Table Of Content

© Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at Diversity and ecology of fungi in the Golfo Dulce region Diversidad y ecología de hongos en la región del Golfo Dulce Meike PIEPENBRING & Armando RUIZ-BOYER Abstract:Fungiplaymanyrolesincomplexsystemsoforganismicinteractionsintropicalforests.Theyprovidewaterandmin- eralstoplantsasmycorrhizalfungi,othersdecomposedeadorganicmaterial,mainlywood,intocompoundswhicharemadeavail- ableforotherorganisms.Asparasitesofinsects,theyperformanaturalbiologicalcontrolofinsectpopulations.Asparasitesof plants,theycontributetothedevelopmentandmaintenanceofplantdiversity.Otherfungicausediseasesinvertebrates,like chytridiomycosisinfrogs,dermatomycosisorsystemicmycosesinhumans.Fungiliveinmutualisticsymbiosiswithvascularplants asmycorrhizalfungiorendophytes,withalgaeasmycobiontsoflichens,withleaf-cuttingantsasfungalgarden,andwithscale insects.Althoughfungiareveryimportantintropicalecosystemsandoffermanypossibilitiestobeusedbyhumansforfood,med- icine,andotherpurposes,therearerelativelyfewmycologistsworkinginthetropics.Ourknowledgeoftropicalfungaldiversity isstillinthepioneerphase.Estimatessuggestthatweknowlessthan4%oftheexistingtropicalfungaldiversity.Muchresearch remainstobedoneintropicalrainforestslikethoseoftheGolfoDulceregion. Keywords:mushrooms,lichens,mycorrhiza,plantparasiticfungi,insectparasiticfungi. Resumen:Loshongosdesempeñanmuchospapelesenloscomplejossistemasdeinter-relacionesdelosorganismosenlosbosques tropicales.Comohongosmicorrízicosabastecendeaguaymineralesalasplantas,otrosdescomponenmateriaorgánicamuerta, principalmentemadera,encompuestosqueseránaprovechadosporotrosorganismos.Comoparásitosdeinsectos,realizanelcon- trolbiológiconaturaldelaspoblacionesdeinsectos.Comoparásitosdeplantas,contribuyenaldesarrolloymantenimientodela diversidaddelasplantas.Otroshongoscausanenfermedadesenvertebrados,comoquitridiomicosisenranas,dermatomicosiso micosissistémicaenhumanos.Loshongosvivenenmutualismoconplantasvascularescomohongosmicorrízicosoendófitos,con algascomomicobiontesenlíquenes,enlashojascortadasporhormigasyenlosdenominadosinsectosescama.Aunqueloshon- gossonmuyimportantesenlosecosistemastropicalesyofrecenmuchasposibilidadesparaelserhumanocomoalimento,medic- ina,yotrospropósitos,hayrelativamentepocosmicólogostrabajandoenlostrópicos.Nuestroconocimientosobreladiversidad deloshongostropicalestodavíaseencuentraenunafaseinicial.Estimacionessugierenqueconocemosmenosdel4%deladi- versidaddehongosqueexistenenlostrópicos.Muchasinvestigacionesfaltanporrealizarenlosbosqueslluviosostropicalesco- molospresentesenlaregióndelGolfoDulce. Palabrasclave:setas,líquenes,micorriza,hongospatógenosdeplantas,hongospatógenosdeinsectos. Introduction species of fungi form conspicuous fruiting bodies from timetotime. Ecology Anyorganicmaterialplacedinthisenvironmentis TheGolfoDulcerainforests,withtheirhighdiver- immediately colonised by fungi. In order to grow, and sityofplantsandanimals,highhumidity,andelevated forthedevelopmentofmacroscopicallyvisiblefruiting temperaturesallyearround,offernumerousnichesand bodies,fungineedenergy.Asheterotrophicorganisms, good living conditions for a high diversity of fungi. however,fungicannotusetheenergyofthesunlikeau- Fungi and fungus-like organisms (certain protozoans, totrophic plants can. They have to find organic com- heterotrophic algae, Myxomycota) are omnipresent in poundslikesugarsandcarbohydrateswhichtheyincor- tropicalecosystems,withtheirestimatedspeciesdiver- poratebyabsorption.Whatarethenutrientsourcesfor sitybeingsecondonlytoinsects.Theyareeasilyover- Stapfia88, afungusinatropicalenvironment? zugleichKatalogeder looked, however, because most of them live as micro- oberösterreichischen scopic hyphae or yeast cells in the soil, or within and Deadorganicmaterial,likedeadpartsofplantsand Landesmuseen NeueSerie80(2008): upon plants and animals. Mycelia of relatively few dead animals, are important substrates for saprophytic 179-192 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at Figs.1-2:MouldsbelongingtotheZygomycota.