Native Soilborne Pathogens Equalize Differences in Competitive Ability Between Plants of Contrasting Nutrient-Acquisition Strategies

RESEARCH REPOSITORY

This is the author’s final version of the work, as accepted for publication following peer review but without the publisher’s layout or pagination. The definitive version is available at:

http://dx.doi.org/10.1111/1365-2745.12638

Albornoz, F.E., Burgess, T.I., Lambers, H., Etchells, H., Laliberté, E. and Power, A. (2017) Native soilborne pathogens equalize differences in competitive ability between plants of contrasting nutrient-acquisition strategies. Journal of Ecology, 105 (2). pp. 549-557.

http://researchrepository.murdoch.edu.au/id/eprint/32564/

diversity and plant pathogens Running headline:Soil-borne [email protected]). *Corresponding author: Canada H1X 2B2, Est,Montréal, Québec de Montréal,4101Sherbrooke 6150,Australia WA Murdoch, Murdoch University, 6009,Australia WA Crawley (Perth), Laliberté Felipe E.Albornoz* This article isprotected Allrights bycopyright. reserved. doi: 10.1111/1365-2745.12638 thisversionandthe between lead todifferences been through the copyediting, typesetting, and proofreading which may pagination process, forpublicati accepted This articlehasbeen 3 2 1 Editor :AlisonPower Article type Date:27-May-2016 Accepted Revised Date:04-May-2016 :19-Nov-2015 Received Date AcceptedInstitut de recherchebiologie en végétale, Département de sciences Université biologiques, Scien CentreforPhytophthora SchoolofPlantBiology, TheUniversity Article Native soil-borne pathogens equalise 1,3 between plants ofcontrasting nutrient-acquisition strategies : Standard Papers Papers :Standard 1 , I. Burgess Treena Albornoz, F. E. ce and Management, SchoolofVe and Management, ce 2 (+61 8 6488 5912; 86488 (+61 , Hans Lambers , Hans of Western Australia, 35 Stirling Highway, Australia, 35Stirlingof Western on and undergone full peer review buthasnot review undergone fullpeer on and

Version of Record. PleaseVersion cite thisarticle as differences incompetitive ability 1 , HannahEtchells terinary andLife Sciences, 1 , Etienne This article isprotected Allrights bycopyright. reserved. Accepted Article Summary 5. 4. 3. 2. 1.

thus supporting the hypothesis proposing a trade-off between highly efficient P efficient highly between proposingthus supporting atrade-off thehypothesis competitive ability between seedlings ofcontrasting nutrient-acquisition strategies, Synthesis cluster-rooted species may mostefficientbeat the acquiring growth-limiting the againstacquisition andresistance root presence of presence grown inthe ECMplantswere onlyECM fungi, when significant butthiswas Growth ofECMplants positively was correl growth competitors. non-mycorrhizal ofthe reduced the of presence the in better ECMspecies were and non-mycorrhizal When of presence the alone,biomassof grown seedlings When were plant groups. defence, and that thisequalises differencescompetitive in ability between these two hi between ECM plants,duetoatrade-off native ( pathogens ofnativesoil-borne or absence alone andincomp hyperdiverse shrublands wegrew glasshouse experiment, Ina associations. (ECM) other P-acquisiti other plantspeciesusing many with co-occur Proteaceae However, P. acquiring at efficient very are Proteaceae insouth-west shrublands In hyperdiverse scarce. remains atrade-off ofsuch evidence empirical However, diversity high in plant could helpexplain agai might trade-off impoverished ecosystems phosphor been hypothesisedthatefficient reducing differences incompetitive ability co-occurring between plantIt species. has contributetothe Soil-borne pathogenscan Phytophthora . Ourstudy thatnativesoil-borne shows Phytophthora. Phytopthora species are more detrimental to Proteaceae than co-occurring co-occurring than Proteaceae to detrimental aremore species Phytophthora

, while ECM species were unaffected by thispathogen by were unaffected , whileECMspecies Proteaceae and ECM plant species from ECMplantspeciesfrom and Proteaceae than in its absence, because its absence, because in than pathogens. We found that non-mycorrhizal foundthatnon-mycorrhizal We pathogens. ern Australia, non-mycorrhizal cluster-rooted non-mycorrhizal ern Australia, nutrient-impoverished ecosystems. severely us (P)acquisitionby plantsinP- on strategies, such as ectomycorrhizal as ectomycorrhizal such on strategies, ghly efficient Pacquisitionandpathogen ghly efficient maintenance of local plantdiversity by oflocal maintenance Phytophthora Phytophthora etition with each other, and in the presence and inthepresence etition witheachother, ated with percentcolonisation ated by root nst resistance to root pathogens. This nst resistancetorootpathogens. non-mycorrhizal plants was reducedin plantswas non-mycorrhizal planted together, ECM plants grew together, ECMplants planted pathogens equalised differences in pathogens equaliseddifferences spp.). We hypothesisedspp.). We that Phytophthora Phytophthora .

This article isprotected Allrights bycopyright. reserved. Accepted 2006;Bagchi,Lewis & enabling Freckleton competitiveplantspecies topersist(Bell, less building uplarger populationsaround)plant speci low hostspecificity promotecan plant species still diversity by beingdetrimental more to(or 1970;Connell1971; Lewis Freckleton &(Janzen andgrowth survival seedling conspecific reducing pathogens, ofhost-specific accumulation of density an increasing when occurs effect) Nega 2012). (Terborgh plantspecies occurring (Wurst dependence Laliberté mechanisms(M diversity different through toplantspecies Plant pathogens contribute can et al. increasing isreceiving plant speciesdiversity ro although apotential given region, species ina of role about theecological pathogens (Cahill against thoseintroduced damage toplan cause significant pathogens can introduced Hovmøller 2002).These & 1987;Brown (Anagnostakis from otherregions Article ad In pathogenscausing the 2012). cases, many globe many (Fisher the plantbiodiversitythreatening biomesacross andproductivity in Most plantpathogens detrimentalimpact have Introduction phosphorus, ectomycorrhizas, Key

words: 2010b; planthyperdiversi the to themaintenanceof suggestpathogens. Ourresults thatnativ ECMsp butthatco-occurring resource, et al. Determinants ofplantcommunity Determinants dive

