Revisión por invitación Polen 11 :5-20(2001)

PRINCIPAL POLLEN FEATURES IN THE LILIES ()

Hesse, M.

lnstitute of Botany and Botanical Garden, Department of Electron Microscopy and Palynology, University of Vienna, A·1030 Wien, Rennweg 14, Austria.

(Muuuscritu recibido d 15 de Muyo de 2000, IICl'[\llhl d de Jc: 2000)

SUMMARY: Araceae genera were screened ror polleo mor¡>hological charactcrs using TEM, SEM and LM. Polleo or Araceac is more diverse than previously reponed. The manifoldness does no1 onl y eonecrn the actual apenure configuration and !he type or ornamcnla!ion, bu! espccia ll y - and ra thc r unexpectcdly - the (>OIIen wall Slralificalion. In mosl Araceae subfa111ilies the ou1er1110SI po lleo wall layc r (!he cktcxinc) is stable 10 acetolysis trca1111en1. In contras!, in !he 111os1 spccializcd subfamily. !he Aroideac wilh more !han 1wo thirds or all Araceae genera. polleo grai ns show ofl cn an ou termos l !ayer. which is no! resistan! 10 acetolysis, and !he 1110Slly smoolh pollcn grains have an uncom111only spongy cndcxinc, which is widcly stable 10 acctolysis lrcatmenl. Pollen grains with a sporopolleninous ektexine should ha ve a good chancc 10 bccome foss il. This is valid for 1110s1 subfa111ilics, however, in Aroidcae therc is a much smallcr chancc bccausc of !he lack of a Slablc eklexine layer, and !he prcsence of a thick, inhomogcncous endcxi ne. Mos1 genera of !he Araceae subfa111 ilies Gymnostachydoideac. Orontioidcae, Pothoidcac, Monsleroi dcae. Lasioidcae. Calloidcac and in Zamiocu/en,¡/Goll alopus (Aroidcac) havc apenurale pollcn grai ns (main ly monosulcalc, somc disulcalc), only rcw are lackin g an apcnure (i.e., the polyplicalc polleo grai ns). lntercslingly, !he rare zonosulcale cond ition is found independen!ly in lwo subfami lics: Monsleroidcae and Zamioruleas!Gonaluptt.l' (Aroideac). No member or !he subfamily has aperturale pollen grni ns. Morcover. !he cnlirc pollen surface is apertura! in nalure; such pollen should be callcd omniapcrlurale rather !han inaperturale. Strikingly, al leas! JO genera show a polyplicale condition and. thcrcforc, sharc parallels with ephedroid (Epltedra) polleo. Suprisingly only 1wo polypli cale genera ha ve an acelolysis-slable ouler layer, while !he polyplic:ue condilion of !he Olher 8 genera is gone after acetolysis. Thc meagre ross il record of Araceae, and !he potenlial confusion or any polyplica1e Araccac wi th ephedroid pollcn (reccm or fossi l) is evaluatcd in !he lighl or lhese exlraordinary pollcn fealures. KEY WORDS: Araceae, polleo. exine, eklcxine, endexine. acetolysis.

RESUMEN: Se han analizado los caracteres de la morfología pol ín ica en los géneros de Araceae usando MET. MEO y MO. Se ha encontrado m~s diversidad que la pre viamente desc rita para el polen de Araccae. Los caracteres más llama tivos no solo awñen a la configuración de la apertura y al tipo de ornamentación. sino especialmente a la estrat ifi­ cación de la pared polínica. algo bastan te inesperado. En la mayoría de las subfa mi lias de Araccae el estrato más externo de la pared polínica (la ec1exina) es rcsislcnlc :11 lralamien­ IO acetolfti co. Por el contrario, en la subfamilia m:ls especia li zada, las Aroidcae con más de dos tercios de lodos los géneros de Araccac. los granos de polen muestran frecuen lemcnlc un estrato externo que no resiste la acelolisis. Por lo que estos granos de polen. normal­ mente lisos. muestran al exterior una endexina esponjosa poco eomun que si es estable bajo la acctolisis. Los granos de polen con una ec1exi na de esporopolenina deberían tener buenas oportunidades de fosi lizar. Esto es vá lido para la mayoría de las subfamil ias, sin

5 flesse. M.

~mba r go . en Aroidcae hay muchas menos oportunidades por l;t carencia de una ectcxina resistente y !:1 presencia de un a gruesa y no homogcnca cndcxina. La mayorfa de los géneros de las subfamilias Gymnostachydoidcac. Oron ti oideae. l'othoideac. Monsteroidcac, Lasioitkac, Calloid.:ac y Zamiocu/cnJ!Cona/opus (Aroidcac) tienen granos de polen apcrtuardos (princiJla lrncnLc monosulcados. algun os disulcados), sólo uno ~ pocos sin apcr· Lura (como algun os d.: los gra nos poliplicados). Es interesante que d poco frecuente caraclcr zonosulcado ~e encuentra indepcndicnLcmcnLc en dos subfamilias: 1- tonsLe roideac y Znmiol'llieas!Grmnlopus (Aroidcac). Ningun miembro de la subfamilia Aroidcac tiene polen apcrturado. Además. toda la su perficie del grano de polen es de naturale7,1 apertura!, por lo que estos gra nos de polen deberían llamarse omniapertu rados en lu ga r de inaperltlados. Es de destacar que al menos 1O géneros muestran el ca racter poliplicado y. por tanto, compan.:n caracteres en paralelo con el polen cfcdroidc (Ephc·dra). Sorprende que sólo dos géneros poliplicados tengan un estrato externo estable bajo la acctolisis. mi entras que el caracter poliplicado de los otros 8 géneros se picrd~ con esta. A la luz de es to~ llamativos caracteres. se eval1ía el pobre registro fósi l de Araccac y la potencial con fu sión de algúno de sus polcncs poli plicados con polen de cfcdroidc acLUa l o fósil. PALAI3RAS CLi\VE: Araccac. polen. cxina. cktcxina, cnd c.~i na. accto l isi~ .

