12/08/2019

Elaphomyces Solioccasus aurantius polychromus

Trappe et al. 2013 Mycologia 105: 888-895 Castellano et al. 2011 Australian Systematic Botany 24: 32-57 Macrolepiota biodiversity and turbinata angustispora distribution

Lebel and Syme 2012 Mycologia 104: 496-520 http://www.natruffling.org/gaa Susan Nuske PhD n.htm Cortinarius SLU, Umeå Rossbeevera Aroramyces argyrionus sp. paracyanea squarepantsii gelatinosporus

© Susan Nuske © Susan Nuske Orihara et al 2016 Persoonia 37: 173-198 Desjardin et al 2011 Mycologia 103: 1119-1123 © Susan Nuske Danks et al. 2010 Persoonia 24: 106- 126 © Susan Nuske

Content A confusion of terms

• What is a truffle? •Gastioid vs Gasteroid •Sequestrate vs Secotioid • Major truffle groups

• Why are endangered mammals important for truffle diversity in •Hypogeous and epigeous Australia?

•What is a truffle!?

Solioccasus Elaphomyces aurantius Cortinarius argyrionus polychromus Major truffle groups • • Trappe et al. 2013 Mycologia Eurotiales e.g. Elaphomyces Castellano et al. 2011 105: 888-895 • ”SEQUESTRATE - describes fungal fruit bodies which have evolved • e.g. Tuber, Amalyscus Australian Systematic Botany Danks et al. 2010 Persoonia 24: 32-57 24: 106-126 from exposed hymenia and forcibly discharged to a closed or • Aroramyces gelatinosporus Gautieria angustispora even hypogeous habit in which the spores are retained in the fruit • e.g. Cortinarius (Thaxterogaster) Mesophellia sp. • e.g. , Solioccasus body until it decays or is eaten by an animal vector. Many sequestrate • e.g. taxa can be clearly recognized as being derived from specific - • e.g. Gautieria • e.g. Mesophellia, shooting ancestors, e.g. Rhizopogon from Suillus ().” © Susan Nuske http://www.natruffling.org/ • e.g. Claustula © Susan Nuske gaan.htm chartaceus • Russuales e.g. Zelleromyces, Macowanites Gymnohydnotrya sp. • Glomeromycota (Arbuscular Bonito et al 2013 PLoS ONE 8: e52765 • http://www.mycolog.com/fifthtoc.html mycorrhizae/Endomycorrhizae) • • Diversisporales e.g. Gigaspora Kendrick, B. (1992). ‘The Fifth Kingdom.’ (Focus Information Group, • Glomales e.g. Glomus Inc.: Newburyport.) • Zygomycota • Endogonales e.g. Endogone

Lebel and Syme 2012 Mycologia 104: 496-520

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Truffle evolution Not a truffle but still sequestrate…? Gasteroid: often epigeous and Epigeous becomes infolded and enclosed have a powdery and some becomes remnant or lost form of dehiscence of the Lack of forcible spore discharge peridium (where the peridium falls away or erodes at maturity). (Sheedy et al 2016 Australian Systematic Botany29: 284-302) Hypogeous

Mushroom ancestor Gastioid = truffle (sometimes Secotioid)

Secotioid

Gastioid

Sequestrate Wilson et al 2011 Evolution © Susan Nuske 65: 1305-1322

Basidiomata Basidiomycota spores

Peridium Non-: • Mechanisms for forcible discharge Ornamentation of spores are caused by changes in Gleba surface tension of liquid on the (Hymenium) spore and spore attachment Stipe • This mechanism requires asymmetrical spores with hilar appendages ( ) and curved sterigmata (spore attachment ) Hilar appendage/ Apiculus

Peglar and Young 1979 Transactions of the British Truffles are loosing these features! Mycological Society 72: 353-388 Pringle et al 2005 Mycologia 97: 866-871

Truffle spores don’t actively release

Non-truffle spore release

Peglar and Young 1979 Transactions of the British Mycological Society 72: 353-388

Peglar and Young 1979 Transactions of the British Mycological Society 72: 353-388

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”Ascomycete truffles can be Ascocarp Asci defined as producing sporocarps below or at ground level and with a simultaneous loss of active Ascospores spore dispersal” Læssøe and Hansen 2007 Mycological Research 111- 1075-1099