(1)Growingondung.(2)Growingonrecentlycutleaves. Fig.3:Aslimemould(Ceratiomyxales,Myxomycota)formingtinyfruitingbodieswithwhitespores. Figs.4-6:Phallales.(4)Staheliomycescinctusexposesawetmassofstinkingbasidiosporesonacomplexstipe. (5-6)Phallus(formerlyDictyophora)sp.enhancestheattractivenessofitsfruitingbodywithawhiteveil.(5) Phallussp.exposingthestinkymassofbasidiospores.(6)Insectsareattractedbythemassofbasidiospores,feed anddispersethem.Atthebaseofthefruitingbodytheremainsoftheenvelopeoftheyoungfruitingbodyare evident.Fig.7:Coccomycessp.(Rhytismatales)onadeadleaf.Fig.8:SlenderfruitingbodiesofMacrotyphula sp.(Basidiomycota)onadeadleaf.Fig.9:Tinygillfungi(Marasmiussp.)onadeadleaf. Fig.10:Fungalmyceliumonadeadleaf.Fig.11:Cookeinaspeciosa.Fig.12:Cookeinatricholoma. Photos1-2,5,7-8,11:M.Piepenbring;3-4,6,9-10,12:A.Weber. fungi.Duetotemperaturesfavourableforgrowthofany selves with thick, hardly penetrable surfaces, tannins, livingbeingallovertheyear,easilydegradableorganic and complex physiological reactions upon infection. materialisscarceintropicallowlandforestslikethoseof Animals protect themselves by their immune system the Golfo Dulce area and has to be shared with other and other complex defence strategies. Fungi protect fungi,bacteria,andanimals. themselves against other fungi by complex secondary Any living organism is formed by organic com- compounds. Parasitic fungi, however, are able to over- pounds on which the fungus might live as well, but is comethedefencesofcertainplants,otherfungi,andan- noteasilyaccessibletothefungus.Plantsdefendthem- imalsandliveonthemcausingdiseases. 180 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at During evolution, plants, fungi, and animals have bodiesisnotagoodindicatorforevolutionaryrelation- developed sophisticated ways to defend themselves ships. For fieldwork and the identification with litera- againstmostparasites.Forastablerelationship,thefun- ture, however, old morphological groups are still very gusshouldthereforetrytobeinsomewaybeneficialto helpful, so we use some of them in the present docu- thehostorganismandassurelongtermsurvivalofboth. ment.Theyareenclosedbysinglequotes(‘…‘)inorder Mutualisticfungihavefoundawayofreceivingorganic todistinguishformsystematicgroupssupportedbymod- compoundsfromotherorganismsbysupportingthemin ernresults. somevitalaspect. Most fungi belong to two major groups, the As- Inatropicalecosystemwithenormousspeciesrich- comycotaandBasidiomycota.Theseareso-called“true” ness, interactions between species are particularly di- fungi (Fungi or Eumycota), characterised by the pres- verseandfarfrombeingwellknownorunderstood. enceofchitinintheircellwalls.Ascomycotaformsex- ual spores, the ascospores (endospores), usually eight Diversityandimportancetohumans withinaspecialcellcalledanascus.Theascusisusual- Fungiareecologically,morphologically,andphysio- lyabletoejectthesporesforciblyintotheair.Ascide- logically very diverse and therefore present numerous velop in flask-shaped fruiting bodies (perithecia), cup- possibilitiestobeutilisedbypeople.Somefungiareed- shaped