he d y
A omon ane o es s o E hiopia.
CRediT au ho ship con ibu ion s a emen
Demelash Alem: Fo mal analysis, W i ing - e iew & edi ing. Ta ek
Dejene: Me hodology, W i ing - e iew & edi ing. Juan And és O ia-
de-Rueda: Supe ision. Józse Geml: Fo mal analysis, W i ing - e iew
& edi ing. Ca les Cas año: W i ing - e iew & edi ing. Jane E. Smi h:
W i ing - e iew & edi ing. Pablo Ma ín-Pin o: Concep ualiza ion,
Me hodology, Supe ision, W i ing - e iew & edi ing.
Decla a ion o Compe ing In e es
The au ho s decla e ha hey ha e no known compe ing financial
in e es s o pe sonal ela ionships ha could ha e appea ed o influ-
ence he wo k epo ed in his pape .
D. Alem, e al. Fo es Ecology and Managemen 474 (2020) 118328
9
Acknowledgemen s
This p ojec was pa ially suppo ed by he E asmus Mundus-D eam
p ojec g an and by he p ojec SUSTIFUNGI_ET unded by he Spanish
Agency o In e na ional De elopmen and Coope a ion. This wo k was
also co- unded by he Spanish Minis y o Educa ion and Cul u e unde
a Sal ado de Mada iaga g an ag eemen , n° PRX17/00315. Men ion
o ade o fi m names does no cons i u e an endo semen by he U.S.
Depa men o Ag icul u e.
Appendix A. Supplemen a y ma e ial
Supplemen a y da a o his a icle can be ound online a h ps://
doi.o g/10.1016/j. o eco.2020.118328.
Re e ences
Alexopoulos, C., Mims, C., Blackwell, M., 1996. In oduc o y Mycology. John Wiley &
Sons, New Yo k.
Ande son, M.J., 2001. A new me hod o non pa ame ic mul i a ia e analysis o a -
iance. Aus al Ecol. 26, 32–46. h ps://doi.o g/10.1111/j.1442-9993.2001.01070.
pp. x.
Ango, T.G., Bewke , W., 2007. Challenges and p ospec s o sus ainable o es manage-
men in Wondo Gene a ea, Sou he n E hiopia. E hiop. J. De . Res. 29, 27–64.
h ps://doi.o g/10.4314/ejd . 29i2.42709.
A aujo, J.P.M., Hughes, D.P., 2016. Di e si y o en omopa hogen ungi: Which g oups
conque ed he insec body? Ad . Gene . 94, 1–39. h ps://doi.o g/10.1016/bs.adgen.
2016.01.001.
A nold, A.E., Mayna d, Z., Gilbe , G.S., Coley, P.D., Ku sa , T.A., 2000. A e opical
ungal endophy es hype di e se? Ecol. Le . 3, 267–274.
Bá cenas-Mo eno, G., a ex backslasha a h, E., Båå h, E., 2009. Bac e ial and ungal
g ow h in soil hea ed a diffe en empe a u es o simula e a ange o fi e in ensi ies.
Soil Biol. Biochem. 41, 2517–2526. h ps://doi.o g/10.1016/j.soilbio.2009.09.010.
Bas ias, B.A., Huang, Z.Q., Blumfield, T., Xu, Z., Cai ney, J.W.G., 2006. Influence o e-
pea ed p esc ibed bu ning on he soil ungal communi y in an eas e n Aus alian we
scle ophyll o es . Soil Biol. Biochem. 38, 3492–3501. h ps://doi.o g/10.1016/j.
soilbio.2006.06.007.
Ba is a, A., Ci e i, R., 1962. The Chae o hy iales. Sydowia 3, 1–129.
Bekele, T., Kassa, K., Mengis u, T., Debele, M., Melka, Y., 2013. Wo king wi h commu-
ni ies o add ess de o es a ion in he Wondo Gene ca chmen A ea, E hiopia : lessons
lea n om a pa icipa o y ac ion esea ch. Res. J. Ag ic. En i on. Manag. 2,
448–456.
Belay, T., 2016. Clima e-g ow h ela ionship o Pinus pa ula Schldl. e Cham. in Wondo
Gene , Sou h Cen al E hiopia. J. Clima ol. Wea he Fo ecas . 04, 1–8. h ps://doi.
o g/10.4172/2332-2594.1000181.
Belaynesh, Z., 2002. Pe cep ions o o es Resou ce changes in and a ound Wondo Gene
Ca chmen and i s nea u u e impac s. MSc Thesis. Wondo Gene College o Fo es y,
Wondo Gene , E hiopia.
Binde , M., Hibbe , D.S., La sson, K.H., La sson, E., Lange , E., Lange , G., 2005. The
phylogene ic dis ibu ion o esupina e o ms ac oss he majo clades o mush oom-
o ming ungi (Homobasidiomyce es). Sys . Biodi e s. 3, 113–157.
Bone , J.A., Palahí, M., Colinas, C., Pukkala, T., Fische , C.R., Miina, J., Ma ínez de
A agón, J., 2010. Modelling he p oduc ion and species ichness o wild mush ooms
in pine o es s o he Cen al Py enees in no heas e n Spain. Can. J. Fo . Res. 40,
347–356. h ps://doi.o g/10.1139/X09-198.
Bonge s, F., Tenngkei , T., 2010. Deg aded o es s in Eas e n A ica: In oduc ion. In:
Bonge s, F., Tenningkei , T. (Eds.), Deg aded Fo es s in Eas A ica: Managemen and
Res o a ion. Ea hscan L d., London, UK, pp. 1–18.
Bouyoucos, G.H., 1951. A eclama ion o he hyd ome e o making mechanical analy.
Soil. Ag o. J. 43, 434–438.
B idge, P., Spoone , B., 2011. Soil ungi: di e si y and de ec ion. Plan Soil 232, 147–154.
B und e , M., 2002. Coe olu ion o oo s and myco hiza o land plan s. New Phy ol
275–304.
B und e , M., 2004. Di e si y and classifica ion o myco hizal associa ions. Biol. Re .
79, 473–495.
B und e , M.C., 2009. Myco hizal associa ions and o he means o nu i ion o ascula
plan s: Unde s anding he global di e si y o hos plan s by esol ing conflic ing
in o ma ion and de eloping eliable means o diagnosis. Plan Soil 320, 37–77.
h ps://doi.o g/10.1007/s11104-008-9877-9.
Busca do, E., Rod íguez-Eche e ía, S., Ba ico, L., Ga cía, M.Á., F ei as, H., Ma ín, M.P.,
De Angelis, P., Mulle , L.A.H., 2012. Is he po en ial o he o ma ion o common
myco hizal ne wo ks influenced byfi e equency? Soil Biol. Biochem. 46, 136–144.
h ps://doi.o g/10.1016/j.soilbio.2011.12.007.
Busca do, E., Rod íguez-Eche e ía, S., Ma ín, M.P., De Angelis, P., Pe ei a, J.S., F ei as,
H., 2010. Impac o wildfi e e u n in e al on he ec omyco hizal esis an p opa-
gules communi ies o a Medi e anean open o es . Fungal Biol. 114, 628–636.
h ps://doi.o g/10.1016/j. unbio.2010.05.004.
Cai ney, J.W.G., Bas ias, B.A., 2007. Influences o fi e on o es soil ungal communi ies.
Can. J. Fo . Res. 37, 207–215. h ps://doi.o g/10.1139/x06-190.
Ca u he s, R., Hu al, K., 1990. Fungi as na u ally occu ing en omopa hogens. New
di ec ions in biological con ol: Al e na i es o supp essing ag icul u al pes s and
diseases. Alan R. Liss.
Cas año, C., Dejene, T., Media illa, O., Geml, J., And es, J., O ia-de-Rueda, Ma ín-Pin o,
P., 2019. Changes in ungal di e si y and composi ion along a ch onosequence o
Eucalyp us g andis plan a ions in E hiopia. Fungal Ecol. 39, 328–335. h ps://doi.
o g/10.1016/j. uneco.2019.02.003.
Cha e i, P., Samuels, G., 2003. Hypoc ea/T ichode ma: Species wi h g een ascospo es.
S ud. Mycol. 48, 1–116.
Cho omanska, U., DeLuca, T.H., 2001. P esc ibed fi e al e s he impac o wildfi e on soil
biochemical p ope ies in a ponde osa pine o es . Soil Sci. Soc. Am. J. 65, 232–238.
h ps://doi.o g/10.2136/sssaj2001.651232x.
Cla idge, A.W., T appe, J.M., Mills, D.J., Cla idge, D.L., 2009. Di e si y and habi a e-
la ionships o hypogeous ungi. III. Fac o s influencing he occu ence o fi e-adap ed
species. Mycol. Res. 113, 792–801. h ps://doi.o g/10.1016/j.myc es.2009.02.014.
Cla ke, K.R., 1993. Non-pa ame ic mul i a ia e analyses o changes in communi y
s uc u e. Aus al Ecol. 18, 117–143. h ps://doi.o g/10.1111/j.1442-9993.1993.
b00438.x.
Cowan, A.D., Smi h, J.E., Fi zge ald, S.A., 2016. Reco e ing los g ound: Effec s o soil
bu n in ensi y on nu ien s and ec omyco hiza communi ies o ponde osa pine
seedlings. Fo . Ecol. Manage. 378, 160–172. h ps://doi.o g/10.1016/j. o eco.2016.
07.030.
C ab ee, C.D., Kelle , H.W., Ely, J.S., 2010. Mac o ungi associa ed wi h ege a ion and
soils a Ha Ha Tonka S a e Pa k, Missou i. Mycologia 102, 1229–1239. h ps://doi.
o g/10.3852/08-138.
Dahlbe g, A., 2002. Effec s o fi e on ec omyco hizal ungi in ennoscandian bo eal
o es s. Sil a Fenn. 36, 69–80. h ps://doi.o g/10.14214/s .551.
Dahlbe g, A., Schimmel, J., Taylo , A.F.S., Johannesson, H., 2001. Pos -fi e legacy o
ec omyco hizal ungal communi ies in he Swedish bo eal o es in ela ion o fi e
se e i y and logging in ensi y. Biol. Conse . 100, 151–161. h ps://doi.o g/10.
1016/S0006-3207(00)00230-5.
Danielson, R.M., 1984. Ec omyco hizal associa ions in jack pine s ands in no heas e n
Albe a. Can. J. Bo . 62, 932–939.
De la Va ga, H., Águeda, B., Ma ínez-Peña, F., Pa ladé, J., Pe a, J., 2012. Quan ifica ion
o ex a adical soil mycelium and ec omyco hizas o Bole us edulis in a Sco s pine
o es wi h a iable spo oca p p oduc i i y. Myco hiza 22.
Dean, S., Fa e , E.C., Menges, E.S., 2015. Fi e effec s on soil biogeochemis y in Flo ida
sc ubby fla woods. Am. Midl. Na . 174, 49–64. h ps://doi.o g/10.1674/0003-0031-
174.1.49.
Dejene, T., O ia-de- ueda, J.A., Ma ín-Pin o, P., 2017a. Fungal di e si y and succession
ollowing s and de elopmen in Pinus pa ula Schiede ex Schl dl. & Cham. plan a ions
in E hiopia. Fo . Ecol. Manage. 395, 9–18. h ps://doi.o g/10.1016/j. o eco.2017.03.
032.
Dejene, T., O ia-de-Rueda, J.A., Ma ín-Pin o, P., 2017b. Fungal communi y succession
and spo oca p p oduc ion ollowing fi e occu ence in D y A omon ane o es s o
E hiopia. Fo . Ecol. Manage. 398, 37–47. h ps://doi.o g/10.1016/j. o eco.2017.05.
011.
Dh uba, S., Kuldip, G., Jaysh ee, D., A.K., S., 2015. Fungal di e si y o wel e majo
ege a ional zones o A unachal Hi-malaya, India. J. Fo . Res. 26, 579–586.
Digh on, J., Poski , J.M., Howa d, D.M., 1986. Changes in occu ence o Basidiomyce e
ui bodies du ing o es s and de elopmen : wi h specific e e ence o myco hizal
species. T ans. B . Mycol. Soc. 87, 163–171. h ps://doi.o g/10.1016/S0007-
1536(86)80017-1.
D eno sky, R., Vo, D., G aham, K., Scow, K., 2004. Soil wa e con en and o ganic ca bon
a ailabili y a e majo de e minan s o soil mic obial communi y composi ion.
Mic ob. Ecol. 48, 424–430.
Edga , R.C., 2010. Sea ch and clus e ing o de s o magni ude as e han BLAST.
Bioin o ma ics 26, 2460–2461.
Egidi, E., McMullan-Fishe , S., Mo gan, J.W., May, T., Zeeman, B., F anks, A.E., 2016. Fi e
egime, no ime-since-fi e, affec s soil ungal communi y di e si y and composi ion
in empe a e g asslands. FEMS Mic obiol. Le . 363, 1–11. h ps://doi.o g/10.1093/
emsle/ nw196.
E iksson, H., S e n, M., 1987. A soil s udy a Wondo Gene Fo es y esou ces Ins i u e,
E hiopia (No. 48). Uppsala.
Eshe u, Z., Högbe g, P., 2000. Recons uc ion o o es si e his o y in E hiopian highlands
based on 13 C na u al abundance o soils. R. Swedish Acad. Sci. 29, 83–89.
Esse , R., El-Gholl, E., 1993. Paecilomyces lilacinus, a ungus ha pa asi izes nema ode
eggs. Flo ida Dep . o Ag icul u e, Di ision o Plan Indus y, Nema ology Ci cula
203.
Fen a, M.M., 2014. Human-wildli e conflic s: case s udy in Wondo Gene dis ic ,
Sou he n E hiopia. Ag ic. Fo . Fish. 3, 352–362. h ps://doi.o g/10.1016/j.jneume h.
2014.08.006.
Fie e , N., Jackson, R., 2006. The di e si y and biogeog aphy o soil bac e ial commu-
ni ies. PNAS 625–631.
Fon aine, S., Ba o , S., Ba e, P., Bdioui, N., Ma y, B., Rumpel, C., 2007. S abili y o o -
ganic ca bon in deep soil laye s con olled by esh ca bon supply. Na u e 450,
277–280.
F iis, B., Demissew, S., B eugel, P., 2010. A las o he po en ial ege a ion o E hiopia.
Roy. Danish Acad. Sci. Le .
F i ze, H., Pennanen, T., Pie ikäinen, J., 1993. Reco e y o soil mic obial biomass and
ac i i y om p esc ibed bu ning. Can. J. Fo . Res. 23, 1286–1290. h ps://doi.o g/
10.1139/x93-164.
Geml, J., Pas o , N., Fe nandez, L., Pacheco, S., Semeno a, T.A., Bece a, A.G.,
Wicaksono, C.Y., Nouh a, E.R., 2014. La ge-scale ungal di e si y assessmen in he
Andean Yungas o es s e eals s ong communi y u no e among o es ypes along
an al i udinal g adien . Mol. Ecol. 23, 2452–2472. h ps://doi.o g/10.1111/mec.
12765.
D. Alem, e al. Fo es Ecology and Managemen 474 (2020) 118328
10
Glassman, S.I., Le ine, C.R., Di occo, A.M., Ba les, J.J., B uns, T.D., 2016.
Ec omyco hizal ungal spo e bank eco e y a e a se e e o es fi e: Some like i ho .
ISME J. 10, 1228–1239. h ps://doi.o g/10.1038/ismej.2015.182.
Guo, H., Wang, W., Wu, X., Luo, X., 2013. Mic obial communi y composi ion o la osols
unde a ubbe plan a ion. In: Xu, J., Wu, J., He, Y. (Eds.), Func ions o Na u al
O ganic Ma e in Changing En i onmen . Sp inge , Ne he lands, pp. 859–862.
Ha , S.C., DeLuca, T.H., Newman, G.S., MacKenzie, M.D., Boyle, S.I., 2005. Pos -fi e
ege a i e dynamics as d i e s o mic obial communi y s uc u e and unc ion in
o es soils. Fo . Ecol. Manage. 220, 166–184. h ps://doi.o g/10.1016/j. o eco.
2005.08.012.
Heino, L., 2012. Fungi and fi e. Aus alian Na ional Bo anic Ga dens and Aus alian
Na ional He ba ium, Canbe a.
He nández-Rod íguez, M., O ia-de-Rueda, J.A., Ma ín-Pin o, P., 2013. Pos -fi e ungal
succession in a Medi e anean ecosys em domina ed by Cis us ladani e L. Fo . Ecol.
Manage. 289, 48–57. h ps://doi.o g/10.1016/j. o eco.2012.10.009.
Hewi , R.E., Ben , E., Hollingswo h, T.N., Chapin, F.S., Taylo , D.L., 2013. Resilience o
A c ic myco hizal ungal communi ies a e wildfi e acili a ed by esp ou ing
sh ubs. Écoscience 20, 296–310. h ps://doi.o g/10.2980/20-3-3620.
Hibbe , D.S., Tho n, R.G., 2001. Homobasidiomyce es. In: Mclaughlin, D.J., McLaughlin,
E.G., Lemke, P.A. (Eds.), The Myco a VII. Sys ema ics and E olu ion. Pa B. Sp inge -
Ve lag, Be lin.
Hobbie, E.A., Macko, S.A., Shuga , H.H., 1999. Insigh s in o ni ogen and ca bon dy-
namics o ec omyco hizal and sap o ophic ungi om iso opic e idence. Oecologia
353–360.
Hul, S., Minna, S., Jukka, P., Kaja , K., F ank, B., Tommaso, R., A i, J., F ed, O.A., Jussi,
H., 2015. Fungal communi y shi s in s uc u e and unc ion ac oss a bo eal o es fi e
ch onosequence. Appl. En i on. Mic obiol. 81, 7869–7880. h ps://doi.o g/10.1128/
AEM.02063-15.Edi o .
Ih ma k, K., Bödeke , I., C uz-Ma inez, K., 2012. New p ime s o ampli y he ungal ITS2
egion –e alua ion by 454-sequencing o a ificial and na u al communi ies. FEMS
Mic obiol. Ecol. 82, 666–677.
Ishida, T.A., Na a, K., Hoge su, T., 2007. Hos effec s on ec omyco hizal ungal com-
muni ies: Insigh om eigh hos species in mixed coni e -b oadlea o es s. New
Phy ol. 174, 430–440. h ps://doi.o g/10.1111/j.1469-8137.2007.02016.x.
Jennings, T.N., Smi h, J.E., C omack, K., Sulzman, E.W., McKay, D., Caldwell, B.A.,
Beldin, S.I., 2012. Impac o pos fi e logging on soil bac e ial and ungal communi ies
and soil biogeochemis y in a mixed-coni e o es in cen al O egon. Plan Soil 350,
393–411.
Johnson, K.B., Jacob, A., B own, M.E., 2013. Fo es co e associa ed wi h imp o ed child
Heal h and nu i ion: E idence om he Malawi Demog aphic and Heal h Su ey and
sa elli e da a. Glob. Heal. Sci. P ac . 1, 237–248. h ps://doi.o g/10.9745/GHSP-D-
13-00055.
Kennedy, A., Gewin, V., 1997. Soil mic obial di e si y: p esen and u u e conside a ions.
Soil Sci. 162, 607–617.
Ken , M., Coke , P., 1993. Vege a ion Desc ip ion and Analysis : A P ac ical App oach.
Belha en P ess, London.
Kidanu, S., 2004. Using Eucalyp us o soil and Wa e Conse a ion on he Highland
Ve isols o E hiopia. Wageningen Uni e si y and Resea ch Cen e .
Kim, H.T., 1996. Soil sampling, p epa a ion and analysis 139–145.
Kip e , T., Egli, S., Ghazoul, J., Mose , B., Wohlgemu h, T., 2010. Suscep ibili y o ec o-
myco hizal ungi o soil hea ing. Fungal Biol. 114, 467–472. h ps://doi.o g/10.
1016/j. unbio.2010.03.008.
Ki k, P., Cannon, P., Min e , D., S alpe s, J., 2008. Dic iona y o he Fungi, 10 h ed.
Walling o d, UK.
Kõljalg, U., Nilsson, R.H., Aba enko , K., Tede soo, L., Taylo , A.F.S., Bah am, M., 2013.
Towa ds a unified pa adigm o sequence-based iden ifica ion o ungi. Mol. Ecol. 22,
5271–5277.
Ko b, J.E., Johnson, N.C., Co ing on, W.W., 2004. Slash pile bu ning effec s on soil bio ic
and chemical p ope ies and plan es ablishmen : Recommenda ions o amelio a-
ion. Res o . Ecol. 12, 52–62. h ps://doi.o g/10.1111/j.1061-2971.2004.00304.x.
K ashe ska, V., Kla ne , B., Widyas u i, R., Ma aun, M., Scheu, S., 2015. Impac o o-
pical lowland ain o es con e sion in o ubbe and oil palm plan a ions on soil
mic obial communi ies. Biol. Fe il. Soils 51, 697–705.
K uys, Å., E iksson, O., Wedin, M., 2006. Phylogene ic ela ionships o cop ophilous
Pleospo ales (Do hideomyce es, Ascomyco a), and he classifica ion o some bi uni-
ca e axa o unknown posi ion. Mycol. Res. 110, 527–536.
Laube , C., Hamady, M., Knigh, T.R., Fie e , N., 2009. Py osequencing based assessmen
o soil pH as a p edic o o soil bac e ial communi y s uc u e a he con inen al scale.
Appl. En i on. Mic obiol. 75, 5111–5120.