Laliberté 2015). For example, this can occur thiscanoccur example, For 2015). et al. et al. 2015), or by reducing differences reducing 2015),orby 2015). native soil-bornepathogens that Phytophthora ills & Mordecai2011; Bever 1998;Gilbert2002; et al. conspecific individuals leads to the local local the to leads individuals conspecific , Proteaceae, soil nutrient availability. soilnutrientavailability. , Proteaceae, attention in recent years 2002;Bagchi (Gilbert inrecent attention s on both natural and managed ecosystems, ecosystems, bothnaturalandmanaged s on tive density dependence (i.e. Janzen-Connell Janzen-Connell (i.e. density dependence tive coexistence andthus coexistence ecies are better defended against root against root defended better are ecies ts that havenotevol ts that e soil-borne pathogens and ECM contribute andECMcontribute pathogens e soil-borne ecline in plant diversity have been introduced beenintroduced inplantdiversity have ecline 2008). By contrast, very little isknown very little 2008).By contrast, le of pathogens to the maintenance of local of tothemaintenance ofpathogens le es showing competitive ability, higher thus 2006). On the other hand, pathogenswith 2006). Ontheotherhand, through conspecific negative density conspecific negative through ty in severely P-im inseverely ty rsity and structure, Cluster roots, and structure,Cluster rsity in competitive ability betweenco- in have co-evolved withplant co-evolved have ved specific defences defences ved specific promotelocalplant poverished ecosystems. ecosystems. poverished et al.

2012). On the other hand, clusterroots 2012). Ontheotherhand, at effective acquisition strategy ishighly successful inthese (Lambers habitats et al. suchascluster strategies non-mycorrhizal with contrasting nutrient-acquisiti Rossel & Bui 2015).Plantcommunitiesinkwong especial nutrient-impoverished, severely insouth-we Soils inthekwongkan shrublands yet hasnot studied. shrublands been as seasonally-dry native pathogens interac onplant pathogens inmaintainingplantdiversity. Howeve fore atropical in diversity seedling reduced tree Bagchi Fordiversity. example, Lewis& Terborgh 2012), 2006; (Freckleton rainforests fortropical exists coexistence species plant to contributing ofpathogens Evidence toroot thus making themmoresusceptible Ptendtobeshor highly atacquiring efficient androotdefen efficiency between P-acquisition coexistence inthese hyperdiverse communities, that thismight and be related toa trade-off This article isprotected Allrights bycopyright. reserved. Accepted Article2015). Laliberté awiderangeofnutrient exhibit Laliberté1994; phosphorus (P)(Huston often occur onold,strongly weathered, very infertile soilsthat are particularly lowin Highly-diverse plant such communities asrainforests tropical Mediterranean and shrublands plantco understand howhighly-diverse fo ofsoil-bornepathogens role the ecological lo maintenanceof can bothcontributetothe effects These different Press & Scholes2010a). 2015). In particular, non-mycorrhizal, clus non-mycorrhizal, In 2015). particular,

et al. (2015) surmised that(2015) lowsoilPavailabilitycontributes toplant -acquisition strategies (Lambers -acquisition strategies (Lambers et al. tions and diversity in other highly-diverse ecosystems such ecosystems in otherhighly-diverse tions anddiversity on strategies, suchasdifferent on strategies, (2014) experimentally showed that applying fungicides fungicides applying showedthat experimentally (2014) et al. are fine short-lived roots (Shane fineshort-lived are mmunities are maintained (Laliberté (Laliberté mmunities aremaintained ly with respect toP(Laliberté ly withrespect et al. acquiring different forms of P (Lambers forms ofP(Lambers different acquiring roots (Lamont, Hopkins & Hnatiuk 1984;Zemunik&roots (Lamont, Hnatiuk Hopkins pathogens (Newsham, Fitter & Watkinson 1995). & Fitter (Newsham, pathogens 2006; Zemunik 2006; cal plant diversity 2002).Determining cal plant (Gilbert which are renowned for their high plant for their arerenowned which t-lived, poorly thinepidermis, t-lived, witha lignified, r plant species coexistence should helpus should speciescoexistence r plant 2013). Some ofthese 2013). plant communities stern Australia are old, strongly-weathered and old,strongly-weathered Australiaare stern st in Belize,st pointing offungal toa role ces against pathogens. Indeed, rootsthatare Indeed, againstpathogens. ces ter-rooted Proteaceae are particularly are particularly Proteaceae ter-rooted of pathogens are not mutually exclusive and notmutually exclusive pathogensare of r, to our knowledge, theecologicalroleof toourknowledge, r, kan are renowned for high plantdiversity forhigh renowned kan are et al. et al. mycorrhizal associationsand mycorrhizal 2015), because thisnutrient- 2015),because 2014;Zemunik et al. et al. , 2015; Viscarra , 2015;Viscarra et al. 2004; Lambers 2004; 2015). 2015). et al. et al. 2006,

This article isprotected Allrights bycopyright. reserved. Accepted non-myco of competitive superiority reduce the native ofdifferent presence the by affected negatively severely more are Proteaceae mycorrhizal aimed we Specifically, species. occurring in hyperdiverse by reducing shrublands differences incompetitive abilityamong theseco- Proteaceae andnon-mycorrhizal Myrtaceae ECM between ofinteractions outcome the affect hownative evaluated In we presentstudy the roles areunknown. of species native On theotherhand,sout 2004). & Cochrane Crane 40% approximately south-west botanicalprovince (Cahill 1900s intheearly Australia sinceitwasintroduced oomycete south-western Australian Oomycetes are considered tobe ecologically im thishas however, toourknowledge efficient between atrade-off because of and of non-mycorrhizal promote thecoexistence Article1972; Strobel& Sinclair and che Smith 2015),butalsoconferphysical notonly to contribute fungi ectomycorrhizal forms ofPinP- different considered tobe nutrient-acquisition strategy, but In associati 2015). particular, Aust impoverished south-western P- hyperdiverse, in with Proteaceae coexist strategies P-acquisition contrasting with species soil nutrient,P,intheseshrublands (Lambe roots mightAlthough bethemosteffi cluster (Laliberté P-acquisition in high efficiency et al. 2006), and thought to behighly 2006),andthought susceptible Phytophthora Phytophthora cinnamomi Phytophthora strains than ECM species; ii) the presence of native ofnative presence the ii) species; ECM than strains 1991). Therefore, it is possible itispossible 1991). Therefore, impoverished soils(Lambers shrublands (Laliberté shrublands (Laliberté ons with ectomycorrhizal (ECM) fungi are another common (ECM)fungi another are ons withectomycorrhizal (Rea (Rea ralian shrublands (Laliberté ralian shrublands Rands has caused de Randshascaused never been tested experimentally. experimentally. tested been never et al. P acquisition and defence against pathogens; against pathogens; and defence P acquisition 2011;Simamora to test the following i)non- hypotheses: to testthe et al. rs, Martinoia & Renton 2015), many & plant other rs, Martinoia Renton2015), plant nutrient acquisition (Smith, Anderson & plantnutrientacquisition(Smith, Anderson cient strategygrowth-limiting atacquiring cient the mical defences against mical defences 2015). et al. rrhizal Proteaceae over Proteaceaeover rrhizal portant soil-bornepathog mycorrhizal plantsinP-impoverishedsoils, to soil-borne pathogens as a trade-off of atrade-off as soil-bornepathogens to less efficient than cluster roots at acquiring acquiring at roots cluster than efficient less h-western Australia al of the native flora is susceptible (Shearer, (Shearer, susceptible is flora native of the 2015). On one hand, the invasive 2015).Ononehand,the et al. that soil-bornepathogens might vastating damage tonativeflorain damage vastating et al, 2008b). However, 2008b).However, et al. et al. 2008). For example, inthe example, 2008).For 2013), whose ecological ecological 2013),whose Phytophthora 2014;Zemunik root pathogens (Marx root pathogens(Marx ECM species;andiii) ECM so harbours several Phytophthora ens inhyperdiverseens speciescould et al. will

