5.2.

j ¡~

,Fol. Bot. Mise., 9: 5·17 Barcelona 1993

ANATOMICAL ASPECTS OF SOME HYPOGEOUS FUNGI

FROM CATALONIA (NE SPAIN)

M.P. MARTtN1, D. SIERRA 1 & M. TABARÉS2

ABSTRACT During our researeh on the mycoflora of Catalonia, two species of

hypogeous fungi were found as first records in the area surveyed: Leuco­gaster lozzianus (Cav. & Saec.) Matt. and Octavianina aSlerosperma (Vitt.) O. Kunlze. We have done a macro- and microscopical study of some analomical features, giving special attention to lhe peridium and reproductive structures of the species mentioned aboye. Moreover, a similar study has been done on some other hypogeous fungi which are very infrequenl or rare in Catalonia: Hymenogaster hessei Soehner, Hys­terangium rickenii Soehner, Hysterangium stoloniferum Tul. var. rubes­cens (Qué\.) Zeller & Dodge and Wakefieldia maerospora (Hawker) Hawker.

Key words: Gasteromycetes, hypogeous, Catalonia.

Introduction

Six hypogeous Basidiomycotina have beeo studied, including the type material of Leucogaster tozzianus (Cav. & Sacc.) Matt.

All the species have been adequately described by different authors, but in this occasion, we want to compare our own observations with theirs, mainly referred to the development of basidia, the development of spor~s

and the morphology of the peridium. The species studied are: Hymenogas~

ter hessei Soehner, Hysterangium rickenii Soehner, Hysterangium stolo­niferum Tul. var. rubescens (Qué\.) Zeller & Dodge, Leucogaster tozzianus (Cav. & Sacc.) Matt., Octavianina asterosperma (Vitt.) O. Kuntze and Wakefieldia macrospora (Hawker) Hawker.

These species are c1assified according to JÜlICH (1989), and have been arranged taxonomically here.

The material examined has been deposited in the University of Barce~

lona Herbarium (BeC).

1. Departament de Biología Vegetal (BotAnica). Universitat de Barcelona. Av. Diagonal. 645. 08028 Barcelona.

2. eoll de Ponell. 44 baixos. 08024 Barcelona.

6

Hymenogastrales Cllnn. 1944 Hymenogastraceae Vitt. 1831

Hyrnenogaster hessei Soehner 1943

Specimens cxamined: Under Faglls syll'atica, Montscny (Barcelona), leg. M. P. Martín & D. Sierra, Oetober 1990, BCC-MPM 1352.- Collsero!a, leg. M. Tabarés, March 1992, BCC-MPM 1547.

Prcvious records: VlDAL (1991) reported t!lis spccies from Girana.

Remarks: Our material fits SOEHNFR'S (1962) deseription. In agreemcnt with this autor, the ripe spores are dark browll, oval (19-22 x 11-15 ¡.¡m), with a more or less distinct apiculum, with eoarsely wrinkled or almost retieulate perisporillm and witll a c\aw-like basal strueture (Fig. le, fig. 8 a-b). Basidia are c\ub-shapcd (30-35 x S-S ¡.¡m), amI bisporie (Fig. 1 a-b).

The peridium has duee different laycrs not always easily separable (Fig. 7a). The outer layer (10-20 ¡.¡m thiek) is formcd hy brown hyphae, the middle (110-130 ¡.¡m) is pseudoparenehymatous and the inncr (20-30 ~Im) is eomposed of hyaline hyphae.

Q() ~@

~0@t Figure lo lIymetlegaster IlI'ssl'i Sochncr. I3CC-MPM 1547: (l. immaturc hasidium: b. Fil mature basidium: e, immalure and mature spores showing the ornamentation. hy

7

Octavianinaceae Locquin ex Pegler et Young 1979

Octavianina asterosperma (Vitt.) O. Kuntze 1898

Specimen examined: Under Fagus sylvatica in Montseny (Barcelona), lego A. Rocabruna, 27 October 1987, BCC-MPM 794.

Previous records: MORENO & al. (1991) previously recorded this species from Cáceres. CALONGE & PASABAN (1992) reported this species from Na­varra.

•A•/

e

(J,':.' ..... {~ l .

a

b

Figure 2. Octavianina asterosperma (Vitt.) O. Kuntzc, BCC-MPM 794: a. part of the hyrncniurn; b, stages in developrnent of basídia; e, stages in developrncnt of the spores.

Rell1arks: With respcct to basídia, \ve have always seen bísporic ones (Fig. 2b), although according to CORDA (IS54), 110UDIER (1905-1910) and LANGE (1956), they can a1s() be tetrasporíe.