Hymenium

Bonito et al. 2013 PLoS ONE 8: e52765 Bonito et al. 2013 PLoS ONE 8: e52765

Solioccasus Elaphomyces aurantius Cortinarius argyrionus polychromus Exceptions to the rule Major truffle groups • Ascomycota • Trappe et al. 2013 Mycologia Eurotiales e.g. Elaphomyces Castellano et al. 2011 105: 888-895 Geopora cooperi • Pezizales e.g. Tuber, Amalyscus Australian Systematic Botany Danks et al. 2010 Persoonia 24: 32-57 24: 106-126 • Basidiomycota Aroramyces gelatinosporus Gautieria angustispora • Agaricales e.g. Cortinarius (Thaxterogaster) Mesophellia sp. • Boletales e.g. Rhizopogon, Solioccasus • Geastrales e.g. Geastrum Læssøe and Hansen 2007 Mycological Research 111- 1075-1099_Figure7E • Gomphales e.g. Gautieria • Hysterangiales e.g. Mesophellia, Hysterangium ”The animal bites or breaks open the ascocarp, and a cloud of © Susan Nuske http://www.natruffling.org/ • Phallales e.g. Claustula © Susan Nuske gaan.htm Agaricus chartaceus ascospores results as the asci (nearly) simultaneously eject their • Russuales e.g. Zelleromyces, Macowanites Gymnohydnotrya sp. spores.” • Glomeromycota (Arbuscular Bonito et al 2013 PLoS ONE 8: e52765 mycorrhizae/Endomycorrhizae) Korf 1973 Repertorium Tottori Mycological Institute 10: 389-403 • Diversisporales e.g. Gigaspora • Glomales e.g. Glomus • Zygomycota • Endogonales e.g. Endogone

Lebel and Syme 2012 Mycologia 104: 496-520

Pseudotulostoma volvatum Eurotiales Elaphomycetaceae

• Ascomycota • Elaphomyces http://tropicalfungi.org/guiana-shield/special-notes-on-fruiting-habit/ • Eurotiales – 1 truffle family and another Elaphomyces • ”the deer truffles” with uncertain placement aurantius • Epigeous relatives: Pseudotulostoma • Elaphomycetaceae, Elaphomyces • Worldwide distributions, ECM • Diehliomyces • Key features: • Pezizales e.g. Tuber, Amalyscus • Thick, multi-layered peridium

Castellano et al. 2011 Australian Systematic • Often brightly coloured hyphae mixed with brown or Botany 24: 32-57 black • Powdery spore mass • Spores spherical and ornamented

Castellano et al. 2011 Australian Systematic Botany 24: 32-57

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Paz et al 2017 Persoonia 38: 197-239 Castellano et al. 2011 Australian Systematic Botany 24: 32-57 Elaphomyces muricatus var. muricatus Elaphomyces queenslandicus

Elaphomyces muricatus var. reticulatus

Elaphomyces muricatus var. variegatus

Amalyscus sp. Gymnohydnotrya sp. Bonito et al 2013 PLoS ONE 8: e52765 Truffle as a weed… Pezizales • Diehliomyces microspores • Ascomycota © Susan Nuske Bonito et al 2013 PLoS ONE (Eurotiales, Ascomycota) is a • Eurotiales 8: e52765 ‘weed’ on Agaricus spp. • Pezizales ~10 Families cultivations • Ascobolaceae, Carbomycetaceae, Discineaceae,

• Most common competitor to A. Glaziellaceae, , Morchellaceae, Helvella lacunose brasiliensis Otideaceae, , Pyronemataceae, coronaria • Never recorded in the wild • 52 Genera, 100’s species • Proposed for Red Listing due to • e.g. Tuber, Amalyscus effective management Tuber sp. Tuber canaliculatum Hydnobolites cerebriformis Terfezialeptoderma

Laessoe and Hansen 2007 Mycological Research 111: 1075-1099 Bonito et al 2013 PLoS ONE 8: e52765