fruiting bodies (apothecia), or other fruiting ible, others can be used for pharmaceuticals, enzymes, structures. Sexual spores of Basidiomycota are exo- foodtechnology,orbioremediation.Somefungiareex- sporesbecause they develop on the surfaceof a special ploited for biological control of weeds, of plant patho- cellcalledabasidium.Thebasidiumusuallycarriesfour genic fungi, insects, and nematodes. Other fungi are basidiospores on outgrowths called sterigmata, which harmfultomanasagentsofdiseases,poisonousfungi,by have special structures at their tips to expel the ba- destroyinghumanartefacts,orbycausinglossesofculti- sidiosporesforciblyintotheair. vatedplantsanddomesticanimals.Mouldsgrowinany moist place with some organic material and form nu- HyphaeofmanyAscomycotaandsomeBasidiomy- meroussporeswhichcancauseallergyorevenintoxica- cotaformasexualspores,calledconidia.Thesporescan tion. be carried on exposed hyphae or can be enclosed in smallcup-shapedfruitingbodies(acervuli)orsmallbot- Classificationandsystematics tle-shaped fruiting bodies (pycnidia). If a fungus only Inthefield,simpleclassificationsareuseful,likethe shows asexual development, it is called an imperfect distinction of macro- and microfungi. Macrofungi de- fungusbelongingtothetraditionalgroupof‘FungiIm- velop conspicuous fruiting bodies from fungal hyphae perfecti‘ (‘Deuteromycota‘). The sexual stage corre- (filiform strandsof cells) which grow in the soil, wood spondstothe“perfect”fungus.Asbothstagescanbeob- orothersubstrates.ToidentifyCostaRicanmacrofungi servedindependentlyfromeachother,thesamefungus (Basidio- and Ascomycota) field-guides published by canhavetwodifferentnames,onetodesignatetheper- MATA (2003), MATA et al. (2003), and HALLING & fect stage and one for the imperfect stage. Further MUELLER (2005) as well as the internet page by groupsbelongingtotheFungiareZygomycota(Figs.1- HALLING&MUELLER(2006)andadatabaseoncollec- 2),Glomeromycota,andChytridiomycota. tionsofCostaRicanmacrofungi(Anonymous2006)are available. Myxomycota and Oomycota, so-called fungus-like organisms, are traditionally studied by mycologists but Microfungi are fungi growing as yeasts and fungal do not belong to the Fungi. Myxomycota, the slime hyphaewhichcanbevisibleasmoulds.Othermicrofun- moulds,shouldbetterbecalledMycetozoa,becausethey giformtinyfruitingbodiesorsmallmassesofspores(on aremorecloselyrelatedtoProtozoathantootherfungi. plants:sori),visibletothenakedeyeastinydots.Efforts As large, brightly-coloured plasmodia (giant cells with to inventory macro- and microfungi in Costa Rica are numerousnuclei)theyfeedonmostlyunicellularorgan- presented by MUELLER et al. (2001). An illustrated list ismswhichtheyingestbyphagocytosis.Whentheplas- of fungi in Costa Rica is found at http://www.inbio.ac. cr/papers/hongos/aclap.htm. modiumattainsacertainsize,itmigratestoanexposed place and transforms into small fruiting bodies which Inthepast,macrofungiweregroupedsystematically developsporesfordispersal(Fig.3). accordingtothemacromorphologyoftheirfruitingbod- ies.Nowadays,wetrytoformsystematicalgroupsbased Oomycota correspond to algae without plastids. on phylogenetic (evolutionary) relationships with the Oophytamightthereforebeamoreadequatenamefor helpofmicroscopical,ultrastructural,andmolecularda- thisgroup.Theycanbeobservedinthefieldasparasites ta.Unfortunately,themacromorphologyofthefruiting ofplantsoraswatermoulds. 181 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at Fig.13:Smallapotheciagrowingamongmosses(Helotiales,Ascomycota).Figs.14-16:Xylariales. (14)FruitingbodiesofXylariasp.coveredbywhiteasexualspores.