Mini-Re iew
SPECIAL ISSUE: E olu iona y Dynamics o T ee In asions
T ee in asions and biosecu i y: eco-e olu iona y dynamics
o hi chhiking ungi
T eena I. Bu gess
1,
*
2
, Caspa us J. C ous
2,3
, Be na d Slippe s
2
, Ja kko Han ula
4
and
Michael J. Wing ield
1,2
1
Cen e o Phy oph ho a Science and Managemen , School o Ve e ina y and Li e Science, Mu doch Uni e si y, Mu doch 6150, Aus alia
2
Fo es y and Ag icul u al Bio echnology Ins i u e, Uni e si y o P e o ia, P e o ia 0002, Sou h A ica
3
P esen add ess: Cen e o Ecology, E olu ion and En i onmen al Changes, Facul y o Sciences, Uni e si y o Lisbon, Campo
G ande, Lisbon 1749-016, Po ugal
4
Na u al Resou ces Ins i u e Finland, Na u al Resou ces and Biop oduc ion Uni , Van aa 01300, Finland
Recei ed: 31 May 2016; Accep ed: 26 Oc obe 2016; Published: 7 No embe 2016
Gues Edi o : Johannes Le Roux
Ci a ion: Bu gess TI, C ous CJ, Slippe s B, Han ula J, Wing ield MJ. 2016. T ee in asions and biosecu i y: eco-e olu iona y dynamics
o hi chhiking ungi. AoB PLANTS 8: plw076; doi:10.1093/aobpla/plw076
Abs ac . When non-na i e plan s each no el en i onmen s, hey ypically a i e wi h hidden mic obiomes. In
gene al, mos o hese hi chhike s emain on hei co-e ol ed hos s, some con ibu e o he in asi eness o hei
hos s, and a small numbe can unde go hos shi s and mo e on o na i e hos s. In asion success can a y depend-
ing upon he di e en ca ego ies o ungal associa es. When an in ade ee elies on a ungal mu ualism o su i e
in he new en i onmen , he e is a undamen ally lowe likelihood o ei he he ee, o he ungus, es ablishing no el
associa ions. In con as , pa asi ic hi chhike s could me ely use hei hos plan s o mo e h ough he landscape
and o become es ablished on new hos s (hos shi s). E idence sugges s he equency o hese hos shi s is low
and depends upon he ungal unc ional g oup. Howe e , epidemics caused by in asi e pa hogens in na i e ecosys-
ems ha e occu ed globally. Thus, elucida ing he po en ial o hidden non-na i e ungi o o m no el hos associa-
ions in a new en i onmen is impo an o biodi e si y conse a ion.
Keywo ds: Canke pa hogens; eco-e olu iona y expe ience; hos shi s; myco hiza; no el en i onmen s; oomy-
ce es; ee pa hogen.
In oduc ion
The nega i e consequences o plan in asions o ecosys-
em in eg i y a e well ecognized (Richa dson and Van
Wilgen 2004;Le Mai e e al. 2011). Howe e , plan s do
no a i e alone, and he e is an ex ensi e body o
li e a u e on he pes s and pa hogens being co-in oduced
wi h non-na i e lo a (B asie 2008;Wing ield e al. 2011;
Eschen e al. 2015;Ghela dini e al. 2016;Bu gess and
Wing ield 2016). The inad e en in oduc ion o pes s and
pa hogens is a global phenomenon s ongly d i en by he
* Co esponding au ho ’s e-mail add ess: bu gess@mu doch.edu.au
V
CThe Au ho s 2016. Published by Ox o d Uni e si y P ess on behal o he Annals o Bo any Company.
This is an Open Access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion License (h p://c ea i ecommons.o g/
licenses/by/4.0/), which pe mi s un es ic ed euse, dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal wo k is p op-
e ly ci ed.
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CThe Au ho s 2016 100
g owing global ade in li e plan s (Liebhold e al. 2012;
San ini e al. 2013). The e o e, unsu p isingly, he e a e
loud and on-going calls o ac ion o be e egula e plan
ade. These seek o ensu e bo h cos -e ec i e biodi e si y
conse a ion (Rouge e al. 2016) and commodi y p oduc-
ion (Han ula e al. 2014;Wing ield e al. 2015).
La gely igno ed in he global anspo a ion o
plan s a e he hidden mic oo ganisms, wi hin seed,
he plan s hemsel es, o he soil in which he plan s
we e g own. These so-called hi chhike s include hose
bene icial o hei hos s, hose de imen al, hose ha
may become na u alized wi hou causing ha m, and
hose nega i ely impac ing na i e plan s ia hos shi
e en s (Table 1). As discussed in his issue (Zenni e al.
