JetfreyK. Stone,Departrnent oi Botanyand PlantPatho ogy OregonState Url vers ty Corva s Oregon9733i MarthaA. Sherwood,Department oi Geoogy Un versty of Oregon,ELrgene Oregon 97403 anal

GeorgeC. Carroll,Departrnent of B o ogy Unvers ty of Ofegon. Eugene O fegof 97403

CanopyMicrofungi: Function and Diversity

Abstract jmponaDr Microiungilrc rn iDcon\picuousbut !,,mp,,nenrnl rhehruu ul luLesr(.,|,,|ie\. \\rlhn canopres.mrcfotungr arc iound inhabimg li!ing.Lnd deadibliagc. bal.k.aDd $ oocl.and are al\o associakd\\'ith canop] epiphi lcs and arthropods.As cpiph)'teson loli.rge and t$ ig\. rnicr(rlungi scrle to concentfatedilure organic nulients. Biomass and nnnualproduction b)'.epiphyric lnic.o- iungi crn rpproach 500 kg,/h.rlDd may |epresenta signilicanr fbod fesourcelbr microarthropods.Saprorrophic decomposers contributeto in situ decomposilionofperched litter. Fungal cndophlte\ occupy hcal1h,"-.uslmptomatic foliagc and stems.Some 01 these fungi also prodlrcc conpounds llnt.rgonisic !o inscct herbi\1res. Canop,vmicrolungi may also providc a ninor link bcl\\een soil and aqualic food \!cbs as early colonists of li\ c lbli.rge and $\'igs rha! conplele their sporularionclctes ir soil of slrcans and as r porlion ofannual rbolegrouncl production thal is ussir liatedinsoil as lirlcrli l. The laried conrponenlsrnd lunctions of crnopies $ith lr'hich l1icrofungi afe .Lssociarcdsuggest thLrt biodiversity of thc microfung.rl biola is high and poten- lit li a rich soufceof novcl tara.

Introduction canopiesis also influenced by epiphytic crypto- gams, phanerogams,and arthropodsand other The canopiesof mature, dd gro\\"thforest trees clnopl rninrul..nhich ll-' inlerJclil) a \ilri.l\ presenta complex, multilaveredhabirat that sup of associationsq'ith canopy microf ports a dch and variedcomnunity of organisms. ungi.Decont- positionand nuffienl cycling processes (such Microfungi re an integralcomponent ofthis com- as in situepiphytc rrunity. interactingin a varicty of rvayswith the decornposition.dead iimbs. lodged needles.perched hosttree as well asthe otherorganisms that to- soil)occur within canopies, but gether-compdsethe canopycommunity. For two littlc infbrmationhas bccn publishedon these processes ofthe authors(JKS. MAS), investigatingthe tas- and the roles of microfungi in thern. iinutinp.. omplcrrolc. ('l'lun! i in rh( loreslccnup) Although many specicsare uniquely adaptedto prorided rrn carll introductionrnd rrpprerrrice- biotic lunctionsand conditionsspecific to the .hip in tnleologllhirl he(!rme r Iilelimccrrr('cr canop)'habitat. thc btal canopy nycobiota also interest. Microllngi in canopiesare more than includes speciesrvith widespreadterrestdal dis- objectsolbiological curiosity.however; they play tribution. More intensiveinvestigations will un- inportant ecologicltl roles in matureforcsts: nu- doubtedlyreveal a multitudeofspecialized, highly trientcvcling. symbioses with canopyepiphvtes, adaptedendemic microfungi, atld inevitably many and symbiosesand trophic interactionswith ne\r,taxa. arthropodsand othel canopy microfauna. Diversity of microfungi occursat an exceed Much lundamentalinfornration on the roles ingly small scale a single conifer needlemay offungi in canopiesremains fragmcntary. a prob- harbor severaldozen diffcrent speciesextemally lem that presentsmany opportunitiesfor ncw and and internally.Although rnicrolungi arc ubiqui- significantdiscoveries. Microt'ungi in calopies Ir)u.in nillure.lhc) r)ficull) rrc ineonspi;uou': lbrm a variety ofdirect associationswith the host u\urll) lhc) arcpre\ent l' internll.un'een. mi trecs,co)onizing foliar and twig surlaces(epi croscoplchyphac and their presenccis revealed phytes).iDtemal foliage (tbliar endophytes),loung externallyonly when they sporulate,usually sea and old bark (bark endophytcs)and wood (xy- sonallyand typically ephemeral.Many arehighly lem endophytesand wood decomposers).The host-or substate specific.Conventional sampling distributionand diversity ofmicrofungi in tbrest methodsofvegetation ecdogy arc inadequateto