(15)OldfruitingbodiesofPhylacia sagraeana.(16)Leprieuriabacillum.Figs.17-19:Jellyfungi.(17)Tremellasp.(Tremellales).(18)Dacryopinax spathularia(Dacrymycetales).(19)Auriculariamesenterica(Auriculariales).Fig.20:Thefan-shapedfruiting bodiescarryasmoothhymeniumonthelowerside(Stereales,Basidiomycota).Fig.21:Caripiamontagnei (Basidiomycota).Figs.22-23:Coralloidfungi(Basidiomycota).(22)Cf.Ramariopsissp.(23)Ramariasp. Photos13,17-19,21-22:M.Piepenbring;14-16,20,23:A.Weber. Saprophytic fungi canmakecontactwithsomeorganicmaterialburiedin theground. Fungionsoil Fungi belonging to the Phallales (Basidiomycota) Exceptforsomelocalsmallniches,likeanimalex- crements (Fig. 1), concentrated, easily accessible dead accumulate nutrients in so-called eggs, which grow organiccompoundsarerareintropicalforests.Tropical close to the surface of the soil during a relatively long soils are mostly poor in nutrients, so fruiting bodies of periodoftime.Inthisprimordium,thefungusprepares saprophytic fungi growing on bare soil are not often everycellfortheentirefruitingbody.Afterheavyrain, found.Therefore,whenwalkingthroughtherainforests water is pumped into the cells and the fruiting body is of the Golfo Dulce area, fungi appear to be rare or ab- quickly unfolded. On elegant, conspicuously coloured sent.Withthehelpoftheirhyphae,however,thefungi structures, the fungus exposes a slimy mass of ba- 182 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at sidiospores (Figs. 4-5). A smell of excrement emanates Basidiomycotaonwoodydebris from this dark mass and attracts flies and other insects WooddecomposingBasidiomycotabelongtomany (Fig.6).Thesefeedonthespores,whichsticktothein- differentgroups.Themostsimpleonesmorphologically sectsorpassthroughtheirdigestivetractandarethere- aretheso-calledcorticioidBasidiomycotawhichmost- bydispersed. lyformwhitecrustsonthesurfaceofwood.Thiswhite layerisformedbyhyphaecarryingbasidiainasuperfi- Fungiondeadorganicmaterial cial layer called hymenium. The hymenium of corti- Dead organic material is mainly produced by trees. cioid fungi is smooth, folded, or provided with tooth- Dead flowers and small thin leaves are easily decom- like outgrowths, pores, or other structures, which in- posed by microscopical fungi like moulds belonging to creasethesurfaceareaofthehymenium(OBERWINKLER AscomycotaorZygomycota(Fig.2).Thedegradationof 1992). coriaceous leaves requires more time and can involve Members of Tremellales have delicate, gelatinous, the development of small but macroscopically visible often conspicuously coloured fruiting bodies (Fig. 17), fruiting bodies. Small immersed cup-shaped fruiting Dacrymycetales less gelatinous, stalk-shaped, vividly bodies (apothecia) containing asci can be formed by coloured fruiting bodies (Fig. 18), and Auriculariales Rhytismatales (Ascomycota; Fig. 7). Basidiomycota formbrownfruitingbodieswiththeconsistencyofhu- can be observed as thin, stalk-shaped fruiting bodies manears(Fig.19).Thesegroupscanbedifficulttodis- (Fig. 8) or small gill fungi (‘Agaricales’), especially tinguishinthefield.Theirbasidiahavetobeanalysed Marasmius spp. (Fig. 9). In addition to these fungi, a withthelightmicroscopetoassurethecorrectsystem- hugediversityofmicroscopicalfilamentousfungipartic- atic placement. These jelly fungi are visible only after ipateinlitterdecay(Fig.10),ashasbeenshownforlit- rainandbecomealmostinvisiblewhendry.CostaRican ter samples from the Golfo Dulce forest (BILLS & PO- jellyfungihavebeenstudiedbyKISIMOVA-HOROVITZet LISHOOK1994). al.