Laube , C.L., S ickland, M.S., B ad o d, M.A., Fie e , N., 2008. The influence o soil
p ope ies on he s uc u e o bac e ial and ungal communi ies ac oss land-use ypes.
Soil Biol. Biochem. 40, 2407–2415. h ps://doi.o g/10.1016/j.soilbio.2008.05.021.
Lemenih, M., Bekele, M., 2008. Pa icipa o y Fo es Managemen Bes P ac ices , Lesson
Lea n and Pa icipa o y Fo es Managemen Bes P ac ices , Lesson Lea n , FAO.
Liu, M., Sui, X., Hu, Y., Feng, F., 2019. Mic obial communi y s uc u e and he e-
la ionship wi h soil ca bon and ni ogen in an o iginal Ko ean pine o es o Changbai
Moun ain. China. BMC Mic obiol. 19, 218. h ps://doi.o g/10.1186/s12866-019-
1584-6.
Lun , I., Mo gan, J., 2002. The Role o fi e egimes in empe a e lowland g asslands o
sou h-eas e n Aus alia. In: Flammable Aus alia: The Fi e Regimes and Biodi e si y
o a Con inen . Camb idge Uni e si y P ess, Camb idge, UK, pp. 177–196.
Luoma, D.L., F enkel, R.E., T appe, J.M., 1991. F ui ing o hypogeous ungi in O egon
Douglas-Fi o es s: seasonal and habi a a ia ion. Mycologia 83, 335–353. h ps://
doi.o g/10.2307/3759994.
Magu an, A.E., 1988. Ecological Di e si y and i s Measu emen . P ince on Uni e si y
P ess, New Je sey.
McCann, J., 1995. People o he Plow: An Ag icul u al His o y o E hiopia, 1800–1900.
Uni e si y o Wisconsis P ess, Madison, USA.
McCune, B., G ace, J.B., 2002. Analysis o Ecological Communi ies. MjM So wa e,
Gleneden Beach, OR, USA.
Mund a, S., 2015. Richness and communi y s uc u e o high A c ic ungi h ough space
and ime explo ed using high- h oughpu sequencing. The Uni e si y Cen e in
S alba d.
Na ayanasamy, P., 2011. De ec ion o ungal pa hogens in plan s. In: Na ayanasamy, P.
(Ed.), Mic obial Plan Pa hogens- De ec ion and Disease Diagnosis, Fungal Pa hogens,
1. Sp inge , Ne he lands, pp. 5–199.
Nea y, G., Klopa ek, C., DeBano, L., F ollio , P., 1999. Fi e effec s on belowg ound sus-
aibabli y: a e iew and syn hesis. Fo . Ecol. Manage. 122, 51–71.
Nehls, U., 2008. Mas e ing ec omyco hizal symbiosis: he impac o ca bohyd a es. J.
Ecpe imen al Bo . 59, 1097–1108.
New Business E hiopia, 2019. Wildfi e bu ns E hiopia’s UNESCO egis e ed pa k [WWW
Documen ].
Nichols, D., 2003. Hallucinogens. Pha macol. The . 101, 135.
O’B ien, H.E., Pa en , J.L., Jackson, J.A., Moncal o, J., Vilgalys, R., 2005. Fungal
Communi y Analysis by La ge-Scale Sequencing o En i onmen al Samples. Appl.
En i on. Mic obiol. 71, 5544–5550. h ps://doi.o g/10.1128/AEM.71.9.5544.
Oli e , A.K., Callaham, M.A., Jumpponen, A., 2015. Soil ungal communi ies espond
composi ionally o ecu ing equen p esc ibed bu ning in a managed sou heas e n
US o es ecosys em. Fo . Ecol. Manage. 345, 1–9. h ps://doi.o g/10.1016/j. o eco.
2015.02.020.
Olsen, S.R., Somme , L.E., 1982. Phospho us. Me hods o soil analysis. In: Page, A.L.,
Mille , R.H., Keeney, D.R. (Eds.), Ag onomy Vol. 9, Pa II. Am. Soc. Ag on, Soil Sci.
Soc. Am. J., Madison. WI. pp. 403–430.
Pa a icini, V., Micheli, F., Mon e alcone, M., Villa, E., Mo i, C., Bianchi, C.N., 2010.
Rapid assessmen o epiben hic communi ies: A compa ison be ween wo isual
sampling echniques. J. Exp. Ma . Bio. Ecol. 395, 21–29. h ps://doi.o g/10.1016/j.
jembe.2010.08.005.
Pa inson, G.S., Hammil, K.A., Su on, B.G., McCGEE, P., 2006. Simula ed fi e educes he
densi y o a buscula myco hizal ungi a he soil su ace. Mycol. Res. 103, 491–496.
Ponde , F., Tad os, M., Loewens ein, E.F., 2009. Mic obial p ope ies and li e and soil
nu ien s a e wo p esc ibed fi es in de eloping sa annas in an upland Missou i
Oza k Fo es . Fo . Ecol. Manage. 257, 755–763. h ps://doi.o g/10.1016/j. o eco.
2008.10.009.
R Co e Team, 2019. R: A language and en i onmen o s a is ical compu ing. R
Founda ion o S a is ical Compu ing, Vienna, Aus ia.
Read, D., Pe ez-Mo eno, J., 2003. Myco hizas and nu ien cycling in ecosys ems –a
jou ney owa ds ele ance? New Phy ol. 157, 475–492.
Reazin, C., Mo is, S., Smi h, J.E., Cowan, A.D., Jumpponen, A., 2016. Fi es o diffe ing
in ensi ies apidly selec dis inc soil ungal communi ies in a No hwes US pon-
de osa pine o es ecosys em. Fo . Ecol. Manage. 377, 118–127. h ps://doi.o g/10.
1016/j. o eco.2016.07.002.
Reeuwijk, L., 2002. P ocedu es o Soil Analysis, 6 h ed. In e na ional Soil Re e ence and
In o ma ion Cen e, Wageningen, The Ne he lands.
Rincón, A., Pueyo, J.J., 2010. Effec o fi e se e i y and si e slope on di e si y and
s uc u e o he ec omyco hizal ungal communi y associa ed wi h pos -fi e e-
gene a ed Pinus pinas e Ai . seedlings. Fo . Ecol. Manage. 260, 361–369. h ps://
doi.o g/10.1016/j. o eco.2010.04.028.
Rincón, A., San ama ía-Pé ez, B., Rabasa, S.G., Coince, A., Ma çais, B., Buée, M., 2015.
Compa men alized and con as ed esponse o ec omyco hizal and soil ungal
communi ies o Sco s pine o es s along ele a ion g adien s in F ance and Spain.
En i on. Mic obiol. 17, 3009–3024. h ps://doi.o g/10.1111/1462-2920.12894.
Rossman, A., Samuels, G., Roge son, C., Lowen, R., 1999. Gene a o bionec iaceae, hy-
poc eaceae and nec iaceae (hypoc eales, ascomyce es). S ud. Mycol. 42, 1–248.
Ruibal, C., Gueidan, C., Selbmann, L., Go bushina, A., C ous, P., G oenewald, J., Muggia,
L., G ube, M., Isola, D., Schoch, C., S aley, J., Lu zoni, F., Hoog, G.D., 2009.
Phylogeny o ock-inhabi ing ungi ela ed o Do hideomyce es. S ud. Mycol. 64,
123–133.
Samuels, G., 1996. T ichode ma: A e iew o biology and sys ema ics o he genus. Mycol.
Res. 923–935.
Sch oe s, H., 2001. A monog aph o bionec ia (ascomyco a, hypoc eales, bionec iaceae)
and i s clonos achys anamo phs. S ud. Mycol. 46, 1–214.
Semeno a-Nelsen, T.A., Pla , W.J., Pa e son, T.R., Huffman, J., Sikes, B.A., 2019.
F equen fi e eo ganizes ungal communi ies and slows decomposi ion ac oss a
he e ogeneous pine sa anna landscape. New Phy ol. 224, 916–927. h ps://doi.o g/
10.1111/nph.16096.
Senbe a, F., Teke ay, D., 2001. Regene a ion o indigenous woody species unde he ca-
nopies o ee plan a ions in cen al E hiopia. T op. Ecol. 42, 175–185.
Shannon, C., Wea e , W., 1949. The ma hema ical heo y o communica ion. Uni e si y
o Illinois P ess, U bana. h ps://doi.o g/10.1145/584091.584093.
Shen, J., Chen, C.R., Lewis, T., 2016. Long e m epea ed fi e dis u bance al e s soil
bac e ial di e si y bu no he abundance in an Aus alian we scle ophyll o es . Sci.
Rep. 6, 19639. h ps://doi.o g/10.1038/s ep19639.
Smilaue , P., Lepš, J., 2014. Mul i a ia e Analysis o Ecological Da a using CANOCO 5.
Camb idge Uni e si y P ess, Camb idge. h ps://doi.o g/10.1017/
CBO9781139627061.
Smi h, J.E., Klube , L.A., Jennings, T.N., McKay, D., B enne , G., Sulzman, E.W., 2017.
Does he p esence o la ge down wood a he ime o a o es fi e impac soil e-
co e y? Fo . Ecol. Manage. 391, 52–62. h ps://doi.o g/10.1016/j. o eco.2017.02.
013.
Smi h, J.E., Mckay, D., B enne , G., Mci e , J., Spa a o a, J.W., 2005. Ea ly impac s o
o es es o a ion ea men s on he ec omyco hizal ungal communi y and fine oo
biomass in a mixed coni e o es . J. Appl. Ecol. 42, 526–535. h ps://doi.o g/10.
D. Alem, e al. Fo es Ecology and Managemen 474 (2020) 118328
11
1111/j.1365-2664.2005.01047.x.
Smi h, J.E., Molina, R., Huso, M.M., Luoma, D.L., McKay, D., Cas ellano, M.A., Lebel, T.,
Valacho ic, Y., 2002. Species ichness, abundance, and composi ion o hypogeous
and epigeous ec omyco hizal ungal spo oca ps in young, o a ion-age, and old-
g ow h s ands o Douglas-fi (Pseudo suga menziesii) in he Cascade Range o
O egon. U.S.A Can. J. Bo . 80, 186–204. h ps://doi.o g/10.1139/b02-003.
S ajich, J.E., 2015. Phylogenomics enabling genome-based mycology, The Myco a: A
Comp ehensi e T ea ise on Fungi As Expe imen al Sys ems o Basic and Applied
Resea ch: VII Sys ema ics and E olu ion Pa B 2nd ed. h ps://doi.o g/10.1007/978-
3-662-46011-5_11.
Taudiè e, A., Richa d, F., Ca caille , C., 2017. Re iew on fi e effec s on ec omyco hizal
symbiosis, an unachie ed wo k o a scalding opic. Fo . Ecol. Manage. 391, 446–457.
h ps://doi.o g/10.1016/j. o eco.2017.02.043.
Taylo , A.F.S., 2002. Fungal di e si y in ec omyco hizal communi ies. Plan Soil 19–28.
Taylo , D.L., Hollingswo h, T.N., McFa land, J.W., Lennon, N.J., Nusbaum, C., Ruess,
R.W., 2014. A fi s comp ehensi e census o ungi in soil e eals bo h hype di e si y
and fine-scale niche pa i ioning. Ecol. Monog . 84, 3–20. h ps://doi.o g/10.1890/
12-1693.1.
Tede soo, L., Bah am, M., Polme, S., Koljalg, U., Yo ou, N.S., Wijesunde a, R., Ruiz, L. V.,
Vasco-Palacios, A.M., Thu, P.Q., Suija, A., Smi h, M.E., Sha p, C., Salu ee , E., Sai a,
A., Rosas, M., Rii , T., Ra kowsky, D., P i sch, K., Poldmaa, K., Piepenb ing, M.,
Phos i, C., Pe e son, M., Pa s, K., Pa el, K., O sing, E., Nouh a, E., Njouonkou, A.L.,
Nilsson, R.H., Mo gado, L.N., Mayo , J., May, T.W., Majuakim, L., Lodge, D.J., Lee, S.
S., La sson, K.-H., Kohou , P., Hosaka, K., Hiiesalu, I., Henkel, T.W., Ha end, H., Guo,
L. -d., G eslebin, A., G ele , G., Geml, J., Ga es, G., Duns an, W., Dunk, C., D enkhan,
R., Dea naley, J., De Kesel, A., Dang, T., Chen, X., Buegge , F., B ea ley, F.Q., Boni o,
G., Anslan, S., Abell, S., Aba enko , K., 2014. Global di e si y and geog aphy o soil
ungi. Science (80-.). 346, 1256688–1256688. h ps://doi.o g/10.1126/science.
1256688.
T appe, M.J., C omack, K., T appe, J.M., Pe akis, D.D.B., Caza es-Gonzales, E.,
Cas ellano, M.A., Mille , S.L., 2009. In e ac ions among p esc ibed fi e, soil a i-
bu es, and myco hizal communi y s uc u e a C a e Lake Na ional Pa k, O egon,
USA. Fi e Ecol. 5, 30–50. h ps://doi.o g/10.4996/fi eecology.0502030.
U celay, C., Longo, S., Geml, J., Tecco, P.A., Nouh a, E., 2017. Co-in asi e exo ic pines
and hei ec omyco hizal symbion s show capabili ies o wide dis ance and al i u-
dinal ange expansion. Fungal Ecol. 25, 50–58. h ps://doi.o g/10.1016/j. uneco.
2016.11.002.
Van De Heijden, M.G.A., Ba dge , R.D., Van S aalen, N.M., 2008. The unseen majo i y:
Soil mic obes as d i e s o plan di e si y and p oduc i i y in e es ial ecosys ems.
Ecol. Le . 11, 296–310. h ps://doi.o g/10.1111/j.1461-0248.2007.01139.x.
Visse , S., 1995. Ec omyco hizal ungal succession in Jack Pine s ands ollowing wildfi e.
New phy ol 129, 389–401.
Voříško á, J., B abco á, V., Caj haml, T., Bald ian, P., 2014. Seasonal dynamics o ungal
communi ies in a empe a e oak o es soil. New Phy ol. 201, 269–278.
Walkley, A., Black, I.A., 1934. An examina ion o he diges ion me hod o de e mining
soil o ganic ma e and a p oposed modifica ion o he ch omic acid i a ion me hod.
Soil Sci. 34, 29–38.
Wang, Q.-K., Wang, S.-L., 2008. Soil mic obial p ope ies and nu ien s in pu e and mixed
Chinese fi plan a ions. J. Fo . Res. 19, 131–135. h ps://doi.o g/10.1007/s11676-
008-0022-7.
Wassie, A., Teke ay, D., Powell, N., 2005. Chu ch o es s in No h Gonde adminis a i e
zone, No he n E hiopia. Fo . T ees Li elihoods 15, 349–373. h ps://doi.o g/10.
1080/14728028.2005.9752536.
Whi e, T., Bu ns, T., Lee, S., Taylo , J., 1990. Amplica ion and di ec sequencing o ungal
ibosomal RNA genes o phylogene ics. In: Ma, I., Gel and, D., Sninsky, J., Whi e,
T.J. (Eds.), PCR P o ocols: A Guide o Me hods and Applica ions. Academic P ess,
New Yo k, pp. 315–322.
Wube , T., Ko ke, I., Teke ay, D., Obe winkle , F., 2003. Myco hizal s a us o indigenous
ees in d y A omon ane o es s o E hiopia. Fo . Ecol. Manage. 179, 387–399.
h ps://doi.o g/10.1016/S0378-1127(02)00546-7.
Ze ga, B., Be a, A., 2016. P e e ence, pu pose, and pa e n o Eucalyp us ee a ming in
Eza We eda, E hiopia. J. Soc. Sci. Humani . Res. 3, 2394–11375.
Zhang, Y., Schoch, C., Fou nie , J., C ous, P., G uy e , J De, Woudenbe g, J., Hi ayama,
K., Tanaka, K., Poin ing, S., Hyde, K., 2009. Mul i-locus phylogeny o he
Pleospo ales: a axonomic, ecological and e olu iona y e-e alua ion. S ud. Mycol.
64, 85–102.
Zhao, A., Liu, L., Xu, T., Shi, L., Xie, W., Zhang, W., Fu, S., Feng, H., Chen, B., 2018.
Influences o canopy ni ogen and wa e addi ion on AM ungal biodi e si y and
communi y composi ion in a mixed deciduous o es o China. F on . Plan Sci. 9.
h ps://doi.o g/10.3389/ pls.2018.01842.
Zhu, W., Cai, X., Liu, X., Wang, J., Cheng, S., Zhang, X., Li, D., Li, M., 2010. Soil mic obial
popula ion dynamics along a ch onosequence o mois e e g een b oad-lea ed o es
succession in sou hwes e n China. J. M . Sci. 7, 327–338. h ps://doi.o g/10.1007/
s11629-010-1098-z.
D. Alem, e al. Fo es Ecology and Managemen 474 (2020) 118328
12
O iginal a icles
97
O iginal a icle II
Comunidades de hongos del suelo bajo Pinus pa ula Schiede ex
Schl dl. &e io; Cham. Bosques de plan aciones de di e en es
edades en E iopía
Demelash Alem1,2, Ta ek Dejene2, Juan And és O ia-de-Rueda1, Józse Geml3 and
Pablo Ma ín-Pin o1,*
1
Sus ainable Fo es Managemen Resea ch Ins i u e, Uni e si y o Valladolid (Palencia), A da. Mad id
44, 34071, Palencia, Spain; [email protected] (D.A.); o ia@ag o.u a.es (J.A.O.-d.-R.)
2
E hiopian En i onmen and Fo es Resea ch Ins i u e, Fo es P oduc s Inno a ion Resea ch Di ec o a e,
P.O. Box 24536, 1000 Addis Ababa, E hiopia; [email protected]
3
MTA-EKE Lendüle En i onmen al Mic obiome Resea ch G oup, Esz e házy Ká oly Uni e si y, Leányka
u. 6, H-3300 Ege , Hunga y
Fo es s 11, 1109. h ps://doi.o g/10.3390/ 11101109
Resumen
Es p obable que el cul i o de plan aciones o es ales cambie la di e sidad y
composición de las comunidades de hongos del suelo. En la ac ualidad, hay poca
in o mación sob e es as comunidades en los sis emas o es ales de plan aciones de
E iopía. E aluamos las comunidades de hongos del suelo en Pinus pa ula Schiede ex
Schl dl. & Cham. S ands de 5, 11 o 36 años de edad u ilizando me aba coding de ADN
de amplicones ITS2. Las condiciones ecológicas de cada pa cela, como clima, al i ud y
suelo, ue on simila es. La edad del odal y la e ilidad del suelo in luye on en la
di e sidad de especies de hongos del suelo y los g emios ecológicos. En o al, se
iden i ica on 2262 unidades axonómicas ope a i as de hongos, de las cuales el 2%
e an ec omico ízicas (ECM). La di e sidad de hongos ECM ue mayo en los odales
de 5 y 36 años que en los odales de P. pa ula de 11 años. Con a iamen e a nues as
expec a i as, se obse ó un al o ni el de di e sidad de especies de ECM en odales
jó enes, lo que sugie e que es as especies de ECM pod ían compensa los e ec os del
es és nu icional en es os odales. Nues os esul ados ambién sugi ie on que la
abundancia de pa ógenos ege ales y sap ó o os no se io a ec ada po la edad del
odal. Es e es udio p opo ciona in o mación de e e encia sob e los cambios en las
comunidades de hongos en los odales de á boles de di e en es edades en las
plan aciones de P. pa ula en E iopía que p obablemen e es én elacionados con los
hongos ECM en odales jó enes donde p e alece una e ilidad del suelo
ela i amen e baja. Sin emba go, dado que las pa celas se es ablecie on en un solo
odal pa a cada clase de edad pa a cada a amien o, es e es udio debe conside a se
como un caso de es udio y, po an o, se debe ene p ecaución al aplica las
conclusiones a o os odales.
Palab as cla e: hongos ec omico ízicos; Secuenciación ion o en ; me aba coding;
Pinus pa ula; di e sidad de hongos en el suelo; sopo a la edad
A icle
Soil Fungal Communi ies unde Pinus pa ula Schiede
ex Schl dl. & Cham. Plan a ion Fo es s o Di e en
Ages in E hiopia
Demelash Alem 1,2, Ta ek Dejene 2, Juan And és O ia-de-Rueda 1, Józse Geml 3,4 and
Pablo Ma ín-Pin o 1,*
1Sus ainable Fo es Managemen Resea ch Ins i u e, Uni e si y o Valladolid (Palencia), A da. Mad id 44,
34071 Palencia, Spain; [email p o ec ed] (D.A.); [email p o ec ed] (J.A.O.-d.-R.)
2E hiopian En i onmen and Fo es Resea ch Ins i u e, Fo es P oduc s Inno a ion Resea ch Di ec o a e,
P.O. Box 24536, 1000 Addis Ababa, E hiopia; [email p o ec ed]
3Biodi e si y Dynamics Resea ch G oup, Na u alis Biodi e si y Cen e , Da winweg 2, P.O. Box 9517,
2300 RA Leiden, The Ne he lands; [email p o ec ed]
4MTA-EKE Lendüle En i onmen al Mic obiome Resea ch G oup, Esz e házy Ká oly Uni e si y,
Leányka u. 6, H-3300 Ege , Hunga y
*Co espondence: [email p o ec ed]; Tel.: +34-979-108-340; Fax: +34-979-108-440
Recei ed: 3 Sep embe 2020; Accep ed: 14 Oc obe 2020; Published: 19 Oc obe 2020
Abs ac :
The cul i a ion o plan a ion o es s is likely o change he di e si y and composi ion
o soil ungal communi ies. A p esen , he e is scan in o ma ion abou hese communi ies in
E hiopian plan a ion o es sys ems. We assessed he soil ungal communi ies in Pinus pa ula Schiede
ex Schl dl. & Cham. s ands aged 5, 11, o 36-yea s-old using DNA me aba coding o ITS2 amplicons.