NorthwestScience, Vol.70. Speciallssuc, 1996 37 accuratclyenumerate nicroflngi, and the details are either leachedf'rom tbliage or interceptcdin of distributions of even the more familiar taxa rainfall. Most fungi in exposedhabitats have remain skctchy.Laborious isolation procedures melanizedhyphal walls, grow sporadically in re- aregererally requiredto detectand quantify theln. sponscto temporally favorable conditions. and Idcntificationrequires microscopic examination. arespecialized to withstandexposure and desic- and generally requires a high dcgrce of exper cation. Needle surfacestypically are colonized tise.Ofien identitjcationis difficult or impossible by fan.iliar,ubquitous epiphytes common on many with isolatesin pure culture that tail to produce plants:such genera as Epict ccun, Altenuria, and sporesor identifiablestucturcs. Conversely. cedain Honnonena. Atichia millardetil Racib.. the groupsdo not grow or sporulatein culture(e.g.. anamor?hof S"rzrtic nrlllarderil(Racib.) Meeker. Metacapnodiales),and must be detectedvisually a loculoascomycetethatgrows as ayeasl-like mass on hostsubstratcs. A pa icularobstacle to eco- in a gelatinousmatrix, is a dominantepiphytic logicalstudies ofcanopy fungi is thatoften basic specieson twigs and needlesof severalconifefs taxonomic infirrmation is lacking oI insufficient. in the Pacific Northwest(Carroll et al. 1980).On This problemcan only partiallybe overcomeby some hosts, sooty molds (.Capnodiun. integratingexisting databases lundamentalbio- Metacapnodium)fungus speciesadds yet (Hughes1976). anotherIevel of complexity. Bccauseof the abil On conit'ers,such as Douglas-fir (Pselr./otsrigr-r ity of fungal hyphaeto anastamoseand become lre.,r:ir:sli(Mirb.)Franco), the topology of needle multinucleate.and the ability of many fungi to surlacesinf luencesdistribution of microepiphytes, reproduceasexually, enumcration of individuals with grelter colonizationnear the needlemidib, of'tencan only be accomplishedusing specialized nearstomata, and along the marginsof anticliral techniquesof moleculargenetics. cell walls (Bernsteinand Carroll 1977;Caroll 1979).Microbial biomasstends to incrcasewith Foliarand Twig Epiphytes needleage through the first thrce years.ln this exposedhabitat, these lungi are also availableas Communitiesof epiphyticlungi in canopiesde- a lbod resourceto grazingmicroarthropods, such velop as result of thc sametypes of biotic and as orabatidmites, and grazing may help explain abiotic intcractionsat play on non-arborealsub- the decreasesin microbial biomassobserved on strates.with the exceptionthat new uncolonized olderneedles. Distribution ef microepiphytesalso substratesarc predictablyand re-qularlyadded by tends to decreasewith increasingheight in the ner!,seasonalgrowth. Foliar and bark surfaces eanopl (Canoll lq79). Vicrobiul hi, rmir.\, 'n rwig\ provide substratesthat supportcharactedstic as sinrilarlyincreases with age(Canoll et al. l980). semblagesof specializedmicroepiphytes that andbio undergochanges in speciescomposition SpecializedParasites and Pathogens mass as the substratcsage. Pa icularly in more nresic habitats,microepiphyte assemblagescan Commonmicrofungal parasites and pathogens of becomewell developed,especially on cvcrgreen foliage and twigs of nofthwesternconittrs arc lbliage and twigs, whcre they nay attaln a sub- describedin detailin Funk (1981, 1985).A re stantialbionass and alnual productivity.Carroll centhost index (Farret al. 19139)lists approxi- ( 1979)estimrted biomass of fungalfoliar epiphytes matcly 80 speciesof microascomycetes,50 spe in an old growth Douglas-fir firrest at 30 kg/ha, cies of hyphomycetes.and 30 species of and Carroll et al. (1980)estimated fungal twig coelomycetesassociated with thetbliagc and twigs nicroepiphytebiomass at l2-20 kg/ha.Annual ofDouglas-fir alonein the PacificNonhwest. This productionoffungi on combinedtwigs andneedle li.t shouldbe con'idered prrtial bec!ru.e r,'uline sudaceswas estimatedto be:150kg/ha. (Canoll isolationsfrom Douglas-tirand other conifer hosts et al. 1980). olien yield taxanot listed(Stone, unpublished). Although mesic,lbliar surlacesexpericncc Endemicpathogcns are not uncommonin the fo extrcmesof temperaturcand desiccationseason- liage of maturetrees, but they often havedisjunct a1lyand diurnally.Epiphytic llngi are adaptedto distributions.appuently affectedby site tirctors leric conditionsand low levelsof nutrientsthat and individual host genetic susceptibility.