(2000,andcitationstherein). Thedecompositionofthickbranches,woodyfruits, More persistent fruiting bodies are formed by so- and trunks is a more tedious process and yields energy called stereoid fungi with smooth hymenia (Figs. 20- formanydifferentfungi. 21)andclavarioid fungiwithcoral-likefruitingbodies (Figs.22-23).Gill-fungi(‘Agaricales‘,Figs.24-27)and Ascomycotaonwoodydebris ‘Polyporales‘(Figs.28-32)canalsogrowondeadwood. Withtheirdistinctiveshapeandscarletcolour,the The‘Polyporales‘(Figs.28-32)areconspicuousfun- stalked apothecia of Cookeina spp. (Pezizales) are gi on wood with large, console-shaped fruiting bodies among the most beautiful fungal fruiting bodies in the laterallyattachedtotreetrunks.Theirhyphaegrowin- tropics, both in the Old and in the New World (Figs. side dead trees decomposing the secondary xylem 11-12).Inourarea,C.tricholoma(MONT.)KUNTZEand (wood),i.e.causingrot,andcankillliving,weakplants C. speciosa (FR.) DENNIS can be found. Apothecia of bydestroyingtheircambium.Fruitingbodiesof‘Polypo- otherfungiarelessconspicuousatfirstsightbutreveal rales’arecharacterisedbythepresenceofporesonthe theirbeautywhenmagnified(Fig.13). lower side of the fruiting body which is more or less broadlyattachedtothesubstratewithoutorwithstipe Hard, perennial, black fruiting bodies on wood (Fig. 29). Most fruiting bodies of ‘Polyporales’ are mostlybelongtospeciesofXylariales.Theycanalsobe formedbydifferentkindsofhyphae,thin-walledliving turned white by the mass of conidia produced during hyphae responsible for reproduction and thick-walled, asexualdevelopment(Fig.14).Themorphologyofthe dead skeletal hyphae. Because of the skeletal hyphae, fruitingbodiesvariesfromcrustscoveringthesurfaceof thefruitingbodiesarehardandcansurviveforlongpe- the wood to cushions, spheres, pedunculate clubs, and riods of time (several years). From time to time during slender branch-like forms (Figs. 14-16). Species of Xy- thelifespanofafruitingbody,thereproductivehyphae lariales form dark ascospores in asci packed in bottle- cover the inner surfaces of pores with hymenia formed shaped perithecia. Numerous perithecia are located by basidia. These develop basidiospores for dispersal. close to the surface of a fruiting body. Ascospores are Systematically, ‘Polyporales’ belong to many different liberated through a small opening of the perithecium systematicgroups,includingPolyporaceae(Figs.28-30), (ostiole)onthesurfaceofthefruitingbody.Ostiolescan Ganodermataceae (Fig. 31) and Hymenochaetaceae beobservedinthefieldwithahandlensassmalldots. (Fig.32).Theydiffermicroscopicallyincellulardetails InthecaseofsomeLeprieuriaspecies,peritheciaarelo- ofthehymenia,themorphologyofbasidiospores,andby cated only at the top of rod-shaped fruiting bodies the fact that some of them cause white rot and others whichresemblesmallblackcigarettes(Fig.16). brownrot.Speciescausingwhiterotareabletodecom- 183 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at Figs.24-27:Agaricales.Figs.24-25:Mycenasp.Fig.26:HyphaeofMarasmiuscf.princepscoverthewoody substratetoretainhumidity.Fig.27:Oudemansiellacanarii.Figs.28-30:Polyporaceae.(28)Laetiporussp. (29)StipitatefruitingbodiesofPolyporustenuiculus.Onefruitingbodyhasbeenturnedaroundsotheporesare visible.(30)Trametescubensis.Theinsertshowstinyporesonthelowersideofafruitingbody.Fig.31:A fruitingbodyofGanodermasp.