Pollen Ultrastructure of the Biovulate Euphorbiaceae Author(s): Michael G. Simpson and Geoffrey A. Levin Reviewed work(s): Source: International Journal of Sciences, Vol. 155, No. 3 (May, 1994), pp. 313-341 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/2475184 . Accessed: 26/07/2012 14:35

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http://www.jstor.org Int.J. Plant Sci. 155(3):313-341.1994. ? 1994by The Universityof Chicago. All rightsreserved. 1058-5893/94/5503-0008$02.00

POLLENULTRASTRUCTURE OF THE BIOVULATE EUPHORBIACEAE

MICHAEL G. SIMPSON AND GEOFFREY A. LEVIN' Departmentof Biology,San Diego StateUniversity, San Diego,California 92182-0057; and BotanyDepartment, San Diego NaturalHistory Museum, P.O. Box 1390,San Diego,California 92112

Pollenultrastructure of the biovulate Euphorbiaceae, including the subfamilies Phyllanthoideae and Oldfieldioideae,was investigatedwith light, scanning electron, and transmissionelectron microscopy. Pollenof Phyllanthoideae, represented by 12 speciesin ninegenera, was prolateto oblate,almost always 3-colporate,rarely 3-porate or pantoporate,and mostlywith reticulate, rarely baculate, echinate, or scabrate,sculpturing. The ektexineshowed little variation in ultrastructure;almost without exception it was tectate-columellatewith a homogeneousfoot layer, columellae continuous with both the tectum and thefoot layer, and a perforate,homogeneous tectum. The onlymajor exception was guianensis, whichwas intectateand baculateas theresult of the evolutionary loss of thetectum. Pollen of Oldfiel- dioideae,in whichwe studied28 speciesfrom 25 genera,and obtaineddata fromthe literature for two of thethree remaining genera in the subfamily,was globoseto oblate,with four or more,rarely only three,apertures that were either equatorial and brevicolporate toporate or pantoporate, and with echinate, rarelyscabrate, sculpturing. The ektexineshowed considerable variation in ultrastructure.The most widespreadstructural type consisted of a footlayer that is eitherthin and irregular or absent, an interstitium composedof irregular to columellateexine deposits that are discontinuous from the foot layer, if present, and a tectumcomposed of laterallyappressed baculate elements that delimit fine microperforations. A secondcommon structural type differed in havinga relativelythick, homogeneous foot layer and thin, granularto tabular,microperforate tectum. Isolated genera have a reducedinterstitium and/or a homo- geneoustectum or show a reversalto a tectate-columellatearchitecture. Variation in aperture morphology, sculpturing,and exineultrastructure is phylogenetically significant in theOldfieldioideae.

Introduction remainingthree subfamilies share the synapo- Palynologicalstudies of the Euphorbiaceae have morphy(shared derived character state) of a sin- beenextremely useful in clarifyingsystematic re- gleovule per locule. The Acalyphoideae (113 gen- lationshipswithin the family.Using lightmi- era, 2,100 ) is probablyparaphyletic, croscopy(LM), Erdtman(1952) was the firstto differingfrom the otheruniovulate subfamilies pointout the great variation in theshape, sculp- mainlyin lackingmilky or coloredlatex. The turing,and apertures of Euphorbiaceae pollen and Crotonoideae(64 genera,1,450 species) share the to suggestthat these characteristics were signifi- synapomorphiesof stellate, dendritic, or lepidote cant systematically.Punt (1962) subsequently trichomes,and mostlyporate or inaperturate pol- conducteda more detailedsurvey, confirming len withthe distinctive"crotonoid" pattern of most of Erdtman'sconclusions. K6hler (1965) exinousprocesses (Nowicke 1994). The Euphor- completeda thoroughstudy of the biovulate gen- bioideae(38 genera,1,800 species) are unitedby era,i.e., those that produce two ovules per locule, thesynapomorphy of a reducedperianth. whichhad long been placed in the subfamily Our understandingof relationships within the Phyllanthoideae.He concludedthat the genera Phyllanthoideaeand Oldfieldioideaehas been withspinose pollen shouldbe placed in a new greatlyincreased by pollen studiesusing SEM subfamily,the Oldfieldioideae. (Bonnefilleand Riollet 1980; Punt 1980, 1987; Subsequentintrafamilial classifications of the Poole 1981; Haydenet al. 1984;Webster 1984a; Euphorbiaceaehave continued to recognizethese Dechampset al. 1985; El-Ghazalyand Raj 1986; two subfamiliesas well as the Acalyphoideae, Lobreau-Callenin McPhersonand Tirel 1987; Crotonoideae,and Euphorbioideae(Webster Websteret al. 1987;Lobreau-Callen and Suarez- 1967,1975, 1994).The Phyllanthoideae(55 gen- Cervera1989). However,only three palynologi- era,2,100 species)is probablya basal, paraphy- cal studies of these subfamilies(Poole 1981; letictaxon, the members of which are united only Haydenet al. 1984; Lobreau-Callenand Suarez- bysharing a numberof ancestral (plesiomorphic) Cervera1989) have used TEM to describethe features.The Oldfieldioideae(28 genera,80 spe- detailsof exinearchitecture, and thoughthe au- cies) appearsto be monophyletic,united by the thorstreated only six genera,they suggested that spinosepollen observed by Kohler(1965). The pollenwall ultrastructuremay be systematically valuable. We investigatedpollen ultrastructurein the ' Authorfor correspondence and reprints. Current address: biovulateEuphorbiaceae with the goal of ex- Centerfor Biodiversity, Illinois Natural History Survey, 607 ploringits contribution to thesystematics of these East PeabodyDrive, Champaign, Illinois 61820. subfamilies.We initiallyfound little variation in Manuscriptreceived September 1993; revisedmanuscript re- exinewall structurewithin the Phyllanthoideae, ceivedJanuary 1994. whereaspollen of Oldfieldioideae varied consid-

313 314 INTERNATIONAL JOURNAL OF PLANT SCIENCES erably.As a consequencewe concentratedour ips EM 410 transmissionelectron microscope at effortson thelatter subfamily, examining a small 80 kV. sampleof Phyllanthoideaeselected to included Mean pollengrain diameter (polar x equato- membersof the major groups recognizedin rial)was determined from LM preparations,mean Webster'sclassification (1975, 1994).We also ex- spinelength from either LM observationsor TEM aminedDidymocistus and ,both micrographs,and mean ektexinefoot layer and Phyllanthoideae,because of questions about their tectumthicknesses from TEM micrographs. relationships. Samplesizes fromLM observationsincluded at This articleis primarilydescriptive. In a sep- least 10 pollengrains, whereas those from TEM aratearticle (Levin and Simpson1994a), we an- micrographswere generally very small. alyzethe pollen characters of the subfamily Old- Our terminologygenerally follows that of fieldioideaephylogenetically, both alone and in Reitsma(1970) and Walkerand Doyle (1975). combinationwith anatomical and morphological Reitsma(1970) distinguishedspines of length > 1 characters.Only the major conclusionsof our ,um,which he termed"echinae" (sculpturing phylogeneticanalysis will be repeatedhere. "echinate"),from those of length < 1 ,um,which he termed"scabrae" (sculpturing "scabrate"). To reflectthe discontinuities among the taxa in our Materialand methods study,we modifiedReitsma's terms and use the Flowersfrom dried herbarium specimens were terms"echinae" or "echinate"when spines are rehydratedeither at roomtemperature or at 600C >0.9 ,umin lengthand "scabrae" or "scabrate" in 1%Aerosol OT for3-5 d,then fixed and stored when <0.5 ,umin length.With regard to tectal in FAA. For LM, pollenwas clearedin Hoyer's structure,we use the term"microperforate" to mountingmedium (Radford et al. 1974) on a describea tectumpenetrated by very narrow pores microscopeslide preparation.LM observations delimitedby closelyappressed tectal elements, weremade with differential interference contrast whereas"homogeneous" refers to theabsence of opticsusing a Nikon Microphot-FXphotomi- microperforationsor any otherwall discontinu- croscope.For SEM, whole antherswere dehy- ities.A microperforatetectum may be composed dratedto 100%ethanol, then gradually infiltrated eitherof laterally appressed baculate elements, a to 100% Freon 113 or methylal(dimethoxyme- structurethat we term "microperforate/bacu- thane).The antherswere placed in a metalcap- late,"or oflaterally appressed granular to tabular suleand critical-pointdried with a Tousimiscrit- elements,a structurethat we term"microperfor- ical-pointdryer using pressurized carbon dioxide ate/granular.""Perforate" refers to a largerhole as thetransition fluid. Pollen grains were tapped in thetectum that is not immediatelybordered ontoa stubcovered with double stick tape, sput- by closelyappressed tectal elements; the tectum ter-coatedwith gold/palladium in a Hummer-4 betweenperforations may be eithermicroperfor- sputteringapparatus, and photographedon a Hi- ateor homogeneous. "Imperforate" simply means tachiS500 scanningelectron microscope (20 kV). thatthe tectum lacks both perforations and mi- In additionto our own preparations, we also stud- croperforations.With regard to footlayer struc- iedSEM micrographsloaned to us byG. Webster. ture,"homogeneous" refers to a continuouswall For TEM, whole anthers,isolated pollen, or whereas"irregular" refers to an interrupted,dis- pollenembedded in 2% agarwas fixedin cold 4% continuouswall. With regard to footlayer thick- gluteraldehydein 0.1 M Sorensen'sphosphate ness,we use theterms "thin" and "thick"to re- bufferfor 2 h, followedby several rinses in buffer flecta major discontinuityamong investigated and furtherfixation in 2% osmiumtetroxide for taxa as determinedby a quantitativeanalysis 2 h. Specimenswere quickly rinsed twice in buff- (Levinand Simpson1 994a); forour purposes, we er,progressively dehydrated to 100%ethanol, in- define"thin" as <0.5 ,umand "thick"as >0.5 filtratedina gradationseries of Spurr's resin (Spurr ,um.Because tectum thickness varied almost con- 1969), and finallypolymerized at 650C for 12- tinuously,we did notrecognize any distinct size 18 h. Sections0.5 ,umthick were stained with 1% classesin thisfeature (Levin and Simpson 1 994a). toluidineblue and mountedon a slide forLM observations.Ultrathin-sections (ca. 95 nmthick) Resultsand comparisons with previous work wereprepared with a Diatomediamond knife on In the resultsthat follow, descriptions of ek- a ReichertUltracut-E ultramicrotome, mounted texineand endexinecorrespond to the nonape- on uncoatedhexagonal 200 meshcopper grids, ruralregion except where noted. Voucher collec- and poststainedwith a saturated50% ethanolso- tiondata and herbariumacronym (after Holm- lutionof uranylacetate for 15 min and 0.2% grenet al. 1990)are in parenthesesfollowing each aqueous lead citratefor 7 min.To inhibitstain investigatedspecies name. precipitation,grids were gentlyand quickly washedin a runningstream of filtered,distilled SUBFAMILYPHYLLANTHOIDEAE ASCHERSON waterbetween and afterpoststain changes. Ob- In thissubfamily the sequence ofgenera follows servationsand photographswere made on a Phil- Webster(1994). SIMPSON & LEVIN-EUPHORBIACEAE POLLEN 315

