Climacodon pulcherrimus a badly known tropical species, present in Europe

Abstract

Climacodon pulcherrimus, a polymorphous species with a large distribution and habitat, is described macro- and microscopically. Its uncertain taxonomic position has led to the description of many synonymous species and placement in different genera. The type species of Hydnum pulcherrimum Berk. & M.A. Curtis is examined for the first time and it is compared with other collections from Malay Peninsula, Pakistan, USA and Spain. The study of Spanish collections enlarges the distribution to the South of Europe.

Full text

Cryptogamie, Mycologie,2007,28 (1):1-00
©2007 Adac.Tous droits réservés
Climacodon pulcherrimus a budlyknowntropicalspecies,
presentin Europe
Gabriel MORENOa*, María NatividadBLANCOa, IbaiOLARIAGAb
& Julia CHECAa
aDpto. Biología Vegetal, Fac.Biología.Univ. de Alcalá,
E-28871, Alcaláde Henares, Madrid.
e-mail:gabriel.moreno@uah.es
bDpto. Biología VegetalyEcología(Botánica). Fac.Ciencias y Tecnología.
Campus de Leioa.Univ. del PaísVasco. Apartado 644. E-48080Bilbao.
Abstract–Climacodon pulcherrimus,apolymorphous species withalarge distribution and
habitat,isdescribed macro- and microscopically.Its uncertain taxonomicposition haslead
tothe description of many synonymous speciesand placementin differentgenera.The type
speciesof Hydnum pulcherrimumBerk. & M.A.Curtisisexamined for the first time and it
iscompared with othercollectionsfrom MalayPeninsula, Pakistan, USA and Spain. The
studyof Spanishcollectionsenlarges the distribution tothe South of Europe.
Basidiomycota/Meruliaceae/Climacodon /Donkia/Hydnum/systematics / chorology/
taxonomy
INTRODUCTION
Inthe last four years,we havecollected some basidiomataof a
saprophyte fungus witha basidiomaof mediumsize,normallydimidiatewith
trametoid appearanceand hydnoid hymenophore. Microscopicallyitis
characterized by the presence of double ormultiple clamp connections,ellipsoid
basidiosporesand absence of cystidia.Finally,wecould determine it,withsome
difficulties, asamemberof the genus Climacodon P.Karst., belonging tothe
familyMeruliaceaeP.Karst.,orderPolyporalesGäum. (Kirketal.,2001). This
genus includes species withconspicuous cystidia and hyphaewithsingle clamp
connections,withthe onlyexception of C. pulcherrimus (Berk. & M.A.Curtis)
M.I.Nikol., collected by us.For thesereasonsits inclusion in Climacodon is very
conflictiveand its taxonomicinsertion is very difficult.
Climacodon pulcherrimus isapolymorphous species withawide
distribution and habitat,thereforethereare manydescriptions underdifferent
names whichweresynonymized byMaasGeesteranus (1971). Hydnum
pulcherrimumBerk& M.A.Curtis, basonym of Climacodon pulcherrimus,has
been characterized depending on the differing interpretations.According toMaas
Geesteranus (1971) ithasgloeocystidiathat sometimesare notdeveloped and
*.Correspondenceand reprints:gabriel.moreno@uah.esPhone number:34918855065, Fax:34918855066
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2G.Moreno, M.N.Blanco, I.Olariaga & J.Checa
double ormultiple clamp connections.Pilát(1936) described it with leptocystidia
without any referencetothe presence of clamp connections.Recently, Gibertoni
etal. (2004) hascommented on the presence of gloeocystidia but providesno
information about the characteristicsof clamp connections.
Onthe otherhand,Hydnum pulcherrimumhasbeen recombined into
such genera asSteccherinum ,Creolophus,Dryodon and Donkia , but hasnotbeen
included in Phanerochaete , although it shares some characters withthisgenus
(Nakasone,1990).
The abovecomments indicatethe necessity tostudy the type material of
Hydnum pulcherrimumdeposited in the herbariumK, and not studied byMaas
Geesteranus (1971),in order toclarify the taxonomicproblems.
The studyof Spanishcollectionshasenlarged the distribution tothe
South of Europe.
MATERIAL AND METHODS
The specimensexamined are keptin the following herbaria: AH,
ARAN-Fungi, BIO-Fungi, K, L, UPS and LLoydMycologicalcollection in BPI.