2016), he e m “second genome”, ecognising he im-
pac o associa ed mic obes on he pheno ype o o -
ganisms, is also applicable o plan in asions, whe e
success is due no only o plan ai s, bu also hose o
he associa ed mic oo ganisms. Thus, hi chhike s, no
only ha e he abili y o p omo e he in asion success
o hei hos s in no el en i onmen s, bu hey po en-
ially also h ea en na i e ecosys em unc ioning
h ough hos -shi s.
Applying eco-e olu iona y expe ience (EEE) p inciples
o no el hos -mic obe in e ac ions (sensu Saul and
Jeschke 2015) can help p edic he in asion isk o hi ch-
hike s. This concep desc ibes he idea ha in oduced
o ganisms, no e ol ed o adap ed o he in oduced
landscape, could s ill possess he ecological and e olu-
iona y ai s allowing hem o es ablish bene icial bio ic
in e ac ions in he new en i onmen . An example o
ungi would be a pa hogen o an in oduced ee species
shi ing hos s on o a phylogene ically ela ed na i e ee
species in he new en i onmen . Con e sely, i he na i e
pa hogens do no ha e high EEE wi h he in oduced ee
species (e.g. compe i ion o p eda ion), he isk o
sp eading o hese non-na i e o ganisms (bo h ee and
pa hogen) inc eases conside ably (Facon e al. 2006;
Saul e al. 2013;Saul and Jeschke 2015). The in e ela-
ionship be ween he EEE o he ee hos and i s ungal
associa es emains unclea . Fo example, when a ee is
in oduced, bu ails o es ablish due o low EEE in he
no el en i onmen (e.g. low esis ance o a ack by na-
i e enemies), could hi chhike s s ill es ablish and sp ead
independen ly?
Fungi can be classi ied in o h ee b oad ophic le -
els: (1) pa ho ophs which ecei e nu i ion by ha ming
hos cells, (2) symbio ophs which ecei e nu i ion by
exchanging esou ces wi h hos cells and (3) sap o-
ophs which ob ain nu ien by b eaking down dead
hos cells (Tede soo e al. 2014). Howe e , wi hin hese
b oads ophic le els, he e a e many ca ego ies ( unc-
ional g oups o guilds) e lec ing ei he he pa o he
plan wi h which he ungus o ms an associa ion, he
ype o associa ion, o he ype o disease symp om i
causes (Nguyen e al. 2016). Thus, he e ms symbion ,
mu ualis o pa asi e, as used in he in asion biology
li e a u e (Richa dson e al. 2000;To chin and Mi chell
2004;Mi chell e al. 2006;Blackbu n and Ewen 2016),
do no ecognize he nuances o he di e en associa-
ions ungi ha e wi h hei hos s. He e we conside un-
gal unc ional g oups wi h en di e en li e his o y
s a egies, p o iding examples o hese ee associ-
a ed ungi (including oomyce es), hei anspo and
in oduc ion, and, using he EEE pla o m, p edic he
po en ial o he di e en g oups o es ablish and
sp ead in o he na u al en i onmen . In o de o in e -
oga e hese heo ies, he ocus o his communica ion
is on he global anspo o ungi (and oomyce es)
wi h long-li ed ee species, because hey ha bou all
hese g oups o ungal associa es. We ecognize he
impo ance o o he mic oo ganisms like bac e ia in
he in asion success o ees (Le Roux e al. 2016), bu
his will no be co e ed he e.
......................... ............................. ............................... ............................. ............................... ............................. ............................... .........
Table 1. Te minology used in his e iew.
Te m De ini ion
In oduced
1
A ecen ly in oduced species
Na u alized
1
A sel sus aining popula ion o an alien species (e idence o ep oduc ion)
In asi e
1
A sel -sus aining popula ion wi h e idence o sp ead o impac
Sp ead
1
An alien ungal species ha has sp ead ac oss a landscape
Impac
1
An in oduced ungal species ha causes disease on na i e lo a o ou compe es na i e ungi and h ea ens biological di e si y
Hos -shi An in asi e pa hogen mo ing om i s non-na i e hos o an na i e hos o isa e sa
Hi chhike s Fungi anspo ed wi h asymp oma ic plan s (co-in ade s), including pa hogens (pa asi es)
1
Based on de ini ions in common use (Blackbu n e al. 2011;Richa dson e al. 2011;Pe ey a 2016).