38 Stone,Sherwood. and Carroll Phaeocr\ptoptrsKoearrrnrril (T. Rohde)Petrand phytesand decomposers.Many arehost specific Rhi:.osphaerakalkoJJii Bu6ik, for examplc, are or have restricted host distributions. but a few comnronly lbund infecting a proportion of the specieswith broad host raDgesarc oiien recov- needlesof nature Douglas-fir trees.but their ef'- eredtiom foliage at low frequencies.P/n/losficla lects are not olten seriousunless other s()urcesof .rbl"d.r Bissett & Palm is the [lost common en- stless.such as drought or cold injuq'. areinvolved. dophyte of Aricr spp. in the Pacitlc Northwest. In young plantationsand non site-adaptedgeno and also occurson Do:uglas-ft.Pleuoplaconemu types.houerer. the'e fungican eru.e.erious sp.. possibly the anamorphof Chloroscypha delbliation. chloromeltt(.Philips &Harkn.) Seaver.is the ntost Anothcr group of tbliar fungi are primarily c mmlrn endoph)le of Scqanla 'sqp1 rvirtn' superticialbut also invadc the inner spacesof (D.Don) Endl. (Espinosa-Garciaand Langenheim foliage.Such colonizationmay be confinedto 1990.Rollinger and Langenheim 1993), and oc stematalchambels or may involveextensive in- curs as a dominantendophytic colonist through- tercellulilrhyphae in mesophyllparenchynra. out the natuml range of the redwood (Rollinger Micfothyrialesor"fly speck"lungi haveflattened, and Langenheim1993). Rhabdocline parkeri shieldlikeascomata produced on living needles. Sherw..Stone & Carroll, the most common fb- Black mildews,such as Melioh, Asteridiella. and liar endophyteof Douglas-tir.is benign.but its Resutoriu.arc typrcallysuperficial. bnt sometimes coDgenersR. pseudotsugueSyd. and R. welrll producc hyphaethat enter needlesat the stonrata Parker& Reid aredefoliating pathogensofDou- or pierceepidermal cells. Again, presumablybe glas lr (Shenvood-Pikeet al. 1986).Several genera causeof theexposed habitat, the hyphac of these arerecurently isolatedas endophytesfrom a va- fungi aremclanized. P hteot:rl ptopusgueum anni i ricty of coniter hosts.including: Phoruopsis, comnonly infecLsnccdles ofDouglas-fir andpro- Cryptosporiop.tis,C r.tptoc line, Phy I lc.'st icta, duces extensivesupedicial and intcrnal hyphae Sei riditrm,GenicuI ispori un, andNoduLisporiu m. (Stoneand Canoll l9tl6). Assemblagesof tbliar endophyteshave been ex- arnined in several conit'er hosts in the Pacific FoliarEndophytes Nofihwest(Carroll and Caroll 1978:Pctrini and Caroll 1981:Espinosa-Garcia and Langenheim Fungal colonization of internal tissue of appar 1990).and in theeastem Unired States (Bills and ently healthy fbliage, pa icularly of plants with Polishook1992). evergrcenor iong-livedfoliage, has been well Littlc is known of the detailsof colonization documented.Such cndophytesare a ubiquitous. of ibtiageby endophytes.In speciesthat ha!e been ccolo-qicallvspecialized group of symbioticfungi studied.colonization is restrictedto minute,lin and arervidely assunrcdto be presentin vifiually itedponions oI ti.sucin theepidennis or me\o- plants(Canoll all land 1988).Inhibition of her- phyll. Ph\llostictqcorc?n /ric.i Sacc.on Tarasspp. bivory by toxic alkaloidsproduced by endophvtes is apparentlyonly subcuticular.whercas P .r1rlell.r infecting ce ain grasseshas been demonstrated on Douglas fir andAbles spp.fbrm limited inter- (reviewedby Clay 1988.).and forms the basis of ccllularinfections within the mesophyll(Stone a mutualisticsynrbiosis in thesehosts. Several 1993.).Infections ofRhabdocLine parkeri arecon- fungus speciesisolated as cndophytestiom co fined to singleepidennal cells in healthyneedles. niferous foliage and bark also have been shown but colonizecxtensively and sporulateon galls produce (Bills to biologicallyactive compounds of the midge Coirtninia pseudot.wgaeCondrashoff et al. 1992;Polishook et al. 1993;Stierle ct al. and also senescent and abscised needles 1993).including compounds toxic to defoliating (Sherwood-Pikeet al. 1986;Stone 1987). Simi- (Calhoun insectssuch as sprucebudworm et al. lar intracellular endophyte infections have also 1992.r.Sererrl ol lhe\eendoph)tc :rs.oeirtirrn. been observedtbr an unidentified endophytein are also believedto be antagonisticto insecther Sequoiusenqtenirers (J. K. Stone,unpublished). bivorcs(Carroll l99l). althoughendophytcs en- Endophytc inf'ectiondensities and speciesrich- compassa varietyof ecologicalroles (StoDe et ness increasewith foliage age (Stone 19871 al. 1994). Espinosa-Garcia;urdLangenheiml990). Douglas Endophytespecies comprise an ccological lir needlesarc repeatedlyinlectedby R. parkeri assemblagethat is distincttrorn saprophytic epi- asthey age (Stone 1987). BecauseR. par,teri occurs