The materialcollected was studied witha binocularmicroscope and after
mounting in KOH 5% and ammoniacalCongo red solution. Spore measurements
were made under the oil immersion objective. The micrographshavebeen made
witha Nikon (Eclipse 80i) microscope and adigitalcamera Nikon (DS-5M).
The abbreviationsforauthorcitationsfollowKirk& Ansell (2003).
TAXONOMY
Climacodon pulcherrimus (Berk. & M.A.Curtis)M.I.Nikol.,Flora Plantarum
CryptogamarumURSS 6 , Fungi 6(Fungi,2):194 (1961) (Figs. 1-11;16-19)
≡Hydnum pulcherrimumBerk. & M.A.Curtis,Hooker’sJ.Bot.KewGard. Misc.
1:235 (1849)
≡Steccherinum pulcherrimum(Berk. & M.A.Curtis)Banker,Mem. TorreyBot.
Club12:129 (1906)
≡Creolophus pulcherrimus (Berk. & M.A.Curtis)Banker,Mycologia5(6):294
(1913)
≡Dryodon pulcherrimus (Berk. & M.A.Curtis)Pilát[as“ pulcherrimum ”], Bull.
trimest.Soc. mycol. Fr.49:315 (1934)
≡Donkiapulcherrima(Berk. & M.A.Curtis)Pilát,Bull. trimest.Soc. mycol. Fr.
52(3):328 (1936)
=Hydnum gilvumBerk.,Hooker’sJ.Bot.KewGard. Misc.3:168 (1851)
=HydnumuleanumHenn.,Hedwigia36:198 (1897)
=Hydnum kauffmanii Peck[as“ kauffmani”], Bull. Torreybot.Club34:348 (1907)
=Hydnumaustrale Lloyd,Mycol. Writ.5( Letter 69 ):11 (1919)
=Hydnum duriusculumLloyd,Mycol. Writ.7:1107 (1922)
Materialstudied: Spain:Hernani, Ugaldetxo, Gipuzkoa, fallen trunk of Quercus
rubra ,02-VII-2002,leg.J.M.Lekuona, ARAN-Fungi A0000412.Barrutia, Gernika, Bizkaia,
fallen trunk of Quercus robur,16-IX-2005,leg.R.Picón & I.Salcedo, BIO-Fungi 10896.
Goizueta-Exkax,Navarra, woody residuesof Fagus sylvatica,8-VII-2000,leg. J.M.Lekuona,
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Climacodon pulcherrimus a budlyknowntropicalspecies,presentin Europe 3
Figs. 1-11 Climacodon pulcherrimusAH 31379. 1-3: Contextual hyphae. 4-5. Hyphae of the
pileipellis.6-7: Hyphae of the subhymenium. 8: Detail of the hymenium. 9-10: Basidia. 11: Spores.
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4G.Moreno, M.N.Blanco, I.Olariaga & J.Checa
ARAN-Fungi L0002309. Abaño, Arano, Navarra, deadtrunk of Quercus rubra ,27-VI-2002,
leg.J.M.Lekuona, ARAN-Fungi A0000403.Jimenade la Frontera, Cádiz,deadbranches
of Quercus suber ,2-XI-2003,leg. M.Madrid, AH 31379 duplicate in the herbarium of
Ryvarden, Larsson & Bernicchia.Ronda, pinarArroyo del Águila, NationalPark
of Grazalema, Málaga, trunk of Quercus ilex ,4-XII-2003,leg. F.Prieto& M.A.González,
AH 31738 duplo in ARAN-Fungi. Artikutza-Elama, Navarra, 30T WN9881,450m,woody
residuesof Corylus avellana ,24-VII-2004,leg. J.M.Lekuona, J.Huarte, P.M.Pasaban, J.L.
Albisu, A.Iñiguez& I.Olariaga, ARAN-Fungi 5011101A.Jimenade la Frontera, Cádiz ,
deadbranchesof Quercus suber ,27-XI-2004,leg. F.Prieto& M.A.González, AH 31805.
U.S.A. :SouthCarolina, Santee River, coll. H.W.Ravenel 1648 (exherb.Berkeley),
K135348 Type Hydnum pulcherrimumBerk. & M.A.Curtis.Florida, Seminole lo.,
Altamontesprings.On decaying oak log. 25-X-1961,leg.PaulO.Schallot,in UPS.Brazil:
Mamamguape Municipality, Paraíba State, Reserva Biológica Guaribas, Mata Cabeça de
Boi,on dead hardwood, III-2002,leg.Tatiana B.Gibertoni 22 in herb.Ryvarden 17620.