(Ganodermataceae)seenfromaboveandfrombelow.Fig.32:Phellinusgilvus (Hymenochaetaceae).Photos24-25,28,31:A.Weber;26-27,29-30,32:M.Piepenbring. posecelluloseandlignin,whilethosecausingbrownrot While most fungi cited above form their ba- onlydecomposecellulose. sidiosporesonthesurfaceofthefruitingbodies,“stom- ach” fungi (‘Gasteromycetes‘, Figs. 33-34) produce In Costa Rica, this group has been studied inten- theirbasidiosporesinclosedfruitingbodies.Onlywhen sively,with314speciesbeingknownforthecountryto thepigmentedbasidiosporesarematuredothefruiting date(CARRANZA&RUIZ-BOYER2005,RYVARDEN2005, bodiesofmostspeciesopen,andthesporesaredispersed RUIZ-BOYER2006).Somespecieshavebeenreportedfor for example by rain drops falling onto the puffballs. the area of the Golfo Dulce: Echinochaete brachiporus, Fruiting bodies of other species do not open by them- Polyporus leprieurii, andTrichaptum sector (MATA et al. selves but rely on fragmentation and dispersal of the 2003). Some other species are illustrated here, many sporesbyanimals. more will can be found in future by field work carried outinthisarea. 184 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at 33 Figs.33-34:Earthstars(Geastrum spp.,´Gasteromycetes´).Theouter layeroftheenvelopehasruptured andbecomestar-shaped,whilethe innerlayerhasacentralopening throughwhichthebasidiosporesare liberated.Photo33:M. 34 Piepenbring;34:A.Weber. Eveninarainforestgrowinginaconstantlywetcli- inthefollowingtext.Anyautotrophicorganismcanbe mate,humidityvaluesmaychangedrasticallyovershort attacked,includingalgae,mosses,andvascularplants. periods of time due to intense radiation by the sun. Therefore, some fungi have developed morphological Ascomycota structures to store humidity. Some ‘Gasteromycetes‘ While in regions with temperate climate, powdery (Fig.34)aswellassomeAgaricalesgrowingonrotting mildews (Erysiphales) are common, tropical plants are wood enclose their substrate in mycelial chambers, so more frequently attacked by black mildews (Melio- thehumidityinthesubstrateisnotlostsoquickly(pers. lales).Blackmildewsdevelopdark-colouredhyphaeon com.G.KOST;Fig.26). thesurfaceoftheleavesofhostplants(Fig.35).Dark- coloured,few-celledascosporesdevelopinglobosefrui- Saprophyticmicrofungi ting bodies (perithecia) which are visible with a hand Saprophytic microfungi can be found as yeasts in lensasdarkdotsonthesurfaceoftheleaf.Inaddition soil,inthenectarofflowers,inthegutsofanimals,and toblackmildews,manyotherAscomycotaandtheirim- inplantresins.Anysurfaceandmaterialwithsomenu- perfect stages grow as black mycelia on the surface of trients can be colonised by yeasts and filamentous mi- leaves.Flyspeckfungi(Asterinaceaeandothergroups) crofungi,whichcanalsoliveonexudatesofleavesand protect their asci by dark coloured shield-shaped fruit- roots. ing bodies called thyriothecia (Fig. 36). These minute fruiting bodies can be mistaken for the excrements of fliesinthefield.Thefruitingbodiesoftropicaltarspot Parasitic fungi fungi (Phyllachorales) are perithecia surrounded by To obtain organic compounds from living orga- moreorlessabundant,darkfungalhyphae(stroma)em- nisms, fungi of many different systematic groups have bedded in host tissue or on the surface of plant organs becomeparasites. (Fig.37). Fungiparasiticonplants FungiImperfecti Toovercomethedefencesystemsofplants,parasitic FortropicalAmerica,themostimportantplantpa- fungi have had to adapt closely to their host species. rasitic imperfect fungus is probably Pseudocercospora Narrowhostrangescanbeobservedespeciallyforfungi fijiensis which causes the Black Sigatoka disease on interacting with living plant cells to obtain nutrients. leavesofbanana(Musaspeciesandhybrids,Musaceae; Other plant parasitic fungi kill parts of the plants