three ECM species from the Myrtaceae ( Myrtaceae the from species ECM three This article isprotected Allrights bycopyright. reserved. cluster roots( plantspecies selectedsix We selection Species Barbetti 2012;Ryan You & overse 2hoursperday pasteurisation at80°Cfor sieved all through a plotswas Then, 2-mmsieve. sterilised bulksoilfrom via triple-steam pointswithin layer randomly-positioned atthree kg pl bulksoilfromeach ~10 collected apart. We 6inTu five plotsintheoldeststage(stage Hayes studies(Laliberté 10m×plotsfromearlier Using ofpermanent anetwork Soil collection (2015). Laliberté & (2012) andTurner description ofsoilpr inagl islocated chronosequence 2013, 2014;Hayes andhasbeende 10km over approximately al. species andfunctional are severe stage this oldestchronosequence in south-westernAu located chronosequence, oldestchronose focused onthe Our study Study areaandsiteselection Materials growthplants. ofECM increase higherECM rootcolonisationgreater willoffer against protection

Accepted Article dunechronosequence Bay 2015).TheJurien et al.

and 2014; Turner & Laliberté 2015; Zemunik Laliberté & 2014;Turner 2015; Banksia attenuate Banksia attenuate

Methods et al. operties along the entire chronosequence can be found in Laliberté in found can be entire chronosequence alongoperties the diversity (Laliberté 2014; Turner & Laliberté 2015;ZemunikLaliberté & 2014; Turner et al. for our experiment: three non-mycorrhizal Proteaceae that form thatform Proteaceae threenon-mycorrhizal experiment: for our R. Br., obal biodiversity hotspot(Myersobal biodiversity 2012). 2012). B. menziesii Calothamnus quadrifidus Calothamnus quence stage of the Jurien Bay dune Bay dune oftheJurien stage quence rner & Laliberté 2015) that were atleast1km Laliberté& 2015)thatwere rner et al. scribed indetail elsewhere (Laliberté ly P-impoverished and host the highest plant P-impoverishedandhostthehighest ly stralia (30.29° S, 115.04° E), because soils from because soilsfrom 115.04°E), (30.29°S, stralia 2014; Turner & Laliberté 2015; Zemunik spans over two million years ofpedogenesis overtwomillion spans each plot. Soils were air-dried, mixed and each mixed plot.Soils wereair-dried, ot. Soils were collected from thetop30-cm ot. Soilswerecollectedfrom ven days, following previous studies(Fang, ven days,previous following R.Br. and et al. 2015), we collected soilsfrom 2015),wecollected Hakea ruscifolia R.Br., et al. Phytophthora et al. , 2000).Adetailed 2015). This 2015). Eucalyptus et al.

, and hence , andhence Labill.), and et al. 2014; 2012, et al. et et

mycelium tofully colonise the medium growing my with actively juice wasinoculated made a sterilemedium Briefly, and cooljarloo(CLJO100), taxon isolatedfromkwon four lesscommonspecies kwongkan (Simamora vegetation of selectedfivestrains We Phytophthora treatments. forall soils triple-pasteurised into transplantation during Proteaceae) mg ofinoculum added50 their roots.We of microorganisms, notraces thatthisinoculumcontai Despite thefact forle visuallyfungal inoculum.We assessed theirroots,cut months. Then,weharvested and growninnon-ster germinated species were ECM ofeach fungi, 20individuals ECM by becolonised would species To ensureECM fungiInoculum withectomycorrhizal Phytophthora insert to space seedlings leave to to next inserted were long) 10cm diameter, cm month oldseedlings wereL transferredAttime ofplanting, into1 pots. small plastic tubes (2 (Zemunik of exception the with This article isprotected Allrights bycopyright. reserved. Accepted Article todtiana P. rosacearum F.Muell. and et al. inoculum preparation inoculumpreparation inoculumtoallowforinfestationof 2015). Seedlings were germinated in were 2015).Seedlings (HSA1658). Inocula were produced as described in Aghighi inAghighi asdescribed Inocula produced were (HSA1658). E. asterocarpa Eremaea asterocarpa Phytophthora P. damage by pathogens were observed in these seedlings and seedlings inthese wereobserved damage pathogens by ofvermiculite(with0.1% taxon kwongan (TCH009), (TCH009), kwongan taxon et al. which can also form arbuscular mycorrhizal association association mycorrhizal arbuscular form also can which 2013); ning ECM fungi likely also contained other fungining alsocontained likely ECM representing different native species isolated from from isolated species native different representing with ECM fungi under each seedlingwith ECMfungi (ECMand each under and mixed them,andusedtheserootsasECM and mixed

Hnatiuk). Myrtaceae species are solely ECM solely ECM are species Myrtaceae Hnatiuk). sions and damping-off symptoms onroots. sions anddamping-offsymptoms gkan vegetation during routine surveys, gkan routine vegetationduring Phytophthora arenaria Phytophthora celium and left for 8–12 weeks at20ºCforthe andleftfor8–12weeks celium ile soils collected from the field forfour soils collectedfromthefield ile the rhizosphere of growing of plants. the rhizosphere triple-steam pasteurised soilandone- triple-steam pasteurised P. millet seed) wetted withV8 milletseed)wetted aff. rosacearum Phytopthora Phytopthora (CBS 127950)and (HSA2350) et al. inoculation (2015). P.

