Heimioporus (Boletineae) in Australia

Australasian Mycologist (2011) 29

Roy E. Halling1,3 and Nigel A. Fechner2

1Institute of Systematic Botany, The New York Botanical Garden, Bronx, New York 10458, United States of America. 2Queensland Herbarium, Brisbane Botanic Garden, Mt Coot-tha Road, Toowong, Brisbane, Queensland 4066, Australia. 3Author for correspondence. Email: [email protected]. Abstract Two species of Heimioporus are fully documented, described and illustrated from recent collections gathered in Queensland. While H. fruticicola is known only from Australia so far, the specimens of H. japonicusMYVT-YHZLY0ZSHUKHUK*VVSVVSHYLWYLZLU[HUL^YLWVY[HUKZPNUPÄJHU[YHUNLL_[LUZPVUMVY this bolete. Key words: Boletes, mycorrhizae, Australia, biogeography.

Introduction Materials and Methods

Heimioporus^HZWYVWVZLKI`/VYHRHZHUL^ General colour terms are approximations, and the colour name to replace the bolete genus Heimiella Boedijn non codes (e.g., 7D8) are page, column, and row designations 3VOTHUU (ZTHU`HZZWLJPLZ^LYLPUJS\KLK from Kornerup & Wanscher (1983). All microscopic observations were made with an Olympus BHS compound I` /VYHR I\[ HZ LU]PZHNLK OLYL [OL NLU\Z microscope equipped with Nomarski differential interference circumscribes 10 species. These have olive-brown contrast (DIC) optics, and measurements were from dried spores which are alveolate-reticulate to reticulate or with TH[LYPHSYL]P]LKPU 26/;OLHIIYL]PH[PVU8YLMLYZ[V[OL pit-like perforations, extremely rarely rugulose and then mean length/width ratio measured from n basidiospores, and with crater–like pits; they are elongate-ellipsoid to short x refers to the mean length × mean width. Scanning electron LSSPWZVPK HUK SHJR H Z\WYHOPSHY WSHNL )VLKPQU micrographs of the spores were captured digitally from a included only the type species of his genus (Boletus Hitachi S-2700 scanning electron microscope operating at retisporus Pat. & C.F. Baker) in the circumscription. The 20 kV. Hymenophoral fragments were removed from dried main feature emphasised by Boedijn was the subovoid, basidiomata, mounted directly on aluminum stubs using carbon adhesive tabs, and coated with 10 nm of gold using reticulated spores. Later, Heim (1963), Hongo (1969, a Hummer II sputter coater. Herbarium acronyms are those *VYULY HUKAHUN KLZJYPILK designated in the online version of Index Herbariorum (Thiers, some new species. Singer et al. (1983) described H. continuously updated). ivoryi from Belize (as a Boletellus), while Watling (2000) and Watling & Hollands (1990) described additional Taxonomy taxa and provided some re-alignment to the genus with Key Macroscopic Features known species (e.g., H. betula, H. fruticicola). During this time, Heimioporus was accepted reluctantly by Corner 1a. Pileus matted subtomentose; (1972; as Heimiella, for the six species known to him) stipe pseudo-reticulate to who noted no clearly demarcated adaxial patch (plage) subpruinose-ridged to subscabrous H. fruticicola compared with Strobilomyces. While that comparison 1b. Pileus subvelutinous; stipe seems an odd one, given that the spores share only a coarsely but shallowly lacerate- reticulate ornamentation, other Boletineae do show an ridged with a dense red pruina adaxial plage area. In contrast, Singer (1986, and earlier overlaying the ridges H. japonicus editions) did not accept segregation from Boletellus and placed all of those reticulate spored taxa into Heimioporus fruticicola (Berk.) E. Horak, Sydowia 56: Boletellus along with others that have smooth and/or ribbed spores. Recently, strict consensus phylogenetic -PNZ(*¶+*¶+ analyses obtained by Osmundson (2009) using three Boletus fruticicola Berk., London J. Bot ! gene loci (nucLSU, atp6, tef1) clearly infer Boletellus and Heimioporus as separate genera. Heimioporus Suillus fruticicola (Berk.) Kuntze, Rev. Gen. Pl. 3(2): fruticicola is the only species of the genus known from Australia so far. On the basis of recent collections, Austroboletus fruticicola (Berk.) E. Horak, Sydowia we can now provide a more detailed description of 33: 76. 1980. H. fruticicola, and a new record of H. japonicus as Heimiella fruticicola (Berk.) Watling & Hollands, occurring in Australia. Notes Roy. Bot. Gard. Edinburgh! 4`JVIHUR!4)