The ecological condi ions o each plo , such as clima e, al i ude, and soil, we e simila . S and age
and soil e ili y in luenced soil ungal species di e si y and ecological guilds. In o al, 2262 ungal
ope a ional axonomic uni s we e iden i ied, o which 2% we e ec omyco hizal (ECM). The di e si y
o ECM ungi was highe in he 5 and 36-yea -old s ands han in he 11-yea -old P. pa ula s ands.
Con a y o ou expec a ions, a high le el o ECM species di e si y was obse ed in young s ands,
sugges ing ha hese ECM species could compensa e o he e ec s o nu ien s ess in hese s ands.
Ou esul s also sugges ed ha he abundance o plan pa hogens and sap o ophs was no a ec ed
by s and age. This s udy p o ides baseline in o ma ion abou ungal communi y changes ac oss
ee s ands o di e en ages in P. pa ula plan a ions in E hiopia ha a e likely ela ed o ECM ungi
in young s ands whe e ela i ely low soil e ili y p e ails. Howe e , gi en ha he plo s we e
es ablished in a single s and o each age class o each ea men , his s udy should be conside ed as a
case s udy and, he e o e, cau ion should be exe cised when applying he conclusions o o he s ands.
Keywo ds:
ec omyco hizal ungi; Ion o en sequencing; me aba coding; Pinus pa ula; soil ungal
di e si y; s and age
1. In oduc ion
A ecen e iew o o es y in E hiopia e ealed ha de o es a ion is a con inuous p ocess [
1
].
When all o es use was included, a de o es a ion a e o 0.93% pe yea was calcula ed in 2010 [
2
,
3
].
Despi e his, es ablishing plan a ions o as -g owing exo ic ee species is becoming a majo pa o
o es y p ac ice in E hiopia [
4
,
5
]. Exo ic ee species plan a ions a e now es ima ed o co e 1,000,000 ha
o land [
5
,
6
]. One o hese in oduced ee species is Pinus, which is mainly being g own o mee he
inc easing demand o woody aw ma e ials [
6
–
8
]. As a consequence, Pinus pa ula Schiede ex Schl dl.
Fo es s 2020,11, 1109; doi:10.3390/ 11101109 www.mdpi.com/jou nal/ o es s
Fo es s 2020,11, 1109 8 o 18
a iables and plan a ion age. The Pe MANOVA analysis also indica ed ha he e we e species
composi ional di e ences be ween s ands in e ms o ECM ungi (F =3.21, p=0.003).
2
(a)
(b)
Figu e 3.
(
a
) De ended co espondence analyses and (
b
) canonical co espondence analysis (CCA)
o dina ion plo s based on Hellinge - ans o med abundance da a o myco hizal ungal species a he
o de le el o ungal communi ies associa ed wi h h ee age g oups o Pinus pa ula s ands in he s udy
a ea in E hiopia. Plo s shown in he same colo a e in he same s and (yellow, plo s in he 5-yea -old
s and; black, plo s in he 11-yea -old s and; ed, plo s in he 36-yea -old s and). Edaphic a iables a e
shown in g een. The pe cen ages o cumula i e explained a ia ion by each axis a e shown in (b).
Table 4.
Canonical co espondence analysis based on simple e m e ec s showing he signi icance
(p<0.05)
o edaphic a iables when conside ing he Hellinge ans o med da a o ec omyco hizal
species a he o de le el o ungal communi y in he s udy a ea.
Va iable Simple Te m E ec s
Explains % Pseudo-F p
Age 26.8 2.60 0.010
Phospho us 19.0 2.10 0.052
Se e al species belonging o he o de s Gomphales, Sebacinales, and Thelepho ales we e associa ed
wi h plo s in he oldes s and, whe e he soil is cha ac e ized by ela i ely high e ili y (based on
he o ganic ma e con en and he C/N a io). In 5 and 11-yea -old s ands, which a e cha ac e ized
by low soil e ili y (based on o ganic ma e con en and he C/N a io), he species belonging o
he o de Can ha ellales o med an associa ion wi h o he ungal species (Figu e 3). Species in he
o de s Bole ales, Pezizales and Aga icales we e associa ed wi h all age g oups o P. pa ula plan a ions
(Figu e 3).
Fo es s 2020,11, 1109 9 o 18
4. Discussion
4.1. Di e si y o Fungal OTUs
Fungi ha e been desc ibed as he mos in e es ing, enigma ic and species- ich o ganisms on
Ea h [
69
]. The use o molecula me hods in ecen yea s has d ama ically inc eased he numbe o
ungal OTUs de ec ed wo ldwide [
70
]. In his s udy, we de ec ed a o al o 2262 high-quali y OTUs,
o which 1303 OTUs (58%) belonged o he Ascomyco a, he la ges phylum o ungi [
71
], indica ing
he dominance o Ascomyco a in he P. pa ula o es s in es iga ed in his s udy. Fungi o en in e ac
wi h o he o ganisms, o ming bene icial o mu ualis ic associa ions. Coni e s in he Pinaceae usually
o m symbio ic ela ionships wi h ECM ungi. Thus, ECM ungi we e likely o play an impo an ole
in he P. pa ula plan a ions in ou s udy a ea. Howe e , o he o al OTUs iden i ied a genus le el
and classi ied by ecological unc ion, 41% we e sap o ophs, 7% we e plan pa hogens, and only 2%
we e ECM ungi. An explana ion o he small p opo ion o ECM ungi de ec ed migh be ha he
plan a ion a ea was loca ed in a non-ECM biome a ea. The na i e ege a ion ha o iginally g ew
in he s udy a ea was des oyed many yea s ago by logging and clea ance o c op cul i a ion [
10
].
The e o e, ungal symbion s compa ible wi h P. pa ula may be absen in he na i e ungal communi y
in he soil, enabling ECM ungi in oduced o he plan a ion a ea along wi h P. pa ula o co-in ade
he soil habi a [
72
]. Howe e , he ecological unc ion o 48% o he ungi iden i ied in his s udy is
unknown, indica ing ha we ha e ha dly sc a ched he su ace in e ms o unde s anding he ole
played by ungi in hese plan a ion o es sys ems. I migh also an indica ion o he lack o scien i ic
s udies on he local ungal lo a in he coun y. Thus, hey a e highligh ing he need o u he s udies
in he s udy a ea.
4.2. Di e si y o Func ional OTUs along he Ch onosequence o S ands
The Shannon and Simpson di e si y indices we e de e mined o explain a ia ions in he soil
ungal unc ional g oups a di e en s ages o P. pa ula s and de elopmen . Only ECM ungi showed
di e ences in hei di e si y among he s and age g oups. Ini ially, we expec ed ha as s ands
de eloped, soil e ili y would dec ease o e ime and ha hese condi ions would lead o highe ECM
ungal di e si y along he ch onosequence. By con as , he soil e ili y o young P. pa ula s ands
was expec ed o be highe han ha o old s ands and, he e o e, he ees we e expec ed o exe less
in luence on he ungal mic obiome. Howe e , ou in es iga ions e ealed ha he 5 and 36-yea -old
s ands had mo e di e se ECM ungi in hei soils han he 11-yea -old s and and we e mo e e ile.
Despi e his, he ela i e p opo ion o ECM abundance was highe in he 11-yea -old s and han in he
5 and 36-yea -old s ands due o he dominance o some ECM species in he 11-yea -old s and.
Soil mic oo ganisms, including ungi, a e in luenced by s and de elopmen in se e al ways [
73
,
74
].
As he s and de elops, he amoun o ee co e di ec ly modi ies he amoun o ligh a ailable, which
a ec s he composi ion o he unde s o y, which egula es ca bon alloca ion, nu ien cycling and soil
wa e con en [
75
]. The ela i ely highe di e si y indices o ECM ungi in he 5-yea -old s and han
in he 11-yea -old s and may possibly be explained by he less de eloped ee canopy a he ea lie
s age o s and de elopmen , which may ha e allowed di e se ECM ungi o in e ac ex ensi ely wi h
he oo sys ems o unde s o y plan s [
75
]. Ano he explana ion o he ela i ely highe di e si y
indices o ECM ungi in he 5-yea -old s and may be he p e ious land use o he plan a ion a ea.
Deacon and Fleming [
76
] demons a ed ha when a o es a ion akes place on land ini ially used
o o he pu poses, he ECM ungal spo es a e he undamen al inoculum du ing he ea ly s age o
ECM succession. In his case, p io o he es ablishmen o P. pa ula plan a ions, he s udy a ea was
p e iously used o ag icul u al pu poses, which migh ha e con ibu ed o he di e si y o ECM ungi
in young s ands o P. pa ula ees due o he p ima y succession o ECM ungi h ough inocula in he
spo e bank de i ed om o he nea by myco hizal-associa ed plan a ions such as Eucalyp us sp. L’H
é
.
plan a ions [24,36].
Fo es s 2020,11, 1109 10 o 18
The ela i ely highe di e si y indices o ECM species in he 36-yea -old s and han in he
11-yea -old s and may e lec a di e ence in he managemen o he 36-yea -old s and.
Chen e al. [77]
indica ed ha hinning could inc ease he ela i e abundance o myco hizal ungi because hinning
opens up he o es canopy, which inc eases soil empe a u e and mois u e [
78
]. Thinning may he e o e
ha e a posi i e e ec on mic obial ac i i y [
79
] because soil empe a u e and mois u e in luence he
eac ion o mic obial enzymes and, hus, shi he mic obial communi y composi ion by al e ing
subs a es and ex acellula enzyme ac i i y [
80
]. Do e and Kee on [
81
] and Tomao e al. [
82
] ha e
sugges ed ha ungal di e si y can be conse ed o e en inc eased using o es managemen p ac ices
ha enhance he s uc u al complexi y o s ands and he la e-successional cha ac e is ics o he o es
and by ca ying ou low-impac logging ope a ions. In his s udy, he 36-yea -old s and had unde gone
hinning as pa o a managemen ope a ion in he s udy a ea [
8
], which could ha e enhanced he oo
g ow h o he emaining ees [
83
,
84
], p o iding new en i onmen s o soil mic obes, which could lead
o an imp o emen in ungal di e si y h ough oo a achmen s. Cas año e al. [
12
] obse ed ha he
species di e si y o soil ungi emained s able a e hinning, ega dless o i s in ensi y, when su icien
hos ees and unc ional oo s om hinned ees we e e ained. This inding has been suppo ed by a
numbe o di e en epo s. Fo example, acco ding o Mölde e al. [
85
], hinning could main ain a high
le el o ECM ungal di e si y in ma u e s ands. Chen e al. [
86
] and Dang e al. [
75
] also hypo hesized
ha when hinning ope a ions a e pe o med, ligh a ailabili y, wa e , and nu ien s inc ease, which
imp o es he o es mic oclima ic condi ions and, hence, he di e si y o ECM ungi could be imp o ed
by his ype o managemen p ac ice. Fu he mo e, Goldmann e al. [
87
] epo ed ha ECM ungi
we e less di e se in unmanaged o es s han in highly managed s ands. Thus, we sugges ha o es
managemen p ac ices such as hinning could be one o he ac o s ha impac ECM ungal di e si y
along he ch onosequence o P. pa ula s ands, al hough his should be u he s udied.
4.3. Fungal Composi ion and Edaphic Va iables
Fo es soils con ain a di e se ange o ungal species. The composi ion o soil ungal communi ies
is in luenced by di e en ac o s, such as dispe sal, plan di e si y, soil p ope ies, land use, and clima e,
which a e key componen s o o es sys ems [
88
,
89
]. Speci ically, di e en ungal species a e likely o
espond o en i onmen al d i e s in di e en ways, depending on hei cha ac e is ic ai s [
90
,
91
],
and, hus, in u n, he composi ion o soil ungal communi ies is di ec ly co ela ed wi h soil e ili y
and plan g ow h s a us [
92
]. Myco hizal species a e a pa icula ly impo an pa o he soil
ungal communi y because hey o m a bene icial symbio ic associa ion wi h plan s, p o iding hem
wi h nu ien s in e u n o pho osyn he ically ixed ca bon [
93
], which is especially ele an unde
nu ien -limi ed condi ions [
94
]. ECM ungi also play a key ole in alle ia ing he d ough s ess
o he hos ee [
95
]. The composi ion o ECM ungi in he soil is also co ela ed wi h soil e ili y
and he g ow h s a us o he hos ees [
92
,
96
]. In his s udy, we ound ha bo h s and age and soil
e ili y we e ac o s ha a ec ed he ungal communi y composi ion in ou s udy a ea. Ou o dina ion
analysis indica ed ha he 36-yea -old s and and he 5-yea -old s and had dis inc i e soil ungal
communi ies, cha ac e ized by a ela i ely high numbe o ECM species. P e ious s udies ha e ela ed
simila indings ega ding ungal communi y composi ion o se e al ac o s, such as changes in soil
e ili y [
24
], changes in oo densi y [
97
], speci ic li e-his o y e en s ha ha e occu ed since he s and
was es ablished o changes in mic oclima e condi ions [
12
]. Fo example, less li e accumula ion in
young P. pa ula s ands esul ed in less o ganic ma e and a lowe C/N a io in he 5 and 11-yea -old
s ands in his s udy compa ed wi h he 36-yea -old s and. This si ua ion leads o ees ha ing a
g ea e dependence on myco hizal ungal associa ions o enhanced nu ien and wa e up ake and
a ailabili y [
24
]. Simila ly, he g ea e di e si y o ECM species in young s ands may indica e ha
sui able symbion s a e p esen . Howe e , olde s ands ha e a g ea e capaci y o educe luc ua ions in
empe a u e and o main ain adequa e mois u e le els [
98
–
100
], which is pa icula ly impo an o
he occu ence o ECM ungi. The abundance o ECM ungi in olde s ands is gene ally g ea e han in
younge s ands, which could be acili a ed by he oo sys ems o old ees, which could inc ease he
Fo es s 2020,11, 1109 11 o 18
chances o ECM associa ions o ming [
85
], he eby acili a ing he easy up ake o nu ien s by ees [
94
].
Thus, he dis inc composi ion o ECM ungi in young and old s ands migh no only be ela ed o si e
quali y ac o s, such as soil e ili y, bu also o s and age ac o s (e.g., he inc easing a ea o ee oo
explo a ion in he soil wi h s and age); howe e , his needs o be in es iga ed u he . Gi en ha he
amoun o o ganic ma e , a ailable P, and he C/N a io o 5 and 11-yea -old s ands showed no g ea e
di e ence in hei alues, his may ha e enabled 11-yea -old s ands o de elop an associa ion wi h
only a limi ed numbe o ECM ungi, bu a highe ela i e abundance o hese ECM ungi, which could
indica e inc eased dependence o P. pa ula ees on a limi ed numbe o dominan symbion species.
In any case, he su i al o P. pa ula in soils in which ECM species comp ise only a small p opo ion o
he mic obial communi y, oge he wi h o he ac o s, suppo s he iew ha P. pa ula is well adap ed
o he condi ions in his s udy a ea; howe e , his also needs u he s udy.
Fe ile soil con ains nu ien s ha enable he g ow h and de elopmen o a soil ungal
communi y [
101
]. Thus, in u n, he ungi a e di ec ly in luenced by edaphic pa ame e s [
102
–
104
].
In his s udy, edaphic ca ion elemen s, such as Mg and K, we e also co ela ed wi h he o e all ungal
communi y om he whole da a se , which indica es ha soil ca ion concen a ions could in luence he
composi ion o he ungal communi y [
105
]. Ca ions in gene al play an impo an pa in a numbe o
physicochemical p ocesses, such as pho osyn hesis [
106
] and, hus, can a ec plan pho osyn hesis
and, hence, he amoun o ca bon ha is a ailable o soil ungi and bac e ia [
107
]. O he a ious
ca ions, Ca is one o he main edaphic ac o s ha in luence he s uc u e o soil ungal communi ies
wo ldwide [
108
]. O he edaphic elemen s ha e also been epo ed o in luence he composi ion o
ungal communi ies in o es sys ems. Fo example, in his s udy, a ailable P and ee age in luenced he
composi ion o myco hizal ungi (Table 4), which was simila o he indings epo ed by Rosens ock
e al. [
109
]. The composi ion o ungi in he soil pa icula ly ha o myco hizal ungi, can also be
in luenced by N a ailabili y [
110
]. High le els o a ailable N could dec ease he dependency o he
hos plan on myco hizal ungi, which could educe he amoun o ca bon alloca ed o ungi [
111
],
which e en ually could cause compe i ion among he ungal species and could lead o changes in hei
composi ion [
96
,
110
]. In his s udy, he C/N a io o soil in 5 and 11-yea -old s ands was ela i ely
low compa ed wi h ha o 36-yea -old P. pa ula s ands (Table 1). This esul is inconsis en wi h
Wang and Wang [
96
] who epo ed ha a high C/N a io nega i ely in luenced ungal communi y
s uc u e, p obably because a high concen a ion o N es ains he expansion o ungi. Ou esul s also
con i med his, in he sense ha he ungal di e si y was low in s ands whe e he soil C/N a io was
high, indica ing ha a high C/N a io migh no a o he ungal communi y in he o es s in he s udy
a ea. Soil o ganic ma e could also impac he composi ion o soil ungal communi ies because ungi
gene ally ex end hei mycelia a he soil–li e in e ace [
112
]. The amoun o o ganic ma e a ec s
he wa e holding capaci y o soil and nu ien a ailabili y, which could a ec mycelial ou g ow h and
ne wo k o ma ion [
113
,
114
]. Howe e , soil acidi y can also in luence he composi ion o soil ungal
communi ies [115,116] h ough i s in luence on spo e ge mina ion and mycelial de elopmen [117].
Fungi ha e di e en li e-his o y s a egies and, in plan a ions, ea ly colonize ungal species
ha elish dis u bance colonize i s , ollowed by supe io compe i o s ha can ou compe e he ea ly
colonize species in olde s ands whe e esou ces a e ge ing sca ce . In his s udy, we ound ha some
ungal species associa ed wi h P. pa ula ees we e de ec ed a all age s ages o ee de elopmen , such as
hose belonging o he gene a Tomen ella,Rama ia, and Inocybe. These gene a ha e se e al hund eds
o species, many s ill undesc ibed, and hei s a egies do no seem o be conse ed a he genus
le el. O hese, Tomen ella and Inocybe a e cosmopoli an species ha inhabi Eucalyp us plan a ions in
E hiopia [
24
]. Species o Rhizopogon we e also associa ed mo e wi h younge s ands (5- and 11-yea -old
s ands) in his s udy, which suppo s p e ious indings ha hey a e ea ly colonize ungal species [
118
].
The Rhizopogon species a e known as spo e bank species ha acili a e he es ablishmen o ees in
o me ly non- o es habi a s. O he axa belonging o he gene a Amani a ha e also been epo ed in
ou P. pa ula plan a ion o es s. These ungi species a e well-known o hei associa ion wi h coni e
o es s as he gene a is cha ac e is ic o la e-s age pine s ands ha a e 30–40 yea s old [119,120].
Fo es s 2020,11, 1109 12 o 18
5. Conclusions
Ou s udy explained he soil ungal communi y composi ion associa ed wi h a P. pa ula plan a ion
in E hiopia. The di e si y alue o i al ungi such as ECM was ela i ely highe in he younges s and
han in he wo olde s ands. S and age and soil e ili y we e also ound o a ec ungal communi y
composi ion. Some ECM ungi we e ound as ea ly colonize species in he young s and and we e
eplaced by supe io compe i o species as he P. pa ula s ands de eloped.
The o e all low le el o ECM species ichness de ec ed in he P. pa ula s ands is p obably because
his is a plan a ion o an ECM ee in a non-ECM biome. Due o he impo ance o ungi in plan a ion
o es sys em, he esul s o his s udy could be ele an o he p omo ion and conse a ion o o es s
in E hiopia h ough he p omo ion o non-wood o es p oduc s such as ungi, which could also
p o ide ood esou ces o poo popula ions du ing imes o ood sca ci y. Thus, i is impe a i e
o in es iga e how soil ungal communi ies espond o managemen egimes such as hinning and
clea -cu ing. The high di e si y and ela i e abundance o plan pa hogenic ungi de ec ed in his
s udy also highligh s he need o p o ec E hiopian plan a ions om plan diseases and pes s.
Al hough he ecological condi ions o all s udied plo s we e simila in e ms o clima e, al i ude,
and soil, he esul s o his s udy should be conside ed as a case s udy, gi en ha he plo s we e
es ablished in a single s and o each age class o each ea men and, he e o e, he applicabili y o
any conclusions o o he s ands should be ea ed wi h cau ion. Fu he mo e, addi ional scien i ic
in es iga ions o he plan a ion o es ecosys em a e needed in o de o consolida e he E hiopian
ungal biodi e si y da abase.
Supplemen a y Ma e ials:
The ollowing a e a ailable online a h p://www.mdpi.com/1999-4907/11/10/1109/s1,
Table S1: Summa y o he Simila i y Pe cen age (SIMPER) analysis showing con as s be ween he cumula i e
o al con ibu ion (50% cu -o ) and he con ibu ion (%) o he mos in luen ial ungal ope a ional axonomic uni s
o he dissimila i y o he soil ungi de ec ed in h ee Pinus pa ula s ands o di e en age g oups in a plan a ion in
Wondo Gene , E hiopia.