CanopyMicrofungi 39 asdiscreet. separate inlection loci. the number of bly, membersof the Hypodcrnrataceae,but aiso individual infections per needlecan be counted inclutJingLtclrne Ll ula spp.(Hyaloscyphaceae) and thc total pcr trcc cstinrtrted.Mccutcheon et are prominent on living conifers in the Pacific al. ( 19931conservativeiy estimate the number of Northwest. Tryblidiopsis plzrrstri (Pers.:Fr.)P infectionsby R.2rirteri in a singlctree 1o bc on Karsten,a conlmon circumborealspecics which the order of l0 in our area occurs on Picea e geLnannii Ptl.rry ex Engelm., aDdDiscocainia treleasei(Sacc.) J. An endophytichabit similar to R. /r.irft.rrimay be widespreadin the Ascomycetetamily Reid & Funk, on P. slrclreirsls(Bong..i Carridre, Hcmiphacidiaccac.In thc Pacific Northwest, arerepresentative. Both tiuit in aburdancein the Didlntoscella thlrjihu (Dular\d) Maire, with its spdng on twigs that have beendead for lcssthan spottydistribution on dcadnccdlcs on othcrwisr: a year, and thus must be suspcctcdof routinely healthybranches Qf Thuja.is sulpect;a better colonizingbark of living twigs. Other species exanple wouldbe Falrl"1li Lrrg.re(Farl.) Kirschsl. whosebiology appears to be similarare l/terna p}rl (Albertini on eastemhemlock. This speciescan be reliably & Schwien.)H6hn. and lfitftr:1li (Rehm) Kujala on Pinus spp.. fbund in late \\"inter on the oldest needlesstill Coccomycesstntbi J. Reid & Cain on P. strobusL.- Cott:omlces attachedto healthyhemlock trees: its appearance lrcterophyllaeFlrnk on TsugaheteropbLla (Rf coincides with Don-nalsenescence. Most endo .1 Sarg.,and LachneLlulqclllrira Dennis and L. phytesof conit'ersapparently cease growth soon cgc.il;ll (Berk. & Curtis) Dennis on P menziesii after initial infection and remain quiescentuntil and,Abies spp.,respectively. Live bark is appar nrlurll neetlle\erre\Lenae,rr irrjur) \'uu.e irjli!e ently also the habitat of Tdxom\'(esantlreanae growth to resume.These fungi have a competi- Strobel.Stierle, & Hess(Strobel et ai. 1993),which tive advantagein occupying lbliage just prior to has helped lbcus attention on the commercial abscission.and are in a positionto intercepttrans- potential of endophytesby vinue of its reported located metabolites.As early colonists.they are ability to producethe anticanceragent taxol i, also tlrst in possessionof the abscisedneedles Lltro(Stierle et al. 1993). and may be consideredthe fi$t serein the suc cessionof decomposers(Stone 1987). Bafk endophytes,which thell becomcthe first successionalspecies in thedecomposition ofdead Barkendophytes branches(a processwhich in someconifer spe- cies procccds to an advancedstage betbre the Many speciesof fungi colonizcliving bark on material lalls to the lbrest floor), are potentially trvigs and small branchesofconiferous trees,but inportantin canopyecology. Perhaps. tbrexample. almostnothing is knownoftheir biologv.Resin- theirprcsencc cxcludes aggressive ggneralists that ousyoung bark ofDouglas fir generallysuppolts lrreactively pathogenic.On the other hand.all of ArthoptreniapLumbarla (Stitzenb. in Hasse)R. lherrhore.pecie. liFure in li't. ol di.eas((lu. C. Hanis and other non-lichenizedmembels of ing fungi and can be found t'ruiting in abundance the Arthopyreniaceaeincluding Mtcoglaent on diseasedand dying trees,although generally siibcoeriilercerrs (Ny).) Hdhn.(=Wir1 1g I iq cs s7 u 1 g q (perhapsinvariably) these trees are alrcadl, se- (Ellis & Everh.)Berl & Voglino)and M1r'oglaeira verelywcakcncd by othercauses.The weJl-adapted sp.