TRIBE AMANOEAE (PAX AND K. HOFFM.) nitida (Pax) Webster (Zimbabwe, Chase 5150, WEBSTER (2 GENERA, 17 SPECIES). MO). Pollen prolate (27 x 22 ,um),3-colporate (fig.8), with lalongate endoaperture;sculpturing AMANOA AUBLET (16 SPECIES). reticulate;ektexine tectate-columellate with a thin Amanoa guianensisAublet (Guyana, Tillettet (0.17 ,um),homogeneous footlayer and a widely al. 45256, DAV). Pollen oblate (36 x 42 ,Am), perforate,homogeneous tectum (0.43 ,um; figs.8, 3-colporate; sculpturingbaculate (4.1 ,Amlong), 9); endexine thinand irregular(fig. 9), thickened verrucate(fig. 1); ektexine apparentlyintectate, at apertural border (fig. 8); intine of apertural with a thick (1.0 ,um),homogeneous foot layer region thickened(fig. 8) Other species of Mar- and elongatedistally rounded baculae (fig.2), these garitariahave generallysimilar pollen (Punt 1962; apparentlyhomologous to columellae (Discus- K6hler 1965). sion); endexine relativelythin (fig.2), thickened at aperturalborder (fig. 3); intine two-to-three- TRIBE DRYPETEAE (GRISEB.) HURUSAWA(4 layered,very thick in aperturalregion (fig.3). GENERA,230 SPECIES). Descriptions and illustrationsof pollen of A. guianensis(Punt 1962, 1987; Websteret al. 1987) DRYPETESVAHL (220 SPECIES). agree with our observations except that Punt Drypetes lateriflora(Sw.) Krug and Urban. (1962) reportedthe grainsto be 39-46 x 45-52 (United States, Chambers and Stem 266, US). jAmand the baculae to be up to 7 jAmlong. The Pollen prolate (30 x 20 ,um),3-colporate with a specimen with reticulatesculpturing that Erdt- short lalongate endoaperture;sculpturing retic- man (1952) cited is properlyassigned to Amanoa ulate; ektexine tectate-columellate,with a thin sinuosa W. J. Hayden (Hayden 1990). (0.18 ,um),homogeneous foot layer and a perfo- Amanoa strobilacea Muell. Arg. (Cameroon, rate,homogeneous tectum(0.37 ,um; fig.10); en- Thomas 4125, MO). Pollen oblate (38 x 54,um), dexine thin(fig. 10), thickenedat aperturalborder 3-colporate; sculpturingcoarsely reticulate,ver- (fig.11); intinethick, two-layered throughout (figs. rucatebetween muri (fig.4); ektexinetectate-col- 10, 11). Pollen of this species has not been de- umellatewith a thick(1.4,um) footlayer, narrow scribedpreviously. The fewother species of Dry- columellae,and a widelyperforate, homogeneous petes examined palynologicallyhave generally tectum(2.7 Am;fig. 5); ektexineextending across similar pollen (Punt 1962; Kohler 1965). apertureas irregularto granulardeposits (fig.6); endexine scanty (fig. 5), thickened at apertural TRIBE (SWEET) HURUSAWA(18 border(fig. 6). Except forlarger diameters (50 x GENERA,500 SPECIES;2 OF 5 SUBTRIBESINVESTI- 58 Am),K6hler's (1965) descriptionand illustra- GATED). tion of this species agree with our observations. SUBTRIBE SCEPINAE(LINDLEY) WEBSTER (8 TRIBE DUMORT. (19 GENERA, GENERA,180 SPECIES). 1,125 SPECIES; 2 OF 6 SUBTRIBES INVESTIGATED). APORUSABLUME (80 SPECIES). SUBTRIBE SECURINEGINAE MUELL. ARG. (1 AporusafalciferaHook. f. (Indonesia, Soepad- , 5 SPECIES). mo 41, MO). Pollen subprolate (16 x 15 ium), 3-colporatewith a lalongateendoaperture; sculp- COMM. EX JUSS. (5 SPECIES). turing reticulate; ektexine tectate-columellate, Securinega durissima J. Gmelin (Mauritius, with a thin (0.17 ,um),homogeneous foot layer Lorence 1397, MO). Pollen oblate (22 x 25,um), and a perforatehomogeneous tectum(0.29 ,m), 3-colporate,apertures widely elliptic; sculpturing the latterwith distal angularprojections that give echinate (1.0 ,Amlong); ektexine tectate-colu- the tectuma decidedlypitted appearance (fig.12 mellate,with a thin(0.28,4m), homogeneousfoot [Punt 1987]); endexinemoderately thick (fig. 12), layerand a perforatehomogeneous tectum(0.32 greatlythickened at aperturalborder (fig. 13); in- ,Am;fig. 7); endexinethin and scanty(fig. 7), thick- tine of aperturalregion two-layered (fig. 13). Pol- ened at aperturalborder. Pollen of this species len of this species was illustratedby Punt (1987); was illustratedby Webster(1 984a). Otherspecies otherspecies have verysimilar pollen (Punt 1962; in this genus described or illustrated(Erdtman Kohler 1965). 1952; Punt 1962; Kohler 1965) are now placed in Chascotheca,Flueggea, and (Web- SUBTRIBEANTIDESMINAE (SWEET) MUELL. ARG. ster 1984a, 1984b). (6 GENERA,240 SPECIES).

SUBTRIBE FLUEGGEINAE MUELL. ARG. (9 ANTIDESMAL. (200 SPECIES). GENERA, 1,050 SPECIES). Antidesmamembranaceum Muell. Arg.(Guin- ea, Adam 4973, MO). Pollen prolate (23 x 12 MARGARITARIA L. F. (14 SPECIES). ,um),3-colporate with a lalongate endoaperture; Margaritariadiscoidea (Baillon) Webster ssp. sculpturingreticulate; ektexine tectate-columel- - 1 w [,