This article isprotected Allrights bycopyright. reserved. in re-hydrated roots were Later, separately. remove soilparticles. Sh carefullyfrom roots.Rootswere washed ove intheglasshouse, monthsofgrowth After four Post-harvest analyses monthsintheglasshouse grown forfour were Seedlings capacity. field 70%to to weekly twice and then capacity field to watered for nine seedlings of usedasamplesize We arenaria either: i)“– weeks insterile soilswithinoculum withECM with ECMfungi asdescribed mg ofinoculum 50 with wasplanted plant ECM Each species. plant ECM and Proteaceae per pot.Thiswasdone a totalofthreeseedlings L oneseedlingin a2.7 of pottogetherwith germination. Oneindividual Furthermore, Phytophthora Given that Experiment 2 growth pot-bound. becoming four for a glasshouse grown in Seedlings were capacity. field to70%of weekly and thentwice capacity, tofield pots werewatered “ of (mix following treatments: i)“– soils withinoculum ECM f quantities (w/w). Afterseedlings were transplant Colonised mediaofstrains Experiment 1 Accepted Article+ P.arenaria P. , P. taxon cooljarloo, P. Phytophthora taxon cooljarloo, taxon

E. asterocarpa strains 1,inthis inExperiment arenaria ”. We used a sample size of10seedlings asamplesize used ”. We didnotshowtobemoredetriment oots and roots were oven-dried for three days at 60 ºC and weighed ºCandweighed at60 days forthree oots androotswereoven-dried ” (double autoclaved inocula), or ii) “+ orii)“+ inocula), ” (doubleautoclaved Phytophthora P. and of either ECM species ( of eitherECMspecies above. After seedlings were tr seedlings were above. After Phytopthora P. taxon kwongan, taxon ungi, we added 5 g of (0.4% of g of added 5 ungi, we taxon kwongan, taxon H. ruscifolia ” (double autoclaved inocula), ii) “+ ii)“+ autoclavedinocula), ” (double and then harvestedas 1. per experiment , except , except water at 5°C for 48 hours, and cleared usingcleared at 5°Cfor48hours,and water B. menziesii this experiment. Three days later, pots were potswere Threedays later, this experiment. r a 1-mmsieve immediately after harvesting to experiment all stra were not used in this experiment, duetopoor notusedinthisexperiment, were months and then harvested to avoidroot andthenharvested to months seedlings were harvested by severing shoots severing by harvested were seedlings fungi, we inoculated each pot with5g of pot fungi, each weinoculated P. in order to maximise ordertomaximise in ed and grown for two weeks in 1 L in1 two weeks potswith and grownfor ed P. aff. rosacearum and aff.rosacearum P. aff. rosacearum and aff.rosacearum C. quadrifidus

arenaria for this experiment. Three days later, later, Threedays forthisexperiment. and one seedling of of andoneseedling al toplantgrowththan theother ansplanted and grown fortwo ansplanted and , were pooled inequal , werepooled total soil weight) each of the each of totalsoilweight) ins were pooled. pooled. ins were Phytophthora or the interaction between the interactionbetween E. todtiana P. rosacearum P . rosacerarum B. attenuata Phytophthora ” (mix of ” (mix ) waspotted ), oriii) ). for P. ”

This article isprotected Allrights bycopyright. reserved. to when plantsexposed Accepted forallthree Indeed, biomass 0.0001; Fig. 1). of presence Phytophthora – the in grown those with compared species, Proteaceae in biomass seedling lower All seedlings survived during thisexperiment. Thetwo+ Experiment 1 Results using lm(). models linear regression Relationship between rootcolonisation and ECM seedling biomass calculated was byfitting from the“multcom using glht() thefunction (Zuur Inform using theAkaike model wasevaluated (Suppor wasused structure appropriate variance a centredonzero assumptions (i.e.residuals inspected visuallycheck to model assumpti from effect) “pot” asrandom Article in thefunctiongls() modelswith mixed-effect andi species inbiomassbetween differences were andfigures conducted were All analyses Statistical analyses each sample. counted for ma the netwhen and/or Hartig at200 (Giovannetti & Mosse1980) Root colonisationby fungi deter was ECM lact (v/v) ina50% were placed we solutiontostain roots(Vierheilig used (v/v)ink-vinegar a 5% at hours (10%,w/v)for three potassium hydroxide et al.

2009). When a main term was significant, amaintermwassignificant, 2009).When Phytopthora Phytopthora treatment; by contrast, th Phytophthora (species × × (species the “nlme” package (Pinheiro the “nlme”package ntle was not conspicuous. At ntle wasnotconspicuous. oglycerol mixture for storage. mixture oglycerol Phytophthora × magnification, counting root were compared with plants grown in the – withplantsgrownin compared were e biomass of ECM plant species was unaffected by the the by unaffected was species plant of ECM e biomass mined using the gridline intersect method gridlineusing the mined intersect ons. When agiven didnotmeetmodel ons. When model p” package (Hothorn, Bretz & Westfall 2008). Westfall Bretz & (Hothorn, p” package nd homoscedasticity), a revised modelwithan arevised nd homoscedasticity), noculum treatmentwere noculum Proteaceae species was reduced by 20to40% reduced was species Proteaceae ation Criterion (AIC) a Criterion(AIC) ation drawn in R (R Core Team, 2015). Statistical inR(RCoreTeam,2015). drawn experiment 1andlme() in experiment ting Information). The quality of thenew Information). of Thequality ting treatment interaction; F 90 °C in a water bath. Following clearing, 90°Cinawaterbath. post hoc Phytophthora et al. least 150totalroottipswere Tukey tests were performed were performed Tukey tests 2012). Residuals were 2012).Residuals et al. tipswithanECMmantle nd likelihood ratiotests nd likelihood tested using linear , 1998).Finally, roots treatments led to experiment 2(with experiment 2,10 =9.99; P

≤

biomass of treatment + the greater in was Proteaceae with competing species ECM ofboth biomass × (species of The effect Experiment 2 ( species three of these asterocarpa treatments for Indeed, thisre treatment (Fig. 3). colonisation inboth+ betweento We foundapositiverelationship root:shoot ratioof with that inthe – root:shoot ratioof treatments that compared inthe – with species, ECM + betweenthetwo observed were differences compared withthat inthe– was root:shootratio Proteaceae, This article isprotected Allrights bycopyright. reserved. Accepted Article × (species Root toshootratiodifferedsignificantly betw ( species Proteaceae + found between were differences + either ofthe by not observedtobeaffected Phytophthora , compared with that in the – the in that with compared Phytophthora Phytophthora B. menziesii ( Phytophthora Phytophthora P treatment ( E. asterocarpa C. quadrifidus

≤ 0.01; Fig. 3), while itwasnotsignificantinthe– 0.01;Fig. 3), Phytophthora E. todtiana C. quadrifidus P

≥ Phytophthora P was less inthe + 0.65; Fig. 1). Fig. 0.65; 1).

treatment interaction, F treatmentinteraction, treatment interaction; F ≥ P 0.18;Fig. 3).