Luteoamylascus aculeatus http://mycoportal.org/portal/collections/in dividual/index.php?occid=4776533 Bonito et al 2013 PLoS ONE 8: e52765 Tuberaceae Pezizaceae Nothojafnea thaxteri • Tuber: 180 species Cabero et al 2016 Mycological Progress 15: 33 • At least 17 Genera Kovács et al 2008 Mycologia 100: 930-939 • Epigeous relatives: Nothojafnea thaxteri • Epigeous relatives: cup fungi Mycoclelandia arenacea • Worldwide distributions, ECM • Distinct Northern and Southern hemisphere Tuber canaliculatum Tuber sp. • Worldwide distribution linages Underwoodia singer • Including desert truffles (Africa and Australia) Labyrinthomyces sp. • North: Tuber, Choiromyces Truffle hunter holding a Kalahari truffle • South: Labyrinthomyces, Dingleya, Trappe et al 2008 Economic Botany 62: 521-529 Trappe et al 2008 Economic Botany 62: 497-506 Reddollomyces Amylascus © Susan Nuske • https://ascomycete.org/2000- Key features: Pezizales/Species/Underwoodia- singeri?mapid=653#prettyPhoto • Spherical or irregularly shaped asci with few spores (<8) • (Tuber) Spore ornamentation either honey- comb-like, spines or spines connected by ridges Hansen et al 2001 Mycologia 93: 958-990 Hansen et al 2001 Mycologia 93: 958-990

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3 types of Elaphomyces aurantius Ptchothecia Peziza ellipsospora Peziza whitei hypogeous Major truffle groups Pezizaceae • Ascomycota • Eurotiales e.g. Elaphomyces Castellano et al. 2011 • Pezizales e.g. Tuber, Amalyscus Australian Systematic Botany Asci 24: 32-57 • Basidiomycota • Agaricales e.g. Cortinarius (Thaxterogaster) Hansen et al 2001 Mycologia 93: 958-990 • Boletales e.g. Rhizopogon, Solioccasus Spores • Geastrales e.g. Geastrum © Susan Nuske • Gomphales e.g. Gautieria • Hysterangiales e.g. Mesophellia, Hysterangium Exothecium Stereothecia Hydnotryopsis setchellii Ruhlandiella berolinensis • Phallales e.g. Claustula • Russuales e.g. Zelleromyces, Macowanites Gymnohydnotrya sp. • Glomeromycota (Arbuscular Bonito et al 2013 PLoS ONE 8: e52765 mycorrhizae/Endomycorrhizae) • Diversisporales e.g. Gigaspora • Glomales e.g. Glomus • Zygomycota • Endogonales e.g. Endogone Hansen et al 2001 Mycologia 93: 958-990 Hansen et al 2001 Mycologia 93: 958-990

Solioccasus Cortinarius argyrionus polychromus Major truffle groups Basidiomycota, Agaricales • Ascomycota Trappe et al. 2013 Mycologia • Eurotiales e.g. Elaphomyces 105: 888-895 • Pezizales e.g. Tuber, Amalyscus Danks et al. 2010 Persoonia • Basidiomycota 24: 106-126 • Basidiomycota • Agaricales – 13 families Aroramyces gelatinosporus Mesophellia sp. Gautieria angustispora • Agaricales e.g. Cortinarius (Thaxterogaster) • , Amanitaceae, Bolbitaceae, Coprinaceae, , Entolomataceae, • Boletales e.g. Rhizopogon, Solioccasus Hydnangiaceae, , Inocybaceae, Lepiotaceae, Physalacriaceae, • Geastrales e.g. Geastrum Strophariaceae, Tricholomataceae • Gomphales e.g. Gautieria • Hysterangiales e.g. Mesophellia, • Boletales e.g. Rhizopogon, Solioccasus Cortinarius argyrionus Hysterangium © Susan Nuske http://www.natruffling.org/ • • Phallales e.g. Claustula © Susan Nuske gaan.htm Geastrales e.g. Geastrum • Russuales e.g. Zelleromyces, Macowanites Agaricus chartaceus • Gomphales e.g. Gautieria • Glomeromycota (Arbuscular • Hysterangiales e.g. Mesophellia, Hysterangium mycorrhizae/Endomycorrhizae) • Phallales e.g. Claustula • Diversisporales e.g. Gigaspora Danks et al. 2010 Persoonia 24: 106-126 • Glomales e.g. Glomus • Russuales e.g. Zelleromyces, Macowanites • Zygomycota • Endogonales e.g. Endogone

Lebel and Syme 2012 Mycologia 104: 496-520

Truffles in Agaricaceae Agaricaceae Australian arid taxa: Agaricus, Barcheria, • Sequestrate represents found in arid Australia, Lepiota/ Macrolepiota, Podaxis Americas, Central Asia and Europe Cryptolepiota spp. • At least 17 genera, mostly stipate, semi- Macrolepiota gasteroidea Macrolepiota turbinata hypogeous - epigeous species • Mostly not Ectomycorrhizal