Bu gess e al. — Fungal in luence on ee in asions
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CThe Au ho s 2016
Mul iple Fungal Associa es: The Hidden
Th ea s o T ee In asions
Endophy es
Endophy ic ungi exis wi hin hos issues wi hou caus-
ing any ob ious symp oms (Saikkonen 2007;Rod iguez
e al. 2009). This g oup o ungi a e mos commonly
anspo ed along wi h hei hos s (Aschehoug e al.
2012), howe e , ela i ely li le is known ega ding he
di e si y and biology o endophy ic ungi, as many a e
uncul u able (Sun and Guo 2012). Al hough some endo-
phy es ha e been iden i ied, hei oles (in gene al, and
in in asion biology), speci ici y and abili y o mo e be-
ween hos species a e poo ly unde s ood. The e a e nu-
me ous ecen s udies using high h oughpu
sequencing echnologies conside ing he di e si y o en-
dophy e communi ies in woody plan s (e.g. Kemle e al.
2013). Howe e , o da e, hese s udies while highligh ing
he ex ao dina y di e si y o mic o-o ganisms ha -
bou ed wi hin a plan canno p o ide insigh s in o he
unc ion o hese endophy es.
The g oup o endophy es o which he mos is known
a e hose Class 3 endophy es (Rod iguez e al. 2009)
classi ied as la en pa hogens (Ca oll 1988), such as
membe s o he Bo yosphae iaceae (Slippe s and
Wing ield 2007;Phillips e al. 2013). No mally, hese
ungi a e benign, bu when hos plan s a e s essed, hey
can cause se ious disease p oblems (Slippe s and
Wing ield 2007). Whe e in ading ees a e plan ed a he
limi s o hei clima ic ange (and hus s essed), o as
he clima e changes, he nega i e impac o endophy ic
la en pa hogens on ee su i al will become impo an .
T ee endophy es in he Bo yosphae iaceae a e no ypi-
cally ansmi ed by seed, bu a e a he acqui ed ho i-
zon ally om he en i onmen as seedlings eme ge
(Bu gess and Wing ield 2002;Bihon e al. 2011a). Seeds
de eloping in nu se ies will hus be ee om hese com-
mon endophy es while hose ound benea h adul ees
acqui e hem soon a e ge mina ion (Ganley and
Newcombe 2006;Bihon e al. 2011b). Many species in
his g oup ha e wide hos anges and a e known o
mo e be ween hos species, om exo ics o na i es and
isa e sa. Fo example, in U uguay, he known
Aus alian eucalyp endophy e, Neo usicoccum eucalyp-
o um, has been isola ed om bo h in oduced eucalyp s
and na i e My ales (Pe´ ez e al. 2010). Simila ly,
Neo usicoccum pa um, a common endophy e o many
woody plan s is associa ed wi h ees in ho icul u e,
ees in plan a ions and na i e o es ees on many con-
inen s (Sakalidis e al. 2013). The endophy ic communi-
ies o Sibe ian la ch (La ix sibi ica) we e mos di e se in
loca ions whe e he ee species had been in oduced
cen u ies ago and no in he a ea o i s na u al
dis ibu ion, as i had acqui ed many associa es om he
new en i onmen (Kauhanen e al. 2006). Endophy es
ep esen a unc ional g oup o plan -associa ed hi ch-
hike s, which a e known o bo h mo e on o na i e ege-
a ion, howe e , in oduced plan s also acqui e
endophy es om he new en i onmen .
A buscula myco hizal ungi
Mos land plan s o m mu ually bene icial myco hizal
associa ions wi h ungi, and many o hese associa ions
a e obliga e. A buscula myco hizal ungi (AMF) ha e
b oad hos s’ anges (€
Opik e al. 2010) and global dis ibu-
ions. Biogeog aphy, clima e and plan communi y com-
posi ion can a ec he di e si y o AMF communi ies, bu
accoun o only a small amoun o he obse ed a i-
ance (Ki lin e al. 2011;€
Opik e al. 2013). The e is a con-
side able body o li e a u e conside ing he ole o AMF in
acili a ing in asion o exo ic plan species (Shah e al.
2009). Howe e , i is unclea whe he he AMF ha e been
in oduced wi h he in asi e plan species, o acqui ed in
he new en i onmen . Addi ionally, he success o he in-
asi e plan s may be in pa due o posi i e plan -soil bi-
o a eedback in he new en i onmen (Reinha and
Callaway 2006). In ac , i is conside ed highly likely ha
in oduced plan s would ind and acqui e new AMF pa -
ne s (Richa dson e al. 2000).