(" Ps e udo pl eu"). Arthopr reniupl wnburiu also parasitethat is neutral or even beneficial under occurson red alderand oLher smooth-barked trees. nrtulalconditions can alwl1. beeornea :erious In easternNofih America.another non-lichenized problem in a stressedcommunity, in artificial mcmbcrof a normallylichcnizcd gcnus, Ai'lronla monoculturc.when trees are introducedoutside npolita (Hoffnt.)Borrer. is ubiquitouson young their normalrange. and when closelyrelated hosts bark of Plirirs strobrrs.Yestigitm felicis Pitoz. & tiom different pans ofthc world arebrought into "cat's Shoem.,an unusualcoelomycete with pa$r' contact. shapedconidia, is knorvn only from young liv Xylotropic endophytcs.f'ungi that are early in-etwigs of Thrla pllcataDonn ex D. Don in the colonistsof soundwood, are another similar. ap- Pacific North\\,est (Pirozynski ard Shoernaker parently widespreadgroup, although coniferous 1912). hostsliom the Pacitic Nofihwest apparentlyhave Ascomycetesthat fruit en recentlydead t$ igs nol becncxamincd for theirpresenca. In Europe. still attachedto otherwise healthy trees nota- healthy,attached branches of oak and beech

:10 Stone,Sherwood, and Canoll (Chapelaard Boddy 19811;Boddy 1992).Alnu.s (Diederich 1990).Related liche nicollichen decornpositionis probabJe. pathogcns. tatlve such as l1_rpo-nloanwntnalultl Epiphyticmosscs and hepatics present another- (Wahienberg) J.H. Milleron aspen,rs u'ell asmany intriguinghost association. Recently Weber ( 1995) wood decayl'un-ei. are adaptedto this strategyof has rediscoveredSelenosl>ora guemisot:ii (P. & earlycndophytic occupation. H. CrourntR. Heim& LcCal.an inc,'n.ficuou. discomycete,associaLcd with mossesin the Pa- PotentialSources of NewTaxa cific Northwest.Dajbbler (1979) has reportcd Colonistsof Epiphytc Pants pvrenocarpousand pezizalean parasites of mosses in Europe.Hepatics, similarly. are known to tbrm Paradoxically, although the lichen flora ol the symbioticintracellular associations q'ith endo- PacificNorlhwest is rich in tcrmsofboth species phyticfungi (endomycothalli)in thegametophytes. and biornass.lichcnicolous fungi fiom the Pacific Fungibelonging toAscomycetes. Basidiomycetes. Northwest are underepresentedin the literatufe. and Zygomyceteshave been reported fion these This region has apparentlynot becn systemati- hosts,in a rangeof cytologicalspecializations cally sampledor investigated.and only scattered ranging from simple to complex (Pocock and collectionsexist. In Europc,firr exanple,where Duckett 19135a.b).Arboreal mossesand hepatics lichenicolousascomycetes have becn more rn- may not harbor speciesdistinct from thc terres- tensivelystudied. a rich and diversemycobiota trial habitat.but they representa categoryof host is known to be spccificallyassociated with lichens wellrepresentedin matureconifer canopies, which (e.g.Hawksu ofih l983).Judging f'ron the rela almost ceftainly harbor a specializedmycobiota tive easeof findingparasitised lichen thalli in our wherenew taxamight predictablybe sought. i,trea,almost ceflainly a large resen'oir of novel Canopy epiphytesalso halbor severalassoci- speciesor speciesnot known from NofihAmedca atedmicroscopic protozoa and small animalsthat await discovery in the Pacific Northwest. arepansitized by specializedfun-qi. In recentyea$. Lichenicolousspecies are u'ell represented in thc discovcriesof new taxa(genora and species)of Hypocrealcs and Dothideales and related fungal predatorsand parasitesof rotife$. amoe- nrit,r.p,rricgencrl orJcr:lhJl 1.,'q9n11in nu. bae,nematodes, tardigrades. springtails, and other merousfungicolous species. Approximately ten organismshave f'lourished. Most habitatswhere gelera of hyphonycetes and roughly an equal thcseanimals exist. e.g. moss, r-otting wood, leaf nunrberof coelonycetc genera ale oligately mold.have also yielded new andinteresting lun lichenicolous(Hawksworth 1981). Recently, gal predatorsand prmsites ( Drechsler | 94,1:Bar:ron Diederichand Christiansen( 199,1) have idcnti- 198 l, 199 J; Banon et al. 1990: Brmon and Szijarto fied thecause of gallscommon on U.ilea spp.in 1990),although relativcly tew groupsarc work- thePacitlc Nothwest asan unusualBasidiomycete ing on them rvorldwide.Ascomycetes, Basidi- related10 thc Tremellales("jelly fun-qi").Other omycetes.Zlrgonrycetes. and Oomvcetes are rep- galflike bodies on Lecanoralesare also appar- resentedin predatorsand parasitesol protozoa cntly causedby undescribcdheterobasidiomycetes anclsrnall animals. Thcse fungi display an aston-