• Morphology varied, often need molecular data Kropp et al 2012 Mycologia 104: 164-174 Barcheria willisiana for placement (Within genera there might be Macrolepiota dolichaula clues) Macrolepiota turbinata

Agaricus chartaceus Agaricus semotus Agaricus chartaceus

Lebel and Syme 2012 Mycologia 104: 496-520

Macrolepiota vinaceofibrillosa

Lebel and Syme 2012 Mycologia 104: 496-520 Agaricus eburneocanus Agaricus erythrosarx Lebel and Syme 2012 Mycologia 104: 496-520 https://mushroomobserver.org/92395 Rizal et al 2016 Chiang Mai Journal of Science 43: 959-971

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Cortinariaceae Truffles evolved many times on Cortinarius Cortinarius, Descolea and Hebeloma. • ‘Spindelskivling’ in Swedish Old generic names: Thaxterogaster, Quadrispora, Protoglossum, • Worldwide, Sequestrate represents remyi and H. diverse in Australia, New Zealand sublilacinus • Key features are: • Cortina – thin ‘spider-web-like’ hyphae that join the cap to the stipe and is can be remnant on the peridium of truffle Cortinarius • Brown spores with rounded apex and ornamented

Danks et al. 2010 Persoonia Soop 2003 Jordstjärnan 24: 24: 106-126 28-43

Cortinarius Danks et al. Cortinarius basorapulus Cortinarius 2010 Persoonia argyrionus argyrionus 24: 106-126

Cortinarius Cortinarius Cortinarius caesibulga cinereoroseolus caesibulga

Cortinarius Cortinarius Cortinarius kaputarensis maculobulga kaputarensis

Cortinarius Cortinarius nebulobrunneus sinapivelus

Basidiomycota, Boletales Boletaceae Solioccasus polychromus

• Basidiomycota Rossbeevera paracyanea • At least 20 genera, many species • Agaricales Trappe et al. 2013 Mycologia 105: 888-895 • Boletales – 10 families • Related to ‘pored’ • Boletaceae, Gomphidiaceae, Hymenogastraceae, Paxillaceae, , • Australia, New Zealand, Asia, Americas, Europe Orihara et al 2016 Persoonia 37: 173-198 , Sclerogastraceae, Serpulaceae, Strobilmycetaceae, Suillaceae • Geastrales e.g. Geastrum • Many new genera discovered in Africa Royoungia sp. • Gomphales e.g. Gautieria • Key features (often varies, need molecular data): • Hysterangiales e.g. Mesophellia, Hysterangium • Soft bodied, often bright colours • Phallales e.g. Claustula • Peridium (outer layer of truffle) may or may not be fully formed Solioccasus polychromus • Russuales e.g. Zelleromyces, Macowanites • Spores spherical – cylindrical, with/without ornaments

Trappe et al. 2013 Mycologia 105: 888- 895 Smith et al 2015 IMAFungus 6: 297-317 Orihara et al 2016 Persoonia 37: 173-198

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Leccinum versipelle Orihara et al Orihara et al Turmalinea Turmalinea 2016 Persoonia 2016 Persoonia persicina yuwanensis 37: 173-198 37: 173-198

Turmalinea Turmalinea http://svampguiden.com/art/visa/leccinum_versipelle persicina chrysocarpa Leccinellum griseum

Turmalinea Turmalinea mesomorpha mesomorpha subsp. subsp. sordida mesomorpha

Rossbeevera Rossbeevera paracyanea cryptocyanea https://commons.wikimedia.org/wiki/Category:L eccinellum_griseum#/media/File:Leccinellum_gri seum_(29072167986).jpg

Gymnogaster boletoides Spongiforma squarepantsii

Desjardin et al 2011 Mycologia 103: 1119-1123 Gelardi et al 2017 Austrobaileya 10: 121-129

Hysterangiales Gomphales Basidiomycota, Hysterangiales Turbinellus • Ancient group – all truffles Gautieria angustispora • Basidiomycota • Share common ancestor with • Agaricales Gomphales and Phallales

• Boletales http://www.natruffling.org/gaa n.htm • Geastrales © Susan Nuske Phallales • Gomphales Mesophellia Phaeoclavulina Lysurus sphaerocephalum Restingomyces reticulatus • Hysterangiales – 5 families Ramaria • Gallaceaceae, , , Phallogastraceae, Trappeaceae • Phallales e.g. Claustula • Russuales e.g. Zelleromyces, Macowanites Sulzbacher et al 2016 Mycologia 108: 954-966 Claustula fischeri