Thc young spores are ovate anJ sll100th (LANGE, 1(56), but when ripened are globose and ornamented. In the various works we have con­sulted, the authors' descriptions of spore ornamentation do not agree. In our opinion, this is a reslllt of the diversity of ornamentation that appears dllrillg sporc development (rig. 2e). At first, the spores have short. single warts (CORDA, 1854; BOUDIER, 1905-1910: SVRCEK, 1958a). Later, they are strongly eehinate-spinose (VELENOVSK Y, 1920; LANGE. 1(56). and have prominent. pyramidal and acute warts (fig. Sc), formed as a consequence 01' the convergenee of groups of single spines (I'vlONTECCHI & LAnARI, 1988: MORENO & al., 1991; CALONGE & PASAIlAN, 1992). Fínally, this fragile ornamentation can easily hreak, creating obtuse warts, and even cavities (Fig. Sd) on the spore (HAWKER, 1l.J53). Basidia are bisporie (Fig. 8e).

The peridillll1, which is lOO-l60 ~lm thick, is 1'ormed by brown hyphae rllnning parallel to the sllrfacc (HAWKER, 1953; LANGE, 1(56). We disagree with MONTECCfH & LAZZARI (1988), who described the peridillm as forll1ed by hyphae and sphaeroeysts, insteaJ we fOllnd that, between the peridillm and the pselldoparenchymatous sllbhymenial layer, there are hyaline hy­phae mixed with short hyphal segrnents (fig. 6b). which resell1ble sphaero­cysts (PEGLER & YOUNG, 1(79).

Wakefie!dia macrospora (Hawker) Hawker 1954 Fi Syn.: Hymenoga.l'ter vacekii Svreek 1958 11:

Specimens examined: Under Querclls sp., Collserola (Barcelona), lego M. Taharés, 1 March 1992, BCC-MPM 1497 and 15 Mareh 1992, BCC-MPM al

1556. p

Previous retords: In Spain, this spceies has only been reported once (VIDA!.. h

1991), as F-Iymcnogaster vacekii Svrcek. h

Remarks: Qur material fits well with HA WKER'S (1951. 1(53) descriptioll. H Thc YOllng spores are colollrless, subglobose, smooth (PEGLER & YOUNG. 1979) or with short warts (SVRCEK, 1958a, as Hymenogaster vacekii Svrcek). S The ripe spores are globose (10.5-15 ~1I11), brown, with thick (1-2 ~lm high). le truncate warts (Fig. Jc, fig. H f-h). Basidia are c1uh-shaped (30-40 x 10-\3 ~111), bisporie (Fig. Jb). P

The peridillm is not easily separable from the gleba and is formed by (1 hyaline, septate hyphae whieh do nol present clamp connections (Fig. 6(1). it AccorJing to DE V¡UES (19RH), the peridium hyphae present clamp eonnec­tions. Thercfore, this taxon would be incillded in the lfydllangiaceac. At B this moment, until more material is availab1e to eonfirm the presence or P

9

501: '¡

\ .. I . I

\ I

U Figure 3. Wakefieldia macrospora (Ilawker) Hawker, BCC-MPM 1556: a. parl of lhe hymenium; b, spores; e, slages in devclopment of lhe basidia.

abscncc of clamp conncctions, we follow PEGLER & YOUNG (1979), who place Wakefieldia macrospora in Octavianinaceae.

Hysterangiales Zelkr 1943 Hysterangiaceae E. Fischer lBY9

Hystcrangium rickenii Soehncr InI

Spccimen examined: Undcr Quercus ilex, Sant Gervasi. Col1serola (Barce­lona), lego M. Tabarés. 27 March 1992, BCC-MPM 1499.

Previous reeords: This taxon has been I'ound in Alfaguara, Granada (MORENO & al., 19B6) and in the provinee 01' Girona (VIDAL, 1991), where it is quite frequcnt.

Remarks: Spores are ycllowish, ellipsoid-fusoid (16-18 x 6-7 pm), shortly pediccllatc, with rounded or sometimes pointcd apiees; the young spore has

10

r.) a 1)'~(Y)l., \ \'1/ Ji

d fl /

,~\~ // I . '::$. '" ID ~m

\¡ f )(

\\ I )

e

000000 o Fi2urc 4. lIySll'rangium rickenii Soehncr, ACC-MPM 14l)l) (a-c): ¡J, immalure sporcs: n, malure spores; c, basidium,- Hysteratlgiwn sl%niferum Tul. val'. rubescl'llS (Qué!.) Zcllcr & Dodgc, BCC-MPM 1500 (d-c); d, basidia; e, slagcs in development of the spores,

a smooth perisporium (Fig. 4a, fig. 9a), but then it beeomes rugase, giving to the spore a thick and dense vcrrucose ornamentatíon (Fig. 4b, fig. 9b). According to MALEN<;:ON (1975), who studied the type material and other samples 01' Soehner, the spores are minutely asperulate. Basidia are bisporic (Fig. 4c).