Ec omyco hizal ungi
Many ec omyco hizal ungi (EMF) display a deg ee o
speci ici y (Tede soo e al. 2014), and alien ees o en
ha e lowe species di e si y and unc ional di e si y o
hyphal o aging s a egies han hose o na i e ees
(Dickie e . al). In o es y, i has long been ecognized
ha he es ablishmen o pine plan a ions in he sou h-
e n hemisphe e (SH) equi ed an associa ion wi h an ap-
p op ia e EMF (Kessell 1927;Rayne 1934)asnoneo he
nume ous local sou he n hemisphe e EMF we e able o
p o ide app op ia e associa ions. Thus, when es ablish-
ing new nu se ies, seedlings we e o en inocula ed wi h
soil om es ablished nu se ies o heal hy plan a ions
(Kessell 1927). Consequen ly, almos all EMF ound asso-
cia ed wi h SH pine plan a ions ha e a na u al dis ibu-
ion in Eu ope o No h Ame ica (Duns an e al. 1988).
EMF no adap ed o eucalyp s ail o o m e ec i e my-
co hiza (Bu gess e al. 1994), and hus he es ablish-
men o eucalyp plan a ions in Asia was acili a ed
h ough he in oduc ion o ec omyco hizal ungi om
hei na i e ange in Aus alia (B und e e al. 1996). In
Spain, Aus alian EMF p omo e eucalyp in asi eness
(D
ıez 2005). Myco hizal ungi, as oo inhabi an s, can
only be anspo ed wi h hei hos s whe e he plan s a e
oo ed in soil o when he ungi ha e been delibe a ely
Bu gess e al. — Fungal in luence on ee in asions
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CThe Au ho s 2016 300
in oduced. Thus, hos -speci ic EMF a e o en equi ed o
success ul in asions by hei hos s in new en i onmen s
(Haywa d e al. 2015). Howe e , he e a e only a ew doc-
umen ed cases o in oduced species o EMF mo ing
on o na i e hos s, and he e ec s on na i e EMF emain
unknown (Nu~
nez and Dickie 2014).
Lea and shoo pa hogens
Many gene alis nec o ophic pa hogens a e oppo unis-
ic, en e ing lea es h ough wounds o li ing on exuda es
ound on lea su aces, and hese can be acqui ed in
he new en i onmen . Howe e , he e a e also nume ous
hos -speci ic lea pa hogens, o a leas in ec only
ela ed plan species (Pa ke e al. 2015). Fo example,
he bes -known pa hogens o plan a ion o es y ees
in he SH belong o he Te a osphae iaceae and
Mycosphae ellaceae (Hun e e al. 2011). They ha e been
mo ed globally wi h hei hos s o caugh up a e ini ial
es ablishmen (C ous e al. 2016), and can o en cause
se e e disease p oblems in plan a ions. Do his oma
needle bligh o pines can be a de as a ing disease in
SH plan a ions ollowing in oduc ion, bu he e is no
e idence o hos shi s on o na i e gymnospe ms
(Ba nes e al. 2004). Simila ly, one o he mos de as-
a ing olia pa hogens o eucalyp s, Te a osphae ia
nubilosa, has been dis ibu ed globally wi h i s hos s,
bu has ne e mo ed on o na i e ege a ion (Pe´ ez
e al. 2012). Many lea pa hogens ha e been co-
in oduced wi h hei hos s, and hey mus , in mos
cases, ha e been anspo ed on in ec ed plan ma e-
ial (Bu gess and Wing ield 2016). The hos speci ici y
o many o hese pa hogens implies i migh be possi-
ble o use hem as biological con ol agen s o in a-
si e plan species.
Rus pa hogens
Rus ungi a e usually highly hos speci ic; howe e , he e
a e also examples whe e he us s hemsel es ha e un-
de gone hos shi s e y soon a e in oduc ion
(Wing ield e al. 2015). A i id example o a ee us
pa hogen mo ing globally on plan p oduc s is he au-
oecious Puccinia psidii, he causal agen o he disease
known as my le us . This pa hogen o na i e My aceae
in Sou h Ame ica (Glen e al. 2007) was in oduced o
Aus alia in 2010 and quickly became in asi e as i
mo ed along he eas e n seaboa d whe e many na i e
My aceae ha e no esis ance (Ca negie e al. 2016).