Hernández Caffot et al 2018 Mycologia 110: 419-433

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Castoreum Gummiglobus Hysterangiaceae Hysterangium inflatum Mesophelliaceae • At least 8 genera • At least 2 genera, probably more • Global distribution: Australia, New Zealand, Asia, • Australasian endemic, ECM with Eucalyptus Africa, Americas, Europe • Introduced elsewhere with plantations © Susan Nuske © Susan Nuske • Local endemism: Northern hemisphere taxa © Susan Nuske • Common in diets of Australian mammals distinct from southern Hysterangium ‘pink’ • pachysporus • Main characteristics: Multi-modal dispersal • ‘Gelatinous’ texture • Main characteristics: • Peridium multi-layered microscopically • Powdery spores • Spores cylindrical, with/without ornaments, • Peridium multi-layered with/without utricle (spore membrane) • Spores cylindrical, with/without ornaments © Susan Nuske © Susan Nuske • Hyphae has unique characteristics (e.g. Aroramyces herrerae Aroramyces gelatinosporus Gummiglobus) Mesophellia Gummivena potorooi

Sulzbacher et al 2010 Mycotaxon 113: 377-384 © Susan Nuske Guevara-Guerrero et al 2016 IMA 7: 235-238 Trappe and Bougher 2002 Australasian Mycologist 21: 9-11 © Susan Nuske

Basidiomycota, Russuales

Macowanites sp. • Basidiomycota • Agaricales • Boletales • Geastrales • Gomphales • Hysterangiales © Susan Nuske • Phallales • Russuales – 3 families • , , Stephanosporaceae

© Susan Nuske

Solioccasus Cystangium sp. Russulaceae Cortinarius argyrionus polychromus Major truffle groups • 7 genera • Ascomycota Trappe et al. 2013 Mycologia © Susan Nuske • Eurotiales e.g. Elaphomyces 105: 888-895 • Russula, are the relatives • Pezizales e.g. Tuber, Amalyscus Danks et al. 2010 Persoonia 24: 106-126 Lactarius angiocarpus • Basidiomycota Aroramyces gelatinosporus Gautieria angustispora • Global distribution with centres of diversity in • Agaricales e.g. Cortinarius (Thaxterogaster) Mesophellia sp. Australasia • Boletales e.g. Rhizopogon, Solioccasus • Geastrales e.g. Geastrum • Major characteristics: • Gomphales e.g. Gautieria • ’fleshy’ • Hysterangiales e.g. Mesophellia, Eberhardt and Verbeken 2004 Mycological Research 108: 1042-1052 Hysterangium © Susan Nuske http://www.natruffling.org/ • Spherical, ornamented spores that react with iodine to • Phallales e.g. Claustula © Susan Nuske gaan.htm become blue-black (amyloid reaction) • Russuales e.g. Zelleromyces, Macowanites Agaricus chartaceus © Susan Nuske Zelleromyces sp. • Glomeromycota (Arbuscular Cystangium spp. spores mycorrhizae/Endomycorrhizae) Macowanites sp. • Diversisporales e.g. Gigaspora • Glomales e.g. Glomus

Trierveiler-Pereira et al. 2015 Mycologia 107: 90- • Zygomycota 103 • Endogonales e.g. Endogone © Susan Nuske © Susan Nuske Lebel and Syme 2012 Mycologia 104: 496-520

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Endogone corticioides Glomeromycota Zygomycota (Arbuscular • Endogonales e.g. Endogone mycorrhizae/ • Ectomycorrhizal Endomycorrhizae) • Spores are big!

Endogone Glomus megalocarpum flammicorona • Diversisporales e.g. Glomus fulvum Endogone lactiflua Gigaspora • Glomales e.g. Glomus

• Associate with >80% of all plants

• Key features • Small fruiting bodies http://www.natruffling.org/ Yamamoto et al 2017 Mycoscience 58: 23-29 • Spores are big! > 60 µm Redecker et al 2007 Mycological Progress 6: 35-44

Solioccasus Elaphomyces aurantius Cortinarius argyrionus polychromus Recap! Major truffle groups