JNTRODUCfiON Cretaceous. However, the famil y has a poor fossil record in general (MAYO e1al. , 1997). The Araccae, an hcrbaceous monocot This depends mostly, but not exclusively, family, are plan ts which are fa miliar to 0 11 the complete absence or woody parts. lts everyo ne, but paradox ically little known. fossil pollen record is tin y, without on first Popular house planls include of, e.g., sight suffi cien t reason. Mons1em, Alllllll riwll, Philode11dron or Die.ffe11bachin. The family is characterized The extraordinary poor pollen record by the di stinctive inllorescence (a spadix with depends not only on the life fonns and thc bi sexual or unisexual Oowers) subtended by a environmental cond iJions, which do not fa ­ spathe. Many Araceae are fam ous for their vor fossil isation. The main reason is on one special ized, unique pollination biology (e.g.. hand the unique pollination mechanism Ar11111). Pollen is shed (mostly) as single (often a moist, warm keitle trap) and on thc grains, bul is often loosely connected, thus oth er hand the very unco mm on wn ll forming threads (e.g .. Zcllltcdcschin). strat ifica tion typical for many Aroidcae (W rmER el al., 1998, 1999). Only quite rccentl y Members of Araceae, currently including lindings of Eocene fully zonat e poli en grains o ver 3.300 spccies in JOS genera (lvLwo el al. , could be related 10 disti nct ful ly zanate 1997, 1998), generally live in (sub-) tropical Araceae (ZETrER el al., in press.). Araceae moist or wet habitat s, only rarcly in dry ones. pollen show a widc rangc or diversity wi lh Lifc forms are very diverse ranging from rcspect to poli en wallmorphology and exi ne aquatics to terrestria l. and rnembers rnay be scul pturing (GRAYUM, 1992). Nevenheless, climbi ng or epiphytic plan ts. The fa mily is the tiny fossil record of Araceae pollcn da­ now rc garded as basal in th e monocots tes only from a few Eocene and Miocene (Angiosperrn Phylogcny Group , 1998). palynomorphs, all auributed 10 Spalhiphyl/um Concluding from the rise of the angiosperms beca use oftheir polypl icate appearancc (VAN in the (Ea r~y) Cretaccous, it is 10 be expected DER HMt ~LE N & G ARCL1\ DE Murts, 1966 ; thal the Araceae ex ists at least sincc Late M ULLER, 198 1; fV(AYO el a(. J'ffi). 'Í1l LS

6 Polen Principal po/len features i 11 1h e 1\ rum Lilies (Araceae)

discrcpancy bctween the fact that Araceae sample of Araceae taxa was investi ga ted are an old, basal branch of the monocots, (more than 60 spccics out of .n genera from and the paucity of published fossil palien all subfamilics, e f. Wr:ur:R el al .. 1999). Only findings is intrigu ing (1-I ESSEel al., 1998). thc following taxa are illustrated: Swudnem colocasiifolia K. Koch, SI. hemyana Engl.. Thc scarcity of fossi l Araceae palien St. assamica l looker f , St. grifjirhii SchotL suggests that taphono mic conditions for For more pollcn micrograph s showing the thcir preservat ion differ from those required high diversity the reader is referred to the for the preservation of palien types wi th papers by GRAYU~ t ( 1992), Wr:om el al. ( 1998, stable exines. The textbook view that the outer 1999), and 1l ussr: el rrl. (2000a, b). pan of the Angiosperm pollen wall (always) consists of a highly resistan! organochemical Preparations for TEM and SEM wcre substance, called sporopolleni n, and will conductcd in the same manncr as describcd in WEBER et al. ( 1998) and in 1-I ESSE et al. become a foss i 1 as it stands, must be (1999). Acetolys is was done following the questioned, at lcast for many Araceae. The Erdtman techniquc, bu t was al so carried out more basal subfamilics of Araceae show a on glass slides. Somc pollcn material was sporopollenin-containing ektex ine (with trcatcd in 5 % boi ling KOll for 20 minutes, tectum, col umellae, and a foot-layer) and indcpendcn t of acctolysis. us uall y a th in, more or less compac t endex ine. Strikingly, this is not the case in the largest subfa mily, the Aroideae, where RESULTSAND DISCUSSlON oftcn an acetolysis-susceptible outer layer (lack ing a subd ivision in tectum , columell ae and foot- layer) and a spongy, thi ck l. !1/IUM (A HO JI)EAE, ARA CEA E) PO LLEN: acctolysis-resis tant end ex ine fo rm s th c SMOOTII OR SI'INY, TIIIS IS TIIE QUESTION sporoderm. A second characteri stic feature Thc case of A mm poli en with respect 10 of Aroideae pollen is th e absence of itsornamentation is typical for quite different apcrt ures, whilc all other subfamilies of reports on the actual ornament ation. Araccae gcnerally have aperturate palien According to the applied preparation (w ith few, but signi fi cant except ions). mcthod (Ta b. 1) Am111 pollen was reportcd asto be cither smooth or spiny. Especial! y The aim ofthis paper is to give an overview aftcr thcapplicat ion of acetolysis, a common on thc palien wall diversi ty in the family mcthod in pal ynology to clcan thc pollen Araceac and, to show the extraordinary type surfacc, the pollcn grains of Anmr, but also ofpollen wall stratilication within thesubfamily of many other Araceae- Aroideac, was qui­ Aroidcae. tedissirnilar (c.g., B EUG, 196 1; B ENZING, 1969; TI!ANIKAIMONI , 1969; P ACINI & J UN II'ER , 1983). Only fcw authors, c.g., RM & SAXG'IA ( 1966) MATERlALANDMETHODS wondcr about thc appcarancc of thcir (acetolyscd) Pis1ia materia l comparcd to Thc poli en material was obta ined mainly Erdtman's dcscription in 1952. from the Botanical Garden Munich, and also from th e Grecnhouses of the Botan ical Thc mai n reason of diffcring rcports on Gardcn ofthc University ofVicnna. A large thc actual surfacc ornarncntation of many

Vol. JI (2000) 7 Hesse, M.

Araceae polleo is the uncommon chemistry Recently research was focused upon this of distinct wall stra ta. The majority of strange fcature (vAN DER HA~I el al., 1998; Aroidcae polleo shows an ornamentation, WEJJERe/a/., 1998,1999;HEssEe/a/.,2{XX)a-b). which is not made of sporopollenin, but of exclusivcly tapetum-derived substances 2. TYI'ES OF I'OLLENWA LL STRATIFICATION IN (polysaccharidic, according to thc Th iéry ARACEAE (TAn. 2, Ftcs. 1 & 2) rcaction); below th is outer !ayer a thick, Arac eae polie n wallsdiffe r signi ficantly spongy endexine is present (WE13ER el al., in morphological and chemical composition L998, 1999). rn so rne Laxa th e surfacc and are represented - to date - by two qui te ornamcntation is not removed completcly or different types (each with two subtypcs, immediately during acetolysis procedurc WEUER el al., 1998, 1999). Both types, and (VAN OER HAM el al., 1998). The effect of the al so the subtypes, have a different resistancc acctolysis procedure depends on temperature to acetolysis and likewise to KOH treatment. and duration of the reaction. Rcmnants of the With sorne precaution a quite di fferen t former ornamentation in distinct Aroideae resistance to decay can be concluded. In the pollcn may depend on incomplete acetolysis more "conventional" type, represented by procedure or treatment not at boi ling Spmhiphyllum, the speci fic pollen omamen­ tcmpcrature. lnteresti ngly th is conflicting tation is preserved by the acetolysis-resistant reports wcre cither ignored for a long time, or ektexine. In the other type, represented by was usually ex pl ained in a simple manner: Dmcunculus, only the highly unspecific. Araceae, espccially Aroideae pollen grains smooth endexine remai ns, and the specilic oftcn cannot withstand acetolysis. poi len ornamentation is gene.