Whi e pine blis e us , C ona ium ibicola, a he e oe-
cious species, is na i e o no he n Asia whe e he local
whi e pines a e esis an , bu apidly became in asi e on
na i e whi e pines ollowing i s in oduc ion in o no h
Ame ica (Maloy 1997). In bo h hese examples, he
pa hogen hos -shi s we e limi ed o phylogene ically e-
la ed hos s. Fo whi e pine blis e us , his was limi ed o
a ew species o i e needle pines, while o my le us ,
hos shi s we e much b oade , bu es ic ed o he am-
ily My aceae.
When a us ungus is highly hos speci ic, hey a e al-
ued biological con ol agen s o in asi e plan species.
Fo example, U omycladium eppe ianum,ahos -speci ic
us ungus o Acacia saligna, was in oduced and suc-
cess ully deployed o con ol he in asion o his ee in
ynbos landscapes in Sou h A ica (Wood and Mo is
2007). I should be no ed ha a pa hogen used as a bio-
logical con ol agen is i sel an in asi e o ganism.
Canke pa hogens
Canke pa hogens p oduce lesions on he s ems o ees
whe e hey ypically en e ia wounds, subsequen ly in-
ec ing he cambial issues. They include gene a and spe-
cies o ungi exhibi ing a ying deg ees o speci ici y
anging om highly hos speci ic o hose wi h ela i ely
wide hos anges (Sinclai and Lyon 2005). Because hese
ungi in ec and exp ess symp oms in olde plan s, i
migh be expec ed hey would a ely be anspo ed.
Howe e , canke pa hogens make up he la ges g oup
o in asi e o es pa hogens in Eu ope (San ini e al.
2013). The bes -known in asi e ee pa hogen is he de -
as a ing canke pa hogen C yphonec ia pa asi ica, he
causal agen o ches nu bligh in Eu ope and No h
Ame ica (Anagnos akis 1987). The pa hogen was in o-
duced om Asia, p obably Japan, whe e local ches nu
species a e na u ally esis an (Milg oom e al. 1996).
Fusa ium ci cina um causes pi ch canke o Pinus adia a
bo h in i s na i e ange in Cali o nia and in some egions
whe e P. adia a is plan ed as an exo ic. This pa hogen is
hough o o igina e om ela ed Pinus spp. in Mexico
(Go don 2006). Con e sely, while he e a e nume ous se-
ious canke pa hogens o exo ic eucalyp s such as
Ch ysopo he cubensis and Te a osphae ia zuluensis,
none o hese ha e been shown o exis in he na i e
ange o he genus indica ing ha hese pa hogens ha e
been acqui ed in he new en i onmen ia hos -shi s
(Bu gess and Wing ield 2016).
Wil pa hogens
Wil pa hogens en e he ascula sys ems o hei hos s
and hus dis up no mal wa e low leading o wil ing.
Mos wil pa hogens, especially hose o ees, equi e
wounds o in ec ion and many a e associa ed wi h in-
sec ec o s p oducing si es o ing ess (Wing ield e al.
2016). Wil pa hogens cause some o he bes -
documen ed in asi e diseases including he in amous
Du ch Elm Disease caused by Ophios oma ulmi and O.
Bu gess e al. — Fungal in luence on ee in asions
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CThe Au ho s 2016
no o-ulmi in Eu ope and No h Ame ica (B asie 1991;
Hubbes 1999). Though o be na i e o No h Ame ica
whe e Pla anus occiden alis is esis an , he in oduc ion
o Ce a ocys is pla ani o Eu ope has been de as a ing
o he na i e P. o ien alis (Ocasio-Mo ales e al. 2007).
Ce a ocys is imb ia a s.l. acommonwil pa hogeno
many c ops and plan a ion ee species, has a ely im-
pac ed in na u al ecosys ems, howe e , pos in oduc-
ion and na u aliza ion in Hawaii, i has now become a
majo pa hogen o he na i e ee species Me oside os
polymo pha (Mo enson e al. 2016). The mos common
pa hways o in oduc ion o hese pa hogens has been
wi h hei insec ec o s, many o which can be ound in
widely aded wood and wood p oduc s (Haack 2006;
Roques e al. 2010), o wi h con amina ed soil (Liebhold
e al. 2012).
Ro pa hogens
Ro pa hogens a e hose capable o in ec ing and o ing
he wood o heal hy ees. Because symp oms a e qui e
ob ious, and hey gene ally only de elop on olde ees,
hey a e no ob ious hi chhike s. Common gene a such
as Phellinus and Ganode ma a e dis ibu ed globally.