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Figs.1-6 Pollenof Euphorbiaceaesubfamily Phyllanthoideae. Figs. 1-3, Amanoaguianensis. Fig. 1, Wholepollen grain, SEM, colporateaperture facing; note baculae and verrucae.Fig. 2, Nonaperturalwall, TEM; arrowindicates endexine. Fig. 3, Aperturalregion, TEM; arrowindicates endexine. Figs. 4-6, Amanoa strobilacea. Fig. 4, Wholepollen grain, SEM; notereticulate tectumand verrucae.Fig. 5, Nonaperturalwall, TEM; arrowindicates endexine. Fig. 6, Aperturalregion, TEM; notethickened endexine(en) at aperturalborder and outerektexinous deposits. Scale bars= 1 jAm in fig.2; 2 MAmin figs.3, 5, 6; 5 Mmin figs. SIMPSON & LEVIN-EUPHORBIACEAE POLLEN 317 late,with a thin(0.11 ,um),homogeneous foot (to brevicolporate),apertures slightly elliptic, per- layerand a perforatehomogeneous tectum (0.30 pendicularto equator, witha raised rim (fig.23); ,im; fig.14); endexinemoderately thick (fig. 14), sculpturingscabrate (0.07 Am long), interspinal thickenedat apertureborder (fig. 15); intineof sculpturingrugulate (figs. 23); ektexine tectate- aperturalregion very thick, two-layered (fig. 15). columellate,with a thin(0.18 um),homogeneous Antidesmavenosum Tul. (Swaziland,Kemp foot layer and a perforatehomogeneous tectum 525, MO). Pollen prolate (20 x 12 ,um), (0.26 ,m; fig.24); footlayer thickened at aperture 3-colporate(fig. 16) witha lalongateendoaper- border,this presumably accounting for the raised ture;sculpturing reticulate; ektexine tectate-col- aperturalrim; endexine very thin to absent (fig. umellate,with a thin(0.15 ,um),homogeneous 24), slightlythickened at aperturalborder; intine footlayer and a perforatehomogeneous tectum of aperturalregion thick, two-layered. (0.31 ,im; fig.16); endexinemoderately thick, Hymenocardiaulmoides Oliver (Zaire, Lebrun thickenedin aperturalregion (fig. 16). 2119, MO). Pollen oblate (19 x 21 ,m), 3-porate; Punt's (1962) descriptionof these species is sculpturingscabrate (0.07 Am long), interspinal entirelyconsistent with ours. Pollen of other spe- sculpturingrugulate; ektexine tectate-columel- cies is verysimilar (Erdtman 1952; Punt 1962; late, with a thin (0.16 gim),homogeneous foot Kbhler1965). layerand a perforatehomogeneous tectum(0.19 gim; fig. 25); ektexine at aperture border with HYERONIMAALLEMAO (15 SPECIES). thickenedfoot layer (fig.26); endexine verythin Hyeronimaalchorneoides Allemao var. al- (fig. 25); intine of apertural region thick, two- chorneoides(Bolivia, Croat 51307, MO). Pollen layered (fig.26). prolate(33 x 19,m), 3-colporatewith lalongate Pollen of these and other species of Hymeno- endoaperture(fig. 17); sculpturingfoveolate (fig. cardia have been describedand illustratedby Punt 17);ektexine tectate-columellate, with a thin(0.21 (1962), Kbhler (1965), and especially Dechamps gim),homogeneous foot layer and a perforateho- et al. (1985). Our observationsare consistentwith mogeneoustectum (0.40 gim;fig. 18); endexine these others,though Dechamps et al. (1985) re- moderatelythick (fig. 18), thickened at apertural ported that the scabrae may be up to 0.25 ,um border(fig. 19); intineof aperturalregion thick, long. 2-3-layered(fig. 19). In additionto thecursory references to pollen SUBFAMILY OLDFIELDIOIDEAE KOHLER AND ofthis species by Punt (1962, 1987)and Webster WEBSTER (1984a), FrancoR. (1990) provideddetailed de- In this subfamilywe list the generain orderof scriptionsand illustrations.Our observationsare the cladogram shown in fig. 75, the preferred in fullagreement with hers, though our small cladogram of Levin and Simpson (1994a), and samplesize includedno grainswith horns at the followtheir classification. endsof the endoaperture, which she described as sometimespresent. TRIBE CROIZATEAE WEBSTER (1 GENUS, 4 SPE- CIES). TRIBE HYMENOCARDIEAE (MUELL. ARG.) CROIZATIA STEYERM. (4 SPECIES). HUTCH. (2 GENERA,9 SPECIES). Croizatia naiguatensisSteyerm. (Venezuela, Berryet al. 4124, DAV). Pollen globose (32 gim), DIDYMOCISTUSKUHLM. (1 SPECIES). 3-brevicolporate;sculpturing echinate (3.3 Am Didymocistuschrysadenius Kuhlm. (Peru, long); ektexinewith a thick (0.63 ,um),homoge- Dodson and Torres 2961, MO). Pollen globose neous foot layer, irregularcolumellae that gen- (12 um),3-colporate, apertures narrow and elon- erally appear discontinuouswith the foot layer, gate (fig. 20) with a lalongateendoaperture; and a microperforate/granulartectum (0.24 um; sculpturingscabrate (0.08 Am long), interspinal figs.27, 28); aperturalregion with foot layer con- sculpturingrugulate (fig. 20); ektexinetectate-col- siderablythickened and interstitiumand tectum umellate,with a thin(0.12 gim),homogeneous reduced (fig.27); endexine scanty,irregular (fig. foot layer and a perforatehomogeneous tectum 28); intine of apertural region thickened,two- (0.20 ,m; fig.21); footlayer slightly thickened at layered (fig.27). Webster et al. (1987) described apertureborder (fig. 22); endexinethin (fig. 21), and illustratedpollen ofthis species. Our descrip- thickenedat aperturalborder (fig. 22); intineof tion is consistentwith theirs,except that they aperturalregion thick, two-to-three-layered (fig. reportedthe diameter of the grainsto be 46-56 22). Pollenof this monotypic genus has notbeen gim. describedpreviously. TRIBE PODOCALYCEAE WEBSTER (2 GENERA, 3 HYMENOCARDIAWALLICH EX LINDLEY (8 SPE- SPECIES; 2 OF 2 SUBTRIBES INVESTIGATED). CIES). Hymenocardiaacida Tul. (Cameroon,de Wilde SUBTRIBE PARADRYPETINAE G. LEVIN (1 GENUS, 4044,MO). Pollenoblate (25 x 28,uin),3-porate 2 SPECIES). 10

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Figs.7-13 Pollenof Euphorbiaceae subfamily Phyllanthoideae. Fig. 7, Securinegadurissima. Nonapertural wall, TEM; arrow indicatesendexine. Figs. 8, 9, Margaritariadiscoidea. Fig. 8, Wholegrain cross-section, TEM; note threeapertures, with thickenedendexine (arrows) at twoapertural borders. Fig. 9, Nonaperturalwall, TEM; arrowindicates endexine. Figs. 10, 1, Drypeteslateriflora. Fig. 10, Nonaperturalwall, TEM; arrowindicates endexine. Fig. 11, Apertural region, TEM; notethickened endexinelayer (arrow). Figs. 12, 13,Aporusa fakcifera. Fig. 12, Nonaperturalwall, TEM; arrowindicates endexine. Fig. 13, Aperturalregion, TEM; notegreatly thickened endexine layer (arrow). Scale bars = 0.5 Amin figs.7, 9, 10, 12; 1 Amin fig. 13;Im in fs. 8.. I .. SIMPSON & LEVIN-EUPHORBIACEAE POLLEN 319

14 17

15

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Figs.14-19 Pollenof Euphorbiaceaesubfamily Phyllanthoideae. Figs. 14, 15, membranaceum. Fig. 14, Nona- perturalwall, TEM; arrowindicates endexine. Fig. 15, Aperturalregion, TEM; notethickened endexine (arrow) at apertural border.Fig. 16,Antidesma venosum. Whole grain cross-section, TEM; notethree apertures with thickened endexine (arrow). Figs.17-19, Hyeronima alchorneoides. Fig. 17,Whole pollen grain, SEM, colporateaperture facing. Fig. 18,Nonapertural wall, TEM; arrowindicates endexine. Fig. 19, Aperturalregion, TEM; notethickened endexine (arrow) at aperturalborder. Scale bars= 0.5 Aimin figs.14, 15, 18; 1 Mm.infigs. 16, 19; 5 ,um.infig. 17.

PARADRYPETES KUHLM. (2 SPECIES). spinalregion (fig. 29); ektexinewith commissure Paradrypetessubintegrifolia G. Levin (Brazil, delimitingthe thin (0.12 ,Am),irregular foot layer Krukoff4999, U [isotype]).Pollen oblate (22 x fromthe imperforatetectum (0.35 ,um;fig. 29); 27 ,um),4-brevicolporate, zoni-aperturate; colpi interstitiumabsent (Discussion); endexine thick- linear(length ca. I/3-1/2grain polar diameter), with ened at aperturalborder; intine of aperturalre- narrowlyelliptic lalongate endoaperture; sculp- gion thick,two-layered. More detailedillustra- turingechinate (1.4 ,umlong), psilate in inter- tionsof this species can be foundin Levin(1992). 4.~~~~

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25;1 ,m nfg. 4,26;2 m i fis.20,23

Figs. 20-26 Pollen of Euphorbiaceae subfamily Phyllanthoideae. Figs. 20-22, Didymocistuschrysadenius. Fig. 20, Whole grain, SEM, obliquely polar view; note three apertures. Fig. 2 1, Nonapertural wall, TEM; arrow indicates thin endexine. Fig. 22, Apertural region, TEM; note thickened endexine (arrow) at apertural border. Figs. 23, 24, Hymenocardiaacida. Fig. 23, Whole grain,SEM; note two of threeporate to brevicolporateapertures. Fig. 24, Nonaperturalwall, TEM; arrowindicates very thin endexine. Figs. 25, 26, Hymenocardia ulmoides. Fig. 25, Nonaperturalwall, TEM; arrow indicates very thin endexine. Fig. 26, Aperturalregion, TEM; note thickenedektexinous foot laver at aperturalborder. Scale bars = 0.5 ,umin figs.21, 22, SIMPSON & LEVIN-EUPHORBIACEAE POLLEN 321

SUBTRIBE PODOCALYCINAE WEBSTER (1 GENUS, ularlyspaced columellae, and a highlymicroper- 1 SPECIES). forate/baculatetectum (1.1 iAm;fig. 40); endexine composedof a thinbasal layer (fig. 40), thickened KLOTZSCH (1 SPECIES). at aperturalborder (fig. 39); intineof apertural Podocalyxloranthoides Klotzsch (Brazil, Vi- region conspicuouslythickened, two-to-three- ciraet al. 195,MO). Pollenoblate (22 x 25,gm), layered(fig. 39). DetailedLM observationsand 4-porate,zoni-aperturate; sculpturing echinate illustrationsof the pollen of this species published (2.8 Amlong; fig. 30); ektexinewith a thin(0.11 by Villamil (1969) generallyagree with ours, A,m),irregular, somewhat granular foot layer and thoughhe reportedthe grains to be larger(33.5 a microperforate/baculatetectum (0.33 ,um;fig. x 36.5 Am)with correspondingly longer spines 30), theinterstitium apparently lacking (Discus- (4-5[-7] im). sion); endexinethick (fig. 30), thickenedfurther at aperturalborder (fig. 31). PIRANHEABAILLON (2 SPECIES). The descriptionby K6hler ([1965], as Piranheatrifoliata Baillon (Brazil,Berg et al. loranthoides[Klotzsch] Muell. Arg.) and illustra- P19789, MO). Pollen oblate (32 x 35 gAm), tionby Websteret al. (1987) are consistentwith 6-porate,zoni-aperturate; sculpturing echinate our observations.Although we have described (2.7,4mlong; fig. 41); ektexinewith no footlayer, the tectumas microperforate/baculate,the tec- irregularlyspaced columellae,and a microper- tumis muchless segmentedthan in mostOld- forate/baculatetectum (0.39,gm; fig. 41); endex- fieldioideaewith this type of tectum (Discussion). ine thin;intine two-layered (fig. 41). Both Punt (1962) and Kohler(1965) describedpollen of this TRIBE PICRODENDREAE (SMALL) WEBSTER (11 speciesto be somewhatsmaller (23-27 x 25-32 GENERA, 24 SPECIES; 4 OF 4 SUBTRIBES INVESTI- gAm)with shorter spines; otherwise their descrip- GATED). tionsagree with ours. Pollen of Piranhealongi- peduculataJabl. appears similar (Hayden et al. SUBTRIBE TETRACOCCINAE G. LEVIN (1 GENUS, 1984). 4 SPECIES). CELAENODENDRONSTANDLEY (1 SPECIES). TETRACOCCUSENGELM. EX PARRY (4 SPECIES). Celaenodendronmexicanum Standley (Mexi- Tetracoccusdioicus Parry (United States, Hen- co,Perez and Chang 1776, MO). Pollensuboblate ry and Dice s.n. [April 8, 1980], SD). Pollen (39 x 40 gim),7 (8)-porate,zoni-aperturate; suboblate(46 x 47 ,im);4-porate, zoni-apertur- sculpturingechinate (2.9,um long; fig. 42); ektex- ate;sculpturing echinate (4.7,4m long), verrucate ine withno footlayer, an irregularinterstitium, in interspinalregion (fig. 32); ektexinewith a thin and a microperforate/baculatetectum (0.59,im; (0.35,gm),irregular, granular foot layer, narrow, fig.42); endexinethin (fig. 42), thickenedat ap- irregularcolumellae that are generallydiscontin- erturalborder (fig. 43); intinemoderately thick, uous withthe footlayer, and a microperforate/two-layered, thickened in aperturalregion (fig. baculatetectum (0.63,gm; fig. 32); endexinethin 43). Pollenof this monotypic genus has notbeen (fig.32). describedpreviously. Publisheddescriptions and illustrationsof pol- len of thisspecies (Kohler 1965; Haydenet al. SUBTRIBEPAIVEUSINAE PAX AND K. HOFFM. 1984; Websteret al. 1987) generallyagree with our observations.Kohler (1965), however,re- OLDFIELDIABENTH. AND HOOK. F. (4 SPECIES). portedthat the grains-were smaller(33 x 36 gAm) Oldfieldiaafricana Benth. and Hook. f.(Sierra and had (5-)6(-7) apertures.Pollen of other spe- Leone, Fox 157, K). Pollen suboblate(28 x 30 cies of Tetracoccusis similar,though somewhat A,m),5-6-porate, zoni-aperturate; sculpturing smallerand with shorter spines (Punt 1962, 1987; echinate(3.5 ,umlong; fig. 44); ektexinewith no Kohler1965). footlayer, irregularly spaced columellae, and an irregular,microperforate/baculate tectum (0.44 SUBTRIBE PICRODENDRINAE (SMALL) WEBSTER gAm;fig. 44); ektexineof aperturalregion with (4 GENERA, 5 SPECIES). thickenedbasal layer;endexine relatively thin, forminga continuous basal layer(fig. 44), slightly PARODIODENDRON HuNz. (1 SPECIES). thickenedat apertureborder; intine of apertural Parodiodendronmarginivillosum (Speg.) Hunz. regiontwo-layered, thickened. Previous descrip- (Argentina,Verveerst and Cuezzo 7610, US). tionsand illustrationsof pollen of this species Pollenoblate (24 x 27 ,gm),ca. 7-porate,zoni- (Erdtman1952; Punt 1962; K6hler 1965; Hay- aperturate;sculpturing echinate (3.1 Amlong), den et al. 1984) are consistentwith our obser- verrucatein interspinalregion (figs. 33, 34, 39, vations,though reported diameters vary widely 40); ektexinewith essentially no footlayer, irreg- (24.5-35.4 x 27.5-43 gAm).Kohler (1965) re- ;'.~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.