Trappe et al. 2013 Mycologia 105: Danks et al. 2010 Persoonia 24: 106- 888-895 Castellano et al. 2011 Australian • Ascomycota 126 Systematic Botany 24: 32-57 • Eurotiales e.g. Elaphomyces • Pezizales e.g. Tuber, Amalyscus Aroramyces gelatinosporus Gautieria angustispora • Basidiomycota Mesophellia sp. • Agaricales e.g. Cortinarius (Thaxterogaster) • Boletales e.g. Rhizopogon, Solioccasus • Geastrales e.g. Geastrum • Gomphales e.g. Gautieria

• Hysterangiales e.g. Mesophellia, Hysterangium © Susan Nuske http://www.natruffling.org/gaa • Phallales e.g. Claustula © Susan Nuske n.htm • Russuales e.g. Zelleromyces, Macowanites Agaricus chartaceus Gymnohydnotrya sp. • Glomeromycota (Arbuscular mycorrhizae) Bonito et al 2013 PLoS ONE 8: e52765 • Diversisporales e.g. Gigaspora • Glomales e.g. Glomus • Zygomycota • Endogonales e.g. Endogone

Lebel and Syme 2012 Mycologia 104: 496-520

Solioccasus Elaphomyces Elaphomyces aurantius Cortinarius argyrionus polychromus Major truffle groups Truffles! aurantius Tuber canaliculatum • Ascomycota • Trappe et al. 2013 Mycologia Eurotiales e.g. Elaphomyces Castellano et al. 2011 105: 888-895 • Pezizales e.g. Tuber, Amalyscus Australian Systematic Botany Danks et al. 2010 Persoonia • Ascomycota 24: 32-57 24: 106-126 • Basidiomycota Aroramyces gelatinosporus Mesophellia sp. Gautieria angustispora • Agaricales e.g. Cortinarius (Thaxterogaster) Castellano et al. 2011 Australian Bonito et al 2013 PLoS ONE 8: e52765 • Boletales e.g. Rhizopogon, Solioccasus Systematic Botany 24: 32-57 • Geastrales e.g. Geastrum • Gomphales e.g. Gautieria Peziza ellipsospora • Hysterangiales e.g. Mesophellia, Peziza whitei Hysterangium © Susan Nuske http://www.natruffling.org/ • Phallales e.g. Claustula © Susan Nuske gaan.htm Agaricus chartaceus • Russuales e.g. Zelleromyces, Macowanites Gymnohydnotrya sp. • Glomeromycota (Arbuscular Bonito et al 2013 PLoS ONE 8: e52765 mycorrhizae/Endomycorrhizae) • Diversisporales e.g. Gigaspora • Glomales e.g. Glomus • Zygomycota Hansen et al 2001 Mycologia 93: 958-990 • Endogonales e.g. Endogone

Lebel and Syme 2012 Mycologia 104: 496-520

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Major truffle groups Major truffle groups • Ascomycota • Ascomycota • Eurotiales – Elaphomycetaceae –Elaphomyces • Pezizales • Round, ornamented spores • Tuberaceae – Tuber • Tough, leathery peridium (‘skin’) • Powdery spore-mass Tuber canaliculatum • Pezizaceae • Epigeous relatives: cup fungi • Spores from cyclindrical or sac-shaped asci

Asci

Spores

Macrolepiota turbinata Solioccasus Aroramyces gelatinosporus Elaphomyces aurantius Cortinarius argyrionus polychromus Major truffle groups Truffles!

Trappe et al. 2013 Mycologia 105: Danks et al. 2010 Persoonia 24: 106- 888-895 Castellano et al. 2011 Australian • Ascomycota 126 • Ascomycota Systematic Botany 24: 32-57 © Susan Nuske • Eurotiales e.g. Elaphomyces • Pezizales e.g. Tuber, Amalyscus • Basidiomycota Lebel and Syme 2012 Mycologia 104: 496-520 Aroramyces gelatinosporus Gautieria angustispora • Basidiomycota Mesophellia sp. Hilar Solioccasus • Agaricales e.g. Cortinarius (Thaxterogaster) appendage/ polychromus • Boletales e.g. Rhizopogon, Solioccasus Apiculus • Geastrales e.g. Geastrum Peglar and Young 1979 Transactions • Gomphales e.g. Gautieria of the British Mycological Society 72: • Hysterangiales e.g. Mesophellia, Hysterangium © Susan Nuske http://www.natruffling.org/gaa 353-388 • Phallales e.g. Claustula © Susan Nuske n.htm Trappe et al. 2013 Mycologia 105: 888-895 • Russuales e.g. Zelleromyces, Macowanites Agaricus chartaceus © Susan Nuske Gymnohydnotrya sp. Cortinarius argyrionus • Glomeromycota (Arbuscular mycorrhizae) Bonito et al 2013 PLoS ONE 8: e52765 Lactarius angiocarpus • Diversisporales e.g. Gigaspora • Glomales e.g. Glomus • Zygomycota • Endogonales e.g. Endogone