The e ha e been limi ed s udies on hei phylogeog a-
phy; howe e , isola ion-by-dis ance o sou he n hemi-
sphe e Ganode ma spp. has been demons a ed
(Moncal o and Buchanan 2008), indica ing ha many o
pa hogens o in asi e ees ha e no been anspo ed,
bu a he acqui ed om he new en i onmen .
P io o he ad en o molecula sys ema ics, he well-
known o (and soil) pa hogen, he honey ungus
A milla ia mellea, was conside ed o ha e a global dis i-
bu ion. I is now known ha he e a e many species o
A milla ia ha ing sepa a e con inen al dis ibu ions
(Coe zee e al. 2000). Howe e , he e is an in iguing ex-
ample o he in oduced A. mellea es ablishing and
sp eading in o pa ks and ga dens o he Sou h A ican
Cape Peninsula; his species was likely in oduced in he
1600s and i emains a p oblem oday (Coe zee e al.
2001). This in oduc ion mos likely occu ed ia he
anspo o po ed ees, whe e he pa hogen would
ha e been esiden in o en oo deb is.
The ee oo pa hogen He e obasidium annosum was
o iginal hough o ha e a b oad dis ibu ion ac oss he
no he n hemisphe e un il, as wi h A milla ia mellea,
molecula sys ema ics and de ailed ma ing s udies
e ealed he e we e se e al species wi h dis inc con i-
nen al dis ibu ions (Ga belo o and Gon hie 2013).
He e obasidum annosum has a na u al dis ibu ion in
No h Ame ica, bu was in oduced in o I aly (du ing he
second wo ld wa , p obably on wood packaging), whe e
i caused mo e damage on he na i e Pinus pinea (s one
pine) han he closely ela ed local pa hogenic species,
H. annosum. The con inuous spo e elease by he in a-
si e species compa ed wi h seasonal elease by he na-
i e H. annosum con ibu es o i s success (Ga belo o
e al. 2010). The No h Ame ican species is also hyb idiz-
ing wi h he local species esul ing in no el gene ic com-
bina ions wi h unp edic able pheno ypes (DAmico Mo a
e al. 2007;Gon hie and Ga belo o 2011). Thus, while
in oduc ions o o pa hogens occu ela i ely a ely,
whe e hey ha e been in oduced wi h wood packaging
o in ec ed soil, hey can na u alize and become in asi e.
Sap o ophs
Sap o ophic ungi de i e hei nu ien s om dead plan
ma e ial. They may ha e been anspo ed globally wi h
hei hos s, and because hey ha e limi ed nu i ional
needs and do no need o o e come he de ence s a e-
gies o li ing plan s, hey should eadily na u alize. This
g oup o ungi would ypically be conside ed as neu al
hi chhike s. One example is Cla h us a che i, a sap o o-
phic ungus na i e o Aus alia, now ound globally, wi h
i s mo emen mos p obably ia con amina ed soil. No
su p isingly, as a sap o oph, he e ha e been no ob ious
nega i e e ec s o ee heal h, wi h he only signs o
p esence due o he unpleasan odou i p oduces
(Desp ez-Lous au 2009). Simila ly, he sap ophy e
Fa olaschia caloce a, i s desc ibed om Madagasca ,
has since been epo ed in se e al coun ies including
I aly, Aus alia and New Zealand (Vizzini e al. 2009).
While he species has become wide sp ead, i is mo e
common on dis u bed si es, and is conside ed a poo
compe i o agains na i e wood-inhabi ing ungi.
In oduced and na u alized sap ophy ic ungi will mos ly
emain unde ec ed unless hey ob iously ou compe e a
na i e sap ophy ic ungal species.
Soil pa hogens (oomyce es)
Pa hogens in his ca ego y a e mo ed globally o new
en i onmen s in con amina ed soils. In en ional mo e-
men o soil wi h po ed plan s was e iden ly common in
he pas , o ins ance du ing ea ly coloniza ion and he
anspo o ui and o he ees. Al hough his is incom-
p ehensible in e ms o plan qua an ine, la ge ameni y
plan s con inue o be p oduced in one egion and ans-
po ed o ano he along wi h la ge olumes o soil
(B asie 2008). Soil pa hogens o en go unde ec ed be-
cause hey ail o p oduce ob ious symp oms du ing he
ea ly s ages o in ec ion. The mos commonly mo ed
ee pa hogens globally oday a e species o
Phy oph ho a (B asie 2008). They a e o en de ec ed in
asymp oma ic nu se y plan s (Miglio ini e al. 2015).