Curiously enough, the clear statement a) Pollen wallswith anektexine(Type 1in in a leading scicntific biological j ournal by WEUER el al., 1999): A potassium hydroxide­ PACINI & JuNIPER ( 1983) on Arum pollen wall and acetolysis-resistant, verrucatelreticul ate, tectate/columellate, or th in and smooth stratification ( ... spaccs ... filled with PAS ektexine upon a loosely packed endexine. positive material produced by the tapetum Examples include: and formed spines on the ex ine") failcd - for Lysichilon, Allll111rium, Ca­ and any reason - make an impact to the Scientific lla, Sparhiphyllum, S1e1wspermmion, 1\ risaema. The ektexine mayal so be thi n and community. E ven onc of the authors (Pacini) smooth, as in Spmllicarpa and . has mcntioned th is finding a single time Note: in the latter four genera a th ick, spongy again (in PARKINSON & PACINI, 1995:71). Simi­ endexinc ispr csent throughout. Figure 1sho ws lar reports by K UPRIANOVA & T ARASEVICII the situation. ( 1984 ). and TARASEV ICII ( 1990), respecti ve! y also madc for many years nearly no impact b) Pollen walls without an ektexine(Type 2 to the Scientific Community. The publication in WEBER el al. , 1999). A thick, spongy, and to in Russian may be an explanation. Only a certain extent acctolysis-resistant endex ine T AKI ITI\JI\N ( 1997:581) is recalling tl1ese papers; is present. This endexine may either becovered he interpretes correctly the acetolysis-suscep­ by an ornarnentation of polysaccharidic naturc, tible Pislia-exine as a separating feature wh ich is not resistan! to acetolysis or bctwecn (hi s families of) Pistiaccae and pota ssium hydroxide treatment, [e. g., in Amm Lemnaccac. Howcver, he calls the fcature as (PACINI &JUNIPER, 1983; WEuER ef(l/., 1999); in being singul ar for Pistiaceae only (!). Sauromarum (WEilER el al., 1998); in Pislia

8 Polen Principal po/len feawres in ti! e Artllll Lilies (Araceae)

(WEBER el al. , 1999); and in ektcxine. This striking differcnce to the palien vu/garis], ore ven may lack such a !ayer (e. g., stratification of !Gorwtopus was in Zamedescilia, WEBER et al., 1999). Figure 2 onc of the arguments, togcthcr with severa] shows this uncommon stratification at hand of morphological arguments to propose a new palien grains. subfamily, the Zamioculcadoideae (BOGNER & HESSE, in publ.). The poll en grains of the Pollcn wall stralificalion wilh rcspcct to ils rcmaining Araceae with unisex ual flowers, i .e. distribulion within thc Araccac. the aperigoniate Aroideae, which represen! the The palien walls may consist of an bulk ofwhatiscommonly called "Ayum Lilies", acetolysis-resistant. elaborated ektexine with are generally characterized by an equally thick, an endexine below, which is thin in non­ spongy, widely acetolysis- res istant endexine. apertura! arcas, but thick and inhomogeneous Very uncommonly this endexinc is covered in aperture regions. This manner of palien wall either by a skin-like, acetolysis-resistant stratification is typical for all subfamilies ektexine, or an outer stratum, which is not (according toMA YO et al., 1997, 1998) with bi­ resistan! to aceto lysis. For additional sex ual flowers, the Gymnostachydoideae, discussion and revicw sec Hr.ssE et al. ( 1999) Orontioideae, Pothoideae, Monsteroideae, and HESSE et al. (2000a, 2000b). L,sioideae and Calloideae, but is found al so in few taxa with unisexual nowers, Zamioculcas and Gonatopus, i.e., two of the three perigoniate 3. Al'ERTURE TYPES Aroideae genera (sensu MAYO er al., 1997). GRAYUM (1992) presentcd an exhaustive The third member of the perigoniate Aroideae, paper on pollen wall features in Araceae, , shows a thin, slightly lamellated including the apertura! con !iguration. In the endexine below a continuous, thin, intectate subfamilies Gymnostachydoideae, Orontioi-

Aroidcac (Ara ccac) Ornmncntation bcrorc acctolysis Ornamcntation artcr acctolysis

Arinac (tri be) TI1anikaimoni 1969: spiny TI1anikai moni t 969: smooth l'acini & Junipcr 1983 smooth Pacini & Junipcr 1983: spiny Ocu)! 1961: smooth An1111 ssp. Grayum 1992: spiny Erdtman 1952: smooth Rcillc 1998: smooth

Ambmsina bnssii Grayum 1992: strimc-pli ca tc Rcillc t 992: smoolh Ocnzing: vcrrucatc

TI1anikaimoni 1969: plica te TI1anikaimoni 1969: smooth Tarascvich 1990: plica te Tarascvich 1990: smooth Pi,¡tia .11m1iotes Kuprianova & Tarascvich 1 98~ : plicatc Kuprianova & Tarascvich 1984: SlllOOlh Erdtn~1n 1952: plicatc Raj & Saxcna 1966: srnooth 10 obscurc sp. Grayum 1992: spiny Tarascvich 1990: srnooth Alotasia sp. Grayum 1992: spiny Tarascvich 1990: smooth Zmnimrpn sp. Grayum 1992: spiny Tarascvich 1990: srnooth

TABLE 1: Sorne Araceae with differing ornamentalion before and alter acetolysis treatment.

Vol. 11 (2000) 9 Hesse, M.

deae, Pothoideae, M onstcroideae, Lasioideae not detached; this feature is restricted to and Calloidcae, we lind mostly monosulcate Angi osperm s and is found espec ially in pollen, but rarcly al so diporate, zonosulcate monocols (cf. MuEt.LER-STOLL, 1956). Thus (in Monstcreae) and i naperturate. In thc we prcfer th c term ornniapcrturatc in Aroideae (scnsu M AYO et nf., 1997), pollcn is describing the Araceae poli en grai ns lack ing inapcrturatc, e.g., Steudncm (Fig. 2). wi th fcw aperturcs. The term inaperturate shou ld be cxceptions, e.g., zonosulcate in Zamioculcns restricted to thosc few cases, whenthc exinc and Gonntoptts, proposcd for a new subfamily splits and gets completcly detached. This :Zamioculcadoideae (B OGNER & H ESSE, in pub!.). featurc is found onl y in Gymnospenns (e.g., It is wonhy to note thal the spectacul ar TtLws: Muw.ER-STOLL, 1948; Ephedra: Et.­ zonosu lcate type was .,invemed" (at least) two GtiA7J\LY et al., 1998; or Gnewm: MAtiESIIWARt times in the Araceae. The zonosulcate pollen & VASIL, 1961:80). In supcrficially similar grains in M onstereac are only supcrlicially si­ angiospenn cases, e.g., in Populus or 1/dipa, milar to those of Zamioculens/Gonalop11s th c split cxine docs not get complctcly (Aroideac) (e f. l-IESSE eral., 2000b.) detachcd: often small pm1s ofthcexinc rema in.