Figs.27-32 Pollenof Euphorbiaceaesubfamily Oldfieldioideae. Figs. 27, 28, Croizatianaiguatensis. Fig. 27, Wholegrain cross-section,TEM, showing(at upperleft) one of threeapertures; note thickened ektexinous foot layer at aperturalborder. Fig. 28, Nonaperturalwall, TEM; arrowindicates endexine. Fig. 29, Paradrypetessubintegrifolia. Nonapertural wall, TEM, showingcommissure (c) delimitingfoot layer from tectum; arrow indicates endexine. Figs. 30, 31, Podocalyxloranthoides. Fig. 30, Nonaperturalwall, TEM, showingcommissure (c) delimitingfoot layer from tectum; arrow indicates endexine. Fig. 31, Wholegrain cross-section, TEM; notethickened endexine (arrow) at aperturalborder. Fig. 32, Tetracoccusdicicus. Nonapertural wall,TEM; arrowindicates thin endexine. Scale bars= 5 zsmin fig.27; 1 ztmin figs.28, 31, 32; 0.5 Mmin fig.29; 0.2 ,umin fig.30.

322 37~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~4

Figs.33-38 Pollenof Euphorbiaceae subfamily Oldfieldioideae. Figs. 33, 34,Parodiodendron marginivillosum. Fig. 33, Whole grain,SEM. Fig. 34, Wall close-up,SEM. Figs.35, 36, Androstachysjohnsonii. Fig. 35, Wholegrain, SEM. Fig. 36, Close-up ofaperture, SEM. Fig. 37, Micrantheumhexandrum. Whole grain, SEM; noteporate apertures. Fig. 38, Neoroeperabuxifolia. Close-upof wall, SEM; noteporate apertures. Scale bars= 5 ,m in figs.33, 35-37; 2 ,umin figs.34, 38.

323 _44

43 v

Figs.39-44 Pollen of Euphorbiaceae subfamilyOldfieldioideae. Figs. 39, 40, Parodiodendronmarginivillosum. Fig. 39, Whole graincross-section, TEM; note thickenedendexine (arrow) at aperturalborder. Fig. 40, Nonaperturalwall TEM; arrowindicates thinendexine. Fig. 41, trifoliata.Nonapertural wall, TEM; arrowindicates thin endexine. Figs. 42, 43, Celaenodendron mexicanum. Fig. 42, Nonaperturalwall, TEM; arrow indicates thin endexine. Fig. 43, Aperturalregion, TEM; note thickened endexine (arrow). Fig. 44, Oldfieldiaafricans. Nonapertural wall, TEM; arrow indicates thin endexine. Scale bars = 5 gm in fig.39; 1 ,umin figs.40-44. SIMPSON & LEVIN-EUPHORBIACEAE POLLEN 325 portedthe apertures to be up to eightin number. turate;sculpturing echinate (1.4 ,m long;fig. 47); Oldfieldiadactylophylla (Oliver) Leonard has ektexinewith no footlayer, a somewhatirregular similarpollen (Punt 1962; K6hler1965). interstitium,and a microperforate/baculatetec- tum (0.52 ,um);endexine forming a thinbasal SUBTRIBEMISCHODONTINAE MUELL. ARG. (5 layer,thickened at aperturalborder; intine two- GENERA, 11 SPECIES). layered(fig. 47), thickenedin aperturalregion. Stachyandrarufibarbis (Airy Shaw) R.-Sm. ANDROSTACHYS PRAIN (1 SPECIES). (Madagascar, Capuron 9177-SF, P [holotype]). Androstachysjohnsonii Prain (South , Pollen globose(46 ium),5-7-porate, zoni-aper- Balsinhas3549, K). Pollenglobose (50 ,im),5- turate;sculpturing echinate (0.9 ,m long) (figs. 7-pantoporate(figs. 35, 36); sculpturingechinate 48, 49); ektexinewith no footlayer, an irregular (1.1 ,umlong), interspinal sculpturing psilate (figs. interstitium,and a microperforate/baculatetec- 35, 36); ektexinetectate-columellate with a thin tum(0.50 ,um)(fig. 48); endexineforming a thin (varyingin thickness;mean 0.07 ,im),homoge- basal layer(fig. 48), thickenedat aperturalborder neous footlayer, sparse narrow columellae that (fig.49); intinetwo-layered, thickened in aper- are continuouswith the foot layer, and a micro- turalregion (fig. 48, 49). perforatetectum (0.36 ,um;fig. 45); ektexineof Pollenof thisrecent segregate from Androsta- aperturalregion with foot layer and interstitium chys(Radcliffe-Smith 1990) has not been de- reduced(fig. 46); endexinethin and appressed scribedpreviously. Although we describethe tec- innerto thefoot layer; endexine extending as a tum as microperforate/baculatein both species thinlayer across aperture(fig. 46); intinetwo- of Stachyandra,they have fewermicroperfora- layered(figs. 45, 46). The verysparsely micro- tionsthan is characteristicboth of other Mischo- perforatetectum of this speciesdoes not show dontinaeand of manyother Oldfieldioideae. thedistinct baculate or granularto tabularstruc- turefound in mostother microperforate Oldfiel- VOATAMALOCAPURON EX BOSSER(2 SPECIES). dioideae. Voatamalo eugenioidesCapuron ex Bosser Previousreports on thenumber and distribu- (Madagascar,Capuron 22327-SF, K). Pollenglo- tion of aperturesdiffer considerably. Erdtman bose (44 ,m), 5-6-porate,zoni-aperturate; sculp- (1952) describedthe pollen as polyforate,i.e., turingechinate (3.3 ,m long);ektexine with a thin pantoporatewith more than 12 apertures(not (0.14 ,um)and irregularto absentfoot layer, an oligoforate,i.e., with12 or fewerpores, as mis- irregularinterstitium that is generallydiscontin- quotedby Dahlgrenand van Wyk 1988), with uous withthe footlayer, and a microperforate/ thepores faintly defined and coveredwith gran- baculatetectum (0.38 ,m; fig.50); endexinethin; ulate membranes.K6hler (1965), studyingthe intinetwo-layered (fig. 50). Pollenof thisgenus samesample, described the pollen as moreor less has notbeen describedpreviously. pantoporateor possiblydizonoporate, with 14- 18 inconspicuous,variably shaped apertures cov- MISCHODONTHWAITES (1 SPECIES). eredwith granular or smoothmembranes. Punt Mischodonzeylanicus Thwaites (Sri Lanka, (1962), who studieddifferent material, consid- Waas 336, MO). Pollen globose(38 ,im), 5-7- ered the pollen inaperturate.All theseauthors porate,zoni-aperturate; sculpturing echinate (3.8 used onlyLM. Dahlgrenand van Wyk(1988) ,umlong); ektexine with a thin(0.25 ,um), irregular used bothLM and SEM foranother sample and footlayer, an irregularinterstitium that is dis- foundthat most grains were inaperturate but some continuouswith the foot layer, and a microper- hada fewplaces where the thin tectum apparently forate/baculatetectum (0.44 ,m; fig.51); endex- was tornto forma small"pore" witha granular ine thin; intine two-layered(fig. 51). Our membrane.Our observationsare based on both observationsare consistentwith those of Erdt- LM and SEM. Thoughclearly visible with SEM, man (1952), Punt (1962), K6hler (1965), and withLM theapertures often were extremely in- Haydenet al. (1984). conspicuousbut could be resolvedusing Herr's clearingfluid (Herr 1971). The possibilitythat ARISTOGEITONIAPRAIN (3 SPECIES). thereare both pantoporate and inaperturatepop- Aristogeitoniamonophylla Airy Shaw (Kenya, ulationsshould be investigatedfurther. Our ob- Faden et al. 45256, K). Pollen oblate(30 x 34 servationsare otherwiseconsistent with reports ,um),5-7-brevicolpate (possibly brevicolporate), by Erdtman(1952), Punt(1962), K6hler(1965), zoni-aperturate;sculpturing echinate (4.1 ,m and Dahlgrenand van Wyk(1988). long); ektexinewith no footlayer, an irregular and oftenvery reduced interstitium, and a mi- STACHYANDRAR.-SM. (4 SPECIES). croperforate/baculatetectum (0.24 ,um;fig. 52); Stachyandra merana (Airy Shaw) R.-Sm. endexineconsisting of a thinbasal layer(fig. 52); (Madagascar, Capuron 23335-SF, P [isotype]). intinetwo-layered, somewhat thickened at ap- Pollen globose (44 ,um),4-6-porate, zoni-aper- erturalborder (fig. 53). 326 INTERNATIONAL JOURNAL OF PLANT SCIENCES