Canopl Mierofungi -+l ishingdegree of spccializedadaptations lbr cap matterof coniecture.The Trichonrycetes, a simi- turc and penetrationof prey species.and consti- larly neglectedgroup ol Zygomlcetes.are obli- tuteone ofthe betterexamplcs ol'adaptive radia gatecommensals or parasitestound in the diges- tion in the fungi. A nunber ol Nemutocto us tive tractsof aflhropods(Moss 1979).An exanple anamorphsof Hymenonrycetessuch as l1.rrc, of insect-fungusinteraction more typical of tree- lnehelio and Pletoolirs are known to fbrm traps tops is that belweeDthe woodboringScolytid for capturingnematodes (Thorn and Banon 1984). beetles,which actively cultivate and arc nutd- "ambrosia presurnablyan adaputionof cellulosedecomposers tionallydependent upon 1ungi."r di- to thc low nitrogeDcontent of the substate(BalTon verseassemblage of anamophicAscomlcetes. The l992).Again, careful examination ofcanopy habi- beetles have specialized anatomical structures tatsis almostcertain to addnoveltaxainthis group. (mycangia)1i)r establishing ncw fungalcultures whena new woody substrateis invaded(Norris Interactionswith Canopy Arthropods 1979).Vectoring of pathogenicfungi by insects is one ofthe betterunderstood and most ecologi- Coniferouscanopies in the Pacillc NorthwesteLre callyinponant lungus-insectinteractions involving (1982) rich in arthropodspecies. Voegtlin repoted tbresttrees. for examplcvcctoring Ophiostomatoid approximately1500 taxa tnrm thecanopics ofold- ftngibl- Dendrottonrisand Scol_rlrisbeetles (see growthDouglas-lir, and concluded that Douglas- Harrington,1993; Malloch and Blackwell. 1993). fir canopiessupported the greatestdiversity of arrhropodsol ary canopysystem studied to date. Aquatc Hyphomycetesn Lodged Ltter Fervof the speciesrepofted rvere cndcmic, i.e. having theil cntirc life cycle completedin the Conidiaof aquatichyphomycetes, mitosporic fungi ctrnopy;those that are endemic are prinarily mites, with tetraradiateor sigmoid conidia specialized Collembola,and Psocoptera.The literaturcon tbr aquaticdispersal, are typically associatedwith arthropod-fungus intcraclionsis enomous and senescentand decaying leaflitter ftom treesgrow- beyondthe scopeof this paperto review,but wc ing nearrapidly llowi ng streams (Webster1911 I ). should at lcast point out that the propensity tbr Conidiacharacteristic ofthese fungi alsoare com fungi to tbrm complex,specialized associations monlyrecovered fiom rainfallsamples collected with insectsis ancicntand fundamental.Detailed bcncathmaturecanopies from uplandsites far from (G. rcviewsoffungus arthropodintenctions canbe streamsin Oregon C. Caroll, unpublished). foundin Batra( 1979)andWheeler and Blackwell Sigrnoid,helicoid, tetraradiate.and branched ( 19134).Again, unfortunately,published informa conidiareprescnting several anamorph genera, tion specificto thecanopy habitat is almostconr- have been collected lrom rainwashedtrunks of pletelylacking. severaltree specicsin the Pacific Northwest (Bandonil98l). While manyofthe conidiathus 11is almostaxiomatic that wherevera high collectcdcan be readily assignedto existing gen- degreeof athropod diversityexists, a con cspond- eraand species,e.g. Cyoerfelb biupperulictrlatu ing diversitl'of associatedfungi will be found. (Arnold) Ingold, apparcntlyundescribed taxa are althoughmany ofthe fungalgroups that tbrm close notuncommon in raintallsamples. Ditfcrcnt spe- symbioseswith insects are among the poorest cics seem1o occur in associationwith different documentedtlIxonomically. The Laboulbeniales. hosttrees. but the sourceof the conidiaand the for exltnpl<.i. rn