Tcrminological note: omniapcrturatc ver­ sus inapcrturatc .¡,i\NCtOSI'ERi\1 I'OLLEN: ITS RESISTANCE Araceae pollen grains lacking apenures TO DECAY (WITll SI'ECIAL REFERENCE TO are olkn called inapcrturate (e.g., G RAYU~ t . ARA CEA E) 1992; F URNI:.SS & RuoALL, 1999). PuNT et ni. STEWART& ROTi tWELL( 1993: 14) point out ( 1994) proposc the term inaperturate for pollcn that the degrec of prescrvation depends grains without aperturcs (Populus and Tnx11s t.:spccially onthe amount of ti ssue decay that as examplcs), while omniapcrturate in thcir occurrcd prior to fossilization. On the onc hand, scnse dcsignatcs such pollen grains, whcre thc individual rcsistancc to pollen dccay thc whole surface is apertura! in nature. depcnds on thc respecti ve chem ism and consistcnce of the pollen wall strata, and to a ln our vicw. inaperturatc is not lesser degree on the apertura! condition. Only synonyrnous with omni aperturatc. and a few expcriments ha ve bccn done to evaluate o mniapcrturatc is no subsurnption of thc sclcctivc destruction of cx incs by chcmical inapcrturatc. Inaperturatc is a morphologit.:al (Rws~ t A, 1969; RowLEY & PRU ANTO, 1977) or tcrm, while om niapcrtu ratc points towards a mcchanicaltreatment (CA~tPOEU.., 1991 ). On thc function, and thu is a functional tcrm. othcr hand, of course the degree of prescr­ Following THA<"tKAI:-.to:-;¡ (1978. 1984), pollen vation depends also on cnvironmental factors of Srylochaeron and of other Araceae with (e. g., soiltypes), or post-depositional altcra­ ''inapcrtu rate" pollcn should be clcarly tions, but publishcd data and considcrations de ignated as omniapcnurate (WEOER et ni., inthis dircction are likewisc rare (GEit\tERAAD 1999:429). T he entire pollen surface of et n/., 1968; ELSIK, 1971 ; 1LWI:'\GA, 1971, 1984; Srylochaeton is apertura! in nature, no TRAVERSE, 1988; Rowt.EY erni ., 1990; STEWi\RT morphological apcnure is prese nt, and thc & RoTIIWEU., 1993; all also for review). intinc is uniformly thickcned. The pollen tube Furthcrmorc, questions conccrning polymeri­ can be formed cverywhcre. Thc ex inc is zation and stability of sporopollenin rcmain rcduced, as always in omniapcrturate grains, widcly unsett led. Both aspccts will be and splits in various manner but is general! y discussed in the following paragraphs.

10 Polen Principal pol/ell [entures i11 tire Arum Lilies (A ra ceae)

The overwhelming maj ority of boi ling KOII). Its stabil ity is intennediate angiosperm palien grains, includin g the between the resistan! tectatc-columell ate subfamilies of Araceae (except Aroideae) typeofstratification and thcextJemely fragile, sensu MAYO el al. ( 1997), has stable, acetolysis­ ex ine-lcss type menti oned abovc. resistant exi nes. Such poli en should be found widely unmod ificd in the fossil record. For a The peculiar cnvironmcnta l condition and pollination ccology ofmany Araccae: atlcast long time it was generali y accepted that in part responsiblc fo r the poor fossil re­ palien wall s ha veto consist of an extreme!y cord of Araceae pollen? resistan! organic polymer, call ee! sporopollenin, Araceae are found prcferably in tropical one of the most resistan! chemicals in nature. to subtropica l climates, relatively few in However, it is well known that in a few tcmperate toeve n subarctic regions. Domina­ Angiosperm families with peculiar pollination ti ng habitats are tropical to subtropical ecology pollen grains complete!y lack an exine (freshwater) swamps or ponds or ri ver margins, (e. g., in some taxa of the Hydrocharitaceae: or warm eutrophic soil (only fcw taxa prefer PETITIT, 1980; or Cymodoceaceae: McCm

Spatlriplryllum /)riiC/1/ICIIIIIS Before acc tolysis aflcr acclolysis 13cforc ncclolysis aftcr acclolysis prcscnt PAS-positivc !ayer, cktcxinc tcctum. col umcll ac unmodiflcd not callcd an ckJcxi nc by ab cnt and foot-laycr \VclJcr et al. ( 1998) cndcxinc prcscnl unmodiflcd prcscnt prcscnt, but modi fi cd intinc prcscnt abscnt prcsc nl absc nt

TABLE 2: Pollen wall slralificalion in main pollen lypes al Araceae, befare and alter acelalysis.

Vol. 11 (2000) 11 Hesse, M.

lower if a stable cktcx inc is present, but will to decay. Araceae palien with an ektexine take place toa greatcr cxtentespecially if"weak survive the acetolysis treatment intact as points" (less stable, fragi le sporodenn rcgions) most dicot palien docs. However, taxa without with are present. Thc pollen walls ofthe m<~ority an ektexi ne do not survive acetolysis. Wh ile of Araceae have indecd somc fragi lc rcgions, the spongy endex ine is, in principal, which may reduce thcir chance to become acetolysis-resistant (Wmn:R et al., 1998; VAN fossil. The fu lly zonate ("hamburger-like") DER I-IM1 et al., 1998), it swells greatly and condition of somc pri ncipi ally stablc palien may split during acetolysis. lf the endexine grains with an acctolysis-resistant cktexinc remains intact it has a fair chanceofbecoming could be seen as onc wcak point: such pollen fossi lized. Thus so far unrecognized Araceae genernll y separatc in to ha lves during pollen with this typc of endexine should be acctolysis (Howevcr, quite recently findings present in the ac tu al fossi l record and ofEocenc fully zona te pollen could be relatcd therefore should be found (but often in a to full y zanate Araccac pollen types, (Zrn1:R surprisingly modified form). ct al.. in press.). A second weak point may be the spongy endcxi nc of most Aroideae: this One can hardly avoid questions about the type of endex ine tcnds 10 swell enormously extreme!y poor foss il pollen record of Araceae during acetolysis, and therefore may split. In taxa with a stable, acetolysis-resistant ektexine. some cases (c.g .• Mon tcrcae) such acetolysed The many monosulcate palien grains typical pollen indeed show an unmod ified cndcxinc. for the basal subfamilies of Araceae in parti­ Jlence, the spongy endexine in Araceae may cular should ha vc a good fossilization hnve a grealer degrcc ofstabi li ty than one might potential. J-l owever, the presence of an ex­ expect. tended sulcus of many poli en grai ns, e.g., in Lysichito11, may be another fragile or weak Thc prcsumcd fossilization potential of point. lt is worthy to note that this pollen Araccac pollcn walls type ha s alm ost no fossi l record (on ly The mcagre fossi l record of Araceae is SRJVASTAVA & BrNDA, 1991, associate cnigmat ic. Thc reasons my be found either dispersed Eocene palynomorphs with in th e conflicting reports o n pollcn Pothos palien, which has a stable ektexine, morphology (unconspi cuous, oflen smooth somewhat representative for this palien or coll apsed pa lynomorphs are overlookcd type). The probably sign ifi can! exception is or mis interpreted), bu t also on the oftcn poor Spathiphy/lum: the continuous ektex ine in fossili zati on poten ti al of such poli en grai ns. the pl icae and the lack of any aperture may The degree of preservation depends on the cause a high resistance to decay. In contrast, amount of tissue decay that occurred prior the zonosul cate grains, found within the 10 fossilizali on and of coursc al so on Zamioculeas!Go11alopus and independently environmental faclors. The individua l in the Mo11stereae, probably ha ve a smaller resistance lo pollen decay is influenced fossilization chance. In the non-apertura! ....."l.l l-~'""''-" ' !1 ·J-:1 "\..thc• ·u\.\\...10 V'lr\t h ..... ~'-'.::t t.7\,..-\.. '\ ''r\... pv•\l.11 regrons the exme cons1sts ol a massrve wnll stratifi calion, and - toa lesser degrec- by ektexi ne (w ith impcrfora te tectum, short the apertura! condi tion. columellae, anda compacl foot-layer), anda The vnri ous types of poll en walls in thin, sli ghtly spongy endexine. The weak Araceae are wi thoul doubt variably resistan! point of thesc zonosulcate (,fully zonate")