45 46

7 7

4.~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ s

e-47i 48 49

f~~49~4 v.-~~ :

Figs.45-49 Pollenof Euphorbiaceae subfamily Oldfieldioideae. Figs. 45, 46, Androstachysjohnsonii.Fig. 45, Nonapertural wall,TEM; arrowindicates scanty endexine beneath foot layer. Fig. 46, Aperturalregion, TEM; arrowindicates endexine. Fig. 47, Stachyandramerana. Nonapertural wall, TEM; arrowindicates endexine. Figs. 48, 49, Stachyandrarufibarbis. Fig. 48, Nonaperturalwall, TEM; arrowindicates thin endexine. Fig. 49, Wallat aperturalregion, TEM; notegreatly thickened endexine (arrow).Scale bars= 0.5 Aimin figs.45, 47; 1 gmin figs.46, 48, 49.

Although pollen of this species has not been er,an irregularinterstitium that is discontinuous described, pollen of Aristogeitonialimoniifolia withthe foot layer, and a microperforate/baculate Prain and Aristogeitoniaperrieri (Leandri) R.-Sm. tectum(0.47 ,um; fig. 54); endexinethin (fig. 54), (= Paragelonium perrieriLUandri) is similar,ap- thickenedat apertureborder (fig. 55); intinetwo- parentlydiffering primarily in having somewhat layered,thickened in aperturalregion (fig. 55). shorter (2.5-3.5 ,um long) spines (Punt 1962; Descriptionsand illustrationsof this species K6hler 1965). These authors were ambivalent (Erdtman1952; Punt 1962, 1987; K6hler 1965) about whetherthe aperturesare simple or com- are generallyconsistent with our observations. pound, a problem we, too, have been unable to Erdtmanand K6hler, however, reported the grains resolve. (as Toxicodendronglobosum [Gaertner] Pax and K. Hoffm.)to be considerablysmaller (29-31 x TRIBE CALETIEAE MUELL. ARG. (14 GENERA, 53 34,m), whereasPunt's (1962) measurements(39 SPECIES; 4 OF 4 SUBTRIBES INVESTIGATED). x 46 ,um)are closerto ours.

SUBTRIBE HYAENANCHiNAE BAILLON EX MUELL. SUBTRIBEDISSILIARIINAE PAX AND K. HoFFM. ARG. (1 GENUS, 1 SPECIES). (6 GENERA,28 SPECIES).

HYAENANCHE LAMBERT (1 SPECIES). WHYANBEELIAAIRY SHAWAND B. HYLAND(1 Hyaenancheglobosa(Gaertner) Lambert (South SPECIES). Africa,Lavranos and Bleck 20843A, MO). Pollen Whyanbeeliaterrae-reginae Airy Shaw and B. suboblate (40 x 42 ,um),6-7-aperturate, zoni- Hyland (, Hyland 3041, DAV). Pollen aperturate;sculpturing echinate (2.1 ,um long); oblate (27 x 30,um),5-6-porate, zoni-aperturate; ektexine with a thin (0.34 Aim),irregular foot lay- sculpturingechinate (4.1 ,um long); ektexinewith SIMPSON & LEVIN-EUPHORBIACEAE POLLEN 327

50 51

52

Figs.50-53 Pollenof Euphorbiaceaesubfamily Oldfieldioideae. Fig. 50, Voatamaloeugenioides. Nonapertural wall, TEM; arrowindicates endexine. Fig. 51, Mischodonzeylanicus. Wall nearapertural region, TEM, obliquesection; note thickened endexine(arrow). Figs. 52, 53,Aristogeitonia monophylla. Fig. 52, Nonaperturalwall, TEM; arrowindicates endexine. Fig. 53, Aperturalregion, TEM; arrowindicates thin endexine. Scale bars= 1 ,umin figs.50, 51, 53; 0.5 ,m in fig.52.

no footlayer, an interstitiumofirregularly spaced layered,thick, somewhat more thickened in ap- columnarelements, and a microperforate/bacu-erture region (figs. 57, 58). latetectum (0.48 ,um;fig. 56); ektexineat aperture Priordescriptions and illustrationsof this spe- borderwith thickened basal layer;endexine con- cies (Erdtman1952; Punt 1962, 1987; K6hler sistingof a thinbasal layer(fig. 56), thickenedat 1965; Martin 1974 [as Austrobuxusbuxoides apertureborder. Pollen of this genus has notbeen Baillon];and Lobreau-Callenin McPhersonand describedpreviously. Tirel 1987) are generallyconsistent with our ob- servations,though all authorsreported the pollen LONGETIABAILLON (1 SPECIES). to be smaller(18-22 x 24-27 ,um).Martin's Longetia buxoidesBaillon (, (1974) statement,based on LM, thatthe sculp- McPherson3789, MO). Pollen oblate(27 x 30 turingis finelyreticulate is mistaken,as shown ,um),6-7-brevicolporate, zoni-aperturate, with byour observations and SEMs publishedby Lob- circularendoaperture; sculpturing scabrate (0.4 reau-Callen(in McPhersonand Tirel 1987) and ,umlong); ektexine with no footlayer, an inter- Punt(1987). Punt(1962) apparentlymissed see- stitiumof sparse,irregular to columella-likeel- ingthe minute scabrae with LM and incorrectly ements,and a nearlyimperforate tectum (0.84 describedthe pollen as psilate. ,um)with occasional minute scabrae (fig. 58); ek- texineof aperturalregion with tectum bulging CHORICERAs BAILLON (2 SPECIES). outward,delimiting the outer widely elliptic ex- Choricerasmajus AiryShaw (Australia,Hy- oaperture,and withbasal thickeningsconstitut- land 10633, K). Pollen oblate (26 x 28 ,um), ingthe inner circular endoaperture (fig. 57); en- 6-porate,zoni-aperturate; sculpturing scabrate dexine moderatelythick (fig. 58), thickened (0.2 ,umlong); ektexinewith no footlayer, an slightlyat apertureborder (fig. 57); intinetwo- irregularinterstitium, and a microperforatetec- 57

59

_ t _ ~~ ~ ~~~~~~61

V__ t . ' .^ ..... ,~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

60

f.9.

Figs.54-62 Pollenof Euphorbiaceaesubfamily Oldfieldioideae. Figs. 54, 55, Hyaenache globosa. Fig.54, Nonaperturalwall, TEM; arrowindicates very thin endexine below foot layer. Fig. 55, Aperturalregion, TEM, showingthickened endexine (arrow). Whyanbeelia Fig.56, terrae-reginae.Nonapertural wall, TEM; arrowindicates thin endexine. Figs. 57, 58, Longetiabuxoides. SIMPSON & LEVIN-EUPHORBIACEAE POLLEN 329 tum(0.43 ,m; fig.59); ektexineat apertureborder Petalostigmaquadriloculare F. Muell.(Austra- with thickenedbasal layer (fig.60); endexine lia, Mocanochie1993, K). Pollen oblate(32 x forminga thinbasal layer(fig. 59), somewhat 34,m), 5-6-porate,zoni-aperturate; sculpturing thickenedin aperturalregion (fig. 60); apertural echinate(1.0 ,m long);ektexine with no footlay- intinethickened, two-layered (fig. 60). er, an irregularinterstitium, and a microperfor- Althoughthis is thefirst description of the pol- ate/baculatetectum (0.51 ,um;fig. 63); endexine len of thisspecies, pollen of Choricerastricorne forminga thinbasal layer(fig. 63), thickenedat (Benth.)Airy Shaw, the only other species in the aperturalborder (fig. 64); intinetwo-layered (fig. genus,has been describedand illustratedunder 63), thickenedin aperturalregion (fig. 64). itssynonym Dissiliaria tricornis Benth. by several Erdtman(1952) studiedpollen identified as P. authors(Erdtman 1952; Punt 1962; Kohler 1965; pubescens,and Punt (1962) and Kohler(1965) Martin1974). The two speciesappear to have studiedwhat they called P. quadriloculare.Un- verysimilar pollen, perhaps with that of C. tri- fortunately,prior to AiryShaw's revisionof the cornebeing somewhat smaller (18-22 x 20-25 genusin 1976, manycollections were misiden- ,um).Martin's (1974) statement,based on LM, tified(Airy Shaw 1976). All our samplescame thatthe sculpturing is finelyreticulate is contra- fromspecimens annotated by AiryShaw, but he dictedboth by ourobservations and thoseof the didnot cite any of the specimens that were sources remainingauthors cited above. Punt(1962) ap- forthe pollen studied by the others, so we cannot parentlydid not see the scabraewith LM and determineif differencesin observationsreflect incorrectlydescribed the pollen as psilate.The variationwithin species or simplymisidentifi- tectumof Choriceras has fewer microperforations cations. In generalour observationsare consis- and lacks the baculatestructure found in most tentwith these earlier descriptions. All authors Oldfieldioideae(Discussion). reportedsmaller diameters than we measured:26 x 28 Amfor P. pubescens(Erdtman 1952) and DISSILIARIA F. MUELL. EX BAILLON (3 SPECIES). 25-28.5 x 28-32 umfor P. quadriloculare(Punt Dissiliariabaloghioides F. Muell. ex Baillon 1962; K6hler1965). More significantly,they all (Australia,MacPherson s. n. [January23, 1980], reportedthat the aperturesof Petalostigmado QRS). Pollensuboblate (36 x 38 ,um),5-6-por- not lie exactlyin the equatorialplane. Our ob- ate,zoni-aperturate; sculpturing echinate (4.1 ,m servationsare notentirely consistent with theirs. long);ektexine with no footlayer, an irregular In P. pubescenswe foundthat some of the ap- interstitium,and a microperforate/baculatetec- erturesindeed lay outsidethe equatorialplane, tum(0.75 ,im; fig.61); ektexineat apertureborder but in P. quadriloculareall the apertureswere with thickenedbasal layer (fig.62); endexine strictlyequatorial. Because they are oblique polar forminga thinbasal layer(fig. 61), apparently views,the LM photographsof this species shown extendingacross aperture (fig. 62); intineof ap- byMartin ([1974], as Petalostigmahaplocladum erturalregion thick, two-layered (fig. 62). Martin Pax and K. Hoffm.)are difficultto interpret.It is (1974) illustratedpollen of thisspecies and de- possiblethat aperture distribution in Petalostig- scribedit as globosewith smaller diameter (27- ma mayrepresent a transition between zoni-aper- 30,m) and shorterspines (2.5-3 gm). turateand pan-aperturate,particularly ifthe spe- cies themselvesare polymorphic. SUBTRIBE PETALOSTIGMATINAE PAX AND K. HoFEM.(1 GENUS, 6 SPECIES). SUBTRIBE PSEUDANTHINAE MUELL. ARG. (6 GENERA, 18 SPECIES). PETALOSTIGMAF. MUELL. (6 SPECIES). Petalostigmapubescens Domin (Australia, NEOROEPERA MUELL. ARG. & F. MUELL. (2 SPE- Speck 1818, K). Pollen oblate (32 x 34 ,um), CIES). 5-porate,? zoni-aperturate;sculpturing echinate Neoroeperabuxifolia Muell. Arg.& F. Muell. (0.9 ,m long); ektexine with no foot layer, an (Australia,White 12095, US). Pollenglobose (33 irregularinterstitium, and a microperforate/bac-Jim), 16-20-pantoporate; sculpturing echinate (5.1 ulatetectum (0.38 ,im); endexineforming a thin ,m long),psilate with evident micropores in in- basal layer,thickened at aperturalborder; intine terspinalregion (fig. 38); ektexinewith no foot of aperturalregion thick, two-layered (not illus- layer,an interstitiumofirregularly spaced colum- trated). narelements, and a microperforate/baculatetec-