Fig. 1. Habits of Heimioporus. A Heimioporus fruticicola (Halling 8970) × 1. B Heimioporus japonicus (Halling 9288) × 1. C Stipe surface detail of H. japonicus/HSSPUN í Fig. 2. (next page left) Light micrographs with Nomarski Fig. 3. (next page right) Scanning electron micrographs of DIC of spores of Heimioporus. A H. japonicus (holotype). B spores of Heimioporus. A–B H. japonicus (Halling 9288). C–D H. japonicus (Halling 9288). C H. fruticicola (holotype). D H. H. fruticicola/HSSPUN :JHSLIHYZ$T fruticicola/HSSPUN :JHSLIHYZ$T © 2011 Australasian Mycological Society Inc. Australasian Mycologist (2011) 29

Pileus¶¶ ¶ JTIYVHKJVU]L_[VWSHUV Habit, habitat, and distribution: solitary to gregarious convex to plane, viscid when wet, soon dry, matted on soil, in the vicinity of Allocasuarina littoralis (Salisb.) subtomentose, red to lake red (10C8, 9C–D8,7), fading L.A.S. Johnson, Eucalyptus camaldulensis Dehnh., [VULHYNYL`PZOYLK)ZVTL^OH[ISV[JO`^P[OHNL" Eucalyptus sp., Acacia sp. (known mycorrhizal ÅLZO pale yellow when young, white with age, not plants), and Hibbertia riparia (R.Br. ex DC.) Hoogland; blueing, or very rarely with a hint of pale blue, with Queensland, Tasmania, Victoria. mild odour and taste. Tubes 10–13 mm deep, adnexed to depressed around the stipe, pale yellow to yellow Material examined: Australia: Tasmania Penguite, becoming greenish yellow, (3A6 to 3E6) or dull yellowish Gunn 1775 (HOLOTYPE: K). Queensland Mareeba, green to olive, not blueing, or only slightly with injury; Davies Creek National Park, Davies Creek Road, pores concolorous, 1–2 per mm, rarely blueing, and 19 Feb 1992, Halling 6837 (*0(9 , 7,9;/" eventually staining pale brown. Stipe ¶ ¶ JT »»»:»»»,T4HYHalling SVUN ¶ ¶ JT IYVHK KY` Z[YHPNO[ VY J\Y]LK 8958)905@"»»»:»»»,T [LYL[L VY ÅH[[LULK LX\HS [V IYVHKS` Z\IJSH]H[L VY Mar 2007, Halling 8970 (BRI, NY); Kuranda, Black tapering downward, usually pinched at the base, white 4V\U[HPU 9VHK RT 5 VM 2\YHUKH »»»: to pale yellow to pale greenish yellow at apex, yellow »»»,T4HYHalling 8962 (BRI, at base, pseudo-reticulate to subpruinose-ridged to NY); Cooloola, Mutyi, 17 Sep 1982, BRIP 9148 (BRI); 17 Z\IZJHIYV\Z ^P[O ZJHIYVZP[` JVUÄULK [V [OL YPKNLZ" Sep 1982, BRIP 9150 (BRI); near Rainbow Beach, 17 these red or pink on pale yellow to yellow ground Sep 1982, BRIP 9149 (BRI); Cooloola National Park, on colour; interior solid, pale yellow to yellowish white, -PN;YLL7VPU[[YHJR(WYPS SLNC. Sandercoe & unchanging; basal mycelium white. J. Milne (JECA 86/66=BRIP 19814) det. R. Watling (BRI). Victoria: Grampians. Victoria Range, Cultivation Creek, Basidiospores ¶ í ¶ T n = 16; x = ULHY)\HUKPR*HTWPUN.YV\UK¢»:¢», í T" Q = 1.96), subfusoid to ellipsoid, Nov 1992, May 816 (MEL 2030279). rugulose with crater-like pits, inamyloid (rarely lightly dextrinoid), honey brown in KOH. Basidia ¶í¶ Commentary! ;OPZ ZWLJPLZ ^HZ ÄYZ[ KLZJYPILK I` T JSH]H[L Z[LYPNTH[L O`HSPUL Hymenophoral )LYRLSL` IHZLKVUHJVSSLJ[PVUMYVT;HZTHUPH trama bilateral, of the BoletusZ\I[`WL^P[OJLSSZ¶ The locality was published as ‘Penguite’ but this T IYVHK O`HSPUL ÅLL[PUNS` HT`SVPK PU 4LSaLY»Z is clearly a typographical error for ‘Penquite’ near PleurocystidiaYHYL\W[VTSVUNM\ZVPK]LU[YPJVZL Launceston, where the collector R.C. Gunn lived and hyaline, thin-walled. Cheilocystidia Z\IJSH]H[L ¶ worked for some time. Horak (1980) examined the T SVUN O`HSPUL [OPU^HSSLK Pileipellis a collapsed type specimen, provided some modern details on [YPJOVKLYTP\T^P[OJLSSZ¶TIYVHKJ`SPUKYPJHS microscopic features, and transferred the species to to narrowly clavate-subcapitate, smooth, thin-walled, Austroboletus. Our examination shows that the spores inamyloid, hyaline or with golden yellow content in HYLÄULS`HUKPYYLN\SHYS`Y\N\SVZL^P[OVJJHZPVUHSHUK KOH, with an amorphous, soluble, reddish brown, scattered, shallowly cratered pits; the rugulosity is plasmatic pigment. Stipitipellis hyphae hyaline, continuous over the apex (Fig. 3C–D). In optical section smooth, thin-walled, with caulocystidia¶í¶ ^P[OIYPNO[ÄLSKVW[PJZ[OLZWVYLZHWWLHY[VOH]LWLN T Z\IJSH]H[L [V JSH]H[L VY ZOVY[JSH]H[L [V VISVUN like warts and have been described as Ganoderma-like or subrectangular. Clamp connections absent (sparse, (Watling & Gregory, 1986) (Fig. 2C). Watling & Gregory ÄKL>H[SPUN .YLNVY` (1986) had examined material from the Cooloola portion