MalayPeninsula : Singapore, BotanicalGardens, Inclusters of horizontalbranchets,1-IX-
1913,leg. E.M.Burkill, Mm. Burkill’s88,4923 Lloyd in BPI US0324672 Type Hydnum
duriusculumLloyd. Idem, Isotype L0628153.BotanicalGardens, Straits Settlements, at
base of living Hevea brasiliensis ,15-VI-1914,leg. E.M.Burkill, Mm. Burkill’s 345,4865
Lloyd in BPI US0324671. Pahang, Tembeling,7-XI-1930,leg. E.J.H.Corner, Herb.Lugd.
Batav.24162 in L0628155. Ibidem,17-XI-1930, Herb.Lugd. Batav.24184 in L0628157.
Pahang, Sungei Cheka, 12-VI-1931,leg. E.J.H.Corner, L 0628154;Singapore, Botanical
Gardens,16-II-1932,leg. E.J.H.Corner, L 0628152; Johore, Mawai,2-IX-1934,leg. E.J.H.
Corner, L 0628156.Pakistan : Swat, Sharhan,on decayed log,24-VIII-1959,leg. S.Ahmad,
Herb.Lugd. Batav. 14407 in L0628151.
Basidiocarps solitary,often imbricated,3.5-11 ×2-6cm, broadlyattached
tothe substrate,dimidiate,semicircular, applanate,uptotriangularin section,
upper surface pale brownishwith orange ororange-reddishtints,tomentose,
azonate,margin concolorous.Hymenophore hydnoid,orange-creamto pale
orange brown,sometimes withcaramelized aspectin herbarium material,teethup
to6×1 mm,joined at the base, cylindricaltosomewhatflattened,withacute ends
without branches,sometimes slightlyciliate or tuberculate. Context whiteto
brownish,soft,2-5 mm. Smell scarcelynotable. Flavour to fungi hardly relevant.
Hyphalsystem monomitic;contextual hyphae hyaline,thin tothickwalled,
4-6-(-8) µ m,septate,occasionallybranched, afibulate or with 1-2(-5) clampsin each
septum. Hyphae of the pileipellis 7-9 µ m diameter,double walled,hyaline,
sometimes with oilycontent,septate, afibulate or with 1-2-3-4 (-5) clampsin each
septum. Hyphae of the tramaof the teeth3-4 µm diameter,parallel,septate,hyaline,
sometimes withabundantoil drops,without or withvery scanty clamps.Hyphae of
the subhymenium2.5-3µ m,with prismatictexture,without clamps.Basidia(15-)20-
30 ×4-4.5 µ m,subclavatetocylindrical,hyaline,thin walled,tetrasporic, without
clampsat the base. Cystidialacking,withsome hyphal ends with obtuseapex,
projecting from the hymeniumwhicharevisible withstereoscopicmicroscopy,
giving avelutinous appearance. Basidiospores4-5(-6)×1.5-2(-2.8) µ m,ellipsoid to
allantoid,hyaline,smooth,thin walled,non-amyloid,non-dextrinoid. Oil dropsare
very common in the hymenophore,mainlyin the trama.
STUDY OF THE TYPE MATERIAL
The type material of Hydnum pulcherrimumBerk. & M.A.Curtisis
conserved inside of a brown envelope,thatiskeptin a brownish pack labelled as
K(M) 135348 (Fig. 12-13). Thismaterialconsists of remainsof a basidioma
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Climacodon pulcherrimus a budlyknowntropicalspecies,presentin Europe 5
fragmented in three portions(Fig. 14). The smallest portion isaffixed toa
pasteboardand itispossible to observethe hydnoid hymenophore in it(Fig. 15).
The second portion iscrushed,of approx.2.5 ×1.5 cmand the largest isapprox
5×3cmand isalsocrushed.
Description.–Basidiomastrawishcreamcoloured,fibrous; hymenophore
hydnoid,teeth orangishbrown, approx.2mm long. Hyphalsystem monomitic.