Danks et al. 2010 Persoonia 24: 106-126 Eberhardt and Verbeken 2004 Mycological Research 108: 1042-1052 Lebel and Syme 2012 Mycologia 104: 496-520

Major truffle groups Major truffle groups

• Basidiomycota • Basidiomycota • Agaricales – Cortinariaceae -- Cortinarius • Boletales -- Rhizopogon, Bolete • Brown spores • Mushroom with pores instead of gills • ‘Spindelskivling’ in Swedish = Cortina – thin • Spores often cylindrical and fatter at one ‘spider-web-like’ hyphae end • Smooth, shiny peridium • Some groups have no peridium

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Major truffle groups

• Basidiomycota • Russuales – Russula, Zelleromyces, Macowanites • Mushrooms with fleshy gills and stipe • Round, ornamented spores

Ectomycorrhizal fungi Truffles vs mushrooms (and other forms for dispersal)

• Symbiotic with plants • Plant health • Nutrient cycling (C, N, P) http://www.tuber.it/en/tartufo.php • Plant diversity © Susan Nuske

http://www.tomentella.de

Leake et al. 2001. Tree Physiology (21): 71-82)

World-wide Fungi-Lovers Many mammals eat fungi, although not equally

• Bank Voles (Myodes glareolus) in Europe: Austria and Lithuania Fungi specialists: Potoroos and Bettongs Fungi generalists (Kataržytė and Kutorga 2011; Schickmann et al. 2012) (2 exceptions: Aepyprymnus rufescens and Bettongia lesueur)

• (Glaucomys sabrinus) (Flaherty et al. 2010) and Red-back Vole (Clethrionomys californicus) in North America (Hayes et al. 1986)

http://kleinsaeuger.at/myodes-glareolus.html; http://photorator.com/photo/29741/bank-vole-myodes-glareolus-; http://nicbutler.weebly.com/; http://www.raywilsonbirdphotography.co.uk/Galleries/Mammals/Bank%20Vole.html http://www.qm.qld.gov.au , http://wetlandinfo.ehp.qld.gov.au

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Mammals, truffles and The decline of Australian mammals plants

• Australia has the highest rate of mammal extinction and decline, including fungal specialists! • 3 species of are Extinct • Potorous gilbertii – Critically endangered • P. longipes – Vulnerable • P. tridactylus – Near Threatened © Susan Nuske • Bettongia gaimardi – Near Threatened • B. penicillata – Critically Endangered • B. tropica - Endangered

Functional redundancy Do fungal specialists perform a unique fungal dispersal role compared to fungal generalists?

• Can a diverse group of • Hypotheses: mammalian generalists • Bettongs and Potoroos contribute disproportionally more to the dispersal of compensate for the lose of a ≈ fungi than other mammal species fungal specialist? • Some fungal generalists will contribute more to dispersal of fungi than others

Bush rat Long-nosed potoroo

≈ ?

http://wetlandinfo.ehp.qld.gov.au © Susan Nuske Giant white-tailed rat Northern brown bandicoot Specialist Northern bettong Generalists

Meta-analysis Seasonality of fungi in mammal diets

100

90 b b Bettongs and Potoroos eat more 80 b 70 b fungi than other food across all

60 seasons compared to (methods criteria) 50 - Rats and Mice* Australian mammal species’ diets ab a ab 40 a P ≤ 0.004 ( ) • Fungal taxa P=0.04 a - Bandicoots * 30 P ≤ 0.001 P=0.03 a • a Fungal abundance within diet 20 a

relative food other to relative Nuske et al 2017 Fungal • Frequency of fungi within diets 10

Mean abundance of fungi fungi of abundance Mean Ecology 27: 1-13 • Seasonality 0 Nuske et al 2017 Data in • Location Summer Autumn Winter Spring Brief 12: 251-260 Muridae (5) Peramelidae (3) Potoriodae (5)

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Patterns influencing fungal diversity in diets Northern Bettong case study