Fig. 4. Microscopic features of Heimioporus fruticicola Fig 5. Microscopic features of Heimioporus japonicus (Halling 8970). A Pileipellis elements. B Pleurocystidia. C (Halling 9288). A Pileipellis elements. B Caulocystidia. C Caulocystidia. D*OLPSVJ`Z[PKPH:JHSLIHY$T *OLPSVJ`Z[PKPH:JHSLIHY$T of the Great Sandy National Park, which extended Pileus ¶ JT IYVHK WSHUVJVU]L_ KY` ÄULS` the range beyond the type locality in Tasmania. They subvelutinous, deep red to pale red, with some hints were able to provide only some sparse details from the of olive at margin from fading; ÅLZO pale yellow, ÄLSKKH[HSVKNLK^P[O[OVZLZWLJPTLUZI\[ZWLJPÄJZ unchanging, with mild odour and taste. Tubes adnexed, outlining the macromorphology were still lacking. Until bright yellow to yellow with a hint of pale greenish, now, a habit image has not been available. The dry, unchanging; pores 1–2 per mm, yellow, unchanging. basically red colours overall, yellowish hymenophore, Stipe_JTIHYLS`Z\IJSH]H[LZ[YHPNO[KY`KHYR a typical lack of cyanescence, non-reticulate (but dull red, pale yellow near base, white at base, coarsely not unornamented) stipe, and medium stature can and shallowly lacerate-ridged with a dense red pruina IL KPZ[PUN\PZOPUN THJYVZJVWPJ MLH[\YLZ PU [OL ÄLSK overlaying the ridges, pseudoscabrous; ÅLZO pale :\WLYÄJPHSS` ZPTPSHY Boletellus obscurecoccineus has yellow above, white toward and at base, unchanging. more conspicuous scales on the stipe and is of less substantial stature. In H. fruticicola[OLÄULS`Y\N\SVZL Basidiospores¶í¶ Tn = 16; x$ spore ornamentation with cratered pits appears unique í T" Q = 1.66), ellipsoid to subamygdaliform, in the boletes (Figs 2C, 3C). In our experience, some reticulate to alveolate-reticulate, honey brown in KOH. Austroboletus spores can be rugulose and will become Basidia ¶ í ¶ T JSH]H[L Z[LYPNTH[L pitted with maturity, but these lack the rim around hyaline. Hymenophoral trama bilateral, of the Boletus- the pit. Furthermore, the spore colours are different Z\I[`WL ÅLL[PUNS` HT`SVPK PU 4LSaLY»Z O`HSPUL PU (pinkish vinaceous in Austroboletus, olivaceous in 26/^P[OJLSSZ¶ TIYVHKPleurocystidia absent. Heimioporus). References to this species in lists and Cheilocystidia ¶ í ¶ T IYVHKS` JSH]H[L [V catalogues have been compiled by May & Wood (1997). sphaeropedunculate, smooth, thin-walled. Pileipellis a (NHZ[LYVPKMVYTMYVT=PJ[VYPH4,3 PZRUV^U O`TLUPMVYTLWP[OLSP\T^P[OJLSSZ¶¶TIYVHK to have similar spore morphology, but further studies broadly clavate to napiform, sometimes isodiametric, are needed to ascertain its relationship to H. fruticicola. hyaline in KOH, subtended with subpellis elements containing an amorphous, soluble, reddish brown, Heimioporus japonicus (Hongo) E. Horak, Sydowia plasmatic pigment. Pileus trama interwoven, with 56! O`WOHL ¶ T IYVHK [OPU^HSSLK O`HSPUL PU 26/ -PNZ)(¶)(¶) inamyloid. Stipitipellis hyphae smooth and thin-walled, Heimiella japonica Hongo, J. Jap. Bot ! with caulocystidia¶í¶TJSH]H[L[VZOVY[ 1969. clavate to subcylindrical or oblong and subrectangular. Boletellus japonicus (Hongo) L.D. Gómez, Rev. Biol. Clamp connections absent. Trop:\WWS! 4`JVIHUR!4)