Au ho Con ibu ions:
Concep ualiza ion, P.M.-P., J.A.O.-d.-R. and T.D.; me hodology, J.G., P.M.-P. and T.D.;
so wa e, D.A., P.M.-P. and T.D.; alida ion, P.M.-P.; o mal analysis, P.M.-P., J.G. and T.D.; in es iga ion, P.M.-P.,
T.D. and D.A.; da a cu a ion, D.A.; w i ing—o iginal d a p epa a ion, T.D. and D.A.; w i ing— e iew and
edi ing, P.M.-P., T.D. and J.A.O.-d.-R. All au ho s ha e ead and ag eed o he published e sion o he manusc ip .
Funding:
This esea ch wo k was pa ially suppo ed by he E asmus Mundus-D eam p ojec g an and by he
p ojec SUSTIFUNGI_ET (Sus ungi_E h:2017/ACDE/002094) unded by he Spanish Agency o In e na ional
De elopmen and Coope a ion. This wo k was also co- unded by he Spanish Minis y o Educa ion and Cul u e
unde a Sal ado de Mada iaga g an ag eemen , n◦PRX17/00315.
Acknowledgmen s:
We would like o exp ess ou g a i ude o he people in ol ed in he ield wo k o his s udy.
Con lic s o In e es : The au ho s decla e no con lic o in e es .
Re e ences
1. Geb u, T. De o es a ion in E hiopia: Causes, Impac s and Remedy. In . J. Eng. De . Res. 2016,4, 204–209.
2.
FAO. Global Fo es Resou ces Assessmen . Rome, I aly. A ailable online: h p://www. ao.o g/3/i1757e/
i1757e00.h m (accessed on 1 Sep embe 2020).
3.
Zewdie, M.; Tes aye, A.; Gi ma, Y. Managemen Plan o Fo es Plan a ions o WGCF-NR; Final Documen ;
WGCF-NR: Wondo Gene , E hiopia, 2010.
4.
Moges, Y. The Expe iences o REDD+ o E hiopian Condi ion, 1s ed.; Technology Dissemina ion Wo kshop:
Dama, E hiopia, 2015.
5.
Tes aye, M.A.; Ga di, O.; Anbessa, T.B.; Blase , J. Abo eg ound biomass, g ow h and yield o some selec ed
in oduced ee species, namely Cup essus lusi anica, Eucalyp us saligna, and Pinus pa ula in Cen al
Highlands o E hiopia. J. Ecol. En i on. 2020,44, 1–18. [C ossRe ]
6. Bekele, M. Fo es Plan a ions and Woodlo s in E hiopia. A ican Fo . Fo um. 2011,1, 52.
7.
Gezahgne, A. Diseases o Exo ic Plan a ion Fo es y T ees in E hiopia. Ph.D. Thesis, Uni e si y o P e o ia,
P e o ia, Sou h A ica, 2003.
Fo es s 2020,11, 1109 13 o 18
8.
Dejene, T.; O ia-De-Rueda, J.A.; Ma
í
n-Pin o, P. Fungal di e si y and succession ollowing s and de elopmen
in Pinus pa ula Schiede ex Schl dl. & Cham. plan a ions in E hiopia. Fo . Ecol. Manag.
2017
,395, 9–18.
[C ossRe ]
9.
T , B. Clima e-g ow h Rela ionship o Pinus pa ula Schldl. e Cham. in Wondo Gene , Sou h Cen al E hiopia.
J. Clim. Wea he . Fo ecas . 2016,4, 1–8. [C ossRe ]
10. Teshome, T. Analysis o esin and u pen ine oil cons i uen s o Pinus pa ula g own in E hiopia. E hiop. e-J.
Res. Inno . o esigh . 2011,3, 38–48.
11.
Canini, F.; Zucconi, L.; Pacelli, C.; Selbmann, L.; Ono i, S.; Geml, J. Vege a ion, pH and Wa e Con en as
Main Fac o s o Shaping Fungal Richness, Communi y Composi ion and Func ional Guilds Dis ibu ion in
Soils o Wes e n G eenland. F on . Mic obiol. 2019,10, 2348. [C ossRe ]
12.
Cas año, C.; Alday, J.G.; Lindahl, B.D.; De A ag
ó
n, J.M.; De-Miguel, S.; Colinas, C.; Pa lad
é
, J.; Cas año, C.;
Bone , J.A. Lack o hinning e ec s o e in e -annual changes in soil ungal communi y and di e si y in a
Medi e anean pine o es . Fo . Ecol. Manag. 2018,424, 420–427. [C ossRe ]
13.
Fe nandez, C.W.; Nguyen, N.H.; S e anski, A.; Han, Y.; Hobbie, S.E.; Mon gome y, R.A.; Reich, P.B.;
Kennedy, P.G. Ec omyco hizal ungal esponse o wa ming is linked o poo hos pe o mance a he
bo eal- empe a e eco one. Glob. Chang. Biol. 2016,23, 1598–1609. [C ossRe ] [PubMed]
14. Tede soo, L.; Bah am, M.; Zobel, M. How myco hizal associa ions d i e plan popula ion and communi y
biology. Science 2020,367, eaba1223. [C ossRe ]
15.
Lindahl, B.D.; Ih ma k, K.; Bobe g, J.; T umbo e, S.E.; Högbe g, P.; S enlid, J.; Finlay, R.D. Spa ial sepa a ion
o li e decomposi ion and myco hizal ni ogen up ake in a bo eal o es . New Phy ol.
2006
,173, 611–620.
[C ossRe ] [PubMed]
16.
Dahlbe g, A.; Schimmel, J.; Taylo , A.F.; Johannesson, H. Pos - i e legacy o ec omyco hizal ungal
communi ies in he Swedish bo eal o es in ela ion o i e se e i y and logging in ensi y. Biol. Conse .
2001
,
100, 151–161. [C ossRe ]
17.
Dalong, M.; Luhe, W.; Guo ing, Y.; LiQiang, M.; Chun, L. G ow h esponse o Pinus densi lo a seedlings
inocula ed wi h h ee indigenous ec omyco hizal ungi in combina ion. B az. J. Mic obiol.
2011
,42,
1197–1204. [C ossRe ]
18.
A e ill, C.; Tu ne , B.L.; Finzi, A.C. Myco hiza-media ed compe i ion be ween plan s and decompose s
d i es soil ca bon s o age. Na . Cell Biol. 2014,505, 543–545. [C ossRe ] [PubMed]
19.
Lin, G.; McCo mack, M.L.; Ma, C.; Guo, D. Simila below-g ound ca bon cycling dynamics bu con as ing
modes o ni ogen cycling be ween a buscula myco hizal and ec omyco hizal o es s. New Phy ol.
2016
,
213, 1440–1451. [C ossRe ] [PubMed]
20.
O win, K.H.; Ki schbaum, M.U.F.; John, M.G.S.; Dickie, I.A. O ganic nu ien up ake by myco hizal ungi
enhances ecosys em ca bon s o age: A model-based assessmen . Ecol. Le . 2011,14, 493–502. [C ossRe ]
21.
S e kenbu g, E.; Clemmensen, K.E.; Ekblad, A.; Finlay, R.D.; Lindahl, B.D. Con as ing e ec s o
ec omyco hizal ungi on ea ly and la e s age decomposi ion in a bo eal o es . ISME J.
2018
,12, 2187–2197.
[C ossRe ]
22.
Bald ian, P.; Voˇ
í
ško
á
, J.; Dobi
á
šo
á
, P.; Me hau o
á
, V.; Lis
á
, L.; Val
á
ško
á
, V. P oduc ion o ex acellula
enzymes and deg ada ion o biopolyme s by sap o ophic mic o ungi om he uppe laye s o o es soil.
Plan . Soil 2010,338, 111–125. [C ossRe ]
23.
Shanmugam, S.G.; Kinge y, W.L. Changes in soil mic obial communi y s uc u e in ela ion o plan succession
and soil p ope ies du ing 4000 yea s o pedogenesis. Eu . J. Soil Biol. 2018,88, 80–88. [C ossRe ]
24.
Cas año, C.; Dejene, T.; Media illa, O.; Geml, J.; O ia-De-Rueda, J.A.; Ma
í
n-Pin o, P. Changes in ungal
di e si y and composi ion along a ch onosequence o Eucalyp us g andis plan a ions in E hiopia. Fungal Ecol.
2019,39, 328–335. [C ossRe ]
25.
Dickie, I.A.; Ma
í
nez-Ga c
í
a, L.B.; Koele, N.; G ele , G.-A.; Tylianakis, J.M.; Pel ze , D.A.; Richa dson, S.J.
Myco hizas and myco hizal ungal communi ies h oughou ecosys em de elopmen . Plan . Soil
2013
,367,
11–39. [C ossRe ]
26.
K üge , C.; Kohou , P.; Janouško
á
, M.; Püschel, D.; F ouz, J.; Rydlo
á
, J. Plan Communi ies Ra he han
Soil P ope ies S uc u e A buscula Myco hizal Fungal Communi ies along P ima y Succession on a Mine
Spoil. F on . Mic obiol. 2017,8, 719. [C ossRe ] [PubMed]
Fo es s 2020,11, 1109 14 o 18
27.
Gassibe, P.V.; Fabe o, R.F.; He n
á
ndez-Rod
í
guez, M.; O ia-De-Rueda, J.A.; Ma
í
n-Pin o, P. Fungal communi y
succession ollowing wild i e in a Medi e anean ege a ion ype domina ed by Pinus pinas e in No hwes
Spain. Fo . Ecol. Manag. 2011,262, 655–662. [C ossRe ]
28.
Luoma, D.L.; F enkel, R.E.; T appe, J.M. F ui ing o Hypogeous Fungi in O egon Douglas-Fi Fo es s:
Seasonal and Habi a Va ia ion. Mycologia 1991,83, 335. [C ossRe ]
29.
He n
á
ndez-Rod
í
guez, M.; O ia-De-Rueda, J.A.; Ma
í
n-Pin o, P. Pos - i e ungal succession in a
Medi e anean ecosys em domina ed by Cis us ladani e L. Fo . Ecol. Manag. 2013,289, 48–57. [C ossRe ]
30.
Cla idge, A.W.; T appe, J.M.; Lunney, D. Managing habi a o mycophagous ( ungus- eeding) mammals:
A bu ning issue? In Conse a ion o Aus alia’s Fo es Fauna; Royal Zoological Socie y o New Sou h Wales:
Mosman, Aus alia, 2004; pp. 936–946.
31.
Reazin, C.; Mo is, S.; Smi h, J.; Cowan, A.; Jumpponen, A. Fi es o di e ing in ensi ies apidly selec dis inc
soil ungal communi ies in a No hwes US ponde osa pine o es ecosys em. Fo . Ecol. Manag.
2016
,377,
118–127. [C ossRe ]
32.
Yang, T.; Adams, J.M.; Shi, Y.; He, J.-S.; Jing, X.; Chen, L.; Tede soo, L.; Chu, H. Soil ungal di e si y in na u al
g asslands o he Tibe an Pla eau: Associa ions wi h plan di e si y and p oduc i i y. New Phy ol.
2017
,215,
756–765. [C ossRe ]
33.
Blaalid, R.; Ca lsen, T.; Kuma , S.; Hal o sen, R.; Ugland, K.I.; Fon ana, G.; Kause ud, H. Changes in he
oo -associa ed ungal communi ies along a p ima y succession g adien analysed by 454 py osequencing.
Mol. Ecol. 2011,21, 1897–1908. [C ossRe ]
34.
Clemmensen, K.E.; Finlay, R.D.; Dahlbe g, A.; S enlid, J.; Wa dle, D.A.; Lindahl, B.D. Ca bon seques a ion is
ela ed o myco hizal ungal communi y shi s du ing long- e m succession in bo eal o es s. New Phy ol.
2014,205, 1525–1536. [C ossRe ]
35.
Bone , J.A.; Gonz
á
lez-Olaba ia, J.R.; De A ag
ó
n, J.M. Mush oom p oduc ion as an al e na i e o u al
de elopmen in a o es ed moun ainous a ea. J. M . Sci. 2014,11, 535–543. [C ossRe ]
36.
Dejene, T.; O ia-De-Rueda, J.A.; Ma
í
n-Pin o, P. Fungal di e si y and succession unde Eucalyp us g andis
plan a ions in E hiopia. Fo . Ecol. Manag. 2017,405, 179–187. [C ossRe ]
37.
O ega-Ma
í
nez, P.; Ma inez-Pena, F. A sampling me hod o es ima ing spo oca ps p oduc ion o wild
edible mush ooms o social and economic in e es . In es ig. Ag a . Sis . Recu . Fo .
2008
,17, 228. [C ossRe ]
38.
T
ó
h, B.B.; Ba a, Z. Ecological s udies o ec omyco hizal ungi: An analysis o su ey me hods. Fungal
Di e s. 2010,45, 3–19. [C ossRe ]
39.
Nielsen, U.; Ay es, E.; Wall, D.; Ba dge , R. Soil biodi e si y and ca bon cycling: A e iew and syn hesis o
s udies examining di e si y– unc ion ela ionships. Eu . J. Soil Sci. 2011,62, 105–116. [C ossRe ]
40.
B ussaa d, L.; De Rui e , P.C.; B own, G.G. Soil biodi e si y o ag icul u al sus ainabili y. Ag ic. Ecosys .
En i on. 2007,121, 233–244. [C ossRe ]
41.
Desalegn, T.; Gonzalo, J.; Tu ion, M.-B. E ec s o sho - o a ion Eucalyp us plan a ions on soil quali y
a ibu es in highly acidic soils o he cen al highlands o E hiopia. Soil Use Manag.
2016
,32, 210–219.
[C ossRe ]
42.
Belaynesh, Z. Pe cep ions o Fo es Resou ce Changes in and A ound Wondo Gene Ca chmen and i s Nea
Fu u e Impac s. Mas e ’s Thesis, Wondo Gene College o Fo es y, Wondo Gene , E hiopia, 2002.
43.
Cos a, A.D.A.; Mo a o, S.; Roque, A.C.; Tin
ó
s, R. A compu a ional model o explo a o y ac i i y o a s wi h
di e en anxie y le els in ele a ed plus-maze. J. Neu osci. Me hods 2014,236, 44–50. [C ossRe ] [PubMed]
44.
Ze ga, B.; Be a, A. P e e ence, pu pose, and pa e n o Eucalyp us ee a ming in Eza We eda, E hiopia.
J. Soc. Sci. Humani . Res. 2016,3, 30–38.
45.
E iksson, H.; S e n, M. A Soil S udy a Wondo Gene Fo es y Resou ces Ins i u e, E hiopia. A ailable online:
h ps://ag is. ao.o g/ag is-sea ch/sea ch.do? eco dID=SE19880048966 (accessed on 1 Sep embe 2020).
46.
Eshe u, Z.; Högbe g, P. Recons uc ion o Fo es Si e His o y in E hiopian Highlands Based on 13 C Na u al
Abundance o Soils. Ambio 2000,29, 83–89. [C ossRe ]
47.
Bekele, T.; Kassa, K.; Mengis u, T.; Debele, M.; Melka, Y. Wo king wi h communi ies o add ess de o es a ion
in he Wondo Gene ca chmen A ea, E hiopia: Lessons lea n om a pa icipa o y ac ion esea ch. Res. J.
Ag ic. En i on. Manag. 2013,2, 448–456.
Fo es s 2020,11, 1109 15 o 18
48.
Smi h, J.E.; Molina, R.; Huso, M.M.; Luoma, D.L.; McKay, D.; Cas ellano, M.A.; Lebel, T.; Valacho ic, Y.
Species ichness, abundance, and composi ion o hypogeous and epigeous ec omyco hizal ungal spo oca ps
in young, o a ion-age, and old-g ow h s ands o Douglas- i (Pseudo suga menziesii) in he Cascade Range
o O egon, U.S.A. Can. J. Bo . 2002,80, 186–204. [C ossRe ]
49.
De La Va ga, H.; Agueda, B.; Ma
í
nez-Peña, F.; Pa lad
é
, J.; Pe a, J. Quan i ica ion o ex a adical soil
mycelium and ec omyco hizas o Bole us edulis in a Sco s pine o es wi h a iable spo oca p p oduc i i y.
Myco hiza 2011,22, 59–68. [C ossRe ] [PubMed]
50.
Voˇ
í
ško
á
, J.; B abco
á
, V.; Caj haml, T.; Bald ian, P. Seasonal dynamics o ungal communi ies in a empe a e
oak o es soil. New Phy ol. 2013,201, 269–278. [C ossRe ]
51.
Ih ma k, K.; Bödeke , I.T.; C uz-Ma inez, K.; F ibe g, H.; Kuba o a, A.; Schenck, J.; S id, Y.; S enlid, J.;
B ands öm-Du ling, M.; Clemmensen, K.E.; e al. New p ime s o ampli y he ungal ITS2 egion - e alua ion
by 454-sequencing o a i icial and na u al communi ies. FEMS Mic obiol. Ecol.
2012
,82, 666–677. [C ossRe ]
52.
Whi e, T.J.; Bu ns, T.; Lee, S.; Taylo , J. Amplica ion and Di ec Sequencing o Fungal Ribosomal RNA Genes
o Phylogene ics. In PCR P o ocols: A Guide o Me hods and Applica ions; Michael, A.I., Gel and, D., Sninsky, J.,
Whi e, T.J., Eds.; Academic P ess: New Yo k, NY, USA, 1990; pp. 315–322.
53.
Reeuwijk, L. P ocedu es o Soil Analysis. In e na ional Soil Re e ence and In o ma ion Cen e, Wageningen,
The Ne he lands. A ailable online: h ps://www.boku.wzw. um.de/ ileadmin/downloads/w b/ISRIC_
TechPap09_2002.pd (accessed on 1 Sep embe 2019).
54.
Walkley, A.; Black, I.A. An examina ion o he diges ion me hod o de e mining soil o ganic ma e and a
p oposed modi ica ion o he ch omic acid i a ion me hod. Soil Sci. 1934,34, 29–38. [C ossRe ]
55.
Kim, J.; K elle , A.C.R.; G eenbe g, M.M. P epa a ion and Analysis o Oligonucleo ides Con aining he
C4‘-Oxidized Abasic Si e and Rela ed Mechanis ic P obes. J. O g. Chem.
2005
,70, 8122–8129. [C ossRe ]
[PubMed]
56.
Me hods o Soil Analysis, Pa 2. A ailable online: h ps://books.google.com.hk/books?hl=zh-CN&l =
&id=P WDwAAQBAJ&oi= nd&pg=PR15&dq=Me hods+o +Soil+Analysis&o s=TwMB-l4x6H&sig=
RcejRQxwE 3YDFWz9e UT5y9ye4& edi _esc=y# =onepage&q=Me hods%20o %20Soil%20Analysis& =
alse (accessed on 3 Sep embe 2020).
57.
Bouyoucos, G.H. A Reclama ion o he Hyd ome e o Making Mechanical Analysis. Ag on. J.
1951
,43,
434–438. [C ossRe ]
58.
Edga , R.C. Sea ch and clus e ing o de s o magni ude as e han BLAST. Bioin o ma ics
2010
,26, 2460–2461.
[C ossRe ]
59.
K
õ
ljalg, U.; Nilsson, R.H.; Aba enko , K.; Tede soo, L.; Taylo , A.F.S.; Bah am, M.; Ba es, S.T.; B uns, T.D.;
Beng sson-Palme, J.; Callaghan, T.M.; e al. Towa ds a uni ied pa adigm o sequence-based iden i ica ion o
ungi. Mol. Ecol. 2013,22, 5271–5277. [C ossRe ]
60.
Shannon, C.E. A ma hema ical heo y o communica ion. ACM SIGMOBILE Mob. Compu . Commun. Re .
2001,5, 3–55. [C ossRe ]
61.
Taylo , D.; Ken , M.; Coke , P. Vege a ion Desc ip ion and Analysis: A P ac ical App oach. Geog . J.
1993
,159,
237. [C ossRe ]
62.
Magu an, A.E. Ecological Di e si y and I s Measu emen ; Sp inge Science and Business Media LLC:
Be lin/Heidelbe g, Ge many, 1988.
63.
Kind , R.; Coe, R. T ee di e si y analysis. In A Manual and So wa e o Common S a is ical Me hods o Ecological
and Biodi e si y S udies; Wo ld Ag o o es y Cen e (ICRAF): Nai obi, Kenya, 2005.
64.
R Co e Team. R: A Language and En i onmen o S a is ical Compu ing; R Founda ion o S a is ical Compu ing:
Vienna, Aus ia, 2019.
65.
Smilaue , P.; Lepš, J. Mul i a ia e Analysis o Ecological Da a Using CANOCO 5; Camb idge Uni e si y P ess
(CUP): Camb idge, UK, 2014.
66.
Ande son, M.J. A new me hod o non-pa ame ic mul i a ia e analysis o a iance. Aus al. Ecol.
2001
,26,
32–46. [C ossRe ]
67.
Cla ke, K.R. Non-pa ame ic mul i a ia e analyses o changes in communi y s uc u e. Aus al. Ecol.
1993
,
18, 117–143. [C ossRe ]
68.
Pa a acini, V.; Micheli, F.; Mon e alcone, M.; Villa, E.; Mo i, C.; Bianchi, C.N. Rapid assessmen o epiben hic
communi ies: A compa ison be ween wo isual sampling echniques. J. Exp. Ma . Biol. Ecol.