Mo eo e , hey may e en be anspo ed as hi chhike s
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CThe Au ho s 2016 500

on non-hos s. Fo example, in Aus alia, Phy oph ho a
cinnamomi is he mos de as a ing in oduced pa hogen
and a key h ea o he biodi e si y o he megadi e se
ege a ion in he sou h-wes bo anical ho spo (Da ison
and Shea e 1989). This pa hogen was acciden ally in o-
duced in o Aus alia on ole an o asymp oma ic hos s
used o es ablish o cha ds (Zen mye 1985) and i s
global dis ibu ion has p obably ollowed he same pa -
e n (Bu gess e al. 2016).
Fungal Associa es and T ee In asion
Success
The in oduc ion o mu ualis s, such as myco hizal
ungi, can con ibu e o he apid es ablishmen and
sp ead o he non-na i e ee species (Dickie e al.
2010;Zenni e al. 2016)(Table 2). He e, he high EEE
o he ee-hos in he no el en i onmen is di ec ly
in luenced by he p esence o he ungal mu ualis .
Howe e , i he ungus and he hos a e in oduced
sepa a ely, especially in o landscapes whe e he esi-
den lo a is phylogene ically dis inc (Pa ke and
Gilbe 2004), hen each may ha e low EEE. Based on
he e olu iona y dynamics necessa y o o m close
mu ualisms, co-in oduced ungal mu alis s should
ha e a undamen ally lowe likelihood o sp eading
on o na i e hos s. Howe e , a low likelihood o es ab-
lishmen and sp ead migh only be ue o hos -
speci ic mu ualis ic ungi, since mo e gene al o
oppo unis ic mu ualis ic ungi could ha e highe EEE
when in oduced in o egions whe e he esiden lo a
is phylogene ically simila . Endophy es, he g oup o
ungi mos likely o a i e as hi chhike s, a y in hei
in luence on ee in asions (Table 2). In ac , while
e y li le is known abou he bene i s o endophy es
in gene al, he sub-g oup known o be la en pa ho-
gens (Rod iguez e al. 2009) will cause disease in hei
hos s i hey a e in oduced in o unsui able
en i onmen s.
The success o ee in asions has o en been linked
o escape om i s na u al enemies (Keane and
C awley 2002), including plan pa hogens, all o which
would impac nega i ely on po en ial in asion
success (Table 2). Howe e , pa hogens usually ca ch-
up o hei hos s o e ime (C ous e al. 2016).
Addi ionally, na i e pa hogens can e en ually mo e
on o he in oduced ees. This is especially e iden i
componen s o he esiden lo a a e closely ela ed
o he in oduced ee species. Fo example, in
Eu ope, phylogene ically ela ed na u alized and na-
i e ee species sha ed simila numbe s o in e ac-
ions wi h simila ypes o ungal pa hogens (Vache
e al. 2010). Thus, se e al cen u ies a e in oduc ion,
he ne wo k has assimila ed he na u alized species,
bo h he ees and hei pa hogens. I could be a gued
ha phylogene ically dis inc ee species would ha e
a g ea e chance o becoming in asi e as hey would
a ac ewe na i e pa hogens.
...... ...... ........ ...... ...... ...... ........ ...... ........ .. .......... ........ .......... .......... ........ ........ ................
......................... ............................. ............................... ............................. ............................... ............................. ............................... .........
Table 2. Documen ed impac s o ungal hi chhike s on he success o ee in asions and on he in aded ecosys em.
Success o ee in asions Impac on in aded ecosys em
Posi i e
1
Nega i e
2
Nega i e
3
Neu al
4
A buscula myco hiza 1 1
Ec omyco hiza 1 1
Endophy es 11 1
Lea pa hogens 11
Canke pa hogens 111
Wil pa hogens 111
Rus pa hogens 111
Ro pa hogens 11
Oomyce es 111
Sap ophy es 1
1
Facili a e hos in asion.
2
Cause disease on in oduced hos and could limi hos in asion.
3
Unde go hos shi s and cause disease in new en i onmen .
4
Na u alize and in eg a e in o exis ing ne wo ks wi hou ob ious impac .