12 Pole11 Pri11cipal polle11 jent11res in the A 1'11111 Lilies (Araceae)

pollen grai ns could be represented by the thin ektex ine !ayer covers the endexine in zonosulcus: a thick, bilayered, distal! y tubular the ape1ture region (HESsE et al., 2000b). 1-Ience, inti ne is covered by the endexine only. the zonosulcate condition may be more stable According to GRAYUM (1992) and HESSE et al. than firs t supposed. Recentl y, fi ndings of (2000b) after acetolysis the Mo11stereae Eocene fu lly zonate pollen grains or "pollen pollen grains split into hal ves. lnterestingly hal ves" were related to Araceae (ZE'rrER et al., this is not the case inthe zonosulcate grains in press.), wh ich was tentatively done earlier of Zamioculcas and Go11atopus, because a by TIIANIKA IMONI et nf. ( l984).

FIGURE 1. Anthurium radicans K. Koch. Porate, reticulate pollen grains in SEM and TEM view. A, poli en grain in cross section. P porus. B, detail of cross-sectioned pollen grain. Pollen wall stratification: t tectum, e columellae, fl foot·layer, en spongy endexine, i electron-dense intine. C, individual pollen grain. D, detail, with porate aperture.

Vol. JI (2000) 13 llessc, M.

T he second type of pollen grains with S. A CLOSE LOOK ON A Sl'ECIAL CASE: TIIE an aceto lysi s- res i stant !ayer upon the l'OLYI'LICATE CON DITION IN VARIOUS ARA CEAE, E/'1/ fi)R¡\ ANO "El'IIEDRO IDS" AS spongy endex ine general! y may have a much A 1\IATI'ER OF CO NVE RGF.NCE smaller foss il izatio n potential. Duri ng Dispcrscd polyplicate cphedroid pollcn acetolysis the dimcnsion of thc poli en grain occur in scdimcnts ranging from Lowcr Pe1mian enl arges enormousl y. The endex ine quickly to Rcccnt and are especially abundanl in the swclls and often gct ruptured indicating thn t Mid -Crctaceous, but also common in the thc endcxine cannot stand completely lhis Tc11i;uy (e.g., KRUT/SCI I, 1961; TAKAIIASIII et al., chcmical stress. Pollcn of thi s lype should 1995; and especial! y CRANE, 1996; for review ha vc a considernble fossilization potential and discussion). or the numerous ephcdroids only if the spongy endcxi ne is covered by only threc genera have becn cxamined using an acelolys is-rcsista nt eklcxinc. Generally theT ransmission Elccu·on Microscope (TEM): thc ektexine is more resistnnt to microbi­ Ephedripites medio!obnrus Bolkhovilina olooical attack than the endexinc. As in b • (TREVISAN, 1980), E. l'irginiaensis Brenncr and Calndiun1 or SpMhicarpa, lhe cndcx1ne E. mulricosrarus Brcnner (KEDVES, 1994), rcrnains covered by the cktexine, and docs Equiserosporites chin/eann Daughcn y not !>plit or swell (our unpubl. results). lf (ZA\\\DA, 19s.t;PococK& VASAo\"lliY, I988),and fou nd as a fossil such pollen would typically Cometipollis rcticulaw Pocock & Vasanthy form inconspicuous smooth (collapsed) (PococK& VAS,\t-'lliY, 1988),all fromL1urasian ovoicl s o r bca n-shaped bod ies. T hcsc localitics. The ephcdroid poli en grains from thc products of partial decay may be perhaps Lowcr Crctaceous of Brazil, a Gondwana misintcrpreted as fungal spores (BEUG, 196 1). locality, are most similar lo Ephedripites I3ut without know ledge of lhc polcnlial (OsooRN ct ni., 1993). Somctimes ephedroid dram atic change from spi ny 10 psi late pollcn pollcn are found in siru, for eample, attachcd surf:1cc at lcast such smooth pa lynomorphs to thc Early Creta ceous prc-nower organ of will not be recognized as A raccac pollcn. Vi th iman tlw (KRA SS ILOV, 1997). Foss i 1 The third 1ype of pollen grains should ephcdroid poli en grains may rcprescnt an arti­ bchave in a different manncr: the sp iny, or ficial group (OsuoRN et al., 1993). l lowcvcr, vcrrucate, or striate pollen ornamcnlation of cphcdroid grains may share affinities wi th many Aroidca\! is made of polysaccharidic various modcrn taxa and the Gnctalcs or substances (W euER et al., 1998. 1999), not Araccac in particular. Therefore, it was resistan! LO acelolys is and lhus has surely qucstioncd if sorn e of the presumed Gnetalean no fo~sil i z at ion potential. ln con tras t the dispcrscd pollcn grains might be confuscd smooth spongy endex ine, which is prescnt in with angiosperm polyplicate pollen grains. all Aroideac, probably has some fossilizalion Polyplicatc, inapcrturatc ¡JOIIen grains (in potential. 1t shows a restricted rcsistance to part strongly rese mbl ing thc var ious acctolvsi s: the clia mctcrs of tll es.e ovoicls or ·'cptlc&o,(t"' types)' ex 1st' ,¡, severat' reccnt' sphcr;s are cnlargccl. but simultaneously the gymnospcrm and angiospcrm taxa(s urprisingly pollcn grains often collapse and ma y ruptu rc. within two subfamilics of the Araceae 10 ge­ Su, if rcsistant to dccay and found in cl ispersed nera with polyplicate poli en exisl). Polyplicatc form, the pollcn rcmnants may appear ns pollcn grains of Araccae (Spnthiphylftllll, rupturcd. collapsed, inconspicuous bodics. /lolochlamys, Am01plwphnllus, Pseudodm-

14 Polen Principal po/lenfearures in rhe Amm Lilies (A raceae)

comitun, . , Stettd11era, What about a possiblc confusion and Pisria), and Ephedraceac (Epltedra ) werc conccrning "ephedroids" (di spcrsed recent analyscd with regard to their pollen walls. From and fossil poli en ofthc Ephedra-type including thc position of a palynologist workin g thc fossil form genera Ephedripires and stratigraphicall y it is understandable that Equiserosporires) and Spa rltipltyllum? (almos!) all dispersed polyplicate pollen grai ns According to H uv:-~ 11 ( 1975) Ephedra and are called "ephcdroids", and often considered Sparhipltyllum sharc six p::~ra ll c l features, as related wi th Gnetales. including the (all egcd) s::~ me tetrad arran-

FIGURE 2. Sleudnera ssp. Omniaperturate, polyplicale pollen grains in SEM and TEM view. A, Sleudnera griffilhii Schott. Pollen grain in cross section. B, SI. griffilhii Schott. Detail of cross-sectioned pollen grain. Pollen wall stratification: pi acetolysis-susceptible plicae (ribs) in cross-sections, en spongy endexine, i intine. C, SI. co/ocasiifolia K. Koch. Acetolysed pollen grain. D, SI. henryana Engl. Pollen grain before acetolysis.