Despite Potoroidae having more references and samples, they still Does the Northern Bettong eat more fungal species contribute disproportionally more to Variable p-value the dispersal of fungi than aim of study did not include mycophagy 0.4416 aim of study included mycophagy 0.9807 generalist mammals? number of samples 0.0075* number of references 0.0000* mammal family Hypsiprymnodontidae 0.7077 Macropodidae 0.9274 Muridae 0.4595 Nuske et al 2017 Fungal Peramelidae 0.0594 Ecology 27: 1-13 Phalangeridae 0.0247* Figure from Bateman Nuske et al 2017 Data in Potoroidae 0.0482* et al. 2011, Australian Brief 12: 251-260 Thylacomyidae 0.8684 Journal of Zoology

Whole community sampling via high throughput Mean number of OTUs per sample sequencing

• >300 Scats All OTUs ECM OTUs Truffle OTUs • Tree roots and soil Mammal species N Mean ± se (total) N Mean ± se (total) N Mean ± se (total) • DNA sequencing • Illumina MiSeq (collaboration with Specialist 93 188.1 ± 9.34b (4176) 92 10.0 ± 0.75b (254) 89 8.6 ± 0.80b (135) University of Tartu) Generalists 120 101.2 ± 8.25a (5266) 108 4.1 ± 0.32a (159) 85 3.8 ± 0.44a (73)

a,b: Different superscript letters represent significant differences in Tukey HSD comparisons between B. tropica and generalist mammal species (P < 0.05).

Dr. Leho Tedersoo, Sten Anslan Nuske et al. 2018 Molecular Ecology

Truffle OTUs Zyzomys Trichosurus argurus vulpecula Antechinus Uromys flavipes Isoodon Isoodon caudimaculatus Unique OTUs macrourus obesulus Bettongia tropica Rattus sp. Perameles nasuta Melomys sp.

All Fungi ECM Fungi Truffle Fungi Northern Northern Northern Bettong Generalists Bettong Generalists Bettong Generalists

Northern Bettongs eat more unique ectomycorrhizal and truffle fungi species

These fungal species are not dispersed by generalists Rhizopogonaceae Tuberaceae Boletaceae Hysterangiaceae Mesophelliaceae Pyronemataceae Russulaceae Strophariaceae Gallaceaceae Nuske et al. 2018 Molecular Ecology Nuske et al. 2018 Molecular Ecology Stephanosporaceae

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Truffle OTUs Nuske et al. 2018 Molecular Ecology Data Chapter 1 Fungal community structure Relative abundance Dominant root-associating taxa included truffles >90% of relative abundance

Chondrogaster Hysterangium © Susan Nuske © Susan Nuske © Susan Nuske Cortinarius Mesophellia © Susan Nuske These taxa were in mammal diets Nuske et al. 2018

Overall conclusions

Fungal specialists perform unique fungal dispersal roles compared to fungal generalists

© Susan Nuske

Endemic 83 genera 294 species sequestrate taxa: Estimated 12-23 % of all 35 % genera species described 95 % species ~1287-2450 species (Bougher and Lebel 2001)

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A hypothesis worthy of testing…

http://alert-conservation.org/issues-research-highlights/2015/10/16/bushland-destruction-escalates-in-queensland-australia

http://www.abc.net.au/news/2016-03-01/northern-bettong/7208426

AVH

The Australasian Virtual Herbarium

- All fungi Andrew et al. 2017 Fungal Biology - Named to genus Reviews 31(2): 88-98 - Good spatial records “ClimFun” database

South-east Queensland

- Macro-fungi Angiosperm records Fungi records - Preserved specimen - Named to genus or species

Image kindly supplied by Megan Prance, BRI, Queensland herbarium Images kindly supplied by Megan Prance, BRI, Queensland herbarium

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How do we know to conserve the unknown? Indirect evidence for threatened truffle species

• We don’t have species distributions • Land clearing… • Mammal decline… • We don’t have evidence of population declines

• We have an adequate understanding of species’ habitat requirements • Changed fire regimes • Nutrient population • We don’t know which species have gone extinct • Erosion • Plant invasions • Invasive non-native mammals

Evans 2016 Pacific Conservation Biology 22(2): 130-150 Evans 2016 Pacific Conservation Biology 22(2): 130-150

What does this history of land clearing mean How do we verify directly that truffle taxa are for fungi? declining? • Large areas of vegetation loss = populations of ECM fungi lost • Population genetics • Increase in population fragmentation • Lack of new recruitment • Meta-genomics • Loss of vectors (mammalian specialists) • More structured surveys

• Ecological experiments

• Utilising natural variation as an ecological experiment…

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