Hyphae of the pileipellishyaline,septate,double walled,7-10µ m diam.,1-2-3-4
clamp connectionsin eachseptum or rarelyafibulate (Figs. 16-17). Hymenophore
Figs. 12-17Hydnum pulcherrimumType. 12.Label of the herbariumK. 13.Detail of writing.
14. Basidioma. 15. Detail of the trama and the hydnoid hymenophore. 16-17.Multiclamped
hyphae of the pileipellis.
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6G.Moreno, M.N.Blanco, I.Olariaga & J.Checa
composed by very collapsed hyphae,difficult tosee in ammoniac Congo red
solution and KOH 5%. Hyphae of the tramaof the teethcylindricaland narrow,
2.5-4 µ m diam. Sporeshyaline,small and very collapsed,making itdifficult to
observetheirmorphologyand size.
The type material of Hydnum duriusculumfrom Singapore isconserved
in BPI US0324672 (type),in the same packet there isanothercollection with
numberBPI US0324671. Bothcollectionsare in a badcondition,duetothe
treatment with mercury chloride and ithasbeen impossible to do the macroand
microscopicstudy.Thisproblem hasalreadybeen indicated byMaasGeesteranus
in arevision label dated to 1969. Onlyin BPI US0324672,labelled as type,we
havebeen able tosee the hydnoid aspectof the hymenophore.
Figs. 18-21Climacodon pulcherrimus. 18-19 Detail of basidiomafrom Andalusia(Spain), AH
31739. 20.Detail contexto,trama and hidnoid hymenophore, AH 31805. 21. Detail acute ends,
AH 31805.
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Climacodon pulcherrimus a budlyknowntropicalspecies,presentin Europe 7
DISCUSSION
This speciesischaracterized by the dimidiatebasidiocarp,irpicoid,with
orange tint,hyphae of the pileipelllisand the tramawith2-3-4 clamps,manyoil
dropsin the tramaof the hymenophore,lacking cystidia, although sometimesitis
possible to observesome hyphal endsin the hymeniumand small and hyaline
spores(4-5 ×1.5-2µ m),ellipsoid toallantoid.
Inthe point9 of the keyof the monograph of MaasGeesteranus (1971)
on the hydnaceous fungi,the presence of cystidiapoints toClimacodon, but in the
description of Climacodon pulcherrimum(p. 140)the following description is
given:“Gloeocystidia2.7-4.5 µ mwide,projecting but little beyond the basidia,
thin-walled tothick-walled,notencrusted,sometimesnotdeveloped”. In our
observations,we haveseen no cystidia, neitherin type material of Hydnum
pulcherrimumand duetothisfact,itis very difficult to determine Climacodon
pulcherrimumusing thispaper.
The genus Climacodon wascreated byKarsten (1881) based in the type
speciesHydnumseptentrionale Fr.,which has thick-walled cystidia, often with
encrusted tipsand hyphae,never with morethan one clamp connectionsper
septum (MaasGeesteranus,1971).
Pilát(1933)recombined Hydnum pulcherrimumtoDryodon pul-
cherrimumand described the materialcollected from Siberiaon Fagus sylvatica,
Betulaverrucosa ,Abies sibirica and Populus tremula ,withthin-walled and
cylindricalcystidia(38-35×3-3.5 µ m) projecting 15 µmabovethe hymenium. We
have notobserved thesecystidiain the Iberian materialand nothing in the type
of Hydnum pulcherrimum .Thisauthordoesnotcommenton the presence or
absence of clamp connections.
LaterPilát(1936)created the genus Donkiafor this species withthe
following latin diagnosis“ Genus exaffinitate generisDryodon aquo deficientia
gloeocystidarum in hymenio membranaquesporarum haudamyloideadiscrepat.
Intergenera Mycoleptodon etDryodon genus intermedium. Carposomata
effusoreflexavel laterilateradnata, lignicola, in latere inferioriaculeosferentia.
Hymeniumsolum e basidiiscompositumvel solumcystidiola basidiformia, plus
minus vacua adsunt.Sporae hyalinae,ovataevel ellipsoideae,membranalaevivi
solutionisjodi haudcoerulescenti instructae ”. Asitispossible tosee, Pilát
described the presence of cystidia basidiformia, absence of gloeocystidia and he
did notindicatethe presence of clamp connections.Weagree withPilátin the
absence of gloeocystidiain the materialrevised by us,however we have not
observed cystidia basidiformiadrawnand described byhim.