Vol. 11 (2000) 15 Hesse, M.

gcmcnt. In fact there are only four parallel pollcn fromAmbr osina is "expected" to occur featurcs: l. thc presence of acetolysis-rcsistant in a polyplicate condition, but in fact this poli en, ridgcs, 2. thc whole exine is resistant to decay, if al all preserved, will not appear in a polypli­ 3. the cvenly thick inti ne, and 4. the inapcrturate cate, but in a psil ate condition! In contrast, as cond ition. llowever, the two genera are all Eplledra-"ephedroids" only the pollen separated by livc different features: J. ridges grains of the Araceae genera Spmhipllyllum, not columell ate (Ephedra) versus columellate 1-/olocltlamys, and probably Arisamm have ridges in Spnrhiphylltmt, 2. endexinc lamellatcd high fossilization potential: they should be and e venly thickened (Ephedra ) or not found as polyplicate grains in the fossil re­ lamcll ated and th in (Spathiphyllum). 3. in cord. But a "mix-up" of these pollen grains Epltedra the cndexinc is always totall y with Eplledra or "ephedroid" pollen grains is covered by thc continuous cktcx inous ridgcs, unlikely: form and details of the respecti ve while in Spmltipltylllltll the discontinuous ridges diffcr signilicantly (HESSE el al., 2000a). ridges do not covcr the endexinous grooves, 4. plicate pollcn caps in Ephedra absent or much smallcr than in Sparltiphyl/um, and CONCLUSIONAND OUTLOOK 5. tetrad arrangcmcnt in Eplt edra mostly tetrahcdral (Et.-GII AZALY et al. , 1998), in An invcstigation of recent and especially Sparhiphyl/11111 isobilateral (Huv:-: 11, 1975; fossil, dispcrsed poli en material by TEM is time TII AN IK AI.\IONt, 1969). So confusing Spathi­ consuming and exhausti ve. Nevertheless phy/111111 and Epltedra pollen grains is unlikely: important palynological features can be found m lcast form and na tu re of t.he ridgcs and the only if using the TEM with its analytical prcsence of the distinct "caps" in Spa!lti­ strcngth. A non-sporopolleninous outer pollen pltylltttll are clcarly separating features. wall !ayer seems 10 be a unique featurc of Aroidcae poli en: the nature of the respective H ESSE et al. (2000a) comp ile their spi nes, ribs, ve1Tucae or whatsoever is neithcr findings togcth cr with th e publi shed ontogencti call y nor chem i call y homologous to informations by Et -GI IAZALY & Rowu;v corresponding features of other taxa as, e.g., ( 1997), Et.-GII AZ,\LY e1 al. ( 1998), G RAY L' ~l Spa!ltipllyllum (Monsteroideae, Araccae: ( 1992), H UYl'\ 11 ( 1975), LuGA tUXlN el al. (1987/ W EBER el al., 1999), and this might be vali d for 88), RE!Lt.E ( 1992, 1998), TttM IKM IOSI ( 1969), -so far known - all other angiosperms. VA':-1 DER H M I e / a/. ( 1998), and ZAVi\Dt\ (1990). It was clcarly demonstrated thatthe various Sometimes seemingly well established polyplicatc types are mere!y supc r!icially si­ tcxtbook vicws should be abandoned, in our milar. The polyplicate palien grains distinctly case that the outermost poli en walllaycr with diffcr in various morphological details and its oftcn typical ornamentation must consist cspecially within thc Araceae in theuncommon of sporopollenin and thus must be found more chemical conwosition of the rid_ges. lt is or lcss unmodilied, either in modern pollen no­ concluded that the Araceae polyplicate pollen ras or even in the fossil record. As every grai ns ha ve ei ther a low fossilization potential experi enced palynologist knows, such and - if at all prescrved - will be found in a insignificant pal ynomorphs may be casil y hi ghl y modili ed form (c.g., , Ambrosina overloked, therefore not realizing the possible and Slettd11era, as smooth. ruptured bodies, taxonomic value, or may be supposed as an rcspecti vcly). M u LLE!~ (1981 ) pointedoutthat artifact.

16 Polen Principal pollenfeatures in the Arwn Lilies (Araceae)

Spccial attention is called to many incons­ CRANE, P.R. ( 1996). Thc fossi 1 history of thc picuous, smooth, oftcn collapsed or ruptured Gnctalcs. Int. J. l'lant Scicncc 157(6 Suppi.):S50-S57. grains, sometimes resembling fungal or fern sporcs. A smooth ovoid or sphere may be EL-GHAZALY. G. & ROWLEY. J.R. ( 1997). Polleo deriving either from pollcn grains with a thin, wall of Ephedrn foliaw. Palynol. 21:7-1 8. smooth, acetolysis-resistant ektcxinc, or more EL-GHAZALY. G.: ROWLEY, J.R. & HESSE. M. oftcn from originally spi nose, verrucate or (1998). Polarity. apcnurc condition and polyplicate pollen grains with an acetolysis­ gcrmina tion in poll cn grains of Epht'dra (Gnctalcs). Syst. Evo l. 2 13:217-231. susceptible ornamentation. Thosc ''overlooked'' palynomorphs should be typical for many ELS IK, \V. C. ( 197 1). Mi crobial dcgradation of Aroidcae, represen ting two thirds of all sporopollcnin. In: J. IJ ROOKS; P.R. GRANT; M.O. MUIR; P. VAN GIJ ZEL & G. SHAW (eds). Araceae genera. Sporopollcnin, pp. -1 80-511. Acadcmic Prcss, London.

ACKNOWLEDGEMENfS ERDTMAN. G. ( 1952). l'nllcn morphology and plan! . A ngiospcrms. A lmq vist Sincere thanks are due cspecially to Mr. & Wiksc ll . Stockholm. Josef Bogner (Botanical Garden Munich), f' URNESS. C.A. & RUDA LL. P.J. (1999). lnaper­ providing most of thc Araccae material, to lllratc pollcn in Monocotylcdons. lnt. .T. l'lant Prof. Dr. Martina Weber, to Dr. Heidemarie Sci. 160:395-41-1 . Halbritter, to Mrs. Andrea Frosch-Radivo GERMERAAD. J.l-1.; IIOPPING, C.A. & MULLER, and to Mrs. Ursula Schachner (Vicnna), for their J. (1%8). Palynology of Tcrtiary sedimcnts extensive discussions and help in technical from tropical arcas. Rcv. l'alacobot. Palynol. 6:189-3-18. matters. Support from thc Hochschuljubila­ cu msstil'tung der Stadt Wien ist gratefully GRAYUM, M. ( 1992). Comparativc (!X tcrnal polleo acknowledged. ultrastructurc of thc Araccao.: and putati vc ly rclatcd taxa. Monogr. Syst. Uot. Missouri llot. Gard. 43: 1- 167.