and Fig. 38). Infected leaves present elongated striae of live on the dead tissue saprophytically. Few fungi kill brown to lilac colour, on which the fungus develops entireplants–alifestyleonlypossiblewithmanyhost elongatedconidia.Thesearedispersedandgerminateto plants available. During evolution, some fungi of most infect other leaves. Infected leaves die earlier than major systematic groups opted for the plant parasitic healthy ones, and the infection affects the process of lifestyle,withonlythemostimportantonesbeingcited ripening of the fruit which has to be predictable and 185 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at Figs.35-38:Plant parasiticAscomycota. (35)Ablackmildew, Asteridiellasp. (Meliolales),on Spondiaspurpurea (Sapindaceae). (36)Aflyspeck fungus (Microthyriales)on Trichiliatuberculata (Meliaceae). (37)Atropicaltarspot fungus,Camarotella costaricensis 35 36 (Phyllachorales)on Acrocomiaaculeata (Arecaceae). (38)Aleafofa bananaplant(Musa sp.)showing symptomsoftheBlack Sigatokadisease causedby Pseudocercospora fijiensis(Fungi Imperfecti). 37 38 Fig.39:TheCoffeeRust,Hemileiavastatrix(Uredinales)onacoffeeleaf. Fig.40:TheCornSmut,Ustilagomaydis oncorn(Zeamays,Poaceae). Photos:M.Piepenbring 186 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at Figs.42-43:Fungi parasiticoninsects. (42)Isariatenuipes (FungiImperfecti) growingonthelarva ofaninsect. (43)Cordycepssp. (Hypocreales, Ascomycota)growing onakilledant.The fruitingbodyatthe headoftheant carriesperithecia. Photos33,35-43:M. Piepenbring;34:A. Weber. 42 Fig.41:UstilagoschroeterianaonPaspalumvirgatum (Poaceae)withahealthyhostplantontherighthand side.Photo:M.Piepenbring uniform in large-scale banana plantations. Although fungicidesareappliedcontinuouslytoplantations,they only reduce the infection by the fungus. When an in- fectedleafisallowedtodecomposeontheground,the fungusformsperitheciawithascosporesforsexualrepro- duction and dispersal. The perfect stage is called My- cosphaerellafijiensis(Mycosphaerellales,Ascomycota). Basidiomycota 43 AmongBasidiomycota,therustfungi(Pucciniales, formerlyUredinales)arethemostspecies-richgroupof 40).Thisfungusprovokeshypertropicgrowthofovaries plant parasitic fungi (Fig. 39). SHIVAS & HYDE (1997) andotherpartsofthecornplant.Withinthegalls,the suggest that, in addition to the approx. 7.000 species fungus forms its brown teliospores for dispersal. When knownworld-wide,about270.000furtherspeciesmight thegallsarestillwhite(young)theycanbeeatenlikea bediscoveredinthetropics.Thishyperdiversitycanbe vegetable. People in Mexico consume it as huitlacoche explainedbythefactthatrustsinteractinahighlycom- (“crow excrement” in nahuatl). Most other smut fungi plexwaywithspecifichostplants.Ahighspeciesrich- growonwildplants,mostlyweeds,likethosegrowingin ness of plants therefore is a precondition for a high deforestedareasclosetotheBiologicalStationLaGam- species richness of parasites. BERNDT (2005) cites 292 ba(Fig.41). speciesinhischecklistofrustfungiinCostaRica. Fungiparasiticonanimals Theeconomicallymostimportantspeciesofrustis the Coffee Rust, Hemileia vastatrix (Fig. 39). It causes Insectsandspidersarehighlydiverseandnumerous devastation in coffee plantations by destroying leaves. intropicallowlandrainforest.Thelargerthepopulation Onthelowersideoftheleaf,groupsoforange-coloured ofagivenspeciesofarthropodsis,themorefrequently uredosporescanbeobserved.Thesecanbemixedwith theindividualsareinfectedandkilledbyparasiticfun- teliospores.Asinthecaseoftheagentofblacksigato- gi.Inthisway,fungiparasiticonarthropodsachievea