Tree invasions and biosecurity: eco-evolutionary dynamics of hitchhiking fungi

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. AoB PLANTS www.aobplan s.ox o djou nals.o g V 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 002AoB PLANTS www.aobplan s.ox o djou nals.o g V 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 AoB PLANTS www.aobplan s.ox o djou nals.o g V 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 004AoB PLANTS www.aobplan s.ox o djou nals.o g V 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 Bu gess e al. — Fungal in luence on ee in asions AoB PLANTS www.aobplan s.ox o djou nals.o g V 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. Acknowledgemen s We hank William Duns an o discussion on in oduc ion o ec omyco hiza o Aus alia, and Kay Howa d o he ca e ul edi o he manusc ip . Li e a u e Ci ed Anagnos akis SL. 1987. Ches nu bligh : The classical p oblem o an in oduced pa hogen. Mycologia 79:23–37. 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