≤ inoculum treatmentonfinalbiom Phytophthora 0.02; Fig. 1). On the other hand, biomass of ECM specieswas other hand,biomassofECM 0.02;Fig. Onthe 1). ( showed a lower root:shoot ratioinboth+ root:shoot showedalower was affected by by wasaffected ≤ treatment ( 0.05;Fig. 3),

lationship wassignificant forboth+ was only lower when exposed to when exposed wasonly lower 40 to 50% lower in thetwo+ 40 to50%lower Phytophthora treatments, although notforthe– treatments,although Phytophthora Phytophthora Phytophthora treatment ( P tal ECMseedlingECM root biomassand ≤ Phytophthora een treatments, but this varied among species amongtreatments, butthisvaried species een Phytophthora E. todtiana 0.05). There was no evidence thatthe was noevidence There 0.05). Phytophthora and the+ and 1,3 2,10 =17.58; =3.32; treatment ( treatment ( P

treatment compared withthat inthe – ≤ 0.01; Fig. 2). However, no 0.01;Fig. However, 2). ( P P. arenaria treatments ( treatments ( P

treatments (Fig. 2). treatments(Fig. 2). P ≤

ass varied among plant species plantspecies ass variedamong ≤ 0.01;Fig.and 3)

≤ Phytophthora 0.0001; Fig. 2). For all three 0.0001;Fig. 2).For P 0.0001;Fig.Final 4). P

≤ ≤ P. arenaria P. arenaria Phytophthora 0.01; Fig. Conversely, 0.01; 4). 0.01; Fig. whilethe 0.01; 2); Phytophthora treatments forECMor treatments Phytophthora Phytophthora P Phytophthora P

≥ ≥ 0.08;Fig. No 1). 0.7;Fig. For 2). treatment Phytophthora compared compared E. soilforany

species. Additionally, this increase in ECM plant biomass in presence of presence of in biomass plant ECM in increase this Additionally, species. competitive can modulate borne pathogens native of presence the in gain higher biomass showed species ECM Proteaceae, with competing to soil-bornepathogensthan This supportsthecontentionthatnon-mycorrhizal ofnative presence the ~26% in by reduced was gain biomass ofProteaceae that found we our hypotheses, soils,P(Lambers,limiting resourceinthese Ma growth- the acquiring in effective most are species Proteaceae because non-mycorrhizal competition between species withthese twonutrient-acquisition strategies,presumably ECMplantspecies, than soil-borne pathogens showthatnon-mycorrhizal Overall, ourresults Discussion ≥ different the in Proteaceae competing of andbiomass Myrtaceae There were nostatisticallycorrelationssignificant between of ECMrootcolonisation 0.04; Fig. notsignificant whileitwas inthe– 6), inthe+ andseedling biomass between ECMrootcolonisation Finally, both treatments inroot:shoot + the quadrifidus This article isprotected Allrights bycopyright. reserved. Phytophthora and Root toshootratiovariedamong species among ( treatments Phytophthora Accepted 0.8). Article Phytophthora Phytophthora and C. quadrifidus treatmentinteraction,F treatment ( E. todtiana Phytophthora Phytophthora P treatment ( treatment species than in their absence, suggesting that the presence of native soil- of native presence the that suggesting absence, their in than species = 0.2; Fig. 4). Fig.= 0.2; 4). ratio were found for either of the Proteaceae ( oftheProteaceae either found for ratio were P ≤ was almost twice as highinthe – and ECM species (Laliberté ECMspecies(Laliberté 0.05;Fig. thatof 4); P

E. todtiana ≤ species, while the growth of ECM species was not affected. wasnotaffected. species, whilethegrowthofECMspecies 0.001; Fig. 5). By contrast, no differences between By nodifferences 0.001;Fig.contrast, 5). 1,3 =18.48; interactions between ECM and Proteaceae Proteaceae betweenECM and interactions showed a significant positive relationship Phytophthora and thistranslatedand of intoa relaxation Proteaceae were more susceptible tonative susceptible more were Proteaceae rtinoia & Renton 2015). In agreement with Inagreement rtinoia & Renton2015). Phytophthora cluster-rooted species are moresusceptible are cluster-rootedspecies P B. attenuata

≤ et al. 0.0001;Fig. Root:shootratioof 5). 2015). Furthermore, when 2015).Furthermore, treatments (species × (species treatments Phytophthora was not observed to differ wasnotobservedtodiffer Phytophthora treatment ( Phytophthora P = 0.1; Fig. 5). Fig.= 0.1; 5). Phytophthora Phytophthora P treatment than in