Fig. 57, Aperturalregion, TEM; notethickened basal ektexine(ek) and endexine(arrow). Fig. 58, Nonaperturalwall, TEM; arrowindicates endexine. Figs. 59, 60, Choricerasmajus. Fig. 59, Nonaperturalwall, TEM; arrowindicates endexine. Fig. 60, Aperturalregion, TEM. Notethickened, basal ektexine (ek) and thin endexine (arrow) at apertural border. Figs. 61, 62, Dissiliaria baloghioides.Nonapertural wall, TEM; arrowindicates endexine. Fig. 62, Aperturalregion, TEM; notethickened ektexinous layer(ek) at aperturalborder. Scale bars= 0.5 ,umin figs.54, 59; 1 ,umin figs.55, 56, 60-62; 2 ,umin figs.57, 58. 330 INTERNATIONAL JOURNAL OF PLANT SCIENCES tum (0.63 ,im; fig.65); nonaperturalendexine MICRANTHEUMDESF. (3 SPECIES). forminga thinbasal layer(fig. 65). Henderson's Micrantheumhexandrum Hook. f. (Australia, (1992) illustrationof the pollen of this species is Briggsand Johnson4419, DAV). Pollenglobose consistentwith our observations. K6hler's (1965) (34 ,um),ca. 30-40-pantoporate(fig. 37); sculp- descriptiondiffers from ours in thathe reported turingechinate (3.0 ,m long); ektexinewith a thatthe grains were 27 ,m in diameterand bore thick(1.5 ,um),homogeneous foot layer, an ir- 30-40 pores.Otherwise his description agrees with regularinterstitium that is discontinuouswith the our observations. footlayer, and a microperforate,granular tectum Neoroeperabanksii Benth. (Australia, Hyland (0.33 ,um;fig. 71); footlayer at apertureborder 6945, K). Pollenglobose (36 ,um),ca. 25-panto- slightlythickened (fig. 71); endexineabsent or porate;sculpturing echinate (3.7 ,m long); ek- veryscanty (fig. 71); intinetwo-to-three-layered, texinewith a thick(0.98 ,m), homogeneousfoot theouter one to twolayers thickened in apertural layer,an irregularinterstitium that is generally region(fig. 71). discontinuouswith the footlayer, and a micro- Pollenof this species has been describedand/ perforate,granular tectum (0.26 ,im; fig.66); foot or illustratedby Erdtman(1952), Punt (1962), layerat apertureborder slightly thickened (fig. K6hler (1965), Martin(1974), and Henderson 66); endexinenot observed; intine two-to-three- (1992). Thesereports differ from ours only in that layered,the outer one to twolayers thickened in Punt(1962) statedthe pollen diameter to be 45 aperturalregion (fig. 66). Punt's(1962) descrip- ,um(whereas the others gave diameters very close tionand Martin's(1974) and Henderson's(1992) to our measurementof 34,im) and thatboth he illustrationsof the pollen of this species are gen- and K6hler(1965) reported40-50 apertures.The erallyconsistent with our observations,though pollenof Micrantheum ericoides Desf. differsin Puntreported the pollento be somewhatlarger itssmaller size, fewer apertures with spines clus- (40,m) withshorter spines (2 gm) and up to 30 teredaround them, and thickerexine (Erdtman apertures. 1952; Punt 1962; K6hler 1965), indicatingthat pollenmight provide systematically useful infor- KAIROTHAMNUS AIRY SHAW (1 SPECIES). mationat theinfrageneric level in Micrantheum. Kairothamnusphyllanthoides(Airy Shaw) Airy Shaw (Papua New Guinea, StreimannNFG PSEUDANTHUS SIEBER EX SPRENGEL (7 SPECIES). 24462, K). Pollenglobose (26 gim),10-12-pan- Pseudanthusdivericatissimus (Muell. Arg.) toporate;sculpturing echinate (1.8 ,m long);ek- Benth.(Australia, Coveny 5253, DAV). Pollen texinewith a thick(0.61 gm),homogeneous foot globose(23 ,m), 10- 14-pantoporate; sculpturing layer,an interstitiumof irregulargranular ele- echinate(1.2,um long); ektexine with a thick(0.65 mentsthat are discontinuouswith the foot layer, ,im)foot layer, an interstitiumofirregular colum- and a microperforate,granular to tabulartectum narelements that are discontinuous with the foot (0.21 gim;fig. 67); footlayer at apertureborder layer,and a microperforate,granular tectum (0.22 slightlythickened (fig. 68); endexineobvious only ,im; figs.72, 73); footlayer at apertureborder at apertureborder (fig. 68); intinetwo-to-three- thickened(fig. 72); endexinenot observed; intine layered(figs. 67, 68), theouter one to twolayers two-to-three-layered,theouter one to twolayers thickenedin aperturalregion (fig. 68). Pollen of thickenedin aperturalregion (fig. 73). thisgenus has notbeen describedpreviously. Pollen of thisspecies has not been described previously,but our observationsare consistent SCAGEA MCPHERSON (2 SPECIES). withdescriptions of the pollenof otherspecies Scagea oligostemon(Guillaumin) McPherson (Erdtman1952; Punt 1962; K6hler 1965). Ap- (New Caledonia,Webster 19181, DAV). Pollen erturenumber varies considerably within the ge- globose(30,um), 16-20-pantoporate; sculpturing nus,with reports of six to eightapertures in Pseu- echinate(1.9,um long); ektexine with a thick(0.70 danthusnematophorus F. Muell., Pseudanthus gim),homogeneous foot layer, an interstitiumof orientalisF. Muell. and Pseudanthuspimeloides irregular,granular elements that are discontinu- Sieber; 10-14 in Pseudanthusdivericatissimus; ous withthe footlayer, and a microperforate, 18-25 in Pseudanthusvirgatus (Klotzsch) Muell. granularto tabulartectum (0.19,um; fig. 69); foot Arg.; and 20-25 in Pseudanthusovalifolius F. layerat apertureborder slightly thickened (fig. Muell.With further study, aperture number may 70); endexineobserved only at apertureborder proveto be of systematicvalue in thisgenus. (fig.70); intinetwo-layered (fig. 69), the outer layerthickened in aperturalregion (fig. 70). De- STACHYSTEMONPLANCHON (3 SPECIES). scriptionsand illustrationsof the pollenof this Stachystemonpolyandrus (F. Muell.) Benth. species (Punt [1962], as Longetia gynotricha (Australia,Young Y-325, DAV). Pollenglobose Guillaumin;Lobreau-Callen in McPhersonand (22,um),ca. 12-pantoporate(apertures obscure); Tirel [1987]) are consistentwith our observa- sculpturingechinate (1.8 gmlong); ektexine with tions. a thin (0.34 gim),homogeneous foot layer, an SIMPSON & LEVIN-EUPHORBIACEAE POLLEN 331