2010
,395,
21–29. [C ossRe ]
Fo es s 2020,11, 1109 16 o 18
69. Pu is, A.; Hec o , A. Ge ing he measu e o biodi e si y. Na . Cell Biol. 2000,405, 212–219. [C ossRe ]
70.
Wu, B.; Hussain, M.; Zhang, W.; S adle , M.; Liu, X.; Xiang, M. Cu en insigh s in o ungal species di e si y
and pe spec i e on naming he en i onmen al DNA sequences o ungi. Mycology
2019
,10, 127–140.
[C ossRe ]
71.
James, T.Y.; Kau , F.; Schoch, C.L.; Ma heny, P.B.; Ho s e e , V.; Cox, C.J.; Celio, G.; Gueidan, C.; F ake , E.;
Miadlikowska, J.; e al. Recons uc ing he ea ly e olu ion o Fungi using a six-gene phylogeny. Na . Cell Biol.
2006,443, 818–822. [C ossRe ]
72.
U celay, C.; Longo, S.; Geml, J.; Tecco, P.; Nouh a, E. Co-in asi e exo ic pines and hei ec omyco hizal
symbion s show capabili ies o wide dis ance and al i udinal ange expansion. Fungal Ecol.
2017
,25, 50–58.
[C ossRe ]
73.
Mi chell, R.; Kei h, A.M.; Po s, J.M.; Ross, J.; Reid, E.; Dawson, L.A. O e s o y and unde s o y ege a ion
in e ac o al e soil communi y composi ion and ac i i y. Plan . Soil 2011,352, 65–84. [C ossRe ]
74.
Pe al a, R.M.; Ahn, C.; Gille e , P.M. Cha ac e iza ion o soil bac e ial communi y s uc u e and
physicochemical p ope ies in c ea ed and na u al we lands. Sci. To al. En i on.
2013
,443, 725–732.
[C ossRe ]
75.
Dang, P.; Gao, Y.; Liu, J.; Yu, S.; Zhao, Z. E ec s o hinning in ensi y on unde s o y ege a ion and soil
mic obial communi ies o a ma u e Chinese pine plan a ion in he Loess Pla eau. Sci. To al. En i on.
2018
,
630, 171–180. [C ossRe ] [PubMed]
76.
Deacon, J.W.; Fleming, L.V. In e ac ions o Ec omyco hizal Fungi. In Myco hizal Func ioning an In eg a i e
Plan -Fungal P ocess; Allen, M., Ed.; Chapman and Hall: New Yo k, NY, USA, 1992; pp. 249–300.
77.
Chen, J.; Xu, H.; He, D.; Li, Y.; Luo, T.; Yang, H.; Lin, M. His o ical logging al e s soil ungal communi y
composi ion and ne wo k in a opical ain o es . Fo . Ecol. Manag. 2019,433, 228–239. [C ossRe ]
78.
Wang, Y.; Wei, X.; Del Campo, A.D.; Winkle , R.; Wu, J.; Li, Q.; Liu, W. Ju enile hinning can e ec i ely
mi iga e he e ec s o d ough on ee g ow h and wa e consump ion in a young Pinus con o a s and in he
in e io o B i ish Columbia, Canada. Fo . Ecol. Manag. 2019,454, 117667. [C ossRe ]
79.
Pang, X.; Bao, W.; Zhu, B.; Cheng, W. Responses o soil espi a ion and i s empe a u e sensi i i y o hinning
in a pine plan a ion. Ag ic. Fo . Me eo ol. 2013,171, 57–64. [C ossRe ]
80.
Hasse , J.E.; Zak, D.R. Aspen Ha es In ensi y Dec eases Mic obial Biomass, Ex acellula Enzyme Ac i i y,
and Soil Ni ogen Cycling. Soil Sci. Soc. Am. J. 2005,69, 227. [C ossRe ]
81.
Do e, N.C.; Kee on, W.S. S uc u al Complexi y Enhancemen inc eases ungal species ichness in no he n
ha dwood o es s. Fungal Ecol. 2015,13, 181–192. [C ossRe ]
82.
Tomao, A.; Bone , J.A.; Cas año, C.; De-Miguel, S. How does o es managemen a ec ungal di e si y and
communi y composi ion? Cu en knowledge and u u e pe spec i es o he conse a ion o o es ungi.
Fo . Ecol. Manag. 2020,457, 117678. [C ossRe ]
83.
G an , C.D.; No man, M.A.; Smi h, M.A. Fi e and Sil icul u al Managemen o Res o ed Bauxi e Mines in
Wes e n Aus alia. Res o . Ecol. 2007,15, S127–S136. [C ossRe ]
84.
Lin, W.; Chen, W.; Wang, P. E ec s o o es hinning on di e si y and unc ion o mac o ungi and soil
mic obes. Sydowia 2011,63, 67–77.
85.
Mölde , A.; S ei , M.; Schmid , W. When beech s ikes back: How s ic na u e conse a ion educes
he b-laye di e si y and p oduc i i y in Cen al Eu opean deciduous o es s. Fo . Ecol. Manag.
2014
,319,
51–61. [C ossRe ]
86.
Chen, X.; Wang, N.; Chen, X.; Wang, J.; Diao, J.-J.; Zhang, J.-Y.; Guan, Q.-W. Soil mic obial unc ional di e si y
and biomass as a ec ed by di e en hinning in ensi ies in a Chinese i plan a ion. Appl. Soil Ecol.
2015
,92,
35–44. [C ossRe ]
87.
Goldmann, K.; Schöning, I.; Busco , F.; Wube , T. Fo es Managemen Type In luences Di e si y and
Communi y Composi ion o Soil Fungi ac oss Tempe a e Fo es Ecosys ems. F on . Mic obiol.
2015
,6, 1300.
[C ossRe ] [PubMed]
88.
Liang, Y.; He, X.; Chen, C.; Feng, S.; Liu, L.; Chen, X.; Zhao, Z.; Su, Y. In luence o plan communi ies and soil
p ope ies du ing na u al ege a ion es o a ion on a buscula myco hizal ungal communi ies in a ka s
egion. Ecol. Eng. 2015,82, 57–65. [C ossRe ]
89.
Rillig, M.C.; Aguila -T igue os, C.A.; Be gmann, J.; Ve b uggen, E.; Ve esoglou, S.D.; Lehmann, A. Plan
oo and myco hizal ungal ai s o unde s anding soil agg ega ion. New Phy ol.
2014
,205, 1385–1388.
[C ossRe ] [PubMed]
Fo es s 2020,11, 1109 17 o 18
90.
C ow he , T.W.; S an on, D.W.G.; Thomas, S.M.; A’Bea , A.D.; Hiscox, J.; Jones, T.H.; Voˇ
í
ško
á
, J.; Bald ian, P.;
Boddy, L. Top-down con ol o soil ungal communi y composi ion by a globally dis ibu ed keys one
consume . Ecology 2013,94, 2518–2528. [C ossRe ]
91.
Koide, R.T.; Fe nandez, C.W.; Malcolm, G. De e mining place and p ocess: Func ional ai s o ec omyco hizal
ungi ha a ec bo h communi y s uc u e and ecosys em unc ion. New Phy ol.
2014
,201, 433–439. [C ossRe ]
92.
Cozzolino, V.; Di Meo, V.; Monda, H.; Spaccini, R.; Piccolo, A. The molecula cha ac e is ics o compos a ec
plan g ow h, a buscula myco hizal ungi, and soil mic obial communi y composi ion. Biol. Fe il. Soils
2015,52, 15–29. [C ossRe ]
93. Smi h, S.E.; Read, D. Myco hizal Symbiosis; Else ie : Ams e dam, The Ne he lands, 2008.
94.
Read, D.J.; Pe ez-Mo eno, J. Myco hizas and nu ien cycling in ecosys ems—A jou ney owa ds ele ance?
New Phy ol. 2003,157, 475–492. [C ossRe ]
95.
Mohan, J.E.; Cowden, C.C.; Baas, P.; Dawadi, A.; F ankson, P.T.; Helmick, K.; Hughes, E.; Khan, S.; Lang, A.;
Machmulle , M.; e al. Myco hizal ungi media ion o e es ial ecosys em esponses o global change:
Mini- e iew. Fungal Ecol. 2014,10, 3–19. [C ossRe ]
96.
Wang, Q.-K.; Wang, S.-L. Soil mic obial p ope ies and nu ien s in pu e and mixed Chinese i plan a ions.
J. Fo . Res. 2008,19, 131–135. [C ossRe ]
97.
Peay, K.G.; Ga belo o, M.; B uns, T.D. E idence o dispe sal limi a ion in soil mic oo ganisms: Isola ion
educes species ichness on myco hizal ee islands. Ecology 2010,91, 3631–3640. [C ossRe ] [PubMed]
98.
Fe n
á
ndez-Toi
á
n, L.;
Á
g eda, T.; Olano, J.M. S and age and sampling yea e ec on he ungal ui body
communi y in Pinus pinas e o es s in cen al Spain. Can. J. Bo . 2006,84, 1249–1258. [C ossRe ]
99.
Pinna, S.; G
é
y, M.-F.; Co
é
, M.; Si ois, L. Fac o s in luencing uc i ica ion phenology o edible mush ooms
in a bo eal mixed o es o Eas e n Canada. Fo . Ecol. Manag. 2010,260, 294–301. [C ossRe ]
100.
Toi anen, T.; Ma kkanen, A.; Ko iaho, J.S.; Halme, P. The e ec o o es uel ha es ing on he ungal
di e si y o clea -cu s. Biomass Bioene gy 2012,39, 84–93. [C ossRe ]
101.
Siciliano, S.D.; Palme , A.S.; Winsley, T.; Lamb, E.; Bisse , A.; B own, M.V.; Van Do s , J.; Ji, M.; Fe a i, B.C.;
G ogan, P.; e al. Soil e ili y is associa ed wi h ungal and bac e ial ichness, whe eas pH is associa ed wi h
communi y composi ion in pola soil mic obial communi ies. Soil Biol. Biochem.
2014
,78, 10–20. [C ossRe ]
102.
D eno sky, R.; Vo, D.; G aham, K.; Scow, K. Soil Wa e Con en and O ganic Ca bon A ailabili y A e Majo
De e minan s o Soil Mic obial Communi y Composi ion. Mic ob. Ecol.
2004
,48, 424–430. [C ossRe ]
[PubMed]
103.
Laube , C.L.; S ickland, M.S.; B ad o d, M.A.; Fie e , N. The in luence o soil p ope ies on he s uc u e o
bac e ial and ungal communi ies ac oss land-use ypes. Soil Biol. Biochem. 2008,40, 2407–2415. [C ossRe ]
104.
Laube , C.L.; Hamady, M.; Knigh , R.; Fie e , N. Py osequencing-Based Assessmen o Soil pH as a P edic o
o Soil Bac e ial Communi y S uc u e a he Con inen al Scale. Appl. En i on. Mic obiol.
2009
,75, 5111–5120.
[C ossRe ]
105.
Song, J.; Chen, L.; Chen, F.-M.; Ye, J. Edaphic and hos plan ac o s a e linked o he composi ion o a buscula
myco hizal ungal communi ies in he oo zone o endange ed Ulmus chenmoui Cheng in China. Ecol.
E ol. 2019,9, 8900–8910. [C ossRe ]
106.
He, J.; Tede soo, L.; Hu, A.; Han, C.; He, D.; Wei, H.; Jiao, M.; Anslan, S.; Nie, Y.; Jia, Y.; e al. G ea e di e si y
o soil ungal communi ies and dis inguishable seasonal a ia ion in empe a e deciduous o es s compa ed
wi h sub opical e e g een o es s o eas e n China. FEMS Mic obiol. Ecol. 2017,93. [C ossRe ]
107.
Shi, L.-L.; Mo ime , P.E.; Slik, J.W.F.; Zou, X.-M.; Xu, J.-C.; Feng, W.-T.; Qiao, L. Va ia ion in o es soil ungal
di e si y along a la i udinal g adien . Fungal Di e s. 2013,64, 305–315. [C ossRe ]
108.
Tede soo, L.; Bah am, M.; P
õ
lme, S.; K
õ
ljalg, U.; Yo ou, N.S.; Wijesunde a, R.; Ruiz, L.V.; Vasco-Palacios, A.M.;
Thu, P.Q.; Suija, A.; e al. Global di e si y and geog aphy o soil ungi. Science
2014
,346, 1256688. [C ossRe ]
[PubMed]
109.
Rosens ock, N.P.; Be ne , C.; Smi s, M.M.; K
á
m, P.; Wallande , H. The ole o phospho us, magnesium
and po assium a ailabili y in soil ungal explo a ion o mine al nu ien sou ces in No way sp uce o es s.
New Phy ol. 2016,211, 542–553. [C ossRe ] [PubMed]
110.
Zhao, A.; Liu, L.; Xu, T.; Shi, L.; Xie, W.; Zhang, W.; Fu, S.; Feng, H.; Chen, B.-D. In luences o Canopy Ni ogen
and Wa e Addi ion on AM Fungal Biodi e si y and Communi y Composi ion in a Mixed Deciduous Fo es
o China. F on . Plan Sci. 2018,9, 9. [C ossRe ]
Fo es Ecology and Managemen 496 (2021) 119391
4
2.5. Vege a ion sampling
To ela e he ege a ion cha ac e is ics o he mac o ungal ichness
and di e si y, ege a ion in en o ies we e conduc ed in he plo s
es ablished o mac o ungal species sampling as desc ibed abo e.
Vascula plan s iden i ied in each plo s we e eco ded using hei
e nacula names. Fo hose species di icul o iden i y hei scien i ic
name in he ield, specimens we e collec ed and hei axonomic iden-
i ica ion was conduc ed using published olume o he lo a o E hiopia
and E i ea (Hedbe g and Sue, 1989). La ge ees g owing ou side he
plo s we e included in he su ey i hei c owns o e hung he plo s
because ee c own p ojec ion a eas can a ec mac o ungal occu ence
(Collins e al., 2018). Fu he mo e, la ge ees c ea e hei own mic o-
habi a and de elop a la ge oo sys em, p o iding mo e space o ungal
associa ions (Sch¨
on e al., 2018). Then, he ascula plan species ich-
ness and di e si y pa ame e s we e de e mined (Table 3). Plan pa-
ame e s and hei co ela ions we e also used o u he in e p e a ion
o mac o ungal pa e n om each s udy a eas. The myco hizal s a us o
he ascula ee species ound in each o he s udied plo s we e checked
using eely accessible da abases (Soudzilo skaia e al., 2020) and he
da a is p o ided (Table S1).
2.6. S a is ical analysis
Da a we e ans o med when needed o achie e he pa ame ic
c i e ia o no mali y and homoscedas ici y. The mac o ungi da a we e
no malized by a e ying he abundance da a o he smalles numbe o
mac o ungi pe plo . Also, he da a om soil a iables we e scaled using
base R and used o subsequen s a is ical analyses. Shannon’s H′di-
e si y index, H′=–Σpi (lnpi) (Shannon and Wea e , 1949), was es i-
ma ed o each o es , whe e pi indica es he ela i e abundance o he
species (Ken and Coke , 1993). Simpson’s di e si y, D =1 −Σ(pi2),
whe e pi is he impo ance p obabili y in elemen i; and he e enness, J
=H′/H′max, whe e H′is he numbe de i ed om he Shannon di e si y
index and he H′max is he maximum possible alue o H′we e also
calcula ed (Magu an, 1988). In addi ion o species ichness alues,
mac o ungi biomass p oduc ion le els in each o es we e es ima ed and
con e ed in o Kg bases. All di e si y measu es o mac o ungi and
ascula plan s we e analyzed using he Biodi e si y R package (Kind
and Coe, 2005) in R e sion 4.0.3 (R Co e Team, 2020). The di e ence in
he soil, ege a ion and spo oca ps a iables ac oss o es s we e assessed
by Linea Mixed E ec s models (LME, Pinhei o e al., 2016), whe e
block (a se o plo s in a same si e in each o es ) was de ined as andom
and o es was de ined as ixed ac o . The LME used o p e en he alse
posi i e associa ions due ela edness s uc u e in he sampling. Tukey
Tes was la e used o check signi ican di e ences (p ≤0.05) be ween
o es s when needed.
Species accumula ion cu es we e cons uc ed o compa e he a e a
which new ungal species we e ound in he h ee o es s and o p o ide
an es ima e o mac o ungal species ichness. Cu es we e gene a ed
using a sample-based es ima o o Es ima eS Ve sion 9 (Colwell, 2013).
The numbe o ungal species collec ed du ing each weekly isi o a plo
wi hin a o es cons i u ed he sample. Cu es we e gene a ed based on
he o al o he weekly sampling da ase s. A R´
enyi di e si y p o ile
(T´
o hm´
e ´
esz, 1995) was also used o depic he di e si y cu es o he
h ee chu ch o es s. When pa ame e alpha =0, his unc ion gi es he
o al species numbe and when alpha =1, his gi es an index p opo -
ional o he Shannon index.
The ela ionship o mac o ungal composi ion wi h he edaphic,
clima e and loca ion pa ame e s was isualized using non-me ic
mul idimensional scaling (NMDS), based on absence and p esence spe-
cies da a ma ix and en i onmen al scaled da a. A pe mu a ion-based
nonpa ame ic MANOVA (Pe MANOVA) (Ande son, 2001) using
B ay–Cu is dis ance was conduc ed o analyze di e ences in mac o-
ungal communi ies ac oss o es s. The isolines o he ele a ion also
plo ed on he NMDS o dina ions using he o disu unc ion. The co -
ela ion o NMDS axes sco es wi h explana o y a iables was assessed
using en i unc ion in R. To es he in luence o ca ego ies o he
edaphic, clima e and loca ion a iables on he ungal communi y, we
used Man el Tes (B ay-Cu is dis ance) on o al species ma ix and
scaled en i onmen al pa ame e s. Also, an analysis o simila i y pe -
cen ages (SIMPER; Cla ke, 1993) was pe o med o iden i y mac o ungal
species ha we e mos esponsible o he obse ed pa e ns and was
also used o de e mine he pe cen age con ibu ion o mac o ungal
species o signi ican dissimila i ies be ween he h ee o es s (Pa a i-
cini e al., 2010). The SIMPER analysis was pe o med using he sim
unc ion o he Vegan package in R (R Co e Team, 2020).
3. Resul s
3.1. Mac o ungal ichness and di e si y
In o al, 13,736 spo oca ps we e collec ed om he h ee chu ch
Table 1
Cha ac e is ics o he s udy si es and selec ed edaphic p ope ies.
Desc ip ions Fo es s
Ta agedam Alemsaga Banja
Geog aphical
loca ion
12◦06′–12◦07′N
37◦46′– 37◦47′E
11◦54′–11◦56′N
37◦55′–37◦57′E
10◦57′–11◦03′N
36◦39′– 36◦48′E
Al i ude ange
(m asl)
2142–2484 2180–2470 1870–2570
Mean annual
p ecipi a ion
(mm)
1098 1926 1884.3
Mean annual
empe a u e
(◦C)
19.5 15.8 18.7
Fo es a ea
(ha)
875 814 897
Densi y o ees
ha
−1
48.11 17.19 43.13
Sand (%) 58.89 ±2.93b 51.78 ±2.99b 68.67 ±2.21a
Sil (%) 28.44 ±2.38a 32.44 ±2.13a 20.00 ±1.76b
Clay (%) 12.67 ±1.37a 15.78 ±1.93a 11.33 ±1.33a
pH H2O 1:2.5 7.04 ±7.03a 5.85 ±6.59b 5.60 ±6.24c
EC (dS/m) 0.43 ±0.05b 0.28 ±0.03b 0.81 ±0.14a
Ex.Ca (cmol
(+)/kg)
13.95 ±0.60a 9.19 ±0.52b 13.55 ±0.87a
Ex.Mg (cmol
(+)/kg)
6.16 ±0.10a 4.58 ±0.15c 5.54 ±0.20b
Ex.Na (cmol
(+)/kg)
1.95 ±0.05a 2.05 ±0.10a 1.82 ±0.12a
Ex.K (cmol
(+)/kg)
0.73 ±0.06a 0.61 ±0.04a 0.77 ±0.06a
CEC (cmol
(+)/kg)
47.21 ±1.36a 34.89 ±0.92b 44.51 ±1.96a
O ganic ma e
(%)
4.46(0.60)a 3.35(1.34)b 4.87(0.10)a
Ni ogen (%) 0.23 ±0.01a 0.17 ±0.02b 0.26 ±0.01a
P (ppm) 17.18 ±5.72a 7.8 ±0.73b 17.64 ±6.05a
Dominan
species in
each plo s
May enus obscu a,
Ca issa edulis, Olea
sp.
Acacia abyssinica,
Buddleja
polys achya, Acacia
nilo ica
Albizia
gummi e a,
P unus a icana,
B ucea
an idysen e ica
Re e ences Gede aw and
So omessa (2014),
Zegeye e al.
(2011), Ze ihun
e al. (2013)
Bi hane e al.
(2017), Mas esha
e al. (2015), Wube
e al. (2004)
Abe e e al.
(2017)
No e: Values shown a e means; s anda d e o s o he means a e indica ed in
pa en heses. Values wi h di e en lowe case le e s a e signi ican ly di e en (p
<0.05). The mean annual p ecipi a ion and mean annual empe a u e a e gi en
based on nea by s a ions da a o each s udy a ea by he yea 2019. Abb e ia-
ions: EC, elec ical conduc i i y; CEC, ca ion exchange capaci y; m, me e ; mm,
millime e ; asl, abo e sea le el. The e e ences lis ed a e ela ed o he clima ic
and geog aphical desc ip ions o he s udy a eas.