We have observed a brown-coloured proscnchymatous peridium (100­200 flm thick), which is formed by interwovell hyphae.

II

Hysterangium stoloniferum Tul. val'. rubcscens (Quél.) Zellcr & Dodge 1929

Specimens examined: Undcr QlIcrC/lS ilex in CoJlseroJa (Barcelona), leg. M. Tabarés, 27 March 1992. BCC-MPM 1500.- Undcr Querms cerrioide.l' in Sant Just Desvcrn (Barcelona). kg. L Llistosella. 13 May 1992, BCC­MPM 1501.

Previous recorcls: This spccies has bcen cited from Cúceres and Córdoba (MORENO & al.. 19lJl) and fmm Girana (YIDAL, 1(91).

Remarks: 111 agrcement with MORENO & al. (tlJ9 J). spores are ycJlowish. ellipsoid-fusoid (19-22 X 6-8 prn). shortly pedicellatc at lhc basc (2-3 11111). without apiculum and with a rugose perisporiurn (Fig. 4e, fig. 9 c-d). Neither these authors llor SVRCFK (llJ58a) descrioed the basiclium. which is club-shapcd (30-50 X 5-6 pm). bisporic or tetrasporic, wilh a short sterig­mata 5 Ilm high (Fig. 4d).

The peridium is mainly psellcloparenchymatous (2()l)-300 pm thick). with hyaline cells. In contrasto the external cclls are collapscd and brownish. There is a1so a thin layer (20-30 11m) of hyaline hyphae oetwcen lhe pseudo­parcnchyma and the gleba.

Leucogasrrales Fogel 1979 Leucogasrraceae Moreau ex Fogel 1979

Leucogaster tozzianus (Cav. & Sacc.) Matt. apud Zellcr & Dodge 1924 Syn.: Leucogaster fragans Matt. 1990

Spccimens examincd: In a forest of Fagus sy/vatica and Beru/a pendu/ll, La Satut (Barcelona), lego M. Tabarés. 9 October 1990, BCC-MPM 1339.­Under Pinus pinea, Punta de la Mora (Tarragona). leg. M. P. Martín & D. Sierra, 16 Dccember 19<)0, BCC-MPM 1502. Other materials: S.M. Zcller 2577 (Typc), Yallombrosa (ltaly). coll. el del. O. Mattirolo, sent by O. Mattirolo, Nov. 23. 1489. NY herbarium.- S. M. Zeller 2577 (cotype), Yallombrosa (Italy). coll. et del. O. Mattirolo, senI by O. Mattirolo, Nov. 23,1989, NY hcrbarium.- D. Saccardo 1424. Myco­theca italica (Leucogaster fragalls Matt.). Yallombrosa. Fil'enze (Italy). in abietinis, A. Fiori. Jun. 1904. NY heroarium.

Previous records: According to the available data. this species docs nol seem frcquent in Europe. It has becn found in (taly, living under Picea 01'

Pinus and in Czechoslovakia living under cleciduous trces (SVRCEK, 1958b: JÜLlCH, 1(84). ('ALQNCE & al. (1992) previollsly recorcled t!lis species from Logroño (Spain).

12

Description: 13asidiocarps suhspherical, ahout 1.5-3 cm diam. Peridium with several protubcrances (height 1.5-2 111m), ochraceous, thick (130-160 ~!m),

duplex (Fig. 7b). Outer layer (20-3Ü ~lm) constituted of ochraceous 01'

brown collapsed hyphae and the ¡nner layer (110-130 flm) pseudoparenchy­matous and hyaline. Gleba composed 01' subglobose 01' polygonaJ chambers which are surrounded by the tramal plates and filled with a gelatinous tluid, producing copious cxudation of latex when cut. Trama plates are pseudo­parenchymatous and hyalinc (Fig. 5a). Hymenium collapsed. We have not seen basidia. Spores spherical (10-13 ~un) 01' subspherical (8-U x 9.5-13 ~lm), heavily reticulate and covered with a thick perisporium (to 3 flm) as in figure 5 b-e and figure 9 c-f.