treatment ( ≥ 0.64;Fig. 6). treatments ( was P

C. ≤ P

This article isprotected Allrights bycopyright. reserved. Accepted ecosystems. these in coexistence species plant to contribute further might which biota soil associated and their this possibility,as thisprocesscouldleadto (Laliberté hypothesised plant species,ashasbeen ofsoil-bornepathogen promote thelocalbuild-up study,Inwe soil-borne pathogens. this Phytophthora not thatwedid hand, thefact (Lam species ectomycorrhizal than strategy systems, P-impoverished dominate inseverely Laliberté proposed by P-ac Results supportthetrade-offbetween contra canhave different nutrient-acquisition inoculatedwith previously chestnut seedlings chestnutseedlings ofnon-mycorrhizal root size seedlings by that theinoculationofchestnut native of these presence the by affected Articlegrowth. Ontheotherha a reductioninoverall For the Proteaceae here, tested while the notkilled native by coexistence inhyperdiverse vegetation (Laliberté helpusbe will research that for future nutrient- contrasting of plantspecies occurring pathogen-mediated nega how 2001). Quantifying Gibson (e.g., and Myrtaceae among Proteaceae notallowustoquantifydesign does howpa contrastingamong nutrient-acqui of plantspecies maintenance highly-diverse of ecosystems by reducing differencescompetitive in ability that Our study suggests ECMfungi. by defence ECMrootcolonisati positively with correlated treatments suggests that coexistence suggests thatcoexistence treatments et al. (2015). This trade-off could pa (2015).Thistrade-off find differences in growth among in find differences tter understandmechanisms did not evaluate if non-mycorrhizal Proteaceae Proteaceae ifnon-mycorrhizal did notevaluate Phytophthora quisition efficiency quisition efficiency bers, Martinoia & Renton 2015). Ontheother Martinoia & Renton2015). bers, negative plant-soil feedback between Proteaceae Proteaceae between feedback plant-soil negative thogens modulatedensit P. cinamomi sting responses to the same native pathogen. responsestothesamenative sting nd, growth of ECM plants was notnegativelygrowth ofECMplantswas nd, ECM fungi. Our results show howplantswith resultsshow fungi. Our ECM on, suggesting inpathogen animportantrole acquisition strategiesacquisition is despite having a more despite having amore by 43-48%, while not affecting growth of whilenotaffecting 43-48%, by soil-borne pathogens may contribute tothe may soil-bornepathogens et al. tive density dependence varies among co- among varies density dependence tive sition strategies. However, our experimental ourexperimental sition strategies. However, s to a greater extent than ectomycorrhizal ectomycorrhizal than extent agreater to s et al. et al. among Proteaceae is not modulatedby isnot among Proteaceae 1999; Connolly, Wayne & Bazzaz 1999;Connolly,Bazzaz & Wayne species. Branzanti Branzanti species. 2015). 2015). Future studies shouldevaluate 2015).Future studies or rtly explain why Proteaceae donot Proteaceae why explain rtly P. cambivora Phytophthora and pathogen defence and pathogen Proteaceae species inthe+ species Proteaceae of plant species ofplantspecies y-dependent competition efficient P-acquisition efficient an important avenue animportant et al. reduces leaf and leaf reduces species, there was there species, (1999)showed This article isprotected Allrights bycopyright. reserved. attention as ECMfungi couldstillenhance uptake, nutrient which might be reflected not in nutrients, buttoprotectECM pl the fungi main function inthese ofECM P-impoverished soilsmay toscavenge notbe fromthepresentstudy,This, togethercolonisation beingwith ourresults that suggests high. younge impoverished soilscomparedwiththatin biomass hyphal external (2016) showedhow Phytophthora wasfoundbetween other hand,norelationship plat onagar cultured together species when showed detrime 2004). Apreviousstudy shown(Branzanti as previously defence, inpathogen role ofECMfungi of ECM rootcolonisation,butonly inthepresence In bothexperiments, seedling biomass ofECMplant species positively was with correlated (Dodd finerootsofboths and where plantnutrients layers, soil superficial in place takes primarily acquisition nutrient andplant system, this comp becauseplant matureplants, relevant for our results tolonger-term inter plants.As perennial woody lived, slow-growing mature than rather usedseedlings experiment glasshouse Our shrubland. seasonally-dry plantsinahyperdiverse, of thisforwoody Mills & toourknowledgethisis Bever 1998),but andw ecosystems inother has beenreported coexistence plant Pathogen-mediated resources. P scarce accessing of terms in species ECM co-occurring of that affecting not while species suggest ourresults b). Hence, that fu biosynthesis of 1972)andthe (Marx barrier pathogens totheirhos from fungi protection offer Like waslower. species ofProteaceae biomass of presence the in greater gain was biomass plant ECM Proteaceae, with together planted When

Accepted Article Phytophthora et al. 1984). 1984). treatment.Ina recent study fromthe compared with that when grown in the absence of pathogens; conversely, conversely, pathogens; grownin theabsenceof withthatwhen compared actions between mature plants.We mature actions between ants against Th rootpathogens. Phytophthora ntal effects ofECMfungi ontwo ntal effects es (Branzanti, Rocca & Zambonelli 1994).Onthe Zambonelli Rocca& (Branzanti, es ith herbaceous plants (Burdons & Chilvers1974; (Burdons plants ith herbaceous eedlings and mature plants are concentrated concentrated are plants andmature eedlings plants, because the studied species are long- are species studied becausethe plants, of mycorrhizal fungi was very low inP- fungi wasveryof mycorrhizal ngicides (Duchesne, (Duchesne, ngicides etition is mainly for belowground resources in resources etition ismainlyfor belowground wise, several studies have shown how ECM howECM haveshown studies several wise, ECM species, thus conferring an advantage to advantage an species,thusconferring ECM biomass andECMcolonisationinthe– biomass can affect growth of non-mycorrhizal plant growth non-mycorrhizal of canaffect such, care must be taken when extrapolating when extrapolating mustbetaken care such, r and P-richer soils, despite mycorrhizal root mycorrhizal andP-richersoils,despite r t by several mechanisms, such as a physical such asa physical mechanisms, by several t the firststudy toshowempiricalevidence Phytophthora same shrublands studied here, Teste here,Teste same shrublandsstudied is hypothesis deserves further deserves is hypothesis . Thissuggestsanimportant believe that our results are ourresultsare believethat Peterson & Ellis1988a; Peterson et al. Phytophthora 1999; Whipps 1999;Whipps et al.