D. Alem e al.
Fo es Ecology and Managemen 496 (2021) 119391
5
Table 2
Fungal spo oca ps collec ed in July and Augus in h ee chu ch o es s in No he n E hiopia.
Taxa O de Family T A B E LM
Aga icus augus us F . Aga icales Aga icaceae x E SS
Aga icus bi o quis (Qu´
el.) Sacc. Aga icales Aga icaceae x E SS
Aga icus campes is L. Aga icales Aga icaceae x x x E SS
Aga icus cup eob unneus (Jul.Sch¨
a e & S ee ex F.H.Mølle ) Pil´
a Aga icales Aga icaceae x x E SS
Aga icus megalospo us J. Chen, R.L. Zhao, Ka un. & K.D. Hyde Aga icales Aga icaceae x x x E SS
Aga icus moelle i Wasse Aga icales Aga icaceae x x E SS
Aga icus mu inaceus Bull. Aga icales Aga icaceae x E SS
Amani a agina a (Bull.) Lam. Aga icales Amani aceae x x EM
Amani a sp. Pe s. Aga icales Amani aceae x x E EM
Amani a e na (Bull.) Lam. Aga icales Amani aceae x x x E EM
Ampullocli ocybe cla ipes (Pe s.) Redhead, Lu zoni, Moncal o & Vilgalys Aga icales T icholoma aceae x x E LS
A omyces pyxida us (Pe s.) Jülich Russulales Amylos e eaceae x x x WS
Au icula ia au icula-judae (Bull.) Qu´
el. Au icula iales Au icula iaceae x E WS
Bispo ella ci ina (Ba sch) Ko & S.E.Ca p. Helo iales Helo iaceae x WS
Bje kande a adus a (Willd.) P.Ka s . Polypo ales Me uliaceae x x WS
Bolbi ius sp. F . Aga icales Bolbi iaceae x x DS
Bo is a aes i alis (Bono d.) Demoulin Aga icales Aga icaceae x x SS
Bo is a plumbea Pe s. Aga icales Aga icaceae x SS
Cal a ia cya hi o mis (Bosc) Mo gan. Aga icales Aga icaceae x x E SS
Cal a ia gigan ea (Ba sch) Lloyd Aga icales Aga icaceae x E SS
Cal a ia sp. F . Aga icales Aga icaceae x E SS
Can ha ellula umbona a (J.F.Gmel.) Singe Aga icales T icholoma aceae x x LS
Can ha ellus cinnaba inus (Schwein.) Schwein. Can ha ellales Hydnaceae x E EM
Chlo ophyllum molybdi es (G. Mey.) Massee Aga icales Aga icaceae x x x E LS
Chlo ophyllum hacodes (Vi ad.) Vellinga Aga icales Aga icaceae x x x E LS
Cla a ia alca a Pe s. Aga icales Cla a iaceae x SS
Climacodon sep en ionalis (F .) P. Ka s . Polypo ales Phane ochae aceae x WS
Cli ocybe ca olinensis H.E. Bigelow & Hesle Aga icales T icholoma aceae x x E LS
Cli ocybe cis ophila Bon & Con u Aga icales T icholoma aceae x E LS
Cli ocybe oe ens Melo . Aga icales T icholoma aceae x x x E LS
Cli ocybe ag ans (Wi h.) P.Kumm. Aga icales T icholoma aceae x x x E LS
Cli ocybe geo opa (Bull.ex DC.) Qu´
el Aga icales T icholoma aceae x E LS
Cli opilus hobsonii (Be k. & B oome) P.D. O on Aga icales En oloma aceae x x x LS
Conocybe apala (F .) A nolds Aga icales Bolbi iaceae x SS
Conocybe au ea (Jul.Sch¨
a .) Hongo Aga icales Bolbi iaceae x x SS
Conocybe dume o um (Velen.) S cek Aga icales Bolbi iaceae x x SS
Conocybe ene a (Schae .) Fayod Aga icales Bolbi iaceae x x x SS
Conocybe elu ipes (Velen.) Hauskn. & S cek Aga icales Bolbi iaceae x x x SS
Cop inellus dissemina us (Pe s.) J.E.Lange Aga icales Psa hy ellaceae x x SS
Cop inellus micaceus (Bull.) Vilgalys, Hopple & Jacq. Johnson Aga icales Psa hy ellaceae x x x SS
Cop inopsis sp. P. Ka s . Aga icales Cop inaceae x x SS
Cop inus coma us (O.F.Müll.) Pe s. Aga icales Cop inaceae x x x E DS
Cop inus lagopus (F .) F . Aga icales Cop inaceae x x DS
Cop inus micaceus (Bull.) F . Aga icales Cop inaceae x E DS
Cop inus ni eus (Pe s.) F . Aga icales Cop inaceae x x x E DS
Co ina ius ubellus Cooke Aga icales Co ina iaceae x x EM
C a e ellus ignicolo (R.H. Pe e sen) Dahlman, Danell & Spa a o a Can ha ellales Hydnaceae x E EM
C epido us applana us (Pe s.) P. Kumm. Aga icales Inocybaceae x x x E WS
C epido us mollis (Schae .) S aude Aga icales Inocybaceae x x x E WS
C ucibulum lae e (Huds.) Kambly Aga icales Aga icaceae x LS
Cys ode mella g anulosa (Ba sch) Ha maja Aga icales Aga icaceae x x LS
Dac ymyces palma us (Schwein.) Bu Dac ymyce ales Dac ymyce aceae x WS
Daedaleopsis con agosa (Bol on) J.Sch ¨
o . Polypo ales Polypo aceae x x WS
Daldinia concen ica (Bol on) Ces. & De No . Xyla iales Hypoxylaceae x WS
Deconica mon ana (Pe s.) P.D. O on Aga icales S opha iaceae x x x LS
En oloma asp ellum (F .) Fayod. Aga icales En oloma aceae x x x SS
En oloma oli aceohebes Noo del. & Hauskn. Aga icales En oloma aceae x x SS
En oloma poliopus (Romagn.) Noo del. Aga icales En oloma aceae x x SS
En oloma sp. F . ex P. Kumm. Aga icales En oloma aceae x x SS
En oloma unda um (Gille ) M.M. Mose Aga icales En oloma aceae x x SS
Fa olaschia caloce a R. Heim Aga icales Ma asmiaceae x WS
Gale ina badipes (Pe s.) Kühne . Aga icales S opha iaceae x x x WS
Geas um iplex Jungh. Geas ales Geas aceae x x x LS
Geoglossum sp. Pe s. Geoglossales Geoglossaceae x x SS
Gymnopilus sp1. P.Ka s . Aga icales Omphalo aceae x x WS
Gymnopilus sp2. P.Ka s . Aga icales Omphalo aceae x x WS
Gymnopilus sp3. P.Ka s . Aga icales Omphalo aceae x WS
Gymnopus d yophilus (Bull.) Mu ill Aga icales Omphalo aceae x x x LS
Gymnopus luxu ians (Peck) Mu ill Aga icales Omphalo aceae x LS
Gymnopus pu illus (F .) An onín, Halling & Noo del. Aga icales Omphalo aceae x x LS
Hebeloma ebu neum Malençon Aga icales S opha iaceae x EM
Hemimycena delec abilis (Peck) Singe . Aga icales T icholoma aceae x x x LS
Hexagonia enuis (Hook.) F . Polypo ales Polypo aceae x x x WS
Hohenbuehelia pe alodes (Bull.) Schulze . Aga icales Pleu o aceae x WS
(con inued on nex page)
D. Alem e al.
Fo es Ecology and Managemen 496 (2021) 119391
6
Table 2 (con inued)
Taxa O de Family T A B E LM
Hyg ocybe chlo ophana (F .) Wünsche Aga icales Hyg opho aceae x x x E SS
Hyg ocybe chlo ophana a . au an iaca Bon. Aga icales Hyg opho aceae x E SS
Hyg opho opsis au an iaca (Wul en) Mai e Bole ales Hyg opho opsidaceae x x x LS
Hyg opho us hypo hejus F . (F .) Aga icales Hyg opho aceae x x x E EM
Hymenaga icus sp1. Heinem. Aga icales Aga icaceae x E SS
Hymenaga icus sp2. Heinem. Aga icales Aga icaceae x SS
Inocybe i idiumbona a Pegle Aga icales Inocybaceae x EM
Lacca ia glab ipes McNabb. Aga icales Hydnangiaceae x EM
Lacca ia lacca a (Scop.) Cooke Aga icales Hydnangiaceae x EM
Lae ipo us sulphu eus (Bull.) Mu ill Polypo ales Fomi opsidaceae x x x E PP
Len inellus cochlea us (Pe s.) P. Ka s . Russulales Au iscalpiaceae x x E WS
Lepio a c is a a (Bol on) P.Kumm. Aga icales Aga icaceae x LS
Lepio a e mine (F .) P.Kumm. Aga icales Aga icaceae x x LS
Lepio a himalayensis Khalid & Razaq Aga icales Aga icaceae x x LS
Lepio a sp1. (Pe s.) G ay Aga icales Aga icaceae x LS
Lepio a sp2. (Pe s.) G ay Aga icales Aga icaceae x LS
Lepio a sp3. (Pe s.) G ay Aga icales Aga icaceae x x LS
Lep onia lamp opus (F .) Qu´
el. Aga icales En oloma aceae x x x SS
Leucoaga icus ame icanus (Peck) Vellinga. Aga icales Aga icaceae x x x E SS
Leucoaga icus pu pu eolilacinus Huijsman Aga icales Aga icaceae x x x E SS
Leucoaga icus sp1. Locq. ex Singe Aga icales Aga icaceae x x E SS
Leucoaga icus sp2. Locq. ex Singe Aga icales Aga icaceae x SS
Leucocop inus cepaes ipes (Sowe by) Pa . Aga icales Aga icaceae x x SS
Leucocop inus agilissimus (Be k. &M.A.Cu is) Pa . Aga icales Aga icaceae x SS
Lyophyllum in uma um (B es.) Kühne Aga icales Lyophyllaceae x EM
Mac olepio a p oce a (Scop.) Singe Aga icales Aga icaceae x E LS
Mac olepio a sp. Singe Aga icales Aga icaceae x E LS
Ma asimus sp1. F . Aga icales Ma asmiaceae x E LS
Ma asmiellus chamaecypa idis (Hongo) Hongo Aga icales Omphalo aceae x LS
Ma asmius a bo escens (Henn.) Beeli Aga icales Ma asmiaceae x x LS
Ma asmius candidus F . Aga icales Ma asmiaceae x E LS
Ma asmius guyanensis Mon . Aga icales Ma asmiaceae x x x E LS
Ma asmius o eades (Bol on) F . Aga icales Ma asmiaceae x x E LS
Ma asmius pu pu eos ia us Hongo Aga icales Ma asmiaceae x x x E LS
Ma asmius sco odonius (F .) F . Aga icales Ma asmiaceae x E LS
Ma asmius siccus Schwein. ex F . Aga icales Ma asmiaceae x x E LS
Ma asmius sp2. F . Aga icales Ma asmiaceae x x x E LS
Ma asmius sp3. F . Aga icales Ma asmiaceae x x E LS
Ma asmius unda us (Be k.) F . Aga icales Ma asmiaceae x x x E LS
Mic opsallio a sp. H¨
ohn. Aga icales Aga icaceae x SS
Mycena g iseo i idis A.H. Sm. Aga icales Mycenaceae x x LS
Mycena in e up a (Be k.) Sacc. Aga icales Mycenaceae x LS
Mycena henana Maas Gees . & Win e h. Aga icales Mycenaceae x x x LS
Mycena osea G ambe g Aga icales Mycenaceae x LS
Mycena sp1. (Pe s.) Roussel Aga icales Mycenaceae x LS
Mycena sp2. (Pe s.) Roussel Aga icales Mycenaceae x LS
Mycena s ipa a Maas Gees . & Schw¨
obel Aga icales Mycenaceae x x x LS
Mycena ene ima (Be k.) Qu´
el. Aga icales Mycenaceae x LS
Neopaxillus plumbeus Singe & Lodge. Bole ales Se pulaceae x x SS
Onnia omen osa (F .) P.Ka s . Hymenochae ales Hymenochae aceae x x WS
Panaeolina oenisecii (Pe s.) Mai e Aga icales Psa hy ellaceae x x x SS
Panaeolus imicola (F .) Qu´
el. Aga icales Psa hy ellaceae x DS
Panaeolus papilionaceus (Bull.) Qu´
el Aga icales Psa hy ellaceae x x DS
Panellus mi is (Pe s.) Singe Aga icales Mycenaceae x x WS
Phaeolus schweini zii (F .) Pa . Polypo ales Fomi opsidaceae x x WS
Phellinus noxius (Co ne ) G. Cunn. Hymenochae ales Hymenochae aceae x x PP
Phellinus populicola Niemel¨
a Hymenochae ales Hymenochae aceae x PP
Pholio a au i ella (Ba sch) P. Kumm. Aga icales S opha iaceae x x E WS
Pleu o us lu eoalbus Beeli Aga icales Pleu o aceae x x x E WS
Pleu o us populinus O.Hilbe &O.K.Mill. Aga icales Pleu o aceae x x E WS
Pleu o us pulmona ius (F .) Qu´
el. Aga icales Pleu o aceae x x E WS
Plu eus longis ia us (Peck) Peck Aga icales Plu eaceae x LS
Plu eus mammilla us (Longyea ) Minnis, Sundb. & Me h en. Aga icales Plu eaceae x LS
Plu eus umb osus (Pe s.) P. Kumm. Aga icales Plu eaceae x x x LS
Polypo us b umalis (Pe s) F . Polypo ales Polypo aceae x x x WS
Polypo us enuiculus (P. Beau .) F . Polypo ales Polypo aceae x x WS
Polypo us a ius (Pe s.) F . Polypo ales Polypo aceae x x x WS
Psa hy ella candolleana (F .) Mai e Aga icales Psa hy ellaceae x x x WS
Psa hy ella co ugis (Pe s.) Kon ad & Maubl. Aga icales Psa hy ellaceae x x WS
Psa hy ella mul ipeda a (Peck) A.H. Sm. Aga icales Psa hy ellaceae x x x WS
Psa hy ella g acilis (F .) Qu´
el. Aga icales Psa hy ellaceae x x x WS
Psa hy ella ammophila (Du ieu &L´
e .) P.D. O on Aga icales Psa hy ellaceae x x x WS
Psa hy ella piluli o mis (Bull.) P.D.O on Aga icales Psa hy ellaceae x x x WS
Psa hy ella sp1. F . ex Qu´
el. Aga icales Psa hy ellaceae x WS
Psa hy ella sp2. F . ex Qu´
el. Aga icales Psa hy ellaceae x WS
Psa hy ella sp3. F . ex Qu´
el. Aga icales Psa hy ellaceae x x WS
(con inued on nex page)
D. Alem e al.
Fo es Ecology and Managemen 496 (2021) 119391
7
o es s and classi ied in o 258 ungal axa (Table 2). Al hough iden i i-
ca ion o spo oca ps down o species le el was no possible, ou o he
o al axa collec ed, 155 (60%) we e iden i ied o species le el, 33 (13%)
o genus le el and u he 69 (27%) we e comple ely uniden i ied. The
uniden i ied spo oca ps we e excluded om u he analysis. The Basi-
diomyco a was he dominan phylum and was ep esen ed by 10 o de s,
62 amilies, 90 gene a, and 180 species. Ascomyco a was ep esen ed by
h ee o de s, se en amilies, se en gene a, and eigh species (Table 2).
Among he axa iden i ied, he Aga icaceae was he mos di e se
amily wi h 58 di e en axa, ollowed by Psa hy ellaceae (26), T i-
choloma aceae (22), and Mycenaceae (20), which oge he accoun ed
o 33.6% o he o al collec ed axa (Table 2). The mos abundan
gene a we e Te mi omyces, Psa hy ella, Leucoaga icus, Ma asmius, and
Mycena. The p opo ions o mac o ungal axa a he genus le el a e
p o ided (Fig. 2A). The Aga icales was he mos p e alen o de in he
h ee o es s (77.66%). Since many Aga icales a e conspicuous mac o-
ungi, i is no su p ising o ind a highe abundance du ing sampling.
The amily o genus and genus o species a ios we e 0.70 and 0.50,
espec i ely. To al numbe s o ungal axa pe amily encoun e ed in he
h ee s udied o es s a e p o ided (Fig. 2B). In e ms o he ophic
g oups, he majo i y o species we e sap ophy ic (81%) ollowed by
ec omyco hizal (14%) and pa asi ic axa (4%).
The accumula ion cu es (Fig. 3A) gene a ed o he axa iden i ied
in he h ee o es s show ha he sa u a ion o mac o ungal ichness was
no eached du ing he su ey gi en ha he cu es showed a s eady
inc ease wi h addi ional samplings. Al hough he e was no signi ican
di e ence in species ichness be ween he h ee o es s (p >0.05), he
axa accumula ion cu e o Banja o es showed a ela i ely s eepe
ising slope and yielded highe mac o ungal ichness alues han he
o he o es s. The highes mac o ungal di e si y alues we e ob ained
o Ta agedam o es ; howe e , di e si y was no signi ican ly di e en
o ha o he o he wo o es s (Fig. 3B). The occu ence o mac o ungi
was mo e une en in Banja o es han in he o he o es s (Table 3), wi h
no ungal species ound a all sampling e en s and ce ain mac o ungal
Table 2 (con inued)
Taxa O de Family T A B E LM
Psa hy ella sp4. F . ex Qu´
el. Aga icales Psa hy ellaceae x WS
Psa hy ella sp5. F . ex Qu´
el. Aga icales Psa hy ellaceae x x x WS
Psa hy ella sp6. F . ex Qu´
el. Aga icales Psa hy ellaceae x WS
Pseudocli ocybe cya hi o mis (Bull.) Singe Aga icales T icholoma aceae x LS
Pseudohydnum gela inosum (Scop.) P.Ka s . Au icula iales Exidiaceae x x x WS
Pseudoomphalina pachyphylla (F .) Knudsen. Aga icales T icholoma aceae x LS
Psilocybe o oideocys idia a Guzm´
an & Gaines Aga icales S opha iaceae x x LS
Psilocybe samuiensis Guzm´
an, Bandala & J.W.Allen Aga icales S opha iaceae x LS
Rama ia s ic a (Pe s.) Qu´
el. Gomphales Gomphaceae x x x E EM
Rhizopogon lu eolus K ombh. Bole ales Rhizopogonaceae x x x E EM
Rhizopogon pseudo oseolus A.H. Sm. Bole ales Rhizopogonaceae x E EM
Russula g acillima Jul. Sch¨
a . Russulales Russulaceae x EM
Russula och oleuca Pe s. Russulales Russulaceae x x x EM
Sa coscypha occiden alis (Schwein.) Sacc. Pezizales Sa coscyphaceae x x x WS
Scle ode ma a eola um Eh enb. Bole ales Scle ode ma aceae x EM
Scle ode ma au an ium (L.) Pe s. Bole ales Scle ode ma aceae x EM
Sebacina conc escens (Schwein.) P. Robe s Au icula iales Exidiaceae x EM
Skele ocu is ca neog isea A.Da id Polypo ales Polypo aceae x x WS
Suillus lu eus (L.) Roussel Bole ales Suillaceae x E EM
Suillus sp. G ay Bole ales Suillaceae x EM
Te ezia leonis (Tul. & C.Tul.) Tul. Pezizales Te eziaceae x x E EM
Te mi omyces clypea us R.Heim Aga icales Lyophyllaceae x x x E LS
Te mi omyces mic oca pus (Be k. & B oome) R. Heim Aga icales Lyophyllaceae x x E LS
Te mi omyces obus us (Beeli) R. Heim Aga icales Lyophyllaceae x x E LS
Te mi omyces sp. R. Heim Aga icales Lyophyllaceae x x x E LS
Te mi omyces schimpe i (Pa .) R.Heim Aga icales Lyophyllaceae x x x E LS
T ichap um bi o me (F .) Ry a den Polypo ales Polypo aceae x WS
T icholoma po en osum (F .) Qu´
el. Aga icales T icholoma aceae x E EM
T icholoma saponaceum (F .) P.Kumm. Aga icales T icholoma aceae x E EM
T icholoma sp. (F .) S aude Aga icales T icholoma aceae x E EM
T icholomopsis u ilans (Schae .: F .) Sing. Aga icales T icholoma aceae x x x WS
Vol a iella speciosa (F .) P.Kumm. Aga icales Plu eaceae x x LS
Wilcoxina mikolae (Chin S. Yang & H.E. Wilcox) Chin S. Yang & Ko Pezizales Py onema aceae x x E EM
Xe omphalina caulicinalis (Bull.) Kühne & Mai e Aga icales Mycenaceae x x x WS
Xe omphalina enuipes (Schwein.) A.H.Sm. Aga icales Mycenaceae x x x WS
Xe ula adica a (Relhan) D¨
o el Aga icales Physalac iaceae x x PP
Xyla ia hypoxylon (L.) G e . Xyla iales Xyla iaceae x WS
Xyla ia sc uposa (F .) F . Xyla iales Xyla iaceae x x WS
No e: Abb e ia ions: T = he Ta agedam o es g oup; A = he Alemsaga o es g oup; B = he Banja o es g oup; x =spo oca p p oduc ion; E =edible; LM =mode o
li e; PP =Plan pa hogen; EM =ec omyco hizal, SS =Soil sap o oph, WS =Wood sap o oph, LS =Li e sap o oph, DS =Dung sap o oph.