Habit, habitat, and distribution: solitary to gregarious; at the CUNY–Lehman College campus (Bronx, NY, USA). associated with pine and oak in Japan; with Melaleuca, The Queensland Parks and Wildlife Service assisted with Allocasuarina, Eucalyptus, and Leptospermum in accommodation and I. Thrash provided orientation on Australia; China (associate unknown). Fraser Island.

Material examined: Australia: Queensland Fraser References 0ZSHUK2PUNÄZOLY)H`»»»:»»», )LYRLSL`41 +LJHKLZVM-\UNP+LJHKL??;HZTHUPHU-\UNP m, 28 Mar 2010, Halling 9288 (BRI, NY); Cooloola, on London Journal of Botany 7¶ 2PUN»Z)VYL>HSRPUN[YHJRZHUK`ZVPS+\ULZ`Z[LT )VLKPQU2) :VTLT`JVSVNPJHSUV[LZ Sydowia 5, 211–229. THWYLM 0=*VVSVVSH "»»» Corner EJH 1972. Boletus in Malaysia. Singapore. 263 pp. *VYULY,1/ Boletus and Phylloporus in Malaysia: further notes Feb 1980, D.J. Ross & P. Seguin, JECA 80/30 (BRIP 9132, and descriptions. The Gardens’ Bulletin Singapore 27, 1–16. BRI). China: Yunnan Kunming market, 29 Jun 2001, Halling RE 1989. A synopsis of Colombian boletes. Mycotaxon 34, X.H. Wang 1212 (HKAS 3886, NY). Japan: Shiga Ôtsu ¶ City, Senjô, 31 Aug 1966, T. Hongo 3294 (HOLOTYPE: Halling RE, Mueller GM 2002. Agarics and boletes of neotropical oakwoods, pp. 1–10 in Watling R, Frankland JC, Ainsworth AM, ;5:-Õ[Z\0ZOP`HTH;LYHIL:LW Isaac S, Robinson CH (eds), Tropical Mycology, vol. 1. CABI Hongo 18587(9(;@7,!;5:- Õ[Z\:LUQ Publishing, Wallingford, UK. 11 Sep 1981, T. Hongo 6291 (TNS-F-10187). Ibaraki /HSSPUN9,4\LSSLY.4Common Mushrooms of the Talamanca Naka-gun, Naka-mach, Ibaraki Prefectural Forest Park, Mountains, Costa Rica. New York Botanical Garden, New York. WW 28 Aug 1997, A. Yamada s.n.;5:-Shimane /HSSPUN 9, 6ZT\UKZVU ;> 5L]LZ 4( 7HJPÄJ IVSL[LZ! 5HRHN\U(ZHOPJOV6J[ E. Nagasawa (TMI Implications for biogeographic relationships. Mycological Research 5@ 112¶ Heim R 1963. Diagnoses latines des espèces de champignons, ou nonda, associés à la folie du komugl taï et du ndaadl. Revue Commentary: The material from Cooloola was cited by Mycologie (Paris) 28, 277–283. Watling & Gregory (1986, p. 117) as Heimiella sp. and Horak E 1980. Supplementary remarks to Austroboletus (Corner) is the earliest collection of the species from Australia. Wolfe (Boletaceae). Sydowia 33, 71–87. Although Hongo (1969) described the stipe as reticulate, /VYHR,Heimioporus E. Horak gen. nov.—replacing Heimiella Boedijn Z`UWVZ[)VSL[HSLZ)HZPKPVT`JV[HSydowia 56, the type, as well as the other material examined, ¶ possess the coarsely and shallowly lacerate-ridged Hongo T 1963. Notes on Japanese larger fungi (20). The Journal of stipe surface that is overlain with a dense, red pruina Japanese Botany 44, 230–238. (Fig. 1C). This could be construed as a reticulum of Hongo T 1973. 