REFERENCES HAV IN Gi\, A.J. (197 1). An experimental invcstigation into thc dccay of r oll en and ANGIOSPERM I'IIYLOGENY GROUI' (1998). An sporcs in various soil types. In : J. llROOKS: ordinal classificati on for th c familics of P.R. GRi\NT; M.D. MUIR; P. VAN G IJ ZEL nowcring . Ann. l\lissouri llot. Ga rd . & G. SIIAW (cds). Spnrnpollcnin, pp. 4-16· 85:53 1-553. 479. Acadcrnic Prcss. London. llENZING. L. (1969). llcitrng zur Kltirung dcr IIAVINGi\. i\.J . ( 1984). A 20 yc;tr experimental Vcrwandtschaftsvcrhli ltnissc dcr Tribus invcst igation into thc di ffercntial corros ion Arcac (= Aroidcac-Araccac) auf vcrglci· susccplibility of pollcn and spores in various chcnd-hlütcnmorphologischcr Grundlagc. so il typcs. l'ollcn Sporcs 26:5-11-55 8. Disscnation Univcrsit:il Mainz. HERENDEEN. P.S.; CREPET, W.L. & NIXON. llE UG, II.J. ( 196 1). Lcitfaclcn dcr l'ollcnbc­ K.C. (199 -1) . Fossil flowcrs and pollen of stimmung. G. f'ischcr. Swugan. Lauraccac from thc Uppcr Crctaccous of Ncw Jersey. l'lant Syst. Evol. 189:29-40. CAMI'OELL. l.D. (199 1). Experimental mccha­ nical dcstruction of pollcn grains. Palynol. II ESSE. M.; WEBER. M. & HALOR ITTER. H. 15:29-33. (1998). Why is fossi l Araccac pollcn so rarc? l'alyno-Ny tt 37:6-7.

Vol. 11 (2000) 17 Hesse, M.

I!ESSE. M.: WE BER. M. & II ALBR ITTER, 11. MAYO. S.J.: llOGNER, J. & 130YCE, P.C. (1997). (2000:t). A compamti vc study of thc polyplicatc Thc Gcnrra of Araccac. Thc Royal Botanic polleo typc; in Aralcs. Lau ralcs, Zingibcrales Gardcns, Kcw. and Gnctalcs. In: M .M. II AR LEY: C.M. MORTON & S. IJLACKMORE (ccls). Pollcn MAYO, S.J.; BOGNER, J. & DOYCE, P.C. (1998). and Sporcs: l\lorphology and Diology, pp. Ar.1ccac. In: K. KUB ITZKI (cd.). Thc Familics 227-239. Royal Botanic Gardcns. Kcw. and Genera of Vascular l'lants. i\lonocoty­ lcdnns: Alismatanac and Commcli:mac IIESSE. M .: WEBER. M . & IIALBRITTER, H. (exccpt Gr:tmincac), pp. 26-74. Sprin ger. (1999). l'ollcn walls of Araccac, with spccial Bcrlin. rcfcrcncc to thcir fossili t.ation potential. G rann: 38:203-209. ~ I CONC HI E , C.A.: KNOX. R.ll.: DUCKER . S.C. & PETTITT. J. M. ( 1982). Poli en wall IIES SE. M .; BOGNER. J.; HALBRITTER, 11. & structurc ami cytochcmistry in thc scagrass WE BER. M . (2000b). Palynology of thc ,\mphibo/iJ· griffithii (Cymodoccaccac). Aun. pcrigoni atc Aroidcac: Znmiorrdras, Gmww¡ms llol. 50:729-732. and Stylorlwcum (Araccac): Grana: in prcss. ~IUELLER-STOLL. W.R. (19-1 8). Zytomorpholo­ IIUYNII. K.-L. ( 1975). Quclqucs phé n o m~ncs de gischc Studicn am Polkn von T~tws barrara L. polarité du palien il plis multiplcs du gcnrc und andcrcn Konifcrcn. J'lanta 35 :60 1-641. Spathiphyllum (Arncca c). Bcitr. lliol. J>flanzcn 50:4-15 -456. MUELLER-STOLL. \V.R. (1956). Übcr das Vcrha ltcn dcr Exinc nonapcrturatcr Angiospcrmcn-l'ollcn KEDVES, M. ( 199-1). Trausmission clcctron bci Qucllung und Kcimung. Grana l'alynol. micruscopy of thc fossil gymnospcrm (N. S.) 1:38·58. C:\incs. Stcgcd. MULLER. J. (1981). Fossil pollcn rccords of cxtant KRASSILOV. V.A. (1997). Angiospcrm origins: Angiospcrms. llol. Rcv. 47: 1-142. morphological and ccological aspcc ts. Pcnsoft. Solia and Moscow. OSI30RN, J.M.: TAYLOR. T.N. & DE LIMA, M.R. (1993). The ultrastructurc of foss il cphcdroid KR UTZSCH, W. ( 196 1). Übcr Funde von "cphc· pollcn with gnctalcan affi ni tics from thc clroidcm" Pollcn im dcutschcn Tcrti!ir. Gcol. Lowcr Crctaccous of Brazil. RC\'. l'alacobot. 10:15-53. l'alynol. 77 : 17 1-18-1 .

KU PRIANOVA, LA. & TARASEV ICII, V.T. (1984). I'AC INI, E. & JUNII'ER. ll .E. (1983). Tite ultra· 1l1c ull~tructurc of thc surfacc of pollcn gr:tin structure of tite formation and dcvclopmcnt of wall in somc gcncr:1 of thc famil y Lcnutat·eac thc amocboid tapetum in Arum italinm1 ~lillcr. and thc rdatcd genera of the family Aracc:1c. Protoplasma 117: 116-129. llo t. Zhum. 69: 1656- 1662. I'ARKINSON, ll.M . & PACINI. E. (1995 ). A LUGA RDO N, 13 .: LOB REAU-CALLEN. D. & LE co mparison of tapcta l ~ t r uc t u r c ami function TI-IOt>·IAS. A. ( 1987/88). Structurcs polliniqucs in ptcridophytcs and angiospcrms, l'lant chcl les Ar.tccac - l . tribu des Spathiphylleac. J, Syst. Evol. 198:55-88. Paly nol. 23-2~ : 5 1-57. PETTITT, J.M. (1980). Rcprocluction in scagrasscs: MAI-I ESWA RI , P. & VASI L. V. (1961). Gnetum . naturc of thc polleo and rcccptivc surfacc of Council of Scicnt ilic and Industrial Re carch. thc stigma in thc Hydrocharitaccac. Aun. llot. Ncw Dclhi. 4):l) /-lll .