Table 3
Mac o ungal and ascula plan ichness and di e si y indices in h ee chu ch
o es s in No he n E hiopia.
Fo es s a us Banja o es Ta agedam o es Alemsaga o es
All mac o ungi
Richness 22.56 ±3.02a 18.44 ±2.34a 22.67 ±1.84a
Shannon 2.03 ±0.23a 2.57 ±0.13a 2.06 ±0.20a
Simpson 0.73 ±0.05b 0.88 ±0.02a 0.77 ±0.05ab
E enness 0.38 ±0.03c 0.60 ±0.03a 0.47 ±0.02b
Vascula plan s
Richness 5.78 ±0.55c 16.89 ±1.25a 12.67 ±1.04b
Shannon 1.38 ±0.12b 2.18 ±0.08a 2.04 ±0.07a
Simpson 0.67 ±0.05b 0.83 ±0.02a 0.82 ±0.02a
E enness 0.73 ±0.04a 0.55 ±0.03b 0.63 ±0.03ab
Ec omyco hizal ungi
Richness 3.88 ±0.64a 2.57 ±0.3a 2.67 ±0.21a
Shannon 1.09 ±0.1a 0.80 ±0.06a 0.90 ±0.07a
Simpson 0.61 ±0.03a 0.53 ±0.02a 0.57 ±0.02a
E enness 0.85 ±0.05a 0.91 ±0.05a 0.94 ±0.03a
No e: Values shown a e means ± he SE o he mean. Di e en lowe case le e s
indica e a signi ican di e ence (p <0.05) in ichness o di e si y be ween
o es s.
D. Alem e al.
Fo es Ecology and Managemen 496 (2021) 119391
8
species we e mo e dominan in Banja o es han in he o he wo o es s.
The Shannon index and ichness o ascula plan s we e signi i-
can ly co ela ed wi h Shannon and Simpson di e si y indices o he
ungal communi ies (Fig. 4). In e es ingly, o all hese a iables, he
highes alues we e ound in Ta agedam o es s and he lowes alues
we e obse ed in Banja o es s (Table 3).
Al hough he h ee o es s we e no signi ican ly di e en (p >0.05;
Table 3) in e ms o measu e o di e si y o hei ec omyco hizal ungal
species and ichness, mo e ec omyco hizal species we e collec ed om
Banja o es (20) han om Ta agedam (15) o Alemsaga (7) o es s
(Table 2).
3.2. Spo oca p p oduc ion
Ta agedam o es p oduced he g ea es quan i y o spo oca ps (25.4
kg ha
−1
), al hough p oduc ion le els we e no signi ican ly di e en (p
=0.63) o hose o Alemsaga o es (21.6 kg ha
−1
; Fig. 5). Howe e , bo h
o hese o es s p oduced signi ican ly g ea e quan i ies o spo oca ps
han Banja o es (p <0.05).
Six y eigh (36%) o he o al mac o ungi collec ed we e deemed o
be edible (Table 2). Banja o es p oduced he g ea es quan i y o edible
ungi (mean esh weigh , 1.8 kg ha
−1
) and Alemsaga o es p oduced
he leas (0.4 kg ha
−1
); howe e , he p oduc ion o edible species did no
di e signi ican ly among he h ee o es s (Fig. 5; p =0.01).
Fig. 2. (A) The p opo ions o mac o ungal axa a he genus le el (name o genus; he numbe o species; pe cen age); and (B) o al numbe s o ungal axa pe
amily encoun e ed in he h ee s udied o es s.
Fig. 3. Taxa accumula ion cu es gene a ed o he ungal communi y ound in he h ee s udied o es s using a a e ac ion sample-based es ima o (A) and R´
enyi
di e si y p o iles (B).
D. Alem e al.
Fo es Ecology and Managemen 496 (2021) 119391
9
3.3. Mac o ungal communi ies and edaphic a iables
The pe MANOVA analyses indica ed he h ee chu ch o es s di e ed
signi ican ly in hei mac o ungal composi ion (F =2.05, R
2
=0.14, p =
0.001; Fig. 6). Wi h espec o he explana o y a iables, ca ego ized
edaphic, clima e and loca ion pa ame e s we e co ela ed o he mac-
o ungal communi y composi ion (p <0.05; Table 4). O hese, Man el
es con i med ha loca ion a iables agg ega ely had a s ongly sig-
ni ican e ec on mac o ungal communi y s uc u e (p =0.000) han
ha o he clima e (p =0.009) and he edaphic a iables (p =0.112).
The signi icance o each explana o y a iable and hei agg ega ed
con ibu ion o he di e ence o he mac o ungal communi y composi-
ions is p o ided (Table 4).
The SIMPER analysis also iden i ied mac o ungal species ha
dis inguished be ween he h ee o es s (Table 5). The o e all be ween-
g oup dissimila i y (Sø ensen) was 88.73% o Ta agedam and Alem-
saga o es s, 94.44% o Alemsaga and Banja o es s, and 93.76% o
Ta agedam and Banja o es s. In his ega d, he Cop inellus species a e
ound he mos impo an in dis inguishing all o es loca ions along
wi h he o he s (Table 5). The cumula i e con ibu ion o he mos
in luen ial mac o ungal species o he dissimila i y be ween hese o -
es s is shown in Table 5.
4. Discussion
Al hough agmen a ion poses majo h ea s o o es ecosys ems, he
D y A omon ane o es s in he highland egion o E hiopia, including
o es agmen s owned by he chu ch o loca ed a ound chu ch o es
e i o ies, a e conside ed o be majo ese oi s o biodi e si y (Ae s
e al., 2016; Aynekulu e al., 2016; Da byshi e e al., 2003; Nyssen e al.,
2014). This s udy p o ides a comp ehensi e analysis o mac o ungal
communi ies and showed he di e ences in ungal communi y compo-
si ions o he agmen ed o es sys ems in No he n E hiopia. The di -
e ence in mac o ungal species among he h ee o es s migh be due o
he di e ence in ege a ion composi ion o he a ia ion in ecological
ac o s such as soils, which a e among he mos impo an ac o s ha
could a ec mac o ungal species (O ia-de-Rueda e al., 2010). The
a ailabili y o sui able subs a es due o he di e ence in plan inpu s on
Fig. 4. Sca e plo ma ices showing co ela ion coe icien s be ween he en i e ee and mac o ungal a iables and hei signi icance le els. Abb e ia ions: T =
ee, F = ungi. On he bo om o he diagonal, bi- a ia e sca e plo s wi h a i ed line a e displayed. On he op o he diagonal, he alue o he co ela ion is shown,
plus he signi icance le el o he p- alues, which a e indica ed by ed as e isks. p- alues: ***, <0.001; **, <0.01; and *, <0.05; *<0.1. (Fo in e p e a ion o he
e e ences o colo in his igu e legend, he eade is e e ed o he web e sion o his a icle.)
D. Alem e al.
Fo es Ecology and Managemen 496 (2021) 119391
10
he o es loo could be also a ac o explaining he a ia ion in ungal
species composi ion among he h ee o es s. The e en ion o plan
esidues is hough o enhance ungal ac i i y by p omo ing mois u e
e en ion and p o iding a sou ce o o ganic ca bon, which is impo an
o ungal su i al and g ow h (Blum ield and Xu, 2003). Thus, he
di e ences in subs a e ichness among hese h ee o es s can in luence
he di e si y and ichness o mac o ungal species (Re e chon e al.,
2010). Besides, he a ia ion in mac o ungal species among he h ee
o es s p obably e lec he he e ogenei y o hese habi a s, esul ing in
Fig. 5. F esh weigh o spo oca ps collec ed om h ee o es s in No he n
E hiopia. Da k-g ay ba s indica e he o al ungal species collec ed; ligh -g ay
ba s indica e edible ungal species. The da a shown a e means ± he SE o
he mean. Values wi h di e en lowe case le e s a e signi ican ly di e en (p
<0.05).
Fig. 6. Non-me ic Mul idimensional Scaling (NMDS) o dina ion g aph wi h
i ed explana o y a iables based on dissimila i ies calcula ed using he
B ay–Cu is index o mac o ungal communi ies composi ions om plo s in he
h ee o es s in No he n E hiopia wi h al i ude displayed as isolines. A ows
ep esen en i onmen al a iables ha we e mos signi ican ly (p <0.005)
ela ed o o dina ion. Ellipses indica e o es g oups wi h he names indica ed.
The explana o y a iables a e shown in blue colo : CEC, ca ion exchange ca-
paci y; OM, o ganic ma e ; Tmax, maximum daily empe a u e; and Tmin,
minimum daily empe a u e. (Fo in e p e a ion o he e e ences o colo in
his igu e legend, he eade is e e ed o he web e sion o his a icle.)
Table 4
Signi icance o he explana o y a iables o mac o ungal communi y compo-
si ions. Numbe s in bold indica e a highly signi ican e ec s (p <0.001).
Sou ces Con ibu ion% Va iables pseudo-F p
Edaphic a iables 7.13% pH 0.4358 0.004
CEC 0.3191 0.010
OM 0.2767 0.017
Clima e 14.11% Tmax 0.3441 0.004
Tmin 0.6150 0.001
Spa ial ac o s 33.92% La i ude 0.6162 0.001
No e: he a iables a e: CEC, ca ion exchange capaci y; OM, o ganic ma e ;
Tmax, maximum daily empe a u e and Tmin, minimum daily empe a u e.
Table 5
Summa y o simila i y pe cen age (SIMPER) esul s showing he cumula i e
o al con ibu ion (50% cu -o ) and he con ibu ion (%) o he mos in luen ial
species o he dissimila i y be ween s ands in he h ee o es s in No he n
E hiopia.
Species Indi idual
con ibu ion o he
dissimila i y
Cumula i e
con ibu ion o he
dissimila i y
Edibili y
s a us
Alemsaga and Banja o es s
Cop inellus
dissemina us
13.07 13.07
Cop inellus
micaceus
10.37 23.44
Cop inellus
micaceus
6.49 29.93
Geas um iplex 5.35 35.27
Ma asmius
guyanensis
4.19 39.46 edible
Psa hy ella sp. 3.33 46.31
Aga icus
megalospo us
3.06 49.37 edible
Ta agedam and Alemsaga o es s
Cop inellus
micaceus
7.42 7.42
Sa coscypha
occiden alis
6.02 13.44
Geas um iplex 5.36 18.80
Psa hy ella sp3. 3.83 30.81
Psa hy ella
candollena
3.60 34.41
Gymnopus
d yophilus
3.14 37.55
Ma asmius
guyanensis
2.92 40.47 edible
Phellinus noxius 2.74 43.20
Te mi omyces
obus us
2.24 45.44 edible
Psa hy ella sp. 2.04 47.49
Ma asmius
guyanensis
1.71 49.19 edible
Polypo us a ius 1.69 50.88
Ta agedam and Banja o es s
Cop inellus
dissemina us
13.21 13.21
Cop inellus
micaceus
10.45 23.67
Sa coscypha
occiden alis
5.68 29.34
Ma asmius
guyanensis
3.90 33.24 edible
Geas um iplex 3.50 40.63
Aga icus
megalospo us
3.08 43.71 edible
C epido us mollis 2.37 46.08 edible
Xyla ia sc uposa 1.96 48.04
C epido us
applana us
1.85 49.89 edible
Psa hy ella
co ugis
0.93 67.45
Psa hy ella
candollena
0.89 68.35
Psa hy ella
candolleana
0.87 69.22
Psa hy ella sp. 0.84 70.05
D. Alem e al.
Fo es Ecology and Managemen 496 (2021) 119391
11
a ia ions in mic oclima e and, hence, a ia ions in mois u e, empe -
a u e, and o he ac o s among hese di e en o es sys ems (Suggi
e al., 2011) ha in luence he ichness and p oduc i i y o ungi
(G´
omez-He n´
andez and Williams-Line a, 2011). Howe e , he cha ac-
e is ics o he mac o ungi hemsel es could also explain he a ia ion in
ungal species among he h ee o es s. Many mac o ungal species a e
belie ed o ui spon aneously, wi h no consis en pa e n o occu ence
a any ime gi en a o able en i onmen al condi ions and sui able
subs a es (Piepenb ing e al., 2012; Tibuhwa e al., 2011). Fu he mo e,
ungal spo oca ps a e sho -li ed and may las only a ew days be o e
decomposing o being ea en and, he e o e, may no ha e been obse ed
du ing ou weekly su eys (Mau ice e al., 2021).
Habi a agmen a ion can in luence he ungal communi ies in o -
es s (Saps o d e al., 2017). Lack o symbio ic ungal coloniza ion in
hese sys ems may be a limi ing ac o o seedling es ablishmen , which
is he main egene a ion ecological p ocess in he s udied o es s. Thus,
ees species mo e dependen on myco hizal ungi could po en ially
ha e a subs an ial dec ease in ec ui men , pa icula ly in he ehabili-
a ion o conse a ion scheme o he o es s (Tonn and Ib´
a˜
nez, 2017).
Al hough, ecen ly s udies epo ed he a ailabili y o Ec omyco hizal
(ECM) hos s plan om he opic egions (Tede soo e al., 2010), he
ECM associa ions has long been conside ed a e o absen om opical
o es ecosys ems (Co ales e al., 2018), pa icula ly o he A ican
o es s like ha o E hiopian. A p e ious s udy also epo ed he absence
o ECM ungi in he D y A omon ane o es s o E hiopia (Dejene e al.,
2017a). Though he majo i y o he species collec ed in his s udy we e
sap ophy ic, abou 14% we e cha ac e ized as ec omyco hizal. Species
om he gene al o Amani a, En oloma, Geas um, Lacca ia, Russula and
Rhizopogon we e epo ed om hese s udied o es s. Al hough he
myco hizal s a us o each ee species in he s udy a ea a e unknown
(Table S1), he exis ence o ECM species may be due o he di e se
ege a ion (F iis e al., 2010a,b) and, hence, he e may be mo e ees
p esen ha can ac as hos s o myco hizal ungi (Hailema iam e al.,
2013; Wube e al., 2003). Also, he exis ence o myco hizal species in
he s udied o es s can be explained by he dispe sion o myco hizal
inocula om nea by plan a ion o es s ha a e supposed o hos ees.
The plan a ions a e cons i u ed by Eucalyp us camaldulensses, Eucalyp us
globulus, Pinus pa ula and o he highland Aacacia species. Thus, he
indings p esen ed he e may ha e impo an implica ion o he indig-
enous o es sys em o he main enance o unc ional ungal di e si y in
E hiopia (Dejene e al., 2017a). Besides, he coexis ence o myco hizal
ungi wi h na u al o es s has many p ac ical ad an ages, such as he
exchange o wa e and nu ien s h ough hyphal ne wo ks (B und e ,
2002; B und e , 2004). They a e also commonly he key de e minan s
o plan popula ion and communi y dynamics in he o es s sys ems
(Tede soo e al., 2020). This esul p esen s an insigh in o he conse -
a ion o ungal unc ional g oups in he o es sys em in he s udy a eas
as hese unc ional g oups a e impo an o he ehabili a ion and
conse a ion o hese agmen ed o es s as he ungi, pa icula ly o he
ECM, species could po en ially ha e a subs an ial ole in ec ui men s
seedlings (Tonn and Ib´
a˜
nez, 2017). Thus, u he s udies on opical
ec omyco hizae a e deeply needed, pa icula ly in A ica whe e he
ege a ion esou ce is immense wi h signi ican li elihood and en i-
onmen al bene i s.
In E hiopia, wild mush ooms ha e been used o hei nu i ional and
medicinal p ope ies (Aba e, 2014; Dejene e al., 2017b; Tuno, 2001).
Equally o o he wild edibles, hey ha e also been used as a coping ood
du ing ood sho age pe iods (Alemu e al., 2012; Si o aw e al., 2020).
In some local ma ke s mush ooms a e also a ailable whe e hey a e sold
by he local people o ea n some income o supplemen he household
economy (Aba e, 2014). The spo oca p p oduc ions ob ained in his
s udy we e no high. Al hough u he esea ch is needed o e i y he
claim, he lowe biomass yield epo ed he e could be explained by he
single one species and he species composi ion. Some o he species
we e collec ed in a single ime du ing he collec ion pe iod. Majo i y o
he species we e sap ophy ic ungi and a e cha ac e ized by low biomass
p oduc ions (Gassibe e al., 2011; Media illa e al., 2014). Howe e ,
aluable edible mac o ungal species belonging o he Cal a ia, Lae ipo-
us, Pleu o us, Te mi omyces sp., and Mac olepio a gene a we e also
collec ed in his s udy. Among hese edible species, Te mi omyces sp. is
highly ega ded by local people in sou hwes E hiopia because o i s
good as e and a oma (Aba e, 2014). Al hough he o e all quan i y o
spo oca p biomass p oduced in he s udied o es s was low, he mos
p oduc i e species had biomass alues o app oxima ely 0.46 kg
ha
–1
y
−1
, which p o ides an insigh in o he po en ial p oduc ion le els
o aluable spo oca p species. This also p o ides a s a ing poin in
e ms o b oadening he managemen and conse a ion o agmen ed
o es s o he p oduc ion o non- imbe o es s p oduc s in E hiopia. In
addi ion, impo an ec omyco hizal species such as T icholoma, Rhizo-
pogon, and Suillus we e also ound in his s udy. The p esence o hese
species in he s udy a eas may be due o he high le el o plan di e si y
in chu ch o es s, which may p o ide ec omyco hizal ungi wi h a e y
b oad hos ange (Roy e al., 2008; Smi h and Read, 2008) and, hence,
he e may be a numbe o ees ha can ac as hos s o myco hizal
ungi (Hailema iam e al., 2013; Wube e al., 2003). In e es ingly, some
o he ungi in he gene a o T ichode ma could also unc ion as
biocon ol ac i i y (Vinale e al., 2008) in he o es s. In addi ion, he
o e all landscape connec i i y o exo ic ee plan a ions o nea by
agmen ed na u al o es s could also con ibu e o he p esence o
ec omyco hizal ungi in he ungal communi y assembly (Boe ae e
e al., 2018; Peay and B uns, 2014; Vanne e e al., 2016). In hese kind
o plan a ions, he local communi ies in E hiopia a e collec ing edible
mush ooms, pa icula ly in he Sou hwes pa o he coun y o hei
subsis ence use o o gene a e income in some cases (Dejene e al.,
2017c). Howe e , his inding may ha e impo an implica ions o
indigenous o es sys ems in e ms o he main enance o aluable
mac o ungal species o comme cial p oduc ion in E hiopia (Dejene
e al., 2017a). Thus, ou su ey o mac o ungi p o ides an insigh in o
he aluable ungal unc ional g oups p esen in he agmen ed D y
A omon ane o es sys em o E hiopia, which may aid hei conse a-
ion and managemen h ough inc easing hei economic ou pu s
h ough NTFPs p oduc ion in addi ion o o he o es s p oduc s.
Vascula plan s a e o en used as a su oga e o o al biodi e si y
(Schmi e al., 2005; Sæ e sdal e al., 2004). Thus, he ascula plan s
ha e also been conside ed a use ul indica o o ungal di e si y in
managemen p og ams based on he ac ha a species- ich plan com-
muni y assumed o ha e mo e ecological niches o mic ohabi a s
a ailable o ungi han a species-poo communi y (Chia ucci e al.,
2005). Howe e , in his s udy epo ed a lack o cong uence be ween he
species ichness o ascula plan s and mac o ungi in line wi h Rudol
e al. (2013) who indic ed he nega i e co ela ion be ween he wo
communi ies ega ding species ichness. Such co ela ion migh be due
o he ac ha highe species ichness o ascula plan s could cause
a ia ion o ligh a ailabili y o he g ound species, including mac o-
ungi, due o canopy (H¨
a d le e al., 2003). Thus, he ungal communi y
and hei species ichness could be in luenced by he amoun and a i-
a ion o ligh a ailabili y on he o es loo (Rudolph e al., 2018). The
low co ela ion o species ichness o ascula plan and ungi migh be
due o he ac ha he pooled plan species ichness no always maxi-
mize species ichness o o he o ganisms, including all mac o ungi
(Chia ucci e al., 2005). This is p obably because o he special ecolog-
ical equi emen s o he ungal ha cons i u e he composi ion o he
communi y, which a e linked o subs a e o o he ac o s ela ed o
habi a s such as edaphic a iables (Liang e al., 2015; Rillig e al., 2015).
In con a y o his, howe e , we ound an indica ion o he posi i e
co ela ion in he Shannon di e si y index alues o he wo commu-
ni ies. Such associa ion could sugges s ha he ee species iden i y can
be used as a ac o o mac o ungal di e si y (O sing e al., 2021). Gabel
and Gabel (2007) and McMullan-Fishe e al. (2010) also epo ed
posi i e co ela ions be ween plan iden i ies and ungal di e si y based
on abundance as a measu e o di e si y. This associa ion is pa icula ly
e iden o sap o ophic ungi because sap o ophic ungi inc ease hei
D. Alem e al.
Fo es Ecology and Managemen 496 (2021) 119391
12
communi y di e si y h ough he p o ision o wide a ie y o subs a es
om he di e se ege a ion o es ablish acili a i e in e ac ions in he
sys ems (Gessne e al., 2010; Wu e al., 2019; Zhang e al., 2018), which
in u n p omo e hei highe le els o di e si y (Ye e al., 2019). The
obse ed co ela ion o plan s and mac o ungi di e si y indices may
sugges he in luence o habi a mic ohe e ogenei y, causing a posi i e
co ela ion be ween bo h plan di e si y and mac o ungal di e si y
(Rudol e al., 2013). Thus, he p omo ion o ascula ee plan a ions in
hese agmen ed o es sys ems, such as en ichmen plan ings o assis-
ed na u al egene a ion sys ems, should o e sui able habi a s wi h
a iable mic oclima es ha would in luence and/o assis he di e si y
and p oduc i i y o ungal species in he agmen ed D y A omon ane
o es s o E hiopia.