~"~ ~~I

~jO

10 llm

ed

© Figure 5. Leucoguster toZÚUlIU,\' (Cav, el Sacc.) Mal!. apu¡j. Zcllcf & Dodgc: a. par! of lhc gleba I3CC-MPM 133<J; b, sporcs BCC-MPM 133\); e, spores BCC-MPM 1502; ¡jo lype spores; e. cotype spores.

13

a

-e 3

'"

b

Figure 6. Wakejieldia macro.l'pora (Hawker) Hawker, BCC-MPM 1556: a, peridillITl.­Oclavianina a.l'lero.l'perma (Vitt.) O. Kunllc. BCC-MPM 71.)4: h, pcricJiuITl.

'" a

-e 3

Figure 7. 1fymelloga.l'11'I' hl'SSl'i Sochncr, nCC-MPM 1';47: a, pericJiuITl.- LCllcoga.l'lcr lozziallll.\· (Cav. el Sacc.) Malt. aplld. Zcllcr & Dodgc, BCC-MPM 1339: b. pcridiuITl.

14

Whcn first pickcd, the matcriét! die! not have a particular odour. bUI

after a fcw minuks it bl:camc rlL:clsant ane! swect, like a banana, ano graJu­ally changcú lO a strong smell, Iike that 01' an organic snlvent.

Figure !l. "Y"II'//o/iI/.I'('·I'!It'I'SL'i Sochncr. 13CC-ivIPM ¡S,n: a. illllllalllrl' "'pore ... (bar= 5 ~un): h, malurc sporcs (bar= 10 ¡un).- r. «(I/I'il///illlI l/.I'(t'f(I,\j!1'1'II1II (Vil!.) O. KUIHZC. B . '·MI'M 7q: . rores (bar- S ~11ll): J. 'f,ore ... (har= 5 Ilm): e. basidiulll bar= 5 ¡lIn),· Wake[iddia 1I/(WI'IJS!lOm (I-Iawk '1') Hawkn. n: ',MPI\,{ 155,: r. Immalllr' ~porL'''' ((bar 5 pm): ',malur pore, (har - 5 ~llll).· ¡¡'l/A:I'j/'c1t1il/ IIIII"'-O.\P0l'1/ (Ilawkcr) Ha\\'­k "1': h. l 'pe spor S (bar= ,) ¡1m).

l.'i

f'igurr 1), /I.I's(t:r¡¡Il~illlll rick<'llií S'lt.:hnt.:r Bl'C-i\II'M l-l')l): a. ilTlmóllll'lt.: 'pllrc'; (b(lr= • /1m): b. mOlture sporcs (har prn).- 1l1'.\lc'r//llgl//111 \'IO/Ollif(,1'I1/11 Tul. varo ruhescul/I

(Oué!.) Zcllcr & Dllll'e. B ·MI'M 15Ul: . spnrt.:s (b, l' /1m): d. srnrt.:~ (har= .5 pm),· L<'I/('ngus(('I' ((I~"i<7l1l1.\· (Cav. '1 Sacc.) M'lll. apud. Zt.:lkr &. Don 'c. 13 - 1PI\1 1.\39: ',spor 's (h,I[= 5 11m): r. sp ~ (har= 5 ~un),

16

When first picked, the material did no[ llave ;\ rarticlIJar mlollr, hut after a fcw minutes it became pleasant and s\Vect, likL' a hanana. and gradll­ally changed to a strong smell, like that 01' an org,lIlic solvenl.

Acknowledgcments

This paper was presented at the Xl 1h Congrcss 01' Europcan Mycolo­gists at Kew, England, fmm 6-11 September, by M. P. Martín and D. Sierra. who wish lo express tlleir c1eep gratitule lo the Organizing Comrnittee for providing financial assistance.

The authors are gratdul to the following pcrsons and institutions: to Mr. 1\. Rocahruna rOl' giving part of the matcrial, to the Director and Curator 01' New York Herbariul11 (NY) for the loan of type and other specimens, to Dr. F. D. Calonge for sending us sorne elcctron photo1l1icro­graphs (Fig. 8h, fig. 9f), to Mr. J. Llistosella for assistance with the SEM, to the Servci de Microscúpill Electrónica of the University 01' Barcelona, to Dr. M. Glenn (New Jersey, USA) 1'01' hcr kind English correction.

Refcrcnces

BOUDIEIl., 1::. 1')05·191O - lcul/es Atl'('ologi({le Tom. l. PI. 1·19.'. Par!';. CALONGE. r. D. & PASABAN, P. M. 1,!l)2 .- Nuevos datos sohre los hongos hipogeos Ue

España. IV. GYIII/lomyces XIlI//J¡O.l'flOI'll.1 (flawkn) A. H. Smith. no\euau para el catálogo español. Bol. Soc ,'I/lico/. Madrid. 16: 1'!-·ti.