Nakasone (1990)treats this speciesasDonkiapulcherrimaand hasmade
cultures with materialcollected on diversespeciesof Quercus ( Q.virginiana ,Q.
nigra ,Q. phellos ,Q.sp.)and Abiessp. from different statesof U.S.A.Inthis
paper,the morphologicalcharacters are described and he stressed the whiterot
character, aspreviouslycommented byGilbertson etal. (1975). Nakasone
indicates thatculturallyD. pulcherrimaresembles some PhanerochaeteP.Karst.
speciesand he mentions the presence of double ormultiple clamp connectionsin
the myceliaof the cultures, asalso occurs in P.burtii (Romell exBurt)Parmasto,
P.crassa(Lév.) Burds. , P. ericina(Bourdot)J.Erikss.& Ryvarden (now
Peniophoraericina ) , P. exilis(Burt)Burds. , P. flavidoalba (Cooke) S.S.Rattan , P.
gigantea(Fr.) S.S.Rattan (nowPhlebiopsisgigantea ) , P. laevis(Fr.) J.Erikss.&
Ryvarden, P.rimosa(Cooke) Burds. (nowScopuloides rimosa ). Burdsall (1985)
05_MORENO.fm Page 7Mercredi,28. février 2007 11:14 11

8G.Moreno, M.N.Blanco, I.Olariaga & J.Checa
cites13 speciesof Phanerochaetewhosesubicularhyphae have double ormultiple
clamp connections.
Wesentaportion of the Iberian materialbefore placing itin Climacodon
pulcherrimus,toDr.Larsson to do molecularbiology studies.Heanswered us
(com. pers.):“the most similar sequencesfrom our dataset representmonomitic,
non-clamped specieslike Phanerochaetespp. and Phlebiadeflectens .Itpoints in a
certain direction but doesnotgive enough guidance foradecision about generic
placement”.
Weconclude that the insertion of Climacodon pulcherrimus in thisgenus
isinappropriate,duetothe presence (onlyin this speciesof Climacodon) of
hyphaewith double ormultiple clamp connectionsand the absence of cystidiain
the studied material. Also,this species shareculturaland molecularcharacteristics
withthe genus Phanerochaete ,so perhapsitmust be placed again in the genus
Donkiaorincluded in the genus Phanerochaete.
Otherclosely related genera areOdonticiumand Spongipellis .
Odonticiumdiffers because of its resupinatebasidiocarpsand the total
absence of fibulae, but shares the type of hymenophorewithteeththatare fused
at the base, absence of cystidia and basidiosporesof small dimensions.
Spongipellishasdimidiate fructifications with pores.An exception is
S. pachyodon (Pers.) Kotl. & Pouz.,thathasahydnoid hymenophore. However,
itdiffers because one of the characters of the genus is the presence of fibulae in
all the septae.
Climacodon pulcherrimus hasatropical distribution,itisknown from
Asia: Japan, Java, Pakistan, Peninsula Malaysia, Philippines, Sikkim and Thailand
(Pilát,1936; MaasGeesteranus,1971). InEurope itisknown onlyfrom France
(Candousseau,1981) and Russia(Pilát,1933,1936). InAmerica ithasbeen cited
byBononi (1979) and Gibertoni etal . (2004) from Brazil, but theyindicatethe
presence of gloeocystidia, dimitichyphalstructureand mention nothing about
hyphae having multiple clamp connectionsin the pileipellis.We haverevised this
materialand find it tobe monomitic, and find thatithasfibulae onlyin the
generative hyphaewith2-3-4 clampsin the context.
Nakasone (1990)and Gilbertson etal. (1975) cited this speciesfrom
U.S.A.
Acknowledgements.Thisinvestigation hasbeen partlyfinanced by the Research
Projectof the “Ministerio de CienciayTecnología, PlanNacional de Investigación
Científica, Desarrollo e Innovación Tecnológica REN2002-01965”. We express our
gratitude toDr.L.Ryvarden, Dr.K.H.Larssen yA.Bernicchia, for their your suggestions
and revision of the paper.
We express our gratitude toD.W.Mitchell and H.Singerfor the revision of the
manuscript.Wewant tothank F.Prieto, M.A.González, J.M.Lekuona and P.M.Pasabán
for the collection of part of the studied material. Weare especiallygratefultothe curators
of the herbariumAH, BPI, K, L, forhercollaboration and the shipmentof specimens.
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