S udies demons a ed ha ungal communi y composi ion can be
go e ned by a ious en i onmen al a iables and landscape he e oge-
nei y (Bah am e al., 2015; Fe a i e al., 2016; Peay e al., 2010;
Tede soo e al., 2014b). Thus, e alua ing he ungal communi ies in
di e en ecosys ems is essen ial o il e ou he ela i e con ibu ions o
en i onmen al ac o s o ungal di e si y and composi ion in an
ecosys em (Tian e al., 2018). In his s udy, he NMDS o dina ion agains
he en i onmen al a iables is shown dis inc mac o ungal pa e n o
he h ee s udied o es s. O he ca ego ized a iables, he spa ial ac o s
con ibu ed highly o d i ing he mac o ungi assembly oge he wi h
clima e and edaphic a iables. This may an indica ion ha he clima e,
and soil cha ac e is ics oge he a e i al in se ing spa ial a ia ion
(Chen e al., 2015), e lec ing he combined e ec s o hese a iables on
he ege a ion and hus on mac o ungal communi y (Li e al., 2020).
Al hough he ela i e deg ee o which o ganisms can mo e is de e -
mined by mul iple ac o s, Golan and Anne (2017) indica ed ha dis-
ances as a spa ial ac o could a ec he dispe sal o ungal p opagules.
This could a ec he la ge scale connec i ely o he di e en ungal
species o o m simila i y in communi y s uc u e o mo phology (Cal-
him e al., 2018). Howe e , his needs u he in es iga ion o p o ide
an ecological meaning ul explana ion om ou s udy a eas. Con e sely,
speci ic ungal species a e likely o espond o en i onmen al a iables,
mainly edaphic pa ame e s, in di e en ways (Cozzolino e al., 2016;
Koide e al., 2014), and, hus, in u n, he composi ion o he ungal
communi y is di ec ly co ela ed wi h edaphic a iables (Cozzolino
e al., 2016). In pa icula , pH is known o be he mos c i ical soil
cha ac e is ic a ec ing he composi ion and s uc u e o ungal com-
muni ies ac oss di e en con inen s (Doche y e al., 2015; Fie e and
Jackson, 2006; Zhang e al., 2016). Simila ly in his s udy also, soil pH
appea ed o be co ela ed wi h ungal species composi ion. We ound
ha he p esence o g ea e numbe s o mac o ungal species was asso-
cia ed wi h lowe pH alues. A ela i ely lowe pH alues we e ound in
he Alemsaga and Banja o es s. This suppo s he indings o Puang-
somba e al. (2010) and Zhang e al. (2016) who epo ed ha highe
pH le els nega i ely in luenced ungal communi y s uc u e, p obably
because a highe pH es ains he expansion o ungi and he p oduc ion
o spo oca ps. Howe e , he species om he Ta agedam o es s showed
excep ional o dina ion owa ds a ela i ely highe end poin o he pH
g adien . This migh be associa ed wi h hei adap abili y o he species
o highe pH alues in he soil. We also ound ha CEC and EC a e
explana o y ac o s o mac o ungal composi ion. Al hough he exac
ole ha he CEC and EC play in mac o ungal composi ion and spo o-
ca p p oduc ion is no ully unde s ood, C ab ee e al. (2010) obse ed
ha ungal species ichness was low, pa icula ly when he CEC was
high. This is p obably because he CEC and EC in luence nu ien
a ailabili y, soil pH, and soil eac ions o o he amelio an s in he soil
(Ogeleka e al., 2017). The majo i y o species in ou o dina ion we e
di ec ed owa ds plo s wi h low CEC and EC alues. This is p obably also
because soils wi h a high CEC a e less suscep ible o he discha ge o
base sa u a ion as base sa u a ion is an impo an ac o in he dis i-
bu ion o mac o ungal species. Base sa u a ion indica es he p opo ion
o si es occupied by basic ca ions such as Ca
2+
, Mg
2+
, Na
+
, and K
+
(Zheng e al., 2019). These elemen s a e i al in many physicochemical
p ocesses, such as pho osyn hesis (He e al., 2017) and, hus, can a ec
plan pho osyn hesis and, hence, he amoun o ca bon ha is a ailable
o ungi in he soil (Shi e al., 2014).
O ganic ma e also appea ed o be an impo an ac o associa ed
wi h he composi ion o mac o ungi in he s udied o es s. This is likely
because ungi ypically ex end hei mycelia a he soil–li e in e ace
(Boddy e al., 2009) and, he eby, o ganic ma e in luences mycelial
ou g ow h and ne wo k o ma ion (Zaka ia and Boddy, 2002). O ganic
ma e also in luences he ungal communi y h ough i s impac on he
wa e -holding capaci y o soil and nu ien a ailabili y (Ha ing on,
2003). Thus, a high le el o o ganic ma e accumula ion implies a high
le el o mac o ungal assembly, pa icula ly o sap ophy ic species.
Howe e , he accumula ion o o ganic ma e in some cases may also
a ac he ec omyco hizal ungi as some o he ECM species can be
bene i om o ganic ma e decomposi ion in a simila manne o ee-
li ing sap o ophs; ha is, as a sou ce o educed C compounds o sup-
po me abolism (Lindahl and Tunlid, 2015). Ni ogen was also co e-
la ed wi h he composi ion o ungal species. This inding is in line wi h
hose o K anabe e e al. (2009) and Re e chon e al. (2010), who
epo ed ha ungi assembly inc eased along soil N g adien s. This is
because ni ogen can in luence he o ma ion o mycelium in he soil and
play a ole in spo oca p o ma ion (T udell and Edmonds, 2004).
Fu he mo e, many ungal species can adap o mo e ni ogen- ich si es
(K anabe e e al., 2009; Toljande e al., 2006). In addi ion o he
edaphic a iables, he analysis also showed a signi ican ole o max and
minimum empe a u e on he composi ion o mac o ungal composi ion.
This may be due o he ac ha he mycelium o he ungal species is
mo e eadily a ec ed by a mosphe ic changes (Sale ni e al., 2002),
being mo e supe icial speci ically o hose sap o ophs species ha
cons i u e mainly he communi y composi ion o ou s udied o es s.
Fu he mo e, he empe a u e can play ole in nu ien cycling p ocess
(Geng e al., 2017). An inc ease in empe a u e gene ally acili a es he
decomposi ion o ganic ma e in he soil and accele a es he a ailabili y
o nu ien s. Thus, he ungal species likely a e esponding o his con-
di ion and o m dis inc communi ies, pa icula ly o he ungi ha a e
soil depende as a subs a e (Nicol´
as e al., 2019).
5. Conclusions
We in es iga ed he di e si y and composi ion pa e n o mac o ungi
in h ee chu ch o es s in No he n E hiopia o help us o unde s and he
s a egies equi ed o he managemen and conse a ion o hese
emnan D y A omon ane o es s and he c ucial oles played by ungi
in he managemen and p o ec ion o hese o es sys ems. The di e si y
indexes and communi y composi ion o mac o ungi in he s udy a eas
we e in luenced by si e condi ions, including ascula plan di e si y
and soil e ili y g adien s. F om he analysis on ungi and plan di e si y
indices, we can see ha he species ichness o mac o ungi is indepen-
den o he di e si y and ichness o ascula plan communi ies. In ou
analysis, no co ela ions we e obse ed o ichness, sugges ing ha
ichness o ascula plan s canno be used as a p oxy o mac o ungi
ichness. Howe e , a posi i e co ela ion was ound be ween he wo
communi ies o hei di e si y Shannon index, indica ing he ee
iden i y migh be used as a ac o o mac o ungal di e si y as he e was
a highes ungal di e si y alue in o es s wi h he highes le el o ee
di e si y alues. Unsu p isingly, mac o ungal communi ies as a whole
we e in luenced by edaphic a iables gi en ha edaphic a iables a e
he main ac o s a ec ing mycelial de elopmen and, hence, he p o-
duc ion o spo oca ps by di e en mac o ungal species. Thus, he p o-
mo ion o ascula ee di e si y in agmen ed o es sys ems by
en ichmen plan ings o assis ed na u al egene a ion managemen
sys ems would o e sui able habi a s wi h a iable mic oclima es ha
should assis mac o ungal species di e si y and p oduc i i y in he
agmen ed D y A omon ane o es s o E hiopia. In addi ion, he e ec s
o he a o emen ioned managemen p ac ices on soil e ili y should be
aken in o conside a ion owing o he impo an ela ionship be ween
D. Alem e al.
Fo es Ecology and Managemen 496 (2021) 119391
13
edaphic a iables and mac o ungal composi ion in hese o es s. Fo es s
and si es showed a signi ican in luence in he composi ion o he ungal
communi ies associa ed. The e o e, conse a ion o a highe numbe o
hese agmen ed o es s, can lead o he conse a ion o a highe ugal
ichness in an o e all landscape scale. Ou su ey also e ealed he
p esence o aluable edible mac o ungal species belonging o he T i-
choloma, Suillus, and Te mi omyces gene a, which could po en ially be
ma ke ed and, hence, could p o ide supplemen a y incomes o o es -
dependen local people and o es manage s. Thus, we sugges ha he
p oduc ion o aluable non- imbe o es p oduc s such as wild mush-
ooms should be inco po a ed in o managemen and conse a ion s a-
egies o hese agmen ed o es sys ems. Mo eo e , he applica ion o
he baseline in o ma ion p o ided in his s udy could assis o he
coun ies ha a e acing simila o es conse a ion issues due o
de o es a ion and o es agmen a ion.
CRediT au ho ship con ibu ion s a emen
Demelash Alem: In es iga ion, Da a cu a ion, W i ing - o iginal
d a . Ta ek Dejene: Supe ision, In es iga ion, W i ing - e iew &
edi ing. Juan And ´
es O ia-de-Rueda: Concep ualiza ion, Me hodol-
ogy. Pablo Ma ín-Pin o: Supe ision, Concep ualiza ion, Me hodol-
ogy, W i ing - e iew & edi ing.
Decla a ion o Compe ing In e es
The au ho s decla e ha hey ha e no known compe ing inancial
in e es s o pe sonal ela ionships ha could ha e appea ed o in luence
he wo k epo ed in his pape .
Acknowledgemen s
We would like o exp ess ou g a i ude o he people in ol ed in he
ieldwo k. This esea ch was suppo ed by he p ojec s SUSTIFUNGI_ET
(Sus ungi_E h: 2017/ACDE/002094) and MYCOPROED_ET (Myco-
p oed_E h: 2019/ACDE/000921) unded by he Spanish Agency o In-
e na ional De elopmen and Coope a ion. This s udy was also co-
unded by he Spanish Minis y o Educa ion and Cul u e unde a Sal-
ado de Mada iaga g an ag eemen , n◦PRX17/00315.
Appendix A. Supplemen a y ma e ial
Supplemen a y da a o his a icle can be ound online a h ps://doi.
o g/10.1016/j. o eco.2021.119391.
Re e ences
Aba e, D., 2014. Wild mush ooms and mush oom cul i a ion e o s in E hiopia.
WSMBMP Bull. 11, 1–3.
Aba e, D., 2008. Wild mush ooms in E hiopia and ou ea ing habi . In: Na ional
Mush oom Con e ence, Facul y o Science, Addis Ababa Uni e si y, May. Addis
Ababa, E hiopia, pp. 14–15.
Abe e, F., Bele e, Y., Ke alew, A., So omessa, T., 2017. Ca bon s ock o Banja o es in
Banja dis ic , Amha a egion, E hiopia: An implica ion o clima e change
mi iga ion. J. Sus ain. Fo . 36, 604–622. h ps://doi.o g/10.1080/
10549811.2017.1332646.
Abiyu, A., Mok ia, M., Geb eki s os, A., B ¨
auning, A., 2018. T ee- ing eco d in E hiopian
chu ch o es s e eals successi e gene a ion di e ences in g ow h a es and
dis u bance e en s. Fo . Ecol. Manage. 409, 835–844. h ps://doi.o g/10.1016/j.
o eco.2017.12.015.
Adeniyi, M., Adeyemi, Y., Odeyemi, Y., Odeyemi, O., 2018. Ecology, di e si y and
seasonal dis ibu ion o wild mush ooms in a Nige ian opical o es ese e.
Biodi e si as J. Biol. Di e s. 19, 285–295. h ps://doi.o g/10.13057/biodi /
d190139.
Ae s, R., Van O e eld, K., No embe , E., Wassie, A., Abiyu, A., Demissew, S., Daye, D.
D., Giday, K., Haile, M., TewoldeBe han, S., Teke ay, D., Teklehaimano , Z.,
Binggeli, P., Decke s, J., F iis, I., G a ze , G., He my, M., Heyn, M., Honnay, O.,
Pa is, M., S e ck, F.J., Muys, B., Bonge s, F., Healey, J.R., 2016. Conse a ion o he
E hiopian chu ch o es s: Th ea s, oppo uni ies and implica ions o hei
managemen . Sci. To al En i on. 551–552, 404–414. h ps://doi.o g/10.1016/j.
sci o en .2016.02.034.
Alem, D., Dejene, T., O ia-de-Rueda, J.A., Geml, J., Ma ín-Pin o, P., 2020. Soil Fungal
Communi ies unde Pinus pa ula Schiede ex Schl dl. & Cham. Plan a ion Fo es s o
Di e en Ages in E hiopia. Fo es s 11, 1109. h ps://doi.o g/10.3390/ 11101109.
Alemu, H., Debela, N., Mamuye, A., Jano, M., 2012. Wild Edible Plan s by Gumuz T ibes
as nu i ious and sus ainable ood s u s in he Me ekel and Kamashi Zones o
Benishangul-Gumuz Regional S a e. An assessmen s epo submi ed o Tiku e
Legumuz Hizb Lima Mahib , Assosa E hiopia.
Ande son, M.J., 2001. A new me hod o non pa ame ic mul i a ia e analysis o
a iance. Aus al Ecol. 26, 32–46. h ps://doi.o g/10.1111/j.1442-
9993.2001.01070. pp. x.
An onin, V., 2007. Monog aph o Ma asmius, Gloiocephala, Palaeocephala and Se ulipes
in T opical A ica. Fungus Fl T op A 1, 177.
Aynekulu, E., Ae s, R., Denich, M., Negussie, A., F iis, I., Demissew, S., Boehme , H.J.,
2016. Plan di e si y and egene a ion in a dis u bed isola ed d y A omon ane
o es in no he n E hiopia. Folia Geobo . 51, 115–127. h ps://doi.o g/10.1007/
s12224-016-9247-y.
Bah am, M., Peay, K.G., Tede soo, L., 2015. Local-scale biogeog aphy and
spa io empo al a iabili y in communi ies o myco hizal ungi. New Phy ol. 205,
1454–1463. h ps://doi.o g/10.1111/nph.13206.
Bekele, M., Lemenih, M., 2008. Pa icipa o y Fo es Managemen Bes P ac ices, Lesson
Lea n and challenges encoun e ed: The E hiopian and Tanzanian expe iences. Fa m
A ica/SOS-Sahel, E hiopia.
Bi hane, E., Geb emedihin, K.M., Tadesse, T., Hailema iam, M., Solomon, N., 2017.
Exclosu es es o ed he densi y and oo coloniza ion o a buscula myco hizal
ungi in Tig ay, No he n E hiopia. Ecol. P ocess. 6, 33. h ps://doi.o g/10.1186/
s13717-017-0101-9.
Blum ield, T., Xu, Z., 2003. Impac o ha es esidues on soil mine al ni ogen dynamics
ollowing clea all ha es ing o a hoop pine plan a ion in sub opical Aus alia. Fo .
Ecol. Manage. 179, 55–67. h ps://doi.o g/10.1016/S0378-1127(02)00485-1.
Boa, E., 2004. Wild edible ungi: A global o e iew o hei use and impo ance o
people, Non-wood Fo es P oduc s N
o
17. FAO, Rome.
Boddy, L., Hynes, J., Bebbe , D.P., F icke , M.D., 2009. Sap o ophic co d sys ems:
Dispe sal mechanisms in space and ime. Mycoscience 50, 9–19. h ps://doi.o g/
10.1007/s10267-008-0450-4.
Boe ae e, M., Honnay, O., Mullens, N., Vandeke kho e, K., De Kee smaeke , L.,
Thomaes, A., Jacquemyn, H., 2018. The impac o spa ial isola ion and local habi a
condi ions on coloniza ion o ecen o es s ands by ec omyco hizal ungi. Fo .
Ecol. Manage. 429, 84–92. h ps://doi.o g/10.1016/j. o eco.2018.06.043.
Bone , J.A., Fische , C.R., Colinas, C., 2004. The ela ionship be ween o es age and
aspec on he p oduc ion o spo oca ps o ec omyco hizal ungi in Pinus syl es is
o es s o he cen al Py enees. Fo . Ecol. Manage. 203, 157–175. h ps://doi.o g/
10.1016/j. o eco.2004.07.063.
Bone , J.A., Gonz´
alez-olaba ia, J.R., A ag´
on, J.M.D.E., 2014. Mush oom p oduc ion as
an al e na i e o u al de elopmen in a o es ed moun ainous a ea. J. M . Sci. 11,
535–543. h ps://doi.o g/0.1007/s11629-013-2877-0.
Bonge s, F., Tenngkei , T., 2010. Deg aded o es s in Eas e n A ica: In oduc ion. In:
Bonge s, F., Tenningkei , T. (Eds.), Deg aded Fo es s in Eas A ica: Managemen and
Res o a ion. Ea hscan L d., London, UK, pp. 1–18.
Bouyoucos, G.H., 1951. A Reclama ion o he Hyd ome e o Making Mechanical Analy.
Soil. Ag o. J. 43, 434–438.
B und e , M., 2002. Coe olu ion o Roo s and Myco hiza o Land Plan s. New Phy ol
275–304.
B und e , M., 2004. Di e si y and classi ica ion o myco hizal associa ions. Biol. Re .
79, 473–495.
Bu gess, N.D., Hales, J.D.A., Ricke s, T.H., Dine s ein, E., 2006. Fac o ing species, non-
species alues and h ea s in o biodi e si y p io i isa ion ac oss he eco egions o
A ica and i s islands. Biol. Conse . 127, 383–401. h ps://doi.o g/10.1016/j.
biocon.2005.08.018.
Calhim, S., Halme, P., Pe e sen, J.H., Læssøe, T., B¨
assle , C., Heilmann-Clausen, J., 2018.
Fungal spo e di e si y e lec s subs a e-speci ic deposi ion challenges. Sci. Rep. 8,
5356. h ps://doi.o g/10.1038/s41598-018-23292-8.
Cas a˜
no, C., Alday, J., Lindahl, B., Ma ínez de A ag´
on, J., S, D.-M., Colinas, C., Pa lad´
e J,
P.J., Bone , J., 2018. Lack o hinning e ec s o e in e -annual changes in soil ungal
communi y and di e si y in a Medi e anean pine o es . Fo . Ecol. Manage. 424,
420–427.
Chen, J., Xu, H., He, D., Li, Y., Luo, T., Yang, H., Lin, M., 2019. His o ical logging al e s
soil ungal communi y composi ion and ne wo k in a opical ain o es . Fo . Ecol.
Manage. 433, 228–239. h ps://doi.o g/10.1016/j. o eco.2018.11.005.
Chen, X.-L., Wang, D., Chen, X., Wang, J., Diao, J.-J., Zhang, J., Guan, Q.-W., 2015. Soil
mic obial unc ional di e si y and biomass as a ec ed by di e en hinning
in ensi ies in a Chinese i plan a ion. Appl. Soil Ecol. 92, 35–44. h ps://doi.o g/
10.1016/j.apsoil.2015.01.018.
Chen, Y., Yuan, Z., Bi, S., Wang, X., Ye, Y., S enning, J.-C., 2018. Mac o ungal species
dis ibu ions depend on habi a pa i ioning o opog aphy, ligh , and ege a ion in a
empe a e moun ain o es . Sci. Rep. 8, 13589. h ps://doi.o g/10.1038/s41598-
018-31795-7.
Chia ucci, A., D’au ia, F., De dominicis, V., Lagana, A., Pe ini, C., Sale ni, E., 2005. Using
Vascula Plan s as a Su oga e Taxon o Maximize Fungal Species Richness in
Rese e Design. Conse . Biol. 19, 1644–1652. h ps://doi.o g/10.1111/j.1523-
1739.2005.00202.x.
Cla ke, K.R., 1993. Non-pa ame ic mul i a ia e analyses o changes in communi y
s uc u e. Aus al Ecol. 18, 117–143. h ps://doi.o g/10.1111/j.1442-9993.1993.
b00438.x.
Collins, C.G., S ajich, J.E., Webe , S.E., Pombubpa, N., Diez, J.M., 2018. Sh ub ange
expansion al e s di e si y and dis ibu ion o soil ungal communi ies ac oss an
D. Alem e al.