Bu gess e al. — Fungal in luence on ee in asions
006AoB PLANTS www.aobplan s.ox o djou nals.o g V
CThe Au ho s 2016
Hos -Shi s in New En i onmen s
In oduced ungi, especially hose emaining associa ed
wi h hei na u alized o in asi e hos s, o en ha e a neu-
al e ec on na i e plan communi ies (Table 2).
Howe e , he e a e documen ed examples o nume ous
in oduced plan pa hogens unde going hos shi s on o,
and impac ing on na i e ee species. Among hese pa h-
ogens, oomyce es and hose classi ied as canke o wil
pa hogens ha e had he g ea es impac s (Table 2).
In asi e pa hogens esul ing in no el disease associa-
ions a e gene ally hose anspo ed be ween egions
na u ally ha bou ing ela ed hos s in simila ecosys ems;
i.e. ac oss he no he n hemisphe e (Hansen 2008;Loo
2009;Bu gess and Wing ield 2016;Ghela dini e al. 2016;
Mu¨lle e al. 2016). These ungi ha e been co-in oduced
wi h hos s om a di e en con inen and ha e mo ed
on o ela ed species (naı¨ e hos s) ha ing li le esis ance
(Mu¨lle e al. 2016). They o en do no ad e sely a ec
he heal h o hei co-e ol ed hos s and ha e hus used
hei hos s’ EEE o es ablish as a pa hway o in asion. In
con as , disease ou b eaks in he SH end o be on ex-
o ic ee species, mos ly hose in oduced o o es y
(Wing ield e al. 2015;Bu gess and Wing ield 2016).
Disease ou b eaks o in asi e pa hogens in na i e eco-
sys ems in he SH a e a e, wi h he mos ex ensi e and
bes eco ded being he in asi e oomyce e, P. cinna-
momi. Oomyce es mos o en a i e as hi chhike s wi h
in ec ed plan ma e ial o wi h con amina ed soil.
The e o e, ea ly de ec ion and he apid e adica ion o in-
asi e plan s popula ions is c i ical because hei pe sis-
ence in he landscape may allow he ime o hidden
ungi o inc ease hei i ness on ela ed na i e species.
Conclusions
While nume ous ungi ha e been in oduced along wi h
non-na i e ees globally, mos appea o emain on hei
co-e ol ed hos s; some con ibu e o he in asi eness o
hei hos s and only a ew unde go hos -shi s on o na-
i e plan s. None heless, he hi chhike s o ee in asions,
he hidden non-na i e ungi, ep esen a neglec ed e-
sea ch ield, and his is in need o c i ical ed ess. I is
easy o see how hese ungi no only p omo e he suc-
cess o in asi e ees in he no el en i onmen s, bu due
o hos -shi po en ial, could inc ease he u u e in asion
deb in ecipien coun ies (Rouge e al. 2016).
The necessa y eco-e olu iona y cha ac e is ics o a-
cili a e in asion success can a y be ween di e en
g oups o ungal associa es and hei hos s. P edic ing
he likelihood o hi chhike s o ming no el in e ac ions in
he in aded ange mus , he e o e, depend s ongly on
he phylogene ic ela edness and EEE o in oduced
gene a o he lo a in he ecipien communi y (Pa ke
and Gilbe 2004;Saul e al. 2013;Saul and Jeschke
2015). The ac ha EEE p inciples can help explain bo h
ee and ungal associa e in e ac ions in he no el and
ela ed landscapes, sugges s much mo e a en ion
should ha e been aken his o ically o minimize he in-
oduc ion o ela ed plan s in o ecipien ecosys ems.
Wi h his knowledge, he global ade in plan s can, and
should, be be e egula ed.
Sou ces o Funding
This pape had i s o igin a a wo kshop on “E olu iona y
dynamics o ee in asions’’ hos ed by he DST-NRF
Cen e o Excellence o In asion Biology (C•I•B) in
S ellenbosch, Sou h A ica, in No embe 2015. Funding
o he wo kshop was p o ided by he C•I•B, S ellenbosch
Uni e si y ( h ough he o ice o he Vice Rec o :
Resea ch, Inno a ion and Pos g adua e S udies), and he
Sou h A ican Na ional Resea ch Founda ion (DVGR
G an no. 98182). Mu doch Uni e si y h ough he Si
Wal e Mu doch Scheme (awa ded o M.W.) suppo ed
he a el o T.B. o a end he wo kshop.
Con ibu ions by he Au ho s
All au ho s con ibu ed o discussions and subsequen
w i ing o he manusc ip .
Con lic o In e es S a emen
None decla ed.
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