21. Enumeration of the Hygrophoraceae, Boletaceae and Strobilomycetaceae. Mycological reports from New Guinea ZVY[ZI\[PZUV[HYL[PJ\S\THZL_LTWSPÄLKI`Boletus and the Solomon Islands (16–21) Bulletin of the National Science edulis Bull. or Tylopilus felleus (Bull.) P. Karst., for Museum 16¶ L_HTWSL;OLÄULS`Z\I]LS\[PUV\ZUH[\YLVM[OLWPSL\Z Lohmann H 1913. Über Coccolithophoriden. Verhandlungen der Z\YMHJL ^V\SK OPU[ H[ [OL O`TLUPMVYT JVUÄN\YH[PVU Deutschen Zoologischen Gesellschaft 23¶ May TW, Wood AE 1997. Fungi of Australia Volume 2A. Catalogue and of the cells forming that surface. With these surface Bibliography of Australian Macrofungi I. Basidiomycota Australian features and alveolate-reticulate spores, the species is )PVSVNPJHS9LZV\YJLZ:[\K`*HUILYYH WW distinctive in the Australian mycota. Mueller GM, Strack BA 1992. Evidence for a mycorrhizal host shift during migration of Laccaria trichodermophora and other agarics into Neotropical oak forests. Mycotaxon 45 ¶ The broad geographic distribution and the association Osmundson TW 2009. Systematic, biogeographical, and ecological with a range of mycorrhizal partners are not unique perspectives on the diversity and conservation of microbial for H. japonicus. Clinal distributions on continental obligate symbionts, using mycorrhizal boletes (fungi) as exemplar scales and switching of mycorrhizal partners have taxa. PhD dissertation, Columbia University, New York. 176 pp. Singer R 1986. The Agaricales in Modern Taxonomy. Koenigstein, been documented before (Halling 1989; Mueller & Germany. 981 pp. :[YHJR "/HSSPUN 4\LSSLY"/HSSPUNet Singer R, Araujo I, Ivory MH 1983. The ectotrophically mycorrhizal al. 2008). Notwithstanding Watling & Gregory’s (1986) fungi of the neotropical lowlands, especially central Amazonia. initial synopsis of the neighboring Cooloola boletes, it Beihefte zur Nova Hedwigia 77¶ Thiers, B. [continuously updated]. Index Herbariorum: A global is reasonable to expect that our intensive survey for directory of public herbaria and associated staff. New York macrofungi on Fraser Island would reveal novel or little Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/ known distribution patterns. ih/ Watling R 2000. Bresadola, Cesati and Patouillard’s old world IVSL[LZ WW ¶ in Papetti C, Consiglio G (eds), Micologia Acknowledgements Duemila. Associazione Micologica Bresadola, Trento, Italy. Watling R, Gregory NM 1986. Observations on the boletes of the The authors are grateful to the National Science Foundation Cooloola Sandmass, Queensland and notes on their distribution <:(MVYM\UKPUNZ\WWVY[PUNYHU[+,) HUK[OL in Australia. Proceedings of the Royal Society of Queensland 97, National Geographic Society Committee for Research 97–128. HUK,_WSVYH[PVU<:(PUNYHU[ -\Y[OLY;4H` Watling R, Hollands R 1990. Boletes from Sarawak. Notes from the T. Lebel, K. Hosaka, E. Nagasawa, and B. Spooner kindly Royal Botanic Garden Edinburgh 46¶ AHUN4 5V[LZVU[OL)VSL[HSLZMYVTLHZ[LYU/PTHSH`HZHUK facilitated loans from MEL, TNS, TMI, and K. We thank adjacent of China. Acta Botanica Yunnanica 7 ¶ M. Baxter for expertise and access to the SEM facility © 2011 Australasian Mycological Society Inc.