This article isprotected Allrights bycopyright. reserved. fungipathogens andmycorrhizal may strongly studies onplantinteractions aswellplan persistence their hosts.Ourresults of highlightconsidering theneed for soilmicrobiota in impoverished soils,ECMfungi important are (Laliberté defence andpathogen efficiency P-acquisition between trade-off a is there that hypothesis shrublands. in thesehyperdiverse strategies a key roleincoexisten root pathogensmay play competition among seedlings ofcontrasting strategies. nutrient-acquisition We surmise that In showhownativ conclusion, ourresults onse potential effects any and treatment.Hence, intr wouldhavebeen otherpathogens However, bypotential contamination othe fungi. Hence, species withECMfungi. Thisapproach lik and Myrtaceae Proteaceae both inoculate to roots fresh weused Notwithstanding, themselves. than fungi, rather ECM species isprovidedby ECM rootcolonisationresults, cluster-rooted non-mycorrhizal, Phytophthora aboutthehost- noinformation now, therewas speciesgeneralist are inAustralia (Scott al. E. todtiana of butalso root:shoot ratioofnotonly Proteacecae both plant families, despite notaffecting gain total biomass ECMplant of species.Indeed, that nativespeciesof resultsshow Finally, our 2015). seedling biomass, butinincreased leaf nutrient concentrations (Smith,Anderson & Smith 2006), and hence reduce theroot:shootra reduce 2006),andhence Accepted ArticlePhytophthora et al. . Oomycetes cause damping-off andro damping-off cause . Oomycetes . However, Rea . However, 2015). We propose that in old, strongly-weathered and severely P- andseverely proposethatinold,strongly-weathered 2015).We compared with that of plants grown insoilwithout withthatofplantsgrown compared et al. provides some evidence that the resistance of ECM plant plant ECM of resistance the that evidence some provides Banskia (2011) reported that (2011)reported species. This observation, taken together withour Thisobservation,takentogether species. et al. e soil-borne pathogens can equalise plant can equalise pathogens e soil-borne ely introduced microorganisms otherthanECM microorganisms introduced ely t diversity and ecosystem functioning, since functioning, and ecosystem t diversity Moreover, we provide further evidence for the for evidence further weprovide Moreover, tio of their hosts.Many invasive tio of for pathogen defence and potentially the and potentially defence pathogen for 2009; Scott, Burgess & Hardy 2013), yet, 2009;Scott,Burgess until Hardy & 2013), r endophytes or pathogens cannot be discarded. cannot orpathogens endophytes r specificity of many native speciesof native ofmany specificity affect the outcome of plant competition. the outcomeofplant affect species plant ECM ofthe defence intrinsic an Phytophthora ce of plantswithdiffere ce oduced equally, irrespective of plant species species ofplant irrespective oduced equally, ECM plant species was lower in the presence inthepresence plantspecieswaslower ECM edlings wouldnothave ot damage (Cohen & 1986;Bell Coffey ot damage(Cohen P. arenaria were generalist pathogens for pathogensgeneralist were isoftenassociatedwith Phytophthora nt nutrient-acquisition nt nutrient-acquisition obscured our results. our obscured Phytophthora , except for , except et et

This article isprotected Allrights bycopyright. reserved. AcceptedBagchi, Gripenberg, S.,Gurr, R.E., R.,Gallery, LeBagchi, Gallery, R.E., R.,Swinfield,T., Bagchi, & Scholes,J.D. R.,Press,M.C. Anagnostakis, S.L. Chestnutblight (1987) Calv Scott,J.K., Aghighi, S.,Burgess,T.I., References Article DOI: doi:10.5061/dryad.515j4 at DRYAD: Data isavailable Data accessibility th that declare authors Finally, BECASCHILE/DOCTORADO (72130286),andthe fi Endowment toF.E.A. alsoacknowledge We theHolsworthWildlife Research and grantand T.B, toE.L. Slade Foundation research assistanceinsoil Lamoureux for Sébastian thankAgnes Simamoraforproducing We Acknowledgments Pathology pathogenicity of diversity and composition. diversity and Lewis,R.P. & Pathogens and O.T.(2014) 1269. densityovercompensating depe TestingFreckleton, theJa R.P.(2010b) seedlings. ofdipterocarp controlsurvival dependence Mycologia . DOI: 10.1111/ppa.12436 . DOI: 10.1111/ppa.12436 , 79 , 23–37. , 23–37. Phytophthora ey have no conflic ey no have Nature species fromdeclining ndence in a tropical tree. inatropical ndence , 506 Evolutionarydistance (2010a) history and

Phytophthora : the classical problem of an introduced pathogen. pathogen. problemofanintroduced : theclassical er, M. & Hardy, G.E.S.J. (2015) Isolation (2015) and G.E.S.J. er, M.& Hardy, wis, O.T., Gripenberg, S., Narayan, L.& S.,Narayan, Gripenberg, wis, O.T., collection. Funding was provided by a Hermon bycollection. Fundingwas provided a , 85–88. nzen-Connell mechanism: pathogens cause mechanism:pathogens nzen-Connell nancial supporttoF.E.A. through CONICYTnancial insect herbivores drive rainforest plant rainforest drive insect herbivores S.J., Narayan, L., Narayan, Addis,C.E.,Freckleton, S.J., t of interest. University of Western Australia. ofWestern University inocula, and Kenny Png and Png inocula,andKenny Rubus anglocandicans Ecology Letters Ecology Ecology Letters , 13 , , 51–59. 13 , 1262– . Plant This article isprotected Allrights bycopyright. reserved. Accepted & Dixon, Heddle,E.M.,Pate,J.S. Dodd, J., Connolly, Wayne, J., & Bazzaz, P. 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This article isprotected Allrights bycopyright. reserved. treatments: i)– Acceptedquadrifidus menziesii 1 Figure Figures andlegends Zuur, A.F., Leno, E.N., Walker, N.J., Laliberté,& plant nutrient- Lambers, B.L., E.(2015)Diversity H. of Zemunik, G.,Turner, Wurst, S.,Kaiser,N.,Nitzsche,Haase,J (2004)Prospectsandlimitations Whipps, J.M. ArticleA ne Bui, Rossel,R.A.&Viscarra E.N.(2015) A.,Wyss, U.& Piche, H., Coughlan, Vierheilig, E.(2015)Soildeve Laliberté, &B.L. Turner, Lambers,Laliberté, Teste, F.P.,H.,Au E., soil feedbacks of temperate trees. trees. temperate feedbacksof soil Tree diversity modifies dist Models andExtensions 1 acquisition strategies increases during long-term ecosystem development. pathogens. Australian soil. 64 fungi. arbuscular-mycorrhizal technique for in southwesternAustralia. under million-yearcoastal dunechronosequence during retrogression. ecosystem biomassandscavenging fungal Mycorrhizal , 1–4. , 5004–5007. Final biomass of non-mycorrhizal cluster-rooted (toprow; cluster-rooted non-mycorrhizal Final biomassof and , Eremaea asterocarpa Hakea Phytophthora Canadian JournalofBotany

Science of The Total Environment Total The of Science ruscifolia in EcologywithR , ii)“+ ) and ectomycorrhizal plantspecies(bottomrow; ) andectomycorrhizal Ecosystems ance-dependent effects onseed effects ance-dependent and Phytophthora Soil BiologyandBiochemistry Saveliev, A.A.& Smith,G.M.(2009) Ecology Eucalyptus todtiana Eucalyptus er, Y., Kramer, S. & Kandeler, E. (2016) & Kandeler, Kramer, S. er, Y., , ., Auge,H.,Rillig, M.C. 18 , lopment and nutrient availability along a2 along lopment andnutrientavailability 82 , . Springer, New York. York. . Springer,New w detailed mapoftotal w , 287–309. for mycorrhizas inbiocontrolofroot 96 , 1198–1227. Y. (1998) Ink and vinegar, a simplestainingInk (1998) andvinegar, Y. declines inphosphorus-impoverished soils declines Applied andEnvironmentalMicrobiology Applied , 1529–1539. , 1529–1539. ” (mix of ” (mix species-rich Mediterranean shrubland Mediterranean species-rich . DOI:10.1016/j.scitotenv.2015.09.119 ) grown under three inoculum three ) grown under P. taxon cooljarloo, taxon ling emergence but notplant– but emergence ling , Banskia & Powell, J.R. (2015) J.R. & Powell, 92 phosphorus stocksin phosphorus , 119-132. , 119-132. Mixed Effects Effects Mixed

attenuata Nature Plants P. Calothamnus taxon taxon , B.