CALONGF., F. D., CABALLERO, A. & PALACIOS. J. IlJ91 .- Contribuciún .i1l'llnocirniento dc los hongos dc La Rioja (Logruño. Espaii;i). (/11.1'/1'1'011I.\'('<'11'.1. Bol. Soc. M icol.

Madrid. 16: 115-140. CORDA, A.J. IR~4 - lcolles jil/lgorll/ll. Tom. VI. 1)1 pág. XX 1;'lm. Praga. DE VRIES, G. A. IlJRR - Wakf'fieldill lIIaCI'U.lporu (Hawker) Hawker. Gasteromyel'te

hypogé nouveau pour la myeoflore hclge. Lc:jCIIllill (llouvcJle séric). 125: 1·5. HAWKFI(, L. E. IlJ51 - Hypogcous fungi. 1. A hypogcous gasterolllycctC. Se/erogll.I·/e/,

macro.l'[Io/"ll.l'. n. sp. T/'!IIl.l'. Bril. myco/. .'loc.. :H: 2Ió-21 '). HAWREIl., L. E. 1953 - British hypogcous fllngi. Phi/. Tmll.l'. 1\0)'. tOlldoll. 237: -+2')­

546. JÜLlCH. W. 19S1J - Guida ¡¡JI,¡ uClermillazionc lIei fungbi. Vol. 2. IIl'h.\'l/o/ilwm/n.

1!1'/1'robll.l'idiolll}'c1'/1'.l'. (;11.1'/1'1"0/11.1'1'1'(1'.1'. ElI. Saturnia. TrL'lltll. 597 pp. LANGE. M. !lJ5ó - Danish I-Iypogcolls M¡¡cromyee(cs. Dal/Sk. Ho/. IIrk .. 16( 1): I-S-+. MALEN<;ON. G. IlJ75 - Champignolls hypogés du Noru uc l' Afrique 11. I::lasidiomyeéles.

!?1'vue de /'v/vcolo¡.:ic, .'1')(4): 27lJ-306. MONTECCHI, A. & LAZZAR!. G. 19f1S - Invito '1110 studio uci funghi ipogei IV. I

Gasteromieeti (11 Pime). Bol/. A~.I'. Micol. LJr1's/I(lola. XXI (1·2): 77-l)2. MORENO. G., GALAN, R. & ORTEGA. 1\. IlJX6 - HYPllgCllS lungi from continental

Spaill. CrYl){ogamie M)'wl., 7(3): 201-22lJ. MORENO, G .. GALAN, R. & MONTECCHI, A. I"')I - Hvpogeus lungi frol1l PeninsuJ¡tr

Spain 11. MYUJ/axo/l. 42: 201-23S. PEGLER. D. N. & '(OUNG, T. W. K. JlJ7lJ .- The gaslel'l\iu Russul¡¡les. rUIII.I'. nI'.

mvcol. Su,.. 72(3): 353-JXS. Sm:IINI·.R. E. 1%2 -- Die CiallUn!! 1l1'1I1(·lIo~a.l'/('1 Vil!. Ueih. SOI'O !-ied,,· .. 2: 1-113 (S

tah. ).

SVH

I SVR

I

VE!. VID,

E m

17

, .

SVR(T,K, M. 1')5;-;" - f{n/I'rIlI/l;/11lcs. 111 ,\. 1'i1;il (c'd.) FI'lI;1 C. S, R.. (i"'l"lllIllH·C'll".

Pr"h", CS. A. V: ')('-12l1. ' SVRCEK, M. 19~5Il - M<'iWIOK<lSI/<I{C.I. 111 A. i'il,íl (nI.) !'Im" C. S. ){ .. ('aSlc'r"IllI'l'l'ks.

Praha. CS, 1\. VIII: 'i27-'i5S.

VI'.I.FNOVSKY.1. II)2l1 ... Ccsk(' IHlllhy. 9511 1'. Praga, VID,\L, .1, M, 19l)1 - C"'llrihllcilÍll al ClllHlCilllicl11t) de- la 1'101''' IlllcollÍgll'a del l3ai\

Flllpol'llil v ZlJllas limítrofes (CaWllll1ya), IV. Hl1l1gos hipogClh (Zigollnc(lril/o ..·\sco­IUI'Co/iI/II y lIosidioll1yco/il/o) , Jiu/II. SOL Cololol/U ,I!lcor, 1-1·15: 1-13·1'1-1,