ka, control measurements only help to reduce the naturalcontrolofthepopulationsofinsectsandspiders amountofinfection,whichcannotbeeradicated. innaturalecosystems.Deadinsectsandspiderscovered by fungi can be found attached to plants. After infect- Thesecondmostimportantgroupofplantparasitic ing and killing the animals by hyphae within the bod- fungi among Basidiomycota are the ‘smut fungi‘ ies,thefungusgrowsontothesurfaceofthearthropod (Figs.40-41).Theymostlyformdusty,darkmassesof te- and forms spores which can be asexual conidia (Fungi liosporesontheirhostplants.ForCostaRica,54species Imperfecti, Fig. 42) or ascospores enclosed in asci in ofsmutfungiareknown(PIEPENBRING1996,2003). perithecia (Ascomycota, Fig. 43). We can isolate and The most famous smut in tropical America is the multiply these fungi to use them for biological control cornsmut,UstilagomaydisonZeamays(Poaceae)(Fig. measuresagainstarthropodpestsoncultivatedplants. 187 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at Otherfilamentousmicrofungiareabletotrapandto digestnematodes.Theycanbetechnicallyusedforbio- logical control and reduction of nematodes causing damagetorootsofplantsorlivingasparasitesincattle. Since several years, the populations of certain speciesoffrogslikethecolourfulpoison-arrowfrogsof tropicalAmericadecreasedalarminglyindifferentparts of the world, due to a disease called chytridiomycosis (WELDONetal.2004andcitationstherein).Theagent ofthisdiseaseisamicroscopicfunguswhichwasdiscov- eredinthiscontextasaspeciesnewtoscienceinanew genus, Batrachochytrium dendrobatidis, in the Chytri- diomycota.Wedonotknowforcertainwhythisfungus suddenly kills many frogs so quickly. Maybe the resist- Fig.44:AhumannaildestroyedbyFusariumsp.(FungiImperfecti). anceoffrogsagainstdiseasesisdiminishedbypesticide Fig.45:Theblack contaminationandchangingclimate. dotscorrespondto fruitingbodiesof Otherfungiarelessharmfultoanimals.Microscop- Sphaerellopsisfilum icLaboulbeniales(Ascomycota)liveattachedtotheex- (FungiImperfecti) growinginsoriofa oskeletonoflivingarthropods.Trichomycetes(Zygomy- rust. cota)canbefoundingutsoflivingarthropods. Fungiparasiticonhumans Humanbeingsdonotusuallyprovidesubstratesfor parasitic fungi, because they are protected by their immune system and a healthy flora including bacteria on thesurfaceoftheirskin.Bywearingtightshoesandex- cessive sweating, for example in boots in the tropics, Figs.46-47:Plants parasiticon however, the environmental conditions for fungal mycorrhiza. growthonskinandnailscanbeexcellentfordermato- (46)Gymnosiphonsp. phyticandotherimperfectfungi(Fig.44). (Burmanniaceae). (47)Voyriasp. Whenthehumanimmunesystemisweakeneddue (Gentianaceae). todiseaseorimmunosuppressivemedication,fungican alsodevelopinsideourbody,causingsystemicmycoses. HistoplasmosisisaseriouslungdiseasecausedbyHisto- plasma capsulatum (asexual Onygenales, Ascomycota). Sporesofthisfungusdeveloponexcrementofbats,es- peciallyincavesintropicalregionslikeCostaRica. 46 Further effects of fungi on humans are caused by consumptionofpoisonousfruitingbodies,bymycotox- insproducedbycertainmoulds(FungiImperfecti),and byallergenicspores. Fungiparasiticonfungi Some mainly microscopic fungi have opted for the mycoparasitic life style, and they live as parasites on other fungi. The host fungi are macro- or microfungi, saprophyticorparasitesofplants.Inthelattercase,the mycoparasitic fungi are called hyperparasites. A com- monhyperparasiteofrustsisSphaerellopsisfilum,anim- 47 perfect fungus which develops pycnidia in sori of rust fungi(Fig.45). 188