ofdrr l ohliPirleecl, rp.rrrsilc: ecological role of thesefungi in the canopy re ofinsectsand mitcs andspiders (reviewed byWeir mainsenigmatic. L( gedleaves and dcbris are a andBeakes 1995). While manygenera and spe- probablesource.Ando (1992) has shown that some ciesof Laboulbenialeshave broad hosL distribu- "terestrial aquatichyphonycetes" are endophytic tions.a t'ewspccics have sex- and even positional leaf colonistsor parasitesthat sporulateephem- specificity (Benjamin 1971). Although the crally in surfacecondensation of leaves. Lahuulbenirles.u ith rounJ2000 \pccic.. i\ one of the mostspeciose orders ofAscomycetes and Fungi on Standing Dead Wood is probabJythe llrrgcstand most highly special ized groupof entomogenousfungi. only a frac- Dcpcnding on the species,coniferous trees may tion of the potentialhosts havc bccn examined. support a large volume of dead branchesin the andthus the numbcrof undescribedspecies is a canopy.particularly at high elevations.This aeriaJ

12 Stone.Shervood, and Carroll nichesupports a diverseassenblage of unusual threatenedif its host is threatcned.The impor 1ungi,whose adaptations and taxonomic divelsity tanceof leavingsome proportion of deadwood havebccn discussed in detailby Sherwood(1981). in managedforests is increasingly recognized. Threespecies predoninatc on standingdead co- which should have a positive effcct on preseN nil'erouswood at high elevations:Agl.i,nn ndlr? inguncommon species oflignicokrus tungi. Most (Pers.)Fr.. an unusual non-lichcnized member of of the [ungu..pccies menrioned i]l\o oc(ur in lhc Lccanoraleswhose closest relatilcs are maturesecond growth within the nornal geo lesinicolousfungi, also occurring on living coni graphic rangc of the host species. fets;Xtlopeziuluni.rplrrierir.a (Fr.) Hiihn.. a taxo nonricrlly isolatedIoculoascomycete. and Crypro- Besidesthe possibilityof harboringunique disotsptllidus (Pers.:Fr)Corda (Ostroprles). Also microfungal species.old-grou'th standsand in- conmon in this habitat are DureLkt utro.\rtne.t dividual trccs nray also representa largc reser- (Ft.) Hohn..Propolis spp.,Melittosporiwn prcpo voir of infiaspecific genotypic diversity. lidloides(Rehnr) Rehm. Stictisspp., MtcocaLiciL! nl MccutcheoDet al. (1993)provide evidence that spp..and Odontotrenrataceae.This habitatis un- thc foliage of old-growth trees supportsa large usuall.vrich in taxa (gencraand tirmilies) that in diversity of genotypes of the endophyte cludeboth lichenized and nonJichcnized species. Rhobdoclinepurkerl, and showedthat the num Basidiomycetesarc not prominentin the known ber of unique genotypesof R. parfteri infecting mycobiotaon smallstanding dead-woody conif- younglrcc\ in mitnirped.tands in clo.cpr,'rinr- erousmaterial in thc Pacific Northu,est.It seems ity to old-growth standswas similar to that ofthe improblble that Basidionycetes arc actually as old-grouthlrec\ bul muchgreuler thiln in rnitn- little rcprcscntedin naturcas oul presentknowl- agcdstands of similar agefarther awav tiom old edgesuggests. At high elevationsand drier areas gro\\,thffees. A trcc from an isolatedsite had the aerial decompositionis clearly a lengthy process fcwest R.pal,tcrl strains.For microfungi suchas proliding a stableniche with considerablespa- R.parkeri, old-growth treesrepresent an archivc tial and telnpofal differentiation. ofgeneticdivcrsity. Carrdl ( 1988)has suggcsted thatgenotypic diversity of an endophytemay help Specificity to old-growth? conler acquiredresistance against herbivorous Manv of the speciesincluded in this discussion lnsectsto the host tree through the combinedac- are known tionr only a te\\" collections. so that tivity ofa varietyofantagonistic metabolites pro- anygeneralizations about their specificity to un duccd by the fungus.The canopy microfungi of disturbedsites must necessarily be speculative. isolatedtrees. urban plantings. and trees grow- Clearly.a host specilicfungus growing only on ing outside their normal range is quite difftrent a rare spcciescontined to undisturbedsites is tiom that occuning naturally.