63 64

. ~ ~ ~ ~ .

~~~~~~~~~~~~~~~~~~~~~~~~~4-'

65 ~~~~~~66

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6 7

6 8

444 44~~~~

Figs.63-68 Pollenof Euphorbiaceae subfamily Oldfieldioideae. Figs. 63, 64, Petalostigmaquadriloculare. Fig. 63, Nonaper- turalwall, TEM; arrowindicates endexine. Fig. 64, Aperturalregion, TEM; noteendexine (arrow), thickened at apertural border.Fig. 65, Neoroeperabuxifolia. Nonapertural wall, TEM; arrowindicates thin endexine. Fig. 66, Neoroeperabankcsii. Nonapertural(center) and apertural(far right)walls, TEM; note thick foot layer. Figs. 67, 68, Kairothamnusphyllanthoides. Fig. 67, Nonaperturalwall, TEM. Fig. 68, Aperturalregion, TEM; arrowindicates endexine. Scale bars = 0.5 um in fig.63, 64; 1 'min figs.65-68. interstitiumof irregularcolumnar elements that endexinepossibly deposited at apertureperiph- are discontinuouswith the foot layer, and a mi- ery(fig. 74); intinetwo-to-three-layered, theouter croperforate,granular tectum (0.14 ,um;fig. 74); one to two layersthickened in aperturalregion footlayer at apertureborder thickened (fig. 74); (fig.74). Pollen of thisspecies has not been de- 332 INTERNATIONAL JOURNAL OF PLANT SCIENCES

69 70

0~~~~~~~~~~~~~~~~~~~~~~~~0

73 s -: 74

Figs.69-74 Pollen of Euphorbiaceae subfamilyOldfieldioideae. Figs. 69, 70, Scagea oligostemon.Fig. 69, Nonaperturalwall, TEM. Fig. 70, Wall, TEM, showingtwo apertures;arrow indicates endexine. Fig. 71, Micrantheumhexandrum. Wall, TEM, showingtwo apertures.Figs. 72, 73, Pseudanthusdivericatissimus.Fig. 72, Whole graincross-section, TEM. Fig. 73, Nonapertural wall, TEM. Fig. 74, Stachystemonpolyandrus. Wall, TEM, showingone aperture.Scale bars = 1 ,umin figs.69, 73, 74; 2 ,um in figs.70, 71; 5 Am in fig.72.

scribedpreviously. Pollen of Stachystemonver- Discussion micularisPlanchon apparently is larger(28-36 ,um)but otherwisesimilar (Erdtman 1952; Punt Thesepalynological data provideseveral char- 1962; K6hler1965). Aperturenumber in thelat- actersof systematic significance (table 1). We have terspecies is unclear,with Punt (1962) reporting previouslyutilized these data, along withmor- 12 aperturesin agreementwith our countfor S. phologicaland anatomicalcharacters, in a cla- polyandrus,but K6hler(1965) reporting17-22. disticanalysis of the subfamilyOldfieldioideae SIMPSON & LEVIN-EUPHORBIACEAE POLLEN 333

(Levin and Simpson 1994a). In thatstudy, re- 1962), may constitutea synapomorphyuniting lationshipsin thesubfamily Phyllanthoideae were some taxa withinthe Phyllanthoideae,but our not well resolved.In contrast,phylogenetic re- studyof this subfamily is tooincomplete to verify lationshipswithin the Oldfieldioideae were well this.All investigatedmembers of the subfamily resolved,with the palynological data almost com- Oldfieldioideaehave apertures that with SEM ap- pletelycompatible with the morphologicaland pear to be brevicolpateor porate(table 1; figs. anatomicaldata. We tracefour of the pollen char- 35-38), a synapormorphyfor the subfamily (Lev- actersonto our preferredcladogram (fig. 75) for in and Simpson 1994a). Structurally,the aper- referencewith the following discussion. turesof most Oldfieldioideae probably are brev- icolporateor pororate,i.e., theyhave a circular, POLLEN SHAPE differentiallythickened endoaperture in addition Most investigatedmembers of the subfamily to theexoaperture (Punt [1962], Kohler [1965], Phyllanthoideaehave prolategrains (table 1; fig. Haydenet al. [1984], all of whomused LM to 17).Other studies (Punt 1962; Kohler 1965)have studyacetolysed pollen grains, the best technique shownthat both prolateand globoseto oblate fordetecting the endoaperture of colporate or po- pollengrains are widespreadin thePhyllanthoi- roratepollen). deae. All membersof thesubfamily Oldfieldioi- deae, as delimitedhere, have a globoseto oblate APERTURE NUMBER pollenshape (table 1; figs.33, 35, 37). It is not Croizatia(Oldfieldioideae) and all investigated clearwhich pollen shape is evolutionarilyderived membersof the Phyllanthoideaehave 3-aper- in thesesubfamilies (Levin and Simpson1 994a). turatepollen grains (table 1; figs.8, 16,20). How- POLLEN SIZE ever,some species of the large genus Phyllanthus, notinvestigated in thisstudy, may have up to 60 Mode ofpreparation can greatly influence grain apertures(table 1). All membersof the Oldfiel- size(reviewed by Moore et al. 1991).In ourstudy, dioideae(except Croizatia) have fromfour to ca. all pollensamples were prepared in thesame way 40 apertures(table 1). Withinthe Oldfieldioideae, and comparisonsamong them are valid. How- theoccurrence of more than three apertures con- ever,differences in pollen size fromother studies stitutesa synapomorphyfor the tribesPodoca- aredifficult to evaluatebecause of differing meth- lyceae,Picrodendreae, and Caletieae(i.e., forall ods ofpreparation. In addition,we did noteval- but Croizatia,the mostbasal taxonof theOld- uateintraspecific variation in pollensize because fieldioideae[Levin and Simpson1 994a]). of our limitedsamples. A strongcorrelation exists between aperture Investigatedmembers of the Phyllanthoideae shapeand aperture number. The 3-aperturatetaxa have pollengrains ranging from ca. 12 to 33 ,um mostlyhave a colporate(rarely brevicolporate) maximumdiameter, except for Amanoa spp., apertureshape, the exception, mentioned above, whichhave distinctlylarger grains, ranging from beingHymenocardia, which has threeessentially ca. 40-52 Atmmaximum diameter (table 1). (Pol- porateapertures (fig. 23). Taxa withfour or more len of Phyllanthusspp., not investigatedhere, aperturesall have porate(to pororate)or brevi- have diametersup to 45 ,um[table 1].) In the colpate(to brevicolporate)aperture shape. Of the Oldfieldioideaemaximum diameters range from Oldfieldioideaewith more than three apertures, ca. 22 to 50 ,4m(table 1). Taxa of thetribe Cal- aperturenumber varies considerably.No clear etieaehave on averageslightly smaller grains (ca. discontinuityis apparent between taxa with four 22-42 ,ummaximum diameter) than members of and thosewith up to ca. 40 apertures;a corre- thetribe Picrodendreae (ca. 27-50 ,ummaximum lation is evident,however, between aperture diameter).The Podocalyceaehave relatively small numberand apertureposition. grains(ca. 25-27 Ammaximum diameter); Cro- izatia (Croizateae)has intermediate-sizedpollen APERTURE POSITION (32 ,ummaximum diameter). Obviously, there is Pollenof all investigatedmembers of the Phyl- considerableoverlap in pollensize amongthese lanthoideaeis zoni-aperturate(table 1; figs.17, taxa,and no cleartrends are apparent. 20, 23). However,some species of the large genus Phyllanthus,not investigatedin this study,are APERTURE SHAPE pan-aperturate(table 1). In the Oldfieldioideae All 12 investigatedmembers of thesubfamily the zoni-aperturatecondition is ancestral(fig. Phyllanthoideaehave colporate apertures with the 75A). Withinthis subfamily the pan-aperturate exceptionof Hymenocardia, which has short,es- condition(figs. 35-38) is a synapomorphyfor the sentiallyporate apertures (table 1; fig.23). How- subtribePseudanthinae of the tribe Caletieae, and ever,some species of the large genus Phyllanthus, it aroseindependently in Androstachysjohnsonii not investigatedin this study,have porateap- (fig.75A; Levinand Simpson1994a). ertures(table 1). The presenceof a lalongate Apertureposition and numberare correlated (transverselyor latitudinallyoriented) endoap- to some degree.Taxa withthree apertures are erture,also calleda "colpustransversalis" (Punt alwayszoni-aperturate, as are most taxa with four Y ? t ~~~~~~0>e0 0> 0 00 0- 00 0 ?

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BjpuBAqoL,jS ujpuEAqoBjS 0 +5 sAqoujsojpuV// sAqoEjsojpuV// cd LIIPIGIIPIO 1-4 j LIIPIOIIPIO -2 uoipuepoueBle 0 d; uoipuepoueeleo 0 10 r_; E84uuJld eequeiid UOJPUGPOJO'd uOJPuGPOJO'd 4-4 uOJPuGPOIPOJud uoipuepoi snooooeile i snooooeiie 1 xAlLI30POd xAIB3OPOd solodAiPEJud 10 0 Blieziojo EIIBZIOJO 0 40 U rv-, SIMPSON & LEVIN-EUPHORBIACEAE POLLEN 339 to eightapertures (table 1). The exceptionis A. ingtectate pollen in whichthe tectumand col- johnsonii,which has fiveto sevenapertures (fig. umellaeform a coarsereticulum (figs. 4, 5; Erdt- 35),and somespecies of Pseudanthus that we did man 1952; Kohler 1965; Punt 1962). The notinvestigate, which have sixto eightapertures structurein A. guianensismay have evolvedei- (Punt1962, Kohler 1965). Taxa with10 or more therby loss of the foot layer and interstitium, and aperturesare alwayspan-aperturate. additionof the baculae, or by loss ofthe tectum withthe columellae appearing as baculae.We ac- POLLEN SCULPTURING ceptthe latter hypothesis mainly because of the Almostall investigatedmembers of thePhyl- similarityin ektexinestructure between A. gui- lanthoideaehave pollenwith nonspinose, retic- anensisand A. strobilacea.The basal layerof A. ulateto foveolateexine sculpturing (fig. 17). Iso- guianensisis homogeneousand unstratified,re- latedexceptions are Amanoa guianensis(fig. 1), semblingin bothstructure and thicknessthe foot whichhas baculate sculpturingapparently de- layerof A. strobilacea.The baculae of A. gui- rivedfrom an ancestrallyreticulate condition, and anensisare similarin size to thecolumellae of A. Securinega(fig. 7), whichis echinatewith psilate strobilacea.In addition,some grainsof A. gui- interspinalsculpturing. Didymocistus (figs. 20) and anensisshow occasionaldistal connections be- Hymenocardia(figs. 23, 25) both have minute tweenadjacent baculae, resembling partial muri scabraewith rugulate interspinal sculpturing, par- of a reticulateexine (e.g., Punt 1987,fig. 9). We tialevidence for a closerelationship