, , cooljarloo, treatments: i)– withboth one ECMplantspeciesplanted quadrifidus B. 4 Figure relationship ( lines indicate significantrelationship ( for was 0.64and0.56,respectively; For species. plant ECM This article isprotected Allrights bycopyright. reserved. for+ onlyand biomasswere significant and ii)+ line; of mix Phytophthora Eucalyptus todtiana ( species plant ectomycorrhizal three in Figure 3 shown. are (CI) intervals confidence Meansand95% tests. letters indicate significant (P kwongan, taxon inoculum treatments:i)– Calothamnus quadrifidus B. Figure 2 shown. are (CI) intervals confidence Means and95% (P significant indicate kwongan,

menziesii Accepted Articlemenziesii Final biomass of non-myoccorh Final biomassof P. arenaria Relationships between ectomycorrhizal root ectomycorrhizal between Relationships ofnon-mycoRoot toshootratio P. P. and ) and ectomycorrhizal (ECM) plant species (bottom row; row; (bottom species plant (ECM) ) andectomycorrhizal and P. aff. rosacearum and rosacearum aff. P taxon kwongan, taxon (red circles and dashed line), ii) “+ anddashedline),ii) (redcircles taxon cooljarloo, taxon

≥ Phytophthora Eucalyptus todtiana P. 0.05). 0.05). Hakea aff. rosacearum and rosacearum aff. ). Seedlings were grown with th grown with ). Seedlings were (blue squares and solidline).Rela squares (blue ≤

0.05) differences among treatment among 0.05)differences ruscifolia C. quadrifidus , Phytophthora Eremaea asterocarpa ≤ orii)“+ 0.05) differences among treatme among 0.05)differences P. P. aff. P ) and ectomycorrhizal plantspecies(bottomrow; ) andectomycorrhizal taxon kwongan, kwongan, taxon . E. asterocarpa rosacerarum ) when grown together incompetitionwitheach other: ) whengrown rosacearum P , Phytophthora Calothamnus quadrifidus Calothamnus , ii)“+ P

R Phytophthora ≤ . izal cluster-rooted (top row; cluster-rooted izal 2 rrhizal cluster-rooted (top row; (toprow; cluster-rooted rrhizal 0.05), while dashed line indicates non-significant non-significant while dashedlineindicates 0.05), cluster-rooted species under twoinoculum speciesunder cluster-rooted was 0.41 and 0.53, respectively; for was0.41and0.53,respectively; rosacerarum Phytophthora and and ), andii)+ ), and Phytophthora , P. ree inoculum treatments: i)– ree inoculumtreatments: R ” (mix of ” (mix Eucalyptus todtiana colonisationandfinalseedling biomass 2 and+ aff. rosacearum and aff.rosacearum P was0.7and0.97,respectively.Solid tionships between ECM colonisation tionships betweenECM ), andii)+ . rosacerarum s based on post hoc Tukey tests. s basedonpost P. ” (mix of ” (mix P P. arenaria .

arenaria ” (green triangles andsolid triangles ” (green nts based on posthocTukey nts basedon arenaria , Eremaea asterocarpa P.

arenaria Calothamnus ). Different letters Banskia P. . Different letters . Different treatments forall taxon cooljarloo, Banskia ) grown under three underthree ) grown , P. P . taxon taxon rosacerarum

. Different attenuata E. todtiana

attenuata and and , P. ), , R

( relationship non-significant 0.05), whiledashedlineindicates quadrifidus + the This article isprotected Allrights bycopyright. reserved. kwongan, taxon Phytophthora inoculum treatments:i)– non-mycorrhizal grown togetherwithcompeting of twoECMspecies( Figure 6 areshown. intervals(CI) confidence trea among 0.05) differences kwongan, – both plant speciesplantedwith and and Figure 5 shown. are (CI) intervals confidence Means and95% (P significant indicate

Accepted ArticlePhytophthora Eucalyptus todtiana B. Phytophthora

menziesii Relationship between ectomycorrhizal root betweenectomycorrhizal Relationship ofnon-mycoRoot toshootratio P. and aff. rosacearum and rosacearum aff. ” (green triangles and solid line; mix of andsolidline;mix triangles ” (green , and ii) “+ , andii)“+ ) and ectomycorrhizal plant species (bottomrow; plantspecies ectomycorrhizal ) and E. todtiana P. aff. aff. treatment for both plant species, and were 0.87 and 0.38 for 0.87 and0.38 andwere forbothplantspecies, treatment Calothamnus quadrifidus Calothamnus ≤ rosacearum 0.05) differences among treatment among 0.05)differences ) grown together in competition with each other: one ectomycorrhizal ectomycorrhizal witheachother:one ) grown togetherincompetition Phytophthora Phytophthora , respectively. Solidlines indicate significant relationship ( tments based on post hoc Tuke tments basedonpost cluster-rooted plant speciesunder cluster-rooted plant P . and rosacerarum (red circles and dashed line), and ii)“+ anddashedline), (redcircles P ” (mix of ”(mix . rrhizal cluster-rooted (top row; (toprow; cluster-rooted rrhizal rosacerarum and ). Different). letters indicate significant (P cluster-rooted species, and exposed totwo exposed and species, cluster-rooted P. arenaria Eucalyptus todtiana colonisationandfinalseedling biomass P. arenaria ). R s based on post hoc Tukey tests. s basedonpost 2 y 95% and tests.Means values were significant only for , P P.

≥ , two inoculum treatments:i) two inoculum Calothamnus quadrifidus taxon cooljarloo, taxon P. 0.05). taxon cooljarloo, taxon ). Seedlings were were ). Seedlings Banskia C.

attenuata P. P taxon taxon P.

≤

This article isprotected Allrights bycopyright. reserved. Accepted Article