MARTINSSON, K. (1993). The polleo of Swcdish PETTITT. J.M.: MCCONCIII E. C.A.: DUCKER. Cnllitriclll! (Callitrichaccac) · trcnds towards S.C. & KNOX. R.l3 . (198-1). Rcproclucti on in submcrge. Grana 32:198-209. scagrasses: pollcn wall morphogcncsis in Amphiboli.l' anwrr1ira and wall structurc in filiform grains. No rcl. J, Bol. -1 :199-216.

18 Polen

• Pri11cipal pollelljeamres in rhe A mm Lilies (Araceae)

POCOC K, S.A.J. & VASANTHY. G. ( 1988). TAKA II AS HI, M.: TAKA I. K. & SA IK I. K. (1995). Co mt•tipollis relirulata. ~ ncw pollcn with Ephcdroicl fossil pollcn from thc Lowcr ~ngiospcrmid fcaturcs from Uppcr Triassic Crctaccous (Upper Albian) of Hokkaido. (Carnian) scdimcnts of Arizon~ (U.S.A.), with Japan. J. J> lant Res. 108:11-15. notes on Equilt'/ol'poriles. Rcv. l'alacobol. Palynol. 55:337-356. TAKI ITAJAN. A. (1997). Oh•crsily :md Classili­ cation of Flowcring Pla nts. Columbia I'UNT, \V.; BLACKMORE, S.; NILSSON, S. & LE Univcrsi ty l'ress. Ncw York. THOMAS. A. (1994). Glossary of Pollcn :111 d Sporc Tcrm inology. Un ivcrsity of TARASEV ICII, V.F. (1990). Palynological cvidcncc Utrccht, Utrccht. of thc r osition of thc Lcmnaccac farnily in thc systcrn of nowcring pla nts. llol. Zilur n. RAJ. B. & SAXENA, M.R. ( 1966). l'ollcn morpho­ 75:959-965. logy of aquatic Angiospcrms. l'ollcn Sporcs 8:49-55. TII AN IKAIMONI, G. (1969). Esquissc palynologiquc des i\racécs. lnst. Fr. Pondicilcry, Tr:m Scc. REILLE. M. (1992). I'ollcn el sporcs d'Europc Sci. Tcch. 5: 1-31. el d •Afri< ¡uc du Nord. Laboratoirc de botaniquc historiquc el palynologic, Marsei Iic. TIIANIKA IMON I. G. ( 1978). Pollcn morpholo­ gical tcrms: proposcd dcfinitions. J. REILLE, M. (1998). r ollen el sporcs d'Euro¡Jc el Procccdings of thc IV lntcrnationa l Palynolo­ d 'Afriquc du Nord. Snpplcmcnlll. l...1boratoi­ gical Confcrcncc Lucknow 1, pp. 228-239. n: d~ botaniquc histOtiquc ct palynologic. Marscillc. TII ANIKAIMONI, G. ( 1984). Omniapcrturatc REITSMA. T. (1969). Size modific~tion of rcccm Euphorbiaccac pollcn wi th striatc spincs. pollen gr~i n s undc r diffcrent trcatrnents. Rcv. Hui!. J ard. Bot. llclg. 54 : 105- 125. Palacobol. l'alynol. 9: 175-202. THAN IKA IMONI, G.; CAHATIN I. C.; VEN KATA­ IWWLEY, J.R. & I'RIJANTO, 13. (1977). Sclcctivc CII ALA, B.S.; RAMANJ UJAM. C.G.K. & KAH, destructi on or the exinc or pollcn gra in s. R.K. ( 1984). Sclectcd Tcrti ary ;\ngiospcrrn Gcophylology 7:1-23. pollens from India and tht:ir rclation hiop with African Tcni ary pollcns. lnst. Fr. l'ondichcry, ROWLEY. J.R.: ROWLEY, J.S. & SKVARLA, J.J. Trav. Scc. Sci. Tcch. 19: 1- 92. (1990). Corrodcd exines from H ~v in ga's lcaf mold experirncnt. Palynol. 14:53-79. TRAVERSE. A. (1988). P:1 lacopalynology. Unwin llyman . Bosto n. ROWLEY, J.R.; SKVARLA. J.J . & CHISSOE, W.F. ( 1997). Exine, onciforrn zonc ~nd intine TREVISAN. L. ( 1980). Ultrastructural notes and structurc in Rm•ennla ~nd l'lll'lwko.rpt•rmum and considcrations on Eplwrlripile.l', Et u·m~rm iiditl'.l" e~rly wa ll development in Strelit:in ~nd and Moll o.,·ull'ite.l' poll cn grains from Lowcr Pllenakospermum (Str e lit z i~ ce~c) b~sed on Crctaccous scdimcnts of sout hcrn Tuscany abortcd rnicrosporcs. Rcv. 1':1lacobot. Palynol. (llaly). Pollcn Sporcs 22:85- 132. 98:293-30 l. VAN DER IIAM , R.W.J.M.; IIETTERSCI·IEID. SR IVASTAVA . S.K. & BINDA, P.L. (1991). W.L.i\. & VAN HEUVEN. B.J . ( 1998). Notes Dcpositional history of the c~rly coccnc on thc gcnus Amurphoplwllux (Araccac). Shumaysi formation, Saudi Arabia. l'alynol. S. Pollcn morphology of Amorphoplwllu.,· and 15:47-61. Pseudodrm·muiw11. n cv. l'alcobot. Pa lynol. 103:95-142. STEWART, \V.N . & ROTI IWELL, G.W. {1993). l'alacobolany nnd thc Evolul ion of l'lants VAN DER HAMMEN, T. & GAHC IA DE MUTIS. (2'' cdi tion). Cambridge University l'rcss. G. ( 1966). Thc l'a lacoccnc po li en flora of Cambridge. Colombia. Lcidsc C eo l. 1\lcd. 35: 105-1 1ó .

Vol. 11 (2000) 19 Hesse, M.

VAN DER MEI{\VE. J .J.M.: VAN WYK, A.E. & ultrastructurc. Aun. 1\lissouri Bot. Gard. KOK, P.D.f'. ( 1990). Pollcn typcs in thc 71:444-463. Lauraccac. Grana 29: 185-196. ZAVADA, M. (1990). Thc ultrastructurc of thrcc WEBER, M.: 11 ALI3RITIER, H. & HESSE. M. monosulcatc polleo grains from thc Triassic ( 1998). Thc spiny pollcn wall in Snummatum Chinlc formation. wcstcrn Uoitcd Statcs. (Araccac) - with ~pccial rcfcrcncc to thc cndcxinc. Palynol. 1-1:41-51. Jnt. J, l'lant Sci. 159:744-749. ZETTER. R.: HESSE, M. & FROSCH-RADIYO. WEBER . M.: IIALUR ITIER, H. & II ESSE. M. A. (2001). Early Eoccnc zona-apcrturatc ( 1999). Thc basic poli en wall typcs in Aracc;~c. pollcn grains of thc Pm.mpertites - typc with Int. J . I'lnnt Sc i. 160:415-423. affinity 10 Araccac. Rcv. Palacobot. Palynol. (in prcss). ZAVADA. M. (198-1). Angiospcrm origins and cvolution ba~cd on dispcrscd fossil polleo

20 Pole11