between them thereforeinterpret the pollen of A. guianensisas (Levin and Simpson1994b). beingintectate sensu Walker and Doyle (1975), All investigatedOldfieldioideae have pollen thebaculae being homologous with the columel- withradially elongate, sharply tapering spines that lae of otherAmanoa species.The similaritybe- are continuouswith the tectum(figs. 40-42), tweenthe distallyrounded baculae of A. gui- whichconstitutes a synapomorphyfor the sub- anensisand the distallypointed echinae of the familyOldfieldioideae as a whole (Levin and Oldfieldioideaeis, therefore,only superficial and Simpson 1994a). The spines of most Oldfiel- notthe result of homology(Levin and Simpson dioideaeare prominent echinae, ranging from 0.9 1994a). ,umto as longas 5.5 ,m in length(table 1). Within Hymenocardiahas sometimesbeen removed theOldfieldioideae, Choriceras (figs. 59, 60) and fromthe Euphorbiaceae and placednear the Urt- Longetia(figs. 57, 58) have veryshort scabrae icales,in parton the basis of palynology(Airy lessthan 0.4,um long, a synapomorphyfor these Shaw 1965; Dechampset al. 1985). Our obser- twogenera (Levin and Simpson1 994a). The bac- vationsshow thatHymenocardia (figs. 24, 25) ulate pollen of A. guianensisand the echinate has thetectate-columellate exine structure typical pollenof Securinega(both Phyllanthoideae) ap- ofthe Phyllanthoideae, which is veryunlike that pearto haveevolved independently from similar foundin theUrticales (Zavada andDilcher 1986), pollenin theOldfieldioideae (Levin and Simpson thussupporting the retention of this genus in the 1994a). Euphorbiaceae(Levin and Simpson1994b). The surfacesculpturing pattern between the In thesubfamily Oldfieldioideae there are sev- spinesin Oldfieldioideaeis oftenambiguous. The eralbasic ektexinous structures, all differentfrom appearancemay depend on pollen preparation thosewe observedin the Phyllanthoideae.The and the presenceof pollenkitt,which may ob- predominantstructural pattern in the Oldfiel- scurethe underlying exine (figs. 29, 49, 63). In- dioideae(figs. 32, 40) consistsof (1) a footlayer terspinalsculpturing of severaltaxa is verrucate thatis eitherthin and irregularor absent,a syn- (fig.34) and for othersfoveolate (fig. 38); re- apomorphyfor the Oldfieldioideaeexcept Cro- mainingtaxa have eithersmooth or "wrinkled" izatia (fig.75B); (2) an interstitiumconsisting of interspinalsculpturing (fig. 36). We detectedno irregularcolumellate to granularelements that clearphylogenetic patterns (Levin and Simpson are discontinuousfrom the footlayer, a syna- 1994a). pomorphyfor the Oldfieldioideae as a whole(fig. 75C); and (3) a microperforate/baculatetectum, EXINE ULTRASTRUCTURE composed of laterallyappressed baculate ele- All investigatedmembers of the Phyllanthoi- mentsthat delimit fine perforations, a synapo- deae exceptA. guianensishave a typicalthree- morphyfor the Oldfieldioideae except Croizatia layeredtectate-columellate ektexine architecture (fig.75D). Kohler(1965), usingLM, described consistingof a perforate/homogeneoustectum, a thisassemblage of structuralfeatures as the Te- homogeneousfoot layer, and interveningcolu- tracoccustype. mellaethat are continuous with the foot layer (fig. Withinthe Oldfieldioideae, all membersof the 14). Amanoaguianensis, in contrast,has a two- subtribePseudanthinae except Neoroepera bux- layeredektexine consisting of a thick,ektexinous ifolia(fig. 65)-thus includingKairothamnus (figs. basal layerand baculae(fig. 2). All otherspecies 67, 68), Scagea (figs.69, 70), Neoroeperabanksii ofAmanoa resemble Amanoa strobilacea in hav- (fig.66), Micrantheum (fig. 7 1),Pseudanthus (figs. 340 INTERNATIONAL JOURNAL OF PLANT SCIENCES

72, 73), and (fig. 74)-have an ex- fieldioideaeand most closelyrelated to Stach- ine architecturequite different from that typical yandra(fig. 75). Thus,the exine structure of An- of the subfamily(Levin and Simpson 1994a). drostachysis independentlyderived from that of Althoughsimilar in havingan irregularintersti- the Phyllanthoideae(fig. 75 B-D). In fact,the tium,the exine of these taxa has a homogeneous exinestructure of Androstachys and thePhyllan- (not irregular),relatively thick foot layer and a thoideaediffer in thatAndrostachys has a much relativelythin, microperforate tectum in which thinnerfoot layer (0.07 Amvs. 0.1 1 Amfor the thetectal elements are granularto tabularrather thinnestinvestigated Phyllanthoideae), very than baculate. Kohler (1965), using LM, de- sparse,delicate columellae, and a microperfor- scribedthis assemblage of structuralfeatures as ate/homogeneoustectum. The two investigated the Micrantheumtype. Both the footlayer and speciesof Stachyandra have a tectumthat, though tectumconditions are synapomorphiesfor the microperforate/baculate,may be transitionalto Pseudanthinae,minus N. buxifolia(fig. 75B, D) thatfound in Androstachysin havingfewer mi- Notethat the "relatively thick" foot layer of these croperforationsand a lessbaculate structure than Pseudanthinaeis not alwaysabsolutely thicker mostother Oldfieldioideae. A similarbut evo- thanall otherOldfieldioideae; however, the foot lutionarilyindependent loss of microperforations layerto tectum ratio for all Pseudanthinae(except and baculatestructure is apparentlyshown by N. buxifolia)is greaterthan 2.5, whereasthat for Choricerasand Longetia(fig. 75D). all otherOldfieldioideae (including N. buxifolia In mosttaxa of the Oldfieldioideae,the foot butwith the exception of Croizatia)is less than layerand/or endexine are thickened at theborder 1. AlthoughMcPherson and Tirel (1987) referred of the aperture,which may functionto provide Scagea to theCrotonoideae because of its unio- structuralsupport for the aperture.This basal vulatelocules, our study shows that it has pollen thickeningpresumably is equivalentto themar- ultrastructureidentical to otherPseudanthinae gin of an endoapertureor "os." In mostof the (Levin and Simpson 1994a) and verydifferent observedtaxa, this is theresult of an abruptthick- fromthat of the Crotonoideae(Nowicke 1994). eningof the endexine and an associatedthinning The structurallysimilar exine of Croizatia(figs. ofthe ektexinous foot layer. However, in thegen- 27,28) evolvedindependently ofthat in the Pseu- era Whyanbeelia,Longetia, Choriceras, and Dis- danthineae(fig. 75B, D). siliariathe apertural border thickening occurs not Paradrypetes(fig. 29) and Podocalyx(figs. 30, in theendexine but in theektexinous foot layer 31) are unusualin havinga two-layeredexine (figs.60, 62). Basedon thecladistic study of Levin consistingof an irregularinner layer that is dis- and Simpson(1994a), thisthickening of theek- continuousfrom an imperforateor microperfor- texinousfoot layer represents a synapomorphy ate/baculateouter layer. We interpretthe outer of thesefour genera. Similar ektexinous thick- layerto be homologousto the tectumin other eningsare foundin Croizatia,some Pseudan- Oldfieldioideaebecause it is continuouswith the thinae,and questionablyOldfieldia, but are usu- echinaeand, in Podocalyx,it exhibitsthe micro- allyless well developed and areall independently perforate/baculatestructure found in mostOld- derived(Levin and Simpson1994a). fieldioideae.Because the interstitial elements of In conclusionthere is considerablepalynolog- all otherOldfieldioideae are continuouswith the ical diversityin thesubfamilies Phyllanthoideae tectum,we interpretthe inner exine layer of Par- and Oldfieldioideaeof the Euphorbiaceae.Our adrypetesand Podocalyxas homologouswith the observations,particularly those using TEM, not footlayer, not the interstitium;thus, the inter- onlyreinforce results from prior studies but also stitiumis absent,a synapomorphyfor these two providesignificant new data. This is especially genera(fig. 75C). A close relationshipbetween truewith regard to exinewall structure. Cladistic thesetwo genera is also supportedby anatomical analysis(Levin and Simpson1994a) of our pal- characters(Levin and Simpson1994a). The tec- ynologicaldata along with data from morphology tumof Podocalyx,though microperforate/bacu- and anatomyhas demonstratedtheir phyloge- late,is less segmentedthan that in mostOldfiel- neticsignificance, particularly for delimiting the dioideaeand maybe evolutionarilyintermediate Oldfieldioideaeand inferring its phylogeny. These betweenthe typical microperforate/baculate results,like thoseof Nowicke's(1994) studyof structureof manyOldfieldioideae and the ho- the Crotonoideae,emphasize the importance of mogeneoustectum found in Paradrypetes. TEM in palynologicalstudies and underscorethe Androstachys(fig. 45) is exceptionalin theOld- need formore extensive use of thistechnique in fieldioideaein havinga tectate-columellateexine studiesof theEuphorbiaceae. architecture,as in all investigatedPhyllanthoi- deae. Our cladisticanalysis of palynological and Acknowledgments otherdata (Levin and Simpson1994a) showed We thankthe staffsat DAV, GH, K, MO, P, thatAndrostachys, rather than being a member RSA/POM, QRS, U, and US forremoving or ofthe Phyllanthoideae, is nested within the Old- allowingus to removepollen from collections in SIMPSON & LEVIN-EUPHORBIACEAE POLLEN 341 theircare; Grady Webster for loaning us unpub- ickeand an anonymousreviewer for helpful com- lishedSEM photographs;Steve Barlow and Lisa mentson themanuscript. This research was sup- Bairdfor help with SEM; and JonBlevitt, Nicki portedin partby a San Diego StateUniversity Watson,Marcelle Benzel, Scott McMillan, and FoundationGrant-in-aid Award to Michael G. KittyHuntley for help in TEM sectioningand Simpson. photographicprinting. We also thankJoan Now-

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