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11 Stone,Sherwood, and Canoll Siebef.l N. 1989.[ndoph] trc i|Lngiin t$'igs of health] .rnd Thom. R. G.. nclG. L. B.trlon.198,1. Clni\orous nush diserscd \ors.1,,- spruce and r\hire fif. \lfcol. Res. rooms. Science22,1 76-7i1. 92:lll-326 Voegtlin,D. J. 1982.In\ertebrrres ol theH. J.Andrc$\ E\ StierLe.A..Ci. Slrobcl. ard l). Stierle.1991. Tr\ol .Lndtaxane lefimentalForesr. i!eslern Ctrscadcs nrountain!. Or pfoduclion b) 7ilrdrlr'..r dr../,1r.,r.1.,.rn cndophltrc egon:A sufve)ol dlxopods.r\\ocirtcd $ilh lhccanop) lu.gu! of llre Paciilc]e!\,. Science 260:21.1 216. uf old growlh Pr.x./orjr.rrl ,nl, r:&,rii . SpecialPubli Sione.J.K. 1987 I nitiationand dc\'.lopncnt o I latcnt i nfec cuti|)n.l. For.!t Rcscarchl-aborator!. Oregon SIaIe ttotlsb\ Rhabtlo(lifi( paitfii on Douglas-flf. C.rn.J. Llnivehity.29 p. uot.65:261,12621. [Jebef.N. S. I995 \Ve\ten Amcricar Pcrilrlcs. Scll,,r.ryr,ll 199-r.Paltcr.s of coloniTrtion of conilef finr- qr?r,ilrd.rll. ne\\'to NolthAmeic.r. Mycologia 87:90 ge b,r-endophrlic Prr'l/r-rrl( r.r species. lnocLrhm,[,]:58 95. Stdre.J K.. and G. C. Cardl. 1986.obser\'alion\ on the \\'cbncr.J. I 98 L tsiolog,v and ecok)gt of rquatich) phon) cetes. de\elopnenl ol a\cocarps nf I'hue ^11/rl \ ,, D. L Wicklo$ rnd G. C. Crroll (eds.).Thc fun gd. r tutnii and on lhe possiblee\istence ot an galCommunil).its Ofganizrtion and Rolc in thc Eco lnrmophrcsrare. S,,''.do$in l8:l l7-123. sysreln.Nlafcel Dekler. \c$ \brk. Pp. arS| 691. St|)nc.J. K.. O. Virc!. O. Petrini.and L H. Chapeh. i991. \\:eif. A. and G. Beakes. 1q95.An inlroducrio. 1o the Hinological studieson host penetralionlLlld coloni Lrboulberi les:.rlirsci tirggroupl)1cnlornogcnous ration b) cndoplryricfu.gi. tr O. Petrinirnd G. B. rungi.N{}cologisr 9:G I0. Ouellette(eds.), Altcralion of IIosi \v|1llsby Fungi. whcclcr.Q., and NI. Black$'el1.198-1. Fungus'lnsect Rel.r pfoceednrg\of the slmposiun hcld al ilrc 6th Inter- lion\hips. Perspecti\'esin Ecolog] and E\olLrtx)n nrtidul Congressof Phnt Ptrtholog). Nionl rcal. I 993. r'' r',,hJl r\.-,r ) Pre.' \i{ 1: f1,. APS Pres\.St. Ptrul. Pp. 115 126. Zrgnrricr. \\.. R. Bauer. rnd F. ObeNinklef. 199,1 Strobel-G.. A. Stierle.D. Sticrlc.and w. Nl. Hes\. 199-:. Niycoparasitismin,tome //",r.11, \pp. NI)-cologirr 1'.1\ottt\r.s ruw(. a proposed nex txxon for .r E6:19-56. bulbilliieroush)phonlcclc a!$ciated $ith Pacific) e\,, (./d-rlrr/,/"rilrlnl). Nllclrlrron,l7:71 IJ0.

Crnopy Microfungi ,15